Sanitation and Disease Health Aspects of Excreta and Wastewater Management Richard G. Feachem David J. Bradley Hemda Garelick * D. Duncan Mara FILE COPY r u t- Report No.:11616 Type: (PUB) _ i -.- Title: SANITATION AND DISEASE: HEALTH _ Author: FEACHEM, PICHARD Ext.: 0 Roonl: Dept.: BOOKSTORE 1983 -U ) | i 6 ~ILE COPY V~~~~~~~~~~ X - UL A Wod E. Stu \ W World Bank Studies in Water Supply and Sanitationl 3 Sanitation and Disease WORLD BANK STUDIES IN WATER SUPPLY AND SANITATION 3 Sanitation and Disease Health Aspects of Excreta and Wastewater Management Richard G. Feachem, David J. Bradley, Hemda Garelick and D. Duncan Mara with contributions from J. Coghlan, C. F. Curtis, D. M. E. Curtis W. A. M. Cutting, B. S. Drasar, B. Lloyd W. W. MacDonald, D. M. Mackay, R. L. Muller, J. S. Slade B. A. Southgate, D. C. Warhurst and A. J. Zuckerman Publishedfor the World Bank by John Wiley & Sons Chichester New York Brisbane Toronto Singapore Copyright 'll 1983 by The International Bank for Reconstruction and Development / THE WORLD BANK, 1818 H Street, N.W., Washington, D.C. 20433, U.S.A. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, or other- wise, without the written permission of the World Bank. The views and interpretations in this book are the authors' and should not be attributed to the World Bank, to its affiliated organizations, or to any individual acting on their behalf. Printed and bound in Great Britain at The Pitman Press. Bath Contents Tables and Figures xix 2. Environmental Preface xxiii Classification of Excreta- Scope and Organization related Infections 23 Origins and Related Publications Understanding Exereta- Contributors related Infections 23 Acknowledgments Excreted load 24 Acronyms and Abbreviations xxvii Latency 24 Persistence 25 Multiplication 25 Infective dose 25 PART ONE. THE HEALTH Host response 26 HAZARDS OF EXCRETA: Nonhuman hosts 31 THEORY AND CONTROL Categories of Excreta-related Infections 32 Category I 37 1. Elements and Health Category II 37 Risks of Excreta and Category III 38 Wastewater 3 Category Iv 39 Category v 39 Excreta and Health 3 Category VI 39 Characteristics of Excreta and Summary 39 Sewage 4 Literature Cited 40 Quantities 4 Chemical composition 6 Pathogens in exereta 9 3. The Risks of Excreta to Viruses in excreta 9 Bacteria in excreta 9 Protozoa in excreta 12 Illustrative Sketches 43 Helminths in excreta 12 A Southeast Asian family 43 Magnitude of pathogen A North African family 44 excretion 16 Children and Exereta A note on urinary pathogens 16 Disposal 46 Characteristics of Sullage 16 Distribution of Sanitation Quantities 16 Benefits 47 Composition 18 Health Benefits of Sullage disposal and health 20 Sanitation 48 Literature Cited 20 Methodological issues 48 vi CONTENTS The literature 48 5. Health Aspects of Limitations in Assessing Health Excreta and Night Soil Benefits 49 Best inferences in an optimal case 49 PitLatrines 67 Best inferences in Cleanliness 67 actuality 50 Odor 67 Literature Cited 50 Insect breeding 67 Pathogen survival in the 4. Detection, Survival, and pit 68 Removal of Pathogens in Groundwater pollution 68 Composting Toilets 68 the Environment 53 Technical description 68 Fecal Indicator Bacteria 53 Pathogen survival in Coliform bacteria 54 product 71 Fecal streptococci 54 Cartage Systems 74 Fecal coliform to fecal Night soil deposition 75 streptococci ratio 55 Night soil collection 77 Clostridium perfringens 55 Night soil transport 77 Pseudomonas aeruginosa 55 Night soil treatment 77 Bifidobacterium and other Night soil reuse 77 anaerobic bacteria 56 Composting 78 Fecal concentrations, Pathogen survival 78 detection, and Fly breeding 80 enumeration of bacterial Literature Cited 80 indicators 56 Relation of Fecal Indicator 6. Health Aspects of Bacteria to Excreted Pathogens 56 Sewage Systems 83 Pathogen Indicators 57 A quaprivies and Septic Pathogen indicators for pond Tanks 83 effluents 58 Technical description 83 Pathogen indicators for Pathogen survival 83 effluents from other Conventional Sewage sewage treatment Treatment 86 processes 58 Pretreatment and primary Pathogen indicators for sedimentation 86 noneffluents 58 Trickling filters 87 Survival of Indicators and Activated sludge 88 Pathogens 59 Sludge digestion 88 In feces, night soil, and Sludge dewatering 89 sludge 60 Other sludge treatment In water and sewage 60 processes 89 In soil 61 Complete treatment On crops 61 works 90 Pathogen Survival versus AeratedLagoons 92 Removal in Waste Technical description 92 Treatment 62 Pathogen survival 93 Objectives of Night Soil and Oxidation Ditches 93 Sewage Treatment 62 Technical description 93 Excreta and night soil Pathogen survival 94 treatment 63 Tertiary Treatment 94 Sewage treatment 63 Rapid sand filtration 94 Literature Cited 64 Slow sand filtration 94 CONTENTS vii Land treatment 94 Reuse for Biogas Maturation lagoons 94 Production 107 Other tertiary treatment Technical description 107 processes 95 Pathogen control in reuse of Effluent Chlorination 95 biogas plant slurry 107 Waste Stabilization Discharge of Effluents 109 Ponds 96 Into rivers and lakes 109 Technical description 96 Health issues 109 Pathogen survival 96 Waterborne Literature Cited 96 pathogens 109 Helminths with aquatic 7. Reuse of Excreta and intermediate Discharge of hosts 109 Effluents 99 Into the sea 110 Health issues 110 Reuse in Agriculture 99 Pathogen survival 110 Foodstuffs for human Seafood consumption 99 contamination 110 Health issues 99 Recreational hazards 111 Pathogens reaching the To groundwater 111 field 100 Health issues 111 Pathogen survival 100 Pathogen travel 112 Pathogen Pathogen survival 112 transmission 100 Pathogen control 112 Foodstuffs for animal Nitrates from effluents 112 consumption 101 Health issues 112 Health issues 101 Nitrate control 113 Beef tapeworm Literature Cited 113 infection 101 Salmonellosis 101 8. The Human Element in Tuberculosis 101 SanTation Ssems i1 Other agricultural Sanitation Systems 117 products 102 Relevance of Cultural Values Occupational hazards 102 and Attitudes 118 Pathogen control in Influence of Social Structure agricultural reuse 103 and Organization 119 Reuse in Aquaculture 104 Social and Behavioral Aspects Fish farmning 104 ofLatrine Design 119 Health issues 104 Cost 119 Passive transference of Convenience 119 excreted pathogens 104 Comfort 120 Helminths havingfish as Group or communal intermediate toilets 121 hosts 105 Social and Organizational Helminths with other aquatic Aspects of Exereta intermediate Cartage Systems 121 hosts 105 Social and Organizational Pathogen control 105 Aspects of Exereta Algal culture 105 Reuse Systems 123 Health issues 106 Improving the Management of Pathogen control 106 Urban Sanitation Macrophyte culture 106 Systems 124 Health issues 106 Effectiveness andLimitations Pathogen control 106 of Self-help Schemes 125 'lii CONTENTS Appropriate Health By waste stabilization Education 126 ponds 154 Literature Cited 126 By aerated lagoons 155 By tertiary treatment 155 Lagooning 155 PART TWO. ENVIRONMENTAL Cocigulation 155 BIOLOGY AN1D F 155 EPIDEMIOLOGY OF SPECIFIC DisiyiJection 156 Lanzd treatinent 158 EXCRETED PATHOGENS Otheer processes 16(0 Inactivation by Night Soil and SECTION I. EXCRETED VIRUSES Sludge Treatment Processes 160 9. Enteroviruses, Poliomyelitis, By pit latrines 160 and Similar Viral By anaerobic digestion 160 Infections 133 By drying 161 Description of Pathogens and By heating 162 Diseases 133 By composting 163 Identification 133 By other processes 164 Occurrence 135 Literature Cited 164 Infectious agents 135 Reservoir 135 10. Hepatitis A Virus and Transmission 135 Infectious Hepatitis 173 Incubation period 136 Description of Pathogen and Period of Disease 173 communicability 136 Identification 173 Resistance 137 Occurrence 1 73 Epidemiology 137 Infectious agent 174 Control Measures 137 Reservoirs 174 Individual 137 Transmission 174 Environmental 137 Incubation period 174 Occurrence and Survival in the Period of Environment 138 communicability 174 In surface waters 139 Resistance 174 In ground water 140 Epidemiology 1 74 In drinking water 140 Control Measures 175 In seawater 141 Occurrence and Survival in In feces and night soil 143 the Environment 176 In sewage 144 Inactivation by Sewage In sludge 145 Treatment Processes 177 In soil 146 Inactivation by Night Soil and On crops 147 Sludge Treatment In fish and shellfish 148 Processes 1 77 In the air 150 Literature Cited 178 Inactivation by Sewage Treatment Processes 151 11. Rotavirus and Viral By primary and secondary Gastroenteritis 181 sedimentation 151 By storage 151 Description of Pathogens and By septic tanks 152 Diseases 181 By trickling filters 152 Identification 181 By activated sludge 153 Occurrence 181 By oxidation ditch 154 Infectious agents 181 CONTENTS ix Rotaviruses 182 13. Pathogenic and Adenoviruses 182 Nonpathogenic Astroviruses 182 * * a Calicivirutses 182 Coronavirruses 182 Other Bacterial Enteroviruses 184 Indicators of Fecal Measles viirus 184 Pollution 199 Ani ail ageot and other Description of Pathogen and smiiall r-ouind Disease 199 vliruises 184 Identification 199 Reservoirs 184 Occurrence 199 Transmission 184 Ocrec 9 Incubation period 184 Infectious agents 199 Period fr Enterotoxigenic E. coli Perio mmunicabil y 1 4 (ETEC) 200 communicability 184 Enteroinvasive E. coli Resistance 185 (EIEC) 200 Epidemiology 185 Enteropathogenic E. coli Control Measures 186 (EPEC) 200 Occurrence and Survival in the Reservoirs 201 Environment 187 Transmission 201 Inactivation by Sewage Tration 201 Treatment Processes 188 Icbion p d Inactivation by Night Soil and Period of Sludge Treatment ~~~~~~~~~~~~~~communicability 201 Sludge Treatment Processes 188 Resistance 201 T raue Cie 188 Epidemiology 201 Control Measures 205 SECTION 11. EXCRETED Individual 205 BACTERIA Environmental 205 Fecal Indicator Bacteria 12. Campylobacter and Occurrence and Survival in Campylobacter the Environment 206 Enteritis In surface waters 206 In groundwater 209 Description of Pathogen and In drinking water 210 Disease 193 In seawater 212 Identification 193 In feces and night soil 213 Occurrence 193 In sewage 214 Infectious agent 193 In sludge 215 Reservoirs 195 In soil 215 Transmission 195 On crops 216 Incubation period 196 In fish and shellfish 217 Period of communicability 196 In the air 218 Resistance 196 Inactivation by Sewage Epidemiology 196 Treatment Processes 221 Control Measures 197 By primary and secondary Occurrence and Survival in the sedimentation 221 Environment 197 By storage 222 Inactivation by Sewage By septic tanks 222 Treatment Processes 197 By trickling filters 223 Inactivation by Night Soil and By activated sludge 224 Sludge Treatment By oxidation ditch 224 Processes 197 By waste stabilization Literature Cited 197 ponds 224 x CONTENTS Mechanisms of E. coli 15. Salmonella, Enteric removal in ponds 224 Fevers, and Kinetics of E. coli remnoval SalmonelloseS 251 in ponds 225 By aerated lagoons 226 Description of Pathogens and By tertiary treatment 228 Diseases 251 Lagooning 228 Identification 251 Coagtilation 228 Occurrence 251 Filtration 228 Infectious agents 252 Disinfection 229 Reservoirs 252 Land treatment 230 Transmission 253 Other processes 231 Incubation period 254 Inactivation by Night Soil and Period of Sludge Treatment communicability 255 Processes 231 Resistance 255 By pit latrines 231 Epidemiology 256 By anaerobic digestion 231 Control Measures 259 By heating 232 Individual 259 By composting 232 Carrier surveillance and By limne treatment 233 control 259 By other processes 233 Environmental 260 Literature Cited 233 Occurrence and Survival in the Environment 261 14. Leptospira and In surface water 261 In groundwater 263 Leptospirosis 243 In drinking water 266 Description of Pathogen and In seawater 266 Disease 243 In feces and night soil 267 Identification 243 In sewage 267 Occurrence 243 In sludge and slurry 268 Infectious agent 243 In soil 269 Reservoirs 244 On pasture 270 Transmission 244 On crops 271 Incubation period 244 In fish and shellfish 271 Period of In the air 272 communicability 245 Inactivation by Sewage Resistance 245 Treatment Processes 273 Epidemiology 245 By primary and secondary Control Measures 246 sedimentation 273 Individual 246 By septic tanks 273 Environmental 247 By conventional Occurrence and Survival in the treatment 273 Environment 247 By oxidation ditch 274 In water and sewage 247 By waste stabilization In urine 247 ponds 275 In feces and night soil 248 By tertiary treatment 275 In soil 248 Lagooning 275 Inactivation by Sewage Disinfection 275 Treatment Processes 248 Land treatment 276 Inactivation by Night Soil and Inactivation by Night Soil and Sludge Treatment Sludge Treatment Processes 248 Processes 276 Literature Cited 249 By pit latrines 276 CONTENTS xl Transmission 300 By storagerobicdigesti 276 Incubation period 300 By aerobic digestion 277 Period of By aerobic digestion 277 communicability 300 By drying 277 Resistance 300 By composting 278 Epidemiology 301 By composting 278 ~~Control Measures 301 By coagulation and vacuum Indvul .30 filtration 278 Environmental 302 By lime treatment 278EviomDa 30 By limertreatment 278 Carrier surveillance and By irradiation 278 international regulations 303 16. Shigella and Occurrence and Survival in the Environment 303 SlhigellOSiS 287 In water 303 Description of Pathogen and In feces and night soil 307 Disease 287 In sewage 309 Identification 287 Summary of survival in water Occurrence 287 and wastewater 309 Infectious agent 287 Prolonged survival in water Reservoir 288 and wastewater 313 Transmission 288 A possible aquatic reservoir Incubation period 288 for V. cholerae 315 Period of In sweat 316 communicability 288 On surfaces 316 Resistance 288 In soil 317 Epidemiology 288 On food and crops 317 Control Measures 290 Inactivation by Sewage Individual 290 Treatment Processes 317 Environmental 290 Inactivation by Night Soil and Occurrence and Survival in the Sludge Treatment Environment 291 Processes 322 In water 292 Literature Cited 322 In feces and sewage 292 On surfaces 292 18. Yersinia and In food 293 Yersiniosis 327 On crops 293 In thc air 293 Description of Pathogen and Inactiviation by Sewage Disease 327 I,activiation by Sewage Identification 327 Treatment Processes 293 Occurrence 327 Inactivation by Night Soil and Infectious agent 327 Sludge Treatment Reservoirs 328 Processes 293 Transmission 328 Literature Cited 294 Incubation period 328 17. Vibrio cholerae and Period of communicability 328 Cholera 297 Resistance 328 Description of Pathogens and Epidemiology 328 Disease 297 Control Measures 329 Identification 297 Occurrence and Survival in the Occurrence 298 Environment 329 Infectious agents 299 Inactivation by Sewage Reservoir 300 Treatment Processes 330 xii CONTENTS Inactivation by Night Soil and Environmental 340 Sludge Treatment Occurrence and Survival in the Processes 330 Environment 342 Literature Cited 330 In water and water supplies 342 SECTION III. EXCRETED In seawater 342 PROTOZOA In feces and night soil 342 19. Balantidium and In sewage 342 On surfaces 342 BalantidiasiS 333 In soil 342 Description of Pathogen and On crops 342 Disease 333 Summary 343 Identification 333 Inactivation by Sewage Occurrence 333 Treatment Processes 343 Infectious agents 333 By sedimentation 343 Reservoirs 334 By trickling filter 344 Transmission 334 By activated sludge 344 Prepatent and incubation By oxidation ditch 344 periods 334 By waste stabilization Period of ponds 344 communicability 334 By aerated lagoons 344 Resistance 334 By tertiary treatment 344 Epidemiology 335 IH'u.'. 344 Control Measures 335 Disintftction 344 Individual 335 Land treatmnent 344 Environmental 335 Inactivation by Night Soil and Occurrence and Survival in the Sludge Treatment Environment 335 Processes 344 Inactivation by Sewage Literature Cited 345 Treatment Processes 336 Inactivation by Night Soil and 21. Giardia and Sludge Treatment Giardiasis 349 Processes 336 Description of Pathogen and Literature Cited 336 Disease 349 20. Entamoeba histolytica Identification 349 Occurrence 349 and Amebiasis 337 Infectious agent 349 Description of Pathogen and Reservoirs 350 Disease 337 Transmission 350 Identification 337 Prepatent and incubation Occurrence 337 periods 351 Infectious agent 337 Period of Reservoirs 338 communicability 351 Transmission 338 Resistance 351 Prepatent and incubation Epidemiology 351 periods 338 Control Measures 352 Period of Individual 352 communicability 338 Environmental 352 Resistance 339 Occurrence and Survival in the Epidemiology 339 Environment 352 Control Measures 340 In water and water Individual 340 supplies 353 CONTENTS Xiii In feces and night soil 353 By drying 370 In sewage 353 By heating 370 Summary 353 By composting 370 Inactivation by Sewage Literature Cited 371 Treatment Processes 354 Inactivation by Night Soil and 23. Ascaris and Sludge Treatment Processes 354 Ascariasis 375 Literature Cited 354 Description of Pathogen and Disease 375 SECTION IV. EXCRETED Identification 375 HELMINTHS Occurrence 375 22. Ancylostoma, Necator, Infectious agent 375 Reservoir 376 and Ancylostomiasis 359 Transmission 376 Description of Pathogen and Prepatent and incubation Disease 359 periods 377 Identification 359 Period of Occurrence 359 communicability 377 Infectious agents 361 Resistance 377 Reservoir 361 Epidemiology 377 Transmission 361 Control Measures 380 Prepatent and incubation Individual 380 periods 362 Environmental 380 Period of Occurrence and Survival in the communicability 362 Environment 384 Resistance 362 In surface water 384 Epidemiology 362 In groundwater 385 Control Measures 364 In drinking water 385 Individual 364 In seawater 385 Environmental 365 In feces and night soil 385 Occurrence and Survival in the In sewage 385 Environment 366 In sludge 385 In water 366 In soil 386 In feces and night soil 367 On crops 386 In sewage 367 Inactivation by Sewage In sludge 367 Treatment Processes 387 In soil 367 By septic tanks 387 On crops 367 By conventional Inactivation by Sewage treatment 388 Treatment Processes 368 By waste stabilization By septic tanks 368 ponds 388 By conventional By tertiary treatment 389 treatment 368 Inactivation by Night Soil and By waste stabilization Sludge Treatment ponds 368 Processes 389 By tertiary treatment 369 By pit latrines 389 Inactivation by Night Soil and By biogas plants 389 Sludge Treatment By digestion 390 Processes 369 By storage 390 By digestion 369 By drying 391 By ovicides and By heating 391 larvicides 369 By composting 392 xiv CONTENTS By other processes 392 Inactivation by Night Soil and ., ~~~~~~~~Sludge Treatment Chemical ovicides 392 Plocesseat410 Irradiation 392 Literature Cited 410 Literature Cited 393 24. Clonorc his and 26. Enterobius and Enterobiasis 413 Clonorchiasis 401 Description of Pathogen and Description of Pathogen and Disease 413 Disease 401 Identification 413 Identification 401 Occurrence 413 Occurrence 401 Infectious agent 413 Infectious agents 401 Reservoir 413 Reservoirs 401 Transmission 413 Transmission 401 Prepatent and incubation Prepatent and incubation periods 413 periods 402 Period of Period of communicability 414 communicability 402 Resistance 414 Resistance 403 Epidemiology 414 Epidemiology 403 Control Measures 415 Control Measures 404 Occurrence and Survival in the Occurrence and Survival in the Environment 415 Environment 404 Inactivation by Sewage Inactivaction by Sewage Treatment Processes 415 Treatment Processes 404 Inactivation by Night Soil and Inactivation by Night Soil and Sludge Treatment Sludge Treatment Processes 416 Processes 404 Literature Cited 416 Literature Cited 404 27. Fasciola and 25. Diphyllobothrium and Fascioliasis 417 Diphyllobothriasis 407 Description of Pathogen and Description of Pathogen and Disease 417 Disease 407 Identification 417 Identification 407 Occurrence 417 Occurrence 407 Infectious agent 417 Infectious agent 407 Reservoirs 417 Reservoir 407 Transmission 417 Transmission 407 Prepatent and incubation Prepatent and incubation periods 418 periods 409 Epidemiology 418 Period of Control Measures 418 communicability 409 Occurrence and Survival in the Resistance 409 Environment 418 Epidemiology 409 Inactivation by Sewage Control Measures 409 Treatment Processes 419 Occurrence and Survival in the Inactivation by Night Soil and Environment 409 Sludge Treatment Inactivation by Sewage Processes 419 Treatment Processes 410 Literature Cited 419 CONTENTS xv 28. Fasciolopsis and 30. Minor Intestinal Flukes Fasciolopsiasis 421 and Infections They Description of Pathogen and Cause 431 Disease 421 Identification 421 Description of Pathogens and Occurrence 421 Diseases 431 Ifctusente 421 Identification 431 Infectsous agent421 Occurrence 431 Transmission 421 Infectious agents 431 Transmission 421 Reservoirs 431 Prepatent and incubation Transmission 431 periods 421 Period of Prepatent and incubation communicability 422 periods 434 Resistance 422 Period of Epidemiology 422 communicability 434 Control Measures 423 Resistanc 434 Occurrence and Survival in the Epidemology 434 Control Measures 435 Environment 423 Occurrence and Survival in the Inactivation by Sewage Environment 435 Treatment Processes 424 Inactivation by Night Soil and Inactivation by Sewage ,. ~~~~~~~~~Treatment Processes 435 Sludge Treatment Inactivation by Night Soil and Processes 424 Literature Cited 424 Sludge Treatment Processes 435 Literature Cited 435 29. Hymenolepis and 31. Paragonimus and Hymenolepiasis 425 Paragonimiasis 437 Description of Pathogen and Description of Pathogen and Disease 425 Disease 437 Identification 425 Identification 437 Occurrence 425 Occurrence 437 Infectious agent 425 Infectious agent 437 Reservoirs 425 Reservoir 437 Transmission 425 Transmission 437 Prepatent and incubation Prepatent and incubation periods 427 periods 439 Period of Period of communicability 427 communicability 439 Resistance 427 Resistance 439 Epidemiology 427 Epidemiology 439 Control iVMeasures 427 Control Measures 439 Occurrence and Survival in the Occurrence and Survival in the Environment 427 Environment 440 Inactivation by Sewage Inactivation by Sewage Treatment Processes 427 Treatment Processes 440 Inactivation by Night Soil and Inactivation by Night Soil and Sludge Treatment Sludge Treatment Processes 428 Processes 440 Literature Cited 428 Literature Cited 440 xci CONTENTS 32. Schistosoma and Inactivation by Night Soil and Schistosomiasis 443 Sludge Treatment Description of Pathogen and Pirocesses 460 Disease 443 ~~~~~Literature Cited 460 Disease 443 Identification 443 34. Taenia, Taeniasis, and Occurrence 444 Infectious agents 444 Cysticercosis 463 Reservoirs 444 Description of Pathogen and Transmission 444 Disease 463 Prepatent and incubation Identification 463 periods 447 Occurrence 463 Period of Infectious agent 463 communicability 447 Reservoirs 465 Resistance 447 Transmission 465 Epidemiology 447 Prepatent and incubation Control Measures 449 periods 465 Individual 449 Period of Environmental 449 coniinunicability 465 Occurrence and Survival in the Resistance 465 Environment 451 Epidemiology 467 In water 451 Control Measures 468 In feces and night soil 451 Individual 468 In urine 451 Environmental 468 In sewage 451 Occurrence and Survival in the Inactivation by Sewage Environment 468 Treatment Processes 452 In water 468 Inactivation by Night Soil and In sewage 468 Sludge Treatment In sludge 469 Processes 452 On pasture 469 Literature Cited 453 Inactivation bJ' Sewage Treatment Processes 469 33. Strongyloides and Inactivation by Night Soil and Strongyloidiasis 457 Sludge Treatment Processes 470 Description of Pathogen and L itrueCied 470 Disease 45 7 ~~~~~Literature Cited 470 Disease 457 Identification 457 35. Trichuris and Occurrence 457 Infectious agent 457 Trichuriasis 473 Reservoirs 457 Description of Pathogen and Transmission 457 Disease 473 Prepatent and incubation Identification 473 periods 458 Occurrence 473 Period of Infectious agent 473 communicability 458 Reservoir 473 Resistance 459 Transmission 473 Epidemiology 459 Prepatent and incubation Control Measures 459 periods 474 Occurrence and Survival in the Period of Environment 460 communicability 474 Inactivation by Sewage Resistance 474 Treatment Processes 460 Epidemiology 474 CONTENTS x)ii Control Measures 475 The Association of Culex Individual 475 pipiens with Polluted Environmental 475 Water 485 Occurrence and Survival in the Culex pipiens Breeding in Environment 476 Waste Stabilization In water 476 Ponds 487 In feces and night soil 476 Methods for Culex pipiens In sewage 476 Control 488 In sludge 476 Case studies in control 488 In soil 476 Control by modifying the On crops 476 physical Inactivation by Sewage environment 489 Treatment Processes 477 Control by insecticides and Inactivation by Night Soil and oils 490 Sludge Treatment Conclusions 492 Processes 477 Literature Cited 492 Literature Cited 478 37. Flies, Cockroaches, and Excreta 495 SECTION v. INSECTS AND Flies Associated with Waste EXCRETA Disposal 495 Cockroaches 496 36. Culex pipiens Flies, Cockroaches, and Mosquitoes and the Health 496 Transmission of Transmission of Excreted Bancroftian Pathogens 497 Methods of Fly and Cockroach Filariasis 483 Control 498 The Biology of Culex pipiens Modifying the physical Mosquitoes 483 environment 498 Bancroftian Filariasis 483 Insecticides and other Culex pipiens as a Vector and chemicals 499 as a Nuisance 484 Literature Cited 499 Tables and Figures Tables 3-2. Ranking of excreta disposal technologies by 1-1. Fecal weights around the world 5 ease of operation and maintenance, water 1-2. Composition of human feces and urine 6 needs, and health benefits 51 1-3. Possible standard biochemical oxygen 4-1. Number of indicator bacteria commonly demand (BoD5) content of exereta and night found in human feces 56 soil 7 4-2. Survival times of excreted pathogens in feces, 1-4. BOD5 contributions per capita in urban night soil, and sludge at 20-30°C 60 sewage 8 4-3. Survival times of excreted pathogens in fresh 1-5. Viral pathogens excreted in feces 9 water and sewage at 20-30°C 60 1-6. Bacterial microflora of human feces by 4-4. Factors affecting survival time of enteric national diet 11 bacteria in soil 61 1-7. Bacterial pathogens excreted in feces 12 4-5. Survival times of excreted pathogens in soil 1-8. Protozoal pathogens excreted in feces 13 at 20-30°C 61 1-9. Helminthic pathogens excreted in feces 14 4-6. Survival times of excreted pathogens on 1-10. Possible output of selected pathogens in the crops at 20-30°C 62 feces and sewage of a tropical community of 5-1. Probable pathogen content in final product 50,000 in a developing country 17 of anaerobic composting toilets operating at 1-11. Allocation of water use in sewerless rural ambient temperatures in warm households in developing countries 18 climates 74 1-12. Pollution loads of wastewater sampled from 6-1. Theoretical settling velocities of protozoal various plumbing fixtures in the USA 19 cysts and helminth eggs 87 1-13. Bacterial content of sullage in the USA 19 9-1. Human excreted viruses 134 2-1. Summary of selected literature on the effect 12-1. Prevalence of excretion of Campylobacter on health of improved excreta disposal 26 and other enteric pathogens by individuals 2-2. Environmental classification of excreted with and without diarrhea in twelve infections 33 countries 194 2-3. Basic epidemiological features of excreted 13-1. Etiology of diarrhea reported to Matlab pathogens by environmental category 34 Hospital, Bangladesh, during 1977 202 2-4. Category I and ii pathogens (from table 2-2) 13-2. Some reported concentrations of fecal ranked by median infective dose (ID50) 36 bacteria in untreated domestic water sources 2-5. Category I and ii pathogens (from table 2-2) in developing countries 208 ranked by persistence outside host 36 13-3. Fecal bacteria removal rate constants in 2-6. ID50 and persistence of category I and II series of waste stabilization ponds 227 pathogens (from table 2-2) commonly and 15-1. Variations in the nomenclature of some rarely transmitted in affluent European important types of Salmonella 252 communities 36 15-2. Period and point prevalences of Salmnonella 3-1. Maximum prevalence of excreted pathogens and Shigella excretion by black school- (from table 2-2) by age in indigenous children in the Transvaal, Republic of South populations of endemic areas 46 Africa 264 xix xx TABLES AND FIGURES 15-3. Salmonella removal at the Woking trickling 2-2. Factors affecting the transmission of an filter plant, UK 274 infective dose 24 15-4. Saimoniella removal at the Guildford 2-3. Involvement of other vertebrates in activated sludge plant, UK 274 transmission of human excreted 17-1. Survival of Vibrio cholerae in surface infections 32 waters 304 2-4. Persistence outside the host of excreted 17-2. Survival of V cholerae in well water 306 pathogens (categories I-v from table 2-2) 17-3. Survival of V cholerae in tap water 308 over time 37 17-4. Survival of V chlolerae in mineral 2-5. Length and dispersion of transmission cycles water 309 of excreted infections (categories i-V from 17-5. Survival of 1' cholerae in seawater 310 table 2-2) 38 17-6. Survival of V cholerae in feces 311 5-1. Conventional unimproved pit latrine 68 17-7. Survival of V cholerae in sewage 312 5-2. Ventilated improved pit (VIP) latrine 69 17-8. rg9 values in hours for various types of V 5-3. Reed Odorless Earth Closet (ROEC) 70 chlolerae in various waters and 5-4. "Multrum" continuous-composting wastewaters 314 toilet 71 17-9. Survival of V chlolerace on surfaces 316 5-5. Double-vault composting (DVC) 17-10. Survival of V cholerae on food and toilets 72 crops 318 5-6. Pathogen flow through a batch composting 20-1. Some studies on the relationships between toilet (double-vault) 74 Entamioeba histolvtica infection and 5-7. Bucket latrine and cartage 75 environmental sanitation 341 5-8. Alternative designs for vault toilets 76 22-1. Prevalence of hookworm infection in fifteen 5-9. Influence of time and temperature on countries 363 selected pathogens in night soil and 22-2. Some studies on the effect of mass sludge 79 chemotherapy on hookworm 5-10. Pathogen flow through a well-managed infection 365 thermophilic composting process 80 22-3. Some studies on environmental influences on 6-1. Septic tank designs 84 hookworm infection 366 6-2. Conventional aquaprivy 85 2'-4. Reduction of helminth eggs by sewage 6-3. Pathogen flow through a septic tank 86 treatment processes in India 369 6-4. Components of conventional sewage 92-5. Tolerance of hookworm eggs and larvae to treatment 87 high and low temperatures 371 6-5. Pathogen flow through various continuous 23-1. Some studies on the reduction and sludge treatment processes 89 subsequent rise of ascariasis prevalence 6-6. Pathogen flow through various batch sludge following mass chemotherapy 381 treatment processes 90 23-2. Some studies on environmental influences on 6-7. Pathogen flow through a conventional ascariasis 383 sewage treatment plant featuring trickling 23-3. Some studies on Ascaris eggs in composting filters 91 processes 392 6-8. Pathogen flow through a conventional 23-4. Some literature on Ascar-is ovicides 393 sewage treatment plant featuring activated 29-1. Duration of infectivity of Hy inmenolepis nana sludge 91 eggs stored under various conditions 42N 6-9. Flow diagram for an aerated lagoon 34-1. Some studies on the survival of Taeniia eggs incorporating sludge digestion 92 in grass, silage. and soil 469 6-10. Stages in development of a waste 35-1. Some studies on environmental influences on stabilization pond-aerated lagoon trichuriasis 476 system 93 37-1. Insect fauna of "dry" latrines 497 6-11. Flow diagram for an oxidation ditch 93 6-12. Pathogen flow through a waste stabilization Figures pond system 97 7-1 Tvpical biogas digesters 108 2-1. The links between excreta and 9-1. Polio-, adeno- and reoviruses under infection 23 electronmicroscopy 136 TABLES AND FIGURES xxi 9-2. The influence of time and temperature on 27-1. An adult Fasciola hepatica under a light enteroviruses 163 microscope 418 10-1. Hepatitis A viruses under transmission 28-1. Known geographical distribution of electronmicroscopy 174 Fasciolopsis buski 422 11-1. Agents of viral gastroenteritis 183 28-2. An adult Fasciolopsis buski under a light 12-1. Campylobacter under scanning microscope 423 electronmicroscopy 195 29-1. Head (scolex) and neck of Hymenolepis nana 13-1. Escherichia coli and Streptococcus under under scanning electronmicroscopy 426 scanning electronmicroscopy 200 30-1. Known geographical distributions of 14-1. Leptospira under scanning Heterophyes heterophyes and Metagonimnus electronmicroscopy 244 yokogawai 432 15-1. Salmonella enteritidis under scanning 30-2. Known geographical distribution of electronmicroscopy 252 Gastrodiscoides hominis 432 15-2. The influence of time and temperature on 30-3. Adult Heterophyes heteroplhyes (a) and salmonellae 277 Metagonimus yokogawai (b) under a light 16-1. The influence of time and temperature on microscope 433 Shigella 294 30-4. An adult Gastrodiscoides hominis under a 17-1. The global spread of cholera. 1961-75 298 light microscope 434 17-2. Vibrio cholerae under scanning 31-1. Known geographical distribution of electronmicroscopy 299 Paragonimus 438 17-3. The influence of time and temperature on 1 31-2. An adult Paragonimuis westermani under a cholerae 322 light microscope 438 19-1. Drawing of a trophozoite of Balantidium 32-1. Known geographical distribution of coli 334 Schistosoma haematobium and S. 20-1. A trophozoite of Entamoeba histolytica japonicum 445 under scanning electronmicroscopy 338 32-2. Known geographical distribution of S. 20-2. The influence of time and temperature on mansoni 445 Ent. histolytica cysts 343 32-3. A male and female S. mansoni under 21-1. Trophozoites of Giardia lamblia under scanning electronmicroscopy 446 scanning electronmicroscopy 350 32-4. The influence of time and temperature on 22-1. Known geographical distribution of Schiistosoma eggs 453 Ancylostoma duodenale 360 33-1. An adult Strongyloides stercoralis under a 22-2. Known geographical distribution of Necator light microscope 458 anlericanius 360 34-1. Known geographical distribution of Taenia 22-3. The head (scolex) of an Ancvlostomna under a saginata 464 light microscope 361 34-2. Known geographical distribution of T 22-4. The influence of time and temperature on soliumn 464 hookworm eggs and larvae 370 34-3. T solium and T. saginata 466 23-1. Ascaris in situ 376 34-4. The influence of time and temperature on 23-2. The influence of time and temperature on Taenia eggs 470 Ascaris eggs 391 35-1. A male (left) and female (right) Trichwl7is 24-1. Known geographical distribution of t7ic/ziu7a under a light microscope 474 Clonorchis sinensis 402 36-1. Known geographical distribution of Culex 24-2. An adult of OpisthorchisJelinetis under a pipiens mosquitoes and Bancroftian light microscope 403 filariasis 484 25-1. Known geographical distribution of 36-2. Larval and adult Culex pipiens Diphyllobothrium latum 408 mosquitoes 485 25-2. A length of D. latunm expelled after 36-3. Insect traps for pit latrines 491 treatment 408 37-1. The common housefly, Musca 26-1. Adult pinworms, Enrteobius comnestic a 496 ve1 nriclularis 414 Preface MANY IMPORTANT infectious diseases are associated disposal systems. To achieve this gain as much with human excreta. The most common association is information as possible is needed about the interactions that the pathogens causing the disease leave an infected between excreta and health-information not only person by way of the feces orurine. Excreta are thus the about broad epidemiological issues of disease pre- direct source of these infections. Less commonly and vention through improved excreta disposal, but also directly, excreta may be associated with the breeding of about the effect of particular excreta disposal and reuse insects that are vectors of disease. The hygienic technologies on the survival and dissemination of management and disposal of human excreta is thus of particular pathogens. central importance in the control of these associated diseases. This is true in both poor and rich countries and across all climatic zones. Most people in the developing countries do not have adequate disposal systems for human wastes. A survey Scope and Organization of developing countries by the World Health Organization (WHO) in 1975 indicated that 75 percent This book sets out to provide such information for a of urban dwellers did not have sewerage (that is, sewers broad readership. It is intended for the wide spectrum for disposal of excreta) and that 25 percent had no of professionals concerned with sanitation and public disposal system of any kind. In rural areas, 85 percent health: those who control -such as health planners, lacked any adequate excreta disposal facility. Major economists, and public health administrators; those national and international initiatives are clearly who implement-such as environmental hygienists, required if any substantial improvement in sanitation sanitary engineers, public health workers, and health systems in the developing world is to be made in the educators; and those who study and advise- next few decades. especially epidemiologists, microbiologists, and para- In the more wealthy and industrialized countries, sitologists. The book has been written with a minimum most people have adequate excreta disposal arrange- of technical jargon so that it can be readily absorbed by ments in their homes and places of work. The people from different professional backgrounds; treatment and disposal of human wastes, however, technical terms are defined when they are used, and pose enormous problems for the responsible agencies. acronyms and abbreviations are listed on page 22. Large cities produce such volumes of sewage and such The book has two parts. Part One, entitled "The quantities of sludge that the infrastructure for the safe Health Hazards of Excreta: Theory and Control," disposal of these wastes may be stretched to the limit. It presents a distillation of available knowledge about is in this context that decisions about pathogen excreta, night soil, and sewage and their effects on destruction in sewage and sludge and about the risks to health. The emphasis is on presenting the complex, public health of various treatment and disposal and sometimes contradictory, evidence as clearly and options become of the utmost importance. concisely as possible. The source for Part One is In all countries, public health is of central largely, but not entirely, the literature. On occasion, we importance in the design and implementation of have gone beyond the literature to state what we excreta disposal projects, and better health is the main anticipate to be the case; this theoretical content is social and economic benefit that planners and based on a fundamental understanding of the economists hope to gain by investing in excreta particular disease or pathogen. Inevitably, the need for xxiii xxitv PREFACE clarity and the demands of limited space have Appropriate Sanitation Alternlatives: A Planninzg and necessitated some oversimplification. Design Manual (by J. M. Kalbermatten, D. S. Julius, C. Part Two, entitled "Environmental Biology and G. Gunnerson, and D. D. Mara). In addition, the Epidemiology of Specific Excreted Pathogens," con- Transportation and Water Department of the World tains twenty eight chapters, each describing the Bank issues a series of reports under the main environmental properties of a specific excreted title Appropriate T1 .1m. ; jor Water Supply and pathogen or group of excreted pathogens and the Sanitation-available from the Bank's Publication epidemiology and control of the infections these Unit (for information on obtaining these and related pathogens cause. Emphasis is placed on the occurrence World Bank publications, see the last page of this and survival of the pathogen in the environment and on book). Twelve reports have been published in this the efficacy of various waste treatment processes in series so far. reducing or eliminating the pathogen. For ease of reference. the chapters of Part Two are grouped by biological class of pathogen in five sections-the excreted viruses, bacteria, protozoa, and helminths, Contributors and the excreta-related insect vectors of disease. As in Part One, the material in Part Two is derived from the The book has been pepared by the Ross Institute of literature. Where documentation is ambiguous or Tropical Hygiene from the work of a group of contradictory, we have attempted to give a conser- bacteriologists, engineers, entomologists, epidemio- vative opinion-overestimating, for example, the logists, parasitologists, and virologists from the ability of a pathogen to survive hostile environmental London School of Hygiene and Tropical Medicine and conditions. elsewhere. Contributing specialists, their affiliations, Each chapter in Parts One and Two has its own list and the chapters to which they contributed are: of literature cited. The several hundred papers and publications cited were selected from among a total ('i collection of several thousand items assembled during Dr. J. Coghlan 14 the writing of this book. The literature searches for the Lepto-spirosis Reference Laboratory, London various chapters were ended between late 1980 and mid- 1981. The literature throughout has been selected from Ross C. .titute of Trop3cai H6oienc, London Shool 3 international sources (a considerable number of Czech. of H,giene and Tropcal Medicine French, German. Japanese. Korean, Russian, Spanish. and other non-English language publications have been Dr. D. M. E. Curtis 8 used). i ustit ite of Local Gov erenent Studtes. tUnirersit!y of Despite its division into two parts, the book is meant Bir;ninghaoi to be used as a unit. Readers desiring elaboration or Dr. W. A. M. Cutting I support of statements made in Part One must refer to Department of Child Lije and Health, Uini.er.itt of Part Two. Edinburgh IjormerlyH of Ross Institute. Lon'don Schzool of Hygiene and Tropical Medicinel Dr. B. S. Drasar 12. 13. 16 Origins and Related Publications Deparnment of V'edical Microbiology, Lonidon Scthool of Higiene and 7ropical Medicine This book arises out of a World Bank research Dr. B. Llovd ]5. 17. 18 project in appropriate technology for waste disposal D o . t 3 ~~~~~~~~~~~~~~~~Department of Mvticobiology, Uniersitr of Sarrse; that was initiated in 1976 by the Bank's chief water and wastes adviser. Mr. John M. Kalbermatten. The results Professor W. W'. Macdonald 36 of this research are published in three books, under the Department oj Entomology. Lirerpool Schlool of series title "World Bank Studies in Water Supply and Tropicail Medicine (fortmerlh Department of Sanitation." Numbers 1 and 2 of this series were Entomology, London School of Hygiene andel published in 1982 by the Johns Hopkins University Tropical Medicinee) Press and are entitled Appropriate Sanitation Alternac- Dr. D. M. Mackas 17 tives: A Technical and Econonfic .4ppraisal (by J. M. Ross Inistitute of 7ropical HYgiene. London School Kalbermatten. D. S. Julius, and C. G. Gunnerson) and of Hygiene and Tropical .Mledicine PREFACE xx U Dr. R. L. Muller 24, 25. 26, 27, Department of The World Bank was instrumental in Commonwealthl Institute o( Helminthology, St. 28, 29. 30. 31. guiding this book from its first manuscript in 1978 to its .41bans (former/v Department oj Medical 33 34 final manuscript in 1981, and so to the printed book in Helminthology, London School of HJygiene aind 1983. We are especially indebted to Mr. James McEuen Tr-opical Medlicinie) for his major contribution to the structure and content Dr. J. S. Slade 9 of the book. Jamie Cameron, Ian McIntosh, Lyn Udall Thames Water Authority, London and their colleagues at John Wiley & Sons, UK, ensured the rapid and efficient publication of the final Dr. B. A. Southgate 22 manuscript. Ross Institute of Tropical Hygiene, London School We thank the reviewers of earlier manuscripts for of Hygiene anid Tropical Medicine their thoughtful and constructive suggestions: Dr. F. Dr. D. C. Warhurst 19. 20. 21 A. Butrico, Dr. V. J. Cabelli, Dr. W. Crewe, Dr. B. Departnment of Medical Protoz00logy, Londmi Cvjetanovic, Dr. R. H. Gilman, Dr. J. M. Hughes, Dr. B. School of Hvgiene anld Tropical Medicine R. Laurence, Dr. J. C. Leighty, Mr. W. L. Reyes, Dr. H. 1. Shuval, Dr. B. B. Sundaresan, Professor A. Wolman, Professor A. J. Zuckerman 10 and Professor A. M. Wright. Departmnent of Medical Microbiology, London Many others have assisted in various ways, and we Schiool of Hygienie and Tr-opical Medicine especially acknowledge Dr. F. 1. C. Apted, Ms. Angela * Sadly, Dr. Donald Mackay died while this book was going to Batten, Ms. Pauline Berrington, Dr. M. Blaser, Ms. press. He made a substantial contribution to it, and we trust that he Elizabeth Burge, Ms. Margaret Carroll, Mr. P. would have been pleased by the final result. Hawkins, Professor K. Ives, Dr. B. Karlin, Ms. Jane Lillywhite, Dr. M. McGarry, Dr. G. Groenen, Mr. C. The book evolved, the group of contributors was Milr an'r .B.Sirw convened, and the chapters on specific diseases initially Dr. a.d DuggMn an Ms.S each comprised a short general account followed by W c Museum of Mec Sciec London we abstracted references. Following the review ofthis draft, Wellcome Museum of Medcal Science, London, were Dr. Feachem rewrote these chapters, incorporating of great assistance in collecting the photographi ad. Feachem r o thters,lninuscrorat.i illustrations for Part Two. A considerable number of aTinchalptersai toeirf form a econtin account. the references cited were translated from the originals. Thb hpesi their fiagfrawrah and we acknowledge the valuable work of Sandy Cairncross (Portuguese), Mario Campa (Italian), Agnes Candler (French), Zuzana Feachem (Czech, Acknowledgments Slovak, and Russian), and Rieko Fukano (Japanese). Bibliographic, editorial, and secretarial assistance was This review of sanitation and disease was originally ably provided by Mary-Grace Browning, Agnes commissioned by The World Bank, and the Bank Candler, Jackie Channon, Margaret Dawson, Alison comm1ssloned ~ ~ ~ ~ ~ ~ aves Lynn Daves Dianne Fishman and Jilln '. ' covered a proportion of the costs involved in the Davies, Lynne Davies, Dianne Fishman. and preparation of the manuscript. We are indebted to the ha Bank's staff for their support and encouragement. We RICHARD G. FEACHEM particularly acknowledge the assistance of Mr. John DAVID J. BRADLEY Kalbermatten, Mr. Charles Gunnerson, Dr. DeAnne London HEMDA GARELICK Julius, and Mr. Richard Middleton. The Publications June 1982 D. DUNCAN MARA Acronyms and Abbreviations BOD Biochemical oxygen demand BOD, Biochemical oxygen demand by the standard test (5 days at 20°C) °C Degrees Celsius DNA Deoxyribonucleic acid DVC Double-vault composting [toilet] EIEC Enteroinvasive Escherichia coli ELISA Enzyme-linked immunosorbent assay ENT E. coli enterotoxin plasmids EPEC Enteropathogenic E. coli ETEC Enterotoxigenic E. coli ID50 Median infective dose IEM Immuno-electronmicroscopy LT Heat-labile [E. coli enterotoxin] PFU Plaque-forming unit PVc Polyvinyl chloride RNA Ribonucleic acid ROEC Reed Odorless Earth Closet ST Heat-stable [E. coli enterotoxin] t9o Time at which 90 percent re- duction [in number of excreted pathogens] is achieved TAB Salmonella typhi and S. paratyphi A and B [vaccine] TCID,, Median tissue culture infective dose VIP Ventilated improved pit [latrine] WHO World Health Organization xxvii Part One The Health Hazards of Excreta: Theory and Control 1 Elements and Health Risks of Excreta and Wastewater IN THIS OPENING CHAPTER the nature and health risks children and infants in developing countries. Cholera, of excreta, sewage and sullage are examined. Attention whether endemic or epidemic in form, is accompanied is given to both the composition and likely pathogen by numerous deaths in all age groups-although content of human wastes, the quantities of excreta and under endemic conditions, it is children who suffer the sullage produced in different countries of the world, most fatalities. Other diseases, such as hookworm and the hazards posed to public health by the infection and schistosomiasis, cause chronic debilitat- microbes, parasites, and insects implicated in the ing conditions that impair the quality of life (however spread of excreta-related human infections. defined) and make the individuals more liable to die from superimposed acute infections. These diseases, and the many others discussed in this Excreta and Health book, start their journey from an infected individual to a new victim when the causative agent is passed in the This book is about human excreta and disease. excreta. Therefore the collection, transport, treatment, Excreta are defined here as human feces and urine. and disposal of human excreta are of the utmost Many infections, in excess of fifty even if the different importance in the protection of the health of any numbered types of viruses and serotypes of enteric community. They become even more important in bacteria are ignored, are transmitted from the excreta those societies which recognize the value of human of an infected person to the mouth of another. The excreta in agriculture, aquaculture or gas production disease-causing agents (the pathogens) of these and therefore reuse, rather than dispose of, their raw or infections travel from anus (or, rarely, bladder) to treated wastes. Such reuse systems have a positive role mouth by a variety of routes-sometimes directly on in supporting economic activity and food production contaminated fingers and sometimes on food, utensils, and are often cheaper than alternative methods of in water, or by any other route which allows minute disposal. However, reuse systems present a challenge to amounts of infected excreta to be ingested. Some of the public health engineer to design and develop these pathogens may reinfect, not only through the technologies that will not pose unacceptable risks to mouth, but by inhalation of dust or aerosol droplets. health. There are also a few infections (notably hookworms Around the world, and in most countries, there are and schistosomiasis) that can penetrate through the millions of people who lack any hygienic and skin. acceptable method of excreta disposal. There are also Human excreta are the principal vehicle for the governments and international agencies spending, or transmission and spread of a wide range of preparing to spend, large sums of money to improve communicable diseases. Some of these diseases rank this situation. If these governments and agencies could among the chief causes of sickness and death in arrange, by massive investment and miraculous social societies where poverty and malnutrition are ubiqui- and economic transformation, that everyone be tous. Diarrheas, for instance, are-together with provided with a modern house with water and malnutrition, respiratory disease and endemic sewerage connections, the health dimensions discussed malaria-the main causes of death among small in this book would be less relevant. But change will not 3 4 HEALTH HAZARDS OF EXCRETA come in this way. Change will come slowly and fecal weights than others. The data in table 1-1 show unevenly, and resources of money, manpower, and wet fecal weights reported by various authors from institutions will often be very scarce. The recipients of several countries. new excreta disposal technologies may be unable to The water content of feces varies with fecal weight. In pay completely for them, or they may lack the a community with an average wet fecal weight of necessary experience and education to use them 100-1 50 grams per day, for instance, the water content effectively. Always there will be many constraints, and will be around 75 percent. As fecal weight increases, so with these constraints will come difficult choices. does the proportion of water: at a fecal weight of 500 Choices need to be made about all aspects of excreta grams per day, the water content of the stool may be disposal. There will be choices about technology, about 90 percent. The frequency of defecation also about ultimate disposal, about reuse, about sullage, varies with fecal weight. In Europe and North America, about payment, about management, and about all the where fecal weights are generally under 200 grams per other elements that make up a sanitation system. day, the average frequency is one stool daily. In rural A number of factors will influence these choices, areas of developing countries, especially where diet is but one central factor is heealth. Since a primary vegetarian and fecal weights are high, a daily frequency motivation for investing in excreta disposal is of two or three stools is common. improved health, decisionmakers will need to under- Most adults produce between 1.0 and 1.3 kilograms stand the health implications of the various choices. of urine per day, but this depends on how much they The more limited are the resources, the more difficult drink and sweat, and this-as with fecal output-in the choices and decisions become-and the more it is turn depends on diet, occupation, climate, and other necessary to understand precisely and in detail the factors. If possible, local data should be consulted in relationships between excreta and health. designing a night soil system. In the absence of such data, a working assumption in a developing country is that adults will produce daily about 350 grams of feces Characteristics of Excreta and Sewage and 1.2 kilograms of urine in rural areas, and 250 grams of feces and 1.2 kilograms of urine in urban areas. Feces not only are malodorous and considered Volumes of night soil produced for cartage and esthetically offensive in most societies, but they may treatment may be computed from the sum of the per contain an array of pathogenic viruses, bacteria, cysts capita contribution of feces and urine plus any water of protozoa, and eggs of helminths (the collective term used for ablution or for cleaning the toilet area. Daily for worms parasitic to man) that may cause disease in a night soil volumes are typically in the range of 1.5-2.0 new host. Feces are therefore the beginning of the liters per capita. Data from Kiangsu Province, China, transmission routes of the diseases considered in this show that a bucket-latrine system produces 2 liters of book; the objective of improving excreta disposal waste per capita daily, including the bucket wash water facilities is to intercept these routes at their point of (McGarry and Stainforth 1978). origin. Volumes of domestic sewage depend on quantities of water used in the home. Houses connected to sewers Qtia tities must also be connected to water systems and usually have comprehensive plumbing fittings. Such houses There are marked differences in the volumes of may, rarely, use as little as 30 liters per capita daily excreta and sewage produced by different com- (White 1977).Ifdailyusefallsbelow50literspercapita, munities. Volume, composition, and consistency of however, the sewers can lose their self-cleansing flow feces depend on such factors as diet, climate, and state and become blocked. At the other extreme, households of healih. Individual wet fecal weights vary from under with many water-using appliances (such as washing 20 grams per day to 1.5 kilograms per day. When machines and dishwashers) may use 300 or more liters national or regional averages are considered, however, per capita daily. Europeans and North Americans produce daily The consistency or solids content of night soil may between 100 and 200 grams, whereas people in be calculated from these figures. Assume a daily fecal developing countries have average daily wet fecal weight of 250 grams per capita, with a water content of weights of 130-520 grams. Vegetarians generally have 80 percent. Further assume a daily urine production of higher fecal weights than other groups, and fecal 1.2 liters plus 0.35 liters of water for anal cleansing per weights in rural areas are higher than in towns. capita. The night soil of one individual then, will Children, adolescents, and the elderly produce lower contain 50 grams of solids in 1.8 liters of night soil; in ELEMENTS AND HEALTH RISKS 5 Table 1-1. Fecal weights around the world Daily wetftcal weight (grams) Number of Country Population' subjects Auerage Range Sourceb India Nurses 13 155 ND Burkitt, Walker and Painter (1972. 1974) Less than 15 years old in New 36 374 50-1060 Tandon and Tandon (1975) Delhi More than 15 years old in New 514 311 19-1505 Ibid. Delhi Kenya Hospital staff in rural area 16 520 300->500 Cranston and Burkitt (1975) Malaysia Chinese Urban 1 227 180-270 Balasegaram and Burkitt (1976) Rural 10 489 386-582 Ibid. Malays Rural 10 465 350-550 Ibid. Indians Urban 5 170 110-240 Ibid. Rural 8 385 255-520 Ibid. Doctors Urban 6 135 40-300 Ibid. Peru Rural Indians 20 325 60-650 Crofts i1975) South Africa Rural Schoolchildren (black, age 9-12 32 16 ND Walker (1975) years) (dry weight) Schoolchildren (black) 500 275 150-350 Burkitt, Walker and Painter (1972, 1974) Urban Schoolchildren (black) 500 165 120-260 Ibid. Tertiary students (white) 100 173 120-195 Ibid. Uganda Teenage boarding school pupils 27 185 48-348 Burkitt, Walker and Painter (1972, 1974) Villagers 15 470 178-980 Ibid. United Kingdom Naval recruits and wives 15 104 39-223 Burkitt, Walker and Painter (1972, 1974) Teenage boarding school pupils 9 110 71-142 Ibid. Vegetarians 24 225 71-488 Ibid. Hospital patients (fiber added to 6 175 128-248 Ibid. diet) Laboratory staff 4 162 123-224 Greenberg (1976) Medical students 33 132 ND Cummings (personal communication) Medical staff (age 22-36 years) 11 107 60-182 Goy and others (1976) United States Cincinnati, Ohio 5 115 76-148 Connell and Smith (1974) Philadelphia, Penn. Black students 10 148 ND Goldsmith and Burkitt (1975) White students 10 192 ND Ibid. San Francisco, Calif. Medical staff 5 91 ND Gray and Tainter (1941) Norwalk, Conn. Volunteers (age 23-47 years) 6 103 49-160 Fuchs, Dorfman and Floch (1976) ND. No data. Source: John Cummings (British Medical Research Council's Dunn Nutrition Unit, University of Cambridge) compiled the information contained in the table. a. Subjects were on ad fib. diets except where indicated b. Full citations of sources in this and subsequent tables appear in the reference lists. 6 HEALTH HAZARDS OF EXCRETA other words, a solids content of 2.8 percent. If paper is whatever BOD5 contribution is made by the paper or used for anal cleansing, the solids content will increase other material used for anal cleansing. In the United to around 5 percent. The solids content of night soil is States, Laak (1974) has found that urine contains 8.6 therefore similar to that of primary sewage works grams of BOD5 per liter and that feces contain 9.6 grams sludge. Data from Japan, the island of Taiwan, and of BOD5 per 100 grams. As fecal weights increase and Thailand indicate a solids content for night soil in the moisture content rises, the BOD5 contribution per unit range 2.0-4.2 percent, with mean figures of 2.7-3.7 weight of wet feces clearly will fall. In addition, it is percent (Pescod 1971). possible that higher fecal weights will be associated with a higher fiber content that may not be readily Chemical composition biodegradable, causing the higher fecal weights to be accompanied by lower BOD5 contributions per unit Excreta, especially feces, are of complex and variable weight of dry feces. composition. Typical figures of some constituents are Possible ROD5 contributions at different fecal given in table 1-2. Of particular interest to the sanitary weights are given in table 1-3. These are speculative engineer are the data on carbon and nitrogen content calculations and require confirmation by field testing. indicating that the C:N ratio in feces is in the region of Laak (1974) has found that the daily BOD5 contri- 8, whereas in urine it is under 1. These figures have bution of toilet paper in the United States is 3.5 grams considerable bearing on the design of composting per capita, and this figure may be lower in some systems in which the C:N ratio must be around 20-30 developing countries where water or non- for the process to proceed efficiently (Gotaas 1956). biodegradable material is used. Where heavy paper Of equal importance to the public health engineer is (cement bags or newspaper), corncobs, or leaves are the concentration of organic material, measured by the used, however, the contribution of anal cleansing biochemical oxygen demand (BOD) or other similar material may be as in the United States. Figures have index (such as chemical oxygen demand, or total been added in table 1-3 to account for the contribution organic carbon).' In a night soil system, the per capita of anal cleansing material to the BOD5 in night soil. BOD5 contribution is equal to the BOD5 in excreta plus If a total daily volume of excreta and anal cleansing material of 1.5 liters per adult is assumed, it is possible to calculate the BOD5 strength of adult night soil (table Table 1-2. Composition of human feces 1-3). Although the weights of BOD5 for children will be and urine lower, the volumes will also be lower, so that the concentration will be similar to that for adults, and the Approximate composition final night soil strength may be as calculated. Pradt (percent of dry weight) (1971) found a night soil BODs content of 10,000 milligrams per liter in Japan, and Hindhaugh (1973) Constituent Feces Urine found 46,000 milligrams per liter of HOD5 in night soil in Lagos, Nigeria. This last figure is extremely high and Calcium (CaO) 4.5 4.5-6.0 may reflect the practice in Lagos of disposing of Carbon 44-55 11-17 garbage in the night soil buckets.2 However, the daily Nitrogen 5.0-7.0 15-19 volume of night soil produced in Lagos is about 1.5 Organic matter 88-97 65-85 Phosphorus (P205) 3.0-5.4 2.5-5.0 liters per capita, the figure assumed in table 1-3. Potassium (K20) 1.0-2.5 3.0-4.5 In a sewerage system the per capita BOD5 contribution is augmented by sullage, which contains Source: Adapted from Gotaas (1956). organic wastes and thus will also exert an oxygen demand. Typical figures for sewage that includes sullage are presented in table 1-4. Further data on the 1. The BOD is the mass of oxygen required by microorganisms to BOD5 in sullage can be found in the section oxidize the organic content of the waste. It is an indirect Characteristics of Sullage" in this chapter. measurement of the concentration of biodegradable material present. BOD5 denotes the oxygen demand exerted during the standard test, which is conducted at 20'C over 5 days. The chemical 2. Garbage may be placed in the night soil buckets because of the oxygen demand is the mass of oxygen consumed when the organic lack of an adequate refuse disposal system. Huponu-Wusu and matter present is oxidized by strong oxidizing agents in acid solution. Daniel (1977) found that only 39 percent of 1,099 randomly sampled It includes some substances (such as cellulose) that are not available households in metropolitan Lagos are reached by the refuse to microorganisms but excludes some (such as acetic acid) that are. collection service of the city council. Table 1-3. Possible standard biochemical oxygen demand (BOD5) content of excreta and night soil BOD5 content Assumed Per adult Strength Assumed adult urine Estimated In wet Total in anal- oJ night adultfecal weight water feces Per adult Per adult per adult cleansing soil weight (kilograms in feces (0 I" I I infeces in urine in excreta material ( Population (grams daily) daily) (percent) per gram)b (grams da,i l (grams daily) (grams daily) (grams daily) per liter)c Europe and North America 150 1.2 75 96d 14.4 10.3 24.7 3.5d 18,800 Developing country Urban 250 1.2 80 77 19.3 10.3 29.6 3.0' 21,700 Rural 350 1.2 85 58 20.3 10.3 30.6 2.0' 21,700 Notes: This table is speculative and should not be used if actual data are available. a. Fecal weights are taken from the ranges given in table 1-1. b. Calculated by assuming that the BOD5 contribution is constant per unit weight of dry feces. This assumption is unlikely to be accurate because the proportion offiber will increase as fecal weight increases, and fiber is not readily biodegradable. c. Assuming that 1.5 liters are produced by each adult daily. d. From Laak (1974). e. Where water is used for anal cleansing, this figure will be 0. Table 1-4. BOD5 contributions per capita in urban sewage BOD, per capita daily Country or region in sewage (grams) Brazil (Sao Paulo) 50 France (rural) 24-34 India 30-55 > Kenya 23-40 > Nigeria 54 Southeast Asia 43 o United Kingdom 50- 59 United States 45-78 Zambia 36 D Note: These figures were calculated by measuring the BOD5 of raw sewage and multiplying it by the estimated daily water use per capita. This gives a most approximate result because urban sewage may contain a substantial proportion of commercial andindustrial wastes. Domestic water use and BoD5 contributions are not readily derived from data on total urban sewage, and these figures arc not directly comparablc with those in table 1-3. ELEMENTS AND HEALTH RISKS 9 Pathogens in exereta (listed in table 1-5) are particularly important- Part Two of this work contains detailed information adenoviruses, enteroviruses (including poliovirus), about the organisms causing human excreta-related hepatitis A virus, reoviruses and diarrhea-causing diseases; however, a brief summation here of the major viruses (especially rotavirus). Other virus groups are disease agents examined in Part Two may be of also found in feces. Infections with all of these, diseae agets exmine in Prt Tw may e of especially in children, are often subclinical. assistance. Four groups of pathogens-viruses, bac- -sregards theden, tero subelimstpli teria, protozoa, and worms-cause these diseases. In i s r d nte risest any i ica . inss addition, excreta disposal may favor the breeding of Sometimes howeverinecto an lead ild insects, particularly mosquitoes, flies, and cockroaches, inlenikes, illessr, tirs eti s,"nor to mild which will always have Duisance value aDd may act as ifunalk lns,t vrsmnnii, rt whchrs wil humalysehave niagence vhaluetan may acts s paralytic poliomyelitis, which may lead to permanent vectors of human disease agents that may themselves diailt or det.I.setmtdta aayi no be fon in fee *ruie disability or death. It iS estimated that paralytic not be found in feces or urine. poliomyelitis occurs worldwide in only about I out of every 1,000 poliovirus infections, but most children VIRUSES IN EXCRETA. Numerous virusesm in fect become infected in developing countries, and con- thernesina treyact andfet passedmin ,th fe sequently the number of paralysis cases can be high. wherupontheymay nfec newhuma hoss by Echovirus and coxsackievirus infections can cause a ingestion or inhalation. One gram of human feces may contain i09 infectious virus particles, regardless of wide range of diseases and symptoms including simple whether the individua is experiencing any d e fever, meningitis, respiratory illness, paralysis, myocar- whether the individual IS experiencing any discernible diis an.te .oniin se hpe ) illness. Although they cannot multiply outside a d otis, and other viruses apr f i e suitable~~~~~ ~~~~ hscelthexrtdvrssmasviefr Rotaviruses, and other viruses, are found in the feces sutal .hs 'cl,hecetdvuemy s f of a large number of young children suffering from many weeks in the environment, especially if diarrhea and are another important group of excreted temperatures are cool ( <15°0C). Concentrations of 10 .. . viruses. Their precise causative role and epidemiology infectious particles per liter of raw sewage have been remain uncertain, but they are responsible for a reported, and excreted viruses can be readily isolated substantial roportion of diarrhea episodes amon from soil and natural waters at sites which have been c tphpt g young children in many countries (see chapter 11). exposed to fecal discharges (World Health Organiz- Hepatitis A virus is the causative agent of infectious ation 1979). Five groups of pathogenic excreted viruses hepatitis. Infection may lead to jaundice but, especially in young children, is often symptomless (see chapter 3. The term "excreted virus' is used here for comparability with 10). "excreted bacterium," "'excreted helminth," and so on. "Excreted virus" is synonymous with "enteric virus," which must be distinguished from the genus Enterovirtus, which includes polio-, BACTERIA IN EXCRETA. The feces of a healthy person echo-, and coxsackieviruses. contain large numbers of commensal bacteria of many Table 1-5. Viral pathogens excreted injeces Can Chapter symptomless containing infections detailed Virus Disease occuir? Reservoir information Adenoviruses Numerous conditions Yes Man 9 Enteroviruses Polioviruses Poliomyelitis, paralysis and other Yes Man 9 conditions Echoviruses Numerous conditions Yes Man 9 Coxsackie viruses Numerous conditions Yes Man 9 Hepatitis A virus Infectious hepatitis Yes Man 10 Reoviruses Numerous conditions Yes Man and 9 animals Rotaviruses, Norwalk agent and Diarrhea Yes Probably II other viruses man Note: See table 9-1 for more information. 10 HEALTH HAZARDS OF EXCRETA species. The species of bacteria found in the normal are at risk, but the patient is not disseminating bacteria stool, and the relative numbers of different species, will in the community. A paticnt with a mild case, or a vary among communities. The bacteria most com- carrier, by contrast may look relatively healthy and be monly found and an indication of the variations in mobile while excreting up to 106 chloera vibrios per their concentrations in feces are given in table 1-6. gram of feces. In some infections the carrier state may Because these bacteria are ubiquitous and numerous in last for a duration similar to the illness itself, but in the feces of healthy people, they have been used as others it may persist for months or even a lifetime. indicators of fecal pollution.4 The most widely used Some carriers may show symptoms of illness and indicator has been the fecal coliform Escherichia coli, continue to excrete the bacteria, whereas others may be the main constituent of the "enterobacteria" group in healthy throughout infection. A carrier becomes table 1-6, but enterococci (or, more generally, fecal especially dangerous when engaged in food prepara- streptococci), another widespread commensal group, tion or handling or in water supply. are also used as indicators. Anaerobic bacteria also, Some of the pathogens listed in table 1-7 are excreted such as Clostridium, Bacteroides, and Bifidobacterium, entirely (or almost entirely) by man, but others are have served as indicators, and their potential value as excreted by a wide range of animals. This fact limits indicators is currently attracting increased attention disease control through improvements in human (Evison and James 1977). excreta disposal alone, because any changes made will On occasion, some bacteria listed in table 1-6, or likely not affect transmission of pathogens from animal their particular strains, may give rise to disease, as may feces to humans. Three of the major infections listed in other groups of bacteria normally absent from the table 1-7 (typhoid, shigellosis, and cholera), however, healthy intestine. These pathogenic, or potentially are assumed to be exclusively human infections, whose pathogenic, bacteria are listed in table 1-7. They most spread is from one person to another. commonly enter a new host by ingestion (in water, on In summary, all the viral and bacterial pathogens food, on fingers, in dirt), but some may also enter listed, respectively, in tables 1-5 and 1-7 are passed in through the lungs (after inhalation of aerosol particles) the feces of man or animals; they are not free living.5 or through the eye (after rubbing the eye with fecally Infection of a new host normally follows ingestion of contaminated fingers). At some time during the course the pathogens and because transmission is primarily of an infection, large numbers of the bacteria will be through the swallowing of minute quantities of infected passed in the feces, thus allowing the spread of infection feces, the sanitary disposal of all feces (both human and to new hosts. animal) and perfect personal hygiene would largely Diarrhea is a major symptom of many bacterial eliminate these diseases. For many infections, this has intestinal infections. The bacteria may also invade the unfortunately proved an unattainable goal in even the body from the gut and cause either generalized or most affluent societies, and so a more modest target localized infections. This invasion is characteristic of than eradication must be set: the reduction of typhoid infections and other enteric fevers caused by transmission to a manageable level. salmonellae. During infections restricted to the gut, Bacteria of the genus Leptospira have been excluded bacteria will be passed only in the feces. When invasion from the discussion above because they cannot be has occurred, bacteria may be passed in the urine as included in the generalizations made. Although well and will also be found in the bloodstream at some leptospirosis in the majority of human cases gives rise stage. to a benign, self-limiting, febrile illness, it occasionally A carrier state exists in all the infections listed in leads to severe, even fatal disease characterized by table 1-7. Thus, in communities where these infections jaundice and hemorrhage (Weil's syndrome) where- are endemic, a proportion of perfectly healthy upon death may result from kidney failure. Leptospira individuals will be excreting pathogenic bacteria. are excreted in the urine of animal carriers, and usually These carriers play a prominent role in transmitting reach new animal and human hosts through skin the infection they carry because they are mobile, abrasions or mucous membranes contaminated by dispersing their feces widely. Cholera provides an infected urine. Man may be an intermittent carrier for a example of the problem. A patient with severe cholera few weeks (rarely months) after an acute infection. will be in bed for most of the time he or she is excreting Leptospirosis is considered here because of the risk to Vibrio cholerae. Those who nurse the patient clearly workers who handle excreta, which may contain leptospires either from animal carriers (for example, 4. The use of indicator organisms is discussed in more detail in chapters 4 and 13. 5. This may not be true for Vibrio cholerae; see chapter 17. Table 1-6. Bacterial microflo7a of humanfeces by national diet Number of bacteria infeces (mean log,0 per gram) National Entero- Bifido- diet Country bacteriaa,b Enterococcib Lactobacilli Clostridia Bacteroides bacteria Eubacteria Largely Guatemala 8.7 7.9 9.0 9.3 10.3 9.4 ND m carbo- Hong Kong 7.0 5.8 6.1 4.7 9.8 9.1 8.5 i m hydrate India 7.9 7.3 7.6 5.7 9.2 9.6 9.5 m Japan 9.4 8.1 7.4 5.6 9.4 9.7 9.6 - Nigeria 8.3 8.0 ND 5.9 7.3 10.0 ND > z Sudan 6.7 7.7 6.4 4.9 7.8 8.5 ND Uganda 8.0 7.0 7.2 5.1 8.2 9.4 9.3 Mixed Denmark 7.0 6.8 6.4 6.3 9.8 9.9 9.3 _ Western England 7.9 5.8 6.5 5.7 9.8 9.9 9.3 Finland 7.0 7.8 8.0 6.2 9.7 9.7 9.5 m Scotland 7.6 5.3 7.7 5.6 9.8 9.9 9.3 United States 7.4 5.9 6.5 5.4 9.7 9.9 9.3 ND. No data. Sources: England, India, Japan, Scotland, United States, Uganda (Drasar 1974); Denmark, Finland (International Agency for Research on Cancer 1977); Hong Kong (Crowther and others 1976); Nigeria, Sudan (Draser, personal communication); Guatemala (Mata, Carrillo and Villatoro 1969). a. This group mainly contains Escherichia coli. b. These two groups are the most commonly used fecal indicator bacteria. 12 HEALTH HAZARDS OF EXCRETA Table 1-7. Bacterial pathogens excreted in feces Caln Chapter svllptoinless containing illect ion detailed Bacterium Disease occU r? Reservoir informnation Campylobacrer fetus ssp. jejoiii Diarrhea Yes Animals and man 12 Pathogenic Escherichia colia Diarrhea Yes Man' 13 Sulmonella S. typhi Typhoid fever Yes Man 15 S. paratyphi Paratyphoid fever Yes Man 15 Other salmonellae Food poisoning and other Yes Animals and man 15 salmonelloses * ..: spp. Bacillary dysentery Yes Man 16 Vibrio 1: chlolerae Cholera Yes Man 17 Other vibrios Diarrhea Yes Man 17 Versinia enterorolitica Diarrhea and septicemia Yes Animals and man' 18 a. Includes enterotoxigenic, enteroinvasive, and enteropathogenic E. coli. b. Although many animals are infected by pathogenic E. coli, each serotype is more or less specific to a particular animal host. c. Ofthe 30 or more serotypes identified so far, a number seem to be associated with particular animal species. There is at present insufficient epidemiological and serological evidence to say whether distinct serotypes are specific to primates. the sewer rat, Raittus norcegicus) attracted to such agent of human onchocerciasis, or river blindness), are environments or, occasionally, from infected people. not considered.6 Helminths (except for Strongyloides) do not multiply PROTOZOA IN EXCRETA. Many species of protozoa within the human host, and this is of great importance can infect man and cause disease. Among them are in understanding their transmission, the ways they several species that are harbored in the intestinal tract cause disease, and the effects of environmental changes of man and other animals, where they may cause on their control. Helminthic disease is not an all-or- diarrhea or dysentery. Infective forms of these nothing phenomenon. In infections due to viruses, protozoa are often passed as cysts in the feces, and man bacteria and protozoa, where massive asexual repro- is infected when he ingests them. Only three species of duction occurs within the host, once infection occurs its human intestinal protozoa are considered to be severity cannot be related easily to the infecting dose of frequently pathogenic: Giardia lamiblia, Balanitiduntl organisms. One either has measles, or a common cold, coli, and Entamoeba histolytica (see table 1-8). An or not and it is not meaningful to say that someone has asymptomatic carrier state is common in all three and, 'a lot of measles"'. By contrast, with helminthic in the case of Entamoeba histoltica, it is carriers who infections it is essential to think quantitatively. The are primarily responsible for continued transmission. HELM4INTHSIN EXCRETA. Many species of parasitic 6. An exception, discussed in detail in chapter 36, is the HELMtNHS tN XCRETA Many peciesof parsitic bloodborne larva of the filarial worm causing elephantiasis. which worms, or helminths. have human hosts. Some can may be transmitted by Ctlex pipiens mosquitoes. which breed in cause serious illnesses, but a number generate few sewage, sullage. and other polluted waters. Culex pipiens is a complex symptoms. Only those helminths whose eggs or larval of mosquito species and subspecies. The main tropical species. and forms are passed in the excreta are of concern to this the major vector of filariasis in those tropical areas where the infection is Culex-transmitted. is Culex quinquejasciatus (previously study. Only Schistosorala hcaematobitan7l (the agent of also known as Culex pipiens latigan.s. C.p. quinquejasciutus. or C. urinary schistosomiasis) is voided in the urine: Jatigats(. Other important species are C.p. pipien., C.p. ozolestus (the the others examined are all excreted in the leces. vector of filariasis in Egypt), and C.p. pallens. More details on the The helminths that begin a new cycle of transmission complex are provided in chapter 36. 'Culex pipiens" will be used by escaping from a blister on the carrier's skin (guinea throughout the text unless a particular member of the complex is being referred to. Because they are not specifically associated with wormn Dracunculus mediulensis), or by entermg the excreta, othcr inscctborne pathogens (such as trypanosomes and body of a blood-feeding insect to be transmitted I. ,... ... i their vectors, and the diseases they cause are excluded through its bite to a new host (Onchocerca volvulus, the from the purview of this study. ELEMENTS AND HEALTH RISKS 13 Table 1-8. Protozoal pathogens excreted infeces Can Chapter symnptomlness containing infections detailed Proto-oon Disease occur? Reservoir information Balantidium Diarrhea, dysentery and colonic Yes Man and animals (especially pigs 19 coli ulceration and rats) Entamoeba Colonic ulceration, amebic histolvtica dysentery, and liver abscess Yes Man 20 Giardia Diarrhea and malabsorption Yes Man and animals 21 lamblia question is not just whether or not someone has a Because of this quantitative characteristic, the hookworm infection but how many worms has he (in development of pathology in helminthic infections is other words, how "heavy" or "intense" is the infection). usually the result of cumulative worm burdens, often Sometimes worm burdens can be determined by carried over many years as a product of regular and purging the patient immediately after an anthel- repeated reinfection. This further contrasts with the minthic, but more usually the output of eggs in the asexually replicating organisms, which may cause an exereta is determined and used as an index of the overwhelmingly heavy infection and a state of gross intensity of infection. Even though there is a good deal disease within a few days or weeks after a single of variation from day to day, the relation is valid at infective dose enters the body. community level and in any case the egg output is The excreted helminths are listed in table 1-9. Often always a better measure of transmission and the developmental stages through which they pass sometimes a better guide to pathology than the burden before reinfecting man, their life cycles, are very of adult worms. complex (as is shown in the table). The helminths are Worm burdens and levels of egg output are not evenly classified in two main groups: the roundworms or randomly distributed among their human hosts, and (nematodes) and those worms that are flat in cross- within any sex and age group of an infected community section. The flatworms again form two groups: the there will be a few people who are carrying a heavy tapeworms (cestodes), which form chains of helminth worm burden and a much larger number with light 'Isegments," and the flukes (trematodes), which have a intensities of infection. In general, the risk of illness and single flat, unsegmented body. The roundworms may its severity increases with the worm burden. It is cause mechanical obstruction (Ascaris), rectal pro- therefore common in helminth infections to find many lapse (Trichuris), itching around the anus (Enterobils), of the community infected, occasional people (often or anemia (hook-worms). They also divert food to with heavy infections) ill, and a few dying. It is themselves and produce abdominal pain in some cases relatively easy to see the public health importance of (many cases, however, are symptomless). Adult the heavy infections but far harder to assess disability tapeworms create health problems mainly by depriving in the lightly infected majority where consequences are their host of nutrients. Of the trematodes, some inhabit likely tobe nonspecific andeffects cumulative with those and damage the liver (Clonorchis) or lungs (Paragoni- from other infections. nizis). The schistosomes live outside the intestine in The number of heavy infections is not simply small blood vessels; their eggs that fail to escape from proportional to the prevalence of infection. At high the host may damage several organs. The intestinal prevalences, increased transmission will tend mainly to flukes may occur in large numbers, are mostly push up the proportion of heavy infections while at low transmitted through food, and cause relatively mild prevalences there may be few people heavily infected symptoms. and the number may change little with transmission. Most of the roundworms infecting man, and also the Where immunity acquired by the host is unimportant, a schistosome flukes, have separate sexes, so that reduction in transmission due to control of excreta transmission depends upon infection with both male may reduce the number of heavy infections and so and female worms and upon the meeting, mating, and reduce the burden of disease even if it affects the egg production of these worms within the human body. prevalence of infection rather little. A number of individuals may be infected with a single Table 1-9. Helminthic pathogens excreted infeces Chapter containing detailed Helminth Common name Disease Transmission Distribution information Ancylostoma Hookworm Hookworm Man -* soil -man Mainly in warm 22 duodenale wet climates N Ascaris Round worm Ascariasis Man -, soil -- man Worldwide 23 hlimbr icoides Clonorchis Chinese liver Clonorchiasis Man or animal -* Southeast Asia 24 sinensis fluke aquatic snail -* fish -+ man Diphyllobothrium Fish Diphyllobothriasis Man or animal - Widely distributed foci. 25 latum tapeworm copepod - fish - man mainly temperate regions Enterobius Pinworm Enterobiasis Man - man Worldwide 26 vermicularis Fasciola Sheep liver Fascioliasis Sheep -- aquatic snail -; Worldwide in sheep- 27 hepatica fluke aquatic vegetation - and cattle-raising man areas Fasciolopsis Giant intestinal fluke Fasciolopsiasis Man or pig -- aquatic Southeast Asia, 28 buski snail -- aquatic mainly China vegetation -- man Gastrodiscoides n.a. Gastrodiscoidiasis Pig - aquatic snail - India, Bangladesh, 30 hominis aquatic vegetation - Vietnam, Philippines man Heterophyes n.a. Heterophyiasis Dog or cat -+ brackish- Middle East, 30 heterophyes water snail -- brackish- southern Europe, water fish -- man Asia Hymenolepis nana Dwarf tapeworm Hymenolepiasis Man or rodent - man Worldwide 29 Metagonimus n.a. Metagonimiasis Dog or cat -- aquatic East Asia, 30 yokogawai snail -+ freshwater Siberia (USSR) fish -+ man Necator amnericanus Hookworm Hookworm Man -* soil -+ man Mainly in warm 22 wet climates Opisthorchis Cat liver Opisthorchiasis Cat or man -+ aquatic USSR, 24 felineus fluke snail - fish -. man Thailand 0. viVerrini n.a. Paragoniimus Lung fluke Paragonimiasis Pig, man, dog, cat, or Southeast Asia, 31 westernnani other animal -- aquatic scattered foci in Africa snail -+ crab or cray- and South America fish -> man Schistosorna Schistosome Schistosomiasis; Man -- aquatic snail -+ Africa, Middle East, 32 haemnatobiunt bilharziasis man India S. japonictan Animals and man -* Southeast Asia 32 snail -- man S. rnansoni Man -+ aquatic snail -, Africa, Middle East, 32 man Central and South America Strongyloides Threadworm Strongyloidiasis Man -- man Mainly in warm 33 m z stercoralis wet climates Taenia saginata Beef tapeworm Taeniasis Man -,cow --man Worldwide 34 T solium Pork tapeworm Taeniasis Man -'pig Worldwide 34 (or man) man > Tricihuris Whipworm Trichuriasis Man - soil -+ man Worldwide 35 H trichiura n.a. Not applicable. 16 HEALTH HAZARDS OF EXCRETA sex or with unmated worms. These cases are of no for a period of about 4-6 weeks; chronic human epidemiological significance because they do not carrier states are rare. transmit infection. Magnitude of patlhogen excretion Characteristics of Sullage We can dramatize the magnitude of the potential Sullage. also known as gravwater, is domestic health hazard from excreta by considering a typical wastewater not containing excreta-the water discar- load of pathogens excreted by a poor tropical ded from baths, sinks, basins and the like that may be community in a single day. Estimated data on the more expected to contain considerably fewer pathogenic prominent diseases threatening public health and the microorganisms than sewage. Interest and research in large fecal volume, often containing significant the handling of sullage has increased in recent years, concentrations ofpathogenic organisms, produced in a both in developing and affluent countries. In affluent hypothetical community are given in table 1-10. countries there is growing interest in the use of Excreta-related diseases account for some 10-25 sewerless chemical toilets and separate sullage disposal percent of illnesses that reach the health care services, as a way of overcoming environmental problems and cause a vast amount of misery that goes associatedwiththedisposaloflargevolumesofheavily unreported. Given the dangers of poor sanitation, it is contaminated sewage from urban areas. There is also crucial that the engineering profession and the interest in chemical toilets and on-site sullage disposal appropriate governmental agencies of the world take for use in nature parks, where environmental seriously the responsibility to collect, transport, treat, considerations are paramount (Winneberger 1974). and reuse human waste substances in ways that do not There is also a growing realization in developing endanger the public. countries of the financial and other difficulties associated with providing waterborne sewerage sys- tems, and consequent increased interest in dry or on- site techniques such as improved pit latrines, In general, urine is a sterile and harmless substance. composting toilets or cartage systems (Kalbermatten There are, however, occasions when host infections and others 1982). Some of these sewerless technologies cause passage of pathogens in the urine. The three require the separate disposal of sullage when the principal infections leading to the significant ap- volumes of domestic wastewater become too great pearance of pathogens in the urine are urinary simply to drain away in the yard. Furthermore, a schistosomiasis, typhoid, and leptospirosis. Coliform worldwide awareness is dawning that it is extravagant and other bacteria may be numerous in the urine to use up to half of a household's high quality drinking during cystitis and other urinary infections, but they water just to flush excreta along sewers. The need to constitute no public risk. In venereal infections the design a sullage disposal system accompanies the microbial agents will also reach the urine, but they are development of any toilet not flushed by water. so vulnerable to conditions outside the body that excreta are unimportant vehicle of transmission. People infected with urinary schistosomiasis (caused Quantities by Schistosonia haematobium) will pass eggs chiefly in Sullage volumes depend upon domestic water use. their urine. The worms live for years (occasionally Where people use public taps, daily domestic water use decades) and superinfection occurs, so that those may be as low as 10 liters per capita (White 1977). In affected may pass eggs-sometimes accompanied by affluent households with full plumbing, daily water use blood-for much of their lifetimes. In heavy infections, may be 200 or more liters per capita, and all water not 10 millilitres of urine may contain over a thousand eggs used for flushing toilets may be classed as sullage. if the urine is collected near to midday, when eggs are Bennett, Linstedt and Felton (1974). studying homes in most numerous. During the phase of typhoid and the United States. found that the toilet was used 3.6 paratyphoid fevers when bacteria are disseminated in times daily per capita, that the average flush used 15 the blood, the organisms will usually be shed in the liters, and that toilet flushing accounted for 33 percent urine. In cases where S. haematobiunm is also present, of domestic water use. Witt. Siegrist and Boyle (1974), however, prolonged urinary carriage of typhoid may also studying homes in the United States, found occur over many years. An individual with lepto- corresponding figures of 2.3 times daily per capita, 15 spirosis will pass Leptospira intermittently in the urine liters for flush, and 22 percent of water use allocated to Table 1-10. Possible output of se/ected ,'- o H1 in thc feces and sewage o.j]a tropical communitY of 50,000 in a developing counlry prevalence of Average tnumbei oj infection in country organisms per grain 7Ttal excreted daily Concentration per Pathogen I j0. 'il of ffees6 pe- injected persoit lotal excreted dailY by town liter in town sevagd' Viruses Etterorirusesd 5 10o 1o8 2.5 x 101 5,000 Bacteria Pathogenic E. colie lo ,0 10'° ? ? Salmonella spp. 7 106 lo, 3.5 x 10" 7,000 *, spp. 7 106 lo, 3.5 x 101 7.000 l'ibrio cholerae 106 io8 5 x 10i' 1.000 m rn Protozoam Elntatnioeba hiseoirtica 30 15 x 10 15 x 10" 2.25 x 1011 4,500 Z Helmintbs > .Ascoaris lun,bricoides 60 lo4O 10" 3 x 10'° 600 Hookworms" 40 800o 8 x 104 1.6 x 109 32 Schistosomoa rnOtlsoIli 25 40' 4 x 103 5 x 107 1I Toaenic saginiata 1 104 106 5 x 108 10 Irichliris trichiura 60 2 x 10a 2 x 105 6 x109 120 C4 '? Uncertain. Note: [his table is hypothetical, and the data are not taken from any actual, single town. For each pathogen, however, the figures are reasonable and congruous with those tound in the literature. The concentrations derived for each pathogen in sewage are in line with higher figures in the literature, but it is unlikely that all these infections at such relatively high prevalences would occur in any one community. a. The prevalences given in this column refer to infection and not to morbidity. b. It must be recognized that the pathogens listed have different abilities to survive outside the host and that the concentrations of some of them will rapidly decline after the feces have been passed. The concentrations of pathogens per liter in the sewage of the town were calculated by assuming that 100 liters of sewage are produced daily per capita and that 90 percent of the pathogens do not enter the sewers or are inactivated in the first few minutes after the excretion. c. To calculate this figure it is necessary to estimate a mean fecal weight for those people infected. This must necessarily be the roughest of estimates because of the age-specific fecal weights and the age distribution of infected people in the community. It was assumed that people over 15 years old excrete 150 grams daily and that people under 15 excrete, on average, 75 grams daily. It was also assumed that two-thirds of all infected people are under 15. This gives a mean fecal weight for infected individuals of 100 grams. d. Includes polio-, echo-, and coxsackieviruses. e. Includes enterotoxigenic, enteroinvasive, and enteropathogenic E. coli. f. The distribution of egg output from people infected by these helminths is extremely skewed; a few people excrete very high egg concentrations. g. Ancvlostoma diuodeniale atid Necator uriericanus. 18 HEALTH HAZARDS OF EXCRETA flushing. Reviewing data from several studies, Witt and 1974). The sullage contributed 53 percent of the sewage colleagues found that water from toilet flushing was flow, 52 per cent of the BOD5, 43 percent of the chemical between 22 and 45 percent of the total domestic water oxygen demand, about 15 percent of the nitrogen, and usage. Laak (1974) reviewed data from Canada, 45 percent of the phosphates. The data in table 1-12 Sweden, and the United States that show the following further indicate that, if the ratio of chemical oxygen percentage allocations of water use in houses with full demand to BOD5 is used as the criterion, toilet wastes plumbing: are more resistant to biodegradation than sullage. Meani Range Hypes (1974) points out the effect of sink-installed Bathroom 26 12-40 garbage disposal units on the quality of sullage. In his Kitchen 9 5-16 ~~~~~~~test, sullage had a BOD5 of 328 milligrams per liter Kitchen 18 5-16 when without garbage solids and 480 milligrams per Tolanr 18h 4t-2 liter when with garbage. Another report found that in Toilet flushing 47 41-65 Taipei, sullage contributed 40 percent of BOD5 in We have been unable to obtain comparable figures sewage (but in Taipei, scraps were fed to pigs rather from urban households, either with or without sewer than washed down the sewers; World Health connections, in developing countries. Data for rural Organization 1970). households without sewers, however, are available, and Witt, Siegrist and Boyle (1974) examined the examples of water use allocations in Lesotho, Papua bacterial content of sullage in the United States. Their New Guinea, and Uganda are given in table 1-11. results,summarizedintablel-13,showthatwaterused These figures highlight the immense differences in for bathing and showering became less contaminated water use practice, and thus in the kind of sullage with fecal bacteria than water used in washing clothes. produced, in areas varying in culture, environment, Furthermore, 38 percent of the total fecal streptococcal wealth, and other factors. The health implications of isolates were enterococci (Streptococcuis Jaecalis, S. sullage disposal will depend on the technologies used, faecium, and S. duranis); the majority of the bath water which in turn must consider such variables as the enterococci were S. faecalis var. Iiquefaciens (in household volume of sullage, density of housing, local contrast, only a few enterococci isolated from the climate, soil type, and groundwater conditions. clothing waters were of this species, now widely regarded as being nonfecal in origin). S. bovis, a primnarily nonhuman species, accounted for 22 percent Composition of all streptococcal isolates. These findings suggest that The results of surveys of five households in the under half of the streptococci isolated were from United States are shown in table 1-12 (from Laak human feces, and that the bath water was even less Table 1-11. Allocation of water use in sewerless rural households in developing countries Couitry Uganda Papua New Guinea Water use Lesotlio (Enga Province) Lango Kigezi Average total daily use per capita (liters) 18 0.68 18 8 Bathroom (personal hygiene) (percent) 15 0 66 20 Laundry (percent) 22 0 Drinking Animals (percent) 2 8 0 0 Humans (percent) 45 79' 19 6' Kitchen (cooking and utensil hygiene) (percent) J 11 13 74 Vegetable gardens (percent) 6 0 0 0 Other (percent) 10 2 2 0 Sources: Lesotho (Feachem and others 1978); Papua New Guinea (Feachem 1977); Uganda (White, Bradley and White 1972). a. These are very small volumes of drinking water. In Papua New Guinea they may be due to low salt intake and consequent low fluid demand and to water intake from food, especially sugar cane. In Kigezi, Uganda. the practice of eating gruels and other high liquid foods may account for the low drinking water consumption. ELEMENTS AND HEALTH RISKS 19 Table 1-12. Pollution loads of wastewater sampledfrom various plumbingfixtures in the USA (milligrams per capita daily) Biochemical Chemical oxygen oxygen demand (BOD) demand NO3-N NH3-N P04 Wastewater source Mean Percent Mean Percent Mean Percent Mean Percent Mean Percent Bathroom sink 1,860 4 3,250 2 2 3 9 0.3 386 3 Bathtub 6,180 13 9,080 8 12 16 43 1 30 0.3 Kitchen sink 9,200 19 18,800 16 8 10 74 2 173 2 Laundry machine 7,900 16 20,300 17 35 49 316 10 4,790 40 Toilet 23,540 48 67,780 57 16 22 2,782 87 6,473 55 Total 48,690 100 119,410 100 73 100 3,224 i0oa 11,862 100, Source: Adapted from Laak (1974). a. Total percentage rounded to 100. contaminated relative to the clothing water than the coliforns and 326 fecal streptococci per 100 milliliters), total counts suggested. Hypes (1974) found that than those given in table 1-13 (Small Scale Waste coliform counts in sullage were about 1.9 x 107 per 100 Management Project 1978). milliliters irrespective of garbage content. After 24 Although data are lacking, it may be assumed that hours of storage, this count had increased to 5.4 x 108, sullage from bathrooms and laundries will contain indicating that sullage is a favorable medium for small numbers of any pathogenic viruses, bacteria, coliform growth. protozoa, or helminth eggs being excreted by the Available information on the microbiological people who use them. The washing of babies and their quality of sullage is very limited and neither of these soiled clothing may substantially raise the pathogen two data sets (Hypes 1974 and Witt, Siegrist and Boyle content of sullage. It is also possible that some bacteria 1974) may be representative. A more recent study in the find warm sullage a suitable medium for multi- USA reports lower bacterial counts in clothing wash plication. Data on the microbiological quality of water (215 total coliforms, 107 fecal coliforms and 77 sullage from the tropics might verify this possibility, fecal streptococci per 100 milliliters), and higher counts and its collection should be a priority of sanitation in bath water (1,810 total coliforms, 1,210 fecal research. Table 1-13. Bacterial content of sullage in the USA (per 100 milliliters) Total coliforms Fecal coliforms Fecal streptococci Geometric Geometric Geometric Sullage source mean Range mean Range mean Range Bath and shower water 1.100 70-(8.2 x 103) 220 1-(2.5 x 103) 44 1-(7 x 104) Clothing washwater 18,000 85-(8.9 x 105) 1,400 9-(1.6 x 104) 210 1-(1.3 x 106) Clothing rinsewater 5,300 190-(1.5 x 105) 320 35-(7.1 x 103) 75 1-(2.3 x 105) Source: Adapted from Witt, Siegrist and Boyle (1974). 20 HEALTH HAZARDS OF EXCRETA Sullage disposal and health But in areas of seasonal rainfall, and where the drains are liable to blockage and ponding, the addition of Theresal ar fiveind wastewofer sullptaglesdisposa casul sullage will create year-round standing water and thus disposal by tipping wastewater receptacles in the yard; errudClxbedn hr nysaoa garden watering on-site disposl by soakaway' year-round Culex breeding where only seasonal grardenageinto opendrain-siten draissal byto soakaw; breeding may previously have occurred. It is not, drains or sewers. Each of these has different health therefore, the quality of the sullage that poses a health drplicatinsornss. Each of these has different health risk, since ponded stormwater will also be sufficiently implications. Tipping in the yard may create breeding sites for polluted to allow Culex breeding, but the continuous insects such as Culex pipienis as well as muddy and addition of sullage to storm drains subject to ponding conditions close to the dwellings. Because it that converts wet season breeding into year-round unesanitaofery concealment, a clean, dry yard is less breeding. In this case the rise in Cutlex populations may does not offer concealment, a clean, dry yard IS less ledtinradfirassrnmsioadthso likely to be used by children for defecation, and any lead to increased filariasis transmored thus to worm eggs their feces might contain will be less likely to Aeme of isfect an be foundinearec mature (nematode eggs require a moist environment to develop).7 Sullage containing pathogens from babies' resurgence of Bancroftian filariasis as a major public bath water or adults' ablution water may also infect health problem in Egypt (Southgate 1979). Since children playing in the yard. In well-draining soils, approximately 1965 a complex of factors-including wheldren sulaynge p uion oard. hsIng w -deinsit oilslw, major changes in irrigation practice, a proliferation of where sullage production or housmig unliky to bewa poorly maintained water supplies, and inadequate tipping of sullage outside the home Is unlikely to be a exrt .dsoa faiite cotmntn.ufc excreta-dis osal facilities contaminating surface major health hazard. Where soils are less permeableg manr whereth wazaerd useore housine densis high, water-has increased C. pipiens breeding in parts of the a Nile Delta. Consequently, the prevalence, intensity, however, an adequate method of sullage disposal is and geographic spread of Bancroftain filariasis have essential. (It should be noted that high housing increased. It has also contributed to explosive densities are generally associated with poverty and epidemics of Rift Valley fever in Egypt during 1977 and thus with low water use and sullage production.) 1978 (Hoogstraal, Meegan and Khalil 1979). Sullage disposal by watering vegetable gardens near U the house is likely to create few if any health hazards, lrge-saleasulae sposal sinto oen rins whea provided that prolonged ponding of wastewater is prevented (to discourage mosquito breeding) and that tendency to blockage. Too often sullage makes its way children are dsuato streams by natural gullies, and no formally defined children are discouraged from defecating in or near the dang ytmeit.Teslto oteepolm gardens. Sullage disposal by soakaway provides a low . isae to usea. aTernative method pof lem riskof goundate conamintio; th ris of IS either to use an alternative method of sullage risk ogrudae cnaia . disposal or to prevent drains from blocking by microbiological groundwater pollution is much lower c with sullage than it is with sewage.' The same is true of g y g high nitrate pollution (as indicated in table 1-12, clear. The latter approach is the more realistic and ' labor intensive and can be Implemented by the sullage contains little nitrogen compared with sewage). empl oyent o nicia we bypsubcntractin Drainage of wastewater into open drains, perhaps temjobet ot privat sor,eor by sorgani inga into~ ~ ~ ~~~. str dris.rvdstems edl the Job to the private sector, or by organizing and into~~~~ str dris prvdstems.edl motivating community effort on a neighborhood basis. identifiable health risk, namely that of promoting the breeding of C. pipiens and other mosquitoes. In areas of Finally, sullage may be disposed of into a sewerage system, as is sewage, except that smaller-bore pipes are yer-ondrinal,str daiswilcotanwae used. This means of disposal raises no special health continuously. If they are kept free of garbage and are poems and onvnional ratment beforeadis well designed, the drains will flow freely and provide few sites for mosquito breeding, and the presence or charge or reuse should be highly effective. The load of absence of sullage will not affect community health pathogenic microorganisms in sullage will be small, so that discharge or reuse can take place without tertiary 7. Some of the classic studies on nematode infections tfor instance, treatment. Cort, Otto and Spindler 1930: Otto, Cort and Keller 1931: Otto and Spindler 1930; and Winfield 1937) suggest that, among households of similar socioeconomic status, the contamination ofthe yard by the Literature Cited feces of young children is associated with increased Ascarts prevalence and intensity in the family (see chapter 23). Balasegaram, M. and Burkint. D. P. ( 1976). Stool 8. See chapter 7. characteristics and Western diseases. Lancer, 1, 152. ELEMENTS AND HEALTH RISKS 21 Bennett, E. R., Linstedt, K. D. and Felton, J. T. (1974). Rural Amnerican Journal oj Clinical Altirition, 29, 1480-1484. home wastewater characteristics. In / '. ., of the Gray, H. and Tainter. M. L. (1941). Colloid laxatives National Home Sewage Disposal Symposimi, Chicago, Dec. available for clinical use, American Journal oj'Digestive 9-10, 1974, pp. 74-78. St. Joseph, Mich.: American Society Diseases, 8, 130-139. of Agricultural Engineers. Greenberg, C. J. (1976). Studies on the Fibre in Human Diets. Burkitt, D. P., Walker, A. R. P. and Painter, N. S. (1972). Ph.D. dissertation. Cambridge: University of Cambridge. Effect of dietary fibre on stools and transit-times, and its Hindhaugh, G. M. A. (1973). Nightsoil treatment. The role in the causation of disease. Lzancet, 2, 1408-1412. Consiulting Engineer, 37, 47 and 49. (1974). Dietary fiber and disease. Journal ot the Hoogstraal, H., Meegan, J. M. and Khalil, G. M. (1979). The American Medical Association, 229, 1068-1074. Rift Valley fever epizootic in Egypt. 1977-78: ecological Connell, A. M. and Smith, C. L. (1974). The effect of dietary and entomological studies. Transactionzs oJ the Royal fibre on transit times. In Proceedings of' the Fourth Society of Tropical Medicine and Hygiene, 73, 624-629. International Symposium on Gastrointestinal Motility, Huponu-Wusu, 0. 0. and Daniel, S. 0. (1977). Public health Banif, Alberta, 1973; eds. Daniel, E. E. and others, pp. aspects of housing in Nigeria: observations on the human 365-368. Vancouver: Mitchell Press. factors in refuse disposal in Lagos. Health and Hygiene, 1, Cort, W. W., Otto, G. F. and Spindler, L. A. (1930). 153-158. Investigations on Ascaris lumbricoides and the associated Hypes, W. D. (1974). Characterization of typical household intestinal helminths of man in southwestern Virginia. gray water. In Man nal of'Gray Water Treartment Practice, Anmerican Journal of Hygiene, 11, 1-55. ed. Winneberger, J. H. T., pp. 79-88. Ann Arbor, Mich.: Cranston, D. and Burkitt, D. P. (t975). Diet, bowel Ann Arbor Scicncc Publishers. behaviour and disease. Lancet, 2, 37. International Agency for Research on Cancer, Instestinal Crofts, T. J. (1975). Bowel-transit times and diet. Lancet, 1, Microecology Group (1977). Dietary fibre, transit time, 801. faecal bacteria, steroids, and colon cancer in two Crowther, J. S., Drasar, B. S., Hill, M. J., MacLennan, R., Scandinavian populations. Lancet, 2, 207-211. Magnin, D., Peach, S. andTeoh-Chan, C. H. (1976). Faecal Kalbermatten, J. M., Julius, D. S., Gunnerson, C. G. and steroids and bacteria and large bowel cancer in Hong Mara, D. D. (1982). Appropriate Sanzitation Alternatives: A Hong by socio-economic groups. British Journal of Planning and Design Manual. World Bank Studies in Cancer, 34, 191-198. Water Supply and Sanitation 2. Baltimore, Md.: Johns Drasar, B. S. (1974). Some factors associated with Hopkins University Press. geographical variations in the intestinal microflora. In Laak, R. (1974). Relative pollution strength of undiluted Nomnal Microbiological Flora of'Man, Society for Applied waste materials discharged in households and the dilution Bacteriology Symposium no. 3; eds. Skinner, F. A. and waters used for each. In Manual of'Grey Water Treatinent Carr, J. G., pp. 187-196. London: Academic Press. Practice, ed. Winneberger, J. H. T., pp. 68-78. Ann Arbor, Evison, L. M. and James, A. (1977). Microbiological criteria Mich.: Ann Arbor Science Publishers. for tropical water quality. In Water, Wastes and Health in McGarry, M. G. and Stainforth, J. (1978). Co0npost, Hot Clim71ates; eds. Feachem, R. G. A., McGarry, M. G. and Fertilizer, adl Biogas ProduLctionfrom Humnan and Farm Mara, D. D., pp. 30-51. London: John Wiley. Wastes in the People's Republic of China. Ottawa: Feachem, R. G. A. (1977). Environmental health engineering International Development Research Centre. as human ecology: an example from New Guinea. In Mata, L. J., Carrillo, C. and Villatoro, E. (1969). Fecal Subsistence and Survival-Rural Ecology in the Pacific, eds. microflora in healthy persons in a preindustrial region. Bayliss Smith, T. and Feachem, R. G. A., pp. 129-182. Applied Microbiology, 17, 596-602. London: Academic Press. Otto. G. F., Cort, W. W. and Keller, A. E. (1931). Feachem, R.,G. A., Burns, E., Cairncross, A., Cronin, A., Environmental studies of families in Tennessee infested Cross, P., Curtis, D., Khalid Khan, M., Lamb, D. and with Ascaris. Trichuris and hookworm. American Journal Southall, H. (1978). Water, Healthz and Development: An of Hygiene, 14, 156-193. Interdisciplinary Evaluation. London: Tri-Med Books. Otto, G. F. and Spindler, L. A. (1930). Effect of partial Fuchs, H.-M., Dorfman, S. and Floch, M. H. (1976). The sanitation on infestation with intestinal parasites in effect of dietary fiber supplementation in man. II. southwest Virginia. Southern Medical Journal, 23, Alteration in fecal physiology and bacterial flora. 556-560. American Journal oj Clinical Nuttritionz, 29, 1443-1447. Pescod, M. B. (1971). Wastewater solids utilization and Goldsmith, H. S. and Burkitt, D. P. (1975). Stool disposal in tropical developing countries. In W"ater Supply characteristics of black and white Americans. Lancet, 2, and Wastewater Disposal in Developing Cotuntries: 407. Proceedings of a Water Slupply and Sanitation Seminar. Gotaas, H. B. (1956). Compostinig: Sanitary Disposal anid Bangkok, January 19-23, 1970, eds. Pescod, M. B. and Reclamation of' Organic Wastes. Monograph Series 31. Okun, D. A., pp. 208-226. Bangkok: Asian Institute of Geneva: World Health Organization. Technology. Goy, J. A. E., Eastwood, M. A., Mitchell, W. D., Britchard, J. Pradt, L. A. (1971). Some recent developments in nightsoil L. and Smith, A. N. ( ! r., Fecal characteristics contrasted treatment. Wl'ater Research, 5, 507-521. in the irritable bowel syndrome and diverticular disease, Small Scale Waste Management Project (1978 ). Management 22 HEALTH HAZARDS OF EXCRETA oJ Small Waste Flows. Report EPA-600/2-78-173. diseases in North China. III. Family environmental factors Cincinnati, Ohio: US Environmental Protection Agency. affecting the spread of Ascaris lumbricoides in a rural Southgate, B. A. (1979). Bancroftian filariasis in Egypt. population. Chinese Medical Journal, 51, 643-658. Tropical Diseases Bulletin, 76, 1045-1068. Winneberger, J. H. T. (1974). Manual oJ Gray Water Treat- Tandon, R. K. and Tandon, B. N. (1975). Stool weights in ment Practice. Ann Arbor, Mich.: Ann Arbor Science North Indians. Lancet, 2, 560-561. Publishers. Walker, A. R. P. (1975). Effect of high crude fiber intake on Witt, M., Siegrist, R. and Boyle, W. C. (1974). Rural transit time and the absorption of nutrients in South household wastewater characteristics. In Proceedings of African Negro schoolchildren. American Journal of the National Home Sewage Disposal Symposium, Chicago, Clinical Nutrition, 28, 1161-1169. December 9-10, 1974, pp. 79-88. St. Joseph, Mich.: White, A. U. (1977). Patterns of domestic water use in low- American Society of Agricultural Engineers. income communities. In Water, Wastes and Health in Hot WHO (1970). Sewerage Planning in the Greater Taipei Area: Climates, eds. Feachem, R. G. A., McGarry, M. G. and A Master Plan Report, Report no. Mara, D. D., pp. 96-112. London: John Wiley. WHO/UNDP/SF/CHA-27. Geneva: World Health White, G. F., Bradley, D. J. and White, A. U. (1972). Drawers Organization. of Water: Domestic Water Use in East Africa. Chicago: (1979). Human Viruses in Water, Wastewater and Soil. University of Chicago Press. Technical Report Series no. 639. Geneva: World Health Winfield, G. F. (1937). Studies on the control of faecal-borne Organization. 2 Environmental Classification of Excreta-related Infections VARIOUS DISEASES are related to excreta, and the environment, and the infective dose for humans-and engineer, administrator, and community development these and other key concepts are discussed before the worker cannot consider each disease separately in environmental classification is set forth. selecting improved excreta disposal technologies. Rather, a conceptual framework that links various kinds of excreta-related infections to the design and Understanding Excreta-Related implementation of particular disposal or reuse Infections technologies is required. Yet a biological classification grouping the excreted viruses, bacteria, protozoa, and Excreta may be related to human disease in two helminths may be less helpful to understanding the ways (figure 2-1). The agents of many important health aspects of alternative approaches to excreta infections escape in the body's excreta eventually to disposal than a classification of infections based upon reach others-the first means of relation-and these transmission routes and life cycles. Such a classification are "excreted infections." In some cases the reservoir of would be an "environmental" one. In fact, the infections escape in the body's excreta eventually to resemblance between a biological and an en- Because such infections cannot be controlled through vironmental classification is much closer in the case of changes in human excreta disposal practices, this study the excreta-related infections than in the case of the does not examine them. (A number of infections for water-related infections (see Bradley 1977). which both man and other animals serve as a reservoir, The purpose of an environmental classification is to however, have been included.) group infections in such a way that the efficacy of The second way in which excreta relate to human different preventive measures is made clear. An disease is through the insect breeding that waste environmental classification for the water-related disposal often encourages. Insects may be a nuisance in infections has already been proposed (Bradley 1977; themselves (as are flies, cockroaches, mosquitoes), but Feachem, McGarry and Mara 1977); the object here is they may also mechanically transmit excreted pa- to propose an environmental classification for the thogens either on their bodies or in their intestinal infections associated with excreta. The devising of such tracts (as do cockroaches and flies), and sometimes a classification encounters two major limitations. The first is that remarkably little is known precisely about (a) Infected excreta the transmission of several of these infections and the numbers of microbes needed to pass on the infections New infections to susceptible people. The second is that the bulk of the excreted viruses, bacteria, and protozoa differ quanti- (b) Excreta - Vector breeding/ tatively rather than qualitatively in their transmission Figure2-1. Thelinksbetweenexcretaandinjkction.In characteristics, making it easy to end up with a large, (a), the excreta themselves contain the pathogens which relatively uninformative category containing the may be transmitted by various routes to a new host. In majority of infections. Understanding these infections (b), the excreta (or sewage) permits the breeding of depends on some basic facts of transmission- certain flies and mosquitoes that may act as vectors of especially latency, persistence of pathogens in the excreted and other pathogens 23 24 HEALTH HAZARDS OF EXCRETA they may be vectors for pathogens that circulate in the blood (as are mosquitoes). The capacity of flies or Excreted load Lrtency Excreted loadPersistence -*-Infective dose cockroaches to serve as mechanical vehicles for lictlon excreted pathogens represents one of the many ways in which excreted disease agents are transmitted from anus to mouth. Careful disposal of human wastes, Figure 2i2 Fctors un1 'r the transmissio n of a precautions in food storage and handling, and controlfectiLe dose measures directed against flies and cockroaches would minimize the threat to health of these pests. The blood- feeding nature of the mosquito, however, poses a more Ex-creted load complex problem. The mosquito ingests agents of the diseases it transmits through biting already infected The concentration of pathogens passed by an persons and perpetuates the cycle of infection to new infected person, or excreted load, varies widely. A hosts by the same means. The pathogens it carries are person infected by a small number of nematode worms, therefore nonexcreted, and the concepts discussed in for instance, may pass only a few eggs per gram of feces, this chapter have little relevance; the important factors whereas a cholera carrier may excrete 106 vibrios per are those which determine the breeding habits of those gram, and a patient with an acute attack of cholera particular mosquito vectors that breed in sewage or may pass 1013 vibrios in a day. In areas where large sullage.' numbers of pathogenic organisms are being passed in The distinction between the state of being infected the feces, high pathogen concentrations in sewage are and the state of being ill must be kept in mind in common (see table 1-10). Even in a developed, considering the transmission of excreted infections. temperate country such as England, where water use is The most important segment of the population relatively high and salmonellosis relatively rare, raw involved in transmitting an infection frequently shows sewage may contain 104 salmonellae per liter. At these few or no signs of disease; conversely, individuals in concentrations a removal efficiency of 99 percent in advanced states of disease may be of little or no sewage works will still leave 102 pathogenic organisms importance in transmission. Schistosomiasis is a good per liter of effluent. The health implications of these example: as much as 80 percent of the total egg output in pathogens will depend upon the effluent disposal feces and urine reaching water from a human method, the pathogens' ability to survive or multiply. population may be produced by children 5 to 15 years and the infective dose required. old, many of whom will show minimal signs of disease. Conversely, middle-aged people in terminal stages of schistosomiasis may produce few or no viable LatencY schistosome eggs. If an excreted infection is to spread, an infective dose Latency is the interval between the excretion of a of the disease agent has to pass from the excreta of a pathogen and its becoming infective to a new host. patient, carrier, or reservoir of the infection to the Some organisms-including all excreted viruses, mouth or some other entryway of a susceptible person. bacteria, and protozoa-have no latent period and are Spread will depend upon the numbers of pathogens immediately infectious in raw excreta. The require- excreted, upon how these numbers change during the ments for the safe disposal of excreta containing these particular transmission route or life cycle, and upon agents are different from those for helminthic infections the dose required to infect a new individual. Infective which have prolonged latent periods. Latency can dose is in turn related to the susceptibility of the new affect the choice of disposal systems: infections that host. Three key factors intervene to govern the have a considerable latent period are largely risk free in probability that, for a given transmission route, the carted night soil, whereas the others constitute a major numbers of excreted pathogens (excreted load) from health hazard in fresh night soil. In the environmental one host will form an infective dose for another: classification that follows, therefore, the first two latency, persistence, and multiplication. These concepts categories, in which no latency is observed, are will be discussed in turn; their relation is expressed in separated from the remaining categories, in which a figure 2-2. definite latent period occurs. 1. See category \i in the next main section of this chapter. The Among the helminthic infections (see table 1-9), only relation of insects to excreta and disease is examined in detail in three have eggs or larvae that may be immediately chapters 36 and 37. infectious to man after being passed in the feces. These ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 25 are the pinworm (Enterobius vermicularis), a dwarf bacterial infections. This may determine the usual tapeworm (Hylnenolepis uiana), and occasionally a mode of infection, since multiplication in water is rare minute nematode ( -i. 1. stercoralis). All the and limited compared with the massive increases other excreted helminths require a distinct latent possible in food. Excreted viruses and protozoa do not period, either because their eggs must develop into an multiply outside their animal hosts. infectious stage in the environment outside the body, or Among the helminths transmitted by excreta, all the because these parasites have one or more intermediate trematodes infecting man undergo multiplication in hosts through which they must pass in order to complete aquatic snails. This aquatic stage in their life cycles their life cycles. introduces a prolonged latent period of a month or more while the trematodes develop in the snail, Persistenice followed by an output to the environment of up to several thousand larvae for each egg reaching the Viability of the pathogen in the environment, or water. (Category v of the environmental classification persistence, is a measure of how quickly it dies after below contains infections of this sort.) leaving the human body. This single property is the most indicative of the fecal hazard: a highly persistent Infective dose pathogen will create a risk throughout most treatment processes and during the reuse of excreta. In a predictable world the assessment of health risk A pathogen with short persistence outside the body, could simply be calculated from the output of however, must rapidly find a new, susceptible host. pathogens in the excreta of those infected, the median Transmission, therefore, cannot follow a long route infective dose (ID,O) of particular organisms, and the through sewage works and the final effluent disposal efficiency of excreta treatment processes in inactivating site back to man, but will rather involve the family or pathogens. Because of the variable infective dose of other close group, within which infection is transferred most pathogens and the uneven distribution of from one person to another through lax personal infection in the environment, the real world is much cleanliness. More persistent organisms, in contrast, can less calculable than this. Although the minimal readily generate new cases of disease much farther infective dose for some diseases may be a single afield. As persistence increases, so then must concern organism, or very few, the doses required in most for the ultimate means of excreta disposal. Similarly, bacterial infections are much higher. Data on infective pathogens that tend to persist in the general doses are very hard to acquire, since they involve environment will require more elaborate processes to administering a known dose of a pathogen to a human inactivate them in a sewage works. Methods of volunteer. Information is scanty and concerned with sequestering these pathogens, such as sedimentation doses required to infect half those exposed (ID50), into a sludge for special treatment, are often needed. rather than a small proportion, at a single exposure. Measurement of pathogen persistence in a labo- The volunteers generally have been well-nourished ratory is easy. Laboratory results, however, need adults usually from non-endemic areas. Results of this confirmation by field studies which are more difficult. kind must therefore be applied with great caution to Interpreting field results on persistence requires malnourished peasant children continually exposed to knowledge of how many pathogens are being shed in a an infection. It has been found that changes in the community's excreta (relatively easy to determine) and manner of administering experimental doses, such as the infective doses for man (extremely difficult). preceding a dose of cholera vibrios with an alkaline substance to reduce temporarily free gastric acid. may Multiplication lower the tD50 of such organisms by a factor of 103 (Hornick and others 1971). And, although ID50 may be Under favorable conditions certain pathogens will the most reliable gauge of infectivity in human multiply in the environment. Originally low numbers experimental studies, in natural transmission the can thus produce a potentially infective dose (see the infective dose for 5 percent or less of the population next section). Bacteria may multiply on a favored may be of greater epidemiological significance. substrate (for instance, Salmonella on food) and Uncertainty over the size of the minimal infective trematode worms multiply in their molluscan in- dose in nature makes it a difficult criterion to use in termediate hosts. In the former case, light fecal devising a classification; nevertheless, it is too contamination may increase bacterial numbers to the important to be left out. The difficulties are greatest high minimal infective doses required in many excreted with the major excreted bacterial infections and with 26 HEALTH HAZARDS OF EXCRETA protozoa. For excreted viruses there is evidence of low and disease is limited to a few of the youngest children, ID,0s in the laboratory, and in human populations who may suffer chronic paralysis. If sanitation is (World Health Organization 1979). In helminthic improved, infection is deferred to later in life, when its infections a single egg or larva can infect if ingested, pathological consequences are more serious. Thus, even though a high proportion of worms can fail to although poliovirus transmission may be reduced by mature (especially in locations where immunity is improving sanitation, improvements will not neces- present). sarily curtail the disease, a result achieved in practice by immunization. This pattern may also apply to other excreted infections such as infectious hepatitis, and it Host response has been proposed for typhoid. There are several other Host response is important in determining the effect excreted infections, however, in which human im- once an individual has received a given dose of an munity is of importance in regulating the amount of infectious agent. Acquired immunity, and the relation disease. Immunity tends to diminish the health of age to pathology, are particularly important in significance of moderate sanitary improvements, and predicting the effects of sanitation. At one extreme may in part explain the disappointing effects of some would be infection with a short-lived parasite to which sanitary programs (table 2-1).2 little immunity develops and for which the relation In other words, the balance between exposure to between infection and disease is not age dependent. A infection and host response to it will determine the close, almost linear relationship between exposure and pattern of the excreta-related disease. If transmission, disease might be expected in this case, with appropriate creating exposure to a particular infection, is limited, improvements in sanitation yielding health benefits then most people will not have encountered the proportional to effect. Ascaris closely approximates infection and will be susceptible. If a sudden increase in this model. transmission of the disease occurs, it will affect all age At the other extreme would be infection with viruses groups in the form of an epidemic. Under these or bacteria to which long-lasting immunity develops circumstances improvements in sanitation that strike and for which the chance of overt, symptomatic disease at pathogen transmission will have a considerable in those infected rises with increasing age. An example of this case is infection with poliovirus (see table 1-5). Under poor sanitary conditions all persons are infected 2. See also chapter 3 for a detailed discussion of the health benefits at a young age, older children and adults are immune, from improvements in sanitation. Table 2-1. Summary of selected literature on the effect on health of imnprovled excreta disposal Country and type of study Finding Source Brazil In a village of 1,041 inhabitants, a socioeconomic From 1961 to 1968, Schistosoma mansoni Barbosa, Pinto and Souza and schistosomiasis survey in 1961 was prevalence rates fell from 7 to 0 percent among (1971) followed by introduction of schistosome control 0-4 year olds, from 27 to 4 percent among 5-9 measures, including latrines, water supplies, year olds and from 56 to 9 percent among laundry facilities, showers and health education. 10-14 year olds. The prevalence of S. mansoni Fecal surveys were carried out in 1961, 1966, infection in domestic rodents and snails also fell 1967 and 1968. Other villages without these considerably. The cost of the control measures interventions were surveyed in 1963 and 1969. was US$0.98 per month per protected person over 7 years. Colombia 15 municipal primary schools in a poor suburb of Diarrhea and vomiting were more common Koopman (1978) Cali were visited and 8,444 schoolchildren were among children in schools with lower hygienic interviewed. The school's toilet facilities were scores. The individual factors most associated inspected and the children were asked if they with diarrhea prevalence were feces in the toilet had had diarrhea, vomiting, colds or headlice bowl, and an absence of toilet paper, towels, over the past week. The observations of toilet soap or taps for hand washing. Hygienic scores facilities were used to compute a "hygienic were not related to colds or headlice, and score" for each school. classroom crowding was weakly related to vomiting, colds and headlice. ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 27 Table 2-1 (continued) Country and type of study Finding Source Costa Rica Diarrheal morbidity, intestinal bacteria, parasites, Ascaris prevalence decreased as the type of Moore, de la Cruz and Vargas- quality of water, meat and milk and the fly excreta disposal improved. Trichuris prevalence Mendez (1965) population were surveyed among 1,202 houses. was the same among individuals with or Three types of excreta disposal facility were without a latrine but was lower among distinguished: none (12 percent of houses), pit individuals having a septic tank. Shigella latrine (76 percent of houses) and flush toilets organisms were not recovered where a septic with septic tanks (12 per cent of houses). tank was present. Diarrhea morbidity was least amongst those living in houses with no latrine. Excreta disposal facility was not associated with protozoal prevalence. An outbreak of 167 cases of infectious hepatitis Infectious hepatitis cases occurred in 1.6 percent Villarejos and others (1966) was investigated between December 1963, and of houses with a flush toilet, 2.7 percent of July 1964. The outbreak occurred during a houses with an outdoor latrine and 2.6 percent severe drought. Person-to-person contact was of houses with no facility. considered the likely mode of spread. Egypt Surveys were made in 1952 of helminthic and Protozoal prevalence rates and the mean number Chandler (1953 and 1954) protozoal infections in two neighboring of protozoal infections per person were not villages: A and B. Village A had been surveyed reduced in Village A. Ascaris and hookworm in 1950. Village A had improved water supply, prevalence rates and intensities were reduced. a borehole latrine in 90 percent of houses, a refuse collection service and visiting nurses. Village B was untouched. Prisoners used bucket latrines and treated Nile Schistosomiasis and hookworm prevalences in the Khalil (1931) water. Nearby villagers had no latrines and local population were approximately 75 percent used untreated Nile water. Parasite infections and 70-88 percent respectively. Among of the villagers were compared with those of prisoners, the rates fell from 30 percent and 68 the prisoners after various periods of percent respectively to less than 20 percent in incarceration. both cases after 5 years of incarceration and to about 10 percent after 12 years. Reinfection with Ascaris occurred regularly owing to contamination of sewage-irrigated vegetables. Various combinations of latrines and drug Latrines had no impact on Ascaris, hookworm or Scott and Barlow (1938) therapy were investigated in villages for 6 years schistosome infections. from 1928. Various combinations of water supply, latrines, The installation of water supply and latrines did Weir and others (1952) refuse disposal, fly control and therapy were not alter the infant mortality or crude death investigated in 5 villages during 1948-51. rates and did not change the fly status in any of the villages. Guatemala Acute diarrheal rates among families having a In those families having a latrine, diarrheal rates Gordon and others (1964) latrine were compared with rates amongst were somewhat lower for those over 2 years those with no latrine. old, but not for those under 2. Two lowland villages were studied during The results of this study have not yet (mid-1981) Schneider, Shiffman and 1973-76. In-house water supply and sanitary been fully published. Preliminary reports Faigenblum (1978); Shiffman education were implemented in one village; the indicate that malabsorption was somewhat and others (1979) other village provided a control. lower in the intervention than the control village, that there were no differences in overall diarrhea incidence but that there was less diarrhea among 2-7 year olds in the intervention than the control village. 28 HEALTH HAZARDS OF EXCRETA Table 2-1 (continuied) CountrY and type of study Finding Source 'itzdti The impact of a bored-hole pit latrine and health The authors state that the invervention was Kumar. Sehgal and Singh (19701 education program on the incidence of diarrhea related to "a declining trend in diarrhoeal in children in the village of Bharwara, near morbidity", but the data presented do not Lucknow, was investigated. support this. A single stool examination on 13.267 hospital The prevalence of Eniroinoehu histolytica excretion Mathur and Kaur (19721 patients and their contacts was carried out at among those living in homes with no latrines Karnal. Haryana State. A sanitary inspector (38.3 percent) was a little higher than for those was sent to the homes of the patients to collect using latrines j31.6 percent) (p<.01). The information on hygiene and domestic facilities. authors point out that this difference cannot necessarily be attributed to the latrines. Iran Impact of mass treatment, sanitation and Mass treatment was highly effective tn reducing Arfaa and others (19771 sanitation plus mass treatment on soil- both the prevalence and intensity of transmitted helminths was studied in 15 villages Aclcylostonia and Ascaris. Sanitation, added to in southwest Iran. Sanitation was one pit mass treatment, contributed nothing. Sanitation latrine per family and a communal water atone had an impact upon the intensity of both supply. hookworm and roundworm and had a little impact on the prevalence of roundworm only. Ascariasis was studied in a village of 850 people The prevalence of infection fell from 67 percent to Sabba and Arfaa 11967) in southwest Iran before and after the 57 percent over the study period (February construction of a water supply, a public bath- 1963 to December 1965J. Mean egg output fell house, a laundry and 114 pit latrines (nearly from around 11 per milligram of feces to 4. The one for every household). pit latrines cost US$0.5 per capita and were the major cause of the reduced ascariasis. Japan A program of heat treating (with firev-ood) of The prevalence of hookworm and A.scori.s Katayama (19551 night soil (up to 601C) prior to agricultural declined "strikingly" in the intervention village application was implemented in a village in and there was a marked decrease in the count Shiga Prefecture. A control village was left of Ascaris eggs found in the soil. These changes untouched. were not observed in the control village. Heat treating of night soil (with surplus night Night soil treatment alone had only a slight effect Kawagoe and others (195S) electricity) was implemented in a village near on the prevalence of parasite infections. When Osaka city. mass chemotherapy was carried out. prevalences fell markedly (hook"orm from 52 percent to 11 percent, Ascaris from 33 percent to 12 percent) and remained at this low level throughout the 5 month observation period. Night soil treatment with thiabendazole was The prevalence of ascariasis fell by 50 percent in Kutsumi 11969) implemented in a village of 5,000 people near Area A, by 30 percent in Area B and hardly at Tokyo. Three areas were distinguished: Area A, all in Area C. The rate of new infections with night soil treatment + chemotherapy: Area B. Tricltris was one-third. and that of hookworm night soil treatment only; Area C. was one-half in Area A compared with Area C. chemotherapy only. Parasite prevalence was surveyed between July 1964 and March 1966. Alucufritius Diarrheal rates in households with differing Compared with families with an indoor toilet, van Zijl (1966) sanitation facilities were studied in 1960, families with an outdoor toilet had 4 times the diarrhea incidence and families with no toilet had 10 times the diarrhea incidence. Pauoi lest A series of egg counts were made in two villages. Reinfection after mass treatment was rapid, but Cort, Schapiro and Stoll (1929) one partially sanitated and the other entirely reinfection with hookworm was delayed in without latrines, before and after mass those groups with more and better maintained chemotherapy. latrines. ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 29 Table 2-1 (continued) Country and type of study Finding Source Panama (cont.) Children presenting at a clinic in Panama City The three pathogens were absent from children Kourany and Vasquez (1969) were examined for excretion of coming from the best housing type, whereas for enteropathogenic Escherichia coli. Shigella and other housing types, about 8 percent of Salmonella. These data were related to children had one or more of the pathogens in information about type of housing and sanitary their feces. facilities. Surveys were conducted over 7 years into In villages without latrines, the prevalence and Sweet and others (1929) environmental conditions and helminthiases. intensity of hookworm rose to, or above, original levels within 3 or 4 years after a mass drug campaign. In villages with latrines, prevalence and intensity also rose again following drug treatment but a degree of protection against reinfection was observed among women. Philippines A region with endemic cholera was divided into 4 The apparent reductions in cholera incidence Azurin and Alvero (1974) areas: Area A, control area having poor water were 73 percent in Area B, 68 percent in Area and sanitation facilities; Area B, improved C and 76 percent in Area D. water supply; Area C, pour-flush pit latrines; Area D, improved water supply and communal latrines. Singapore 159 families living in modern flats and 169 Ascaris, hookworm and Trichuris prevalence rates Kleevens (1966) families living in squatter housing were studied. were 9, 1 and 28 percent, respectively, among The people in the flats had previously lived in flat dwellers and 63, 2 and 58 percent among the squatter housing but had been rehoused squatters. The high Trichuris prevalence among following a fire in 1961. Average family income flat dwellers was attributed to the longevity of of flat dwellers was S$165 per month whereas this worm. for squatters it was SS130 per month. Stool samples were collected from all children under 13 years old in the selected households. St. Lucia A longitudinal study of 229 children in three Children in the valley with improved water and Henry (1981) valleys. Weights and heights were recorded the valley with improved water and latrines had monthly; stools were examined for worm eggs less ascariasis. trichuriasis and diarrhea, and every 6 months, and parents kept diarrhea grew better, than children in the valley with no diaries for their children. The children were 0-6 improvements. months old at the start of the study and were followed for 2 years. Sudan Diarrhea incidence in households with differing In one particular month, families having a van Zijl (1966) sanitary facilities were studied in 1961. communal unsanitary privy experienced a higher diarrheal morbidity rate than similar families having no toilet. Union ol Soniet Socialist Republics A village of 1,600 people was studied before and Before the intervention, the prevalence of Ascasis Rosenberg (19601 after the abolition of untreated night soil as a eggs was 100 percent in soil samples and 71 fertilizer and a campaign of "improving general percent in fruit samples. 41 percent of soil eggs hygiene." and 19 percent of fruit eggs were viable. After the intervention, 35 percent of soil samples and 25 percent of fruit samples contained eggs. No eggs were viable. 30 HEALTH HAZARDS OF EXCRETA Table 2-1 (continued) Country and type of study Finding Source United States 400 patients at a veterans' hospital in Georgia The overall prevalence of infection with Brooke, Donaldson and Brown had stool examinations for intestinal protozoa Entamoeba histolytica was 9.3 percent. Among (1954) and helminths, and completed questionnaires those not infected, 22 percent had outside on their military service and living conditions. toilets, whereas among those infected, 55 percent had outside toilets (p <.01). Income was not significantly associated with Ent. histolytica infection. A survey of 357 people in 4 areas near Little The overall prevalence of infection with one or Brooke and others (1963) Rock, Arkansas, was carried out in 1961. Stools more protozoon (APR) was 33 percent. Among were examined for intestinal protozoa. all individuals served with piped indoor water supply the APR was 31 percent, whereas among those using well water it was 35 percent (no significant difference). However, among 0-4 year old piped water users the APR was 13 percent, whereas among 0-4 year old well- water users it was 37 percent (p<.05). Many of the houses with piped water also had sewerage, whereas well-water houses had septic tanks or outside pit latrines. 2,657 people living in a rural area of West Entamoeba histolytica and Ascaris prevalence Eyles, Jones and Smith (1953) Tennessee were surveyed for intestinal parasites. rates were 19 and 8 percent, respectively, 90 percent were black. Details of family size, among those with clean latrines, 36 and 11 cleanliness, housing, water supply and excreta percent among those with dirty latrines, and 29 disposal were also collected. and 15 percent among those with no latrines. Parasite prevalence was also found to be associated with family size, fecal contamination of the premises, cleanliness of house and person but not with water pollution. A survey of shigellosis among children under 10 The prevalence rates of Shigella excretion were 1.6 Hollister and others (1955) years old in farm labor camps in California was percent in cabins with inside water, shower and conducted. toilet, 3.0 percent in cabins with inside water but shared shower and toilet facilities, and 5.8 percent in cabins with all services shared. White females (age 18-76 years) at a mental The percentage of people infected with Ent. Jeffery (1960) institution in California were studied during histolytica and Giardia lamblia rose steadily 1954-57. They were originally housed in an old during the survey, indicating that transmission building in which standards of sanitation were was continuing throughout the period. poor. They were then rehoused in a new, However, although the percentage of people modern hospital building with excellent infected with hookworm (73 percent) and sanitary facilities. Stool examinations were Trichuris (83 percent) remained constant, as made on 110 patients prior to rehousing and would be expected in the absence of mass on 8 subsequent occasions. chemotherapy, no new cases of hookworm and only 3 new cases of Trichuris were reported while the patients were in the new building. Thus, the move to the new building interrupted the transmission of the helminths but not the protozoa. ln 1952 a program of borehole latrines was The latrine program was associated with a McCabe and Haines (1957) implemcnrted in Boston, Georgia. The reduction in the detection of Shigella from prevalence of Shigella excretion, in Boston and rectal swabs from 4.7 percent to 2.8 percent. control towns, was surveyed in children under Rates in control towns did not fall over this 10 years old. period. ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 31 Table 2-1 (continued) Country and type of study Finding Source United States (cont.) Excretion of Entamoeba histolytica among 1,115 Ent. histolytica prevalence rates were 6 percent for Mackie and others (1956) urban school children in North Carolina was those with an inside flush toilet, 12 percent for studied. These data were related to excreta those with a shared flush toilet and 58 percent disposal, water supply and garbage disposal for those with a pit latrine. Infection with Ent. facilities in the homes of the children. histolytica was also associated with type of water supply and garbage disposal facilities. Hookworm and Ascaris surveys were conducted The introduction of pit privies in the Otto and Spindler (1930) in Virginia. mountainous areas of Virginia was effective in reducing the hookworm prevalence, but not Ascaris. Environmental studies were made of 329 families Ascaris and Trichuris infections were confined Otto, Cort and Keller (1931) in the mountain region of Tennessee and 202 largely to the mountain areas. Yard pollution. families living in the central basin, western and with it heavy Ascaris infection, were plains and lowlands of the state. present regardless of the presence or absence of latrines. Studies were conducted in 11 mining camps in Shigella and Ascaris prevalence rates were 1.1 and Schliessmann and others (1958) eastern Kentucky from 1954 to 1957. Reported 7 percent, respectively, among those with water diarrheal disease rates, Shigella isolations from and flush toilet inside, 2.4 and 25 percent rectal swabs of pre-school children and parasite among those with water inside and latrine prevalence were investigated. outside, and 5.9 and 42 percent among those with water and latrine outside. Shigella infection data from 28,000 rectal swabs The rates of new Shigella infections occurring Stewart and others (1955) were analysed according to the type of housing. during the study period were: Housing was divided into 4 categories (poor, 6.2 percent among those in "poor" houses, fair, good, very good) according to water 2.2 percent among those in "fair" houses, supply, excreta disposal, fly population and 0.6 percent among those in "good" houses and esthetic and structural quality. 0.3 percent among those in "very good" houses. Note: The limitations of the literature on health benefits from sanitation and the difficulties in assessing these benefits are discussed in chapter 3. effect in reducing an epidemic's likelihood and its and of water supplies, and poliomyelitis, which can be magnitude if one occurs. prevented only by immunization. By contrast, if transmission is vigorous, most people The consequences of a disease's juvenile will be repeatedly exposed to an infection, having first prevalence-not only that children chiefly suffer, but acquired it in childhood. Subsequent exposures may be also that children are the main sources of infection- without effect if immunity is developed after the first presents a further challenge to sanitation. The acute attack, or immunity may develop cumulatively from a need for better community excreta disposal must focus series of attacks. The infection will nevertheless always on young children, the group perhaps least inclined to be present, and can be described as endemic. Under use any facilities that are made available. these conditions much of the transmission is ineffective because of human acquired immunity, and reduced transmission through improved sanitation will only Nonhuman hosts delay the occurrence of infection somewhat, so that older children exhibit symptoms. Extensive sanitary Some excreted infections (for example, shigellosis) improvements will either render the infection rare or, if are confined strictly to humans, and the control of the disease was originally highly transmitted, make it human excreta alone is required for their prevention. an adult disease. Diseases exemplifying this state of Many others (for example, salmonellosis) involve wild affairs are typhoid, which can be completely prevented or domestic vertebrate animals as well as man. Such an in a community by adequate management of excreta infection is called a zoonosis. 32 HEALTH HAZARDS OF EXCRETA Zoonoses infective dose, persistence, multiplication, and trans- mission. Further data on specific excreted pathogens- A,1n/ma/s arranged by category and epidemiological feature- g > Animal are provided in table 2-3.3 Control measures in parallel appropriate to each environmental category of pathogen are indicated in table 2-2, and data on immunity and pathogen concentrations in excreta, Aoimcs \which vary with each organism, are contained in table Animal 2-3. in There is a clear difference between the first five series categories of excreted pathogens and the last, which Man contains exereta-breeding insect vectors of disease, in Figure 2-3. Involvement of other vertebrates it? that the insects themselves are not pathogens and that a transmission oj human excreted inJections. Examples of variety of sanitation methods and additional specific zoonoses in parallel are salmonellosis and balan- measures can be directed against these vectors. For tidiasis; examples of zoonoses in series are beef and these reasons category vt Is not Included in table 2-3. pork tapeworm infections The excreted infections are divided on the basis of There are two groups of zoonoses, and each has the presence (categories in to v) or absence (categories quite different implications for sanitation (figure 23). and II) of a latent period (health problems associated In the first group, animals act as hosts alternative to with fresh feces or night soil occur primarily in these first two categories). The distinction between cate- man: even If human excreta IS under completely safe gre adI n aeoisH oVi udmna n control, the excreta of other animals can continue to gories i and II and categones iii to v IS fundamental and transmit the infection. In effect, the animal involved is clear-cut, correspondig closely to the biology f th 'in parallel" with man, and it is necessary to control pathogens (in that all infections in categories jn to v are both human and animal excreta. In the second group. helminthic). The subdivisions of the infections having latency are the animal is an essential step in the transmission of the disease from one human to another (figure 2-3, "in also clear, with category III containing the soil- series"). In this case control of either human excreta transmitted worms, Iv the tapeworms, which depend alone or the animal infection alone will suffice to end on the access of cattle and pigs to human feces, and v transmission. In the environmental classification the trematodes and other worms requiring aquatic below, this second group which contains the human intermediate hosts. The subdivision of categories I and tapeworm of. the genus Taenia,is therefore separated II, however, is difficult and somewhat arbitrary because tapeworm s of ther tgreus Thenia,is therefore separated the various concepts discussed above can arrange the from the other categories. ~infections of these categonies in different ways. If Some excreted helminthic infections have in- categories anddffarctgwy catgores an 11arcdivided, for instance, on thc basis vertebrate intermediate hosts (see table 1-9); they will ofies Ith th gre limitatinstof the bdata be controlled if excreta are prevented from reaching on iti doe kept inimind, the aprimate the intermediate hosts, or the intermediate hosts are on infective dose kept in mind, the approximate controlled, or if people do not eat the intermediate host ranking of pathogens (in order of increasing ID50) uncooked . do not. have contact with thewaterin shown in table 2-4 emerges. But if the infections are unicoohed ontermedoothe ontact withs thepen g wather listed in the order of increasing persistence outside whrtichlar thegintermediae hoste) l .(dependingonth their animal host, the approximate ranking shown in table 2-5 is appropriate. Another important factor in Categories of Excreta-related Infections predicting the effects of improved exereta disposal facilities is whether or not a significant nonhuman There are several ways in which the excreted reservoir of infection (see figure 2-3) exists for a infections can be grouped according to the epide- miological features discussed above, but a 3. Part Two of the book is devoted to detailed analyses of classification that considers the effects of excreta individual pathogens and diseases according to these and additional disposal and changes in disposal facilities and environmental factors. But it was thought that, for easier reference, technologies has been chosen, and is given in table 2-2. Part Two should group the pathogens by kind and not by the categories described in this chapter. Part Two is divided into section Six categories of infection have been distinguished In ............ L the excreted viruses; section II, the excreted bacteria, section III, the table, and the relevant environmental or epidemio- the excreted protozoa: section IV, the excreted helminths; and logical features broadly considered are latency, section V, the exereta-breeding insects and the diseases they transmit. ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 33 Table 2-2. Environmental classification of excreted infections Category and Emnironmental Major control epidemiological ftatures3 Infection transmission Jbcus measure t. Non-latent; low Amebiasis Personal Domestic water supply infective dose Balantidiasis Domestic Health education Enterobiasis Improved housing Enteroviral infections' Provision of toilets Giardiasis Hymenolepiasis Infectious hepatitis Rotavirus infection n. Non-latent; medium or Campylobacrer infection Personal Domestic water supply high infective dose; Cholera Domestic Health education moderately persistent; Pathogenic Escherichia Water Improved housing able to multiply coli infection' Crop Provision of toilets Salmonellosis Treatment of excreta Shigellosis prior to discharge Typhoid or reuse Yersiniosis iii. Latent and persistent; Ascariasis Yard Provisions of toilets no intermediate host Hookworm infectiond Field Treatment of excreta Strongyloidiasis Crop prior to land Trichuriasis application iv. Latent and persistent: Taeniasis Yard Provision of toilets cow or pig as Field Treatment of excreta intermediate host Fodder prior to land application Cooking, meat inspection v. Latent and persistent; Clonorchiasis Water Provision of toilets aquatic intermediate Diphyllobothriasis Treatment of excreta host(s) Fascioliasis prior to discharge Fasciolopsiasis Control of animal Gastrodiscoidiasis reservoirs Heterophyiasis Control of intermediate Metagonimiasis hosts Opisthorchiasis Cooking of water plants Paragonimiasis and fish Schistosomiasis Reducing water contact iv. Spread by excreta-related Bancroftian filariasis Various fecally Identification and insects (transmitted by Culex contaminated sites elimination of pipiens) in which insects breed suitable insect All the infections in breeding sites i-v able to be transmitted mechanically by flies and cockroaches a. See table 2-3 for data on additional epidemiological features by pathogen. b. Includes polio-, echo-, and coxsackievirus infections. c. Includes enterotoxigenic, enteroinvasive, and enteropathogenic E. coli infections. d. Ancylostoma duodenale and Necator aonericanus. Table 2-3. Basic epideiniologicalifeatures oJ excreted pathogens by environmental category Median Mtiltiplication injective Major Excreted outside human dose Significant nonihuman Intermediate Pathogen load' Latenctb Persistencec host (ID50) immunity? reservoir? host CATEGORY I Enteroviruses' 107 0 3 months No L Yes No None Hepatitis A virus 106?) 0 ? No I(?) Yes No None Rotavirus 106(?) 0 ? No L(?) Yes No(?) None Balartidium coli ? 0 ? No L(?) No(?) Yes None Entamoeba hisiolytico l0o 0 25 days No L No(?) No None Giardia lamblia t05 0 25 days No L No(?) Yes None Enterobius vermiciilaris Not 0 7 days No L No No None usually found in feces Hymenolepis nana ? 0 1 month No L Yes(?) Not'?) None CATEGORY 11 Campylobacter fetus N ssp. jejuni l0o 0 7 days Yese H(?) ? Yes None Pathogenic a Escherichia coli' i0, 0 3 months Yes H Yes(?) No(?) None Salmonella m S. typhi ol 0 2 months Yesc H Yes No None Other salmonellae 108 0 3 months Yes' H No Yes None Shigella spp. 107 0 1 month Yes' M No No None i Vibrio cholerae 107 0 1 month(?) Yes H Ycs(?) No None Yersinia enterocolitica l05 0 3 months Yes H(?) No Yes None CATEGORY III Ascaris lumbricoides 104 10 days 1 year No L No No None Hookwormsg 102 7 days 3 months No L No No None Strongyloides stercoralis 10 3 days 3 weeks Yes L Yes No None (free-living stage much longer) 7richuris trichlira 103 20 days 9 months No L No No None CATEGORY IV Taenia sagilrata and 104 2 months 9 months No L No No Cow T solium1i (7: saginata) or pig (T soliun) CATEGORY V Clonorchis sinensis' 102 6 weeks Life of fish Yesi L No Yes Snail and fish Diphyllohothrium 104 2 months Life of fish No L No Yes Copepod and latumi fish Fasciola hepaticah ? 2 months 4 months Yesi L No Yes Snail and aquatic plant Fasciolopsis buskih 103 2 months ? Yes' L No Yes Snail and aquatic plant Gastrodiscoides homibish ? 2 months(?) 7 Yesi L No Yes Snail and aquatic plant Heterophyes heterophyes' ? 6 weeks Life of fish Yes' L No Yes Snail and z fish C Metagonimus 7 6 weeks(?) Life of fish Yesi L No Yes Snail and 0 yokogawai' fish Paragonimus ? 4 months Life of crab Yesi L No Yes Snail and westermani' crab or - crayfish r Schistosoma S. haematobium' 4 per 5 weeks 2 days Yesi L Yes No Snail ;> milliliter of - urine S. japonicumh 40 7 weeks 2 days Yesi L Yes Yes Snail H S. mansoni" 40 4 weeks 2 days Yesi L ? No Snail C S~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ Leptospira spp. urine(?) 0 7 days No L Yes(?) Yes None L Low (106). ° ? Uncertain. a. Typical average number of organisms per gram of feces (except for Schistosoma haematobium and Leptospira, which occur in urine). b. Typical minimum time from excretion to infectivity. c. Estimated maximum life of infective stage at 20°-30°C. d. Includes polio-, echo-, and coxsackieviruses. e. Multiplication takes place predominantly on food. f. Includes enterotoxigenic, enteroinvasive, and enteropathogenic E. coli. g. Ancylostoma duodenale and Necator americaons. h. Latency is minimum time from excretion by man to potential reinfection of man. Persistence here refers to maximum survival time of final infective stage. Life cycle involves one intermediate host. i. Latency and persistence as for 'Taenia. Life cycle involves two intermediate hosts. j. Multiplication takes place in intermediate snail host. k. For the reasons given in chapter 1, Leptospira spp. do not fit any of the categories defined in table 2-2. 36 HEALTH HAZARDS OF EXCRETA Table 2-4. Category I and 11 pathogens Table 2-5. Category I and II pathogens (from table 2-2) (from table 2-2) rcanked by median infective ranked by persistence outside host diose (ID5s) Pathogen Persistence Balantidium coli Balantidium coli (?) Campylobacterfetus spp. jejuni ?) Entamoeba histoitrica Entamnoeba histolytica L Enterobius cermnicularis Enterobius rermicularis L Enterovirusesa Giardia lamblia Giardia lamblia L HyGiearolepis nana Hepatitis A virus (2/ Salmonella typhi Hymenolepis nana Shigella spp. M Rotavirus (?) Vibrio cholerae J Shigella M Enterovirusesa Campylobacterjetus ssp. jejuti /i) Pathogenic Eschiericliia coli' H Pathogenic Escherichia colib 1 Salmonellae Salmonella | Yersinia enterocolitica S. tvphi H Other salmonellae L Low (<1 month): M medium I month): H high (> I Vibrio cholerae I month). Yersinia enterocoiitica (?) J ? Uncertain. a. Includes polio-, echo-, and coxsackieviruses. L Low ( < 102; M medium t 104): H > 106). b. Includes enterotoxigenic, enteroinvasive, and enteropatho- ? Uncertain. genic E. coli. a. Includes poaio-, echo-, and coxsackieviruses. b. Includes enterotoxigenic. enteroinvasive, and enteropathogenic E. coli. Table 2-6. ID50 and persistence oj categorv I anid If pathogens (from table 2-2) commonly' and rarely particular pathogen; four of the pathogens in transmitted in European communities categories I and it (Campylobacter, salmonellae Balantidiuim coli and Giardia lamblia) have significant P"" ID50 Persistetnce animal reservoirs (table 2-3). Socioeconomic considerations would divide the Common/t transmitted Camp[v/obacte? litus SSp. jejani H('') L(?) infections in categories t and II in yet another way. Enterobius term/cularis L L Infections that are commonly transmitted in affluent Enteroviruses, L H communities (in Europe, for instance) that enjoy high Pathogenic Escheric/ria coli' H H standards in sanitary facilities and hygiene might be Giardia lamb/ia L L expected to be reduced insignificantly by the Rotavirus L(?) 2 introduction of limited sanitary improvements in poor Salmonellae H H communities of the developing countries. An approxi- Shigel/o sonnei M M mate division on these grounds is shown in table 2-6. Yersinia enterocolitica H(?) H In some cases the reasons for this division are clear (the Rare/c transmitted salmonellae, for instance, continue to be transmitted Balantidium coli L (?/ L from animals to man in affluent communities through Entamoeba histoictica L L contaminated foodstuffs), whereas in other cases (such Hy.menolepis nana L L as the continued transmission of Shigella sonnei Salmonella typhi H M throughout Europe) they are obscure. Shigella (other than sonnei) M M The most useful division of categories I and II has Vibria cholerae H M nevertheless proved to be one based on ID50, even though knowledge of the ID50 for infections affecting L LowU M medium H high. malnourished peasant children in the tropics is a. Includes polio-, echo-, and coxsackieviruses. nonexistent. With ID50 as the criterion, categories I and b. Includes enterotoxigenic. enteroinvasive. and enteropatho- II break in a way that makes theoretical sense and also genic E. co/i. ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 37 correlates in some degree with the likely effects of hygiene are not ideal (see figure 2-5). It is therefore improved excreta disposal facilities. likely that changes in excreta disposal technology will The transmission characteristics of the first five have little effect on the incidence of these infections if categories are illustrated in figure 2-4, in which the such changes are unaccompained by sweeping changes typical survival, latency, and multiplication features of in personal cleanliness, which, in turn, may require the groups of infections are shown. These factors, in major improvements in water supply and housing, and turn, affect the "length" of particular transmission major efforts in health education. cycles. Length has spatial as well as temporal But what subsequently happens to excreta-how implications, in that a long transmission cycle increases they are transported, treated, and reused is of less the opportunity of an infection's spreading over a wider importance for this group than the transmission of area, thus changing the pattern of risk. These issues are infection in the home. Although transmission can and developed in the next chapter, and are represented here does occur by more complex routes, most transmission in figure 2-5, in which the relative efficiency of in category I is direct, from person to person, and thus sanitation improvements in controlling the various the provision of hygienic toilets alone will have categories of infection is also indicated. Each category negligible impact. A qualification of category I must in table 2-2 implies some minimum sanitary require- follow this statement: categories I and ii grade into ments for control of the diseases within it and often each other and actually form a continuum (see a control measures ancillary to excreta disposal facilities further explanation in the next section). In particular, that further contribute to success. These requirements the parasitic protozoa have some features of both are elaborated in the discussion that follows. groups. One extreme of the category I parasites is the pinworm, Enterobius, whose sticky eggs are laid on the Categorv I anal skin by emerging females, so that transmission is by way of scratching fingers rather than by excretion of These are the infections that have a low ID50 (<102) eggs in the feces. At the other extreme is Giardia, and are infective immediately upon excretion. We associated with well-documented, waterborne out- argue that these infections may spread easily from breaks of diarrhea, and therefore presumably subject person to person whenever personal and domestic to partial control by excreta management. Infective organisms Category 11 m The infections in this category are all bacterial. They II Lying. bL as yet2ninfect;ve stages (latency). L'vng bt c yt niTeciv sags (laeny) have medium or high ID50S () 10 ), and so are less Environmentacl likely to be transmitted by person-to-person contact category X than are category I infections. The bacteria are TandI ~persistent and can multiply, so that even the small land TT' numbers remaining a few weeks after excretion can, if they find a suitable substrate (such as food), multiply to form an infective dose. Direct transmission routes are important, but so too are others with longer environmental cycles, such as the contamination of water sources or crops with fecal material (see figure 2- 5). The control measures listed in table 2-2 for category 1V ' IN DOMESTIC ANIMALS I are important with the added provisions of sound IN DOESI _N excreta treatment and reuse practice. But, as in category I, changes in excreta disposal and treatment " St practices alone may have little effect on transmission. Numbers A " Control measures may most affect those infections of .' > LS ___ X///S/ that-as noted earlier are not normally transmitted organisms L among affluent groups in Europe or elsewhere: Ttme > cholera, typhoid, and shigellosis (other than S. '- -o. : Any monitoring or evaluation program would do well Figure 2-4. Persistence outside the host oJfexcreted to examine these, rather than infections with pathogens (categories I- VJiom table 2-2) over time nontyphoid salmonellae or pathogenic E. coli. 38 HEALTH HAZARDS OF EXCRETA 'Sanitary barrier' <\\//X~~~~~~~~~~~~~~~~ \J VI Figure 2-5. Lengthanddispersionoftranismission cyclesofexcretedi,fectionis(categoriies I-V.-forom Table2-2). The possible efficacy of improved excreta disposal is indicated by the "sanitary barrier" The criteria used to differentiate categories i and ii II, the role of sanitation improvement is to interfere have been ID50 and length of the environmental cycle, with the efficiency of the longer cycles and thus obtain a factors with predictive value for the efficacy of greater overall benefit than that possible for category 1, sanitation as a control measure. The reason that in which these longer cycles have little significance. categories I and II do not form tidy groups is that the persistences of the pathogens involved vary. The Category III extreme category I case-an environmentally fragile organism with a low ID,,-will clearly tend to be This category contains the soil-transmitted hel- spread in a familial or similar tight pattern and will minths, which are both latent and persistent (see figure depend for its control more on personal cleanliness 2-4). Their transmission has little or nothing to do with than on sanitation. (An extreme example, though not personal cleanliness because these helminth eggs are excreta-transmitted, can be found in the venereal not immediately infective to man. Domestic cleanliness diseases, which do not survive in the environment and is relevant only as it concerns the preparation of depend on intimate contact for their spread.) However, vegetables grown in fields enriched by human excreta an environmentally persistent organism with a low or the maintenance of latrines in conditions that do not ID,0 will lead to infection difficult to reduce either by allow helminth eggs to remain in the vicinity for the sanitation or personal and domestic cleanliness. Many duration of their latency. If eggs are not deposited in excreted viruses exemplify this pattern and pose such soil, or other suitable media, transmission will not major problems of control that induced immunity may occur. Any kind of latrine that contains or removes be the best solution (this is certainly the case for excreta and does not permit contamination of the floor, poliomyelitis and probably also for infectious hepatitis yard, or fields, will therefore limit transmission. and rotavirus diarrhea). For the infections of category Because the persistence of helminth eggs is so long (see ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 39 table 2-3), it is not sufficient simply to prevent infected egg can give rise to many infective larvae. A fresh feces from reaching the yard or fields: any fecal thousandfold multiplication is not uncommon, and product that has not been adequately treated must not effective transmission can continue at low con- reach the soil. In societies that reuse their excreta on tamination levels. The requirements for adequate the land, treatment prior to application is therefore excreta disposal, in terms of the percentage of all feces vital. Effective treatment for the removal of helminth reaching the toilet, may therefore be demanding. eggs generally requires waste stabilization ponds or thermophilic digestion,4 although prolonged storage Category VI will inactivate the eggs of many species. The excreta-related insect vectors of disease form Category IV three main groups. In the first of these, the cosmopolitan Culex pipiens complex of mosquito Category iv is for the beef and pork tapeworms. Any species preferentially breeds in highly contaminated disposal system that prevents untreated human excreta water and is medically important as a vector of the from being eaten by cattle and pigs will control the worm (Wuchereria bancrojti) that causes Bancroftian transmission of these infections (see figure 2-5). Cattle filariasis. The other two groups, flies and cockroaches, are likely to be infected in fields treated with sewage proliferate where feces are exposed. Both have been sludge or effluent and may also eat feces deposited in shown to carry numerous excreted pathogens on their the cowshed. Pigs are likely to become infected by feet and in their intestinal tract, but their role in eating human feces deposited around the dwelling or in actually spreading disease from person to person is the pigpen. The provision of toilets to which pigs and disputed (though their nuisance value is certain). Flies cattle cannot have access, and the treatment of all have been implicated, however, in the transmission of wastes prior to land application, are the necessary eye infections and in infecting and spreading skin control methods. Measures to prevent birds, especially lesions. The control measures implied for insects are gulls, from feeding on trickling filters and sludge drying those sanitary improvements of differing sophisti- beds and subsequently depositing tapeworm eggs in cation which prevent their access to excreta. In general, their droppings on pastures are also required. In the the simpler the facility, the more care is needed to absence of the measures described above, however, the maintain it insect-free. Cockroaches, flies, and Culex thorough cooking of beef and pork is the most pipiens mosquitoes often have breeding places in important control measure. Personal and domestic addition to those associated with excreta disposal and cleanliness, except the use and maintenance of safe will in many cases elude control by disposal toilets, are ineffective controls. improvements alone. Category V Summary This category contains the water-based helminths, The correlation of the environmental features of the which need an aquatic host or hosts to complete their categories with the length and spread of transmission life cycles. Control is achieved by preventing untreated routes has been indicated in figure 2-5, and the excreta or sewage from reaching water in which these discussion has emphasized the importance of com- aquatic hosts live (see figure 2-5). Any land application plementary controls for most diseases. If excreta or dry composting system will therefore reduce disposal alone is improved, however, likely control for transmission. There are two complications. First, in all each category is as follows: cases except Schistosoma mansoni and S. haematobium, Category Control animals are an important reservoir of infection (see I Control tables 1-9 and 2-3), and any measures restricted solely I N Slight to moderate to human excreta can only have a partial effect. Second. II Moderate to great in the case of S. haernatobiuim it is the disposal of urine, IV Moderate to great far more difficult to control than the disposal of feces, v Moderate that is important. Because multiplication of these VI Slight to moderate helminths takes place in the intermediate hosts (except The outstanding difference is between categories I and in the case of the fish tapeworm, Diphyllobothrium), one ii, which depend strongly on personal and domestic cleanliness, and the other categories, which do not. The 4. See the discussion of these processes in chapters 5 and 6. central changes necessary to control infections in 40 HEALTH HAZARDS OF EXCRETA categories ini and iv are relatively simple namely, the Eyles, D. E., Jones, F. E. and Smith, C. S. (1953). A study of provision of toilets which people ol'all ages? will use anid Endamoeha histolytica and other intestinal parasites in a keep clean, and the treatment of fecal products prior to rural west Tennessee community. Aimerican Journal Jo recycling on the land. The reason that reports on the Tropical Medicine and Hygiene, 2, 173-190. effects of latrine programs often do not show a marked 'achem, R. . A., McGarry, M. G. and Mara, D. D. (1977). Water, Wastes and Health in Hot Climates. London: John decrease in the prevalence of the infections in Wiley. categories in1 and 1v6 is that, although latrines have Gordon, J. E., Behar. M., Scrimshaw, N. S., Guzman, M. A. been built, they have typically neither been kept clean and Ascoli, W. (1964). Acute diarrhoeal disease in less nor been used by children or by adults when working in developed countries. Bulletin of the World Health the fields. Organization, 31, 1-28. Henry, F. J. (1981). Environmental sanitation, infection and Literature Cited nutritional status of infants in rural St. Lucia, West Indies. Transactions of'the Royal Society .' 1 I Medicine and Arfaa, F., Sahba, G. H., Farahmandian, 1. and Jalali. H. Hvgiene, 75, 507-513. (1977). Evaluation of the effect of different methods of Hollister, A. C., Beck, M. D., Gittelsohn, A. M. and Hemphill, control of soil-transmitted helminths in Khuzestan, E. C. (1955). Influence of water availability on \',L southwest Iran. American Journal T, I T .. ; Medicine and prevalence in children of farm labor families. American Hygiene, 26, 230-233. Journal oJ'Public Health, 45, 354-362. Azurin, J. C. and Alvero, M. (1974). Field evaluation of Hornick, R. B., Music, S.I., Wenzel, R., Cash, R., Libonati. J. environmental sanitation measures against cholera. P., Snyder, M. J. and Woodward. T. E. (1971). The Broad Bulletin of' the World Health Organization, 51, 19-26. Street pump revisited. Response of volunteers to ingested Barbosa, F. S., Pinto, R. and Souza, 0. A. (1971). Control of cholera vibrios. Bulletin of the New York Academy oJ schistosomiasis in a small northeast Brazilian community. Medicine, 47, 1181-1191. Transactions of the Royal Society' of' Tropical Medicine and Jeffery, G. M. (1960). A three-year epidemiologic study of Hygiene. 65, 206-213. intestinal parasites in a selected group of mental patients. Bradley, D. J. (1977). Health aspects of water supplies in American Journal of Hygiene, 71, 1-8. tropical countries. In Water, Wastes and Health in Hot Katayama, Y. (1955). Sanitary treatment of human excreta Climates, eds. Feachem, R. G. A., McGarry, M. G. and by heating process. 16. Effect of the treatment applied to a Mara, D. D., pp. 3-17. London: John Wiley. farm village (Part 1). Japanese Joturnal of the Nation's Brooke, M. M., Donaldson, A. W. and Brown, E. (1954). An Health, 24, 1-12. amebiasis survey in a Veterans Administration Hospital, Kawagoe, K., Nishi, H., Shibata, E. and Yamada, S. (1958). Chamblee, Georgia. with comparison of technics. On the effect of nightsoil treatment upon heating process American Journal of' Tropical Medicine and Hygienie, 3, utilizing surplus midnight electric power upon the 615-620. incidence of parasitic infection of farmers. Japanese Brooke, M. M., Healy, G. R., Levy, P., Kaiser, R. L. and Journal of'the Nation's Health, 27, 162-165. Bunch, W. L. (1963). A sample survey of selected areas in Khalil, M. (1931). The pail closet as an efficient means of and near Little Rock, Arkansas, to assess the prevalence of controlling human helminth infection as observed in Tura Entamoeba histolytica. Bulletin oJ' the World Health Prison, Egypt, with a discussion on the source of Ascar-is Organization, 29, 813-822. infection. Annals of Tropical Medicine and Parasitology, 25, Chandler, A. C. (1953). An evaluation of the effects, after two 3 5-62. years, of sanitary improvements in an Egyptian village. Kleevens, J. W. L. 11966). Re-housing and infections by soil Journal of'the Egyptian Medical Association, 36, 357-367. transmitted helminths in Singapore. Singapore Medical (1954). A comparison of helminthic and protozoan Journal, 7, 12-29. infections in two Egyptian villages two years after the Koopman. J. S. (1978). Diarrhea and school toilet hygiene in installation of sanitary improvements in one of them. Cali, Colombia. American Journal of Epidemiology, 107, Americani Journal of' Tropical Medicine and Hygiene, 3, 412-420. 59-73. Kourany, M. and Vasquez, M. A. (1969). Housing and Cort, W. W., Schapiro, L. and Stoll, N. R. (1929). A study of certain socioenvironmental factors and prevalence of reinfection after treatment with hookworm and Ascaris in enteropathogenic bacteria among infants with diarrheal two villages in Panama. American Journal of 'Hygiene, 10, disease in Panama. American Journal of' Tropical Medicine 614-625. and Hygiene, 18, 936-941. 5. Otcoursebabiesandveryyoungchildrenareunabletouseatoilet. Kumar, P., Sehgal, B. S. and Singh, R. (1970). Bore-hole Health education programsmust include advice tomothers on how to disposal of excreta of children and diarrhoeal morbidity in dispose of their children's excreta in a suitablv hygienic way. a rural community. Environmental Healtlh, 12, 155-159. Kutsumi, H. (1969). Epidemiological study on the preventive 6. See the next chapter and table 2-t. effect of thiabendazole as an ovicide against human ENVIRONMENTAL CLASSIFICATION OF INFECTIONS 41 hookworm, Trichurtis and Ascaris infections. Japanese Schneider,R.E.,Shiffman,M.andFaigenblum,J. (1978). The Journal of Medical Science and Biology. 22, 51-64. potential effect of water on gastrointestinal infections McCabe, L. J. and Haines, T. W. (1957). Diarrhoeal disease prevalent in developing countries. American Journal of control by improving human excreta disposal. Public Clinical Nutrition, 31, 2089-2099. Health Reports, 72, 921-928. Scott, J. A. and Barlow, C. H. (1938). Limitations to the Mackie, T. T., Mackie, J. W., Vaughn, C. M., Gleason, N. N., control of helminth parasites in Egypt by means of Greenberg, B. G., Nenninger, E. S., Lunde, M. N., Moore, treatment and sanitation. American Journal oJHygiene, 27, L. L. A., Kluttz, J. A. and Taliafero, M. 0. (1956). Intestinal 619-648. parasitic infections in Forsyth County, North Carolina. Shiffman, M. A., Schneider, R., Faigenblum, J. M., Helms, R. IV. Domestic environmental sanitation and the prevalence and Turner, A. (1979). Field studies on water sanitation of Entamoeba histolytica. American Journal of Tropical and health education in relation to health status in Central Medicine and Hygiene, 5, 29-39. America. Progress in Water Technology, 11, 143-150. Mathur, T. N. and Kaur, J. (1972). The epidemiology of Stewart, W. H., McCabe, L. J., Hemphill, E. C. and DeCapito, amoebiasis in an urban area. Indian Journal of Medical T. (1955). Diarrheal disease control studies. IV. Research, 60, 1t34-1137. Relationship of certain environmental factors to the Moore, H. A., de la Cruz, E. and Vargas-Mendez, 0. (1965). prevalence of Shigella infection. American Journal oJ Diarrheal disease studies in Costa Rica. IV. The influence Tropical Medicine and Hygiene, 4, 718-724. of sanitation upon the prevalence of intestinal infection Sweet, W. C., Cort, W. W., Schapiro, L., Stoll, N. R. and Riley, and diarrheal disease. American Journal of Epidemiology, W. A. (1929). A study of the effect of treatment and 82, 162-184. sanitation on the level of hookworm infestation in certain Otto, G. F., Cort, W. W. and Keller, A. E. (1931). areas in Panama. American Journal oJ Hygiene Environmental studies of families in Tennessee infested Monographic Series no. 9, 98-138. with Ascaris, Trichuris and hookworm. American Journal van Zijl, W. J. (1966). Studies on diarrhoeal diseases in seven of Hygiene, 14, 156-193. countries by the World Health Organization Diarrhoeal Otto, G. F. and Spindler, L. A. (1930). Effect of partial Disease Advisory Team. B,,h. ',. of the World Health sanitation on infestation with intestinal parasites in Organization, 35, 249-261. Southwest Virginia. Southern Medical Journal, 23, Villarejos, V. M., Pelon, W., Picado, B., Ortiz, J. G., Jimenez, 556-560. R. and Navas, H. (1966). Epidemiologic investigation of an Rosenberg, A. I. (1960). Sanitary and hygienic measures for outbreak of infectious hepatitis in Costa Rica. American the control of focal ascariasis. Meditsinskaia Parazitologiia Journal of Epidemiology, 84, 457-466. i Parazitarnye Boleznii, 29, 143-149. Weir, J. M., Wasif, I. M., Hassan, F. R., Attia, S. D. M. and Sahba, G. H. and Arfaa, F. (1967). The effect of sanitation on Kader, M. A. (1952). An evaluation of health and ascariasis in an Iranian village. Journal of Tropical sanitation in Egyptian villages. Journal of the Egyptian Medicine and Hygiene, 70, 37-41. Public Health Association, 27, 53-122. Schliessmann, D. J., Atchley, F. O., Wilcomb, M. J. and WHO (1979). Human Viruses in Water, Wastewater, and Soil. Welch, S.F. (1958). Relationship of environmentalJactors to Technical Report Series no. 639. Geneva: World Health the occurrence of enteric diseases in areas of eastern Organization. Kentucky. Public Health Monograph no. 54. Washington, D.C.: Government Printing Office. 3 The Risks of Excreta to Public Health THE DISCUSSION has dwelled at length on the survival mother has had six babies, one of whom died at the age of pathogenic organisms in excreta, on which there is a of 15 months after a sudden attack of diarrhea; a good deal of information. This is the main health- school-age child died in a cholera epidemic that swept related concern of the engineer when he is designing the region 4 years ago. sanitary facilities. The planner and economist have a It is particularly difficult to control excreta in this greater interest in epidemiological risk: if, in a given damp environment-most feces are deposited close to situation specific changes in excreta disposal are made, the house, and the younger children urinate in the how much less disease will there be? This question can nearby canals. Several years ago a government be rephrased in two ways, the first of which can be campaign to provide pit latrines was mounted, and one answered readily and the other only with the greatest was dug near the family's house. They used it for a difficulty. The easier question is: what are the disease while, until the pit flooded over in the monsoon season problems associated with excreta, and thus, by and a large quantity of fecal material was spread implication, with inadequate excreta disposal facilities around the house. It was during the flooding that the or inadequate personal or domestic cleanliness? The cholera epidemic occurred; its sad consequences for difficult question concerns the health benefits of the family, together with the unpleasant mess from the improved sanitation: how much disease will be latrine, discouraged further use of the facility. The next eradicated if a given sanitary improvement is government recommended that a concrete aquaprivy undertaken? These questions are considered in general be built above the ground to avoid the floods, but the terms in this chapter. family could not afford this and returned to defecating close to the house during the day. Nocturnal excreta were collected in a bucket and deposited in a nearby Illustrative Sketches fishpond. How does this situation affect the family's health? The effects of the diseases accompanying unsafe All the children get diarrhea several times a year, the exereta disposal are dramatized in the sketches of two parents less regularly. The worst occasion was when imaginary settings that follow. Formal case studies of two of the girls got it at the same time. The younger sanitation and health are then outlined before a one, 15 months old, seemed to wither overnight, and discussion of the benefits of sanitation improvements. she died the next day. Death was from rotavirus infection. (Why it is more often lethal in the tropics than in temperate countries is unclear: perhaps the poor sanitary facilities in this case gave the child an In areas of Southeast Asia with high rainfall, a overwhelming dose of the virus; perhaps malnutrition, perennially hot climate, and a main cereal crop of ubiquitous during the weaning period in communities irrigated rice, the diverse health hazards from excreta such as this one, complicated the attack?) Most of the are illustrated by the following case history, a diarrheas are watery, sudden attacks, but last year the composite of several real sites and people. A family lives grandmother who shares the house with the family, in a palm-roofed, wooden house surrounded by rice was one of several people in the village who came down paddies and small irrigation channels, one of which, with a more painful diarrhea with bloody stools, from flowing near the house, acts as the domestic water which she nearly died. Medicine from the dispensary supply. There are four children in the family: the four miles away helped initially, but she remained ill for 43 44 HEALTH HAZARDS OF EXCRETA weeks. This attack was from bacillary dysentery temperatures are at least as high as in the Asian village (shigellosis), though to distinguish it from amebiasis just visited. The houses cluster on a mound rising from would have required laboratory diagnosis. surrounding irrigated areas. The irrigation is from All these illnesses were dramatic, but the family has water brought from afar by great rivers, not from heavy several health problems of which they are barely aware. rainfall, and the ground is baked hard where it has not The eldest son has not grown properly: although he is recently been irrigated. Within the village the streets 23, he looks as if he were in his early teens; his belly is are narrow and unpaved, and large quantities of debris always grossly swollen, and the dispensary attendant lie around. can feel his hard liver and spleen under the taut skin of The family selected consists of the parents, three his abdomen. His condition is caused by schistoso- children, and some elderly relatives. This family has miasis, which is spread from one person to another by a also suffered the death of children from diarrheal tiny snail living in the damp grass beside the canals and disease. (Indeed, it would be difficult to find a tropical in the water itself. Several members of the family are or subtropical area in which this is not a problem.) infected, but only this boy shows signs of the disease. As in Asia, schistosomiasis and elephantiasis are In this region of paddies and canals, fish present. These are of somewhat different varieties, but sometimes cooked, sometimes pickled raw in create disability in similar ways. Although intestinal vinegar is an acceptable and available food. A schistosomiasis occurs here, two of the younger portion of the fish consumed is from ponds fertilized children have a urinary form of the disease and pass with human feces, and this practice has caused some of blood in their urine every day. This looks more serious the family to be infected by the liver fluke Cloniorchis than it is (in fact, the blood loss is small); however, the sinensis. Another helminth that the family harbors in children do suffer the pain and inconvenience of having large numbers is Fasciolopsis buski, an intestinal fluke to get up frequently to urinate at night. Not too long acquired from eating raw aquatic vegetables. Neither ago their uncle had to go to the hospital in the nearby of these parasites causes catastrophic illness, but the city, where he was told that he had inoperable cancer of diversion of nutrients to the parasites and their other the bladder. He died a very painful death, and the insidious effects make life less satisfactory than it surgeon told the family his death may have been a late otherwise would be. The family also suffers from other consequence of the same infection causing blood in the intestinal worms occurring in even greater numbers urine of the children, but that only a few unfortunate and causing more illness (these are discussed in relation people developed cancer from the infection. to another family, below). The helminths associated with fish and aquatic One more infection attends the family's lack of safe plants that plagued the previous family are absent from excreta disposal. Within the pits of the latrines that this environment, but microscopic examination of the have been flooded and abandoned, the liquid waste is feces of the family show hookworm (Ancylostoma), colonized by mosquito larvae of the Culex pipiens roundworm (Ascaris) and whipworm (Trichuris) eggs group. When the adult mosquitos bite the members of in large numbers. The hookworm eggs are especially the household, they transmit into the bloodstream the numerous the infection has been picked up by larvae of a parasitic worm (Wuchereria bancrofti) that walking barefoot on land that has been used for lives in the tissues under the skin of the legs and defecation and that has been kept moist enough by the elsewhere, particularly in the lymph nodes, where it nearby drains and canals for the worm larvae to blocks the lymphatic flow. Tissues near the blockage develop in the soil. The mother has a particularly heavy consequently become swollen from the accumulation infection. The worms inhabit the small intestine where of lymph, and some affected people develop massive they attach themselves to the intestinal wall; they are elephantiasis. The father of the family is troubled by messy feeders, and a large amount of the blood they this in his right leg, which is so swollen that he cannot suck for their growth and production of their eggs work in the fields as productively as he could before. passes straight through their bodies and is lost into the intestinal lumen. As a result the blood losses from this infection are high-indeed. the mother's loss is twice as A Nor-th African fiimily heavy as that from menstruation and, because her diet The next region visited is quite different in general is not overly rich in iron, she has become anemic and appearance, but behind this exterior are certain unable to work as hard as a fit person. The same is true similarities in the disease pattern. The village entered is of one of the children: his abdomen is swollen; he a cluster ofmud brick houses located in the subtropics. cannot run fast enough to keep up with the other It is quite cold in the winter though summer children, and his condition gives considerable cause for RISKS TO PUBLIC HEALTH 45 anxiety. Some other infection in addition to the their way onto vegetables that are eaten raw. Eggs also hookworm might well claim his life. occur in the mud and sand of the compound, where All the family have roundworms. These parasites are they readily contaminate the hands of crawling babies. quite large (over 100 millimeters long), and every now Another intestinal worm somewhat important in and then one of the younger children passes one in the this milieu is the beef tapeworm (Taenia saginata), stool. This elicits little more than comment, since there which is acquired from an infected cow by eating its is no obvious illness except pain in the abdomen, a beef undercooked (this readily occurs when a large complaint difficult to ascribe to a specific cause. What piece of meat is roasted). The adult tapeworm matures is certain is that the worms are absorbing a good in the intestines, adding segments to its length and percentage of the nutrients the children need, and there competing for the family members' limited nutrients; is also the risk that the worms will get stuck in the its eggs, often contained in its swollen segments, are narrowest part of the intestine and block it, thus shed in large numbers when a tapeworm segment necessitating a faraway surgeon's attention. The family wriggles out of the anus. These worm segments are are well aware of the problem, and have often visited frequently ingested by browsing cattle; the worm the dispensary to get medicine. But in the absence of undergoes further development within the muscles of instruction and better methods of disposing of their the cow; the beef is inadequately cooked and eaten, and excreta, the infection comes back every few months. the cycle of infection is resumed. The family's religion The adults seem to have become somewhat immune to prohibits the eating of pork and so they are spared its reinfection, and the children carry the brunt of the tapeworm (Taenia soliuin), whose larvae can develop in recurrence. human muscles-an added and sometimes fatal hazard. Most of those, especially the children, who have Except in the case of hookworm infection with its roundworms also have whipworm infections. These dramatic blood loss, all these helminth infections are so little worms, found mostly on the wall of the colon and long lasting and ennervating that it is difficult to assess rectal passage, have an uncertain effect on most of the their specific damage; they are all infections that are family, generally adding to the burden of other often underrated because of their widespread occur- parasites. Some while ago a neighbor's child picked up rence and insidious, drawn-out course. The family also a very heavy infection with the whipworm. The rectal suffers from several acute infections, not only diarrheas passage gradually prolapsed (that is, got partly pushed but also typhoid and hepatitis. The incidence of out of the anal orifice), which was both painful and typhoid in the village is particularly high because of unsightly, while an intractable diarrhea that had begun inadequate excreta disposal. In addition, the presence some months earlier persisted and made the child very of schistosomiasis in the inhabitants modifies typhoid anemic. A concurrent amebic infection led to some and lengthens its course, and up to one in every twenty- confusion over what was causing which symptoms, but five people may become a typhoid carrier in some of the prolapse was certainly not a regular feature of these villages, a rate which is an order of magnitude amebiasis and the diarrhea could have been due to higher than seen elsewhere. Consequently, typhoid is either cause. extremely common, no less severe than elsewhere, and What arrangements are made for excreta disposal an appreciable cause of mortality. Hepatitis also here? Bore-hole latrines were made for each family's occurs frequently: in the younger children it rarely use but they filled up rather quickly and were then so produces serious symptoms, but in adults the patient unpleasant that no one wanted to use them. In any may be bedridden for weeks or months, and sudden case, the latrines were in or near the houses and, death is not unknown. because the families spend much of the day in the fields One feature that clearly emerges from the account of working on their rice and other crops most felt that it this family in North Africa is the extent to which it would be an unreasonable waste of their time to come shares in the excreta-related health problems of the all the way back to the house to defecate. It is also more family in Southeast Asia. Indeed, as in few other disease convenient to relieve themselves in the field because patterns, there is a sameness to most of the serious, their religion insists that they wash the anus after frequently transmitted, excreted infections that cannot defecation, and there is no water readily available for be avoided: certain infections are peculiar to particular this purpose within the compound. Because of the localities, but the pattern of diarrheal disease, enteric varying sites for defecation, roundworm and whip- fever, numerous viral infections, and intestinal worms worm eggs are spread widely throughout the is repeated worldwide. Of the major excreted environment. The eggs are extremely resistant, even in infections, only cholera and schistosomiasis have the harsh climate of this part of the world, and find variable and patchy distributions. 46 HEALTH HAZARDS OF EXCRETA Table 3-1. Maximum prevalence of excreted pathogens (from table 2-2) bv age in indigenous populations of endemic areas Age group of highest prevalence of infection (years) Babies C ii., Teenagers Adults Patlhogen (0-2) (3-12) (13-19) (20+) CATEGORY I Balantidium coli * Entamoeba histolytica * * Enterobius vermiclularis * * Enterovirusesa * * Giardia lamblia * Hepatitis A virus * * * Hymenolepis nana * * Rotavirus * CATEGORY 11 Campylobacterfetus ssp. jejuni * * Pathogenic Excherichia colib * * Salmonella S. typhi * * Other salmonellae * * * * Shigella spp. * * Vibrio cholerae * Yersinia enterocolitica * * CATEGORY II] Ascaris lumbricoides * * Hookwormsc * * * Strongy loides stercoralis * * Trichuris trichiura * CATEGORY IV Tuenia saginata and T solium * * CATEGORY V Clonorchis sitensis I) , i., P. I . .,*. latum * Fasciola hepatica * * * Fasciolopsis buski * * Gastrodiscoides hominis * Heterophyes heterophves * Metagonimus yokagawai * Paragonimus uestermani * Schistosoma spp. * * a. Includes polio-, echo-. and coxsackieviruses. b. Includes enterotoxigenic, enteroinvasive, and enteropathogenic E. coli. c. Ancylostoma duodenale and Necator americanus. Children and Excreta Disposal found in people of all ages, many are concentrated in particular age groups. The age groups most afflicted by Many of the excreted infections examined in this the main excreted infections in areas where these book have a markedly nonuniform distribution among infections are endemic are shown in table 3-1. The data different age groups. Although all the infections are ofthe table clearly show that many ofthese illnesses are RISKS TO PUBLIC HEALTH 47 primarily childhood infections, or that the infections happy to use and health education for mothers, so that afflict children as well as adults. This fact has the they will compel their children to use them. Health greatest relevance for disease control through improve- education for school-aged children could also be ments in excreta disposal. effective here, and it is essential that all schools have In all societies children below the age of about 3 will well-maintained latrines as positive examples for the defecate whenever and wherever they feel the need. A children.' proportion of these children will be excreting substantial quantities of pathogens. In some societies these children's feces are regarded as relatively inoffensive, and the children are allowed to defecate The transmission cycles typically followed by the anywhere in or near the house. In this case it is highly infections in categories I through v (table 2-2 and figure likely that these feces will play a significant role in 2-5) have been compared and discussed and the shorter transmitting infection to other children and adults. or tighter cycles that categories l and II may follow over This applies not only to those infections without a categories III to v have been indicated. The implication latency period but also to infections such as ascariasis, is that categories III to V are associated with a wider in which the defecation habits of children may spread of their infections, a factor important in the determine the degree of soil pollution in the yard and selection of appropriate excreta disposal technology around the house and thus the prevalence and intensity and, in particular, in assessing the willingness of an of infection in the household. In other societies individual family to adopt an innovation. If, on the one strenuous efforts are made to control and manage the hand, a household head believes, or can be persuaded stools of young children, either by making them wear to believe, that the adoption of a new technology will diapers (nappies) or by cleaning up their stools bring appreciable health benefits to his family, whenever they are found. Either of these reactions regardless of what is taking place in the neighborhood, should have an important controlling influence on the then he will be more willing to innovate. If, on the other intrafamilial transmission of excreted infections. hand, it is clear that his action alone will have a Between these two extremes is a range of negligible effect on his family's health, he is more likely intermediate behavioral patterns by which adults react to sit back and await clear evidence that a viable and to the stools of young children. In most poor effective improvement program is being carried out communities, the pattern is closer to the first reaction throughout his neighborhood. than to the second. The relevant response of In cases in which most pathogen transmission is government and other responsible agencies where intrafamilial-as in category I and, to a lesser extent, these attitudes prevail should be health education category iI it can be expected that improvement in programs to encourage in mothers the belief that the excreta disposal and cleanliness in an individual family stools of young children are dangerous and should be may lead to health benefits for that family. In fact, as we hygienically disposed of. Although the problem is have already argued, cleanliness is probably more primarily in attitudes and behavior, the provision of important than excreta disposal facilities per se in the some form of toilet for the disposal of a child's stool reduction of category I (and to a lesser extent category and, perhaps more important, a convenient water iI) infections, and therefore it is changes in hygienic supply will greatly assist child hygiene. behavior that may bring the greatest benefit to a single Children over 3 years in age, in contrast, are capable family in isolation from widespread changes in the of using a toilet if one of suitable design is available. community's sanitation. Children of 3 to 12 years frequently do not use There is one infection from categories III to v available toilets because they find their use incon- ascariasis-which, although potentially having a long venient and it is not encouraged by adults; they are transmission cycle, is frequently transmitted within the afraid of falling down the toilet's hole or of being family and diminishes with improvements in excreta attacked by the pigs that may live next to the latrine; disposal facilities without accompanying changes in they cannot use a toilet not designed to their scale; or personal cleanliness. Work in China and the US in the they are prevented from doing so by adults who want 1920's and 1930's showed that poor families, who used to avoid cleaning up the toilet area after them. their latrines and prevented their children from As with very young children, it is of vital importance defecating in the yard, had significantly lower that the stools of children over age 3 be hygienically 1. Indeed, the whole subject of health education, so difficult to disposed of because some will be rich in pathogens. The discuss incisively, is crucial to thefull realisation ofthe potential health solution lies in providing both toilets that children are benefits of improved excreta disposal facilities see Chapter 8. 48 HEALTH HAZARDS OF EXCRETA intensities of Ascaris infection than their neighbors several changes to benefit the community's health. To (Otto, Cort and Keller 1931; Winfield 1937). Similar allocate all the health benefits to improved sanitation reductions on an individual family basis can be alone would therefore be unjustified. Conversely, a expected from the adoption of improvements in excreta study that demonstrates no health improvement after disposal today. There are other specific circumstances appropriate changes in sanitary facilities cannot in which a given infection may readily be reduced by validly imply that such changes are useless. The the independent action of a single family. An example is facilities may have been unused for lack of health hookworm in rural India, where in many villages much education or may have been improperly sited-it is of the infection occurs when barefoot people visit the often a mistake to generalize from a particular local communal defecation grounds on the edge of the result. community. A family which installs a pit latrine and no The economist ideally wishes to use data on health longer visits the defecation ground may substantially benefits to decide priorities in resource allocation, and reduce its exposure to hookworm infection. These the total health benefits are needed for such a decision. cases demonstrate that, in planning and implementing However, health as such is not measureable (except, an excreta disposal program, officials may find it useful possibly, in the form of statistics on the growth of to identify infections for which individual household infants), and it is diseases that are studied instead. action may be particularly effective. These infections Because sanitation affects a range of diseases not all might then be monitored and the family results used as measurable in a single study, a few indicator or index part of a community propaganda exercise (for diseases are usually chosen to assess benefits. More example: "the Sanchez family has adopted the new often still, particular disease agents such as -Ji.'gt .i: latrine and improved their domestic hygiene and they bacteria or worm eggs are assessed in the feces. The now have less roundworms than their neighbors>). resulting measures of how infection rates change as sanitation is applied are several removes from health Health Benefits of Sanitation benefits pe- se. and the intermediate causal relation- ships are by no means linear. The relation between an Although major health problems are clearly infection and the development of disease depends on associated with inadequate excreta disposal facilities, variables such as: the intensity of infection, nutritional to relate the two causally-in particular, to say what status, other infections, age of the host, and health the health benefits will be from a given proposed care available locally. improvement of facilities-is difficult. The difficulties and the studies attempting to overcome them are The literature reviewed in this section. Critical comments must not obscure the fact that without improved excreta Some of the relevant literature on the assessment of disposal many of the diseases discussed will never be health benefits is listed in table 2-1. Almost none of the overcome, yet other complementary measures and in studies described therc reaches the standards of some cases major social, economic, and political epidemiological demonstration that make a study changes--will generally be required for success. conclusive; melancholy criticism of the limitations of each paper is therefore avoided. Rather, the con- clusions reported in the literature should be taken as an Methodological issues indication of trends. Studies of the health benefits of sanitation in the field An important component of any evaluation, but one have either compared disease levels in communities that is much neglected, is time. The attainment of with varying sanitary facilities or monitored disease comparability between an area that has experienced patterns before and after the improvement of sanitary sanitary interventions and one that has not requires facilities within a community. In both cases the that surveys be done soon after installation of the difficulties in attributing benefits to the improved sanitary facilities. In the common case, observations sanitation have arisen because other variables are often are recorded only for up to a year and are begun associated with the sanitation facilities. People who months after construction. Such information has poor have better sanitation than their neighbors often also predictive value for the long term. If a special campaign have higher incomes, better water supplies, and has been mounted in relation to new facilities, the different habits of cleanliness. Similarly, if a single results may be transiently impressive but may fall off community is followed over time, improvements in the over time. Conversely, the community may take some sanitary facilities are likely to be only one among years to adjust to and use the innovations, so that a RISKS TO PUBLIC HEALTH 49 short-term study fails to demonstrate the real benefits of treating sanitation-related diseases, but these changes bring. Even if these problems are avoided estimates are-small in relation to the estimates of the through long-term study or the observation of work and life lost to these diseases. The latter estimates variations between communities with long-established themselves are subject to great uncertainty, and any differences in excreta disposal patterns, the difficulty of figures put on such losses may be largely spurious. confounding variables arises: it is most unlikely that Two examples may be given. Wagner and Lanoix communities will stay comparable in all differences (1969) attempted to estimate the costs of diarrheal other than excreta disposal and its consequences over disease and found that the largest component was from many years. premature death in children under the age of 2 years. Considering these complexities, it is not surprising There are several means of placing an economic value that studies on the benefits of excreta disposal assessed to death at this age that give widely differing answers. by health changes in the field are almost all of an More recently Latham, Latham and Basta (1977) insufficient standard to be convincing. Few indeed can estimated the cost of Ascaris infection to Kenya. The be described as scientifically impeccable and produc- largest single component was the estimated reduction tive of results inspiring confidence. This discussion of in food absorption and utilization by those infected, methodology might be considered niggling and given as US$4.4 millions yearly, as compared with a academic if most of the published studies gave total of US$0.7 million for all other costs such as concordant results-but this is not the case, and some present treatment, health care, and transport to health studies are frankly contradictory. Again, a detailed care facilities. Yet it is possible to pose reasons for the critique of each study listed in table 2-1 is not given US$4.4 millions varying by ± 50 percent. because these defects in sampling, comparability of It is also possible, however, to make informed samples, and confounding variables recur with such assessments of the comparative benefits of different consistency, whereas the actual use of facilities excreta disposal systems, and this is attempted below. provided is scarcely ever assessed. A further methodo- No cost figures on different excreta disposal systems logical difficulty is that, in studies using recurrent are given here-these may be found in the various medical treatment, observations are made during other documents issuing from the World Bank's periods too short in duration to show long-term investigations of appropriate sanitation technologies.2 outcomes and to detect the large rise in noncompliance It will be clear from our discussion of human behavior with therapy that tends to occur in time. here and in chapter 8 that the greatest determinants of If all the studies in table 2-1 were summarized, the efficacy of alternative facilities are, first, whether however, they would collectively suggest that it is they are used by everyone all the time, and second, reasonable to hope for a halving of the incidence of whether they are adequately maintained. Use will be category iII, iv and v infections through improved dependent on the locality concerned: for instance, in excreta disposal facilities and concomitant supporting urban situations, where alternative defecation sites are programs for facility maintenance and health educ- scarce, it will be easier to ensure widespread use of new ation. If such programs are combined with safe water facilities. There are also both private and public aspects supply and appropriate behavioral changes, the risk to maintenance of all but basic on-site systems, and from some other serious excreta-related diseases can systems vary in their public maintenance needs (some become small, and such illnesses as typhoid and withstand public neglect better than others). cholera (category II) can cease to be endemic. The impact of improved excreta disposal on category l . . infections is likely to be small in the absence of major Best inferences In an optimal case improvements in domestic conditions, which may In the evaluation of the health benefits of excreta imply substantial socioeconomic change in the disposal, an optimal situation would be one in which community at large. everyone uses the facilities all the timne and the town council responsible for their maintenance is meticulous in its duties. A corresponding worst case would be the Limitations in Assessing Health Benefits total lack of sanitation facilities. In both cases, it is the disposal technologies rather than management sys- The planner seeks a clear, preferably monetary, tems that are the objects of comparison. The baseline statement of the health benefits of alternative sanitation improvements. The data are not adequate to 2. See, for example, Kalbermatten, Julius and Gunnerson (1982) provide one. It is quite feasible to list the present costs and Feachem, Mara and Iwugo (1980). 50 HEALTH HAZARDS OF EXCRETA situation will vary greatly in the absence of any water to a treatment plant, oxidation ponds for sewage, sanitary provisions. Where population densities are and batch thermophilic composting for night soils and high, as in many parts of rural Asia and in all the sludges, will give a safe product. Alternative processes world's major cities, the base level of disease caused by in treatment plants are inferior. excreted pathogens will be quite high. On a crude scale of ill health, this situation would be rated at 0. Where conditions include flush toilets, sewers and an efficient Best iiiferences in actUalir' treatment plant-the best case-the resulting health In the real world, of course, systems are not benefits will rate a 10 as long as water supplies are maintained impeccably, nor are facilities invariably adequate for optimal use of the sanitation system. used. Moreover, some systems clearly require less effort Although not adapted to the water use levels needed to maintain and use than others. Cartage in some for the personal cleanliness required to minimize the Japanese towns using vacuum trucks is fully compara- infections of categories I and ii (see table 2-2), pit ble to waterborne sewerage (Kalbermatten, Julius and latrines would, from the viewpoint of health rather Gunnerson 1982). In some cities in other countries, than convenience, approximate the same rating as a however, the great majority of trucks are typically out waterborne sewerage system. Because a pit latrine has of operation. Health benefits are closely tied to no effluent or product, it is in this regard safer than a operation and use, and some societies are better than sewerage system producing large volumes of a polluted others at operating particular systems. If change is effluent that is in general, even in the best treatment contemplated, much greater effort than hitherto plants, not made completely pathogen free. A rating of assumed may need to be allocated to the operation and 9 is given to pit latrines (but this rating does not apply use, rather than the installation, of new facilities. wherever fecal material might soak through latrine Operation and maintenance require both user effort walls to gain access ultimately to drinking water or and municipal endeavor, and the necessary blend wherever flooding or a high water table regularly between these differs according to the chosen recur). technology. A ranking of the various disposal Where composting, double-vault latrines (a rating of technologies by ease of maintenance for the user and 8) are used and are dug out frequently, a residual the municipality, water requirements, and the ideal (as hazard from long-lived helminth eggs persists and discussed in the section above) and actual health benefits are less. Reuse of the compost will further benefits is given in table 3-2. It should be noted that the spread the eggs in the community. The "multrum" ideal benefits vary little among processes when the composting toilet is, again, safe if operated ideally, but facilities are well maintained and used; only bucket in general its risks tend to be greater (hence a rating of latrines are intrinsically and substantially inferior. The 7) because the latrine's continuous process involves proposed ranking of actual benefits reflects variables hazards from insufficiently composted pathogens. leading to neglect of the particular facilities, but this is a An aquaprivy with a retention time longer than a very provisional evaluation, and many other factors month may yield an effluent with a low pathogen must be taken into account in selecting technology for content, but this requires the regular addition of water a given site. The infonned speculation in table 3-2 is to the tank at a rate that will not seriously reduce the intended to stimulate thought about the health-related retention time. Provided that an efficient sludge aspects of technology choice, and to draw attention to removal and treatment system is available, the the disparate advantages of the pit latrine and the resulting health benefits from the aquaprivy might bucket system. approximate 9 on the scale. A septic tank with a retention time of only 1-3 days produces an effluent rich in pathogens and therefore is associated with greater risk (a rating of 8 is assigned). With a bucket- Literature Cited latrine system, major reductions in disease are unlikely, Feachem, R. G. A., Mara, D. D. and Iwugo, K. 0. (1980). even in an ideal world, and a rating of 5 is considered appropriate. A well-managed vault and vacuum-truck Afria. Appropriate Technology for Water Supply and cartage system would be a great improvement, but Sanitation, vol. 7. Washington, D.C.: The World Bank, some risk of spillage and contact with fresh feces would Transportation, Water and Telecommunications still exist (hence a rating of 8). Department. The preceding ranks the health benefits of mainly Kalbermatten, J. M., Julius, D. S. and Gunnerson, C. G. on-site systems. If excreta are transported by cartage or (1982). Appropriate Sanitation Alternatives: A Technical RISKS TO PUBLIC HEALTH 51 Table 3-2. Ranking of exereta disposal technologies by ease of operation and maintenance, water needs, and health benefits (scale of 10) Lack of effort requiredt Healtii benefitsb Water Technology By user By municipality needs Ideal Actual Flush toilet/ sewers/oxidation ponds 10 4 H 10 9 Vault/vacuum truck 8 0 L 8 6 Pit latrine 8 5 L 9 6 Septic tank 6 5 H 8 7 Aquaprivy 5 5 M 9 6 Bucket latrine 3 1 L 5 1 Batch composter (double vault) 1 to L 8 5 Continuous composter (multrum) 0 10 L 7 3 L Low; M medium; H high. a. 0 = maximum effort; 10 = minimum effort. b. 0 = no benefits: 10 = maximum benefits. and Economic Appraisal. World Bank Studies in Water with Ascaris, Trichuris and hookworm. American Journal Supply and Sanitation, 1. Baltimore, Md.: Johns Hopkins of Hygiene, 14, 156-193. University Press. Wagner, E. G. and Lanoix, J. N. (1969). Water Supply for Latham, L., Latham, M. and Basta, S. S. (1977). The Rural Areas and Small Communities. Geneva: World Nutritional and Economic Implications oJ Ascaris Infection Health Organization. in Kenya. World Bank Staff Working Paper no. 271. Winfield, G. F. (1937). Studies on the control of faecal-borne Washington, D.C. diseases in North China. III. Family environmental factors Otto, G. F., Cort, W. W. and Keller, A. E. (1931). affecting the spread of Ascaris lumbricoides in a rural Environmental studies of families in Tennessee infested population. Chinese Medical Journal, 51, 643-658. 4 Detection, Survival, and Removal of Pathogens in the Environment THE COMMENSAL and pathogenic organisms found in concern of water supply engineers was to reduce the human feces-and the environmental characteristics incidence of epidemics of strictly waterborne disease. It of the latter's transmission and control-have been is still an epidemiologically valid testing technique for examined in earlier chapters. The focus of this chapter disinfected water supplies throughout the world, but it is on the suitability of various excreted bacteria as has certain limitations when applied indiscriminately diagnostic organisms to indicate environmental fecal in the examination of wastes and wastewaters, pollution and on the relation of these bacteria to other particularly in hot climates. (These limitations are bacterial and nonbacterial pathogens. In addition to discussed in the section "Relation of Fecal Indicator bacterial indicators, generic "pathogen indicators" are Bacteria to Excreted Pathogens," below.) proposed for assessing the safety of the products of The ideal fecal indicator bacterium should be: excreta treatments. The survival times of indicators and pathogens in different environments (the reader is C A normal member of the intestinal flora of healthy referred to Part Two in this regard) and several issues people affecting the choice of excreta treatment technologies * Exclusively intestinal in habitat, and hence ex- are analyzed in the remainder of the chapter. clusively fecal in origin when found in the environment * Absent from nonhuman animals (a requirement not Fecal Indicator Bacteria met by any of the indicator bacteria currently used) * Present whenever fecal pathogens are present, and Fecal indicator bacteria' are selected from among present only when fecal pathogens might re- those commensal species that exclusively live in the asonably be expected to be present intestinal tract of man and other warm-blooded * Present in higher numbers than fecal pathogens animals without causing disease. Because they are * Unable to grow outside the intestine, with a die-off always and naturally present in feces and are excreted rate slightly less than that of fecal pathogens in large numbers (up to 109 or 1010 cells per gram of * Resistant to natural antagonistic factors and to feces), their presence in water indicates beyond doubt water and waste treatment processes to a degree that the water has been contaminated with fecal equal to or greater than that of fecal pathogens material and possibly with excreted pathogens. If a * Easy to detect and count water is shown to contain fecal indicator bacteria, it is * Nonpathogenic. considered unsafe for human consumption. This is the rationale for the bacteriological testing of public water No one bacterial species or group completely fulfills supplies that was developed in Europe and North all these requirements, but a few come close to doing so. America at the turn of the century when the major Three main groups of bacteria are used as fecal indicators in conventional water bacteriology: the fecal 1. Fecal indicator bacteria are discussed in greater detail in coliforms, the fecal streptococci and the anaerobic chapter 13; see also specific chapters in Part Two for notes on the bacterium Clostridium perfringens. Recently, some taxonomic nomenclature of particular pathogens. other members of the anaerobic intestinal flora, 53 54 HEALTH HAZARDS OF EXCRETA notably Bifidobacterium spp., have been proposed as occurrence has prompted a search in recent years for additional indicator bacteria. Pseudomonas aeruginosa alternative, more satisfactory indicator organisms for has also been proposed, but its status as an intestinal use in hot climates. A further disadvantage of fecal organism is in doubt. An analysis of these bacteria and coliforms is that most standard enumeration pro- their uses as indicators follows. cedures require an accurately controlled incubation period at 440 or 44.5°C, which is difficult to achieve in Coliform bacteria any small, or nonspecialized, laboratory. There are two principal groups of coliform bacteria; the fecal coliforms (comprising mainly the bacterium Fecal streptococci Escherichia coli) and the total coliform group, that includes the fecal coliforms and comprises mainly The fecal streptococci (or Group D streptococci) are species of the genera Citrobacter, Enterobacter, a group of bacteria that are morphologically similar Escherichia, and Klebsiella. The former are exclusively (Gram-positive cocci, measuring approximately 1 fecal in origin, whereas the latter, although commonly micrometer in diameter and occurring in short chains) found in feces also occur naturally in unpolluted soils and are mostly found in the intestines of man and and waters. Of the total coliform organisms found in otherwarm-bloodedanimals.Thegroupincludesspecies fresh feces of warm-blooded animals, generally >90 mainly associated with animals (Streptococcus boutis percent are E. coli, the remainder being species of and S. equinus), other species with a wider distribution Citrobacter, Enterobacter, and Klebsiella (Dufour (for example, S. faecalis and S. faecium, which occur 1977). both in man and other animals), as well as two biotypes Only the fecal coliforms (and especially E. coli) are (S.fraecalis var. liquefaciens and an atypical S. jaecalis definitive indicators of fecal pollution. In water that hydrolyzes starch) that appear to be ubiquitous, bacteriology the total coliforms are regarded as occurring in both polluted and unpolluted environ- "presumptive" indicators of pollution and should be ments. These last two strains, essentially nonfecal absent from disinfected water supplies. In wastewater (although included in the group of fecal streptococci), bacteriology, however, the total coliforms are of are indistinguishable from the true fecal streptococci considerably less importance because many are under routine detection or counting procedures. nonfecal in origin and, especially in hot climates, they Because S. faecalis var. liquefaciens has been reported can multiply in the environment under suitable as the predominant biotype present at low densities conditions, so that their presence or numbers may not (below about 100 fecal streptococci per 100 milliliters; necessarily relate to either the occurrence or degree of Geldreich 1970), the usefulness of the fecal streptococci fecal pollution. In general, and despite the one report group as an indicator is open to question, especially in from India to the contrary (Raghavachari and Iyer clean water bacteriology. Yet fecal streptococci may 1939), only fecal coliforms (or better still, E. coli) still have a place in wastewater bacteriology, although should be used as indicators or tracers of fecal bacterial not as indicators of the bacteriological quality of pathogens in wastes, wastewaters, and treatment and wastewater-irrigated crops, on which the two nonfecal reuse processes. biotypes may both be present as natural flora unrelated Fecal and total coliforms are indistinguishable to the degree of fecal pollution. There is no under the microscope: they are all Gram-negative rods information, however, on the distribution of these two measuring some 2-5 by 0.4 micrometers. In practice biotypes in tropical environments. they are differentiated by the ability of fecal coliforms Aside from the possible problem of nonfecal strains (mainly E. coli and thermotolerant K. pneumoniae) to of Group D streptococci, fecal streptococci have major ferment lactose with the production of acid and gas advantages as fecal indicators. They are enumerated by within 24 to 48 hours at a temeprature of 44°C. In a single-step membrane-filter procedure at 37°C, a addition, the most common fecal coliform, E. coli, can temperature readily attained in small field labora- produce indole from the amino acid tryptophan at this tories. They are less prone to regrowth, and generally temperature. In hot climates, however, some nonfecal survive somewhat longer, than fecal coliforms and may coliforms can grow at 44°C and some can also produce thus be better indicators of excreted bacterial indole at this temperature, thus mimicking the fecal pathogens (that have little regrowth tendency) and coliforms (E. coli in particular). There are no excreted virus (that survive for longer than fecal satisfactory routine methods for differentiating be- coliforms in cool waters). These points are discussed in tween these organisms, and their simultaneous greater detail in chapter 13. DETECTION, SURVIVAL. AND REMOVAL OF PATHOGENS 55 Fecal coliform tofecal streptococci ratio length by 1-2 micrometers in width. It is exclusively It has been found that human feces in the USA fecal in origin and is also pathogenic, causing gas contain at least 4 times as many fecal coliforms as fecal gangrene and food poisoning (Chakrabarty, Narayan and Chandiramani 1977). Because it is a spore-forming times . streptococci,t a fec ai atleas.4 organism, it can persist for long periods outside the times as many fecal streptococci as fecal cohiforms inetn,adteeoecnb sda nidctro (Geldreich 1966). It was therefore suggested that intestine, and therefore can be used as an indicator of American surface waters that have fecal coliform- occaslional or watermittent polluthonp or of previous streptococci ratios of > 4 are likely to have received pollution of waters In which the presence of neither streptococinrantiosh pof ll4tare,likelyet thae receivd fecal coliforms nor fecal streptococci can be demon- ratios of <0m 7 mainly have been contaminated by the strated (Bisson and Cabelli 1980; Cabelli 1977). C. raio of <0. manyhv.encotmntdbh pe7:fringe71s iS also more resistant than both fecal feces of wild and domestic animals (Geldreich 1966). . r . . . This method, however, is of no value in practice. The coliforms and fecal streptococci to antagonistic ' ' . . . ~~~~~~substances such as chlorine. fecal coliform-streptococci ratios in fresh feces vary widely in different animal species and geographical In wastewater bacteriology, however, its long persistence is a disadvantage because residual, locations. It is not true that humans the world over dormant populations of the bacterium in waters may excrete a ratio of >4, and animals <0.7 (Wheater, nor reflect the true degree of pathogenic contamin- Mara and Oragui 1979). Once the feces have been ation. Type A C. perfringens from human feces may excreted, the ratios will change because of the also grow in the soil (in contrast to other types of C. differential death rates of the various bacteria. The .g . . enterococci (S. flaecalis, S. faecium, and S. dur-ans) perrilngens of anm.al origin, which seem to die-out in typically survive longer than fecal coliforms which in soil). turn survive longer than S. bovis and S. equinus (McFeters and others 1974). It was therefore suggested Pseudlomonas aerugi72osa that for human pollution, in which enterococci are the The organism is an opportunistic human dominant fecal streptococcal species, fecal.coliform- pathogen that causes infection in wounds (especially streptococci ratios in water samples returned to the burns) and also ear and urinary tract infections, laboratory will fall; whereas for animal pollution, m a o n which S. bovis or S. equinus may be more numerous, the meigts'eprtr netosadohrcniin whics. iorstor s.pes may be morem numerut (Cross 1979). It is often associated with sepsis in ratios in stored samples may rise (Feachem 1975). But ohriedblttdptet nhsia ad.P it nw apearsthat wheeas ntercocc arethe otherwise debilitated patients in hospital wards. P. domitnow aecars that,cweralspenteroin har the aeruginosa is being increasingly implicated as a cause dominant fecal streptococcal species in humans inoma neto n knrs olwn xouei developed countries (and therefore human pollution is of ear yfectlion and skm rash followlng exposure l associated with falling ratios), enterococci can also be poolebaths (cson,eHoad and Fam r17 the dominant fecal streptococcal species in some McCausland and Cox 1975 Seyfried and Fraser 1978; animals (for instance, cats, ducks, hens, mice, pigs, Waushund and Cot 1976). rabbits, rats, and seagulls in Scotland; Wheater, Mara and Oragui 1979). Furthermore, S. equinus and S. bovis P. aeruginosa is a Gram-negative, aerobic, nonspor- are common in the feces of people in some countries ulating rod measuring approximately 0.5 by 2 micro- meters. It occurs, normally at low concentrations of (for intance, India and Uganda; Drasar and Hill 1974). abu 50ognssprga,intefcso' ml It may be concluded, therefore, that neither the ratio at about 50 organisms per gram m the feces of a small the time of sampling, nor the change in ratio in a stored proportion (about 3 to 15 percent) of healthy people. It sample, conveys useful information about the origins of probably does not grow in the intestine of healthy fecal pollution. The development of a routine test to people, and P. aeruginosa isolated in feces may be fectiolutio Th developmen t ofea rounetest survivors of ingested bacteria. Studies in which P. dstiongisthe human from nonhma f.earctin aeruginosa was fed to volunteers demonstrated that sation miscthe bighest currentpriort y fo r ragesearc i large numbers (Ž, 106) must be ingested to produce fecal carriage, which did not persist for more than 6 days (Buck and Cooke 1969). Closti-idiur/t pe7yi-ingenis P. aeruginosa is common in sink traps and flower water. It has been reported in fairly high concentra- The bacterium Clostridiuni perfi ingens (formerly C. tions (> 103 per 100 milliliters) in urban stormwater welchii) is anaerobic, spore-forming, Gram-positive, runoff in Canada (Qureshi and Dutka 1979), and in and measures approximately 4-6 micrometers in higher concentration in sewage (> 105 per 100 56 HEALTH HAZARDS OF EXCRETA milliliters) and hospital sewage (> 106 per 100 Fecal concentrationis, detection, andl enumeration qJ milliliters) in Scotland (Wheatcr and othcrs 1980). It bacterial indicators has been suggested (Cabelli, Kennedy and Levin 1976) that a consideration of P. aerugittosa-E. coli ratios in Approxlmate numbers of indicator bacteria co4 - fecally contaminated waters can provide evidence on monly found in human feces are given in table 4-1. The the possible origins of the pollution, with coun cell counts in the table are average figures only and >100fecal coliforms and < 1 P. alerulginlosa per 100 are mainly derived from American literature. Some 1lt,000 fers being and p.ttieithganima communities, because of dietary differences (see table milliliters being associated putatively with animal. 1-6), may display considerably different numbers for rather than human, pollution. But P. aeruginosa occurs rathe than human, pollution. ButP . aeruginosaoone or more of the listed indicators (see also chapter widely (albeit in highly variable numbers) in nature as a 13) free-living organism (Green and others 1975; Parker 13). e 1 r ^ r ~~~~~~Methods suitable for the detection and enumeration 1971); it can therefore have little usefulness in studies of of coliform bacteria, fecal streptococci, and C. fecal contamination. pefrfingens are described in the 15th edition of Standard Methods for the Examination oJ Waters and Bt ,1..4., and other anaterobic bacteria Wastewvaters (American Public Health Association Bifidobacteria (previously known as anaerobic 1980) and in the 4th edition of The Bacteriological E.xamination oJ Water Supplies (Department of Health lactobacilli) are nonsporulating, anaerobic organisms andnSoiety Ser 1969). A membrane-filter that occur in the intestines of man and other animals: they areGram-positiveV- orY-shapedcells, with each technique for enumerating C. peirringens is also branch measurinabu 0b to 4 cetes. the described by Bisson and Cabelli (1979). P. aeruginosa branch marnat. T populations can be counted by membrane filtration most common species in man are Br, .i.l;,; :rnum? adolescent ismand B.s in gum.nar BiFidobacteriauhave using the medium of Levin and Cabelli (1972) rdolescently beenp d as lnindic. ator anisms frue supplemented with 0.1 percent cetrimide (Wheater and recently been proposed as indicator organisms for use ohr 90 e loBosyadCei 98 uk in topial wter becusethelactose-fermenting others 1980; see also Brodsky and Ciebin 1978; Dutka in tropical waters because the r and Kwan 1977; Hoadley 1977). The membrane species are exclusively fecal in origin (Cabelli 1978; . filtration method and medium for Bfifdobacterium spp. Levin 1977). Thev therefore overcome the principal are described by Evison and Morgan (1978), but no disadvantage of fecal coliform counts on tropical satisfactory routine procedure for enumerating these samples that such samples may contain a significant bacteria has yet been developed. Reference may also be proportion of strains that can ferment lactose and made to Mara (1974). FsSee note on page 66.] produce indole at 44°C but do not derive from feces. An additional advantage of bifidobacteria is that, because they are strict anaerobes and grow poorly below 30°C, Relation of Fecal Indicator Bacteria to they have very low multiplication potential in Excreted Pathogens extraintestinal environments. Work on bifidobacteria has only commenced relatively recentlv. and there is little informatin on tFecal indicator bacteria were originally identified to littleinvironments ot thanrsurviva in ri w terainesoinand assess the bacteriological quality of potable waters at a Morganm1978) other than in riverwater Evisonand time when only the transmission of bacterial Morgan 1978). The bacterial flora of feces is predominantly composed of anaerobic bacteria (table 1-6). Bifido- Table 4-1. Number oj indicator bacterica commonlv bacteria have been described, but feces contain large fiund in humanjeces numbers of other nonsporulating anaerobes. such as Bacteroides spp. (commonly B. j a ,i , the anaerobic Cells per grain oj fece.s Gram-positive cocci (Peptoccus spp. and Peptostrepto- Incdicu tor (xwet weight) coccus spp.) and Eubacterium spp. Current research is investigating the usefulness of these organisms as fecal BuctreoidIes spp. lo--lo, indicators, but at present there are insufficient data on Bifidobacterhion spp. 10- 10'' their extraintestinal ecology to know whether or not Clostridiun, pertrin,gen7S 103_01") use of all or some of them as indicators will be Coliforms Fecal 106-0o, practicable. Moreover. current techniques for their Nonfecal t0-109 detection and enumeration are rather complex for Fecal streptococci V510-1 routine use. DETECTION, SURVIVAL, AND REMOVAL OF PATHOGENS 57 enteropathogens (such as salmonellae, shigellae, and pathogens are considered, the bacterial fecal indicators cholera vibrios) was considered the major public are of limited usefulness. They are of some use in health risk from drinking water. Historically (and to assessing the quality and resulting risks to health of some extent, even now), attention has therefore focused irrigation waters, but even here the gaps in knowledge on the relation of the fecal indicators to bacterial are considerable. Much of the existing information on pathogens. Recent literature, continuing this emphasis, the relation of fecal indicators and excreted pathogens contains many reports on the persistence of fecal comes from relatively wealthy communities (for coliforrms and salmonellae in the extraintestinal example North America, South Africa, and Israel), and environment, but only a few reports on the these data cannot be applied with much confidence to comparative survival of the fecal indicators and other communities in which climate, diet, disease nonbacterial fecal pathogens (such as viruses, pro- patterns, agricultural practice and cultural attitudes to tozoal cysts, and helminth eggs). This has partly been a excreta reuse products are all different. This does not result of the difficulty of routinely analyzing samples mean that information on, say, fecal coliform survival for these other pathogens (especially viruses), but an in Israel cannot be used to predict fecal coliform uncritical acceptance of the historical direction of survival in, say, rural India but it does mean that the research in the field has also contributed to the neglect. information may not be all that relevant to conditions Thus, for example, there has been no report on the in rural India, where the ability to make statements relation of the indicator bacterium C. perfringens and about fecal coliform survival may not help assess the the eggs of the fecal helminth Ascaris lumbricoides degree of fecal pathogen contamination of crops (both persist for longer periods in the extraintestinal irrigated with sewage effluent or fertilized with treated environment than do other organisms of their excreta. Caution must therefore be exercised in respective kind). Knowledge of such a relation would applying data on fecal indicator survival in environ- be of little value in assessing the safety of urban water ments other than those from which the information supplies (in which Ascaris eggs are not a public health was obtained. hazard) but it might be of assistance in assessing the In summary, little is known about the relative quality of sewage sludges, composted feces, and some concentrations of indicator bacteria and bacterial wastewater effluents. pathogens in effluents and fecal products in warm This one example illustrates the longstanding climates and practically no information exists on the preoccupation of sanitary bacteriologists with urban relative concentrations of indicator bacteria and water supplies to the near exclusion of appropriate nonbacterial pathogens. In addition, it must be noted consideration of wastes and wastewaters, and of the that the stability of the ratio between the concentration comparative removal and persistence of fecal pa- of an indicator bacteria and the concentration of a thogens and indicator bacteria in treatment processes particular pathogen decreases as the size of the and reuse products. There are many data (mainly from contributing population decreases. Thus, for systems North America and admittedly of variable quality) on serving small communities, or for individual systems the relation between the survival ofbacterial pathogens such as aquaprivies or composting toilets, the ratios and indicators in sewage treatment processes in will vary enormously from place to place and from time temperate climates, but very little data from tropical to time, and no organism will act as a good indicator of countries. Predicting with confidence the likely density another organism. of salmonellae in a tropical sewage effluent, even when the number of fecal coliforms present is known, is extremely difficult; in contrast, reasonable estimates Pathogen Indicators are possible with a temperate climate effluent. This neglect makes the establishment of a fecal coliform Fecal indicator bacteria only demonstrate fecal standard for most tropical sewage effluents a highly contamination. This fact is useful in assessing the safety unscientific process. Because engineers design, for of drinking water supplies, but when the health aspects example, maturation pond systems on the basis of fecal of sanitation systems, excreta and sewage treatments coliform removal to the desired standard, this state of and reuse processes are considered, what is needed is scientific uncertainty can lead to either overdesign not a fecal indicator bacterium (for feces are obviously (with a consequent unnecessary increase in cost) or present) but, rather, a pathogen indicator organism. A underdesign (with a consequent increased risk, and reliable measure ofthe total pathogen content ofthe end perhaps actual damage, to public health). product of a treatment process is needed, so that the When the hazards from nonbacterial excreted health risks associated with any reuse of the end 58 HEALTH HAZARDS OF EXCRETA product, or with its discharge into the environment, can fecal coliforms and fecal streptococci are perhaps the be gauged as accurately as possible. If these risks can be best pathogen indicators. It is difficult to determine judged, responsible and informed decisions can be what density of fecal coliforms or fecal streptococci- made-for instance, on whether the benefits from end- as an indication of the presence of endemic product reuse outweigh the possible health costs and pathogens should be permissible. The rather unhelp- whether further treatment is necessary to protect the ful answer is that the densities should be as low as health of those involved (either as producers or possible, which in practice means at least below 1,000 consumers) in the reuse process or, in the case ofthe end per 100 milliliters of effluent (and preferably below 100 products being discharged into the environment, of the per 100 milliliters). Effluents reused for the irrigation of users of the environment. crops that may be consumed raw must have fecal It would be unrealistic to expect the same pathogen coliform and fecal streptococci counts that are both indicator organism to be useful in assessing the below 100 per 100 milliliters. Viral and bacterial pathogen content of different kinds of fecal products pathogens may or may not be absent at these indicator for example, composted feces and the effluent from organism densities, but in general health risks will be waste stabilization ponds. In the former case the so minimal that further treatment will not normally be concern is primarily the viability of the persistent economic. helminth eggs (notably Ascaris Itlmbricoides eggs) whereas in the latter case it is known that, if the total .. . . ~~~~~~Pathogeii indicatorsfor , ni-,, -;i fi-om other sewzage retention time in a stabilization pond system is more Pathenir than 20 days, the effluent will be free of both helminth treatments eggs and larvae but may contain excreted viruses and The effluents produced by sewage treatment bacteria. Because of these variations, it is convenient to processes other than waste stabilization ponds are divide fecal products into two groups, effluents and likely to contain a full range of fecal pathogens- noneffluents, and to examine which organisms are viruses, bacteria, protozoal cysts, and helminth eggs. suitable pathogen indicators for each. There is no suitable fecal indicator organism in these circumstances; it is not possible to have a single organ- Pathogen indicatorsj. r pond ism indicate the presence of so diverse a group of pathogens. Fecal coliforms have been used, but only for The effluents from waste stabilization ponds and historical reasons (they are totally inappropriate other sewage treatment processes are best considered indicators for the helminth eggs for instance). This separately because the vastly different retention times subsection can conclude with the generalization that if involved (weeks in ponds, hours or days in other a sound economic argument can be put forward for the processes) produce effluents with markedly different use of treatment processes other than ponds, then the pathogen contents. If a pond system has a retention effluent from such treatments should undergo tertiary time of more than 20 days its effluent will be free from treatment or be heavily disinfected or discharged well both pathogenic protozoa and helminth eggs and out to sea because, in the tropics, the health risks from larvae, but it may still contain viral and bacterial the effluent may be similar to those from raw sewage. It pathogens. Because a routine analysis of pond effluents should be noted that heavy disinfection is often for pathogenic viruses and bacteria is not yet feasible ineffective (especially against viruses and helminth (nor likely to become so in the immediate future), the eggs) and has undesirable environmental con- choice of a suitable pathogen indicator is exceedingly sequences. difficult. Bacteriophages--and more specifically, coli- phages--may provide a solution in the future but the Pathogen indicators.]br laboratory techniques are not yet widely known. Fecal coliforms or fecal streptococci would seem an obvious Noneffluents are taken here to include night soil, the choice, but there is little data on the usefulness of either contents of pit latrines and composting toilets and the as viral indicators, and the literature on their respective sludges from aquaprivies, septic tanks and con- survival compared to pathogenic bacteria is only ventional sewage treatment works. It is reasonable to slightly less scant (especially for tropical pond assume that, if ascariasis is endemic and there are no effluents). There is no information available on the viable Ascaris eggs present in the wastes analyzed, then usefulness of bifidobacteria and the other non- sporulating anaerobes. 2. Effluent disinfection is discussed further in chapters 6,9, 13, and Although they are less than ideal for the purpose, 23. DETECTION, SURVIVAL, AND REMOVAL OF PATHOGENS 59 other pathogens are absent as well, since Ascaris eggs environmental condition likely found in a night soil or are so resistant. Thus, and in the current absence of any sewage treatment system that is highly fatal to all data on the comparative survival of the bacterium C. pathogens in a reasonably short time (a few hours) is perfringens, the viable eggs of Ascaris lumbricoides raised temperature (in the range 55-65°C). The only would appear to be the best pathogen indicator other low-cost process that causes 100 percent removal currently available for noneffluents. This indicator has or destruction of most pathogens is the waste been accepted in China, where standards of 95 percent stabilization pond system with its long retention times, Ascaris egg mortality have been adopted for the exposure to sunlight, and good sedimentation proper- agricultural reuse of excreta (McGarry and Stainforth ties. 1978). The elapse of time is a feature common to all treatment, disposal and reuse technologies; in many cases, it is the feature that most determines the Survival of Indicators and Pathogens pathogen removal achieved. The rate of loss of infectivity of an organism also depends very much on From the time of excretion, the concentration of all temperature; most organisms survive well at low pathogens usually declines from the death or loss of temperatures (; 5°C) and rapidly die at high infectivity of a proportion of the organisms. Viruses temperatures (>40°C). Except in sludge or night soil and protozoa will always decrease in numbers digestion processes, temperatures approximate following excretion, but bacteria may multiply if they environmental temperatures-in most developing find themselves in a suitably nutrient-rich environment countries, generally in the range of 1 5-350C and with a minimum of competition from other micro- commonly of 20-30°C. It is therefore useful to know organisms. This can occur when salmonellae, for the persistence of pathogens at ambient temperatures instance, contaminate certain foods, or when E. coli in different environments so that the likely pathogen multiply in a chlorinated sewage effluent from which content of various fecal products can be predicted. In many other bacteria have been eliminated. Multi- this section pathogen survival at ambient temperatures plication of bacterial pathogens is generally rare, is reviewed with the following considered in turn: however, and is unlikely to continue for very long. survival in feces, night soil and sludge; survival in water Intestinal helminths-except the trematodes, which and sewage; survival in soil; and survival on crops. have a multiplication phase in their molluscan Under each heading that follows, the available intermediate hosts-will decrease in numbers follow- knowledge is summarized as succinctly as possible. A ing excretion. The multiplication possibilities for the greal deal of additional information is given in Part excreted pathogens were summarized in table 2-3. Two and some of the data are further tabulated in The ability of an excreted organism to survive is Feachem and others (1980). defined as its persistence (discussed in chapter 2). The The shape of the curve describing pathogen survival natural death of organisms when exposed to a hostile over time should determine the way in which survival is environment is of the utmost importance because it reported. Many bacterial populations decline expo- reduces the infectivity of excreta independently of any nentially, so that 90 or 99 percent of the bacteria are treatment process. In fact, some treatment processes lost relatively quickly with a few organisms persisting have little effect on excreted pathogens and simply for longer periods. Such a situation is best described by allow the necessary time for natural die-off to occur. the probability of survival for a given time or by half The effect of conventional sewage treatment on life, the time required for half the population to die. For protozoal cysts is of this kind (see chapter 20). Certain instance, 50 percent of fecal coliforms may die in 20 treatment processes, however, create conditions that hours in water, whereas a few may persist for up to 50 are particularly hostile to excreted pathogens and that days, and the results obtained will depend heavily on promote their rapid death. The effects of activated sampling procedures. Most of the literature gives data sludge on fecal bacteria, or of thermophilic digestion on the persistence of the small proportion of long-term on all organisms, are of this kind. The essential survivors and only a few authors have reported the environmental factors in limiting pathogen persistence shape of the death curve or given the 50 to 90 percent are time and temperature. The success of a given destruction times. The discussion below will therefore treatment process in reducing the pathogenicity of an mainly concern the overall persistence of a few effluent or sludge thus depends, in general, upon its organisms. This focus is epidemiologically appropriate retention time and its creation of an environment for organisms that can replenish their numbers if they especially hostile to particular organisms. The sole find themselves on food or other suitable substrates 60 HEALTH HAZARDS OF EXCRETA (for example shigellae, salmonellae and pathogenic E. are summarized in table 4-3. For all organisms survival coli) or for organisms whose infective dose is believed is highly dependent on temperature, with greatly to be low (the excreted viruses, for example). It is less increased persistence at lower temperatures. Survival appropriate for cases in which regrowth is unlikely and of bacteria is also highly dependent on the presence of infective doses may be high (for example, Vibrio other microorganisms in the water that might provide cholerae); in these cases it is the rapid decline of the competition or predation. Bacteria often survive bacteria to a level that no longer presents a major longer in clean water than in dirty water and the public health hazard that is important. In organisms longest survival times are obtained by inoculating a having several developmental stages outside the single bacterial species into sterilized polluted water. human host (such as hookworms and schistosomes), There is some evidence that virus survival is enhanced each stage will have its own separate survival pattern. in polluted waters, presumably a result of some When a developmental stage is actively moving yet protective effect that the viruses may receive when they dependent on an unreplenished energy source (for are adsorbed onto solid particles in dirty water (see example, the schistosome miracidium seeking its snail chapter 9). Coliforms, in particular E. coli, have host) the length of life may be precisely defined. attracted the most interest because of their established role as indicator bacteria. Substantial regrowth of coliforms is possible in organically polluted waters, but In fe?ces, night soil, and sludge this growth phase will give way to a progressive die-off. There is less literature on the survival of pathogens in Survival in excess of 50 days is most unlikely and, at these media than in the aqueous environments 20-30°C, 20 days is a more likely maximum survival discussed in the following subsection. Some sources time. Mixed fecal streptococci have a similar (perhaps a refer to survival of pathogens in sewage works' sludges, little longer) survival but, if the streptococci are but survival in feces and night soil may be assumed to predominantly S. bovis or S. equinus, the survival times be broadly similar. Research on pathogen survival in are substantially shorter (see chapter 13). aiim- "di these media may be summarized as shown in table 4-2.' survival has also been widely reported. Survival of over 2 months has been recorded, but 1 month is a more common upper limit (see chapter 15). Shigella spp. and In wrater and seusage Many studies on the survival of excreted organisms Table 4-3. Survival times of excreted pathogens in in water and sewage have been conducted.' The data fresh water and sewage at 20-30'C Table 4-2. SUtrvivcal times of excreted pathogens in feces. night soil, and sluidge at 20-30oC Survoival time ____________________'_________ Pathogen (days) Survival time Virusesa Pathogen (days) Enteroviruses' < 120 but usually <50 Viruses Bacteria EVterovirusses < I 00 but usually < 20 Fecal coliformsa <60 but usually <30 Salnmonella spp.a < 60 but usually <30 Bacteria Shigella spp.3 <30 but usually <10 Fecal coliforms <90 but usually <50 Vibrio choleraec <30 but usually <10 Salmonella spp. <60 but usually < 30 Protozoa -_= ,. spp. <30 but usually <10 EntaPoebahistolvocacysts <30butusually <15 liibrio cholerae <30 but usually <5 Protozoa Helminths 1l ~~~~Ascaris lumbricoides eggs Many months Enrtamoeba histoltrica cysts <30 but usually <15 Helminths a. In seawater, viral survival is less, and bacterial survival is very Ascaris lumbricoides eggs Many months much less, than in fresh water. b. Includes polio-, echo-, and coxsackieviruses. a. Includes polio-, echo-, and coxsackieviruses. c. 1V cholerae survival in aqueous environments is a subject of current uncertainty-see chapter 17. 3. A compilation of original sources and findings on survival in feces, night soil, and sludge can be found in the appropriate sections 4. These studies are reviewed in the appropriate sections of Part of Part Two. chapters 9 through 35. Two, chapters 9 through 35. DETECTION, SURVIVAL, AND REMOVAL OF PATHOGENS 61 Vibrio cholerae are less persistent, and survival of these Table 4-4. Factors affecting survival time of enteric bacteria for more than 20 days is seldom reported (see bacteria in soil chapters 16 and 17). The development of viral detection techniques in the Soiljactor I u_, oni bacterial surcival 1950s led to the demonstration of the presence of excreted viruses in the environment. The enteroviruses Antagonism from soil (polio-, coxsackie-, and echoviruses) have been microflora Increased survival time in sterile soil frequently isolated from water and wastewater Moisture content Greater survival time in moist soils and (chapter 9) and the literature on this subject is growing during times of high rainfal (chaptery 9) Moisture-holding Survival time is less in sandy soils than rap1dly at the present tzme. V1ral surv-1val may oe capacity in soils with greater water-holding longer than bacterial survival and it is greatly increased capacity at lower temperatures. In the 20-30'C range, 2 months Organic matter Increased survival and possible re- seems a typical survival time, whereas at around 10'C, growth when sufficient amounts of 9 months is a more realistic figure. organic matter are present 9mns1amrratcfuepH Shorter survival time in acid soils Protozoal cysts are poor survivors in any environ- (pH 3-5) than in alkaline soils ment. A likely maximum for Entamoeba histolvtica in Sunlight Shorter survival time at soil surface sewage or polluted water is about 20 days (see chapter Temperature Longer survival at low temperatures: 20). Helminth eggs vary from the very fragile to the very longer survival in winter than in persistent. The most persistent of all are Ascaris eggs, summer which may survive for a year or more (see chapter 23). Source: Adapted from Gerba. Wallis and Melnick (1975). In soil but Ascaris eggs can survive for several years (see Survival times in soil are relevant in all situations chapter 23). The situation is summarized in table 4-5. where effluent, sludge, compost, or other fecal products are being applied to the land as fertilizers or soil conditioners.5 Several factors, shown in table 4-4, affect On crops the survival time of enteric bacteria in soil (Gerba, Excreted viruses and bacteria cannot penetrate Wallis and Melnick 1975). Fecal coliforms can survive undamaged vegetable skins. However, there are many for many months under optimal conditions. In warm reports in the literature on the isolation of all kinds of climates, especially when arid, survival is limited to 2-3 excreted pathogens from the surface of vegetables that months at most. Fecal streptococcal survival is likely to have been irrigated or fertilized with fecal products.6 be longer if human enterococcal species are dominant Root vegetables are more prone to contamination than (see chapter 13). Survival of salmonellae may be up to 1 others. Weather conditions have an important year if the soil is cool, moist and rich in organics (for example, if it is fertilized), but strain variation is Table 4-5. Survival times of excreted pathogens in considerable and 50 days would be a more typical soil at 20-30°C maximum (see chapter 15). Data on NhŽliy,ul or Vibrio cholerae survival in soil are limited (see chapters 16 and Survival time 17). Pathogeni (days) The information available on viruses suggests that virus particles adsorb to soil particles and become Viruses protected from environmental factors. Viral survival is Enterovirusesa < 100 but usually < 20 greater at low temperatures: survivals of up to around Bacteria 3 months have been reported in warm weather, Fecal coliforms <70 but usually <20 increasing to around 5 months in European winter Salmonella spp. <70 but usually <20 conditions (see chapter 9). Protozoal cysts in soil are Vibrio cholerae <20 but usually <10 most unlikely to survive for more than 10 days (see Protozoa chapter 20). Helminth egg survival varies enormously, Entamoeba histolytica cysts <20 but usually < 10 Helminths 5. A comprehensive review of the persistence of excreted Ascaris lumbricoides eggs Many months pathogens in soil is contained in the appropriate sections of Part Two, chapters 9 through 35. a. Includes polio-, echo-, and coxsackieviruses. 62 HEALTH HAZARDS OF EXCRETA influence on the survival of pathogens on plants; The emphasis in the literature on the exact warmth, sunshine, and low air humidity greatly proportions of pathogens removed by various treat- promote pathogen death. The survival characteristics ment processes is thus misleading. For instance, most of various excreted organisms on crops may be conventional treatment plants remove 90 to 99 percent summarized as shown in table 4-6. As indicated in the of enteric bacteria.' This is a very poor removal; table, pathogen survival times on vegetables are short whether trickling filters remove a little less (say 95 compared to survivals in other environments. percent) than activated sludge plants (say 99 percent), Protozoal cysts are rapidly killed. Viruses, bacteria, they are both technologies with poor pathogen and worm eggs survive for longer, but little survival of removal characteristics (but they were never designed any species is to be expected after 2 months. to have them-see the next section). A removal ability of less than 99 percent means always more than 1 percent survival, or always less than a log unit Pathogen Survival versus Removal in reduction of 2. In developing countries, where Waste Treatment incoming wastes have high concentrations of pa- thogens (especially viruses, bacteria, and protozoal Pathogen survival, rather than pathogen removal, is cysts-see table 1-10), a survival of more than 1 percent purposely referred to in this book. This is because is usually inadequate. health hazards are posed by the pathogens that survive In considering treatment technologies by their a treatment process, not by those that are removed by ability to remove pathogens, it is necessary not to dwell treatment. Figures such as 99 percent or 99.9 percent on trivial differences (for instance, 92.3 percent versus removal appear highly impressive but they represent 1 97.8 percent removal), but to translate removal or 0.1 percent survival, respectively, and this degree of efficiencies into orders of magnitude. Conventional survival may be highly significant wherever incoming treatment works remove between 1 and 2 log units of concentrations are great. If an influent to a sewage enteric bacteria and should be contrasted with works contains, say, 105 pathogenic bacteria per liter, technologies, such as waste stabilization ponds, which then 99 percent removal will produce an effluent with remove 5 log units. In considering stabilization ponds 103 pathogenic bacteria per liter. In areas where the or thermophilic digesters, which have high removal effluent is to be reused, or where it is to be discharged to performances, it is also misleading to talk in terms of a stream that populations downstream use as a source percentage removal (use of this convention disguises, of drinking water, such effluent quality may be for instance, the important difference between 99.99 inadequate. and 99.999 percent removal). The removal characteristics of treatment techno- Table 4-6. Survival times of excreted patihogens on logies should be related to the incoming con- crops at 20-30°C centrations of particular pathogens, to the intended reuse or disposal arrangements, and to the associated Survival time health risks. Different pathogens occur in varying Pathogen (days) concentrations and are affected in different ways by a given treatment technology. For instance, protozoal Viruses cysts will be found in raw sludge in relatively low Enterovirusesa <60 but usually <15 numbers and will not survive sludge treatment. In Bacteria contrast, Ascaris eggs may be found in sludge in high Fecal coliforms <30 but usually <15 concentrations and will survive most sludge treatment Salmonella spp. <30 but usually <15 processes. s... .: . spp. < 10 but usually < 5 Vibrio cholerae <5 but usually <2 Protozoa Objectives of Night Soil and Sewage Entamoeba hsistolNtica cysts <10 but usually <2 Treatments Helminths The primary objective in the treatment of night soil or sewage from communities in which excreted infections are endemic is the destruction of excreted a. Includes polio-, echo-, and coxsackieviruses. 7. The processes that conventional sewage treatment comprises. 6. These reports are reviewed in the appropriate sections of Part and their ability to remove various excreted pathogens, are discussed Two, chapters 9 through 35. in chapter 6 and reviewed at length in the chapters of Part Two. DETECTION, SURVIVAL, AND REMOVAL OF PATHOGENS 63 pathogens. This is principally achieved by a com- excreted pathogens will be present (see table 5-1). bination of time and temperature, although other Composting toilets thus have definite health risks that, conditions of the extraintestinal environment are also although slight, should be recognized by the designers important (for example, sunlight and oxygen availab- and users of these systems. In strictly economic terms ility). From the extensive literature review in part 2, it the value of the compost must be greater than the appears that no excreted pathogen-with the excep- possible cost to health from its use. tion of spore-forming bacteria (for example C. The health hazards associated with the collection of perfringens) and possibly hepatitis A virus-can night soil from bucket and vault latrines are described survive a temperature of more than 65°C for a few in the section "Cartage Systems" in the next chapter. If minutes. As the temperature falls survival increases; urine is collected as well as feces, the night soil is a fecal thus, at 10°C, for instance, Ascaris eggs may survive for suspension similar to primary sewage sludge and may several years, enteroviruses for 12 months, and be treated by mesophilic or thermophilic digestion. It shigellae for 2-3 months. also may be treated in a pond system which can be The degree to which night soil and sewage are designed to produce little effluent so that very long treated is largely influenced by what is to be done with retention times are possible (> 1 year) and, con- the sludge, compost or sewage effluent.8 It is thus sequently, no survival of excreted pathogens. If the accepted engineering practice to discharge untreated urine is not collected, or is allowed to drain away, the sewage into the sea, provided that the outfall is night soil (now principally feces) may be disposed of, designed to ensure that no pollution of beaches or treated, and reused in a number of ways (see also the shellfish-growing areas will occur; but if reuse of an section "Composting" in chapter 5). Night soil cartage effluent for the irrigation of edible crops is intended, the and treatment systems will tend to have higher health designer's goal should be the absence of excreted risks than many other systems, although risks can be pathogens on the surface of crops, and he should greatly reduced by the use of modern methods (such as accordingly design the treatment works for a very low those found in Japan). In high-density urban settings, degree of pathogen survival. where the only technological alternative may be a sewerage system, cartage systems will often be economically attractive despite their health hazards. In other settings, where a greater range of technologies The effectiveness of treatment methods for excreta is feasible, cartage may be less attractive. and night soil depends greatly upon their time- temperature characteristics. The effective processes are Sewage treatment those that retain the excreta for a long time (> 1 year), or make it warm (>55°C), or effectively combine Those whose job is to select and design appropriate adequate retention time and high temperature. systems for the collection and treatment of sewage in Pit latrines (see the section of that title in the next developing countries must bear in mind that European chapter) have a useful life of a few years; when one and North American practices do not represent the becomes full, a second is dug, and the contents of the zenith of scientific achievement, nor are they the first are left undisturbed while the second is in use. product of a logical and rational design process. Because of the time interval there are no health hazards Rather, treatment practices in the developed countries associated with digging out the contents of previously are the product of history, a history that started about filled and covered pit latrines. Provided the squatting 100 years ago when little was known about the plate is regularly cleaned, pit latrines pose no greater fundamental physics and chemistry of the subject and risks to health than do flush toilets (though insect when practically no applicable microbiology had been breeding can be a serious problem-see chapters 36 discovered. Only since 1970 have the tools to do serious and 37 and odor can be a nuisance). work in water and wastewater virology been Composting toilets (see the section of that title in the developed, and only since 1975 have the roles of next chapter) are of two types: batch and continuous. If rotavirus, Campylobacter, and E. coli9 in the etiology of the composting period is over 1 year, only a few Ascaris diarrheas been demonstrated. eggs will be present in the product. With composting periods of under 1 year, varying numbers of other 9. The epidemiology of infections with rotavirus, Campylobacter, 8. Treatment strategies for different reuse and disposal practices and pathogenic E. coli are reviewed in chapters 11, 12, and 13, are discussed in chapter 7. respectively. 64 HEALTH HAZARDS OF EXCRETA The historical development of European and North 35°C, allow high pathogen survivals, and the full range American sewerage systems can be roughly summar- of excreted pathogens present in the raw sewage ized as follows: appears in the effluent. The sludges produced in conventional sewage works and oxidation ditches also .. A n e fcontain the full range of excreted pathogens and An the consequentisks to hualor the l.e .to e require some form of treatment before disposal or and the consequent risks to health ledt to the rue reuse. construction of sewers that discharged raw wastes Conventional sewage works were originally de- into rivers (in the mid-nineteenth century in veloped in order to prevent gross organic pollution in London, for instance). European and North American rivers; they were never * This discharge of raw wastes yielded massive intended to achieve high removal of excreted pollution and oxygen depletion in the rivers, which pathogens. Their use in tropical countries in which often became foul, open sewers. excreted infections are endemic is only justifiable in Varousce te s echnologes were developede special circumstances, for there is an alternative reduc the suspended load and the oxygen demand treatment process much superior in obtaining low of the discharged wastes (for example, the UK Royal s o e Cmiso on Seag Dipoal, 189195 survivals of excreted pathogens-the waste stabiliz- Commission~~~~~~ ~ on Seag Dipsl'19 95 ation pond system."1 Retention times commonly proposed effluent standards of < 30 milligrams per encounterd insproprlyedesiged pondssstemsnar liter for suspended solids and < 20 milligrams per 5encountered m properly designed pond systems are ltr fr biceia oxge deans or BOD >2 5 days, and this feature, in conjunction with such lIn the for 0s biochemical a o genomnd owar BO) . environmental factors as sunlight, high oxygen content enironmthen1tsand pro s, aowingd awihar s no and the presence of algal toxins, is responsible for the environmental problems, coupled with a now . ability of pond systems to reduce greatly the survival greatly increased population, led to tertiary of excreted pathogens. Indeed, protozoal cysts and treatment processes being Introduced to protect.. treatment p rocesses being introduced tolprotect helminth eggs and larvae can be completely eliminated receiving waters from further oxygen depletion, from pond effluents. Pond systems have several more toxic substances, and eutrophication. Atothe substames,and timeuitrocametclearothat advantages over other treatment methods: they are the sophisate trment technoloes w ere cheapest form of treatment, both to construct and sophistmcated treatment technologoes were not operate, with minimal requirements for foreign efficient at removing pathogenic microorganisms. ' . . effcient aountriem pahogeenvio, .exchange; their maintenance is very simple, requiring Thus, in countries where environmentalconcern only unskilled labor; they are easily designed to was acute (for example, the USA), or whlere wafluents acuerecommonlyre d (for example,t achieve any required degree of treatment; and the algae effluents were commonly reused (for example. Israel), effluent chlorination was borrowed from produced in the ponds are a potentially valuable source the water treatment industry as a way of killing of protein. - bacteria (and possibly viruses) in effluents. This technology, however, brought with it new and Literature Cited different environmental concerns.' American Public Health Association, American Water This highly simplified account illustrates the historical Works Association, and Water Pollution Control and conservative nature of the development of current Federation (1980). Standard Methods/lor the Examination waste treatment practices in industrialized countries. of Water and Wastewater. 15th ed. Washington, D.C.: These practices are not especially clever, nor logical, nor American Public Health Association. ..ltlefci-nitsntnesrlwhat Bisson. J. W. and Cabelli, V. J. (1979). Membrane filter completely doeffecti-an ifthe isam notuneessharil th enumeration method for Clost7idiuni perfringens. Applied would be done today If these same countries had the and Enuironmental Microbiology. 37, 55-66. chance to start again. (1980). Clostridiun perfijingens as a water pollution Fluid retention times in conventional sewage works, indicator. Journal of the Water Pollution Control oxidation ditches, and aerated lagoons treating Federation, 52, 241-248. domestic sewage are commonly less than 1, 3, and 6 Brodsky, M. H. and Ciebin. B. W. (1978). Improved medium days, respectively. Septic tanks typically have re- for recovery and enumeration of Pseudomnonas aeruginosa tentions of 1-3 days. These short retention times, in conjunction with temperatures that rarely exceed t 1. Waste stabilization ponds are examined in more detail in the section of that title in chapter 6. 10. See chapter 6, the section "Effluent Chlorination." 12. See the section "Reuse in Aquaculture" in chapter 7. DETECTION, SURVIVAL, AND REMOVAL OF PATHOGENS 65 from water using membrane filters. Applied and Environ- (1970). Applying bacteriological parameters to mental Microbiology. 36, 36-42. recreational water quality. Journal of the American Water Buck, A. C. and Cooke, E. M. (1969). The fate of ingested Works Association, 62, 113-120. Pseudomonas aeruginosa in normal persons. Journal of Gerba, C. P., Wallis, C. and Melnick, J. L. (1975). Fate of Medical Microbiology, 2, 521-525. wastewater bacteria and viruses in soil. Journlal of the Cabelli, V. J. (1977). Clostridiwn perjfringens as a water Irrigation and Drainage Division, American Society of Civil quality indicator. In Bacterial IndicatorsjHealth Hazards Engineers, 101, 157-174. Associated with Water, eds. Hoadley, A. W. and Dutka, B. Green, S. K., Schroth, M. N., Cho, J. J., Kominos, S. D. and J., pp. 65-79. Philadelphia: American Society for Testing Vitanza-Jack, V. B. (1975). Agricultural plants and soil as a and Materials. reservoir for Pseudomonas aeruginosa. Applied Micro- - (1978). Obligate anaerobic bacterial indicators. In biology, 28, 987-991. inadicators of Viruses in Water and Food, ed. Berg, G. pp. Hoadley, A. W. (1977). Potential health hazards associated 171-200. Ann Arbor. Mich.: Ann Arbor Science with Pseudomonas aeruginosa in water. In Bacterial Publishers. Indicators/Health Hazards Associated with Water, eds. Cabelli, V. J., Kennedy, H. and Levin, M. A. (1976). Hoadley, A. W. and Dutka, B. J. pp. 80-114. Philadelphia: Pseudomonas aeruginosa--fecal coliform relationships in American Society for Testing and Materials. estuarine and fresh recreational waters. Journal of the Jacobson, J. A., Hoadley, A. W. and Farmer, J. J. (1976). Water Pollution Conztrol Federation, 48, 367-376. Pseudomonas aeruginosa serogroup 11 and pool- Chakrabarty, A. K., Narayan, K. G. and Chandiramani, N. associated skin-rash. American Journal of Public Health, K. (1977). Association of Clostridium pezfringens type A 66, 1092-1093. with human diarrhoeal cases. Indian Journzal of Medical Levin, M. A. (1977). Bifidobacteria as water quality Research, 65, 495-499. indicators. In Bacterial Indicators/Health Hazards Cross, A. S. (1979). Pseudomonas aeruginosa. In Principles Associated with Water, eds. Hoadley, A. W. and Dutka, B. and Practice of Infectious Diseases, eds. Mandell, G. L., J. pp. 131-138. Philadelphia: American Society for Testing Douglas, R. G. and Bennett, J. E. pp. 1705-1720. New and Materials. York: John Wiley. Levin, M. A. and Cabelli, V. J. (1972). Membrane filter Department of Health and Social Security (1969). The technique for enumeration of Pseudomonas aeruginosa. Bacteriological Examination of Water Supplies. Reports on Applied Microbiology, 24, 864-870. Public Health and Medical Subjects, no. 71. 4th ed. McCausland, W. J. and Cox, P. J. (1975). Pseudomonus London: Her Majesty's Stationery Office. infection traced to motel whirlpool. JournEal of Drasar, B. S. and Hill, M. J. (1974). Human Intestinal Flora. Enviironmental Health, 37, 455-459. London: Academic Press. McFeters, G. A., Bissonnette, G. K., Jezeski. J. J.. Thomson, Dufour, A. P. (1977). Escherichia coli: the fecal coliform. In C. A. and Stuart, D. G. (1974). Comparative survival of Bacterial Indicators/Health Hazards Associated witli indicator bacteria and enteric pathogens in well water. Water. eds. Hoadley, A. W. and Dutka, B. J. pp. 48-58. Applied Microbiology, 27, 823-829. Philadelphia: American Society for Testing and Materials. McGarry, M. G. and Stainforth, J. (1978). Compost, Fertilizer Dutka, B. J. and Kwan, K. K. (1977). Confirmation of the and Biogas ProductionJifomHutnat and Farm Wastes in the single-step membrane filtration procedure for estimating People's Republic of China. Ottawa: International Pseudomonas aeruginosa densities in water. Applied and Development Research Centre. Environmental Microbiology, 33, 240-245. Mara, D. D. (1974). Bacteriology for Sanitary Engineers. Evison, L. M. and Morgan, S. (1978). Further studies on Edinburgh: Churchill Livingstone. bifidobacteria as indicators of faecal pollution in water. Parker, M. T. (1971). Causes and prevention of sepsis due to Progress in Water Technology, 10, 341-350. Gram-negative bacteria: ecology of the infecting or- Feachem, R. G. A. (1975). An improved role for faecal ganisms. Proceedings of'the Royal Society ofMedicine, 64, coliform to faecal streptococci ratios in the differentiation 979-980. between human and non-human pollution sources. Water Qureshi, A. A. and Dutka, B. J. (1979). Microbiological Researchi, 9, 689-690. studies on the quality of urban stormwater runoff in Feachem, R. G. A., Bradley, D. J., Garelick, H. and Mara, D. Southern Ontario, Canada. Water Research, 13, 977-985. D. (1980). Health Aspects of Exereta and Sullage Raghavachari, T. N. S. and lyer, P. V. S. (1939). The coli- Management: A State-of-the-Art Review. Appropriate aerogenes index of pollution used in the bacteriological Technology for Water Supply and Sanitation, vol. 3. analysis of water. Indian Journal of Medical Research, 26, Washington, D.C.: The World Bank, Transportation, 867 875. Water and Telecommunications Department. Seyfried, P. L. and Fraser, D. J. (1978). Pseudomonas Geldreich, E. E. (1966). Sanitary , , K of Fecal aeruginosa in swimming pools related to the incidence of Coliforms in the Environment. Water Pollution Control otitis externa infection. Journal of Health Laboratory Research Series no. WP-20-3, US Department of the Science, 15, 50-57. Interior. Washington, D.C.: Government Printing Office. Washburn, J., Jacobson, J. A., Marston, E. and Thorsen, B. 66 HEALTH HAZARDS OF EXCRETA (1976). Pseudomonas aeruginosa rash associated with a Wheater, D. W. F., Mara, D. D. and Oragui, J. (1979). whirlpool. Journal of the A4merican Medical Associa ion, Indicator systems to distinguish sewage from stormwater 235, 2205-2207. run-off and human from animal faecal material. In Wheater, D. W. F., Mara, D. D., Jawad, L. and Oragui. J. Biological Indicators of Water Quality, eds. James, A. and (1980). Pseudomonias aeruginosa and Escherichia coli in Evison, L. pp. 21/1-21//27. Chichester: John Wiley. sewage and fresh water. Water Research. 14, 713-721. Note added in proof Recent work in Yorkshire, England (Oragui 1982) has led to the development of bacteriological methods for distinguishing between human and animal fecal pollution of waters. Streptococcu.s bouis, which can be enumerated in water samples by the method of Oragui and Mara (1981), appears to be excreted exclusively by animals, whereas sorbitol-fermenting strains of Bifidobacteritmn adolesce72tis and B. breve are only excreted by man. Enumeration media for both sorbitol-fermenting and total bifidobacteria are described by Oragui (1982). These methods for distinguishing between human and animal pollution are currently being evaluated in Mexico, Nigeria and Zimbabwe. References Oragui, J. I. (1982). Bacteriological Methods Jbr tlze Distinction between Hunian and Animal Faecal P(dla,noa. Ph.D. Thesis. Leeds: University of Leeds. Oragui, J. 1. and Mara, D. D. (1981). A selective medium for the enumeration of Streptococcus bouis by membrane filtration. Journal of Applied Bacteriology, 51, 85-93. 5 Health Aspects of Excreta and Night Soil Systems IN THIS AND THE NEXT CHAPTER, the health impli- bowls may block up. Fouled and unhygienic pit cations of the principal varieties of excreta collection latrines are found all over the wbrld, often because they and treatment systems are discussed. These are have been constructed in communities previously separated into night soil (or "dry") and sewage (or accustomed to defecation on the open ground who "wet") systems. (The health implications of reuse and have also had inadequate community involvement or effluent-discharge practices are considered in chapter health education. Fouled pit latrines become a focus of 7.) Little attention is paid here to the technical details disease transmission and may make health matters of the systems examined, except to those bearing on worse than before the sanitation intervention. specific health problems. The reader wishing more information on technical aspects should consult the Odor second volume of this series (Kalbermatten and others 1982), the related document published by the Pit latrines with squatting slabs often are malo- International Development Research Centre dorous. If they are, they may not be used and thus (Rybczynski, Polprasert, and McGarry 1978), and cannot yield any potential benefits in improved standard sanitary engineering texts. In this chapter, health. Odors can virtually be eliminated by fitting a three excreta collection systems-the pit latrine and its vent pipe to the pit. This pipe should be at least 100 various modifications, the composting latrine, and millimeters in diameter, painted black, and fitted on the cartage systems-are described, and the discussion sunny side of the latrine so that it can heat up, the heat concludes with an examination of the health creating an updraught. [See note on page 82.] implications of dry treatment of night soil by trenching and composting. Excreta collection and treatment by Insect breeding wet systems are examined in chapter 6. Pit latrines with squatting slabs will usually become breeding sites for flies. Flies that visit a pit latrine to Pit Latrines breed or feed may carry pathogens when they leave and thus promote disease transmission. If the pits are wet, Pit latrines are the simplest of all on-site disposal they may also become Culex pipiens breeding sites. Well systems. Excreta fall into a hole in the ground, and a constructed pits with pour-flush bowls will not allow new pit is dug when the hole is about two-thirds full such insect breeding. If squatting slabs are used, a (see figure 5-1). A ventilated improved pit (vip) latrine, vertical vent pipe 100-200 millimeters in diameter, and a modified pit latrine called a ROEC (Reed covered by a fly screen, and combined with a dark Odorless Earth Closet), are shown in figures 5-2 and 5 interior to the superstructure-will greatly reduce 3, respectively. Pits are covered by sqatting slabs, seats, both the amount of fly breeding and the escape of any or pour-flush bowls. flies that do breed. Flies breeding in the pit will be attracted by the light coming down the vent pipe and Cleanliness will attempt to escape by this route, only to be prevented by the fly screen. The effect of vent pipes on In all latrines cleanliness is of the utmost importance. mosquito breeding in wet pits remains uncertain and Squatting slabs easily become fouled and pour-flush the latest findings are reviewed in chapter 36. 67 68 HEALTH HAZARDS OF EXCRETA survival is of no concern because all pathogenic organisms will be dead. In some areas, however, two Open for alternating pit sites are used, a pit is dug out a year or ventilation two after closing, and the contents are used as fertilizer. This system resembles the double-vault composting toilet (see below) except that it operates on a longer cycle. If the pit has been left for a minimum of one year. there will be no viable pathogens (except, possibly, a few Ascaris eggs). The chances of viable Ascaris eggs being present are greater if the pit is wet and partly below the water table. The risk involved in reusing material that has been buried for at least 12 months is -Removable small, however, and the pit contents may immediately be used on the fields with confidence. [See note on page Vent hole W Base 82.7 Ground level _ Ground lee .,. ., , ................ ... _ ,,Groiunddwater pollution /W/ t+-B. wConcreiu (Jr \;u tilc. sheet metal, (noncorrosie) or corrugated metal roof 100- t 2 diame vent pipe Joint detail i Removablc cover 11)11_ _ /'-mm,4. concrete. I sections JOG-mm bl< ock. .^ or-, i 0 n Sover sectons a-a St _-_ subStit d fr stor manhole C ston , a a locascaled with F a _ E v m~~rlortar or tar.,_ ___L ;[ < _ 2.000to _ F '~~~~~~~~~~~~~~~~~.00) \mm 31100 mm a I q F I()()~~~~~~~10-mm concrete.,l -111" ~~~~~lvq 7, s 2(00-mm block, or ax t!6 200-mm brick liner Section a-a Section b-b (vent pipe not shown) Figure 5-3. Reed0Odorltess Earth Closet (ROEC) (dimensions in millimeters). Pedestal seat with curved chute may be substituted forsquattingplate. Constructionmaterials and dimensions forthesuperstructuremayvary according to local practice. From Kalbermatten and others (1982) HEALTH ASPECTS OF EXCRETA AND NIGHT SOIL SYSTEMS 71 Fly-proof mesh 150-mm-diameter vent pip Long-handled cover to _ _Ii squatting plate Squattingl Removable < L t t I E ~~~~~cover r= _.* .......-- ..._ n- or A-shaped channels- A i r; M. Air Ground level Air _ z^^> i ~~~~~~~~~Air_ o L L H~~~~~~~~~vuaulitS Decomposing ) ) ( * .C c<.) Gravel soakaway waste 's Figure 5-4. 'tlulo ii" continuous-composting toilet. From Kalbermatten and others (1982); adapted from a drawing by U. Winblad Only limited and inadequate microbiological data main factors affecting the survival of excreted exist on continuous composters (Gurak 1978; re- pathogens are time and temperature. Temperature in viewed by Feachem, Mara and Iwugo 1980). The batch the composting pit or vault depends on the air supply, composter is common in China and Vietnam, and the the C:N ratio, and the moisture content. If the most usual design is the double vault (see figure 5-5). digestion is anaerobic, the temperature may remain Again, no appreciable microbiological data on these ambient or it may rise at most to around 35°C. If it is toilets have been located, although such data may exist aerobic, the temperature will rise to the 50-70°C range in China and Vietnam. if the C:N ratio and moisture content are correctly regulated. These conditions may be difficult to achieve, especially in arid developing countries where little Pathogen survival in product organic material (needed as a source of carbon) is In both kinds of composting toilet, the composted available for adding to the wastes. product is used as an agricultural fertilizer and soil It is certain that double-vault composters will be conditioner. It is important, therefore, that pathogen anaerobic, and it is probable that multrums will be destruction should be as complete as possible. The two also. Anaerobicity and ambient temperature certainly 72 HEALTH HAZARDS OF EXCRETA ,_ 75-mm r. unplasticized vent pipe Air space Removable 690 1,000 640 superstructure formed from timber frame .__. _ ., and galvanized …jr- - - - -1- - -- milled steel Icr r---1 r--~~ ---1 1 ~ Concrete Concrete -1 = -Fiberglass I ,,,,~~~ Concreteet t | l l 1l ~~~~~closure cover acs oe I oe ~~"'~~'~~' access cover n S ntosecond 50, .i lvault F.- L- - ON I__jfiio ___ ~ ~~~~~~Concret L °S° 450 | Plan Section Model used in Botswana 50 _ _ _ _ _ 25 3 3-mm ferrocement 50 1,050 450 Plan Section Model used in Tanzania Figure 5-5. Double-ivault comlposting (DVC) toilet (dimensions in millimeters). From Kalbermatten and others (1982); top, adapted from a drawing by R. A. Boydell 1,420 73 Ash 340 100 ~540 10034 storage Urn area 0; outlet Superstructure corner posts Plain Bamboo wall cladding 130 ~ ~ ~ Urine removal port b , 1,,xv,, ... . 4 . ,,,^sv,+ ] , ................. b 250 150 1140 720 1401 100 100 1.200 Section a-a 1,620 100 500 500 100 - I141 < 11401- -1 500 O Section b-b Figure 5-5 (continiued) Model used in Vietnam 74 HEALTH HAZARDS OF EXCRETA EXCRETA Viruses --- -- Bacteria - - Composting toilet wifh 3-month minimum retention time. Protozoa - COMPOST Helminths 0 Helminths Figure 5-6. Pathogen flow through a batch composting toilet (double-vault) are the correct, conservative assumptions to make above a bucket which is filled within a few days by the where pathogen removal is the concern. Pathogen excreta of an average family (see figure 5-7). The bucket removal then depends on the retention time in the unit. is positioned adjacent to an outside wall and is There appears to be a wide variation in retention time accessible from the street or back lane. A night soil used in both the multrum (continuous) and double- collector ("scavenger" or "sweeper") will call vault (batch) systems, and the pathogen removal regularly-preferably every day, but more typically efficiency of any given design can be estimated by once or twice a week-to empty the bucket. consulting table 5-1. It is clear from the table that a minimum retention time of 3 months will yield a product free of all pathogens except the more persistent Table 5-1. Probable pathogen content in final helminth eggs, as visualized in figure 5-6. Three product of anaerobic composting toilets operating at possible pathogen control strategies can be adopted for ambient temperatures in warm climates compost: Retention time Pathogen (months) * To use the compost as produced and accept the level of risk involved. This risk could be reduced to 1 2 3 4 6 8 10 sufficiently low levels by using the compost only to prepare ground prior to planting or by not Viruses applying compost within 2 months of harvesting. Enterovirusesa + + 0 0 00 0 * To apply the compost only to industrial or fodder Bacteria crops. Fecal coliforms + + 0 0 0 0 0 * To provide further treatment for the compost Leptospira spp. 0 - 0 0 0 0 0 through heating it (probably impracticable) or Shigella spp. + 0 0 0 0 0 through mixing it with an ovicide (also often Vibrio cholerae + 0 0 0 0 0 0 impracticable). Protozoa Balantidium coli + 0 0 0 00 0 The first of these strategies is probably the most Entamoeta realistic, and the quality of the product will become Giardia lamblia - 0 0 0 0 0 0 better as the retention time is increased beyond 3 months. ~~~~~~~~~~~~~Helminth eggs months. Ascaris lumbricoides + + + + + + + + + + + Hookwormsb + + 0 0 0 0 0 Cartage Systems Schistosoma spp. 0 0 0 0 0 0 0 Taenia spp. + + + + + + + + + + + Cartage systems include a variety of technologies by Trichuris trichiura ++ ++ + + + - 0 which night soil is periodically removed from containers in or near the house. One of the oldest- concontration, and, generally, least hygienic-systems is the bucket a. Includes polio-, echo-, and coxsackieviruses. latrine. A squatting slab or seat is placed immediately b. Ancylostoma duodenale and Necator americanus. HEALTH ASPECTS OF EXCRETA AND NIGHT SOIL SYSTEMS 75 Squatting plate Fly-proof door Paved surface and drain / Ground surface _ . ~~25 mm, _ -vzt '.v: :.00 maximuma.- _ f-,,- ;eM Soakage pit for bucket washwater L - Bucket latrine Night-soil collection by dipper and bucket (here a vault rather than a bucket is located in house) Night-soil bucket and scraper Cartage wheelbarrow for three or six buckets Figure 5-7. Bucket latrine and cartage. Fly-proof doors and paved surfaces and drains are commonly missing in most existing bucket latrines. From Kalbermatten and others (1982); top left, adapted from Wagner and Lanoix (1958); top right, from a photograph courtesy of Michael G. McGarry; bottom, Department of Social Welfare, Ahmedabad, India Many households in East Asia, and elsewhere, store in which the night soil is deposited, collected, their excreta (plus the small amounts of water used for transported, treated, and reused. Each of these will be pour flushing and anal cleansing) in sealed vaults considered in turn. under or beside the house (see figure 5-8) that are emptied by a vacuum truck about once every 2 weeks. Night soil deposition This system has relatively high operating costs but may have relatively low initial costs. It is suitable for high- The two normal methods of deposit are into the density urban areas where access by truck is possible bucket or vault. Both these depositories can be and truck maintenance facilities exist. The health satisfactory if they are hygienically maintained. The dimensions of a cartage system depend on the manner bucket, a smaller vessel than the vault, is more likely to 76 HEALTH HAZARDS OF EXCRETA Val5-mm vent pipe s to tVacuum tanker Toilet-_ ~Manhole t a House / OffseVault v Vault below squatting plate Vent Hose to tanker House 1 Offset vault Figure 5-8. Alternative designsjor rault toilets. From Kalbermatten and others (1982) overflow and to contaminate its surroundings. The to develop from egg to adult, and so a bucket emptied bucket latrine is also almost certain to be malodorous, every 5 days will not permit fly breeding, provided it is and this will discourage use. In contrast, the vault can well cleaned each time it is emptied. Vaults, however, be ventilated, making a hygienic and pleasant latrine. are emptied less frequently, and fly breeding is a The possibility of fly breeding depends on the danger. Breeding can be reduced by installing a pour- frequency with which the depositories are emptied. flush water seal to prevent access of adult flies or by Houseflies and blowflies require a minimum of 1 week installing a vent pipe with a fly screen similar to the one HEALTH ASPECTS OF EXCRETA AND NIGHT SOIL SYSTEMS 77 recommended above for pit latrines. A pour-flush table 2-2). This risk is not simply to the sweepers water seal is probably the only reliable method of themselves, but also to anyone who lives on or walks, preventing fly breeding in vault latrines. plays, or works in the streets or back lanes where the night soil has been spilled. The risk to children is Night soil collection obviously great because they commonly play in back lanes and alleys. The latent pathogens that develop on Collection of night soil from vaults by vacuum soil (category ti-hookworms, Ascaris, and Trichuris) trucks can be hygienic and risk free-provided that the may well develop into their infective stages where they outlet pipe from the vault is in good repair and that all have been spilled in fresh night soil, and there is fittings on the truck and suction hose are well evidence that the cartage of night soil is partly maintained. A little spillage is probably inevitable, but responsible for the high levels of Ascaris egg it can be reduced to an acceptable minimum by good contamination found in the soil of some cities. Vacuum equipment and well-trained operating personnel. trucks, by contrast, can transport night soil through the By contrast, collection from bucket latrines is always streets with minimal risk of spillage. messy. The worst method is to empty the buckets and immediately return them, which causes the latrine area to become progressively more fouled (with consequent risk of infection to the household, the sweeper, and Night soil treatment is also discussed in conjunction passersby). Emptying the bucket, rinsing it out, and with wet systems in the next chapter. Night soil can be returning it is also undesirable and will probably result digested and dewatered (as is sludge), it can be mixed in the washwaters being deposited in the street. The with sewage and treated in conventional plants, or it best arrangement is to replace the bucket by another can be sluiced into waste stabilization ponds (see cleaned and disinfected one, with dirty buckets being chapter 6 for descriptions of these treatments). Night returned to a central depot for cleaning and soil can also be treated by dry systems, such as disinfection. Operation of this system is facilitated by trenching or, preferably, composting. Following use of a color code in which all buckets collected on adequate treatment, night soil can be used in Monday, for example, are red and the replacement agriculture, aquaculture or gas production (see chapter buckets green. Such a bucket-replacement system is 7). often not feasible on a large scale because of the Where trenching is used, the health implications can difficulty of transporting large numbers of buckets. It be serious. A badly managed and inadequately can, however, work well in army camps, prisons, controlled trenching ground will be a major health disaster relief camps, and other institutions of limited hazard to all who work on it or to those-children, for size. example-who may gain access. The families and It is clear that the risks from a cartage system depend close contacts of these people are also at risk. The greatly on the quality and regularity of the service proper management of a trenching ground is largely provided. The system is sensitive to a few days' common sense: trenches should be at least 0.6 meters interruption in collections, whether from mechanical deep and should be filled with night soil to a depth of breakdown or absence of the sweeper.4 not more than 0.3 meters; they should then be rapidly covered with tamped earth, to make a small mound of earth over the trench, after which they are left for at least 2 years. Yet, however well managed the surface of The differences in health risks between the a trenching ground is, the risk of groundwater alternative bucket and vault-and-truck systems be- pollution may always be present. This risk is minimized come obvious at the transport stage. The worst system by careful location of the trenching ground following a is the one in which buckets are emptied by hand into hydrogeological survey. Given these limitations, in open carts or into larger buckets, which are then many situations the most appropriate and attractive carried by hand or on yokes. Under these arrange- method of night soil treatment is by mixing it with ments there will always be spillage. People who come refuse and composting (see below). into contact with this fresh night soil risk infection from any of the nonlatent pathogens (categories I and it in Night soil reuse 4. See chapter 8. the sections "Influence of Social Structure and Organization" and "Social and Organizational Aspects of Excreta Reuse is described in detail in chapter 7. The reuse of Cartage Systems." untreated night soil in agriculture is a widespread 78 HEALTH HAZARDS OF EXCRETA practice, but one that is to be strongly condemned for thermophilic microorganisms, and degradation is its health hazards. There is much evidence that the use more rapid and usually free of odor. of untreated night soil on crops contributes to the A newly erected compost pile will contain entrapped transmission of infection to those working in the fields oxygen and, if the other factors mentioned above are and. to a lesser (but still significant) degree, to those correctly regulated, thermophilic aerobic processes handling or consuming the crops. Treatment or will be established and the temperature at the center of storage of night soil should therefore always be the pile will rapidly rise to 55°C or above. As the provided prior to its reuse. available oxygen is used up, however, the process will become progressively more anaerobic and tempera- tures will fall. There are three methods commonly used Composting to sustain the supply of oxygen and therefore maintain thermophilic temperatures: the pile is regularly turned, Again it must be stressed that temperature and time or ventilation tubes are arranged in the pile, or forced are the two most important factors in the achievement aeration is provided by blowers or suckers. In the last of low pathogen survival in waste treatment processes. two cases, the pile is usually lagged to prevent heat loss. In the treatment of night soil or sludge for reuse, an Temperatures can rise to 80°C in these well-managed, almost pathogen-free product is required. This is only thermophilic, aerated composting systems, and it is achieved by processcs incorporating long retention possible to ensure that all parts of the pile spend several times (such as ponds or protracted digestion and hours at temperatures above 60°C-of the utmost drying; see the next chapter), heat (such as thermo- importance in curtailing pathogen survival. philic digestion; see the next chapter), or thermophilic composting (discussed here). The attraction of thermophilic composting is that it can yield a safe Pathogen survival product for reuse in a relatively short time (<2 Pathogen survival in compost systems depends months) and that it does not require an external source upon the time-temperature characteristics of various of energy for heat. In addition, composting tech- parts of the pile. The death curves derived for some nologies are available that are relatively low cost and pathogens, discussed further in Part Two, are plotted labor intensive. The compost produced is a useful soil in figure 5-9. Time-temperature points above the curve conditioner and source of plant nutrients that may for each pathogen represent certain, total destruction. increasingly be in demand among poor farmers as the It is clear that enteroviruses and Ascaris eggs are the cost of industrially produced fertilizers rises (Food and most hardy, but the time-temperature combinations Agriculture Organization 1975). given in the note to figure 5-9 will ensure their Composting has been thoroughly reviewed by destruction. If all parts of a compost pile can be Gotaas (1956), and more recent accounts are provided brought to a time-temperature state within the "safety by Haug (1979); Polprasert, Wangsuphachart, and zone" in figure 5-9, complete pathogen destruction Muttamara (1980); and Shuval, Gunnerson, and Julius should be guaranteed (see figure 5-10). There are two (1981). A wide range of fecal composting technologies possible exceptions. First, spore-forming bacteria- are available. They all incorporate the mixing of night such as Clostridium perfringens, discussed in chapter soil or sludge with a carbon source (such as refuse or 4-are more resistant but present little risk. Second, sawdust) to achieve a C:N ratio of approximately hepatitis A virus appears to resist rapid heating, and its 20-30. Moisture content (20-60 percent) must also be ability to survive temperatures around 60'C for several regulated for optimal performance, with wetting or hours is unknown. turning (for drying) at appropriate intervals. Much of the literature on pathogen survival in The most important feature of composting, from the compost, which has previously been reviewed by others health viewpoint, is the temperature achieved-and (for intance, Kawata, Cramer, and Burge 1977; Krige this depends on the oxygen content of the pile, C:N 1964; Nell and Wiechers 1978; Reeves 1959; Shuval, ratio, moisture content, particle size, and pH. If the Gunnerson and Julius 1981; Wiley 1962; Wiley and process is anaerobic, temperatures will remain at (or Westerberg 1969; WHO Intemational Reference only a little above) ambient temperature, and Centre for Wastes Disposal 1978) is reported in Part mesophilic microorganisms will predominate. Foul- Two. This literature indicates that a well-designed smelling gases are usually produced, and the process of system under good management produces a pathogen- degradation proceeds slowly. If the process is aerobic, free, or almost pathogen-free, compost if all sections of substantial heat is generated by the proliferation of the pile reach the required temperature for the required HEALTH ASPECTS OF EXCRETA AND NIGHT SOIL SYSTEMS 79 70 70 Enteric viruses 65 65 Shigella \/ 60 - SAFETY ZONE 60 so- 'N 50 Vibrio cholerae \ , , G. 45 45 45' N. 40 -N - Ascaris -40 'N N\> & Salmonella 35 _ X - _ 35 30 _ ;_30 25 _ ,Emn-aoba \ 25 ',histolytica 20 I 1 20 0.1 1 1 0 I 100 1, 00 1 '°° I'°°° I day I week I month I year Time (hours) Figure 5-9. Influence of time and temperature on selected pathogens in night soil and sludge. The lines represent conservative upper boundaries for pathogen death-that is, estimates of the time-temperature combinations required for pathogen inactivation. A treatment process with time-temperature effects falling within the "safety zone" should be lethal to all excreted pathogens (with the possible exception of hepatitis A virus at short retention times). Indicated time temperature requirements are at least: I hour at > 62°C, I day at > 50'C, and I week at >, 46°C. For more detail on the time-temperature combinations lethal to these and other pathogens, see the graphs in chapters 9, 15-17, 20, 22, 23, 32, and 34 of Part Two (from which this composite was made) 80 HEALTH HAZARDS OF EXCRETA EXCRETA Viruses --- - Bacteria -- 3m Wel/-managed (olparts of the pilet required time-temperature) thermophiiic compostinIg. Protozwoa COMPOST Helminths > Figure 5-10. Pathogen flow throuigh a well-managed thermophilic compostinlg process time. The organism most likely to survive this useful to the staffin charge. Fly breeding will, of course, treatment is Ascaris, and Ascaris eggs may therefore be fluctuate markedly with the seasons, irrespective of the used as the indicator of successful composting. condition of the compost pile. Fly breeding Literature Cited One of the major problems in managing composting operations is fly control. All raw materials used for Feachem, R. G. A., Mara, D. D. and Iwugo, K. 0. (1980). composttflies and are good media for fly Alternative Sanitation Technologies for Urban Areas in brmpee ting. Flies cattract eggs in the material attheplace Africa. Appropriate Technology for Water Supply and breeding. Flies can lay eggs in the material at the place Sanitation, vol. 7. Washington, D.C.: The World Bank, of collection or during the handling of the material at Transportation, Water and Telecommunications the compost site. Different species predominate under Department. different conditions, but good control measures should Food and Agriculture Organization (1975). Organic affect them all. Fly larvae cannot survive temperatures materials as fertilizers. Soils Bulletin, 27. above 50'C, and so, as for other pathogens, the Gotaas H. B. (1956). Composting. Sanitary disposal and achievement of high temperatures in all parts of the pile reclaniation of organic wastes. Monograph Series no. 31. is the essential requirement for control. Fly larvae may Geneva: World Health Organization. however, migrate along temperature gradients to seek Gurak, R. S. (1978). Final Report on the Alternative Waste the cooler parts of the pile (such as the edges or the Disposal Methods Project in Tanzania, East Africa: Chemical, Microbiological and Parasitological Results. areas near ventilation shalts). These larvae may be Ottawa: International Development Research Centre. destroyed by effective and well-controlled turning orby Haug, R. T. (1979). Engineering principles of sludge lagging unturned piles. The use of insecticides in composting. Journal of the Water Pollution Conjtrol compost piles is not desirable unless it has been Federation, 51, 2189-2206. demonstrated that these chemicals will not affect the Kalbermatten, J. M., Julius, D. S., Gunnerson, C. G. and composting process or the acceptability of the product Mara. D. D. (1982). Appropriate Sanitation Alternatives: to farmers. Plannling and Design Manual. World Bank Studies in Fly breeding may pose a general problem in all Water Supply and Sanitation 2. Baltimore. Md.: Johns composting systems. The level of fly breeding provides Hopkins University Press. some gauge ofhow successfully the pile is managed and Kawata, K.. Cramer, W. N. and Burge. W. D. (1977). whether it is being thoroughly heated, with minimum Composting destroys pathogens in sewage solids. Water fly breeding an explicit goal for the management of all and Sewage Works, 124, 76-79. compstig plnts It s pssibe t montorthe eve of Krige. P. R. (1964). A survey of the pathogenic organisms and composthng plants. It IS possible to monitor the level of helminthic ova in composts and sewage sludge. Jour nal fly breeding by positioning flytraps at appropriate sites and Proceedings of the Institute of Sewage Purification, part around the plant and recording the daily gatch. This 3, 215-220. provides a continuous and immediate check of Nell, J. H. and Wiechers, S. G. (1978). High temperature management and temperature control that is most composting. Water South Africa, 4, 203-212. HEALTH ASPECTS OF EXCRETA AND NIGHT SOIL SYSTEMS 81 Polprasert, C., Wangsuphachart, S. and Muttamara, S. Wagner, E. G. and Lanoix, J. N. (1958). Exereta Disposalfor (1980). Composting night soil and water hyacinth in the Rural Areas and Small Communities. Geneva: World tropics. Compost Science/Land Utilization, 21, 25-27. Health Organization. Reeves, J. B. (1959). Sanitary aspects of composted sewage, Wiley, B. B. and Westerberg, S. C. (1969). Survival of human sludge and sawdust. Sewage and Industrial Wastes, 31, pathogens in composted sewage. Applied Microbiology, 18, 557-564. 994-1001. Rybczynski, W., Polprasert, C. and McGarry, M. G. (1978). Wiley, J. S. (1962). Pathogen survival in composting Lowv-Cost Technology Options fbr Sanitation: A State-of- municipal wastes. Journal of the Water Pollution Control the-Art Review and Annotated Bibliography. IDRC-102e. Federation, 34, 80-90. Ottawa: International Development Research Centre. WHO, International Reference Centre for Wastes Disposal Shuval, H. I., Gunnerson, C. G. and Julius, D. S. (1981). (1978). Compost: An Annotated Bibliography on Compost, Night-soil Composting. Appropriate Technology for Water Compost Quality and Composting, 1971-1977. Dubendorf, Supply and Sanitation, vol. 10. Washington, D.C.: World Switzerland: wHo International Reference Centre for Bank, Transportation, Water and Telecommunications Wastes Disposal. Department. Note added in proof Since this chapter was written, there have been a number of developments in the design of ventilated improved pit latrines, especially with regard to ventilation mechanisms (wind shear across the top of the vent pipe is now known to be more important than absorption of solar radiation) and the use oftwin pit V IP latrines (which are permanentstructures requiringeach pit to be emptied in alternate years). There have also been significant developments in superstructure design, notably the spiral shape used in Zimbabwe which obviates the need for a door, while still ensuring privacy and good fly control. In rural Zimbabwe spiral latrines have been built almost entirely out of local materials and at a financial cost to the householder of only US$tO. These and other developments are described in a series of working papers and technical notes prepared by the Technology Advisory Group established by the World Bank as executing agency for the United Nations Development Programme Interregional Project INT181,/047 "Development and Implementation of Low-cost Sanitation Investment Projects", they may be obtained by writing to The Project Manager, UNDP INT/81/047, Transportation and Water Department, World Bank. 1818 H St NW, Washington DC 20433. USA. 6 Health Aspects of Sewage Systems IN THIS CHAPTER the "wet" systems, which collect and Pathogen survival treat excreta diluted by water, are considered. Not only Two fundamental processes affecting pathogen conventional sewerage and sewage treatment systems removal in waste treatment operate in septic tanks and are included, but also on-site sewage .disposal methods aquaprivies. First, solids settle to the sludge layer at the such as septic tanks and aquaprivies. The reader bottom of the chamber; with them settle any bacteria wishing more technical information should refer to o Kalberatten and ohers 1982) Rybcynski or viruses adsorbed onto the solids and any helminth Polprasert and McGarry (1978); Mara (1976); Metcalf eggs or protozoal cysts sufficiently dense to settle. The and Eddy, Inc (1979) Okun and Ponghis (1975); and settling action of the tanks is their chief function and Tebbutt (1983).' their efficiency depends on retention time and design (particularly with regard to baffles or compartments designed to prevent hydraulic short-circuiting and to create quiescent conditions). Those pathogens which Aquaprivies and Septic Tanks do not settle will remain in the liquid layers and eventually pass out of the tanks in the effluent. The Aquaprivies and septic tanks are similar systems and degree to which their concentration decreases depends are thus examined together. They both incorporate a on retention time and on their reaction to the rich, sealed settling chamber in which solids accumulate and anaerobic liquor in which they are held. out of which an effluent flows. Generalizations about pathogen removal in aqua- privies and septic tanks are difficult to make because Technical description designs and retention times vary enormously. Moreover, as the sludge layer of a septic tank builds up, Septic tanks typically are located in the gardens of retention times decrease and the pathogen content of individual houses having water connections and full the effluent increases. It is common to find operating plumbing; they receive all wastewater from a house aquaprivies and septic tanks that are long overdue for and have liquid retention times in the order of 1-3 days, desludging; in these cases any good design features and after which the effluent normally goes to a soakaway. pathogen removal abilities initially present will largely Aquaprivies are located directly under the toilet; they have been negated by the failure to desludge at the usually receive only excreta and small volumes of correct, regular intervals. flushing water and have liquid retention times as high Because the quality of aquaprivy effluent depends as 60 days, after which effluents flow to soakaways or greatly on retention time, the system is sensitive to into small-bore sewerage systems. In some designs variations in hydraulic loading. If the loading rate is aquaprivies also receive sullage, in which case retention too low and the water level is allowed to fall below the times may decrease to a few days (depending on the drop pipe, the result will be the release of offensive odor volume of sullage produced). Designs for septic tanks and, probably, large-scale mosquito breeding. and aquaprivies are shown in figures 6-1 and 6-2. Attempts to guarantee an adequate water level by running sullage into the tanks, however, will shorten retention times and raise the pathogen content of the effluent. 1. See also Part Two for a detailed review of the pathogen removal There are few available data on the quality of effluent capabilities of the treatment systems examined in this chapter. from aquaprivy installations. The literature on septic 83 84 HEALTH HAZARDS OF EXCRETA Inlet Compartment Outlet baffle Outlet 'FT !r'' ; ''' ' Outlet Inlet - - @ E . _ = _ 9 i t _ t40 percent Scum I _ of liquid depth . Clear space _ L .-Sclear space _ Scum ____________Scum 3 length V 1 length Conventional two-compartment Conventional two-compartment septic tank septic tank with inlet with baffle walls connector and outlet "T" Effluent weir Sludge . - - * cha~~~~~~ ~ ~~~~nnel -. . 1 / / ra tffl 1 ~~~~~~~~~To L ... . * : . Fit ; . te TXdrainfield 7 ~ ~ ~ ~ /' Toilet wastes Sullage and settled wastes Two-compartment septic tank with upflow filter Three-compartment septic tank Animal excreta Sullage inlet Slurry 600-mmn diameter and animal exreta removal access manhole 1 [ X 1. a | g 42 : a Human Human - - exereta h excreta - h b __ Equal Equal Equal Section a-a Section b-b Three-compartment septic tank for resource recovery Figure 6-1. Septic tanik designs. From Kalbermatten and others (1982) HEALTH ASPECTS OF SEWAGE SYSTEMS 85 a r ra L 900 _ ~~~~~~~~~~~~~~~~~Outlet -- ___ a 0 t ) 1-- S ~to soakaway 25-mm I I I vent pipe I Removable slab I I I I for desludging access L--L - - - ___J Plan 25-mm vent pipe Removable slab for desludging access Outlet to soakawav 1,370 Section a-a Figure 6-2. Cont entionzul oqoopriryi (dimensions in millimeters). From Kalbermatten and others (1982): adapted from Wagner and Lanoix (1958) 86 HEALTH HAZARDS OF EXCRETA tanks, reviewed in detail in Part Two, will therefore be is probable that an aquaprivy incorporating baffles summarized here. In a septic tank having a normal and with a retention time this long will produce an retention time (1-3 days), the effluent produced will be effluent of substantially better quality than a normal rich in all pathogens contained in the influent. This septic tank (or, indeed, than a conventional sewage flow is illustrated in figure 6-3. Removal of various works). It must be assumed at present, however, that types of pathogens from the effluent is as follows: aquaprivy and septic tank effluents are highly patho- genic (figure 6-3). If they flow to sewers, they require Viruses Re0t,cion2 (log10 tout) treatment (probably in ponds) prior to any reuse. If Bacteria 0-2 they flow to soakaways, a groundwater pollution Protozoa 0-2 hazard may exist.2 Helminths 0-2 Badly maintained and inadequately desludged tanks Conventional Sewage Treatment will have especially poor pathogen removal character- istics. A proportion of all pathogens will settle, and fresh A variety of unit processes combine to form sludge will therefore contain significant numbers of conventional sewage treatment; commonly used pathogenic bacteria, viruses, protozoal cysts, and combinations are shown in figure 6-4. These com- peamithogeni eggs eri (i reu6- Wenero oal 'setc tank i ponent processes will be discussed in turn, followed by helminth eggs (figure 6-3). Whenever a septic tank IS adicsonfthefcsofaomletrtet desludged, it is inevitable that some portion of the a discussion of the effects of a complete treatment sludge will be fresh and, consequently, hazardous. Septic tank sludge should therefore be handled with great care and disposed of by burial, composting, or Pretreatment and primarY sedimentation digestion (either aerobic or anaerobic) in the same way Pretreatment by screening or comminution will have as any sewage sludge (and with the same effect on effetmentbyscreengcommmutionwage v pathgensseethe previous chapter and the following no effect on the pathogen content of sewage. pathogens-see the previous chapter and the following An almost universal first stage in conventional section). A well-designed aquaprivy, with a longer retention time (>20 days) than a septic tank, may sewagetreatmentisthesettligofsuspendedparticles produce an effluent with only low concentrations of enteric bacteria, protozoa, or helminth eggs, and many 2. See chapter 7, the section "Effluent Discharge. To ground- of the viruses may settle when adsorbed onto solids. It water." INFLUENT EFFLUENT Viruses ---------- - Viruses Bacteria A -Sptic - a-j- - Bacteria Sept ic tank with /-3 day retention time Protozoa _ .> Protozoa Helminths > Helminths Helminths Protozoa Bacteria Viruses SLUDGE Figure 6-3. Pathogen flow through a septic tank. HEALTH ASPECTS OF SEWAGE SYSTEMS 87 Pretreatment the theoretical settling velocities shown in table 6-1. + Actual settling velocities will be lower than these <0 Primary sedimentation figures because in actual sedimentation tanks many t factors hamper ideal settlement. The calculations Activated sludge or trickling filters indicate that only schistosomes, and maybe Trichuris, would have a reasonable degree of removal. Secondary sedimentation (humus tanks) Studies on laboratory and full-scale primary sedimentation tanks have been done, but laboratory models always give higher removal efficiencies than (Tertiary treatment ) actual plants because of more idealized and carefully t controlled conditions.3 Entamoeba histolytica cysts are Effluent discharge reduced by 50 percent or less. Between 35 percent and 98 percent of helminth eggs settle, with 50-70 percent Sludge digestion being the typical figure. Removal of various pathogens . from the effluent is as follows: Sludge drying Reduction (log1, unit) . Viruses 0-l Sludge disposal Bacteria 0-1 Protozoa 0-1 Figure 6-4. Components of conventional sewage Helminths 0-2 treatment in primary sedimentation tanks. A retention time in the Similar performance may be expected from secondary tankof26hoursis.A proportion of settlng tanks, except that these are often designed with tank of 2-6 hours IS normal. hihe overflowo rates. pathogens in the sewage will settle to the sludge layer hlgher overflow rates. either by direct sedimentation or by being adsorbed Flocculatlon of sewage (with ferrtc chlonde, lome, or onto solids that are in the process of settling. alum) will greatly improve the settlement of cysts and Many studies have found little or no virus removal eggs and perhaps of other pathogens as well. by primary sedimentation, and in actual treatment works a removal rate of 50 percent seems to be a Trickling filters maximum. Bacterial removal by primary sedimen- Trickling filters alone do not appear to be efficient tation may achieve 50-90 percent in 3-6 hours. in removing viruses from sewage. Reductions reported Shuval (1978) has collected data on the size and shape of eggs and cysts and has used these to compute 3. See Part Two, where the findings of such studies are reviewed. Table 6-1. Theoretical settling velocities of protozoal cysts and helminth eggs Characteristics of Cysts and Eggs Density Settling Size (grams per cubic Assumed velocity Pathogen (micrometers) centimeter) shape (meters per hour) Protozoa Entamoeba hartmanni 5 1.1 Spherical 0.007 Entamoeba histolytica 20 1.1 Spherical 0.11 Helminths Ascaris lumbricoides 55 x 40 1.11 Spherical 0.65 Hookwormsa 60 x 40 1.055 Spherical 0.39 Schistosoma spp. 150 x 50 1.18 Cylindricalb 12.55 Taenia saginata 30 1.1 Spherical 0.26 Trichuris trichiura 50 x 22 1.15 Cylindrical 1.53 Source: Adapted from Shuval (1978). a. Ancylostoma duodenale and Necator americanus. b. S. japonicum eggs are spherical. 88 HEALTH HAZARDS OF EXCRETA in the literature vary from 15 to 75 percent, with most protozoal cysts and helminth eggs, but substantial results indicating 30-40 percent removal.4 proportions of eggs will be removed in the secondary Reductions in indicator bacteria in trickling-filter settling tanks. Complete activated sludge treatment effluent vary between 25 and 99 percent. Typical plants have been reported to remove 80-100 percent of reductions appear to be 80-95 percent. Salmonella helminth eggs. reductions in the range of 71-99 percent are reported Considering the activated sludge process in isol- when removal by secondary sedimentation is included. ation, pathogen removal efficiencies may be sum- The lower the loading rate on the filter, the higher the marized as follows: bacterial removal. Many protozoal cysts and helminth eggs will pass Viruses Reductioni (log,( uirt) through trickling filters. Entamoeba histolytica removal Bacteria 0-2 of 83-99 percent has been reported. Egg removal Protozoa 0-1 appears to be in the range of 20-90 percent, with higher Helminths 0-1 reductions when the effect of secondary sedimentation is included. Removal of various pathogens by trickling filters is Sludge digestion as follows: It is clear from the discussion above that sludge from primary and secondary sedimentation tanks will Viruses Reduction g15 unit) contain a heavy load of excreted viruses, bacteria, Bacteria 0-2 protozoa, and helminth eggs. The fate of these Protozoa 0-2 pathogens depends on which of the many systems of Helminths 0-1 sludge treatment is adopted. Anaerobic sludge Several studies of trickling filters have examined digestion usually operates at one of three time- effluent after it has passed through a secondary temperature combinations: 13 days at 50°C, 28 days at sedimentation or humus tank. This tank may be 32°C, or 120 days unheated. The first stage is often expected to act as a primary sedimentation tank. followed by a second-stage settling or thickening Reductions in helminth eggs of 94-100 percent have process, in which the sludge stands for a time similar to been reported in combinations of trickling filters and that of the first stage to allow the supernatant liquor to humus tanks. be drawn off. If the digestion process is a batch process, thus Acririated sludge ensuring that all the sludge has been at temperature x for time y, the following pathogen removal perfor- Both laboratory data and field experience indicate mances at the specified time-temperature combinations that activated sludge systems are more effective in may be expected: removing viruses than trickling filters.5 Virus removals Coinntion Pathogens remoced in activated sludge treatment works have been 13 days at 50'C All reported as up to 90 percent, although better results 28 days at 32°C Viruses and protozoa: some bacteria (up to 99 percent) are achieved in laboratory or pilot- and many helminth eggs remain scale models. In poorly maintained activated sludge 120 days unheated Protozoa: persistent helminth eggs plants, the finding of low virus removal rates is not (in warm climate) (especially Asearis and Toenial and a of low virus removal rates is not ~~few bacteria and viruses remain unusual. Reductions of excreted bacteria are similar or a little better. Indicator bacteria removal rates are But if the digesters are worked as a continuous process, reported at up to 99 percent, but increases may occur, with sludge being added and removed daily or more Pathogenic bacteria removal rates are commonly frequently, it is not possible to guarantee retention reported as between 60 and 99 percent at normal t aeporati times (6-ween2 0 hours), but mayberasc as 9l times, and pathogen survival will be appreciably higher aeration times (6- t12 hours), but may be as high as 999 than indicated above. percent following extended aeration for Ž1 24 hours. The expected pathogen removal characteristics of The activated sludge process has little effect on sludge treatments, as well as the effect of subsequent sludge thickening, are summarized in figures 6-5 and 4. See Part Two for reports of pathogen removal by trickling 6-6.6 Protozoa will survive none of the digestion and filters. 5. Literature on the efficiency of activated sludge plants in 6. See Part Two for a review of the literature on pathogen survival removing excreted organisms is reviewed in Part Two. in sludge digestion. HEALTH ASPECTS OF SEWAGE SYSTEMS 89 DIGESTION THICKENING DEWATERING (CONTINUOUS) (CONTINUOUS) l SLUEdrying SLUDGE Viruses _ _1- _ _ _ _ _'_ _' (3months) >IHelminths Bacteria /3 days at /3 days _ Protozoa = - 50°C Helminths Ofher l l _ __ _ Lunheated - - Bacteria melhoos >Helminths SLUDGE |Sludge drying SLUDGE Viruses -- - --- ___ (3 months) > Helminths Bacteria 28o dcys at 28 days Protozoa s 32°C Helminths 1- i ------ Vactes unheate - Bacteric Methods Helminths SLUDGE Sludge drying SLUDGE Viruses -- months) Helminths Bacteria - ..120.dayse--;nthl Protozoa unhea/eday /20 days Helminths Other l I ~~~~~~~~~unheated l methods > Heiminths Figure 6-5. Pathogen flow throuigh various continuous sludge treatment processes thickening processes considered. Protozoal cysts are a possibly all, of excreted viruses and bacteria at warm feature of the effluents from conventional treatment temperatures (>20°C). Protozoal cysts will be de- plants and will not be found in treated sludges. With stroyed. Only persistent helminth eggs will survive in continuous operation, thermophilic digestion will significant numbers, especially those of Ascaris, leave small numbers of helminth eggs and excreted Trichuris, and Taenia.7 Other unheated dewatering viruses and bacteria, whereas 120 days of unheated processes-such as vacuum filtration, pressure digestion in warm climates will leave only helminth filtration, and centrifugation-will have little effect on eggs. The sole digestion process producing a pathogen content. thoroughly pathogen-free sludge is batch thermophilic digestion. Helminth eggs will always, and excreted Other sludge treatment processes viruses and bacteria will sometimes, be found in the sludges from all other digestion processes considered Sludge may be composted with refuse, sawdust, (Berg and Berman 1980). woodehips, bark, straw or other material added to provide carbon, lower moisture content and improve texture. Thermophilic composting can achieve excel- Sludge dewatering lent pathogen removal and is discussed in the previous Figures 6-5 and 6-6 also illustrate the effect of sludge dewatering on digested sludges. Drying sludge in open 7. The fate of various excreted pathogens during sludge drying is beds for 2-3 months will remove the great majority, reviewed fully in Part Two. 90 HEALTH HAZARDS OF EXCRETA DIGESTION (BATCH) THICKENING (BATCH) DEWATERING SLUDGE Sludge dr.ying Viruses (3 months) Bacteria - /3 days at /3 days Protozoa 50°C SLUDGE Helminths Ot I lOher l o~~~~~~~~~~nheated methods l l ~~~~~~~~~~~~~~~SLUDGE SLUDGE . P _ __SS/udg F drying Viruses (3 monthHelminths Bacteria -- _ 28 days elths Protozoa F 32 aCy 28 days Helminths Other - Bacteria vinheoted I methods Helminths l l ~~~~~~~~~~~~~~SLUDGE SLUDGE Sludge Viruses - d__lyb mnhs Hgin, Bacteria--- - 20 days Helminths Protozoa 12- unheated dS Hedminths I l I ~~~~~~~~~unheoted l l methods >> Helminths Figure 6-6. Pathogen flow through various batch sludge treatment processes chapter (the section "Composting"). Several other conventional sewage treatment can now be discussed.8 sludge treatment processes are in use or under First considered is a treatment plant featuring trickling experimentation, but most of them are too technically filters and primary and secondary sedimentation. complex and expensive to be appropriate for sludge The effluent from such a plant will contain treatment in developing countries. Those processes- significant concentrations of excreted viruses, bacteria, such as wet oxidation (heating under pressure), protozoa, and helminth eggs and is unsuitable for pasteurization, incineration and pyrolysis-that in- direct reuse in agriculture (see figure 6-7). It may often volve temperatures of 80°C or above-produce a be unsuitable for discharge to freshwater where such pathogen-free product (Osborn and Hattingh 1978). bodies of water are used without treatment for Sludge irradiation has attracted research interest and domestic water supplies by downstream populations. its effects on enteroviruses and fecal indicator bacteria The minimum retention time for liquids in the total are reviewed in chapters 9 and 13, respectively. plant may be around 5 hours, and this explains why the effluent-even if it is of adequate chemical quality (for Complete treatment works instance, the effluent might conform to the established The effect on pathogens of the unit processes having 8. The effect of conventional treatment plants on various been examined, the effect of their combinations in pathogens is reviewed fully in Part Two. HEALTH ASPECTS OF SEWAGE SYSTEMS 91 IN FLU ENT EFFWENT Viruses -----t _ ----- Viruses Bacteria - - Sewage treatment with ---- Bacteria primary sedimentation trickling filters, ond Protozoa = secondary sedimentotion Protozoa Helminths Helminths Helminths Protozoa Bacteria Viruses FRESH UNTREATED SLUDGE Figure 6-7. Pathogen flow through a conventionial sewage treatment plant featuring trickling filters physicochemical standard of <30 milligrams per liter quality from a health viewpoint is through certain of suspended solids and <20 milligrams per liter of tertiary treatment processes; even effluent chlorination standard biochemical oxygen demand, (BOD5)-will be may not be effective (see a discussion of both, below). of poor microbiological quality. Effluent quality may Effluents from activated sludge plants will be of be improved by using double filtration or recirculation, marginally better quality than those produced by but the final effluent will still be highly pathogenic. The trickling filters but will still be heavily contaminated only way to produce an effluent of reasonably good regardless of their chemical quality (see figure 6-8). The INFLUENT EFFLUENT Viruses --- --- XL- Viruses Bacteria -- Sewage treatment with Bacteria primary sedimentation activated sludge and Protozoa ~ secondary sedimentation Protozoa Helminths Helminths Helminths Protozoa Bacteria Viruses FRESH UNTREATED SLUDGE Figure 6-8. Pathogen flow through a conventional sewage treatment plantfeaturing actiuated sludge 92 HEALTH HAZARDS OF EXCRETA minimum liquid retention time in the plant may be illustrated in figures 6-5 and 6-6. From a health only 12 hours, and the final effluent will contain viewpoint, the object of a sewage treatment works significant numbers of any pathogen found in the raw should be to retain all solids and liquids for the sewage. Tertiary treatment is indicated prior to reuse maximum time or to heat them to the maximum or prior to discharge into a river that downstream temperature feasible, or both. Batch processes are far populations are using for water supplies. more reliable in achieving this than continuous The microbiological quality of the sludge depends processes, and thought must be given to the design and on what treatment it receives. Fresh sludges from economics of batch digesters in circumstances where primary and secondary sedimentation tanks will sludge is to be reused in agriculture. contain pathogens of all kinds. Digestion at 50°C for 13 days will kill all pathogens, and digestion at 32°C for 28 days will remove protozoa and enteroviruses, provided Aerated Lagoons that a batch process is used in both instances. Digestion for 120 days without heat in warm climates Aerated lagoons resemble small waste stabilization will remove all pathogens except helminth eggs, also ponds with floating mechanical aerators, but they are only if a batch process is used. Continuous addition more correctly considered as a simple modification of and removal of sludge will allow pathogens to pass the activated sludge process. Reference to the section through all processes. Sludge drying for at least 3 on activated sludge earlier in the chapter and to the months in a warm climate is highly effective against all section on stabilization ponds below, along with the pathogens except helminth eggs. Other unheated description here, will clarify the specifics of this system. dewatering techniques have little effect on the pathogenic properties of sludge. The illustration of this somewhat complex situation Technical description in figures 6-5 and 6-6 shows that only a batch digester In aerated lagoons screened rather than settled operated at 50°C will produce a pathogen-free sludge. sewage is aerated, and there is no sludge return (see Continuous digestion (as in practice) at 50°C may figures 6-9). Retention times for domestic sewage are produce a sludge with excreted viruses and bacteria typically 2-6 days and lagoon depths are 2-4 meters. and helminth eggs if sludge drying beds are not used. The effluent from the lagoon contains 200-500 All other alternatives will produce a sludge containing milligrams per liter of suspended solids (activated helminth eggs and some (such as mesophilic digestion sludge flocs) and therefore requires further treatment followed by vacuum filtration) will produce a sludge either in an ordinary secondary sedimentation tank with excreted viruses and bacteria as well. (retention time: 2 hours, minimum) or in a settling The importance of temperature and time is clearly pond (retention time: 5-10 days). The latter is more Sedimentation tank Sewage -* ( Loon Effluent Sludge Digester Disposal Drying beds Figure 6-9. Flow diagran jbr an aerated lagoonl incorporating siludge digestion. From Mara (1976) HEALTH ASPECTS OF SEWAGE SYSTEMS 93 F M M Stoge I Sewoge_ -0 Stage 2 Aerator Stcige 3 gX_ Figure 6-10. Stages in development of a waste stabilization pond-aerated lagoon system. F. Facultative pond; M maturation pond; A anaerobic pond; AL aerated lagoon. At stage 3 additional maturation ponds will probably be necessary. In some cases septic tanks may replace anaerobic lagoons (usually for populations below 10,000) advantageous because it is often cheaper, easier to however, be treated in one or more maturation ponds maintain, and more efficient in terms of removal of to achieve any desired level of pathogen survival. excreted pathogens. Aerated lagoons are often used to extend the capacity of existing waste stabilization pond systems (see figure 6-10). Oxidation Ditches Pathogen survival In addition to the aerated lagoon, the oxidation ditch is another modification of the activated sludge In the aerated lagoon itself there will be incomplete process. removal of excreted pathogens, although as a result of the longer retention times the removal achieved is Technical description better than that obtained in the conventional activated sludge process. In the settling pond there will be Screened sewage is aerated in, and circulated complete removal of excreted protozoa and helminth around, a continuous oval ditch by one or more special eggs, but schistosome and hookworm larvae may aerators (called "rotors") placed across the ditch (see appear in the effluent, which will also contain figure 6-11). The ditch effluent is settled in a pathogenic bacteria and viruses. The effluent may, conventional secondary sedimentation tank, and Rotor\ Ditch Sewage Effluent 1 Sludge Drying beds Figure 6-11. Flow diagranifo7 an oxidation ditch. From Mara (1976) 94 HEALTH HAZARDS OF EXCRETA almost all the sludge ( > 95 percent) is returned to the the effluent may be reduced but not substantially, and ditch. The small quantity of excess sludge is placed probably insufficiently to justify investment in this directly on sludge drying beds. The hydraulic retention filtration method by the health benefits it yields. times are 1-3 days in the ditch and 2 hours, minimum, in the sedimentation tank. Because a high proportion of the sludge is recycled, the mean retention time for Slow sandfiltration solids is 20-30 days; as a result there is only a small This method may be used in small treatment works. production of excess sludge, which is highly mineralized The low loading rates of the filters (2-5 cubic meters and requires only dewatering on drying beds. The main per square meter daily) causes them to occupy a large engineering advantages of the process are that primary land area. Substantial biological activity builds up, sedimentation is eliminated and that sludge produc- especially in the upper layers of the filter, and pathogen tion and treatment are minimal. removal may be very high. Removal of 4 log,10 units of excreted viruses and bacteria may be expected from a Pathogen survival well-run unit, with virus removal a little higher than bacteria removal. Complete retention of protozoal The effluent from the sedimentation tank has a cysts and helminth eggs has been recorded. Slow sand pathogen content similar to that of the effluent filters are therefore highly effective in removing produced by a conventional activated sludge process, pathogens from a secondary effluent, but their land although as a result of the increased retention time requirement makes them suitable only for small slightly lower survivals are achieved. The small treatment works. quantity of sludge produced is similar in quality to that produced by an anaerobic digester and contains the Land treatment same range of excreted pathogens. Secondary effluents may be applied to land in three ways; application to land for deep percolation and Tertiary Treatment groundwater recharge, application to land for col- lection in underdrains, and application to sloping grass Tertiary treatment methods are increasingly used in plots for collection in downslope channels. The first Europe and North America to improve the quality of two systems can have extremely high pathogen effluent produced by conventional treatment works. removal performances,l" whereas the grass plot system Sophisticated systems designed to reclaim effluent for is less effective because some of the effluent runs over potable water, such as the one used at Windhoek, the surface of the soil, rather than through it. There is Namibia (Stander and Clayton 1977), are not intended little or no information about the application of these by the term, but rather those treatment processes used processes in the tropics or in developing countries. If to upgrade the physicochemical quality of an effluent poorly managed, they will probably lead to the prior to discharge. Tertiary treatment processes creation of a foul and unsanitary bog. In addition, all originally were not designed primarily for pathogen land application systems pose the potential threat of removal, but some of them do have good pathogen groundwater contamination. removal characteristics.9 Maturation lagoons Rapid sanidfiltration Conventional effluents can be upgraded in matur- This is perhaps the most common tertiary treatment ation lagoons. The principles involved are exactly as found in larger treatment works. High loading rates described for waste stabilization ponds (see the section (200 cubic meters per square meter daily) and frequent of that title, below, and figure 6-10). If two or more backwashing (1-2 days) prevent the build up of much maturation ponds are used, with perhaps 5 days of biological activity in the filter. Some viruses will be retention in each, total removal of protozoal cysts and adsorbed to solids and some bacteria retained. helminth eggs will be achieved. High levels of virus and Protozoal cysts and helminth eggs may be retained because of their size. In short, the pathogen content of 10. See chapters 9 and 13 and Uiga and Crites (1980). 9. The effect of tertiary processes in removing excreted pathogens 11. See chapter 7, the section "Effluent Discharge. To ground- from secondary effluents is reviewed in Part Two. water." HEALTH ASPECTS OF SEWAGE SYSTEMS 95 bacteria removal are also effected, and a pathogen-free the effluent are affected by the chlorine, many of which effluent may be produced by adding sufficient ponds. are essential for the effluent's natural self-purification. If the effluent is discharged into a river or lake, the chlorine may adversely affect the ecology of the Other tertiary treatment processes receiving water and hinder its natural oxidation Several other tertiary treatment processes are in use processes. Further, the chlorine will be present in such or under experimentation, including coagulation, forms as chlorinated organic compounds, which are carbon adsorption, irradiation, and ozonation. The less biodegradable than their parent compounds and effects of these on enteroviruses and fecal indicator are directly toxic to fish and other aquatic life (Water bacteria are reviewed in chapters 9 and 13. These Research Centre 1979). processes are, in general, too technically complex and Excreted viruses are more resistant to chlorination costly to be appropriate for sewage treatment in than bacteria.13 Chlorine doses of 30 milligrams per developing countries. liter and above have been recommended; even so, complete viral removal may not be achieved (Melnick, Gerba, and Wallis 1978). It appears, at least from Effluent Chlorination South African experience (Nupen, Bateman and McKenny 1974), that chlorination beyond the The chlorination of sewage effluents is commonplace breakpoint-with resultant free, residual chlorine as in only a few countries (notably the USA, Canada, and HOCI-may be necessary to effect viral removal. Israel). Its purpose is to reduce the pathogen content of Depending on the chlorine demand and pH of the conventional effluents. As discussed earlier, it repre- effluent, breakpoint chlorination may require high sents the borrowing from the water treatment industry doses and will always require efficient and vigilant of a technology that might overcome the poor process control. pathogen removal characteristics of conventional It is most unlikely that chlorination of effluents will treatment systems."2 Effluent chlorination has a be effective in eliminating protozoal cysts because they number of serious limitations, the principal one being are more resistant than either excreted viruses or that in some senses it does not work. At best, bacteria. Most helminth eggs will be totally unharmed chlorination is complex and difficult to control. by effluent chlorination. Chambers (1971) writes that It is evident from these shortcomings that effluent chlorination may not be particularly effective in Chlorination of wastewater effluents iS a vastly more rmvn ahgn rmcnetoa flet.Ta complex and unpredictable operation than chlori- removing pathogens from conventional effluents. That nation of water supplies. It is extremely difficult to maintain a high, uniform, and predictable level of consequences-including the proliferation in water disinfecting efficiency in any but the most efficiently supplies of carcinogenic chlorinated hydrocarbons, diecatingwast treffiien nt panytbu themosteffiently which are formed by the reaction of chlorine with organic material-must also be considered (Buxton For these reasons it should be rejected except where the and Ross 1979; Carlo and Mettlin 1980; Deinzer, highest levels of management and process control are Schaumburg, and Klein 1978; Grabow 1979; Hais and guaranteed. Venosa 1978; Wilkins, Reiches, and Kruse 1979). Chlorine has to be applied in heavy doses (10-30 Nupen and Morgan (1978) write, regarding effluent milligrams per liter) to achieve coliform concentrations chlorination below the breakpoint in South Africa, of less than 100 per 100 milliliters of effluent. These that levels of chlorine will also kill pathogenic bacteria if the chloinedemnd o th efluen isnottoo igh ifthe Present findings indicate that the practice not only chlorine demand of the effluent isre ot well hixedh if th fails to provide an effective barrier to the spread of chlorine and the effluent are well mixed, and if diseases but ignores the environmental impact on adequate contact time (at least 1 hour) is allowed. But receiving waters ... Under no conditions can this regrowth of coliforms and Escherichia coli following type of chlorination be considered as a substitute for chlorination has been widely reported (for instance, Shuval 1977), and the regrowth of pathogenic bacteria the adequate treatment of wastes. has not been fully ruled out. Moreover, all bacteria in 12. See chapter 4, the section "Objectives of Night Soil and 13. Inactivation of enteroviruses and fecal indicator bacteria by Sewage Treatment." effluent chlorination is reviewed in chapters 9 and 13. 96 HEALTH HAZARDS OF EXCRETA Waste Stabilization Ponds normally be used in conjunction with one another to form a series. Although it is all too common to find only a single facultative pond treating domestic wastes, Waste stabilization ponds are the most economic this represents a false economy when health is method of sewage treatment wherever land is available considered.Mtura pondsyare ne arto es at~~~~~~~~~~~~~ reaieylwcs Mig n ed17) hs considered. Maturation ponds are necessary to ensure e. T low pathogen survivals. Good designs (see figure 6-10) they are widely used in North America. But their incorporate a facultative ond and two or more principal advantage in warm climates is that they paturation pond astes orhmore maturation ponds; for strong wastes (biochemical achieve low survival rates of excreted pathogens at a . . much lower cost than any other form of treatment, with of anaerobic ponds as pretreatment units ahead of maintenance requirements simpler by several orders of facultative ponds is often advantageous because they magnitude. In fact, a pond system can be designed to minimizvhe land requirements of the whole pond ensure, with a high degree of confidence, the total mi elimination of all excreted pathogens. This is not system usually achieved in practice because the incremental benefits resulting from achieving zero survival, rather Pathogen survival than low survival, are less than the associated Several authors have reported the fate of fecal incremental costs. Yet waste stabilization ponds are indicator bacteria in ponds (see chapter 13)i4 High the best form of treatment in tropical, developing removal rates of 99.99 percent or better have been countries because they can achieve any level of reported for series of three, four, or more ponds. pathogen removal desired. From a strictly health- reported elimination of Salmour, or o ther directed viewpoint, the fact that ponds can do this at Cmlt lmnto fSloel n te directed viewpoint, thenteropathogenic bacteria can be achieved in pond lowest comparable cost is an additional advantage. systems with long retention times (30-40 days), particularly if ambient temperatures are above 25°C Technical description (see chapters 13 and 15). It is known from both Waste stabilization ponds are large, shallow ponds theoretical considerations and field experience that a in which organic wastes are decomposed by micro- series of ponds will perform far better in removing BOD organim in waste a re dcombination posed na l proes and excreted bacteria than will a single pond with the organisms in a combination of natural processes sm vrl eeto ie eiso iet ee invotving both bacteria and algae. The waste fed into aof five to seven stabilization pond system can be raw sewage, ponds, each with a retention time of 5 days, can aquaprivy effluent, or diluted night soil (figure 6-10). produce an effluent containing 100 fecal coliforms and There are three kinds of ponds in common use: fecal streptococci per 100 milliliters. Such an effluent can be safely used for unrestricted irrigation. Little is known at present about the fate of viruses in * Anaerobic pretreatment ponds, which function ponds in warm climates or developing countries (see similarly to open septic tanks; they have retention chapter 9). Viruses adsorb to solid particles that may times of 1-5 days and depths of 2-4 meters. settle to the sludge layer, and other biological and c Facultative ponds, in which the oxygen necessary physical factors may be specifically virucidal; for for biooxidation of the organic material is supplied instance an increase in pH to Ž. 9 caused by blooms of principally by photosynthetic algae, which grow algae. Irrespective of such effects, inactivation of naturally and with great profusion in them; they excreted viruses will proceed rapidly in warm waters, have retention times of 10-40 days and depths of and may be 1-2 log units per 5 days in ponds at 1-1.5 meters. > 25°C. A pond system with an overall retention of 30 C Maturation ponds, which receive facultative pond days in a warm climate should therefore achieve a effluent and are responsible for the quality of the reduction of excreted viruses of not less than 6 log final effluent; they have retention times of 5-10 units (99.9999 percent). days and depths of 1-1.5 meters. Reports on the effect ofponds on protozoal cysts and helminth eggs (see chapters 20 and 23) indicate 100 percent removal in all cases in which well-designed, Anaerobic and facultative ponds are essentially multicelled ponds with a total retention time of > 20 designed for biochemical oxygen demand (BOD) removal, whereas the function of maturation ponds is 14. A compilation of original sources and findings on pathogens the destruction or removal of excreted pathogens. in waste stabilization ponds is given in Part Two, especially chapters These three ponds are complementary and should 9, 13. 20. and 23. HEALTH ASPECTS OF SEWAGE SYSTEMS 97 days were investigated. Hookworm larvae may survive supervised staff of laborers who should be employed on for up to 16 days in aerobic ponds. Because of this fact, all waste stabilization pond plants. Mosquito breeding hookworm larvae have been reported in the effluent in ponds can thus be largely circumvented by good from ponds with an overall retention time of < 10 days; design and good maintenance. they have not, however, been reported in the effluent of In summary, well-designed pond systems- ponds with retention times of > 20 days. The majority incorporating a minimum of three cells, and having a of schistosome eggs in an aerobic pond will settle; in a minimum total retention time of 20 days (see figure 6- facultative pond they will either settle or hatch into 12)-produce an effluent that will contain only small miracidia. Miracidia will either die or infect an concentrations of excreted bacteria and viruses. intermediate snail host if the correct snail species is Excreted helminth eggs and protozoal cysts will be colonizing the pond (as may be the case in badly completely eliminated. Bacterial or viral pollution can maintained and vegetated ponds). Even if cercariae be further reduced (or eliminated) by adding more emerge, they should not find a human host to invade ponds to the system. The effluent is suitable for direct and will die within 48 hours. reuse or discharge into receiving waters. An important consideration in the design and operation of waste stabilization ponds is that they may become sites for mosquito breeding. The most Literature Cited common mosquitoes found breeding in ponds belong to the Culex pipiens complex, which favors polluted Berg, G. and Berman, D. (1980). Destruction by anaerobic water. The distance between the town producing the mesophilic and thermophilic digestion of viruses and indicator bacteria indigenous to domestic sludges. Applied sewage and the pond system treatingsit ishusay we and Environmental Microbiology, 39, 361-368. withinthe flight range of the mosquitoes,whichmaybe Buxton, G. V. and Ross, S. A. (1979). Wastewater as great as 10 kilometers. Any large outbreak of disinfection-toward a national policy. Journal of the mosquitoes will thus be a nuisance (depending on the WVater Pollution Conitrol Federation, 51, 2023-2032. weather conditions at the time). Moreover, because the Carlo, G. L. and Mettlin, C. J. (1980). Cancer incidence and mosquitoes can serve as vectors for disease, it is trihalomethane concentrations in a public drinking water essential to attempt to keep waste stabilization ponds system. American Journal of Public Health, 70, 523-525. free of mosquitoes. Studies on mosquitoes in ponds Chambers, C. W. (1971). Chlorination for control of bacteria (reviewed in chapter 36) indicate that emerging and and viruses in treatment plant effluents. Journal of the encroaching vegetation are important in encouraging Water Pollution Conttrol Federation, 43, 228-241. breeding. It is easy in practice to discourage vegetation Deinzer, MI., Schaumburg, F. and Klein, E. (1978). growth in ponds by making the ponds > 1 meter deep Environmental Health Sciences Center Task Force review growth inpndsing thcreteslabs,rip , pondsoi cementen dhee of halogenated organics in drinking water. Envir-onmiental and usmg concrete slabs, rip-rap, or soll cement on the Health Perspectives. 24, 209-239. embankments at the surface water level. Reinforcing Grabow, W. 0. K. (1979). Disinfection of water: pros and the pond's banks not only prevents vegetation from cons. Water South Africa, 5, 98-105. growing down the embankment but also halts erosion Hais, A. B. and Venosa, A. D. (1978). EPA overview of of the embankment by wave action. Any residual municipal wastewater disinfection. Joturnal of tlte Wiater vegetation problem may be dealt with by the well- Pollution Conttrol Federation, 50, 2470-2476. INFLUENT EFFLUENT Viruses ----__ _ -----e- Viruses Waste-stcabi/&ictibn ponds Bacte ria *- 6 teristics similar to this hypothetical example (Cohen months). Their removal from effluent will require and others 1971). either the use of waste stabilization ponds or tertiary treatment in the form of sand filtration, land Foodstuffs for animal consumption application, or lagooning. Removal of Taenia eggs from sludge requires either a thermophilic process or A widespread use of sewage effluents, sludge, and retention for over a year. T saginata infection in night soil is in application to pastures or fodder crops humans is not a major public health problem in most subsequently fed to animals. In the United Kingdom, countries. The importance of controlling the infection for instance, 74 percent of all sewage works sludge is lies in its consequences for the beef industry. Carcasses disposed of on land, the remainder dumped at sea. Of found to contain the cysts of T saginata are condemned the sludge disposed of on land, 21 percent is spread on in whole or in part and the economic loss is substantial grazing land, 35 percent on general arable land, 33 in areas of high transmission. percent is dumped, and the remainder is used in horticulture, forestry, and land reclamation. Of the SALMONELLOSIS. Sewage effluents, sludges, and sludge applied to grazing land, 29 percent is applied night soil from all large communities in both rich and raw and 71 percent is applied following digestion poor countries will contain substantial numbers of (Standing Committee on the Disposal of Sewage salmonellae. Figures of 104 organisms per liter of raw Sludge 1978). A wide variety of animal pathogens may sewage and of raw sludge are not uncommon in be encountered in sewage sludge, and night soil, Europe. These salmonellae may reach pastures or including: fodder crops and may infect animals and animals may subsequently infect people. The infective doses Viruses causing: Bacteria causing: Helminths calusing: required are high, however, and Salmonella infections Foot and mouth Anthrax Beef tapeworm are transmitted among cattle by many ways other than disease Brucellosis infection contaminated fodder. There is no clear evidence that Porcine Leptospirosis Pork tapeworm cattle grazed on pastures fertilized with wastes are at encephalomyelitis Salmonellosis infection Rabies Tuberculosis more risk from salmonelloses than other cattle (see Rinderpest chapter 15). Swine fever TUBERCULOSIS. Wastes from institutions treating tuberculosis patients, or from industries such as dairies HEALTH ISSUES. Despite this alarming array of and abattoirs that handle tuberculous animals, will infections, it is clear that, in most cases, the sewage or almost certainly contain Mycobacterium tuberculosis. sludge will contain an insignificant number of these Studies in Denmark (Jensen 1954) showed tubercle pathogens and will have a negligible effect in transmitting these diseases. There are three exceptions, . Pork tapeworm (Taenia solium) infection has been omitted ' from this discussion because, although the use of human wastes on however,,in whic the use of huma wastesonpastres fodder crops fed to pigs would undoubtedly promote the or fodder crops may promote the transmission of transmission ofthis helminth, in practice its life cycle usually depends diseases of significant human or veterinary impor- on pigs gaining direct access to human feces, which they eagerly eat. 102 HEALTH HAZARDS OF EXCRETA bacilli in the sewage produced by 5 towns with elsewhere, of using effluents to irrigate parks, lawns, tuberculosis sanatoria. Tubercle bacilli were also central concourses or medians of highways, and other demonstrated in the effluent, digested sludge, and 5- open amenity areas. Effluents are sometimes brought week-old dried sludge from the treatment plants olthese in tankers from the treatment works to the city center towns. for this purpose. Where conventional treatment works Chlorination will remove tubercle bacilli from without tertiary processes are operating, this practice sewage effluent, although they are more resistant than involves great risk to the public health and should be Escherichia coli. In one experiment an applied dose of condemned. It is only acceptable to use the effluents 10 milligrams per liter of chlorine removed tubercle from waste stabilization pond or tertiary treatment bacilli from an effluent having a BOD5 of 11-63 processes and, even then, very careful monitoring ofthe milligrams per liter (Jensen 1954). Greenberg and pathogen content in these effluents is required. Kupka (1957) concluded, however, that a chlorine dose Compared with other reuses described in this chapter, of 20 milligrams per liter and a contact time of at least 2 the irrigation of amenity areas is a high-risk activity. hours were required to remove tubercle bacilli from a well-oxidized effluent. Sludge has been recorded as containing at least 7 x 105 tubercle bacilli per gram of Occupational hazards dry matter (Heukelekian and Albanese 1956), and 15 A health hazard common to all the agricultural reuse months on a drying bed were required to remove these practices considered above is the risk to those who in Denmark (Jensen 1954). Sludge may also be actually work in the fields. Although there is very disinfected by thermophilic processes, in which limited epidemiological evidence to demonstrate the tubercle bacilli are killed after 20 minutes at 66°C. fact, it is likely that those who work in fields In summary, tubercle bacilli may be numerous in contaminated by excreted pathogens are at greater risk sewage, sludge, and night soil, and they are more than others. If fieldworkers bring these infections back persistent and resistant to disinfection than the enteric into their homes and subsequently infect their families, bacteria. The epidemiological significance of this is then a measurable difference in their health compared unclear. There is a case reported of tuberculosis in with that of nonagricultural workers and the whole children who fell into a river polluted by sanatorium community may not be apparent. Moreover, in many wastes (Jensen 1954). It remains most doubtful, agricultural communities practically the whole popu- however, that transmission of either human or bovine lation works in the fields at some time of the year, and tuberculosis is significantly affected by exposure to so all may be exposed to the risk (although not wastes or polluted water.2 equally). The only sure way to protect the health of the Other agricultural products agricultural workers is to use only wastes that are pathogen free or nearly so.3 Once again this means Fecal wastes may also be used to produce crops not only effluents that have undergone waste stabilization intended for consumption by animals or humans. pond or conventional treatment followed by land Examples are tree cultivation for timber production, application, sand filtration, or lagooning. Similarly, beautification, or the control of desertification; the sludges or night soil require batch thermophilic irrigation of parks; and the cultivation of commercial processing, protracted drying, or storage for over I crops such as cotton or coconuts (Sundaresan, year. Muthuswamy and Govindan 1978). These reuse A special problem affecting the health of agricultural technologies pose health hazards mainly of an workers is spray irrigation using sewage effluent. occupational kind. Workers in the fields and in the Aerosol droplets containing excreted viruses and factories where the crops are processed are at risk (see bacteria may travel several hundred meters downwind, the next section). and excreted bacteria may be more infective (that is, One reuse system worth special mention is the have a lower infective dose) when inhaled than when practice, now widespread in the Middle East and 3. This recommendation, with some others in Part One of this 2. Tuberculosis has not been considered in Part Two. Those book, concerns ideal practice and is directed to those contemplating wishing to read further may consult Greenberg and Kupka (1957); the establishment of new waste treatment and reuse projects. For Heuke1ekien and Albanese (1956); Jensen (1954); Maddock (1933); those trying to upgrade existing systems, it should he noted that any Pramer, Heukelekien and Ragotzkie (1950); Viraraghavan and measurable reduction in the pathogen content of a waste is likely to Raman (1967); and Williams and Hoy (1930). improve public health. EXCRETA REUSE AND EFFLUENT DISCHARGE 103 otherwise ingested.4 There is therefore some cause for Pathogen control in agricultural reuse concern that aerosol-disseminated excreted viruses and acteia an ifec, byinhaatin, tosewho ork There is now a substantial literature on the health and bacteria can infect, by inhalation, those who work implications of the agricultural reuse of excreta, much in, or live near to, spray-irrigated fields. A quite of which is reviewed in Part Two. Several reviews of the different potential hazard of spray irrigation is that it topic, which some readers may find of additional value, often causes ponding of effluent, and this might lead to ar6lso alable.f increased populations of Culex pipiens, and other are also avarlable d mosquitoes breeding in dirty water (Sorber and Guter It is clear from the dwscusslon above that a desirable 1975). public health policy would be to require the highest A study in Israel (Katzenelson, Buium, and Shuval quality standards for all wastes reused in agriculture. 1976) showed that people in kibbutzim (cooperative For effluents, this standard might be expressed in terms agricultural settlements) practising spray irrigation of a fecal coliform count of less than 100 per 100 . . . . ~~~~~milliliters (World Health Or anization 1973). Such a with waste stabilization pond effluent had a higher g incidence of shigellosis, salmonellosis, typhoid, and standard, however, may tell little about the effluent infectious hepatitis than people in kibbutzim practis- content of viruses, protozoa, and helrrinth eggs, ing no form of wastewater irrigation. This could be especially following the chlorination of the effluent, a attributed either to the agricultural use of wastewater process considerably more lethal to excreted bacteia or specifically to the spray technique promoting than to other excreted pathogens (see the previous aerosol transmission. Subsequent debate, and new chapter). As discussed in chapter 4, E. coli is also an studies in Israel (Shuval and Fattal 1980), have cast inappropriate indicator for the quality of treated doubt on tsfsludges or night soil. For these materials the doub on hesefindngs Thee isno cncluive concentration of Ascaris eggs is a better guide to epidemiological evidence of adverse health effects overathon cnet7 Criteisa for Acis hv caused by exposure to wastewater aerosols at spray overall pathogen contenta CrGtera for Ascaris have irrigation sites or sewage treatment plants (Pahren and 1978). Jakubowski 1980). Such health effects, if they do exist, 1978). are less likely in dry, sunny climates than in temperate Teipsto fsrnetqaiysadrso arealess lelys vin y sunny baclteshan in tempere effluents (for example, < 100 fecal coliforms and fecal climates because viruses and bacteria in aerosols are stetooc pe 10 millies retit.herneo rapidly inactivated by warm temperatures, low streptococci per 100 mlliliters) restricts the range of humidit an brig sunlight.5 treatment technologies considerably. It is fortunate humpeidity ig h i that waste stabilization ponds are able to meet these A specific occupational hazard in the agricultural stnadadaralo-s,aporiefrm f reuse of excreta is schistosomiasis. Of the various standards and are a low-cost, appropriate form of species, the one whose transmission has been related to waste treatment in hot climates (see chapters 4 and 6). deliberate reuse rather than incidental pollution is Irrigation with waste stabilization pond effluent is Schistosoma japonicum. The eggs survive in feces for therefore recommended. The imposition of strict quality standards on sludges over a week, so that when excreta are applied fresh to irrigated rice fields containing the amphibious snail or night soil (< 10 viable Ascaris eggs per 100 grams, hosts, the snails may become infected. This occurs in for example) poses greater problems. Such standards several parts of Southeast Asia and, most notably, in can only be achieved by well-managed thermophilic China. After the schistosomes have developed within digestion or composting, or by retention times of > 1 the snails, larvae that can bore through the human skin year. A second-best choice, as indicated in figure 6-6, areshedintothewater, thus creatingtheoccupational would be batch mesophilic digestion followed by are~~~ ~ she inotewtr.hsceaigteocptoa several months on drying beds. An alternative for night risk to farmers. The snail-transmitted larvae of other seue isnts os in A altative stabizt flatworms encyst on vegetables or in fish and crabs, so soil reuse is its deposit in a facultative stabilization that they infect the consumer rather than the pond to produce a small effluent flow for irrigation or agricultural worker. Excreta can be rendered free of fish farming. live schistosome eggs by suitable treatment (see 6. See, for instance Benarde (1973): Bryan (1977); Burge and chapter 32). Marsh (1978); Crook (1978);Engelbrecht (1978); Gerba, Wallis and Melnick (1975); Goldberg (1979); Hickey and Reist (1975); Pahren and others (1979); Petrik (1954); Rudolfs, Falk and Ragotzkie (1950 4. Enteroviruses and fecal indicator bacteria in aerosol droplets and 195i a f); Shuval (1977); Sorber and Guter (1975); Sorber and are discussed fully in the relevant sections of chapters 9 and 13. Sagik (1978); Wiley (1962); Wiley and Westerberg (1969) and World Health Organization (1973). 5. The costs of alternative methods of reducing any health hazards associated with spray irrigation are reviewed by Young (1980). 7. See Chapter 4, the section "Pathogen Indicators." 104 HEALTH HAZARDS OF EXCRETA In conclusion, stringent quality standards may be set In addition to promoting productivity, growing fish upon waste intended for agricultural reuse, and these in waste-enriched ponds has other advantages. With standards can be achieved by relatively simple and low- reference to sewage treatment, nutrient removal is cost technologies. Major problems in pathogen improved because nitrates and phosphates concentrate removal will only be encountered where conventional in the food chain and are thus removed during sewage treatment plants are in use. Such plants harvesting of the fish (Wert and Henderson 1978). The produce both an effluent and a sludge that are rich in bacteriological quality of the sewage may also improve pathogens and that require expensive additional because the presence of fish appears to raise the oxygen treatment (see the previous chapter) before they can be levels and the pH (generally, to over 8.5) of the ponds, recommended for unrestricted agricultural reuse. and both of these effects increase the death rate of enteric bacteria. Furthermore, there is some evidence that fish reared in sewage are less prone to disease than Reuse in Aquaculture others. Human excreta may be reused to promote the HEALTH ISSUES. There are three distinct health growth of aquatic flora and fauna, a practice known as problems associated with fish farming in excreta- aquaculture. Three principal kinds of aquaculture are enriched ponds: common: fish farming, algae production, and mac- . P rophte (acrocopc aqaticplat) poducion* Passive transference of animal pathogens by fish rophyte (macroscopic aquatic plant) production. contaminated by polluted water. * Transmission of helminths whose life cycles involve Fish lfrming fish as intermediate. host. The raising of fish in ponds enriched with human * Transmission of other helminths with life cycles and animal excreta has a long tradition. In China and inmvolvmg other pond fauna, such as the snal elsewhere in Asia it has been operating continuously for centuries; it was practised in ancient Egypt and was The first of these problems is a cause for concern widely used by European monasteries in the Middle throughout the world, whereas the second and third Ages. apply only in areas where particular eating habits are The controlled addition of wastes to ponds causes a found, where the helminths concerned are endemic, or large population of bacteria to thrive; these organisms both. in turn promote communities of phytoplankton (algae) and zooplankton, which then graze on the algae. With PASSIVE TRANSFERENCE OF EXCRETED this rich food chain available, some fish, notably carp PATHOGENS. Fish may passively carry excreted human and tilapia, grow rapidly. Different fish species pathogens in their intestines or on their body surfaces, occupy different ecological niches-some feeding on and these pathogens may subsequently infect people large algae, some on small algae, some on zooplankton, who handle, prepare, or eat these fish. There is little risk some in the bottom layers, and some nearer the surface. to fish eaters except in areas where fish are eaten raw or For this reason, polyculture (the growing of several partially cooked. Thorough cooking will destroy all species in the same pond) is widely practiced excreted pathogens. The risk to those who handle or (Muthuswamy and others 1978) because it greatly prepare the fish, however, is unaffected by the local increases the total fish yield. eating habits. Fish may be grown in ponds enriched with sewage or Most studies on pathogen carriage by fish are night soil. Where sewage is used, it is usually related to fish caught in sewage-polluted seawater or pretreated, diluted, or both. An appropriate system is rivers, but the principles of pathogen carriage will to grow fish in the maturation ponds of a chain of waste apply to fish farming as well. There is abundant stabilization ponds (seefigure6-lO);fish (except theair- evidence that the intestinal bacteria of humans and breathing varieties) cannot be grown in facultative animals are not the normal resident flora of fish. Fish ponds because the biochemical oxygen demand (BOD) raised in contact with these bacteria may, however, may exceed the oxygen supply. with the result that the acquire substantial numbers of them on their bodies water becomes deoxygenated, and the fish die. Night and in their intestines. Fecal coliforms, fecal streptoc- soil is commonly added to ponds either by locating occi, and salmonellae are easily isolated from fish latrines directly over them or by delivering night soil to grown in polluted waters. A concentration effect is them in carts or trucks. discernible, and concentrations of enteric bacteria in EXCRETA REUSE AND EFFLUENT DISCHARGE 105 fish intestines tend to be higher than in the water in preservative and pickling techniques for fish have little which the fish live. There is even evidence of their effect (see chapter 24). ability to multiply in the intestines of some fish (see Where fish are grown in pretreated or presettled chapters 13 and 15). sewage, Clonorchis eggs will have settled. Transmission It is quite possible for pathogenic bacteria carried by is therefore associated with the direct enrichment of fish in this way to infect people. It is equally possible for ponds with night soil or raw sewage. Clonorchis eggs the contaminated fish to infect (especially with are fragile and die if stored for a few days in night soil. Salmonella) the animals fed on fishmeal and the people Seven-day storage of night soil prior to pond who eat these animals. In practice, however, it is enrichment is therefore a sound strategy for the control equally likely that the fish will become infected after of this infection, but it must be noted that this helminth harvesting and during handling, transport, and has other vertebrate hosts (such as dogs and cats) processing (Brown and Dorn 1977). The major besides man and that the control of human excreta may outbreaks of salmonelloses in animals and man known only partially reduce transmission. to be associated with fish have been associated with contamination after harvesting. It remains quite HELMINTHS WITH OTHER AQUATIC INTERMEDIATE possible for fish to carry bacterial pathogens passively HOSTS. Third, it is possible that schistosomiasis from enriched ponds to humans and thereby to cause transmission through the presence of the approp- infection. The survival of excreted bacteria in fish riate species of snails as intermediate hosts-may entrails or in fish transferred to clean water is generally occur in the ponds and infect fishermen. This requires reported as less than 14 days (see chapter 13), although that fresh eggs or miracidia are reaching the ponds, an some data suggest that salmonellae may survive for 2 event that can be prevented by using only sewage months in fish guts (see chapter 15). treated in stabilization ponds or stored night soil (see There is little information about the carriage of chapter 32). nonbacterial pathogens by fish. One must assume that viruses, protozoal cysts, and helminth eggs can all be PATHOGEN CONTROL. In summary, fish farming carried, and even concentrated, in or on fish and that uses excreta or sewage carries with it the hazards thereby infect the eaters or handlers of fish. Helminth of passive carriage of a range of pathogens and of eggs will tend to settle to the pond bottom and therefore transmission of Clonorchis and schistosomes in some may only be ingested by bottom-feeding fish (such as parts of the world. Pathogen control may be the common carp, Cvprinus carpio). accomplished by: HELMINTHS HAVING FISH AS INTERMEDIATE HOSTS. * Enriching ponds only with treated sewage, stored The second, and quite distinct, health problem night soil, or sludge associated with fish farming is the transmission of * Allowing fish to reside in clean water for several worms parasitic to man that have fish as intermediate weeks prior to harvesting hosts. The major helminths of this kind are Clonorchis * Clearing vegetation from pond banks to discourage host. Te mjor elmnth of hiskin are Clnorhis the molluscan intermediate hosts of Clonorchis and sinensis (Chinese liver fluke), Diphyllobothrium latum the scansoso es (fish tapeworm), Heterophyes heterophyes, and Meta- the schistosomcs gonimus yokogawai. Of these, Heterophyes and * Promoting good hygiene in all stages of fish Metagonimus are of no major public health importance handling and processing (they are primarily parasites of dogs and cats, and * Discouraging the consumption of undercooked Heterophyes only infects fish in brackish water-see fish. chapter 30). Diphyllobothrium infects pike, perch, turbot, and other fish found in lakes or rivers and is not Algal culture associated with enriched ponds (see chapter 25). Instead of growing fish in waste-enriched ponds with Clonorchis sinensis and the related species of cat liver large algal populations, it is possible to harvest the flukes, Opisthorchis viverrini and 0. felineus, however, algae directly. This is as yet only an experimental are associated with excreta-fed fishponds and are technique, but it may well find large-scale application intensively transmitted where fish are eaten raw or in the coming decades. The advantage is that partially cooked. Infection occurs principally in China, harvesting at a lower trophic level ensures far higher Korea, Taiwan, Thailand, and Vietnam, and the local yields of biomass and protein. For instance, the yields prevalencecanreach60percent.Cookingoffishmustbe to be hoped for from sewage-enriched fishponds are in thorough to kill the encysted larvae, and most the order of 10,000 kilograms per hectare yearly 106 HEALTH HAZARDS OF EXCRETA (Muthuswamy and others 1978), whereas algae Some are harvested wild, and some are cultivated; they production in high-rate ponds may be up to 150,000 include water spinach (Ipomoea aquatica), water kilograms per hectare yearly. The algae are appro- chestnut (Eleocharis dulcis or E. tuberosa), water ximately 50 percent protein, and thus protein yields of hyacinth (Eichhornia crassipes), water bamboo 75,000 kilograms per hectare yearly are achieved. This (Zigania spp.), water calthrop (Trapa spp.), and lotus compares favorably with protein yields from rice (56 (Nelumbo nucifera). Some of these plants (for instance, kilograms per hectare yearly), corn (270 kilograms per water spinach) are intensively fertilized with human hectare yearly), and soybeans (650 kilograms per and animal wastes, whereas others are grown in water hectare yearly) (McGarry 1971). that may be incidentally contaminated (National Algae may be harvested by flocculation with lime or Academy of Sciences 1976). aluminum sulfate followed by flotation (McGarry Attention has recently focussed upon the use of 1971), or by partial removal by microstraining. Oswald water hyacinth in waste treatment and recycling and others (1978) reported that algae are harvested systems (Dinger 1978a, 1978b; Wolverton and from shallow ponds in the Philippines by simple MacDonald 1979). Water hyacinth removes nutrients, sedimentation, with a production of 47,000 kilograms metals, and phenols from wastewaters (Cornwall and per hectare yearly. These various methods produce an others 1977). The hyacinth can be harvested and used algal paste or sludge containing 8-10 percent solids, as animal feed, processed to produce fertilizer, or used which is then sun dried. An overview of the engineering to generate methane (see the section on biogas below). and economic aspects of algae production in high-rate If water hyacinth is introduced, however, the ecological ponds is given by Lee and others (1980). consequences of its escape into irrigation systems (it grows rapidly and can clog waterways) must also be HEALTH ISSUES. High-rate ponds have a short considered. Such systems for intense recycling of retention time of around 1 day. Pathogen removal is wastes are usually fed by sewage but could be fed by therefore minimal, and the harvested algae will be rich night soil or sludge. in excreted viruses, bacteria, protozoa, and helminth eggs. HEALTH ISSUES. The health hazards associated with these aquacultural practices are of three types. PATHOGEN CONTROL. The most effective removal First, there is the occupational risk to those who process is sun drying. Ifthe algae are dried to less than 5 work in the water, especially where intensive use of percent water, pathogen removal will be complete. If night soil occurs. These workers may accidentally not, pathogens will survive to a degree dependent upon swallow pathogens or carry pathogens back to their drying time, final moisture content achieved, and homes on their clothing or bodies, and they may sunlight intensity. There are no data on pathogen become infected percutaneously with schistosomiasis survival on drying algae, but it may be assumed that in areas where the disease is endemic and the protozoa will be rapidly removed (in a few weeks) and intermediate host snails reside in the ponds or flooded that bacteria may be killed by algal toxins and other fields. factors. Viruses and helminth eggs will be long-term Second, the harvested plants may be heavily survivors, with the latter enduring for a year or more if contaminated with pathogens and may infect those who moisture content in the algal sludge stays above 10 harvest, handle, prepare, or eat them. Some of these percent. plants, such as water chestnut in China, are eaten raw. The health hazards involved in the reuse of this algal Third, the parasitic fluke Fasciolopsis buski is locally product will vary. If the algae are fed to cattle, the important in some parts of Asia and may infect 10 major requirement will be the elimination of Taenia million people. This worm has a life cycle that moves saginata eggs, Salmonella spp., and Mycobacterium from man (or pig or dog) to snail to water plant to tuberculosis (see above). If they are fed to chickens, the man. Animals or people become infected by eating major requirement may be removal of Salmonella and the encysted metacercariae on water plants, especially Campylobacter. If they are fed to people (as in Japan), Eleocharis, Eichhornia, Trapa, and Zigania (see chapter they will require thorough disinfection prior to 28). packaging and marketing. PATHOGEN CONTROL. Control of these health Macrophyte culture problems depends chiefly upon the treatment of night Around the world, but especially in Southeast Asia, soil and other wastes prior to their discharge or prior to many water plants are used for human or animal food. their use as fertilizer for aquatic plants. The health EXCRETA REUSE AND EFFLUENT DISCHARGE 107 requirements for a particular plant production system heated (although they may be lagged or buried), and so must derive from a consideration of exactly what kinds they operate at around ambient temperatures. Gas of process are being used to grow which crops, and the production falls off considerably at lower temperatures degree of mechanization incorporated. In addition to and may be negligible below 15°C. adequate treatment of the fecal wastes used, attention to crop harvesting and marketing techniques and education for both producers and consumers are Pathogen control in reuse of biogas plant slurry important preventive health strategies. The health problems associated with biogas plants come entirely from the reuse of the slurry because the gas production itself has no health implications (that is, Reuse for Biogas Production unless the digesters explode or the gas starts a fire). Average retention times in biogas plants are commonly When organic wastes are digested anaerobically, a short (5-30 days), and the operation is usually mixture of methane, carbon dioxide, and other gases is continuous, rather than batch. Pathogen removal will given off. This gas has become known as "biogas" and therefore be considerably less effective than in can be produced in various quantities by different conventional sludge digestion processes."0 Protozoal technologies. In conventional sewage treatment works, cysts should not survive, but pathogenic viruses, anaerobic sludge digestion produces biogas that is bacteria, and helminth eggs may be expected to be sometimes used to heat the digesters or for some of the present in the effluent slurry in considerable con- other energy needs of the works. Biogas production centrations. usually refers to the production of methane on a small There is little information from the field on the scale by individual farmers, communes, or rural quality of effluent from biogas plants. Data from China institutions in hot climates. (McGarry and Stainforth 1978) indicate an average of 15,000 helminth eggs, 4 hookworm eggs and 8 x 107 E. Technical description coli per liter of biogas-plant effluent. In the same report the authors found that survival times for Salmonella, Biogas digesters have been installed in large Shigella, spirochetes, schistosome eggs, and hookworm numbers in China, and it is probably there that the eggs in the anaerobic environment of the biogas tank technology has become most developed (McGarry and are up to 44 days, 30 hours, 30 hours, 40 days, and 75 Stainforth 1978) (see figure 7-t1). Significant numbers days, respectively. Therefore, for a plant with a also operate in India, Korea, and Taiwan. The biogas retention time of 10-30 days, it can be expected that plants are fed with diluted animal feces, with or without salmonellae, schistosomes, and hookworms will be in human excreta and with or without vegetable refuse. the effluent, but that shigellae or spirochetes will not. The effluent slurry is reused in agriculture9 and can Ascaris eggs will survive considerably longer than also be used to enrich fishponds; the biogas is used hookworm eggs and therefore will also be present. (It is primarily for domestic cooking and lighting. The dung likely that the major proportion of the 15,000 helminth from one medium-size cow or similar animal may eggs per liter reported in the study mentioned above produce around 500 liters of gas daily, and the calorific were Ascaris.) In another investigation in China value of this gas may be around 4-5 kilocalories per (Research Institute of Military Medical Sciences 1977), liter (McGarry 1977). In contrast, human excreta only inflow to a biogas plant contained 5.4 x 106 E. coli per produce 30 liters of biogas per person daily. The liter, whereas the outflow contained 1.4 x 104 (a 99.7 process is very sensitive to temperature. In the percent reduction). Shigellaflexneri, kept in conditions mesophilic range, optimum gas production occurs at simulating those of a biogas tank, survived for up to 13 around 35°C, but in rural applications digesters are not days, thus contradicting the study reported above. It is clear from the data above that the effluent slurry 8. Inadditiontothetwodesignsofbiogasunitsshowninfigure7- from a biogas plant is unlikely to be significantly less 1, the reader will find further details of the technology in Barnett, pathogenic than raw sludge. Its direct reuse on crops is Pyle and Subramanian (1978); Freeman and Pyle (1977); McGarry therefore not advised (see "Reuse in Agriculture," (1977); McGarry and Stainforth (1978); Rybczynski, Polprasert and above). It may, however, be reused in agriculture McGarry (1978); Subramanian (1977); and Van Buren (1979). following prolonged drying (>1 year) or after 9. It is reported from China that biogas slurry increases the yields of corn and wheat by 19 percent and of vegetables by 50-60 percent 10. See the previous chapter, the section "Conventional Sewage (Research Institute of Military Medical Sciences 1977). Treatment" and figures 6-5 and 6-6. 108 HEALTH HAZARDS OF EXCRETA 2.000 1.000 Gas Cylinder made of welded iron sheet Polyvinyl chloride pipe inlet Used sump oil Liquor outlet pipe Digesting Settling waste tank 2 Concrete or brick wAalls ; Concrete slab South Pacific design Slurry Gas draw-off pipe Displaced liquid Connected settlement \ storage area opening area Ground r > - > c ~~~~~~~~~~~~~~~~~~~~~~~~~ ~~level * . :*. 4 *.d A.\44, '*@4. c .o Gas storage area Liquid level v . .. ~~~~~~~~~~~~~~~~~~~~~Slurrv outlet Exceeta inlet .chamber chamber ._ Digesting / Groove for drop board Chinese design Figure 7-1. Tvpiccd bio gas digesters (dimensions in millimeters). From Kalbermatten and others (1982): top, from a design by G. L. Chan EXCRETA REUSE AND EFFLUENT DISCHARGE 109 composting (see chapter 5; the area of land required for chapters 2 and 3). Poor and seasonally arid countries prolonged drying will be so great that composting will are especially at risk from rivcr or lake pollution of this generally be the preferred treatment method). Biogas kind for two reasons. First, the waterside dwellers may plant effluent may also be used to enrich fishponds. have no alternative, potable water supply and therefore Clonorchis sinensis eggs will be eliminated in the plant, may be compelled to use the polluted water. Second, at and the health hazard involved is the passive some period of the year river flow may be low or transmission of other pathogens by harvested fish (see nonexistent, so that the discharged effluent will receive "Reuse in Aquaculture," above). little or no dilution. These factors make it essential to guard against substantial pathogen pollution of lakes and rivers. Discharge of Effluents HELMINTHS WITH AQUATIC INTERMEDIATE HOSTS. This chapter began with an expression of the view The excreted helminths that require one or more that sewage effluent, sludge, and night soil are intermediate aquatic hosts are: Clonorchis sinensis, important natural resources to be reused if possible. Diphyllobothrium latutm1, Fasciola hepatica, Fasciolopsis There will be occasions, however, when the most buski, Gastrodiscoides hominis, Heterophyes heter- economically or environmentally appropriate solution opliyes, Metagonirnus vokogawai, Paragonimnus wester- to disposal is not reuse but the discharge of wastes to mani, and Schistosoma spp.11 rivers, lakes, the sea, or groundwater. The health Fasciola is primarily a parasite of cattle and sheep implications of each of these alternatives are discussed and is present in wet pastures and small streams. in this section. Fasciolopsis and Gastrodiscoides are associated with the cultivation and ingestion of water plants (see Into rivers and lakes "Reuse in Aquaculture," above). Heterophyes and Metagonimnus are of limited public health importance The survival of pathogens in freshwater has been and have a very restricted geographical distribution. It examined in chapter 4. Survival times are considerable is thus Clonorchis, Diphyllobothrium, Paragonimus, and for all groups of organisms, and they increase in the Schistosoma infections that are associated primarily following order: protozoa, bacteria, viruses, and with discharge of effluents to rivers and lakes. helminths. Moreover, pathogens may travel sub- Clonorchis sinensis-and the related helminth stantial distances after being discharged into fresh- species Opisthorchis felineus and 0. viuerrini-are water. Pathogens discharged into rivers and lakes may transmitted from human (or dog or cat or other fish- contaminate fish in the same way described for marine eating mammal) to snail to fish to human, and they are discharge (below). Where discharge is to a river, particularly associated with fish farming in ponds pathogens may be carried to its mouth, where they may enriched with excreta. Diphyllobothrium latumn is infect shellfish. transmitted from human (or dog or bear or other fish- eating mammal) to copepod (minute crustacean) to HEALTH ISSUES. There are two overriding health fish to human. It is especially prevalent in lakeside problems associated with discharge of effluents into areas of temperate countries. Paragonimus westermani rivers or lakes: pathogens may be ingested by is transmitted from human (or many other animals) to waterside human populations who use the river or snail to crab or crayfish to human. These three lakewater for domestic purposes; and discharge to parasites all maybe controlled by preventing untreated freshwater may promote the transmission of those human excreta from reaching bodies of water where the parasitic worms that have aquatic intermediate hosts. intermediate hosts are found and by persuading affected communities not to eat undercooked fish, WATERBORNE PATHOGENS. People who use a crabs, or crayfish. In the case of Clonorchis and polluted river or lake for their drinking water may Paragoniimus, asexual multiplication takes place in the become infected by pathogens that have previously snail, so that one viable miracidium infecting a snail been discharged into their water supplies. Viral, can ultimately infect many fish or crabs and, thus, bacterial, and protozoal pathogens may all be transmitted in this way-although, where these Ii. A full account of the life cycles and distribution of these infections are endemic in the community, the par.asitic worms, and guidance on the treatment processes req uired to magnitude of this waterborne transmission may be remove eggs from sewage, sludge, or night soil, will be found in Part minor compared with other, more direct routes (see Two. 110 HEALTH HAZARDS OF EXCRETA many people. The discharge of the parasite eggs in the their survival in freshwater.'2 Excreted viruses and effluent must accordingly be cut to extremely low levels bacteria are eliminated very much faster in warm if transmission is to be reduced significantly. In all seawater than in cool seawater. Protozoal cysts and cases, animals other than man act as definitive hosts, helminth eggs do not experience any particular lethal and the management of human excreta alone can never effects in seawater, and their survival is similar to that guarantee the cessation of transmission. But keeping in freshwater (table 4-3). They do tend to settle, all untreated human wastes out of rivers and lakes however, and so present little health hazard. should have a dramatic effect on transmission in most endemic areas. SEAFOOD CONTAMINATION. Fish and shellfish in Schistosome worms are transmitted from human to polluted seawater may be contaminated by human snail and directly to humans through the skin. The excreted viruses and bacteria. The spread of patho- discharge of inadeqately treated wastes to rivers and genic pollution for more than a few kilometers from lakes is a major factor in the transmission of these sewage outfalls is not normally reported, and fish important parasites. Adequate treatment of all wastes caught in the open sea are thereforefound to harbor no before discharge should be helpful in the control of the human pathogens. Fish caught in the littoral zone, fecal species (S. mansoni and S. japonicum). Waste however, may well have excreted viruses and bacteria treatment will have less effect on S. haematobium, on their body surfaces and in their intestines, a hazard whose eggs are passed in the urine, because people may examined in the subsection "Fish farming," above. freely urinate near water. Once again, multiplication Excreted viruses and bacteria may survive in fish guts takes place in the snail, so that a great reduction in the for a few weeks and can infect humans who handle or number of viable eggs reaching the water is necessary eat them, and may also infect animals fed on fishmeal, before a marked reduction in transmission can be which may in turn infect humans. However, a more expected. common hazard is the contamination of fish after they are caught, and most fish-associated outbreaks of salmonellosis or typhoid have been linked to this form Into the sea of contamination. A more serious problem than fish contamination is Night soil and raw sludge are often taken out to the the contamination of edible shellfish (Hughes, Merson open sea by boat and dumped; less commonly, these and Gangarosa 1977). Mussels and oysters are grown wastes are dumped from the shore. Dumping of night along coasts and in estuaries where the salt soil or sludge in the open sea should pose no significant concentration is 0.8-3 percent (compared with 3.5 health problems, but dumping from the shore is so percent in the sea). Shellfish therefore live in the marine offensive that it should never be a feature of any well- environment most exposed to pollution from sewage designed disposal system. Only the more usual practice outfalls and from contaminated riverwater. Because of discharging effluents from sewage treatment they filter water to feed, shellfish concentrate excreted facilities into the sea near the shore is discussed below. bacteria and viruses in their tissues. Salmonella spp. (including S. typhi) and enteroviruses have frequently HEALTH ISSUES. The discharge of sewage effluent been isolated from shellfish at concentrations well into coastal waters can create two kinds of health above those of surrounding seawater (see chapters 15 problem: the risk of contaminating fish or shellfish, and 9). Outbreaks of poliomyelitis, hepatitis A, and which may subsequently be eaten, and the risk of diarrheal diseases all have been associated with the contaminating bathing areas and beaches. ingestion of of shellfish originating in polluted water. Shellfish can be decontaminated by placing them in PATHOGEN SURVIVAL. Enteric viruses and bacteria clean water. Chlorinated water that has been discharged into seawater survive for considerably dechlorinated is often used (chlorinated water is shorter periods than they do in freshwater. Coliforms ineffective because it discourages the shellfish from in seawater undergo a 90 percent reduction in 0.6-8 hours compared with 20-100 hours in freshwater. 12. The survival of indicator bacteria, salmonellae, and en- Fecal streptococci may survive a little longer than teroviruses in seawater are reviewed in chapters 13, 15, and 9, coliforms in seawater, and salmonellae longer still. respectively. Rapid bacterial death rates may be due to the injury of bacterial cells by seawater, such that they cannot grow on standard Enteroviruses survive for longer periods in seawater laboratory isolation media, rather than to actual death (Dawe and than excreted bacteria-90 percent reductions in Penrose 1978). These injured bacteria can be resuscitated by special 15-70 hours-but this is stillconsiderably shorter than techniques, but it is not known whether they are still infective. EXCRETA REUSE AND EFFLUENT DISCHARGE l1l pumping and feeding and so will not flush out viruses and nonswimmers at polluted beaches. The recorded or bacteria lodged in their tissues). Studies reviewed in risks of swimming in seawater containing 102t -0I fecal chapters 9,13, and 15 indicate that 2 days in disinfected coliforms per 100 milliliters were an additional attack water may be sufficient to cleanse shellfish of E. coli, but rate of one to two cases of gastrointestinal illness per that several days are required for elimination of 100 people in the 8-10 days following the visit to the enteroviruses and several weeks for elimination of beach. It must be kept in mind, however, that especially salmonellae. Even small numbers of pathogenic in developing countries the infections that may be bacteria remaining in the shellfish tissues may transmitted to swimmers at polluted beaches will subsequently multiply in warm conditions and infect usually be highly endemic in the community at large someone eating inadequately cooked shellfish. (the community producing the wastes that are A related problem is that of acute gastroenteritis polluting the sea), and swimming may constitute a caused by Vibrio parahaemolyticus. V parahaemolyticus negligible additional risk. Set against this is the has been reported as a cause of acute diarrhea in possibility that swimmers from high socioeconomic several countries, and it may be the single most strata (who experience a low risk at home owing to common cause of food poisoning in Japan (Miwatani adequate water supply, sanitation, and hygiene) may and Takeda 1976). The bacterium occurs widely in be exposed to a substantially increased risk of infection nature and is not restricted to the animal intestine. It is when they bathe in seawater polluted by the wastes of a halophile and has frequently been isolated from all socioeconomic strata. The same level of additional seawater, estuarine water, brackish lagoon water, risk may apply to tourists-who are usually either marine sediments, fish, shellfish, crabs, and prawns local residents from upper socioeconomic groups or (Baross, Liston and Morita 1978; De and others 1977; foreign visitors. A perceived risk to tourists, whether it Felsenfeld and Cabirac t977; Franca and others 1980; is real or imaginary, may have serious economic Sirca and others 1979; van den Broek, Mossel and consequences. Eggenkamp 1979; and Vanderzant and Nickelson 1973). Outbreaks of V parahaemolyticus diarrhea in humans have usually been associated with the To groundwater ingestion of inadequately cooked seafood, and the organism may also be a pathogen of marine fish and Effluents and liquid wastes are frequently discharged shellfish. It remains unclear to what degree disease to groundwater. This usually occurs unintentionally- outbreaks are associated with V parahaemolyticus when soakaway effluent or pit latrine seepage deriving from sewage discharges into estuaries and percolates down to reach the water table, for instance. coastal waters, rather than to naturally occurring It can also occur through seepage losses from the base aquatic reservoirs of V parahaemolyticus. In this of waste stabilization ponds or, in arid areas, when connection it is noteworthy that pathogenicity in effluents are discharged into low- or no-flow streams humans is particularly associated with those strains of that are losing flow to the ground. In some countries in V parahaemolyticus which produce a thermostable which groundwater resources are being deliberately hemolysin (the Kanagawa phenomenon). Yet, in conserved or augmented, treated effluents may be studies in the Andaman Islands (Lall and others 1979), recharged to groundwater as a means of indirect Britain (Ayres and Barrow 1978), India (Chatterjee recycling. [See note on page 116.] and others 1978; De and others 1977; Natarajan, Abraham, and Nair 1980), and Togo (Bockemuihl and HEALTH ISSUES. There are two central questions in Triemer 1974), from 89 to 100 percent of en- considering the health implications of waste discharge vironmental isolates were Kanagawa negative. to groundwater: how far do the pathogens move vertically and horizontally from the point of discharge, RECREATIONAL HAZARDS. An active debate con- and for how long are they able to survive? The tinues about the magnitude of the health risk movement of protozoan cysts and helminth eggs can be associated with swimming in fecally polluted seawater expected to be limited because their size will cause and the correct approach to water quality standards them to be retained in soil. It is therefore viral and and legislation (Cabelli 1979; Evison and Tosti 1980; bacterial movement and survival that are of interest, Moore, Perin and Maiden 1979). Recent evidence from and inadequately treated groundwater is a major Egypt and the USA (Cabelli 1979; Cabelli and others cause of outbreaks of diarrhea (both viral and 1979) revealed a small but measurable difference in the bacterial) and hepatitis A in some countries (Craun incidence of gastrointestinal illness between swimmers 1979). 112 HEALTH HAZARDS OF EXCRETA PATHOGEN TRAVEL. Studies on bacterial movement Nitrates from effluents through soil and rock indicate normal maximum travel This study concerns health problems related to distances of up to 30 meters in sand and fine soils and biological agents contained in excreta. It would be up to several hundred meters in gravel or fractured rock inappropriate, however, not to mention one chemical (see chapter 13). Despite their tendency to become pollution problem, the problem of nitrate accumu- adsorbed onto soil particles, viruses may travel lation, which can occur as a result of waste discharge to through soil for longer distances than bacteria (see rivers lakes or groundwater. Nitrates are an end chapter 9). Retention does not necessarily imply rie,ls or oundater. Nate areaend , . ~~~~~product of the oxidation of many nitrogenous inactivation. It must be noted that, when moving compounds. Nitrate levels may be high in lakes and through soils, the great majority of bacteria and viruses are retained in the first meter and that only a groundwater receiving continuing discharge of raw or treated sewage or wastewaters leaching from pit small fraction is able to travel more than 10 meters. latrines, soakaways, or garbage dumps (Berwick 1979; Brooks and Cech 1979: Nicholson 1979; Schalscha PATHOGEN SURVIVAL. Excreted bacteria and viruses and others 1979). Domestic and industrial effluents are likely to survive for longer in groundwater than in may cause high nitrate levels in receiving rivers during surface water (table 4-3) because groundwater is periods of low rainfall when the rivers are providing cooler, not exposed to sunlight, and has less microbial inadequate dilution. High nitrate levels in surface and and biological activity. Bacterial survival in ground- groundwater may also derive from surface runoff water water may be up to 5 months, with most reduction that has picked up organic material and nitrates from taking place in the first few days. Fecal coliforms soil or agricultural fertilizers. survive longer than salmonellae and can multiply in the The reduction of nitrite and nitrate levels in presence of nutrients (for example, when effluent is wastewaters prior to discharge is normally achieved by reaching the groundwater; see chapters 13 and 15). the action of denitrifying bacteria under anaerobic Virus survival may be similar or somewhat longer (see conditions. Such a process may be included as a chapter 9). tertiary treatment stage in a sewage treatment plant (Anderson and Ibrahim 1978), but its expense and PATHOGEN CONTROL. In areas where there are sophistication makes it inappropriate in most circum- many pit latrines, soakawastabilization stances in developing countries. In hot climates, many pit latrines, soakaways, unlined denitrification sometimes occurs in secondary sedim- ponds, or a recharge system, there will always be a risk entation tanks that have become almost anaerobic. of pathogenic viruses and bacteria reaching ground- The consequent release of gas (N2 and N20) seriously water. In pit latrines, soakaways, and ponds the waste-s . oI pinterfae quiklyabecomes cogds the interferes with the settlement process within the tanks. waste-soil interface quickly becomes clogged with solids and thus more effectively retains these microorganisms. The risks to health occur wheni the HEALTH ISSUEs. Nitrate levels of over 100 milligrams contaminated groundwater is used as a source of per liter of NO3 have been associated with clinical drinking water. The pathogen content of polluted methemoglobinemia in bottle-fed infants (Winton, groundwater will, in general, be much lower than that Tardiff and McCabe 1971). The nitrates are reduced to of surface waters in the same area. Where untreated nitrites in the intestine and thence enter the water is being used for domestic purposes, there will bloodstream, where they oxidize hemoglobin to therefore be a lower risk from wells than from nearby methemoglobin. This molecule is unable to transport streams or ponds. Where water is chlorinated, the oxygen; thus if too great a proportion of methemo- bacterial pathogens will be effectively destroyed. globin is created, serious and sometimes fatal anoxia Special vigilance is required wherever dense and cyanosis may ensue. This condition is rare and populations use untreated wellwater as their only apparently restricted to infants (chiefly those under 3 domestic source and wherever there is widespread use months of age). Exposure to excessive nitrite may also of soakaways or pit latrines. If routine water quality cause methemoglobinemia in animals and fish (Raju monitoring demonstrates a significant pollution and Rao 1979). problem from groundwater, it is necessary to supply Methemoglobinemia is particularly associated with piped water of better quality or to change the excreta bottle-fed infants ingesting powdered milk formula disposal method in use. The former solution will in made up with high-nitrate water. However, Shuval and general be less costly and more practicable than the Gruener (1977) studied the liquid intake of 104 infants latter. (1-5 months old) in Israel and showed that "while EXCRETA REUSE AND EFFLUENT DISCHARGE 113 during the cool months 90 percent of the total liquid soil, it may be possible to prevent these occurrences. intake is made up of milk, as much as 50 percent can be Nitrates may, however, come from many other sources, in the form of tap water supplements during the hottest particularly agricultural runoff, and it may be more month." Thus, in hot climates, even young breast-fed practical to provide an affected community with piped infants may be exposed to a considerable intake of water of low nitrate content. There is currently no high-nitrate water. The same study detected raised simple and economic method of removing nitrate from levels of methemoglobin in bottle-fed infants whose drinking water (Adam 1980; Nicolson 1979), and so water supply contained 45-55 milligrams per liter of nitrate reduction is normally achieved by blending NO3 (the usual accepted standard for NO3 in drinking high-nitrate water with waters having lower nitrate water is <45 milligrams per liter of nitrate or 10 concentrations. milligrams per liter of nitrate-nitrogen). Several factors operating in hot climates and developing countries may have the effect of increasing the probability of an infant's developing methemoglo- Literature Cited binemia. These factors include high fluid intakes due to heat; the practice of boiling water of uncertain Adam, J. W. H. (1980). Health aspects of nitrate in drinking- microbiological quality, which increases the nitrate water and possible means of denitrification (literature concentration; and the high incidence of infant review). Water South Africa, 6, 79-84. diarrheal disease, malaria, and anemia, which may all Anderson, G. K. and Ibrahim, A. B. (1978). Treatment of act to compound any methemoglobinemia caused by high-nitrate wastewaters by plastic media anaerobic filters high-nitrate water. In addition, some antimalarial with particular reference to latex processing. Progress in drugs may induce an increased level of methemoglobin Water Technology, 10, 237-253. in the blood. Despite these theoretical dangers, and Ayres, P. A. and Barrow, G. I. (1978). The distribution of despite the fact that some communities in some 7iVibrio parahaemolyticus in British coastal waters: a report despit the fct tha somecommunties i some of a collaborative study 197 5-6. Journall of Hvgiene, 80, developing countries (for instance, Botswana, Senegal, 281 294. and Tanzania) habitually drink wellwater with several Barnett, A.. Pyle, L. and Subramanian, S. K. (1978). Biogas hundred milligrams per liter of nitrate, it remains Technology in the Third Wtorld: A Multidisciplinar vReview. undemonstrated that any significant amount of Publication IDRC-103e. Ottawa: International morbidity or mortality results. Development Research Centre. High nitrate intake (from drinking water or food) Baross, J. A., Liston, J. and Morita, R. Y. (1978). Incidence of has also been implicated in adult stomach cancers in Vibrio parahoeniolyticus bacteriophages and other Vibrio Chile, Colombia, England, Japan and elsewhere bacteriophages in marine samples. AppliedI and (Cuello and others 1976; Drasar and Hill 1974; Environmentul Microbiology, 36, 492-499. Haenszel and others 1976; Hill, Hawksworth and Benarde, M. A. (1973). Land disposal and sewage effluent: Tattersall 1973). It is hypothesized that nitrite appraisal of health effects of pathogenic organisms. Journal of the Americant Water Works Association, 65, (produced by the bacterial reduction of mgested 432-440. nitrate), secondary amines, and bacteria may come Berwick, M. (1979). Nitrate levels in groundwater from the together in the stomach of individuals with gastric Fleuve, Senegal. Progress in Water Technology, 11, achlorhydria (reduced stomach acidity), or in the 117-120. bladder ofindividuals (especially females) with bladder Bockemuhl, J. and Triemer, A. (1974). Ecology and infection, to produce dimethylnitrosamine-a potent epidemiology of Vibrio parahaemolYticus on the coast of carcinogen of the stomach. The health hazards Togo. Bulletini oJ the World Health OrganiZation, 51, associated with high nitrate ingestion have been 353-360. reviewed more fully elsewhere (Fraser and Chilvers Brooks. D. and Cech, L. (1979). Nitrates and bacterial 1981; National Academy of Sciences 1978). distribution in rural domestic water supplies. Water Research, 13, 33-41. NITRATECONTROL These roblemsmay be Brown. L. D. and Dorn, C. R. (1977). Fish, shellfish, and NITRATE CONTROL. These problems may be human health. Journaii of Food Protectionz, 40, 712-717. countered by surveillance of drinking water sources to Bryan, F. L. (1977). Diseases transmitted by foods identify the communities at risk. In any one country, contaminated by wastewater. Journal of Food Protectiont. communities affected by highly nitrate-contaminated 40, 45-56. water will probably be small in number and restricted Burge. W. D. and Marsh, V. B. (1978) Infectious disease in geographical distribution. If the nitrate problem hazards of landspreading sewage wastes. Journzal oj derives from discharges or seepages of sewage or night Environmental Quality, 7, 1-9. 114 HEALTH HAZARDS OF EXCRETA Cabelli, V. J. (1979). Evaluation of recreational water quality, waters. Journal of the American Medical Association, 244, the EPA approach. In Biological Indicators of Water 587-588. Quality. eds. James, A. and Evison, L. pp. 14/1-13/23. Fraser, P. and Chilvers, C. (1981). Health aspects ofnitratein Chichester: John Wiley. drinking water. Science of the Total Enuironmnent, 18, Cabelli, V. J., Dufour, A. P., Levin, M. A., McCabe, L. J. and 103-116. Haberman, P. W. (1979). Relationship of microbial Freeman, C. and Pyle, L. (1977). Methane Generation by indicators to health effects at marine bathing beaches. Anaerobic Fermentation: An Annotated B.l ,.':, American Journal of Public Health, 69. 690-696. London: Intermediate Technology Development Group. Chatterjee, B. D., De, P. K., Hati, A. K. and Tandon, N. Gerba, C. P., Wallis, C. and Melnick. J. L. (1975). Fate of (t978). Fly-borne Vibrio parahaemolyticus in Calcutta. wastewater bacteria and viruses in soil. Journal of the Tropical and Geographical Medicine, 30, 499-503. Irrigation and Drainage Division. American Society of Civil Cohen, J., Schwartz, T., Klasmer, R., Pridan, D., Ghalayini, Engineers, 101, 157-174. H. and Davies, A. M. (1971). Epidemiological aspects of Goldberg, S. D. (1979). Domestic Wastewater Reuse for cholera El Tor outbreak in a non-endemic area. Lancet, 2, Agriculture. Opportunities and Methods. A Primer. Public 86-89. Utility Notes 51-T. Washington D. C.: The World Bank, Cornwall, D. A., Zoltek, J., Patrinely, C. D., des Furman, T. Transportation. Water and Telecommunications and Kim, J. I. ( 1977). Nutrient removal by water hyacinth. Department. Journal of the Water Pollution Control Federation, 49, Greenberg, A. E. and Kupka, E. (1957). Tuberculosis 57-65. transmission by waste waters-a review. Sewage and Craun, G. F. (1979). Waterborne disease a status report Industrial Wastes, 29, 524-537. emphasizing outbreaks in ground-water systems. Ground Haenszel, W., Kurihara, M., Locke, F. B., Shimuzu, K. and Water, 17, 183-191. Segi, M. (1976). Stomach cancer in Japan. Journal of the Crook, J. (1978). Health aspects of water reuse in California. National Cancer Institute, 56, 265-274. Journal of the Environmental Engineering Division, Heukelekian, H. and Albanese, M. (1956). Enumeration and American Society oJ Civil Engineers, 104, 601-616. survival of human tubercle bacilli in polluted waters. 11. Cuello, C., Correa, P., Haenszel, W., Gordillo, G., Brown, C., Effect of sewage treatment and natural purification. Archer, M. and Tannenbaum, S. (1976). Gastric cancer in Sewage and Industrial Wastes, 28, 1094-1102. Colombia. 1. Cancer risk and suspect environmental Hickey, J. L. S. and Reist, P. C. (1975). Health significance of agents. Journal of the National Cancer Institute, 57, airborne microorganisms from wastewater treatment 1015-1020. processes. Part 1. Summary of results. Journal of the Water Dawe, L. L. and Penrose, W. R. (1978). "Bactericidal" Pollution Control Federation, 47, 2741-2757. property of seawater: death or debilitation? Applied and Hill, M. J., Hawksworth, G. and Tattersall, G. (1973). Environmental Microbiology, 35, 829-833. Bacteria, nitrosamines and cancer of the stomach. British De, S. P., Banerjee, M., Deb, B. C., Sengupta, P. G., Sil, J., Journal of Cancer, 28, 562-567. Sircar, B. K., Sen, D., Ghosh, A. and Pal, S. C. (1977). Hughes, J. M., Merson, M. H. and Gangarosa E. J. (1977). Distribution of vibrios in Calcutta environment with The safety of eating shellfish. Journal of the American particular reference to V parahaemolyticus. Indian Journal Mledical Association, 237, 1980-1981. of Mtedical Researchi, 65, 21-28. Jensen, K. E. (1954). Presence and destruction of tubercle Dinges, R. (1978a). Aquatic vegetation and water pollution bacilli in sewage. Bulletin of the World Health Organization, control: public health implications. American Journal of 10, 171-179. Public Health, 68, 1202-1205. Kalbermatten, J. M., Julius, D. S., Gunnerson. C. G. and (1978b). Upgrading stabilization pond effluent by Mara, D. D. (1982). Appropriate Sanitation Alternatives. A water hyacinth culture. Journal of the Water Pollution Planning and Design Manual. World Bank Studies in Control Federation, 50, 833-845. Water Supply and Sanitation 2. Baltimore, Md.: Johns Drasar, B. S. and Hill, M. J. (1974). Human Intestinal Flora. Hopkins University Press. London: Academic Press. Katzenelson, E., Buium, I. and Shuval, H. 1. (1976). Risk of Engelbrecht, R. S. (1978). Microbial hazards associated with communicable disease infection associated with waste- the land application of wastewater and sludge. Public water irrigation in agricultural settlements. Science, 194, Health Engineer, 6, 219-226 and 264. 944-946. Evison, L. and Tosti, E. (1980). Bathing water quality in the Lall, R., Sen, D., Saha, M. R., Bose, A. K., De, S. P., North Sea and the Mediterranean. Marine Pollution Palchowdhury, N. C. and Pal, S. C. (1979). Prevalence of Bulletin, 11, 72-75. Vibrio parahaemolyticus in Port Blair. Indian Journal of Felsenfeld, 0. and Cabirac, H. B. (1977). A study of the Medical Research, 69, 217-221. ecology of Vibrio parahaemolyticus and V alginolyticus in Lee, B. Y., Lee, K. W., McGarry, M. G. and Graham, M. southeast Louisiana with special consideration of seafood (1980). Wastewater Treatment and Resource Recovery. consumption. Journal of Applied Nutrition, 29, 17-23. Publication IDRC-154e. Ottawa: International Franca, S. M. C., Gibbs, D. L., Samuels, P. and Johnson, W. Development Research Centre. D. (1980). Vibrio parahaemolyticus in Brazilian coastal McGarry, M. G. (1971). Water reclamation and protein EXCRETA REUSE AND EFFLUENT DISCHARGE 115 production through sewage treatment. In Water Supply Raju, T. N. and Rao, J. V. R. (1979). Nitrite induced and Wastewater Disposal in Developing Countries: methaemoglobinaemia in cat fish Clarias batrachus (Linn). Proceedings of a Water Supply and Sanitation Seminar, Indian Journal of Environmental Health, 21, 79-81. Bangkok, 19-23 January. 1970, eds. Pescod, M. B. and Research Institute of Military Medical Sciences (1977). Okun, D. A. Bangkok: Asian Institute of Technology. Nightsoil digestion for bacteria destruction. Chinese (1977). Domestic wastes as an economic resource: Medical Journal, 3. 361-363. biogas and fish culture. In Water, Wastes and Health in Hot Rudolfs, W., Falk, L. L. and Ragotzkie, R. A. (1950). ( fi-i tu,, eds. Feachem, R. G. A., McGarry, M. G. and Literature review on the occurrence and survival of enteric, Mara, D. D. London: John Wiley. pathogenic and relative organisms in soil, water, sewage McGarry, M. G. and Stainforth, J. (1978). Compost, and sludges, and on vegetation. 1. Bacterial and virus Fertilizer, and Biogas Production fr0om Human and Farm diseases. Sewage and Industrial Wastes, 22, 1261-1281. Wastes in the People's Republic of China. Ottawa: (1951a). Contamination of vegetables grown in International Development Research Centre. polluted soil. 1. Bacterial contamination. Sewage and Maddock, E. C. G. (1933). Studies on the survival time of the Industrial Wastes, 23, 253-268. bovine tubercle bacillus in soil, soil and dung, in dung and (1951b). Contamination of vegetables grown in on grass, with experiments on the preliminary treatment of polluted soil. 11. Field and laboratory studies on Entamoeba infected organic matter and the cultivation of the cysts. Sewage and Industrial Wastes, 23, 478-485. organism. Journal of Hygiene, 33, 103-117. (1951c). Contamination of vegetables grown in Miwatani, T. and Takeda, Y. (1976). Vibrio parahaemolyticus. polluted soil. III. Field studies on Ascaris eggs. Sewage and .4 Causative Bacterium of Food Poisoning. Tokyo: Saikon. Industrial Wastes, 23, 656-660. Moore, J. L., Perin, D. E. and Maiden, B. G. (1979). (1951d). Contamination of vegetables grown in Estimating the effect of water quality improvement on polluted soil. IV. Bacterial decontamination. Sewage and public swimming. Water Resources Research. 15, Industrial Wastes, 23, 739-753. 1323-1328. _ (1951e) Contamination of vegetables grown in Muthuswamy, S., Jamrud Basha, C., Govindan. V. S. and polluted soil. V. Helminthic decontamination. Sewage and Sundaresan, B. B. (1978). Fish polyculture in sewage Industrial Wastes, 23, 853-860. effluent ponds. IndianJouirnal ofEnvironmental Health, 20, (1951f). Contamination of vegetables grown in 219-231. polluted soil. VI. Application of results. Sewage and Natarajan, R., Abraham, M. and Balakrish Nair, G. (1980). Industrial Wastes, 23, 992-1000. Distribution of Vibrio parahaemolyticus in Porto Novo Rybczynski, W., Polprasert, C. and McGarry, M. G. (1978). environment. Indian Journal of Medical Research, 71, Low-Cost Technology Optionsfor Sanitation: A State-of-the 679-687. Art Review and Annotated Bibliography. Publication National Academy of Sciences (1976). Making Aquatic IDRC-102e. Ottawa: International Development Weeds Usefuil: Some Perspectivesfor Developing Countries. Research Centre. Washington, D.C.: National Academy Press. Schalscha, E. B., Vergara, I., Schirado, T. and Morales, M. (1978). Nitrates: An Environmental Assessment. (1979). Nitrate movement in a Chilean agricultural area Washington, D.C.: National Academy Press, irrigated with untreated sewage water. Journal of Nicholson, N. J. (1979). A review of the nitrate problem. Environmental Quality, 8, 27-30. Chemistry and Industry, no. 6, 189-195. Shuval, H. I. (1977). Public health considerations in Oswald, W. J., Lee, E. W., Adan, B. and Yao, K. H. (1978). wastewater and excreta re-use for agriculture. In Water, New wastewater treatment method yields a harvest of Wastes and Health in Hot Climates, eds. Feachem, R. G. A., saleable algae. World Health Organization Chronicle, 32, McGarry, M. G. and Mara, D. D., pp. 365-381. London: 348-350. John Wiley. Pahren, H. and Jakubowski, W., eds. (1980). Wastewater Shuval, H. I. and Fattal, B. (1980). Epidemiological study of Aerosols and Disease. Report EPA-600/9-80-028. wastewater irrigation in kibbutzim in Israel. In Wastewater Cincinnati, Ohio: US Environmental Protection Agency. Aerosols and Disease. Report EPA-600/9-80-028. Eds. Pahren, H. R., Lucas, J. B., Ryan, J. A. and Dotson, G. K. Pahren, H. and Jakubowski. W. pp. 228-238. Cincinnati, (1979). Health risks associated with land application of Ohio: US Environmental Protection Agency. municipal sludge. Journal of the Water Pollution Control Shuval, H. I. and Gruener, N. (1977). Health Effects of Federation, 51, 2588-2599. Nitrates in Water. Report no. EPA-600/1-77-030. Petrik,M. (1954). Utilizationofnightsoil,sewage,andsewage Cincinnati, Ohio: US Environmental Protection Agency. sludge in agriculture. Bulletin of the World Health Sircar, B. K., De, S. P., Sengupta, P. G.. Mondal, S.. Sen, D., Organization, 10, 207-228. Deb, B. C. and Pal, S. C. (1979). Studies on transmission of Pramer, D., Heukelekian, H. and Ragotzkie, R. A. (1950). V parahaemolyticus infection in Calcutta communities: a Survival of tubercle bacilli in various sewage treatment preliminary report. Indian Journal of Medical Research, processes. I: Development of a method for the quantitative 70, 898-907. recovery of mycobacteria from sewage. Public Health Sorber, C. A. and Guter, K. J. (1975). Health and hygiene Reports, 65, 851-859. aspects of spray irrigation. American Journal of Public 116 HEALTH HAZARDS OF EXCRETA Heealth. 65, 47-52. a7nd Waste Treatmlent, 11, 294-295. Sorber, C. A. and Sagik, B. P. (1978). Health effects of land Wert, F. S. and Henderson. U. B. (1978). Feed fish effluent application of wastewater and sludge: what are the risks? and reel in savings. Witer and 14a'astes Enginieerintg. 15, Wtiter nfid Sewage Works, 125, 82-84. 38-39 and 43-44. Standing Committee on the Disposal of Sewage Sludge Wiley, B. B. and Westerberg, S. C. (1969). Survival of human (1978). Senwage S., i, Dispossal Data aind Reriews of pathogensincomposted sewage .p pplied Microbiology, 18, Disposal to Sea. London: Department of the Environment 994-1001. and National Water Council. Wiley, J. S. (1962). Pathogen survival in composting Subramanian, S. K. (1977). Bio-Gas Systemns in Asia. New municipal wastes. Journal of the W1ater Poilution Cointiol Delhi: Management Development Institute. Federation. 34, 80-90. Sundaresan. B. B.. Muthuswamy, S. and Govindan, V. S. \, liii, R. S. and Hoy, W. A. (1930). The viability of B. (1978). A wastewater treatment and re-use demonstration, tutberculwosis (Boriiius) on pasture land, in stored faeces, and In Sainitation in Deceloping Couintries, ed. Pacey. A., pp. in liquid manure. Journal ot Hygiene. 30, 413-419. 208--210. Chichester: John Wiley. Winton. E. F.. Tardiff, R. G. and McCabe. L. J. (1971). Van Buren, A., ed. (1979). A Chinese Biogas Manual. Nitrate in drinking water. Jour-al of the American Wirter London: Intermediate Technology Publications. IWorks Association, 63, 95-98. Van den Broek, M. J. M., Mossel, D. A. A. and Eggenkamp. Wolverton, B. C. and McDonald, R. C. (1979). The water A. E. (1979). Occurrence of Vibrio parahuemolvticus in hyacinth: from prolific pest to potential provider. .4mbio, Dutch mussels. Applied antd Environmental Microbiology, 8, 2-9. 37, 438 442. WHO (1973). Reiuse ol nmethods of wvastewater Vanderzant. C. and Nickelson. R. (1973). Vibrio paca- treatment and health safeguards. Technical Report Series haemoltyticus: a problem in mariculture'? JouErntal ofl .Vilk no. 517. Geneva: World Health Organization. Ind Food Technology. 36, 135-139. Young, E. E. (1980). Costs of maintaining public health Viraraghavan. T. and Raman. A. (1967). Sewage treatment in standards tor spray irrigation of municipal waste water oxidation pond at T. B. sanitorium, Madras, India. Water systems. Journal of Enrironmental Q .,i. . 9, 354-358. Note added in proof Since this chapter was written a comprehensi- e hydrogeological review of groundw,ater pollution by excrcta andsewage has been published: Lewis. W. J.. Foster. S. S. and Drasar. B. S. (1982). Tlze Risk of Groundwater Pollution hby On-site Sanitrtion .in Developintg Cozintries. Duebendorf, Switzerland: International Reference Centre for Wastes Disposal. 8 The Human Element in Sanitation Systems DURING THE DISCUSSION of the possible health any sanitation intervention, but program designers benefits from improved sanitation (chapter 3) and the should ask themselves which changes are really specific, alternative technologies for excreta disposal practicable and, conversely, how far social, admini- (chapters 5-7), some rather demanding stipulations strative, or political factors should be viewed as about the social conditions under which maximum constraints on policy options. To do this requires that a benefits can be achieved have been made. Several planner have a good "feel" for a society and the way in beneficial effects can only be expected to occur, for which sanitation is handled within it. Two questions instance, if latrines are properly used and maintained. form the basis of the discussion in this chapter: how do Changes in the public's knowledge and practices may social values and understandings associated with be required before some systems are acceptable. Good health or defecation influence sanitation programs, maintenance of both the private and the public and what possibilities are there for controlling excreta components of sanitation systems is vital. That there disposal through the activities of households, com- are many calls for health education or more effective munity groups or urban government? The questions program administration is a clear indication that the are interrelated because understandings and values social prerequisites for effective sanitation are seldom influence institutions, and the consequences of achieved in practice. Yet the diagnosis of social ills has institutional behavior in turn influence individual often taken a simply deductive form: if a sanitation understandings and values. technology fails, the fault must lie with the users. The social, behavioral and institutional aspects of Careful analysis of these social factors may reveal that excreta disposal, and of programs designed to change sometimes the public's response cannot reasonably be excreta disposal practice, are severely neglected areas otherwise. of study. Very few good field studies or thorough A recurrent theme in this study has been that excreta project evaluations have been carried out. The writings disposal systems must be suited to their environmental of Curtis, Goyder, Kochar, and Streefland in Pacey conditions (the climate, endemic diseases, water (1978) are of interest, as are studies on the comfort availability, or civic wealth), many of which are clearly stations in Ibadan, Nigeria (Ademuwagun 1975 and beyond the control of public authorities. It is too often Pasteur 1979). Recent studies undertaken by the assumed, however, that society is within governmental World Bank have yielded insights into behavioral and control and that communities should simply change to institutional aspects of sanitation programs in Latin accommodate a technology that has been introduced. America (Elmendorf 1980) and in Africa (Feachem, The task is considerably more complex. Because of Mara and Iwugo 1980) and have led to a general review their low capital cost, several of the technologies that of current knowledge on these matters (Elmendorf and are appropriate for the urban or rural poor make heavy Buckles 1980). Some valuable work in this field has demands on the users (table 3-2). They may also levy been carried out not only by those investigating social considerable demands on the limited resources of aspects of sanitation programs, but also by those finance and trained manpower of the public bodies that investigating the social aspects of the transmission of have responsibilities for operation and maintenance. particular excreta-related pathogens. For instance, It is reasonable to hope for some social change from Dunn has written on the behavioral aspects of Note: The first draft of this chapter was prepared by Dr. Donald intestinal parasitism (Dunn 1972), Bancroftian and Curtis. Institute of Local Government Studies, University of Malayan filariases (Dunn 1976) and parasitic diseases Birmingham, England. in general (Dunn 1979), and Kochar (1978, 1979) has 117 118 HEALTH HAZARDS OF EXCRETA done outstanding work on hookworm transmission in of common ground-if not in interpretation, then at West Bengal. Other recent works of interest include a least in practice-between science and these other comprehensive literature review of community partici- beliefs. The ancient Israelites, for example, were pation and education (Van Wijk-Sijbesma 1979) and instructed to take a stick with them on their early contributions by Feachem (1980) and Jackson (1979). morning journeys from the camp to the bush, the stick to be used for burying their feces. This is an effective Relevance of Cultural Values and sanitary prescription in the modern sense, but it is clear Attitudes from the context that the instruction had more to do with the ritual cleanliness of warriors before battle than How people react to excreta disposal schemes or with disease transmission as such (Deuteronomy arrangements depends both upon deep-rooted cultural 23:12). values and upon more mundane matters of cost, Mary Douglas, seeking an explanation of the convenience, and comfort. Each of these may affect user universal existence of taboos, suggests that those things preference or acceptance, and each should be explored become taboo which are difficult to classify culturally in every project in which the acceptability of the (Douglas 1966). A corollary to this idea is that most technology is the least bit in doubt.' Resistance to new societies prefer to maintain a clear distinction between latrines, for example, might be due to inadequate door man and animal: man is the thinker, tool user, made in catches (a mundane factor, yet indicative of a the image of divinity, and so on, whereas animals are preference for individual privacy) or perhaps, for instinctive, confined to their creature strengths, and of Muslims, inadvertent and inappropriate orientation of a lower order of existence. But this distinction is the facilities in relation to Mecca (an objection difficult to maintain, particularly in relation to bodily implicating values and conventions; Goyder 1978). functions. Defecation and excreta are taboo because Cultural interpretations of excreta and defecation they reveal to man an aspect of his animal existence underlie people's responses both to the deposition that he would prefer to forget. This anthropological technologies and to removal and reuse processes. observation may have sufficiently widespead relevance Excreta usually have a rather special psychosocial to explain why man seeks privacy to defecate, status. In many societies excreta are only referred to in defecation is confined to the bush, and excreta are, if everyday speech with calculated disrespect for the possible, avoided. values of society. Excrement is a thing apart, despised, Interpretation aside, a number of fairly universal taboo. How deeply this view prevails varies: for some and deeply felt human reactions to the phenomenon of peoples, excrement is simply dirty, but for others it is defecation exist, all of which can be utilized to promote dangerous, a matter for personal defilement or for evil practices conducive to improved hygiene in the uses, to be scrupulously avoided or carefully disposed scientific sense of the word. Privacy, apartness, and dirt of (Curtis 1978). There are in fact many interpretations avoidance are all values that lend themselves to the use of the significance of excreta besides that of modern of modern excreta disposal technologies. Beyond these science, with its concern for the pathogens that excreta there are a range of widely shared values: smell contain. avoidance, household cleansing, sweeping, clothes These culturally relative interpretations are reflected washing, and so on that contribute to a reliable in the principles and practices of personal hygiene common basis for domestic sanitation programs. found around the world. Many hygienic practices have Effective excreta disposal may, of course, require that little to do with pathogen avoidance (for instance, the people come to have some new understandings of the doctoring of a house against witchcraft), and many health hazards from excreta and of the measures that substances that are of little interest to modern science can be taken to avoid these hazards. There will be some (such as fingernails or hair clippings) may be regarded situations in which traditional understanding and as dangerous. Yet in most cases there is a large element practice-for example, defecating into rivers that are 1. The study of community reaction to a proposed sanitation also water supplies-is strongly contraindicated by project, and the elicitation of support and acceptance, are valuable modern interpretations of health and disease. In these activities in all countries. Krauss (1979) described the replacement of instances, authorities may have to assume didactic a malfunctioning tertiary sewage treatment plant in Greenville, roles, but they can nearly always do so by building Maine, USA, by an innovative land application system after upon traditional culture rather than by starting from extensive public consultation and participation. An immediate scratch. practical outcome was an increased willingness to pay sewer rates on the part of households connected, and an increased demand for The widely shared cultural evaluations of excreta connections on the part of those households unconnected. have an equally common but regrettable side effect: THE HUMAN ELEMENT IN SANITATION 119 people who, by their occupation, come into regular appreciating the position of the user and looking at contact with excreta become themselves persons to be innovations from the user's point of view. For the user, avoided. In many towns throughout the world, the toilet itself is a most important element in the sweepers and night soil removers are drawn from excreta disposal system. He may have to decide disadvantaged minority groups living in segregated whether to invest in one, and he has daily to face using communities within the towns, and their occupation it. Even the most hygiene-conscious people will take tends only further to reinforce their segregation. This is more than cleanliness into account in making these a rather intractable problem wherever some kind of decisions, and disadvantages may not have to be great cartage system is necessary for night soil removal. before some people will opt out of whatever innovation is being proposed. Influence of Social Structure and Organization Cost The most obvious and perhaps most cogent of all Any excreta disposal system IS a complex social soilcntatsnsnttonsthcstfltre. activity involving planners, administrators, politicians, The existing on of sntr faltie(bt and corporation workers as well as the individual user. aThe existing dastributon of sanitary facilities (both Officials, for their part, can plan improved systems but tardothelrichdoiatlargeiexentybecauseaanitationei may face difficulties in raising the necessary resources, e ni. yo the altenatie techno is cooperating with other agencies, delivering the goods, discussed. int bo are heate sech and, crucially, building up routine services for maintenance. There are additional problems in cheaper) in capital terms than the sewerage systems of securing political support for low-income schemes the industrial West, but most of the savings occur in the cost to the public authority that is spared the expense of when upper-income groups, who can better afford to sees2Thcotftetilstemlvsaytllb pay and have more political weight, themselves clamor siderale ast omthe tolets themselves may still be for hiher sandard of srvice considerable, and at some point down the scale of for higher standards of service. Politicians face the full brunt of deciding priorities in poverty it ceases to be reasonable to expect people to urban development and, if they have to recruit public pay for their own installations. In many urban support to keep themselves in office, they often face environments sanitation programs must be seen as pressures to employ more sweepers or to favor attempts to overcome one of the multifarious effects of particular parts of the community. Workers, such as poverty; as such, they are bound to involve a degree of the operatives of cartage systems, will also have a government intervention through subsidies. Where excreta have an economic value, some of the disposal number of preoccupations besides service to the city. cotcabealndagisthexcednom They must secure for themselves a living wage and costs canre b talanced agaim st the expected income tolerable working conditions, and in their struggles with the authorities or with a public unwilling to see cartage than the in-house costs of toilet fitments. taxes increased they will use what sanctions they have at their disposal, chiefly the disruption of services. Convenience In short, whatever high ideals about the quality of The location of latrines is important and must human life may be embodied in sanitation programs, balance advantages. Sometimes a technology con- such programs cannot escape being a part of the strains the choice of location, but, assuming that all complex social system of a city, and any attempt to options are open, toilets may be sited inside the house make them work better has to take this complex system or compound or some distance away. People may be into account. The following sections exanmine these sensitive about such matters as the prominence of the social values and organizational issues in relation to toilet to public view, and such factors must be the deposition, transport, and reuse of excreta. evaluated in detail for each situation. Some general principles, however, may be postulated. Social and Behavioral Aspects of Latrine If the latrine is sited at some distance from the living Design quarters, people may be discouraged from using it on 2. See Kalbermatten, Julius and Gunnerson (1982) for an economic comparison of alternative sanitation technologies and for technical innovations because many factors enter into proposed "sanitation sequences" that enable users to improve their their choice. But much can be gained by the planner's sanitation facilities to a level and at a pace they can afford. 120 HEALTH HAZARDS OF EXCRETA dark nights or in inclement weather. Yet if it is close to are difficult to predict. There are the well-recognized the house, there may be a feeling that defecation is not cultural preferences for sitting or squatting (the latter adequately segregated from the rest of daily living. In a in part an act of avoidance of physical contact with new tenement project in Madras where toilets were possibly defiling surfaces), and there are also strong provided in each flat, housing officials found that some commitments to particular anal cleansing procedures of these were filled with sand and the space used for that must either be accommodated by the new other purposes. One explanation of this response is technology or, if necessary, changed. Additional design that defecation within these small apartments, even considerations are that children have anxieties about behind closed doors, was unacceptable to the cavernous holes in squatting plates, that the aged may occupants (Curtis 1978). have special needs (the surroundings must not be Sufficiently private locations for outside toilets may slippery, for example), and that hot and malodorous be difficult to find in urban environments. Draft plans latrines discourage all users. for an urban site and service scheme in Africa made A vital aid to comfort has been the inclusion of provision for the siting of latrines in the front corner of personal washing facilities in toilet installations, as in plots, where they could be conveniently linked to sewer the comfort station program in Ibadan, Nigeria lines along the roads. But there were considerable (Ademuwagun 1975; Pasteur 1979). Facilities for hand doubts as to whether this technical convenience would washing at the place of defecation are highly desirable be socially acceptable-the first thing to confront in any case, but total body washing in privacy could household visitors would be the toilet. A privy should also be much appreciated. In India, for example, be private. Most societies have conventions relating to customary sanitary prescriptions require a bath to domestic space-for example, that the back of the follow defecation (Kochar 1978); in these circum- house is private, the front public and these stances, linked bathing and toilet facilities would conventions need to be discovered and respected. greatly encourage use of both private and public People may be sensitive not only about the location latrines. Comfort concerns both physical conditions of the toilet but about the journey to it as well. In and the fulfillment of conventional expectations. Botswana it was found, through careful monitoring of Householders in B6tswana found the ventilation gap a latrine program, that the act of carrying a container left at the bottom of doors to their outside toilets of water to the new privy (something quite acceptable disconcerting because people could see their feet. in India) was an embarrassing announcement to the Conventional expectations may be numerous, and the world at large of an individual's intentions. The design only way to discover them is by carefully monitoring was subsequently modified to provide a water source at reactions to new designs in each situation. the latrine. In many rural areas latrine programs may face the A major difficulty with toilets may be providing problem that people find the bush more acceptable and access to the right people at the right time. more comfortable than pit latrines or even some more Householders may be inclined to keep outdoor latrines sophisticated teclnologies. This choice may reflect locked to prevent misuse by passers by, with the both that defecation is often regarded as a shameful unfortunate consequence that they are then not activity properly confined to the wilds [as Muhondwa available for children to use during the day. Similarly, (1976) found in Tanzania] and that the latrines may be in the tenement project in Madras, interior toilets were hot, malodorous, and fly ridden (an acknowledged inaccessible to children while both parents were out tendency of many pit latrines). The first problem seeking work during the day (Curtis 1978). Private decreases when the bush becomes inaccessible, as in toilets have to be carefully designed and located to town, or is so diminished that it constitutes highly secure both adequate access and adequate control. contaminated spinneys or copses in areas of intensive Counterbalancing these factors is the fact that most cultivation. At this point the population presumably toilets provide a degree of privacy such that the time of becomes susceptible to new interpretations of what day when defecation may conveniently take place is constitutes an appropriate environment for defecation. greatly extended from the dawn or dusk periods that Latrines can be presented as answers to the problem of are often favored by those with no facilities at all. privacy, and an analogy with the bush may be maintained by siting the facility at a suitable distance Comfort from the house. Crowded urban environments present opportunities for creating new conventions, practices, Comfort has been found to be a great selling point and concepts of comfort that program directors should for latrine programs, but again the social requirements seize upon. THE HUMAN ELEMENT IN SANITATION 121 Group or communal toilets and pays him from a communal fund or allocates Private, domestic latrines have so many advantages responsibility for cleaning and maintaining the to the user over any arrangements by which members separate toilets to each of the participating households. to te usr oer ay arangment by hlc memers The pilot scheme was monitored by a health education of different households share their facility that they are te who ideme seved blems educatin alwys refrabe wereerpeole an ffod tem nd team who identified several problems (Ademuwagun always preferable wherever people can afford them and 1975). Cleaners were often badly in arrears in their pay, space is available. High costs and problems of land an hr h ol hmsle neto ocr scarcity, however, may oblige authorities to select ' w p y communal facilities even though, from past experience, out cleaning and maintenance, the constant attention commnallaclltes een houn, rom asteXprleceX of the health education team seemed to be necessary if their success is highly problematical. The difficulty in tandards ere to be u A ceproble all cases is maintenance. Public toilets have a poor appeared to be paying for water and electricity, and in record in this respect and have inherent shortcomings. some cases supplies were withdrawn. This last problem It takes only one misuser, perhaps a child avoiding the . . frightening squatting hole, to establish a chain of rie quesio about h s d t ask betwee subsequent mius fo whc nooei .iln otk the public authority and the local groups. Voluntary r qesonsbii. . . groups often have difficulties in collecting money from responsibility. their members on a routine basis (Feachem and others There are two possible responses to the problem of 1978) because defaulters encourage those who would neglect of public facilities that public authorities can otherwise be inclined to pay regularly to be similarly make: attendance by a cleaner, or the provision of lax public toilets for identified or self-identified groups of In most cases public facilities must be provided households. The first is an expensive proposition either by public authorities or by these authorities in requiring the deployment of cleaning personnel on a conjunction with the users. Where night soil has a large scale. In general, arrangements of this sort are commercial value, however, there may be potential for common only in public places such as market areas or the commercial organization responsible for reuse to main thoroughfares, where provision must be made for provide the toilets themselves. In Indonesia fishpond large numbers of occasional users who are passers by. owners, who stand to make a profit from the The additional expense of an attendant is often covered cultivation of fish, provide a number of latrines by a small charge to the users, which of course is not overhanging their ponds for the use of the neigh- possible in toilets designed to serve the requirements of borhood. Whatever virtues or vices attend this system, a resident population. The arrangement most likely to the great advantage is that management and ensure sustained cleanliness is to have one cleaner . . a A chaper maintenance by a public authority IS minilmized constantly stationed at each public toilet. Abecause the fishpond owner has to maintain the alternative is to have a cleaner responsible for several facilities in a manner that is attractive to the requisite public toilets, which he continually travels among. This potential users. It is not clear, however, whether in latter option can work well if the cleaner has adequate other circumstances cartage systems, for instance water supply and equipment, so that he can cope with a it is possible to push contractors beyond servicing into toilet that has become grossly fouled since his last visit. providing the latrines. This system is used to maintain public toilets in Beijing, China: the cleaner has a three-wheeled bicycle, with equipment and boxes, and water is available at each Social and Organizational Aspects of facility (Feachem, personal observation). The potential for achieving better management of E C public toilets by associating them with an identifiable group of households is currently being explored in the It is perhaps regrettable that a sewerage system is not Ibadan comfort station program in Nigeria where, in only a technically efficient removal system (given the the old town, the indigenous social structure of family massive financial outlays to introduce it) but, once groups provides a framework for the social control of constructed, that it is also the easiest to organize and latrines (Pasteur 1979). The facilities, designed to serve run. The technology may in part be complex, but the between 350 and 700 people, are built by the need for servicing is limited. Instead of an army of authorities with the people themselves providing the sweepers required to empty buckets and pushcarts, a land from family holdings and contributing to the cost sewerage system may be run by white-coated of construction. The group, under the leadership of the technicians assisted by a few manual workers whose traditional family head, then either appoints a cleaner job is performed away from the public gaze, 122 HEALTH HAZARDS OF EXCRETA either underground or beyond the urban bounds. The regarded occupation, and that is being of low social labor force required is small, elite, and dispensable for status without any occupation at all. Thus, from a short periods. Breakdowns in a sewage system usually social as well as economic point of view, whether night cause environmental pollution at the treatment works soil cartage systems are appropriate or not depends on and beyond rather than any direct contamination or the state of the wider economy. If there are equally well- disruption of the domestic environment of the users. In paid or better jobs available, then it must be assumed other words, as is the case with many modern that night soil removers will select these, and there will technologies (Dickson 1974), a sewerage system is more be a strong argument for changing the disposal system. amenable to social control than any of the less If there are not otherjobs available, there will be strong automated technical alternatives. pressure from the disadvantaged groups themselves to By contrast, cartage in its simplest bucket-latrine maintain the cartage systems. form requires large numbers of workers carrying out If hand-operated cartage systems remain necessary, routine collection of night soil from households by something can be done to improve the social position using buckets, boxes, or barrows that must be emptied of the operator by improving the terms and conditions into carts of some sort for conveyance to a disposal of service. Low status frequently is reinforced by low point. The buckets have limited capacity, and the pay, which, if improved, would somewhat counteract system is prone to crises both from mismanagement low status. It may be difficult, however, to alter the pay and from collective action on the part of the workers. structure radically while there remains a reserve corps Civic authorities face on the one side citizens with of unemployed sweepers without simply encouraging various means at their disposal for insisting upon subcontracting. Government policy on public sector reasonable service; on the other, authorities face pay may also limit the options and create problems of workers who wish to exercise what strength they have its own. In some cases minimum wage legislation may to get a reasonable reward for performing an set the scale for manual labor in the public sector above unpleasant and socially degrading job. Which party market rates, causing labor-intensive technologies to gets the relative advantage depends upon the labor be uneconomic while there are still surplus workers market, politicians' need for political support, and willing to do the job. In other cases, as in Port Sudan, other factors; in any case, cartage systems often present Sudan (Spencer 1978), rates of pay set at levels not organizational and political problems for civic competitive with private sector employment make it authorities. If these authorities decide to change to difficult to build up and train adequate staff. But even if sewerage systems, the decision may reflect a desire to it is difficult to make major changes in pay, working escape from the organizational problems involved in conditions can be improved in other ways. Where work cartage. clothes are issued, they often are similar in appearance Direct handling of night soil in cartage systems leads to those of convicts and serve to set the users socially to a situation in which it is often only groups of apart more than to protect their bodies. Equipment is strangers, refugees, or other disadvantaged minorities also often poorly designed and badly maintained, and of the urban community who are prepared to take the facilities for washing and changing after work are job. In the Indian subcontinent the work is associated inadequate or neglected altogether. Improvement in with the sweeper castes, whose untouchable status the any of these dimensions will improve the social status Indian government has been endeavoring to overcome. of night soil removers. In practice this kind of social change has proved very Operators of vacuum trucks have a stronger difficult wherever there is continuing association of a bargaining position than workers in manual cartage caste or single group with occupations such as night systems because they are more skilled and, in any soil removal, and eliminating a stigmatized occupation one town, fewer in number. Sealed vaults, because they is a major additional incentive to changing an excreta have no treatment potential and limited capacity, also disposal system. But even stigmatized occupations have a crisis point if they are not emptied on time, and may be in strong demand if alternative sources of organized labor can use this to its advantage. Septic employment are unavailable. Operators in parts of tanks, in contrast, are less crisis prone and may for this cities covered by private cartage systems may have to reason be favored by authorities worried about the purchase the rights to service a street (Streefland 1978), power of their organized labor force to make demands. and municipalities are often under strong political Improved technologies, requiring less direct handl- pressure to expand the number of sweepers in their ing of feces, may facilitate an upgrading of the status of employ. For a sweeper there is perhaps only one thing night soil removers. Jobs with more skill will attract worse than being of low social status in a lowly higher pay, enabling the workers to maintain a higher THE HUMAN ELEMENT IN SANITATION 123 standard of living. One seemingly counterproductive conclusion brings experts into line with the large part effect herc is that, if the social stigma attached to night of mankind that has always favored reuse. In many soil removal is effectively lifted by improved tech- parts of the world the problem is not reuse but how to nology, these jobs may then be open and attractive to persuade people that additional stages of treatment are people outside the minority traditionally filling the sufficiently important for their health to warrant the occupation, so that this minority group loses its increased time and expense that treatment requires. employment monopoly while keeping its low social Elsewhere, however, the idea of reuse is not easily status. accepted culturally. Many people share the prejudice Because many towns will require improved cartage of the villagers in Zola's novel La Terre against the old systems of one kind or another in the future, it is lady who nurtured beautiful vegetables by night soil, important to discover whether the social stigma thus relieving her poverty but placing herself beyond attached to night soil removal can under any the bounds of social acceptance. However deep seated circumstances be removed. Evidence is hard to come these prejudices may be, the situation is far from by. Some reports from China (Streefland 1978) indicate irredeemable. There are several reasons why the that, because of the importance attached to health in significance of cultural barriers to reuse is less than it that society, the status of night soil removers has might first appear. Processing can transform some- improved since the revolution. In a society where reuse thing that is socially unacceptable into something that of excreta has always been practiced, however, it is is much more easily accepted. An analogy may be unlikely that the job has ever carried the stigma that it drawn to the universal practice of food preparation: an does, say, in India, where the rituals of excreta animal or vegetable, unattractive in the wild state, avoidance are highly developed. Furthermore, the becomes appetizing when cooked, arranged on a plate, Chinese approach of involving the public in hygiene and served with a sauce; so may excreta, despite their and sanitation improvement committees (Schwartz malodorous nature and value-laden associations, 1977), if tried elsewhere, would not necessarily become attractive when treated and moved to another lead to an improvement in the status of those people environment as compost or fertilizer. Part of the art of who are employed in night soil removal. As with treatment must be the achievement of this cultural attitudes towards excreta and waste disposal, the transformation that would enable farmers to use a willingness of a society to participate in an organized substance with pleasant texture and acceptable odor way in this sector is culturally dependant. This remains for the enrichment of their land. an important area for future investigation. Unlike the true subsistence farmer who experiences In many societies where night soil is valued as a the whole cycle of agriculture from production to fertiLizer, cartage is a private sector activity. Cartage consumption and back to production, a commercial contractors make their money by selling the material farmer produces for a distant and impersonal market to farmers, by being paid for the job of removal itself, or and is better prepared to use any agricultural aids by a combination of both. In some towns, different conducive to a good market return. The urban areas are serviced by small-scale contractors who make consumer, for his part, can only judge food by its agreements with individual householders for night soil appearance in the market stall and knows little of its removal. In others, larger-scale operatives undertake origins. The separation of producer and customer is contracts with city corporations. Some operate simple both geographical and institutional. Its positive aspect cartage systems, others may service septic tanks with is the diminished significance of individual preferences vacuum trucks. Private contractors may be difficult to and prejudices upon the production processes; its control, particularly where they are numerous and negative aspect is that the public must be protected stand to gain from dumping their loads in the nearest from unscrupulous or unhygienic practices through watercourse instead of removing them from the city to bureaucratically administered controls upon these agreed disposal points. A good price for the product, production and marketing processes. Thus, fish grown however, is an effective incentive to efficient night soil in oxidation ponds managed by city corporations removal. under controlled conditions can escape any stigma Social and Organizational Aspects of because, in the marketplace, they cannot be easily identified. In India, for example, produce grown in Excreta Reuse Systems sewage-irrigated fields enters the market unnoticed, It is now widely accepted among agricultural and although in parts of that country reuse of night soil is sanitation planners that reuse of wastes is a desirable not a favored practice. In London, England, on objective if it can be hygienically achieved. This December 23 and 24, housewives of slavonic extraction 124 HEALTH HAZARDS OF EXCRETA (mainly Poles) buy imported carp for their traditional vision of routine operations to the collection of dues Christmas Eve feast, little suspecting that some of these and the control of access to services. Experience past carp have been raised in sewage ponds. and present indicates that this management ability is Finally, at least in the West (and the West as a often the chief limiting factor in sanitation programs great consumer of natural resources is very important (Rybczynski, Polprasert and McGarry 1978). Not only in this respect), prejudices against reuse are being are urban services often inadequate in extent (to be counteracted by a new consciousness of a need to expected in rapidly growing cities), but existing achieve ecologically sound farming practices and systems also suffer from malpractices that add to their patterns of human existence. This takes the form both deficiency. Contractors dump night soil indiscrimi- of an awareness of the undesirability of polluting rivers nately in rivers or drains. Workers gain political and seaboards with untreated or inadequately treated protection when attempts are made to enforce work sewage and of the need to find substitutes for the routines. Members of the public get their houses energy-consuming (often petroleum-derived) artificial preferentially connected to water supplies or sewer fertilizers that are required in large volumes in lines by paying "speed money" to minor officials. The agriculture. This transformation of values, coinciding poor pay their dues while the rich avoid payment. as it does with the more structural changes described These difficulties are unlikely to occur if the public at above, has now proceeded to the point that constraints large is solidly behind the policies of their authorities upon effective reuse are more questions of cost and and can effectively exercise some influence upon the technical feasibility (particularly the problem of mixing course of events. It is noteworthy that in postrevolu- domestic and industrial wastes in most urban sewerage tionary China, where improved sanitation has high systems) than questions of cultural predisposition. If priority, urban public services are backed by voluntary there remain effective scruples regarding reuse, these committees, sponsored by the ruling party, that serve are more likely to lie with policymakers than with the to keep the authorities on their toes, while at the same users themselves, and top managers are the people time mounting health improvement campaigns and most exposed to the new ideologies about conservation other voluntary activities (Streefland 1978). Elsewhere, and the need to manage resources effectively. a major role for community development officials, In summary, how successfully the reuse of urban health education teams, and civic leaders must be the wastes can be controlled depends upon organization. generation of public support for and commitment to On the urban periphery, people may treat and reuse environmental improvement-not so much for the their own night soil in local fields or gardens, making it direct action that this can achieve as for the backing of very difficult for local authorities to establish workable the authorities attempting to carry out their proposals. controls. Similarly, small-scale private contractors in No civic administration can maintain the integrity of night soil removal who service a number of households its programs for long without active public support. and sell their product to farmers in the countryside Furthermore, because the kinds of sanitation schemes may easily escape bureaucratically administered envisaged here require radical changes in the control measures. If the municipality itself administers distribution and organization of services, radical night soil removal or contracts it to large-scale changes in civic consciousness will also be required. commercial enterprises. however, the authority is then Such changes are not always forthcoming. In this in a position to enforce suitable treatment before the imperfect world, realistic plans may need to accommo- product is made available for reuse. date existing interests and commitments and endeavor to promote change in spite of weaknesses in urban government and administration. Two different re- Improving the Management of Urban sponses are currently in evidence. The first is to create Sanitation Systems special-purpose agencies beyond the influence of local interest groups to take responsibility for the develop- The success of sanitation programs hinges largely on ment of a single city (as in the case of the urban the capability of the municipal governments or other development authorities found in most Indian cities), public authorities who must promote, control, and to look after the interests of a particular class of citizen, service the schemes. These authorities must not only or to provide for one kind of service on a regional basis. understand the nature of the task but must also be able There is a trend toward specialized water and to exercise their authority to enforce routines and sanitation authorities in many different parts of the ensure that the public plays its part. The need for world. The protagonists of these special-purpose administrative discipline extends beyond the super- agencies believe that such agencies will be more THE HUMAN ELEMENT IN SANITATION 125 effective development bodies than the traditional civic because some health benefits depend upon authorities because they are free to draw up rational complete coverage of the population, incomplete plans and follow priorities. Yet these bodies often find coverage will frustrate the objectives of the themselves in a competitive position with other program. authorities with similar or overlapping responsibilities, * There is no guarantee that those people who are and they still require constant political support to be most in need will be those who are most willing to effective. participate. To encourage self-help, the authorities The other approach is to rely upon technologies that will be obliged to help those who are prepared to require minimal municipal commitment and to ask the help themselves. Thus, self-help initiatives can potential users to construct and maintain latrines curtail the authorities' ability to decide upon through "self help." Pit latrines or on-site composting priorities. toilets require little municipal effort (see table 3-2) * Self-help can become a popular movement, backed beyond grants or technical assistance as inducements, by politicians for whom it provides a following, enforcement of bylaws if this is deemed necessary, and through which government finds itself committed some long-term emptying arrangements. to providing a level of service it lacks the financial Neither of these two approaches can be regarded as a or manpower resources to meet. substitute for getting wholehearted commitment to * Self-help programs have shown themselves to be improved hygiene and sanitation, based upon a broad much more effective at generating capital in the understanding of potential health and welfare benefits, form of "one-shot" projects such as classrooms, from politicians and citizens alike. This chapter clinics, or dams than in main1taininig services once concludes with a discussion of the strengths and they have been established. weaknesses of self-help schemes (which can be more Some of these difficulties can be overcome if than simple substitutes for municipal endeavor) in authorities take a more rigorous approach to the meeting these objectives, and of health education. organization of self-help projects from their inception.3 For instance, they may need to: Effectiveness and Limitations of Self-help * Enact by-laws requiring all households to provide Schemes themselves with latrines * Stipulate what categories of households they are Thllingness poteint iviauof lself rogrms, lies iong the prepared to assist with grants or technical guidance wilinnes o inivduas r gous, ve amngth and only help those who help themselves within poorest elements in society, to perform tasks such as laying pipes, digging pits, or improving their physical these categories environment for themselves. Self-help schemes can take * Ensure that the number of projects undertaken advantage of the spirit of self-reliance sometimes found does not outrun the funds available by persuading in informal or squatter settlements; they may also political leaders of the dangers in overstimulating work well where the ruling political party is active in demand and by requiring local groups to register urban management and can organize and control their intentions with the authorities before development, as in recent sites-and-services projects in undertaking a project Lusaka, Zambia. Carefully planned self-help exercises * Limit the scope of a scheme to a size that can be Luaa Zaba.aeul lne efhl xrie adequately serviced by the authority in the future. can totally transform a town, as in the case of Port Sudan, Sudan, where unplanned settlements have been In summary, self-help can best be used for clearly rebuilt and provided with basic services through the defined and limited operations, such as urban authorities and the people working in unison for a few cleanliness campaigns or the initial construction of days in each quarter of the town. Critical evaluations of public or private facilities, in which the people's self-help schemes (Chambers 1974; Feachem and contribution reduces costs and generates enthusiasm. others 1978; Holmquist 1970; Lamb 1971; Schaffer It can also be conveniently linked with the broader task 1969) reveal, however, that self-help often gets out of of health education. hand and ends in frustration for all parties. The potential hazards of self-help schemes in sanitation can be summarized as follows: 3. The advantages and dangers of self-help strategies in rural water supply programs, which have many similarities with sanitation * If participation is voluntary, some households will programs, are discussed in detail by Cairncross and others (1980). not participate for one reason or another and, The case against self-help is set out by Feachem (1980). 126 HEALTH HAZARDS OF EXCRETA Appropriate Health Education Curtis, D. (1978). Values of latrine users and administrators. In Sanitation in Developing Countries. Compiled by Oxfam At the beginning of this chapter it was said that some and The Ross Institute of Tropical Hygiene; ed. Pacey, A., values, attitudes, and understandings can be pp. 170-175. Chichester: John Wiley. accommodated by sanitary engineers, whereas other Dickson, D. (1974). Alterniative Technology and the Politics of social factors must be confronted and changed. In rural Technical ( i , London: Fontana/Collins. areas little progress can be made in cholera elimination Douglas, M. (1966). Purity and Danger. London: Routledge while people continue to locate privies over rivers that and Kegan Paul. downstream are other people's water supply. Health Dunn, F. L. (1972). Intestinal parasitism in Malayan education campaigns have to address specific issues of aborigines (Orang Asli). Bulletin of tihe Worldt Health this kind while simultaneously creating a general Organtization, 46, 99-113. awareness of the potentials of new technologies for - (1976). Human behavioural factors in the epide- improving living conditions. Health education is, miology and control of Wuchereria and Brugia infections. however,~~ ofe diapitn bot i.ndeig an n H. i, - sthePublic Health Societ'v i I I .,,-- .. 10, 34-44. however, otten disappointig both in deslgn and In (1979). Behavioural aspects of the control ofparasitic results. There is a tendency to lecture the public about diseases. Bulletin oJ tile World Health Organization, 57, good hygiene, or balanced diet, or birth control, 499 512. repeating textbook prescriptions without considering Elmendorf, M. (1980). Seven Case Studies ofRural and Urban how the ideas apply in the listeners' particular Fringe Areas in Latin America. Appropriate Technology circumstances. This tendency to patronize not only for Water Supply and Sanitation, vol. 8. Washington, minimizes the many real strengths in existing D.C.: World Bank, Transportation, Water and Tele- knowledge and practice, it is also ineffectual. It fails to communications Department. explore the users' viewpoint or to reveal the genuine Elmendorf, M. and Buckles, P. (1980). Sociocultural Aspects problems that technical innovations pose for them. of Wciter Supply and Excreta Disposal. Appropriate Health education has to be, above all, a dialogue Technology for Water Supply and Sanitation, vol. 5. between officials and users if full benefits are to be Washington, D.C.: World Bank, Transportation, Water obetwnee ofIcals Sandogouse ifd fullrbenefit Are tood b and Telecommunications Department. Obtained (Isely, Sanwogou and Martin 1979). A good Feachem. R. G. A. (1980). Community participation in example of this two-way communication is the health appropriate water supply and sanitation technologies: the education program that accompanied the Ibadan mythology ofthe Decade. P.......1. . ofthe RoYal Society comfort station pilot scheme (Ademuwagun 1975). of London. B, 209, 15-29. Not only were the positive values of the users explored Feachem, R. G. A., Burns, E., Cairncross, S., Cronin, A., here, but practical problems in implementation and Cross. P., Curtis, D., Khan, M. K., Lamb, D. and Southall, maintenance, such as finding suitable sites and paying H. (1978). Water, Health and Development: An Interdisci- for water, were clarified. Without this kind of detailed plinary Evaluation. London: Tri-Med Books. knowledge of the users' perceptual and organizational Feachem, R., Mara, D. and lwugo, K. (1980). Alternative c' . .Sanitation Techiologies Jor Urhan Areas in Africa. problems, campaigns instituted by the authorities are Appropriate Technology for Water Supply and almost certain to founder in disenchantment and Sanitation, vol. 7. Washington, D.C.: World Bank, disorder. Health education has a critical, sensory role Transportation, Water and Telecommunications in community affairs. It cannot merely be the vocal Department. chords of the sanitation authorities, it must be their Goyder, C. (1978) Voluntary and government sanitation eyes and ears as well. programmes. In Sanitation in Developing Countries. Compiled by Oxfam and The Ross Institute of Tropical Hygiene; ed. Pacey, A., pp. 162-170. Chichester: John Wiley. Literature Cited Holmquist, F. (1970). Implementing rural development projects. In Development Administration: The Kenyan Ademuwagun, Z. A. (1975). The Ibadan Comfort Stations: An Experience, eds. Hyden, G., Jackson, R. and Okumu, J., pp. Experiment in Environmental Sanitation Health Education. 201 229. Nairobi: Oxford University Press. Ibadan: African Regional Health Education Centre, Isely, R. B., Sanwogou, L. L. and Martin, J. F. (1979). Faculty of Medicine, University of Ibadan. Community organization as an approach to health Cairncross, S., Carruthers, I., Curtis, D., Feachem, R., education in rural Africa. International Journal of Health Bradley, D. and Baldwin, G. (1980). Evaluationfor Village Education, 22 (supplement), 1-19. Water Supply Planning. Chichester: John Wiley. Jackson,T. (1979). Rural sanitation technology:lessonsfrom Chambers, R. (1974). Managing Rural Development: Ideas participating research. .4ssignment Children, 45/46, 51-74. and Experiencefrom East .4frica. Uppsala: The Scandina- Kalbermatten, J. M., Julius, D. S. and Gunnerson, C. G. vian Institute of African Studies. (1982). Appropriate Sanitation Alternatives: A Technical THE HUMAN ELEMENT IN SANITATION 127 and Economic Appraisal. World Bank Studies in Water Low-Cost Technology Options for Sanitation: A State-of- Supply and Sanitation 1. Baltimore, Md.: Johns Hopkins the-Art Review and Annotated Bibliography. Publication University Press. IDRC-102e. Ottawa: International Development Kochar, V. (1978). Culture and hygiene in rural West Bengal. Research Centre. In Sanitation in Developing Countries. Compiled by Oxfam Schaffer, B. B. (1969). The deadlock in development and The Ross Institute of Tropical Hygiene; ed. Pacey, A., administration. In Politics and Change in Developing pp. 176-185. Chichester: John Wiley. Countries, ed. Leys, C., pp. 177-211. Cambridge: (1979). Culture Parasite Relationship: Socio- Cambridge University Press. behavioural Regulation of Hookworm Transmission in a Schwartz, D. (1977). The mass line as consumer participation West Bengal Region. Studies in Medical Social Science no. and community involvement: a comparison between the 1. Varanasi, India: Centre for Medical Social Science and Chinese approach and "Western" health education Social Medicine, Banaras Hindu University. principles. International Journal of Health Education, 20 Krauss, A. P. (1979). Design involvement leads to public (supplement), 1-17. acceptance. Water and Wastes Engineering, 16, 50-52. Spencer, K. (1978). Managing the expansion of Port Sudan. Lamb, G. B. (1971). Peasant Politics. London: Julian Paper presented to the Red Sea Hills Development Friedmann. Conference, 1978. Birmingham: Institute of Local Muhondwa, E. P. Y. (1976). Latrine Installation and Use in Government Studies, Birmingham University. Bagamoyo District: A Study of Sociological Factors. M.A. Streefland, P. H. (1978). The social organization of nightsoil thesis. Dar es Salaam: University of Dar es Salaam. collection. In Sanitation in Developing Countries. Compiled Pacey, A., ed. (1978). Sanitation in Developing Countries. by Oxfam and The Ross Institute of Tropical Hygiene; ed. Compiled by Oxfam and The Ross Institute of Tropical Pacey, A., pp. 133-138. Chichester: John Wiley. Hygiene. Chichester: John Wiley. Van Wijk-Sijbesma, C. (1979). Participation and Education in Pasteur, D. (1979). The Ibadan comfort stations programme: Community Water Supply and Sanitation Programmes: A a case study of the community development approach to Literature Review. Technical Paper no. 12. The Hague: environmental health improvement. Journal of Admini- World Health Organization International Reference stration Overseas, 18, 46-58. Centre for Community Water Supply. Rybczynski, W., Polprasert, C. and McGarry, M. G. (1978). Part Two Environmental Biology and Epidemiology of Specific Excreted Pathogens SECTION I Excreted Viruses Chapter 9 Enteroviruses, Poliomyelitis, and Similar Viral Infections 10 Hepatitis A Virus and Infectious Hepatitis 11 Rotavirus and Viral Gastroenteritis 9 Enteroviruses, Poliomyelitis, and Similar Viral Infections OVER 100 DIFFERENT VIRUSES are known to be fecally wide variety of diseases (table 9-1). The polioviruses are excreted by man. New viruses are still being discovered, probably the most important. They were the first and several have yet to be fully characterized. Typically enteroviruses to be fully investigated, and because they they infect the alimentary canal and are shed in very are relatively easy to culture they have been used in large numbers by infected persons (Madeley 1979). most experimental work. Diseases caused by these organisms range from the trivial to the serious or even fatal. The occurrence and Identification medical significance of excreted viruses in the Poliomyelitis is unique in being the major per- environment is the most rapidly changing field of manently crippling disease of infectious origin. It is knowledge reported here. A combination of heightened caused by the infection of the central nervous system by environmental concern (especially in the USA), poliovirus or occasionally another enterovirus. It is improvements in laboratory techniques, and the recent usually recognized by a sudden and unexpected onset discovery of important new human viral pathogens of tiredness and weakness in the limbs. Fortunately, the (especially rotavirus) have caused a marked increase in clinical symptoms of poliomyelitis occur in only a very scientific activity, with several hundred papers yearly small proportion of the persons infected, usually a now being published on aspects of excreted viruses maximum of 2 and often less than 1 percent of the total. (EPA 1978, WHO 1979). mxmmo n fe esta ecn ftettl Table 9-1 presents a classification of some excreted The clinical effects of infection range from the viruses similar to that recently proposed by the World asymptomatic through nonspecific minor illness to Health Organization (WHO 1979). This classification meningitis, paralysis and possibly death. There are two Health undoubtedlyunderganization chang 1r this c ati basic patterns of symptoms. The first is a minor illness will undoubtedly undergo changes over the next few arising a few days after infection, lasting 1-2 days and years as new viral agents are characterized and the characterized by mild fever, listlessness, sore throat and taxonomy is revised. For the purposes of this book, vomiting. The second, developing 3-4 days later but excreted viruses are divided into three groups: often occurring without the first phase, is much more e The enteroviruses (chiefly polioviruses, coxsackie- serious. Symptoms of aseptic meningitis, fever, severe viruses and echoviruses), described in this chapter, headache, and vomiting are followed by stiffness of the which also contains some information on aden- neck and back. In paralytic cases the disease usually ovirus and reovirus, as these are often considered leads to progressive weakness resulting in severe jointly with enteroviruses; (see figure 9-1) paralysis. Death, usually caused by respiratory failure, * The hepatitis A virus described in chapter 10 may occur. * The viruses possibly associated with gastroenteritis The disease is short-lived and most people recover (rotavirus, Norwalk agent, and others) described in fully, but many of the most severely affected are chapter 11. permanently disabled. Mortality among the paralytic cases varies between 4 and 10 percent depending on the Description of Pathogens and Diseases virulence of the virus, the degree of medical care and the age of the patient. Diagnosis in asymptomatic cases The enteroviruses are an acid-stable subgroup of the is dependent on laboratory facilities in which the virus small picornaviruses. They are a large group causing a can be cultured from throat swabs or feces. Serological 133 134 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Table 9-1. Human Excreted Viruses Chapter Number in which Size and of described Virus group Family composition types Diseases or symptoms caused 9 Enterovirus Picornaviridae About 20-30 nanometers diameter. Single- Poliovirus stranded RNA in a 3 Poliomyelitis, meningitis, fever protein shell Coxsackievirus 24 Herpangina, respiratory disease, meningitis, A fever Coxsackievirus 6 Myocarditis, congenital heart anomalies, B meningitis, respiratory disease, pleurodynia, rash, fever Echovirus 34 Meningitis, respiratory disease, rash, diarrhea, fever New 4 Meningitis, encephalitis, respiratory disease, enteroviruses acute hemorrhagic conjunctivitis, fever Adenovirus Adenoviridae About 70-80 nanometers > 30 Respiratory disease, eye infections diameter. Double- stranded DNA in a protein shell Reovirus Reoviridae About 75 nanometers 3 Not clearly established diameter. Double- stranded RNA in a double protein shell 10 Hepatitis A ? About 24-29 nanometers I Infectious hepatitis virus Picornaviridae diameter. Single- stranded RNA 11 Rotavirus Reoviridae About 70 nanometers ? Vomiting and diarrhea diameter. Double- stranded RNA in a double protein shell Astrovirus ? About 28 nanometers ? ? diameter Calicivirus ? About 35-40 nanometers ? Vomiting and diarrhea diameter. Single- stranded RNA in a protein shell Coronavirus Coronaviridae Between 20 and 220 ? Common cold nanometers diameter. Pleomorphic with petal-shaped projec- tions 20 nanometers long. Single-stranded RNA in protein shell and lipid envelope Norwalk agent ? About 20-35 nanometers ? Vomiting and diarrhea and other diameter small round viruses Not Adeno- Parvoviridae About 19 nanometers 4 Not clearly established but associated with described associated diameter. Single- respiratory disease in children virus stranded DNA in protein shell ENTEROVIRUSES, POLIOMYELITIS. AND SIMILAR INFECTIONS 135 tests can also be used. Treatment is supportive in infection for the other enteroviruses. A number have nature. been isolated from pets and other animals associated The other enteroviruses can cause a wide variety of with man, but it is unclear whether or not they were symptoms (table 9-1). These viruses are generally less naturally infected. Reovirus appears to be an dangerous than poliovirus and like poliovirus they exception, having been isolated from a surprisingly only cause significant disease in a small proportion of large range of animal species. Even so, animals have cases. They normally infect the alimentary canal or the not been shown to be a significant source of infection respiratory tract, giving rise to gastroenteritis or for man. influenza-like symptoms. More severe disease is often associated with the spread of the virus to other organs such as the liver or central nervous system. As with .s . polio, the effects are generally short-lived, and Transmission treatment is supportive. Infected persons can shed very large numbers of Diagnosis is either based on symptoms or on virus particles-more than 106 per gram of feces. laboratory culture and identification. Diagnosis is Viruses are also present in throat secretions, especially complicated by the fact that the same virus may cause during the early stages of infection. These particles are different symptoms in different patients and that highly infectious and can remain viable for a different viruses may give rise to similar symptows. considerable period under suitable conditions. Infection takes place when the virus is ingested, possibly in food or water. The primary sites of infection Occurrence are the throat and the lower alimentary canal. Within a few days the virus spreads to the lymphatic system and Thesen. infetionsocatedcurwor tide handve very the blood stream. This phase corresponds with the common. Some Isolated communities have been mnrsmtm fifcin ntesalpooto known that were not infected with poliovirus but few or mosor symptoms of vfectionf In the small propouti none now remain. The other enteroviruses have a of severe cases the virus mfects the central nervous similar distribution, but there are local variations in system, possibly by spread along nerve fibers. both'virustypesan in the virulence of varios . On infecting a suitable cell, the virus diverts the cell's b metabolic activity to the production of large numbers of virus particles identical to the original virus. These are liberated when the cell breaks down, and they either Infectious agents infect other cells or, in the case of the cells lining the Poliovirus is a small spherical particle 28 nano- alimentary canal, are passed out in the feces. meters in diameter and is therefore not visible by Transmission is mainly directly from person to person normal light microscopy (figure 9-1). It occurs in three either by the oral-oral route or the fecal-oral route. serotypes, numbered 1 to 3. A most important There is some indication that in unhygienic conditions characteristic is the degree of neurovirulence, which is the latter route is the most common, with the former known to vary from strain to strain in all three types. route being more important under more sanitary The infective dose is small: probably as little as one conditions. Children under the age of 2 years are the virus particle. Poliomyelitis can occasionally be caused most potent disseminators by both routes. by coxsackie- and echoviruses. There are indications that poliovirus is carried Like poliovirus, the other enteroviruses are sub- between family groups by young children who are both microscopic spherical particles with sizes ranging susceptible and mobile (2-6 year age group). Infection between 20 and 30 nanometers in diameter. The then spreads within the family downwards to number of types in each group is given in table 9-1. nonmobile children and upwards to older children and adults. Up to 50 percent of persons having resistance from earlier infections may become reinfected, but in Reservoir these cases the excretion of viruses is much reduced and symptoms absent. The reservoir of poliovirus is man. Chimpanzees The other enteroviruses are probably transmitted by have been known to catch the disease in captivity, and the same route as poliovirus, whereas the adenoviruses, monkeys may also act as natural hosts, but nonhuman which are normally associated with upper respiratory reservoirs have not been shown to be significant. tract infections, are mainly spread by an airbornc route As with poliovirus, man is the main reservoir of from contaminated throat secretions. 136 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Figure 9-1. Polio-, adeno-, and reoriiruses under electronmicroscopy. (a) Polioviruses under scanning electronmicroscopy. Other enteroviruses have a similar appearance. Scale bar = 0.1 micrometers. (Photo: World Health Organization, Geneva, Switzerland.) (b) Adenoviruses under transmission electronmicroscopy. Scale bar = 0.1 micrometers. (Photo: A. J. Zuckerman, London School of Hygiene and Tropical Medicine, London, U.K.) (c) Reoviruses under transmission electronmicroscopy. Scale bar = 0.1 micrometers. (Photo: A. J. Zuckerman, London School of Hygiene and Tropical Medicine, London, U.K.) Incubation period Period of communicability Minor illness when present occurs within 2-3 days of Viruses have been found in the throat secretions and infection. Nervous system involvement possibly lead- feces within 24 hours of infection, and contact cases ing to paralytic poliomyelitis may occur between 5 and have been observed within 3 days. Virus excretion, 35 days after infection-on average 17 days. The other mainly in the feces, has been observed for as long as 17 enteroviruses are generally similar to poliovirus. weeks, and on average 7 weeks. ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 137 Most of the other enteroviruses are excreted for a Control Measures shorter period than poliovirus. Coxsackie B viruses, for example, are excreted for I week or less. The In considering the control of enterovirus infections, adenoviruses, however, may persist in a latent form in one must distinguish clearly between reducing the tonsils and adenoids. infection and reducing disease. In the case of poliovirus, for instance, environmental measures may reduce transmission and thus the incidence of infection. Resistatnce However, these measures may increase the incidence of serious clinical disease by deferring the age of first infection to that at which disease is more likely to be Young children are the most susceptible age group, most adults having acquired resistance to poliovirus severe. A survey of 10,000 households in 25 villages in during earlier infections or by vaccination. Infection Gujarat (India) found that the number of paralytic leads to the development of life-long immunty to the poliomyelitis cases per 1,000 households was related to ...i u i mm y s . household income. Among low-income households infecting type of virus, but the individual may still be there were 12 cases per 1,000 houses; among middle- vulnerable to other types. there were 18 cases per 1,000 The severity of the disease is markedly dependent on houses;handeamong high-income householdsrthere the age of the patient; in a nonresistant population, were 24 cases per 1,000 houses (Jhala, Goel and Dave teenagers and young adults show the most severe 1979 2 Contrapevidence isures a recent reve symptoms. Certain other factors have been found to increase the severy of te dshowing that the real (as opposed to reported) annual incsillecthey severity,of theent disculasetionc,uhyn incidence of paralytic poliomyelitis in Burma, Egypt, tonsillectomy, pregnancy, recent noculations physical Ghana and the Philippines is between 233 and 3,800 exertion, and trauma.e Infection by theotherenterovirusesusuallyconfers per 1 million children age 0-4 years, and between 37 Infection by the other enteroviruses usually confers and 589 per 1 million of the total population (Sabi resistance in a similar manner, but vaccines are not 19 per cen of paral epion tSe generally available. 1980). About 90 percent of paralytic episodes m these countries occurred during the first 3 years of life. Despite the fact that for various technical reasons these annual incidences are underestimates, they are similar Epidemiology to or considerably higher than the rates occurring in the USA in the immediate prevaccine era. These data During this century the incidence of poliomyelitis cast doubt on the belief that improved living has been observed to change from a constant conditions, in the absence of vaccination, increase the background infection to epidemics of increasing incidence of poliomyelitis disease. severity. In temperate climates these occur in late summer and early autumn. In the tropics and subtropics the fluctuations are less marked, but the Indftidual trend is the same. The reasons for this change are not fully understood but may be due to variations in Highly efficient vaccines are available for the three hygiene or other factors affecting virus transmission polioviruses. Both killed and live attenuated vaccines and so leading to variations in the resistance within the can be used. The live vaccine is probably preferable in community. In areas with poor hygiene children developing countries because it is easily administered acquire immunity while very young, and the pro- on a lump of sugar, whereas several injections are portion of paralytic cases is therefore low and confined required for the killed vaccine. The live vaccines to this age group. Disruption of this pattern of infection contain a mixture of attenuated (weakened) strains of may lead to a higher incidence of severe symptoms at a virus that establish an infection which leads to later period. Another possibility is that more virulent resistance but, unlike many of the wild strains, does not strains of virus have been introduced. infect the nervous system. These attenuated strains can Many of the other enteroviruses act in a similar also spread from person to person and so immunize a manner to poliovirus. Often serial waves of infection greater number of people but do not spread as move through the community, fading away to a very efficiently as the wild virus. The wild viruses are low or undetectable level and being replaced by suppressed but not eliminated from the community. It infection with another type of virus. Seasonal is therefore necessary to maintain the vaccination of variations also occur. young children to prevent the build up of a susceptible 138 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES group. Resistance appears 7-10 days after vaccination. is a rate process, and the removal of infectivity The response is sufficiently rapid to be of great benefit therefore depends on both the efficiency of removal and during an epidemic. No vaccines are available for the the numbers initially present. In feces and sewage these other enteroviruses. may be higher than 106 per gram and 106 per liter, No specific drugs are available either for chem- respectively. otherapy or prophylaxis. Good personal hygiene and The enteroviruses (chiefly polio, coxsackie, and the avoidance of contaminated food and water may echo), and to a lesser extent adenoviruses and reduce the risk of mild infection in early childhood but reoviruses, have been the only excreted viruses to be thereby increase the risk of severe infection later. extensively studied in the environment. This is partly because certain other important excreted viruses Environmental (particularly hepatitis A virus and rotavirus) cannot be routinely grown in cell culture at the present time. Improvements in excreta disposal alone are unlikely However, as laboratory skills improve, and as models to have a great impact. The highly infectious nature of for human excreted viruses are developed (for instance, viruses, the preponderance of young children among reoviruses and simian rotaviruses may provide models the cases, and the large proportion of symptomless for human rotaviruses), more data will be obtained on infections indicate that the main route of infection will the environmental behavior of excreted viruses other remain from person to person. The elimination of than the enteroviruses. Preliminary evidence from a excreta as a source of infection may change the primary few studies indicates that there may be significant means of transmission from the fecal-oral to the oral- differences between rotavirus, hepatitis A virus, and the oral route. Improvements in both general hygiene and enteroviruses in their environmental characteristics excreta disposal are likely to have an effect and may be (Farrah and others 1978: Wallis and Melnick 1967), responsible for the trend toward the epidemic type of although a recent study has shown that simian poliovirus transmission. In these circumstances in- rotavirus has survival properties in fresh and saline fection will probably be delayed rather than prevented, waters similar to enteroviruses (Hurst and Gerba and the proportion of patients with severe symptoms 1980). may increase. This can be prevented in the case of Throughout the rest of this chapter, data are poliomyelitis by the use of vaccines. presented on the numbers of viruses that researchers Polioviruses and other enteroviruses have been have isolated from various environmental samples. It isolated from flies and cockroaches. For instance, in must be stressed that these numbers depend very Texas (USA)polioviruses were isolated from 15 percent considerably on the techniques used; in general, as of flies, while coxsackieviruses were isolated from 45 techniques improve reported concentrations of en- percent, and flies experimentally fed polioviruses teroviruses from a particular source (for example, river continued to excrete them for up to 2 weeks (Melnick water) increase. The very earliest studies reported only and Dow 1953). It is clear from this and similar studies the proportion of samples from which viruses could be that insects can pick up viruses and may subsequently isolated-for instance, 62 percent of sewage effluent contaminate food, but it is unknown whether this mode samples contained enteroviruses. Subsequently, quan- of transmission is of any epidemiological significance titive techniques were developed that were based on (see chapter 37). observed cell death following inoculation with varying dilutions of sample, and these yielded a count of median tissue culture infective doses (TCID50) per Occurrence and Survival in the volume of sample. More recently, most laboratories Environment have adopted a technique whereby a direct count is made of plaques formed by viruses on cell monolayers, Viruses are not capable of multiplying outside of or in cell suspensions, which yields a count of plaque- living cells; therefore, in the environment their forming units (PFUS) per volume of sample. In both the numbers can only decrease. In favorable conditions, TCID and PFU techniques, counts depend upon the however, they can survive for months. Their survival is choice of cell line because different viruses will replicate aided by neutral pH and the presence of particulate or with varying readiness in different primate cells organic matter, moisture and, in particular, low (Schmidt and others 1978). temperatures. Resistance to inactivation varies con- When viruses are present in small numbers in large siderably among different types of virus and even volumes of sample, a variety of different methods can among different strains of the same virus. Inactivation be used to concentra te them. When viruses are bound ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 139 to each other in clumps, or are adsorbed to solid nonpolluted fresh water at 20°C and found that a 3 log particles, efforts must be made to disaggregate them. unit reduction occurred in 3 to > 14 days. For each Even adopting the most careful and sophisticated virus, survival times were similar in polluted and techniques, recovery of seeded enteroviruses from nonpolluted waters. The strong influence of tempera- environmental samples is typically below 60 percent. ture on enterovirus survival is illustrated by the To add to the complexity and uncertainty, results survival of 34 percent of enterovirus during 7.1 days of obtained are still too dependent upon the personal travel under the ice of a frozen 317 kilometer section of technique of the laboratory staff and the whole the Tanana River (Alaska, USA) (Dahling and tradition and routine of the particular laboratory. Safferman 1979). Quantitative data on viruses in the environment A number of workers (for instance, Cubbage and should therefore be taken as indicative only. others 1979, Katzenelson 1978, Young and Sharp Throughout this chapter concentrations are given as 1977) have noted that the observed loss of infectivity of viruses per volume or weight of sample although, viruses in water may be due in part to genuine damage strictly speaking, they should be as infective units or to the virus and in part to an artifact caused by many TCID5o or PFUS per sample. viruses aggregating and simulating a single infectious particle. This aggregation may involve the adsorption of viruses onto suspended particulate matter or it may Inl surface waters involve the formation of virus clumps. Enteroviruses can be isolated in low concentrations An important aspect of the behaviour and survival of from almost all surface waters receiving human wastes. viruses in natural waters is their tendency to become For instance, the Thames at London (UK) contains up adsorbed to organic or inorganic suspended particles. to about 100 enteroviruses per liter, with a peak usually Adsorption is enhanced at slightly acidic pH and in the occurring in winter (WHO 1979; the River Sowe (UK) presence of divalent cations and is deterred by the in December contained up to 620 enteroviruses per presence of soluble proteins (Schaub and Sagik 1975; liter (Morris and Waite 1980); the Missouri and Schaub, Sorber and Taylor 1974). Furthermore, Mississippi rivers (USA) have yielded up to 0.1 and 0.4 viruses adsorbed to solids retain their infectivity both enteroviruses per liter respectively; the Seine at Paris to tissue culture cells and mice (Moore, Sagik and and the Moselle at Nancy (France) have contained up Malina 1975; Schaub and Sagik 1975; Schaub, Sorber to 170 and 280 enteroviruses per liter, respectively and Taylor 1974). Adsorption to solids may cause an (Berg and Metcalf 1978). accumulation of viruses in bottom sediments, from Survival in water is dependent primarily upon which they may subsequently be resuspended in the temperature and the degree of contamination. Studies overlying waters. Wellings, Lewis and Mountain listed in the appendixes of Feachem and others (1980) (1976) isolated more than 15 excreted viruses per 100 show that at temperatures less than 10°C survival times grams of mud nearly 1 kilometer dowstream from a of between 24 and more than 272 days are reported, primary effluent discharge site. No virus was isolated while at temperatures above 20°C the range is 4 to 135 from the overlying river water at this site. days. In a study of enterovirus survival in the Rio There is very little evidence that the transmission of Grande (New Mexico, USA), at 23-27C, 90 percent enteroviruses during recreation in polluted surface inactivation occurred in 25 hours for poliovirus 1, 19 waters is of any public health importance. The spread hours for poliovirus 3, and 7 hours for coxsackievirus of adenovirus in swimming pools has been de- A13. At river temperatures of 4-8°C, the time for 90 monstrated or suspected in several investigations (for percent inactivation of poliovirus 1 was 46 hours instance, Heinz and others 1976). (O'Brien and Newman 1977). Niemi (1976) studied the In summary, a few enteroviruses may survive for survival of coliphage T7 in samples of Finnish river many months, although 90 percent reduction usually water and found that, after 64 days at 3°C, a 99.5 occurs within a few days, and 99 percent reduction percent reduction occurred, whereas after 64 days at within 1 month. Temperature is the single most 20°C a 99.98 percent reduction was recorded. Joyce determining factor and 99 percent reduction at 20°C and Weiser (1967) found that poliovirus did not survive may be expected within about 10 days. Survival is for more than 63-84 days at 20-25°C, but survived for longer in heavily polluted or in very clean waters. Very more than 91 days at 4°C when stored in samples of little data are available on virus survival in surface various farm pond waters. Hurst and Gerba (1980) waters in the tropics (Lund 1979), and more research is studied the survival of poliovirus 1, echovirus 7, required. Addy and Otatume (1976) isolated en- coxsackievirus B3 and simian rotavirus in polluted and teroviruses from 28 percent of surface water samples in 140 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES the Accra area (Ghana), with highest isolation rates (80 the sections below on survival in soil and on sewage percent) obtained from polluted street drains. treatment by septic tanks and land application. The However, because surface waters in the tropics are literature on viruses in groundwater has been reviewed typically in the temperature range of 20-30°C, it is elsewhere (Keswick and Gerba 1980). reasonable to expect that survival times will be considerably shorter than those generally reported In drinking water from temperate areas. Attention has been paid recently to the occurrence In groundwater- and epidemiological significance of enteroviruses in water supply systems (Anon. 1978: Committee on Enteroviruses have been isolated from groundwater, Viruses in Drinking Water 1979; EPA 1978; Mahdy especially in situatiorn where the groundwater is 1979; Melnick, Gerba and Wallis 1978; WHO 1979). shallow and sewage effluent or sludge has been applied Enteroviruses have been isolated in very low to the overlying soil. Survival of enteroviruses in concentrations from some treated, chlorinated water groundwater may be somewhat longer than in similar supplies in France, India, Israel, Italy, Rumania, South surface waters at the same location because in hot Africa, USA and USSR (Committee on Viruses in climates the groundwater is cooler than the surface Drinking Water 1979; Gamble 1979; Kott and others water (in cold climates the opposite may be true) and 1974; Melnick, Gerba and Wallis 1978: Rao, Lakhe groundwater is not exposed to sunlight. and Waghmare 1978; WHO 1979). A considerable Wellings and others (1975) demonstrated en- debate has developed over whether these very low virus teroviruses in shallow groundwater beneath a waste- concentrations in treated drinking water constitute a water irrigation site in Florida (USA) and showed that cause for concem on public health grounds. There is the viruses could survive in groundwater for at least 28 strong support, especially among environmental days. Wellings also reported a tentative association virologists in the USA, for the concept that, because between the pollution of groundwater by septic tank viral infectious doses may be very low, small numbers effluent and an outbreak of disease associated with of viruses in large volumes of drinking or recreational echovirus 22/23 complex at a migrant labor camp in water are important. It is postulated that viruses in Florida (Wellings, Mountain and Lewis 1976). Vaughn water may cause low-level transmission which remains and others (1978) reported low levels of virus undetected due to the large proportion of asympto- contamination (up to 3 viruses per liter) in wastewater matic infections and the varied symptomatology (table recharged groundwater on Long Island (New York, 9-1) in those individuals experiencing frank disease USA) at sites where recharge basins were located less (Berg 1967; Committee on Viruses in Drinking Water than 10 meters from the aquifer. This contamination 1979; WHO 1979). Some of those who take this view occurred despite the fact that all wastewaters had urge the adoption of stringent virus quality standards, undergone either chlorination or tertiary treatment by such as less than one infective unit per 40-100 liters in sand filtration. Slade and Edworthy (1981) isolated up recreational water and less than one infective unit per to 1.3 x 104 viruses per liter from groundwater in 100-1,000 liters in drinking water (Mahdy 1979; chalk beneath groundwater recharge lagoons receiving Melnick, Gerba and Wallis 1978; Shuval 1975; WHO raw comminuted sewage, but failed to detect viruses 1979). This school of thought has been influenced by from boreholes 120 meters and 400 meters downstream the unfortunate view that, because it is technically (in relation to groundwater flow) from the recharge possible to achieve a certain level of water purity, it is area. A study of groundwater pollution in Israel therefore desirable.' isolated enteroviruses in 20 percent of 99 samples and 1. For example. Melnick (1976) writes: "I suggest a... d in 12 samples enteroviruses were isolated in the maximum of one detectable virus unit per 10 gallons of recreational absence of fecal coliforms and fecal streptococci water and a maximum of one infectious virus unit per 100 gallons of (Marzouk, Goyal and Gerstreptococci drinking water. As our methods for detecting and monitoring water (Marzouk, Goyal and Gerba 1979). supplies have continued to improve, I would suggest that we can do Little is known about virus survival in groundwater, better, and raise the standards to a maximum of one infectious virus but estimates may be made from the data on survival in per 1,000 gallons ofc drinking water." Simtlarly, the WHO Scientific surface waters reported above. Yeager and O'Brien Working Group on Human Viruses in Water, Wastewater and Soil (1977) reported that a 90 percent reduction of concluded that "the presence of even a few enteric viruses in a large enteroviruses in groundwater occurred in 11 to 14 volume of drinking water should be prevented, since treatment measures exist to achieve this goal and detection techniques are days. Information on the travel of enteroviruses becoming available which can provide the required level of through soils to pollute groundwater is contained in monitoring" (WHO 1979). ENTEROVIRUSES, POLIOMYELlTIS, AND SIMILAR INFECTIONS 141 This point of view is refuted by others (especially likely that this was a wild strain of poliovirus. More European workers and those with an epidemiological data of this type are urgently required. perspective) who point out that there is no evidence for the existence of low-level waterborne transmission and that, even if it did exist, it might make no significant In seawater contribution to the maintenance of the endemicity of Many coastal communities discharge untreated or enterovirus infections (Gamble 1979). The authors of partially treated wastes into the sea. This is not only the this book support this second viewpoint. There is case in developing countries but is common practice strong epidemiological and theoretical evidence that throughout the world; for instance untreated sewage is enterovirus transmission is primarily by the person-to- discharged in large quantities at Honolulu and Miami person route2 and may indeed be oral-oral as well as Beach (USA) (Ruiter and Fujioka 1978; Edmond, fecal-oral. It is unlikely that very low concentrations of Schaiberger and Gerba 1978). The potential health enteroviruses in treated drinking water make any hazards are those of infection of bathers and marine epidemiologically significant contribution to trans- sportsmen and the contamination of shellfish. Recent mission3, and any decision on increased water quality advances in laboratory techniques have permitted the standards, implying increased treatment costs, must concentration of small numbers of viruses from large await evidence of the benefits to be expected from such volumes of turbid seawater (Payment and others 1976) a policy. This view is especially pertinent in developing and have encouraged a number of investigations into countries where there are severe shortages of both viral pollution of the marine environment. financial and technical resources. Edmond, Schaiberger and Gerba (1978) studied Some studies on the survival of enteroviruses in enterovirus contamination of seawater along the treated drinking water are listed in the appendixes of Florida coast (USA), an area of exceptional impor- Feachem and others (1980). One study (Lefler and Kott tance for marine recreation. Between Palm Beach and 1975) found that at 18-25°C 99.9 percent of Virginia Key there are 10 ocean outfalls discharging polioviruses were inactivated in 91 days in tap water and approximately 6 x I 05 cubic meters per day of raw and in 112 days in distilled water. At 4-8°C, poliovirus was treated sewage. The Miami Beach outfall discharges completely stable in tap water and distilled water for 231 1.8 x 105 cubic meters per day of untreated sewage at a days. Kott, Ben-Ari and Vinokur (1978) reporteda99.9 depth of 44 meters. The authors found enteroviruses at percent reduction of poliovirus after 80 days in tap the surface above the outfall at concentrations between water at 18-23cC. 21 and 42 infectious units per 400 liters. Fecal coliforms A quite distinct problem is that of enteroviruses in at this site were in the range 0.9-1.4 x 104 per 100 untreated and polluted drinking water. Very few data milliliters, and fecal streptococciwereO.5-4.9 x 10' per exist on virological aspects of water supplies in l00milliliters.AtMiamitheoutfalldischarges2 x 105 developing countries (Lund 1979), but the bacte- cubic meters per day of sewage treated by activated riological data indicate the probability of substantial sludge and chlorination at a depth of only 5 meters. At viral pollution of many sources. A study in Ghana this site between 0 and 3 enteroviruses per 400 liters (Addy and Otatume 1976) isolated enteroviruses from were detected, with fecal coliforms always less than 3 3 out of 8 water samples taken from 3 drinking water per 100 milliliters and fecal streptococci less than 33 per wells near Accra. Poliovirus 1 was isolated from one 100 milliliters. The marked difference in fecal pollution well and, since vaccination rates are extremely low, it is caused by discharging untreated and treated effluent was clearly demonstrated. 2. In this connection, it is unlikely that the assertion of Berg Loh, Fujioka and Lau (1979) reported that the city (1978a) that "the source of most of the viruses that infect man of Honolulu (Hawaii, USA) discharges 2.5 x 105 cubic through the oral route is wastewater" is true. There is certainly no meters of raw sewage per day into the Mamala Bay at a evidence to support it, whereas there is ample evidence of the point 3.2 kilometers from Ala Moana beach and 6.5 vigorous transmission of enteroviruses, particularly vaccine-derived kilometers from Waikiki beach. Up to 420 en- polioviruses, among members of the same household and especially terovir among very young children (see the subsection below on uses perlter were isolated from the sewage, and enteroviruses in feces and night soil). enteroviruses were isolated from the bay water at distances of up to 3.2 kilometers from the discharge 3. Further evidence of this is provided by unpublished data from ste.cAt om splingklocatios distan fromhthe Britain which shows that enterovirus levels in rivers and reservoirs site. At some samplmg locations distant from the (and therefore presumably in drinking water) tend to peak in winter, sewage outfall, enteroviruses were isolated from waters whereas enterovirus infections, and levels in sewage, tend to peak in which contained negligible numbers of fecal indicator late summer. bacteria. 142 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Survival of enteroviruses in seawater is generally centration of enteroviruses was weakly but reported to be shorter than in freshwater. However, significantly correlated with rainfall, total coliform enteroviruses survive for longer in seawater than counts and salinity (accounting together for appro- coliform bacteria and there have been several reports of ximately 16 percent of the variance in the virus data). enterovirus isolations from seawater containing very Enteroviruses were isolated from 43 percent of few or no coliforms (Berg and Metcalf 1978). Won and recreational water samples judged acceptable by total Ross (1973) reported a 99.9 percent reduction of coliform standards (<1,000 per 100 milliliters), and echovirus 6 in aerated seawater after about 2 days at from 35 percent of shellfish-harvesting waters judged 22°C and after about 6-7 weeks at 3-5°C. The survival acceptable by total coliform standards ( < 230 per 100 in seawater was unaffected by the addition of organic milliliters). Similar studies in the same area are substances. Akin and others (1976) reported a 99.9 reported by Goyal, Gerba and Melnick (1978). percent reduction in poliovirus 1 in 5-6 days at 24°C in Studies of pollution in the Firth of Forth estuary the Gulf of Mexico. Fujioka, Lau and Loh (1978) (Scotland) revealed adenoviruses, coxsackieviruses, found a 90 percent reduction in poliovirus at 25°C in 1 polioviruses and echoviruses at two sites where median day in seawater collected close to the shore, and in 2-3 fecal coliform levels were 2.1 x 104 per 100 milliliters days in seawater collected farther out. Further and 4.2 x 103 per 100 milliliters (Watson 1977). experiments revealed the strong possibility of a specific Studies in an estuarine environment in the USA virucidal activity displayed by unidentified marine (salinity 0.9-2.8 percent, temperature 6-24°C) isolated microorganisms. In another study the same authors enteroviruses from 6 percent of water samples and 17 (Loh, Fujioka and Lau 1979) reported 90 percent percent of bottom sediment samples (Vaughn and reduction of poliovirus 1 in 2 days, and 99.9 percent Metcalf 1975). Survival experiments in the same study reduction in 4 days, in both sewage-contaminated and showed a 99 percent reduction in coxsackievirus B3 in sewage-free seawater at 24°C. about 12 days at summer temperatures (18-21°C), Considerable attention has focussed upon the study whereas this degree of reduction took approximately of enteroviruses in estuaries and the associated risk of 28 days during winter and spring (4-15°C). viral disease transmission via contaminated shellfish. Colwell and Kaper (1978) reported viral stability for Metcalf, Wallis and Melnick (1974) reported studies of 322 days at 4°C, whereas at 25°C viruses were rarely pollution of the Houston ship canal (temperature detected after 56 days. These results were unaffected by 10-33°C; salinity 0.1-1.1 percent; fecal coliforms salinity changes in the range 1 to 3.4 percent. Roberts, 6.6-500 x 103 per 100 milliliters) and Galveston Bay Haggerty and Johnson (1976) found that poliovirus 2 (temperature 9-30'C; salinity 1-2.4 percent; fecal suffered an 84-88 percent reduction after 20 days at coliforms <2-330 per 100 milliliters) in Texas (USA). 17°C when held in seawater, estuary water, river water Two activated sludge plants were discharging up to or lake water. Hurst and Gerba (1980) recorded a 99.9 1.7 x l0O enteroviruses per day into the ship canal, and percent reduction of poliovirus 1, echovirus 7, the dominant virus types identified were polioviruses 1 coxsackievirus B3 and simian rotavirus in estuarine and 2 and echovirus 7. In the ship canal, 0.8 kilometers water (temperature 20°C, salinity 1.2-2.8 percent) in downstream from the nearest effluent discharge site, 2-3 days. The rate of inactivation was unrelated to salt enterovirus concentrations were 0.05-0.9 per liter, concentration. The same virus types in clean and whereas 6.4 kilometers further downstream con- polluted freshwater at the same temperature were centrations were 0.08-0.7 per liter. Enteroviruses were reduced by 99.9 percent in 3 to > 14 days. The also isolated from the bottom sediments of the ship unimportance of salinity in determining virus survival canal at concentrations of up to 4 per 100 grams. In has been shown also by Berry and Noton (1976), Galveston Bay, 33 kilometers from the discharge site, Matossian and Garabedian (1967) and Metcalf, Wallis no enteroviruses could be detected in the water, but and Melnick (1974). polioviruses 1 and 2 were isolated from oysters Of particular relevance to recreational hazards are (concentrations up to 26 per 100 grams). Further the findings of Baylor and others (1977), which show examination of 89 poliovirus isolates from the ship that viruses can be transferred from surf to the air and canal and oysters indicated that 8 percent might be blown onto the beach. This is caused by viruses wild, virulent strains. Survival tests in the laboratory adsorbing to air bubbles as they rise through the water. indicated that, in ship canal water at 22°C, poliovirus 1, When they burst at the surface, tiny droplets rich in coxsackievirus B5 and echovirus 7 were eliminated viruses are ejected into the air and are carried on the within 21 days. Further studies in Galveston Bay wind. The concentration of viruses in these droplets (Gerba and others 1979) showed that the con- may be at least 100 times greater than in the seawater ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 143 from which they came. This presents a potential health of enterovirus excretion, are high. Otatume and Addy risk similar to that postulated for aerosol droplets (1975) isolated enteroviruses from 44 percent of 386 produced by activated sludge plants, spray irrigation fecal specimens collected from 45 healthy infants in systems and flush toilets (see the section below on the Accra (Ghana). Virus isolation rates were not affected occurrence and survival of enteroviruses in air). by seasons, were higher in urban (44 percent) than in A number of other studies (for instance, Gerba and rural (21 percent) areas, and were higher among infants others 1977; Hetrick 1978; Metcalf and Stiles 1968; from houses without flush toilets (50 percent) than Pietri and Breittmayer 1976; Shuval 1978; Vaughn and among infants from houses with flush toilets (30 others 1979a) have investigated enteroviruses in percent). Out of 138 typed virus isolates, 12 percent marine and estuarine environments and have reached were poliovirus (presumed to be wild), 4 percent were broadly similar conclusions. Survival in seawater is coxsackieviruses, and the remainder were echoviruses. generally shorter than in freshwater, and a specific In Ibadan (Nigeria) three separate studies showed 39 virucidal property of seawater (possibly of micro- percent of infants excreting enteroviruses or aden- biological origin) has been postulated. The evidence for oviruses (Montefiore and others 1963), 49 percent of this has been reviewed by Kapuscinski and Mitchell children under 3 years excreting enteroviruses other (1980) and Katzenelson (1978). Sunlight may have than polioviruses (Poliomyelitis Commission 1966), some slight virucidal action on viruses suspended near and 45 percent of children between 3 and 24 months the surface. Viruses are found associated with bottom excreting enteroviruses (Peradze, Montefiore and sediments in a greater proportion of samples, and at Coker 1968). In Yaounde (Cameroon), 39 percent of higher concentrations, than in the overlying waters, 524 children age 0-6 years were excreting en- and their survival is prolonged in this state (Gerba and teroviruses, and 11 percent were excreting polioviruses others 1977; LaBelle and Gerba 1979; Smith, Gerba (Boche, Millan and Le Noc 1973). Sabin and others and Melnick 1978; Vaughn and Metcalf 1975). (1960) found that 11 percent of children 1-5 years old Sediment may serve as a reservoir of enteroviruses that in Toluca (Mexico) were excreting wild poliovirus, may be resuspended into the overlying water by wind, while 51 percent were excreting other viruses. Rao, currents, dredging or boats. Lakhe and Waghmare (1978) reported that 45 percent Temperature is the most determining factor in viral of children between 1 and 15 years old in Nagpur survival, with greatly increased inactivation rates in (India) were excreting enteroviruses. These data on the warmer waters (Berry and Noton 1976; Colwell and prevalence of enterovirus excretion among children in Kaper 1978). Few or no data are available on marine Africa, Asia, and Central America show a quite pollution near major tropical coastal towns (Lund remarkable consistency. 1979). However, these towns typically discharge Another gauge of the very high incidence of considerable volumes of untreated or partially treated enterovirus infections among young children in wastes into the sea, and so substantial viral pollution is developing countries is data on the proportion of to be expected. Survival times are probably shorter unvaccinated children having antibodies to poliovirus. than those reported from temperate areas. For instance, John and Jayabal (1972) found that 79 percent of 191 unvaccinated infants and children under Infeces and night soil 5 years old in Vellore (India) had antibodies to one or more types of poliovirus, thus indicating a history of The source of enteroviruses in the environment is the infection. Sabin and others (1960) found that 100 feces of infected individuals, which may contain 106 or percent of children in Toluca (Mexico) developed more viruses per gram. There is extensive information antibodies to one or more polioviruses before the age of on the proportion of people, especially children, 4 years, and that over 90 percent of 4 year olds had excreting enteroviruses at a given time. Little is known antibodies to all three polioviruses. Montefiore and directly about the occurrence of viruses in night soil, others (1963) reported that 100 percent of children over although typical concentrations may be inferred from 3 years in Ibadan (Nigeria)had immunity to poliovirus 1. data on enteroviruses in feces (given here) and in In a subsequent study in Ibadan (Poliomyelitis sewage (given below). Enterovirus survival in feces and Commission 1966), the prevalence of immunity to night soil may be estimated from data on survival in polioviruses 1, 2, and 3 in children between 24 and 36 sludge (see below and the appendixes to Feachem and months old was 68, 48, and 68 percent respectively. others 1980). Studies in Kabul (Afghanistan) showed that over 90 Under conditions of poverty and poor hygiene the percent of unvaccinated children had acquired incidence of enteroviral infections, and the prevalence immunity to polioviruses by the age of 5 and that peak 144 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES transmission occurred in the early summer (Sery and a sewage especially rich in enteroviruses, and reported others 1970; Thraenhart and others 1970). concentrations of enteroviruses will continue to rise as By contrast, enterovirus isolation rates from laboratory techniques improve and as more studies are healthly individuals in industrialized countries are carried out in developing countries. Sewage in much lower. Froeschle, Feorino and Gelfand (1966) developing countries must be assumed to contain at isolated enteroviruses (excluding polioviruses, which least 105 enteroviruses per liter, and sewage effluents they assumed to be vaccine derived) from 4.9 percent of produced by conventional treatment plants will also healthy 1-5 year old children in six cities in the USA. contain high concentrations of enteroviruses (see the Isolation rates peaked in late summer and early fall section below on enterovirus inactivation by sewage with a maximum of 12.4 percent positive in September. treatment processes). Infection rates were higher in males than in females and In an early study of this subject, Bloom and others highest in 1 year olds, with rates decreasing with (1959) investigated the enteroviruses in the sewage of increasing age. Cooney, Hall and Fox (1972) studied Lansing and East Lansing (Michigan, USA) between over 14,000 fecal specimens in Seattle (USA) and found 1955 and 1957. East Lansing sewage yielded en- polioviruses (presumed to be vaccine derived) in 8.8 teroviruses in 14 percent of samples, compared with 7 percent, adenoviruses in 2.2 percent, coxsackieviruses percent in Lansing, which had large volumes of in 0.7 percent, and echoviruses in 0.6 percent. From industrial wastes in its sewage. Peak isolations 18,000 respiratory specimens, polioviruses were isol- occurred during July through November. Thirty-three ated in 0.8 percent, adenoviruses in 0.9 percent, percent of samples of influent at the East Lansing coxsackieviruses in 0.1 percent, and echoviruses in 0.5 activated sludge plant were positive for enteroviruses, percent. Isolation rates were inversely related to age. while only 10 percent of samples of the final effluent In summary, it is clear that enteroviruses spread were positive. vigorously by the fecal-oral route (and possibly also by Haifa (Israel) sewage between 1972 and 1974 the oral-oral route) in conditions of poverty and low contained a monthly average of between 6 x I03 and personal and domestic hygiene. Thus the prevalence of 4.9 x 105 viruses per liter. The highest value recorded enterovirus excretion is high (40-50 percent among was 1 x 106 viruses per liter (Buras 1976). Fattal and infants and young children), as is the prevalence of Nishmi (1977) reported a predominance of po- antibodies to enteroviruses, which indicate past or lioviruses amongst enteroviruses isolated from the current infection. Under conditions of relative sewage of six Israeli towns and found that 13 percent of affluence and optimal hygiene (as in the USA) wild isolated polioviruses were wild strains rather than enteroviruses, and vaccine-derived polioviruses, con- attenuated vaccine strains. By contrast, Katzenelson tinue to circulate in the community and among and Kedmi (1979) reported detecting poliovirus in members of the same family. However, the prevalence only about 50 percent of 25 samples of raw sewage and of enterovirus excretion is very much lower (around 5 sewage effluents in Jerusalem, Tel Aviv and elsewhere percent in young children) than in the developing in Israel. The proportion of polioviruses to all countries. In all countries studied, the prevalence of enteroviruses was low. virus excretion is inversely related to age, so that the In Seattle (USA) Heyward and others (1979) highest virus excretion rates are found among infants. isolated up to 1.3 x I03 viruses per liter from combined As hygiene improves in the absence of vaccination sewer-stormwater overflows. In Ottawa (Canada) programs, the age distribution of infections tends to Sattar and Westwood (1977) detected pathogenic shift upwards, and the amount of clinically serious viruses in 79 percent of sewage samples. Of 72 isolates disease may increase (see, for instance, Anon. 1971, identified, 56 (78 percent) were reoviruses; the Hillis 1979, Metselaar 1968). remaining 16 were enteroviruses. Of the 16 en- teroviruses, 1 was coxsackie, 10 were vaccine strains of In sewage poliovirus, and 5 were wild polioviruses. The authors point out that the presence of these wild strains in Since enteroviruses are not normally excreted for sewage, at a time when immunity against poliovirus is prolonged periods by healthy individuals, their declining due to a fall-off in vaccination, is a cause for occurrence in sewage is subject to wide fluctuations. concern. Fujioka and Loh (1978) isolated en- However, nearly all sewages contain enteroviruses, and teroviruses from 100 percent of raw sewage samples the larger the contributing population the less variable investigated in Hawaii (USA) at concentrations is the concentration of viruses. Communities with poor between 27 and 1.9 x 104 per liter. In the same study, hygiene and a high proportion of children will produce 26 poliovirus isolates were assayed for virulence and 3 ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 145 (all from chlorinated effluent) were found to be wild. enteroviruses per liter (maximum 218 per liter). This Rao, Lakhe and Waghmare (1978) reported virus difference was attributed to the differences in socioecon- concentrations of up to 11,500 per liter in Indian raw omic status and age structure between the two sewage. There was a pronounced diurnal and seasonal communities. Enteroviruses in sewage reflect the levels variation in virus load; maximum concentrations of infection and vaccination within the contributing occurred between 8 and 10 a.m. and during the rainy population and may be used as an aid to epidemiological season. Nearly 80 percent of viruses isolated were surveillance (see, for instance, Zdrazilek, Sramova and polioviruses and 60-80 percent of these were wild Hoffmanova 1977). strains. The authors noted that about 60 percent of Little information is available on the concentration recorded cases of paralytic poliomyelitis cases in India of enteroviruses in tropical sewage. It is to be expected are reported during the rainy season. that poor communities, living in conditions of Virus survival in sewage has been investigated in inadequate hygiene, will produce a sewage with 107 or several studies (see the appendixes of Feachem and more infectious virus units per liter (Lund 1979), others 1980). The results generally indicate longer although, of course, most such communities produce survivals than in river water, with survival times of over no sewage at all because they are not connected to a 231 days at cool temperatures (< 10°C) and up to 110 sewerage system. However, even fairly affluent days at warmer temperatures (20°C). Lefler and Kott communities in developing countries will almost (1975) showed 99.9 percent reduction of poliovirus in certainly produce a sewage with a greater con- sewage, after 42 days at 18-25°C, and after 231 days at centration of pathogenic viruses than in Europe and 4-8°C. Kott, Ben-Ari and Vinokur (1978) reported the North America, because the incidence of viral complete disappearance of enteroviruses in lagooned infections is higher, water use is lower, and a greater trickling filter effluent within 73 days, and the proportion of the population is under 15 years old (see disappearance of poliovirus in oxidation pond effluent the previous section on viruses in feces). at 18-23°C within 110 days (99.9 percent reduction in about 70 days). Rao and others (1977) found up to In sludge 1,250 enteroviruses per liter in Bombay sewage and report that, when stored at 8°C for 2 days, a 22 to 40 The sludges of sewage works are rich in en- percent loss occurred. teroviruses because a high proportion of viruses in Prolonged survival of enteroviruses in sewage may sewage are, or become, solids associated and are be due in part to the protective effects of adsorption to therefore concentrated into both primary and secon- solids. Wellings, Lewis and Mountain (1976) found dary sludges (Lund 1973,1976; Lund and Ronne 1973; that between 16 and 100 percent of viruses in raw Wellings, Lewis and Mountain 1976). It is probable sewage and sewage effluent, at two treatment plants in that most of the difference between the virus Florida (USA), were solids associated. Gerba, Stagg concentration of the influent and the effluent of a and Abadie (1978) reported that 3 to 49 percent of sewage treatment plant is accounted for by the viruses viruses were solids associated in treatment plant in the sludge. The few studies on virus survival in sludge effluents near Houston (Texas, USA). are listed in the appendixes to Feachem and others In a unique study Ruiter and Fujioka (1978) (1980). investigated the sewage produced by two communities Subrahmanyan (1977) studied the survival of several in Honolulu (Hawaii, USA). Kuhio Park Terrace had a types of enteroviruses added to sewage sludge at a total population of 2,745, of whom 46 percent were concentration of 107 per liter and kept at 22°C. children under 14 years. The density of settlement was Survival times ranged from a minimum of 2 weeks 376 persons per hectare, 73 percent of households had (coxsackievirus A9) to a maximum of over 12 weeks an income of under US$5,000 per year, and 23 percent (coxsackievirus B5 and echovirus 9). Polioviruses of heads of household were unskilled laborers. Nuuanu survived from 8 to 12 weeks. Damgaard-Larsen and had a total population of 2,302, of whom 10 percent others (1977) inoculated digested and dewatered were children under 10 years. The density of settlement sludge with coxsackievirus B3 at a concentration of 106 was only 19 persons per hectare, 4 percent of per gram. The sludge was applied outdoors in households had an income of under US$5,000 per year, Denmark to sandy and clay soils during December to and 4 percent of household heads were unskilled May, when rainfall totalled 300 millimeters and laborers. Kuhio Park Terrace produced a sewage with temperatures ranged from -12 to 260C. Virus an average of 345 enteroviruses per liter (maximum 820 inactivation took place at a rate of about 1 log unit per per liter), while Nuuanu produced an average 93 month, and it took 23 weeks before viruses could not be 146 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES detected. Viruses remained bound to the sludge and by low temperatures but was unaffected by whether the did not travel downward through the soil. Nielsen and soil was wetted with distilled water or with various Lydholm (1980) reported the survival of naturally concentrations of sewage effluent. Virus inactivation occurring coxsackievirus B5 for 4 months occurred much more rapidly under nonsterile aerobic (March-July) in digested sludge applied to land in conditions than under sterile aerobic conditions or Denmark. under sterile and nonsterile anaerobic conditions. Sattar and Westwood (1979) studied the viruses Duboise, Moore and Sagik (1976) found that present in raw sludge (5 percent solids), anaerobically polioviruses held for 84 days in loamy sand were digested sludge (20 days at 35°C), and lagoon-dried reduced by less than 90 percent at 4°C but by 99.999 sludge (minimum of 6 months drying time) from the percent at 20°C. In studies into the disposal of septic largest sewage treatment plant in Ottawa (Canada). tank effluent it was found that poliovirus 1 adsorbed to Excreted viruses were isolated from 84 percent of raw sandy soils was reduced by 97.5 percent after 28 days at sludge samples, 53 percent of digested sludge samples, 20°C and by less than 50 percent after 56 days at 7°C and 39 percent of dried sludge samples. Viruses were (Small Scale Waste Management Project 1978). isolated from sludge that had been drying for over 8 Lefler and Kott (1974a) studied the survival of months. Most virus isolates were reoviruses, the poliovirus 1 in sand kept in the dark at room remainder being enteroviruses. temperature (18-22°C). With the sand saturated in Hurst and others (1978) isolated viruses from distilled water, no poliovirus was detected after 112 various activated sludge samples at a sewage treatment days, and 99 percent inactivation was achieved in plant at Houston (Texas, USA) in concentrations of about 63 days. With tap water or oxidation pond around 30 viruses per liter of sludge. After sludge effluent, complete inactivation took 105 days, while 99 thickening, aerobic digestion and centrifugation the percent reduction took 42 days. Coliphage f2 survived concentration of viruses rose to 231 per liter. This for longer than poliovirus 1. When the saturated sand sludge was then applied to land, where the virus was kept at 4-8°C, 20 percent of poliovirus was still concentration was monitored over two separate active after 175 days. On dried sand at 4-8°C, 96 periods. During the first 7 day period (during percent inactivation occurred in 21 days and virus was September with no rain), the solids content of the still detectable (at 0.02 percent of the original sludge rose from 6.9 to 18.4 percent, and 97 percent of concentration) after 77 days. the viruses were inactivated. During the second 7 day Tiemey, Sullivan and Larkin (1977) inoculated period (during September with rain on day 6), the poliovirus 1 into samples of activated sludge and solids content of the sludge stayed almost constant at secondary effluent to produce a viral concentration of 13-14 percent, and 99.5 percent of the viruses were 2.5 x 108 viruses per liter. The fluids were sprayed over inactivated. A sample of sludge which had been on the soil plots so as to flood them to a depth of 25 field for 3 months had a solids content of 59 percent millimeters. Runoff water from the plots contained 106 and no demonstrable virus. Thus in a Texas summer a viruses per liter on the day of flooding but this fell to 0 2 log reduction per week was recorded, compared with by day 6. In winter (- 14 to 27°C) viruses applied in a unit log reduction per month during a Danish winter effluent survived in soil for between 89 and 96 days, (Damgaard-Larsen and others 1977). whereas viruses applied in sludge survived between 96 and 123 days. In early summer (19°C to 34°C), viruses In soil were not detected for more than 11 days after flooding with either effluent or sludge. Increased interest in the health aspects of the Yeager and O'Brien (1979a) elucidated several agricultural use of sewage and sludge has generated aspects of virus survival in soil. They found that several studies on virus survival in soil. However, little poliovirus survival was heavily temperature de- information is yet available. More is known about pendent, with virus survival in saturated soil being up virus travel and adsorption in soils, and this subject is to 12 days at 37°C, up to 92 days at 22°C, and up to 180 reviewed below in the section dealing with land days at 4°C. Viruses survived longer in soils saturated treatment. with septic tank liquor (90 percent reduction in 8-21 A review by Gerba, Wallis and Melnick (1975a), and days at 22°C) than in soils saturated with river or the studies listed in the appendixes to Feachem and groundwater (90 percent reduction in 5-7 days at others (1980), indicate that survival times of over 175 22°C). Viruses survived for longer in sandy loam (90 days are possible. Hurst, Gerba and Lance (1979) percent reduction in 6-21 days at 22°C) than in sand found that enterovirus survival in soil was prolonged (90 percent reduction in 4-8 days at 22°C). Soil drying ENTEROVIRUSES. POLIOMYFLITIS. AND SIMILAR INFECTIONS 147 was found to be highly virucidal, irrespective of soil the survival of various viruses on strawberries, cherries, type, and speed of soil drying depended on and peaches at 4°C and investigated the effect of temperature. Soil moistures of below 2.9 percent inoculating the viruses in water or in dilute feces and of appeared to be especially virucidal. In an accompany- storing the fruit in humid or dry atmospheres. Viruses ing study (Yeager and O'Brien 1979b) the same were inactivated far more rapidly under dry than under authors investigated the nature of virus inactivation in humid conditions, and virus survival was prolonged by soil. They concluded that loss of infectivity is due to inoculation in feces rather than in water. Viruses irreversible damage to the virus particles. They survived longer on cherries and peaches than on speculate that two general mechanisms may underly strawberries, and coxsackieviruses and echoviruses the inactivation of picornaviruses in the environment: survived for longer than polioviruses and reoviruses. under temperate, saturated conditions RNA de- Under dry conditions survival of viruses was between gradation may occur, whereas in dried soil (and also 40 and < 1 percent after 1-2 days, and viruses were perhaps in aerosols and under a variety of hostile undetectable after 4-6 days. The short survival times circumstances such as heat, irradiation and de- are notable in view of the cool temperature (4°C), and siccation) the virions may dissociate into intact RNA the authors consider that an antiviral substance and isoelectrically altered capsids (see also O'Brien and produced by the fruit is active. The authors also Dacus 1978). consider that the longer survival of viruses inoculated Virus survival in soil depends upon many factors in dilute feces is due to delayed desiccation as including the type of soil, its pH, the sterility of the soil, compared with viruses inoculated in water. and the type of liquid in which the viruses are applied. Subsequently, the same authors (Konowalchuk and However, temperature and moisture appear to be the Speirs 1977) reported that the concentration of dominant factors. While very long virus survival times poliovirus 1 and coxsackievirus B5 was reduced by (over 5 months) are possible at cool temperatures about 99 percent after 5 days on grape bunches hung (< 10°C), at warmer temperatures (> 25°C) viruses are indoors at 22°C. likely to be eliminated within 2 weeks. Soil drying is Kott and Fishelson (1974) investigated the effect of also highly virucidal, and the evidence suggests that, in effluent chlorination and sunlight on the survival of warm climates, intermittent agricultural application of seeded poliovirus 1 on tomatoes and parsley. The sewage, night soil or sludge, with drying periods of 3-5 maximum recoveries of polioviruses from vegetables 6 days between applications, would result in little or no hours after application in waste stabilization pond build-up of viable pathogenic viruses in the soil. This effluent were: 2.2 percent when applied in un- contention is further supported by the studies of chlorinated effluent with exposure to sunlight, 1.6 Sadovski and others (1978)-reported in the next percent when applied in chlorinated effluent with subsection, concerning viruses on crops. exposure to sunlight, 12.7 percent when applied in unchlorinated effluent and kept in darkness, and 8.5 percent when applied in chlorinated effluent and kept On crops in darkness. Poliovirus applied outdoors did not survive for more than 1 day on tomatoes or 2 days on The interest in virus survival in soil has been parsley at 15-31°C. Poliovirus survival was con- accompanied by interest in virus occurrence and siderably prolonged when viruses were applied in survival on vegetables fertilized or irrigated with sludge phosphate-buffered saline rather than effluent. or sewage. Larkin, Tierney and Sullivan (1976) planted lettuces Konowalchuk and Speirs (1975a) studied virus and radishes and, 8-10 days later, sprayed them with survival on vegetables stored at 4°C. In a humid secondary effluent or sludge seeded with 2.5 x 108 atmosphere, coxsackievirus, poliovirus, echovirus, polioviruses per liter. These experiments were con- reovirus, and adenovirus inoculated in a water droplet ducted in Ohio (USA) in the summer of 1973 and 1974 onto lettuce, celery, green peppers, tomatoes, radish, when there was extensive direct sunlight, periodic rain, and carrots were undetectable after 4-5 days. When air temperatures of 19-340C, and soil surface inoculated in dilute feces, 4-5 percent were detectable temperatures rising to 45°C. On the days immediately after 5 days; when inoculated in feces, 7-12 percent after spraying, large amounts of virus (up to 2.9 x 104 were detectable after the same time. Additional studies per 100 grams) could be recovered from the vegetables. on virus survival in vegetable infusions indicated that Two weeks after spraying no more than 100 viruses per the vegetables contained no antiviral agents. In a later 100 grams could be detected, and small numbers (10 study Konowalchuk and Speirs (1975b) investigated per 100 grams) persisted for at least 36 days. In similar 148 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES studies, Tierney, Sullivan and Larkin (1977) were still Feachem and others (1980)4, indicate highly variable able to isolate 60 polioviruses per 100 grams of lettuce survival times for enteroviruses on vegetables and fruit. 23 days after spraying. (Lettuces and radishes in this Type of virus and type of crop are clearly important, climate are normally harvested 3 to 4 weeks after but the dominant factors are temperature, sunlight and planting.) humidity (which will control the degree of warming), Sadovski and others (1978) studied the survival of and radiation and desiccation experienced by the polioviruses inoculated into waste stabilization pond viruses. Survival times of up to 2 months are possible, effluents and applied by drip irrigation to cucumber but at day temperatures above 25°C (and especially in plots on two farms in Israel. At one site (air dry climates) one may anticipate negligible survival of temperature 13-30°C, soil temperature at noon enteroviruses on crops for more than 2 weeks. Indeed, 22-30°C, sunlight 9.5 hours per day, relative humidity it may be that almost complete elimination will occur 27-55 percent), a single irrigation was performed with in under 5 days and that the longer survival times inoculated effluent containing 9 x 107 polioviruses per reported by some investigators are only achieved by liter. Viruses were still detectable in the irrigation the untypically high concentration of seeded en- system, at a concentration of > 104 per liter, 8 days terovirus in the applied effluent [for instance Larkin, after the flow of inoculated effluent. The soil Tierney and Sullivan (1976) employed 2.5 x 108 contamination immediately after irrigation with polioviruses per liter, and Sadovski and others (1978) inoculated effluent was l04viruses per 100 grams ofsoil had 2.2 x 1012 per liter]. It has been clearly (dry weight) and persisted at a level of > 103 per 100 demonstrated by Israeli workers that drip irrigation, grams for at least 8 days. Cucumbers grown in exposed particularly when combined with soil covered with soil were contaminated by 2.2 x 103 viruses per 100 plastic sheets, is a method of effluent application that grams immediately following irrigation, and this minimizes the risks of crop contamination by contamination fell to 30 per 100 grams on day 8. enteroviruses. However, when the soil and drip lines were covered with plastic sheets no viruses could be isolated from the I cucumbers after a few hours had elapsed after Infshand .1o,!/ti .',' inoculated irrigation. At the second site (air tempera- The primary hazard associated with estuarine and ture 23-28°C, soil temperature at noon 40-43°C, marine discharge of fecal wastes may not be risks to sunlight 11.8 hours per day, relative humidity 62-70 bathers and water sportsmen but to those who eat the percent), three irrigations were performed with fish and shellfish that are harvested in polluted waters. inoculated effluent containing 2.2 x 1012 polioviruses The greatest risks of viral infection are associated with per liter. After the third inoculated irrigation the soil the ingestion of contaminated molluscs (such as contained 9.1 x 103 viruses per 100 grams (dry oysters, mussels, cockles, and clams) and crustacea weight), and this contamination fell to 47 per 100 (such as crabs, lobsters, shrimps, and prawns) in a raw grams after 10 days and to O after 15 days. Unlike at the or partially cooked state. Most attention has focussed first site, where irrigation with uninoculated effluent upon oysters because they are commonly eaten raw had continued throughout the study, in this case and their method of filter feeding (common to all irrigation terminated 5 days after the third inoculated bivalve molluscs) concentrates pathogenic organisms irrigation, and consequently the soil moisture content from the water into their tissues (Anon. 1976; Gerba fell from 15 to 3 percent. Virus contamination of the and Goyal 1978; Hughes, Merson and Gangarosa cucumbers grown in exposed soil rose to 0.13 per 100 1977; Metcalf 1978; Wood 1979). Attention has also grams, but was undetectable 6 days after the last been paid to improved laboratory techniques for inoculated irrigation. In covered soil no viral isolating enteroviruses from shellfish (Gerba and contamination of the vegetables could be detected. At Goyal 1978; Metcalf 1978; Vaughn and others 1979b). both sites, virus survival in the soil was unaffected by Mitchell and others (1966) placed 600 eastern whether plastic sheets were lain over the soil and the oysters (Crcassostrea virginica) in seawater at 20°C drip lines. Earlier studies at the first site by the same containing 106 polioviruses per liter and found that workers (Sadovski, Fattal and Goldberg 1978) showed viruses rapidly accumulated in the oyster tissue such that no viruses could be isolated from cucumber or that after 1 hour the virus concentration in the oyster eggplants drip-irrigated with uninoculated waste was 27 times higher than in the surrounding water. stabilization pond effluent containing 103 entero- viruses per liter. 4. See also Engley (1956) and Berg (1978b) for reviews of literature These studies, and others listed in the appendixes of on virus survival in food (as opposed to on cropsJ. ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 149 When the seawater contained 3 x 105 polioviruses per harvesting waters in Galveston Bay (Texas, USA). Of a liter, viruses accumulated less rapidly but were always total of 44 water samples, 26 yielded viruses in concentrated in the oyster by at least 10-fold after 3 concentrations of up to 0.4 per liter, whereas of 40 hours. When the oysters were rinsed and placed in pools of 10 to 12 oysters each, viruses were isolated sterilized seawater, over 95 percent and 99.9 percent of from 14 pools at concentrations of up to 224 per 100 viruses were eliminated after 8 and 24 hours grams. On five occasions viruses were found in oysters respectively. Viruses were sometimes undetectable but not in the overlying waters. Gerba and Goyal after 48 hours and sometimes detectable in very small (1978) reviewed 17 reported isolations of viruses from numbers (2 per gram) for up to 96 hours. shellfish. Hoff and Becker (1969) studied the accumulation of It is generally agreed that no human enterovirus poliovirus by the Olympia oyster, the Pacific oyster, multiplication takes place in shellfish (Chang and and the Manila clam and found that these species others 1971) and that the dangers lie in the uptake, concentrated the virus to a level between 10 and 180 concentration, and survival of viruses in shellfish tissue. times higher than in the surrounding waters. When the Uptake, depuration, and survival in oysters has been contaminated shellfish were held in disinfected found to be temperature dependent. Below a given seawater (6-16°C), poliovirus concentrations in the temperature, a particular species of shellfish will cease meat were reduced by at least 99.9 percent after 96 to filter. The European flat oyster (Ostrea edulis) hours. Hedstrom and Lycke (1964) found that appears to filter at temperatures down to 5°C, whereas poliovirus survived for 3.5 days in seawater but for well the eastern oyster (Crassostrea 0irginica) will not filter over 6 days in oysters in contaminated seawater. below 7°C. The edible mussel (Mytilus edulis) filters at Oysters did not cleanse themselves of poliovirus within temperatures down to 2°C, but the hard clam 22 hours when transferred to uninfected water or to (Mercenaria mercenaria) ceases active filtration at water containing up to 1.7 milligrams per liter of free about 12°C (Metcalf and Stiles 1968; Wood 1979). As chlorine. the temperature falls, the rate of filter feeding declines DiGirolamo, Liston and Matches (1975) placed and so does the rate of accumulation of viruses. Below oysters in seawater (salinity 2.8 percent, temperature the critical temperatures mentioned above, virus 13°C) containing 1.9 x 107 polioviruses per liter and accumulation should cease. The same is true of found that after 2 days the oysters had accumulated depuration, and so a contaminated shellfish will about 104 polioviruses per gram of meat. Most viruses cleanse itself more slowly as temperature falls and will were concentrated in the digestive organs and feces. cease to cleanse itself at all below a critical temperature. When placed in stationary sterilized seawater (salinity Survival of viruses in stored shellfish is very much 2.8 percent, temperature 13°C), contaminated oysters prolonged by low temperatures. Vaughn and Metcalf lost between 79 and 84 percent of polioviruses in 5 (1975) reported that coxsackievirus B3 in oysters days. When placed in flowing sterile seawater, oysters survived for up to 42 days at 1-11°C, but for only 22 lost over 99 percent of accumulated poliovirus after 3 days at 14-21°C. Metcalf and Stiles (1965) found that days. Gerba and Goyal (1978) reviewed 17 other viruses in oysters stored at 5°C remained relatively studies on the accumulation and depuration of stable for at least 28 days. DiGirolamo, Liston and excreted viruses by shellfish. Matches (1970) found that 10 percent of polioviruses The isolation of enteroviruses from oysters living in survived for 84 days in oysters after freezing at - 36°C lightly contaminated waters has been frequently and storage at - 17.5°C. DiGirolamo and Daley reported. Metcalf and Stiles (1965) isolated coxsackie (1973) froze crabs at -20°C and found that 17-35 B4 and echo 9 viruses from oysters in estuary waters at percent of seeded coliphage T4 survived after 30 days. distances of up to 4 miles from the nearest sewage Other studies of viruses in refrigerated shellfish have outlet. Vaughn and Metcalf (1975) found that 7.6 shown that survival times of up to 120 days are possible percent of oyster samples contained enteroviruses in (Gerba and Goyal 1978). waters from which only 5.6 percent of samples were These and many other studies (reviewed in Gerba and positive for viruses. Vaughn and others (1979a) Goyal 1978) show that viruses in water are readily isolated up to 30 viruses per 100 grams of flesh from accumulated by shellfish. In edible bivalve molluscs clams in Great South Bay (New York, USA), the (clams, mussels, oysters) the viruses are concentrated waters from which contained no more than 2 viruses mainly in the digestive system and may be present in per liter. concentrations over 100-fold higher than in the Goyal, Gerba and Melnick (1979) studied the surrounding waters. This is because these shellfish are presence of enteroviruses in oysters and oyster- filter feeders, and one oyster may filter as much as 1,500 150 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES liters of seawater per day in its quest for food. Crustacea In the air that inhabit polluted waters or that feed on Airborne droplets of water and wastewater may contaminated molluscs may also accumulate en- contain enteroviruses, and these viruses may cause teroviruses, although less work has been done on this, infection when inhaled. Droplets containing viruses DiGirolamo and others (1972a) showed that crabs kept m in contaminated seawater for 2 days at lO°C, or allowed may be formed by the flushing of a toilet, by spray to feed on contaminated mussels for 12 hours, irrigation, or by any occasion in which bubbles are tocumufeted onrcontamoina ussels for 12 hours, rising through contaminated waters and bursting at Depuration or cleansing of viruses from shellfish is a the surface (such as activated sludge plants, waves and Deph a ti on p or leasin g of res filr or sheli sh is a surf, or the passage of boats). As a bubble rises through mechanical process induced by the filter feeding of the wtrvrssbcm dobdt t ufc h mollusc in clean water. Maximum depuration occurs water, viruses become adsorbed to its surface. The when feeding activit is.greatest.This bubble bursting at the surface ejects a tiny jet of water when feeding activity is greatest. Thus, cleansing thtbek1nomnSrplt,adteedolt more rapid at warmer temperatures, at optimal that breaks mto many droplets, and these droplets s ies rand in flowi n water.epuat o ftim contain most of the viruses that were adsorbed to the salInities, and in flowing water. Depuration of bubble. Thus the droplets contain a much higher commercially harvested oysters by placing them in concentration of viruses than the water from which clean water is practiced. Chlorination of the water to came. maintain its purity has been advocated, but this is Bey came. .. ... .. ,.' , ...... Baylor, Peters and Baylor (1977) bubbled air antagonistic to the oyster, inhibits feeding, and thus through a column of liquid containing coliphages T2 delays depuration. Preliminary experiments have been and T4 and produced droplets that contained a conducted on virus removal from contaminated conduted prion virus taqcuuremoa from adsorintminted t concentration of phage 50 times that in the column. seawater prior to aquaculture by adsorbing viruses to Baylor and others (1977) seeded the breaking surf with magnetite and removing them in a magnetic field coliphages T2 and T4 at beaches near New York. (Bitton and others 1977). Droplets were formed in the surf that contained a When contaminated shellfish reach the market, the concentration of phages 100 to 250 times higher than risks are obviously greatest if they are eaten raw. the seawater, and these droplets were carried by the However, a residual risk remains even with cooked the forwateand m ets. shellfish. Studies have shown that a proportion of wi o at least 30 meters. . * r. r ~The aerosohized excreted viruses most encountered polioviruses in oysters survived stewing (after 8 by people in developed countries are those produced minutes, 10 percent survived), frying (after 10 minutes, by the flush toilets in their houses. Gerba, Wallis and 13 percent survived), baking (20 minutes, 13 percent Melnick (1975b) seeded 108 polioviruses into a toilet survived), steaming (30 minutes, 7 percent survived), bowl and found that flushing ejected at least 2.8 x 103 and irradiation (4 kilogray,5 7-13 percent survived) infectious units to the level of the seat. Further and that up to 20 percent of coliphage T4 in crabs experiments with seeded coliphage MS2 showed that survived boiling (DiGirolamo, Liston and Matches survived boiling (DiGirolamoand Listhers 1972b. Mthese organisms remain airborne long enough to settle 1970, 1972; DiGirolamo and others 1972b). out in large numbers on surfaces throughout the Nearly all the documented disease outbreaks bathroom, and presumably also to be inhaled by associated with excreted virus contamination of people in the bathroom. In an unventilated bathroom, shellfish are outbreaks of hepatitis A (see chapter 10) or 94 percent of recovered coliphage had settled out viral gastroenteritis (see chapter 11). These outbreaks within 2 hours of the flush, and most of the remainder have been reviewed by Gerba and Goyal (1978) and had settled within 4 hours. Small numbers of viruses Levin (1978). However, as reported above. most studies on viruses in shellfish have focussed on the ould apparently remain airborne for much longer. enteroviruses because it is for these viruses that well- Fanmno and others (1977) studied airborne viruses developed laboratory isolation methods exist. Before produced by a trickling filter plant and an activated A. sludge plant in Michigan (USA). The naturally the development of isolation techniques for hepatitis A occurring level of animal viruses in sewage at the virus and rotavirus, it must be assumed that these trickling filter and activated sludge units was 100 per viruses behave in shellfish similarly to the en- liter, while the coliphage concentration was 5 x 105 per liter. No animal viruses were recovered from air samples at the plants,-but coliphage was recovered at concentrations up to 0.5 per cubic meter of air. 5. The Si unit ofradiation dose is the Grav' Gy), which is equal to Airborne coliphage recovery was correlated with 100 rads and is the equivalent of 1 joule per kilogram. relative humidity (higher humidity associated with ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 151 higher recovery) but was not correlated with wind Inactivation by Sewage Treatment speed or ambient temperature (see also Cochran and Processes Fannin 1976 and Fannin and others 1976). Earlier laboratory studies by de Jong and Winkler (1968) had The realization that raw sewage is rich in pathogenic shown that the inactivation of poliovirus 1 during viruses, and recent advances in laboratory techniques spraying was greatest at low humidities. (for instance, Lydholm and Nielsen 1980), have given Sorber, Schaub and Bausum (1974) developed a rise to many investigations into the effectiveness of theoretical model of the transmission of viruses in various treatment processes in reducing viral con- aerosols produced by spray irrigation with effluents centrations in sewage effluents. These studies have containing various enterovirus concentrations. The almost exclusively examined the removal of en- model indicates that a healthy young male working at teroviruses and coliphages, and these two groups of the wetted perimeter when strong effluent (6,000 viruses do not always behave in a similar way (nor may viruses per liter) is being sprayed may inhale as many they be good models for rotavirus or hepatitis A virus). as 240 viruses in 10 minutes; whereas if he is working Several reviews have been published (for instance Berg 200 meters from the wetted perimeter when weak 1973; Sproul 1976; WHO 1979). effluent (10 viruses per liter) is being sprayed, he may inhale only 0.0006 viruses in 10 minutes. These findings dependupon ssumpions mde abut clmatic By primary and seco7ndary sedimentation depend upon assumptions made about clitnatic conditions. The authors conclude that spray irrigation Primary sedimentation tanks, with retention times with chlorinated effluents from conventional treatment of 2-6 hours, allow a proportion of the viruses in the plants poses considerable risk of virus inhalation and sewage to adsorb onto solids and settle. Many viruses that better virus removal systems need to be applied will already be adsorbed to settleable solids in the prior to spray irrigation. influent. Removals reported in the literature, listed in Moore, Sagik and Sorber (1979) were able to isolate the appendixes of Feachem and others (1980), suggest small numbers of coliphages (up to 1.5 per cubic meter between 0 and 83 percent removal from influent to of air) and enteroviruses (up to 1.7 x 102 per cubic effluent. meter of air) from large volumes of air sampled 50 Rao and others (1977) recorded a 24 to 33 percent meters downwind of the wet-line edge of a wastewater removal of enteroviruses by primary settling tanks in spray irrigation site in California (USA). Teltsch and the wet season in Bombay. At other times of the year Katzenelson (1978) isolated echoviruses from 4 out of removal was between 41 and 83 percent with a 2-hour 12 air samples collected 40 meters downwind of retention time. Rao, Lakhe and Waghmare (1978) wastewater sprinklers in Israel. Bausum, Schaub and reported a 50 percent reduction of viruses in a pilot Kenyon (1978) studied a spray-irrigated golf course in plant settling tank at Nagpur (India). Sherman and Arizona (USA) and isolated seeded coliphage f2 from others (1975) and Naparstek and others (1976) studied aerosol droplets 563 meters downwind of sprinklers removal of seeded coliphage f2 in treatment plants in delivering secondary effluent and 137 meters dow- Maryland (USA) and found 35-47 percent average nwind of sprinklers delivering chlorinated effluent. removals in primary sedimentation tanks and 30 The possibility of virus transmission via aerosol percent removal during secondary sedimentation. One droplets will undoubtedly be the subject of a report suggests that factors other than settlement may considerable amount of research over the next few be operative in removing viruses from sedimentation years. Attention will focus upon risks to workers at tank effluent (Clarke and others 1961). sewage treatment facilities and at agricultural sites Similar performance may be expected from secon- employing spray irrigation with wastewater. A study dary sedimentation tanks, except that these are often from Israel (Katzenelson, Buium and Shuval 1976) designed with higher overflow rates. The sludge showed that the populations of kibbutzim that removed from sedimentation tanks will normally practiced spray irrigation with waste stabilization contain a 10-100 times higher concentration of pond effluent had a higher incidence of hepatitis A enteroviruses than the raw sewage. infection than kibbutzim in which no form of wastewater irrigation was used. However, it is most unlikely that transmission by aerosol droplets plays By storage any major part in the maintenance of endemic Storage is an effective method of virus inactivation, enteroviral infections in poor communities where basic especially at temperatures above 20'C. In any storage hygienic facilities are lacking. vessel, some sedimentation will also be taking place 152 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES that will remove a proportion of viruses to the sludge sludge treatment). The inactivation of enteroviruses, layer. Expected removal rates in stored sewage may both in sludge within the septic tank and in the be derived from the data given above on the survival of drainfield, will be considerably enhanced by warm enteroviruses in sewage (see also the appendixes of temperatures. Feachem and others 1980), although little is known about survival under tropical climatic conditions. Bv tricklingfilters By septic tanks The basic mechanism for virus removal by trickling filter plants is adsorption onto the biological slime, Removal of enteroviruses by septic tanks has been retention times are too brief for other processes to be very little studied, and not at all in developing significant. However, reported removal rates are low, countries. A septic tank is simply a settling chamber (or and this suggests that there is poor contact between chambers) with a mean retention time of 3 days or less. viruses and slime surface, that adsorbed viruses are In poorly designed tanks, or those requiring desludg- subsequently eluted by the flow of sewage passing ing, there is very considerable carryover of solids into through the filter, or both. the effluent. Viruses will be removed both by Sherman and others (1975) found that 9 percent and inactivation in the anaerobic liquor and by adsorption 19 percent of seeded coliphage 2 were removed by the to solids that settle to the sludge layer. Some studies of trickling filter beds in two treatment plants. When enterovirus removal have been conducted, and primary sedimentation trickling filters and secondary estimates may also be derived from information on sedimentation were considered together, coliphage survival in sewage and on removal by primary removals were 55 percent and 64 percent. Buras (1976) sedimentation (see the appendixes to Feachem and studied the performance of the Haifa (Israel) trickling others 1980). A series of laboratory experiments filter plant over a two year period. Average influent showed that a 99 percent reduction of poliovirus 1 in biochemical oxygen demand by the standard test septic tank effluent took 14 days at 20°C and 43 days at (ROD5) was 500 milligrams per liter, while average 7°C (Small Scale Waste Management Project 1978). effluent BOD5 was 70 milligrams per liter. The monthly Therefore, if all influent was held for 3 days at 20°C average enterovirus concentrations in the influent (because of short circuiting, it never is). a 64 percent varied between 6 x 103 per liter and 4.9 x 105 per liter, virus reduction might be expected. In practice, with a 2-year mean of the monthly means of 1.3 x 105 enterovirus reductions of 50 percent and under are to per liter. The monthly average concentrations in the be expected. Septic tanks usually serve small effluent varied between 3 x 103 per liter and 4.5 x I05 populations (5-200 people), and so influent and per liter, with a 2-year mean of the monthly means of effluent virus concentrations will fluctuate dramati- 9.6 x 104 per liter. An overall removal efficiency of cally. only 26 percent is derived. Kott, Ben-Ari and Vinokur The ultimate fate of viruses entering a septic tank (1978) isolated between 2.4 x 103 and 1.2 x 104 depends on the disposal of the effluent and the sludge. enteroviruses per liter of trickling filter plant effluent at Effluents are normally discharged to drainfields, where Haifa. viruses may be retained and inactivated in the soil. Clarke and Chang (1975) studied the performance of Cliver, Green and Bouma (1975) reported that septic bench-scale, rotary-tube trickling filters. At medium tank effluent (containing 109 seeded polioviruses per filtration rates poliovirus 1, echovirus 12, and liter) was rendered virus free after travelling 0.4 meters coxsackievirus A9 were reduced by 85, 83, and 94 through sand. with an application rate of 0.05 cubic percent, respectively. At higher filtration rates re- meters per square meter per day at 20°C. Higher movals were 59, 63, and 81 percent, respectively. The application rates or lower temperatures greatly authors failed to disassociate viruses from the reduced virus removal. This and other studies relevant biological slime in the filters and concluded that either to enterovirus removal from septic tank effluent have the slime-virus complex is very stable or that the virus been recently reviewed in detail (Small Scale Waste is somehow inactivated by adsorption to the slime. Management Project 1978). More information on Fecal coliform and fecal streptococci removal rates virus removal by sand and soil is given in the closely paralleled those for enteroviruses and lead the subsections below on filtration and land treatment. authors to suggest that these bacteria may be used as Septic tank sludge will be rich in accumulated indexes of viral removal by trickling filters. Gerba, enteroviruses and requires treatment by digestion, Stagg and Abadie (1978) investigated the association drying or composting (see the subsections below on with solids of enteroviruses in the effluent of a trickling ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 153 filter plant in Houston (Texas, USA). Between 9 and Since retention times in activated sludge plants are 196 enteroviruses per liter were contained in the short (typically 6-12 hours), it is to be expected that effluent, and between 3 and 20 percent of these were most removal of virus is by adsorption to flocs that are adsorbed onto solids. This is a much lower solids- subsequently removed by sedimentation. Glass and associated proportion than that reported by the same O'Brien (1980) calculated that the inactivation rate of authors for activated sludge effluent (49 to 100 percent) enteroviruses in activated sludge mixed liquor at 25°C and supports the contention that the poor virus was about 12 percent per hour. Therefore, in an removal efficiency of trickling filters is due to the activated sludge tank with a mean retention of 9 hours, system's providing insufficient opportunity for virus only 68 percent virus removal would be obtained by adsorption to solids or slime. inactivation even if all liquor were retained for the Few data are reported on the removal of mean retention time. enteroviruses by trickling filters in developing count- Moore and others (1974) studied a contact ries. Nupen (1970) reported that the trickling filter stabilization plant (contact time of 20-30 minutes plant (together with primary and secondary sedimen- followed by a 4-hour stabilization period) near Austin tation) at Windhoek (Namibia) reduced an influent (Texas, USA). Incoming enterovirus concentrations concentration of 2 x 104 viruses per liter by 82 percent. were 250-1,500 per liter. Between 80 and 90 percent of In a subsequent report (Nupen, Bateman and enteroviruses became solids associated in the mixed McKenny 1974) it was stated that the outflow from the liquor, and overall removal varied from 80 to 90 primary sedimentation tanks at Windhoek contained percent. In subsequent laboratory studies it was found 7 x 104 viruses per liter and that, following trickling that 99 percent of poliovirus in mixed liquor became filtration and secondary sedimentation, this was solids associated after 1 hour's aeration. The same reduced by 70 percent in winter and by 95 percent in authors (Malina and others 1974) also reported summer. laboratory model studies on seeded poliovirus removal Removal rates reported in the literature listed in the by activated sludge and contact stabilization processes. appendixes of Feachem and others (1980) vary Poliovirus removals by the activated sludge model between 0 and 95 percent. It is not always clear from were 92-99.9 percent and were not especially sensitive the literature whether removal in the trickling filter to changes in aeration time (range of 5-15 hours) or to alone, or across the whole treatment plant, are being mixed liquor suspended solids concentration (range of recorded. Predictably, removal achieved in laboratory 1940-2710 milligrams per liter). Poliovirus removal models (for instance Clarke and Chang 1975) is far was also not affected by whether pure oxygen or higher than that achieved in practice (for instance, compressed air was used. Contact stabilization Buras 1976), and removal is reduced at higher loading (contact time of 16-32 minutes followed by 2.1 hours rates. A typical removal rate for a trickling filter unit stabilization period) removed 84-99.8 percent of alone might be 5 to 20 percent, whereas a complete poliovirus. Sludges, from both the activated sludge and trickling filter plant (with no tertiary processes) could contact stabilization models, contained between 70 be expected to remove 25-60 percent of enteroviruses. and 5,800 enteroviruses per gram. Many of the viruses removed from the sewage will be Balluz, Jones and Butler (1977) studied a concentrated into the primary and secondary sludges. laboratory-scale activated sludge plant that received raw settled sewage from Guildford (UK) with a mean BOD5 of 270 milligrams per liter and produced an By activated sludge effluent with a mean BOD5 of 11 milligrams per liter. The temperature was 15°C. An average poliovirus The most significant variables in the removal of removal of 99.8 percent was recorded, with 85 percent enteroviruses from activated sludge effluent are of virus associated with the solids fraction of the mixed temperature, retention time (Heyward and others liquor. The authors stress that the efficiency of the 1977; Malina and others 1975), the degree of plant in removing viruses may be closely related to the adsorption of viruses onto activated sludge flocs ability to remove suspended solids and that the (which may vary considerably between different virus subsequent treatment of the virus-rich sludge is of the types-Farrah and others 1978; Gerba and others utmost importance. In similar experiments with 1980), and the efficiency of removal of suspended solids coliphage f2, the same authors (Balluz, Butler and from the final effluent. Studies on virus removal by Jones 1978) found a removal of only 68 percent and activated sludge are listed in the appendixes of that a mere 16 percent of phage was associated with the Feachem and others (1980). solids fraction. It was concluded that coliphage is an 154 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES unsuitable indicator of enterovirus behavior in sewage removed from the sewage will be concentrated into the treatment processes (see also Butler and Balluz 1979). primary and secondary sludges. These findings on coliphage in activated sludge are important in interpreting the results of studies in which dih coliphage has been seeded into treatment plants to By oxidation itc study virus removal. Naparstek and others (1976) Practically no information is available on en- recorded the removal of seeded coliphage f2 at an terovirus removal by oxidation ditches (see the activated sludge plant in Maryland (USA). On appendixes of Feachem and others 1980). The process average, only 11 percent of coliphage was removed by is essentially similar to activated sludge, but the longer the aeration tanks and secondary sedimentation units, hydraulic retention times (1-3 days), and the higher and the removal across the whole plant (which proportion of sludge recycling giving a solids retention included chlorination) was only 80 percent. Safferman time of 10-30 days, are features that should produce and Morris (1976) studied the coliphage removal improved virus removal. This is supported by ability of a sophisticated pilot plant that incorporated laboratory studies in the USSR indicating the high-rate activated sludge, clarification, nitrification, elimination of seeded enteroviruses following 2 day's denitrification, aeration, and filtration. Average flow aeration (Goncharuk and others 1970) and by pilot- was 200 cubic meters per day, and the final effluent had plant studies in India showing 97-99.7 percent a BOD5 of 2 milligrams per liter. Removal of coliphage reduction of naturally occurring enteroviruses (Rao by the high-rate activated sludge unit was between 90 and others 1973). However, full-scale ditches will and 99 percent, whereas removal across the whole achieve considerably lower removal rates, and poorly plant averaged 99.97 percent. operating plants will most likely remove a negligible Gerba, Stagg and Abadie (1978) found between 0.1 proportion of enteroviruses. and 7 enteroviruses per liter in the effluents from two activated sludge plants in Houston (Texas, USA). Between 49 and 100 percent of viruses in the effluent B' waste stabilization ponds were adsorbed onto solids. Fujioka and Loh (1978) Very few systematically compiled data exist on the investigated a treatment plant in Hawaii (USA) that virus removal properties of well-constructed waste employed settling and activated sludge. Influent stabilization pond systems in warm climates. Removal contained 27-19,000 viruses per liter, while effluent rates reported (see the appendixes of Feachem and contained 7-5,222 per liter. Rao and others (1977) others 1980), vary widely, which is partly due to poor studied virus removal at the Dadar sewage treatment pond design, poor experimental procedures and short- plant (Bombay, India) where about 19,000 cubic circuiting of sewage flow across the ponds (Malherbe meters of sewage per day are treated by activated and Strickland-Cholmley 1967). sludge prior to marine discharge. Effluent BOD5 over a Rao, Lakhe and Waghmare (1978) reported that 2-year period averaged 6 milligrams per liter (98.5 even very poorly designed stabilization ponds in India percent reduction), and effluent suspended solids achieved virus removal rates similar to those of averaged 20 milligrams per liter (97.2 percent activated sludge plants. A single pond with 3-10 days reduction). Raw sewage contained 250-1,250 en- retention removed 89.9-96.2 percent of viruses; a teroviruses per liter, and final effluent contained 5-60 single pond with a 2.7 days retention time removed per liter. Removal rates were between 90 and 99 94.8-97.3 percent, and 4 ponds in series with a 17.2 percent. days retention time removed 88-98.9 percent of Both laboratory and field experience indicate that viruses. activated sludge systems are not particularly effective There is ample evidence of reduced survival of in removing enteroviruses but are more effective than enteroviruses in stabilization ponds at warm summer trickling filters (see above and Heyward and others temperatures when compared with the same ponds at 1977). Enterovirus removal in activated sludge cooler winter temperatures (Funderberg and others treatment works is in the range 0 to 99 percent, 1978; Kott, Ben-Ari and Betzer 1978; Lefler and Kott although better results (up to 99.9 percent) have been 1975; Slanetz and others 1970). Viruses adsorbed to achieved in laboratory and pilot-scale models. It is settleable solids will fall to the sludge layer at the base reasonable to assume that a well-run activated sludge of the facultative pond where they may survive for plant may reduce the enterovirus concentration by extended periods (Funderberg and others 1978). Other 50-95 percent, but that a poorly operated plant will biological and physical factors-such as a virucidal achieve negligible removal. Many of the viruses increase in pH to 9 or above caused in part by blooms ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 155 of algae (Funderberg and others 1978)-also may (1 8-20°C), with initial concentrations of 2,000 per liter, determine virus survival. inactivation was complete within 11-35 days. Nupen Lund (1979) estimated that virus inactivation in (1970) and Nupen, Bateman and McKenny (1974) heavily polluted water might proceed at approximately reported a 95 percent reduction in enteroviruses in a I log unit in 5 days at 32°C and I log unit in I day at chain of 9 maturation lagoons (total retention time 14 35°C. Funderberg and others (1978) reported polio- days) receiving the trickling filter plant effluent at virus removal in model outdoor ponds near Austin Windhoek (Namibia). Lagoon effluent contained up to (Texas, USA). During the summer over 99 percent of 25 enteroviruses per liter in summer and up to 842 per added virus was lost within 5 days, whereas this degree liter in winter. of removal took 15 and 25 days in spring and winter, respectively. COAGULATION. Coagulation is one of the more These data suggest that well-designed stabilization cheGULaT Coagulation isoone ofrthe more ponds in the tropics (with minimal short-circuiting, efete hem procse fo removing viruses from water temperature above 25°C, and overall retention wastewater. Alum [A12(S04)33, lime [Ca(OH)2], iron watr t r a e 2, asalts, and polyelectrolytes have all been used. Wolf and time of 30 days or more) should achieve very high levels others (1974) reported a greater than 99.6 percent of virus removal (at least a 4 log reduction). removal of seeded coliphage f2 and poliovirus 1 in a Confirmation of this must await further experimen- laboratory model coagulation-sedimentation system tation on well-designed waste stabilization ponds in employing alum. Lime is probably the most effective coagulant, since the high pH values produced are strongly virucidal (particularly above pH 11-see, for By aerated lagoons example, Nupen, Bateman and McKenny 1974). For An aerated lagoon on its own may be expected to maximum efficiency, coagulation should be followed have a virus removal rate similar to, or a little better by slow sand filtration (Berg 1973; Berg, Dean and ' . . ~~Dahling 1968; Derbyshire and Brown 1979; Grabow, than, an oxidation ditch. If the effluent is treated in Midn and Dbssone1978 Nupen 1970; Shelton maturation ponds, removal rates as in waste andDre 193 spou1978 Nupe197)0. Shelton stabilization ponds are expected. No specific data are reviewro virus Sreol by c onrandipH available, but warm temperatures will certainly revaew of vnrus removal by coagulation and pH increase enterovirus inactivation rates. The sludge adjustments has been recently published (Sproul 1980). drawn off from secondary sedimentation tanks or settling ponds will be rich in enteroviruses. FILTRATION. Sand filters can remove a high proportion of viruses from secondary effluents, but By tertiary treatment reported performances are erratic. Higher removal rates are achieved at lower filtration rates. Removal of Some tertiary, or advanced physicochemical, treat- viruses is also cnhanced by low or high pH and by the ment processes are effective in removing viruses. presence of cations (Jenkins and others 1980) and very However, they add cost to sewage treatment and in much enhanced by coagulation prior to filtration (Berg some cases are too technically and mechanically 1973). sophisticated to be appropriate in developing count- Sproul (1976) reported 99.7 percent removal from ries. activated sludge effluent at a filtration rate of 0.04 cubic meters per square meter per day and 100 percent LAGOONING. Secondary effluents may be further removal at 0.007 cubic meters per square meter per treated in maturation lagoons. Enterovirus removal day. Safferman and Morris (1976) reported very poor rates and processes are the same as in waste removal of coliphage (0 to 48 percent) by dual and stabilization ponds, except that little or no sedimen- multimedia filters without precoagulation. Berg, Dean tation takes place. High rates of virus removal can be and Dahling (1968) recorded an 82-99.8 percent achieved if several lagoons are employed and short- removal of viruses in lime coagulated effluent at a circuiting is avoided. filtration rate of 131 cubic meters per square meter per Kott, Ben-Ari and Betzer (1978) investigated the use day. of lagoons for the tertiary treatment of trickling filter Very significantly from the viewpoint of developing effluent at Haifa (Israel). In winter (temperatures down country operating problems, Vaughn and others to 8°C), initial enterovirus concentrations of 1.1 x 104 (1978) stated that the treatment plant at Holbrook per liter were reduced to zero in 47-73 days. In summer (New York, USA), which features extended aeration, 156 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES denitrification, and gravity sand filtration, was combined chlorine added to primary effluent in- experiencing "operating difficulties" and they isolated activated only between 1 and 2 log units of enterovirus up to 283 enteroviruses per liter from the final effluent. in 15 minutes, whereas in the same experiments fecal Assuming a raw influent concentration of about 1,000 coliform reductions ranged from 3 to more than 5 log per liter, a removal rate of only 72 percent was achieved units, and total coliform reductions ranged from 5 to in filtered tertiary effluent in an industrialized country. more than 7 log units. Similarly, Rao, Lakhe and Waghmare (1978) reported Different species of human excreted virus have that a sewage reclamation plant at a factory in Bombay different sensitivities to inactivation by chlorine. incorporated extended aeration, alum coagulation, Reoviruses are among the most sensitive, and rapid sand filtration, and deionization but achieved a polioviruses are among the most resistant (Drulak, virus removal of only 81-99 percent. These are Wallbank and Lebtag 1979; Englebrecht and others powerful illustrations both of the operating difficulties 1978; Shuval and others 1966: Sproul 1976). frequently experienced with advanced wastewater Boardman and Sproul (1977) studied the in- treatment plants even in developed countries and of the activation of coliphage T7 by chlorine when the phage inapplicability of much virus removal data obtained in was adsorbed to particles of clay, aluminium oxide, or laboratory or pilot-scale plants to full-scale operating calcium carbonate in water. It was concluded that treatment plants. adsorption of virus to the surface of inorganic particles offered no protection against inactivation by chlorine, DISINFECTION. Enterovirus removal from secon- but that encapsulation by a particle may afford dary or tertiary effluents by disinfection has been the protection. This conclusion has been confirmed by subject of numerous investigations in recent years. The studies by Hejkat and others (1979) into the most widely used disinfection technique for sewage inactivation by chlorine of poliovirus in fecal effluents is chlorination, and there is considerable homogenates.Theyfoundthatthevirusthatwasclosely evidence that viruses are less readily destroyed by associated with, or occluded within, small fecal effluent chlorination than enteric bacteria (Berg and particulates was protected from chlorine inactivation. Metcalf 1978; Snead and others 1980), although, A combined chlorine residual of 6.6 milligrams per liter unlike some bacteria, viruses cannot regrow in the (at pH 8 and 220C) achieved a 50 percent inactivation effluent subsequently. of solids-associated virus in 15 minutes, whereas only As with the bactericidal effects of chlorine in water 1.4 milligrams per liter of combined chlorine were treatment, free chlorine (especially in the form of sufficient to obtain the same reduction of free virus in hypochlorous acid at low pH and particularly at warm the same time. However, these differences were small temperatures) is a far more potent virucide than compared with differences in inactivation due to combined chlorine (monochloramine, dichloramine, dissolved organics that determined whether any free and other compounds), which is formed in the presence chlorine, as opposed to combined chlorine, was of ammonia and organic matter (Olivieri, Donovan present. Stagg and others (1978) studied three and Kawata 1971). Chlorine added to most sewage treatment plants in Houston (Texas, USA) and found plant effluents is rapidly converted to combined that between 2 and 21 percent of coliphages in plant chlorine, and this, together with the protective effect of effluent prior to chlorination were solids associated. virus association with solid particles, may result in very Passage through chlorine contact chambers in- poor virus removal. activated freely suspended phages to a greater extent In clean water at pH 7-8 1-2 milligrams per liter of than solids-associated phages, and increased the free chlorine maintained for 1-2 hours will be more proportion of solids-associated phages in the final than sufficient for complete virus inactivation. effluent to between 6 and over 99 percent. Only about Englebrecht and others (1978) showed that 6 different 15 percent of the solids-associated viruses were enteroviruses in water were all inactivated by 99 embedded; the remainder were adsorbed. percent in under 5 minutes when 0.5 milligrams per It is clear from the above that the efficacy of effluent liter of free chlorine were applied at 5C and pH 7-8. In chlorination in virus removal depends considerably a secondary sewage effluent (BOD5 of 45 milligrams per upon the quality of the effluent prior to chlorination. liter), however, poliovirus was reduced by 50 and 90 The better the quality of the effluent, the higher the percent in 6 hours after applying 5 and 11 milligrams virus inactivation attained by a given chlorination per liter of chlorine, respectively (Shuval and others system; tertiary treatment (for instance, by filtration) is 1966). Similarly, Berg and Metcalf (1978) reported therefore often recommended to reduce further that, at 22-240C, 11-23 milligrams per liter of suspended solids and dissolved organics prior to ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 157 chlorination (Dryden, Chen and Selna 1979; Bausum, Schaub and Kenyon (1978) found that Kirkpatrick and Presecan 1978). chlorination of a trickling filter effluent in Arizona Several reports indicate that well-run chlorination (USA) reduced the concentration of seeded coliphage units, receiving high quality effluents, can produce a by only 95 percent, as compared with a bacterial virus-free final effluent. Kott, Ben-Ari and Betzer reduction of 99.97 percent. Kott and others (1974) (1978) investigated the effect on enteroviruses of studied chlorinated waste stabilization pond effluents chlorinating a trickling filter effluent at Haifa (Israel). in Israel (8 milligrams per liter of applied chlorine for 1 At a chlorine dose of 20 milligrams per liter and a hour at 20°C) and found an average enterovirus contact time of 2 hours, enterovirus concentrations reduction of only about 10 percent, whereas the total were reduced from up to 5,900 per liter to zero (see also coliform reductions were 2 log to > 6 log units. The Kott, Ben-Ari and Vinokur 1978; Lindeman and Kott chlorinated pond effluents contained between 300 and 1971). 1,000 enteroviruses per liter. Other experiments found The possibility of a virus-free chlorinated effluent is that, at pH 6.0 with a 2-hour contact time, seeded also illustrated by data from some of the advanced poliovirus 1 in stabilization pond effluent was reduced wastewater reclamation plants. Culp (1974a, 1974b) by 86 percent with 20 milligrams per liter of applied reports complete virus inactivation at a Lake Tahoe chlorine, by 87 percent with 40 milligrams per liter of (USA) sewage treatment plant by carefully controlled chlorine, and by 100 percent with 60 milligrams per chlorination. Grabow and Isaacson (1978) failed to liter of chlorine. isolate any enteroviruses from 144 10-liter samples of The chlorination of inadequately treated sewage, in water produced by the advanced wastewater re- the hope of thereby removing much of the microbial clamation plants at Windhoek (Namibia) and Pretoria hazard, is disturbingly widespread despite clear (South Africa). These plants incorporated a train of evidence that it is generally ineffective and represents advanced processes and included break-point chlori- bad engineering practice. The authors of this book nation sufficient to produce 0.2-0.6 milligrams per liter have observed this practice on several occasions, and of free residual chlorine after 2-3 hours of contact time have frequently heard it recommended in developing (Nupen 1970; Nupen, Bateman and McKenny 1974). countries when concern is being expressed about the However, chlorination in no way guarantees a virus- discharge of highly polluted effluents from improperly free effluent. Sherman and others (1975) found that the designed or malfunctioning sewage treatment plants. chlorination of trickling filter plant effluents from two An interesting case study of this problem is the treatment plants in Maryland (USA) reduced seeded investigations by Sattar and Westwood (1978) in coliphage by 60 percent. Overall reductions of phage Ottawa (Canada), a city of 500,000 people that across the two plants were 82 percent and 86 percent. discharged 90 percent of its sewage into the Ottawa Fujioka and Loh (1978) reported isolating 25-34 and River after the wastes received only primary treatment 2-750 enteroviruses per liter from the chlorinated (sedimentation) and chlorination. Two treatment effluent of two treatment plants in Hawaii (USA). plants were studied that received a raw sewage with a Influent concentrations were 5-268 and 27-19,000 1oD5 of 79-98 milligrams per liter and that produced a enteroviruses per liter, respectively. Wellings and chlorinated primary effluent with a ROD5 of 44-48 others (1975) found on average 0.13 enteroviruses per milligrams per liter. Raw sewage samples were 80 liter (53 percent of samples positive) in the chlorinated percent positive for enteroviruses, with an average effluent from a package treatment plant receiving concentration of 1,000 per liter. Samples of sedimen- sewage containing 161 viruses per liter from a mobile tation tank effluent were 72 percent positive for home park. Wellings, Lewis and Mountain (1974, enteroviruses and also contained 1,000 viruses per liter. 1976) isolated up to 12 and 98 enteroviruses per liter, in Samples of final chlorinated effluent were 56 percent two studies on the chlorinated effluent from an positive for enteroviruses and contained 27 viruses per activated sludge plant in St. Petersburg (Florida, liter. The Ottawa River is used for recreation and USA). Metcalf, Wallis and Melnick (1974) isolated up provides the raw water source for about 600,000 to 4 enteroviruses per liter from a chlorinated effluent people. (1.2-1.9 milligrams per liter of residual chlorine after Various other wastewater disinfection systems have 10 minutes of contact) at an activated sludge plant near been studied with respect to their ability to inactivate Houston (Texas, USA). Vaughn and others (1978) viruses. Ozone is a very potent virucide, and its activity isolated up to 26 and 98 viruses per liter from the is less disturbed by organic pollution than is the case chlorinated secondary effluents from two sewage for chlorinc (De Michele 1974; Dryden, Chen and treatment plants on Long Island (New York, USA). Selna 1979; Evison 1978; Katzenelson and 158 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Biedermann 1976; Munger, Heyward and Swartz percent of poliovirus in primary effluent was removed 1977; Pavoni and Tittlebaum 1974; Rakness and Hegg in the top 0.2 meters of loamy sand, and no poliovirus 1979; Sproul 1976). Bromine chloride and paracetic was detected below 0.8 meters, when the flow rate was acid have been evaluated and are also little affected by approximately 0.2 cubic meters per square meter per organic matter in the effluent (Hajenian and Butler day. In other experiments it was shown that poliovirus 1980). Chlorine dioxide also effectively inactivates adsorption by loamy sand is reduced when the flow enteroviruses in water at a rate similar to hypochlorous rate is increased above some critical value, whereas acid. Unlike hypochlorous acid, chlorine dioxide is flow rate changes above and below this value do not more potent at higher pH values (Cronier, Scarpino affect adsorption. The critical value for loamy sand was and Zink 1978). Radiation at a level of 3-5 kilogray6 about 1 cubic meter per square meter per day; below inactivates approximately 90 percent of viruses in this flow rate poliovirus penetration was less than 1.6 sewage effluent, whereas only 1-1.5 kilogray are meters, whereas above it viruses penetrated the entire required to achieve the same inactivation of viruses in 2.5-meter column. distilled water (Metcalf 1977; Sullivan and others Duboise, Moore and Sagik (1976) reported that 1971). Photodynamic oxidation has also been eva- poliovirus and coliphage adsorbed to cores of loamy luated for the disinfection of wastewaters (Gerba, sand were eluted less by intermittent application of Wallis and Melnick 1977a, 1977b). However, all these effluent or water than by continuous application. In techniques are currently at the experimental stage; in addition, the chemical quality of the effluent improved any case, they may involve a level of technical more by soil filtration when the effluent was applied sophistication and cost that would make them intermittently than when it was applied continuously inappropriate in many situations in developing (see also Duboise and others 1974). countries. Bitton, Masterton and Gifford (1976) found that under experimental conditions coliphage T2 and LAND TREATMENT. Land treatment by soil filtration poliovirus were adsorbed more readily when suspen- or groundwater recharge can be highly effective in ded in tap water than in secondary effluent, and that removing viruses from primary or secondary sewage effluent is a more potent eluent than tap water for effluents, but results reported in the literature vary washing adsorbed viruses out of soil columns. Lefler widely. and Kott (1976) also found higher elution of poliovirus Lance, Gerba and Melnick (1976) showed, in and coliphage from sand with effluent as compared laboratory studies, that poliovirus in secondary with tap water. However, Duboise, Moore and Sagik effluent was almost completely removed by filtration (1976) reported that flooding cores of loamy sand with through loamy sand after flowing to a depth of 1.6 dechlorinated effluent eluted fewer polioviruses than meters and was reduced by 99 percent after 0.4 meters when distilled water was used. of flow. These results were obtained at filtration rates of Landry and others (1979) found that 72-100 percent both 0.55 cubic meters per square meter per day and of polioviruses, coxsackieviruses, and echoviruses were 0.15 cubic meters per square meter per day. Flooding retained when tertiary sewage effluent was passed the soil with deionized water (to simulate a rainstorm) through 1.25-meter natural cores of gravelly sand at a caused some downward movement of the viruses. but rate of 20 cubic meters per square meter per day. this was greatly reduced when CaC12 was added to the Flooding the cores with artificial rain water released deionized water. Drying of the soil between effluent 0-67 percent of the adsorbed viruses, whereas flooding application and a simulated rainstorm considerably with sewage effluent released 0-14 percent. A total of reduced desorption of viruses; 5 days drying prevented eight laboratory and field strains of enteroviruses were subsequent desorption completely. The authors used in these experiments. Some differences in concluded that viruses would move through 2.5 meters adsorption among the strains were recorded (with of calcareous sand only if heavy rains fell within a day echovirus 1 showing the greatest soil affinity), and the following the cessation of sewage application. In proportion of adsorbed viruses being eluted by follow-up studies (Gerba and Lance 1978; Lance and rainwater or sewagediffered markedly (with echovirus 1 Gerba 1980; Lance, Rice and Gilbert 1980), similar being the least mobilized and a wild strain of poliovirus adsorption and elution results were obtained in loamy 3 being the most readily eluted). The authors concluded sand whether polioviruses were suspended in primary that soil adsorption-elution behavior is strain de- or secondary effluent. In one series of experiments, 99 pendent and warn against the application of laboratory data from experiments using only a single strain of 6. See footnote 5, above. poliovirus 1. Gerba and others (1980), Goyal and Gerba ENTEROVIRUSES, POLIOMYELITIS. AND SIMILAR INFECTIONS 159 (1979), and Goyal and Melnick (1978) also reported and around the dome. Enteroviruses were isolated from wide intertypic and intratypic variation in adsorptive 3 out of 48 well-water samples, and horizontal behavior among enteroviruses in various soils. mnovement of viruses through the saturated soils of at Burge and Enkiri (1978a) reported substantial least 7 meters was demonstrated. differences in the ability of five soils to adsorb Gilbert and others (1976a, 1976b) studied virus coliphage viruses. More acidic soils had higher removal from activated sludge effluent (up to 75 viruses adsorption rates, and one loamy sand adsorbed no per liter) applied to loamy sand (infiltration rate of 0.27 viruses (see also Burge and Enkiri 1978b; Vilker and cubic meters per square meter per day) at a 7-year-old Burge 1980). Similarly, Lefler and Kott (1974b) found wastewater renovation plant near Phoenix (Arizona, that many coliphage f2 and poliovirus 1 were able to USA).Novirusesweredetectedintheobservationwells, pass through a 0.2-meter sand column (at an indicating at least a 99.99 percent removal after flow application rate of 1.7 cubic meters per square meter through 3-9 meters of soil. In contrast, Schaub and per day) and that only a high concentration of bivalent Sorber (1977) reported very low viral removal by soil cations (Ca' + and Mg' +) prevented this. Funderberg filtration (infiltration rate 0.07 cubic meters per square and others (1979), Goyal and Gerba (1979), and meter per day) of primary effluent at a 30-year-old Moore and others (1979) have also reported wide treatment plant in Massachusetts (USA). The soil was variation in virus adsorption behavior dependent on unconsolidated silty sand and gravel. Seeded coliphage soil properties. f2 viruses were reduced by an average of 53 percent after Studies by Scheuerman and others (1979) showed 18 meters of percolation, and seeded f2 and indigenous that some organic soils have poor virus adsorption enteroviruses were sporadically detected in the potential due to the presence of water-soluble humic groundwater at horizontal distances of 180 meters from substances (humic and fulvic acids), which may the application zone. compete with viruses for adsorption sites on soil It is clear from these and other studies that particles or may react with certain surface groups on adsorption to soil particles, rather than viral death, is virus particles that are functionally important in the dominant removal mechanism. Adsorption is adsorption to soil. increased by low infiltration rates (say <0.1 cubic Wellings, Lewis and Mountain (1974) studied an meters per square meter per day), by low pH, and by effluent spray irrigation site near St. Petersburg the presence of divalent cations (Ca++ and Mg +). (Florida, USA). The effluent from the activated sludge Adsorption is reduced in the presence of soluble plant contained up to 240 enteroviruses per liter, and organic matter which competes for adsorption sites on the final chlorinated effluent contained up to 98 per the soil particles. Adsorption and elution behavior liter. The effluent was applied to a sandy soil at between depend very much upon the characteristics of the soil 0.007 and 0.04 cubic meters per square meter per day. and the particular strain of virus. A great deal of further Water collected in drains 1.5 meters under the soil experimentation will be required before the optimal contained polioviruses, echoviruses, and reoviruses soil structures-and their relationships to infiltration (2 out of 9 samples positive). Enteroviruses were also rates, application schedules, and virus removal isolated from wells 3 and 6 meters deep at the site performance-are fully understood. It is already following heavy rain. apparent, however, that by passing even raw sewage Wellings and others (1975) studied the discharge of through less than 1 meter of a suitable soil it is possible effluent from a 154-unit mobile home park into a to reduce the virus concentration by as much as, or more cypress dome in the wetlands of Florida (USA). The than, that normally achieved by wastewater chlori- population of the park varied between 310 and 337 nation (Gerba 1979). Because of higher temperatures during the study and produced a raw sewage with an there, the effectiveness of land application in virus average of 161 enteroviruses per liter (range between 0 removal in the developing countries is likely to be and more than 700 per liter). Polioviruses 1, 2, and 3 greater than that generally reported from temperate accounted for 40 percent of isolates identified, with areas. It must be remembered, however, that without coxsackieviruses (B3 and B4) making up 43 percent, efficient management, operation, and maintenance and echoviruses (7, 11, and 14) the remaining 17 land application systems will become insanitary bogs. percent. Chlorinated effluent from a package treatment The above discussion has dealt exclusively with soil plant yielded polioviruses and coxsackieviruses in 8 filtration and groundwater recharge as methods of out of 15 samples taken. The effluent was discharged land treatment for wastewaters. The other major type into the cypress dome, and groundwater quality was of land treatment technology is the grass plot or monitored in 18 3-meter-deep wells constructed in overland run-off method. In these systems a significant 160 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES proportion of the effluent may run over the surface of Even less is known about the virological aspects of the soil and not flow through it, and it may be expected night soil and night soil treatment. that virus removal will be poor compared with the soil filtration data reported above. Experiments by Schaub and others (1980) confirmed this, showing a removal of B' pit latrines only 30-60 percent of seeded f2 bacteriophage and Little information is available, but it is probable that only 76-88 percent of indigenous excreted virus during enteroviruses survive for several weeks in pit latrines treatment on 36 meter long grass plots with a 3 percent (see the sections above on occurrence and survival in slope. feces and night soil and in sludge; see also the appendixes to Feachem and others 1980). In warm OTHER PROCESSES. A variety of other treatment climates, the pit contents should be free of en- processes are associated with advanced wastewater teroviruses if they are left for at least 3 months before treatment plants and with water reclamation or digging out. renovation projects. Some of these processes have been A pit latrine may act as a source of viral groundwater assessed for virus removal capability. Carbon adsor- pollution depending on the type of soil, groundwater ption and nitrification do not seem particularly levels, and the proximity of local wells (see the sections effective, whereas denitrification was reported to above on occurrence and survival in groundwater and remove 97 percent of coliphage (Berg 1973; Gerba and on virus removal by land treatment). others 1974; Safferman and Morris 1976; Sproul 1976). Francis, Brown and Ainslie (1953) isolated po- Complete water reclamation plants, incorporating a lioviruses (16 out of 220 samples positive) and train of advanced processes, are generally reported to coxsackieviruses (10 out of 63 samples positive) from achieve total virus removal when operating pit latrines in poor areas of four towns in southern perfectly. The Lake Tahoe (Nevada, USA) recla- Texas (USA). Pit latrines with polioviruses were not mation plant has occasionally let through viruses associated with known cases of poliomyelitis, an beyond the carbon adsorption stage, but they were epidemic of which was taking place at the time eliminated by chlorination (Berg 1973). Similarly, the (March-July of 1948), but were associated with the Windhoek (Namibia) reclamation plant is reported to isolation of polioviruses from flies in the vicinity. have achieved a virus-free effluent, despite an influent virus concentration of up to 2 x t04 per liter (Grabow and Isaacson 1978; Nupen 1970; Stander and Clayton B anaerobic digestion 1977). Although some form of anaerobic digestion is used to treat sludge from most larger sewage treatment plants, very little information is available on the virus removal performance of full-scale digesters. (Some Inactivation by Night soil and Sludge laboratory studies are discussed below and arc listed in Treatment Processes the appendixes of Feachem and others 1980). Ward and Ashley (1976) investigated the in- activation rate of poliovirus in digested sludge and Raw night soil contains all the viruses being excreted found that it was greater than 1 log unit per day at by the contributing population. Sewage works sludges 28°C and about 1 log unit per 5 days at 4°C. They are rich in viruses because a high proportion of viruses concluded that anaerobically digested sludge contains in sewage are, or become, solids-associated and are a specific virucidal agent; in a subsequent study (Ward therefore concentrated into both primary and secon- and Ashley 1977a) they identified this agent as dary sludges (Lund 1973; Lund 1976; Lund and Ronne ammonia (see also Fenters and others 1979). Ammonia 1973; Wellings, Lewis and Mountain 1976). Interest in is not virucidal in its charged state, but free ammonia, viruses in sludges has been stimulated by the fact that a which is formed at pH values of 8 and above, is highly large proportion of sewage sludge is applied to the land virucidal to enteroviruses but much less so to as a method of disposal and soil enrichment. reoviruses. Ward and Ashley concluded that ammonia Information on this subject is restricted to acts as a potent enterovirucide in raw and digested laboratory studies and a few field studies conducted in sludges with high pH values. At pH 9.5 and 21°C, North America and Europe. Little is known about greater than 3 log unit and 5 log reductions in viruses in sludge in developing countries or about poliovirus concentrations were obtained in 72 hours in sludge treatment under tropical climatic conditions. raw and digested sludges, respectively. A later study ENTEROVIRUSES. POLIOMYELITIS, AND SIMILAR INFECTIONS 161 confirmed that reovirus 3 was unaffected by the and centrifuged at a Houston (Texas, USA) treatment presence of ammonia (Ward and Ashley 1977c). plant. Eisenhardt, Lund and Nissen (1977) studied the Investigators who have looked for viruses in digested inactivation of coxsackievirus B3 in a laboratory-scale sludge have generally found them in considerable anaerobic sludge digester at pH 7. At 32°C a 5 log numbers (Berg and Metcalf 1978; Grigoryeva, reduction in virus concentration occurred in about 14 Korchak and Bey 1969; Hurst and others 1978; Sattar days, whereas at 35°C the same reduction took only 4 and Westwood 1979; Wellings, Lewis and Mountain days. Inactivation was slightly faster when the virus 1976). Some laboratory studies have reported an was held in pasteurized sludge. Bertucci and others inactivation rate of around 1 log unit per day at (1977) ran a laboratory anaerobic digester (pH 30-35°C (for instance, Eisenhardt, Lund and Nissen 7.2-7.4) at 35°C and compared inactivation rates of 1977; Fenters and others 1979; Ward and Ashley various enteroviruses. Inactivation rates varied from 1976). At this rate of inactivation, typical anaerobic 75 percent per day for echovirus 11 to 97 percent per digestion at 35°C for 35 days should produce a virus- day for coxsackievirus A9. free sludge with a wide margin of safety. However, Sanders and her coworkers (1979) pointed out that Sanders and others (1979) have shown that in- most previous laboratory studies investigated the activation rates of solids-associated viruses after the inactivation of free viruses inoculated into sludge first day of digestion may be very much slower (around immediately prior to digestion. However, to simulate 1 log unit every 2-7 days). In addition, most digesters more exactly real operating conditions it is necessary are operated by continuous, or regular, addition and to allow the viruses to become associated with solids removal of sludge. Therefore, some sludge has a prior to commencing digestion. Sanders therefore retention time of very much less than the design value investigated the inactivation by anaerobic digestion of and will contain significant concentrations of viruses solids-associated poliovirus and found that survival after digestion. It is probable that only batch digestion was enhanced by solids incorporation. The in- at 35°C, for 35 days, or digestion at temperatures of activation rates at 34 and 37°C were 84 to 99 percent around 50°C, will produce a virus-free sludge. More per day, respectively, for the first 24 hours. After that field data are required, on the actual virus removal time inactivation slowed considerably to between 30 performance of operating plants of these types, to and 60 percent per day. At 50°C the inactivation rate confirm this assumption. was high at more than 7 log units per day. Berg and Metcalf (1978) reported the destruction of between 76 and 96 percent of viruses by mesophilic By drying digestion (35°C for 20 days) and between 98.9 and > 99.9 percent by thermophilic digestion (50°C for 20 Both raw and digested sludges are normally days). Enterovirus concentrations in raw sludge were dewatered prior to disposal, and the most common 4 x 103 to > 1 x 105 per liter, 300 to 4,100 per liter in technique is spreading on outdoor sludge drying beds. mesophilically digested sludge, and 0 to 170 per liter in Very little information is available on virus removal by thermophilically digested sludge. In these experiments, sludge drying (see below and the appendixes of samples of digested sludge were taken shortly after the Feachem and others 1980), and no studies have been addition of fresh sludge to the digesters, and so reported from developing countries. However, the data theoretical retention times would not have applied to on enterovirus survival in sludge are also relevant (see all aliquots of digested sludge. the section above on the occurrence and survival of Wellings, Lewis and Mountain (1976) isolated enteroviruses in sludge and the appendixes of Feachem enteroviruses and reoviruses, at concentrations of up to and others 1980). 34 per liter, from sludge from an anaerobic digester in Ward and Ashley (1977b) investigated the in- Florida (retention time >60 days at 34°C) to which no activation of viruses in sewage sludge that occurs raw sludge had been added for the previous 7 days. during dewatering by evaporation. Sludge, with a Sattar and Westwood (1979) found excreted viruses in solids content of 5 percent and a pH of 6, was 53 percent of samples of digested sludge (20 days at inoculated with 2.7 x 107 viruses per milliliter and air 35°C) and in 39 percent of dried sludge samples (>6 dried at 21°C in 1 centimeter thick layers over 4 days. months' drying time) at a large sewage treatment plant As evaporation proceeded, poliovirus 1 was in- in Ottawa (Canada). Hurst and others (1978) isolated activated at a low but constant rate until, at a solids viruses, at concentrations of up to 231 per liter, from concentration of 65 percent, approximately 75 percent sludge that had been thickened, aerobically digested, inactivation had occurred. At this stage inactivation 162 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES increased rapidly so that, during concentration up to present at the high pH levels found in anaerobically 83 percent solids, a further 99.9 percent inactivation digested sludge. At 43°C after 200 minutes, poliovirus occurred. Further concentration up to 91 percent concentration was reduced by over 3 log units in solids produced little more inactivation. A similar digested sludge, but it was almost stable in raw sludge. result was obtained with coxsackievirus BH and At 51°C, the poliovirus concentration was reduced by reovirus 3. In a subsequent study (Ward and Ashley over 5 log units in under 5 minutes in digested sludge 1978b), it was found that sludge drying increased the and by over 4 log units after 50 minutes in raw sludge. heat required to inactivate enteroviruses and reovirus. In a second study (Ward and Ashley 1977c), the heat Sattar and Westwood (1979) isolated viruses from inactivation of reovirus 3 in sludge was investigated. anaerobically digested sludge that had been drying for Reovirus was found to be quite heat resistant 8 months in Canada. Wellings, Lewis and Mountain compared with poliovirus but was not protected (1976) isolated 10 enteroviruses per 100 grams of against heat inactivation by sludge. At 50°C for 20 sludge that had been on sludge drying beds for two minutes, reovirus concentrations were reduced by 4 log weeks during February in Florida (USA). units in digested sludge and by 2 log units in raw 'These studies, and the reports on virus survival in sludge. At 60°C after 20 minutes; the reductions were 5 sludge indicate that during cool, wet weather en- log units in digested sludge and 4 log units in raw teroviruses may survive in drying sludge for several sludge. A virucidal agent against reoviruses was months. Data on rapid virus inactivation at solids discovered in the sludge that had greatly increased concentrations between 65 and 83 percent may be activity at pH values above 8. Unlike the case of the irrelevant, since under temperate conditions sludges enteroviruses (Ward and Ashley 1977a), this agent was may achieve a solids content of only about 25 percent not ammonia. A follow-up study (Ward and Ashley after about 2 months on a drying bed. Even in Texas 1978a) determined that ionic detergents found in (USA) in the summer, a sludge that had been applied to sewage sludges reduce the heat required to inactivate land for 3 months had dried to only 59 percent solids reoviruses (cationic detergents being more active than (Hurst and others 1978). However, a comparison anionic detergents, and nonionic detergents having no between virus inactivation rates in sludge during activity). In contrast, some detergents were found to Danish winters (1 log unit per month), and during protect poliovirus against heat inactivation. (More Texan summers (2 log units per week), clearly indicates information on the virucidal activity of detergents, and that enterovirus inactivation is far more rapid in hot the effects of differing pH values, is given in Ward and climates under bright sunshine. A good virus removal Ashley 1979). In a subsequent study (Ward and Ashley performance may therefore be obtained by sludge 1978b), a reduction in moisture content was found to drying beds in many developing countries, and field reduce significantly the rates of heat inactivation of studies are required to confirm this possibility. both enteroviruses and reovirus. Poliovirus in raw sludge at 51°C was reduced by over 5 log units in 5 minutes when the sludge had 5 percent solids but by By heating less than 2 log units after 100 minutes when the sludge had an 80 percent solids content. Reovirus in raw Under certain circumstances enteroviruses can be sludge at 51 °C was reduced by 4 log units in 50 minutes remarkably resistant to heating. For instance, Larkin when the sludge had 5 percent solids and by less than 2 and Fassolitis (1979) reported that infectious ribonuc- log units after 50 minutes when the sludge had a solids leic acid (RNA) liberated from poliovirus 1 and content of 80 percent. coxsackievirus B2 could withstand 65 minutes at 70°C. When compared with the reality of sludge treatment In general, however, heat is a potent virucide, and the processes, however, these are trivial differences and heating of sludges, or their digestion at elevated distinctions. Figure 9-2 presents data on the survival of temperatures, is an effective method of virus in- different types of enteroviruses under different activation. conditions for various time-temperature combi- Ward, Ashley and Moseley (1976) studied the effect nations. A conservative upper bound is drawn, above of raw and anaerobically digested sludge on the heat which the combinations of time and temperature inactivation of poliovirus. Raw sludge was found to be should guarantee enterovirus elimination. From this very protective of poliovirus inactivation whereas figure it is postulated that holding sludge at 30°C for 3 digested sludge was not, and subsequent studies (Ward months, at 40°C for 2 weeks, at 50°C for 1 day, or at and Ashley 1977a) determined that this difference was 60'C for 2 hours, will inactivate all enteroviruses, due to the virucidal activity of uncharged ammonia reoviruses, and adenoviruses. ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 163 OD - so8 75 -75 70 - ZONE -70 65 - Z65 60 - OF -60 55 -SAFETY -5s .~45- 4 -40 35 -3 '30 - IL IL 25 - 25 20 - s IL s O- 20 15 * 100% inactivation of nterovirus 15 10 | 1e ta n I00% inactivation of entorovirusm | 10 5 - it * X* 5 0.0) o'. 1 b I I lio io oo Insin Ihow 1d, Iw& Imonth lyom TIME (HOURS) Figure 9-2. The influence of time and temperature on enteroviruses. The data probably also apply to adenoviruses and reoviruses. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death By composting seeded bacteriophage (originally present at a con- centration of 106 per gram) took about 50 days in Aerobic thermophilic composting is an effective composting raw sludge and up to 70 days in method of inactivating viruses in sludge if all parts of composting digested sludge. Naturally occurring the pile or mass are heated to 50°C or above for enteric viruses were isolated throughout the windrow sufficient time (see figure 9-2 and the appendixes of phase of the composting but were never isolated from Feachem and others 1980). the curing piles. All these experiments were conducted Krige (1964) reported that seeded poliovirus 1 was during the cold and wet months of October-March. eliminated from a sludge, grass, and refuse mixture Experiments were later conducted into the inactivation composted at 38-58°C for 7 days. Wiley and of seeded coliphage f2 by a forced air composting Westerberg (1969) determined that the thermal death system (21 days of aerated composting followed by 30 points for poliovirus 1 were 60°C for 5 minutes or 55°C days of curing) at the same site (Burge, Cramer and for 30 minutes. When poliovirus 1 was added to a Epstein 1978). Temperatures rose to 50°C and above forced-air sludge-composting unit operating at within the first five days, and coliphage destruction 60-76°C, it could not be detected after 1 hour. deep in the pile was complete within 13 days. However, Kawata, Cramer and Burge (1977) reported the at the edge of the pile, very small proportions (around inactivation of seeded bacteriophage f2 in a sludge and 0.001 percent) of virus survived after 21 days. The wood chips mixture composted at a plant in Maryland inactivation rate in the pile was approximately 1 log (USA). The mixture was formed into windrows, which unit per 2 days. Pile temperatures in the forced air were turned regularly (up to once per day depending system were unaffected by ambient temperature or upon the temperature within the mass) for 2 weeks and rainfall. were then made into large piles for 4 weeks of curing. Much more research is required on virus removal When raw sludge was composted, the temperatures from various types of composting system using night rose to 50-70°C within 3 days and remained there soil, sludge, refuse, woodchips, and other materials. except for short periods following rainstorms. When Pending this work, virus inactivation may be digested sludge was composted, the temperature rose tentatively predicted from figure 9-2. Even where the gradually to 40-60°C after 10-14 days, and during time-temperature characteristics in the pile are well cold wet winter weather the temperatures rose only to within the safety zone in figure 9-2, virus survival may the 20-30°C range. Complete inactivation of the still be occurring at the edges of the pile, which are 164 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES usually much cooler, especially during rain. Complete Anon. (1976). Shellfish and public health. British Medical elimination of enteroviruses is therefore dependent Journal, 2, 1-2. upon pile management techniques such as turning, Anon. (1978). Viruses and reclaimed water. British Medical lagging, or forced aeration. Journal, 2, 1662. Balluz, S. A., Bulter, M. and Jones, H. H. (1978). The behaviour of f2 coliphage in activated sludge treatment. By other sludge treatment processes Journal oJ Hygiene, 80, 237-243. Balluz, S. A., Jones. H. H. and Butler, M. (1977). The persistence of poliovirus in activated sludge treatment. tures of 50'C or above should yield a virus-free product Journal of Hygiene, 78, 165- 173. if the process is well controlled and carried out for Bausum, H. T., Schaub, S. A. and Kenyon, K. F. (1978). Viral sufficiently long to ensure that all parts of the mass are and Bacterial Aerosols at a Wastewater Spray Irrigation heated. This latter point is particularly important when Site. Technical Report 7804. Washington, D.C.: US Army continuous, rather than batch, processes are being Medical Research and Development Command. used. Examples include pasteurization (70-80°C), Baylor, E. R., Baylor, M. B., Blanchard, D. C., Syzdek, L. D. anaerobic or aerobic thermophilic digestion and Appel, C. (1977). Virus transfer from surf to wind. (46-55°C), wet oxidation (180-220°C), incineration Scienzce, 198, 575-580. (over 650C), and pyrolysis, as well as heating and Baylor, E. R., Peters, V. and Baylor, M. B. (1977). Water-to- composting (discussed above), air transfer of virus. Science, 197, 763-764. Berg,G.ed.(1967).Trani,sminssion of, l , l. Wiatei Route. Sludge disinfection by irradiation with high-energy New York: Wiley Interscience. electrons is attracting increasing interest. (Osborn and . 1973) Removal ofviruses from sewage, effluents. and Hattingh 1978). The few data available on virus waters: a review. Bulletin of the World Heulth Organization. inactivation in sludge by irradiation indicate a rather 49, 451-460. poor removal of 75-90 percent after the application of , (1978a). Detection, occurrence and removal of 3-5 kilograys.7 (Lessel and Suess 1978; Sullivan and viruses. Journal ot the Water Polltutionz Conztrol Federatioz., others 1971; Ward 1977). Sludge protects poliovirus 50. 1395-1402. from irradiation, but little or no extra protection is , ed. (1978b). Indicators ojf Viruses in Water anid Food. afforded by increasing solids content above about 1 Ann Arbor, Mich.: Ann Arbor Science Publishers. percent (Ward 1977). Superchlorination or chlorine Berg, G., Dean. R. B. and Dahling, R. D. (1968). Removal of percent (Ward 197.uecpoliovirus 1 from secondary effluents by lime flocculation oxtdation (the application of 700-4,000 milligrams per and rapid sand filtration. Journal of the American Water liter of chlorine under pressure) may inactivate most Works Association, 60, 193-198. viruses in sludge but has been objected to because it Berg, G. and Metcalf, T. G. (1978). Indicators of viruses in proliferates chlorinated organic compounds in the waters. In Indicators ofjViruses in Water and Food, ed. Berg, environment (Kamlet 1979). G.. pp. 267-296. Ann Arbor. Mich.: Ann Arbor Science Most of these technologies for sludge disinfection Publishers. are still in the research and development stage, and Berry. S. A. and Noton, B. G. (1976). Survival of many of them will prove to be too costly and too bacteriophages in seawater. Water Research, 10, 323-327. technically complex to be appropriate in most Bertucci, J. J., Lue-Hing, C., Zenz, D. and Sedita, S. J. (1977). situations in developing countries. Inactivation of viruses during anaerobic sludge digestion. Jour nal of the Water Pollutioni Control Feder ationl, 49, 1642- 1651. Ltterature Ctted Bitton, G.. Masterton, N. and Gifford, G. E. (1976). Effect of a secondary treated effluent on the movement of viruses through a cypress dome soil. Journal of Enrironniental Addy, P. A. K. and Otatume, S. (1976). Ecology of i , ,.......i 5 370-375. enteroviruses in Ghana: isolation of poliomyelitis and Bitton, G., Monteith, C., Pancorbo, 0. and Gifford, G. E. other enteroviruses from water and sewage. Ghana (1977). Virus removal in marine aquaculture systems. Medical Journal. 18, 102-108. Rerue Internationale d'Oceanographie Medicale, 48,47-52. Akin, E. W., Hill, W. F., Cline, G. B. and Benton. W. H. Bloom, H. H., Mack, W. N., Krueger, B. J. and Mallmann, W. (1976). The loss of poliovirus 1 infectivity in marine waters. L. (1959). Identification of enteroviruses in sewage. Journal Water Research, 10, 59-63. of Iniectious Diseases. 105, 61-68. Anon. (1971). Poliomyelitis in 1970. World Healthl Boardman, G. D. and Sproul, 0. J. (1977). Protection of Organization Chronicle, 25, 513-519. viruses during disinfection by adsorption to particulate matter. Journal of the Water Pollution Control Federation. 49, 1857-1861. 7. See footnote 5, above. Boche, R., Millan, J. and Le Noc, P. (1973). La poliomyelite ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 165 au Cameroun: enquete virologique et serologique dans la Culp, R. L. (1974a). Breakpoint chlorination for virus population infantile de Yaounde, Revue d'Epidemiologie, inactivation. Journal of the American Water Works Medecine Sociale et Sante Publique, 21, 79-93. Association, 66, 699-703. Buras, N. (1976). Concentration of enteric viruses in (1974b). Breakpoint chlorination for virus in- wastewater and effluent: a two year study. Water Research, activation. In Virus Survival in Water and Wastewater 10, 295-298. Systems, eds. Malina, J. F. and Sagik, B. S., pp. 158-165. Burge, W. D., Cramer, W. N. and Epstein, E. (1978). Austin, Texas: Center for Research in Water Resources. Destruction of pathogens in sewage sludges by compost- University of Texas at Austin. ing. Transactions of the American Society of Agricultural Dahling, D. R. and Safferman, R. S. (1979). Survival of enteric Engineers, 21, 510-514. viruses under natural conditions in a subarctic river. Burge, W. D. and Enkiri, N. K. (1978a). Virus adsorption by Applied and Environmental Microbiology, 38, 1103-1110. five soils. Journal of Environmental Quality, 7, 73-76. Damgaard-Larsen, S., Jensen, K. O., Lund, E. and Nissen, B. (1978b). Adsorption kinetics of bacteriophage <)X- (1977). Survival and movement of enterovirus in 174 on soil. Journal of Environmental Quality, 7, 536-541. connection with land disposal of sludges. Water Research, Butler, M. and Balluz, S. A. (1979). A comparison of the 11, 503-508. behaviour of poliovirus and f2 coliphage in activated de Jong, J. C. and Winkler, K. C. (1968). The inactivation of sludge treatment. In Biological Indicators of Water Quality, poliovirus in aerosols. Journal of Hygiene, 66, 557-565. eds. James, A. and Evison, L., pp. 19/1-19/21. Chichester: De Michele, E. (1974). Water reuse, virus removal and public John Wiley. health. In Virus Survival in Water and Wastewater Systems, Chang, P. W., Liu, 0. C., Miller, L. T. and Li, S. M. (1971). eds. Malina, J. F. and Sagik, B. P., pp. 45 56. Austin, Multiplication of human enteroviruses in northern Texas: Center for Research in Water Resources, quahogs. Proceedings of the Society fbr Experimental University of Texas at Austin. Biology and Medicine, 136, 1380-1384. Derbyshire, J. B. and Brown, E. G. (1979). The inactivation of Clarke, N. A. and Chang, S. L. (1975). Removal of viruses in cattle and pig slurry by aeration or treatment enteroviruses from sewage by bench-scale rotary-tube with calcium hydroxide. Journal of Hygiene, 82, 293-299. trickling filters. Applied Microbiology, 30, 223-228. DiGirolamo, R. and Daley, M. (1973). Recovery of Clarke, N. A., Stevenson, R. E., Chang, S. L. and Kabler, P. bacteriophage from contaminated chilled and frozen W. (1961). Removal of enteric viruses from sewage by samples of edible West Coast crabs. Applied Microbiology, activated sludge treatment. American Journal of Public 25, 1020-1022. Health, 51, 1118-1129. DiGirolamo, R., Liston, J. and Matches, J. (1970). Survival of Cliver, D., Green, K. M. and Bouma, J. (1975). Viruses in virus in chilled, frozen and processed oysters. Applied Septic Tank Effluent. Madison, Wis.: College of Microbiology, 20, 58-63. Agricultural and Life Sciences, University of Wisconsin- (1972). Effects of irradiation on the survival of virus in Madison. West Coast oysters. Applied Microbiology, 24, 1005-1006. Cochran, K. W. and Fannin, K. F. (1976). Viral Monitoring of (1975). Uptake and elimination of poliovirus by West Wastewater Aerosols. Ann Arbor, Mich.: School of Public Coast oysters. Applied Microbiology, 29, 260-264. Health, University of Michigan. DiGirolanio, R., Wiczynski, L., Daley, M. and Miranda, F. Colwell, R. R. and Kaper,J. (1978). Distribution, survival and (1972a). Preliminary observations on the uptake of significance of pathogenic bacteria and viruses in estuaries. poliovirus by West Coast shore crabs. Applied In Estaurine Interactions. ed. WileN. M. L., pp. 443-457. Microbiology, 23, 170-171. New York: Academic Press. DiGirolamo, R., Wiczynski, L., Daley, M., Miranda, F. and Committee on Viruses in Drinking Water (1979). Viruses in Viehweger, C. (1972b). Uptake of bacteriophage and their drinking water. Journal of the American Water Works subsequent survival in edible West Coast crabs after Association, 71, 441-444. processing. Applied Microbiology, 23, 1073-1076. Cooney, M. K., Hall, C. E. and Fox, J. P. (1972). The Seattle Drulak, M., Wallbank, A. M. and Lebtag, I. (1979). The virus watch. III. Evaluation of isolation methods and relative resistance of f2 bacteriophage to inactivation by summary of infections detected by virus isolations. disinfectants. Journal of Hygiene, 83, 111-119. American Journial ol Epidemiology, 96, 286-305. Dryden, F. D., Chen, C. and Selna, M. W. (1979). Virus Cronier, S., Scarpino, P. V. and Zink, M. L. (1978). Chlorine removal in advanced wastewater treatment systems. dioxide destruction of viruses and bacteria in water. In Journal of the Water Pollution Control Federation, 51, Water Chlorination: Environmental Impact and Health 2098-2109. Eri' . f2, eds. Jolley, R. L., Gorchev, H. and Hamilton, Duboise, S. M., Moore, B. E. and Sagik, B. P. (1976). D. H., pp. 651-658. Ann Arbor, Mich.: Ann Arbor Science Poliovirus survival and movement in a sandy forest soil. Publishers. Applied and Environmental Microbiology, 31, 536-543. Cubbage, C. P., Gannon, J. J., Cochran, K. W. and Williams, Duboise, S. M., Sagik, B. P., More, B. E. D. and Malina, J. F. G. W. (1979). Loss of infectivity of poliovirus 1 in river (1974). Virus migration through soils. In Virus Survival in water under simulated field conditions Water Research, 13, Waters and Wastewater Systems, eds. Malina, J. F. and 1091-1099. Sagik, B. P., pp. 233-240. Austin, Texas: Center for 166 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Research in Water Resources, University of Texas at system disease. American Journal of Epidemiology, 83, Austin. 455-469. Edmond, T. D., Schaiberger, G. E. and Gerba, C. P. (1978). Fujioka, R. S., Lau, L. S. and Loh, P. C. (1978). Detection of enteroviruses near deep marine sewage Characterization of the virucidal agent(s) in the ocean outfalls. Marine Pollution Bulletin, 9, 246-249. waters off Hawaii. Abstract Q23. Abstracts oJ the Annual Eisenhardt, A., Lund, E. and Nissen, B. (1977). The effect of Meeting of the American Society for Microbiology. sludge digestion on virus infectivity. Water Research, 11, Washington, D.C. 579-581. Fujioka, R. S. and Loh, P. C. (1978). Recycling of water for Englebrecht, R. S., Weber, M. J., Schmidt, C. A. and Salter, B. irrigation: persistence of enteroviruses in sewage effluent L. (1978). Virus Sensitivity to Chlorine Disinfection oJ Water and natural waters receiving the effluent. Water, Air and Supplies. Report EPA-600/2-78-123. Cincinnati, Ohio: US Soil Pollution, 9, 213-226. Environmental Protection Agency. Funderberg, S. W., Moore, B. E., Sagik, B. P. and Sorber, C. Engley, F. B. (1956). The persistence (survival) of A. (1979). Comparison of viral transport in several soils. microorganisms. IV. In food. Texas Reports on Biology and Abstract Q45. Abstracts of tile Annual Meeting of the Medicine, 14, 313-361. American Society for Microbiology. Washington, D.C. EPA (1978). Human Viruses in the Aquatic Environmenit: A Funderberg, S., Moore, B. E., Sorber, C. A. and Sagik, B. P. Status Report with Emphasis on the EPA Research (1978). Survival of poliovirus in model wastewater holding Program. Report EPA-570/9-78/006. Washington, D.C.,: ponds. Progress in Water Technology, 10, 619-629. US Environmental Protection Agency. Gamble, D. R. (1979). Viruses in drinking-water: recon- Evison, L. M. (1978). Inactivation of enteroviruses and sideration of evidence for postulated health hazard and coliphages with ozone in waters and waste waters. proposals for virological standards of purity. Lancet, 1, Progress in Water Technology, 10, 365-374. 425-428. Fannin, K. F., Gannon, J. J., Cochran, K. W. and Spendlove, Gerba, C. P. (1979). Pathogen removal from wastewater J. C. (1977). Field studies on coliphages and coliforms as during groundwater recharge. Municipal Wastewater indicators of airborne animal viral contamination from Reuse News, (26), 20-23. wastewater treatment facilities. Water Research, 11, Gerba, C. P. and Goyal, S. M. (1978). Detection and 181-188. occurrence of enteric viruses in shellfish: a review. Journal Fannin, K. F., Spendlove, J. C., Cochran, K. W. and Gannon, of Food Protection, 41, 743-754. J. J. (1976). Airborne coliphages from wastewater Gerba, C. P., Goyal, S. M., Hurst, C. J. and LaBelle, R. L. treatment facilities. Applied and Environmental (1980). Type and strain dependence of enterovirus Microbiology, 31, 705-710. adsorption to activated sludge, soils and estuarine Farrah, S. R., Goyal, S. M., Gerba, C. P., Conklin, R. H. and sediments. Water Research, 14, 1197-1198. Smith, E. M. (1978). Comparison between adsorption of Gerba, C. P., Goyal, S. M., LaBelle, R. L., Cech, I. and poliovirus and rotavirus by aluminum hydroxide and Bodgan, G. F. (1979). Failure of indicator bacteria to activated sludge flocs. Applied and Environmental reflect the occurrence of enteroviruses in marine waters. Microbiology, 35, 360-363. American Journal of Public Health, 69, 1116-1119. Fattal, B. and Nishmi, M. (1977). Enterovirus types in Israel Gerba, C. P., Goyal, S. M., Smith, E. M. and Melnick, J. L. sewage. Water Research, 11, 393-396. (1977). Distribution of viral and bacterial pathogens in a Feachem, R. G., Bradley, D. J., Garelick, H. and Mara, D. D. coastal canal community. Marine Pollution Bulletin, 8, (1980). Health Aspects of Excreta and Sullage 279-282. Management-A State-of-the-Art Review. Appropriate Gerba, C. P. and Lance, J. C. (1978). Poliovirus removal from Technology for Water Supply and Sanitation, vol. 3. primary and secondary sewage effluent by soil filtration. Washington, D.C.: World Bank, Transportation, Water Applied and Environmental Microbiology, 36, 247-251. and Telecommunications Department. Gerba, C. P., Sobsey, M. D., Wallis, C. and Melnick, J. L. Fenters, J., Reed, J., Lue-Hing, C. and Bertucci, J. (1979). (1974). Enhancement of poliovirus adsorption in waste- Inactivation of viruses by digested sludge components. water onto activated carbon. In Virus Survival in Water and Journal of the Water Pollution Control Federation, 51, Wastewater Systems, eds. Malina, J. F. and Sagik, B. P., pp. 689-694. 115-126. Austin, Texas: Center for Research in' Water Francis, T., Brown, G. C. and Ainslie, J. D. (1953). Resources, University of Texas at Austin. Poliomyelitis in Hidalgo County, Texas, 1948: po- Gerba, C. P., Stagg, C. H. and Abadie, M. G. (1978). liomyelitis and coxsackie viruses in privy specimens. Characterization of sewage solid-associated viruses and American Journal of Hygiene, 58, 310 318. behavior in natural waters. Water Research, 12, 805-812. Froeschle, J. E., Feorino, P. M. and Gelfand, H. M. (1966). A Gerba, C. P., Wallis, C. and Melnick, J. L. (1975a). Fate of continuing surveillance of enterovirus infection in healthy wastewater bacteria and viruses in soil. Journal of the children in six United States cities: surveillance of Irrigation and Drainage Division, American Society of Civil enterovirus isolates 1960-1963 and comparison with Engineers, 101, 157-174. enterovirus isolates from cases of acute central nervous (1975b). Microbiological hazards of household ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 167 toilets: droplet production and the fate of residual adenovirus type 3. CJeskoslovenskd Epidemiologie, organisms. Applied Microbiology, 30, 229-237. Mikrobiologie, Imunologie, 25, 321-325. (1977a). Disinfection of wastewater by photodynamic Hejkal, T. W., Wellings, F. M., LaRock, P. A. and Lewis, A. L. oxidation. Journal of the Water Pollution Control (1979). Survival of poliovirus within organic solids during Federation, 49, 575-583. chlorination. Applied and Environmental Microbiology, 38, (1977b). Application of photodynamic oxidation to 114-118. the disinfection of tapwater, seawater and sewage Hetrick, F. M. (1978). Survival of human pathogenic viruses contaminated with poliovirus. Photochemistry and in estuarine and marine waters. American Society for Photobiology, 26, 499-504. Microbiology News, 44, 300-303. Gilbert, R. G., Gerba, C. P., Rice, R. C., Bouwer, H., Wallis, C. Heyward, A. A., Swartz, R. G., Munger, S. F. and Condon, J. and Melnick, J. L. (1976a). Virus and bacteria removal (1977). Virus removal in three secondary wastewater from wastewater by land treatment. Applied and treatment plant systems. Abstract Q48. Abstracts of the Environmental Microbiology, 32, 333-338. Annual Meeting of the American Societyfor Microbiology. Gilbert, R. G., Rice, R. C., Bouwer, H., Gerba, C. P., Wallis, Washington, D.C. C. and Melnick, J. L. (1976b). Wastewater renovation and Heyward, A. A., Swartz, R. G., Munger, S. F. and Cooney, M. reuse: virus removal by soil filtration. Science, 192, K. (1979). Viruses associated with combined sewer 1004-1005. overflows and storm water overflows in the city of Seattle. Glass, J. S. and O'Brien, R. T. (1980). Enterovirus and Abstract Q5. Abstracts of the Annual Meeting of the coliphage inactivation during activated sludge treatment. American Society .for Microbiology. Washington, D. C. Water Research, 14, 877-882. Hillis, A. (1979). A mathematical model for the epidemiologic Goncharuk, E. I., Grigoryeva, L. V., Bey, T. V., Shulyak, E. V. study of infectious diseases. International Journal of and Korchak, G. I. (1970). Removal of certain enteric Epidemiology, 8, 167-176. viruses and bacteria from sewage in a circulation oxidizing Hoff, J. C. and Becker, R. C. (1969). The accumulation and channel. Gigiena i Sanitariya, 35, 32-36. elimination of crude and clarified poliovirus suspensions Goyal, S. M. and Gerba, C. P. (1979). Comparative by shellfish. American Journal of Epidemiology, 90, 53-61. adsorption of human enteroviruses, simian rotavirus and Hughes, J. M., Merson, M. H. and Gangarosa, E. J. (1977). selected bacteriophages to soils. Applied and The safety of eating shellfish. Journal of the American Environmental Microbiology, 38, 241-247. Medical Association, 237, 1980-1981. Goyal, S. M., Gerba, C. P. and Melnick, J. L. (1978). Hurst, C. J., Farrah, S. R., Gerba, C. P. and Melnick, J. L. Prevalence of human enteric viruses in coastal canal (1978). Development of quantitative methods for the communities. Journal of the Water Pollution Control detection of enteroviruses in sewage sludges during Federation, 50, 2247-2256. activation and following land disposal. Applied and (1979). Human enteroviruses in oysters and their Environmental Microbiology, 36, 81-89. overlying waters. Applied and Environmental Microbiology, Hurst, C. J. and Gerba, C. P. (1980). Stability of simian 37, 572-581. rotavirus in fresh and estuarine water. Applied and Goyal, S. M. and Melnick, J. L. (1978). Capacity of soils to Environmental Microbiology, 39, 1-5. adsorb enteroviruses. Abstract Q15. Abstracts of the Hurst, C. J., Gerba, C. P. and Lance, J. C. (1979). Effect of Annual Meeting of the American Societyfor Microbiology. environmental conditions on enterovirus survival in soil. Washington, D.C. Abstract Q47. Abstracts of the Annual Meeting of the Grabow, W. 0. K. and Isaacson, M. (1978). Microbiological American Societyfor Microbiology. Washington, D.C. quality and epidemiological aspects of reclaimed water. Jenkins, S. R., Copperthite, C. A., Barton, J. L. and Jordan, C. Progress in Water Technology, 10, 329-335. G. (1980). Removal of bacteriophage Escherichia coli Tl Grabow, W. 0. K., Middendorff, I. G. and Basson, N. C. by sand columns using Ca2 as a filter aid. Water Research, (1978). Role of lime treatment in the removal of bacteria, 14, 437-440. enteric viruses and coliphages in a wastewater reclamation Jhala, C. I., Goel, R. K. D. and Dave, S. K. (1979). plant. Applied and Environmental Microbiology, 35, Epidemiology of poliomyelitis in rural area of Gujarat: a 663-669. report of house to house survey in Patan Taluka. Indian Grigoryeva. L. V., Korchak. G. 1. and Bey, T. V. (1969). Journal of Medical Sciences, 33, 143-149. Survival of bacteria and viruses in sewage sludges. John, T. J. and Jayabal, P. (1972). Oral polio vaccination of Mikrobiologichnyi Zhurnal, 31, 659-664. children in the tropics. I. The poor seroconversion rates Hajenian, H. and Butler, M. (1980). Inactivation of f2 and the absence of viral interference. American Journal of coliphage in municipal effluent by the use of various Epidemiology, 96, 263-269. disinfectants. Journal of Hygiene, 84, 247-255. Joyce, G. and Weiser, H. H. (1967). Survival of enteroviruses Hedstr6m, C. E. and Lycke, E. (1964). An experimental study and bacteriophage in farm pond waters. Journal of the on oysters as virus carriers. American Journal of Hygiene, American Water Works Association, 59, 491-501. 79, 134-142. Kamlet, K. S. (1979). Superchlorination of sewage sludge: Heinz, F., Bindas, B., Cervenka, P. and Zdebska, E. (1976). adding injury to insult? Sludge, 2, 16-18, 27-31. Epidemics of swimming pool conjunctivitis caused by Kapuscinski, R. B. and Mitchell, R. (1980). Processes 168 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES controlling virus inactivation in coastal waters. Water of wastewater by soil columns flooded with primary Research, 14, 363-371. effluent. Journal ofthe Water Pollution Control Federation, Katzenelson, E. (1978). Survival of viruses. In Indicators of 52, 381-388. Viruses in Water and Food, ed. Berg. G., pp. 39-50. Ann Landry, E. F., Vaughn, J. M., Thomas, M. Z. and Beckwith, Arbor, Mich.: Ann Arbor Science Publishers. C. A. (1979). Adsorption of enteroviruses to soil cores and Katzenelson, E. and Biedermann, N. (1976). Disinfection of their subsequent elution by artificial rainwater. Applied viruses in sewage by ozone. Water Research, 10, 629-631. and Environmental Microbiology, 38, 680-687. Katzenelson, E., Buium, I. and Shuval, H. I. (1976). Risk of Larkin, E. P. and Fassolitis, A. C. (1979). Viral heat resistance communicable disease infection associated with waste- and infectious ribonucleic acid. Applied and Environmental water irrigation in agricultural settlements. Science, 194, Microbiology, 38, 650-655. 944-946. Larkin, E. P., Tierney, J. T. and Sullivan, R. (1976). Katzenelson, E. and Kedmi, S. (1979). Unsuitability of Persistence of virus on sewage-irrigated vegetables. polioviruses as indicators of virological quality of water. Jour nal oj the Environmental Engineering Division. Applied and Environmental Microbiology, 37, 343-344. American Society of Civil Engineers, 102, 29-35. Kawata, K., Cramer, W. N. and Burge, W. D. (1977). Lefler, E. and Kott, Y. (1974a). Virus retention and survival Composting destroys pathogens. Water and Se age in sand. In Virus Survival in Water and Wastewater Systems, Works, 124, 76-79. eds. Malina, J. F. and Sagik, B. P., pp. 84-91. Austin, Keswick, B. H. and Gerba, C. P. (1980). Viruses in Texas: Center for Research in Water Resources, groundwater Environmental Science and Technology, 14, University of Texas at Austin. 1290-1297. (1974b). Enteric virus behavior in sand dunes. Israel Kirkpatrick, W. R. and Presecan, N. L. (1978). Filtration Journal of Technology, 12, 298-304. reduces bacteria and viruses in secondary effluent. Water (1975). Virus survival in water and wastewater. Israel and Sewage Works, reference number, R10-R21. Journal of Medical Science, 11, 511-512. Konowalchuk, J. and Speirs, J. I. (1975a). Survival of enteric (1976). Effect of wastewater effluents on the elution of viruses on fresh vegetables. Journal of Milk and Food viruses adsorbed on sand columns. Israel Journal of Technology, 38, 469-472. Medical Science, 12, 710. (1975b). Survival of enteric viruses on fresh fruit. Lessel, T. and Suess, A. (1978). Hygienization of sewage Journal of Milk and Food Technology, 38, 598-600. sludge by gamma radiation: experience with an operating (1977). Virus detection on grapes. Canadian Journal plant. Progress in Water Technology, 10, 641-652. of Microbiology, 23, 1301-1303. Levin, M. (1978). Fish and shellfish associated disease Kott, H. and Fishelson, L. (1974). Survival of enteroviruses outbreaks. Journal of the Water Pollution Control on vegetables irrigated with chlorinated oxidation pond Federation, 50, 1377-1381. effluents. Israel Journal of Technology, 12, 290-297. Lindeman, S. and Kott, Y. (1971). The effect of chlorination Kott, Y., Ben-Ari, H. and Betzer, N. (1978). Lagooned, on enteroviruses in the effluents of the Haifa sewage secondary effluents as water source for extended treatment plant. Israel Journal oj Medical Sciences, 7, agricultural purposes. Water Research, 12, 1101-1106. 1111. Kott, Y., Ben-Ari, H. and Vinokur, L. (1978). Coliphage Loh, P. C., Fujioka, R. S. and Lau, L S. (1979). Recovery, survival as viral indicator in various wastewater quality survival and dissemination of human enteric viruses in effluents. Progress in Water Technology, 10, 337-346. ocean waters receiving sewage in Hawaii. Water, Air and Kott, Y., Roze, N., Sperber, S. and Betzer, N. (1974). Soil Pollution, 12, 197-217. Bacteriophages as viral pollution indicators. Water Lund, E. (1973). The effect of pretreatments on the virus Research, 8, 165-171. contents of sewage samples. Water Research, 7, 873-879. Krige, P. R. (1964). A survey of the pathogenic organisms and (1976). Disposal of sludges. In Viruses in Water, eds. helminthic ova in composts and sewage sludge. Journal of Berg, G., Bodily, H. L., Lennette, E. H., Melnick, J. L. and the Institute of Sewage Purification, Part 3, 215-220. Metcalf, T. G., pp. 196-205. Washington, D.C.: American LaBelle, R. L. and Gerba, C. P. (1979). Influence of pH, Public Health Association. salinity and organic matter on the adsorption of enteric (1979). The survival of viral pathogens in water and viruses to estuarine sediment. Applied and Environmental waste in the tropics. Progress in Water Technology, 11, Microbiology, 38, 93-101. 73-79. Lance, J. C. and Gerba, C. P. (1980). Poliovirus movement Lund, E. and Ronne, V. (1973). On the isolation ofvirus from during high-rate land filtration of sewage water. Journal of sewage treatment plant sludges. Water Research. 7, Environmental Quality, 9, 31-34. 863-871. Lance, J. C., Gerba, C. P. and Melnick, J. L. (1976). Virus Lydholm, B. and Nielsen, A. L. (1980). Methods for detection movement in soil columns flooded with secondary sewage of virus in wastewater. applied to samples from small scale effluent. Applied and Environmental Microbiology, 32, treatment systems. Water Research, 14, 169-173. 520-526. Madeley, C. R. (1979). Viruses in stools. Journal of Clinical Lance,J. C., Rice, R. C. and Gilbert, R. G. (1980). Renovation Pathology, 32, 1-10. ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 169 Mahdy, M. S. (1979). Viruses in the water environment: an poliovirus by the Eastern oyster. American Journal of underestimated problem. Journal of the American Water Fpidemiology, 84, 40-50. Works Association, 71, 445-449. Montefiore, D., Jamieson, M. F., Collard, P. and Jolly, H. Malherbe, H. H. and Strickland-Cholmley, M. (1967). (1963). Trial of type 1 oral poliomyelitis vaccine (Sabin) in Quantitative studies on viral survival in sewage Nigerian children. British Medical Journal, 1, 1569-1572. purification processes. In Transmission of Viruses by the Moore, B. E. D., Funderberg, L., Sagik, B. P. and Malina, J. Water Route, ed. G. Berg, pp. 379-388. New York: Wiley F. (1974). Application of viral concentration techniques to Interscience. field sampling. In Virus Survival in Water and Wastewater Malina, J. F., Ranganathan, K. R., Moore, B. E. and Sagik, B. Systems, eds. Malina, J. F. and Sagik, B. P., pp. 3-15, P. (1974). Poliovirus inactivation by activated sludge. In Austin, Texas: Center for Research in Water Resources, Virus Survival in Water and Wastewater Systems, eds. University of Texas at Austin. Malina. J. F. and Sagik, B. P., pp. 95-106. Austin, Texas: Moore, B. E., Sagik, B. P. and Malina, J. F. (1975). Viral Center for Research in Water Resources, University of association with suspended solids. Water Research, 9, Texas at Austin. 197-203. Malina, J. F., Ranganathan, K. R., Sagik, B. P. and Moore, B. Moore, B. E., Sagik, B. P. and Sorber, C. A. (1979). Procedure E. (1975). Poliovirus inactivation by activated sludge. for the recovery of airborne human enteric viruses during Journal oJ the Water Pollution Control Federation, 47, spray irrigation of treated wastewater. Applied and 2178-2183. Environmental Microbiology, 38, 688-693. Marzouk, Y., Goyal, S. M. and Gerba, C. P. (1979). Moore, R. S., Taylor, D. H., Sturman, L. S. and Reddy, M. M. Prevalence of enteroviruses in groundwater of Israel. (1979). pH and ionic effects on poliovirus interaction with Ground Water, 17, 487-491. three soils. Abstract Q46. Abstracts of the Annual Meeting Matossian, A. M. and Garabedian, G. A. (1967). Virucidal of the American Society for Microbiology. Washington, action of sea water. American Journal of Epidemiology, 85, D.C. 1-8. Morris, R. and Waite, W. M. (1980). Evaluation of Melnick, J. L. (1976). Viruses in water. In Viruses in Water, procedures for recovery of viruses from water. II. Detection eds. Berg, G., Bodily, H. L., Lennette, E. H., Melnick, J. L. systems. Water Research, 14, 795-798. and Metcalf, T. G., pp.3- l. Washington, D.C.: American Munger, S. F., Heyward, A. A. and Swartz, R. G. (1977). Public Health Association. Inactivation of virus by chlorination or ozonation in four Melnick, J. L. and Dow, R. P. (1953). Poliomyelitis in wastewater treatment system effluents. Abstract Q47. Hildalgo County, Texas, 1948: poliomyelitis and coxsac- Abstracts of the Annual Meeting of the American Societyfor kie viruses from flies. American Journal of Hygiene, 58, Microbiology. Washington, D.C. 288-309. Naparstek, J. D., Olivieri, V. P., Kawata, K. and Sherman, V. Melnick, J. L., Gerba, C. P. and Wallis, C. (1978). Viruses in R. (1976). Virus removal in an activated sludge plant. water. Bulletin of the World Health Organization, 56, Water and Sewage Works, 123, R16 and R20. 499-508. Nielsen, A. L. and Lydholm, B. (1980). Methods for the Metcalf, T. G. (1977). Control of Virus Pathogens in Municipal isolation of virus from raw and digested wastewater sludge. Waste Water and Residuals by Irradiation with High Energy Water Research. 14, 175-178. Electrons. Report PB 272347. Springfield, Virginia: US Niemi, M. (1976). Survival of Escherichia coli phage T7 in National Technical Information Service. different water types. Water Research, 10, 751-755. (1978). Indicators of viruses in shellfish. In Indicators Nupen, E. M. (1970). Virus studies on the Windhoek oJ Viruses in Water and Food, ed. Berg, G., pp. 383-415. wastewater reclamation plant (South West Africa). Water Ann Arbor, Mich.: Ann Arbor Science Publishers. Research, 4, 661-672. Metcalf, T. G. and Stiles, W. C. (1965). The accumulation of Nupen, E. M., Bateman, B. W. and McKenny, N. C. (1974). enteric viruses by the oyster, Crassostrea virginica. Journal The reduction of virus by the various unit processes used in of Infectious Diseases, 115, 68-76. the reclamation of sewage to potable waters. In Virus (1968). Enteroviruses within an estuarine environ- Survival in Water and Wastewater Systems, eds. Malina, J. ment. American Journal of Epidemiology, 88, 379-391. F. and Sagik, B. P., pp. 107-114. Austin, Texas: Center for Metcalf, T. G., Wallis, C. and Melnick, J. L. (1974). Virus Research in Water Resources, University of Texas at enumeration and public health assessments in polluted Austin. surface water contributing to transmission of virus in O'Brien, R. T. and Dacus, J. M. (1978). Viral changes nature. In Virus Survival in Water and Wastewater Systems, associated with inactivation in freshwater and marine eds. Malina, J. F. and Sagik, B. P., pp. 57-70. Austin, environments. Abstract N29. Abstracts of the Annual Texas: Center for Research in Water Resources, University Meeting of the American Society for Microbiology. of Texas at Austin. Washington, D.C. Metselaar, D. (1968). Virology and public health. East O'Brien, R. T. and Newman, J. S. (1977). Inactivation of African Medical Journal, 45, 597-604. polioviruses and coxsackieviruses in surface water. Applied Mitchell, J. R., Presnell, M. W., Akin, E. W., Cummins, J. M. and Environmental Microbiology, 33, 334 340. and Liu, 0. C. (1966). Accumulation and elimination of Olivieri, V. P., Donovan, T. K. and Kawata, K. (1971). 170 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Inactivation of virus in sewage. Journal of the Sanitarv population under conditions of massive enteric infection Engineering Division, American Society of Civil Engineers, with other viruses. Journal of the American Medical 97, 661-673. Association, 173, 1521-1526. Osborn, D. W. and Hattingh, W. H. J. (1978). Disinfection of Sadovski, A. Y., Fattal, B. and Goldberg, D. (1978). sewage sludge: a review. Water South Africa, 4, 169-178. Microbial contamination of vegetables irrigated with Otatume, S. and Addy, P. A. K. (1975). Ecology of sewage effluent by the drip method. Journal of Food enteroviruses in tropics. I. Circulation of enteroviruses in Protection, 41, 336-340. healthy infants in tropical urban area. Japanese Journal of Sadovski, A. Y., Fattal, B., Goldberg, D., Katzenelson, E. and Microbiology, 19, 201-209. Shuval, H. I. (1978). High levels of microbial con- Pavoni, J. L. and Tittlebaum, M. E. (1974). Virus inactivation tamination of vegetables irrigated with wastewater by the in secondary wastewater treatment plant effluent using drip method. Applied and Environmental Microbiology, 36, ozone. In Virus Survival in Water and Wastewater Systems, 824-830. eds. Malina, J. F. and Sagik, B. P., pp. 180-197. Austin, Safferman, R. S. and Morris, M. E. (1976). Assessment of Texas: Center for Research in Water Resources, virus removal by a multi-stage activated sludge process. University of Texas at Austin. Water Research, 10, 413-420. Payment, P., Gerba, C. P., Wallis, C. and Melnick, J. L. Sanders, D. A., Malina, J. F., Moore, B. E., Sagik, B. P. and (1976). Methods for concentrating viruses from large Sorber, C. A. (1979). Fate of poliovirus during anaerobic volumes of estuarine water on pleated membranes. Water digestion. Journal of the Water Pollution Control Research, 10, 893-896. Federation, 51, 333-343. Peradze, T., Montefiore, D. and Coker, G. (1968). Oral Sattar, S. A. and Westwood, J. C. N. (1977). Isolation of poliovirus vaccination and breast feeding. West African apparently wild strains of poliovirus type 1 from sewage in Medical Journal, 17, 122-124. the Ottawa area. Canadian Medical Association Journal, Pietri, C. and Breittmayer. J. P. (1976). Etude de la survie 116, 25-27. d'un enterovirus en eau de mer. Revue Internationale (1978). Viral pollution of surface waters due to d'Oceanographie Medicale, 41/42, 77-86. chlorinated primary effluents. Applied and Environmental Poliomyelitis Commission (1966). Poliomyelitis vaccination Microbiology, 36, 427-431. in Ibadan, Nigeria, during 1964 with oral vaccine (Sabin (1979). Recovery of viruses from field samples of raw, strains). Bulletini of the World Health Organization, 34, digested and lagoon-dried sludges. Bulletin of the World 865-876. Health Organization, 57, 105-108. Rakness, K. L. and Hegg, B. A. (1979). Field-scale evaluation Schaub, S. A., Kenyon, K. F., Bledsoe, B. and Thomas, R. E. for ozone wastewater disinfection. Water and Sewage (1980). Evaluation of the overland runoff mode of land Works, 126, 82-84. wastewater treatment for virus removal. Applied and Rao, V. C., Kumaran, P., Lakhe, S. B., Dube, P. and Rao, N. Environmental Microbiology, 39, 127-134. U. (1973). Virus removal in sewage treatment pilot plants. Schaub, S. A. and Sagik, B. P. (1975). Association of I. Oxidation ditch. In Proceedings of a Symposium on enteroviruses with natural and artificially introduced Environmental Pollution, pp. 174-180. Nagpur, India: colloidal solids in water and infectivity of solids-associated Central Public Health Engineering Research Institute. virions. Applied Microbiology. 30, 212-222 Rao, V. C., Lakhe, S. B. and Waghmare, S. V. (1978). Schaub, S. A. and Sorber, C. A. (1977). Virus and bacteria Developments in environmental virology in India. Indian removal from wastewater by rapid infiltration through Associationfbr Water Pollution Control Technical Annual, soil. Applied and EnvironmentalMicrobiology, 33,609-619. 5, 1-16. Schaub, S. A., Sorber, C. A. and Taylor, G. W. (1974). The Rao, V. C., Lakhe, S. B., Waghmare, S. V. and Dube, P. association of enteric viruses with natural turbidity in the (1977). Virus removal in activated sludge sewage aquatic environment. In Virus Survival in Water and treatment. Progress in Water Technology, 9, 113-127. Wastewater Systems, eds. Malina, J. F. and Sagik, B. P., pp. Roberts, M. J., Haggerty, P. G. and Johnson, J. C. (1976). 71-83. Austin, Texas: Center for Research in Water Survival of poliovirus, type 2, W-2 in natural water sources Resources, University of Texas at Austin. obtained from southeastern Virginia. Virginia Journal of Scheuerman, P. R., Bitton, G., Overman, A. R. and Gifford, Science, 27, 91. G. E. (1979). Transport of viruses through organic soils Ruiter, G. G. and Fujioka, R. S. (1978). Human enteric and sediments. Journal of the Environmental Engineering viruses in sewage and their discharge into the ocean. Water, Division, American Society of Civil Engineers, 105, 629-640. Air and Soil Pollution, 10, 95-103. Schmidt, N. J., Ho, H. H., Riggs, J. L. and Lennette, E. H. Sabin, A. B. (1980). Vaccination against poliomyelitis in (1978). Comparative sensitivity of various cell culture economically underdeveloped countries. Bulletin of the systems for isolation of viruses from wastewater and fecal World Health Organization, 58, 141-157. samples. Applied and Environmental Microbiology, 36, Sabin, A. B., Ramos-Alvarez, M., Alvarez-Amezquita, J., 480-486. Pelon, W., Michaels, R. H., Spigland, I., Koch, M. A., Sery, V., Thraenhart, O., 2acek, K., Brogger, S., Omar, A. and Barnes, J. M. and Rhim, J. S. (1960). Live, orally given Saboor, A. (1970). Basis for poliomyelitis surveillance in poliovirus vaccine: effects of rapid mass immunization on Kabul City. Z.,,.,1l ,r,,r Bakteriologie, Parasitenkunde. ENTEROVIRUSES, POLIOMYELITIS, AND SIMILAR INFECTIONS 171 Infektionskrankheiten und Hygiene, 1 213, 311-318. construction of wastewater reclamation schemes as an Sherman, V. R., Kawata, K., Olivieri, V. P. and Naperstek, J. integral part of water supply. In Water Wastes and Health D. (1975). Virus removals in trickling filter plants. Water in Hot Climates, eds. Feachem, R., McGarry, M., and and Sewage Works, 122, R36-R44. Mara, D., pp. 383-391. Chichester: John Wiley. Shuval, H. I. (1975). The case for microbial standards for Subrahmanyan, T. P. (1977). Persistence of enteroviruses in bathing beaches. In Discharge of Sewagefrom Sea Outfalls, sewage sludge. Bulletin of the World Health Organization, ed. Gameson, A. L. H., pp. 95-101. Oxford: Pergamon. 55, 431-434. (1978). Studies on bacterial and viral contamination Sullivan, R., Fassolitis, A. C., Larkin, E. P., Read, R. B. and of the marine environment. Revue Internationale Peeler, J. T. (1971). Inactivation of thirty viruses by gamma d'Oceanographie Medicale, 50, 43-50. radiation. Applied Microbiology, 22, 61-65. Shuval, H. I., Cymbalista, S., Wachs, A., Zohar, Y. and Teltsch, B. and Katzenelson, E. (1978). Airborne enteric Goldblum, N. (1966). The inactivation of enteroviruses in bacteria and viruses from spray irrigation with wastewater. sewage by chlorination. In Proceedings of the Third Applied and Environmental Microbiology, 35, 290-296. International Conference on Water Pollution Research. pp. Thraenhart, O., Omar, A., Habib, A. and Miakhail, M. R. 37-44. Washington, D.C.: Water Pollution Control (1970). Poliomyelitis surveillance in Kabul City. Federation. Zentralblatt fur Bakteriologie, Parasitenkunde, Infek- Slade, J. S. and Edworthy, K. J. (1981). Virology of tionskrankheiten und Hygiene, 1, 213, 319-324. wastewater recharge of the chalk aquifer. II. Microbiology Tierney, J. T., Sullivan, R. and Larkin, E. P. (1977). and water quality. In Viruses and Wastewater Treatment, Persistence of poliovirus 1 in soil and on vegetables grown eds. Goddard, M. and Butler, M. Oxford: Pergamon. in soil previously flooded with inoculated sewage sludge or Slanetz, L. W., Bartley, C. H., Metcalf, T. G. and Nesman, R. effluent. Applied and Environmental Microbiology, 33, (1970). Survival of enteric bacteria and viruses in 109-113. municipal sewage lagoons. In Proceedings of the Second Vaughn, J. M., Landry, E. F., Baranosky, L. J., Beckwith, C. International Symposium Jor Water Treatment Lagoons, A., Dahl, M. C. and Delihas, N. C. (1978). Survey of human ed. McKinney, R. E., pp. 132-141. Kansas City: Missouri virus occurrence in wastewater-recharged groundwater on Basin Engineering Health Council. Long Island. Applied and Environmental Microbiology, 36, Small-Scale Waste Management Project (1978). 47-51. Management of Small Waste Flows. Report EPA-600/2-78- Vaughn, J. M., Landry, E. F., Thomas, M. Z., Vicale, T. J. and 173. Cincinnati, Ohio: US Environmental Protection Penello, W. F. (1979a). Survey of human enterovirus Agency. occurrence in fresh and marine surface waters on Long Smith, E. M., Gerba, C. P. and Melnick, J. L. (1978). Role of Island. Applied and Environmental Microbiology, 38, sediment in the persistence of enteroviruses in the estuarine 290-296. environment. Applied and Environmental Microbiology, 35, Vaughn, J. M., Landry, E. F., Vicale, T. J. and Dahl, M. C. 685-689. (1979b). Modified procedure for the recovery of naturally Snead, M. C., Olivieri, V. P., Kawata, K. and Kruse, C. W. accumulated poliovirus from oysters. Applied and (1980). The effectiveness of chlorine residuals in in- Environmental Microbiology, 38, 594-598. activation of bacteria and viruses introduced by post- Vaughn, J. M. and Metcalf, T. G. (1975). Coliphages as treatment contamination. Water Research, 14, 403-408. indicators of enteric viruses in shellfish and shellfish raising Sorber, C. A., Schaub, S. A. and Bausum, H. T. (1974). An estuarine waters. Water Research, 9, 613-616. assessment of a potential virus hazard associated with Vilker, V. L. and Burge, W. D. (1980). Adsorption mass spray irrigation of domestic wastewaters. In Virus Survival transfer model for virus transport in soils. Water Research, in Water and Wastewater Systems, eds. Malina, J. F. and 14, 783-790. Sagik, B. P., pp. 241-252. Austin Texas: Center for Wallis, C. and Melnick, J. L. (1967). Concentration of viruses Research on Water Resources, University of Texas at on aluminum and calcium salts. American Journal of Austin. Epidemiology, 85, 459-468. Sproul, 0. J. (1976). Removal of viruses by treatment Ward, R. L. (1977). Inactivation of poliovirus in wastewater processes. In Viruses in Water, eds. Berg, G., Bodily, H. L., sludge with radiation and thermoradiation. Applied and Lennette, E. H., Melnick, J. L. and Metcalf, T. G., pp. Environmental Microbiology, 33, 1218-1219. 167-179. Washington, D.C.: American Public Health Ward, R. L. and Ashley, C. S. (1976). Inactivation of Association. poliovirus in digested sludge. Applied and Environmental (1980). Critical Review of Virus Removal by Microbiology, 31, 921-930. Coagulation Processes and pH Modifications. Report EPA- (1977a). Indentification of the virucidal agent in 600/2-80-004. Cincinnati, Ohio: US Environmental wastewater sludge. Applied and Environmental Protection Agency. Microbiology, 33, 860-864. Stagg, C. H., Wallis, C., Ward, C. H. and Gerba, C. P. (1978). (1977b). Inactivation of enteric viruses in wastewater Chlorination of solids-associated coliphages. Progress in sludge through dewatering by evaporation. Applied and Water Technology, 10, 381-387. Environmental Microbiology, 34, 564-570. Stander, G. J. and Clayton, A. J. (1977). Planning and (1977c). Discovery of an agent in wastewater sludge 172 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES that reduces the heat required to inactivate reovirus. Wiley, B. B. and Westerberg, S. C. (1969). Survival of human Applied and Environmernal Microbiology, 34, 681-688. pathogens in composted sewage Applied Microbiology, 18, (1978a). Identification of detergents as components 994-1001. of wastewater sludge that modify the thermal stability of Wolf, H. W., Safferman, R. S., Mixson, A. R. and Stringer, C. reovirus and enteroviruses. Applied and Environmental E. (1974). Virus inactivation during tertiary treatment. In Microbiology, 36, 889-897. Virus Survival in Water and Wastewater Systems, eds. (1978b). Heat inactivation of enteric viruses in Malina, J. F. and Sagik, B. P., pp. 145-157. Austin, Texas: dewatered wastewater sludge. Applied and Environmental Center for Research in Water Resources, University of Microbiology, 36, 898-905. Texas at Austin. - (1979). pH modification of the effects ofdetergentson Won, W. D. and Ross, H. (1973). Persistence of virus and the stability of enteric viruses. Applied and Environmental bacteria in seawater. Journal of the Envlironmental Microbiology, 38, 314-322. Engineering Division, American Society oJ Civil Engineers, Ward, R. L., Ashley, C. S. and Moseley, R. H. (1976). Heat 99, 205-211. inactivation of poliovirus in wastewater sludge. Applied Wood, P. C. (1979). Public health aspects of shellfish from and Environmental Microbiology, 32, 339-346. polluted water. In Biological Indicators of Water Quality, Watson, P. G. (1977). A virological survey of polluted eds. James, A. and Evison, L., pp. 13/1-13/18. Chichester: seawater. Journal of Applied Bacteriology, 43, 11-12. John Wiley. Wetlings, F. M., Lewis, A. L. and Mountain, C. W. (1974). Yeager, J. G. and O'Brien, R. T. (1977). Enterovirus and Virus survival following wastewater spray irrigation of bacteriophage inactivation in groundwater and translo- sandy soils. In Virus Survival in Water and Wastewater cation in soil. Abstract N57. Abstracts of the Annual Systems, eds. Malina, J. F. and Sagik, B. P., pp. 253-260. Meetinig of the American Society jbr Microbiology. Austin, Texas: Center for Research in Water Resources, Washington, D.C. University of Texas at Austin. (1979a). Enterovirus inactivation in soil. Applied and (1976). Demonstration of solids-associated virus in Environmental Microbiology, 38, 694-701. wastewater and sludge. Applied and Entvironmental (1979b). Structural changes associated with po- Microbiology, 31, 354-358. liovirus inactivation in soil. Applied and Environmental Wellings, F. M., Lewis, A. L., Mountain, C. W. and Pierce, L. Microbiology, 38, 702-709. V. (1975). Demonstration of virus in groundwater after Young, D. C. and Sharp, D. G. (1977). Poliovirus aggregates effluent discharge onto soil. Applied Microbiology. 29, and their survival in water. Applied and Environmental 751-757. Microbiology, 33, 168-177. Wellings, F. M., Mountain, C. W. and Lewis, A. L. (1976). Zdrazilek, J., Sramova, H. and Hoffmanova, V. (1977). Virus in groundwater. In Second National Conference on Comparison of poliovirus detection in sewage and stool Individual On-site Wastewater Systems, pp. 61-65. Ann samples: a study in a creche in the third week after Arbor, Mich.: National Sanitation Foundation. vaccination. International Journal of Epidemiology, 6, WHO (1979). Human Viruses in Water, Wastewater and Soil. 169-172. Technical Report Series no. 639. Geneva: World Health Organization. 10 Hepatitis A Virus and Infectious Hepatitis MUCH OF THE WORK on poliovirus and other Recently a third form of viral hepatitis has been enteroviruses in the environment described in chapter described: non-A:non-B hepatitis. This new form of 9 was inspired by an interest in other excreted viruses hepatitis is now known to be the most common type of that cause major public health problems but cannot be post-transfusion hepatitis in some areas. Non-A: non-B routinely isolated at the present time. Foremost among hepatitis may prove to be divisible into more than one these other excreted viruses is hepatitis A virus, which form. As far as is known, only hepatitis A is primarily is a common and important cause of disease an excreted infection, and therefore it alone will be throughout the world. discussed in this chapter. The study of the hepatitis viruses is a rapidly moving field of research hepatitis A virus was not identified in fecal extracts until 1973, although the Identfication disease it causes has been recorded by civil and military The clinical picture of viral hepatitis varies in its historians since the fifth century BC. This chapter is presentation from inapparent or subclinical infection, brief, because little is known at the time of writing about to slight malaise, mild gastrointestinal symptoms hepatitis A virus in the environment, and tentative, and the anicteric (without jaundice) form of the because the rate of scientific progress is rapid, and much disease, to acute icteric iliness, severe prolonged new information will come to light in the next few years. jaundice, and chronic liver disease. The anicteric form A recent and comprehensive account of the hepatitis is characterized by malaise, anorexia, various gastro- viruses is given by Zuckerman and Howard (1979). intestinal disturbances, an enlarged and tender liver, and perhaps a fever. In acute icteric infections these symptoms may be more pronounced and may be Description of Pathogen and Disease followed after 5-10 days by dark urine, clay-colored stools, and jaundice, which persists commonly for 1-2 Two distinct forms of viral hepatitis have been weeks. Typically, the disease is especially mild in recognized: hepatitis A (also known as infectious children, for whom the ratio of anicteric to icteric hepatitis, epidemic hepatitis, or epidemic jaundice) illness may be 10 or more to 1. Convalescence usually is and hepatitis B (also known as serum hepatitis). prolonged. In general, severity increases with age, but They differ in etiology and in some epidemio- complete recovery without sequelac or recurrences is logical, immunological, clinical, and pathological the rule. Many mild cases without jaundice, especially characteristics. From the environmental viewpoint, in children, are recognizable only by liver-function or the primary distinction between them is that serum-enzyme tests. hepatitis A is transmitted by the fecal-oral route, whereas hepatitis B is normally transmitted by infected blood or tissue fluid (for instance, during blood Occurrence transfusion, injection, immunization, tattooing, and Viral hepatitis type A occurs endemically in all parts acupuncture) but may also rarely be transmitted by of the world, with frequent reports of minor and major saliva, semen, breastmilk, other body fluids, and feces if outbreaks. The exact incidence is difficult to estimate contaminated with blood. Because of these differences because of the high proportion of subclinical infections in mode of transmission, the approaches to prevention and infections without jaundice, differences in sur- and control of hepatitis A and B are very different. veillance, and differing patterns of disease. The degree 173 174 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES of underreporting is very high; even in developed Reservoirs countries with compulsory notification, it is doubtful Man is almost certainly the important reservoir for whether more than 50 percent of cases of jaundice are human hepatitis A infection. However, cases have been actually reported. Bctuause seprogia reported that suggest transmission to man from Because serological tests for hepatitis A antibody are chmaze,grls,Cebsps,ibo,an now available, it has become possible to study the chimpanzees, gorillas, Celebes apes, gibbons, and incidence and it he paisAinfections in woolly monkeys. Antibodies to hepatitis A virus are andidenceau ion vparios gfeog hicl found in nonhuman primates, and susceptible chimpan- different populations zees and marmosets are readily infected in the areas. A recent survey of sera for hepatitis A antibody laboratory. by immune adherence hemagglutination from samples of healthy adults, mostly volunteer blood donors, from seven geographical populations has shown that the age-standardized prevalence of hepatitis A antibody Transmission was 29 percent in Switzerland, 45 percent in the USA, Hepatitis A virus is spread by the fecal-oral route, 76 percent in Senegal, 81 percent in Belgium, 89 percent most commonly by person-to-person contact, and in Taiwan, 95 percent in Israel, and 97 percent in infection occurs readily in conditions of poor Yugoslavia (Szmuness and others 1977). This survey sanitation and overcrowding. Common-source out- confirmed that infections with hepatitis A virus are breaks are most frequently initiated by fecal con- widespread throughout the world. tamination of water and food, but waterborne transmission is not a major factor in the maintenance of this infection. Ingestion of shellfish cultivated in Infectious agent polluted water is associated with a high risk of Small cubic particles measuring 27 nanometers have acquiring hepatitis A. been seen by electron microscopy in infective feces of human subjects (see figure 10-1). The virus contains single-stranded RNA and has the biochemical and Incubation period biophysical properties of a picornavirus. The incubation period of hepatitis A is between 3 rx 4ib,, and 5 weeks, with a mean of 28 days. Period of communicability * t ^ , Hepatitis A virus is shed in the stools primarily - i iduring the period from 2 weeks before, to 2 weeks after, the onset of symptoms; in other words, for up to 4 weeks commencing 1-3 weeks after infection. * Persistent carriage or excretion of hepatitis A virus in humans does not occur. Resistance Susceptibility is general. Low clinical incidence in infants and preschool children suggests that mild and anicteric infections are common. The degree and duration of homologous immunity after attack are unknown but presumed to be long lasting. Figure 10-1. Hepatitis A viruses under transmission Epidemiology electronmicroscopy. Scale bar = 0.1 micrometers. (Photo: A. J. Zuckerman and A. Thornton, London All age groups are susceptible to hepatitis. Until School of Hygiene and Tropical Medicine, London, recent years the highest incidence in the civilian UK) population was observed in children of school age, but HEPATITIS A VIRUS AND INFECTIOUS HEPATITIS 175 in a number of countries, including Sweden and the USA). Antibody was not detected in any individual USA, as many as 60-70 percent of notified cases now under 20 years old, and the highest age-specific occur in adults. This shift in age incidence in the prevalence for hepatitis A antibody was 59 percent in developed countries is reminiscent of the changing the 40-49 age group. Antibody prevalences were pattern of poliomyelitis (see chapter 9) and may reflect higher among institutionalized individuals in reduced transmission, caused by improved socioecon- Philadelphia. Szmuness and others (1976) studied 947 omic conditions, which defers infection to an older age randomly selected individuals in New York City group when the clinical consequences are usually more (USA) and found an overall prevalence of hepatitis A severe. antibody of 45 percent. Lower social classes had In conditions of poor hygiene, it is probable that significantly higher prevalences (72-80 percent) than transmission of hepatitis A virus occurs among higher social classes (18-30 percent). Jews had a children by direct fecal-oral routes. This leads to a significantly lower prevalence (7 percent) than other high incidence of subclinical or very mild infections whites (39 percent), but sex and homosexuality did not that confer substantial immunity. Moritsugu and affect prevalence. Antibody prevalence was closely others (1979) found that 92 percent ofchildren under 9 related to age in all groups; for instance, among years old in Colombo (Sri Lanka) had evidence of Chinese the prevalence rose to over 90 percent by the antibodies to hepatitis A virus. In Costa Rica age of 40 years. For both blacks and whites, antibody (Villarejos and others 1976), age-specific antibody prevalence was 2.5 to 4 times lower among individuals prevalences reached 80 percent by the age of 9 years. In with postgraduate education than among those Liberia, 90 percent of children over 5 years old in both without. urban and rural areas had hepatitis A antibodies These various studies show clearly that transmission (Willcox and others 1980). Similar results have been of hepatitis A virus is more common, and thus the obtained from Kenya (Wankya and others 1979) and prevalence of antibodies among children is higher, from Fiji, Tuvalu (formerly Ellice Islands), Niue, Cook among people of lower socioeconomic and educational Islands, and Western Samoa (Gust, Lehmann and status. This relationship can be detected both between Dimitrakakis 1979). and within countries. These and other aspects of In developed countries, improved hygiene reduces hepatitis A epidemiology, as revealed by serological the incidence of hepatitis A infection in the young, but surveys, have been reviewed by Dienstag and others many people become infected at some time in life. Gust, (1978). Recent investigations of hepatitis A outbreaks Lewis and Lehmann (1978) examined the sera in day care centers in the USA have highlighted the (collected in 1954-55) of 959 people (mainly of low major role of children who are not toilet trained (those socioeconomic status) in Melbourne (Australia) and under 2 years old) in spreading the infection (Hadler found that the prevalence of those having hepatitis A 1980; Vernon 1980). antibodies as 38 percent in the 6 to 10 year olds, 56 In temperate zones the characteristic seasonal trend percent in the 20 year olds, and over 97 percent in those has been for a marked rise in incidence in the autumn over 40 years old. The sera were collected prior to mass and early winter months, with a progressive fall to a poliomyelitis vaccination campaigns, and it was found minimum in midsummer. that the age-related acquisition of poliovirus anti- bodies was extremely similar to hepatitis A antibodies. Control Measures This strengthens the possibility that the epidemiology and transmission of polio and hepatitis A infections The spread of infection is reduced by simple hygienic may be similar and that they share a common response measures and the sanitary disposal of excreta. Normal to improved hygiene. A repeat survey in Melbourne in human immunoglobulin may prevent or attenuate a 1975 found antibody prevalences of 23 percent in 6 to clinical illness but may not always prevent the 10 year olds, 45 percent in 20 year olds, and 66 to 97 infection. The use of normal immunoglobulin is of percent in those over 40 years old (Gust and others value in the control of outbreaks of infection in specific 1978). The decrease in antibody prevalence pre- circumstances, such as in institutions and nursery sumably reflects an improvement in economic and schools. Following the recent development of a tissue environmental conditions between the mid- 1950s and culture technique for hepatitis A virus, hopes of the mid-1970s. developing a specific vaccine are high. The epide- Villarejos and others (1976) found low prevalence of miology of hepatitis A infection, and approaches to its hepatitis A antibody among people of high socioecon- control, would be altered considerably by the omic status in the Philadelphia area (Pennsylvania, widespread use of such a vaccine. 176 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES Occurrence and Survival in the seepage from cesspools traveling a horizontal distance Environment of 23-55 meters through fissured red shale and limestone to pollute a well 67 meters deep. Similarly, 24 There is no direct evidence of the behavior or cases of hepatitis A occurred among 180 residents of occurrence of hepatitis A virus in the environment holiday cottages near Pilsen (Czechoslovakia) when because the virus has never been isolated from an their well was contaminated by seeping sewage (Vilim environmental sample. Such isolations must await and others 1977). However, there is no evidence that the development of sensitive and specific serological water conforming to conventional bacteriological techniques for detecting small amounts of hepatitis A criteria has ever caused hepatitis A, and the disease antigen or routine tissue culture techniques. The recent occurs under conditions similar to those which lead to successful propagation of hepatitis A virus in other waterborne, fecal-oral outbreaks of disease marmoset liver, fetal rhesus monkey kidney, and other (Grabow 1976). cells gives hope that tissue culture techniques will Known waterborne cases of hepatitis A in the USA become available soon. range between 35 and 120 year, which is only about 0.4 The available evidence on hepatitis A virus in the percent of total reported cases. Recent studies have environment is indirect. The knowledge that hepatitis sought to associate hepatitis incidence in the USA A incidence is high in some communities leads to the with raw water quality, water treatment practices, or assumption that hepatitis A virus may be present old distribution systems. However, many of these where fecal pollution is present, and especially where physical parameters are associated with socioecon- high concentrations of enteroviruses are present (see omic status in the area, and it is well established that chapter 9). However, far too little is known about the hepatitis A incidence is higher in poor and deprived prevalence of hepatitis A virus excretion, or the communities. To clarify the situation, Batik and others iiumbers of virus particles excreted, to predict at what (1980) compared hepatitis incidence with water supply concentration hepatitis A virus might be found in, for factors among a sample of nearly 3 million people who instance, sewage. Some evidence is provided by experienced 11,633 reported cases of hepatitis A during outbreaks of hepatitis A infection that can be traced by 1965-77. The comparisons were controlled for age epidemiological analysis to a particular source, such as distribution, educational levels, population density, contaminated water or food or shellfish. and poverty. None of the water supply source or Many outbreaks of hepatitis have been linked to treatment variables were significantly correlated with polluted drinking water. An explosive outbreak hepatitis A incidence. occurred in New Delhi in December-January 1955-56 Another source of circumstantial evidence of (Viswanathan 1957). About 30,000 cases were reported hepatitis A virus behavior in the environment are the (presumably many cases were subclinical or went many documented accounts of hepatitis outbreaks unreported) when sewage contaminated the city water associated with contaminated shellfish (Gerba and supply after heavy rain. This outbreak produced Goyal 1978; Hughes, Merson and Gangarosa 1977; evidence that this presumed hepatitis A virus-like strain Levin 1978). As many as 8.6 percent of reported is more resistant to chlorination than some enteric hepatitis A cases in the USA are associated with bacteria, and this is predictable from the data on the shellfish consumption (Levin 1978), usually with effect of chlorination on enteroviruses (see chapter 9). A consumption of raw oysters and raw or steamed clams. more recent report from India (Newaskar, Vidwans and Koff and others (1967) interviewed 270 adult hepatitis Vachha 1978) also suggests a link between sewage patients in Boston (Massachusetts, USA) hospitals and contamination of water supplies and an outbreak of concluded that ingestion of raw or steamed shellfish hepatitis in Maharashtra. was as common a source of infection as contact with Numerous small outbreaks attributed to water jaundiced persons, even during a nonepidemic period. pollution are reported from North America and An outbreak of hepatitis A (278 cases) that occurred Europe (see Craun 1978). These outbreaks typically in Louisiana during October and November 1973 was are associated with contamination of the water investigated and shown to be related to simultaneous distribution system by cross-connection or back- outbreaks in Texas and Georgia (USA). The outbreak siphonage or with the use of small untreated rural was attributed to the consumption of contaminated water supplies that are contaminated by sewage oysters harvested from approved growing areas on the discharges or leaks. Neefe and Stokes (1945) reported east Louisiana coast. The oysters were probably an outbreak of 350 cases over 13 weeks at a summer polluted when contaminated river water was dischar- camp in the USA. The outbreak was attributed to ged into the area during floods earlier in the year. HEPATITIS A VIRUS AND INFECTIOUS HEPATITIS 177 Oyster fishing was prohibited while the counts of It is to be expected that isolation and enumeration coliform bacteria were in excess of 70 per 100 milliliters. techniques for hepatitis A virus will become available Oysters harvested some 4 weeks after the coliform over the next few years and will be followed by a surge counts fell below this limit led to the disease outbreak. of investigations into the inactivation of the virus by The evidence suggests that the oysters concentrated the sewage treatment processes. In the meantime, it is hepatitis virus and retained it for a period of 1.5-2 reasonable to assume that hepatitis A virus behaves in months. A more severe outbreak was probably avoided a way similar to the enteroviruses (chapter 9). This because oysters in heavily contaminated areas were assumption will become more plausible if it is killed by changes in salinity (Mackowiak, Caraway confirmed that hepatitis A virus is an enterovirus. and Portnoy 1976; Portnoy and others 1975). On the basis of the epidemiological evidence, there is good reason to believe that shellfish accumulate and Inactivation b Night Soil and Sludge retain hepatitis A virus from polluted waters in the Tratment Proegs sg same way that they accumulate and retain poliovirus Treatment Processes (chapter 9). There is also good epidemiological evidence that cooking of shellfish does not necessarily As with sewage treatment processes, no direct inactivate all hepatitis A virus, just as it does not evidence is available on the inactivation of hepatitis A necessarily inactivate all poliovirus. Recent virus by night soil or sludge treatment processes. A confirmation of this was provided by Peterson and study by Ragka and others (1966) provided indirect others (1978), who reported that hepatitis A virus evidence of hepatitis A virus survival in cesspool sludge injected into oysters and treated at 60'C for 19 minutes applied to farm land. During the winter months of could still induce acute disease and seroconversion December and January (1962-63), cesspool sewage when fed to fasted marmosets. was spread on farmland near a small stream used as the source of water for a dairy near Jablonec (Czechoslovakia). On March 11-13 a thaw combined Inactivation by Sewage Treatment with rain led to the contamination of the stream. The Processes organic content of the water was sufficient to overwhelm the chlorination of the supply, and The lack of isolation techniques for hepatitis A virus contaminated water was used by the dairy. The water has prevented any direct studies on the inactivation of treatment process included chlorination followed by the virus by sewage treatment. Indirect evidence on the sand filtration. An epidemic of hepatitis A spread by reaction of hepatitis A virus to chlorination is provided dairy products occurred during April-June. There by the work of Neefe and others (1947), who were 424 cases, with the highest incidence in the 15-20 contaminated water with feces known to contain age group. Relatively few contact cases occurred hepatitis A virus, subjected the water to various possibly due to the mass administration of gamma treatment regimes, and then asked volunteers to drink globulin, particularly to children. The average it. The results indicated that coagulation and filtration incubation period was 45 days. There was no increase reduced but did not eliminate hepatitis A virus but that in other enteric infections, and the authors attribute coagulation, filtration, and chlorination (to provide 0.4 this either to a lack of the disease organisms in the milligrams per liter of free residual chlorine after 30 sewage or to the marginal chlorination having been minutes) eliminated the virus. However, direct sufficient to inactivate bacterial pathogens. It is evident chlorination of the contaminated water (to provide a from the information supplied that under cold weather total chlorine residual after 30 minutes of 1 milligram conditions hepatitis A virus survived at least 5 to 6 per liter) did not prevent infection in the volunteers, weeks in sewage spread on farmland. whereas heavier chlorine doses applied to the There is some evidence that hepatitis A virus may be contaminated water (15 milligrams per liter of total more resistant to heat than the enteroviruses discussed chlorine after 30 minutes) rendered the water in chapter 9. Krugman, Giles and Hammond (1970) noninfective to all volunteers. These results suggest found that hepatitis A virus was rendered nonin- that hepatitis A virus, like the enteroviruses (see fectious and nonimmunogenic by treatment at 98°C for chapter 9), is insensitive to combined chlorine and may 1 minute. Deinhardt (1976) reported that some only be inactivated in sewage disinfection by the hepatitis A virus survived treatment at 60°C for 1 hour. application of heavy chlorine doses to highly purified However, ability to withstand fairly high temperatures effluents. (>.60°C) for short times (< 1 hour) may not be 178 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES indicative of the ability of the virus to withstand cooler outbreaks. Journal of the Water Pollution Control temperatures for longer periods (see figure 9-2). Federation, 50, 1377-1381. Mackowiak, P. A., Caraway, C. T. and Portnoy, B. L. (1976). Oyster associated hepatitis: lessons from the Louisiana experience. American Journal of Epidemiology, 103, Literature Cited 181-191. Moritsugu, Y., Miyamura, K., Utagawa, E., Kono, R., de la Batik, O., Craun, G. F., Tuthill, R. W. and Kraemer, D. F. Motte, P. U. and Forbes, C. A. L. (1979). Prevalence of (1980). An epidemiologic study ofthe relatioriship between antibody to hepatitis A virus in Sri Lanka. Asian Journal of hepatitis A and water supply characteristics and treatment. Inzfectious Diseases, 3, 33-36. American Journal oJ Public Health, 70, 167-168. Neefe, J. R., Baty, J. B.. Reinhold, J. G. and Stokes, J. (1947). Craun, G. F. (1978). Disease outbreaks caused by drinking Inactivation of the virus of infectious hepatitis in drinking water. Journal of the Water Pollution Control Federation, water. American Journal of Public Health, 37, 365-372. 50, 1362-1374. Neefe, J. R. and Stokes, J. (1945). An epidemic of infectious Deinhardt, F. (1976). Hepatitis in primates. Advances in Virus hepatitis apparently due to a water-borne agent. Jmaurnal oq Research, 20, 113-157. the American Medical Association. 128, 1063 1075. Dienstag, J. L., Szmuness, W., Stevens, C. E. and Purcell, R. Newaskar, L. D., Vidwans, A. H. and Vachha, S. M. (1978). H. (1978). Hepatitis A virus infection: new insights from Outbreak of viral hepatitis due to water pollution in seroepidemiologic studies. Journal of Infectious Diseases, Pimpri-Chinchwad township. Indian Journal of 137, 328-340. Environmental Health, 20, 79-83. Gerba, C. P. and Goyal, S. M. (1978). Detection and Peterson, D. A., Wolfe, L. G., Larkin, E. P. and Deinhardt, F. occurrence of enteric viruses in shellfish: a review. Journal W. (1978). Thermal treatment and infectivity ofhepatitisA of Food Protection, 41, 743-754. virus in human feces. Journal of Medical 1 , !. . 2, Grabow, W. 0. K. (1976). Progress in studies on the type A 201-206. (infectious) hepatitis virus in water. Water South Africa, 2, Portnoy, B. L., Mackowiak, P. A., Caraway, C. T., Walker, J. 20-24. A.. McKinley, T. W. and Klein, C. A. (1975). Oyster- Gust, I. D., Lehmann, N. I. and Dimitrakakis, M. (1979). A associated hepatitis: failure of shellfish certification seroepidemiologic study of infection with HAV and HBV programs to prevent outbreaks. Journal of the American in five Pacific islands. American Journal of Epidemiology, Medical Association, 233, 1065-1068. 110, 237-242. Ragka, K., Helcl, J., Jezek, J., Kubelka, Z., Litov, M., Novak, Gust, I. D., Lehmann, N. I., Lucas, C. R., Ferris, A. A. and K., Radkovsky, J., Sery, V., Zejdl, J. and Zikmund, V. Locarnini, S. A. (1978). Studies on the epidemiology of (1966). A milk-borne infectious hepatitis epidemic. Journtal hepatitis A in Melbourne. In Viral Hepatitis: A of Hygiene, Epidemiology, Microbiology and Immunology, Contemporary Assessment of Etiology, Epidemiology, 10, 413-428. Pathogenesis and Prevention, eds. Girish, N. V., Cohen, S. Szmuness, W., Dienstag, J. L., Purcell, R H, Harley, E. J., N. and Schmid, R., pp. 105-112. San Francisco: Abacus Stevens, C. E. and Wong, D. C. (1976). Distribution of Press. antibody to hepatitis A antigen in urban adult Gust, I. D., Lewis, F. A. and Lehmann, N. I. (1978). populations. New England Journal of Medicine, 295, Prevalence of antibody to hepatitis A and polioviruses in 755-759. an unimmunized urban population. American Journal of Szmuness, W., Dienstag, J. L., Purcell, R. H., Stevens, C. E., Epidemiology, 107, 54-56. Wong, D. C., Ikram, H., Bar-Shany, S., Beasley, R. P., Hadler, S. C. (1980). Risk factors for the occurrence of Desmyter, J. and Gaon, J. A. (1977). The prevalence of hepatitis A outbreaks in day care centers. In Epidemic antibody to hepatitis A antigen in various parts of the Intelligence Service 29th Annual Conference, pp. 33-34. world: a pilot study. American Journal of Epidemiology, Atlanta, Georgia: Centers for Disease Control. 106, 392-398. Hughes. J. M., Merson, M. H. and Gangarosa, E. J. (1977). Vernon, A. A. (1980). Hepatitis A associated with a day care The safety of eating shellfish. Journal of the American center in Tulsa, 1979. In Epidemic Intelligence Service 29th Medical Association, 237, 1980-1981. Annual Conference. p. 34. Atlanta, Georgia: Centers for Koff, R. S., Grady, G. F., Chalmers, T. C., Mosley, J. W. and Disease Control. Swartz, B. L. (1967). Viral hepatitis in a group of Boston Vilim, V., Pesek, J., Brejcha, O., Zakova, M., Jindr. J. and hospitals: importance of exposure to shellfish in a Pruchova, M. (1977). Viral hepatitis A, water epidemic in a nonepidemic period. The New England Medical Journal, bungalow community. Ceskoslovenska Epidemiologie, 276, 703-710. Mikrobiologie, Immunologie, 26, 46-51. Krugman, S., Giles, J. P. and Hammond, J. (1970). Hepatitis Villarejos, V. M., Provost, P. J., Ittensohn, 0. L., McLean, A. virus: effect of heat on the infectivity and antigenicity ofthe A. and Hilleman, M. R. (1976). Seroepidemiologic MS- 1 and MS-2 strains. Journal of Infectious Diseases, 122, variations of human hepatitis caused by A, B and a 432-436. possible third virus. Proceedings of the Society for Levin, M. (1978). Fish and shellfish associated disease Experimental Biology and Medicine, 152, 524-528. HEPATITIS A VIRUS AND INFECTIOUS HEPATITIS 179 Viswanathan, R. (1957). Infectious hepatitis in Delhi Willcox, M., Brohult, J., Olsson, I. and Bengtsson, E. (1980). (1955-56), acritical study: epidemiology. Indian.lournal of Antibody to hepatitis A virus in Liberians. Transactions of Medical Research, supplementary number, 45, 1-29. the Royal Society of Tropical Medicine and Hygiene, 74, Wankya, B. M., Hansen, D. P., Ngindu, A. M. N., Feinstone, 690. S. F. and Purcell, R. H. (1979). Seroepidemiology of Zuckerman, A. J. and Howard, C. R. (1979). Hepatitis Viruses hepatitis A and B in Kenya. A rural population survey in of Man. London: Academic Press. Machakos District. East African Medical Journal, 56, 134-138. 11 Rotavirus and Viral Gastroenteritis THE AWARENESS THAT VIRUSES play a major role in and recovery occurs within about a week. Mortality the causation of diarrheal disease has been one of the rates are low in hospitalized children in developed outstanding medical advances of recent time. countries but may be considerable among untreated Previously, surveys of diarrheal disease had failed to children in developing countries. Dehydration and determine the causative agent in up to two-thirds of all shock are the most likely terminal processes, and oral cases-no known pathogen could be isolated from the rehydration is as effective in treating viral diarrhea as it stools of these patients. Since 1972, however, several is in treating bacterial diarrhea (Nalin and others different viruses have been identified in stools by 1979). Rotavirus gastroenteritis may occur as a single electronmicroscopy and have been shown to be case, or one episode of an epidemic outbreak. There is associated with diarrheal disease throughout the also a form of continuing infection in some newborn world. Rotaviruses have received the most attention nurseries in which a high proportion of the infants are and have been accepted as a major cause of childhood asymptomatic. gastroenteritis. Occurrence Description of Pathogens and Diseases Rotavirus appears to be almost universally distri- buted in human populations around the world. It has A growing number of different viruses are now been found in the stools of children with diarrhea from associated with diarrheal disease (see table 9-1). Japan and New Zealand in the East, to Canada and Rotaviruses appear to be the most important of these Argentina in the West. It has been identified in tropical and are therefore given greatest attention in this as well as temperate climates, although it may not be chapter. Several reviews of the rotaviruses have been quite such an important etiological agent for diarrhea published (Flewett and Woode 1978; Holmes 1979; in tropical countries as in temperate regions (patho- McNulty 1978; Steinhoff 1980; Yolken and Kapikan genic E. coli may be more dominant in the tropics; see 1979). chapter 13). Identification Infectious agents A number of different viruses may cause gastroen- Acute nonbacterial gastroenteritis has long been teritis, and the disease may vary accordingly. In recognized as a clinical entity. There was epidemiologi- rotavirus gastroenteritis, the onset is generally quite cal evidence of outbreaks of infectious diarrheas in sudden, and vomiting may be the presenting symptom which neither bacterial nor parasitic organisms could or may accompany diarrhea at the start. Vomiting is be found. Volunteer experiments demonstrated that often the dominant feature rather than diarrhea. Fever diarrhea could be transmitted by oral administration is present in many cases. Dehydration frequently of bacteria-free fecal filtrates. A particle of sub-bacterial occurs, but may be more severe in combined infections size, presumably a virus, seemed likely. The develop- with pathogenic Escherichia. coli. There is no ment of techniques to culture enteroviruses and consistent pattern of association between rotavirus adenoviruses from stool samples failed to identify any and pathogenic E. coli. In hospitalized children the organisms that occurred predominantly in patients fever and vomiting usually resolve in the first 5 days, with diarrhea. The application of electronmicroscopy 181 182 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES to diarrheal stool samples was the decisive advance. ADENOVIRUSES. These viruses are found in small The technique was enhanced by ultracentrifugation, numbers in feces of some patients with diarrhea, but antiserum clumping of particles (immuno-electron- occasionally in great numbers (see, for instance, microscopy, IEM), and negative staining. These methods Richmond and others 1979). The evidence that have their limitations because, unless particles adenoviruses can cause diarrhea is circumstantial, and occur in concentration of greater than 106 per gram there is no equivalent animal model. However, their of feces, they may not be detectable. More recent occasional presence in large numbers indicates that techniques for the identification of rotavirus particles they must have replicated in and destroyed cells. from stools include infected cell immunofluorescence, counter-immunoelectrophoresis, radioimmune assay, ASTROVIRUSES. These are particles of 28 nanometers and enzyme-linked immunosorbent assay (ELISA), and in diameter that are roughly spherical with surface the methodology is still rapidly improving. indentations that result in the appearance of a 5- or 6- Any form of examination of the feces may give a pointed star (figure 11-1b). They have been found in the distorted indication of the pathophysiology of feces of normal children and of those with gastro- gastroenteritis, a condition in which the primary lesion enteritis (see, for instance, Kurtz, Lee and Pickering is in the small bowel. The large bowel is distal to the site 1977). There is still no firm evidence that they are of infection and, even in a child, contains some 10 p o bacteria and also many fungi, mycoplasmas, and pathogenc. protozoa. All of these frequently have their own viral infections and may shed particles into the feces. CALICIVIRUSES. These are picornaviruses of appro- Bacteriophages, unless they have tails, may be very ximately 35 nanometers in diameter (figurel -lc) and difficult to distinguish from small spherical human were previously known as fecal viruses in such diverse viruses. The colon and its flora alter the effluent from species as sealions, pigs, and cats. Calicivirus has now the small bowel in a number of ways before it presents been associated with several outbreaks of gastro- enteritis and has also been found in the stools of as fecal material. asymptomatic individuals (Schaffer 1979; Studdert ROTAVIRUSES. These viruses from the stools of 1978). children are morphologically identical to those found in the stools of some calves, piglets, foals, lambs, mice, CORONAVIRUSES. These are well-known agents of and young monkeys with acute diarrhea. The human acute gastroenteritis in piglets and calves. They vary in virus has been transmitted to a number of these shape and size but have a distinctive appearance in animals. The virus particles are spherical, 70 nano- electron micrographs (figure 11-id). Recently they meters in diameter, and made up of double-stranded have been described in feces from young adults in RNA in two distinct capsid layers that on electron- Britain and from children in Canada and Australia. microscopy give the appearance of a wheel, hence the They have been isolated in tissue culture. They are not name rotavirus (figure 11-la). Rotaviruses are now proven human enteric pathogens, although they are a classifiedasagenusofthefamilyReoviridae(seetable9- major cause of the common cold (Clarke, Caul and 1). There are at least two, and possibly four, serotypes Egglestone 1979; McIntosh 1979; Robb and Bond of human rotavirus. 1979). Figure 11-1. Agents of viral gastroenteritis. (a) Rotaviruses under scanning electronmicroscopy. Scale bar = 0.1 micrometers. (Photo: J. Cohen, Station de Recherches de Virologie et d'Immunologie, Institute National de la Recherche Agronomique, Thiverval, France.) (b) Astroviruses under transmission electronmicroscopy, showing the characteristic 5- or 6-pointed star appearance. Scale bar = 0.1 micrometers. (Photo: C. R. Madeley, Royal Victoria Infirmary, Newcastle-upon-Tyne, UK.) (c) Caliciviruses under transmission electronmicroscopy, showing the characteristic surface hollows. Scale bar = 0.1 micrometers. (Photo: A. J. Zuckerman, London School of Hygiene and Tropical Medicine, London, UK.) (d) Coronaviruses under transmission electronmicroscopy. The virus particles vary in shape and size and possess a distinctive array of widely spaced surface projections, approximately 20 nanometers long, which give the characteristic "corona" appearance. Scale bar = 0.1 micrometers. (Photo: E. 0. Caul, Public Health Laboratory Service, Bristol, UK.) (e) Norwalk agent particles under transmission electronmicroscopy. Scale bar = 0.1 micrometers. (Photo: E. 0. Caul, Public Health Laboratory Service, Bristol, UK) ROTAVIRUS AND VIRAL GASTROENTERITIS 183 s _ ~ ~~~~ - ;-S '~~~~~~~~~ 'I' _rSv 'S 1*1 Nso--i~ ~~d 184 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES ENTEROVIRUSES. Most studies have indicated that containing cockles (Appleton and Pereira 1977). IEM the occurrence of these viruses is no more common in suggests this agent (cockle virus) is antigenically the stools of children with diarrhea than in those from similar to W agent. but different from Norwalk agent. control groups. However, in one outbreak of There is still considerable confusion in identifying gastroenteritis, believed to be due to a failure of water viruses in feces, especially when variations in methods, supply purification, coxsackie- and echoviruses were possible artifacts, and the presence of bacteriophages found as frequently as Shigella sonnei in the stools of are considered. It is far from proven that all the viruses those with diarrhea (Green and others 1968). discussed above cause gastroenteritis, and all have been isolated from healthy persons as well as from MEASLES VIRUS. In temperate climates measles is those with gastroenteritis. On some occasions, more now an exanthem which affects children primarily with than one virus has been present. However, it appears respiratory symptoms and a systemic upset. In the past, likely that, just as the upper respiratory tract reacts to a however, diarrhea was associated with measles and 28 range of viruses by producing the symptoms of the percent of children with measles in a London clinic in common cold, the alimentary tract will react to a range 1904 had diarrhea (Balme 1904). In tropical countries of viruses by developing gastroenteritis. It is only the where measles is frequently more severe, not only is the rotaviruses that are unquestionably a major cause of rash very prominent, but there is evidence of invasion gastroenteritis worldwide, and it is these which are of the bowel epithelium. The giant cells associated with discussed in the rest of this chapter. measles have been seen in the mucosa of biopsy specimens, and the excretion of giant cells in the feces Resoir may be prolonged. Diarrhea is frequently associated servos with measles in the tropics. A study in Guatemala Man is probably the only important reservoir for showed that half of the children under 5 years old with human rotavirus infection. measles had acute diarrhea (Scrimshaw and others 1966). Transmissioni NORWALK AGENT AND OTHER SMALL ROUND It is probable that transmission modes are similar to VIRUSES. Norwalk agent is a small round virus particle those of the enteroviruses and hepatitis A virus; that is, of 27 nanometers in diameter (figure 1 1-le) that caused fecal-oral and usually person-to-person but sometimes an outbreak of nonbacterial gastroenteritis in 50 via contaminated water, food, or shellfish. Airborne percent of students and staff of an elementary school in respiratory transmission remains an additional possi- Norwalk, Ohio (USA) in 1968. There was a 32 percent bility. attack rate among family contacts. Rectal swab filtrates produced disease in volunteers, and sub- sequently the particle was visualized by IEM. Other Incubation period morphologically similar viruses (Montgomery County Studies that include information about more than agent and Hawaii agent) have been isolated from one case of rotavirus diarrhea within a family or closed different epidemics of diarrhea (Dolin 1979). Some of community indicate that the incubation period is these show a cross-immunity, but several distinct between 24 and 72 hours. serotypes have been demonstrated. These agents produce a mild, self-limited gastroenteritis that lasts Period of communicabilitv 24-48 hours and affects older children and adults more often than the rotavirus. This is very uncertain because many details about Particles of similar size have been associated with the route and mode of spread are unknown. Moreover, small epidemics of winter vomiting disease in Britain: rotavirus diarrhea apparently disappears from a the W and Ditchling agents. These particles differ community for months at a time in hot weather; antigenically from the Norwalk agent and a high also, the organism cannot be found in stools unless it is proportion of adults appear to have antibody against present in high concentrations (> 106 per gram). If them. Some patients continued to excrete the particles transmission is dependent on the ingestion of a large for over 2 months after the illness. Smaller spherical number of virus particles, communicability from a particles of 25-26 nanometers were recently found in patient will be at its maximum on about the third to the feces of a high proportion of patients suffering from fourth day of the disease, coinciding with the period of food poisoning in Britain after eating seafood cocktails maximum virus shedding (101l per gram or more) and ROTAVIRUS AND VIRAL GASTROENTERITIS 185 would be unlikely after the eighth day-although By 18 months of age 85 percent of children in the excretion of rotavirus can continue for more than 20 area of Washington, DC (USA) have acquired days. Asymptomatic infection and excretion certainly antibodies to both Type 1 and Type 2 rotaviruses, and occur, but persistent carriage has not been the high antibody prevalence is maintained through- demonstrated. out life (Yolken and others 1978a). In contrast, in the same area, only about 10 percent of 3 year old children Resistance have Norwalk agent antibodies, and this prevalence rises to only around 50 percent later in life (Kapikian Facts are limited by ignorance about the epi- and others 1978). The same picture of rapid acquisition demiology and pathophysiology of rotavirus infection. of rotavirus antibodies by nearly all children, Newborn babies are apparently susceptible to the contrasted with gradual acquistion of Norwalk agent infection, particularly in the nursery situation, but antibodies (to a maximum prevalence of only 33 only a proportion of them develop clinical symptoms. percent), was found in Bangladesh (Kapikian and The low pathogenicity at this age may possibly be due others 1978; Sack and others 1980). to passively acquired maternal immunoglobulins. In temperate countries there is a striking seasonal Although the majority of older children and adults variation, with most cases occurring in the coldest have antibody to rotavirus, adults can be infected as months of the year, whereas in tropical climates (and is shown by rising antibody titers and sometimes by poorer communities) there appears to be much less clinical infections. The existence of at least two seasonal variation. At a children's hospital in rotavirus serotypes that are not cross-protective may Washington, DC (USA) during 1974-78. rotavirus partly explain repeat attacks. accounted for 39 percent of inpatient diarrhea and 22 percent of outpatient diarrhea. The equivalent figures Epidemiology in January were 71 percent and 62 percent, whereas during June and July they were 4.4 percent and 4.8 Rotavirus gastroenteritis is primarily a disease of percent for inpatients and outpatients, respectively children, especially those between 6 months and 3 (Brandt and others 1979). A comparative study in years old. Rotavirus infection can spread very rapidly Dallas (Texas, USA) and San Jose (Costa Rica) among neonates in nurseries, but many of these showed that in both settings rotavirus accounted for infections are asymptomatic (Jesudoss and others 50-60 percent of acute nonbacterial pediatric gastro- 1979). Rotavirus infection has been recorded in adults, enteritis episodes occurring from December through often in association with infection of their children (for February. This is the cool period in Dallas and the dry instance. Wenman and others 1979: Zissis and others season in San Jose. During the rest of the year the virus 1976). In all age groups asymptomatic infection is fairly was not recovered from any Dallas patients but was common, but persistent carriage is not demonstrated. found in 30-40 percent of Costa Rican patients in every Seroepidemiological surveys show that neonates month except May (Hieber and others 1978). have a high prevalence of rotavirus antibodies In developed and temperate countries (such as (presumably of maternal origin) that falls over the first Australia, Britain, Japan, and the USA), about half of 6 months of life. Antibody prevalence then rises again all diarrhea in children that requires hospitalization is until, by about 3 years, 80-90 percent have rotavirus caused by rotavirus infection. During the summer, antibodies, and this high prevalence is maintained 0-20 percent of cases are rotavirus associated, and in thoughout adult life. For instance, a survey of 266 winter this figure rises to 70-80 percent. Studies in children in Vellore (India) showed that the antibody developing and tropical countries have indicated that prevalence was 75 percent among neonates, 30 percent rotavirus accounts for a somewhat lower proportion of among 5-6 month old infants, and 87 percent among 3 hospitalized childhood diarrhea cases-maybe 25-50 year olds (Jesudoss and others 1978). Similar results percent. are found in affluent communities, indicating that Schnagl, Holmes and Mackay-Scollay (1978) rotavirus transmits successfully even in conditions of studied 537 episodes of diarrhea among 473 hospita- good hygiene, pure water, and full sewerage. This lized children under 6 years old in Western Australia. suggests direct person-to-person, fecal-oral, or re- Among aboriginal children the percentages of 387 spiratory routes of transmission, particularly within diarrheal stools from which known pathogens could be family groups. Parent-to-child, child-to-parent, and isolated were: parasites 17 percent, rotavirus 16 sibling-to-sibling spread are all likely (see, for instance, percent, Salmonella or Shigella 13 percent, pathogenic Wyn-Jones, Lillington and Alzaka 1978). E. coli 9 percent, adenovirus 3 percent, and astrovirus 2 186 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES percent. Among nonaboriginal children the per- infants and children with diarrhea at 3 hospitals in centages of 150 diarrheal stools from which known Kenya. Rotavirus accounted for 41 percent of pathogens could be isolated were: rotavirus 25 percent, inpatients in Nairobi, for 14 percent of inpatients and parasites 1 percent, Salmonella or Shigella 10 percent, 17 percent of outpatients in Mombasa, and for 29 pathogenic E. coli 10 percent, adenovirus 4 percent, percent of inpatients and 11 percent of outpatients in and astrovirus 3 percent. The data suggest the Kisumu (see also Mutanda 1980b; Mutanda, possibility of a winter peak of rotavirus gastroenteritis Cruickshank and Itotia 1979). Hansen and others among nonaboriginals and a summer peak among (1978) found that 6 percent of adult inpatients with aboriginals. Rotavirus was detected in the stools of diarrhea in Nairobi had serological evidence of only 2 out of 170 children without diarrhea. rotavirus infectiofi, whereas 26 percent had Shigella Black and others (1979) investigated 4,498 diarrhea and 18 percent had enterotoxigenic E. coli. cases reporting to Matlab hospital (Bangladesh) and Some studies have found that rotavirus infection is were able to identify a pathogen in the stools of 85 associatedwithdiarrheaofmorethanaverageseverity; percent (see table 13-1). Rotavirus was associated with if this is the case, the proportion of hospitalized 23 percent of all reported diarrhea cases and with 40 diarrhea cases due to rotavirus may be greater than the percent of diarrhea cases under 5 years old. proportion of all diarrhea cases. Two community During January-June 1976, Echeverria and others studies support this hypothesis. Spencer and others (1978) studied 82 hospitalized infants and children (1980) isolated rotavirus from only 7 percent (5 of 74) with diarrhea in Manila (Philippines). A viral etiology of nonhospitalized children under 4 years old with was indicated in 17 percent of cases, enterotoxigenic E. diarrhea in a coastal area of El Salvador. Similarly, coli in 11 percent, Salmonella or Shigella in 7 percent, rotavirus accounted for only 14 percent (26 of 183) of Vibrio cholerae in 4 percent, Giardia lamblia in 5 diarrheal episodes, from which no bacterial or percent, and Entamoeba histolytica in 2 percent. Ten protozoal pathogen could be isolated, among 0-3 year percent of children had evidence of infection with more old nonhospitalized children in a highland village in than one enteric pathogen. Only 1 out of 49 healthy Guatemala (Wyatt and others 1979). If all diarrhea children had rotavirus particles in their stools. among these children is considered, the proportion due Echeverria and others (1977) found evidence of to rotavirus was approximately 7 percent. The rotavirus infection in 56 percent (42/75) of children (3 incidence of rotavirus diarrhea was estimated at only days to 4 years old) with diarrhea seen at hospitals in 1.1 episode per child during the first 3 years of life. Taipei (Taiwan) during the summer. Studies of 293 hospitalized children under 5 years old with diarrhea in Caracas (Venezuela) showed a Control Measures rotavirus etiology in 41 percent of cases (Viera de Torres, Mazzali de Ilja and Esparza 1978). Only 3 out The spread of infection may be reduced by improved of 66 healthy children were excreting rotavirus. Espejo personal and domestic hygiene and by the sanitary and others (1978) studied 242 children under 5 years disposal of excreta, but this is uncertain. The very high old with acute diarrhea in two hospitals in Mexico City prevalence of antibodies to rotavirus in children over 2 (Mexico) and found rotavirus excretion in 25 percent. years old in affluent communities indicates that Although the peak of all diarrhea cases in Mexico rotavirus transmits successfully even in conditions of occurred in June-September, the peak of rotavirus near optimum hygiene, water supply, and sanitary diarrhea occurred in October. The highest age-specific facilities. proportions of diarrhea cases with rotavirus excretion Infections by rotavirus in breast-fed infants are less were in the 4-10 month age group. Of the 60 children likely and less severe than in bottle-fed infants. Breast who excreted rotavirus, 22 also excreted Salmonella, milk has been shown to contain specific antibodies to Shigella, or potentially pathogenic serotypes of E. coli. rotavirus (Yolken and others 1978a), but it now Rotavirus infection was less common among breastfed appears that other unidentified properties of breast infants with diarrhea (10 percent) than among milk are responsible for its protective effect (Totterdell, nonbreastfed infants with diarrhea (27 percent). Chrystie and Banatvala 1980). Little information is yet available on rotavirus The development of rotavirus vaccines is a distinct gastroenteritis in Africa. Brookfield and others (1979) possibility within the next few years, but delivering detected rotavirus in the stools of 31 percent of 123 them to the most vulnerable individuals (children aged hospitalized children under 4 years with diarrhea in 5-24 months) will be a difficult task in most developing Dar es Salaam (Tanzania). Mutanda (1980a) studied countries. ROTAVIRUS AND VIRAL GASTROENTERITIS 187 Occurrence and Survival in the a common history of eating seafood cocktails Environment containing cockles grown in waters polluted by scwage (Appleton and Pereira 1977). There is no direct evidence on the behavior or Dismukes and others (1969) reported 33 cases of occurrence of human rotavirus in the environment gastroenteritis of unknown etiology, and 4 cases of because the virus cannot be routinely isolated from hepatitis, occurring among 128 persons attending a environmental samples. Tissue culture methods have picnic at which raw clams were eaten. Ironically, at an been developed (Wyatt and others 1980), but rotavirus annual convention of a shellfish sanitation association does not grow readily in cell culture, and de- held at New Haven (Connecticut, USA) in November monstration of cytopathic effects is difficult. 1968, 19 persons ate raw clams and 17 of them Investigations into rotaviruses in the environment developed acute gastroenteritis of unknown etiology must await the development of improved tissue culture (Ratzan and others 1969). There was subsequently a 37 techniques or sensitive immunological antigen- percent secondary attack rate among family contacts detecting techniques. of the 17. The available evidence on human rotavirus in the The largest outbreak of viral gastroenteritis so far environment is indirect. The knowledge that rotavirus reported occurred in Australia during June and July may be excreted in large numbers (10" per gram) by 1978 (Murphy and others 1979). At least 2,000 cases infected individuals, and that incidence of infection were reported throughout the country; cases had a appears to be very high in some communities, leads to common history of eating rock oysters harvested from the assumption that human rotavirus may be present polluted estuaries near Sydney. The causative or- where fecal pollution is present, especially where high ganism was shown to be Norwalk agent. As a result of concentrations of enteroviruses are found (see chapter this outbreak, the New South Wales state government 9). However, far too little is known about the has required that all oysters harvested from the prevalence of rotavirus excretion, or about the incriminated areas be depurated for at least 2 days in numbers of viruses excreted by asymptomatic ex- disinfected water, and a panel of volunteers has been set creters, to predict at what concentration human up to test-consume samples of oysters prior to rotaviruses might be found in, for instance, sewage. marketing. The data reviewed in chapter 9 on the Some evidence is provided by outbreaks of gastro- elimination of enteroviruses from oysters in sterilized enteritis believed to be of viral etiology that have been water suggest that a 2-day depuration time is traced by epidemiological analysis to a particular inadequate to remove the risk of viral contamination source, such as contaminated water or shellfish. with reliability. Many outbreaks of gastroenteritis have been linked Little is known about the survival of human to polluted water, and many of these have had an rotavirus in the environment, and it is reasonable to undetermined etiology and could be of viral origin. assume, for the time being, that its environmental Craun (1978) reported that during 1975 and 1976 an behavior is similar to that of the enteroviruses (chapter etiological agent could not be identified in 75 percent of 9). Simian rotaviruses and reoviruses may provide a waterborne gastroenteritis outbreaks in the USA. closer model for human rotavirus in the environment From observations of the symptoms, it is more than than the enteroviruses, and recently data on simian probable that some of these outbreaks were due to rotaviruses in water have been reported. Hurst and rotaviruses or other diarrhea-causing viruses. Gerba (1980) compared the survival of poliovirus 1, However, there is no evidence that water conforming to echovirus 7, coxsackievirus B3, and simian rotavirus in conventional bacteriological criteria has ever caused clean and polluted freshwaters and in estuarine waters rotavirus infection, and waterborne gastroenteritis of various salinities (1.2-2.8 percent) at 20°C. All occurs in circumstances similar to those which may viruses survived for a very similar time, undergoing a 3 lead to other outbreaks of waterborne, fecal-oral log reduction in concentration in 6 to over 14 days gastroenteritis (see, for instance, Morens and others in freshwaters and in 2 to 3 days in estuarine waters. 1979). This preliminary experiment suggests that simian Other sources of circumstantial evidence of ro- rotavirus in fresh and saline water exhibits death rates tavirus behavior in the environment are the documen- well within the range reported for enteroviruses. ted accounts of gastroenteritis associated with the Rotavirus is very stable under some conditions. The ingestion of contaminated shellfish. The so-called virus is stable in the pH range 2-9.8 and survives for at cockle virus was detected during outbreaks of least 7 months, but not 4 years, at 18-20°C. Rotavirus gastroenteritis in the UK affecting 797 people who had in feces remained infectious and virulent for calves after 188 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES 5 years storage at 4°C. Preliminary studies indicate Inactivation by Night Soil and Sludge that rotavirus may resist a temperature of 60'C, but not Treatment Processes 63°C, for 30 minutes (G. N. Woode, personal communication). As with sewage treatment processes, no direct evidence is available on the inactivation of human rotavirus by night soil or sludge treatment. As noted above, reoviruses may provide a suitable model for Inactivation by Sewage Treatment environmental studies on human rotaviruses, and Processes several differences in the environmental characteris- tics of enteroviruses and reovirus are known to exist. The lack of adequate detection techniques has For instance, a series of studies by Ward and Ashley prevented any direct studies on the inactivation of (1976, 1977a, 1977b, 1977c, 1978) have shown that human rotavirus by sewage treatment. However, there reovirus is more heat resistant than poliovirus but that, is some indication that rotaviruses may be less unlike poliovirus, it is not protected against heat inactivated in treatment systems than polioviruses. inactivation by being in sludge. These studies also Farrah and others (1978) compared the ability of showed that ammonia, although it is highly virucidal poliovirus, human rotavirus and simian rotavirus to to enteroviruses at pH above 8, does not affect adsorb to aluminum hydroxide flocs and activated reoviruses, and that some detergents sensitize reovirus sludge flocs. Aluminum hydroxide flocs reduced the to heat inactivation while they protect poliovirus. concentration of poliovirus in tap water by 3 log units but only reduced the concentration of simian rotavirus by 1 log unit or less and did not noticeably reduce the Literature Cited number of rotavirus particles present in a dilute stool suspension. Activated sludge flocs reduced the concentraion. ofvaded pliudgefls byd07 et 1.h Appleton, H. and Pereira, M. S. (1977). A possible virus concentratio of added poliovirus by 07to log aetiology in outbreaks of food-poisoning from cockles. units but reduced simian rotavirus numbers by 0.5 log Lancet, 1, 780-781. units or less. This suggests that the adsorptive Balme, H. (1904). The signs and symptoms of measles in characteristics of poliovirus and rotavirus are different relation to diagnosis and prognosis. Practitioner, 1, and that lesser removals of rotavirus occur during 504-506. water coagulation or activated sludge treatment than Black, R. E., Merson, M. H., Rowe. B., Taylor, P. R., Mizanur have been reported for polioviruses (see chapter 9). Rahman, A. S. M., Azizal Huq, M., Abdul Aleem, A. R. M., Goyal and Gerba (1979) compared the proportion Sack, D. A. and Curlin, G. T. (1979). Epidemiology of of 27 different excreted viruses that were adsorbed to a enterotoxigenic Escherichia coli in rural Bangladesh. In sandy loam soil when shaken in water for 30 minutes. Proceedings of the 14th Joint Conferences US-Japan Between 91 and 99.99 percent of all viruses adsorbed to Cooperatite Medical Science Program. Cholera Panel, the soil, except for echovirus 1 (55 percent), echovirus Symposium on Cholera, eds. Takeya, K. and Zinnaka, Y., 12 (78 percent), echovirus 29 (14 percent), and simian pp 292-301. Tokyo: Toho University. Brandt, C. D., Kim, H. W., Yolken, R. H., Kapikian, A. Z., rotavirus (52 percent ). However, in another series of Arrobio, J. O., Rodriguez, W. J.. Wyatt, R. G., Chanock. R. adsorption experiments using nine different soils, M. and Parrott, R. H. (1979). Comparative epidemiology simian rotavirus tended to adsorb more than all other of two rotavirus serotypes and other viral agents asociated viruses studied except poliovirus 1, echovirus 7, and with pediatric gastroenteritis. Americani Journal of bacteriophage T4. A considerable amount of ad- Epidemiology, 110, 243-254. ditional experimentation will be required before it is Brookfield, D. S. K., Cosgrove, B. P.. Bell, E. J. and Madeley, clear whether rotaviruses are less readily adsorbed C. R. (1979). Viruses demonstrated in children in than enteroviruses or merely less readily adsorbed than Tanzania; studies in diarrhoea and measles. Jou7nal of poliovirus 1. Injection, 1, 249-255. The next few years will undoubtedly see many Clarke, S. K. R., Caul, E. 0. and Egglestone, S. I. (1979). The The next ~~~~~~~~~~human enteric coronaviruses. Postgradluate Medlical investigations into the removal of rotavirus from humn 55, 135 142. sewage and water. Pending the development of Journal, 55, 135-142. Craun, G. F. (1978). Disease outbreaks caused by drinking adequate concentration and detection techniques for water. Journal of the Water Pollutioni Control Federation, human rotaviruses, studies may be done using seeded 50, 1362-1374. simian rotaviruses and reoviruses, which may provide Dismukes, W. E.. Bisno. A. L., Katz, S. and Johnson, R. F. suitable models for human rotavirus. (1969). An outbreak of gastroenteritis and infectious ROTAVIRUS AND VIRAL GASTROENTERITIS 189 hepatitis attributed to raw clams. American1 Journal oj Kapikian, A. Z., Greenberg, H. B., Cline, W. L., Kalica, A. R., Epidemiology, 89, 555-561. Wyatt, R. G., James, H. D., Lloyd, N. L., Chanock, R. M., Dolin, R. (1979). Norwalk-like agents of gastroenteritis. In Ryder, R. W. and Kim, H. W. (1978). Prevalence of Principles anddPractice of Infectious Diseases, eds. Mandell, antibody to the Norwalk agent by a newly developed G. L., Douglas, R. G. and Bennett, J. E., pp. 1364-1370. immune adherence hemagglutination assay. Journal of New York: John Wiley. Medical Vo. i4. .: , 2, 281-294. Echeverria, P., Blacklow, N. R., Vollet, J. L., Ulyangco, C. V., Kurtz, J. B., Lee, T. W. and Pickering, D. (1977). Astrovirus Cukor, G., Soriano, V. B., DuPont, H. L., Cross, J. H., associated gastroenteritis in a children's ward. Journal oj Orskov, F. and 0rskov, I. (1978). Reovirus-like agent and Clinical Pi. l. .1. i, 30, 948-952. enterotoxigenic Escherichia coli infections in pediatric McIntosh, K. (1979). Coronavirus. In Principles and Practice diarrhea in the Philippines. Journal of Infectious Diseases, of Infectious Diseases, eds. Mandell, G. L., Douglas, R. G. 138, 326-332. and Bennett, J. E., pp. 1212-1217. New York: John Wiley. Echeverria, P., Ho, M. T., Blacklow, N. R., Quinnan, G., McNulty, M. S. (1978). Rotaviruses. Journal of General Portnoy, B., Olson, J. G., Conklin, R., DuPont, H. L. and Virology, 40, 1-18. Cross, J. H. (1977). Relative importance of viruses and Morens, D. M., Zweighaft, R. M., Vernon, T. M., Gary, G. W., bacteria in the etiology of pediatric diarrhea in Taiwan. Eslien, J. J., Wood, B. T., Holman, R. C. and Dolin, R. Journal of Infectious Diseases, 136, 383-390. (1979). A waterborne outbreak of gastroenteritis with Espejo, R. T., Calder6n, E., Gonzalez, N., Salom6n, A., secondary person-to-person spread. Lancet, 1, 964-966. Martuscelli, A. and Romero, P. (1978). Rotavirus Murphy, A. M., Grohmann, G. S., Christopher, P. J., Lopez, gastroenteritis in hospitalized infants and young children W. A., Davey, G. R. and Millsom, R. H. (1979). An in Mexico City. Revista Latinamericano de Micraobiologia, Australia-wide outbreak of gastroenteritis from oysters 20, 239-246. caused by Norwalk virus. Medical Journal of Australia, 2, Farrah, S. R., Goyal, S. M., Gerba, C. P., Conklin, R. H. and 329-333. Smith, E. M. (1978). Comparison between adsorption of Mutanda, L. N. (1980a). Epidemiology of acute gastro- poliovirus and rotavirus by aluminum hydroxide and enteritis in early childhood in Kenya. III. Distribution of activated sludge flocs. Applied and Environmental the aetiological agents. East African Medical Journal, 57, Microbiology, 35, 360-363. 317-326. Flewett, T. H. and Woode, G. N. (1978). The rotaviruses. (1980b). Epidemiology of acute gastroenteritis in Archives of lV. . i. ., . 57, 1-23. early childhood in Kenya. IV. Some clinical and Goyal, S. M. and Gerba, C. P. (1979). Comparative laboratory characteristics relative to the aetiological adsorption of human enteroviruses, simian rotavirus and agents. East Ajiican Medical Journal, 57, 599-606. selected bacteriophages to soils. Applied and Mutanda, L. N., Cruickshank, B. and Itotia, J. N. (1979). Environmental Microbiology, 38, 241-247. Rotavirus infection in private practice in Nairobi City. Green, D. M., Scott, S. S., Mowat, D. A. E., Shearer, E. J. M. East African Medical Journal, 56, 589-592. and MacFarlane Thomson, J. (1968). Water-borne Nalin, D. R., Levine, M. M., Mata, L., de Cespedes. C., outbreak of viral gastroenteritis and Sonne dysentery. Vargas, W., Lizano, C., Loria, A. R., Simhon, A. and Mohs, Journal of Hygiene, 66, 383-392. E. (1979). Oral rehydration and maintenance of children Hansen, D. P., Kaminsky, R. G., Bagg, R., Kapikian, A. Z., with rotavirus and bacterial diarrhoeas. Bulletin of the Slack, R. C. B. and Sack, D. A. (1978). New and old agents World Health Organization, 57, 453-459. in diarrhea: a prospective study of an indigenous adult Ratzan, K. R., Bryan, J. A., Krackow, J., Meyer, G. and African population. American Journal of Tropical Medicine Larson, C. D. (1969). An outbreak of gastroenteritis and Hygiene, 27, 609-615. associated with ingestion of raw clams. Journal of Hieber, J. P., Shelton, S., Nelson, J. D., Leon, J. and Mohs, E. Infectious Diseases, 120, 265-268. (1978). Comparison of human rotavirus disease in tropical Richmond, S. J., Caul, E. O., Dunn, S. M., Ashley, C. R., and temperate settings. American Journal of Diseases of Clarke, S. K. R. and Seymour, N. R. (1979). An outbreak of Children, 132, 853-858. gastroenteritis in young children caused by adenoviruses. Holmes, 1. H. (1979). Viral gastroenteritis. Progress in Lancet, 1, 1178-1180. Medical Virology, 25, 1-36. Robb, J. A. and Bond, C. W. (1979). Coronaviridae. In Hurst, C. J. and Gerba, C. P. (1980). Stability of simian Comprehensive Virology, 14, eds. Fraenkel-Conrat, H. rotavirus in fresh and estuarine water. Applied and and Wagner, R. R., pp. 193-247. New York: Plenum. Environmental Microbiology, 39, 1-5. Sack, D. A., Gilman, R. H., Kapikian, A. Z. and Aziz, K. M. S. Jesudoss, E. S., John, T. J., Maiya, P. P., Jadhav, M. and (1980). Seroepidemiology of rotavirus infection in rural Spence, L. (1979). Prevalence of rotavirus infection in Bangladesh. Journal ofClinical Microbiology, 11,530-532. neonates. IndianJournalofMedical Research, 70,863-867. Schaffer, F. L. (1979). Caliciviruses. In Comprehensive Jesudoss, E. S.,John,T. J., Mathan, M. and Spence, L. (1978). i,,.1. .,, 14, eds. Fraenkel-Conrat. H. and Wagner, R. Prevalence of rotavirus antibody in infants and children. R., pp. 249-284. New York: Plenum. Indian Journal of Medical Research, 68, 383-386. Schnagl, R. D., Holmes, I. H. and Mackay-Scollay, E. M. 190 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: VIRUSES (1978). A survey of rotavirus associated with gastro- dewatered wastewater sludge. Applied and Enuironmenital enteritis in aboriginal children in Western Australia. Microbiology, 36, 898-905. Medical Journal of Australia, 1, 304-307. Wenman, W. M., Hinde, D., Feltham, S. and Gurwith, M. Scrimshaw, N. S., Salomon,J. B., Bruch, H. A. and Gordon, J. (1979). Rotavirus infection in adults: results of a E. (1966). Studies of diarrheal disease in Central America. prospective family study. New England Journal oj VIII. Measles: diarrhea and nutritional deficiency in rural Medicine, 301, 303-306. Guatemala. American Journial of Tropical Medicinie and Wyatt, R. G., James, W. D., Bohl, E. H., Theil, K. W., Saif, L. Hygiene, 15, 625-631. J., Kalica, A. R., Greenberg, H. B., Kapikian, A. Z. and Spencer, H. C., Wells, J. G., Gary, G. W., Sondy, J., Puhr, N. Chanock. R. M. (1980). Human rotavirus type 2: D. and Feldman, R. A. (1980). Diarrhea in a non- cultivation in vitro. Science, 207, 189-191. hospitalized rural Salvadoran population: the role of Wyatt, R. G., Yolken, R. H., Urrutia, J. J., Mata, L., enterotoxigenic Escherichia coli and rotavirus. American Greenberg, H. B., Chanock, R. M. and Kapikian, A. Z. Journal oj Tropical Medicine and Hygiene, 29, 246-253. (1979). Diarrhea associated with rotavirus in rural Steinhoff, M. C. (1980). Rotavirus: thefirstfive years. Journial Guatemala: a longitudinal study of 24 infants and young oj Pediatrics, 96, 611-622. children. American Jou-nal of Tropical Medicinie and Studdert, M. J. (1978). Caliciviruses: brief review. Archives of Hygiene, 28, 325-328. 1,, . .. ., 58, 157-191. Wyn-Jones, A. P., Lillington, A. W. and Alzaka, A. (1978). An Totterdell, B. M., Chrystie, I. L. and Banatvala, J. E. (1980). investigation into the possible role of the family unit in the Cord blood and breast-milk antibodies in neonatal transmission of rotavirus infections of children. Public rotavirus infection. British Medical Journal, 1, 828-830. Health, 92, 291-293. Viera de Torres, B., Mazzali de Ilja, R. and Esparza, J. Yolken, R. H. and Kapikian, A. Z. (1979). Rotavirus. In (1978). Epidemiological aspects of rotavirus infection in Principles and Practice of Infectious Diseases, eds. Mandell, hospitalized Venezuelan children with gastroenteritis. G. L., Douglas, R. G. and Bennett, J. E., pp. 1268-1281. American Journal of Tropical Medicine and Hygiene, 27, New York: John Wiley. 567-572. Yolken, R. H., Wyatt, R. G., Mata, L., Urrutia, J. J., Garcia, Ward, R. L. and Ashley, C. S. (1976). Inactivation of B., Chanock, R. M. and Kapikian, A. Z. (1978a). Secretory poliovirus in digested sludge. Applied and Environmental antibody directed against rotavirus in human milk, Microbiology, 31, 921-930. measurement by means of enzyme-linked immunosorbent (1977a). Identification of the virucidal agent in assay. Journal of Pediatrics, 93, 916-921. wastewater sludge. Applied and Environmenital Yolken, R. H., Wyatt, R. G., Zissis, G., Brandt, C. D., Microbiology. 33, 860-864. Rodriguez, W. J., Kim, H. W., Parrott, R. H., Urrutia, J. J., (1977b). Inactivation of enteric viruses in wastewater Mata, L., Greenberg, H. B., Kapikian, A. Z. and Chanock, sludge through dewatering by evaporation. Applied and R. M. (1978b). Epidemiology of human rotavirus types 1 Environmental Microbiology, 34, 564-570. and 2 as studied by enzyme-linked immunosorbent assay. (1977c). Discovery of an agent in wastewater sludge New England Journal of Medicine, 299, 1156-1161. that reduces the heat required to inactivate reoviruses. Zissis, G., Lambert, J. P., Fonteyne, J. and de Kegel, D. D. Applied and Environmental Microbiology, 34, 681-688. (1976). Child-mother transmission of rotavirus. Lancet, 1, - (1978). Heat inactivation of eniteric viruses in 96. SECTION II Excreted Bacteria Chapter 12 Campylobacter and Campylobacter Enteritis 13 Pathogenic and Nonpathogenic Escherichia coli and'other Bacterial Indicators of Fecal Pollution 14 Leptospira and Leptospirosis 15 Salmonella, Enteric Fevers, and Salmonelloses 16 Shigella and Shigellosis 17 Vibrio cholerae and Cholera 18 Yersinia and Yersiniosis 12 Campylobacter and Campylobacter Enteritis THREE CHAPTERS of this book describe recently Identification recognized causes of diarrhea that are now believed to . . be of major importance throughout the world. These Campylobacter enterits (also called campylo- are the rotaviruses and other viruses (chapter 11); the bacter etei infecion cue by various pathogenic forms of Escherichia coli (chapter 13and some bacteria of the genus Campylobacter, sequences of the infection vary from asymptomatic 1; . . . ' excretion or mild symptoms to severe disease. In some which are described in this chapter. Knowledge of Campylobacter as a cause of diarrhea in man is recent affected patients the diarrhea is profuse and watery and .. . . . ...............is often accompanied by strong abdominal pain, and limited. The first isolations of the organism from isotnacmnedb srngboialpn' andolimited. T f isolathiosfhea oanism from headache, and fever. Dysenteric stools containing blood Australia (Cooper and Slee 1971) and in 1972 in and mucus are fairly common, especially in children. Austalgia (Cooper and othees 1971) and ins 197 n Vomiting is uncommon. Illness usually persists for a few Belgium (Dekeyser and others 1972). It was only husofwasbtnoeainstacniu durig 197 tat te sale f th prblembecme cear hours to a few days, but in some patients it may continue during 1977 that the scale of the problem became clear frwes eyrto n lcrlt elcmn r in Europe; information on Cam.pylobacter enteritis . for weeks. Rehydration and electrolyte replacement are the USA is even more recent. Very little is yet known sometimes required. Antibiotic therapy is usually about this infection in the developing countries. . . . ' . i . Several comprehensive reviews have been published proven. Complications include an abdominal pain of since 1977 (Butzler 1978, Butzler and Skirrow 1979. such intensity that acute peritonitis is diagnosed and Karmali and Fleming 1979; Skirrow 1977; Smibert surgery often undertaken. Reactive arthritis has been 1978). reported as a complication of Campylobacter enteritis in 2 percent (8 of 340) of cases in Finland (Kosunen and others 1980). Description of Pathogen and Disease Occurrence The delayed recognition of the important role of The exact distribution and importance of Campylobacter as a cause of diarrhea is due to the Campylobacter enteritis in various geographical problems of isolating these bacteria. As strict aerobes regions arenot yet known. It isvery probable, however, growing under low oxygen levels, they will not grow that C. fetus ssp. jejuni is a major cause of diarrhea under the aerobic or anaerobic growth conditions throughout the world (table 12-1). used in most laboratories; furthermore, unless selective growth systems are used they are overgrown by other bacteria present in feces. Now that these difficulties have been overcome, it seems that campylobacters are the single most common bacterial Campylobacters are microaerophilic, Gram- cause of diarrhea in several countries (table 12-1). negative, motile, slender (0.2-0.4 micrometers in However, the mechanism by which campylobacters width), curved or spiral bacteria (figure 12-1). They are cause diarrhea remains obscure. Although they are oxidase positive and do not attack sugars. The genus is commonly isolated from fecal specimens, their divisible into two groups on the basis of the catalase significance as pathogens is not always clear. reaction and nitrate reduction test. The organisms 193 194 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY:BACTERIA Table 12-1. Prevalence of excretion of Campylobacter and other enteric pathogens by individuals with and without diarrhea in twelve countries Number Prevalenc e Of of excretion persons Prevalence of other with (+) of bacterial or and Campylobacter protozoal without (-) excretion pathogens Country Age group diarrhea (percent) (percent) Source Australia All ages +224 5.8 (5.4)a NDb Steele and McDermott All ages -530 0 ND (1978) Bangladesh All ages +204 12.0 ND Blaser and others (1980a) All ages + 97b 5.2 ND 1-4 years +80 8.6 ND 1-4 years + 34b 5.9 ND 1-5 years -141 18.0 ND Belgium Children + 3200 5.8 ND Butzler (1978) Children -6500 1.7 ND Adults + 600 2.3 ND Adults -700 0.7 ND Brazil 0-12 years +217 6.4 ND Ricciardi and Ferreira (1980) England All ages +280 14.0 (12) 13.0 Bruce, Zochowski and All ages -156 0.6 1.9 Ferguson (1977) All ages + 182 7.6 ND Dale (1977) All ages -60 0.2 ND All ages +-860 4.2 4.4 Pearson and others (1977) All ages +-330 5.8 ND Tanner and All ages -120 0.8 ND Bullin (1977) Indonesia 0-9 years + 150 10.0 ND Rockhill >9 years +200 2.0 ND and others 0-9 years +7c 28.0 ND (1980) >9 years +150l 2.0 ND All ages -ND < 1.0 ND Rwanda Children + 150 11 42 De Mol and Children -58 0 31 Bosmans (1978) Scotland All ages + 196 8.7 (7.1) 16 Tefler Brunton All ages -50 0 0 and Heggie (1977) South Africa 0-8 months +-47 32 (31) 40 Bokkenheuser 0-8 months -45 4 15 and others (1979) 9-24 months +31 39 (38) 39 9-24 months -18 44 50 Spain All ages + 446 4.5 17 Lopez Brea, Molina and Baquero (1979) USA All ages +238 4.6 ND MMWR (1979a) All ages +956 4.1 ND Blaser and All ages -548 0 ND others (1980c) Zaire Children + 70 8.6 (8.6) ND Butzler (1973) Children -30 0 ND ND No data. a. Figures in parentheses refer to Campylobacter isolations in the absence of other known bacterial or protozoal pathogens. b. These patients had dysentry (bloody stools). c. These patients had suspected typhoid. CAMPYLOBACTER AND CAMPYLOBACTER ENTERITIS 195 . 4~~~~~~~~ Figure 12-1. Campylobacter under scanning electronmicroscopy. The polar flagella are clearly seen. Scale bar micrometer. (Photo: J. P. Butzler, H6pital Universitaire Saint Pierre, Brussels, Belgium) considered in this chapte r are catalase positive, countries have implicated domestic animals (especially Although campylobacters have aerobic metabolism, puppies), caged birds, poultry (alive or undercooked), they are unable to grow in atmospheric oxygen. pigs, sheep, and cows as possible sources of human Growth occurs at oxygen concentrations of between 3 infections (Blaser and others 1980c; Bruce, Zochowski and 7 percent. Incubation on isolation media at 430C and Ferguson 1977; Butzler and Skirrow 1979; aids the isolation of C.jetus ssp. jejuni, and incubation MMWR 1978b, 1979a, 1979b; Pearson and others at 250C favors C. fetus ssp. intestinalis and ssp. 1977). The degree to which man is an important venerealis. C. fetus ssp. jejuni has been the most reservoir for human infection is not clear. Most studies commonly described isolate associated with diarrhea, listed in table 12-1 found a very low prevalence (0-1.7 but the significance of other campylobacters has not percent) of Campylobacter excretion among healthy been fully assessed. C. fetus ssp. venerealis causes individuals. By complete contrast, the data from enzootic sterility in cattle and is transmitted venereally. Bangladesh and South Africa (table 12-1) showed that C.jfetus ssp. intestinalis causes abortion in sheep and Campylobacter are excreted by a substantial proportion cattle, is transmitted by the fecal-oral route, and is a of healthy children. The important reservoirs of rare, opportunistic pathogen of man. The taxonomy of Campylobacter in poor communities in developing the catalase-positive campylobacters remains con- countries remain to be elucidated. fused. The organism described here as C. fetus ssp. jejuni is also called C.jejuni, or C.jejuni and C. coli, or, in Transmission the older literature, "related vibrios." Transmission is presumed to be fecal-oral, from the Reservoirs feces of infected people, animals, or birds. Infected persons with diarrhea excrete 106-109 C. fetus ssp. Although it is known that a wide variety of animals jejuni per gram of feces. In affluent communities there is and birds may excrete C.fetus ssp. jejuni, the reservoirs little evidence of direct person-to-person spread, except that are functionally important for human infection among young children in nurseries. In poor com- have not been determined. Studies in developed munities and developing countries it is very probable 196 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY:BACTERIA that person-to-person spread is of considerable zoonotic salmonelloses (chapter 15). It is possible that importance, although studies are required to confirm the dominant route of transmission, in developed this. Several reports in developed countries indicate countries, is from infected animals to man, either as a transmission via undercooked poultry (Butzler and result of handling pets or farm animals or as a result of Skirrow 1979; MMWR 1979a) and unpasteurized milk ingesting poorly cooked meat (especially poultry) or (Blaser and others 1979; MMWR 1978b; Robinson and unpasteurized milk. If this is the case, then its others 1979; Taylor, Weinstein and Bryner 1979), and epidemiology in developed countries should indeed be human infection from contact with infected pet animals very similar to the salmonelloses. This interpretation and birds is also suspected (Blaser and others 1978, would also explain why C. fetus ssp. jejuni is such a 1980c; Butzler and Skirrow 1979; MMWR 1979b). The prominent cause of bacterial diarrhea, even in affluent organism can persist in chicken and turkey carcasses communities with high standards of environmental during preparation and refrigeration for commercial sanitation (table 12-1). Reportings of Campylobacter marketing (Simmons and Gibbs 1979). Waterborne enteritis tend to peak during the warm summer months transmission was suspected in one major outbreak in in England and Wales, Belgium. and the USA (Butzler the USA (MMWR 1978a). and Skirrow 1979). Data on infective dose are not yet available, but a The data in table 12-1 show that C.fetus ssp. jejuni medical laboratory technician in Australia successfully has been associated with 4-14 percent of diarrhea cases infected himself by ingesting 106 C. fetus ssp. jejuni in in developed countries. In these same countries, the milk (Steele and McDermott 1978). prevalence of Campylobacter excretion by healthy persons is low (0-1.7 percent). The picture in Incubation period developing countries is unclear. In some (for instance, Indonesia, Rwanda, and Zaire) the prevalences of Incubation periods for Campylobacter enteritis are Campylobacter infection among those with and somewhat longer than is common for other bacterial without diarrhea are similar to the prevalences enteric infections. Recorded or estimated incubation reported from developed countries. In Bangladesh and periods are from 1.5 to ll days, but usually are between South Africa, however, a very different picture has 3 and 5 days. emerged. In Bangladesh, 18 percent of 141 village children (1-5 years old) were excreting Cantiplobacter Period of comnmunicability during the dry season. whereas only 2 percent were excreting Shigella, and none were excreting Salmonella One study in the USA (Blaser and others 1980c) (Blaser and others 1980a). Fifty-two percent (13 of 25) found that fecal carriage of C.fetus ssp. jejuni was for a of these Campylobacter-positive children had had no median period of 15 days from the onset of illness. history of diarrhea in the 30 days prior to specimen Most patients were not excreting the organism after 21 collection. The prevalence of Campylobacter excretion days, and the maximum period of excretion recorded in the 12-23 months age group was 39 percent. was 7 weeks. Jones (1979) reported excretion of the Similarly, in Soweto (South Africa), Bokkenheuser and pathogen for 18-39daysby 12 adult patients employed others (1979) reported a 44 percent prevalence of at a food factory in England. Campylobacter excretion among healthy, black child- ren age 9 to 24 months (see also Koornhof and others Resistance 1979). While it seems certain that C.fetus ssp.jejuni is a cause of some diarrhea in developing countries, the The disease has been described in both children and relative importance of this etiologic agent in com- adults. Circulating antibody can be detected, and it parison with other known major agents (especially may well be that some immunity is conferred by enterotoxigenic E. coli and rotavirus) remains un- infection. determined. Data from England (Butzler and Skirrow 1979; Dale Epidemiology 1977) suggest that the highest incidence of disease occurs among people 5 to 34 years old, whereas some The epidemiology of Campylobacter enteritis is reports from developing countries suggest that infants poorly understood in the developed countries and and young children are the most affected (Blaser and totally obscure in the developing countries. It seems others 1980a; DeMol and Bosmans 1978; Ricciardi clear that it is a zoonosis, and it may be that the nearest and Ferreira 1980). This, in turn, suggests the possible known parallel is with the epidemiology of the importance of person-to-person transmission in CAMPYLOBACTER AND CAMPYLOBACTER ENTERITIS 197 developing countries. However, Blaser and others 25°C. Comparative studies in acid and water showed (1980a) found that Campylobacter infection among that survival was significantly curtailed at pH values of children in a rural area of Bangladesh was not clustered less than 3. A 7 log reduction occurred in 20 minutes at by household and considered that there might be pH 2.4 "relatively little person-to-person transmission." Of peripheral interest are the experiments of An outbreak of Campylobacter enteritis affected Lindenstruth and Ward (1948) with Vibriofetus, which 2,000 out of the 10,000 inhabitants of Bennington might now be classified as Campylobacter fetus ssp. (Vermont, USA) during a 2-week period in May-June intestinalis. They showed that, at 20°C and 37°C, 1978 (MMWR 1978a). All parts of the town were inoculations of 1.5 x 109 organisms survived for 10 involved, and there was no evidence of secondary days but not for 20 days in hay, soil, and sheep manure. person-to-person spread. The town water supply was At 6°C, the same inoculation in the same environments partially chlorinated, but not otherwise treated, and survived for 20 days but not for 30 days. several areas of the town were receiving water with no residual chlorine over the period of the outbreak. No Inactivation by Sewage Treatment Campylobacter was isolated from the water, but the Processes water supply was strongly implicated as the common source of the outbreak. No information is available on the destruction of C. fetus ssp.jejuni by sewage treatment processes or on the Control Measures occurrence of this organism in sewage. Very little can be said with certainty about the Inactivation by Night Soil and Sludge control of Campylobacter enteritis until its epide- Treatment Processes miology is further understood. Hygienic excreta disposal, good personal and domestic cleanliness, No information is available on the destruction of C. adequate cooking of poultry and care in handling pets fetus ssp. jejuni by night soil and sludge treatment and farm animals are all presumed to be important processes or on the occurrence of this organism in protective measures. night soil and sludge. Occurrence and Survival in the Literature Cited Environment Blaser, M.. Cravens, J., Powers, B. W. and Wang, W. L. Although it is known that C. fetus ssp. jejuni is (1978). Campylobacter enteritis associated with canine excreted by a wide variety of animals and birds, almost infection. Lancet, 2, 979-981. no data exist on the presence of these organisms in the Blaser, M. J., Cravens, J., Powers, B. W., LaForce. F. M. and Wang, W. L. (1979). Camnpylobacter enteritis associated environment. Knmll, Suckling and Pearson (1978) wihunatu'zdmik meia.Junl.fMdiie isolated C.fetus ssp.jejuni from 21 percent (7 of 34) of w6th unpasteu1zed milk. Aner8can Journal of Medicine, seawater samples, and from 74 percent (37 of 50) of Blaser, M. J., Glass, R. I., Huq, M. I., Stoll. B., Kibriya. G. M. river and pond samples, in the Southampton area and Alim, A. R. M. A. (1980a). Isolation of Camnpylobacter (UK). All positive water samples also contained E. coli. fetus ssp. jejuni from Bangladeshi children. Journal of Very little is yet known about the survival of C.fetus Clinical Microbiology, 12, 744-747. ssp. jejuni in various environmental habitats. In one Blaser, M. J., Hardesty, H. L., Powers, B. and Wang, W. L. study, C. fetus ssp. jejuni was enumerated in stored (1980b). Survival of Campylobacter fetus subsp. jejuni in feces, urine, water, and milk (Blaser and others 1980b). biological milieus. Journal of Clinical Microbiology, 11, In naturally infected feces, a 7 to 9 log reduction 309-313. occurred in 9 to 22 days at 4°C and in 3 to 8 days at Blaser, M. J., LaForce, F. M., Wilson, N. A. and Wang, W. L. 25.C. In urinehighinitilconentraion(1980c). Reservoirs for human campylobacteriosis. 25°C. In urine, high initial concentrations became Journal of Infectious Diseases, 141, 665-669. undetectable in less than 2 days at 37°C, but organisms Bokkenheuser, V. D., Richardson, N. J., Bryner, J. H., Roux, were viable for up to 35 days at 4°C. In autoclaved D. J., Schutte, A. B., Koornhof, H. J., Freiman, I. and stream water, a 7 log reduction took 5 to 33 days at 4°C Hartman, E. (1979). Detection of enteric campylobac- and 2 to 4 days at 25°C. In pasteurized milk, maximum teriosis in children. Journal of Clinical Microbiology, 9, survival times were 22 days at 4°C and less than 3 days at 227-232. 198 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Bruce, D., Zochowski, W. and Ferguson, I. R. (1977). (1978b). Campylobacter enteritis-Colorado. Camnpylobacter enteritis. Britishl Medical Journal., 2, 1219. Morbidity and Mortality Weekly Report, 27, 226 and 231. Butzler, J. P. (1973). Related vibrios in Africa. Lancet. 2, 858. - (1979a). Cam pylobacter enteritis-Iowa. Morbidity (1978). Infection with campylobacters. In Modern and Mortality Weekly Report, 28, 565-566. Topics in Infection, ed. Williams, J. D., pp. 214-239. (1979b). Campylobacter enteritis in a household London: Heinemann. Colorado. Morbidity and Mortality Weekly Report, 28, Butzler, J. P. and Skirrow. M. B. (1979). Campylobacter 273-274. enteritis. Clinics in Gastroenterology. 8. 737-765. Pearson, A. D., Suckling, W. G., Ricciardi, I. D., Knill. M. and Cooper, I. A. and Slee, K. J. (1971). Human infection by Ware, E. (1977). Campylobacter-associated diarrhoea in Vibrio fetus. Medical Journal of Australia, 1, 1263-1267. Southampton. British Medical Journal, 2, 955-956. Dale, B. (1977). Campylobacter enteritis. British Medical Ricciardi, I. D. and Ferreira, M. C. S. (1980). The age Journal, 2, 318. distribution in children with Campylobacter enteritis. Dekeyser, P., Gossuin-Detrain, M., Butzler, J. P. and Transactions of the Royal Society of Tropical Medicine and Sternan,J. (1972). Acute enteritis due to relatedvibrio: first Hygiene, 74, 687. positive stool cultures. Journal of'lnfectious Diseases, 125, Robinson, D. A., Edgar, W. J., Gibson, G. L., Matchett, A. A. 390-392. and Robertson, L. (1979). Campylobacter enteritis De Mol, P. and Bosmans, E. (1978). Campylobacter enteritis associated with consumption of unpasteurized milk. in Central Africa. Lancet, 1, 604. British Medical Journal, 1, 1171-1173. Jones, A. (1979). Campylobacter enteritis in a food factory. Rockhill, R. C., Ringerts. S.. Moechtar Muhammad, A. and Lancei, 1, 618-619. Soetomo, A. (1980). Prevalence of Campylobacter fetus Karmali, M. A. and Fleming, P. C. (1979). Campylobacter subsp. jejuni-caused gastroenteritis in some patients in enteritis. Canadian Medical Association Journal, 120, Jakarta, Indonesia. In Abstracts of'the 10th Internzational 1525-1532. Conigress on Tropical Medicine and Malaria, pp. 28-29. Knill, M., Suckling. W. G. and Pearson, A. D. (1978). Manila: Institute of Public Health. University of the Environmental isolation of heat-tolerant Campylobacter in Philippines. the Southampton area. Lancet, 2. 1002-1003. Simmons, N. A. and Gibbs, F. J. (1979). Campylobacter spp. Koornhof, H. J., Robins-Browne, R. M., Richardson, N. J. in oven-ready poultry. Journal of Infection, 1, 159-162. and Cassel, R. (1979). Etiology of infantile enteritis in Skirrow, M. B. (1977). Campjylobacter enteritis: a "new" South Africa. Israel Journal of Medical Sciences, 15, disease. British Medical Journal, 2, 9-11. 341-347. Smibert, R. M. (1978). The genus Campvlobacter. Annual Kosunen, T. U., Kauranen, O., Martio, J., Prikanen, T., Review of'Microbiology, 32, 673-709. Ponka, A., Hortling, L., Aittoniemi, S., Mutru, O., Penttila, Steele, T. W. and McDermott, S. (1978). Cam pylobacter 0. and Koskimies, S. (1980). Reactive arthritis after enteritis in South Australia. Medical Journal of Australia, Campylobacter jejuni enteritis in patients with HLA-B27. 2, 404-406. Lancet, 1, 1312-1313. Tanner, E. I. and Bullin, C. H. (1977). Campylobacter Lindenstruth, R. W. and Ward, B. Q. (1948). Viability of enteritis. British Medical Journal, 2, 579. Vibrio fetus in hay, soil, and manure. Journal of the Taylor, P. R., Weinstein, W. M. and Bryner, J. H. (1979). American Veterinary Medical Association, 113, 163. Campylobacter fetus infection in human subjects: asso- Lopez Brea, M., Molina, D. and Baquero, M. (1979). ciation with raw milk. American Journal of Medicine. 66, Campylobacter enteritis in Spain. Transactions ofthe Royal 779-783. Society of Tropical Medicine and Hygiene, 73, 474. Tefler Brunton, W. A. and Heggie, D. (1977). Campylobacter- MMWR (1978a). Waterborne Camppylobacter gastro- associated diarrhoea in Edinburgh. British Medical enteritis Vermont. Morbidity and Mortality Weekly Journal, 2, 956. Report, 27, 207. 13 Pathogenic and Nonpathogenic Escherichia coli and Other Bacterial Indicators of Fecal Pollution THIS CHIAPTER combines two distinct areas of coli diarrhea is of limited clinical value and is, in any knowledge. The first two sections ("Description of case, difficult because all patients are excreting large Pathogen and Disease" and "Control Measures") numbers of commensal E. coli, and the laboratory cover recent information on the role of certain types of methods for identifying the suspected pathogens are Escherichia coli as major causes of acute diarrhea in complex and slow. The magnitude of the problem many countries. Subsequent sections of the chapter results from the fact that E. coli virulence factors are briefly review the enormous compilation ofliterature on plasmid encoded and may be transmitted to many other the fecal indicator bacteria, which have been used for 80 Enterobacteriaceae. years as a measure of the degree of fecal contamination of the environment. Occurrence Description of Pathogen and Disease Gastroenteritis due to E. coli occurs in all parts of the world. Particular types of enterotoxigenic E. coli In the last 30 years, and especially in the last tO years, apparently cause infantile diarrhea in particular it has becomeclearthatvariousf s . ci a countries. It is thought that the acquisition of such itjor hausbe e clediartheat vrios fetonbrmofFcly arev s a. infantile strains is one of the major causes of travelers' major cause of diarrhea. This section briefly reviews F diarrhea. Enterotoxigenic E. coli appears to be a more important cause of diarrhea in developing countries than in developed countries. It may be that certain Identification enteroinvasive strains, causing disease in adults, are Diarrhea produced by E. coli cannot be also of restricted geographical distribution. differentiated clinically from similar disease produced by other enteric pathogens. The spectrum of disease Injectious agents includes a cholera-like syndrome produced by enterotoxigenic organisms, a dysentery-like syndrome E. coli is a Gram-negative, rod-shaped bacterium caused by enteroinvasive organisms, and many milder belonging to the family Enterobacteriaceae (figure forms of diarrhea. Asymptomatic infection is very 13-1). These organisms are usually thought of as common. The severity of disease caused by the lactose-fermenting saprophytes, in contrast with the enterotoxigenic E. coli depends upon the degree of non-lactose fermenting Salmonella spp. and Shigella dehydration, and treatment is primarily by rehy- spp. Lactose-fermenting Salmonella spp. and Shigella dration and electrolyte replacement oral rehydration spp. do occur, however, and non-lactose-fermenting having proved very effective in most patients. Death Escherichia coli may be common from some sources. rates of 5-10 percent may be experienced among E. coli is a normal inhabitant of the intestinal tract of untreated infants and children but are very low among man and many other animal species. Conventional those receiving rehydration therapy. Diagnosis of E. biochemical tests used in the identification of bacteria 199 200 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA j i jh' -ij Figure 13-1. Escherichia coli and Streptococcus faecalis under scanning electronmicioscopy. (a) E. coli. Scale bar =1 micrometer.ReproducedbypermissionofDavidScharf'PileofE. co/icells',published in ,s l American Vol 237 No 1 July 1977 pp 22-23.) (b) S.faecalis. Scale bar = 1 micrometer. (Photo: N. J. Horan. Department of Civil Engineering, University of Leeds, Leeds, UK) do not yield information that enables these sap- particularly associated with toxigenicity are 6, 8, 15, 20, rophytic organisms to be differentiated from the 25. 78, 115, 128, 148. 159. pathogenic strains. Serological tests are more useful. The ability to cause disease depends not only on the Particular serological groups, distinguished by their production of enterotoxin but also upon the ability to somatic antigen (O antigen), are commonly associated colonize the intestine. Various colonization factors, or with gastrointestinal disease. However, a particular adhesins, have been described that enable the bacteria strain cannot be assumed to be a pathogenic to attach to the small intestinal mucosa. These representative of a particular 0 group, unless a adhesins are plasmid controlled and are associated pathogenic mechanism (toxin production or invasive- with hair-like protein structures on the bacterial cell, ness) can be demonstrated or epidemiological evidence known as pili or fimbriae. There is now extensive links the strain to an outbreak. evidence that the presence of one or more of three It is valuable to distinguish between three different piliate bacterial antigens (K88, K99, and 987P) is types of pathogen within the E. coli group, a required for successful colonization by ETEC of the description of which follows. small intestine of piglets and calves. More recent work has identified two pili, CFAI and CFAII, as the adhesins ENTEROTOXIGENIC E. COLI (ETEC). Enterotoxigenic of functional importance in human infection. There is strains of E. coli can be the cause of a cholera-like some degree of host specificity among adhesins: K88 is syndrome in infants, children, and adults. ETEC especially associated with piglet infections, and K99 is produce either a heat-labile enterotoxin (LT), serologi- associated with calves and lambs. cally related to cholera enterotoxin, or a heat- stable enterotoxin (ST), which are structurally ENTEROINVASIVE E. COLI (ETEC). Enteroinvasive E. heterogeneous and may consist of LT complexed to coli produce disease by a mechanism similar to that of endotoxin. Some strains produce both toxins. Action Sligialla spp. These organisms invade the colonic of LT is analogous to that of cholera toxin. Production mucosa and cause bloody diarrhea. The property of enterotoxin is controlled by extrachromosomal seems to be restricted to a few 0 groups, 0 groups transferable DNA (plasmids). The ability to accept these particularly implicated are 28, 112, 115, 124, 136, 143, plasmids may be enhanced by particular 0 group 144, 147, 152, 164. antigens but, although this may be important in nature, in the laboratory enterotoxin plasmids (ENT) can be ENTEROPATHOGENIC E. COLI (EPEC). Organisms transferred to nonpathogenic 0 groups. 0 groups belonging to this group were first recognized as a result ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 201 of the serological examination of strains of E. coli cause diarrhea in fourteen volunteers at doses of isolated from outbreaks of diarrheal disease among 106-1010. Two ETEC strains isolated from patients in infants. Though undoubtedly some enterotoxigenic Vietnam caused mild diarrhea (three watery stools in and enteroinvasive strains have been included in this 24 hours) in three out of ten volunteers at a dose of 108, group, the pathogenic mechanism employed by most and severe diarrhea (ten or more watery stools over 48 of these organisms is not known. These strains have hours) in seven out of ten volunteers given a dose of been particularly associated with outbreaks of infantile 10 10. Two EIEC strains at a dose of 108 caused diarrhea gastroenteritis; they may, however, cause disease in (mild or severe) in eight of thirteen volunteers and adults. Experiments in adult volunteers have shown dysentry in three of thirteen volunteers; at a dose of 106 that nontoxigenic and noninvasive strains of E. coli they caused diarrhea in one of fourteen volunteers; and isolated from epidemics are able to produce diarrhea 0 at a dose of 104 they caused no diarrhea in ten groups particularly implicated are 18,20,25, 26, 28,44, volunteers. However, when the 106 dose of EIEC was 55, 86, 111, 112, 114, 119, 125, 126, 127, 128, 142. preceded by 2 grams of sodium bicarbonate, severe diarrhea and dysentery were induced in two of three Reservoirs volunteers. These results suggest a median infective dose (ID50) of around 109 for the ETEC strains tested It seems likely that pathogenic E. coli is and an ID50 of around 108 for the EIEC strains tested. transmitted from man to man. Studies on infection in Those infected excreted 10' EIEC per gram and 10'-109 pigs and calves, when considered in the context of the ETEC per gram of feces. problems that have been experienced in developing animal models of human infection, suggest a considerable degree of host specificity. Nonpathogenic Incubation period or commensal E. coli are numerous in the gut of all Most reports suggest an incubation period of 6 to 72 warm-blooded animals and for this reason have been hours. widely used as indicators of fecal pollution of the environment. Period of communicability Transm.issio The organisms are excreted typically for 3-5 days, but sometimes for 2-3 weeks. Colonization of the In nursery outbreaks, the main route of trans- intestine in which saprophytic F. coli is replaced by mission is by way of the hands of those nursing infected pathogenic E. coli can occur. Asymptomatic carriers of infants. It seems likely that fecal contamination of the ETEC and EPEC have frequently been reported. environment, fomites, and hands constitute the primary means of transmission and infection both among children and adults. Water- and foodborne Resistance outbreaks have been described. The presence of the receptors for K88 antigen in the As with the other bacterial enteric pathogens (except small intestine of the pig is genetically determined. Pigs Shigella), large numbers of ingested organisms are lacking the receptors cannot be infected by ETEC. It required to produce infection in healthy adults. seems likely that among human populations similarly Ferguson and June (1952) fed an EPEC serotype in milk unsusceptible individuals may occur. Over 50 percent to adult male prisoners in the USA. A dose of of children have antibodies to common EPEC serotypes 6.5 x 109 produced moderate or severe diarrhea in by the age of 1 year. These seem to confer resistance to seven of eleven volunteers, whereas a dose of 5.3 x 108 infection. Adults are susceptible to strains they have produced comparable symptoms in only one of twelve not previously encountered. Neonates and infants are subjects. In subsequent experiments, in the same prison the most susceptible group, and breast feeding may (June, Ferguson and Worfel 1953) with a different confer some protection. EPEC serotype, moderate or severe symptoms were produced by 1.6 x 1010 organisms in three of eight volunteers, by 5.3 x 109 in one of eight, by 1.7 x 109 in Epidemiology one of seven, and by 1.4 x 108 in one of eight. The great importance of ETEC in childhood diarrhea DuPont and others (1971) sought to infect adult in developing countries has only recently been male volunteers with EJ1 EC and EIEC strains in milk. An recognized. Knowledge of which strains of E. coli cause ETEC strain associated with diarrhea in piglets failed to diarrhea in which ways, and how these infections may 202 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA be diagnosed and categorized, is increasing rapidly. under 2 years old) in Central Java (Indonesia) in The newness and fluid state of the subject mean that January and February. Among those with diarrhea, 15 understanding of E. coli epidemiology is limited and percent excreted rotavirus, 12 percent excreted EPEC, subject to continual revision. In addition, the 24 percent excreted ETEC, 2 percent excreted laboratory techniques for declaring a particular Salmonella, and 2 percent excreted Shigella. Among organism to be ETEC (LT, ST, or LT + ST), EIEC, or EPEC those without diarrhea, the equivalent percentages are developing and are not entirely standardized were 0, 19, 58, 0, and 0, respectively. among different laboratories. Much of the data Freiji and others (1979) found that ETEC and EPEC produced by various surveys in the last five years are accounted for around 6.6 percent of reported therefore not strictly comparable. childhood diarrhea cases in the dry season Several studies in different parts of the world have (March-April), and around 14 percent in the wet shown that E. coli is a major cause of diarrhea, season (May-June), in Addis Ababa (Ethiopia). The especially among young children in poor communities. equivalent proportions for rotavirus were 1 1 and 34 Sack and others (19 75a) studied 59 Apache children, all percent in the dry and wet seasons, respectively. under 5 years of age, hospitalized with acute watery Koornhof and others (1979) recorded in South diarrhea at Whiteriver (Arizona, USA). These patients Africa that 33 percent of 479 black and white children had sixty-four episodes of diarrhea of which 9 percent with diarrhea, mostly under 2 years of age, were were associated with ETEC, I l percent with EPEC, 20 excreting EPEC serotypes compared with only 15 percent with Shigella, 3 percent with Salmonella, and 6 percent of 498 age-matched healthy control children. percent with ETEC plus another bacterial pathogen. Among those excreting EPEC, children with diarrhea Guerrant and others (1975) studied forty infants and excreted significantly greater numbers than healthy children (age 9 days to 10 years) admitted to the control children. ETEC were associated with only 10 hospital in Florian6polis (Brazil) with diarrhea. A percent of diarrhea cases, and no EIEC were recovered. potential pathogen was isolated from thirty-one cases EPEC appeared to be particularly prominent as a cause (78 percent). ETEC alone were isolated from twenty of diarrhea during the annual summer diarrhea peak. cases (50 percent), ETEC plus EIEC from five cases, ETEC In studies conducted prior to about 1970 it was plus Salmonella from two cases, EIEC alone from two common to fail to identify a known pathogen in the cases. EIEC plus Salmonella from one case, and stools of approximately 70 percent of diarrhea cases Salmonella alone from one case. Only one of twenty (see, for instance, Gordon 1964). The enormous healthy controls was excreting ETEC. progress in diarrheal etiology is illustrated by studies in Sebodo and others (1977) examined stool specimens Bangladesh. One study investigated forty-eight pa- from forty-one hospitalized children with acute tients with diarrhea admitted to Matlab hospital who diarrhea and sixteen healthy control children (all did not have V chlolerae, Salmonella, or Shigella in their Table 13-1. Etiology of diarrhea reported to Matlab Hospital, Bangladesh, during 1977 All patients Patients under 5 years Annual incidence Percentage wvith Percentage with Pathogen per 1,000 stated infectioni stated infection Enterotoxigenic E. coli 8.1 25 25 Rotavirus 7.5 23 40 Vibrio cholerue 3.7 12 5 Other vibrios 3.1 9 5 Shigella 1.5 5 5 Salmonella < I 103 fecal coliforms per 100 milliliters. a. When only a single value is given, it is a geometric mean. b. Total coliforms rather than fecal coliforms. ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 209 longer than those for Vibrio cholerae and other water, and the warmer the temperature the higher the salmonellae. death rate. Death rates are also higher in natural Waters with little or no microbial life will sustain waters with an active biological population, than in indicator bacteria for considerably longer than similar sterilized, filtered, or other "dead" waters (Poynter and waters with an active flora and fauna. Geldreich (1976) Stevens 1975). Under certain special conditions, reported that the tgo for fecal coliforms in filtered however, growth of indicator bacteria may occur. The stormwater was 40 hours at 20°C and 230 hours at growth phase is usually of limited duration and is 10'C. Gallagher and Spino (1968) found that the tgo for especially likely where nutrient levels are high, fecal coliforms in filtered streamwater was 168 hours at temperatures are warm, but overall microbial and 200C. zoological activity is low. Thus chlorinated effluents As with all the microbial survival data discussed in sometimes provide suitable growth environments for this book, temperature is a crucial factor. Mancini indicator bacteria (see the section below on effluent (1978) used published data to compute a relationship chlorination). Hendricks (1972) found that E. coli between decay rate and temperature in fresh water. The would grow at 30°C in autoclaved river water collected results showed a tgo of about 120 hours at 0°C, falling downstream of a sewage outfall, but not at 20°C or 5oC to about 15 hours at 30°C. Evison and James (1973) and not in autoclaved water collected upstream of the found that indicator bacteria in sewage effluent were outfall (see also Gorden and Fliermans 1978; reduced by 96.5 percent within 5 miles following Hendricks 1971; McFeters, Stuart and Olson 1978). discharge into the Nairobi River (Kenya; temperature Coliform growth is more likely than fecal coliform 18.5°C), whereas only a 56 percent reduction took growth, which is more likely than fecal streptococcal place over an equivalent distance in the River Tees growth (see, for instance, Allen, Pasley and Pierce (UK; temperature 20C). Davenport, Sparrow and 1952). The growth of indicator bacteria is more likely Gordon (1976) found fecal coliform and fecal than the growth of pathogenic bacteria. This latter fact streptococci reductions of only 84 and 67 percent, seriously reduces the value of the indicator bacteria as respectively, after 170 hours of travel under the ice of indicators of pathogenic microbes in situations where the frozen Tanana River (Alaska, USA), whereas a growth is possible or suspected; also, the human similar travel time in a tropical river might cause a excreted viruses (chapters 9-11) can neter increase in reduction of over six log units assuming that there were numbers in the aquatic environment. no additional inputs of fecal pollution. Many investigators have found that total coliform and fecal coliform decay rates are similar, whereas fecal streptococci often persist for longer (for instance, The microbiological quality of groundwater is Cohen and Shuval 1973; Poynter and Stevens 1975).2 becoming an increasing cause for concern worldwide Str. bovis, and to a lesser extent Str. equinus, however, as greater use is made of limited groundwater resources die-off considerably faster than fecal coliforms and and as the practice of disposing of fecal wastes in on- other species of fecal streptococci (Geldreich 1976; site sanitation systems or by land application becomes Geldreich and Kenner 1969; Guy and Small 1977; more common. The potential for groundwater con- McFeters and others 1974). Therefore, because Str. tamination depends upon a complex of factors includ- bovis and Str. equinus are the dominant streptococcal ing the rainfall, the rate of groundwater abstraction, species in some animal feces but never in human feces, groundwater depth and flow patterns, the method of it is sometimes the case that in stored samples waste disposal, and the type, texture, and depth of containing mainly human fecal pollution the fecal the overlying soil or rock. Marzouk, Goyal and Gerba coliform to fecal streptococci ratio falls over time, (1980) reported on the quality of ninety-nine whereas when nonhuman pollution predominates the groundwater samples in Israel. Measures of fecal ratio may rise (Feachem 1975; see chapter 4). coliforms per 100 milliliters were range 0-2 x 104, As a general rule indicator bacteria die in fresh mean l0O, and median 0. Measures of fecal streptococci per 100 milliliters were range 0-104, mean 300, and median 0. Tjostem and others (1977) found low levels 2. A recent report, however, suggested that Str.faecalis survived of coliform contamination in groundwater pumped for a shorter period in Canadian lake water than E. coli (Dutka and from a limestone aquifer in northeastern Iowa (USA). Kwan 1980). There is probably considerable inter- and intra-species variation in survival ability, and studies on mixed populations of Below the limestone, and separated from it by a shale fecal streptococci and E. coli cannot be compared directly with band, was a sandstone aquifer. Water pumped from the studies on the survival of single laboratory-maintained strains. sandstone in uncased wells was also contaminated, but 210 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA wells that were fully cased and grouted through the through the base of waste stabilization ponds (see, for limestone into the sandstone produced relatively instance, Ciravolo and others 1979). unpolluted water. This illustrates an important general There are few data available on the survival of principle-that unpolluted groundwater can often be indicator bacteria in groundwater. It may be obtained from below polluted shallow aquifers if anticipated that survival will be for longer than in must carefully designed abstraction technologies are em- surface waters because of the absence of sunlight, cool ployed. temperatures, and a low level of microbial and Over the past 60 years, studies have been conducted biological activity. Kudryavtseva (1972) reported that to determine the risks of shallow groundwater coliforms introduced into saturated alluvial sands in pollution from pit latrines and septic tank soakage the USSR during the summer survived for up to 3.5 systems. Stiles and Crohurst (1923) recorded the months. A pathogenic serotype of E. coli similarly movement of E. coli for 20 meters horizontally through inoculated into the groundwater survived for 3 months. fine sand in the direction of groundwater flow. In an In groundwater samples returned to the laboratory early study in Singapore (Yeager 1929) to investigate and stored in darkness, coliforms survived for up to 5.5 the required separation of bored hole latrines from months, and pathogenic E. coli survived for up to 4 shallow unprotected wells, it was found that coliforms months. traveled for more than 23 meters but less than 31 These and other data (Allen 1979) show that meters through very permeable soils. Similar studies whether or not on-site soakage or land application in West Bengal (India) showed that wells located 1.6 cause bacterial pollution of the groundwater depends meters from a bored hole latrine (dug in alluvial sandy on numerous site-specific factors. Where soils are of loam with a percolation rate of about 56 meters per fine or medium texture, unsaturated, and more than 1 day) became heavily contaminated with fecal coli- meter deep, little or no bacterial contamination of the forms, whereas most wells located 3.3 meters distant underlying aquifer may occur. Where wastewater can remained uncontaminated (Dyer, Bhaskaran and drain down through "macropores" (such as root Sekar 1945). Further information on the ability of channels, structural voids, rodent burrows, solution excreta disposal systems, especially septic tank channels or fissures) the groundwater may become drainfields, to pollute groundwater is reviewed below significantly polluted with fecal coliforms and fecal in the sections on septic tanks and land treatment. streptococci. Even in this latter case, however, the Groundwater pollution by fecal coliforms and fecal enteric bacterial concentrations in groundwater are streptococci may also be due to the deliberate recharge likely to be far less than in surface waters in the same of sewage effluents to groundwater. Vaughn and others location and will be readily eliminated by any water (1978) studied three sewage recharge installations on treatment process including chlorination. Even where Long Island (New York, USA). At site 1, the untreated waters are being used for domestic purposes, chlorinated effluent contained up to 2.4 x 106 fecal contaminated groundwater will usually pose a lesser coliforms per 100 milliliters, and the groundwater (9 health risk than available surface water. meters below the recharge basins) contained up to 150 fecal coliforms per 100 milliliters. At site 2, the In drinking water chlorinated effluent contained up to 4.3 x 105 fecal coliforms per 100 milliliters, and the groundwater (24 Treated and chlorinated drinking water should meters below the recharge basins) contained up to 930 contain no fecal indicator bacteria. Most people in fecal coliforms per 100 milliliters. At site 3, the tertiary developing countries, however, drink unchlorinated effluent contained up to 9.3 x 105 fecal coliforms per and untreated water. In cases where this water derives 100 milliliters, and the groundwater (5.5 meters below from protected groundwater, or upland surface water the recharge basins) contained up to 150 fecal sources, it may be of moderately good quality (say coliforms per 100 milliliters at a point 46 meters < 100 fecal coliforms per 100 milliliters). In other cases horizontally downslope from the recharge site. Slade the water used may be highly polluted and, on and Edworthy (1981) isolated up to 1.2 x 105 E. coli occasions, has an indicator bacteria concentration and fecal streptococci per 100 milliliters of ground- similar to that of a weak raw sewage. In table 13-2, water from a chalk aquifer directly below groundwater some information on the pollution of drinking water recharge lagoons receiving raw comminuted sewage. sources in developing countries is summarized. Bacteriological aspects of groundwater recharge in This problem of fecally polluted drinking water is by Israel are summarized by Goldshmid (1974). Ground- no means restricted to the developing countries. water contamination may also result from seepage Sandhu, Warren and Nelson (1979) reported that ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 211 around 60 percent of people in three counties in South 100 milliliters, and this level of contamination can only Carolina (USA) were served by wells, springs, and be removed by adding a chlorination unit. Therefore, other private water sources. In one county, private to set a zero fecal coliform standard is equivalent to water sources had a mean E. coli count of 1.4 x 106 per requiring that all water supplies be chlorinated (at 100 milliliters and a mean fecal streptococci count of least). Many developing countries, however, have 2.6 x 106 per 100 milliliters. It was concluded that decided to adopt a flexible policy toward water defective septic tank systems were responsible for most treatment and are installing numerous spring, well, or of the fecal contamination. upland stream supplies that have no treatment The question of bacteriological standards for processes. The advantage of designing a supply drinking water remains a subject of considerable without treatment is that it is somewhat cheaper, and debate. In countries where all, or nearly all, the much easier to operate and maintain, than a similar population drink treated piped water it is reasonable supply with treatment (for instance, slow sand filtration and correct to stipulate that no coliforms or other and chlorination). For many developing countries, indicator bacteria should be detected in tap water. therefore, a zero fecal coliform standard is in- Failure to meet this standard indicates a malfunction appropriate. A preferable approach is to set flexible of the treatment plant (especially of the chlorination quality goals that can be changed as the water supply unit) or an inflow of pollution through a damaged sector progresses. To install an improved supply section of the distribution system, which should be providing water with up to 50 fecal coliforms per 100 immediately investigated and rectified. In developing milliliters, for instance, is a great advance when many countries, however, the great majority of the popu- people in the same country may be drinking water lation drink water that is untreated, either from containing over 103 fecal coliforms per 100 milliliters. improved but untreated supplies (such as handpumps) The effect collecting, carrying, and storing water or from unimproved supplies (such as ponds). This have on bacteriological water quality has attracted water, as indicated in table 13-2, may be grossly increasing concern in recent years. Clearly, there is less polluted, and it is pointless for the government of such purpose in supplying good quality water at a public tap a country to require that all water supplies contain no if it is to become subsequently polluted prior to use. If fecal coliforms. At the best such a ruling will simply be water is collected in clean vessels and stored in such a ignored and thus bring similar regulations into way that polluting material cannot enter, water quality disrepute; at the worst it may force people to abandon is likely to improve-as suggested by the data from improved but lightly contaminated supplies in favor of Malumfashi (Nigeria) presented by Tomkins and the only alternative, which may be unimproved and others (1978) and summarized in table 13-2. It may be heavily polluted supplies. For example, there have been more usual, however, for water quality to deteriorate cases where overzealous health officials have closed between collection and use because the water down contaminated shallow tubewells in a village collection vessels are contaminated and the water is because the wells were found to contain 50 fecal stored in the home in such a way that it can be further coliforms per 100 milliliters and have thus forced the contaminated by children and animals. Studies in villagers to use polluted irrigation canals containing Lesotho (Feachem and others 1978) showed that clean 104 fecal coliforms per 100 milliliters. water collected from a handpump (0-6 fecal coliforms The World Health Organization (WHO) has and 0-1 fecal streptococci per 100 milliliters) could generally advocated standards or guidelines for small become considerably contaminated before use (maxi- untreated water supplies that stipulate less than 10 mum of 1,340 fecal coliforms and 4,280 fecal coliforms and zero fecal coliforms per 100 milliliters streptococci per 100 milliliters). Similarly, Oluwande (WHO 1971). These recommendations have been (1980) reported that public tap water in Western State questioned by those primarily concerned with water (Nigeria) contained 0-3 coliforms and 0 fecal coliforms supplies in developing countries on the grounds that per 100 milliliters, whereas stored water in homes they are too stringent (for instance, see Feachem 1977). contained 0-1,800 coliforms and 0-10 fecal coliforms Even if great attention is paid to selecting the purest per 100 milliliters. The epidemiological significance of available water source and distributing the water water pollution occurring after collection is different through a well-designed and well-maintained system, it from that of pollution of the water source. The first type will not in general be possible to meet a zero fecal of pollution promotes intrafamilial disease trans- coliform standard without incorporating chlorination. mission, whereas the second allows the spread of Well-designed untreated spring supplies, for instance, infection throughout a community using a common will typically contain up to about 25 fecal coliforms per source. 212 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA In concluding this section on indicator bacteria in fecal bacteria, especially coliforms, is considerably drinking water, a note of caution must be sounded more extensive. about the validity of the standard tests for fecal Numerous studies have documented high levels of coliforms, which were developed in Europe and North indicator bacteria (up to 103-105 per 100 milliliters) in America, when they are applied to tropical waters. ocean or estuarine waters near sewage outfalls. Recent Some workers studying water pollution in upland examples from the USA include studies at Miami tropical areas, where surface water temperatures are Beach (Florida; Edmond, Schaiberger and Gerba not greatly higher than in temperature zones, have 1978), Honolulu (Hawaii; Loh, Fujioka and Lau obtained satisfactory results using standard methods 1979), the Texas Gulf Coast (Gerba and others 1977; for enumerating fecal coliforms [for instance, Feachem Goyal, Gerba and Melnick 1977, 1978, 1979), Long (1974) in the highlands of Papua New Guinea and Island, (New York; Vaughn and others 1979), and the White, Bradley and White (1972) in Uganda]. Other New York Bight (Berg and Metcalf 1978). Studies from studies in the tropics [for instance, Banerjea and Sen other countries include those at Tel Aviv (Israel; (1940) and Raghavachari and Iyer (1940) in India; Shuval 1978), Alexandria (Egypt; Hakim 1978), Boizot (1941) in Singapore; Evison and James (1973) Kerala (India; Raveendran, Gore and Unnithan 1978). in Kenya; Katugampola and Assim (1958) in Sri Naples (Italy; Evison and Tosti 1980), Tuscany (Italy; Lanka; and Moussa (1965) in Egypt] have detected a Petrilli and others 1979), Whitely Bay (UK; Evison considerable proportion of coliforms of probable and Tosti, 1980), Liverpool (UK; Karthegisan and nonfecal origin that have the ability to ferment lactose Pugh Thomas 1980), Belgium (Yde and de Maeyer- at 44°C. In this respect they mimic the truly fecal Cleempoel 1980), and New South Wales and Tasmania coliforms and are thus able to give false positive (Australia; Roper and Marsall 1979). In several of reactions on standard fecal coliform tests. Recent water these studies (for instance, those in Texas) fecal testing in the Gambia (Barrell and Rowland 1979b) indicator bacteria were isolated at higher con- and Tanzania (Brokunsult and Ross Institute 1978) centrations (10-1,000 times higher) from bottom has shown a high prevalence (up to 55 percent) of false sediments than from the overlying waters. Roper and positive results presumably caused by nonfecal Marshall (1979) showed that E. coli in saline sediments coliforms that reside in warm tropical waters and have were protected against attack by viruses, bacteria, and the ability to ferment lactose at 44°C. There is an amoebae, and growth of coliforms in marine sediments urgent need for the development of a test for fecal has been demonstrated (Gerba and McLeod 1976). indicator bacteria in tropical waters that will reliably Numerous estimates of coliform death rates have and simply distinguish between organisms of enteric been made. Chamberlin and Mitchell (1978) and origin and others that are free-living and adapted to Mitchell and Chamberlin (1978) reviewed eighty-seven warm, aqueous habitats. [See note on page 66.] of these estimates and concluded that the times of 90 percent reduction (tgo) lay between 0.6 and 8 hours, Ill seawflater with a geometric mean of about 2 hours (correspond- ing h- values are 0.3-4 per hour with a mean of 1.15 per The great majority of coastal towns and cities that hour-see footnote 1, above). These values reveal have a sewerage system discharge their sewage into the considerably faster death of coliforms in seawater than sea following little or no treatment. This is true in fresh water (where t90 values are between 20 and 115 throughout the world. The design of these marine hours, with a median of about 60 hours). Death rates of outfalls has attracted considerable interest over the coliforms in seawater are also considerably faster than past two decades and involves complex decisions about the death rates of viruses in seawater (tgo values in the the degree of treatment and the design of the outfall range of 15-70 hours-see chapter 9). There is now and complex tradeoffs between costs and environ- widespread agreement that, owing to the greater mental hazards. The principal health-related fecal persistence of enteric viruses, fecal coliforms are an hazards are the risks to swimmers and the con- inadequate index of saline water quality, especially in tamination of fish and shellfish. shellfish-growing areas (Berg and Metcalf 1978). Fecal To design outfalls in such a way that fecal bacteria streptococci survive longer in marine environments and viruses do not pollute beaches or seafood requires than fecal coliforms (Baross, Hanus and Morita 1975; a detailed knowledge of the dispersion, sedimentation, Hanes and Fragala 1967; Petrilli and others 1979; and death of fecal microorganisms discharged into Vasconcelos and Swartz 1976), but not sufficiently long coastal waters. The information on viruses is briefly for them to act as an adequate indicator of the reviewed in chapter 9, and the available knowledge of enteroviruses. Pichot and Barbette (1978) found a t90 ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 213 of 3.7 hours for fecal coliforms and 5.7 hours for fecal Recent evidence from Egypt and the USA (Cabelli streptococci under the same experimental conditions. 1979; Cabelli and others 1979) revealed a small but The reasons for the rapid death of coliforms in measurable difference in the incidence of gastrointes- seawater have been the subject of many investigations tinal illness between swimmers and nonswimmers at (Mitchell 1968). Faust, Aotaky and Hargadon (1975) polluted beaches. The recorded risks of swimming in found temperature, dissolved oxygen, and salinity to be seawater containing 102-103 fecal coliforms per 100 the major determinants of the rate of death, and milliliters were an additional attack rate of 1-2 cases of Enzinger and Cooper (1976), McCambridge and gastrointestinal illness per 100 people in the 8-10 days McMeekin (1979) and Mitchell and Yankofsky (1969) following thevisit to the beach. It must be kept in mind, drew attention to the important role of protozoan however, that especially in developing countries the predators. Gerasimenko (1977) found that oil pol- infections that may be transmitted to swimmers at lution did not affect coliform death rates. polluted beaches will usually be highly endemic in the An increasingly convincing case has been built for community at large (the community producing the the importance of light-induced cell damage in wastes which are polluting the sea), and swimming may determining coliform death rates in sea water constitute a negligible additional risk. Set against this (Chamberlin and Mitchell 1978; Chojnowski, Mancini is the possibility that swimmers from high socio- and Jeris 1979; Gameson and Gould 1975; Gameson economic strata (who experience a low risk at home and Saxon 1967; Mitchell and Chamberlin 1975,1978). due to adequate water supply, sanitation, and hygiene) Experiments on fecal coliforms in Sydney harbor may be exposed to a substantially increased risk of (Australia) showed a minimum daytime t90 of 1.9 infection when they bathe in seawater polluted by the hours and a night time tgo of 40 hours (Bellair, Parr- wastes of all socioeconomic strata. The same level of Smith and Wallis 1977). Fecal streptococci appear to additional risk may apply to tourists who are usually be substantially less sensitive to light than coliforms either local residents from upper socioeconomic (Chamberlin and Mitchell 1978). groups or foreign visitors. Little information is available on the survival of indicator bacteria in tropical seawater. In extrapolat- ing results from temperate areas, temperature is the variable of most importance. Even relatively small The fecal indicator bacteria are excreted by almost temperature differences can substantially affect the all people, and by almost all warm-blooded animals, death rate. Jamieson, Madri and Claus (1976) reported nearly all of the time. They are therefore ubiquitous that in sterilized saline waters a pathogenic serotype of and numerous in all materials containing fresh human E. coli had a tgo of about 40 hours at 40C and about 8 or animal feces. The fecal indicator bacteria are a part hours at 37°C. Vasconcelos and Swartz (1976) of the vast total intestinal microflora. A healthy reported that E. coli concentrations in seawater individual may commonly excrete 1011-1012 bacterial declined by less than 2 log units at 8.9°C, but by 7 log cells per wet gram of feces, and these cells may units at 14.5°C, after 6 days. Burdyl and Post (1979) constitute about 9 percent of the total fecal wet weight studied E. coli survival in the Great Salt Lake (USA) or 25 percent of the fecal dry weight (Geldreich 1978). and estimated a tgo of about 110 hours at 9°C and The composition of this total bacterial population is about 21 hours at 19°C. Faust, Aotaky and Hargadon set out in table 1-6. It is usual for the anaerobes, (1975) reported t,0 values for E. coli in estuarine water especially Bifidobacterium and Bacteroides, to be a of 39 hours at 0°C and 14 hours at 30°C. Mancini more numerous and more stable component of the (1978) reviewed reported death rates and temperatures fecal flora than the fecal coliforms or fecal streptococci and computed typical tgo values of 60 hours at OC and (see, for instance, Mata, Carrillo and Villatoro 1969; 7 hours at 30°C. Clearly, coliforms discharged into Tomkins and others 1981; Zubrzycki and Spaulding tropical seawater will rapidly decline in numbers, as 1962). will other excreted bacteria, although not necessarily at The numbers and the serotypes or species of fecal the same rate. Excreted virus concentrations will coliforms and fecal streptococci excreted by humans decline considerably more slowly (see chapter 9). vary considerably between individuals according to An active debate continues about the magnitude of age (Gorbach and others 1967), diet (Bettleheim and the health risk associated with swimming in fecally others 1977), state of health, and chemical and polluted seawater and the correct approach to water microbiological properties of the intestine. Wheater, quality standards and legislation (Cabelli 1979; Evison Mara and Oragui (1979) studied twelve adults in and Tosti 1980; Moore, Perin and Maiden 1979). Dundee (Scotland) and found between 8 x 104 and 214 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA 8 x 107 fecal coliforms, and between 3 x 102 and effluents. Concentrations of indicator bacteria in 2 x 107 fecal streptococci, per gram of wet feces. sewage vary through the day, but this variability is However, community averages are less variable and considerably less in the sewage derived from large are in the ranges of 106-109 fecal coliforms per gram communities than in that derived from small and 105-10' fecal streptococci per gram (table 1-6). communities. Communities with a high water use per Fecal coliform concentrations are usually higher than capita produce a sewage with a lower concentration of those for fecal streptococci by a factor of 4 or more, at indicator bacteria than communities with lower water least in the developed countries whence most such data usage. Thus, indicator bacteria concentrations in come. sewage in developing countries are generally higher The numbers and serotypes of fecal coliforms than those reported from industrialized countries. excreted by a single individual vary through time due Raw sewage typically contains between 105 and 108 to the influence of many factors. In particular, the fecal coliforms and fecal streptococci per 100 milliliters. proliferation of a pathogenic bacterium may modify Berg and Metcalf (1978) reported between 3.8 x 104 the commensal flora in the intestine. Dale and Mata and 4.6 x 106 fecal coliforms per 100 milliliters of (1968) found that eight children in Guatemala with sewage in the USA. Geldreich (1978) reported that shigellosis excreted between 104 and 108 coliforms per twenty-one towns in the USA had between 3.4 x 105 gram and that coliform excretion had a roughly inverse and 4.9 x 107 fecal coliforms and that seven towns had relation to Shigella excretion. Streptococci were between 6.4 x 104 and 4.5 x 106 fecal streptococci per excreted by the same children in concentrations of 100 milliliters of sewage. Davis (1979) found that raw 108-109 per gram. sewage in Houston (Texas, USA) contained 3 x 10' to Most nonhuman animals excrete 105 or more fecal 3 x 107 fecal coliforms and 5 x 105 to 2 x 106 fecal coliforms and fecal streptococci per gram of feces. streptococci per 100 milliliters. In the Dundee area However, some animals excrete <105 per gram, as (Scotland), raw sewage contained 5.8 x 106 to reported for horses and rabbits, respectively, by 1.5 x 107 E. coli per 100 milliliters (Wheater and others Geldreich (1978) in the USA and by Wheater, Mara 1980). and Oragui (1979) in Scotland. It has often been Evison and James (1973) reported that raw sewage claimed in the literature from the USA (for instance, in Nairobi (Kenya) contained up to 1.6 x 108 E. coli, Geldreich 1976) that fecal streptococci concentrations and up to 3.5 x 107 fecal streptococci, per 100 generally exceed fecal coliform concentrations in milliliters. In contrast, and presumably because of animal feces and that the reverse is true for human higher levels of water use, raw sewage in Pietermaritz- feces. However, Wheater, Mara and Oragui (1979) burg (South Africa) contained only 1.5 x 104 E. coli showed that this was not the case for sheep, pigs, cats, per 100 milliliters (Grabow and Nupen 1972). In dogs, hens, ducks, pigeons, and seagulls in Scotland Brazil, Mara and Silva (1979) reported a mean of (see also Williams Smith and Crabb 1961). This 5 x 107 fecal coliforms and 7 x 106 fecal streptococci variability in fecal coliform to fecal streptococci ratios per 100 milliliters of raw sewage. is one of the reasons for the current rejection of the Concentrations of indicator bacteria in sewage may ratio as a method for distinguishing between human be affected by the presence of industrial wastes that and nonhuman fecal pollution (see chapter 4). often contain chemicals antagonistic to enteric Jordan (1926) studied the survival of E. coli in stored bacteria. Data on raw sewages from different areas of feces. At room temperature, numbers increased to Birmingham (UK) showed E. coli concentrations of 108-101" per gram after 2-5 days and subsequently 1.7-3.7 x 108 per 100 milliliters where sewage was decreased to undetectable levels in 6-12 weeks. At principally of domestic origin, compared with only 37°C, numbers initially increased markedly but then 9 x 105 per 100 millimeters where sewage flow was 60 declined to zero within 1-3 weeks. At 10°C, a slower percent of industrial origin and contained 20-30 increase in numbers occurred, to a maximum of milligrams per liter of phenols (Pike and Carrington l08 1010 per gram after 20 days, and 104 per gram 1979). could still be detected after 23 weeks. Studies of sewage produced by small rural communities in the hills of Yorkshire (UK) have shown the fecal coliform concentrations to vary between 105 and 108 per 100 milliliters, whereas fecal streptococci Because the fecal indicator bacteria are ubiquitous vary between 104 and 107 per 100 milliliters (Feachem, and numerous in feces, they are also ubiquitous and unpublished data). Sanitation technologies that use numerous in raw sewage and in most treated sewage little water, for instance the pour-flush designs, will ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 215 produce a sewage with an exceptionally high survived for longer in summer than in winter. At concentration of indicator bacteria. Daniel and Lloyd warmer temperatures (say > 25°C), however, it is likely (1980) reported a geometric mean from twelve samples that a vigorous growth period would be followed by a of 8.4 x 10i coliforms per 100 milliliters of sewage rapid decline. Overall survival times of indicator flowing into an Oxfam sanitation unit installed in a bacteria in sludge in the tropics will typically be shorter refugee camp near Dacca (Bangladesh). than in temperate climates. Some studies on the survival of coliforms and streptococci in sewage are listed in the appendixes of I soil Feachem and others (1980). Survival is greatly prolonged at cool temperatures, when dissolved Fecal indicator bacteria occur in only very low oxygen is low (Hanes, Sarles and Rohlich 1964), or concentrations (typically less than 2 per gram) in when the overall microflora have been reduced by most uncontaminated soils (Geldreich and others chlorination or some other means. In warm climates, 1962). In contrast, they are found in high con- with sewage temperatures around 25-30°C, a >99 centrations in soil wherever effluent, night soil, sludge, percent reduction in indicator bacteria concentrations or manure are being used for irrigation or fertilization may be expected in about 10-15 days, depending on or where livestock are grazing. The literature on the the level of oxygenation of the sewage. It is generally survival of enteric bacteria in soil is extensive and dates reported that fecal streptococci survive for a little back to the early 1920s (see the appendixes of Feachem longer than fecal coliforms in sewage (see, for instance, and others 1980). This literature has been periodically Berg and Metcalf 1978; Cohen and Shuval 1973). reviewed (see, for instance, Elliott and Ellis 1977; One study recorded a far more rapid rate of death for Gerba, Wallis and Melnick 1975a; Rudolfs, Falk and fecal indicator bacteria in sewage under natural Ragotzkie 1950). conditions (Dor, Schechter and Shuval 1976). The Reported survival times vary widely. The work of undiluted raw sewage of Jerusalem (Israel) entered Van Donsel, Geldreich and Clarke (1967) clearly the Nahal Soreq wadi at a rate of about 21,000 cubic demonstrated the importance of sunlight and tempera- meters per day. After a flow of 45 kilometers (which ture in determining the death rate of fecal bacteria in took about 44 hours), at a temperature of around 20°C soil. Times for 90 percent reduction (tgo) varied from a (March), the fecal coliform and fecal streptococci minimum of about 3 days in summer in exposed sites to concentrations were reduced by 99.9 and 99 percent, maxima of about 14 days for E. coli and 20 days for Str. respectively. The combination of warm temperatures, faecalis in autumn and winter at shaded sites. In spring highly turbulent flow in some sections of the wadi, and and winter Str. faecalis survived for approximately a rich algal community contributing photosynthetic twice as long as E. coli whereas in summer and autumn oxygen produced a warm and well-aerated environ- the two survival times were similar. This may have been ment that caused rapid death of excreted bacteria. because some E. coli growth was occurring in summer and autumn. In sludge In Alberta (Canada) studies were conducted on the weekly application of 45 millimeters of unchlorinated Fecal indicator bacteria are always present in high waste stabilization pond effluent to plots of canary concentrations in fresh sewage works sludge. grass (Bell and Bole 1978). The effluent contained Concentrations of 10i-10i total coliforms, 10i_107 between 2.3 x 104 and 1.7 x 105 fecal coliforms per fecal coliforms, and 104 106 fecal streptococci per 100 milliliters, and most coliforms were retained in the gram are normal. Dudley and others (1980) in- upper 80 millimeters of the loamy sand. Fecal coliform vestigated an anaerobically digested sludge and two dieoff occurred in two phases. Over the first 2 days after primary sludges at San Antonio (Texas, USA) and effluent application a 90 percent reduction occurred. found 5 x 10i-5 x 106 fecal coliforms and Subsequently, the reduction was about 33 percent per 7 x 104-5 x 105 fecal streptococci per gram of day at 15°C and about 25 percent per day at 10°C. In suspended solids. spring and summer, little or no fecal coliform As with coliforms in feces, night soil, and soil, contamination could be detected 2 weeks after the coliforms in sludge may survive for several months in cessation of irrigation. cool, moist conditions. Growth may also occur, and Chandler and Craven (1978a) studied the disposal to this will be more rapid at warmer temperatures. land of piggery waste containing 10'-108 E. coli per Edmonds (1976) reported that fecal coliforms in sludge 100 milliliters in Victoria (Australia). E. coli con- applied to forest soil in Washington State (USA) centrations in the soil declined by 99 to 99.99 percent 216 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA after 3-6 weeks, and rapid downward movement of E. plants compared with their survival on the underlying coli was recorded in late summer when the soil was dry soil (Chandler and Craven 1978a, 1978b, 1980). Under and cracked. In other experiments, Chandler and conditions in which E. coli survived on soil for 8 weeks, Craven (1978b) recorded a 99 percent reduction of E. no E. coli were recovered from grass after 16 days. coli in 1 day in dry soil, whereas in saturated soil the Persistence of E. coli on the grass stems was greatest reduction was less than 90 percent after 3 weeks. near the soil surface. Similarly, Chandler and Craven (1980) recorded tg9 Experiments in Alberta (Canada) on the spray values for E. coli at 20°C of 18 days in soil with 30 irrigation of fodder crops with waste stabilization pond percent moisture and 2.5 days in soil with 10 percent effluent (containing 102_106 fecal coliforms per 100 moisture. milliliters) have demonstrated the importance of Kibbey, Hagedorn and McCoy (1978) found that climatic conditions and the anatomy of the plant in the survival of Str.faecalis in various loams was mostly determining the survival of excreted bacteria (Bell dependent upon temperature and moisture levels. The 1976; Bell and Bole 1976). Fecal coliforms on alfafa time for 95 percent reduction (t95) in saturated soils (Medicago sath,a) declined by over 99 percent in 1 day was 94 days at 4°C, 80 days at 10°C, 53 days at 25°C, when temperatures were warm (12-23°C), relative and 29 days at 37°C. In air-dried soil the tr5 values were humidity was low (20-65 percent) and there were 23 days at 4°C, 18 days at 10°C, 9 days at 25°C, and 5 about 9 hours per day of bright sunshine. When days at 37°C. temperatures were cooler (9-18°C), relative humidities Under certain soil conditions coliform and fecal higher (48-95 percent), and the sky was overcast, a 99 coliform concentrations will increase, and this increase percent reduction required 4 days. In contrast, fecal will be more rapid at warmer temperatures (see, for coliforms on reed canary grass (Phalaris arundinacea), instance, Guy and Small 1977). Survival times and the bromegrass (Bromus inermus) and orchard grass potential for growth are influenced by the availability (Dactylis glomerata) grasses that, unlike alfafa, of nutrients in the soil. Thus, survival is prolonged in possess leaf sheaths-only underwent a 99 percent soil that is regularly receiving effluent or night soil reduction in 5 days even in bright weather conditions. applications. Dazzo, Smith and Hubbell (1973) The authors argued that sunlight is an important recorded tgo values forE. coli of 4 days in soil receiving determinant of bacterial death rates and that plant no manure and 8.5 days in soil receiving 50 millimeters anatomy controls the degree to which effluent droplets of cow manure slurry per week. on plant surfaces are exposed to sunlight. Greenhouse Survival of indicator bacteria in soil is influenced by studies (Brown, Jones and Donnelly 1980) showed that moisture content, temperature, shade, soil organic 25 millimeters of simulated rainfall, falling in 1 hour, content and the overall biological activity present in reduced E. coli on grass by 90-99.9 percent. In the the soil. These conditions are so variable that reported absence of rainfall, the same level of reduction under survival times and tgo values cover a wide range. From the same conditions took 10-25 days. an overview of the literature (see the appendixes of Sadovski and others (1978) studied the survival of a Feachem and others 1980), it appears that fecal mutant E. coli inoculated into waste stabilization pond coliforms generally survive for less than 10 weeks, with effluents that were applied to drip irrigation to a 90 percent reduction taking place within 10 days. cucumber plots on two farms in Israel. At one site (air Under cool, moist conditions a hardy residual fraction temperature 13-30°C, soil temperature at noon of fecal coliforms may survive for many months. Where 22-30°C, sunlight 9.5 hours per day, relative humidity conditions are hot and arid very limited survival can be 27-55 percent), a single irrigation was performed with expected, and it is probable that almost complete inoculated effluent containing 107 mutant E. coli per elimination of fecal indicator bacteria will occur within 100 milliliters. Mutant E. coli were still detectable in the 2 weeks. irrigation water, at a concentration of > 103 per 100 milliliters, 8 days after the flow of inoculated effluent. The soil contamination immediately after irrigation On crops with inoculated effluent was 107 mutant E. coli per 100 Crops irrigated or fertilized with effluent, night soil, grams of dry soil and persisted at a level of > 106 per sludge, or manure may be heavily contaminated by 100 grams for at least 8 days. Cucumbers grown in fecal indicator bacteria, whereas untreated plants and exposed soil were contaminated by 104 mutant E. coli crops are not (Geldreich, Kenner and Kabler 1964). per 100 grams immediately following the inoculated Studies in Victoria (Australia) demonstrated the irrigation, and this contamination fell to 65 per 100 very limited survival times of excreted bacteria on grams after 8 days. When the soil and drip lines were ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 217 covered with polyethylene sheets to reduce evap- place within I week. In arid regions with low cloud oration and raise temperature, no mutant E. coli could cover, complete elimination is likely to take place be detected on cucumbers 1 day following the within 1 week. inoculated irrigation. At the second site (air tempera- The reduction of fecal contamination of harvested ture 23-28°C, soil temperature at noon 40-43°C, crops depends not only on the microbial death rates on sunlight 11.8 hours per day, relative humidity 62-70 plant surfaces but also on the technology employed for percent), three irrigations were performed with irrigation or fertilization. The use only of treated inoculated effluent containing 4.4 x 1011 mutant E. effluent, night soil or sludge; the application of the fecal coli per 100 milliliters. After the third inoculated material to the soil (for instance, by drip irrigation) irrigation the soil contained 1.3 x 106 mutant E. coli rather than over the crops (for instance, by spray per 100 grams (dry weight), and this contamination fell irrigation); covering the soil with plastic sheets to to 130 per 100 grams after 9 days and maintained this reduce evaporation; and the cessation of irrigation level for a further 11 days. Unlike at the first site, where about two weeks prior to harvesting will all greatly irrigation with uninoculated effluent had continued reduce crop contamination. throughout the study, in this case the irrigation terminated 5 days after the third inoculated irrigation, Infish and shellfish and consequently the soil moisture content fell from 15 percent to 3 percent. Bacterial contamination on Fish and shellfish that live in water contaminated by cucumbers grown in exposed soil rose to 1.7 x 103 fecal discharges are frequently found to contain fecal mutant E. coli per 100 grams but rapidly declined indicator bacteria. Several studies have shown that following the last inoculated irrigation. When the soil these bacteria are not part of the normal flora of the and drip lines were covered with polyethylene sheets, intestines of freshwater or saltwater fish (Geldreich no mutant E. coli could be detected on the cucumbers. and Clarke 1966; Guelin 1962). Fish intestines may Earlier studies at the first site by the same workers contain fecal coliforms and fecal streptococci only (Sadovski, Fattal and Goldberg 1978) showed that when the fish have been living in fecally contaminated harvested cucumbers and eggplants, irrigated with water, and these bacteria may survive, and perhaps sewage effluent containing 106 fecal coliforms per 100 multiply, for periods of up to 14 days (Glantz and milliliters, were contaminated by, on average, 389 fecal Krantz 1965) in the fish intestines. coliforms per 100 grams when drip-irrigated through- Most investigations have concentrated on the out the growing season on exposed soil, but by only 30 bacterial contamination of shellfish rather than fish. per 100 grams when drip-irrigated on soil covered by This is because the method of filter feeding of bivalve polyethylene sheets. Irrigating with sewage effluent only molluscs concentrates bacteria in the same way as it during the early stage of growth (up to flowering) concentrates viruses (see chapter 9; Metcalf 1978; produced a final contamination level on harvested Wood 1979) and because molluscs are often eaten raw vegetables similar to that found when irrigation was or only lightly cooked. Goyal, Gerba and Melnick with fresh water (around 2.5 fecal coliforms per 100 (1979) investigated oyster beds in Galveston Bay grams). (Texas, USA) and found fecal coliform concentrations Other reports of coliform survival on crops are listed per 100 milliliters of up to 2,400, 46,000, and 46,000, in the appendixes of Feachem and others (1980) and respectively, in water, sediment, and oysters. Similar have been reviewed elsewhere (for instance, Elliott and results were obtained by Slanetz, Bartley and Stanley Ellis 1977; Geldreich and Bordner 1971; Rudolfs, Falk (1968). Munger, Heyward and Dutton (1979) recorded and Ragotzkie 1950). Fecal bacteria in soil may be in that fecal coliform concentrations in clams in the relatively sheltered and supportive microhabitats Seattle area (Washington, USA) were up to 59 times where moisture, shade, and nutrient availability permit higher than in the surrounding water. survival for many weeks. In contrast, bacteria on crop Mitchell and others (1966) studied the uptake and surfaces will in general be exposed to desiccation and elimination of E. coli by the Eastern oyster sunlight, and their survival is very much shorter than in (Crassostrea virginica) in sterilized seawater at 20°C. soil. Rapid death is promoted by high air temperatures, When the seawater was inoculated with 103 E. coli per bright sunlight, low relative humidity, and a plant milliliter, the oysters accumulated over 104 E. coli per anatomy that does not offer many sheltered sites. gram within 4 hours. When the seawater contained Under most conditions, fecal indicator bacteria are about 10 E. coli per milliliter, the oysters accumulated unlikely to survive for more than 4 weeks on crop over 100 per gram within 4 hours. When the surfaces with at least a 99 percent reduction taking contaminated oysters were rinsed in clean water and 218 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA placed in sterilized seawater, the E. coli concentrations produced droplets that contained an average declined by 99 percent in 10 hours, and fell below the concentration of E. coli 30 times greater than that in the level of detection after 50 hours. In similar experiments column. In similar experiments Blanchard and Syzdek Hoff and Becker (1969) reported that Olympia oysters (1970) produced droplets that contained up to 1,000 (Ostrea lurida), in sterilized seawater containing 10 E. times more Serratia marcescens per milliliter than the coli per milliliter, accumulated 110-320 E. coli per water column from which the droplets were produced. gram after 24 hours at 6-il VC. When the oysters were The concentration of bacteria in the droplet depended rinsed and replaced in sterilized seawater, E. coli levels on the size of the droplet, with highest concentrations fell to about 1 per gram after 48 hours. occurring in droplets 60-80 micrometers in diameter. Jegathesan and others (1976) purchased three The aerosolized excreted bacteria most encountered species of commonly eaten shellfish (cockles, Anadura by people in developed countries are those produced granosa, and two species of mussels, Modiolus by the flush toilets in their houses. Darlow and Bale senhaussi and M. metcalfi) from markets in Malaysia (1959) inoculated wash-down toilet bowls with and examined them for bacterial entericpathogens. Of 1011_10i2 Serratia marcescens and investigated the twenty cockles examined, nine contained coliforms production of airborne organisms when the low-level, (mean concentration of 8.9 x 104 per gram), and seven 9-liter cistern was flushed. At the level of the seat, near isolations of pathogenic serotypes of E. coli were made. the bowl, 7 x 104 Serratia per cubic meter of air were Of eighteen mussels examined, six contained coliforms isolated, and 1.2 meters above the seat the con- (mean concentration of 1.2 x 106 per gram), and centration was 7 x 102 per cubic meter. About 10 twelve isolations of pathogenic serotypes of E. coliwere minutes after flushing there remained 70 bacteria per made. The authors noted that these shellfish are cubic meter widely distributed about the toilet room. A normally eaten partially cooked in Malaysia. tenfold reduction in the inoculum to the bowl reduced Although most attention in the developed countries the aerosol concentrations by about one-quarter. A has turned to the risks of contaminated shellfish second flush, 15 minutes later and without rein- transmitting excreted virus (especially hepatitis A oculation of bacteria, still produced 2.8 x 104 bacteria virus, rotavirus, and Norwalk agent), the risks of per cubic meter at seat level. Swabs taken from surfaces bacterial infections due to pathogenic E. coli, shigellae, throughout the room yielded Serratia. Adding sheets of salmonellae, and Vibrio cholerae being spread by toilet paper to the bowl before flushing did not affect shellfish harvested from polluted waters are very real aerosol production by the first flush, but increased (Hughes, Merson and Gangarosa 1977; Janssen 1974). aerosol production by the second flush by retaining a Considerable debate surrounds the use of quality greater number of organisms in the bowl during the standards for shellfish growing waters based on first flush. Even with the lid closed, the first flush permissible concentrations of fecal indicator bacteria produced 3.1 x 104 bacteria per cubic meter of air at (Cabelli 1978; Evison 1979; Metcalf 1978). The USA seat level. Aerosol production was unaffected by sets limits of 70 coliforms per 100 milliliters (median whether the seat was covered by its lid or by a value) and 14 fecal coliforms per 100 milliliters (median cardboard replica of the human buttocks. value) for waters used for shellfish production. It is Bound and Atkinson (1966) compared aerosol widely accepted, however, that these bacteriological production by wash-down and syphonic types of flush measures are poor indicators of the risk of viral toilets, each flushed by a low-level, 9-liter cistern. The contamination, and most countries have yet to legislate bowls were inoculated with a suspension of E. coli, and for shellfish water quality or to decide whether a air samples were taken 0.4 meters from the bowl at seat standardbasedonindicatorbacteriaaloneisadequate. level. Wash-down toilets produced on average 13 E. coli per cubic meter of air, whereas syphonic bowls In the air produced only 0.9 per cubic meter. Closing the lid before flushing did not affect aerosol production. Airborne droplets of water and wastewater may Newson (1972) studied hospital toilets in England. contain excreted bacteria, and these may cause He sampled water from the bowls of toilets in normal respiratory or enteric infection if inhaled in sufficient use and found no E. coli in 62 percent of samples (109 of numbers by a susceptible host. The mechanisms by 176); only 5 percent of samples (9 of 176) contained which aerosolized bacteria may be produced are more than 2.5 x 105 per 100 milliliters. The seats, lids, similar to those that generate viral aerosols (see flush handles, and door handles in the same toilets were chapter 9). Baylor, Peters and Baylor (1977) bubbled swabbed, and 6 percent of specimens (19 of 293) were air through a column of liquid containing E. coli and positive for E. coli. When 10l E. coli were added to a ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 219 bowl, an aerosol of up to 186 E. coli per cubic meter of (USA). The sewage contained 2 x 1010 coliforms per air was produced. The same proccdure also produced 100 milliliters. Within 5 meters of the source, the air at 70-80 visible droplet splashes, of which 39-75 the activated sludge plant contained 130-390 coliforms contained E. coli. More droplet splashes were per cubic meter, whereas at the trickling filter plant the produced by high-level cistern flushes and, surpris- air contained 21-79 coliforms per cubic meter. Wind ingly, syphonic bowls generated more splashes than speed and air temperature were significantly correlated wash-down bowls. The first flush reduced the with the concentration of airborne coliforms. concentration of inoculated E. coli in the bowl water Katzenelson, Teltch and Shuval (1977) isolated up to from 10' to 106 per 100 milliliters; the second flush 452 coliforms per cubic meter of air 30 meters took the concentration down to 1 O0 per 100 milliliters; downwind of an aerated lagoon in Israel. and the third flush left no E. coli detectable in bowl Goff and others (1973) isolated up to 965 coliforms water. per cubic meter of air 100 meters downwind from Gerba, Wallis and Melnick (1975b) seeded 1011 E. trickling filter plants in the USA. Coliform aerosol coli into a flush toilet bowl with a 14-liter cistern flush. detection increased at high relative humidities and low Total numbers of E. coli in the bowl water were reduced solar radiation. Cronholm (1980) detected aerosolized to 107 after one flush, 104 after two flushes, and enteric bacteria up to 930 meters downwind from small remained at around 104 for at least seven flushes. This activated sludge plants in Kentucky (USA). Foliage was because E. coli were adsorbed to the porcelain downwind of the plants was contaminated by 1-830 inner bowl surface and were gradually eluted by enteric bacteria per square millimeter of leaf surface. successive flushes. Public toilet bowls in normal use Six mice forced to inhale air at a sewage treatment were sampled and found to contain between 102_108 plant and observed for 2 weeks exhibited no symptoms, coliforms per total bowl volume. One flush ejected and cultures of their respiratory organs were negative 27-104 visible droplets, and up to 6.6 x 104 E. coli, for enteric bacteria. when 1011 organisms were seeded into the bowl. A Fedorak and Westlake (1980) sampled total reduction of 5 log units in the number of E. coli in the airborne bacteria at an activated sludge plant at bowl reduced the number ejected by a flush by under 3 Edmonton (Canada) and found up to 1.8 x 103 per log units. The numbers of E. coli ejected were not cubic meter of air, compared to a background level of appreciably affected by whether the bowl contained 27 per cubic meter. Similar bacterial concentrations similar original numbers in culture, homogenized (up to 2.6 x 103 per cubic meter) were found indoors stool, or fecal pellets. An estimated 800-1000 bacteria near taps used to sample sewage and sludge from the fell out on bathroom surfaces after a flush (1011 treatment plant. Increased airborne bacterial con- seeded E. coli in the bowl), and 75-80 percent of these centrations occurred in the laboratory when sludge fell out in the first 2 hours after the flush. Coliforms was being dispensed for analysis and when the floor were detected on surfaces of all of twenty private and was being mopped. public toilets in normal use. Walls, floors, toilet seats, Randall and Ledbetter (1966) studied the aerosols and bowl rims were the most contaminated surfaces. produced by an activated sludge plant in Texas (USA). Sewage treatment plants, especially those that The opportunistic respiratory pathogens Klebsiella, involve the pumping of air or oxygen into sewage or the Aerobacter, and Proteus constituted II percent of all mechanical aeration of a sewage tank, produce aerosol isolates, 19 percent of isolates of enteric origin, and 56 droplets that contain excreted bacteria as well as percent of Enterobacteriaceae. The Klebsiella- excreted viruses (see chapter 9). Bitton and Smith- Aerobacter group survived for longer in the air than Holmes (1978) sampled air above the aeration tank of a other enteric bacteria and made up an increasingly high package sewage treatment plant, above an activated proportion of isolates further from the activated sludge sludge plant, and on the roof of a building in Florida tanks. The authors suggested that Klebsiella should be (USA). In a cubic meter of air above the package plant used as an indicator of bacterial air pollution from there were 154 coliforms, 22 fecal coliforms, and 2 fecal sewage treatment plants. streptococci; above the activated sludge plant there Crawford and Jones (1978) studied the emissions of were 165 coliforms, 27 fecal coliforms, and 5 fecal airborne bacteria from aerated grit removal tanks at a streptococci; and on the roof there were 16 coliforms, 2 sewage treatment plant in Toronto (Canada). The rate fecal coliforms, and 1 fecal streptococcus. of bacterial emission from the tanks was strongly Fannin and others (1977) investigated airborne inversely correlated to relative humidity but not to air coliform bacteria near an activated sludge and a temperature, pressure, or sewage flow rate. The rate of trickling filter sewage treatment plant in Michigan decay of downwind airborne bacterial concentrations 220 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA was correlated only to wind speed. When the decay irrigation sites utilizing sewage effluents (Katzenelson rates of various indicator bacteria were compared it and Teltch 1976; Katzenelson, Teltch and Shuval was found that fecal coliforms decayed faster than total 1977; Teltch and Katzenelson 1978). Coliform bacteria coliforms, which decayed considerably faster than fecal were found in the air up to 350 meters downwind from streptococci. By the use of a mathematical model, the the irrigation site. The concentration of bacteria in the authors predict a maximum downwind travel distance air was directly related to the concentration in the of 505 meters for fecal coliforms and 757 meters for Str. effluent, and coliforms could only be detected in the air faecalis. when their concentration in effluent exceeded 105 per The source of excreted bacterial aerosols that is 100 milliliters. Coliforms survived for longer in receiving the most scientific attention at present is the aerosols when relative humidity was high, when solar spray irrigation of sewage effluents. Sorber and others radiation was low, and when the effluent contained a (1976) investigated airborne bacteria produced by the higher concentration of organic matter. Up to 10 times spray irrigation of secondary sewage effluent at a golf more aerosolized bacteria were detected at night than course in Arizona (USA). The effluent contained a during the day. Earlier studies in Israel (Katzenelson, mean of 3.7 x 105 coliforms and 170 fecal streptococci Buium and Shuval 1976) had suggested that residents per 100 milliliters, and the average background level of on kibbutzim that practised spray irrigation with coliforms in the air was 2.4 per cubic meter. At 47 sewage effluent experienced a higher incidence of some meters downwind of the sprinklers up to 330 coliforms bacterial excreted infections (shigellosis, salmonellosis, per cubic meter were recovered, and at 152 meters only and typhoid) than members of kibbutzim that 30 coliforms per cubic meter were found. Coliform practiced no form of wastewater irrigation. These levels significantly higher than the background were findings have been doubted and appear to be detected up to 198 meters downwind. The aero- contradicted by subsequent work (Feliciano 1979). solization efficiency (the proportion of effluent that Airborne excreted bacteria can be produced by was divided into droplets sufficiently small to remain many situations other than toilet flushing, sewage airborne) was estimated as 0.32 percent. The decay rate treatment, or spray irrigation. Edmonds and Littke of airborne bacterial concentrations was markedly (1978) sampled airborne coliforms 80 millimeters reduced at night. In subsequent experiments at the above anaerobically digested, dewatered (20-40 same site, effluent contained 2.8 x 105 coliforms, percent solids) sludge applied to land. Coliforms in the 2.3 x 104 fecal coliforms, and 1.3 x 103 fecal streptoc- sludge over a 7-month sampling period were between occi per 100 milliliters (Bausum, Schaub and Kenyon 5 x 10i and 3.5 x 10' per gram, while coliforms in the 1978). The concentrations of aerobic bacteria-bearing air ranged from 0 to 1.5 x 104 per cubic meter. particles per cubic meter of air, downwind of the Maximum coliform emission was associated with no sprinklers, were up to 10,500 at 46 meters, up to 4,700 rainfall and high air temperature, wind speed, and solar at 76 meters, up to 3,200 at 100 meters, up to 500 at 150 radiation. Adams and others (1980) have reported on meters, and up to 13 at 560 meters. (All these bacterial aerosol emissions from cooling towers using concentrations are expressed as values in excess of the disinfected sewage effluents or polluted river water. background levels of 15-198 colony-forming particles The risks to health associated with inhaling per cubic meter.) When the effluent was heavily aerosolized bacteria depend on factors such as the dose chlorinated prior to spraying, colony-forming particles inhaled, the dose required to cause an infection, and the fell to between 0 and 57 per cubic meter at 46 meters aerosol size. Katzenelson, Teltch and Shuval (1977) downwind. The proportion of Enterobacteriaceae in estimated that an individual working 100 meters from the total aerobic bacterial flora was 2 percent in the an effluent sprinkler in Israel would inhale about 36 effluent but 26 percent in the aerosol isolates. coliforms every 10 minutes. Considering the very high Parker and others (1977) investigated a spray ratio of coliforms to pathogens, this rate of inhalation irrigation system that utilized effluent from a potato- appears low. Infective doses for some pathogens may processing plant. The sprayed effluent contained be lower, however, by the respiratory route than by the 1.6 x 106 coliforms per 100 milliliters. At 15 meters alimentary route. Crozier and Woodward (1962) downwind there were up to 1,100 coliform-bearing reported that typhoid fever was established in particles per cubic meter, and at 1-1.5 kilometers chimpanzees by the respiratory route with doses of S. downwind there were up to 30 coliform-bearing typhi a thousandfold less than those needed for particles per cubic meter. infection by oral challenge. A series of experiments were conducted in Israel to The infective dose of inhaled bacteria depends in investigate the production of airborne bacteria at spray part upon the ability of the aerosols to penetrate deep ESCHERICHIIA COLI AND OTHER BACTERIAL INDICATORS 221 into the lungs. Lung penetration is especially operators) have higher infection or disease rates than important in the establishment of respiratory in- others (Feliciano 1979). It may be that, in most fections. Aerosols that penetrate best are those which situations, the inhalation of excreted bacteria is are less than 5 or 6 micrometers in diameter (Druett, insignificant compared with the ingestion of the same Henderson and Peacock 1956; Druett and others pathogens and that the numbers of bacteria inhaled are 1953; Harper and Morton 1953; May and Druett usually well below the required infective doses. 1953). Reported aerosol sizes from sewage sources vary considerably but, in general, smaller aerosols pre- dominate as distance from the source increases because Inactivation by Sewage Treatment larger particles have settled. Although only small Processes aerosols are likely to penetrate to the lower respiratory tract, it is probable that bacteria (and viruses) in larger The fate of bacterial indicators of pollution in aerosols caught in the upper respiratory tract may sewage treatment processes has been the subject of a subsequently be swallowed. number of studies over the past 50 years. The literature Baylor, Peters and Baylor (1977) found a significant is not, however, as extensive as might be expected, negative correlation between droplet size and the partly because it is only very recently that the concentration of E. coli within a droplet. Droplets importance of E. coli as an enteric pathogen has been produced by surf and blown into the beach had a mean recognized and partly because the traditional focus of size of 35 micrometers at the water's edge and 21 attention has been the ability of sewage treatment micrometers 10 meters up the beach (Baylor and others processes to improve the physicochemical quality, 1977). Sorber and others (1976) found that 50 percent rather than the microbiological quality, of sewage. of airbome bacteria at a spray irrigation site were Indeed, interest in the performance of sewage associated with particles in the range of 1-5 treatment plants in removing enteric bacteria has been micrometers. Darlow and Bale (1959) found that a so low that many engineers are unaware of the poor toilet flush produced aerosols with a mean diameter of bacterial quality of secondary effluents from con- 2.3 micrometers, 87 percent of them being less than 4 ventional treatment plants. micrometers. Goff and others (1973) recorded that the The interest in enteric bacteria in sewage treatment majority of aerosols emitted by trickling filter plants processes is now increasing for two reasons. First, more were less than 5 micrometers in diameter. Randall and stringent effluent quality legislation is being in- Ledbetter (1966) found that 40 percent of viable troduced in the developed countries, and this has airborne bacteria in the immediate vicinity of activated promoted research into disinfection and tertiary sludge units were associated with particles of less than 5 treatment as methods for improving the quality of micrometers in diameter, but that this proportion rose unsatisfactory secondary discharges. Second, there is to 70 percent at a downwind distance of 6 meters. growing awareness in developing countries of the Teltch and Katzenelson (1978) found that the median dangers of discharging highly pathogenic secondary aerosol size produced by effluent sprinklers in Israel effluents into streams that downstream communities was greater than 7 micrometers but that 50 percent of may use for domestic purposes. bacteria sampled were associated with aerosols of less than 7 micrometers in diameter. The studies reported above, and the laboratory By primary and secondary sedimenration investigations of Poon (1968), clearly show that, Primary sedimentation tanks, with retention times although bacterial aerosol production may be of 2-6 hours, produce quite variable results in removal increased by low relative humidity, high temperature, of indicator bacteria (see the appendixes to Feachem high solar radiation, and high wind speed, these same and others 1980). Usually a reduction of fecal coliforms conditions also promote rapid death and dispersion of and fecal streptococci is reported in the range 0-60 bacteria in the air. Thus the dissemination of percent. For instance, at two sewage treatment plants aerosolized bacteria from treatment plants and spray in Scotland, primary sedimentaton removed on irrigation sites in hot arid climates should be average 32 and 50 percent of E. coli and 57 and 53 appreciably less than that reported from temperate percent of Pseudomonas aeruginosa (Wheater and climates. In addition there is no convincing epidem- others 1980). Removal is primarily caused by iological evidence that those exceptionally exposed settlement of bacteria, which are adsorbed to, or to sources of bacterial aerosols (for instance, workers in entrapped within, solid particles in the influent sewage. fields receiving sprayed effluent or sewage plant The data on bacterial dieoff in sewage reported above 222 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA suggest that only a very small reduction ( < 10 percent) three-compartment septic tank used in Kiangsu would be expected due to natural death in the short Province, China (see also figure 6-1 in Part One). The period during which the sewage resides in the first two compartments have retention times of 10 days sedimentation tank. Growth of indicator bacteria, each, and the third has a retention time of 30 days. especially of total coliforms, is sometimes recorded in Tests on these tanks showed that, in winter at sedimentation tanks. temperatures of 3-7°C, E. coli reductions of 4 log units were achieved (suggesting a tgo of 300 hours). The data (see the appendixes of Feachem and others By storage 1980) suggest that in a well-designed and well- Storage will be an especially effective method of maintained septic tank with 3 days' retention in a warm reducing enteric bacteria in sewage at warm tropical climate (>25°C), a reduction of fecal indicator and subtropical temperatures (say, > 25°C). Although bacteria of 50-95 percent may be achieved. In poorly little specific information is available, it may be designed and poorly maintained tanks (the most usual anticipated that fecal bacteria in warm sewage would kind), little or no reduction can be expected. It must be have a tgo of 120 hours or less. stressed, however, that the distinction between a 90 percent removal (say, influent = 10' per 100 milliliters; By septic tanks effluent = 105 per 100 milliliters) and a 10 percent removal (say, influent= 106 per 100 milliliters; The removal of fecal indicator bacteria by septic effluent = 9 x 105 per 100 milliliters) is trivial. In tanks has attracted increased interest recently because either case the effluent is heavily contaminated with of concern about the pollution of groundwater by enteric bacteria, and the ultimate fate of these bacteria septic tank effluents. A septic tank is simply a settling depends on the method of disposal of the effluent and chamber, or chambers, usually having retention time of the sludge. 3 days or less. In poorly designed tanks, or those Effluents are normally discharged to soakaway pits requiring desludging, there is very considerable solids or drainfields where bacteria may be retained in the soil carryover into the effluent. Enteric bacteria are and eventually die. Under certain conditions, however, removed both by death in the anaerobic liquor and by fecal bacteria may travel from the drainfield to pollute association with solids that settle to the sludge layer. shallow groundwater aquifers or nearby wells. The short retention times, and poor sedimentation Kudryavtseva (1972) recorded that coliforms in- performance that is often the result of insufficiently oculated into saturated alluvial sands (percolation rate frequent desludging, are the reasons why high 13 meters per day) in the USSR traveled for a concentrations of fecal indicator bacteria are found in horizontal distance of not more than 3 meters in the septic tank effluents. direction of groundwater flow. However, the same Viraraghavan (1978) reported that a septic tank in author cited other data from the USSR indicating a Canada produced an effluent containing geometric horizontal travel of indicator bacteria of 850 meters mean values of 2.3 x 106 coliforms, 1.6 x 105 fecal through pebble deposits and 1 kilometer through coliforms, and 1.1 x 105 fecal streptococci per 100 weathered limestone. milliliters. Brandes (1978a) reported that approx- Several studies have shown that the travel of imately 2.5 million residents of Ontario (Canada) use bacterial indicators through soil from pit latrines or septic tank systems. He studied three septic tanks with septic tank drainfields decreases over time as the soil retention times of 2-10 days and recorded the following becomes increasingly clogged with fecal solids and ranges of concentrations of fecal coliforms per 100 biological slime. Caldwell and Parr (1937) found that, milliliters: 4 x 105-2 x 106 in first compartment after two months of operation, fecal coliforms and supernatant, 1 x 105-1 x 106 in second compartment Clostridium perfringens could be recovered at 8 meters, supernatant, 9 x 105_8 x 106 in first compartment and occasionally at 11 meters, from a bored hole sludge, 6 x 104-6 x 105 in second compartment latrine. After 7 months, however, bacterial travel was sludge, and 5 x 105-4 x 106 in the effluents (see also less than 1.5 meters. McCoy and Ziebell (1976) applied Brandes 1978b). McCoy and Ziebell (1976) sampled septic tank effluent (5.1 x 106 fecal coliforms and effluents from five septic tanks in the USA with 7.3 x 106 fecal streptococci per 100 milliliters) to 0.6 retention times of 2-13 days and found geometric meter deep columns of loamy sand at 25°C. At an mean values of 4.2 x 105 fecal coliforms and 3.8 x 103 application rate of 0.1 cubic meters per square meter fecal streptococci per 100 milliliters. per day, 92 percent of fecal coliforms were removed McGarry and Stainforth (1978) have described a over the first 100 days of application. After this time a ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 223 clogging zone developed at the top of the column, and in the saturated soils throughout a 32-day sampling removal of fecal coliforms improved to 99.999 percent. period. Reneau and others (1977) recorded the travel of Fecal streptococci removal rates were around 3 log fecal coliforms for a horizontal distance of at least 28 units during the first period and over 6 log units after meters from a septic tank drainfield through saturated 100 days. In field experiments it was found that an sandy loam in Virginia (USA). At one site, fecal effluent contained 1.9 x 106 fecal coliforms per 100 coliform concentrations were up to 4.6 x 104 per 100 milliliters; the soil in the clogging zone at the base of milliliters adjacent to a drainfield but were never more the drainfield trench contained 4 x 106 per 100 grams; than 430 per 100 milliliters at a distance of 28 meters and the soil 0.3 meters below the clogging zone (see also Reneau and Pettry 1975). Further important contained less than 200 fecal coliforms per 100 grams. work on bacterial movement through saturated soil The authors noted, however, that these are optimal was reported by McCoy and Hagedorn (1979) and removals under ideal conditions in nonaggregated Rahe, Hagedorn and McCoy (1979). soils. Other literature on the retention and survival of Brown and others (1979) studied the movement of bacteria in soil is reviewed above in the sections on septic tank effluent containing 106 fecal coliforms per groundwater and soil and below in the sections on 100 milliliters through a sandy loam, a sandy clay, and filtration and land treatment. A detailed review of the a clay, with percolation rates of 6, 0.9, and 0.06 meters fate of enteric bacteria in septic tank and drainfield per day, respectively. Fecal coliform concentrations systems has been published (Small Scale Waste decreased greatly with increasing distance from the Management Project 1978). septic line, and a 90-99 percent reduction in 50 Septic tank sludge is rich in excreted bacteria millimeters was common. In most tests fecal coliforms (Brandes 1978a, 1978b) and requires treatment by were not present more than 0.3 meters below the septic digestion, drying, or composting prior to application line, and only very occasionally were they detected in to agricultural land. The destruction of fecal indicator leachate drawn from 1.2 meters below the septic line. bacteria in tanks, in drainfields, and in sludges will be The tendency for nearly all fecal coliforms to be more rapid at warmer temperatures; therefore, given concentrated at the interface between the gravel packing correct design and good maintenance, performance in around the septic line and the soil was especially developing countries may often be better than that marked in soils of low permeability and increased with reported from temperate areas. time of effluent application for all soils. Fecal coliform concentrations in the soil decreased by about 99 . . percent in 2 weeks following the termination of effluent By trickling fIters application. Little information is available on the performance of Studies on septic tank drainfields have clearly shown trickling filters as a unit process. Most studies report that the risks of groundwater pollution are very much the removal of fecal indicator bacteria across a greater if the drainfield is located in, or only a little complete trickling filter plant (pretreatment-primary above, the saturated zone. Viraraghavan (1978) sedimentation-trickling filters-secondary sediment- studied the movement of indicator bacteria horizon- ation). tally through sandy clay and clay (percolation rates Literature on fecal indicator bacteria removal in 0.02-1.0 meters per day) from a septic tile discharging trickling filters is listed in the appendixes of Feachem effluent containing about 105 fecal coliforms and fecal and others (1980). In a well-operated plant the trickling streptococci per 100 milliliters. The septic line was 0.6 filter itself may remove 20-80 percent of influent meters below ground level, and the water table was enteric bacteria, whereas the total treatment plant will only 0.15 meters or less below the line. Fifteen meters remove 70-97 percent. Poor maintenance or overload- downslope from the septic line the groundwater ing will result in considerably lower removal rates. contained about 102 fecal coliforms and 102_103 fecal Fecal coliform and fecal streptococci removal rates are streptococci per 100 milliliters. generally similar. Hagedorn, Hansen and Simonson (1978) seeded In Britain it is common for the removal of fecal antibiotic-resistant E. coli and Str. faecalis into two coliforms across complete trickling filter plants to be pits, 0.3 and 0.6 meters deep, dug into saturated silty 90-95 percent. This poor removal performance results loam and clay loam (percolation rates 0.01-0.2 meters in an effluent containing 104-107 fecal coliforms per per day) in Oregon (USA). The bacteria were detected 100 milliliters. Wheater and others (1980) recorded in wells 15 meters from the pits within 8-16 days of that two trickling filter plants in Scotland achieved inoculation, and they survived in appreciable numbers average overall E. coli reductions of 87 and 90 percent 224 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA and produced effluents containing up to 6.9 x 106 and By waste stabilization ponds 1.4 x 106 E. co/i per 100 milliliters. The removal of E. coli and other fecal indicator By activated sludge bacteria in waste stabilization ponds has been studied The removal of fecal indicator bacteria by activated by many investigators throughout the world during the last 30 years (see the appendixes of Feachem and others sldewhat pessesthan isypor,calthoughl. remo i 1980). It is now well established that ponds, if properly somewhat better than by trickling filters. The mean dsge,cnaheesbtnilyhge eoa retention time in the aeration tanks (6-12 hours) is designed, can achieve substantially higher removal such that only a less than 50 percent reduction by rates of fecal bacteria (and indeed of other excreted natural die-off would be expected, even at warm pathogens) than other forms of sewage treatment. For temperatures and assuming that all the liquor were example, Mara and Silva (1979) report the reduction of held for the mean retention time. Most reduction of fecal coliform bacteria in a series of five ponds in indicator bacteria is in practice achievenortheast Brazil, with a total retention time of 29 days indicator bacteria IS in practice achieved by adsorption 1 0 , and an average temperature of 26°C, from 5 x 107 per to flocs, which are subsequently removed in secondary ada vrg eprtr f2',fo e todflcs,awich tar s entlby rem oveding secondar 100 milliliters in raw sewage to 17 per 100 milliliters in sdmtozoatioan tanks,ift and bthegr ofclae the final effluent; this represents a very high overall protozoa (Van der Drift and others 1977). rdcino 9996pret Studies on removal of fecal indicator bacteria by reduction of 99.99996 percent. activated sludge are listed in the appendixes of MECHANISMS OF E. COLI REMOVAL IN PONDS. There Feachem and others (1980). Reductions ofinfluent fecal is a variety of environmental factors that are bacteria are between 0 and 99.9 percent, with some considered to be responsible, or at least partially so, for experimenters reporting increasing numbers during the removal of E. coli and other fecal indicator bacteria aeration. Most experience suggests that reductions will in ponds. These factors include time and temperature, be 80-99 percent across a complete activated sludge ultraviolet radiation, the antibacterial effect of plant that is well-operated and well-maintained but extracellular algal toxins, low concentrations of that does not include effluent disinfection or tertiary dissolved carbon dioxide, high pH, high (especially treatment. Overloaded or poorly maintained plants supersaturated) concentrations of dissolved oxygen, will achieve very much lower removal rates. These low and predation by the microinvertebrate fauna. These levels of removal (always less than 2 log units) factors are reviewed briefly below, but it should be mean that activated sludge plant secondary emphasized that their relative importance, apart from effluents contain high concentrations of enteric perhaps that of time and temperature, is largely bacteria. Berg and Metcalf (1978) reported unknown. 1.1 x 105-4.9 x 106 fecal coliforms per 100 milliliters Compared with other forms of sewage treatment, of activated sludge effluent. The settled sludge from the ponds are characterized by long mean hydraulic secondary sedimentation tanks will also contain a high retention times, ranging from a few weeks in hot concentration of fccal indicator bacteria that have climates to several months in cold climates. Thus, adsorbed to flocs in the aeration tanks. ponds provide a considerably greater opportunity for fecal bacterial removal than other treatment processes. BY oxidation ditch It is now well established (Mara 1976), both Practically no information has been published on theoretically and from field observation, that removal removal of fecal indicator bacteria by oxidation of fecal bacteria is greater in a series of ponds than in a ditches, although a certain amount is known about single pond providing the same overall hydraulic removal of Salmonella (see chapter 15). The process is retention time, and that this efficiency increases with essentially similar to that of activated sludge, but the the number of ponds in the series. The microbial flora longer hydraulic retention times (1-3 days), and the and fauna vary considerably from pond to pond in a higher proportion of sludge recycling giving a solids series ofponds, and it is therefore likely that the relative retention time of 10-30 days, are features that should effect on fecal bacterial removal of the environmental produce improved bacterial removal. Laboratory factors discussed below changes in a similar manner. studies in the USSR indicated that coliforms declined Moeller and Calkins (1980) investigated the effect of by 6 log units after 3 days in an oxidation ditch, and the ultraviolet component of solar radiation (wave- that an EPEC strain (0111) survived for 3-7 days when length range: 280-320 nanometers) on the removal of seeded at a concentration of I05 per 100 milliliters and fecal coliforms in a series of four maturation ponds for 15-18 days when seeded at 107 per 100 milliliters treating the effluent from a conventional activated (Goncharuk and others 1970). sludge plant in Kentucky (USA). The overall hydraulic ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 225 retention time in the pond series was 5-7 days, and the due merely to the anaerobic pond functioning as an pond temperatures varied from below 10°C to above additionalunitintheseries,orwhethersolidsremovalin 25°C. No relationship between fecal coliform removal anaerobic ponds permits an enhanced efficiency of and either temperature or algal density was found, but whatever factors are responsible for fecal bacterial a significant correlation between fecal coliform removal in facultative ponds. The results obtained by removal and the received dosage of ultraviolet Mara and Silva (1979) in northeast Brazil suggest, radiation was apparent, with the bacterial removal rate however, that the latter explanation is not valid under being directly proportional to the dose received. all climatic conditions. Several investigators have studied the direct and Loedolff (1965) examined the removal of E. coli indirect effects of pond algae on the removal of fecal through predation by microinvertebrates in experi- bacteria. Many common pond microalgae produce mental ponds in Pretoria (South Africa). Cladocera antibacterial substances that have been shown to be were found to be the numerically greatest group of inhibitory to E. coli (Davis and Gloyna 1972), although microinvertebrates, with Moina dubia and Daphnia in vitro toxicity tests have shown that the degree of magna, respectively, predominating in facultative and inhibition effected by different algae not only varies maturation ponds. In vitro studies showed that M. from alga to alga, but that there appears to be a marked dubia remove 93 cells of E. coli per individual per hour synergistic effect when two or more algae are present, and D. magna 55, the difference being ascribed to the with the synergism increasing with the number of algal difference in coarseness of the filtering setae of the two species present. Moreover, removal of fecal bacteria in species. At these rates of predation it was concluded samples of pond water is higher than in laboratory that Cladocera do not contribute significantly to mixtures of large numbers of different algal species bacterial removal in ponds because, in practice, their (Jackson 1979). numbers never rise to the level required for them to Algal demand for carbon dioxide is often greater have a major effect on bacterial numbers. than its supply as an end-product of pond bacterial metabolism, with the result that bicarbonate ions KINETICS OF E. COLI REMOVAL IN PONDS. Removal reverse to carbon dioxide and hydroxyl ions, leaving an kinetics have been studied in detail by only a few excess of the latter that raises the pH of the pond. High investigators. The most favored approach (for ex- pH values (above 9.5) are known to be detrimental to ample, Marais 1974) is the assumption that removal of the survival of E. coli in ponds (Parhad and Rao 1974), fecal bacteria follows first-order kinetics and that the although Gray (1975) suggests that, since carbon pond is a completely mixed reactor.3 Although this dioxide is an essential growth factor for E. coli, its assumption undoubtedly represents a gross unavailability to E. coli as a result of its rapid utilization by photosynthesizing algae is an important factor in determining the removal of E. coli in natural 3. The resulting kinetic equation is thus: environments. .vN, - ,/1 + K,t*), The concentration of dissolved oxygen in ponds is where N, and N- are the numbers of a fecal indicator bacterium (or controlled by the pond algae. In facultative ponds there is bacterial pathogen) per 100 milliliters of pond effluent and influent, a diurnal variation in dissolved oxygen concentration at respectively; K, is the first-order rate constant for the removal of the any depth above the oxypause and also in the position bacterium in reciprocal days; and t* is the mean hydraulic retention of the oxypause itself. The survival of E. coli is enhanced time in the pond in days ( = the pond volume in cubic meters divided by the influent flow rate in cubic meters per day). A formal derivation under anaerobic conditions (Klock 197 1; Marais 1974). of the equation is given, for example, by Mara (1976). A more In thermally stratified facultative ponds in northeast rigorous approach to pond kinetics would be to use the Wehner and Brazil, E. coli forms a reasonably stable layer some Wilhelm (1956) equation for first-order removal in dispersed flow 10-20 centimeters below the oxygen-supersaturated reactors; such an approach is not normally possible, however, as algal zone, presumably to provide protection against pond dispersion numbers are usually unknown. For a fuller , . ' , . . ~~~~~~~~~~~discussion of this point, see Mara (1976). the detrimental effect of very high dissolved oxygen dsuso fti on,seMr 17) The value of Kb is strongly temperature dependent and is usually concentrations (Pearson and Mara, unpublished data). described by an Arrhenius equation of the form: However, Davis and Gloyna (1972) have shown that in K2OT-20 Texas (USA) pretreatment in anaerobic ponds is KS(T,= b(20) advantageous in that the overall removal in a series of where Ks,rT is the value of Kb at T'C, Kb(20) its value at 20'C, and 0 the dimensionless Arrhenius constant. Marais (1974), using the ponds which includes an anaerobic pond is greater than results reported by Slanetz and others (1970), calculatedvalues of 2.6 in one which does not. From the details given by these reciprocal days and 1.19 for Kb(20, and 0, respectively, for facultative authors it is not possible to determine whether this is and maturation ponds in the temperature range 5-20'C. 226 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA simplification of the environmental factors involved in ponds located in Australia, Brazil, and South Africa.' fecal bacterial removal in ponds and also of the These series of ponds were selected because they are hydraulic regime therein, it is nonetheless empirically representative of well-operated ponds, with sufficient justified and in the past has served as a reasonable basis information given about their performance to permit for design (Marais 1974; Mara 1976). However, a more the kinetic constants to be calculated. It is apparent recent and more rigorous analysis of removal of fecal from table 13-3 that there is considerable variation in bacteria in ponds is given by Dissanayake (1980), who the values of the kinetic constants for each bacterial studied the removal of fecal coliforms in laboratory- group-even for ponds in the same series at the same scale, pilot-scale, and full-scale ponds in Bangkok temperature-and that little can be concluded about (Thailand). He found that the first-order rate constant the relative removal rates of the different groups. for fecal coliform removal (Kb, in reciprocal days) was Insufficient data were reported for this series of ponds best described by the following multiple linear to permit the validity ofDissanayake's (1980) model to regression equation: be ascertained. exp(Kb) = 0.7716(1.0281 )T(1 .0016)c- (0.9990)', At present it appears, therefore, that design exp(K) =engineers have no alternative but to follow the design where T is the temperature in degrees Celsius, C, the procedure based on the work of Marais (1974) and average concentration of algae in the pond in Mara (1976) fortheremoval offecal bacteria in a series milligrams per liter,4 and A the organic loading on the of ponds, even though its only environmental pond in kilograms of chemical oxygen demand per parameter is temperature. It is clear, however, that in hectare per day. The intensity of ultraviolet radiation the future pond design will have to include the effect of was shown to be an unimportant factor in influencing other variables such as algal biomass and organic the value of Kb, and no account was taken of predation loading. The pioneering approach shown by by microinvertebrates (which, as noted above, is Dissanayake (1980) requires that it be followed by insignificant). When used with the Wehner and further work to determine its validity as a design tool. Wilhelm (1956) model for first-order removal of fecal coliforms in dispersed flow reactors, this equation was By aerated lagoons found to be very satisfactory in predicting fecal coliform removal in full-scale ponds. Dissanayake The survival of fecal indicator bacteria in aerated (1980) also gives regression equations for predicting lagoons has scarcely been studied. Menon and Bedford the value of Cs, so that his model for fecal coliform (1973) reported that coliform and fecal coliform removal can be used by design engineers. Application removal rates were 38 and 63 percent, respectively, in of Dissanayake's model has of course been limited an aerated lagoon treating wood pulp processing because of its recentness, and further work is required effluents at Fort Frances (Canada). The study was to determine the global applicability of its regression conducted during summer when the lagoon tempera- constants. Nonetheless, the model at least gives some ture was 28°C, but other process details were not given. idea of the relative importance of the principal There was evidence of coliform and fecal coliform environmental factors involved in removal of fecal growth on some occasions in the aerated lagoon, and bacteria in ponds. laboratory studies showed that in sterilized aerated Much of the large volume of literature in removal of lagoon liquor total coliforms multiplied at 15°C and fecal bacteria in ponds does not contain all the 28°C, that fecal coliforms multiplied at 28°C but not at information required for a kinetic analysis ofthe results 15°C, and that fecal streptococci died at both given therein; for example, many publications do not temperatures. This particular study was not well contain details of the retention time, and almost none designed or reported, and it may be that the results are gives information on the dispersion number or algal not typical. From a theoretical standpoint, an aerated biomass of the ponds studied. The complexity of the lagoon (retention time 2-6 days) may be expected to removal offecal bacteria in ponds is shown in table 13- have bacteria removal properties similar to, or a little 3, which presents values of the first-order rate constant better than, an oxidation ditch. If the effluent is treated for the removal ofvarious fecal bacteria in four series of 5. Since the dispersion numbers for these ponds were not given in the literature cited, it is only possible to analyze the results therein on 4. Rather than using algal dry weight in milligrams per liter, it is the assumption of either complete mixing or plug flow. For the preferable to express algal biomass concentrations in ponds in terms purpose of table 13-3. the former was used, although the latter would of photosynthetic pigment; for example, micrograms of chlorophyll have served the argument equally well. The kinetic equation for a a per liter. completely mixed pond is given in footnote 3, above. Table 13-3. Fecal bacteria removal rate constants in series of waste stabilization ponds First-order rate consttzt (reciprocal dav's, base e) jor removal of: Retention -- - Temperoature Pond time Fecal Fecal Clostridium Pseudomonas CoUn1tr'y re erence (0C) number (days) olhuim-111 streptococci perfringens Salmonellae aeruginosa Australia (Parker 1962)' 21 1 3.8 0.13 0.21 2 8.0 1.13 1.30 3 13.0 0.07 0.13 4 18.0 0.12 0.61 5 23.0 1.11 0 6 28.5 0.55 0.91 7 33.5 0.38 0.99 8 38.5 0.19 0.23 Australia (Parker 1962)' 9 1 4.1 0.11 0.16 2 8.6 0.44 0.21 z 3 14.0 0.23 0.17 4 19.2 0.28 0.04 H 5 24.6 0.14 1.01 6 30.5 0.28 3.17 Brazil (Mara and 26 1 6.75 2.17 3.69 Silva 1979)b 2 5.46 2.26 2.17 3 5.46 2.40 2.38 4 5.46 15.00 5.79 5 5.79 1.91 0.12 South Africa (Coetzee ND 1 20.0 1.96 2.44 0.55 4.19 and Fourie 1965)' 2 15.0 8.47 1.40 1.27 0.26 0 South Africa (Caetzee ND 1 2.5 1.71 0.17 3.73 and Fourie 1965)d 2 2.5 0.43 0.19 0.24 3 2.5 0.35 0.62 2.36 4 2.5 1.11 0.15 3.60 ND No data. a. Data for full-scale ponds receiving raw sewage (anaerobic, facultative and six or four maturation ponds). b. Data for pilot-scale ponds receiving raw sewage (anaerobic, facultative and three maturation ponds). c. Data for full-scale ponds receiving raw sewage (facultative and maturation ponds). d. Data for full-scale ponds receiving humus tank effluent (four maturation ponds). 228 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA in maturation ponds, removal as in waste stabilization effluent (pH 9.6) held in an aerated pond for a mean ponds is anticipated. The sludge drawn off from period of 10 hours in Pretoria (South Africa). secondary sedimentation tanks or settling ponds will be rich in excreted bacteria. COAGULATION. Coagulation or flocculation of a secondary effluent, followed by solids removal in Bi, tertiary treatmnent sedimentation or flotation chambers, will remove those bacteria which are bound up within, or adsorbed to, The growing environmental concern in developed the flocs. This bacterial removal mechanism is countries in recent years, coupled with some awareness analogous to that of activated sludge, although the that the effluents from conventional secondary retention times in the sedimentation tanks are processes (trickling filter and activated sludge) are considerably shorter and poor removal percentages heavily contaminated with excreted viruses and may be expected. Coagulation is commonly promoted bacteria, has led to an increasing use of tertiary by the addition of alum [A12(SO4)33, iron salts (for treatment. This section discusses the effect on fecal example, FeCl3), or polyelectrolytes. indicator bacteria of some of the tertiary processes that High removal rates can be achieved by lime are being used to upgrade the chemical or micro- treatment followed by sedimentation. The lime biological quality of secondary effluents prior to treatment raises the pH to a level that is extremely discharge or agricultural reuse. hostile to many bacteria and viruses, although some This section does not consider the advanced Gram-positive bacteria (for example, fecal strepto- wastewater reclamation plants designed to transform cocci) and spore-forming bacteria (for example, sewage into drinking water. Such plants incorporate a Clostridium spp.) are comparatively resistant to high complex combination of biological, physicochemical, pH. Grabow, Middendorff and Basson (1978) studied and disinfection processes and can eliminate excreted the effect of lime treatment, plus sedimentation with bacteria completely. Grabow and Isaacson (1978) added FeCl3 (1.5-2.5 milligrams per liter as Fe) and reported that the water produced by the sewage polyelectrolyte (0.5 milligrams per liter), on enteric reclamation plants in Windhoek (Namibia) and bacteria in activated sludge effluent. With a final pH of Pretoria (South Africa) contained no fecal coliforms in 9.6, 62 percent of coliforms and 68 percent of 94 percent of samples, no fecal streptococci in 100 enterococci were removed. When the lime dose was percent of samples, no Pseudomonas aerugintosa in 96 raised to give a final pH of 11.1, the removals were percent of samples, no Staphylococcus aureus in 91 99.98 and 97 percent, respectively, for coliforms and percent of samples, and no Clostridiuin perfringens in enterococci. 92 percent of samples. The Windhoek and Pretoria plants receive secondary effluents and treat them by FILTRATION. The data on bacterial retention and lime treatment, primary coagulation and sedimen- death in soil, reviewed elsewhere in this chapter (see tation, ammonia stripping, primary chlorination, above, the sections on groundwater, soil, and septic recarbonation, secondary coagulation and sedimen- tanks and below, the section on land treatment), show tation, pH adjustment, sand filtration, secondary that a well-designed sand filter, with a sufficiently deep chlorination, activated carbon, and final chlorination bed and a sufficiently low filtration rate, will remove a (Grabow, Bateman and Burger 1978). A treatment considerable proportion of fecal indicator bacteria in train of this complexity, although highly effective, has the effluent. In particular, a slow sand filter, receiving no application in most countries (whether developed 2-5 cubic meters per square meter per day of effluent, or developing) because of its high cost and excessive should remove around 99 percent of enteric bacteria. operation and maintenance problems. Rapid processes, however, may be relatively ineffective. A combination of ammonia stripping, recarbonation, LAGOONING. If retention times are several days, secondary clarification (with added FeCl3 and lagooning can be highly effective in removing excreted polyelectrolyte), and sand filtration reduced the bacteria. Removal mechanisms and rates are as average concentration of enterococci by only 98 reported above for waste stabilization ponds. With percent (Grabow, Middendorff and Basson 1978). short retention times, lagooning will not achieve Similarly, a tertiary effluent from a gravity sand filter worthwhile reductions in concentrations of excreted on Long Island (New York, USA) contained up to bacteria. Grabow, Middendorff and Basson (1978) 9.3 x 105 fecal coliforms per 100 milliliters (Vaughn report a removal of only 31 percent of coliforms and 18 and others 1978). Removal rates will be enhanced at percent of enterococci from lime-treated tertiary warm temperatures. ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 229 DISINFECTION. The realization that secondary percent of tests. Stenquist and others (1977) found that effluents from conventional sewage treatment plants treating a secondary effluent (BOD5 = 19 milligrams (trickling filters or activated sludge) contain high per liter) with 39 milligrams per liter of chlorine concentrations of excreted viruses and bacteria has reduced coliform concentrations from 106 to <2 per caused a growing interest in effluent disinfection as a 100 milliliters after a 1-hour contact time. means of achieving a major improvement in micro- Although effluent chlorination can produce very low biological quality prior to discharge. The technique concentrations of indicator bacteria at the point of most practiced and most studied is effluent chlori- discharge, it does not always do so. Vaughn and others nation. (1978) reported that chlorinated secondary effluents on As with water chlorination, the level of bacterial kill Lond Island (New York, USA) contained between 0 achieved in effluent chlorination increases as chlorine and 2.4 x 106 fecal coliforms per 100 milliliters. dose, temperature, and contact time increase and as pH Kampelmacher, Fonds and van Noorle Jansen (1977) decreases. The additional factor of critical importance found that the chlorination of three secondary effluents is the chemical quality of the effluent being chlorinated. in the Netherlands (2-6 milligrams per liter of chlorine When chlorine is added to an effluent, free chlorine added) reduced E. coli by between 24 and 99.999 (HOCI + OCI-) disappears almost immediately, and percent and fecal streptococci by 0 to 99.99 percent. the chlorine rapidly combines with ammonia and This great variability of bacteria removal is character- organic compounds. This combined chlorine is very istic of effluent chlorination systems and in part is a considerably less bactericidal than free chlorine- result of the variable chlorine demand of the effluent. although, as with free chlorine, it will be more effective The environment produced by effluent chlorination, as contact times and temperatures increase. namely one of high nutrients but low microbiological When a chlorinated effluent is discharged into a activity, is ideal for the growth of some excreted river, it is possible that the fecal indicator bacteria in bacteria. Several studies have reported massive the river will also be reduced in the stretch of river regrowth of fecal indicator bacteria, especially immediately downstream of the outfall (Snow 1977). coliforms, in chlorinated sewage effluents. Shuval, The chlorine may also have a negative impact on the Cohen and Kolodney (1973) studied trickling filter receiving water by killing certain species of flora and effluent in Jerusalem (Israel) that was treated with 10 fauna and thus upsetting the aquatic ecology (Silvey, milligrams per liter of chlorine and then stored for 3 Abshire and Nunez 1974). In addition, the discharge of days prior to agricultural use. The geometric mean chlorinated effluents will add to the load of chlorinated concentrations of coliforms per 100 milliliters were organic compounds in the water and in the food chain, 5 x 10' in the secondary effluent, 120 in the and some of these compounds are known or suspected chlorinated effluent, and 800 in the stored effluent. carcinogens. Laboratory experiments with 5 milligrams per liter of Properly controlled effluent chlorination can pro- chlorine added to secondary effluent stored at 20°C duce a very dramatic reduction in the concentrations of showed that coliform concentrations fell to 0.001 excreted bacteria. The better the quality of the effluent, percent of their initial value after chlorination but 4 the greater will be the bacterial reduction achieved by a days later had regained their initial level, whereas fecal given dose of applied chlorine. Berg and others (1978) coliform concentrations fell to 0.0001 percent of initial added sodium hypochlorite (NaOCI) to primary levels and had climbed back to 0.1 percent after 5 days. effluents to achieve final combined chlorine residuals of Kinney, Drummond and Hanes (1978) compared 11 to 23 milligrams after 15 minutes at pH 8.2-9.2 and bacterial death rates in chlorinated secondary effluent 22°C. This treatment reduced enterovirus (initial mixed with stream water and in unchlorinated tertiary concentrations 109-427 per liter) by 85-99 percent, fecal effluent mixed with stream water (three parts effluent coliforms (initial concentrations 10'-107 per 100 to one part of stream water). The effluent had a BOD5 milliliters) by 99.95- >99.99998 percent, and fecal value of 7-11 milligrams per liter. The applied chlorine streptococci (initial concentration 105 per 100 dose was 2.3-3.5 milligrams per liter, which produced a milliliters) by 99.997->99.9998 percent (see also Berg total residual of around 1 milligram per liter after 15 and Metcalf 1978). minutes. The mixtures were held in the dark at 20°C. Kott and others (1974) reported that the addition of The chlorinated mixture contained 6 E. coli per 100 8 milligrams per liter of chlorine to waste stabilization milliliters, which rose to 102 per 100 milliliters after 5 pond effluent (1 hour contact time at 20°C) reduced the days. The unchlorinated mixture contained concentration of coliforms from 105-107 per 100 1.9 x 103-2.2 x 104 E. coli per 100 milliliters, which milliliters down to less than 2 per 100 milliliters in 50 fell to 102 per 100 milliliters after 5 days. Similar 230 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA experiments were conducted with total coliforms, per liter (as Cl2) with a contact time of 3 minutes at Klebsiella, Enterobacter, and Citrobacter. In all cases 220C. Reduction of fecal coliforms averaged over 5 log there was no statistically significant difference in units with chlorine dioxide and over 3 log units with bacterial concentrations between the chlorinated and chlorine. This and other studies (for instance, Cronier, unchlorinated mixtures after 4 days of storage. Scarpino and Zink 1978) have shown that chlorine Irving (1980) reported great variability in the dioxide is often a more powerful bactericide than bacterial reductions obtained when chlorine was added chlorine and has other advantages such as being less to raw sewage. Average results showed that, after a affected by pH and less prone to generate carcinogenic contact time of 30 minutes, the coliform reductions trihalogenated methanes. Similarly, Keswick and were 3 log units at 5 milligrams per liter of applied others (1980) found that bromine chloride (BrCI) had chlorine, 4 log units at 10 milligrams per liter of applied several advantages over chlorine as a wastewater chlorine, and > 5 log units at 15 milligrams per liter of disinfectant. applied chlorine. To investigate regrowth, samples of Various other disinfecting methods have been tried, chlorinated sewage were added to seawater and stored at least on an experimental basis. Ozone is able to in the dark at 15°C. When the effluent to seawater mix eliminate fecal solids-associated coliforms after 20 was 1:10, coliform concentrations increased in the seconds with an applied dose of less than 0.1 milligram chlorinated mixture to more than the initial (pre- per liter (Foster and others 1980; see also Wyatt and chlorination) level after 160 hours' storage, whereas the Wilson 1980). Ultraviolet and gamma radiation have unchlorinated control had concentrations of only 10 also been shown to be effective in killing bacteria in percent of initial values. When the effluent to seawater effluent (Myhrstad 1979; Woodbridge and Cooper mix was 1:100, no regrowth occurred and the 1979). These techniques are very much at the chlorinated mixture had coliform concentrations of experimental stage, and their economical and technical 0.001 percent of initial levels after 160 hours' storage, appropriateness are doubtful. The same comments whereas the unchlorinated control had concentrations apply to disinfection by photodynamic oxidation of 1 percent of initial values. The ratio of effluent to (Gerba, Wallis and Melnick 1977). seawater, and thus the concentration of bacterial nutrients, was found to influence strongly the coliform LAND TREATMENT. The treatment of a primary or regrowth potential. When actual marine outfall secondary effluent by application to land, with conditions were simulated (ten-fold dilution of sewage subsequent flow through the soil to underdrains or to initially rising to a hundredfold dilution after 3.5 groundwater, can be an effective method of removing hours), no regrowth of coliforms or fecal coliforms was high concentrations of excreted viruses (see chapter 9) recorded in the chlorinated effluent and seawater and bacteria. Lance, Rice and Gilbert (1980) reported mixture. a 5 log removal of fecal coliforms from primary Fecal coliforms are more susceptible to chlorination, effluent (settled sewage) as it passed through 2.5 meters and undergo lesser regrowth in chlorinated effluents, of loamy sand at the rate of 0.2 cubic meters per square than coliforms as a whole. Fecal streptococci may be meter per day and at a temperature of 24°C. Under slightly less susceptible to chlorination of effluents than similar conditions, but with double the infiltration rate, fecal coliforms. Major regrowth of fecal indicator there was a 3 log removal of fecal coliforms from bacteria in chlorinated effluents and their receiving secondary effluents. A theoretical approach to waters is more likely in fresh water than in seawater, computing the degree of bacteria removal by land where dilution is low (less than ten-fold) and where treatment systems has been proposed by Hendricks, temperatures are warm. Thus, the discharge of Post and Khairnar (1979). chlorinated effluents into tropical streams, which have Gilbert and others (1976) recorded that the fecal little or no flow during the dry season, is a situation coliforms and fecal streptococci in a secondary effluent almost certainly accompanied by major regrowth of were reduced by 99.9 percent after flow through 9 coliforms, fecal coliforms, and possibly other excreted meters of soil (fine loamy sand underlain by coarse sand bacteria. and gravel) under groundwater recharge basins at Chlorine dioxide (CI02) has attracted interest Phoenix (Arizona, USA). The application rates recently as a disinfectant of water and wastewater, average 0.25 cubic meters per square meter per day, although its mode of action is not elucidated (Roller, and the mean daily air temperatures ranged between Olivieri and Kawata 1980). Longley, Moore and 10°C in January and 32°C in July. Fecal coliforms were Sorber (1980) compared chlorine and chlorine dioxide not detected in water from a well 90 meters distant from applied to secondary effluent at doses of 5 milligrams the recharge basins (Bouwer and others 1980). Schaub ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 231 and Sorber (1977) studied a rapid infiltration site (1.4 concentrations of fecal indicator bacteria are typically cubic meters per square meter per day) in found (105-10' per gram). This section describes Massachusetts (USA) where primary effluent had been methods of killing bacteria contained in night soil or applied to unconsolidated silty sand and gravel for sludge and emphasizes the important role of time and over 30 years. Nearly all indicator bacteria were temperature in creating conditions lethal to bacteria. removed in the top 1 meter of soil, but, on occasion, up to 104 fecal streptococci per 100 milliliters were By pit latrines detected in the groundwater, as compared with 105-106 per 100 milliliters of effluent. Pit latrines are an effective method of containing and Land treatment will in general be more effective in storing excreted bacteria. Death rates will be very warm climates than in temperate ones. Maintenance much more rapid at warm temperatures than at cold and management of these installations must be highly temperatures and may be more rapid in dry pits than in efficient, otherwise, the treatment site will degenerate flooded pits. A pit in use will always contain fresh layers into an unsanitary bog. of pathogenic material. The contents of a sealed pit in a warm climate, however, should contain a very low OTHER PROCESSES. A variety of other processes for concentration of fecal indicator bacteria after 3 the treatment of sewage are being tried on a laboratory months' storage. or pilot scale. Many of these research and development Stiles and Crohurst (1923) buried human feces in pits projects focus on the need to produce a final effluent in an area with a high water table and covered them almost completely free of excreted organisms and with sawdust. Three years and 2 months later, the feces attempt to reclaim sewage for agricultural or other were both macroscopically, and, microscopically productive purposes. Some of the technologies being recognizable but had developed a "musty" odor. Three developed have high performance in removing fecal out of five samples contained viable E. coli. Jordan indicator bacteria-for instance, solar distillation (1926) found that E. coli in stored human feces became (Qasim 1978)-but are unlikely to be economically undetectable after 6-12 weeks at room temperature and and technically appropriate for application in develop- after 1-3 weeks at 37°C. At 10°C they were still ing countries. Technologies that are simple, relatively detectable in high concentrations after 23 weeks. low cost, and highly effective in removing excreted bacteria are already known (for instance, waste By anaerobic digestion stabilization ponds or land treatment of secondary effluents), and the priority in most developing Anaerobic digestion is the most commonly adopted countries is the successful and widespread application method of sludge treatment at large sewage treatment of these established technologies. works. The process is usually mesophilic (35°C) but is sometimes heated to the thermophilic range (55°C). Retention times are typically 10-60 days. Inactivation by Night Soil and Sludge Cooke, Thackston and Malaney (1978) studied Treatment Processes mesophilic anaerobic digestors at three treatment plants near Nashville (Tennessee, USA). Since fresh feces commonly contain 105-109 fecal Concentrations of coliforms in the raw primary sludge coliforms and fecal streptococci per gram, the fecal were 108_1010 per 100 milliliters and in the digested products from dry sanitation systems contain high sludge were 104-109 per 100 milliliters. All digesters concentrations of fecal indicator bacteria. It is this very were operating at 33-37°C, but retention times varied concentration of excreted organisms that makes the considerably. The mean removal rates at different dry systems attractive compared with the wet systems, retention times were less than 2 log units after 9 days, 3 which mix the fecal material with large volumes of log units, after 38 days, and nearly 4 log units after 50 water that are then difficult to purify and contain. days. Berg and Metcalf (1978) reported that a From a microbiological viewpoint the essential continuously operated mesophilic digester (35°C for 20 principle of the dry sanitation systems is that they days) removed 95 to 99 percent of fecal coliforms and should concentrate and contain the excreted or- 80 to 97 percent of fecal streptococci, whereas a ganisms in the smallest possible volume where they thermophilic digester (50°C for 20 days) removed 99.9 may then be killed. The sludge from a sewage treatment to > 99.9999 percent of fecal coliforms and 99.8 to plant contains those bacteria which were adsorbed to, >99.999 percent of fecal streptococci. Studies in the or trapped within, settleable solids, and high USSR showed that an enteropathogenic serotype of E. 232 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA coli survived thermophilic digestion for not more than per week; windrow 2 contained pig waste turned 20 10 days (Grigoryeva, Korchak and Bey 1969). times per week; windrow 3 contained pig waste plus Continuously fed mesophilic digesters will produce old compost turned 20 times per week; windrow 4 sludge that still contains high concentrations of fecal contained pig waste plus straw turned 20 times per indicator bacteria (103-106 per 100 milliliters), even if week. The speed of temperature rise declined in the retention timnes are around 50 days. For substantially order of windrows 4, 3, 2, 1. All windrows eventually higher levels of bacterial reduction the process should reached 60°C. Windrow 4 reached 60°C in 3 days, after be thermophilic, with retention times of at least 20 days which it rose to 72°C, stayed above 60°C for over 30 and preferably with batch operation. Thermophilic days, and fell back to ambient temperature (20-30°C) operation is more economical in warm climates than in by day 38. In windrow 1, fecal coliforms and fecal temperate areas because heat loss to the environment is streptococci numbers increased for the first 40 to 60 reduced; therefore less energy input is required (from days until temperatures reached 50°C, after which digester biogas or other sources). However, the most bacterial concentrations decreased as the temperatures economical method of achieving thermophilic con- rose into the thermophilic range. In windrows 2 and 3, ditions, and thereby high levels of excreted bacterial the concentrations of fecal coliforms fell from 107 to reduction, is often by aerobic composting. Finstein and 103 per gram after 35 days, whereas in windrow 4 fecal others (1980) compared anaerobic digestion with coliforms became undetectable after 14 days. The composting and found that, although digestion combination of frequent turning and the addition of required less labor and produced methane, composting straw (which provided a source of carbon and was advantageous with respect to pathogen kill, improved the structure of the compost by furnishing process stability, decomposition of industrial com- more opportunity for aeration) produced a windrow pounds, drying, and residue acceptability. that achieved very high bacterial death rates (7 log units in 14 days). By heating Burge, Cramer and Epstein (1978) have reviewed the composting work conducted at Beltsville Agricultural Any process that heats night soil or sludge to over Research Center (Maryland, USA). In early experi- 60°C for the required length of time will ments raw or digested sludge filter cake (20 per cent eliminate fecal indicator bacteria. Most of the heating solids) was mixed with woodchips (1 volume sludge to processes such as pasteurization (80°C), wet oxid- 3 volumes of woodchips), placed in windrows, and ation (120-370°C), incineration, and pyrolysis-will turned daily for 2 weeks, after which it was stockpiled completely destroy all excreted organisms but are for a minimum of 30 days. Temperatures in the technically complex and require considerable energy windrows rose to 50-70'C in 3 days with raw sludge, input. More attractive is thermophilic, aerobic and to 40-60° in 14 days with digested sludge, except in composting, which elevates temperatures to above rainy winter weather when temperatures stayed at 60°C without thc nccd for any external energy source. 20-30°C. Fecal coliforms typically declined from 107 Time-temperature combinations that will destroy per gram to undetectable levels during the windrow enteroviruses (see chapter 9) and Ascaris eggs (see phase at depths of 0.8 meters and more. At depths of chapter 23) will certainly destroy the nonspor- less than 0.4 meters, where the windrow was cooler, ulating excreted bacteria. fecal coliform concentrations declined from 107 to 102_104 per gram during the windrow phase and By composting maintained these concentrations during 30 days of stockpiling. Because of lowered temperature during The composting of night soil and sludge is a simple heavy rain, poor bacterial kill at the edges of the means of producing a fecal product that is safe and windrows, and bad odor release from the raw sludge convenient to use in agriculture. Of greatest interest are windrows, new experiments were started in which the aerobic processes that generate sufficient heat to windrows (raw sludge plus woodchips) were aerated raise the temperature of the composting mass to 550C (by sucking air downwards into slotted pipes laid under or above and thus kill a large proportion of excreted the windrow) and lagged by covering with a layer of old pathogens. compost. Composting by forced aeration was Savage, Chase and MacMillan (1973) studied the continued for 21 days, after which the material was composting of pig waste (uneaten garbage and pig stockpiled for a minimum of 30 days. Temperatures feces) in four windrows, which were mechanically rose into the thermophilic range within 5 days, turned. Windrow 1 contained pig waste turned twice irrespective of the weather conditions. Fecal coliforms ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 233 were reduced to undetectable levels after 10 days in the and no significant additional dieoff occurred during 2 windrows, and this bacterial destruction occurred at all days storage at 25°C. parts of the composting mass (see also Kawata, Cramer and Burge 1977). Unpublished data obtained by Vietnamese scientists have suggested that E. coli are reduced to undetectable Various other methods have been proposed for the levels after 7 weeks treatment in a sealed vault of a disinfection of sludges prior to agricultural use. double-vault composting latrine (Nimpuno, personal Irradiation of sludges by 3-3.5 kilogray produces a communication). McGarry and Stainforth (1978) 4 to 9 log reduction in Gram-negative enteric describe aerobic (average pile temperature 40°C) and bacteria such as fecal coliforms. Gram-positive anaerobic (average pile temperature 29°C) composting bacteria such as fecal streptococci appear to be with equal parts by weight of human feces and urine, somewhat more resistant and may be reduced by only 2 animal feces, rubbish (sweepings, brushwood, grass, to 3 log units (Lessel and Suess 1978; Osborn and ashes, weeds, leaves), and soil held for one month in Hattingh 1978). A radiated sludge, however, is a China. Initial E. coli concentrations of the mixture were nutrient-rich but biologically impoverished medium, 2.5 x 105 per gram, and these were reduced to 91-233 and major regrowth of fecal indicator bacteria may be per gram in both the aerobic and anaerobic processes. predicted and has been reported (Osborn and It is clear from these and other studies (listed in the Hattingh 1978). Superchlorination of sludges (chlorine appendixes of Feachem and others 1980) that well- doses of 700-4,000 milligrams per liter applied under managed composting plants can reduce fecal indicator pressure) will certainly destroy fecal bacteria, but it has bacteria in night soil and sludge to undetectable levels to be questioned seriously on environmental grounds in under 1 month. For this to occur, the process must (Kamlet 1979). become thermophilic rapidly. This in turn requires the addition of carbon, aeration by turning or forced ventilation, moisture control, and a good physical Literature Cited structure with adequate air voids for the pile. To ensure that all parts of the pile achieve a disinfecting Adams, A. P., Garbett, M., Rees, H. B. and Lewis, B. G. temperature, the compost must be turned or lagged. (1980). Bacterial aerosols produced from a cooling tower The experiments at Beltsville have shown that forced using wastewater effluent as makeup water. Journal of the ventilation and lagging can create high temperatures Water Pollution Control Federation, 52, 498-501. throughout a windrow even during cold and rainy Allen, L. A., Pasley, S. M. and Pierce, M. A. F. (1952). Some winters. factors affecting the viability of faecal bacteria in water. Journal of General Microbiology, 7, 36-43. Allen, M. J. (1979). Microbiology of groundwater. Journal of By lime treatment the Water Pollution Control Federation, 51, 1743-1746. Lime treatment, resulting in high pH values, should Banerjea, R. and Sen, A. K. (1940). Study of the Eijkman test be effective in reducing fecal indicator bacteria in night and modifications as given by coliform organisms isolated soileand sludge,m althucmgh little spcific informationght from human faeces. Indian Journal of Medical Research, soil and sludge, although little specific information 1S 28, 315-319. available. Lime treatment is certainly effective in Baross, J. A., Hanus, F. J. and Morita, R. Y. (1975). Survival eliminating salmonellae from sludges and animal of human enteric and other sewage microorganisms under slurries (see chapter 15). Polprasert and Valencia simulated deep-sea conditions. Applied Microbiology, 30, (1981) applied various concentrations of lime to fecal 309-318. samples collected from school children in Bangkok Barrell, R. A. E. and Rowland, M. G. M. (1979a). Infant foods (Thailand). Initial pH was 5.8-6.0, and the fecal as a potential source of diarrhoeal illness in rural West coliform concentrations were 4.6 x 1010 to 1 x 10" Africa. Transactions of thze Royal Society of Tropical per milliliter. The addition of 5,700 milligrams of CaO Medicine and Hygiene, 73, 85-90. per liter raised the pH to 9 and reduced the fecal (1979b). The relationship between rainfall and well colif. co bwater pollution in a West African (Gambian) village. coliform concentration by 0-1 log units. The addition Journal of Hygiene, 83, 143-150. of 19,000 milligrams of CaO per liter raised the pH to Bausum, H.T., Schaub,S. A. and Kenyon, K. F. (1978). Viral 12 and reduced the fecal coliform concentration by 4-6 and Bacterial Aerosols at a Wastewater Spray Irrigation log units. Intermediate doses produced intermediate Site. Technical Report 7804. Washington, DC: US Army pH values and bacterial reductions. Fecal coliform Medical Research and Development Command. death occurred in the first 3 hours after lime dosing, Baylor, E. R., Baylor, M. B., Blanchard, D. C., Syzdek, L. D. 234 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA and Appel, C. (1977). Virus transfer from surf to wind. black water septic tanks. Journal of the Water Pollution Science, 198, 575-580. Control Federation, 50, 2547-2559. Baylor, E. R., Peters, V. and Baylor, M. B. (1977). Water-to- Brokunsult and Ross Institute (1978). Rural Water Quality air transfer of virus. Science, 197, 763-764. Programme in Tanzania. Dar es Salaam: Ministry of Water Bell, R. G. (1976). Persistence of fecal coliform indicator Development, Energy and Minerals. bacteria on alfalfa irrigated with municipal sewage lagoon Brown, K. W., Jones, S. G. and Donnelly, K. C. (1980). The effluent. Journal of'Environmental Quality, 5, 39-42. influence of simulated rainfall on residual bacteria and Bell, R. G. and Bole, J. B. (1976). Elimination of fecal coliform virus on grass treated with sewage sludge. Journal of bacteria from reed canarygrass irrigated with municipal Environmental Quality, 9, 261-265. sewage lagoon effluent. Journal of Environmental Q,.,,, Brown, K. W., Wolf, H. W., Donnelly, K. C. and Slowey, J. F. 5, 417-418. (1979). The movement of fecal coliforms and coliphages (1978). Elimination of fecal coliform bacteria from below septic lines. Journal of Environmental Quality, 8, soil irrigated with municipal sewage lagoon effluent. 121-125. Journal of Environmental Quality, 7, 193-196. Burdyl, P. and Post, F. J. (1979). Survival of Escherichia coli Bellair, J. T., Parr-Smith, G. A. and Wallis, I. G. (1977). in Great Salt Lake water. Water Air and Soil Pollution, 12, Significance of diurnal variations in fecal coliform die-off 237-246. rates in the design of ocean outfalls. Journlal of the Water Burge, W. D., Cramer, W. N. and Epstein, E. (1978). '.1 Contr ol Federation, 49, 2022-2030. Destruction of pathogens in sewage sludge by composting. Berg, G., Dahling, D. R., Brown, G. A. and Berman, D. Transactions of the American Society oJ Agricultural (1978). Validity offecal coliforms, total coliforms and fecal Engineers. 21, 510-514. streptococci as indicators of viruses in chlorinated primary Cabelli, V. J. (1978). New standards for enteric bacteria. In sewage effluents. Applied and Environmental Microbiology, Water Pollution Microbiology. 2, ed. Mitchell, R.. pp. 36, 880-884. 233-271. New York: Wiley-Interscience. Berg, G. and Metcalf, T. G. (1978). Indicators of viruses in (1979). Evaluation of recreational water quality, the waters. In Indicators of Viruses in Water and Food, ed. Berg, EPA approach. In Biological Indicators of 'Water Qualitv, G., pp. 267-296. Ann Arbor, Mich.: Ann Arbor Science eds. James, A. and Evison, L., pp. 14/1-14/23. Chichester: Publishers. John Wiley. Bettelheim, K. A., Cooke, E. M., O'Farrell, S. and Shooter, R. Cabelli, V. J., Dufour, A. P., Levin, M. A., McCabe, L. J. and A. (1977). The effect of diet on intestinal Escherichia coli. Haberman, P. W. (1979). Relationship of microbial Journal of'Hygiene, 79, 43-45. indicators to health effects at marine bathing beaches. Bitton, G. and Smith-Holmes, W. (1978). Bacterial aerosols American Journal of Public Health, 69, 690-696. generated by a package treatment plant. Journzal of Caldwell, E. L. and Parr, L. W. (1937). Groundwater Environmental Science and Health, A13, 391-401. pollution and the bored hole latrine. Journal of'Infectious Black, R. E., Merson, M. H., Rowe, B., Taylor, P. R., Mizanur Diseases, 61, 148-183. Rahman, A. S. M., Azizal Huq, M., Abdul Aleem, A. R. M., Chamberlin, C. E. and Mitchell, R. (1978). A decay model for Sack, D. A. and Curlin, G. T. (1979). Epidemiology of enteric bacteria in natural waters. In Water Pollution enterotoxigenic Escherichia coli in rural Bangladesh. In Microbiology, 2, ed. Mitchell, R., pp. 325-348. New Proceedings of the 14th Joint Conference, US-Japan York: Wiley-Interscience. Cooperative Medical Science Program, Cholera Panel, Chandler, D. S. and Craven, J. A. (1978a). Bacteriological Symposium on Cholera, eds. Takeya, K. and Zinnaka, Y., studies of land disposal of piggery effluent. Proceedings of pp. 292-301. Tokyo: Toho University. the Australian Society of Animal Production, 12, 158. Blanchard, D. C. and Syzdek, L. (1970). Mechanism for - (1978b). Environmental factors affecting Escherichia water-to-air transfer and concentration of bacteria. coli and Salmonella typhimurium numbers on land used for Science, 170, 626-628. effluent disposal. Australian Journal of Agricultural Boizot, G. E. (1941). An examination of the modified Research, 29, 577-585. Eijkman method applied to pure coliform cultures (1980). Persistence and distribution of Erysipelothrix obtained from waters in Singapore. Journal ofHygiene, 41, rhusiopathiae and bacterial indicator organisms on land 566-569. used for disposal of piggery effluent. Journal of Applied Bound, W. H. and Atkinson, R. 1. (1966). Bacterial aerosol Bacteriology, 48, 367-375. from water closets. Lancet, 1, 1369-1370. Chojnowski, K. J., Mancini, J. L. and Jeris, J. S. (1979). Bouwer, H., Rice, R. C., Lance, J. C. and Gilbert, R. G. (1980). Influence of light on coliform mortality rates in fresh water Rapid infiltration research at Flushing Meadows Project, and sea water. Journal of the Water Pollution Cont0ol Arizona. Journal of the Water Pollution Control Federation, 51, 2538-2539. Federation, 52, 2457-2470. Ciravolo, T. G., Martens, D. C., Hallock, D. L., Collins, E. R., Brandes, M. (1978a). Accumulation rate and characteristics Kornegay, E. T. and Thomas, H. R. (1979). Pollutant of septic tank sludge and septage. Journal of the Water movement to shallow ground water tables from anaerobic Pollution Control Federation, 50, 936-943. swine waste lagoons. Journal of Environmental Quality, 8, (1978b). Characteristics of effluents from gray and 126-130. ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 235 Coetzee, 0. J. and Fourie, N. A. (1965). The efficiency of wastewater stream. Journal oj Applied Ecology, 13, conventional sewage purification works, stabilization 475-489. ponds and maturation ponds with respect to the survival of Druett, H. A., Henderson, D. W., Packman, L. and Peacock, pathogenic bacteria and indicator organisms. Journal of S. (1953). Studies on respiratory infection. I. The influence the Institute of Sewage Purification, part 3, 210-215. of particle size on respiratory infection with anthrax Cohen, J. and Shuval, H. I. (1973). Coliforms, fecal coliforms spores. Journal of Hygiene, 51, 359-371. and fecal streptococci as indicators of water pollution. Druett, H. A., Henderson, D. W. and Peacock, S. (1956). Water, Air, and Soil Pollution, 2, 85-95. Studies on respiratory infection. III. Experiments with Cooke, M. B., Thackston. E. L. and Malaney, G. W. (1978). Brucella suis. Journal of Hygiene, 54, 49-57. Reducing coliform and Salmonella bacteria during Dudley, D. J., Guentzel, M. N., Ibarra, M. J., Moore, B. E. anaerobic digestion. Water and Sewage Works, 125, 50-53. and Sagik, B. P. (1980). Enumeration of potentially Crawford, G. V. and Jones, P. H. (1978). The airborne pathogenic bacteria from sewage sludges. Applied and transmission of organisms emitted from wastewater Environmental Microbiology, 39, 11 8-126. treatment processes. Water Pollution Research in Canada, Dudley, D. R. and Karr, J. R. (1979). Concentration and 13, 33-43. sources of fecal and organic pollution in an agricultural Cronholm, L. S. (1980). Potential health hazards from watershed. Water Resources Bulletin, 15, 911-923. microbial aerosols in densely populated urban regions. Dunigan, E. P. and Dick, R. P. (1980). Nutrient and coliform Applied and Environmental Microbiology, 39, 6-12. losses in runoff from fertilized and sewage sludge-treated Cronier, S., Scarpino, P. V. and Zink, M. L. (1978). Chlorine soils. Journal of Enuironmental Quality, 9, 243-250. dioxide destruction of viruses and bacteria in water. In DuPont, H. L., Formal, S. B., Hornick, R. B., Snyder, M. J., Water Chlorination: Environmental Impact and Health Libonati, J. P., Sheahan, D. G., LaBrec, E. H. and Kalas, J. Effects, eds. Jolley, R. L., Gorchev, H. and Hamilton, D. H.. P. (1971). Pathogenesis of Escherichia coli diarrhea. New pp. 651-658. Ann Arbor, Mich.: Ann Arbor Science England Journal of Medicine, 285, 1-9. Publishers. Dutka, B. J. and Kwan, K. K. (1980). Bacterial die-off and Crozier, D. and Woodward, T. E. (1962). Armed Forces stream transport studies. Water Research, 14, 909-915. Epidemiological Board: activities of the Commission on Dyer, B. R., Bhaskaran. T. R. and Sekar, C. C. (1945). Epidemiological Survey, 1961. Military Medicine, 127, Investigations of groundwater pollution. III. Groundwater 701-705. pollution in West Bengal, India. Indian Journal of Medical Dale,, D. C. and Mata, L. J. (1968). Studies of diarrheal Research, 33, 23-62. disease in Central America. Xl. Intestinal bacterial flora in Echeverria, P., Blacklow, N. R., Vollett, J. L., Ulyangco, C. V., malnourished children with shigellosis. American Journal Cukor, G., Soriano, V. B., DuPont, H. L., Cross, J. H., of Tropical Medicine and Hygiene, 17, 397-403. Orskov, F. and Orskov, I. (1978a). Reovirus-like agent Daniel, R. R. and Lloyd, B. J. (1980). Microbiological studies and enterotoxigenic Escherichia coli infections in pediatric on two Oxfam Sanitation Units operating in Bengali diarrhea in the Philippines. Journal of Infectious Diseases, refugee camps. Water Research, 14, 1567-1571. 138, 326-332. Darlow, H. M. and Bale, W. R. (1959). Infective hazards of Echeverria, P., Verhaert, L., Basaca-Sevilla, V., Banson, T., water-closets. Lancet, 1, 1196-1200. Cross, J., Orskov, F. and Orskov, 1. (1978b). Search for Davenport, C. V., Sparrow, E. B. and Gordon, R. C. (1976). heat-labile enterotoxigenic Escherichia coli in humans, Fecal indicator bacteria persistence under natural livestock, food and water in a community in the conditions in an ice-covered river. Applied an(d Philippines. Journlal o1 Infectious Diseases. 138, 87-90. Environmental Microbiology, 32, 527 536. Echeverria, P., Blacklow, N. R., Zipkin, C., Vollet, J. J., Olson, Davis, E. M. (1979). Bacterial Characteristics of Stormwaters J. A., Dupont, H. L. and Cross, J. H. (1979). Etiology of in Developing Rural Areas. Report EPA-600/2-79-050f. gastroenteritis among Americans living in the Philippines. Cincinnati, Ohio: US Environmental Protection Agency. American Journal of Epidemiology, 109, 493-501. Davis, E. M. and Gloyna, E. F. (1972). Bacterial die-off in Echeverria, P., Ho, M. T., Blacklow, N. R., Quinnan, G., ponds. Journal of the Sanitary Engineering Division, Portnoy, B., Olson, J. G., Conklin, R., DuPont, H. L. and Proceedings of the American Society of Civil Engineers, 98, Cross, J. H. (1977). Relative importance of viruses and 59-69. bacteria in the etiology of pediatric diarrhea in Taiwan. Dazzo, F., Smith, P. and Hubbell, D. (1973). The influence of Journal of Infectious Diseases, 136, 383-390. manure slurry irrigation on the survival of fecal organisms Edmond, T. D., Schaiberger, G. E. and Gerba, C. P. (1978). in Scranton fine sand. Journal of Environmental Quality, 2, Detection of enteroviruses near deep marine sewage 470-473. outfalls. Marine Pollution Bulletin, 9, 246-249. Dissanayake, M. G. (1980). Kinetics of bacterial die-off in Edmonds, R. L. (1976). Survival of coliform bacteria in waste stabilization ponds. Ph.D. dissertation no. EV-80-2. sewage sludge applied to a forest clearcut and potential Bangkok: Asian Institute of Technology. movement into groundwater. Applied and Environmental Dor, I., Schechter, H. and Shuval, H. I. (1976). Biological and Microbiology, 32, 537-546. chemical succession in Nahal Sareq: a free-flowing Edmonds, R. L. and Littke, W. (1978). Coliform aerosols 236 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA generated from the surface of dewatered sewage applied to Water and Telecommunications Department. a forest clearcut. Applied and Environmental Microbiology, Fedorak. P. M. and Westlake, D. W. S. (1980). Airborne 36, 972-974. bacterial densities at an activated sludge treatment plant. Elliot, L. F. and Ellis, J. R. (1977). Bacterial and viral Journ1al of the Water Pollutioni Contol Federationi, 52, pathogens associated with land application of organic 2185-2192. wastes. Journal of Environmental Quality, 6, 245-251. Feliciano, D. V. (1979). Wastewater aerosols and health risks. Enzinger, R. M. and Cooper, R. C. (1976). Role of bacteria Journal of the Water Pollution Control Federation, 51, and protozoa in the removal of Escherichia coli from 2573-2576. estuarinewaters. Applied and EnvironmentalMicrobiology. Ferguson, W. W. and June, R. C. (1952). Experiments on 31, 758-763. feeding adult volunteers with Escherichia (oli. II[ B,. a Essien, E. S. and Osuhor, P. C. (1979). Rural water quality coliform organism associated with infant diarrhea. control measures: an experience in the Malumfashi American Journal of Hygiene, 55, 155-169. District of Northern Nigeria. Public Health, 93, 363-370. Finstein, M. S., Cirello, J., Suler, D. J., Morris, M. L. and Evans, M. R. and Owens, J. D. (1972). Factors affecting the Strom, P. F. (1980). Microbial ecosystems responsible for concentration of faecal bacteria in land-drainage water. anaerobic digestion and composting. Journal of the Water Journal of General Microbiology, 71, 477-485. Pollution Control Federation, 52, 2675-2685. Evison,L. (1979). Microbial parameters of raw water quality. Foster, D. M., Emerson, M. A.. Buck, C. E.. Walsh, D. S. and In Biological Indicator of 'Water ch,,,ia i. eds. James, A. and Sproul, 0. J. (1980). Ozone inactivation of cell- and fecal- Evison, L., pp. 16/1-t6/19. Chichester: John Wiley. associated viruses and bacteria. Journal of the Water Evison, L. and James, A. (1973). A comparison of the Pollution Control Federation, 52, 2174-2184. distribution of intestinal bacteria in British and East Freiji, L.. Sterky, G., Wadstrom, T. and Wall. S. (1979). African water sources. Journal oj Applied Bacteriology, 36, Child health and diarrhoeal disease in relation to supply 109-118. and use of water in African communities. Progress in Water Evison, L. and Tosti, E. (1980). Bathing water quality in the Technology, 11, 49-55. Nor,th Sea and the Mediterranean. Marine Pollution Gallagher, T. P. and Spino, D. F. (1968). The significance of Bulletin, 11, 72-75. numbers of coliform bacteria as an indicator of enteric Fannin, K. F., Gannon, J. J., Cochran, K. W. and Spendlove, pathogens. Water Research, 2, 169-175. J. C. (1977). Field studies on coliphages and coliforms or Gameson. A. L. H. and Gould, D. J. (1975). Effects of solar indicators of airborne animal viral contamination from radiation on the mortality of some terrestrial bacteria in wastewater treatment facilities. Water Research, 11, seawater. InR I" .. -.. . fthelnternationalSymposiumzon 181-188. Discharge of Sewagefrom Sea Outfalls, ed. Gameson, A. L. Faust, M. A., Aotaky, A. E. and Hargadon, M. T. (1975). H., pp. 209-219. Oxford: Pergamon. Effect of physical parameters on the in situ survival of Gameson, A. L. H. and Saxon, J. R. (1967). Field studies on Escherichia coli MC-6 in an estuarine environment. effect of daylight on mortality of coliform bacteria. Water Applied Microbiology, 30, 800-806. Research, 1, 279-295. Feachem, R. (1973). The Raiapu Enga pig herd. Mankiind, 9, Gangarosa, E. J. (1978). Epidemiology of Escherichia coli in 25-31. the United States. Journal of Infectious Diseases, 137, (1974). Faecal coliforms and faccal streptococci in 634-638. streams in the New Guinea Highlands. Water Research, 8, Geldreich, E. E. (1976). Faecal coliform and faecal 367-374. streptococcus density relationships in waste discharges ------(1975). An improved role for faecal coliform to faecal and receiving water. CRC Critical Reviews in streptococci ratios in the differentiation between human Environmental Control, 5, 349-368. and non-human pollution sources. Water Research, 9, (1978). Bacterial populations and indicator concepts 689-690. in feces, sewage, stormwater and solid wastes. In Indicators (1977). Water supplies for low income communities: of Viruses in Water and Food, ed. Berg, G., pp. 51-97. Ann resource allocation, planning and design for a crisis Arbor, Mich.: Ann Arbor Science Publishers. situation. In Water, Wastes and Health in Hot (','.: , Geldreich, E. E., Best, L. C., Kenner, B. A. and Van Donsel. eds. Feachem, R., McGarry, M. and Mara, D.. pp. 75-95. D. J. (1968). The bacteriological aspects of stormwater Chichester: John Wiley. pollution. Journal of the Water Pollution Control Feachem, R., Burns, E., Cairneross, S., Cronin, A., Cross, P.. Federation, 40, 1861-1872. Curtis, D., Khan, M. K., Lamb, D. and Southall, H. (1978). Geldreich, E. E. and Bordner, R. H. (1971). Fecal Water Health and Development: An Interdisciplinary contamination of fruits and vegetables during cultivation Evaluation. London: Tri-Med Books. and processing for market. A review. Journal of Milk and Feachem, R. G. A., Bradley, D. J., Garelick, H. and Mara, D. Food Technology, 34, 184-195. D. (1981). Health Aspects of' Exereta and Sullage Geldreich, E. E. and Clarke, N. A. (1966). Bacterial pollution Management: A State-of-the-Art Review. Appropriate indicators in the intestinal tract of freshwater fish. Applied Technology for Water Supply and Sanitation, vol. 3. Microbiology, 14, 429-437. Washington. DC: The World Bank, Transportation. Geldreich, E. E., Huff, C. B., Bordner, R. H., Kabler, P. W. ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 237 and Clark, H. F. (1962). The faecal coli-aerogenes flora of Water Research, 12, 343-352. soils from various geographical areas. Journial of Applied Gordon, J. E. (1964). Acute diarrheal disease. American Bacteriology, 25, 87-93. Journal of the Medical Sciences, 248, 345-365. Geldreich, E. E. and Kenner, B. A. (1969). Concepts of fecal Goval. S. M., Gerba. C. P. and Melnick. J. L. (1977). streptococci in stream pollution. Journal of the Water Occurrence and distribution of bacterial indicators and Pollution Control Federation, 41, R336-R352. pathogens in canal communities along the Texas coast. Geldreich, E. E., Kenner, B. A. and Kabler, P. W. (1964). Applied and Environmental Microbiology, 34, 139-149. Occurrence of coliforms, fecal coliforms and streptococci (1978). Prevalence of human enteric viruses in coastal on vegetation and insects. Applied Microbiology, 12, 63-69. canal communities. Journal of the Water Pollution Control Gerasimenko, D. D. (1977). On survival rate of colon bacillus Federation, 50, 2247-2256. in oil-polluted sea water. AIl 1 (',. Ji. . , Zhurnal Kiev, (1979). Human enteroviruses in oysters and their 39, 726-728. overlying waters. Applied and Enviroonmental Microbiology, Gerba. C. P., Goyal, S. M., Smith, E. M. and Melnick, J. L. 37, 572-581. (1977). Distribution of viral and bacterial pathogens in a Grabow, W. O. K., Bateman, B. W. and Burger, J. S. (1978). coastal canal community. Marine Pollution Bulletin, 8, Microbiological quality indicators for routine monitoring 279-282. of wastewater reclamation systems. Progress in Water Gerba, C. P. and McLeod, J. S. (1976). Effect of sediments on Technology, 10, 317-327. the survival of Escherichia coli in marine waters. Applied Grabow, W. 0. K. and Isaacson, M. (1978). Microbiological and Environmental Microbiology, 32, 114-120. quality and epidemiological aspects of reclaimed water. Gerba, C. P., Wallis, C. and Melnick, J. L. (1975a). Fate of Progress in Water Tecilnology, 10, 329-335. wastewater bacteria and viruses in soil. Journal of the Grabow, W. 0. K., Middendorff, I. G. and Basson, N. C. Irrigation and Drainage Division, Proceedings of the (1978). Role of lime treatment in the removal of bacteria, American Society of Civil Engineers, 101, 157-174. enteric viruses and coliphages in a wastewater reclamation (1975b). Microbiological hazards of household plant. Applied and Environmenital Microbiology, 35, toilets: droplet production and the fate of residual 663-669. organisms. Applied Microbiology, 30, 229-237. Grabow, W. 0. K. and Nupen, E. M. (1972). The load of (1977). Disinfection of wastewater by photodynamic infectious microorganisms in the waste water of two South oxidation. Journal of the Water Pollution Control African hospitals. Water Research, 6, 1557-1563. Federation, 49, 575-583. Gracey, M., Ostergaard, P., Adnan, S. W. and Iveson, J. B. Gilbert, R. G., Gerba, C. P., Rice. R. C., Bouwer, H., Wallis, C. (1979). Faecal pollution of surface waters in Jakarta. and Melnick, J. L. (1976). Virus and bacteria removal from Transactions of the Royal Society of Tropical Medicine and wastewater by land treatment. Applied and Environmental Hygiene, 73, 306-308. Microbiology, 32, 333-338. Gray, E. A. (1975). Survival of Escherichia coli in stream Gilman, R. H., Spira, W. M., Rabbani, G. H. and Al- water in relation to carbon dioxide and plant photo- Mahomod, A. (1980). Invasive E. coli and V para- synthesis. Journal of Applied Bacteriology, 39, 47-54. haemolyticus: a rare cause of dysentery in Dacca. Grigoryeva, L. V., Korchak, G. I. and Bey, T. V. (1969). Transactions of the Royal Society of Tropical Medicine and Survival of bacteria and viruses in sewage sludges. Hygiene, 74, 688-689. Mikrobiologichnyi Zhurnal, 31, 659-664. Glantz, P. J. and Krantz, G. E. (1965). Escherichia coli Gu&lin, A. (1962). Polluted waters and the contamination of serotypes isolated from fish and their environment. Health fish. In Fislh as Food, 2, ed. Borgstrom, G., pp. 481-502. Laboratory Science, 2, 54-63. New York: Academic Press. Goff, G. D., Spendlove, J. C., Adams, A. P. and Nicholas, P. S. Guerrant, R. L., Moore, R. A., Kirschenfeld, P. M. and (1973). Emission of microbial aerosols from sewage Sande, M. A. (1975). Role of toxigenic and invasive treatment plants that use trickling filters. Health Services bacteria in acute diarrhea of childhood. New England Reports, 88, 640-652. Journal of'Medicine, 293, 567-573. Goldshmid, J. (1974). Water quality aspects of ground-water Guy, E. M. and Small, J. A. (1977). Survival of streptococci recharge in Israel. Journal of the American Water Works and coliforms of bovine faecal origin in drainage water and Association, 5, 163-166. soil stored at different temperatures. New Zealand Journal Goncharuk, E. I., Grigoryeva, L. V., Bey, T. V., Shulyak, E. V. of'Agricultural Research, 20, 13-18. and Korchak, G. M. (1970). Removal of intestinal viruses Hagedorn, C., Hansen, D. T. and Simonson, G. H. (1978). and bacteria from sewage by a circulating oxidizing canal. Survival and movement of fecal indicator bacteria in soil Gigiena i Sanitariya, 35, 36-41. under conditions of saturated flow. Journal of Gorbach, S. L., Nahas, L., Lerner, P. 1. and Weinstein, L. Environmental i.ti 7, 55-59. (1967). Studies in intestinal microflora. I. Effects of diet, Hakim, K. E. (1978). Study of Relationship of Microbial age, and periodic sampling on numbers of fecal Indicators to Health Effects at Alexandria Bathing microorganisms in man. Gastroenterology, 53, 845-855. Beaches Progress Report, 1976-1977. Alexandria, Gorden, R. W. and Fliermans, C. B. (1978). Survival and Egypt: High Institute of Public Health. viability of Escherichia coli in a thermally altered reservoir. Hanes, N. B. and Fragala, R. (1967). Effect of seawater 238 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA concentration on survival of indicator bacteria. Journal of Katugampola, D. C. and Assim, T. H. (1958). Coliform the Water Pollution Control Federation, 39, 97-104. organisms in domestic water supplies in Ceylon. Ceylon Hanes, N. B., Sarles, W. B. and Rohlich, G. A. (1964). Journal of Medical Science, 9, 95-101. Dissolved oxygen and survival of coliform organisms and Katzenelson, E., Buium, 1. and Shuval, H. I. (1976). Risk of enterococci. Journal of the American Water Works communicable disease infection associated with waste- Association, 56, 441-446. water irrigation in agricultural settlements. Science, 194, Harper, G. J. and Morton, J. D. (1953). The respiratory 944-946. retention of bacterial aerosols: experiments with radioac- Katzenelson, E. and Teltch, B. (1976). Dispersion of enteric tive spores. Jouirnal of Hygiene, 51, 372-385. bacteria by spray irrigation of wastewater. Journal of thle Hendricks, C. W. (1971). Enteric bacterial metabolism of Water Pollution Control Federation, 48, 710-716. stream sediment eluates. Canadian Journal of Katzenelson, E., Teltch, B. and Shuval, H. 1. (1977). Spray Microbiology, 17, 551-556. irrigation with wastewater: the problem of aerosolization (1972). Enteric bacterial growth rates in river water. and dispersion of enteric microorganisms. Progress in Applied Microbiology, 24, 168-174. Water Technology. 9, 1-ll. Hendricks, D. W., Post, F. J. and Khairnar, D. R. (1979). Kawata, K., Cramer, W. N. and Burge. W. D. (1977). Adsorption of bacteria on soils: experiments, thermody- Composting destroys pathogens. Water and Sewage Wbrks, namic rationale, and application. Water, Air and Soil 124, 76-79. Pollution, 12, 219-232. Keswick, B. H.. Fujioka, R. S., Loh, P. C. and Burbank, N. C. Hoff. J. C. and Becker. R. C. (1969). The accumulation and i1980). Comparative disinfection by bromine chloride and elimination of crude and clarified poliovirus suspensions chlorine of viruses and bacteria in wastewater. Journal of by shellfish. Amiericani Journal of Epidemiology, 90, 53-61. the Water Pollution Control Federation, 52, 2581-2588. Hughes, J. M., Merson, M. H. and Gangarosa, E. J. (1977). Kibbey, H. J., Hagedorn, C. and McCoy, E. L. (1978). Use of The safety of eating shellfish. Journal of' the American fecal streptococci as indicators of pollution in soil. Applied Medical Association, 237, 1980-1981. and Environmental Microbiology, 35, 711-717. Irving, T. E. (1980). Sewage Chlorination and Bacteriai Kinney, E. C., Drummond, D. W. and Hanes, N. B. (1978). Regrowth. Technical Report TR 132. Stevenage, UK: Effects of chlorination on differentiated coliform groups, Water Research Centre. Journal of' the Wuter Pollution Control Federiationz. 50, Jackson, G. B. (1979). Conventional chlorination found 2307-2312. nonfeasible for lagoons. Journ7lal of the Water Pollution Klock, J. W. (19711. Survival of coliform bacteria in Control Federationi, Deeds & Data, 16(1), 9 and 14-16. wastewater treatment lagoons. Journial of' the WIater Jamieson, W., Madri, P. and Claus, G. (1976). Survival of Pollution Control Federation, 43, 2071-2083. certain pathogenic microorganisms in sea water. Koornhof, H. J., Robins-Browne, R. M., Richardson, N. J. Hydrobiologia, 50, 117-121. and Cassel, R. (1979). Etiology of infantile enteritis in Janssen, W. A. (1974). Oysters: retention and excretion of South Africa. Israel Journlal of Medical Sciences, 15, three types of human waterborne disease bacteria. Healtlh 341-347. Laboratory Science, 11, 20-24. Kott, Y., Roze, N.. Sperber, S. and Betzer, N. (1974). Jegathesan, M., Lim Teong Wah, Lim Eng Soon, Ding Su Bacteriophages as viral pollution indicators. Water Har and Lim Boo Liat (1976). Bacterial enteropathogens Researchz, 8, 165 -171. in Malaysian shellfish. Tr opical and Geographical Kudoh, Y., Matsushita, S., Yamada, S., Tsuno, M., Ohta, K., Medicine, 28, 91-95. Kai, A., Sakai, S. and Ohashi, M. (1979). Travelers' Jordan, E. 0. (1926). The changes in bacterial content of diarrhea and enterotoxigenic Escherichia coli a survey in stored normal and typhoid feces. Journal of Infectiou.s 1977-1979 in Tokyo. In Proceedings of' the 15th Joint Diseases, 38, 306-322. US-Japan Cooperative Medical Scienzce Program, June, R. C., Ferguson, W. W. and Worfel, M. T. (1953). Conference on Cholera, pp. 225-236. Bethesda. Md.: Experiments in feeding adult volunteers with Escherichia National Institutes of Health. coli 55, Bs. a coliform organism associated with infant Kudryavtseva. B. M. (1972). An experimental approach to diarrhea. Americant Journal of'Hygiene, 57, 222-236. the establishment of zones of hygienic protection of Kamlet, K. S. (1979). Superchlorination of sewage sludge: underground water sources on the basis of sanitary adding injury to insult? Sludge, 2, 16-18 and 27-31. bacteriological indices. Journal of Hygiene, Epidemiology. Kampelmacher. E. H.. Fonds, A. W. and van Noorle Jansen. L. Microbiology and Immuntology. 16, 503-511. M. (1977). Reduction of Salmonella. E. coli, coliforms and Lance, J. C., Rice, R. C. and Gilbert. R. G. (1980). Renovation faecal streptococci by chlorination of sewage treatment of wastewater by soil columns flooded with primary plant effluents. Water Research, 11, 545--550. effluent. Journal of the Water Pollution Control Federation, Karthegisan, J. and Pugh Thomas, M. (1980). The effect of 52, 381-388. tidal heights on the distribution and abundance of Lee, J. A. and Kean, B. H. (1978). International conference on coliform bacteria in the sediments of two sites in the the diarrhea of travelers. New directions in research. Mersey estuary. International Journal oJ Environmental Journal of Infectious Diseases, 137, 355-369. Studies, 14, 299-308. Lessel, T. and Suess, A. (1978). Hygienization of sewage ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 239 sludge by gamma irradiation, experience with an operating Mehlman, 1. J., Fishbein, M., Gorbach, S. L., Sanders, A. C., pilot plant. Progress in Water Technology, 10, 641-652. Eide, E. L. and Olson, J. C. (1976). Pathogenicity of Loedolff, C. J. (1965). The function of Cladocera in oxidation Escherichia coli recovered from food. Journal of the ponds. In Aduances in Water Pollution Research. 1, ed. Association of'Official Analytical Chemists, 59, 67-80. Jaag, O., pp. 307-325. Oxford: Pergamon. Menon, A. S. and Bedford, W. K. (1973). A Study oJ the Loh, P. C., Fujioka, R. S. and Lau, L. S. (1979). Recovery, Seasonal Ejjects on the Microbiology oJ a Northern Pulp survival and dissemination of human enteric viruses in and Paper Mill Aeration Lagoon. Report No. EPS 4-AR- ocean waters receiving sewage in Hawaii. Water, Air and 73-I. Ottawa: Environmental Protection Service, Soil Pollution, 12, 197-217. Environment Canada. Longley, K. E., Moore, B. E. and Sorber, C. A. (1980). Merson, M. H., Morris, G. K., Sack, D. A., Wells, J. G., Comparison of chlorine and chlorine dioxide as disinfec- Feeley, J. C., Sack, R. B., Creech, W. B., Kapikian, A. Z. and tants. Journal oJ the Water Pollution Control Federation, Gangarosa, E. J. (1976). Travellers' diarrhea in Mexico: a 52, 2098-2105. prospective study of physicians and family members McCambridge, J. and McMeekin, T. A. (1979). Protozoan attending a congress. New England Journal oJ Medicine, predation of Escherichia coli in estuarine waters. Water 294, 1299-1305. Research, 13, 659-663. Metcalf, T. G. (1978). Indicators of viruses in shellfish. In McCoy, E. L. and Hagedorn, C. (1979). Quantitatively Indicators of Viruses in Water and Food, ed. Berg, G., pp. tracing bacterial transport in saturated soil systems. 383-415. Ann Arbor, Mich.: Ann Arbor Science Water, Air and Soil Pollution, 11, 467-479. Publishers. McCoy, E. L. and Ziebell, W. A. (1976). The effects of Mitchell, J. R., Presnell, M. W., Akin, E. W., Cummins, J. M. effluents on groundwater: bacteriological aspects. In and Liu, 0. C. (1966). Accumulation and elimination of Second National Conference on Indiuidual Onsite poliovirus by the Eastern oyster. American Journal of Wastewater Systems, pp. 67-75. Ann Arbor, Mich.: Epidemiology, 84, 40-50. National Sanitation Foundation. Mitchell, R. (1968). Factors affecting the decline of non- McFeters, G. A., Bissonnette, G. K., Jezeski, J. J., Thomson, marine micro-organisms in seawater. Water Research, 2, C. A. and Stuart, D. G. (1974). Comparative survival of 535-543. indicator bacteria and enteric pathogens in well water. Mitchell, R. and Chamberlin, C. (1975). Factors influencing Applied Microbiology, 27, 823-829. the survival of enteric microorganisms in the sea: an McFeters, G. A., Stuart, S. A. and Olson, S. B. (1978). Growth overview. In Proceedings of the International Symposium on of heterotrophic bacteria and algal extracellular products Discharge of Sewagefrom Sea Outfalls, ed. Gameson, A. L. in oligotrophic waters. Applied and Environmental H., pp. 237-251. Oxford: Pergamon. Microbiology, 35, 383-391. (1978). Survival ofindicator organisms. In Indictors of McGarry, M. G. and Stainforth, J., eds. (1978). Compost. Viruses in Water and Food, ed. Berg, G., pp. 15-37. Ann Fertilizer and Biogas Production from Human and Farm Arbor, Mich.: Ann Arbor Science Publishers. Wastes in the People's Republic of China. Ottawa: Mitchell, R. and Yankofsky, S. (1969). Implication of a International Development Research Centre. marine ameba in the decline of Escherichia coli in seawater. Mancini, J. L. (1978). Numerical estimates of coliform Environmental Science and Technology, 3, 574-576. mortality rates under various conditions. Journal of the Moeller, J. R. and Calkins, C. (1980). Bactericidal agents in Water Pollution Control Federation, 50, 2477-2484. wastewater lagoons and lagoon design. Journal of the Mara, D. D. (1976). Sewage Treatment in Hot Climates. Water Pollution Control Federation, 52, 2442-2451. Chichester: John Wiley. Moore, J. L., Perin, D. E. and Maiden, B. G. (1979). Mara, D. D. and Silva, S. A. (1979). Sewage treatment in Estimating the effect of water quality improvement on waste stabilization ponds: recent research in northeast public swimming. Water Resources Research, 15, Brazil. Progress in Water Technology, 11, 341-344. 1323-1328. Marais, G. v. R. (1974). Faccal bacterial kinetics in Moussa, R. S. (1965). Type distribution of coliforms isolated stabilization ponds. Journal of the Environmental from faecal and non-faecal habitats. Indian Journal of Engineering Division, Proceedings of the American Society Medical Research, 53, 629-637. oj'Civil Engineers, 100, 119-139. Munger, S. F., Heyward. A. A. and Dutton, R. T. (1979). A Marzouk, Y., Goyal, S. M. and Gerba, C. P. (1980). survey of the microbiological quality of shellfish on Relationship of viruses and indicator bacteria in water and metropolitan Seattle area beaches. Abstract Q14. wastewater of Israel. Water Research, 14, 1585-1590. Abstracts of the Annual Meeting of'the American Society of' Mata, L. J., Carrillo, C. and Villatoro, E. (1969). Fecal Microbiology. Washington, DC. microflora in healthy persons in a preindustrial region. Myhrstad, J. A. (1979). Disinfection of sewage by ultraviolet Applied Microbiology, 17, 596-602. irradiation. National Institute of Public Health Annals, 2, May, K. R. and Druett, H. A. (1953). The pre-impinger, a 11-16. selective aerosol sampler. British Journal of Industrial Newson, S. W. B. (1972). Microbiology of hospital toilets. Medicine, 10, 142-151. Lancet, 2, 700-703. 240 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Olivieri, V. P., Kawata, K. and Kruse, C. W. (1978). comparison of fluorescein dye and antibiotic resistant Relationship between indicator organisms and selected Escherichia coli as indicators of pollution in groundwater. pathogenic bacteria in urban waterways. Progress in Water Water, Air and Soil Pollution, 11, 93-103. Technology, 10, 361-379. Randall, C. W. and Ledbetter, J. 0. (1966). Bacterial air Oluwande, P. A. (1980). Public health implications of pollution from activated sludge units. American Industrial chemical and bacteriological characteristics of treated Hygienie Association Journal, 27, 506-519. water in Western State of Nigeria. Nigerian Medical Raveendran, O., Gore, P. S. and Unnithan, R. V. (1978). Journal, 7, 86-89. Observations on faecal contamination of Cherai Beach in Osborn, D. W. and Hattingh, W. H. J. (1978). Disinfection of Kerala. Indian Journal of Marine Science, 7, 128-129. sewage sludge: a review. Water South Africa, 4, 169-178. Reneau,R.B.andPettry,D.E. (1975).Movementofcoliform Parhad, N. M. and Rao, N. U. (1974). Effect of pH on survival bacteria from septic tank effluent through selected coastal of Escherichiia coli. Journal of the Water Pollutionz Control plain soils in Virginia. Journal of Environmental Quality, 4, Federation, 46, 980-986. 41-44. Parker. C. D. (1962). Microbiological aspects of lagoon Reneau, R. B.. Pettry. D. E.. Shanholtz. M. I., Graham, S. A. treatment. Journal of the Water Pollution Control and Weston, C. W. (1977). Distribution of total and fecal Federation, 34, 149-161. coliform organisms from septic effluent in selected coastal Parker, D. T., Spendlove, J. C., Bondurant, J. A. and Smith. J. plain soils. Public Health Reports, 92, 251-259. H. (1977). Microbial aerosols from food-processing waste Roller. S. D., Olivieri, V. P. and Kawata. K. (1980). Mode of spray fields. Journal of the Water Pollution Control bacterial inactivation by chlorine dioxide. Water Research, Federation, 49, 2359-2365. 14, 635-641. Petr, T. (1980). Bacterial densities and faecal pollution in the Roper, M. M. and Marshall, K. C. (1979). The Survival of Purari River catchment, Papua New Guinea. In Purari Coliform Bacteria in Saline Sediments. Australian Water River (Wabo) Hydroelectric Schemne Environmental Studies. Resources Council Technical Paper 43. Canberra: Vol II Aquatic Ecology oj the Purari River Catchment, ed. Australian Government Publishing Service. Petr, T., pp. 41-58. Konedobu, Papua New Guinea: Rosenberg, M. L.. Kaplan. J. P., Wachsmuth, 1. K., Wells, J. Department of Minerals and Energy. G., Gangarosa, E. J., Guerrant, R. L. and Sack, D. A. Petrilli, F. L., de Renzi, G. P., Palmerini Morelli, R. and de (1977). Epidemic diarrhea at Crater Lake from en- Flora, S. (1979). Survey of the pollution in a coastal area of terotoxigenic Escherichia coli, a large waterborne out- the Tyrrhenian Sea. Aerial photography. physico-chemical break. Annals of Internal Medicine, 86, 714-718. and microbiological investigations and mutagenic mo- Rudolfs, W., Falk, L. and Ragotzkie, R. A. (1950). Literature nitoring. Water Research, 13, 895-904. review on the occurrence and survival of enteric. Pichot, G. and Barbette, J. (1978). Estimation des taux pathogenic, and relative organisms in soil, water, sewage moyens de disparition des bacteries fecales dans les eaux and sludges, and on vegetation. 1. Bacterial and viral cotieres Belges de la Mer du Nord. Revue Internationale diseases. Sewage and Industrial Wastes, 22, 1261-1281. d'Oceanographie Medicale, 51/52, 115-126. Ryder, R. W., Sack, D. A., Kapikian, A. Z., McLaughlin, J. C.. Pike, E. B. and Carrington, E. G. (1979). The fate of enteric Chakraborty, J., Rahman, A., Merson, M. and Wells, J. bacteria and pathogens during sewage treatment. In (1976). Enterotoxigenic Eschericlhia coli and reovirus-like Biological Indicutors oJ Water Qualilt, eds. James, A. and agent in rural Bangladesh. Lancet. 1, 659-663. Evison, L., pp. 20/1-20/32. Chichester: John Wiley. Sack, D. A., Kaminsky. D. C., Sack, R. B., Itotia, J. N., Arthur. Polprasert, C. and Valencia, L.G. (1981). The inactivation of R. R., Kapikian, A. Z., Orskov, F. and 0rskov, 1. (1978). faecal coliforms and Ascaris ova in faeces by lime. Water Prophylatic doxycycline for travellers' diarrhea: results of Research, 15, 31-36. a prospective double-blind study of Peace Corps Poon, C. P. C. (1968). Viability of long-storaged airborne volunteers in Kenya. New England Journal of Medicine. bacterial aerosols. Journal of the Sanitary Engineering 298, 758-763. Division, American Society of Civil Enginieers, 94, Sack, R. B., Hirschhorn, N., Brownlee, 1., Cash, R. A., 1137-1146. Woodward, W. E. and Sack, D. A. (1975a). Poynter, S. F. B. and Stevens, J. K. (1975). The effects of Enterotoxigenic Escherichia coli associated diarrheal storage on the bacteria of hygienic significance. In Tihe disease in Apache children. News England Medical Journal, Ln ol Storage on Water Quality, pp. 69-90. 292, 1041-1045. Medmenham, UK: Water Research Centre. Sack, R. B., Hirschhorn, N., Woodward, W. E., Sack, D. A. Qasim, S. R. (1978). Treatment of domestic sewage by using and Cash, R. A. (1975b). Antibodies to heat-labile solar distillation and plant culture. Journal of Escherichia coli enterotoxin in Apaches in Whiteriver, Environmental Science and Health, A13, 615-627. Arizona. Injection and Immunity, 12, 1475-1477. Raghavachari, T. N. S. and lyer. P. V. S. (1940). The Sack, R. B., Sack, D. A., Mehlman, I. J., Orskov, F. and occurrence of the Aerogenes group of coliform organisms 0rskov, 1. (1977). Enterotoxigenic Escherichia coli isolated in faeces and its significance in water analysis. Indian from food. Journal of Infectious Diseases, 135, 313-317. Journal of Medical Research, 28, 55-60. Sadovski, A. Y., Fattal, B. and Goldberg, D. (1978). Rahe, T. M., Hagedorn, C. and McCoy, E. L. (1979). A Microbial contamination of vegetables irrigated with ESCHERICHIA COLI AND OTHER BACTERIAL INDICATORS 241 sewage effluent by the drip method. Journal of' Food Abstracts of the Annual Meeting of'the American Societyfor Protection. 41, 336-340. Microbiology. Washington, DC. Sadovski, A. Y., Fattal, B., Goldberg, D., Katzenelson, E. and Sorber, C. A., Bausum, H. T., Schaub, S. A. and Small, M. J. Shuval, H. I. (1978). High levels of microbial con- (1976). A study of bacterial aerosols at a wastewater tamination of vegetables irrigated with wastewater by the irrigation site. Journal of the Water Pollution Control drip method. Applied and Enlvlironmental Microbiology, 36, Federationi, 48, 2367-2379. 824-830. Spencer, H. C., Wells, J. G., Gary. G. W., Sondy, J., Puhr, N. Saleh, F. A. (1980a). Bacteriological quality of Nile Water D. and Feldman, R. A. (1980). Diarrhea in a non- before and after impoundment (1963-1973): a review. hospitalized rural Salvadoran population: the role of Zentralblatt Jaiu Bakteriologie. Parasitenlkunde, enterotoxigenic Eschzerichiia coli and rotavirus. American InJektionskrankheiten und Hygiene, I, 135, 123-129. Journal of Tropical Medicine and Hygiene, 29, 246-253. (1980b). Isolation and enumeration of faecal strepto- Stenquist, R. J., Parker, D. S., Loftin, W. E. and Brenner, R. C. cocci from Nile water (1975-1976). Water Research, 14, (1977). Long-term performance of a coupled trickling 1669-1678. filter-activated sludge plant. Journal of the Water Pollution Sandhu, S. S., Warren, W. J. and Nelson, P. (1979). Control Federation, 49, 2265-2284. Magnitude of pollution indicator organisms in rural Stiles, C. W. and Crohurst, H. R. (1923). The principles potable water. Applied and Environmental Microbiology, underlying the movement of Bacillus coli in groundwater, 37, 744-749. with resulting pollution of wells. Public Health Reports, 38, Savage, J., Chase, T. and MacMillan, J. D. (1973). Population 1350-1353. changes in enteric bacteria and other microorganisms Teitch, B. and Katzcnelson, E. (1978). Airborne entcric during aerobic thermophilic windrow composting. Applied bacteria and viruses from spray irrigation with wastewater. Microbiology, 26, 969-974. Applied and Environmental Microbiology, 35, 290-296. Schaub, S. A. and Sorber, C. A. (1977). Virus and bacteria Tjostem, J. L., Young, J., Hoilien, C. and Elson Iverson, R. removal from wastewater by rapid infiltration through (1977). Bacterial and nitrate contamination of well water soil. Applied and Environmnental Microbiology, 33,609-619. in northeast Iowa. Proceedings of the Iowa Academy of Sebodo, T., Soenarto, Y., Rohde, J. E., Ryan, N. J., Taylor, B. Science, 84, 14-22. J., Luke, R. J. K., Bishop, R. F., Barnes, G. L., Holmes, I. H. Tomkins, A. M., Drasar, B. S., Bradley, A. K. and and Ruck, B. J. (1977). Aetiology of diarrhoea in children Williamson, W. A. (1978). Water supply and nutritional aged less than two years in Central Java. Lancet. 1, status in rural Northern Nigeria. Transactions of the Royal 490-491. Society of Tropical Medicine and Hygiene, 72, 239-243. Shuval, H. I. (1978). Studies on bacterial and viral Tomkins, A. M., Bradley, A. K., Oswald, S. and Drasar, B. S. contamination of the marine environment. Reviue (1981). Diet and the faecal microflora of infants, children Internationale d'Oceanographie Medicale, 50, 43-50. and adults in rural Nigeria and urban UK. Journal of' Shuval, H. I., Cohen, J. and Kolodney, R. (1973). Regrowth of Hygiene, 86, 285-'93. coliforms and fecal coliforms in chlorinated wastewater Train, R. E. (1979). Q,,.d,:, Criteria Jfr Water. London: effluent. Water Researchl, 7, 537-546. Castle House. Silvey, K. G., Abshire, R. L. and Nunez, W. J. (1974). Van der Drift, C., van Seggelen, E._ Stumm, C., Hol, W. and Bacteriology of chlorinated and unchlorinated wastewater Tuinte, J. (1977). Removal of Escherichia coli in wastewater effluents. Journal of the Water Pollution Control by activated sludge. Applied and Environmenital Federation, 46, 2153-2162. Microbiology, 34, 315-319. Slade, J. S. and Edworthy, K. J. (1981). Virology of Van Donsel, D. J., Geldreich, E. E. and Clarke, N. A. (1967). wastewater recharge of the chalk aquifer. II. Microbiology Seasonal variations in survival of indicator bacteria in soil and water quality. In Viruses and Wastewater Treatmenzt, and their contribution to storm-water pollution. Applied eds. Goddard, M. and Butler, M. Oxford: Pergamon. Microbiology, 15, 1362-1370. Slanetz, L. W., Bartley, C. H., Metcalf, T. G. and Nesman, R. Vasconcelos, G. J. and Swartz, R. G. (1976). Survival of (1970). Survival of enteric bacteria and viruses in bacteria in seawater using a diffusion chamber apparatus municipal sewage lagoons. In Proceedings of the Second in situ. Applied and Environmental Microbiology, 31, International Symposium for Waste Treatment Lagoons, 913-920. ed. McKinney, R. E., pp. 132-141. Lawrence, Kansas: Vaughn, J. M., Landry, E. F., Baranosky, L. J., Beckwith, C. University of Kansas. A., Dahl, M. C. and Delihas, N. C. (1978). Survey of human Slanetz, L. W., Bartley, C. H. and Stanley, K. W. (1968). virus occurrence in wastewater-recharged groundwater on Coliforms, fecal streptococci and Salmonella in seawater Long Island. Applied and Environmental Microbiology, 36, and shellfish. Health Laboratory Science, 5, 66-78. 47-51. Small Scale Waste Management Project (1978). Management Vaughn, J. M., Landry, E. F., Thomas, M. Z., Vicale, T. J. and of' Small Waste Flows. Report EPA-600/2-78-173. Penello, W. F. (1979). Survey of human enterovirus Cincinnati, Ohio: US Environmental Protection Agency. occurrence in fresh and marine surface waters on Long Snow, G. E. (1977). The effects of chlorinated wastewater Island. Applied and Environmental Microbiology, 38, effluent on in situ river coliform bacteria. Abstract N60. 290-296. 242 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Viraraghavan, T. (1978). Travel of microorganisms from a eds. James, A. and Evison, L., pp. 13/l-131l8. Chichester: septic tile. Water, Air and Soil Pollution, 9, 355-362. John Wiley. Wehner, J. F. and Wilhelm, R. H. (1956). Boundary Woodbridge, D. D. and Cooper, P. C. (1979). Synergistic conditions of flow reactor. Chemical Engineering Science, effects for irradiation of fecal coliforms. Journal of the 6, 89-93. Water Pollution Control Federation, 51, 2717-2723. Wheater, D. W. F., Mara, D. D., Jawad, L. and Oragui, J. Wyatt, T. D. and Wilson, T. S. (1980). An investigation of the (1980). Pseudomonas aeruginosa and Escherichia coli in bacteriological water quality in two pools disinfected with sewage and fresh water. Water Research, 14, 713-721. ozone. Baths Service and Recreation Management, Wheater, D. W. F., Mara, D. D. and Oragui, J. (1979). Jan./Feb., 22-24. Indicator systems to distinguish sewage from stormwater Yde, M. and de Maeyer-Cleempoel. S. (1980). Faecal run-off and human from animal faecal material. In pollution of Belgian coastal waters. Marine Pollution Biological Indicators of Water Quality, eds. James, A. and Bulletini, 11, 108-110. Evison, L., pp. 21/1-21/27. Chichester: John Wiley. Yeager, C. H. (1929). Well pollution and safe sites for bored- White, G. F., Bradley, D.J. and White, A. U. (1972). Drawers hole latrines. Malayan Medical Journal, 4, 118-125. of Water. Chicago: University of Chicago Press. Zanoni, A. E., Katz, W. J., Carter, H. H. and Whaley, R. C. WHO (1971). International Standards for Drinking Water (1978). An in situ determination of the disappearance of Quality, 3rd ed. Geneva: World Health Organization. coliforms in Lake Michigan. Journal ofthe Water Pollution Williams Smith, H. and Crabb, W. E. (1961). The faecal Control Federation, 50, 321-330. bacterial flora of animals and men: its development in the Zubrzyoki, L. and Spaulding, E. H. (1962). Studies on the young. Journal of Pathology and Bacteriology, 82, 53-66. stability of the normal human fecal flora. Journal of Wood, P. C. (1979). Public health aspects of shellfish from Bacteriology, 83, 968-974. polluted waters. In Biological Indicators of Water Quality, 14 Leptospira and Leptospirosis LEPTOSPIRAS are quite distinct from the other bacteria fever, and brucellosis. In tropical countries it has to be discussed in chapters 12 through 18 in that they are not differentiated from malaria, scrub-typhus, dengue, and normally transmitted from person to person. They sand fly fevers. Such illnesses can only be diagnosed as infect rodents and other animals and occasionally leptospirosis by laboratory tests-isolation of the infect man when he comes into contact with infected organisms in blood culture and serological tests that animal urine. Leptospiras are included here because show a rise in the specific antibody levels. sewer workers are exceptionally exposed to the risk of leptospirosis. Occurrence Leptospiras exist in most countries of the world, but Description of Pathogen and Disease whereas certain serotypes (for example, ictero- haemorrhagiae and canicola) are widespread, others Leptospirosis can be a severe illness, but rarely is it tend to be restricted only to certain regions, where their sufficiently common to constitute a major public natural (reservoir) hosts are found. In most tropical health problem. Good accounts of leptospirosis have areas multiple serotypes are circulating. been published by Alston and Broom (1958) and Although it appears that the incidence of human Turner (1967, 1968, and 1970). leptospirosis is low compared with that of other infectious diseases and that cases tend to be sporadic Identification rather than epidemic, it is likely that in certain parts of the world many cases are being missed because they are Leptospirosis is an infection with bacteria of the misdiagnosed and leptospirosis is not being looked for. genus Leptospira that may take several forms. One of At certain times and under certain circumstances, these forms is Weil's syndrome, which develops in leptospirosis may become a major problem, as it was about 40 percent of cases of infection by the more among the British forces stationed in the jungles and virulent serotypes, notably L. icterohaemorrhagiae.' It swamps of Malaya and Burma, and as it still is among is a severe illness with jaundice, neck stiffness, rice field and sugarcane plantation workers. hepatomegaly, sometimes splenomegaly, hemorrhages in the eyes and skin, albuminuria, and hematuria. It has a high fatality rate unless diagnosed and treated in the infectious agent early stages. However, milder forms of illness can also Bacteria of the genus Leptospira are essentially result from infection by L. icterohaemorrhagiae as well parasites of animals, notably rodents-rats, mice, as by the many other serotypes (over 100) that are voles, and the like. Leptospiras are slender, flexuous, pathogenic to man. In such cases the disease cannot be spiral organisms that are actively motile by means of diagnosed clinically with accuracy because of its internal axial filaments analogous to the external protean nature. Its signs and symptoms may mimic flagella of Gram-negative bacilli. They are approx- many other illnesses such as influenza, septic imately 0.1 micrometers in width and 6-20 micro- meningitis, Q-fever, enteric-like illnesses, glandular meters in length, with bent or hooked ends (see figure 14-1). Some of them are free-living, nonpathogenic, 1. See the subsection "Infectious agent,'' below, for a note on common in fresh water; others are parasites of animals taxonomic nomenclature. and potential pathogens of man. Leptospiras are 243 244 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA effects. It colonizes the kidney tubules, from which it is periodically washed out in the urine. Ad The rat, Rattus norvegicus (brown rat, sewer rat), is the reservoir host of the icterohaemorrhagiae serotype, and any environment where these rats are found is a potential hazard to the men who may work there, should they handle material contaminated with rat urine. Persons who have been infected with ictero- haemorrhagiae include fish workers, butchers, refuse collectors, bricklayers, dock laborers, factory workers, miners, sewer workers, and many others. Any environment that encourages the proliferation of rats is potentially a source of infection with icterohaemnor- v Ji rhhagiae. Domestic animals may also be infected by this serotype, and they transmit the infection to each other and to the people who look after them. Transmission Provided that the external conditions are favorable Figure 14-1. Leptospira iunder scannitng electronmnic- (moist, relatively warm, shaded from the ultraviolet roscopy. The organism is spiral and has bent or hooked light of the sun, not salty, and of a neutral pH). ends. Scale bar = 1 micrometer. (Photo: J. D. Fulton teptospiras can remain viable for a time outside the and D. F. Spooner, National Institute for Medical animal body and are then transmissible to other hosts, Research, London, UK) including man or his domestic animals. The organisms gain access to the body through its contact with the strictly aerobic. They require animal serum or a serum urn-otmaednvomntbwyofcsad urine-contaminated environment by way of cuts and derivative for growth. The optimum temperature for abrasions of the skin or by way of the mucous growth is 28-30sC. membranes of the nose and mouth during immersion Approximately 150 serotypes of pathogenic leptos- in water containing leptospiras. If the new, accidentally piras are recognized. Before 1967 these serotypes were infected host is a human being or an animal of a considered as separate species. Recently the antigeni- different species than the reservoir host a disease state cally distinct types have been classified as serovarieties diffrent In the resero st, ie state (or erotpes of sinle pecis, Lptopirain- may result. In the convalescent stage of the infection, (or serotypes) of a single species, Leptospira in- man and these animals may become urinary excretors terrogans. For example, an organism referred to as L. of leptospras although, unlike the reservoir hosts, they canicola in the older literature would now be called L. Free-living tend to be temporary rather than chronic shedders. snterrophansc sertovrar arernot clansicold as serovars Dogs, cattle (including milking cows), pigs, and horses saprotyphyticftheptspecirs areno ciflexasd ase serovas have all been incriminated in the spread of the disease (serotypes) of the species L. blfiex-a and are commonly vateruie a-omntasiso srr n isolated from surface waters, sediments, and soils va thelr urline. Man-to-man transmission IS rare and (Henry and Johnson 1978). usually lmited to direct contact (for example, by The first pathogenic serotype to be isolated from venereal or transplacental routes), but an exceptional human teptospirosis was named icterohaemorrhagiae. case from Vietnam has been reported (Spinu and others 1963) and is discussed below. It IS one of the more virulent of the leptospiral ohr 93 n sdsusdblw Ierotypis one of the moe vrulenbt nof the onle usp Although it is not possible to determine the infective serotypes and IS the main cause (but not the only cause) doefviuntepsirsnma,xeietsn of the severe form of the disease, Weil's syndrome. dose of virulent leptospiras in man experiments on Many different serotypes pathogenic to man and guinea pigs have indicated that the icterohaenmor- rhagiae serotypes (derived directly from an infected animals have since been reported. guinea pig) may have a lethal dose, and consequently an infective dose, as low as 1 organism. Reservoirs Each serotype of Leptospira has its own preferred Incuibation period host (mainly rodents) in which it exists as a commensal Symptoms develop after a period ranging from 2 to bacterium without causing any apparent harmful 14 days, with an average of 7-8 days. LEPTOSPIRA AND LEPTOSPIROSIS 245 Period of communicabilitv leptospiras subsequently shown to be present in the The length of time a patient may be considered to be slime. These men frequently sustained abrasions and capable of communicating leptospiras to other cuts on the hands. The flushers were less likely to individuals within his environment depends on te .sustain abrasions of the skin. They may, however, have indiiduas wthinhisenvionmnt dpens onthe become infected through the mucous membranes of the time he carries the organism in the kidney tubules. alimentaryeorerespiratoryhractcbystouchingethefmout Unlike some animal hosts that may remain carriers for alimentary or respiratory tract by touching the mouth the whole of their life span, humans rarely shed and nose during work. Virulent strains of leptospiras in their urine for longer than 4-6 weeks cterohaemorrhagiae were isolated from sewer rats, from the onset of infection (see, for instance, Ido and caught in sewers in eight different parts of London, and others 1917). also from slime taken from the floor of the sewer near where the first patient (the fatal case) had been working and from the outlet of a house drain into another sewer. Resistanice The isolation of virulent leptospiras from sewers recalls the isolation of icterohaemorrhagiae serotype from All known vertebrate animals are susceptible to slime in a coal mine recorded in 1927 (Buchanan 1927). leptospiral infection, and there is no known example of Johnson, Brown and Derrick (1937) recorded the first natural resistance. Acquired immunity may help to three cases of classical Weil's disease in Australia. control the incidence of clinical disease in communities Cabelli (1978) stated that leptospirosis has been living and working in close proximity to sources of reported with increasing frequency in the USA over the infection. This applies especially to rural communities. past five decades and that many cases are no longer related to occupational exposure but to contact with soil or water contaminated by urine. Swimming or wading in small ponds or creeks, recently used by cattle Many of the accounts of leptospirosis record or receiving run-off from nearby pastures, is a common outbreaks of infection among groups of workers in setting for infection. In 1975, 119 cases of leptospirosis developed countries who have been occupationally were reported in the USA and 36 (29 percent) were exposed to animal urine. For instance, Fairley (1934) attributed to contact with water containing cattle made the first report of a fatal case of leptospiral urine. Diesch and McCullouch (1966) isolated jaundice in a sewer worker in Britain. The patient had serotype pomona from bathing water implicated in an been working in a London sewer for only 3 weeks outbreak of 15 human cases of pomona leptospirosis in before becoming infected. A serological investigation Iowa (USA) in 1964; these authors induced leptospiral revealed that eight other sewer workers who had infections by inoculating guinea pigs with the suspect suffered from jaundice had also been infected by the water (see also Gillespie and Ryno 1963). same leptospiral serotype (icterohaemorrhagiae), and In 1977, 86 cases of leptospirosis were reported in the five other cases of leptospiral jaundice in London sewer USA, of which 69 percent were males, and there were workers were subsequently diagnosed. Alston (1935) four deaths. The most probable sources of infection described three of them. The first was a man, age 52, were livestock, domestic pets, and contaminated water. employed intermittently for 5 years as a flusher; the Only 26 percent of cases could be linked to particular second was a man 35 years old who had been employed vocational activities; of these, farmers were at the for 3 years, also as a flusher; the third, a fatal case, was a greatest risk (Centers for Disease Control 1979). The man 52 years old employed relaying sewers. He worked association between leptospirosis and farming in in old open trenches and in sewers that contained much developed countries is further highlighted by the fact slime and silt. He cut a finger on a broken drain pipe. that 42 percent of leptospirosis cases in the UK in The wound was dressed, and he went on working until 1979-80 were farmers (Coghlan 1981). his illness occurred about 2 weeks later. An Detailed accounts of leptospirosis epidemiology in investigation into the length of service of the men developing countries are few. The pattern of infection involved in these cases showed that it was not dFnly normally depends upon the interaction between man recent recruits who were liable to infection. It occurred and infected animals in a particular environment. in men who had worked in sewers for a few months to 5 Willis and Wannan (1966) found leptospiral antibodies years or more. Infection occurred among those who in the blood of between 31 and 79 percent of people in worked as building laborers as well as among sewer six villages in different parts of Papua New Guinea. flushers. Laborers who chiseled out and handled slime- Antibody prevalence rose with age and was similar in covered brickwork in sewers were in direct contact with males and females. Antibodies, to the same leptospiral 246 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA serogroups as were found in humans, were also found employed in two different forest sites, cutting down in rats, dogs, and pigs. The authors noted that in Papua trees and bringing them down to the beds of several New Guinea the daily pattern of village life brings most streams, where a third group of 80 men with a team of individuals into close contact with these animals. Thus, buffaloes had the task of dragging the logs downstream high antibody prevalence is not associated with a and across marshland to the place where the logs were particular sex or occupation. By contrast, Damude and stacked before being loaded onto lorries for further others (1979) found that 43 percent of sanitation transport. Cases of leptospirosis occurred among workers and 39 percent of sugarcane workers in soldiers in this third group and among men from the Barbados had antibodies to leptospiras and that this other two teams who were drafted to do the same work. antibody prevalence was significantly higher than that No cases developed among the soldiers felling trees. for all other occupations studied. Further, 74 percent of The pH of the mud and water was 7-7.2, and the the 215 reported cases of human leptospirosis atmospheric shade temperature 22-26°C-conditions occurring on Barbados during 1968-74 were males. favorable to the survival of leptospiras. Leptospiras Caldas and Sampaio (1979) reported on leptospirosis inoculated into samples of water taken from the in Salvador (Bahia, Brazil) during 1975. The highest streams remained viable in the laboratory for 2-5 days. incidence occurred during the rainy season, especially There was no evidence that either the buffaloes or April and May, and possible sources of infection were rodents in the area were carriers of the infecting strains sewage, rats, water, dogs, mud, and garbage-in that of Leptospira. The inability of the investigators to find order of frequency. an animal reservoir of infection led to the conclusion The operation of foreign armies in tropical areas has that the epidemic had been spread by person-to-person stimulated important research on a number of tropical transmission. Soldiers urinated directly onto the infections for over a century. The study of leptospirosis waterlogged track down which the logs were dragged in Malaysia during the 1950s and 1960s is a relatively and around the loading platforms where the ground recent case in point (Alexander and others 1975; Baker was equally boggy. The soldiers, clad only in shorts, 1965; Baker and Baker 1970; Gordon Smith and others worked barefoot and were liable to sustain scratches 1961; McCrumb and others 1957). About 40 percent of and abrasions of the skin, and these small wounds nonmalarial fever among foreign troops was due to allowed the ready entry of leptospiras into the body. leptospirosis. Infection was strongly associated with The prolonged period of leptospiruria (up to 97 days) jungle maneuvers, and an average case rate of about I shown by some of the patients was thought to be due to per battalion per day of jungle duty was reported. The the near normal pH of the urine (pH 6.2-7.2). a result of primary rain forests of Malaysia were found to be a their predominantly vegetarian diet. hyperendemic focus of leptospirosis. Infection of wild and domestic animals was common, and rats were implicated as the reservoir of greatest importance in the Control Measures epidemiology of human infection. Pathogenic lepto- spiras (serotypes of L. interrogans) were readily isolated Both individual and environmental approaches to from stagnant and swamp waters in the jungle and also leptospirosis control are employed, although in from streams, especially following periods of rain; soil general environmental approaches are more effective. near the stream banks, presumably contaminated by animal urine, frequently contained pathogenic lepto- Indi. dual spiras, and it was thought that these were being washed into the streams during rain. Persons who are known to have been at risk through A report from Vietnam (Spinu and others 1963) tells contact with material contaminated with the urine of a different and unusual story. In Vietnam, as elsewhere, infected animals should be given a course of penicillin, cases of human leptospirosis tend to occur sporadi- 2 mega-units per day for 5 days, administered cally, usually on the plains among workers in the intramuscularly. No special prophylactic drugs are flooded rice fields, where there is a great diversity of available for leptospirosis. Avoidance of contact with rodent species as well as domestic animals to act as the any material containing animal urine (especially rat reservoir hosts for the various serovars that are urine) will greatly reduce the risk of infection. Cuts and responsible for human infection. During 1959, abrasions should be covered and protective clothing however, an epidemic amounting to 121 cases occurred worn. among 240 soldiers working in the jungle territory of In high-risk occupations, vaccination has proved to northeast Vietnam. Two groups of 80 soldiers were be effective. It is necessary to prepare the vaccine from LEPTOSPIRA AND LEPTOSPIROSIS 247 strains prevalent in the area, since the level of cross- Chang, Buckingham and Taylor (1948) also found protection afforded by one serotype may not be that survival in water was greatly reduced by high or adequate for another. Undesirable side effects have low pH and by salinity. In tap water without bacterial been reported, but these have been minimized by the contamination, the leptospiras remained viable for use of vaccines prepared by methods similar to that of over 4 weeks at neutral pH, provided that some Babudieri (1962). nutrients were present. At pH 5 the survival time was reduced to less than 2 days. High pH values were also detrimental. Leptospiras survived for only 18-20 hours in seawater. The hostility of salinity to leptospiras is To avoid direct transmission of leptospiras con- confirmed by the work of Jamieson, Madri and Claus tained in animal urine, working premises should be (1976). At a range of salinities (0.5, 2.0, and 3.5 percent) made rat-proof: refuse and food waste should not be and temperatures (4, 25, and 37°C), serotype pomona left lying around to attract rodents, dogs, foxes, and survived for less than 24 hours. other scavengers. Chlorination of water supplies will The addition of nutrients to sterile water enhances prevent transmission by this route. the survival of leptospiras. In sterile tap water plus 1 Human urine is an uncommon source of infection percent tryptose, survival was up to 50 days, whereas because prevalence of human infection is relatively low the addition of 0.1 percent horse serum increased the and leptospiras do not multiply or survive for long in survival time still further to 102 days. However, in the urine. Leptospirosis is not an intestinal infection, and presence of other bacteria the addition of nutrients had the organisms are not likely to be present in the feces. the opposite effect. By favoring the multiplication of Workers in occupations likely to bring them into the other bacteria, addition of nutrient reduced the contact with human or animal urine should be survival of the leptospiras to approximately 40 hours encouraged to wear protective clothing, rubber boots, (Chang, Buckingham and Taylor 1948). and gloves. This applies especially to anyone employed Spinu and others (1963) reported that leptospiras to remove night soil, especially urine, manually. survived for 2-5 days in stream water at 22-26°C. Diesch (1971) recorded a 3-day survival period for leptospiras in stream water and well water. Occurrence and Survival in the Noguchi (1918) reported that in unpolluted water, Environment such as drinking water, leptospiras (serotype ictero- haemorrhagiae) did not remain infectious for longer Leptospiras that infect animals may be found in the than one week. Further experiments proved that environment where animal urine is present, especially leptospiras will not grow or survive for long in highly in water, mud, slime, or soil. contaminated water, such as polluted river water, sewage, or stagnant cesspools. They invariably In water and sewage disappeared in 48 hours. Noguchi tested the survival time of icterohaemorrhagiae in culture medium to Chang, Buckingham and Taylor (1948) found that which various species of aerobic bacteria had been the survival of L. icterohaemorrhagiae in water was added. He showed that bacilli of intestinal origin were heavily dependent on the temperature and the level of extremely antagonistic to the growth of the leptospiras. bacterial contamination. In river water, the leptospiras In summary (see also the appendixes of Feachem survived for 8-9 days at 5-6°C, but at 20-27°C they and others 1980), leptospiras in clean, sterile water at survived for only 5-6 days, and at 31-32°C their life cool temperatures may survive for up to 20 days, and span was reduced to 3-4 days. In tap water containing they may grow and survive for 100 days in the presence 10 per cent human sewage they survived for 6-7 days at of suitable nutrients. However, in water with a rich 5-6°C, 3-4 days at 25-27°C, and 2-3 days at 31-32°C. bacterial flora and at warm temperatures, precisely the At atmospheric temperature, survival times were environment in which leptospiras are likely to be found 18-20 days in sterile tap water, 10-12 days in tap water after being shed from an infected animal in the tropics, with added mixed bacterial flora, and only 12-14 hours survival times are probably between 1 and 5 days. in undiluted sewage. When the sewage was aerated, however, the leptospiras survived for 2-3 days, In urine indicating that the adverse effect of heavy bacterial growth may be due to anaerobic conditions and to a Leptospiras are shed in the urine, and therefore lowered pH value. survival in urine is an important determinant of the risk 248 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA of new infections, especially in excreta disposal systems conditions was 15 days, with preservation of their such as the Vietnamese double-vault latrine, which pathogenic properties for at least 5 days. disposes of urine separately from feces. Noguchi (1918) added serotype icterohaemorrhagiae to normal human urine and found that it survived for less than 24 hours Inactivation by Sewage Treatment due to the acidity. When the urine was neutralized Processes or made slightly alkaline they survived for 24 hours but not for 48 hours. However, when nutrients were added Chang, Buckingham and Taylor (1948) conducted in the form of rabbit serum plasma to neutral or experiments to determine the resistance of leptospiras slightly alkaline urine, growth occurred for appro- to halogen compounds and synthetic detergents and ximately 10 days. Highly alkaline conditions were as showed that leptospiras are more sensitive to chlorine detrimental to leptospiras as was acidity. than are the enteric bacteria. Synthetic detergents that are cationic were shown to be highly leptospiricidal, whereas the anionic detergents were inactive except at Injeces an7d night soil high dosage. Leptospiras are not passed in the feces of infected Diesch (1971) seeded a laboratory model oxidation animals but will be mixed with feces in most excreta ditch with a virulent strain of serotype pomona to disposal systems in which urine and feces are treated simulate the shedding of leptospiras by beef cattle. together. Noguchi (1918) showed that leptospiras Leptospiras were recovered for at least 61 days. Diesch would not survive for longer than 24 hours in an concluded that an oxidation ditch containing cattle emulsion of feces, either normal or from jaundiced manure is an adequate environment for the survival of patients, with or without added nutrients. This was leptospiras. If sludge or effluent from such a ditch is thought to be due to bacterial contaminants that used to fertilize land, or if effluents are discharged to outgrew the leptospiras, since in sterile fecal material rivers, there is clearly a risk of leptospiral transmission with added nutrients leptospiras survived and re- to men and other animals. mained virulent to guinea pigs for 4 days. Diesch (1971) Diesch (1971) also reported a 5-day survival in the found that serotype pomona survived for up to 5 days in effluent, and a 4-day survival in the sludge, from a cattle liquid cattle manure. manure settling chamber. When compared with the 61- day survival time in the oxidation ditch, these results In soil highlight the importance of oxygen to the survival of leptospiras. Similarly, McGarry and Stainforth (1978) Noguchi (1918) added leptospiras to samples of soil reported Chinese data that leptospiras survive for less rich in organic matter and neutral in pH. The than 30 hours in the rich anaerobic fecal liquor of a organisms were not detected after 72 hours because of biogas plant. bacterial overgrowth. The more vigorous the growth of Processes with short retention times and involving bacteria, the less able were the leptospiras to survive. aeration (for example, trickling filters. activated sludge. Karaseva, Chernukha and Piskunova (1973) con- oxidation ditches) cannot guarantee the destruction of taminated measured areas of soil with urine of voles leptospiras. However, if sewage is held for a week or shown to be carriers of leptospiras belonging to sero- more, as in waste stabilization lagoons, leptospiras will groups Grippotyphosa or Hebdomadis. It was found not survive. Any anaerobic process, such as a septic that the shortest survival time occurred in areas where tank, will also rapidly destroy leptospiras. the moisture content was low (9.5-16.5 percent), where there was little shade, and where the pH was 5.5. Under these conditions the leptospiras survived for only 6-12 Inactivation by Night Soil and Sludge hours. In marshy areas where the moisture content was Treatment Processes high (40-60 percent) and the pH 6.9-7.4, leptospiras were seen actively motile for 4-7 days. In deep shade Most night soil and sludge treatment processes are provided by reeds on the shore of a lake, the survival anaerobic and will rapidly destroy leptospiras. Diesch time was 15 days. In one experiment a leptospirosis- (1971) reported a 4-day survival for serotype pomona in freevolewas infected with Grippotyphosaserogroup by a cattle manure sludge. However, under many inoculation with washings from soil contaminated with anaerobic conditions survival times are unlikely to infected vole urine 5 days before. Thus, the survival exceed 2 days, and there may well be differences among time of pathogenic leptospiras in soil under favorable the survival characteristics of the different serotypes (for LEPTOSPIRA AND LEPTOSPIROSIS 249 instance, serotype pomona may survive for longer than pathogenic leptospires from waters used for recreation. icterohaemorrhagiae). Public Health Reports, 81, 299-304. Leptospiras are sensitive to heat and will be rapidly Fairley, N. H. (1934). Weil's disease among sewer workers in inactivated by thermophilic sludge treatment pro- London. British Medical Journal, 2, 10-14. cesses. Chang, Buckingham and Taylor (1948) Feachem, R. G. A., Bradley, D. J., Garelick, H. and Mara, D. recorded the following thermal death points in distilled D. (1980). Health Aspects of Excreta and Sullage water: 30 minutes at 45°C, 10 minutes at 50°C 10 Management: A State-of:the-Art Review. Appropriate seconds a6Technology for Water Supply and Sanitation, vol. 3, seconds at 60°C, and <10 seconds at 70°C. Washington, DC: The World Bank, Transportation. Water and Telecommunications Department. Gillespie, R. W. H. and Ryno, J. (1963). Epidemiology of Literature Cited leptospirosis. American Journal of Public Health, 53, 950-955. Alexander, A. D., Evans, L. B., Baker, M. F., Baker, H. J., Gordon Smith, C. E., Turner, L. H., Harrison, J. L. and Ellison, D. and Marriapan, M. (1975). Pathogenic Broom, J. C. (1961). Animal leptospirosis in Malaya. I. leptospiras isolated from Malaysian surface waters. Methods, zoogeographical background and broad ana- Applied Microbiology, 29, 30-33. lysis of results. Bulletin of the World Health Organization., Alston, J. M. (1935). Leptospiral jaundice among sewer- 24, 5-21. workers. Lancet, 1, 806-809. Henry, R. A. and Johnson, R. C. (1978). Distribution of the Alston, J. M. and Broom, J. C. (1958). Leptospirosis in Man genus Leptospira in soil and water. Applied and and Animals. Edinburgh: E. & S. Livingstone. Environmental Microbiology, 35, 492-499. Babudieri, B. (1962). The prevention of leptospirosis Ido, Y., Hoki, R., Ito, H. and Wani, H. (1917). The rat as a infection. Scientific Reports of lInstituto Superiore di Sanita, carrier of Spirochaeta icterohaemorrhagiae, the causative 2, 208-221. agent of Weirs disease (Spirochaetosis icterohaemor- Baker, H. J. (1965). Leptospirosis in Malaysia. Military rhagica). Journal of Experimental Medicine, 26, 341-353. Medicine, 130, 1101-1102. Jamieson, W., Madri, P. and Claus, G. (1976). Survival of Baker, M. F. and Baker, H. J. (1970). Pathogenic Leptospira certain pathogenic microorganisms in sea water. in Malaysian surface waters. I. A method of survey for Hydrobiologia, 50, 117-121. Leptospira in natural waters and soils. American Journal of Johnson, D. W., Brown, H. E. and Derrick, E. H. (1937). Tropical Medicine and Hygiene, 19, 485-492. Weil's disease in Brisbane. Medical Journal of Australia, 1, Buchanan, G. (1927). Spirochaetal Jaundice. Medical 811-818. Research Council Special Report Series no. 113. London: Karaseva, E. V., Chernukha, Y. G. and Piskunova, L. A. Medical Research Council. (1973). Results of studying the time of survival of Cabelli, V. J. (1978). Swimming associated disease outbreaks. pathogenic leptospira under natural conditions. Journal of Journal of the Water Pollution Control Federation, 50, Hygiene, Epidemiology, Microbiology and Immunology, 17, 1374-1377. 339-345. Caldas, E. M. and Sampaio, M. B. (1979). Leptospirosis in McCrumb, F. R., Stockard, J. L., Robinson, C. R., Turner, L. the city of Salvador, Bahia, Brazil: a case-control H., Levis, D. G.. Maisey, C. W., Kelleher, M. F.. Gleiser, C. seroepidemiologic survey. International Journal of A. and Smadel, J. E. (1957). Leptospirosis in Malaya. I. Zoonoses, 6, 85-96. Sporadic cases among military and civilian personnel. CentersforDiseaseControl(t979).LeptospirosisSurveillance, American Journal of Tropical Medicine and Hygiene, 6, Annual Summary, 1977. Atlanta, Georgia. 238-256. Chang, S. L., Buckingham, M. and Taylor, M. P. (1948). McGarry, M. and Stainforth, J. eds. (1978). Compost, Studies on Leptospira icterohaemorrhagiae. IV. Survival in Fertilizer and Biogas Production from Human and Farm water and sewage: destruction in water by halogen Wastes in the People's Republic of China. Ottawa: compounds, synthetic detergents and heat. Journal of International Development Research Center. Infectious Diseases, 82, 256-266. Noguchi, H. (1918). The survival of Leptospira (Spirochaeta) Coghlan, J. D. (1981). Leptospirosis in man, British Isles, icterohaemorrhagiae in nature: observations concerning 1979-80. British Medical Journal. 282, 2066. microchemical reactions and intermediary hosts. Journal Damude, D. F., Jones, C. J., White, H. St. C. and Myers, D. M. of Experimental Medicine, 27, 609-625. (1979). The problem of human leptospirosis in Barbados. Spinu, I., Topciu, V., Trinh Thi Hang Quy, Vo Van Hung, Transactions of the Royal Society of Tropical Medicine and Nguyen Sy Quoc, Chu Xuan Luong, Lu Vam Tuyen and Hygiene, 73, 169-177. Nguyen Van An (1963). Man as a reservoir of infection in Diesch, S. L. (1971). Survival of leptospires in cattle manure. an epidemic of leptospirosis occurring in the jungle. Journal of the American Veterinary Medical Association, Archives Roumaines de Pathologie Experimentale et de 159, 1513-1517. Microbiologie, 22, 1081-1100. Diesch, S. L. and McCullouch, W. F. (1966). Isolation of Turner, L. H. (1967). Leptospirosis. 1. Transactions of the 25) ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Royal Society' of Tropical Medicine and Hygiene, 61, Society of Tropical Medicine and Hygiene, 64, 623-646. 842-855. Willis, M. F. and Walnan, J. S. (1966). Some aspects of the -- (1968). Leptospirosis. II. Trantsactionis of the Royal epidemiology of leptospirosis in New Guinea. MWedical Society of Tropical Medicine and Hvgiene, 62, 880-899. Journial of Australia., 1, 129-136. - (1970). Leptospirosis. III. Transactions of the Royal 15 Salmonella, Enteric Fevers, and Salmonelloses SALMONELLA bacteria are a cause of diarrhea, and less associated mainly with particular serotypes. but commonly enteric fever, throughout the world. They especially in people with impaired resistance to are distinct from most of the other major bacterial and infection-includes pyogenic lesions of internal or- viral agents of diarrhea (see chapters 11, 13, 16, and 17) gans. The salmonellae involved include S. paratyphi C in that, with the exception of the typhoid and (also designated S. hirschfeldii), S. enteritidis var. chaco, paratyphoid bacteria, they commonly infect many S. sendai, S. dublin, S. typlziinurium, and S. cholerae-suis. species of mammals, birds, reptiles, and other animals. Most other serotypes predominantly give rise to acute Human infections are frequently associated with gastroenteritis, but many Salmtionella infections are contact with animal feces or ingestion of contaminated symptomless. animal products. For convenience in this chapter, the septicemic syndrome seen most typically in typhoid will be referred to as enteric fever, and the primarily Description of Pathogens and Diseases gastrointestinal pattern of infection as salmonellosis. Diagnosis in cases of gastroenteritis is by isolation of Salmnonella bacteria, and the infections they cause, the bacteria from feces or rectal swab, but in the first are well described in a voluminous medical and week of enteric fever isolation of the bacteria is more veterinary literature. Only a brief summary is given likely from blood culture, and only later are the here. organisms regularly found in the feces. In enteric fever there is commonly a rise in agglutinating antibodies during the course of infection. This is the basis of the Widal reaction as a method of diagnosis in the absence Salmonellosis is any infection with bacteria of the of bacteriological facilities. A positive reaction should genus Salmonella. In man, most of the many serotypes be based on a fourfold or higher rise in the titer of of Salmonella give rise to a transient intestinal infection antibodies, since past exposure or vaccination may have manifested as acute gastroenteritis with diarrhea and led to preexisting antibodies, but even then the test is abdominal cramps. Some of the bacteria may unreliable because as many as half of all cases may fail to transiently be found in the blood, and there may be demonstrate a fourfold rise in antibody titer. fever, nausea, and vomiting as additional symptoms. But in infections with some serotypes, particularly S. Occurrence typhi' (the causative organism of typhoid fever), S. paratyphi A, and S. paratyphi B (also designated S. Salmonellae are found world-wide but the pattern of schottmuelleri). the bacteria invade the tissues and common serotypes varies considerably from region to produce a septicemia with a high temperature rather region. Some serotypes, for instance S. typhi and S. than diarrhea. This is known as enteric fever. Other tvphimurium, are found in many parts of the world, salmonellae may sometimes give rise to a disease whereas others have a very localized occurrence. In all resembling typhoid, and a third syndrome-again countries a few serotypes are responsible for most reported human and animal infections, and many other serotypes are found rarely. In many developed 1. See the subsection "Infectious agents". below, for a note on countries S. typhi is now rare, and most of the cases that taxonomic nomenclature. do occur are contracted elsewhere. 251 252 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA -l l l _In an attempt to simplify the situation, Edwards and Ewing (1972) proposed that only three species of - ~~Salmtonella should be recognized: S. typhzi (one serotype), S. cholerae-suis (one serotype). and S. -i i! _ ,enteritidis (around 2,000 serotvpes). Following this schema, all serotypes except S. typhli and S. cliolerae- suis should be designated S. enteritidis serotype (table 15-1). S. arlzonae was considered to be a separate genus (Ari-ona) rather than a subgenus of Salmoniella. r- -- _ X # j A similar reform was proposed by Cowan and Steel (1974). save that S. ,I .ntTh,a. was the name given to l | f the aggregate species. This move towards a reduced - number of species is reflected in the approved list of -f > g v " - ^ - , , bacterial names (Skerman, McGowan and Sneath * q8 s -^ , 1980): S. cholerae-suis and S. tvphi retain their specific status; S. tvphimurium is retained because of the frequency of its occurrence; S. enteritidis is the aggregate species and S. arizonae consists ofmembers ofsubgenus 111 w w ~~~~~~~~~~~~~~~III. In this book we have adhered to the system of Figure 15-1. Salmonella enteritidis under sc-anning nomenclature described in the 8th edition of Bergy's electronmicroscopy. Colonization of the small intestine Manual, except that we have continued to use the of a rat. Scale bar = 3 micrometers. (Photo: C. D. names S. paratypphi B and S. paratyphi C, since they are Garland, Department of Agricultural Science, more familiar to medical microbiologists. University of Tasmania, Hobart, Australia) Reseruoirs InJictious agents Salmonellae are primarily pathogens of animals, The genus Salmonella is a member of the family which provide important reservoirs for the infections of Enterobacteriaceae and is distinguished from other so- man other than enteric fever. Person-to-person called genera of Enterobacteriaceae primarily on transmission also occurs, and the relative importance biochemical criteria. For example, unlike most E. coli (chater 3), almoellastrans tpicaly d not Table 15-1. Variations inl the nomenclature of some (chapter 13), Salmonella strains typically do not important types of Salmonella ferment lactose. Salmonellae are nonsporulating, Gram-negative, motile, noncapsulate rods (0.5 by 2-4 micrometers) with peritrichous flagella (see figure 15- Bergv s e.unual Edwards and Ewing (1972 1). They are facultative anaerobes. In 1934 it was agreed that each new antigenically Subgenus i (numerous named serotvpes) distinct isolate of Salmonella should be assigned a s. typhi S. tvphi specific Linnaean epithet, often according to the place S. cholerae-suis S. cholerae-stuis at which it was first isolated. This led, however, to an S. enteritidis S. enteritidis serotvpe enteritidis unhelpful proliferation of names and, at the time of S. . .. S. enteritidis serotype writing there are around 2,000 named serotypes. Not *S hirschfjldii (paratiphi C) S. enteritidis serotype paratyvphi C S. paratyphi A S. enteritidis serotype paratyphi A all the serotypes listed in the 8th edition of Bergy's s. schottmuelleri (paratyphi B) S. enteritidis serotype paratyphi B Mantual (1974) have been given names, and the practice s. tvphimuriniu S. enteritidis serotype tyjphimurium has been discontinued. Subgenus i1 (numerous named serotypes) The genus Salmonella can be sub-divided on S. salamae S. enteritidis serotvpe dar es biochemical grounds into four subgenera: only salaam subgenus I is common in human disease. Subgenera L Subgenus ii (numerous unnamed sero[ypes) II, and IV include many named serotypes, whereas s. arizonae Ari0ona hinsihaxii subgenus III contains only the named species. S. Suibgenuis iv (numerous named serotypes) arizonae, although many unnamed serotypes have been S. houtenae S. enteritidis serotype houten described (table 15-1). SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 253 of the human and nonhuman reservoirs depends upon 1976; Bartlett, Trust and Lior 1977; Lamm and others the dietary, agricultural, and sanitary situation in a 1972). It has becn suggcsted that thc decrease in human particular community. infection with S. java, S. litclield, and S. urbana in A few Salmonella serotypes are almost species Canada since 1975 has been due to the government specific. Most importantly, S. typhi is a pathogen of prohibition of the importation of turtles, which were man, and therefore the source of infection is the human popular as pets (D'Aoust and Lior 1978). In 1975 the case or carrier. S. paratyphi A, B, and C and S. sendai interstate transport of pet turtles became illegal in the also have their reservoirs primarily in man, although USA (MMWR 1975). Among the arthropods, fleas, infections of other animals have been reported. ticks, lice, cockroaches, and houseflies may harbor Salmonellae are commonly isolated from poultry, salmonellae. especially chickens, turkeys, and ducks (Goyal and Nonhuman isolations of Salmonella in England and Singh 1970), and from livestock such as pigs, cows, Wales during 1968-74 were reviewed by Sojka and sheep, and horses (Baker 1970). The prevalence of others (1977). Of a total of 23,609 incidents of infection among these potiltry and farm animals is Salmonella infection, 86 percent were in cattle, 7.4 especially high under some systems of intensive indoor percent in poultry and other birds, 2.9 percent in sheep, farming or where contaminated foodstuffs (especially 2.4 percent in pigs, and 1.3 percent in other species, fish meal and bone meal) are used (Al-Hindawi and especially horses, dogs, mink, guinea pigs, and cats. Taha 1979; Joint Working Party 1965; Lee 1974). In These figures do not reflect the relative incidence of the UK and the USA between 15 and 50 percent of salmonellosis among various species but rather the dressed poultry in retail stores may be contaminated by commercial importance of certain farm animals and Salmonella. Other domestic animals and pets (for the policies of veterinary laboratories. Although 153 instance, cats, dogs, mice, guinea pigs, and hamsters) serotypes were isolated, 88 percent of incidents were are frequently infected. Both rats and mice that live in due to S. dublin and S. typhimurium. Other common close proximity to human communities may be serotypes, in decreasing order of importance, were S. infected. Their carrier rate may sometimes rise above cholerae-suis (almost entirely restricted to pigs), S. 10 percent, which is in contrast to the very low abortus-ouis (entirely restricted to sheep), S. newport, S. prevalence observed in surveys of other wild mammals agona, S. tirchow, S. anatum, S. enteritidis, and S. that do not appear to constitute a reservoir of infection montev,ideo. for man or domestic animals (Jones and Twigg 1976). Gulls, pigeons, and doves have been implicated as .s . major reservoirs of salmonellae, but other wild birds are more rarely infected. Jones, Smith and Watson The transmission of typhoid fever was partly (1978) isolated salmonellae from 62 percent of samples elucidated before the bacteriological era by William of gull droppings from a large gullery in northwestern Budd (1856, 1873). He showed that it was spread by England, whereas Plant (1978) isolated Salmonella contagion, that infective material was excreted in the from only 0.17 percent 1/599) of wild birds examined feces, and that the disease could be spread by the at two sewage treatment works in southeastern tainted hands of those who waited on the sick or by England. Hussong and others (1979) failed to isolate contamination of water and milk. Salmonella from forty-four migratory waterfowl Salmonella transmission takes place when the wintering at Chesapeake Bay (USA). The infection of infected feces of man or animal are ingested by a gulls may be due to their habit of scavenging for food at susceptible person. In the case of typhoid fever, rubbish tips and sewage treatment works. Gulls have transmission is only from human feces or urine to been implicated in the contamination of water mouth. This fecal-oral (or occasionally urinary-oral) reservoirs by salmonellae, and in the spread of transmission may be direct where personal cleanliness salmonellaefromrefusetipstocattleonnearbypastures is poor, or it may be via contaminated food or water. (Williams and others 1977). Large numbers of bacteria are excreted, and high Many species of reptiles and other cold-blooded infective doses are required to infect most persons and animals are carriers of Salmonella (Goyal and Singh animals. 1970). This is of epidemiological importance in cases Cases of salmonellosis or enteric fever may excrete where these animals have close contact with man. up to 1010 Salmonella per gram of feces. Unlike other Particular concern has been expressed over the high bacterial enteric infections, asymptomatic carriers may prevalence of Salmonella excretion among pet turtles, also excrete very high concentrations. Thomson (1954, terrapins, tortoises, frogs, and snails (Bartlett and Trust 1955) studied Salmonella excretion by cases and 254 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA carriers. Twenty cases of salmonellosis excreted per day to which 105 S. dublin per liter were added, 2.5 x 105-1 x t09 Salmonella per gram of feces, and 6 three out of four were infected but none developed Salmonella carriers excreted 1 x 104-5 x 107. Seven diarrhea. The authors pointed out that these exposures cases of paratyphoid B excreted 1 x 10'-5 x 109 S. (105 Salmonella per day) are higher than would be paratyphi B per gram, and 12 paratyphoid B expected under normal farming conditions in which carriers (known duration 1-20 years) excreted cattle graze on pasture spread with sludge. However, 5 x l0-1.2 x 1010 S. paratyphi B per gram. Half of the some cattle, like some humans, may be infected by fewer paratyphoid B carriers excreted more Salmonella per organisms if they are for any reason especially gram than E. coli. Eight typhoid carriers (known susceptible.Aitkenand others (1976)showed thatcows duration 3-12 years) excreted 5 x 105-4.5 x 107 S. were more susceptible to S. dublin if they were also typhi per gram. Merselis and others (1964) found that infected by the liver fluke, Fasciola hepatica (see thirteen typhoid carriers (known duration 4-41 years) chapter 27). excreted 104-101 S. typhi per gram of feces. Although fecal-oral transmission of salmonellae is The infective dose for typhoid and other salmonellae the norm for man and animals, the organism may be is high in healthy adults. In a major series of studies, spread by other routes. Garg and Sharma (1979) McCullough and Eisele (1951a, 1951b, 1953a, 1953b) isolated salmonellae from the nasal passages of 2 calves fed eggnog containing various doses of S. anatum, S. and 2 piglets out of 395 young farm animals in India. bareilly, S. derby, S. meleagridis, S. newport, and S. Crozier and Woodward (1962) found that chimpan- pulloruim to healthy adult prisoners. The doses needed zees could be given typhoid fever by the respiratory to produce clinical symptoms in about half of the route with a dose of 108 S. typlli, compared with a dose volunteers were between 9 x 105 for S. anatuin and of 1011 organisms needed for successful oral infection. 4 x 109 for S. pullorum. No clinical disease was Darlow, Bale and Carter (1961) found that 57 percent produced with less than 1.3 x 105 organisms, but (34 of 60) of mice inhaling 5 x 10' S. tyvphimuriunl died infection and a temporary carrier state was established in 4 weeks, and all except 1.7 percent (1 of 60) were with only 1.2 x 104 S. anatum. infected. By contrast, when mice ingested the same dose Hornick and others (1970) reported a median only 1.7 percent (1 of 60) died in 4 weeks, and 75 infective dose (ID,,) of S. typhi for healthy adult male percent (45 of 60) were not infected. Morse, Myhrom volunteers of l0' organisms in 30 milliliters of milk. No and Greenwood (1976) cited studies from the USSR disease was produced in any of 14 volunteers by 103 showing that Salmonella infection of sheep and cows by organisms. In subsequent tests, five different S. typhi aerosols was possible with 27 percent of the dose strains were fed to volunteers at a dose of 107 and required for infection by the oral route. Moore (1957) induced disease in between 21 and 56 percent and reported that the ID,0 of S. enteritidis for guinea pigs infection or disease in between 60 and 93 percent. As was 109 when fed by mouth and only 102 when placed with all ID50 data, it must be remembered that the on the eye (see also Duguid, Darekar and Wheater attack rate in most common source outbreaks is very 1976). Thus, although fecal-oral transmission is the much less than 50 percent. norm, fecal-nasal, fecal-ocular, and nasal-nasal routes Although the ID50s for salmonellae are high, some are also theoretical possibilities (see also Wray and individuals may be infected and made ill by much Sojka 1977). smaller doses. D'Aoust and Pivnick (1976) reported outbreaks caused by 15,000 S. cutbana in carmine dye Incubation period capsules, by 1,000 Salmonella in ice-cream, and by chocolates containing only 100 S. eastbourne per gram. In typhoid fever the incubation period is usually In children with abnormal gastrointestinal tracts due between 5 and 21 days, whereas that of paratyphoid to cystic fibrosis, Lipson (1976) reported infection with tends to be less. Typically, the first symptom to appear S. schiwarzengrund from probably <100 bacteria. is fever due to bacteremia; only later, usually in the The infective dose of Salmonella for healthy cattle is second and third weeks of the illness, do bacteria high, although young calves can be readily infected, invade the intestine from the blood stream in and sometimes killed, by a dose of only 104 S. increasing numbers to be detected in fecal specimens. typhimurium (Deans Rankin and Taylor 1966; The typical symptoms of enteric fever may be preceded Robinson and Loken 1968). Hall and Jones (1978) by acute gastroenteritis. Most other salmonelloses detected no infection in four cows each fed 1 liter of raw have considerably shorter incubation periods, gen- sludge per day containing 102_105 Salmonella per liter. erally between 8 and 36 hours, typically followed by In another group of cows fed 1 liter of sterilized sludge headache, nausea, vomiting, abdominal pain, fever, SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 255 and diarrhea. Incubation periods are inversely personnel, 4.2 percent of slaughterhouse workers, 6.2 proportional to infecting dose. percent of poultry processers, and 8.6 percent of food handlers (Al-Ani and Saadallah 1979). No salmonellae were isolated from the urine of 905 people. Al-Dulaimy Period of commun7nuicability and Al-Allaf (1979) reported a 1.2 percent (23 of 2,000) In typhoid and other enteric fevers, the Salmonella prevalence of Salmonella excretion in Mosul (Iraq). species responsible appears in the excreta late in the Becerril, Bessudo and Gonzalez Cortes (1979) found first week of illness or thereafter. During the first few that 13 percent (110 of 850) of food handlers, and 5 weeks of convalescence the proportion of patients percent (73 of 1,527) of the general population, were excreting typhoid bacilli falls, until about 3 months Salmonella carriers in Mexico City (Mexico). Various after the onset of illness less than 10 percent of clinical studies in South Africa showed Salmonella excretion in cases continue to excrete S. typhi in their feces. Two to 2-6 percent of hospitalized children 0-2 years old five percent may become chronic carriers and excrete without diarrhea and in 0-12 percent of healthy the pathogen for over 1 year. A small proportion schoolchildren (Koornhof and others 1979). remain carriers for 10, 20, 30 years or a lifetime. As In contrast, Gordon and others (1961) reported an noted above, chronic typhoid carriers may excrete average prevalence of Salmonella excretion among 104-10' S. typhi per gram of feces and therefore about 10,000 healthy children under 10 years old in constitute a major source of infection within a highland and lowland villages in Guatemala of only 0.2 community. The gall bladder is the organ that typically percent. Other data showed the Salmonella was not an remains infected, and gall stones may predispose important cause of diarrhea in that age group in those towards the carrier state. villages (Pierce and others 1961). Similarly, studies in Some typhoid and paratyphoid cases pass the USA in the 1950s showed that Salmonella was Salmonella in their urine. Chronic urinary carriers of rarely excreted by healthy children from lower typhoid and paratyphoid are, however, much less socioeconomic groups. Among preschool children in common than fecal carriers, except in countries where Kentucky the prevalence of Salmonella excretion was urinary schistosomiasis (see chapter 32) is common. In 0.2 percent, whereas that for Shigella was 3.1 percent such areas many urinary carriers of enteric fever bacilli (Schliessmann and others 1958), and among children are found, and the prevalence may be as high as 3 under 10 years old in California the prevalence of percent of typhoid convalescents. Hathout and others Salmonella excretion was 0.4 percent, whereas 4.6 (1966) found that, among forty-nine males in Egypt percent excreted Shigella (Watt and others 1953). with Schistosoma haematobium infection who con- tracted typhoid or paratyphoid A, 47 percent were still excreting Salmonella in their urine 1 year after the Resistance diagnosis of enteric fever. (Among those with For the enteric fevers and the salmonelloses, Schistosoma mansoni infection, typhoid and some other individuals who have gastric hypochlorhydria, who are Salmonella infections give rise to severe illness over sick or who are on antibiotic therapy are especially many months.) susceptible. Indeed, Salmonella infections frequently In other salmonelloses, the bacterium appears in the select debilitated individuals, and hospital outbreaks feces concurrently with the diarrhea and for a few days are often especially serious. to a few weeks thereafter. A temporary carrier state for An attack of typhoid fever confers some immunity to around 2 months occurs in 5-10 percent of reinfection, usually life-long, but second and third convalescents, but chronic carriers (over 1 year) are attacks have been reported. Although antibodies to rare (less than 1 percent of cases). several Salmonella antigens are readily detectable in In many poor communities the incidence of serum, they correlate poorly with resistance. In some Salmonella infection is high, and many infections do areas where typhoid is endemic, about 5 percent of not produce disease. Therefore, at any time 1-5 percent cases occur in those under 5 years old and perhaps 4 of the healthy population will be excreting Salmonella percent are fatal. About 45 percent of cases occur in the bacteria. Infection prevalences are higher among 5- 19 age group, and fatalities range from 2 to 6 percent. workers who come into daily contact with potentially Thereafter, from ages 20 to above 60 years, the infected people, animals, or animal products. The incidence rate falls progressively, but the case fatality carrier rates for salmonellae among healthy adults in rate increases to over 30 percent in cases over 60 years Baghdad (Iraq) were 1.9 percent of random persons, old. It may be inferred that many in the community 2.9 percent of buffalo owners, 3.2 percent of hospital become immune during childhood and adolescent 256 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA exposure, though proof is lacking. The outcome of (Watt and others 1953), Kentucky (Schliessmann and challenge depends also on dose size and the virulence of others 1958), and Texas (Watt and Lindsay 1948) in the strain of S. typhi. the USA. It may be concluded that there are major Among the other salmonelloses, attack rates are unexplained differences in the prominence of highest in the age group under 5 years and especially Salmonella diarrheas in children (as there are with all high in infants under 1 year. Significant immunity is individual agents of diarrhea), but that in many poor not conferred; in any case, the next challenge is likely to communities salmonellae do not make a major be from a different serotype. contribution to overall pediatric diarrheal morbidity and mortality. Typhoid is commonly endemic in Africa and is Epidemiology especially prominent in some upland areas. Characteristic features of endemic highland typhoid The salmonelloses have a markedly seasonal are illustrated by the situation in Lesotho described by incidence, peaking in the warmest months along with Feachem and others (1978). At one major hospital (St. all diarrheal diseases. This may be in the warm-wet Joseph's Hospital. Roma) during 1971-74, typhoid season, as in Lesotho and India, or in the warm-dry accounted for 1 percent of all attendances (inpatients season, as in such countries as the UK, El Salvador, and outpatients) and 5 percent of all admissions Guatemala. and the USA. In those countries where it is (inpatients). The highest age-specific incidence occur- endemic, typhoid may peak at the same time or a few red in the 15-24 age group. The fatality rate among all weeks later. A late summer or autumn high incidence of hospitalized typhoid cases was about 6 percent, typhoid, for example, follows the summer peak whereas in patients over 35 years it was 13 percent. salmonellosis incidence in Lesotho, India, and Tunisia. Typhoid in Lesotho had a pronounced seasonal Although salmonelloses constitute an important pattern, with major outbreaks occurring every 2 or 3 cause of diarrhea, especially foodborne diarrhea, in years during March-April, temperature and rainfall many developed countries and are also of major peaked during November-March, and all diarrhea veterinary importance in some areas, Salmonella are reportings peaked during December-February. responsible for only a very small proportion of infant The maximum typhoid incidence among the 10-30 and childhood diarrhea in some developing countries. age group is typical of endemic typhoid and has been In these latter places Salmonella are completely over- reported from, for instance, Antigua (Uttley 1960), shadowed as a cause of childhood diarrhea by Dominica (Grell 1979), India (Mathur and Sharma enterotoxigenic E. coli (chapter 13), rotavirus (chapter 1971), Jamaica (Miller, Grant and Irvine 1961), and 11), and sometimes also Shigella (chapter 16) and Tunisia (Miled, Zribi and Ben Rachid 1973). Ashcroft Campylobacter (chapter 12). For example, Salmonella (1962) reported a peak incidence of typhoid in Guyana was associated with only I percent of childhood (1-5 during 1956-60 among slightly younger children (5-14 years) diarrhea in Guatemala (Pierce and others 1961), years) and suggested that the age of peak incidence 0-1.7 percent of childhood diarrhea in Panama might rise as sanitation improved and children were (Kourany and Vasquez 1969), less than 1 percent of less frequently immunized by mild or asymptomatic childhood (under 5 years) diarrhea in Bangladesh infections. (Black and others 1979), and 1.4 percent of diarrhea Typhoid fever in the UK has been reviewed (Public cases among young children in a Gambian village Health Laboratory Service Standing Sub-Committee (Barrell and Rowland 1979). In contrast, studies on on the Bacteriological Examination of Water Supplies both black and white children (0-2 years) in South 1978). A major waterborne outbreak (341 cases and 43 Africa showed Salmnonella excretion in between 6 and deaths) occurred in Croydon in 1937 (Holden 1939). 17 percent of diarrhea cases and 2-6 percent of healthy Between 1941 and 1970, several small outbreaks were controls (Koornhof and others 1979). This contrast traced to the ingestion of well or stream waters might suggest that Salmonella diarrhea becomes more contaminated by chronic typhoid carriers. Other prominent as economic conditions improve, since the outbreaks were caused by contaminated milk, oysters. South African children studied were probably more and imported corned beef. A major typhoid outbreak urban and wealthier than the Guatemalan or in Aberdeen (Scotland) in 1964, with 507 cases and 3 Bangladeshi groups. However, this economic distin- deaths, was caused by a single tin of contaminated ction falls down in the case of Panama, and it was corned beef from South America. The meat was sliced shown in the 1940s and 1950s that Salmonella were not and sold at a supermarket, and about 50 people were a major cause of childhood diarrhea in California infected from this corned beef. The remainder were SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 257 infected by eating other cold meats that had been sliced several different organisms, including Staphylococcus by the same machine in the same supermarket (Howie aureus, Clostridium botulinum and Cf. perfringens, and 1968; Walker 1965). Since about 1955 the annual Vibrio parahaemolyticus. The bacteria multiply in the incidence of typhoid in Britain has been very low. contaminated food and may produce exotoxins in the During 1975 and 1976, 419 cases were reported in case of Staphylococcus and Clostridinim, when symp- England, Wales, and Northern Ireland, and 85 percent toms result from ingestion of the preformed toxin. In of these were infected abroad. By contrast, only 33 infective food poisoning the gastrointestinal symptoms percent of 1,418 S. typhi infections in the USA during follow proliferation of the bacteria in the human 1967-72 were associated with foreign travel, although intestine. When the pattern of food preparation there was a markedly rising trend in this percentage (17 provides opportunities for salmonellae to multiply, percent in 1967, 46 percent in 1972) (Rice, Baine and infection is naturally more likely. Gangarosa 1977). Over this period, indigenous cases of In developed countries the primary vehicles of S. typhi infection were mainly between 5 and 30 years foodborne salmonelloses depend on dietary habits and old, cases associated with travel were mainly in those particularly on the main source of animal protein. aged 10-30 years, and known typhoid carriers were Poultry and egg products are the most frequently predominantly elderly women. implicated vehicles in many countries. In developing Human salmonelloses in the USA during 1963-67 countries, where less animal protein is eaten and were reviewed by Aserkoff. Schroeder and Brachman animals are not typically raised by "factory farming" (1970). About 20,000 cases were bacteriologically methods, the contamination of food by infected food confirmed and reported annually. The annual peaks handlers may be more important than the ingestion of occurred in July-October, and the age-specific naturally contaminated animal products. incidence was by far the highest in those under 4 years Food contamination is believed to be an important old. The reported incidence in Hawaii was nearly 10 factor contributing to the high prevalences of times the national average in each year, and this was Salmonella excretion among African schoolchildren in attributed to the use of pig intestinesin soups and stews South Africa (table 15-'). Surveys of food in Pretoria by certain ethnic groups. There were 180 epidemics, and Soweto showed that 48 percent of tripe samples, 29 comprising 16.772 cases, during 1963-67, and 156 of percent of intestines, 40 percent of pork sausage, 64 these were due to a common vehicle of infection- percent of minced beef samples, 20 percent of chicken especially eggs, egg products, and turkey. Less carcasses, and 16 percent of biltong samples (dried commonly chicken, beef, pork, milk, pet chickens, pet meat eaten raw) were contaminated by salmonellae ducks, and pet turtles were implicated. The largest (Prior and Badenhorst 1974; Richardson, Burnett and number of epidemics were domestic, but the largest Koorhof 1968). Bokkenheuser and Richardson (1959) epidemics were those associated with banquets and found that 4.3 percent (67 of 1,565) of food handlers schools. During the period S. typhimurium was by far employed at nineteen gold mines in the Transvaal were the most commonly identified serotype, constituting 30 infected by Salmonella. percent of all human isolations and 17 percent of all An outbreak of sixty-nine typhoid cases after a party nonhuman isolations. Poultry and poultry products in Cape Town (South Africa) in 1978 was traced to the accounted for half of all nonhuman isolations of main caterer who had prepared and stored chickens for Salmonella. Some serotypes exhibited a considerable the party under grossly unhygienic conditions degree of species specificity: S. piullorum and S. (Popkiss 1980). The main caterer was found to excrete gallinarum in fowl, S. abortus-ovis in sheep, and, to a S. typhi of the same phage type as those isolated from lesser degree of specificity, S. cholerae-suis in pigs and S. the cases. On May 5-7,1977, 545 university students at dublin in cattle. Trujillo (Peru) were hospitalized with acute gastroin- Food-borne outbreaks of typhoid and other testinal symptoms due to S. thiompson (Gunn and salmonelloses are commonly reported. Sometimes they Loarte 1979). The outbreak was traced to the are due to contaminated raw materials, such as poultry, university dining hall, and 93 percent of the students tinned meat, or eggs, while in other cases the food is who regularly ate there became ill. The implicated contaminated by a food handler. Carrier rates for vehicle was sardine-mayonnaise salad. Barrell and Salmonella are typically higher among food handlers Rowland (1979) found that Salmonella were associated than among the general population and there is a close with 1.4 percent of diarrhea cases among young relationship between contaminated food and infected children in a Gambian village and that 4.7 percent of food handlers which places the consumer of the food at infant food samples were contaminated by risk. salmonellae. "Food poisoning" of bacterial origin may be due to Waterborne outbreaks have been chiefly associated 258 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA with S. typhi and much less frequently with S. paratyphi person spread led to the contamination of the hospital or other Salmonella serotypes. The evidence implicat- water system as a result of the suction of wastewater ing a water supply is usually circumstantial, and the into water mains. S. bareilly became established in the causative organism is rarely isolated because the water system and appeared to grow in the interior of pollution that gives rise to an epidemic is often taps and on the walls of water tanks at the water level. temporary or intermittent. Waterborne outbreaks due The contaminated water spread the infection through- to gross contamination are usually characterized by an out the hospital during 1968-69 so that. during explosive onset. The majority of cases develop over a January-March 1969, 48 percent (20 of 42) of hospital period of a few days, and these may be followed by a staff were infected. The rectification of certain secondary crop of contact cases. Sometimes the plumbing defects, and the chlorination of the mains outbreaks may happen as a series of scattered cases and tanks, led to the disappearance of S. bareilly from occurring over a considerable period of time, and this the water system, and the outbreak subsided. may be due to a lower and intermittent contamination A report from Trinidad (West Indies) described of the supply. forty-eight cases of acute diarrhea among eighty-eight Waterborne disease outbreaks in the USA during children and adults attending a church camp (Koplan 1971-73 have been reviewed (Hughes and others 1975; and others 1978). S. arechevalata (a rare serotype) was Merson and others 1974). Typhoid fever was the cause isolated from cases, asymptomatic persons, two food of 2.5 percent (217 of 8,537) of known cases and 4.2 items (a fish dish and stewed peas that had been percent (3 of 71) of known outbreaks, while other prepared with roof-collected rain water), and from salmonelloses were the cause of 0.04 percent (3 of roof-collected rain water. The roof used for rainwater 8,537) of cases and 1.4 percent (1 of 71) of outbreaks. catchment was overhung by trees in which mocking Large, and probably waterborne, outbreaks of diarrhea birds, wrens, and doves nested and rested, and the roof due to S. typhimurium occurred in Riverside was covered with dried and fresh bird feces. This may (California) in 1965 (Greenberg and Ongerth 1966) be the only account of a salmonellosis outbreak due to and in Suffolk County (New York State) in 1976 (Zaki contaminated roof-collected rain water, but small and others 1979). outbreaks, in individual households, having roofs Feldman and others (1974) described an outbreak of contaminated by bird droppings, may be com- typhoid (225 cases and no deaths) at a migrant farm monplace where such rain water is a widely used water labor camp in Florida (USA) in 1973. A case-control source. study linked the infection to the camp water supply, The complex interactions possible between human which was pumped from two wells. The water supply and nonhuman reservoirs, and waterborne and was chlorinated but with inadequate contact time foodborne transmission are illustrated by an outbreak during peak water demand, and the chlorinator had a of S. paratyplli B infection in five cows and ninety history of malfunction. High coliform counts were people in North Yorkshire (England) in 1970. The obtained from the camp water on several occasions, probable chain of events was that a chronic human and it was discovered that surface drainage and sewage carrier contaminated a stream, which infected a herd of might gain access to the wells. It was estimated that the cows, which infected farm workers-one of whom average infecting dose in the outbreak was 103-105 S. contaminated the water supply serving several villages tyvphi and that such doses could have been administered (George and others 1972; Harbourne and others 1972). by the water supply if a case or carrier with heavily The failure of two types of sewage treatment to remove contaminated stools (say 10' S. typhi per gram) had S. paratyphi B from sewage is also suggested by this defecated in the pump house, around the well, or into study. The original chronic carrier contaminated the the water storage tank. stream by way of sewage effluent from a "conventional" In the notorious typhoid outbreak in Zermatt treatment plant (probably trickling filters), and the (Switzerland) in March 1963 (Bernard 1965) there were farm worker contaminated the village water supply by 437 cases and 3 deaths. Some evidence implicated the way of septic tank effluent from his cottage. inadequately chlorinated water supply, which may There is extensive evidence of direct person-to- have become contaminated by a carrier working on the person spread of salmonelloses and enteric fevers catchment or by leakage of sewage into the water under conditions of poor hygiene, in crowded system. institutions, or simply in a normal family setting. Budd Mendis and others (1976) described a very persistent (1856) described an outbreak of typhoid at a military outbreak of diarrhea due to S. bareilly in the maternity school in France in 1826 and reported that among hospital in Colombo (Sri Lanka). Initial person-to- twenty-nine cases nursed at home, eight were known to SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 259 have transmitted the disease to persons attending ampicillin, or cotrimoxazole, is required for the them. Rosenstein (1967) studied the family contacts of treatment of enteric fevers. Prophylactic use of twenty-eight sporadic index cases of Salmonella antibiotics for man and farm animals (a very common diarrhea in Rhode Island (USA). Thirty-five percent practice, although now illegal in some countries) is (42 of 121) of family contacts were found to be infected generally condemned. Antibiotic resistance in by Salmonella of the same serotype as the index case, Salmonella is usually caused by transmissible plasmids and 55 percent (23 of 42) of infected contacts had conferring multiple antibiotic resistance. Thus, misuse diarrhea. Sixty-one percent (17 of 28) of the families of of a single antibiotic can give rise to multiresistant the index cases had at least one infected contact. strains. Some major epidemics of enteric fever and Among all family contacts, children were more likely to salmonellosis, caused by multiresistant Salnionella be infected and, if infected, were more likely to be ill. strains (especially of S. typphi, S. typhimurium, and S. Baine and others (1973) reviewed Salmonella out- wien), have occurred recently in man and animals. breaks in institutions in the USA between 1963 and Typhoid fever is the only disease considered in this 1972. Person-to-person transmission (as opposed to book, except poliomyelitis, for which there is a widely common vehicle outbreaks associated with con- used and moderately effective vaccine, and vaccination taminated food, water, or pharmaceutical products) can play a role in typhoid control. Inactivated whole- was the major mode of transmisson in nurseries and cell vaccines against typhoid are given in two pediatric wards and was also important in outbreaks intradermal or intramuscular doses, with an interval of among hospitalized adults. Person-to-person spread 2-4 weeks, and provide 70-85 percent protection for a was implicated in 61 percent (46 of 76) of institutional period of 3-4 years. To maintain immunity at a high outbreaks in which the mode of transmission was level, revaccination is required every 2-3 years. It has elucidated. been common practice to use a TAB vaccine. which S. anatum could be recovered from artificially combines S. typhi (T) with S. paratyphi A and B (AB) contaminated fingertips for over 180 minutes when the organisms and purports to protect against all three initial inoculation was 530 organisms per fingertip, and enteric fevers. The use of TAB vaccines is, however, for 90 minutes when the initial inoculum was only 36 officially discouraged (WHo 1979) because the addition organisms (Pether and Gilbert 1971). In the same of the S. paratyphi organisms requires a reduction in the study, 106 S. anatum per fingertip were not removed number of S. tvphi present below the 109 organisms completely by hand washing (a 15-second wash with necessary to produce significant antityphoid immunity. soap and running warm water and drying on paper It is therefore recommended that antityphoid vaccine towels), and unwashed contaminated fingertips could alone should be used. A new live oral typhoid vaccine readily contaminate corned beef and cooked ham. has been tested in Egypt and is currently (1982) undergoing further field trials in Chile. Control Measures Carrier surveillance and control The control of enteric fevers, which are primarily Eradication of typhoid from the community requires infections of man, has been achieved in many wealthy the prevention or cure of the carrier state. No countries. The control of other salmonelloses has uniformly successful method of curing this condition proved impossible due to their large and widespread has yet been devised, although a high proportion of animal reservoirs. both typhloid and paratyphoid fecal carriers can be freed from their infection by surgical removal of the gall Individual bladder and concomitant ampicillin therapy. The names of all chronic carriers should be registered with The widespread resistance of Salmonella species, the local health authority, occupational restrictions including S. typhi, to many antibiotics is a serious imposed, and careful instructions given on strict problem brought about by excessive curative and personal hygiene to avoid infecting others. Besides prophylactic use of antibiotics in both human and being prevented from handling food for others, carriers veterinary medicine. Antibiotic therapy in man is not should not be employed on or admitted to water beneficial in uncomplicated Salmonella diarrhea, since works. it does not accelerate recovery and may prolong the Outbreaks of enteric fever can seldom be traced to period of Salmonella excretion during convalescence. the known chronic carriers, and it is the unknown Chemotherapy, usually with chloramphenicol, carrier that is the main danger. It is valuable to 260 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA question new employees in the catering or water supply US$3.15 per latrine or US$0.50 per capita served. The industries to establish whether they have previously value of benefits was also underestimated, however, suffered from enteric fever and to examine them by since it was taken to be the costs of hospital treatment standard serological and cultural procedures. These and lost wages for typhoid only and thus excluded the tests should be repeated at regular intervals and on cost of death (future working days forgone) and the individuals returning to work after any enteric many other health benefits that might result from infection. Excreters of pathogenic organisms identified latrine construction. The model showed immunization by these procedures should be legally precluded from at 5-year intervals to be greatly more cost effective than working in food handling and water supply until it can was the case for cholera (chapter 17), because of the be demonstrated that they are completely cured. greater effectiveness (80 percent assumed) of the typhoid vaccine and its longer period of protection (5 Enrironmental years assumed). The costs of five-yearlv vaccinations of the population (assuming 75 percent coverage), and Wide-ranging economic and sanitary changes in latrine provision for the entire population over a 10- Europe and North America over the last century, year period, were found to be very similar, and the two combined with methods to prevent, detect and cure strategies were predicted to have a similar effect on typhoid carriers, have caused a very great reduction in typhoid incidence-reducing it from around 7.2 cases the incidence of the enteric fevers and have certainly to 2.5 cases per 10,000 people per year over a 30-year removed them from the list of major infectious diseases. period. However. if five-yearly vaccinations were Whether simple water and sanitary improvements discontinued, incidence would increase sharply- applied to poor communities in developing countries whereas the 10-year latrine program, and a low level can have a measurable impact upon typhoid and follow up program to cope with population increase, paratyphoid incidence remains uncertain. It is would continue to bring the incidence down. With probable that a combination of improved water vaccination alone, cumulative benefits would exceed supply, adequate exereta disposal facilities, strenuous cumulative costs after 10 years; with latrine con- health education programs, and national systems for struction alone this point would be reached after 20 identifying, controlling and treating carriers are years, whereas with both vaccination and latrine con- required. struction benefits would not exceed costs until after 25 The control of salmonelloses will inevitably prove years. Cvjetanovic and his colleagues concluded, by much more difficult because of the widespread animal using both the model and actual data on typhoid reservoir. In the developed countries salmonelloses incidence in England and Wales and the USA, that may have decreased since the last century (although continuing improvements in sanitary and economic this is not known), but they remain a major medical conditions would lead eventually to the eradication of and veterinary problem. The trends in diet and farming typhoid (except for imported cases) without recourse practice that accompany economic development will to mass vaccination. Models of this type are useful in tend to increase the salmonellosis problem. Improved focussing attention on the dynamics of a disease and water supply and excreta disposal, coupled with tighter the potential impact of various interventions. The cost- control of the catering industry and improved food benefit analyses could be greatly improved by hygiene at home, will have a beneficial effect. reconsidering some of the epidemiological variables, Cvjetanovic, Grab and Uemera (1971, 1978) especially the effect of sanitation on transmission, and constructed a mathematical model of endemic typhoid by incorporating more rigorous economic costing and to predict the impact of immunization and latrine discounting techniques. construction. The values fed into the model were those Studies in Lesotho (Feachem and others 1978) corresponding to the demographic, medical, and suggested that the periodic summer typhoid outbreaks, economic situation in Western Samoa. As with their and the sporadic cases between outbreaks, were not cholera model (see chapter 17), Cvjetanovic and his associated with rainfall or increased water pollution coworkers overestimated the impact, and greatly and that villages with improved water supplies underestimated the costs, of latrine construction. They providing water of good quality were not protected excluded all labor and material costs, which were against these outbreaks. It was also shown that the met by the householders, and deemed the cost of a temporal and spatial patterns of two typhoid latrine to be only the costs borne by the govern- outbreaks studied in detail were not suggestive of ment in the provision of supervision and technical waterborne transmission. It was concluded that much assistance. This government input was valued at typhoid transmission in Lesotho was nonwaterborne SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 261 and that wide ranging improvements in waste disposal, Other work in South Africa by the same authors has cleanliness, food hygiene, and water supply were strongly implicated Salmonella contamination of meat necessary to reduce typhoid incidence. Identical and meat products in the transmission of salmonellosis conclusions were reached for all diarrheal diseases in (Prior and Badenhorst 1974; Richardson, Burnett and Lesotho, an unknown proportion of which are due to Koornhof 1968). The contention is indirectly sup- Salmonella infections. ported by parasitological data, obtained during the It is illuminating to review a series of studies 1966 survey at Tlaseng, showing that 16 percent of on salmonellosis and shigellosis among healthy children had Taenia infections (compared with only 3 African schoolchildren in the Transvaal (Republic of percent having Ascaris, 2 percent having Trichuris, and South Africa, Bokkenheuser and Richardson 1960; 2 percent having Necator), data that indicate the Richardson and Bokkenheuser 1963; Richardson and common consumption of undercooked meat. Koornhof 1965; Richardson, Koornof and Hayden- Smith 1966; and Richardson and others 1968). The schools took children from very different economic Occurrence and Survival in the backgrounds and were, in rising order of economic Environment standard and urbanization, located at Tlaseng, Komatipoort, Witkoppen, and Soweto. The results are Because of their very extensive nonhuman reservoir, summarized in table 15-2. The water supply and salmonellae can be isolated frequently from a wide sanitation facilities were very poor, except at Tlaseng in variety of environmental samples. Before the role of E. 1966 after a new water supply had been constructed coli and Campylobacter in human diarrhea was and at Soweto where high standards of water supply recognized in the 1970s, the bacterial enteric pathogens and excreta disposal prevailed. The authors of these of prime interest were the salmonellae, the shigellae, studies started out believing that waterborne trans- and Vibrio. cholerae. Of these it is the salmonellac that mission of Salmonella and Shigella was important and are by far the most common in environmental samples, ended up concluding that it was not. After the first and so a great deal of work was done on the occurrence Tlaseng study, Bokkenheuser and Richardson (1960) and survival of salmonellae in water and soils. Indeed, wrote that "water supply was probably implicated in Salmonella became the favorite pathogen of the the conveyance of the infections". After the Witkoppen sanitary engineers and environmental microbiologists; study, Richardson and Bokkenheuser (1963) wrote whenever data on more than harmless indicator that "the poor quality of the water, particularly that organisms were required, salmonellae would be drawn from surface wells, made it highly probable that studied. This situation has generated a large literature, drinking water was involved in the transmission of the second only to that on fecal indicators in the infections". After the Komatipoort study, Richardson environment (see chapter 13), and only a small portion and Koornhof (1965)wrotethat "the suspicion that the of it can be reviewed here. In the absence of specific water supply is a factor in the transmission of information, it may generally be assumed that the salmonellosis is strengthened by the results of the survival, and the factors affecting survival, of present survey". Then came the shock of finding Salmonella in the environment is similar to that prevalences in Soweto as high as, or higher than, those described for fecal coliforms and E. coli in chapter 13. reported from relatively impoverished rural areas with poor sanitation. Richardson, Koornhof and Hayden- Smith (1966) then wrote that "although it is reasonable In surface water to assume that water contamination plays some part in Salmonellae will be found in surface waters wherever the transmission of these organisms, it does not appear there are animal populations. Those workers who have to be the most important factor", and again that "water failed to find them have probably not looked hard supplied to each house by the Johannesburg enough. This involves sampling large volumes of water, municipality was of good quality, yet it did not affect or using suspended swabs to sample flowing water for the incidence of salmonellosis and shigellosis". The several days. The occurrence and survival of salmon- complete turnabout came after the resurvey of Tlaseng ellae in surface waters has been reviewed by Wray in 1966, when Richardson and others (1968) concluded and Sojka (1977). that "in the environment of the Bantu children the Salmonellae are found in rural streams receiving provision of high quality community water as the only run-off from agricultural land and discharges of sanitary measure was without effect on the prevalence domestic and other effluents from villages and rural of intestinal Salmonella and Shigella infections". industries. Harbourne (1977) and Harbourne, Thomas 262 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA and Luery (1978) readily isolated salmonellae from isolated 4,500 S. tilompson per 100 milliliters from a swabs suspended in streams in North Yorkshire sample of urban stormwater in Cincinnati (Ohio, (England). Smith, Jones and Watson (1978) sampled USA). Olivieri, Kawata and Kruse (1978) reported rivers and streams running through agricultural land that salmonellae were nearly always present in samples in Cheshire and Lancashire (England). Salmonellae of urban stream water and stormwater in Baltimore were detected at 71 percent (10 of 14) of the sites (Maryland, USA) and that geometric mean con- investigated. Sewage effluent discharges were believed centrations at various sites were between 6 and 140 per to be the major source of the salmonellae, but farms, a 100 milliliters. dairy, an abattoir, and gulls were also implicated. In The detection of salmonellae in waters with very low one stream the concentration of salmonellae was 1,100 fecal indicator counts is not uncommon. Dutka and per 100 milliliters at an effluent discharge point and Bell (1973) studied the St. Lawrence river (Canada) 23 per 100 milliliters at a point 0.5 kilometer and detected salmonellae in 24 percent (17 of 72) of downstream. samples containing less than 9 fecal coliforms per 100 Davis (1979) studied stream water quality in a rural milliliters. Samples that contained more than 1,000 area north of Houston (Texas, USA). During low flow, fecal coliforms per 100 milliliters were 86 percent (6 of salmonellae concentrations were up to 5,800 per 100 7) positive for salmonellae. Geldreich and Bordner milliliters, and during storms the maximum con- (1971)reviewedavariety of stream pollution data from centration was 2,500 per 100 milliliters. Salmonellae the USA and found that salmonellae had been detected were sometimes detected when fecal coliforms were in 54 percent of samples containing 1-1,000 fecal absent. Dondero and others (1977) isolated salmon- coliforms per 100 milliliters and in 96 percent of ellae from 39 percent of 322 swabs suspended in six samples containing more than 1,000 fecal coliforms per streams in central New York state (USA). Cherry and 100 milliliters. others (1972) found that 44 percent of samples Many attempts have been made to relate the collected from unpolluted mountain streams ("judged presence of salmonellae in surface waters to the to be completely free from human, domestic animal concentrations of fecal coliforms or other fecal and industrial pollution") in Georgia (USA) contained indicator bacteria (see chapter 13). Although in general salmonellae. One "unpolluted" stream acquired the chances of isolating salmonellae increase as water salmonellae within 100 meters of its source. The pollution (and therefore indicator densities) increase, authors suggest that some salmonellae may have an there is no precise or generally applicable relationship. aquatic reservoir and that they may be '"superior to Increed, when analyzing data from a particular location coliforms as indexes of water quality". These several workers have found that Salmonella con- suggestions, apart from being contradictory, have not centrations are among the most difficult bacterial been supported by subsequent work. pathogens to predict on the basis of indicator Drainage from farms raising animals by intensive concentrations (Davis 1979; Olivieri, Kawata and methods are responsible for major contributions of Kruse 1978). Gallagher and Spino (1968) reviewed salmonellae to rural streams (see, for instance, Miner, water pollution data from several rivers in the USA and Fina and Piatt 1967). The Salmonella serotypes found failed to show any fecal coliform density below which in a particular water may reflect the special character of Salmonella isolation would be particularly unlikely. the wastes contaminating that water. S. agona, a Smith, Twedt and Flanigan (1973) isolated salmonel- serotype associated with fish meal used as a poultry lae from the Huron and Saline rivers (Michigan, USA) and animal feed, was found in all water samples from a at sites where fecal coliform concentrations were low creek receiving poultry wastes in Georgia (USA; Cook, and found that, probably due to technical difficulties in Champion and Ahearn 1974). the laboratory, "the probability of Salmonella isolation Salmonellae can travel considerable distances in decreased as the fecal coliform concentration streams and rivers, especially at low water tempera- increased". tures. Spino (1966) showed that S. saintpaul and S. Salmonellae are more likely to be found in bottom thompson traveled for at least 120 kilometers under the sediments than in the overlying waters. Hendricks frozen surface of the Red River of the North from their (1971a) isolated salmonellae from 0.6 percent (1 of 195) source at the Fargo-Moorhead (North Dakota- of water samples and from 4.6 percent (9 of 195) of Minnesota, USA) effluent discharge sites. bottom sediment samples in a stretch of river (Georgia, Salmonellae are also found in urban streams and USA) below a sewage effluent outfall. Van Donsel and stormwater run-off, although in the absence of waste Geldreich (1971) collected simultaneous sediment and discharges the concentrations may be lower than found water samples at a variety of lake and river sites. Forty- in rural catchments. Geldreich and others (1968) six percent of sediment samples, and only 8 percent of SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 263 water samples, contained salmonellae. The highest Survival is greatly prolonged at lower temperatures Salmonella concentration in sediment was 790 per 100 and somewhat prolonged in darkness. Experimental milliliters. Salmonellae were isolated from 19 percent data show that survival is prolonged in more polluted of sediment samples when the fecal coliform con- waters, but many experiments are done in biologically centration in the overlying water was between 1 and inactive polluted waters (autoclaved or filtered), or in 200 per 100 milliliters, from 50 percent when between chambers suspended in polluted waters, where the 201 and 2,000, and from 80 percent when the fecal salmonellae are not exposed to predation and coliform concentration in the water was over 2,000 per competition. Experiments in New Zealand, however, 100 milliliters. showed that S. typhimurium and S. bovis-morbificans The survival of salmonellae, especially S. typhi, in survived for under 2 weeks (tgo <56 hours) in clean water has been investigated by several researchers over water and for 12-16 weeks (t90 = 340-450 hours) in the past 80 years (see the appendixes to Feachem and unsterilized water containing 5 percent (weight per others 1980). McFeters and others (1974) studied the volume) sheep feces (Tannock and Smith 1971). survival of several species of enteric bacteria in Growth of salmonellae in polluted water is possible membrane chambers suspended in well water at but unlikely, although concentration and perhaps 9-13°C. Approximate tgo values over 2 days were 80 growth in bottom sediments is more likely. Hendricks hours for S. paratyphi A and S. typhimurium, 32 hours (1972) showed that S. senftenberg grew in autoclaved for S. typhi, and 19 hours for S. paratyphi B. Geldreich river water collected downstream of a sewage effluent and others (1968) derived t90 values over 14 days for S. outfall at 30°C. No growth occurred at 20'C or 50Cor in typhimurium in storm water of 240 hours at 10°C and autoclaved river water collected upstream from the 160 hours at 20°C. At both temperatures the dieoff of same outfall (see also Hendricks 197lb and Hendricks S. typhimurium was similar to that of fecal coliforms and Morrison 1967). and considerably more rapid than Str.faecalis. Viewed with hindsight, the interest in low levels of Dutka and Kwan (1980) studied the death of S. salmonellae in surface waters, and their relationship to thompson in membrane chambers suspended in Lake the concentrations of indicator bacteria, seems Ontario and Hamilton Bay (Canada) when water excessive. From the viewpoint of human public health, temperatures were 17-19°C. Over the first 3 days, tgo the greater importance of other bacterial agents of values were 19-180 hours, and over the entire 28 days diarrhea, the frequent transmission of salmonelloses by of the experiments average tgo values were 122-224 contaminated animal products, and the high infective hours. Death rates were considerably greater near the dose for salmonellae make the presence of low surface than at greater depth and were higher in less concentrations in surface water a matter of only minor polluted water (Lake Ontario) than in more polluted concern in developed countries. From a veterinary water (Hamilton Bay). S. thompson dieoff was similar viewpoint, it has been suggested that the con- to Str. faecalis and faster than E. coli. tamination of rural streams by salmonellae may help to The range of death rates reported is large and there is maintain infection among farm animals (Smith, Jones considerable interserotype, and probably also in- and Watson 1978). There are other more likely routes traserotype, variation in ability to survive in water. It of transmission among farm animals, although stream has been suggested that these differences in survival pollution has undoubtedly contributed to some may partly explain why some serotypes are common outbreak (George and others 1972; Williams 1975; and others are very rare in human and animal infection Wray and Sojka 1977). In developing countries, surface (Enkiri and Alford 1971). Few comparative studies on water contamination by salmonellae must be seen in different serotypes in water under identical conditions the light of the probable minor importance of have been conducted, but the data of McFeters and Salmonella in pediatric diarrhea and of the many others (1974) showed that S. typhimurium, a very alternate transmission routes for salmonellae in areas common serotype, survived for longer than S. typhi and of poverty and poor hygiene (see table 15-2 and the S. paratyphi B. discussion of salmonellosis in South Africa and Overall survival times reported range from 1 to over typhoid in Lesotho, above). 100 days, with typical tgo values in the range of 20-200 hours. These results are similar to the fecal coliform tgo In groundwater data reviewed in chapter 13, and most comparative studies have found Salmonella survival to be similar to Salmonellae are unlikely to be present in ground- that of fecal coliforms (see, for instance, Smith, Twedt water unless the water table is very shallow or fissured and Flanigan 1973). The factors affecting Salmonella strata allow the direct flow of surface waters into an survival are the same as those affecting fecal coliforms. aquifer. Salmonellae have not been isolated from dual z Table 15-2. Period and point prevalences of Salmonella and Shigella excretion by black schoolchildren in the Transvaal, Republic of South Africa Water supply3 (E. coli a~~~~~~~~~~ concentra- I year period prevalencea Meani point prevalencee No. of tions are (percent) (percent) Age of surveys per 100 Excreta - No. of chiildren per milliliters disposal Salmonella Shigella Salmonella Shigella Site Year children (years) year (? water) facilities excretion excretion excretion excretion Source Tiaseng school. 1958- 59 75 6-16 7 Polluted Noneb 36' 25' 6.3d 4.2 Bokken- rural shallow heuser Western wells and Transvaal (2-900 Richardson E. coli) (1960t 1966 92 7-16 4 Borehole Pit 13' 20( 3.8 5.5 Richardson with retic- latrines' and ulation others (0 E. coli) (1968) School near 1964 99 7 17 2 Piped Pit 6 3 3.5 2.0 Richardson Komati- water latrines5 and poort on (0 E. coli) Koornhof Mozambique River water (1965) border (50-250 in rural E. coli) Eastern and Transvaal salmon- Lowveld ellae) School at 1961 75 7-18 8 Protected Pit 30 2.7 5.8 0.3 Richardson Witkoppen, well with latrines' and a periurban hand-pump Bokken- area 25 (0 E. coli) heuser kilometers Borehole (1963) from with Johannes- motor pump burg (0- 4 E. coli) Borehole with wind pump (0->4 E. coli) Open well (>4 E. coli) Two schools 1964 55 7-18 8 Chlorinated Water- 36 9 5.9 1.1 Richardson, in Soweto, piped borne Koornhof a large water sewerage and African (0 E. coli) Hayden- city near Smith (1966) Johannes- burg a. The recorded annual period prevalence of an acute and readily transmissible infection, such as salmonellosis, rises markedly as the number of surveys per year increases, Therefore, the figures for Komatipoort, for instance, are not comparable with those from Witkoppen. b. This information is not given in the original source but in the summary by Koornhof and others (1979). z c. For the reasons stated in note a, it is not possible to compare the period prevalences from 1958-59 (seven surveys) with those from 1966 (four surveys). d. This figure is elevated due to an outbreak of S. mobeni infection that coincided with the survey in December 1958. 0 z 0 c,) C,) 266 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA purpose wells in Israel used for groundwater recharge The contamination of clean drinking water by E. coli and abstraction (Goldshmid 1974). Salmonellae will be while the water is stored in the home is well found in many open wells due to the drainage of documented (chapter 13). No similar data exist for contaminated surface waters down unprotected well salmonellae, although such pollution may be expected shafts. and has been shown for clean water used by infected turkeys (Gauger and Greaves 1946). In drinking water It is uncommon to isolate salmonellae from piped In seawater water supplies, whether treated or untreated, and their Salmonellae are found in estuarine and marine presence suggests a serious fault in the design or environments where there is fecal contamination from maintenance of the system. Raman and others (1979) domestic or agricultural wastewater discharges or found that 9 percent (3 of 33) of tap water samples in where there are large populations of water birds. The Aurangabad (Maharashtra, India) contained salmon- occurrence and survival of salmonellae in seawater ellae due to leakage of polluted water into the have been reviewed by Buttiaux (1962). distribution system. Colwell and Kaper (1978) reported that the ratios of S. typhimurium was isolated from 7 percent (5 of 74) salmonellae to fecal coliforms in Chesapeake Bay of water samples from taps and reservoirs of the water (USA)ranged from 1:100 to 1: 1000 and that there were supply system of Riverside (California, USA) during up to 240 salmonellae per 100 milliliters in Baltimore the major outbreak of salmonellosis in May-June 1965 Harbor (Maryland, USA). Salmonellae could not be (Boring, Martin and Elliot 1971). One composite isolated from Chesapeake Bay in the winter, only sample examined quantitatively revealed 1.7 S. during April-November. In contrast, Carney, Carty typhimurium and 0.14 E. coli per 100 milliliters. All and Colwell (1975) failed to isolate salmonellae in an S. tYphimurium isolates examined were of phage type extensive survey of microbiological pollution in a 10, as were the clinical isolates during the outbreak. subestuary of Chesapeake Bay, despite occasionally The water sources were deep wells, and the water was elevated concentrations of fecal coliforms (up to 5,400 delivered unchlorinated. per 100 milliliters) Schubert and Scheiber (1979) reported that salmon- Goyal, Gerba and Melnick (1977, 1978) studied the ellae could frequently be isolated from piped drinking occurrence of fecal indicator bacteria and salmonellae water in Togo, even in the absence of E. coli and in the waters (salinities 1.0-2.2 percent) and bottom coliforms. This was attributed to faulty wellheads and sediment of canals bordering Galveston Bay (Texas, broken reservoir covers allowing access to rainbow USA). The canal networks are largely man-made, and lizards (Agama agama), which were often found to holiday homes are located along their banks. Domestic excrete salmonellae and sometimes few or no E. coli wastes are discharged into the canals through septic and coliforms. Keeping small animals out of water tanks or small treatment plants, and the canals are systems, and thus reducing the risk of contamination greatly used for bathing, boating, skiing, and diving. by salmonellae, can prove extremely difficult, es- Salmonellae were isolated from 47 percent (17 of 36) of pecially in arid areas. sediment samples but from only 3 percent (1 of 36) of A large proportion of the population of the water samples. Salmonellae concentrations in sedi- developing countries drink untreated and unprotected ment were between 0 and 150 per 100 milliliters. surface waters or open well waters that are often The limited information on Salmonella survival in heavily polluted by feces (table 13-1). Salmonellae may seawater indicates that it may be only slightly less than be expected in these drinking water sources, although survival in fresh water. Since E. coli survival is very few data on their presence exist. Salmonellae will be far much shorter in seawater than in fresh water (chapter more common than shigellae (chapter 16) in 13), it follows that Salmonella are more persistent in unprotected water sources because, unlike shigellae, marine environments than are E. coli. Therefore E. coli they are excreted by some pigs and by donkeys, goats, are poor indicators of salmonellae, as they are of cattle, camels, rats, dogs, and other village animals enteroviruses, in marine environments (see Petrilli and whose excreta commonly pollute streams, ponds, and others 1979). open wells. Gracey and others (1979) isolated Jamieson, Madri and Claus (1976) added 1.5 x 107 salmonellae from 48 percent of water samples and from S. typhi to samples of sterilized seawater, adjusted to 63 percent of sediment samples collected from a river salinities of 0.5, 2, and 3.5 percent, and stored them at 4, and canals in Jakarta (Indonesia) used as drinking 25, and 37°C. Survival was inversely proportional to water sources by the poorer inhabitants of the city. salinity and temperature. Maximum survival was for 7 SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 267 days (tgo = 23 hours) at 4°C and 0.5 percent salinity, samples, with overall survival times being 148 days at and minimum survival was for 5 days (t,, = 17 hours) 1 °C. It may be concluded that storing undried at 37°C and 3.5 percent salinity. Survival of E. coli was excreta is more effective in eliminating Salmonella than shorter than that of S. typhi at all temperatures and promoting initial rapid drying. salinities. Vasconcelos and Swartz (1976) compared the These and other studies (listed in the appendixes of survival of S. heidelberg and E. coli in sterilized seawater Feachem and others 1980) suggest tgi9 values of 40-100 at 14.5°C. After 6 days, the E. coli concentration had hours for Salmonella in feces or night soil in tropical declined by 6 log units (tgo = 24 hours), whereas the climates (20-30'C). concentration of S. heidelberg was reduced by only 1.5 log units (tgo = 6 hours). In sewage In feces and night soil The monitoring of sewage for salmonellae in general, In developing countries, pooled human feces are or for S. typhi in particular, is of practical public health likely to contain Salmonella in areas where asympto- value in epidemiological surveillance, investigating matic excretion of the organism is fairly common (see outbreaks of salmonellosis or typhoid, and, especially, above). Similarly, pooled animal excreta are also likely in tracing typhoid carriers. The favored technique is the to contain Salmonella. Screening night soil for S. typhi Moore's swab, an absorbant pad suspended in the flow is potentially useful in epidemiological investigations for 2-3 days. If a pad of calcium alginate wool is used, it of typhoid, and screening farm wastes for specific can be completely dissolved in sodium hexametaphos- Salmonella serotypes can assist livestock and poultry phate on return to the laboratory, thereby liberating all hygiene. the entrapped bacteria. For more rapid results, a wipe Jordan (1926) studied the bacterial content of feces swab can be used-the sewer wall is wiped and the from typhoid patients and carriers (Chicago, USA); swab immediately returned to the laboratory the feces were stored at room temperature in sealed (Bokkenheuser 1964; Gell and others 1945; Harvey cans. S. typhi survived for between 3 and 52 days. and Phillips 1955; Kelly, Clark and Coleman 1955; Desiccation was not a factor contributing to death, Moore, Perry and Chard 1952; Robinson 1958; since the moisture content of the feces stored in this Shearer and others 1959). Alternatively, various manner was still over 80 percent after 77 days. No filtration methods have been devised for detecting multiplication of S. typhi in stored feces was observed. salmonellae in large volumes of sewage collected at a Tannock and Smith (1972) reported that S. single time. Hirn (1980) suggested that monitoring the typhimurium survived for 6-18 weeks (tgo = 150-450 effluent of food-processing plants for salmonellae was a hours) in sheep feces outdoors in New Zealand. useful contribution to the microbiological quality Survival was longer on shaded than exposed sites and control of the processed food. longer in summer than winter (presumably because of Reported concentrations of salmonellae in sewage the bactericidal effect of freeze-thaw cycles in winter). vary considerably. Concentrations per 100 milliliters of Berkowitz, Kraft and Finstein (1974) studied the 7-250 in India (Phirke 1974), 2-41 in South Africa survival of various Salmonella serotypes (typhimurium, (Grabow and Nupen 1972), 500 in Baltimore saintpaul, thompson, and infantis) inoculated into (Maryland, USA; Olivieri, Kawata and Kruse 1978), samples of wet poultry excreta (80 percent water) and 8,000 in Houston (Texas, USA; Davis 1979), up to 2.3 stored at various temperatures. Initial concentrations in Finland (Hirn 1980), up to 7,240 in northwest were 1.6 x 105-2.4 x 106 Salmonella per gram. England (Jones 1977), and 670 in Holland Overall persistence was usually less than I month; t90 (Kampelmacher and van Noorle Jansen 1970) have values (averaged over the first 3 log units' decline) been reported. averaged 184 hours at 9-12°C, 112 hours at 18-20°C, Several workers have recorded concentrations of and 40 hours at 30°C. Growth occurred before decline salmonellae in sewage that are difficult to explain by in sixteen of twenty-three tests, with concentrations of analyzing known inputs from patients, carriers, farm Salmonella rising to a maximum of 1.4 log units above wastes, or food-processing effluents. One such study in initial values. No clear pattern of differential survival Holland concluded that salmonellae must be multiply- among the four serotypes emerged. When samples ing in the sewerage system (Kampelmacher and van were allowed to dry for 2 days (12 percent water after 2 Noorle Jansen 1976). days) tgo values became 21 hours at 20°C. However, the The concentration of salmonellae in sewage may organisms that survived the 2 days drying then fluctuate on a regular basis. McCoy (1977) reported survived for considerably longer than in the undried that raw sewage in Hull (England) contained most 268 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA salmonellae (median concentration of 150-400 per 100 In sludge and slurry milliliters) during July-September and least durin ng s 2 January-March. Yaziz and Lloyd (1979) studied the Thecommonpracticeofapplyigsludgeandslurry to arable and pasture land has stimulated interest in hourly fluctuations of Salmonella concentrations in raw the occurrence and survival of salmonellae in these sewage at Guildford (England). Peak concentrations materials. Sludges from sewage treatment works will occurred at 0900-1000 hours, 2 hours before the peak almost always contain salmonellae. Reported cencen- flow of sewage at midday. Samples of raw sewage trations vary greatly and may fluctuate seasonally. In collected during the morning peak over a 9-month England, concentrations of salmonellae per 100 period contained 20- > 1,800 (median 130) Salmonella milliliters of raw sludge have been reported as around per 100 milliliters at Guildford and 11-1,600 (median 70 (median value), with 7 percent of samples containing 170) Salmonella per 100 milliliters at Woking a 1' S l pover 2,400 near Hull (McCoy 1977, 1979),40-1 1,000 in nearby town. Salmonella concentrations were higher in Yorkshire (Fennell 1977), and 4,000-23,000 in the the cooler months than In the summer. During the 1930s, a survey of sewage in Bandung northwest (Jones. F. 1977). In Switzerland, over 90 (Java,inde then1930s,asurvey had sewagein polati o percent of raw sludge samples contained Salmonella (Java, Indonesia)-whichthen had a populationo with maximum and mean concentrations of 106 and 200,000, of whom 40,000 were sewered-demonstrated 104 per 100 milliliters respectively (Hess and Breer the presence of typhoid bacilli in 62 out of 80 samples 1975; Obrist 1979). (Mom and Schaeffer 1940): S. typhi concentrations .' .' varied from less than 1,000 to 45,000 per 100 milliliters, Pike (1981 iEwed an salmonetain ' ' ..... . ' ~sewage sludges in England and Wales. Geometric with an average of 5,000 per 100 mitliliters. Despite mean counts per 100 milliliters of raw sludge reported individual accounts of high levels of Salmonella in develping from various regions were between 8 and 1,400. sewage, reported concentrations from Salmonellae were more numerous and more frequently countries are typically lower than from developed isolated from sludge at treatment works serving countries. This may reflect the greater input of effluents communities of 10,000-100,000 people than at works from food-processing plants in developed countries or serving larger or smaller communities. Common it may be an artifact caused by differences in laboratory Salmonella serotypes in sludge were those (particularly, technique. Daniel and Lloyd (1980) reported geomet- . . . agona, ryphlimuriuin. heidelberg, virchlow. anatu7n and ric mean concentrations of salmonellae in two refugee hadar) that infect a wide range of animals and man and camps in Bangladesh of only 7.1 and 7.7 per 100 milllilters, and they noted that these results could have nothshs-apederyes(uhsdblni bellilitenscau d bthey difficulty ofeselecsutive isoulatig cattle, abortus-ovis in sheep, cholerae-suis in pigs, and saeencaused fromhedifficultyf sewivery i sol'id gallinarum and pulloruitn in poultry) that are a major calmontenta ( fmillig e ite . r cause of salmonelloses in farm animals in the UK. coterae few00 siei s on Slte a s Interestingly, of the ten most common serotypes in sewage (see the apedies of Fachemla others sludge, six were among the ten most common serotypes in human infections and only four were among the ten 1980), and most attention has focussed instead on .' . . ~~~~~~~~~most common isolates from farm animal infections. survival in sludges and slurries (see below). tgo values of This suggestssthatesludge an is al onflando 77- 108 hours may be comnputed from the data of Green ta v . t . an.ead(13)on .iiawswaea .C , not play a major role in transmitting salmonellae and Beard (1938) on S. typhi in raw sewage at 7-20'C. S. tennessee inoculated at 109 per 100 milliters into among farm animals in England and Wales. Hall and strong Jerusalem (Israel) sewage (BOD 800-1200 Jones (1978) examined eight raw sludges from sewage treatment plants in England and found between 34 and milligrams per liter), survived for 22 days (r90 60 11,000 Salmonella per 100 milliliters. The most hours) in outdoor storage tanks in summer (Bergner- commonlyoisolat ery wee m inecreasin more Rabinowitz 1956). Gallagher and Spino (1968) of commonly oisolated serotypes were, in decreasing order reported the survival of S. typhimurium and fecal coliforms in various process waters and effluents at two I. In this context, -slurrv" refers to the mixture of animal feces. sugar beet factories in the USA. tgo values for S. urine, water. and sometimes some straw or other bedding produced typhimuriuim were generally over 72 hours and under at farms. This material may be rich in salmonellae: it has a solids 168 hours, and those for fecal coliforms were similar. In content similar to that of sewage works sludge (I -10 percent), and it the absence of other information, it is reasonable to presents disposal problems very similar to those of sludge produced at a sewage works receiving primarily domestic, rather than assume that Salmonella survival in sewage is similar to industrial. sewage The major distinction is between a sludge of that of fecal coliforms (chapter 13), with tgo values in primarily human origin and a slurry that contains the wastes offarm warm climates of 20-100 hours. animals. SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 269 typhimurium, paratyphi B, oranienberg, and kaapstad. increased as the solids content of the slurry was Only one of these serotypes, typhimurium, is a increased from 1 to 5 percent, but did not increase prominent cause of farm animal infection in Britain. further at solids contents above 5 percent. When the The frequency and concentration of salmonellae in survivals of eight strains (four serotypes) were animal slurries are typically lower than those in sewage compared (at 10°C and 5.5 percent solids), overall works sludges. The lower frequency is partly due to the survival times ranged from 90-140 days and appeared size of the contributing population; the herd of animals to be related to strain not to serotype. There was no on a typical farm is much smaller than the number of evidence of multiplication. Jones suggested that the people in a typical town. Jones and Mathews (1975) storage of slurry for 1 month prior to spreading on isolated Salmonella from 11 percent (20 of 187) of cattle pasture, followed by a further month during which the slurry samples taken randomly throughout England pasture is not grazed, would be a minimal treatment and Wales; concentrations were up to 180 per 100 regime for protecting cattle from Salmonella infection milliliters. Jones, Bew and Gammack (1975) isolated by this route. Salmonella from only 3 percent (2 of 63) of dairy factory Salmonellae can multiply vigorously in sterilized sludge samples in England. Jones and others (1976) sludge or slurry, but under natural conditions they are isolated Salmonella from 22 percent (12 of 54) of pig strongly inhibited by the activity of other microflora slurries in southern England at concentrations up to (Findlay 1973; Jones, Smith and Bew 1977). 2 x 105 per 100 milliliters. Kraft and others (1969) isolated Salmonella from the wastes of 50 percent (18 of In soil 36) of poultry farms in New Jersey (USA) at Salmonellae are likely to be found in soils that have concentrations of up to 3.4 x 106 per 100 grams. been treated with sludges, slurries, or effluents. Monitoring animal slurries for salmonellae can assist Reported survival times in several countries are: S. the detection and control of infection in the herds dublin for up to 12 weeks in the autumn in southern (Jones and Hall 1975). England (Taylor and Burrows 1971); S. dublin for 24 The literature on Salmonella survival in sludges and weeks in winter and 13 weeks in summer in northeast slurries is extensive (see the appendixes of Feachem England (Findlay 1972); S. typhimurium for more than and others 1980). Jones (1978), reviewing European 35 weeks in England (Mair and Ross 1960); S. literature, reports the survival of salmonellae in slurry typhimurium for 4-10 weeks in New Zealand (Tannock as being between 13 and 286 days. Strauch (1978) and Smith 1972); S. typhi for up to 17 weeks during the reported the survival of various Salmonella serotypes in rainy season in California (USA; Beard 1940); and S. animal waste slurries of up to about 1 year at 8°C and typhi for 5-19 days in Michigan (USA; Mallman and up to about 6 months at 17°C. At both temperatures Litsky 1951). and in four different slurries, S. enteritidis and S. cairo The long reported survival times represent residual consistently survived for longer than S. gallinarum, S. contamination by a very small proportion of the large typhimurium, or S. paratyphi B. Braga (1964) found that original inoculum of bacteria. Delage (1961) found that S. cholerae-suis survived for longer than S. typhi- 106 S. abortus-ovis in 1 gram of soil were reduced by murium, S. typhli, or S. enteritidis in sewage sludges at 6 99.9 percent after 50 days but were still detectable for and 28°C. Initial concentrations were 6 x 105 per 100 over 300 days. milliliters, and survival times ranged from 20-38 days Watson (1980) applied digested sludge, containing at 6°C and 4-9 days at 28°C. Findlay (1972) recorded 25-30 Salmonella per 100 milliliters, to cabbage fields the survival of S. dublin in cattle slurry in northeastern at a rate of 70 cubic meters per hectare. Survival times, England for 31-33 weeks in winter and 18-19 weeks in during spring and summer in northern England summer. Ekesbo (1979) found that S. dublin and S. (temperatures 3-32°C), were 42-49 days, with tgo zanzibar survived for at least 13 weeks in cattle slurry values of 336-528 hours. Chandler and Craven (1978) (8-9 percent solids) and settled cattle slurry (5-6 also reported about 8 weeks survival for S. percent solids) at 5°C. typhimurium on dry soil in Australia. Jones (1976) experimented with various Salmonella Zibilske and Weaver (1978) studied the effect of soil serotypes inoculated into cattle slurry from a dairy. type, moisture, and temperature on the survival of S. When S. dublin was inoculated at 106 per milliliter into typhimurium applied to soil in cattle slurry or saline. slurry (4.7 percent solids), tgo values were 528 hours at Survival was inversely proportional to temperature but 5°C and 10C, 228 hours at 20°C, and 52 hours at 30°C. was not obviously related to soil type or delivery Overall survival times were 132 days at 5°C and 10°C, medium. At 22°C survival times ranged from 3 days 57 days at 29°C, and 13 days at 30°C. Survival (tgo = 17 hours) to 84 days (tgo = 483 hours). 270 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Dazzo, Smith and Hubbell (1973) studied the Williams 1975. 1979) has been accumulated in West survival of S. enteritidis in fine sand (soil moisture 10 Germany, Holland, and Switzerland (Hess and Breer percent), which was returned to the laboratory 1975; Obrist 1979) to suggest that the use of following different regimes of cattle slurry application. inadequately treated sludges and slurries on pasture is Samples were stored in darkness at 22°C. Death rate a major factor in spreading bovine Salmonella was inversely related to the rate at which the sand had infections. Some countries, Switzerland among them, received slurry. When no slurry was applied, overall have banned the use of unpasteurized sludge on survival was 8 weeks (from an initial concentration of pasture in summer (Williams 1979). In the UK, a 106 Salmonella per gram of soil), and the tgo was 254 general association between sludge application to hours. At the maximum rate of slurry application pasture and salmonellosis in grazing animals has not tested (508 cubic meters per hectare per week), the tg0 been demonstrated. Wray and Sojka (1977) reviewed was 363 hours, and over 100 Salmonella per gram of soil the subject and mention that, in addition to remained after 8 weeks. The effect of slurry application documented outbreaks in which pasture contam- in enhancing Salmonella survival in fine sand was not ination has been implicated (for instance, Jack and due to moisture content, since this was controlled at 10 Hepper 1969), the salmonellosis peak in cattle in many percent throughout each experiment. European countries occurs in late summer when the Bergner-Rabinowitz (1956) studied the survival of S. cattle are grazing and that the incidence declines tennessee seeded into sewage (at about 108 per 100 markedly when cattle are brought indoors for the milliliters) and applied to soil of low organic content winter. This is scarcely evidence; the human salmonell- near Jerusalem (Israel). During the winter (air osis peak occurs at the same time. and people neither temperature 2-21°C), at the soil surface (soil moisture graze contaminated pasture nor contract most of their 8-39 percent) overall survival times averaged 46 days, infection from contaminated beef and milk. Further whereas at a depth of 100 millimeters (soil moisture evidence against the importance of pasture con- 19-30 percent) survival was for 70 days. Coliforms tamination in cattle salmonellosis is the high infective were still detectable in low concentrations after 74 dose of Salmonella (see the subsection on transmission, days. During the summer (temperature not given) above, and the studies of Taylor 1973 and Taylor and survival at the surface (soil moisture 4-23 percent) was Burrows 1971). 15 days, and at 150 millimeters depth (soil moisture The interim guidelines produced by the Commission 17-29 percent) 11 days. These experiments were all on of the European Communities (Kelly 1978) recom- uncultivated plots using a single application of sewage mended that, ideally, slurry should be applied only to seeded with S. tennessee. In subsequent experiments in arable land. If applied to pasture. it should receive a summer, S. tennessee in sewage was applied to plots minimum of 60 days storage before spreading. and growing sunflowers, and the plots were reirrigated with there should be a further interval of 30 days before sewage not containing Salmonella every 6-8 days (in grazing. Only healthy adult animals should be grazed line with normal practice in Israel). Survival at the on treated pasture. surface (soil moisture 4-31 percent) was increased to Hess and Breer (1978) reported that salmonellae on 23 days, and at a depth of 150 millimeters (soil moisture grass treated with sludge could survive for up to 16 18-30 percent) to 37 days. months in Switzerland. Most reported survival times These and other studies show that salmonellae can are much shorter than this. In New Zealand, Josland survive in soil for periods of many months when (1951) reported survival of S. typhimurium on pasture of conditions are ideal. The factors most affecting survival 12-24 weeks, and Tannock and Smith (1971) reported are temperature, exposure to sunlight, and the 6-14 weeks for S. typhimurium and 2-8 weeks for S. moisture content, pH, and the organic content of the borlis-morbificans. soil (Gerba, Wallis and Melnick 1975; Rudolfs, Falk Taylor and Burrows (1971) applied cattle slurry (0.2 and Ragotzkie 1950). In hot and sunny climates, percent solids) containing 109 S. dublin per 100 maximum survival times may be around 2 months, milliliters to pasture during September-December in with almost complete elimination after 2 weeks. southern England. S. dublin survived for 11 days on grass 75-150 millimeters above ground, 18 days on Oni pastuire grass at ground level, and 12 weeks in the soil. In similar experiments, with slurry impregnated with 108 The role of sludge and slurry application to pasture E. coli per 100 milliliter. E. coli survival was only 3 days in transmitting Salmonella infections remains con- at 75-100 millimeters, 7 days at ground level, and 11 troversial. Considerable evidence (reviewed by days in soil. Calves, given a choice of contaminated and SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 271 uncontaminated pasture, avoided the contaminated readily removed by washing. Lovett and Francis (1976) pasture for 2 days but then grazed it. When twelve concluded that fecal coliforms were good indicators of calves were grazed on pasture that had been treated Salmonella survival on vegetables, but that coliforms with slurry containing 108 avirulent S. dublin per and fecal streptococci were not. milliliter, eight showed evidence of infection. None of The use of waters containing sewage effluents to six calves was infected when grazed on pasture treated irrigate crops is commonplace in developing countries with slurry containing 105 avirulent S. dublin per 100 and will increase as growing urban populations milliliters. produce more wastewater and create an increasing Salmonella survival on pasture is considerably market for intensively cultivated crops. The risks of shorter than in soil and is shorter high up the blades of crop contamination are reduced by adopting drip, grass than near the ground. Heat, desiccation, and furrow, or subsurface irrigation methods instead of sunlight are all lethal factors, and survival on pasture in using spray or flood irrigation. A further safeguard is to the tropics is unlikely to exceed 10 days. discontinue irrigation or fertilization with fecal materials 2 weeks prior to harvesting; the survival of On crops salmonellae on crop surfaces will be very much reduced by heat, sunlight, and low humidity. If these precautions Several outbreaks of salmonellosis and typhoid have are taken Salmonella survival on crops is unlikely to been linked to the contamination of vegetables and exceed 10 days in hot and arid climates. fruit by sewage or sludge (Geldreich and Bordner 1971). Gayler and others (1955) linked an outbreak of Infish and shellsh gastroenteritis due to S. miami with sliced watermelon and showed that the act of cutting a dirty watermelon Fish and shellfish from unpolluted waters, such as could contaminate the inner fruit and that multipli- the open sea or mountain streams, do not contain cation of S. miami in the melon could then occur. Sixty- salmonellae. Fish and shellfish living in waters polluted eight percent of lettuce and 72 percent of fennel samples by waste discharges are commonly found to harbor marketed in Bari (southern Italy) were contaminated Salmonella (Buttiaux 1962). Salmonellae are not with salmonellae (Ercolani 1976). Twenty-two percent known to cause disease in fish or shellfish, but they do of vegetables purchased in Holland contained salmon- cause temporary infection when the fish or shellfish are ellae, and contamination was especially prevalent on residing in waters containing salmonellae. Fish or tropical imports (Tamminga, . Beumer and Kam- shellfish can be decontaminated by placing them in pelmacher 1978). clean water, but salmonellae seem to be eliminated In Colorado (USA) 100 percent of settled sewage rather more slowly than enteroviruses or E. coli. samples contained salmonellae (concentrations Fish caught in deep-sea areas are free of Salmonella 43-360 per 100 milliliters), and 63 percent of irrigation but may become contaminated prior to sale. Likely water samples from streams receiving raw or treated means of contamination are from ice made from sewage contained salmonellae (concentrations 1-360 polluted water, from storage in contaminated boxes or per 100 milliliters) (Dunlop and Wang 1961). Only I baskets, and from handling by infected packers or out of 97 samples of irrigated turnips, cabbage, process workers. When salmonellae are isolated from spinach, endive, and lettuce contained Salmonella. This fish intestines, contamination in polluted water is was attributed to the inadequate laboratory methods, indicated; when salmonellae are isolated only from which could only detect high levels of contamination, external surfaces, contamination during transport and and to the use of furrow irrigation on sandy soil in a dry handling is more probable. The contamination of fish climate, which minimized the survival of salmonellae. mealusedasahighproteinfoodforpoultryandpigshas Salmonella survival data (see the appendixes of been of great importance in the epidemiology of Feachem and others 1980), reviewed by Geldreich and salmonelloses in Europe in recent years. Bordner (1971), indicate up to 53 days on root crops, Geldreich and Clark (1966) studied the survival of up to 40 days on leafy vegetables, up to 5 days on various enteric bacteria in the sterilized intestinal berries, and over 2 days on orchard crops. Two early contents of fish. In carp intestinal contents (pH = 7.3) studies of S. typhi on radish and lettuce showed survival at 10°C, S. typhi, S. typhimurium, Shigellafiexneri, and for 10 days in sunny sites and for 31 days in the shade fecal coliforms declined, whereas fecal streptococci (Creel 1912) and for 21-37 days (Melick 1917). The grew slowly. At 20°C, fecal streptococci grew rapidly, latter study also showed that S. typhi became attached fecal coliforms and S. typhimurium grew slowly, and S. to leaves lying on contaminated soil and were not typhi and Sh. flexneri declined. In bluegill intestinal 272 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA material (pH = 8.0) at 20°C, all species of bacteria coli elimination (DiGirolamo, Liston and Matches tested grew rapidly except S. typhi. 1975; Hedstrom and Lycke 1964; Hoff and Becker In order to clarify the risks of salmonellosis 1969; Mitchell and others 1966). associated with fish culture in sewage effluents, Slanetz, Bartley and Stanley (1968) studied salmon- Heuschmann-Brunner (1974) experimented with carp ellae in water and oysters in an estuary at Portsmouth and tench kept in water heavily contaminated by S. (New Hampshire, USA). Water salinities were 1.1-2.5 enteritidis and S. typhimurium. A few hours residence in percent and temperatures were 8-26°C. Salmonellae heavily polluted water caused infection, and Salmnonella were readily isolated from water in which the coliform spread rapidly along blood and lymph vessels count was below the limit recommended for shellfish- throughout the body, including the musculature. growing waters (70 per 100 milliliters) and were on two Salmonellae were found most often, and for the longest occasions isolated from shellfish that met the coliform time, in the digestive tract. At 9-12°C, Salin,nlcllI standard (less than 230 per 100 grams). On three infection persisted in the tench gut for 60 days and in occasions salmonellae were isolated from estuarine the carp gut for 68 days. In warmer water, infection waters and shellfish containing no fecal coliforms per persisted for longer-the reverse of what occurs with 100 milliliters and per 100 grams, respectively. depurating shellfish, which cleanse themselves faster in Jegathesan and others (1976) studied 38 shellfish warmer water because their rate of filter feeding bought at markets in Malaysia. Three species were increases. Lesions in the gut were produced by massive included: cockles (Anadura granosa) cultivated on intralymphatic injection of salmonellae. Salmonellae muddy shores of the Malaysian west coast and mussels isolated from fish several weeks after exposure were (Modiolus senhaussi and M. metcalfi) harvested from still pathogenic to mice. A great deal more research is muddy and sandy shores, respectively. Cockles are required on the uptake and elimination of Salmonella commonly eaten half-boiled, whereas mussels are by fish grown in sewage in developing and tropical normally fried or baked. Two specimens contained countries. ',,Ii . Shellfish are often harvested from estuaries where polluted or potentially polluted waters flow into the sea. Salmonellae may be concentrated in the flesh of In tue air filter-feeding molluscs in the same manner as enteroviruses (chapter 9) and E. coli (chapter 13). Salmonellae are likely to be aerosolized and Salmonellae are frequently isolated from shellfish dispersed from flush toilets, spray irrigation devices, harvested from contaminated waters and have given and activated sludge plants in the same manner as E. rise to major and many minor outbreaks of coli (see chapter 13). Comparatively few data on salmonelloses and enteric fevers (Buttiaux 1962). airborne Salmonella are available because they have Depuration of shellfish, by placing them in clean water. been seldom studied and because they are present seems to be less effective in removing Salmonella than sporadically or in low concentrations in feces and in removing enteroviruses (chapter 9) and E. coli sewage and so are far more difficult to detect in the air (chapter 13). than E. coli. Janssen (1974) took oysters (Crassostrea uirginica) Newson (1972) added 10'°1o01l S. typhimw'iwin to from the Chesapeake Bay (USA) and kept them in an toilet bowls and flushed, producing an average aerosol aquarium with salinity of 1.5 percent and water of 132 -'. .',. li, per cubic meter of air. The survival temperature of 20°C. Oysters were exposed to artificial ability of Salmonella in splashes produced by toilet seawater containing 2 x 107 S. typhimurium per 100 flushing wastested by studying 0.1 milliliter droplets of miltiliters for 48 hours and then kept in clean water water and feces, containing 108 S. typhimurium, on a continually decontaminated by ultraviolet light. laboratory bench. Salmonella survived for 12 days in Oysters accumulated S. typhimurium up to a con- both aqueous and fecal droplets, compared with 2-11 centration of 2.8 x 104 per oyster and still contained days for E. coli and 5 days for Shigella sonnei in parallel 170 per oyster after 42 days in sterilized water. In other experiments. Katzenelson, Teltch and Shuval (1977) experiments in which the depuration water was only detected S. infantis 60 meters downwind from spray intermittently sterilized by ultraviolet light, oysters irrigators delivering raw sewage in Israel (see also excreted S. typhimurium for 14 days and after 49 days Katzenelson and Teltch 1976). Hickey and Reist (1975) still contained 6,000 per mollusc. These rates of and Pereira and Benjaminson (1975) failed to detect Salnmonella elimination by oysters in clean water are far Salmonella downwind of activated sludge tanks and slower than the reported rates for enteroviruses and E. grit chambers in the USA. SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 273 Inactivation by Sewage Treatment influent were reduced by 98.8 percent (tgo = 100 Processes hours). From the data on survival in sewage reviewed above The literature on Salmonella in sewage treatment and in the appendixes of Feachem and others (1980), it plants is limited, both in coverage of the various may be concluded that Salmonella removal in septic technologies and in the quality of the experimental tanks is unlikely to exceed 95 percent and will be very procedures. Some studies are reviewed below, and much less in an overloaded or sludge-filled unit. others are listed in the appendixes of Feachem and others (1980). Unless otherwise stated, it may be By conventional treatment assumed that removal of Salmonella during sewage treatment processes is similar in nature and degree to Perhaps the most detailed study on Salmonella removal of E. coli (chapter 13). removal in conventional treatment plants is that on the trickling filter plant at Woking and the activated By, primary and secondary sedimentation sludge plant at Guildford (both in the county of Surrey in southern England) reported by Yaziz and Lloyd Mom and Schaeffer (1940) recorded that an Imhoff (1979). The results are summarized in tables 15-3 and tank at Bandung (Indonesia) reduced an influent S. 15-4. Whereas the efficiencies of the two primary typhi concentration of 5,100 per 100 milliliters to an sedimentation systems are similar (79 percent removal effluent concentration of 800 per 100 milliliters (an 84 at Woking, 73 percent at Guildford), the performance percent reduction). Data on the removal of salmonellae of the activated sludge plant is very much better in by primary and secondary sedimentation at two terms of Salmonella removal than that of the trickling treatment plants in southern England are given in filter plant. This difference results in a total removal of tables 15-3 and 15-4, below, and are discussed in the only 93 percent (1.2 log units) of Salmonella at Woking section below on conventional treatment. Further compared with 99.86 percent (2.9 log units) at literature is cited in the appendixes of Feachem and Guildford. Judging from the extremely good BOD5 others (1980). removal performance of the two plants, they were in Although the number of studies reported is small, it good operating order and were not overloaded. It is may be concluded that Salmonella removal during likely that the Salmonella removal rates reported are sedimentation is similar to fecal coliform removal close to the maximum achievable by full scale plants (chapter 13) and that salmonellae become con- employing conventional trickling filter and activated centrated in the sludge, as do all excreted viruses and sludge processes. Many plants that are poorly designed bacteria undergoing sedimentation. or maintained, or that are overloaded, will achieve considerably lower removal rates. Studies on four treatment plants in Holland showed overall Salmonella removals of 90 percent, 94 percent Salmonellae, like all enteric pathogens, are not and 79 percent in three trickling filter plants and 99.4 normal residents of the healthy gut and are found only percent in an activated sludge plant (Kampelmach- sporadically, and in widely varying concentrations, in er, Fonds and van Noorle Jansen 1977 and sewage treatment systems serving individual buildings Kampelmacher and van Noorle Jansen 1970). Early or small clusters of buildings. Surprisingly, a survey of laboratory studies on S. typhi showed a 90-99 percent seven septic tanks in the USA detected Salmonella in 15 reduction after 6 hours aeration in activated sludge percent (4 of 27) of effluent samples even though the and 95-99 percent reduction by trickling filters (Green average number of people per septic tank was only 3.9 and Beard 1938). Green and Beard (1938), like other (Small Scale Waste Management Project 1978). early workers, were impressed by removal efficiencies Green and Beard (1938) simulated a septic tank in of 95 percent and wrote that conventional treatment the laboratory and found that S. typhi in the 'may be expected to reduce greatly typhoid organisms supernatant liquor at 15-21°C declined at a t90 rate of present in sewage, and are, therefore, effective barriers 52 hours. Howard, Lloyd and Webber (1975) installed for the protection of public health." This view, an Oxfam sanitation unit (two large flexible septic although widely held, was and is erroneous. It is only tanks in series) in the yard of the cholera hospital in more recently that researchers have emphasized that, Dacca (Bangladesh). At a mean retention time of 8 with high influent concentrations, 90-99 percent days (4 days in each tank), and sewage temperatures of removal rates are poor and that, in any case, most of 22-32°C, the 2,900 Salmonella per 100 milliliters of those Salmonella removed from the liquor are 274 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 15-3. Salmonella removal at the Woking tricklingfilter plant, UK Salmonella per 100 milliliters Percentage reduction Sewage and process Minimum Maximnum Median Minimum Maximum Mean Raw sewage' 11 1600 170 Primary sedimentationb 29 99.00 79' Settled sewage 1 160 20 Trickling filters -92.3d 91.7 68 Trickling filters plus secondary sedimentation 86 99.6 92.3 Final effluent' 0 250 3 Total plant 64 100 93.0 Source: Adapted from Yaziz and Lloyd (1979). a. BOD5 = 194 milligrams per liter. Total flow - 7,600-12,100 cubic meters per day. b. 6-7 hours' detention. c. Salmonella removal correlated with suspended solids removals (r = 0.82). d. Increase of 92.3 percent. e. BOD5 = 7 milligrams per liter. concentrated in the sludge, which then presents its own treating cattle slurry (0.5-1.0 percent solids). treatment and disposal problems. Maximum survival times were 17 days under simulated Kabler (1959) reviewed several studies on S. typhi summer conditions (20"C) and 47 days under removal by conventional treatment. These, plus other simulated winter conditions (2°C). When oxidation studies mentioned above and in the appendixes of ditch effluent was held in a settling chamber, S. Feachem and others (1980), indicate removal by typhimurium survived for 66 days in the liquid layer and trickling filter plants of 75-95 percent and by activated 87 days in the sludge layer at 2-3°C. sludge plants of 90-99.9 percent. In other words, Oxidation ditches are commonly used in Holland to Salmonella removal by these processes is similar to the treat the sewage of small communities, and two were removal of fecal coliforms (chapter 13). studied by Kampelmacher and van Noorle Jansen (1973). Salmonella concentrations per 100 milliliters ranged from 23 to 2,400 in the influent and from 0 to By oxidation ditch 350 in the effluent. Salmonella reductions of 90-99 percent were recorded. Kampelmacher and van Noorle Will, Diesch and Pomeroy (1973) studied S. Jansen (1971) also studied an oxidation ditch treating typltimurium in a 1:10 scale model oxidation ditch pigwastesinHolland.ConcentrationsofSalmonellaper Table 15-4. Salmonella removal at the Guildford activated sludge plant, UK Salmonella per 100 inilliliters Percentage removal Sewage anid process Minimtunm Maximum Medlian MiniLmum Maximtiin Mean Raw sewage' 20 > 1,800 130 Primary sedimentation' 35 96.9 73' Settled sewage 7 250 35 Activated sludge' plus secondary sedimentation 93.6 100 98.7 Final effluent' 0 1.7 0.1 Total plant 98.7 100 99.86 Source: Adapted from Yaziz and Lloyd (1979). a. Bon5 = 259 milligrams per liter. Total flow = 7,600-22,800 cubic meters per day. b. 6-7 hours' detention. c. Salmonella removal correlated with suspended solids removal (r = 0.651. d. 6-9 hours' detention in the activated sludge tanks. e. BOD, = 8 milligrams per liter. SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 275 100 milliliters were 33-1,600 in the influent, 3-75 in the LAGOONING. Lagooning of secondary effluents will ditch, and 1-12 in the effluent. remove salmonellae if retention times are long enough. Removal will be greatly enhanced at warmer temperatures. The secondary effluent from an acti- By waste stabilization ponds vated sludge plant in London (England) was held in Joshi, Parhad and Rao (1972) studied bacterial three lagoons in series with a total retention time of 17 removal in a series of three ponds, with total retention days (Metro.politan Watr Board 1963-64)' The lagoon influent contained 0.2-29 salmonellae per 100 time of 7 days, near Nagpur (India). Salmoefella ilfluent contained 0-0.2 per 100 concentrations in the influent were 4-540 per 100 milliliters, and none was detected in the effluent. The ml reductions of coliforms, E. coli, and fecal streptococci DISINFECTION. Brezenski, Russomanno and in the same ponds were in the range 99-99.9999 DeFalco (1965) studied the effluents and receiving percent. In a subsequent study (Joshi, Parhad and Rao w ' . ~~~waters of four sewage treatment plants discharging 1973) on two ponds with 12 days total retention in into Raritan Bay (New York-New Jersey, USA). The Nagpur, Salmoniella were present in the influent (3-100 treatment plants incorporated primary treatment per 100 milliliters) and in all effluent samples . . c . (qualitative determinations only). Reductions of (sedlmentation) and chlorination (0 25-2.5 millras indicator bacteria were only 43-98 percent. The striking per liter of combined chlorine residual). When effluents difference in performance between the two sets of ponds were chlorinated, no salmonellae were isolated from was~~~~~~ ~ atrbue tosotcrutn.n orydsge the effluents or receiving waters. When chlorination was attributed to short-circuiting and poorly designed was suspended for 1 week, salmonellae were recovered interpond connections in the second set of ponds. Two from two of the effluents and from the receiving waters. ponds in series in Lima (Peru), with total retention of 37 Kampelmacher, Fonds and van Noorle Jansen days and temperatures of 18-27'C, yielded salmonellae (1977) studied three sewage treatment plants in (mainly paraty phi B. der-bv and newport) in all influent Holland discharging effluents into lakes used for and effluent samples (Yanez 1980). This must reflect recreation during the summer. Plant 1 had trickling poor pond design and major short-circuiting. filters followed by chlorination (6 milligrams per liter As far as is known, the processes affecting chlorine added); plant 2 had trickling filters. aeration, salmonel.ae removal in ponds are the same as thosechlori- determining the removal of indicator bacteria (chapter na tion i ra persliter chlorin added);oand 13). One study suggested that Salmonella death rates in panto3 ha activater slude chlorineatin( ponds were similar to those of E. coli (Davis and pmilligrams per liter of chlorine added) Reductions of Gloyna 1972). More commonly it has been found that SaGl a by bitolgca tlrine atm eiue tiompare Salmonella reduction is significantly less than that of Salmonella by biological treatment (influent compared Saliformon Ell reducion iscal signifi cca l ess thn th at of with effluent prior to chlorination) were 94 percent in coniforms, c'l, ortfean s occie in theksam plant 1, 79 percent in plant 2, and 99.4 percent in plant ponds~~ ~ (tbl 133'ote n oui 95 akr 3. Salmonella concentrations per 100 milliliters were Carbonnelle and Leclerc 1977). The removal rate for 2- Salmin inuents ation bere ch lition 0-wer salmonellae in ponds is very temperature dependent: 2-> 104 in influents, 0-104 before chlorination, _103 higher removal is obtained in summer than in winter after chlorination, and 0-103 in the receiving lake (for instance, Slanetz and others 1970), and ponds in Ninety-two percent (68 of 74) of samples contained the tropics remove salmonellae more effectively than Salmonella before chlorination, whereas only 17 those in temperate climates. percent (9 of 52) were positive afterward. Schiemann, Brodsky and Ciebin (1978) compared three methods of disinfection of an activated sludge By tertiary treatment plant effluent in Ontario (Canada) with respect to their ability to remove wild Salmonella. Salmonella were The realization that salmonellae, like all excreted recovered from 89 percent of primary effluent samples, viruses and bacteria, may be present in moderately 73 percent of secondary effluent samples, 13 percent of high concentrations in the secondary effluents of chlorine dioxide treated effluent samples, 8 percent of conventional sewage treatment plants has stimulated ozonated effluent samples, and 0 percent of chlorinated some research into Salmonella removal by tertiary effluent samples. processes. In the absence of other information it may Oliver and Carey (1976) reviewed data showing that be assumed that Salmonella behave like fecal coliforms S. typlhi was inactivated by chlorine and ultraviolet during tertiary treatment (chapter 13). light to the same degree as E. coli but was considerably 276 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA more resistant to ozone. This finding was not By anaerobic digestion supported by Burleson, Murray and Pollard (1975), Pike (1981) reviewed data on Salmonella removal by who found that S. typhimurium and E. coli had a similar sludge digestion at various sewage treatment plants in response to ozone, both in saline and secondary E effluent. England and Wales. Reductions Salmonella concentrations were between 16 and 98 percent. Two mesophilic digesters in Yorkshire (England) with LAND TREATMENT. Near Phoenix (Arlzona, USA) g ' mean retention times of 30 days, were receiving on secondary effluent from an activated sludge plant was . . . average 5,900 and 2,500 Salmonella per 100 milliliters treated by intermittent floodingontos and putting out on average 3,600 and 37 Salmonella per (Gilbert and others 1976). Secondary effluent con- 100 milliliters-thus achieving very different removal tained, on average, 21 Salmonella per 100 milliliters efficiencies of 39 and 98.5 percent, respectively (Fennell and no Salmonella were detected from ground water 9 1977). Stokes and others (1945) found that S. meters under the slte. The Salmonella had been removed 1977). Sok ad oters (4 found thats by prcoatio ofwastwatr troug 1 eterof ine typhimurium could be detected in sludge after 45 days by percolation of wastewater through I meter of fine anaerobic digestion at 26°C. loamy sand and 8 meters of sand and gravel,.neoi iesina 6C Obrist (1979) reported that approximately 70 percent of the 2 million cubic meters of municipal sewage sludge produced annually in Switzerland is Inactivation by Night Soil and Sludge applied to land, and of this 52 percent is applied to Treatment Processes pasture and forage crops. Raw sludge contained Salmonella in 91 percent of samples, with maximum and mean concentrations being 10' and 104 per 100 The realization that 70-99 percent of salmonellae milliliters respectively. Digested sludge contained entering a sewage treatment plant are concentrated in Salmonella in 81 percent of samples, with maximum the sludge, and the widespread use of sludge in and mean concentrations being 105 and 102 per 100 agriculture, have stimulated an increasing amount of milliliters respectively. research on the fate of salmonellae during sludge Dudley and others (1980) studied the bacterial treatment. More research is urgently needed on content of digested sludges from three sewage salmonellae in simple sludge treatment processes treatment plants in the southern USA. Salmonella (storing, drying, and composting) in warm climates concentrations were 200-2,400 per 100 milliliters. and on the fate of salmonellae in night soil treatment Cooke, Thackston and Malaney (1978) studied and disposal systems in developing countries. Salmonella removal by three anaerobic mesophilic digesters at sewage treatment plants near Nashville (Tennessee, USA). Digester 1 had a mean retention Bx, pit latrines time of 9 days, operated at 34°C, and reduced Galvagno and Calderini (1908) reported S. typ/li Salmonella concentration by 98 percent. Digester 2 had survival in pit latrines for 15-30 days. Survival may be a retention time of 50 days, operated at 37°C, and estimated from reports on survival in feces, night soil reduced Salmonella concentrations by 99.4 percent. sludge. and slurry (see above and the appendixes of Digester 3 had a retention time of 38 days, operated at Feachem a anothers 1980). 36°C, and removed 99.9 percent of salmonellae. Mom and Schaeffer (1940) studied sludge digestion in an Imhoff tank in Bandung (Indonesia). Raw sludge contained 0-2,400 S. typhi per 100 milliliters; after 30 By storage days digestion at 27°C, the concentration was 0-2,200 Sludges stored for long periods will normally be free per 100 milliliters. from Salmonella. In Yorkshire (England) lagooned raw Clearly, mesophilic digestion produces a sludge that sludges over 1 year old were negative or gave low may still retain a considerable population of counts commensurate with possible recontamination Salmonella. Thermophilic anaerobic digestion at (Fennell 1977). Jones, P. (1977) found Salmonella in 50 around 500C will certainly eliminate Salmonella if percent of lagooned sludge samples less than 2 years operated as a batch process with a retention time of 5 old, but in no samples more than 2 years old. Jones days or more. Under continuous feed Salmonella (1975) reported that S. duiblin underwent no loss of elimination can never be guaranteed, although virulence when stored in cattle slurry for 1 month at concentrations in the digested sludge should be very tO0C. low. SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 277 65 - - 65 - ~~~~~~~~ZONE 60 - - 60 ~~~~~~~~~OF 55 SAFETY - 55 50 - - 50 45 --45 40 - 40 35 35 30 ~~~~~~~~~~~~~~~~~~~~~~~~~~~~30 zU 25 - * - 25 20 - X 20 15- X,1 15 10 x 100% destruction of Salmonella 10 5 less than 100% destruction of Salmonella 5~~~~~~~~~~~~~~~~~~~~~ s5 0 I 0 0.1 10 100 1000 10000 Ihour iday lweek Imornth lyear TIME (HOURS) Figure 15-2. The influence of tiune and temperature on7 salmonellae. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death By aerobic digestion their levels of Salmonella contamination for up to 85 Thermophilic aerobic digestion (wet composting) is days. Stokes and others (1945) inoculated sludge (5.8 similar to composting in its effect upon enteric bacteria. percent solids) with 2.5 x 109 S. paratyphi B per 100 milliliters and found that they were detectable after 27 If temperatures are maintained at the required level for y the required time (figure 15-2) throughout the sludge days (solids content 36 percent), but not after 41 days mass, total destruction of Salmonella will occur. Smith, (solids content 43 percent), on sludge drying beds in Young tand Dealn 1975)reported reduawllctionsml in England during the summer. In similar experiments Youngea Da (1975) ore redionstin conducted during December-June with S. typhi- Salmonella of 99.8 percent in one aerobic digester mtirium, the bacteria could be detected after 180 days (t m erature 469CC retention 4 days) and 100 percent on the drying beds, by which time the solids content in another (temperature 49°C, retention 4 days). had risen to 86 percent. Aeration of stored slurry is used on some farms to promote bacterial dicoff. Willinger and Thiemann (1978) found that S. typhimurium survived for 6-12 days in continuously aerated cattle slurry in Austria. By heating Average ambient temperature was 3-24°C, whereas All high temperature processes, such as pasteuriz- the temperature in the aerated slurry was 29-35°C. E. ation, wet oxidation, and the Porteous process, will coli survival in the same experiments was 9-12 days. eliminate Salmonella from sludge. Pasteurization is commonly used in Switzerland to treat digested or By drying aerobically stabilized sludges prior to land application (Obrist 1979). Sludge is heated to 70°C for 30 minutes Pike (1981) reported that raw and aerobically bysteaminjection. Hess and Breer (1975)reported that digested sludges on drying beds in England maintained pasteurized sludges from five treatment plants 278 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA contained less than 10 Enterobacteriaceae per gram in salmonellae again increased initially but were unde- 98-1O0 percent of samples. tectable after 10 days (Burge, Cramer and Epstein In many situations, and especially in developing 1978; Kawata, Cramer and Burge 1977). The countries, the more practical and appropriate technol- importance of management and process control are ogies for harnessing heat to destroy pathogens in illustrated by the poor Salmonella removal properties sludge are aerobic thermophilic digestion (see above) of a digested sludge plus sawdust composting plant at and composting (see below). The time-temperature El Paso (Texas, USA) reported by Reeves (1959). requirements for the destruction of salmonellae are Samples of compost from Vietnamese double-vault shown in figure 15-2, and it may be seen that 1 hour at composting toilets (retention times 6-7 weeks) have 60°C, 1 day at 50°C, and 1 week at 45°C are lethal been found not to contain Salmonella (Nimpuno, combinations. personal communication). These results must be treated with caution, however, because they may result from studies of toilets operating under controlled, By composting experimental conditions. In laboratory experiments on composting poultry To eliminate salmonellae, all parts of the compost- excreta, S. typhimurium were eliminated after 19 hours ing mass have to be brought to a warm enough of composting during which the temperature rose to temperature for a long enough time (figure 15-2). This 64°C at hour 10 (Platz 1978). Salmonellae were more generally requires the presence of a carbon source readily eliminated by composting when inoculated into (refuse, straw, or woodchips), careful moisture control, the compost than when held in sealed glass ampoules and a supply of oxygen throughout the mass provided within the compost, and this indicates that factors by turning or forced aeration. other than heat were contributing to bacterial death. In both cases 'm ,.. -l-a could not be detected after Bv coagulation and vacuum filtration temperatures had risen to about 62°C. Wiley and Westerberg (1969) determined that S. Sludge coagulation followed by vacuum filtration is newport in nutrient broth was destroyed in 40 minutes commonly used to dewater sludges in some developed at 60°C and in 30 minutes at 65°C. Dewatered primary countries. Kampelmacher and van Noorle Jansen sludge, containing 2.4 x 106 S. newport per gram, was (1972) studied three treatment plants in Holland; two then treated for 5 days in a continuously mixed, forced plants added lime and ferrous sulfate prior to vacuum air, laboratory composter containing 1.1 cubic meters filtration, whereas the third used lime and ferric of sludge. The temperature within the composter was chloride. The solids contents were 4-10 percent and 60-760C. S. newport was not detectable in the sludge 25-30 percent, respectively, before and after dewater- after 25 hours of composting. ing. At the three plants raw sludge contained Savage, Chase and MacMillan (1973) experimented salmonellae in 59, 65, and 100 percent of samples, with various regimes for composting pig wastes (a whereas dewatered sludge contained salmonellae in combination of uneaten garbage and pig feces) in New only 5, 5, and 14 percent of samples. The bactericidal Jersey (USA). In a windrow comprising 36 tons of pig properties of this process are due to the addition of waste that was turned twice per week, Salmonella coagulants and especially to their action of raising the concentrations rose from day 0 (temperature within pH. windrow 36°C) to day 40 (temperature 48°C) and then declined to negligible levels by day 187 (temperature By lime treatment 68°C). In another windrow, comprising 36 tons of pig waste plus 1.4 tons of straw, turned 20 times per week, Any sludge treatment process involving the addition temperatures rose to 72°C within 10 days and of lime is likely to produce a sludge free from remained above 60°C for 20 days. Coliforms, and salmonellae. Pike (1981) reviewed sludge treatment presumably also salmonellae, were eliminated within data for England and Wales and found that lime 14 days. treatment was highly effective in removing Salmonella. The effect on enteroviruses and coliforms of the composting experiments at Beltsville (Maryland, .a . USA) are described in chapters 9 and 13. In windrows By irradiaton of sludge and woodchips turned daily, salmonellae Experiments in the Federal Republic of Germany grew at first but were eliminated after 14 days. In piles showed that 102_103 wild Salmonella in 100 milliliters of sludge and woodchips subjected to forced aeration, of raw sludge could be reduced to zero by the SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 279 application of 3 kilogray (Lessel and Suess 1978). Hess Bartlett, K. H., Trust, T. J. and Lior, H. (1977). Small pet and Breer (1975) concluded that a dose of 3 kilogray aquarium frogs as a source of Salmonella. Applied and has an effect on Enterobacteriaceae in sludge similar to Environmental Microbiology, 33, 1026-1029. heating to 70°C for 30 minutes. Salmonella in sludge Beard, P J. (1940). Longevity of Eberthella typhosus (S. typhi) and in composted sludge (60 percent solids) were in various soils. American Journal of Public Health, 30, reduced by approximately 1 log unit for each 300 gray Bcri P. of ioizn raito aple (Banon Bug an Becerrl,X P., Bessudo, D. and Gonzalez-Cortes, A. (1979). oi ionizing radiation applied (Brandon, Burge and Busqueda de portadores de Salmonella en diferentes Enkiri 1977). Similarly, White (1979) reported grupos de problaci6n de la ciudad de Mexico. Revista inactivation of coliforms at a rate of 1 log unit per 200 Latinoamericana de Microbiologia, 21, 115-119. gray at 20°C and inactivation of Salmonella at a rate of Bergner-Rabinowitz, S. (1956). The survival of coliforms, 1 log unit per 300 gray at 23°C. Streptococcusfaecalis and Salmonella tennessee in the soil It is clear that the radiation doses necessary to and climate of Israel. Applied Microbiology, 4, 101-106. eliminate Salmonella are similar to those required for Bergy's Manual (1974). Bergy's Manual of Determinative other Gram-negative enteric bacteria (Osborn and Bacteriology, 8th ed. Eds. Buchanan, R. E. and Gibbons, N. Hattingh 1978) and are about one-tenth of the doses E. Baltimore, Md.: Williams and Wilkins. required to inactivate enteroviruses (2.5-5 kilogray Berkowitz, J. H., Kraft, D. J. and Finstein, M. S. (1974). for a I log unit reduction-see chapter 9). Therefore, Persistence of salmonellae in poultry excreta. Journal of' ionizing radiation treatment designed to inactivate Environmental Quality, 3, 158-161. vionizswing eraiation trelinliatment dSinedla. toinaBernard, R. P. (1965). The Zermatt typhoid outbreak in 1963. viruses will certainly eliminate Salmonella. Journal of Hygiene, 63, 537 563. Black, R. E., Merson, M. H., Rowe, B., Taylor, P. R., Rahman, A. S. M., Huq, A., Abdul Aleem, A. R. M., Sack, D. A. and Curlin, G. T. (1979). Epidemiology of enterotoxigenic Literature Cited Escherichia coli in rural Bangladesh. In Proceedings of the 14th Joint Conference, US-Japan Cooperative Medical Aitken, M. M., Jones, P. W., Hall, G. A. and Hughes. D. L. Science Program, Cholera Panel, Symposiun on Cholera. (1976). The effect of fascioliasis on susceptibility ofcattle to Eds. Takeya, K. and Zinnaka, Y., pp. 292-301. Tokyo: Salmonella dublin. British Veterinary Journal, 132, Toho University. 119-120. Bokkenheuser, V. (1964). Detection of typhoid carriers. Al-Ani, Z. I. and Saadallah, S. (1979). Salmonella carriers in American Journal of Public Health, 54, 477-486. Baghdad. Journal of'the Faculty ofjMedicine Baghdad. 21, Bokkenheuser, V. and Richardson, N. J. (1959). The 65-73. bacteriology of the Bantu food-handler: Enterobacte- Al-Dulaimy, S. B. and Al-Allaf, G. A. (1979). Salmonellae riaceae. South African Medical Journal, 33, 784-786. isolated from human carriers in Mosul. Annals of' the (1960). Salmonellae and shigellae in a group of rural College of Medicine Mosul, 10, 5-11. South African Bantu school children. Journal of Hygiene, Al-Hindawi, N. and Taha, R. R. (1979). Salmonella species 58, 109-117. isolated from animal feed in Iraq. Applied and Boring,J. R., Martin, W. T. and Elliot, L. M. (1971). Isolation Environmental Microbiology. 37, 676-679. of Salmonella typhimurilim from municipal water, Aserkoff, B., Schroeder, S. A. and Brachman, P. S. (1970). Riverside, California, 1965. American Journal of' Salmonellosis in the United States a five year review. Epidemiology, 93, 49-54. American Journal of Epidemiology, 92, 13-24. Braga, A. (1964). Research on the survival of salmonellae in Ashcroft, M. T. (1962). The morbidity and mortality of sludges of a fertilizing irrigation plant. Igiene Moderna, 57, enteric fever in British Guiana. West Indian Medical 635-647. Journal, 11, 62-71. Brandon, J. R., Burge, W. D. and Enkiri, N. K. (1977). Baine, W. B., Gangarosa, E. J., Bennett, J. V. and Barker, W. Inactivation by ionizing radiation of Salmonella enteritidis H. (1973). Institutional salmonellosis. Journal of'Infectious serotype montevideo grown in composted sewage sludge. Diseases, 128, 357-360. Applied and Environmental Microbiology, 33, 1011-1012. Baker, J. R. (1970). Salmonellosis in the horse. British Brezenski,F.T.,Russomanno,R.andDeFalco.P.(1965).The Veterinary Journal, 126, 100-105. occurrence of Salmnonella and Shigella in post-chlorinated Barrell, R. A. E. and Rowland, M. G. M. (1979). Infant foods and non-chlorinated sewage effluents and receiving waters. as a potential source of diarrhoeal illness in rural West Health Laboratory Science, 2, 40-47. Africa. Transactionis of the Royul Society oJf Tropical Budd, W., (1856). On the fever at the clergy orphan asylum. Medicine and Hygiene, 73, 85-90. Lancet, 2, 617-619. Bartlett, K. H. and Trust, T. J. (1976). Isolation of (1873). Typhoid Fever: Its Nature, Mode ofSpreading salmonellae and other potential pathogens from the and Prevention. Tondon: Longham Green. freshwater aquarium snail Ampullaria. Applied and Burge, W. D., Cramer, W. N. and Epstein, E. (1978). Environmental Microbiology. 31, 635-639. Destruction of pathogens in sewage sludge by composting. 280 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Tran7sactions of' the .4mericani Society of Agricultural Public Health, 69, 107-108. Engineers. 21, 510-514. D'Aoust, J. Y. and Pivnick, H. (1976). Small infectious doses Burleson, G. R., Murray, T. M. and Pollard. M. (1975). of Salmonella. Lancet. 1, 866. Inactivation of viruses and bacteria by ozone, with and Darlow, H. M., Bale, W. R.andCarter,G. B. (1961). Infection without sonication. Applied Microbiology. 29, 340-344. of mice by the respiratory route with Salmoniella Buttiaux. R. (1962). Sal"monella problems in the sea. In Fish as tIphimtnuriun. Journal of Hygiene, 59, 303-308. Food. 2. Ed. Borgstrom, G., pp. 503-519. New York: Davis, E. M. (1979). Bacterial Characteristics ojStormwaters Academic Press. in Developing Rural Areas. Report EPA-600,/2-79-050f. Carney, J. F., Carty. C. E. and Colwell. R. R. (1975). Seasonal Cincinnati, Ohio: US Environmental Protection Agency. occurrence and distribution of microbial indicators and Davis, E. M. and Glovna, E. F. (1972). Bacterial dieoff in pathogens in the Rhode River of Chesapeake Bay. Applied ponds. Jour7nal of' the Sanitary Engineerinig Dirision. Microbiology. 30. 771-780. Proceedinigs of thze Amnericani Society of Civil Engineers, 98. Chandler, D. S. and Craven, J. A. (1978). Environmental 59-69. factors affecting Escherichia coli and Salmoniella tt'phi- Dazzo. F., Smith, P. and Hubbell, D. (1973). The influence of inurinm numbers on land used for effluent disposal. manure slurry irrigation on the survival of fecal organisms Australian Journal of Agricultural Researcl, 29, 577-585. in Scranton fine sand. Journal of Enviromnental Quality, 2, Cherry. W. B.. Hanks, J. B.. Thomasen, B. M., Murlin, A. M., 470-473. Biddle. J. W. and Croom, J. M. (1972). Salmonellae as an Deans Rankin, J. and Taylor, R. J. ( 1966). The estimation of index of pollution of surface waters. Applied Microbiology, doses of Sahnonellua tiphinurium7 suitable for the 24, 334-340. experimental production of disease in calves. Veterinary Coetzee, 0. J. and Fourie. N. A. (1965). The efficiency of Record. 78, 706-707. conventional sewage purification works, stabilization Delage, B. (1961). Survival of salmonellae in soil. Archives de ponds and maturation ponds with respect to the survival of l'Institiut Pasteur du Mar-oc 6, 139-142. pathogenic bacteria and indicator organisms. Journal of DiGirolamo. R., Liston, J. and Matches, J. (1975). Uptake thie Institute qf'Sewage F ' . . part III, 210-215. and elimination of poliovirus by West Coast oysters. Colwell, R. R. and Kaper. J. (1978). Distribution. survival and Applied Microbiology. 29, 260 264. significanice of pathogenic bacteria and viruses in estuaries. Dondero, N. C.. Thomas, C. T.,, Khare, M., Timonev, J. F. In Estuarine Interactions. Ed. Wiley, M. L., pp. 443-457. and Fukui, G. M. (1977). Salnonella in surface waters of New York: Academic Press. central New York State. Applied7 and Environmnental Cook, W. L.. Champion. R. A. and Ahearn, D. G. (1974). Microbiology. 33, 791--801. Isolation of Salmonella enteritidis serotype agona from Dudley. D. J., Guentzel. M. N., Ibarra, M. J., Moore, B. E. entrophic regions of a freshwater lake. Appilied and Sagik, B. P. (1980). Enumeration of potentially Mlicrobiology. 28, 723-725. pathogenic bacteria from sewage sludges. .4pplied and Cooke, M. B., Thackston. E. L. and Malaney. G. W. (1978). Environmental Microbiology, 39. 118-126. Reducing coliform and SaloIonella bacteria during Duguid. J. P.. Darekar, M. R. and Wheater, D. W. F. (1976). anaerobicdigestion. WVater and Sewiage IVorks. 125, 50-53. Fimbriae and infectivity of Salmonella typhliinurium. Cowan. S. T. and Steel. K. J. (19741. Identifcation I ;. .. .1 Journal of Medical Microbiology, 9, 459-473. Bacteria. 2nd ed. Cambridge: Cambridge University Press. Dunlop, S. G. and Wang, W. L. (1961). Studies on the use of Creel. R. H. (1912). Vegetables as a possible factor in tne sewage effluent for irrigation of truck crops. Joulrnlal of' dissemination of typhoid fever. Public Healthl Reports. Milk and Food Technology, 24, 44-47. 27(6). 187-195. Dutka. B. J. and Bell. J. B. (1973). Isolation of salmonellae Crozier. D. and Woodward, T. E. (1962). Armed Forces from moderately polluted waters. Jou7iial of the Water Epidemiological Board. Activities of the Commission on Pollution Federation, 45, 316-336. Epidemiological Survey, 1961. Military Medicine, 127, Dutka, B. J. and Kwan, K. K. (1980). Bacterial die-off and 701-705. stream transport studies. Water Researclh. 14, 909--915. Cvjetanovic, B., Grab, B. and Uemura, K. (1971). Edwards, P. R. and Ewing. W. H. (t972). Identification of Epidemiological model of typhoid fever and its use in the Ente7robacter iaceae. 3rd ed. Minneapolis, Minn.: Burgess. planning and evaluation ofantityphoid immunization and Ekesbo, I. (1979). A study of methods for handling and sanitation programmes. Bulletin of' the World Healtlh composting cattle and swine manure and urine from the OrganiZation. 45, 53- 75. point of view of hygiene. Agricuiltuiral Wastes. 1, 205-221. -(1978). Dynamnics of Acute Bacterial Diseases Enkiri, N. K. and Alford, J. A. (1971). Relationship of the Epidemiological Models and their Application in Puiblic frequency of isolation of salmonellac to their resistance to Healtlh. Geneva: World Health Organization. drying and freezing. Applied Microbiology, 21, 381-382. Daniel, R. R. and Lloyd, B. J. (1980). Microbiological studies Ercolani. G. L. (1976). Bacteriological quality assessment of on two Oxfam Sanitation Units operating in Bengali fresh marketed lettuce and fennel. .4pplied and refugee camps. Walter Research. 14, 1567-1571. Environmnental Microbiology, 31, 847-852. D'Aoust, J. Y. and Lior, H. (1978). Pet turtle regulations and Feachem. R., Burns, E., Cairncross, S.. Cronin, A., Cross, P., abatement of human salmonellosis. Canadian Journal oj' Curtis, D.. Khan, M. K., Lamb, D. and Southall. H. (1978). SALMONELLA., ENTERIC FEVERS, AND SALMONELLOSES 281 Water, Health and Development. An Interdisciplinary wastewater bacteria and viruses in soil. Journal of Evaluation. London: Tri-Med Books. Irrigation and Drainage Diuisionz, Proceedings of the Feachem. R. G. A., Bradley, D. J., Garelick, H. and Mara, D. American Societv of Civil Engineers, 101, 157-174. D. (1980). Health Aspects of Excreta and '. ,, Gilbert, R. G., Gerba, C. P., Rice, R. C., Bouwer, H., Wallis, C. Management: A State-of-the-Art Review. Appropriate and Melnick, J. L. (1976). Virus and bacteria removal from Technology for Water Supply and Sanitation, vol. 3. wastewater by land treatment. Applied and Environmental Washington, DC: The World Bank. Transportation, Microbiology, 32, 333--338. Water and Telecommunications Department. Goldshmid. J. (1974). Water quality aspects of ground-water Feldman, R. E., Baine, W. B., Nitzkin, J. L., Saslaw, M. S. and recharge in Israel. Journal of the American Water Works Pollard, R. A. (1974). Epidemiology of Salmonella typhi Association, 5, 163-166. infection in a migrant labor camp in Dade County, Gordon, J. E., Pierce, V., Ascoli, W. and Scrimshaw, N. S. Florida. Journal ofJInfectious Diseases, 130, 334-342. (1961). Studies of diarrheal disease in Central America. It. Fennell, H. (1977). Pathogens in sewage sludge. In Research Community prevalence of \I,, H.. and Salnonella Seminar on Patlhogens in Sewage Sludge, London, 9 infections in childhood populations of Guatemala. February 1977. pp. 8-12. London: Department of the American Journal of Tropical Medicine and Hygiene, 11, Environment. 389-394. Findlay, C. R. (1972). The persistence of Salmonella dublih in Goyal, S. M., Gerba. C. P. and Melnick, J. L. (1977). slurry in tanks and on pasture. Veterinary Record, 91, Occurrence and distribution of bacterial indicators and 233-235. pathogens in canal communities along the Texas coast. (1973). Salmonellae in sewage sludge. II. Applied anzd Enuironmnental Microbiology. 34, 139-149. Multiplication. Veterinary Record, 93, 102-103. - (1978). Prevalence of human entericvirusesin coastal Gallagher, T. P. and Spino, D. F. (1968). The significance of canal communities. Journal of the Water Pollutioni Control numbers of coliform bacteria as an indicator of enteric Federation, 50, 2247-2256. pathogens. Water Research, 2, 169-175. Goyal, S. M. and Singh, I. P. (1970). Probable sources of Galvagno, 0. and Calderini, A. (1908). Survival and virulence salmonellae on a poultry farm. Britishz Veterinary Journial, of typhoid bacilli in pit latrines, tanks and in soil. 126, 180-184. Z. .i a f ir Hygiene und Infektionskrankheiten, 61, Grabow, W. 0. K. and Nupen, E. M. (1972). The load of 185-208. infectiousmicroorganismsonthewastewateroftwoSouth Garg, D. N. and Sharma. V. K. (1979). The detection of nasal African hospitals. Water Research. 6, 1557-1563. carriers of Salmnonella and other enterobacteria amongst Gracey, M., Ostergaard, P., Adnan, S. W. and Iveson, J. B. young farm animals. Zentralblatt fOir Bakteriologie (1979). Faecal pollution of surface waters in Jakarta. Parasitentkunde. Infektionsk-rankheiten und Hygiene. Transactions of the Royal Society of Tropical Medicine and Abteilung 1, Originale A, 243, 542-546. Hygiene, 73, 306-308. Gauger, H. C. and Greaves, R. E. (1946). Isolations of Green. C. E. and Beard. P. J. (1938). Survival of S. tvphi in Salmonella typhimnurium from drinking water in an infected sewage treatment plant processes. Anmerican Journlal oj environment. Poultry Science, 25, 476-478. Public Health, 28, 762-770. Gayler, G. E., MacCready, R. A., Reardon, J. P. and Greenberg, A. E. and Ongerth. H. J. (1966). Salmonellosis in McKernan. B. F. (1955). An outbreak of salmonellosis Riverside, California.Journal oftheAmerican Wate- Works traced to watermelon. Public Health Reports, 70, 311-313. Association, 58, 1145-1150. Geldreich, E. E., Best. L. C., Kenner, B. A. and Van Donsel, Grell, G. A. C. (1979). Typhoid fever in Dominica. W.I.: D. J. (1968). The bacteriological aspects of stormwater Report on the clinical features of 78 cases. West Indlian pollution. Journal of the Water Pollution Control Medical Journal, 28, 94-99. Federation, 40, 1861-1872. Gunn, R. A. and Loarte, F. B. (1979). Salmonzella Geldreich, E. E. and Bordner. R. H. (1971). Fecal enterocolitis. Report of a large foodborne outbreak in contamination of fruits and vegetables during cultivation Trujillo, Peru. Bzilletin of the Panamerican Health and processing for market: A review. Journal of Milk and Organization, 13, 162-168. Food Technology, 34, 184-195. Hall, G. A. and Jones, P. W. (1978). A study of the Geldreich, E. E. and Clarke, N. A. (1966). Bacterial pollution susceptibility of cattle to oral infection by salmonellas indicators in the intestinal tract of freshwater fish. Applied contained in raw sewage sludge. Journal of Hygiene, 80, Microbiology. 14, 429-437. 409-414. Gell, P. G. H., Hobbs, B. C. and Allison, V. D. (1945). An Harbourne, J. F. (1977). Intestinal infections of animals and outbreak of water-borne typhoid investigated by bacte- man. Salmonellae in waterways in North Yorkshire riophage typing and selective sewage examination. Journal associated with human and animal effluent. Royal Society of Hygiene, 44, 120-128. of Health Journal, 97, 106-114. George, J. T. A., Wallace, J. G., Morrison. H. R. and Harbourne, J. F., Randall, C. J., Luery, K. W. and Wallace, J. Harbourne, J. F. (1972). Paratyphoid in man and cattle. G. (1972). Salmonella paratyphi B infection in dairy cows. British Medical Journial, 2, 208-211. Veterinary Record, 91, 112-114. Gerba, C. P., Wallis, C. and Melnick, J. L. (1975). Fate of Harbourne, J. F.. Thomas, G. W. and Luery, K. W. (1978). 282 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Salmonellae in effluent waters and river sites in North States, 1973. Journal of Infectious Diseases, 132, 336-339. Yorkshire. British Veterinary Journal. 134, 350-357. Hussong, D., Damare, J. M., Limpert, R. J., Sladen, W. J. L., Harvey, R. W. S. and Phillips, W. P. (1955). Survival of Weiner, R. M. and Colwell, R. R. (1979). Microbial impact Salmonella paratyphi B in sewers: its significance in the of Canada geese (Branta canadensis) and whistling swans investigation of paratyphoid outbreaks. Lancet, 2, (Cygnus columbianus columbianus) on aquatic ecosystems. 137-139. Applied and Environmental Microbiology, 37, 14-20. Hathout, S. E-D., El-Ghaffar, Y. A., Awny, A. Y. and Hassan, Jack, E. J. and Hepper, P. (1969). An outbreak of Salmonella K. (1966). Relation between urinary schistosomiasis and typhimurium infection in cattle associated with the chronic enteric urinary carrier state among Egyptians. spreading of slurry. Veterinary Record, 84, 196-199. American Journal of Tropical Medicine and Hygiene, 15, Jamieson, W., Madri, P. and Claus. G. (1976). Survival of 156-161. certain pathogenic microorganisms in sea water. Hedstrom, C. E. and Lycke, E. (1064). An experimental study Hydrobiologia, 50, 117-121. on oysters as virus carriers. American Journal of Hygiene, Janssen, W. A. (1974). Oysters: retention and excretion of 79, 134-142. three types of human waterborne disease bacteria. Health Hendricks, C. W. (1971a). Increased recovery rate of Laboratory Science, 11, 20-24. salmonellae from stream bottom sediments versus surface Jegathesan, M_. Wah, L. T., Soon, L. E., Har. D. S. and Liat, waters. Applied Microbiology, 21, 379-380. L. B. (1976). Bacterial enteropathogens in Malaysian (1971b). Enteric bacterial metabolism of stream shellfish. Tropical and Geographical Medicine, 28, 91-95. sediment eluates. Canadian Jouirnal of Microbiology, 17, Joint Working Party i1965). Salmonellae in cattle and their 551-556. feeding stuffs, and the relation to human infection. Journal (1972). Enteric bacterial growth rates in river water. ofHygiene, 63, 223-239. Applied Microbiology, 24, 168-174. Jones. F. (1977). Sludge application to pasture and arable Hendricks, C. W. and Morrison, S. M. (1967). Multiplication land. In Research Seminar on Pathogens in Sewvage Sludge, and growth of selected enteric bacteria in clear mountain London, 9 February 1977, pp. 13-14. London: Department stream water. Water Research, 1, 567-576. of the Environment. Hess, E. and Breer, C. (1975). Epidemiology of salmonellae Jones, F., Smith, P. and Watson, D. C. (1978). Pollution of a and fertilizing of grassland with sewage sludge. water supply catchment by breeding gulls and the Z. a,i. J; fuir Bakteriologie, Parasitenkuinzde, potential environmental health implications. Journal oftlhe Infektionsklrankheiten und Hygiene. IB, 161, 54-60. Institutioni of W1ater Engineers and Scientists, 32, 469 -482. Heuschmann-Brunner, G. (1974). Experiments on the Jones. P. W. (1975). The effect of storage in slurry on the possibilities and course of infections with Salmonella virulence of Salmonella dublin. Journal of Hvgiene, 74, enteritidis and Salmonella typhimurium in freshwater fish. 65-70. Z." ,i ,, i.-, Jiir Bakteriologie, Parasitenkunide, (1976). The effect of temperature, solids content and Infektionskrankheiten und Hygiene, IB, 158, 412-431. pH on the survival of salmonellas in cattle slurry. British Hickey. J. L. S. and Reist, P. C. (1975). Health significance of Veterinary Journal, 132, 284-293. airborne micro-organisms from wastewater treatment (1977). Work on slurry systems. In Research Semiinlar processes. 1. Summary of investigations. Journial of the on Pat hogenis in Sewvage Sludge, London, 9 February 1977, Water . I.,. , Control Federation, 47, 2741-2757. pp. 25- 26. London: Department of the Environment. Hirn, J. (1980). Indicator bacteria and Salmoniella in food- - (1978). Health hazards associated with the handling processing and domestic effluent. Journal oJ the Waiter of animal wastes. In Animal and Humnan Health Hazard7s Pollution Control Feder-ation, 52, 48-52. Associatedi with the Utilization of 'Animilal L u, ., Ed. Hoff, J. C. and Becker. R. C. (1969). The accumulation and Kelly. W. R., pp. 189-202. Luxembourg: Office of Official elimination of crude and classified poliovirus suspensions Publications of the European Communities. by shellfish. American Journal of Epidemiology. 90, 53-61. Jones, P. W., Bew. J., Burrows, M. R., Matthews, P. R. J. and Holden. 0. M. (1939). The Croydon typhoid outbreak. Collins, P. (1976). The occurrence of salmonellas. Public Healtlh. 52. 135-146. mycobacteria and pathogenic strains of Escherichia coli in Hornick, R. B., Greisman, S. E., Woodward, T. E., DuPont. pig slurry. Journial of Hygiene, 77, 43- 50. H. L., Dawkins. A. T. and Snyder, M. J. (1970). Typhoid Jones, P. W., Bew, J. and Gammack. D. B. (1975). An fever: pathogenesis and immunologic control. Ne;v investigation into the potential hazard to animal health of England Journal of Medicine. 283, 686-691. cffluent sludge from dairy factories. Journal of Hygiene. 75, Howard, J.. Lloyd. B. and Webber, D. (1975). Ofoam's 143 -149. Sanitation Unit. The Design and 7esting oJfa Saniitation and Jones. P. W. and Hall. G. A. (1975). Detection of Salmonella Sewaage Treatmzent UnitJfr Disasters and Long Term Use. infection in pig herds by examination of the slurry. Oxford: Oxfam. Veterinary Record. 97, 351- 352. Howie, J. W. (1968). Typhoid in Aberdeen, 1964. Journal of Jones, P. W. and Matthews, P. R. J. (1975). Examination of .4ppliea7 Bacteriology, 31, 171-178. slurry from cattle for pathogenic bacteria. Journal of Hughes, J. M., Merson, M. H., Craun. G. F. and McCabe. L. Hygiene, 74, 57 64. J. (1975). Outbreaks of waterborne disease in the United Jones, P. W., Smith, G. S. and Bew, J. (1977). The effect of the SALMONELLA, ENTERIC FEVERS, AND SALMONELLOSES 283 microflora in cattle slurry on the survival of Salmonella and Cassel, R. (1979). Etiology of infantile enteritis in dublin. British Veterinary Journal, 133, 1-8. South Africa. Israel Journal of Medical Sciences, 15, Jones, P. W. and Twigg, G. I. (1976). Salmonellosis in wild 341-347. mammals. Journal of Hygiene, 77, 51-54. Koplan., J. P., Deen, R. D., Swanston, W. H. and Tota, B. Jordan, E. 0. (1926). The changes in the bacterial content of (1978). Contaminated roof-collected rainwater as a stored normal and typhoid faeces. Journal of Infectious possible cause of an outbreak of salmonellosis. Journal of Diseases, 38, 306-322. Hygiene, 81, 303-309. Joshi, S. R., Parhad, N. M. and Rao, N. U. (1972). Kourany, M. and Vasquez, M. A. (1969). Housing and Elimination of Salmonella in oxidation ponds. In certain socio-environmental factors and prevalence of Proceedings of a Symposium on Low Cost Waste Treatment. enteropathogenic bacteria among infants with diarrheal Ed. Sastry, C. A., pp. 284-289. Nagpur, India: Central disease in Panama,. American Journal of Tropical Medicine Public Health Engineering Research Institute. and Hygiene, 18, 936-941. (1973). Elimination of Salmonella in stabilization Kraft, D. J., Olechowski-Gerhardt, C., Berkowitz, J. and ponds. Water Research, 7, 1357-1365. Finstein, M. S. (1969). Salmonella in wastes produced at Josland, S. W. (1951). Survival of S. typhimurium on various commercial poultry farms. Applied Microbiology, 18, substances under natural conditions. Australian Veterinary 703-707. Journal, 27, 264-266. Lamm, S. H., Taylor, A., Gangarosa, E. J., Anderson, H. W., Kabler, P. (1959). Removal of pathogenic micro-organisms Young, W., Clark, M. H. and Bruce., A. R. (1972). Turtle- by sewage treatment processes. Sewage and Industrial associated salmonellosis. 1. An estimation of the Wastes, 31, 1373-1382. magnitude of the problem in the United States, 1970-1971. Kampelmacher, E. H., Fonds, A. W. and van NoorleJansen, American Journal of Epidemiology, 95, 511-517. L. M. (1977). Reduction of Salmonella, E. coli, coliforms Lee, J. A. (1974). Recent trends in human salmonellosis in and fecal streptococci by chlorination of sewage treatment England and Wales: the epidemiology of prevalent plant effluents. Water Research, 11, 545-550. serotypes other than Salmonella typhimurium. Journal of Kampelmacher, E. H. and van Noorle Jansen, L. M. (1970). Hygiene, 72, 185-195. Salmonella its presence in and removal from a waste Lessel, T. and Suess, A. (1978). Hygienization of sewage water system. Journal of the Water Pollution Control sludge by gamma irradiation: experience with an Federation, 42, 2069-2073. operating pilot plant. Progress in Water Technology, 10, (1971). Reduction of Salmonella in compost in a hog- 641-652. fattening farm oxidation vat. Journal ofthe Water Pollution Lipson, A. (1976). Infecting dose of s 1. L. a , 1, 969. Control Federation, 43, 1541-1545. Lovett, J. and Francis, D. W. (1976). Persistence of micro- (1972). Reduction of bacteria in sludge treatment. organisms on vegetables irrigated by flooding with sewage Journal of the Water Pollution Control Federation, 44, treatment plant effluent and sludge. Abstract P19. 309-313. Abstracts of the Annual Meeting of the American Society of (1973). Occurrence of Salmonella in oxidation ditches. Microbiologists. Washington, D.C. Journal of the Water Pollution Control Federation, 45, McCoy, J. H. (1977). The microbiological background to the 348-352. examination of crude sewage, sludges and sewage effluents. - (1976). Salmonella in effluenten van rioolwater- In Research Seminar on Pathogens in Sewage Sludge, zuiveringsinstallaties, in rioolafvoeren van slagerijen en London. 9 February 1977, pp. 3-7. London: Department of oppervlaktewater op Walcheren. H20, 9, 334-337. the Environment. Katzenelson. E. and Teltch, B. (1976). Dispersion of enteric McCoy, J. (1979). The risks to public health from pathogens bacteria by spray irrigation. Journal of the Water Pollution in sewage sludges. In Utilization of Sewage Sludge on Land. Control Federation, 48, 710-716. pp. 191-197. Stevenage, England: Water Research Centre. Katzenelson, E., Teltch, B. and Shuval, H. 1. (1977). Spray McCullough, N. B. and Eisele, C. W. (1951a). Experimental irrigation with wastewater: the problem of aerosolization human salmonellosis. 1. Pathogenicity of strains of and dispersion of enteric microorganisms. Progress in Salmonella meleagridis and Salmnontella anatum obtained Water Technology, 9, 1-11. from spray-dried whole-egg. Journial of Infectious Diseases, Kawata, K., Cramer, W. N. and Burge, W. D. (1977). 88, 278-289. Composting destroys pathogens. Water and Sewage (1951b). Experimental human salmonellosis. II. Works, 124, 76-79. Immunity studies following experimental illness with Kelly, S. M., Clark, M. E. and Coleman, M. B. (1955). Salmonella meleagridis and Salmonella anatum. Joturnal of Demonstration of infectious agents in sewage. American Immunology, 66, 595-608. Journal of Public Healtl, 45, 1438-1446. (1953a). Experimental human salmonellosis. III. Kelly, W. R., ed. (1978). Animal and Human Healthi Hazards Pathogenicity, of strains of Salmonella newport. Salmonella Associated with the Utilization of Animal Effluents. derby and Salmonella bareillv obtained from spray-dried ,Iuxembourg: Office of Official Publications of the whole-egg. Journal of Intfectious Diseases, 89, 209-213. European Communities. (1953b). Experimental human salmonellosis. IV. Koornhof, H. J., Robins-Browne, R. M., Richardson, N. J. Pathogenicity of strains of Salmonella pulloruin obtained 284 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA from spray-dried whole-egg. Journal oj'nfectious Diseases, Moore, B., Perry, E. L. and Chard. S. T. (1952). A survey by 89, 259-265. the sewage swab method of latent enteric infection in an McFeters, G. A.. Bissonnette, G. K., Jezeski, J. J., Thomson, urban area. Journal of Hygiene, 50, 137-156. C. A. and Stuart, D. G. (1974). Comparative survival of Morse, E. V., Myhrom, E. P. and Greenwood, D. E. (1976). indicator bacteria and enteric pathogens in well water. Salmonellosis in man and animals as an environmental Applied Microbiology, 27, 823-829. health problem. Journal oJ Encironmiental Science and Mair. N. S. and Ross, A. I. (1960). Survival of Salmoniella Health, All, 755-769. typhimurium in the soil. Monthly Bulletin of'the Ministry7 of Newson, S. W. B. (1972). Microbiology of hospital toilets. Health and the P.H.L.S.. 19, 39-41. Laancet, 2, 700-703. Mallman, W. L. and Litsky, W. (1951). Survival of selected Obrist. W. (1979). Research and practice of sludge enteric organisms in various types of soil. American pasteurization in Switzerland. In Utilisationi of' Sewage Journial oj'Public Healthl. 41, 38-44. sill..,, on Land. pp. 503-511. Stevenage, England: Water Mathur, G. M. and Sharma, R. (1971). A study of typhoid Research Centre. fever in Jaipur. India. Tropical and Geograpzic Medicine, Oliver, B.G. and Carey,J. H. (1976). Ultraviolet disinfection: 23, 329-334. an alternative to chlorination. Journal of' thze Water Melick, C. 0. (1917). The possibility of typhoid infection Pollution Contol Federation, 48, 2619-2624. through vegetables. Journal of' Infectious Diseases, 21, Olivieri, V. P_. Kawata, K. and Kruse. C. W. (1978). 28-38. Relationship between indicator organisms and selected Mendis, N. M. P., De La Motte, P. U., Gunatillaka, P. D. P. pathogenic bacteria in urban waterways. Progress in Water and Nagaratnam, W. (1976). Protracted infection with Techzzology, 10, 361-379. Salmonella b. 9L! in a maternity hospital. Journal of Osborn, D. W. and Hattingh. W. H. J. (1978). Disinfection of Tropical Medicine and Hygiene. 79, 142-150. sewage sludge: a review. Water South Africa. 4, 169-178. Merselis, J. G., Kaye, D., Conolly, C. S. and Hook. E. W. Pether, J. V. S. and Gilbert, R. J. (1971). The survival of (1964). Quantitative bacteriology of the typhoid carrier salmonellas on finger-tips and transfer of the organisms to state. American Journal of'Tropical Medicine and Hygiene. foods. Journal of Hygiene, 69, 673-681. 13, 425-429 Petrilli. F. L. de Renzi. G. P., Palmerini Morelli, R. and de Merson, M. H., Barker, W. H., Craun, G. F. and McCabe, L. Flora, S. (1979). Survey of the pollution in a coastal area of J. (1974). Outbreaks of waterborne disease in the United the Tyrrhenian Sea: aerial photography, physico-chemical States, 1971-1972. Journal of' Infectious Diseases, 129, and microbiological investigations and mutagenic mo- 614 615. nitoring. Water Research, 13, 895-904. Metropolitan Water Board (1963-1964). Improvement in Phirke, P. M. (1974). Elevated temperature technique for quality of sewage works effluent during passage through a enumeration of salmonellae in sewage. Indian Journal of series of lagoons. In Forty-first Report on the Results of Medical Research, 62, 938-944. Bacteriological, Choemical and Biological Examination of Pierce, V., Ascoli, W., de Leon, R. and Gordon. J. E. (1961). the London Waters. pp. 111-129. London. Studies of diarrheal disease in Central America. III. Miled, M., Zribi, A. and Ben Rachid, M. S. (1973). Specific etiology of endemic diarrhea and dysentery in Epidemiological study of typhoid fever in the region of Guatemalan children. American Journ-al ol Tropical Tunis Miled. 4rchiues de l'Instirut Pasteur de Tunis, 50, Medicine and Hygiene. 11, 395-400. 1-17. Pike. E. B. (1981). Salmonellaein sewage sludges; a survey of Miller,C., Grant. L. S. andIrvine, R. A. (1961). Typhoidfever. sewage works in England and Wales. In Proceedings of the West Ina'ian Medical Journal, 10, 189-197. European Symposiulmn on Characterization, Treat7nent and Miner, J. R., Fina, L. R. and Piatt, C. (1967). Salmonella Use of'Sewzage Sludge. Luxembourg: Office of Official infantis in cattle feedlot runoff. Applied Microbiology, 15, Publications of the European Communities. 627-628. Plant. C. W. (1978). Salmonellosis in wild birds feeding at Mitchell, J. R., Presnell, M. W., Akin, E. W., Cummins, J. M. sewage treatment works. Journal of' Hygiene. 81, 43-48. and Liu, 0. C. (1966). Accumulation and elimination of Platz,S. (1978). Survival ofpathogenicbacteriaand protozoa poliovirus by the eastern oyster. American Journal of after short-time composting of poultry manure. In Animal Epidemiology, 84, 40-50. and Human Health Hazards Associated with the Utilization MMWR (1975). Ban on pet turtles-United States. Morbidity of Animal FT'. - Ed. Kelly, W. R., pp. 209-215. and Mortality Weeklly Reports, 24, 188. Luxembourg: Office for Official Publications of the Mom, C. P. and Schaeffer, C. 0. (1940). Typhoid bacteria in European Communities. sewage and in sludge: an investigation into the hygienic Popkiss, M. E. E. (1980). Typhoid fever: a report on a point- significance of sewage purification in the tropics with source outbreak of 69 cases in Cape Town. South African regard to typhoid fever. Sewage Works Journtal. 12, Medical Journial, 57, 325-329. 715-737. Prior. B. A. and Badenhorst. L. (1974). Incidence of Moore, B. (1957). Observations pointing to the conjunctiva salmonellae in some meat products. South .4Aiican iledical as the portal of entry in Salmionella infection of guinea-pigs. Journ al. 48, 2532-2533. Journal of'Hygiene. 55, 414-433. Public Health Laboratory Service Standing Sub-Committee SALAIONELLA, ENTERIC FEVERS, AND SALMONELLOSES 285 on the Bacteriological Examination of Water Supplies Welch, S. F. (1958). Relation of Environmental Factors to (1978). Waterborne infectious disease in Britain. Journal of the Occurrence of Enteric Diseases in Areas oJ' Eastern Hygiene, 81, 139-149. Kentuckv. Public Health Monograph no. 54. Washington, Raman, V., Parhad, N. M., Deshpande, A. W. and Pathak, S. D.C.: US Government Printing Office. K. (1979). Assessment and control of water quality in a Schubert, R. H. W. and Scheiber, P. (1979). Investigation on town distribution system with reference to the incidence of the presence of Salmonella in drinking water from water gastrointestinal diseases. Progress in Water Technology, supplies and distribution systems in Togo. Zentralblattfiir 11, 65-71. Bakteriologie, Parasitenkunde, Inifektionskrankheiteni und Reeves, J. B. (1959). Sanitary aspects of composted sewage Hygiene, I Originale B, 168. 356-360. sludge and sawdust. Sewvage and Induistr ial Wastes, 31, Shearer, L. A., Browne, A. S., Gordon, R. B. and Hollister, A. 557-564. C. (1959). Discovery of typhoid carrier by sewage Rice, P. A., Baine. W. B. and Gangarosa, E. J. (1977). sampling. Journal of the American Medical Association, Salmonella typhi infections in the United States, 169. 1051-1055. 1967-1972: increasing importance of international travel- Skerman, V. B. D., McGowan, V. and Sneath, P. H. A., eds. lers. American Journal of Epidemiology, 106, 160-166. (1980). Approved lists of bacterial names. International Richardson, N. J. and Bokkenheuser, V. (1963). Salmonellae Journal of Systematic Bacteriology, 30, 225-420. and shigellae in a group of periurban South African Bantu Slanetz, L. W., Bartley, C. H., Metcalf, T. G. and Nesman, R. school children. Journal of Hygiene, 61, 257-263. (1970). Survival of enteric bacteria and viruses in Richardson, N. J.. Burnett. G. M. and Koornhof. H. J. (1968). municipal sewage lagoons. In Proceedings of the Second A bacteriological assessmcnt of meat, offal and other International Symposiumfor lWaste Treatmnent Lagoons. Ed. possible sources of human enteric infections in a Bantu McKinney, R. E., pp. 132--141. Lawrence, Kansas: township. Journal of H1-ygiene, 66, 365-375. University of Kansas. Richardson, N. J., Hayden-Smith, S.. Bokkenheuser. V. and Slanetz, L. W., Bartley, C. H. and Stanley, K. W. (1968). Koornhof, H. J. (1968). Salmonellae and shigellae in Bantu Coliforms, faecal streptococci and Salmonella in seawater children consuming drinking water of improved quality. and shellfish. Health Laboratory Science, 5, 66-78. South Africani Medical Journlal. 42, 46-49. Small Scale Waste Management Project (1979). Management Richardson, N. J. and Koornhof, H. J. (1965). Salmonellae of Small Waste Flowis. Report EPA-600/2-78-173. and shigellae in a group of Bantu schoolchildren in the Cincinnati, Ohio: US Environmental Protection Agency. Eastern Transvaal Lowveld. Sooth African Medical Smith. J. E., Young, K. W. and Dean, R. B. (1975). Biological Journal, 39, 367-370. oxidation and disinfection of sludge. Water Research, 9, Richardson, N. J., Koornhof, H. J. and Hayden-Smith, S. 17-24. (1966). Salmonellae and shigellae in a group of urban Smith, P. J., Jones. F. and Watson, D. C. (1978). Salmonella South African Bantu school children. Journal of Hygiene, pollution of surface waters. Journal of Hygiene, 81, 64, 245-253. 353-360. Robinson, R. A. and Loken, K. I. (1968). Age susceptibility Smith, R. J., Twedt, R. M. and Flanigan, L. K. (1973). and excretion of Salmoniaella typhlimuriumn in calves. Journal Relationships of indicator and pathogenic bacteria in of Hygiene. 66, 207-216. stream waters. Journial of the Water Pollution Control Robinson, R. G. (1958). The isolation of enteric organisms Federation, 45, 1736-1745. from sewage and the development of the sewage and the Sojka, W. J., Wray, C...Shreeve, J. and Benson, A. J. (1977). development of the sewage pad technique. Journal of Incidence of Salmonella infection in animals in England Medical Laboratory Technology, 15, 79-95. and Wales, 1968-1974. Journal of Hygiene. 78, 43-56. Rosenstein, B. J. (1967). Salmonellosis in infants and Spino, D. F. (1966). Elevated-temperature technique for the children: epidemiologic and therapeutic considerations. isolation of Salmonella from streams. Applied Journal of Pediatrics, 70, 1-7. Microbiology. 14, 591-596. Rudolfs, W., Falk, L. L. and Ragotzkie, R. A. (1950). Stokes, E. J., Jones, E. E.. Mohun. M. B. and Miles, A. A. Literature review on the occurrence and survival of enteric, (1945). Effect of drying and digestion of sewage sludge on pathogenic, and relative organisms in soil, water, sewage certain pathogenic organisms. Journal and Proceedings of and sludges, and on vegetation. 1. Bacterial and virus the Institute of Sewage Purification, 1, 36-44. diseases. Sewage and Industrial Wastes, 22, 1261-1281. Strauch (1978). Identifying the priority contaminants: Savage, J.. Chase, T. and MacMillan, J. D. (1973). Population microbiological agents. In Animal and Human Health changes in enteric bacteria and other microorganisms Hazards Associated with the Utilization of Animal during aerobic thermophilic windrow composting. Applied Etluenui. Ed. Kelly, W. R., pp. 1-23. Luxembourg: Office Microbiology, 26, 969-974. of Official Publications of the European Communities. Schiemann, D. A.. Brodsky, M. H. and Ciebin, B. W. (1978). Tamminga, S. K., Beumer, R. R. and Kampelmacher, E. H. Salmonella and bacterial indicators in ozonated and (1978). The hygienic quality of vegetables grown in or chlorine dioxide-disinfected effluent. Journal of the Water imported into The Netherlands: a tentative survey. Pollution Cont0ol Federation. 50, 158-162. Journal of Hygiene, 80, 143-154. Schliessmann, D. J., Atchley, F. O., Wilcomb, M. J. and Tannock, G. W. and Smith, J. M. B. (1971). Studies on the 286 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA survival of Salmonella typhimurium and Salmonella 568-594. Stevenage, England: Water Research Centre. bovismorbificans on pasture and in water. Australian WHO (1979). Intestinal immunity and vaccine development. Veterinary Journal. 47, 557-559. Bulletin of the World Health Organization. 57, 719-734. (1972). Studies on the survival of Salmnonella Wiley, B. B. and Westerberg, S.C. (1969). Survival of human typhimurium and S. bouis-morbificans on soil and sheep pathogens in composted sewage. Applied Microbiology, 18, faeces. Research in Veterinary' Science, 13(2), 150-153. 994-1001. Taylor, R. J. (1973). A further assessment of the potential Will, L. A.. Diesch, S. L. and Pomeroy, B. S. (1973). Survival hazard for calves allowed to graze pasture contaminated of Salmonella typhiinurium in animal manure disposal in a with Salmonella dublin in slurry. British Veterinary Journal, model oxidation ditch. American Journal of'Public Health. 129, 354-358. 63, 322-326. Taylor, R. J. and Burrows. M. R. (1971). The survival of Williams. B. M. (1975). Environmental considerations in Escherichia coli and Salmonella dublin in slurry on pasture salmonellosis. Veterinary Record, 96, 318-321. and the infectivity of S. dublin for grazing calves. British ( 1979). The animal health risks from the use of sewage Veterinary Journal, 127, 536-543. sludge on pastures. In Utilization of Sewage Sludge on Thomson, S. (1954). The number of bacilli harboured by Land. pp. 177-190. Stevenage. England: Water Research enteric carriers. Jou7rnal of Hygiene, 52, 67-70. Centre. - _ (1955). The numbers of pathogenic bacilli in faeces in Williams, B. M., Richards, D. W., Stephens, D. P. and intestinal diseases. Journlal of Hygiene. 53, 217-224. Griffiths, T. (1977). The transmission of S. livingstone to Uttley, K. H. (1960). The mortality and epidemiology of cattle by the herring gull (Lasus argentatus). Veterinary typhoid fever in the coloured inhabitants of Antigua. West Record, 100, 450-451. Indies, over the last hundred years. West Indian Medical Willinger. H. and Thiemann, G. (1978). On the survival of Journal, 9, 114-123. bacterial pathogens in aerated liquid manure of cattle. In Van Donsel, D. J. and Geldreich, E. E. (1971). Relationships Animal and Hiunan Health Hazards Associated wvith the of salmonellae to fecal coliforms in bottom sediments. Utiliation of Animal Effiuents. Ed. Kelly, W. R., pp. Water Research, 5, 1079-1087. 203-208. Luxembourg: Office of Official Publications of Vasconcelos, G. J. and Swartz, R. G. (1976). Survival of the European Communities. bacteria in seawater using a diffusion chamber apparatus Wray. C. and Sojka, W. J. (1977). Reviews of the progress of in situ. Applied and Environmental Microbiology, 31, dairy science: bovine salmonellosis. Journal of Dairy 913-920. Research, 44, 383-425. Walker, J., Carbonnelle, B. and Leclerc, H. (1977). Auto- Yanez, F. (1980). Evaluation of'the San Juan Stabilization epuration microbienne par lagunage. Water Research, II, Ponds, Final Research Report ofthe First Phase. Lima: Pan 17-29. American Center for Sanitary Engineering and Walker, W. (1965). The Aberdeen typhoid outbreak of 1964. Environmental Sciences. Scottish Medical Journal, 10, 466-479. Yaziz, M. I and Lloyd, B. J. (1979). The removal of Watson, D. C. (1980). The survival of salmonellae in sewage salmonellas in conventional sewage treatment proccsses. sludge applied to arable land. Water Pollution Control, 79. Journial of'Applied Bacteriology, 46, 131-142. 11-18. Zaki, M. H., Miller, G. S., Sheppard, R. J.. Harris, D. and Watt, J., Hollister, A. C., Beck, M. D. and Hemphill, E. C. McLaughlin, M. C. (1979). An extensive Salnionella (1953). Diarrheal diseases in Fresno County, California. typhimurium outbreak of probable waterborne origin. American Journal of Public Health, 6, 728-741. Journal of the American Water Works Association, 71, Watt, J. and Lindsay, D. R. (1948). Diarrheal disease control 287 291. studies. 1. Effect of fly control in a high morbidity area. Zibilske, L. M. and Weaver, R. W. (1978). Effect of Public Health Reports, 63, 1319-1334. environmental factors on survival of ii, typhi- White, K. E. (1979). Use of ionizing radiation to disinfect murium in soil. Journal of' Environmental Qualitv, 7. sludge. In Utilisation of Sewage Sludge on Land, pp. 593-597. 16 Shigella and Shigellosis DYSENTERY, the frequent passing of bloody presence of many pus cells in the stool is highly stools, has been recognized and feared throughout suggestive of this diagnosis. history as a serious and sometimes fatal condition. One major cause of dysentery is infection by members of the Occurrence bacterial genus Shigella (the other major cause is infection by the protozoon Entamoeba histolytica- Shigellosis has a worldwide distribution, with the described in chapter 20). highest incidence in communities where hygiene is poor. Children aged 1-4 years are the most affected, and 60 percent of cases and most fatalities are children under 10 years of age. Description of Pathogen and Disease The different species of Shigella vary in their relative importance in different parts of the world. In Asia, South America, and Africa, Shigella dysenteriae is often Shigellae, and the infections they cause in man, are well documented in many countries. Together with responsible for severe disease, but all species are Salmonella species (chapter 15) and Vibrio cholerae common. Shigellosis in the developed countries is most (chapter 17), they are the classic bacterial agents of commonly caused by Shigella sonnei. In England and (chaptertinal 17)cth. Wales 43,285 cases were reported in 1960 and 10,765 intestinal infection. cases in 1970. At present some 98 percent of the infections in England and Wales are caused by Sh. sonnei, and the majority of known cases of infection Identification with Sh. flexneri, Sh. boydii, or Sh. dysenteriae are persons recently returned from developing countries. Shigellosis (bacillary dysentery) is an acute diarrheal All types of shigellae are found in areas of inadequate disease caused by bacteria of the genus Shigella. The sanitation and poverty; Sh. dysenteriae, Sh. flexneri, disease, which primarily involves the large intestine, and Sh. boydii are the most frequently identified, and may be asymptomatic or may have symptoms ranging Sh. sonnei infections are relatively rare. As hygiene from mild diarrhea to a severe disease accompanied by improves, Sh. sonnei becomes the dominant species, fever, vomiting, cramps, and tenesmus, with blood, Sh. flexneri the next most common, and Sh. boydii and mucus, and pus in the stools. The typical case is of short Sh. dysenteriae become rare. When conditions of duration (about 4 days), but in exceptional cases the hygiene degenerate, such as with an army in the field, symptoms may last for up to 2 weeks. The severity of infections with species other than Sh. sonnei again the illness and the mortality rate depend on the become common. nutritional state and age of the patient, on the serotype of the organism, and on the infecting dose. The severe form of the disease, bacillary dysentery, is Infectious agent often due to Shigella dysenteriae. Disease due to type I Shigellae are Gram-negative, nonmotile rods be- (Shiga's bacillus) is particularly serious. Mortality of longing to the family Enterobacteriaceae and closely untreated cases of bacillary dysentery may be as high as resembling Escherichia coli and Salmonella (figures 13- 25 percent but is usually much lower. Diagnosis is by la and 15-1). Four major serological groups have been isolation of the bacteria from feces or rectal swabs. The described, with some forty serotypes making up these 287 288 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA groups. The group and type antigens are all cell-wall produced disease (oral temperature >37.80C, with antigens, but group antigens are difficult to de- four or more watery stools per 24 hours) in 59 percent monstrate. of eighty-eight adult male volunteers, whereas a dose of eincludes at least ten 180 produced disease in 22 percent of thirty-six segrouypeA, with dethriaee,othersprovisionally volunteers. Levine and others (1973) induced disease serotypes, with three others provisionally re- cognized. Phage-typing systems are also used. (oral temperature >Ž 37.8°C, with three or more watery stools ner 24 hoursl in one out of ten adult male * group B, Sh. flexneri, includes nine serotypes that are r 2 related not only by a common group antigen but volunteers with only 10 virulent Sh. dysenteriae type 1. also by various shared type antigens. Phage-typing By contrast, Shaughnessy and others (1946) required systems are also used. massive doses of Sh. flexneri (108 organisms) to induce systems are also used. . group C, Sh. bovdi. includes fifteen serotypes and disease in volunteers who had previously ingested 2 .'. ' - '. . . ~~~grams of sodium bicarbonate to lower their gastric two additional, provisional serotypes. Phage-typing gamdityo systems are also used. acidity. l group D, Sh. sonnei, includes only one serotype, and colicin-typing and phage-typing are used to Incubation period subdivide the group. The incubation period ranges from 36-72 hours; frank dysentery usually appears within 2 days. Reseruoir Period of communicability Shigellae have no natural hosts other than the higher Patients recovering from an acute attack of primates. Although experimental infections can be . . . shigellosis may continue to excrete bacilli in their produced in other primates, man is the only effective source of infection. Unlike Salmonella and Escherichia stools. In general, this excretion lasts for only a week or so, but a small proportion become persistent carriers. infections, animal feces are not a source of inocula, DuPont and others (1970) found that 75 percent of 542 though animals may become contaminated by the children who contracted shigellosis at an institution for ingestion of human feces. the mentally retarded in New York (USA) excreted Sligella for less than I month, but that 7 percent Transmission continued to excrete the organism for over a year. There is also evidence of the presence of shigellae in Shigellae are transmitted from man to man, from ill completely symptomless carriers, and carriage for persons, healthy convalescents, or symptomless car- periods of years may be common under conditions of riers to susceptible persons. The organisms, which are poor hygiene. In this context the carriage of shigellae excreted in the feces, are usually transmitted by the for long periods by breast-fed infants should be noted. direct fecal-oral route. Infected persons with diarrhea In such infants overt disease is seldom seen until breast typically excrete 105-109 shigellae per gram of wet feeding ceases. feces, while symptomless carriers may excrete 102-106 per gram (Dale and Mata 1968; Thomson 1955). Food may be contaminated through the contaminated fingers of patients or carriers. Foodborne and Children are especially susceptible, and natural waterborne outbreaks occur. However, contamination resistance to Shigella infection has not been reported. of the environment (such as seats, door handles, and Individuals in closed communities may have numerous water-flushing devices in toilets) by infected feces and repeated infections with a single serological type of their transfer to the mouth seems to be the usual mode Shigella. Such immunity as does occur is probably of infection. Transfer of shigellae by flies breeding on group specific and may involve the local production of feces has been ofcrucial importance in some outbreaks. short-lived antibodies in the colonic mucosa. The infective dose for Shigella is reported to be lower than for the other main diarrhea-causing bacterial pathogens (Salmonella, Vibrio cblolerae, and E. coli). Epidemiolog: The median infective dose (ID50) for Shigella may be Shigellosis is endemic and common in almost all around 104 in healthy adults; for the other bacterial communities where living standards are low and water pathogens listed above, it is 107 or higher. Dupont and and excreta disposal facilities inadequate. It may also others (1972) found that a dose of 104 Sh. flexneri be endemic in some institutions, such as schools and SHIGELLA AND SHIGELLOSIS 289 geriatric wards, where poor hygiene occurs. Children, Shahidullah (1980) found similar infection and especially weanlings, suffer the highest incidence of diarrhea rates among family contacts of index cases infection and mortality, and malnourished children are having Sh. dysenteriae type I infection. Among family especially vulnerable. contacts of index cases having Sh. flexneri infection, 20 Shigella infections among poor people in developing percent were infected, but the proportion of those countries are often very common. Over a 1-year period infected who experienced diarrhea was only 20 percent. in an Egyptian village, for instance, 51 percent of Reller, Gangarosa and Brachman (1969) reviewed eighty-two children between 6 months and 5 years old shigellosis in the USA over the period 1964-68. had one episode, 17 percent had two episodes, and 5 Approximately 10,000 cases per year were reported percent had three or more episodes (Higgins and Floyd (very many will have gone unreported), and the highest 1955). Several studies have shown that up to about 18 attack rate occurred in the 0-4 age group. Peak percent of young children in poor communities may be incidence was in the late summer of each year. excreting Shigella at any time. Beck, Munoz and Residents of mental institutions, Indian reservations, Scrimshaw (1957) reported that the point prevalence of and urban slums were identified as being especially at Shigella excretion among children under 10 years old risk from shigellosis. Fifty-four percent of isolations in twelve communities in Guatemala varied between were Sh. sonnei and 40 percent were Sh. flexneri. Only 3.7 and 16.2 percent. Richardson and others (1968) 6.6 percent of reported cases of shigellosis were recorded that 13 percent of African school children associated with either foodborne or waterborne (7-16 years old) in the Western Transvaal (South outbreaks (Black, Craun and Blake 1978). Africa) were excreting Shigella (mainly Sh. flexneri) in The transmission of Sh. sonnei among school summer. In the USA, Shigella excretion prevalences of children in England was studied by Hutchinson up to 10 percent among children have been recorded in (1956), who isolated the organism from toilet seats, some samples of farm labor families in California and toilet floors, chamber pots, clothes, bedding, toys, and mining families in Kentucky (Hollister and others floors. Eleven out of thirty-four toilet seats were found 1955; Schliessmann and others 1958; Watt and others to be contaminated in a school during an epidemic. 1953). It has been estimated that the prevalence of When heavily infected, loose, bulky stools were flushed Shigella excretion among the whole population is 0.46 away it was found that contamination of the seat could percent in the USA, 0.33 percent in England and Wales, occur, but this did not appear to happen with solid and 2.4 percent in rural Sri Lanka (Geldreich 1972). stools. As many as 50 percent of children were found to Khan and Mosley (1968) studied shigellosis in Rayer be hand carriers after visiting a toilet at the peak of an Bazar, a village on the outskirts of Dacca (Bangladesh). outbreak. Observations at a nursery school showed Shigellosis occurred throughout the year with a peak that, of thirty-seven children, half handled the seat when during the monsoon (June-October). Seventy-one settling themselves on it, and one-third of these then percent of shigellosis cases identified were children either handled their face or mouth or sucked their under 5 years old. The proportion of all recorded fingers. On the skin of the fingers Sh. sonnei remained diarrheas that were associated with Shigella was 4.4 alive for over 3 hours. Tests with five types of toilet percent. Khan, Curlin and Huq (1979) studied the paper showed that, when double thicknesses of paper families of forty-seven index cases with diarrhea due to were used, organisms from fluid or semisolid feces Sh. dysenteriae type I in Dacca. Twenty percent (49 of passed through the paper to the fingers each time. With 240) of family contacts of index cases were infected with solid feces the organisms passed through four out of Shigella at some time during the 10 days following the five of the papers. reporting of the index case. The proportion of infected There is general agreement in the literature that the family contacts was highest (31 percent) among maintenance of endemic shigellosis has little or no children 0-4 years old. Of the forty-nine infected family relationship to water quality, but that it is strongly contacts, five (10 percent) required hospitalization and related to water availability and associated hygienic twenty-seven (55 percent) developed mild to moderate behavior. However, there will always be specific diarrhea. The equivalent proportions among the 0-4 exceptions to this; for instance, Sultanov and age group were 27 percent and 73 percent-in other Solodovnikov (1977) considered that the maintenance words, there were no asymptomatic infections in this of dysentery in Dagestan (USSR) during 1959-73 was age group. Poor families living in one-room houses due to the widespread use of polluted surface water for with "open latrines" and unprotected water sources domestic purposes. had higher secondary infection rates than other Shigellosis occurs in epidemics in addition to being families. In another study in Dacca, Khan and endemic. In 1969 and 1970 an epidemic due to Shiga's 290 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA bacillus (Sh. dysenteriae type i) occurred in Central Individual America and Mexico in which there were an estimated 112,000 cases and 8,300 deaths in Guatemala alone in it, antiobiap hlaxis hase to recommen the first 10 months of 1969 (Gangarosa and others ,t although individual agents have been used for the the9first Majr montbs o f 1969 hiGgarosa dysndte lso control of institutional outbreaks. Sulphonamide and 1970). Major outbreaks of Shiga dysentery also tetracycline have been used widely in some communi- occurred in Bangladesh in 1973 (Rahaman and others ties, but their use has a dubious effect. It must be 1975) and in Somalia in 1963-64 (Cahill, Davies and Johndson1966) Shigella strains 196 4 (Casmi,d-eiates a remembered that resistance transfer factors were first Johnson 1966). Shigella strains with plasmid-mediat described in Shigella and that the worldwide resistance multiple drug resistance were involved in Cent of these bacteria to sulphonamides (and often also to Somerica epidei Banlares waterborne.Anoutbreak other antibiotics including tetracycline, streptomycin, some 2,000 cases of shigellosis due to Sh. sonnei chloramphenicol, and ampicillin) is the result of the some2,00 caes o shiellsis ue t Sh sonei' spread of such factors. occurred in 1966 in Montrose (Scotland) when the sra fsc atr Killed vaccines are ineffective. Live oral vaccines are chlorination plant on the town's water supply broke still at an experimental stage. They are type specific and down (Green and others 1968). During 1961-75, sila neprmna tg.Te r yeseii n thirty-eight waterborne outbreaks (comprising 5,893 protect for short periods against the disease. They are thiry-eiht wterorneoutbeaks(coprisng 5893 difficult to prepare and administer and are therefore of cases) of shigellosis were reported in the USA (Black, limited use. Craun and Blake 1978). Most of these outbreaks tdu. iraunvol d s Blice or78). indviua wthe sytbemsa Scrupulous personal hygiene is the most effective volved semipublc or idividual water systems and .means of individual rotection. Breast feedin were usually the result of inadequate or interrupted gonsiofralyvrduct rof Breast fants. chlorination of water contaminated by feces. An considerably reduces the risk of disease in Infants. outbreak due to Sh. sonnei and linked with bathing in a polluted section of the Mississippi River in Iowa (USA) Environmental has been reported (Rosenberg and others 1976). Some epidemics are foodborne. An outbreak of at There is probably more information available on the least 600 cases occurred on the island of Maui (Hawaii, effect of environmental improvements in reducing USA) in 1970. Shigella sonnei was the causative shigellosis than on any other infection described in this bacterium, and the outbreak was spread by the book. Studies have been conducted into the spread and contamination of poi (ground taro root) produced at a control of shigellosis in institutions in developed single factory and distributed around the island (Lewis countries (such as the work of Hutchinson, sum- and others 1972). It was shown that Sh. sonnei in poi marized above), and other investigations have could undergo a tenfold increase in concentration in 1 examined the role of environmental modifications in day at room temperature. An outbreak of at least 140 controlling shigellosis in poor communities (see table cases (culture-positive for Sh. sonnei) occurred in 1979 2-1). These later studies have either used diarrhea rates among hospital staff in the USA and was linked to the or the prevalence of Shigella isolations from rectal contamination of tuna salad by an infected cafeteria swabs from a sample of the community, often children. employee (Bowen 1980). During 1961-75, seventy-two In towns in Georgia (USA) Stewart and others foodborne outbreaks (comprising 10,648 cases) of (1955) found that Shigella infection was related to poor shigellosis were reported in the USA (Black, Craun and water supply, poor excreta disposal facilities, high fly Blake 1978). Most of these outbreaks were caused by counts, and to poor housing in general. More contaminated salads associated with poor hygiene specifically it was found that, among otherwise similar among food handlers. households, those with water close to the house had a lower incidence than those who fetched water from further away, but that the type of water source (well or tap) did not affect shigellosis incidence. A subsequent Control Measures study in Georgia (McCabe and Haines 1957) recorded that a latrine program (bored hole latrines, 2.5 meters deep) in the town of Boston was associated with a Shigella bacteria are transmitted from person to reduction in the detection of Shigella from 4.7 percent person, especially where hygiene is poor and the to 2.8 percent of rectal swabs. Rates in the control domestic environment is fecally contaminated. towns did not fall over the period. After completion of Effective control depends upon personal hygiene and the latrine program, the rate of reported diarrhea was the sanitary disposal of excreta. half that in the control towns. Although the housefly SHIGELLA AND SHIGELLOSIS 291 population was not reduced, the breeding of flies in data give no indication that privies as used in the excreta was much reduced. villages had any influence on the diarrheas of children Schliessmann and others (1958) investigated in the first two years of life, the important part of the environmental influences on shigellosis in 11 mining problem." A summary of surveys of diarrhea among camps in the eastern coalfields of Kentucky (USA) preschool children in Bangladesh, Egypt, Iran, during 1954 to 1957. Reported diarrheal disease rates Mauritius, Sri Lanka, Sudan, and Venezuela (van Zijl ranged from 9.4 to 53.6 per 100 persons per year in the 1966) concluded that water supplies and excreta different study areas. More than half the total cases disposal facilities were important determinants of were children between 0 and 4 years old, and more than shigellosis (see also Wolff, van Zijl and Roy 1969). one-quarter were under 2 years old. The highest Rajasekaran, Dutt and Pisharoti (1977) studied incidence occurred in August and September. Shigella 1,041 children under 5 years old for 1 year in five isolation rates, obtained by rectal swabbing of villages in Tamil Nadu (India). Thirty-two percent of preschool children, ranged between 0.7 percent and 10 all diarrheal episodes were associated with Shigella percent in individual study areas. Seventy-six percent excretion. Those who used an open well (98 percent of of Shigella isolates were Sh. flexneri. Shigellosis was the water samples contained > 10 coliforms per 100 major cause of acute diarrhea in the areas with poor milliliters) had a significantly lower incidence of sanitation but was not a primary cause in the areas diarrhea and shigellosis than those who used a street with the best sanitation. Housefly populations were tap (25 percent of water samples contained > 10 generally low and were not associated with Shiigella coliforms per 100 milliliters). Those who used tap water prevalence. Water quality was not related to the in the house had a lower incidence than both well users incidence of diarrhea or to the prevalence of Shigella and street tap users. Preliminary findings from Teknaf excretion. Those having flush toilets and inside water (Bangladesh) suggested that diarrhea and shigellosis had an incidence of diarrhea of 14 per 100 persons per incidences were inversely related to the daily per capita year and a Shigella excretion prevalence of 1.1 percent; usage of tubewell water (Rahaman 1979). those having inside water but an outside latrine had These and other studies (see table 2-1) indicate that a figures of 24 per 100 per year and 2.4 percent; and those plentiful water supply located close to or in the home having outside water and an outside latrine had an (to allow good personal cleanliness) and an adequate incidence of 36 per 100 per year and a Shigella latrine that is properly used are key elements in the prevalence of 5.9 percent. Where water was not piped control of shigellosis. Good personal and domestic inside the house, persons having access to water in their hygiene and restricting the access of flies to human yard had a diarrhea incidence one-third less than excreta are also important. Water quality is not of individuals obtaining water away from their premises particular importance in communities where shigell- (see also Schliessmann 1959). osis is highly endemic. In the San Joaquin Valley of California (USA), Watt It must be emphasized that those who most and others (1953) reported that the Shigella excretion commonly experience shigellosis, those who most prevalences among children under 10 years old were commonly excrete Shigella, and those for whom the higher in migrant worker camps (6.1 percent) than in consequences of infection are potentially the most poor but permanent housing on urban fringe areas (3.9 serious are small children. Small children are not only percent). A follow-up study on the camps (Hollister the major sufferers but also the major source of the and others 1955) recorded the following Shigella bacteria, which will contaminate the domestic environ- excretion prevalences among children under 10 years ment and subsequently infect other children and old: in cabins with inside water, shower, and toilet, 1.6 adults. The personal hygiene of small children, and percent; in cabins with inside water but with mother-child behavior patterns, are therefore of great communal shower and toilet, 3.0 percent; in cabins importance in controlling shigellosis. with no internal facilities, 5.8 percent. Studies in the Lower Rio Grande Valley in Texas (USA) showed that fly control with DDT reduced the rates of both Occurrence and Survival in the diarrheal disease and Shigella isolation (Watt and Environment Lindsay 1948). Gordon, Behar and Scrimshaw (1964) reported a Although the shigellae are among the most comparison of acute diarrheal disease rates between important pathogenic excreted bacteria, their presence families having a latrine and those having no latrine in and persistence in the environment have been studied rural Guatemala. The authors concluded that "the far less than is the case for E. coli and the salmonellae. 292 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA In water Limited tests on Sht,lgifo in seawater (Nakamura and others 1964) suggest that survival times (15 to Shigellae will be found in low concentrations in most more than 70 days at 15°C) may be somewhat longer surface waters contaminated by human feces. They will mr hn7 asa 5Qmyb oehtlne therefore be present in many contaminated drinking than those in freshwater-in contrast to the fecal indicator bacteria (chapter 13), which die more rapidly water sources in developing countries, although their in seawater than in freshwater. Tests in sterile saline presence is almost never sought In routine water tresting.cUnlikethe salmo nelaver t in co/ti,and ftea waters (salinities = 0.5, 2.5, and 3.5 percent) at various testing. Unlike the salmonellae, E. coli, and fecal tepraue (4 5 7 oee,shwdta streptococci, the shigellae are excreted only byman and temperatures (4, 25, 37 C), however, showed that because much contamination of village water supplies S/i dvsenteria survived or ess than 6 days, even at 4C derives from animals, the concentrations of shigellae (Jamieson, Madri and Claus 1976). will in general be much lower than the concentrations of the fecal indicator bacteria or the salmonellae. In feces and sewage Tap water will only contain shigellae if it is untreated and drawn from a contaminated source, or if the Between perhaps 0.2 percent and 4 percent of a treatment plant has broken down-as in the Montrose community will be excreting ll,,',iio depending on (Scotland) outbreak (Green and others 1968). the levels of hygiene that prevail. Sewage may Some studies on the survival of shigellae in water are therefore contain between about 10 and 104 ,.w, Pi listed in the appendixes of Feachem and others (1980). per liter. Survival depends upon factors such as the concen- Few data are available, but it is likely that survival in trations of other bacteria, nutrients, and oxygen and on feces and sewage is curtailed by the activity of the large the temperature. In clean waters, survival times are populations of other bacteria present. Survival is typically less than 14 days at warm temperatures enhanced at low temperatures, by sterilizing the feces (>20°C), whereas the bacteria may survive for a few or sewage prior to introducing the shigellae, or by weeks below 10°C. At warm temperatures, 99 percent raising the pH. Hutchinson (1956) studied the survival reduction in M;'.,t/i.: numbers is likely to occur in less time of Sh. sonnei in naturally infected feces. At room than 5 days. McFeters and others (1974) found that temperature, survival times varied between 2 and 26 shigellae died more slowly in well water at 9-12°C than days depending on the initial concentration of the fecal indicators, salmonellae, or Vibrio chole7ae (the shigellae, which varied from 7 x 103 to 3.2 x I 0 per half-life of the shigellae was about 24 hours). gram. With an initial concentration of 1.5 x 106 per Survival is most prolonged in very clean waters (such gram, none could be detected after 7 days storage at as unchlorinated tap water) or in polluted water 37°C, whereas an 82 percent reduction occurred at containing nutrients but having a minimum of other 20°C. Kligler (1921) reported that Sh. dysenteriae bacteria present. In these latter conditions, i survived for less than 6 days in septic tank effluent. may grow. Talayeva (1960) recorded survival of Experiments in China (McGarry and Stainforth 1978) Shigellaflexneri at 19-24°C for up to 21 days in clean showed that Sh. dysenteriae survived for up to 17 days river water, up to 47 days in autoclaved river water, up in biogas plant effluent (I 1-28°C) but for less than 30 to 9 days in well water, up to 44 days in autoclaved tap hours in the biogas plant itself (14 24°C). water, and for up to 6 days in polluted well water. McGarry and Stainforth (1978) reported experiments in China that showed the survival of Sh. dysenteriae for On surlaces up to 93 days in sterilized water at 11 28°C. The transmission of shigellosis depends substan- Shrewsbury and Barson (1957) made up sterile tially on the contamination of clothes, hands, and synthetic well water of the same general composition as household surfaces the bacteria are transferred from that obtained from Hagar's Well in Mecca (Saudi these surfaces to the mouth. Hutchinson (1956) Arabia) at the time of the 1883 cholera outbreak. recorded that Sh. sonnei could survive for over 3 hours Shigellae could survive for between 2.5 and 29 months on the fingers and for up to 17 days on a wooden toilet in this sterile but fecally contaminated water at 21°C. seat. Survival was prolonged by low temperature, high Hendricks (1972) reported that Sh. flexneri multiplied humidity, and poor lighting. Spicer (1959) found that in sterilized river water collected downstream from a Sh. sonnei survived for 7-10 days on cotton threads at sewage outfall. Growth occurred at 30°C but not at cool temperatures and high or low humidities. 20°C or 50C, and no growth at any temperature was Nakamura (1962) studied Sh. sonnei survival at various recorded in water collected upstream from the sewage temperatures on metal, wood, cotton, paper, and glass outfall (see also Hendricks 1971). in a laboratory with relative humidities between 17 and SHIGELLA AND SHIGELLOSIS 293 33 percent. Survival times were 10-5 7 days at - 20'C. nine bacteria per cubic meter of air and that shigellae 4-40 days at 4°C, 2-28 days at 15°C, 0-13 days at 37°C dispersed in splashes from the toilet could survive for and 0 2 days at 45°C. At 15°C, survival was longer on up to 4 days. cotton, wood, and paper than on glass and metal. It is Hickey and Reist (1975) failed to isolate any noteworthy that toilets and latrines are often relatively airborne shigellae downwind from two activated cool, humid, and poorly lit conditions ideal for the sludge tanks in the USA, and they attribute this to the optimal survival of shigellae on interior surfaces. very low concentrations of shigellae in the sewage. Katzenelson, Buium and Shuval (1976) found that the In lbod incidence of shigellosis on 77 kibbutzim practicing wastewater spray irrigation was 10 cases per 1,000 The contamination of food with shigellae is persons per year, whereas the incidence on 130 probably an important route of transmission in many kibbutzim practising no form of wastewater irrigation communities (see, for instance, Barrell and Rowland was 4.5 cases per 1,000 per year. 1979). Taylor and Nakamura (1964) reported that Sh. sonnei and Sh. flexneri survived for considerable periods (80 days or more) in foods such as flour, eggs, Inactivation by Sewage Treatment oysters, clams, and milk. At warm temperatures (25°C) Processes some growth was noted. Acidic foods, such as orange juice, were more hostile environments for shigellae; Few studies have been conducted on the inactivation even so, the organisms remained detectable in these of shigellae by sewage treatment plants-in part foods for up to 10 days. because they are difficult organisms to enumerate in sewage and in part because it is quite common to fail to find any in sewage, even where the community is On crops known to be infected (for instance Brezenski, The few studies on Shigella survival on crops Russomanno and DeFalco 1965; Daniel and Lloyd irrigated with night soil or sewage are listed in the 1980; Dixon and McCabe 1964; Olivieri, Kawata and appendixes of Feachem and others (1980). Shigellae on Kruse 1978; Wang, Dunlop and De Boer 1956). The crop surfaces will typically be exposed to warm data that are available suggest that removal of shigellae temperatures, bright sunlight, and rapid drying. These is very similar to E. coli removal (chapter 13). factors are all hostile to shigellae, and reported survival Conventional treatment plants, without tertiary times are nearly always less than 7 days (Geldreich and processes, will remove between 90 and 99 percent Bordner 1971; Rudolfs, Falk and Ragotzkie 1951). It is (Kabler 1959), whereas waste stabilization ponds can probable that, in arid hot climates, only a very small remove a far higher proportion. It is likely that the fraction of shigellae on crops would survive beyond 2 survival of shigellae in sewage and sewage effluents is days. Babov, Nadvornyi and Keimakh (1967) reported considerably shorter than the survival of E. coli. that a variety of vegetables grown on sewage farms at Slijkhuis, Betzer and Kott (1976) reported that Odessa (USSR) were contaminated by Sh. flexneri. Sh. flexneri were not detectable after 2 days in a waste Contamination was eliminated when irrigation was stabilization pond in Israel. stopped 2 weeks before harvest, but harvested vegetables could be recontaminated by being laid on the soil. Inactivation by Night Soil and Sludge Treatment Processes In the air There are no data available on Shigella destruction As with other enteric bacteria and viruses (see in most sludge treatment processes. However, the chapters 9 and 13), shigellae may be spread in aerosol conditions of sludge treatment will be highly droplets produced by flush toilets, activated sludge antagonistic to shigellae, and high rates of destruction plants, and spray irrigation systems. Hutchinson may be expected. It is probable that Shigella (1956) found that toilet seats were contaminated by destruction will proceed considerably more rapidly droplets containing shigellae when a loose stool was than that of the fecal indicator bacteria (chapter 13). flushed away but not when a solid stool was flushed. Processes about which data are available are Newson (1972) found that flushing a fluid suspension composting and heating. Studies on aerobic thermo- of 1010 Sh. sonnei produced an aerosol of about thirty- philic composting of night soil and garbage in Beijing 294 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA 60 - - 60 ss- ZONE - 55 50- OF -s ~~~~~~~~~~~~~~SAFET 45- 45 40D 40 35 35 30 - 100% destruction of Shigella 30 * less than 1000% destruction of Shigella |2 25- 25 Ar -V Jr JrX It 20 I I l lI I I l 20 0.1 10 100 1000 10000 Ihour Iday Iweek lmonth lyeor TIME (HOURS) Figure 16-1. The influence of time and temperature on Shigella. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death (China) showed that seeded Sh. dysenteriae were on the survival of pathogens in nightsoil compost. Indian destroyed within 5 days in piles with a temperature of Journal of Agricultural Science, 27, 91-102. up to 50°C (Chinese Academy of Medical Sciences Black, R. E., Craun, G. F. and Blake, P. A. (1978). 1975). Other studies and reviews (for instance Epidemiology of common-source outbreaks of shigellosis Bhaskaran and others 1957; Petrick 1954; Wiley 1962) in the United States, 1961-1975. American Journal oJ confirm the elimination of shigellae from well- Epidemiology, 108, 47-52. managed thermophilic composting systemsbutBowen, G. S. (1980). An outbreak of shigellosis among staff managed thermophilic composting systems but warn mebr' falreubn optl nEiei members of a large urban hospital. In Epidemic that shigellae, and other enteric bacteria, may survive Intelligence Service 29th Annual Conference, p. 46. Atlanta, on the edge of a pile where temperatures remain low Georgia: Centers for Disease Control. (Reeves 1959). Various data on Shigella destruction by Brezenski, F. T., Russomanno, R. and L)eFalco, P. (1965). time-temperature effects have been compiled in figure The occurrence of Salmonella and Shigella in post- 16-1, and it may be seen that 1 hour at 55°C, 1 day at chlorinated and non-chlorinated sewage effluents and 45°C, and 1 week at 40°C are lethal combinations. receiving waters. Health Laboratory Science, 2, 40-47. Cahill, K. M., Davies, J. A. and Johnson, R. (1966). Report on an epidemic due to Shigella dvsenteriae Type I in the Literature Cited Somali interior. American Journal of Tropical Medicine and Hygiene, 15, 52-56. Babov, D. M., Nadvornyi, N. N. and Keimakh, A. S. (1967). Chinese Academy of Medical Sciences, Department of The microflora of vegetables and other crops grown on Environmental Health, Institute of Health, Beijing (1975). sewage farms. Hygiene and Sanitation, 32, 273-275. Sanitary effects of urban garbage and nightsoil compost- Barrell, R. A. E. and Rowland, M. G. M. (1979). Infant foods ing. Chinese Medical Journal, 1, 407-412. as a potential source of diarrhoeal illness in rural West Dale, D. C. and Mata, L. J. (1968). Studies of diarrheal Africa. Transactions of the Royal Society of Tropical disease in Central America. XI. Intestinal bacterial flora in Medicine and Hygiene, 73, 85-90. malnourished children with shigellosis. American Journal Beck, M. D., Munoz, J. A. and Scrimshaw, N. S. (1957). of Tropical Medicine and Hygiene, 17, 397-403. Studies on diarrheal diseases in Central America. 1. Daniel, R. R. and Lloyd, B. J. (1980). Microbiological studies preliminary findings on cultural surveys of normal on two Oxfam sanitation units operating in Bengali population groups in Guatemala. American Journal of refugee camps. Water Research, 14, 1567-1571. Tropical Medicine and Hygiene, 6, 62-71. Dixon, F. R. and McCabe, L. J. (1964). Health aspects of Bhaskaran, T. R., Ghosh Roy, B. K., Sampathkumaran, M. wastewater treatment. Journal of the Water Pollution A., Radhakrishnan, I. and Mukherjee, D. B. (1957). Studies Control Federation, 36, 984-989. SHIGELLA AND SHIGELLOSIS 295 DuPont, H. L., Gangarosa, E. J., Reller, L. B., Woodward, W. by sewage treatment processes. Sewage and Industrial E., Armstrong, R. W., Hamrnond, J., Glaser, K. and Wastes, 12, 1373-1382. Morris, G. K. (1970). Shigellosis in custodial institutions. Katzenelson, E., Buium, I. and Shuval, H. I. (1976). Risk of American Journal of Epidemiology, 92, 172-179. communicable disease infection associated with wastewater DuPont, H. L., Hornick, R. B., Snyder, M. J., Libonati, J. P., irrigation in agricultural settlements. Science, 194, Formal, S. B. and Gangarosa, E. J. (1972). Immunity in 944-946. shigellosis. II. Protection induced by oral live vaccine or Khan, M., Curlin, G. T. and Huq, I. (1979). Epidemiology of primary infection. Journal of Infectious Diseases, 125, Shigella dysenteriae, type 1 infections, in Dacca urban area. 12-16. Tropical and Geographical Medicine, 31, 213-223. Feachem, R. G. A., Bradley, D. J., Garelick, H. and Mara, D. Khan, M. and Mosley, W. H. (1968). The significance of D. (1980). Health Aspects of Excreta and Sullage Shigella as a cause of diarrhea in a low economic urban Management: A State-of-the-Art Review. Appropriate community in Dacca. East Pakistan Medical Journal, 12, Technology for Water Supply and Sanitation, vol. 3. 45-51. Washington, DC: The World Bank, Transportation, Khan, M. and Shahidullah, Md. (1980). Epidemiologic Study Water and Telecommunications Department. of Dysentery Cases of Dacca Urban Area. Scientific Report Gangarosa, E. J., Perera, D. R., Mata, L. J., Mendizabal- no. 33. Dacca: International Centre for Diarrhoeal Morris, C., Guzman, G. and Reller, L. B. (1970). Epidemic Disease Research, Bangladesh. Shiga bacillus dysentery in Central America. II. Epidemio- Kligler, I. J. (1921). Investigation on Soil Pollution and the logic studies in 1969. Journal of Infectious Diseases, 122, Relation of the Various Types of Privies to the Spread of 181-190. Intestinal Infections. Monographs of the Rockefeller Geldreich, E. E. (1972). Water-borne pathogens. In: Water Institute for Medical Research, 15. New York. Pollution Microbiology. Ed. Mitchell, R. pp. 207-241. New Levine, M. M., DuPont, H. L., Formal, S. B., Hornick, R. B., York: Wiley-Interscience. Takeuchi, A., Gangarosa, E. J., Snyder, M. J. and Libonati, Geldreich, E. E. and Bordner, R. H. (1971). Fecal J. P. (1973). Pathogenesis of Shigella dysenteriae 1 (Shiga) contamination of fruits and vegetables during cultivation dysentery. Journal of Infectious Diseases, 127, 261-270. and processing for market: a review. Journal of Milk and Lewis, J. N., Loewenstein, M. S., Guthrie, L. C. and Sugi, M. Food Technology, 34, 184-195. (1972). Shigella sonnei outbreak on the Island of Maui. Gordon, J. E., Behar, M. and Scrimshaw, N. S. (1964). Acute American Journal of Epidemiology, 96, 50-58. diarrhoeal disease in less developed countries. Bulletin of McCabe, L. J. and Haines, T. W. (1957). Diarrheal disease the World Health Organization, 31, 1-28. control by improved human excreta disposal. Public Green, D. M., Scott, S. S., Mowat, D. A. E., Shearer, E. J. M. Health Reports, 72, 921-928. and Macfarlane Thomson, J. (1968). Water-borne McFeters, G. A., Bissonnette, G. K., Jezeski, J. J., Thomson, outbreak of viral gastroenteritis and Sonne dysentery. C. A. and Stuart, D. G. (1974). Comparative survival of Journal of Hygiene, 66, 383-392. indicator bacteria and enteric pathogens in well water. Hendricks, C. W. (1971). Enteric bacterial metabolism of Applied Microbiology, 27, 823-829. stream sediment eluates. Canadian Journal of Micro- McGarry, M. G. and Stainforth, J., eds. (1978). Compost, biology, 17, 551-556. Fertilizer and Biogas Production from Human and Farm -_ (1972). Enteric bacterial growth rates in river water. Wastes in the People's Republic of China. Ottawa: Applied Microbiology, 24, 168-174 International Development Research Centre. Hickey, J. L. S. and Reist, P. C. (1975). Health significance of Nakamura, M. (1962). The survival of Shigella sonnei on airborne micro-organisms from wastewater treatment cotton, glass, wood, paper and metal at various processes. 1. Summary of investigations. Journal of the temperatures. Journal of Hygiene, 60, 35-39. Water Pollution Control Federation, 47, 2741-2757. Nakamura, M., Stone, R. L., Krubsack, J. E. and Pauls, F. P. Higgins, A. R. and Floyd, T. M. (1955). Studies in shigellosis. (1964). Survival of Shigella in sea water. Nature, 203, American Journal of Tropical Medicine, 4, 263-300. 213-214. Hollister, A. C., Beck, M.D., Gittelsohn, A. M. and Hemphill, Newson, S. W. B. (1972) Microbiology of hospital toilets. E. C. (1955). Influence of water availability on Shigella Lancet, 2, 700-703. prevalence in children of farm labor families. American Olivieri, V. P., Kawata, K. and Kruse, C. W. (1978). Journal of Public Health, 45, 354-362. Relationship between indicator organisms and selected Hutchinson, R. I. (1956). Some observations on the method pathogenic bacteria in urban waterways. Progress in Water of spread of Sonne dysentery. Monthly Bulletin of the Technology, 10, 361-379. Ministry of Health and the Public Health Laboratory Petrick, M. (1954). Utilization of night soil, sewage and Service, 15, 110-118. sewage sludge in agriculture. Bulletin of the World Health Jamieson, W., Madri, P. and Claus, G. (1976). Survival of Organization, 10, 207-228. certain pathogenic microorganisms in sea water. Rahaman, M. M. (1979). A strategy for control of shigellosis Hydrohiologia, 50, 117-121. (dysentery) in Teknaf-a rural Bangladesh village. Kabler, P. (1959). ' Removal of pathogenic micro-organisms Progress in Water Technology, 11, 303-308. 296 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Rahaman, M. M., Khan, M. M., Aziz, K. M. S., Islam, M. S. Shigellaflexneri in an experimental oxidation pond. Israel and Kibriya, A. K. M. G. (1975). An outbreak of dysentery Journal of Medical Science, 12, 704-705. caused by Shigella dysenteriae Type 1 on a coral island in the Spicer, C. C. (1959). The survival of Shigella sonnei on cotton Bay of Bengal. Journal of Infectious Diseases, 132, 15-19. threads. Journal of Hygiene, 57, 210-215. Rajasekaran, P., Dutt, P. R. and Pisharoti, K. A. (1977). Stewart, W. H., McCabe, L. J., Hemphill, E. C. and DeCapito, Impact of water supply on the incidence of diarrhoea and T. (1955). Diarrheal disease control studies. IV. Relation- shigellosis among children in rural communities in ship of certain environmental factors to the prevalence of Madurai. Indian Journal of Medical Research,66, 189-199. Shigella infection. American Journal of Tropical Medicine Reeves, J. B. (1959). Sanitary aspects of composted sewage and Hygiene, 4, 718-724. sludge and sawdust. Sewage and Industrial Wastes, 31, Sultanov, G. V. and Solodovnikov, Y. P. (1977). Significance 557-564. of water factor in epidemiology of dysentery. Zhurnal Reller, L. B., Gangarosa, E. J. and Brachman, P. S. (1969). Mikrobiologii, Epidemiologii i Immutzobiologii, no.6 (June), Shigellosis in the United States, 1964-1968. Journal of' 99-101. Infectious Diseases, 120, 393-396. Talayeva, J. G. (1960). Survival of dysentery bacteria in water Richardson, N. J., Hayden-Smith, S., Brokkenheuser, V. and according to the results of a reaction with haptenes. Koornhof, H. J. (1968). Salmonellae and shigellae in Bantu Journal of Hygiene, Epidemiology, Microbiology and children consuming drinking water of improved quality. Immunology, 4, 314-320. South African Medical Journal, 42, 46-49. Taylor, B. C. and Nakamura. M. (1964). Survival of shigellae Rosenberg, M. L., Hazlet, K. K., Schaefer, J., Wells, J. G. and in food. Journal of Hygiene, 62, 303-311. Pruneda, R. C. (1976). Shigellosis from swimming. Journal Thomson, S. (1955). The numbers of pathogenic bacilli in of the American Medical Association, 236, 1849-1852. faeces in intestinal diseases. Journal of Hygiene, 53, Rudolfs, W., Falk, L. L. and Ragotzkie, R. A. (1951). 217-224. Contamination of vegetables grown in polluted soil. VI. van Zijl, W. J. (1966). Studies on diarrhoeal diseases in seven Application of results. Sewage and Industrial Wastes, 23, countries by the WHO Diarrhoeal Diseases Advisory 992-1000. Team. ,.,. of the World Healtlh Organization, 35, Schliessmann, D. J. (1959). Diarrhoeal disease and the 249-261. environment. Bulletin ofthe World Health Organization, 21, Wang, W. L. L., Dunlop, S. G. and De Boer, R. G. (1956). The 381-386. survival of Shigella in sewage. 1. An effect of sewage and Schliessmann, D. J., Atchley, F. O., Wilcomb, M. J. and faecal suspensions on Shigella flexneri. Applied Micro- Welch, S. F. (1958). Relation of Environmental Factors to biology, 4, 34-38. the Occurrence of Enteric Diseases in Areas of Eastern Watt, J. and Lindsay, D. R. (1948). Diarrheal disease control Kentucky. Public Health Monograph no. 54. Washington. studies. 1. Effect of fly control in a high morbidity area. DC: US Government Printing Office. Public Health Reports, 63, 1319-1334. Shaughnessy, H. J., Olsson, R. C., Bass, K., Friewer, F. and Watt, J., Hollister, A. C., Beck, M. D. and Hemphill, E. C. Levinson, S. 0. (1946). Experimental human bacillary (1953). Diarrheal diseases in Fresno County. California. dysentery. Journal of the American Medical Association, American Journal of'Public Health, 6, 728-741. 132, 362-368. Wiley, J. S. (1962). Pathogen survival in composting Shrewsbury, J. F. D. and Barson, G. J. (1957). On the municipal wastes. Journal oJ the Water Pollution C'ontrol absolute viability of certain pathogenic bacteria in a Federation, 34, 80-90. synthetic well water. Journal of Pathology and Bacterio- Wolff, H. L., van Zijl, W. J. and Roy, M. (1969). Houseflies. logy, 74, 215-220. the availability of water, and diarrhoeal diseases. Bulletin Slijkhuis, H., Betzer, N. and Kott, Y. (1976). Survival of oJ'the World Health Organization, 41, 952-959. 17 Vibrio cholerae and Cholera CHOLERA is probably the best known and most feared blood potassium levels (hypokalemia). If untreated, of the diarrheal diseases discussed in this book. some patients become rapidly dehydrated, pass into Although it is by no means the most important cause of shock, and die. Other patients experience much milder diarrhea in terms of total morbidity or mortality, it has diarrheal illness. Sixty percent or more of untreated caused, and in some parts of the world continues to classical chloera cases die, whereas El Tor is generally cause, dramatic outbreaks of acute disease accom- regarded as a milder infection with a lower fatality rate panied by considerable loss of life. In other areas cholera and a higher proportion of asymptomatic infections. is a part of the overall spectrum of endemic diarrhea, Recent evidence from Bangladesh suggests, however, and in these situations it often occurs with a regular that El Tor virulence may be increasing (Khan and seasonal periodicity. Cholera has a long history of Shahidullah 1980). It is not possible to distinguish scientific investigation, with some features of its classical from El Tor cholera clinically by reference to epidemiology being clarified in London (England) by any particular case. John Snow in the 1850s; the first full accounts of its The effects of cholera are due to the action of an clinical, bacteriological, and epidemiological aspects exotoxin, produced by the vibrios, which affects the were published in the 1880s as a result of work done in epithelial cells of the gastrointestinal mucosa and leads Egypt (Koch 1884). to massive secretion of water into the lumen of the gut. Diagnosis is by isolation of the bacteria either from stool samples early in the clinical phase of watery Description of Pathogens and Disease diarrhea or by rectal swab from convalescents. It is usual to attempt direct plating on selective media as Despite the long history of study referred to above, well as enrichment in alkaline peptone water before cholera is attracting renewed scientific interest, and plating. To confirm suspected isolates, agglutination some traditional understandings are being con- tests with anticholera 0-group 1 serum are carried out siderably modified. New information is being gained together with microscopic investigation for vibrio not only on the mechanisms of pathogenesis and morphology and biochemical charactrerization for immunity but also on certain aspects of epidemiology isolates failing to agglutinate. The El Tor biotype and transmission. The information summarized in this differs from the classical vibrio in very few of its chapter must therefore be considered as somewhat laboratory properties. provisional. Fatality rates can be reduced to under 1 percent in well-managed treatment centers. The treatment of Identification cholera primarily consists of preventing the patient from dying from loss of salts and water. The infection is Cholera is caused by bacterial infection of the small then self-limited, but its duration is shortened by intestine. The causative organism, Vibrio cholerae, appropriate antibiotic therapy. Rehydration may be exists in two biotypes-classical and El Tor. Both can by mouth in patients that are not vomiting and is by cause an acute intestinal disease characterized by giving clean water containing appropriate quantities of profuse rectal loss of water and electrolytes. The salt, potassium chloride, alkali such as sodium disease begins with sudden painless evacuation from bicarbonate, and glucose to promote the absorption of the bowel; as it progresses, (acidotic) vomiting may the electrolytes. Patients, particularly children, in a state start, together with muscle cramps due to lowered of shock or vomiting require appropriate intravenous 297 298 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA fluids rapidly. Normal hydration and acid-base the Middle East, and Europe. It also spread into East balance should be achieved for adults within 2 hours of and West Africa and the Pacific islands (figure 17-1). admission to a treatment center but is achieved more Where it is endemic, cholera develops a regular slowly for children weighing less than 20 kilograms. periodicity, and epidemic waves occur at one or two seasons of the year. These seasonal patterns are not the Occurrence same in various places, and there is no good explanation of how the cholera infection cycle The classical cholera vibrio is the historic cause of correlates with climatic conditions. cholera. From its homeland in Bengal and the Ganges Endemic cholera prior to 1960/1961 was confined to Valley, six classical cholera pandemics have spread. India, especially the Ganges system, Bangladesh, and The El Tor biotype, first identified in Sinai in 1905, has Sulawesi. Since then it has invaded many parts of the only comparatively recently been accepted as V. world and is, at the time of writing, considered to be cholerae. A focus of El Tor cholera was known to exist endemic in several areas of Africa and Asia. Many in the Indonesian island of Sulawesi in the 1930s. In national health authorities are very reluctant to admit 1961 this focus exploded and began to spread, thereby or report endemic cholera because of the possible effect initiating the seventh known pandemic of cholera. It on tourism and international travel (for instance, the spread eastward to the Philippines, northward to pilgrimage to Mecca). For this reason endemic El Tor Taiwan and Korea, and westward into India, where it cholera exists in a number of countries that officially replaced the classical biotype, and then on to Pakistan, deny it. The present pandemic has not yet spread to the Endemic focus of classical cholera [J Source area of cholera El Tor C:3 _4 >) First isolation of El Tor vibrios (1906) * Isoloted imparted cholera cases I Figure 7-1. The global spread of chole, 5Not shown /~~~~~~~~~~~~~~~~~~~~~~~~~Cp Verd Island (1974) \~~~~~~~~~~~~~~~~~~~~~~~~~Go 9749/7\ Figure 17-1. The global spread of cholera, 1961-75 VIBRIO CHOLERAE AND CHOLERA 299 Americas, although the risk of its introduction is very been recently recognized. These are known as atypical great. V. cholerae 0 1 (in this chaptcr atypical V. cholerae), and some of them have biochemical properties that differ from those of V. cholerae. Atypical V. cholerae have Injectious agents been isolated from water both in areas where endemic The family Vibrionaceae includes several human clinical cholera is known to occur and in areas-such enteric pathogens of the genus Vibrio, and the as Brazil, England, and the USA-where it does not taxonomic status of some of them remains uncertain occur. Atypical V. cholerae are thought not to be and controversial. They are all Gram-negative, motile enteric pathogens. rods (0.5 by 1.5-3 micrometers) usually having a The third group of V. cholerae strains are those curved or comma shape. They are nonsporulating, which do not agglutinate O1 antisera but which are noncapsulated, facultative anaerobes and possess a biochemically and genetically similar to V. cholerae 01. single polar flagellum (figure 17-2). The terminology These are now called non-O1 V. cholerae, but until very for the various pathogenic and closely related vibrios recently were called non-agglutinating vibrios (NAGs) used here is the one most commonly used at the present or non-cholera vibrios (NCVS). They are currently time, although it is not ideal and may be revised (WHO classified into seventy-two 0-group serotypes, but this Scientific Working Group 1980). typing scheme is tentative and provisional. Non-O1 V. Of greatest public health importance, and the main cholerae have been associated with many individual topic of this chapter, are organisms that have cases of cholera-like diarrhea and with some small traditionally been called Vibrio cholerae or cholera outbreaks. Some non-O1 V. cholerae produce acholera- vibrio, but which are now strictly known as V. cholerae like enterotoxin. 0-group 1 or 01. They will be called V. cholera in this Finally, there are other potentially pathogenic chapter. V. cholerae is the cause of epidemic cholera vibrios that are clearly not V. cholerae. V. para- and exists in two biotypes (classical and El Tor) and haemolyticus is a halophilic marine organism re- three serotypes (Inaba, Ogawa, and the much less sponsible for numerous outbreaks and attacks of food common Hikojima). V. cholerae produces an en- poisoning associated with seafood. It has a marine terotoxin that has been extensively studied and is rather than an enteric reservoir and so is not similar to Escherichia coli heat-labile enterotoxin (see considered in this chapter, although it is briefly chapter 13). Adherence to the intestinal mucosa is also discussed in chapter 7. The Group F (or Group EF6) an important virulence factor but is poorly vibrios (often mistakenly identified as Aeromonas) have understood. been isolated from the stools of patients with diarrhea A second group of V. cholerae, which agglutinate 0 1 in many countries, but it is uncertain whether they are antiserum but which do not produce enterotoxin, have toxin-producing or pathogenic. Other vibrio species Figure 17-2. V ibrio cholerae under scanning electronmicroscopy. The single polar flagellum of the organism is prominent. Scale bar = I micrometer. (Photo: J. Gallut, Institut Pasteur, Paris, France. Reproduced by courtesy of Bulletin of the World Health Organization) 300 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA occasionally isolated from man-V. alginol vticus, V. chlorhydria) may be infected by lower doses than metschnikovii, V. vulnificus, and L+ Vibrio are not others. More recent volunteer studies with El Tor believed to cause diarrhea. strains have shown that infective doses are lower when the organisms are administered in food than in small Reservoir volumes of water (WHO Scientific Working Group 1980). This could be due to more rapid gastric The primary source of infection that has been clearly emptying, neutralization of gastric acid by food, or documented is the human case or carrier. There is protection of vibrios that are adsorbed to, or speculation over the role of environmental isolates of embedded within. food particles. Nothing is known atypical V. cholerae and non-O1 V cholerae in cholera about the dose needed to cause acute diarrhea in 1 epidemiology and the possibility of an environmental percent of malnourished children, but it may be 102 or reservoir (see below, the section "Occurrence and even less. Survival in the Environment"). There is also specu- If it is assumed that the environmental reservoirs of lation about the role of animal reservoirs, especially for V. cholerae described below are epidemiologically non-O1 V cholerae or for V. cholerae were isolated unimportant, then cholera transmission must take interepidemic periods. Sanyal and others (1974) place by direct person-to-person contact or by the fecal examined 1,287 fecal samples from 195 domestic contamination of water or food. Waterborne and animals following an outbreak of cholera in Varanasi foodborne transmission have both been clearly (India) during 1972. The proportions of animals from demonstrated on specific occasions. Cholera has which V. cholerae or non-O1 V. cholerae were isolated classically been regarded as a waterborne disease, and were: dogs, 27 percent; chickens, 18 percent; cows and there are some experts who believe that this is its goats, each 11 percent. There were no isolations from dominant and normal mode of transmission. Others buffalo, donkeys, or horses. Out of a total of fifty-four maintain that this may be true in Bangladesh but not strains of V- cholerae isolated, eight were V cholerae 01 elsewhere, while a third opinion holds that cholera (El Tor, Ogawa). Neither this nor other studies have transmission among poor people in developing clearly shown that animal infections with V. cholerae or countries is primarily nonwaterborne. This subject has non-O1 V. cholerae play any role in the epidemiology of attracted recent debate (for instance Feachem 1976; human infection and disease. Levine and Nalin 1976) and is of considerable importance in designing control strategies. The topic has been comprehensively reviewed bv Feachem (1981. 1982). Cholera is transmitted by the fecal-oral route from person to person, and transmission is encouraged by Incubation period inadequate water supply and excreta disposal facilities and, ore gneralv, b povrty ad ovrcrowing. The incubation period is generally short and clinical and moreseneraly 'by mptovet andi overcro mi symptoms occur within 0.5 to 5 days (usually 1-3 days) Convalescent and asymptomatic individuals may o netn h atra nuainprosmyb excrete 10' 105 V. cholerae per gram of feces, whereas of ingesting the bacteria. Incubation periods may be an active case excretes 10 V10e per milliliter of rice- inversely related to the dose of organisms ingested. water stool (Dizon and others 1967; Greig 1914; Period of communicability Smith, Freter and Sweeney 1961). Infective doses are high in healthy adult males. Convalescents generally excrete V. cholerae in- Hornick and others (1971) required 108 classical V. termittently and only for short periods. Thus, 50 percent cholerae in water to produce diarrhea in 50 percent of of cholera cases will be found to excrete the pathogen adult volunteers (the median infective dose, or ID50), for up to 5 days, 30 percent continue to excrete for up to and 10" organisms to produce cholera-like diarrhea. 15 days, and 10 percent for up to 25 days. By 1 month With the prior administration of 2 grams of sodium usually less than 5 percent of cases are still excreting V. bicarbonate, the ID50 was lowered to 104 for diarrhea cholerae, and it is very uncommon to find carriage and 108 for cholera-like diarrhea. No diarrhea or persisting beyond 2 months. The truly chronic infection was produced by < 108 organisms without carrier such as Cholera Dolores from the Philippines NaHCO3 or by < 103 organisms with NaHCO3 (see (Azurin and others 1967)-is a very rare phenomenon. also Cash and others 1974). Asymptomatic infection is common, and the El Tor Gastric acidity is an important barrier to cholera biotype produces a higher infection to case ratio than infection, and those with lowered acidity (hypo- classical cholera. VIBRIO CHOLERAiE AND CHOLERA 301 Resistance plausible but usually unproven explanations of In edemc aras,it apeas tht rpeatd rin- waterbornc transmission. fcion endemichareas, itapears that grepeate reind-upo One of the most characteristic features of endemic immunity with increasing age (Gangarosa and Mosley instance, int Dacca (Banonglds)choeaued sesnlpttmForpa 1974). This may be one reason why the attack rates in dramatc,ic allyaduringlNovemb oer-anuary, whereask0 children in endemic areas are considerably higher than kilometersaway duing Calcuttr-aIndiary thereak was in adults, whereas in epidemic situations where cholera klmtrawy i acta(ni)tepa a has been recently introduced the reverse is often true. April-June. Recently these peaks have shifted and However, among those infected overt disease is more no ocudrigSpeb-Nvmrin ot common in adults than in children. areas. The reasons for these and other seasonal A previous attack of cholera diarrhea confers solid patterns of cholera remain entirely unexplained. immunity against reinfection with the same serotype of Non-0l V. cholerae has been isolated from stools of V. coleae or bou I ear.An nvetigtio in persons with diarrhea in many countries in Asia, VBahorain fhore tabot infyear.wAn investigationlin Africa, Europe, and, significantly, North and South bahrai-fe showd tat signifiantsy whogwere prinkofcipally America. Large epidemics have not been reported. In than infants who were breast-fed, although it was not thUS motifconocudrnghewmr clea whthe thi arse rom ontminted ilkand summer months, while in Bangladesh there appears to cotlear whthrtirs from conciv nreiitaminmatedna milkan be a peak in spring and summer before the annual bottesno from pothectiv inreint7n9aeraml cholera peak. Small foodborne outbreaks are common Cholera is a disease of the lower socioeconomic intransmission e onre,btltlskono groups. Fishermen and boatmen, living along polluted cutrasies.in adeieilg ndvlpn water courses, are specially at risk. So also are people Thenepidemilgsfcolr.ean i aywy with hypochlorhydria, either due to malnutrition or unc ertinademontovyocoersal Theman inmprance ofy other natural causes, or following gastric surgery (Sack ucranadcnrvril h motneo and others 1972). Although the El Tor biotype may be waterborne transmission, the maintenance of cholera less virulent than the classical, causing more mild cases during interepidemic months of the year, the of cholera, the host is probably equally susceptible to explanation of seasonality, the failure of tubewells in colonization by either. Bangladesh to reduce incidence, and the role of a possible aquatic reservoir for V cholerae are all topics of current debate. Space does not permit a full Epidemiology ~~~~~~~~review of these issues here. For a conventional account Epidemiology ~~~~~~~of cholera epidemiology, the reader should consult Studies on V. cholerae El Tor infection, in both Gangarosa and Mosley (1974); Feachem (1981, 1982) epidemic and endemic situations, have repeatedly provides a review of the more recent literature and emphasized that the severe eases that reach the debates. attention of treatment centers and physicians are the tip of an iceberg of widespread asymptomatic and mild clinical infection in the community. Estimates of a case to infection ratio of 1: 30, or less, are commonly quoted. Control Measures The asymptomatic infections are generally short lived but can be of crucial epidemiological importance in The most cost-effective control measures to deal transmitting and geographically spreading cholera. with either endemic or epidemic cholera remain Attempts to reconstruct the modes of transmission and uncertain. Understanding of control will increase as spread of cholera that concentrate on known clinical more information is gathered on the epidemiological cases are unlikely to be successful. To understand issues discussed above. Cholera control among people cholera epidemiology, it is necessary to take full who are poor has so far proved to be extremely difficult. account of the transient carrier, and to document the The course of a cholera epidemic is often dramatic and occurrence of transient carriage it may be necessary to short-lived, and by the time control measures are undertake multiple fecal examinations and use applied the epidemic may be waning naturally. This serological techniques to determine whether an can give a false impression of the efficacy of the control asymptomatic individual has been infected. These measures and lead to unjustified claims--as was the difficulties are one reason why so many investigations ease when John Snow removed the handle from the of cholera outbreaks are inconclusive or fall back on Broad Street pump in London (England) in 1855. 302 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Individual have been made for the efficacy of various en- vironmental control methods, but few of these have Prophylactic antibiotics have been used to control been justified, and most programs have been some cholera outbreaks and to limit their spread. unsuccessful. Indeed, the experience with environmen- There is no evidence that this practice is effective, and tal control among the rural and urban poor has been so there is mounting concern over the rising prevalence of bad that some experts feel that the priority allocation antibiotic-resistant strains of V. cholerae in some of resources should be toward the establishment of countrles. Large amounts of tetracycllne ( 1,788 kilountries. in e firta6mounths)of tetracyclined the i networks of treatment centers for providing simple but kilograms in the first 6 months) were used therapeuti- highly effective rehydration therapy to reduce mort- cally and prophylactically following the outbreak of higy (efectiv e rrp e e cholera in Tanzania in October 1977. Initially, all atY (Greogh 17). chola in T a iThe impact of water supply and sanitation schemes strains of V. cholerae tested were fully sensitive to .o.n.i.i bu afte 6 moth 76pretofioae on endemic or epidemic cholera in poor communities iS tetracycline, but after 6 months 76 percent of isolates uncertain. Six studies in Bangladesh showed no impact were resistant (Mhalu, Mmari and ljumba 1979). (Briscoe 1978; Feachem 1982), whereas a study in the Subsequent work showed that this antibiotic resistance P was mediated by transferable plasmids that confer aPhilippines showed a very considerable impact (Azurin multiple antibiotic resistance (Towner and others and Alvero 1974) Thes nterpretatlon ofthese findgs 1980;~ ~ ~ ~ ~ ~ ~~, Tonr1ero n 'rd 99.Mlil S controversial and has been recently reviewed in 1980; Towner, Pearson and O'Grady 1979). Multiple dealbFece(18) antibiotic resistance has also been reported from 5-36 percent of V. cholerae isolates from Bangladesh In some outbreaks-for instance, in Tanzania from (Threlfall, Rowe and Huq 1980). 1977 to 1980-the geographical spread of cholera was (Thefl,owclpeeand t 8 ) . . due to the movement of infected individuals and gave dimmupoinolog.Kicalpeventio vaccines isaffd at psresn rise to the characteristic pattern of spread along major disappointing. Killled vaccines do afford a measure of ala n odrue. nsc icmtne h protection but are usually less than 70 percent effective, railway and road routes. In such circumstances the protectionmbuntyar usually less t 7 poerenot elcte limitation of movement of people in or out of areas and such immunity as IS produced does not last at reasonable levels for more than about 4 months. A known to be affected may reduce the risk of spreading the disease. Travel restrictions are difficult to enforce, study In Bangladesh Sowed ass vaccinaion3wa however, and may seriously disrupt the movement of Current neffected( tfmm er Mosceyi173) foodstuffs. If travel restrictions are combined with Currogentesesarch isvirlented factor fut cractdering issuing prophylactic tetracycline to those who must pathogenesis and virulence factors and at developing tae,a a oei azna h rbeso and testing a variety of alternate vaccines based on travel, as was done in Tanzania, the problems of live mutant strains or nonviable antigens such as the B increased antibiotic resistance described above may subunit of the cholera enterotoxin. occur. Rigorous personal cleanliness and care in eating and Cvjetanovid (1979) and Cvjetanovi', Grab and drinking habits are probably the surest ways by which Uemura (1978) used a mathematical model to compute an individual can reduce the risk of cholera in an the relative economic merits of sanitation, chemopro- endemic or epidemic situation. phylaxis, and immunization as methods of cholera control. Unfortunately, the cost of sanitation was set far too low (US$0.15 per capita at 1971 prices), and the Environmental effectiveness of sanitation was overestimated. Not surprisingly, this analysis showed sanitation to be There is no doubt that some combination of highly cost-beneficial (with benefits taken only as the improved water supplies, excreta disposal facilities, medical treatment costs saved), whereas immunization better housing, and all the various improvements in was shown to have costs far exceeding benefits because daily life that come with increased wealth and the currently available vaccine would have to have education have been responsible for the elimination of been given annually to have had any major impact on cholera from the developed countries and from many disease. Nonetheless, the analysis highlighted the middle-class communities in developing countries. benefits of sanitation as a measure having potential Cholera was and remains a disease of poverty and the effects on a range of enteric and other diseases, as living conditions that are associated with poverty. compared with vaccination, which, even if a more Countries that experience the problem of endemic or protective vaccine were available, is difficult to epidemic cholera today are faced with the question of administer to most children, probably requires how to control the disease among poor communities in repeated readministration, and only protects against a the short-term while poverty persists. Many claims single pathogen. VIBRIO CHOLERAE AND CHOLERA 303 Carrier surveillance and international regulations cholerae isolations from rivers, tanks, ponds, wells, and household water jars in or near communities where Since the chronic carrier is extremely rare, cholera cases or infections are known to be occurring. surveillance to identify carriers is notof significance i Some of these reports are reviewed in a separate the control of this disease. This is in m arked contrast publication s(Feachems1981) eSecond theresarerte with typhoid. The principal types of cholera carriage are publication (Feachem 1981). Second, there are the more recent findings of V. cholerae, especially but not icubatory, convalescent, and contact. exclusively atypical 01 and non-Ot strains, in water Up to December 31, 1970 International Sanitary an watwae atstsdsatfo n nw ua Reguatios wre i fore. hey tipuate a 5day and wastewater at sites distant from any known human Regulations were in force. They stipulated a 5-day V cholerae infection. These findings are reviewed below quarantine speriod.for relesfom areasahr in the section on possible aquatic reservoirs. cholera was established. The regulations were aban- The reason that the view expressed by Felsenfeld was doned when it was recognized that they were not so strongly held for nearly 100 years is, first, that preventing the spread of the current pandemic. Among researchers had failed to find V cholerae in the aquatic the reasons for this failure were the concealment or environment except in close association with human denial of the existence of the disease in a country, neto det obnto fntloig okn together with the unknown importation of cases across infection (due to a combiation of not lookmg, loohng unpatrolled borders. Current surveillance at national in the wrong manner and looking in the wrong place), udnpaterolledtbonaldlevers Current svenianfcati in and, second, that survival experiments conducted in the and international levels has been ineffective laboratory had shown V cholerae to be an organism preventing the spread of cholera into receptive with only limited survival ability in certain aquatic countries-those with poor sanitation, hygiene, and environments. health services. Nonetheless, surveillance to identify Some of the considerable accumulation of data on V. clinical cases (and, hence, the geographical advance of cholerae survival in water is summarized in tables 17-1 the disease) provides valuable epidemiologcal minfor- to 17-5. In clean water (for instance, dechlorinated tap mation and allowsthe organizationoftreatmentinthe water), survival times are up to 1 month at 4°C and absence of effective control measures. 2-14 days at 20-30°C. In raw well water, survival times are over a month at 4°C and generally between 1 and 20 Occurrence and Survival in the days at 20-30°C, although reports from India and Environment Tanzania suggest survival of the El Tor biotype in raw well water of up to 55 days. A single report of V. The study of V cho*erae, atypical V cholerae, and cholerae survival in refrigerated raw surface water gives non-01 V cholerae in the environment is attracting a survival time of 48 days, while survival at 20-30'C is increasing attention at the present time. The con- generally 1-6 days, with occasional reportings of ventional view that V. cholerae is an organism only longer survival and one exceptional report from found in the environment in close association with Tanzania of 48 days. As would be expected, survival in human cases or infections, and only surviving for a few seawater is prolonged, with durations of 2 months at days at most, is now being revised. 4XC and 6-60 days at 20-30'C. Finally, a single report from the USSR (table 17-4) and epidemiological evidence from Portugal (Blake and others 1977) suggest the ability of V. cholerae to survive for The relationship between V. cholerae and water has prolonged periods in certain mineral waters. been the focus of many investigations and is crucial to It is clear from the tables that survival can be greatly an understanding of the epidemiology of cholera. The prolonged in nutrient-rich waters and seawaters that traditional view of this subject-as stated by Felsenfeld have been boiled or autoclaved prior to contamination (1974): with V cholerae, thus eliminating competing micro- organisms and possibly also making the chemical some authors claimed that cholera vibrios may comp osition of the water more favorable for V survive in water, particularly, seawater, for as long as chosition o u the nature avorable or V 2 months. This is, however, scarcely possible under cholerae survival. Although the nature and extent of V. natural conditions ' reinfection of te w r d cholerae inhibition by a mixed microflora in a natural natural conditions if reinfection of the water does surface water are not known, one study showed a failure of E. coli, Pseudomonas spp., and Aerobacter -is now known to be incorrect. spp. to suppress V. cholerae El Tor survival in artificial Data on the occurrence of V. cholerae in water are of sterile well water (Pandit and others 1967). Sunlight two types. First, there are the numerous reports of V. considerably curtails V. cholerae survival. 304 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-1. Survival of Vibrio cholerae in surface waters Biotype and initial concentration Source per milliliter Type of sample Temperature Survivala Cheng (1963) El Tor River water 21-31°C 3 days 1.5 x 105 Drain water 2 days Pond water 6 hours (all taken in or near Taipei) Gohar and Classical Nile water Room temp. Makkawi from feces (Egypt) 5 days (1948) from culture 10 days Khan and Classical Jumna and Ganges Room temp. Agarwal (clinical isolate) river waters (Allahabad) (1929) Raw 8 days Filtered 18 days Boiled 29 days Boiled & filtered 14 days Non-Of Raw 20 days (water isolate) Filtered 20 days Boiled 18 days Boiled & filtered 20 days Konchady Classical Calcutta 250C and others 104 River Hooghly 6 days (1969) Canal water 6 days Pond water 6 days Lahiri, Das Classical Spring water Room temp. and Malik (1939) (Inaba) Raw (Calcutta) 1 hour 106 Autoclaved 18 hours River Hooghly (Calcutta) Raw 18 hours Autoclaved 3 days Filtered 2 days Autoclaved & fiitered 2 days Tank waters (Calcutta) Raw 2 3 days Autoclaved 3-12 days Filtered 7 days Autoclaved & filtered 15-18 days Lema, Ogwa El Tor Swamp water in Dar 4°C 48 days and Mhalu 105 es Salaam 30°C 48 days (1979) 32°C in 3 days sunlight Mukerjee, Rudra Classical River Hooghly Room temp. and Roy (1961) 2 x 106 (Calcutta) (Calcutta) Raw 1-6 days Autoclaved 4-22 days Filtered 3-12 days VIBRIO CHOLERAE AND CHOLERA 305 Table 17-1 (continued) Biotype and initial concentration Source per milliliter Type of sample Temperature SurvivaP Tank water (Calcutta) Raw 1-6 days Autoclaved 4-23 days Filtered 3-7 days El Tor River Hooghly (clinical isolate) (Calcutta) 2 x 106 Raw 2 days Autoclaved 11 days Tank water (Calcutta) Raw 2 days Autoclaved 13 days El Tor River Hooghly (Calcutta) (water isolate) Raw 2 days 2 x 106 Autoclaved 11 days Tank water (Calcutta) Raw 2 days Autoclaved 16 days Non-OI River Hooghly (Calcutta) (clinical isolate) Raw 2 days 2 x 106 Autoclaved 9 days Tank water (Calcutta) Raw 2 days Autoclaved 12 days Non-O1 (water isolate) River Hooghly (Calcutta) 2 x 106 Raw 2 days Autoclaved 11 days Tank water (Calcutta) Raw 2 days Autoclaved 13 days Neogy (t965) Classical Pond water Room temp. 1-2 days El Tor (India) 8 days Read and Classical Autoclaved tank Room temp. >30 days others (1939) waters (Calcutta) (Calcutta) Note: Older literature is reviewed by Pollitzer (1959). a. Times given, for instance, as 22 days are durations at which viable organisms could no longer be detected. Times given as > 30 days indicate that organisms were still viable at that time but that sampling was discontinued. Some experiments have included direct comparisons for longer than classical V. cholerae 01 (Khan and of the survival of classical and El Tor biotypes, and Agarwal 1929); and one study showed no difference in occasionally also non-O1 strains (tables 17-1, 17-2 and survival between classical O1,ElTorOl and non-O1 V. 17-4). Two studies showed markedly longer survival of cholerae (Mukerjee, Rudra and Roy 1961). It would El Tor than classical V. cholerae (Felsenfeld 1965; appear from this literature review that the widely held Neogy 1965); one study showed similar survival belief that El Tor V. cholerae survives for considerably between the two biotypes (Sayamov and Zaidenov longer periods in water than the classical biotype is not 1978); one study showed non-O1 V. cholerae surviving firmly based. This is especially true in view of the major 306 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-2. Survival of V. cholerae in well water Biotype and initial concentration Source per milliliter Type of sample Temperature Survivala Cheng El Tor Well water 21-31°C I day (1963) 1.5 x 105 (village near Taipei) Felsenfeld Classical Shallow well water ? 8 days (1965) El Tor ? 19 days Khan and Classical Well water Room temp. Agarwal (clinical (Allahabad) (Allahabad) (1929) isolate) Raw I day Filtered 6 days Boiled 9 days Boiled & filtered 8 days Non-OI Raw 12 days (water Filtered 6 days isolate) Boiled 18 days Boiled & filtered 26 days Konchady Classical Well water 25°C 6 days and others 104 (Calcutta slum) (1969) Lema, Ogwa El Tor Well water 4°C 55 days and Mhalu 105 (Tanzania) 30°C 55 days (1979) 320C in I day sunlight McFeters ? Sterile well water 9.5-12.5°C >2 days and others 105 (tso = 1.3 days)b (1974) Pandit and El Tor Well water 21°C 18 days others (Ogawa) (Punjab) 37°C 4 days (1967) 103 Well water 2 VC 51 days (Uttar Pradesh) 250C Fourfold growth after 1 day Survival for > 7 days 37°C 4 days Experiments with well water 25°C 10-12 days simulating actual removal and replacement of water in well following single contamination with 103 V cholerae per milliliter Pesigan, El Tor Deep well water Plantilla 106 (Manila) and Rolda Raw 5-100C 18 days (1967) 30-32°C 13 days Sunlight 4 days Autoclaved 5-10°C 42 days 30-32°C 17 days Sunlight 8 days VIBRIO CHOLERAE AND CHOLERA 307 Table 17-2 (continued) Biotype and initial concentration Source per milliliter Type of sample Temperature Survivala Raw well water stored 30-32°C 32 days in clay jar ambient, but jar storage may have cooled water Shrewsbury Classical Sterile, synthetic 5°C 1 day and well water of same 21°C I day Barson composition (pH = 5.6) 25CC I day (1957) as Hagar's Well (Mecca, Saudi Arabia) during the cholera epidemic of 1883 Same water with: pH 7 5°C 3 days 21'C 3 days pH 8 5°C 3 days 21°C 77 days pH 9 5°C 3 days 21°C 3 days Note: Older literature is reviewed by Pollitzer (1959). a. Times given, for instance, as, 18 days are durations at which viable organisms could no longer be detected. Times given as > 7 days indicate that organisms were still viable at that time but that sampling was discontinued. b. t55 Time for 90 percent reduction. probable strain-by-strain differences within each fauna, and plant surfaces; therefore, laboratory data biotype and the differences between laboratory must be interpreted with extreme caution. cultures, fresh clinical isolates, and water isolates. On the basis of the literature reviewed here it remains unproven than El Tor is a more persistent organism in water than the classical biotype, and the true Fxcept for the atypical V cholerae and non-O1 V. interbiotypic and intrabiotypic variabilities in survival cholerae which may maintain an environmental remain to be documented. It follows that explanations reservoir, the primary source of V. cholerae in the of the differences in epidemiology between El Tor and environment is the feces of man. Persons infected by V. classical cholera-for instance, the greater "endemic cholerae, though not sick, may excrete 102-105 per tendency" of the former-cannot, at the present time, gram of feces, while those with active and severe disease make use of putative differences in environmental may excrete 106-109 per milliliter of rice-water stool persistence between the two biotypes. (Dizon and others 1967; Greig 1914; Smith, Freter and Laboratory experiments on V. cholerae survival in Sweeney 1961). Unlike most other enteric bacterial water may accurately reflect conditions in manmade infections, the prevalence of excretion of V. cholerae by containers of clean water (such as reservoirs, cisterns, the general healthy population is very low-typically jars, and glasses), but they cannot replicate conditions well under 1 percent, even in endemic areas. in natural water bodies such as rivers, ponds, or even In areas of endemic cholera, or during a cholera open wells. In these latter waters there may be outbreak, it is to be expected that V. cholerae will occur abundant flora and fauna, and many varied surfaces, in the night soil produced by the affected communities. not reproduced or simulated in the laboratory Forbes, Lockhart and Bowman (1967) and van de experiments. There is increasing evidence (reviewed Linde and Forbes (1965) reported numerous isolations below) that V. cholerae in natural waters are frequently of V. cholerae from night soil in Hong Kong, both when in close association with bottom sediments, chitinous cholera cases were and were not occurring in the city. 308 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-3 Survival of V. cholerae in tap water Biotype and Cilt/rine reSidL1l initial concentration milligrams Source per mnilliliter Type of samnple Temperatu7e per liter Surcirala Cheng El Tor Taipei tap 21-31CC 0.5 2 hours (1963) 1.5 x 105 water Konchady Classical Tap water 25°C 0 6 days and others 104 from deep (1969) tubewell (Calcutta) Lahiri, Das Classical Calcutta tap Room temp. ? and Malik (Inaba) water (Calcutta) (1939) 106 Raw 18 hours Autoclaved 24 hours Filtered 2 days Filtered & autoclaved 12 days Lema, Ogwa El Tor Dar es Salaam 4°C Chlorinated 34 days and Mhalu 105 tap water 30°C at treatment 14 days (1979) 32°C in works but 3 days sunlight probably no residual chlorine remaining at tap Mukerjee, Classical Calcutta tap Room temp. ? Rudra and 2 x 10' water (Calcutta) Roy Raw 2-8 days (1961) Autoclaved 4-18 days Filtered 2-6 days Pandit and El Tor Delhi tap 21°C De-chlorinated 12 days others (1967) (Ogawa) water 37°C 1 day to3 Pesigan, El Tor Manilla tap Plantilla lob water and Rolda Raw 5-1 0C 0.6 1 hour 1967) Raw 30-32°C 0.6 1 hour Raw Sunlight 0.6 1 hour Autoclaved 5- l0C 0 10 days Autoclaved 30-32°C 0 1.6 days Autoclaved Sunlight 0 12 hours Note: Older literature is reviewed by Pollitzer (1959). a. Times given are durations at which viable organisms could no longer be detected. During a 10-month sampling period, 46 percent (200 of total of 72.494 night soil samples yielded only 56 433) of bucket latrines in the slums of eastern Calcutta isolations of V. cholerae. all of which occurred at times (India) were positive for V. cltolerae on one or more when cholera cases were being reported (Bart, Khan occasions (Sinha and others 1967). V. cholerae and Mosley 1970). isolations from latrines were obtained during months Some reported data on V. cholerae survival in feces when no cholera cases were reported. In contrast, are summarized in table 17-6. Clearly survival is during 1968 in Dacca and Chittagong (Bangladesh) a inversely related to temperature. Cheng (1963) and l'IBRIO CHOLERAE AND CHOLERA 309 Table 17-4. Survival of V. cholerae in mineral water Biotype and initial concenitration Source per milliliter Type of samnple Temperature Survivala Sayamov and Classical Spring water from spa Zaidenov (Matsesta, USSR) (1978) 9 x 105 Raw 20-24°C 22 days 1.5 x 103 Diluted 15-65 days 9.5 x 10W Boiled > 1429 days 1.6 x 10' Diluted 370C >289 days El Tor 1.2 x 106 Raw 20-24°C 22 days t03 Diluted 18-39 days 9 x lo, Boiled >1429 days 1.6 x 10' Diluted 37°C >413 days Note: Further evidence of prolonged survival of V cholerae in mineral water is provided by the investigation of the cholera outbreak in Portugal in 1974 (Blake and others 1977). a. Times given, for instance, as 22 days are durations at which viable organisms could no longer be detected. Times given as > 289 days indicate that organisms were still viable at that time but that sampling was discontinued. Shoda, Koreyeda and Otomo (1934) found that Daniel and Lloyd 1980b; Zaidenov and others 1976) survival was longer in liquid stools than in soft or solid suggested that some sewages provide a permanent stools. In summary, at ambient temperatures in tropical culture medium for some strains of classical, El Tor, and subtropical countries, V. cholerae is unlikely to and non-O1 V. cholerae. The other studies found that survive beyond 5 days in feces. survival times were 1-24 days in sewage at 20-30°C. Survival times are shorter at warmer temperatures and In sewage longer in sterilized sewage than in raw sewage. Direct comparisons of different biotypes and There are very few reports of V. cholerae in sewage. serotypes showed no differences in survival among This is primarily because, in most developing classicalO1, El Tor 01,and non-Ol strains (Mukerjee, countries, the section of the population that ex- Rudra and Roy 1961). Altukhov and others (1975) periences the highest attack rates of cholera produces found an El Tor, Ogawa strain better able to multiply no sewage because their houses do not have flush in bath house sewage at 37°C than a classical, Ogawa toilets. Instead, they produce night soil (where V. strain, although even the classical strain had not fallen cholerae has been found) or they defecate beside or below its initial concentration after 10 days. Daniel and into open water bodies (where V. cholerae has also Lloyd (1980b) found a sewage-derived non-01 strain been found). better able to multiply in sewage than a laboratory Kott and Betzer (1972) reported estimates that reference strain of El Tor 01, although even the El Tor Jerusalem sewage contained between 10 and 104 V. strain showed no reduction in concentration between 6 cholerae per 100 milliliters during the 1970 cholera hours and 48 hours at 22-25°C. As with water, epidemic in Israel. Daniel and Lloyd (1980a) reported therefore, there is little evidence at present to suggest geometric mean concentrations of 2,600 and 160 non- that the El Tor biotype is necessarily better able to 01 V. cholerae per 100 milliliters of very strong sewage survive in sewage than the classical biotype. (suspended solids 17,000 and 7,400 milligrams per liter, respectively) in two refugee camps near Dacca (Bangladesh). Isaacson and others (1974) reported the Summary of survival in water and wastewater use of Moore pads to detect V. cholerae in sewage at mines in the Transvaal (South Africa) during 1973-74, In some survival studies the initial concentration of when the spread of cholera from Malawi, organisms present was reported, and it is therefore Mozambique, and Angola was feared. V. cholerae (El possible to estimate a death rate expressed as a tgo Tor, Inaba) was isolated from the sewage prior to and value-the time in hours for a 90 percent or 1 log unit during cholera outbreaks at the mines and acted as an decline in concentration. In only a few studies were effective early warning system for the outbreaks. death curves plotted from which accurate tgo values Survival of V. cholerae in sewage is summarized in might be taken. For other studies the tgo value can only table 17-7. Three studies (Altukhov and others 1975; be estimated from the initial concentration and the 310 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-5. Survival of V. cholerae in seawater Biotype and initial concentration Source per milliliter Type of sample Temperature Suirvirala Cheng (1963) El Tor Coastal water 21-31°C 6 days 1.5 x 105 near a fresh- water source Jamieson, El Tor Sterilized seawater Madri and 1.5 x 107 with adjusted salinity (percent) Claus 0.5 4°C 5 days (1976) 25°C 3 days 37°C 2 days 2.0 4°C 4 days 25°C 3 days 37°C 1 day 3.5 4°C 4 days 250C 1 day 37°C 1 day Lema, Ogwa El Tor Seawater 4°C > 58 days and Mhalu 105 (Dar es Salaam) 30°C >58 days (1979) 320C in 5 days sunlight Pesigan, El Tor Seawater (Manilla) 5-10°C 58-60 days Plantilla 106 30 32°C 10-13 days and Rolda Sunlight 10- 1 days (1967) Various Classical Sterilized seawater ? 81 days studies (Marseilles) between Seawater Summer 7-17 days 1885 and (Copenhagen) Winter 47 days 1920 Seawater (New York) reviewed Raw ? 7-47 days by Pollitzer Sterilized ? >285 days (t959j Seawater (Japan) Raw 4°C 9-27 days Raw Room temp. 7-41 days Raw 37°C 3-12 days Sterilized 4°C 53-230 days Sterilized Room temp. 152 209 days Sterilized 37°C 30-83 days Yasukawa Classical Artificial seawater (1933) 3 x 104 Top of tank 18°C 23 days Bottom of tank 18°C 30 days 3 x 105 In sunlight 19-40°C 2 hours a. Times given, for instance, as 6 days are durations at which viable organisms could no longer be detected. Times given as > 58 days indicate that organisms were still viable at that time but that sampling was discontinued. VIBRIO CHOLERAE AND CHOLERA 311 Table 17-6. Survival of V. cholerae in feces Biotype and initial concentration Source per milliliter Type of sample Temperature Survivala Abel and Classical Naturally infected 13 16CC 10 days Claussen cholera stools for over (1895); cited half the by Pollitzer samples with (1959) a maximum of 29 days Cheng El Tor Naturally infected 29-31°C 1-4 days (1963) stools Artificially 29-31°C 2 4 days infected stools Gildemeister Classical Naturally infected 12-21°C 10 days for and stools half the Baerthlein samples; (1915); cited with a by Pollitzer maximum of (1959) 51 days Greig Classical Naturally infected 22°C Min. 1-3 days (1914) 1.5 x 108- ricewater stools Max. 10-17 days 2 x 109 Av. 3-8 days 29°C Min. 1 day Max. 2 13 days Av. 1-7 days Shoda, Classical Naturally and 4°C 1-5 days Koreyeda and artificially infected Room temp. 0.5-2 days Otomo (1934) stools (Japan) 37°C 6 hours a. Times given are durations at which viable organisms could no longer be detected. Max. = maximum, Min. = minimum, Av. = average. overall survival time, without knowing the shape of the uncertain whether the interbiotypic variability of intervening death curve or whether the number of survival is greater than the intrabiotypic variability. organisms fell below detectable levels considerably These tgo values may be compared with typical tgo prior to the stated survival time. values for coliforms of 20 to 115 hours (median 60 Bearing in mind these limitations, tgo values have hours) in surface waters and with 0.6 to 8 hours (mean 2 been derived where possible. The few studies that hours) in seawater (chapter 13). For shigellac, in showed prolonged maintenance of concentrations surface waters at temperatures of over 20°C, tgo values equal to or greater than initial values have been generally fall well below 60 hours (chapter 16). Thus, excluded and are discussed separately in the next even discounting the prolonged survival findings section. Derived tgo values are presented in table 17-8. reviewed below, the tgo values for V. cholerae are not The mean figures in table 17-8 suggest maximum greatly lower than those reported for coliforms and survival in well water and seawater. The mean figures may be similar to those reported for other bacterial for the El Tor biotype are greater than for the classical enteric pathogens. In a direct comparison of various biotype, but this comparison is invalid since each bacteria in sterile well water, McFeters and others experiment used very different techniques and a wide (1974) found the following t5o values: shigellae, 22-27 variety of strains of various origins. It remains hours; coliforms, 17 hours; salmonellae, 2-19 hours; 312 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-7. Survival of V. cholerae in sewage Biotype and initial concentration Source per milliliter Type of sample Temperature Suruival6 Altukhov Classical Sewage of a bath 37°C > 10 days and others (Ogawa) house (USSR; (1975)P lo0 BOD = 320 milli- grams per liter) El Tor (Ogawa) > 10 days t0o Daniel and El Tor Strong sewage at 22-25°C Concentration Lloyd (1980b) 2 x 10' refugee camp fell by 1 log (Bangladesh) in 6 hours and remained steady for further 42 hours Non-Ol Concentration (sewage isolate) rose to 4 x 106 2 x 105 in 6 hours and remained steady for a further 42 hours Flu (1921) Classical Sewage in Ambient 2 days septic tanks temperature (Batavia) Gerichter El Tor Sewage 20-28°C Two phase and others (Jerusalem) decline: t90 = (1975) 1.8 days for first 5 logs and tg, = 8 days subsequently. V cliolerae not detected after 24 daysc Howard and El Tor Raw sludge Lloyd (1979) 106 1 percent solids 25'C t90 = 2 days max survival 14 days 5 percent solids t,, = 3 days max survival - > 14 days Kott and El Tor Diluted Room temp. I day Betzer 10 sewage (Haifa: (Israel) (1972) BOD = 200 milli- grams per liter) Mukerjee. Classical Sewage (Calcutta) Room temp. Rudra and 2 x 106 Raw (Calcutta) 1-5 days Roy 11961) Autoclaved 4-24 days Filtered 2-7 days El Tor Raw 2 days (clinical isolate) Autoclaved 9 days 2 x l0' VIBRIO CHOLERAE AND CHOLERA 313 Table 17-7 (continued) Biotype and initial concentration Source per milliliter Type of sample Temperature Survivala El Tor Raw 2 days (water isolate) Autoclaved 10 days 2 x 106 Non-Ol Raw 2 days (clinical isolate) Autoclaved 8 days 2 x 106 Non-Ol Raw 2 days (water isolate) Autoclaved 8 days 2 x 10' Ohwada Classical Sewage 4°C 12 days (1924); cited Room temp. by Pollitzer (Japan) 4 days (1959) 37°C 1 day Zaidenov El tor (Ogawa) and others 104 Locomotive depot 18-24°C >39 days (1976) wastewater Domestic sewage 3 days Dairy effluent 14 days 10 Oil and water > 14 months Diesel fuel and water > 14 months Note: Older literature is reviewed by Pollitzer (1959). a. Times given, for instance, as 6 days are durations at which viable organisms could not be detected. Times given as > 10 days indicate that organisms were still viable at that time but that sampling was discontinued. b. These experiments were discontinued after 10 days, at which time the concentration of classical V cholerae was 5 x 102 while that of El Tor had risen to over 10' per milliliter. Data from the bath house suggested that V cholerae (El Tor, Ogawa I survived for at least 13 months in the sewerage system (temperature 20-25°C) despite repeated disinfection and no known external recontamination. c. tgo: time for 90 percent reduction. and V cholerae, 7 hours. Pandit and others (1967)found of 9 x 105 per milliliter remained steady for 4 years for that V.cholerae (El Tor) survived2to 5timeslongerthan both biotypes. Other results from these experiments E. coli, Pseudomonas spp., and Aerobacter spp. when are given in table 17-4. they were added to artificial well water and stored at More remarkable are reports of prolonged survival 250C. in raw sewage. Altukhov and others (1975) studied a bath house in the USSR. V. cholerae (El Tor, Ogawa) was isolated from 49 percent of samples of wastewater from the bath house over a 13-month period. Repeated Pollitzer (1959) cited several early studies that attempts to disinfect the wastewater system had no reported prolonged survival of V. cholerae in various effect on V. cholerae isolation. There was no known waters. Examples are up to a year in sterilized spring or cholera infection in the community. V. cholerae was not well water, up to a year in sterilized river water, and isolated from the incoming water supply, nor from large over 9 months in sterilized seawater. numbers of samples of human feces, water, fish, and Sayamov and Zaidenov (1978)'studied the survival frogs that were examined. Serological surveillance also of classical and El Tor V. cholerae in mineral waters failed to detect evidence of V. cholerae infection. V. from a spa at Matsesta (USSR). In raw mineral water, cholerae was isolated from river water contaminated by survival did not exceed 22 days for either biotype. In the discharge from the bath house. In laboratory boiled mineral water at 20-24°C, initial concentrations experiments, wastewater from the bath house 314 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA (BOD5 = 320 milligrams per liter, pH = 7.6) was was 7.1 to 9.3. Over a 17-month period 1,454 samples of inoculated with an El Tor (Ogawa) strain previously sewage from various points in the system were isolated from the bath house and with a reference strain examined, and 17 percent were positive for V. cholerae of classical V. cholerae (Ogawa), and stored at 37C. (El Tor, Ogawa). The wastewater from the locomotive The concentration of El Tor organisms was 105 per depot was far more frequently infected (18-42 percent) milliliter at the start, rose to over 108 per milliliter after than the domestic sewage (5 percent). The oil traps and 3 days, and maintained this concentration up until 10 flotation chamber were most frequently infected. The days when sampling was discontinued. The con- V. cholerae strain isolated was always the same and was centration of classical organisms was 103 per milliliter nontoxigenic. Fecal examination of 2,708 people in the at the start, rose to 105 after 3 days, and fell back to depot and the housing estate revealed only three 5 x 102 after 10 days. The investigation failed to infections with non-O1 V. cholerae. When one oil trap discover how the bath house sewerage system became was isolated from the system, V. cholerae were shown to infected, but it was clear that, once infection had taken survive in it for 36 days (the temperature in this oil trap place, V. cholerae (El Tor, Ogawa) maintained itself in fell to 10°C after isolation from the sewerage system). the warm sewage (20-25°C) and was remarkably In laboratory experiments, the El Tor strain isolated resistant to disinfection. from the locomotive depot was inoculated into various A very similar experience was reported by Zaidenov wastewaters and stored at 18-24°C. In mixtures of oil and others (1976). A sewerage system serving a plus water and diesel fuel plus water, survival was for locomotive depot and a housing estate was in- over 14 months, with an initial concentration of 10 per vestigated. Wastewater from the locomotive depot (450 milliliter. In domestic sewage, survival was less than 3 cubic meters per day) was rich in oil products and days; in locomotive depot wastewater, survival was passed through oil traps and a flotation chamber over 39 days; and in dairy effluent (included for before being mixed with domestic sewage (150-250 comparison), survival was less than 14 days. All cubic meters per day). The mixed sewage was then experiments were performed with initial inocula of 104 pumped to treatment fields. Because hot water was V. cholerae per milliliter. The source of infection of the used in the locomotive depot, the sewage was warm, sewerage system was not discovered. Repeated even in winter, and temperatures of 19-24°C were disinfection failed to clear V cRolerae from the network recorded throughout the year. The pH of the sewage until massive doses of chlorine (to achieve 10 Table 17-8. tg, values in hours for various types of V. cholerae in various waters and wastewaters Classical 01 El Tor 01 Non-OI Type of water Arith. Arith. Arith. enuironment No. mean Range No. mean Range No. mean Range Dechlorinated tap 8 22 3-48 8 49 2 163 ND ND ND water Well water 1 36 NA 13 116 5-264 ND ND ND Surface water 8 18 0.16-36 10 53 1-230 4 8 8-8 Seawater 3 95 0.36-161 7 56 3-235 ND ND ND Sewage 1 12 NA 9 66 8 240 2 8 8-8 Sterilized well 7 34 3-65 9 59 32 168 6 39 31-50 water, surface water or sewage No. Number of results. Arith. mean Arithmetic mean. ND No data. NA Not applicable. VIBRIO CHOLERAE AND CHOLERA 315 milligrams per liter throughout the system) and been isolated from Chesapeake Bay. V. cholerae 01 sulphuric acid (to lower sewage pH to 3-4) were added. (Inaba) has also been isolated from Louisiana salt Following this, no V. cholerae were isolated for the next marshes. Some of the V. cholerae 01 and V. cholerae 12 months. non-O1 strains isolated from the Chesapeake Bay and Further evidence of multiplication and prolonged the Louisiana coast showed evidence of toxin survival in some wastewater is provided by reports of production. A marked association of V. cholerae non- the multiplication of V. cholerae (El Tor, Inaba) in a 01 with zooplankton was found both in the clinic septic tank in Japan (MMWR 1979) and the Chesapeake Bay and in surface water samples collected multiplication of V. cholerae (non-O1) in a trickling in Bangladesh. filter in Bangladesh (Daniel and Lloyd 1980b). These Bashford and others (1979) and West, Knowles and occurrences, and their relationship to environmental Lee (1980) reported the isolation of up to several reservoirs of some atypical and non-Ol V cholerw. hundred V. cholerae per milliliter from streams and await clarification. drainage ditches in Kent (England), including sites where there was no known sewage contamination. Isolations were more common during the summer. Except for one occasion, all isolations have been of Perhaps the greatest upset to traditional concepts of non-O1 serotypes, and all have been nontoxigenic (J. cholera epidemiology and bacteriology has come from Lee, personal communication). Muller (1978, 1979) the recent discoveries of V. cholerae and related isolated non-O1 V. cholerae from 33 percent of river organisms occurring in surface waters not known to be water samples in the Federal Republic of Germany, but fecally contaminated or in areas where no human not from sewage treatment plant effluents. Isolations infection has been recorded. V. cholerae, El Tor and were more numerous in summer. non-O1, were frequently isolated from wells, tanks, and V cholerae 01, atypical V cholerae 01 and non-Ol V rivers in India in the 1930s and 1940s, but their close cholerae have been isolated variously from freshwater, relationship with classical V. cholerae 01, and their saline water, and wastewater in Australia, Bangladesh, potential pathogenicity, were not recognized at that Brazil, England, Germany, Guam, Japan, the USA, time (Read and Pandit 1941; Taylor and Ahuja 1938; and the USSR (WHO Scientific Working Group 1980). Venkatraman, Krishnaswami and Ramakrishnan Most of these isolates have been found to be 1941). nontoxigenic and nonpathogenic. They have been Colwell, Kaper and Joseph (1977) reported the found in areas where cholera cases or infections are not isolation of non-O1 V. cholerae from various parts of known to occur (for example, Brazil, England, and the Chesapeake Bay (USA). Subsequently, Kaper and USA) and in waters that are not thought to have others (1979) described the ecology of non-O1 V. received any human fecal contamination (for example, cholerae in Chesaspeake Bay in some detail. England and the USA). It is very probable that some of Concentrations were up to 7 per liter, and isolations these V. cholerae isolates are free-living aquatic were only made at sites with salinities between 0.4 and organisms. Whether they are in any way related to 1.7 percent. There was no correlation between V. human disease or to the epidemiology of cholera cholerae counts and counts of total bacteria, coliforms, remains to be determined. fecal coliforms, or salmonellae. V. cholerae were not The speculation concerning a possible environmen- especially associated with bottom sediment or oysters. tal reservoir for atypical and non-O1 V. cholerae, and In a recent publication (Colwell and others 1980), possibly also for V. cholerae 01, has been increased by data on V. cholerae isolations from various brackish findings on the affinity of these organisms for chitin. and estuarine environments are summarized. V. Nalin and others (1979) found that about 70 percent of cholerae isolations in Chesapeake Bay were de- V. cholerae 01 organisms, which were shaken for 6 pendent on salinity and temperature, with the highest hours with powdered crabshell in a 4.2 percent salt recoveries (up to 46 per liter) being reported at solution at pH 6.2 and 20°C. adsorbed to the chitin salinities of 0.3 to 1.7 percent and during the summer particles. These adsorbed V. cholerae were then when water temperatures were 28°C. V. cholerae somewhat resistant to an acid environment simulating isolations were not correlated with known fecal the stomach (pH) 1.6-1.8 for 13 minutes). V. cholerae contamination, nor with fecal coliform counts, thus also multiplied (>4 log increase) when incubated suggesting that V. cholerae "is an autochthonous for 2 days at 37°C in 4.2 percent salt solution species in the estuarine ecosystem". Both non-O1 V. containing chitin. Other studies have shown that V. cholerae serotypes and V. cholerae 01 (Inaba) have cholerae 01 (classical and El Tor) and non-O1 can 316 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA produce chitinase (Dastidar and Narayanaswami considered that these findings had considerable 1968) and that non-Ol V. cholerae, like V. para- relevance to the epidemiology of cholera in arid areas hlaemolvticus, can adsorb to, and multiply on, chitinous of West Africa. Isaacson and Smit (1979) showed that fauna such as crab, shrimp, and zooplankton (Colwell, V. cholerae (El Tor, Inaba) multiplied, and could Kaper and Joseph 1977; Kaneko and Colwell 1973, survive for at least 120 hours, in pooled human sweat. 1975, 1978; Kaper and others 1979; Nalin 1976; Multiplication of V. cholerae in sweat was believed to Sochard and others 1979). have promoted the transmission of cholera among South African gold miners undergoing heat acclimati- In sweat zation (Isaacson and others 1974). It is not known Dodin and F&lix (1972) found that V. cholerae, El whether V. cIIolera survives well in sweat on the skin. Tor, was still viable after seven weeks at 28°C in human sweat and on gauze pads soaked in sweat and On surlaces stored in humid conditions. From one quantitative V. cholerae survival on surfaces is usually limited experiment a tgo of 215 hours at 28°C in sweat can be because of the sensitivity of the organism to computed. This is much longer than typical t90 values desiccation. Four studies on V. cholerae on various at that temperature (table 17-8). Dodin and Felix household items are summarized in table 17-9. Table 17-9. Survival of V. cholerae on surfaces Source Biotype Type of surface Temperature Survtiala Felsenfeld Classical Absorbent materials (1965) and Cotton 28-30'C 5-7 days El Tor Chopsticks 2-3 days Paper 2-3 days Shoes 2-3 days Silk 3-5 days Non-absorbent materials Aluminium foil 28-30°C 1 day Coins 1 day Tin cups 1 day Plastic envelopes 1-2 days China plates 1-2 days Metal utensils 1-2 days Gohar and Classical Linen Room temp. 6 days Makkawi Wool (Egypt) 5 days (1948) Leather 3 days Paper and rubber 10 hours Coins 6 hours Pesigan, El Tor Frying pan 30-32°C 4 hours Plantilla China plates 4 hours and Rolda Pestle and mortar 4 hours (1967) Drinking glass 4 hours Metal utensils 24 hours Kitchen knife 48 hours Wooden chopping 24 hours block Shousha (1948) Classical Cotton and cloth Room temp. 4 days Bank note (Egypt) 3 days Postage stamp 2 days Coin I day Note: Older literature is reviewed by Pollitzer (1959). a. Times given are those at which viable organisms could no longer be detected. VIBRIO CHOLER4E AND CHOLERA 317 The longer persistence on absorbent materials, likely that some foods can and do act as a primary especially cotton, is interesting and suggests that vehicle for spreading cholera, especially within the clothing (especially clothing soaked in sweat) may act household or at feasts and markets. as a temporary habitat for V. cholerae. It is also noteworthy that survival times are markedly shorter than those reported for other enteric bacteria-for instance, Shigella (chapter 16)-on similar surfaces. Inactivation by Sewage Treatment Processes In soil There is very little information on the fate of V cholerae in sewage treatment plants partly because, as Experiments in Israel (Gerichter and others 1975) metoe abve motpol ih hlr rdc found that V. cholerae (El Tor ) in soil survived for up to mentioned above, most people with cholera produce no sewage; therefore V. cholerae is only very rarely 4 days when the soil was allowed to dry slowly, but for g y y y up t dy h how r afound in sewage, and even then in low concentrations. wupnton10tdaysmwenathe sowas regulal c rem ois Flu (1921) studied seeded V. cholerae in septic tanks with uncontaminated sewage (initial concentrations in Batavia (now Jakarta; Indonesia). A total of five were 10 per gram of soil, and the storage temperature setcanswrsudd,ndiolyneasV was 20-28°C). Nalin and others (1980) reported septic tanks were studied, and in only one was V. wasurviv al inorover6 dayswhendV. hotherse(1980) rportd w cholerae detected in the effluent. Early studies reviewed survival for over 6 days when V. cholerae (El Tor) was inoculated into sterile potting soil and stored at 26°C. by Kabler (1959) reported a 98 percent reduction of V. inocuatedinto terie poting oil ad streda 6 cholerae in an activated sludge plant. In the same experiments it was found that common Kott an Beted sludge ant. earthworms (Luimbricus terrestris) ingested V cholerae Kott and Betzer (1972) studied a 70-liter model in sol ad swaste stabilization pond with a retention time of 5 in soil and subsequently died. V. cholerae multiplied in days. The pond was fed with diluted sewage the earth worms and were isolated at concentrations days. T 20 nigams per lite siked .wihV up to .0 pe .illtro wr ooeae (BOD5 = 200 millilgrams per liter) spiked with V. up to 10~ per milllihter of worm homogenate. cholerae (El Tor). Influent coliform and V cholerae concentrations were 3 x 106'8 x 108 and On food and crops 1 x 103-8 x 103 per 100 milliliters, respectively. Effluent coliform and V. cholerae concentrations were In looking at the potential of food for transmitting 8 x 104-4 x 107 and 0-2 per 100 milliliters re- cholera, it is important to make the distinction between spectively. The addition of 8 milligrams per liter of food that acts as a primary vehicle for cholera, chlorine to the waste stabilization pond effluent becoming infected through direct contact with the eliminated all remaining V. cholerae. stools of a case or carrier, and food that acts as a Daniel and Lloyd (1980a) studied two Oxfam secondary vehicle of spread, becoming contaminated Sanitation Units in refugee camps near Dacca by polluted water. Most documented occurrences of (Bangladesh). These units treated very strong sewage foodborne cholera are of the second kind, and the most (17,000 and 7,400 milligrams of suspended solids per numerous of these incidents are those involving fish liter) in two unbaffled, flexible tanks connected in and shellfish. Alternatively, food can act as a secondary series. Each tank had a volume of 18 cubic meters, and vehicle of cholera through the use of polluted water to the flow of sewage was 2.5 to 3 cubic meters per day. irrigate or freshen vegetables. Thus, the total mean retention times were 12-15 days. The evidence for foods acting as the primary vehicles The geometric mean inflowing concentrations of non- for cholera is very limited. This is to be expected 01 V cholerae at the two camps were 2.6 x 103 and because few studies have examined the domestic 1.6 x 102 per 100 milliliters, respectively. The geomet- environment in a cholera area during an outbreak and ric mean effluent concentrations were 6.5 and 5.3 per carried out a systematic investigation of food for V. 100 milliliters. Thus, overall removal rates at the two cholerae. Table 17-10 summarizes some literature on camps were 99.8 and 96.4 percent, respectively. These the survival of V. cholerae on food. It is clear that removal rates give tgo values of 106 and 257 hours, survival times of several days are commonly achieved, respectively, which are longer than those reported in even at around 30°C. Survival is longest in moist, table 17-7, especially if the warm ambient temperature nonacidic, and sterile (that is, cooked) foods. Only two is taken into account. This suggests either short- studies (Felsenfeld 1965; Neogy 1965) directly com- circuiting in the tanks, which is quite probable, or non- pared the survival of the classical and El Tor biotypes, 0 1 V. cholerae multiplication in the warm sewage in the and both found that El Tor survived for longer. It seems tanks. 318 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-10. Survival of V. cholerae on food and crops Source Biotype Type offood Temperature SurviualI .4. Meat Cheng (1963) El Tor Beef Day 1: 22°C 5 days Thereafter: 3-4°C Felsenfeld El Tor and Raw beef 2-4°C 5-7 days (1965) classical 28-30°C 1-2 days Cooked beef 2-4°C 1-2 weeks 28-30°C 3-7 days Sausages 2-4°C 1 day (surface and inside) 28-30°C 1 day Pesigan, El Tor Raw meat 5-10°C 4-9 days Plantilla 30-32°C 2-4 days and Rolda (1967) Cooked meat 5-I0'C 3-5 days 30-32°C 2 5 days B. Fish Cheng (1963) El Tor Lice-eye fish Day 1: 21.5°C 16 days Sliced sword-fish Thereafter: 4°C 10 days Felsenfeld El Tor and Shrimp 2-4°C 1-3 days (1965) classical 28-30°C 1-2 days Catfish Raw 2 4°C 1-2 weeks 28-30°C 2-4 days Dried 2-4°C 3-5 days 28-30°C 1-2 days Salted 2-4°C 1-2 days 28-30°C I day Cooked 2-4°C 2-7 days 28-30°C 1-6 days Pesigan, El Tor Various fish and 5-10°C 4-9 days Plantilla shellfish 30-32°C 2-4 days and Rolda (1967) C. Vegetables and fruit Cheng (1963) El Tor Horseradish Day 1: 22°C 21 days Cucumber Thereafter: 3-4°C 23 days Tomato 16 days Orange 14 days El Shawi and El Tor Date Room temp. 3 days Thawaini Melon (Iraq) 2 days (1967) Felsenfeld El Tor and A comprehensive 2-4°C Up to 4 weeks (1965) classical survey of a wide range 28-30°C Up to 7 days (except inside melon, of cooked and which was 2 weeks); survival uncooked fruits and was especially long on cabbage, vegetables cucumber, eggplant, melon, okra, peas, and potatoes. VIBRIO CHOLERAE AND CHOLERA 319 Table 17-10 (continued) Source Biotype Type offood Temperature Survivala Gerichter El Tor Parsley 20-26'C 1 day and others Tomato and carrot 1.5 days (1975) Cucumber, pepper, and okra 1-2 days Lettuce 2-3 days Mean death rates for all the above were 4-6 log units per day Parsley Wet 20-28°C 2 days Dry 1 day Lettuce Group of leaves 18-26°C 68 hours Single leaf 44 hours Tomato in sunlight 22-30°C 4 hours Parsley 4°C 2 days Lettuce 4 days Gohar and Classical Date Room temp. 4 days Makkawi (1948) Vegetables (Egypt) 6 days Neogy El Tor and Papaya Room temp. 1 day (1965) classical Cucumber (India) >1 day Pineapple 15 minutes Boiled rice soaked overnight 1 hour Pesigan, El Tor Cooked fruit and 5-1OIC 3-5 days Plantilla vegetables 30-32°C 2-5 days and Rolda 5-10°C 2-3 days (1967) Fresh fruit 30-32°C 1 day Fresh vegetables 5-10°C 6-9 days 30-32°C 2-5 days Prescott El Tor Lime, lemon, and and date 20-25°C 1 hour Bhattacharjee Orange, grape, (1969) fig, raisin, and tomato 1 day Banana, guava, papaya, onion, eggplant, pea, celery, green bean. bean sprout, and rice. 2-5 days Okra, lima bean, pumpkin, and potato 6-8 days Shousha Classical Onion and date Room temp. 4 days (1948) Garlic, rice, (Egypt) lentil, and grape 3 days Orange and lemon 7 hours 320 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Table 17-10 (continued) Source Biotype Type of food Temperature Survivala D. Milk and Milk products Felsenfeld El Tor and Butter, 2-4°C 1-2 weeks (1965) classical unsalted 28-30°C 1 week Cheese 2-4'C 2-3 weeks 28-30°C I week Custard 2-4 DC 3-4 weeks 28-30°C 1-2 weeks Ice cream 2-40C 3-4 weeks 28-30°C 5-7 days Milk 2-4°C 3-4 weeks 28-30'C 1-3 weeks Lema, Ogawa El Tor Milk 4°C 3 weeks and Mhalu 30°C 4 days (1979) Neogy El Tor and Milk desserts Room temp. I day (1965) classical (India) Pesigan, El Tor Milk, ice cream, 5-10'C I week->2 weeks Pantilla and butter 30-32°C 5-14 days and Rolda (1967) Prescott and El Tor Milk desserts 20-25'C 1-2 days Bhattacharjee (1969) Shousha Classicat Milk 4°C > 2 days (1948) Sour milk Room temp. 2 hours Butter [_ rr) >2 days Cheese 7 hours E. Other foods El Shawi El Tor Barley and Room temp. 2 days and Thewaini wheat (Iraq) (1967) Felsenfeld El Tor and A comprehensive 2-4°C Up to 4 weeks (1965) classical survey of a 28-30°C Not more than wide range of 7 days, cooked and except for uncooked foods coconut cream (10 days), coconut dishes (3 weeks). and noodles (2 weeks) Gohar and Classical Honey and Room temp. 3 hours Makkawi (1948) treacle Fl -. I Neogy (1965) El Tor and Sweet and sour Room temp. 5 minutes classical curd (India) F . n and 1 day sandesh Pesigan. El Tor Cooked noodles. 5-10°C 3-5 days Plantilla rice cake, and 30-32CC 2-5 days and Rolda jam (1967) VIBRIO CHOLERAE AND CHOLERA 321 Table 17-10 (continued) Source Biotype Type offood Temperature Survivala Prescott and El Tor Wheat and nuts 2025aC 3 days Bhattacharjee Spices 20-25°C 1-5 days (1969) Shousha Classical Sugar Room temp. 4 days (1948) Bread (Egypt) 3 days Honey 2 days F Beverages El Shawi El Tor Soft drinks Room temp. 1 day and Thewaini (Iraq) (1967) Felsenfeld El Tor and Beer, carbonated 2-4°C I day (1965) classical water, 28-30°C I day carbonated soft drinks, ime and whisky Cocoa 2-4°C 1-2 weeks 28-30'C 3-5 days Coffee 2-4°C 1-2 days 28-30°C 1 day Ice cubes 2-4°C 4-5 weeks Lemonade 2-4°C 2-3 weeks 28-30°C 5-7 days Tea 2 4°C 1 week 28-30°C 2-3 days Lema, Ogwa El Tor Coconut fluid 4'C 4 days and Mhalu 3OcC 2 days (1979) Beer, gin, and 4°C I hour traditional (except for alcoholic mnbege, in which beverages chibuku survival was (maize and beans) 2 days) and mbege (bananas and millet) 30°C I hour Pesigan, El Tor Coca cola 5-1O°C 2 days Pantilla 30-32°C 4 hours and Rolda (1967) Prescott and El Tor Coca cola 20-25WC 1 day Bhattacharjee Rosewater 2 days (1969) Ground coffee I hour Tea leaves I day Note: Older literature is reviewed by Pollitzer (1959). a. Times given, for instance, as 2 days are durations at which viable organisms could no longer be detected. Times given as > 2 days indicate that organisms were still viable at that time but that sampling was discontinued. 322 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA ZONE 45- t-45 40 SAFETY - 40 X x 35- -35 x x~ ~ ~~ x0 ,15 Y ~= = - a ) fi20 - xXx- 20 15- x x _15 X 100°h destruction of Vibrio cholerae 10 e* less than 100%/c destrvction of Vibrio cholerae -10 5- * wxOx - 5 1 10 100 1000 10000 iday Iweek lmonth lyear TIME (HOURS) Figure 17-3. The influence of time and temperature on V. cholerae. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death Daniel and Lloyd (1980b) reported that small Literature Cited trickling filters were installed to treat further the effluents from these Oxfam Sanitation Units. Influent Abel, R. and Claussen, R. (1895). Untersuchungen uiber die concentrations (effluents from the second tank of the lebensdauer der cholera-vibrionen in fakalien. Zentralblatt main unit (non-O1 V. cholerae were 3-9 per 100 fur Bakteriologie, und Parasitenkunde, I, 17, 77-81 and milliliters, while effluents from the trickling filters 118-130. contaied 3-,400 pr 100milliiters.The athors Altukhov, A. A., Ivanov, S. I., Semiotrochevl, V. L., Bulegenov, contained 3-2,400 per 100 milliliters. The authors E. I., Lebedev, K. K., Filimonova, L. V., Zakharov, N. I. concluded that non-O1 V. cholerae was multiplying in and Rybak, E. t. (1975). Prolonged detection of El Tor ponded sewage in the trickling filters. cholera vibrio in sewage of a bath-house. Zhurnal Mikrobiologii, Epidemiologii i Immunobiologii, 2, 41-44. Azurin, J. C. and Alvero, M. (1974). Field evaluation of Inactivation by Night Soil and environmental sanitation measures against cholera. Sludge Treatment Processes Bulletin of the World Health Organization, 51, 19-26. Azurin, J. C., Kobari, K., Barua, D., Alvero, M., Gomez, C. Z., No reports of V. cholerae reduction during night soil Dizon, J. J., Nakano, E-I., Suplido, R. and Ledesma, L. or sludge treatment were located. The data given in (1967). A long-term carrier of cholera: Cholera Dolores. table 17-6 suggest that V. cholerae will be eliminated by Bulletin of the World Health Organization, 37, 745-749. ,,hn e ic Bart, K. J., Khan, M. and Mosley, W. H. (1970). Isolation of anyoproestha as hing a waretenimatio Time-ofappreiaby Vibrio cholerae from nightsoil during epidemics of classical and El Tor cholera in East Pakistan. Bulletin of the World combinations lethal to V. cholerae are given in figure Health Organization, 43, 421-429. 17-3. It appears that V. cholerae will be eliminated by Bashford, D. J., Donovan, T. J., Furniss, A. L. and Lee, J. V. almost any sludge digestion, composting, or storage (1979). Vibrio cholerae in Kent. Lancet, 1, 436-437. process and will certainly be removed far more readily Blake, P. A., Rosenberg, M. L., Florencia, J., Costa, J. B., than E. coli and other fecal indicator bacteria (chapter Quintino, L. D. P. and Gangarosa, E. J. (1977). Cholera in 13). Portugal, 1974. II. Transmission by bottled mineral water. VIBRIO CHOLERAE AND CHOLERA 323 American Journal of Epidemiology, 105, 344-348. epidemic situations during 1961-1980. Tropical Diseases Briscoe, J. (1978). The role of water supply in improving Bulletin. 78, 675-698. health in poor countries (with special reference to Bangla (1982). Environmental aspects of cholera epidem- Desh). American Journial of Clinical Nutrition, 31, iology. III. Transmission and control. Tropical Diseases 2100-2113. Bulletin, 79, 1-47. Cash, R. A., Music, S. I., Libonati,J. P.,Snyder,M.J.,Wenzel, Felsenfeld, 0. (1965). Notes on food, beverages and fomites R. P. and Hornick, R. B. (1974). Response of men to contaminated with Vibrio cliolerae. Bulletin of the World infection with Vibrio cholerae. I. Clinical, serologic and Health Organization, 33, 725-734. bacteriologic responses to a known inoculum. Journal of (1974). The survival of cholera vibrios. In Cholera, Infectious Diseases, 129, 45-52. eds. Barua, D. and Burrows, W., pp. 359-366. Philadelphia: Cheng, C. T. (1963). Survival of El Tor vibrio outside the W. B. Saunders. human body. Nagasaki Igakkai Zassi, 38, 870-876. Flu, P. C. (1921). Investigations of the duration of life of Colwell, R. R., Kaper, J. and Joseph, S. W. (1977). Vibrio cholera vibriones and typhoid bacteria in septic tanks at cholerae, Vibrio parahaemolyticus, and other vibrios: Batavia. Mededeelingen van der Burgerlijken occurrence and distribution in Chesapeake Bay. Science, Geneeskundigen Dienst in Nederlandschindie, 3, 289-297. 198, 394-396. Forbes, G. I. Lockhart, J. D. F. and Bowman, R. K. (1967). Colwell, R. R., Kaper, J., Seidler, R., Voll, M. J., MeNicol, L. Cholera and nightsoil infection in Hong Kong, 1966. A. Garges, S., Lockman, H., Maneval, D. and Remmers, E., Bulletin of the World Health Organization, 36, 367-373. Joseph, S. W., Bradford. H., Roberts, N., Huq, I. and Huq, Gangarosa, E. J. and Mosley, W. H. (1974). Epidemiology A. (1980). Isolation of 01 and non-Ol Vibrio cholerae from and surveillance of cholera. In Cholera, eds. Barua, D. and estuaries and brackish water environments. In Proceedings Burrows, W., pp. 381-403. Philadelphia: W. B. Saunders. of the 15th Joint Conference on Cholera, US-Japan Gerichter, C. B., Sechter, I. Gavish, A. and Cahan, D. (1975). Cooperative Medical Science Program, pp. 44-51. Viability of Vibrio cholerae biotype El Tor and of cholera Bethesda, Md.: National Institutes of health. phage on vegetables. Israel Journal of Medical Science, 11, Cvjetanovic, B. (1979). Sanitation versus immunization in 889-895. control of enteric and diarrhoeal diseases. Progress in Gildemeister, E. and Baerthlein, K. (1915). Beitrag zur Water Technology, 11, 81-87. cholerafrage. Mainchener Medizinische Wochenschrift, 62, Cvjetanovic, B., Grab, B. and Uemura, K. (1978). Dynamnics of 705-708. Acute Bacterial Diseases, Epidemiological Models and their Gohar, M. A. and Makkawi, M. (1948). Cholera in Egypt: Application in Public Health. Geneva: World Health Laboratory diagnosis and protective inoculation. Journal Organization. of Tropical Medicine anid Hygiene, 51, 95-99. Daniel, R. R. and Lloyd, B. J. (1980a). Microbiological Greenough, W. B. (1979). Vibrio cholerae. In Principles and studies on two Oxfam Sanitation Units operating in Practice of Infectious Diseases, eds. Mandell, G. L., Bengali refugee camps. Water Research, 14, 1567-1571. Douglas, R. G. and Bennett, J. E., pp. 1672-1687. New (1980b). A note on the fate of El Tor cholera and other York: John Wiley. vibrios in percolating filters. Journal of Applied Grieg, E. D. W. (1914). On the vitality of the cholera vibrio Bacteriology, 48, 207-210. outside the human body. Indian Journal of Medical Dastidar, S. G. and Narayanaswami, A. (1968). The Research, 1, 481-504. occurrence ofchitinasein vibrios.IndianJournalofMedical Gunn, R. A., Kimball, A. M., Pollard, R. A., Feeley, J. C. and Research, 56, 654-658. Feldman, R. A. (1979). Bottle feeding as a risk factor for Dizon,J., Fukumi, H., Barua, D., Valera,J.,Jayme,F., Gomez, cholera in infants. Lancet, 2, 730-732. F., Yamamoto, S-I., Wake, A., Gomez, C. Z., Takahira. Y., Hornick, R. B., Music, S. 1., Wenzel, R., Cash, R., Libonati, J. Paraan, A., Rolda, L., Alvero, M., Abou-Gareeb, A. H., P., Snyder. M. J. and Woodward, T. E. (1971). The Broad Kobari, K. and Azurin, J. C. (1967). Studies on cholera Street pump revisited: response of volunteers to ingested carriers. Bulletin of the World Health Organization, 37, cholera vibrios. Bulletin of the New York Academy of 737-743. Medicine. 47, 1181-1191. Dodin, A. and Felix, H. (1972). Du role de la sueur dans Howard, J. and Lloyd, B. (1979). Sanitation and disease in l'epidemiologie du cholera en pays sec. Bulletin de Bangladesh urban slums and refugee camps. Progress in l'Academie Nationale de Medicine, 156, 845-852. Water Technology, 11, 191-200. El-Shawi, N. N. and Thewaini, A. J. (1967). El Tor vibrios Isaacson, M., Clarke, K. R., Ellacombe, G. H.. Smit. isolated in Iraq and their survival on some foods and W. A., Smit, P., Koornhof, H. J., Smith, L. S. and Kriel, L. J. beverages. WHO/Cholera Information/67.9 Geneva: (1974). The recent cholera outbreak in the South African World Health Organization, Unpublished document. gold mining industry. South African Medical Journal, 49, Feachem, R. G. A. (1976). Is cholera primarily water-borne? 2557-2560. Lancet, 2, 957. Issacson, M. and Smit, P. (1979). The survival and (1981). Environmental aspects of cholera epidem- transmission of V. cholerae in an artificial tropical iology. I. A review of selected topics reports of endemic and environment. Progress in Water Technology, 11, 89-96. 324 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA Jamieson. W., Madri, P. and Claus, G. 11976). Survival of - (1979). NAG-vibrionen. choleraahnliche erreger in certain pathogenic microorganisms in sea water. unseren gewassern. Forum Stidte-HlYgiene, 30, 211-214. Hydrobiologia, 50, 117-121. Nalin, D. R. (1976). Cholera, copepods and chitinase, Lanicet, Kabler, P. (1959). Removal of pathogenic micro-organisms 2, 958. by sewage treatment processes. Sewage and Industrial Nalin, D. R., Dava, V., Reid. A., Levine, M. M. and Cisneros. Wastes, 31, 1373-1382. L. (1979). Adsorption and growth of Vibrio cliolerae on Kaneko, T. and Colwell, R. R. (1973). Ecology of Vibrio chitin. Infection and Immutnity. 25, 768-770. parahaemnolyticus in Chesapeake Bay. Journal of Nalin, D. R., Robbins-Browne, R., Levine, M. M.. Daya, V. Bacteriology, 113, 24-32. and Noble, P. (1980). Multiplication of Vibrio cholerae in (1975). Adsorption of l'ibrio parahaemnolyticus onto earthworms. In Curreit Ci, i .. l . and Infectious chitin and copepods. Applied Microbiology. 29, 269-274. Disease: Proceedings of'the 11th International Congress of' (1978). The annual cycle of Vibrio paralhaemiolvticus Chemvotherapy and the 19th Ilnterscienzce Conference on in Chesapeake Bay. Microbial Ecology. 4, 135-155. Anti-Microbial Agents and Chemotherapy, eds. Nelson, J. Kaper, J.. Lockman, H.. Colwell. R. R. and Joseph, S. W. D. and Grassi, C., pp. 936-937. Washington. D.C.: (1979). Ecology, serology, and enterotoxin production of American Society of Microbiology. Vibrio cliolerae in Chesapeake Bay. .4pplied aniid Neogy, K. N.. (1965). Viability of V. clolerae and V. cholerae Environmental Microbiology, 37, 91-103. El Tor in food and water. Bulletini of'thle Calcutta School of Khan, M. and Shahidullah. M. (1980). Cholera due to the El Tropical Medicine, 13, 10-11. Tor biotype equals the classical biotype in severity and Ohwada, S. (1924). Destination of cholera vibrios in the attack rates. Journal of' Tropical Medicine and Hygiene. 83, sewage watcr of Tokyo city. Journal of the Kejo Medical 35-39. Society. 3, 11-12. Khan, S. and Agarwal. M. N. (1929). On the duration of the Pandit, C. G., Pal, S. C., Murti, G. V., Misra, B. S., Murty, D. life of vibrios in the Ganges and Jumna river water. Inldiani K. and Shrivastav, J. B. (1967). Survival of V. cliolerae Journial of'Medical Research, 16, 993-1008. biotype El Tor in well water. Bulletin of the World Health Koch, R. (1884). An address on cholera and its bacillus. Organiiation, 37, 681-685. British Medical Journal, August 30, 403-407 and 453-459. Pesigan, T. P., Plantilla, J. and Rolda, M. (1967). Applied Konchady. D. Prescott, L. M., Datta, A. and De, S. P. (1969). studies on the viability of El Tor vibrios. Bulletini oj'tlhe Survival of Vibrio clholerae in some of the waters of World Health Organization, 37. 779-786. Calcutta. Inidian Journal of'Medical Researclh, 57, 60-65. Pollitzer, R. (1959). Cholera. Monograph 43. Geneva: World Kott, Y. and Betzer, N. (1972). The fate of Vibrio cholerae (El Health Organization. Tor) in oxidation pond effluents. Israel Journlal ofMedical Prescott, L. M. and Bhattacharjee, N. K. (1969) Viability of Science. 8, 1912-1916 El Tor vibrios in common foodstuffs found in an endemic Lahiri, M. N., Das, P.C. and Malik, K. S. (1939). The viability cholera area. Bulletin of thle World Health Organzization, 40, of Vibrio chlolerae in natural waters. Indiat. Medical 980-982. Gazette. 74, 742-744. Read, W. D. B.. Gurkirpal Singh. J., Seal, S. C. and Bose. S. Lema, O., Ogwa, M. and Mhalu, F. S. (1979). Survival of El (1939). Growth and survival of V. chlolerae with special Tor cholera vibrio in local water sources and beverages in reference to growth and survival in water. Indiani Journal of Tanzania. East African Medical Journal, 56, 504-508. Medical Researchl, 27, 1-40. Levine, R. J. and Nalin, D. R. (1976). Cholera is primarily Read, W. D. B. and Pandit, S. R. (1941). Distribution of V. waterborne in Bangladesh. Lancet. 2. 1305. cholerae and El Tor type strains in certain rural areas in McFeters, G. A.. Bissonnette. G. K.. Jezeski, J. J., Thomson, India. Indian Journlal of'Medical Researclh, 29, 403-415. C. A. and Stuart, D. G. (1974). Comparative survival of Sack, G. H.. Pierce, N. F., Hennessey. K. N., Mitra. R. C., indicator bacteria and enteric pathogens in well water. Sack, R. B. and Mazumder, D. N. G. (1972). Gastric acidity Applied Microbiology. 27, 823-829. in cholera and non cholera diarrhoea. Bulletin of the World Mhalu, F. S.. Mmari, P. W. and Ijumba. J. (1979) Rapid Health Organization, 47. 31-36. emergence of El Tor Vibrio cliolerae resistant to Sanyal. S. C.. Singh. S. J., Tiwari, 1. C., Sen, P. C.. Marwah, S. antimicrobial agents during first six months of fourth M., Hazarika, U. R., Hardas Singh, Shimada, T. and cholera epidemic in Tanzania. Lancet, 1, 345-347. Sakazaki, R. (1974). Role of household animals in MMWR (1979). Cholera surveillance-Japan. Miorbidirv and maintenance of cholera infection in a community. Journal It./ i. ;,,, Weekly Report. 29, 98-99. of Infectiouis Diseases, 130, 575-579. Mukerjee, S., Rudra, B. C. and Roy, U. K. G. (1961). Sayamov, R. M. and Zaidenov, A. M. (1978). Survival and Observations on cholera endemicity in Calcutta and properties of cholera vibrios cultivated in mineral water. survival of Vibrio cholerae in the water sources. Annials of Zhurnal Mikrobiologii, Epidemiologii i 1 .i., ,,, 11, Biochemistry and Experiniental Medicine, 11, 31-40. 66-70. Muller, H. E. (1978). Occurrence and ecology of NAG vibrios Shoda, T., Koreyeda, T. and Otomo, T. (1934). The viability in surface waters. Zentralblatt foir Bakteriologie. of cholera vibrios in the human excreta. .Journal of the Parasitenikuinde, Inifektions krankheiten und Hygiene, 1. B. Public Health Association of Japan, 10, 1-9. 167, 272-284. Shousha. A. T. (1948). Cholera epidemic in Egypt (1947): a I IBRIO CHOLERAE AND CHOLERA 325 preliminary report. Bulletin ol the llorld Healthi Towner, K. J., Pearson, N. J. and O'Grady, F. (1979). Organization, 1, 353--381. Resistant Vibrio cholerae El Tor in Tanzania. Lancer, 2, Shrewsbury, J. F. D. and Barson, G. J. (1957). On the 147-148. absolute viability of certain pathogenic bacteria in a Van de Linde, P. A. M. and Forbes. G. l. (I 9651. Observations synthetic well-water. Journlal ol Pathology and on the spread of cholera in Hong Kong, 1961--1963. Bacteriology, 74, 215-220. Bulletin of tile World Health Organlizationi, 32. 515-530. Sinha, R.. Deb, B. C.. De, S. P., Abou-Gareeb, A. H. and Venkatraman. K. V., Krishnaswami, A. K. and Shrivastava, D. L. (1967). Cholera carrier studies in Ramakrishnan,C. S. (1941). Occurrence of vibrio El Tor in Calcutta in 1966-67. Bulletin of the World Health natural sources of water in the absence of cholera. Indian OrganiZation, 37, 89--100. Journial of Medical Researchi, 29, 419-424. Smith, H. L., Freter, R. and Sweeney, F. J. (1961). West, P. A.. Knowles, C. J. and Lee, J. V. (1980). Ecology of Enumeration of cholera vibrios in fecal samples. Journal of Vibrio species, including Vibrio cholerae, in waters of Kent, InJectious Diseases. 109, 31-34. United Kingdom. Society for General Microbiology Sochard, M. R., Wilson, D. F., Austin, B. and Colwell. R. R. Quarterly, 7, 80. (1979). Bacteria associated with the surface and gut of WHO Scientific Working Group (1980). Cholera and other marine copepods. Applied and Environmental vibrio-associated diarrhoeas. Bulletinz of the World Health Microbiology, 37, 750-759. Organization, 58, 353-374. Sommer, A. and Mosley. W. H. (1973). Ineffectiveness of Yasukawa, Y. (1933). Experiments on sea water and Vib7io cholera vaccination as an epidemic control measure. cholerae. Japanese Journlal of Experimnental Medicinie, 11, Lancet, 1, 1232-1235. 119-127. Taylor, J. and Ahuja, M. L. (1938). Incidence and characters Zaidenov. A. M., Sayamov, R. M., Maloletkov, 1. S., of vibrios in waters in northern India. Indian Journal oJ Lazorenko, N. F., Bichul, K. G., Milyutin, V. N., Titenko, Medical Research, 26, 1-32. M. T.. Popov. G. M., Kotov, V. K., Galtseva, G. V.. Threlfall, E. J., Rowe, B. and Huq, 1. (1980). Plasmid-encoded Goldberg, A. M.. Kiseleva. V. l., Stepanets, V. 1., multiple antibiotic resistance in Vibrio cholerae El Tor Seliverstov, V. I., Goryachkina. T. Ya., Reznikov. L. G.. from Bangladesh. Lancet, 1, 1247-1248. Lukash, V. O., Arendarskava, L. S. and Azykovskaya, 1. S. Towner, K. J., Pearson, N. J., Mhalu, F. S. and O'Grady, F. (1976). Prolonged survival of El Tor cholera vibrio in (1980). Resistance to antimicrobial agents of Vibrio naturally infected sewage. Zhu1rnal Mikrobiologii. cholerae El Tor strains isolated during the fourth cholera Epidemiologii i Iinniunobiologii, 12, 61-69. epidemic in the United Republic of Tanzania. Bulletin o. the World Health Organiization, 58, 747 -751. 18 Yersinia and Yersiniosis IT IS ONLY in the last few years that Yersinia causes of Reiter's syndrome, which involves all three), enterocolitica has been recognized as an etiological and also infections of skin, wounds, and throat. agent of acute enteritis. It may therefore be grouped with Diagnosis is by isolation of the bacteria from fecal or Campylobacter (chapter 12) and the pathogenic forms of blood specimens. Some of the selective media used for Escherichia coli (chapter 13) as a "new" bacterial agent isolation of salmonellae are appropriate for recovery of diarrheal disease-although, unlike these other two, from feces, but with the important difference that an Yersinia is unlikely to prove to be a major cause of incubation temperature in the range of 22 to 29°C, diarrhea. rather than 37 to 420C, is optimal. Presumptive yersinias must be typed biochemically and may be Description of Pathogen and Disease further characterized by serotyping and phage typing. The genus Yersinia comprises three species, each of Occurrence which is essentially an animal parasite that sometimes infects man. Y. pestis is the causative agent of human Although the organism was first isolated in the USA plague and is primarily a parasite of rodents. y. in 1923,itwasnotrecognizedasahumanpathogenuntil pseudotuberculosis is primarily a parasite of guinea pigs the early 1960s. The first human cases of infection were and other rodents and occasionally infects humans, diagnosed in France, Belgium, and Sweden in 1963; causing a variety of pathological conditions. y. since then it has been identified as a human pathogen in enterocolitica causes gastroenteritis and other sym- thirty countries throughout the world. In Europe and ptoms in man and infects a wide range of wild and North America, Y. enterocolitica may be responsible for domestic animals. Only Y. enterocolitica will be dealt between 1 and 3 percent of recorded acute cases of with in this chapter because it alone out of the three is gastroenteritis, but no comparable data are yet primarily an excreted pathogen. available from developing countries. It is certain that its recorded incidence and geographical distribution are Identification artificially low as a result of widespread inadequacies in diagnostic expertise and, hence, reporting. Yersiniosis is caused by bacterial infection primarily of the intestine and blood circulatory system. The causative organism Y. enterocolitica most commonly Infectious agent gives rise to an acute enterocolitis and septicaemia. Y. enterocolitica possesses all the characteristics of Diarrhea may be the only symptom, or it may be the Enterobacteriaceae, to which family yersinias were accompanied by abdominal pain, fever, or both. It is assigned in 1966. It is a Gram-negative ovoid or rod- often difficult to distinguish the disease clinically from shaped organism measuringO.8-3.0 micrometers by 0.8 other enteric infections such as those produced by micrometers. It is a facultative anaerobe. About thirty- certain shigellae and salmonellae. However, the acute four serotypes have been recognized, of which a number infection sometimes resembles appendicitis, and in such are characteristically associated with particular non- cases surgery will reveal inflammation of the appendix human animal species, whereas others are associated together with terminal ileitis and mesenteric adenitis. with several human and nonhuman animals. Serotypes Other less frequent forms of infection include pyuria, 03,08, and 09 are particularly associated with human polyarthritis, and conjunctivitis (that is, it is one of the disease. 327 328 ENVIRONMENTAL BIOLOGY & EPIDEMlOLOGY: BACTERIA Reservoirs that, knowledge of its epidemiology is very limited. It is likely that wild animals including shrews, red The more it is looked for, the more it is found, and the It is lkely tat wildanimal includng shrws, re worldwide picture of its epidemiology will continue to foxes, hares, and beavers form a natural reservoir for Y. buildwupislow e ov th exdde . in 1only enecoiia doesi anml fro whc. h build up slowly over the next decade. In 1966 only enterocolitica; domestic animals from which the pathogen has been isolated include cattle, sheep pigs, twenty-three cases of infection with Y. enterocolitica pathon hs bn iwere reported worldwide (Highsmith, Feeley and dogs, chinchillas, and geese. The number of animal dogs. chinchillas, and geese. The number of animal M orris 1977). By 1974 this had increased to over 4,000, species identified as affected by yersiniosis continues to . . . s b rise and now includes primates other than man. It has with most cases still being reported from Europe, where also been demonstrated that bivalves such as mussels many laboratories routiely screen stool specimens for and ovsters effectively concentrate these bacteria, this pathogen. .' The first documented foodborne outbreak of although they are unlikely to multiply in them in versiniosis occurred in New York (USA, Wakelee and seawater. It has been suggested that this organism I others 1977). Serotype 08 was isolated from children follows the same epidemic and epizootic pathways as sufrnfomad ialpn,evrad,nsme the salmonellae (see chapter 15). suffering from abdominal pain. fever, and, in some, diarrhea and slightly inflamed appendixes. Two hundred and eighteen children attending five county Transmission schools were affected. Out of ten possible sources of The means by which Y. enterocolitica is spread are infection including water, food, and milk, only still not proven. Fecal-oral transmission is most chocolate milk was associated with the illness. probable, and respiratory transmission is also a Serotype 08 was isolated from a carton of chocolate possibility. Foodborne and waterborne outbreaks have milk during the investigation. In the dairy plant, which been reported. supplied the schools, chocolate syrup was manually In one experiment with a human volunteer, a dose of added to a large open vat of pasteurized milk. Morris 3.5 x 109 organisms was required to produce an and Feeley (1976) reviewed the evidence of foodborne infection (Morris and Feeley 1976). Under natural yersiniosis. They noted that the organism is commonly conditions it is likely that considerably smaller doses found in specimens from swine slaughterhouses and will produceinfectioninaproportion of the population. has been isolated from samples of market meat, In any case, high infective doses may be obtained in vacuum-packed beef, mussels, oysters, and ice cream. It contaminated food since Y. enterocolitica multiplies has also been found in nonchlorinated well water used readily in many foods, even under refrigeration for drinking purposes. (Kendall and Gilbert 1980). Flies may play a role in contaminating food and thus in initiating foodborne transmission. Fukushima and Inicuibationi period others (1979) isolated Y. enterocolitica 03 from flies caught in the piggeries and the kitchens of two farms in Three to seven days is the normal range. Japan. Y enterocolitica 03 was also isolated from a ham hung in one piggery and from the feces of pigs in Period of communicability both piggeries. All 03 strains were of a common phage type. In infants and young children, the watery diarrhea Studies of the occurrence ofthe various serotypes and may persist for3to 14 days. In untreated cases excretion phage types of Y. enterocolitica have cast doubt upon oftheorganismmaycontinuefor2-3months.Achronic some of the more simple explanations of yersiniosis carrier state has not been demonstrated in man. but epidemiology (Mollaret 1976). Caprioli, Drapeau and certainly exists in other animals. Kasatiya (1978) isolated and typed Y. enterocolitica from 31 specimens of water and food and from 143 Resistance human specimens, in Quebec (Canada). Seventy-four The infection has been identified in people of all age percent of all isolates from human sources were serotype groups, but there is a much higher incidence in young 03 and this was the only serotype isolated from children. children under 4 years old. However, no serotype 03 isolates were obtained from any environmental Epidemiology, samples. It remains unclear whether yersiniosis is primarily an infection of nonhuman animals transmit- Because Y. enterocolitica is a recently recognized ted infrequently to man, often via food (as with pathogen, and possibly not a terribly important one at salmonellosis); whether man is his own reservoir for i'ERSINIA AND YERSINIOSIS 329 specific serotypes, or whether, as suggested by Mollaret tests, for the presence of Y enterocolitica. The organism (1976), animals and man both contaminate and are was identified in a total of 44 samples taken from dug infected from shared environmental reservoirs. wells, drilled wells, a spring, lakes, bathing water, and a municipal supply. Five positive well samples were from treated supplies: three chlorinated and two filtered. The Control Measures single positive spring sample was from a chlorinated supply, as was the single municipal sample, which was Not enough is known about the epidemiology and additionally treated by a home-installed filter. Water transmission of Y. enterocolitica to allow any confident samples yielding Y. enterocolitica showed only light recommendations about control. General techniques coliform contamination (the median fecal coliform of environmental hygiene, food hygiene, and sanitation count was 1 per 100 milliliters), and 25 percent of Y. are likely to be most effective. enterocolitica positive samples were negative for both total and fecal coliforms. Bearing in mind that the author had no control over sample collection and did not inspect the water sources concerned, these findings Occurrence and Survival in the suggest that at least some strains of Y. enterocolitica Environment behave very differently from coliforms in water systems and may survive some water treatment processes. Little is known about the occurrence and survival of There is, as yet, very little information on the ability of Y. enterocolitica in the environment. The organism has Y. enterocolitica to survive in the environment. been isolated from a variety of environmental samples, Dominowska and Malottke (1971) studied the survival especially food and water, but the isolated serotypes of Y. enterocolitica inoculated into various types of are often not those especially associated with human water and kept outdoors in Poland. The average disease (for instance, see Caprioli, Drapeau and survival time in unfiltered surface waters was 38 days in Kasatiya 1978). spring and 7 days in summer. In filtered water the Lassen (1972) isolated Y. enterocolitica from ten out bacteria survived 197 days in spring and 184 days in of fifty drinking water samples in Norway. Saari and summer. Under laboratory conditions at 18-22°C, Y. Quan (1976) surveyed rivers, reservoirs, and private ente7ocolitica at an inoculum of 103 per milliliter wells in Colorado (USA). Forty-seven percent of 125 survived in tap water for about 7 days and in lake water river sites, 11 percent of 26 reservoirs, and 1 percent of for 28 days. However, larger inocula allowed survival 563 wells tested contained this organism, with up to 5 beyond 77 days. distinct strains per water source. The authors noted Schillinger and McFeters (1978) found a 2 log that although Y. enterocolitica commonly occurs in reduction in Y. enterocolitica concentrations in stream Colorado waters, serotypes pathogenic to humans are water at 5-8.5°C after 14 days, compared with a 3-5 log rarely found. Harvey and others (1976) isolated Y. reduction of E. coli over the same period (t,0 values enterocolitica at ten out of thirty-four stream and lake were 63 hours for Y. enterocolitica and 25 hours for E. sites in a mountainous area of California (USA) and coli). In chlorinated tap water, however, E. coli considered that the organisms probably derived from (tr5 = 0.5 hours) survived a little longer than Y. wild animals. Kapperud (1977) isolated Y. en- enterocolitica (t50 = 0.4 hours). terocolitica from nine out of twenty-nine surface water Highsmith and others (1977) demonstrated that Y. samples collected in areas of Norway and Denmark, enterocoliticacouldgrowinsteriledistilledwaterat4°C, where the organism infected small rodents, shrews, and 25°C, and 370C, but not at 42°C, and that the organism foxes. could survive in sterile distilled water for over 18 A few outbreaks of cases of gastroenteritis in months at 4°C. This, and other evidence presented by developed countries have been tentatively linked to Highsmith and her coworkers, suggests that Y. waterborne transmission of Y. enterocolitica. For enterocolitica may survive for considerable periods in instance, Eden and others (1977) reported the isolation cool, clean waters with a minimum of bacterial of Y. enterocolitica from well water at a Montana competition. By contrast, in sterilized saline waters (USA) ski resort soon after an outbreak of gastroen- (salinities = 0.5, 2.0, and 3.5 percent) and at various teritis of unknown cause. temperatures (4, 25, 37°C), an initial inoculum of Schiemann (1978) examined 2,588 surface and well 1.5 x 107 Y. enterocolitica per milliliterfailed to survive water samples, submitted to the Toronto (Canada) for more than 4 days, with a 6 log reduction after public health laboratory for routine bacteriological only 1 day (Jamieson, Madri and Claus 1976). 330 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: BACTERIA No data are available on the survival of Y. enterocolitica.Applied and Environmental Microbiology,38, enterocolitica in feces or sewage. 1009-1010. Harvey, S., Greenwood, J. R., Pickett, M. J. and Mah, R. A. (1976). Recovery of Yersinia enterocolitica from streams Inactivation by Sewage Treatment and lakes of California. Applied and Environmental Processes Microbiology, 32, 352-354. Highsmith, A. K., Feeley, J. C. and Morris, G. K. (1977). Isolation of Yersinia enterocolitica from water. In Bacterial No information is available on the destruction of Y. Indicators: Health Hazards Associated with water, eds. enterocolitica in sewage treatment plants or on the Hoadley, A. W. and Dutka, B. J., pp.265-274. Philadelphia: occurrence of this organism in sewage. In a laboratory American Society for Testing and Materials. study Y. enterocolitica, serotype 06, was inoculated Highsmith, A. K., Feeley, J. C. Skaliy, P., Wells, J. G. and continuously into a model activated sludge plant Wood, B. T.(1977). Isolation of Yersiniaenterocolitica from (volume 1 liter, retention time 8.3 hours) at a well water and growth in distilled water. Applied and concentration of 106 per milliliter. Y. enterocolitica and Environmental Microbiology, 34, 745-750. Jamieson, W., Madri, P. and Claus, G. (1976). Survival of tures. Removal rates were 99.8 percent and 97 percent at certain pathogenic microorganisms in sea water. 5ures. Removal rates wee9. percent a 0C and 97. percent t Hydrobiologia, 50, 117-121. 5° C, 95 percent and 80 percent at 200C, and 99.6 percent Kapperud, G. (1977). Yersinia enterocolitica and Yersinia-like and 98 percent at 30°C for Y. enterocolitica and microbes isolated from mammals and water in Norway and coliforms, respectively (Lloyd, personal com- Denmark. Acta Pat hologica et Microbiologica munication). Scandinavica: Section B: Microbiology and Immunology, 85, 129-135. Kendall, M. and Gilbert, R. J. (1980). Survival and growth of Yersinia enterocolitica in broth media and in food. In Inactivation by Night Soil and Sludge Microbial Growth in Extreme Envlironments, pp. 215-226. Treatment Processes Technical Series 15. London: Society of Applied Bacteriology. No information is available on the destruction of Y. Lassen, J. (1972) Yersinia enterocolitica in drinking water. enterocolitica by night soil and sludge treatment Scandinavian Journal of Infectious Diseases, 4, 125-127. enterocssesortica bye nightrence soiltand sludgeni n t nt Mollaret, H. H. (1976). Contribution to the epidemiological processes or onsthe occurrence oflthisorganism inenight study of Yersinia enterocolitica infections. III. Provisional soil and sludge. Available laboratory techniques are still summing-up of facts. Med ecines et Maladies Infectieuses, 6, inadequate for this type of investigation. 442-448. Morris, G. K. and Feeley, J. C. (1976). Yersinia enterocolitica: a review of its role in food hygiene. Bulletin of the World Health Organization, 54, 79-85. Literature Cited Saari, T. N. and Quan, T. J. (1976). Waterborne Yersinia enterocolitica in Colorado. Abstract Cl 19. Abstracts of the Caprioli, T. Drapeau, A. J. and Kasatiya, S. (1978) Yersinia Annual Meeting of the American Society of Microbiology. enterocolitica: serotypes and biotypes isolated from Washington, D.C. humans and the environment in Quebec, Canada. Journal Schiemann. D. A. (1978). Isolation of Yersinia enterocolitica of Clinical Microbiology, 8, 7-11. from surface and well waters in Ontario. Canadian Journal Dominowska, C. and Malottke, R. (1971). Survival of Yersinia of Microbiology, 24, 1048-1052. in water samples originating from various sources. Bulletin Schillinger, J. E. and McFeters, G. A. (1978). Survival of of the Institute of Marine Medicine in Gdansk, 22, 173-182. Escherichia coli and Yersinia enterocolitica in stream and Eden, K. V., Rosenberg, M. L., Stooper, M., Wood, B. T., tapwaters.AbstractN79.AbstractsoftheAnnualMeetingof Highsmith, A. K. Skaliy, P., Wells, J. G. and Feeley, J. C. the American Society of Microbiology. Washington, D.C. (1977). Waterborne gastrointestinal illness at a ski resort: Wakelee, A., Macleod, K. I. E., Mellon, W., Moldt, M., Paul, isolation of Yersinia enterocolitica from drinking water. L., Bacorn, R. W., Lyman, D. O., Medvesky, M., Shayegani, Public Health Reports, 92, 245-250. M. and Toly, M. H. (1977). Yersinia enterocolitica outbreak Fukushima, H., Ito Y., Saito, K., Tsubokusa, M. and Otsuki, in New York. Morbidity and Mortality Weekly Report. 26, K. (1979). Role of the fly in the transport of Yersinia 53-54. Section III. Excreted Protozoa Chapter 19 Balantidium and Balantidiasis. 20 Entamoeba histolytica and Amebiasis. 21 Giardia and Giardiasis. 19 Balantidium and Balantidiasis THREE PROTOZOAL INFECTIONS of the human cystitis have also been observed. An inadequate diet intestinal tract are described in this book. Two of them, may exacerbate the pathogenesis. Death may occur amebiasis due to Entamnoeba histolytica (chapter 20) through the development of extensive ulceration and and giardiasis due to Giardia lamblia (chapter 21), are gangrenous changes, and may result from hemorrhage of major public health importance in many countries. and dehydration. Reports of mortality range from 5 to The third, balantidiasis due to Balantidiutm coli, is 35 percent among clinical cases in the tropics. relatively rare and is included for completeness. Two Treatment is by antibiotics, particularly tetracycline or others about which little is known, isosporiasis due to ampicillin. Isospora belli and sarcocystiasis due to Sarcocystis Diagnosis depends on demonstrating the character- species, are also rare as significant diseases of man and istic Bal. coli trophozoites or cysts in the stools. The are omitted from this study. Also omitted are the stool examined should ideally be fresh, but cysts and, nonpathogenic and rarely pathogenic amebae, and under favorable conditions, trophozoites can be some flagellates of no public health importance. detected in fecal material preserved in 5 percent formol-saline. Description of Pathogen and Disease Occurrence Balantidiasis is a little-studied infection, and theefoe te fllwin setios lckmuc ofthedetil This infection, although rare, is found worldwide, iserefoun thefollowingterchates lackmuchofthedetai most commonly in the tropical and subtropical zones that is found in other chapters. (Arean and Koppisch 1956). In areas where sanitation is poor and where pigs associate closely with man, Identification prevalence of infection may exceed 20 percent. Bal. coli infects all ages, with the highest prevalence in endemic Balantidiasis is an infection of the large intestine by areas occurring among teenagers and adults. the ciliate protozoon, Balantiditum coli. In many infections (perhaps 80 percent) Bal. coli lives as a commensal in the lumen of the colon and causes no symptoms. Less frequently invasion of the colonic fe mucosa takes place, giving rise to a disease known as Bal. coli is the only parasitic ciliate of man. It is a balantidial dysentery. Sufferers may present with flattened oval organism covered with cilia, with a gullet diarrhea. sometimes bloody, and abdominal discom- at the anterior end (figure 19-1). The trophozoite is fort. The colonic lesions are grossly similar to those of 30-170 micrometers long by 25-120 micrometers amebic dysentery, but may reach the lymphatic vessels broad. As in Entainoeba infection, cysts are found in the deep in the intestinal wall. The parasites may then large intestine and passed in the formed stool. The cysts penetrate to the regional lymph nodes, where a mild are ovoid or spherical and measure 45-65 micrometers reaction occurs. Hematogenous spread to distant in diameter. The trophozoite also may be an infective organs does not occur, in contrast with Enta7noeba stage; it can live several days outside the host histolvtica, but Balantidiumn may attack the terminal (Svensson 1955) and can withstand passage through ileum and also cause acute appendicitis. Vaginitis and the guinea pig stomach. 333 334 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA relevant in this context. Sewer rats (Rattus norvegictus) are susceptible to infection with Bal. coli from man, pigs, or wild rats but are most susceptible to rat strains. =7 ,, 4 4 W.t i ; - Transmission 5 'il t-. .I w i;;--It is assumed that the cyst of Bal. coli is the im- %,. . fs[.......>,'portant resistant stage involved in transmission. Contamination of food, drinking water, and utensils by feces of pigs and., probably more important, by fecal material from persons carrying the infection, as well as direct fecal-oral contact appear to be the main modes of transmission. The same comments on transmission *-f - f,a -, . made for Ent. histolvtica (chapter 20) apply here, . ' L :-1: , o).. R 0though fewer cysts are produced per infected person in balantidiasis, and the proportion of infected persons producing cysts is also lower. Thus the incidence of Bal. " '" '' < ed y""'< ' > ' 'K'';o -coli is probably lower than that of Ent. histolytica. An I S ~ .g'- wVXj @;,-,CF . - * \ early report suggests that the trophozoite is capable of passing the stomach barrier, so that acute cases, not producing cysts, could possibly be infective to people 'r 'Fp- ' ' ';' / closely associated with them. However, other work has suggested that trophozoites are highly sensitive to pH , T ,.-, ,( values below 5. The median infective dose (ID50) is not e _________ known, asman hasnot beensuccessfullyexperimentally infected (Young 1950). It may well be comparable to Figure 19-1. Drawing of a trophozoite of Balantidium that of Entamoeba and Giardia: 10-100 cysts (chapters coli. Scale bar = 10 micrometers. (From: Wenyon, C. 20 and 21). M. (1926). Protozoology, vol. 2. London: Bailliere, Tindall and Cassel. Reproduced by courtesy of the publishers) Prepatent and incubation periods Because man has not been infected experimentally Reservoirs and detailed epidemiological studies are lacking, the prepatent and incubation periods are not known. Balantidiasis is a zoonosis. Many mammals are naturally infected, but it is the pig, and to a lesser extent the rat, that act as the main reservoirs for human Period of communicability infection (Awakian 1937; Ayeni 1973; Letonja and others 1975; Misra and others 1972). Prevalence The disease is communicable for as long as the among pigs is typically 50-100 percent, with 80 percent infection persists, although cysts are not often found in of pigs in the UK infected (Knight 1978). The majority the stool. A 5-year history of chronic diarrhea, revealed of cases have a history of contact with pigs, but cases do as balantidial dysentery, has been described in one occur in Moslem countries such as Iran. It is possible patient in Northern Ireland (Kennedy and Stewart that only certain animal strains can infect man and 1957). then only under particular conditions of host susceptibility. Human strains will infect experimental Resistance animals including apes, pigs, cats, rodents, and guinea pigs (for instance, Westphal 1971), but it has not yet Man appears to be a very resistant host. High proved possible to infect man experimentally with cysts prevalences of balantidiasis are found only in the of human, simian, or porcine strains. Bal. coli has also exceptional circumstances of close contact with pigs. been found in wild rats, and some human infections are Attempts to infect man with cysts experimentally have thought to be derived from this source. The almost so far failed. Disease may occur only when there is universal association of rats with domestic pigs may be malnutrition or intercurrent infection. BALANTIDI UM AND BALANTIDIASIS 335 Epidemiology Walzer and his colleagues considered that the Balantidiasis is extremely rare in many countries, balantidiasis outbreak occurred because the in- and its epidemiology is not well described. An endemic habitants used ground and surface water supplies, and ts eidemoloy isnot elldescibed Ancontaminated by pigS, after their relatively clean focus has been reported from the Seychelles (Nuti, de Comarmond and de Bac 1980). sources of water were destroyed by the typhoon. Most epidemiological data come from Papua New Guinea and Irian Jaya (Indonesia). Balantidiasis in the highlands of both countries is common due to the Control Measures practice of keeping, and often living with, large herds of domestic pigs (Bayliss Smith and Feachem 1977; Balantidiasis is not a major public health problem, Feachem 1973). Human prevalences in different and its control has not been studied. All the comments communities in Papua New Guinea range from 2 to 29 made about amebiasis and giardiasis control (chapters percent and are twice as high in females as in males 20 and 21) may apply to balantidiasis control. (Radford 1973). This is due to the fact that pigs sleep in the "women's houses" with the adult females and children. In the mountains of Irian Jaya, balantidiasis Individual is especially prevalent where domestic or semidomestic Mass chemotherapy has not been tried, and there is pig populations are high and where altitude and harsh no vaccine. Individual protection may be achieved by climate create a greater need for pigs to shelter in personal and domestic cleanliness and by care in the human houses at night (Couvee and Rijpstra 1961; van choice and preparation of drinking water and der Hoeven and Rijpstra 1957). vegetables. Pig farmers may be especially at risk. Following a typhoon in May 1971 there was an outbreak of balantidiasis involving 110 persons on Truk (Caroline Islands; Pacific Islands Trust Environmental Territory) described by Walzer and others (1973). The A single study in Venezuela showed that preschool patients presented with gastrointestinal symptoms, children in houses with inside water and washing and there was no serious morbidity. Both tetracycline facilities had a balantidiasis prevalence of 4 percent, and metronidazole were used in treatment, but there whereas those in other houses had a prevalence of 9 was no evidence that either was effective. The epidemic percent (van Zijl 1966). Confounding socioeconomic terminated spontaneously in early July. In 1970 there variables were not controlled. had been 410 cases of amebiasis and 4 of balantidiasis. The importance of hygienic excreta disposal to Before the typhoon in 1971 there had been 1 case of prevent transmission of the cysts directly to other balantidiasis. During the outbreak the youngest case individuals is accepted. Equally important is the was 2 months old and the oldest 70 years. Highest hygienic disposal of porcine excreta, and its separation rates of attack were noted in the 1-4, 30-39, and 50 59 from human food. Personal and domestic cleanliness, age groups, indicating that the source of transmission encouraged by adequate water supplies and strenuous was something common to all age groups. hygiene education, are essential. Where cultural and The 30,000 people of the Truk archipelago (119 farming norms cause the cohabitation of people and square kilometers) lived in overcrowded conditions, pigs, as in some parts of Papua New Guinea, the often 15 persons per household. Privies discharging control of balantidiasis may be impossible. into the lagoon were shared by several families, and there was indiscrimate defecation by children around the houses. Pigs were kept by most householders, and Bal. coli was found in the fresh feces of four of six pigs Occurrence and Survival in the examined. During the typhoon most of the houses in Environment Truk were destroyed, together with their roof-water catchment systems, and this led to a reliance on wells There is no information on Bal. coli cysts in the and streams highly contaminated with pig feces. Cases environment. It may be assumed that in most moist of balantidiasis occurred almost simultaneously in environments their survival is dependent on time and widely separate areas, where the only common factors temperature and is similar to that of Ent. histolytica were the occurrence of the typhoon, the presence of cysts (see figure 20-2). They are rapidly killed by pigs, and reliance on the roof-water catchment systems. desiccation. 336 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA Inactivation by Sewage Treatment dysentery: a human case in Northern Ireland. Transactions Processes otrhe Royal Society of Tropical Medicine anid Hygiene, 51, 549-558. No specific information has been reported. The cysts Knight, R. (1978). Giardiasis, isosporiasis and balantidiasis. of Bal. coli are appreciably larger than those of Ent. Clinics in Gastroenterology, 7, 31-47. Itistolytica and are likely to settle more rapidly (no Letonja, T., Henriquez, A., Reyes, G. and Zapata. L. (1975). likormatonhas elyfoundondensity). O eraidy it Prevalence of Balantidium1l coli infections in swine from information has been found on density). Otherwise it Santiago. Chile. Boletin Chilena de Parasitologia. 30, may be assumed that Bal. coli cysts in sewage treatment 88- 89. respond like Ent. histolytica cysts (chapter 20). Misra, S. C., Das, D. N., Patnaik. K. C. and Mohapatra. H. C. (1972). Incidence of gastrointestinal parasites in pigs with evaluation ofan effective technique for the recovery of their Inactivation by Night Soil and Sludge ova or cysts in the faeces. Indian Veterinarv Journal, 49, Treatment Processes 140-145. Nuti. M., de Comarmond. C. and de Bac, C. (1980). An No specific information has been reported. It mav be endemic focus of balantidiasis in the Seychelles islands. assumed that Bal. coli cysts in night soil and sludge Abstract18.AbstractsofthelOrb InternationalCongresso ,in the same way as Er. Tropical Medicine an7cd Malaria. Manila, Philippines. treatment processes responde 20w. Radford. A. J. (1973). Balantidiasis in Papua New Guinea. ilcedical Jouirnal of .4Australia. 60, 238-241. Svensson. R. 1955). On the resistance to heating and cooling of Balantidiurn coli in culture, and some observations Literature Cited regarding conjugation. Experimilenital Parasitology. 4, 502- 525. Arean,V.M.andKoppisch,E.(1956).Balantidiasis.Areview van der Hoeven, J. A. and Rijpstra, A. C. (1957). Intestinal and report of cases. American Joturnil of Pathology, 32, parasites in the central mountain district of Netherlands 1089-1115. New Guinea. An important focus of Baianiidiumn coli. Awakian,A. (1937). Studiesontheintestinal protozoaofrats. Documenta de Medicina Geograplhica et Tro pica. 9, II. Rats as carriers of Balantidiuyn. Tranisactions oj' the 225_228. RoYalSocietyof]'Tropical MedicineandHYgiene, 31. 93-98. van Zijl. W. J. (1966). Studies on diarrhoeal diseases in seven Ayeni. A. 0. (1973). Internal parasites of livestock in the countries by the WHO Diarrhoeal Diseases Advisory Team. Western State of Nigeria. 1. Helminth parasites of pigs. Bulletin of the World Healt1z Organiiation, 35. 249- 261. \Nigerian Agriculltur7al Journual, 10, 43-45. Walzer, P. D., Judson, F. N., Murphy. K. B., Healy, G. R., Bavliss Smith, T. P. and Feachem, R. G. (1977). Subsistence English, D. K. and Schultz. M. G. (1973). Balantidiasis and Surirail: Rural Ecology in tlze Pacific. London: outbreak in Truk. American Journal i - .f...' Medicine Academic Press. and Hygiene, 22. 33-41. Couvee, L. M. J. and Rijpstra, A. C. (1961). The prevalence of Westphal, A. (1971). Experimental infection of mice and Balantidiumiii coli in the central highlands of western New guinea pigs with Balantidiuma coli. Z.-,. . Jiir Guinea. Tropical and Geographical Medicine, 13, 284-286. Tropenmedizin ulnd Parasitologie. 22, 138-148. Feachem, R. G. (1973). The Raiapu Enga pig herd. Manzkinzd. Young, M. D. (1950). Attempts to transmit human 9. 25 31. Balantidiumn coli. Amnerican Journial oJ Tropical Medicine. Kennedy, C. C. and Stewart. R. C. (1957). Balantidial 30, 71- 72. 20 Entamoeba histolytica and Amebiasis THERE ARE TWO MAIN forms of dysentery. Bacillary extraintestinal amebiasis the intestinal infection may dysentery caused by infection with Shigella bacteria have been lost and serological tests are used. (chapter 16) and amebic dysentery caused by infection The degree of morbidity resulting from infections with the protozoon Entamoeba histolytica. Amebic with Ent. histolytica is hard to assess, but seropositivity, dysentery is the subject of this chapter. taken as an index of active invasion, is found in 40 percent or more of asymptomatic carriers in endemic areas. The incidence of liver abscess is related to the length of time an intestinal infection has been present; Description of Pathogen and Disease frequent infection extends the period and makes abscess development more likely. The ingestion of Amebiasis may describe an infection by any of the dietary hepatotoxins, alcohol, nutritional deficiencies, amebae some of which are parasites and live in the and the presence of other parasites may all play a part gut and some of which are free living and occasionally in the development of active invasion by a potentially infect man. In this book, however, amebiasis describes invasive amebic strain. Reports of case mortality vary only the infection of man by Ent. histolytica. from 0.02 to 6 percent in different countries (Elsdon- Dew 1968). Recent evidence of strain variation based Identificationi on isoenzyme typing suggests marked differences in pathogenicity, and many of the previously intractable Ent. histolytica is primarily a parasite of the large questions of the epidemiology of serious amebic intestine. Symptoms, when present, consist of diarrhea, disease can now be reopened. sometimes bloody, and mild pyrexia, with or without abdominal pain. Trophozoites (vegetative forms) of an invasive Ent. histolvitica erode the epithelial lining of Occurrence the colon and colonize the submucosal tissues, forming Amebiasis is found associated with insanitary ulcers. Migration of amebae from ulcers may take conditions in all parts of the world. World prevalence place via the hepatic portal vein to the liver and other has been estimated at 10 percent, and, although it is organs, where an amebic abscess may develop. The unusual for it to exceed 30 percent, rates of up to 80 typical hepatic abscess is in the right lobe of the liver, percent or more have been reported in some resulting in pain and swelling in that area. The abscess communities. (Mistaken identification of Ent. har- may burst into the pleural cavity and lung. Cutaneous tmanni as Ent. histolytica has led in some cases to falsely amebiasis may develop around the anus or an abscess high prevalence values.) fistula. In general, in severe cases of amebiasis, pyrexia, sweating, a raised erythrocyte sedimentation rate, and slightly raised neutrophil white cell count occur. If Injectious agent there is hepatic involvement, liver function tests may Ent. histolytica is the dysentery ameba of man. The show abnormalities and obstructive jaundice may trophozoite is about 20-25 micrometers in diameter, develop. Diagnosis of intestinal amebiasis is primarily generally elongated, and lives in the lumen of the large by direct demonstration of hematophagous tro- intestine (commensal phase) or in the gut wall (invasive phozoites in the diarrheic stool, or of the typical 1-4 phase) (fig. 20-1). It is generally agreed that some nucleate cysts in the formed stool. In cases of strains of Ent. hlistolytica are more virulent than others, 337 338 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA dogs and cats and has been transmitted experimentally to many mammalian species. : . . Transmission - W -,} ^ An asymptomatic infected individual is estimated to produce 1.5 x 107 cysts per day in the stool. A variable proportion of these are mature quadrinucleate cysts, r- 7 j {and these are apparently the only ones capable of further development in a new host. Little further maturation of cysts takes place after they have left the Fiw body. The trophozoite of Ent. histolytica is not of importance in the transmission of the disease, since it dies rapidly on exposure to air and cannot survive passage through the normal stomach. The cystic stage is produced in the intervals between active bouts of dysentery, and it is the convalescent or asymptomatic carrier, producing cysts, who is usually responsible for transmission. When viable cysts are ingested, in water, Figure 20-1. A trophozoite oj Entamoeba histolytica on food, or directly from fecally-contaminated hands, tinder scanning electronmicroscopy. The organism is they hatch in the intestine and produce an infection adhered to a monolayer of human intestinal epithelial that may or may not develop invasive characteristics cells. Scale bar = 10 micrometers. (Photo: D. and give rise to symptoms. Mirelman, Department of Biophysics, Weizmann Infections of Ent. coli in man have been produced Institute of Science, Rehovot, Israel) after the ingestion of a single cyst, but the median infective dose for this organism appears to be between and also that by "adaptation" (selection) it is possible 10 and 100 cysts (Rendtorff 1954; Rendtorff and Holt for virulence to increase or decrease. The cystic 1954b). In experimental Ent. hlistolytica infections in resistant stage of Ent. histolytica is produced in the man, infections were consistently produced by inocula lower parts of the large intestine. The cyst is spherical of 2,000-4,000 cysts. and ranges from 10-15 micrometers in diameter. The ameba Ent. hartmanni, which used to be called the iismall race" of Ent. histolytica, has trophozoites much Prepatent and incubation periods smaller than those of Ent. histolytica and cysts less than The median prepatent period in experimental 10 micrometers in diameter. It is now recognized that infections of man with Ent. histolytica is 5 days. For Ent. hartmanni is not pathogenic. Ent. coli, an ameba Ent. coli the prepatent period ranged from 6-22 days closely related to Ent. histolytica, is not pathogenic and (mean 10 days) in one study (Rendtorff 1954) and 4-14 has cysts ranging in diameter from 14-20 micrometers. days (mean 8 days) in another (Rendtorff and Holt This organism has been used in some epidemiologic 1954b). studies as an alternative to Ent. histolytica. Ent. The median incubation period in the 1933 Chicago moshkouskii is a free-living organism, found in sewage, outbreak was 21.4 days. Other reports indicate that the whose trophozoites and cysts are morphologically incubation period is 2-6 weeks. In extraintestinal identical to those of Ent. histolytica. In culture it can be amebiasis the incubation period may be years. distinguished because it is capable of growing at Development of amebic abscess is thought to follow temperatures from 25 to 37°C. Ent. histolytica will not the action of some precipitating factor, possibly liver grow at 25°C. damage due to hepatotoxins or alcohol. Reservoirs Period of communicability The reservoir of Ent. histolytica is man, although the As long as a chronic infection is present in the gut, organism is harbored by primates and there are the cysts continue to be detectable in the stool. The instances where transmission from primates to man median duration of untreated intestinal infections in may have occurred. Ent. histolytica is also found in man is about 2 years. ENTAMOEBA HISTOLYTICA AND AMEBIASIS 339 Resistance A major study on the epidemiology of amebiasis was Susceptibilit to infection wit histolytica reported from the Gambia (Bray and Harris 1977). Susepibiit t inecio wih nt Twenty-six villages throughout the country were appears to be general, although there may be cultural . . . t c w and racial factors affecting morbidity. Humoral visited in the dry season, and single stool samples were antibodies are produced in response to tissue invasion collected from fifty persons in each village. In all ages by amebae. These may be detected by indirect and villages, infection rates were 36 percent among hemagglutination, fluorescent antibody, or immuno- both sexes, 26 percent among males, and 45 percent precipitin techniques. Various aspects of cell-mediated among females. A longitudinal survey over 2.5 years in immunity have also been demonstrated. The steady one district showed prevalences falling to around 15 loss of intestinal infections, with a median duration of 2 percent at the end of each dry season (April-May) and years, suggests that some of the acquired immune at the end of each wet season (October). Peak ' . . . . ~~~~~~~~prevalences (30-> 50 percent) occurred early in the response is protective. Information on the protective pdry season (January and at the start of the rains e o r ti ck (June-August). Of individuals followed throughout the 2.5-year survey, 98 percent passed cysts on one or Epidemiology more occasions. Combining both surveys, prevalence rates by age rose steadily from 2 percent in 0-1 year Amebiasis occurs throughout the world and is more olds to 35 percent in those over 40 years. Many samples prevalent in poor communities with inadequate of water, hand washings, fingernail clippings, soiled sanitation. There is no simple correlation, however, clothing, houseflies, lettuce, and soil were examined, between levels of sanitation or economic development but only one sample of well water yielded Ent. and the prevalence of amebiasis. Considerable histolytica. The authors concluded that "the lack of unexplained variations in prevalence exist, even within success in our attempts to elucidate the transmission a small geographical area. pathway was remarkable." They found some evidence As with other common enteric parasites, the pattern of clustering of infection by compound and suggested of infection is typically endemic. A poor community that defecation by small children around the houses may have a substantial proportion of asymptomatic could be the major mode of transmission within the carriers continuously contaminating the environment compound. As mothers, and older female siblings, with Ent. histolytica cysts. Over 80 percent of infected are responsible for the care of small children, this might persons may be asymptomatic. Recorded prevalences explain the higher infection rates among females. of Ent. histolytica cyst excretion in various com- Endemic amebiasis is found in temperate developed munities include 3-47 percent in India, I 1 percent in countries as well as tropical developing countries. The Lagos (Nigeria), 7 percent in Bangkok (Thailand), 50 carrier rate in the UK is 2-5 percent, with an estimated percent in Medellin (Colombia), and 72 percent in San 300 hospitalized cases and 3 deaths per year (WHO Jose (Costa Rica) (WHO Scientific Working Group Scientific Working Group 1980). Many of the clinical 1980). cases of amebiasis seen in developed countries are Prevalences of Ent. histolytica cyst excretion among associated with infection while traveling abroad. The healthy children 1-5 years old in Guatemala were 18 Ent. histolytica carriage rate in the USA is estimated as percent of rural children, 6 percent of "low social 3-4 percent overall, but may be closer to 40 percent status" urban children, and 1 percent of "high social among adult, male homosexuals (Jones 1979; status" urban children (Pierce and others 1962). A Schmerin, Gelston and Jones 1977). Within developed longitudinal study of forty-five children from birth to 3 countries, prevalences of Ent. histolytica infection are years of age in a Guatemalan village showed that 82 higher among the lower socioeconomic groups and percent had had one or more Ent. histolytica infections among disadvantaged ethnic groups-for instance before their third birthday (Mata and others 1977). A Indians and Eskimos in North America (see, for survey in Egypt showed a 16 percent prevalence of cyst instance, Melvin and Brooke 1962; Sole and Croll excretion amrong students (15-20 years old) in the Nile 1980). Amebiasis is also especially common in mental Delta and 11 percent among similar students from hospitals (Jeffery 1960; Sexton and others 1974). Upper Egypt (Arafa and others 1978). Ent. histolytica In addition to the endemic picture of amebiasis cyst excretion rates among healthy preschool children described above, outbreaks also occur. The best (0-6 years) were 4 percent in Sri Lanka, 15 percent in documented of these are in developed countries, for Iran, 6 percent in Bangladesh, and 11 percent in instance in Chicago (USA) in 1933 and Indiana (USA) Venezuela (van Zijl 1966). in 1950, and many of these outbreaks have been 340 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA waterborne (Brooke and others 1955; LeMaistre and information on the seasonality of amebiasis or on the others 1956; Morton, Stamm and Seidelin 1952). important routes of transmission in poor communities. Supposed waterborne outbreaks have occurred among The relationship and comparative epidemiology of persons using chlorinated water supplies, and it is commensal or lumenal amebiasis (the parasite living in suggested that the chlorine levels were able to destroy the lumen of the colon, with no evidence of invasion or the fecal bacteria but not all the amebic cysts. disease) and invasive or pathogenic amebiasis remain Outbreaks in poor communities having endemic unclear, and research is in progress (for instance, amebiasis are unlikely. Sargeaunt and others 1980). For informative reviews, The role of water contaminated by sewage has been see Elsdon-Dew (1968, 1978) and Knight (1975). clearly established in some outbreaks of amebiasis. The major transmission routes in endemic areas remain uncertain, however. Direct fecal-oral transmission from Control Measures person to person under conditions of poverty, over- crowding. and inadequate water supply and sanitation Both individual and environmental approaches to is the most likely mechanism. Several studies have amebiasis control may be adopted. although only an pointed to family clustering of infection and intra- environmental approach can have lasting and familial transmission; for instance, Bray and Harris community-wide benefits. (1977) in The Gambia, Engbaek and Larsen (1979) in Denmark, Mathur and Kaur (1972a) in India, and Nnochiri (1965) in Nigeria. This last study. in Lagos, found that 96 percent of healthy mothers of sick There are several effective drugs for thc treatment of children with amebiasis had Ent. histozlytica infections. intestinal amebiasis. most of which are without serious All the children and some of the mothers were treated. toxic hazards at the recommended dosage. Mass Six months later the prevalences of amebiasis among chemotherapy has been applied with success and the treated children were 14 percent of those with results in a rapid reduction in prevalence. In the long treated mothers and 40 percent of those with untreated term. a mass chemotherapy program is unlikely to be mothers. Person-to-person transmission has also been effective, unless frequently repeated, without concom- strongly implicated in the USA by studies on mental itant improvements in sanitary education. excreta institutioins (Jeffery 1960; Sexton and others 1974), on disposal, and probably also improved water supplies. a village in Arkansas (Spencer and others 1976), and on There is no vaccine. an extended Spanish-American family in Texas Drug prophylaxis is not considered desirable. For (Spencer and others 1977). individual prophylaxis, the treatment of drinking water The contamination of food, especially salad by boiling-coupled with the treatment of vegetables vegetables, is probably of some importance in with strong vinegar, iodine solutions, or hot water--is transmiiissioni to higher socioeconomiiic groups in urban recommended. Personal and domestic cleanliness are areas. This type of transmission may also be essential to prevent intrafamilial spread. responsible for a considerable proportion of infection among tourists and travelers. Foodborne transmission EinLirownnental can be caused both by the contamination of crops by the use of night soil as a fertilizer and by the Eat. histolytica excretion has been used as an index contamination of food by infected food :,l-, .iI .l of excreta-related or water-related (or both) infection iSchoenleber 1940). in several studies on the relationships between health Some studies suggest that insect vectors, such as and environmental sanitation. Some of these studies cockroaches and flies, play a role in mechanically are summarized in table 20-1 and more details are transporting cysts in their guts and in contaminating given in table 2-1. Studies in India and the USA-- food with their feces and vomitus (Frye and Meleney Arkansas (twvo studies). Georgia. North Carolina, 1936; Gupta and others 1972; Pipkin 1949: Rendtorff Tennessee and Texas -suggested that excreta disposal and Holt 1954a: Root 1921). However, the epide- facilities were related to amebiasis prevalence, whereas miological importance of insects in transmitting studies in Costa Rica and Egypt suggested they were amebiasis is uncertain. not. Studies in Costa Rica, Japan, Arkansas, and North Theoretically. transmission is likely to be greatest in Carolina suggested that water supplies were associated the wettest and coolest season, when cysts are most with amebiasis prevalence, whereas studies in able to survive outside the gut. There is very little Denmark. Egypt, Arkansas, Tennessee, and Texas ENTAMOEBA HISTOL) I ICA AND AMEBIASIS 341 Table 20-1. Some studies on the relationiships betwveen Entamoeba histolytica inJfction and environmental sanitationz Country Finding Source Costa Rica Prexalence of amebiasis was betw cen 6 and 17 percent tn 6 areas Moore, de la Cruz and Vargas- studied; no relationship between amebiasis prevalence and etther Mendez (1965) rental value of house or sanitation facilities; association of amebiasis with one source of piped water Denmark Ent. coli infection was associated with lower socioeconomic status Engbaek and Larsen (1979) but not with water supplies Egypt Improved water supplies, bored-hole latrines, refuse disposal, and Chandler (1954) preventive work by visiting nurses failed to reduce the prevalence of protozoal infections (Ear. histolrtic--- 57 percent) or the mean number of infections per person (2.3) India Family contacts of amebiasis patients were surveyed: prevalences Mathur and Kaur (1972b) of Eiat. hlistolvtica excretion were 32 percent of those with latrines and 38 percent of those without: the lack of a latrine was associated with a generally poor domestic environment Japan Type of water supply was believed to be an important determinant Wykoff, Fonseca and Ritchie of Ea,r. histolytica prevalence (1955) and Wykoff and Ritchie (1960) USA (Arizona, Dakota. Prevalence of Eat. histolytica among Indians was 15 percent and Melvin and Brooke (19621 Montana, New Mexico, was related to crowding and Wisconsin) USA (Arkansas) Prevalence of protozoal infection Aas lower (13 percentj among Brooke and others (1963j small children living in houses with indoor water and sewerage than among those with well water and no sewerage (37 percent) Ent. hiistrOlrtico prevalence among blacks was related to crowding Spencer and others (1976) and lack of indoor toilets. but not to water quality USA (California) The prevalence of Eat. histolvtica infection among white female Jeffery (1960) mental patients rose from 10 to 39 percent over a 3-year period during which they were transferred to a much more hygienic new building USA (Georgia) Ent. histoNltica infection among patients at a veterans' hospital was Brooke, Donaldson and Brown associated with having an outside latrine but not with income 1954) USA (North Carolina) Ent. histolytica prevalences among schoolchildren were associated Mackie and others (1956) with sanitation facilities, type of water supply. and garbage disposal USA (Tennessee) Eat. Iistolx'tica prevalences among rural blacks were associated Eyles, Jones and Smith (1953) with sanitation, family size, fecal contamination of the home and cleanliness but not with water pollution USA (Texas) Ent. hiistolitica prevalence in a Spanish American extended family Spencer and others (1977) was related to lack of an indoor toilet but not to water supply suggested they were not. Most of the studies failed to halving the hypothetical "transmission constant" by control the numerous confounding variables or to improvements in hygiene will ensure the virtual disentangle the effects of income, education, water, disappearance of amebic infection, but this will take sanitation, and housing. The situation is therefore time. This point should be remembered in assessments confused. of the effect of improvements in excreta disposal alone Improvements in excreta disposal and other sanitary on prevalence of amebiasis. facilities are likely to have little short-term effect on Untreated night soil should not be used to fertilize prevalence, but over a decade a marked effect should be vegetables and fruit destined to be eaten raw, and all detectable. Mass chemotherapy combined with im- night soil application should be halted about a week provements in excreta disposal would enable the before harvesting. Polluted water should not be used to lowered prevalence due to the former to be maintained. freshen the vegetables before sale. According to the mathematical model of Knight The importance of education of the general (t975), in a population where prevalence is 50 percent, population, and especially mothers and food handlers, 342 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA in the basic principles of hygiene cannot be In seawater overestimated. It is also likely that, despitc improve- Entamoeba histolytica cysts are not affected by salt ments in water supply and sanitation, indiscriminate concentrations encountered in seawater, and survival defecation by small children around houses, and by may be expected to be as in fresh water (Dobell 1928; workers in agriculture, can still lead to an appreciable Kheissin and Dmitrieva 1935). amount of transmission. Occurrence and Survival in the Injfeces and niglit soil Environment Cysts will frequently be present in feces and night soil, as suggested by the high prevalence rates discussed Despite the high prevalence of excretion of amebic above in the section on epidemiology. cysts in many communities, there is very little Survival in feces will be similar to that in other moist information on their occurrence in the extraintestinal environments (Chang 1955; Simitch, Petrovitch and environment. This is partly because they are difficult to Chibalitch 1954), and may be conservatively estimated detect in water and other environmental samples. As from figure 20-2. In desiccated feces, as with stools most transmission is probably by direct fecal-oral exposed to bright sunshine and warm temperatures, routes within the home, the presence of cysts in the cyst survival will be very much reduced. environment has not attracted much research. Although Ent. histolytica trophozoites are also excreted, they very rapidly die, are not responsible for In sew'age transmission. and thus are of no environmental interest. The sections that follow deal entirely with Ent. histolytica cysts may be expected in sewage but cysts. have seldom been reported. Raw sewage in Denver Eare s (Colorado, USA) contained Ent. coli in 100 percent of morphlogy oriexsion oe esuvina or nutrl redas samples, at an average concentration of 52 cysts per morphology or exclusion of eosin or neutral red as lier NoEt Gitltc yt eefudoigt h criteria of viability. These approaches, although liter. No Ent. hisolytica cysts were found owing tothe generally reliable, are now superseded by cultivation as low prevalence of amebiasis in Colorado (Wang and a test of viability. Dunlop 1954). The survival of Ent. histolytica cysts in sewage In water and water supplies resembles that in water (Chang 1943) and may be estimated from figure 20-2. Waterborne outbreaks of amebiasis have been circumstantially documented, but there have been very few isolations of Ent. histolytica cysts from domestic On surfaces water supplies or from natural surface waters. Where Cysts are killed within 10 minutes by desiccation on human fecal contamination is present, cysts may be the surface of the hands (Spector and Buky 1934), but expected, but their presence has not been documented. they survive for periods up to 45 minutes in fecal The survival of Ent. histolytica cysts in water is teria lor unds up to (Andres 1934ca dependent on temperature and not on water quality. Survival times at various temperatures may be conservatively estimated from figure 20-2. In soil Heating water is the simplest method of destroying cysts. As shown in figure 20-2, temperatures of 60°C for Survival of Ent. histolytica in wet soil is as in water 1 minute, or 55°C for 10 minutes, are effective (see also and may be estimated from figure 20-2 (Beaver and Chang 1943; Jones and Newton 1950; Rudolfs, Falk Deschamps 1949a). Survival in dry soil is very much and Ragotzkie 1950). shorter (Rudolfs, Falk and Ragotzkie 1951). Chlorination of water will destroy cysts, but more slowly than fecal bacteria. Cysts may therefore persist in waters that are judged bacteriologically safe. On CrOpS Chlorination is more cysticidal when chlorine is free (at Cysts of Ent. histolvtica are extremely sensitive to a concentration of at least 3 milligrams per liter), at desiccation, with or without the presence of additional lower pH, at warmer temperatures, and with longer organic matter. Crops growing in the field may become contact times (Chang and Fair 1941). Iodine is also contaminated with Ent. histolytica directly, through effective. irrigation with polluted water or night soil, or ENTAMOEBA HISTOLYTICA AND AMEBIASIS 343 60- - 60 ss- ZO7NE -ss5 50 - S sOF - 50 4s- s ss X X ~~~~~SAFETY_4 40 - SS---- 40 35 - 'A s - 35 > 25- x x x ' -25 15- -~~~~~~~~~~~~x15 15- | ^.100%/o destruction, of Ent.histolyticc cysts 10 5- X - 5 0 ~~~~~~~~~~~~~~~~~~~~~~~~~~~~0 10 1 o00 I 1000 10000 Irrin Ihour Idoy lweek Imooth lyear TIME (HOURS) Figure 20-2. The influence of time and temperature on Ent. histolytica cysts. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death indirectly, through contact with the polluted soil environments Ent. histolytica cyst survival may be containing cysts. Three days of dry weather kill cysts estimated directly from figure 20-2. on the surface of vegetables (Rudolfs, Falk and Ent. coli is considerably more resistant to Ragotzkie 1951). In hot, dry climates, survival times desiccation than Ent. histolytica (see Reardon, Verder may be less than 1 day. and Rees 1952; Spector and Buky 1934), and this may Vegetables may be decontaminated by soaking in partly explain the considerably higher prevalence of warm water (55°C) or in vinegar or salad dressing the former in most communities. (containing 5 percent acetic acid) for 30 minutes (Beaver and Deschamps 1949b; Chang 1950). Inactivation by Sewage Treatment Summary Processes Cysts are a protected resting stage of the parasite Information on Ent. histolytica in sewage treatment and are remarkably unaffected by their chemical is limited. Sewage treatment processes do not involve surroundings. They can survive a wide range of pH freezing or desiccation, and in a primarily domestic and values and osmotic pressures. They will die rapidly if unchlorinated sewage Ent. histolytica cysts will not dried or frozen. In the absence of desiccation, freezing, experience any strongly cysticidal chemicals. or any specifically cysticidal substance like chlorine or Therefore, survival will be a function of time and acetic acid, their survival depends on temperature temperature and may be estimated from figure 20-2 for (Chang 1943; Chang and Fair 1941). For this reason any given process. the points plotted in figure 20-2 form a smooth curve despite the very variable physicochemical conditions of the experiments. The pattern of points for en- By sedimentation teroviruses (figure 9-2), or even a worm egg (figure 23- Primary and secondary sedimentation remove only 2), show far more scatter, and this indicates the effect of a small proportion of cysts because cysts are small and circumstances other than temperature. In most moist not dense (average diameter 12 micrometers; specific 344 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA gravity 1.06) and so have a very low settling velocity By aerated lagoons (<0.1 meters per hour) (Chang 1945). Pilot-scale aerated lagoon treatment (without Primary sedimentation in Denver (Colorado, USA) secondary sedimentation) in India removed 84 percent halved the concentration of Ent. coli cysts from 52 per of Eit. histolytica cysts (Panicker and Krishnamoorthi liter to 27 per liter. In India, 2 hours of sedimentation 1978ca removed 64 percent of Ent. histolytica cyst, whereas 1.5 ) hours of sedimentation removed only 27 percent (Panicker and Krishnamoorthi 1978). By' tertiary treatment Certain tertiary processes can eliminate Ent. By' trickling filter 1histolytica cysts from secondary effluents. In Haifa (Israel) raw sewage contained 4 Ent. histolytica cysts and 28 Ent. coli cysts per liter (Kott FILTRATIoN. Filtration through sand or suitable soil and Kott 1967). After primary sedimentation and can remove all cysts (Cram 1943; Gordon 1941: trickling filter treatment, these concentrations were Spector, Bayliss and Gullans 1934). reduced to 3 (25 percent reduction) and 16 (43 percent reduction) per liter, respectively. Two complete DISINFECTION. Chlorination of secondary effluents trickling filter plants (including secondary sedimen- was found to eliminate cysts in Haifa (Israel: Kott tation) in India removed 74 and 91 percent of Enit, and Kott 1967), but not in Denver (USA; Wang and histolytica cysts (Panicker and Krishnamoorthi 1978). Dunlop 1954) or Moscow (USSR; Gordon 1941). The results obtained clearly depend on the chlorine dose applied. the quality of the effluent, the contact time, By' actiuated sludge and the temperature. It may be assumed that the The activated sludge process itself will have little effectiveness of chlorine on cysts in effluents is effect on Ent. histolv!tica cysts. The environment is wet considerably lower than on enteroviruses in effluents and not hostile, temperatures are ambient, and (chapter 9). detention times are short (6-12 hours). Cysts may become entrapped in the flocs, in which case they will LAND TREATMENT. Land treatment of secondary be removed during secondary sedimentation. A effluents should theoretically be able to remove all complete activated sludge plant (including secondary cysts. sedimentation) in India removed 83 percent of Ent. histolvtica cysts (Panicker and Krishnamoorthi 1978). Inactivation by Night Soil and Sludge By oxidationz ditch Treatment Processes A pilot-scale oxidation ditch (including sedimen- Night soil and sludge treatment processes do not tation) in India removed 91 percent of Ent. histolY'tica involve freezing. rarelv involve desiccation, and do cysts (Panicker and Krishnamoorthi 1978). n p e not produce environments that are especially or particularly hostile to Ent. histolYtica cysts. Therefore By .aste stabilization ponds cyst destruction is simply a function of time and temperature may be conservatively predicted for Well-operated waste stabilization ponds with any process by reference to figure 20-2. sufficient cells (at least three) and retention time (at least Most mesophilic and all thermophilic sludge and 20 days) produce an effluent completely free of Eiit. night soil treatment processes will eliminate Ent. hisrolytica cysts. A single pond in India, with 7 days histolytica cysts (Cram 1943; Kawata, Cramer and retention, achieved 100 percent reduction (Arceivala Burge 1977). Aerobic thermophilic composting is the and others 1970). Three ponds in India with unknown process ofchoice and will eliminate Ent. Ibistolytica cysts characteristics achieved 87, 94, and 100 percent inlhourat50CC.TheextensivestudiesofScott(1952)in reductions (Panicker and Krishnamoorthi 1978). China demonstrated the effectiveness of aerobic Ponds with 20 days retention in Israel completely composting of feces, manure, and vegetable matter in eliminated Enit. histolvtica cysts (Wachs 1961). eliminating protozoal cysts. E?T4AMOEBA HIS TOLYTIC A AND AMEBIASIS 345 Literature Cited Chang, S. L. and Fair, G. M. (1941). Viability and destruction of the cysts of Endantoeba histolytica. Journal ol thie Andrews, J. (1934). The retention of Endamoeba 1histolvtica Americani Water Works Association, 33, 1705-1715. cysts under finger-nails. Americani Journal of Tropical Cram, E. B. (1943). The effect of various treatment processes Medicine, 14, 439-441. on the survival of helminth ova and protozoan cysts in Arafa, M. S., El-Ridi, A. M. S., Ezzat, H. 0. A. and Makhlouf, sewage. Sewage Works Journlal, 15, 1119-1138. L. M. (1978). A seroparasitological study of Entainoeba Dobell, C. (1928). Further observations and experiments on histolvtica in Egypt. JoUi7'7al of the Egyptian Society of the cultivation of Entatmioeba htistolytica from cysts. Parasitology, 8, 329-332. Parasitology, 19, 288-313. Arceivala, S. J., Lakshminarayana, J. S. S., Alagarsamy, S. R. Elsdon-Dew, R. (1968). The epidemiology of amoebiasis. and Sastry, C. A. (1970). Health aspects. In Waste Advances in Parasitology. 6, 1-62. Stabilization Ponds: Design, Conzstruction and Operation in (1978). Enta/noeba histolytica and Hormo sapienis. India, pp. 87-95. Nagpur, India: Central Public Health Drugs, 15(Supplement 1), 1-9. Engineering Research Institute. Engbaek, K. and Larsen, S. 0. (1979). A comparative socio- Beaver, P. C. and Deschamps, G. (1949a). The viability of E. epidemiological study of families with Giardia lamblia, histolytica cysts in soil. Americani Journal of Tropical Entainoeba coli and Trich1uris trichiura. Ugeskrijt for Medicine, 29, 189-191. Laeger, 141, 1128-1131. (1949b). The effect of acetic acid on the viability of Eyles, D. E., Jones, F. E. and Smith, C. S. (1953). A study of Endamoeba histolytica cysts. American Journal of Tropical Endamoeba histolytica and other intestinal parasites in a Medicine, 29, 193-197. rural West Tennessee Community. Americani Journal of Bray, R. S. and Harris, W. G. (1977). The epidemiology of Tropical Medicine and Hygiene, 2, 173-190. infection with Entanmoeba histolytica in The Gambia. West Frye, W. W. and Meleney, H. E. (1936). The viability of Africa. Transactions of the Royal Society of Tropical Endamioeba histolytica cysts after passage through the Medicine and Hygiene, 71, 401-407. cockroach. Journal of Parasitology. 22, 221 --222. Brooke. M. M.. Donaldson. A. W. and Brown. E. (1954). An Gordon, E. I. (1941). Purification of sewage from cysts of amebiasis survey in a Veterans Administration Hospital. intestinal protozoa. 11. . , . P. Paracitologiya i Chamblee, Georgia, with comparison of technics. Parasitarn1ye Bolezni, 10, 236-243. American JouinaIl of Tropical Medicine and Hvgiene, 3, Gupta, S. R., Rao, C. K., Biswas, H.. Krishnaswami, A_. K. 615-620. Wattal. B. L. and Raghavan, N. G. S. (1972). Role of the Brooke, M. M., Healy, G. R., Levy, P., Kaiser, R. L. and housefly in the transmission of intestinal parasitic Bunch, W. L. (1963). A sample survey of selected areas in cysts/ova. Indian Journal of Medical Research. 60, and near Little Rock, Arkansas. to assess the prevalence of 1120 1125. Entamoeba 1histolvtica. Bulletin of the World Health Jeffery, G. M. (1960). A three-year epidemiologic study of Organization, 29, 813- 822. intestinal parasites in a selected group of mental patients. Brooke, M. M., Melvin. D. M., Sappenfield. R., Payne, F., Americani Journial of Hygienie, 71, 1-8. Carter, F. R. N., Offutt, A. C. and Frye, W. W. (1955). Jones. M. F. and Newton, W. L. (1950). The survival of cysts Studies of a water-borne outbreak of amebiasis. South of Endamiioeha istolytica in water at temperatures between Bend. Indiana. III. Investigation of family contacts. 45°C and 55°C. American Journal of Tropical Medicine, 30, American Journal of Hygiene, 62, 214-226. 53-58. Chandler, A. C. (1954). A comparison of helminthic and Jones, T. C. (1979). Entanmoeba Ihistolytica (amebiasis). In protozoan infections in two Egyptian villages two years Principles andl Practice oj'InJectious Diseases. eds. Mandell, after the installation of sanitary improvements in one of G. L., Douglas, R. G. Jr and Bennett. J. E., pp. 2087-2094. them. American Journal oJ Tropical Medicinie and Hygiene, New York: John Wiley. 3, 59-73. Kawata, K.. Cramer, W. N. and Burge, W. D. (1977). Chang, S. L. (1943). Studies on Enda7noeba histoll7tica. II. Composting destroys pathogens. Water and Sewvage Observations concerning encystation, maturation and Works, 124, 76-79. excystation of E. Imistolytica. and on the longevity of Kheissin, E. M. and Dmitrieva, E. K. (1935). The influence of culture-induced cysts in various fluids and at different salts on the cysts of Entamoeba histoliytica. Trudy temperatures. Jour nal of Infectiouls Diseases, 72, 232-241. Lenin gradskogo Instituta Epidemniologii i Bakteriologii (1945). Sedimentation in water and the specific i7neni Pastera, 2, 22-31. gravity of cysts of Entamoeba histolytica. American Journal Knight, R. (1975). Surveys for amoebiasis: interpretation of oJ Hygiene, 41, 156-163. data and their implications. Annals oJ Tropical Medicine (1950). Kinetics in the thermodestruction of cysts of and Parasitology, 69, 35-48. End7amnoeba histolytica in water. American Journal of Kott, H. and Kott, Y. (1967). Detection and viability of Hygiene, 52, 82-90. Endamoeba hlistolytica cysts in sewage effluents. Water and (1955). Survival of cysts of Endamoeba histul vtica in Sewage WVorks, 140, 177-180. human feces under low-temperature conditions. Am4,erican LeMaistre, C. A., Sappenfield, R., Culbertson, C., Carter, F. Journial of Hygiene, 61, 103-120. R. N., Offutt, A., Black, H. and Brooke, M. M. (1956). 346 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA Studies of a water-borne outbreak of amebiasis, South Attempts to transmit Endamoeba coli and Giardia lamblia Bend, Indiana. I. Epidemiological aspects. American cysts by flies. American Journal of Hygiene, 60, 320-326. Journal of Hygiene, 64, 30-45. (1954b). The experimental transmission of human Mackie, T. T., Mackie, J. W., Vaughn, C. M., Gleason, N. N., intestinal protozoan parasites. IV. Attempts to transmit Greenberg, B. G., Nenninger, E. S., Lunde, M. N., Moore, Endamoeba coli and Giardia lamblia cysts by water. L. L. A.. Kluttz, J. and Taliafero, M. 0. (1956). Intestinal American Journal of Hygiene, 60, 327-338. parasitic infections in Forsyth County, North Carolina. Root, F. M. (1921). Experiments on the carriage of intestinal IV. Domestic environmental sanitation and the prevalence protozoa of man by flies. American Journal of Hygiene, 1, of Entamoeba histolytica. American Journal of Tropical 131-153. Medicine and Hvgiene, 5, 29-39. Rudolfs, W., Falk, L. L. and Ragotzkie, R. A. (1950). Mata, L. J., Kromal, R. A., Urrutia. J. J. and Garcia. B. (1977). Literature review on the occurrence and survival of enteric, Effect of infection on food intake and the nutritional state: pathogenic and related organisms in soil, water, sewage perspectives as viewed from the village. American Journal and sludges, and on vegetation. II. Animal parasites. of Clinical Nutrition, 30, 1215-1227. Sewage and Industrial Wastes, 22, 1417-1427. Mathur, T. N. and Kaur, J. (1972a). Epidemiology of (1951). Contamination of vegetables grown in amoebiasis with particular reference to amoebiasis as a polluted soil. II. Field and laboratory studies on Emt- familial infection. Journal of the Association of Physicians amoeba cysts. Sewage and Industrial Wastes, 23, 478-485. of India, 20, 693-696. Sargeaunt, P. G., Williams, J. E., Kumate, J. and Jimenez, E. (1972b). The epidemiology of amoebiasis in an urban (1980). The epidemiology of Entamoeba histolytica in area. Indian Journal of Medical Research, 60, 1134-1137. Mexico City. A pilot survey. I. Transactionzs of'the Roval Melvin, D. M. and Brooke, M. M. (1962). Parasitologic Society of Tropical Medicine and Hygiene, 74, 653-656. surveys on Indian reservations in Montana, South Schmerin, M. J., Gelston, A. and Jones, T. C. (1977). Dakota, New Mexico, Arizona, and Wisconsin. American Amebiasis: an increasing problem among homosexuals in Journal of Tropical Medicine and Hygiene, 11, 765-772. New York City. Journal of the American Medical Moore, H. A., de la Cruz, E. and Vargas-Mendez, 0. (1965). Association. 238, 1386-1387. Diarrheal disease studies in Costa Rica. IV. The influence Schoenleber. A. W. (1940). The food handler as a transmitter of sanitation upon the prevalence of intestinal infection of amebiasis. Americani Journal of Tropical Medicine, 20, and diarrheal disease. American Journal of Epidemiology, 99-106. 82, 162-184. Scott, J. C. (1952). Healthl and Agriculture in China: a Morton, T. C., Stamm, W. P. and Seidelin, R. (1952). Fundamental Approach to some of the Problems of'World Indigenous amoebiasis: a recent outbreak in England. Hunger. London: Faber and Faber. British Medical Journlal, 2, 114-116. Sexton, D. J., Krogstad, D. J., Spencer, H. C. Jr. Healy, G. R., Nnochiri. E. (1965). Observations on childhood amoebiasis Sinclair, S.. Sledge, C. E. and Schultz, M. G. 11974). in urban family units in Nigeria. Journal of Tropical Amebiasis in a mental institution: serologic and Medicine and Hygiene. 68, 231--236. epidemiologic studies. American Jouirnal of Epidemiology, Panicker. P. V. R. C. and Krishnamoorthi, K. P. (1978). 100, 414-423. Elimination of enteric parasites during sewage treatment Simitch, T., Petrovitch. Z. and Chibalitch, D. (1954). processes. Indian Association bfo Water Pollution Control Viability ofcysts of Entamoeba histolytica outside the host. Technical Annual, 5, 130-138. Archiives de l'Institut Pasteur d'Algerie, 32, 223-231. Pierce, V.. Ascoli, W., de Leon, R. and Gordon, J. E. (1962). Sole, T. D. and Croll, N. A. (1980). Intestinal parasites in man Studies of diarrheal disease in Central America. III. in Labrador, Canada. American Journal of' Tropical Specific etiology in endemic diarrhea and dysentery in Medicine and Hygiene. 29, 364-368. Guatemalan children. American Journal of' Tropical Spector. B. K., Baylis, J. R. and Gullans, 0. (1934). Medicine and Hygiene, 11, 395-400. Effectiveness of filtration in removing from water, and of Pipkin, A. C. (1949). Experimental studies on the role of filth chlorine in killing, the causative organism of amoebic flies in the transmission of Endamoeba histolytica. dysentery. Public Healt/z Reports, 49, 786-800. American Journal of Hygiene, 49, 255-275. Spector, B. K. and Buky, F. (1934). Viability of Endamoeba Reardon, L. V., Verder, E. and Rees, C. W. (1952). The histolytica and Endamoeba coli: effect of drying. Public cultural requirements of Endamoeba coli and the Health Reports, 49, 379-385. comparative effects of drying on the cysts of E. coli and E. Spencer, H. C. Jr. Hermos, J. A., Healy. G. R., Melvin, D. M. histolytica. American Journal of Tropical Medicine and and Shmunes, E. (1976). Endemic amebiasis in an Hygiene. 1, 155-161. Arkansas community. American Journial of Epidemiology. Rendtorff, R. C. (1954). The experimental transmission of 104, 93-99. human intestinal protozoan parasites. 1. Endamoeba coli Spencer, H. C., Muchnik, C.. Sexton, D. J., Dodson, P. and cysts given in capsules. American Journal of Hygiene. 59, Walls, K. W. (1977). Endemic amebiasis in an extended 196-208. family. American Journal of Tropical Medicine and Rendtorff, R. C. and Holt, C. J. (1954a). The experimental Hygiene, 26, 628-635. transmission of human intestinal protozoan parasites. III. van Zijl. W. J. (1966). Studies on diarrhoeal diseases in seven ENTAMWOEBA HISTOLYTICA AND AMEBIASIS 347 countries by the wHo Diarrhoeal Diseases Advisory Team. Wykoff. D. E., Fonseca, J. R. C. and Richie, L. S. (1955). Bulletin of the World Health Organization, 35, 249-261. Epidemiology of amebiasis: possible infltuence of water Wachs, A. (1961). Studies on Sewage Stabilization Ponds in supply, coincident with diverse features of terrain, on the Israel: I. Oxidation Ponds at HerzhVa. Haifa: Technion occurrence of intestinal protozoa. American Journal of Sanitary Engineering Laboratories. Tropical Medicine and Hygiene, 4, 465-471. Wang,W.-L.L.andDunlop, S.G. (1954).Animalparasitesin Wykoff, D. E. and Ritchie, L. S. (1960). Intenstinal protozoa sewage and irrigation water. Sewage and Industrial Wastes, in family groups of four Japanese villages. US Armed 26, 1020-1032. Forces Medical Journal, 11, 1106-1116. WHO Scientific Working Group (1980). Parasite-related diarrhoeas. Bulletin of the World Health Organization, 58, 819-830. 21 Giardia and Giardiasis THE PARASITE Giardia,' and the infections and Symptoms may be absent, but when present may diseases it causes, attracted little interest for the first include frequent diarrhea with greasy, foul-smelling 110 years after its description by Lambl in Prague in stools, usually without blood. There may be fatigue, 1859. It was widely believed that Gia7dia was a abdominal cramps, flatulence, anorexia, and in some commensal parasite of doubtful pathogenicity. It is cases fever and vomiting. During the infection, damage now recognized that Giardia lamnblia frequently causes to the intestinal epithelium, detectable histologically, a mild, self-limiting disease in man and is, more rarely, may take place; bacterial colonization of the small responsible for serious illness. It is now the most intestine may be a predisposing condition for this commonly isolated intestinal pathogenic protozoon damage or may be consequent upon it. The damage worldwide; in countries such as the USA and the UK leads to malabsorption of carbohydrates, fats, fat- where worm infections are rare, it is the most soluble vitamins, and vitamin B12. Malabsorption and commonly isolated of all intestinal pathogenic bile duct inflammation are the most serious complica- parasites. In addition, G. Iamblia has been found to be tions of giardiasis, since the malnutrition consequent responsible for several recent waterborne diarrhea on malabsorption increases susceptibility to other outbreaks in the USA and USSR, and a combination of diseases. The disease is diagnosed by identifying the these circumstances has created a wave of interest and cysts or trophozoites of G. lamblia in the stools, or by research in this previously neglected parasite. Recent recognition of the trophozoites in duodenal or jejunal reviews of the subject include Jakubowski and Hoff aspirates or biopsies. G. lamblia is morphologically (1979), Knight (1978), Meyer and Jarroll (1980), Meyer indistinguishable from other Giardia species common and Radulescu (1980), Raizman (1976), WHO Scientific in many mammals. In cases of malabsorption, serology Working Group (1980), and Wolfe (1978, 1979a. can aid the diagnosis. 1979b). Occurrence Description of Pathogen and Disease The disease is cosmopolitan, associated with poor sanitation and inadequate protection of drinking water Although the clinical picture of giardiasis is well sources. Prevalence of Giardia infection worldwide is described, several aspects of its pathology, immuno- estimated to be about 7 percent. It is about 3 times logy, and epidemiology remain uncertain, and some of more common in children than in adults. Local the information in this chapter is therefore preliminary prevalence in children may exceed 50 percent. In and tentative. Europe and the USA, there is a considerable variation from place to place in the likelihood of contracting Identification the disease, and this appears to be related to the safety of the drinking water. Intrafamilial infection is well Giardiasis is an infection of the small intestine of recognized. man by the flagellate protozoon Giardia lamblia. The bile duct and gall bladder may also be infected. Infectiotts agent 1. See the subsection 'Infectious Agent," below, for a note on The taxonomy and nomenclature of Giardia are in a taxonomic nomenclature. confused and fluid state. Two genus names are used 349 350 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA interchangeably: Giardia (giardiasis) is most com- is pear or kite shaped, 9-21 micrometers long by 6-12 monly used in North America and Western Europe, micrometers broad, with an anterior sucking disc on whereas Lamblia (lambliasis) is favored in Eastern the flattened ventral surface (figure 21-1). There are Europe and the USSR. Resolution of this issue is four pairs of flagella, and the organism is binucleate. simply a question of agreement about the historical The cysts are ovoid, 14-16 micrometers long and 6-12 precedence of the rival names the nature of the micrometers broad, and are quadrinucleate. organism being described is not in doubt. It is probable that Giardia will become adopted worldwide, and Reservoirs Giardia is used in this book. The definition of species within the genus Giardia is The reservoir of G. lamblia is man, but there is some far more complex. In the first half of this century it was evidence that man may acquire infections from other believed that Giardia species were highly host specific, animals. Many mammalian species harbor their own and therefore specific names were allocated on this Giardia species whose relationship to G. lamblia has basis. It is now known, that some Giardia species infect not yet been properly elucidated. Beavers have been several different animals. The morphology of the incriminated as a reservoir of infection for hikers trophozoites provides the other main avenue for drinking stream water that is contaminated by wild species definition. Three primary species have been animal feces. G. lamblia from man has been transmit- suggested on the grounds of trophozoite morphology: ted to the rat, gerbil, guinea pig, beaver, dog, cat, G. agilis in frogs and tadpoles, G. muris in rodents and racoon, bighorn, mouflon, and pronghorn (Davies and birds, and G. duodenalis in mammals including man. Hibler 1979; Meyer and Radulescu 1980). Giardia The matter remains unresolved, and research is in cysts from beavers and deer have caused infection in progress on improved species definition. human volunteers (Davies and Hibler 1979). The species or subspecies that infects man is called G. lamblia in this book, although it is also referred to in Transmission the literature as G. intestinalis, G. enterica. or, in Eastern Europe, Lamblia intestinalis. Up to 900 million cysts may be passed in the stools G. lamblia is a flagellated protozoon. The tropho- during 1 day. The cystic infective stage is quadri- zoite, found in the small intestine or in diarrheic stools, nucleate and relatively thick walled, and earlier thin- walled "precysts" and the trophozoites rapidly die and are not important in transmission. The median infective dose for man is between 25 and 100 cysts 1 1 w 1 - (Rendtorff 1954, 1979; Rendtorff and Holt 1954b). On .t |1 - w being ingested, the cyst resists stomach acid and hatches in the small intestine, where the two trophozoites that emerge multiply by longitudinal * = L r ^'1 binary fission in the crypts of the duodenum, jejunum, and ileum and attach themselves to the mucosa by means of the sucking disc. Infection of the lining of the of ~ F- s - 'bile duct and gall bladder has been reported, although Mfl.a i on i, a rt * T there is no evidence for invasion of other sites. The * -- @; at ~~~~~~~~trophozoites transform into cysts in the ileum, and the cysts are passed in the stool. Unlike the acute amebic dysentery case, the patient Xwith marked symptoms of intestinal giardiasis is a potent source of infective cysts. This may be a reason why outbreaks of giardiasis are more common than Figure 21-1. Trophozoites of Giardia lamblia, oni and thsofaeiis over the surjace of the small intestine oj a patient with those of Gr ibflo nan giardiasis, under scanning electronmicroscopy. Scale Transmission of Giardia IS by fecal contamiation of bar = 10 micrometers. (Photo: R. L. Owen, Cell hands, food, and water supplies. Water supply Biology Section, Veterans Administration Medical contamination has been definitely incriminated in Center, San Francisco, USA. Reproduced by permis- several outbreaks. Although houseflies and other sion of the Royal Society of Tropical Medicine and insects have not been shown to be efficient distributors Hygiene) of cysts, it is likely that flyborne transmission of the GIARDIA AND GIARDIASIS 351 organism may play a part in areas of high prevalence. The pattern of infection is typically endemic. A poor Fecal contamination of the hands probably plays an community may have a substantial proportion of even more important part in the transmission of asymptomatic carriers continuously contaminating Giardia than of Ent. histolytica. Although transmission the environment with Giardia cysts, although the of Ent. histolytica occurs only sporadically in the UK, duration of carriage is typically shorter than for Giardia is regularly transmitted, and in this country the amebiasis (chapter 20). Recorded prevalences in water supply can probably be ruled out as a possible various communities range from 1 to over 20 percent. source. Children between 1 and 5 years old have the highest infection rates. Prevalences of Giardia excretion among healthy children 1-5 years old in Guatemala were 26 percent of In man the prepatent period has been recorded as rural children, 44 percent of poor urban children, and 6-36 days, averaging 9 days in one study (Rendtorff 15 percent of more wealthy urban children (Pierce and 1954), 13 days in another (Rendtorff and Holt 1954b), others 1962). A longitudinal study of 45 children from and 14 days (median) in a third (Jokipii and Jokipii birth to 3 years of age in a Guatemalan village showed 1977). The incubation period in natural outbreaks is that 93 percent had had one or more Giardia infections generally between 1 and 3 weeks, and a study of thirty- before their third birthday (Mata and others 1977). five cases in Finland recorded a range of 3-42 days and Studies in the Gambia showed that age-specific a median of 8 days (Jokipii and Jokipii 1977). prevalences of giardiasis rose from 1 percent in infants (under 1 year), to 24 percent in children 3-4 years old Period of communicability and fell steadily to 6 percent in those over 40 years old Perod of communicability (Bray and Harris 1977). Giardiasis was more common Infections in adults, demonstrable by the presence of than amebiasis in children under 5 years old, but less cysts in the feces (and therefore communicable), have common in the whole community. In northern Nigeria been experimentally observed to last up to 41 days. In the giardiasis prevalence rose from t percent in 0-3 children the course of the infection may be much longer month old babies to 51 percent in 2-3 year old children and has been reported to last for several years (the and fell to 18 percent in adults (Tomkins 1981). possibility of self-reinfection cannot be excluded). In a Giardia excretion rates among healthy preschool report from Delhi, two-thirds of adults and children children (0-6 years) were 4 percent in Sri Lanka, 22 naturally infected had lost their infections within 3 percent in Iran, 14 percent in Bangladesh, and 21 months. percent in Venezuela. Except in Sri Lanka, giardiasis was more prevalent than amebiasis (van Zijl 1966). Resistance Giardiasis prevalences among Laotian refugees in Thailand were 23 percent in the under-5 age group and The higher prevalence of the disease in children and 7 percent in the total population (Temcharoen and the relatively short duration of an infection indicate others 1979). Corresponding figures for amebiasis were that a protective immune response, possibly age- 3 percent and 2 percent. Mello and others (1978) found related, may be involved. Antibody to Giardia is G. lamblia cysts under the fingernails of 1 out of 148 detectable in the serum of patients with the intestinal schoolchildren in Brazil. malabsorption syndrome and a Giardia infection, but Endemic giardiasis is found in temperate developed there is no evidence of protection in such cases. countries as well as in tropical developing countries. Resistance following infection is probably not long- Prevalences are especially high among poor com- lasting, and reinfection is common, even in adults. munities and disadvantaged ethnic groups. Prevalences among poor children (6 months to 16 Epidemiology years) in Glasgow (Scotland) were 13 percent of Scots, 10 percent of Asians, 1 percent of Africans, and 1 Giardiasis occurs throughout the world but is more percent of Chinese (Goel and others 1977). Sole and prevalent in poor communities with inadequate Croll (1980) recorded a giardiasis prevalence of 5 sanitation. There is no simple correlation, however, percent among one racial group in Labrador between levels of sanitation or economic development (Canada), with no infections occurring in adults over and the prevalence of giardiasis. Considerable un- 20 years old. Over a 1-year period 24 percent of explained variations in prevalence exist, even within a Cherokee schoolchildren in the USA had giardiasis, small geographical area. and 14 percent had Ent. hlistolytica infection (Healy 352 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA 1979). A survey in Tasmania (Australia) found that human reservoirs of G. lamiblia, the survival of Giardia G. Iamblia was the most commonly identified intestinal cysts in the environment, and the epidemiology of parasite of any kind (Goldsmid 1981). Giardiasis in giardiasis in developing countries prohibit any developed countries is especially common in mental definitive statements to be made on control. institutions (Jeffery 1960), in nurseries (Black and others 1977; Brown 1948), and among male homo- Individual sexuals (Mildvan, Gelb and William 1977). Giardiasis is also associated with recent foreign travel to A number of drugs are effective in treatment (for developing countries or to Leningrad (USSR). instance, metronidazole) but are not appropriate for In addition to the endemic picture of giardiasis mass chemotherapy or prophylaxis. There is no described above, outbreaks also occur. The best vaccine. documented of these are in developed countries, Individual protection is achieved by cleanliness and especially the USA and USSR, and most are believed to care in choice and preparation of drinking water and have been waterborne. In the USA, between 1965 and food. Suspected water should be boiled, and suspect 1977 there were twenty-three waterborne outbreaks of fruit and vegetables should be washed and treated with giardiasis reported involving 7.009 cases (Craun warm water (55°C) or vinegar for 30 minutes. 1979a; 1979b). Giardia cysts were isolated from the water in five of these outbreaks. The outbreaks EnEiironmental occurred mainly in the mountainous areas of the There is little direct evidence on the relative Rocky Mountains, in the Northwest, and in New effectiveness of various environmental control ap- England. The incriminated waters were mostly surface proaches. In vareas ennme (USA), ap- waters either untreated (six outbreaks) or treated only proaches. In rural areas of Tennessee (USA), giardiasis by chlr (ten (six outbreaks) Gior - tr ite ivey prevalence was related to fecal pollution of the home, household cleanliness, personal cleanliness. and family beavers were implicated as the source of infection in one outbreak in Washington State. Colorado has been size but not to water supply or sanitation facilities (Evles, Jones and Smith 1953). Moving mental patients the most affected state and has now made the filtration i I and chlorination of all surface water supplies in California (USA) from old and unhygienic premises mandachlori.Enationo giardall s su wrat su pies to a new and well-equipped building did not reduce mandtory Enemicgiariass inColoadohas een Giardia transmission (Jeffery 1960). Improved water associated with the drinking of mountain stream water by hikers (Wright and others 1977). Waterborne supplies, bored-hole latrines, refuse disposal, and giardiasis in the USA is reviewed at length in preventive work by visiting nurses failed to reduce the Jakubowski and Hoff (1979). prevalence of giardiasis in Egypt (Chandler 1954). Jakubowski an Hoff (1979).The comments on environmental control of There is evidence for (Gupta and others 1972' Root 1921) and against (Rendtorff and Holt 1954a) the amebiasis (chapter 20) apply to giardiasis. Improved personal and domestic cleanliness are probably crucial, transmission of Giar-dia cysts from feces to food by flics animrvdwtrspladsnttonfciie J ....................and improved water supply and sanitation facilities and cockroaches. It a clear theoretical possibility. may also be important. but of unknown epidemiological importance. As with amebiasis (chapter 20), waterborne out- breaks occur, but endemic transmission is much more Occurrence and Survival in the likely to be by person-to-person transfer especially in Environment conditions of poverty, overcrowding, and inadequate water supply and sanitation. Person-to-person trans- Tests for G. lamniblia cysts in water and other samples mission has been strongly implicated in nurseries, are currently very inadequate. Cysts may be missed schools, and other children's institutions in altogether at concentrations below 4,000 cysts per liter Czechoslovakia (Cerva 1955), the USA (Black and of water (a high concentration), and the cyst count may others 1977). and elsewhere. Person-to-person trans- underestimate the true count by as much as 99 percent. mission, and family clustering of infection, have also When a cyst has been detected microscopically, there is been suggested in community studies (for instance. no way of proving it to be a species capable of infecting Eyles, Jones and Smith 1953). man (other than by human volunteer studies). nor of showing it to be infective (other than by feeding it to Control Measures laboratory animals). Even establishing viability (by eosin exclusion or excystation in vitro) is complex and The gaps in knowledge about possible non- controversial. There will be little progress in the GIARDIA AND GIARDIASIS 353 environmental study of Giardia until laboratory with Eatr. histolytica cysts (chapter 20). Both these techniques are greatly improved. approaches are unsatisfactory. and the recent develop- The recent documentation of waterborne outbreaks ment of in vitro excystation tests for viability will of giardiasis in developed countries has stimulated an permit more informative research on Giardia chlori- explosion of research interest in this disease and nation to be conducted (Hoff 1979). The first reported engineering approaches to control. Most of this study of the effect of disinfection on excystation interest is focused on Giardia cyst removal by water confirmed that both chlorine and iodine compounds treatment processes and is therefore not relevant to this have considerably reduced cysticidal properties at 3°C book. The state of the art, as in 1978, is compre- compared with 20°C (Jarroll, Bingham and Meyer hensively described by Jakubowski and Hoff (1979). 1980). Pending more research, the best estimate of Giardia Filtration experiments have indicated that Giardia cyst survival in the environment is that it is similar to cysts can be removed by coagulation plus granular Ent. histolytica survival and may therefore be estimated medium filtration, or by diatomaceous earth filtration, from figure 20-2. but only with "conscientious, high quality filter plant operation"' (Logsdon, Symons and Hoye 1979). In water and water supplies The inadequacy of laboratory techniques for In Jeces and night soil isolating Giardia cysts from water has prevented Cyst production by an infected individual is progress in the study of Giardia in the environment. In typically 10i-107 per gram of stool but varies greatly. five of the waterborne outbreaks of giardiasis recorded Some individuals excrete only small numbers of cysts in the USA during 1965-77. Giardia cysts were found in intermittently, with 60 percent of stools negative. raw water sources or tap water (Craun 1979a; Jakubowski and Ericksen 1979). Cysts were located with extreme difficulty, and, if the waterborne In sewage assumptions were correct, recorded cysts must have The probable concentration of Giardia cysts in grossly underestimated the actual occurrence of cysts sewage in the USA has been estimated theoretically as in the waters. In the case of the outbreak at Rome (New 9 x 103-2 x 10i per liter (Jakubowski and Ericksen York, USA) in 1974, 1.1 x 106 liters of raw water were 1979). These concentrations of cysts have not been filtered over 10 days, and one cyst was identified confirmed, and the literature contains only the microscopically in the residue. Two of ten samples of occasional, and mainly qualitative, report of Giardia the residue induced giardiasis in beagle puppies that cysts in sewage. Fox and Fitzgerald (1979) reported up ingested them (Jakubowski and Ericksen 1979). to 530 Giardia cysts per liter of raw sewage in Chicago Bingham, Jarroll and Meyer (1979) studied Giardia (USA). The cysts were more common in domestic than cyst survival in unchlorinated tap water (pH 6.8) at industrial sewage and occured more frequently during various temperatures and evaluated cyst viability both April-September. by eosin-exclusion and by the ability to excyst in vitro. Judged by eosin staining (indicating dead cysts), 100 percent destruction took place in 24 days at 37°C, in 31 days at 21°C, and in over 77 days at 8°C. Judged by the There are only a few studies on Giardia cyst survival failure to excyst, the equivalent times were 6 days, 25 and all except the most recent use overconservative days, and 77 days. Cysts were instantly rendered dead, tests for viability. Workers have had to rely on by the criterion of failure to excyst, in boiling water. observations of morphological changes, and the fact It is widely believed that Giardia cysts are resistant to that eosin or neutral red will stain the contents of cysts chlorination under conditions often found in water which are (probably) dead (see Boeck 1921a, 1921b; treatment plants. They are particularly resistant at Cerva 1955). By analogy with Ent. histolytica, we might low temperatures, and this fact has been linked to the expect that stained cysts would certainly be dead, occurrence of several waterborne outbreaks in the whereas some unstained cysts might also be dead. USA and the USSR in the winter months. Current No definitive statements on Giardia cyst survival can concepts of Giardia disinfection come partly from early be made until a new generation of experiments, using studies that adopted the very conservative criterion of in tvitro excystation as the measure of viability, have eosin exclusion as the test of viability (for instance, been completed. In the meantime the literature Cerva 1955: Thomas 1952), and partly from analogy suggests that Giardia cysts are somewhat similar to 354 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA Ent. histolytica cysts. They are rapidly killed by (>20°C) for 6 weeks or more should also eliminate desiccation and freezing. They are resistant to a wide Giardia cysts (figure 20-2). range of pH and osmotic pressure. Their survival in most moist environments is primarily temperature Literature Cited dependent and may be similar to Ent. histolytica (figure 20-2). The most recent data, using excystation Bingham, A. K.. Jarroll, E. L. Jr and Meyer, E. A. (1979). techniques, on survival in water (6 days at 37°C, 25 Induction of Giardia excystation and the effect of days at 21°C and 77 days at 8°C) show a remarkably temperature on cyst viability as compared by eosin- close agreement with figure 20-2 (Bingham, Jarroll and exclusion and in vitro excystation. In Waterborne Meyer 1979). Transmission of Giardiasis, eds. Jakubowski, W. and Hoff, J. C., pp. 217-229. Report EPA-600,/9-79-001. Cincinnatti, Ohio: US Environmental Protection Agency. Inactivation by Sewage Treatment Black, R. E., Dykes, A. C., Sinclair, S. P. and Wells, J. G. Processes (1977). Giardiasisin day-care centers: evidence of person- to-person transmission. Pediatrics, 60, 486-491. Very little is known about the fate of Giardia cysts Boeck, W. C. (1921a). The thermal death point of the human intestinal protozoan cysts. American Journal of Hygiene, 1, during sewage treatment. The cysts are similar in size 365-387. to those of Ent. histolytica but are reported to (1921b). On the longevity of human intestinal be slightly denser (specific gravity 1.1 : Rachmanow protozoan cysts. American Journal of Hygiene, 1, 527-539. 1936). Bray, R. S. and Harris, W. G. (1977). The epidemiology of The best assumption at present is that Giardia cysts infection with Entamoeba histolytica in The Gambia, West respond to sewage treatment in the same manner as Africa. Transactions of the Royal Society of Tropical Ent. histolytica cysts (chapter 20). Studies on Medicine and Hygiene, 71, 401-407. sedimentation, trickling filters, activated sludge, Brown, E. H. (1948). Giardia lamblia, the incidence and biodiscs, aerated lagoons, oxidation ditches, and waste results of infestation of children in residential nurseries. stabilization ponds in India showed very similar Archives of Disease in Childhood, 23, 119-128. removablrates fonds the two protozowed vPaery andl Cerva, L. (1955). The effects of disinfectants on cysts of removal rates for the two protozoa (Panicker and Lamblia intestinalis (Giardia intestinalis). Ceskoslovenski Krishnamoorthi 1978). All systems removed 52-93 Parasitologie, 2, 17-21. percent of Giardia cysts (except waste stabilization Chandler, A. C. (1954). A comparison of helminthic and ponds, which removed 100 percent). protozoan infections in two Egyptian villages two years after the installation of sanitary improvements in one of them. American Journal of Tropical Medicine and Hygiene, Inactivation by Night Soil and Sludge 3, 59-73. Treatment Processes Craun, G. F. (1979a) Waterborne giardiasis in the United States: a review. American Journal of Public Health, 69, This subject has not been investigated. Night soil 817-819. and sludge treatment processes do not involve freezing, _ (1979b). Waterborne outbreaks of giardiasis. In andy sludge treatment proessesat , ndo not invole freuez Waterborne Transmission of Giardiasis, eds. Jakubowski. very rarely involve desiccation, and do not produce W. and Hoff, J. C., pp. 127 149. Report EPA-600/9-79-001. environments that are especially or particularly hostile Cincinnati, Ohio: US Environmental Protection Agency. to Giardia cysts. Therefore, cyst destruction may be Davies, R. B. and Hibler, C. P. (1979). Animal reservoirs and expected to be a function of time and temperature. cross-species transmission of Giardia. In Waterborne Pending research, the best assumption is that Giardia Transmission of Giardiasis, eds. Jakubowski, W. and Hoff, cysts behave as Ent. histolytica cysts, and their fate J. C., pp. 104-126. Report EPA-600/9-79-001. Cincinnati, during any given process can be estimated from figure Ohio: US Environmental Protection Agency. 20-2. Eyles, D. E., Jones, F. E. and Smith, C. S. (1953). A study of Most mesophilic and all thermophilic digestion and Endamoeba histolytica and other intestinal parasites in a composting processes are likely to eliminate Giardia rural West Tennessee Community. American Journal of c n i Ur o Tropical Medicine and Hygiene, 2, 173-190. cysts. In Chicago (USA), despite the presence of Fox, J. C. and Fitzgerald, P. R. (1979). The presence of Giardia cysts in raw sewage, none were found in Giardia lamblia cysts in sewage and sewage sludges from anaerobically digested sludges (Fox and Fitzgerald the Chicago area. In Waterborne Transmission of 1979). Thermophilic composting may be expected to Giardiasis, eds. Jakubowski, W. and Hoff, J. C., pp. eliminate Giardia cysts with a wide margin of safety. 268-269. Report EPA-600/9-79-001. Cincinnati, Ohio: US Storage of night soil or sludge at tropical temperatures Environmental Protection Agency. GIARDIA AND GIARDIASIS 355 Goel, K. M., Shanks, R. A., McAllister, T. A. and Follett, E. A. Meyer. E. A. and Jarroll, E. L. (1980). Giardiasis. American C. (1977). Prevalence of intestinal parasitic infestation, Journal of Epidemiology, 111, 1-12. salmonellosis, brucellosis, tuberculosis, and hepatitis B Meyer, E. A. and Radulescu, S. (1980). Giardia and giardiasis. among immigrant children in Glasgow. British Medical Advances in Parasitology, 17, 1-47. Journal, 1, 676-679. Mildvan, D., Gelb, A. M. and William, D. (1977). Venereal Goldsmid, J. M. (1981). Intestinal parasitic infections of man transmission of enteric pathogens in male homosexuals. in Tasmania. Transactions of the Royal Society of Tropical Journal of the American Medical Association, 238, Medicine and Hygiene, 75, 110-111. 1387 1389. Gupta, S. R., Rao, C. K., Biswas, H., Krishnaswami, A. K., Panicker, P. V. R. C. and Krishnamoorthi, K. P. (1978). Wattal, B. L. and Raghavan, N. G. S. (1972). Role of the Elimination of enteric parasites during sewage treatment house-fly in the transmission of intestinal parasitic processes. Indian Associationfor Water Pollution Control cysts/ova. Indian Journal of Medical Research, 60, Teclnical Annual, 5, 130-138. 1120-1125. Pierce, V., Ascoli, W., de Leon. R. and Gordon, J. E. (1962). Healy, G. R. (1979). The presence and absence of Giardia Studies of diarrheal disease in Central America. III. lamblia in studies on parasite prevalence in the U.S.A. In Specific etiology of endemic diarrhea and dysentery in Waterborne Transmission of Giardiasis, eds. Jakubowski, Guatemalan children. American Journal of Tropical W. and Hoff, J. C., pp. 92-103. Report EPA-600/9-79-001. Medicine and Hygiene, 11, 395-400. Cincinnati, Ohio: US Environmental Protection Agency. Rachmanow, H. (1936). Determination of the specific gravity Hoff, J. C. (1979). Disinfection resistance of Giardia cysts: of Lamblia intestinalis (Giardia intestinalis) cysts. Archiufar origins of current concepts and research in progress. In Sch.iffs- u. Tropenhlvgiene, 40, 395-396. Waterborne Transmission of Giardiasis, eds. Jakubowski, Raizman, R. E. (1976). Giardiasis: an overview for the W. and Hoff, J. C., pp.231-239. Report EPA-600 /9-79-001. clinician. Digestive Diseases, 21, 1070-1074. Cincinnati, Ohio: US Environmental Protection Agency. Rendtorff, R. C. (1954). The experimental transmission of Jakubowski, W. and Ericksen, T. H. (1979). Methods for human intestinal protozoan parasites. IL. Giardia lamblia detection of Giardia cysts in water supplies. In Waterborne cysts given in capsules. American Journal of Hygiene, 59, Transmission of Giardiasis, eds. Jakubowski, W. and Hoff, 209-220. J. C., pp. 193-210. Report EPA-600/9-79-001. Cincinnati, (1979). The experimental transmission of Giardia Ohio: US Environmental Protection Agency. lamblia among volunteer subjects. In Waterborne Trans- Jakubowski, W. and Hoff, J. C., eds. (1979) Waterborne mission of Giardiasis, eds. Jakubowski, W. and Hoff, J. C., Transmission oJ Giardiasis. Report EPA-600/9-79-001. pp. 64-81. Report EPA-600/9-79-001. Cincinnati. Ohio: Cincinnati. Ohio: US Environmental Protection Agency. US Environmental Protection Agency. Jarroll, E. L. Jr, Bingham. A. K. and Meyer, E. A. (1980). Rendtorff, R. C. and Holt, C. J. (1954a). The experimental Giardia cyst destruction: effectiveness of six small-quantity transmission of human intestinal protozoan parasites. III. water disinfection methods. American Journal of Tropical Attempts to transmit Endamoeba coli and Giardia lamblia Medicine and Hygiene, 29, 8-11. cysts by flies. American Journal of Hygiene, 60, 320-326. Jeffery, G. M. (1960). A three-year epidemiologic study of (1954b). The experimental transmission of human intestinal parasites in a selected group of mental patients. intestinal protozoan parasites. IV. Attempts to transmit American Journal of Hygiene. 71, 1-8. Endamoeba coli and Giardia lamblia cysts by water. Jokipii, A. M. M. and Jokipii, L., (1977). Prepatency of American Journal of Hygiene, 60, 327-338. giardiasis. Lancet, 1, 1095-1097. Root, F. C. (1921). Experiments on the carriage of intestinal Knight, R. (1978). Giardiasis, isosporiasis and balantidiasis. protozoa of man by flies. American Journal of Hygiene, 1, Clinics in Gastroenterology, 7, 31-47. 131-153. Logsdon, G. S., Symons, J. M. and Hoye, R. L. (1979). Water Sole, T. D. and Croll, N. A. (1980). Intestinal parasites in man filtration techniques for removal of cysts and cyst models. in Labrador, Canada. American Journal of Tropical In Waterborne Transmission of Giardiasis, eds. Jakubowski, Medicine and Hygiene, 29, 364-368. W. and Hoff, J. C., pp.240-256. Report EPA-600/9-79-001. Temcharoen, P., Viboolyavatana, J., Tongkoom, B., Sume- Cincinnati, Ohio: US Environmental Protection Agency. thanurugkul, P., Keittivuti, B. and Wanaratana, L. (1979). Mata. L. J., Kromal, R. A., Urrutia, J. J. and Garcia, B. (1977). A survey of intestinal parasitic infections in Laotian Effect of infection on food intake and the nutritional state: refugees at Ubon Province, Northeastern Thailand, with perspectives as viewed from the village. American Journal special reference to schistosomiasis. Southeast Asian of Clinical Nutrition, 30, 1215-1227. Journal of Tropical Medicine and Public Health, 10, Mello, E. de B. F., Souza, F. L. Jr, Padua, H. B., Campos, M. 552-555. S. and Tanabe, T. H. (1978). Econtro de ovos de helmintos Thomas, M. E. M. (1952). Observations upon the effects of e de cistos de protozoarios intestinais na regiao mepacrine and other substances on Giardia intestinalis. subungueal de crianQas em idade escolar dos municipios de Parasitology, 42, 262-268. Diadema e de BraganQa Paulista. Sao Paulo. Revista de Tomkins, A. (1981). The significance of intestinal parasites in Patologia Tropical, 7, 47-50. malnourished populations. Parasitology, 82, 38-40. 356 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: PROTOZOA van Zijl. W. J. (1966). Studies on diarrhoeal diseases in seven (1979a). Giardiasis. Pediatric Cliniei of Noril countries by the WHO Diarrhoeal Diseases Advisory Team. America, 26, 295-303. Builletin of the W7korld Healthi Orga,iiation, 35. 249-261. (1979h). Giardia lainblia. In Principles and(i Practice of WHO Scientific Working Group (1980). Parasite-related InlecLiu 'o eds. Mandell. G. L.. Doug.Ias. R. (i. Jr diarrhoeas. Builletin oj the World Health Orglanization, 58, and Bennett, J. E. pp. 2143-2147. New York: John Wiley. 819-830. Wright. R. A.. Spencer, H. C.. Brodsky. R. E. and Vernon. T. Wolfe, M. S. (1978). Giardiasis. New England Jouirial of M. (1977). Giardiasis in Colorado: an epidemiologic Medicine. 298, 319-321. study. Amlefica72 Journlal of Epidenliology. 105, 330-336. Section IV. Excreted Helminths Chapter 22 Ancylostoma, Necator and Ancylo- stomiasis 23 Ascaris and Ascariasis 24 Clonorchis and Clonorchiasis 25 Diphyllobothrium and Diphyllobothriasis 26 Enterobius and Enterobiasis 27 Fasciola and Fascioliasis 28 Fasciolopsis and Fasciolopsiasis 29 Hymenolepis and Hymenolepiasis 30 Minor Intestinal Flukes and Infections They Cause 31 Paragonimus and Paragonimiasis 32 Schistosoma and Schistosomiasis 33 Strongyloides and Strongyloidiasis 34 Taenia, Taeniasis, and Cysticercosis 35 Trichuris and Trichuriasis 22 Ancylostoma, Necator, and Ancylostomiasis ANCYLOSTOMIASIS, or hookworm infection, is not in early childhood, and in such cases there may be only very common but also produces serious clinical retardation of mental and physical development. consequences among a proportion of those infected. Hookworm is seldom recorded as a direct cause of With the possible exception of schistosomiasis death. Some grossly anemic individuals die of high- (chapter 32), it is the excreted worm with the greatest output heart failure. The disease is undoubtedly a worldwide public health importance. common contributory cause of death when other normally nonfatal infections attack a severely anemic and debilitated person. Description of Pathogen and Disease Numerous symptoms and signs cause suspicion of hookworm infection, but definitive diagnosis depends Ancylostomiasis is an infection of the small intestine on finding eggs in fecal samples. Since the eggs of N. with one of the two species of human hookworms, americanus and A. duodenale appear identical on Necator americanus or Ancylostoma duodenale. microscopical examination, species recognition re- Incidental infections with animal hookworms such as quires, in practice, either: A. caninum, A. ceylanicum and A. braziliense are not considered here, as they are unrelated to the disposal of (i) The administration of a vermifuge, followed by human excreta. Ancylostomiasis is a comprehensively collection of feces and microscopic study of the studied infection, and only a brief summary of expelled adults, which are morphologically dis- information on the worms and the diseases they cause tinct, or is given below. Several reviews are available, and (ii) The cultivation of hookworm eggs to the filariform Banwell and Schad (1978) and Miller (1979) are infective larval stage, when the two species can be particularly recommended. differentiated. Identification Occurrence Ancylostomiasis is frequently symptomless. When Historically, human hookworm infections were it does produce illness and constitutes a public probably confined to the eastern hemisphere, N. health problem, the most important features are americanus occurring south of 200 north latitude, and anemia and its resulting weakness, debility and A. duodenale north of 200 north latitude. In the past 500 other consequences (Roche and Layrisse 1966). years, population migrations, most notably those Gastrointestinal pain, transient cutaneous and pul- involving Spanish and Portuguese colonization in the monary symptoms, and edema may also be experienc- New World and Southern Africa, led to the ed. In heavily affected endemic areas, ancylostomiasis introduction of A. duodenale into these areas, as well as produces its most severe clinical effects in older the importation of N. americanus to Portugal. At the children and in young and middle-age adults, same time, the slave trade from Africa to North and especially in those vulnerable groups subject to South America and the Caribbean islands led to the physiological iron losses, such as pregnant and present widespread distribution of N. americanus in the lactating women or women suffering from abnormally western hemisphere. heavy menstruation. In areas of very intense trans- The present geographical distribution of the mission, however, heavy worm burdens can be built up hookworm species is given in figures 22-1 and 22-2. It 359 360 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS E ANCYLOSTOMA DUODENALE Figure 22-1. Known geographical ,1, r,b,ia,{. ,,of Ancylostoma duodenale. The infection may occur in areas as yet unrecorded E NECATOR AMERICANUS Figure 22-2. Known geographical distribution of Necator americanus. The infection may occur in areas as yet unrecorded ANC YLOSTOMA, NECATOR, AND ANCYLOSTOMIASIS 361 must be stressed, however, that many of the studies upon which these maps are based used egg detcction . techniques only and assumed the species identity of the parasites on the basis of existing knowledge for the , r locality. It is likely that future studies using adult worm recovery or cultivation of infective larvae will lead to considerable extensions of the geographical range of both worms. Furthermore, maps give no indication of the relative importance of each species in areas where 1. both species are sympatric, nor do they indicate intensity of infection and, hence, clinical importance. It | is essential that species prevalence and species intensity i be determined for an area before the planning and execution of any control intervention. Infectious agents The two hookworms that infect man, A. duodenale /lj ? and N. americanus, are diecious, sexually dimorphic roundworms belonging to the phylum Nematoda, |'3 ' order Strongylida, superfamily Ancylostomatoidea. The r X l adult worms are small and off-white or rusty in color (figure 22-3). A. duodenale is somewhat larger than N. i1d americanus, the males being 5-10 millimeters long and the females 10-18 millimeters, depending on the species. The eggs of A. duodenale measure 56-60 by 36-40 micrometers, and those of N. americanus are Figure22-3. Thehead(scolex)ojfanAncylostomaunider 64-76 by 36-40 micrometers in size. a light microscope. Scale bar = 0.1 millimeters. (Photo: A. ceylanicum, a hookworm of dogs, cats, and other Wellcome Museum of Medical Sciences) animals, can infect man and develop to the adult stage. It has been reported to be of some importance in India, Surinam, West Irian (Indonesia) and elsewhere conditions for hatching and subsequent larval (Banwell and Schad 1978). A braziliense and A. development are: caninum, the cat and dog hookworms, rarely develop to the adult stage in man, but their larvae can cause a (i) Shade from strong sunlight creeping dermatitis called larva migrans. (ii) Soil of the right particle size, denseness and structure; ideally a light sandy loam Reservoir (iii) Adequate, but not excessive, moisture; both desiccation and water-logging are rapidly lethal Man is the reservoir for the human hookworms. to hatched hookworm larvae (iv) A temperature between 28-32°C for N. amer- Transmission icanus, and between 20-27°C for A. duodenale; above and below these temperature ranges, larval Thin-shelled, ovoid, unsegmented eggs are dischar- development is slowed down and it is completely ged by the adult female worms into the lumen of the arrested below 10°C and above 40'C small intestine. The longer and stouter females of A. (v) Adequate decomposing organic material and duodenale produce approximately twice the number of microorganisms in the soil to provide a food eggs per day (104 to 2 x 104) as do those of N. supply for the developing larvae. americanus (5 x 103 to 104). The eggs develop rapidly in the gut and are usually at the four- or eight-cell stage If conditions are satisfactory, the larvae undergo two when evacuated in the feces. If feces are deposited in a moults outside the human body, on the third and fifth suitable environment, the eggs hatch in 24-48 hours to days of their free-living existence, giving rise to third- give rise to rhabditiform first-stage larvae. Optimum stage filariform larvae, which become infective to man 362 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS about 6 days after hatching from the egg. These larvae hookworms may live for up to 7 years in the case of A. normally survive for 3-6 weeks, and have a maximum duodenale and 15 years for N. americanus (Miller 1979). life span of 15 weeks. Larvae have a maximum vertical These are exceptional life spans, however, and 80 range of migration of about 1 meter in suitable soil, but percent of worms survive for less than 3 years. their lateral movement is restricted to about 0.3 meters and usually much less. Resistance Infection of man occurs most commonly when the third-stage larvae penetrate the skin, usually between Some degree of acquired resistance appears to the toes or on the feet and ankles. In the case of A. develop with age and repeated reinfection, at least in duodenale only, the third-stage larvae can also infect some individuals. The problems of distinguishing man when they are ingested with unwashed, raw between the effects of an immune response and the vegetables, onto which they can migrate from the soil. effects of varied exposure to infection are enormous in It is impossible to be certain of the relative importance ancylostomiasis. Elderly people are frequently obser- of cutaneous and oral routes of infection with A. ved with high prevalence rates and high worm burdens. duodenale; probably they differ in different parts of the At present, the problem of immunity is of more world with the food-eating and fertilizing habits of interest to research workers than to those involved in local populations. Experimental infections of man with investigating and controlling hookworm in field A. duodenale are more easily produced by the oral than situations. by the cutaneous route. Oral transmission of N. americanus is insignificant. Epidemiology After penetration of the skin, larvae of both Hookworm infections are extremely common and hookworm species enter small veins or lymphatic occur in many countries (figures 22-1 and 22-2). vessels and are carried to the heart and then to the Pe lungs N. merianusunderoes perod o de- rhaps 700 million persons are infected worldwide. velopment in the lungs, then ascends the bronchi and There are many hundreds of reports of hookworm 'lpeintlugthnsedteintsi ind prevalence rates from almost every country in the trachae, is swallowed, and reaches the small world. A few are summarized in table 22-1. In some 24-48 hours after skin penetration; two further moults localities hookworm infects over half of the population, occur, about 1 day and 13 days after reaching the small and it may be the most common intestinal worm. In intestine, A. duodenale undergoes the whole of its other areas it is less common and is exceeded in development in the small intestine, regardless of prevalence by Ascaris or Trichuris or both. - whether it enters the human body by the oral or There are major unexplained differences among cutaneous routes. Sexually mature fertilized females of communities in their prevalence of hookworm both species begin egg laying between 4 and 8 weeks infection and in the relative prevalence of ascarasis, after infection. meto n h eav rvlneo saiss trichuriasis, and hookworm. These variations may occur even in a small geographical area-for example, within both northern and southwestern Iran The prepatent period (the interval between infection (Ghadirian, Croll and Gyorkos 1979; Massoud and and the appearance of eggs in the stools) ranges from 4 others 1980). These variations may sometimes be to 8 weeks, with averages of 5 weeks for A. duodeniale related to soil type and climate and the effect of these and 6 weeks for N. americanus. on egg and larval development and survival. They may The incubation period (the interval between also be due to differences in behaviour, settlement infection and the development of symptoms and signs pattern, and agricultural practice. Because hookworm of illness) varies from a few weeks to several years, and transmission is sometimes particularly vigorous in or depends on the number of worms that parasitize an near fields, rural prevalence rates are nearly always individual, the individual's daily iron intake, body iron higher than urban rates (table 22-1). Rates are also stores, and other blood losses. In light infections in higher in lower socioeconomic groups than among the healthy people, no evidence of illness may ever appear, more wealthy (table 22-1). although such individuals may be epidemiologically The distribution of hookworm infection among significant as egg-passers. different age groups is typically fairly even, with the exception that prevalences are lower among children Period of communicability under 5 years old and sometimes in elderly adults. Ages Eggs will continue to be excreted for as long as there of maximum prevalence vary considerably from are adult female worms in the small intestine. Adult community to community (table 22-1). Typically, ANCYLOSTOMA, NECATOR, AND ANCYLOSTOMIASIS 363 Table 22-1. Prevalence of hookworm infection in fifteen countries Age of maximum Age Prevalence prevalence Population Location (years) (percent) (years) Source Bangladesh Rural All ages 29 ND Mackay and others (1979) Colombia Urban All ages 35 10-14 Faust and Mugaburu (1965) 40-49 Egypt Rural All ages 28 20-39 Chandler (1954) Gambia Rural All ages 23 40+ Bray and Harris (1977) Guatemala Rural 1-5 12 ND Pierce and others (1962) Urban (poor) 1-5 4 ND Urban (wealthy) 1-5 0 ND Haiti Rural All ages 24 15-19 Raccurt, Vial and Pierre-Louis (1977) India Urban All ages 8 ND Biswas and others (1978) Ruiral 1-11 68 ND Nawalinski, Schad and Chowdhury (1978a) Iran Rural All ages 44-71 ND Arfaa and others (1977) Rural All ages 25 11-15 Massoud and others (1980) Urban All ages 8 6-10 Ivory Coast Rural 7-14 73 ND Nozais, Dunand and Le Brigant (1979) Malaysia Rural 6-12 43 ND Lo and others (1979) Urban (poor) 4-6 5 13-15 Yan and others (1978) Urban (wealthy) 4-6 0 ND Papua New Guinea Rural All ages 68 20-29 Jones (1976) South Korea Urban All ages 14 30-39 Seo and others (1969) Rural All ages 19 30-39 Taiwan Rural All ages 52 over 60 Hsieh (1970) Thailand Rural All ages 61 ND Bhaibulaya and others (1977) Zambia Rural All ages 49 6-10 Wenlock (1979) ND No data. teenagers or young adults are the most infected, and in adults, average worm burdens, as estimated by prevalence rates are usually somewhat higher in males average fecal egg outputs, are nearly always greatest in than in females. This may be because much children. transmission takes place outside the village at the Improved living standards and better sanitation communal defecation place or in the fields. Young men have eradicated hookworm from some areas of Europe may therefore be most exposed, and immunological and North America and have made it rare in others. factors may prevent ever increasing prevalences among Nevertheless, in the USA an estimated 700,000 persons older men. are infected (Warren 1974), and it is especially common Risk of hookworm infection in some rural areas is in poor rural areas of the southeast. Hookworm linked to occupation. Thus, in rice-growing villages in prevalences of l0-20 percent are still recorded among northern Iran much transmission takes place in or near schoolchildren in parts of Alabama, Kentucky, and the rice fields, and the 10-40 age group has the highest Georgia. Hookworm control has, however, proved prevalence rate (Ghadirian, Croll and Gyorkos 1979). easier than control of the other major intestinal The immunological factors mentioned above have a nematodes, and ascariasis and trichuriasis are typically greater influence on intensity of infection than on more prevalent than hookworm in poor southern areas prevalence. Although prevalence rates are often highest of the USA (Fulmer and Huempfner 1965). 364 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Early studies on hookworm in Tennessee (Otto, Control Measures Cort and Keller 1931) and Virginia (Otto and Spindler Many of the comments made about ascariasis control 1930) suggested that high hookworm prevalences were in chapter 23 apply equally to hookworm control. The associated with sandy soils and that most transmission in differe23 arequally t heok gr ontreaTe took place at moist and shady sites where older major differences are, hrst, that the age of greatest children and adults defecated. This was in contrast to prevalence of infection is typically higher in hookworm than ascariasis; second, that most ascariasis trans- Ascaris transmission, which was concentrated in the msin aycake pe veyna th e home wheras yard where young children defecated. It is unclear mission may take place very near the homc, whereas yard~~~~~ ~~ whr yon chlrndfctd-ti nla hookworm transmission typically occurs further whether this model of transmission has global validity, howr tanmsin ypcly cusfrhe whetherg thereis moidel ceof rhookworm transmissionhasglo afield; and, third, that Ancylostoma and Necator adult although there IS evidence for hookworm transmisslon' ' worms live very much longer in the intestine than inmthe fields in several countries, and the hard packed Ascaris, and therefore the impact of reduced trans- earth around houses is unsuitable for development of missionw become appar t oreslwyi the hookworm larvae. mission will become apparent more slowly in the absence of mass chemotherapy. In some countries, for It is possible that most percutaneous hookworm instance South Korea and the USA, hookworm infection takes place at habitual defecation sites and infection has been easier to control than ascariasis, and during defecation. The heavy fecal contamination of this may be because it is less related to the hygienic the soil can lead to a high density of larvae, and these bhavior of young cItlden rad ao becasen may survive for several days if the soil is moist, loose, behavior of youtr ngs children and also because and shaded. The act of defecation by a barefooted hekprn wearin is where Ascris in person ensures the prolonged contact between foot and spractice of wearng shoes, where Ascaris trans- soil needed for successful infection. Hookworm eggs and larvae can be transported by houseflies (Oyerinde Iddul 1976), and this may conceivably add to the transmission of A. duodenale by the oral route. No special prophylactic drugs are available for The seasonality of hookworm infection remains hookworm infection. A valuable method of personal poorly understood. In areas where A. duodenale is prophylaxis is the wearing of adequate footwear at all endemic, a pronounced seasonal fluctuation in egg times when the skin might come into contact with output has been recorded. In Assam and Bengal infective larvae, especially in latrines themselves and in (Bangladesh and India), hookworms are lost during the immediate vicinity of human habitations, as well as the period from the late monsoon (September) till during agricultural work. However, universal wearing February, and this worm loss is accompanied by falling of footwear is clearly not an immediately practicable egg outputs (Maplestone 1930, 1932; Nawalinski, proposition, for economic as well as customary Schad and Chowdhury 1978a, 1978b; Schad and reasons. others 1973). Hookworm egg outputs then rise sharply In rural Costa Rica it was found that hookworm during the period March-May, before the start of the prevalence was not associated with sanitation but was monsoon. The simple explanation of this would be an related to the use of shoes (Moore, de la Cruz and increase in transmission approximately 6 weeks before, Vargas Mendez 1965). Males who always or sometimes during January-March. This is a dry hot period in wore shoes had a prevalence of 20-23 percent Bengal, however, when larvae are rapidly killed in the compared with 36 percent among males who never soil and when soil surveys find few if any infective wore shoes. The figures for females were 13 percent for larvae (Banwell and Schad 1978). Rises in egg output those who always wore shoes, 29 percent for those who before the rainy season have also been recorded in sometimes wore shoes, and 39 percent for those who Taiwan (Hsieh 1970) and in Indian prisoners who were never wore shoes. Much transmission took place at not exposed to transmission during the preceding few customary defecation sites in coffee plantations. months (Maplestone 1930). It is postulated that Several drugs are effective against hookworm hookworm larvae acquired during the rainy season of infections and are administered orally. Some of these one year become dormant and subsequently develop to drugs also treat infections with other common maturity before the next rainy season. This arrested intestinal worms; for instance, mebendazole is useful development of A. duodenale remains controversial, for combined infections of hookworm, Ascaris, and and there are few data from areas other than Bengal. Trichuris (Nagalingam and others 1976). Anti- No similar seasonal phenomenon has been reported hookworm drug therapy, in combination with oral from areas where N. americanus is the only endemic iron therapy, should form part of any specific hook- human hookworm. worm control campaign. .ANCILOSTOM.4, NECATOR, AND ANCYLOSTOMIASIS 365 Mass chemotherapy will rapidly reduce the pre- has in Europe and North America. What is uncertain is valence and intensity of hookworm infection. The whether limited and specific improvements can either benefits may be short lived, however, in the absence of reduce infection or maintain lower levels following a improvements in sanitation and education, and mass treatment campaign. Existing studies indicate precontrol prevalence rates and intensities of infection not, but such studies have generally been very deficient recur within t-5 years of the drug campaign. Some in behavioral observation, and behavior is all important studies on the fall and subsequent rise of hookworm in the success of any excreta disposal program. Poorly prevalence following mass chemotherapy are listed in used and maintained latrines will clearly not reduce table 22-2. ancylostomiasis, and they may act as new foci for transmission. Toddlers (1-3 years old) may continue to Environmental defecate around the home and transmit infection to their siblings. Even if excreta disposal is improved Improvements in excreta disposal facilities, in areas around the home, it may be unaffected in the fields or of high prevalence, have failed to achieve a marked work places where transmission may continue impact (table 22-3). In some studies, a combination of unchecked. More work is required on this topic, and it mass chemotherapy and improved sanitation has should incorporate detailed observations on behavior failed to affect the prevalence in the long term but has and studies of community acceptance and attitude. caused a marked decrease in the intensity of infection. Available evidence indicates that excreta disposal Other studies have indicated that the treatment of programs will fail to control hookworm infection night soil used as a fertilizer, combined with mass by themselves. They have a valuable ancillary role to chemotherapy, is effective in reducing the prevalence play, however, in conjunction with: (and presumably the intensity) of infection. This is probably due to a reduction in transmission to people * Mass repeated specific chemotherapy working in fertilized fields. It is to be expected that * Mass oral iron therapy night soil treatment will be particularly effective in * Increased use of footwear communities where prevalences are not extremely * Intensive health education campaigns high, where most transmission occurs in the fields, and * Development of basic health services and where hygiene in and around the home is relatively infrastructure. good. There can be no doubt that a massive improvement This approach reduced the national prevalence of in hygiene and excreta disposal would greatly reduce hookworm infection in South Korea from 39 percent in the prevalence and intensity of ancylostomiasis, as it 1949 to 7 percent in 1972 (Soh 1973). Table 22-2. Some studies on the effect of mass chemotherapy on hookworm infection Country Drug Source Bangladesh Pyrantel Mackay and others (1979) Brazil Chenopodium Smillie (1922) Costa Rica Thiabendazole Arguedas and others (1975) Iran Piperazine and bephenium hydroxynaphthoate Arfaa and others (1977) Japan ND Kawagoe and others (1958) ND Kozai (1962) 1-bromo-2-naphthot Kutsumi (1969) Panama Tetrachloroethylene and chenopodium Cort, Schapiro and Stoll (1929) ND Sweet and others (1929) Puerto Rico ND Hill (1925, 1926) Thailand Pyrantel Bhaibulaya and others (1977) Zaire Levamisole Jancloes. Cornet and Thienpont (1979) ND No data. 366 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Table 22-3. Some studies on environmental influences on hookworm infection Country Result Source Brazil Sanitation was effective in reducing hookworm intensity Smillie (1922) but not prevalence Costa Rica Hookworm prevalence was associated with type of house Moore, de la Cruz and Vargas floor and wearing shoes but not with sanitation Mendez (1965) Egypt A village receiving improved water supplies, latrines, and Chandler (1954) refuse collection had a lower prevalence (10 percent) of hookworm than a village with unimproved sanitation (28 percent) Improved sanitation did not reduce hookworm prevalence Scott and Barlow (1938) Iran Water and sanitation improvements had almost no impact on Arfaa and others (1977) prevalence and a modest impact on intensity of hookworm infection; water and sanitation improvements plus regular mass chemotherapy added nothing to the impact of mass chemotherapy alone Japan Heat treatment of night soil using firewood led to reduced Katayama (1955) prevalence of hookworm infection Night soil treatment, by heating with electricity, did not Kawagoe and others (1958) reduce hookworm prevalence, but delayed reinfection following mass chemotherapy Night soil treatment with sodium nitrite and calcium Kozai (1960a, 1960b, 1960c and 1962) superphosphate reduced but did not prevent reinfection of hookworm following mass chemotherapy Night soil treatment with thiabendazole reduced transmission Kutsumi (1969) of hookworm Panama Sanitation delayed reinfection following mass chemotherapy Cort, Schapiro and Stoll (1929) Sanitation delayed reinfection (especially in females) following Sweet and others (1929) mass chemotherapy Puerto Rico Sanitation delayed reinfection following mass chemotherapy Hill (1925, 1926) Singapore Poor families rehoused in modern flats had a hookworm Kleevens (1966) prevalence of 1.0 percent compared with that of squatters (2.2 percent) USA California Rehousing mental patients in modern buildings interrupted Jeffery (1960) hookworm transmission Virginia Sanitation appeared to be effective in reducing hookworm Cort, Otto and Spindler (1930): Otto prevalence and intensity and Spindler (1930) Occurrence and Survival in the dissemination of hookworm eggs and larvae in the Environment environment. There has also been little interest in the survival of hookworm eggs in the environment because Hookworm eggs and larvae in nature have been they are known to be less hardy than Ascaris eggs, and found mainly in soil at places where people defecate, or the latter therefore provide a better indicator organism where night soil is applied to fields, and it is at these for environmental helminthology. same sites that most percutaneous infection takes place. Eggs and larvae are also found on crops In water contaminated by night soil, sewage, or sludge. This pattern of contamination and infection has meant that Hookworm eggs will tend to settle in water and there has been little interest in the possible wider eventually die in the bottom sediments. Their survival ANCYLOSTOMA, NECATOR, AND ANCYLOSTOMIASIS 367 in seawater has been reported as under 5 hours, examined sludges from California, Georgia, Indiana, compared with over 30 hours for Ascaris eggs under Kentucky, Montana, Ohio, and Wisconsin and found the same experimental conditions (Livingstone 1978). hookworm eggs only in the sludge from Frankfort, In river water hookworm eggs can probably survive for Indiana (Theis, Bolton and Storm 1978). An earlier a few weeks. survey of hookworm eggs and larvae in sludges in the USA was reported by Wright, Cram and Nolan (1942). Hookworm eggs do not survive for long in sludge In feces and night soil under tropical conditions. In Colombo (Sri Lanka) High concentrations of hookworm eggs are found in hookworm eggs could not be recognized microscopi- feces and night soil in endemic areas. Studies in Canton cally after 43 days in sludge at 27'C and could not be (China) in the 1920s recorded up to 85,000 viable cultivated after 23 days (Hirst 1932). hookworm eggs per liter of night soil (Oldt 1926). More recent studies from China found 840 eggs per In soil liter (McGarry and Stainforth 1978). Survival times of hookworm eggs in feces and night Under unfavorable conditions in soil (too hot, too soil are considerably less than those of Ascaris eggs. In cold, or too dry), hookworm eggs will either die or fail southern China, hookworm eggs in night soil and to develop and hatch. In either case they pose no risk. water mixtures were dead after 6-12 weeks (Oldt 1926). Under favorable conditions they will hatch and the More recent work in China showed that hookworm resulting larvae will survive for less than 12 weeks. eggs in biogas plant liquor at 9-18'C were reduced by Experiments on A. duodenale eggs in sterilized sandy 77 percent after 20 days, and by 99.5 percent after 70 soil in India (Vinayak, Chitkara and Chhuttani 1979) days in winter (McGarry and Stainforth 1978). Similar showed that in the hot dry months eggs hatched after results were reported by the Szechwan Research 9-17 days, and the larvae survived for an average of 24 Institute (1974). Petrik (1954) considered that days. During the monsoon the eggs hatched after 5- Ancylostoma eggs did not survive for more than 3 12 days, and the larvae survived for an average of 90 weeks in stored excreta at 20 22°C. days; in winter the equivalent periods were 45-62 days and 33 days. Clearly, warm wet conditions favor rapid In sewage hatching and prolonged larval survival. This was also found during experiments on A. caninum larvae At Daspoort (South Africa) settled sewage contained on grass plots at Urbana, USA (Mark 1975). Mean 6 hookworm eggs per liter (Nupen and de Villiers 1975). larval survival times were < 1 day during Very much higher concentrations may be expected in December-February, 7 days during March-July, and sewage from poor communities in developing count- 24 days during August-November. ries. Sewage in Colombo (Sri Lanka) in the 1920s It may be expected that under field conditions larval contained up to 330 hookworm eggs per liter (Hirst survival in soil is shorter than recorded in laboratory 1932). More recent data from Calcutta (India) showed experiments with sterilized soil. Even under ideal that there were 22-750 hookworm eggs per gram of conditions (shaded, moist, sandy loam), over 99 BOD5 in the sewage (Bhaskaran and others 1956). percent of larvae die within 1 month (Banwell and Assuming a sewage strength of 250 milligrams of BOD5 Schad 1978). per liter, a hookworm egg concentration of 6-188 per The microhabitat of the hookworm larvae in soil is liter may be computed. Lakshminarayana and the moisture film surrounding the soil particles. If the Abdulappa (1969) detected up to 254 hookworm eggs larvae are near or on the surface and the moisture film per liter of sewage in Nagpur (India). dries, they will rapidly die from desiccation. In a loamy soil, larvae can move downwards to protect themselves In sludge from desiccation and bright sunlight. Following rain, they will move up to the surface again where they are at Sludge from sewage treatment plants in areas of risk if the soil surface dries out very rapidly after a endemic hookworm may be expected to contain shower (Beaver 1953). substantial hookworm egg concentrations. In Colombo (Sri Lanka) in the 1920s up to 96,000 On crops hookworm eggs per liter of sludge from Imhoff tanks were recorded (Hirst 1932). In other areas hookworm After rain, the moisture film on the surface soil eggs will be uncommon in sludge. A survey in the USA particles may be continuous with the moisture films on 368 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS low vegetation, and hookworm larvae can make their obscures the fact that most eggs not found in the way up onto leaves and stems. If the plant surfaces dry effluent have not been destroyed but are merely out, the larvae will rapidly die unless they are secluded concentrated in the sludge. Conventional sewage in the axillae or other moisture-retaining and sheltered treatment plants have short retention times and sites. Vegetable contamination by hookworm larvae is operate at ambient temperatures and therefore do not of importance in A. duodenale endemic areas only, destroy hookworm eggs. Their role is to transfer the since it is this species that can readily infect via the oral, eggs from the liquid fraction (the effluent) to the solid as well as the percutaneous, route. fraction (the sludge). In countries where night soil is widely used to fertilize vegetables, hookworm larvae are commonly isolated from market produce. In South Korea, for By septic tanks instance, Choi (1970) isolated hookworm eggs and Most hookworm eggs will settle in septic tanks and larvae from leafy vegetables, watercress, and carrots. be eventually removed in the sludge. Bhaskaran and Vegetables suspected of being contaminated may be others (1956) reported 72 percent removal of soaked in a solution of iodine or other ovicidal hookworm eggs by a septic tank and trickling filter bed chemical. Iodine concentrations needed to destroy in Calcutta (India). McGarry and Stainforth (1978) hookworm eggs are roughly double those required to reported studies in China on a biogas plant, which may kill larvae (Thitasut 1961). It is simpler and more be likened to a septic tank with a long retention time. reliable, however, to soak the vegetables in warm water The influent contained hookworm eggs in 87 percent of (60°C) for 10 minutes. samples, with an average concentration of 840 per liter: the effluent contained hookworm eggs in 23 percent of samples, with an average concentration of 4 per liter. Inactivation by Sewage Treatment Processes sB conventional treatment Large numbers of hookworm eggs enter sewage Bhaskaran and others (1956) studied sewage treatment plants in endemic areas. The fate of treatment plants in the Calcutta area (India). hookworm eggs during sewage treatment is similar to Hookworm egg removals were 46 percent by 1.5 hours that of Ascaris eggs (discussed in greater detail in sedimentation (compared with 67 percent for Ascaris), chapter 23). The two major differences are that 75 percent by 2 hours sedimentation (75 percent for hookworm eggs are less dense and that they may hatch. Ascaris), 100 percent by an experimental trickling filter Hookworm eggs are of similar size to Ascaris eggs plant, and 81 and 96 percent by two activated sludge but they have a lower specific gravity (1.055 compared plants. with 1.1 I). Hookworm eggs therefore have a lower Panicker and Krishnamoorthi (1978) reported on settling velocity and thus are less prone to removal by hookworm egg removal by a variety of sewage sedimentation processes (Cram 1943). Sedimentation treatment plants in India (table 22-4). Removal rates is the main mechanism of removal of helminth eggs for hookworm eggs are consistently less than those for during sewage treatment, and therefore reported Ascaris eggs, and this is almost certainly due to the removals for hookworm eggs are typically a little less lower specific gravity of hookworm eggs and the than those for Ascaris eggs. resultant poorer removal by sedimentation. Unlike Ascaris eggs, hookworm eggs may hatch during sewage treatment. Cram (1943) observed the By waste stabili.ation ponds hatching of hookworm eggs on trickling filter stones, in activated sludge tanks, and in drying sludge. Larvae Waste stabilization ponds are able to eliminate will tend to stay in the liquid fraction and be carried out hookworm eggs completely and reliably. Table 22-4 in the effluent; the eggs, however, tend to be indicates that two pond systems in India achieved this, concentrated in the sludge. The larvae may survive in whereas two other pond systems did not. No design sewage for up to 5 days (Cram 1943), which is quite details are given by Panicker and Krishnamoorthi sufficient for them to be discharged in the effluent and (1978) for these ponds, but it is certain that ponds not carried some distance. removing hookworm eggs are poorly designed or Hookworm egg removal by sewage treatment is poorly operated or both. Earlier research in India had generally quoted as a percentage reduction in shown that some hookworm eggs will hatch in aerobic concentration between influent and effluent. This waste stabilization ponds and that the larvae may be ANCYLOSTOMA, NECATOR, AND ANCYLOSTOMIASIS 369 Table 22-4 Reduction of belminth eggs by sewage treatment processes in India Trichuris Taenia Process Hookwvorma Ascaris Hymenolepis trichiura spp. Two hours' sedimentation 80 96 90 90 75 Complete activated sludge plant 85 98 95 100 ND Two complete trickling filter plants 82 95 80 93 ND 92 96 89 100 ND Pilot-scale biodisc plant with 1 hour of secondary 50 79 60 60 ND sedimentation Pilot-scale oxidation ditch with secondary 81 94 89 100 100 sedimentation Pilot-scale aerated lagoon without secondary 70 92 78 100 100 sedimentation Four waste stabilization pond systems 93 100 too too 100 88 100 100 100 100 100 100 too 100 100 100 100 too too ioo ND No data. Souirce: These data all taken from Panicker and Krishnamoorthi (1978). Note: Percent reductions refer to influent compared with effluent. Most eggs not found in the effluent are concentrated in the raw sludge. a. Ancylostoma duodeoiale and Necator americaonus. found in the effluent (Lakshminarayana and moist hookworm larvae will still be able to rise to the Abdulappa 1969). In a three-cell pond system with only surface. 6 days' overall retention time, all hookworm eggs settled in the first and second ponds, but some larvae By digestion passed into the final effluent. Sludge digestion at temperatures below 40°C does not eliminate hookworm eggs (Petrik 1954). Cram By tertiary treatment (1943) found that hookworm eggs did not develop in Tertiary treatment of secondary effluents by digesting sludge but that they could survive for up to 64 filtration, land treatment, or lagooning will remove the days at 20°C and 41 days at 300C. remaining hookworm eggs (Cram 1943). Effluent chlorination will have little effect on hookworm eggs. By ouicides and laruicides The addition of chemical ovidices and larvicides to Inactivation by Night Soil and Sludge night soil and sludge is a treatment option. Treatment Processes Thiabendazole (Kutsumi and Komiya 1965) and several other chemicals (see, for instance, Sturrock Hookwormeggsandlarvaearelessresistanttonight 1966} have been tried or proposed. Hookworm eggs soil and sludge treatment processes than Ascaris eggs. are considerably less resistant to ovicides than Ascaris If the recommendations on Ascaris egg destruction are eggs, and the treatments found effective against Ascaris followed (chapter 23), the destruction of hookworm (table 23-4) will certainly eliminate hookworm. For eggs is guaranteed. instance, the concentrations of thiabendazole nec- The application to pasture or arable land of raw or essary to destroy helminth eggs in 3 days in night soil at inadequately treated sludges containing hookworm 15°C were 100 milligrams per liter for Ascaris, 6 eggs is especially undesirable because, once eggs are in milligrams per liter for Trichuris, and 1.6 milligrams the soil, development will continue and infective larvae per liter for hookworms (Kutsumi and Komiya 1965). will be produced. The risks may be reduced by This approach to night soil treatment will, however, be plowing the sludge deeply in. or by injecting it below the impractical and unaffordable in many circumstances. surface (Romanenko 1967), but if the soil is loose and Of greater interest is the possibility that some chemical 370 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS fertilizers when added to night soil or sludge may have hookworm eggs, and time-temperature combinations the combined effect of enhancing the agricultural value that destroy the former (see figure 23-2) will certainly of the product and eliminating hookworm eggs and destroy the latter. Data on time-temperature com- larvae. Oldt (1926) in China found that ammonium binations required to destroy hookworm eggs are sulphate, lime, and gypsum were effective, whereas presented in figure 22-4. Table 22-5 presents data on Penso (1933) in Italy preferred ferrous sulphate. In the upper and lower temperature tolerances for A. Japan, the application of sodium nitrite to night soil duodenale and N. americanus eggs and larvae. Clearly, that had been acidified by adding calcium super- eggs are considerably more resistant than larvae to phosphate controlled hookworm eggs in the night soil both heat and cold. Also, N. americanus is more and also delayed reinfection in the community tolerant of higher temperatures and A. duodenale of following mass chemotherapy (Kozai, 1960a, 1960b, lower. This is one underlying factor in their geographical 1960c and 1962). distribution. The most practical method of achieving the elevated By drying temperatures needed to destroy hookworm eggs and larvae is by composting as described below. In Japan, Cram (1943) found that hookworm eggs hatched in heating night soil with firewood (Katayama 1955), or drying sludge and that the larvae remained viable for with cheap-rate night-time electricity (Kawagoe and up to 62 days until the moisture content of the others 1958), has been found to kill hookworm eggs in sludge had fallen to 10 percent. At warmer tempera- night soil and to reduce hookworm infection in the tures, hookworm elimination in sludge is more rapid; community. These techniques use large amounts of Hirst (1932), working in Sri Lanka, suggested that 1 energy, however, and are not generally applicable. month of sludge storage would eliminate hookworm eggs. By composting By heating Composting of night soil or sludge with garbage, woodchips, or other suitable carbonaceous bulking Ascaris eggs are considerably more hardy than material is highly effective in eliminating hookworm . 60 6 x0 a- 0/ det-to ofhowrmeg ndlra ss- ZON _s 5s- 50 45- x x - 45 40 . - 40 35- -_ 35 0U 0 30 X - 30 2 - 2 5r * e o 2 y5 E 20- *-x 20 e 2. Tx 10oftm destruction of hookworm eggs and larvae T p p a 10o u wIess than 100% destri cti of hoonworm eggs and larerae a -10 5f 5 C 1 1 10 o 1 cl00 1 0 1000 l o o lhour Ilday lweek lmonth Iyear TIME (HOURS) Figure 22-4. The inft'uence oJ'time and temperature on hookworm eggs and larurae. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death. See also table 22-5 ANCYLOSTOMA. NECATOR, AND ANCYLOSTOMIASIS 371 Table 22-5. Tolerance of hookworm eggs and larvae to high and low temperatures Ancylostoma duodenale Necator americanus Temperature limit Eggs Larvae Eggs Larvae Upper 50°C for 5 minutes 45°C for 5 minutes 50'C for 5 minutes 50°C for 5 minutes 60°C for 1 minute 50°C for 1 minute 650C for 1 minute 55°C for 1 minute Lower -50C for 9 hours 0°C for 7 days -5°C for 9 hours 5°C for 1 day (41 percent dead (93 percent dead after 3 hours) after 3 hours) Note: See also figure 22-4. eggs and larvae. Time-temperature combinations treatment processes on the survival of intestinal parasites. shown in figure 22-4 must be achieved throughout the Indian Journal of Medical Research, 44, 163-180. compost pile. Hookworm eggs may hatch before Biswas, H., Sehgal, Saraljit, Arora, R. R. and Mathur, K. K. temperatures have risen, and the resulting larvae may (1978). Intestinal parasites and different species of migrate to the cooler edges of the pile. Regular turning hookworm in slum dwelling people around Delhi. Journal or good pile insulation is therefore required. of Communicable Diseases, 10, 234-237. Bray, R. S. and Harris, W. G. (1977). The epidemiology of Studies on hookwortedfrm einatiHon byd comot ting 195infection with Entamoeba histolytica in The Gambia, West have been reported from China (Hou and othersl1959; Africa. Transactions of the Royal Society of Tropical Oldt 1926), Sri Lanka (Nicholls and Gunawardana Medicine and Hygiene, 71, 401-407. 1939), and the USSR (Gudzhabidze and Lyubchenko Chandler, A. C. (1954). A comparison of helminthic and 1959). Other studies are reviewed by Petrik (1954) and protozoan infections in two Egyptian villages two years Wiley (1962). Ascaris eggs are considerably more after the installation of sanitary improvements in one of resistant to composting than hookworm eggs; in areas them. American Journal of Tropical Medicine and Hygiene, where both nematodes are endemic, it therefore is 3, 59-73 preferable to monitor Ascaris eggs in the final compost. Choi, D. W. (1970). Incidence of parasite eggs attached to vegetable leaves, watercress and carrots. Korean Journal of Parasitology, 8, 19. Cort, W. W., Otto, G. F. and Spindler, L. A. (1930). Literature Cited Investigations on Ascaris lumbricoides and the associated intestinal helminths of man in southwestern Virginia. Arfaa, F., Sahba, G. H., Farahmandian, I. and Jalali, H. American Journal of Hygiene, 11, 1-55. (1977). Evaluation of the effect of different methods of Cort, W. W., Schapiro, L. and Stoll, N. R. (1929). A study of control of soil-transmitted helminths in Khuzestan, reinfection after treatment with hookworm and Ascaris in southwest Iran. American Journal of Tropical Medicine and two villages ini Panama. American Journal of Hygiene, 10, Hygiene, 26, 230-233. 614-625. Arguedas. G. J. A., Villarejos, V. M., Swartzwelder, J. C., Cram, E. B. (1943). The effect of various treatment processes Chavarria, A. P., Zeled6n, R. and Kotcher, E. (1975). on the survival of helminth ova and protozoan cysts in Community control of Strongyloides stercoralis by sewage. Sewage Works Journal, 15, 1119-1138. thiabendazole. Texas Reports on Biology and Medicine. 33, Faust, E. C. and Mugaburu, L. G. (1965). Parasitologic 265-268. surveys in Cali, Departamento del Valle, Colombia. XI. Banwell, J. G. and Schad, G. A. (1978). Hookworm. Clinics in Intestinal parasites in Ward Silcoe, Cali, during a four-year Gastroenterology, 7, 129-156. period 1956-1960. American Journal of Tropical Medicine Beaver, P. C. (1953). Persistence of hookworm larvae in soil. and Hygiene, 14, 276-289. American Journal of Tropical Medicine and Hygiene. 2, Fulmer, H. S. and Huempfner, H. R. (1965). Intestinal 102-108. helminths in eastern Kentucky: a survey in three rural Bhaibulaya. M., Punnavutti, V., Yamput, S.. Indra-Ngarm, counties. American Journal of Tropical Medicine and S., Pahuchon, W., Hongsuwan, S., Vajsasthira, S. and Hygiene, 14, 269-275. Harinasuta, C. (1977). Control trial of soil-transmitted Ghadirian, E., Croll, N. A. and Gyorkos, T. W. (1979). Socio- helminthic infections with pyrantel pamoate. Southeast agricultural factors and parasitic infections in the Caspian Asian Journal of Tropical Medicine and Public Health, 8, littoral region of Iran. Tropical and Geographical Medicine, 329-334. 31, 485-491. Bhaskaran, T. R., Sampathkumaran, M. A., Sur, T. C. and Gudzhabidze, S. I. and Lyubchenko, S. D. (1959). Control of Radhakrishnan, I. (1956). Studies on the effect of sewage ascariasis and ancylostomiasis by composting of organic 372 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS waste material. Meditsinskaia Parazitologiia i effect of sewage stabilization ponds on helminths. In Low Parazitarnye Bolezni, 28, 576-578. Cost Waste Treatment, ed. Sastry, C. A., pp. 290-299. Hill. R. B. (1925). Hookworm reinfestation in sanitated and Nagpur. India: Central Public Health Engineering unsanitated areas. Southern Medical Journal, 18, 665-668. Research Institute. (1926). Hookworm reinfestation for three years after Livingstone, D. J. (1978). Decay of micro-organisms in the treatment in a sanitated area in Porto Rico and its bearinig marine environment. In Proceedings of tle S-vmposiunn on on permanent hookworm control in the group studied. Disinfection of' Water. Pretoria, South Africa: National American Journal of' Hygiene, 6 (July supplement). Institute for Water Research. 103-117. Lo. E. K. C.. Varughese, J.. Ghouse, A. and Noor. M. (1979). Hirst, L. F. (1932). Hookworm disease and Ceylon sewage Helminthiases in peninsular Malaysia-prevalence and works. Ceylon Journal of'Science. Section D, 2, 245-275. density of infestation of hookworm. Ascaris and Trichuris Hou, T. C., Chung. H. L., Ho, L. Y. and Weng, H. C. (1959). in rural school children. Medical Journal of'Malaysia, 34. Achievements in the fight against parasitic diseases in New 95-99. China. Chinese Medical Journal, 79. 493-520. McGarry, M. G. and Stainforth, J. (1978). Conmpost. Fertili-er Hsieh, H. C. (1970). Studies on endemic hookworm. I. Survey and Biogas Production ftomn Hutman and Farm Wastes in the and longitudinal observation in Taiwan. Japanese Journ-al People's Republic of' China. Ottawa: International of Parasitology, 19, 508-522. Development Research Centre. Jancloes, M. F., Cornet, P. and Thienpont, D. (1979). Mass Mackay,D. M.,Ahmad,T.,AliT. andAliS. (1979). Pyrantel control of ascariasis with single oral doses of levamisole. in the mass eradication of roundworm and hookworm. Tropical and Geographic Medicine, 31. 111-122. Health anzd IHygiene, 2, 123-125. Jeffery, G. M. (1960). A three-year epidemiologic study of Maplestone, P. A. (1930). Seasonal variation in hookworm intestinal parasites in a selected group of mental patients. infection. Indian Journal of Medical Research. 18, 685-698. American Journal of Hygiene, 71. 1-8. (1932). Further observations on seasonal variation in Jones, H. 1. (1976). A study of human intestinal helminthiases hookworm infection. Indian Journal of Medical Research, on Kar Kar Island, Madang Province. Paputa Newt Guinea 19, 1145-1151. Medical Journal, 19, 165-172. Mark, D. L. (1975). Survival of Ancylostomna caninium on Katayama, Y. (1955). Sanitary treatment of human excreta bluegrass pasture. Journal of Parasitology, 61, 484-488. by heating process. 16. Effect of the treatment applied to a Massoud, J., Arfaa, F., Jalali, H. and Keyvan, S. (1980). farm-village (Part I1. Japanese Journal of thie Nation's Prevalence of intestinal helminths in Khuzestan, south- Health, 24, 1-12. west Iran, 1977. American Joulrnlal of 'Tropical Medicinie and Kawagoe. K., Nishi, H., Shibata, E. and Yamada, S. (1958). Hygiene, 29, 389-392. On the effect of nightsoil treatment by heating process Miller, T. A. (1979). Hookworm infection in man. Adranices in utilizing surplus midnight electric power upon the Parasitology. 17, 315-384. incidence of parasitic infection of farmers. Japanese Moore, H. A., de la Cruz, E. and Vargas-Mendez, 0. (1965). Journal of the Nation's Health, 27, 162-165. Diarrheal disease studies in Costa Rica. IV. The influence Kleevens. J. W. L. (1966). Re-housing and infections by soil- of sanitation upon the prevalence of intestinal infection transmitted helminths in Singapore. Singapore Medical and diarrheal disease. American Journal of Epidemiology, Journal, 7, 12-29. 82, 162-184. Kozai, 1. (1960a). Re-evaluation of sodium nitrite as an Nagalingam, I., Lam, L. E., Robinson, M. J. and Dissanaike. ovicide used in nightsoil (1). Japanese Journal of A. S. (1976). Mebendazole in treatment of severe Trichluris Parasitology, 9, 202-210. trichiura infection in Malaysian children. American (1960b). Re-evaluation of sodium nitrite as an ovicide Journal of Tropical Med icine and Hygiene. 25, 568-572. used in nightsoil (2). Japanese Journal of'Parasitology. 9, Nawalinski, T.. Schad, G. A. and Chowdhury, A. B. (1978a). 519-528. Population biology of hookworms in children in rural (1960c). Re-evaluation ofsodiumnitriteasan ovicide West Bengal. 1. Generail parasitological obserxations. used in nightsoil (3). Japanese Journal oj Parasitology, 9. American Journal of Tropical Medicine and Hygiene. 27, 529-540. 1152-1161. (1962). Re-evaluation of sodium nitrite as an ovicide (1978b). Population biology of hookworms in used in nightsoil (4). Japanese Journal of'Parasitology, 11, children in rural West Bengal. II. Acquisition and loss of 400-410. hookworms. American Journal of Tropical Medicine and Kutsumi, H. (1969). Epidemiological study on the preventive Hygiene. 27, 1162-1173. effect of thiabendazole as an ovicide against human Nicholls, L. and Gunawardana, S. A. (1939). The destruction hookworm, Trichuris and Ascaris infections. Japanese ofhelminth ovain nightsoil by composting. Ceylon Journal Journal of'Medical Science and Biology, 22, 51-64. oj Science, Section D, 5, 1-9. Kutsumi, H. and Komiya, Y. (i965). Effect of thiabendazole Nozais. J. P., Dunand. J. and Le Brigant. S. (1979). as an ovicide on helminth eggs in nightsoil. Japane.se Repartitions d'Ascaris lunbricoides. de Necator amer- Journal oj Medical Science and Biology. 18, 203-224. icanus et de Triclhuris tricIhiura dans 6 villages de Cote Lakshminarayana, J. S. S. and Abdulappa. M. K. (1969). The d'Ivoire. Medicine Tropicale, 39, 315-318. ANCYLOSTOM.4, NECATOR, AND ANCYLOSTOMIASIS 373 Nupen, E. M. and de Villiers, R. H. (1975). The Eualuation of Seo, B. S., Rim, H. J., Loh, I. K.. Lee, S. H., Cho. S. Y., Park, S. Pathogenic Parasites in Water Environments. Project C., Bae, J. W., Kim, J. H., Lee, J. S.. Koo, B. Y. and Kim, K. Report No. 13. Pretoria: National Institute for Water S. (1969). Study on the status of helminthic infections in Research. Koreans. Korean Journzal of Parasitology, 7, 53-70. Oldt, F. (1926). XIII. Studies on the viability of hookworm Smillie, W. G. (1922). Studies on Hookwvorm Infection in eggs in stored nightsoil in South China. American Journal BraZil. 1918-1920. Second paper, Monograph no. 17. New of Hygiene Monographic Series No. 7, 265-291. York: The Rockefeller Institute for Medical Research. Otto, G. F., Cort, W. W. and Keller, A. E. (1931). Soh. C. T. (1973). Control of soil-transmitted helminths in Environmental studies of families in Tennessee infested Korea. A progress report. Yonsei Reports on7 Tropical with Ascaris, Trichuris and hookworm. Americanz Journal Medicine, 4, 102-125. of Hygiene, 14, 156-193. Sturrock, R. F. (1966). Chemical control of hookworm Otto, G. F. and Spindler, L. A. (1930). Effect of partial larvae. [Correspondence.] Lancet, 2, 1256-1257. sanitation on infestation with intestinal parasites in Sweet, W. C., Cort, W. W., Schapiro, L., Stoll, N. R. and Riley, southwest Virginia. Southern Medical Journal, 23, W. A. (1929). VI. A study of the effect of treatment and 556-561. sanitation on the level of hookworm infestation in certain Oyerinde, J. P. 0. (1976). The role of the housefly (Musca areas in Panama. American Journal ofHygiene Moniograpl domestica) in dissemination of hookworm. Annals (f Series No. 9, 98-138. Tropical Medicine and Parasitology, 70, 455-462. Szechwan Research Institute of Antiparasitic Diseases and Panicker, P. V. R. C. and Krishnamoorthi, K. P. (1978). Mienchu County Antischistosomiasis Office, Szechwan. Elimination of enteric parasites during sewage treatment (1974). Digestion of nightsoil for destruction of parasite processes. Indian Association for Water Pollution Control ova. A report of investigation and experimental obser- Technical Annual, 5, 130-138. vation. Chinese Medical Journal, 93, 31. Penso, G. (1933). Studies on ancylostomiasis. Chemical Theis, J. H., Bolton, V. and Storm, D. R. (1978). Helminth ova fertihzers in ancylostomiasis prophylaxis in rural areas. in soil and sludge from twelve U.S. urban areas. Journal of Annali d'lgiene Sperimnentale, 5, 352-360. the Water Pollution Control Federation, 50, 2485-2493. Petrik, M. (1954). Utilization of nightsoil, sewage and sewage Thitasut, P. (1961). Action of aqueous solutions of iodine on sludge in agriculture. Bulletin of the World Health fresh vegetables and on the infective stages of some Organization, 10, 207-228. common intestinal nematodes. American Journal of Pierce, V., Ascoli, W., de Leon, R. and Gordon, J. E. (1962). Tropical Medicine and Hygiene, 10, 39-43. Studies of diarrheal disease in Central America. Ill. Vinayak, V. K., Chitkara, N. L. and Chhuttani. P. N. (1979). Specific etiology of endemic diarrhea and dysentery in Soil dynamics of hookworm larvae. Indian Journal of Guatemalan children. American Journal of Tropical Medical Research, 70, 609-614. Medicine and Hygiene, 11, 395-400. Warren, K. S. (1974). Helminthic diseases endemic in the Raccurt, C., Vial, P. and Pierre-Louis, J. M. (1977). Etude United States. American Journal of Tropical Medicine and epidemiologique des helminthiases intestinales A ]'ile de la Hygiene, 23, 723-730. Tortue (Haiti). 2. Bulletin de la Societe de Pathologie Wenlock, R. W. (1979). The epidemiology of tropical Exotique et de ses Filiales, 70, 240-249. parasitic diseases in rural Zambia and the consequences Roche, M. and Layrisse, M. (1966). The nature and causes of for public health. Journal of Tropical Medicine and "hookworm anemia". American Journal of Tropical Hygiene, 82, 90-98. Medicine and Hygiene, 15, 1029-1100. Wiley, J. S. (1962). Pathogen survival in composting Romanenko, N. A. (1967). Sanitary and helminthological municipal wastes. Journal of the Water Pollution Control evaluation of some new methods for treating sewage sludge Federation, 34, 80-90. used in agriculture. Meditsinskaia Parazitologiia i Wright, W. H., Cram, E. B. and Nolan, M. 0. (1942). Parazitarnye Bolezni, 36, 188-189. Preliminary observations on the effect of sewage treatment Schad, G. A., Chowdhury, A, B., Dean, C. G., Kochar, V. K., processes on the ova and cysts of intestinal parasites. Nawalinski, T. A., Thomas, J. and Tonascia, J. A. (1973). Sewiage Works Journal, 14, 1274-1280. Arrested development in human hookworm infections: an Yan, C. W., bin Ishak, F., Hee, G. L., Devaraj, J. M.. bin adaptation to a seasonally unfavourable external environ- Ismail, K., Jalleh, R. P.. Peng, T. L. and Jalil, T. M. bin A. ment. Science, 180, 502-504. (1978). The problem of soil transmitted helminths in Scott, J. A. and Barlow, C. H. (1938). Limitations to the squatter areas around Kuala Lumpur. Medical Journal of control of helminth parasites in Egypt by means of Malaysia, 33, 34-43. treatment and sanitation. American Journal of Hygiene, 27, 619-648. 23 Ascaris and Ascariasis AsCARIASIS IS AN INFECTION of particular importance has been estimated that a child who has twenty-six to those engaged in sanitation programs because it is worms may lose 10 percent of his total daily intake of extremely common in most parts of the world and protein. There is also evidence that ascariasis in because the eggs of the Ascaris worm are very children may contribute to vitamin A and C persistent in the environment and difficult to eliminate deficiencies. The effect on child growth of light by sewage or night soil treatment processes. Ascaris infections, and the nutritional benefits from regular deworming, are subjects of current debate and research (Freij and others 1979; Gupta and others Description of Pathogen and Disease 1977; Stephenson 1980; Stephenson and others 1980; Willett, Kilama and Kihamia 1979). Knowledge of the biology and epidemiology of Diagnosis is by microscopic identification of the ascariasis is extensive, and only a brief summary is eggs in the feces. The number of eggs counted gives an presented in this section. indication of the number of adult worms present. Identification Occurrence Ascariasis is a helminthic infection of the Ascariasis occurs worldwide and especially in warm small intestine by the human roundworm, Ascaris climates and among poor people. It is one of the most lumbricoides. About 85 percent of infections are prevalent human helminths and infects 700-1,000 symptomless, although the presence of even a few million people. Prevalence and intensity of infection worms is potentially dangerous. The earliest symptoms are particularly high in preschool and young school are a pneumonitis with cough, dyspnea, substernal children, among whom prevalences of 60-90 percent pain, fever, moderate eosinophilia, and sometimes are reported. The fatality rate is about 0.02 percent and blood-stained sputum (which may contain larvae). higher in children. This is known as Loeffler's syndrome. These symptoms begin 5-6 days after infection, usually last 10-12 days, Infectious agent and are caused by the Ascaris larvae migrating and developing. A. lumbricoides, a nematode, is the roundworm of Heavy burdens of adult worms in the small intestine man. Females are 200-400 millimeters in length, may cause digestive disorders, nausea, abdominal pain, whereas males are 150-300 millimeters (figure 23-1). vomiting, restlessness, and disturbed sleep. Adult The fertile eggs are ovoid and measure 45-70 worms may be passed in the feces or by mouth. Serious micrometers by 35-50 micrometers. The pig round- complications, especially among children, include worm, A. suum, closely resembles A. lumbricoides. bowel obstruction (figure 23-1) or death due to the There is evidence that A. suum may occasionally migration of the adult worms to the liver, gall bladder, develop to maturity in man and that the larvae can or appendix and, rarely, due to perforation of the cause pneumonitis even if the parasite does not mature. intestine. Several of the studies on Ascaris egg survival reported Where the prevalence and intensity of infection are here use A. suum eggs because they are more readily high, the nutritional consequences of ascariasis in an available. The identical appearance of the eggs of undernourished population may be considerable. It A. lumbricoides and A. suum has almost certainly 375 376 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS _A- j . _~~~j Figure 23-1. Ascaris in situ. Shown is the small intestine of aperson who died from intestinal obstruction caused by large numbers of entangled Ascaris worms. (Photo: Wellcome Museum of Medical Science) confused some of the environmental studies of development will depend on environmental conditions. ascariasis in communi'ties where domestic pigs are Under ideal conditions of moist, shady soil at 22-330C, numerous. a minimum of 10-15 days is required for about 75 percent of freshly passed eggs to become infective. Unfavorable conditions will retard development or Reservoir may even interrupt it completely-to be recommenced on return to a favorable environment. Infective eggs The reservoir of A. luinlbricoides is man. Pigs cnsriefrln eid,ad7yassria nsi and dogs may disperse the undeveloped eggs of hasen s rvieforde.Drn hs long periods, n er uvvli eggs A. liumbroicoides by eating them in human feces and hsbe eodd ui-teeln eid.eg excretng thm late at aother lace.may be widely dispersed from the site of original excretingthem late at anothr place.defecation. When the infective eggs are ingested-on hands. Transmirssion food, utensils, dust, and so forth-the larvae hatch in the duodenum. They are carried in the lymphatics or Female worms lay up to 200.000 eggs per day. The blood vessels, through the liver and heart, to reach the unsegmented. fertilized eggs are passed in the feces, lungs in 3 days. The larvae develop further in the lungs, About 15 percent of the excreted eggs are infertile, and penetrate the air passages. ascend the trachea, are these are longer and narrower than the fertile eggs. swallowed, and pass down the esophagus to reach the They occur either because rapid production of eggs small intestine. They develop into adults in about allows some to pass through unfertilized or because 60-75 davs and then live for up to 1.5 years. only female worms are present. The dominant vehicles for Asnar-is egg ingestion are The first-stage larva in the egg must moult to contaminated fingers, objects that have been placed on produce a second-stage larva before the egg is infective, the ground (and can be sucked by children), dirt from The proportion of eggs that develop and the time of the yard (that can be eaten by children) and ASCARIS AND ASCARIASIS 377 contaminated vegetables. Waterborne transmission is among more wealthy urban children (Pierce and possible but is of very minor importance. Infection may others 1962). In one village in Guatemala. 93 percent of take place by the inhalation of eggs stuck to particles of children had at least one Asccai.s infection between birth wind-blown dust. This is especially likely in dry and and the age of 3 years (Mata and others 1977). Surveys windy regions or seasons. There is practically no firm of preschool children showed prevalences of 11 percent evidence on the degree to which this mode of in Iran, 48 percent in Sri Lanka, 53 percent in transmission takes place, and the subject has scarcely Venezuela, and 69 percent in Bangladesh (van Zijl advanced since the early review by Lane (1934). 1966). There is now a considerable body of evidence to A survey of 4-6 year old children in Kuala Lumpur indicate that ascariasis in highly endemic areas is a (Malaysia) found a prevalence of ascariasis of 64 familial infection. Most transmission occurs when the percent among poor children and 2.5 percent among house, floor, yard, or area around the house is "upper middle class" children (Yan and others 1978). It contaminated by promiscuous defecation by small was noted that, in the poor communities, most adults children. This contaminated soil then reinfects other (90 percent) did not know how these worms are children and adults in the same family. Visitors may transmitted and that children under 10 years old also be infected. Infection is clustered by family and is defecated indiscriminately around the houses because strongly associated with soil contamination around a the rudimentary latrines available were unsafe for family's home. children to use on their own. A study of rural school children (6-12 years old) 72 kilometers from Kuala Prepatent and incuibation periods Lumpur found an 87 percent prevalence of ascariasis (Lo and others 1979). Sanitation facilities did not affect The prepatent period (the interval between ingesting ascariasis prevalences among these children. infective eggs and the appearance of eggs in the stools) There are major unexplained variations among is about 2 months. communities in the prevalence of Ascaris and in the The incubation period (the interval between relative prevalences of Ascaris, Trichiuris. and hook- ingesting infective eggs and the development of worm. These may be related to soil types; it has been symptoms and signs of illness) varies from a few days suggested that hookworm is especially common in (in the case of symptoms due to migrating larvae) to areas of sandy soil, whereas Ascaris rates are highest in several months. The development of clinical illness areas of fine silts and clays. Such theories appear to depends upon the number of worms in the body and have no global validity. Climatic factors certainly the state of health of the host. In many light infections influence egg development in the soil and, therefore, in healthy people, no evidence of illness ever appears. transmission. Temperatures of 20-32°C are ideal, with little development taking place below 18°C. A moist, Period of communicability shady environment also encourages egg development, Adult worms generally live for less than 10 months, and eggs may be killed or inhibited by desiccation or with maximum life spans of up to 1. years. As long as exposure to sunlight (Nolf 1932). Spindler (1929) withre maxili.fesans ofmu ars. Asvlng as concluded that the different moisture requirements of matuestine fertswilbed femalsedwormsarei in the fthe eggs was the primary influence on the variation in the relative prevalences of ascariasis and trichuriasis and caused trichuriasis to be the more common in Resistance wetter areas. whereas the reverse was true in drier Susceptibility is general, but there is evidence of areas. limited immunity. Some children experience decreas- A study of the distribution of ascariasis in Tennessee ing worm burdens despite continuing exposure. (USA) concluded that the marked variations in prevalence were due neither to soil type, rainfall, nor Epidemiology temperature, but to behavior, and especially to the practice of defecating in the yard near the house (Otto, Ascaris infection is extremely common in many Cort and Keller 1931). Similarly, rainfall was found not countries, and there are many hundreds of reports on to be a determining factor in Ascaris distribution in its prevalence in various communities. Surveys of 1-5 Panama (Cort and others 1929), nor soil type in year old children in Guatemala revealed ascariasis Virginia (USA; Cort, Otto and Spindler 1930). prevalences of 46 percent among rural children, 26 In areas where ascariasis is highly endemic, one of percent among poor urban children. and 3 percent two distinct age distributions is found. In some 378 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS communities there is a peak prevalence among are about 2 cases of intestinal obstruction caused by children, typically 70-95 percent in the 5-9 age group, ascariasis per 1,000 preschool children per year there; 3 with prevalence gradually decreasing in older age percent of these cases of obstruction die (Blumenthal groups to 10-50 percent among old adults. This 1977). In the poorer parts of the USA it has been pattern has been reported from China (Cort and Stoll noticed that, whereas the wearing of shoes has caused a 1931), Colombia (Faust and Mugaburu 1965), Haiti considerable decline in hookworm prevalence, Ascaris (Raccurt, Vial and Pierre-Louis 1977), Iran (Massoud and Trichuris remain common (up to 60 percent of and others 1980), Mexico (Biagi and Rodriguez 1960), schoolchildren infected) owing to a lack of adequate Panama (Cort and others 1929), Papua New Guinea improvements in sanitation and hygienic behavior (Jones 1976b), and the USA (Cort, Otto and Spindler (Fulmer and Huempfner 1965). 1930; Schliessmann and others 1958). In other Intensity of infection (the number of worms living in localities there is a high prevalence (typically 40-80 the intestine) is quite as important in the epidemiology percent) in all age groups. This has been found in China of ascariasis as prevalence (the proportion of (Cort and Stoll 1931), Iran (Ghadirian and others persons having at least one worm). Heavy infections 1973; Mobedi, Arfaa and Movafegh 1971; Sahba and have more serious clinical consequences and are the Arfaa 1967), Japan (Kutsumi 1969), Philippines infections most likely to be seen at clinics. In addition, (Cabrera, Arambulo and Portillo 1975), South Korea persons with heavy infections are excreting huge (Seo and others 1969; Soh 1973) and Tunisia (Thiers, numbers of eggs (up to 200,000 per female worm per Lassoued and Abid 1976). day) and are therefore causing considerable potential Possible explanations for these two patterns of age- for transmission. Individual egg outputs of up to about specific prevalence are differences in the parasites or in 300,000 per gram of feces are reported; assuming 100 host reactions. Geographical differences in the grams of feces per day, this suggests at least 150 mature parasites or in immune responses to childhood female worms in the intestine. The ratio of male to infection are theoretically possible although not female worms in the intestine varies from about 0.3 to 1. recorded. Immune response differences between racial Children have higher egg outputs, owing to greater groups are an unlikely explanation because both intensity of infection, than adults. This applies in both patterns have been found in a single racial group (for the age-specific prevalence situations described above. instance, in China-Cort and Stoll 1931). It is more Thus, whether or not prevalence falls with age, likely, therefore, that the two patterns of age-specific intensity does, and this suggests an immune response prevalence derive from differences in exposure due to that does not prevent infection but limits the intensity differences in behavior, housing, agricultural practice, of infection by reducing the proportion of ingested eggs sanitation, and other environmental and cultural that develop into mature adults. Women may have factors. Cort and Stoll (1931) suggested that the heavy higher egg outputs, indicating heavier infections, than and common infection of adult males with Ascaris in men, which may be explained by the greater exposure some parts of China was due to the intensive use of of women discussed above. human feces in agriculture. A fundamental influence on the epidemiology of Several surveys, for instance in Virginia (USA; Cort, ascariasis is that a small minority of infected people are Otto and Spindler 1930) and Panama (Cort and others excreting the majority of the eggs. In China it was 1929), have revealed a somewhat higher prevalence of found that 5 percent of those infected excreted half of infection in women than in men. This difference is not all eggs (Cort and Stoll 1931). Heavy infections tend to seen in children. If the main source of infection is eggs be single-brood infections. In other words, they are not deposited by infected children around the house, an accumulation of worms from eggs ingested women may be more exposed because they spend more regularly over several months; rather, they are worms time than men working in the yard and tending to of a single age arising from the ingestion of a batch of children. If vegetables fertilized by night soil are a eggs at one time. This may be due to an immune major source of infection, women may also have mechanism triggered by adult worms in the intestine greater exposure if they are responsible for their and acting against the migrating larvae resulting from harvesting, cleaning, and preparation. subsequent egg ingestions. More research is required in Ascariasis is common in some developed countries. this area. There are an estimated 4 million people infected in the Not much is known about the seasonality of USA, with the disease being especially common in the ascariasis. During a pronounced dry season trans- southeast (Warren 1974). As in other countries, mission may decrease because the Ascaris eggs are infection rates are highest among children, and there desiccated in the dry soil. Therefore, there may be few ASCARIS AND ASCARIASIS 379 new infections, and these will tend to be light. Since The pattern of yard contamination and infection natural death is occurring among adult worms, may be modified by coprophagous domestic animals. intensity of infection, and possibly prevalence, will fall Chickens, cats, and dogs in Tennessee (USA) were all during the dry season. Transmission may increase with found able to ingest A. lumbricoides eggs and to pass a the rains and may cause an increased intensity, and proportion of them unharmed in their feces (Otto, Cort possibly prevalence, about 2 months later. These and Keller 1931). Pigs are enthusiastic consumers of climatic factors may be reinforced or negated by other human feces and may be especially important in seasonal changes, such as agricultural and dietary distributing human Ascaris eggs. Jones (1976a) practices, that may influence exposure and resistance suggested that pigs in Papua New Guinea may play a to infection. A November-December peak in trans- role in transporting Ascaris eggs into villages, or even mission in Korea was attributed to contaminated into homes, from human defecation sites that are often pickled vegetables (Seo, Cho and Chai 1979). in thick undergrowth away from dwellings. The climatic influence on transmission described Transmission may take place not only in the fecally above might cause a pronounced seasonal pattern in contaminated yard, but also in the home if the floor is intensity of infection (mean egg output) but little made of a material that will permit the maturation of change in prevalence. Studies in Colombia (Faust and Ascaris eggs. Brown (t927) found that eggs deposited Mugaburu 1965), Panama (Cort and others 1929), and by small children onto hut floors in Panama developed Taiwan (Chen and Hsieh 1969) have confirmed this to maturity in 14 days. Viable eggs have also been seasonal picture. Seasonality in transmission may also isolated from house floors in China (Winfield 1937) lead to a seasonal peak in pneumonitis associated with and Egypt (Chandler 1954). Studies in the USSR found Ascaris larvae migration, as has been reported from that Ascaris eggs could develop on household objects Saudi Arabia (Gelpi and Mustafa 1967). and in floor cracks if humidities were high, and could There are three primary contexts for Ascaris remain viable for over 3 months in cool, humid transmission: environments such as cellars (Barchenko 1955). The other two contexts for transmission mentioned * Transmission in yards and compounds that have .. been contaminated by feces, especially those of above, transmission in the fields and via contaminated children vegetables, are prominent either where feces are much * Transmission to persons working in fields where used in agriculture or where hygiene is improved to the night soil or sewage is used as fertilizer point at which yard transmission becomes relatively unimportant. The role of field infection has been much that have been grown in fields enriched with night stressed in the Chinese literature, whereas both fields soil or sewage. and contaminated vegetables are emphasized by workers in Japan, Korea, Taiwan and neighboring Yard transmission is probably the dominant mode areas. The importance of vegetable contamination as a in areas of poverty and inadequate sanitation. Families single factor has been stressed by writers from with heavily polluted yards tend to have high countries in which a well-educated and moderately prevalences and intensities of ascariasis, and ascariasis wealthy population lives near to, and buys vegetables is typically clustered by household. Familial aggre- from. a poor community with endemic ascariasis; gation of ascariasis has been reported from China prominent examples in the literature are Israel, South (Winfield 1937), Tennessee (USA, Otto, Cort and Africa, and parts of the USSR. Keller 1931), Virginia (USA; Cort, Otto and Spindler The very high prevalences of ascariasis around 1930; Hendley, Williams and Burke 1973), and Darmstadt (Federal Republic of Germany) in the late Panama (Brown 1927; Cort and others 1929). The 1940s were due to the widespread practice of applying studies in Tennessee and Virginia also suggested that untreated sewage and sludge to fields and vegetable children from households with good sanitation could gardens (Baumhogger 1949). The prevalence of become infected when they visited heavily infected ascariasis among the Jewish population of Jerusalem families and that rural schools with inadequate decreased from 35 percent in the period 1934-47, to 1 sanitation and heavy soil pollution acted as dissemi- percent in the period 1947-60. The decrease was nation points for ascariasis in the community. Ascaris attributed to the cessation of supplies of sewage- eggs were recovered in Egypt from the playgrounds of irrigated vegetables from Jordan after the partition of schools with no latrines, or with poorly maintained the city in 1948. In contrast, the prevalence of ascariasis latrines, but not from schools with well-maintained in the Jordanian section of Jerusalem remained high, at latrines (Chandler 1954). 78 percent, in the early 1950s (Ben-Ari 1962). Khalil 380 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS (1933) documented a 96 percent prevalence of Control Measures ascariasis among 5-16 year old children in the oasis of Siwa (Egypt) and attributed this to use of human Only environmental and behavioral changes can wastes in agriculture. have a sustained impact on ascariasis, but mass Workers in formal sewage farms or sewage effluent chemotherapy may be used to reduce infection rates in irrigation schemes are also exposed to increased risk of the short term. Ascaris infection (Clark and others 1976). A study in Germany during 1954-56 showed ascariasis prevalences Indd of 3 percent among sewermen, 16 percent among sewage treatment plant workers, 30 percent among sewage No vaccines or prophylactic drugs are available. irrigation workers, and 8 percent among a control group Individual protection can be obtained by scrupulous (Sinnecker 1958). personal hygiene and care in choice and preparation of This section is concluded by citing the account by food, especially vegetables. Winfield (1937) of ascariasis in northern China in the The most immediately effective method yet applied 1930s. Each house had a combined animal shed and pit in areas with high prevalence is mass chemotherapy. tatrine. This comprised a pit, 3-5 meters square and The administration of appropriate drugs (such as about 2 meters deep, lined with brick or stone and with levamisole, mebendazole, or pyrantel pamoate) to all a base of tamped lime and clay, so that the whole pit individuals, or to all children, at regular intervals has was fairly watertight. The family defecated into the pit dramatically reduced prevalences in several local trials. and also placed animal manure, organic refuse, and Mass treatment should start at the period in the year slops in the pit. Field earth was added at the rate of when worm burdens are highest and should ideally be about one basketful per day. During dry weather, repeated at intervals of not more than 60 days for as water was added to keep the pit contents wet; in the long asinfective eggsremain in the soil. In most regions rainy season, the pit contained standing water and was it would be impossible to prevent the reintroduction of the site of mosquito breeding. Adjacent to the pit was a infection following a mass treatment program, and shed where pigs and other animals were housed. Steps therefore it is unlikely that mass treatment will be led down into the pit to allow the pigs to enter to eat effective in the long term without concurrent fresh feces and to wallow in the muck. Usually the pit improvements in excreta disposal and hygiene. In the was emptied every spring and the waste was piled along absence of these preventive measures, prevalence may the streets or on the village threshing floor. After a few return to pretreatment levels within 6-12 months, days the waste was carted to the fields and placed although intensities (as measured by mean egg output) carefully about the roots of the winter wheat or worked take somewhat longer to build up again. Literature on into the ground in preparation for the spring crop. mass chemotherapy and reinfection in various Some families emptied their pits more than once a year. countries is listed in table 23-1. in which case the waste would be piled along the streets with a layer of straw-reinforced mud as a protective Environnental cover. It would then be used at the time of the next spring sowing. Transmission of ascariasis generally occurs follow- Ascaris infection was very common, especially in ing the contamination with feces of the house floors, those families having contaminated yards. Ascaris eggs the yard, or the area around the house. Eggs develop to were readily found in samples of soil from yards, floors the infective stage and reinfect a child or adult who and streets. Winfield concluded that fecal contami- accidentally ingests a particle of contaminated soil or nation of the yards and floors was the dominant cause dirt. In areas of high prevalence, there is good evidence of transmission and that contaminated water and that most infection takes place in, or close to, the house vegetables were unimportant (see also Winfield and and is clustered by family. Eggs are deposited primarily Yao 1937). Yard and floor contamination were caused by small children who may defecate promiscuously in by the casual defecation of children, who tended not to or near the home. Eggs may also be deposited by pigs, use the latrines because of inconvenience and fear of the dogs, or chickens that have fed on human feces and can pigs. Ascaris eggs were also distributed in the yards by pass the human Ascaris eggs unharmed in their own chickens and dogs that fed on human excreta, both in feces. the latrine and elsewhere. Contamination of the yard This kind of family-centred transmission can be also occurred during the periodic emptying of muck controlled, in theory, by providing a hygienic toiletfor from the pit for transport to the fields. all members ofthefamily and by providing the necessary ASCARIS AND ASCARIASIS 381 Table 23-1. Some studies on the reduction and subsequient rise of ascariasis prevalencefollowing mass chemothlerapy Country Drug Source Colombia Pyrantel pamoate Spillmann (1975) India Tetramisole Gupta and others (1977) Iran Piperazine Arfaa and others (1977) Levamisole Arfaa and Ghadirian (1978) Levamisole Massoud (1980) Mexico Piperazine Biagi and Rodriguez (1960) Panama Tetrachlorethylene and chenopodium Cort, Schapiro and Stoll (1929) Philippines Pyrantel pamoate Cabrera, Arambulo and Portillo (1975) Piperazine Garcia and others (1961) Levamisole Jucco and Cabrera (1971) Reunion Thiabendazole Coumbaras and others (1976) (Indian Ocean) L-tetramisole Taiwan Piperazine Chen and Hsieh (1969) Thailand Pyrantel pamoate Bhaibulaya and others (1977) USA Piperazine Atchley, Wysham and Hemphill (1956) Zaire Levamisole Jancloes, Cornet and Thienpont (1979) health education to ensure that the toilet is used. will tend to decrease community enthusiasm for the Because children are the main excreters of Ascaris eggs, preventive measures being advocated. It is for this it is essential that any toilets should be acceptable and reason that a combination of mass chemotherapy and appropriate for use by children. In addition, it is sanitation is the best approach to ascariasis control. necessary to clear up the stools of babies who are too In a combined program of mass chemotherapy, young to use a toilet. Fresh stools are not immediately sanitation, and education the role of sanitation and infective for Ascaris, and so they may be cleaned up any education is to maintain the low intensities and time up to a few days after deposition and still interrupt prevalences created by the mass chemotherapy. This Ascaris transmission except that delay in clearing up should be perfectly possible, and in recent years several will increase the risk of dispersion or ingestion of eggs East Asian countries have achieved notable success in by domestic animals. ascariasis reduction by this approach. South Korea has Improvements in excreta disposal facilities, de- had mass campaigns for the prevention of ascariasis fecation behavior, and child care can greatly reduce including health education, stool examination and transmission. Bearing in mind that adult worms die mass chemotherapy. Latrines have been widely naturally after 6-18 months in the small intestine, provided. In 1949, the national prevalence of ascariasis reduced transmission will cause a gradual fall in was 81 percent, but by 1971 it was 46 percent (Soh intensity of infection followed by a gradual fall in 1973). These measures were also effective against prevalence. Because the domestic environment may be trichuriasis (from 87 to 47 percent) and hookworm heavily contaminated with Ascaris eggs that may (from 39 to 7 percent). remain infective for many months, transmission will There is no doubt that behavior is all important in continue for some time after sanitation has been the success of an excreta disposal program. Poorly improved, and there may be a considerable lag before used and maintained latrines will achieve little and may reduced intensities and prevalences are measurable. even increase transmission. Children may continue to There will be an even greater lag before reduced defecate around the home and transmit eggs to their infection reaches a level at which it is apparent to siblings. Even if excreta disposal is improved around mothers. This delayed response to reduced trans- the home, it may be unaffected in the fields, work mission is undesirable from a clinical viewpoint and places, or schools, where transmission may continue 382 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS unchecked. Following studies in southwestern Virginia ascariasis prevalence in some communities in Costa (USA) in 1928, Cort, Otto and Spindler (1930) Rica, Egypt, Germany, Iran, Singapore, South Korea, wrote: and the USA, but it appeared to have little or no influence in Egypt, Panama, and the USA. Treatment Several groups of negroes, one of which was of night soil, by heat or chemical ovicides, was effective extremely poor, as well as numbers of poor white ontroling ascariasis in some communities in Japan families showed little or no Ascaris infestation because and the USSR. Cases in which sanitation appeared ineffective are of the control of the chfldren and the use of the privies ms rbbydet nufcetueo,o opo by all members of the families. On the other hand some most probably due to insufficient use of or to poor of the better-off rural families with well-kept yards and hygiene in, the latrines or to transmission continuing good privies and certain families in very well-sanitated away from the home at the place of work or recreation. mining camps had heavy infestations. Suchinfestatio Unfortunately, most studies do not clearly demon- strate this because they are deficient in behavioral were almost always due to soll pollutlon near they observations. Constructing latrines and measuring houses by the young children, who were not taught to health changes does not provide the data necessary to use the sanitary facilities provided, explain any impact, or lack of impact, observed. Detailed observations of actual use of latrines, Similarly, following work in China, Cort and Stoll especially usc by children, are required but are very (1931) wrote: seldom carried out. Also rare are studies on traditional beliefs and practices concerning ascariasis such as It was of interest to find one group in the Yangtze that conducted in rural west Malaysia by Chen delta with a comparatively low infestation with both education campaigns to accompany sanitation and parasites [Ascaris and Trichuris] associated with a good economic status and habits of cleanliness much mass chemotherapy programs. better than the average for rural China. This shows that In conclusion, it is sobering to consider two human infection with these parasites can be much statements made half a century ago, which remain true hut sadly ignored today. Otto and Spindler (1930)) restricted even where their eggs are spread widely by wrote: the use of human feces as fertilizer. The application of untreated nightsoil or sludge to The building of privies is a fundamental step in the the land undoubtedly contributes to Ascaris trans- control of infectious diseases spread by soil pollution, mission. People working in the fields may be infected, but to be successful they must be used exclusively. In and eggs may be brought into the home on soiled the regions just discussed [Virginia] the situation is vegetables. Undeveloped eggs brought into the home difficult because many of the people are doubtful of the can subsequently become infective if they end up on an value of a privy. In many cases they feel that it produces earth floor or in a moist cranny. This route of infection an unwise accumulation of odorous and obnoxious is likely to be of minor importance where prevalence waste which if daily dropped in various parts of the and intensity are high and where transmission is yard would be destroyed by insects or chickens and occurring primarily around the house. However, in washed into the soil by the rains. Those adults who do areas where domestic hygiene is relatively good and consent to build and use the privy often do not feel toilets are used, contaminated crops may be the major sufficiently convinced of its beneficial results to take route by which eggs are introduced into the household. any time to teach the young children to use it. Control of this agricultural transmission route is by Furthermore, as has already been pointed out, the pit adequate treatment of sludge and night soil prior to privy as usually built is structurally ill adapted to land application. children's use and frequently inconveniently situated. Studies on the environmental control of ascariasis The seat is too high and the hole too large to be are listed in table 23-2, more details of some ot them conveniently and safely used by young children. A are given in table 2-1. In most studies confounding lower seat or a step to part of the main seat with a variables were not adequately controlled, and it is not smaller hole for the convenience of young children possible to separate the effect of sanitation, for should certainly be encouraged. The real problem, instance, from that of socioeconomic and educational however, is the slow process of educating these people changes. Sanitation appeared to have an influence on to consider the sanitary privy as one of the most ASCARIS AND ASCARIASIS 383 Table 23-2. Some studies on environmental influences on ascariasis Country Result Source Costa Rica Ascariasis prevalence was lower among those with Moore, de la Cruz and Vargas-Mendez (1965) improved sanitation Egypt A village receiving improved water supplies, Chandler (1954) latrines, and refuse collection had a lower prevalence (50 percent) and intensity (4,200 eggs per gram) of ascariasis than a village with unimproved sanitation (prevalence = 76 per cent; intensity = 6,900 eggs per gram) Ascaris rates remained,high among prisoners, Khalil (1926, 1931) despite falling rates of hookworm and schistosomiasis, owing to regular reinfection by contaminated vegetables grown on the prison sewage farm Improved sanitation, with and without Scott and Barlow (1938) chemotherapy, did not reduce ascariasis in several villages Germany Prevalences of ascariasis in schoolchildren in Anders (1954) Berlin were 3 percent in sewered areas, 7 percent in unsewered rural areas, and 14 percent in unsewered urban areas Iran Water and sanitation improvements had little Arfaa and others (1977) impact on prevalence but considerable impact on intensity of ascariasis; water and sanitation improvements plus regular mass chemotherapy added nothing to the impact of mass chemotherapy alone Prevalence of ascariasis was the same among Sadighian and others (1976) people with and without sewerage in Isfahan Water supply, sanitation, and bathing Sahba and Arfaa (1967) improvements were associated with a fall in prevalence (67 to 57 percent) and intensity (11,000 to 4,000 eggs per gram) in a single village Japan Heat treatment of night soil prior to agricultural Katayama (1955) application was associated with a declining prevalence of ascariasis Heat treatment of night soil had little effect on Kawagoe and others (1958) ascariasis but was effective in maintaining a lowered prevalence achieved by mass chemotherapy Night soil treatment with sodium nitrite and Kozai (1960a, 1960b, 1960c, 1962) calcium superphosphate reduced but did not prevent rising prevalence of ascariasis following mass chemotherapy Night soil treatment with thiabendazole reduced Kutsumi (1969) ascariasis prevalence by 30 percent over 2 years and night soil treatment plus mass chemotherapy reduced it by 50 percent Panama Sanitation did not delay reinfection following mass Cort, Schapiro and Stoll (1929) chemotherapy Singapore Poor families rehoused in modern flats had an Kleevens (1966) ascariasis prevalence of 9 percent compared with that of squatters (63 percent) 384 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Table 23-2. (continued) Cowatn tr Result Source South Korea Higher intensities of ascariasis occurred in poorer Soh and others (1973) parts of Seoul using vault latrines than in wealthier areas with sewerage USA Kentuck\ Ascariasis prevalence was associated with both Schliessmann and others (1958) water supply and sanitation facilities Tennessee Ascariasis prevalence was associated with Eyles, Jones and Smith (1953) sanitation, fecal contamination. domestic and personal cleanliness, family size, but not water quality Pit latrines were not effective in reducing ascariasis Otto, Cort and Keller (1931) because they were commonly not used by children, who defecated in the yard Virginia Pit latrines were not effective in reducing ascariasis Otto and Spindler (1930) because they were commonly not used by children, who defecated in the yard USSR Cessation of use of untreated night soil as a Rosenberg (1960) fertilizer was associated with a marked decrease in Ascaris egg contamination of soil and fruit necessary buildings on the premises of every family and environmental conditions for periods of months or its use taken as a matter of course. When this is even years. They need small quantities of oxygen to accomplished, and not until then, will human excreta develop but can remain viable for long periods in be so disposed as to protect not only against Ascaris anaerobic conditions. infestation but against bacterial diseases as well. Cort (1931) wrote: In surface water In many places Ascaris infestation has been reduced The occurrence and survival of Ascaris eggs in waters is not a very important subject because little or or eliminated by sanitary programs carried out over.. long periods of time, especially where other factors no transmission is waterborne. have raised the social and economic level of the Usacheva (1951) found Ascaris eggs in a high population. It has been shown, however, that very proportion of river water and river sediment samples in frequently sanitary work has not been successful in the USSR. All samples contained Ascaris eggs at times controlling this parasite because ofthe failure of young of flooding. Survival experiments revealed that 12 children to use the facilities provided. For Ascaris percent of eggs in river water, and 17 percent of eggs in control, therefore, it is necessary to provide facilities sediment, were viable after 15 months (presumably the well adapted for children's use and to concentrate the temperatures were cool). Goryachev (1947) also isolated Ascaris eggs from river water and sediment educatlonal program on the preventton of soil g pollution by young children. Since the presence of this near Omsk and found more ae wanter than In spring parasite in both cities and rural communities over such . ' Xg_ wide areas of the world can be used as an index of the per 100 grams of soil at six public beaches on the shores status of sanitation it seems that campaigns for its of the River Vistula in Poland. The largest number of control miaht form a larger part than at present of eggs and the most advanced in development were r, . . ......................... found in the damper zones, such as the water's edge, in programs for the improvement of sanitary conditions. the shade of bushes, and near public toilets. The beaches were not close to sewage outfalls and it is Occurrence and Survival in the probable that most eggs came from defecation by Environment beach visitors, rather than from the river water. Ascaris eggs are especially likely to occur directly Ascaris eggs may be the most hardy and resistant of downstream from sewage outfalls. Near Denver all excreted pathogens. They can survive a variety of (Colorado, USA) a river contained 0-1 eggs per liter ASCARIS AND ASCARIASIS 385 above a sewage outfall, and 0-14 per liter below it. volume of 2 liters per capita daily, then the night soil Ascaris eggs were also recovered 3 kilometers will contain 3 x 107 eggs per liter. Concentrations this downstream from the outfall (Wang and Dunlop high have not been reported. Night soil in Kiangsu 1954). Province (China) contained 2.3 x 106 Ascaris eggs per liter (McGarry and Stainforth 1978). In groundwater Takenouchi and others (1980) studied Ascaris eggs in night soil in Kochi Prefecture in Japan. Ascaris egg Ascaris eggs are unlikely to occur in groundwater concentrations were higher in night soil from mountain because their size causes them to be retained as areas than from coastal regions, and it is suggested that polluted surface waters percolate down through the regular enumeration of Ascaris eggs in night soil is porous strata. They may, however, occur where surface a useful method of monitoring ascariasis in the waters are flowing directly into groundwaters via community. fissures in metamorphic rocks or solution channels in Survival of Ascaris eggs for over 1 year is possible in limestone. feces and night soil. In anaerobic conditions develop- ment is arrested but recommences when air is In drinking water introduced. Urine is ovicidal and will kill eggs in 16 hours. Eggs fail to develop in dilutions of urine down to No reports of Ascaris eggs in drinking water have 10 percent (Hamdy 1970a). been found. As mentioned above, their presence is of little interest because waterborne transmission is unimportant relative to yard and field transmission. In sewage Chlorine and chloramine are completely ineffective Raw sewage has been reported to contain up to 38 against Ascaris eggs at, or even greatly above, the Ascaris eggs per liter in eleven towns in the German concentrations typically applied during water treat- Democratic Republic (Kalbe 1956); 10-80 per liter in ment. Tokyo, Japan (Liebmann 1965); 38 per liter in San Ascaris eggs were found in the raw river water Juan, Puerto Rico (Rowan and Gram 1959); 5 to 110 supplying Ufa (USSR) but not in the tap water (Bukh per liter in Denver, USA (Wang and Dunlop 1954); 1945). and 19 per liter of settled sewage in Daspoort, South Africa (Nupen and de Villiers 1975). Wang and Dunlop In seawater (1954) reported that 87 percent of the eggs in raw sewage were viable. Yarulin (1955) found Ascaris eggs in the coastal Sewage from some communities in developing waters of the Caspian Sea near sewage outfalls. Eggs countries may be expected to contain much higher remained viable for considerable periods in seawater concentrations of Ascaris eggs than these. In Calcutta but did not develop until removed. Laboratory (India) 20,000 to 213,000 Ascaris eggs per capita per experiments in South Africa found that 97 percent of day were reaching the sewage works; assuming 100 Ascaris eggs were killed after 2 days in seawater. They liters of sewage per capita per day, this implies were considerably more resistant than Trichuris, concentrations of 200-2,130 Ascaris eggs per liter hookworm, or Enterobius eggs, but somewhat less (Bhaskaran and others 1956). Raw sewage in Aleppo resistant than Taenia eggs (Livingstone 1978). The (Syria) contained 1,000 to 8,000 Ascaris eggs per liter specific gravity of Ascaris eggs is about 1.11, and so due to an estimated 42 percent of the population they will settle in seawater and in seawater and sewage excreting, on average, 800,000 eggs daily per person mixtures with specific gravities of 1.00 to 1.03. (Bradley and Hadidy 1981). Infeces and night soil In sludge The high prevalence of Ascaris egg excretion in some The effect of many sewage treatment plants is to communities has been described above in the section concentrate Ascaris eggs in the sludge. In South Africa on epidemiology. Some individuals excrete large raw sludges contained 0-250 Ascaris eggs per gram numbers of eggs, up to 300,000 per gram of feces, and (Keller and Hide 1951] Krige 1964). In the thus night soil may be rich in Ascaris eggs. If the Johannesburg area, 74 percent of eggs in raw sludge prevalence is 60 percent, the mean egg output of those were viable (Keller and Hide 1951). In Kharkov infected 10,000 eggs per gram, and the mean night soil (USSR) raw sludge from the trickling filter plant 386 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS contained 20-48 Ascaris eggs per gram (Vishnevskaya for up to 1 year at 0.1-0.2 meters and up to 1.5 years at 1938). Near Moscow (USSR) the sludge from trickling 0.4-0.6 meters (Drozdova and others 1973). In the filter plants contained up to 466 helminth eggs per Federal Republic of Germany Ascaris eggs in sewage gram (Vassilkova 1936). irrigated fields survived for up to 1.5 years (Gartner Ascaris eggs were recovered from 6 to 95 percent of and Muting 1951 b). In contrast, Ascaris eggs deposited sludge samples collected from several sites in the USA on sewage irrigated pasture in South Africa were and were the most frequently identified parasitic inactivated in a few days owing to rapid dessication helminth (Theis, Bolton and Storm 1978). Sludge from (Keller and Hide 1951). The run-off water from the Los Angeles (California) contained up to 100 Ascaris pasture contained no eggs. The work of Lysek and his eggs per gram, but most sludges contained less than 50 colleagues has suggested that fungi are instrumental in per gram. An earlier study (Wright, Cram and Nolan killing Ascaris eggs in soil, especially in the tropics 1942) found Ascaris eggs in 36 percent of sludge (Lysek 1964; Lysek and Bacovsky 1979). samples from seventeen army camps in the southern Surface soil contamination with Ascaris eggs can be USA. Ascaris was the most frequently identified reduced by the use of subsurface irrigation methods. parasitic helminth. Romanenko (1969) studied subsurface irrigation Sludge in developing countries may contain a much with raw sewage via earthenware pipes laid at a depth of higher concentration of Ascaris eggs. Trickling filter 0.6 meters, over a 9-year period. No Ascaris eggs were plant sludge in Isfahan (Iran) contained 18,100 eggs found in the surface layers of soil. per gram (Sadighian and others 1976), and septic tank Night soil cartage systems may contaminate the soil sludge in China contained 2,300 Ascaris eggs per gram of city streets and lanes with Ascaris eggs. Nineteen (McGarry and Stainforth 1978). percent of soil samples collected from the streets of Isfahan (Iran) contained Ascaris eggs (Hoghooghi and In soil others 1973). The soil contamination rate and the proportion of viable eggs were highest in winter and Ascaris eggs are found in soil in fields where night lowest in summer. Both of these parameters were soil or sewage are applied for fertilization or irrigation directly related to the rainfall and inversely related to and in places used as defecation sites by infected the air temperature. people. Ascaris eggs will survive for several years in soil. The maximum recorded survival time is 7 years (Kirpichnikov 1963). Survival is promoted by cool, On crops moist, and shaded soil and by being under the surface As mentioned previously, the contamination of rather than on top. Exposure to sunlight and vegetables by Ascaris eggs may be an important desiccation will reduce survival time very considerably. transmission route in some communities where family- Gartner and Muting (1951a) studied land irrigated centered transmission is relatively unimportant, owing by sewage effluent in the Federal Republic of Germany. to improved sanitation and hygiene, but where night Samples were taken from land that had been irrigated soil or sewage are applied to vegetable gardens. The 11 months earlier and from land irrigated only 4 to 6 subject was reviewed 30 years ago by Rudolfs, Falk and days previously. There were many more Ascaris eggs Ragotzkie (1950, 1951a-c). present in the latter than in the former: in both cases The contamination of vegetables by Ascaris eggs, the concentration diminished with increased depth. In following the use of sewage, night soil, or sludge for no case did Ascaris eggs penetrate into the sand 0.3 fertilization, has been a major concern of para- meters beneath the cultivated soil. No Ascaris eggs sitologists in the USSR for many years (Khaustov were found on vegetables grown in sewage-irrigated 1935). Vassilkova (1941) reported that cucumbers, fields. Rosenberg (1960) found that soil around a tomatoes, and carrots, grown outside Moscow and village in the USSR contained Ascaris eggs in 100 irrigated with sewage, were contaminated by Ascaris percent of samples;41 percent of these eggs were viable. eggs and that 36 percent of these were viable. On the After cessation of fertilization with night soil, the basis of these findings she suggested that sewage proportion of positive soil samples fell to 35 percent, irrigation should be discontinued before harvesting and no eggs were viable. and that vegetables should be gathered directly into The survival times of Ascaris eggs in clean silty soil in baskets and not laid on the ground. In a later study the USSR were 23-29 days on the surface, up to 1.5 (Vassilkova 1950), she found that tomatoes and years at 0.1-0.2 meters' depth and over 2.5 years at cucumbers irrigated with raw sewage contained about 0.4-0.6 meters. In soil with sewage sludge, survival was 20 eggs per 100 vegetables, whereas those irrigated with ASCARIS AND ASCARIASIS 387 settled sewage contained about 3 per 100 vegetables. and lettuce under hot and dry conditions and found In Lithuania, 98 percent of vegetables from gardens that they did not survive for more than 1 month. using raw sewage contained helminth eggs, compared Several studies have been conducted into methods of with 9-16 percent of vegetables from other gardens and cleaning suspect vegetables prior to eating. In 7-11 percent of cleaned vegetables on sale in markets. Czechoslovakia, Lysek (1959) found that thorough Of all helminth eggs isolated from vegetables, 94 rinsing removed Ascaris eggs but that wiping did not. percent were Ascaris, 5 percent Trichuris, and 1 percent In South Korea, Choi (1970) found that keeping Enterobius (Biziulevicius 1954). vegetable leaves in water for 10 minutes, and then Rosenberg (1960) found that the proportion of fruit shaking them 20 times, removed only 40 percent of that was contaminated by Ascaris eggs in a village Ascaris eggs. Thitasut (1961) concluded that soaking dropped from 71 percent to 25 percent following the vegetables in a solution of 100 milligrams per liter of cessation of use of untreated night soil in agriculture. iodine for 10 minutes would kill Ascaris eggs without No helminth eggs were detectable in samples of damaging the vegetables. Zaman and Visuvalingam cucumbers, beetroot, potatoes, onions, and grass (1967) recommended 250 milligrams per liter of iodine grown in fields irrigated by subsurface irrigation, for 10 minutes. Soh (1960) experimented with a wide whereas similar vegetables grown in fields irrigated by range of pickling and food preservative substances sewage flooding were heavily contaminated with viable (salt, sugar, vinegar, alcohol, bean sauce, garlic, Ascaris, Trichuris, and Enterobius eggs (Romanenko mustard, onion, pepper, clove, allspice, cinnamon, and 1971). ginger) and found that none of them was strongly There is less literature on this topic from countries ovicidal. Rudolfs, Falk and Ragotzkie (1951b) other than the USSR, but substantial vegetable concluded that immersing vegetables in warm water contamination may be expected where night soil or (60°C) for 10 minutes was the most reliable method of sewage is being used. In the USA, 6 percent of sewage- destroying Ascaris eggs. irrigated vegetable samples were contaminated with The effect of vegetable decontamination on as- Ascaris eggs despite furrow irrigation, dry climate, cariasis was studied at a boys' school in Japan sandy soil, and the fact that the sewage had undergone (Tomomatsu and Takeuchi 1961). Ascaris prevalence primary sedimentation and chlorination (Dunlop and was originally 37 percent and fell to 5 percent following Wang 1961). administration of a vermifuge. From that time, In China and neighboring countries, where night soil vegetable washing began using potassium iodide. After is widely used for vegetable gardening, extensive 5 months the prevalence had risen to 12 percent, and Ascaris contamination of vegetables may be expected. after 8 months to 16 percent. The authors claim that the Vegetable leaves in South Korea contained 38 eggs per rate of reinfection would have been greater if it had not 100 grams, and carrots had 0.6 eggs per 100 grams been for the vegetable washing program, but there was (Choi 1970). Early studies in northern China (Winfield no control group and they were unable to substantiate and Yao 1937) suggested that vegetables were their claim. unimportant in Ascaris transmission. During 1933-34, 275 kilograms of vegetables from Tsinan market were Inactivation by Sewage Treatment examined. No eggs were found. Other vegetables were Processen examined with the same result. Soil samples were rocesses collected from vegetable gardens, of which 57 percent Ascaris egg removal in sewage treatment processes is were positive for Ascaris eggs. These data were held to priarly a remon m the treentocehich substantiate the finding of Winfield (1937) that. primarily a function of the degree to which although night soil compost was used to fertilize vegetables, contaminated vegetables were not an k important transmission route. Most transmission occurred in and around the home. In an experimental septic tank in India with 3 days In a humid environment and a shady site, Ascaris retention time, 99.4 percent of Ascaris eggs settled. eggs can develop to the infective stage and survive for However, in operational septic tanks removal was far considerable periods on vegetables (Barchenko 1953). lower than this (Bhaskaran and others 1956). In an arid climate, and if exposed to sunlight, a An unpublished report from the United Nations combination of desiccation and ultraviolet irradiation Environment Program (UNEP 1976) described the causes more rapid death. Rudolfs, Falk and Ragotzkie effect on Ascaris eggs of the Chinese three- (1951a) sprayed A. suum eggs onto growing tomatoes compartment septic tank. The retention time of each 388 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS chamber was 15-20 days, assuming a daily inflow of 2.4 chlorinated settled sewage 0-20. The relative per- liters per capita. Each unit served a group of houses, sistence of Ascaris eggs versus coliform bacteria is and the contents of bucket latrines were emptied into it. illustrated by the egg to coliform ratios, which were Studies on Ascaris eggs indicated that 80-96 percent 1:14.000,000 in raw sewage, 1:10,000,000 in settled were retained in the first two chambers. Eggs sewage, and 1: 7,000 in chlorinated effluent (Wang and accumulated primarily in the sludge in the first Dunlop 1954). No loss of viability occurred in the chamber (at about 3,000 eggs per gram), where 67-95 treatment plant, and the proportion of viable eggs was percent of them died if stored for 2 months. A different 87 percent in the influent and 88 percent in the effluent. account of the Chinese three-compartment septic tank Three types of sewage treatment works in Puerto is given in McGarry and Stainforth (1978). The Rico were investigated by Rowan (1964). Primary retention times in the three compartments were 10, 10, sedimentation plants removed 35-74 percent of and 30 days, respectively. The contents of the first Ascaris eggs, trickling filter plants removed 95-99 compartment were semisolid. specific gravity fell percent, and activated sludge plants 97-100 percent of and egg sedimentation improved as the liquor eggs from the effluent. Typically, small numbers of passed through the second and third compartments. Ascarifs eggs (up to I per liter) could be recovered from The effluent was free of Ascaris eggs. The sludge in the the effluent of secondary settling tanks following either third compartment contained 2,300 eggs per gram, and trickling filter or activated sludge treatment. It was all of these were judged on morphological grounds to expected that large numbers of eggs would have be dead. been found in the sludges from these treatment plants but this was not investigated. The survival of helminth eggs was studied in five sewage works in and around Calcutta (India) over a 4- The effect of conventional sewage treatment plants is year period (Bhaskaran and others 1956). The average to concentrate Ascaris eggs in the sludge. A few may be number of Ascaris eggs per capita per day reaching the found in the effluent, but sometimes they are absent sewage works ranged from 20,000 to 213,000. Far (for intance. see Forstner 1960). Typical Ascaris egg greater numbers of Ascaris eggs than hookworm or reduction rates are 35-90 percent by primary Trichuris eggs were found. Primary sedimentation for sedimentation alone, 90-99 percent by a complete about 2 hours caused the settlement, on average, of trickling filter plant, and 90-100 percent by a complete around 70 percent of Ascaris eggs. Ascaris eggs settled activated sludge plant (see Cram 1943; Feachem and more rapidly than those of hookworm or Trichturis. others 1980; Kabler 1959; and the studies mentioned Removal of Ascaris eggs from the effluent of activated below). sludge plants was over 90 percent and was higher when At the Kharkov (USSR) trickling filter plant, raw the plant was well maintained and well operated. sewage contained on average 60 Ascaris eggs per liter. Panicker and Krishnamoorthi (1978) summarized after primary sedimentation 20, after trickling filter 13. Ascaris egg removal by various treatment plants in and after secondary sedimentation 2 per liter India. Reductions were 96 percent after 2 hours (Vishnevskaya 1938). At two other treatment plants in primary sedimentation, 47 percent after 1.5 hours the USSR, raw sewage contained the eggs of Ascaris, sedimentation, 98 percent by a complete activated Trichuris. Enterobius, Diphvllobothriumn, and Taenia at sludge plant. 95 and 96 percent by two complete a concentration of up to 2,000 eggs per liter. Egg trickling filter plants, 79 percent by a pilot scale biodisc concentrations were reduced by 97 percent in Imhoff plant, 92 percent by a pilot-scale aerated lagoon tanks, by 18-26 percent in trickling filters, and by 87 without secondary sedimentation, and 94 percent by a percent in secondary sedimentation tanks. pilot-scale oxidation ditch with secondary sedimen- Chlorination of the effluent had no effect. Predictably, tation (see table 22-4). sludge contained many helminth eggs: up to 466 per gram (Vassilkova 1936). At the trickling filter plant in Daspoort (South Africa), the concentrations of Ascaris eggs per liter A well-designed series of waste stabilization ponds, were 19 in the settled sewage, 1 in the trickling filter with 3 or more cells and an overall retention time of at effluent, and I in the final effluent from the secondary least 20 days, removes all Ascaris eggs from the effluent. sedimentation tank (Nupen and de Villiers 1975). In Eggs settle to the sludge layer where they die after a few Denver (Colorado. USA) raw sewage contained 5-110 months. Ascaris eggs per liter, settled sewage 2-30, and In India, 100 percent removal of Ascaris eggs was ASCARIS AND ASCARIASIS 389 recorded in a three-pond system with total retention of ovicidal chemicals are added, Ascaris egg destruction only 6 days (Lakshminarayana and Abdulappa 1969), in night soil and sludge depends almost entirely on and Panicker and Krishnamoorthi (1978) found no time and temperature. Ascaris eggs in the effluent from four-pond systems. Sewage in Dushanbe (Tadzhik SSR, USSR) was treated in four ponds (an anaerobic pond with area 2 By pit latrines hectares, depth 1.5 meters and retention time 10 hours, Ascaris eggs in pit latrines can survive for 1-2 years, and three following ponds with area 4-4.5 hectares and especially if conditions are cool and wet and if the depth 0.6 meters). The total retention time was only 33 latrines are sealed with a covering of soil. Available hours. The effluent from the ponds was used to irrigate data come from temperate regions, and it is probable a rice paddy. Owing to the short overall retention time that survival times will be shorter in warmer climates. in the ponds, the quality of the effluent was not good In tropical and subtropical areas it can be assumed that (coliform count 106 per 100 milliliters; BOD5 39 pit contents will be free of viable Ascaris eggs after milligrams per liter). Inflowing sewage contained an being sealed for 1 year, and the necessary period is average of 23 helminth eggs per liter, whereas the probably less than this if the pit is in dry soil above the effluent contained none. Most eggs were removed in water table. the first anaerobic pond (Koltypin 1969). In early experiments in the USA, Stiles and Crohurst Ponds with short retention time may not remove all (1923) found that all Ascaris eggs died after being Ascaris eggs, especially during heavy rain or freezing buried under sawdust for 38 months. Experiments on conditions. Experiments in the Ukraine (USSR) found the viability of Ascaris eggs in pit latrines were that two-cell ponds, with total retention of 3.6 days, let conducted in the USSR with the object of determining through Ascaris eggs in winter when the ponds froze the length of storage before the excreta could be safely and the increased velocities of flow along the base of the employed for manuring fields and kitchen gardens. ponds picked up solids and eggs and carried them out Experimental pit latrines were in constant use by in the effluent. An average of 0.5 Ascaris eggs per liter workers of a state farm for a prescribed period of time, was found in the effluent in winter. A similar effect was after which three were covered with boards and earth, experienced during heavy summer rain, which also while one was left open. Samples were removed once a increased the velocity of flow through the ponds month. When examined immediately after removal, the (Ptitsyna 1966). eggs were invariably unsegmented-indicating that they were not developing in the pit latrines. In the open By tertiary treatment pit all eggs were dead after 6 months. In the covered pits 97 percent died after 6-8 months, and 10-13 months Filtration through soil or sand should remove were required for 100 percent destruction. Egg Ascaris eggs from sewage effluents. The retained eggs destruction was more rapid in summer, and complete may develop to the infective stage and survive for many Ascaris elimination was obtained by sealing the pit in months. early spring (February-March) and reopening in Effluent chlorination is of no value in Ascaris November. In feces diluted with water (1 :1 by volume), removal. Chlorine and chloramine are ineffective survival was prolonged, and 95.5 percent of the eggs against Ascaris eggs at, or greatly above, the perished only after 20 months (Vassilkova 1940). More concentrations typically applied to sewage. Low recent work in the USSR found that some Ascaris eggs chlorine doses may even accelerate Ascaris egg in pit latrines survived for over 18 months and outlived development. (Iwariczuk and Dozaiska 1957; Trichuris eggs (Biziulevicius 1965). Krishnaswami and Post 1968). Inactivation by Night Soil and Sludge By biogas plants Treatment Processes The removal of Ascaris eggs in biogas plants depends on the retention time and the degree to which Ascaris eggs tend to become concentrated in the the design prevents short-circuiting of flow. Chinese sludge of all sewage treatment processes, and high data suggest that 2-7 percent of influent Ascaris eggs concentrations are found in night soil. Their removal will appear in the effluent (Hou and others 1959; from these materials is therefore of considerable McGarry and Stainforth 1978; Szechwan Research importance. Unless extreme desiccation occurs or Institute 1974). The eggs removed settle to the sludge 390 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS layer, where they remain viable for many months. taneous hatching in aerobic digestion may have Studies in Szechwan showed that adding small contributed to egg destruction. At 30°C, viability was amounts of waste frequently, improving design to better maintained when eggs were kept in night soil reduce short-circuiting, and increasing the organic than when they were kept in water. Complete egg content of the influent all reduced the egg concentration destruction was not possible unless temperatures were in the effluent. maintained above 45°C in aerobic processes and 38°C in anaerobic processes. By digestion A. suum eggs in swine wastes (2 volumes of pig feces plus 1 volume of pig urine plus 17-32 volumes of water) Mesophilic digestion, or digestion at cooler tem- readily survived aerobic and anaerobic digestion for 68 peratures, does not greatly reduce the concentration of days at 12°C (over 90 percent remained viable). At Ascaris eggs in sludge (Kabler 1959). Ascaris eggs have 22°C over 47 days, under aerobic conditions 89 percent been frequently isolated from digested sludge, for of eggs developed to the infective stage, whereas under instance in the USA (Cram 1943; Fitzgerald 1981) and anaerobic conditions eggs did not develop but the USSR (Vassilkova 1936), and digestion periods far remained alive (Marti, Booram, and Hale 1980). longer than normally employed are required before a Thermophilic digestion, like all other processes significant Ascaris reduction can be obtained. involving raised temperatures ( >45°C), can be highly Experiments in India showed that 40 percent of effective in Ascaris egg destruction (figure 23-2). Ascaris eggs held at 36°C for 50 days were still viable, Burden and Ginnivan (1978) studied seeded A. suum and a few viable eggs could still be isolated after 150 eggs in pig slurry (95 percent water) under aerobic days (Bhaskaran and others 1956). A. suum eggs were thermophilic digestion at 55°C. Ninety percent of held for 21 days at 38°C in sludge from various sewage unembryonated A. suum eggs were dead (judged by treatment works in the Chicago area (USA). With the failure to embryonate in culture) after 15 minutes, and exception of one sample, at least 46 percent of the eggs all were dead after 30 minutes. Embryonated eggs were remained viable, and some were then found to be all dead (judged by failure to infect piglets) after 15 infective to pigs (Fitzgerald and Ashley 1977). minutes. Cram and Hicks (1944) reported that 10 percent of Ascaris eggs in digesting sludge were viable after 6 months, and some were still viable after 1 year. Eggs By storage previously embryonated appeared to be more suscep- Storage of sludge at ambient temperatures will tible to subsequent anaerobic digestion than unde- eliminate Ascaris eggs if the storage period is long veloped eggs. In Johannesburg (South Africa) raw enough. Nine months were not sufficient in Pretoria, sludges contained between 50 and 243 Ascaris eggs per South Africa (Murray 1960), no loss of viability gram, whereas digested sludges contained 105-552 per occurred after 44 days in pulverized sludge in the USA gram. The effect of sludge digcstion in concentrating (Cram and Hicks 1944), and 2 years were required for eggs was noted. However, 74 percent of eggs in raw complete elimination of Ascaris eggs in Moscow, sludge were viable compared with only 39 percent USSR (Vassilkova 1936). A. suum eggs stored in silage viable in digested sludge (Keller and Hide 1951). At for up to 4 months were still infective to mice, but eggs Koutim (Czechoslovakia) up to 100 percent of Ascaris stored for 5 months were not (Pavlov 1958). eggs in raw sludge were viable, whereas only 58 percent If storage is accompanied by drying, death will be in digested sludge were viable (Kralova and Safranek more rapid, but survival times of several months are 1957). still possible. In laboratory experiments in India, Under anaerobic conditions eggs tend to stay alive sludge samples were kept in open dishes exposed to but not develop. Under aerobic conditions and diffused sunlight. After 51 days, the moisture content temperatures above 20°C, eggs develop and may had dropped to 3.1 percent, and yet 10 percent of eggs become infective. Reyes, Kruse and Batson (1963) were still viable (Bhaskaran and others 1956). reported studies on aerobic and anaerobic batch Survival of Ascaris eggs in night soil is more limited digestions of night soil seeded with A. suum eggs. At low than in sludge if the night soil contains urine. Tests in temperatures, both aerobic and anaerobic digestion Japan on the viability of Ascaris eggs in night soil (1 tended to preserve eggs in a viable condition. In the volume feces to 5 volumes urine) indicated that the 25°C-35°C range, both systems resulted in some egg minimum storage temperatures and times needed for destruction attributable to factors other than heat. complete kill were 30°C for 40 days, 32°C for 25 days, Oxygen starvation in anaerobic digestion and spon- or 34°C for 11 days (Nishi 1969). ASCARIS AND ASCARIASIS 391 Storage will be more effective in destroying Ascaris thicker layers (Hogg 1950). In other experiments, eggs in warm or dry climates than in cool or wet Ascaris survived drying to a point where the moisture climates. content of the sludge reached 5.8 percent but failed to survive when the moisture content reached a lower By drying figure (Cram and Hicks 1944). Desiccation is antagonistic to Ascaris eggs. At moisture contents below about 5 percent, death may be By heating fairly rapid, especially at warm temperatures (Keller The only method of achieving Ascaris egg elim- 1951a). These low moisture contents are never ination, without prolonged storage or adding ovicides, achieved in normal sludge drying practice, and a is by heating. The literature contains many studies into typical "dewatered" sludge contains about 75 percent the time-temperature survival of eggs under different water. Therefore, sludge drying processes are anal- environmental conditions. These studies are some- ogous to sludge storage (see above) in their effects upon times contradictory. All relevant data found in the Ascaris eggs, and long holding times are necessary to literature have therefore been plotted on figure 23-2, eliminate Ascaris eggs. Required holding times will be and an upper boundary line has been drawn. somewhat less in warm climates than in temperate Temperatures and times above this line should regions. guarantee complete destruction of Ascaris eggs. After 4 years on drying beds at Kharkov (USSR), It is clear from figure 23-2 that temperatures of over sludge still contained 18 Ascaris eggs per gram near the 45°C must be reached, and preferably over 50°C. The surface and 7 eggs per gram at a depth of 1 meter practical way of achieving this is aerobic thermophilic (Vishnevskaya 1938). When sludge was dried in the sun composting of sludge or night soil mixed with organic in South Africa for 4 months in layers ranging in refuse. Other, somewhat impractical methods have thickness from 37 to 150 millimeters, Ascaris eggs were been tried. completely eliminated from the 37-millimeter layer, in In a village in Shiga Prefecture in Japan, a sheet-iron which the moisture content had fallen from 84 percent container with a capacity of 14 liters was installed to below 3 percent. Ascaris eggs still remained in the under the seat of each domestic privy (Katayama 80. _0 75 75 70s ONF 70 65- x; xx 65 6C,a 0 o 5CoO 40 0 * - 4 5- SAFETY xo 5IT x x -40 4 0~~~~~~~~~~~~~~~~~xe 35 . X 35 30 DD 100% destruction of Asccis eggs | 4xs * 30 2 L-ss thon 100%/o destructiH of Ascori, eggs * 20 ' 20 0.01 0.1 1.0 10 100 1000 10000 lm,in Ihour Iday I week lI eth Iyear TIME (HOURS) Figure 23-2. The itifluence of time and tempe7-ature on Ascaris eggs. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death 392 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS 1955). The contents were emptied occasionally into a Table 23-3. Some studies on Ascaris eggs in 200-liter drum and heated to 60°C with firewood. All composting processes parasite eggs and fly maggots were completely destroyed. The night soil was then used for fertilization. Countrjy Source The effect was demonstrated by a decline in the prevalence of Ascaris and hookworm infections as well China Department of Environmental Health (1975) as by a decrease in the count of embryonated Ascaris Hou and others (1959) eggs found in the farm soil of the village, compared with McGarry and Stainforth (1978) a nearby control village. Scott (1952. 1953) Germany Borchert and Kalbe (1955) Democratic Kalbe (1955) By composting Republic Aerobic composting of night soil or sludge with India Bhaskaran and others (1957) refuse, woodchips, straw or other carbonaceous Malaysia Scharff (1940) bulking material is an efficient method of eliminating Poland Iwaficzuk (1963) Ascaris eggs. Success depends on careful process South Africa Keller (1951b, 1951c) management and, in particular, on regulation of the Krige (1964) moisture content, the carbon to nitrogen ratio, and the Murray (1960) pile temperature. It is pile temperature that is crucial to Steer and Windt (1978) Ascaris egg elimination, and the required time- Sri Lanka Nicholls and Gunawardana (1939) temperature combinations may be read off figure 23-2. USA Brandon (1978) To achieve these time-temperature conditions through- Theis, Bolton and Storm (1978) out the composting mass requires lagging by covering Wiley and Westerberg (1969) the heap with old compost or mud, forced draft USSR Biziulevicius (1961) aeration, regular turning, or a combination of these. Gudzhabidze and Lvubchenko (1959) Studies on Ascaris eggs in composting processes are Reviews of Feachem and others (19R0) listed in table 23-3. Ascaris eggs are the most hardy of several Hays (1977) all excreted pathogens considered in this book. The countries Petrik (1954) time-temperature requirements for complete in- Wiley (1962) activation are more stringent than for other pathogens, with the exception of enteroviruses at short retention times (see figure 9-2). For this reason, and because great variety of chemicals have been tried in the field viruses are technically difficult to enumerate in and in the laboratory. Two field trials in Japan, one of compost samples, Ascaris eggs make an excellent sodium nitrite in acidified night soil and one of indicator of compost quality. Ascaris egg standards for thiabendazole, have shown that night soil treatment compost have been adopted in China and Vietnam. reduced ascariasis prevalence (Kozai 1960a; Kutsumi Where facilities are excellent, a combined enterovirus- 1969). The literature on chemical ovicides is listed in Salmonella-Ascaris standard is appropriate. Where table 23-4. A wide variety of chemicals have effect. laboratory facilities are more limited, a Salmonella- Sodium nitrite and thiabendazole are the most widely Ascaris or fecal streptococci-Ascaris standard should tried. The practicability and cost of this method must be adopted. Where laboratory facilities are poor, an be questioned, however. Thermophilic composting of Ascaris standard alone will prove adequate. night soil or sludge with refuse is a more realistic, and probably cheaper, method of making fecal products safe for land application. An added advantage of By other processes thermophilic composting is that it will destroy all other A variety of more technically complex sludge pathogens in the compost, which has not been claimed treatment processes is available. Those that involve for the application of chemical ovicides. heating may be highly effective; those that do not will not. The two exceptions to this are the use of chemical IRRADIATION. Data on the effect of radiation on ovicides and irradiation. Ascaris eggs in sludge are limited. Brandon (1978) reported that 1.5 kilogray killed over 99 percent of CHEMICAL OVICIDES: An alternative to heating is to Ascaris eggs. Lessel and Suess (1978) found a 100 treat night soil or sludge with an ovicidal chemical. A percent kill at a dose of 3 kilogray, whereas Osborn ASCARIS AND ASCARIASIS 393 Table 23-4. Some literature on Ascaris ovicides bacteria (1 log reduction per 200-300 gray), and the effect on enteroviruses (1 log reduction per 2-5 Media in which kilogray). Ovicide eggs contained Source Benzylphenol Water Nasi4owska (1963) Literature Cited Carbathion Dried sludge Chilikin (1975) Carbon Cesspool Matsumura and Anders, W. (1954). The Berlin sewer workers. ZeitschriJtfuir disulphide contents Osawa (1954) Hygiene und Infektionskrankheiten, 139 341 371. Chlorobenzyl- Water Nasilowska (1963) H d phenol Arfaa, F. and Ghadirian, E. (1978). The effect of mass- Coca Cola ND Bacev, Kolev and treatment in the control of helminthiasis in Isfahan, central Peeva (1972) Iran. Iranian Journal of Public Health, 7, 100-111. Creolin Water Simanek, Kr6 and Arfaa, F., Sahba, G. H., Farahmandian. I. and Jalali, H. Svoboda (1963) (1977). Evaluation of the effect of different methods of Cresol Water Fujita (1959) control of soil-transmitted helminths in Khuzestan, Cesspool Matsumura and southwest Iran. American Journal of Tropical Medicine and contents Osawa (1954) Hygiene, 26, 230-233. Detergents Water Jaskoski (1951) Atchley, F. O., Wysham, D. N. and Hemphill, E. C. (1956). Vegetables Kumada (1965a: Mass treatment of ascariasis with a single dose of 1965b) Dicapthon Night soil Fujita (1960a) piperazine citrate. American Journal of Tropical Medicine (isochloro- Water Fujita (1960b) and Hygiene, 5, 881-887. thion) Bacev, K., Kolev, G. and Peeva, Z. (1972). Inhibitors of the Fertilizers Water Hamdy (1969, 1970b) development of helminth eggs and of rabbit coccidial Hexachloro- Water Nasilowska (1963) oocysts. Epideniiologiia, Microbiologiia i Infektsionzni phenol Bolesti, 9, 195-200. Nitric acid ND Hsu and Hsu (1940) Barchenko, L. I. (1953). The importance of some food p-Thiocresol Cesspool Matsumura and products as possible factors in the geohelminth infection of contents Osawa (1954) a population. In Papers on Helminthology Presented to Pentachiloro- Water Fujita (1959) Academician K. I. Skryabin on his 75th Birthdav, pp. 39-43. phenol Phenol ND Hsu and Hsu (1940) Moscow: Izdatelstvo Akademii Nauk SSR. Water Simunek, Krn and (1955). Routes of infection with ascariasis in living Svoboda (1963) quarters. Meditsinskaia Parazitologiia i Parazitarnye Cesspool Matsumura and Bolezni, 24, 122-125. contents Osawa (1954) Baumhogger, W. (1949). Ascariasis in Darmstadt and Hessen Proteins Night soil Matsumura and Oda as seen by a water-waste engineer. Z, ,i . i,, it far Hygiene (1954) und Infektionskrankheiten, 129, 488-506. Sodium nitrite Pickle Kim and Yoon (1966) Ben-Ari, J. (t962). The incidence of Ascaris lumbricoides and Acidified night Kozai (1960a, 1960b, Trichuris trichiiura in Jerusalem during the period of soil 1960c,1962) 1934-1960. American Journal of Tropical Medicine and Acidified night Kozai and soil Kobayashi (1961) Hygiene, 11, 366-368. Sodium penta- Water. Kutsumi (1963) Bhaibulaya, M., Punnavutti, V., Yamput, S., Indra-Ngarm, chloro- acidified night S., Pahuchon, W., Hongsuwan. S., Vajrasthira, S. and phenate soil Harinasuta, C. (1977). Control trial of soil-transmitted Sulphuric acid ND Hsu and Hsu (1940) helminthic infections with pyrantel pamoate. Southeast Thiabendazole Pickle Kim and Yoon (1966) Asian Journal of Tropical Medicine and Public Healthz, 8, Night soil Kutsumi (1964a, 329-334. 1964b, 1969): Bhaskaran, T. R., Gosh Roy, B. K., Sampathkumaran, M. A., Kutsumi and Radhakrishnan, I. and Mukherjee, D. B. (1957). Studies on Komiya 11965) the survival of pathogens in nightsoil compost. Indian Xylene Cesspool Matsumura and contents Osawa (1954) Journal of Agricultural Science, 27, 91-102. Bhaskaran, T. R., Sampathkumaran, M. A., Sur, T. C. and ND No data. Radhakrishnan, I. (1956). Studies on the effect of sewage treatment processes on the survival of intestinal parasites. and Hattingh (1978) reported 99 percent inactivation Indian Journal oJ Medical Researchl, 44, 163-180. at 1 kilogray but less than 100 percent inactivation at Biagi, F. F. and Rodriguez, 0. (1960). A study of ascariasis 5 kilogray. It appears that the effect of radiation on eradication by repeated mass treatment. American Journal Ascaris eggs lies somewhere between the effect on of Tropical Medicine and Hygiene, 9, 274-276. 394 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Biziulevicius, S. (1954). Role of vegetables and berries in the miology of human ascariasis. Journal of Parasitology, 17, epidemiology of helminthiasis in the population of 121-144. Lithuania. Meditsinskaia Parazitologiia i Parazitarnye Cort, W. W., Otto, G. F. and Spindler, L. A. (1930). Bolezni, 23, 124-126. Investigations on Ascaris lumbricoides and the associated (1965). Studies on the viability of Ascaris and intestinal helminths of man in southwestern Virginia. Trichuris eggs in buried lavatory pits. Acta Parasitologica American Journal of Hygiene, 11, 1-55. Lithuanica, 5, 77-84. Cort, W. W., Schapiro, L. and Stoll, N. R. (1929). A study of - (1961). On the vitality of ascarid (Ascaris lum- reinfection after treatment with hookworm and Ascaris in bricoides) and whipworm (Trichuris trichiura) eggs in two villages in Panama. American Journal of Hygiene, 10, compost manure heaps. Acta Parasitologica Lithuanica, 3, 614 625. 51-69. Cort, W. W. and Stoll, N. R. (1931). Studies on Ascaris Blumenthal. D. S. (1977). Intestinal nematodes in the United linbricoides and Trichuris trichiura in China. American States. New England Journal of Medicine, 297, 1437-1439. Journal of Hygiene, 14, 655-689. Borchert, A. and Kalbe, 1. (1955). Resistance of Ascaris eggs Cort, W. W., Stoll, N. R.. Riley, W. A. and Sweet, W. C. (1929). in natural compost. Archic fOir experimentelle VIII. Quantitative studies on the distribution of Ascaris Veterindrmedizin, 9, 142-144. lumbricoides and Trichuris trichiiura in Panama. American Bradley, R. M. and Hadidy, S. (1981). Parasitic infestation Journal of Hygiene Monographic Series No. 9, 161-209. and the use ofuntreated sewage for irrigation ofvegetables Coumbaras, A., Lariviere, M., Beauvais, B., Languillat, G. with particular reference to Aleppo, Syria. Public Health and Turquet, M. (1976). Le charge parasitaire moyenne, Engineer, 9, 154-157. critere d'evaluation de la contamination geohelminthique Brandon, J. R. (1978). Parasites in Soil/Sludge Systems. d'une population, et d'application des actions Report SAND77-1970. Albuquerque, N.M.: Sandia d'assainissement. Bulletin de la Societe de Pathologie Laboratories. Exotique et de ses Filiales, 69, 95-100. Brown, H. W. (1927). Human Ascaris as a household Cram, E. B. (1943). The effect of various treatment processes infection. Journal of Parasitology, 13, 206- 12. on the survival of helminth ova and protozoan cysts in Bukh, F. L. (1945). The data ofhelminth egg inspection ofthe sewage. Sewage Works Journal, 15, 1119-1138. sources of water supply of Ufa. Meditsinskaia Cram, E. B. and Hicks, D. 0. (1944). The effect of sludge Parazitologiia i Parazitarnye Bolezli, 14, 66-67. digestion, drying and supplemental treatment on eggs of Burden, D. J. and Ginnivan, M. J. (1978). The destruction of Ascaris lumbricoides. P . - d', . of the Helminthological pig helminth ova and larvae in a slurry treatment process. Society of Waslhington, 11, 1-9. Veterinary Record, 103, 373-375. Department of Environmental Health, Institute of Health, Cabrera, B. D.,Arambulo, P. V.III and Portillo. G. P. (1975). Chinese Academy of Medical Sciences, Peking (1975). Ascariasis control and/or eradication in a rural com- Sanitary effects of urban garbage and nightsoil compost- munity in the Philippines. Southeast Asian Journal of ing. Chinese Medical Journal, 1, 407-412. Tropical Medicine and Public Health, 6, 510 518. Drozdova, Z. K., Romanenko, N. A., Lapshina, I. G., Chandler, A. C. (1954). A comparison of helminthic and Andreeva, N. L., Vlasova, N. I. and Guseva., M. K. (1973). protozoan infections in two Egyptian villages two years The survival rate of Ascaris eggs in the soil and sludge in a after the installation of sanitary improvements in one of silty area of the Volgograd region. Meditsinskaia them. American Journal of Tropical Medicine and Hygiene, Parazitologiia i Parazitarnye Bolezni, 42, 146-148. 3, 59-73. Dunlop. S. C. and Wang, W. L. L. (1961). Studies on the use Chen, E. R. and Hsieh, H. C. (1969). Study of ascariasis of sewage effluent for irrigation of truck crops. Journal of control in Taiwan. Journal of the Formosan Medical Milk and Food Technology, 23. 44-47. Association, 68, 411-427. Eyles, D. E., Jones, F. E. and Smith, C. S. (1953). A study of Chen, P. C. (1970). Ascariasis: beliefs and practices of a rural Endantoeba hlistolytica and other intestinal parasites in a Malay community. Medical Journal of Malaysia, 24, rural West Tennessee community. American Journal of 176-182. Tropical Medicine and Hygiene, 2, 173-190. Chilikin, M. M. (1975). The use of carbathion for the Faust, E. C. and Mugaburu, L. G. (1965). Parasitological anthelminthic treatment of sewage sludge. Medistinskaia surveys in Cali, Departamento del Valle, Colombia. XI. .i, 1:.!. i. . ,,. i Parazitarnve Bolezni, 44, 82-86. Intestinal parasites in Ward Siloe, Cali, during a four-year Choi, D. W. (1970). Incidence of parasite eggs on vegetable period 1956-1960. American Journal of Tropical Medicine leaves, watercress and carrots. Korean Journal of and Hygiene, 14, 276-289. Parasitology. 8, 19. Feachem, R. G., Bradley, D. J., Garelick, H. and Mara, D. D. Clark, C. S., Cleary. E. J., Schiff, G. M., Linnemann, C. C. Jr, (1980). Health Aspects of Excreta and Sullage Phair, J. P. and Briggs, T. M. (1976). Disease risks of Management: A State-of-the-Art Reuiew. Appropriate occupational exposure to sewage. Journal of the Technology for Water Supply and Sanitation, vol. 3. Environmental Engineering Division, American Society of Washington, D.C.: The World Bank, Transportation, Civil Engineers, 102, 375-388. Water and Telecommunications Department. Cort, W. W. (1931). Recent investigations on the epide- Fitzgerald, P. R. (1981). Helminth and Heavy Metals ASCARIS AND ASCARIASIS 395 Transmissionfrom Anaerobically Digested Sewage Sludge. Hamdy, E. I. (1969). Effect of some nitrogenous fertilizers on Report EPA-600/S2-81-024. Cincinnatti, Ohio: US Ascar-is lumbricoides eggs. Journal of the Egyptian Medical Environmental Protection Agency. Association, 52, 949-953. Fitzgerald, P. R. and Ashley, R. F. (1977). Differential (1970a). Urine as an Ascaris lumbricoides ovicide. survival of Ascaris ova in wastewater sludge. Journal of the Journal of the Egyptian Medical Association, 53, 261-264. Water Pollution Control Federation, 49, 1722-1724. (1970b). On the value of some non-nitrogenous Forstner, M. J. (1960). Parasitological investigations in the fertilizers as Ascaris ovicides. Journal of the Egyptian sewage works of Mindelheim to answer the question of Medical Association, 53, 363-367. worm infection of pasturing cattle on pastures watered Hays, B. D. (1977). Review paper: Potential for parasitic with waste water. Berliner und Miinchener tierarztliche disease transmission with land application of sewage plant Woclhenschrift, 73, 161-164. effluents and sludges. Water Research, 11, 583-595. Freij, L., Meeuwisse, G. W., Berg, N. O., Wall, S. and Gebre- Hendley, J. O., Williams, D. and Burke, G. (1973). Familial Medhin, M. (1979). Ascariasis and malnutrition. A study carriage of Ascaris. Pediatric Research, 7, 375/147. in urban Ethiopian children. American Journal of Clinical Hogg, E. S. (1950). A preliminary study of ova and cysts in Nutrition, 32, 1545-1553. Cydna digested sludge. Journal of the Institute of Sewage Fujita, K. (1959). Studies on the ovicidal effects of various Purification, part 1, 57 58. agricultural chemicals on Ascaris eggs. 1. Experiments in Hoghooghi, N., Badami, N., Barnett, R. and Jalayer, T. vitro. Japanese Journal of Parasitology, 8, 580-585. (1973). A survey of soil contamination and viability of (1960a). Studies on the ovicidal effects of agricultural Ascaris lumbricoides eggs in Isfahan, Iran. Pahlavi Medical chemicals on Ascaris eggs. 2. Effects on the eggs in Journal, 4, 53-60. nightsoil. Japanese Journal of Parasitology, 9, 69-72. Hou. T. C., Chung, H. L., Ho, L. Y. and Weng. H. C. (1959). (1960b). Studies on the ovicidal effects of agricultural Achievements in the fight against parasitic diseases in New chemicals on Ascaris eggs. 3. Influence of temperatures China. Chinese Medical Journal, 79, 493-520. upon the effectiveness. Japanese Journal of Parasitology, 9, Hsu, Y. C. and Hsu, H. S. (1940). Effects of chemical reagents 125-128. on the development of eggs of Ascaris lumbricoides. Peking Fulmer, H. S. and Huempfner, H. R. (1965). Intestinal Natural History Bulletin, 15, 103-118. helminths in eastern Kentucky: a survey in three rural Iwariczuk, 1. (1963). Influence of compost making on the eggs counties. American Journal of Tropical Medicine and of man human intestinal helminths. Przeglad Hygiene, 14, 269-275. Epidemiologiczny, 17, 327-335. Garcia, E. G., Cabrera, B. D., Cruz, T. A. and Jueco, N. L. (1969). Exploration of river shores for the presence of (1961). Reinfection rates of successfully treated cases of human intestinal parasites. Wiadomosci Parazytologiczne, ascariasis. Journal of the Philippine Medical Association, 15, 67 70. 37, 239-243. Iwariczuk, I. and Do2afiska, W. (1957). The influence of Gartner, H. and Muting, L. (1951a). On the infiltration depth chlorination on the survival of Ascaris suis eggs in sewage. of Ascaris eggs in land. Zeitschrift fzir Hygiene und Acta Parasitologica Polonica, 5, 429-448. Infektionskrankheiten, 132, 59-63. Jancloes, M. F., Cornet, P. and Thienpont, D. (1979). Mass (1951b). SurvivalofAscariseggsin land irrigatedwith control of ascariasis with single oral doses of levamisole: a sewage. Zeitschriftfiir Hygiene und Infektionskrankheiten, controlled comparison in 3,056 subjects between three 132, 244-249. incomplete population coverages. Tropical and Gelpi, A. P. and Mustafa, A. (1967). Seasonal pneumonitis Geographical Medicine, 31, 111-121. with eosinophilia: a study of larval ascariasis in Saudi Jaskoski, B. J. (1951). Effects of detergents on embryogeny of Arabs. American Joutrnal of Tropical Medicine and Ascaris lumbricoides var. suum. Journal of Parasitology, 37, Hygiene, 16, 646-657. 22. Ghadirian, E., Arfaa, F., Missaghian, Gh. and Bahrani, H. Jones, H. I. (1976a). The role of pigs in the dissemination of (1973). Prevalence of intestinal helminthiasis in Ascaris and hookworm infections in Papua New Guinea. Kermanshah city and some villages in the province. Papua New Guinea Medical Journal, 19, 153-155. Iranian Journal of Public Health, 2, 90-101. (1976b). A study of human intestinal helminthiases on Goryachev, P. P. (1947). Investigation of helminth eggs in the Kar Kar Island, Madang Province. Papua New Guinea waters of the rivers Irtish and Om. Meditsinskaia Medical Journal, 19, 165-172. Parazitologiia i Parazitarnye Bolezni, 16, 75-78. Jueco, N. L. and Cabrera, B. D. (1971). Reinfection rates of Gudzhabidze, S. I. and Lyubchenko, S. D. (1959). Control of successfully treated cases of ascariasis in Victoria, Laguna. ascariasis and ancylostomiasis by composting of organic Journal of the Philippine Medical Association, 47, 449-454. waste material. Meditsinskaia Para7itologlia i Kabler, P. (1959). The removal of pathogenic micro- Parazitarnye Bolezni, 28, 576-578. organisms by sewage treatment processes. Sewage and Gupta, M. C., Mithal, S., Arora, K. L. and Tandon, B. N. Industrial Wastes, 31, 1373-1382. (1977). Effect of periodic deworming on nutritional status Kalbe, 1. (1955). The action of natural composting on the of Ascaris-infested preschool children receiving sup- viability of Ascaris ova. Deutsche Landwirtschatl, 6, plementary food. Lancet, 2, 108-110. 440-441. 396 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS ---(1956). Investigations of parasites in sewage in several ovicide for nightsoil. (1). Japanese Journ7al of .1 towns in East Germany. Zeitschri/t /fii die Gesainte 9, 202-210. Hygiene und i/ire Gren7gebiete, 2, 334-343. ---(1960b). Re-evaluation of sodium nitrite as an ovicide Katayama, Y. (1955). Sanitary treatment of human excreta for night soil. (21. Japanese Journzal oJ P . ; ' ., 9, by heating process. 16. Effect of the treatment applied to a 519-528. farm-village. Part 1. Japan?ese Journal of the Nation's (1960c). Re-evaluation of sodium nitrite as an ovicide Health. 24, 1-12. for night soil. (3). Jpapnese Journal of Parasitology, 9, Kawagoe, K.. Nishi. H.. Shibata. E. and Yamada, S. (1958). 529-540. On the effect of nightsoil treatment upon heating process - (1962). Re-evaluation of sodium nitrite as an ovicide utilizing surplus midnight electric power upon the for night soil. (4). Japanese Journal of Parusitology. 11, incidence of parasitic infection of farmers. Japanese 400-410. Journal of tle Nation's Healtl, 27, 162-165. Kozai, I. and Kobayashi. A. (1961). Ovicidal effect of a Keller, P. (1951a). Sterilization of sewage sludges. 1. A review sodium nitrite preparation 'Derisan' on Ascaris ova in of the literature pertaining to the occurrence and viability nightsoil. Japanese Journ2al of Parasitology, 10, 56-61. of parasitic ova and cysts in sewage with particular Kralovd. E. and Safranek. V. (1957). Helminthological reference to Ascaris lIinbr icoides. Journal of thie Institute oJ investigation of sediments from the waste water refining Seuoage Purification, part 1, 92-99. station at Kourim. Ceskoslorenskdi Hygiena, 2, 399-404. -- (19516). Sterilization of sewage sludges. 2. The Krige.P. R. (1964). Asurvey of thepathogenic organisms and influence of heat treatment on the ova of Ascaris helminthic ova in composts and sewage sludge. Journal of lunitbri-coides in sewage. Journal oJ the Institutte oJ Sewage the Institute of Sewage Purification. part 3, 215-220. 1"", '. ,,,, part 1, 100-109. Krishnaswami, M. A. and Post. F. J. (1968). Effect of chlorine --(1951c). Sterilization of sewage sludges. Public on Ascaris (Nematoda) eggs. Heatlr Laboratory Science, 5, Health, Johannesburg. 15, 11-17. 225-232. Keller, P. and Hide, C. G. (1951). Sterilization of sewage Kumada,M. (1965a). Tests ofsyntheticdetergents on sale for sludges. Incidence and relative viability of Ascaris ova at their potency in eliminating Ascuris eggs on vegetable sewage disposal works in the Johannesburg area. Southl leaves, with special reference to fat removal test. Jopanese African Medical Journual. 25, 338-342. Journal of Parasitology, 14, 162-168. Khalil, M. (1926). The relation between sanitation and (1965b). Some factors influencing the action of parasitic infections in the tropics. Journal of tlhe Royal detergent in eliminating Ascuris eggs from vegetable Sanitarv Institute, 47, 210-215. leaves. Japanese Journal of Parasitology. 14, 495-499. (1931). The pail closet as an efficient means of Kutsumi, H. (1963). Studies on ovicides against helminth controlling human helminth infection as observed in Tura eggs in ritro. I. Ovicidal activity of NaPCP on Ascaoits eggs Prison, Egypt, with a discussion on the source of Ascaris and its decomposition by ultra-violet irradiation. Japanese infection. Annalsof Tropical Medicine and Parasitology, 25, Journal of Parasitology, 12, 485-496. 35-62. _ (1964a). Studies on ovicides against helminth eggs in - (1933). Report on the Mission of the Researclh citro. II. The ovicidal activity of thiabendazole against Institute, Public Health Department, and the Faculty of Ascaris eggs in water and in nightsoil. Japanese Journal oj' Medicine, Cairo, to Siwa Oasis, in January 1933,fbr rihe Parasitology, 13, 32-42. Study of Parasitic Infections, Malaria and Diplthleria. (1964b). Studies on ovicides against helminth eggs in Cairo: Ministry of the Interior, Public Health vitro. III. Ovicidal effects of water-soluble and semi-water- Department. soluble thiabendazole on Ascaris eggs in nightsoil and the Khaustov, J. M. (1935). Vegetables as a factor in transmission time-concentration relationship for complete inhibition of of Trichocephialus (Trichuris) trichiiuris. Trudy larval formation. Japanese Journial of Parasitology, 13, Leningradskogo Institutu Epidemniologii i Bakteriologii 123-131. imeni Pastera, 2, 148-152. (1969). Epidemiological study on the preventive effect Kim, C. H. and Yoon, T. Y. (1966). Action of several of thiabendazole as an ovicide against human hookworm. chemicals on parasite eggs and larvae in Korean pickle Tric,h2uris and Ascaris infections. Japanese Journal of (kimchi). Korean Journal of Parasitology, 4, 47-51. Medical Science and Biology, 22, 51-64. Kirpichnikov, A. A. (1963). Methods of treating town refuse. Kutsumi, H. and Komiya, Y. (1965). Effect of thiabendazole Meditsinskaia F. A'. ;I !,, i Paracitarnye Bolezni, 32, as an ovicide on helminth eggs in nightsoil. Japanese 147-151. Journal of Medical Science and Biology, 18, 203-224. Kleevens, J. W. L. (1966). Re-housing and infections by soil- Lakshminaravana, J. S. S. and Abdulappa, M. K. (1969). The transmitted helminths in Singapore. Singapore Medical effect of sewage stabilization ponds on helminths. In Low Journal, 7, 12-29. Cost Waste Treat7nent, ed. Sastry, C. A.. pp. 290-299. Koltypin. Y. A. (1969). Decontamination of sewage in paddy Nagpur, India: Central Public Health Engineering ficlds. Gigiena i San/taria, No. 7, 74-76. Research Institute. Kozai, I. (1960a). Re-evaluation of sodium nitrite as an Lane, C. (1934). The prevention of Ascaris infection: a critical ASCARIS AND ASCARIASIS 397 review. Tropical Diseases Bulletin, 31, 605-615. intestinal helminthiasis in Dickleh, Arasbaran, northwest Lessel, T. and Suess, A. (1978). Hygienization of sewage Iran. Acta Medica Iranica, 14, 153-157. sludge by gamma irradiation: experience with an Moore, H. A.. de la Cruz, E. and Vargas-Mendez, 0. (1965). operating pilot plant. Progress in Water Technology, 10, Diarrheal disease studies in Costa Rica. IV. The influence 641-652. of sanitation upon the prevalence of intestinal infection Liebmann, H. (1965). Investigations about helminth ova in and diarrheal disease. American Journal of Epideoiology. sewage and wastes in Japan. Berliner lnod Munchener 82, 162-184. Tierarztliche II .. ., " l. 78, 106-108. Murray, H. M. (1960). The incidence of Ascaris ova in Livingstone, D. J. (1978). Decay of microorganisms in the Pretoria sludge and their reduction by storage (matu- marine environment. In Proceedinigs of'the Symnposiumn on ration) in large heaps. Journtal of the Institute of Sewvage DisinJection of Water. Pretoria, South Africa: National P - ^ K.,i- . parts 3-4. 337-344. Institute for Water Research. Nasitowska, M. (1963). The action of N-methyl- Lo, E. K. C., Varughese, J., Ghouse, A. and Noor, M. (1979). ditiocarbamic acid and preparations based on diphenylo- Helminthiases in peninsular Malaysia-prevalence and methanes on eggs of helminths. Wiadomno.sci density of infestation of hookworm, Ascaris and Tricliuris Parazytologiczne, 9, 139-141. in rural school children. Medical Journal of Malaysia, 34, Nicholls, L. and Gunawardana, S. A. (1939). The destruction 95-99. of helminth ova in nightsoil by composting. Ceylon Journ-llal Lysek, H. (1959). A contribution to the role of soil and of Science, Section D, 5, 1-9. vegetables in the epidemiology of geohelminths. Nishi, S. (1969). Studies on the ovicidal effect of nightsoil on CeskoslovenskdEpidemiologie, ll.;. 12...I....m..-,' I,1unologie, Ascaris eggs. Japanese Journal of Parasitology, 18, 8, 137-140. 131-140. (1964). On the destruction of Ascuris eggs in the soil. Nolf, L. 0. (1932). Experimental studies on certain factors In Pr,,-edU2, of thze First International Congress of influencing the development and viability of the ova of the Par asitology, Romne, Sept. 21-26, 1964, vol. 2, pp. 788-789. human Trichlur is as compared with those of the human Oxford: Pergamon. Ascaris. American Joulrnal of Hygiene, 16, 288-322. Lysek, H. and Bacovsky J. (1979). Penetration of ovicidal Nupen, E. M. and de Villiers, R. H. (1975). Th7e Evaluation of fungi into altered eggs of Ascaris luhbricoides. Folia Patlhogenic Parasites in Water Environmients. Project Pcarasitologica, 26, 139-142. Report no. 13. Pretoria, South Africa: National Institute McGarry, M. G. and Stainforth, J. (1978). Co0npost. Fertilizer for Water Research. and Biogas Production fifi-o Hn inan anid Fcartmi Wastes in the Osborn, D. W. and Hattingh. W. H. J. (1978). Disinfection of People's Repuiblic of China. Ottawa: International sewage sludge: a review. WPater Soluth Africa, 4, 169-178. Development Research Centre. Otto, G. F., Cort, W. W. and Keller, A. E. (1931). Marti, 0. G., Booram, C. V. and Hale, 0. M. (1980). Survival Environmental studies of families in Tennessee infested of eggs and larvae of swine nematode parasites in aerobic with Ascaris, Trichuris and hookworm. American Jou-rnal and anaerobic waste treatment systems. Journzalf f of Hygiene. 14, 156-193. Environmental Quiality, 9, 401-405. Otto, G. F. and Spindler, L. A. (1930). Effect of partial Massoud, J. (1980). Long-term mass-chemotherapy in sanitation on infestation with intestinal parasites in reducin-g some common soil-transmitted helminths in- soutlhwest Virginia. Southiern- Medicul Journlal, 23, fection in Khuzestan, South-West of Iran. Abstract no. 556-561. 232. Abstracts of time lOthu Interniationcal Congress on Panicker, P. V. R. C. and Krishnamoorthi, K. P. (1978). Tropical Medicine and Malaria. Manila. Philippines. Elimination of enteric parasites during sewage treatment Massoud. J.. Arfaa, F., Jalali. H. and Keyvan, S. (1980). processes. Indian Associationfor Water Pollution Control Prevalence of intestinal helminths in Khuzestan, south- Technical Annulal, 5, 130-138. west Iran, 1977. Amnerican Journal of Tropical Medicimie and Pavlov, P. (1958). Research on the action of ensilage on Hygiene, 29, 389-392. nematode eggs and larvae during storage. Ceskosloveniskda Mata, L. J., Kromal. R. A., Urrutia. J. J. and Garcia. B. (1977). Parasitologie, 5. 125-128. Effect of infection on foodintake and the nutritional state: Petrik, M. (1954). Utilization of nightsoil, sewage, and perspectives as viewed from the village. Amnerican Journal sewage sludge in agriculture. Bulletini of the World Health oJ Clinical Nutritioni, 30, 1215-1227. Organization, 10, 207 228. Matsumura, T. and Oda, T. (1954). Studies on increase of Pierce, V., Ascoli, W., de Leon. R. and Gordon, J. E. (1962). death of Ascaris eggs in the mixture of feces and urine on Studies of diarrheal disease in Central America. ITI. protein addition. GunnZa Journal of Medical Sciences, 3, Specific etiology of endemic diarrhea and dysentery in 233-234. Guatemalan children. Anuerican Journial of Tropical Matsumura, T. and Osawa. M. (1954). Experimental studies Medicine and Hygiene, 11, 395-400. on Ascaris prevention by chemical disposal of cesspool. Ptitsyna, E. 1. (1966). Dehelminthization of sewage in Gunma Journlal of Aledical Sciences, 3, 319-320. biological oxidation ponds. Gigienua i Sanitaria, no. 5, Mobedi, I.. Arfaa, F. and Movafegh, C. (1971). Studies on 105-107. 398 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Raccurt, C., Vial, P. and Pierre-Louis, J. M. (1977). Etude Scott, J. C. (1952). Health and Agriculture in China: a epidemiologique des helminthiases intestinales a l'ile de la Fundamental Approach to Some of the Problems of World Tortue (Haiti). Bulletin de la Societe de Pathologie Hunger. London: Faber and Faber. Exotique et de ses Filiales, 70, 240-249. (1953). Health aspects of composting with nightsoil. Reyes, W. L., Kruse, C. W. and Batson, M. St. C. (1963). The Unpublished document, wHO/Env./San.,/44. Geneva: effect of aerobic and anaerobic digestion on eggs of Ascaris World Health Organization. lumbricoides var. suum in nightsoil. American Journal of Seo, B. S.. Cho, S. Y. and Chai, J. Y. (1979). Seasonal Tropical Medicine and Hygiene, 12, 46-55. fluctuation of Ascaris reinfection incidences in a rural Romanenko, N. A. (1969). Sanitary-helminthic evaluation of Korean population. Korean Journal of Parasitology, 17, subterranean irrigation with untreated sewage. 11-18. Meditsinskaia Parazitologiia i ParazitarnYe Bolezni. 38, Seo, B. S., Rim. H. J., Loh, I. K.. Lee, S. H., Cho, S. Y., Park, S. 154-156. C., Bae, J. W.. Kim, J. H., Lee, J. S.. Koo, B. Y. and Kim, K. (1971). Sanitary-helminthological evaluation of new S. (1969). Study on the status of helminthic infections in methods of irrigation with sewage. Meditsinskaia Koreans. Korean Journzal of Parasitology, 7, 53-70. Parazitologiia i Parazitarnye Bolezni, 40, 361-362. Simdnek. J., Krc, M. and Svoboda, L. (1963). A contribution Rosenberg, A. I. (1960). Sanitary and hygienic measures for on the action of ovicides on Ascaris suis in clean and the control offocal ascariasis. Meditsinskaia Parazitologiia polluted environments. Ceskoslouenska Parasitologie, 10, i Parazitarnye Bolezni, 29, 143-149. 277-281. Rowan, W. B. (1964). Sewage treatment and schistosome Sinnecker, H. (1958). The epidemiological significance of eggs. American Journal of Tropical Medicine and Hygiene, urban sewage in the spread of possible zooparasitic 13, 572-576. infections. Zeitschrift far die Gesamte Hygiene und ihre Rowan, W. B. and Gram, A. L. (1959). Quantitative recovery Grenzgebiete. 4, 98-115. of helminth eggs from relatively large samples of feces and Soh, C. T. (1960). The effects of natural food-preservative sewage. Journal of Parasitology, 45, 615-621. substances on the development and survival of intestinal Rudolfs, W., Falk, L. L. and Ragotzkie, R. A. (1950). helminth eggs and larvae. I. Action on Ascaris lumbricoides Literature review on the occurrence and survival of enteric, eggs. American Journal of Tropical Medicine and Hygiene, pathogenic, and related organisms in soil, water, sewage 9, 1-7. and sludges, and on vegetation. II. Animal parasites. (1973). Control of soil-transmitted helminths in Sewage and Industrial Wastes, 22, 1417-1427. Korea. Yonsei Reports on Tropical Medicine, 4, 102-125. (1951a). Contamination of vegetables grown in Soh. C. T., Kim. S. J., Chang, B. P., Youn, B. B. and Lee, J. H. polluted soil. III. Field studies on Ascaris eggs. Sewage and (1973). Faecal pollution in relation to soil-transmitted Industrial Wastes, 23, 656-660. helminthic infections. Korean Journal of Parasitology. 11, (1951b). Contamination of vegetables grown in 133. polluted soil. V. Helminthic decontamination. Sewage and Spillmann, R. K. (1975). Pulmonary ascariasis in tropical Industrial Wastes, 23, 853-860. communities. American Journal of Tropical Medicine and (1951c). Contamination of vegetables grown in Hygiene, 24, 791-800. polluted soil. VI. Applications of results. Sewage and Spindler, L. A. (1929). The relation of moisture to the Industrial Wastes, 23, 992-1000. distribution of human Trichuris and Ascaris. Amnerican Sadighian, A., Arfaa, F.. Ghadirian, E. and Movafagh, K. Journal oJ Hygiene, 10, 476-496. (1976). Contamination with helminth eggs of various Steer, A. G. and Windt, C. N. (1978). Composting and thefate processing stages of the sewage treatment plant in Isfahan, of Ascaris lumbricoides ova. Water South Africa, 4, Central Iran. Iranian Journal of Public Health, 5, 180-187. 129-133. Sahba, G. H. and Arfaa, F. (1967). The effect of sanitation on Stephenson, L. S. (1980). The contribution of Ascaris ascariasis in an Iranian village. Journal of Tropical lumbricoides to malnutrition in children. Parasitology, 81, Medicinte and Hygiene, 70, 37-39. 221-233. Scharff, J. W. (1940). Composting: the safe conversion of Stephenson, L. S., Crompton. D. W. T., Latham. M. C., village refuse and nightsoil into a valuable manure. Journal Schulpen. T. W. J., Nesheim, M. C. and Jansen, A. A. J. of the Malaya Branch, British Medical Association, 4, (1980). Relationships between Ascaris infection and 126- 135. growth of malnourished preschool children in Kenya. Schliessmann. D. J., Atchley, F. O., Wilcomb, M. J. and American Journal of Clinical Nutrition, 33, 1165-1172. Welch, S. F. (1958). Relation of Environmental Factors to Stiles, C. W. and Crohurst, H. R. (1923). The principles the Occurrence of Enteric Diseases in Areas of Eastern underlying the movement of Bacillus coli in groundwater, Kentucky. Public Health Monograph no. 54. Washington, with resulting pollution of wells. Public Health Reports, 38, D.C.: US Government Printing Office. 1350 1353. Scott, J. A. and Barlow, C. H. (1938). Limitations to the Szechwan Research Institute of Antiparasitic Diseases and control of helminth parasites in Egypt by means of Mienchu County Antischistosomiases Office, Szechwan treatment and sanitation. American Journal of Hygiene, 27, (1974). Digestion of nightsoil for destruction of parasite 619-648. ova. A report of investigation and experimental obser- ASCARIS AND ASCARIASIS 399 vation. Chinese Medical Journal, 93, 31. Vishnevskaya, S. M. (1938). The degree of dehelminthization Takenouchi, H., Kataoka, I., Yamamoto, S. and Nagasaki, S. of sewage at the Kharkov bio-station. Meditsinskaiu (1980). Detection of parasite eggs in surplus sludges from Parazitologiia i Parazitarnye Bolezni, 7, 450-454. night soil disposal plants. 1. Distribution survey of parasite Wang, W. L. L. and Dunlop, S. G. (1954). Animal parasites in eggs in Kochi Prefecture. Japanese Journal of Parasitology, sewage and irrigation water. Sewage and Industrial Wastes, 29, 319-324. 26, 1020-1032. Theis, J. H., Bolton, V. and Storm, D. R. (1978). Helminth ova Warren, K. S. (1974). Helminthic diseases endemic in the in soil and sludge from twelve U.S. urban areas. Journal of United States. American Journal of Tropical Medicine and the Water Pollution Control Federation, 50, 2485-2493. Hygiene, 23, 723-730. Thiers, G., Lassoued, H. and Abid, A. (1976). Study of Wiley, B. B. and Westerberg, S. C. (1969). Survival of human ascariasis in a single locality of the Cap Bon region pathogens in composted sewage. Applied Microbiology, 18, (Tunisia). Bulletin de la Societe Pathologie Exotique et de 994-1001. ses Filiales, 69, 320-329. Wiley, J. S. (1962). Pathogen survival in composting Thitasut, P. (1961). Action of aqueous solutions of iodine on municipal wastes. Journal of the Water Pollution Control fresh vegetables and on the infective stages of some Federation, 34, 80-90. common intestinal nematodes. American Journal of Willett, W. C., Kilama, W. L. and Kihamia, C. M. (1979). Tropical Medicine and Hygiene, 10, 39-43. Ascaris and growth rates: a randomized trial of treatment. Tomomatsu, S. and Takeuchi, M. (1961). Studies on American Journal of Public Healtlh, 69, 987-991. prevention of Ascaris infection by soaking raw vegetables Winfield, G. F. (1937). Studies on the control of fecal-borne in iodine-potassium iodide solution. Japanese Journal of diseases in North China. III. Family environmental factors Parasitology, 10, 527-530. affecting the spread of Ascaris lumbricoides in a rural UNEP (1976). Report on UNEP Schistosomiasis Study Tour of population. Chinese Medical Journal, 51, 643-658. China from 31 October to 18 November 1975. Winfield, G. F. and Yao, T. (1937). Studies on the control of Unpublished/mimeographed. Nairobi: United Nations fecal-borne diseases in North China. IV. Vegetables as a Environment Programme. factor in the spread of Ascaris lumbricoides. Chinese Usacheva, A. M. (1951). Survival of helminth eggs in water Medical Journal, 51, 919-926. and in river sediment. Gigiena i Sanitaria, Part 2, no. 12, Wright, W. H., Cram, E. B. and Nolan, M. 0. (1942). 12-17. Preliminary observations on the effect of sewage treatment van Zijl, W. J. (1966). Studies on diarrhoeal diseases in seven processes on the ova and cysts of intestinal parasites. countries by the WHO Diarrhoeal Diseases Advisory Team. Sewage Works Journal, 14, 1274-1280. Bulletin of the World Health Organization, 35, 249-261. Yan, C. W., Ishak, F., Hee, G. L., Devaraj, J. M., Ismail, K., Vassilkova, Z. (1936). On the dehelminthization of purified Jalleh, R. P., Peng, T. L. and Jalil, T. M. A. (1978). The sewage by intensive methods. Meditsinskaia Parazitologiia problem of soil transmitted helminths in squatter areas i Parazitarnye Bolezni, 5, 671-674. around Kuala Lumpur. Medical Journal of Malaysia, 33, (1940). Viability of helminth eggs in pit latrines. 34-43. Meditsinskaia Parazitologiia i Parazitarnye Bolezni, 9, Yarulin, G. R. (1955). Contamination of the coastal zone of 231-237. the Caspian Sea with eggs of geohelminths. Meditsinskaia (1941). Evaluation of the contamination ofvegetables Parazitologiiu i Parazitarnye Bolezni, 24, 117-120. with eggs of helminths in sewage farms with different Zaman, V. and Visuvalingam, N. (1967). Action of aqueous methods of cultivation. Meditsinskaia Parazitologiia i iodine on ova of Ascaris lumbricoides and Ascaris suum. Parazitarnye Bolezni, 10, 217-225. [Correspondence.] Transactions of the Royal Society of (1950). Infestation of vegetables with helminth eggs Tropical Medicine and Hygiene, 61, 443-444. by irrigation with purified sewage water. Gigiena i Sanitaria, No. 6, 41-43. 24 Clonorchis and Clonorchiasis THE WORM Clonorchis. and the closely related instance, Jopling 1978). Praziquantel is under trial for Opisthorchis, follow a classic trematode life cycle from clonorchiasis therapy and shows promise. At present, vertebrate hosts through snails and fish and back to the no treatment is advised for those with asymptomatic vertebrate hosts. These worms are of special import- clonorchiasis. ance in the design of sanitation systems that involve the use of human or animal excreta in aquaculture. Occurrence Clonorchis sinensis occurs in China, Hong Kong, Description of Pathogen and Disease Korea, Taiwan, Japan, and Vietnam (figure 24-1). Opisthorchis viverrini occurs in Thailand and southern Clonorchis and Opistho7-chis worms are found Laos. O.felineus occurs in Poland, various parts of the mainly in East Europe and Eastern Asia and are not USSR (especially the Ukraine), and northern Turkey. well known to public health workers in Western Europe, North or South America, or Africa. Most of Infectious agents the literature on these pathogens is not in English, but Three closely related trematode species are con- an important English-language review was published sidered in this chapter: first C. sinensis, the Chinese by Komiya (1966). liverfluke; second 0. ciuerrini; and third O.felineus, the cat liver fluke. C. sinensis is also called 0. sinensis, it Identification being argued that it is not sufficiently different from 0. .oria infe n . f viverrini and 0. felineus to warrant a separate genus. Chonorchiasis (or opisthorchiasis) IS an infection of The three species are very similar in their biology but the bile ducts by trematodes of the genus Clonorchis (or ocu i fre nt art te world. ,., occur in different parts of the world. Opisthorchis). In light infections, symptoms are likely The adult worms are flat, transparent, flabby, to be absent or vague. Heavier infections result in hermaphroditic organisms that measure l l-20 by 3-5 diarrhea, abdominal discomfort, and some sple- m i nomegaly. Heavy parasite burdens may cause acute mlhmeters (figure 24-2). The eggs are relatively small, pain in the upper right quadrant, liver enlargement and measuring 23-35 by 10-20 micrometers. tenderness, edema, an increased erythrocyte count, raised sedimentation rate, and up to 40 percent Reservoirs eosinophilia. There may be bouts of recurrent gall A wide variety of fish-eating vertebrates provide the bladder colic. Carcinoma of the bile ducts is a lethal definitive hosts for these trematodes. For C. sinensis the complication (Sonakul and others 1978), and death main hosts are man and dogs, for 0. viverrini cats and can also ensue from secondary bacterial infection, man, and for 0. felineus cats. Transmission of 0. Clonorchiasis is a chronic disease, sometimes lasting viverrini and 0. felineus is often maintained in the for 30 years or longer (see, for instance, Attwood and absence of man, and this is also possible for C. sinensis. Chou 1978). Diagnosis is by examining feces microscopically for Transmission eggs. Treatment is by oral drug therapy but, although a large variety of drugs have been tried, they are either There can be up to 6,000 worms in the bile ducts, and not freely available, too toxic, or not effective (see, for each worm produces 2,000-4,000 eggs per day. The 401 402 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS * CLONORCHIS SINENSIS Figure 24-1. Known geographical distribution oJ Clonorchis sinensis. The infection may occur in areas as yet unrecorded number of eggs produced by C. sinensis varies with the When fish are eaten raw or undercooked by man or species of host and with the duration of the infection. other vertebrate host, the larvae hatch out in the The eggs, containing fully formed larvae (miracidia), duodenum and migrate up the bile ducts. Adult worms are passed out in the feces and for further development can live for 25-50 years. From each cyst ingested, one have to reach water and be ingested by particular adult worm may develop and is capable of producing species of freshwater snails. For C. sinensis, snail hosts eggs. include Bulinusfuchsianus in northern China, Alocima longicornis in southern China, and Parafossarulus and periods manchouricus in most endemic areas. For 0. viverrini, Prepatent incubation snail hosts include Bithynia funiculata, B. laevis, B. Worms reach maturity and start producing eggs 3-4 goniomphalus, and B. siamensis. For O.felineus, the host weeks after the ingestion of cysts. Symptoms may is usually B. leachii. develop slowly or not at all. Acute clonorchiasis with Asexual multiplication occurs in the snail, and many an incubation period of only 10 days has been reported free-swimming cercarial larvae are released 3-4 weeks from China (Zhipiao, Huilan and Weiji 1979). after ingestion. These live for only 1-2 days in water unless they can penetrate beneath the scales of almost Period of communicability any species of freshwater fish and form cysts (metacercariae) in the connective tissues. Over eighty As long as mature adult worms are present, eggs may species of freshwater fish have been incriminated as be passed in the feces. Adult worms can live for up to 50 hosts of C. sinensis, and a maximum of 3,000 years. Eggs can live for 1 month in water. metacercariae have been found in a single fish. 0. Metacercariae in fish can survive for the life of the fish felineus commonly encysts in carp. and for some weeks after its death. CLONORCHIS AND CLONORCHIASIS 403 Figure 24-2. An adult of Opisthorchis felineus under a light microscope. Scale bar = 1 millimeter. (Photo: Wellcome Museum of Medical Science) Resistance appropriate snail species (Faust and Khaw 1927). Infection with 0. felineus in Poland and the USSR is immunityh especially associated with eating recently salted fish. immunity. Clonorchiasis in Taiwan has increased in recent years (Chen and others 1980). Prevalences are up to 52 Epidemiology percent in school staff in some areas. Pigs are commonly infected, and up to 100 percent of some fish Infection is normally contracted from eating raw or species in some localities harbor Clonorchis metacer- undercooked fish. The metacercarial cysts are sticky, cariae. Ong and Lu (1979) studied clonorchiasis in a however, and can be transferred from knives, hands, or highly endemic area of Taiwan and found prevalences chopping boards to other foods or directly to the of 3 percent among primary-schoolchildren, 7 percent mouth. Infection is much more common in adults than of middle-school children, 8 percent of high-school children and is rare in young children. It is common for children, and 56 percent of government workers. adult males to have higher prevalences of clonorchiasis Prevalences were higher among males than females than adult females owing to different dietary customs. and higher among those 35-45 years old than among In South Korea, for instance, men eat raw fish at rice- others. wine drinking parties. A survey in South Korea during 1967-69 revealed a Transmission of C. sinensis is especially associated nationwide prevalence of clonorchiasis of 5 percent, with raising fish in excreta-enriched ponds, a practice with prevalences rising to 15 percent locally. Prevalence common in China and elsewhere in East Asia and one and intensity of infection were higher in males than that clearly creates ideal conditions for transmission, females and higher among those over 30 years old than provided that the ponds are colonized by the in younger persons (Seo and others 1969). 404 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Opisthorchiasis is extremely common in northern feces of animals or man in endemic areas. A few reports and northeastern Thailand. Prevalences range from 10 exist; for instance, Opisthorcliis eggs were isolated from to 90 percent, and about 4 million people are infected river water in the USSR (Goryachev 1947). (Harinasuta 1980). In the worst affected areas between Early experiments by Faust and Khaw (1927) 50 and 90 percent of carp are infected and harbor showed that Clonorchis eggs in an isotonic solution 20-50 metacercariae each. Laotian refugees in survived for up to 3 months at 2-4°C, 6 months at Thailand had an opisthorchiasis prevalence of 44 4-8°C, 1 month at 26°C. 3 weeks at 37°C, 4 days at percent, with a peak age-prevalence of 64 percent 45°C. 1 hour at 50°C, and a few minutes at 58°C. At among 30-34 year olds (Temcharoen and others 1979). 6-8°C survival times were 4-5 days in fresh night soil, 2 Other surveys of clonorchiasis or opisthorchiasis days in 5-day-old night soil, and 1 hour in 10-day-old include those from China (Weng and others 1960), night soil. Clonorchis eggs were rapidly killed by Japan (Yokogawa 1969), Malaysia (Rohde 1967), desiccation. In river water Oj.elineus eggs survived for South Korea (Choi and others 1973), Taiwan (Cross over 160 days at 0-5°C, and this suggests that they may 1969), Thailand (Viranuvatti and Stitnimankarn overwinter in the USSR (Drozdov 1962). 1972), and the USSR (Churina 1973; Pantyukhov Clonorchis metacercariae in fish persist throughout 1965). the life of the fish. Thereafter they survive for months if frozen, for several days if salted, for over 2 weeks if Control Measures dried, and for several days in soy sauce, vinegar, or wine (Faust and Kha v 1927; Wykoff 1959). They are killed There is no effective and safe drug for mass by thorough cooking. chemotherapy at present. Praziquantel may well fulfil 0. felineus metacercariae were killed rapidly at this role and is undergoing clinical trials. Personal 55-580C, but in fish of 1-2 kilograms weight they were protection is best achieved by not eating raw or killed by cooking for not less than I hour (Mitrokhin partially cooked fish. 1962). 0. felinieus metacercariae were still infective to Snail control using chemicals is difficult because of foxes after 7 days drying in fish, but not after 9 days the toxic effect that most molluscicides have on fish. (Mitrokhin 1960). Other Soviet workers have recom- Some workers have tried biological control using fish mended that carp should be soaked in brine for 2-3 and crayfish, but this requires further study (Nagano weeks and then dried for at least 3 weeks to kill 0. 1964). Clearing aquatic vegetation from fishponds may felineus metacercariae (Yaldygina and others 1970). reduce snail populations (Komiya 1966). Viable eggs in feces must be prevented from reaching Inactivation by Sewage Treatment bodies of freshwater in which the snail and fish intermediate hosts live. This would be relatively Processes straightforward except for two obstacles. First, in parts No information on Clonorchis or Opisthorchis eggs of thc world where clonorchiasis is endemic, especially during sewage treatment could be located. The nearest China and Taiwan, it is the practice to enrich fishponds parallel is probably that of schistosome eggs (chapter with human and other feces in order to improve 32). productivity. Second, there are several reservoir hosts apart from man, so that the control of human feces alone can only have a partial effect on transmission. Inactivation by Night Soil and Sludge The solution to the first problem is to treat excreta Treatment Processes prior to adding to fish ponds. There is no simple solution to the second problem. No specific data are available but Clonorchis eggs Education is needed to make the population aware are rapidly killed by storage in night soil (Faust and of the cause of clonorchiasis and, in endemic areas, to Khaw 1927; Komiya 1966). Clonorchis eggs should be try to change the habit of eating raw or insufficiently destroyed after storage for 5 days at 5°C or for 2 days at cooked fish. 25°C. Occurrence and Survival in the Literature Cited Environment Attwood, H. D. and Chou, S. T. (1978). The longevity of The eggs, miracidia and cercariae of Clonorchis and Clonorchis sinensis. Pathology, 10, 153-156. Opisthorchis may be found in waters contaminated by Chen, E. R., Yen, C. M.. Hsieh, H. C., Wang, J. S. and Kuo. M. CLONORCHIS AND CLONORCHIASIS 405 (1980). Epidemiological surveys of clonorchiasis in Pantyukhov, A. M. (1965). Degree of Opisthorchis metacer- Taiwan. In Abstracts of the 10th lnternational Congress on cariae infection of fish in the river Irtish in relation to Tropical Medicine and Malaria, p. 193. Manila, sewage regulation. In: Materialy Nauclioi KonJerentsii Philippines. Vsesoyuznogo Obshelestva Gelmintologou, 1965, Part III, Choi, D. W., Joo, C. Y., Park, S. D. and Kim, J. W. (1973). pp. 192-196. Moscow: The All-Union Society of Changing pattern of Clonorchis sinensis infection among Helminthologists. school children in the Gumho Basin, Kyunpook Province, Rohde, K. (1967). The distribution of Opisthorchis and Korea. Korean Journal of Parasitology, 11, 26-31. Paragonimus in Malaya and possible sources of human Churina, N. V. (1973). Distribution and epidemiology of infection with these parasites. Z-'r.. .C far opisthorchiasis in the central Urals. Meditsinskaia Tropenmedizin und Parasitologie, 18, 152-161. Para7itologiia i Parazitarnve Bolezni, 42, 149-153. Seo, B. S., Rim, H. J., Loh, I. K., Lee, S. H., Cho, S. Y., Park, S. Cross, J. H. (1969). Clonorchiasis in Taiwan: a review. In C., Bae, J. W., Kim, J. H., Lee, J. S., Koo, B. Y. and Kim, K. Proceedings of the Fourth Southeast Asian Seminar o07 S. (1969). Study on the status of helminthic infections in Parasitology and Tropical Medicine, Schistosomiasis and Koreans. Korean Journal of Parasitology. 7, 53-70. other Snail-transmitted Helminthiasis, Manila, Feb. 24-27, Sonakul, D., Koompirochana, C.. Chinda, K. and 1969, pp. 231-242. Manila, Philippines. Stitnimakarn, T. (1978). Hepatic carcinoma with opisthor- Drozdov, V. N. (1962). Survival rate of Opisthorchisfelineus chiasis. Southeast Asian Journal of Tropical Medicine and (Rivolta, 1884) eggs under different conditions of external Public Health, 9, 215-219. environment. Meditsinskaia Parazitologiia i Parazitarnuve Temeharoen, P., Viboolyavatana, J., Tongkoom, B., Bolezni, 31, 323-326. Sumethanurugkul, P., Keittivuti, B. and Wanaratana, L. Faust, E. C. and Khaw, 0. K. (1927). Studies on Clonorchis (1979). A survey ofintestinal parasitic infectionsin Laotian sinensis (Cobbold). American Journal of Hygiene refugees at Ubon Province, northeastern Thailand, with Monographic Series No. 8. special reference to schistosomiasis. Sourtleast 4 ian Goryachev, P. P. (1947). Investigation of helminth eggs in the Journal of Tropical Medicine and Public Health, 10, waters of the rivers Irtish and Om. Meditsinskaia 552-555. Parazitologiia i Parazitarnve Bole7ni, 16, 75-78. Viranuvatti, V. and Stitnimankarn, T. (1972). Liver fluke Harinasuta, C. (1980). Liver fluke infection in Thailand. In infection and infestation in Southeast Asia. Progress in Abstracts of the 10th International Congress on Tropical Liver Diseases, 4, 537-547. Medicine and Malaria. p. 186. Manila, Philippines. Weng, H. C., Chung, H. L., Ho, L. Y. and Hou, T. C. (1960). Jopling. W. H. (1978). Treatment of clonorchiasis. Studies on Clonorchis sincnsis in the past ten years. [Correspondence] British Medical Journal, 1, 1346. Chinese Medical Journial, 80, 441-445. Komiya, Y. (1966). Clonorchis and clonorchiasis. Advances in Wykoff, D. E. (1959). A study of the host-parasite relations in Parasitology, 4, 53-106. Clonorchis sinensis infection, with special reference to the Mitrokhin, V. U. (1960). The resistance of Opisthorchis rabbit as an experimental host. Dissertation Abstracts, 19, metacercariae in the drying of fish. Nauchnaya 3285-3286. Konferentsiya Posv)ashchennava 40-Letiyu Moskovskoi Yaldygina, Z. S., Klimshin, A. A., Koval'chuk, E. S. and Veterinarnoi Akademii, 91-93. Smirnova. K. S. (1970). The effect of industrial drying of (1962). Resistance of Opisthorchis felineus metacer- fish on Opisthorchis metacercariae. Meditsinskaia cariae in homecooked stuffed ides. Meditsinskaia Parazitologiia i Parazitarnye Bolezni, 39, 462-467. Parazitologiia i Parazitarnve Bolezni, 31, 364-365. Yokogawa, M. (1969). Clonorchiasis in Japan. In Nagano, K. (1964). The preventive measure of Clonorclhis Proceedings of the Fourth Southeast Asian Seminar on infection. Progress of Medical Parasitology in Japan, 1, Parasitology and Tropical Medicine, Schistosomiasis and 723-738. other Snail-transmitted Helminithiasis, Manila, Feb. 24-27, Ong, S.-J. and Lu, S.-C. (1979). Protozoan and helminthic 1969, pp. 209-218. Manila, Philippines. infections among the government workers and students of Zhipiao, X., Huilan, Z. and Weiji, C. (1979). Acute Miao-Li District in Miao-Li County: a highly endemic clonorchiasis: report of two cases. Chinese Medical area of clonorchiasis in Taiwan. Chinese Journal oJ Journal, 92, 423-426. Microbiology, 12, 13-19. 25 Diphyllobothrium and Diphyllobothriasis DIPHYLLOBOTHRIASIS has a restricted geographical eaten, prevalence may be 10-30 percent locally, and distribution and is not a major public health problem generally increases with age. in most areas where it does occur. It is caused by a cestode (tapeworm) but has a life cycle involving two Infectious agent aquatic hosts that is more reminiscent of the life cycles Diphyllobothrium latum, a cestode, is the broad fish of trematodes. tapeworm of man. The hermaphroditic adult measures 3-10 meters in length and may have 4,000 segments, with a small scolex, which has no hooks, embedded in Description of Pathogen and Disease the mucosa of the ileum (figure 25-2). Immediately behind the scolex, and several times its length, is an There ls a very extensive Russian literature on unsegmented neck region. The neck is followed by diphyllobotliriasis. Only abrief summary of the disease newly formed proglottids that become mature. The is given in this chapter. The disease has been proglottids measure 2-7 by 10-12 millimeters and comprehensively reviewed by von Bonsdorff (1977). contino male and fmlrpouive ans contain both male and female reproductive organs. Eggs are evacuated periodically through a uterine pore Identification on each functional proglottid. The eggs measure 55-80 Diphyllobothriasis is an infection of the small by 40-60 micrometers. intestine by the broad fish tapeworm Diphyllobothrium Reservoir latum. There are often no clinical symptoms associated erv with infection, apart from eosinophilia. However, in a Man is the most important reservoir. Dogs, bears, proportion of cases there is abdominal pain, loss of and other fish-eating mammals may also become weight, anorexia, and vomiting. Megaloblastic anemia infected, but the proportion of viable eggs in dog feces occurs in 20 percent of cases in Finland. (1 percent) is much less than in human feces (79 Diagnosis is by finding eggs, or occasionally percent) (Essex and Magath 1931). segments, in the feces. Drug therapy is with Related tapeworms of nonhuman mammals, that niclosamide, or any other agent effective against Taenia have intermediate stages in fish, also infect man (see chapter 34). occasionally. Examples include a tapeworm of the fur seal, Diphyllobothrium pacificum, in Peru; a tapeworm of the gull, D. dentricum, in Siberia; and a tapeworm of Occurrence the whale, Diplogonoporus grandis, in Japan. Man may Diphyllobothriasis occurs in temperate countries also act as the intermediate host for tapeworms of the with many lakes: in Europe, mainly in Finland, genus Spirometra. Adult Spirometra live in the intestine the USSR, and Poland with sporadic cases in of carnivores (but not man), and the intermediate hosts France, Ireland, Italy, Switzerland, and the Federal are, first, a cyclops in water and, second, amphibia, Republic of Germany; in Asia, in Japan and Siberia; in reptiles, or mammals, including man. the Americas, in the Great Lakes region of Canada and the USA, among Eskimos, and in Chile and Argentina Transmission (figure 25-1). It has also been reported from lakeside Each worm produces up to 1 million unsegmented regions in Africa. Where raw or partly cooked fish is eggs daily, that pass out in the feces. If an egg reaches 407 408 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS E DIPHYLLOBOTHRIUM LATUM Figure 25-1. Knowtn geographical distribution of Diphyllobothrium latum. The infection may occur in areas as yet unrecorded Figure 25-2. A lenigth oj D. latum j'I lafter- treatnienit. (Photo: Wellcome Museum of Medical Science) DIPHYLLOBOTHRIUM AND DIPHYLLOBOTHRIASIS 409 fresh water it develops-in 12 days to many weeks, Esox lucius, 11 percent; Lota Iota, 10 percent; C. depending on the temperature into a ciliated larva lavaratus, 4 percent; and Percafluviatilis, 4 percent. No (coracidium). Diphyllobothrium were found at autopsy of sables, The coracidium escapes into the water and swims gluttons, polar foxes, and wolves. One of twenty-one around, surviving for 1-2 days. For further develop- dogs examined was infected. ment the coracidium must be ingested by a minute Other accounts of diphyllobothriasis include those freshwater copepod (of the genera Diaptomus or from Canada (Turgeon 1974), Finland (Wikstrom Cyclops). Inside the copepod there is further develop- 1972), Japan (Tomita and others 1979; Uhari and ment of the larva, which may take 2-3 weeks. others 1975), Peru (Baer and others 1967), and the Freshwater fish (pike, perch, salmon, burbot) act as USSR (Artamoshin 1968, 1972). second intermediate hosts. The freshwater fish ingest the copepod, and the larva present in the infected copepod works its way through the fish tissue to the Control Measures muscles, where it grows into a plerocercoid larva over about 4 weeks. When an infected fish is eaten raw by Mass chemotherapy with niclosamide, combined man, the larva is released in the small intestine, grows with health education measures, has markedly reduced into a mature tapeworm in 3-6 weeks, and can live for prevalence locally. Thorough cooking, freezing, or up to 25 years. salting of fish will kill larvae. Preventing untreated One larva ingested in fish may develop into the human feces from reaching freshwater will greatly hermaphrodite worm, which is sufficient to maintain reduce transmission. the infection. Successful integrated control campaigns in the USSR have been reported from the Danube Delta (Smolinschi and others 1970) and the Astrakhan River Prepatent and incubation periods (pti n tes16) (Epstein and others 1967). Worms reach maturity about 5-6 weeks after infective larvae in fish are ingested. Symptoms develop slowly or not at all. Occurrence and Survival in the Environment Period of communicability Diphyllobothrium eggs may be found in fecally Eggs are passed in the feces as long as mature worms contaminated waters in endemic areas. They have been are present. Adult worms may live up to 25 years isolated from river water and sediment (Goryachev (Leiper 1936). Larvae in fish areinfective to man for the 1947; Usacheva 1951) and from sewage (Vassilkova life of the fish and for some time thereafter. 1936, 1941) in the USSR. Diphyllobothrium eggs in freshwater at 15-25°C Resistance develop within 11-15 days. The lower the temperature, the slower the development. Eggs are killed after 2 days There is no evidence of innate or acquired resistance at - 10°C or 30 days at 2-6°C (Essex and Magath to infection. 1931; Fedorov 1956). The minimum concentration of oxygen in water needed for eggs to hatch into coracidia Epidemiology is 1.4 milligrams per liter at 24°C (Romanov 1972). At lower oxygen levels eggs can survive for many months Raw or smoked fish is the main source of infection. but will not develop unless transferred to a more Pike roe (caviar) and pike spawn are also major oxygenated environment (Fedorov 1956). Eggs in sources of infection in the USSR (Karaseva and water at depths of over about 20 meters do not hatch Egorova 1965). The age and sex distribution of (Razumova and Artamoshin 1969). Eggs are rapidly infection is related to dietary habits. Diphyl- killed by desiccation (Essex and Magath 1931). lobothriasis is mainly an infection of adults. Eggs in feces on the ground, or on ice in winter, die Chefranova (1964) studied the epidemiology of within 3 days (Chefranova 1964). diphyllobothriasis in the Evenk National District The encysted plerocercoid larvae in fish muscle and (USSR). The prevalence rate of diphyllobothriasis was viscera live for the life of the fish and for some time after. 69 percent. The infection rates of fish harboring larvae The larvae survive in dead fish in river water for up to of Diphyllobothrium were: Coregonus peles, 82 percent; 10 days (Pronin 1967). The larvae can be killed by 410 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS freezing, salting, or cooking, but each of these Epstein, S. I., Sutyrina, L. G.. Shaposhnikova, M. I., operations must be very thorough to be effective. Zhilinskaya, I. N. and Tishechkina. V. A. (1967). Studies on infected pike (Titova 1955) showed that Organization of control of diphyllobothriasis among effective freezing regimes were: at - 6°C, 7 days with a water transport workers. Meditsinskaia Parazitologiia i 9-kilogram fish, 6 days with a 2-kilogram fish, or 3 days Parazitarnye Bolezni, 36, 151-154. with a 0.7-kilogramn fish. At -18°C, larvae were Essex, H. E. and Magath, T. B. (1931). A comparison of the destroyed after 402-kilogram fish.t ad 1C lvays we viability of ova of the broad fish tapeworm, destroyed after 4 days in 2-kilogram fish and 2 days in Diphyllobothrium latum, from man and dogs: its bearing on 0.5-kilogram fish. Salting and cooking also need to be the spread of infestation with the parasite. American carried out for longer in large fish than in small fish to Journal of Hygiene, 14, 698-704. destroy larvae. Fedorov, V. G. (1956). Studies of the influence of oxygen, low temperatures and chloramine on the development and vitality of Diphyllobothrium latum L. (Cestoidea). Inactivation by Sewage Treatment Zoologicheski Zhurnal, 35, 652-656. Processes Goryachev, P. P. (1947). Investigation of helminth eggs in the waters of the rivers Irtish and Om. Meditsinskaia Little is known about Diphyllobothrium eggs in Parazitologiia i Parazitarnye Bolezni, 16, 75-78. sewage treatment plants. Sedimentation will remove a Karaseva, A. N. and Egorova. P. S. (1965). Treatment of pike high proportion to the sludge layer and will be more spawn to disinfect it of Diphyllobothrium latum plerocer- high proportion to the sludge layer and willl be more cod. Meisn. i . .,~ P iBlzi effective if a coagulant is used (Doschl 1972). In the 34, 148 151. absence of specific data, it may be assumed that Leiper, R. T. (1936). Some experiments and observations on Diphyllobothrium eggs react to sewage treatment in the the longevity of D r1 i ..,,.- infections. Journal of same manner as Ascaris eggs (chapter 23). Helminthology. 14, 127-130. Pronin, N. M. (1967). The effect of some physical and chemical factors on the survival of encysted plerocercoids of Inactivation by Night Soil and Sludge Diphyllobothrium sp. Meditsinskaia I., .i. ; Treatment Processes Parazitarnye Bolezni, 36, 154-158. Razumova, E. P. and Artamoshin, A. S. (1969). Development Any process effective against Ascaris eggs (chapter of Diphyllobothrium latum eggs in the Volgograd water- 23wilbehitDiphyllobothrium reservoir at different depths. Meditsinskaia Parazitologiia i 23) willl be highly effective against ID.':,." i. olznit38 8487 Pa' " ,._l!,. , ', Boleznii. 38, 84-87. eggs. Romanov, 1. V. (1972). Experimental determination of the minimum oxygen concentration in water necessary for the normal development of Diphyllobothrium latum eggs. Literature Cited Meditsinskaia Parazitologiia i Parazitarnye Bolezni, 41, 612-613. Artamoshin, A. S. (1968). The role of ecological conditions in Smolinschi, M. I., Dranga, A. C., Marinov, R. P. and Mihai, the epidemiology of diphyllobothriasis in the area of the M. V. (1970). The fight against Diphyllobothrium in the Volgograd water reservoir. Meditsinskaia Parazitologiia i Danube Delta. Journal oJ Parasitology, 56, 471-472. Parazitarnye Bolezni, 37, 160-168. Titova, S. D. (1955). Survival of plerocercoids of (1972). Some information on contamination of the Diphyllobothrium latum in the presence of low tempera- Volgograd water reservoir with eggs of Diphyllobothrium tures and salt. Meditsinskaia Parazitologiia i Parazitarnye latum. Meditsinskaia Parazitologiia i Parazitarnye Bolezni, Bolezni, 24, 255-256. 41, 87-90. Tomita, S. I., Tongu, Y., Sakumoto, D., Suguri, S., Itano, K., Baer, J. G., Miranda, H., Fernandez, W. and Medina, J. Inatomi, S. and Kawaguchi, K. (1979). Epidermiological (1967). Human diphvllobothriasis in Peru. Z. a,, I-1 fur survey for Diphyllobothrium latum in Okayama Prefecture. Parasitenkunde, 28, 277-289. Japanese Journal of Parasitology, 28, 317-321. Chefranova, Y. A. (1964). On the epidemiology of Turgeon, E. W. T. (1974). Diphyllobothrium latum (fish diphyllobothriasis in the regions of the extreme North. In tapeworm) in the Sioux Lookout zone. [Correspondence.] Problems in Medical Parasitology and Prophylaxis of Canadian Medical Association Journal, 111, 507, 507. Infections, ed. Moshkovski, S. D., pp. 495-500. Moscow: Uhari, M., Vierimaa, E., Siivola, J., Tarkka, M., Ervasti, J. Martinovski Institute of Medical Parasitology and and Heinonen, M. (1975). Fish tapeworm infections in Tropical Medicine. Kuusamo county. Duodecim, 91, 671-674. Doschl, R. (1972). Studies on the sedimentation of eggs of the Usacheva, A. M. (1951). Survival of helminth eggs in water fish tapeworm Diphyllobothrium latum using the and in river sediment. Gigiena i Sanit aria, Part 2, No. 12, flocculation agent aluminium sulphate. Inaugural disser- 12-17. tation. Munich: Ludwig-Maximilians-Universitat. Vassilkova, Z. (1936). On the dehelminthization of purified DIPHYLLOBOTHRIUM AND DIPHYLLOBOTHRIASIS 411 sewage waters by intensive methods. Meditsinskaia vonBonsdorff,B. (1977).DiphyllobothriasisinMan.London: Parazitologiia i Parazitarnye Bolezni, 5, 671-674. Academic Press. (1941). Evaluation of the contamination of vegetables Wikstrom, M. (1972). The incidence of the broad fish with eggs of helminths in sewage farms with different tapeworm in the human population in Finland. methods of cultivation. Meditsinskaia Parazitologiia i Commentationes Biologicae Societas Scientarum Sennica, Parazitarnye Bolezni, 10, 217-225. Helsinki, no. 48, 8 pp. 26 Enterobius and Enterobiasis FIVE INTESTINAL NEMATODE INFECTIONS- over 1,000 million cases in the world. It is likely that ancylostomiasis (chapter 22), ascariasis (chapter 23), virtually every person living in a temperate country is strongyloidiasis (chapter 33), trichuriasis (chapter 35), infected some time during childhood. and enterobiasis (this chapter)-are described in this book. Enterobiasis is atypical within this group Infectious agent because it is transmissable directly from one person to another without the need for a period of development E. vermicularis, a nematode, is the pinworm, in soil elsewhere, and because the Enterobius eggs are threadworm, or seatworm of man. It is also known as not normally excreted in the feces. Although Oxyuris vermicularis. The female worm measures 8-13 enterobiasis is extremely common the commonest in millimeters and contains about 10,000 eggs; and the fact of all infections discussed in this book-it is of very male measures 2-5 millimeters (figure 26-1). The eggs minor public health importance. measure 50-60 micrometers by 20-30 micrometers. Reservoir Description of Pathogen and Disease E. vermicularis is exclusively a parasite of man. The literature on enterobiasis is limited because it is an infection that does not commonly cause serious Transmission disease. The female worm migrates down the intestine and colon and emerges from the anus, usually at night. Eggs Identificalion are normally laid on the perianal skin and are seldom found in the feces. Most female worms die after egg Enterobiasis is an infection of the large intestine and laying. The eggs develop to the infective stage in 4-7 appendix by the nematode Enterobius vermicularis. hours at 35°C and 48 hours at 25°C. Under cool, moist The heads of the worms are attached to the mucosa of conditions infective eggs remain alive for up to 8 weeks. the intestinal wall. There are usually only minor When infective eggs are ingested, the larvae hatch in the symptoms or none at all. Pruritus ani, causing small intestine and the adults are found in the large disturbed sleep, is common, and there is sometimes intestine, cecum, and appendix. Autoinfection often mild catarrhal inflammation with nausea and diarrhea. occurs by transmitting eggs from the anus to the mouth Symptoms of appendicitis are a very rare occurrence. on contaminated fingers or by eggs hatching on the Migration of worms to the female genitalia frequently anal mucosa and the larvae migrating up into the occurs. Diagnosis is by finding eggs on the perianal bowel and there developing into an adult worm. Each skin by means of sticky tape. Enterobiasis is treated by egg ingested may develop into a male or female worm, oral drug therapy with mebendazole, pyrantel so at least two are necessary for transmission. pamoate, or piperazine citrate. Prepatent and incubation periods Occurrence Adult female worms begin to pass eggs 40-50 days Enterobiasis occurs worldwide and is extremely after ingestion of eggs. The infections are often common, particularly in children. There are probably asymptomatic. 413 414 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Figure 26-1. Adult pinworms, Enterobius vermicularis. Each worm is 5-10 millimeters long. (Photo: Wellcome Museum of Medical Science) Period of communicability chapters 22 to 35. Eggs are found in the feces of 5 The duls lve or bou 50 ays bu beaus of percent or less of infected individuals. Eggs are athinecautso live feror aout5 days,nicbulty becausealof normally laid on the perianal skin by female worms autfctonghe p that have emerged from the anus at night. It follows much longer. ~~~~~~~~~that stool surveys greatly underestimate the prevalence of enterobiasis. For an accurate survey it is necessary to Resistance adopt the sticky tape method to pick eggs off the Susceptibility is general, and there is no evidence of perianal skin and examine them under a microscope. resistance due to past infection. Eor best results, the sticky tape should be applied very soon after waking and before bathing or passing stool. Epidemiology ~~~~~~~~Even then a single survey will detect only 50 percent of Epidemiology ~~~~~~~~infections; three tests will detect 90 percent, and five Fnterobiasis is a group infection, most common in tests 99 percent (Wolfe 1978). Owing to these children. Its transmission, by the anal-oral route, difficulties, practically no reliable community-wide depends very much on personal hygiene. prevalence data on enterobiasis exist, and most figures Contaminated fingers, fingernails, bed linen, table tops, quoted are gross underestimates. This is not a matter doorknobs, and so forth can serve as sources of for concern. Enterobiasis is an infection of negligible infection. In some cases airborne eggs, dislodged from public health importance, and there is generally no contaminated areas, are inhaled and swallowed and reason for needing accurate prevalence data. cause infection. Overcrowding and poor housing A survey of enterobiasis in orphanages in Taipei encourage infection. Infection is most common in large (Taiwan) showed an overall prevalence of 74 percent, families and institutions such as boarding schools, with higher infection rates in more crowded or- hospitals, prisons, and orphanages. phanages (Chung, Chang and Horng 1978). Children's Enterobiasis is not an excreted infection in the same bodies were heavily contaminated with Enterobius sense as the other worm infections described in eggs, and 12 percent had eggs on their ears. Bedpans, ENTEROBI US AND ENTEROBIASIS 415 linen, toilets, dust, stair rails, bedposts, closets, desks, of the family, especially women. Sanitary measures and and toys were contaminated by Enterobius eggs in mass treatment with specific anthelminthics of all the decreasing order of frequency of egg detection (see also children and personnel of nineteen kindergartens in Chiu and others 1975). Seo and others (1969) found Baku resulted in a marked and rapid reduction in the high rates (up to 80 percent) of enterobiasis among cases of enterobiasis, which dropped from 35-68 rural school children in South Korea. Other fairly percent to 4-17 percent a year later. At present, new recent surveys of enterobiasis in developing countries pupils and personnel are admitted only after include those from Brazil (Dias 1967), Chile (Cuevas undergoing prophylactic treatment. Studies on en- and others 1969), India (Sengbusch 1970), Mexico terobiasis in the USSR are also reported by Epifantsev (Garrocho Sandoval and Rodriguez Medina 1968; and Petrov (1972) and Zhuravlev and Parfenova Vazquez Compean and Garrocho Sandoval 1972), the (1974). Philippines (Sengbusch 1963; Sengbusch and Sengbusch 1971), and Singapore (Kan, Siak and Singh Control Measures 1971). Enterobiasis is more common in temperate than in Drugs such as piperazine, pyrantel pamoate, and tropical climates because transmission is encouraged mebendazole can be used for mass chemotherapy. by wearing many clothes and by infrequent bathing. Reduction of overcrowding in living accom- These practices maintain the perianal region in a cool, modation and adequate facilities for hand washing and dark, and moist state that is ideal for the survival of personal cleanliness help in the prevention of the Enterobius eggs on the perianal skin. Entroiu egg on th peinlsi. infection. Educational effort should be directed to Enterobiasis is the most common worm infection in infection. ationae the USA and is found throughout the country and stress personal hygiene. among all socioeconomic groups (Warren 1974). It is less common among black than white people for Occurrence and Survival in the reasons that are not known. Prevalence is greatest Environment among the 5-9 age group and is especially high in institutions. It was estimated that 42 million US Enterobius eggs are not usually passed in the feces citizens were infected in 1972 (Warren 1974). but are found in bedclothes and house dust. Eggs have In the course of 3 years (1975-78), systematic been found in sewage in the German Democratic surveys were carried out in Azerbajian (USSR) on Republic (Kalbe 1956), India (Lakshminarayana and enterobiasis among the urban and rural populations Abdulappa 1969), and the USSR (Vassilkova 1936); in (Chobanov and Salekhov 1979). A total of 9,914 river water contaminated by sewage in the USSR persons were examined, using adhesive cellophane (Bukh 1945; Goryachev 1947; Usacheva 1951); in tap swabs. The prevalence of enterobiasis in towns and water in the USSR (Bukh 1945); and on crops irrigated villages was similar (39 percent and 38 percent, with sewage in the USSR (Biziulevicius 1954; respectively), and there was no difference in the Khaustov 1935; Romanenko 1971). These eggs infection rates that could be attributed to the level of probably came from egg-filled female worms, which are sanitation and personal hygiene. The lowest infection often passed in the feces. rate was found in children of preschool age brought up Enterobius eggs are not robust and survive for at home (9 percent), whereas the highest was in considerably shorter periods than Ascaris eggs children attending kindergartens, especially in the 4-7 (chapter 23). Eggs can survive for up to 8 weeks if kept age group (57-60 percent). The incidence among cool and moist, but they are killed in a few days by adults was considerably lower (6-11 percent). The high desiccation. Mature eggs can remain viable for 2-3 prevalence of enterobiasis in schools was mainly due to days at 22°C and a relative humidity of 34-44 percent the introduction of the infection by children previously (Hulinska 1974). infected in kindergartens, for Enterobius eggs were found in up to 60 percent of this group, in comparison with 12 percent in schoolchildren brought up at home. Inactivation by Sewage Treatment A survey of 889 households showed that in childless Processes families only 4 percent were infected, whereas in families with children the infection rate increased in Little information is available on Enterobius eggs proportion to their number, reaching 70 percent in during sewage treatment. It may be assumed that their families with six children and involving adult members removal characteristics closely resemble those of 416 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Ascaris eggs (chapter 23). Enterobius eggs are absent Hulinska, D. (1974). Morphogenesis and viability of larvae in from the effluent of well-designed waste stabilization the eggs of Enterobius vermicularis. Folia Parasitologica. pond systems (Lakshminarayana and Abdulappa 21, 225-232. 1969). Kalbe. I. (1956). Investigations of parasites in sewage in several towns in East Germany. Zeitschlriftjfir die Gesamrte Hygiene und ihire Grenzgebiete, 2, 334-343. Inactivation by Night Soil and Sludge Kan, S. P. Siak, C. L. and Singh. M. (1971). Prevalence of Treatment Processes enterobiasis in children admitted to a hospital in Singapore Annlals of Tropical Medicine and Parasitology, Nothing is known about Enterobius eggs during night 65, 81-83. Nothing slknown treaboutm Enterobis eggs during nit Khaustov. J. M. (1935). Vegetables as a factor in transmission soll or sludge treatment. Enqterobiufs eggs are more of Trichocephialus (Triclutiris) trichiaris. Trudy Lenin- rapidly killed by hostile environmental factors gradskogo Instituta Epidemiologii i Bakteriologii imeni (especially heat and desiccation) than are Ascaris eggs, Pastera, 2, 148-152. and they will be eliminated from night soil and sludge Lakshminarayana, J. S. S. and Abdulappa. M. K. (1969). The long before Ascaris eggs. effect of sewage stabilization ponds on helminths. In Low Cost Waste Treatmiienit, ed. Sastry, C. A., pp. 290-299. Nagpur, India: Central Public Health Engineering Literature Cited Research Institute. Romanenko. IN. A. (1971). Sanitary-helminthological eva- Biziulevicius. S. K. (1954). Role of vegetables and berries in luation of new methods of irrigation with sewage. the epidemiology of helminthiasis in the population of Meditsin.skaia Parazitologiia i Parazitarn-ye Bolezni. 40, Lithuania. Meditsinskaia Parazitologiia i Parazitaornye 361-362. Bolezni, 23, 124-126 Sengbusch, H. G. (1963). Enterobiasis in school children in Bukh, F. L. (1945). The data of helminth egg inspection of the the vicinity of Iloilo City, Republic of the Philippines. sources of water supply of Ufa. Meditsinskaia Journal ofjthe Plilippine Medical Association. 39, 802-812. Parazitologiia i Para-zitarnve Bolezni. 14, 66-67. (1970). Studies on enterobiasis. 3. The incidence of Chiu, J. K.. Huang, R. J., Wang, Y. T. and Su, C. S. (1975). pinworm infection in a Mysore school. Indian Journal of Prevalence of enterobiasis among children in Taipei Citv. Paediatrics, 37, 229-238. Taiwan, with an evaluation of pyrantel pamoate in Sengbusch, H. G. and Sengbusch, C. H. (1971). Studies on treatment. Journal of the Formosan Medical Association. enterobiasis. II. The incidence of pinworm infection in a 74, 728-733. secondary school in Iloilo City. R. P. Journlal ofl the Chobanov, R. E. and Salekhov A. A. (1979). Prevalence of Philippine Medical Association, 47, 455-462. enterobiasis among the urban and rural population of the Seo, B. S., Rim, H. J., Loh, I. K., Lee. S. H., Cho, S. Y. Park. S. Azerbaijan SSR. Meditsinskaia Parazitologiia i C., Bae, J. W., Kim, J. H., Lee, J. S., Koo, B. Y. and Kim. K. Parazitarnye Bolezni, 5, 79-83. S. (1969). Study on the status of helminthic infections in Chung. W. C.. Chang. K. C. and Horng. S. H. (1978). Koreans. Korean Journial oJ Parasitology, 7, 53-70. Epidemiology of Enterobius cermiclularis infection among Usacheva, A. M. (1951). Survival of he]minth eggs in wvater orphans in orphanages in Taipei City. Chinese Jou7nal of and in river sediment. Gigiena i Sanitaria, No. 12, 1217. Microbiology, 11, 30-36. Vassilkova, Z. (1936). On the dehelminthization of purified Cuevas, R., Schenone, H., Silva, R., Galdames, M., Inzunza. sewage waters by intensive methods. Meditsinskaia E. and Romero, E. (1969). Prevalence of Enterobius Parazitologiia i Para-zitarnve Bolezni, 5, 671-674. rerniicularis infection in a boarding school. Boletin Chileno Vazquez Compean, R. F. and Garrocho Sandoval, C. (1972). de Parasitologia, 24, 121-123. Childhood enterobiasis in the Mexican plateau. Revista de Dias, J. C. P. (1967). Enterobiasis among the juvenile Investigacibn en Salud Publica, 31, 209-214. population in western Minas Gerais. Hospital, 72, Warren, K. S. (1974). Helminthic diseases endemic in the 1611-1621. United States. American Journal of Tropical Medicine and Epifantsev, G. D. and Petrov, V. I. (1972). Problem of HIygiene, 23, 723-730. enterobiasis control among the population. Meditsinskaia Wolfe, M. S. (1978). Oxyuris. Trichostrongylus and Trichluris. F i,,. i., ;,. i Para-zitarnye Bolezni, 41, 745-746. Cliniics in Gastroenterology, 7. 201-217. Garrocho Sandoval, C. and Rodriguez Medina, J. M. (1968). Zhuravlev, S. E. and Parfenova, E. S. (1974). Intestinal Enterobiasis among students of Mexquitic, San Luis. infections. Contamination of hands with Escherichia coli Potosi. Salud P(iblica de Mexico, 10, 215-217. and the micro flora condition of the large intestine in Goryachev, P. P. (1947). Investigation of helminth eggs in the children affected and unaffected with Oxyaris vermicularis. waters of the river Irtish and Om. Meditsinkaia Meditsiniskaia Pora7itologiia i Para-zitarnye Bolezni. 43, Parazitologiia i Parazitarnlye Bolezni. 16, 75-78. 482-485. 27 Fasciola and Fascioliasis FASCIOLIASIS is an infection of sheep and cattle. Occurrence Human infection is not common, and transmission Fascioliasis (or liver rot) is a disease of sheep and from man to man, rather than from animal to man, is cattle throughout the world. Human infection is not probably very rare. Fascioliasis transmission is not an t common and has been mainly reported from Central affected, therefore, by excreta disposal practices, and it and South America, Cuba, southern France, western is included in this book for completeness only. England, Wales, and North America. It is to be expected that sporadic human infection will occur Description of Pathogen and Disease wherever fascioliasis is endemic in the local sheep flocks. The literature on fascioliasis is chiefly veterinary, and little is known of the epidemiology of human Infectious agent infections. Fasciola hepatica, a trematode, is also known as the Identification liver fluke. The adult is a moderately fleshy, flat, hermaphroditic fluke measuring 20-30 millimeters in Fasioliasis is an inlfection of the bile ducts by the length by 13 millimeters in breadth (figure 27-1). The trematode Fasciola hepatica that results in inflam- eggs are large and ovoid, measuring 130-150 mation and fibrosis. In heavy infections small abscesses micrometers by 60-85 micrometers. may be produced in the liver parenchyma. There is an The related fluke, F. gigantica, measuring 25-75 early acute phase, when the larvae migrate through the millimeters by 12 millimeters, is a common parasite of liver, and a late chronic phase caused by the adult flukes cattle, camels, and other herbivores in Africa, Asia, and in the bile ducts. some Pacific islands and has been reported from man Symptoms recorded from human cases in the acute in Africa, Iran, and Hawaii. phase include dyspepsia, nausea and vomiting, abdominal pain, and irregular high fever. Allergic symptoms can also occur. Anemia occurs in a Reservoirs proportion of cases, as does leucocytosis and The main reservoirs of Fasciola hepatica are sheep eosinophilia. In the chronic phase there is often painful and cattle. Infections of rabbits, horses' donkeys, liver enlargement, and occasionally an obstructive camels, pigs, and deer are also reported. Human jaundice develops. infection is infrequent. Diagnosis is by recovery of eggs from the feces or from bile duct aspirate. In about 30 percent of cases, Transmission however, eggs cannot be found in either feces or bile. Fever, liver enlargement, and high eosinophilia are The eggs are laid in the proximal biliary tract of the very suggestive of fascioliasis, especially if there is a host and are evacuated in the feces. They mature in concomitant history of eating homegrown watercress. water or in moist conditions within 9-15 days at an Treatment is by oral drug therapy with bithionol or by optimal temperature of 22-25°C. The miracidia hatch intramuscular injection of dihydroemetine. Both drugs and within 8 hours invade an amphibious snail, usually are toxic and of limited effectiveness. Praziquantel, a a species of Lymnaea. During 30-40 days the larvae newer drug, has been effective in some recent trials. develop into sporocysts followed by two redial stages, 417 418 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS A~~~- _ _ - ~ ~ ~ ~ - Figure 27-1. An adult Fasciola hepatica under a light microscope. Scale bar = 5 millimeters. (Photo: Wellcome Museum of Medical Science) and cercariae emerge. The cercariae swim in the water prevalence of fascioliasis (Stork and others 1973). for up to 8 hours and then encyst as metacercariae on Watercress was not consumed in this area, and it was aquatic vegetation. Sheep and cattle become infected considered that lettuce and alfalfa were the sources of when they eat encysted metacercariae on grass. People human infections. Other accounts of fascioliasis become infected when they eat encysted metacercariae include those from Australia (Wood, Stephens and on watercress, salad vegetables, or any water plant Porter 1975), Britain (Anon 1978), Dominican eaten raw. When the cysts are ingested, the larvae Republic (Ueno and others 1973), Egypt (Farag and excyst in the duodenum, migrate through the intestinal others 1979), France (Rondeland, Amat-Frut and wall, and reach the bile ducts by eating their way Pestre-Alexandre 1982), Iran (Farid 1971), Japan through the surface of the liver and through the liver (Ueno and others 1975), Madagascar (Moreau and parenchyma. others 1975), Norway (Brandt 1974), and Switzerland The life cycle of F. gigantica is similar, except that the (Boray 1971). F. gigantica infection in animals in West snail hosts are aquatic, not amphibious. Africa was reviewed by Schillhorn van Veen (1980). Prepatent and incubation periods Control Measures The adult fluke matures 3-4 months after ingestion Because the animal reservoir is more important for of the encysted metacercariae. Acute symptoms due to transmission of fascioliasis than the human reservoir. the migrating larvae in the liver may be experienced excreta disposal will have little effect on the control of soon after the ingestion of metacercariae. the infection. Snail control, though difficult to achieve, can be attempted by the use of molluscicides and by Epidemiology drainage of pasture. Watercress beds should be protected from contamination by animal feces, and the Fascioliasis is an infection of herbivores, principally public should be informed of the danger of eating sheep and cattle. Man sometimes accidentally takes the watercress, or other salad vegetables, grown in wet land place of the herbivore as the vertebrate host in the where sheep or cattle have access. parasitic life cycle. Small foci of human fascioliasis have been reported, but it is a rare infection in man. There is no firm evidence of man-to-man transmission, and it is Occurrence and Survival in the probable that human infections only occur where there Environment is endemic fascioliasis among sheep or cattle. A stool survey of 1,011 schoolchildren from six There is a substantial literature on the survival and villages in the Peruvian Andes showed a 9 percent development of Fasciola eggs, and this information has FASCIOLA AND FASCIOLIASIS 419 been used to explain the seasonal pattern of fascioliasis Inactivation by Night Soil and Sludge in animals in Europe. Eggs survive for many months Treatment Processes below 10°C but do not develop. Therefore, in temperate climates many eggs overwinter, and the Fasciola eggs in night soil and sludge are of no miracidia hatch out in spring. The development in interest because transmission is maintained by eggs in snails takes place over the summer, and the encysted sheep and cattle feces. Fasciola eggs in manure and metacercariae on herbage build up in early autumn. farm slurry are important, and it may be assumed that These metacercariae can also survive over winter. any processes that eliminate Ascaris eggs (chapter 23) Fasciola eggs must be free of feces and surrounded will also eliminate Fasciola eggs. by moisture to develop. They are rapidly killed by desiccation. They develop most rapidly at 25-30°C; they do not develop below 10°C and they are killed at Literature Cited -5°C (Becejac and Lui 1959; Rowcliffe and Ollerenshaw 1960; Tunker 1940; Valenzuela 1979). Anon. (1978). Liver fluke in Brtain. British MedicalJournal, Fasciola eggs survive in slightly brackish water but 1,19. notcinla seawatervi(Saint suighain brandkchwteur 19; Becejac, S. and Lui, A. (1959). The influence of temperature not in seawater (Saint Guillain and Pecheur 1967; and oxygen on the development of Fasciola hepatica eggs. Styczfiska-Jurewicz 1965b). In anaerobic water, eggs Veterinarski Arhiv, 29, 293-301. survive but do not develop. Development recom- Boray, J. C. (1971). Progress in the control of fascioliasis. mences when oxygen is supplied (Becejac and Lui Schweizer Archiv f[r Tierheilkunde, 113, 361-386. 1959; Styczriska-Jurewicz 1965a). Eggs develop in Boray, J. C. and Enigk, K. (1964). Laboratory studies on the waters with pH between 4.2 and 9.0, a wider pH range survival and infectivity of Fasciola hepatica and Fasciola than is tolerated by the snail host (Rowclifle and gigantica metacercariae. Z. ,: -i ,fur Tropenmedizin und Ollerenshaw 1960; Saint Guillain and Pecheur 1967). Parasitologie, 15, 324-331. Fasciola eggs develop not only in water, but also in a Brandt, G. (1974). Public health aspects of fascioliasis. 1:1 mixture of water and liquid manure. The survival Nordisk Veterinaermedicin, 26, 56. Dwaronat, A. (1966). Results on free-living helminth stages. 3. Experimental results on the longevity of miracidia of F. days at 4-8°C (Six and Hoffman 1970). hepatica under various external influences. Angewandte Miracidia usually survive in water for only a few Paiasitologia, 7, 31-38. hours. Survival is enhanced by cool water tempera- Farag, H. F., Barakat, R. M. R., Ragab, M. and Omar, E. tures, by darkness, by high oxygen levels, and by (1979). A focus of human fascioliasis in the Nile Delta, neutral pH (Dwaronat 1966; Gebauer 1958). Egypt. Journal of Tropical Medicine and Hygiene, 82, Encysted metacercariae of F. hepatica can survive for 188-190. several months, especially if conditions are cool and Farid, H. (1971). Human infection with Fasciola hepatica and moist. They survive on a wet surface for 12 hours at Dicrocoelium dendriticum in Isfahan area, central Iran. -20°C, 4 weeks at - 10°C, 13 weeks at -2°C, and 19 Journal of Parasitology, 57, 160. weeks at 10-20'C. Survival times decrease at Gebauer, 0. (1958). Lime and its relation to the control of tempe e a e hliver-flukes. ArchivfCir experimentelle Veterinarmedizin, 12, temperatures above 25°C or at lower humidities 79-81. (Boray and Enigk 1964; Kakatcheva-Avramova 1963). Kakatcheva-Avramova, D. (1963). Temperature limits of Metacercariae of F. gigantica are more resistant to viability of Fasciola hepatica metacercariae. Helmin- warm temperatures but more susceptible to de- thologia, 4, 183-190. siccation (Boray and Enigk 1964). Moreau, J. P., Gentelet, B., Barbier, D. and Goasguen, J. (1975). Does Fasciola gigantica infection exist in man in Madagascar? A report of one case checked by immu- nological methods. Medecine Tropicale, 35, 402-406. Rondeland, D., Amat-Frut, E. and Pestre-Alexandre, M. Inactivation by Sewage Treatment (1982). La distomatose humaine a Fasciola hepatica L. Processes Bulletin de la Societe de Pathologie Exotique, 75, 291-300. Roweliffe, S. A. and Ollerenshaw, C. B. (1960). Observations Fasciola eggs rarely occur in sewage and in very low on the bionomics of the egg of Fasciola hepatica. Annals of concentrations. Their removal during sewage treat- Tropical Medicine and Parasitology, 54, 172-181. ment is of no interest, since it is Fasciola eggs in sheep Saint Guillain, M. and Pecheur, M. (1967). Influence of pH and cattle feces that are responsible for the and salts on the development of Fasciola hepatica eggs. maintenance of transmission. Annales de Medecine Veterinaire., 111, 251-257. 420 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Schillhorn van Veen, T. W. (1980). Fascioliasis (Fasciola Tunker. H. F. (1940). On the effect of different temperatures gigantica) in West Africa: a review. Veterinary l-,i. i., 50. and desiccation on the development of early stages of 529-533. helminths in Anatolian sheep. Arheiten aus dCnC Yiil/sek Six. F. and Hoffman. K. (1970). The survival of Fasciola ziraat enstitjish Ankara, 71, 1-30. hepritica eggs in liquid manure and diluted liquid manure Ueno, H., Alvarez V., J. M.. Mergen, A. M. R. and Sanchez. V. with or without the addition of one of the Shell products, M. (1973). Observation on the prevalence of parasitic Birlane Fluid or Frescon 16 °O. Tlerarztliche Unischiau, 25, diseases in cattle, especially fascioliasis. in the Dominican 584-586, 589-590. Republic. National Institute of Ani7imal Health Quarterly, Stork. M. G.. Venables. G. S.. Jennings, S. M. F., Beesley, J. 13, 59-68. R., Bendezu, P. and Capron. A. (1973). An investigation of Ueno, H.. Yoshihara. S., Sonobe. 0. and Morioka, A. (1975). endemic fascioliasis in Peruvian village children. Joutrnal oj Appearance of Fasciola cercariae in rice fields determined Tropical Medicine and Hvgiene, 76, 231-235. 238. by a metacercaria-detecting buoy. Nationial Institrte o,t Styczvnska-Jurewicz, E. (1965a). Adaptation of eggs and Aninzal Health Quarterly, 15, 131-138. larvae of Fasciola hepatica to the conditions of astatic Valenzuela, G. (1979). Estudio epidemiologico sobre el habitats of Galba truncatula. Acta Parasitologica Polonica, desarrollo de huevos de Fasciola hepatica en el medio 13, 151-170. ambiente de Valdivia. Chile. Boletin Chilenio de (1965h1. The influence of a brackish environment on Parasitologia, 34, 31-35. the development of eggs and viability of miracidia of Wood. I. J.. Stephens, W. B. and Porter. D. D. (1975). Fasciola hepatica. Acta Parasitologica Polonica, 13, Fascioliasis causing hepatitis in eaters of watercress. 483-497. Mledical Jouirnal oj Australia, 2, 829-831. 28 Fasciolopsis and Fasciolopsiasis FASCIOLOPSIASIS is a disease of rural people in areas of Infectious agent eastern Asia where certain water plants are eaten raw. Fasciolopsis buski, a trematode, is the giant intestinal It is not of great public health importance. fluke of man. The adult is fleshy, elongated, and ovoid and is the largest trematode of man, measuring 20-75 Description of Pathogen and Disease millimeters by 8-20 millimeters (figure 28-2). The eggs are 130-140 micrometers by 80-85 micrometers and The literature on fasciolopsiasis is not large, are very similar to those of Fasciola hepatica. although the disease is attracting increased research interest in Bangladesh and elsewhere. Reservoirs Man, pigs, and dogs are definitive reservoir hosts of Identification adult flukes. Pigs are especially important in the Fasciolopsiasis is an infection of the small intestine maintenance of endemic fasciolopsiasis in central particularly the duodenum, by the trematode Thailand and some other areas Fasciolopsis buski. In the majority of cases the infection is light, and there are no symptoms. Heavy infections Transmission may cause intestinal obstruction and symptoms such as nausea, diarrhea, fever, and abdominal pains. The adult worm, which lives attached to the wall of Patients may show edema of the face, the abdominal the small intestine, lays about 25,000 unembryonated wall, and the legs within 20 days after massive infection, eggs per day. The eggs are passed in the feces. When the Ascites is common, as is eosinophilia; secondary eggs reach fresh water they develop and hatch under anemia occurs occasionally; death is rare. favorable conditions (temperature 27-32°C)within 3-7 Diagnosis is by finding flukes or characteristic eggs weeks. in the feces. Treatment is by oral drug therapy with The hatched miracidia penetrate a freshwater hexylresorcinol, tetrachlorethylene, or bithionol. planorbid snail, and a process of asexual multiplication occurs that results in developed cercariae, which then emerge into the water. They swim in the water and become attached to aquatic vegetation such as seed Fasciolopsis buski occurs in man in Southeast Asia, pods of water caltrop, bulbs of water chestnuts, and especially in central and south China. It seems to be roots of lotus, water bamboo, and others. There they restricted to areas where cultivation of water plants encyst as metacercariae. such as water caltrop, water chestnuts, water hyacinth, When ingested with edible plants, the metacercariae and water bamboo takes place and in communities excyst in the duodenum of man, and the young flukes that consume uncooked infected plants. Endemic areas develop. are found in Bangladesh, Kampuchea, China, India, Indonesia, Laos, Taiwan, Thailand and Vietnam (figure 28-1). Human infections reported in Japan, the Prepatent and incubation periods Philippines, and Malaysia probably occur in people Mature flukes develop and start laying eggs within who have emigrated from endemic areas. 3-4 months after infective cysts have been ingested. 421 422 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS X g g ~~~~~~~~~~~~~FASCIOLOPSIS BUSKI I < dS c X I %g4~~~~~~~~~~~~~e toD m r1 Figure 28-1. Known geographiical distribution oj Fasciolopsis buski. The infection may occur in areas as yet unrecorded Massive infection can lead to symptoms within 20 watercress are also implicated as sources of infection. days, but more usually symptoms develop slowly or Before the nuts of water caltrop or the bulbs of water not at all. chestnut are eaten, the outer covering is removed with the teeth, and this may be the primary mode of Period of communicability infection. This practice is especially common among children, who are usually more heavily infected than Eggs may be passed in the feces as long as a mature adults. Peak prevalences have been reported in the worm is present in the intestine. Adult worms live for 10-14 age group in central Thailand (Sadun and only about 6 months in man. Maiphoom 1953) and in Taiwan (Hsieh 1960) and in Resistance the 5-14 age group in Bangladesh (Rahman, Idris and Khan 1981). In Taiwan, Thailand, and other areas, There is no resistance proved. Malnourished water plants are harvested and fed to pigs, and this individuals are more prone to symptoms. helps to maintain a high prevalence of fasciolopsiasis in pigs. Epidemiology Reports of fasciolopsiasis epidemiology include those from Bangladesh (Rahman, Idris and Khan Prevalences of fasciolopsiasis are over 70 percent in 1981). China (Barlow 1925; Chu and others 1959), some endemic foci. The seed pods of water caltrop are Taiwan (Hsieh 1960; Lee 1972), Thailand (Manning, an important source of infection, especially where they Brockelman and Viyanant 1971; Manning and are cultivated in ponds enriched with night soil. Water Ratanarat 1970; Sadun and Maiphoom 1953), and chestnut, water bamboo, water hyacinth, lotus. and elsewhere in Southeast Asia (Cross 1969). FASCIOLOPSIS AND FASCIOLOPSIASIS 423 Figure 28-2. An adult Fasciolopsis buski under a light microscope. Scale bar = 5 millimeters. (Photo: Wellcome Museum of Medical Science) Control Measures Occurrence and Survival in the Environment Metacercariae on plants can be killed by drying the plants or dipping them in boiling water. The four stages of Fasciolopsis found in the The use of excreta as fertilizer in fields and ponds is environment are eggs, miracidia, cercariae, and an important factor in the transmission of fasciolop- encysted metacercariae. Eggs hatch in water within 3-7 siasis. It is relatively simple to treat the excreta and kill weeks at 27-32°C, and hatching is inhibited at the Fasciolopsis eggs because these eggs are quite temperatures above and below this range (Barlow susceptible to adverse conditions. In areas where pigs 1925). In winter in Taiwan, with water temperatures are important in maintaining a reservoir of below 20°C, immature eggs may survive but do not Fasciolopsis, steps must be taken to prevent pig excreta continue their development (Suzuki 1922). Eggs die in from reaching water in which plants for human human urine within a few hours (Komiya 1964) and in consumption are grown. feces within 18 days (Barlow 1925). Eggs are rapidly The transmission of fasciolopsiasis depends on the killed by desiccation. Miracidia in water must find an customs and habits of inhabitants of endemic areas appropriate snail within 8 hours or die. who grow and eat water plants. Public health Encysted metacercariae are killed by desiccation, education should promote changes in night soil reuse direct sunlight, and warm temperatures. They survive and disposal and in the consumption of raw water for up to 30 minutes in direct sunlight, 15 minutes at plants. 60°C, and 1 minute in boiling water (Barlow 1925; 424 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Komiya 1964). Metcercariae are also killed in 2 percent infestation among school children in Canton. Chinese acetic acid in 9 days, 5 percent salt solution in 3 hours, Medical Journal, 78, 273. and soybean sauce in 30 minutes (Komiya 1964). Cross, J. H. (1969). Fasciolopsiasis in Southeast Asia and the Far East: A review. In Proceedings of the Fourth Southeast Asian Seminar on Parasitology and Tropical Medicine., Inactivation by Sewage Treatment Schistosomiasis and other Snail-transmitted Helminthiases, ed. Harinasuta, C., pp. 177-196. Bankok: Thai Watana Processes Panich Press. Hou, T. C., Chung, H. L., Ho, L. Y. and Weng, H. C. (1959). The fate of Fasciolopsis eggs in sewage treatment Achievements in the fight against parasitic diseases in New plants has not been studied. Most transmission is China. Chinese Medical Journal, 79, 493-520. associated with direct enrichment of ponds with feces Hsieh, H. C. (1960). Studies on the epidemiology of or night soil rather than with accidental contamination Fasciolopsis buski in South Taiwan. Formosan Science. 14, from poorly treated sewage effluents. In addition, 95-120. fasciolopsiasis is endemic in poor rural areas where Komiya, Y. (1964). Fasciolopsis buski. In Progress of Medical most people use simple latrines, or no latrines, and Parasitology in Japan, 1, eds. Morishita, K., Komiya, certainly produce nosewage.Y. and Matsubayashi. H., pp. 277-285. Tokyo: Meguro certainly produce no sewage.PasiogcaMuem Parasitological Museum. Lee, H. H. (1972) Fasciolopsis buski infection among children of Liu-ying Primary School in Tainan Hsien south Inactivation by Night Soil and Sludge Taiwan. Chinese Journal of Microbiology, 5, 110-114. Treatment Processes Manning, G. S., Brockelman, W. Y. and Viyanant. V. (1971). An analysis of the prevalence of Fasciolopsis buski in Fasciolopsis eggs in night soil or sludge may be killed central Thailand using catalytic models. American Journal by drying, freezing, heating, or storage for 18 days of Epidemiology, 93, 354-360. (Barlow 1925). Eggs survived for up to 28 days in Manning, G. S. and Ratanarat, C. (1970). Fasciolopsis buski (barlowg 1925).lEggsssurvivediforaupHtou281days in (Lankester, 1857) in Thailand. American Journal of Tropical Medicine and Hygiene, 19, 613-619. Rahman, K. M., Idris, M. and Khan, A. K. A. (1981). A study on fasciolopsiasis in Bangladesh. Journal of Tropical Literature Cited Medicine and Hygiene, 84, 81-86. Sadun, E. H. and Maiphoom, C. (1953). Studies on the Barlow, C. H. (1925). The Life Cycle of the Human Intestinal epidemiology of the human intestinal fluke. Fasciolopsis Fluke, Fasciolopsis buski. American Journal of Hygiene buski (Lankester) in Central Thailand. American Journal of Monographic Series no. 4. Tropical Medicine and Hygiene, 2, 1070-1084. Chu, S. H., Peng, W. W., Chou, C. C., Lo, C. Y., Liu, T. C.. Suzuki, S. (1922). Effects of certain physical and chemical Hsien, T. C.. Chang, P. C., Chu, P. L., Wu, W. C. and influences upon the eggs of Fasciolopsis buski. Taiwan Chang, Y. S. (1959). Mass treatment of Fasciolopsis buski Igakkai Zasshi, 21, 1. 29 Hymenolepis and Hymenolepiasis THREE GENERA of tapeworm are parasites of the Infectious agent human intestine and are transmitted when proglottids Hymenolepis nana, a cestode, is the dwarf tapeworm or eggs are passed in the feces. These are of man. The entire worm measures only 15-40 Diphyllobothrium (chapter 25), Taenia (chapter 34), millimeters by 1 millimeter and has approximately 200 and Hymenolepis (this chapter). The Hymenolepis speiestha inect ma, H nna,is nusal n tat t roglottids. The minute scolex has four suckers and a species that Infects man, H. nana, Is unusual in that it row of hooks and is embedded in the wall of the ileum can be transmitted directly from person to person (figure 29-1). The mature proglottids measure 0.22 by without a cystic stage in an intermediate host. This is in 0.88 millimeters and the eggs measure 30-47 contrast to Diphyllobothrium (which has intermediate stages in a copepod and a fish) and Taenia (which has micrometers In diameter an intermediate stage in a cow or a pig). Reservoirs The reservoir of H. nana is probably man. A Description of Pathogen and Disease morphologically identical tapeworm (H. nana var. fraterna) is common in mice, but it is not certain Hymenolepiasis is not a major public health whether this normally infects man. problem, although in certain localities it is common The rat tapeworm, H. diminuta, is a common and is regarded seriously by clinicians. The literature parasite of rodents in many parts of the world. Like on hymenolepiasis epidemiology is limited. most cestodes it has an intermediate host, in this case a rat flea or flour beetle that must eat the excreted eggs. Identification H. diminuta cannot be transmitted directly from rodent to rodent (Salem, Sidky and Abdel-Rehim 1980). The Hymenolepiasis is an infection of the small intestine rodent is reinfected by eating the flea or beetle by the tapeworm (cestode) Hymenolepis. With a light containing the encysted worm. Children occasionally infection, symptoms are often vague or absent. Heavy ingest infected fleas or beetles, and H. diminuta infections can result in enteritis with abdominal pain, infections are found in children in some countries. H. diarrhea, loss of appetite, and dizziness. Epileptic fits diminuta has little medical or public health importance are an occasional complication in children. Diagnosis but has been much used as a laboratory model for is by identifying Hymenolepis eggs in the feces. cestode infections, and there is a substantial literature Treatment is by oral drug therapy with niclosamide. on it. A very similar pattern of occasional human Praziquantel, a newer drug under trial, shows promise infection is found for the dog tapeworm (Dipylidium (Schenone 1980). caninum), for which the intermediate host is a dog flea. Occurrence Transmission Hymenolepiasis occurs worldwide and is especially The gravid proglottids containing 80-200 eggs are prevalent among children. It is more common in warm usually broken up in the intestine so that free eggs are climates than in cold climates. It is most common in found in the feces. Eggs passed in feces are immediately South America, North India, the Mediterranean infective if ingested by a new host. The eggs are not countries, Eastern Europe, and the Pacific islands. resistant to heat or desiccation and normally survive 425 426 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS ~~~~~~~~. ~. l, . . , -,, - 4 * A 'x xtQ ' 0{~K r _ X ^< # X- 7 _; @ -- :. - ... - ' w: '1{-' . --'-A -nt s -, '--- N, -~~~~~~~A A A' ~ ~ r X~~r M-r ., - v i - .- i~>- _- - 4 .r .'t ,,;.' '%§144 >240 <72 <8 <4 <3 d'Igiene, 28, 571-579. Feces in Ghadirian, E. and Arfaa, F. (1972). Human infection with water ND ND > 720 < 120 <10 < 30 Hymeniolepis dininuta in villages of Minab, southern Iran. International Journalfbr Parasitology, 2, 481-482. ND No data. Gudzhabidze, S. I. and Lyubchenko, S. D. (1959). Control of Source: Simitch. Bordjochki and Angelovski (1955). ascariasis and ancylostomiasis by composting of organic waste material. Meditsinskaia Parazitologiia i Para- zitarnye Bolezni, 28, 576-578. Ascaris eggs during sewage treatment. Nonetheless, It Hira, P. R. (1975). Human infection with the cestode is to be expected that H. nana eggs, like all other Hymnenolepis diminuta (Rudulphi, 1819; Blanchard. 1891). helminth eggs, are mainly concentrated into the raw Medical Journal of Zambia, 9, 93-95. sludge of the primary and secondary sedimentation Huggins, D., Siqueira. M. W., Souza, E. M. and Da Silva. S. tanks. H. nana eggs are completely removed from the M. (1973). Incidence of hymenolepiasis nana and Taenia effluent of well-designed waste stabilization pond sp. in the Institute of Tropical Medicine at the Federal systems (table 92-4 and Lakshiminarayana and University of Pernambuco from 1968 to 1970. Anais do Abdulappa 1969). Instituto de Higiene e Medicina Tropical. 1, 63-68. Krdlova, E. and Safrtnek, V. (1957). Helminthological investigation of sediments from the wastewater refining Inactivation by Night Soil and Sludge station at Kurim. Ceskoslovenskc Hygiena, 2, 399-404. Kuznetsov, I. V. (1979). Economic losses prevented as a result Treatment Processes of a sharp decline in hymenolepiasis. Meditsinskaia Parazitologiia i Parazitarnye Bolezni, 48, 106-108. H. nana eggs will be readily eliminated from night Lakshminarayana, J. S. S. and Abdulappa, M. K. (1969). The soil and sludges, especially if warm temperatures are effect of sewage stabilization ponds on helminths. In Low created (table 29-1) or if desiccation takes place. Cost Waste Treatment, ed. Sastry, C. A., pp. 290-299. Thermophilic composting destroys H. nana eggs Nagpur: Central Public Health Engineering Research (Gudzhabidze and Lvubchenko 1959), and H. nana Institute. eggs will be eliminated from all processes long before Lerner, P. M., Bedzhanyanc, A. S., Cvetkova. E. N., Gogol, V. eggs will be eliminate~ from all processes long before A. and Sayfulina, A. K. (1970). Experience of two years Ascaris eggs. work on mass sanitation from hymenolepiasis of the population in Samarkand. Meditsinskaia ParaZitologiia i Parazitarnve Bolezni, 39, 559-564. Literature Cited McMillan. B., Kelly, A. and Walker, J. C. (1971). Prevalence of Hymenolepis diminuta infection in man in the New Biswas. H., Arora, R. R. and Sehgal, S. (1978). Epidemiology Guinea Highlands. Tropical and Geographzical Medicine, of Hymnenolepis nania infection in a selected rural 23, 390-392. community. Journal of Communicable Diseases, 10, Massoud, J., Arfaa. F.. Jalali. H. and Keyvan, S. (1980). 170-174. Prevalence of intestinal helminths in Khuzestan, south- Buscher, H. N. and Haley A. J. (1972). Epidemiology of west Iran, 1977. American Joturnal ofTropical Medicine and Hymenolepis nana infections of Punjabi villagers in West Hygiene, 29, 389-392. Pakistan. American Journal of Tropical Medicine and Melvin, D. M. and Brooke, M. M. (1962). Parasitologic Hygiene, 21, 42-49. surveys on Indian reservations in Montana, South Chandler, A. C. (1954). A comparison of helminthic and Dakota, New Mexico, Arizona, and Wisconsini. Amlericca protozoan infections in two Egyptian villages two years Journ,Zal of Tropical Medicinie and Hygienie, 11, 765-772. after the installation of sanitary improvements in one of Panicker, P. V. R. C. and Krishnamoorthi. K. P. (1978). HYMENOLEPIS AND HYMENOLEPIASIS 429 Elimination of enteric parasites during sewage treatment Sinniah, B. (1978). Hymenolepis diminuta infection in a processes. Indiani Associationzfor Water Pollution Control Malaysian oil palm estate worker: first case from Technical Annual, 5, 130-138. Malaysia. Southeast Asian Journal of Tropical Medicine Rifaat, M. A., Salem, S. A. and Hegazi, M. M. (1978). The and Public Health, 9, 453-454. mechanism of resistance to a superimposed infection with Van Niekerk, C. H., Weinberg, E. G., Lorn Shore, S. C. and Hymenolepis nana. Journal of the Egyptian Society of Heese, H. de V. (1979). Intestinal parasitic infestation in Parasitology, 8, 85-94. urban and rural Xhosa children. Southz African Medical Salem, S. A., Sidky, H. A. and Abdel-Rehim, L. (1980). A Journal, 55, 756-757. study of the direct mode of transmission of the intestinal van Zijl, W. J. (1966). Studies on diarrhoeal diseases in seven tapeworm Hymenolepis diminuta (Rudolphi, 1819). countries by the WHo Diarrhoeal Diseases Advisory Team. Journal of the Egyptian Society of Parasitology, 10, 95-99. Bulletin of the World Health Organization, 35, 249-261. Schenone, H. (1980). Praziquantel in the treatment of Warren, K. S. (1974). Helminthic diseases endemic in the Hymenolepis nana infections in children. American Journal United States. American Journal of Tropical Medicine and of Tropical Medicine and Hygiene, 29, 320-321. Hygiene. 23, 723-730 Seo, B. S., Rim, H. J., Loh, I. K., Lee, S. H., Cho, S. Y., Park, S. Wright, W. H., Cram, E. B. and Nolan, M. 0. (1942). C., Bae, J. W., Kim, J. H., Lee, J. S., Koo, B. Y. and Kim, K. Preliminary observations on the effect of sewage treatment S. (1969). Study of the status of helminthic infections in processes on the ova and cysts of intestinal parasites. Koreans. Korean Journal of Parasitology, 7, 53-70. Sewage Works Journal, 14, 1274-1280. Simitch, T., Bordjochki, A. and Angelovski, T. (1955). Yasarol, S., Orhan, V. and Erefe, I. (1970). Incidence of Survival of embryos in the eggs of Hymenolepis nana hymenolepiasis in children of the Egge Province. Turk outsidethehost.Archiresdel'InstitutPasteurd'AlgMrie,33, Hijiyen ye Tecrubi Biyoloji Dergisi, 30, 132-137. 30-34. 30 Minor Intestinal Flukes and Infections They Cause THREE TREMATODES, in addition to Fasciolopsis, Infectious agents infect the human intestine: Heterophyes heterophyes, These are all hermaphroditic flattened trematodes. Metagonimus yokogawai, and Gastrodiscoides hominis. Heterophyes heterophyes and Metagonimus yokogawai They are quite common in limited geographical areas. (which are very similar in morphology and life history) They are of only minor public health importance, and are very s5mllim (figure 30t3 ) are included in this book for completeness. Gasrrodiscoides hominis measures 6 by 4 millimeters (figure 30-4). The eggs of H. heterophyes and M. yokogawai measure 30 by 15 micrometers, and those of Description of Pathogens and Diseases G. hominis 146 by 66 micrometers. Little is known of these infections or their Reservoirs epidemiology. These are all primarily parasites of animals. H. heterophyes and M. yokogawai infect dogs, cats, foxes, Identification and other fish-eating mammals, and perhaps birds. G. hominis infects pigs, monkeys, and rats. All three Heterophyiasis, metagonimiasis, and infection by parasites can probably be maintained in the absence of Gastrodiscoides hominis are trematode infections of the man. small intestine. Infections are usually asymptomatic, but occasionally minor intestinal disturbances such as nausea, diarrhea, fever, and abdominal pain may Transmission occur. For all these parasites, eggs are passed in the feces Diagnosis is by identifying eggs in the feces, and have to reach water for further development. Treatment is by appropriate oral drug therapy. Larvae develop in specific freshwater snails, and a process of asexual multiplication occurs so that some hundreds of the next free-living stage, the cercariae, are Occurrence released from the snail into the water. These cercariae then form encysted metacercariae. Heterophyes and Heterophves heteroph yes has a disjunct distribution, Metagonimus encyst under the scales, on the surface, or being found in southern Europe (Romania and in the superficial muscle of fish. Gastrodiscoides encysts Greece), the Middle East (Egypt and Israel), and East on water plants. The habitat of the snail and fish Asia (China, Japan, Philippines, South Korea, and intermediate hosts of Heterophyes is brackish water. Taiwan) (figure 30-1). Metagonimus yokogawai occurs The habitat of the snail intermediate host of in China, Japan, Korea, Taiwan and the eastern USSR Metagonimus is freshwater, whereas the fish in- (figure 30-1). Gastrodiscoides hominis is found in termediate host lives in both fresh and brackish water. Bangladesh, India, Philippines, and Vietnam (figure Animal or human infection takes place when raw fish 30-2). or water plants are ingested. Thus the life cycles of 431 432 El HETEROPHYES HETEROPHYES METAGONIMUS YOKOGAWAI Figure 30-1. Known geographic distributions of Heterophyes heterophyes and Metagonimus yokogawai. The infections may occur in areas as yet unrecorded Z GASTRODISCOIDES HO MINIS ~~~~~~~~~~0 AY Figure 30-2. Known geographical distribution oj'Gastrodiscoides hominis. The infection may occur in areas as yet unrecorded MINOR INTESTINAL FLUKES AND INFECTIONS THEY CAUSE 433 n is -a # -. (b) Figure 30-3. Adult Heterophyes heterophyes (a) and Metagonimus yokogawai (b) unider- a light microscope. Scale bars = 0.1 millimeter. (Photos: Weilcome Museum of Medical Science) 434 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS I- - -. Figure 30-4. An adult Gastrodiscoides hominis under a light microscope. Scale bar 1 millimeter. (Photo: Wellcome Museum of Medical Science) Heterophyes and Metagonimus are similar to lieterophyes and M. -vokogawai and almost nothing of Clonorchis (chapter 24), whereas the life cycle of G. hominis. It may be broadly assumed that the Gastrodiscoides resembles that of Fasciolopsis (chapter epidemiology of the first two resembles that of 28). Clonorchis or Opisthorchis (chapter 24), whereas that of G. hominis resembles Fasciolopsis (chapter 28). Prepatent and incubation periods In Egypt, heterophyiasis is associated with eating freshly salted mullet (Khalil 1933; Martin and Kuntz Metagonimus and Heterophyes flukes develop and 1955). Heterophyiasis in the Philippines was reviewed begin to lay eggs 15-20 days after encysted by Africa and Garcia (1935). Metagonimiasis does not metacercariae have been ingested. occur in areas where the summer water temperatures are below 180C because the cercariae do not emerge Period of communicability from the snails in cool water. Seo and others (1969) As long as mature flukes are present in the intestine, surveyed 40,000 people in South Korea and found a eggs will be passed. Mature flukes live for about 2 prevalence of metagonimiasis of 0.4 percent. Infection months. rates were higher in males than females and higher in adults than in children. These age and sex differences are typical of heterophyiasis and metagonimiasis and Resistance are due to differences in diet. Metagonimiasis in the There is no evidence of immunity or resistance. USSR was discussed by Zubov, Drozdov and Chernova (1970). The epidemiology of G. hominis Epidemiology ~~~~~~~infection is poorly understood, although there have Epigurem 30-4. AnadultGastrodiscoideshominisunderabeen several reports from India (Ahluwalia 1960h Little is known of the epidemiology of H. Buckley 1939: Dutt and Srivastava 1972m Varma 1957). MINOR INTESTINAL FLUKES AND INFECTIONS THEY CAUSE 435 Control Measures Literature Cited Control of H. heterophyes and M. yokogawai is as Africa, C. M. and Garcia, E. Y. (1935). Heterophyid recommended for Clonorchis (chapter 24). Control of trematodes of man and dog in the Philippines with G. hominis is as recommended for Fasciolopsis (chapter descriptions of three new species. Philippine Journal of 28). Science, 57, 253-267. Ahluwalia, S. S. (1960). Gastrodiscoides hominis (Lewis and McConnell) Leiper, 1913 the amphistomate parasite of Occurrence and Survival in the man and pig. Indian Journal of Medical Research, 48, 315-325. Environment Buckley, J. J. C. (1939). Observations on Gastrodiscoides hominis and Fasciolopsis buski in Assam. Journal of Little is known. H. heterophyes cercariae survive for Helminthology, 17, 1-12. 20 minutes in freshwater and for 2 days in seawater. M. Dutt, S. C. and Srivastava, H. D. (1972). The life history of yokogawai cercariae survive for 8 hours in freshwater Gastrodiscoides lhomintis (Lewis and McConnell, 1876) (Ito 1964). Leiper, 1913 the amphistome parasite of man and pig. M. yokogawai encysted metacercariae in fish survive Journzal of Helminthologya, 46, 35-46. fr15 minutes at 70-80'C, 2 hours in vinegar, 6 hours Ito, J. (1964). Metagonimus and other human heterophyid foryba saue, 3 70 in 2 hour s in begr, 6o trematodes. In Progress of Medical Parasitology in Japan, in soybean sauce, 3 days in rice wine, 7 days in beer, 10 vol. 1, eds. Morishita, K., Komiya, Y. and Matsubayashi, days frozen, and 14 days in tap water (Ito 1964). H.,Ipp.31t7-393.Tokyo: Meguro Parasitological Museum. Khalil, M. (1933). The life history of the human trematode parasite. Heterophyes heterophyes, in Egypt. Lancet, 2, 537. Inactivation by Sewage Treatment Martin, W. E. and Kuntz, R. E. (1955). Some Egyptian Processes heterophyid trematodes. Journal of Parasitology, 41, 374-382. There is no specific information. Seo, B. S., Rim, H. J.. Loh, I. K., Lee, S. H., Cho, S. Y.. Park, S. C., Bae, J. W., Kim, J. H., Lee, J. S., Koo, B. Y. and Kim, K. S. (1969). Study on the status of helminthic infections in Koreans. Korean Journal of Parasitology, 7, 53-70. Inactivation by Night Soil and Sludge Varma, A. K. (1957). On a collection of Paramphistomes Treatment Processes from domesticated animals in Bihar. Indian Journal of Veterinary Science and Animal Husbandry, 27, 67-76. There is no specific information. Zubov, N. A., Drozdov. V. N. and Chernova, A. S. (1970). Clinical picture and pathology of metagonimiasis. Meditsinskaia Parazitologiia i Parazitarnve Bolezni, 39, 392-394. 31 Paragonimus and Paragonimiasis THE LIFE CYCLE of Paragonimus is similar to that of Infectious agent Clonorchis, Heterophyes, and Metagonimus except that Paragonimus westermani, a trematode, is the lung the metacercariae encyst in crabs and crayfish rather fluke of man. The adult worm, which typically lives than fish. Paragonimiasis is therefore a disease of encapsulated in pockets of the lung, is a thick, fleshy, people who customarily cat raw crabs or crayfish. ovoid fluke measuring 8-16 by 4-8 millimeters (figure 31-2). The eggs are 80-110 by 50-60 micrometers. Description of Pathogen and Disease Reservoir Paragonimiasis can be a very serious disease and has Paragonimiasis is an infection found in a great been studied in detail, especially in China, Japan, variety of mammals that feed on crabs. P. westermani South Korea, and Taiwan. can infect a range of wild animals such as tigers, lions, wild cats, and foxes and domestic animals such as cats Identification and dogs. Although in endemic areas man is the most important reservoir, the persistence of P. westermani in Paragonimiasis is an infection, principally of the nature does not depend only on the human reservoir. lungs but sometimes of the brain, with a trematode of Various other Paragonimus species are maintained the genus Paragonimus. It is characterized by severe solely by animals in most tropical areas of the world chest pains, dyspnea, and bronchitis. Symptoms and are the cause of occasional cases in man. For resemble those of tuberculosis, especially blood- instance, P. africanus is the lung fluke of the crab-eating stained sputum. Cerebral paragonimiasis may result in mongoose and infects man in parts of eastern Nigeria epileptic seizures, headache, visual disturbances, and and Cameroon. symptoms of meningitis. Diagnosis is by finding eggs in feces or sputum. Treatment is by oral drug therapy with bithionol or Transmission praziquantel. The unsegmented fertilized eggs are passed out in sputum or swallowed and passed out in feces. For Occurrence further development they have to reach water. At an optimum temperature of 27°C, a larva (miracidium) Paragonimiasis in animals occurs worldwide among develops in 3 weeks. After hatching, it swims in the mammals that feed on crabs or crayfish. water and survives for around 24 hours. Further Paragonimiasis in man is limited to areas where development takes place inside various operculate dietary customs allow infection. P. westermani freshwater snails (Semisulcospira libertina, S. amur- infections occur mainly in China, Japan, Korea, the ensis, Thiara graniJera, Oncomelania nosophora). Philippines and Taiwan-with cases also reported Asexual multiplication, taking 3 months, occurs in the from India, Indonesia, Malaysia, Thailand, and snail so that a few hundred of the emerging larval stage Vietnam. Other Paragonimus species occasionally (cercariae) are formed from each miracidium. infect man in Asia, Africa, and Central and South The cercariae can swim in the water for 24-48 hours America (figure 31-1). but require another intermediate host, a freshwater 437 438 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS * PARAGONIMUS ISOLATED CASES Figurc 31-l. Known geographical distribution ofParagonimus. The infection may occur in areas as yet unrecorded -,.- Figure 31-2. An adult Paragonimus westermani under a light nticroscope. Scale bar= 1 millimeter. (Photo: Wellcome Museum of Medical Science) PARAGONIM US AND PARAGONIMIASIS 439 edible crab or crayfish. This second intermediate host Major reviews of paragonimiasis include those by lives mainly in fast-flowing mountain streams, Yokogawa (1964, 1969) and Yokagawa, Cort and although some species can be found in rivers and rice Yokogawa (1960). Other accounts of paragonimiasis fields. The parasites form encysted metacercariae in the include those from Africa (Nwokolo 1974), Cameroon muscles or gills of the crustaceans and reach a new (Sachs and Voelker 1975; Sirol, Kerfelec and mammalian host when crabs or crayfish are eaten raw. Papinutto 1967), China (Chung and others 1975; Fan, The cysts hatch in the duodenum, and the young flukes Zihe and Daixia 1976), Costa Rica (Miyazaki 1974), migrate through the peritoneal cavity and diaphragm Indonesia (Kwo and Miyazaki 1968), Ivory Coast to the lungs, reaching maturity 5-6 weeks later and (Nozais and others 1980), Japan (Katamine and others living for 6-20 years. 1970, 1972; Sano and others 1979; Yoshida 1916), Laos (Soh 1973), Liberia (Voelker 1973), Malaysia Prepatent and incubation periods (Miyazaki and Kwo 1969; Rohde 1967), Mexico (Martinez-Baez 1970), Nigeria (Nwokolo 1972; Worms reach maturity 5-6 weeks after encysted Voelker and Nwokolo 1973), North America (Ameel metacercariae in freshwater crustacea are ingested. 1934), Panama (Miyazaki 1972), Peru (Miyazaki and Symptoms develop over longer and variable periods. Grados 1972), Philippines (Cabrera 1973; Cabrera and Fevidal 1974; Cabrera and Vajrasthira 1972, 1973), Period of communicability South Korea (Kim and Bang 1974; Rim and others 1975; Sadun and Buck 1960; Yun and others 1966), Sri The adult worm can live between 6-20 years and can''.' produce eggs all this time, but worms normally become Lanka (Kannangara and Karunaratne 1969), Taiwan walled off after 1-2 years, and very few eggs are passed. (Huang and Chiu 1966; Huang and others 1966; Liu 1970; Liu and Cross 1971), and Thailand (Miyazaki and Vajrasthira 1967). Resistance Susceptibility is general. Increased resistance pos- sibly develops as a result of infection. Control Measures Epidemiology Mass chemotherapy with bithionol has been The distribution of paragonimiasis in man is effective in Japan and the Philippines. determined by numerous factors-especially by the In areas where the zoonotic reservoir is more presence of particular snails and crustacean hosts in important in maintaining transmission than the human local streams and by dietary customs that include reservoir (because it is primarily animal feces that eating the crustaceans in a raw or semicooked state. reach the stream where the intermediate hosts reside), Infection is not only associated with eating raw or excreta disposal programs may not greatly reduce pickled crabs and crayfish, but also with eating crab or transmission. In areas, such as parts of Japan, where crayfish juices, which are popular in parts of China, the human reservoir is important in maintaining Korea, the Philippines and elsewhere. The encysted transmission, any measures that prevent untreated metacercariae are sticky and can contaminate knives, human excreta from reaching surface waters should chopping boards, hands, and vegetables in the kitchen reduce the prevalence of infection in snails and may while crabs or crayfish are being prepared. As with reduce infection in crabs and humans. clonorchiasis, infection is generally more common in Another important approach to paragonimiasis adults than in children and in males than in females. control is to attempt to change human habits of This is due to different dietary customs. consuming raw or insufficiently cooked crabs and In some endemic areas the crab and crayfish hosts crayfish. Infection often occurs when uncooked soft live in mountain streams that are some distance from parts (such as leg muscles) are eaten raw. Pickling in human settlement. It is likely that they become infected brine, vinegar, or wine will not kill the encysted chiefly as a consequence of the contamination of these metacercariae, but heating for 10 minutes in water at streams by animal, rather than human, feces. In such 55°C is effective. Educational campaigns should inform situations the eggs passed in human feces may be the public of the danger of eating raw or insufficiently unimportant in maintaining transmission; therefore cooked crabs and crayfish and explain the possibility of excreta disposal programs are irrelevant as an initial infection through contamination of kitchen utensils control strategy. while preparing infected crabs. 440 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Occurrence and Survival in the Jotonal of' Tropical Medicine and Public Healtlh, 3, Environment 446-448. (1973). Endemicity of Paragoninmus siamensis Miyazaki and Wykoff 1965, the second species of lung Paraonimu raeggs devlo ost rapidlytin werkat fluke found in the Republic of the Philippines. Southeast Eggs20C, and miracidia ht out inrabou 3 weks Asian Journal of Tropical Medicine and Public Health, 4, Eggs are quickly killed by freezing but survive for long 509-518. periods at 4°C. Eggs do not develop at temperatures Chung, H. L., Ho, L. Y., Tsao, W. C., Hsu, C. P. and Kao. P. above 35°C and are rapidly killed by desiccation C. (1975). On the metacercariae of some Paragoninuis-spp (Yokogawa, Cort and Yokogawa 1960). Paragonimus and other trematodes found in Chinese fresh water crabs. eggs in a biogas plant in China survived for 13 days Acto Zoologica Sinica. 21, 155-168. (Hou and others 1959). Fan, P., Zihe, Z. and Daixia, C. (1976). Observations of the Encysted metacercariae can live for one week in the incidence for metacercariae of Paragonimus in crabs in Xi tissue of dead crabs at cool temperatures. Traditional county Anhui Province. Acta Zoologica Sinica, 22, 84-88. methods of preparing crabs-such as soaking in a Hou, T. C., Chung. H. L., Ho, L. Y. and Weng, H. C. (1959). weak solution of salt, rice wine and spices-do not kill Achievements in the fight against parasitic diseases in New weak solutacererio of sal rice China. Chiniese Medical Journal, 79, 493-520. all metacercariae (Khaw 1935). Chemical treatments Huang, W. H. and Chiu, J. K. (1966). Epidemiologic studies are also not reliable (Tsuda 1959). Metacercariae are of Paragoni7nus wiestermani (Kerbert, 1978) and related rapidly killed above 50°C, and so most techniques of species in Taiwan (Formosa). lI. Seasonal variations in the cooking, or dipping in boiling water, should destroy incidence of Paragonimns westermani infection in Eriocheir encysted larvae in the tissues of crabs and crayfish. japonicus. Journal of the Formosan Medical Association, 65, 529-535. Huang, W. H., Chiu, J. K., Lu, S. C. and Chen, H. H. (1966). Epidemiologic studies of Paragonimnus westermani Inactivation by Sewage Treatment (Kerbert, 1878) and related species in Taiwan (Formosa). Processes 1. Distribution patterns of Paragonimus westermani metacercariae in Erioclheir crabs. Journal of'the Formosan Medical Association, 65, 141-152. No specific data are reported. Kannangara, D. W. W. and Karunaratne, G. M. S. (1969). Paratelphusa cevloncnsis and Paratelphusa r ugosa as crab hosts of the human lung fluke Paragonimus westermani Inactivation by Night Soil and Sludge (Kerbert, 1878), in Ceylon. Ceylon Journal of Medical Treatment Processes Science, 18, 31-32. Katamine. D., Imai, J., Aoki. Y. and Nojima, H. (1972). An No specific data are reported. epidemiological survey of paragonimiasis in Hata district, Kochi Prefecture. Tropical Medicine, 14, 186-197. Katamine, D., Imai, J., Aoki, K., Nojima, H., Murakami, F., Hamada, Y. and Kanda, S. (1970). A study on Literature Cited paragonimiasis in Shimanto river area Kochi Prefecture. Japanese Journal of Parasitology, 19, 348-349. Ameel, D. J. (1934). Paragonimus, its life history and Khaw,O.K.(1935).In ritroexperimemtsontheviabilityand distribution in North America and its taxonomy excystment of Paragonimus cyst. Proceetlings of the Society (Trematoda: Troglotrematidae). American Journal of tor Experimental Biology and Medicine, 32, 1003-1005. Hygiene, 19, 279-317. Kim, J. S. and Bang, F. B. (1974). A follow-up study to Cabrera, B. D. (1973). Studies on Paragonimufs and evaluate the efficacy of mass chemotherapy for control of paragonimiasis in the Republic of the Philippines. I. paragonimiasis. Korean Journal of Parasitology, 12, 8-13. Paragonimus metacercariae infection in Parathelphusa Kwo, E. H. and Miyazaki. 1. (1968). Paragonimus westermani grapsoides. Sourtheast Asian Journal of 'ropical Medicine (Kerbert. 1878) from tigers in North Sumatra, Indonesia. and Public Health. 4, 55-62. Journal of Parasitology, 54, 630. Cabrera, B. D. and Fevidal. P. M. (1974). Studies on Liu, J. C. (1970). Epidemiological characteristics of Paragonimus and paragonimiasis in the Philippines. III. paragonimiasis westermani in Taiwan. Chinese Journal oj Prevalence and treatment of human paragonimiasis with Microbiology, 3, 149. bithionol in Jaro. Leyte, Philippines. Southeast Asian Liu, J. C. and Cross. J. H. (1971). Paragonimiasis westermani Journal of Tropical Medicine and Public Health, 5, 39-45. among rural school children in Taipei County, Taiwan. Cabrera, B. D. and Vajrasthira. S. (1972). Occurrence of the Chinese Jour nal of Microbiology, 4, 97-105. lung fluke Paragonimus siamnensis Miyazaki and Wykoff Martinez-Baez. M. (1970). Paragonimiasis in Mexico. 1965, in the Republic of the Philippines. Southeast Asian Gaceta Medica de Mexico. 100, 136. PARAGONIMUS AND PARAGONIMIASIS 441 Miyazaki, I. (1972). Occurrence of the lung fluke, (1979). Epidemiological studies on the lung fluke in Paragonimus peruuianus, in Panama. Journal of Shizuoka Prefecture. 2. Discovery of a freshwater snail, Parasitology, 58, 841-842. Saganoa sp., as a first intermediate snail host of (1974). Occurrence of the lung fluke, Paragonimus Paragonimus miyazakii. Japanese Journal of Parasitology, peruvianus in Costa Rica. Japanese Journal of Parasitology, 28, 21-2t17. 23, 280-284. Sirol, J., Kerfelec, J. and Papinutto, J. P. (1967). Pulmonary Miyazaki, I. and Grados, 0. (1972). Occurrence of the lung paragonimiasis in Africa. Apropos of 26 cases collected in fluke, Paragonimnus caliensis, in Peru. Journal of Western Cameroon. I. Statement of the parasitologic, Parasitology, 58, 1210-1211. anatomopathologic, epidemiologic and clinical facts. Miyazaki, I. and Kwo, E. H. (1969). Potamiscus cognatus Bulletin de la Societe de Pathologie Exotique et de ses (Roux, 1936), a new crab host for Paragonimus westermani Filiales, 60, 533-543. in Malaysia, Journal of Parasitology, 55, 459. Soh, C. T. (1973). Epidemiological investigation of Miyazaki, I. and Vajrasthira, S. (1967). Occurrence of the Paragonimus infection in Laos. Yonsei Reports on Tropical lung fluke Paragoni7nus hieterotremus Chen et Hsia, 1964, Medicine, 4, 65-77. in Thailand. Journal of Parasitologv, 53, 207. Tsuda, M. (1959). Biological studies on Paragonimus Nozais, J. P., Doucet, J., Dunan, J. and Assale N'Dri, G. uestermani. 2. On the resistance of the metacercariae of (1980). Les paragonimoses en Afrique Noire. A propos Paragonimus westermani. Japanese Journal of d'un foyer recent de Cote-d'Ivoire. Bulletin de la Societe de Parasitology, 8, 812-821. Pathologie Exotique et de ses Filiales, 73, 155-163. Voelker, J. (1973). Morphological taxonomical studies on Nwokolo, C. (1972). Endemic paragonimiasis in Eastern Paragoniiiinu.s uterohikateralis (Trematoda, Troglo- Nigeria: clinical features and epidemiology of the recent trematidae) as well as observations of the life cycle and the outbreak following the Nigerian civil war. Tropical and spread of the parasite in Liberia. Zeitschrift fur Geographical Medicine, 24, 138-147. Tropenmedizin und Parasitologie, 24, 4-20. (1974). Endemic paragonimiasis in Africa. Bulletini of Voelker, J. and Nwokolo, C. (1973). Human paragonimiasis the World Health Organization, 50, 569-571. in Eastern Nigeria caused by Paragonimus uterobilateralis. Rim, H. J., Lee, J. S., Chung, H. S., Hyun, I. and Jung, K. H. Zeitschrift fuir Tropenmedizin und Parasitologie, 24, (1975). Epidemiological survey on paragonimiasis in 323-328. Kang-hwa-gun, Korea. Korean Journal of Parasitology. Yokogawa, M. (1964). Paragonintus and paragonimiasis. In 13, 139-151. Progress oJ Medical Parasitology in Japan, vol. 1, eds. Rohde, K. (1967). The distribution of Opisthorchis and Morishita, K., Komiya, Y. and Matsubayashi, H., pp. Paragonimus in Malaya and possible sources of infection of 61-156. Tokyo: Meguro Parasitological Museum. man with these parasites. Zeitschrili uiir TropenmnediZin (1969). Paragonimus and paragonimiasis. Advances in und Parasitologie, 18, 152-161. Parasitology, 7. 375-387. Sachs. R. and Voelker, J. (1975). A primate, Mandrillus Yokogawa, S., Cort, W. W. and Yokogawa, M. (1960). leucophaeus, as natural host of the African lung fluke Paragonimus and paragonimiasis. Experimental Paragonimus africanus in West-Cameroon. Tropenmedizin Parasitology, 10, 81-137 and 139-205. und Parasitologie, 26, 205-206. Yoshida, S. (1916). On the intermediate hosts of the lung Sadun, E. H. and Buck, A. A. (1960). Paragonimiasis in South distome P. weslermani Kerbert. Journal of Parasitology, 2, Korea-immunodiagnostic, epidemiologic, clinical, roent- 111-117. genologic and therapeutic studies. American Journal of Yun, D. J., Lee, K. Y., Ahn, Y. K. and Lee, Y. H. (1966). Tropical Medicine and Hygiene, 9, 562-599. Environmental studies on paragonimiasis in Korea. Yonsei Sano, M., Ishii, A., Kino, H., Hayashi. M., Fujio, Y. and Ito. J. Medical Journal. 7, 64-75 32 Schistosoma and Schistosomiasis SCHISTONIASIS is one of the major parasitic and are responsible for transmission to other persons diseases of man. It affects many countries and, as well as for damaging the tissues through which they especially in Africa, it has increased in importance pass. The majority of eggs are retained in the body, following the development of manmade lakes and either in the bowel and bladder wall, or are carried to irrigation schemes. the liver, where many become stuck in the blood vessels, or to the lungs and even the brain or spinal cord on occasion. An impacted egg induces a chronic Description of Pathogen and Disease inflammatory response around it; the size of reaction depends in part on acquired immune responses. The literature on schistosomiasis is truly volu- Gradually the egg becomes calcified (especially in the minous, and only a brief summary of the salient bladder wall) or destroyed. features can be given here. A series of major abstracted Escaping eggs cause tissue damage with loss of blood bibliographies, most recently Hoffman and Warren and protein into the urine (where it is obvious) or feces. (1978), provides an invaluable guide to the literature The heavier the infection, with more eggs being passed, on schistosomiasis for those wishing to study the greater the blood loss, and up to thousands of particular aspects in greater detail. worm pairs have been found at autopsy. With an inflamed bladder wall, caused by the passage of S. 1taematobium eggs, urine is passed frequently and Identification painfully. Growths in the bladder lining may occur, Schistosomiasis, known in the older literature and in and they or the schistosome eggs act as nuclei for the common usage as bilharziasis, comprises infections of formation of urinary stones. In a few people infected the venous system by several species of the trematode with S. hlaeM1atobiurn?, bladder wall damage leads on genus Schistosoma. One species, S. haematobium, to cancer and death. Reactions to retained eggs may inhabits the veins around the bladder (urinary block the escape of urine from the kidneys to the bladder schistosomiasis), whereas the others predominantly in up to 20 percent of infected children, and the resulting involve the portal venous system that transports blood back pressure may damage or even destroy the kidney. from the intestines to the liver (intestinal schistoso- Where this is bilateral, renal failure and death follow, miasis). The most important species of intestinal but the ureteric lesions of a fair proportion of patients schistosome are S. mansoni and S. japonicum: S. are reversible with chemotherapy. intercalatum is similar to these but has a localized The intestinal schistosomiases (S. mansoni and S. distribution in West Africa. japonicum) cause occult bleeding into the bowel, The range of disease produced in infected individuals papillomata of the bowel wall, and, in heavy infections, is very great. Infection is through the skin and may be bouts of dysentery with passage of blood. The brunt of accompanied by itching and skin inflammation. Early damage falls on the liver, and although all cases have development in the lungs may give rise to marked fever scattered reactions to impacted eggs, in a proportion and respiratory symptoms. The adult worms in the (usually small but reaching 23 percent in one veins give rise to few disorders; the problems arise from community) there is a proliferation of fibrous tissue to the eggs, of which each female worm lays hundreds, or produce a fibrous liver. A fibrous liver may function thousands in the case of S. japonicuni, daily. A badly, leading to hepatic coma, but more usually the proportion of these escape into the bowel or bladder main effect is a back pressure on the blood supply, with 443 444 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS great enlargement of the spleen and a series of bypasses dren of urinary schistosomiasis may often exceed 80 developing that return blood to the heart other than percent, and this level is reached at a later age for S. through the liver. Such blood vessels above the mansoni. Worm loads in a few people will be in the stomach may burst and give rise to profuse bleeding thousands, although the majority will be less heavily from the mouth, which may be lethal. Yet other eggs infected. The proportion going on to progressive may reach and damage the lungs or the nervous disease will vary with intensity of infection. It may be system, but a swollen abdomen with ascites from the locally up to 25 percent, but a lower proportion is liver damage is more frequent. These life-threatening usual, and of these only some will die of liver or urinary complications occur mostly in the heavily infected, but tract disease, most of them during early to middle adult even light infections give rise to lassitude in many life. patients. Others may have few or no symptoms, although even some of these, if heavily infected, have decreased ability to do physical work (Awad El Karim Infectious agents and others 1981) and impaired growth in childhood. The schistosomes are digenetic trematodes in which Diagnosis is by the identification of Schistosoma eggs the sexes are separate and differ in size and shape. The in the feces (for S. mansoni and S. japonicum infections) broader males are around 10 millimeters in length, and or in the urine (for S. haematobium infections), the slender female normally lies enclosed by the folded Serological techniques for diagnosis are also available body of the male (figure 32-3). The several species that and are useful in mass surveillance in support of infect man are most readily distinguished by the shape control programs (see. for instance, McLaren and of their eggs: those of S. haematobium and S. others 1979). Treatment of infections is by drug intercalatum have a terminal spine, whereas S. mansoni therapy, and great advances in drug development have eggs have a lateral spine, and S. japonicum eggs are been made in recent years. Hycanthone or oxam- rounded with a small knob. Several more or less closely niquine are often used for S. mansoni infections; related blood flukes infect domestic animals and birds. hycanthone. niridazole, or metrifonate for S. haemat- The bird schistosomes can give rise to dermatitis in obium; and niridazole for S. japonicum. Praziquantel, a bathers in temperate climates. newer drug still undergoing field trials, is effective against all three schistosome species. Reservoirs Man is the effective reservoir of S. hlaenzatobium and Occurrence S. mansoni. Though wild animals may become infected Human schistosomiasis is found in many parts ofthe with S. mansoni and one small epidemic was traced to tropics, with some 200 million cases in all. Unlike most infected baboons, they may for practical purposes be other infections, it has been steadily spreading and disregarded. S.japonicum is a zoonosis, however, and in increasing in intensity over much of its range for some fact the Taiwan strain is noninfective to man and decades, as a result of water impoundments for power entirely transmitted between animals. Elsewhere, a and agriculture and the development of irrigated variety of domestic animals -dogs, cattle, water farming. Urinary schistosomiasis (due to S. haemat- buffaloes, and rats-act as reservoirs of infection, obium) occurs throughout the inhabited parts of Africa although man is still usually responsible for the and is particularly common in the Nile valley. It majority of transmission, it is likely that it would extends into irrigated and other parts of the Middle continue, albeit at a lower level, in his absence. East, with small foci in South Asia and Europe (figure 32-1). S. mansoni is widespread in Africa and in Brazil and other countries of northeast South America, with a patchy distribution in the Caribbean (figure 32-2). Of the other intestinal schistosomiases, S. intercalatum has Each paired female worm of S. mansoni and S. a restricted distribution in central West Africa, whereas haernatobiumi lays some hundreds of eggs daily, but S. S.japonicum occurs in the Philippines. Sulawesi, China, japonicum lays thousands. The eggs are large, some 140 and other parts of Southeast Asia and was formerly micrometers in length, and elongated. The proportion important in Japan (figure 32-1). A closely related form that escape. which may be as low as 20 percent, pass is found along the Mekong River. through the tissues into the urine (S. haeniatobilan) or Within endemic areas the prevalence in schoolchil- feces (other species). Although they take several days to SCHISTOSOMA AND SCHISTOSOMIASIS 445 -_ m S.haematobium S .japonicum Figure 32-1. Known geographical distribution ofSchistosoma haematobium and S.japonicum. The infections may occur in areas as yet unrecorded. S. haematobiumn transmission is most unlikely at altitudes above 1,500 meters - w S.mansoni Figure 32-2. Known geographical distribution of S. manosni. The infection may occur in areas as yet unrecorded. S. mansoni transmission is most unlikely at altitudes above 2,000 meters 446 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS '7/1 7.I_ .X~~~~~~~~~~~~. Figure 32-3. A male and Jemale S. mansoni undei scanning electronmicroscopy. The slender female (10-20 millimeters long and 0.16 millimeters wide) lies in a groove in the body of the sturdier male (6-12 millimeters long and 1.1 millimeters wide) and can be seen protruding at one end. Scale bar = 1 millimeter. (Photo: M. M. Wong, Primate Research Center, University of California, Davis, California, USA) develop after being laid by the female, by the time they 48 hours in the water, swimming to the surface and then pass out of the body with the excreta they are mature slowly sinking during rest periods, but on encountering and ready to hatch. After the worms have died or been human skin they rapidly penetrate it and, after killed by therapy, a few dead and calcified eggs may migrating to the lungs where they develop for some continue to be excreted over months or years, but these days, they move to the portal venous system of the liver are not hatchable. to mature and pair before migrating to the intestinal and The eggs hatch when osmotic pressure of the vesical blood vessels. surrounding medium falls, as when they reach water, The snail hosts vary by region, and the schistosomes and light and warmth speed hatching. The egg shell are very species specific. The principal genera of snails splits, and a motile ciliated larva called a miracidium that act as host for the main species of schistosomes emerges and scans the aquatic snail environment for up are: to 6 hours. On encountering a suitable species of aquatic snail, the larva penetrates it and undergoes a Biomphalaria for S. mansoiii series of developmental stages. Between 1 month and 3 Oncomelania and months later, depending on the temperature and on the Tricula for S. japonicum species of snail, further aquatic larvae called cercariae begin to emerge from the snail. The pattern varies from The hosts of S. japonicum are amphibious and leave the less than a dozen each day for many months for S. water for muddy canal-banks from time to time. The japonicum in Oncomelania quadrasi to nearly a snail hosts of other schistosomes are truly aquatic, thousand daily from S. mansoni in Biomphalaria although many, even if infected, can survive a dry glabrata, though in the latter case the snail may only season by burrowing into the drying mud of a seasonal survive two weeks of shedding cercariae. These live up to pond. Still or gently flowing water favors the snails, as SCHISTOSOMA AND SCHISTOSOMIASIS 447 does a high calcium content of water, neutral or Epidemiology alkaline pH, and aquatic vegetation. Where scattered The epidemiology of schistosomiasis is a complex families use separate ponds for water supplies the and much studied subject, and space does not permit a infection can be highly focal, but cercariae may be full discussion here. In a given locality, schistosome carried many meters in flowing water to fect dynamics depend upon both the macroecological downstream settlements. effects of topography, hydrology, water quality, Although people may become infected through the settlement patterns, agriculture, sanitation, human mucosa of the mouth when drinking water, the bulk of behavior, snail behavior, and the microecological infections are acquired through water contact with the factors of host-parasite relationships in man and in the skin. snail. The total system is complex, and many gaps in scientific understanding remain, particularly on the Prepatent and incubation periods role of immunity in natural infections. Attempts to construct mathematical models of transmission, and The shortest times recorded between cercarial thus to predict the impact of alternate control penetration and the appearance of S. mansoni eggs in strategies, have been mathematically sophisticated but the excreta are j ust over a month, but 2 months is more of limited usefulness. usual, and a longer period is normal for the other For successful transmission, man must live near to schistosome species. An incubation period cannot be bodies of surface water that have the characteristics stated because symptoms may develop gradually, or (temperature, chemistry, pH, plant life, velocity) not at all, depending on the number of schistosome necessary to support the appropriate species of snail. worms infecting and the immune status of the host. For transmission from man to snail to take place, fresh human excreta (urine for S. haematobium and feces for Period of communicability other species) must reach these bodies of water where the snail colonies are living. This may happen owing to Once mature worm pairs are established, they may promiscuous defecation, urination while near or in persist and continue laying eggs for a long time, and water, or to the discharge of untreated sewage into worm survival for 30 years is documented. However, water. Finally for transmission from snail to man to the majority of worms die sooner, and a half-life of 3 to take place, there must be a pattern of behavior in the 6 years is probable, though evidence of even shorter community that causes people to enter regularly those survival is appearing (for instance, Goddard and surface waters that harbor the snails and have been Jordan 1980). In endemic areas, the relative import- polluted by the excreta. ances of prolonged worm survival and superinfection In most communities where schistosomiasis is are not yet well defined. The eggs, once excreted, may endemic, prevalence and intensity of infection are persist for weeks or months, as discussed below, but highest in the 5-20 age group. This age group is likely hatch promptly in water and have only a few hours of to be heavily exposed during play or bathing and life thereafter unless a snail is found. possibly also when performing household tasks such as collecting water, tending water buffalo, fishing, or Resistance helping a parent in the fields. Adults are exposed to infection while working in irrigated fields, fishing, Most, if not all, people are susceptible to collecting water, washing clothes, bathing, or any other schistosomiasis, although some races may be more activity involving water contact. susceptible to the severer forms than others. Acquired Different patterns of work may cause differences in resistance due to natural exposure to infection is well schistosomiasis prevalence. Thus, in a village in the documented in several animal species and is clearly Nile Delta (Egypt) women who consistently worked in indicated to occur in human S. haematobium and S. the fields had a schistosomiasis prevalence similar to japonicum infections. The evidence in S. mansoni is men, whereas women who worked exclusively around equivocal. Acquired immunity is certainly incomplete, the home had an appreciably lower rate of infection and its importance in the natural history of the (Abdel-Wahab and others 1980). Another study in infections in communities is not well defined. Peak Egypt (Farooq and others 1966) showed that, for infection loads are usually seen around tha age of 10 males, there was an increased prevalence of S. mansoni years in S. haematobium and a little later in S. among fishermen, water carriers, and washermen and japonicum; egg output declines thereafter even where an increase in S. haematobium infection among water contact persists. boatmen. 448 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS The transmission of schistosomiasis can be highly that piped water supplies and clothes washing facilities localized both in time and space. Regular seasonal in the villages might reduce water contact for females, variations can be due to temperature if there is a winter but would not affect the recreational activities of males period when snail populations decrease and it is too or the time they spend around canoes in the shallow cold for schistosomes to develop outside their human water at the lake edge. hosts. Seasonality of transmission can also be due to Excretion behavior studies are more difficult to rainfall and surface water hydrology. High rainfall may carry out than water-contact studies, and there is, as wash out snail habitats or swell rivers to a point where yet, little information on this important aspect of water contact is reduced and cercarial concentrations schistosomiasis epidemiology. Studies in the Gezira are greatly diluted. More usually, dry periods eliminate irrigation scheme in the Sudan by Cheesmond and ponds and streams completely. It is common in Africa Fenwick (1981) found that 46 percent of all observed for S. haematobium transmission to take place in ponds acts of excretion took place before 9.00 AM. Men and and waterholes in the wetter seasons, reaching a peak women squatted in the open to urinate, although as water bodies shrink and man-water contact women did not urinate in sight of men. Nearly all becomes more focal in the early dry season, but ceasing observed urination was onto soil, not into water, later when the ponds dry up and the snails estivate in although children may have urinated unseen while the mud and await the next rains. immersed in water. Privacy was the prime determinant Focal transmission occurs if it is associated not with of defecation site. 93 percent of defecations took place surface water bodies in general but with certain specific in the fields in cotton, sorghum, or among trees. Only streams or ponds that are polluted by excreta, that 31 percent of people washed themselves after excretion support the correct snail species, and that are visited by and only 7 percent washed their anal region directly people for play or work. Thus, as mentioned above, S. into a water body. This study, unlike some others, haematobium transmission may largely take place at found that privacy was more important than closeness one or two sites in or near a village. The correct to water in determining defecation sites and that most identification of these sites is essential to the design of observed excretion could not lead to the entry of control programs. schistosome eggs from urine or feces into canals or Two aspects of human behavior are integrally linked other water bodies. with the epidemiology of schistosomiasis: water- A study of excretion behavior was carried out in the contact behavior and excretion behavior. Water- Nile Delta (Egypt; Farooq and Mallah 1966). Children contact behavior has been increasingly studied over the under 10 years played frequently in water and often past decade, and these studies are a rare and urinated while doing so. Both sexes and most ages encouraging example of the value of collaboration usually urinated and defecated within 2 meters of between sociologists and epidemiologists. water. Boys commonly urinated directly into water. A water-contact study, in an area of northern Adult males performed ablution after defecation by Nigeria heavily infected with S. haematobium, showed squatting close to the water's edge and splashing water that most contact with water at a dam site took place and washing with the left hand. Adult females who during fishing, bathing, swimming, and playing (Tayo, defecated in the open did so early in the morning or Pugh and Bradley 1980). The great majority (94 after sunset and did not perform ablution. Although percent) of all water contacts observed involved males, females had more frequent water contact than males, because females were relatively secluded in this Muslim males were observed to contaminate water 5 times society. Schistosomiasis prevalences were much higher more frequently than females, and those girls polluting among males than females in the area. Peak water- were mostly under the age of frequent schistosomal contact activity occurred in the afternoon: the time of infection. peak urinary egg output and peak cercarial shedding The contamination of surface waters by excreta, and by infected snails. the subsequent infection of snails, occur not only as a Water-contact studies on the shore of Lake Volta result of promiscuous defecation but also because of (Ghana), another S. haematobium area, showed that the discharge ofinadequately treated sewage. In Minas women were most exposed during domestic tasks such Gerais (Brazil) the effluent from a septic tank was as water fetching and clothes washing and that men entering a stream, and 65 percent of Biomphalaria were most exposed during swimming, bathing, and glabrata less than 10 meters from the sewage outfall, 15 entering canoes (Dalton and Pole 1978). Overall, males percent of those snails between 90 and 100 meters from had more water contact and higher intensities of the outfall, and no snails 200 meters away were infected schistosomiasis infection than females. It is pointed out (Paulini 1964). In addition, snail density was much SCHISTOSOMA AND SCHISTOSOMIASIS 449 greater near the outfall because some snail species have associated with a rise in S. mansoni prevalence and a fall a preference for polluted waters (see also Watson in S. haematobium prevalence (Abdel-Wahab and 1958). A similar situation in South Africa is reported by others 1979). Bayer (1954). Although schistosomiasis is primarily a rural disease, urban communities are also infected. Transmission may take place in urban streams, borrow Control Measures pits, or ponds, or it may be due to urban people leaving town for recreational or agricultural purposes and Schistosomiasis control is at present in a state of flux. becoming infected in the countryside. A survey of During the 1960s the only control method shown to be residents in San Juan (Puerto Rico) showed that effective was application of molluscicides to host snails, swimming and fishing were the main reasons for water but more recently control programs have used several contact and that these activities took place in streams methods simultaneously and at high cost. Chemo- throughout the island. Most water contact involved therapy is likely to play an increasing role in the future. the 5-19 age group but was not associated with socioeconomic status (Lipes and Hiatt 1977). In a working class suburb of Sao Paulo (Brazil), where thirty locally acquired infections of children with S. Individual mansoni and three infected Biomphalaria tenagophila Until recently, there was no drug suitable for mass were detected, the sites of transmission were two borrow pits used as communal bathing pools, chiefly chemotherapy on a large scale. The antimonial by children (Rodriques and Ferreira 1966). compounds used to treat schistosomiasis were toxic Schistosomiasis is closely related to surface-water and required repeated intravenous or intramuscular hydrology and irrigated agriculture and is therefore injections spread over up to a month. Now there are sensitive to the development of manmade lakes and several oral schistosomicides available, and others are irrigation schemes. The typical experience has been undergoing trial. Metrifonate, only active against S. that major irrigation and lake development projects in haematobium, causes negligible side effects and costs areas of endemic schistosomiasis have increased the little. Two or three spaced doses are required. A single prevalence and intensity of this infection among the dose of oxamniquine treats S. mansoni, has few side local population. There are well documented cases of effects, but is expensive. The chemotherapy of S. this from Egypt, Ghana, Iran, Nigeria, Sudan, japonicum is unsatisfactory. A long course of niridazole Tanzania, Zambia, Zimbabwe, and elsewhere is needed, with indifferent cure rates, but a very (Rosenfield and Bower 1979). The development of the promising drug (praziquantel) is under field trial. Mass lakes and the irrigation and drainage canals increases chemotherapy can now reduce prevalence and the number of habitats for snails; the development of intensity of infection greatly; the duration of the irrigated agriculture and fishing increase the frequency reduction is limited (Costa, Katz and Dias 1980), and and duration of water contact; the increased accompanying transmission control measures are availability of surface water for recreation also necessary. Advantages of chemotherapy are its increases water contact; population densities rise to immediate effects on worm load and the disease in man. take advantage of the new agroeconomic opportu- Cost is the chief defect, except for S. haematobium, and nities; and the fecal contamination of the surface water the cooperation of the population may be difficult to is assured by the general poverty of the local sustain in the long term. communities and the lack of concurrent sanitation programs. All these factors contribute to rising transmission rates leading to rising infection rates and, Environmental ultimately, to more frank disease. In some areas, the ecological changes caused by lake The intermediate host snails may be controlled and irrigation development may not only increase either by rendering the habitat unfavorable to them or schistosomiasis transmission but may also affect the by the use of molluscicides. Environmental control has type of schistosomiasis that is dominant. Thus, in some been most dramatically used against hosts of S. villages in the Nile Delta (Egypt) the major changes in japonicum: in Japan, where irrigation canals were lined hydrology and agriculture that have followed from the with concrete; in China, where labor-intensive construction of the Aswan High Dam have been methods of resiting canals and burial of the snails in the 450 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS old canal were used; and in the Philippines, where it Empirical testing of excreta disposal, when facilities are was shown that improved methods of irrigated field used, as a sole means of schistosome control is lacking. management both raised the production of rice and In general, one would doubt its efficacy, but as a reduced the host snail populations in the fields. For the concomitant measure with mass chemotherapy to aquatic snail hosts of other schistosomes, such prevent rapid build-up of the worm population after measures as channel straightening, weed clearance, treatment it may have value, provided that those who and intermittent drying out of irrigation canals and "escape" the treatment regimen are not those who also drains have limited snail numbers. Biological control fail to use excreta disposal facilities. Children below of snail populations by competitor species of snails has school age, and males who have recently left school and been shown in small specialized habitats and is claimed become migrants in search of work, are groups of to have a significant effect on a larger scale, but as an particular concern. operational control method has been little used. Three factors mitigate against the efficacy of Molluscicides have a long history, beginning with improved sanitation in schistosomiasis control. First, a copper sulphate, but niclosamide (Bayluscide) and n- single stool or urination may contain many eggs, and a trityl-morpholine (Frescon) are the only ones in single miracidium reaching a snail may give rise to operational use now (McCullough and others 1980). several thousand cercariae. Therefore, the con- They are relatively nontoxic to man, although they tamination of surface waters by excreta may have to be may harm fish and nontarget invertebrates. To achieve reduced to an extremely low level. Second, although it good snail kills the dosage needs careful control, and is possible to improve defecation behavior in some this can best be achieved where irrigation flows are communities and to reduce the contamination of the appropriately managed. There is, as yet, no clear environment by feces, it is very difficult to modify evidence of snail resistance to Bayluscide, even after urination behavior. Therefore, the impact of sanitation prolonged application (Barnish and Prentice 1981). programs on S. haemnatobium is likely to be markedly Although mollusciciding can stop transmission, the less than their impact on S. mansoni and S. japonicum. long survival of adult worms in man implies continuing In addition, S. haematobium egg output is at its the program for many years to maintain control or maximum in the early afternoon (Stimmel and Scott combining the molluscicide program with mass 1956), a time when children are likely to be playing in chemotherapy and improvements in water supply and water and adults to be working in water. Third, those sanitation (Hiatt and others 1980). Apart from altering people in the community excreting most eggs are in the snail habitats, environmental approaches to control age group of 5-20 years. This group is likely to be less consist either of preventing infected excreta from affected by sanitation programs than adults. reaching the snails or of preventing human contact In summary, schistosomiasis control depends upon with infected water. Two control programs (in Brazil a carefully designed mix of chemotherapy, snail and St. Lucia), which provided water supplies, bathing control, water supply, sanitation, and health education or laundry facilities, and attempted to reduce infected (Sandbach 1975; WHO 1980). The nature of this mix water contact, have reduced transmission con- will be different in different places and must arise from siderably, whereas other successful programs have detailed study of the local epidemiology of schistoso- included water supply and sanitation (Barbosa, Pinto miasis. Some bizarre control strategies have been and Souza 1971; Jordan 1977; Jordan and others 1978; suggested, such as the maintenance of crocodile and Jordan and Unrau 1978). hippopotamus populations in Lake Sibaya (Natal, The few recorded attempts to control schistoso- South Africa) to discourage water contact (Appleton miasis by providing excreta disposal facilities alone and Bruton 1979). have been unsuccessful (Scott and Barlow 1938). This Some poor countries have achieved notable progress has been ascribed to people's failure to use the facilities in schistosomiasis control by the sustained application because they were wrongly located -in villages, while of integrated control measures and the mobilization of defecation took place in the fields -or offensive, or ill- popular support and participation. An example is adapted to the cultural tradition or to use by children. China (Anon. 1977; Cheng 1971; Chung 1977; One epidemiological model of schistosomiasis trans- Sandbach 1977). Other countries have achieved mission (Macdonald 1965) has been interpreted as substantial levels of control by specific antischistosome showing that excreta management is inefficient as a measures in the context of rising incomes and control method, even when latrines are used. However, improved socioeconomic conditions. Examples are this results more from the structure and assumptions of Japan, Puerto Rico, and Venezuela (Bhajan and others the model, rather than being a robust conclusion. 1978; Negr6n-Aponte and Jobin 1979; WHO 1973). SCHISTOSOMA AND SCHISTOSOMIASIS 451 Occurrence and Survival in the In feces and night soil Environment The survival of S. mansoni and S. japonicum eggs in The stages of schistosomes found in the environment feces is of epidemiological importance. S. mansoni eggs are eggs, miracidia, and cercariae. Schistosome eggs in feces in South Africa all survived for 3 days, only half are considerably less rugged and long lived than those were hatchable after 6 days, and none after 8 days of Ascaris, Trichuris, or Taenia worms. Schistosome (Porter 1938). Experiments in Puerto Rico showed S. miracidia and cercariae are fragile and must find a snail mansoni eggs survived for over 2 days in formed feces, or vertebrate host within hours or they die. but only 1 day in liquid feces, at 24-32°C. In formed feces at 7-10°C, survival was for over 7 days (Faust and In water Hoffman 1934). Schistosome eggs hatch rapidly on reaching water, ~ S.japonicum eggs in feces may survive for longer than a S. mansoni eggs. Early studies in Japan found that S. Hoffmightand1934; Maldon edo hatcsa MFausti and japonicum eggs in cow dung survived for up to 2-4 Hoffman 1934; Maldonado, Acosta Matienzo and weeks (Miyairi and Suzuki 1913). Subsequent studies Velez Herrera 1950; Miyairi and Suzuki 1913; Standen in Japan showed that S. japonicum eggs in wet rabbit 1951). S.japonicum eggs will not hatch at temperatures feces survived for 20 days at 28°C, 113 days at 18'C, below 3°C or above 38°C, with temperatures of and 180 days at 80C (Ito 1954b) S.japonicum eggs in the 13-28°C being most suitable for hatching (Ito 1953). anaerobic fecal liquor of a biogas plant in China Standen (1951) found the S. mansoni eggs had an survived for up to 14 days in summer, 22 days in optimal temperature for hatching of 28°C. Hatching of survived u o days in summer 22cday in S. manson eggss copreduced at sal06tpes as low as nde5 Stainforth 1978). The addition of urine to the feces, or percent and ceases completely at 0.6 percent (Standen drying to a moisture content of 5 percent, greatly 1951). S. mansoni egg hatching is also inhibited by low reduces S. japonicum egg survival (National Schistoso- dissolved oxygen levels (Kawata and Kruse 1966). miasis Research Comr.ittee 1959). Miracidia swim in the water; if they come close to a snail, they are attracted to it and penetrate. If they do not encounter a snail, they may live for up to 3 days but In urine are probably unable to penetrate a snail after a few For S. haematobium eggs it is survival in urine, rather hours (Faust and Meleney 1924; Miyairi and Suzuki than feces, that affects transmission. Studies on S. 1913; Porter 1938). Experiments on S. douthitti haematobium eggs in urine at room temperature in miracidia showed that mean longevity falls with South Africa showed that 60 percent were hatchable increasing temperature, from 11 hours at 8°C, to 7 after 2 days, 10 percent after 3 days, 4 percent after 5 hours at 20°C, and 1.5 hours at 35°C (Farley 1962). days, and none after 8 days (Porter 1938). Survival Kawata and Kruse (1966) found that S. mansoni times were prolonged at cooler temperatures. Ito miracidia in water at 260C survived for up to 18 hours, (1954b) studied S.japonicum eggs in urine. At 28°C they with a mean of 6 hours. Miracidial survival is enhanced were unhatchable within a day in rabbit urine, 2 days in at pH values of around 7.5. cow urine, and 3 days in human urine. Survival times Schistosome cercariae are shed from the snail into doubled at 18°C and quadrupled at 8°C. the water and must find an appropriate vertebrate host and penetrate. Cercarial survival in water seldom exceeds 2 days and is temperature dependent. S. In sewage japonicum cercariae survive for over 7 days at 5°C and Schistosomiasis is primarily an infection of poor under 4 hours at 40°C (Jones and Brady 1947). As the people in rural areas, and such people typically length of time in the water increases, the ability of a produce no sewage. There are, however, some urban cercaria to penetrate decreases, and it is probable that communities with flush toilets and sewerage systems nearly all cercariae in warm tropical waters lose their where schistosomiasis prevalences are high enough to ability to infect after less than 24 hours. S. japonicum cause a detectable level of schistosome eggs in the cercariae tolerate pH in the range 5.5 to 8.4 (Jones and sewage. An example was San Juan (Puerto Rico), Brady 1947). where raw sewage contained 2 S. mansoni eggs per liter Schistosome cercariae are readily removed from (Rowan and Gram 1959). Jones and others (1947) drinking water by chlorination (Coles and Mann 1971; reported that S. japonicum eggs would not hatch in raw Frick and Hillyer 1965: Wittenberg and Yofe 1938) or or settled sewage, but would hatch in raw sewage by storage for 2 days. diluted to one-quarter strength in water or settled 452 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS sewage diluted to one-third strength. Sewage with a Schistosome eggs entering a pond system will either low oxygen content seriously inhibited hatching and die or hatch but will not be carried through to the reduced the viability of S. mansoni eggs (Kawata and effluent. Those that hatch will liberate miracidia that Kruse 1966). must find a suitable snail host rapidly or die. If the ponds are colonized by an appropriate snail species, some miracidia will encounter snails and penetrate. Inactivation by Sewage Treatment Subsequently numerous cercariae will be shed, but Processes these must reach the outfall and find a human host within about 1 day. In a well-designed pond system, Schistosome egg removal in sewage treatment with an overall retention time of 15 or more days, processes has been little studied but is similar to cercariae will die long before they reach the outfall. Ascaris egg removal (chapter 23). The major difference Workers entering the ponds for maintenance purposes is that many schistosome eggs will hatch during sewage are at risk and need protective clothing. treatment, especially in well-aerated environments Effluent chlorination to the level needed to have a such as activated sludge tanks or maturation ponds. satisfactory effect on excreted viruses (chapter 9) and Hatching promotes schistosome removal because the bacteria (chapter 13) will also inactivate most released miracidium is far more vulnerable than the egg schistosome eggs and all miracidia (Jones and Hummel and must find a suitable snail within a few hours or die. 1947; Mercado-Burgos 1975; Rowan 1964b). Sand Laboratory studies on S. japonicum eggs in sewage filtration of effluents will also remove schistosome eggs, showed settling velocities of over 1 meter per hour for but not all miracidia (Jones and others 1947; Newton, 73 percent of eggs (Jones and others 1947). Bench-scale Figgat and Weibel 1948). trickling filter experiments showed higher removal of S. japonicum eggs at lower loading rates, and many eggs hatched during secondary sedimentation. Most eggs Inactivation by Night Soil and Sludge hatched after 24 hours aeration in a simulated Treatment Processes activated sludge unit (Jones and others 1947). Studies in Puerto Rico showed that 83 percent of S. As with all helminth eggs, schistosome eggs in mansoni eggs were removed during primary sedimen- sewage treatment processes become concentrated in tation and 99.5-100 percent by complete trickling filter the sludge. Schistosome eggs are not long lived in feces, or activated sludge plants (Rowan 1964a). It is possible sludge, or night soil compared with Ascaris. Trichuris, that these very high removal rates were partly caused by or Taenia eggs, and any process that removed these some eggs hatching in the treatment plants and by the other worm eggs will guarantee schistosome egg miracidia not being detected by the method used to destruction. detect eggs in the effluent. However large numbers of S.japonicum eggs did not survive 21 days in sludge at Biomphalaria glabrata snails were exposed for 3-6 16-24°C or 9 days at 29-32°C (Newton, Figgat and hours to the plant effluents, but none became infected; Weibel 1948). S. japonicum eggs in digesting sludge at although in an earlier study done at the same activated 24-30'C survived less than 25 days (Jones and others sludge plant when it was receiving a higher influent egg 1947). Kawata and Kruse (1966) found that 91 percent load B. glabrata snails did become infected by miracidia of S. mansoni eggs would not hatch after only 4 hours in in the final effluent. waste stabilization pond sludge at room temperature, Schistosome eggs, miracidia, and cercariae should again suggesting that S. mansoni eggs are considerably be completely removed by waste stabilization ponds. less robust in the environment than are S. japonicum Laboratory experiments with S. mansoni eggs showed eggs. Normal anaerobic sludge digestion processes that hatching was inhibited, though not prevented, in should therefore eliminate schistosome eggs if operated anaerobic ponds and that hatching proceeded on a batch basis. normally in facultative and maturation ponds. Sludge drying processes do not normally achieve the Miracidia survived for up to 6 hours (mean 2 hours) in very low moisture contents needed to kill schistosome an anaerobic pond and for up to 10 hours (mean 4 eggs by desiccation. Three weeks of sludge drying in hours) in a maturation pond at 26°C. Biomphalaria warm climates should eliminate schistosome eggs glabrata snails survived for up to 42 days (mean 20 irrespective of the moisture content reached (Jones and days) in an anaerobic pond and lived and reproduced others 1947). normally in a maturation pond (Kawata and Kruse Schistosome eggs are readily killed by heating and 1966). are therefore eliminated by well-managed thermophilic SCHISTOSOMIA AND SCHISTOSOMIASIS 453 60- ss - Z ONE ss so- \OF -s 4s_-5AFT -45 40 - -40 35 - 35 o- 30 - - 30 25- X-X .< 2 5 , 20- 20 15- IS 10 - Io 100% dest,t.clio c of Schistoso-so eggs 0- I-,es th-o 1000/ desO,ocioo of hils,o gg -5~~~~~~~~~~~~~~~~~~~~~~~~ -10c 1 .lI1 180 I io 11 oooo 0.01 ~~~0.1 loIEI oe o'doo0 0 lmin Ihour Iday lweek Imonth lye., TIME (HOURS) Figure 32-4. The itifluenzce of time and temperature on Schistosoma eggs. The points plotted are the results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death composting processes. Data on the heat inactivation of note on other areas of Tongaland (Natal, South Africa). schistosome eggs, from Ito (1954a) and other studies, Annals of Tropical Medicine and Parasitology,73, 547-561. are plotted on figure 32-4. Awad El Karim, M. A., Collins, K. J., Sukkar, M. Y., Omer, A. Work in China has shown that schistosome egg H. S., Amin, M. A. and Dore, C. (1981). An assessment of destruction in nanti-schistosomal treatment on physical work capacity. adertion in night soil maybe, promotdbuh Journal of Tropical Medicine and Hygiene. 84, 67-72. addition of urea, calcium cyanamide, or ammonium Barbosa, F. S., Pinto, R. and Souza, 0. A. (1971). Control of bicarbonate (Cheng 1971; National Schistosomiasis schistosomiasis mansoni in a small north east Brazilian Research Committee 1959), and these add to the community. Transactions of the Royal Society of Tropical nitrogen value of the resulting fertilizer. Medicine and Hygiene, 65, 206-213. Barnish, G. and Prentice, M. A. (1981). Lack of resistance of the snail Biomphalaria glabrata after nine years of exposure Literature Cited to Bayluscide. Transactions of the Royal Society of Tropical Medicine and Hygiene, 75, 106-107. Abdel-Wahab, M. F., Strickland, G. T., El-Sahly, A., Ahmed, Bayer. F. A. H. (1954). Schistosome infection of snails in a L., Zakaria, S., El Kady, N. and Mahmoud, S. (1980). dam traced to pollution with sewage. Transactions of the Schistosomiasis mansoni in an Egyptian village in the Nile Royal Society of Tropical Medicine and Hygiene. 48, Delta. American Journal of Tropical Medicine and Hygiene, 347-350. 29, 868-874. Bhajan, M. M., Martinez, V., Ruiz-Tiben, E. and Jobin, W. R. Abdel-Wahab, M. F., Strickland, G. T., El-Sahly. A., El- (1978). Socioeconomic changes and reduction in pre- Kady, N., Zakaria, S. and Ahmed, L. (1979). Changing valence of schistosomiasis in Puerto Rico. Boletin pattern of schistosomiasis in Egypt 1935-79. Lancet, 2, Asociation Medica de Puerto Rico, 30, 106-112. 242-244. Cheesmond, A. K. and Fenwick, A. (1981). Human excretion Anon. (1977). Report of the American Schistosomiasis behaviour in a schistosomiasis endemic area of the Gezira, Delegation to the People's Republic of China. American Sudan. Journal of Tropical Medicine and Hygiene, 84, Journal of Tropical Medicine and Hygiene, 26, 427-462. 101-107. Appleton, C. C. and Bruton, M. N. (1979). The epidemiology Cheng, T. H. (1971). Schistosomiasis in mainland China. A of schistosomiasis in the vicinity of Lake Sibaya, with a review of research and control programs since 1949. 454 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS American Journal of' Tropical Medicine and Hygiene, 20, hatchability of eggs of Schistosomna japonicujm. Japanese 26-53. Journal of Medical Progress, 41, 88-95. Chung, H. F. (1977). How schistosomiasis control work is (1954b). Studies on the survival of Schistosonia run in New China. Chin1ese Medical Journal, 3, 86-94. japonicum in vitro. 5. The viability of eggs of Schistosoina Coles, G. C. and Mann. H. (1971). Schistosomiasis and water japonicuin in the exereta of several hosts. Japanese Jouirnal works practice in Uganda. East African Medical Journal, of Medical Progress, 41, 370-374. 38, 40-43. Jones. M. F. and Brady, F. J. (1947). Studies on Costa. M. F. F. de L., Katz, N. and Dias, J. C. P. (1980). schistosomiasis. Survival of Schistosonma japonicurn cer- Reinfeccao de pacientes em dreas end6micas de esquisto- cariae at various temperatures in several types of water. ssomose mansoni ap6s tratamento especifico. IV. National Institutes of Health Bulletin, 189, 131-136. Observacoes em Belo Horizonte. Rerlista do Instituto de Jones, M. F. and Hummel, M. S. (1947). Studies on Medicina Tropical de Sio Patulo, 22, 97-107. schistosomiasis. The effect of chlorine and chloramine on Dalton, P. R. and Pole, D. (1978). Water-contact patterns in schistosome ova and miracidia. National Institutes of relation to Schistosoina haemnatobium infection. Builletin of Health Bulletin, 189, 173-179. the World Health Organization, 56, 417-426. Jones, M. F., Newton, W. L., Weibel, S. R.. Warren, H. B., Farley, J. (1962). The effect of temperature and pH on the Steinle, M. L. and Figgat. W. B. (1947). Studies on longevity of Schistosomatium douthitti miracidia. Canadian schistosomiasis: the effects of sewage treatment processes Journal of Zoology, 40, 615-620. on the ova and miracidia of Schistosoma japonicum. Farooq, M. and Mallah, M. B. (1966). The behavioural National Institutes of' Health Bulletini, 189, 137-172. pattern of social and religious water-contact activities in Jordan. P. (1977). Schistosomiasis-research to control. the Egypt-49 bilharziasis project area. Bulletin of the World American Journal of Tropical Medicine and Hygiene, 26, Health Organiziation, 35, 377-387. 877-886. Farooq, M., Nielsen, J., Samaan, S. A., Mallah, M. B. and Jordan, P., Bartholomew, R. K., Unrau, G. O., Upatham. E. Allam, A. A. (1966). The epidemiology of Schistosoma S., Grist. E. and Christie, J. D. (1978). Further observations haematobium and S. mnansoni infections in the Egypt-49 from St Lucia on control of Schistosoma mansoni project area. 2. Prevalence of bilharziasis in relation to transmission by provision of domestic water supplies. personal attributes and habits. Bulletin of' the W"orld Bulletin of the World Health Organization, 56, 965-973. Health Organization, 35, 293-318. Jordan. P. and Unrau, G. 0. (1978). Simple water supplies to Faust, E. C. and Hoffman, W. A. (1934). Studies on reduce schistosomiasis. Tropical Doctor. 8, 13-18. schistosomiasis mansoni in Puerto Rico. III. Biological Kawata, K. and Kruse, C. W. (1966). The effect of sewage studies. 1. The extra-mammalian phases of the life cycle. stabilization ponds on the eggs and miracidia of Puerto Rico Journial of Public Health and Tropical Schistosoma mansoni. American Journal of Tropical Medicine, 10, 1-47. Medicine and Hygiene. 15, 896-901. Faust, E. C. and Meleney, H. E. (1924). Studies on Lipes, J. K. and Hiatt, R. A. (1977). Determinants of human schistosomiasis japonicum. Amer ican Journal of Hygiene water contact patterns in urban Puerto Rico with special Monograph Series No. 3, 1-339. reference to schistosomiasis. Boletin Asociacion Medico de Frick, L. P. and Hillyer, G. V. (1965). The influence of pH and Puerto Rico, 69, 35-44. temperature on the cercaricidal activity of chlorine. McCullough, E. S.. Gayral, P., Duncan. J. and Christie, J. D. Military Medicine, 131, 372-378. (1980). Molluscicides in schistosomiasis control. Bulletin of Goddard, M. J. and Jordan. P. (1980). On the longevity of the World Health Organization, 58, 681-689. Schistosoma mansoni in man on St. Lucia, West Indies. Macdonald, G. (1965). The dynamics of helminth infections Transactions of the Royal Society of Tropical Medicine and with special reference to schistosomes. Transactions of the Hygiene, 74, 185-191. Royal Society of Tropical Medicine and Hygiene, 59, Hiatt, R. A., Cline, B. L., Ruiz-Tiben, E., Knight, W. B. and 489-506. Berrios-Duran, L. A. (1980). The Boqueron project after 5 McGarry, M. G. and Stainforth, J. (1978). Compost, years. A prospective community-based study of infection Fertilizer, and Biogas Production Jrom Humnan and Farm with Schistosoina mansoni in Puerto Rico. American Wastes in the People's Republic of China. Ottawa: Journal of Tropical Medicine and Hygiene, 29, 1228-1240. International Development Research Centre. Hoffman, D. B. and Warren, K. S. (1978). Schistosomiasis IV. MeLaren, M. L., Long. E. G., Goodgame, R. W. and Condenzsations of the Selected Literature, 1963-1975. vols. Lillywhite, J. E. (1979). Application of the enzyme linked I/II. Washington, D.C.: Hemisphere Publishing. immunosorbent assay (ELISA) for the serodiagnosis of Ito, J. (1953). Studies on the survival of Schistosoma Schistosoma mansoni infections in St. Lucia. Transactions japonictmn in vitro 2. The effects of temperature on the eggs of the Roy al SocietY of Tropical Medicine and Hygiene, 73, of Schistosoma japonicum. Japanese Journal of Med7ical 636-639. Progress, 40, 569-573. Maldonado, J. F., Acosta Matienzo, J. and Velez Herrera, F. (1954a). Studies on the survival of Schistosoma (1950). Biological studies on the miracidium of japonicum in vitro. 3. The effects of temperature on the Schistosoma mansoni. 3. The role of light and temperature SCHISTOSOMA AND SCHISTOSOMIASIS 455 in hatching. Puerto Rico Journal of Public Health and Rowan, W. B. and Gram, A. L. (1959). Quantitative recovery Tropical Medicine, 26, 359-366. of helminth eggs from relatively large samples of feces and Mercado-Burgos, N. (1975). The relative effectiveness of sewage. Journal of Parasitology, 45, 615-621. three halogens and ozone against ova of Schistosoma Sandbach, F. R. (1975). Preventing schistosomiasis: a critical mansoni in sewage. Ph.D. Thesis. Virginia State University. assessment of present policy. Social Science and Medicine, Miyairi, K. and Suzuki, M. (1913). On the development of 9, 517-527. Schistosoma japonicumn. Tokyo Iji Shinski, 1836, 1-5. (1977). Farewell to the god of plague the control of National Schistosomiasis Research Committee (1959). schistosomiasis in China. Social Science and Medicine, 11, Studies on schistosomiasis japonicum in New China. 27-33. Chinese Medical Journal, 78, 368-379. Scott, J. A. and Barlow, C. H., (1938). Limitations to the Negr6n-Aponte, H. and Jobin, W. R. (1979). Schistosomiasis control of helminth parasites in Egypt by means of control in Puerto Rico. Twenty-five years of operational treatment and sanitation. American Journal of Hygiene, 27, experience. American Journal of Tropical Medicine and 619-648. Hygiene, 28, 515-525. Standen, 0. D. (1951). The effects of temperature, light and Newton, W. L., Figgatt, W. B. and Weibel, S. R. (1948). The salinity upon the hatching of the ova of Schistosoma effect of sewage treatment processes upon ova and mansoni. Transactions of the Royal Society of Tropical miracidia of Schistosoma japonicum. 2. Sewage Works Medicine and Hygiene, 45, 225-241. Journal, 20, 657-664. Stimmel, C. M. and Scott J. A. (1956). The regularity of egg Paulini, E. (1964). The contribution of the Public Health output of Schistosoma haematobium. Texas Reports in Engineer to schistosome prevention and its value from an Biology and Medicine, 14, 440-458. epidemiological viewpoint. Revista Brasileira de Tayo, M. A., Pugh, R. N. H. and Bradley, A. K. (1980). Malariologia e Doenta.s Tropicais, 18, 163-174. Malumfashi Endemic Diseases Research Project. XI. Porter, A. (1938). The larval Trematoda found in certain Water-contact activities in the schistosomiasis study area. South African Mollusca with special reference to Annals of Tropical Medicine and Parasitology, 74, 347-354. schistosomiasis (bilharziasis). Publications of the South Watson, J. M. (1958). Ecology and distribution of Bulinus African Institute for Medical Research, 8, 1-492. truncatus in the Middle East, with comments on the effect Rodriques, D. C. and Ferreira, C. S. (1966). Schistosoma of some human activities in their relationship to the snail inansoni infection in the Municipality of Sao Paulo (Brazil) host on the incidence of bilharziasis haematobia in the as the result of deficient urban sanitation. Hospital, 70, Middle East and Africa. Bulletin of the World Health 1609-1615. Organization, 18, 833-894. Rosenfield, P. L. and Bower, B. T. (1979). Management WHO (1973). Schistosomiasis Control. Technical Report strategies for mitigating adverse health impacts of water Series no. 515. Geneva: World Health Organization. resources development projects. Progress in Water (1980). Epidemiology and Control of Schistosomiasis. Technology, 11, 285-301. Technical Report Series no. 643. Geneva: World Health Rowan, W. B. (1964a). Sewage treatment and schistosome Organization. eggs. American Journal of Tropical Medicine and Hygiene, Wittenberg, G. and Yofe, J. (1938). Investigation of the 13, 572-576. purification of water with respect to schistosoma cercariae. -(l946b). Schistosomiasis and the chlorination of Transactions of the Royal Societyof Tropical Medicine and sewage effluent. Americani Journal of Tropical Medicine Hygiene, 31, 549-570. and Hygiene, 13, 577-581. 33 Strongyloides and Strongyloidiasis SOME ASPECTS of the epidemiology and transmission coextensive with hookworm but has a lower pre- of Strongyloides resemble those of the hookworms valence. It is probable that strongyloidiasis is described in chapter 22. In other aspects, however, it is everywhere more common than prevalence figures entirely different, and it must be considered quite would indicate, since it is difficult to diagnose. separately from Ancylostoma and Necator. Infectious agent Description of Pathogen and Disease Strongyloides stercoralis is a minute nematode The curious life cycle of Strongylodes, and the parasitizing man. The adult females are only 2-2.5 danger of very severe consequences of strongyloidiasis millimetres long and live embedded in the mucosa of in immunodeficient or otherwise debilitated in- the small intestine (figure 33-1). The eggs are ovoid and dividuals, have generated considerable research in- measure 50-60 by 30-35 micrometers but are seldom terest in this worm. A recent review is provided by seen because larvae hatch out and are passed in the Carvalho Filho (1978). feces. Identification Reservoirs Strongyloidiasis is an infection of the small intestine The reservoir of S. stercoralis is man, although dogs by the nematode worm Strongyloides stercoralis. and apes have been found naturally infected. Symptoms are often vague or absent, but infection is Another species, S. fuelleborni, infects man in potentially serious, particularly in malnourished or Cameroon, Central African Republic, Congo, immunosuppressed individuals. Nonspecific sym- Ethiopia, Malawi, Togo, Zaire, Zambia, Zimbabwe, ptoms such as diarrhea with abdominal discomfort, and other African countries and in Papua New Guinea recurrent respiratory symptoms, and perhaps a rash and West Irian (Indonesia). It is a common parasite of are common. In a few patients, enteritis with a monkeys and baboons in Africa and Asia, probably malabsorption syndrome, loss of elasticity in the gut, also a natural parasite of man, and the predominant and emaciation occur. When the body's immune Strongyloides species infecting man in the rain-forest responses are deficient, disseminated strongyloidiasis belt of Central Africa. may occur, with larvae attacking most organs of the body; such cases are usually fatal. Diagnosis is by finding larvae in feces examined Transmission under a microscope. Clinically, watery diarrhea with The mature parasitic female, which lives embedded mucus is suggestive of infection if accompanied by in the mucosa of the small intestine, deposits several lesions on the buttocks, in the anal region, and an dozen partially embryonated eggs each day. These eggs eosinophilia of up to 30 percent. Treatment is by oral hatch and liberate noninfective rhabditiform larvae drug therapy with thiabendazole or mebendazole. that migrate into the lumen of the small intestine. The rhabditiform larvae either leave the host with the feces Occurrence or develop into dwarfed filariform larvae that may Strongyloidiasis occurs worldwide and particularly invade the mucosa of the lower portion of the small in warm, wet climates. In most areas strongyloidiasis is intestine or large intestine and cause infection. The 457 458 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS S~~~~~~~~~~~~ K - j,i . Figure . Ad =m (Photo: g~elloe Museu '-' Medca Scince r ~ ~~~~ , Figure 33-1. An adullt Strongyloides stercoralis under a lighlt microscope. Scale bar = 0.1 millimeters. (Photo: Wellcome Museum of Medical Science) latter course is known as autoinfection. Autoinfection A new infection can be initiated by the penetration of can also occur when rhabditiform larvae in feces are a single larva. An adult female worm can produce eggs deposited on the perianal skin and develop into without fertilization by a male worm (partheno- infective filariform larvae that penetrate the body genesis), and male adults are rarely found in the through the skin. Thus. Strongyloides is the one human intestine. helminth that can increase its numbers within the The transmission and life cycle of S. luellchorni is intestine without any form of reinfection or external similar to S. stercoralis exccpt that eggs, rather than transmission. larvae. are shed in the feces. The rhabditiform larvae passed in the feces continue their development in the soil. When conditions are favorable (high nutrient concentration and high Prepatent and incubation periods moisture in soil), they develop into free-living adults. Worms become mature and larvae appear in the These adults continue a free-living life cycle in the soil Worms beom atur apin the .. .. ~~~~~~~feces 17-28 days after skin enetration by filariform as long as conditions allow. When conditions are y y unfavorable (low nutrient concentration and low soil moisture), the rhabditiform larvae develop into infective filariform larvae that can remain alive in moist . . soil for a few weeks. These infective filariform larvae penetrate the skin, usually of the foot, and are carried in As long as mature females are present in the small the blood, through the heart, to the lungs. The larvae intestine, larvae will be passed in the feces. Because penetrate capillary walls around the alveoli (lung sacs). autoinfection is common, patients may pass larvae for enter alveoli, ascend the bronchus and trachea to the many years. Larvae in soil live for less than 2 weeks, but epiglottis, and descend the digestive tract to reach the free-living cycles can occur under favorable conditions upper part of the small intestine where development of to prolong contamination of soil for an unknown the adult parasite is completed. period. STRONGYLOIDES AND STRONGYLOIDIASIS 459 Resistanice not (9 percent). Other accounts of strongyloidiasis in Susceptibility is general, but thereisgoodevdeveloped countries include those from Japan (Tanaka for limited immunity. 1968), Poland (Soroczan 1976), the USSR (Shablovskaya 1964: Stefanov 1970), and Yugoslavia (Bezjak and Breitenfeld 1969). Accounts of S. ftiellebovhii infection in man include Epidemiology those from Papua New Guinea (Vince and others The epidemiology of strongyloidiasis has been little 1979), Zambia (Hira and Patel 1980), and elsewhere in studied, and most prevalance figures are probably central Africa (Pampiglione and Ricciardi 1971, 1972). underestimates because microscopic examination of feces for larvae detects only some infections. Strongyl- oides is usually, although not always, coextensive with hookworm infection. Promiscuous defecation, poverty Control Measures (no shoes), and a wet humid climate are conditions favoring the transmission of both infections. Strongyl- oidiasis typically is rarer than hookworm infection, Mass chemotherapy is an ingredient of any control which is surprising in view of the greater egg program, but it is hampered by the limited effectiveness production of the Strongyloides female and its free- and possible side effects of the drugs available. living cycle, which may build up higher populations of Environmental and educational control measures infective larvae in the soil. Counter influences are that are similar to those for hookworm (chapter 22) and the Strongyloides rhabditiform larva in the feces is less must emphasize excreta disposal, excreta treatment rugged than the hookworm egg, and the infective prior to agricultural application, and the wearing of filariform larva of Strongyloides is shorter lived than shoes. The free-living Strongyloides cycle and the risk of that of the hookworm. continuing autoinfection, however, suggest that en- Studies in Cali (Colombia) during 1956-61 showed vironmental and educational measures will be less an overall prevalence of strongyloidiasis of 14 percent, effective against Strongyloides than against hookworm. with a maximum of 30 percent among people 40-49 Successful reduction of strongyloidiasis in mental years old (Faust and Mugaburu 1965). As with institutions by a combination of chemotherapy and hookworm, infection was more common in males than environmental improvement has been reported from females. Other reports of strongyloidiasis in develop- Hungary (Banki and others 1963), the USA (Jeffery ing countries include those from Brazil (Asami, 1960), and the USSR (Shablovskaya and Smaga 1967). Enomoto and Miura 1970; Dias 1968), Cuba (Raz6n There has been little work on the control of endemic 1971), India (Nawalinski, Schad and Chowdhury strongyloidiasis in villages in developing countries. An 1978), Iran (Ghadirian and Amini 1970), and Tunisia exceptional report comes from Costa Rica (Arguedas (Dancesco and others 1971). and others 1975). In 1965, the inhabitants of the village Strongyloidiasis is found in some areas of some of Palomo were given mass treatment with thiabend- industrialized countries. It occurs throughout the USA azole in a dose of 75 milligrams per kilogram, but is more common in the rural south (Blumenthal repeated after 6 weeks. A neighboring village, Purisil, 1977; Burke 1978; Warren 1974). Infection rates are was used as a control. For the first 2 years there was a high in some institutions, especially in homes for the dramatic drop in the prevalence of strongyloidiasis in mentally retarded. Continuing autoinfection can Palomo from 19 to 1 percent, whereas Purisil showed a maintain strongyloidiasis in individuals long after they drop only from 18 to 10 percent. Hookworm, Trichulris, leave endemic areas, and these infections may become and Ascaris infection rates were not improved after 2 serious and even fatal if resistance is lowered by other years. Seven years after the mass treatment, another diseases or by certain types of drug therapy (Weller, survey was done in 1973. Meanwhile, sanitary and Copland and Gabriel 1981). It has recently been shown socioeconomic conditions had improved: latrines, in Britain (Gill and Bell 1980) and Australia (Grove piped water, and electricity had been installed. The 1980) that up to 28 percent of former prisoners of war prevalence of Strongyloides had dropped to 6 percent in of the Japanese have chronic strongyloidiasis, even 40 Purisil but remained very low at 0.5 percent in Palomo. years after their supposed infection in eastern Asia. For These findings suggest that mass treatment with British ex-prisoners, strongyloidiasis is significantly thiabendazole, combined with concurrent social and morc common among those who worked on the Thai- environmcntal improvements, had a considerable Burma railway (21 percent) than among those who did long-term effect. 460 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Occurrence and Survival in the sewage treatment processes in a manner similar to Environment hookworm eggs (chapter 22). No studies have been reported. The eggs of S. stercoralis are not found in the environment, although those of S. fiielleborni are. The larvae of S. stercoralis may be expected in night soil and Inactivation by Night Soil and Sludge sewage in endemic areas and have been reported from Treatment Processes sewage in the German Democratic Republic (Kalbe 1956). S. stercoralis exists in night soil and sludge as a S. stercoralis larvae typically live for less than 3 delicate larva. not as a robust egg, and it is to be weeks, even in soil under optimal conditions. The expected that complete elimination will take place optimal conditions for the infective filariform larvae during most night soil and sludge treatment processes. are 20-25°C and high moisture. Larvae die rapidly in dur, ing mos nigh e soil an solu tatmen proesses dry soil or at temperatures of over 46°C. Rhabditiform s. eggs in night soil and sludge treatment larve ae lss ble o wthsanddesicaton han processes may be eliminated in a manner similar to larvae are less able to withstand desiccation than hookworm eggs (chapter 22). No studies have been filariform larvae. and at low temperatures they will not reported develop further (Kreis 1932; Little and Gutierrez 1968 reported. Melashenko 1963). It was observed in Colombia that most human teces were buried by dung beetles within a few hours after Literature Cited being deposited on the ground (Little and Gutierrez 1968). It was concluded that, although the burial of Arguedas G., J. A.. Villarejos, V. M., Swartzwelder, J. C., fecesbydungbeetlesmighthavereducedthenumberof Chavarria, A. P., Zeled6n, R. and Kotcher. E. (1975). infective larvae developing in the soil, it probably also Community control of Strongyloides stercoralis by increased larve hancesoofpInothe oming in prontably wh thiabendazole. Texas Reports on7 Biology and Medicine, 33, increased the chances of people coming in contact with 265-268. the larvae that did develop. Since dung beetles kept the Asami. K., Enomoto. Y. and Miura. S. (1970). Infestations by surface of the defecating sites relatively clean, people ancylostomides and Strongyloides stercoralis in tended to return repeatedly to the same site to defecate Pernambuco: survey based on the identification of larvae. and thus increased their chances of becoming infected. Revista do IJnstituto de Medicina Tropical de Sao Paulo, 12, Studies in the Ukraine (USSR) showed that rhabdi- 31-35. tiform and filariform larvae of S. sterco7alis did not Banki, G.. Lengyel, A.. Zoltai. N. and Vilimszky, Z. (1963). move vertically in soil, but that free-living adults Eradication of endemic strongyloidiasis in infant and penetrated to a depth of 0.3 meters (Shablovskaya mental hygienic homes in Hungary. Helniinthologia, 4, 1963). 51-58. A variety of alkalis and acids, especially hy- Bezjak, B. and Breitenfeld. V. (1969). Strongyloidiasis in drochloric acid and alcohol, are effective larvicides northwestern Croatia. (Clinical, diagnostic and thera- (Karbach 1966; Melashenko 1963: Rai 1935). Larvae Parasesitarie. 21, 43-47. are also susceptible to halogens, especially' iodine Blumenthal. D. S. (1977). Intestinal nematodes in the United (Thitasut 1961). Thiabendazole has also been used as a States. New England Journal of Medicine, 297, 1437-1439. larvicide. Some plants and plant products (such as Burke, J. A. (1978). Strongyloidiasis in childhood. Ainerican Cymbopogon citratus,Eucalyptus globuilus, and Mentha Journal of Diseases of Children, 132, 1130- 1136. spicata) have larvicidal properties (Goulart and others Carvalho Filho. E. (1978). Strongyloidiasis. Clinics in 1972). Gastroenterology, 7, 179-200. Dancesco, P.. Chadli. A., Ben Rachid. M. S. and Ben Salem, M. (1971). An endemic-focus of strongyloidiasis in North Africa. Archives de l'Institut Pasteur de Tunis, 48, 337-348. Inactivation by Sewage Treatment Dias, J. C. P. (1968). Observations on strongyloidiasis in the Processes western region of Minas Gerais. Brazil. Rerista do Instituto de Medicina Tropical de Saio Paulo, 10, 305-31 1. Faust, E. C. and Mugaburu. L. G. (1965). Parasitologic S. sterco7ralis exists in sewage as a delicate larva, not surveys in Calle, Departamento Del Valle, Colombia. Xl. as a robust egg, and it is to be expected that complete Intestinal parasites in Ward Silo&, Cali, during a four-year elimination will take place during most sewage period, 1956- 1960. A7nerican Journzal of Tropical Medicine treatment processes. S. Iuelleborni eggs may react to and Hygiene, 14, 276-289. STRONG YLOIDES AND STRONGYLOIDIASIS 461 Ghadirian, E. and Amini, F. (1970). Human strongyloidiasis experimental infection. Bulletin de la Societe de Pathologie in Iran with a report of a case of massive infection. Bulletin Exotique et de ses Filiales, 65, 112 119. de la Societe de Pathologie Exotiqtue et de ses Filiales. 63, Rai, S. (1935). Experimental-therapeutical observation on 590-592. Shikunshi' (Quisqualia indica Linn.) the anthelmintica of Gill, G. V. and Bell, D. R. (1980). Strongyloidiasis in ex- the Chinese medicine for Ascaris. Taiwan Igakkai Zasshi, prisoners of war in south-east Asia. [Correspondence.] 34, 1628-1638. British Medical Journal, 280, 1319. Raz6n. B. R. (1971). Strongyloidiasis in infancy. Revista Goulart, E. G., De Holanda, J. C., Ribeiro de Costa, J. A., Cubana de Medicina Tropical, 23, 13-109. Gilbert, B., Dos Santos, F. D., Turco, A. M. T. and Lopes, Shablovskaya, E. A. (1963). Some,data on the vertical J. L. C. (1972). Inhibition of external development of migration of Strongyloides stercoralis in the soil. Trudi Strongyloides stercoralis and hookworms by natural Ukrainskogo Respublikanskogo Nauchnogo Obshchestva products. Revista Brasileira de Medicina, 29, 14-16. Para-itologov, No. 2, 74-80. Grove, D. I. (1980). Strongyloidiasis in Allied ex-prisoners of (1964). Role of some garden crops in the epide- war in south-east Asia. British Medical Journal, 280, miology of strongyloidiasis. In Materialy Nauclinoi 598-601. Konferentsii Vsesoyuznogo Obschestva Gelnintologou. Hira, P. R. and Patel, B. G. (1980). Human strongyloidiasis 1964, Part II, pp. 235-238. Moscow: The All-Union due to the primate species Strongyloides fulleborni. Society of Helminthologists. Tropical and Geographical Medicine, 32, 23-29. Shablovskaya. E. A. and Smaga, M. F. (1967). An experience Jeffery, G. M. (1960). A three-year epidemiologic study of of eradication of a focus of strongyloidiasis in a psychiatric intestinal parasites in a selected group of mental patients. hospital. Meditsinskaia Parazitologiia i Parazitarnye American Journal of Hygiene. 71, 1-8. Bolezni, 36, 172-174. Kalbe, I. (1956). Investigations of parasites in sewage in Soroczan, W. (1976). The incidence of Strongyloides several towns in East Germany. Zeitschriftffir die Gesainte stercoralis in eastern and south-eastern Poland. Hygiene und ihre Grenzgebiete, 2, 334-343. Wiadomosci Parazytologiczne, 22, 261-272. Karbach, Y. I. (1966). Effects of some drugs and mineral salts Stefanov, G. (1970). Prevalence of strongyloidiasis in the on the viability of Strongyloides stercoralis larvae in vitro village of Aidemir, Silistra County, Bulgaria. and in vivo. Meditsinskai a Parazitologiia i Parazitarnve Meditsinskaia Parazitologiia i Parazitarniye Bolezni, 39, Bolezni, 35, 488-490. 538-540. Kreis, H. A. (1932). Studies on the genus Strongvloides Tanaka, H. (1968). Human strongyloidiasis in Japan. In (Nematodes). American Journal ol Hygiene, 16, 450 491. Medicina Tropical, ed. Anselmi, A., pp. 169-195. Mexico: Little, M. D. and Gutierrez, Y. (1968). Soil relations in the Editorial Fournier. epidemiology of strongyloidiasis. In Eighth International Thitasut, P. (1961). Action of aqueous solutions of iodine on Congress on Tropical Medicine and Malaria. Teheran, 7-15 fresh vegetables and on the infective stages of some September 1968, Abstracts and Reviews, pp. 221-222. common intestinal nematodes. American Journal of Melashenko, V. F. (1963). The effect of some external factors Tropical Medicine and Hygiene, 10, 39-43. on Strongyloides stercoralis larvae. Meditsinskaia Vince, J. D., Ashford, R. W., Gratten, M. J., and Bana-Koiri, Parazitologiia i Parazitarnye Bolezni, 32, 163-168. J. (1979). Strongyloides species infestation in young infants Nawalinski. T., Schad, G. A. and Chowdhury, A. B. (1978). of Papua New Guinea: association with generalized Population biology of hookworms in children in rural oedema. Papua New Guinea Medical Journal, 22, 120-127. West Bengal. I. American Journal of Tropical Medicine and Warren, K. S. (1974). Helminthic diseases endemic in the Hygiene, 27, 1152-1161. United States. American Journal of Tropical Medicine and Pampiglione, S. and Ricciardi, M. L. (1971). The presence of Hygiene, 23, 723-730. Strongyloides fiulleborni Von Linstow, 1905, in man in Weller, I. V. D., Copland, P. and Gabriel. R. (1981). Central and East Africa. Parassitologia, 13, 257-269. Strongyloides stercoralis infection in renal transplant (1972). Presence of Strongyloides fiulleborni in man in recipients. British Medical Journal, 282, 524. tropical Africa. Further epidemiological studies on human 34 Taenia, Taeniasis, and Cysticercosis THE TAENIASES OF MAN, infection by the beef or pork gravid proglottids or eggs from the feces or perianal tapeworms, are common in some areas but are typically region. Differential diagnosis cannot readily be made not a major public health problem. They are, however, between T. saginata and T solium by the examination a major veterinary problem because infected cattle and of Taenia eggs in the stool. Recovery of the gravid pigs arc not suitable for human consumption and there proglottids and a count of the main lateral arms of thc is considerable financial loss and wastage in endemic uterus (7-13 on each side in the case of T. solium and areas. The taeniases are of special interest to sanitary 15-30 in the case of T. saginata) is the specific engineers because their transmission depends on the pretreatment diagnosis. Diagnosis of cysticercosis ingestion by cattle or pigs of inadequately treated usually awaits excision of the larvae and microscopic human feces. examination, although serological techniques are available and radiology may be useful. Treatment for taeniasis is by oral drug therapy, with Description of Pathogen and Disease niclosamide, praziquantel, or other suitable agent. Treatment of cysticercosis is usually surgical, by The medical and veterinary pathology, immu- attempting to remove the cysts. Fenbendazole and nology, and therapy of taeniasis have been much praziquantel are under trial for the drug therapy of studied, and a brief summary is given in the following human cysticercosis. sections. The epidemiology, in contrast, is poorly understood. Occurrence Identification T. saginata and T. solium occur in almost all countries where beef or pork are eaten raw or Taeniasis is an infection with the adult stage of the undercooked (figures 34-1 and 34-2). T. saginata has its beef tapeworm (Taenia saginata) or pork tapeworm (T. highest prevalence in East and Central Africa, in the solium). The adult worm is attached to the wall of the Middle East, and in Latin America. T. solium is most small intestine and typically causes no symptoms. frequently found in Southeast Asia and Latin America. There may be irritation at the site of mucosal Both are quite common in East Europe, where T. attachment and, rarely, abdominal pain, nausea, saginata and T. solium coexist, although the former is weakness, loss of weight, increased appetite, headache, by far the more common. In some areas the prevalence and intestinal obstruction. of infection of man by adult worms is low (about 0.01 Cysticercosis describes an infection with the larval percent), whereas the prevalence of cysticercosis in stage of T. saginata or T. solium; in man, only the larval cattle may be substantial (about 10 percent). stage of T. solium can infect. Human cysticercosis is a severe somatic disease involving many different organs and tissues in which encystment may occur. The Infectious agent manifestation of symptoms depends on the number of Worms of the genus Taenia are cestodes or cysticerci and the tissues or organs involved. tapeworms. The adult Taenia worm lives attached to Cysticercosis is most common in muscles, the brain, the wall of the small intestine; its body winds back and and the heart. forth in the lumen of the small bowel. T. solium is Diagnosis of taeniasis is based on the recovery of usually between 2-4 meters in length, whereas T. 463 464 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS TAENIA SAGINATA E OCCURS (COMMON TO RARE) E VERY COMMON Figure 34-1. Known geographical distributioni of Taenia saginata. The infection may occur in areas as yet unrecorded Moderate to high prevalence ELow prevalence D Low sporadic occurrence Figure 34-2. Known geographical distribution oJ T. solium. The infection may occur in areas as yet unrecorded TAENIA, TAENIASIS, AND CYSTICERCOSIS 465 saginata under favorable conditions can reach a length It is usual to find living and dead cysticerci in the same of 15 meters or more but is usually not more than 6-10 host. Calves may differ from cattle in the maximal meters long (figure 34-3). survival time of cysticerci, which may be 21-30 months. The adult tapeworm consists of a scolex 1-2 When raw or undercooked infected beef or pork is millimeters in diameter, which bears four suckers that eaten by man, the larval tapeworm attaches itself to the are attached to the gut wall (the scolex of T solium also mucosa of thejejunum, where a mature worm develops has a ring of hooks-see figure 34-3), and an area just in 5-12 weeks. behind the scolex that is a region of active cell division, Human infection with C. cellulosae is caused by the the neck. From the neck the chain of proglottids ingestion of T. solium eggs. This may occur via (segments) is generated. The number of proglottids is contaminated food or water (heteroinfection) or via 800-1,000 for T solium and 1,000-2,000 for T. saginata. contaminated fingers when they are introduced into Each mature proglottid is roughly square and the mouth by patients who have the adult worm in measures 10 by 12 millimeters. The mature proglottids their intestine (external autoinfection). Internal auto- have completely formed female and male sexual organs infection-where the eggs are carried by reversed and are followed by the gravid proglottids, which peristalsis back to the stomach and hatch-has been consist essentially of a uterus distended with eggs. The postulated, but there is no firm evidence that it occurs. gravid proglottids break off from the chain, usually One cysticercus ingested may give rise to one adult pass out complete in the feces, and release the eggs in hermaphroditic tapeworm and so may be enough to the soil. The number of eggs per proglottid can be transmit the infection. One egg of T. solium ingested 3 x 10'4-9 x 104 for T solium and 8 x 10-i X 1 05 for can give rise to one larva in the tissues. Although each T. saginata. The eggs are roughly spherical and egg is potentially infective to the animal host, there is measure 30-70 micrometers in diameter. an indication that a minimal dose is needed to cause cysticercosis. In previously unexposed calves 30-100 Reservoirs eggs developed 3-8 cysticerci, respectively, and 500 eggs produced 60-80 cysticerci (Jepsen and Roth The adult stage of T. saginata lives only in man; the 1949). The infective doses of Taenia eggs for cattle and larval stage lives in cattle and can possibly also infect pigs vary according to the previous history of infection, buffalo, giraffe, llama and reindeer. The adult stage of since immunity is developed in the intermediate host. T. solium lives only in man; its larval stage lives in pigs and can also infect man, apes, dogs, and possibly cats Prepatent and incubation periods and sheep. T. saginata reaches maturity in the human intestine within 6-10 weeks from ingestion. T. solium reaches Transmission maturity in 5-12 weeks. An incubation period cannot The adult tapeworm passes about 8 x 105-1 x 106 be stated because symptoms may never develop. eggs a day inside gravid segments. The eggs of the tapeworm that are passed in the stool are immediately Period of communicability infective to the intermediate host. The eggs of T. The adult worms of T saginata and T. solium can live saginata cannot be distinguished readily from those of in the human intestine up to 25 years or more. As long T. solium. When mature eggs are ingested by the as the adult worms are present, infective eggs will be intermediate host (cattle for T. saginata and pigs for T passed in the feces, and thus the possibility of solium) and reach the duedenum, hatching of the transmission persists. oncospheres occurs. An oncosphere is a term for the embryo within the egg. The embryo escapes from its Resistance shell, penetrates the intestinal wall, enters lymphatic or blood vessels, and is carried into the voluntary muscles Man is universally susceptible. There is no evidence where it develops into a mature bladder worm, known for the development of immunity against Taenia as a Cysticercus bovis (in the case of T. saginata) or C. infections in the human host. Unlike the adult worm, cellulosae (in the case of T. solium) within 60-75 days. which is weakly immunogenic, the larval stage of The longevity of T. saginata cysticerci in the Taenia produces an active immunological response in intermediate host depends on the host and on the type cattle or pigs, and there is also an immunological of tissue involved. In the liver, lung, and heart some response in man to infection by Cysticercus cellulosae cysticerci degenerate as early as 20 days after infection. (Flisser, Perez-Montfort and Larralde 1979). 466 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS 1J~~~~~1 Figure 34-3. T. solium aind T. saginata. (a) The head (scolex) and neck of T. solioni-type under scanning electronmicroscopy, showing two of the four suckers and the two rows of hooks that aid attachment to the wall of the small intestine. T saginata has the four suckers but no hooks. Scale bar = 0.1 millimeters. (Photo: A. Jones, Commonwealth Institute of Helminthology, St. Albans, UK.) (b) An adult T1 saginata, several meters long. (Photo: Wellcome Museum of Medical Science) TAENIA, TAENIASIS, AND CYSTICERCOSIS 467 Epidemiology others 1969; Sinnecker 1958), whereas T. solilni is very rare. In the USA there are at least 200,000 cases of T. The epidemiology of taeniasis is not well documen- saginata infection in man, mainly in the west and ted. This is partly because it is not a major public health northeast (Warren 1974). Taeniasis is more common in problem, even in areas where it is common, and also wealthy than in poor communities in the USA, because it is a difficult infection to survey. Eggs are presumably owing to higher meat consumption and excreted intermittently in proglottids (Sterba and more sophisticated recipes (steak tartare. for example). Dykova 1979) and are not evenly distributed in the The prevalence of cysticercosis among slaughtered feces. Therefore, a single stool survey will grossly cattle in the USA is 0.05-0.08 percent. underestimate the prevalence of infection in man. The Beef tapeworm has been attracting increased interest prevalence of infection in cattle or pigs is also difficult in Britain (Crewe and Owen 1978). It was very rare to measure. Serological techniques are under develop- prior to 1945, but there is evidence of an increasing ment; in the meantime, the only method is to slaughter prevalence since that time. The overall prevalence of and minutely inspect the carcases for cysts. Routine bovine cysticercosis is estimated at 0.1 percent, with a inspection of carcases at abattoirs underestimates the resultant economic loss to the beef industry of over prevalence of infection (Rickard and Adolph 1977). US$1 million a year (Crewe and Owen 1978). To maintain their life cycles, T. saginata and T. The modes of transmission of beef tapeworm in solium require two essential and specific conditions. Britain and other industrialized countries remain First, cattle and pigs must eat human feces or fodder uncertain and controversial. The link from cow to man contaminated by human feces; second, beef and pork is readily explained by the eating of undercooked beef; must be eaten raw or undercooked. The first condition the link from man to cow is more difficult to explain in is essential for transmission from man to animal and a society in which nearly everybody defecates into a the second for transmission from animal to man. It sanitary toilet. Two main explanations have been follows that taeniasis is especially prevalent in propounded. First, that the increasingly widespread communities where large herds of cattle or pigs are application of sewage sludge to pasture land provides kept in close proximity to houses, where there is the necessary opportunities for cattle to ingest fecal indiscriminate defecation by humans or the appli- material of human origin. Second, that birds, especially cation of fecal products to pasture (or both), and where seagulls, feeding on trickling filters and sludge drying meat is not always thoroughly cooked. Simanjuntak beds pass the Taenia eggs or proglottids unharmed and others (1977) described endemic taeniasis on Bali through their guts and excrete them later on pasture. (Indonesia) and its relationship to the consumption of Both these transmission mechanisms are theoretically lawar, a dish of spiced minced pork often eaten possible, and T. saginata eggs have been isolated both uncooked, and the lack of adequate excreta disposal from sludge applied to pasture and from gull droppings systems on the island. Fischer (1938) described how the (Crewe 1967; Silverman and Griffiths 1955). It remains outside pit latrines on farms in Germany in the 1930s unresolved, however, which mechanism is the more were cold and unpleasant in winter and so encouraged important, and this uncertainty is a major constraint to the use of the warm cowsheds, often adjoining the policy formulation on sludge treatment prior to house, for defecation by the farmer and his family. He pasture application or other possible control recommended that latrines be made more accessible strategies. and more attractive than the cowsheds and that Human cysticercosis can be a very severe disease and educational campaigns should encourage infected occurs following the ingestion by man of T. solium eggs. individuals to report for treatment and should Man accidentally takes the place of the pig in the discourage the eating of raw beef. normal pork tapeworm life cycle. Human cysticercosis In developing countries, infection of cattle and pigs occurs wherever there is endemic pork tapeworm with Cysticercus bovis and C. cellulosae, respectively, is infection (figure 34-2), and especially where taeniasis very common in communities where these animals prevalances in man are high and sanitation and have ready access to human excreta. Thus, 11 percent hygiene are poor. Thus cysticercosis is to be expected of slaughtered cattle in Sokoto State (Nigeria) had C. among poor people who keep pigs and eat pork. bovis infection (Dada and Belino 1979). Up to 80 The highlands of West Irian (Indonesia) and Papua percent of cattle in some East African herds are infected New Guinea are ideal sites for endemic T. solium and (WHO 1979). consequent human cysticercosis. West Irian was free In developed countries T. saginata infection remains of T. solium, however, until the introduction of infected common, especially in East Europe (Hajduk and pigs from elsewhere in Indonesia during 1971. This 468 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS introduction caused an epidemic of taeniasis and Occurrence and Survival in the cysticercosis in certain areas. This in turn led to an Environment outbreak of severe burns from open fires sustained during epileptic fits caused by Cysticercus cellutlosae The information available on Taenia eggs in the cysts in the brain (Gajdusek 1978). environment is less extensive than for Ascaris eggs and has recently been reviewed by Lawson and Gemmel Control Measures (1983). Survival of Taenia eggs is dependent primarily on temperature and moisture, with greatly reduced Control rests upon denying cattle and pigs access to survival times in hotter and dryer conditions. Survival Control~ ~ ~ ~ ~ ~~tie inst variou envronent aretl less than thoses of inadequately treated human excreta, meat inspection, times In varous env(ronments are less than those of and encouraging thorough cooking of beef and pork. Asca7 is egg (chapter 23) Individual In water There are no specific prophylactic drugs available Taenia eggs have been isolated from river water in for Taenia infections. Compulsory mass diagnosis and the USSR (Bukh 1945: Usacheva 1951) and elsewhere. treatment campaigns carried out in Poland, Bulgaria, Taenia eggs have also been isolated from seawater near and the USSR have successfully reversed a rising sewage outfalls in the USSR (Amirov and Salamov incidence of taeniasis. Other measures, such as 1967) and from coastal and riverine beaches (Amirov improved meat inspection and excreta disposal, have and Salamov 1967; Iwariczuk 1969). to be taken in conjunction with mass chemotherapy to Survival in water is temperature dependent, with prevent reinfection. longer survival at lower temperatures. Laboratory There is no immunological control technique experiments on T. saginata eggs in normal saline at against taeniasis in man. There is, however, a 2-5°C showed survival of up to 168 days (Froyd 1962), possibility of immunizing cattle against infection, and between 95 and 116 days (Penfold, Penfold and research is in progress. Phillips 1937), and up to 335 days (Silverman 1956). In A comprehensive system of meat inspection at saline at room temperature, survival times were abattoirs, and the discarding of parts or all of infected reduced to about 60 days (Silverman 1956). Suvorov carcases, is an essential element in tapeworm control (1965) reported that survival times of T. saginata eggs programs. Most industrialized countries, and some in water increased as temperature fell from 37°C to developing countries, have a meat inspection system, - 4°C, at which temperature eggs remained viable for but effectiveness depends on the training and 63 days. Survival then decreased with lower tempera- supervision of the inspectors, on their ability to tures and was 17 days at -30°C. withstand inducements to overlook infected carcases. Jepsen and Roth (1949) demonstrated that T. and on the absence of an alternate meat distribution saginata eggs were still infective to calves after storage system that circumvents the registered abattoirs. These in water for 33 days at 18°C, and Hajduk and others conditions may be very difficult to achieve. (1969) reported that T. saginata eggs survived in river water in the German Democratic Republic for 35 days. Environmenital Livingstone (1978) reported that Taenia eggs survived in seawater for periods similar to Ascaris eggs. Long-term reduction in transmission of Taenia Eggs in proglottids are more resistant to ovicidal depends on improved sanitation and sanitary educ- chemicals than are free eggs (Gall and Wikerhauser ation. Disposal of feces in a way that prevents any 1968), but free eggs survive longer in water than eggs in contact between the infective eggs and the intermediate proglottids (Suvorov 1965). host will break the life cycle and, together with chemotherapy and meat inspection, will help to In sewage eliminate the disease. The use of night soil or sludge as a fertilizer on pasture, or disposal of effluents into rivers Taenia eggs are found in sewage deriving from any that are a source of drinking water for cattle, community with endemic taeniasis. They may be necessitates adequate treatment. Educational pro- present only in very low concentrations, and they may grams should cover sanitary education, prevention of be still retained in their proglottids, thus making illegal slaughter and unsupervised meat distribution, detection difficult. Taenia eggs have been isolated from meat inspection, and cooking habits. sewage in the German Democratic Republic (Kalbe TAENIA, TAENIASIS, AND CYSTICERCOSIS 469 1956; Sinnecker 1958), Japan (Liebmann 1965). South silage that is later fed to cattle. The survival of T. Africa (Nupen and de Villiers 1975), the USA (Wang saginata eggs on pasture and in silage is therefore of and Dunlop 1954), the USSR (Vassilkova 1941), and epidemiological importance. elsewhere. Some reported survival times are listed in table 34-1. Jepsen and Roth (1949) demonstrated that T. Survival is inversely related to temperature above 0°C, saginata eggs remained infective to calves after 16 days and T saginata eggs may survive for 6 months under at 18°C in sewage, and Hajduk and others (1969) cool, moist conditions. Under hot, dry conditions reported that T. saginata eggs survived in sewage in the survival is unlikely to exceed 2 months. German Democratic Republic for 20 days. In sludge Inactivation by Sewage Treatment Taenia eggs are concentrated in the sludge of sewage Processes treatment plants. Newton, Bennett and Figgat (1949) found that 30-46 percent of Taenia eggs survived for Taenia eggs respond to sewage treatment processes more than 6 months in sludge at 24-30°C. Hajduk and in the same way as Ascaris eggs, and the probable others (1969) reported that T. saginata eggs survived in efficacy of various treatment technologies may be dung from cowsheds in the German Democratic judged from chapter 23. Data from Britain (Silverman Republic for 71 days. 1955; Silverman and Griffiths 1955), India (table 22-4). the USA (Greenberg and Dean 1958; Newton, Bennett On pasture and Figgat 1949), the USSR (Vassilkova 1936), Federal Republic of Germany (Liebmann 1963, 1964), T. saginata is transmitted from man to cattle when and other countries confirm that most removal takes cattle ingest infected human feces. This may occur place by sedimentation and that tapeworm eggs are when feces, sludge, or night soil are deposited concentrated in the sludge. Waste stabilization pond accidentally or deliberately on pasture or are added to effluent should contain no Taenia eggs. Table 34-1. Some studies on the survival of Taenia eggs in grass, silage, and soil Site of Temperature Surviual Country eggs or season (days) Source Australia Grass July- 57 Penfold, Penfold September and Phillips (1937) Denmark Soil February- 159 Jepson and Roth July (1949) Dem. Rep. Germany Grass ND 180 Hajduk and others (1969) USA Hay 1-30°C 22 Lucker and Douvres (1960) USSR Nakhichevan Grass Winter 30 Abbasov (1965) (Azerbaydzhan) (10 to - 16°C) Grass Summer 60 Samarkand Soil Autumn and 180-210 Babaeva (1966) (Uzbekistan) winter Soil Spring 45-105 Soil Summer "Several days" Vologodskaya Hay Winter 210 Shepelev (1961) Province Soil Summer 180 Fed. Rep. of Germany silage 10°C 80 Enigk, Stoye and Zimmer (1969) ND No data. Note: All experiments used T. saginata eggs except those of Abbasov (1965) and Shepelev (1961), which used T. hYdatigena eggs. 470 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS 80 80 75 75 70 70 , ~~~~~~~ZONE 65- OF 65 60 - > SAFETY - 60 o 55 55 '0 - -50 E 45 45 40 40 35 - 35 So - Ix 10Q% det,octicw of Tceoia eggs 0 30 25 - |- Less fhfn 100% destrodtie of T.e-o eggs 25 20 1 - 20 I l l l I l l~~~~~~~~~~~' I' I 0.01 0.1 1.0 10 00 1000 10000 I hoIdy week IIo-nFIth I TIME (HOURS) Figure 34-4. Tihe iifiuenceoJ tinme and temperature on Taenia eggs. The points plottedarethe results of experiments done under widely differing conditions. The line drawn represents a conservative upper boundary for death Inactivation by Night Soil and Sludge readily destroyed than Ascaris eggs. Any night soil or Treatment Processes sludge treatment process that destroys Ascaris eggs may be assumed also to destroy Taenia eggs. Time, temperature, and desiccation are the principal lethal factors acting on Taenia eggs during the treatment of night soil or sludge. Mesophilic digestion Literature Cited is generally thought not to eliminate Taenia eggs (Liebmann 1964: Pawlowski and Schultz 1972). Abbasov, M. T. (1965). Periods of survival on pasture of the although contrary evidence is given by Silverman and oncospheres and bladder-worms of Mtulticeps mullticeps, Guiver (1960). Echiinococcus granu/loslus and Taenia hvdatigena. For elimination of Taenia eggs, night soil and sludge Vete7rinoa7ia, 42, 46-47. must be stored for a protracted period or be heat- Allen, R. W. (1947). The thermal death point of cysticerci of treated by thermophilic composting. Necessary stor- Taenia saginata. Jouirnal oj Parasitology, 38, 331-338. age times depend on ambient temperatures; 1 year Amirov, R. 0. and Salamov, D. A. (1967). Sanitary and may be required in temperate regions, whereas 6 helminthological evaluation of the use of sewage water for months is probably adequate in the tropics. If the field irrigation in the Apsheronsic Peninsula. Gigiena i stored sludge becomes extremely dry (moisture Sanitaria. no. 6, 104-105. content <10O per cent), Taenia egg destruction is onBabaeva R. . (t966). Survival of beef tapeworm oncospheres hastened. on the soil surface in Samarkand. Meditsioiskaia Para- hastime-te rature requirements for the inactivation -itologiia i Parazitarnye Bolezui. 35, 557-559. Time-temperature requirements for the inactivation Bukh, F. L. (1945). The data of helminth egg inspection of the of Taenia eggs have been reported by Allen (1947). sources of water supply of Ufa. Meditsinskaia Para- Silverman (1956), and other workers cited above. -. !.; i Parazitarnme Bole7ni, 14, 66-67. These data are plotted on figure 34-4, and comparison Crewe. S. M. (1967). Worm eggs found in gull droppings. with figure 23-2 shows that Taenia eggs are more A.... I. l fropical Medicine and Parasitology, 61. 358-359. TAENIA, TAENIASIS. AND CYSTICERCOSIS 471 Crewe, W. and Owen, R. (1978). 750,000 eggs a day Wochenschrift, 78, 106-108. £750,000 a year. New Scientist, 80, 344-346. Livingstone, D. J. (1978). Decay of micro-organisms in the Dada, B. J. 0. and Belino. E. D. (1979). Prevalence of bovine marine environment. In Proceedings of the Symposium on cysticercosis and hydatid disease in food animals Disinfection of Water. Pretoria, South Africa: National slaughtered in Sokoto State, Nigeria. International Journal Institute for Water Research. of Zoonoses, 6, 115-117. Lucker, J. T. and Douvres, F. W. (1960). Survival of Taenia Enigk, K., Stoye, M. and Zimmer, E. (1969). The survival of saginata eggs on stored hay. Proceedings of the Taenia eggs in silage. Deutsche tier5rztliche WochenschriJt, Helminthological Society, 27, 110-111. 76, 421-425. Newton, W. L., Bennett, H. J. and Figgat, W. B. (1949). Fischer, C. (1938). Tapeworm. Deutsche tierarztliche Observations on the effects of various sewage treatment Wochenschrift, 46. 391-392. processes upon eggs of Taenia saginata. American Journal Flisser, A., Perez-Montfort, R. and Larralde, C. (1979). The of Hygiene, 49, 166-175. immunology of human and animal cysticercosis: a review. Nupen, E. M. and de Villiers, R. H. (1975). The Evaluation of Bulletin of the World Health Organization. 57, 839-856. Pathogenic Parasites in Water Environments. Project Froyd, G. (1962). Longevity of Taenia saginata eggs. Journal Report no. 13. Pretoria, South Africa: National Institute of Parasitology, 48, 279. for Water Research. Gajdusek, D. C. (1978). Introduction of Taenia solium into Pawlowski, Z. and Schultz, M. G. (1972) Taeniasis and West New Guinea with a note on an epidemic of burns cysticercosis (Taenia saginata). Advances in Parasitology, from cysticercus epilepsy in the Ekari people of the Wissel 10, 269-343. Lakes arca. Papua New Guinea Medical Journal, 21, Penfold, W. J., Penfold, H. B. and Phillips, M. (1937). The 329-342. criteria of life and viability of mature Taenia saginata ova. Gall, Z. and Wikerhauser, T. (1968). The effect of some Medical Journal of Australia, 2, 1-5. substances upon the eggs of Taenia saginata. In Reports Rickard, M. D. and Adolph, A. J. (1977). The prevalence of from the 5th International Meeting on Diseases of Cattle, cysticerci of Taenia saginata in cattle reared on sewage- pp. 1035-1038. Belgrade, Yugoslavia: Institut za irrigated pasture. Medical Journal of.4ustralia, 1,525-527. Patologiju i Terapiju Domacih Zivotinja. Shepelev, D. S. (1961). Survival of Taenia hydatigena eggs in Greenberg, A. E. and Dean, B. H. (1958). The beef tapeworm, the external environment. Sbornik Rabot Vologodskoi measly beef and sewage a review. Sewage and Industrial Nauchno-lssledovatelskoi Veterinarnoi Opytnoi Stantsii, 5, Wastes, 30, 262-269. 143-145. Hajduk, F., Muller, K. H., Saalbreiter, R., Eymmer, H. J., Silverman, P. H. (1955). The survival of the egg of the "beef Hiepe, Th., Bruckner, B. and Wilhelm, W. (1969). tapeworm", Taenia saginata. Advancement of Science, 12, Occurrence, spread. and fight against taeniasis and 108-111. cysticercosis. 71,,, , f'ur hrztliche F. 1;1.. 63, (1956). The longevity of eggs of Taenia ,.^ ,,,,; and 1146-1152. T. saginata under various conditions. Transactions of the Iwafnczuk, I. (1969). Exploration of river shores for the Royal Society of Tropical Medicine and Hygiene, 50, 7. presence of human intestinal parasites. Wiadonmosci Silverman, P. H. and Griffiths. R. B. (1955). A review of Parazytologiczne, 15, 67-70. methods of sewage disposal in Great Britain with special Jepsen. A. and Roth, H. (1949). Epizootiology of Cysticercus reference to the epizootiology of Cysticercus bovis. Annals bovis resistance of the eggs of Taenia saginata. In Report of Tropical Medicine and Parasitology, 49, 436-450. of the 14th International Veterinary Conigress, vol. 2, pp. Silverman, P. H. and Guiver, K. (1960). Survival of eggs of 43-50. London: His Majesty's Stationery Office. Taenia saginata (the human beef tapeworm) after Kalbe, I. (1956). Investigations of parasites in sewage in anaerobic digestion. Proceedings of the Institute of Sewage several towns in East Germany. Zeitschriftfiir die Gesamte Purification, (part 3), 345-347. Hygiene und ihre Grenzgebiete, 2, 334-343. Simanjuntak, G. M., Margono. S. S., Sachlan, R., Harjono, Lawson, J. R. and Gemmel, M. A. (1983). Hydatidosis and C., Rasidi, R. and Sutopo, B. (1977). An investigation on cysticercosis: the dynamics of transmission. Advances in taeniasis and cysticercosis in Bali. Southeast Asian Journal Parasitology, 22 (forthcoming). of Tropical Medicine and Public Health, 8, 494-497. Liebmann, H. (1963) Investigation into the significance of the Sinnecker, H. (1958). The epidemiological significance of different systems of mechanical and biological sewage urban sewage in the spread of possible zooparasitic purification in the fight against cysticercosis in cattle. In infections. . ; . ,i fur die Gesamte Hygiene und ihre Proceedings of the 17th International Veterinary Congress, Grenzgebiete, 4, 98-115. vol. 2, pp. 861-866. Hanover: World Veterinary Sterba, J. and Dykova, I. (1979). Symptomatology of Association. taeniasis caused by Taenia saginata. Folia Parasitologica, (1964). Parasites in sewage and the possibilities of 26, 281-284. their extinction. Advances in Water Pollution Researclh, 11, Suvorov, V. Y. (1965). On viability of beef tapeworm 269-276. oncospheres. Meditsinskaia Parazitologiia i Parazitarnye (1965). Investigations about helminth ova in sewage Bolezni, 34, 98-100. and wastes in Japan. Berliner und Munchener tierarztliche Usacheva, A. M. (1951). Survival of helminth ova in water 472 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS and river sediment. Gigiena i Sanitaaria, Part 2. no. 12. Wang. W. L. L. and Dunlop, S. G. (1954). Animal parasites in 12-17. sewage and irrigation water. Sewage and IndnIstrrial Wastes. Vassilkova. Z. (1936). On the dehelminthization of purified 26, 1020-1032. sewage by intensive methods. Meditsinskaia Parazitologiia Warren, K. S. (1974). Helminthic diseases endemic in the i Parazitarnye Bolezni. 5, 671-674. United States. Anlerican Journ7lal oj Tropical Medicine anld (1941). Evaluation of the contamination of vegetables Hygiene, 23, 723-730. with eggs of helminths in sewage farms with different wHo (1979). Parasitic Zoonoses. Technical Report Series 637. methods of cultivation. Meditsinskaia Para7itologiia i Geneva: World Health Organization. Parazitarnye Bolezni, 10, 217-225. 35 Trichuris and Trichuriasis THERE ARE THREE intestinal worm infections of man although 25-40 percent is more usual. Prevalence and having cosmopolitan distributions and producing intensity of infection are highest among children 5-15 severe clinical consequences in heavily infected years old. individuals. These are hookworm infection (chapter 22), ascariasis (chapter 23), and trichuriasis (this . . chapter). Trichuriasis is often considered jointly with InJectious agent ascariasis because they are usually endemic in the same Trichuris trichiura (formerly called Trichocephalus communities and their life cycles, modes of trans- dispar, Tricho. trichiura, and Tricho. hominis), a mission, and epidemiologies are similar. nematode, is the human whipworm. Adult female worms are 25-50 millimeters in length; males measure 30-45 millimeters, with a tightly coiled posterior end Description of Pathogen and Disease (figure 35-1). The eggs are lemon-shaped with plug- like, translucent prominences at each end. The eggs are 50-55 micrometers long and 22 micrometers wide. The Trichuriasis is an infection of man by the human pig whipworm, T. suis, is very similar and can also whipworm Trichuris trichiura. It is commonly referred infect man; routine stool examination does not to as whipworm infection and, rarely, as tri- distinguish between eggs of T. trichiura and those of T. chocephaliasis. Recent reviews include Chanco and suis. Closely related species infect other animals; for Vidad (1978), Mahmoud (1979), and Wolfe (1978). instance, T. ovis in sheep, T. vulpes in dogs and foxes, and T. muris in mice. Identification Trichuriasis is a helminthic infection of the large Reservoir intestine and cecum. Most infections in adults are The reservoir of T. trichiura is man, who may also act symptomless, but there may be slight abdominal pain as a minor reservoir of T. suis. It is possible that pigs, and some diarrhea. In malnourished children heavy lemurs, and monkeys may also act as a reservoir of T. infection can cause anemia, bloody diarrhea, and trichiura. occasionally, prolapse of the rectum (Jung and Beaver 1951; Jung and Jelliffe 1952; Kamath 1973). Diagnosis is by identification of Trichuris eggs in the feces. Safe Transmission and effective drugs -for instance, mebendazole- are Female worms lay 2,000-10,000 eggs per day. The now available for treating trichuriasis, and some of unsegmented fertilized eggs are discharged in the feces these are effective in mixed infections with hookworm and take 2-5 weeks to develop into the infective stage and Ascaris. in a moist, warm environment (usually soil or the perineum). Development time is temperature de- Occurrence pendent and may be 4-6 months at 15°C, 3-4 weeks at 26°C, 17 days at 30°C, and 11 days at 35°C. The eggs of Trichuriasis occurs throughout the world and is very Trichuris are less resistant than those of Ascaris, but common in some areas with warm and humid climates. even so they may survive for several months in shaded, Local prevalences of 50-99 percent are reported, moist soil. Once ingested -from contaminated hands, 473 474 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS / , f~~~~~~~~~~~~t' _ew-~ 4~ _ /o;T 'S. Figure 35-1. A male (left) andJemale (right) Trichuris trichiura under a light microscope. The worms are 30-50 millimeters in length. (Photo: Wellcome Museum of Medical Science) food, or soil-infective eggs hatch in the intestine to remain infective for several months in a moist liberate small larvae, which feed and grow in the small environment. intestine before passing to the cecum to become mature adults. Adult worms anchor themselves to the large Resistance bowel mucosa by means of a spear-like projection at their anterior end. This process of maturity takes about Little is known of the immunology of trichuriasis. 2 months, and the adult worm can live for 3-5 years in Susceptibility is general, and the age distribution of man. Heavy infections are associated with egg counts infection may be due to the varying degrees of exposure in excess of 30,000 per gram of feces. at different ages. Prepatent and incubation periods Epidemiology A female worm may mature and start producing Trichuriasis is extremely common in some areas of eggs about 2 months after the ingestion of infective the world, especially where the climate is wet and eggs. Clinical symptoms may never develop or may humid and where there is extreme poverty. Surveys of develop gradually as a result of continuing reinfection children 1-5 years old in Guatemala revealed and increasing worm burdens. trichuriasis prevalences of 33 percent among rural children, 9 percent among poor urban children, and 4 Period of communicability percent among more wealthy urban children (Pierce and others 1962). In one village in Guatemala, 48 Eggs are discharged in the feces as long as there is an percent of children became infected by Trichuris adult fertilized female worm living in the cecum. The between birth and 3 years (Mata and others 1977). life span of an adult worm may be up to 8 years but is A survey of children 4-6 years old in Kuala Lumpur typically around 3 years. The eggs may develop and (Malaysia) found a prevalence of trichuriasis of 84 TRICH URIS AND TRICHURIASIS 475 percent among poor children and 8 percent among The epidemiology of trichuriasis is closely similar to "upper middle class" children (Yan and others 1978). A that of ascariasis, and the remarks made on study of rural schoolchildren (6-12 years old) 72 epidemiology in chapter 23 are applicable. A major kilometers from Kuala Lumpur found an 85 percent difference is the greater longevity of the adult Trichuris prevalence of trichuriasis (Lo and others 1979). worm, which provides greater opportunity for In the late 1960s, trichuriasis was the most common accumulating high worm burdens and delays the effects intestinal worm infection in South Korea, with of any control program. prevalence rates of 72 percent in Seoul and 75 percent Students of trichuriasis epidemiology, and of the in rural areas (Seo and others 1969). Trichuris was also comparative epidemiology of ascariasis, trichuriasis, the most common intestinal worm in Cali (Colombia) and hookworm infection, should read the early during 1956-61, when the prevalence among children accounts of these infections from China, Panama, and 5-9 years old was 91 percent (Faust and Mugaburu the USA (Cort, Otto and Spindler 1930; Cort, 1965). Similarly, Trichuris was more prevalent than Schapiro and Stoll 1929; Cort and Stoll 1931; Cort and Ascaris or hookworm in Haiti, with an 85 percent others 1929; Otto 1932; Otto, Cort and Keller 1931). prevalence among children 10-14 years old (Raccurt, Vial and Pierre-Louis 1977). There are major unexplained variations among communities in the prevalence of trichuriasis and in the Control Measures relative prevalence of Trichuris, Ascaris, and hook- worm infections. It is often asserted that areas of high Only environmental and behavioral changes can rainfall are associated with more Trichuris and less have a sustained impact on trichuriasis, but mass Ascaris, whereas in drier regions Ascaris may be chemotherapy may be used to reduce infection rates in expected to be the more prevalent worm (Spindler, the short term. 1929). Some data support this, and high prevalences are frequently found in hot wet climates, especially in Individual areas of East Asia where night soil is widely used in agriculture. In Iran, the prevalence of trichuriasis was 6 No prophylactic drugs or vaccines are available. percent in the dry southwest (Massoud and others Mass chemotherapy has not been as successful in 1980); compared with up to 60 percent in the wetter controlling trichuriasis as it has been with ascariasis area bordering the Caspian Sea (Ghadirian, Croll and and hookworm infection, because until recently safe Gyorkos 1979). Low prevalences are reported, and effective drugs were not available. With the advent however, from areas with seasonally wet climates, such of new drugs, especially mebendazole and oxantel- as Delhi (Biswas and others 1978) and Bengal pyrantel, mass chemotherapy has become an impor- (Nawalinski, Schad and Chowdhury 1978) in India tant control strategy. and from areas with perennially wet climates, such as Papua New Guinea (Jones 1976). As with ascariasis (chapter 23), both the prevalence Environmental and intensity of trichuriasis infection typically peak in The remarks made about the environmental control the 5-15 age group. At older ages intensities decline, of ascariasis (chapter 23) apply to trichuriasis. The and prevalences either decline similarly or maintain major difference is that the longer life span of Trichuris fairly constant levels throughout later life. in the human host results in prevalence rates falling Trichuriasis is common in some developed count- more slowly following a successful campaign to control ries. There are an estimated 2.2 million people infected transmission. in the USA, and the disease is especially common in the Control rests upon major improvements in excreta southeast (Fulmer and Huempfner 1965; Warren disposal, especially for children, and changes in 1974). Male homosexuality is associated with risk of behavior associated with defecation. In areas where trichuriasis in some developed countries (McMillan night soil is used in agriculture, it is necessary to treat 1978). A survey of trichuriasis among mentally the night soil thoroughly before application to the subnormal patients at seventeen hospitals in the UK fields. Environmental measures that interrupt trans- revealed that the overall prevalence was 13 percent, mission will reduce prevalence rates slowly, and it may with markedly more infection in southern England be many months before measurable reductions in than northern England and no infection in Scotland trichuriasis in the community are obtained. Therefore (Lynch and others 1972). environmental and behavioral modifications should be 476 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS combined with periodic mass chemotherapy in any eggs. Ascaris eggs therefore provide a better parasito- trichuriasis control program. This integrated approach logical indicator than Trichuris eggs in areas where to control has been successful in several countries; for both are endemic. Ascaris eggs are better able to instance in South Korea (Soh 1973). survive both warm and cold temperatures than Some studies on environmental interventions and Trichuris eggs (Nolf 1932); and the latter require a trichuriasis are listed in table 35-1. The discussion of higher moisture level in soil to develop than Ascaris table 23-2 applies fully to these findings. eggs (Spindler 1929). In the city of Kermanshah (Iran), Ghadirian and A few studies on Trichuris eggs in the environment others (1973) recorded trichuriasis prevalences of 72 are mentioned below. It may be assumed that the percent in a low-income area near an open sewer and comments on Ascaris eggs in the environment made in 58 percent in a high-income area far from the sewer. chapter 23 apply to Trichuris, except that Trichuris eggs This latter high prevalence in a more wealthy section of will typically remain viable for shorter periods. the city was attributed to the irrigation of vegetables with night soil and sewage. In South Africa it was reported that Xhosa children (6-9 years old) living in I Cape Town (piped water and sewer connections to Yarulin (1955) isolated Trichuris eggs from 3 percent every house) had a trichuriasis prevalence of 89 of Caspian Sea water samples near a sewage outfall in percent, whereas rural Xhosa children in villages in the the USSR. Usacheva (1951) isolated Trichuris eggs Transkei (water collected from streams and sanitation from river water and river sediment in the USSR. comprising pit latrines or indiscriminate defecation) Iwaiiczuk (1969) found Trichuris eggs in greater had a prevalence of only 3 percent (van Niekerk and numbers than Ascaris eggs on public beaches on the others 1979). The reason for this strange finding was River Vistula (Poland), but these probably derived not known but may be connected with the wetter from promiscuous defecation by visitors rather than climate of Cape Town. Both the Iranian and South from the river water. Livingstone (1978) reported that African data strongly suggest that limited environ- Trichuris eggs rapidly swelled and died in seawater. mental improvements may not be sufficient to control Trichuris transmission. In feces and night soil Some Trichuris eggs in pit latrines remained viable Occurrence and Survival in the for over 18 months but died sooner than Ascaris eggs Environment (Biziulevicius 1965). There is considerably more information on the occurrence and survival of Ascaris eggs in the n sewage environment than on the survival of Trichuris eggs. This Reported concentrations of Trichuris eggs per liter of is partly because, worldwide, Ascaris is probably the sewage include 10-20 in Tokyo (Japan; Liebmann more common worm and also because Ascaris eggs are 1965) and 41 in San Juan (Puerto Rico; Rowan and more resistant to hostile environments than Trichuris Gram 1959). Many accounts of Trichuris eggs in Table 35-1. Some studies on environmental influences on trichuriasis Country Result Source Costa Rica Trichuriasis prevalence was the same among individuals with or without a latrine but Moore, de la Cruz and was lower among those having a septic tank system. Vargas-Mendez (1965) Japan Night soil treatment with thiabendazole reduced trichuriasis prevalence from 65 percent Kutsumi (1969) to 47 percent over 2 years. Singapore Poor families rehoused for I year in modern flats had a trichuriasis prevalence of 28 Kleevens (1966) percent; in comparison squatter families had a 58 percent prevalence. USA Trichuris transmission was interrupted when adult female mental patients were moved Jeffery (1960) from old unsanitary quarters to a modern building. TRICH URIS AND TRICHURIASIS 477 sewage in the German Democratic Republic (for percent in 1960, possibly owing to the cessation of the instance, Kalbe 1956; Sinnecker 1958), and the USSR supply of sewage-irrigated vegetables from Jordan (for instance, Vassilkova 1936) have been published. (Ben-Ari 1962). Crops may be decontaminated by soaking in an In sludge ovicidal chemical, although Trichuris eggs are more resistant to iodine than are Ascaris eggs (Thitasut Trichuris eggs, like Ascaris eggs, tend to settle in 1961). It will usually be more reliable and appropriate primary and secondary sedimentation tanks and are to immerse the vegetables in warm water (60°C) for 10 therefore concentrated in the sludge from sewage minutes (see chapter 23). treatment plants. Trichuris eggs have been found in sludges in Czechoslovakia (Kralova and Safranek 1957) and the USA (Theis, Bolton and Storm 1978), Inactivation by Sewage Treatment and may be expected at every sewage treatment plant Processes serving a population with endemic trichuriasis. Little information is available on Trichuris egg In soil removal by sewage treatment processes because most researchers have focussed on Ascaris egg removal. The Trichuris eggs, like Ascaris eggs, can remain alive in data presented for Ascaris egg removal (chapter 23) soil for extended periods, especially if conditions are may be assumed to apply to Trichuris egg removal. moist, cool, and shaded. A study at a hospital near Indian data assembled by Panicker and London (England) showed that 21 percent of T. Krishnamoorthi (1978) are presented in table 22-4 and trichiura eggs were still potentially infective after 18 show that Trichuris and Ascaris removals are similar. months in "clay-flint" soil (Burden and others 1976). This is also shown by studies on sedimentation and activated sludge treatment in Calcutta (Bhaskaran and On crops others 1956). Correctly designed and operated waste stabilization ponds remove all Trichuris eggs (table 22- Where trichuriasis is endemic and fecal materials 4 and Lakshminarayana and Abdulappa 1972). (sewage, night soil, or sludge) are used in agriculture, Vassilkova (1936) studied Trichuris eggs in sewage Trichuris eggs may be found on crops, and this may treatment plants near Moscow (USSR), and play some role in transmission. Trichuris eggs on Plyushcheva (1974) experimented with ionizing ra- vegetables have been extensively studied in the USSR diation to kill Trichuris eggs in sewage. (Barchenko 1953; Biziulevicius 1954; Khaustov 1935; Romanenko 1971; Vassilkova 1941) and other East European countries. Sinnecker (1958) isolated Inactivation by Night Soil and Sludge Trichuris eggs from sewage-irrigated lettuce in the Treatment Processes German Democratic Republic and reported that prevalences of trichuriasis were higher (20 percent) Trichuris eggs tend to be concentrated in the sludge among irrigation workers than among sewermen (8 of all sewage treatment processes, and high con- percent) or sewage treatment plant operators (0 centrations may be expected in night soil in areas percent). Trichuris contamination of vegetables is where trichuriasis is endemic. The data presented on especially common in areas of East Asia-for Ascaris egg removal (chapter 23) may be assumed to instance, in South Korea (Choi 1970), where untreated apply to Trichuris egg removal, except that Trichuris night soil is a commonly used fertilizer. eggs are probably eliminated somewhat earlier than The prominence of contaminated vegetables in Ascaris eggs during storage, digestion, or composting. trichuriasis transmission is partly dependent on the Reports on Trichuris eggs in sludge following level of domestic hygiene and sanitation, and thus on various forms of treatment are available from the USA the degree to which yard transmission among children (Wright, Cram and Nolan 1942), the USSR is taking place. In more wealthy communities where (Vassilkova 1936), China (Szechwan Research hygiene and sanitation are good, it is possible that Institute 1974), and other countries. Most research has contaminated vegetables may be a major transmission concentrated on Ascaris eggs in sludge and night soil route. This was thought to be the situation among the treatment processes because they are usually more Jewish residents of Jerusalem (Israel), where tri- numerous and are believed to be more persistent than churiasis prevalence fell from 13 percent in 1947 to 5 Trichuris eggs. Contrary evidence is provided by Enigk 478 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS and others (1975), who found that Trichuris eggs Cort, W. W. and Stoll, N. R. (1931). Studies on Ascaris survived thermophilic digestion for up to 5 days, lumbricoides and Trichuris trichiura in China. American whereas Ascaris eggs were eliminated within 3 days. Journal of Hygiene, 14, 655-689. Trichuris eggs in sludge and night soil can be Cort, W. W., Stoll, N. R., Riley, W. A. and Sweet, W. C. (1929). eliminated by the addition of appropriate ovicides VIII. Quantitative studies on the distribution of Ascaris (table 2314). Kutsumi and Komiya '1965) experimen- lumbricoides and Trichuris trichiura in Panama. American (taed 23-4). th utsenda and Kouniythat(19 expersimenr Journal of Hygiene, Monographic Series No. 9, 161-209. ted with thiabendazole and found that, under similar Enigk, K., Thaer, R., Dey-Hazra, A: and Ahlers, R. (1975). conditions, Trichuris eggs were killed by the appli- Survival of resistant external stages of parasites during cation of concentrations one-sixth to one-sixteenth of fermentation of liquid cattle manure at raised tempera- those required for Ascaris egg destruction. tures. Zentralblatt Jfr Veterindrmedizin, Reihe B, 22, 687-702. Faust, E. C. and Mugaburu, L. G. (1965). Parasitologic Literature Cited surveys in Cali, Departamento del Valle, Colombia. Xl. Intestinal parasites in Ward Siloe, Cali, during a four-year Barchenko, I. P. (1953). The importance of some food period 1956-1960. American Journal of Tropical Medicine products as possible factors in the geohelminth infection of and Hygiene, 14, 276-289. a population. In Papers in Helminthology Presented to Fulmer, H. S. and Huempfner, H. R. (1965). Intestinal Academician K. I. Skryabin on his 75th Birthday, pp. 39-43. helminths in eastern Kentucky: a survey in three rural Moscow: Izdatelstvo Akademii Nauk SSR. counties. American Journal of Tropical Medicine and Ben-Ari, J. (1962). The incidence of Ascaris lumbricoides and Hygiene, 14, 269-275. Trichuris trichiura in Jerusalem during the period of Ghadirian, E., Arfaa, F., Missaghian, Gh. and Bahrani, H. 1934-1960. American Journal of Tropical Medicine and (1973). Prevalence of intestinal helminthiasis in Hygiene, 11, 366-368. Kermanshah City and some villages in the province. Bhaskaran, T. R., Sampathkumaran, M. A., Sur, T. C. and Iranian Journal of Public Health, 2, 90-101. Radhakrishnan, I. (1956). Studies on the effect of the Ghadirian, E.. Croll, N. A. and Gyorkos, T. W. (1979). Socio- sewage treatment processes on the survival of intestinal agricultural factors and parasitic infections in the Caspian parasites. Indian Journal of Medical Research, 44, littoral region of Iran. Tropical and Geographical Medicine, 163-180. 31, 485-491. Biswas, H., Saraljit, S., Arora, R. R. and Mathur, K. K. (1978). Iwariczuk, I. (1969). Exploration of river shores for the Intestinal parasites and different species of hookworm in presence of human intestinal parasite. Wiadomosci slum dwelling people around Delhi. Journal of Parazytologiczne, 15, 67-70. Communicable Diseases, 10, 234-237. Jeffery, G. M. (1960). A three-year epidemiologic study of Biziulevicius, S. (1954). Role of vegetables and berries in the intestinal parasites in a selected group of mental patients. epidemiology of helminthiasis in the population of American Journal of Hygiene, 71, 1-8. Lithuania. Meditsinskaia Parazitologiia i Parazitarnye Jones, H. I. (1976). A study of human intestinal helminthiases Bolezni, 23, 124-126. on Kar Kar Island, Madang Province. Papua New Guinea (1965). Studics on the viability of Ascaris and Medical Journul, 19, 165-172. Trichuris eggs in buried lavatory pits. Acta Parasitologica Jung, R. C. and Beaver, P. C. (1951). Clinical observations on Lithuanica, 5, 77-84. Tricocephalus trichiurus (whipworm) infestation in child- Burden, D. J., Whitehead, A., Green, E. A., McFadzean, J. A. ren. Paediatrics, 8, 548-557. and Beer, R. J. S. (1976). The treatment of soil infested with Jung, R. C. and Jelliffe, D. B. (1952). The clinical picture and the human whipworm Trichuris trichiura. Journal of treatment of whipworm infection. West African Medical Hygiene, 77, 377-382. Journal, 1, 11-15. Chanco, P. P. and Vidad, J. Y. (1978). A review oftrichuriasis, Kalbe, I. (1956). Investigations of parasites in sewage in its incidence, pathogenicity and treatment. Drugs, 15 several towns in East Germany. Zeitschritffir die Gesamte (Suppl. 1), 87-93. Hygiene und ihre Grenzgebiete, 2, 334-343. Choi, D. W. (1970). Incidence of parasite eggs attached to Kamath, K. R. (1973). Severe infection with Trichuris vegetable leaves, water cress and carrots. Korean Journal trichiura in Malaysian children. American Journal of of Parasitology, 8, 19. Tropical Medicine and Hygiene, 22, 600-605. Cort, W. W., Otto, G. F. and Spindler, L. A. (1930). Khaustov,J. M. (1935). Vegetables asafactor in transmission Investigations on Ascaris lumbricoides and the associated of Trichocephalus (Trichuris) trichiurus. Trudy Leningrads- intestinal helminths of man in southwesterni Virginia. kogo Instituta Epidemiologii i Bakteriologii imeni Pastera, American Journal of Hygiene, 11, 1-55. 2, 148-152. Cort, W. W., Schapiro, L. and Stoll, N. R. (1929). A study of Kleevens, J. W. L. (1966). Re-housing and infections by soil- reinfection after treatment with hookworm and Ascaris in transmitted helminths in Singapore. Singapore Medical two villages in Panama. American Journal of Hygiene, 10, Journal, 7, 12-29. 614-625. Kralova, E. and Safranek, V. (1957). Helminthological TRICH URIS AND TRICHURIASIS 479 investigation of sediments from the wastewater refining Ascaris. American Journal of Hygiene, 16, 288-322. station at Koutim. Ceskoslovenskd Hygiena, 2, 399-404. Otto, G. F. (1932). .4scaris and Trichuris in southern United Kutsumi, H. (1969). Epidemiological study on the preventive States. Journal of Parasitology, 18, 200-208. effect of thiabendazole as an ovicide against human Otto, G. F., Cort, W. W. and Keller, A. E. (1931). hookworm. Triclhuris and Ascaris infections. Japanese Environmental studies of families in Tennessee infested Journal of Medical Science and Biology, 22, 51-64. with Ascaris, Trichuris and hookworm. American Journal Kutsumi, H. and Komiya, Y. (1965). Effect of thiabendazole of Hygiene, 14, 156-193. as an ovicide on helminth eggs in nightsoil. Japanese Panicker, P. V. R. C. and Krishnamoorthi, K. P. (1978). Journal of Medical Science and Biology, 18, 203-224. Elimination of enteric parasites during sewage treatment Lakshminarayana, J. S. S. and Abdulappa, M. K. (1972). The processes. Indian Association for Water Pollution Control effect of sewage stabilization ponds on helminths. In Low Technical Annual, 5, 130-- 138. Cost Waste Treatment. ed. Sastry, C. A., pp. 290-299. Pierce, V., Ascoli, W., de Leon, R. and Gordon, J. E. (1962). Nagpur, India: Central Public Health Engineering Studies of diarrheal disease in Central America. III. Research Institute. Specific etiology of endemic diarrhea and dysentery in Liebmann, H. (1965). Investigations about helminth ova in Guatemalan children. American Journal of Tropical sewage and wastes in Japan. Berliner und Miinchener Medicine and Hygiene, 11, 395-400. tierarztliche Wochenschrift, 78, 106-108. Plyushcheva, G. L. (1974). The effect of ionizing radiation on Livingstone, D. J. (1978). Decay of micro-organisms in the Trichuris trichiura and Diphyllobothrium latum eggs in marine environment. In P, - i,,, of a Symposium on domestic sewage: an experimental study. Meditsinkaia Disinfection of Water. Pretoria, South Africa: National Parazitologiia i Parazitarnye Bole_ni, 43, 463--468. Institute for Water Research. Raccurt,_C., Vial, P. and Pierre-Louis, J. M. (1977). Etude Lo, E. K. C., Varughese, J., Ghouse, A. and Noor, M. (1979). epidemiologique des helminthiases intestinales a l'ile de la Helminthiases in peninsular Malaysia: prevalence and Tortue (Haiti). Bulletin de la Societe de Pathologie density of infestation of hookworm, Ascaris and Trichuris Exotique et des ses Filiales, 70, 240-249. in rural school children. Medical Journal of Malaysia, 34, Romanenko, N. A. (1971). Sanitary-helminthological eva- 95-99. luation of new methods of irrigation with sewage. Lynch, D. M., Green, E. A., McFadzean, J. A. and Pugh, I. M. Meditsinskaia Parazitologiia i Parazitarnye Bolezni, 40, (1972). Trichuris trichitura infestations in the United 361-362. Kingdom and treatment with difetarsone. British Medical Rowan, W. B. and Gram, A. L. (1959). Quantitative recovery Journal, 4, 73-76. of helminth eggs from relatively large samples of feces and McMillan, A. (1978). Threadworms in homosexual males. sewage. Journal of Parasitology, 45, 615-621. [Correspondence.] British Medical Journal, 1, 367. Seo, B. S., Rim, H. J., Loh, I. K., Lee, S. H., Cho, S. Y., Park, S. Mahmoud, A. A. F. (1979). Intestinal nematodes. In C., Bae, J. W., Kim, J. H., Lee, J. S., Koo, B. Y. and Kim, K. Principles and Practice of Infectious Diseases,eds. Mandell, S. (1969). Study on the status of helminthic infections in G. L., Douglas, R. G. and Bennett, J. E., pp. 2157-2164. Koreans. Korean Journal of Parasitology, 7, 53-70. New York: John Wiley. Sinnecker, H. (1958). The epidemiological significance of Massoud, J., Arfaa, F., Jalali, H. and Keyvan, S. (1980). urban sewage in the spread of possible zooparasitic Prevalence of intestinal helminths in Khuzestan, South- infections. Zeitschrift ffir die Gesamte Hygiene und ihre west Iran, 1977. American Journal of Tropical Medicine Grenzgebiete, 4, 98-115. and Hygiene, 29, 389-392. Soh, C. T. (1973). Control of soil-transmitted helminths in Mata, L. J., Kromal, R. A., Urrutia, J. J. and Garcia, B. (1977). Korea: a progress report. Yonsei Reports on Tropical Effect of infection on food intake and the nutritional state: Medicine, 4, 102-125. perspectives as viewed from the village. American Journal Spindler, L. A. (1929). The relation of moisture to the of Clinical Nutrition, 30, 1215-1227. distribution of human Trichuris and Ascaris. American Moore, H. A., de la Cruz. E. and Vargas-Mendez, 0. (1965). Journal of Hygiene, 10, 476-496. Diarrheal disease studies in Costa Rica. IV. The influence Szechwan Research Institute of Antiparasitic Diseases and of sanitation upon the prevalence of intestinal infection Mienchu County Antischistosomiasis Office, Szechwan and diarrheal disease. American Journal of Epidemiology, (1974). Digestion of nightsoil for destruction of parasite 82, 162-184. ova: a report of investigation and experimental obser- Nawalinski, T., Schad, G. A. and Chowdhury, A. B. (1978). vation. Chinese Medical Journal, 93, 31. Population biology of hookworms in children in rural Theis, J. H., Bolton, V. and Storm, D. R. (1978). Helminth ova West Bengal. I. General parasitological observations. in soil and sludge from twelve US urban area. Journal of American Journal of Tropical Medicine and Hygiene. 27, the Water Pollution Control Federation, 50, 2485-2493. 1152- 1161. Thitasut, P. (1961). Action of aqueous solutions of iodine on Nolf, L. 0. (1932). Experimental studies on certain factors fresh vegetables and on the infective stages of some influencing the development and viability of the ova of common intestinal nematodes. American Journal of human Trichuris as compared with those of the human Tropical Medicine and Hygiene, 10, 39-43. 480 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: HELMINTHS Usacheva, A. M. (1951). Survival of helminth ova in water Wolfe, M. S. (1978). Oxynris, Trichostrongylus and Trichuris. and river sediment. Gigiena i Sanitaria. Part 2, no. 12, Clinics in Gastroenterologv, 7, 201-217. 12- 17. Wright, W. H., Cram, E. B. and Nolan, M. 0. (1942). van Niekerk, C. H., Weinberg, E. G., Shore, S. C. L. and Preliminary observations on the effect of sewage treatment Heese, H. de V. (1979). Intestinal parasitic infestation in processes on the ova and cysts of intestinal parasites. urban and rural Xhosa children: a comparative study. Sewage Works Journal, 14. 1274-1280. South African Medical Journal, 55, 756-757. Yan, C. W., bin Ishak, F., Hee, G. L.. Devaraj, J. M., bin Vassilkova, Z. (1963). On the dehelminthisation of purified Ismail, K., Jalleh, R. P., Peng, T. L. and Jalil, T. M. bin A. sewage waters by intensive methods. Meditsinkskaia (1978). The problem of soil transmitted helminths in P.:.' ii. ,,o i Parazitarnve Bolezni, 5, 671-674. squatter areas around Kuala Lumpur. Medical Journal of (1941). Evaluation of the contamination of vegetables Malaysia, 33, 34-43. with eggs of helminths in sewage farms with different Yarulin, G. R. (1955). Contamination of the coastal zone of methods of cultivation. Meditsinskaia Parazitologiia i the Caspian Sea with eggs of geohelminths. Meditsinskaia Parazitarnye Bolezni. 10, 217-225. Parazitologiia i Parazitarnye Bolezli, 24, 117-120. Warren, K. S. (1974). Helminthic diseases endemic in the United States. American Journal of Tropical Medicine and Hygiene, 23, 723-730. Section V. Insects and Excreta Chapter 36 Culex pipiens Mosquitoes and the Transmission of Bancroftian Filariasis 37 Flies, Cockroaches, and Excreta 36 Culex pipiens Mosquitoes and the Transmission of Bancroftian Filariasis CHAPTERS 36 AND 37 are different from the other pipiens complex live anywhere that man accidentally chapters in Part Two in that they deal not with creates suitable conditions for them within the excreted infections per se but with insects that may geographical range shown in figure 36-1. transmit both excreted and nonexcreted infections and The eggs of Culex pipiens mosquitoes are laid in that breed in or visit excreta or sewage. This chapter clumps ("rafts") of 50-250. The larvae hatch after 1-2 describes the Culex pipiens mosquitoes, which breed in days and then pass through four stages (instars), sewage and sullage and are a vector of Bancroftian lasting a total of 1-2 weeks at tropical temperatures, filariasis. Because of the very different nature of the during which they breathe air through a siphon at the subject matter, the standard headings adopted for posterior end while hanging diagonally from the chapters 9-35 have not been used in this chapter and surface film of the water (figure 36-2) and feed on chapter 37. detritus. The comma-shaped pupae swim about, like the larvae, and give rise to the adult mosquito after about two days (figure 36-2). The female adults mate The Biology of Culex pipiens Mosquitoes once only in the first few days of life and, as with other mosquitoes, only the females feed on blood. One blood The immature stages (eggs, larvae, and pupae) of meal is taken between the laying of each egg raft. mosquitoes live in water. Among the many mosquitoes Feeding takes place at night, and the favored blood able to transmit human disease, three groups of species sources are man and birds. are particularly important. One group, the Culex pipiens complex, has the most relevance to sanitation methods because it favors polluted water for breeding. Bancroftian Filariasis Of the other two groups, Anopheles species (vectors of malaria) breed in stretches of fairly clean water, such as In some parts of the world, especially in continental flood or irrigation water, and Aedes aegypti (vector of Asia, Culex pipiens mosquitoes are the vectors of the yellow fever, dengue, and dengue hemorrhagic fever causative agent of Bancroftian filariasis, the nematode viruses) breeds especially in clean water stored in pots, worm Wuchereria bancrofti (figure 36-1). W. bancrofti cisterns, and the like, unless these are carefully screened is transmitted by quite different mosquito species in to prevent their access. different parts of the world. In some places the vector is The Culex pipiens complex consists of several closely Anopheles (the malaria-carrying mosquito genus), related forms such as C. p. pipiens, C. quinquefasciatus' whereas elsewhere the vectors are Aedes mosquitoes. (previously called C. p.fatigans, C. p. quinquefasciatus, The adult worms live in the lymphatic ducts of man. and C.fatigans), C. p. molestus, and C. p. pallens. These Embryos (microfilariae) are shed in vast numbers into vary in such physiological characters as ability to the blood stream. In the periodic form of the disease, hibernate or lay their first batch of eggs without taking which is the only form transmitted by C. pipiens, the a blood meal. One or another of the members of the C. microfilariae only occur in the blood at night, and the routine mcthod of diagnosing thc infection is by 1. This description was proposed by Sirivanakarn and White examination of blood samples taken at night for the (1978) and later adopted by the World Health Organization. presence of microfilariae. If a susceptible mosquito 483 484 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA < \\ //t ° aS-\~~r7 44 X~~~~~~~~~~~~~~~~~~~~~~~~~~0 0 - w!9 4/1// "aF/F I /_ H NORTHERN AND SOUTHERN LIMITS Fr RESIDUAL FILARIASIS OF THE RANGE OF CULEX PIPIENS Lii TRANSMISSION BY CULEX PIPIENS FILARIASIS TRANSMITTED MAINLY BY OTHER SPECIES OF MOSQUITO E FILARIASIS TRANSMITTED MAINLY BY CULEX PIPIENS Figure 36-1. Known geographical distribution of Culex pipiens mosquitoes and BancroJfianfilariasis ingests microfilariae during a blood meal, they develop areas-for example, Japan, Western Samoa, China, inside the mosquito over a period of 10-15 days to and French Polynesia. The other approach to filariasis become infective larvae. When the mosquito feeds control, by control of the vector mosquitoes, is dealt again, they may be reintroduced into another person with below after further consideration of their ecology. where male and female worms establish themselves in Figure 36-1 shows the areas in the world in which the lymphatic system and recommence the cycle of Bancroftian filariasis is known to occur. More microfilaria production. extensive surveys may reveal further infected areas; for Several years (often 20 or more) after the adult example, in India the known infected areas have worms have established themselves, a reaction by the steadily expanded as surveys have increased in tissues of the infected person may block the lymphatic thoroughness. Recent estimates in India are that 8 vessels and so prevent the return of the lymph. This million people are infected, and that a population of 136 may lead to swellings of the genitalia, legs, or arms. The million is at risk from the disease. (ICMR 1971). first is known as hydrocele, whereas the stage of gross deformity of the legs or arms is called elephantiasis. Filariasis is not a lethal disease. The economic impact Culex pipiens as a Vector and as a of the disablement that it causes has not been assessed, Nuisance but the disease is much feared in areas where it is endemic. The member of the Culex pipiens complex most There is no vaccine available as yet against filariasis, widespread as a vector of Bancroftian filariasis is Culex but the drug diethylcarbamazine is effective against the quinquefasciatus. C. quinquefasciatus is the principal filarial worms while they are still alive and before severe vector in South America, on the coast of East Africa, symptoms of the disease appear. The drug may cause and through much of Asia (see figure 36-1). However, unpleasant side effects if used at the dosages required in China and Japan the vector is C. p. pallens, whereas for effectiveness in a short course of treatment. in Egypt it is C. p. molestus (Southgate 1979). C. p. Nevertheless, drug treatment has been effective in some molestus is also the vector of Rift Valley fever in Egypt, CULEX PIPIENS AND BANCROFTIAN FILARIASIS 485 Not only in West Africa, but throughout the tropics in recent years there has been rapid urbanization without adequate excreta or sullage disposal systems, and this has led to massive increases in C. > , ^quinquefasciatus numbers. It is feared that this is leading to corresponding increases in filariasis incidence. Quite apart from their role as disease vectors, C. quinquefasciatus are the main nuisance mosquitoes of tropical urbanized areas. They can be extremely unpleasant, especially where most of the population sleep out of doors or in inadequately mosquito-proofed houses. In Calcutta (India), over 700 C. quinquefasciatus bites per person per night have been recorded (Gubler and Bhattacharya 1974). In Pondicherry (India) in January, over 9 million Culex quinquefasciatus mosquitoes are emerging per day, and _ f>\ 90 percent of these are breeding in drains (Menon and Rajagopalan 1980). The Association of Culex pipiens with Polluted Water --- f~ - -The breeding places of C. pipiens are mostly / ~-\- associated with sewage or sullage; stagnant open drains are perhaps the most prolific source. In many cases these drains were installed originally for storm Figure 36-2. Larval and adult Culex pipiens mos- water but, with the increased human population and quitoes. (a) Two larvae and one pupa of C. pipiens inadequacies in the sewage disposal system, they have mosquitoes suspended from the water surface. (b) An become the repository for sewage and sullage and tend adult C. pipiens taking a blood meal. (Photos: R. Page, to block and stagnate. Even if excreta are not disposed Department of Medical Entomology, London School of in open drains, the use of such drains for sullage of Hygiene and Tropical Medicine, London, UK) water creates equally important C. pipiens breeding places if the water is allowed to stagnate. where there were explosive epidemics during 1977 and Pit latrines are another important breeding place, 1978 (Hoogstraal and others 1979). although this problem can be avoided if it is possible to As indicated in figure 36-1, there are large areas of dig the latrines so that they do not reach the water the world where Culex pipiens exists but there is no table. The installation of pit latrines in some villages in Bancroftian filariasis or where other species of East Africa has been associated with invasion of these mosquito are the main vectors of filariasis. C. rural areas by C. quinquefasciatus. Where septic tanks quinquefasciatus has increased substantially in density and soakage pits are not made mosquito-proof, or are in West African towns over the last 30 years, but at cracked, they too can become major breeding places. present filariasis is mainly a rural disease transmitted Examples of the relationship between Culex breeding by Anopheles species in the region. There is evidence and the availability of polluted water are given below. that West African strains of C. quinquefasciatus have a It is thought that before 1926 Bancroftian filariasis relatively low susceptibility to W. bancrofti, in contrast transmitted by C. quinquefasciatus was limited in Sri to Indian strains of C. quinquefasciatus. However, there Lanka to two towns. However, between 1926 and 1946 is no cause for complacency about the danger of high there was compulsory introduction of a system of C. quinquefasciatus populations in West Africa because bucket latrines in the southwestern part of the island of the risk that the local W. bancrofti will adapt to the and 30,000 were installed, each with an associated new potential vector that has become available in cement-lined pit to receive water used for ablution after recent years. defecation. These pits provided breeding sites for C. 486 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA quinquefasciatus and appeared to be associated with a pit latrines C. quinquefasciatus biting densities rose major spread of filariasis. As part of a control program, dramatically in the wet season, whereas in villages with 10,874 of the catch pits were converted to the water- soakage pits only there was little seasonal variation. seal type with a subsidy of 60 rupees each. Additional Chlorpyrifos (Dursban) was an effective and persistent control measures included the use of organophosphate larvicide in the pit latrines but has high mammalian insecticides and campaigns to dispose of water-filled toxicity. Drinking water wells were often dug close to receptacles. In areas where the control program was in pit latrines, and there was serious risk of diffusion of progress, the proportion of mosquitoes infected with chlorpyrifos from flooded pit latrines to drinking Wuchereria bancrofti declined from 12-24 percent in water. Digging pit latrines less deeply so as not to reach 1949 to 0.7-3.3 percent in 1962 (Abdulcader 1967). the water table was considered the most effective Afridi and Abdul Majid (1938) reported that control method. Temephos (Abate), with low mam- measures against C. quinquefasciatus larvae had been malian toxicity and lower persistence than chlor- taken throughout the inhabited area of New Delhi and pyrifos, was recommended for use as a larvicide in for half a mile around it, but a severe C. soakage pits. quinquefasciatus biting nuisance was experienced Goettel, Toohey and Pillai (1980) studied Aedes and during the months of April and May. It was thought Culex breeding in Suva (Fiji). C. quinquefasciatus that the breeding source was a suburban sewage farm larvae were found in half of all septic tanks sampled. C. in which very large numbers of larvae were found when quinquefasciatus breeding, unlike that of Aedes species, sewage was pumped onto fields of grass and into showed no seasonal trend, and this suggests that stagnant connecting channels. Evidence that the city's breeding was associated more with permanent water problem did originate from this source came from bodies created by human water use than with trapping data that showed a gradation in mosquito ephemeral water bodies created by rainfall. density as one proceeded for several kilometers away Bang, Sabuni and Tonn (1973) recorded the changes from the sewage farm. Also, in the traps nearer the farm in mosquito populations between 1954 and 1971 in a higher proportion of males was obtained, which is Dar es Salaam (Tanzania). Whereas urbanization and generally an index of nearness to the breeding source. routine control measures had led to a reduction in About 138,000 mosquitoes marked with silver dust malaria vectors, there had been a steady increase, were released at the sewage farm. Eleven marked despite control measures, in the population of C. mosquitoes were recaptured among the many thou- quinquefasciatus. Part of the change was attributed to sands caught in the traps. Two of the recaptures were at urbanization, which had led to a reduction of the clean more than 3.5 kilometers from the release point, the pools suitable for Anopheles and to an increase in farthest being at 5 kilometers. These data indicate that polluted water sources suitable for C. quinquefasciatus. C. quinquefasciatus from one massive breeding source Several permanent swamps known for decades as could infest the whole city and emphasize the great sources of malaria vectors had become Culex breeding dispersal power of this species when conditions are sites owing to pollution from new human settlements. favorable. In an uncontrolled area of Dar es Salaam, for example, Subra and Hebrard (1975) studied the ecology of C. the C. quinquefasciatus population had increased since quinquefasciatus larvae in the Comoro Islands, where 1954 at an annual rate of 0.97 females per room. this mosquito is the main vector of Bancroftian The Culex breeding problem in Asian towns and filariasis. Its main breeding places were pit latrines, cities has been reviewed by Singh (1967). Many towns soakage pits used for washing water, water-filled in Asia are growing rapidly, and the sewerage receptacles, and streams that became blocked by sand arrangements are not keeping pace; there is a bars and stagnated in the dry season. Of the three main consequent increase in exposed polluted water that is ethnic groups on the islands, the Sakalava (Malagasys) available for breeding by C. quinquefasciatus. The had soakage pits but no latrines in their villages; the situation is exemplified by Rangoon (Burma), where Anjouan had pit latrines but no soakage pits; and the breeding is intense in drains, swampy ground near Moharais had both latrines and soakage pits. In bucket latrines, pools polluted by effluent from the semiurbanized areas the proportion of houses with pit overloaded and defective waterborne sewage systems, latrines, soakage pits, or both was greater than in rural unprotected septic tanks, and pit latrines in swampy areas. Pit latrines did not contain water or become ground. Both Hyderabad and Bangalore (India) were breeding places unless ground water entered them, free of C. quinquefasciatus in the 1940s, but with which only occurred in deep pits and in the wet season increases in population and industrialization with when the water table rose. Thus, in villages with deep poor sanitation the mosquito is now widespread, and CULEX PIPIENS AND BANCROFTIAN FILARIASIS 487 filariasis transmission is occurring. The presence of Culex pipiens Breeding in Waste extensive C. quinquefasciatus breeding does not Stabilization ponds necessarily lead to intense filariasis transmission, since this is only possible where the adult mosquito life span Under certain circumstances, waste stabilization is long enough to allow maturation of the parasite. In ponds can become important breeding places for Culex the humid parts of south India the mosquito life span is mosquitoes. Beadle and Harmston (1958) studied long throughout the year, but in northwest India it is twenty-six stabilization ponds in the USA. The main only long enough to allow transmission from July to mosquito species found was Culex tarsalis, which is the October. vector of western equine encephalitis virus. The Useful reviews of Culex breeding and filariasis in presence or absence of mosquito breeding in the ponds Asia and Africa have also been prepared by Gratz was closely correlated with the presence or absence of (1973) and Hamon and others (1967). From this and emergent or overhanging vegetation. Smith and Enns other literature, several matters of grave concern (1967) also studied stabilization ponds in the USA. emerge. First, rapid urbanization unaccompanied by Two ponds receiving animal waste were overloaded, adequate excreta disposal and drainage infrastructure frequently anaerobic, and had overhanging or causes substantial increases in the Culex population, emergent vegetation. They produced large numbers of and these may cause an increase in filariasis Culex pipiens and other Culex species (30,000-60,000 transmission, prevalence, and intensity of infection. larvae in a standard sample). This contrasted with Second, C. quinquejasciatus is becoming increasingly 20-600 larvae in comparable samples from well- numerous in urban areas of Africa where, at present, planned and well-maintained municipal sewage ponds. the vector of filariasis is the Anopheles mosquito. If W. Steelman and Colmer (1970) studied two ponds, also bancrofti became adapted to transmission by C. in the USA. One was newly dug, and the other had been quinquefasciatus in these areas of Africa, the con- used for 6 years for the reception of effluent from a pig sequences would be most serious. Third, there is some farm. For the first 9 months of its life the new pond was evidence that Anopheles and Aedes mosquitoes, filled with rainwater and from wells, but subsequently commonly known as clean water breeders, are effluent from the farm began to be introduced. In the adapting to take advantage of the breeding opportu- old pond large populations of C. quinquejasciatus nities provided by the proliferation of contaminated larvae were found at each survey. In the new pond no C. surface water bodies in fast-growing tropical cities. quinquejasciatus was found, and the insect larvae Chinery (1969) reported that Anopheles gambiae and before and for a few months after the introduction of Aedes aegypti were found breeding in earth drains, effluent differed markedly from those in the old pond. concrete drains, septic tanks, soakaways, and pit In the old pond 7,000 to 13,000 coliform bacteria were latrines in Accra (Ghana). Yao (1975) found Anopheles found per milliliter. None was found in the new pond stephensi larvae in puddles of sewage effluent outside before introduction of effluent, but 7,000 per milliliter Lahore (Pakistan). were found 5 months after this introduction, and at It should be pointed out that not all recent increases about this time C. quinquefasciatus larvae began to be in Culex pipiens populations are associated with found in the new pond. After 2 years the bacterial and sewage and sullage. In villages near Delhi (India) large insect populations of the two ponds had become very numbers of seasonally disused irrigation wells, which similar. Laboratory cage studies showed that suspens- had been dug as part of the "green revolution" in ions of Escherichia coli, E. freundii, and E. intermedia agriculture, are major sources of C. quinquefaisciatus were more attractive as oviposition sites for C. breeding (Yasuno 1974). In Egypt a very substantial quinquefasciatus than were suspensions of Aerobacter increase in the C. p. molestus population over the past aerogenes, and that all these suspensions were much 20 years has been promoted by poorly maintained more attractive than sterile water. wells, stagnant pools of spilled water near public taps Yao (1975) reviewed limited data on mosquito and handpumps, and by the drastically altered breeding in waste stabilization ponds in India and irrigation practices and rising water tables that have concluded that pond colonization by vegetation was followed the opening of the Aswan High Dam in 1971. the main factor predisposing to breeding. In his own The increased vector population, together with other experiment outside Lahore (Pakistan), Yao (1975) factors, is responsible for a marked increase in the studied four ponds (each 46 meters by 18 meters in plan prevalence and intensity of infection with Bancroftian and 1.2 meters deep) receiving domestic sewage and an filariasis in Egypt and a widening geographical range experimental irrigation system. The ponds were lined (Southgate 1979). with bricks, were in good operating order, and had no 488 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA emerging or encroaching vegetation. Two of the ponds gave satisfactory results. A granular formulation of the showed no evidence of mosquito breeding, whereas the organophosphate chlorfenvinphos (Birlane) was tested other two had minimal breeding in one month out of at a dosage of 2.5-5 grams per pit latrine. This five. Many C. quinquefasciatus larvae were found in a completely prevented breeding for 9- 0 days. One man roughly vegetated earth pond receiving effluent. can apply granules to thirty pits per hour, and it was Breeding ceased, however, when the vegetation was estimated that the labor costs of a program would be 20 cleared. Vegetated puddles of effluent in the irrigation percent of those for oiling. Chlorfenvinphos has fairly canals were also the sites of prolific breeding of C. high acute mammalian toxicity, and the possibility of quinquefasciatus, C. theileri, and Anopheles stephensi. seepage from pit latrines into streams must be These studies have shown that the most important considered. measure to prevent mosquito breeding is avoidance of In Guyana the breeding place of C. quinquejasciatus vegetation hanging into or emerging through the is principally pit latrines and secondarily clean water in surface of the ponds. Other ecological factors drums and tanks. Spraying of latrines with oil was associated with the presence or absence of mosquito carried out at a dosage of about 650 grams each, which breeding in stabilization ponds have been studied in prevented breeding for 4-6 weeks. The cost of the oil the USA, and studies of this subject in tropical for a monthly program of spraying over 2,000 latrines countries would be very valuable. Little is known was US$71. In addition, all unused drums containing about the relationships between water pollution and water were turned over, but some were used for female oviposition behaviour or about the ability of drinking water and could not be emptied or sprayed. mosquito eggs to develop through their larval and The campaign produced a dramatic reduction in the pupal stages to become adults. The literature, reviewed density of mosquitoes in houses. In addition, the by Darwall (1979), suggests that location, salt filaricidal drug diethylcarbamazine was issued to all concentration, organic pollution, dissolved oxygen, the inhabitants of the area. The result of the program surface tension, larval nutrients, and aquatic flora and was that the proportion of filaria-infected mosquitoes fauna may be important determining factors. Even was reduced from 17.7 to 2.2 percent (Burton 1967). after 70 years of research, however, these relationships Graham and others (1972) reported a field trial in are poorly understood, and more research is urgently Rangoon (Burma) of C. quinquefasciatus control in an required. area of 4 square kilometers. Breeding of the mosquitoes was mainly in open drains, which frequently became blocked by debris and the activities of rats. The drains Methods for Culex pipiens Control had originally been built for stormwater, but they were now used for sewage because of the deterioration of the There are two approaches to Culex control, and underground waterborne sewage system and the successful control programs will almost always apply a increase in population of the city. Additional breeding combination of both of them. The two approaches, sources included soakage pits for sullage, improperly which are clear from the discussion above on preferred maintained septic tanks, and latrines. Much of the C. breeding sites, are modifications of the physical quinquefasciatus population rests and feeds out of environment and the use of insecticides or other doors, so that a house-spraying program against adult chemicals. Before describing these approaches, it is mosquitoes would have been inappropriate, as would instructive to report a few case studies of control efforts the use of organochlorine insecticides because of in various environments. resistance. Among the organophosphate insecticides, fenthion has been found to be one of the most effective Case sttidies in contr-ol and persistent as a larvicide in polluted water, and this chemical was used for the trial in the form of White (1971) reviewed the C. quinquefasciatus emulsifiable concentrate applied with a compression control practices in East Africa and pointed out that sprayer to larval breeding sites, especially drains and malathion is unsuitable as a larvicide in polluted water septic tanks. No resistance to fenthion appeared over because it is rapidly destroyed at acid or alkaline pH. the 3-year period of the trial. The overall effect of the 3- Oiling of breeding places is frequently used, but in year program was an average reduction by 97 percent sullage pits detergents emulsify the oil and reduce its in the man-biting rate in the trial area compared with a efficiency. Experiments with 110 milliliters of Flit comparison area, where the municipality's routine mosquito larvicide oil per pit latrine gave poor control, program of oiling breeding sources was in progress. but dosages of 450 milliliters of used engine oil per pit Apart from the much greater effectiveness of the C ULEX PIPIENS AND BANCROFTIAN FILARIASIS 489 fenthion program, it was considered that the higher make it impossible for the egg-laying female to reach labor and transport costs of applying the necessary the site. The particular strategies that might succeed in large volumes of oil made oiling more expensive than a particular place can only be designed after a detailed the use of fenthion. The authors considered this field survey of Culex breeding in that area. In other words, trial to be a model for what could be done in other control methods should be sharply focussed upon tropical cities. eliminating, or restricting access to, the known primary Culex control in Singapore was described by Chan breeding sites. The main methods of environmental Kai-Lok (1973). Surface flood water drains had control include: originally been built as an Anopheles control measure, but these were now used for sullage and had become i Avoidance, if at all possible, of using open drains for breeding places for C. quinquefasciatus. About 78 sewage or sullage percent of the C. quinquefasciatus breeding in the city * If the use of open drains for sewage or sullage is was in these concrete drains. Much of the remainder absolutely unavoidable for the time being, pre- was in cracked septic tanks. A survey indicated that 6 vention of stagnation in the drains by frequent percent of the septic tanks in the city were cracked and cleaning and the provision of adequate garbage had C. quinquefasciatus breeding. Control measures disposal services used in the drains consisted of cleansing to improve the a Fitting and maintenance of mosquito-proof netting flow rate and oiling with Flit MLO refined light oil. over ventilation pipes on septic tanks, aquaprivies Guppy fish (Poecilia reticulata) had been established in and improved pit latrines some concrete drains and canals and had had a a Sealing and repairing covers on septic tanks, significant effect in controlling C. quinquefasciatus. soakage pits, and improved pit latrines Sealing of inspection slabs on septic tanks reduced a Fitting of water seals on pit latrines breeding. a Clearance of vegetation from waste stabilization An experiment to eradicate Bancroftian filariasis by ponds. vector control in a village in Nagasaki Prefecture (Japan) was recorded by Omori, Wada and Oda Pit latrines are becoming increasingly commonplace (1972). Culex pipiens pallens bred in ditches and in poor urban and rural communities. If they are well polluted pools in the village and was the primary vector constructed and well maintained, they provide an of Bancroftian filariasis. A program of vector control acceptable excreta disposal method for those families was carried out for 9 years using diazinon as a house that cannot afford more elaborate systems. But if the spray against adult mosquitoes and for treatment of pits are wet, owing to a high water table or the addition breeding sites. The latter treatments were carried out of excess washing water, they provide an ideal breeding about twenty times per year during the mosquito ground for Culex pipiens mosquitoes. Four approaches breeding season, the target dosage being 1 milligram to overcoming this problem are recognized. First, to per liter. No filaricidal drugs were given, but all replace the drop-hole slab by a pour-flush slab, thus members of the village population (about 500) were providing a water seal that prevents the entry or exit of examined annually for microfilariae. Entomological mosquitoes to the pit. Second, to install a ventilation observations showed partial suppression of the C. p. pipe with mosquito-proof gauze at the top (see figure pallens density in the first two years of treatment 36-3). Third, to install exit traps over the squat holes. relative to the pretreatment year. During the last 7 Fourth, to spray the pits with oil or insecticide. years of treatment there was almost complete The role of vent pipes (as on ventilated improved suppression of the vector. The prevalence of human pit-VIP-latrines) in controlling Culex breeding was microfilaria carriers declined from 14 percent before investigated in Dar es Salaam (Tanzania) and the trial to 0.5 percent at the end of it. This experiment Gaborone (Botswana) by Curtis and Hawkins (1982). is one of the very few demonstrations that filariasis in It was found that 67 percent of Culex mosquitoes some areas can be drastically reduced solely by vector emerging from the pits did so via the vent pipe rather control if this is continued long enough for the adult than the squat slab. If the vent pipe was properly worms in the human population to die out. screened at the top, these mosquitoes could not escape. The effect of vent pipes on mosquito production was Control by modifyin thephysicalemconsiderably less than their effect on blowfly production, of which about 90 percent went up the Control methods based on environment modi- vent. Some latrines produced over 1,000 Culex per fication must either eliminate the breeding site or night through the squat slab, despite having a vent pipe. 490 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA Insect traps placed over the squat hole can be used method. The method works by interfering with larval on pit latrines with or without vent pipes (figure 36-3). respiration, and studies in Guyana showed that it can The traps can be cheaply made of a box or tin partly be a very effective method in pit latrines if con- covered in mosquito proof gauze and with a gauze cone scientiously applied (Burton 1967). Light oils with high in the bottom surface. Mosquitoes and flies enter the spreading pressures have been developed especially trap through this cone, presumably attracted upward for mosquito control ("Flit MLO") and are routinely from the pit by light and/or fresh air. They do not used for example, in Singapore-but relatively large readily find their way out again, but if some do they go amounts of transport and labor are required for an back into the pit. Insects caught in the traps die there in effective oiling program. a day or two. No provision is made for removing the Organophosphate insecticides such as temephos corpses, but ants have been seen removing dead (Abate), chlorfenvinphos (Birlane), chlorpyrifos mosquitoes. In future a lizard might be placed in each (Dursban), diazinon (Basudin), and fenthion (Baytex) trap to eat captured insects. Provision is made, with are lethal to mosquito larvae at extremely low appropriately placed flaps, to block other easy exit concentrations (much less than 1 milligram per liter) routes, but a precision fit is not necessary because and can be applied as emulsifiable concentrate or insects emerging from pits take the obvious route into absorbed into granules, which greatly reduces the the well-lit and aerated trap rather than follow the transport and labor required compared with oiling. more tortuous alternatives. This is one of the The chemicals are fairly expensive, but temephos, advantages of a trap as compared with a lid- chlorpyrifos, and fenthion remain effective for several mosquitoes will eventually find small imperfections in weeks in stagnant polluted water, so that very frequent the fitting of a lid. treatment is not necessary. Large-scale urban trials The principle of the trap is readily understood, and have shown substantial suppression of adult biting catches of mosquitoes or flies obtained from heavily populations as a result of prolonged application of infested pits are impressive and informative in showing fenthion in Rangoon (Burma; Graham and others the householder where an insect pest problem 1972), chlorpyrifos and temephos in Bobo-Dioulasso originates and that it can be stopped at source by the (Upper Volta; Subra, Bouchite and Gayral 1970), "self-help" measure of always ensuring that the trap is chlorpyrifos in Dar es Salaam (Tanzania; Bang, put back in place after using the pit. Initial trials in Dar Sabuni and Tonn 1975), chlorpyrifos in Morogoro es Salaam and Gaborone (Curtis 1980; Curtis and (Tanzania; Mrope. Bang and Tonn 1974), and Hawkins 1982) on a variety of pit latrines, cess pits, and chlorfenvinphos in Tanga (Tanzania; White 1971). It a soakage pit produced large catches of C. quinquefas- has been shown in Japan that applications of diazinon ciatus and blowflies. There were uniformly favorable to breeding places several times each year for 9 years reactions of householders to the traps, which were suppressed C. p. pallens populations and reduced the always found in place when checks were made. It incidence of filariasis virtually to extinction (Omori, remains to be seen whether such cooperation can be Wada and Oda 1972). achieved over the long term by an appropriate initial Despite the success achieved with organophosphate program of public information followed by periodic insecticides, it would be unwise to rely on them checking on the traps for correct usage and for the exclusively. It seems possible that they might adversely repair of any damage. It also remains to be affect the essential microbial activity in waste demonstrated that the area-wide use of traps is effective stabilization ponds, septic tanks, and aquaprivies, and in suppressing the density of C. quinqueJasciatus and this question demands investigations of the kind blowflies in houses. already conducted with regard to the use of kerosene as an insecticide (Razeghi, Lawrence and King 1972). In Control by insecticides and oils addition, there are reports from many parts of the world of the evolution of resistance to organophos- Control of C. pipiens breeding by environmental phates in C. pipiens mosquitoes (see, for instance, management methods alone is often not feasible, and Curtis and Pasteur 1981; Hamon and Mouchet 1967). insecticidal methods must also be considered. C. Recent experience in Tanzania provides a good pipiens mosquitoes are now almost universally example of the problems caused by the development of resistant to organochlorine insecticides such as DDT organophosphate resistance in C. quinquefasciatus. and dieldrin (Hamon and Mouchet 1967). Gas oil or Following the trials in Dar es Salaam and Morogoro used lubricating oil are routinely used on mosquito described above, chlorpyrifos was adopted in the early breeding places in many tropical cities as a control 1970s for routine spraying (every 10 weeks) of all pit Cross section 491 Insert-proof PVC coated fibreglass mesh 4litre plastic paint container J lcm diameter ...... '-_ hole ....... Lid of paint container Methods of fixing traps Over mass produced squatting plate Over traditional squatting plate PLAN SECTION PLAN SECTION I SL o pn c netalr e metal met 0 I ~~~~~~~Drop Squatting hole I Meta flap \ Slb slab pivoted on Drop wire between hole footrests Over pedestal seat On vent pipe .--Trap Seat *'. Seatover -Trap Foam . Sheet rubber- metal tKidn seat Fibreglass strips Bindingof pedestal adhesive tape Vent _ pipe- Slab Drop hole Figure 36-3. Insect traps Jor pit latrines. The traps shown can be fitted over the squat hole or seat of a latrine, or over the vent pipe, to catch flies and mosquitoes emerging from the pit. (from Curtis and Hawkins 1982; reproduced by permission of the Royal Society of Tropical Medicine and Hygiene) 492 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA latrines and soakage pits in Dar es Salaam. When the mosquito-control activities. This is especially impor- program was initiated, the insecticide residue remain- tant in those parts of the world where C. pipiens ing up to 10 weeks after a spraying was sufficient to give mosquitoes are the vectors of Bancroftian filariasis, and continuous control of larvae. However, unpublished it will become even more crucial if Anopheles and Aedes data of Curtis and others indicate that the resistance species adapt locally to use polluted water as breeding that has evolved in Tanzania is now seriously sites in urban areas. interfering with the effectiveness of the program. Freshly sprayed chlorpyrifos is able to kill the resistant larvae, but after the insecticide residue has been degraded, diluted, or both, for I to 4 weeks it is no Literature Cited longer able to kill them. Thus, mosquito breeding can proceed in the sprayed pits for a large fraction of the 10- Abdulcader, M H M. (1967). The significance of the Culex week spraying cycle. The program already costs about pipienslatigans Wiedemann problem in Ceylon. Bulletin of U 13,000 per yer fo th imotto of insecticide, the World Health Organization, 37, 245-249. US $135,000 per year for the importation of insecticide, Afridi, M. K. and Abdul Majid, S. (1938). Observations on and increasing the frequency of spraying would require the range of dispersion of Culexfatigans and its infiltration considerable additional expenditure, as well as the into the Delhi urban area. Journ-'al of thle Malaria Instituite employment of more spray men. of India, 1, t55-167 It may be that practical alternatives to conven- Bang, Y. H., Sabuni, 1. B. and Tonn, R. J. (1973). Mosquito tional insecticides will eventually become widely applic- control service in Tanzania. III. The effects of mosquito able using insect growth regulators, lipid monolayers control and urbanization on mosquito populations in Dar (Levy and others 1980), insoluble foams, biological es Salaam, Tanzania, from 1954 to 1971. Unpublished control by pollution-tolerant fish, algae (Ilyaletdinova document, WHO/VBC/73.440. Geneva: World Health 1978), microorganisms, or genetic systems based on Organization. cytoplasmic incompatibilit and.genesconfi -(1975). Integrated control of urban mosquitoes in cyopsasmc incomtibility .an gene conei Dar es Salaam using communitv sanitation supplemented by larviciding. East African Medical Journal, 52, 578-588. however, should be viewed only as ancillary to the Beadle, L. D. and Harmston, F. C. (1958). Mosquitoes in installation and maintenance of well-designed excreta sewage stabilization ponds in the Dakotas. Mosquito and sullage disposal systems that minimize the News, 18, 293-296. breeding opportunities available to C. pipiens. Burton, G. J. (1967). Observations on the habits and control of Cuilex pipiensfatigans in Guyana. Bulletin oJftie World Health7 Organization, 37, 317--322. Conclusions Chan Kai-Lok (1973). Culexfatigans control in Singapore. In l'ector Conitrol in South-East Asia, eds. Chan Yow- It is clear from this review that water supply projects Cheong, Chan Kai-Lok and Ho Beng-Chuan, pp. and on-site sanitation systems have the potential for 150 -57 Bangkok SoutheastAsiaMinisterofEducation greatly increasing the population of C. pipiens Organization. greatly oesin the townsan of C el Chinery. W. A. (1969). A survey of mosquito breeding in mosquitoes in tropical towns and cities. Of special Accra. Ghana, during a two-year period of larval mosquito concern are inadequately maintained open drains, control. I. The mosquitoes collected and their breeding flooded pit latrines, soakage pits, and septic tanks. In places. Ghan1a Medical Journal. 8, 266-274. villages, the construction of pit latrines in areas with Curtis, C. F. (1980). Insect traps for pit latrines. Mosquito high water table, and increased water usage leading to News, 40, 626-628. ponded sullage, may bring the traditionally urban Curtis, C. F. and Hawkins, P. M. (1982). Entomological problem of C. quinquefasciatus to these rural sites. studies of on-site sanitation systems in Botswana and Minimizing this problem depends on a carefully Tanzania. Transactions of the Royal Society of Tropical thought-out combination of correct design features for Medicine and HvgiC7ne. 76. 99-108. drainage and on-site sanitation, of appropriate self- Curtis, C. F. and Pasteur. N. (1981). Organophosphate resistance in vector populations of the Culex pipiens help action by the community (for intance, using exit complex.Bulletin of'EntomologicalResearch,71, 153-161. traps on pit latrines and keeping open drains free from Darwall, A. M. (1979). Pollution tolerance of various species garbage), and of larvicide-spraying programs. It is of mosquito. M.Sc. dissertation. London: Imperial College necessary for those designing and implementing water of Science and Technology. supply and sanitation schemes to discuss their work Goettel. M. S., Toohey, M. K. and Pillai. J. S. (1980). The with entomologists having detailed local knowledge, urban mosquitoes of Suva. Fiji: seasonal incidence and an and sullage disposal systems that will minimize the evaluation ofenvironmental sanitation and ULV spraying C ULEX PIPIENS AND BANCROFTIAN FILARIASIS 493 for their control. Journal of Tropical Medicine and Hygiene, mosquitoes in Nagate village, Nagasaki Prefecture. In 83, 165-171. Research in Filariasis and Schistosomiasis, ed. Yokogawa, Graham, J. E., Abdulcader, M. H. M., Mathis, H. L., Self, L. S. M., vol. 2, pp. 21-30. Tokyo: University of Tokyo Press and Sebastian, A. (1972). Studies on the control of Culex (and Baltimore, Md.: University Park Press). pipiensfatigans Wiedemann. Mosquito News, 32, 399-416. Razeghi, N. H., Lawrence, C. H. and King, E. D. (1972). The Gratz, N. G. (1973). Mosquito-borne disease problems in the effects of a larvicide on waste stabilization pond urbanization of tropical countries. Critical Reviews in performance. Journal of Environmental Health, 34, Environmental Control, 3, 455-495. 614-616. Gubler, D. J. and Bhattacharya, N. C. (1974). A quantitative Singh, D. (1967). The Culex pipiens fatigans problem in approach to the study of Bancroftian filariasis. American South-East Asia. With special reference to urbanization. Journal of Tropical Medicine and Hygiene, 23, 1027-1036. Bulletin of the World Health Organization, 37, 239-243. Hamoni, J., Burnett, G. F., Adam, J. P., Richenbach, A. and Sirivanakarn, S. and White, G. B. (1978). Neotype Grjebine., A. (1967). Culex pipiens fatigans Wiedemann, designation of Culex quinquejasciatus. Say (Diptera: Wuchereria bancrofti Cobbold, and economic develop- Culicidae). Proceedings of the Entomological Society of ment of tropical Africa. Bulletin of the World Health Washington, 80, 360-372. Organization, 37, 217-237. Smith, W. L. and Enns, W. R. (1967). Laboratory and field Hamon, J. and Mouchet, J. (1967). Culex pipiens Jatigans investigations of mosquito populations associated with Wiedemann resistance to insecticides. Bulletin of the World oxidation lagoons in Missouri. Mosquito News. 27, Health Organization, 37, 277-286. 462-466. Hoogstraal, H., Meegan, J. M., Khalil, G. M. and Adham, F. Southgate, B. A. (1979 ). Bancroftian filariasis in Egypt. K. (1979). The Rift Valley fever epizootic in Egypt 1977-78. Tropical Diseases Bulletin, 76, 1045-1068. 2. Ecological and entomological studies. Transactions oJ Steelman, C. D. and Colmer, A. R. (1970). Some effects of the Royal Society of Tropical Medicine and Hygiene, 73, organic wastes on aquatic insects in impounded habitats. 624-629. Annals of the Entomological Society of America, 63, ICMR (1971). Assessment of the National Filaria Control 397-400. Programme 1I0,.,. 1961-1971.New Delhi: IndianCouncil Subra, R., Bouchite, B. and Gayral, P. L. (1970). Large-scale of Medical Research. evaluation of Dursban and Abate in the control of Culex Ilyaletdinova, S. G. (1978). Algal control of bloodsucking pipiens fatigans in Bobo-Dioulasso (Haute Volta). insects. Water Resources, 5, 619-621. Medecine Tropicale, 30, 393-402. Levy, R., Garrett, W. D., Chizzonite, J. J. and Miller, T. W. Subra, R. and Hebrard, G. (1975). The ecology of Culex (1980). Control of Culex spp. mosquitoes in sewage pipiens fatigans larvae in an area of high endemicity of treatment systems of southwestern Florida with monomo- filariasis, Mayotte, Comoro Islands. Tropenmedizin und lecular organic surface films. Mosquito News, 40, 27-35. Parasitologie, 26, 48-59. Menon, P. K. B. and Rajagopalan, P. K. (1980). Relative White, G. B. (1971). The present importance of domestic importance of different types of breeding habitats in mosquitoes (Culex pipiens Jatigan1s) in East Africa and contributing to the population of Culex pipiensfatigans in recent steps towards their control. East African Medical Pondicherry. Itidian Journal of Medical Research, 71, Journal, 48, 266-274. 725-733. Yao, K. M. (1975). Mosquito breeding in oxidation ponds. In Mrope, F. M., Bang, Y. H. and Tonn, R. J. (1974). Proceedings of the National Symposium on Wastewater Comparative trial of three larvicides against Culex pipiens Disposal, pp. 56-61. Lahore: University of Engineering fatigans in Morogoro, Tanzania. International Pest and Technology. Control, 16, 8-16. Yasuno, M. (1974). Ecology of Culex pipiensfatigans in rural Omori, N., Wada, Y. and Oda, T. (1972). Eradication Delhi, India. Journal of Communicable Diseases, 6, experiment of bancroftian filariasis in the control of vector 106-116. 37 Flies, Cockroaches, and Excreta MANY INSECTS are associated with exereta. Those of or family Culicidae; and the flies that breed in importance to health, however, are mainly from two fecal material and also come into contact with groups of insects: the two-winged flies (Diptera) and man as adults by feeding on his food (the housefly and the cockroaches (Dictyoptera). There are many species the blowfly, families Muscidae and Calliphoridae). of Diptera, including the mosquitoes (dealt with in the Other flies cause a nuisance by invading human preceding chapter), so that this chapter concentrates habitation (families Psychodidae, Chironomidae, and on other flies and the cockroaches. Anisopodidae), may land in food, and are known to Patches of animal feces are worlds unto themselves, cause contact and inhalation allergy in sensitized with parasites, predators and dung feeders living as a persons. In addition, other families of fly community together (Laurence 1977). Manmade (Stratiomyidae, Syrphidae, Sepsidae, Ephydridae, environments with innovations such as sanitation and Phoridae, and Sphaeroceridae) are very common on waste disposal units are invaded and colonized from sewage installations or in cess pits, but normally have more natural breeding places. Waste disposal provides little contact with man and are less of a problem except two attractive materials for the development of that they can cause confusion in the identification of insects rich organic material and water. The kinds of the more important sewage-breeding nuisances. insect found breeding in human waste disposal systems Among the flies that breed in or feed on excreta, two are, in consequence, those that breed in various forms of families are implicated in particular in the carriage of decaying organic material, including feces, or those that fecal material: the Muscidae and the Calliphoridae. breed in freshwater and yet tolerate organic pollution. The most important species are the housefly (Musca Relatively few species are able to take advantage of the domestica) and species of the tropical green blowfly new opportunities for breeding provided by waste (Chrysomya). The adults of these flies will enter houses disposal, but these often appear in very large numbers. and shops readily and are attracted to human food. as The balance of a more varied fauna found in the natural well as to feces and garbage around the home. They are breeding places may be lacking in the new manmade medium to large flies, 7-10 millimeters long, and have habitats. Consequently, the numbers of insects may greyish (Musca) (figure 37-1) or green (Chrysomya) build up to a level sufficient to cause a definite nuisance body color. The larvae are maggot-like and 10-12 or endanger health. The presence of animal life in waste millimeters long when fully grown. The three larval treatment systems, where there is a mixed culture of stages are found in excreta or mixtures of excreta organisms (including the insects), is also part of the and decaying vegetable matter. For the breeding of the process of purification and breakdown of the organic housefly, Musca domestica, solid, moist, and ferment- material (Lloyd 1945; Usinger and Kellen 1955). ing matter are required; other species of Musca breed in wetter materials. Human feces are attractive to houseflies mainly in their solid state. The presence of another fly. Hermetia, in latrines renders the contents Flies Associated with Waste Disposal soupy and less attractive to houseflies. Reduction of the water content, by drainage or by killing the Hermetia The most common flies associated with waste with insecticides, causes an increase in housefly disposal are found in eleven families (Laurence 1977). breeding (Kilpatrick and Schoof 1959). In contrast, the The most important families are the flies that transmit larvae of the blowfly, Chrysomya, are found in more disease organisms from man to man: the mosquitoes, liquid feces and may liquify masses of fecal material. 495 496 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA Fgr371Tho olosa-M d . Fig hurefl37-1. Thvelom rmo ouegglt, Mduscan1 domsia (Potko:aelcomesMsu fMdclSine 20 days over the temperature range 20-300C (the higher the temperature, the shorter the period of Cockroaches are attracted by the moisture of waste development), with a minimum developmental period disposal systems of various kinds. They are also of about 1 week. No development takes place below potential carriers of fecal pathogens, and they live in 120C, and eggs, larvae, and pupae are killed at 470C and around human dwellings. They often visit human (Keiding 1976). Chrysomya (blowfly) larvae develop food when they emerge at night from their noisome from egg to adult in Sri Lanka at room temperature in daytime hiding places. Cockroaches, in contrast to the 8.5 days. very rapid turnover of the fly population, take several A survey of the insect fauna in some latrines in east months to more than a year to develop to the adult Africa and Taiwan was conducted in 1978 by B. R. stage, but large populations of adult and young Laurence. The results are summarized in table 37-1, cockroaches may be found together in the same which shows that Ci?. .. was ubiquitous. In east habitat. Also, young cockroaches resemble the adult Africa ChrysomvaW putori a was the species involved, insect, whereas fly larvae have a very different whereas in Taiwan it was Chr vsomya niegacephala. appearance from the adult fly. Flies are able to breed in Similarly, Lien and Chen (1974) reported that the much more transient habitats than cockroaches. majority of flies breeding in VilLUltS in Taipei (Taiwan) were ChrYsomnyv n7egacephala. Pit latrines are not- orious as breeding places for blowflies. Raybould Flies, Cockroaches, and Health (1966) reported that, at Amani in Tanzania, ninety pit latrines produced 3.5 kilograms of Chirysomya ptutoria Disregarding Cuttex mosquitoes. which are dis- in a single month (one adult Chrv1som_va weighs about cussed in chapter 36, there are two ways in which 50 milligrams). insects related to excreta may affect man. First, large FLIES, COCKROACHES, AND EXCRETA 497 Table 37-1. Insect fauna of "dry" latrines Location Type of toilet Insectfauna Tanzania, Kenya Pit latrines including Reed Odorless Earth Closets Chrysomya, cockroaches (ROECS) Culex quinquefasciatus, if flooded Tanzania Continuous 'multrum' type composting toilets Chrysomya in feces and vegetable fiber Musca in dry compost Telmatoscopus, Hermetia and Eristalis in wet compost Phorid flies, cockroaches Tanzania Batch double-vault composting toilets Chrysomya in feces Phorid flies, cockroaches Taiwan Latrine vaults ChrYsomya Phorid flies Telmuaoscoppus, Hermetia, Eristalis Note: ChrYsomva blow fly; Eristalis = rat tailed maggot; Herm?letia = soldier fly; Musca = housefly; Telinatoscopus = moth fly. Source: B. R. Laurence. unpublished data. numbers of flies will breed in the various environments and others 1978; Burgess and Chetwyn 1978; Cox, associated with waste disposal systems. Some of these Lewis and Glynn 1912; Steinhaus and Brinley 1957), may have a close association with man (the so-called the excreted protozoal cysts (see, for instance, Frye and synanthropic species) and can cause a nuisance. More Meleney 1936, Gupta and others 1972; Pipkin 1949; seriously, they can cause allergy, with sensitization Rendtorff and Holt 1954; Root 1921), and the excreted reactions (skin rash and asthma) as a response to the helminth eggs and larvae (see, for instance, Gupta and presence of the bodies of the flies (see, for instance, others 1972; Oyerinde 1976; Round 1961). The Ordman 1946; Phanichyakarn, Dockhorn and literature on insectborne pathogens is very extensive Kirkpatrick 1969). Second, and of greater importance, and has been reviewed by Greenberg (1971, 1973) is the potential role of flies and cockroaches, which for flies and by Cornwell (1968, 1976) and Roth and either breed in excreta or eat excreta, in disseminating Willis (1960) for cockroaches. fecal pathogens. It is on this aspect that we concentrate The medical significance of the carriage of excreted here. pathogens by insects depends in part upon the Any insect that breeds in excreta or visits excreta to behavior of the insect and in part upon the other modes feed may carry particles of feces from place to place. of transmission of these pathogens. Insects that enter This may be done either on the legs or other parts of the human dwellings and visit human food are especially external body surface or by the insect vomiting or likely to promote disease transmission, and it is for this depositing pathogenic organisms, previously ingested, reason that the flies Musca and Chrysomya and in the feces. Either of these mechanisms can assist the cockroaches are so often implicated. Given that these dissemination of human fecal pathogens in the insects are moving fecal pathogens into houses and environment. onto food, however, it remains unclear what their contribution is to the spread of particular infections. A feces-fingers-food cycle is more direct and more Transmission of Excreted Pathogens probable than a feces-insect-food cycle. The main epidemiological evidence of the import- Many studies have shown that insects that breed in ance of flies and cockroaches in the transmission of excreta, or feed on it, may carry human pathogens on enteric infections comes from the results of surveys of their bodies or in their gut. The massive literature on infection in the human population before and during this subject shows that practically every excreted insecticidal control programs. Decrease of human pathogen has been isolated at some time in a viable enteric infection (especially Shigella infections) has state from a fly or cockroach. This includes the sometimes been recorded in the sprayed areas (see, for excreted viruses (see, for instance, Melnick and Dow instance, Abdel-Gawaad and El-Gayar 1972; Mackie 1953), the excreted bacteria (see, for instance, Bidawid and others 1956; Watt and Lindsay 1948; Wolff, van 498 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA Zijl and Roy 1969). In some experiments a rise in residentsoftropicalcountries,andwouldprobablyalso human infection accompanied the development of attract cockroaches. Hence, there is no easy, universal insecticide resistance in the flies (see, for instance, solution. Lindsay, Stewart and Watt 1953). The feces of different animals attract different associations of insect species, and this reflects the differing consistencies of the feces. Sanitary measures Methods of Fly and Cockroach Control designed to prevent housefly breeding, such as bored hole latrines, may not be successful against the Whatever their exact role in disease transmission, it blowfly. Wherever possible, improvement in sanitation is always desirable to control any fly or other insect design should aim to protect the feces from the visiting nuisance associated with excreta disposal. Control of insects and provide conditions of disposal unsuitable human excreta alone. however, will not be sufficient for the development of the larval stages in the fecal because the insects will with some certainty be breeding material. elsewhere (in the excreta of other animals and in Housefly eggs are killed at 42°C, larvae at 47°C, and other materials), and the flies will disperse quickly into pupae at 45°C (Keiding 1976). Hence, composting the controlled areas. For instance, surveys in three should aim at maintaining the lethal temperature cities in the USA (Charleston, Phoenix, and Topeka) throughout the consolidated mass of excreta. Low showed that the primary site for housefly and blowfly temperatures at the edges will still permit larval breeding was garbage (Schoof, Mail and Savage 1954). development to adult fly. A survey of garbage disposal pits in an army camp in A variety of design suggestions for controlling fly the USA also showed them to be a major breeding site breeding in latrines, animal manure, and garbage are (Mathis, Schoof and Mullenix 1969). In Dar es Salaam given by Busvine (1982). Fly control in garbage disposal (Tanzania), the majority of flies emerging from pit plants using composting and sanitary landfill is latrines were Clhrysomya putoria, whereas 9 percent of described by Alvarez. Blanton and Putnam (1972) and flies caught in kitchens were Musca domestica, thus Black and Barnes (1956), respectively. Data on fly clearly indicating that major breeding activity was controlincompostingplantsforexcretaplusgarbagein taking place in other sites (Bang, Sabuni and Tonn China are given by Scott (1952). 1975). The most important advances in thinking on The control of fly and cockroach breeding in the control of fly breeding in pit latrines concern the association with human excreta may not, therefore, role of pit ventilation and the use of exit traps. Modern have any measurable effect on the total fly and concepts of pit latrine design include a pit vent pipe or cockroach population. However, such control will chimney, one major role of which is to exhaust foul reduce the population of flies and cockroaches that gases and thus make the latrine odor-free and pleasant have been in contact with human excreta, and- (see, for instance, Feachem and Cairncross 1978). because many excreted pathogens are found ex- Experiments conducted in Botswana, Tanzania, and clusively, or almost exclusively, in human excreta (for Zimbabwe have shown that vent pipes also play an instance, poliovirus, hepatitis A virus, Shigella, Vibrio important role in reducing fly production by pit cholerae, Entamoeba histolytica, and the eggs of human latrines. In Zimbabwe (Morgan 1977), four pit latrines roundworms and hookworms)-this reduction could were built in a row, two with vent pipes and two be epidemiologically important (McCabe and Haines without, and were used for 6 months prior to the start 1957). of the experiment. During 2.5 months, 13,953 flies were trapped from the unvented pits, but only 146 were trapped from the vented pits. Most flies were -odifying the physical environment Chrysomya. The studies in Botswana and Tanzania An ideal sanitary unit should exclude flies and (Curtis and Hawkins 1982) found that, in vented pit other insects and prevent access to the feces but latrines with their doors kept closed, about 90 should not inhibit people from using it. The percent of the emerging flies (mainly Chrysomya success of fly-proofing methods (self-closing lids, putoria) went up the vent pipe and were caught by the screening, darkness, proper coverage of the fecal gauze at the top. When the doors were left open, only material) depends upon the acceptance and mainten- about 50 percent of flies attempted to exit via the vent ance of these methods by the local population. pipe; the rest left through the drop hole. This suggests An enclosed, dark and fly-proof box that overheats that keeping the latrine dark by closing the door would clearly not be acceptable as a toilet to the encourages the newly emerged flies to go toward the FLIES, COCKROACHES, AND EXCRETA 499 main light source, which comes down the vent pipe. roaches. Fumigation of sewers, the use of residual The studies in Botswana and Tanzania also showed insecticides as sprays or lacquer paints, and poison that female flies attempting to enter latrines to lay eggs baits have been found to be effective, but the control of were strongly attracted by the fecal odors from the cockroach infestation in excreta disposal units is part vent pipes and therefore tried to enter the pits by flying of a wider problem of cockroach control in the human down the vent pipes. They were prevented from doing community. A combination of water, food, and this by the gauze at the top end of the vent pipe. Thus, darkness is ideal for renewed cockroach infestation in screened vent pipes reduce the numbers of gravid the tropics. A comprehensive review of cockroach female flies gaining access to the pits and prevent a control strategies is given by Cornwell (1968, 1976), considerable proportion of young flies from leaving the and a recent survey of approaches to cockroach pits. [See note on page 81.] control in Hungary is presented by Bajomi and Elek The second important new approach to fly control in (1979). pit latrines is the use of an exit trap on the squatting hole instead of a lid. This is described in chapter 36 and by Curtis (1980) and Curtis and Hawkins (1982) and Literature Cited requires large-scale field testing. Abdel-Gawaad, A. A. W. and El-Gayar, F. H. (1972). House Insecticides and other chemicals fly control in Alexandria City and its effects on the prevalence of certain summer diseases. Zeitschrift fur The ideal cheap and nonbulky compound that angwandte Entomologie, 71, 44-52. reduces the attractiveness of feces to flies has yet to be Alvarez, C. G., Blanton, F. S. and Putnam, H. D. (1972). found. Addition to feces of diesel oil, chloride of lime, Identification and control of flies associated with a borax, paradichlorbenzene, and thiourea, as well as compost plant. Environmental Entomology, 1, 710-716. other larvicides-some toxic to man-has been Bajomi, D. and Elek, S. (1979). The importance of used. Such chemicals should be used with caution cockroaches and methods for their control. International whenevea. the xcretawll soulbsequsently undergo some Pest Control, 21, 31-38 and 47. whenever the excreta will subsequently undergo some Bang, Y. H., Sabuni, I. B. and Tonn, R. J. (1975). Integrated biological treatment process, such as digestion or control of urban mosquitoes in Dar es Salaam using composting, that could be adversely affected by the community sanitation supplemented by larviciding. East added chemicals. Caution is also required if the excreta African Medical Journal, 52, 578-588. may be reused in agriculture or aquaculture. Bidawid, S. P., Edeson, J. F. B., Ibrahim, J. and Matossian. R. Fly control programs with the use of chlorinated M. (1978). The role of non-biting flies in the transmission hydrocarbon insecticides, such as DDT and BHC, of enteric pathogens (Salmonella species and Shigella have produced widespread resistance in the housefly, species) in Beirut, Lebanon. Annals of Tropical Medicine and resistance to other insecticides has also developed, and Parasitology, 72, 117-121. Resistance to insecticides has also been recorded in Black, R. J. and Barnes, A. M. (1956). Effect of earth cover on Chrysomya. In some control programs resistance of housefly emergence. Public Works, 87, 109-111. flies to insecticides has developed extremely rapidly- Burgess, N. R. H. and Chetwyn, K. N. (1978). Cockroaches as for instance, in about 3 months (Lindsay, Stewart and a hazard to health. In Proceedings of the Medical Entomology Centenary Symposium. London, 23 to 25 Watt 1953). In Georgia (USA) the use of dieldrin, November, 1977, p. 137. London: Royal Society of BHC, or chlordane in pit latrines greatly increased the Tropical Medicine and Hygiene. breeding of insecticide-resistant Musca domestica Busvine, J. R. (1982). Control of Domestic Flies. Bulletin No. 5. because it reduced the population of Hermetia illucens London: The Ross Institute of Tropical Hygiene. larvae, which were making the pit contents too liquid Cornwell, P. B. (1968). The Cockroach: A Laboratory Insect for housefly breeding (Kilpatrick and Schoof 1959). and an Industrial Pest. London: The Rentokil Library and Flypapers, insecticide-impregnated cords and plas- Associated Business Programmes. tic blocks, baited fly traps, and poison baits have all (1976). The Cockroach: Insecticides and Cockroach been used against theaultly.istrbControl. London: The Rentokil Library and Associated been used against the adult ly. Distribution of this type Business Programmes. of equipment is a possibility given the organization, Cox, G. L., Lewis, F. C. and Glynn, E. E. (1912). The number understanding, and cooperation of the local popu- and varieties of bacteria carried by the common housefly in lation. sanitary and insanitary city areas. Journal of Hygiene, 12, The control of insects other than houseflies and 290-312. blowflies presents similar problems. As with the flies, Curtis, C. F. (1980). Insect traps for pit latrines. Mosquito widespread insecticide resistance is known in cock- News, 40, 626-628. 500 ENVIRONMENTAL BIOLOGY & EPIDEMIOLOGY: INSECTS AND EXCRETA Curtis, C. F. and Hawkins, P. M. (1982). Entomological Melnick, J. L. and Dow, R. P. (1953). Poliomyelitis in studies of on-site sanitation systems in Tanzania and Hildalgo County, Texas, 1948. Poliomyelitis and cox- Botswana. Transactions of the Royal Society of Tropical sackie viruses from flies. American Joturnial of HYgiene. 58, Medicinie anld Hygicne. 76. 99-108. 288-309. Feachem, R. and Cairncross, S. (1978). Small Exereta Morgan, P. (1977). The pit latrine-revived. Central African Disposal Systems. London: The Ross Institute of Tropical Journal of Medicine, 23, 1-4. Hygiene. Ordman, D. (1946). Sewage filter flies (Psechoda) as a cause Frye, W. W. and Meleney, H. E. (1936). The viability of of-bronchial asthma. South African Medical Journal, 20, Endamoeba histolytica cysts after passage through the 32-35. cockroach. Journtal of Parasitology, 22, 221-222. Oyerinde, J. P. 0. (1976). The role of the house fly (Musca Greenberg, B. (1971). Flies and Disease: Ecology, domestica) in the dissemination of hookworm. Annals of Cl,;.2, * ... ,r;. .'' and Biotic Associations. New Jersey: Tropical Medicine and Parasitology, 70, 455-462. Princeton University Press. Phanichyakarn, P., Dockhorn, R. J. and Kirkpatrick, C. H. (1973). Flies and Disease: Biology and Disease (1969). Asthma due to inhalation of moth flies. Journal of Transmission. New Jersey: Princeton University Press. Allergy, 44, 51-58. Gupta, S. R., Rao, C. K., Biswas, H., Krishnaswami, A. K.. Pipkin, A. C. (1949). Experimental studies on the role of filth Wattal, B. L. and Raghavan, N. G. S. (1972). Role of the flies in the transmission of Endamoeba histolytica. housefly in the transmission of intestinal parasitic American Journal of Hygiene, 49, 255-275. cysts/ova. Indian Journal of Medical Research, 60, Raybould, J. N. (1966). The control of Chrjysomyia putoria 1120-1125. and Culexfatigans at Amani. In Annual Reportfor 1965 of Keiding, J. (1976). The housefly. Biology and control. the East African Institute of Malaria and Vector-Borne Unpublished document, WHO/VBC/76.650. Geneva: Diseases, Amani, Tanzania, p. 48. Nairobi: East African World Health Organization. Common Services Organization. Kilpatrick, J. W. and Schoof, H. F. (1959). Interrelationship Rendtorff, R. C. and Holt, C. J. (1954). The experimental of water and Hermetia illucens breeding to Musca transmission of human intestinal protozoan parasites. III. domestica production in human excrement. American Attempts to transmit Endamoeba coli and Giardia lamblia Journal of Tropical Medicine and Hygiene, 8, 597-602. cysts by flies. American Journal of Hygiene, 60, 320-326. Laurence, B. R. (1977). Insect breeding in relation to Root. F. M. (1921). Experiments on the carriage of intestinal sanitation and waste disposal. In Water, Wastes and Health protozoa of man by flies. American Journal of Hygiene, 1, in Hot Climates, eds. Feachem, R., McGarry, M. and Mara, 131-153. D., pp. 284-298. London: John Wiley. Roth, L. M. and Willis, E. R. (1960). The biotic associations of Lien, J. C. and Chen, C. Y. (1974). Species of flies breeding in cockroaches. Smithsonian Miscellaneous Collections, 141, latrines in the Taipei area. Chinese Journal of 1-470. Microhiology, 7, 165-170. Round, M. C. (1961). Observations on the possible role of Lindsay, D. R.. Stewart. W. H. and Watt, J. (1953). Effect of filth flies in the epizootiology of bovine cysticercosis in fly control on diarrhoeal disease in an area of moderate Kenya. Journal of Hygiene, 59, 505-513. morbidity. Public Health Reports, 68, 361-367. Schoof, H. F., Mail, G. A. and Savage, E. P. (1954). Fly Lloyd, L. (1945). Animal life in sewage purification processes. production sources in urban communities. Journal of Journal of the Institute of Sewage Purification, (part 1), Economic Entomology, 47, 245-253. 119-139. Scott, J. C. (1952). Health and Agriculture in China: A McCabe, L. J. and Haines, T. W. (1957). Diarrhoeal disease Fundamental Approach to Some of the Problems of World control by improving human excreta disposal. Public Hunger. London: Faber and Faber. Health Reports, 72, 921-928. Steinhaus, E. A. and Brinley, F. J. (1957). Some relationships Mackie, T. T., Mackie, J. W., Vaughn, C. M., Gleason, N. N., between bacteria and certain sewage-inhabiting insects. Greenberg, B. G., Nenninger, E. S., Lunde, M. N., Moore, Mosquito News, 17, 299-302. L. L.A., Kluttz,J. A. and Taliafero, M. 0. (1956). Intestinal Usinger, R. L. and Kellen, W. R. (1955). The role of insects in parasitic infections in Forsyth County, North Carolina. sewage disposal beds. Hilgardia, 23, 263-321. IV. Domestic environmental sanitation and the prevalence Watt, J. and Lindsay, D. R. (1948). Diarrhoeal disease of Entamoeba histolytica. American Journal of Tropical control studies. 1. Effect of fly control in a high morbidity Medicine and Hygiene, 5, 29-39. area. Public Health Reports, 63, 1319-1334. Mathis, W., Schoof, H. F. and Mullenix, T. L. (1969). Fly Wolff, H. L., van Zijl, W. J. and Roy, M. (1969). Houseflies, production in relation to refuse disposal in recreational the availability of water, and diarrhoeal diseases. Bulletin areas. Journal of Economic Entomology, 62, 1288-1291. of the World Health Organization, 41, 952-959. 501 World Bank Publications The full range of World Bank Publications, both free and for sale, is described in the Catalog of World Bank Publications; the Bank's continuing research program is outlined in World Bank Research Program: Abstracts of Current Studies. Both booklets are updated annually; the most recent edition of each is available without charge from the Publications Unit, World Bank, 1818 H Street NW, Washington, DC 20433, USA. The Authors Richard G. Feachem is senior lecturer in tropical health engineering at the Ross Institute of Tropical Hygiene, of the London School of Hygiene and Tropical Medicine, University of London, England. David J. Bradley is professor of tropical hygiene at, and director of, the Ross Institute. Hemda Garelick is a research fellow at the Ross Institute. D. Duncan Mara is professor of civil engineering at the University of Leeds, England. A World Bank Publication The United Nations has designated the 1980s as the International Drinking Water Supply and Sanitation Decade. Its goal is to provide two of the most fun- damental human needs-safe water and sanitary disposal of human wastes-to all people. To help usher in this important period of international research and cooperation, the World Bank has arranged the publication of three volumes on appropriate technologies for water supply and sanitation and the public health aspects of these technologies. Since 1976, Bank staff and resear- chers from various countries have been analyzing the economic, environmen- tal, health, and sociological effects of various technologies to identify the most appropriate systems for the needs and resources of different areas. The re- search has included field investigations in nineteen countries. Since the technology and health aspects of water supply are better understood, the emphasis in these volumes is on sanitation and waste reclamation, their contribution to better health, and how they are affected by water service levels and the ability and willingness of communities to pay for the systems. This book, the third volume of the series, addresses the public health, microbiological and parasitological aspects of sanitation. In all countries, public health is of central importance in the design and im- plementation of excreta disposal projects, and better health is the main social and economic benefit that planners and economists hope to realize by investing in excreta disposal systems. To achieve this gain, as much information as possi- ble is needed about the interaction of excreta and health-information con- cerning not only broad epidemiological issues of disease prevention through improved excreta disposal, but also the effect of particular excreta disposal and reuse technologies on the survival and dissemination of particular pathogens. JOHN WILEY & SONS Chichester - New York - Brisbane - Toronto - Singapore ISBN 0 471 90094 X