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Home , Opisthorchis viverrini, Schistosoma mansoni

eONTENTS

NOTE TO THE READER ...... 9

LIST OF PARTICIPANTS ...... Il

PREAMBLE ...... 17 Background ...... 17 Objective and Scope ...... 17 Selection of Topics for Monographs ...... 18 Data for Monographs ...... 19 The Working Group ...... 19 Working Procedures ...... 19 Exposure Data...... " 20 Studies of in Humans ...... 21 Studies of Cancer in Experimental Animais ...... 25 Other Data Relevant to an Evaluation of Carcinogenicity and Its Mechanisms . . 27 Summary of Data Reported ...... 29 Evaluation ...... 30 References ...... 34

GENERA REMARKS ...... 39 THE MONOGRAHS with schistosomes ( haematobium, S. mansoni and S. japonicum). 45 1. Exposure data ...... 45 1. 1 Structure and biology of schistosomes ...... 45 1.1.1 ...... 45 1.1.2 Structure...... 45 1. 1.3 Life cycle and biology of the adult worm ...... 46 1.2 Methods for detection of infection ...... 48 1.2.1 History taking ...... 48 1.2.2 Clinical diagnosis ...... 48 1.2.3 Parasitological tests ...... 49 1.2.4 Immunological tests ...... 49 1.2.5 Establishment of absence of infection ...... 50 CONTENTS

1.3 Epidemiology of infection ...... " 50 1.3.1 Geographical distribution ...... 50 1.3.2 Risk factors for infection ...... " 55 1.3.3 Aggregation of infection ...... 55 1.3.4 Prevalence and intensity of infection ...... 55 1.3.5 Sex-related patterns of infection ...... 58 1.3.6 Relationship of morbidity to intensity of infection ...... 58 1.3.7 Relationship of morbidity to mortality from infection...... " 58 1.4 Clinical disease in humans (other than cancer) ...... 59 1.5 Treatment and control ...... " 61 1.5.1 Treatment...... 61 1.5.2 Control ...... 62 2. Studies of cancer in humans ...... 63 2.1 Descriptive studies ...... 63 2.1.1 ...... 63 2.1.2 ...... 66 2.1.3 . . ; ...... 67 2.2 Case reports and case series ...... 70 2.2.1 Schistosoma haematobium ...... 71 2.2.2 Schistosoma mansoni ...... 72 2.2.3 Schistosoma japonicum ...... 73 2.3 Cohort study ...... 73 2.4 Case-control studies (with retrospective exposure assessment) ...... 74 2.4.1 Schistosoma haematobium ...... 74 2.4.2 Schistosoma japonicum ...... 77 3. Studies of cancer in animais...... 81 3.1 Infection wi th Schistosoma haematobium alone ...... 81 3.1.1 Mouse...... 81 3.1.2 Rat...... 81 3.1.3 Hamster...... 82 3.1.4 Opossum...... 82 3.1.5 Nonhuman primate ...... 82 3.2 Infection with Schistosoma haematobium in combination with administration of known ...... 83 3.2.1 2-Acetylaminofluorene...... 83 3.2.2 ortho-Aminoazotoluene...... 84 3.2.3 N-Nitrosamines...... 84 3.3 Infection with Schistosoma mansoni alone ...... 84 3.3.1 Mouse...... 84 3.3.2 Mastomys natalensis ...... 85 3.3.3 Hamster...... 85 3.3.4 Nonhuman primate ...... 85 CONTENTS

3.4 Infection with Schistosoma mansoni in combination with administration of known carcinogens ...... 86 3.4.1 2-Amino-5-azotoluene...... 86 3.4.2 2-Naphthylamine and 2-acetylaminofluorene ...... 86 3.5 Infection with Schistosoma mansoni in combination with administration of compounds used or evaluated in the past as antischistosomal agents " 87

3.6 Infection with Schistosoma japonicum al one ...... 87 3.7 Infection with Schistosoma japonicum in combination with administration of known carcinogens ...... 87 3.7.1 Dimethylaminobenzene...... 87 3.7.2 2-Acetylaminofluorene...... 88 4. Other data relevant for evaluation of carcinogenicity and Its mechanisms . . .. 88 4.1 Pathology of infection ...... 88 4.1.1 Humans...... 88 4.1.2 Experimental systems ...... " 92 4.2 Other observations relevant to the interpretation of carcinogenicity and mechanisms of ...... 93 4.2.1 Humans...... 93 4.2.2 Experimental systems...... 95 5. Summary of data reported and evaluation ...... 96 5.1 Exposure data...... 96 5.2 Human carcinogenicity data ...... 97 5.3 carcinogenicity data ...... 99 5.4 Other relevant data ...... 99 5.5 Evaluation...... 99 6. References ...... 100

Infection with liver flukes ( viverrini, O. jelineus and ). 121 1. Exposure data ...... 121 1. 1 Structure and biology of liver flukes ...... 121 1.1.1 Taxonomy ...... 121 1.1.2 Structure...... 121 1.1.3 Life cycle and biology of the adult worm ...... 122 1.1.4 Immune response to infection...... 124 1.2 Methods for detection of infection ...... 124 1.2.1 Qualitative faecal examination for eggs ...... 124 1.2.2 Quantitative faecal assessment of intensity of infection ...... 125 1.2.3 Serological tests for helminth-specific antibody and antigen .... 125 1.2.4 Intradermal tests...... 126 1.3 Epidemiology of infection ...... 126 1.3.1 Geographical distribution ...... 126 1.3.2 Risk factors for infection ...... 130 CONTNTS

1.3.3 Age- and sex-related patterns of infection ...... " 132 1.3.4 Aggregation of infection ...... 132 1.4 Clinical disease in humans (other than cancer) ...... 134 1.5 Treatment and control ...... " 135 2. Studies of cancer in humans ...... " 136 2.1 Descriptive studies ...... " 136 2.1.1 ...... 136 2.1.2 Opisthorchis feIineus ...... 137 2.2 Case reports and case series ...... 13 7 2.2.1 Opisthorchis viverrini ...... 137 2.2.2 ...... " 137 2.2.3 Clonorchis sinensis ...... 141 2.3 Case-control studies ...... 141 2.3.1 Opisthorchis viverrini ...... 141 2.3.2 Clonorchis sinensis ...... " 143 3. Studies of cancer in animais...... " 144 3.1 Infection with Opisthorchis viverrini alone ...... " 144 3.2 Infection with Opisthorchis viverrini in combination with administration of known carcinogens ...... 146 3.2.1 N-Nitrosodimethylamine...... 146 3.2.2 N-Nitrosodiethylamine...... 148 3.2.3 N-Nitrosodihydroxydi-n-propylamine...... 148 3.3 Infection with Opisthorchis viverrini in combination with administration of other modifyng factors ...... 149 3.4 Infection with Opisthorchis feIineus ...... 150 3.5 Infection with Clonorchis sinensis alone ...... 150 3.5.1 Rat...... 150 3.5.2 Cat...... 150 3.5.3 Dog...... 150 3.6 Infection with Clonorchis sinensis in combination with administration of known carcinogens ...... 150 3.6.1 AfatoxIn Bi ...... 150 3.6.2 N-Nitrosodimethylamine...... 151 3.6.3 2-Acetylaminofluorene...... 152 4. Other data relevant for evaluation of carcinogenicity and its mechanisms . " 152 4.1 Pathology of infection ...... 152 4.1.1 Humans...... 152 4.1.2 Experimental systems...... 155

4.1.3 Comparison of hum ans and experimental animais ...... 157 4.2 Other observations relevant to the interpretation of carcinogenicity and mechanisms of carcinogenesis ...... 157 4.2.1 Humans...... 157 CONTENTS

4.2.2 Experimental systems...... 158 5. Summary of data reported and evaluation ...... 159 5.1 Exposure data...... 159 5.2 Human carcinogenicity data ...... 160 5.3 Animal carcinogenicity data ...... 161 5.4 Other relevant data ...... 161 5.5 Evaluation...... 161 6. References ...... " 162

Infection with pylori ...... 177 1. Exposure data ...... 177 1.1 Structure and biology of HeIicobacter pylori...... 177 1.1.1 Taxonomy...... 177 1.1.2 Biology ...... 177 1. 1.3 Agent- relationship ...... 179 1.2 Methods for detection of infection ...... 181 1.2.1 Methods based on gastric biopsy specimens...... 181 1.2.2 Methods based on gastric juice samples ...... 182 1.2.3 Methods based on faecal specimens ...... 182 1.2.4 Methods based on dental plaque and saliva samples ...... 182 1.2.5 Methods based on blood samples ...... 183 1.2.6 Urea breath test...... 183 1.3 Epidemiology of infection ...... 183 1.3.1 Prevalence...... 183 1.3.2 Risk factors for infection ...... 184 1.3.3 Routes of ...... 186 1.4 Clinical disease in humans (other than cancer) ...... 187 1.4.1 Gastritis...... 187 1.4.2 Duodenal ulcer disease ...... 187 1.4.3 Gastric ulcer disease ...... 187 1.4.4 Hypertrophic protein-Iosing gastritis ...... 188 1.4.5 Childhood diseases ...... 188 1.5 Treatment and control ...... 188 1.5.1 Antibiotics and acid suppressive therapy ...... 188 1.5.2 Vaccination...... 188 2. Studies of cancer in humans ...... 188 2.1 Descriptive studies ...... 188 2.1.1 Geographical correlations ...... 188 2.1.2 Time trends...... 191 2.1.3 Socioeconomic trends ...... 191 2.2 Case series ...... 191 2.2.1 Gastric carcinoma ...... 191 CONTNTS

2.2.2 Gastric lymphoma ...... 192 2.3 Cohort studies ...... 192 2.3.1 GastrIc carcinoma ...... 192 2.3.2 Gastric Iymphoma ...... 197 2.4 Case-control studies ...... 197 2.4.1 Gastric carcinoma ...... 197 2.4.2 Other ...... 203 2.5 Intervention studies ...... 203 3. Studies of cancer in experimental animais...... 203 3.1 Infection with alone ...... 203 3.2 Infection with Helicobacter pylori in combination with administration of known carcinogens ...... 203 3.3 Infection with other Helicobacter species' ...... 205 3.4 Infection with other Helicobacter species in combination with administration of known carcinogens ...... 205 4. Other data relevant for evaluation of carcinogenicity and its mechanisms . .. 206 4.1 Pathology of infection ...... 206 4.1.1 Humans...... 206 4.1.2 Experimental systems ...... " 211 4.2 Other observations relevant to the interpretation of carcinogenicity and mechanisms of carcinogenesis ...... 213 4.2.1 Humans...... 213 4.2.2 Experimental systems...... 217 5. Summary of data reported and evaluation ...... 218 5.1 Exposure data...... 218 5.2 Human carcinogenicity data ...... 218 5.3 Animal carcinogenicity data ...... 219 5.4 Other relevant data ...... 219 5.5 Evaluation...... 220 6. References ...... 220 SUMMARY OF FINAL EVALUATIONS...... 241 CUMULATIVE INDEX TO THE MONOGRAPHS SERIES...... 243 NOTE TO THE READER

The term 'carcinogenic risk' in the lARC Monographs series is ta ken to me an the proba- bility that exposure to an agent willlead to cancer in humans. Inclusion of an agent in the Monographs does not imply that it is a , only that the published data have been examined. Equally, the fact that an agent has not yet been evaluated in a monograph does not mean that it is not carcinogenic. The evaluations of carcinogenic risk are made by international working groups of in- dependent scientists and are qualitative in nature. No recommendation is given for regu- lation or legislation. Anyone who is aware of published data that may alter the evaluation of the carcinogenic risk of an agent to humans is encouraged to make this information available to the Unit of Carcinogen Identification and Evaluation, International Agency for Research on Cancer, 150 cours Albert Thomas, 69372 Lyon Cedex 08, France, in order that the agent may be considered for re-evaluation by a future Working Group. A1though every effort is made to prepare the monographs as accurately as possible, mistakes may occur. Readers are requested to communicate any errors to the Uni t of Carcinogen Identification and Evaluation, so that corrections can be reported in future volumes.

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