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Level ofOpisthorchis infestation and carcinogen dose-dependence of cholangiocarcinoma induction in Syrian golden hamsters

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Virchows Archiv B

Summary

The relationship between different levels of liver fluke,Opisthorchis viverrini infestation and dimethylnitrosamine (DMN) dosage in the induction of cholangiocarcinomas was investigated in Syrian golden hamsters. Two hundred and eighty male, weanling animals were divided into 4 groups: Group 1 served as untreated controls; group 2 receivedO. viverrini metacercariae only at levels of 100, 50, 25 or 12 per animal; group 3 received DMN only at doses of 12.5, 6.25 or 3.125 ppm; group 4 received various combinations of metacercariae and DMN. Only 2 of 17 animals (12%) in group 3 receiving 12.5 ppm had detectable tumours and no neoplastic lesions were seen in the 6.25 and 3.125 ppm DMN subgroups or in parasite alone or untreated control hamsters. In contrast, high carcinogen and parasite dose-dependent yields of cholangiocarcinomas (incidences up to 93%) and putative preneoplastic cholangiofibrotic lesions were observed in group 4. Thus the results indicate clear dose-dependent synergistic effects for the two agents and reveal the crucial importance of the presence of parasite, even at levels as low as 12 metacercariae, for DMN induction of bile duct carcinogenesis.

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References

  • Bannasch P (1978) Cellular and subcellular pathology of liver carcinogenesis. In: Remmer H, Bolt HM, Bannasch P, Popper H (eds) Primary liver tumors. University Park Press, Baltimore, p 87

    Google Scholar 

  • Bannasch P, Massner B (1976) Histogenese und Cytogenese von Cholangiofibromen und Cholangiocarcinomen bei Ni-trosomorpholinvergifteten Ratten. Z Krebsforsch 87: 239–255

    Article  CAS  Google Scholar 

  • Bannasch P, Massner B (1977) Die Feinstruktur des Nitrosomorpholin-induzierten Cholangiofibroms der Ratte. Virchows Arch [Cell Pathol] 24:295–315

    CAS  Google Scholar 

  • Bannasch P, Reiss W (1971) Histogenese und Cytogenese cholangiocellularer Tumoren bei Nitrosomorpholin-vergifteten Ratten. Zugleich ein Beitrag zur Morphogenese der Cystenleber. Z Krebsforsch 76:193–215

    Article  CAS  Google Scholar 

  • Belamaric J (1973) Intrahepatic bile duct carcinoma and C. sinensis infection in Hong Kong. Cancer 31:468–473

    Article  PubMed  CAS  Google Scholar 

  • Bergman F, Wahlin T (1981) Tumour induction in Syrian hamsters fed a combination of aminopyrine and nitrite. Acta Pathol Microbiol Scand Sec. A 89:241–245

    CAS  Google Scholar 

  • Bhamarapravati N, Viranuvatti V (1966) Liver diseases in Thailand. An analysis of liver biopsies. Am J Gastroenterol 45:267–275

    PubMed  CAS  Google Scholar 

  • Bhamarapravati N, Thamavit W, Vajrasthira S (1978) Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. Am J Trop Med Hyg 27:787–794

    PubMed  CAS  Google Scholar 

  • Boonpucknavig S, Kurathong S, Thamavit W (1986) Detection of antibodies in sera from patients with Opisthorchiasis. J Clin Lab Immunol 19:135–137

    PubMed  CAS  Google Scholar 

  • Chan PH, Teoh TB (1969) The pathology of Clonorchis sinensis infestation of the pancreas. J Pathol Bacteriol 93:185–189

    Article  Google Scholar 

  • Chou ST, Gibson JB (1972) A comparative histochemical study of rat livers in alpha-napthyl-iso-thiocyanate (ANIT) and DL-ethionine intoxication. J Pathol 108:73–83

    Article  PubMed  CAS  Google Scholar 

  • Columbano A, Rajalakshmi S, Sarma DS (1981) Requirement of cell proliferation for the initiation of liver carcinogenesis as assayed by three different procedures. Cancer Res 41:2096–2102

    Google Scholar 

  • Craddock VM (1971) Liver carcinomas induced in rats by single administration of dimethylnitrosamine after partial hepatectomy. J Natl Cancer Inst 47:899–907

    PubMed  CAS  Google Scholar 

  • Cruickshank AH, Sparshott SM (1971) Malignancy in natural and experimental cysts: experiments with aflatoxin in rats and the malignant transformation of cysts in human livers. J Pathol 104:185–190

    Article  PubMed  CAS  Google Scholar 

  • Falchuk KR, Lesser PB, Galdabini JJ, Isselbacher KJ (1976) Cholangiocarcinoma as related to chronic intrahepatic cholangitis and hepatolithiasis. Am J Gastroenterol 66:57–61

    PubMed  CAS  Google Scholar 

  • Flavell DJ, Lucas SB (1982) Potentiation by the human liver fluke Opisthorchis viverrini of the carcinogenic action of N-nitrosodimethylamine upon the biliary epithelium of the hamster. Br J Cancer 46:985–989

    PubMed  CAS  Google Scholar 

  • Flavell DJ, Lucas SB (1983) Promotion of N-nitrosodimethylamine-initiated bile duct carcinogenesis in the hamster by the human liver fluke, Opisthorchis viverrini. Carcinogenesis 4:927–930

    Article  PubMed  CAS  Google Scholar 

  • Floot BGJ, Philippus EJ, Hart AAM, Den Engelse L (1979) Persistence and accumulation of (potential) single-strand breaks in liver DNA of rats treated with diethylnitrosamine or dimethylnitrosamine: correlation with hepatocarcinogenicity. Chem-Biol Interact 25:229–242

    Article  PubMed  CAS  Google Scholar 

  • Giambarresi KG, Katyal SL, Lombardi B (1982) Promotion of liver cancer in the rat by a choline devoid diet: role of liver necrosis and regeneration. Br J Cancer 46:825–829

    PubMed  CAS  Google Scholar 

  • Herrold KM (1967) Histogenesis of malignant liver tumors induced by dimethylnitrosamine. An experimental study in Syrian hamsters. J Natl Cancer Inst 39:1099–1111

    PubMed  CAS  Google Scholar 

  • Hou PC (1956) The relationship between primary liver cancer and infestation with Clonorchis sinensis. J Pathol Bact 72:239–246

    Article  CAS  Google Scholar 

  • Hou PC (1984) Primary carcinoma of bile duct of the liver of the cat (Felis catus) infested with Clonorchis sinensis. J Pathol Bact 87:239–244

    Google Scholar 

  • Hou PC (1965) Hepatic clonorchiasis and carcinoma of the bile duct in a dog. J Pathol Bact 89:356–367

    Google Scholar 

  • Hsu SM, Raine L, Farger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody PAP procedures. J Histochem Cytochem 29:577–580

    PubMed  CAS  Google Scholar 

  • Kim Y II, Yang DH, Chang KR (1974) Clonorchis sinensis infestation and cholangiocarcinoma of the liver in Korea: epidemiological and pathological reappraisal of 495 consecutive primary carcinomas of the liver in Seoul and Pusan areas. Seoul J Med 15:247–253

    Google Scholar 

  • Kozuka S, Kurashina M, Tsubone M, Hachisuka K, Yasui A (1984) Significance of intestinal metaplasia for the evolution of cancer in the biliary tract. Cancer 54:2277–2285

    Article  PubMed  CAS  Google Scholar 

  • Kurathong S, Lerdvirasirikul P, Wougpaitoon V, Pramoolsinsap C, Kanjanapitak A, Varawithaya W, Phupradit P, Bunyaratvej S, Upatham S, Brockelman WY (1985) Opisthorchis viverrini infection and cholangiocarcinoma: a prospective, case-control study. Gastroenterol 89:151–156

    CAS  Google Scholar 

  • McClean AEM, Smith M, Driver HE (1982) Liver tumors after single dose dimethylnitrosamine, low and high protein diet, and phenobarbitone. Carcinogenesis 3:707–709

    Article  Google Scholar 

  • Melia WM, Johnson PJ, Neuberger J, Zaman S, Portmann BC, Williams R (1984) Hepatocellular carcinoma in primary biliary cirrhosis: detection by a-fetoprotein estimation. Gastroenterol 87:660–663

    CAS  Google Scholar 

  • Migasena P, Changbumrung S (1974) The role of nitrosamines in the causation of primary carcinoma. J Med Assoc Thailand 57:175–178

    CAS  Google Scholar 

  • Migasena P, Reaunsuwan W, Changbumrung S (1980) Nitrates and nitrites in local Thai preserved protein foods. J Med Assoc Thailand 63:500–505

    CAS  Google Scholar 

  • Moore MA, Fukushima S, Ichihara A, Sato K, Ito N (1986) Intestinal metaplasia and altered enzyme expression in propylnitrosamine-induced Syrian hamster cholangiocellular and gallbladder lesions. Virch Archiv B Cell Pathol 51:29–38

    Article  CAS  Google Scholar 

  • Moore MR, Pitot HC, Miller EC, Miller JA (1982) Cholangiocellular carcinomas induced in Syrian golden hamsters administered aflatoxin Bl in large doses. J Natl Cancer Inst 68:272–278

    Google Scholar 

  • Mowry RW, Morard JC (1957) The distribution of acid mucopolysaccharides in normal kidneys, as shown by the Alcianblue Feulgen (AB-F) and Alcian-blue-periodic acid-Schiff (AB-PAS) stains. Am J Pathol 3:620–621

    Google Scholar 

  • Pitot HC, Scirica AE (1980) The stages of initiation and promotion in hepatocarcinogenesis. Biochim Biophys Acta 605:191–215

    PubMed  CAS  Google Scholar 

  • Pound AW, McGuire LJ (1978a) Repeated partial hepatectomy as a promoting stimulus for carcinogenic response of liver to nitrosamines in rats. Br J Cancer 37:585–594

    PubMed  CAS  Google Scholar 

  • Pound AW, McGuire LJ (1978b) Influence of repeated liver regeneration on hepatic carcinogenesis by diethylnitrosamine in mice. Br J Cancer 37:595–602

    CAS  Google Scholar 

  • Pour P, Kruger FW, Althoff J, Cardesa A, Mohr U (1974) Effect of beta-oxidised nitrosamines on Syrian hamsters. III. 2,2′-Dihydroxy-di-n-propymitrosamine. J Natl Cancer Inst 54:141–145

    Google Scholar 

  • Rao MS, Pour P (1978) Development of biliary and hepatic neoplasms in Guinea pigs treated with nitrosobis(2-oxopro-pyl)amine. Cancer Lett 5:31–34

    Article  PubMed  CAS  Google Scholar 

  • Reddy KP, Buschmann RJ, Chomet B (1977) Cholangiocarcinomas induced by feeding 3′-methyl-4-dimethylaminoazobenzene to rats: histopathology and ultrastructure. Am J Pathol 87:189–204

    PubMed  CAS  Google Scholar 

  • Reuber MD (1967) Poorly differentiated cholangiocarcinomas occurring “spontaneously” in C3H and C3H×Y hybrid mice. J Natl Cancer Inst 38:901–907

    PubMed  CAS  Google Scholar 

  • Reuber MD (1968) Histogenesis of cholangiofibrosis and welldifferentiated cholangiocarcinoma in Syrian hamsters given 2-acetamidofluorene or 2-diacetamidofluorene. Gann 59: 239–246

    PubMed  CAS  Google Scholar 

  • Satoh K, Kitahara A, Soma Y, Hatayama I, Sato K (1985) Purification, induction and distribution of placental glutathione transferase: a new marker enzyme for preneoplastic cells in the rat chemical carcinogenesis. Proc Natl Acad Sci USA 82:3964–3968

    Article  PubMed  CAS  Google Scholar 

  • Sirisinha S, Wongratanacheewin S (1986) Immunization of hamsters against Opisthorchis viverrini infection. Southeast Asian J Trop Med Pub Hlth 17:567–573

    CAS  Google Scholar 

  • Sirisinha S, Tuti S, Tawatsin A, Vichasri S, Upatham ES, Bunnag D (1983) Attempts to induce protective immunity in hamsters against infection by a liver fluke of man (Opisthorchis viverrini). Parasitology 86:127–136

    Article  PubMed  Google Scholar 

  • Sonakul D, Koompirochana C, Chinda K, Stitnimakarn T (1978) Hepatic carcinoma with opisthorchiasis. Southeast Asian J Trop Med Pub Hlth 9:215–219

    CAS  Google Scholar 

  • Srivatanakul P, Viyanant V, Kurathong S, Tiwawech D (1985) Enzyme-linked immunosorbent assay for detection of Opisthorchis viverrini infection. Southeast Asian J Trop Med Pub Hlth 16:234–239

    CAS  Google Scholar 

  • Terao K, Nakano M (1974) Cholangiofibrosis induced by short-term feeding of 3′-methyl-4-dimethylaminoazobenzene to rats: an electron microscope observation. Gann 65:249–260

    PubMed  CAS  Google Scholar 

  • Thamavit W, Bhamarapravati N, Sahaphong S, Vajrasthira S, Angsubhakorn S (1978) Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverriniinfected Syrian golden hamsters. Cancer Res 38:4634–4639

    PubMed  CAS  Google Scholar 

  • Upatham ES, Viyanant V, Kurathong S, Brockelman WY, Menaruchi A, Soawakontha S, Intarakhao S, Vajrasthira S, Warren KS (1982) Morbidity in relation to intensity of infection inOpisthorchis viverrini: study of a community in Khon Kaen, Thailand. Am J Trop Med Hyp 31:1156–1163

    CAS  Google Scholar 

  • Upatham ES, Viyanant V, Kurathong S, Rojborwonwitaya J, Brockelman WY, Ardsurgnoen S, Lee P, Vajrasthira S (1984) Relations between prevalence, intensity of infection, and clinical symptoms and signs inOpisthorchis viverrini infection in a rural community in northeast Thailand. Bull WHO 62:451–461

    PubMed  CAS  Google Scholar 

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Supported by the Thai National Research Council and the NSW State Cancer Council

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Thamavit, W., Kongkanuntn, R., Tiwawech, D. et al. Level ofOpisthorchis infestation and carcinogen dose-dependence of cholangiocarcinoma induction in Syrian golden hamsters. Virchows Archiv B Cell Pathol 54, 52–58 (1987). https://doi.org/10.1007/BF02899196

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  • DOI: https://doi.org/10.1007/BF02899196

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