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Fluke-Associated Cholangiocarcinoma: A Regional Epidemic

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Diagnosis and Management of Cholangiocarcinoma

Abstract

Cholangiocarcinoma (CCA) is an uncommon malignancy but occurs as a leading cancer in both sexes in Northeastern Thailand, an endemic area of a known CCA risk factor, the liver fluke (Opisthorchis viverrini). CCA is considered as an epidemic cancer in this geographic region, albeit based on serology testing, at least one fifth of CCA cases show no previous chronic exposure to fluke infestation. CCAs are adenocarcinoma that can present with various clinical features and differentiation. The histogenesis of the small bile duct type CCA is from hepatic stem cells in the canals of Hering and bile ductules, whereas the large bile duct type CCA is from bile duct stem cells located in peribiliary glands, embedded in the wall of large bile ducts. CCAs in the endemic area of liver flukes are primarily of the large bile duct type, which have two major phenotypes: tubular adenocarcinoma (accounting for two third of cases) and papillary carcinoma (accounting for the remaining third). The prognosis of CCA is dismal, with only half of patients surviving more than a year. Of note, the papillary phenotype of CCA has a better prognosis, which is attributable to the exophytic nature of the tumors, their late invasion into liver parenchyma, and ultrasonography screening being capable of detecting disease at an early stage. In this chapter, we discuss these and other aspects of fluke-associated CCA.

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Abbreviations

5-FU:

5-Fluorouracil

BilIN:

Biliary intraepithelial neoplasia

C. sinensis :

Clonorchis sinensis

CCA:

Cholangiocarcinoma

dCCA:

Distal cholangiocarcinoma

eCCA:

Extrahepatic cholangiocarcinoma

ELISA:

Enzyme-linked immunosorbent assay

HBsAg:

Hepatitis B surface antigen

HBV:

Hepatitis B virus

HCV Ab:

Hepatitis C antibody

HCV:

Hepatitis C virus

iCCA:

Intrahepatic cholangiocarcinoma

ID:

Intraductal-growing intrahepatic cholangiocarcinoma

IL-1:

Interleukin-1

IL-1β:

Interleukin-1β

IL-6:

Interleukin-6

IPNB:

Intraductal papillary neoplasm of bile duct

KKCR:

Khon Kaen Cancer Registry

KKH:

Khon Kaen University Hospital

MF:

Mass-forming intrahepatic cholangiocarcinoma

NF-κB:

Nuclear factor-κB

O. felineus :

Opisthorchis felineus

O. viverrini:

Opisthorchis viverrini

PBG:

Peribiliary gland

pCCA:

Perihilar cholangiocarcinoma

PI:

Periductal-infiltrating intrahepatic cholangiocarcinoma

TNF:

Tumor necrosis factor

References

  1. Khan SA, Tavolari S, Brandi G. Cholangiocarcinoma: epidemiology and risk factors. Liver Int. 2019;39:19–31.

    Article  PubMed  Google Scholar 

  2. Bragazzi MC, et al. Cholangiocarcinoma: epidemiology and risk factors. Transl Gastrointest Cancer. 2011;1(1):21–32.

    Google Scholar 

  3. Thamavit W, et al. Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverrini-infected Syrian golden hamsters. Cancer Res. 1978;38(12):4634–9.

    CAS  PubMed  Google Scholar 

  4. Flavell DJ, Lucas SB. 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. 1982;46(6):985–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lee JH, Rim HJ, Bak UB. Effect of Clonorchis sinensis infection and dimethylnitrosamine administration on the induction of cholangiocarcinoma in Syrian golden hamsters. Korean J Parasitol. 1993;31(1):21–30.

    Article  CAS  PubMed  Google Scholar 

  6. Sripa B, Tangkawattana S, Brindley PJ. Update on pathogenesis of opisthorchiasis and cholangiocarcinoma. Adv Parasitol. 2018;102:97–113.

    Article  PubMed  Google Scholar 

  7. Nakajima T, et al. A histopathologic study of 102 cases of intrahepatic cholangiocarcinoma: histologic classification and modes of spreading. Hum Pathol. 1988;19(10):1228–34.

    Article  CAS  PubMed  Google Scholar 

  8. Shirai T, et al. Histomorphological characteristics of cholangiocellular carcinomas in northeast Thailand, where a region infection with the liver fluke, Opisthorchis viverrini is endemic. Acta Pathol Jpn. 1992;42(10):734–9.

    CAS  PubMed  Google Scholar 

  9. Titapun A, et al. Outcome of curative resection for perihilar cholangiocarcinoma in Northeast Thailand. World J Gastrointest Oncol. 2015;7(12):503–12.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Pairojkul C. Liver fluke and cholangiocarcinoma in Thailand. Pathology. 2014;46(Suppl 2):24.

    Article  Google Scholar 

  11. Luvira V, et al. Long-term outcome of surgical resection for intraductal papillary neoplasm of the bile duct. J Gastroenterol Hepatol. 2017;32(2):527–33.

    Article  PubMed  Google Scholar 

  12. Luvira V, et al. Morphological classification of intraductal papillary neoplasm of the bile duct with survival correlation. Asian Pac J Cancer Prev. 2017;18(1):207–13.

    PubMed  PubMed Central  Google Scholar 

  13. Mas-Coma S, Valero MA, Bargues MD. Fascioliasis. Adv Exp Med Biol. 2014;766:77–114.

    Article  PubMed  Google Scholar 

  14. Farag HF, el Sayad MH. Biomphalaria alexandrina naturally infected with Fasciola gigantica in Egypt. Trans R Soc Trop Med Hyg. 1995;89(1):36.

    Article  CAS  PubMed  Google Scholar 

  15. Mas-Coma S, Bargues MD. Human liver flukes: a review res. Rev Parasitol. 1997;57(3–4):145–218.

    Google Scholar 

  16. Chen MGM, Mott KE. Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. World Health Organization. 1990. Unpublished: 44.

    Google Scholar 

  17. Shin HR, et al. Epidemiology of cholangiocarcinoma: an update focusing on risk factors. Cancer Sci. 2010;101(3):579–85.

    Article  CAS  PubMed  Google Scholar 

  18. Suwannatrai A, Saichua P, Haswell M. Epidemiology of Opisthorchis viverrini infection. Adv Parasitol. 2018;101:41–67.

    Article  PubMed  Google Scholar 

  19. Rollinson D. Control of foodborne trematode infections. Report of a WHO Study Group. Trans R Soc Trop Med Hyg. 1995;89(6):704.

    Article  Google Scholar 

  20. Lun ZR, et al. Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis. 2005;5(1):31–41.

    Article  PubMed  Google Scholar 

  21. Jongsuksuntigul P, Imsomboon T. Opisthorchiasis control in Thailand. Acta Trop. 2003;88(3):229–32.

    Article  CAS  PubMed  Google Scholar 

  22. Preuksaraj S. Public health aspects of opisthorchiasis in Thailand. Arzneimittelforschung. 1984;34(9B):1119–20.

    CAS  PubMed  Google Scholar 

  23. Srivatanakul P, et al. Liver cancer in Thailand: temporal and geographic variations. J Gastroenterol Hepatol. 1988;3(5):413–20.

    Article  Google Scholar 

  24. Sripa B, et al. Liver fluke induces cholangiocarcinoma. PLoS Med. 2007;4(7):e201.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Sithithaworn P, et al. The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitol Int. 2012;61(1):10–6.

    Article  PubMed  Google Scholar 

  26. Harinasuta T, Riganti M, Bunnag D. Opisthorchis viverrini infection: pathogenesis and clinical features. Arzneimittelforschung. 1984;34(9B):1167–9.

    CAS  PubMed  Google Scholar 

  27. Enes JE, et al. Prevalence of Opisthorchis viverrini infection in the canine and feline hosts in three villages, Khon Kaen Province, northeastern Thailand. Southeast Asian J Trop Med Public Health. 2010;41(1):36–42.

    PubMed  PubMed Central  Google Scholar 

  28. Johansen MV, Lier T, Sithithaworn P. Towards improved diagnosis of neglected zoonotic trematodes using a one health approach. Acta Trop. 2015;141(Pt B):161–9.

    Article  PubMed  Google Scholar 

  29. Jamornthanyawat N. The diagnosis of human opisthorchiasis. Southeast Asian J Trop Med Public Health. 2002;33(Suppl 3):86–91.

    PubMed  Google Scholar 

  30. Prakobwong S, et al. A large scale study of the epidemiology and risk factors for the carcinogenic liver fluke Opisthorchis viverrini in Udon Thani Province, Thailand. Asian Pac J Cancer Prev. 2017;18(10):2853–60.

    PubMed  PubMed Central  Google Scholar 

  31. Hughes T, et al. Opisthorchiasis and cholangiocarcinoma in Southeast Asia: an unresolved problem. Int J Gen Med. 2017;10:227–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Boonstra K, et al. Population-based epidemiology, malignancy risk, and outcome of primary sclerosing cholangitis. Hepatology. 2013;58(6):2045–55.

    Article  CAS  PubMed  Google Scholar 

  33. Nakanuma Y, et al. Are hepatolithiasis and cholangiocarcinoma aetiologically related? A morphological study of 12 cases of hepatolithiasis associated with cholangiocarcinoma. Virchows Arch A Pathol Anat Histopathol. 1985;406(1):45–58.

    Article  CAS  PubMed  Google Scholar 

  34. Matsumoto K, et al. Hepatitis B and C virus infection is a risk factor for the development of cholangiocarcinoma. Intern Med. 2014;53(7):651–4.

    Article  PubMed  Google Scholar 

  35. Segura-Lopez FK, Guitron-Cantu A, Torres J. Association between Helicobacter spp. infections and hepatobiliary malignancies: a review. World J Gastroenterol. 2015;21(5):1414–23.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kim TS, et al. Clonorchis sinensis, an oriental liver fluke, as a human biological agent of cholangiocarcinoma: a brief review. BMB Rep. 2016;49(11):590–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. IARC. Infection with liver flukes Opisthorchis viverrini, Opisthorchis felineus and Clonorchis sinensis. IARC Monogr Eval Carcinog Risks Hum. 1994;61:121–75.

    Google Scholar 

  38. Upatham ES, et al. Morbidity in relation to intensity of infection in Opisthorchiasis viverrini: study of a community in Khon Kaen, Thailand. Am J Trop Med Hyg. 1982;31(6):1156–63.

    Article  CAS  PubMed  Google Scholar 

  39. Upatham ES, et al. Relationship between prevalence and intensity of Opisthorchis viverrini infection, and clinical symptoms and signs in a rural community in north-east Thailand. Bull World Health Organ. 1984;62(3):451–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Riganti M, et al. Opisthorchis viverrini eggs and adult flukes as nidus and composition of gallstones. Southeast Asian J Trop Med Public Health. 1988;19(4):633–6.

    CAS  PubMed  Google Scholar 

  41. Sripa B, et al. The tumorigenic liver fluke Opisthorchis viverrini–multiple pathways to cancer. Trends Parasitol. 2012;28(10):395–407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lim JH. Liver flukes: the malady neglected. Korean J Radiol. 2011;12(2):269–79.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Sorvillo FJ. Food-borne parasitic zoonoses fish and plant-borne parasites (world class parasites). Emerg Infect Dis. 2008;14(9):1503a–1503.

    Article  Google Scholar 

  44. Hou PC. The pathology of Clonorchis sinensis infestation of the liver. J Pathol Bacteriol. 1955;70(1):53–64.

    Article  CAS  PubMed  Google Scholar 

  45. Bhamarapravati N, Thammavit W, Vajrasthira S. Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. Am J Trop Med Hyg. 1978;27(4):787–94.

    Article  CAS  PubMed  Google Scholar 

  46. Kim YI. Liver carcinoma and liver fluke infection. Arzneimittelforschung. 1984;34(9B):1121–6.

    CAS  PubMed  Google Scholar 

  47. Riganti M, et al. Human pathology of Opisthorchis viverrini infection: a comparison of adults and children. Southeast Asian J Trop Med Public Health. 1989;20(1):95–100.

    CAS  PubMed  Google Scholar 

  48. Rim HJ. Clonorchiasis: an update. J Helminthol. 2005;79(3):269–81.

    Article  PubMed  Google Scholar 

  49. Pairojkul C, et al. Multistage carcinogenesis of liver-fluke-associated cholangiocarcinoma in Thailand. Princess Takamatsu Symp. 1991;22:77–86.

    CAS  PubMed  Google Scholar 

  50. Sripa B, et al. Opisthorchiasis-associated biliary stones: light and scanning electron microscopic study. World J Gastroenterol. 2004;10(22):3318–21.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Verweij KE, van Buuren H. Oriental cholangiohepatitis (recurrent pyogenic cholangitis): a case series from the Netherlands and brief review of the literature. Neth J Med. 2016;74(9):401–5.

    CAS  PubMed  Google Scholar 

  52. Harris CC. Chemical and physical carcinogenesis: advances and perspectives for the 1990s. Cancer Res. 1991;51(18 Suppl):5023s–44s.

    CAS  PubMed  Google Scholar 

  53. Cardinale V, et al. Multipotent stem/progenitor cells in human biliary tree give rise to hepatocytes, cholangiocytes, and pancreatic islets. Hepatology. 2011;54(6):2159–72.

    Article  CAS  PubMed  Google Scholar 

  54. Carpino G, et al. Biliary tree stem/progenitor cells in glands of extrahepatic and intrahepatic bile ducts: an anatomical in situ study yielding evidence of maturational lineages. J Anat. 2012;220(2):186–99.

    Article  PubMed  Google Scholar 

  55. Bragazzi MC, et al. New insights into cholangiocarcinoma: multiple stems and related cell lineages of origin. Ann Gastroenterol. 2018;31(1):42–55.

    PubMed  Google Scholar 

  56. Sutton ME, et al. Regeneration of human extrahepatic biliary epithelium: the peribiliary glands as progenitor cell compartment. Liver Int. 2012;32(4):554–9.

    Article  PubMed  Google Scholar 

  57. Lanzoni G, Cardinale V, Carpino G. The hepatic, biliary, and pancreatic network of stem/progenitor cell niches in humans: a new reference frame for disease and regeneration. Hepatology. 2016;64(1):277–86.

    Article  PubMed  Google Scholar 

  58. De Jong IEM, et al. Repopulating the biliary tree from the peribiliary glands. Biochim Biophys Acta Mol basis Dis. 2018;1864(4 Pt B):1524–31.

    Article  PubMed  CAS  Google Scholar 

  59. Nakanuma Y, et al. Intrahepatic peribiliary glands of humans. II. Pathological spectrum. J Gastroenterol Hepatol. 1994;9(1):80–6.

    Article  CAS  PubMed  Google Scholar 

  60. Hughes NR, et al. Liver fluke-associated and sporadic cholangiocarcinoma: an immunohistochemical study of bile duct, peribiliary gland and tumour cell phenotypes. J Clin Pathol. 2006;59(10):1073–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Pinlaor S, et al. iNOS-dependent DNA damage via NF-kappaB expression in hamsters infected with Opisthorchis viverrini and its suppression by the antihelminthic drug praziquantel. Int J Cancer. 2006;119(5):1067–72.

    Article  CAS  PubMed  Google Scholar 

  62. Pinlaor S, et al. Mechanism of NO-mediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammation-mediated carcinogenesis. Nitric Oxide. 2004;11(2):175–83.

    Article  CAS  PubMed  Google Scholar 

  63. Pinlaor S, et al. 8-nitroguanine formation in the liver of hamsters infected with Opisthorchis viverrini. Biochem Biophys Res Commun. 2003;309(3):567–71.

    Article  CAS  PubMed  Google Scholar 

  64. Kawanishi S, et al. Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol Chem. 2006;387(4):365–72.

    Article  CAS  PubMed  Google Scholar 

  65. Sia D, et al. Intrahepatic cholangiocarcinoma: pathogenesis and rationale for molecular therapies. Oncogene. 2013;32(41):4861–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Endo K, et al. ERBB-2 overexpression and cyclooxygenase-2 up-regulation in human cholangiocarcinoma and risk conditions. Hepatology. 2002;36(2):439–50.

    Article  CAS  PubMed  Google Scholar 

  67. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol. 2003;15(6):740–6.

    Article  CAS  PubMed  Google Scholar 

  68. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest. 2003;112(12):1776–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Guarino M, Tosoni A, Nebuloni M. Direct contribution of epithelium to organ fibrosis: epithelial-mesenchymal transition. Hum Pathol. 2009;40(10):1365–76.

    Article  CAS  PubMed  Google Scholar 

  70. Sripa B, Pairojkul C. Cholangiocarcinoma: lessons from Thailand. Curr Opin Gastroenterol. 2008;24(3):349–56.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Zen Y, et al. Proposal of histological criteria for intraepithelial atypical/proliferative biliary epithelial lesions of the bile duct in hepatolithiasis with respect to cholangiocarcinoma: preliminary report based on interobserver agreement. Pathol Int. 2005;55(4):180–8.

    Article  PubMed  Google Scholar 

  72. Zen Y, et al. Biliary intraepithelial neoplasia: an international interobserver agreement study and proposal for diagnostic criteria. Mod Pathol. 2007;20(6):701–9.

    Article  PubMed  Google Scholar 

  73. Holzinger F, Graggen KZ, Buchler MW. Mechanisms of biliary carcinogenesis: a pathogenetic multi-stage cascade towards cholangiocarcinoma. Ann Oncol. 1999;10(Suppl 4):122–6.

    Article  PubMed  Google Scholar 

  74. Nagtegaal ID, et al. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182–8.

    Article  PubMed  Google Scholar 

  75. Miyata T, Uesaka K, Nakanuma Y. Cystic and papillary neoplasm at the hepatic hilum possibly originating in the peribiliary glands. Case Rep Pathol. 2016;2016:9130754.

    PubMed  PubMed Central  Google Scholar 

  76. Nakanishi Y, et al. Intraductal oncocytic papillary neoplasm of the bile duct: the first case of peribiliary gland origin. J Hepato-Biliary-Pancreat Surg. 2009;16(6):869–73.

    Article  Google Scholar 

  77. Nakanishi Y, et al. Intraductal papillary neoplasm arising from peribiliary glands connecting with the inferior branch of the bile duct of the anterior segment of the liver. Pathol Int. 2011;61(12):773–7.

    Article  PubMed  Google Scholar 

  78. Nakanuma Y, Kakuda Y. Pathologic classification of cholangiocarcinoma: new concepts. Best Pract Res Clin Gastroenterol. 2015;29(2):277–93.

    Article  PubMed  Google Scholar 

  79. Aishima S, et al. Histological features of precancerous and early cancerous lesions of biliary tract carcinoma. J Hepatobiliary Pancreat Sci. 2014;21(7):448–52.

    Article  PubMed  Google Scholar 

  80. Schlitter AM, et al. Intraductal papillary neoplasms of the bile duct: stepwise progression to carcinoma involves common molecular pathways. Mod Pathol. 2014;27(1):73–86.

    Article  CAS  PubMed  Google Scholar 

  81. Banales JM, et al. Expert consensus document: Cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European Network for the Study of Cholangiocarcinoma (ENS-CCA). Nat Rev Gastroenterol Hepatol. 2016;13(5):261–80.

    Article  PubMed  Google Scholar 

  82. Sia D, et al. Liver cancer cell of origin, molecular class, and effects on patient prognosis. Gastroenterology. 2017;152(4):745–61.

    Article  CAS  PubMed  Google Scholar 

  83. Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17(6):1471–4.

    Article  PubMed  Google Scholar 

  84. Blechacz B, et al. Clinical diagnosis and staging of cholangiocarcinoma. Nat Rev Gastroenterol Hepatol. 2011;8(9):512–22.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Krasinskas AM. Cholangiocarcinoma. Surg Pathol Clin. 2018;11(2):403–29.

    Article  PubMed  Google Scholar 

  86. Kamsa-Ard S, et al. Cholangiocarcinoma trends, incidence, and relative survival in Khon Kaen, Thailand from 1989 through 2013: a population-based cancer registry study. J Epidemiol. 2019;29(5):197–204.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Aishima S, et al. Proposal of progression model for intrahepatic cholangiocarcinoma: clinicopathologic differences between hilar type and peripheral type. Am J Surg Pathol. 2007;31(7):1059–67.

    Article  PubMed  Google Scholar 

  88. Nakanuma Y, Miyata T, Uchida T. Latest advances in the pathological understanding of cholangiocarcinomas. Expert Rev Gastroenterol Hepatol. 2016;10(1):113–27.

    Article  CAS  PubMed  Google Scholar 

  89. Uchida T, et al. Cystic micropapillary neoplasm of peribiliary glands with concomitant perihilar cholangiocarcinoma. World J Gastroenterol. 2016;22(7):2391–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Kudo M, et al. general rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: the outstanding achievements of the Liver Cancer Study Group of Japan. Dig Dis. 2015;33(6):765–70.

    Article  PubMed  Google Scholar 

  91. Isaji S, et al. Clinicopathological features and outcome of hepatic resection for intrahepatic cholangiocarcinoma in Japan. J Hepato-Biliary-Pancreat Surg. 1999;6(2):108–16.

    Article  CAS  Google Scholar 

  92. Luvira V, et al. Association between repeated praziquantel treatment and papillary, and intrahepatic cholangiocarcinoma. Ann Hepatol. 2018;17(5):802–9.

    Article  CAS  PubMed  Google Scholar 

  93. Chen TC, et al. Intraductal papillary neoplasia of the liver associated with hepatolithiasis. Hepatology. 2001;34(4 Pt 1):651–8.

    Article  CAS  PubMed  Google Scholar 

  94. Nakanuma Y, et al. Biliary papillary neoplasm of the liver. Histol Histopathol. 2002;17(3):851–61.

    CAS  PubMed  Google Scholar 

  95. Barusrux S, et al. Viral hepatitis B, C infection and genotype distribution among cholangiocarcinoma patients in northeast Thailand. Asian Pac J Cancer Prev. 2012;13(Suppl):83–7.

    PubMed  Google Scholar 

  96. Ariizumi S, Yamamoto M. Intrahepatic cholangiocarcinoma and cholangiolocellular carcinoma in cirrhosis and chronic viral hepatitis. Surg Today. 2015;45(6):682–7.

    Article  PubMed  Google Scholar 

  97. Aishima S, Oda Y. Pathogenesis and classification of intrahepatic cholangiocarcinoma: different characters of perihilar large duct type versus peripheral small duct type. J Hepatobiliary Pancreat Sci. 2015;22(2):94–100.

    Article  PubMed  Google Scholar 

  98. Luvira V, et al. Cholangiocarcinoma patient outcome in Northeastern Thailand: single-center prospective study. Asian Pac J Cancer Prev. 2016;17(1):401–6.

    Article  PubMed  Google Scholar 

  99. Park J, et al. Natural history and prognostic factors of advanced cholangiocarcinoma without surgery, chemotherapy, or radiotherapy: a large-scale observational study. Gut Liver. 2009;3(4):298–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Yusoff AR, et al. Survival analysis of cholangiocarcinoma: a 10-year experience in Malaysia. World J Gastroenterol. 2012;18(5):458–65.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Bridgewater J, et al. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. J Hepatol. 2014;60(6):1268–89.

    Article  PubMed  Google Scholar 

  102. Konstantinidis IT, Arkadopoulos N, Ferrone CR. Surgical management of intrahepatic cholangiocarcinoma in the modern era: advances and challenges. Chin Clin Oncol. 2016;5(1):9.

    PubMed  Google Scholar 

  103. Spolverato G, et al. Management and outcomes of patients with recurrent intrahepatic cholangiocarcinoma following previous curative-intent surgical resection. Ann Surg Oncol. 2016;23(1):235–43.

    Article  PubMed  Google Scholar 

  104. Luvira V, et al. Patterns of recurrence after resection of mass-forming type intrahepatic cholangiocarcinomas. Asian Pac J Cancer Prev. 2016;17(10):4735–9.

    PubMed  PubMed Central  Google Scholar 

  105. Adachi T, Eguchi S. Lymph node dissection for intrahepatic cholangiocarcinoma: a critical review of the literature to date. J Hepatobiliary Pancreat Sci. 2014;21(3):162–8.

    Article  PubMed  Google Scholar 

  106. Morine Y, Shimada M. The value of systematic lymph node dissection for intrahepatic cholangiocarcinoma from the viewpoint of liver lymphatics. J Gastroenterol. 2015;50(9):913–27.

    Article  CAS  PubMed  Google Scholar 

  107. Igami T, et al. Surgical treatment of hilar cholangiocarcinoma in the “new era”: the Nagoya University experience. J Hepatobiliary Pancreat Sci. 2010;17(4):449–54.

    Article  PubMed  Google Scholar 

  108. Neuhaus P, et al. Oncological superiority of hilar en bloc resection for the treatment of hilar cholangiocarcinoma. Ann Surg Oncol. 2012;19(5):1602–8.

    Article  PubMed  Google Scholar 

  109. Yeh TS, et al. Characterization of intrahepatic cholangiocarcinoma of the intraductal growth-type and its precursor lesions. Hepatology. 2005;42(3):657–64.

    Article  PubMed  Google Scholar 

  110. Yeh TS, et al. Cholangiographic spectrum of intraductal papillary mucinous neoplasm of the bile ducts. Ann Surg. 2006;244(2):248–53.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Jarnagin WR, et al. Papillary phenotype confers improved survival after resection of hilar cholangiocarcinoma. Ann Surg. 2005;241(5):703–12. discussion 712-4.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Jan YY, et al. Prognostic analysis of surgical treatment of peripheral cholangiocarcinoma: two decades of experience at Chang Gung Memorial Hospital. World J Gastroenterol. 2005;11(12):1779–84.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Yeh CN, et al. Hepatic resection for hepatocellular carcinoma in elderly patients. Hepato-Gastroenterology. 2004;51(55):219–23.

    PubMed  Google Scholar 

  114. Taal BG, et al. Phase II trial of mitomycin C (MMC) in advanced gallbladder and biliary tree carcinoma. An EORTC Gastrointestinal Tract Cancer Cooperative Group Study. Ann Oncol. 1993;4(7):607–9.

    Article  CAS  PubMed  Google Scholar 

  115. Okada S, et al. A phase II study of cisplatin in patients with biliary tract carcinoma. Oncology. 1994;51(6):515–7.

    Article  CAS  PubMed  Google Scholar 

  116. Okusaka T, et al. Gemcitabine alone or in combination with cisplatin in patients with biliary tract cancer: a comparative multicentre study in Japan. Br J Cancer. 2010;103(4):469–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Valle J, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362(14):1273–81.

    Article  CAS  PubMed  Google Scholar 

  118. Skipworth JR, et al. Review article: surgical, neo-adjuvant and adjuvant management strategies in biliary tract cancer. Aliment Pharmacol Ther. 2011;34(9):1063–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Wirasorn K, et al. Adjuvant chemotherapy in resectable cholangiocarcinoma patients. J Gastroenterol Hepatol. 2013;28(12):1885–91.

    Article  CAS  PubMed  Google Scholar 

  120. Ringborg U. Adjuvant chemotherapy. a discussion of some basic principles. Acta Oncol. 1991;30(2):251–3.

    Article  CAS  PubMed  Google Scholar 

  121. Epstein RJ. Maintenance therapy to suppress micrometastasis: the new challenge for adjuvant cancer treatment. Clin Cancer Res. 2005;11(15):5337–41.

    Article  CAS  PubMed  Google Scholar 

  122. Bunnag D, Harinasuta T. Studies on the chemotherapy of human opisthorchiasis in Thailand: I. Clinical trial of praziquantel. Southeast Asian J Trop Med Public Health. 1980;11(4):528–31.

    CAS  PubMed  Google Scholar 

  123. Upatham ES, et al. Rate of re-infection by Opisthorchis viverrini in an endemic northeast Thai community after chemotherapy. Int J Parasitol. 1988;18(5):643–9.

    Article  CAS  PubMed  Google Scholar 

  124. Jongsuksuntigul P, Imsomboon T. Epidemiology of opisthorchiasis and national control program in Thailand. Southeast Asian J Trop Med Public Health. 1998;29(2):327–32.

    CAS  PubMed  Google Scholar 

  125. Steele JA, et al. Thinking beyond Opisthorchis viverrini for risk of cholangiocarcinoma in the lower Mekong region: a systematic review and meta-analysis. Infect Dis Poverty. 2018;7(1):44.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Kamsa-ard S, et al. Association between praziquantel and cholangiocarcinoma in patients infected with Opisthorchis viverrini: a systematic review and meta-analysis. Asian Pac J Cancer Prev. 2013;14(11):7011–6.

    Article  PubMed  Google Scholar 

  127. Weber A, Schmid RM, Prinz C. Diagnostic approaches for cholangiocarcinoma. World J Gastroenterol. 2008;14(26):4131–6.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Mairiang E, et al. Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand. Parasitol Int. 2012;61(1):208–11.

    Article  PubMed  Google Scholar 

  129. Mairiang E, et al. Relationship between intensity of Opisthorchis viverrini infection and hepatobiliary disease detected by ultrasonography. J Gastroenterol Hepatol. 1992;7(1):17–21.

    Article  CAS  PubMed  Google Scholar 

  130. Weill F, Eisencher A, Zeltner F. Ultrasonic study of the normal and dilated biliary tree. The “shotgun” sign. Radiology. 1978;127(1):221–4.

    Article  CAS  PubMed  Google Scholar 

  131. Catalano OA, et al. Biliary infections: spectrum of imaging findings and management. Radiographics. 2009;29(7):2059–80.

    Article  PubMed  Google Scholar 

  132. Sripa B, et al. Advanced periductal fibrosis from infection with the carcinogenic human liver fluke Opisthorchis viverrini correlates with elevated levels of interleukin-6. Hepatology. 2009;50(4):1273–81.

    Article  CAS  PubMed  Google Scholar 

  133. Karcaaltincaba M, et al. Multidetector CT and MRI findings in periportal space pathologies. Eur J Radiol. 2007;61(1):3–10.

    Article  PubMed  Google Scholar 

  134. Chamadol N, et al. Histological confirmation of periductal fibrosis from ultrasound diagnosis in cholangiocarcinoma patients. J Hepatobiliary Pancreat Sci. 2014;21(5):316–22.

    Article  PubMed  Google Scholar 

  135. Sripa B, et al. Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Trop. 2011;120(Suppl 1):S158–68.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

    Sakda Waraasawapati, Raksawan Deenonpoe, Prakasit Sa-ngiamwibool, Yaovalux Chamgramol & Chawalit Pairojkul

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  1. Sakda Waraasawapati
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  2. Raksawan Deenonpoe
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  3. Prakasit Sa-ngiamwibool
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  4. Yaovalux Chamgramol
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  5. Chawalit Pairojkul
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Correspondence to Chawalit Pairojkul .

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  1. Division of Gastroenterology, Department of Medicine, Olive View-UCLA Medical Center, Sylmar, CA, USA

    James H. Tabibian

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Waraasawapati, S., Deenonpoe, R., Sa-ngiamwibool, P., Chamgramol, Y., Pairojkul, C. (2021). Fluke-Associated Cholangiocarcinoma: A Regional Epidemic. In: Tabibian, J.H. (eds) Diagnosis and Management of Cholangiocarcinoma. Springer, Cham. https://doi.org/10.1007/978-3-030-70936-5_11

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