Journal of Korean Medical Science

Korean Acad Medical Sciences (대한의학회)
권호 표지
DOI QR코드

DOI QR Code

Descriptive Epidemiology of Cholangiocarcinoma and Clonorchiasis in Korea

  • Shin, Hai-Rim (International Agency for Research on Cancer) ;
  • Oh, Jin-Kyoung (National Cancer Control Institute, National Cancer Center) ;
  • Lim, Min-Kyung (National Cancer Control Institute, National Cancer Center) ;
  • Shin, Ae-Sun (Research Institute, Center for Liver Cancer, National Cancer Center) ;
  • Kong, Hyun-Joo (The Korea Central Cancer Registry, National Cancer Center) ;
  • Jung, Kyu-Won (The Korea Central Cancer Registry, National Cancer Center) ;
  • Won, Young-Joo (The Korea Central Cancer Registry, National Cancer Center) ;
  • Park, So-Hee (The Korea Central Cancer Registry, National Cancer Center) ;
  • Park, Sang-Jae (Research Institute and Hospital, National Cancer Center) ;
  • Hong, Sung-Tae (Department of Parasitology, Seoul National University, College of Medicine)
  • Published : 2010.07.30
⟨ Previous Next ⟩

Abstract

In 2009, infection with the liver fluke Clonorchis sinensis (C. sinensis) was classified as "carcinogenic to humans" (Group 1) based on its involvement in the etiology of cholangiocarcinoma by the International Agency for Research on Cancer. However, little is known about the descriptive epidemiology of cholangiocarcinoma in Korea. We examined incidence trends of intrahepatic and extrahepatic cholangiocarcinomas, using data from the Korea National Cancer Incidence database for 1999-2005. The prevalence of C. sinensis infection was estimated from a recent population-based survey in rural endemic areas. Cholangiocarcinoma incidence rates are currently rising, even while primary liver cancer incidence rates are decreasing. Annual percent changes in cholangiocarcinoma incidence rates were 8% for males and 11% in females. Known areas of C. sinensis endemicity showed high incidence rates of cholangiocarcinoma. The positivity of C. sinensis eggs in stool samples from endemic areas was more than 25% of adults tested during 2005-2008. From a meta-analysis, the summary odds ratio for cholangiocarcinoma due to C. sinensis infection was 4.7 (95% confidence interval: 2.2-9.8). Approximately 10% of cholangiocarcinomas in Korea were caused by chronic C. sinensis infections. More specific policies, including health education and an extensive effort for early detection in endemic areas, are needed.

Keywords

References

  1. Kaewkes S. Taxonomy and biology of liver flukes. Acta Tropica 2003; 88: 177-86. https://doi.org/10.1016/j.actatropica.2003.05.001
  2. Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY. Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 2005; 5: 31-41. https://doi.org/10.1016/S1473-3099(04)01252-6
  3. International Agency for Research on Cancer. Schistosomes, liver flukes and Helicobactor pylori. IARC monographs on the evaluation of carcinogenic risks to humans., vol. 61. Lyon France: International Agency for Research on Cancer, 1994.
  4. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V. A review of human carcinogens-Part B: biological agents. Lancet Oncol 2009; 10: 321-2. https://doi.org/10.1016/S1470-2045(09)70096-8
  5. Lim MK, Ju YH, Franceschi S, Oh JK, Kong HJ, Hwang SS, Park SK, Cho SI, Sohn WM, Kim DI, Yoo KY, Hong ST, Shin HR. Clonorchis sinensis infection and increasing risk of cholangiocarcinoma in the Republic of Korea. Am J Trop Med Hyg 2006; 75: 93-6.
  6. Shin HR, Lee CU, Park HJ, Seol SY, Chung JM, Choi HC, Ahn YO, Shigemastu T. Hepatitis B and C virus, Clonorchis sinensis for the risk of liver cancer: a case-control study in Pusan, Korea. Int J Epidemiol 1996; 25: 933-40. https://doi.org/10.1093/ije/25.5.933
  7. Choi D, Lim JH, Lee KT, Lee JK, Choi SH, Heo JS, Jang KT, Lee NY, Kim S, Hong ST. Cholangiocarcinoma and Clonorchis sinensis infection: a case-control study in Korea. J Hepatol 2006; 44: 1066-73. https://doi.org/10.1016/j.jhep.2005.11.040
  8. Lee TY, Lee SS, Jung SW, Jeon SH, Yun SC, Oh HC, Kwon S, Lee SK, Seo DW, Kim MH, Suh DJ. Hepatitis B virus infection and intrahepatic cholangiocarcinoma in Korea: a case-control study. Am J Gastroenterol 2008; 103: 1716-20. https://doi.org/10.1111/j.1572-0241.2008.01796.x
  9. Kim YI, Yang DH, Chang KR. Relationship between Clonorchis sinensis infestation and cholangiocarcinoma of the liver in Korea. Seoul J Med 1974; 15: 247-53 (in Korean).
  10. Chung CS, Lee SK. An epidemiological study of primary liver carcinomas in Busan area with special reference to clonorchis. Korean J Pathol 1976; 10: 33-46.
  11. World Health Organization. International Classification of Diseases, vol. 10. Geneva: World Health Organization, 1992.
  12. Fritz A, Percy C, Jack A, Shanmugaratnam K, Parkin M. International classification of diseases for oncology (ICD-O), 3rd ed. Geneva, Switzerland: World Health Organization, 2000.
  13. Shin HR, Won YJ, Jung KW, Park JG, Hong EK, Suh CI, Lee SY, Kim KY, Seo SW, Lee JK. Cancer Incidence in Korea (1999-2002). Cancer Incidence in Five Continents Volume IX. Lyon: International Agency for Research on Cancer, 2007.
  14. Won YJ, Sung J, Jung KW, Kong HJ, Park SK, Shin HR, Park EC, Ahn YO, Hwang IK, Lee DH, Choi JS, Kim WC, Lee TY, Yoo CI, Bae JM, Kim ON, Park IS, Kong IS, Lee DH, Lee JS. Nationwide Cancer Incidence in Korea, 2003-2005. Cancer Res Treat 2009; 41: 122-31. https://doi.org/10.4143/crt.2009.41.3.122
  15. Kim TS, Cho SH, Huh S, Kong Y, Sohn WM, Hwang SS, Chai JY, Lee SH, Park YK, Oh DK, Lee JK. A nationwide survey on the prevalence of intestinal parasitic infections in the Republic of Korea, 2004. Korean J Parasitol 2009; 47: 37-47. https://doi.org/10.3347/kjp.2009.47.1.37
  16. McGlynn KA, Tarone RE, El-Serag HB. A comparison of trends in the incidence of hepatocellular carcinoma and intrahepatic cholangiocarcinoma in the United States. Cancer Epidemiol Biomarkers Prev 2006; 15: 1198-203. https://doi.org/10.1158/1055-9965.EPI-05-0811
  17. West J, Wood H, Logan RF, Quinn M, Aithal GP. Trends in the incidence of primary liver and biliary tract cancers in England and Wales 1971-2001. Brit J Cancer 2006; 94: 1751-8. https://doi.org/10.1038/sj.bjc.6603127
  18. Welzel TM, McGlynn KA, Hsing AW, O'Brien TR, Pfeiffer RM. Impact of classification of hilar cholangiocarcinomas (Klatskin tumors) on the incidence of intra- and extrahepatic cholangiocarcinoma in the United States. J Natl Cancer Inst 2006; 98: 873-5. https://doi.org/10.1093/jnci/djj234
  19. Rim HJ. Clonorchiasis: an update. J Helminthol 2005; 79: 269-81. https://doi.org/10.1079/JOH2005300
  20. Blechacz BR, Gores GJ. Cholangiocarcinoma. Clin Liver Dis 2008; 12: 131-50. https://doi.org/10.1016/j.cld.2007.11.003
  21. Khan SA, Toledano MB, Taylor-Robinson SD. Epidemiology, risk factors, and pathogenesis of cholangiocarcinoma. HPB (Oxford) 2008; 10: 77-82. https://doi.org/10.1080/13651820801992641
  22. de Groen PC, Gores GJ, LaRusso NF, Gunderson LL, Nagorney DM. Biliary tract cancers. N Engl J Med 1999; 341: 1368-78. https://doi.org/10.1056/NEJM199910283411807
  23. Okuda K, Nakanuma Y, Miyazaki M. Cholangiocarcinoma: recent progress. Part 1: epidemiology and etiology. J Gastroenterol Hepatol 2002; 17: 1049-55. https://doi.org/10.1046/j.1440-1746.2002.02781.x
  24. Chen MF, Jan YY, Jeng LB, Hwang TL, Wang CS, Chen SC, Chao TC, Chen HM, Lee WC, Yeh TS, Lo YF. Intrahepatic cholangiocarcinoma in Taiwan. J Hepatobiliary Pancreat Surg 1999; 6: 136-41. https://doi.org/10.1007/s005340050096
  25. Kubo S, Kinoshita H, Hirohashi K, Hamba H. Hepatolithiasis associated with cholangiocarcinoma. World J Surg 1995; 19: 637-41. https://doi.org/10.1007/BF00294744
  26. Kim YT, Byun JS, Kim J, Jang YH, Lee WJ, Ryu JK, Kim SW, Yoon YB, Kim CY. Factors predicting concurrent cholangiocarcinomas associated with hepatolithiasis. Hepatogastroenterology 2003; 50: 8-12.

Cited by

  1. Estimation of cancer incidence and mortality attributable to alcohol drinking in china vol.10, pp.1, 2010, https://doi.org/10.1186/1471-2458-10-730
  2. Risk factors for cholangiocarcinoma vol.54, pp.1, 2010, https://doi.org/10.1002/hep.24351
  3. Developmental Transcriptomic Features of the Carcinogenic Liver Fluke, Clonorchis sinensis vol.5, pp.6, 2011, https://doi.org/10.1371/journal.pntd.0001208
  4. Prevalence of Clonorchis sinensis infection in dogs and cats in subtropical southern China vol.4, pp.None, 2011, https://doi.org/10.1186/1756-3305-4-180
  5. The global epidemiology of clonorchiasis and its relation with cholangiocarcinoma vol.1, pp.1, 2010, https://doi.org/10.1186/2049-9957-1-4
  6. In Vitro Maintenance of Clonorchis sinensis Adult Worms vol.50, pp.4, 2010, https://doi.org/10.3347/kjp.2012.50.4.309
  7. Liver Transplantation for the Curative Treatment of Hilar Cholangiocarcinoma - Model of the Mayo Clinic - vol.26, pp.1, 2010, https://doi.org/10.4285/jkstn.2012.26.1.1
  8. Biochemical characterization and functional analysis of fructose-1,6-bisphosphatase from Clonorchis sinensis vol.40, pp.7, 2010, https://doi.org/10.1007/s11033-013-2508-4
  9. Two Cases of Unresectable Cholangiocarcinoma Treated by Yttrium-90 Microspheres vol.69, pp.2, 2010, https://doi.org/10.3348/jksr.2013.69.2.143
  10. A Survey of Intestinal Parasite Infection during a 10-Year Period (2003-2012) vol.16, pp.3, 2010, https://doi.org/10.5145/acm.2013.16.3.134
  11. Clinical Update on Parasitic Diseases vol.85, pp.5, 2013, https://doi.org/10.3904/kjm.2013.85.5.469
  12. Pathogenesis, Diagnosis, and Management of Cholangiocarcinoma vol.145, pp.6, 2010, https://doi.org/10.1053/j.gastro.2013.10.013
  13. Secular Trends in the Incidence of Cholangiocarcinoma in the USA and the Impact of Misclassification vol.59, pp.12, 2010, https://doi.org/10.1007/s10620-014-3276-2
  14. Prevalence and Risk Factors of Clonorchiasis among Residents of Riverside Areas in Muju-gun, Jeollabuk-do, Korea vol.52, pp.4, 2010, https://doi.org/10.3347/kjp.2014.52.4.391
  15. Control of clonorchiasis in Korea: effectiveness of health education for community leaders and individuals in an endemic area vol.19, pp.9, 2010, https://doi.org/10.1111/tmi.12338
  16. Infection and Cancer: Global Distribution and Burden of Diseases vol.80, pp.5, 2014, https://doi.org/10.1016/j.aogh.2014.09.013
  17. Mutation Profiling in Cholangiocarcinoma: Prognostic and Therapeutic Implications vol.9, pp.12, 2010, https://doi.org/10.1371/journal.pone.0115383
  18. Estimation of Cancer Burden Attributable to Infection in Asia vol.25, pp.10, 2010, https://doi.org/10.2188/jea.je20140215
  19. Sarcomatoid cholangiocarcinoma with osteoclast-like giant cells associated with hepatolithiasis: A case report vol.21, pp.3, 2010, https://doi.org/10.3350/cmh.2015.21.3.309
  20. Involvement of PSMD10, CDK4, and Tumor Suppressors in Development of Intrahepatic Cholangiocarcinoma of Syrian Golden Hamsters Induced by Clonorchis sinensis and N-Nitrosodimethylamine vol.9, pp.8, 2015, https://doi.org/10.1371/journal.pntd.0004008
  21. Clonorchis sinensis ova in bile juice cytology from a patient with severe hyperbilirubinemia and portal vein thrombosis vol.44, pp.3, 2010, https://doi.org/10.1002/dc.23400
  22. Ring finger protein 43 expression is associated with genetic alteration status and poor prognosis among patients with intrahepatic cholangiocarcinoma vol.52, pp.None, 2016, https://doi.org/10.1016/j.humpath.2015.12.027
  23. C3H/He Mice as an Incompatible Cholangiocarcinoma Model by Clonorchis sinensis, Dicyclanil and N-Nitrosodimethylamine vol.54, pp.3, 2016, https://doi.org/10.3347/kjp.2016.54.3.281
  24. Clonorchis sinensis, an oriental liver fluke, as a human biological agent of cholangiocarcinoma: a brief review vol.49, pp.11, 2016, https://doi.org/10.5483/bmbrep.2016.49.11.109
  25. In-vivo monitoring of development of cholangiocarcinoma induced with C. sinensis and N-nitrosodimethylamine in Syrian golen hamsters using ultrasonography and magnetic resonance imaging: a preliminary vol.27, pp.4, 2010, https://doi.org/10.1007/s00330-016-4510-4
  26. Unexpected hosts: imaging parasitic diseases vol.8, pp.1, 2010, https://doi.org/10.1007/s13244-016-0525-2
  27. Cohort Profile: Community-based prospective cohort from the National Cancer Center, Korea vol.46, pp.2, 2010, https://doi.org/10.1093/ije/dyv302
  28. The Role of Cancer-Associated Fibroblasts and Fibrosis in Liver Cancer vol.12, pp.None, 2017, https://doi.org/10.1146/annurev-pathol-052016-100322
  29. Characteristics and outcomes of cholangiocarcinoma by region in Thailand: A nationwide study vol.23, pp.39, 2010, https://doi.org/10.3748/wjg.v23.i39.7160
  30. Increasing burden of liver cancer despite extensive use of antiviral agents in a hepatitis B virus‐endemic population vol.66, pp.5, 2010, https://doi.org/10.1002/hep.29321
  31. Responding to Letter “Comments on ‘Screening US Vietnam Veterans for Liver Fluke Exposure 5 Decades After the End of the War’” by Theodore E. Nash, David Sullivan, Edward Mitre vol.26, pp.4, 2010, https://doi.org/10.1097/ipc.0000000000000660
  32. Prediction of thromboembolic complications after liver resection for cholangiocarcinoma: is there a place for thromboelastometry? vol.29, pp.1, 2010, https://doi.org/10.1097/mbc.0000000000000672
  33. Programmed knockout mutation of liver fluke granulin attenuates virulence of infection-induced hepatobiliary morbidity vol.8, pp.None, 2010, https://doi.org/10.7554/elife.41463
  34. Incidence and Overall Survival of Biliary Tract Cancers in South Korea from 2006 to 2015: Using the National Health Information Database vol.13, pp.1, 2019, https://doi.org/10.5009/gnl18105
  35. Cholangiocarcinoma: Epidemiology and risk factors vol.39, pp.suppl, 2010, https://doi.org/10.1111/liv.14095
  36. Mitogen-Activated Protein Kinases (MAPKs) and Cholangiocarcinoma: The Missing Link vol.8, pp.10, 2010, https://doi.org/10.3390/cells8101172
  37. Global Trends in Incidence Rates of Primary Adult Liver Cancers: A Systematic Review and Meta-Analysis vol.10, pp.None, 2020, https://doi.org/10.3389/fonc.2020.00171
  38. Review of Successful Control of Parasitic Infections in Korea vol.52, pp.3, 2010, https://doi.org/10.3947/ic.2020.52.3.427
  39. Management Strategies for Patients with Hilar Cholangiocarcinomas: Challenges and Solutions vol.12, pp.None, 2010, https://doi.org/10.2147/hmer.s223022
  40. Clonorchiasis in Patients with Biliary and Pancreatic Diseases: Diagnosis and Risk Factors vol.2020, pp.None, 2010, https://doi.org/10.1155/2020/2946541
  41. Clinical implication of tumor site in terms of node metastasis for intrahepatic cholangiocarcinoma vol.46, pp.5, 2010, https://doi.org/10.1016/j.ejso.2019.11.511
  42. Clinicopathological characteristics of intrahepatic cholangiocarcinoma according to gross morphologic type: cholangiolocellular differentiation traits and inflammation- and proliferation-phenotypes vol.22, pp.6, 2010, https://doi.org/10.1016/j.hpb.2019.10.009
  43. Global trends in intrahepatic and extrahepatic cholangiocarcinoma incidence from 1993 to 2012 vol.126, pp.11, 2010, https://doi.org/10.1002/cncr.32803
  44. High endemicity of Clonorchis sinensis infection in Binyang County, southern China vol.14, pp.8, 2010, https://doi.org/10.1371/journal.pntd.0008540
  45. Intrahepatic cholangiocarcinomas with IDH1/2 mutation-associated hypermethylation at selective genes and their clinicopathological features vol.10, pp.1, 2010, https://doi.org/10.1038/s41598-020-72810-0
  46. Trends and Characteristics of Endoscopic Retrograde Cholangiopancreatography: A Nationwide Database Study in Korea vol.26, pp.3, 2010, https://doi.org/10.15279/kpba.2021.26.3.186
  47. Clinical Characteristics of Clonorchis sinensis-Associated Cholangiocarcinoma: A Large-Scale, Single-Center Study vol.8, pp.None, 2010, https://doi.org/10.3389/fmed.2021.675207
  48. The Clinical Management of Cholangiocarcinoma in the United States and Europe: A Comprehensive and Evidence-Based Comparison of Guidelines vol.28, pp.5, 2010, https://doi.org/10.1245/s10434-021-09671-y
  49. Omega-Class Glutathione Transferases of Carcinogenic Liver Fluke, Clonorchis sinensis, Modulate Apoptosis and Differentiation of Host Cholangiocytes vol.10, pp.7, 2010, https://doi.org/10.3390/antiox10071017
  50. Microbiome in human cancers vol.3, pp.8, 2010, https://doi.org/10.1099/acmi.0.000247
  51. Cholangiocarcinoma vol.7, pp.1, 2010, https://doi.org/10.1038/s41572-021-00300-2