Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Relationship between Clonorchis sinensis Infection and Cholangiocarcinoma in Korea

  • Kim, Hwa Sun (Department of Family Medicine, Veterans Health Service Medical Center) ;
  • Nam, Ho-Woo (Department of Parasitology, College of Medicine, Catholic University of Korea) ;
  • Ahn, Hye-Jin (Department of Parasitology, College of Medicine, Catholic University of Korea) ;
  • Kim, Dongjae (Department of Biomedicine Health Science, College of Medicine, The Catholic University of Korea) ;
  • Kim, Yeong Hoon (Department of Ophthalmology, College of Medicine, Catholic University of Korea)
  • Received : 2022.05.09
  • Accepted : 2022.07.28
  • Published : 2022.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

This study provides an overview of the current status of clonorchiasis and cholangiocarcinoma (CCA), and their relationship in Korea during 2012-2020. Data were obtained from the Health Insurance Review & Assessment Service of Korea. Cluster, trend, and correlation analyses were performed. Gyeongsangnam-do and Seoul had the highest average number of cases (1,026 and 4,208) and adjusted rate (306 and 424) for clonorchiasis and CCA, respectively. The most likely clusters (MLC) for clonorchiasis and CCA were Busan/Gyeongsangnam-do/Ulsan/Daegu/Gyeongsangbuk-do (Relative Risk; RR=4.55, Likelihood Ratio; LLR=9,131.115) joint cluster and Seoul (RR=2.29, LLR=7,602.472), respectively. The MLC for clonorchiasis was in the southeastern part of Korea, while that for CCA was in the southern part. Clonorchiasis showed a decreasing trend in the southeastern districts, while increased in the southwestern districts. Cities in the central region had a decreasing trend, while the western districts had an increasing trend. In most adults (30-59), infection rate of clonorchiasis showed a significant decrease until 2018, while thereafter increased, although not significant. CCA showed a sharply decreasing tendency. The incidence of clonorchiasis and CCA were positively correlated. In general, the correlation was weak (r=0.39, P<0.001), but it was strongly positive around the 4 river basins (r=0.74, P<0.001). This study might provide an analytic basis for developing an effective system against clonorchiasis and CCA.

Keywords

Acknowledgement

This study was supported by a research grant from the Korean Association of Health Promotion (No. 2015-01), Republic of Korea.

References

  1. Jeong YI, Shin HE, Lee SE, Cheun HI, Ju JW, Kim JY, Park MY, Cho SH. Prevalence of Clonorchis sinensis Infection among Residents along 5 Major Rivers in the Republic of Korea. Korean J Parasitol 2016; 54: 215-219. https://doi.org/10.3347/kjp.2016.54.2.215
  2. Hong ST, Chai JY, Choi MH, Huh S, Rim HJ, Lee SH. A successful experience of soil-transmitted helminth control in the Republic of Korea. Korean J Parasitol 2006; 44: 177-185. https://doi.org/10.3347/kjp.2006.44.3.177
  3. Shin EH, Guk SM, Kim HJ, Lee SH, Chai JY. Trends in parasitic diseases in the Republic of Korea. Trends Parasitol 2008; 24: 143-150. https://doi.org/10.1016/j.pt.2007.12.003
  4. Rim HJ. Clonorchiasis: an update. J Helminthol 2005; 79: 269-281. https://doi.org/10.1079/joh2005300
  5. Brindley PJ, Bachini M, Ilyas SI, Khan SA, Loukas A, Sirica AE, Teh BT, Wongkham S, Gores GJ. Cholangiocarcinoma. Nat Rev Dis Primers 2021; 7: 65-81. https://doi.org/10.1038/s41572-021-00300-2
  6. Cho SH, Lee KY, Lee BC, Cho PY, Cheun HI, Hong ST, Sohn WM, Kim TS. Prevalence of clonorchiasis in southern endemic areas of Korea in 2006. Korean J Parasitol 2008; 46: 133-137. https://doi.org/10.3347/kjp.2008.46.3.133
  7. Hong ST, Fang Y. Clonorchis sinensis and clonorchiasis, an update. Parasitol Int 2012; 6117-6124. https://doi.org/https://doi.org/10.1016/j.parint.2011.06.007
  8. 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: 321-322. https://doi.org/10.1016/S1470-2045(09)70096-8
  9. Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, MacIntyre MF, Allen C, Hansen G, Woodbrook R, Wolfe C, Hamadeh RR, Moore A, Werdecker A, Gessner BD, Te Ao B, McMahon B, Karimkhani C, Yu C, Cooke GS, Schwebel DC, Carpenter DO, Pereira DM, Nash D, Kazi DS, De Leo D, Plass D, Ukwaja KN, Thurston GD, Yun Jin K, Simard EP, Mills E, Park EK, CatalaLopez F, deVeber G, Gotay C, Khan G, Hosgood HD 3rd, Santos IS, Leasher JL, Singh J, Leigh J, Jonas JB, Sanabria J, Beardsley J, Jacobsen KH, Takahashi K, Franklin RC, Ronfani L, Montico M, Naldi L, Tonelli M, Geleijnse J, Petzold M, Shrime MG, Younis M, Yonemoto N, Breitborde N, Yip P, Pourmalek F, Lotufo PA, Esteghamati A, Hankey GJ, Ali R, Lunevicius R, Malekzadeh R, Dellavalle R, Weintraub R, Lucas R, Hay R, Rojas-Rueda D, Westerman R, Sepanlou SG, Nolte S, Patten S, Weichenthal S, Abera SF, Fereshtehnejad SM, Shiue I, Driscoll T, Vasankari T, Alsharif U, Rahimi-Movaghar V, Vlassov VV, Marcenes WS, Mekonnen W, Melaku YA, Yano Y, Artaman A, Campos I, MacLachlan J, Mueller U, Kim D, Trillini M, Eshrati B, Williams HC, Shibuya K, Dandona R, Murthy K, Cowie B, Amare AT, Antonio CA, Castaneda-Orjuela C, van Gool CH, Violante F, Oh IH, Deribe K, Soreide K, Knibbs L, Kereselidze M, Green M, Cardenas R, Roy N, Tillmann T, Li Y, Krueger H, Monasta L, Dey S, Sheikhbahaei S, Hafezi-Nejad N, Kumar GA, Sreeramareddy CT, Dandona L, Wang H, Vollset SE, Mokdad A, Salomon JA, Lozano R, Vos T, Forouzanfar M, Lopez A, Murray C, Naghavi M. The global burden of cancer 2013. JAMA Oncol 2015; 1: 505-527. https://doi.org/10.1001/jamaoncol.2015.0735
  10. Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, Pairojkul C, Bhudhisawasdi V, Tesana S, Thinkamrop B, Bethony JM, Loukas A, Brindley PJ. Liver fluke induces cholangiocarcinoma. PLoS Med 2007; 4: e201. https://doi.org/10.1371/journal.pmed.0040201
  11. 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: 1066-1073. https://doi.org/10.1016/j.jhep.2005.11.040
  12. Shin HR, Oh JK, Lim MK, Shin A, Kong HJ, Jung KW, Won YJ, Park S, Park SJ, Hong ST. Descriptive epidemiology of cholangiocarcinoma and clonorchiasis in Korea. J Korean Med Sci 2010; 25:1011-1016. https://doi.org/10.3346/jkms.2010.25.7.1011
  13. 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: 93-96. https://doi.org/10.4269/ajtmh.2006.75.93
  14. Seo HJ, Kim SY, Lee YJ, Jang BH, Park JE, Sheen SS, Hahn SK. A newly developed tool for classifying study designs in systematic reviews of interventions and exposures showed substantial reliability and validity. J Clin Epidemiol 2016; 70: 200-205. https://doi.org/10.1016/j.jclinepi.2015.09.013
  15. Kulldorff M. A spatial scan statistic. Commun Stat Theory Methods 1997; 26: 1481-1496. https://doi.org/10.1080/03610929708831995
  16. Kulldorff M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med 1995; 14:799-810. https://doi.org/https://doi.org/10.1002/sim.4780140809
  17. Mathes RW, Lall R, Levin-Rector A, Sell J, Paladini M, Konty KJ, Olson D, Weiss D. Evaluating and implementing temporal, spatial, and spatio-temporal methods for outbreak detection in a local syndromic surveillance system. PLoS One 2017; 12: e0184419. https://doi.org/10.1371/journal.pone.0184419
  18. Stelling J, Yih WK, Galas M, Kulldorff M, Pichel M, Terragno R, Tuduri E, Espetxe S, Binsztein N, O'Brien TF, Platt R. Automated use of WHONET and SaTScan to detect outbreaks of Shigella spp. using antimicrobial resistance phenotypes. Epidemiol Infect 2010; 138: 873-883. https://doi.org/10.1017/S0950268809990884
  19. Chen J, Roth RE, Naito AT, Lengerich EJ, MacEachren AM. Geovisual analytics to enhance spatial scan statistic interpretation: an analysis of U.S. cervical cancer mortality. Int J Health Geogr 2008; 7: 57-74. https://doi.org/10.1186/1476-072X-7-57
  20. Wang W, Zhang T, Yin F, Xiao X, Chen S, Zhang X, Li X, Ma Y. Using the maximum clustering heterogeneous set-proportion to select the maximum window size for the spatial scan statistic. Sci Rep 2020; 10: 4900-4913. https://doi.org/10.1038/s41598-020-61829-y
  21. Yoo H, Jung I. Optimizing the maximum reported cluster size for normal-based spatial scan statistics. CSAM 2018; 25: 373-383. https://doi.org/10.29220/CSAM.2018.25.4.373
  22. Azage M, Kumie A, Worku A, Bagtzoglou AC. Childhood diarrhea exhibits spatiotemporal variation in northwest Ethiopia: a SaTScan spatial statistical analysis. PLoS One 2015; 10: e0144690. https://doi.org/10.1371/journal.pone.0144690
  23. Clegg LX, Hankey BF, Tiwari R, Feuer EJ, Edwards BK. Estimating average annual per cent change in trend analysis. Stat Med 2009; 28: 3670-3682. https://doi.org/10.1002/sim.3733
  24. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 2000; 19: 335-351. https://doi.org/10.1002/(SICI)1097-0258(20000215)19:3<335::AID-SIM336>3.0.CO;2-Z
  25. Molnar A, Iancu M, Radu R, Borzan CM. A joinpoint regression analysis of syphilis and gonorrhea incidence in 15-19-year old adolescents between 2005 and 2017: a regional study. Int J Environ Res Public Health 2020; 17: 5385-5396. https://doi.org/10.3390/ijerph17155385
  26. Grech V. WASP (Write a Scientific Paper) using Excel-13: correlation and regression. Early Hum Dev 2018; 122: 60-63. https://doi.org/10.1016/j.earlhumdev.2018.04.009
  27. Lachin JM. Introduction to sample size determination and power analysis for clinical trials. Control Clin Trials 1981; 2: 93-113. https://doi.org/10.1016/0197-2456(81)90001-5
  28. Bujang MA, Baharum N. Sample size guideline for correlation analysis. World J Soc Sci Res 2016; 3: 37-46. https://doi.org/10.22158/wjssr.v3n1p37
  29. Lee MR, Shin HE, Back SO, Lee YJ, Lee HI, Ju JW. Status of helminthic infections in residents around river basins in the Republic of Korea for 10 Years (2011-2020). Korean J Parasitol 2022; 60: 187-193. https://doi.org/10.3347/kjp.2022.60.3.187
  30. Hong ST, Yong TS. Review of successful control of parasitic infections in Korea. Infect Chemother 2020; 52: 427-440. https://doi.org/10.3947/ic.2020.52.3.427
  31. Kim TS, Pak JH, Kim JB, Bahk YY. Clonorchis sinensis, an oriental liver fluke, as a human biological agent of cholangiocarcinoma: a brief review. BMB Rep 2016; 49: 590-597. https://doi.org/10.5483/bmbrep.2016.49.11.109
  32. Yang YM, Choi H, Ryu DH, Woo CG, Han JH, Park SM. Clonorchis sinensis infection presenting as acute cholangitis and acute cholecystitis. Korean J Pancreas Biliary Tract 2019; 24: 79-83. https://doi.org/10.15279/kpba.2019.24.2.79
  33. Phyo Myint EE, Sereemaspun A, Rocklov J, Nithikathkul C. Discovery of carcinogenic liver fluke metacercariae in second intermediate hosts and surveillance on fish-borne trematode metacercariae infections in Mekong region of Myanmar. Int J Environ Res Public Health 2020; 17: 4108-4119. https://doi.org/10.3390/ijerph17114108
  34. Korea National Institute of Health. Korea National Institute of Health: Annual Report 2018. Korea National Institute of Health. Cheongju, Korea.
  35. Cho IR, Yi SW, Choi JS, Yi JJ. Comparison of risk factors for cholangiocarcinoma and hepatocellular carcinoma: a prospective cohort study in Korean adults. Cancers 2022; 14: 1709-1724. https://doi.org/10.3390/cancers14071709
  36. Pfeifer CM, Bourm KS, Brandt MR, Ali K. Liver fluke-induced choledocholithiasis with biliary ductal obstruction. Radiol Case Rep 2019; 14: 1483-1486. https://doi.org/10.1016/j.radcr.2019.09.022
  37. Prueksapanich P, Piyachaturawat P, Aumpansub P, Ridtitid W, Chaiteerakij R, Rerknimitr R. Liver fluke-associated biliary tract cancer. Gut Liver 2018; 12: 236-245. https://doi.org/10.5009/gnl17102
  38. Fedorova OS, Fedotova MM, Zvonareva OI, Mazeina SV, Kovshirina YV, Sokolova TS, Golovach EA, Kovshirina AE, Konovalova UV, Kolomeets IL, Gutor SS, Petrov VA, Hattendorf J, Ogorodova LM, Odermatt P. Opisthorchis felineus infection, risks, and morbidity in rural Western Siberia, Russian Federation. PLoS Negl Trop Dis 2020; 14: e0008421. https://doi.org/10.1371/journal.pntd.0008421
  39. Saiyachak K, Tongsotsang S, Saenrueang T, Moore MA, Promthet S. Prevalence and factors associated with Opisthorchis viverrini infection in Khammouane Province, Lao PDR. Asian Pac J Cancer Prev 2016; 17: 1589-1593. https://doi.org/10.7314/apjcp.2016.17.3.1589
  40. Shen C, Li S, Zheng S, Choi MH, Bae YM, Hong ST. Tissue parasitic helminthiases are prevalent at Cheongjin, North Korea. Korean J Parasitol 2007; 45: 139-144. https://doi.org/10.3347/kjp.2007.45.2.139
  41. Kim JA, Yoon S, Kim LY, Kim DS. Towards actualizing the value potential of Korea Health Insurance Review and Assessment (HIRA) data as a resource for health research: strengths, limitations, applications, and strategies for optimal use of HIRA data. J Korean Med Sci 2017; 32: 718-728. https://doi.org/10.3346/jkms.2017.32.5.718
  42. Booth CM, Cescon DW, Wang L, Tannock IF, Krzyzanowska MK. Evolution of the randomized controlled trial in oncology over three decades. J Clin Oncol 2008; 26: 5458-5464. https://doi.org/10.1200/JCO.2008.16.5456