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The Risk of Colorectal Cancer After Cholecystectomy or Appendectomy: A Population-based Cohort Study in Korea

  • Lee, Joonki (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Choe, Sunho (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Park, Ji Won (Division of Colorectal Surgery, Department of Surgery, Seoul National University College of Medicine) ;
  • Jeong, Seung-Yong (Division of Colorectal Surgery, Department of Surgery, Seoul National University College of Medicine) ;
  • Shin, Aesun (Department of Preventive Medicine, Seoul National University College of Medicine)
  • Received : 2018.05.12
  • Accepted : 2018.10.09
  • Published : 2018.11.30

Abstract

Objectives: We investigated the association between cholecystectomy or appendectomy and the subsequent risk of colorectal cancer (CRC) in the Korean population. Methods: A retrospective cohort study was conducted with the National Health Insurance Service-National Sample Cohort of Korea; this sample was followed up from January 1, 2002, until the date of CRC incidence, loss to follow-up, or December 31, 2015. The exposure status of cholecystectomy and appendectomy was treated as a time-varying covariate. The calculated risk of CRC was stratified by follow-up period, and the association between these surgical procedures and CRC was investigated by a Cox regression model applying appropriate lag periods. Results: A total of 707 663 individuals were identified for analysis. The study population was followed up for an average of 13.66 years, and 4324 CRC cases were identified. The hazard ratio (HR) of CRC was elevated in the first year after cholecystectomy (HR, 1.71; 95% confidence interval [CI], 1.01 to 2.89) and in the first year and 2-3 years after appendectomy (HR, 4.22; 95% CI, 2.87 to 6.20; HR, 2.34; 95% CI, 1.36 to 4.03, respectively). The HRs of CRC after applying 1 year of lag after cholecystectomy and 3 years of lag after appendectomy were 0.80 (95% CI, 0.57 to 1.13) and 0.77 (95% CI, 0.51 to 1.16), respectively. Conclusions: The risk of CRC increased in the first year after cholecystectomy and appendectomy, implying the possibility of bias. When appropriate lag periods after surgery were applied, no association was found between cholecystectomy or appendectomy and CRC.

Keywords

References

  1. Haggar FA, Boushey RP. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg 2009;22(4):191-197. https://doi.org/10.1055/s-0029-1242458
  2. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015;136(5):E359-E386. https://doi.org/10.1002/ijc.29210
  3. Jung KW, Won YJ, Kong HJ, Lee ES; Community of Population-Based Regional Cancer Registries. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2015. Cancer Res Treat 2018;50(2):303-316. https://doi.org/10.4143/crt.2018.143
  4. Macrae FA. Colorectal cancer: epidemiology, risk factors, and protective factors; 2018 Jun 25 [cited 2018 Nov 1]. Available from: https://www.uptodate.com/contents/colorectal-cancer-epidemiology-risk-factors-and-protective-factors.
  5. American Cancer Society. Colorectal cancer risk factors [cited 2018 Nov 1]. Available from: https://www.cancer.org/cancer/colon-rectal-cancer/causes-risks-prevention/risk-factors.html#references.
  6. Hearing SD, Thomas LA, Heaton KW, Hunt L. Effect of cholecystectomy on bowel function: a prospective, controlled study. Gut 1999;45(6):889-894. https://doi.org/10.1136/gut.45.6.889
  7. Schottenfeld D, Fraumeni JF Jr. Cancer epidemiology and prevention. 3rd ed. New York: Oxford University Press; 2006, p. 809-829.
  8. Zuccato E, Venturi M, Di Leo G, Colombo L, Bertolo C, Doldi SB, et al. Role of bile acids and metabolic activity of colonic bacteria in increased risk of colon cancer after cholecystectomy. Dig Dis Sci 1993;38(3):514-519. https://doi.org/10.1007/BF01316508
  9. Nagengast FM, Grubben MJ, van Munster IP. Role of bile acids in colorectal carcinogenesis. Eur J Cancer 1995;31A(7-8):1067-1070.
  10. Pomare EW, Heaton KW. The effect of cholecystectomy on bile salt metabolism. Gut 1973;14(10):753-762. https://doi.org/10.1136/gut.14.10.753
  11. Randal Bollinger R, Barbas AS, Bush EL, Lin SS, Parker W. Biofilms in the large bowel suggest an apparent function of the human vermiform appendix. J Theor Biol 2007;249(4):826-831. https://doi.org/10.1016/j.jtbi.2007.08.032
  12. Schernhammer ES, Leitzmann MF, Michaud DS, Speizer FE, Giovannucci E, Colditz GA, et al. Cholecystectomy and the risk for developing colorectal cancer and distal colorectal adenomas. Br J Cancer 2003;88(1):79-83. https://doi.org/10.1038/sj.bjc.6600661
  13. Shao T, Yang YX. Cholecystectomy and the risk of colorectal cancer. Am J Gastroenterol 2005;100(8):1813-1820. https://doi.org/10.1111/j.1572-0241.2005.41610.x
  14. Chen YK, Yeh JH, Lin CL, Peng CL, Sung FC, Hwang IM, et al. Cancer risk in patients with cholelithiasis and after cholecystectomy: a nationwide cohort study. J Gastroenterol 2014; 49(5):923-931. https://doi.org/10.1007/s00535-013-0846-6
  15. Giovannucci E, Colditz GA, Stampfer MJ. A meta-analysis of cholecystectomy and risk of colorectal cancer. Gastroenterology 1993;105(1):130-141. https://doi.org/10.1016/0016-5085(93)90018-8
  16. Zhang Y, Liu H, Li L, Ai M, Gong Z, He Y, et al. Cholecystectomy can increase the risk of colorectal cancer: a meta-analysis of 10 cohort studies. PLoS One 2017;12(8):e0181852. https://doi.org/10.1371/journal.pone.0181852
  17. Peng YC, Lin CL, Sung FC. The association between cholecystectomy and colorectal neoplasm in inflammatory bowel diseases: a population-based cohort study. PLoS One 2017;12(5):e0177745. https://doi.org/10.1371/journal.pone.0177745
  18. Zhao C, Ge Z, Wang Y, Qian J. Meta-analysis of observational studies on cholecystectomy and the risk of colorectal adenoma. Eur J Gastroenterol Hepatol 2012;24(4):375-381. https://doi.org/10.1097/meg.0b013e328350f86b
  19. Chiong C, Cox MR, Eslick GD. Gallstone disease is associated with rectal cancer: a meta-analysis. Scand J Gastroenterol 2012;47(5):553-564. https://doi.org/10.3109/00365521.2012.660538
  20. Shang J, Reece JC, Buchanan DD, Giles GG, Figueiredo JC, Casey G, et al. Cholecystectomy and the risk of colorectal cancer by tumor mismatch repair deficiency status. Int J Colorectal Dis 2016;31(8):1451-1457. https://doi.org/10.1007/s00384-016-2615-5
  21. Jorgensen T, Rafaelsen S. Gallstones and colorectal cancer--there is a relationship, but it is hardly due to cholecystectomy. Dis Colon Rectum 1992;35(1):24-28. https://doi.org/10.1007/BF02053334
  22. Nogueira L, Freedman ND, Engels EA, Warren JL, Castro F, Koshiol J. Gallstones, cholecystectomy, and risk of digestive system cancers. Am J Epidemiol 2014;179(6):731-739. https://doi.org/10.1093/aje/kwt322
  23. Ergul E, Gozetlik E. Does appendectomy increase the risk of colorectal adenocarcinoma? Open Med 2009;4(3):315-319.
  24. Lai HW, Loong CC, Tai LC, Wu CW, Lui WY. Incidence and odds ratio of appendicitis as first manifestation of colon cancer: a retrospective analysis of 1873 patients. J Gastroenterol Hepatol 2006;21(11):1693-1696. https://doi.org/10.1111/j.1440-1746.2006.04426.x
  25. Wu SC, Chen WT, Muo CH, Ke TW, Fang CW, Sung FC. Association between appendectomy and subsequent colorectal cancer development: an Asian population study. PLoS One 2015; 10(2):e0118411. https://doi.org/10.1371/journal.pone.0118411
  26. Wu SC, Chen WT, Muo CH, Sung FC. Appendicitis as an early manifestation of subsequent malignancy: an asian population study. PLoS One 2015;10(4):e0122725. https://doi.org/10.1371/journal.pone.0122725
  27. Song H, Abnet CC, Andren-Sandberg A, Chaturvedi AK, Ye W. Risk of gastrointestinal cancers among patients with appendectomy: a large-scale Swedish register-based cohort study during 1970-2009. PLoS One 2016;11(3):e0151262. https://doi.org/10.1371/journal.pone.0151262
  28. Tamim H, Monfared AA, LeLorier J. Application of lag-time into exposure definitions to control for protopathic bias. Pharmacoepidemiol Drug Saf 2007;16(3):250-258. https://doi.org/10.1002/pds.1360
  29. Armenian HK. Incubation periods of cancer: old and new. J Chronic Dis 1987;40 Suppl 2:9S-15S. https://doi.org/10.1016/S0021-9681(87)80004-8
  30. Lee J, Lee JS, Park SH, Shin SA, Kim K. Cohort profile: the National Health Insurance Service-National Sample Cohort (NHIS-NSC), South Korea. Int J Epidemiol 2017;46(2):e15. https://doi.org/10.1093/ije/dyv319
  31. Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI, Levin B, et al. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control 2013;24(6):1207-1222. https://doi.org/10.1007/s10552-013-0201-5
  32. Thiebaut AC, Benichou J. Choice of time-scale in Cox's model analysis of epidemiologic cohort data: a simulation study. Stat Med 2004;23(24):3803-3820. https://doi.org/10.1002/sim.2098
  33. Wysocki A, Lejman W, Bobrzynski A. Abdominal malignancies missed during laparoscopic cholecystectomy. Surg Endosc 2001;15(9):959-961. https://doi.org/10.1007/s004640090022
  34. Goldacre MJ, Wotton CJ, Abisgold J, Yeates DG, Collins J. Association between cholecystectomy and intestinal cancer: a national record linkage study. Ann Surg 2012;256(6):1068-1072. https://doi.org/10.1097/SLA.0b013e3182759efb
  35. Gal I, Szivos J, Jaberansari MT, Szabo Z. Laparoscopic cholecystectomy. Risk of missed pathology of other organs. Surg Endosc 1998;12(6):825-827. https://doi.org/10.1007/s004649900722
  36. Wolkewitz M, Allignol A, Harbarth S, de Angelis G, Schumacher M, Beyersmann J. Time-dependent study entries and exposures in cohort studies can easily be sources of different and avoidable types of bias. J Clin Epidemiol 2012;65(11):1171-1180. https://doi.org/10.1016/j.jclinepi.2012.04.008

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