Journal of Preventive Medicine and Public Health

The Korean Society for Preventive Medicine (대한예방의학회)
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Helicobacter pylori Infection and Risk of Gastric Cancer in Korea: A Quantitative Systematic Review

  • Bae, Jong-Myon (Department of Preventive Medicine, Jeju National University School of Medicine) ;
  • Kim, Eun Hee (Department of Preventive Medicine, Jeju National University School of Medicine)
  • Received : 2016.02.26
  • Accepted : 2016.07.07
  • Published : 2016.07.31
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Abstract

Objectives: In the context of the global decrease in mortality due to gastric cancer, previous studies have reported that the effect of chronic Helicobacter pylori (H. pylori) infection on the incidence of gastric cancer varies among regions. This systematic review was conducted to investigate H. pylori as a risk factor for gastric cancer in Korea, where the incidence of gastric cancer is among the highest in the world. Methods: A search strategy was established to identify articles published in Korean as well as in English. Ultimately, we included observational studies conducted among Korean patients that designed with an age-matched and sex-matched control group that reported the odds ratio associated with H. pylori. Gastric cancer cases were subdivided into overall (OGC), cardia (CGC), non-cardia (NGC), early (EGC), advanced, intestinal (IGC), and diffuse forms of gastric cancer. Summary odds ratios (SORs) with 95% confidence intervals (CIs) were calculated in the meta-analysis using a random-effect model. Results: Eleven case-control studies were ultimately selected. H. pylori was associated with an SOR of 1.81 (95% CI, 1.29 to 2.54) for OGC. Additionally, statistically significant risks were observed for CGC, NGC, EGC, and IGC. Conclusions: Chronic H. pylori infection was found to raise the risk of gastric cancer among Koreans, with the highest risk observed for CGC and EGC (SOR=2.88 for both). Follow-up clinical epidemiologic studies are needed to assess the effects of current treatments aimed at eradicating H. pylori infections.

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References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61(2):69-90. https://doi.org/10.3322/caac.20107
  2. Crew KD, Neugut AI. Epidemiology of gastric cancer. World J Gastroenterol 2006;12(3):354-362. https://doi.org/10.3748/wjg.v12.i3.354
  3. Howson CP, Hiyama T, Wynder EL. The decline in gastric cancer: epidemiology of an unplanned triumph. Epidemiol Rev 1986;8:1-27. https://doi.org/10.1093/oxfordjournals.epirev.a036288
  4. Bertuccio P, Chatenoud L, Levi F, Praud D, Ferlay J, Negri E, et al. Recent patterns in gastric cancer: a global overview. Int J Cancer 2009;125(3):666-673. https://doi.org/10.1002/ijc.24290
  5. Blaser MJ. Helicobacter pylori and gastric diseases. BMJ 1998;316(7143):1507-1510. https://doi.org/10.1136/bmj.316.7143.1507
  6. Konturek PC, Konturek SJ, Brzozowski T. Gastric cancer and Helicobacter pylori infection. J Physiol Pharmacol 2006;57 Suppl 3:51-65.
  7. Correa P. Gastric cancer: two epidemics? Dig Dis Sci 2011;56 (5):1585-1586. https://doi.org/10.1007/s10620-011-1642-x
  8. Song M, Kang D, Yang JJ, Choi JY, Sung H, Lee Y, et al. Age and sex interactions in gastric cancer incidence and mortality trends in Korea. Gastric Cancer 2015;18(3):580-589. https://doi.org/10.1007/s10120-014-0411-x
  9. Kim JI, Kim SG, Kim N, Kim JG, Shin SJ, Kim SW, et al. Changing prevalence of upper gastrointestinal disease in 28 893 Koreans from 1995 to 2005. Eur J Gastroenterol Hepatol 2009;21 (7):787-793. https://doi.org/10.1097/MEG.0b013e32830e285a
  10. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984;1(8390):1311-1315.
  11. Wroblewski LE, Peek RM Jr. Helicobacter pylori in gastric carcinogenesis: mechanisms. Gastroenterol Clin North Am 2013;42 (2):285-298. https://doi.org/10.1016/j.gtc.2013.01.006
  12. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006;118(12):3030-3044. https://doi.org/10.1002/ijc.21731
  13. Herrera V, Parsonnet J. Helicobacter pylori and gastric adenocarcinoma. Clin Microbiol Infect 2009;15(11):971-976. https://doi.org/10.1111/j.1469-0691.2009.03031.x
  14. EUROGAST Study Group. An international association between Helicobacter pylori infection and gastric cancer. Lancet 1993;341(8857):1359-1363. https://doi.org/10.1016/0140-6736(93)90938-D
  15. Helicobacter and Cancer Collaborative Group. Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 2001;49 (3):347-353. https://doi.org/10.1136/gut.49.3.347
  16. Cavaleiro-Pinto M, Peleteiro B, Lunet N, Barros H. Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis. Cancer Causes Control 2011;22(3):375-387. https://doi.org/10.1007/s10552-010-9707-2
  17. Kim HY, Cho BD, Chang WK, Kim DJ, Kim YB, Park CK, et al. Helicobacter pylori infection and the risk of gastric cancer among the Korean population. J Gastroenterol Hepatol 1997; 12(2):100-103. https://doi.org/10.1111/j.1440-1746.1997.tb00391.x
  18. Lee BM, Jang JJ, Kim JS, You YC, Chun SA, Kim HS, et al. Association of Helicobacter pylori infection with gastric adenocarcinoma. Jpn J Cancer Res 1998;89(6):597-603. https://doi.org/10.1111/j.1349-7006.1998.tb03260.x
  19. Shin A, Shin HR, Kang D, Park SK, Kim CS, Yoo KY. A nested case-control study of the association of Helicobacter pylori infection with gastric adenocarcinoma in Korea. Br J Cancer 2005;92(7):1273-1275. https://doi.org/10.1038/sj.bjc.6602467
  20. Bae JM, Lee EJ, Guyatt G. Citrus fruit intake and stomach cancer risk: a quantitative systematic review. Gastric Cancer 2008; 11(1):23-32. https://doi.org/10.1007/s10120-007-0447-2
  21. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21(11):1539-1558. https://doi.org/10.1002/sim.1186
  22. Harbord RM, Egger M, Sterne JA. A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 2006;25(20):3443-3457. https://doi.org/10.1002/sim.2380
  23. Gwack J, Shin A, Kim CS, Ko KP, Kim Y, Jun JK, et al. CagA-producing Helicobacter pylori and increased risk of gastric cancer: a nested case-control study in Korea. Br J Cancer 2006;95 (5):639-641 https://doi.org/10.1038/sj.bjc.6603309
  24. Ko KP, Park SK, Park B, Yang JJ, Cho LY, Kang C, et al. Isoflavones from phytoestrogens and gastric cancer risk: a nested case-control study within the Korean Multicenter Cancer Cohort. Cancer Epidemiol Biomarkers Prev 2010;19(5):1292-1300. https://doi.org/10.1158/1055-9965.EPI-09-1004
  25. Yang JJ, Yang JH, Kim J, Ma SH, Cho LY, Ko KP, et al. Soluble c-Met protein as a susceptible biomarker for gastric cancer risk: a nested case-control study within the Korean Multicenter Cancer Cohort. Int J Cancer 2013;132(9):2148-2156. https://doi.org/10.1002/ijc.27861
  26. Yang JJ, Ko KP, Cho LY, Shin A, Gwack J, Chang SH, et al. The role of TNF genetic variants and the interaction with cigarette smoking for gastric cancer risk: a nested case-control study. BMC Cancer 2009;9:238. https://doi.org/10.1186/1471-2407-9-238
  27. Ko KP, Park SK, Cho LY, Gwack J, Yang JJ, Shin A, et al. Soybean product intake modifies the association between interleukin-10 genetic polymorphisms and gastric cancer risk. J Nutr 2009;139(5):1008-1012. https://doi.org/10.3945/jn.108.101865
  28. Kim Y, Shin A, Gwack J, Ko KP, Kim CS, Park SK, et al. Epstein-Barr virus antibody level and gastric cancer risk in Korea: a nested case-control study. Br J Cancer 2009;101(3):526-529. https://doi.org/10.1038/sj.bjc.6605146
  29. Kim JY, Lee HS, Kim N, Shin CM, Lee SH, Park YS, et al. Prevalence and clinicopathologic characteristics of gastric cardia cancer in South Korea. Helicobacter 2012;17(5):358-368. https://doi.org/10.1111/j.1523-5378.2012.00958.x
  30. Shin CM, Kim N, Cho SI, Kim JS, Jung HC, Song IS. Association between alcohol intake and risk for gastric cancer with regard to ALDH2 genotype in the Korean population. Int J Epidemiol 2011;40(4):1047-1055. https://doi.org/10.1093/ije/dyr067
  31. Kim N, Park YS, Cho SI, Lee HS, Choe G, Kim IW, et al. Prevalence and risk factors of atrophic gastritis and intestinal metaplasia in a Korean population without significant gastroduodenal disease. Helicobacter 2008;13(4):245-255. https://doi.org/10.1111/j.1523-5378.2008.00604.x
  32. Kang KP, Lee HS, Kim N, Kang HM, Park YS, Lee DH, et al. Role of intestinal metaplasia subtyping in the risk of gastric cancer in Korea. J Gastroenterol Hepatol 2009;24(1):140-148. https://doi.org/10.1111/j.1440-1746.2008.05546.x
  33. Hwang JJ, Lee DH, Lee AR, Yoon H, Shin CM, Park YS, et al. Characteristics of gastric cancer in peptic ulcer patients with Helicobacter pylori infection. World J Gastroenterol 2015;21 (16):4954-4960. https://doi.org/10.3748/wjg.v21.i16.4954
  34. Kim HJ, Kim N, Kim HY, Lee HS, Yoon H, Shin CM, et al. Relationship between body mass index and the risk of early gastric cancer and dysplasia regardless of Helicobacter pylori infection. Gastric Cancer 2015;18(4):762-773. https://doi.org/10.1007/s10120-014-0429-0
  35. Shin CM, Kim N, Yang HJ, Cho SI, Lee HS, Kim JS, et al. Stomach cancer risk in gastric cancer relatives: interaction between Helicobacter pylori infection and family history of gastric cancer for the risk of stomach cancer. J Clin Gastroenterol 2010;44(2): e34-e39. https://doi.org/10.1097/MCG.0b013e3181a159c4
  36. Cho SJ, Choi IJ, Kim CG, Lee JY, Kook MC, Seong MW, et al. Helicobacter pylori seropositivity is associated with gastric cancer regardless of tumor subtype in Korea. Gut Liver 2010;4 (4):466-474. https://doi.org/10.5009/gnl.2010.4.4.466
  37. Cho SJ, Choi IJ, Kim CG, Kook MC, Lee JY, Kim BC, et al. Risk factors associated with gastric cancer in patients with a duodenal ulcer. Helicobacter 2010;15(6):516-523. https://doi.org/10.1111/j.1523-5378.2010.00805.x
  38. Nam JH, Choi IJ, Cho SJ, Kim CG, Lee JY, Nam SY, et al. Helicobacter pylori infection and histological changes in siblings of young gastric cancer patients. J Gastroenterol Hepatol 2011; 26(7):1157-1163. https://doi.org/10.1111/j.1440-1746.2011.06717.x
  39. Chang WK, Kim HY, Kim DJ, Lee J, Park CK, Yoo JY, et al. Association between Helicobacter pylori infection and the risk of gastric cancer in the Korean population: prospective case-controlled study. J Gastroenterol 2001;36(12):816-822. https://doi.org/10.1007/s005350170003
  40. Kim HJ, Lee SS, Choi BY, Kim MK. Nitrate intake relative to antioxidant vitamin intake affects gastric cancer risk: a case-control study in Korea. Nutr Cancer 2007;59(2):185-191. https://doi.org/10.1080/01635580701460554
  41. Kim HJ, Kim MK, Chang WK, Choi HS, Choi BY, Lee SS. Effect of nutrient intake and Helicobacter pylori infection on gastric cancer in Korea: a case-control study. Nutr Cancer 2005;52(2): 138-146. https://doi.org/10.1207/s15327914nc5202_4
  42. Kim YS, Park HA, Kim BS, Yook JH, Lee MS. Efficacy of screening for gastric cancer in a Korean adult population: a case-control study. J Korean Med Sci 2000;15(5):510-515. https://doi.org/10.3346/jkms.2000.15.5.510
  43. Lee SA, Kang D, Shim KN, Choe JW, Hong WS, Choi H. Effect of diet and Helicobacter pylori infection to the risk of early gastric cancer. J Epidemiol 2003;13(3):162-168. https://doi.org/10.2188/jea.13.162
  44. Kim DS, Lee MS, Kim YS, Kim DH, Bae JM, Shin MH, et al. Effect modification by vitamin C on the relation between gastric cancer and Helicobacter pylori. Eur J Epidemiol 2005;20(1):67-71. https://doi.org/10.1007/s10654-004-1027-y
  45. Chung SJ, Park MJ, Kang SJ, Kang HY, Chung GE, Kim SG, et al. Effect of annual endoscopic screening on clinicopathologic characteristics and treatment modality of gastric cancer in a high-incidence region of Korea. Int J Cancer 2012;131(10): 2376-2384. https://doi.org/10.1002/ijc.27501
  46. Gong EJ, Ahn JY, Jung HY, Lim H, Choi KS, Lee JH, et al. Risk factors and clinical outcomes of gastric cancer identified by screening endoscopy: a case-control study. J Gastroenterol Hepatol 2014;29(2):301-309. https://doi.org/10.1111/jgh.12387
  47. Woo HD, Lee J, Choi IJ, Kim CG, Lee JY, Kwon O, et al. Dietary flavonoids and gastric cancer risk in a Korean population. Nutrients 2014;6(11):4961-4973. https://doi.org/10.3390/nu6114961
  48. Brenner H, Arndt V, Stegmaier C, Ziegler H, Rothenbacher D. Is Helicobacter pylori infection a necessary condition for noncardia gastric cancer? Am J Epidemiol 2004;159(3):252-258. https://doi.org/10.1093/aje/kwh039
  49. Hansen S, Vollset SE, Derakhshan MH, Fyfe V, Melby KK, Aase S, et al. Two distinct aetiologies of cardia cancer; evidence from premorbid serological markers of gastric atrophy and Helicobacter pylori status. Gut 2007;56(7):918-925. https://doi.org/10.1136/gut.2006.114504
  50. Sim YK, Kim CY, Jeong YJ, Kim JH, Hwang Y, Yang DH. Changes of the clinicopathological characteristics and survival rates of gastric cancer with gastrectomy: 1990s vs early 2000s. J Korean Gastric Cancer Assoc 2009;9(4):200-206 (Korean). https://doi.org/10.5230/jkgca.2009.9.4.200
  51. Kang KJ, Lee JH. Characteristics of gastric cancer in Korea: with an emphasis on the increase of the early gastric cancer (EGC). J Korean Med Assoc 2010;53(4):283-289 (Korean). https://doi.org/10.5124/jkma.2010.53.4.283
  52. Correa P. Helicobacter pylori and gastric cancer: state of the art. Cancer Epidemiol Biomarkers Prev 1996;5(6):477-481.
  53. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23(4):713-739. https://doi.org/10.1128/CMR.00011-10
  54. Lunet N, Azevedo A. On the comparability of population-based and hospital-based case-control studies. Gac Sanit 2009;23(6):564. https://doi.org/10.1016/j.gaceta.2009.02.014
  55. Peleteiro B, Lunet N, Barros R, La Vecchia C, Barros H. Factors contributing to the underestimation of Helicobacter pylori-associated gastric cancer risk in a high-prevalence population. Cancer Causes Control 2010;21(8):1257-1264. https://doi.org/10.1007/s10552-010-9553-2
  56. Bae JM, Kim EH. Hormone replacement therapy and risk of breast cancer in Korean women: a quantitative systematic review. J Prev Med Public Health 2015;48(5):225-230. https://doi.org/10.3961/jpmph.15.046
  57. Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH. Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 2003;125(6):1636-1644. https://doi.org/10.1053/j.gastro.2003.08.033
  58. Lee S, Park JM, Park SH, Kim EH, Hahm KB. The Korean perspective of Helicobacter pylori infection: lessons from Japan policy to prevent gastric cancer. J Cancer Prev 2013;18(2):107-112. https://doi.org/10.15430/JCP.2013.18.2.107

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