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Helicobacter pylori status and risks of metachronous recurrence after endoscopic resection of early gastric cancer: a systematic review and meta-analysis

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Abstract

The impact of different Helicobacter pylori (H. pylori) status (H. pylori negative, H. pylori eradication and H. pylori persistence) on the development of metachronous gastric lesions after endoscopic resection of early gastric cancer is not well defined. Thus, a systematic review and meta-analysis was performed to investigate this relationship. Two authors independently searched the electronic databases (Pubmed, Embase, the Cochrane Library and Web of Science) through March 2018, without language restriction. Pooled risk ratio for metachronous gastric lesions with regard to H. pylori status was calculated using fixed- or random-effects models, and heterogeneity and publication bias were also measured. 20 eligible studies were finally identified in systematic review, and 17 out of 20 studies were further included in meta-analysis. H. pylori eradication was associated with overall 50% lower odds of metachronous events (RR = 0.50; 95 % CI 0.41–0.61). Pooled risk ratios for metachronous gastric neoplasm were 0.85 (95 % CI 0.43–1.68) between H. pylori-eradicated and -negative patients, and 0.63 (95 % CI 0.35–1.12) between H. pylori-negative and -persistent patients, respectively. In conclusion, based on the best available evidence, eradication of H. pylori can provide protection against secondary gastric neoplasm, and this quantitative benefit seemed greater than among asymptomatic individuals. Metachronous risk seems comparable between H. pylori-eradicated and -negative population, or between H. pylori-negative and -persistent patients.

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References

  1. Fukunaga S, Nagami Y, Shiba M, et al. Long-term prognosis of expanded-indication differentiated-type early gastric cancer treated with endoscopic submucosal dissection or surgery using propensity score analysis. Gastrointest Endosc. 2017;85:143–52.

    Article  PubMed  Google Scholar 

  2. Choi KS, Jung HY, Choi KD, et al. EMR versus gastrectomy for intramucosal gastric cancer: comparison of long-term outcomes. Gastrointest Endosc. 2011;73:942–8.

    Article  PubMed  Google Scholar 

  3. Abe S, Oda I, Minagawa T, et al. Metachronous gastric cancer following curative endoscopic resection of early gastric cancer. Clin Endosc. 2018;51:253–9.

    Article  PubMed  Google Scholar 

  4. Yoon H, Kim N, Shin CM, et al. Risk factors for metachronous gastric neoplasms in patients who underwent endoscopic resection of a gastric neoplasm. Gut Liver. 2016;10:228–36.

    Article  PubMed  CAS  Google Scholar 

  5. Kim H, Shin J, Bang B, et al. Risk factor of metachronous recurrence after endoscopic submucosal dissection for gastric epithelial neoplasm. Helicobacter. 2017;22:70–1.

    Google Scholar 

  6. Moon HS, Yun GY, Kim JS, et al. Risk factors for metachronous gastric carcinoma development after endoscopic resection of gastric dysplasia: retrospective, single-center study. World J Gastroenterol. 2017;23:4407–15.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Amieva M, Peek RM Jr. Pathobiology of Helicobacter pylori-Induced gastric cancer. Gastroenterology. 2016;150:64–78.

    Article  PubMed  CAS  Google Scholar 

  8. Uemura N, Mukai T, Okamoto S, et al. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomarkers Prev. 1997;6:639–42.

    PubMed  CAS  Google Scholar 

  9. Fukase K, Kato M, Kikuchi S, et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008;372:392–7.

    Article  PubMed  Google Scholar 

  10. Choi J, Kim S, Yoon H, et al. Eradication of Helicobacter pylori after endoscopic resection of gastric tumors does not reduce incidence of metachronous gastric carcinoma. Clin Gastroenterol Hepatol. 2014;12:793–800.

    Article  PubMed  Google Scholar 

  11. Choi IJ, Kook MC, Kim YI, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med. 2018;378:1085–95.

    Article  PubMed  CAS  Google Scholar 

  12. Shiotani A, Uedo N, Iishi H, et al. Predictive factors for metachronous gastric cancer in high-risk patients after successful Helicobacter pylori eradication. Digestion. 2008;78:113–9.

    Article  PubMed  Google Scholar 

  13. Maehata Y, Nakamura S, Fujisawa K, et al. Long-term effect of Helicobacter pylori eradication on the development of metachronous gastric cancer after endoscopic resection of early gastric cancer. Gastrointest Endosc. 2012;75:39–46.

    Article  PubMed  Google Scholar 

  14. Kim SB, Lee SH, Bae SI, et al. Association between Helicobacter pylori status and metachronous gastric cancer after endoscopic resection. World J Gastroenterol. 2016;22:9794–802.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Ami R, Hatta W, Iijima K, et al. Factors associated with metachronous gastric cancer development after endoscopic submucosal dissection for early gastric cancer. J Clin Gastroenterol. 2017;51:494–9.

    Article  PubMed  Google Scholar 

  16. Schlemper RJ, Riddell RH, Kato Y, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47:251–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Juni P, Altman DG, Egger M. Systematic reviews in health care: assessing the quality of controlled clinical trials. BMJ. 2001;323:42–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Kim SY, Park JE, Lee YJ, et al. Testing a tool for assessing the risk of bias for nonrandomized studies showed moderate reliability and promising validity. J Clin Epidemiol. 2013;66:408–14.

    Article  PubMed  Google Scholar 

  19. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.

    Article  PubMed  Google Scholar 

  22. Nakagawa S, Asaka M, Kato M, et al. Helicobacter pylori eradication and metachronous gastric cancer after endoscopic mucosal resection of early gastric cancer. Aliment Pharmacol Ther. 2006;24:214–8.

    Article  Google Scholar 

  23. Han JS, Jang JS, Choi SR, et al. A study of metachronous cancer after endoscopic resection of early gastric cancer. Scand J Gastroenterol. 2011;46:1099–104.

    Article  PubMed  Google Scholar 

  24. Kim HJ, Hong SJ, Ko BM, et al. Helicobacter pylori eradication suppresses metachronous gastric cancer and cyclooxygenase-2 expression after endoscopic resection of early gastric cancer. Korean J Helicobacter Up Gastrointest Res. 2011;11:117–23.

    Article  Google Scholar 

  25. Bae SE, Jung HY, Kang J, et al. Effect of Helicobacter pylori eradication on metachronous recurrence after endoscopic resection of gastric neoplasm. Am J Gastroenterol. 2014;109:60–7.

    Article  PubMed  Google Scholar 

  26. Kim YI, Choi IJ, Kook MC, et al. The association between Helicobacter pylori status and incidence of metachronous gastric cancer after endoscopic resection of early gastric cancer. Helicobacter. 2014;19:194–201.

    Article  PubMed  Google Scholar 

  27. Kwon YH, Heo J, Lee HS, et al. Failure of Helicobacter pylori eradication and age are independent risk factors for recurrent neoplasia after endoscopic resection of early gastric cancer in 283 patients. Aliment Pharmacol Ther. 2014;39:609–18.

    Article  PubMed  CAS  Google Scholar 

  28. Jung S, Park CH, Kim EH, et al. Preventing metachronous gastric lesions after endoscopic submucosal dissection through Helicobacter pylori eradication. J Gastroenterol Hepatol. 2015;30:75–81.

    Article  PubMed  Google Scholar 

  29. Chung C-S, Woo HS, Chung J-W, et al. Risk factors for metachronous recurrence after endoscopic submucosal dissection of early gastric cancer. J Korean Med Sci. 2017;32:421–6.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Han SJ, Kim SG, Lim JH, et al. Long-term effects of Helicobacter pylori eradication on metachronous gastric cancer development. Gut Liver. 2018;12:133–41.

    Article  PubMed  CAS  Google Scholar 

  31. Kwon Y, Jeon S, Nam S, et al. Helicobacter pylori infection and serum level of pepsinogen are associated with the risk of metachronous gastric neoplasm after endoscopic resection. Aliment Pharmacol Ther. 2017;46:758–67.

    Article  PubMed  CAS  Google Scholar 

  32. Seo JY, Lee DH, Cho Y, et al. Eradication of Helicobacter pylori reduces metachronous gastric cancer after endoscopic resection of early gastric cancer. Hepatogastroenterology. 2013;60:776–80.

    PubMed  Google Scholar 

  33. Jeong YH, Lee SH, Sohn SH, et al. The effect of Helicobacter pylori eradication on metachronous gastric cancer after endoscopic submucosal resection. United Euro Gastroenterol J. 2015;3:A122.

    Google Scholar 

  34. Yoon SB, Park JM, Lim CH, et al. Effect of Helicobacter pylori eradication on metachronous gastric cancer after endoscopic resection of gastric tumors: a meta-analysis. Helicobacter. 2014;19:243–8.

    Article  PubMed  Google Scholar 

  35. Bang CS, Baik GH, Shin IS, et al. Helicobacter pylori eradication for prevention of metachronous recurrence after endoscopic resection of early gastric cancer. J Korean Med Sci. 2015;30:749–56.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Lee YC, Chiang TH, Chou CK, et al. Association between Helicobacter pylori eradication and gastric cancer incidence: a systematic review and meta-analysis. Gastroenterology. 2016;150:1113–24.

    Article  PubMed  Google Scholar 

  37. Fuccio L, Zagari RM, Eusebi LH, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Ann Intern Med. 2009;151:121–8.

    Article  PubMed  Google Scholar 

  38. Ford AC, Forman D, Hunt RH, et al. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomised controlled trials. BMJ. 2014;348:g3174.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Li X. Effect of Helicobacter pylori eradication timing on metachronous recurrence after endoscopic submucosal dissection of early gastric cancer. J Dig Dis. 2017;18:122–3.

    Article  CAS  Google Scholar 

  40. Huh CW, Youn YH, Jung DH, et al. Early attempts to eradicate Helicobacter pylori after endoscopic resection of gastric neoplasm significantly improve eradication success rates. PLoS One. 2016;11:e0162258.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Yang HJ, Kim SG, Lim JH, et al. Surveillance strategy according to age after endoscopic resection of early gastric cancer. Surg Endosc. 2018;32:846–54.

    Article  PubMed  Google Scholar 

  42. Gisbert JP, Pajares JM. Review article: 13C-urea breath test in the diagnosis of Helicobacter pylori infection—a critical review. Aliment Pharmacol Ther. 2004;20:1001–17.

    Article  PubMed  CAS  Google Scholar 

  43. Kwon YH, Kim N, Lee JY, et al. The diagnostic validity of citric acid-free, high dose (13)C-urea breath test after Helicobacter pylori eradication in Korea. Helicobacter. 2015;20:159–68.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This article was supported by the National Natural Science Foundation of China (81672410).

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Authors and Affiliations

  1. Department of Gastroenterology, Peking University Third Hospital, 49 North Garden Road, Haidian District, Beijing, 100191, China

    Shiyu Xiao, Sizhu Li, Liya Zhou, Wenjun Jiang & Jinzhe Liu

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  1. Shiyu Xiao
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  2. Sizhu Li
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Correspondence to Liya Zhou.

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Xiao, S., Li, S., Zhou, L. et al. Helicobacter pylori status and risks of metachronous recurrence after endoscopic resection of early gastric cancer: a systematic review and meta-analysis. J Gastroenterol 54, 226–237 (2019). https://doi.org/10.1007/s00535-018-1513-8

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