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Published in: Gastric Cancer 6/2020

01-11-2020 | Helicobacter Pylori | Original Article

Effect of Helicobacter pylori eradication after subtotal gastrectomy on the survival rate of patients with gastric cancer: follow-up for up to 15 years

Authors: Yonghoon Choi, Nayoung Kim, Chang Yong Yun, Yoon Jin Choi, Hyuk Yoon, Cheol Min Shin, Young Soo Park, Sang-Hoon Ahn, Do Joong Park, Hye Seung Lee, Ji-Won Kim, Jin Won Kim, Keun-Wook Lee, Won Chang, Ji Hoon Park, Yoon Jin Lee, Kyoung Ho Lee, Young Hoon Kim, Dong Ho Lee, Hyung-Ho Kim

Published in: Gastric Cancer | Issue 6/2020

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Abstract

Objective

Helicobacter pylori (HP) is known to play an important role in the development of gastric cancer (GC). The aim of this study was to analyze the effect of HP eradication on the survival rate and cancer recurrence in patients who underwent subtotal gastrectomy for GC.

Design

Totally 1,031 patients diagnosed with gastric adenocarcinoma who received surgical treatment at the Seoul National University Bundang Hospital from 2003 to 2017 and positive for HP infection were analyzed. The overall and GC-related survival according to HP eradication were compared; risk factors for GC-specific death and cancer recurrence were analyzed, and propensity score matching (PSM) was performed.

Results

Statistically significant benefits of overall and GC-specific survival were observed in the eradicated group compared to the non-eradicated group (P < 0.001), and these benefits were maintained after PSM (P < 0.001) in both of early and advance stage. In Cox proportional hazards multivariate analyses, cancer stage (stage II, adjusted hazard ratio [aHR] = 9.33, P < 0.001; stage III or IV, aHR = 26.17, P < 0.001), and HP positivity (aHR = 3.41, P = 0.001) were independent risk factors for GC-specific death; cancer stage (cancer stage II, aHR = 7.08, P < 0.001; cancer stage III or IV, aHR = 19.64, P < 0.001) and HP positivity (aHR = 2.70; P = 0.005) were independent risk factors for cancer recurrence.

Conclusion

Our results suggest that HP needed to be conducted more intensively in patients who are surgically treated for GC, regardless of cancer stage.
Appendix
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Literature
1.
go back to reference Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991;325:1127–31.PubMedCrossRef Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991;325:1127–31.PubMedCrossRef
3.
go back to reference Meimarakis G, Winter H, Assmann I, Kopp R, Lehn N, Kist M, et al. Helicobacter pylori as a prognostic indicator after curative resection of gastric carcinoma: a prospective study. Lancet Oncol. 2006;7:211–22.PubMedCrossRef Meimarakis G, Winter H, Assmann I, Kopp R, Lehn N, Kist M, et al. Helicobacter pylori as a prognostic indicator after curative resection of gastric carcinoma: a prospective study. Lancet Oncol. 2006;7:211–22.PubMedCrossRef
4.
go back to reference Marrelli D, Pedrazzani C, Berardi A, Corso G, Neri A, Garosi L, et al. Negative Helicobacter pylori status is associated with poor prognosis in patients with gastric cancer. Cancer. 2009;115:2071–80.PubMedCrossRef Marrelli D, Pedrazzani C, Berardi A, Corso G, Neri A, Garosi L, et al. Negative Helicobacter pylori status is associated with poor prognosis in patients with gastric cancer. Cancer. 2009;115:2071–80.PubMedCrossRef
5.
go back to reference Kang SY, Han JH, Ahn MS, Lee HW, Jeong SH, Park JS, et al. Helicobacter pylori infection as an independent prognostic factor for locally advanced gastric cancer patients treated with adjuvant chemotherapy after curative resection. Int J Cancer. 2012;130:948–58.PubMedCrossRef Kang SY, Han JH, Ahn MS, Lee HW, Jeong SH, Park JS, et al. Helicobacter pylori infection as an independent prognostic factor for locally advanced gastric cancer patients treated with adjuvant chemotherapy after curative resection. Int J Cancer. 2012;130:948–58.PubMedCrossRef
6.
go back to reference Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto 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.PubMedCrossRef Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto 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.PubMedCrossRef
7.
go back to reference Choi IJ, Kook MC, Kim YI, Cho SJ, Lee JY, Kim CG, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med. 2018;378:1085–95.PubMedCrossRef Choi IJ, Kook MC, Kim YI, Cho SJ, Lee JY, Kim CG, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med. 2018;378:1085–95.PubMedCrossRef
8.
9.
go back to reference Shao L, Li P, Ye J, Chen J, Han Y, Cai J, et al. Risk of gastric cancer among patients with gastric intestinal metaplasia. Int J Cancer. 2018;143:1671–7.PubMedCrossRef Shao L, Li P, Ye J, Chen J, Han Y, Cai J, et al. Risk of gastric cancer among patients with gastric intestinal metaplasia. Int J Cancer. 2018;143:1671–7.PubMedCrossRef
10.
go back to reference Cho SJ, Choi IJ, Kook MC, Yoon H, Park S, Kim CG, et al. Randomised clinical trial: the effects of Helicobacter pylori eradication on glandular atrophy and intestinal metaplasia after subtotal gastrectomy for gastric cancer. Aliment Pharmacol Ther. 2013;38:477–89.PubMedCrossRef Cho SJ, Choi IJ, Kook MC, Yoon H, Park S, Kim CG, et al. Randomised clinical trial: the effects of Helicobacter pylori eradication on glandular atrophy and intestinal metaplasia after subtotal gastrectomy for gastric cancer. Aliment Pharmacol Ther. 2013;38:477–89.PubMedCrossRef
11.
go back to reference Hwang JJ, Lee DH, Kang KK, Lee AR, Yoon H, Shin CM, et al. Eradication rate and histological changes after Helicobacter pylori eradication treatment in gastric cancer patients following subtotal gastrectomy. World J Gastroenterol. 2015;21:3936–43.PubMedPubMedCentralCrossRef Hwang JJ, Lee DH, Kang KK, Lee AR, Yoon H, Shin CM, et al. Eradication rate and histological changes after Helicobacter pylori eradication treatment in gastric cancer patients following subtotal gastrectomy. World J Gastroenterol. 2015;21:3936–43.PubMedPubMedCentralCrossRef
12.
go back to reference Yoo S, Lee KH, Lee HJ, Ha K, Lim C, Chin HJ, et al. Seoul national university bundang hospital's electronic system for total care. Healthc Inform Res. 2012;18:145–52.PubMedPubMedCentralCrossRef Yoo S, Lee KH, Lee HJ, Ha K, Lim C, Chin HJ, et al. Seoul national university bundang hospital's electronic system for total care. Healthc Inform Res. 2012;18:145–52.PubMedPubMedCentralCrossRef
13.
go back to reference Bae S, Kim N, Kang JM, Kim DS, Kim KM, Cho YK, et al. Incidence and 30-day mortality of peptic ulcer bleeding in Korea. Eur J Gastroenterol Hepatol. 2012;24:675–82.PubMedCrossRef Bae S, Kim N, Kang JM, Kim DS, Kim KM, Cho YK, et al. Incidence and 30-day mortality of peptic ulcer bleeding in Korea. Eur J Gastroenterol Hepatol. 2012;24:675–82.PubMedCrossRef
14.
go back to reference Bae S, Shim KN, Kim N, Kang JM, Kim DS, Kim KM, et al. Incidence and short-term mortality from perforated peptic ulcer in Korea: a population-based study. J Epidemiol. 2012;22:508–16.PubMedPubMedCentralCrossRef Bae S, Shim KN, Kim N, Kang JM, Kim DS, Kim KM, et al. Incidence and short-term mortality from perforated peptic ulcer in Korea: a population-based study. J Epidemiol. 2012;22:508–16.PubMedPubMedCentralCrossRef
15.
go back to reference Hwang YJ, Kim N, Yun CY, Yoon H, Shin CM, Park YS, et al. Validation of administrative big database for colorectal cancer searched by international classification of disease 10th codes in Korean: a retrospective big-cohort Study. J Cancer Prev. 2018;23:183–90.PubMedPubMedCentralCrossRef Hwang YJ, Kim N, Yun CY, Yoon H, Shin CM, Park YS, et al. Validation of administrative big database for colorectal cancer searched by international classification of disease 10th codes in Korean: a retrospective big-cohort Study. J Cancer Prev. 2018;23:183–90.PubMedPubMedCentralCrossRef
16.
go back to reference Hwang YJ, Park SM, Ahn S, Lee JC, Park YS, Kim N. Accuracy of an administrative database for pancreatic cancer by international classification of disease 10th codes: a retrospective large-cohort study. World J Gastroenterol. 2019;25:5619–29.PubMedPubMedCentralCrossRef Hwang YJ, Park SM, Ahn S, Lee JC, Park YS, Kim N. Accuracy of an administrative database for pancreatic cancer by international classification of disease 10th codes: a retrospective large-cohort study. World J Gastroenterol. 2019;25:5619–29.PubMedPubMedCentralCrossRef
18.
go back to reference Yun CY, Kim N, Lee J, Lee JY, Hwang YJ, Lee HS, et al. Usefulness of OLGA and OLGIM system not only for intestinal type but also for diffuse type of gastric cancer, and no interaction among the gastric cancer risk factors. Helicobacter. 2018;23:e12542.PubMedCrossRef Yun CY, Kim N, Lee J, Lee JY, Hwang YJ, Lee HS, et al. Usefulness of OLGA and OLGIM system not only for intestinal type but also for diffuse type of gastric cancer, and no interaction among the gastric cancer risk factors. Helicobacter. 2018;23:e12542.PubMedCrossRef
20.
go back to reference Yoon K, Kim N, Kim J, Lee JW, Lee HS, Lee JC, et al. Dynamic changes in Helicobacter pylori status following gastric cancer surgery. Gut Liver. 2017;11:209–15.PubMedCrossRef Yoon K, Kim N, Kim J, Lee JW, Lee HS, Lee JC, et al. Dynamic changes in Helicobacter pylori status following gastric cancer surgery. Gut Liver. 2017;11:209–15.PubMedCrossRef
21.
go back to reference Kim HJ, Kwon M, Kim N, Lee JB, Won S. The influence of family history on stage and survival of gastric cancer according to the TGFB1 C-509T polymorphism in Korea. Gut Liver. 2020;14:79–88.PubMedPubMedCentralCrossRef Kim HJ, Kwon M, Kim N, Lee JB, Won S. The influence of family history on stage and survival of gastric cancer according to the TGFB1 C-509T polymorphism in Korea. Gut Liver. 2020;14:79–88.PubMedPubMedCentralCrossRef
22.
go back to reference Lopes AI, Vale FF, Oleastro M. Helicobacter pylori infection - recent developments in diagnosis. World J Gastroenterol. 2014;20:9299–313.PubMedPubMedCentral Lopes AI, Vale FF, Oleastro M. Helicobacter pylori infection - recent developments in diagnosis. World J Gastroenterol. 2014;20:9299–313.PubMedPubMedCentral
23.
go back to reference Lee JY, Kim N, Kim MS, Choi YJ, Lee JW, Yoon H, et al. Factors affecting first-line triple therapy of Helicobacter pylori including CYP2C19 genotype and antibiotic resistance. Dig Dis Sci. 2014;59:1235–43.PubMedCrossRef Lee JY, Kim N, Kim MS, Choi YJ, Lee JW, Yoon H, et al. Factors affecting first-line triple therapy of Helicobacter pylori including CYP2C19 genotype and antibiotic resistance. Dig Dis Sci. 2014;59:1235–43.PubMedCrossRef
24.
go back to reference Yoon K, Kim N, Nam RH, Suh JH, Lee S, Kim JM, et al. Ultimate eradication rate of Helicobacter pylori after first, second, or third-line therapy in Korea. J Gastroenterol Hepatol. 2015;30:490–5.PubMedCrossRef Yoon K, Kim N, Nam RH, Suh JH, Lee S, Kim JM, et al. Ultimate eradication rate of Helicobacter pylori after first, second, or third-line therapy in Korea. J Gastroenterol Hepatol. 2015;30:490–5.PubMedCrossRef
25.
go back to reference Yoon K, Kim N. Eradication rates of 10-day sequential therapy for Helicobacter pylori: Results of an 8-year prospective study conducted at a tertiary Korean hospital. Korean J Gastroenterol. 2019;73:99–104.PubMedCrossRef Yoon K, Kim N. Eradication rates of 10-day sequential therapy for Helicobacter pylori: Results of an 8-year prospective study conducted at a tertiary Korean hospital. Korean J Gastroenterol. 2019;73:99–104.PubMedCrossRef
26.
go back to reference Information Committee of Korean Gastric Cancer Association. Korean gastric cancer association nationwide survey on gastric cancer in 2014. J Gastric Cancer. 2016;16:131–40.CrossRef Information Committee of Korean Gastric Cancer Association. Korean gastric cancer association nationwide survey on gastric cancer in 2014. J Gastric Cancer. 2016;16:131–40.CrossRef
27.
go back to reference Kim JH, Kim SS, Lee JH, Jung DH, Cheung DY, Chung WC, et al. Early detection is important to reduce the economic burden of gastric cancer. J Gastric cancer. 2018;18:82–9.PubMedPubMedCentralCrossRef Kim JH, Kim SS, Lee JH, Jung DH, Cheung DY, Chung WC, et al. Early detection is important to reduce the economic burden of gastric cancer. J Gastric cancer. 2018;18:82–9.PubMedPubMedCentralCrossRef
28.
go back to reference Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol. 2017;112:212–39.PubMedCrossRef Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol. 2017;112:212–39.PubMedCrossRef
29.
go back to reference Malfertheiner P, Megraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017;66:6–30.PubMedCrossRef Malfertheiner P, Megraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017;66:6–30.PubMedCrossRef
30.
go back to reference Hwang YJ, Kim N, Lee HS, Lee JB, Choi YJ, Yoon H, et al. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication - a prospective study for up to 10 years. Aliment Pharmacol Ther. 2018;47:380–90.PubMedCrossRef Hwang YJ, Kim N, Lee HS, Lee JB, Choi YJ, Yoon H, et al. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication - a prospective study for up to 10 years. Aliment Pharmacol Ther. 2018;47:380–90.PubMedCrossRef
31.
go back to reference Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64:1353–67.PubMedCrossRef Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64:1353–67.PubMedCrossRef
32.
go back to reference Hiroi S, Sugano K, Tanaka S, Kawakami K. Impact of health insurance coverage for Helicobacter pylori gastritis on the trends in eradication therapy in Japan: retrospective observational study and simulation study based on real-world data. BMJ Open. 2017;7:e015855.PubMedPubMedCentralCrossRef Hiroi S, Sugano K, Tanaka S, Kawakami K. Impact of health insurance coverage for Helicobacter pylori gastritis on the trends in eradication therapy in Japan: retrospective observational study and simulation study based on real-world data. BMJ Open. 2017;7:e015855.PubMedPubMedCentralCrossRef
34.
go back to reference Lee WJ, Lin JT, Shun CT, Lee WC, Yu SC, Lee PH, et al. Comparison between resectable gastric adenocarcinomas seropositive and seronegative for Helicobacter pylori. Br J Surg. 1995;82:802–5.PubMedCrossRef Lee WJ, Lin JT, Shun CT, Lee WC, Yu SC, Lee PH, et al. Comparison between resectable gastric adenocarcinomas seropositive and seronegative for Helicobacter pylori. Br J Surg. 1995;82:802–5.PubMedCrossRef
35.
go back to reference Kim YI, Cho SJ, Lee JY, Kim CG, Kook MC, Ryu KW, et al. Effect of Helicobacter pylori Eradication on long-term survival after distal gastrectomy for gastric cancer. Cancer Res Treat. 2016;48:1020–9.PubMedCrossRef Kim YI, Cho SJ, Lee JY, Kim CG, Kook MC, Ryu KW, et al. Effect of Helicobacter pylori Eradication on long-term survival after distal gastrectomy for gastric cancer. Cancer Res Treat. 2016;48:1020–9.PubMedCrossRef
36.
go back to reference Kato S, Matsukura N, Tsukada K, Matsuda N, Mizoshita T, Tsukamoto T, et al. Helicobacter pylori infection-negative gastric cancer in Japanese hospital patients: incidence and pathological characteristics. Cancer Sci. 2007;98:790–4.PubMedCrossRef Kato S, Matsukura N, Tsukada K, Matsuda N, Mizoshita T, Tsukamoto T, et al. Helicobacter pylori infection-negative gastric cancer in Japanese hospital patients: incidence and pathological characteristics. Cancer Sci. 2007;98:790–4.PubMedCrossRef
37.
go back to reference Yoon H, Kim N, Lee HS, Shin CM, Park YS, Lee DH, et al. Helicobacter pylori-negative gastric cancer in South Korea: incidence and clinicopathologic characteristics. Helicobacter. 2011;16:382–8.PubMedCrossRef Yoon H, Kim N, Lee HS, Shin CM, Park YS, Lee DH, et al. Helicobacter pylori-negative gastric cancer in South Korea: incidence and clinicopathologic characteristics. Helicobacter. 2011;16:382–8.PubMedCrossRef
38.
go back to reference Kim YI, Kim YA, Lee JW, Kim HJ, Kim SH, Kim SG, et al. Effect of Helicobacter pylori treatment on long-term mortality in patients with hypertension. Gut Liver. 2020;14:47–56.PubMedCrossRef Kim YI, Kim YA, Lee JW, Kim HJ, Kim SH, Kim SG, et al. Effect of Helicobacter pylori treatment on long-term mortality in patients with hypertension. Gut Liver. 2020;14:47–56.PubMedCrossRef
39.
go back to reference Lim SH, Kim N, Kwon JW, Kim SE, Baik GH, Lee JY, et al. Positive association between Helicobacter pylori infection and metabolic syndrome in a Korean population: a multicenter nationwide study. Dig Dis Sci. 2019;64:2219–30.PubMedCrossRef Lim SH, Kim N, Kwon JW, Kim SE, Baik GH, Lee JY, et al. Positive association between Helicobacter pylori infection and metabolic syndrome in a Korean population: a multicenter nationwide study. Dig Dis Sci. 2019;64:2219–30.PubMedCrossRef
40.
go back to reference Choi JM, Lim SH, Han YM, Lee H, Seo JY, Park HE, et al. Association between Helicobacter pylori infection and arterial stiffness: results from a large cross-sectional study. PLoS ONE. 2019;14:e0221643.PubMedPubMedCentralCrossRef Choi JM, Lim SH, Han YM, Lee H, Seo JY, Park HE, et al. Association between Helicobacter pylori infection and arterial stiffness: results from a large cross-sectional study. PLoS ONE. 2019;14:e0221643.PubMedPubMedCentralCrossRef
42.
go back to reference Benedetto U, Head SJ, Angelini GD, Blackstone EH. Statistical primer: propensity score matching and its alternatives. Eur J Cardiothorac Surg. 2018;53:1112–7.PubMedCrossRef Benedetto U, Head SJ, Angelini GD, Blackstone EH. Statistical primer: propensity score matching and its alternatives. Eur J Cardiothorac Surg. 2018;53:1112–7.PubMedCrossRef
43.
45.
go back to reference Guo CG, Cheung KS, Zhang F, Chan EW, Chen L, Wong IC, Leung WK. Incidences, temporal trends and risks of hospitalisation for gastrointestinal bleeding in new or chronic low-dose aspirin users after treatment for Helicobacter pylori: a territory-wide cohort study. Gut. 2020;69:445–52.PubMedCrossRef Guo CG, Cheung KS, Zhang F, Chan EW, Chen L, Wong IC, Leung WK. Incidences, temporal trends and risks of hospitalisation for gastrointestinal bleeding in new or chronic low-dose aspirin users after treatment for Helicobacter pylori: a territory-wide cohort study. Gut. 2020;69:445–52.PubMedCrossRef
Metadata
Title
Effect of Helicobacter pylori eradication after subtotal gastrectomy on the survival rate of patients with gastric cancer: follow-up for up to 15 years
Authors
Yonghoon Choi
Nayoung Kim
Chang Yong Yun
Yoon Jin Choi
Hyuk Yoon
Cheol Min Shin
Young Soo Park
Sang-Hoon Ahn
Do Joong Park
Hye Seung Lee
Ji-Won Kim
Jin Won Kim
Keun-Wook Lee
Won Chang
Ji Hoon Park
Yoon Jin Lee
Kyoung Ho Lee
Young Hoon Kim
Dong Ho Lee
Hyung-Ho Kim
Publication date
01-11-2020
Publisher
Springer Nature Singapore
Published in
Gastric Cancer / Issue 6/2020
Print ISSN: 1436-3291
Electronic ISSN: 1436-3305
DOI
https://doi.org/10.1007/s10120-020-01076-2

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