Skip to main content
Top
Published in: BMC Cancer 1/2019

Open Access 01-12-2019 | Gastric Cancer | Research article

Smoking status and subsequent gastric cancer risk in men compared with women: a meta-analysis of prospective observational studies

Authors: Wen-Ya Li, Yunan Han, Hui-Mian Xu, Zhen-Ning Wang, Ying-Ying Xu, Yong-Xi Song, Hao Xu, Song-Cheng Yin, Xing-Yu Liu, Zhi-Feng Miao

Published in: BMC Cancer | Issue 1/2019

Login to get access

Abstract

Background

Smoking is one of the well-established risk factors for gastric cancer incidence, yet whether men are more or equally susceptible to gastric cancer due to smoking compared with women is a matter of controversy. The aim of this study was to investigate and compare the effect of sex on gastric cancer risk associated with smoking.

Methods

We conducted a systemic literature search in MEDLINE, EMBASE, and the Cochrane CENTRAL databases to identify studies published from inception to December 2018. We included prospective observational studies which reported effect estimates with 95% confidence intervals (CIs) for associations of current or former smokers with the incidence of gastric cancer by sex. We calculated the ratio of relative risk (RRR) with corresponding 95% CI based on sex-specific effect estimates for current or former smokers versus non-smokers on the risk of gastric cancer.

Results

We included 10 prospective studies with 3,381,345 participants in our analysis. Overall, the summary RRR (male to female) for gastric cancer risk in current smokers was significantly increased compared with non-smokers (RRR: 1.30; 95% CI: 1.05–1.63; P = 0.019). Furthermore, there was no significant sex difference for the association between former smokers and gastric cancer risk (RRR: 1.20; 95% CI: 0.92–1.55; P = 0.178). However, the result of sensitivity analysis indicated the pooled result was not stable, which was altered by excluding a nested case-control study (RRR: 1.31; 95% CI: 1.10–1.57; P = 0.002).

Conclusion

This systematic review showed a potential sex difference association between current smokers and the risk of gastric cancer. The sex differential in smokers can give important clues for the etiology of gastric cancers and should be examined in further studies.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRef Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRef
3.
go back to reference Bae JM, Kim EH. Helicobacter pylori infection and risk of gastric Cancer in Korea: a quantitative systematic review. J Prev Med Public Health. 2016;49:197–204.CrossRef Bae JM, Kim EH. Helicobacter pylori infection and risk of gastric Cancer in Korea: a quantitative systematic review. J Prev Med Public Health. 2016;49:197–204.CrossRef
4.
go back to reference Deng W, Yang H, Wang J, et al. Coffee consumption and the risk of incident gastric cancer--a meta-analysis of prospective cohort studies. Nutr Cancer. 2016;68:40–7.CrossRef Deng W, Yang H, Wang J, et al. Coffee consumption and the risk of incident gastric cancer--a meta-analysis of prospective cohort studies. Nutr Cancer. 2016;68:40–7.CrossRef
5.
go back to reference Sun Y, Lin LJ, Sang LX, et al. Dairy product consumption and gastric cancer risk: a meta-analysis. World J Gastroenterol. 2014;20:15879–98.CrossRef Sun Y, Lin LJ, Sang LX, et al. Dairy product consumption and gastric cancer risk: a meta-analysis. World J Gastroenterol. 2014;20:15879–98.CrossRef
6.
go back to reference Song P, Lu M, Yin Q, et al. Red meat consumption and stomach cancer risk: a meta-analysis. J Cancer Res Clin Oncol. 2014;140:979–92.CrossRef Song P, Lu M, Yin Q, et al. Red meat consumption and stomach cancer risk: a meta-analysis. J Cancer Res Clin Oncol. 2014;140:979–92.CrossRef
7.
go back to reference Chen Y, Liu L, Wang X, et al. Body mass index and risk of gastric cancer: a meta-analysis of a population with more than ten million from 24 prospective studies. Cancer Epidemiol Biomark Prev. 2013;22:1395–408.CrossRef Chen Y, Liu L, Wang X, et al. Body mass index and risk of gastric cancer: a meta-analysis of a population with more than ten million from 24 prospective studies. Cancer Epidemiol Biomark Prev. 2013;22:1395–408.CrossRef
8.
go back to reference Bonequi P, Meneses-González F, Correa P, et al. Risk factors for gastric cancer in Latin America: a meta-analysis. Cancer Causes Control. 2013;24:217–31.CrossRef Bonequi P, Meneses-González F, Correa P, et al. Risk factors for gastric cancer in Latin America: a meta-analysis. Cancer Causes Control. 2013;24:217–31.CrossRef
9.
go back to reference Tredaniel J, Boffetta P, Buiatti E, et al. Tobacco smoking and gastric cancer: review and meta-analysis. Int J Cancer. 1997;72:565–73.CrossRef Tredaniel J, Boffetta P, Buiatti E, et al. Tobacco smoking and gastric cancer: review and meta-analysis. Int J Cancer. 1997;72:565–73.CrossRef
10.
go back to reference Barstad B, Sorensen TI, Tjonneland A, et al. Intake of wine, beer and spirits and risk of gastric cancer. Eur J Cancer Prev. 2005;14:239–43.CrossRef Barstad B, Sorensen TI, Tjonneland A, et al. Intake of wine, beer and spirits and risk of gastric cancer. Eur J Cancer Prev. 2005;14:239–43.CrossRef
11.
go back to reference Franke A, Teyssen S, Singer MV. Alcohol-related diseases of the esophagus and stomach. Dig Dis. 2005;23:204–13.CrossRef Franke A, Teyssen S, Singer MV. Alcohol-related diseases of the esophagus and stomach. Dig Dis. 2005;23:204–13.CrossRef
12.
go back to reference Ladeiras-Lopes R, Pereira AK, Nogueira A, et al. Smoking and gastric cancer: systematic review and meta-analysis of cohort studies. Cancer Causes Control. 2008;19:689–701.CrossRef Ladeiras-Lopes R, Pereira AK, Nogueira A, et al. Smoking and gastric cancer: systematic review and meta-analysis of cohort studies. Cancer Causes Control. 2008;19:689–701.CrossRef
13.
go back to reference Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.CrossRef Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.CrossRef
15.
go back to reference Huxley R, Barzi F, Woodward M. Excess risk of fatal coronary heart disease associated with diabetes in men and women: meta-analysis of 37 prospective cohort studies. BMJ. 2006;332:73–8.CrossRef Huxley R, Barzi F, Woodward M. Excess risk of fatal coronary heart disease associated with diabetes in men and women: meta-analysis of 37 prospective cohort studies. BMJ. 2006;332:73–8.CrossRef
16.
go back to reference DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.CrossRef DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.CrossRef
17.
go back to reference Ades AE, Lu G, Higgins JP. The interpretation of random-effects metaanalysis in decision models. Med Decis Mak. 2005;25:646–54.CrossRef Ades AE, Lu G, Higgins JP. The interpretation of random-effects metaanalysis in decision models. Med Decis Mak. 2005;25:646–54.CrossRef
18.
go back to reference Deeks JJ, Higgins JP, Altman DG. Analyzing data and undertaking meta-analyses. In: Higgins J, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions 5.0.1. Oxford, UK: The Cochrane Collaboration: 2008; chap 9. Deeks JJ, Higgins JP, Altman DG. Analyzing data and undertaking meta-analyses. In: Higgins J, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions 5.0.1. Oxford, UK: The Cochrane Collaboration: 2008; chap 9.
19.
go back to reference Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.CrossRef Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.CrossRef
20.
go back to reference Tobias A. Assessing the influence of a single study in meta-analysis. Stata Tech Bull. 1999;47:15–7. Tobias A. Assessing the influence of a single study in meta-analysis. Stata Tech Bull. 1999;47:15–7.
21.
go back to reference Thompson SG, Higgins JP. How should meta-regression analyses be undertaken and interpreted? Stat Med. 2002;21:1559–73.CrossRef Thompson SG, Higgins JP. How should meta-regression analyses be undertaken and interpreted? Stat Med. 2002;21:1559–73.CrossRef
22.
go back to reference Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.CrossRef Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.CrossRef
23.
go back to reference Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRef Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRef
24.
go back to reference Fujino Y, Mizoue T, Tokui N, et al. Cigarette smoking and mortality due to stomach Cancer: findings from the JACC study. J Epidemiol. 2005;15(Suppl 2):S113–9.CrossRef Fujino Y, Mizoue T, Tokui N, et al. Cigarette smoking and mortality due to stomach Cancer: findings from the JACC study. J Epidemiol. 2005;15(Suppl 2):S113–9.CrossRef
25.
go back to reference Kato I, Tominaga S, Matsumoto K. A prospective study of stomach cancer among a rural Japanese population: a 6-year survey. Jpn J Cancer Res. 1992;83:568–75.PubMedPubMedCentral Kato I, Tominaga S, Matsumoto K. A prospective study of stomach cancer among a rural Japanese population: a 6-year survey. Jpn J Cancer Res. 1992;83:568–75.PubMedPubMedCentral
26.
go back to reference Tverdal A, Thelle D, Stensvold I, et al. Mortality in relation to smoking history: 13 years follow-up of 68,000 Norwegian men and women 35-49 years. J Clin Epidemiol. 1993;46:475–87.CrossRef Tverdal A, Thelle D, Stensvold I, et al. Mortality in relation to smoking history: 13 years follow-up of 68,000 Norwegian men and women 35-49 years. J Clin Epidemiol. 1993;46:475–87.CrossRef
27.
go back to reference Engeland A, Andersen A, Haldorsen T, et al. Smoking habits and risk of cancers other than lung cancer: 28 years' follow-up of 26,000 Norwegian men and women. Cancer Causes Control. 1996;7:497–506.CrossRef Engeland A, Andersen A, Haldorsen T, et al. Smoking habits and risk of cancers other than lung cancer: 28 years' follow-up of 26,000 Norwegian men and women. Cancer Causes Control. 1996;7:497–506.CrossRef
28.
go back to reference Lindblad M, LA G’a R’g, Lagergren J. Body mass, tobacco and alcohol and risk of esophageal, gastric cardia, and gastric non-cardia adenocarcinoma among men and women in a nested case-control study. Cancer Causes Control. 2005;16:285–94.CrossRef Lindblad M, LA G’a R’g, Lagergren J. Body mass, tobacco and alcohol and risk of esophageal, gastric cardia, and gastric non-cardia adenocarcinoma among men and women in a nested case-control study. Cancer Causes Control. 2005;16:285–94.CrossRef
29.
go back to reference Jee SH, Samet JM, Ohrr H, et al. Smoking and cancer risk in Korean men and women. Cancer Causes Control. 2004;15:341–8.PubMed Jee SH, Samet JM, Ohrr H, et al. Smoking and cancer risk in Korean men and women. Cancer Causes Control. 2004;15:341–8.PubMed
30.
go back to reference Chao A, Thun MJ, Henley SJ, et al. Cigarette smoking, use of other tobacco products and stomach cancer mortality in US adults: the Cancer prevention study II. Int J Cancer. 2002;101:380–9.CrossRef Chao A, Thun MJ, Henley SJ, et al. Cigarette smoking, use of other tobacco products and stomach cancer mortality in US adults: the Cancer prevention study II. Int J Cancer. 2002;101:380–9.CrossRef
31.
go back to reference Akiba S, Hirayama T. Cigarette smoking and cancer mortality risk in Japanese men and women--results from reanalysis of the six-prefecture cohort study data. Environ Health Perspect. 1990;87:19–26.PubMedPubMedCentral Akiba S, Hirayama T. Cigarette smoking and cancer mortality risk in Japanese men and women--results from reanalysis of the six-prefecture cohort study data. Environ Health Perspect. 1990;87:19–26.PubMedPubMedCentral
32.
go back to reference González CA, Pera G, Agudo A, et al. Smoking and the risk of gastric cancer in the European prospective investigation into Cancerand nutrition (EPIC). Int J Cancer. 2003;107:629–34.CrossRef González CA, Pera G, Agudo A, et al. Smoking and the risk of gastric cancer in the European prospective investigation into Cancerand nutrition (EPIC). Int J Cancer. 2003;107:629–34.CrossRef
33.
go back to reference Nomura AM, Wilkens LR, Henderson BE, et al. The association of cigarette smoking with gastric cancer: the multiethnic cohort study. Cancer Causes Control. 2012;23:51–8.PubMed Nomura AM, Wilkens LR, Henderson BE, et al. The association of cigarette smoking with gastric cancer: the multiethnic cohort study. Cancer Causes Control. 2012;23:51–8.PubMed
34.
go back to reference Koizumi Y, Tsubono Y, Nakaya N, et al. Cigarette smoking and the risk of gastric cancer: a pooled analysis of two prospective studies in Japan. Int J Cancer. 2004;112:1049–55.CrossRef Koizumi Y, Tsubono Y, Nakaya N, et al. Cigarette smoking and the risk of gastric cancer: a pooled analysis of two prospective studies in Japan. Int J Cancer. 2004;112:1049–55.CrossRef
35.
go back to reference Nishino Y, Inoue M, Tsuji I, et al. Tobacco smoking and gastric cancer risk: an evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Jpn J Clin Oncol. 2006;36:800–7.CrossRef Nishino Y, Inoue M, Tsuji I, et al. Tobacco smoking and gastric cancer risk: an evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Jpn J Clin Oncol. 2006;36:800–7.CrossRef
36.
go back to reference Hoshiyama Y, Sasaba T. A case-control study of stomach cancer and its relation to diet, cigarettes and alcohol consumption in Saitama prefecture, Japan. Cancer Causes Control. 1992;3:441–8.CrossRef Hoshiyama Y, Sasaba T. A case-control study of stomach cancer and its relation to diet, cigarettes and alcohol consumption in Saitama prefecture, Japan. Cancer Causes Control. 1992;3:441–8.CrossRef
37.
go back to reference Tramacere I, Negri E, Pelucchi C, et al. A meta-analysis on alcohol drinking and gastric cancer risk. Ann Oncol. 2012;23:28–36.CrossRef Tramacere I, Negri E, Pelucchi C, et al. A meta-analysis on alcohol drinking and gastric cancer risk. Ann Oncol. 2012;23:28–36.CrossRef
Metadata
Title
Smoking status and subsequent gastric cancer risk in men compared with women: a meta-analysis of prospective observational studies
Authors
Wen-Ya Li
Yunan Han
Hui-Mian Xu
Zhen-Ning Wang
Ying-Ying Xu
Yong-Xi Song
Hao Xu
Song-Cheng Yin
Xing-Yu Liu
Zhi-Feng Miao
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2019
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-019-5601-9

Other articles of this Issue 1/2019

BMC Cancer 1/2019 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine