Advertisement
Mayo Clinic Proceedings Home

Smokeless Tobacco and Cigar and/or Pipe Are Risk Factors for Barrett Esophagus in Male Patients With Gastroesophageal Reflux Disease

      Abstract

      Objective

      To investigate the effect of smokeless tobacco (ST), cigar and/or pipe smoking (CP) on the development of Barrett esophagus (BE) in white male patients with gastroesophageal reflux disease (GERD).

      Patients and Methods

      A total of 1015 records of white male adults with BE (cases; n=508) or GERD (controls, n=507) were reviewed for lifestyle factors. Logistic regression analyses were performed after adjusting for lifestyle factors to assess the effects of ST and CP on the risk of developing BE. Differences between patients with BE and those with GERD were compared using chi-square and t tests.

      Results

      Patients with BE were significantly older than patients with GERD (mean age, 66±12 years for patients with BE and 55±15 years for patients with GERD; P<.001). The odds of developing BE in patients who used CS were 1.7 times higher than that in patients who never smoked cigarettes (odds ratio [OR], 1.7; 95% CI, 1.3-2.2). It was observed that when CS use was combined with either ST or CP use, the odds of having BE significantly increased (OR, 2.5; 95% CI, 1.2-5.2; P=.01 and OR, 1.9; 95% CI, 1.03-3.58; P=.04) in comparison to CS alone. There were no significant differences in body mass index and alcohol consumption between BE and GERD groups.

      Conclusion

      This study suggests that there is indeed an association between CS and BE. We believe that this is the first time that ST and CP were associated with an even higher odds of developing BE. Further studies are needed to investigate whether the use of ST and CP is also associated with an increased risk of developing BE-associated adenocarcinoma.

      Abbreviations and Acronyms:

      BE (Barrett esophagus), BMI (body mass index), CP (cigar and/or pipe), CS (cigarette smoking), EAC (esophageal adenocarcinoma), GERD (gastroesophageal reflux disease), OR (odds ratio), ST (smokeless tobacco)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Mayo Clinic Proceedings
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Ronkainen J.
        • Talley N.J.
        • Storskrubb T.
        • et al.
        Erosive esophagitis is a risk factor for Barrett's esophagus: a community-based endoscopic follow-up study.
        Am J Gastroenterol. 2011; 106: 1946-1952
        • Zagari R.M.
        • Fuccio L.
        • Wallander M.A.
        • et al.
        Gastro-oesophageal reflux symptoms, oesophagitis and Barrett's oesophagus in the general population: the Loiano-Monghidoro study.
        Gut. 2008; 57: 1354-1359
        • Bhat S.
        • Coleman H.G.
        • Yousef F.
        • et al.
        Risk of malignant progression in Barrett’s esophagus patients: results from a large population-based study.
        J Natl Cancer Inst. 2011; 103 ([published correction appears in J Natl Cancer Inst. 2013;105(8):581]): 1049-1057
        • Hvid-Jensen F.
        • Pedersen L.
        • Drewes A.M.
        • Sørensen H.T.
        • Funch-Jensen P.
        Incidence of adenocarcinoma among patients with Barrett's esophagus.
        N Engl J Med. 2011; 365: 1375-1383
        • Corley D.A.
        • Kubo A.
        • Levin T.R.
        • et al.
        Race, ethnicity, sex and temporal differences in Barrett’s oesophagus diagnosis: a large community-based study.
        Gut. 2009; 58: 182-188
        • Cook M.B.
        • Wild C.P.
        • Forman D.
        A systematic review and meta-analysis of the sex ratio for Barrett's esophagus, erosive reflux disease, and nonerosive reflux disease.
        Am J Epidemiol. 2005; 162: 1050-1061
        • Ford A.C.
        • Forman D.
        • Reynolds P.D.
        • Cooper B.T.
        • Moayyedi P.
        Ethnicity, gender, and socioeconomic status as risk factors for esophagitis and Barrett's esophagus.
        Am J Epidemiol. 2005; 162: 454-460
        • Shapiro J.
        • van Lanschot J.J.
        • Hulshof M.C.
        • et al.
        • CROSS Study Group
        Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial.
        Lancet Oncol. 2015; 16: 1090-1098
        • Bhat S.K.
        • McManus D.T.
        • Coleman H.G.
        • et al.
        Oesophageal adenocarcinoma and prior diagnosis of Barrett's oesophagus: a population-based study.
        Gut. 2015; 64: 20-25
        • Fountoulakis A.
        • Zafirellis K.D.
        • Dolan K.
        • Dexter S.P.
        • Martin I.G.
        • Sue-Ling H.M.
        Effect of surveillance of Barrett's oesophagus on the clinical outcome of oesophageal cancer.
        Br J Surg. 2004; 91: 997-1003
        • Lagergren J.
        • Bergström R.
        • Lindgren A.
        • Nyrén O.
        Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma.
        N Engl J Med. 1999; 340: 825-831
        • Anderson L.A.
        • Cantwell M.M.
        • Watson R.G.
        • et al.
        The association between alcohol and reflux esophagitis, Barrett's esophagus, and esophageal adenocarcinoma.
        Gastroenterology. 2009; 136: 799-805
        • Cook M.B.
        • Shaheen N.J.
        • Anderson L.A.
        • et al.
        Cigarette smoking increases risk of Barrett’s esophagus: an analysis of the Barrett's and Esophageal Adenocarcinoma Consortium.
        Gastroenterology. 2012; 142: 744-753
        • El-Serag H.B.
        • Hashmi A.
        • Garcia J.
        • et al.
        Visceral abdominal obesity measured by CT scan is associated with an increased risk of Barrett's oesophagus: a case-control study.
        Gut. 2014; 63: 220-229
        • El-Serag H.B.
        • Lagergren J.
        Alcohol drinking and the risk of Barrett's esophagus and esophageal adenocarcinoma.
        Gastroenterology. 2009; 136: 1155-1157
        • Kramer J.R.
        • Fischbach L.A.
        • Richardson P.
        • et al.
        Waist-to-hip ratio, but not body mass index, is associated with an increased risk of Barrett's esophagus in white men.
        Clin Gastroenterol Hepatol. 2013; 11: 373-381.e381
        • Su Z.
        • Gay L.J.
        • Strange A.
        • et al.
        • Esophageal Adenocarcinoma Genetics Consortium
        • Wellcome Trust Case Control Consortium 2
        Common variants at the MHC locus and at chromosome 16q24.1 predispose to Barrett's esophagus.
        Nat Genet. 2012; 44: 1131-1136
        • Thrift A.P.
        • Cook M.B.
        • Vaughan T.L.
        • et al.
        Alcohol and the risk of Barrett's esophagus: a pooled analysis from the International BEACON Consortium.
        Am J Gastroenterol. 2014; 109: 1586-1594
        • National Cancer Institute and Centers for Disease Control and Prevention
        Smokeless Tobacco and Public Health: A Global Perspective.
        National Cancer Institute, Centers for Disease Control and Prevention and National Institutes of Health, US Dept of Health and Human Services, Bethesda, MD2014 (NIH publication 14-7983)
        • Maki J.
        The incentives created by a harm reduction approach to smoking cessation: Snus and smoking in Sweden and Finland.
        Int J Drug Policy. 2015; 26: 569-574
        • Statens Folkhälsoinstitut
        Minskat bruk av tobak—var star vi i dag? Statistik, Oktober 2007.
        Statens Folkhälsoinstitut, Stockholm, Sweden2014
        • Rigotti N.A.
        • Lee J.E.
        • Wechsler H.
        US college students' use of tobacco products: results of a national survey.
        JAMA. 2000; 284: 699-705
        • Centers for Disease Control and Prevention (CDC)
        Cigar smoking among teenagers—United States, Massachusetts, and New York, 1996.
        MMWR Morb Mortal Wkly Rep. 1997; 46: 433-440
        • National Cancer Institute
        Smoking and Tobacco Control Monographs, Volume 9: Cigars: Health Effects and Trends.
        National Cancer Institute, National Institutes of Health, Public Health Service, US Dept of Health and Human Services, Bethesda, MD1998
        • U.S. Department of Health and Human Services
        E-Cigarette Use Among Youth and Young Adults: A Report of the Surgeon General—Executive Summary.
        Office on Smoking and Health, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, US Dept of Health and Human Services, Atlanta, GA2016
      1. Cigars aren’t a safe alternative to cigarettes.
        Mayo Clin Health Lett. 1998; 16: 4
        • Iribarren C.
        • Tekawa I.S.
        • Sidney S.
        • Friedman G.D.
        Effect of cigar smoking on the risk of cardiovascular disease, chronic obstructive pulmonary disease, and cancer in men.
        N Engl J Med. 1999; 340: 1773-1780
        • Henley S.J.
        • Thun M.J.
        • Chao A.
        • Calle E.E.
        Association between exclusive pipe smoking and mortality from cancer and other diseases.
        J Natl Cancer Inst. 2004; 96: 853-861
        • IARC Working Group on the Evaluation of Carcinogenic Risk to Humans
        Smokeless Tobacco and Some Tobacco-Specific N-Nitrosamines: IARC Monographs on the Evaluations of Carcinogenic Risks to Humans, No. 89.
        International Agency for Research on Cancer, Lyon, France2007
      2. IARC Monographs programme on the evaluation of the carcinogenic risk of chemicals to humans: Preamble.
        IARC Monogr Eval Carcinog Risk Chem Hum. 1986; 39: 13-32
        • Henningfield J.E.
        • Hariharan M.
        • Kozlowski L.T.
        Nicotine content and health risks of cigars.
        JAMA. 1996; 276: 1857-1858
        • Siddiqi K.
        • Shah S.
        • Abbas S.M.
        • et al.
        Global burden of disease due to smokeless tobacco consumption in adults: analysis of data from 113 countries.
        BMC Med. 2015; 13: 194
        • Sinha D.N.
        • Abdulkader R.S.
        • Gupta P.C.
        Smokeless tobacco-associated cancers: a systematic review and meta-analysis of Indian studies.
        Int J Cancer. 2016; 138: 1368-1379
        • Aro P.
        • Ronkainen J.
        • Storskrubb T.
        • et al.
        Use of tobacco products and gastrointestinal morbidity: an endoscopic population-based study (the Kalixanda study).
        Eur J Epidemiol. 2010; 25: 741-750
        • Clemons N.J.
        • McColl K.E.
        • Fitzgerald R.C.
        Nitric oxide and acid induce double-strand DNA breaks in Barrett's esophagus carcinogenesis via distinct mechanisms.
        Gastroenterology. 2007; 133: 1198-1209
      3. Centers for Disease Control and Prevention. Smokeless tobacco fact sheets. Presented at: 3rd International Conference on Smokeless Tobacco: Advancing Science and Protecting Public Health; September 22-25, 2002; Stockholm, Sweden.

        • Cook M.B.
        • Kamangar F.
        • Whiteman D.C.
        • et al.
        Cigarette smoking and adenocarcinomas of the esophagus and esophagogastric junction: a pooled analysis from the international BEACON Consortium.
        J Natl Cancer Inst. 2010; 102: 1344-1353
        • Aiyer H.S.
        • Li Y.
        • Harper N.
        • Myers S.R.
        • Martin R.C.
        Molecular changes in the esophageal epithelium after a subchronic exposure to cigarette smoke in the presence of bile-acid reflux.
        Inhal Toxicol. 2011; 23: 304-311
        • Nguyen T.
        • Tang Z.
        • Younes M.
        • et al.
        Esophageal COX-2 expression is increased in Barrett's esophagus, obesity, and smoking.
        Dig Dis Sci. 2015; 60: 65-73
        • Shin V.Y.
        • Wu W.K.
        • Ye Y.N.
        • et al.
        Nicotine promotes gastric tumor growth and neovascularization by activating extracellular signal-regulated kinase and cyclooxygenase-2.
        Carcinogenesis. 2004; 25: 2487-2495
        • Lagergren J.
        • Bergström R.
        • Lindgren A.
        • Nyrén O.
        The role of tobacco, snuff and alcohol use in the aetiology of cancer of the oesophagus and gastric cardia.
        Int J Cancer. 2000; 85: 340-346
        • Phukan R.K.
        • Ali M.S.
        • Chetia C.K.
        • Mahanta J.
        Betel nut and tobacco chewing; potential risk factors of cancer of oesophagus in Assam, India.
        Br J Cancer. 2001; 85: 661-667
        • Kubo A.
        • Levin T.R.
        • Block G.
        • et al.
        Cigarette smoking and the risk of Barrett’s esophagus.
        Cancer Causes Control. 2009; 20: 303-311
        • Singh T.
        • Arrazola R.A.
        • Corey C.G.
        • et al.
        Tobacco use among middle and high school students—United States, 2011-2015.
        MMWR Morb Mortal Wkly Rep. 2016; 65: 361-367
        • Bostean G.
        • Trinidad D.R.
        • McCarthy W.J.
        E-Cigarette Use Among Never-Smoking California Students.
        Am J Public Health. 2015; 105: 2423-2425
        • Lei W.
        • Lerner C.
        • Sundar I.K.
        • Rahman I.
        Myofibroblast differentiation and its functional properties are inhibited by nicotine and e-cigarette via mitochondrial OXPHOS complex III.
        Sci Rep. 2017; 7: 43213
        • Canistro D.
        • Vivarelli F.
        • Cirillo S.
        • et al.
        E-cigarettes induce toxicological effects that can raise the cancer risk.
        Sci Rep. 2017; 7: 2028
        • Thrift A.P.
        • Pandeya N.
        • Smith K.J.
        • et al.
        Lifetime alcohol consumption and risk of Barrett’s esophagus.
        Am J Gastroenterol. 2011; 106: 1220-1230
        • El-Serag H.
        The association between obesity and GERD: a review of the epidemiological evidence.
        Dig Dis Sci. 2008; 53: 2307-2312