Skip to main content

Advertisement

SpringerLink
Log in

Smoking and Barrett’s Esophagus in Women Who Undergo Upper Endoscopy

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background

Cigarette use is associated with esophageal adenocarcinoma, and cross-sectional studies suggest an association between smoking and Barrett’s esophagus.

Aims

We sought to examine prospectively the effect of smoking on the risk for Barrett’s esophagus.

Methods

This was a prospective cohort study among 20,863 women within the Nurses’ Health Study who underwent upper gastrointestinal endoscopy for any reason between 1980 and 2006. We assessed the association between smoking and pathologically-confirmed Barrett’s esophagus (n = 377). Self-reported data on smoking and potential confounding variables were collected from biennial questionnaires.

Results

Compared with women who never smoked, former smokers of 1–24 cigarettes/day had a multivariate odds ratio for Barrett’s esophagus of 1.25 (95% CI 0.99–1.59), former smokers of ≥25 cigarettes/day had a multivariate odds ratio of 1.52 (95% CI 1.04–2.22), current smokers of 1–24 cigarettes/day had a multivariate odds ratio of 0.89 (95% CI 0.54–1.45), and current smokers of ≥25 cigarettes/day had a multivariate odds ratio of 0.92 (95% CI 0.34–2.54). The risk for Barrett’s esophagus increased significantly with increasing pack-years smoked among former (P = 0.008) but not current smokers (P = 0.99), especially when considering exposure ≥25 years before index endoscopy. Results were similar among women reporting regular heartburn/acid-reflux one or more times a week, and were not accounted for by changes in weight.

Conclusions

Heavy, remote smoking is associated with an increased risk for Barrett’s esophagus. This finding suggests a long latency period between exposure and development of the disease, even after discontinuation of smoking.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

GERD:

Gastroesophageal reflux disease

SIM:

Specialized intestinal metaplasia

MET:

Metabolic equivalent task

CI:

Confidence interval

OR:

Odds ratio

References

  1. Caldwell MT, Lawlor P, Byrne PJ, Walsh TN, Hennessy TP. Ambulatory oesophageal bile reflux monitoring in Barrett’s oesophagus. Br J Surg. 1995;82:657–660.

    Article  PubMed  CAS  Google Scholar 

  2. Vaezi MF, Richter JE. Role of acid and duodenogastroesophageal reflux in gastroesophageal reflux disease. Gastroenterology. 1996;111:1192–1199.

    Article  PubMed  CAS  Google Scholar 

  3. Jankowski J, Wright N, Meltzer S, et al. Molecular evolution of the metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am J Pathol. 1999;154:965–973.

    Article  PubMed  CAS  Google Scholar 

  4. Boch J, Shields H, Antonioli D, Zwas F, Sawhney R, Trier J. Distribution of cytokeratin markers in Barrett’s specialized columnar epithelium. Gastroenterology. 1997;112:760–765.

    Article  PubMed  CAS  Google Scholar 

  5. Okamoto R, Yajima T, Yamazaki M, et al. Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nature Med. 2002;8:1011–1017.

    Article  PubMed  CAS  Google Scholar 

  6. Cameron A. Epidemiology of columnar-lined esophagus and adenocarcinoma. Gastroenterol Clin North Am. 1997;26:487–494.

    Article  PubMed  CAS  Google Scholar 

  7. Winters C, Spurling T, Cohbanian S, et al. Barrett’s esophagus: a prevalent, occult complication of gastroesophageal reflux disease. Gastroenterology. 1987;92:118–124.

    PubMed  Google Scholar 

  8. Gerson L, Shetler K, Triadafilopoulos G. Prevalence of Barrett’s esophagus in asymptomatic individuals. Gastroenterology. 2002;123:461–467.

    Article  PubMed  Google Scholar 

  9. Rex DK, Cummings OW, Shaw M, et al. Screening for Barrett’s esophagus in colonoscopy patients with and without heartburn. Gastroenterology. 2003;125:1670–1677.

    Article  PubMed  Google Scholar 

  10. Cameron A, Zinsmeister A, Ballard D, Carney J. Prevalence of columnar-lined (Barrett’s) esophagus: comparison of population-based and autopsy findings. Gastroenterology. 1990;99:918–922.

    PubMed  CAS  Google Scholar 

  11. O’Connor J, Falk GW, Richter JE. The incidence of adenocarcinoma and dysplasia in Barrett’s esophagus. Am J Gastroenterol. 1999;94:2037–2042.

    PubMed  Google Scholar 

  12. Spechler S, Zeroogian J, Antonioli D, Wang H, Goyal R. Prevalence of metaplasia at the gastro-oesophageal junction. Lancet. 1994;344:1533–1536.

    Article  PubMed  CAS  Google Scholar 

  13. Caygill C, Reed P, McIntyre A, Hill M. The UK national barrett’s oesophagus registry: a study between two centres. Eur J Cancer Prev. 1998;7:161–163.

    PubMed  CAS  Google Scholar 

  14. Blot WJ, Devesa SS, Kneller RW, Fraumeni JF. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA. 1991;265:1287–1289.

    Article  PubMed  CAS  Google Scholar 

  15. Conio M, Cameron AJ, Romero Y, et al. Secular trends in the epidemiology and outcome of Barrett’s oesophagus in Olmsted County, Minnesota. Gut. 2001;48:304–309.

    Article  PubMed  CAS  Google Scholar 

  16. Devesa S, Blot WJ, Fraumeni JF. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer. 1998;83:2049–2053.

    Article  PubMed  CAS  Google Scholar 

  17. Prach AT, MacDonald TA, Hopwood DA, Johnston DA. Increasing incidence of Barrett’s oesophagus: education, enthusiasm, or epidemiology? Lancet. 1997;350:933.

    Article  PubMed  CAS  Google Scholar 

  18. van Soest E, Dieleman J, Siersema P, Sturkenboom M, Kuipers E. Increasing incidence of Barrett’s oesophagus in the general population. Gut. 2005;54:1062–1066.

    Article  PubMed  Google Scholar 

  19. Spechler SJ, Robbins AH, Rubins HB, et al. Adenocarcinoma and Barrett’s esophagus: an overrated risk? Gastroenterology. 1984;87:927–933.

    PubMed  CAS  Google Scholar 

  20. Cameron A, Ott B, Payne W. The incidence of adenocarcinoma in columnar-lined (Barrett’s) esophagus. N Engl J Med. 1985;313:857–859.

    Article  PubMed  CAS  Google Scholar 

  21. Spechler S, Lee E, Ahnen D, et al. Long-term outcome of medical and surgical therapies for gastroesophageal reflux disease: follow-up of a randomized controlled trial. JAMA. 2001;285:2331–2338.

    Article  PubMed  CAS  Google Scholar 

  22. Corey K, Schmitz S, Shaheen N. Does a surgical antireflux procedure decrease the incidence of esophageal adenocarcinoma in Barrett’s esophagus? A meta-analysis. Am J Gastroenterol. 2003;98:2390–2394.

    Article  PubMed  Google Scholar 

  23. Shaheen N, Crosby M, Bozymski E, Sandler R. Is there publication bias in the reporting of cancer risk in Barrett’s esophagus? Gastroenterology. 2000;119:333–338.

    Article  PubMed  CAS  Google Scholar 

  24. Murray L, Watson P, Johnston B, SLoan J, Mainie I, Gavin A. Risk of adenocarcinoma in Barrett’s esophagus: population based study. BMJ. 2003;327:534–535.

    Article  PubMed  Google Scholar 

  25. Conio M, Blanchi S, Lapertosa G. Long-term endoscopic surveillance of patients with Barrett’s esophagus. Incidence of dysplasia and adenocarcinoma: a prospective study. Am J Gastroenterol. 2003;98:1931–1939.

    Article  PubMed  Google Scholar 

  26. Enzinger P, Mayer R. Esophageal Cancer. N Engl J Med. 2003;349:2241–2252.

    Article  PubMed  CAS  Google Scholar 

  27. Brown LM, Silverman DT, Pottern LM, et al. Adenocarcinomas of the esophagus and esophagogastric junction in white men in the United States: alcohol, tobacco, an socioeconomic factors. Cancer Causes Control. 1994;5:333–340.

    Article  PubMed  CAS  Google Scholar 

  28. Gammon MD, Schoenberg JB, Ahsan H, et al. Tobacco, alcohol, and socioeconomic status and adenocarcinomas of the esophagus and gastric cardia. J Natl Can Inst. 1997;89:1277–1284.

    Article  CAS  Google Scholar 

  29. Kabat GC, Ng SK, Wynder EL. Tobacco, alcohol intake, and diet in relation to adenocarcinoma of the esophagus and gastric cardia. Cancer Causes Control. 1993;4:123–132.

    Article  PubMed  CAS  Google Scholar 

  30. Vaughan TL, Davis S, Kristal AR, Thomas DB. Obesity, alcohol, and tobacco as risk factors for cancers of the esophagus and gastric cardia: adenocarcinoma versus squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 1995;4:85–92.

    PubMed  CAS  Google Scholar 

  31. Wu AH, Wan P, Bernstein L. A multiethnic population-based study of smoking, alcohol and body size and risk of adenocarcinomas of the stomach and esophagus. Cancer Causes Control. 2001;12:721–732.

    Article  PubMed  CAS  Google Scholar 

  32. Veugelers P, Porter G, Guernsey F, Casson A. Obesity and lifestyle risk factors for gastroesophageal reflux disease, Barrett esophagus and esophageal adenocarcinoma. Dis Esophagus. 2006;19:321–328.

    Article  PubMed  CAS  Google Scholar 

  33. Edelstein Z, Farrow DC, Bronner M, Rosen S, Vaughan TL. Central adiposity and risk of Barrett’s esophagus. Gastroenterology. 2007;133:403–411.

    Article  PubMed  Google Scholar 

  34. Hirota WK, Loughney TM, Lazas DJ, Maydonovitch CL, Rholl V, Wong RK. Specialized intestinal metaplasia, dysplasia, and cancer of the esophagus and esophagogastric junction: prevalence and clinical data. Gastroenterology. 1999;116:277–285.

    Article  PubMed  CAS  Google Scholar 

  35. Kulig M, Nocon M, Vieth M, et al. Risk factors of gastroesophageal reflux disease: methodology and first epidemiological results of the ProGERD study. J Clin Epidemiol. 2004;57:580–589.

    Article  PubMed  CAS  Google Scholar 

  36. Ronkainen J, Aro P, Storskrubb T, et al. Prevalence of Barrett’s esophagus in the general population: an endoscopic study. Gastroenterology. 2005;129:1825–1831.

    Article  PubMed  Google Scholar 

  37. Edelstein ZR, Bronner MP, Rosen SN, Vaughan TL. Risk factors for Barrett’s esophagus among patients with gastroesophageal reflux disease: a community clinic-based case-control study. Am J Gastroenterol. 2009;104:834–842.

    Article  PubMed  Google Scholar 

  38. Smith KJ, O’Brien SM, Green AC, Webb PM, Whiteman DC. Current and past smoking significantly increase risk for Barrett’s esophagus. Clin Gastroenterol Hepatol. 2009;7:840–848.

    Article  PubMed  Google Scholar 

  39. Anderson LA, Watson RG, Murphy SJ, et al. Risk factors for Barrett’s oesophagus and oesophageal adenocarcinoma: results from the FINBAR study. World J Gastroenterol. 2007;13:1585–1594.

    PubMed  Google Scholar 

  40. Conio M, Filiberti R, Blanchi S, et al. Risk factors for Barrett’s esophagus: a case-control study. Int J Cancer. 2002;97:225–229.

    Article  PubMed  CAS  Google Scholar 

  41. Kubo A, Levin T, Block G, et al. Dietary antioxidants, fruits, and vegetables and the risk of Barrett’s esophagus. Am J Gastroenterol. 2008;103:1614–1623.

    Article  PubMed  CAS  Google Scholar 

  42. Johansson J, Hakansson HO, Mellblom L, et al. Risk factors for Barrett’s oesophagus: a population-based approach. Scand J Gastroenterol. 2007;42:148–156.

    Article  PubMed  Google Scholar 

  43. Smith KJ, O’Brien SM, Smithers BM, et al. Interactions among smoking, obesity, and symptoms of acid reflux in Barrett’s esophagus. Cancer Epidemiol Biomarkers Prev. 2005;14:2481–2486.

    Article  PubMed  Google Scholar 

  44. Al-Delaimy WK, Willett WC. Measurement of tobacco smoke exposure: comparison of toenail nicotine biomarkers and self-reports. Cancer Epidemiol Biomarkers Prev. 2008;17:1255–1261.

    Article  PubMed  CAS  Google Scholar 

  45. Rimm EB, Stampfer MJ, Colditz GA, Chute CG, Litin LB, Willett WC. Validity of self-reported waist and hip circumferences in men and women. Epidemiology. 1990;1:466–473.

    Article  PubMed  CAS  Google Scholar 

  46. Wolf AM, Hunter DJ, Colditz GA, et al. Reproducibility and validity of a self-administered physical activity questionnaire. Int J Epidemiol. 1994;23:991–999.

    Article  PubMed  CAS  Google Scholar 

  47. Willett WC, Sampson L. M.J. S. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol. 1985;122:51–65.

    PubMed  CAS  Google Scholar 

  48. Jacobson B, Moy B, Colditz GA, Fuchs CS. Postmenopausal hormone use and symptoms of gastroesophageal reflux. Arch Intern Med. 2008;168:1–7.

    Article  Google Scholar 

  49. Jacobson BC, Somers SC, Fuchs CS, Kelly CP, Camargo CA Jr. Body-mass index and symptoms of gastroesophageal reflux in women. N Engl J Med. 2006;354:2340–2348.

    Article  PubMed  CAS  Google Scholar 

  50. Colditz G, Stampfer M, Willett W, Stason W, Rosner B, Hennekens CH. Reproducibility and validity of self-reported menopausal status in a prospective cohort study. Am J Epidemiol. 1987;126:319–325.

    PubMed  CAS  Google Scholar 

  51. Fuchs CS, Colditz GA, Stampfer MJ, et al. A prospective study of cigarette smoking and the risk of pancreatic cancer. Arch Intern Med. 1996;156:2255–2260.

    Article  PubMed  CAS  Google Scholar 

  52. Riffenburgh R. Statistics in Medicine. 2nd ed. ed. San Diego: Academic Press; 2005.

    Google Scholar 

  53. Adams P, Schoenborn C. Health behaviors of adults: United States, 2002-04.2006.

  54. Kubo A, Levin TR, Block G, et al. Cigarette smoking and the risk of Barrett’s esophagus. Cancer Causes Control. 2009;20:303–311.

    Article  PubMed  Google Scholar 

  55. Calkins BM. A meta-analysis of the role of smoking in inflammatory bowel disease. Dig Dis Sci. 1989;34:1841–1854.

    Article  PubMed  CAS  Google Scholar 

  56. Kornbluth A, Sachar DB. Ulcerative colitis practice guidelines in adults: American College Of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol. 2010;105:501–523. doi:10.1038/ajg.2009.727. (quiz 24).

    Article  PubMed  Google Scholar 

  57. McGrath J, McDonald J, MacDonald J. Transdermal nicotine for induction of remission in ulcerative colitis. Cochrane Database Syst Rev 2004. doi:10.1002/14651858.CD004722.pub2.

  58. Olliver J, Hardie L, Gong Y, et al. Risk factors, DNA damage, and disease progression in Barrett’s esophagus. Cancer Epidemiol Biomarkers Prev. 2005;14:620–625.

    Article  PubMed  CAS  Google Scholar 

  59. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr. 2001;131:3109S–3120S.

    PubMed  CAS  Google Scholar 

  60. Giovannucci E, Pollak MN, Platz EA, et al. A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer Epidemiol Biomarkers Prev. 2000;9:345–349.

    PubMed  CAS  Google Scholar 

  61. Chiuve S, Rexrode K, Spiegelman D, Logroscino G, Manson J, Rimm E. Primary prevention of stroke by healthy lifestyle. Circulation. 2008;118:947–954.

    Article  PubMed  Google Scholar 

  62. Goldhaber S, Grodstein F, Stampfer M, et al. A prospective study of risk factors for pulmonary embolism in women. JAMA. 1997;277:642–645.

    Article  PubMed  CAS  Google Scholar 

  63. Meza R, Hazelton W, Colditz G, Moolgavkar S. Analysis of lung cancer incidence in the Nurses’ Health and the Health Professionals’ Follow-Up Studies using a multistage carcinogenesis model. Cancer Causes Control. 2008;19:317–328.

    Article  PubMed  Google Scholar 

  64. Chan A, Tranah G, Giovannucci E, Willett W, Hunter D, Fuchs C. Prospective study of N-acetyltransferase-2 genotypes, meat intake, smoking and risk of colorectal cancer. Int J Cancer. 2005;115:648–652.

    Article  PubMed  CAS  Google Scholar 

  65. McGrath M, Wong J, Michaud D, Hunter D, De Vivo I. Telomere length, cigarette smoking, and bladder cancer risk in men and women. Cancer Epidemiol Biomarkers Prev. 2007;16:815–819.

    Article  PubMed  CAS  Google Scholar 

  66. Heidemann C, Sun Q, van Dam RM, et al. Total and high-molecular-weight adiponectin and resistin in relation to the risk for type 2 diabetes in women. Ann Intern Med. 2008;149:307–316.

    PubMed  Google Scholar 

  67. Kenfield S, Stampfer M, Rosner B, Colditz G. Smoking and smoking cessation in relation to mortality in women. JAMA. 2008;299:2037–2047.

    Article  PubMed  CAS  Google Scholar 

  68. Corley DA, Kubo A, Levin T, et al. Abdominal obesity and body mass index as risk factors for Barrett’s esophagus. Gastroenterology. 2007;133:34–41.

    Article  PubMed  Google Scholar 

  69. Corley DA, Kubo A, DeBoer J, Rumore GJ. Diagnosing Barrett’s esophagus: reliability of clinical and pathologic diagnoses. Gastrointest Endosc. 2009;69:1004–1010.

    Article  PubMed  Google Scholar 

  70. Wang K, Sampliner R. Updated Guidelines 2008 for the diagnosis, surveillance, and therapy of Barrett’s esophagus. Am J Gastroenterol. 2008;103:788–797.

    Article  PubMed  Google Scholar 

  71. Spechler SJ. The role of gastric carditis in metaplasia and neoplasia at the gastroesophageal junction. Gastroenterology. 1999;117:218–228.

    Article  PubMed  CAS  Google Scholar 

  72. Playford RJ. New British Society of Gastroenterology (BSG) guidelines for the diagnosis and management of Barrett’s oesophagus. Gut. 2006;55:442.

    Article  PubMed  CAS  Google Scholar 

  73. Kahrilas P, Shaheen NJ, Vaezi MF. American Gastroenterological Association medical position statement on the management of gastroesophageal reflux disease. Gastroenterology. 2008;135:1383–1391.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The Nurses’ Health Study is funded by the National Cancer Institute program project grant CA087969. Dr Jacobson was funded by a grant from the National Institutes of Diabetes and Digestive and Kidney Diseases (RO1DK088782). None of the authors has any other financial disclosures.

Author information

Authors and Affiliations

  1. Section of Gastroenterology, Department of Medicine, Boston University Medical Center, 85 East Concord Street, Room 7721, Boston, MA, 02118, USA

    Brian C. Jacobson

  2. Boston University School of Medicine, Boston, MA, USA

    Brian C. Jacobson

  3. Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA

    Edward L. Giovannucci

  4. Department of Nutrition, Harvard School of Public Health, Boston, MA, USA

    Edward L. Giovannucci

  5. Cancer Epidemiology Program, Dana-Farber and Harvard Cancer Center, Boston, MA, USA

    Charles S. Fuchs

  6. Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA

    Charles S. Fuchs

  7. Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Edward L. Giovannucci & Charles S. Fuchs

Authors
  1. Brian C. Jacobson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edward L. Giovannucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Charles S. Fuchs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian C. Jacobson.

Additional information

The sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript. The content is solely the responsibility of the authors and should not be constituted to represent the official views of the National Institute of Diabetes and Digestive and Kidney Diseases or the National Institutes of Health.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jacobson, B.C., Giovannucci, E.L. & Fuchs, C.S. Smoking and Barrett’s Esophagus in Women Who Undergo Upper Endoscopy. Dig Dis Sci 56, 1707–1717 (2011). https://doi.org/10.1007/s10620-011-1672-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-011-1672-4

Keywords

Search

Navigation