Clinical Gastroenterology and Hepatology
Volume 8, Issue 3 , Pages 235-244 , March 2010

Risk of Esophageal Adenocarcinoma and Mortality in Patients With Barrett's Esophagus: A Systematic Review and Meta-analysis

  • Marjolein Sikkema

      Affiliations

    • Department of Gastroenterology and Hepatology, Erasmus MC – University Medical Center, Rotterdam, The Netherlands
    • Corresponding Author InformationReprint requests Address requests for reprints to: Marjolein Sikkema, MD, Department of Gastroenterology and Hepatology, Erasmus MC – University Medical Center Rotterdam, PO Box 2040, 3000 CA Rotterdam, The Netherlands. fax: (31) 10-7032793
  • ,
  • Pieter J.F. de Jonge

      Affiliations

    • Department of Gastroenterology and Hepatology, Erasmus MC – University Medical Center, Rotterdam, The Netherlands
  • ,
  • Ewout W. Steyerberg

      Affiliations

    • Department of Public Health, Erasmus MC – University Medical Center, Rotterdam, The Netherlands
  • ,
  • Ernst J. Kuipers

      Affiliations

    • Department of Gastroenterology and Hepatology, Erasmus MC – University Medical Center, Rotterdam, The Netherlands
    • Department of Internal Medicine, Erasmus MC – University Medical Center, Rotterdam, The Netherlands

References 

  1. Haggitt RC. Barrett's esophagus, dysplasia, and adenocarcinoma. Hum Pathol. 1994;25:982–993
  2. Hameeteman W, Tytgat GN, Houthoff HJ, et al. Barrett's esophagus: development of dysplasia and adenocarcinoma. Gastroenterology. 1989;96:1249–1256
  3. van der Burgh A, Dees J, Hop WC, et al. Oesophageal cancer is an uncommon cause of death in patients with Barrett's oesophagus. Gut. 1996;39:5–8
  4. Blot WJ, Devesa SS, Kneller RW, et al. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA. 1991;265:1287–1289
  5. Devesa SS, Blot WJ, Fraumeni JF. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer. 1998;83:2049–2053
  6. van Soest EM, Dieleman JP, Siersema PD, et al. Increasing incidence of Barrett's oesophagus in the general population. Gut. 2005;54:1062–1066
  7. Lund O, Kimose HH, Aagaard MT, et al. Risk stratification and long-term results after surgical treatment of carcinomas of the thoracic esophagus and cardia (A 25-year retrospective study). J Thorac Cardiovasc Surg. 1990;99:200–209
  8. Wang KK, Sampliner RE. Updated guidelines 2008 for the diagnosis, surveillance and therapy of Barrett's esophagus. Am J Gastroenterol. 2008;103:788–797
  9. Corley DA, Levin TR, Habel LA, et al. Surveillance and survival in Barrett's adenocarcinomas: a population-based study. Gastroenterology. 2002;122:633–640
  10. Dulai GS, Guha S, Kahn KL, et al. Preoperative prevalence of Barrett's esophagus in esophageal adenocarcinoma: a systematic review. Gastroenterology. 2002;122:26–33
  11. Conio M, Blanchi S, Lapertosa G, et al. 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
  12. Hage M, Siersema PD, van Dekken H, et al. Oesophageal cancer incidence and mortality in patients with long-segment Barrett's oesophagus after a mean follow-up of 12.7 years. Scand J Gastroenterol. 2004;39:1175–1179
  13. Provenzale D, Schmitt C, Wong JB. Barrett's esophagus: a new look at surveillance based on emerging estimates of cancer risk. Am J Gastroenterol. 1999;94:2043–2053
  14. Cameron AJ, Ott BJ, Payne WS. The incidence of adenocarcinoma in columnar-lined (Barrett's) esophagus. N Engl J Med. 1985;313:857–859
  15. Aldulaimi DM, Cox M, Nwokolo CU, et al. Barrett's surveillance is worthwhile and detects curable cancers (A prospective cohort study addressing cancer incidence, treatment outcome and survival). Eur J Gastroenterol Hepatol. 2005;17:943–950
  16. Shaheen NJ, Crosby MA, Bozymski EM, et al. Is there publication bias in the reporting of cancer risk in Barrett's esophagus?. Gastroenterology. 2000;119:333–338
  17. Cook MB, Wild CP, Everett SM, et al. Risk of mortality and cancer incidence in Barrett's esophagus. Cancer Epidemiol Biomarkers Prev. 2007;16:2090–2096
  18. Moayyedi P, Burch N, Akhtar-Danesh N, et al. Mortality rates in patients with Barrett's oesophagus. Aliment Pharmacol Ther. 2008;27:316–320
  19. Garside R, Pitt M, Somerville M, et al. Surveillance of Barrett's oesophagus: exploring the uncertainty through systematic review, expert workshop and economic modelling. Health Technol Assess. 2006;10:1–142iii–iv
  20. Anderson LA, Murray LJ, Murphy SJ, et al. Mortality in Barrett's oesophagus: results from a population based study. Gut. 2003;52:1081–1084
  21. Yousef F, Cardwell C, Cantwell MM, et al. The incidence of esophageal cancer and high-grade dysplasia in Barrett's esophagus: a systematic review and meta-analysis. Am J Epidemiol. 2008;168:237–249
  22. Thomas T, Abrams KR, De Caestecker JS, et al. Meta analysis: Cancer risk in Barrett's oesophagus. Aliment Pharmacol Ther. 2007;26:1465–1477
  23. Chang EY, Morris CD, Seltman AK, et al. The effect of antireflux surgery on esophageal carcinogenesis in patients with Barrett esophagus: a systematic review. Ann Surg. 2007;246:11–21
  24. Sutton AJ. Methods for meta-analysis in medical research. New York, NY: John Wiley; 2000;
  25. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560
  26. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–188
  27. Begg CB, DuMouchel W, Harris J, et al. Publication bias in meta-analysis: A Bayesian data-augmentation approach to account for issues exemplified in the passive smoking debate—comments and rejoinders. Statistical Science. 1997;12:241–250
  28. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634
  29. Spechler SJ, Robbins AH, Rubins HB, et al. Adenocarcinoma and Barrett's esophagus (An overrated risk?). Gastroenterology. 1984;87:927–933
  30. Robertson CS, Mayberry JF, Nicholson DA, et al. Value of endoscopic surveillance in the detection of neoplastic change in Barrett's oesophagus. Br J Surg. 1988;75:760–763
  31. Ovaska J, Miettinen M, Kivilaakso E. Adenocarcinoma arising in Barrett's esophagus. Dig Dis Sci. 1989;34:1336–1339
  32. Miros M, Kerlin P, Walker N. Only patients with dysplasia progress to adenocarcinoma in Barrett's oesophagus. Gut. 1991;32:1441–1446
  33. Williamson WA, Ellis FH, Gibb SP, et al. Barrett's esophagus (Prevalence and incidence of adenocarcinoma). Arch Intern Med. 1991;151:2212–2216
  34. Iftikhar SY, James PD, Steele RJ, et al. Length of Barrett's oesophagus: an important factor in the development of dysplasia and adenocarcinoma. Gut. 1992;33:1155–1158
  35. Attwood SE, Barlow AP, Norris TL, et al. Barrett's oesophagus: effect of antireflux surgery on symptom control and development of complications. Br J Surg. 1992;79:1050–1053
  36. Ortiz A, Martinez de Haro LF, Parrilla P, et al. Conservative treatment versus antireflux surgery in Barrett's oesophagus: long-term results of a prospective study. Br J Surg. 1996;83:274–278
  37. Wright TA, Gray MR, Morris AI, et al. Cost effectiveness of detecting Barrett's cancer. Gut. 1996;39:574–579
  38. Komorowski RA, Hogan WJ, Chausow DD. Barrett's ulcer: the clinical significance today. Am J Gastroenterol. 1996;91:2310–2313
  39. Sharma P, Morales TG, Bhattacharyya A, et al. Dysplasia in short-segment Barrett's esophagus: a prospective 3-year follow-up. Am J Gastroenterol. 1997;92:2012–2016
  40. Younes M, Ertan A, Lechago LV, et al. p53 Protein accumulation is a specific marker of malignant potential in Barrett's metaplasia. Dig Dis Sci. 1997;42:697–701
  41. Katz D, Rothstein R, Schned A, et al. The development of dysplasia and adenocarcinoma during endoscopic surveillance of Barrett's esophagus. Am J Gastroenterol. 1998;93:536–541
  42. Streitz JM, Ellis FH, Tilden RL, et al. Endoscopic surveillance of Barrett's esophagus: a cost-effectiveness comparison with mammographic surveillance for breast cancer. Am J Gastroenterol. 1998;93:911–915
  43. Schoenfeld P, Johnston M, Piorkowski M, et al. Effectiveness and patient satisfaction with nurse-directed treatment of Barrett's esophagus. Am J Gastroenterol. 1998;93:906–910
  44. Teodori L, Gohde W, Persiani M, et al. DNA/protein flow cytometry as a predictive marker of malignancy in dysplasia-free Barrett's esophagus: thirteen-year follow-up study on a cohort of patients. Cytometry. 1998;34:257–263
  45. Wilkinson SP, Biddlestone L, Gore S, et al. Regression of columnar-lined (Barrett's) oesophagus with omeprazole 40 mg daily: results of 5 years of continuous therapy. Aliment Pharmacol Ther. 1999;13:1205–1209
  46. Macdonald CE, Wicks AC, Playford RJ. Final results from 10 year cohort of patients undergoing surveillance for Barrett's oesophagus: observational study. BMJ. 2000;321:1252–1255
  47. Reid BJ, Levine DS, Longton G, et al. Predictors of progression to cancer in Barrett's esophagus: baseline histology and flow cytometry identify low- and high-risk patient subsets. Am J Gastroenterol. 2000;95:1669–1676
  48. Srinivasan R, Katz PO, Ramakrishnan A, et al. Maximal acid reflux control for Barrett's oesophagus: feasible and effective. Aliment Pharmacol Ther. 2001;15:519–524
  49. Eckardt VF, Kanzler G, Bernhard G. Life expectancy and cancer risk in patients with Barrett's esophagus: a prospective controlled investigation. Am J Med. 2001;111:33–37
  50. 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
  51. Rana PS, Johnston DA. Incidence of adenocarcinoma and mortality in patients with Barrett's oesophagus diagnosed between 1976 and 1986: implications for endoscopic surveillance. Dis Esophagus. 2000;13:28–31
  52. Fitzgerald RC, Saeed IT, Khoo D, et al. Rigorous surveillance protocol increases detection of curable cancers associated with Barrett's esophagus. Dig Dis Sci. 2001;46:1892–1898
  53. Spechler SJ, 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
  54. Parrilla P, Martinez de Haro LF, Ortiz A, et al. Long-term results of a randomized prospective study comparing medical and surgical treatment of Barrett's esophagus. Ann Surg. 2003;237:291–298
  55. Murray L, Watson P, Johnston B, et al. Risk of adenocarcinoma in Barrett's oesophagus: population based study. BMJ. 2003;327:534–535
  56. Hurschler D, Borovicka J, Neuweiler J, et al. Increased detection rates of Barrett's oesophagus without rise in incidence of oesophageal adenocarcinoma. Swiss Med Wkly. 2003;133:507–514
  57. Hillman LC, Chiragakis L, Clarke AC, et al. Barrett's esophagus: Macroscopic markers and the prediction of dysplasia and adenocarcinoma. J Gastroenterol Hepatol. 2003;18:526–533
  58. Solaymani-Dodaran M, Logan RF, West J, et al. Risk of oesophageal cancer in Barrett's oesophagus and gastro-oesophageal reflux. Gut. 2004;53:1070–1074
  59. Basu KK, Pick B, de Caestecker JS. Audit of a Barrett's epithelium surveillance database. Eur J Gastroenterol Hepatol. 2004;16:171–175
  60. Meining A, Ott R, Becker I, et al. The Munich Barrett follow up study: suspicion of Barrett's oesophagus based on either endoscopy or histology only--what is the clinical significance?. Gut. 2004;53:1402–1407
  61. Dulai GS, Shekelle PG, Jensen DM, et al. Dysplasia and risk of further neoplastic progression in a regional Veterans Administration Barrett's cohort. Am J Gastroenterol. 2005;100:775–783
  62. Murphy SJ, Dickey W, Hughes D, et al. Surveillance for Barrett's oesophagus: results from a programme in Northern Ireland. Eur J Gastroenterol Hepatol. 2005;17:1029–1035
  63. Oberg S, Wenner J, Johansson J, et al. Barrett esophagus: risk factors for progression to dysplasia and adenocarcinoma. Ann Surg. 2005;242:49–54
  64. Gladman L, Chapman W, Iqbal TH, et al. Barrett's oesophagus: an audit of surveillance over a 17-year period. Eur J Gastroenterol Hepatol. 2006;18:271–276
  65. Vieth M, Schubert B, Lang-Schwarz K, et al. Frequency of Barrett's neoplasia after initial negative endoscopy with biopsy: a long-term histopathological follow-up study. Endoscopy. 2006;38:1201–1205
  66. Sharma P, Falk GW, Weston AP, et al. Dysplasia and cancer in a large multicenter cohort of patients with Barrett's esophagus. Clin Gastroenterol Hepatol. 2006;4:566–572
  67. Olithselvan A, Gorard DA, McIntyre AS. A surveillance programme for Barrett's oesophagus in a UK general hospital. Eur J Gastroenterol Hepatol. 2007;19:305–309
  68. Gatenby PA, Caygill CP, Ramus JR, et al. Barrett's columnar-lined oesophagus: demographic and lifestyle associations and adenocarcinoma risk. Dig Dis Sci. 2008;53:1175–1185
  69. Musana AK, Resnick JM, Torbey CF, et al. Barrett's esophagus: incidence and prevalence estimates in a rural Mid-Western population. Am J Gastroenterol. 2008;103:516–524
  70. Martinek J, Benes M, Brandtl P, et al. Low incidence of adenocarcinoma and high-grade intraepithelial neoplasia in patients with Barrett's esophagus: a prospective cohort study. Endoscopy. 2008;40:711–716
  71. Bani-Hani K, Sue-Ling H, Johnston D, et al. Barrett's oesophagus: results from a 13-year surveillance programme. Eur J Gastroenterol Hepatol. 2000;12:649–654
  72. O'Connor JB, Falk GW, Richter JE. The incidence of adenocarcinoma and dysplasia in Barrett's esophagus: report on the Cleveland Clinic Barrett's Esophagus Registry. Am J Gastroenterol. 1999;94:2037–2042
  73. Drewitz DJ, Sampliner RE, Garewal HS. The incidence of adenocarcinoma in Barrett's esophagus: a prospective study of 170 patients followed 4.8 years. Am J Gastroenterol. 1997;92:212–215
  74. Solaymani-Dodaran M, Logan RF, West J, et al. Mortality associated with Barrett's esophagus and gastroesophageal reflux disease diagnoses—a population-based cohort study. Am J Gastroenterol. 2005;100:2616–2621
  75. Jankowski JA, Provenzale D, Moayyedi P. Esophageal adenocarcinoma arising from Barrett's metaplasia has regional variations in the west. Gastroenterology. 2002;122:588–590
  76. Overholt BF, Wang KK, Burdick JS, et al. Five-year efficacy and safety of photodynamic therapy with Photofrin in Barrett's high-grade dysplasia. Gastrointest Endosc. 2007;66:460–468
  77. Pech O, Behrens A, May A, et al. Long-term results and risk factor analysis for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma in Barrett's oesophagus. Gut. 2008;57:1200–1206

 This article has an accompanying continuing medical education activity on page e32. Learning Objectives—At the end of this activity, the learner should recognize the low risk of esophageal adenocarcinoma in Barrett's esophagus and appreciate that no randomized trials have compared surveillance to a no surveillance strategy.

 Conflict of interest The authors disclose no conflicts.

PII: S1542-3565(09)01045-3

doi: 10.1016/j.cgh.2009.10.010

Clinical Gastroenterology and Hepatology
Volume 8, Issue 3 , Pages 235-244 , March 2010