Surveillance in Barrett’s Oesophagus: Will a Strategy Focused on a High-Risk Group Reduce Mortality from Oesophageal Adenocarcinoma?

Background and Study Aims: The incidence of oesophageal adenocarcinoma has increased significantly in recent years. While surveillance of people with Barrett’s oesophagus, its usual precursor, has been advocated in order to detect dysplasia and early cancer in those considered to be at greatest risk, the impact of such a strategy on survival from oesophageal adenocarcinoma is unclear. This study aimed to determine the effect of surveillance on mortality from oesophageal adenocarcinoma in a group of patients considered to be at high risk of developing Barrett’s oesophagus and adenocarcinoma.
Patients and Methods: After performing a Medline search of the literature published between 1985 and 2004 for studies on gastro-oesophageal reflux disease, Barrett’s oesophagus and adenocarcinoma, we examined the impact of surveillance on mortality from oesophageal adenocarcinoma in a hypothetical sample of 100 high-risk patients (men aged over 50 with Barrett’s oesophagus but without high-grade dysplasia at entry).
Results: Four patients in this high-risk group developed adenocarcinoma during surveillance, with survival rates of 78.9 % (95 %CI 64.9 % - 88.5 %) at 2 years and 78.6 % (95 %CI 62.8 % - 89.2 %) at 5 years. Meanwhile, between 515 and 2060 patients with Barrett’s oesophagus were not detected or surveyed by this strategy and between 16 and 61 of these developed adenocarcinoma, with much lower survival rates of 37.1 % (95 %CI 25.4 % - 50.3 %) at 2 years and 16.7 % (95 %CI 9 % - 28.3 %) at 5 years. Although surveillance in the high-risk group resulted in the long-term survival of three patients who would not otherwise have survived, this gain was dramatically offset by the 13 to 51 patients, excluded from surveillance by this strategy, who died from oesophageal adenocarcinoma.
Conclusions: A surveillance programme based on current concepts of risk cannot have an impact on mortality from oesophageal adenocarcinoma. To be effective, it will be necessary for surveillance programmes to utilise more precise methods for the identification of those who are most at risk of progression to adenocarcinoma.

References

• 1 Williamson W A, Ellis F H Jr, Gibb S P. et al . Barrett’s esophagus. Prevalence and incidence of adenocarcinoma.  Arch Intern Med. 1991;  151 2212-2216
• 2 Spechler S J. Clinical practice: Barrett’s esophagus.  N Engl J Med. 2002;  346 836-842
• 3 Jankowski J A, Wright N A, Meltzer S J. et al . Molecular evolution of the metaplasia-dysplasia-adenocarcinoma sequence in the esophagus.  Am J Pathol. 1999;  154 965-973
• 4 Jankowski J A, Harrison R F, Perry I. et al . Barrett’s metaplasia.  Lancet. 2000;  356 2079-2085
• 5 Reid B J. Barrett’s esophagus and esophageal adenocarcinoma.  Gastroenterol Clin North Am. 1991;  20 817-834
• 6 Theisen J, Nigro J J, DeMeester T R. et al . Chronology of the Barrett’s metaplasia-dysplasia-carcinoma sequence.  Dis Esophagus. 2004;  17 67-70
• 7 Shaheen N J, Crosby M A, Bozymski E M, Sandler R S. Is there publication bias in the reporting of cancer risk in Barrett’s esophagus?.  Gastroenterology. 2000;  119 333-338
• 8 Devesa S S, Blot W J, Fraumeni J F Jr. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States.  Cancer. 1998;  83 2049-2053
• 9 Sampliner R E. Updated guidelines for the diagnosis, surveillance, and therapy of Barrett’s esophagus. Practice Parameters Committee of the American College of Gastroenterology.  Am J Gastroenterol. 2002;  97 1888-1895
• 10 Dulai G S, Guha S, Kahn K L. et al . Preoperative prevalence of Barrett’s esophagus in esophageal adenocarcinoma: a systematic review.  Gastroenterology. 2002;  122 26-33
• 11 Lagergren J, Bergstrom R, Lindgren A, Nyren O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma.  N Engl J Med. 1999;  340 825-831
• 12 Fleiss J L. Statistical methods for rates and proportions. New York; John Wiley & Sons 1981
• 13 Hirota W K, Loughney T M, Lazas D J. et al . Specialized intestinal metaplasia, dysplasia, and cancer of the esophagus and esophagogastric junction: prevalence and clinical data.  Gastroenterology. 1999;  116 277-285
• 14 Csendes A, Smok G, Burdiles P. et al . Prevalence of intestinal metaplasia according to the length of the specialized columnar epithelium lining the distal esophagus in patients with gastroesophageal reflux.  Dis Esophagus. 2003;  16 24-28
• 15 Cameron A J, Kamath P S, Carpenter H A. Barrett’s esophagus: the prevalence of short and long segments in reflux patients.  Gastroenterology. 1995;  108 A65
• 16 Cameron A J, Kamath P S, Carpenter H A. Prevalence of esophagus and intestinal metaplasia at the esophagogastric junction.  Gastroenterology. 1997;  112 A82
• 17 Chalasani N, Wo J M, Hunter J G, Waring J P. Significance of intestinal metaplasia in different areas of esophagus including esophagogastric junction.  Dig Dis Sci. 1997;  42 603-607
• 18 Rex D X, Cummings O W, Shaw M. et al . Screening for Barrett’s esophagus in colonoscopy patients with and without heartburn.  Gastroenterology. 2003;  125 1670-1677
• 19 Schnell T, Sontag S, Warner J. et al . Endoscopic screening for Barrett’s esophagus (BE), esophageal adenocarcinoma (AdCa) and other mucosal changes in ambulatory subjects with symptomatic gastroesophageal reflux (GER).  Gastroenterology. 1985;  88 1576
• 20 Winters C Jr, Spurlin T J, Chobanian S J. et al . Barrett’s esophagus: a prevalent, occult complication of gastroesophageal disease.  Gastroenterology. 1987;  92 118-124
• 21 Mann N S, Tsai M F, Nair P K. Barrett’s esophagus in patients with symptomatic reflux esophagitis.  Am J Gastroenterol. 1989;  84 1494-1496
• 22 Abo S R, Stevens P D, Abedi M. et al . Prevalence of short-segment Barrett’s epithelium in patients with gastroesophageal reflux disease.  Gastroenterology. 1995;  108 A43
• 23 Corder A P, Jones R H, Sadler G H. et al . Heartburn, oesophagitis and Barrett’s oesophagus in self-medicating patients in general practice.  Br J Clin Pract. 1996;  50 245-248
• 24 Robinson M, Earnest D, Rodriguez-Stanley S. et al . Heartburn requiring frequent antacid use may indicate significant illness.  Arch Intern Med. 1998;  158 2373-2376
• 25 Dietz J, Meurer L, Maffazzoni D R. et al . Intestinal metaplasia in the distal esophagus and correlation with symptoms of gastroesophageal reflux disease.  Dis Esophagus. 2003;  16 29-32
• 26 Morales T G, Sampliner R E, Bhattacharyya A. Intestinal metaplasia of the gastric cardia.  Am J Gastroenterol. 1997;  92 414-418
• 27 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
• 28 O’Connor J B, Falk G W, Ritcher J E. 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
• 29 Miros M, Kerlin P, Walker N. Only patients with dysplasia progress to adenocarcinoma in Barrett’s esophagus.  Gut. 1991;  32 1441-1446
• 30 Weston A P, Badr A S, Hassanein R S. Prospective multivariate analysis of clinical, endoscopic, and histological factors predictive of the development of Barrett’s multifocal high-grade dysplasia or adenocarcinoma.  Am J Gastroenterol. 1999;  94 3413-3419
• 31 Cameron A J, Lomboy C T. Barrett’s esophagus: age, prevalence, and extent of columnar epithelium.  Gastroenterology. 1992;  103 1241-1245
• 32 Macdonald C E, Wicks A C, Playford R J. Final results from 10 years cohort of patients undergoing surveillance for Barrett’s esophagus: observational study.  BMJ. 2000;  321 1252-1255
• 33 Murray L, Watson P, Johnston B. et al . Risk of adenocarcinoma in Barrett’s esophagus: population based study.  BMJ. 2003;  327 534-535
• 34 Gopal D V, Lieberman D A, Magaret N. et al . Risk factors for dysplasia in patients with Barrett’s esophagus (BE): results from a multicenter consortium.  Dig Dis Sci. 2003;  48 1537-1541
• 35 Weston A P, Banerjee S K, Sharma P. et al . p53 Protein overexpression in low grade dysplasia (LGD) in Barrett’s esophagus: inmunohistochemical marker predictive of progression.  Am J Gastroenterol. 2001;  96 1355-1362
• 36 Benipal P, Garewal H S, Sampliner R E. et al . Short segment Barrett’s esophagus: relationship of age with extent of intestinal metaplasia.  Am J Gastroenterol. 2001;  96 3084-3088
• 37 Hameeteman W, Tytgat G NJ, Houthoff H J, van den Tweel J G. Barrett’s esophagus: development of dysplasia and adenocarcinoma.  Gastroenterology. 1989;  96 1249-1256
• 38 Schnell T G, Sontag S J, Chejfec G. et al . Long-term nonsurgical management of Barrett’s esophagus with high-grade dysplasia.  Gastroenterology. 2001;  120 1607-1619
• 39 Lao C D, Simmons M, Syngal S. et al . Dysplasia in Barrett’s esophagus.  Cancer. 2004;  100 1622-1627
• 40 Cameron A J, Zinsmeister A R, Ballard D J, Carney J A. Prevalence of columnar-lined (Barrett’s) esophagus. Comparison of population-based clinical and autopsy findings.  Gastroenterology. 1990;  99 918-922
• 41 Prach A T, Macdonald T A, Hopwood D A, Johnston D A. Increasing incidence of Barrett’s esophagus: education, enthusiasm, or epidemiology?.  Lancet. 1997;  350 933
• 42 Montgomery E, Goldblum J R, Greenson J K. et al . Dysplasia as a predictive marker for invasive carcinoma in Barrett esophagus: a follow-up study based on 138 cases from a diagnostic variability study.  Hum Pathol. 2001;  32 379-388
• 43 Reid B J, Levine D S, Longton G. et al . Predictors of progression to cancer in Barrett’s esophagus: baseline histology and flow cytometry identify low- and high-risk patient subset.  Am J Gastroenterol. 2000;  95 1669-1676
• 44 Burdiles P, Csendes A, Smok G. et al . Progression from intestinal metaplasia to adenocarcinoma in Barrett’s esophagus: usefulness of endoscopic surveillance.  Rev Med Chil. 2003;  131 587-596
• 45 Skacel M, Petras R E, Gramlich T L. et al . The diagnosis of low-grade dysplasia in Barrett’s esophagus and its implications for disease progression.  Am J Gastroenterol. 2000;  95 3383-3387
• 46 Eckardt V F, Kanzler M D, Bernhard G. Life expectancy and cancer risk in patients with Barrett’s esophagus: a prospective controlled investigation.  Am J Med. 2001;  111 33-37
• 47 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
• 48 Sharma P, Morales T G, Bhattacharayya A. et al . Dysplasia in short-segment Barrett’s esophagus: a prospective 3-year follow-up.  Am J Gastroenterol. 1997;  92 2012-2016
• 49 Drewitz D J, Sampliner R E, Garewal H S. 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
• 50 Conio M, Cameron A J, 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 Wright T A, Gray M R, Morris A I. et al . Cost-effectiveness of detecting Barrett’s cancer.  Gut. 1996;  39 574-579
• 52 Robertson C S, Mayberry J F, Nicholson D A. et al . Value of endoscopic surveillance in the detection of neoplastic change in Barrett’s oesophagus.  Br J Surg. 1988;  75 760-763
• 53 Ovaska J, Miettinen M, Kivilaasko E. Adenocarcinoma arising in Barrett’s esophagus.  Dig Dis Sci. 1989;  34 1336-1339
• 54 Sampliner R E, Machel C, Fennerty M B. Prospective incidence of cancer in Barrett’s oesophagus.  Gastroenterology. 1991;  100 A153
• 55 Iftikhar S Y, James P D, Steele R J. et al . Length of Barrett’s oesophagus: an important factor in the development of dysplasia and adenocarcinoma.  Gut. 1992;  33 1155-1158
• 56 Ferraris R, Bonelli L, Conio M. et al . Incidence of Barrett’s adenocarcinoma in an Italian population: an endoscopic surveillance programme. Gruppo Operativo per lo Studio della Precancerosi Esopagee (GOSPE).  Eur J Gastroenterol Hepatol. 1997;  9 881-885
• 57 Levine D S, Haggitt R C, Blount P T. et al . An endoscopic biopsy protocol can differentiate high-grade dysplasia from early adenocarcinoma in Barrett’s esophagus.  Gastroenterology. 1993;  105 40-50
• 58 Peters J H, Clark G W, Ireland A P. et al . Outcome of adenocarcinoma arising in Barrett’s esophagus in endoscopically surveyed and nonsurveyed patients.  J Thorac Cardiovasc Surg. 1994;  108 813-821
• 59 Tseng E E, Wu T T, Yeo C J, Heitmiller R F. Barrett’s esophagus with high-grade dysplasia: surgical results and long-term outcome - an update.  J Gastrointest Surg. 2003;  7 164-170
• 60 Thomson B N, Cade R J. Oesophagectomy for early adenocarcinoma and dysplasia arising in Barrett’s oesophagus.  ANZ J Surg. 2003;  73 121-124
• 61 Reid B J, Weinstein W M, Lewin K J. et al . Endoscopic biopsy can detect high-grade dysplasia or early adenocarcinoma in Barrett’s esophagus without grossly recognizable neoplastic lesions.  Gastroenterology. 1988;  94 81-90
• 62 Nigro J J, Hagen J A, DeMeester T R. et al . Occult esophageal adenocarcinoma: extent of disease and implications for effective therapy.  Ann Surg. 1999;  230 433-440
• 63 Zaninotto G, Parenti A R, Ruol A. et al . Oesophageal resection for high-grade dysplasia in Barrett’s oesophagus.  Br J Surg. 2000;  87 1102-1105
• 64 Buttar N S, Wang K K, Sebo T J. et al . Extent of high-grade dysplasia in Barrett’s esophagus correlates with risk of adenocarcinoma.  Gastroenterology. 2001;  120 1630-1639
• 65 Heitmiller R F, Redmond M, Hamilton S R. Barrett’s esophagus with high-grade dysplasia: an indication for prophylactic esophagectomy.  Ann Surg. 1996;  224 66-71
• 66 Pellegrini C A, Pohl D. High-grade dysplasia in Barrett’s esophagus: surveillance or operation?.  J Gastrointest Surg. 2000;  4 131-134
• 67 Romagnoli R, Collard J M, Gustschow C. et al . Outcomes of dysplasia arising in Barrett’s esophagus: a dynamic view.  J Am Coll Surg. 2003;  197 365-371
• 68 van Sandick J W, van Lanschot J J, Kuiken B W. et al . Impact of endoscopic biopsy surveillance of Barrett’s oesophagus on pathological stage and clinical outcome of Barrett’s carcinoma.  Gut. 1998;  43 216-222
• 69 Incarbone R, Bonavina L, Saino G. et al . Outcome of esophageal adenocarcinoma detected during endoscopic biopsy surveillance for Barrett’s esophagus.  Surg Endosc. 2002;  16 263-266
• 70 Headrick J R, Nichols F C IIIrd, Miller D L. et al . High-grade esophageal dysplasia: long-term survival and quality of life after esophagectomy.  Ann Thorac Surg. 2002;  73 1697-1702
• 71 Rice T W, Falk G, Achkar E, Petras P E. Surgical management of high-grade dysplasia in Barrett’s esophagus.  Am J Gastroenterol. 1993;  88 1832-1836
• 72 Pera M, Trastek V F, Carpenter H A. et al . Barrett’s esophagus with high-grade dysplasia: an indication for esophagectomy?.  Ann Thorac Surg. 1992;  54 199-204
• 73 Edwards M J, Gable D R, Lentsch A B, Richardson J D. The rationale for esophagectomy as the optimal therapy for Barrett’s esophagus with high-grade dysplasia.  Ann Surg. 1996;  223 585-589
• 74 Altorki N K, Sunagawa M, Little A G, Skinner D B. High-grade dysplasia in the columnar-lined esophagus.  Am J Surg. 1991;  161 97-99
• 75 Menke-Pluymers M B, Schoute N W, Mulder A H. et al . Outcome of surgical treatment of adenocarcinoma in Barrett’s oesophagus.  Gut. 1992;  33 1454-1458
• 76 Corley D A, Levin T R, Habel L A. et al . Surveillance and survival in Barrett’s adenocarcinoma: a population-based study.  Gastroenterology. 2002;  122 633-640
• 77 Streitz J M Jr, Andrews C W Jr, Ellis F H Jr. Endoscopic surveillance of Barrett’s esophagus: does it help?.  J Thorac Cardiovasc Surg. 1993;  105 383-387
• 78 Cameron A J, Ott B J, Payne W S. The incidence of adenocarcinoma in columnar-lined epithelium (Barrett’s esophagus).  N Eng J Med. 1985;  313 857-859
• 79 Van der Veen A H, Dees J, Blankensteijn J D, Blankenstein M. Adenocarcinoma in Barrett’s esophagus: an overrated risk.  Gut. 1989;  30 14-18
• 80 Van der Burgh A, Dees J, Hop W C, van Blankenstein M. Oesophageal cancer is an uncommon cause of death in patients with Barrett’s oesophagus.  Gut. 1996;  39 5-8
• 81 Spechler S J, Barr H. Review article: screening and surveillance of Barrett’s oesophagus: what is a cost-effective framework?.  Aliment Pharmacol Ther. 2004;  19 (Suppl 1) 49-53
• 82 Anderson L A, Murray L J, Murphy S J. et al . Mortality in Barrett’s oesophagus: results from a population based study.  Gut. 2003;  52 1081-1084
• 83 Sharma P, McQuaid K, Dent J. et al . A critical review of the diagnosis and management of Barrett’s esophagus: the AGA Chicago workshop.  Gastroenterology. 2004;  127 310-330
• 84 Ramnath G, Bampton P. Surveillance for Barrett’s oesophagus: if you do it, do it properly.  Med J Aust. 2004;  180 139-140
• 85 Patti M G, Corvera C U, Glasgow R E, Way L W. A hospital’s annual rate of esophagectomy influences the operative mortality rate.  J Gastrointest Sug. 1998;  2 186-192
• 86 Swisher S G, Deford I, Merriman K W. et al . Effects of operative volume on morbidity, mortality, and hospital use after esophagectomy for cancer.  J Thorac Cardiovasc Surg. 2000;  19 1126-1132
• 87 Birkemeyer J D, Siewers A E, Finlayson E W. et al . Hospital volume and surgical mortality in the United States.  New Engl J Med. 2002;  346 1128-1137
• 88 Streitz J M Jr, Ellis F H Jr, Tilden R L, Erickson R V. Endoscopic surveillance of Barrett’s esophagus: a cost-effectiveness comparison with mammographic surveillance for breast cancer.  Am J Gastroenterol. 1998;  93 911-915
• 89 Provenzale D, Schmitt C, Wong J B. Barrett’s esophagus: a new look at surveillance based on emerging estimates of cancer risk.  Am J Gastroenterol. 1999;  94 2043-2053
• 90 Sonnenberg A, Soni A, Sampliner R E. Medical decision analysis of endoscopic surveillance of Barrett’s oesophagus to prevent oesophageal adenocarcinoma.  Aliment Pharmacol Ther. 2002;  16 41-50
• 91 Shaheen N J, Provenzale D, Sandler R S. Upper endoscopy as a screening and surveillance tool in esophageal adenocarcinoma: a review of the evidence.  Am J Gastroenterol. 2002;  97 1319-1327
• 92 Inadomi J M, Sampliner R, Lagergren J. et al . Screening and surveillance for Barrett’s esophagus in a high-risk group: a cost-utility analysis.  Ann Intern Med. 2003;  138 176-186
• 93 Eisen G M, Sandler R S, Murray S, Gottfried M. The relationship between gastroesophageal reflux disease and its complications with Barrett’s esophagus.  Am J Gastroenterol. 1997;  92 27-31
• 94 McManus D T, Olaru A, Meltzer S J. Biomarkers of esophageal adenocarcinoma and Barrett’s esophagus.  Cancer Res. 2004;  64 1561-1569
• 95 Faruqi S A, Arantes V, Bhutani M S. Barrett’s esophagus: current and future role of endosonography and optical coherence tomography.  Dis Esophagus. 2004;  17 118-123