Risk of recurrence of Barrett’s esophagus after successful endoscopic therapy

Published:February 20, 2016DOI:https://doi.org/10.1016/j.gie.2016.02.009

      Background and Aims

      Previous estimates of incidence of intestinal metaplasia (IM) recurrence after achieving complete remission of IM (CRIM) through endoscopic therapy of Barrett's esophagus (BE) have varied widely. We performed a systematic review and meta-analysis of studies to estimate an accurate recurrence risk after CRIM.

      Methods

      We performed a systematic search of multiple literature databases through June 2015 to identify studies reporting long-term follow-up after achieving CRIM through endoscopic therapy. Pooled incidence rate (IR) of recurrent IM, dysplastic BE, and high-grade dysplasia (HGD)/esophageal adenocarcinoma (EAC) per person-year of follow-up after CRIM was estimated. Factors associated with recurrence were also assessed.

      Results

      We identified 41 studies that reported 795 cases of recurrence in 4443 patients over 10,427 patient-years of follow-up. This included 21 radiofrequency ablation studies that reported 603 cases of IM recurrence in 3186 patients over 5741 patient-years of follow-up. Pooled IRs of recurrent IM, dysplastic BE, and HGD/EAC after radiofrequency ablation were 9.5% (95% CI, 6.7-12.3), 2.0% (95% CI, 1.3-2.7), and 1.2% (95% CI, .8-1.6) per patient-year, respectively. When all endoscopic modalities were included, pooled IRs of recurrent IM, dysplastic BE, and HGD/EAC were 7.1% (95% CI, 5.6-8.6), 1.3% (95% CI, .8-1.7), and .8% (95% CI, .5-1.1) per patient-year, respectively. Substantial heterogeneity was noted. Increasing age and BE length were predictive of recurrence; 97% of recurrences were treated endoscopically.

      Conclusions

      The incidence of recurrence after achieving CRIM through endoscopic therapy was substantial. A small minority of recurrences were dysplastic BE and HGD/EAC. Hence, continued surveillance after CRIM is imperative. Additional studies with long-term follow-up are needed.

      Abbreviations:

      APC (argon plasma coagulation), BE (Barrett’s esophagus), CRIM (complete remission of intestinal metaplasia), DBE (dysplastic Barrett’s esophagus), EAC (esophageal adenocarcinoma), GEJ (gastroesophageal junction), HGD (high-grade dysplasia), IM (intestinal metaplasia), IR (incidence rate), NDBE (nondysplastic Barrett’s esophagus), PDT (photodynamic therapy), RFA (radiofrequency ablation)
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      References

        • Evans J.A.
        • Early D.S.
        • Fukami N.
        • et al.
        The role of endoscopy in Barrett's esophagus and other premalignant conditions of the esophagus.
        Gastrointest Endosc. 2012; 76: 1087-1094
        • Spechler S.J.
        • Sharma P.
        • Souza R.F.
        • et al.
        American Gastroenterological Association technical review on the management of Barrett's esophagus.
        Gastroenterology. 2011; 140: e18-e52
        • Blevins C.H.
        • Iyer P.G.
        Endoscopic therapy for Barrett's oesophagus.
        Best Pract Res Clin Gastroenterol. 2015; 29: 167-177
        • Shaheen N.J.
        • Sharma P.
        • Overholt B.F.
        • et al.
        Radiofrequency ablation in Barrett's esophagus with dysplasia.
        N Engl J Med. 2009; 360: 2277-2288
        • Phoa K.N.
        • van Vilsteren F.G.
        • Weusten B.L.
        • et al.
        Radiofrequency ablation vs endoscopic surveillance for patients with Barrett esophagus and low-grade dysplasia: a randomized clinical trial.
        JAMA. 2014; 311: 1209-1217
        • Overholt B.F.
        • Lightdale C.J.
        • Wang K.K.
        • et al.
        Photodynamic therapy with porfimer sodium for ablation of high-grade dysplasia in Barrett's esophagus: international, partially blinded, randomized phase III trial.
        Gastrointest Endosc. 2005; 62: 488-498
        • May A.
        • Gossner L.
        • Pech O.
        • et al.
        Local endoscopic therapy for intraepithelial high-grade neoplasia and early adenocarcinoma in Barrett's oesophagus: acute-phase and intermediate results of a new treatment approach.
        Eur J Gastroenterol Hepatol. 2002; 14: 1085-1091
        • Orman E.S.
        • Li N.
        • Shaheen N.J.
        Efficacy and durability of radiofrequency ablation for Barrett's Esophagus: Systematic review and meta-analysis.
        Clin Gastroenterol Hepatol. 2013; 11: 1245-1255
        • Orman E.S.
        • Kim H.P.
        • Bulsiewicz W.J.
        • et al.
        Intestinal metaplasia recurs infrequently in patients successfully treated for Barrett's esophagus with radiofrequency ablation.
        Am J Gastroenterol. 2013; 108: 187-195
        • Phoa K.N.
        • Pouw R.E.
        • Van Vilsteren F.G.
        • et al.
        Remission of Barrett's esophagus with early neoplasia 5 years after radiofrequency ablation with endoscopic resection: a Netherlands cohort study.
        Gastroenterology. 2013; 145: 96-104
        • Shaheen N.J.
        • Overholt B.F.
        • Sampliner R.E.
        • et al.
        Durability of radiofrequency ablation in Barrett's esophagus with dysplasia.
        Gastroenterology. 2011; 141: 460-468
        • Gupta M.
        • Iyer P.G.
        • Lutzke L.
        • et al.
        Recurrence of esophageal intestinal metaplasia after endoscopic mucosal resection and radiofrequency ablation of Barrett's esophagus: results from a US Multicenter Consortium.
        Gastroenterology. 2013; 145: 79-86
        • Madisch A.
        • Miehlke S.
        • Bayerdorffer E.
        • et al.
        Long-term follow-up after complete ablation of Barrett's esophagus with argon plasma coagulation.
        World J Gastroenterol. 2005; 11: 1182-1186
        • Vaccaro B.J.
        • Gonzalez S.
        • Poneros J.M.
        • et al.
        Detection of intestinal metaplasia after successful eradication of Barrett’s esophagus with radiofrequency ablation.
        Dig Dis Sci. 2011; 56: 1996-2000
        • Shue P.
        • Kataria R.
        • Pathikonda M.
        • et al.
        Factors associated with recurrence of Barrett’s esophagus after completion of radiofrequency ablation.
        Gastroenterology. 2013; 144 (S-697)
        • Higgins J.
        • Green S.
        Cochrane handbook for systematic reviews of interventions version 5.1. 0.
        The Cochrane Collaboration. 2011; 5
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • et al.
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        Ann Intern Med. 2009; 151: 264-269
        • Blevins C.
        • Gorospe E.C.
        • Devanna S.
        • et al.
        Outcomes of recurrent intestinal metaplasia following successful endotherapy of Barrett’s esophagus associated dysplasia.
        Gastrointest Endosc. 2014; 79 ([abstract]): AB396
        • Chandra S.
        • Gorospe E.C.
        • Leggett C.L.
        • et al.
        Durability of photodynamic therapy for barrett's dysplasia: a single center 20-year experience.
        Gastroenterology. 2013; 144 (S-692)
        • Gorospe E.
        • Tian J.
        • Dunagan K.
        • et al.
        Can a single EMR cure Barrett's dysplasia? Complete remission after a single endoscopic mucosal resection with negative margins 2011 ACG Presidential Poster.
        Am J Gastroenterol. 2011; 106: S12-S13
        • van Vilsteren F.G.
        • Pouw R.E.
        • Seewald S.
        • et al.
        Stepwise radical endoscopic resection versus radiofrequency ablation for Barrett's oesophagus with high-grade dysplasia or early cancer: a multicentre randomised trial.
        Gut. 2011; 60: 765-773
        • Dulai P.S.
        • Pohl H.
        • Levenick J.M.
        • et al.
        Radiofrequency ablation for long-and ultralong-segment Barrett's esophagus: a comparative long-term follow-up study.
        Gastrointest Endosc. 2013; 77: 534-541
        • Stang A.
        Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses.
        Eur J Epidemiol. 2010; 25: 603-605
        • DerSimonian R.
        • Laird N.
        Meta-analysis in clinical trials.
        Control Clin Trials. 1986; 7: 177-188
        • Guyatt G.H.
        • Oxman A.D.
        • Kunz R.
        • et al.
        GRADE guidelines: 7. Rating the quality of evidence—inconsistency.
        J Clin Epidemiol. 2011; 64: 1294-1302
        • Easterbrook P.J.
        • Gopalan R.
        • Berlin J.
        • et al.
        Publication bias in clinical research.
        Lancet. 1991; 337: 867-872
        • Akiyama J.
        • Roorda A.K.
        • Marcus S.N.
        • et al.
        Erosive esophagitis is a major predictor for recurrence of barrett's esophagus after successful radiofrequency ablation.
        Gastroenterology. 2013; 144: S-692
        • Allison H.
        • Banchs M.A.
        • Bonis P.A.
        • et al.
        Long-term remission of nondysplastic Barrett's esophagus after multipolar electrocoagulation ablation: report of 139 patients with 10 years of follow-up.
        Gastrointest Endosc. 2011; 73: 651-658
        • Cameron G.
        • Jayasekera C.
        • Williams R.
        • et al.
        Victorian Barrett's experience: outcomes of patients undergoing combination endoscopic therapy for dysplastic Barrett's oesophagus.
        J Gastroenterol Hepatol. 2012; 27: 53-57
        • Choi K.D.
        Clinical outcomes of patients with Barrett’s esophagus treated with radiofrequency ablation using only the focal device.
        Am J Gastroenterol. 2013; 108: S4
        • Conio M.
        • Fisher D.A.
        • Blanchi S.
        • et al.
        One-step circumferential endoscopic mucosal cap resection of Barrett's esophagus with early neoplasia.
        Clin Res Hepatol Gastroenterol. 2014; 38: 81-91
        • Cotton C.C.
        • Wolf W.A.
        • Pasricha S.
        • et al.
        Recurrent intestinal metaplasia after radiofrequency ablation for Barrett’s esophagus: endoscopic findings and anatomic location.
        Gastrointest Endosc. 2015; 81: 1362-1369
        • Familiari L.
        • Scaffidi M.
        • Bonica M.
        • et al.
        Endoscopic treatment of Barrett's epithelium with argon plasma coagulation. Long-term follow-up.
        Min Gastroenterol Dietol. 2003; 49: 63-70
        • Ferraris R.
        • Fracchia M.
        • Foti M.
        • et al.
        Barrett’s oesophagus: long-term follow-up after complete ablation with argon plasma coagulation and the factors that determine its recurrence.
        Aliment Pharmacol Therap. 2007; 25: 835-840
        • Fisher R.S.
        • Bromer M.Q.
        • Thomas R.M.
        • et al.
        Predictors of recurrent specialized intestinal metaplasia after complete laser ablation.
        Am J Gastroenterol. 2003; 98: 1945-1951
        • Gad Y.Z.
        • Zeid A.A.
        The role of argon plasma coagulation in the management of Barrett's esophagus: a single-center experience.
        Gastrointest Cancer Targets Ther. 2011; 1: 21-26
        • Gerke H.
        • Siddiqui J.
        • Nasr I.
        • et al.
        Efficacy and safety of EMR to completely remove Barrett's esophagus: experience in 41 patients.
        Gastrointest Endosc. 2011; 74: 761-771
        • Goldberg M.E.
        • Horwhat D.
        • Cash B.D.
        Long-term analysis of outcomes associated with endoscopic spray cryotherapy for Barrett’s esophagus with and without dysplasia.
        Gastrointest Endosc. 2012; 75 ([anstract]): AB463
        • Gupta N.
        • Wani S.
        • Hollander T.G.
        • et al.
        Recurrence of disease after endoscopic eradication therapy (EET) for Barrett's esophagus (BE) with high grade dysplasia (HGD) and early cancer (EC).
        Gastroenterology. 2012; 142 (S-750-1)
        • Haidry R.J.
        • Banks M.R.
        • Gupta A.
        • et al.
        Five year outcomes for patients undergoing endoscopic therapy for Barrett's related neoplasia from the United Kingdom's largest single centre experience.
        Gastrointest Endosc. 2014; 79 ([abstract]): AB497
        • Johnson C.S.
        • Louie B.E.
        • Wille A.
        • et al.
        The durability of endoscopic therapy for treatment of Barrett’s metaplasia, dysplasia, and mucosal cancer after nissen fundoplication.
        J Gastrointest Surg. 2015; 19: 799-805
        • Konda V.J.
        • Ruiz M.G.H.
        • Koons A.
        • et al.
        Complete endoscopic mucosal resection is effective and durable treatment for Barrett's-associated neoplasia.
        Clin Gastroenterol Hepatol. 2014; 12: 2002-2010
        • Korst R.J.
        • Santana-Joseph S.
        • Rutledge J.R.
        • et al.
        Patterns of recurrent and persistent intestinal metaplasia after successful radiofrequency ablation of Barrett’s esophagus.
        J Thorac Cardiovasc Surg. 2013; 145: 1529-1534
        • Larghi A.
        • Lightdale C.
        • Ross A.
        • et al.
        Long-term follow-up of complete Barrett's eradication endoscopic mucosal resection (CBE-EMR) for the treatment of high grade dysplasia and intramucosal carcinoma.
        Endoscopy. 2007; 39: 1086-1091
        • Mörk H.
        • Al-Taie O.
        • Berlin F.
        • et al.
        High recurrence rate of Barrett's epithelium during long-term follow-up after argon plasma coagulation.
        Scand J Gastroenterol. 2007; 42: 23-27
        • Pagani M.
        • Granelli P.
        • Chella B.
        • et al.
        Barrett's esophagus: combined treatment using argon plasma coagulation and laparoscopic antireflux surgery.
        Dis Esoph. 2003; 16: 279-283
        • Pasricha S.
        • Bulsiewicz W.J.
        • Hathorn K.E.
        • et al.
        Durability and predictors of successful radiofrequency ablation for Barrett’s esophagus.
        Clin Gastroenterol Hepatol. 2014; 12: 1840-1847
        • Pedrazzani C.
        • Catalano F.
        • Festini M.
        • et al.
        Endoscopic ablation of Barrett's esophagus using high power setting argon plasma coagulation: a prospective study.
        World J Gastroenterol. 2005; 11: 1872-1875
        • Phoa K.N.
        • Pouw R.E.
        • Bisschops R.
        • et al.
        Multimodality endoscopic eradication for neoplastic Barrett oesophagus: results of a European multicentre study (EURO-II).
        Gut. 2016; 65: 555-562
        • Pouw R.E.
        • Seewald S.
        • Gondrie J.J.
        • et al.
        Stepwise radical endoscopic resection for eradication of Barrett's oesophagus with early neoplasia in a cohort of 169 patients.
        Gut. 2010; 59: 1169-1177
        • Pouw R.E.
        • Wirths K.
        • Eisendrath P.
        • et al.
        Efficacy of radiofrequency ablation combined with endoscopic resection for Barrett's esophagus with early neoplasia.
        Clin Gastroenterol Hepatol. 2010; 8: 23-29
        • Schulz H.
        • Miehlke S.
        • Antos D.
        • et al.
        Ablation of Barrett's epithelium by endoscopic argon plasma coagulation in combination with high-dose omeprazole.
        Gastrointest Endosc. 2000; 51: 659-663
        • Strauss A.C.
        • Agoston A.T.
        • Dulai P.S.
        • et al.
        Radiofrequency ablation for Barrett’s-associated intramucosal carcinoma: a multi-center follow-up study.
        Surg Endosc. 2014; 28: 3366-3372
        • Wolf W.A.
        • Overholt B.F.
        • Li N.
        • et al.
        Durability of radiofrequency ablation (RFA) in Barrett's esophagus with dysplasia: the AIM Dysplasia Trial at five years.
        Gastroenterology. 2014; 5: S-131
        • Tian J.
        • Gorospe E.
        • Sun G.
        • et al.
        What should be the goal for Barrett's ablation: is elimination of dysplasia enough?.
        Am J Gastroenterol. 2011; 106: S26
        • Chandra S.
        • Gorospe E.C.
        • Leggett C.L.
        • et al.
        Durability of radiofrequency ablation for Barrett’s esophagus: a single center 10-year experience.
        Gastroenterology. 2013; 5: S-685
        • Gondrie J.
        • Pouw R.
        • Sondermeijer C.
        • et al.
        Effective treatment of early Barrett's neoplasia with stepwise circumferential and focal ablation using the HALO system.
        Endoscopy. 2008; 40: 370-379
        • Pereira-Lima J.C.
        • Busnello J.V.
        • Saul C.
        • et al.
        High power setting argon plasma coagulation for the eradication of Barrett's esophagus.
        Am J Gastroenterol. 2000; 95: 1661-1668
        • Herrero L.A.
        • van Vilsteren F.G.
        • Pouw R.E.
        • et al.
        Endoscopic radiofrequency ablation combined with endoscopic resection for early neoplasia in Barrett's esophagus longer than 10 cm.
        Gastrointest Endosc. 2011; 73: 682-690
        • Gondrie J.
        • Pouw R.
        • Sondermeijer C.
        • et al.
        Stepwise circumferential and focal ablation of Barrett's esophagus with high-grade dysplasia: results of the first prospective series of 11 patients.
        Endoscopy. 2008; 40: 359-369
        • Yassin B.
        • Kazemi S.
        • Kalaghchi B.
        Results of one year follow-up of RF ablation of dysplastic Barrett’s esophagus in community setting.
        Am J Gastroenterol. 2012; 107: S39-S40
        • Pinotti A.
        • Cecconello I.
        • Sakai P.
        • et al.
        Endoscopic ablation of Barrett's esophagus using argon plasma coagulation: a prospective study after fundoplication.
        Dis Esoph. 2004; 17: 243-246
        • Van Laethem J.-L.
        • Cremer M.
        • Peny M.-O.
        • et al.
        Eradication of Barrett’s mucosa with argon plasma coagulation and acid suppression: immediate and mid term results.
        Gut. 1998; 43: 747-751
        • Bonavina L.
        • Ceriani C.
        • Carazzone A.
        • et al.
        Endoscopic laser ablation of nondysplastic Barrett’s epithelium: is it worthwhile?.
        J Gastrointest Surg. 1999; 3: 194-199
        • Bowers S.
        • Mattear S.
        • Waring P.
        • et al.
        KTP laser ablation of Barrett's esophagus after anti-reflux surgery results in long-term loss of intestinal metaplasia.
        Surg Endosc Other Intervent Techn. 2003; 17: 49-54
        • Sharma P.
        • Bhattacharyya A.
        • Garewal H.S.
        • et al.
        Durability of new squamous epithelium after endoscopic reversal of Barrett’s esophagus.
        Gastrointest Endosc. 1999; 50: 159-164
        • Almond L.
        • Hodson J.
        • Barr H.
        Meta-analysis of endoscopic therapy for low-grade dysplasia in Barrett's oesophagus.
        Br J Surg. 2014; 101: 1187-1195
        • Small A.J.
        • Araujo J.L.
        • Leggett C.L.
        • et al.
        Radiofrequency ablation is associated with decreased neoplastic progression in patients with Barrett’s esophagus and confirmed low-grade dysplasia.
        Gastroenterology. 2015; 149: 567-576