Endoscopic submucosal dissection and endoscopic mucosal resection for Barrett’s-associated neoplasia: a systematic review and meta-analysis of the published literature

Abstract

Background The role of endoscopic submucosal dissection (ESD) in the treatment of Barrett esophagus-associated neoplasia (BEN) has been evolving. We examined the efficacy and safety of ESD and endoscopic mucosal resection (EMR) for BEN.

Methods A database search was performed for studies reporting efficacy and safety outcomes of ESD and EMR for BEN. Pooled proportional and comparative meta-analyses were performed.

Results 47 studies (23 ESD, 19 EMR, 5 comparative) were included. The mean lesion sizes for ESD and EMR were 22.5 mm and 15.8 mm, respectively; most lesions were Paris type IIa. For ESD, pooled analysis showed rates of en bloc, R0, and curative resection, and local recurrence of 98%, 78%, 65%, and 2%, respectively. Complete eradication of dysplasia and intestinal metaplasia were achieved in 94% and 59% of cases, respectively. Pooled rates of perforation, intraprocedural bleeding, delayed bleeding, and stricture were 1%, 1%, 2%, and 10%, respectively. For EMR, pooled analysis showed rates of en bloc, R0, and curative resection, and local recurrence of 37%, 67%, 62%, and 6%, respectively. Complete eradication of dysplasia and intestinal metaplasia were achieved in 94% and 75% of cases. Pooled rates of perforation, intraprocedural bleeding, delayed bleeding, and stricture were 0.1%, 1%, 0.4%, and 8%, respectively. The mean procedure times for ESD and EMR were 113 and 22 minutes, respectively. Comparative analysis showed higher en bloc and R0 resection rates with ESD compared with EMR, with comparable adverse events.

Conclusion ESD and EMR can both be employed to treat BEN depending on lesion type and size, and center expertise.

Publication History

Received: 21 September 2023

Accepted after revision: 28 June 2024

Accepted Manuscript online:
28 June 2024

Article published online:
09 September 2024

• References

• 1 Rubenstein JH, Shaheen NJ. Epidemiology, diagnosis, and management of esophageal adenocarcinoma. Gastroenterology 2015; 149: 302-317.e301
• 2 Fitzgerald RC. Molecular basis of Barrett's oesophagus and oesophageal adenocarcinoma. Gut 2006; 55: 1810-1820
• 3 Sharma P, Shaheen NJ, Katzka D. et al. AGA Clinical Practice Update on endoscopic treatment of Barrett's esophagus with dysplasia and/or early cancer: expert review. Gastroenterology 2020; 158: 760-769
• 4 Weusten B, Bisschops R, Dinis-Ribeiro M. et al. Diagnosis and management of Barrett esophagus: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2023; 55: 1124-1146
• 5 Shaheen NJ, Sharma P, Overholt BF. et al. Radiofrequency ablation in Barrett's esophagus with dysplasia. NEJM 2009; 360: 2277-2288
• 6 Yang D, King W, Aihara H. et al. Effect of endoscopic submucosal dissection on histologic diagnosis in Barrett's esophagus visible neoplasia. Gastrointest Endosc 2022; 95: 626-633
• 7 Podboy A, Kolahi KS, Friedland S. et al. Endoscopic submucosal dissection is associated with less pathologic uncertainty than endoscopic mucosal resection in diagnosing and staging Barrett's-related neoplasia. Dig Endosc 2020; 32: 346-354
• 8 Codipilly DC, Dhaliwal L, Oberoi M. et al. Comparative outcomes of cap assisted endoscopic resection and endoscopic submucosal dissection in dysplastic Barrett's esophagus. Clin Gastroenterol Hepatol 2022; 20: 65-73.e61
• 9 Forbes N, Elhanafi SE. ASGE Standards of Practice Committee. et al. American Society for Gastrointestinal Endoscopy guideline on endoscopic submucosal dissection for the management of early esophageal and gastric cancers: summary and recommendations. Gastrointest Endosc 2023; 98: 271-284
• 10 Pimentel-Nunes P, Libanio D, Bastiaansen BAJ. et al. Endoscopic submucosal dissection for superficial gastrointestinal lesions: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2022. Endoscopy 2022; 54: 591-622
• 11 Ishihara R, Arima M, Iizuka T. et al. Endoscopic submucosal dissection/endoscopic mucosal resection guidelines for esophageal cancer. Dig Endosc 2020; 32: 452-493
• 12 Bos V, Chan MW, Pouw RE. Towards personalized management of early esophageal adenocarcinoma. Curr Opin Gastroenterol 2024; 40: 299-304
• 13 Page MJ, McKenzie JE, Bossuyt PM. et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021; 372: n71
• 14 Desai M, Saligram S, Gupta N. et al. Efficacy and safety outcomes of multimodal endoscopic eradication therapy in Barrett's esophagus-related neoplasia: a systematic review and pooled analysis. Gastrointest Endosc 2017; 85: 482-495 e484
• 15 Team RC. R: A language and environment for statistical computing. Vienna; Austria: R Foundation for Statistical Computing;: 2022
• 16 McGrath S, Zhao X, Steele R. et al. Estimating the sample mean and standard deviation from commonly reported quantiles in meta-analysis. Stat Methods Med Res 2020; 29: 2520-2537
• 17 Bahdi F, Katti CC, Mansour N. et al. Outcomes of endoscopic submucosal dissection (ESD) plus radiofrequency ablation (RFA) for nodular Barrett's esophagus. Scand J Gastroenterol 2022; 58: 1-10
• 18 Barret M, Cao DT, Beuvon F. et al. Endoscopic submucosal dissection for early Barrett’s neoplasia. United European Gastroenterol J 2016; 4: 207-215
• 19 Chevaux JB, Piessevaux H, Jouret-Mourin A. et al. Clinical outcome in patients treated with endoscopic submucosal dissection for superficial Barrett's neoplasia. Endoscopy 2015; 47: 103-112
• 20 Coman RM, Gotoda T, Forsmark CE. et al. Prospective evaluation of the clinical utility of endoscopic submucosal dissection (ESD) in patients with Barrett's esophagus: A Western center experience. Endosc Int Open 2016; 4: E715-E721
• 21 Doumbe-Mandengue P, Beuvon F, Belle A. et al. Outcomes of endoscopic submucosal dissection for early esophageal and gastric cardia adenocarcinomas. Clin Res Hepatol Gastroenterol 2021; 45: 101700
• 22 Höbel S, Dautel P, Baumbach R. et al. Single center experience of endoscopic submucosal dissection (ESD) in early Barrett´s adenocarcinoma. Surg Endosc 2015; 29: 1591-1597
• 23 Hoteya S, Matsui A, Iizuka T. et al. Comparison of the clinicopathological characteristics and results of endoscopic submucosal dissection for esophagogastric junction and non-junctional cancers. Digestion 2013; 87: 29-33
• 24 Joseph A, Draganov PV, Maluf-Filho F. et al. Outcomes for endoscopic submucosal dissection of pathologically staged T1b esophageal cancer: a multicenter study. Gastrointest Endosc 2022; 96: 445-453
• 25 Joo DC, Kim GH, Lee BE. et al. Endoscopic submucosal dissection for superficial Barrett’s neoplasia in Korea: a single-center experience. J Gastric Cancer 2021; 21: 426-438
• 26 Kagemoto K, Oka S, Tanaka S. et al. Clinical outcomes of endoscopic submucosal dissection for superficial Barrett's adenocarcinoma. Gastrointest Endosc 2014; 80: 239-245
• 27 Mehta NA, Abe S, Vargo JJ. et al. Insulated-tip knife tunneling and c-shaped incision for esophageal endoscopic submucosal dissection: an initial Western experience. Techn Innov Gastrointest Endosc 2021; 23: 152-158
• 28 Motomura D, Bechara R. Single operator experience of endoscopic submucosal dissection for Barrett's neoplasia in a North American academic center. DEN Open 2022; 2: e81
• 29 Nagami Y, Machida H, Shiba M. et al. Clinical efficacy of endoscopic submucosal dissection for adenocarcinomas of the esophagogastric junction. Endosc Int Open 2014; 2: E15-E20
• 30 Neuhaus H, Terheggen G, Rutz EM. et al. Endoscopic submucosal dissection plus radiofrequency ablation of neoplastic Barretts esophagus. Endoscopy 2012; 44: 1105-1113
• 31 Osumi H, Fujisaki J, Omae M. et al. Clinicopathological features of Siewert type II adenocarcinoma: comparison of gastric cardia adenocarcinoma and Barrett’s esophageal adenocarcinoma following endoscopic submucosal dissection. Gastric Cancer 2017; 20: 663-670
• 32 Othman MO, Bahdi F, Ahmed Y. et al. Short-term clinical outcomes of non-curative endoscopic submucosal dissection for early esophageal adenocarcinoma. Eur J Gastroenterol Hepatol 2021; 33: e700-e708
• 33 Probst A, Ebigbo A, Märkl B. et al. Stricture prevention after extensive endoscopic submucosal dissection of neoplastic Barrett's esophagus: individualized oral steroid prophylaxis. Gastroenterol Res Pract 2019; 2019: 2075256
• 34 Probst A, Aust D, Märkl B. et al. Early esophageal cancer in Europe: Endoscopic treatment by endoscopic submucosal dissection. Endoscopy 2015; 47: 113-121
• 35 Shimizu T, Fujisaki J, Omae M. et al. Treatment outcomes of endoscopic submucosal dissection for adenocarcinoma originating from long-segment Barrett's esophagus versus short-segment Barrett's esophagus. Digestion 2018; 97: 316-323
• 36 Subramaniam S, Chedgy F, Longcroft-Wheaton G. et al. Complex early Barrett's neoplasia at 3 Western centers: European Barrett's Endoscopic Submucosal Dissection Trial (E-BEST). Gastrointest Endosc 2017; 86: 608-618
• 37 van Munster SN, Verheij EPD, Nieuwenhuis EA. et al. Extending treatment criteria for Barrett's neoplasia: results of a nationwide cohort of 138 endoscopic submucosal dissection procedures. Endoscopy 2022; 54: 531-541
• 38 Yang D, Coman RM, Kahaleh M. et al. Endoscopic submucosal dissection for Barrett's early neoplasia: a multicenter study in the United States. Gastrointest Endosc 2017; 86: 600-607
• 39 Brahmania M, Lam E, Telford J. et al. Endoscopic mucosal resection: early experience in British Columbia. Can J Gastroenterol 2010; 24: 239-244
• 40 Spadaccini M, Bhandari P, Maselli R. et al. Multi-band mucosectomy for neoplasia in patients with Barrett's esophagus: in vivo comparison between two different devices. Surg Endosc 2020; 34: 3845-3852
• 41 Pouw RE, Beyna T, Belghazi K. et al. A prospective multicenter study using a new multiband mucosectomy device for endoscopic resection of early neoplasia in Barrett's esophagus. Gastrointest Endosc 2018; 88: 647-654
• 42 Alzoubaidi D, Graham D, Bassett P. et al. Comparison of two multiband mucosectomy devices for endoscopic resection of Barrett's esophagus-related neoplasia. Surg Endosc 2019; 33: 3665-3672
• 43 Pouw RE, van Vilsteren FG, Peters FP. et al. Randomized trial on endoscopic resection-cap versus multiband mucosectomy for piecemeal endoscopic resection of early Barrett's neoplasia. Gastrointest Endosc 2011; 74: 35-43
• 44 Thomas T, Singh R, Ragunath K. Trimodal imaging-assisted endoscopic mucosal resection of early Barrett's neoplasia. Surg Endosc 2009; 23: 1609-1613
• 45 Peters FP, Kara MA, Curvers WL. et al. Multiband mucosectomy for endoscopic resection of Barrett's esophagus: feasibility study with matched historical controls. Eur J Gastroenterol Hepatol 2007; 19: 311-315
• 46 Shimamura Y, Iwaya Y, Kobayashi R. et al. Clinical and pathological predictors of failure of endoscopic therapy for Barrett's related high-grade dysplasia and early esophageal adenocarcinoma. Surg Endosc 2021; 35: 5468-5479
• 47 Pateria P, Chong A, Muwanwella N. et al. To investigate outcomes in endoscopic management of early oesophageal adenocarcinoma in Barrett oesophagus: experience at three Australian tertiary centres. Intern Med J 2022; 52: 633-639
• 48 White JR, Ortiz-Fernandez-Sordo J, Santiago-Garcia J. et al. Endoscopic management of Barrett's dysplasia and early neoplasia: efficacy, safety and long-term outcomes in a UK tertiary centre. Eur J Gastroenterol Hepatol 2021; 33: e413-e422
• 49 Hasan Y, Murali AR, Gerke H. Endoscopic mucosal resection for early esophageal carcinoma is effective and safe but necessitates continued surveillance. Indian J Gastroenterol 2020; 39: 487-494
• 50 Barret M, Belghazi K, Weusten BL. et al. Single-session endoscopic resection and focal radiofrequency ablation for short-segment Barrett's esophagus with early neoplasia. Gastrointest Endosc 2016; 84: 29-36
• 51 Agoston AT, Strauss AC, Dulai PS. et al. Predictors of treatment failure after radiofrequency ablation for intramucosal adenocarcinoma in Barrett esophagus: a multi-institutional retrospective cohort study. Am J Surg Pathol 2016; 40: 554-562
• 52 Li N, Pasricha S, Bulsiewicz WJ. et al. Effects of preceding endoscopic mucosal resection on the efficacy and safety of radiofrequency ablation for treatment of Barrett's esophagus: results from the United States Radiofrequency Ablation Registry. Dis Esophagus 2016; 29: 537-543
• 53 Phoa KN, Pouw RE, Bisschops R. et al. Multimodality endoscopic eradication for neoplastic Barrett oesophagus: results of an European multicentre study (EURO-II). Gut 2016; 65: 555-562
• 54 Saligram S, Chennat J, Hu H. et al. Endotherapy for superficial adenocarcinoma of the esophagus: an American experience. Gastrointest Endosc 2013; 77: 872-876
• 55 Caillol F, Bories E, Pesenti C. et al. Radiofrequency ablation associated to mucosal resection in the oesophagus: experience in a single centre. Clin Res Hepatol Gastroenterol 2012; 36: 371-377
• 56 Okoro NI, Tomizawa Y, Dunagan KT. et al. Safety of prior endoscopic mucosal resection in patients receiving radiofrequency ablation of Barrett's esophagus. Clin Gastroenterol Hepatol 2012; 10: 150-154
• 57 Ganz RA, Overholt BF, Sharma VK. et al. Circumferential ablation of Barrett's esophagus that contains high-grade dysplasia: a U.S. Multicenter Registry. Gastrointest Endosc 2008; 68: 35-40
• 58 Terheggen G, Horn EM, Vieth M. et al. A randomised trial of endoscopic submucosal dissection versus endoscopic mucosal resection for early Barrett's neoplasia. Gut 2017; 66: 783-793
• 59 Mejia Perez LK, Yang D, Draganov PV. et al. Endoscopic submucosal dissection vs endoscopic mucosal resection for early Barrett's neoplasia in the West: A retrospective study. Endoscopy 2022; 54: 439-446
• 60 Subramaniam S, Kandiah K, Chedgy F. et al. The safety and efficacy of radiofrequency ablation following endoscopic submucosal dissection for Barrett's neoplasia. Dis Esophagus 2018; 31: dox133
• 61 Draganov PV, Wang AY, Othman MO. et al. AGA Institute Clinical Practice Update: endoscopic submucosal dissection in the United States. Clin Gastroenterol Hepatol 2019; 17: 16-25 e11
• 62 Leers JM, DeMeester SR, Oezcelik A. et al. The prevalence of lymph node metastases in patients with T1 esophageal adenocarcinoma a retrospective review of esophagectomy specimens. Ann Surg 2011; 253: 271-278
• 63 Otaki F, Ma GK, Krigel A. et al. Outcomes of patients with submucosal (T1b) esophageal adenocarcinoma: a multicenter cohort study. Gastrointest Endosc 2020; 92: 31-39 e31
• 64 Yang D, Zou F, Xiong S. et al. Endoscopic submucosal dissection for Barrett's early neoplasia: A systematic review and meta-analysis. United European Gastroenterol J 2017; 5: A83
• 65 Fujiyoshi Y, Khalaf K, He T. et al. Comparison of endoscopic mucosal resection versus endoscopic submucosal dissection for Barrett's neoplasia and esophageal adenocarcinoma: a systematic review and meta-analysis. Gastrointest Endosc 2024; 2024