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

Dhruvil Radadiya; Madhav Desai; Harsh Patel; Jena Velji-Ibrahim; Marco Spadaccini; Sachin Srinivasan; Shruti Khurana; Viveksandeep Thoguluva Chandrasekar; Abhilash Perisetti; Alessandro Repici; Cesare Hassan; Prateek Sharma

doi:10.1055/a-2357-6111

Endoscopy, Table of Contents

Endoscopy 2024; 56(12): 940-954
DOI: 10.1055/a-2357-6111

Systematic review

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

Dhruvil Radadiya

¹Gastroenterology, University of Kansas School of Medicine, Kansas City, United States (Ringgold ID: RIN12251)

,

Madhav Desai

²Gastroenterology, University of Minnesota Medical Center, Minneapolis, United States (Ringgold ID: RIN14400)

³Gastroenterology and Hepatology, The University of Texas Health Science Center at Houston, Houston, United States (Ringgold ID: RIN12340)

,

Harsh Patel

¹Gastroenterology, University of Kansas School of Medicine, Kansas City, United States (Ringgold ID: RIN12251)

,

Jena Velji-Ibrahim

⁴Internal Medicine, University of South Carolina School of Medicine, Greenville, United States (Ringgold ID: RIN12322)

,

Marco Spadaccini

⁵Endoscopy Unit, Humanitas Clinical and Research Center - IRCCS, Rozzano, Italy (Ringgold ID: RIN551905)

,

Sachin Srinivasan

¹Gastroenterology, University of Kansas School of Medicine, Kansas City, United States (Ringgold ID: RIN12251)

,

Shruti Khurana

¹Gastroenterology, University of Kansas School of Medicine, Kansas City, United States (Ringgold ID: RIN12251)

,

Viveksandeep Thoguluva Chandrasekar

⁶Gastroenterology, Augusta University, Augusta, United States (Ringgold ID: RIN1421)

,

Abhilash Perisetti

⁷Gastroenterology, Kansas City VA Medical Center, Kansas City, United States (Ringgold ID: RIN20044)

,

Alessandro Repici

⁵Endoscopy Unit, Humanitas Clinical and Research Center - IRCCS, Rozzano, Italy (Ringgold ID: RIN551905)

⁸Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Italy (Ringgold ID: RIN437807)

,

Cesare Hassan

⁵Endoscopy Unit, Humanitas Clinical and Research Center - IRCCS, Rozzano, Italy (Ringgold ID: RIN551905)

,

Prateek Sharma

¹Gastroenterology, University of Kansas School of Medicine, Kansas City, United States (Ringgold ID: RIN12251)

⁷Gastroenterology, Kansas City VA Medical Center, Kansas City, United States (Ringgold ID: RIN20044)

› Author Affiliations

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.

Full Text

References

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

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