Predictors of long-term outcomes of endoscopic submucosal dissection of early gastric neoplasia in the West: a multicenter study

Abstract

Background This study aimed to determine long-term outcomes of gastric endoscopic submucosal dissection (ESD) in Western settings based on the latest Japanese indication criteria, and to examine predictors of outcomes and complications.

Methods Data were collected from consecutive patients undergoing gastric ESD at four participating centers from 2009 to 2021. Retrospective analysis using logistic regression and survival analysis was performed.

Results 415 patients were included (mean age 71.7 years; 56.4 % male). Absolute indication criteria (2018 guideline) were met in 75.3 % of patients. Median follow-up was 52 months. Post-resection histology was adenocarcinoma, high grade dysplasia, and low grade dysplasia in 49.9 %, 22.7 %, and 17.1 %, respectively. Perforation, early and delayed bleeding occurred in 2.4 %, 4.3 %, and 3.4 %, respectively. Rates of en bloc and R0 resection, and recurrence on first endoscopic follow-up were 94.7 %, 83.4 %, and 2.7 %, respectively. Relative indication (2018 guideline) for ESD was associated with R1 outcome (P = 0.02). Distal location (P = 0.002) and increased procedure time (P = 0.04) were associated with bleeding, and scarring (P = 0.009) and increased procedure duration (P = 0.003) were associated with perforation. Recurrence-free survival at 2 and 5 years was 94 % and 83 %, respectively.

Conclusion This is the largest Western multicenter cohort and suggests that gastric ESD is safe and effective in the Western setting. A quarter of patients fell outside the new absolute indications for ESD, suggesting that Western practice involves more advanced lesions. We identified the predictors of complications, which should help to inform future Western practice and research.

• References

• 1 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424 Erratum in: CA Cancer J Clin 2020; 70: 313
• 2 Japanese Gastric Cancer Association. Japanese Classification of Gastric Carcinoma. 15th edn. [in Japanese]. Tokyo: Kanehara Shuppan; 2017
• 3 Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018. 5th edn. Gastric Cancer 2021; 24: 1-21
• 4 Ma MX, Bourke MJ. Endoscopic submucosal dissection in the West: current status and future directions. Dig Endosc 2018; 30: 310-320
• 5 Gotoda T, Yanagisawa A, Sasako M. et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 2000; 3: 219-225
• 6 Hirasawa T, Gotoda T, Miyata S. et al. Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer 2009; 12: 148-152
• 7 Ahn JY, Jung HY, Choi KD. et al. Endoscopic and oncologic outcomes after endoscopic resection for early gastric cancer: 1370 cases of absolute and extended indications. Gastrointest Endosc 2011; 74: 485-493
• 8 Suzuki H, Oda I, Abe S. et al. High rate of 5-year survival among patients with early gastric cancer undergoing curative endoscopic submucosal dissection. Gastric Cancer 2016; 19: 198-205
• 9 Zullo A, Manta R, De Francesco V. et al. Endoscopic submucosal dissection of gastric neoplastic lesions in Western countries: systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2021; 33: e1-e6
• 10 The Paris endoscopic classification of superficial neoplastic lesions. esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 2003; 58 (Suppl. 06) S3-43
• 11 Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T. et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: 829-854
• 12 Banks M, Graham D, Jansen M. et al. British Society of Gastroenterology guidelines on the diagnosis and management of patients at risk of gastric adenocarcinoma. Gut 2019; 68: 1545-1575
• 13 Ngamruengphong S, Ferri L, Aihara H. et al. Efficacy of endoscopic submucosal dissection for superficial gastric neoplasia in a large cohort in North America. Clin Gastroenterol Hepatol 2021; 19: 1611-1619
• 14 Manta R, Galloro G, Pugliese F. et al. Endoscopic submucosal dissection of gastric neoplastic lesions: an Italian, multicenter study. J Clin Med 2020; 9: 737
• 15 Pimentel-Nunes P, Mourão F, Veloso N. et al. Long-term follow-up after endoscopic resection of gastric superficial neoplastic lesions in Portugal. Endoscopy 2014; 46: 933-940
• 16 Probst A, Schneider A, Schaller T. et al. Endoscopic submucosal dissection for early gastric cancer: are expanded resection criteria safe for Western patients?. Endoscopy 2017; 49: 855-865
• 17 Oda I, Saito D, Tada M. et al. A multicenter retrospective study of endoscopic resection for early gastric cancer. Gastric Cancer 2006; 9: 262-270
• 18 Sugimoto T, Okamoto M, Mitsuno Y. et al. Endoscopic submucosal dissection is an effective and safe therapy for early gastric neoplasms: a multicenter feasible study. J Clin Gastroenterol 2012; 46: 124-129
• 19 Hotta K, Oyama T, Akamatsu T. et al. A comparison of outcomes of endoscopic submucosal dissection (ESD) for early gastric neoplasms between high-volume and low-volume centers: multi-center retrospective questionnaire study conducted by the Nagano ESD Study Group. Intern Med 2010; 49: 253-259
• 20 Costa RS, Ferreira A, Leal T. et al. Endoscopic submucosal dissection for the treatment of superficial epithelial gastric neoplasia in a Portuguese centre. GE Port J Gastroenterol 2019; 26: 90-98
• 21 Repici A, Zullo A, Hassan C. et al. Endoscopic submucosal dissection of early gastric neoplastic lesions: a Western series. Eur J Gastroenterol Hepatol 2013; 25: 1261-1264
• 22 Oda I, Gotoda T, Hamanaka H. et al. Endoscopic submucosal dissection for early gastric cancer: technical feasibility, operation time and complications from a large consecutive series. Dig Endosc 2005; 17: 54-58
• 23 Hasuike N, Ono H, Boku N. et al. Gastrointestinal Endoscopy Group of Japan Clinical Oncology Group (JCOG-GIESG). A non-randomized confirmatory trial of an expanded indication for endoscopic submucosal dissection for intestinal-type gastric cancer (cT1a): the Japan Clinical Oncology Group study (JCOG0607). Gastric Cancer 2018; 21: 114-123
• 24 Takizawa K, Ono H, Hasuike N. et al. Gastrointestinal Endoscopy Group (GIESG) and the Stomach Cancer Study Group (SCSG) of Japan Clinical Oncology Group. A nonrandomized, single-arm confirmatory trial of expanded endoscopic submucosal dissection indication for undifferentiated early gastric cancer: Japan Clinical Oncology Group study (JCOG1009/1010). Gastric Cancer 2021; 24: 479-491
• 25 Suzuki H, Takizawa K, Hirasawa T. et al. Short-term outcomes of multicenter prospective cohort study of gastric endoscopic resection: ‘real-world evidence’ in Japan. Dig Endosc 2019; 31: 30-39
• 26 Suzuki H, Ono H, Hirasawa T. et al. J-WEB/EGC group. Long-term survival after endoscopic resection for gastric cancer: real-world evidence from a multicenter prospective cohort. Clin Gastroenterol Hepatol 2022;
• 27 Zhang X, Ly EK, Nithyanand S. et al. Learning curve for endoscopic submucosal dissection with an untutored, prevalence-based approach in the United States. Clin Gastroenterol Hepatol 2020; 18: 580-588
• 28 Lim H, Jung HY, Park YS. et al. Discrepancy between endoscopic forceps biopsy and endoscopic resection in gastric epithelial neoplasia. Surg Endosc 2014; 28: 1256-1262
• 29 Hatta W, Tsuji Y, Yoshio T. et al. Prediction model of bleeding after endoscopic submucosal dissection for early gastric cancer: BEST-J score. Gut 2021; 70: 476-484
• 30 Takizawa K, Oda I, Gotoda T. et al. Routine coagulation of visible vessels may prevent delayed bleeding after endoscopic submucosal dissection (ESD). An analysis of risk factors. Endoscopy 2008; 40: 179-183
• 31 Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 2017; 20: 1-19