Abstract
Background
The criteria for endoscopic resection for early gastric cancer (EGC) have been expanded recently, and it has become acceptable to use techniques that are regarded as having equivalent technical and pathological outcomes to absolute indication (AI). However, the long-term oncological outcomes of expanded indication (EI) have yet to be clarified. This meta-analysis aimed to assess the long-term outcome of EI versus AI, to identify the endoscopic feasibility and safety according to the indication, and to provide the appropriate recommendations for each indication.
Methods
Electronic databases including PubMed, EMBASE, Cochrane Central Register of Controlled Trials, and KoreaMed were searched for articles published between January 2000 and October 2014. After screening, the reviewers extracted the information from 12 retrospective cohort studies. A total of 9635 EGC lesions, 4150 lesions in the EI group and 5485 lesions in the AI group, were included in this study.
Results
Meta-analyses showed that the local recurrence rate [risk ratio (RR) 1.34; 95 % CI 0.67–2.70] was not significantly higher in the EI group compared with the AI group, although the metachronous recurrence rate was higher in the EI group than in the AI group (RR 1.60; 95 % CI 1.22–2.10). The rates of en bloc resection [odds ratio (OR) 0.57; 95 % CI 0.41–0.78), complete resection (OR 0.37; 95 % CI 0.25–0.57), and curative resection (OR 0.34; 95 % CI 0.20–0.58) were significantly inferior in the EI group than in the AI group, whereas overall bleeding risk (RR 1.47; 95 % CI 1.19–1.82) and procedure-related perforation rate (OR 2.04; 95 % CI 1.56–2.68) were significantly higher in the EI group than in the AI group.
Conclusions
This meta-analysis suggests that the EI group showed acceptable long-term outcomes with local recurrence rate that was not significantly inferior, although the metachronous recurrence rate was higher compared with that in the AI group.
Similar content being viewed by others
References
Bertuccio P, Chatenoud L, Levi F, Praud D, Ferlay J, Negri E, Malvezzi M, La Vecchia C (2009) Recent patterns in gastric cancer: a global overview. Int J Cancer 125(3):666–673
Lee KS, Oh DK, Han MA, Lee HY, Jun JK, Choi KS, Park EC (2011) Gastric cancer screening in Korea: report on the national cancer screening program in 2008. Cancer Res Treat 43(2):83–88
Soetikno R, Kaltenbach T, Yeh R, Gotoda T (2005) Endoscopic mucosal resection for early cancers of the upper gastrointestinal tract. J Clin Oncol 23(20):4490–4498
Takekoshi T, Baba Y, Ota H, Kato Y, Yanagisawa A, Takagi K, Noguchi Y (1994) Endoscopic resection of early gastric carcinoma: results of a retrospective analysis of 308 cases. Endoscopy 26(4):352–358
Uedo N, Iishi H, Tatsuta M, Ishihara R, Higashino K, Takeuchi Y, Imanaka K, Yamada T, Yamamoto S, Yamamoto S, Tsukuma H, Ishiguro S (2006) Longterm outcomes after endoscopic mucosal resection for early gastric cancer. Gastric Cancer 9(2):88–92
Kojima T, Parra-Blanco A, Takahashi H, Fujita R (1998) Outcome of endoscopic mucosal resection for early gastric cancer: review of the Japanese literature. Gastrointest Endosc 48(5):550–554 (discussion 554–555)
Horiki N, Omata F, Uemura M, Suzuki S, Ishii N, Fukuda K, Fujita Y, Ninomiya K, Tano S, Katurahara M, Tanaka K, Gabazza EC, Takei Y (2012) Risk for local recurrence of early gastric cancer treated with piecemeal endoscopic mucosal resection during a 10-year follow-up period. Surg Endosc 26(1):72–78
Nakamoto S, Sakai Y, Kasanuki J, Kondo F, Ooka Y, Kato K, Arai M, Suzuki T, Matsumura T, Bekku D, Ito K, Tanaka T, Yokosuka O (2009) Indications for the use of endoscopic mucosal resection for early gastric cancer in Japan: a comparative study with endoscopic submucosal dissection. Endoscopy 41(9):746–750
Japanese Gastric Cancer A (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14(2):113–123
Gotoda T (2007) Endoscopic resection of early gastric cancer. Gastric Cancer 10(1):1–11
Lian J, Chen S, Zhang Y, Qiu F (2012) A meta-analysis of endoscopic submucosal dissection and EMR for early gastric cancer. Gastrointest Endosc 76(4):763–770
Oka S, Tanaka S, Kaneko I, Mouri R, Hirata M, Kawamura T, Yoshihara M, Chayama K (2006) Advantage of endoscopic submucosal dissection compared with EMR for early gastric cancer. Gastrointest Endosc 64(6):877–883
Gotoda T, Yanagisawa A, Sasako M, Ono H, Nakanishi Y, Shimoda T, Kato Y (2000) Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 3(4):219–225
Ahn JY, Jung HY, Choi KD, Choi JY, Kim MY, Lee JH, Choi KS, Kim do H, Song HJ, Lee GH, Kim JH, Park YS (2011) Endoscopic and oncologic outcomes after endoscopic resection for early gastric cancer: 1370 cases of absolute and extended indications. Gastrointest Endosc 74(3):485–493
Ishikawa S, Togashi A, Inoue M, Honda S, Nozawa F, Toyama E, Miyanari N, Tabira Y, Baba H (2007) Indications for EMR/ESD in cases of early gastric cancer: relationship between histological type, depth of wall invasion, and lymph node metastasis. Gastric Cancer 10(1):35–38
Jee YS, Hwang SH, Rao J, Park DJ, Kim HH, Lee HJ, Yang HK, Lee KU (2009) Safety of extended endoscopic mucosal resection and endoscopic submucosal dissection following the Japanese Gastric Cancer Association treatment guidelines. Br J Surg 96(10):1157–1161
Kang HJ, Kim DH, Jeon TY, Lee SH, Shin N, Chae SH, Kim GH, Song GA, Kim DH, Srivastava A, Park do Y, Lauwers GY (2010) Lymph node metastasis from intestinal-type early gastric cancer: experience in a single institution and reassessment of the extended criteria for endoscopic submucosal dissection. Gastrointest Endosc 72(3):508–515
Chung JW, Jung HY, Choi KD, Song HJ, Lee GH, Jang SJ, Park YS, Yook JH, Oh ST, Kim BS, Kim JH (2011) Extended indication of endoscopic resection for mucosal early gastric cancer: analysis of a single center experience. J Gastroenterol Hepatol 26(5):884–887
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62(10):1006–1012
Japanese Gastric Cancer A (1998) Japanese classification of gastric carcinoma—2nd English edition. Gastric Cancer 1(1):10–24
Yamaguchi N, Isomoto H, Fukuda E, Ikeda K, Nishiyama H, Akiyama M, Ozawa E, Ohnita K, Hayashi T, Nakao K, Kohno S, Shikuwa S (2009) Clinical outcomes of endoscopic submucosal dissection for early gastric cancer by indication criteria. Digestion 80(3):173–181
Japanese Gastric Cancer A (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558
Park CH, Shin S, Park JC, Shin SK, Lee SK, Lee YC, Lee H (2013) Long-term outcome of early gastric cancer after endoscopic submucosal dissection: expanded indication is comparable to absolute indication. Dig Liver Dis 45(8):651–656
Isomoto H, Shikuwa S, Yamaguchi N, Fukuda E, Ikeda K, Nishiyama H, Ohnita K, Mizuta Y, Shiozawa J, Kohno S (2009) Endoscopic submucosal dissection for early gastric cancer: a large-scale feasibility study. Gut 58(3):331–336
Gotoda T, Iwasaki M, Kusano C, Seewald S, Oda I (2010) Endoscopic resection of early gastric cancer treated by guideline and expanded National Cancer Centre criteria. Br J Surg 97(6):868–871
Ohnita K, Isomoto H, Shikuwa S, Yajima H, Minami H, Matsushima K, Akazawa Y, Yamaguchi N, Fukuda E, Nishiyama H, Takeshima F, Nakao K (2014) Early and long-term outcomes of endoscopic submucosal dissection for early gastric cancer in a large patient series. Exp Ther Med 7(3):594–598
Choi MK, Kim GH, Park do Y, Song GA, Kim DU, Ryu DY, Lee BE, Cheong JH, Cho M (2013) Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a single-center experience. Surg Endosc 27(11):4250–4258
Kosaka T, Endo M, Toya Y, Abiko Y, Kudara N, Inomata M, Chiba T, Takikawa Y, Suzuki K, Sugai T (2014) Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a single-center retrospective study. Dig Endosc 26(2):183–191
Choi J, Kim SG, Im JP, Kim JS, Jung HC (2014) Long-term clinical outcomes of endoscopic resection for early gastric cancer. Surg Endosc. doi:10.1007/s00464-014-3800-7
Shin KY, Jeon SW, Cho KB, Park KS, Kim ES, Park CK, Chung YJ, Kwon JG, Jung JT, Kim EY, Kim KO, Jang BI, Lee SH, Park JB, Yang CH (2014) Clinical outcomes of the endoscopic submucosal dissection of early gastric cancer are comparable between absolute and new expanded criteria. Gut Liver 9(2):181–187
Probst A, Pommer B, Golger D, Anthuber M, Arnholdt H, Messmann H (2010) Endoscopic submucosal dissection in gastric neoplasia—experience from a European center. Endoscopy 42(12):1037–1044
Park CH, Lee H, Kim DW, Chung H, Park JC, Shin SK, Hyung WJ, Lee SK, Lee YC, Noh SH (2014) Clinical safety of endoscopic submucosal dissection compared with surgery in elderly patients with early gastric cancer: a propensity-matched analysis. Gastrointest Endosc 80(4):599–609
Matsukura N, Tajiri T, Kato S, Togashi A, Masuda G, Fujita I, Tokunaga A, Yamada N (2003) Helicobacter pylori eradication therapy for the remnant stomach after gastrectomy. Gastric Cancer 6(2):100–107
Onoda N, Maeda K, Sawada T, Wakasa K, Arakawa T, Chung KH (2001) Prevalence of Helicobacter pylori infection in gastric remnant after distal gastrectomy for primary gastric cancer. Gastric Cancer 4(2):87–92
Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, Terao S, Amagai K, Hayashi S, Asaka M, Japan Gast Study G (2008) Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 372(9636):392–397
Shiotani A, Uedo N, Iishi H, Yoshiyuki Y, Ishii M, Manabe N, Kamada T, Kusunoki H, Hata J, Haruma K (2008) Predictive factors for metachronous gastric cancer in high-risk patients after successful Helicobacter pylori eradication. Digestion 78(2–3):113–119
Park DJ, Lee HK, Lee HJ, Lee HS, Kim WH, Yang HK, Lee KU, Choe KJ (2004) Lymph node metastasis in early gastric cancer with submucosal invasion: feasibility of minimally invasive surgery. World J Gastroenterol 10(24):3549–3552
Schlemper RJ, Kato Y, Stolte M (2000) Diagnostic criteria for gastrointestinal carcinomas in Japan and Western countries: proposal for a new classification system of gastrointestinal epithelial neoplasia. J Gastroenterol Hepatol 15(Suppl):G49–G57
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Disclosures
Se Woo Park, Hyuk Lee, Chan Hyuk Park, Hyun Joo Jang and Hongyup Ahn have no conflicts of interest or financial ties to disclose.
Additional information
Hyuk Lee and Hyun Joo Jang have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Park, S.W., Lee, H., Park, C.H. et al. Endoscopic and oncologic outcomes according to indication criteria of endoscopic resection for early gastric cancer: a systematic review and meta-analysis. Surg Endosc 30, 1270–1281 (2016). https://doi.org/10.1007/s00464-015-4376-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-015-4376-6