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Endoscopic and oncologic outcomes according to indication criteria of endoscopic resection for early gastric cancer: a systematic review and meta-analysis

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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.

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References

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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)

    Article  CAS  PubMed  Google Scholar 

  7. 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

    Article  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. Japanese Gastric Cancer A (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14(2):113–123

    Article  Google Scholar 

  10. Gotoda T (2007) Endoscopic resection of early gastric cancer. Gastric Cancer 10(1):1–11

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  PubMed  Google Scholar 

  15. 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

    Article  PubMed  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. 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

    Article  PubMed  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. Japanese Gastric Cancer A (1998) Japanese classification of gastric carcinoma—2nd English edition. Gastric Cancer 1(1):10–24

    Article  Google Scholar 

  21. 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

    Article  PubMed  Google Scholar 

  22. Japanese Gastric Cancer A (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112

    Article  Google Scholar 

  23. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558

    Article  PubMed  Google Scholar 

  24. 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

    Article  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. 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

    PubMed  PubMed Central  Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. 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

    Google Scholar 

  31. 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

    Article  PubMed Central  Google Scholar 

  32. 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

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    PubMed  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

  38. 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

    Article  PubMed  PubMed Central  Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

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Correspondence to Hyuk Lee or Hyun Joo Jang.

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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.

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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

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  • DOI: https://doi.org/10.1007/s00464-015-4376-6

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