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Long-term clinical outcomes of endoscopic vs. surgical resection for early gastric cancer with undifferentiated histology

  • Joo Hyun Lim
  • Jung Kim
  • Sang Gyun KimEmail author
  • Hyunsoo Chung
Article

Abstract

Background

The efficacy of endoscopic submucosal dissection (ESD) for undifferentiated early gastric cancer (UD EGC) is controversial due to the relatively high risk of lymph node metastasis. We compared long-term clinical outcomes of UD EGC between ESD and surgical resection groups.

Methods

We retrospectively reviewed the medical records of patients with UD EGC treated by either ESD or surgical resection between January 2007 and December 2014. Long-term clinical outcomes were compared between the two groups in terms of survival.

Results

A total of 1147 patients were enrolled with median follow-up duration of 59.1 months. ESD and surgical resections were performed in 126 and 1021 patients respectively. Additional surgery was performed in 22 patients after ESD. There were no significant differences in overall survival [total, p = 0.641; propensity score matching (PSM), p = 0.330; expanded criteria, p = 0.512]. Although the disease-free survival rate was lower in ESD group because of the higher rate of metachronous cancer development (total, p < 0.001; PSM, p = 0.001), the difference was not significant in the group within expanded criteria (p = 0.071).

Conclusions

ESD could be a comparable treatment option with surgical resection for UD EGC within expanded criteria in terms of long-term survival. It is mandatory to establish a meticulous indication of ESD for UD EGC considering the risk of lymph node metastasis.

Keywords

Endoscopic submucosal dissection Undifferentiated Early gastric cancer Survival rate 

Notes

Funding

This work was supported by a Grant No 04-2016-0970 from SNUH Research Fund and a grant from Liver Research Institute, Seoul National University College of Medicine.

Compliance with ethical standards

Disclosure

The authors, Joo Hyun Lim, Jung Kim, Sang Gyun Kim, and Hyunsoo Chung, declare that they have no conflict of interest or financial ties to disclose.

References

  1. 1.
    Oda I, Gotoda T, Hamanaka H, Eguchi T, Saito Y, Matsuda T, Bhandari P, Emura F, Saito D, Ono H (2005) Endoscopic submucosal dissection for early gastric cancer: technical feasibility, operation time and complications from a large consecutive series. Dig Endosc 17:54–58CrossRefGoogle Scholar
  2. 2.
    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 58:331–336CrossRefGoogle Scholar
  3. 3.
    Chung IK, Lee JH, Lee SH, Kim SJ, Cho JY, Cho WY, Hwangbo Y, Keum BR, Park JJ, Chun HJ, Kim HJ, Kim JJ, Ji SR, Seol SY (2009) Therapeutic outcomes in 1000 cases of endoscopic submucosal dissection for early gastric neoplasms: Korean ESD Study Group multicenter study. Gastrointest Endosc 69:1228–1235CrossRefGoogle Scholar
  4. 4.
    Kim JP, Lee JH, Kim SJ, Yu HJ, Yang HK (1998) Clinicopathologic characteristics and prognostic factors in 10783 patients with gastric cancer. Gastric Cancer 1:125–133CrossRefGoogle Scholar
  5. 5.
    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 3:219–225CrossRefGoogle Scholar
  6. 6.
    Sanomura Y, Oka S, Tanaka S, Noda I, Higashiyama M, Imagawa H, Shishido T, Yoshida S, Hiyama T, Arihiro K, Chayama K (2012) Clinical validity of endoscopic submucosal dissection for submucosal invasive gastric cancer: a single-center study. Gastric Cancer 15:97–105CrossRefGoogle Scholar
  7. 7.
    Hirasawa T, Gotoda T, Miyata S, Kato Y, Shimoda T, Taniguchi H, Fujisaki J, Sano T, Yamaguchi T (2009) Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer 12:148–152CrossRefGoogle Scholar
  8. 8.
    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 of mucosal early gastric cancer: analysis of a single center experience. J Gastroenterol Hepatol 26:884–887CrossRefGoogle Scholar
  9. 9.
    Oh SY, Lee KG, Sun YS, Kim MA, Kong SH, Lee HJ, Kim WH, Yang HK (2017) Lymph node metastasis in mucosal gastric cancer. Reappraisal of expanded indication of endoscopic submucosal dissection. Ann Surg 265:137–142CrossRefGoogle Scholar
  10. 10.
    Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383CrossRefGoogle Scholar
  11. 11.
    Soetikno R, Kaltenbach T, Yeh R, Gotoda T (2005) Endoscopic mucosal resection for early cancers of the upper gastrointestinal tract. J Clin Oncol 23:4490–4498CrossRefGoogle Scholar
  12. 12.
    Oda I, Saito D, Tada M, Iishi H, Tanabe S, Oyama T, Doi T, Otani Y, Fujisaki J, Ajioka Y, Hamada T, Inoue H, Gotoda T, Yoshida S (2006) A multicenter retrospective study of endoscopic resection for early gastric cancer. Gastric Cancer 9:262–270CrossRefGoogle Scholar
  13. 13.
    Chonan A, Mishima T, Andou M, Tamura T, Atami M, Mochizuki F (2001) Endoscopic ultrasonographic diagnosis of the depth of invasion of gastric cancer. Stomach Intestine 36:341–350Google Scholar
  14. 14.
    Okada K, Fujisaki J, Kasuga A, Omae M, Yoshimoto K, Hirasawa T, Ishiyama A, Yamamoto Y, Tsuchida T, Hoshino E, Igarashi M, Takahashi H (2011) Endoscopic ultrasonography is valuable for identifying early gastric cancers meeting expanded-indication criteria for endoscopic submucosal dissection. Surg Endosc 25:841–848CrossRefGoogle Scholar
  15. 15.
    Haruta H, Hosoya Y, Sakuma K, Shibusawa H, Satoh K, Yamamoto H, Tanaka A, Niki T, Sugano K, Yasuda Y (2008) Clinicopathological study of lymph-node metastasis in 1389 patients with early gastric cancer: assessment of indications for endoscopic resection. J Dig Dis 9:213–218CrossRefGoogle Scholar
  16. 16.
    Li C, Kim S, Lai JF, Oh SJ, Hyung WJ, Choi WH, Choi SH, Zhu ZG, Noh SH (2008) Risk factors for lymph node metastasis in undifferentiated early gastric cancer. Ann Surg Oncol 15:764–769CrossRefGoogle Scholar
  17. 17.
    Ye BD, Kim SG, Lee JY, Kim JS, Yang HK, Kim WH, Jung HC, Lee KU, Song IS (2008) Predictive factors for lymph node metastasis and endoscopic treatment strategies for undifferentiated early gastric cancer. J Gastroenterol Hepatol 23:46–50CrossRefGoogle Scholar
  18. 18.
    Li H, Lu P, Lu Y, Liu C, Xu H, Wang S, Chen J (2010) Predictive factors of lymph node metastasis in undifferentiated early gastric cancers and application of endoscopic mucosal resection. Surg Oncol 19:221–226CrossRefGoogle Scholar
  19. 19.
    Takizawa K, Ono H, Kakushima N, Tanaka M, Hasuike N, Matsubayashi H, Yamagichi Y, Bando E, Terashima M, Kusafuka K, Nakajima T (2013) Risk of lymph node metastases from intramucosal gastric cancer in relation to histological types: how to manage the mixed histological type for endoscopic submucosal dissection. Gastric Cancer 16:531–536CrossRefGoogle Scholar
  20. 20.
    Ninomiya Y, Yanagisawa A, Kato Y, Tomimatsu H (2000) Unrecognizable intramucosal spread of diffuse-type mucosal gastric carcinomas of less than 20 mm in size. Endoscopy 32:604–608CrossRefGoogle Scholar
  21. 21.
    Sawada S, Fujisaki J, Yamamoto N, Kato Y, Ishiyama A, Ueki N, Hirasawa T, Yamamoto Y, Tsuchida T, Tatewaki M, Hoshino E, Igarashi M, Takahashi H, Fujita R (2010) Expansion of indications for endoscopic treatment of undifferentiated mucosal gastric cancer: analysis of intramucosal spread in resected specimens. Dig Dis Sci 55:1376–1380CrossRefGoogle Scholar
  22. 22.
    Kang HY, Kim SG, Kim JS, Jung HC, Song IS (2009) Clinical outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Gastrointest Endosc 69:e1–e9CrossRefGoogle Scholar
  23. 23.
    Goh PG, Jeong HY, Kim MJ, Eun HS, Kim HJ, Kim ES, Kim YJ, Lee SY, Moon HS, Lee ES, Kim SH, Sung JK, Lee BS (2011) Clinical outcomes of endoscopic submucosal dissection for undifferentiated or submucosal invasive early gastric cancer. Clin Endosc 44:116–122CrossRefGoogle Scholar
  24. 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 45:651–656CrossRefGoogle Scholar
  25. 25.
    Choi MH, Hong SJ, Han JP, Song JY, Kim DY, Seo SW, Ha JS, Lee YN, Ko BM, Lee MS (2013) Therapeutic outcomes of endoscopic submucosal dissection in undifferentiated-type early gastric cancer. Korean J Gastroenterol 61:196–202CrossRefGoogle Scholar
  26. 26.
    Kim YY, Jeon SW, Kim J, Park JC, Choi KB, Park KS, Kim E, Chung YJ, Kwon JG, Jung JT, Kim EY, Kim KO, Jang B, Lee SH, Yang CH (2013) Endoscopic submucosal dissection for early gastric cancer with undifferentiated histology: could we extend the criteria beyond? Surg Endosc 27:4656–4662CrossRefGoogle Scholar
  27. 27.
    Chung MW, Jeong O, Park YK, Lee KH, Lee JH, Lee WS, Joo YE, Choi SK, Choi SB (2014) Comparison on the long term outcome between endoscopic submucosal dissection and surgical treatment for undifferentiated early gastric cancer. Korean J Gastoenterol 63:90–98CrossRefGoogle Scholar
  28. 28.
    Lee S, Choi KD, Han M, Na HK, Ahn JY, Jung KW et al (2018) Long-term outcomes of endoscopic submucosal dissection versus surgery in early gastric cancer meeting expanded indication including undifferentiated-type tumors: a criteria-based analysis. Gastric Cancer 21:490–499CrossRefGoogle Scholar
  29. 29.
    Park JC, Lee YK, Kim SY, Roh Y, Hahn KY, Shin SK, Lee SK, Lee YC, Kim HI, Cheong JH, Hyung WJ, Noh SH (2018) Long-term outcomes of endoscopic submucosal dissection in comparison to surgery in undifferentiated-type intramucosal gastric cancer using propensity score analysis. Surg Endosc 32:2046–2057CrossRefGoogle Scholar
  30. 30.
    Abe N, Watanabe T, Sugiyama M, Yanagida O, Masaki T, Mori T, Atomi Y (2004) Endoscopic treatment or surgery for undifferentiated early gastric cancer? Am J Surg 188:181–184CrossRefGoogle Scholar
  31. 31.
    Park YD, Chung YJ, Chung HY, Yu W, Bae HI, Jeon SW, Cho CM, Tak WY, Kweon YO (2008) Factors related to lymph node metastasis and the feasibility of endoscopic mucosal resection for treating poorly differentiated adenocarcinoma of the stomach. Endoscopy 40:7–10CrossRefGoogle Scholar
  32. 32.
    Kim HM, Pak KH, Chung MJ, Cho JH, Wyung WJ, Noh SH, Kim CB, Lee YC, Song SY, Lee SK (2011) Early gastric cancer of signet ring cell carcinoma is more amenable to endoscopic treatment than is early gastric cancer of poorly differentiated tubular adenocarcinoma in select tumor conditions. Surg Endosc 25:3087–3093CrossRefGoogle Scholar
  33. 33.
    Kwak DS, Min YW, Lee JH, Kang SH, Jang SH, Lee H, Min BH, Kim JJ, Kim KM, Sohn TS, Kim S (2018) Outcomes of endoscopic submucosal dissection for early gastric cancer with undifferentiated-type histology: a clinical simulation using a non-selected surgical cohort. Gut Liver 12:263–270CrossRefGoogle Scholar
  34. 34.
    Ahn JY, Park HJ, Park YS, Lee JH, Choi KS, Jeong KW, Kim DH, Choi KD, Song HJ, Lee GH, Jung HY (2016) Endoscopic resection for undifferentiated-type early gastric cancer: immediate endoscopic outcomes and long-term survivals. Dig Dis Sci 61:1158–1164CrossRefGoogle Scholar
  35. 35.
    Bang CS, Park JM, Baik GH, Park JJ, Joo MK, Jang JY et al (2017) Therapeutic outcomes of endoscopic resection of early gastric cancer with undifferentiated-type histology: a Korean ESD registry database analysis. Clin Endosc 50:569–577CrossRefGoogle Scholar
  36. 36.
    Lim JH, Kim SG, Choi J, Im JP, Kim JS, Jung HC (2015) Risk factors for synchronous or metachronous tumor development after endoscopic resection of gastric neoplasms. Gastric Cancer 18:817–823CrossRefGoogle Scholar
  37. 37.
    Jiang H, Zhang H, Tian L, Zhang X, Xue Y (2013) The difference in clinic-pathological features between signet ring cell carcinoma and gastric mucinous adenocarcinoma. Tumour Biol 34:2625–2631CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Internal Medicine, Healthcare Research Institute, Healthcare System Gangnam CenterSeoul National University HospitalSeoulSouth Korea
  2. 2.Division of Gastroenterology, Department of Internal Medicine and Liver Research InstituteSeoul National University College of MedicineSeoulSouth Korea

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