Surgical Endoscopy

, Volume 34, Issue 2, pp 880–887 | Cite as

Clinical outcomes of endoscopic submucosal dissection for lesions on the proximal location between remnant and entire stomach

  • Su Jin Kim
  • Cheol Woong ChoiEmail author
  • Dae Hwan Kang
  • Hyung Wook Kim
  • Su Bum Park
  • Hyeong Seok Nam
  • Dae Gon Ryu



Tumors located on the proximal stomach are associated with a longer procedure time and lower en-block resection of endoscopic submucosal dissection (ESD). Additionally, it is more difficult to perform ESD for lesions after distal gastrectomy because of the narrow inner space. We aimed to evaluate the therapeutic outcomes of ESD for lesions on the remnant stomach compared with those on the upper third of the entire stomach.


A total of 135 patients with a neoplasm located on the proximal stomach who received ESD between Aug 2008 and Dec 2016 were enrolled. We retrospectively reviewed en-bloc resection rate, complete resection rate, and complication rate according to whether distal gastrectomy was performed. Clinical outcomes were compared among the 1:2 propensity-matched groups.


Between the remnant stomach and entire stomach, the en-bloc [92% (23/25) and 92.0% (46/50), respectively; P = 1.000] and complete resection [84% (21/25) and 88.0 (44/50), respectively; P = 0.723] rates were not significantly different. In patients with lesions that indicated ESD, there was no significant difference in en-bloc and complete resection rates. In a multivariable analysis, submucosal fibrosis [odds ratio (OR) 5.9, 95% confidence interval (CI) 1.1–30.7] and submucosa invasive cancer (OR 10.1, 95% CI 1.4–74.3) were independent risk factors for incomplete resection.


ESD is a feasible therapeutic option for lesions located on the proximal stomach regardless the operation history of distal gastrectomy. However, the complete resection rate decreases for lesions with submucosal fibrosis or the submucosa invasion.


Endoscopic submucosal dissection Neoplasm Curative resection 


Compliance with ethical standards


Su Jin Kim, Cheol Woong Choi, Dae Hwan Kang, Hyung Wook Kim, Su Bum Park, Hyeong Seok Nam, Dae Gon Ryu have no conflicts of interest or financial ties to disclose.


  1. 1.
    Jung KW, Yim SH, Kong HJ, Hwang SY, Won YJ, Lee JK, Shin HR (2007) Cancer survival in Korea 1993-2002: a population-based study. J Korean Med Sci 22(Suppl):S5–S10CrossRefGoogle Scholar
  2. 2.
    Jun JK, Choi KS, Lee HY, Suh M, Park B, Song SH, Jung KW, Lee CW, Choi IJ, Park EC, Lee D (2017) Effectiveness of the Korean national cancer screening program in reducing gastric cancer mortality. Gastroenterology 152(1319–1328):e1317Google Scholar
  3. 3.
    Lee JH, Kim JG, Jung HK, Kim JH, Jeong WK, Jeon TJ, Kim JM, Kim YI, Ryu KW, Kong SH, Kim HI, Jung HY, Kim YS, Zang DY, Cho JY, Park JO, Lim DH, Jung ES, Ahn HS, Kim HJ, Committee on Stomach Cancer Guideline D (2014) Synopsis on clinical practice guideline of gastric cancer in Korea: an evidence-based approach. Korean J Gastroenterol 63:66–81CrossRefGoogle Scholar
  4. 4.
    Choi IJ, Lee JH, Kim YI, Kim CG, Cho SJ, Lee JY, Ryu KW, Nam BH, Kook MC, Kim YW (2015) Long-term outcome comparison of endoscopic resection and surgery in early gastric cancer meeting the absolute indication for endoscopic resection. Gastrointest Endosc 81(333–341):e331Google Scholar
  5. 5.
    Kim EH, Park JC, Song IJ, Kim YJ, Joh DH, Hahn KY, Lee YK, Kim HY, Chung H, Shin SK, Lee SK, Lee YC (2017) Prediction model for non-curative resection of endoscopic submucosal dissection in patients with early gastric cancer. Gastrointest Endosc 85:976–983CrossRefGoogle Scholar
  6. 6.
    Kim JH, Nam HS, Choi CW, Kang DH, Kim HW, Park SB, Kim SJ, Hwang SH, Lee SH (2017) Risk factors associated with difficult gastric endoscopic submucosal dissection: predicting difficult ESD. Surg Endosc 31:1617–1626CrossRefGoogle Scholar
  7. 7.
    Nonaka S, Oda I, Makazu M, Haruyama S, Abe S, Suzuki H, Yoshinaga S, Nakajima T, Kushima R, Saito Y (2013) Endoscopic submucosal dissection for early gastric cancer in the remnant stomach after gastrectomy. Gastrointest Endosc 78:63–72CrossRefGoogle Scholar
  8. 8.
    Ojima T, Takifuji K, Nakamura M, Nakamori M, Katsuda M, Iida T, Hayata K, Iwahashi M, Yamaue H (2014) Endoscopic submucosal dissection for gastric tumors in various types of remnant stomach. Endoscopy 46:645–649CrossRefGoogle Scholar
  9. 9.
    Song BG, Kim GH, Lee BE, Jeon HK, Baek DH, Song GA (2017) Endoscopic submucosal dissection of gastric epithelial neoplasms after partial gastrectomy: a single-center experience. Gastroenterol Res Pract 2017:6395283CrossRefGoogle Scholar
  10. 10.
    Lee JY, Choi IJ, Cho SJ, Kim CG, Kook MC, Lee JH, Ryu KW, Kim YW (2010) Endoscopic submucosal dissection for metachronous tumor in the remnant stomach after distal gastrectomy. Surg Endosc 24:1360–1366CrossRefGoogle Scholar
  11. 11.
    Endoscopic Classification Review G (2005) Update on the paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 37:570–578CrossRefGoogle Scholar
  12. 12.
    (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112Google Scholar
  13. 13.
    Ono H, Yao K, Fujishiro M, Oda I, Nimura S, Yahagi N, Iishi H, Oka M, Ajioka Y, Ichinose M, Matsui T (2016) Guidelines for endoscopic submucosal dissection and endoscopic mucosal resection for early gastric cancer. Dig Endosc 28:3–15CrossRefGoogle Scholar
  14. 14.
    Kaminishi M, Shimizu N, Shiomoyama S, Yamaguchi H, Ogawa T, Sakai S, Kuramoto S, Oohara T (1995) Etiology of gastric remnant cancer with special reference to the effects of denervation of the gastric mucosa. Cancer 75:1490–1496CrossRefGoogle Scholar
  15. 15.
    Miwa K, Hasegawa H, Fujimura T, Matsumoto H, Miyata R, Kosaka T, Miyazaki I, Hattori T (1992) Duodenal reflux through the pylorus induces gastric adenocarcinoma in the rat. Carcinogenesis 13:2313–2316CrossRefGoogle Scholar
  16. 16.
    Sasako M, Maruyama K, Kinoshita T, Okabayashi K (1991) Surgical treatment of carcinoma of the gastric stump. Br J Surg 78:822–824CrossRefGoogle Scholar
  17. 17.
    Piso P, Meyer HJ, Edris C, Jahne J (1999) Surgical therapy of gastric stump carcinoma–a retrospective analysis of 109 patients. Hepatogastroenterology 46:2643–2647PubMedGoogle Scholar
  18. 18.
    Takenaka R, Kawahara Y, Okada H, Tsuzuki T, Yagi S, Kato J, Ohara N, Yoshino T, Imagawa A, Fujiki S, Takata R, Nakagawa M, Mizuno M, Inaba T, Toyokawa T, Sakaguchi K (2008) Endoscopic submucosal dissection for cancers of the remnant stomach after distal gastrectomy. Gastrointest Endosc 67:359–363CrossRefGoogle Scholar
  19. 19.
    Yabuuchi Y, Kakushima N, Takizawa K, Tanaka M, Kawata N, Yoshida M, Kishida Y, Ito S, Imai K, Ishiwatari H, Hotta K, Matsubayashi H, Ono H (2018) Short- and long-term outcomes of endoscopic submucosal dissection for early gastric cancer in the remnant stomach after gastrectomy. J Gastroenterol 67:359–363Google Scholar
  20. 20.
    Lee JY, Min BH, Lee JG, Noh D, Lee JH, Rhee PL, Kim JJ (2016) Endoscopic submucosal dissection for early gastric neoplasia occurring in the remnant stomach after distal gastrectomy. Clin Endosc 49:182–186CrossRefGoogle Scholar
  21. 21.
    Nishimura J, Nishikawa J, Hamabe K, Nakamura M, Goto A, Okamoto T, Miura O, Sakaida I (2014) Efficacy of endoscopic submucosal dissection for cancer of the operated stomach. J Gastrointest Cancer 45:27–33CrossRefGoogle Scholar
  22. 22.
    Jeong JY, Oh YH, Yu YH, Park HS, Lee HL, Eun CS, Han DS (2012) Does submucosal fibrosis affect the results of endoscopic submucosal dissection of early gastric tumors? Gastrointest Endosc 76:59–66CrossRefGoogle Scholar
  23. 23.
    Isshi K, Tajiri H, Fujisaki J, Mochizuki K, Matsuda K, Nakamura Y, Saito N, Narimiya N (2004) The effectiveness of a new multibending scope for endoscopic mucosal resection. Endoscopy 36:294–297CrossRefGoogle Scholar
  24. 24.
    Yoshida M, Takizawa K, Suzuki S, Koike Y, Nonaka S, Yamasaki Y, Minagawa T, Sato C, Takeuchi C, Watanabe K, Kanzaki H, Morimoto H, Yano T, Sudo K, Mori K, Gotoda T, Ono H (2017) Conventional versus traction-assisted endoscopic submucosal dissection for gastric neoplasms: a multicenter, randomized controlled trial (with video). Gastrointest Endosc 87:1231–1240CrossRefGoogle Scholar
  25. 25.
    Goto O, Fujishiro M, Kodashima S, Kakushima N, Ono S, Yahagi N, Omata M (2009) Feasibility of electrocautery snaring as the final step of endoscopic submucosal dissection for stomach epithelial neoplasms. Dig Liver Dis 41:26–30CrossRefGoogle Scholar
  26. 26.
    Fujishiro M, Yahagi N, Nakamura M, Kakushima N, Kodashima S, Ono S, Kobayashi K, Hashimoto T, Yamamichi N, Tateishi A, Shimizu Y, Oka M, Ogura K, Kawabe T, Ichinose M, Omata M (2006) Successful outcomes of a novel endoscopic treatment for GI tumors: endoscopic submucosal dissection with a mixture of high-molecular-weight hyaluronic acid, glycerin, and sugar. Gastrointest Endosc 63:243–249CrossRefGoogle Scholar
  27. 27.
    Semba S, Kodama Y, Ohnuma K, Mizuuchi E, Masuda R, Yashiro M, Hirakawa K, Yokozaki H (2009) Direct cancer-stromal interaction increases fibroblast proliferation and enhances invasive properties of scirrhous-type gastric carcinoma cells. Br J Cancer 101:1365–1373CrossRefGoogle Scholar
  28. 28.
    Kim SJ, Choi CW, Kang DH, Kim HW, Park SB, Nam HS, Ryu DG (2017) Preoperative predictors of beyond endoscopic submucosal dissection indication or lymphovascular invasion in endoscopic resection for early gastric cancer. Surg Endosc 32:2948–2957CrossRefGoogle Scholar
  29. 29.
    Kim SJ, Choi CW, Kang DH, Kim HW, Park SB, Nam HS, Shin DH (2017) Factors associated with the efficacy of miniprobe endoscopic ultrasonography after conventional endoscopy for the prediction of invasion depth of early gastric cancer. Scand J Gastroenterol 52:864–869CrossRefGoogle Scholar
  30. 30.
    Kikuchi D, Iizuka T, Hoteya S, Yamada A, Furuhata T, Yamashita S, Domon K, Nakamura M, Matsui A, Mitani T, Ogawa O, Watanabe S, Kaise M (2013) Usefulness of magnifying endoscopy with narrow-band imaging for determining tumor invasion depth in early gastric cancer. Gastroenterol Res Pract 2013:217695PubMedPubMedCentralGoogle Scholar
  31. 31.
    Iguchi Y, Niwa Y, Miyahara R, Nakamura M, Banno K, Nagaya T, Nagasaka T, Watanabe O, Ando T, Kawashima H, Ohmiya N, Itoh A, Hirooka Y, Goto H (2009) Pilot study on confocal endomicroscopy for determination of the depth of squamous cell esophageal cancer in vivo. J Gastroenterol Hepatol 24:1733–1739CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Su Jin Kim
    • 1
  • Cheol Woong Choi
    • 1
    Email author
  • Dae Hwan Kang
    • 1
  • Hyung Wook Kim
    • 1
  • Su Bum Park
    • 1
  • Hyeong Seok Nam
    • 1
  • Dae Gon Ryu
    • 1
  1. 1.Department of Internal Medicine, Medical Research Institute, Pusan National University School of Medicine and Research Institute for Convergence of Biomedical Science and TechnologyPusan National University Yangsan HospitalYangsan-siKorea

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