Surgical Endoscopy

, Volume 32, Issue 3, pp 1314–1323 | Cite as

Long-term outcomes of patients with early gastric cancer found to have lesions for which endoscopic treatment is not indicated on histopathological evaluation after endoscopic submucosal dissection

  • Takafumi Yano
  • Kenji Ishido
  • Satoshi Tanabe
  • Takuya Wada
  • Mizutomo Azuma
  • Natsuko Kawanishi
  • Sakiko Yamane
  • Akinori Watanabe
  • Chikatoshi Katada
  • Wasaburo Koizumi



Gastric cancer treatment guidelines recommend additional surgery as the standard treatment for lesions for which endoscopic submucosal dissection (ESD) is not indicated. However, the incidence of lymph-node metastasis is low in most patients.

Methods and materials

The study comprised 231 patients (231 lesions) who underwent ESD for early gastric cancer (EGC) in our hospital from September 2002 through March 2015 and were found to have lesions for which endoscopic treatment is not indicated on histopathological evaluation after ESD. The patients were divided into the additional operation group and the follow-up group, and long-term outcomes were studied retrospectively. Risk factors for metastasis and recurrence were also studied (capture rate, 98.7%).


The median follow-up was 48 months. There were 174 men and 57 women with a median age of 72 years. The additional operation group comprised 118 patients, and the follow-up group comprised 113 patients. The rates of 5-year cause-specific survival and 5-year overall survival were significantly higher in the additional operation group (100 and 96.0%, respectively) than in the follow-up group (92.6 and 73.3%, respectively; p = 0.010, p < 0.001). In the follow-up group, 5 patients (4.4%) died of gastric cancer (p = 0.021). Among elderly patients 75 years or older, long-term outcomes did not differ significantly between the groups. Sixteen patients had metastasis or recurrence, and the presence of lymphatic involvement was an independent risk factor for metastasis, recurrence, or both (p = 0.003; odds ratio 10.594; 95% confidence interval 2.294–48.927).


In patients with EGC who are confirmed to have lesions for which endoscopic treatment is not indicated on histopathological evaluation after ESD, additional surgery should be aggressively performed if the patient can tolerate such treatment. In elderly patients aged 75 years or older and patients with serious underlying diseases, follow-up observation was suggested to be one option in patients who give informed consent after receiving an explanation of the risk of recurrence.


Early gastric cancer Endoscopic submucosal dissection Lesions for which endoscopic treatment is not indicated 



No research support was received for this study.

Compliance with ethical standards


Authors Takafumi Yano, Kenji Ishido, Satoshi Tanabe, Takuya Wada, Mizutomo Azuma, Natsuko Kawanishi, Sakiko Yamane, Akinori Watanabe, Chikatoshi Katada, and Wasaburo Koizumi have no conflicts of interest or financial ties to disclose.

Informed consent

Informed consent was obtained from all patients in accordance with our institutional protocol.


  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:359–386CrossRefGoogle Scholar
  2. 2.
    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 28:3–15CrossRefPubMedGoogle Scholar
  3. 3.
    Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver.4) Gastric cancer 2016 (Published online)Google Scholar
  4. 4.
    Nakata B, Tendo M, Okuyama M, Nakahara K, Ishizu H, Masuda G, Lee T, Hori T, Ohsawa M, Sato H, Ishikawa T (2016) Additional surgical resection after endoscopic mucosal dissection for early gastric cancer: a medium-sized hospital’s experience. Int J Surg 36:335–341CrossRefPubMedGoogle Scholar
  5. 5.
    Gotoda T, Yanagisawa A, Sasako M, 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 3:219–225CrossRefPubMedGoogle Scholar
  6. 6.
    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
  7. 7.
    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 58:331–336CrossRefPubMedGoogle Scholar
  8. 8.
    Tanabe S, Ishido K, Matsumoto T, Kosaka T, Oda I, Suzuki H, Fujisaki J, Ono H, Kawata N, Oyama T, Takahashi A, Doyama H, Kobayashi M, Uedo N, Hamada K, Toyonaga T, Kawara F, Tanaka S, Yoshifuku Y (2017) Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: multicenter collaborative study. Gastric Cancer 20:45–52CrossRefPubMedGoogle Scholar
  9. 9.
    Ishii S, Yamashita K, Kato H, Nishizawa N, Ushiku H, Mieno H, Moriya H, Hosoda K, Katada N, Kikuchi S, Tanabe S, Koizumi W, Saegusa M, Watanabe M (2016) Predictive factors for lymph node metastasis in additional gastrectomy after endoscopic resection of cT1aN0 gastric cancer. Surg Today 46:1031–1038CrossRefPubMedGoogle Scholar
  10. 10.
    Kakushima N, Fujishiro M, Kodashima S, Muraki Y, Tateishi A, Yahagi N, Omata M (2007) Technical feasibility of endoscopic submucosal dissection for gastric neoplasms in the elderly Japanese population. J Gastroenterol Hepatol 22:311–314CrossRefPubMedGoogle Scholar
  11. 11.
    Chinda D, Sasaki Y, Tatsuta T, Tsushima K, Wada T, Shimoyama T, Fukuda S (2015) Perioperative complications of endoscopic submucosal dissection for early gastric cancer in elderly Japanese patients 75 years of age or older. Intern Med 54:267–272CrossRefPubMedGoogle Scholar
  12. 12.
    Ohkuwa M, Hosokawa K, Boku N, Ohtu A, Tajiri H, Yoshida S (2001) New endoscopic treatment for intramucosal gastric tumors using an insulated-tip diathermic knife. Endoscopy 33:221–226CrossRefPubMedGoogle Scholar
  13. 13.
    Ono H, Hasuike N, Inui T, Takizawa K, Ikehara H, Yamaguchi Y, Otake Y, Matsubayashi H (2008) Usefulness of a novel electrosurgical knife, the insulation-tipped diathermic knife-2, for endoscopic submucosal dissection of early gastric cancer. Gastric Cancer 11:47–52CrossRefPubMedGoogle Scholar
  14. 14.
    Hoteya S, Iizuka T, Kikuchi D, Ogawa O, Mitani T, Matsui A, Furuhata T, Yamashita S, Yamada A, Kaise M (2016) Clinicopathological outcomes of patients with early gastric cancer after non-curative endoscopic submucosal dissection. Digestion 93:53–58CrossRefPubMedGoogle Scholar
  15. 15.
    Kusano C, Iwasaki M, Kaltenbach T, Conlin A, Oda I, Gotoda T (2011) Should elderly patients undergo additional surgery after non-curative endoscopic resection for early gastric cancer? Long-term comparative outcomes. Am J Gastroenterol. 106:1064–1069CrossRefPubMedGoogle Scholar
  16. 16.
    Centers for Disease Control and Prevention (2003) Public health and aging: trends in aging—United States and worldwide. JAMA 289:1371–1373CrossRefGoogle Scholar
  17. 17.
    Fried L, Barron J (2005) Older adults. Handbook of urban health: populations, methods, and practice. Springer, New YorkGoogle Scholar
  18. 18.
    Sumiyoshi T, Kondo H, Fujii R, Minagawa T, Fujie S, Kimura T, Ihara H, Yoshizaki N, Hirayama M, Oyamada Y, Okushiba S (2017) Short- and long-term outcomes of endoscopic submucosal dissection for early gastric cancer in elderly patients aged 75 years and older. Gastric Cancer 20:489–495CrossRefPubMedGoogle Scholar
  19. 19.
    Fidler IJ (1995) Clitical factors in the biology of human cancer metastasis. Am Surg 61:1065–1066PubMedGoogle Scholar
  20. 20.
    Hoteya S, Yamashita S, Kikuchi D, Nakamura M, Fujimoto A, Matsui A, Nishida N, Mitani T, Kuroki Y, Iizuka T, Yahagi N (2011) Endoscopic submucosal dissection for submucosal invasive gastric cancer and curability criteria. Dig Endosc 23:30–36CrossRefPubMedGoogle Scholar
  21. 21.
    Kim H, Kim JH, Park JC, Lee YC, Noh SH, Kim H (2011) Lymphovascular invasion is an important predictor of lymph node metastasis in endoscopically resected early gastric cancers. Oncol Rep 25:1589–1595PubMedGoogle Scholar
  22. 22.
    Sunagawa H, Kinoshita T, Kaito A, Shibasaki H, Kaneko K, Ochiai A, Ohtsu A, Nishida T (2016) Additional surgery for non-curative resection after endoscopic submucosal dissection for gastric cancer: a retrospective analysis of 200 cases. Surg Today 47:202–209CrossRefPubMedGoogle Scholar
  23. 23.
    Fujii H, Ishii E, Tochitani S, Nakaji S, Hirata N, Kusanagi H, Narita M (2015) Lymph node metastasis after endoscopic submucosal dissection of a differentiated gastric cancer confined to the mucosa with an ulcer smaller than 30 mm. Dig Endosc 27:159–161CrossRefPubMedGoogle Scholar
  24. 24.
    Sekiguchi M, Oda I, Taniguchi H, Suzuki H, Morita S, Fukagawa T, Sekine S, Kushima R, Katai H (2016) Risk stratification and predictive risk-scoring model for lymph node metastasis in early gastric cancer. J Gastroenterol 51:961–970CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Takafumi Yano
    • 1
  • Kenji Ishido
    • 1
  • Satoshi Tanabe
    • 2
  • Takuya Wada
    • 1
  • Mizutomo Azuma
    • 1
  • Natsuko Kawanishi
    • 1
  • Sakiko Yamane
    • 1
  • Akinori Watanabe
    • 1
  • Chikatoshi Katada
    • 1
  • Wasaburo Koizumi
    • 1
  1. 1.Department of GastroenterologyKitasato University School of MedicineSagamiharaJapan
  2. 2.Research and Development Center for New FrontierKitasato University School of MedicineSagamiharaJapan

Personalised recommendations