Surgical Endoscopy

, Volume 28, Issue 2, pp 639–647 | Cite as

Clinical validity of the expanded criteria for endoscopic resection of undifferentiated-type early gastric cancer based on long-term outcomes

  • Shiro OkaEmail author
  • Shinji Tanaka
  • Makoto Higashiyama
  • Norifumi Numata
  • Yoji Sanomura
  • Shigeto Yoshida
  • Koji Arihiro
  • Kazuaki Chayama



According to the Japanese Gastric Cancer Treatment Guidelines, the expanded criteria for endoscopic resection (ER) of undifferentiated-type early gastric cancer (UEGC) is ulcer-negative, intramucosal cancer 20 mm or less in diameter without lymphovascular invasion. The aim of this study was to confirm validity of the expanded criteria for curative ER of UEGC.


Subjects were 125 patients from whom 125 UEGCs were resected endoscopically between April 1990 and March 2011. Endoscopic mucosal resection (EMR) (28 lesions, 28 patients) or endoscopic submucosal dissection (ESD) (97 lesions, 97 patients) was performed. We determined the complete resection rate, post-ER bleeding rate, perforation rate, and outcome in both groups, and analyzed the survival outcomes of 84 patients who were followed for more than 5 years (mean, 101.9 months) according to the indication for ER [expanded criteria for curative (n = 52) vs. criteria for noncurative (n = 32)].


Complete resection rates for EMR and ESD were 54 % (15 of 28) and 89 % (86 of 97), respectively, with that for ESD being significantly higher (p < 0.01). Outcomes after ER were as follows: among 52 cases of UEGC meeting the expanded criteria, additional surgical resection was performed in 11 cases of incomplete resection. No local recurrence or lymph node metastasis was observed. Forty-eight patients who were simply surveyed clinically (93.6 ± 38.4 months) after ER survived without recurrence; the remaining 7 patients died of other causes. Among the 32 cases of UEGC meeting the criteria for noncurative resection, additional surgical resection was performed in 13 cases. Among the 19 follow-up cases (108.3 ± 38.7 months), death due to metastasis of the primary disease occurred in 3 cases, death from other causes occurred in 5 cases, and local residual submucosal recurrence occurred in 1 case.


ESD is a useful technique for complete resection as a total excisional biopsy compared with EMR and radical cure of UEGCs meeting the expanded criteria.


Endoscopic mucosal resection Endoscopic submucosal dissection Outcome Undifferentiated-type early gastric cancer 



Shiro Oka, Shinji Tanaka, Makoto Higashiyama, Norifumi Numata, Yoji Sanomura, Shigeto Yoshida, Koji Arihiro, and Kazuaki Chayama have no conflicts of interest or financial ties to disclose.


  1. 1.
    Yamao T, Shirao K, Ono H, Kondo H, Saito D, Yamaguchi H, Sasako M, Sano T, Ochiai A, Yoshida S (1996) Risk factors for lymph node metastasis from intramucosal gastric carcinoma. Cancer 77:602–606PubMedCrossRefGoogle Scholar
  2. 2.
    Adachi Y, Mori M, Maehara Y, Sugimachi K (1997) Prognostic factors of node-negative gastric carcinoma: univariate and multivariate analyses. J Am Coll Surg 184:373–377PubMedGoogle Scholar
  3. 3.
    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 3:219–225PubMedCrossRefGoogle Scholar
  4. 4.
    Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma, 3rd English edn. Gastric Cancer 14:101–112CrossRefGoogle Scholar
  5. 5.
    Yamamoto Y, Fujisaki J, Hirasawa T, Ishiyama A, Yoshimoto K, Ueki N, Chino A, Tsuchida T, Hoshino E, Hiki N, Fukunaga T, Sano T, Yamaguchi T, Takahashi H, Miyata S, Yamamoto N, Kato Y, Igarashi M (2010) Therapeutic outcomes of endoscopic submucosal dissection of undifferentiated-type intramucosal gastric cancer without ulceration and preoperatively diagnosed as 20 millimeters or less in diameter. Dig Endosc 22:112–118PubMedCrossRefGoogle Scholar
  6. 6.
    Kang HY, Kim SG, Kim JS, Jung HC, Song IS (2010) Clinical outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Surg Endosc 24:509–516PubMedCrossRefGoogle Scholar
  7. 7.
    Park J, Choi KD, Kim MY, Lee JH, Song HJ, Lee GH, Jung HY, Kim JH (2012) Is endoscopic resection an acceptable treatment for undifferentiated EGC? Hepatogastroenterology 59:607–611PubMedCrossRefGoogle Scholar
  8. 8.
    Kamada K, Tomatsuri N, Yoshida N (2012) Endoscopic submucosal dissection for undifferentiated early gastric cancer as the expanded indication lesion. Digestion 85:111–115PubMedCrossRefGoogle Scholar
  9. 9.
    Okada K, Fujisaki J, Yoshida T, Ishikawa H, Suganuma T, Kasuga A, Omae M, Kubota M, Ishiyama A, Hirasawa T, Chino A, Inamori M, Yamamoto Y, Yamamoto N, Tsuchida T, Tamegai Y, Nakajima A, Hoshino E, Igarashi M (2012) Long-term outcomes of endoscopic submucosal dissection for undifferentiated-type early gastric cancer. Endoscopy 44:122–127PubMedCrossRefGoogle Scholar
  10. 10.
    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 64:877–883PubMedCrossRefGoogle Scholar
  11. 11.
    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 15:97–105PubMedCrossRefGoogle Scholar
  12. 12.
    Higashiyama M, Oka S, Tanaka S, Sanomura Y, Imagawa H, Shishido T, Yoshida S, Chayama K (2011) Risk factors for bleeding after endoscopic submucosal dissection of gastric epithelial neoplasm. Dig Endosc 23:290–295PubMedCrossRefGoogle Scholar
  13. 13.
    Tajiri H, Kitano S (2004) Complications associated with endoscopic mucosal resection: definition of bleeding that can be viewed as accidental. Dig Endosc 16:134–136CrossRefGoogle Scholar
  14. 14.
    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 15:764–769PubMedCrossRefGoogle Scholar
  15. 15.
    Li H, Lu P, Lu Y, Liu CG, Xu HM, Wang SB, Chen JQ (2008) Predictive factors for lymph node metastasis in poorly differentiated early gastric cancer and their impact on the surgical strategy. World J Gastroenterol 226:4222–4226CrossRefGoogle Scholar
  16. 16.
    Ha TK, An JY, Youn HK, Noh JH, Sohn TS, Kim S (2008) Indication for endoscopic mucosal resection in early signet ring cell gastric cancer. Ann Surg Oncol 15:508–513PubMedCrossRefGoogle 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 23:46–50PubMedCrossRefGoogle Scholar
  18. 18.
    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 188:181–184PubMedCrossRefGoogle Scholar
  19. 19.
    Nasu J, Nishina T, Hirasaki S, Moriwaki T, Hyodo I, Kurita A, Nishimura R (2006) Predictive factors of lymph node metastasis in patients with undifferentiated early gastric cancers. J Clin Gastroenterol 40:412–415PubMedCrossRefGoogle Scholar
  20. 20.
    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 40:7–10PubMedCrossRefGoogle Scholar
  21. 21.
    Nakahara K, Tsuruta O, Tateishi H, Watanabe Y, Tamiya Y, Serikawa O, Kaminato K, Sata M, Arima N (2007) Radiological diagnosis of the depressed type of gastric submucosal cancer without fold convergence-based on the vertical invasive depth of a differentiated-type submucosal cancer. Stomach Intest (Tokyo) 42:25–38 (in Japanese with English abstract)Google Scholar
  22. 22.
    Isobe S, Yoshino J, Inui K, Wakabayashi T, Okushima K, Kobayashi T, Miyoshi H, Nakamura Y, Kato Y, Kimura Y (2007) Endosonographic diagnosis of the depth of cancerous invasive of differentiated type gastric cancer. Stomach Intest (Tokyo) 42:79–87 (in Japanese with English abstract)Google Scholar
  23. 23.
    Mouri R, Yoshida S, Tanaka S, Oka S, Yoshihara M, Chayama K (2009) Usefulness of endoscopic ultrasonography in determining the depth of invasion and indication for endoscopic treatment of early gastric cancer. J Clin Gastroenterol 43:318–322PubMedCrossRefGoogle Scholar
  24. 24.
    Nagahama T, Yao K, Maki S, Yasaka M, Takaki Y, Matsui T, Tanabe H, Iwashita A, Ota A (2011) Usefulness of magnifying endoscopy with narrow-band imaging for determining the horizontal extent of early gastric cancer when there is an unclear margin by chromoendoscopy (with video). Gastrointest Endosc 74:1259–1267PubMedCrossRefGoogle Scholar
  25. 25.
    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 9:262–270PubMedCrossRefGoogle Scholar
  26. 26.
    Oka S, Tanaka S, Kaneko I, Mouri R, Hirata M, Kanao H, Kawamura T, Yoshida S, Yoshihara M, Chayama K (2006) Endoscopic submucosal dissection for residual/local recurrence of early gastric cancer after endoscopic mucosal resection. Endoscopy 38:996–1000PubMedCrossRefGoogle Scholar
  27. 27.
    Sano T, Sasako M, Kinoshita T, Maruyama K (1993) Recurrence of early gastric cancer. Follow-up of 1475 patients and review of the Japanese literature. Cancer 72:3174–3178PubMedCrossRefGoogle Scholar
  28. 28.
    Maruyama K, Kaminishi M, Hayashi K, Isobe Y, Honda I, Katai H, Arai K, Kodera Y, Nashimoto A (2006) Gastric cancer treated in 1991 in Japan: data analysis of nationwide registry. Gastric Cancer 9:51–66PubMedCrossRefGoogle Scholar
  29. 29.
    Kitano S, Shiraishi N, Uyama I, Sugihara K, Tanigawa N (2007) A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg 245:68–72PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Goto O, Fujishiro M, Kodashima S, Ono S, Omata M (2009) Outcomes of endoscopic submucosal dissection for early gastric cancer with special reference to validation for curability criteria. Endoscopy 41:118–122PubMedCrossRefGoogle Scholar
  31. 31.
    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 97:868–871PubMedCrossRefGoogle Scholar
  32. 32.
    Yanagita S, Natsugoe S, Uenosono Y, Kozono T, Ehi K, Arigami T, Arima H, Ishigami S, Aikou T (2008) Sentinel node micrometastases have high proliferative potential in gastric cancer. J Surg Res 145:238–243PubMedCrossRefGoogle Scholar
  33. 33.
    Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Higashi H, Watanabe T, Aridome K, Hokita S, Aikou T (2003) Clinical impact of micrometastasis of the lymph node in gastric cancer. Am Surg 69:573–577PubMedGoogle Scholar
  34. 34.
    Nakajo A, Natsugoe S, Ishigami S, Matsumoto M, Nakashima S, Hokita S, Baba M, Takao S, Aikou T (2001) Detection and prediction of micrometastasis in the lymph nodes of patients with pN0 gastric cancer. Ann Surg Oncol 8:158–162PubMedCrossRefGoogle Scholar
  35. 35.
    Hirasawa T, Fujisaki J, Fukunaga T, Yamamoto Y, Yamaguchi T, Katori M, Yamamoto N (2010) Lymph node metastasis from undifferentiated-type mucosal gastric cancer satisfying the expanded criteria for endoscopic resection based on routine histological examination. Gastric Cancer 13:267–270PubMedCrossRefGoogle Scholar
  36. 36.
    Nasu J, Hori S, Asagi A, Nishina T, Ikeda Y, Tanimizu M, Iguchi H, Aogi K, Kurita A, Nishimura R (2010) A case of small undifferentiated intramucosal gastric cancer with lymph node metastasis. Gastric Cancer 13:264–266PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Shiro Oka
    • 1
    Email author
  • Shinji Tanaka
    • 1
  • Makoto Higashiyama
    • 2
  • Norifumi Numata
    • 2
  • Yoji Sanomura
    • 1
  • Shigeto Yoshida
    • 1
  • Koji Arihiro
    • 3
  • Kazuaki Chayama
    • 2
  1. 1.Department of EndoscopyHiroshima University HospitalHiroshimaJapan
  2. 2.Department of Gastroenterology and MetabolismHiroshima University HospitalHiroshimaJapan
  3. 3.Department of PathologyHiroshima University HospitalHiroshimaJapan

Personalised recommendations