Journal of Gastroenterology

, Volume 51, Issue 10, pp 961–970 | Cite as

Risk stratification and predictive risk-scoring model for lymph node metastasis in early gastric cancer

  • Masau Sekiguchi
  • Ichiro Oda
  • Hirokazu Taniguchi
  • Haruhisa Suzuki
  • Shinji Morita
  • Takeo Fukagawa
  • Shigeki Sekine
  • Ryoji Kushima
  • Hitoshi Katai
Original Article—Alimentary Tract



We are increasingly experiencing difficulty in deciding whether to perform gastrectomy after noncurative endoscopic resection of early gastric cancer (EGC) for patients at high risk for surgery. If the differences in risk for lymph node metastasis (LNM) on the basis of noncurative status are understood, the decision becomes easier. The present study aimed to stratify the LNM risk and develop and validate a risk-scoring model for predicting LNM.


By retrospectively reviewing 3131 patients with solitary EGC who underwent gastrectomy with lymphadenectomy at our institution between July 1997 and May 2013, LNM risk was stratified and a risk-scoring model was developed on the basis of the identified independent risk factors for LNM. The scoring was validated using 352 other surgically resected EGC cases. The discriminatory accuracy of the scoring was measured by area under receiver operating characteristic curve (AUROC).


LNM was detected in 386 of 3131 cases. LNM risk in each subgroup, stratified by the identified independent risk factors, such as tumor size, depth, histological type, ulcerative findings, and lymphovascular involvement, considerably varied from 0 % to >50 % even among the current guidelines’ noncurative subgroups. An 11-point scoring model was built, and AUROCs were 0.84 (95 % confidence interval, 0.82–0.86) and 0.82 (0.75–0.88) in the development and validation sets, respectively.


The present study revealed detailed LNM risk stratification data, and developed and validated an 11-point scoring model.


Early gastric cancer Endoscopic resection Lymph node metastasis Mixed-type histology Risk stratification 


Compliance with ethical standards

Conflict of interest

The author(s) declare that they have no competing interests.


  1. 1.
    Rembacken BJ, Gotoda T, Fujii T, et al. Endoscopic mucosal resection. Endoscopy. 2001;33:709–18.CrossRefPubMedGoogle Scholar
  2. 2.
    Ono H, Kondo H, Gotoda T, et al. Endoscopic mucosal resection for treatment of early gastric cancer. Gut. 2001;48:225–9.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Oda I, Gotoda T, Hamanaka H, et al. Endoscopic submucosal dissection for early gastric cancer: technical feasibility, operation time and complications from a large consecutive series. Dig Endosc. 2005;17:54–8.CrossRefGoogle Scholar
  4. 4.
    Oda I, Saito D, Tada M, et al. A multicenter retrospective study of endoscopic resection for early gastric cancer. Gastric Cancer. 2006;9:262–70.CrossRefPubMedGoogle Scholar
  5. 5.
    Sano T, Okuyama Y, Kobori O, et al. Early gastric cancer. Endoscopic diagnosis of depth of invasion. Dig Dis Sci. 1990;35:1340–4.CrossRefPubMedGoogle Scholar
  6. 6.
    Seto Y, Shimoyama S, Kitayama J, et al. Lymph node metastasis and preoperative diagnosis of depth of invasion in early gastric cancer. Gastric Cancer. 2001;4:34–8.CrossRefPubMedGoogle Scholar
  7. 7.
    Choi J, Kim SG, Im JP, et al. Comparison of endoscopic ultrasonography and conventional endoscopy for prediction of depth of tumor invasion in early gastric cancer. Endoscopy. 2010;42:705–13.CrossRefPubMedGoogle Scholar
  8. 8.
    Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14:113–23.CrossRefGoogle Scholar
  9. 9.
    Gotoda T, Yanagisawa A, Sasako M, et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer. 2000;3:219–25.CrossRefPubMedGoogle Scholar
  10. 10.
    Hirasawa T, Gotoda T, Miyata S, et al. Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer. 2009;12:148–52.CrossRefPubMedGoogle Scholar
  11. 11.
    Hanaoka N, Tanabe S, Mikami T, et al. Mixed-histologic-type submucosal invasive gastric cancer as a risk factor for lymph node metastasis: feasibility of endoscopic submucosal dissection. Endoscopy. 2009;41:427–32.CrossRefPubMedGoogle Scholar
  12. 12.
    Takizawa K, Ono H, Kakushima N, et al. 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. 2013;16:531–6.CrossRefPubMedGoogle Scholar
  13. 13.
    Lee JH, Choi IJ, Han HS, et al. Risk of lymph node metastasis in differentiated type mucosal early gastric cancer mixed with minor undifferentiated type histology. Ann Surg Oncol. 2015;22:1813–9.CrossRefPubMedGoogle Scholar
  14. 14.
    Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRefGoogle Scholar
  15. 15.
    Noguchi Y. Blood vessel invasion in gastric carcinoma. Surgery. 1990;107:140–8.PubMedGoogle Scholar
  16. 16.
    Arigami T, Natsugoe S, Uenosono Y, et al. Lymphatic invasion using D2-40 monoclonal antibody and its relationship to lymph node micrometastasis in pN0 gastric cancer. Br J Cancer. 2005;93:688–93.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Yonemura Y, Endou Y, Tabachi K, et al. Evaluation of lymphatic invasion in primary gastric cancer by a new monoclonal antibody, D2-40. Hum Pathol. 2006;37:1193–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Moons KG, Kengne AP, Woodward M, et al. Risk prediction models: I. Development, internal validation, and assessing the incremental value of a new (bio)marker. Heart. 2012;98:683–90.CrossRefPubMedGoogle Scholar
  19. 19.
    Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143:29–36.CrossRefPubMedGoogle Scholar
  20. 20.
    Sasako M, Kinoshita T, Maruyama K. Prognosis of early gastric cancer (in Japanese with English abstract). Stom Intest. 1993;28(Suppl):139–46.Google Scholar
  21. 21.
    Sano T, Sasako M, Kinoshita T, et al. Recurrence of early gastric cancer. Follow-up of 1475 patients and review of the Japanese literature. Cancer. 1993;72:3174–8.CrossRefPubMedGoogle Scholar
  22. 22.
    Saka M, Katai H, Fukagawa T, et al. Recurrence in early gastric cancer with lymph node metastasis. Gastric Cancer. 2008;11:214–8.CrossRefPubMedGoogle Scholar
  23. 23.
    Kitano S, Shiraishi N, Uyama I, Japanese Laparoscopic Surgery Study Group, et al. A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg. 2007;245:68–72.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Korenaga D, Orita H, Maekawa S, et al. Pathological appearance of the stomach after endoscopic mucosal resection for early gastric cancer. Br J Surg. 1997;84:1563–6.CrossRefPubMedGoogle Scholar
  25. 25.
    Nagano H, Ohyama S, Fukunaga T, et al. Indications for gastrectomy after incomplete EMR for early gastric cancer. Gastric Cancer. 2005;8:149–54.CrossRefPubMedGoogle Scholar
  26. 26.
    Ryu KW, Choi IJ, Doh YW, et al. Surgical indication for non-curative endoscopic resection in early gastric cancer. Ann Surg Oncol. 2007;14:3428–34.CrossRefPubMedGoogle Scholar
  27. 27.
    Oda I, Gotoda T, Sasako M, et al. Treatment strategy after non-curative endoscopic resection of early gastric cancer. Br J Surg. 2008;95:1495–500.CrossRefPubMedGoogle Scholar
  28. 28.
    Son SY, Park JY, Ryu KW, et al. The risk factors for lymph node metastasis in early gastric cancer patients who underwent endoscopic resection: is the minimal lymph node dissection applicable? A retrospective study. Surg Endosc. 2013;27:3247–53.CrossRefPubMedGoogle Scholar
  29. 29.
    Yang HJ, Kim SG, Lim JH, et al. Predictors of lymph node metastasis in patients with non-curative endoscopic resection of early gastric cancer. Surg Endosc. 2015;29:1145–55.CrossRefPubMedGoogle Scholar
  30. 30.
    Sekiguchi M, Suzuki H, Oda I, et al. Favorable long-term outcomes of endoscopic submucosal dissection for locally recurrent early gastric cancer after endoscopic resection. Endoscopy. 2013;45:708–13.CrossRefPubMedGoogle Scholar
  31. 31.
    Sekiguchi M, Suzuki H, Oda I, et al. Risk of recurrent gastric cancer after endoscopic resection with a positive lateral margin. Endoscopy. 2014;46:273–8.CrossRefPubMedGoogle Scholar
  32. 32.
    Sekiguchi M, Sekine S, Oda I, et al. Risk factors for lymphatic and venous involvement in endoscopically resected gastric cancer. J Gastroenterol. 2013;48:706–12.CrossRefPubMedGoogle Scholar
  33. 33.
    Kenis C, Decoster L, Van Puyvelde K, et al. Performance of two geriatric screening tools in older patients with cancer. J Clin Oncol. 2014;32:19–26.CrossRefPubMedGoogle Scholar
  34. 34.
    Odagaki T, Suzuki H, Oda I, et al. Small undifferentiated intramucosal gastric cancer with lymph-node metastasis: case report. World J Gastroenterol. 2013;19:3157–60.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kurokawa Y, Hasuike N, Ono H, Gastrointestinal Oncology Study Group of Japan Clinical Oncology Group, et al. A phase II trial of endoscopic submucosal dissection for mucosal gastric cancer: Japan Clinical Oncology Group Study JCOG0607. Jpn J Clin Oncol. 2009;39:464–6.CrossRefPubMedGoogle Scholar
  36. 36.
    Oda I, Shimazu T, Ono H, et al. Design of Japanese multicenter prospective cohort study of endoscopic resection for early gastric cancer using Web registry (J-WEB/EGC). Gastric Cancer. 2012;15:451–4.CrossRefPubMedGoogle Scholar
  37. 37.
    Takizawa K, Takashima A, Kimura A, et al. Gastrointestinal Endoscopy Study Group (GIESG) of Japan Clinical Oncology Group (JCOG), Stomach Cancer Study Group (SCSG) of Japan Clinical Oncology Group (JCOG). A phase II clinical trial of endoscopic submucosal dissection for early gastric cancer of undifferentiated type: Japan Clinical Oncology Group study JCOG1009/1010. Jpn J Clin Oncol. 2013;43:87–91.CrossRefPubMedGoogle Scholar
  38. 38.
    Moons KG, Kengne AP, Grobbee DE, et al. Risk prediction models: II. External validation, model updating, and impact assessment. Heart. 2012;98:691–8.CrossRefPubMedGoogle Scholar

Copyright information

© Japanese Society of Gastroenterology 2016

Authors and Affiliations

  • Masau Sekiguchi
    • 1
  • Ichiro Oda
    • 1
  • Hirokazu Taniguchi
    • 2
  • Haruhisa Suzuki
    • 1
  • Shinji Morita
    • 3
  • Takeo Fukagawa
    • 3
  • Shigeki Sekine
    • 2
  • Ryoji Kushima
    • 2
    • 4
  • Hitoshi Katai
    • 3
  1. 1.Endoscopy DivisionNational Cancer Center HospitalTokyoJapan
  2. 2.Pathology and Clinical Laboratory DivisionNational Cancer Center HospitalTokyoJapan
  3. 3.Gastric Surgery DivisionNational Cancer Center HospitalTokyoJapan
  4. 4.Department of Clinical Laboratory Medicine and Diagnostic PathologyShiga University of Medical ScienceShigaJapan

Personalised recommendations