Gastric Cancer

, Volume 22, Issue 1, pp 123–129 | Cite as

Validation of the prognostic impact of the new tumor-node-metastasis clinical staging in patients with gastric cancer

  • Etsuro Bando
  • Rie Makuuchi
  • Tomoyuki Irino
  • Yutaka Tanizawa
  • Taiichi Kawamura
  • Masanori Terashima
Original Article



In the 8th edition of the tumor-node-metastasis (TNM) classification, the gastric cancer staging system includes two classifications: the clinical stage (cStage) and the postoperative pathologic stage. However, the correlation between the new cStage and overall survival has not been studied. Moreover, clinical N (cN) grade analysis is not included in the new clinical staging system. This study validated the prognostic value of cStage in the 8th edition of the TNM classification and the significance of N classification for pretreatment staging in gastric cancer.


A total of 4374 patients with primary gastric cancer who underwent surgery at the Shizuoka Cancer Center were included. Survival analysis was conducted based on the newly proposed cStage criteria of the TNM 8th edition. Prognostic accuracy was evaluated using Harrell’s concordance index (C-index).


The five-year survival rates according to cStage were as follows: cStageI, 91.2%, cStageIIA: 75.1%, cStageIIB: 57.7%, cStageIII: 43.2%, cStageIVA: 31.6%, and cStageIVB: 7.7%. Significant differences were observed among all stages (P < 0.001). The cStage C-index was 0.802. Meanwhile, the five-year survival rates based on cN were as follows: cN0: 83.7%, cN1: 57.2%, cN2: 42.4%, cN3a: 22.1%, and cN3b: 0.0%. Significant differences were also observed among all cN grades (P < 0.001).


The cStage of the 8th edition of the TNM classification has a good capability to predict prognosis; thus, it may be a useful indicator for selecting appropriate gastric cancer treatment modalities. In addition, cN can be included in developing a more precise clinical staging of gastric cancer.


Stomach neoplasms Neoplasm staging Survival 



This study was supported in part by a scientific research grant from multi-institutional trials to establish a new standard treatment of solid tumors in adults from the National Cancer Center Research and Development Fund (26-A-4) and Practical Research for Innovative Cancer Control from the Japan Agency for Medical Research and Development, AMED (15ck0106043h0002).

Compliance with ethical standards

Conflicts of Interest

The authors declare that they have no conflict of interest.

Ethical standards

All procedures performed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1964 and later versions. Informed consent or an appropriate substitute was obtained from all patients prior to inclusion in the study.

Supplementary material

10120_2018_799_MOESM1_ESM.docx (31 kb)
Supplementary material 1 (DOCX 31 kb)
10120_2018_799_MOESM2_ESM.pptx (398 kb)
Supplementary material 2 (PPTX 398 kb)
10120_2018_799_MOESM3_ESM.docx (30 kb)
Supplementary material 3 (DOCX 30 kb)


  1. 1.
    Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, et al., editors. AJCC cancer staging manual. 8th ed. New York: Springer; 2016.Google Scholar
  2. 2.
    Brierley J, Gospodarowicz M, Wittekind C, editors. TNM classification of malignant tumours. 8th ed. New York: Wiley-Blackwell; 2017.Google Scholar
  3. 3.
    Sobin L, Gospodarowicz M, Wittekind C, editors. TNM classification of malignant tumours. 7th ed. New York: Wiley-Blackwell; 2009.Google Scholar
  4. 4.
    Sano T, Coit DG, Kim HH, Roviello F, Kassab P, Wittekind C, et al. For the IGCA staging project. Proposal of a new stage grouping of gastric cancer: international Gastric Cancer Association Staging Project. Gastric Cancer. 2017;20:217–25.CrossRefGoogle Scholar
  5. 5.
    National Comprehensive Cancer Network Guidelines. (Accessed April 10th 2017).
  6. 6.
    Waddell T, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D. European Society for Medical Oncology (ESMO), European Society of Surgical Oncology (ESSO), European Society of Radiotherapy and Oncology (ESTRO). Gastric cancer: ESMO-ESSO-ESTRO clinical practice guidelines for diagnosis, treatment and follow-up. Eur J Surg Oncol. 2014;40:584–91.CrossRefGoogle Scholar
  7. 7.
    Ahn HS, Lee HJ, Hahn S, Kim WH, Lee KU, Sano T, et al. Evaluation of the seventh American Joint Committee on Cancer/International Union Against Cancer Classification of gastric adenocarcinoma in comparison with the sixth classification. Cancer. 2010;116:5592–8.CrossRefGoogle Scholar
  8. 8.
    Jung H, Lee HH, Song KY, Jeon HM, Park CH. Validation of the seventh edition of the American Joint Committee on Cancer TNM staging system for gastric cancer. Cancer. 2011;117:2371–8.Google Scholar
  9. 9.
    Wang J, Dang P, Raut CP, Pandalai PK, Maduekwe UN, Rattner DW, et al. Comparison of a lymph node ratio-based staging system with the 7th AJCC system for gastric cancer: analysis of 18,043 patients from the SEER database. Ann Surg. 2012;255:478–85.CrossRefGoogle Scholar
  10. 10.
    Marrelli D, Morgagni P, de Manzoni G, Coniglio A, Marchet A, Saragoni L, et al. Italian Research Group for Gastric Cancer (IRGGC). Prognostic value of the 7th AJCC/UICC TNM classification of noncardia gastric cancer: analysis of a large series from specialized Western centers. Ann Surg. 2012;255:486–91.CrossRefGoogle Scholar
  11. 11.
    Park SR, Kim MJ, Ryu KW, Lee JH, Lee JS, Nam BH, et al. Prognostic value of preoperative clinical staging assessed by computed tomography in resectable gastric cancer patients: a viewpoint in the era of preoperative treatment. Ann Surg. 2010;251:428–35.CrossRefGoogle Scholar
  12. 12.
    Bando E, Makuuchi R, Tokunaga M, Tanizawa Y, Kawamura T, Terashima M. Impact of clinical tumor-node-metastasis staging on survival in gastric carcinoma patients receiving surgery. Gastric Cancer. 2017;20:448–56.CrossRefGoogle Scholar
  13. 13.
    Ono H, Yoshida Y. Endoscopic diagnosis of the depth of cancer invasion for gastric cancer. Stomach Intest. 2001;36:334–40 (in Japanese with English abstract).Google Scholar
  14. 14.
    Abe S, Oda I, Shimazu T, Kinjo T, Tada K, Sakamoto T, et al. Depth-predicting score for differentiated early gastric cancer. Gastric Cancer. 2011;14:35–40.CrossRefGoogle Scholar
  15. 15.
    Egahira H, Baba Y, Kato H. Diagnosis of the depth of invasion of gastric cancer, diagnostic indicator of the depth of invasion by the radiological examination. Stomach Intest. 2001;36:321–33 (in Japanese with English abstract).Google Scholar
  16. 16.
    Kumano S, Murakami T, Kim T, Hori M, Iannaccone R, Nakata S, et al. T staging of gastric cancer: role of multi-detector row CT. Radiology. 2005;237:961–6.CrossRefGoogle Scholar
  17. 17.
    Liao SR, Dai Y, Huo L, Yan K, Zhang L, Zhang H, et al. Transabdominal ultrasonography in preoperative staging of gastric cancer. World J Gastroenterol. 2004;10:3399–404.CrossRefGoogle Scholar
  18. 18.
    Kim SK, Kang KW, Lee JS, Kim HK, Chang HJ, Choi JY, et al. Assessment of lymph node metastases using 18F-FDG PET in patients with advanced gastric cancer. Eur J Nucl Med Mol Imaging. 2006;33:148–55.CrossRefGoogle Scholar
  19. 19.
    Association Japanese Gastric Cancer. Japanese gastric cancer treatment guidelines 2014 (Ver. 4). Gastric Cancer. 2017;20:1–19.CrossRefGoogle Scholar
  20. 20.
    Koh DM, Collins DJ, Wallace T, Chau I, Riddell AM. Combining diffusion-weighted MRI with Gd-EOB-DTPA-enhanced MRI improves the detection of colorectal liver metastases. Br J Radiol. 2012;85:980–9.CrossRefGoogle Scholar
  21. 21.
    Tatsubayashi T, Tanizawa Y, Miki Y, Tokunaga M, Bando E, Kawamura T, et al. Treatment outcomes of hepatectomy for liver metastases of gastric cancer diagnosed using contrast-enhanced magnetic resonance imaging. Gastric Cancer. 2017;20:387–93.CrossRefGoogle Scholar
  22. 22.
    Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15:361–87.CrossRefGoogle Scholar
  23. 23.
    Hosmer D, Lemeshow S 2nd, editors. Applied logistic regression. New York: Wiley; 2000.Google Scholar
  24. 24.
    Harrell FE. Regression modeling strategies with applications to linear models, logistic regression, and survival analysis. New York: Springer; 2001.Google Scholar
  25. 25.
    Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.Google Scholar
  26. 26.
    Fukagawa T, Katai H, Mizusawa J, Nakamura K, Sano T, Terashima M, et al. Stomach Cancer Study Group of the Japan Clinical Oncology Group. A prospective multi-institutional validity study to evaluate the accuracy of clinical diagnosis of pathological stage III gastric cancer (JCOG1302A). Gastric Cancer. 2017. [Epub ahead of print].
  27. 27.
    Razavi SM, Khodadost M, Sohrabi M, Keshavarzi A, Zamani F, Rakhshani N, et al. Accuracy of endoscopic ultrasonography for determination of tumor invasion depth in gastric cancer. Asian Pac J Cancer Prev. 2015;16:3141–5.CrossRefGoogle Scholar
  28. 28.
    Pei Q, Wang L, Pan J, Ling T, Lv Y, Zou X. Endoscopic ultrasonography for staging depth of invasion in early gastric cancer: a meta-analysis. J Gastroenterol Hepatol. 2015;30:1566–73.CrossRefGoogle Scholar
  29. 29.
    Park JS, Kim H, Bang B, Kwon K, Shin Y. Accuracy of endoscopic ultrasonography for diagnosing ulcerative early gastric cancers. Medicine (Baltimore). 2016;95:e3955. Scholar
  30. 30.
    Kattan MW, Hess KR, Amin MB, Lu Y, Moons KG, Gershenwald JE, et al. American Joint Committee on Cancer acceptance criteria for inclusion of risk models for individualized prognosis in the practice of precision medicine. CA Cancer J Clin. 2016;66:370–4.CrossRefGoogle Scholar
  31. 31.
    Kattan MW, Karpeh MS, Mazumdar M, Brennan MF. Postoperative nomogram for disease-specific survival after an R0 resection for gastric carcinoma. J Clin Oncol. 2003;21:3647–50.CrossRefGoogle Scholar

Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2018

Authors and Affiliations

  1. 1.Division of Gastric SurgeryShizuoka Cancer CenterSuntougunJapan

Personalised recommendations