Journal of Gastroenterology

, Volume 41, Issue 9, pp 884–892 | Cite as

A modified Japan Integrated Stage score for prognostic assessment in patients with hepatocellular carcinoma

  • Iwao Ikai
  • Kenichi Takayasu
  • Masao Omata
  • Kiwamu Okita
  • Yasuni Nakanuma
  • Yutaka Matsuyama
  • Masatoshi Makuuchi
  • Masamichi Kojiro
  • Takafumi Ichida
  • Shigeki Arii
  • Yoshio Yamaoka
  • for the Liver Cancer Study Group of Japan



For patients with hepatocellular carcinoma (HCC), the selection of effective therapeutic options depends on a reliable prognostic assessment of both the tumor characteristics and liver impairment. This study sought to provide a modified Japan Integrated Stage (m-JIS) score to predict more accurately the survival of patients with HCC.


We analyzed the records of 42 269 patients diagnosed with HCC that were registered between 1992 and 1999 in a nationwide Japanese database. The m-JIS score was calculated from the tumor-node-metastasis stage and the grade of liver damage as defined by the Liver Cancer Study Group of Japan. The predictive accuracy for patient survival based on the m-JIS score was compared with that determined by the modified Cancer of the Liver Italian Program (m-CLIP) score using the cross-validation method.


Patients were divided randomly into two groups, a training sample for construction of prediction models (n = 21 127 patients with 8458 deaths) and a validation sample for assessment of those prediction models (n = 21 142 patients with 8434 deaths). Both the m-JIS score and the m-CLIP score showed good discriminatory ability in the training sample. In the validation sample, the residuals of prediction based on the m-JIS score were smaller than those of the m-CLIP score (P < 0.0001).


The m-JIS scoring system had better predictive accuracy than the m-CLIP score system for survival of Japanese patients with HCC.

Key words

TNM Stage degree of liver damage nationwide survey database Liver Cancer Study Group of Japan CLIP score 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bosch, FX, Ribes, J, Borras, J 1999Epidemiology of primary liver cancerSemin Liver Dis1927185PubMedGoogle Scholar
  2. 2.
    Ikai, I, Arii, S, Ichida, T, Okita, K, Omata, M, Kojiro, M,  et al. 2005Report of the 16th follow-up survey of primary liver cancerHepatol Res3216372PubMedCrossRefGoogle Scholar
  3. 3.
    The Liver Cancer Study Group of Japan1990Primary liver cancer in Japan. Clinicopathologic features and results of surgical treatmentAnn Surg21127787Google Scholar
  4. 4.
    The Liver Cancer Study Group of Japan1994Predictive factors for long term prognosis after partial hepatectomy for patients with hepatocellular carcinomaCancer74277280CrossRefGoogle Scholar
  5. 5.
    Arii, S, Yamaoka, Y, Futagawa, S, Inoue, K, Kobayashi, K, Kojiro, M,  et al. 2000Results of surgical and nonsurgical treatment for small-sized hepatocellular carcinomas: a retrospective and nationwide survey in Japan. The Liver Cancer Study Group of JapanHepatology3212249PubMedCrossRefGoogle Scholar
  6. 6.
    Ikai, I, Arii, S, Kojiro, M, Ichida, T, Makuuchi, M, Matsuyama, Y,  et al. 2004Re-evaluation of prognostic factors for survival after liver resection in patients with hepatocellular carcinoma in a Japanese nationwide surveyCancer101796802PubMedCrossRefGoogle Scholar
  7. 7.
    Live Cancer Study Group of Japan. General rules for the clinical and pathological study of primary liver cancer. 2nd English ed. Tokyo: Kanehara; 2003Google Scholar
  8. 8.
    Wildi, S, Pestalozzi, BC, McCormack, L, Clavien, PA 2004Critical evaluation of the different staging systems for hepatocellular carcinomaBr J Surg914008PubMedCrossRefGoogle Scholar
  9. 9.
    The Cancer of the Liver Italian Program (CLIP) investigators1998A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patientsHepatology287515CrossRefGoogle Scholar
  10. 10.
    Llovet, JM, Bru, C, Bruix, J 1999Prognosis of hepatocellular carcinoma: the BCLC staging classificationSemin Liver Dis1932938PubMedCrossRefGoogle Scholar
  11. 11.
    Leung, TW, Tang, AM, Zee, B, Lau, WY, Lai, PB, Leung, KL,  et al. 2002Construction of the Chinese University Prognostic Index for hepatocellular carcinoma and comparison with the TNM staging system, the Okuda staging system, and the Cancer of the Liver Italian Program staging system: a study based on 926 patientsCancer9417609PubMedCrossRefGoogle Scholar
  12. 12.
    Kudo, M, Chung, H, Osaki, Y 2003Prognostic staging system for hepatocellular carcinoma (CLIP score): its value and limitations, and a proposal for a new staging system, the Japan Integrated Staging score (JIS score)J Gastroenterol3820715PubMedCrossRefGoogle Scholar
  13. 13.
    Kudo, M, Chung, H, Haji, S, Osaki, Y, Oka, H, Seki, T,  et al. 2004Validation of a new prognostic staging system for hepatocellular carcinoma: the JIS score compared with the CLIP scoreHepatology401396405PubMedCrossRefGoogle Scholar
  14. 14.
    Liang, K-Y, Zeger, SL 1986Longitudinal data analysis using generalized linear modelsBiometrika731322CrossRefGoogle Scholar
  15. 15.
    Okuda, K, Ohtsuki, T, Obata, H, Tomimatsu, M, Okazaki, N, Hasegawa, H,  et al. 1985Natural history of hepatocellular carcinoma and prognosis in relation to treatment. Study of 850 patientsCancer5691828PubMedCrossRefGoogle Scholar
  16. 16.
    International Union2002Against Cancer. TNM classification of malignant tumor6th edWileyHoboken, NJGoogle Scholar
  17. 17.
    Makuuchi, M, Belghiti, JB, Belli, G, Fan, ST, Lau, JY, Ringe, B,  et al. 2003IHPBA concordant classification of primary liver cancer: working group reportJ Hepatobiliary Pancreat Surg102630PubMedGoogle Scholar
  18. 18.
    Lau, H, Man, K, Fan, ST, Yu, WC, Lo, CM, Wong, J 1997Evaluation of preoperative hepatic function in patients with hepatocellular carcinoma undergoing hepatectomyBr J Surg8412559PubMedCrossRefGoogle Scholar
  19. 19.
    The Cancer of the Liver Italian Program (CLIP) Investigators2000Prospective validation of the CLIP score: a new prognostic system for patients with cirrhosis and hepatocellular carcinomaHepatology318405CrossRefGoogle Scholar
  20. 20.
    Levy, I Sherman, M Liver Cancer Study Group of the University of Toronto2002Staging of hepatocellular carcinoma: assessment of the CLIP, Okuda, and Child-Pugh staging systems in a cohort of 257 patients in TorontoGut508815PubMedCrossRefGoogle Scholar
  21. 21.
    Ueno, S, Tanabe, G, Sako, K, Hiwaki, T, Hokotate, H, Fukukura, Y,  et al. 2001Discrimination value of the new western prognostic system (CLIP score) for hepatocellular carcinoma in 662 Japanese patients. Cancer of the Liver Italian ProgramHepatology3452934PubMedCrossRefGoogle Scholar
  22. 22.
    Marrero, JA, Su, GL, Wei, W, Emick, D, Conjeevaram, HS, Fontana, RJ,  et al. 2003Des-gamma carboxyprothrombin can differentiate hepatocellular carcinoma from nonmalignant chronic liver disease in American patientsHepatology37111421PubMedCrossRefGoogle Scholar
  23. 23.
    Yamashita, F, Tanaka, M, Satomura, S, Tanikawa, K 1996Prognostic significance of Lens culinaris agglutinin A-reactive alpha-fetoprotein in small hepatocellular carcinomasGastroenterology1119961001PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Tokyo 2006

Authors and Affiliations

  • Iwao Ikai
    • 1
  • Kenichi Takayasu
    • 2
  • Masao Omata
    • 3
  • Kiwamu Okita
    • 4
  • Yasuni Nakanuma
    • 5
  • Yutaka Matsuyama
    • 6
  • Masatoshi Makuuchi
    • 7
  • Masamichi Kojiro
    • 8
  • Takafumi Ichida
    • 9
  • Shigeki Arii
    • 10
  • Yoshio Yamaoka
    • 1
  • for the Liver Cancer Study Group of Japan
  1. 1.Department of Gastroenterological SurgeryKyoto University Graduate School of MedicineKyotoJapan
  2. 2.Department of Diagnostic RadiologyNational Cancer Center HospitalTokyoJapan
  3. 3.Department of GastroenterologyGraduate School of Medicine, University of TokyoTokyoJapan
  4. 4.Department of Gastroenterology and HepatologyYamaguchi University School of MedicineUbeJapan
  5. 5.Department of Human PathologyKanazawa University Graduate School of MedicineKanazawaJapan
  6. 6.Department of BiostatisticsSchool of Health Sciences and Nursing University of TokyoTokyoJapan
  7. 7.Hepato-Biliary-Pancreatic Surgery Division, Department of SurgeryGraduate School of Medicine, University of TokyoTokyoJapan
  8. 8.Department of PathologyKurume University School of MedicineKurumeJapan
  9. 9.Department of GastroenterologyJuntendo University School of MedicineTokyoJapan
  10. 10.Department of Hepato-Biliary-Pancreatic SurgeryTokyo Medical and Dental University Graduate School of MedicineTokyoJapan

Personalised recommendations