Staging of Hepatocellular Carcinoma

  • Hari Nathan
  • Timothy M. Pawlik


Staging systems aim to stratify patients into groups with similar prognoses. As such, these staging systems may serve to guide choice of therapy, aid in patient counseling, allow comparisons of the end results of therapy, and facilitate patient selection and randomization for research protocols.


HCC staging Okuda staging system Cancer of the Liver Italian Program (CLIP) score Barcelona Clinic Liver Cancer (BCLC) staging system Liver Cancer Study Group of Japan (LCSGJ) staging system Japanese Integrated Staging (JIS) score Chinese University Prognostic Index (CUPI) American Joint Committee on Cancer/International Union Against Cancer (AJCC/UICC) staging system 


  1. 1.
    Okuda K, Ohtsuki T, Obata H et al (1985) Natural history of hepatocellular carcinoma and prognosis in relation to treatment. Study of 850 patients. Cancer 56:918–928CrossRefPubMedGoogle Scholar
  2. 2.
    The Cancer of the Liver Italian Program (CLIP) investigators (1998) A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients. Hepatology 28:751–755CrossRefGoogle Scholar
  3. 3.
    Llovet JM, Bru C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19:329–338CrossRefPubMedGoogle Scholar
  4. 4.
    Makuuchi M, Belghiti J, Belli G et al (2003) IHPBA concordant classification of primary liver cancer: working group report. J Hepatobiliary Pancreat Surg 10:26–30PubMedGoogle Scholar
  5. 5.
    Kudo M, Chung H, Osaki Y (2003) Prognostic 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 Gastroenterol 38:207–215CrossRefPubMedGoogle Scholar
  6. 6.
    Leung TW, Tang AM, Zee B et al (2002) Construction 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 patients. Cancer 94:1760–1769CrossRefPubMedGoogle Scholar
  7. 7.
    Greene FL, Page DL, Fleming ID et al (2002) AJCC Cancer Staging Manual, 6th ed. New York, Springer-VerlagGoogle Scholar
  8. 8.
    Edge SB, Byrd DR, Compton CC et al (2010) AJCC Cancer Staging Manual, 7th ed. New York, SpringerGoogle Scholar
  9. 9.
    The Cancer of the Liver Italian Program (CLIP) Investigators. (2000) Prospective validation of the CLIP score: a new prognostic system for patients with cirrhosis and hepatocellular carcinoma. Hepatology 31:840–845CrossRefGoogle Scholar
  10. 10.
    Ueno S, Tanabe G, Sako K et al (2001) Discrimination value of the new western prognostic system (CLIP score) for hepatocellular carcinoma in 662 Japanese patients. Cancer of the Liver Italian Program. Hepatology 34:529–534CrossRefPubMedGoogle Scholar
  11. 11.
    Levy I, Sherman M (2002) Staging of hepatocellular carcinoma: assessment of the CLIP, Okuda, and Child-Pugh staging systems in a cohort of 257 patients in Toronto. Gut 50: 881–885CrossRefPubMedGoogle Scholar
  12. 12.
    Bruix J, Llovet JM (2002) Prognostic prediction and treatment strategy in hepatocellular carcinoma. Hepatology 35:519–524CrossRefPubMedGoogle Scholar
  13. 13.
    Sorensen JB, Klee M, Palshof T et al (1993) Performance status assessment in cancer patients. An inter-observer variability study. Br J Cancer 67:773–775PubMedGoogle Scholar
  14. 14.
    Marrero JA, Fontana RJ, Barrat A et al (2005) Prognosis of hepatocellular carcinoma: comparison of 7 staging systems in an American cohort. Hepatology 41:707–716CrossRefPubMedGoogle Scholar
  15. 15.
    Cillo U, Vitale A, Grigoletto F et al (2006) Prospective validation of the Barcelona Clinic Liver Cancer staging system. J Hepatol 44:723–731CrossRefPubMedGoogle Scholar
  16. 16.
    Guglielmi A, Ruzzenente A, Pachera S et al (2008) Comparison of seven staging systems in cirrhotic patients with hepatocellular carcinoma in a cohort of patients who underwent radiofrequency ablation with complete response. Am J Gastroenterol 103:597–604CrossRefPubMedGoogle Scholar
  17. 17.
    Ng KK, Vauthey JN, Pawlik TM et al (2005) Is hepatic resection for large or multinodular hepatocellular carcinoma justified? Results from a multi-institutional database. Ann Surg Oncol 12:364–373CrossRefPubMedGoogle Scholar
  18. 18.
    Pawlik TM, Poon RT, Abdalla EK et al (2005) Critical appraisal of the clinical and pathologic predictors of survival after resection of large hepatocellular carcinoma. Arch Surg 140: 450–458CrossRefPubMedGoogle Scholar
  19. 19.
    Mazzaferro V, Regalia E, Doci R et al (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699CrossRefPubMedGoogle Scholar
  20. 20.
    Vauthey JN, Lauwers GY, Esnaola NF et al (2002) Simplified staging for hepatocellular carcinoma. J Clin Oncol 20:1527–1536CrossRefPubMedGoogle Scholar
  21. 21.
    Kudo M, Chung H, Haji S et al (2004) Validation of a new prognostic staging system for hepatocellular carcinoma: the JIS score compared with the CLIP score. Hepatology 40: 1396–1405CrossRefPubMedGoogle Scholar
  22. 22.
    Georgiades CS, Liapi E, Frangakis C et al (2006) Prognostic accuracy of 12 liver staging systems in patients with unresectable hepatocellular carcinoma treated with transarterial chemoembolization. J Vasc Interv Radiol 17:1619–1624CrossRefPubMedGoogle Scholar
  23. 23.
    Chen TW, Chu CM, Yu JC et al (2007) Comparison of clinical staging systems in predicting survival of hepatocellular carcinoma patients receiving major or minor hepatectomy. Eur J Surg Oncol 33:480–487CrossRefPubMedGoogle Scholar
  24. 24.
    Kondo K, Chijiiwa K, Nagano M et al (2007) Comparison of seven prognostic staging systems in patients who undergo hepatectomy for hepatocellular carcinoma. Hepatogastroenterology 54:1534–1538PubMedGoogle Scholar
  25. 25.
    Lu W, Dong J, Huang Z et al (2008) Comparison of four current staging systems for Chinese patients with hepatocellular carcinoma undergoing curative resection: Okuda, CLIP, TNM and CUPI. J Gastroenterol Hepatol 23, 1874–1878CrossRefPubMedGoogle Scholar
  26. 26.
    Ishak K, Baptista A, Bianchi L et al (1995) Histological grading and staging of chronic hepatitis. J Hepatol 22:696–699CrossRefPubMedGoogle Scholar
  27. 27.
    Poon RT, Fan ST (2003) Evaluation of the new AJCC/UICC staging system for hepatocellular carcinoma after hepatic resection in Chinese patients. Surg Oncol Clin N Am 12:35–50, viiiCrossRefPubMedGoogle Scholar
  28. 28.
    Vauthey JN, Ribero D, Abdalla EK et al (2007) Outcomes of liver transplantation in 490 patients with hepatocellular carcinoma: validation of a uniform staging after surgical treatment. J Am Coll Surg 204:1016–1028CrossRefPubMedGoogle Scholar
  29. 29.
    Pawlik TM, Abdalla EK, Thomas M et al (2005) Staging of hepatocellular carcinoma. Hepatology 42:738–739; author reply 9–40CrossRefPubMedGoogle Scholar
  30. 30.
    Tateishi R, Yoshida H, Shiina S et al (2005) Proposal of a new prognostic model for hepatocellular carcinoma: an analysis of 403 patients. Gut 54:419–425CrossRefPubMedGoogle Scholar
  31. 31.
    Toyoda H, Kumada T, Kiriyama S et al (2005) Comparison of the usefulness of three staging systems for hepatocellular carcinoma (CLIP, BCLC, and JIS) in Japan. Am J Gastroenterol 100:1764–1771CrossRefPubMedGoogle Scholar
  32. 32.
    Nanashima A, Omagari K, Tobinaga S et al (2005) Comparative study of survival of patients with hepatocellular carcinoma predicted by different staging systems using multivariate analysis. Eur J Surg Oncol 31:882–890CrossRefPubMedGoogle Scholar
  33. 33.
    Testa R, Testa E, Giannini E et al (2003) Trans-catheter arterial chemoembolisation for hepatocellular carcinoma in patients with viral cirrhosis: role of combined staging systems, Cancer Liver Italian Program (CLIP) and Model for End-stage Liver Disease (MELD), in predicting outcome after treatment. Aliment Pharmacol Ther 17:1563–1569CrossRefPubMedGoogle Scholar
  34. 34.
    Cho YK, Chung JW, Kim JK et al (2008) Comparison of 7 staging systems for patients with hepatocellular carcinoma undergoing transarterial chemoembolization. Cancer 112:352–361CrossRefPubMedGoogle Scholar
  35. 35.
    Grieco A, Pompili M, Caminiti G et al (2005) Prognostic factors for survival in patients with early-intermediate hepatocellular carcinoma undergoing non-surgical therapy: comparison of Okuda, CLIP, and BCLC staging systems in a single Italian centre. Gut 54:411–418CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Hari Nathan
    • 1
  • Timothy M. Pawlik
    • 2
  1. 1.Department of SurgeryThe Johns Hopkins University School of MedicineMarylandUSA
  2. 2.Division of Surgical Oncology, Department of SurgeryThe Johns Hopkins School of MedicineMDUSA

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