Overview of Staging Systems for Hepatocellular Carcinoma and Implications for Interventional Radiology

Jan Hansmann; Charles E. Ray Jr.

doi:10.1055/s-0037-1602757

Seminars in Interventional Radiology, Table of Contents

Semin intervent Radiol 2017; 34(02): 213-219
DOI: 10.1055/s-0037-1602757

Clinical Corner

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Overview of Staging Systems for Hepatocellular Carcinoma and Implications for Interventional Radiology

Jan Hansmann

¹Department of Radiology, University of Illinois at Chicago College of Medicine, Chicago, Illinois

,

Charles E. Ray Jr.

¹Department of Radiology, University of Illinois at Chicago College of Medicine, Chicago, Illinois

› Author Affiliations

Abstract

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References

References
1 Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61 (02) 69-90
2 El-Serag HB, Kanwal F. Epidemiology of hepatocellular carcinoma in the United States: where are we? Where do we go?. Hepatology 2014; 60 (05) 1767-1775
3 Ryerson AB, Eheman CR, Altekruse SF. , et al. Annual report to the nation on the status of cancer, 1975-2012, featuring the increasing incidence of liver cancer. Cancer 2016; 122 (09) 1312-1337
4 Llovet JM, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999; 19 (03) 329-338
5 Edge SBBD, Compton CC, Fritz AG, Greene FL, Trotti A. , eds. AJCC Cancer Staging Manual, 7th ed. New York, NY: Springer; 2010
6 A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients: the Cancer of the Liver Italian Program (CLIP) investigators. Hepatology 1998; 28 (03) 751-755
7 Johnson PJ, Berhane S, Kagebayashi C. , et al. Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J Clin Oncol 2015; 33 (06) 550-558
8 Roayaie S, Jibara G, Berhane S. , et al. PALBI-An Objective Score Based on Platelets, Albumin & Bilirubin Stratifies HCC Patients Undergoing Resection & Ablation Better than Child's Classification. AASLD LiverLearning; 2015: 110095
9 Ishak K, Baptista A, Bianchi L. , et al. Histological grading and staging of chronic hepatitis. J Hepatol 1995; 22 (06) 696-699
10 Vauthey JN, Ribero D, Abdalla EK. , et al. Outcomes of liver transplantation in 490 patients with hepatocellular carcinoma: validation of a uniform staging after surgical treatment. J Am Coll Surg 2007; 204 (05) 1016-1027 , discussion 1027–1028
11 Okuda K, Ohtsuki T, Obata H. , et al. Natural history of hepatocellular carcinoma and prognosis in relation to treatment. Study of 850 patients. Cancer 1985; 56 (04) 918-928
12 Llovet JM, Bruix J. Prospective validation of the Cancer of the Liver Italian Program (CLIP) score: a new prognostic system for patients with cirrhosis and hepatocellular carcinoma. Hepatology 2000; 32 (03) 679-680
13 Levy I, Sherman M. ; Liver Cancer Study Group of the University of Toronto. Staging of hepatocellular carcinoma: assessment of the CLIP, Okuda, and Child-Pugh staging systems in a cohort of 257 patients in Toronto. Gut 2002; 50 (06) 881-885
14 Ueno S, Tanabe G, Sako K. , et al. Discrimination value of the new western prognostic system (CLIP score) for hepatocellular carcinoma in 662 Japanese patients. Cancer of the Liver Italian Program. Hepatology 2001; 34 (03) 529-534
15 Huo TI, Huang YH, Lin HC. , et al. Proposal of a modified Cancer of the Liver Italian Program staging system based on the model for end-stage liver disease for patients with hepatocellular carcinoma undergoing loco-regional therapy. Am J Gastroenterol 2006; 101 (05) 975-982
16 Kaseb AO, Hassan MM, Lin E. , et al. V-CLIP: integrating plasma vascular endothelial growth factor into a new scoring system to stratify patients with advanced hepatocellular carcinoma for clinical trials. Cancer 2011; 117 (11) 2478-2488
17 Kaseb AO, Abbruzzese JL, Vauthey JN. , et al. I-CLIP: improved stratification of advanced hepatocellular carcinoma patients by integrating plasma IGF-1 into CLIP score. Oncology 2011; 80 (5-6): 373-381
18 Chevret S, Trinchet JC, Mathieu D, Rached AA, Beaugrand M, Chastang C. A new prognostic classification for predicting survival in patients with hepatocellular carcinoma. Groupe d'Etude et de Traitement du Carcinome Hépatocellulaire. J Hepatol 1999; 31 (01) 133-141
19 El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007; 132 (07) 2557-2576
20 Choo SP, Tan WL, Goh BK, Tai WM, Zhu AX. Comparison of hepatocellular carcinoma in Eastern versus Western populations. Cancer 2016
21 Omata M, Lesmana LA, Tateishi R. , et al. Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma. Hepatol Int 2010; 4 (02) 439-474
22 Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, ter Borg PC. A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology 2000; 31 (04) 864-871
23 Freeman Jr RB, Wiesner RH, Harper A. , et al; UNOS/OPTN Liver Disease Severity Score, UNOS/OPTN Liver and Intestine, and UNOS/OPTN Pediatric Transplantation Committees. The new liver allocation system: moving toward evidence-based transplantation policy. Liver Transpl 2002; 8 (09) 851-858
24 Leise MD, Kim WR, Kremers WK, Larson JJ, Benson JT, Therneau TM. A revised model for end-stage liver disease optimizes prediction of mortality among patients awaiting liver transplantation. Gastroenterology 2011; 140 (07) 1952-1960
25 Leung TW, Tang AM, Zee B. , et al. 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 2002; 94 (06) 1760-1769
26 Kudo M, Chung H, Osaki Y. 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 2003; 38 (03) 207-215
27 Huo TI, Lin HC, Huang YH. , et al. The model for end-stage liver disease-based Japan Integrated Scoring system may have a better predictive ability for patients with hepatocellular carcinoma undergoing locoregional therapy. Cancer 2006; 107 (01) 141-148
28 Tateishi R, Yoshida H, Shiina S. , et al. Proposal of a new prognostic model for hepatocellular carcinoma: an analysis of 403 patients. Gut 2005; 54 (03) 419-425
29 Yau T, Tang VY, Yao TJ, Fan ST, Lo CM, Poon RT. Development of Hong Kong Liver Cancer staging system with treatment stratification for patients with hepatocellular carcinoma. Gastroenterology 2014; 146 (07) 1691-700.e3
30 Adhoute X, Penaranda G, Bronowicki JP, Raoul JL. Usefulness of the HKLC vs. the BCLC staging system in a European HCC cohort. J Hepatol 2015; 62 (02) 492-493
31 Child CG, Turcotte JG. Surgery and portal hypertension. Major Probl Clin Surg 1964; 1: 1-85
32 Okuda K, Musha H, Nakajima Y. , et al. Clinicopathologic features of encapsulated hepatocellular carcinoma: a study of 26 cases. Cancer 1977; 40 (03) 1240-1245
33 Villa E, Colantoni A, Cammà C. , et al. Estrogen receptor classification for hepatocellular carcinoma: comparison with clinical staging systems. J Clin Oncol 2003; 21 (03) 441-446
34 Cescon M, Cucchetti A, Grazi GL. , et al. Role of hepatitis B virus infection in the prognosis after hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a Western dual-center experience. Arch Surg 2009; 144 (10) 906-913
35 Sasaki Y, Yamada T, Tanaka H. , et al. Risk of recurrence in a long-term follow-up after surgery in 417 patients with hepatitis B- or hepatitis C-related hepatocellular carcinoma. Ann Surg 2006; 244 (05) 771-780
36 Roayaie S, Haim MB, Emre S. , et al. Comparison of surgical outcomes for hepatocellular carcinoma in patients with hepatitis B versus hepatitis C: a western experience. Ann Surg Oncol 2000; 7 (10) 764-770
37 Kim BK, Park JY, Kim DY. , et al. Persistent hepatitis B viral replication affects recurrence of hepatocellular carcinoma after curative resection. Liver Int 2008; 28 (03) 393-401
38 Sun H, Teng M, Liu J. , et al. FOXM1 expression predicts the prognosis in hepatocellular carcinoma patients after orthotopic liver transplantation combined with the Milan criteria. Cancer Lett 2011; 306 (02) 214-222
39 Schmitz KJ, Sotiropoulos GC, Baba HA. , et al. AKR1B10 expression is associated with less aggressive hepatocellular carcinoma: a clinicopathological study of 168 cases. Liver Int 2011; 31 (06) 810-816
40 Sherman M. Staging for hepatocellular carcinoma: complex and confusing. Gastroenterology 2014; 146 (07) 1599-1602
41 Sherman M. Staging for hepatocellular carcinoma: an embarrassment of riches. J Hepatol 2016; 64 (03) 535-536
42 Nanashima A, Sumida Y, Abo T. , et al. Modified Japan Integrated Staging is currently the best available staging system for hepatocellular carcinoma patients who have undergone hepatectomy. J Gastroenterol 2006; 41 (03) 250-256
43 Huang YH, Chen CH, Chang TT. , et al. Evaluation of predictive value of CLIP, Okuda, TNM and JIS staging systems for hepatocellular carcinoma patients undergoing surgery. J Gastroenterol Hepatol 2005; 20 (05) 765-771
44 Georgiades CS, Liapi E, Frangakis C. , et al. Prognostic accuracy of 12 liver staging systems in patients with unresectable hepatocellular carcinoma treated with transarterial chemoembolization. J Vasc Interv Radiol 2006; 17 (10) 1619-1624
45 Cho YK, Chung JW, Kim JK. , et al. Comparison of 7 staging systems for patients with hepatocellular carcinoma undergoing transarterial chemoembolization. Cancer 2008; 112 (02) 352-361
46 Liu PH, Hsu CY, Hsia CY. , et al. Prognosis of hepatocellular carcinoma: Assessment of eleven staging systems. J Hepatol 2016; 64 (03) 601-608
47 Helton WS, Strasberg SM. AHPBA/AJCC consensus conference on staging of hepatocellular carcinoma: rationale and overview of the conference. HPB (Oxford) 2003; 5 (04) 238-242
48 Vauthey JN, Dixon E, Abdalla EK. , et al; American Hepato-Pancreato-Biliary Association; Society of Surgical Oncology; Society for Surgery of the Alimentary Tract. Pretreatment assessment of hepatocellular carcinoma: expert consensus statement. HPB (Oxford) 2010; 12 (05) 289-299
49 Gaba RC, Lewandowski RJ, Hickey R. , et al; Society of Interventional Radiology Technology Assessment Committee. Transcatheter therapy for hepatic malignancy: standardization of terminology and reporting criteria. J Vasc Interv Radiol 2016; 27 (04) 457-473
50 Hickey R, Mouli S, Kulik L. , et al. Independent analysis of albumin-bilirubin grade in a 765-patient cohort treated with transarterial locoregional therapy for hepatocellular carcinoma. J Vasc Interv Radiol 2016; 27 (06) 795-802
51 Pinato DJ, Sharma R, Allara E. , et al. The ALBI grade provides objective hepatic reserve estimation across each BCLC stage of hepatocellular carcinoma. J Hepatol 2017; 66 (02) 338-346
52 Liu PH, Hsu CY, Hsia CY. , et al. ALBI and PALBI grade predict survival for HCC across treatment modalities and BCLC stages in the MELD Era. J Gastroenterol Hepatol 2017; 32 (04) 879-886
53 Hiraoka A, Kumada T, Michitaka K. , et al. Usefulness of albumin-bilirubin grade for evaluation of prognosis of 2584 Japanese patients with hepatocellular carcinoma. J Gastroenterol Hepatol 2016; 31 (05) 1031-1036
54 Chan AW, Kumada T, Toyoda H. , et al. Integration of albumin-bilirubin (ALBI) score into Barcelona Clinic Liver Cancer (BCLC) system for hepatocellular carcinoma. J Gastroenterol Hepatol 2016; 31 (07) 1300-1306