Resectability of hepatocellular carcinoma: Evaluation of 333 consecutive cases at a single hepatobiliary specialty center and systematic review of the literature

Hepato-Gastroenterology

Volumn 53, Issue 69, 2006, Pages 322-329

  Sotiropoulos, Georgios C ^a   Lang, Hauke ^a   Frilling, Andrea ^a   Molmenti, Ernesto P ^a   Paul, Andreas ^a   Nadalin, Silvio ^a   Radtke, Arnold ^a   Brokalaki, Eirini I ^a   Saner, Fuat ^a   Hilgard, Philip ^a   Gerken, Guido ^a   Broelsch, Christoph E ^a   Malagò, Massimo ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Chemoembolization; Combined modality therapy; Hepatectomy; Hepatocellular carcinoma

Indexed keywords

ADULT; AGED; CANCER SURGERY; CHEMOEMBOLIZATION; CONTROLLED STUDY; FEMALE; HOSPITAL ADMISSION; HUMAN; LIVER CELL CARCINOMA; LIVER RESECTION; MAJOR CLINICAL STUDY; MALE; MEDICAL LITERATURE; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW;

CARCINOMA, HEPATOCELLULAR; CHEMOEMBOLIZATION, THERAPEUTIC; COMBINED MODALITY THERAPY; FEMALE; GASTROENTEROLOGY; HEPATECTOMY; HOSPITALS, SPECIAL; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; PATIENT CARE TEAM; RETROSPECTIVE STUDIES; SURGERY DEPARTMENT, HOSPITAL;

EID: 33745448225     PISSN: 01726390     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Bosch FX, Ribes J, Cleries R, Diaz M: Epidemiology of hepatocellular carcinoma. Clin Liver Dis 2005; 9:191-211.
2. Pisani P, Parkin DM, Bray F, Ferlay J: Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer 1999; 83:18-29.
3. Okuda K, Ohtsuki T, Obata H, Tomimatsu M, Okazaki N, Hasegawa H, Nakajima Y, Ohnishi K: Natural history of hepatocellular carcinoma and prognosis in relation to treatment. Study of 850 patients. Cancer 1985; 56:918-928.
4. El-Assal ON, Yamanoi A, Soda Y, Yamaguchi M, Yu L, Nagasue N: Proposal of invasiveness score to predict recurrence and survival after curative hepatic resection for hepatocellular carcinoma. Surgery 1997; 122:571-577.
5. Llovet JM, Bru C, Bruix J: Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999; 19:329-338.
6. 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 Hepatocellulaire. J Hepatol 1999; 31:133-141.
7. CLIP investigators: Prospective validation of the CLIP score: a new prognostic system for patients with cirrhosis and hepatocellular carcinoma. The Cancer of the Liver Italian Program (CLIP) Investigators. Hepatology 2000; 31:840-845.
8. Iwatsuki S, Dvorchik I, Marsh JW, Madariaga JR, Carr B, Fung JJ, Starzl TE: Liver transplantation for hepatocellular carcinoma: A proposal of a prognostic scoring system. J Am Coll Surg 2000; 191:389-394.
9. Marsh JW, Dvorchik I, Bonham CA, Iwatsuki S: Is the pathologic TNM staging system for patients with hepatoma predictive of outcome? Cancer 2000; 88:538-543.
10. Chiappa A, Zbar AP, Podda M, Audisio RA, Bertani E, Biella F, Paties C, Staudacher C: Prognostic value of the modified TNM (Izumi) classification of hepatocellular carcinoma in 53 cirrhotic patients undergoing resection. Hepatogastroenterology 2001; 48:229-234.
11. Schoniger-Hekele M, Muller C, Kutilek M, Oesterreicher C, Ferenci P, Gangl A: Hepatocellular carcinoma in Central Europe: Prognostic features and survival. Gut 2001; 48:103-109.
12. Shimada M, Rikimaru T, Hamatsu T, Yamashita Y, Terashi T, Taguchi K, Tanaka S, Shirabe K, Sugimachi K: The role of macroscopic classification in nodular-type hepatocellular carcinoma. Am J Surg 2001; 182:177-182.
13. Tamura S, Kato T, Berho M, Misiakos EP, O'Brien C, Reddy KR, Nery JR, Burke GW, Schiff ER, Miller J, Tzakis AG: Impact of histological grade of hepatocellular carcinoma on the outcome of liver transplantation. Arch Surg 2001; 136:25-30.
14. Vauthey JN, Lauwers GY, Esnaola NF, Do KA, Belghiti J, Mirza N, Curley SA, Ellis LM, Regimbeau JM, Rashid A, Cleary KR, Nagorney DM: Simplified staging for hepatocellular carcinoma. J Clin Oncol 2002; 20:1527-1536.
15. Yao FY, Ferrell L, Bass NM, Bacchetti P, Asher NL, Roberts JP: Liver transplantation for hepatocellular carcinoma: Comparison of the proposed UCSF criteria with the Milan criteria and the Pittsburgh modified TNM criteria. Liver Transpl 2002; 8:765-774.
16. Leung TW, Tang AM, Zee B, Lau WY, Lai PB, Leung KL, Lau JT, Yu SC, Johnson PJ: 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; 94:1760-1769.
17. Lauwers GY, Terris B, Balis UJ, Batts KP, Regimbeau JM, Chang Y, Graeme-Cook F, Yamabe H, Ikai I, Cleary KR, Fujita S, Flejou JF, Zukerberg LR, Nagorney DM, Belghiti J, Yamaoka Y, Vauthey JN; International Cooperative Study Group on Hepatocellular Carcinoma: Prognostic histologic indicators of curatively resected hepatocellular carcinomas: A multi-institutional analysis of 425 patients with definition of a histologic prognostic index. Am J Surg Pathol 2002; 26:25-34.
18. Ueno S, Tanabe G, Nuruki K, Hamanoue M, Komorizono Y, Oketani M, Hokotate H, Inoue H, Baba Y, Imamura Y, Aikou T: Prognostic performance of the new classification of primary liver cancer of Japan (4th edition) for patients with hepatocellular carcinoma: a validation analysis. Hepatol Res 2002; 24:395-403.
19. Kawakita T, Shiraki K, Yamanaka Y, Yamaguchi Y, Saitou Y, Enokimura N, Yamamoto N, Okano H, Sugimoto K, Murata K, Yamakado K, Takeda K, Nakano T: A new prognostic scoring system involving des-gamma-carboxy prothrombin as a useful marker for predicting prognosis in patients with hepatocellular carcinoma. Int J Oncol 2003; 23:1115-1120.
20. Nanashima A, Morino S, Yamaguchi H, Tanaka K, Shibasaki S, Tsuji T, Hidaka S, Sawai T, Yasutake T, Nakagoe T: Modified CLIP using PIVKA-II for evaluating prognosis after hepatectomy for hepatocellular carcinoma. Eur J Surg Oncol 2003; 29:735-742.
21. Makuuchi M, Belghiti J, Belli G, Fan ST, Lau JW, Ringe B, Strasberg SM, Vauthey JN, Yamaoka Y, Yamasaki S; Working Group of the International Scientific Committee of the International Hepato-Pancreato-Biliary Association: IHPBA concordant classification of primary liver cancer: working group report. J Hepatobiliary Pancreat Surg 2003; 10:26-30.
22. 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 Japanese Integrated Staging Score (JIS score). J Gastroenterol 2003; 38:207-215.
23. Nanashima A, Sumida Y, Morino S, Yamaguchi H, Tanaka K, Shibasaki S, Ide N, Sawai T, Yasutake T, Nakagoe T, Nagayasu T: The Japanese integrated staging score using liver damage grade for hepatocellular carcinoma in patients after hepatectomy. Eur J Surg Oncol 2004; 30:765-770.
24. Omagari K, Honda S, Kadokawa Y, Isomoto H, Takeshima F, Hayashida K, Mizuta Y, Murata I, Kohno S: Preliminary analysis of a newly proposed prognostic scoring system (SLiDe score) for hepatocellular carcinoma. J Gastroenterol Hepatol 2004; 19:805-811.
25. Tateishi R, Yoshida H, Shiina S, Imamura H, Hasegawa K, Teratani T, Obi S, Sato S, Koike Y, Fujishima T, Makuuchi M, Omata M: Proposal of a new prognostic model for hepatocellular carcinoma: An analysis of 403 patients. Gut 2005; 54:419-425.
26. Sobin LH, Wittekind CH: TNM Classification of malignant tumours. Fifth Edition. New York: John Wiley & Sons, Inc., 1997.
27. Sobin LH, Wittekind CH: TNM Classification of malignant tumours. Sixth Edition. West Sussex: John Wiley & Sons Ltd., 2002.
28. Fattovich G, Stroffolini T, Zagni I, Donato F: Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004; 127(5 Suppl 1):35-50.
29. Di Bisceglie AM, Lyra AC, Schwartz M, Reddy RK, Martin P, Gores G, Lok AS, Hussain KB, Gish R, Van Thiel DH, Younossi Z, Tong M, Hassanein T, Balart L, Fleckenstein J, Flamm S, Blei A, Befeler AS; Liver Cancer Network: Hepatitis C-related hepatocellular carcinoma in the United States: Influence of ethnic status. Am J Gastroenterol 2003; 98:2060-2063.
30. Kurokohchi K, Watanabe S, Masaki T, Hosomi N, Miyauchi Y, Himoto T, Kimura Y, Nakai S, Deguchi A, Yoneyama H, Yoshida S, Kuriyama S: Comparison between combination therapy of percutaneous ethanol injection and radiofrequency ablation and radiofrequency ablation alone for patients with hepatocellular carcinoma. World J Gastroenterol 2005; 11:1426-1432.
31. Tang ZY, Zhou XD, Ma ZC, Wu ZQ, Fan J, Qin LX, Yu Y: Downstaging followed by resection plays a role in improving prognosis of unresectable hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 2004; 3:495-498.
32. Zeng ZC, Tang ZY, Fan J, Zhou J, Qin LX, Ye SL, Sun HC, Wang BL, Yu Y, Wang JH, Guo W: A comparison of chemoembolization combination with and without radiotherapy for unresectable hepatocellular carcinoma. Cancer J 2004; 10:307-316.
33. Lau WY, Ho SK, Yu SC, Lai EC, Liew CT, Leung TW: Salvage surgery following downstaging of unresectable hepatocellular carcinoma. Ann Surg 2004; 240:299-305.
34. Jang JW, Park YM, Bae SH, Choi JY, Yoon SK, Chang UI, Nam SW, Kim BS: Therapeutic efficacy of multimodal combination therapy using transcatheter arterial infusion of epirubicin and cisplatin, systemic infusion of 5-fluorouracil, and additional percutaneous ethanol injection for unresectable hepatocellular carcinoma. Cancer Chemother Pharmacol 2004; 54:415-420.
35. Yamakado K, Nakatsuka A, Akeboshi M, Shiraki K, Nakano T, Takeda K: Combination therapy with radiofrequency ablation and transcatheter chemoembolization for the treatment of hepatocellular carcinoma: Short-term recurrences and survival. Oncol Rep 2004; 11:105-109.
36. Sotiropoulos GC, Malago M, Molmenti E, Paul A, Nadalin S, Brokalaki EI, Verhagen R, Dirsch O, Gerken G, Lang H, Broelsch CE: Efficacy of transarterial chemoembolization prior to liver transplantation for hepatocellular carcinoma as found in pathology. Hepatogastroenterology 2005; 52:329-332.
37. Mazzaferro V, Battiston C, Perrone S, Pulvirenti A, Regalia E, Romito R, Sarli D, Schiavo M, Garbagnati F, Marchiano A, Spreafico C, Camerini T, Mariani L, Miceli R, Andreola S: Radiofrequency ablation of small hepatocellular carcinoma in cirrhotic patients awaiting liver transplantation: a prospective study. Ann Surg 2004; 240:900-909.
38. Adam R, Azoulay D, Castaing D, Eshkenazy R, Pascal G, Hashizume K, Samuel D, Bismuth H: Liver resection as a bridge to transplantation for hepatocellular carcinoma on cirrhosis: a reasonable strategy? Ann Surg 2003; 238:508-518.
39. Belghiti J, Cortes A, Abdalla EK, Regimbeau JM, Prakash K, Durand F, Sommacale D, Dondero F, Lesurtel M, Sauvanet A, Farges O, Kianmanesh R: Resection prior to liver transplantation for hepatocellular carcinoma. Ann Surg 2003; 238:885-892.
40. Bigourdan JM, Jaeck D, Meyer N, Meyer C, Oussoultzoglou E, Bachellier P, Weber JC, Audet M, Doffoel M, Wolf P: Small hepatocellular carcinoma in Child A cirrhotic patients: hepatic resection versus transplantation. Liver Transpl 2003; 9:513-520.
41. Figueras J, Jaurrieta E, Valls C, Ramos E, Serrano T, Rafecas A, Fabregat J, Torras J: Resection or transplantation for hepatocellular carcinoma in cirrhotic patients: outcomes based on indicated treatment strategy. J Am Coll Surg 2000; 190:580-587.
42. Bismuth H, Chiche L, Adam R, Castaing D, Diamond T, Dennison A: Liver resection versus transplantation for hepatocellular carcinoma in cirrhotic patients. Ann Surg 1993; 218:145-151.
43. Marsh JW, Dvorchik I: Liver organ allocation for hepatocellular carcinoma: are we sure? Liver Transpl 2003; 9:693-696.
44. Wudel LJ Jr, Chapman WC: Indications and limitations of liver transplantation for hepatocellular carcinoma. Surg Oncol Clin N Am 2003; 12:77-90.
45. Lai ECS, Fan ST, Lo, CM, Chu KM, Liu CL, Wong J: Hepatic resection for hepatocellular carcinoma: An audit of 343 patients. Ann Surg 1995; 221:291-298.
46. Fujio N, Sakai K, Kinoshita H, Hirohashi K, Kubo S, Iwasa R, Lee KC: Results of treatment of patients with hepatocellular carcinoma with severe cirrhosis of the liver. World J Surg 1989; 13:211-217.
47. Bruix J, Cirera I, Calvet X, Fuster J, Bru C, Ayuso C, Vilana R, Boix L, Visa J, Rodes J: Surgical resection and survival in Western patients with hepatocellular carcinoma. J Hepatol 1992; 15:350-355.
48. Wakabayashi H, Ushiyama T, Ishimura K, Izuishi K, Karasawa Y, Masaki T, Watanabe S, Kuriyama S, Maeta H: Significance of reduction surgery in multidisciplinary treatment of advanced hepatocellular carcinoma with multiple intrahepatic lesions. J Surg Oncol 2003; 82:98-103.
49. Chang CH, Chau GY, Lui WY, Tsay SH, King KL, Wu CW: Long-term results of hepatic resection for hepatocellular carcinoma originating from the noncirrhotic liver. Arch Surg 2004; 139:320-325.
50. Lang BH, Poon RT, Fan ST, Wong J: Perioperative and long-term outcome of major hepatic resection for small solitary hepatocellular carcinoma in patients with cirrhosis. Arch Surg 2003; 138:1207-1213.
51. Nzeako UC, Goodman ZD, Ishak KG: Hepatocellular carcinoma in cirrhotic and noncirrhotic livers. A clinicohistopathologic study of 804 North American patients. Am J Clin Pathol 1996; 105:65-75.
52. Shiu W, Dewar G, Leung N, Leung WT, Chan M, Tao M, Lui C, Chan CL, Lau WY, Metreweli C, et al: Hepa tocellular carcinoma in Hong Kong: clinical study on 340 cases. Oncology 1990; 47:241-245.
53. Poon RT, Fan ST, Lo CM, Ng IO, Liu CL, Lam CM, Wong J: Improving survival results after resection of hepatocellular carcinoma: a prospective study of 377 patients over 10 years. Ann Surg 2001; 234:63-70.
54. Hanazaki K, Kajikawa S, Shimozawa N, Mihara M, Shimada K, Hiraguri M, Koide N, Adachi W, Amano J: Survival and recurrence after hepatic resection of 386 consecutive patients with hepatocellular carcinoma. J Am Coll Surg 2000; 191:381-388.
55. Michel J, Suc B, Montpeyroux F, Hachemanne S, Blanc P, Domergue J, Mouiel J, Gouillat C, Ducerf C, Saric J, Le Treut VP, Fourtanier G, Escat J: Liver resection or transplantation for hepatocellular carcinoma? Retrospective analysis of 215 patients with cirrhosis. J Hepatol 1997; 26:1274-1280.
56. Ezaki T, Yamamoto K, Yamaguchi H, Sasaki Y, Ishida T, Mori M, Aimitsu S: Hepatic resection for hepatocellular carcinoma existing with liver cirrhosis. Hepatogastroenterology 2002; 49:1363-1368.
57. Roayaie S, Frischer JS, Emre SH, Fishbein TM, Sheiner PA, Sung M, Miller CM, Schwartz ME: Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters. Ann Surg 2002; 235:533-539.
58. Patt YZ, Claghorn L, Charnsangavej C, Soski M, Cleary K, Mavligit GM: Hepatocellular carcinoma. A retrospective analysis of treatments to manage disease confined to the liver. Cancer 1988; 61:1884-1888.
59. Kawarada Y, Imai T, Iwata M, Yokoi H, Noguchi T, Mizumoto R: Significance of multidisciplinary therapy for hepatocellular carcinoma. Cancer Chemother Pharmacol 1992; 31(Suppl I):S13-19.
60. Onodera H, Ukai K, Nakano N, Takeda T, Suzuki H, Okata T, Motojima T, Kuwashima I, Ujiie S, Shoji T: Outcomes of 116 patients with hepatocellular carcinoma. Cancer Chemother Pharmacol 1994; 33(Suppl):103-108.
61. Schwartz ME, Sung M, Mor E, Fisher A, Popescu I, Fiel I, Sheiner P, Emre S, Guy S, Miller CM: A multidisciplinary approach to hepatocellular carcinoma in patients with cirrhosis. J Am Coll Surg 1995; 180:596-603.
62. Marcos-Alvarez A, Jenkins RL, Washburn WK, Lewis WD, Stuart KE, Gordon FD, Kane RA, Clouse ME: Multimodality treatment of hepatocellular carcinoma in a hepatobiliary specialty center. Arch Surg 1996; 131:292-298.
63. Stuart KE, Anand AJ, Jenkins RL: Hepatocellular carcinoma in the United States. Prognostic features, treatment outcome, and survival. Cancer 1996; 77:2217-2222.
64. Sheen PC, Lee KT, Chen HY, Chen JS, Ker CG: Conservative hepatic resection for hepatocellular carcinoma of cirrhotic patients. Int Surg 1996; 81:280-283.
65. Colella G, Bottelli R, De Carlis L, Sansalone CV, Rondinara GF, Alberti A, Belli LS, Gelosa F, Iamoni GM, Rampoldi A, De Gasperi A, Corti A, Mazza E, Aseni P, Meroni A, Slim AO, Finzi M, Di Benedetto F, Manochehri F, Follini ML, Ideo G, Forti D: Hepatocellular carcinoma: Comparison between liver transplantation, resective surgery, ethanol injection, and chemoembolization. Transpl Int 1998; 11(Suppl 1):S193-196.
66. Rose AT, Rose DM, Pinson CW, Wright JK, Blair T, Blanke C, Delbeke D, Debelak JP, Chapman WC: Hepatocellular carcinoma outcomes based on indicated treatment strategy. Am Surg 1998; 64:1128-1134.
67. Sangro B, Herraiz M, Martinez-Gonzalez MA, Bilbao I, Herrero I, Beloqui O, Betes M, de-la-Pena A, Cienfuegos JA, Quiroga J, Prieto J: Prognosis of hepatocellular carcinoma in relation to treatment: a multivariate analysis of 178 patients from a single European institution. Surgery 1998; 124:575-583.
68. Sasaki Y, Imaoka S, Nakano H, Ishikawa O, Ohigashi H, Yasuda T, Nakamori S, Kameyama M, Hiratsuku M, Kabuto T, Furukawa H, Kasugai H, Inoue A, Fujita M, Inoue E: Indications for hepatectomy for hepatocellular carcinoma - what stage of the disease is the best indication for surgery? J Hepatobiliary Pancreat Surg 1998; 5:14-17.
69. Huang YH, Wu JC, Chau GY, Lui WY, King KL, Chiang JH, Yen SH, Sheng WY, Hou MC, Lu CL, Chang FY, Lee SD: Supportive treatment, resection and transcatheter arterial chemoembolization in resectable hepatocellular carcinoma: an analysis of survival in 419 patients. Eur J Gastroenterol Hepatol 1999; 11:315-321.
70. Takano S, Watanabe Y, Ohishi H, Kono S, Nakamura M, Kubota N, Iwai S: Multimodality treatment for patients with hepatocellular carcinoma: a single institution retrospective series. Eur J Surg Oncol 2000; 26:67-72.
71. Christians KK, Pitt HA, Rilling WS, Franco J, Quiroz FA, Adams MB, Wallace JR, Quebbeman EJ: Hepatocellular carcinoma: multimodality management. Surgery 2001; 130:554-559.
72. Medina-Franco H, Sellers MT, Eckhoff DE, Bynon JS, Urist MM, Heslin MJ: Multimodality treatment for patients with hepatocellular carcinoma: analysis of prognostic factors in a single Western institution series. J Gastrointest Surg 2001; 5:638-645.
73. Ueno S, Tanabe G, Nuruki K, Oketani M, Komorizono Y, Hokotate H, Fukukura Y, Baba Y, Imamura Y, Aikou T: Prognosis of hepatocellular carcinoma associated with Child class B and C cirrhosis in relation to treatment: a multivariate analysis of 411 patients at a single center. J Hepatobiliary Pancreat Surg 2002; 9:469-77.
74. Sotiropoulos GC, Malago M, Molmenti E, Paul A, Nadalin S, Brokalaki E, Kuhl H, Dirsch O, Lang H, Broelsch CE: Liver transplantation for hepatocellular carcinoma in cirrhosis: is clinical tumor classification before transplantation realistic? Transplantation 2005; 79:483-487.
75. Krinsky GA, Lee VS, Theise ND, Weinreb JC, Morgan GR, Diflo T, John D, Teperman LW, Goldenberg AS: Transplantation for hepatocellular carcinoma and cirrhosis: Sensitivity of magnetic resonance imaging. Liver Transpl 2002; 8:1156-1164.