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Published in: Journal of Gastrointestinal Surgery 1/2013

01-01-2013 | 2012 SSAT Plenary Presentation

Improved Long-Term Survival after Major Resection for Hepatocellular Carcinoma: A Multicenter Analysis Based on a New Definition of Major Hepatectomy

Authors: Andreas Andreou, Jean-Nicolas Vauthey, Daniel Cherqui, Giuseppe Zimmitti, Dario Ribero, Mark J. Truty, Steven H. Wei, Steven A. Curley, Alexis Laurent, Ronnie T. Poon, Jacques Belghiti, David M. Nagorney, Thomas A. Aloia, From the International Cooperative Study Group on Hepatocellular Carcinoma

Published in: Journal of Gastrointestinal Surgery | Issue 1/2013

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Abstract

Background

Advances in the surgical management of hepatocellular carcinoma (HCC) have expanded the indications for curative hepatectomy, including more extensive liver resections. The purpose of this study was to examine long-term survival trends for patients treated with major hepatectomy for HCC.

Patients and Methods

Clinicopathologic data for 1,115 patients with HCC who underwent hepatectomy between 1981 and 2008 at five hepatobiliary centers in France, China, and the USA were assessed. In addition to other performance metrics, outcomes were evaluated using resection of ≥4 liver segments as a novel definition of major hepatectomy.

Results

Major hepatectomy was performed in 539 patients. In the major hepatectomy group, median tumor size was 10 cm (range: 1–27 cm) and 22 % of the patients had bilateral lesions. The TNM Stage distribution included 29 % Stage I, 31 % Stage II, 38 % Stage III, and 2 % Stage IV. The postoperative histologic examination indicated that chronic liver disease was present in 35 % of the patients and tumor microvascular invasion was identified in 60 % of the patients. The 90-day postoperative mortality rate was 4 %. After a median follow-up time of 63 months, the 5-year overall survival rate was 40 %. Patients treated with right hepatectomy (n = 332) and those requiring extended hepatectomy (n = 207) had similar 90-day postoperative mortality rates (4 % and 4 %, respectively, p = 0.976) and 5-year overall survival rates (42 % and 36 %, respectively, p = 0.523). Postoperative mortality and overall survival rates after major hepatectomy were similar among the participating countries (p > 0.1) and improved over time with 5-year survival rates of 30 %, 40 %, and 51 % for the years 1981–1989, 1990–1999, and the most recent era of 2000–2008, respectively (p = 0.004). In multivariate analysis, factors that were significantly associated with worse survivals included AFP level >1,000 ng/mL, tumor size >5 cm, presence of major vascular invasion, presence of extrahepatic metastases, positive surgical margins, and earlier time period in which the major hepatectomy was performed.

Conclusions

This multinational, long-term HCC survival analysis indicates that expansion of surgical indications to include major hepatectomy is justified by the significant improvement in outcomes over the past three decades observed in both the East and the West.
Literature
1.
go back to reference Ercolani G, Grazi GL, Ravaioli M, et al. Liver resection for hepatocellular carcinoma on cirrhosis: univariate and multivariate analysis of risk factors for intrahepatic recurrence. Ann Surg 2003; 237:536–543.PubMed Ercolani G, Grazi GL, Ravaioli M, et al. Liver resection for hepatocellular carcinoma on cirrhosis: univariate and multivariate analysis of risk factors for intrahepatic recurrence. Ann Surg 2003; 237:536–543.PubMed
2.
go back to reference Poon RT, Fan ST, Lo CM, et al. Improving survival results after resection of hepatocellular carcinoma: a prospective study of 377 patients over 10 years. Ann Surg 2001; 234:63–70.PubMedCrossRef Poon RT, Fan ST, Lo CM, et al. Improving survival results after resection of hepatocellular carcinoma: a prospective study of 377 patients over 10 years. Ann Surg 2001; 234:63–70.PubMedCrossRef
3.
go back to reference Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996; 334:693–699.PubMedCrossRef Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996; 334:693–699.PubMedCrossRef
4.
go back to reference Livraghi T, Meloni F, Di Stasi M, et al. Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: Is resection still the treatment of choice? Hepatology 2008; 47:82–89.PubMedCrossRef Livraghi T, Meloni F, Di Stasi M, et al. Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: Is resection still the treatment of choice? Hepatology 2008; 47:82–89.PubMedCrossRef
5.
go back to reference Poon RT, Fan ST, Lo CM, et al. Extended hepatic resection for hepatocellular carcinoma in patients with cirrhosis: is it justified? Ann Surg 2002; 236:602–611.PubMedCrossRef Poon RT, Fan ST, Lo CM, et al. Extended hepatic resection for hepatocellular carcinoma in patients with cirrhosis: is it justified? Ann Surg 2002; 236:602–611.PubMedCrossRef
6.
go back to reference Chik BH, Liu CL, Fan ST, et al. Tumor size and operative risks of extended right-sided hepatic resection for hepatocellular carcinoma: implication for preoperative portal vein embolization. Arch Surg 2007; 142:63–69.PubMedCrossRef Chik BH, Liu CL, Fan ST, et al. Tumor size and operative risks of extended right-sided hepatic resection for hepatocellular carcinoma: implication for preoperative portal vein embolization. Arch Surg 2007; 142:63–69.PubMedCrossRef
7.
go back to reference Akai H, Kiryu S, Matsuda I, et al. Detection of hepatocellular carcinoma by Gd-EOB-DTPA-enhanced liver MRI: Comparison with triple phase 64 detector row helical CT. Eur J Radiol 2010. Akai H, Kiryu S, Matsuda I, et al. Detection of hepatocellular carcinoma by Gd-EOB-DTPA-enhanced liver MRI: Comparison with triple phase 64 detector row helical CT. Eur J Radiol 2010.
8.
go back to reference Aloia TA, Zorzi D, Abdalla EK, et al. Two-surgeon technique for hepatic parenchymal transection of the noncirrhotic liver using saline-linked cautery and ultrasonic dissection. Ann Surg 2005; 242:172–177.PubMedCrossRef Aloia TA, Zorzi D, Abdalla EK, et al. Two-surgeon technique for hepatic parenchymal transection of the noncirrhotic liver using saline-linked cautery and ultrasonic dissection. Ann Surg 2005; 242:172–177.PubMedCrossRef
9.
go back to reference Donadon M, Abdalla EK, Vauthey JN. Liver hanging maneuver for large or recurrent right upper quadrant tumors. J Am Coll Surg 2007; 204:329–333.PubMedCrossRef Donadon M, Abdalla EK, Vauthey JN. Liver hanging maneuver for large or recurrent right upper quadrant tumors. J Am Coll Surg 2007; 204:329–333.PubMedCrossRef
10.
go back to reference Ishizawa T, Mise Y, Aoki T, et al. Surgical technique: new advances for expanding indications and increasing safety in liver resection for HCC: the Eastern perspective. J Hepatobiliary Pancreat Sci 2010; 17:389–393.PubMedCrossRef Ishizawa T, Mise Y, Aoki T, et al. Surgical technique: new advances for expanding indications and increasing safety in liver resection for HCC: the Eastern perspective. J Hepatobiliary Pancreat Sci 2010; 17:389–393.PubMedCrossRef
11.
go back to reference Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 2005; 12:351–355.PubMedCrossRef Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 2005; 12:351–355.PubMedCrossRef
12.
go back to reference Dahiya D, Wu TJ, Lee CF, et al. Minor versus major hepatic resection for small hepatocellular carcinoma (HCC) in cirrhotic patients: a 20-year experience. Surgery 2010; 147:676–685.PubMedCrossRef Dahiya D, Wu TJ, Lee CF, et al. Minor versus major hepatic resection for small hepatocellular carcinoma (HCC) in cirrhotic patients: a 20-year experience. Surgery 2010; 147:676–685.PubMedCrossRef
13.
go back to reference Capussotti L, Muratore A, Massucco P, et al. Major liver resections for hepatocellular carcinoma on cirrhosis: early and long-term outcomes. Liver Transpl 2004; 10:S64-68.PubMedCrossRef Capussotti L, Muratore A, Massucco P, et al. Major liver resections for hepatocellular carcinoma on cirrhosis: early and long-term outcomes. Liver Transpl 2004; 10:S64-68.PubMedCrossRef
14.
go back to reference Ng KK, Vauthey JN, Pawlik TM, et al. Is hepatic resection for large or multinodular hepatocellular carcinoma justified? Results from a multi-institutional database. Ann Surg Oncol 2005; 12:364–373.PubMedCrossRef Ng KK, Vauthey JN, Pawlik TM, et al. Is hepatic resection for large or multinodular hepatocellular carcinoma justified? Results from a multi-institutional database. Ann Surg Oncol 2005; 12:364–373.PubMedCrossRef
15.
go back to reference Wei AC, Tung-Ping Poon R, Fan ST, et al. Risk factors for perioperative morbidity and mortality after extended hepatectomy for hepatocellular carcinoma. Br J Surg 2003; 90:33–41.PubMedCrossRef Wei AC, Tung-Ping Poon R, Fan ST, et al. Risk factors for perioperative morbidity and mortality after extended hepatectomy for hepatocellular carcinoma. Br J Surg 2003; 90:33–41.PubMedCrossRef
16.
go back to reference Melendez J, Ferri E, Zwillman M, et al. Extended hepatic resection: a 6-year retrospective study of risk factors for perioperative mortality. J Am Coll Surg 2001; 192:47–53.PubMedCrossRef Melendez J, Ferri E, Zwillman M, et al. Extended hepatic resection: a 6-year retrospective study of risk factors for perioperative mortality. J Am Coll Surg 2001; 192:47–53.PubMedCrossRef
17.
go back to reference Zhou L, Rui JA, Wang SB, et al. Outcomes and prognostic factors of cirrhotic patients with hepatocellular carcinoma after radical major hepatectomy. World J Surg 2007; 31:1782–1787.PubMedCrossRef Zhou L, Rui JA, Wang SB, et al. Outcomes and prognostic factors of cirrhotic patients with hepatocellular carcinoma after radical major hepatectomy. World J Surg 2007; 31:1782–1787.PubMedCrossRef
18.
go back to reference Torzilli G, Makuuchi M, Inoue K, et al. No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Arch Surg 1999; 134:984–992.PubMedCrossRef Torzilli G, Makuuchi M, Inoue K, et al. No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Arch Surg 1999; 134:984–992.PubMedCrossRef
19.
go back to reference Fan ST, Mau Lo C, Poon RT, et al. Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg 2011; 253:745–758.PubMedCrossRef Fan ST, Mau Lo C, Poon RT, et al. Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg 2011; 253:745–758.PubMedCrossRef
20.
go back to reference Imamura H, Seyama Y, Kokudo N, et al. One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 2003; 138:1198–1206.PubMedCrossRef Imamura H, Seyama Y, Kokudo N, et al. One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 2003; 138:1198–1206.PubMedCrossRef
21.
go back to reference Miyoshi A, Takahashi T, Otsuka T, et al. Efficacy of major hepatectomy for large hepatocellular carcinoma. Hepatogastroenterology 2009; 56:768–772.PubMed Miyoshi A, Takahashi T, Otsuka T, et al. Efficacy of major hepatectomy for large hepatocellular carcinoma. Hepatogastroenterology 2009; 56:768–772.PubMed
22.
23.
go back to reference Vauthey JN, Chaoui A, Do KA, et al. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery 2000; 127:512–519.PubMedCrossRef Vauthey JN, Chaoui A, Do KA, et al. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery 2000; 127:512–519.PubMedCrossRef
24.
go back to reference Kishi Y, Abdalla EK, Chun YS, et al. Three Hundred and One Consecutive Extended Right Hepatectomies: Evaluation of Outcome Based on Systematic Liver Volumetry. Ann Surg 2009. Kishi Y, Abdalla EK, Chun YS, et al. Three Hundred and One Consecutive Extended Right Hepatectomies: Evaluation of Outcome Based on Systematic Liver Volumetry. Ann Surg 2009.
25.
go back to reference Abdalla EK, Adam R, Bilchik AJ, et al. Improving resectability of hepatic colorectal metastases: Expert consensus statement. Ann Surg Oncol 2006; 13:1271–1280.PubMedCrossRef Abdalla EK, Adam R, Bilchik AJ, et al. Improving resectability of hepatic colorectal metastases: Expert consensus statement. Ann Surg Oncol 2006; 13:1271–1280.PubMedCrossRef
26.
go back to reference Pugh RN, Murray-Lyon IM, Dawson JL, et al. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 1973; 60:646–649.PubMedCrossRef Pugh RN, Murray-Lyon IM, Dawson JL, et al. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 1973; 60:646–649.PubMedCrossRef
27.
go back to reference Zorzi D, Laurent A, Pawlik TM, et al. Chemotherapy-associated hepatotoxicity and surgery for colorectal liver metastases. Br J Surg 2007; 94:274–286.PubMedCrossRef Zorzi D, Laurent A, Pawlik TM, et al. Chemotherapy-associated hepatotoxicity and surgery for colorectal liver metastases. Br J Surg 2007; 94:274–286.PubMedCrossRef
28.
go back to reference Leevy CM, Smith F, Longueville J, et al. Indocyanine green clearance as a test for hepatic function. Evaluation by dichromatic ear densitometry. JAMA 1967; 200:236–240.PubMedCrossRef Leevy CM, Smith F, Longueville J, et al. Indocyanine green clearance as a test for hepatic function. Evaluation by dichromatic ear densitometry. JAMA 1967; 200:236–240.PubMedCrossRef
29.
go back to reference Vauthey JN, Lauwers GY, Esnaola NF, et al. Simplified staging for hepatocellular carcinoma. J Clin Oncol 2002; 20:1527–1536.PubMedCrossRef Vauthey JN, Lauwers GY, Esnaola NF, et al. Simplified staging for hepatocellular carcinoma. J Clin Oncol 2002; 20:1527–1536.PubMedCrossRef
30.
go back to reference Couinaud C. Le foie; études anatomiques et chirurgicales. Paris: Masson & Cie 1957. Couinaud C. Le foie; études anatomiques et chirurgicales. Paris: Masson & Cie 1957.
31.
go back to reference Edmondson HA, Steiner PE. Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer 1954; 7:462–503.PubMedCrossRef Edmondson HA, Steiner PE. Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer 1954; 7:462–503.PubMedCrossRef
32.
go back to reference Ishak K, Baptista A, Bianchi L, et al. Histological grading and staging of chronic hepatitis. J Hepatol 1995; 22:696–699.PubMedCrossRef Ishak K, Baptista A, Bianchi L, et al. Histological grading and staging of chronic hepatitis. J Hepatol 1995; 22:696–699.PubMedCrossRef
33.
go back to reference Ishizawa T, Hasegawa K, Aoki T, et al. Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology 2008; 134:1908–1916.PubMedCrossRef Ishizawa T, Hasegawa K, Aoki T, et al. Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology 2008; 134:1908–1916.PubMedCrossRef
34.
go back to reference Halazun KJ, Al-Mukhtar A, Aldouri A, et al. Right hepatic trisectionectomy for hepatobiliary diseases. Ann Surg 2007; 246:1065–1074.PubMedCrossRef Halazun KJ, Al-Mukhtar A, Aldouri A, et al. Right hepatic trisectionectomy for hepatobiliary diseases. Ann Surg 2007; 246:1065–1074.PubMedCrossRef
35.
go back to reference Abdalla EK, Denys A, Chevalier P, et al. Total and segmental liver volume variations: implications for liver surgery. Surgery 2004; 135:404–410.PubMedCrossRef Abdalla EK, Denys A, Chevalier P, et al. Total and segmental liver volume variations: implications for liver surgery. Surgery 2004; 135:404–410.PubMedCrossRef
36.
go back to reference Mullen JT, Ribero D, Reddy SK, et al. Hepatic insufficiency and mortality in 1,059 noncirrhotic patients undergoing major hepatectomy. J Am Coll Surg 2007; 204:854–862.PubMedCrossRef Mullen JT, Ribero D, Reddy SK, et al. Hepatic insufficiency and mortality in 1,059 noncirrhotic patients undergoing major hepatectomy. J Am Coll Surg 2007; 204:854–862.PubMedCrossRef
37.
go back to reference Kishi Y, Abdalla EK, Chun YS, et al. Three Hundred and One Consecutive Extended Right Hepatectomies: Evaluation of Outcome Based on Systematic Liver Volumetry. Ann Surg 2009; 250:540–548.PubMed Kishi Y, Abdalla EK, Chun YS, et al. Three Hundred and One Consecutive Extended Right Hepatectomies: Evaluation of Outcome Based on Systematic Liver Volumetry. Ann Surg 2009; 250:540–548.PubMed
38.
go back to reference Esnaola NF, Mirza N, Lauwers GY, et al. Comparison of clinicopathologic characteristics and outcomes after resection in patients with hepatocellular carcinoma treated in the United States, France, and Japan. Ann Surg 2003; 238:711–719.PubMedCrossRef Esnaola NF, Mirza N, Lauwers GY, et al. Comparison of clinicopathologic characteristics and outcomes after resection in patients with hepatocellular carcinoma treated in the United States, France, and Japan. Ann Surg 2003; 238:711–719.PubMedCrossRef
39.
go back to reference Kubota K, Makuuchi M, Kusaka K, et al. Measurement of liver volume and hepatic functional reserve as a guide to decision-making in resectional surgery for hepatic tumors. Hepatology 1997; 26:1176–1181.PubMed Kubota K, Makuuchi M, Kusaka K, et al. Measurement of liver volume and hepatic functional reserve as a guide to decision-making in resectional surgery for hepatic tumors. Hepatology 1997; 26:1176–1181.PubMed
40.
go back to reference Azoulay D, Castaing D, Krissat J, et al. Percutaneous portal vein embolization increases the feasibility and safety of major liver resection for hepatocellular carcinoma in injured liver. Ann Surg 2000; 232:665–672.PubMedCrossRef Azoulay D, Castaing D, Krissat J, et al. Percutaneous portal vein embolization increases the feasibility and safety of major liver resection for hepatocellular carcinoma in injured liver. Ann Surg 2000; 232:665–672.PubMedCrossRef
41.
go back to reference Imamura H, Seyama Y, Makuuchi M, et al. Sequential transcatheter arterial chemoembolization and portal vein embolization for hepatocellular carcinoma: the university of Tokyo experience. Semin Intervent Radiol 2008; 25:146–154.PubMedCrossRef Imamura H, Seyama Y, Makuuchi M, et al. Sequential transcatheter arterial chemoembolization and portal vein embolization for hepatocellular carcinoma: the university of Tokyo experience. Semin Intervent Radiol 2008; 25:146–154.PubMedCrossRef
42.
go back to reference Yoo H, Kim JH, Ko GY, et al. Sequential Transcatheter Arterial Chemoembolization and Portal Vein Embolization versus Portal Vein Embolization Only before Major Hepatectomy for Patients with Hepatocellular Carcinoma. Ann Surg Oncol 2011; 18:1251–1257.PubMedCrossRef Yoo H, Kim JH, Ko GY, et al. Sequential Transcatheter Arterial Chemoembolization and Portal Vein Embolization versus Portal Vein Embolization Only before Major Hepatectomy for Patients with Hepatocellular Carcinoma. Ann Surg Oncol 2011; 18:1251–1257.PubMedCrossRef
43.
go back to reference Ogata S, Belghiti J, Farges O, et al. Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma. Br J Surg 2006; 93:1091–1098.PubMedCrossRef Ogata S, Belghiti J, Farges O, et al. Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma. Br J Surg 2006; 93:1091–1098.PubMedCrossRef
44.
go back to reference Choti MA, Geschwind JF. Preoperative Sequential TACE and PVE to Increase Resectability in the Cirrhotic Patient With HCC. Gastrointest Cancer Res 2008; 2:47–48.PubMed Choti MA, Geschwind JF. Preoperative Sequential TACE and PVE to Increase Resectability in the Cirrhotic Patient With HCC. Gastrointest Cancer Res 2008; 2:47–48.PubMed
45.
go back to reference Hwang S, Lee SG, Ko GY, et al. Sequential preoperative ipsilateral hepatic vein embolization after portal vein embolization to induce further liver regeneration in patients with hepatobiliary malignancy. Ann Surg 2009; 249:608–616.PubMedCrossRef Hwang S, Lee SG, Ko GY, et al. Sequential preoperative ipsilateral hepatic vein embolization after portal vein embolization to induce further liver regeneration in patients with hepatobiliary malignancy. Ann Surg 2009; 249:608–616.PubMedCrossRef
46.
go back to reference Farges O, Malassagne B, Flejou JF, et al. Risk of major liver resection in patients with underlying chronic liver disease: a reappraisal. Ann Surg 1999; 229:210–215.PubMedCrossRef Farges O, Malassagne B, Flejou JF, et al. Risk of major liver resection in patients with underlying chronic liver disease: a reappraisal. Ann Surg 1999; 229:210–215.PubMedCrossRef
47.
go back to reference Sotiropoulos GC, Druhe N, Sgourakis G, et al. Liver transplantation, liver resection, and transarterial chemoembolization for hepatocellular carcinoma in cirrhosis: which is the best oncological approach? Dig Dis Sci 2009; 54:2264–2273.PubMedCrossRef Sotiropoulos GC, Druhe N, Sgourakis G, et al. Liver transplantation, liver resection, and transarterial chemoembolization for hepatocellular carcinoma in cirrhosis: which is the best oncological approach? Dig Dis Sci 2009; 54:2264–2273.PubMedCrossRef
48.
go back to reference Ruzzenente A, Capra F, Pachera S, et al. Is liver resection justified in advanced hepatocellular carcinoma? Results of an observational study in 464 patients. J Gastrointest Surg 2009; 13:1313–1320.PubMedCrossRef Ruzzenente A, Capra F, Pachera S, et al. Is liver resection justified in advanced hepatocellular carcinoma? Results of an observational study in 464 patients. J Gastrointest Surg 2009; 13:1313–1320.PubMedCrossRef
49.
go back to reference Ribero D, Abdalla EK, Madoff DC, et al. Portal vein embolization before major hepatectomy and its effects on regeneration, resectability and outcome. Br J Surg 2007; 94:1386–1394.PubMedCrossRef Ribero D, Abdalla EK, Madoff DC, et al. Portal vein embolization before major hepatectomy and its effects on regeneration, resectability and outcome. Br J Surg 2007; 94:1386–1394.PubMedCrossRef
50.
go back to reference Farges O, Belghiti J, Kianmanesh R, et al. Portal vein embolization before right hepatectomy—Prospective clinical trial. Ann Surg 2003; 237:208–217.PubMed Farges O, Belghiti J, Kianmanesh R, et al. Portal vein embolization before right hepatectomy—Prospective clinical trial. Ann Surg 2003; 237:208–217.PubMed
51.
go back to reference AJCC Cancer Staging Manual Seventh Edition. New York: Springer, 2010. AJCC Cancer Staging Manual Seventh Edition. New York: Springer, 2010.
52.
go back to reference Varotti G, Ramacciato G, Ercolani G, et al. Comparison between the fifth and sixth editions of the AJCC/UICC TNM staging systems for hepatocellular carcinoma: multicentric study on 393 cirrhotic resected patients. Eur J Surg Oncol 2005; 31:760–767.PubMedCrossRef Varotti G, Ramacciato G, Ercolani G, et al. Comparison between the fifth and sixth editions of the AJCC/UICC TNM staging systems for hepatocellular carcinoma: multicentric study on 393 cirrhotic resected patients. Eur J Surg Oncol 2005; 31:760–767.PubMedCrossRef
53.
go back to reference Lei HJ, Chau GY, Lui WY, et al. Prognostic value and clinical relevance of the 6th edition 2002 American Joint Committee on Cancer staging system in patients with resectable hepatocellular carcinoma. J Am Coll Surg 2006; 203:426–435.PubMedCrossRef Lei HJ, Chau GY, Lui WY, et al. Prognostic value and clinical relevance of the 6th edition 2002 American Joint Committee on Cancer staging system in patients with resectable hepatocellular carcinoma. J Am Coll Surg 2006; 203:426–435.PubMedCrossRef
54.
go back to reference 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; 204:1016–1027.PubMedCrossRef 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; 204:1016–1027.PubMedCrossRef
55.
go back to reference Pawlik TM, Poon RT, Abdalla EK, et al. Critical appraisal of the clinical and pathologic predictors of survival after resection of large hepatocellular carcinoma. Arch Surg 2005; 140:450–457.PubMedCrossRef Pawlik TM, Poon RT, Abdalla EK, et al. Critical appraisal of the clinical and pathologic predictors of survival after resection of large hepatocellular carcinoma. Arch Surg 2005; 140:450–457.PubMedCrossRef
Metadata
Title
Improved Long-Term Survival after Major Resection for Hepatocellular Carcinoma: A Multicenter Analysis Based on a New Definition of Major Hepatectomy
Authors
Andreas Andreou
Jean-Nicolas Vauthey
Daniel Cherqui
Giuseppe Zimmitti
Dario Ribero
Mark J. Truty
Steven H. Wei
Steven A. Curley
Alexis Laurent
Ronnie T. Poon
Jacques Belghiti
David M. Nagorney
Thomas A. Aloia
From the International Cooperative Study Group on Hepatocellular Carcinoma
Publication date
01-01-2013
Publisher
Springer-Verlag
Published in
Journal of Gastrointestinal Surgery / Issue 1/2013
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-012-2005-4

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