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Published in: Journal of Cancer Research and Clinical Oncology 10/2009

01-10-2009 | Original Paper

Liver transplantation outcomes in 1,078 hepatocellular carcinoma patients: a multi-center experience in Shanghai, China

Authors: Jia Fan, Guang-Shun Yang, Zhi-Ren Fu, Zhi-Hai Peng, Qiang Xia, Chen-Hong Peng, Jian-Ming Qian, Jian Zhou, Yang Xu, Shuang-Jian Qiu, Lin Zhong, Guang-Wen Zhou, Jian-Jun Zhang

Published in: Journal of Cancer Research and Clinical Oncology | Issue 10/2009

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Abstract

Purpose

To evaluate current selection criteria for patients undergoing liver transplantation (LT) in response to hepatocellular carcinoma (HCC), and to analyze the prognostic factors for successful transplantation.

Methods

We evaluated the outcome of 1,078 consecutive patients with HCC from the Shanghai Multi-Center Collaborative LT Group who underwent LT over a 6-year period. Clinicopathologic data for these patients were evaluated. The prognostic significance was assessed using Kaplan–Meier survival estimates and log-rank tests. Multivariate study with Cox’s proportional hazard model was used to evaluate the prognosis-relative aspects.

Results

We determined that expansion of Milan criteria to include: a solitary lesion ≤9 cm in diameter, no more than three lesions with the largest ≤5 cm, a total tumor diameter ≤9 cm without macrovascular invasion, lymph node invasion and extrahepatic metastasis (referred to as the “Shanghai criteria”), resulted in overall survival (OS) and disease-free survival (DFS) rates that were similar to the Milan criteria. Multivariate analysis using the Cox proportional hazards regression model showed that the Child-Pugh-Turcotte classification (P = 0.010, 0.000), tumor differentiation (P = 0.001, 0.000), tumor size (P = 0.000, 0.000) and number (P = 0.014, 0.016), macrovascular invasion (P = 0.022, 0.000) and alpha-fetoprotein (AFP) levels (P = 0.031, 0.003) were independent predictors of OS and DFS, while post-LT chemotherapy (OS, P = 0.000) and tumor encapsulation (DFS, P = 0.038) were independent predictors of OS or DFS.

Conclusion

Shanghai criteria expanded the current criteria while maintaining similar survival.
Literature
go back to reference Duffy JP, Vardanian A, Benjamin E, Watson M, Farmer DG, Ghobrial RM, Lipshutz G, Yersiz H, Lu DS, Lassman C, Tong MJ, Hiatt JR, Busuttil RW (2007) Liver transplantation criteria for hepatocellular carcinoma should be expanded: a 22-year experience with 467 patients at UCLA. Ann Surg 246:502–509. doi:10.1097/SLA.0b013e318148c704 (discussion 509-11)CrossRefPubMed Duffy JP, Vardanian A, Benjamin E, Watson M, Farmer DG, Ghobrial RM, Lipshutz G, Yersiz H, Lu DS, Lassman C, Tong MJ, Hiatt JR, Busuttil RW (2007) Liver transplantation criteria for hepatocellular carcinoma should be expanded: a 22-year experience with 467 patients at UCLA. Ann Surg 246:502–509. doi:10.​1097/​SLA.​0b013e318148c704​ (discussion 509-11)CrossRefPubMed
go back to reference Fan J, Zhou J, Xu Y, Qiu SJ, Wu ZQ, Yu Y, Huang XW, Tang ZY, Wang YQ (2006) Indication of liver transplantation for hepatocellular carcinoma: Shanghai Fudan Criteria. Zhonghua Yi Xue Za Zhi 86:1227–1231PubMed Fan J, Zhou J, Xu Y, Qiu SJ, Wu ZQ, Yu Y, Huang XW, Tang ZY, Wang YQ (2006) Indication of liver transplantation for hepatocellular carcinoma: Shanghai Fudan Criteria. Zhonghua Yi Xue Za Zhi 86:1227–1231PubMed
go back to reference Marubashi S, Dono K, Nagano H, Sugita Y, Asaoka T, Hama N, Miyamoto A, Takeda Y, Umeshita K, Monden M (2007) Detection of AFP mRNA-expressing cells in the peripheral blood for prediction of HCC recurrence after living donor liver transplantation. Transpl Int 20:576–582. doi:10.1111/j.1432-2277.2007.00480.x CrossRefPubMed Marubashi S, Dono K, Nagano H, Sugita Y, Asaoka T, Hama N, Miyamoto A, Takeda Y, Umeshita K, Monden M (2007) Detection of AFP mRNA-expressing cells in the peripheral blood for prediction of HCC recurrence after living donor liver transplantation. Transpl Int 20:576–582. doi:10.​1111/​j.​1432-2277.​2007.​00480.​x CrossRefPubMed
go back to reference Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699. doi:10.1056/NEJM199603143341104 CrossRefPubMed Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699. doi:10.​1056/​NEJM199603143341​104 CrossRefPubMed
go back to reference Mourad W, Khalaf H, Tulbah A, Al Omari M, Al Mana H, Neimatallah M (2007) Clinicopathologic features of hepatic neoplasms in explanted livers: a single institution experience. Ann Saudi Med 27:437–441CrossRefPubMed Mourad W, Khalaf H, Tulbah A, Al Omari M, Al Mana H, Neimatallah M (2007) Clinicopathologic features of hepatic neoplasms in explanted livers: a single institution experience. Ann Saudi Med 27:437–441CrossRefPubMed
go back to reference Onaca N, Davis GL, Goldstein RM, Jennings LW, Klintmalm GB (2007) Expanded criteria for liver transplantation in patients with hepatocellular carcinoma: a report from the International Registry of Hepatic Tumors in Liver Transplantation. Liver Transpl 13:391–399. doi:10.1002/lt.21095 CrossRefPubMed Onaca N, Davis GL, Goldstein RM, Jennings LW, Klintmalm GB (2007) Expanded criteria for liver transplantation in patients with hepatocellular carcinoma: a report from the International Registry of Hepatic Tumors in Liver Transplantation. Liver Transpl 13:391–399. doi:10.​1002/​lt.​21095 CrossRefPubMed
go back to reference Perez-Saborido B, de los Galanes SJ, Meneu-Diaz JC, Romero CJ, Elola-Olaso AM, Suarez YF, Valencia VB, Moreno-Gonzalez E (2007) Tumor recurrence after liver transplantation for hepatocellular carcinoma: recurrence pathway and prognostic factors. Transplant Proc 39:2304–2307. doi:10.1016/j.transproceed.2007.06.059 CrossRefPubMed Perez-Saborido B, de los Galanes SJ, Meneu-Diaz JC, Romero CJ, Elola-Olaso AM, Suarez YF, Valencia VB, Moreno-Gonzalez E (2007) Tumor recurrence after liver transplantation for hepatocellular carcinoma: recurrence pathway and prognostic factors. Transplant Proc 39:2304–2307. doi:10.​1016/​j.​transproceed.​2007.​06.​059 CrossRefPubMed
go back to reference Rossi M, Merli M, Lai Q, Gentili F, Mennini G, Bussotti A, Pugliese F, Della Pietra F, Poli L, Novelli G, Giusto M, Ginanni Corradini S, Iappelli M, Onetti Muda A, Di Tondo U, Gossetti F, Attili AF, Berloco PB (2007) Outcome after liver transplantation in patients with cirrhosis and hepatocellular carcinoma. Transplant Proc 39:1895–1897. doi:10.1016/j.transproceed.2007.05.083 CrossRefPubMed Rossi M, Merli M, Lai Q, Gentili F, Mennini G, Bussotti A, Pugliese F, Della Pietra F, Poli L, Novelli G, Giusto M, Ginanni Corradini S, Iappelli M, Onetti Muda A, Di Tondo U, Gossetti F, Attili AF, Berloco PB (2007) Outcome after liver transplantation in patients with cirrhosis and hepatocellular carcinoma. Transplant Proc 39:1895–1897. doi:10.​1016/​j.​transproceed.​2007.​05.​083 CrossRefPubMed
go back to reference Schwartz ME, Sung M, Mor E, Fisher A, Popescu I, Fiel I, Sheiner P, Emre S, Guy S, Miller CM (1995) A multidisciplinary approach to hepatocellular carcinoma in patients with cirrhosis. J Am Coll Surg 180:596–603PubMed Schwartz ME, Sung M, Mor E, Fisher A, Popescu I, Fiel I, Sheiner P, Emre S, Guy S, Miller CM (1995) A multidisciplinary approach to hepatocellular carcinoma in patients with cirrhosis. J Am Coll Surg 180:596–603PubMed
go back to reference Shi J, Zhu L, Liu S, Xie WF (2005) A meta-analysis of case-control studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma in China. Br J Cancer 92:607–612. doi:10.1038/sj.bjc.6602460 CrossRefPubMed Shi J, Zhu L, Liu S, Xie WF (2005) A meta-analysis of case-control studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma in China. Br J Cancer 92:607–612. doi:10.​1038/​sj.​bjc.​6602460 CrossRefPubMed
go back to reference Tang ZY (2001) Hepatocellular carcinoma—cause, treatment and metastasis. World J Gastroenterol 7:445–454PubMed Tang ZY (2001) Hepatocellular carcinoma—cause, treatment and metastasis. World J Gastroenterol 7:445–454PubMed
go back to reference Tang ZY, Ye SL, Liu YK, Qin LX, Sun HC, Ye QH, Wang L, Zhou J, Qiu SJ, Li Y, Ji XN, Liu H, Xia JL, Wu ZQ, Fan J, Ma ZC, Zhou XD, Lin ZY, Liu KD (2004) A decade’s studies on metastasis of hepatocellular carcinoma. J Cancer Res Clin Oncol 130:187–196. doi:10.1007/s00432-003-0511-1 CrossRefPubMed Tang ZY, Ye SL, Liu YK, Qin LX, Sun HC, Ye QH, Wang L, Zhou J, Qiu SJ, Li Y, Ji XN, Liu H, Xia JL, Wu ZQ, Fan J, Ma ZC, Zhou XD, Lin ZY, Liu KD (2004) A decade’s studies on metastasis of hepatocellular carcinoma. J Cancer Res Clin Oncol 130:187–196. doi:10.​1007/​s00432-003-0511-1 CrossRefPubMed
go back to reference Vitale A, Gringeri E, Valmasoni M, D’Amico F, Carraro A, Pauletto A, D’Amico FJ, Polacco M, D’Amico DF, Cillo U (2007) Long-term results of liver transplantation for hepatocellular carcinoma: an update of the University of Padova experience. Transplant Proc 39:1892–1894. doi:10.1016/j.transproceed.2007.05.031 CrossRefPubMed Vitale A, Gringeri E, Valmasoni M, D’Amico F, Carraro A, Pauletto A, D’Amico FJ, Polacco M, D’Amico DF, Cillo U (2007) Long-term results of liver transplantation for hepatocellular carcinoma: an update of the University of Padova experience. Transplant Proc 39:1892–1894. doi:10.​1016/​j.​transproceed.​2007.​05.​031 CrossRefPubMed
go back to reference Vivarelli M, Cucchetti A, Piscaglia F, La Barba G, Bolondi L, Cavallari A, Pinna AD (2005) Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression. Liver Transpl 11:497–503. doi:10.1002/lt.20391 CrossRefPubMed Vivarelli M, Cucchetti A, Piscaglia F, La Barba G, Bolondi L, Cavallari A, Pinna AD (2005) Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression. Liver Transpl 11:497–503. doi:10.​1002/​lt.​20391 CrossRefPubMed
go back to reference Wittekind C, International Union Against Cancer (2005) TNM atlas : illustrated guide to the TNM/pTNM classification of malignant tumours. Springer, Berlin Wittekind C, International Union Against Cancer (2005) TNM atlas : illustrated guide to the TNM/pTNM classification of malignant tumours. Springer, Berlin
go back to reference Yao FY, Ferrell L, Bass NM, Watson JJ, Bacchetti P, Venook A, Ascher NL, Roberts JP (2001) Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 33:1394–1403. doi:10.1053/jhep.2001.24563 CrossRefPubMed Yao FY, Ferrell L, Bass NM, Watson JJ, Bacchetti P, Venook A, Ascher NL, Roberts JP (2001) Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 33:1394–1403. doi:10.​1053/​jhep.​2001.​24563 CrossRefPubMed
go back to reference Yao FY, Ferrell L, Bass NM, Bacchetti P, Ascher NL, Roberts JP (2002) Liver transplantation for hepatocellular carcinoma: comparison of the proposed UCSF criteria with the Milan criteria and the Pittsburgh modified TNM criteria. Liver Transpl 8:765–774. doi:10.1053/jlts.2002.34892 CrossRefPubMed Yao FY, Ferrell L, Bass NM, Bacchetti P, Ascher NL, Roberts JP (2002) Liver transplantation for hepatocellular carcinoma: comparison of the proposed UCSF criteria with the Milan criteria and the Pittsburgh modified TNM criteria. Liver Transpl 8:765–774. doi:10.​1053/​jlts.​2002.​34892 CrossRefPubMed
go back to reference Zhou J, Fan J, Wang Z, Wu ZQ, Qiu SJ, Huang XW, Yu Y, Sun J, Xiao YS, He YF, Wang YQ, Tang ZY (2006) Conversion to sirolimus immunosuppression in liver transplantation recipients with hepatocellular carcinoma: Report of an initial experience. World J Gastroenterol 12:3114–3118PubMed Zhou J, Fan J, Wang Z, Wu ZQ, Qiu SJ, Huang XW, Yu Y, Sun J, Xiao YS, He YF, Wang YQ, Tang ZY (2006) Conversion to sirolimus immunosuppression in liver transplantation recipients with hepatocellular carcinoma: Report of an initial experience. World J Gastroenterol 12:3114–3118PubMed
go back to reference Zieniewicz K, Patkowski W, Nyckowski P, Alsharabi A, Michalowicz B, Pawlak J, Paluszkiewicz R, Wroblewski T, Najnigier B, Smoter P, Hevelke P, Skwarek A, Remiszewski P, Kotulski M, Skalski M, Paczek L, Krawczyk M (2007) Results of liver transplantation for hepatocellular cancer. Ann Transplant 12:11–14PubMed Zieniewicz K, Patkowski W, Nyckowski P, Alsharabi A, Michalowicz B, Pawlak J, Paluszkiewicz R, Wroblewski T, Najnigier B, Smoter P, Hevelke P, Skwarek A, Remiszewski P, Kotulski M, Skalski M, Paczek L, Krawczyk M (2007) Results of liver transplantation for hepatocellular cancer. Ann Transplant 12:11–14PubMed
Metadata
Title
Liver transplantation outcomes in 1,078 hepatocellular carcinoma patients: a multi-center experience in Shanghai, China
Authors
Jia Fan
Guang-Shun Yang
Zhi-Ren Fu
Zhi-Hai Peng
Qiang Xia
Chen-Hong Peng
Jian-Ming Qian
Jian Zhou
Yang Xu
Shuang-Jian Qiu
Lin Zhong
Guang-Wen Zhou
Jian-Jun Zhang
Publication date
01-10-2009
Publisher
Springer-Verlag
Published in
Journal of Cancer Research and Clinical Oncology / Issue 10/2009
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-009-0584-6

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