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Published in: Langenbeck's Archives of Surgery 5/2018

01-08-2018 | ORIGINAL ARTICLE

Hangzhou criteria are more accurate than Milan criteria in predicting long-term survival after liver transplantation for HCC in Germany

Authors: Zhi Qu, Qi Ling, Jill Gwiasda, Xiao Xu, Harald Schrem, Jan Beneke, Alexander Kaltenborn, Christian Krauth, Heiko Mix, Jürgen Klempnauer, Nikos Emmanouilidis

Published in: Langenbeck's Archives of Surgery | Issue 5/2018

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Abstract

Background

Milan criteria are used for patient selection in liver transplantation for hepatocellular carcinoma (HCC). Hangzhou criteria have been shown in China to enable access to liver transplantation for more patients when compared to Milan criteria without negative effects on long-term survival. The purpose of this study was to evaluate the Hangzhou criteria in a German cohort.

Methods

One hundred fifty-nine patients transplanted for HCC between 1975 and 2010 were investigated. Patients were categorized into four groups depending on the fulfillment of Milan and Hangzhou criteria. General and tumor baseline characteristics were compared. Overall and tumor-free survival rates were investigated with the Kaplan-Meier analysis.

Results

One-, 3-, 5-, and 10-year survival rates for patients fulfilling Milan criteria (n = 68) were 89.7, 83.7, 75.8, and 62.1%, respectively, versus 89.8, 82.2, 75.2, and 62.6% for patients fulfilling Hangzhou criteria (n = 109) (p = 0.833). When comparing patients exceeding Milan or Hangzhou criteria, survival rates were 75.3, 53.2, 48.1, and 41.1% versus 63.3, 31.4, 26.9, and 22.1%, respectively (p = 0.019). The comparison of tumor-free survival rates in patients fulfilling Milan or Hangzhou criteria was statistically not significant (p = 0.785), whereas the comparison of the groups exceeding the criteria showed significantly worse survival for patients outside Hangzhou criteria (p = 0.007). The proportion of patients fulfilling Hangzhou criteria (68.6%) was significantly larger as compared to the proportion fulfilling Milan criteria (42.8%) (p < 0.001).

Conclusion

Hangzhou criteria are more accurate in predicting long-term survival after liver transplantation for HCC in Germany. Deployment of the Hangzhou criteria for patient selection could enlarge the pool of transplantable patients.
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Literature
1.
go back to reference Ferlay J, Shin H, Bray F et al (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917CrossRefPubMed Ferlay J, Shin H, Bray F et al (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917CrossRefPubMed
4.
5.
go back to reference 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(11):693–700CrossRefPubMed 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(11):693–700CrossRefPubMed
6.
go back to reference Clavien P-A, Lesurtel M, Bossuyt PMM et al (2012) Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol 13(1):e11–e22CrossRefPubMed Clavien P-A, Lesurtel M, Bossuyt PMM et al (2012) Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol 13(1):e11–e22CrossRefPubMed
7.
go back to reference Rahimi RS, Trotter JF (2015) Liver transplantation for hepatocellular carcinoma: outcomes and treatment options for recurrence. Ann Gastroenterol 28(3):323PubMedPubMedCentral Rahimi RS, Trotter JF (2015) Liver transplantation for hepatocellular carcinoma: outcomes and treatment options for recurrence. Ann Gastroenterol 28(3):323PubMedPubMedCentral
8.
go back to reference Bundesärztekammer (2008) Richtlinien zur Organtransplantation gem. § 16 TPG. Deutsches Ärzteblatt 105:1461–1464 Bundesärztekammer (2008) Richtlinien zur Organtransplantation gem. § 16 TPG. Deutsches Ärzteblatt 105:1461–1464
9.
go back to reference Yao FY, Ferrell L, Bass NM et al (2001) Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 33(6):1394–1403CrossRefPubMed Yao FY, Ferrell L, Bass NM et al (2001) Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 33(6):1394–1403CrossRefPubMed
10.
go back to reference Mazzaferro V, Llovet JM, Miceli R et al (2009) Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 10(1):35–43CrossRefPubMed Mazzaferro V, Llovet JM, Miceli R et al (2009) Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 10(1):35–43CrossRefPubMed
11.
go back to reference Herrero JI, Sangro B, Quiroga J et al (2001) Influence of tumor characteristics on the outcome of liver transplantation among patients with liver cirrhosis and hepatocellular carcinoma. Liver Transpl 7(7):631–636CrossRefPubMed Herrero JI, Sangro B, Quiroga J et al (2001) Influence of tumor characteristics on the outcome of liver transplantation among patients with liver cirrhosis and hepatocellular carcinoma. Liver Transpl 7(7):631–636CrossRefPubMed
12.
go back to reference DuBay D, Sandroussi C, Sandhu L et al (2011) Liver transplantation for advanced hepatocellular carcinoma using poor tumor differentiation on biopsy as an exclusion criterion. Ann Surg 253(1):166–172CrossRefPubMed DuBay D, Sandroussi C, Sandhu L et al (2011) Liver transplantation for advanced hepatocellular carcinoma using poor tumor differentiation on biopsy as an exclusion criterion. Ann Surg 253(1):166–172CrossRefPubMed
13.
go back to reference Kaido T, Ogawa K, Mori A et al (2013) Usefulness of the Kyoto criteria as expanded selection criteria for liver transplantation for hepatocellular carcinoma. Surgery 154(5):1053–1060CrossRefPubMed Kaido T, Ogawa K, Mori A et al (2013) Usefulness of the Kyoto criteria as expanded selection criteria for liver transplantation for hepatocellular carcinoma. Surgery 154(5):1053–1060CrossRefPubMed
14.
go back to reference Zheng S-S, Xu X, Wu J et al (2008) Liver transplantation for hepatocellular carcinoma: Hangzhou experiences. Transplantation 85(12):1726–1732CrossRefPubMed Zheng S-S, Xu X, Wu J et al (2008) Liver transplantation for hepatocellular carcinoma: Hangzhou experiences. Transplantation 85(12):1726–1732CrossRefPubMed
15.
go back to reference Erkekoglu P, Oral D, Chao M-W et al (2017) Hepatocellular carcinoma and possible chemical and biological causes: a review. J Environ Pathol Toxicol Oncol 36(2):171–190CrossRefPubMed Erkekoglu P, Oral D, Chao M-W et al (2017) Hepatocellular carcinoma and possible chemical and biological causes: a review. J Environ Pathol Toxicol Oncol 36(2):171–190CrossRefPubMed
16.
go back to reference Lafaro KJ, Demirjian AN, Pawlik TM (2015) Epidemiology of hepatocellular carcinoma. Surg Oncol Clin 24(1):1–17CrossRef Lafaro KJ, Demirjian AN, Pawlik TM (2015) Epidemiology of hepatocellular carcinoma. Surg Oncol Clin 24(1):1–17CrossRef
17.
go back to reference Emmanouilidis N, Peters R, Ringe BP, Güner Z, Ramackers W, Bektas H, Lehner F, Manns M, Klempnauer J, Schrem H (2016) Liver transplantation for hepatocellular carcinoma: a single center resume overlooking four decades of experience. J Transplant 2016:7895956. https://doi.org/10.1155/2016/7895956 Emmanouilidis N, Peters R, Ringe BP, Güner Z, Ramackers W, Bektas H, Lehner F, Manns M, Klempnauer J, Schrem H (2016) Liver transplantation for hepatocellular carcinoma: a single center resume overlooking four decades of experience. J Transplant 2016:7895956. https://​doi.​org/​10.​1155/​2016/​7895956
18.
go back to reference Lei JY, Wang WT, Yan LN (2014) Hangzhou criteria for liver transplantation in hepatocellular carcinoma: a single-center experience. Eur J Gastroenterol Hepatol 26(2):200–204CrossRefPubMed Lei JY, Wang WT, Yan LN (2014) Hangzhou criteria for liver transplantation in hepatocellular carcinoma: a single-center experience. Eur J Gastroenterol Hepatol 26(2):200–204CrossRefPubMed
19.
20.
go back to reference Xia W, Ke Q, Guo H et al (2017) Expansion of the Milan criteria without any sacrifice: combination of the Hangzhou criteria with the pre-transplant platelet-to-lymphocyte ratio. BMC Cancer 17(1):14CrossRefPubMedPubMedCentral Xia W, Ke Q, Guo H et al (2017) Expansion of the Milan criteria without any sacrifice: combination of the Hangzhou criteria with the pre-transplant platelet-to-lymphocyte ratio. BMC Cancer 17(1):14CrossRefPubMedPubMedCentral
21.
go back to reference Audet M, Panaro F, Piardi T et al (2009) Are the Hangzhou criteria adaptable to hepatocellular carcinoma patients for liver transplantation in Western countries? Liver Transpl 15(7):822–823CrossRefPubMed Audet M, Panaro F, Piardi T et al (2009) Are the Hangzhou criteria adaptable to hepatocellular carcinoma patients for liver transplantation in Western countries? Liver Transpl 15(7):822–823CrossRefPubMed
22.
go back to reference Xu X, Lu D, Ling Q et al (2015) Liver transplantation for hepatocellular carcinoma beyond the Milan criteria. Gut:1035–1041 Xu X, Lu D, Ling Q et al (2015) Liver transplantation for hepatocellular carcinoma beyond the Milan criteria. Gut:1035–1041
23.
go back to reference Mancuso A, Perricone G (2014) Hepatocellular carcinoma and liver transplantation: state of the art. J Clin Transl Hepatol 2(3):176–181PubMedPubMedCentral Mancuso A, Perricone G (2014) Hepatocellular carcinoma and liver transplantation: state of the art. J Clin Transl Hepatol 2(3):176–181PubMedPubMedCentral
24.
25.
go back to reference Xu X, Lu D, Zheng S (2015) Response to “Influence on the other patients in the waiting list when expanding the Milan criteria” and “Can Milan criteria be expanded effectively for liver transplantation in patients with HCC?”. Transl Gastrointest Cancer 4(6):492–493 Xu X, Lu D, Zheng S (2015) Response to “Influence on the other patients in the waiting list when expanding the Milan criteria” and “Can Milan criteria be expanded effectively for liver transplantation in patients with HCC?”. Transl Gastrointest Cancer 4(6):492–493
26.
go back to reference Venkatesh SK, Chandan V, Roberts LR (2014) Liver masses: a clinical, radiologic, and pathologic perspective. Clin Gastroenterol Hepatol 12(9):1414–1429CrossRefPubMed Venkatesh SK, Chandan V, Roberts LR (2014) Liver masses: a clinical, radiologic, and pathologic perspective. Clin Gastroenterol Hepatol 12(9):1414–1429CrossRefPubMed
27.
go back to reference Berry K, Ioannou GN (2013) Serum alpha-fetoprotein level independently predicts posttransplant survival in patients with hepatocellular carcinoma. Liver Transpl 19(6):634–645CrossRefPubMed Berry K, Ioannou GN (2013) Serum alpha-fetoprotein level independently predicts posttransplant survival in patients with hepatocellular carcinoma. Liver Transpl 19(6):634–645CrossRefPubMed
28.
go back to reference Yang SH, Suh K-S, Lee HW et al (2007) A revised scoring system utilizing serum alphafetoprotein levels to expand candidates for living donor transplantation in hepatocellular carcinoma. Surgery 141(5):598–609CrossRefPubMed Yang SH, Suh K-S, Lee HW et al (2007) A revised scoring system utilizing serum alphafetoprotein levels to expand candidates for living donor transplantation in hepatocellular carcinoma. Surgery 141(5):598–609CrossRefPubMed
29.
go back to reference Toso C, Asthana S, Bigam DL et al (2009) Reassessing selection criteria prior to liver transplantation for hepatocellular carcinoma utilizing the Scientific Registry of Transplant Recipients database. Hepatology 49(3):832–838CrossRefPubMed Toso C, Asthana S, Bigam DL et al (2009) Reassessing selection criteria prior to liver transplantation for hepatocellular carcinoma utilizing the Scientific Registry of Transplant Recipients database. Hepatology 49(3):832–838CrossRefPubMed
30.
go back to reference Muscari F, Foppa B, Kamar N et al (2009) Liberal selection criteria for liver transplantation for hepatocellular carcinoma. Br J Surg 96(7):785–791CrossRefPubMed Muscari F, Foppa B, Kamar N et al (2009) Liberal selection criteria for liver transplantation for hepatocellular carcinoma. Br J Surg 96(7):785–791CrossRefPubMed
31.
go back to reference Lai Q, Avolio AW, Manzia TM et al (2012) Combination of biological and morphological parameters for the selection of patients with hepatocellular carcinoma waiting for liver transplantation. Clin Transpl 26(2) Lai Q, Avolio AW, Manzia TM et al (2012) Combination of biological and morphological parameters for the selection of patients with hepatocellular carcinoma waiting for liver transplantation. Clin Transpl 26(2)
32.
go back to reference Schrem H, Volz S, Koch H-F et al (2017) Statistical approach to quality assessment in liver transplantation. Langenbeck's Arch Surg:1–11 Schrem H, Volz S, Koch H-F et al (2017) Statistical approach to quality assessment in liver transplantation. Langenbeck's Arch Surg:1–11
Metadata
Title
Hangzhou criteria are more accurate than Milan criteria in predicting long-term survival after liver transplantation for HCC in Germany
Authors
Zhi Qu
Qi Ling
Jill Gwiasda
Xiao Xu
Harald Schrem
Jan Beneke
Alexander Kaltenborn
Christian Krauth
Heiko Mix
Jürgen Klempnauer
Nikos Emmanouilidis
Publication date
01-08-2018
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 5/2018
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-018-1696-8

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