Skip to main content
Top
Published in: Current Hepatology Reports 4/2020

01-12-2020 | Liver Transplantation | Hepatic Cancer (N Parikh, Section Editor)

Current Transplant Criteria for Hepatocellular Carcinoma—Overuse or Underuse

Authors: Varun Saxena, Neil Mehta

Published in: Current Hepatology Reports | Issue 4/2020

Login to get access

Abstract

In the USA, hepatocellular carcinoma (HCC) has the most rapidly increasing cancer incidence since 1980, has a rate of death that has increased by 43% between 2000 and 2016 and is currently the second most lethal tumor with a 5-year survival of 18%. While the expected 5-year survival after liver transplant (LT) in patients with HCC is attractive at over 70%, LT is limited by extreme shortage of organs and post-LT immunosuppression. Numerous changes to the liver allocation system for HCC in the USA have been applied since 2002. However, for the most part, USA HCC patients continue to receive similar priority for LT despite ample evidence that tumor size and number is only one of many contributors to urgency (i.e. waitlist dropout), utility (i.e. post-LT survival) and LT survival benefit. In this review, we examine where current LT criteria for HCC has resulted in overuse including 1) compensated patients with a single, small, well-treated tumor and 2) patients with HCC amenable to up-front resection. We further examine where current LT criteria for HCC has resulted in underuse including 1) patients with HCC outside of standard criteria but who have favorable markers of tumor biology based on response to local regional therapies, alpha-fetoprotein and other serum biomarker levels, 18F-FDG-PET scan results and tumor biopsy as well as 2) HCC patients with decompensated cirrhosis who have an increased risk of waitlist dropout and thus likely merit additional priority given their increased LT survival benefit.
Literature
3.
go back to reference Jemal A, Ward EM, Johnson CJ, et al. Annual Report to the Nation on the Status of Cancer, 1975-2014, Featuring survival. J Natl Cancer Inst 2017;109. Jemal A, Ward EM, Johnson CJ, et al. Annual Report to the Nation on the Status of Cancer, 1975-2014, Featuring survival. J Natl Cancer Inst 2017;109.
4.
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;334:693–9.PubMed 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;334:693–9.PubMed
5.
go back to reference Kamath PS, Wiesner RH, Malinchoc M, et al. A model to predict survival in patients with end-stage liver disease. Hepatology. 2001;33:464–70.PubMed Kamath PS, Wiesner RH, Malinchoc M, et al. A model to predict survival in patients with end-stage liver disease. Hepatology. 2001;33:464–70.PubMed
6.
go back to reference Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018;68:723–50.PubMed Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018;68:723–50.PubMed
7.
go back to reference Freeman RB Jr, Wiesner RH, Roberts JP, McDiarmid S, Dykstra DM, Merion RM. Improving liver allocation: MELD and PELD. Am J Transplant. 2004;4(Suppl 9):114–31.PubMed Freeman RB Jr, Wiesner RH, Roberts JP, McDiarmid S, Dykstra DM, Merion RM. Improving liver allocation: MELD and PELD. Am J Transplant. 2004;4(Suppl 9):114–31.PubMed
8.
go back to reference Wiesner RH, Freeman RB, Mulligan DC. Liver transplantation for hepatocellular cancer: the impact of the MELD allocation policy. Gastroenterology. 2004;127:S261–7.PubMed Wiesner RH, Freeman RB, Mulligan DC. Liver transplantation for hepatocellular cancer: the impact of the MELD allocation policy. Gastroenterology. 2004;127:S261–7.PubMed
9.
go back to reference Wald C, Russo MW, Heimbach JK, Hussain HK, Pomfret EA, Bruix J. New OPTN/UNOS policy for liver transplant allocation: standardization of liver imaging, diagnosis, classification, and reporting of hepatocellular carcinoma. Radiology. 2013;266:376–82.PubMed Wald C, Russo MW, Heimbach JK, Hussain HK, Pomfret EA, Bruix J. New OPTN/UNOS policy for liver transplant allocation: standardization of liver imaging, diagnosis, classification, and reporting of hepatocellular carcinoma. Radiology. 2013;266:376–82.PubMed
10.
go back to reference Heimbach JK, Hirose R, Stock PG, et al. Delayed hepatocellular carcinoma model for end-stage liver disease exception score improves disparity in access to liver transplant in the United States. Hepatology. 2015;61:1643–50.PubMedPubMedCentral Heimbach JK, Hirose R, Stock PG, et al. Delayed hepatocellular carcinoma model for end-stage liver disease exception score improves disparity in access to liver transplant in the United States. Hepatology. 2015;61:1643–50.PubMedPubMedCentral
11.
go back to reference Washburn K, Edwards E, Harper A, Freeman R. Hepatocellular carcinoma patients are advantaged in the current liver transplant allocation system. Am J Transplant. 2010;10:1643–8.PubMed Washburn K, Edwards E, Harper A, Freeman R. Hepatocellular carcinoma patients are advantaged in the current liver transplant allocation system. Am J Transplant. 2010;10:1643–8.PubMed
13.
go back to reference Hameed B, Mehta N, Sapisochin G, Roberts JP, Yao FY. Alpha-fetoprotein level > 1000 ng/mL as an exclusion criterion for liver transplantation in patients with hepatocellular carcinoma meeting the Milan criteria. Liver Transpl. 2014;20:945–51.PubMedPubMedCentral Hameed B, Mehta N, Sapisochin G, Roberts JP, Yao FY. Alpha-fetoprotein level > 1000 ng/mL as an exclusion criterion for liver transplantation in patients with hepatocellular carcinoma meeting the Milan criteria. Liver Transpl. 2014;20:945–51.PubMedPubMedCentral
14.
go back to reference Duvoux C, Roudot-Thoraval F, Decaens T, et al. (2012) Liver transplantation for hepatocellular carcinoma: a model including alpha-fetoprotein improves the performance of Milan criteria. Gastroenterology 143:986–94 e3; quiz e14–5 Duvoux C, Roudot-Thoraval F, Decaens T, et al. (2012) Liver transplantation for hepatocellular carcinoma: a model including alpha-fetoprotein improves the performance of Milan criteria. Gastroenterology 143:986–94 e3; quiz e14–5
15.
go back to reference Levi DM, Tzakis AG, Martin P, et al. Liver transplantation for hepatocellular carcinoma in the model for end-stage liver disease era. J Am Coll Surg. 2010;210:727–34 35-6.PubMed Levi DM, Tzakis AG, Martin P, et al. Liver transplantation for hepatocellular carcinoma in the model for end-stage liver disease era. J Am Coll Surg. 2010;210:727–34 35-6.PubMed
16.
go back to reference Grat M, Krasnodebski M, Patkowski W, et al. Relevance of pre-transplant alpha-fetoprotein dynamics in liver transplantation for hepatocellular cancer. Ann Transplant. 2016;21:115–24.PubMed Grat M, Krasnodebski M, Patkowski W, et al. Relevance of pre-transplant alpha-fetoprotein dynamics in liver transplantation for hepatocellular cancer. Ann Transplant. 2016;21:115–24.PubMed
17.
go back to reference Hong G, Suh KS, Suh SW, et al. Alpha-fetoprotein and (18)F-FDG positron emission tomography predict tumor recurrence better than Milan criteria in living donor liver transplantation. J Hepatol. 2016;64:852–9.PubMed Hong G, Suh KS, Suh SW, et al. Alpha-fetoprotein and (18)F-FDG positron emission tomography predict tumor recurrence better than Milan criteria in living donor liver transplantation. J Hepatol. 2016;64:852–9.PubMed
18.
go back to reference Toso C, Meeberg G, Hernandez-Alejandro R, et al. Total tumor volume and alpha-fetoprotein for selection of transplant candidates with hepatocellular carcinoma: a prospective validation. Hepatology. 2015;62:158–65.PubMed Toso C, Meeberg G, Hernandez-Alejandro R, et al. Total tumor volume and alpha-fetoprotein for selection of transplant candidates with hepatocellular carcinoma: a prospective validation. Hepatology. 2015;62:158–65.PubMed
19.
go back to reference Ravaioli M, Grazi GL, Piscaglia F, et al. Liver transplantation for hepatocellular carcinoma: results of down-staging in patients initially outside the Milan selection criteria. Am J Transplant. 2008;8:2547–57.PubMed Ravaioli M, Grazi GL, Piscaglia F, et al. Liver transplantation for hepatocellular carcinoma: results of down-staging in patients initially outside the Milan selection criteria. Am J Transplant. 2008;8:2547–57.PubMed
20.
go back to reference Lai Q, Avolio AW, Manzia TM, et al. Combination of biological and morphological parameters for the selection of patients with hepatocellular carcinoma waiting for liver transplantation. Clin Transpl. 2012;26:E125–31. Lai Q, Avolio AW, Manzia TM, et al. Combination of biological and morphological parameters for the selection of patients with hepatocellular carcinoma waiting for liver transplantation. Clin Transpl. 2012;26:E125–31.
21.
go back to reference Yao FY, Mehta N, Flemming J, et al. Downstaging of hepatocellular cancer before liver transplant: long-term outcome compared to tumors within Milan criteria. Hepatology. 2015;61:1968–77.PubMedPubMedCentral Yao FY, Mehta N, Flemming J, et al. Downstaging of hepatocellular cancer before liver transplant: long-term outcome compared to tumors within Milan criteria. Hepatology. 2015;61:1968–77.PubMedPubMedCentral
22.
go back to reference Berry K, Ioannou GN. Serum alpha-fetoprotein level independently predicts posttransplant survival in patients with hepatocellular carcinoma. Liver Transpl. 2013;19:634–45.PubMed Berry K, Ioannou GN. Serum alpha-fetoprotein level independently predicts posttransplant survival in patients with hepatocellular carcinoma. Liver Transpl. 2013;19:634–45.PubMed
23.
go back to reference Heimbach JK, Kulik LM, Finn RS, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology. 2018;67:358–80.PubMed Heimbach JK, Kulik LM, Finn RS, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology. 2018;67:358–80.PubMed
24.
go back to reference Yao FY, Ferrell L, Bass NM, et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology. 2001;33:1394–403.PubMed Yao FY, Ferrell L, Bass NM, et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology. 2001;33:1394–403.PubMed
25.
go back to reference Yao FY, Xiao L, Bass NM, Kerlan R, Ascher NL, Roberts JP. Liver transplantation for hepatocellular carcinoma: validation of the UCSF-expanded criteria based on preoperative imaging. Am J Transplant. 2007;7:2587–96.PubMed Yao FY, Xiao L, Bass NM, Kerlan R, Ascher NL, Roberts JP. Liver transplantation for hepatocellular carcinoma: validation of the UCSF-expanded criteria based on preoperative imaging. Am J Transplant. 2007;7:2587–96.PubMed
26.
go back to reference Mazzaferro V, Llovet JM, Miceli R, et al. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol. 2009;10:35–43.PubMed Mazzaferro V, Llovet JM, Miceli R, et al. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol. 2009;10:35–43.PubMed
27.
go back to reference Toso C, Asthana S, Bigam DL, Shapiro AM, Kneteman NM. Reassessing selection criteria prior to liver transplantation for hepatocellular carcinoma utilizing the Scientific Registry of Transplant Recipients database. Hepatology. 2009;49:832–8.PubMed Toso C, Asthana S, Bigam DL, Shapiro AM, Kneteman NM. Reassessing selection criteria prior to liver transplantation for hepatocellular carcinoma utilizing the Scientific Registry of Transplant Recipients database. Hepatology. 2009;49:832–8.PubMed
28.
go back to reference Massie AB, Caffo B, Gentry SE, et al. MELD exceptions and rates of waiting list outcomes. Am J Transplant. 2011;11:2362–71.PubMedPubMedCentral Massie AB, Caffo B, Gentry SE, et al. MELD exceptions and rates of waiting list outcomes. Am J Transplant. 2011;11:2362–71.PubMedPubMedCentral
29.
go back to reference Northup PG, Intagliata NM, Shah NL, Pelletier SJ, Berg CL, Argo CK. Excess mortality on the liver transplant waiting list: unintended policy consequences and model for end-stage liver disease (MELD) inflation. Hepatology. 2015;61:285–91.PubMed Northup PG, Intagliata NM, Shah NL, Pelletier SJ, Berg CL, Argo CK. Excess mortality on the liver transplant waiting list: unintended policy consequences and model for end-stage liver disease (MELD) inflation. Hepatology. 2015;61:285–91.PubMed
30.
go back to reference Mehta N, Dodge JL, Hirose R, Roberts JP, Yao FY. Increasing liver transplantation wait-list dropout for hepatocellular carcinoma with widening geographical disparities: implications for organ allocation. Liver Transpl. 2018;24:1346–56.PubMedPubMedCentral Mehta N, Dodge JL, Hirose R, Roberts JP, Yao FY. Increasing liver transplantation wait-list dropout for hepatocellular carcinoma with widening geographical disparities: implications for organ allocation. Liver Transpl. 2018;24:1346–56.PubMedPubMedCentral
31.
go back to reference SRTR Analysis Report, ‘Data Request from the OPTN Liver and Intestinal Organ Transplantation committee.’ Presented December 14, 2016. SRTR Analysis Report, ‘Data Request from the OPTN Liver and Intestinal Organ Transplantation committee.’ Presented December 14, 2016.
32.
go back to reference Kim WR, Lake JR, Smith JM, et al. OPTN/SRTR 2017 annual data report: liver. Am J Transplant. 2019;19(Suppl 2):184–283.PubMed Kim WR, Lake JR, Smith JM, et al. OPTN/SRTR 2017 annual data report: liver. Am J Transplant. 2019;19(Suppl 2):184–283.PubMed
33.
34.
go back to reference Berry K, Ioannou GN (2015) Comparison of liver transplant-related survival benefit in patients with versus without hepatocellular carcinoma in the United States. Gastroenterology 149:669–80; quiz e15–6. Berry K, Ioannou GN (2015) Comparison of liver transplant-related survival benefit in patients with versus without hepatocellular carcinoma in the United States. Gastroenterology 149:669–80; quiz e15–6.
35.
go back to reference Schaubel DE, Guidinger MK, Biggins SW, et al. Survival benefit-based deceased-donor liver allocation. Am J Transplant. 2009;9:970–81.PubMedPubMedCentral Schaubel DE, Guidinger MK, Biggins SW, et al. Survival benefit-based deceased-donor liver allocation. Am J Transplant. 2009;9:970–81.PubMedPubMedCentral
36.
go back to reference Vitale A, Morales RR, Zanus G, et al. Barcelona clinic liver cancer staging and transplant survival benefit for patients with hepatocellular carcinoma: a multicentre, cohort study. Lancet Oncol. 2011;12:654–62.PubMed Vitale A, Morales RR, Zanus G, et al. Barcelona clinic liver cancer staging and transplant survival benefit for patients with hepatocellular carcinoma: a multicentre, cohort study. Lancet Oncol. 2011;12:654–62.PubMed
37.
go back to reference Cillo U, Vitale A, Polacco M, Fasolo E. Liver transplantation for hepatocellular carcinoma through the lens of transplant benefit. Hepatology. 2017;65:1741–8.PubMed Cillo U, Vitale A, Polacco M, Fasolo E. Liver transplantation for hepatocellular carcinoma through the lens of transplant benefit. Hepatology. 2017;65:1741–8.PubMed
38.
go back to reference Halazun KJ, Patzer RE, Rana AA, et al. Standing the test of time: outcomes of a decade of prioritizing patients with hepatocellular carcinoma, results of the UNOS natural geographic experiment. Hepatology. 2014;60:1957–62.PubMed Halazun KJ, Patzer RE, Rana AA, et al. Standing the test of time: outcomes of a decade of prioritizing patients with hepatocellular carcinoma, results of the UNOS natural geographic experiment. Hepatology. 2014;60:1957–62.PubMed
40.
go back to reference Mehta N, Dodge JL, Goel A, Roberts JP, Hirose R, Yao FY. Identification of liver transplant candidates with hepatocellular carcinoma and a very low dropout risk: implications for the current organ allocation policy. Liver Transpl. 2013;19:1343–53.PubMed Mehta N, Dodge JL, Goel A, Roberts JP, Hirose R, Yao FY. Identification of liver transplant candidates with hepatocellular carcinoma and a very low dropout risk: implications for the current organ allocation policy. Liver Transpl. 2013;19:1343–53.PubMed
41.
go back to reference Cucchetti A, Cescon M, Bigonzi E, et al. Priority of candidates with hepatocellular carcinoma awaiting liver transplantation can be reduced after successful bridge therapy. Liver Transpl. 2011;17:1344–54.PubMed Cucchetti A, Cescon M, Bigonzi E, et al. Priority of candidates with hepatocellular carcinoma awaiting liver transplantation can be reduced after successful bridge therapy. Liver Transpl. 2011;17:1344–54.PubMed
42.
go back to reference • Mehta N, Dodge JL, Hirose R, Roberts JP, Yao FY. Predictors of low risk for dropout from the liver transplant waiting list for hepatocellular carcinoma in long wait time regions: Implications for organ allocation. Am J Transplant. 2019;19:2210–8 Using UNOS data, study identified that individuals with hepatocellular carcinoma listed for liver transplant with native MELD-Na less than 15, Child-Turcotte-Pugh class A cirrhosis, single 2 to 3cm lesion and AFP less than 20ng/mL had lower risk of wait-list dropout and therefore may be a group with minimal transplant benefit.PubMedPubMedCentral • Mehta N, Dodge JL, Hirose R, Roberts JP, Yao FY. Predictors of low risk for dropout from the liver transplant waiting list for hepatocellular carcinoma in long wait time regions: Implications for organ allocation. Am J Transplant. 2019;19:2210–8 Using UNOS data, study identified that individuals with hepatocellular carcinoma listed for liver transplant with native MELD-Na less than 15, Child-Turcotte-Pugh class A cirrhosis, single 2 to 3cm lesion and AFP less than 20ng/mL had lower risk of wait-list dropout and therefore may be a group with minimal transplant benefit.PubMedPubMedCentral
43.
go back to reference Manzini G, Henne-Bruns D, Porzsolt F, Kremer M. Is there a standard for surgical therapy of hepatocellular carcinoma in healthy and cirrhotic liver? A comparison of eight guidelines BMJ Open Gastroenterol. 2017;4:e000129.PubMed Manzini G, Henne-Bruns D, Porzsolt F, Kremer M. Is there a standard for surgical therapy of hepatocellular carcinoma in healthy and cirrhotic liver? A comparison of eight guidelines BMJ Open Gastroenterol. 2017;4:e000129.PubMed
44.
go back to reference Menahem B, Lubrano J, Duvoux C, et al. Liver transplantation versus liver resection for hepatocellular carcinoma in intention to treat: an attempt to perform an ideal meta-analysis. Liver Transpl. 2017;23:836–44.PubMed Menahem B, Lubrano J, Duvoux C, et al. Liver transplantation versus liver resection for hepatocellular carcinoma in intention to treat: an attempt to perform an ideal meta-analysis. Liver Transpl. 2017;23:836–44.PubMed
45.
go back to reference Poon RT, Fan ST, Lo CM, Liu CL, Wong J. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg. 2002;235:373–82.PubMedPubMedCentral Poon RT, Fan ST, Lo CM, Liu CL, Wong J. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg. 2002;235:373–82.PubMedPubMedCentral
46.
go back to reference •• Pinna AD, Yang T, Mazzaferro V, et al. Liver Transplantation and Hepatic Resection can Achieve Cure for Hepatocellular Carcinoma. Ann Surg. 2018;268:868–75 Multi-national study comparing liver transplant and hepatic resction for HCC that also projected changes in overall survival based on varying rates of wait-list drop-out. Found that individuals with a single, less than 3cm, HCC with perserved hepatic function who lived in an area where wait-list drop-out was ~20%, overall survival between hepatic resection and liver transplant were similar.PubMed •• Pinna AD, Yang T, Mazzaferro V, et al. Liver Transplantation and Hepatic Resection can Achieve Cure for Hepatocellular Carcinoma. Ann Surg. 2018;268:868–75 Multi-national study comparing liver transplant and hepatic resction for HCC that also projected changes in overall survival based on varying rates of wait-list drop-out. Found that individuals with a single, less than 3cm, HCC with perserved hepatic function who lived in an area where wait-list drop-out was ~20%, overall survival between hepatic resection and liver transplant were similar.PubMed
48.
go back to reference de Haas RJ, Lim C, Bhangui P, et al. Curative salvage liver transplantation in patients with cirrhosis and hepatocellular carcinoma: an intention-to-treat analysis. Hepatology. 2018;67:204–15.PubMed de Haas RJ, Lim C, Bhangui P, et al. Curative salvage liver transplantation in patients with cirrhosis and hepatocellular carcinoma: an intention-to-treat analysis. Hepatology. 2018;67:204–15.PubMed
49.
go back to reference Bhangui P, Allard MA, Vibert E, et al. Salvage versus primary liver transplantation for early hepatocellular carcinoma: do both strategies yield similar outcomes? Ann Surg. 2016;264:155–63.PubMed Bhangui P, Allard MA, Vibert E, et al. Salvage versus primary liver transplantation for early hepatocellular carcinoma: do both strategies yield similar outcomes? Ann Surg. 2016;264:155–63.PubMed
50.
go back to reference Yadav DK, Chen W, Bai X, et al. Salvage liver transplant versus primary liver transplant for patients with hepatocellular carcinoma. Ann Transplant. 2018;23:524–45.PubMedPubMedCentral Yadav DK, Chen W, Bai X, et al. Salvage liver transplant versus primary liver transplant for patients with hepatocellular carcinoma. Ann Transplant. 2018;23:524–45.PubMedPubMedCentral
51.
go back to reference Lee SY, Konstantinidis IT, Eaton AA, et al. Predicting recurrence patterns after resection of hepatocellular cancer. HPB (Oxford). 2014;16:943–53. Lee SY, Konstantinidis IT, Eaton AA, et al. Predicting recurrence patterns after resection of hepatocellular cancer. HPB (Oxford). 2014;16:943–53.
52.
go back to reference Zheng J, Kuk D, Gonen M, et al. Actual 10-year survivors after resection of hepatocellular carcinoma. Ann Surg Oncol. 2017;24:1358–66.PubMed Zheng J, Kuk D, Gonen M, et al. Actual 10-year survivors after resection of hepatocellular carcinoma. Ann Surg Oncol. 2017;24:1358–66.PubMed
53.
go back to reference Lim KC, Wang VW, Siddiqui FJ, et al. Cost-effectiveness analysis of liver resection versus transplantation for early hepatocellular carcinoma within the Milan criteria. Hepatology. 2015;61:227–37.PubMed Lim KC, Wang VW, Siddiqui FJ, et al. Cost-effectiveness analysis of liver resection versus transplantation for early hepatocellular carcinoma within the Milan criteria. Hepatology. 2015;61:227–37.PubMed
54.
go back to reference Clavien PA, Lesurtel M, Bossuyt PM, et al. Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol. 2012;13:e11–22.PubMed Clavien PA, Lesurtel M, Bossuyt PM, et al. Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol. 2012;13:e11–22.PubMed
55.
go back to reference •• Mazzaferro V, Sposito C, Zhou J, et al. Metroticket 2.0 Model for Analysis of Competing Risks of Death After Liver Transplantation for Hepatocellular Carcinoma. Gastroenterology. 2018;154:128–39 Data driven model called Metroticket 2.0 that predicts competing risks of death after liver transplantation for hepatocellular carcinoma based on AFP and tumor burden parameters.PubMed •• Mazzaferro V, Sposito C, Zhou J, et al. Metroticket 2.0 Model for Analysis of Competing Risks of Death After Liver Transplantation for Hepatocellular Carcinoma. Gastroenterology. 2018;154:128–39 Data driven model called Metroticket 2.0 that predicts competing risks of death after liver transplantation for hepatocellular carcinoma based on AFP and tumor burden parameters.PubMed
56.
go back to reference Mehta N, Heimbach J, Harnois DM, et al. Validation of a risk estimation of tumor recurrence after transplant (RETREAT) score for hepatocellular carcinoma recurrence after liver transplant. JAMA Oncol. 2017;3:493–500.PubMedPubMedCentral Mehta N, Heimbach J, Harnois DM, et al. Validation of a risk estimation of tumor recurrence after transplant (RETREAT) score for hepatocellular carcinoma recurrence after liver transplant. JAMA Oncol. 2017;3:493–500.PubMedPubMedCentral
57.
go back to reference Cillo U, Vitale A, Grigoletto F, et al. Intention-to-treat analysis of liver transplantation in selected, aggressively treated HCC patients exceeding the Milan criteria. Am J Transplant. 2007;7:972–81.PubMed Cillo U, Vitale A, Grigoletto F, et al. Intention-to-treat analysis of liver transplantation in selected, aggressively treated HCC patients exceeding the Milan criteria. Am J Transplant. 2007;7:972–81.PubMed
58.
go back to reference Sapisochin G, Goldaracena N, Laurence JM, et al. The extended Toronto criteria for liver transplantation in patients with hepatocellular carcinoma: a prospective validation study. Hepatology. 2016;64:2077–88.PubMed Sapisochin G, Goldaracena N, Laurence JM, et al. The extended Toronto criteria for liver transplantation in patients with hepatocellular carcinoma: a prospective validation study. Hepatology. 2016;64:2077–88.PubMed
59.
go back to reference Zheng SS, Xu X, Wu J, et al. Liver transplantation for hepatocellular carcinoma: Hangzhou experiences. Transplantation. 2008;85:1726–32.PubMed Zheng SS, Xu X, Wu J, et al. Liver transplantation for hepatocellular carcinoma: Hangzhou experiences. Transplantation. 2008;85:1726–32.PubMed
60.
go back to reference Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl. 2005;11:1086–92.PubMed Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl. 2005;11:1086–92.PubMed
61.
go back to reference Court CM, Harlander-Locke MP, Markovic D, et al. Determination of hepatocellular carcinoma grade by needle biopsy is unreliable for liver transplant candidate selection. Liver Transpl. 2017;23:1123–32.PubMed Court CM, Harlander-Locke MP, Markovic D, et al. Determination of hepatocellular carcinoma grade by needle biopsy is unreliable for liver transplant candidate selection. Liver Transpl. 2017;23:1123–32.PubMed
62.
go back to reference Lee JH, Cho Y, Kim HY, et al. Serum tumor markers provide refined prognostication in selecting liver transplantation candidate for hepatocellular carcinoma patients beyond the Milan criteria. Ann Surg. 2016;263:842–50.PubMed Lee JH, Cho Y, Kim HY, et al. Serum tumor markers provide refined prognostication in selecting liver transplantation candidate for hepatocellular carcinoma patients beyond the Milan criteria. Ann Surg. 2016;263:842–50.PubMed
63.
go back to reference Chaiteerakij R, Zhang X, Addissie BD, et al. Combinations of biomarkers and Milan criteria for predicting hepatocellular carcinoma recurrence after liver transplantation. Liver Transpl. 2015;21:599–606.PubMedPubMedCentral Chaiteerakij R, Zhang X, Addissie BD, et al. Combinations of biomarkers and Milan criteria for predicting hepatocellular carcinoma recurrence after liver transplantation. Liver Transpl. 2015;21:599–606.PubMedPubMedCentral
64.
go back to reference Hsu CC, Chen CL, Wang CC, et al. Combination of FDG-PET and UCSF criteria for predicting HCC recurrence after living donor liver transplantation. Transplantation. 2016;100:1925–32.PubMed Hsu CC, Chen CL, Wang CC, et al. Combination of FDG-PET and UCSF criteria for predicting HCC recurrence after living donor liver transplantation. Transplantation. 2016;100:1925–32.PubMed
65.
go back to reference Lee SD, Lee B, Kim SH, et al. Proposal of new expanded selection criteria using total tumor size and (18)F-fluorodeoxyglucose - positron emission tomography/computed tomography for living donor liver transplantation in patients with hepatocellular carcinoma: the National Cancer Center Korea criteria. World J Transplant. 2016;6:411–22.PubMedPubMedCentral Lee SD, Lee B, Kim SH, et al. Proposal of new expanded selection criteria using total tumor size and (18)F-fluorodeoxyglucose - positron emission tomography/computed tomography for living donor liver transplantation in patients with hepatocellular carcinoma: the National Cancer Center Korea criteria. World J Transplant. 2016;6:411–22.PubMedPubMedCentral
66.
go back to reference Kaido T, Ogawa K, Mori A, et al. Usefulness of the Kyoto criteria as expanded selection criteria for liver transplantation for hepatocellular carcinoma. Surgery. 2013;154:1053–60.PubMed Kaido T, Ogawa K, Mori A, et al. Usefulness of the Kyoto criteria as expanded selection criteria for liver transplantation for hepatocellular carcinoma. Surgery. 2013;154:1053–60.PubMed
67.
go back to reference • Lai Q, Vitale A, Iesari S, et al. Intention-to-treat survival benefit of liver transplantation in patients with hepatocellular cancer. Hepatology. 2017;66:1910–9 European HCC and LT (EurHeCaLT) project showing that in a cohort of over 2,100 individuals with HCC, native MELD score less than or equal to 13 significantly decreased the survival benefit of liver transplantation.PubMed • Lai Q, Vitale A, Iesari S, et al. Intention-to-treat survival benefit of liver transplantation in patients with hepatocellular cancer. Hepatology. 2017;66:1910–9 European HCC and LT (EurHeCaLT) project showing that in a cohort of over 2,100 individuals with HCC, native MELD score less than or equal to 13 significantly decreased the survival benefit of liver transplantation.PubMed
68.
go back to reference Freeman RB, Edwards EB, Harper AM. Waiting list removal rates among patients with chronic and malignant liver diseases. Am J Transplant. 2006;6:1416–21.PubMed Freeman RB, Edwards EB, Harper AM. Waiting list removal rates among patients with chronic and malignant liver diseases. Am J Transplant. 2006;6:1416–21.PubMed
69.
go back to reference Toso C, Dupuis-Lozeron E, Majno P, et al. A model for dropout assessment of candidates with or without hepatocellular carcinoma on a common liver transplant waiting list. Hepatology. 2012;56:149–56.PubMed Toso C, Dupuis-Lozeron E, Majno P, et al. A model for dropout assessment of candidates with or without hepatocellular carcinoma on a common liver transplant waiting list. Hepatology. 2012;56:149–56.PubMed
70.
go back to reference Alver SK, Lorenz DJ, Marvin MR, Brock GN. Projected outcomes of 6-month delay in exception points versus an equivalent model for end-stage liver disease score for hepatocellular carcinoma liver transplant candidates. Liver Transpl. 2016;22:1343–55.PubMed Alver SK, Lorenz DJ, Marvin MR, Brock GN. Projected outcomes of 6-month delay in exception points versus an equivalent model for end-stage liver disease score for hepatocellular carcinoma liver transplant candidates. Liver Transpl. 2016;22:1343–55.PubMed
71.
go back to reference Sasaki K, Firl DJ, Hashimoto K, et al. Development and validation of the HALT-HCC score to predict mortality in liver transplant recipients with hepatocellular carcinoma: a retrospective cohort analysis. Lancet Gastroenterol Hepatol. 2017;2:595–603.PubMed Sasaki K, Firl DJ, Hashimoto K, et al. Development and validation of the HALT-HCC score to predict mortality in liver transplant recipients with hepatocellular carcinoma: a retrospective cohort analysis. Lancet Gastroenterol Hepatol. 2017;2:595–603.PubMed
72.
go back to reference Brondfield MN, Dodge JL, Hirose R, Heimbach J, Yao FY, Mehta N. Unfair advantages for hepatocellular carcinoma patients listed for liver transplant in short-wait regions following 2015 hepatocellular carcinoma policy change. Liver Transpl. 2020;26:662–72.PubMed Brondfield MN, Dodge JL, Hirose R, Heimbach J, Yao FY, Mehta N. Unfair advantages for hepatocellular carcinoma patients listed for liver transplant in short-wait regions following 2015 hepatocellular carcinoma policy change. Liver Transpl. 2020;26:662–72.PubMed
73.
go back to reference Kim DJ, Clark PJ, Heimbach J, et al. Recurrence of hepatocellular carcinoma: importance of mRECIST response to chemoembolization and tumor size. Am J Transplant. 2014;14:1383–90.PubMed Kim DJ, Clark PJ, Heimbach J, et al. Recurrence of hepatocellular carcinoma: importance of mRECIST response to chemoembolization and tumor size. Am J Transplant. 2014;14:1383–90.PubMed
74.
go back to reference Lai Q, Avolio AW, Graziadei I, et al. Alpha-fetoprotein and modified response evaluation criteria in solid tumors progression after locoregional therapy as predictors of hepatocellular cancer recurrence and death after transplantation. Liver Transpl. 2013;19:1108–18.PubMed Lai Q, Avolio AW, Graziadei I, et al. Alpha-fetoprotein and modified response evaluation criteria in solid tumors progression after locoregional therapy as predictors of hepatocellular cancer recurrence and death after transplantation. Liver Transpl. 2013;19:1108–18.PubMed
75.
go back to reference Otto G, Herber S, Heise M, et al. Response to transarterial chemoembolization as a biological selection criterion for liver transplantation in hepatocellular carcinoma. Liver Transpl. 2006;12:1260–7.PubMed Otto G, Herber S, Heise M, et al. Response to transarterial chemoembolization as a biological selection criterion for liver transplantation in hepatocellular carcinoma. Liver Transpl. 2006;12:1260–7.PubMed
76.
go back to reference Millonig G, Graziadei IW, Freund MC, et al. Response to preoperative chemoembolization correlates with outcome after liver transplantation in patients with hepatocellular carcinoma. Liver Transpl. 2007;13:272–9.PubMed Millonig G, Graziadei IW, Freund MC, et al. Response to preoperative chemoembolization correlates with outcome after liver transplantation in patients with hepatocellular carcinoma. Liver Transpl. 2007;13:272–9.PubMed
77.
go back to reference Mehta N, Dodge JL, Grab JD, Yao FY. National experience on down-staging of hepatocellular carcinoma before liver transplant: influence of tumor burden, alpha-fetoprotein, and wait time. Hepatology. 2020;71:943–54.PubMed Mehta N, Dodge JL, Grab JD, Yao FY. National experience on down-staging of hepatocellular carcinoma before liver transplant: influence of tumor burden, alpha-fetoprotein, and wait time. Hepatology. 2020;71:943–54.PubMed
79.
go back to reference Parikh ND, Waljee AK, Singal AG. Downstaging hepatocellular carcinoma: a systematic review and pooled analysis. Liver Transpl. 2015;21:1142–52.PubMed Parikh ND, Waljee AK, Singal AG. Downstaging hepatocellular carcinoma: a systematic review and pooled analysis. Liver Transpl. 2015;21:1142–52.PubMed
80.
go back to reference Sinha J, Mehta N, Dodge JL, Poltavskiy E, Roberts J, Yao F. Are there upper limits in tumor burden for down-staging of hepatocellular carcinoma to liver transplant? Analysis of the all-comers protocol. Hepatology. 2019;70:1185–96.PubMed Sinha J, Mehta N, Dodge JL, Poltavskiy E, Roberts J, Yao F. Are there upper limits in tumor burden for down-staging of hepatocellular carcinoma to liver transplant? Analysis of the all-comers protocol. Hepatology. 2019;70:1185–96.PubMed
81.
go back to reference Murali AR, Romero-Marrero C, Miller C, et al. Predictors of successful downstaging of hepatocellular carcinoma outside Milan criteria. Transplantation. 2016;100:2391–7.PubMed Murali AR, Romero-Marrero C, Miller C, et al. Predictors of successful downstaging of hepatocellular carcinoma outside Milan criteria. Transplantation. 2016;100:2391–7.PubMed
82.
go back to reference Lai Q, Vitale A, Halazun K, et al. Identification of an upper limit of tumor burden for downstaging in candidates with hepatocellular cancer waiting for liver transplantation: a west-east collaborative effort. Cancers (Basel). 2020;12. Lai Q, Vitale A, Halazun K, et al. Identification of an upper limit of tumor burden for downstaging in candidates with hepatocellular cancer waiting for liver transplantation: a west-east collaborative effort. Cancers (Basel). 2020;12.
Metadata
Title
Current Transplant Criteria for Hepatocellular Carcinoma—Overuse or Underuse
Authors
Varun Saxena
Neil Mehta
Publication date
01-12-2020

Other articles of this Issue 4/2020

Current Hepatology Reports 4/2020 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.