Semin Liver Dis 2020; 40(04): 358-364
DOI: 10.1055/s-0040-1709492
Review Article

Evolution of Liver Transplant Selection Criteria and U.S. Allocation Policy for Patients with Hepatocellular Carcinoma

Julie K. Heimbach
1   Department of Transplant Surgery, William J. von Liebig Transplant Center, Mayo Clinic College of Medicine, Rochester, Minnesota
› Author Affiliations

Abstract

Liver transplantation (LT) is an optimal treatment option for early-stage unresectable hepatocellular carcinoma (HCC) in patients with cirrhosis as it provides a treatment for underlying liver disease as well as a decreased incidence of recurrent cancer compared with alternative treatment strategies. A primary barrier to LT for HCC is the critical shortage of available liver allografts. The system of prioritization and access to deceased donor transplantation for patient with HCC in the United States has continued to evolve, while variable approaches including no additional priority, are in use around the world. While the Milan criteria remain the most well-established pretransplantation selection criteria, multiple other algorithms which expand beyond Milan have been proposed. The current review focuses on liver allocation for HCC as well as the principles and varied models available for pretransplant patient selection.



Publication History

Article published online:
17 September 2020

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  • References

  • 1 World Health Organization. Liver fact sheets. Available at: http://gco.iarc.fr/today/data/factsheets/cancers/11-Liver-fact-sheet.pdf . Accessed March 16, 2020
  • 2 White DL, Thrift AP, Kanwal F, Davila J, El-Serag HB. Incidence of hepatocellular carcinoma in all 50 United States, from 2000 through 2012. Gastroenterology 2017; 152 (04) 812-820.e5
  • 3 Singal AG, El-Serag HB. Hepatocellular carcinoma from epidemiology to prevention: translating knowledge into practice. Clin Gastroenterol Hepatol 2015; 13 (12) 2140-2151
  • 4 Yang JD, Larson JJ, Watt KD. et al. Hepatocellular carcinoma is the most common indication for liver transplantation and placement on the waitlist in the United States. Clin Gastroenterol Hepatol 2017; 15 (05) 767-775.e3
  • 5 Iwatsuki S, Starzl TE, Sheahan DG. et al. Hepatic resection versus transplantation for hepatocellular carcinoma. Ann Surg 1991; 214 (03) 221-228 , discussion 228–229
  • 6 Ringe B, Pichlmayr R, Wittekind C, Tusch G. Surgical treatment of hepatocellular carcinoma: experience with liver resection and transplantation in 198 patients. World J Surg 1991; 15 (02) 270-285
  • 7 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 (11) 693-699
  • 8 Llovet JM, Bruix J, Fuster J. et al. Liver transplantation for small hepatocellular carcinoma: the tumor-node-metastasis classification does not have prognostic power. Hepatology 1998; 27 (06) 1572-1577
  • 9 Figueras J, Jaurrieta E, Valls C. et al. Survival after liver transplantation in cirrhotic patients with and without hepatocellular carcinoma: a comparative study. Hepatology 1997; 25 (06) 1485-1489
  • 10 Wiesner RH, McDiarmid SV, Kamath PS. et al. MELD and PELD: application of survival models to liver allocation. Liver Transpl 2001; 7 (07) 567-580
  • 11 Kamath PS, Kim WR. Advanced Liver Disease Study Group. The model for end-stage liver disease (MELD). Hepatology 2007; 45 (03) 797-805
  • 12 Biggins SW, Kim WR, Terrault NA. et al. Evidence-based incorporation of serum sodium concentration into MELD. Gastroenterology 2006; 130 (06) 1652-1660
  • 13 Nagai S, Chau LC, Schilke RE. et al. Effects of allocating livers for transplantation based on model for end-stage liver disease-sodium scores on patient outcomes. Gastroenterology 2018; 155 (05) 1451-1462.e3
  • 14 Wiesner RH, Freeman RB, Mulligan DC. Liver transplantation for hepatocellular cancer: the impact of the MELD allocation policy. Gastroenterology 2004; 127 (05) (Suppl. 01) S261-S267
  • 15 Sharma P, Harper AM, Hernandez JL. et al. Reduced priority MELD score for hepatocellular carcinoma does not adversely impact candidate survival awaiting liver transplantation. Am J Transplant 2006; 6 (08) 1957-1962
  • 16 Freeman RB, Edwards EB, Harper AM. Waiting list removal rates among patients with chronic and malignant liver diseases. Am J Transplant 2006; 6 (06) 1416-1421
  • 17 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 (07) 1643-1648
  • 18 Massie AB, Caffo B, Gentry SE. et al. MELD exceptions and rates of waiting list outcomes. Am J Transplant 2011; 11 (11) 2362-2371
  • 19 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 (01) 285-291
  • 20 Gish RG, Wong RJ, Honerkamp-Smith G, Xu R, Osorio RW. United Network for Organ Sharing regional variations in appeal denial rates with non-standard Model for End-Stage Liver Disease/Pediatric End-Stage Liver Disease exceptions: support for a national review board. Clin Transplant 2015; 29 (06) 513-522
  • 21 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 (05) 1643-1650
  • 22 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 (06) 1957-1962
  • 23 Ishaque T, Massie AB, Bowring MG. et al. Liver transplantation and waitlist mortality for HCC and non-HCC candidates following the 2015 HCC exception policy change. Am J Transplant 2019; 19 (02) 564-572
  • 24 Tschuor C, Ferrarese A, Kuemmerli C, Dutkowski P, Burra P, Clavien PA. Liver Allocation Study Group. Allocation of liver grafts worldwide - is there a best system?. J Hepatol 2019; 71 (04) 707-718
  • 25 Neuberger J, Heimbach JK. Allocation of deceased-donor livers - is there a most appropriate method?. J Hepatol 2019; 71 (04) 654-656
  • 26 European Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu; European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of hepatocellular carcinoma. J Hepatol 2018; 69 (01) 182-236
  • 27 Notarpaolo A, Layese R, Magistri P. et al. Validation of the AFP model as a predictor of HCC recurrence in patients with viral hepatitis-related cirrhosis who had received a liver transplant for HCC. J Hepatol 2017; 66 (03) 552-559
  • 28 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 (06) 1394-1403
  • 29 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 (11) 2587-2596
  • 30 Yao FY, Hirose R, LaBerge JM. et al. A prospective study on downstaging of hepatocellular carcinoma prior to liver transplantation. Liver Transpl 2005; 11 (12) 1505-1514
  • 31 Mazzaferro V, Llovet JM, Miceli R. et al; Metroticket Investigator Study Group. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 2009; 10 (01) 35-43
  • 32 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 (01) 128-139
  • 33 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 (06) 2077-2088
  • 34 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 (01) 158-165
  • 35 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 (05) 1053-1060
  • 36 Bertsimas D, Kung J, Trichakis N, Wang Y, Hirose R, Vagefi PA. Development and validation of an optimized prediction of mortality for candidates awaiting liver transplantation. Am J Transplant 2019; 19 (04) 1109-1118
  • 37 Santopaolo F, Lenci I, Milana M, Manzia TM, Baiocchi L. Liver transplantation for hepatocellular carcinoma: Where do we stand?. World J Gastroenterol 2019; 25 (21) 2591-2602