Hepatocellular carcinoma recurrence after liver transplantation: risk factors, targeted surveillance and management options

Filippo Pelizzaro , Alberto Ferrarese , Martina Gambato , Alberto Zanetto , Francesco Paolo Russo , Giacomo Germani , Marco Senzolo , Mario Domenico Rizzato , Caterina Soldà , Alessandro Vitale , Enrico Gringeri , Umberto Cillo , Patrizia Burra

Hepatoma Research ›› 2024, Vol. 10 : 44

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Hepatoma Research ›› 2024, Vol. 10:44 DOI: 10.20517/2394-5079.2024.107
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Hepatocellular carcinoma recurrence after liver transplantation: risk factors, targeted surveillance and management options

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Abstract

Hepatocellular carcinoma (HCC) represents a well-recognized indication for liver transplantation (LT), with improving graft and patient survival rates due to medical and surgical advancements over time. Despite the implementation of selection criteria to ensure the highest transplant benefit, post-LT recurrence of HCC is not uncommon and is often associated with poor outcomes. Therefore, a post-transplant surveillance strategy appears to be a cost-effective approach, particularly in the early post-surgery period when the recurrence rate is high. Although specific guidelines are still lacking, emerging strategies tailored to pre-transplant tumor history and explant pathology show promise. Moreover, new immunosuppressive therapy schemes and aggressive management of post-transplant medical complications can be implemented to reduce the risk of cancer recurrence. Finally, multimodal oncological strategies are increasingly used to improve survival even after cancer recurrence. This paper reviews the evidence on HCC recurrence after LT, providing insights into risk factors, targeted surveillance, and management strategies.

Keywords

Liver transplantation / liver cancer / tumor recurrence / surveillance

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Filippo Pelizzaro, Alberto Ferrarese, Martina Gambato, Alberto Zanetto, Francesco Paolo Russo, Giacomo Germani, Marco Senzolo, Mario Domenico Rizzato, Caterina Soldà, Alessandro Vitale, Enrico Gringeri, Umberto Cillo, Patrizia Burra. Hepatocellular carcinoma recurrence after liver transplantation: risk factors, targeted surveillance and management options. Hepatoma Research, 2024, 10: 44 DOI:10.20517/2394-5079.2024.107

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References

[1]

Ivanics T,De Martin E.Changing trends in liver transplantation: challenges and solutions.Transplantation2021;105:743-56

[2]

Mazzaferro V,Doci R.Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis.N Engl J Med1996;334:693-9

[3]

Mehta N,Yao FY.Liver transplantation for hepatocellular carcinoma. working group report from the ILTS transplant oncology consensus conference.Transplantation2020;104:1136-42

[4]

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;71:707-18.

[5]

Vitale A,Pawlik TM.The concept of therapeutic hierarchy for patients with hepatocellular carcinoma: a multicenter cohort study.Liver Int2019;39:1478-89

[6]

de'Angelis N,Carra MC.Managements of recurrent hepatocellular carcinoma after liver transplantation: a systematic review.World J Gastroenterol2015;21:11185-98 PMCID:PMC4607916

[7]

Bzeizi KI,Vidyasagar K,Broering D.Hepatocellular carcinoma recurrence and mortality rate post liver transplantation: meta-analysis and systematic review of real-world evidence.Cancers (Basel)2022;14:5114 PMCID:PMC9599880

[8]

Al-Ameri A,Zheng S.Predictors of post-recurrence survival in hepatocellular carcinoma patients following liver transplantation: systematic review and meta-analysis.Transplant Rev (Orlando)2022;36:100676

[9]

Mazzaferro V,Sposito C.Milan criteria in liver transplantation for hepatocellular carcinoma: an evidence-based analysis of 15 years of experience.Liver Transpl2011;17 Suppl 2:S44-57

[10]

Escartin A,Bilbao I.Recurrence of hepatocellular carcinoma after liver transplantation.Transplant Proc2007;39:2308-10

[11]

Plessier A,Consigny Y.Underestimation of the influence of satellite nodules as a risk factor for post-transplantation recurrence in patients with small hepatocellular carcinoma.Liver Transpl2004;10:S86-90

[12]

Valdivieso A,Gastaca M.Management of hepatocellular carcinoma recurrence after liver transplantation.Transplant Proc2010;42:660-2

[13]

Sharma P,Hussain H.Incidence and risk factors of hepatocellular carcinoma recurrence after liver transplantation in the MELD era.Dig Dis Sci2012;57:806-12 PMCID:PMC3288660

[14]

Maccali C,Boin I.Recurrence of hepatocellular carcinoma after liver transplantation: prognostic and predictive factors of survival in a Latin American cohort.Liver Int2021;41:851-62

[15]

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;10:35-43.

[16]

Bodzin AS,Markovic D,Busuttil RW.Predicting mortality in patients developing recurrent hepatocellular carcinoma after liver transplantation: impact of treatment modality and recurrence characteristics.Ann Surg2017;266:118-25

[17]

Pelizzaro F,Gringeri E.Management of hepatocellular carcinoma recurrence after liver transplantation.Cancers (Basel)2021;13:4882 PMCID:PMC8508053

[18]

Ekpanyapong S,Loza BL.Predictors, presentation, and treatment outcomes of recurrent hepatocellular carcinoma after liver transplantation: a large single center experience.J Clin Exp Hepatol2020;10:304-15 PMCID:PMC7335705

[19]

Agopian VG,Zarrinpar A.A novel prognostic nomogram accurately predicts hepatocellular carcinoma recurrence after liver transplantation: analysis of 865 consecutive liver transplant recipients.J Am Coll Surg2015;220:416-27

[20]

Sapisochin G,Astete S.Benefit of treating hepatocellular carcinoma recurrence after liver transplantation and analysis of prognostic factors for survival in a large Euro-American series.Ann Surg Oncol2015;22:2286-94

[21]

Invernizzi F,Zavaglia C.Experience with early sorafenib treatment with mTOR inhibitors in hepatocellular carcinoma recurring after liver transplantation.Transplantation2020;104:568-74

[22]

Guerrini GP,Tarantino G.Multimodal oncological approach in patients affected by recurrent hepatocellular carcinoma after liver transplantation.Eur Rev Med Pharmacol Sci2017;21:3421-35

[23]

Cillo U,Polacco M.Liver transplantation for hepatocellular carcinoma through the lens of transplant benefit.Hepatology2017;65:1741-8

[24]

Yao FY,Bass NM.Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival.Hepatology2001;33:1394-403

[25]

Yao FY,Bass NM,Ascher NL.Liver transplantation for hepatocellular carcinoma: validation of the UCSF-expanded criteria based on preoperative imaging.Am J Transplant2007;7:2587-96

[26]

Cillo U,Bassanello M.Liver transplantation for the treatment of moderately or well-differentiated hepatocellular carcinoma.Ann Surg2004;239:150-9 PMCID:PMC1356206

[27]

Cillo U,Grigoletto F.Intention-to-treat analysis of liver transplantation in selected, aggressively treated HCC patients exceeding the Milan criteria.Am J Transplant2007;7:972-81

[28]

Yang SH,Lee HW.A revised scoring system utilizing serum alphafetoprotein levels to expand candidates for living donor transplantation in hepatocellular carcinoma.Surgery2007;141:598-609

[29]

Kwon CH,Han YS.HCC in living donor liver transplantation: can we expand the Milan criteria?.Dig Dis2007;25:313-9

[30]

Duvoux C, Roudot-Thoraval F, Decaens T, et al; Liver Transplantation French Study Group. Liver transplantation for hepatocellular carcinoma: a model including α-fetoprotein improves the performance of Milan criteria. Gastroenterology 2012;143:986-94.e3.

[31]

Lai Q,Manzia TM.Combination of biological and morphological parameters for the selection of patients with hepatocellular carcinoma waiting for liver transplantation.Clin Transplant2012;26:E125-31

[32]

Toso C,Hernandez-Alejandro R.Total tumor volume and alpha-fetoprotein for selection of transplant candidates with hepatocellular carcinoma: a prospective validation.Hepatology2015;62:158-65

[33]

Lai Q,Inostroza Nunez M.A novel prognostic index in patients with hepatocellular cancer waiting for liver transplantation: time-radiological-response-alpha-fetoprotein-INflammation (TRAIN) score.Ann Surg2016;264:787-96

[34]

Sapisochin G,Laurence JM.The extended toronto criteria for liver transplantation in patients with hepatocellular carcinoma: a prospective validation study.Hepatology2016;64:2077-88

[35]

Halazun KJ,Abdelmessih RM.Recurrence after liver transplantation for hepatocellular carcinoma: a new MORAL to the story.Ann Surg2017;265:557-64

[36]

Lai Q, Vitale A, Iesari S, et al; European Hepatocellular Cancer Liver Transplant Study Group. Intention-to-treat survival benefit of liver transplantation in patients with hepatocellular cancer. Hepatology 2017;66:1910-9.

[37]

Sasaki K,Hashimoto K.Development and validation of the HALT-HCC score to predict mortality in liver transplant recipients with hepatocellular carcinoma: a retrospective cohort analysis.Lancet Gastroenterol Hepatol2017;2:595-603

[38]

Halazun KJ,Najjar M.Is it time to abandon the milan criteria?.Ann Surg2018;268:690-9

[39]

Mazzaferro V,Zhou J.Metroticket 2.0 model for analysis of competing risks of death after liver transplantation for hepatocellular carcinoma.Gastroenterology2018;154:128-39

[40]

Parfitt JR,Alghamdi M.Recurrent hepatocellular carcinoma after transplantation: use of a pathological score on explanted livers to predict recurrence.Liver Transpl2007;13:543-51

[41]

Aziz S,Marotta P.Recurrent hepatocellular carcinoma after liver transplantation: validation of a pathologic risk score on explanted livers to predict recurrence.Transplant Proc2021;53:1975-9.

[42]

Cullaro G,Mehta N,Verna EC.Sex-based disparities in hepatocellular carcinoma recurrence after liver transplantation.Transplantation2021;105:2420-6 PMCID:PMC8200371

[43]

Orci LA,Fink M.Predicting recurrence of hepatocellular carcinoma after liver transplantation using a novel model that incorporates tumor and donor-related factors.Transpl Int2021;34:2875-86

[44]

Ferrarese A,Orrù G.Machine learning in liver transplantation: a tool for some unsolved questions?.Transpl Int2021;34:398-411

[45]

Marsh JW,Demetris AJ.Genotyping of hepatocellular carcinoma in liver transplant recipients adds predictive power for determining recurrence-free survival.Liver Transpl2003;9:664-71

[46]

Rodriguez-Luna H,Byrne T.Artificial neural network and tissue genotyping of hepatocellular carcinoma in liver-transplant recipients: prediction of recurrence.Transplantation2005;79:1737-40

[47]

Jonas S,Steinmüller T.Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis.Hepatology2001;33:1080-6

[48]

Lozanovski VJ,Aminizadeh E.Prognostic role of selection criteria for liver transplantation in patients with hepatocellular carcinoma: a network meta-analysis.BJS Open2022;6 PMCID:PMC8874238

[49]

Pommergaard HC, Rostved AA, Adam R, et al; European Liver and Intestine Transplant Association (ELITA). Vascular invasion and survival after liver transplantation for hepatocellular carcinoma: a study from the European liver transplant registry. HPB (Oxford) 2018;20:768-75.

[50]

Yao FY,Flemming J.Downstaging of hepatocellular cancer before liver transplant: long-term outcome compared to tumors within Milan criteria.Hepatology2015;61:1968-77 PMCID:PMC4809192

[51]

Tabrizian P,Mehta N.Ten-year outcomes of liver transplant and downstaging for hepatocellular carcinoma.JAMA Surg2022;157:779-88 PMCID:PMC9301590

[52]

Mazzaferro V,Bhoori S.Liver transplantation in hepatocellular carcinoma after tumour downstaging (XXL): a randomised, controlled, phase 2b/3 trial.Lancet Oncol2020;21:947-56

[53]

Otto G,Heise M.Response to transarterial chemoembolization as a biological selection criterion for liver transplantation in hepatocellular carcinoma.Liver Transpl2006;12:1260-7

[54]

Millonig G,Freund MC.Response to preoperative chemoembolization correlates with outcome after liver transplantation in patients with hepatocellular carcinoma.Liver Transpl2007;13:272-9

[55]

Lai Q, Avolio AW, Graziadei I, et al; European Hepatocellular Cancer Liver Transplant Study Group. 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.

[56]

Biolato M,Marrone G,Grieco A.Upper limits of downstaging for hepatocellular carcinoma in liver transplantation.Cancers (Basel)2021;13:6337 PMCID:PMC8699392

[57]

Cillo U,Volk ML.The survival benefit of liver transplantation in hepatocellular carcinoma patients.Dig Liver Dis2010;42:642-9

[58]

Giannini EG, Aglitti A, Borzio M, et al; Associazione Italiana per lo Studio del Fegato (AISF) HCC Special Interest Group. Overview of immune checkpoint inhibitors therapy for hepatocellular carcinoma, and the ITA.LI.CA cohort derived estimate of amenability rate to immune checkpoint inhibitors in clinical practice. Cancers (Basel) 2019;11:1689. PMCID:PMC6896125

[59]

Harper AM,Washburn WK.An early look at the organ procurement and transplantation network explant pathology form data.Liver Transpl2016;22:757-64

[60]

Llovet JM,Mazzaferro V.Resection and liver transplantation for hepatocellular carcinoma.Semin Liver Dis2005;25:181-200

[61]

Schwartz ME.Liver transplantation for hepatocellular carcinoma: the best treatment, but for which patient?.Hepatology1996;24:1539-41

[62]

Shetty K,Brensinger C.Liver transplantation for hepatocellular carcinoma validation of present selection criteria in predicting outcome.Liver Transpl2004;10:911-8

[63]

Freeman RB,Ruthazer R.Optimizing staging for hepatocellular carcinoma before liver transplantation: a retrospective analysis of the UNOS/OPTN database.Liver Transpl2006;12:1504-11

[64]

Mehta N,Roberts JP,Yao FY.Misdiagnosis of hepatocellular carcinoma in patients receiving no local-regional therapy prior to liver transplant: an analysis of the organ procurement and transplantation network explant pathology form.Clin Transplant2017;31 PMCID:PMC5937711

[65]

Mehta N,Harnois DM.Validation of a risk estimation of tumor recurrence after transplant (RETREAT) score for hepatocellular carcinoma recurrence after liver transplant.JAMA Oncol2017;3:493-500 PMCID:PMC5395317

[66]

Mehta N,Roberts JP.Validation of the prognostic power of the RETREAT score for hepatocellular carcinoma recurrence using the UNOS database.Am J Transplant2018;18:1206-13 PMCID:PMC6445634

[67]

Berry K.Serum alpha-fetoprotein level independently predicts posttransplant survival in patients with hepatocellular carcinoma.Liver Transpl2013;19:634-45

[68]

Levi DM,Martin P.Liver transplantation for hepatocellular carcinoma in the model for end-stage liver disease era.J Am Coll Surg2010;210:727-34, 735

[69]

Grąt M,Patkowski W.Relevance of pre-transplant α-fetoprotein dynamics in liver transplantation for hepatocellular cancer.Ann Transplant2016;21:115-24

[70]

Hong G,Suh SW.Alpha-fetoprotein and (18)F-FDG positron emission tomography predict tumor recurrence better than Milan criteria in living donor liver transplantation.J Hepatol2016;64:852-9

[71]

Toso C,Bigam DL,Kneteman NM.Reassessing selection criteria prior to liver transplantation for hepatocellular carcinoma utilizing the scientific registry of transplant recipients database.Hepatology2009;49:832-8

[72]

Ravaioli M,Piscaglia F.Liver transplantation for hepatocellular carcinoma: results of down-staging in patients initially outside the Milan selection criteria.Am J Transplant2008;8:2547-57

[73]

Hameed B,Sapisochin G,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 Transpl2014;20:945-51 PMCID:PMC4807739

[74]

Decaens T,Badran H.Impact of tumour differentiation to select patients before liver transplantation for hepatocellular carcinoma.Liver Int2011;31:792-801

[75]

Costentin C, Piñero F, Degroote H, et al; French-Italian-Belgium and Latin American collaborative group for HCC and liver transplantation. R3-AFP score is a new composite tool to refine prediction of hepatocellular carcinoma recurrence after liver transplantation. JHEP Rep 2022;4:100445. PMCID:PMC8961219

[76]

Tran BV,Markovic D.Development and validation of a REcurrent Liver cAncer Prediction ScorE (RELAPSE) following liver transplantation in patients with hepatocellular carcinoma: analysis of the US multicenter HCC transplant consortium.Liver Transpl2023;29:683-97

[77]

Halazun KJ,Rana AA.Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma.Ann Surg2009;250:141-51

[78]

Chaiteerakij R,Addissie BD.Combinations of biomarkers and Milan criteria for predicting hepatocellular carcinoma recurrence after liver transplantation.Liver Transpl2015;21:599-606 PMCID:PMC4490162

[79]

Norman JS,Kotwani P,Yao F.AFP-L3 and DCP strongly predict early hepatocellular carcinoma recurrence after liver transplantation.J Hepatol2023;79:1469-77 PMCID:PMC10998694

[80]

Welling TH,Carrier K.Multicenter study of staging and therapeutic predictors of hepatocellular carcinoma recurrence following transplantation.Liver Transpl2018;24:1233-42 PMCID:PMC6153067

[81]

Pawlik TM,Vauthey JN.Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma.Liver Transpl2005;11:1086-92

[82]

Gouw AS,Kusano H,Ichida T.Markers for microvascular invasion in hepatocellular carcinoma: where do we stand?.Liver Transpl2011;17 Suppl 2:S72-80

[83]

Kornberg A,Bärthel E.18F-FDG-uptake of hepatocellular carcinoma on PET predicts microvascular tumor invasion in liver transplant patients.Am J Transplant2009;9:592-600

[84]

Verna EC,Aggarwal A.Liver transplantation for hepatocellular carcinoma: management after the transplant.Am J Transplant2020;20:333-47

[85]

Pawlik TM,Anders RA,Maley W.Preoperative assessment of hepatocellular carcinoma tumor grade using needle biopsy: implications for transplant eligibility.Ann Surg2007;245:435-42 PMCID:PMC1877015

[86]

Young RS,Hakeem AR.Pre-liver transplant biopsy in hepatocellular carcinoma: a potential criterion for exclusion from transplantation?.HPB (Oxford)2013;15:418-27 PMCID:PMC3664045

[87]

Kornberg A,Tannapfel A.Long-term survival after recurrent hepatocellular carcinoma in liver transplant patients: clinical patterns and outcome variables.Eur J Surg Oncol2010;36:275-80

[88]

Fernandez-Sevilla E,Selten J.Recurrence of hepatocellular carcinoma after liver transplantation: is there a place for resection?.Liver Transpl2017;23:440-7

[89]

Kneuertz PJ,Cameron AM.Multidisciplinary management of recurrent hepatocellular carcinoma following liver transplantation.J Gastrointest Surg2012;16:874-81 PMCID:PMC3541014

[90]

Alshahrani AA,Hwang S.Clinical features and surveillance of very late hepatocellular carcinoma recurrence after liver transplantation.Ann Transplant2018;23:659-65 PMCID:PMC6255332

[91]

Cescon M,Grazi GL.Prognostic factors for tumor recurrence after a 12-year, single-center experience of liver transplantations in patients with hepatocellular carcinoma.J Transplant2010;2010:1-8 PMCID:PMC2938428

[92]

Lee DD,Mehta N.Surveillance for HCC after liver transplantation: increased monitoring may yield aggressive treatment options and improved postrecurrence survival.Transplantation2020;104:2105-12

[93]

European Association for the Study of the Liver. EASL clinical practice guidelines: liver transplantation.J Hepatol2016;64:433-85

[94]

Lucey MR,Ojo L.Long-term management of the successful adult liver transplant: 2012 practice guideline by the American association for the study of liver diseases and the american society of transplantation.Liver Transpl2013;19:3-26

[95]

Berenguer M,Ghobrial M.Posttransplant management of recipients undergoing liver transplantation for hepatocellular carcinoma. Working group report from the Ilts transplant oncology consensus conference.Transplantation2020;104:1143-9

[96]

Aggarwal A,Verna EC.A national survey of hepatocellular carcinoma surveillance practices following liver transplantation.Transplant Direct2021;7:e638 PMCID:PMC7725259

[97]

Notarpaolo A,Magistri P.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 Hepatol2017;66:552-9

[98]

Nörthen A,Walson PD.Diagnostic value of alpha-1-fetoprotein (AFP) as a biomarker for hepatocellular carcinoma recurrence after liver transplantation.Clin Biochem2018;52:20-5

[99]

Liu D,Fong DY,Khong PL.Evidence-based surveillance imaging schedule after liver transplantation for hepatocellular carcinoma recurrence.Transplantation2017;101:107-11

[100]

Hoffman D.Recurrence of hepatocellular carcinoma following liver transplantation.Expert Rev Gastroenterol Hepatol2021;15:91-102

[101]

Åberg F,Schult A,Rizell M.The RETREAT score provides valid predictions regarding hepatocellular carcinoma recurrence after liver transplantation.Transpl Int2021;34:2869-74

[102]

Reddy SHS,Dodge JL.Liver transplantation for HCC: validation of prognostic power of the RETREAT score for recurrence in a UK cohort.HPB (Oxford)2022;24:596-605

[103]

Ivanics T,Patel MS.The toronto postliver transplantation hepatocellular carcinoma recurrence calculator: a machine learning approach.Liver Transpl2022;28:593-602

[104]

Liu S,Singhi A.Transcriptome and exome analyses of hepatocellular carcinoma reveal patterns to predict cancer recurrence in liver transplant patients.Hepatol Commun2022;6:710-27 PMCID:PMC8948579

[105]

Lai Q, De Stefano C, Emond J, et al; EurHeCaLT and the West-East LT Study Group. Development and validation of an artificial intelligence model for predicting post-transplant hepatocellular cancer recurrence. Cancer Commun (Lond) 2023;43:1381-5. PMCID:PMC10693300

[106]

Liu Z,Zhang W.Deep learning for prediction of hepatocellular carcinoma recurrence after resection or liver transplantation: a discovery and validation study.Hepatol Int2022;16:577-89 PMCID:PMC9174321

[107]

Hojo M,Maluccio M.Cyclosporine induces cancer progression by a cell-autonomous mechanism.Nature1999;397:530-4

[108]

Maluccio M,Lagman M.Tacrolimus enhances transforming growth factor-beta1 expression and promotes tumor progression.Transplantation2003;76:597-602

[109]

Yokoyama I,Saitsu H,Starzl TE.Accelerated growth rates of recurrent hepatocellular carcinoma after liver transplantation.Cancer1991;68:2095-100

[110]

Rodríguez-Perálvarez M,Naveas MC.Reduced exposure to calcineurin inhibitors early after liver transplantation prevents recurrence of hepatocellular carcinoma.J Hepatol2013;59:1193-9

[111]

Vivarelli M,Piscaglia F.Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression.Liver Transpl2005;11:497-503

[112]

Vivarelli M,La Barba G.Liver transplantation for hepatocellular carcinoma under calcineurin inhibitors: reassessment of risk factors for tumor recurrence.Ann Surg2008;248:857-62

[113]

Rodríguez-Perálvarez M, Colmenero J, González A, et al; Chronic immunosuppression, cancer Spanish consortium. Cumulative exposure to tacrolimus and incidence of cancer after liver transplantation. Cancer Commun (Lond) 2022;22:1671-82. PMCID:PMC9315045

[114]

Zhou J,Wu ZQ.Sirolimus-based immunosuppression therapy in liver transplantation for patients with hepatocellular carcinoma exceeding the Milan criteria.Transplant Proc2008;40:3548-53

[115]

Kneteman NM,Al Saghier M.Sirolimus-based immunosuppression for liver transplantation in the presence of extended criteria for hepatocellular carcinoma.Liver Transpl2004;10:1301-11

[116]

Zimmerman MA,Wachs M.Sirolimus-based immunosuppression following liver transplantation for hepatocellular carcinoma.Liver Transpl2008;14:633-8

[117]

Toso C,Bigam DL,Kneteman NM.Sirolimus-based immunosuppression is associated with increased survival after liver transplantation for hepatocellular carcinoma.Hepatology2010;51:1237-43

[118]

Yanik EL,Gustafson SK.Effects of maintenance immunosuppression with sirolimus after liver transplant for hepatocellular carcinoma.Liver Transpl2016;22:627-34 PMCID:PMC4846564

[119]

Menon KV,Heaton ND.Meta-analysis: recurrence and survival following the use of sirolimus in liver transplantation for hepatocellular carcinoma.Aliment Pharmacol Ther2013;37:411-9

[120]

Liang W,Ling X.Sirolimus-based immunosuppression in liver transplantation for hepatocellular carcinoma: a meta-analysis.Liver Transpl2012;18:62-9

[121]

Cholongitas E,Rodríguez-Castro KI.Mammalian target of rapamycin inhibitors are associated with lower rates of hepatocellular carcinoma recurrence after liver transplantation: a systematic review.Transpl Int2014;27:1039-49

[122]

Grigg SE,Gow PJ.Systematic review with meta-analysis: sirolimus- or everolimus-based immunosuppression following liver transplantation for hepatocellular carcinoma.Aliment Pharmacol Ther2019;49:1260-73

[123]

Yan X,Yang Y.Sirolimus or everolimus improves survival after liver transplantation for hepatocellular carcinoma: a systematic review and meta-analysis.Liver Transpl2022;28:1063-77

[124]

Geissler EK,Zülke C.Sirolimus use in liver transplant recipients with hepatocellular carcinoma: a randomized, multicenter, open-label phase 3 trial.Transplantation2016;100:116-25 PMCID:PMC4683033

[125]

Schnitzbauer AA,Adam R.mTOR inhibition is most beneficial after liver transplantation for hepatocellular carcinoma in patients with active tumors.Ann Surg2020;272:855-62

[126]

Rodríguez-Perálvarez M,Barrera L.Impact of early initiated everolimus on the recurrence of hepatocellular carcinoma after liver transplantation.Transplantation2018;102:2056-64

[127]

Kang I,Choi SH.Impact of everolimus on survival after liver transplantation for hepatocellular carcinoma.Clin Mol Hepatol2021;27:589-602. PMCID:PMC8524068

[128]

De Simone P,Lai Q.Everolimus mitigates the risk of hepatocellular carcinoma recurrence after liver transplantation.Cancers (Basel)2024;16:1243 PMCID:PMC11010831

[129]

Lee SG,Saliba F.Efficacy and safety of everolimus with reduced tacrolimus in liver transplant recipients: 24-month results from the pooled analysis of 2 randomized controlled trials.Transplantation2021;105:1564-75 PMCID:PMC8221719

[130]

Safety and efficacy of everolimus treatment in liver transplantation for liver cancer. Available from: https://clinicaltrials.gov/study/NCT02081755?cond=transplantation%20for%20liver%20cancer&intr=everolimus&rank=1. [Last accessed on 25 Oct 2024].

[131]

Cholongitas E,Vourli G.Safety and efficacy of everolimus initiation from the first month after liver transplantation: a systematic review and meta-analysis.Clin Transplant2023;37:e14957

[132]

Charlton M,Aqel B.International liver transplantation society consensus statement on immunosuppression in liver transplant recipients.Transplantation2018;102:727-43

[133]

De Simone P, Fagiuoli S, Cescon M, et al; Consensus Panel. Use of everolimus in liver transplantation: recommendations from a working group. Transplantation 2017;101:239-51. PMCID:PMC5265697

[134]

Cillo U, Carraro A, Avolio AW, et al; Italian Board of Experts in Liver Transplantation (I-BELT). Immunosuppression in liver transplant oncology: position paper of the Italian Board of Experts in Liver Transplantation (I-BELT). Updates Surg 2024;76:725-41.

[135]

Siegel AB,Finn RS.Phase I trial of sorafenib following liver transplantation in patients with high-risk hepatocellular carcinoma.Liver Cancer2015;4:115-25 PMCID:PMC4439789

[136]

Satapathy SK,Kocak M.No apparent benefit of preemptive sorafenib therapy in liver transplant recipients with advanced hepatocellular carcinoma on explant.Clin Transplant2018;32:e13246

[137]

Bruix J, Takayama T, Mazzaferro V, et al; STORM investigators. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol 2015;16:1344-54.

[138]

Lin HS,Gao LH,Shan RF.Adjuvant chemotherapy after liver transplantation for hepatocellular carcinoma: a systematic review and a meta-analysis.Hepatobiliary Pancreat Dis Int2015;14:236-45

[139]

Guo DZ,Yan JY.Efficacy and safety of lenvatinib for preventing tumor recurrence after liver transplantation in hepatocellular carcinoma beyond the Milan criteria.Ann Transl Med2022;10:1091 PMCID:PMC9652551

[140]

Deng Y,Chen Y.Development of a risk classifier to predict tumor recurrence and lenvatinib benefits in hepatocellular carcinoma after liver transplantation.Transplant Proc2023;55:153-63

[141]

Han B,Zhao S.Potential role of adjuvant lenvatinib in improving disease-free survival for patients with high-risk hepatitis b virus-related hepatocellular carcinoma following liver transplantation: a retrospective, case control study.Front Oncol2020;10:562103 PMCID:PMC7750628

[142]

Qin S, Chen M, Cheng AL, et al; IMbrave050 investigators. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial. Lancet 2023;402:1835-47.

[143]

Pinter M,Peck-Radosavljevic M.Immunotherapy for advanced hepatocellular carcinoma: a focus on special subgroups.Gut2021;70:204-14 PMCID:PMC7788203

[144]

Yang Z,Tian XY.Impact of treatment modalities on patients with recurrent hepatocellular carcinoma after liver transplantation: preliminary experience.Hepatobiliary Pancreat Dis Int2020;19:365-70

[145]

Huang J,Wu H,Liao M.Is radiofrequency ablation applicable for recurrent hepatocellular carcinoma after liver transplantation?.J Surg Res2016;200:122-30

[146]

Jeong YH,Lee GD.Surgical outcome of pulmonary metastasectomy for hepatocellular carcinoma recurrence in liver transplant patients.Ann Transplant2021;26:e930383 PMCID:PMC8122851

[147]

Sposito C,Germini A.Comparative efficacy of sorafenib versus best supportive care in recurrent hepatocellular carcinoma after liver transplantation: a case-control study.J Hepatol2013;59:59-66

[148]

Li BCW,Shing K.The outcomes of systemic treatment in recurrent hepatocellular carcinomas following liver transplants.Adv Ther2021;38:3900-10

[149]

Bang K,Yoo C.Efficacy and safety of lenvatinib in patients with recurrent hepatocellular carcinoma after liver transplantation.Cancer Med2023;12:2572-9 PMCID:PMC9939097

[150]

Iavarone M,Czauderna C.Preliminary experience on safety of regorafenib after sorafenib failure in recurrent hepatocellular carcinoma after liver transplantation.Am J Transplant2019;19:3176-84

[151]

Rezaee-Zavareh MS,Wang T.Impact of pre-transplant immune checkpoint inhibitor use on post-transplant outcomes in HCC: a systematic review and individual patient data meta-analysis.J Hepatol2024;Online ahead of print.

[152]

Di Marco L,Foschi FG.Feasibility, safety, and outcome of second-line nivolumab/bevacizumab in liver transplant patients with recurrent hepatocellular carcinoma.Liver Transpl2023;29:559-63 PMCID:PMC10106106

[153]

Tabrizian P,Schwartz M.Immunotherapy and transplantation for hepatocellular carcinoma.J Hepatol2024;80:822-5

[154]

Tan AT,Lee Krishnamoorthy T.Use of expression profiles of HBV-DNA integrated into genomes of hepatocellular carcinoma cells to select T cells for immunotherapy.Gastroenterology2019;156:1862-1876.e9

[155]

Hafezi M,Chia A.Immunosuppressive drug-resistant armored T-Cell receptor T cells for immune therapy of HCC in liver transplant patients.Hepatology2021;74:200-13

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