Meta-Analysis

. 2025 Jan;82(1):107-119.

doi: 10.1016/j.jhep.2024.06.042. Epub 2024 Jul 10.

Impact of pre-transplant immune checkpoint inhibitor use on post-transplant outcomes in HCC: A systematic review and individual patient data meta-analysis

Mohammad Saeid Rezaee-Zavareh¹, Yee Hui Yeo², Tielong Wang³, Zhiyong Guo³, Parissa Tabrizian⁴, Stephen C Ward⁵, Fatma Barakat⁶, Tarek I Hassanein⁶, Shravan Dave⁷, Veeral Ajmera⁷, Sherrie Bhoori⁸, Vincenzo Mazzaferro⁹, David M H Chascsa¹⁰, Margaret C Liu¹¹, Elizabeth S Aby¹², John R Lake¹², Miguel Sogbe¹³, Bruno Sangro¹³, Maen Abdelrahim¹⁴, Abdullah Esmail¹⁵, Andreas Schmiderer¹⁶, Yasmina Chouik¹⁷, Mark Rudolph¹⁸, Davendra Sohal¹⁸, Heloise Giudicelli¹⁹, Manon Allaire²⁰, Mehmet Akce²¹, Jessica Guadagno²², Clara Y Tow²³, Hatef Massoumi²⁴, Paolo De Simone²⁵, Elise Kang²⁶, Robyn D Gartrell²⁷, Mercedes Martinez²⁸, Ricardo Paz-Fumagalli²⁹, Beau B Toskich³⁰, Nguyen H Tran³¹, Gabriela Azevedo Solino³², Dra Mariana Poltronieri Pacheco³³, Richard S Kalman³⁴, Vatche G Agopian³⁵, Neil Mehta³⁶, Neehar D Parikh³⁷, Amit G Singal³⁸, Ju Dong Yang³⁹

Affiliations

¹ Middle East Liver Diseases Center, Tehran 1417935840, Iran.
² Karsh Division of Gastroenterology and Hepatology, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA.
³ Organ Transplant Center, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China; Guangdong Provincial Key Laboratory of Organ Donation and Transplant Immunology, Guangzhou, China; Guangdong Provincial International Cooperation Base of Science and Technology (Organ Transplantation), Guangzhou, China.
⁴ Recanati/Miller Transplantation Institute, Mount Sinai Medical Center, New York, NY, USA.
⁵ Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁶ Southern California Liver Centers, 131 Orange Avenue, Suite 101, Coronado, CA, 92118, USA.
⁷ Division of Gastroenterology & Hepatology, Department of Medicine, University of California, San Diego, La Jolla CA, USA.
⁸ HPB Surgery, Hepatology and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.
⁹ HPB Surgery, Hepatology and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy; Department of Oncology, and Hemato-Oncology University of Milan, Milan, Italy.
¹⁰ Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ, 85054, USA; Transplant Center, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ, 85054, USA.
¹¹ Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ, 85054, USA.
¹² Division of Gastroenterology, Hepatology, and Nutrition, University of Minnesota, Minneapolis, MN, USA.
¹³ Liver Unit and HPB Oncology Area, Clinica Universidad de Navarra and CIBEREHD, Pamplona, Spain.
¹⁴ Section of GI Oncology, Department of Medical Oncology, Houston Methodist Neal Cancer Center, Houston, TX 77030, USA; Cockrell Center of Advanced Therapeutics Phase I Program, Houston Methodist Research Institute, Houston, TX 77030, USA; Department of Internal Medicine, Weill Cornell Medical College, New York, NY 10021, USA.
¹⁵ Section of GI Oncology, Department of Medical Oncology, Houston Methodist Neal Cancer Center, Houston, TX 77030, USA; Cancer Clinical Trials, Houston Methodist Research Institute, Houston, TX 77030, USA.
¹⁶ Department of Internal Medicine I, Gastroenterology, Hepatology, Endocrinology and Metabolism, Medical University of Innsbruck, Innsbruck, Austria.
¹⁷ Cancer Research Center of Lyon (CRCL), INSERM U1052, Centre National de la Recherche Scientifique UMR5286, Lyon, France; Department of Hepatology, Hôpital Croix-Rousse, Hospices Civils de Lyon, Lyon, France.
¹⁸ Division of Hematology/Oncology, Department of Internal Medicine, University of Cincinnati, Cincinnati, OH, USA.
¹⁹ AP-HP Sorbonne Université, Hôpital Universitaire Pitié-Salpêtrière, Service d'Hépato-gastroentérologie, Paris, France.
²⁰ AP-HP Sorbonne Université, Hôpital Universitaire Pitié-Salpêtrière, Service d'Hépato-gastroentérologie, Paris, France; INSERM UMR 1138, Centre de recherche des Cordeliers, 75006 Paris, France.
²¹ Division of Hematology and Oncology, Department of Medicine, O'Neal Comprehensive Cancer Center, University of Alabama at Birmingham Heersink School of Medicine, Birmingham, Alabama, USA.
²² Department of Hematology and Medical Oncology, Winship Cancer Institute, Emory University, Atlanta, GA, USA.
²³ Division of Hepatology, Montefiore Medical Center, Bronx, New York; Albert Einstein College of Medicine, Bronx, NY, USA.
²⁴ Division of Hepatology, Northwell 261 East 78th Street, Floor 4, New York, NY 10075, USA.
²⁵ Hepatobiliary Surgery and liver Transplantation, University of Pisa Medical School Hospital, Via Paradisa 2, Pisa, 56124, Italy.
²⁶ Department of Pediatrics, Division of Pediatric Hematology/Oncology/SCT, Columbia University Irving Medical Center, New York, New York, USA.
²⁷ Department of Pediatrics, Division of Pediatric Hematology/Oncology/SCT, Columbia University Irving Medical Center, New York, New York, USA; Department of Oncology, Division of Pediatric Oncology, Johns Hopkins School of Medicine, Baltimore, MD, USA.
²⁸ Department of Pediatrics. Vagelos College of Physician and Surgeons. Columbia University, USA.
²⁹ Mayo Clinic Florida, 4500 San Pablo Rd, Jacksonville, FL, 32224, USA.
³⁰ Division of Interventional Radiology, Mayo Clinic Florida, Jacksonville, FL 32224, USA.
³¹ Department of Oncology, Mayo Clinic, Rochester, MN 55905, USA.
³² Escola Superior de Ciências da Santa Casa de Misericórdia de Vitória - Department of Internal Medicine - Vitória/ES - Brazil.
³³ Escola Superior de Ciências da Santa Casa de Misericórdia de Vitória - Department of Gastroenterology and Hepatology - Vitória/ES - Brazil.
³⁴ Division of Hepatology, Department of Medicine, Einstein Healthcare Network, Philadelphia, Pennsylvania, USA.
³⁵ The Dumont-University of California, Los Angeles, Transplant Center, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA.
³⁶ Division of Gastroenterology and Hepatology, Department of Medicine, University of California San Francisco, USA.
³⁷ Division of Gastroenterology and Hepatology, University of Michigan, Ann Arbor, MI, USA.
³⁸ Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX, United States.
³⁹ Karsh Division of Gastroenterology and Hepatology, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA; Comprehensive Transplant Center, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA; Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA. Electronic address: judong.yang@cshs.org.

PMID: 38996924
PMCID: PMC11655254
DOI: 10.1016/j.jhep.2024.06.042

Meta-Analysis

Impact of pre-transplant immune checkpoint inhibitor use on post-transplant outcomes in HCC: A systematic review and individual patient data meta-analysis

Mohammad Saeid Rezaee-Zavareh et al. J Hepatol. 2025 Jan.

. 2025 Jan;82(1):107-119.

doi: 10.1016/j.jhep.2024.06.042. Epub 2024 Jul 10.

Authors

Affiliations

¹ Middle East Liver Diseases Center, Tehran 1417935840, Iran.
² Karsh Division of Gastroenterology and Hepatology, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA.
³ Organ Transplant Center, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China; Guangdong Provincial Key Laboratory of Organ Donation and Transplant Immunology, Guangzhou, China; Guangdong Provincial International Cooperation Base of Science and Technology (Organ Transplantation), Guangzhou, China.
⁴ Recanati/Miller Transplantation Institute, Mount Sinai Medical Center, New York, NY, USA.
⁵ Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁶ Southern California Liver Centers, 131 Orange Avenue, Suite 101, Coronado, CA, 92118, USA.
⁷ Division of Gastroenterology & Hepatology, Department of Medicine, University of California, San Diego, La Jolla CA, USA.
⁸ HPB Surgery, Hepatology and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.
⁹ HPB Surgery, Hepatology and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy; Department of Oncology, and Hemato-Oncology University of Milan, Milan, Italy.
¹⁰ Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ, 85054, USA; Transplant Center, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ, 85054, USA.
¹¹ Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ, 85054, USA.
¹² Division of Gastroenterology, Hepatology, and Nutrition, University of Minnesota, Minneapolis, MN, USA.
¹³ Liver Unit and HPB Oncology Area, Clinica Universidad de Navarra and CIBEREHD, Pamplona, Spain.
¹⁴ Section of GI Oncology, Department of Medical Oncology, Houston Methodist Neal Cancer Center, Houston, TX 77030, USA; Cockrell Center of Advanced Therapeutics Phase I Program, Houston Methodist Research Institute, Houston, TX 77030, USA; Department of Internal Medicine, Weill Cornell Medical College, New York, NY 10021, USA.
¹⁵ Section of GI Oncology, Department of Medical Oncology, Houston Methodist Neal Cancer Center, Houston, TX 77030, USA; Cancer Clinical Trials, Houston Methodist Research Institute, Houston, TX 77030, USA.
¹⁶ Department of Internal Medicine I, Gastroenterology, Hepatology, Endocrinology and Metabolism, Medical University of Innsbruck, Innsbruck, Austria.
¹⁷ Cancer Research Center of Lyon (CRCL), INSERM U1052, Centre National de la Recherche Scientifique UMR5286, Lyon, France; Department of Hepatology, Hôpital Croix-Rousse, Hospices Civils de Lyon, Lyon, France.
¹⁸ Division of Hematology/Oncology, Department of Internal Medicine, University of Cincinnati, Cincinnati, OH, USA.
¹⁹ AP-HP Sorbonne Université, Hôpital Universitaire Pitié-Salpêtrière, Service d'Hépato-gastroentérologie, Paris, France.
²⁰ AP-HP Sorbonne Université, Hôpital Universitaire Pitié-Salpêtrière, Service d'Hépato-gastroentérologie, Paris, France; INSERM UMR 1138, Centre de recherche des Cordeliers, 75006 Paris, France.
²¹ Division of Hematology and Oncology, Department of Medicine, O'Neal Comprehensive Cancer Center, University of Alabama at Birmingham Heersink School of Medicine, Birmingham, Alabama, USA.
²² Department of Hematology and Medical Oncology, Winship Cancer Institute, Emory University, Atlanta, GA, USA.
²³ Division of Hepatology, Montefiore Medical Center, Bronx, New York; Albert Einstein College of Medicine, Bronx, NY, USA.
²⁴ Division of Hepatology, Northwell 261 East 78th Street, Floor 4, New York, NY 10075, USA.
²⁵ Hepatobiliary Surgery and liver Transplantation, University of Pisa Medical School Hospital, Via Paradisa 2, Pisa, 56124, Italy.
²⁶ Department of Pediatrics, Division of Pediatric Hematology/Oncology/SCT, Columbia University Irving Medical Center, New York, New York, USA.
²⁷ Department of Pediatrics, Division of Pediatric Hematology/Oncology/SCT, Columbia University Irving Medical Center, New York, New York, USA; Department of Oncology, Division of Pediatric Oncology, Johns Hopkins School of Medicine, Baltimore, MD, USA.
²⁸ Department of Pediatrics. Vagelos College of Physician and Surgeons. Columbia University, USA.
²⁹ Mayo Clinic Florida, 4500 San Pablo Rd, Jacksonville, FL, 32224, USA.
³⁰ Division of Interventional Radiology, Mayo Clinic Florida, Jacksonville, FL 32224, USA.
³¹ Department of Oncology, Mayo Clinic, Rochester, MN 55905, USA.
³² Escola Superior de Ciências da Santa Casa de Misericórdia de Vitória - Department of Internal Medicine - Vitória/ES - Brazil.
³³ Escola Superior de Ciências da Santa Casa de Misericórdia de Vitória - Department of Gastroenterology and Hepatology - Vitória/ES - Brazil.
³⁴ Division of Hepatology, Department of Medicine, Einstein Healthcare Network, Philadelphia, Pennsylvania, USA.
³⁵ The Dumont-University of California, Los Angeles, Transplant Center, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA.
³⁶ Division of Gastroenterology and Hepatology, Department of Medicine, University of California San Francisco, USA.
³⁷ Division of Gastroenterology and Hepatology, University of Michigan, Ann Arbor, MI, USA.
³⁸ Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX, United States.
³⁹ Karsh Division of Gastroenterology and Hepatology, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA; Comprehensive Transplant Center, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA; Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles 90048, CA, USA. Electronic address: judong.yang@cshs.org.

PMID: 38996924
PMCID: PMC11655254
DOI: 10.1016/j.jhep.2024.06.042

Abstract

Background & aims: Treatment with immune checkpoint inhibitors (ICIs) for hepatocellular carcinoma (HCC) prior to liver transplantation (LT) has been reported; however, ICIs may elevate the risk of allograft rejection and impact other clinical outcomes. This study aims to summarize the impact of ICI use on post-LT outcomes.

Methods: In this individual patient data meta-analysis, we searched databases to identify HCC cases treated with ICIs before LT, detailing allograft rejection, HCC recurrence, and overall survival. We performed Cox regression analysis to identify risk factors for allograft rejection.

Results: Among 91 eligible patients, with a median (IQR) follow-up of 690.0 (654.5) days, there were 24 (26.4%) allograft rejections, 9 (9.9%) HCC recurrences, and 9 (9.9%) deaths. Age (adjusted hazard ratio [aHR] per 10 years 0.72, 95% CI 0.53-0.99, p = 0.044) and ICI washout time (aHR per 1 week 0.92, 95% CI 0.86-0.99, p = 0.022) were associated with allograft rejection. The median (IQR) washout period for patients with ≤20% probability of allograft rejection was 94 (196) days. Overall survival did not differ between cases with and without allograft rejection (log-rank test, p = 0.2). Individuals with HCC recurrence had fewer median (IQR) ICI cycles than those without recurrence (4.0 [1.8] vs. 8.0 [9.0]; p = 0.025). The proportion of patients within Milan post-ICI was lower for those with recurrence vs. without (16.7% vs. 65.3%, p = 0.032).

Conclusion: Patients have acceptable post-LT outcomes after ICI therapy. Age and ICI washout length relate to the allograft rejection risk, and a 3-month washout may reduce it to that of patients without ICI exposure. Number of ICI cycles and tumor burden may affect recurrence risk. Large prospective studies are necessary to confirm these associations.

Impact and implications: This systematic review and individual patient data meta-analysis of 91 patients with hepatocellular carcinoma and immune checkpoint inhibitor use prior to liver transplantation suggest acceptable overall post-transplant outcomes. Older age and longer immune checkpoint inhibitor washout period have a significant inverse association with the risk of allograft rejection. A 3-month washout may reduce it to that of patients without immune checkpoint inhibitor exposure. Additionally, a higher number of immune checkpoint inhibitor cycles and tumor burden within Milan criteria at the completion of immunotherapy may predict a decreased risk of hepatocellular carcinoma recurrence, but this observation requires further validation in larger prospective studies.

Keywords: Graft Rejection; Hepatocellular Carcinoma; Immune Checkpoint Inhibitors; Liver Neoplasms; Liver Transplantation; Recurrence.

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Conflict of interest statement

Conflict of interest

Ju Dong Yang provides a consulting service for AstraZeneca, Eisai, Exact Sciences, Exelixis, Fujifilm Medical Sciences, and Gilead Sciences. Neehar Parikh has served as a consultant or advisor for Genentech, Fujifilm Medical, Eisai, Exelixis, Merck, Exact Sciences, Freenome, and Gilead. Amit Singal has served as a consultant or on advisory boards for Genentech, AstraZeneca, Bayer, Eisai, Exelixis, Merck, Elevar, Boston Scientific, Sirtex, HistoSonics, Fujifilm Medical Sciences, Exact Sciences, Glycotest, Abbott, Roche, Freenome, and GRAIL. Neil Mehta has served as a consultant or advisor for Exelixis, Fujifilm Medical, Genentech, Eisai, Exelixis, Exact Sciences, and Merck. Sherrie Bhoori serves as an advisor or lecturer for Roche, AstraZeneca, Boston Scientific, Terumo. Beau B. Toskich serves as an advisor for Genentech, Eisai, and Astra Zeneca. Robyn D. Gartrell’s laboratory receives funding from Hyundai Hope on Wheels Hope Scholar Award, Swim Across America, Rally Foundation, StacheStrong and Musella Foundation. Bruno Sangro reports consulting or advisory fees from AstraZeneca, Bayer, Boston Scientific, Bristol-Myers Squibb, Eisai, lncyte, IPSEN, Roche, Sirtex Medical, and Terumo; reports being an invited speaker for AstraZeneca, Bristol-Myers Squibb, Eisai, lncyte, IPSEN, Roche, and Sirtex Medical; research funding (to institution) from Bristol-Myers Squibb and Sirtex Medical. Tarek Hassanein serves as an advisory committee member or review panelist for AbbVie, Cymabay, Gilead, HepQuant, Madrigal, Mallinckrodt; has received grant and research support from AbbVie, Amgen, Biolinq, Bristol-Myers Squibb, Astra Zeneca, Boehringerlngelheim, Bristol-Myers Squibb, COUR, DURECT Corporation, Escient, Galectin, Gilead, Grifols, HepQuant, Intercept, Janssen, Merck, Mirum, NeuroBo, Novartis, Novo Nordisk, Pfizer, Regeneron, Salix Pharmaceuticals, Sonic lncytes. Takeda, Terns Pharmaceuticals, Valeant; and also involved in speaking engagements and teaching for for AbbVie, Gilead, Intercept, Mallinckrodt, Salix Pharmaceuticals. Davendra Sohal has served on the speakers Bureau for Astra Zeneca since January 2024, lncyte since January 2021, and Seagen since January 2023; and has received consulting fees or honoraria from Astra Zeneca (ended Jan 2024), Replimune (ended Jan 2024), Cancer Commons (ended Jun 2023), TransThera (ended Jun 2022), Totus Medicines (ended Jul 2023), Valar Labs (ended Dec 2022), Aadi (ended Jun 2023), Elevar, Regeneron; and has received research funding from Aadi, Ability Pharma, Amgen, Apexigen, Astellas, Astra Zeneca, Bexion, Bristol-Myers Squibb, FibroGen, Genentech, Hengrui, Merck, Mirati, NextCure, PanCAN, Regeneron, Roche, Triumvira. Nguyen H Tran has served as an advisor for Astrazeneca, Genentech, Helsinn and TEMPUS. She is a recipient of the K23MD017217–01A1. Parissa Tabrizian serves as an advisor for Bayer. Astrazeneca, boston scientific. -honorarium. Mehmet Akce has been involved in research projects with Bristol-Myers Squibb-Ono Pharmaceutical (Inst), Xencor (Inst), Merck Sharp & Dohme (Inst), Eisai (Inst), GSK (Inst), Bayer (Inst), Relay (Inst), ProDa BioTech (Inst), Exelixis (lnst),and AstraZeneca (Inst) and also has consulting or advisory roles for Eisai, Ipsen, Exelixis, GSK, QED, lsofol, Curio Science, AstraZeneca, Genentech, lncyte, and Taiho. Other authors declare no conflict of interest.

Please refer to the accompanying ICMJE disclosure forms for further details.

Figures

**Fig. 1.. PRISMA flowchart diagram.**
CAR, chimeric antigen receptor; ICIs, immune checkpoint inhibitors; LT, liver transplant.

**Fig. 2.. Comparison of immune checkpoint inhibitor washout period in patients with and without allograft rejection.**

**Fig. 3.. Kaplan-Meier curve comparing overall survival between cases with and without liver transplant allograft rejection.**
The Kaplan-Meier curve showed no difference between cases with and without allograft rejection regarding overall survival (HR 2.158, 95% CI 0.575–8.098, p = 0.2, log-rank test). HR, hazard ratio.

Fig. 4.. Immune checkpoint inhibitor washout period, patient age, and probability of allograft rejection based on a Cox regression model adjusted for age and Immune checkpoint inhibitor washout period.
The median (IQR) washout period(in days) for patients with less than 20% and 30% probability of allograft rejection was 94 (196) and 72 (136), respectively.

See this image and copyright information in PMC

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Impact of pre-transplant immune checkpoint inhibitor use on post-transplant outcomes in HCC: A systematic review and individual patient data meta-analysis

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Impact of pre-transplant immune checkpoint inhibitor use on post-transplant outcomes in HCC: A systematic review and individual patient data meta-analysis

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