Utilization of Immunotherapy for the Treatment of Hepatocellular Carcinoma in the Peri-Transplant Setting: Transplant Oncology View
Abstract
:Simple Summary
Abstract
1. Introduction
2. ICPI Pre-Liver Transplant: HCC Bridging Therapy
3. ICPI Post-Liver Transplant: HCC Palliative Therapy
Age/Sex | ICPIs Agent | ICPIs Cycles | ICPIs Class | Interval Time from Transplant to ICPIs | IST | Type of Response | Graft Outcome | References |
---|---|---|---|---|---|---|---|---|
70 M | Nivolumab | (4) | PD-1 | 33 Months | Tacrolimus/high-dose steroids. | PD | No rejection | Al Jarroudi et al. [31] |
62 F | Nivolumab | (5) | PD-1 | 12 Months | Tacrolimus | PD | No rejection | Al Jarroudi et al. [31] |
66 M | Nivolumab | (6) | PD-1 | 24 Months | Tacrolimus | PD | No rejection | Al Jarroudi et al. [31] |
56 M | Nivolumab | (6) | PD-1 | 31 Months | Tacrolimus | PD | No rejection | DeLeon et al. [32] |
55 M | Nivolumab | (5) | PD-1 | 92 Months | Sirolimus/MMF | PD | No rejection | DeLeon et al. [32] |
34 F | Nivolumab | UK | PD-1 | 43 Months | Tacrolimus | PD | No rejection | DeLeon et al. [32] |
63 M | Nivolumab | UK | PD-1 | 14 Months | Tacrolimus | UK | No rejection | DeLeon et al. [32] |
68 M | Nivolumab | UK | PD-1 | 13 Months | Sirolimus | UK | Graft rejection | DeLeon et al. [32] |
41 M | Nivolumab | (15) | PD-1 | 16 Months | Tacrolimus (1 mg) | PD | No rejection | De Toni and Gerbes et al. [33] |
70 M | Pembrolizumab | PD-1 | 96 Months | Low-dose (50%) Tacrolimus | PD | No rejection | Varkaris et al. [34] | |
53 F | Nivolumab | (1) | PD-1 | 36 Months | Everolimus/MMF | D due to OF (2 weeks after start ICPI) | Graft rejection | Gassmann et al. [35] |
14 M | Nivolumab | (1) | PD-1 | 36 Months | Tacrolimus (4 mg) | D due to OF (5 weeks after start ICPI) | Graft rejection | Friend et al. [36] |
20 M | Nivolumab | (2) | PD-1 | 48 Months | Sirolimus (2 mg) | D due to OF (4 weeks after start ICPI) | Graft rejection | Friend et al. [36] |
4. Assessment of Immune Checkpoint Inhibitors
4.1. Does Immunosuppression Affect the Efficacy of ICPIs?
4.2. Which ICPI Class Is Safer?
4.3. Can Liver Biopsy Help with Patient Selection and Prediction of Rejection?
4.4. The Timing of ICPI Peri-Transplant
4.5. What about Adverse Events of ICPIs?
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Abdelrahim, M.; Esmail, A.; Abudayyeh, A.; Murakami, N.; Saharia, A.; McMillan, R.; Victor, D.; Kodali, S.; Shetty, A.; Fong, J.V.N.; et al. Transplant oncology: An evolving field in cancer care. Cancers 2021, 13, 4911. [Google Scholar] [CrossRef]
- Abdelrahim, M.; Victor, D.; Esmail, A.; Kodali, S.; Graviss, E.A.; Nguyen, D.T.; Moore, L.W.; Saharia, A.; McMillan, R.; Fong, J.N.; et al. Transarterial Chemoembolization (TACE) plus sorafenib compared to TACE alone in transplant recipients with hepatocellular carcinoma: An institution experience. Cancers 2022, 14, 650. [Google Scholar] [CrossRef] [PubMed]
- Abou-Alfa, G.K.; Meyer, T.; Cheng, A.-L.; El-Khoueiry, A.B.; Rimassa, L.; Ryoo, B.-Y.; Cicin, I.; Merle, P.; Park, J.-W.; Blanc, J.-F.; et al. Cabozantinib (C) versus placebo (P) in patients (pts) with advanced hepatocellular carcinoma (HCC) who have received prior sorafenib: Results from the randomized phase III CELESTIAL trial. J. Clin. Oncol. 2018, 36, 207. [Google Scholar] [CrossRef]
- Al Jarroudi, O.; Ulusakarya, A.; Almohamad, W.; Afqir, S.; Morere, J.-F. Anti-programmed cell death protein 1 (PD-1) immunotherapy for metastatic hepatocellular carcinoma after liver transplantation: A report of three cases. Cureus 2020, 12, e11150. [Google Scholar] [CrossRef]
- Balogh, J.; Victor, D.; Asham, E.H.; Burroughs, S.G.; Boktour, M.; Saharia, A.; Li, X.; Ghobrial, R.M.; Monsour, H. Hepatocellular carcinoma: A review. J. Hepatocell. Carcinoma 2016, 3, 41–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barnett, R.; Barta, V.S.; Jhaveri, K.D. Preserved renal-allograft function and the PD-1 pathway inhibitor nivolumab. N. Engl. J. Med. 2017, 376, 191–192. [Google Scholar] [CrossRef] [PubMed]
- Brahmer, J.R.; Lacchetti, C.; Schneider, B.J.; Atkins, M.B.; Brassil, K.J.; Caterino, J.M.; Chau, I.; Ernstoff, M.S.; Gardner, J.M.; Ginex, P.; et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American society of clinical oncology clinical practice guideline. J. Clin. Oncol. 2018, 36, 1714–1768. [Google Scholar] [CrossRef] [PubMed]
- Chau, I.; Peck-Radosavljevic, M.; Borg, C.; Malfertheiner, P.; Seitz, J.F.; Park, J.O.; Ryoo, B.-Y.; Yen, C.-J.; Kudo, M.; Poon, R.; et al. Ramucirumab as second-line treatment in patients with advanced hepatocellular carcinoma following first-line therapy with sorafenib: Patient-focused outcome results from the randomised phase III REACH study. Eur. J. Cancer 2017, 81, 17–25. [Google Scholar] [CrossRef] [PubMed]
- Cidon, E.U. Systemic treatment of hepatocellular carcinoma: Past, present and future. World J. Hepatol. 2017, 9, 797–807. [Google Scholar] [CrossRef] [PubMed]
- Atezolizumab and Bevacizumab Pre-Liver Transplantation for Patients with Hepatocellular Carcinoma Beyond Milan Criteria. (Updated on 1 October 2021). Available online: https://clinicaltrials.gov/ct2/show/NCT05185505?term=abdelrahim&draw=2&rank=3 (accessed on 1 October 2021).
- De Bruyn, P.; Van Gestel, D.; Ost, P.; Kruse, V.; Brochez, L.; Van Vlierberghe, H.; Devresse, A.; Del Marmol, V.; Le Moine, A.; Aspeslagh, S. Immune checkpoint blockade for organ transplant patients with advanced cancer: How far can we go? Curr. Opin. Oncol. 2019, 31, 54–64. [Google Scholar] [CrossRef]
- De Stefano, F.; Chacon, E.; Turcios, L.; Marti, F.; Gedaly, R. Novel biomarkers in hepatocellular carcinoma. Dig. Liver Dis. 2018, 50, 1115–1123. [Google Scholar] [CrossRef]
- De Toni, E.N.; Gerbes, A.L. Tapering of immunosuppression and sustained treatment with nivolumab in a liver transplant recipient. Gastroenterology 2017, 152, 1631–1633. [Google Scholar] [CrossRef] [Green Version]
- DeLeon, T.T.; Salomao, M.A.; Aqel, B.A.; Sonbol, M.B.; Yokoda, R.T.; Ali, A.H.; Moss, A.A.; Mathur, A.K.; Chascsa, D.M.; Rakela, J.; et al. Pilot evaluation of PD-1 inhibition in metastatic cancer patients with a history of liver transplantation: The mayo clinic experience. J. Gastrointest. Oncol. 2018, 9, 1054–1062. [Google Scholar] [CrossRef]
- El-Khoueiry, A.B.; Sangro, B.; Yau, T.; Crocenzi, T.S.; Kudo, M.; Hsu, C.; Kim, T.-Y.; Choo, S.-P.; Trojan, J.; Welling, T.H., 3rd; et al. Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): An open-label, non-comparative, phase 1/2 dose escalation and expansion trial. Lancet 2017, 389, 2492–2502. [Google Scholar] [CrossRef]
- Feun, L.G.; Li, Y.; Wu, C.; Wangpaichitr, M.; Jones, P.D.; Richman, S.P.; Madrazo, B.; Kwon, D.; Garcia-Buitrago, M.; Martin, P.; et al. Phase 2 study of pembrolizumab and circulating biomarkers to predict anticancer response in advanced, unresectable hepatocellular carcinoma. Cancer 2019, 125, 3603–3614. [Google Scholar] [CrossRef] [PubMed]
- Finn, R.S.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.-Y.; Kudo, M.; Breder, V.; Merle, P.; Kaseb, A.O.; et al. Atezolizumab plus bevacizumab in unresectable hepatocellular carcinoma. N. Engl. J. Med. 2020, 382, 1894–1905. [Google Scholar] [CrossRef] [PubMed]
- Finn, R.S.; Ryoo, B.-Y.; Merle, P.; Kudo, M.; Bouattour, M.; Lim, H.Y.; Breder, V.; Edeline, J.; Chao, Y.; Ogasawara, S.; et al. Pembrolizumab as second-line therapy in patients with advanced hepatocellular carcinoma in KEYNOTE-240: A randomized, double-blind, phase III trial. J. Clin. Oncol. 2020, 38, 193–202. [Google Scholar] [CrossRef] [PubMed]
- Finn, R.S.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.-Y.; Lim, H.Y.; Kudo, M.; Breder, V.V.; Merle, P.; et al. IMbrave150: Updated overall survival (OS) data from a global, randomized, open-label phase III study of atezolizumab (atezo) + bevacizumab (bev) versus sorafenib (sor) in patients (pts) with unresectable hepatocellular carcinoma (HCC). J. Clin. Oncol. 2021, 39, 267. [Google Scholar] [CrossRef]
- Freites-Martinez, A.; Santana, N.; Arias-Santiago, S.; Viera, A. Using the common terminology criteria for adverse events (CTCAE—Version 5.0) to evaluate the severity of adverse events of anticancer therapies. Actas Dermo-Sifiliográficas 2020, 112, 90–92. [Google Scholar] [CrossRef] [PubMed]
- Freites-Martinez, A.; Santana, N.; Arias-Santiago, S.; Viera, A. CTCAE versión 5.Evaluación de la gravedad de los eventos adversos dermatológicos de las terapias antineoplásicas. Actas Dermo-Sifiliográficas 2021, 112, 90–92. [Google Scholar] [CrossRef]
- Friend, B.D.; Venick, R.S.; McDiarmid, S.V.; Zhou, X.; Naini, B.; Wang, H.; Farmer, D.G.; Busuttil, R.W.; Federman, N. Fatal orthotopic liver transplant organ rejection induced by a checkpoint inhibitor in two patients with refractory, metastatic hepatocellular carcinoma. Pediatr. Blood Cancer 2017, 64, e26682. [Google Scholar] [CrossRef] [PubMed]
- Garant, A.; Guilbault, C.; Ekmekjian, T.; Greenwald, Z.; Murgoi, P.; Vuong, T. Concomitant use of corticosteroids and immune checkpoint inhibitors in patients with hematologic or solid neoplasms: A systematic review. Crit. Rev. Oncol. 2017, 120, 86–92. [Google Scholar] [CrossRef] [PubMed]
- Gassmann, D.; Weiler, S.; Mertens, J.C.; Reiner, C.S.; Vrugt, B.; Nägeli, M.; Mangana, J.; Müllhaupt, B.; Jenni, F.; Misselwitz, B. Liver allograft failure after nivolumab treatment—A case report with systematic literature research. Transplant. Direct 2018, 4, e376. [Google Scholar] [CrossRef] [PubMed]
- Gordan, J.D.; Kennedy, E.B.; Abou-Alfa, G.K.; Beg, M.S.; Brower, S.T.; Gade, T.P.; Goff, L.; Gupta, S.; Guy, J.; Harris, W.P.; et al. Systemic therapy for advanced hepatocellular carcinoma: ASCO guideline. J. Clin. Oncol. 2020, 38, 4317–4345. [Google Scholar] [CrossRef] [PubMed]
- Ho, C.-M.; Chen, H.-L.; Hu, R.-H.; Lee, P.-H. Harnessing immunotherapy for liver recipients with hepatocellular carcinoma: A review from a transplant oncology perspective. Ther. Adv. Med Oncol. 2019, 11, 1758835919843463. [Google Scholar] [CrossRef] [PubMed]
- Hodi, F.S. Cytotoxic T-lymphocyte–associated antigen-4. Clin. Cancer Res. 2007, 13, 5238–5242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Horvat, T.; Adel, N.G.; Dang, T.-O.; Momtaz, P.; Postow, M.A.; Callahan, M.K.; Carvajal, R.D.; Dickson, M.A.; D’Angelo, S.P.; Woo, K.M.; et al. Immune-related adverse events, need for systemic immunosuppression, and effects on survival and time to treatment failure in patients with melanoma treated with ipilimumab at memorial Sloan Kettering Cancer Center. J. Clin. Oncol. 2015, 33, 3193–3198. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kanwal, F.; Singal, A.G. Surveillance for hepatocellular carcinoma: Current best practice and future direction. Gastroenterology 2019, 157, 54–64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kudo, M.; Finn, R.S.; Qin, S.; Han, K.-H.; Ikeda, K.; Piscaglia, F.; Baron, A.; Park, J.-W.; Han, G.; Jassem, J.; et al. Lenvatinib versus sorafenib in first-line treatment of patients with unresectable hepatocellular carcinoma: A randomised phase 3 non-inferiority trial. Lancet 2018, 391, 1163–1173. [Google Scholar] [CrossRef] [Green Version]
- Kumar, V.; Shinagare, A.B.; Rennke, H.G.; Ghai, S.; Lorch, J.H.; Ott, P.A.; Rahma, O.E. The safety and efficacy of checkpoint inhibitors in transplant recipients: A case series and systematic review of literature. Oncologist 2020, 25, 505–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuo, J.C.; Lilly, L.B.; Hogg, D. Immune checkpoint inhibitor therapy in a liver transplant recipient with a rare subtype of melanoma: A case report and literature review. Melanoma Res. 2018, 28, 61–64. [Google Scholar] [CrossRef] [PubMed]
- Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J.J.; Cowey, C.L.; Lao, C.D.; Schadendorf, D.; Dummer, R.; Smylie, M.; Rutkowski, P.; et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 2015, 373, 1270–1271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Llovet, J.M.; Castet, F.; Heikenwalder, M.; Maini, M.K.; Mazzaferro, V.; Pinato, D.J.; Pikarsky, E.; Zhu, A.X.; Finn, R.S. Immunotherapies for hepatocellular carcinoma. Nat. Rev. Clin. Oncol. 2021, 19, 151–172. [Google Scholar] [CrossRef] [PubMed]
- Jilkova, Z.M.; Ghelfi, J.; Decaens, T. Immunomodulation for hepatocellular carcinoma therapy: Current challenges. Curr. Opin. Oncol. 2021, 34, 155–160. [Google Scholar] [CrossRef] [PubMed]
- Mazzaferro, V.; Regalia, E.; Doci, R.; Andreola, S.; Pulvirenti, A.; Bozzetti, F.; Montalto, F.; Ammatuna, M.; Morabito, A.; Gennari, L. Liver Transplantation for the treatment of Small Hepatocellular Carcinomas in Patients with Cirrhosis. N. Engl. J. Med. 1996, 334, 693–700. [Google Scholar] [CrossRef]
- Mazzaferro, V.; Sposito, C.; Coppa, J.; Miceli, R.; Bhoori, S.; Bongini, M.; Camerini, T.; Milione, M.; Regalia, E.; Spreafico, C.; et al. The long-term benefit of liver transplantation for hepatic metastases from neuroendocrine tumors. Am. J. Transplant. 2016, 16, 2892–2902. [Google Scholar] [CrossRef] [PubMed]
- Morales, R.E.; Shoushtari, A.N.; Walsh, M.M.; Grewal, P.; Lipson, E.J.; Carvajal, R.D. Safety and efficacy of ipilimumab to treat advanced melanoma in the setting of liver transplantation. J. Immunother. Cancer 2015, 3, 22. [Google Scholar] [CrossRef] [Green Version]
- Munker, S.; De Toni, E.N. Use of checkpoint inhibitors in liver transplant recipients. United Eur. Gastroenterol. J. 2018, 6, 970–973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murakami, N.; Mulvaney, P.; Danesh, M.; Abudayyeh, A.; Diab, A.; Abdel-Wahab, N.; Abdelrahim, M.; Khairallah, P.; Shirazian, S.; Kukla, A.; et al. A multi-center study on safety and efficacy of immune checkpoint inhibitors in cancer patients with kidney transplant. Kidney Int. 2021, 100, 196–205. [Google Scholar] [CrossRef] [PubMed]
- Ranganath, H.A.; Panella, T.J. Administration of ipilimumab to a liver transplant recipient with unresectable metastatic melanoma. J. Immunother. 2015, 38, 211. [Google Scholar] [CrossRef]
- Qin, S.; Ren, Z.; Feng, Y.-H.; Yau, T.; Wang, B.; Zhao, H.; Bai, Y.; Gu, S.; Li, L.; Hernandez, S.; et al. Atezolizumab plus bevacizumab versus sorafenib in the Chinese subpopulation with unresectable hepatocellular carcinoma: Phase 3 randomized, open-label IMbrave150 study. Liver Cancer 2021, 10, 296–308. [Google Scholar] [CrossRef]
- Rammohan, A.; Reddy, M.S.; Farouk, M.; Vargese, J.; Rela, M. Pembrolizumab for metastatic hepatocellular carcinoma following live donor liver transplantation: The silver bullet? Hepatology 2018, 67, 1166–1168. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reddy, T.; Esmail, A.; Chang, J.C.; Ghobrial, R.M.; Abdelrahim, M. Utility of cell-free DNA detection in transplant oncology. Cancers 2022, 14, 743. [Google Scholar] [CrossRef] [PubMed]
- Tabrizian, P.; Florman, S.S.; Schwartz, M.E. PD-1 inhibitor as bridge therapy to liver transplantation? Am. J. Transplant. 2021, 21, 1979–1980. [Google Scholar] [CrossRef]
- Tio, M.; Rai, R.; Ezeoke, O.M.; McQuade, J.L.; Zimmer, L.; Khoo, C.; Park, J.; Spain, L.; Turajlic, S.; Ardolino, L.; et al. Anti-PD-1/PD-L1 immunotherapy in patients with solid organ transplant, HIV or hepatitis B/C infection. Eur. J. Cancer 2018, 104, 137–144. [Google Scholar] [CrossRef]
- Varkaris, A.; Lewis, D.W.; Nugent, F.W. Preserved liver transplant after PD-1 pathway inhibitor for hepatocellular carcinoma. Am. J. Gastroenterol. 2017, 112, 1895–1896. [Google Scholar] [CrossRef]
- Wainberg, Z.A.; Segal, N.H.; Jaeger, D.; Lee, K.-H.; Marshall, J.; Antonia, S.J.; Butler, M.; Sanborn, R.E.; Nemunaitis, J.J.; Carlson, C.A.; et al. Safety and clinical activity of durvalumab monotherapy in patients with hepatocellular carcinoma (HCC). J. Clin. Oncol. 2017, 35, 4071. [Google Scholar] [CrossRef]
- Walunas, T.L.; Lenschow, D.J.; Bakker, C.Y.; Linsley, P.S.; Freeman, G.J.; Green, J.M.; Thompson, C.B.; Bluestone, J.A. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1994, 1, 405–413. [Google Scholar] [CrossRef]
- Yau, T.; Park, J.W.; Finn, R.S.; Cheng, A.L.; Mathurin, P.; Edeline, J.; Kudo, M.; Han, K.H.; Harding, J.J.; Merle, P.; et al. CheckMate 459: A randomized, multi-center phase III study of nivolumab (NIVO) vs sorafenib (SOR) as first-line (1L) treatment in patients (pts) with advanced hepatocellular carcinoma (aHCC). Ann. Oncol. 2019, 30, v874–v875. [Google Scholar] [CrossRef]
- Yau, T.; Kang, Y.-K.; Kim, T.-Y.; El-Khoueiry, A.B.; Santoro, A.; Sangro, B.; Melero, I.; Kudo, M.; Hou, M.-M.; Matilla, A.; et al. Nivolumab (NIVO) + ipilimumab (IPI) combination therapy in patients (pts) with advanced hepatocellular carcinoma (aHCC): Results from CheckMate. J. Clin. Oncol. 2019, 37 (Suppl. S15), 4012. [Google Scholar] [CrossRef]
- Yau, T.; Kang, Y.-K.; Kim, T.-Y.; El-Khoueiry, A.B.; Santoro, A.; Sangro, B.; Melero, I.; Kudo, M.; Hou, M.-M.; Matilla, A.; et al. Efficacy and safety of nivolumab plus ipilimumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib: The CheckMate 040 randomized clinical trial. JAMA Oncol. 2020, 6, e204564. [Google Scholar] [CrossRef]
- Zhu, A.X.; Finn, R.S.; Edeline, J.; Cattan, S.; Ogasawara, S.; Palmer, D.; Verslype, C.; Zagonel, V.; Fartoux, L.; Vogel, A.; et al. Pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib (KEYNOTE-224): A non-randomised, open-label phase 2 trial. Lancet Oncol. 2018, 19, 940–952. [Google Scholar] [CrossRef]
- Ziemer, M.; Koukoulioti, E.; Beyer, S.; Simon, J.C.; Berg, T. Managing immune checkpoint-inhibitor-induced severe autoimmune-like hepatitis by liver-directed topical steroids. J. Hepatol. 2017, 66, 657–659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ziogas, I.A.; Evangeliou, A.P.; Giannis, D.; Hayat, M.H.; Mylonas, K.S.; Tohme, S.; Geller, D.A.; Elias, N.; Goyal, L.; Tsoulfas, G. The role of immunotherapy in hepatocellular carcinoma: A systematic review and pooled analysis of 2402 patients. Oncologist 2020, 26, e1036–e1049. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Abdelrahim, M.; Esmail, A.; Saharia, A.; Abudayyeh, A.; Abdel-Wahab, N.; Diab, A.; Murakami, N.; Kaseb, A.O.; Chang, J.C.; Gaber, A.O.; et al. Utilization of Immunotherapy for the Treatment of Hepatocellular Carcinoma in the Peri-Transplant Setting: Transplant Oncology View. Cancers 2022, 14, 1760. https://doi.org/10.3390/cancers14071760
Abdelrahim M, Esmail A, Saharia A, Abudayyeh A, Abdel-Wahab N, Diab A, Murakami N, Kaseb AO, Chang JC, Gaber AO, et al. Utilization of Immunotherapy for the Treatment of Hepatocellular Carcinoma in the Peri-Transplant Setting: Transplant Oncology View. Cancers. 2022; 14(7):1760. https://doi.org/10.3390/cancers14071760
Chicago/Turabian StyleAbdelrahim, Maen, Abdullah Esmail, Ashish Saharia, Ala Abudayyeh, Noha Abdel-Wahab, Adi Diab, Naoka Murakami, Ahmed O. Kaseb, Jenny C. Chang, Ahmed Osama Gaber, and et al. 2022. "Utilization of Immunotherapy for the Treatment of Hepatocellular Carcinoma in the Peri-Transplant Setting: Transplant Oncology View" Cancers 14, no. 7: 1760. https://doi.org/10.3390/cancers14071760