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Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (31 October 2023) | Viewed by 29219

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Dr. Angela Dalia Ricci

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Medical Oncology Unit, National Institute of Gastroenterology, “Saverio de Bellis” Research Hospital, 70013 Castellana Grotte, Italy
Interests: hepatocellular carcinoma; immunotherapy; gastric cancer; HCC; renal cell carcinoma; urothelial carcinoma; biliary tract cancer; cholangiocarcinoma
Special Issues, Collections and Topics in MDPI journals

Dr. Alessandro Rizzo

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Struttura Semplice Dipartimentale di Oncologia Medica per la Presa in Carico Globale del Paziente Oncologico "Don Tonino Bello", I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", 70124 Bari, Italy
Interests: immunotherapy; renal cell carcinoma; gastric cancer; urothelial carcinoma; prostate cancer; biliary tract cancer; hepatocellular carcinoma; HCC; targeted therapies; colorectal cancer; cholangiocarcinoma; bladder cancer; lung cancer; breast cancer; pancreatic cancer
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Hepatocellular carcinoma (HCC) is one of the most common cancers worldwide. Emerging immune checkpoint inhibitors (ICIs) have also made progress in HCC, with two PD-1 inhibitors—nivolumab and pembrolizumab—both being approved by the United States Food and Drug Administration (FDA). ICIs alone as a first-line treatment have not achieved the desired effect; however, clinical trials evaluating combinatorial strategies involving ICIs and other anticancer agents, especially antiangiogenic agents, have produced more compelling results, marking a new era in HCC management. The Practice-Changing Phase III IMbrave150 Trial compared the use of a combination of the PD-L1 inhibitor atezolizumab and bevacizumab versus sorafenib monotherapy in treatment-naïve patients with advanced HCC and showed that combination therapy resulted in higher median overall survival (OS), median progression-free survival (PFS) benefit, and overall response rate (ORR). Atezolizumab–bevacizumab is also currently recognized as the new standard of care in front-line HCC and has been approved for use in several countries worldwide. Similarly, other combinations have been tested and are currently being evaluated.

From this point of view, this Special Issue welcomes basic research, reviews, case reports, etc., on the current state of the art in the immunotherapy of HCC.

Potential topics include, but are not limited to:

Translational research;
Molecular experiments on novel immune-based combinations;
Real-world experience with immune checkpoint inhibitors;
Fighting resistance to immune checkpoint inhibitors;
Biomarker-driven studies.

Dr. Angela Dalia Ricci
Dr. Alessandro Rizzo
Guest Editors

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Keywords

liver cancer
hepatocellular carcinoma
immunotherapy
immune checkpoint inhibitors
atezolizumab

Published Papers (12 papers)

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Editorial

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3 pages, 444 KiB

Open AccessEditorial

Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy

by Alessandro Rizzo and Angela Dalia Ricci

Int. J. Mol. Sci. 2022, 23(19), 11363; https://doi.org/10.3390/ijms231911363 - 26 Sep 2022

Cited by 7 | Viewed by 1657

Abstract

Hepatocellular carcinoma (HCC) is one of the most common cancers worldwide [...] Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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Research

Jump to: Editorial, Review

10 pages, 1396 KiB

Open AccessArticle

Galad Score as a Prognostic Marker for Patients with Hepatocellular Carcinoma

by Silvia Cagnin, Rossella Donghia, Andrea Martini, Pasqua Letizia Pesole, Sergio Coletta, Endrit Shahini, Giulia Boninsegna, Alessandra Biasiolo, Patrizia Pontisso and Gianluigi Giannelli

Int. J. Mol. Sci. 2023, 24(22), 16485; https://doi.org/10.3390/ijms242216485 - 18 Nov 2023

Cited by 2 | Viewed by 1063

Abstract

Background: Hepatocellular carcinoma (HCC) accounts for more than 75% of primary liver cancers, which are the second leading cause of cancer-related deaths. The GALAD (gender, age, AFP-L3, AFP, and des-carboxy-prothrombin) score is a diagnostic tool developed based on gender, age, alpha-fetoprotein, alpha-fetoprotein L3, and des-gamma-carboxy prothrombin, originally designed as a diagnostic tool for HCC in high-risk patients. Methods: We analyzed 212 patients with and without cirrhosis. The population study was divided into patients with liver cirrhosis without evidence of HCC at the time of serum sample collection for GALAD score determination and patients with liver cirrhosis and a confirmed diagnosis of HCC at the time of serum sample collection for GALAD score determination. Patients were followed up until death or liver transplantation. The association between variables and HCC mortality risk was performed, and the results were presented as hazard ratio (HR). The receiver operating characteristic (ROC) curve was used to assess the performance of the GALAD HCC diagnosis. The survival probability was explored using the non-parametric test, and the equality of survival amongst categories was assessed with the log-rank test. Results: Biomarkers were higher in the HCC group compared to cirrhosis. Kaplan–Meier survival probability analysis for individual GALAD categories revealed that a high GALAD level was associated with decreased survival during follow-up, and the difference between the curves was statistically significant (p = 0.01). Conclusions: Our findings suggest that the GALAD score has promise as a prognostic tool, with implications for improving patient management and treatment strategies for HCC. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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17 pages, 2705 KiB

Open AccessArticle

Combined Administration of Escitalopram Oxalate and Nivolumab Exhibits Synergistic Growth-Inhibitory Effects on Liver Cancer Cells through Inducing Apoptosis

by Vincent Chin-Hung Chen, Shao-Lan Huang, Jing-Yu Huang, Tsai-Ching Hsu, Bor-Show Tzang and Roger S. McIntyre

Int. J. Mol. Sci. 2023, 24(16), 12630; https://doi.org/10.3390/ijms241612630 - 10 Aug 2023

Viewed by 1674

Abstract

Liver cancer is one of the most lethal malignant cancers worldwide. However, the therapeutic options for advanced liver cancers are limited and reveal scant efficacy. The current study investigated the effects of nivolumab (Niv) and escitalopram oxalate (Esc) in combination on proliferation of liver cancer cells both in vitro and in vivo. Significantly decreased viability of HepG2 cells that were treated with Esc or Niv was observed in a dose-dependent manner at 24 h, 48 h, and 72 h. Administration of Esc (50 μM) + Niv (20 μM), Esc (75 μM) + Niv (5 μM), and Esc (75 μM) + Niv (20 μM) over 24 h exhibited synergistic effects, inhibiting the survival of HepG2 cells. Additionally, treatment with Esc (50 μM) + Niv (1 μM), Esc (50 μM) + Niv (20 μM), and Esc (75 μM) + Niv (20 μM) over 48 h exhibited synergistic effects, inhibiting the survival of HepG2 cells. Finally, treatment with Esc (50 μM) + Niv (1 μM), Esc (50 μM) + Niv (20 μM), and Esc (75 μM) + Niv (20 μM) for 72 h exhibited synergistic effects, inhibiting HepG2 survival. Com-pared with controls, HepG2 cells treated with Esc (50 μM) + Niv (20 μM) exhibited significantly increased sub-G1 portion and annexin-V signals. In a xenograft animal study, Niv (6.66 mg/kg) + Esc (2.5 mg/kg) significantly suppressed the growth of xenograft HepG2 tumors in nude mice. This study reports for the first time the synergistic effects of combined administration of Niv and Esc for inhibiting HepG2 cell proliferation, which may provide an alternative option for liver cancer treatment. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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16 pages, 3673 KiB

Open AccessArticle

Treatment with a Cholecystokinin Receptor Antagonist, Proglumide, Improves Efficacy of Immune Checkpoint Antibodies in Hepatocellular Carcinoma

by Narayan Shivapurkar, Martha D. Gay, Aiwu (Ruth) He, Wenqiang Chen, Shermineh Golnazar, Hong Cao, Tetyana Duka, Bhaskar Kallakury, Sona Vasudevan and Jill P. Smith

Int. J. Mol. Sci. 2023, 24(4), 3625; https://doi.org/10.3390/ijms24043625 - 11 Feb 2023

Cited by 1 | Viewed by 2019

Abstract

Hepatocellular carcinoma (HCC) is the third leading cause of cancer-associated deaths worldwide. Treatment with immune checkpoint antibodies has shown promise in advanced HCC, but the response is only 15–20%. We discovered a potential target for the treatment of HCC, the cholecystokinin-B receptor (CCK-BR). This receptor is overexpressed in murine and human HCC and not in normal liver tissue. Mice bearing syngeneic RIL-175 HCC tumors were treated with phosphate buffer saline (PBS; control), proglumide (a CCK-receptor antagonist), an antibody to programmed cell death protein 1 (PD-1Ab), or the combination of proglumide and the PD-1Ab. In vitro, RNA was extracted from untreated or proglumide-treated murine Dt81Hepa1-6 HCC cells and analyzed for expression of fibrosis-associated genes. RNA was also extracted from human HepG2 HCC cells or HepG2 cells treated with proglumide and subjected to RNA sequencing. Results showed that proglumide decreased fibrosis in the tumor microenvironment and increased the number of intratumoral CD8+ T cells in RIL-175 tumors. When proglumide was given in combination with the PD-1Ab, there was a further significant increase in intratumoral CD8+ T cells, improved survival, and alterations in genes regulating tumoral fibrosis and epithelial-to-mesenchymal transition. RNAseq results from human HepG2 HCC cells treated with proglumide showed significant changes in differentially expressed genes involved in tumorigenesis, fibrosis, and the tumor microenvironment. The use of the CCK receptor antagonist may improve efficacy of immune checkpoint antibodies and survival in those with advanced HCC. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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Review

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20 pages, 355 KiB

Open AccessReview

Radiation and Immune Checkpoint Inhibitors: Combination Therapy for Treatment of Hepatocellular Carcinoma

by Perla Chami, Youssef Diab, Danny N. Khalil, Hassan Azhari, William R. Jarnagin, Ghassan K. Abou-Alfa, James J. Harding, Joseph Hajj, Jennifer Ma, Maria El Homsi, Marsha Reyngold, Christopher Crane and Carla Hajj

Int. J. Mol. Sci. 2023, 24(23), 16773; https://doi.org/10.3390/ijms242316773 - 26 Nov 2023

Cited by 1 | Viewed by 1601

Abstract

The liver tumor immune microenvironment has been thought to possess a critical role in the development and progression of hepatocellular carcinoma (HCC). Despite the approval of immune checkpoint inhibitors (ICIs), such as programmed cell death receptor 1 (PD-1)/programmed cell death ligand 1 (PD-L1) and cytotoxic T lymphocyte associated protein 4 (CTLA-4) inhibitors, for several types of cancers, including HCC, liver metastases have shown evidence of resistance or poor response to immunotherapies. Radiation therapy (RT) has displayed evidence of immunosuppressive effects through the upregulation of immune checkpoint molecules post-treatment. However, it was revealed that the limitations of ICIs can be overcome through the use of RT, as it can reshape the liver immune microenvironment. Moreover, ICIs are able to overcome the RT-induced inhibitory signals, effectively restoring anti-tumor activity. Owing to the synergetic effect believed to arise from the combination of ICIs with RT, several clinical trials are currently ongoing to assess the efficacy and safety of this treatment for patients with HCC. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

22 pages, 2471 KiB

Open AccessReview

Predicting Outcomes of Atezolizumab and Bevacizumab Treatment in Patients with Hepatocellular Carcinoma

by Ji Won Han and Jeong Won Jang

Int. J. Mol. Sci. 2023, 24(14), 11799; https://doi.org/10.3390/ijms241411799 - 22 Jul 2023

Cited by 3 | Viewed by 2329

Abstract

A combination of atezolizumab with bevacizumab (AB) is the first regimen that has shown superiority compared to sorafenib and is now being used as the systemic treatment of choice for hepatocellular carcinoma (HCC) patients with Barcelona Liver Cancer Clinic stage C. However, a considerable number of patients do not achieve survival or significant responses, indicating the need to identify predictive biomarkers for initial and on-treatment decisions in HCC patients receiving AB. In this manuscript, we summarized the current data from both experimental and clinical studies. This review will be beneficial for both clinicians and researchers in clinical practice as well as those designing experimental, translational, or clinical studies. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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21 pages, 1638 KiB

Open AccessReview

The Synergistic Effect of Interventional Locoregional Treatments and Immunotherapy for the Treatment of Hepatocellular Carcinoma

by Nicolò Brandi and Matteo Renzulli

Int. J. Mol. Sci. 2023, 24(10), 8598; https://doi.org/10.3390/ijms24108598 - 11 May 2023

Cited by 7 | Viewed by 2550

Abstract

Immunotherapy has remarkably revolutionized the management of advanced HCC and prompted clinical trials, with therapeutic agents being used to selectively target immune cells rather than cancer cells. Currently, there is great interest in the possibility of combining locoregional treatments with immunotherapy for HCC, as this combination is emerging as an effective and synergistic tool for enhancing immunity. On the one hand, immunotherapy could amplify and prolong the antitumoral immune response of locoregional treatments, improving patients’ outcomes and reducing recurrence rates. On the other hand, locoregional therapies have been shown to positively alter the tumor immune microenvironment and could therefore enhance the efficacy of immunotherapy. Despite the encouraging results, many unanswered questions still remain, including which immunotherapy and locoregional treatment can guarantee the best survival and clinical outcomes; the most effective timing and sequence to obtain the most effective therapeutic response; and which biological and/or genetic biomarkers can be used to identify patients likely to benefit from this combined approach. Based on the current reported evidence and ongoing trials, the present review summarizes the current application of immunotherapy in combination with locoregional therapies for the treatment of HCC, and provides a critical evaluation of the current status and future directions. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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30 pages, 795 KiB

Open AccessReview

Synergistic Nanomedicine: Photodynamic, Photothermal and Photoimmune Therapy in Hepatocellular Carcinoma: Fulfilling the Myth of Prometheus?

by Laura Marinela Ailioaie, Constantin Ailioaie and Gerhard Litscher

Int. J. Mol. Sci. 2023, 24(9), 8308; https://doi.org/10.3390/ijms24098308 - 5 May 2023

Cited by 2 | Viewed by 2107

Abstract

Hepatocellular carcinoma (HCC) is the most common type of primary liver cancer, with high morbidity and mortality, which seriously threatens the health and life expectancy of patients. The traditional methods of treatment by surgical ablation, radiotherapy, chemotherapy, and more recently immunotherapy have not given the expected results in HCC. New integrative combined therapies, such as photothermal, photodynamic, photoimmune therapy (PTT, PDT, PIT), and smart multifunctional platforms loaded with nanodrugs were studied in this review as viable solutions in the synergistic nanomedicine of the future. The main aim was to reveal the latest findings and open additional avenues for accelerating the adoption of innovative approaches for the multi-target management of HCC. High-tech experimental medical applications in the molecular and cellular research of photosensitizers, novel light and laser energy delivery systems and the features of photomedicine integration via PDT, PTT and PIT in immuno-oncology, from bench to bedside, were introspected. Near-infrared PIT as a treatment of HCC has been developed over the past decade based on novel targeted molecules to selectively suppress cancer cells, overcome immune blocking barriers, initiate a cascade of helpful immune responses, and generate distant autoimmune responses that inhibit metastasis and recurrences, through high-tech and intelligent real-time monitoring. The process of putting into effect new targeted molecules and the intelligent, multifunctional solutions for therapy will bring patients new hope for a longer life or even a cure, and the fulfillment of the myth of Prometheus. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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27 pages, 1165 KiB

Open AccessReview

Predictive Biomarkers for Immune-Checkpoint Inhibitor Treatment Response in Patients with Hepatocellular Carcinoma

by Jun Ho Ji, Sang Yun Ha, Danbi Lee, Kamya Sankar, Ekaterina K. Koltsova, Ghassan K. Abou-Alfa and Ju Dong Yang

Int. J. Mol. Sci. 2023, 24(8), 7640; https://doi.org/10.3390/ijms24087640 - 21 Apr 2023

Cited by 5 | Viewed by 3894

Abstract

Hepatocellular carcinoma (HCC) has one of the highest mortality rates among solid cancers. Late diagnosis and a lack of efficacious treatment options contribute to the dismal prognosis of HCC. Immune checkpoint inhibitor (ICI)-based immunotherapy has presented a new milestone in the treatment of cancer. Immunotherapy has yielded remarkable treatment responses in a range of cancer types including HCC. Based on the therapeutic effect of ICI alone (programmed cell death (PD)-1/programmed death-ligand1 (PD-L)1 antibody), investigators have developed combined ICI therapies including ICI + ICI, ICI + tyrosine kinase inhibitor (TKI), and ICI + locoregional treatment or novel immunotherapy. Although these regimens have demonstrated increasing treatment efficacy with the addition of novel drugs, the development of biomarkers to predict toxicity and treatment response in patients receiving ICI is in urgent need. PD-L1 expression in tumor cells received the most attention in early studies among various predictive biomarkers. However, PD-L1 expression alone has limited utility as a predictive biomarker in HCC. Accordingly, subsequent studies have evaluated the utility of tumor mutational burden (TMB), gene signatures, and multiplex immunohistochemistry (IHC) as predictive biomarkers. In this review, we aim to discuss the current state of immunotherapy for HCC, the results of the predictive biomarker studies, and future direction. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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15 pages, 17654 KiB

Open AccessReview

Navigating through the PD-1/PDL-1 Landscape: A Systematic Review and Meta-Analysis of Clinical Outcomes in Hepatocellular Carcinoma and Their Influence on Immunotherapy and Tumor Microenvironment

by Muhammad Joan Ailia, Jeong Heo and So Young Yoo

Int. J. Mol. Sci. 2023, 24(7), 6495; https://doi.org/10.3390/ijms24076495 - 30 Mar 2023

Cited by 7 | Viewed by 2484

Abstract

This systematic review aimed to assess the prognostic significance of programmed cell death-ligand 1 (PDL-1) and programmed cell death protein 1 (PD-1) in hepatocellular carcinoma (HCC). Medline, EMBASE, and Cochrane Library database searches were conducted, revealing nine relevant cohort studies (seven PDL-1 and three PD-1). Our meta-analysis showed that PD-1/PDL-1 was a marker of poor survival, regardless of the assessment method (PD-1 overall survival (OS): hazard ratio (HR) 2.40; 95% confidence interval (CI), 1.30–4.42; disease-free survival (DFS): HR 2.12; 95% CI, 1.45–3.10; PDL-1: OS: HR 3.61; 95% CI, 2.75–4.75; and DFS: HR 2.74; 95% CI, 2.09–3.59). Additionally, high level of PD-1/PDL-1 expression was associated with aging, multiple tumors, high alpha-fetoprotein levels, and advanced Barcelona Clinic Liver Cancer stage. This high level significantly predicted a poor prognosis for HCC, suggesting that anti-PD-1 therapy is plausible for patients with HCC. Furthermore, HIF-1 induces PD-1 expression, and PD1^lowSOCS3^high is associated with a better prognosis. Taken together, combination therapy may be the key to effective immunotherapy. Thus, exploring other markers, such as HIF-1 and SOCS3, along with PD-1/PDL-1 immunotherapy, may lead to improved outcomes. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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39 pages, 1889 KiB

Open AccessReview

Updating the Clinical Application of Blood Biomarkers and Their Algorithms in the Diagnosis and Surveillance of Hepatocellular Carcinoma: A Critical Review

by Endrit Shahini, Giuseppe Pasculli, Antonio Giovanni Solimando, Claudio Tiribelli, Raffaele Cozzolongo and Gianluigi Giannelli

Int. J. Mol. Sci. 2023, 24(5), 4286; https://doi.org/10.3390/ijms24054286 - 21 Feb 2023

Cited by 12 | Viewed by 2924

Abstract

The most common primary liver cancer is hepatocellular carcinoma (HCC), and its mortality rate is increasing globally. The overall 5-year survival of patients with liver cancer is currently 10–20%. Moreover, because early diagnosis can significantly improve prognosis, which is highly correlated with tumor stage, early detection of HCC is critical. International guidelines advise using α-FP biomarker with/without ultrasonography for HCC surveillance in patients with advanced liver disease. However, traditional biomarkers are sub-optimal for risk stratification of HCC development in high-risk populations, early diagnosis, prognostication, and treatment response prediction. Since about 20% of HCCs do not produce α-FP due to its biological diversity, combining α-FP with novel biomarkers can enhance HCC detection sensitivity. There is a chance to offer promising cancer management methods in high-risk populations by utilizing HCC screening strategies derived from new tumor biomarkers and prognostic scores created by combining biomarkers with distinct clinical parameters. Despite numerous efforts to identify molecules as potential biomarkers, there is no single ideal marker in HCC. When combined with other clinical parameters, the detection of some biomarkers has higher sensitivity and specificity in comparison with a single biomarker. Therefore, newer biomarkers and models, such as the Lens culinaris agglutinin-reactive fraction of Alpha-fetoprotein (α-FP), α-FP-L3, Des-γ-carboxy-prothrombin (DCP or PIVKA-II), and the GALAD score, are being used more frequently in the diagnosis and prognosis of HCC. Notably, the GALAD algorithm was effective in HCC prevention, particularly for cirrhotic patients, regardless of the cause of their liver disease. Although the role of these biomarkers in surveillance is still being researched, they may provide a more practical alternative to traditional imaging-based surveillance. Finally, looking for new diagnostic/surveillance tools may help improve patients’ survival. This review discusses the current roles of the most used biomarkers and prognostic scores that may aid in the clinical management of HCC patients. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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15 pages, 1022 KiB

Open AccessReview

FDA-Approved Monoclonal Antibodies for Unresectable Hepatocellular Carcinoma: What Do We Know So Far?

by Iason Psilopatis, Christos Damaskos, Anna Garmpi, Panagiotis Sarantis, Evangelos Koustas, Efstathios A. Antoniou, Dimitrios Dimitroulis, Gregory Kouraklis, Michail V. Karamouzis, Kleio Vrettou, Georgios Marinos, Konstantinos Kontzoglou and Nikolaos Garmpis

Int. J. Mol. Sci. 2023, 24(3), 2685; https://doi.org/10.3390/ijms24032685 - 31 Jan 2023

Cited by 6 | Viewed by 3599

Abstract

Unresectable hepatocellular carcinoma (HCC) is an advanced primary liver malignancy with a poor prognosis. The Food and Drug Administration (FDA) has, to date, approved nivolumab, pembrolizumab, ramucirumab, nivolumab/ipilimumab, atezolizumab/bevacizumab, as well as tremelimumab/durvalumab, as first- or second-line monoclonal antibodies (mAbs) for unresectable HCC. The present review examines the current state of knowledge, and provides a useful update on the safety and efficacy of these therapeutic agents, thus attempting to define the suitability of each mAb for different patient subgroups. Full article

(This article belongs to the Special Issue Challenges and Future Trends of Hepatocellular Carcinoma Immunotherapy)

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