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Junxiao W, Rui L, Zhenyu W, Zejie S, Xiang Y, Mingchao D, Hui X. Adjuvant sorafenib for hepatocellular carcinoma after radiofrequency ablation versus radiofrequency ablation: analysis of its efficacy and safety. Front Oncol 2024; 14:1383312. [PMID: 39697221 PMCID: PMC11652347 DOI: 10.3389/fonc.2024.1383312] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/07/2024] [Accepted: 11/18/2024] [Indexed: 12/20/2024] Open
Abstract
Objectives For the treatment of early hepatocellular carcinoma, we compared the efficacy and safety of radiofrequency ablation (RFA) alone and radiofrequency ablation combined with sorafenib (RFA+Sor). Methods A total of 164 patients with early HCC were included in the study. There were 87 patients who underwent RFA alone, and 77 patients who underwent RFA+Sor treatment. Overall survival (OS) was the primary endpoint of the study, and recurrence-free survival (RFS) and safety were the secondary endpoints. Results According to the RFA group, the RFS rates were 74.7%, 29.9%, and 11.5% at 1, 2, and 3 years, whereas in the RFA+Sor group, the RFS rates were 72.7%, 19.5%, and 11.7% at 1, 2, and 3 years (P>0.05). RFA and RFA+Sor groups had median OS of 35.0 and 41.0 months, respectively (P>0.05). For the RFA and RFA+Sor groups, the median RFS was 17.0 and 16.0 months, respectively (P>0.05). Based on the univariate regression analysis, there was no statistically significant difference between the subgroups (P>0.05). Skin rashes only occurred in the RFA+Sor group, and other adverse effects were not significantly different between the two groups (P>0.05). Conclusions Treatment with RFA+Sor treatment did not result in a longer OS than treatment with only RFA, however, the adverse effects of adjuvant Sorafenib were acceptable.
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Affiliation(s)
- Wang Junxiao
- Aerospace Medical Center, Aerospace Center Hospital, Beijing, China
- Senior Department of Oncology, Fifth Medical Center of Chinese PLA General Hospital, Beijing, China
| | - Liu Rui
- Department of Interventional Vascular Surgery, Aerospace Center Hospital, Beijing, China
| | - Wen Zhenyu
- Senior Department of Oncology, Fifth Medical Center of Chinese PLA General Hospital, Beijing, China
| | - Sang Zejie
- Senior Department of Oncology, Fifth Medical Center of Chinese PLA General Hospital, Beijing, China
| | - Yang Xiang
- Senior Department of Oncology, Fifth Medical Center of Chinese PLA General Hospital, Beijing, China
| | - Ding Mingchao
- Department of Interventional Vascular Surgery, Aerospace Center Hospital, Beijing, China
| | - Xie Hui
- Senior Department of Oncology, Fifth Medical Center of Chinese PLA General Hospital, Beijing, China
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2
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Cao WH, Zhang YQ, Li XX, Zhang ZY, Li MH. Advances in immunotherapy for hepatitis B virus associated hepatocellular carcinoma patients. World J Hepatol 2024; 16:1158-1168. [PMID: 39474576 PMCID: PMC11514615 DOI: 10.4254/wjh.v16.i10.1158] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/18/2024] [Revised: 08/28/2024] [Accepted: 09/19/2024] [Indexed: 10/21/2024] Open
Abstract
Hepatitis B virus (HBV) infection plays an important role in the occurrence and development of hepatocellular carcinoma (HCC), and the rate of HBV infection in liver cancer patients in China is as high as 92.05%. Due to long-term exposure to chronic antigens from the gut, the liver needs to maintain a certain level of immune tolerance, both to avoid severe inflammation caused by non-pathogenic antigens and to maintain the possibility of rapid and violent responses to infection and tumors. Therefore, HBV infection interacts with the tumor microenvironment (TME) through a highly complex and intertwined signaling pathway, which results in a special TME in HCC. Due to changes in the TME, tumor cells can evade immune surveillance by inhibiting tumor-specific T cell function through cytotoxic T-lymphocy-associated protein-4 (CTLA-4) and programmed cell death 1 (PD-1)/programmed cell death ligand 1 (PD-L1). Interferons, as a class of immune factors with strong biological activity, can improve the TME of HBV-HCC through various pathways. In recent years, the systematic treatment of HCC has gradually come out of the dilemma. In addition to the continuous emergence of new multi-target anti-vascular tyrosine kinase inhibitor drugs, immune checkpoint inhibitors have opened up a new avenue for the systematic treatment of HCC. At present, immunotherapy based on PD-1/L1 inhibitors has gradually become a new direction of systematic treatment for HCC, and the disease characteristics of patients included in global clinical studies are different from those of Chinese patients. Therefore, whether a group of HCC patients with HBV background and poor prognosis in China can also benefit from immunotherapy is an issue of wide concern. This review aims to elucidate the advances of immunotherapy for HBV related HCC patients with regard to: (1) Immunotherapy based on interferons; (2) Immunotherapy based on PD-1/L1 inhibitors; (3) Immunotherapy based on CTLA4 inhibitors; (4) Adoptive cell transfer; (5) Combination immunotherapy strategy; and (6) Shortcomings of immunotherapy.
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Affiliation(s)
- Wei-Hua Cao
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Ya-Qin Zhang
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Xin-Xin Li
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Zi-Yu Zhang
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Ming-Hui Li
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Peking University Ditan Teaching Hospital, Beijing 100015, China
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3
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Cao WH, Zhang YQ, Li XX, Zhang ZY, Li MH. Advances in immunotherapy for hepatitis B virus associated hepatocellular carcinoma patients. World J Hepatol 2024; 16:1338-1348. [DOI: 10.4254/wjh.v16.i10.1338] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/18/2024] [Revised: 08/28/2024] [Accepted: 09/19/2024] [Indexed: 11/22/2024] Open
Abstract
Hepatitis B virus (HBV) infection plays an important role in the occurrence and development of hepatocellular carcinoma (HCC), and the rate of HBV infection in liver cancer patients in China is as high as 92.05%. Due to long-term exposure to chronic antigens from the gut, the liver needs to maintain a certain level of immune tolerance, both to avoid severe inflammation caused by non-pathogenic antigens and to maintain the possibility of rapid and violent responses to infection and tumors. Therefore, HBV infection interacts with the tumor microenvironment (TME) through a highly complex and intertwined signaling pathway, which results in a special TME in HCC. Due to changes in the TME, tumor cells can evade immune surveillance by inhibiting tumor-specific T cell function through cytotoxic T-lymphocy-associated protein-4 (CTLA-4) and programmed cell death 1 (PD-1)/programmed cell death ligand 1 (PD-L1). Interferons, as a class of immune factors with strong biological activity, can improve the TME of HBV-HCC through various pathways. In recent years, the systematic treatment of HCC has gradually come out of the dilemma. In addition to the continuous emergence of new multi-target anti-vascular tyrosine kinase inhibitor drugs, immune checkpoint inhibitors have opened up a new avenue for the systematic treatment of HCC. At present, immunotherapy based on PD-1/L1 inhibitors has gradually become a new direction of systematic treatment for HCC, and the disease characteristics of patients included in global clinical studies are different from those of Chinese patients. Therefore, whether a group of HCC patients with HBV background and poor prognosis in China can also benefit from immunotherapy is an issue of wide concern. This review aims to elucidate the advances of immunotherapy for HBV related HCC patients with regard to: (1) Immunotherapy based on interferons; (2) Immunotherapy based on PD-1/L1 inhibitors; (3) Immunotherapy based on CTLA4 inhibitors; (4) Adoptive cell transfer; (5) Combination immunotherapy strategy; and (6) Shortcomings of immunotherapy.
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Affiliation(s)
- Wei-Hua Cao
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Ya-Qin Zhang
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Xin-Xin Li
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Zi-Yu Zhang
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
| | - Ming-Hui Li
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Beijing 100015, China
- Department of Hepatology Division 2, Beijing Ditan Hospital, Capital Medical University, Peking University Ditan Teaching Hospital, Beijing 100015, China
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Yang YQ, Wen ZY, Liu XY, Ma ZH, Liu YE, Cao XY, Hou L, Xie H. Current status and prospect of treatments for recurrent hepatocellular carcinoma. World J Hepatol 2023; 15:129-150. [PMID: 36926237 PMCID: PMC10011906 DOI: 10.4254/wjh.v15.i2.129] [Citation(s) in RCA: 11] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/18/2022] [Revised: 11/13/2022] [Accepted: 01/23/2023] [Indexed: 02/24/2023] Open
Abstract
Owing to its heterogeneous and highly aggressive nature, hepatocellular carcinoma (HCC) has a high recurrence rate, which is a non-negligible problem despite the increasing number of available treatment options. Recent clinical trials have attempted to reduce the recurrence and develop innovative treatment options for patients with recurrent HCC. In the event of liver remnant recurrence, the currently available treatment options include repeat hepatectomy, salvage liver transplantation, tumor ablation, transcatheter arterial chemoembolization, stereotactic body radiotherapy, systemic therapies, and combination therapy. In this review, we summarize the strategies to reduce the recurrence of high-risk tumors and aggressive therapies for recurrent HCC. Additionally, we discuss methods to prevent HCC recurrence and prognostic models constructed based on predictors of recurrence to develop an appropriate surveillance program.
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Affiliation(s)
- Yu-Qing Yang
- Department of Epidemiology and Biostatistics, Jilin University, Changchun 130021, Jilin Province, China
| | - Zhen-Yu Wen
- Department of Occupational and Environmental Health, Jilin University, Changchun 130021, Jilin Province, China
| | - Xiao-Yan Liu
- Senior Department of Hepatology, The Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
| | - Zhen-Hu Ma
- Senior Department of Oncology, The Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
| | - Yan-E Liu
- Department of Epidemiology and Biostatistics, Jilin University, Changchun 130021, Jilin Province, China
| | - Xue-Ying Cao
- Senior Department of Oncology, The Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
| | - Li Hou
- Senior Department of Oncology, The Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
| | - Hui Xie
- Senior Department of Oncology, The Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
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Guo B, Chen Q, Liu Z, Chen X, Zhu P. Adjuvant therapy following curative treatments for hepatocellular carcinoma: current dilemmas and prospects. Front Oncol 2023; 13:1098958. [PMID: 37139151 PMCID: PMC10149944 DOI: 10.3389/fonc.2023.1098958] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/15/2022] [Accepted: 04/04/2023] [Indexed: 05/05/2023] Open
Abstract
Curative surgical treatments, mainly liver resection, are still one of the optimal options for patients with early-, mid-, and even progression-stage hepatocellular carcinoma (HCC). However, the recurrence rate within 5 years after surgery is as high as 70%, especially in patients with high risk factors for recurrence, most of whom experience early recurrence within 2 years. Effective adjuvant therapy may improve prognosis, previous studies found that adjuvant transarterial chemoembolization, antiviral, and traditional Chinese medicine et al. were helpful in preventing HCC recurrence. Nevertheless, due to controversial results or lack of high-level evidence, there is no standardized postoperative management protocol worldwide at present. Continued exploration of effective postoperative adjuvant treatments to improve surgical prognosis is necessary.
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Affiliation(s)
- Bin Guo
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
| | - Qian Chen
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
- Hepatobiliary Surgery Department, The First Affiliated Hospital of Shihezi University, Shihezi, Xinjiang, China
| | - Zhicheng Liu
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
| | - Xiaoping Chen
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
| | - Peng Zhu
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
- *Correspondence: Peng Zhu,
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Hu J, Gong N, Li D, Deng Y, Chen J, Luo D, Zhou W, Xu K. Identifying hepatocellular carcinoma patients with survival benefits from surgery combined with chemotherapy: based on machine learning model. World J Surg Oncol 2022; 20:377. [PMID: 36451200 PMCID: PMC9714169 DOI: 10.1186/s12957-022-02837-2] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/17/2022] [Accepted: 10/03/2022] [Indexed: 12/03/2022] Open
Abstract
BACKGROUND Hepatocellular carcinoma (HCC) is still fatal even after surgical resection. The purpose of this study was to analyze the prognostic factors of 5-year survival rate and to establish a model to identify HCC patients with gain of surgery combined with chemotherapy. METHODS All patients with HCC after surgery from January 2010 to December 2015 were selected from the Surveillance, Epidemiology, and End Results (SEER) database. Univariate and multivariate logistic analysis were used to analyze the prognostic factors of patients, and the risk prediction model of 5-year survival rate of HCC patients was established by classical decision tree method. Propensity score matching was used to eliminate the confounding factors of whether to receive chemotherapy in high-risk group or low-risk group. RESULTS One-thousand six-hundred twenty-five eligible HCC patients were included in the study. Marital status, α-fetoprotein (AFP), vascular infiltration, tumor size, number of lesions, and grade were independent prognostic factors affecting the 5-year survival rate of HCC patients. The area under the curve of the 5-year survival risk prediction model constructed from the above variables was 0.76, and the classification accuracy, precision, recall, and F1 scores were 0.752, 0.83, 0.842, and 0.836, respectively. High-risk patients classified according to the prediction model had better 5-year survival rate after chemotherapy, while there was no difference in 5-year survival rate between patients receiving chemotherapy and patients not receiving chemotherapy in the low-risk group. CONCLUSIONS The 5-year survival risk prediction model constructed in this study provides accurate survival prediction information. The high-risk patients determined according to the prediction model may benefit from the 5-year survival rate after combined chemotherapy.
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Affiliation(s)
- Jie Hu
- Department of Gastrointestinal Surgery, The Third Xiangya Hospital of Central South University, Changsha, Hunan, China
| | - Ni Gong
- Department of Nursing, The Third Xiangya Hospital of Central South University, Changsha, Hunan, China
| | - Dan Li
- Department of Gastrointestinal Surgery, The Third Xiangya Hospital of Central South University, Changsha, Hunan, China
| | - Youyuan Deng
- Department of General Surgery, The Central Hospital of Xiangtan City, Xiangtan, Hunan, China
| | - Jiawei Chen
- Department of Rehabilitation, The Central Hospital of Xiangtan City, Xiangtan, Hunan, China
| | - Dingan Luo
- Department of Hepatobiliary and Pancreatic Surgery, Affiliated Hospital of Qingdao University, Qingdao, China
| | - Wei Zhou
- Clinical Medical College, Chengdu Medical College, Chengdu, Sichuan, China.
- Department of Radiology, The First Affiliated Hospital of Chengdu Medical College, Chengdu, Sichuan, China.
| | - Ke Xu
- Clinical Medical College, Chengdu Medical College, Chengdu, Sichuan, China.
- Department of Oncology, The First Affiliated Hospital of Chengdu Medical College, Chengdu, Sichuan, China.
- Key Clinical Specialty of Sichuan Province, Chengdu, Sichuan, China.
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Şenol Y, Kaplan O, Varan C, Demirtürk N, Öncül S, Fidan BB, Ercan A, Bilensoy E, Çelebier M. Pharmacometabolomic assessment of vitamin E loaded human serum albumin nanoparticles on HepG2 cancer cell lines. J Drug Deliv Sci Technol 2022. [DOI: 10.1016/j.jddst.2022.104017] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/24/2022]
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Zeng ZM, Mo N, Zeng J, Ma FC, Jiang YF, Huang HS, Liao XW, Zhu GZ, Ma J, Peng T. Advances in postoperative adjuvant therapy for primary liver cancer. World J Gastrointest Oncol 2022; 14:1604-1621. [PMID: 36187393 PMCID: PMC9516643 DOI: 10.4251/wjgo.v14.i9.1604] [Citation(s) in RCA: 19] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/29/2021] [Revised: 05/13/2022] [Accepted: 07/26/2022] [Indexed: 02/05/2023] Open
Abstract
Hepatocellular carcinoma (HCC) is a highly heterogeneous, invasive, and conventional chemotherapy-insensitive tumor with unique biological characteristics. The main methods for the radical treatment of HCC are surgical resection or liver transplantation. However, recurrence rates are as high as 50% and 70% at 3 and 5 years after liver resection, respectively, and even in Milan-eligible recipients, the recurrence rate is approximately 20% at 5 years after liver transplantation. Therefore, reducing the postoperative recurrence rate is key to improving the overall outcome of liver cancer. This review discusses the risk factors for recurrence in patients with HCC radical surgical resection and adjuvant treatment options that may reduce the risk of recurrence and improve overall survival, including local adjuvant therapy (e.g., transcatheter arterial chemoembolization), adjuvant systemic therapy (e.g., molecular targeted agents and immunotherapy), and other adjuvant therapies (e.g., antiviral and herbal therapy). Finally, potential research directions that may change the paradigm of adjuvant therapy for HCC are analyzed.
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Affiliation(s)
- Zhi-Ming Zeng
- Department of Medical Oncology, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Ning Mo
- Department of Medical Oncology, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Jie Zeng
- Department of Medical Oncology, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Fu-Chao Ma
- Department of Medical Oncology, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Yan-Feng Jiang
- Department of Medical Oncology, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Hua-Sheng Huang
- Department of Hepatobiliary Surgery, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Xi-Wen Liao
- Department of Hepatobiliary Surgery, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Guang-Zhi Zhu
- Department of Hepatobiliary Surgery, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Jie Ma
- Department of Medical Oncology, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Tao Peng
- Department of Hepatobiliary Surgery, The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
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Zhang X, Guan L, Tian H, Zeng Z, Chen J, Huang D, Sun J, Guo J, Cui H, Li Y. Risk Factors and Prevention of Viral Hepatitis-Related Hepatocellular Carcinoma. Front Oncol 2021; 11:686962. [PMID: 34568017 PMCID: PMC8458967 DOI: 10.3389/fonc.2021.686962] [Citation(s) in RCA: 21] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2021] [Accepted: 08/20/2021] [Indexed: 12/11/2022] Open
Abstract
Hepatocellular carcinoma (HCC) is a common cancer in the world, and its incidence is increasing yearly. Hepatitis B virus (HBV) infection and hepatitis C virus (HCV) infection are important causes of HCC. Liver cirrhosis, age, sex, smoking and drinking, and metabolic risk factors will increase the risk of cancer in HBV/HCV patients. And viral load, APRI, FIB-4, and liver stiffness can all predict the risk of HCC in patients with viral infection. In addition, effective prevention strategies are essential in reducing the risk of HCC. The prevention of HCC involves mainly tertiary prevention strategies, while the primary prevention is based on standardized vaccine injections to prevent the occurrence of HBV/HCV. Eliminating the route of transmission and vaccination will lead to a decrease in the incidence of HCC. Secondary prevention involves effective antiviral treatment of HBV/HCV to prevent the disease from progressing to HCC, and tertiary prevention is actively treating HCC to prevent its recurrence.
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Affiliation(s)
- Xinhe Zhang
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Lin Guan
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Haoyu Tian
- The 3rd Clinical Department of China Medical University, Shenyang, China
| | - Zilu Zeng
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Jiayu Chen
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Die Huang
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Ji Sun
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Jiaqi Guo
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Huipeng Cui
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
| | - Yiling Li
- Gastroenterology Department, The First Affiliated Hospital of China Medical University, Shenyang, China
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Zhang W, Zhang B, Chen XP. Adjuvant treatment strategy after curative resection for hepatocellular carcinoma. Front Med 2021; 15:155-169. [PMID: 33754281 DOI: 10.1007/s11684-021-0848-3] [Citation(s) in RCA: 60] [Impact Index Per Article: 15.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/09/2020] [Accepted: 02/20/2021] [Indexed: 01/27/2023]
Abstract
Hepatic resection represents the first-line treatment for patients with resectable hepatocellular carcinoma (HCC). However, the 5-year recurrence rates of HCC after surgery have been reported to range from 50% to 70%. In this review, we evaluated the available evidence for the efficiency of adjuvant treatments to prevent HCC recurrence after curative liver resection. Antiviral therapy has potential advantages in terms of reducing the recurrence rate and improving the overall survival (OS) and/or disease-free survival of patients with hepatitis-related HCC. Postoperative adjuvant transarterial chemoembolization can significantly reduce the intrahepatic recurrence rate and improve OS, especially for patients with a high risk of recurrence. The efficacy of molecular targeted drugs as an adjuvant therapy deserves further study. Adjuvant adoptive immunotherapy can significantly improve the clinical prognosis in the early stage. Randomized controlled trial (RCT) studies evaluating adjuvant immune checkpoint inhibitors are ongoing, and the results are highly expected. Adjuvant hepatic artery infusion chemotherapy might be beneficial in patients with vascular invasion. Huaier granule, a traditional Chinese medicine, has been proved to be effective in prolonging the recurrence-free survival and reducing extrahepatic recurrence. The efficiency of other adjuvant treatments needs to be further confirmed by large RCT studies.
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Affiliation(s)
- Wei Zhang
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China
| | - Bixiang Zhang
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China.
| | - Xiao-Ping Chen
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China.
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Lu SD, Li L, Liang XM, Chen W, Chen FL, Fan LL, Ahir BK, Zhang WG, Zhong JH. Updates and advancements in the management of hepatocellular carcinoma patients after hepatectomy. Expert Rev Gastroenterol Hepatol 2019; 13:1077-1088. [PMID: 31648568 DOI: 10.1080/17474124.2019.1684898] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/12/2019] [Accepted: 10/21/2019] [Indexed: 02/07/2023]
Abstract
Introduction: The 5-year recurrence rate of hepatocellular carcinoma (HCC) after hepatic resection or local ablation is up to 70%. Adjuvant therapies to prevent HCC recurrence have been reported but are not currently recommended by EASL or AASLD guidelines. This review examined evidence from randomized controlled trials, meta-analyses and systematic reviews on the safety and efficacy of adjuvant therapies and chemotherapies in HCC patients after resection or local ablation.Areas covered: PubMed was searched through 15 June 2019. Available evidence was assessed based on the GRADE system.Expert commentary: Transarterial chemoembolization is the best adjuvant therapy for HCC patients at high risk of recurrence, antiviral therapy with nucleoside analogs is effective for preventing recurrence of HBV-related HCC, and interferon-α is effective for preventing recurrence of HCV-related HCC. Further studies are needed to clarify the efficacy of adjuvant immune checkpoint inhibitors. Adjuvant sorafenib appears to offer negligible clinical benefit and high risk of adverse effects.
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Affiliation(s)
- Shi-Dong Lu
- Department of Hepatobiliary Surgery, the Third Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Lin Li
- Department of Hepatobiliary Surgery, the Third Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Xin-Min Liang
- Grade 2016, Basic medical college of Guangxi Medical University, Nanning, China
| | - Wu Chen
- Grade 2016, Basic medical college of Guangxi Medical University, Nanning, China
| | - Fu-Li Chen
- Grade 2016, Basic medical college of Guangxi Medical University, Nanning, China
| | - Lang-Lin Fan
- Grade 2016, Basic medical college of Guangxi Medical University, Nanning, China
| | - Bhavesh K Ahir
- Section of Hematology and Oncology, Department of Medicine, University of Illinois at Chicago, Chicago, IL, USA
| | - Wan-Guang Zhang
- Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Jian-Hong Zhong
- Department of Hepatobiliary Surgery, Affiliated Tumor Hospital of Guangxi Medical University, Nanning, China
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12
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Oncul S, Karakaya G, Dilsiz Aytemir M, Ercan A. A kojic acid derivative promotes intrinsic apoptotic pathway of hepatocellular carcinoma cells without incurring drug resistance. Chem Biol Drug Des 2019; 94:2084-2093. [PMID: 31495064 DOI: 10.1111/cbdd.13615] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/11/2019] [Revised: 06/09/2019] [Accepted: 08/03/2019] [Indexed: 12/14/2022]
Affiliation(s)
- Selin Oncul
- Department of Biochemistry Faculty of Pharmacy Hacettepe University Ankara Turkey
| | - Gulsah Karakaya
- Department of Pharmaceutical Chemistry Faculty of Pharmacy Hacettepe University Ankara Turkey
| | - Mutlu Dilsiz Aytemir
- Department of Pharmaceutical Chemistry Faculty of Pharmacy Hacettepe University Ankara Turkey
| | - Ayse Ercan
- Department of Biochemistry Faculty of Pharmacy Hacettepe University Ankara Turkey
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Barber FD. Adverse Events of Oncologic Immunotherapy and Their Management. Asia Pac J Oncol Nurs 2019; 6:212-226. [PMID: 31259216 PMCID: PMC6518984 DOI: 10.4103/apjon.apjon_6_19] [Citation(s) in RCA: 22] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/21/2018] [Accepted: 02/10/2019] [Indexed: 12/26/2022] Open
Abstract
Over the past two decades, immunotherapy has emerged as a promising treatment option for patients with cancer. However, newer versions of immunotherapy, such as checkpoint inhibitors, may be associated with unusual adverse effects (AEs) that can range in severity from mild to life-threatening. Unlike common AEs of conventional chemotherapy, which have a predictable nadir or cyclic pattern after administration, AEs of these newer immunotherapies are variable, depending on the type of immunotherapy, route of administration, and mechanism of action. The onset and resolution of these AEs may be present at any time, during administration of treatment, a few weeks after administration of treatment, or several months after completion of treatment. Therefore, improving outcomes in patients undergoing oncologic immunotherapy requires oncology nurses' knowledge and understanding of various immunotherapy agents, as well as early recognition and management of potential AEs, especially AEs associated with checkpoint inhibitors and other therapies that manipulate T-cell activation causing autoimmune toxicity. This article draws upon current evidence from systematic reviews, meta-analyses, and expert consensus guidelines to provide a brief overview of common immunotherapies used in cancer and management of their associated AEs.
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Affiliation(s)
- Fedricker Diane Barber
- Department of Investigational Cancer Therapeutics (A Phase I Program), University of Texas MD Anderson Cancer Center, Houston, TX, USA
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14
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Xin M, Feng D, Yin B, Li Y. Efficacy of interferon therapy in patients with hepatitis B virus-related primary hepatic carcinoma after transcatheter arterial chemoembolization. PRECISION RADIATION ONCOLOGY 2018. [DOI: 10.1002/pro6.53] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/09/2022] Open
Affiliation(s)
- Meng Xin
- School of Medicine; Shandong University; Jinan China
- Department of Oncology; Shandong Provincial Qianfoshan Hospital; Jinan China
| | - Dongfeng Feng
- Department of Oncology; Shandong Provincial Qianfoshan Hospital; Jinan China
| | - Beibei Yin
- Department of Oncology; Shandong Provincial Qianfoshan Hospital; Jinan China
| | - Yan Li
- Department of Oncology; Shandong Provincial Qianfoshan Hospital; Jinan China
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15
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Wu J, Yin Z, Cao L, Xu X, Yan T, Liu C, Li D. Adjuvant pegylated interferon therapy improves the survival outcomes in patients with hepatitis-related hepatocellular carcinoma after curative treatment: A meta-analysis. Medicine (Baltimore) 2018; 97:e11295. [PMID: 29995763 PMCID: PMC6076097 DOI: 10.1097/md.0000000000011295] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/25/2017] [Accepted: 05/28/2018] [Indexed: 02/07/2023] Open
Abstract
BACKGROUND Hepatocellular carcinoma (HCC) is one of the most common cancers and the second leading cause of cancer-related deaths in men worldwide. Surgical resection of HCC remains the mainstay treatment procedure. As a result of hepatitis viral infection, the postoperative survival outcome in patients with HCC is not satisfactory. Recently, studies have reported that due to its treatment effect on hepatitis infection, pegylated interferon (Peg-IFN)-based therapy could improve the survival outcome after the treatment of hepatitis-related HCC. However, the postoperative effect of this regimen on the survival outcomes in patients with hepatitis-related HCC remains debatable. The present study conducted a meta-analysis to evaluate the effects of adjuvant Peg-IFN-based therapy on the survival outcomes in patients with hepatitis-related HCC after the curative treatment. METHODS A systematic search was conducted to identify studies on the survival outcomes in patients with hepatitis-related HCC after a curative treatment with adjuvant Peg-IFN. PubMed, EmBase, and Cochrane Library databases were searched until September 20, 2017. The retrieved studies were independently assessed by 2 reviewers, to identify the potentially eligible studies and extract data of interest. STATA software (Version 10.0, STATA Corporation, College Station, Texas) software was used for all statistical analyses. RESULTS The pooled results showed that adjuvant Peg-IFN-based therapy improved the 3- and 5-year recurrence-free survival (RFS) rates of patients with hepatitis-related HCC (3-year RFS, HR = 0.80; 95% CI: 0.64-0.99, P = .04; P = .81 for heterogeneity; 5-year RFS, HR = 0.82; 95% CI: 0.67-0.99, P = .04; P = .84 for heterogeneity). For the 5-year overall survival (OS) outcomes of Peg-IFN therapy for hepatitis-related HCC after the curative treatment, the pooled results showed a significant difference between the 2 groups (HR = 0.67; 95% CI: 0.47-0.97, P = .03; P = .99 for heterogeneity). CONCLUSIONS Adjuvant Peg-IFN-based therapy could improve the RFS and OS outcomes in patients after curative treatment of hepatitis-related HCC, with no severe adverse effects.
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Affiliation(s)
- Jiansong Wu
- Department of Infection Disease, General Hospital of the PLA Rocket Force
| | - Zhiwei Yin
- Department of Nephrology, Chinese PLA General Hospital, Chinese PLA Institute of Nephrology, State Key Laboratory of Kidney Diseases, National Clinical Research Center for Kidney Disease
| | - Liuxia Cao
- Department of Infection Disease, General Hospital of the PLA Rocket Force
| | - Xiaodan Xu
- Department of Infection Disease, General Hospital of the PLA Rocket Force
| | - Tao Yan
- Department of Hepatobiliary Surgery, General Hospital of the PLA Rocket Force
| | - Changting Liu
- Nanlou Respiratory Diseases Department, Chinese PLA General Hospital, Beijing, China
| | - Diangeng Li
- Nanlou Respiratory Diseases Department, Chinese PLA General Hospital, Beijing, China
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16
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Ramadori G, Bosio P, Moriconi F, Malik IA. Case report: 8 years after liver transplantation: de novo hepatocellular carcinoma 8 months after HCV clearance through IFN-free antiviral therapy. BMC Cancer 2018; 18:257. [PMID: 29510685 PMCID: PMC5840818 DOI: 10.1186/s12885-018-4175-2] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/04/2017] [Accepted: 03/01/2018] [Indexed: 12/14/2022] Open
Abstract
Background After orthotopic liver transplantation (OLT) for hepatocellular carcinoma (HCC), recurrent HCC mostly develops within 2 years. All cases of de novo HCC described so far occurred later than 2 years after OLT. Prevention of post-transplantation HCC has usually been tried to achieve by curing or controlling recurrent liver disease. This has been rationale for treatment with interferon (IFN)/ribavirin of HCV-recurrence in patients after OLT, transplanted for advanced HCV-induced liver disease and/or HCC. The availability of new and more efficient drugs has improved chances also for previously difficult-to-treat HCV-positive patients. Case presentation A 75 year-old male patient who had undergone OLT for decompensated HCV-cirrhosis in 2009, and bilio-digestive surgery in 2011 under tracrolimus (0.5 mg/day) and prednisone (5 mg/day) immunosuppressive therapy, started to receive antiviral treatment for recurrent HCV-infection of graft with 200 mg/day ribavirin in combination with ledipasvir and sofosbuvir by the end of October 2015. Because of multiple side effects (anemia, asthenia, infections, and reduction of kidney functions - palliated by treatment with erythropoietin), treatment was stopped after 16 weeks. At the third control, a minimal increase in alpha-fetoprotein (AFP) serum level to 10 μg/L was measured 8 months after therapy, whereas both liver sonography and serum transaminases were normal. The patient’s general condition; however, remained poor, and a magnetic resonance imaging (MRI) of abdomen was performed 2 months later. A nodule of 3 cm in diameter with a pseudocapsule was found centrally in the liver. The patient had to be hospitalized for recurrent infections of the lung, overt ascites and peritonitis. Rapid tumor growth (10 cm) was detected during last stay in hospital (April 2017), concomitant with a rise of AFP-serum levels to 91 μg/L. The family decided to take the patient home, and best supportive care was provided by a general practitioner, local nurses and the patient’s dedicated wife until his death. Conclusion Before treating OLT patients with HCV graft reinfection one should not only consider possible advantages of newly effective antiviral-therapies, but also life expectancy and possible side effects (difficult to manage at an outpatient service basis), including severe disadvantages such as the development of HCC.
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Affiliation(s)
- Giuliano Ramadori
- Department of Gastroenterology and Endocrinology, University Medical Center Goettingen, Robert-Koch-Street 40, D-37075, Goettingen, Germany.
| | - Patrizia Bosio
- General Practitioner, National health care system, Palazzago, BG, Italy
| | | | - Ihtzaz A Malik
- Institute of Anatomy and Cell Biology, University Medical Center, Kreuzbering 36, 37075, Goettingen, Germany
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17
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Cheng XS, Sun SB, Zhong F, He K, Zhou J. Knockdown of Histone Methyltransferase hSETD1A Inhibits Progression, Migration, and Invasion in Human Hepatocellular Carcinoma. Oncol Res 2017; 24:239-45. [PMID: 27656834 PMCID: PMC7838640 DOI: 10.3727/096504016x14648701448011] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/28/2022] Open
Abstract
Our aim was to study the expression of human SET domain containing protein 1A (hSETD1A) in hepatocellular carcinoma patients and its relationship with human hepatocellular carcinoma cell function. A total of 30 patients with hepatocellular carcinoma were enrolled in this study. The expression of hSETD1A was detected by real-time polymerase chain reaction (PCR) and Western blotting. The immortalized normal human liver cell line including SMMC-7721 was subjected to real-time PCR for hSETD1A mRNA. Furthermore, hSETD1A-small hairpin RNA (shRNA) was used to knock down hSETD1A expression in SMMC-7721 cells. Cell proliferation, cell apoptosis, and cell migration were determined by CCK8, flow cytometry, and Transwell assays. The positive expression rate level of hSETD1A mRNA and protein in liver carcinoma tissues was 73.33%. hSETD1A knockdown using a specific hSETD1A-shRNA inhibited cell proliferation and promoted cell apoptosis in SMMC-7721 cells. It was also found that downregulation of hSETD1A inhibited cell migration ability but did not affect cell invasion. In conclusion, the expression of hSETD1A occurs at a high rate in hepatocellular carcinoma patients. The expression state of hSETD1A may be a prognostic factor in hepatocellular carcinoma.
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Affiliation(s)
- Xin-Sheng Cheng
- Department of Hepatobiliary Surgery, Nanfang Hospital, Southern Medical University, Guangzhou, China
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Alkhalili E, Greenbaum A, Luo L, Rodriguez R, Caldwell K, Estrada OM, O'Neill J, Nir I, Morris KT. Viral hepatitis status does not affect survival in patients with hepatocellular carcinoma. Ann Gastroenterol 2017; 30:101-105. [PMID: 28042245 PMCID: PMC5198233 DOI: 10.20524/aog.2016.0097] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/16/2016] [Accepted: 09/29/2016] [Indexed: 02/07/2023] Open
Abstract
BACKGROUND There have been few studies on the impact of viral etiology on the prognosis in patients with hepatocellular carcinoma (HCC). The aim of this study was to evaluate the clinical characteristics and survival of patients with viral hepatitis-associated HCC (V-HCC), compared to patients with HCC of non-hepatitis B, non-hepatitis C (NBNC-HCC) etiology. METHODS We performed a retrospective analysis of all patients with HCC treated at our comprehensive cancer center from 2000 through 2014. Patients were divided into two groups according to their viral hepatitis status. Presentation patterns, treatments, and survival data were analyzed. RESULTS We evaluated 366 patients: 233 patients (63.7%) had V-HCC while 133 (36.3%) patients had NBNC-HCC. V-HCC patients were younger (P<0.0001) and more likely to be male (P=0.001). Decompensated cirrhosis was more prevalent in V-HCC patients (P=0.01). There was no difference in the resectability rate or disease stage. In patients with resectable disease, those with V-HCC were less likely to undergo hepatectomy (23.7% vs. 38%; P=0.04) for more advanced liver disease. The estimated median survival for V-HCC was 13 months compared to 16 months in NBNC-HCC patients (P=0.57). On multivariate analysis, disease stage (P<0.0001) and Child-Pugh class (P<0.0001) were independent factors affecting survival, but viral status was not (P=0.75). CONCLUSION Despite presenting with more advanced cirrhosis and being less likely to undergo surgery, V-HCC patients had similar survival to patients with NBNC-HCC.
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Affiliation(s)
- Eyas Alkhalili
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Alissa Greenbaum
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Li Luo
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Rodrigo Rodriguez
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Katharine Caldwell
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Oscar Munoz Estrada
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Jacqueline O'Neill
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Itzhak Nir
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
| | - Katherine T Morris
- Department of Surgery, School of Medicine, University of New Mexico, New Mexico, USA
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19
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Wirth TC, Manns MP. The impact of the revolution in hepatitis C treatment on hepatocellular carcinoma. Ann Oncol 2016; 27:1467-74. [PMID: 27226385 DOI: 10.1093/annonc/mdw219] [Citation(s) in RCA: 42] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/24/2016] [Accepted: 05/18/2016] [Indexed: 12/13/2022] Open
Abstract
Hepatitis C infection represents a global health problem affecting ∼200 million chronically infected patients worldwide. Owing to the development of a fibrogenic and inflammatory micromilieu in the liver, hepatitis C virus (HCV)-infected patients are at a high risk of developing fibrosis, cirrhosis and hepatocellular carcinoma (HCC). The advent of direct-acting antiviral agents (DAAs), however, has spurred a revolution in the treatment of HCV patients with sustained viral response (SVR) rates exceeding 90% in real-life settings. Recent clinical trials suggest that these novel treatments will not only alter the epidemiology of HCV infection but also the incidence of HCV-induced complications including hepatic decompensation, liver transplantation and hepatocarcinogenesis. Here, we summarize data from clinical trials carried out in HCV patients with compensated and decompensated cirrhosis and analyze the impact of viral clearance on HCC development and treatment. Finally, we review and discuss current and future treatment options of HCV patients with HCC in pre- and post-transplantation settings.
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Affiliation(s)
- T C Wirth
- Department of Gastroenterology, Hepatology and Endocrinology, Medical School Hannover, Hannover
| | - M P Manns
- Department of Gastroenterology, Hepatology and Endocrinology, Medical School Hannover, Hannover German Center for Infectious Diseases (DZIF), Hannover-Braunschweig, Germany
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20
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Sacco R, Antonucci M, Bresci G, Corti A, Giacomelli L, Mismas V, Rainieri M, Romano A, Eggenhoffner R, Tumino E, Cabibbo G. Curative therapies for hepatocellular carcinoma: an update and perspectives. Expert Rev Anticancer Ther 2015; 16:169-175. [PMID: 26588992 DOI: 10.1586/14737140.2016.1123625] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/03/2025]
Abstract
Curative treatments, including liver transplantation, surgical resection and percutaneous treatments, are the recommended therapies in BCLC-0 (Barcelona Clinic of Liver Cancer) or BCLC-A hepatocellular carcinoma (HCC). This review provides an overview of some issues of clinical importance concerning curative treatments in HCC.
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Affiliation(s)
- Rodolfo Sacco
- a Department of Gastroenterology , Pisa University Hospital , Pisa , Italy
| | - Michela Antonucci
- b Section of Radiology - Di.Bi.Me.F. , University of Palermo , Palermo , Italy
| | - Giampaolo Bresci
- a Department of Gastroenterology , Pisa University Hospital , Pisa , Italy
| | | | - Luca Giacomelli
- d Department of Surgical Sciences and Integrated Diagnostics, School of Medicine , Genova University , Genoa , Italy
| | - Valeria Mismas
- a Department of Gastroenterology , Pisa University Hospital , Pisa , Italy
| | - Maurizio Rainieri
- e Section of Gastroenterology - Di.Bi.M.I.S. , University of Palermo , Palermo , Italy
| | - Antonio Romano
- a Department of Gastroenterology , Pisa University Hospital , Pisa , Italy
| | - Roberto Eggenhoffner
- d Department of Surgical Sciences and Integrated Diagnostics, School of Medicine , Genova University , Genoa , Italy
| | - Emanuele Tumino
- a Department of Gastroenterology , Pisa University Hospital , Pisa , Italy
| | - Giuseppe Cabibbo
- e Section of Gastroenterology - Di.Bi.M.I.S. , University of Palermo , Palermo , Italy
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