Comprehensive Treatment Strategy for Hepatocellular Carcinoma Centered on Surgical Intervention_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YOU Yu , LIU Zuojin ,  GONG Jianping

Hepatobiliary Surgery Department, Second Affiliated Hospital of Chongqing Medical University, Chongqing, 400010, P. R. China;

Corresponding author：

GONG Jianping, Email: gongjianping@126.com

Keywords：

hepatocellular carcinoma; liver resection; liver transplantation; targeted therapy; immune checkpoint inhibitors

DOI：

10.7507/1007-9424.202409124

Video：

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Hepatocellular carcinoma (HCC) is one of the most prevalent malignant tumors worldwide. Although surgery remains the key approach for achieving long-term survival, the majority of patients are ineligible for surgery at the time of initial diagnosis, resulting in suboptimal overall treatment outcomes. This paper reviews the current treatment strategies for HCC, with a particular focus on comprehensive treatment plans centered around surgery. It explores the status and advancements in multidisciplinary treatment approaches, including preoperative conversion therapy, minimally invasive surgery, and postoperative adjuvant therapies. Through the adoption of rational comprehensive treatment strategies, it is anticipated that the therapeutic outcomes and quality of life for HCC patients can be improved.

1.	姚一菲, 孙可欣, 郑荣寿. 《2022全球癌症统计报告》解读: 中国与全球对比. 中国普外基础与临床杂志, 2024, 31(7): 769-780.
2.	郝运, 李川, 文天夫, 等. 全球及中国的肝癌流行病学特征: 基于《2022全球癌症统计报告》解读. 中国普外基础与临床杂志, 2024, 31(7): 781-789.
3.	Vogel A, Meyer T, Sapisochin G, et al. Hepatocellular carcinoma. Lancet, 2022, 400(10360): 1345-1362.
4.	Xie DY, Ren ZG, Zhou J, et al. 2019 Chinese clinical guidelines for the management of hepatocellular carcinoma: updates and insights. Hepatobiliary Surg Nutr, 2020, 9(4): 452-463.
5.	Zhang H, Zhang W, Jiang L, et al. Recent advances in systemic therapy for hepatocellular carcinoma. Biomark Res, 2022, 10(1): 3. doi: 10.1186/s40364-021-00350-4.
6.	Brown ZJ, Tsilimigras DI, Ruff SM, et al. Management of hepatocellular carcinoma. JAMA Surgery, 2023, 158(4): 410-420.
7.	四川大学华西医院肝癌MDT团队, 严律南, 文天夫. 肝细胞肝癌全程多学科规范化管理: 华西医院多学科专家共识(第二版). 中国普外基础与临床杂志, 2020, 27(9): 1062-1077.
8.	中国抗癌协会肝癌专业委员会. 中国肝癌多学科综合治疗专家共识. 临床肝胆病杂志, 2021, 37(2): 278-285.
9.	Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg, 2009, 250(5): 825-830.
10.	洪海杰, 蔡欣然, 陈敏敏, 等. 腹腔镜解剖性与非解剖性肝切除术治疗原发性肝癌的近、远期疗效分析. 福建医科大学学报, 2021, 55(2): 116-120.
11.	中华医学会外科学分会肝脏外科学组. 腹腔镜肝切除专家共识与手术操作指南(2013版). 中华消化外科杂志, 2013, 12(3): 161-165.
12.	Beard RE, Wang Y, Khan S, et al. Laparoscopic liver resection for hepatocellular carcinoma in early and advanced cirrhosis. HPB (Oxford), 2018, 20(6): 521-529.
13.	翟国, 李冉冉. 特殊部位肝癌腹腔镜切除术的可行性分析. 中国现代普通外科进展, 2018, 21(1): 34-35.
14.	刘杰, 张成武, 洪德飞, 等. 完全腹腔镜下肝脏困难部位肿瘤切除术. 中华普通外科杂志, 2016, 31(6): 475-478.
15.	Di Benedetto F, Magistri P, Di Sandro S, et al. Safety and efficacy of robotic vs open liver resection for hepatocellular carcinoma. JAMA Surg, 2023, 158(1): 46-54.
16.	肝癌术后辅助治疗中国专家共识协作组, 中国医师协会外科医师分会, 中国抗癌协会肝癌专业委员会, 等. 肝癌术后辅助治疗中国专家共识(2023版). 中华消化外科杂志, 2023, 22(4): 437-448.
17.	曾永毅, 傅俊, 林孔英, 郭洛彬: 肝细胞癌术后辅助治疗的现状与展望. 中华消化外科杂志 2024, 23(2): 221-227.
18.	Wang L, Ke Q, Lin N, et al. Does postoperative adjuvant transarterial chemoembolization benefit for all patients with hepatocellular carcinoma combined with microvascular invasion: a meta-analysis. Scand J Gastroenterol, 2019, 54(5): 528-537.
19.	Zeng G, Zou B, Li Y, et al. Efficacy of adjuvant transarterial chemoembolization after radical hepatectomy in solitary hepatocellular carcinoma patients: a retrospective study. J Invest Surg, 2022, 35(6): 1208-1216.
20.	Li SH, Mei J, Cheng Y, et al. Postoperative adjuvant hepatic arterial infusion chemotherapy with FOLFOX in hepatocellular carcinoma with microvascular invasion: A multicenter, phase Ⅲ, randomized study. J Clin Oncol, 2023, 41(10): 1898-1908.
21.	Bruix J, Takayama T, Mazzaferro V, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol, 2015, 16(13): 1344-1354.
22.	Pinyol R, Montal R, Bassaganyas L, et al. Molecular predictors of prevention of recurrence in HCC with sorafenib as adjuvant treatment and prognostic factors in the phase 3 STORM trial. Gut, 2019, 68(6): 1065-1075.
23.	Dai MG, Liu SY, Lu WF, et al. Survival benefits from adjuvant lenvatinib for patients with hepatocellular carcinoma and microvascular invasion after curative hepatectomy. Clin Med Insights Oncol, 2023, 17: 11795549231180351. doi: 10.1177/11795549231180351.
24.	中华人民共和国国家卫生健康委员会医政司. 原发性肝癌诊疗指南(2024年版). 中华肝脏病杂志, 2024, 32(7): 581-630.
25.	Qin S, Chen M, Cheng AL, et al. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial. Lancet, 2023, 402(10415): 1835-1847.
26.	刘鹏, 解宇威, 张露旬, 等. 预防性肝动脉化疗栓塞联合抗肿瘤药物对合并微血管侵犯肝癌术后近期复发的影响. 中华肝胆外科杂志, 2021, 27(9): 652-657.
27.	中国抗癌协会肝癌专业委员会转化治疗协作组. 原发性肝癌转化及围手术期治疗中国专家共识(2024版). 中华消化外科杂志, 2024, 23(4): 492-513.
28.	Charalel RA, Sung J, Askin G, et al. Systematic reviews and meta-analyses of portal vein embolization, associated liver partition and portal vein ligation, and radiation lobectomy outcomes in hepatocellular carcinoma patients. Curr Oncol Rep, 2021, 23(11): 135. doi: 10.1007/s11912-021-01075-1.
29.	Li PP, Huang G, Jia NY, et al. Associating liver partition and portal vein ligation for staged hepatectomy versus sequential transarterial chemoembolization and portal vein embolization in staged hepatectomy for HBV-related hepatocellular carcinoma: a randomized comparative study. Hepatobiliary Surg Nutr, 2022, 11(1): 38-51.
30.	Chan A, Zhang WY, Chok K, et al. ALPPS versus portal vein embolization for hepatitis-related hepatocellular carcinoma: A changing paradigm in modulation of future liver remnant before major hepatectomy. Ann Surg, 2021, 273(5): 957-965.
31.	ChebaroA, BucE, DurinT, et al. Liver venous deprivation or associating liver partition and portal vein ligation for staged hepatectomy?: A retrospective multicentric study. Ann Surg, 2021, 274(5): 874-880. doi: 10.1097/SLA.0000000000005121.
32.	Wehrenberg-Klee E, Gandhi RT, Ganguli S. Patient selection and clinical outcomes of Y90 in hepatocellular carcinoma. Tech Vasc Interv Radiol, 2019, 22(2): 70-73.
33.	Tomonari T, Sato Y, Tanaka H, et al. Conversion therapy for unresectable hepatocellular carcinoma after lenvatinib: Three case reports. Medicine (Baltimore), 2020, 99(42): e22782. doi: 10.1097/MD.0000000000022782.
34.	Zhang Y, Huang G, Wang Y, et al. Is salvage liver resection necessary for initially unresectable hepatocellular carcinoma patients downstaged by transarterial chemoembolization? Ten years of experience. Oncologist, 2016, 21(12): 1442-1449.
35.	He M, Li Q, Zou R, et al. Sorafenib plus hepatic arterial infusion of oxaliplatin, fluorouracil, and leucovorin vs sorafenib alone for hepatocellular carcinoma with portal vein invasion: A randomized clinical trial. JAMA Oncol, 2019, 5(7): 953-960.
36.	Moeckli B, Majno P, Orci LA, et al. Liver transplantation selection and allocation criteria for hepatocellular carcinoma: a european perspective. Semin Liver Dis, 2021, 41(2): 172-181.
37.	王征, 周俭. 中国肝癌肝移植现状及展望. 实用器官移植电子杂志, 2019, 7(1): 1-3.
38.	Orlacchio A, Chegai F, Merolla S, et al. Downstaging disease in patients with hepatocellular carcinoma outside up-to-seven criteria: Strategies using degradable starch microspheres transcatheter arterial chemo-embolization. World J Hepatol, 2015, 7(12): 1694-1700.
39.	Zhan QF, Ling SB, Deng YN, et al. Hangzhou criteria as downstaging criteria in hepatocellular carcinoma before liver transplantation: A multicenter study from China. Hepatobiliary Pancreat Dis Int, 2020, 19(4): 349-357.
40.	Muhammad H, Tehreem A, Ting PS, et al. Hepatocellular carcinoma and the role of liver transplantation: a review. J Clin Transl Hepatol, 2021, 9(5): 738-748.
41.	Terrault NA, Francoz C, Berenguer M, et al. Liver transplantation 2023: status report, current and future challenges. Clin Gastroenterol Hepatol, 2023, 21(8): 2150-2166.
42.	中华医学会器官移植学分会, 中国医师协会器官移植医师分会肝移植学组, 中国康复医学会器官移植康复专业委员会: 中国肝癌肝移植受者免疫检查点抑制剂应用专家共识(2024版). 中华器官移植杂志, 2024, 45(7): 415-431.

1. 姚一菲, 孙可欣, 郑荣寿. 《2022全球癌症统计报告》解读: 中国与全球对比. 中国普外基础与临床杂志, 2024, 31(7): 769-780.
2. 郝运, 李川, 文天夫, 等. 全球及中国的肝癌流行病学特征: 基于《2022全球癌症统计报告》解读. 中国普外基础与临床杂志, 2024, 31(7): 781-789.
3. Vogel A, Meyer T, Sapisochin G, et al. Hepatocellular carcinoma. Lancet, 2022, 400(10360): 1345-1362.
4. Xie DY, Ren ZG, Zhou J, et al. 2019 Chinese clinical guidelines for the management of hepatocellular carcinoma: updates and insights. Hepatobiliary Surg Nutr, 2020, 9(4): 452-463.
5. Zhang H, Zhang W, Jiang L, et al. Recent advances in systemic therapy for hepatocellular carcinoma. Biomark Res, 2022, 10(1): 3. doi: 10.1186/s40364-021-00350-4.
6. Brown ZJ, Tsilimigras DI, Ruff SM, et al. Management of hepatocellular carcinoma. JAMA Surgery, 2023, 158(4): 410-420.
7. 四川大学华西医院肝癌MDT团队, 严律南, 文天夫. 肝细胞肝癌全程多学科规范化管理: 华西医院多学科专家共识(第二版). 中国普外基础与临床杂志, 2020, 27(9): 1062-1077.
8. 中国抗癌协会肝癌专业委员会. 中国肝癌多学科综合治疗专家共识. 临床肝胆病杂志, 2021, 37(2): 278-285.
9. Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg, 2009, 250(5): 825-830.
10. 洪海杰, 蔡欣然, 陈敏敏, 等. 腹腔镜解剖性与非解剖性肝切除术治疗原发性肝癌的近、远期疗效分析. 福建医科大学学报, 2021, 55(2): 116-120.
11. 中华医学会外科学分会肝脏外科学组. 腹腔镜肝切除专家共识与手术操作指南(2013版). 中华消化外科杂志, 2013, 12(3): 161-165.
12. Beard RE, Wang Y, Khan S, et al. Laparoscopic liver resection for hepatocellular carcinoma in early and advanced cirrhosis. HPB (Oxford), 2018, 20(6): 521-529.
13. 翟国, 李冉冉. 特殊部位肝癌腹腔镜切除术的可行性分析. 中国现代普通外科进展, 2018, 21(1): 34-35.
14. 刘杰, 张成武, 洪德飞, 等. 完全腹腔镜下肝脏困难部位肿瘤切除术. 中华普通外科杂志, 2016, 31(6): 475-478.
15. Di Benedetto F, Magistri P, Di Sandro S, et al. Safety and efficacy of robotic vs open liver resection for hepatocellular carcinoma. JAMA Surg, 2023, 158(1): 46-54.
16. 肝癌术后辅助治疗中国专家共识协作组, 中国医师协会外科医师分会, 中国抗癌协会肝癌专业委员会, 等. 肝癌术后辅助治疗中国专家共识(2023版). 中华消化外科杂志, 2023, 22(4): 437-448.
17. 曾永毅, 傅俊, 林孔英, 郭洛彬: 肝细胞癌术后辅助治疗的现状与展望. 中华消化外科杂志 2024, 23(2): 221-227.
18. Wang L, Ke Q, Lin N, et al. Does postoperative adjuvant transarterial chemoembolization benefit for all patients with hepatocellular carcinoma combined with microvascular invasion: a meta-analysis. Scand J Gastroenterol, 2019, 54(5): 528-537.
19. Zeng G, Zou B, Li Y, et al. Efficacy of adjuvant transarterial chemoembolization after radical hepatectomy in solitary hepatocellular carcinoma patients: a retrospective study. J Invest Surg, 2022, 35(6): 1208-1216.
20. Li SH, Mei J, Cheng Y, et al. Postoperative adjuvant hepatic arterial infusion chemotherapy with FOLFOX in hepatocellular carcinoma with microvascular invasion: A multicenter, phase Ⅲ, randomized study. J Clin Oncol, 2023, 41(10): 1898-1908.
21. Bruix J, Takayama T, Mazzaferro V, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol, 2015, 16(13): 1344-1354.
22. Pinyol R, Montal R, Bassaganyas L, et al. Molecular predictors of prevention of recurrence in HCC with sorafenib as adjuvant treatment and prognostic factors in the phase 3 STORM trial. Gut, 2019, 68(6): 1065-1075.
23. Dai MG, Liu SY, Lu WF, et al. Survival benefits from adjuvant lenvatinib for patients with hepatocellular carcinoma and microvascular invasion after curative hepatectomy. Clin Med Insights Oncol, 2023, 17: 11795549231180351. doi: 10.1177/11795549231180351.
24. 中华人民共和国国家卫生健康委员会医政司. 原发性肝癌诊疗指南(2024年版). 中华肝脏病杂志, 2024, 32(7): 581-630.
25. Qin S, Chen M, Cheng AL, et al. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial. Lancet, 2023, 402(10415): 1835-1847.
26. 刘鹏, 解宇威, 张露旬, 等. 预防性肝动脉化疗栓塞联合抗肿瘤药物对合并微血管侵犯肝癌术后近期复发的影响. 中华肝胆外科杂志, 2021, 27(9): 652-657.
27. 中国抗癌协会肝癌专业委员会转化治疗协作组. 原发性肝癌转化及围手术期治疗中国专家共识(2024版). 中华消化外科杂志, 2024, 23(4): 492-513.
28. Charalel RA, Sung J, Askin G, et al. Systematic reviews and meta-analyses of portal vein embolization, associated liver partition and portal vein ligation, and radiation lobectomy outcomes in hepatocellular carcinoma patients. Curr Oncol Rep, 2021, 23(11): 135. doi: 10.1007/s11912-021-01075-1.
29. Li PP, Huang G, Jia NY, et al. Associating liver partition and portal vein ligation for staged hepatectomy versus sequential transarterial chemoembolization and portal vein embolization in staged hepatectomy for HBV-related hepatocellular carcinoma: a randomized comparative study. Hepatobiliary Surg Nutr, 2022, 11(1): 38-51.
30. Chan A, Zhang WY, Chok K, et al. ALPPS versus portal vein embolization for hepatitis-related hepatocellular carcinoma: A changing paradigm in modulation of future liver remnant before major hepatectomy. Ann Surg, 2021, 273(5): 957-965.
31. ChebaroA, BucE, DurinT, et al. Liver venous deprivation or associating liver partition and portal vein ligation for staged hepatectomy?: A retrospective multicentric study. Ann Surg, 2021, 274(5): 874-880. doi: 10.1097/SLA.0000000000005121.
32. Wehrenberg-Klee E, Gandhi RT, Ganguli S. Patient selection and clinical outcomes of Y90 in hepatocellular carcinoma. Tech Vasc Interv Radiol, 2019, 22(2): 70-73.
33. Tomonari T, Sato Y, Tanaka H, et al. Conversion therapy for unresectable hepatocellular carcinoma after lenvatinib: Three case reports. Medicine (Baltimore), 2020, 99(42): e22782. doi: 10.1097/MD.0000000000022782.
34. Zhang Y, Huang G, Wang Y, et al. Is salvage liver resection necessary for initially unresectable hepatocellular carcinoma patients downstaged by transarterial chemoembolization? Ten years of experience. Oncologist, 2016, 21(12): 1442-1449.
35. He M, Li Q, Zou R, et al. Sorafenib plus hepatic arterial infusion of oxaliplatin, fluorouracil, and leucovorin vs sorafenib alone for hepatocellular carcinoma with portal vein invasion: A randomized clinical trial. JAMA Oncol, 2019, 5(7): 953-960.
36. Moeckli B, Majno P, Orci LA, et al. Liver transplantation selection and allocation criteria for hepatocellular carcinoma: a european perspective. Semin Liver Dis, 2021, 41(2): 172-181.
37. 王征, 周俭. 中国肝癌肝移植现状及展望. 实用器官移植电子杂志, 2019, 7(1): 1-3.
38. Orlacchio A, Chegai F, Merolla S, et al. Downstaging disease in patients with hepatocellular carcinoma outside up-to-seven criteria: Strategies using degradable starch microspheres transcatheter arterial chemo-embolization. World J Hepatol, 2015, 7(12): 1694-1700.
39. Zhan QF, Ling SB, Deng YN, et al. Hangzhou criteria as downstaging criteria in hepatocellular carcinoma before liver transplantation: A multicenter study from China. Hepatobiliary Pancreat Dis Int, 2020, 19(4): 349-357.
40. Muhammad H, Tehreem A, Ting PS, et al. Hepatocellular carcinoma and the role of liver transplantation: a review. J Clin Transl Hepatol, 2021, 9(5): 738-748.
41. Terrault NA, Francoz C, Berenguer M, et al. Liver transplantation 2023: status report, current and future challenges. Clin Gastroenterol Hepatol, 2023, 21(8): 2150-2166.
42. 中华医学会器官移植学分会, 中国医师协会器官移植医师分会肝移植学组, 中国康复医学会器官移植康复专业委员会: 中国肝癌肝移植受者免疫检查点抑制剂应用专家共识(2024版). 中华器官移植杂志, 2024, 45(7): 415-431.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Latest ArticlesComprehensive Treatment Strategy for Hepatocellular Carcinoma Centered on Surgical Intervention

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