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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Abstract Full text Figures/Tables Video References Cited by

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.

Citation： YOU Yu, LIU Zuojin, GONG Jianping. Comprehensive treatment strategy for hepatocellular carcinoma centered on surgical intervention. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(12): 1413-1418. doi: 10.7507/1007-9424.202409124 Copy

1.	姚一菲, 孫可欣, 鄭榮壽. 《2022全球癌癥統計報告》解讀: 中國與全球對比. 中國普外基礎與臨床雜志, 2024, 31(7): 769-780.
2.	郝運, 李川, 文天夫, 等. 全球及中國的肝癌流行病學特征: 基于《2022全球癌癥統計報告》解讀. 中國普外基礎與臨床雜志, 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.	四川大學華西醫院肝癌MDT團隊, 嚴律南, 文天夫. 肝細胞肝癌全程多學科規范化管理: 華西醫院多學科專家共識(第二版). 中國普外基礎與臨床雜志, 2020, 27(9): 1062-1077.
8.	中國抗癌協會肝癌專業委員會. 中國肝癌多學科綜合治療專家共識. 臨床肝膽病雜志, 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, 陳敏敏, 等. 腹腔鏡解剖性與非解剖性肝切除術治療原發性肝癌的近、遠期療效分析. 福建醫科大學學報, 2021, 55(2): 116-120.
11.	中華醫學會外科學分會肝臟外科學組. 腹腔鏡肝切除專家共識與手術操作指南(2013版). 中華消化外科雜志, 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.	翟國, 李冉冉. 特殊部位肝癌腹腔鏡切除術的可行性分析. 中國現代普通外科進展, 2018, 21(1): 34-35.
14.	劉杰, 張成武, 洪德飛, 等. 完全腹腔鏡下肝臟困難部位腫瘤切除術. 中華普通外科雜志, 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.	肝癌術后輔助治療中國專家共識協作組, 中國醫師協會外科醫師分會, 中國抗癌協會肝癌專業委員會, 等. 肝癌術后輔助治療中國專家共識(2023版). 中華消化外科雜志, 2023, 22(4): 437-448.
17.	曾永毅, 傅俊, 林孔英, 郭洛彬: 肝細胞癌術后輔助治療的現狀與展望. 中華消化外科雜志 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.	中華人民共和國國家衛生健康委員會醫政司. 原發性肝癌診療指南(2024年版). 中華肝臟病雜志, 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.	劉鵬, 解宇威, 張露旬, 等. 預防性肝動脈化療栓塞聯合抗腫瘤藥物對合并微血管侵犯肝癌術后近期復發的影響. 中華肝膽外科雜志, 2021, 27(9): 652-657.
27.	中國抗癌協會肝癌專業委員會轉化治療協作組. 原發性肝癌轉化及圍手術期治療中國專家共識(2024版). 中華消化外科雜志, 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, 周儉. 中國肝癌肝移植現狀及展望. 實用器官移植電子雜志, 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.	中華醫學會器官移植學分會, 中國醫師協會器官移植醫師分會肝移植學組, 中國康復醫學會器官移植康復專業委員會: 中國肝癌肝移植受者免疫檢查點抑制劑應用專家共識(2024版). 中華器官移植雜志, 2024, 45(7): 415-431.

1. 姚一菲, 孫可欣, 鄭榮壽. 《2022全球癌癥統計報告》解讀: 中國與全球對比. 中國普外基礎與臨床雜志, 2024, 31(7): 769-780.
2. 郝運, 李川, 文天夫, 等. 全球及中國的肝癌流行病學特征: 基于《2022全球癌癥統計報告》解讀. 中國普外基礎與臨床雜志, 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. 四川大學華西醫院肝癌MDT團隊, 嚴律南, 文天夫. 肝細胞肝癌全程多學科規范化管理: 華西醫院多學科專家共識(第二版). 中國普外基礎與臨床雜志, 2020, 27(9): 1062-1077.
8. 中國抗癌協會肝癌專業委員會. 中國肝癌多學科綜合治療專家共識. 臨床肝膽病雜志, 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, 陳敏敏, 等. 腹腔鏡解剖性與非解剖性肝切除術治療原發性肝癌的近、遠期療效分析. 福建醫科大學學報, 2021, 55(2): 116-120.
11. 中華醫學會外科學分會肝臟外科學組. 腹腔鏡肝切除專家共識與手術操作指南(2013版). 中華消化外科雜志, 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. 翟國, 李冉冉. 特殊部位肝癌腹腔鏡切除術的可行性分析. 中國現代普通外科進展, 2018, 21(1): 34-35.
14. 劉杰, 張成武, 洪德飛, 等. 完全腹腔鏡下肝臟困難部位腫瘤切除術. 中華普通外科雜志, 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. 肝癌術后輔助治療中國專家共識協作組, 中國醫師協會外科醫師分會, 中國抗癌協會肝癌專業委員會, 等. 肝癌術后輔助治療中國專家共識(2023版). 中華消化外科雜志, 2023, 22(4): 437-448.
17. 曾永毅, 傅俊, 林孔英, 郭洛彬: 肝細胞癌術后輔助治療的現狀與展望. 中華消化外科雜志 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. 中華人民共和國國家衛生健康委員會醫政司. 原發性肝癌診療指南(2024年版). 中華肝臟病雜志, 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. 劉鵬, 解宇威, 張露旬, 等. 預防性肝動脈化療栓塞聯合抗腫瘤藥物對合并微血管侵犯肝癌術后近期復發的影響. 中華肝膽外科雜志, 2021, 27(9): 652-657.
27. 中國抗癌協會肝癌專業委員會轉化治療協作組. 原發性肝癌轉化及圍手術期治療中國專家共識(2024版). 中華消化外科雜志, 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, 周儉. 中國肝癌肝移植現狀及展望. 實用器官移植電子雜志, 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. 中華醫學會器官移植學分會, 中國醫師協會器官移植醫師分會肝移植學組, 中國康復醫學會器官移植康復專業委員會: 中國肝癌肝移植受者免疫檢查點抑制劑應用專家共識(2024版). 中華器官移植雜志, 2024, 45(7): 415-431.

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The difficulties and countermeasures of laparoscopic hepatectomy in the treatment of hepatocellular carcinoma in the difficult sites of liver

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Comprehensive treatment strategy for hepatocellular carcinoma centered on surgical intervention

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