Status and progress of surgical treatment of postoperative recurrent hepatocellular carcinoma_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

HU Han ,  WU Dequan

Department of Liver Surgery, The Second Affiliated Hospital of Harbin Medical University, Harbin 150001, P. R. China;

Corresponding author：

WU Dequan, Email: dqwu56@163.com

Keywords：

recurrent hepatocellular carcinoma; re-hepatectomy; salvage liver transplantation

DOI：

10.7507/1007-9424.202006111

Video：

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Objective To summarize the current status and progress of surgical treatment for postoperative recurrent hepatocellular carcinoma (HCC).Method The literatures about studies of surgical treatment of postoperative recurrent HCC were reviewed.Results The surgical operation was an effective method for the treatment of recurrent HCC. The operation methods included re-hepatectomy and salvage liver transplantation. There was no uniform standard for the indication of re-hepatectomy, but the basic principles were the same. At present, the indication of salvage liver transplantation was mainly based on Milan criteria. For patients with recurrent HCC who met the operation indications, surgical operation could improve the long-term survival rate of patients and benefit the patients.Conclusion It migh prolong the survival time and improve the long-term survival rate of patients with recurrent HCC when the appropriate patients and reasonable surgical methods are chosen according to the surgical indications, the tumor situation of initial hepatectomy, postoperative recurrence time, and other factors.

Citation： HU Han, WU Dequan. Status and progress of surgical treatment of postoperative recurrent hepatocellular carcinoma. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(4): 551-555. doi: 10.7507/1007-9424.202006111 Copy

1.	Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin, 2011, 61(2): 69-90.
2.	Yoh T, Seo S, Taura K, et al. Surgery for recurrent hepatocellular carcinoma: achieving long-term survival. Ann Surg, 2019 Apr 30. doi: 10.1097/SLA.0000000000003358.
3.	Li M, Wang Z, Cao J, et al. Risk factors and prognosis of patients with recurrent hepatocellular carcinoma who undergo liver re-resections. Eur J Surg Oncol, 2019, 45(9): 1684-1690.
4.	Tabrizian P, Jibara G, Shrager B, et al. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg, 2015, 261(5): 947-955.
5.	Roayaie S, Bassi D, Tarchi P, et al. Second hepatic resection for recurrent hepatocellular cancer: a Western experience. J Hepatol, 2011, 55(2): 346-350.
6.	Xia Y, Li J, Liu G, et al. Long-term effects of repeat hepatectomy vs percutaneous radiofrequency ablation among patients with recurrent hepatocellular carcinoma: a randomized clinical trial. JAMA Oncol, 2019, 6(2): 255-263.
7.	Lu LH, Mei J, Kan A, et al. Treatment optimization for recurrent hepatocellular carcinoma: Repeat hepatic resection versus radiofrequency ablation. Cancer Med, 2020, 9(9): 2997-3005.
8.	陈康, 刘新宇, 滕煜宪, 等. 再次肝切除与射频消融治疗复发性肝癌疗效对比研究. 中国实用外科杂志, 2019, 39(10): 1060-1064.
9.	张杰, 周仲国, 周东升, 等. 复发肝癌腹腔镜再切除的临床分析. 中华腔镜外科杂志(电子版), 2015, 8(1): 16-19.
10.	Onoe T, Yamaguchi M, Irei T, et al. Feasibility and efficacy of repeat laparoscopic liver resection for recurrent hepatocellular carcinoma. Surg Endosc, 2019, 34(10): 4574-4581.
11.	Liang Y, Lin C, Zhang B, et al. Perioperative outcomes comparing laparoscopic with open repeat liver resection for post-hepatectomy recurrent liver cancer: A systematic review and meta-analysis. Int J Surg, 2020, 79: 17-28.
12.	Chan AC, Poon RT, Chok KS, et al. Feasibility of laparoscopic re-resection for patients with recurrent hepatocellular carcinoma. World J Surg, 2014, 38(5): 1141-1146.
13.	Liu K, Chen Y, Wu X, et al. Laparoscopic liver re-resection is feasible for patients with posthepatectomy hepatocellular carcinoma recurrence: a propensity score matching study. Surg Endosc, 2017, 31(11): 4790-4798.
14.	Yamashita Y, Shirabe K, Tsuijita E, et al. Third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery, 2013, 154(5): 1038-1045.
15.	Mise Y, Hasegawa K, Shindoh J, et al. The feasibility of third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg, 2015, 262(2): 347-357.
16.	Majno PE, Sarasin FP, Mentha G, et al. Primary liver resection and salvage transplantation or primary liver transplantation in patients with single, small hepatocellular carcinoma and preserved liver function: an outcome-oriented decision analysis. Hepatology, 2000, 31(4): 899-906.
17.	Bhangui P, Allard MA, Vibert E, et al. Salvage versus primary liver transplantation for early hepatocellular carcinoma: do both strategies yield similar outcomes? Ann Surg, 2016, 264(1): 155-163.
18.	邹卫龙, 朱雄伟, 李自强, 等. 挽救性肝移植治疗肝切除术后复发性肝细胞癌临床效果分析. 中国实用外科杂志, 2018, 38(2): 200-204.
19.	史瑞, 张雅敏, 许洋, 等. 直接肝移植与挽救性肝移植治疗原发性肝癌疗效分析. 中华肝胆外科杂志, 2017, 23(2): 87-89.
20.	Chan KM, Wu TH, Cheng CH, et al. Advantage of early liver transplantation whenever indicated for hepatocellular carcinoma recurrence after primary liver resection. Biomed J, 2019, 42(5): 335-342.
21.	Kim SH, Kim KH, Ha TY, et al. Salvage living donor liver transplantation for recurrent hepatocellular carcinoma after prior laparoscopic hepatectomy. Hepatobiliary Pancreat Dis Int, 2018, 17(5): 473-476.
22.	Abe T, Tashiro H, Teraoka Y, et al. Efficacy and feasibility of salvage living donor liver transplantation after initial liver resection in patients with hepatocellular carcinoma. Dig Surg, 2016, 33(1): 8-14.
23.	Yamashita Y, Yoshida Y, Kurihara T, et al. Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: Repeat hepatectomy versus salvage living donor liver transplantation. Liver Transpl, 2015, 21(7): 961-968.
24.	Kim JM, Joh JW, Yi NJ, et al. Living donor liver transplantation should be cautiously considered as initial treatment in recurrent hepatocellular carcinoma within the Milan criteria after curative liver resection. Ann Transl Med, 2020, 8(6): 288.
25.	蔡秀军, 金仁安. 复发性肝癌治疗方式合理选择. 中国实用外科杂志, 2019, 39(10): 1015-1020.
26.	Fang JZ, Xiang L, Hu YK, et al. Options for the treatment of intrahepatic recurrent hepatocellular carcinoma: Salvage liver transplantation or rehepatectomy? Clin Transplant, 2020, 34(5): e13831.
27.	Lim C, Shinkawa H, Hasegawa K, et al. Salvage liver transplantation or repeat hepatectomy for recurrent hepatocellular carcinoma: An intent-to-treat analysis. Liver Transpl, 2017, 23(12): 1553-1563.
28.	Huang ZY, Liang BY, Xiong M, et al. Long-term outcomes of repeat hepatic resection in patients with recurrent hepatocellular carcinoma and analysis of recurrent types and their prognosis: a single-center experience in China. Ann Surg Oncol, 2012, 19(8): 2515-2525.
29.	PLOS ONE Editors. Retraction: Salvage liver transplantation for recurrent hepatocellular carcinoma after liver resection: retrospective study of the Milan and Hangzhou criteria [retraction of: PLoS One. 2014 Jan 27;9(1):e87222]. PLoS One, 2019, 14(7): e0220431.
30.	Ali MA, Li WF, Wang JH, et al. Impact of pathological features of primary hepatocellular carcinoma on the outcomes of intrahepatic recurrence management: single center experience from Southern Taiwan. HPB (Oxford), 2016, 18(10): 851-860.
31.	向邦德, 黎乐群, 赵荫农, 等. 复发性肝癌再切除术患者预后因素分析. 中国肿瘤临床, 2010, 37(17): 994-997.
32.	Wang P, Li H, Shi B, et al. Prognostic factors in patients with recurrent hepatocellular carcinoma treated with salvage liver transplantation: a single-center study. Oncotarget, 2016, 7(23): 35071-35083.
33.	Minagawa M, Makuuchi M, Takayama T, et al. Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg, 2003, 238(5): 703-710.
34.	Shimada K, Sakamoto Y, Esaki M, et al. Analysis of prognostic factors affecting survival after initial recurrence and treatment efficacy for recurrence in patients undergoing potentially curative hepatectomy for hepatocellular carcinoma. Ann Surg Oncol, 2007, 14(8): 2337-2347.
35.	Lee HS, Choi GH, Joo DJ, et al. The clinical behavior of transplantable recurrent hepatocellular carcinoma after curative resection: implications for salvage liver transplantation. Ann Surg Oncol, 2014, 21(8): 2717-2724.
36.	丛文铭, 吴孟超. 肝癌术后复发发生机制及临床病理学意义. 中国实用外科杂志, 2012, 32(10): 809-811.
37.	Cheng Z, Yang P, Qu S, et al. Risk factors and management for early and late intrahepatic recurrence of solitary hepatocellular carcinoma after curative resection. HPB (Oxford), 2015, 17(5): 422-427.
38.	Xing H, Sun LY, Yan WT, et al. Repeat hepatectomy for patients with early and late recurrence of hepatocellular carcinoma: A multicenter propensity score matching analysis. Surgery, 2019: S0039-6060(19)30741-X.
39.	Jung SM, Kim JM, Choi GS, et al. Characteristics of early recurrence after curative liver resection for solitary hepatocellular carcinoma. J Gastrointest Surg, 2019, 23(2): 304-311.
40.	Hu Z, Zhou J, Li Z, et al. Time interval to recurrence as a predictor of overall survival in salvage liver transplantation for patients with hepatocellular carcinoma associated with hepatitis B virus. Surgery, 2015, 157(2): 239-248.
41.	Portolani N, Coniglio A, Ghidoni S, et al. Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann Surg, 2006, 243(2): 229-235.

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin, 2011, 61(2): 69-90.
2. Yoh T, Seo S, Taura K, et al. Surgery for recurrent hepatocellular carcinoma: achieving long-term survival. Ann Surg, 2019 Apr 30. doi: 10.1097/SLA.0000000000003358.
3. Li M, Wang Z, Cao J, et al. Risk factors and prognosis of patients with recurrent hepatocellular carcinoma who undergo liver re-resections. Eur J Surg Oncol, 2019, 45(9): 1684-1690.
4. Tabrizian P, Jibara G, Shrager B, et al. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg, 2015, 261(5): 947-955.
5. Roayaie S, Bassi D, Tarchi P, et al. Second hepatic resection for recurrent hepatocellular cancer: a Western experience. J Hepatol, 2011, 55(2): 346-350.
6. Xia Y, Li J, Liu G, et al. Long-term effects of repeat hepatectomy vs percutaneous radiofrequency ablation among patients with recurrent hepatocellular carcinoma: a randomized clinical trial. JAMA Oncol, 2019, 6(2): 255-263.
7. Lu LH, Mei J, Kan A, et al. Treatment optimization for recurrent hepatocellular carcinoma: Repeat hepatic resection versus radiofrequency ablation. Cancer Med, 2020, 9(9): 2997-3005.
8. 陈康, 刘新宇, 滕煜宪, 等. 再次肝切除与射频消融治疗复发性肝癌疗效对比研究. 中国实用外科杂志, 2019, 39(10): 1060-1064.
9. 张杰, 周仲国, 周东升, 等. 复发肝癌腹腔镜再切除的临床分析. 中华腔镜外科杂志(电子版), 2015, 8(1): 16-19.
10. Onoe T, Yamaguchi M, Irei T, et al. Feasibility and efficacy of repeat laparoscopic liver resection for recurrent hepatocellular carcinoma. Surg Endosc, 2019, 34(10): 4574-4581.
11. Liang Y, Lin C, Zhang B, et al. Perioperative outcomes comparing laparoscopic with open repeat liver resection for post-hepatectomy recurrent liver cancer: A systematic review and meta-analysis. Int J Surg, 2020, 79: 17-28.
12. Chan AC, Poon RT, Chok KS, et al. Feasibility of laparoscopic re-resection for patients with recurrent hepatocellular carcinoma. World J Surg, 2014, 38(5): 1141-1146.
13. Liu K, Chen Y, Wu X, et al. Laparoscopic liver re-resection is feasible for patients with posthepatectomy hepatocellular carcinoma recurrence: a propensity score matching study. Surg Endosc, 2017, 31(11): 4790-4798.
14. Yamashita Y, Shirabe K, Tsuijita E, et al. Third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery, 2013, 154(5): 1038-1045.
15. Mise Y, Hasegawa K, Shindoh J, et al. The feasibility of third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg, 2015, 262(2): 347-357.
16. Majno PE, Sarasin FP, Mentha G, et al. Primary liver resection and salvage transplantation or primary liver transplantation in patients with single, small hepatocellular carcinoma and preserved liver function: an outcome-oriented decision analysis. Hepatology, 2000, 31(4): 899-906.
17. Bhangui P, Allard MA, Vibert E, et al. Salvage versus primary liver transplantation for early hepatocellular carcinoma: do both strategies yield similar outcomes? Ann Surg, 2016, 264(1): 155-163.
18. 邹卫龙, 朱雄伟, 李自强, 等. 挽救性肝移植治疗肝切除术后复发性肝细胞癌临床效果分析. 中国实用外科杂志, 2018, 38(2): 200-204.
19. 史瑞, 张雅敏, 许洋, 等. 直接肝移植与挽救性肝移植治疗原发性肝癌疗效分析. 中华肝胆外科杂志, 2017, 23(2): 87-89.
20. Chan KM, Wu TH, Cheng CH, et al. Advantage of early liver transplantation whenever indicated for hepatocellular carcinoma recurrence after primary liver resection. Biomed J, 2019, 42(5): 335-342.
21. Kim SH, Kim KH, Ha TY, et al. Salvage living donor liver transplantation for recurrent hepatocellular carcinoma after prior laparoscopic hepatectomy. Hepatobiliary Pancreat Dis Int, 2018, 17(5): 473-476.
22. Abe T, Tashiro H, Teraoka Y, et al. Efficacy and feasibility of salvage living donor liver transplantation after initial liver resection in patients with hepatocellular carcinoma. Dig Surg, 2016, 33(1): 8-14.
23. Yamashita Y, Yoshida Y, Kurihara T, et al. Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: Repeat hepatectomy versus salvage living donor liver transplantation. Liver Transpl, 2015, 21(7): 961-968.
24. Kim JM, Joh JW, Yi NJ, et al. Living donor liver transplantation should be cautiously considered as initial treatment in recurrent hepatocellular carcinoma within the Milan criteria after curative liver resection. Ann Transl Med, 2020, 8(6): 288.
25. 蔡秀军, 金仁安. 复发性肝癌治疗方式合理选择. 中国实用外科杂志, 2019, 39(10): 1015-1020.
26. Fang JZ, Xiang L, Hu YK, et al. Options for the treatment of intrahepatic recurrent hepatocellular carcinoma: Salvage liver transplantation or rehepatectomy? Clin Transplant, 2020, 34(5): e13831.
27. Lim C, Shinkawa H, Hasegawa K, et al. Salvage liver transplantation or repeat hepatectomy for recurrent hepatocellular carcinoma: An intent-to-treat analysis. Liver Transpl, 2017, 23(12): 1553-1563.
28. Huang ZY, Liang BY, Xiong M, et al. Long-term outcomes of repeat hepatic resection in patients with recurrent hepatocellular carcinoma and analysis of recurrent types and their prognosis: a single-center experience in China. Ann Surg Oncol, 2012, 19(8): 2515-2525.
29. PLOS ONE Editors. Retraction: Salvage liver transplantation for recurrent hepatocellular carcinoma after liver resection: retrospective study of the Milan and Hangzhou criteria [retraction of: PLoS One. 2014 Jan 27;9(1):e87222]. PLoS One, 2019, 14(7): e0220431.
30. Ali MA, Li WF, Wang JH, et al. Impact of pathological features of primary hepatocellular carcinoma on the outcomes of intrahepatic recurrence management: single center experience from Southern Taiwan. HPB (Oxford), 2016, 18(10): 851-860.
31. 向邦德, 黎乐群, 赵荫农, 等. 复发性肝癌再切除术患者预后因素分析. 中国肿瘤临床, 2010, 37(17): 994-997.
32. Wang P, Li H, Shi B, et al. Prognostic factors in patients with recurrent hepatocellular carcinoma treated with salvage liver transplantation: a single-center study. Oncotarget, 2016, 7(23): 35071-35083.
33. Minagawa M, Makuuchi M, Takayama T, et al. Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg, 2003, 238(5): 703-710.
34. Shimada K, Sakamoto Y, Esaki M, et al. Analysis of prognostic factors affecting survival after initial recurrence and treatment efficacy for recurrence in patients undergoing potentially curative hepatectomy for hepatocellular carcinoma. Ann Surg Oncol, 2007, 14(8): 2337-2347.
35. Lee HS, Choi GH, Joo DJ, et al. The clinical behavior of transplantable recurrent hepatocellular carcinoma after curative resection: implications for salvage liver transplantation. Ann Surg Oncol, 2014, 21(8): 2717-2724.
36. 丛文铭, 吴孟超. 肝癌术后复发发生机制及临床病理学意义. 中国实用外科杂志, 2012, 32(10): 809-811.
37. Cheng Z, Yang P, Qu S, et al. Risk factors and management for early and late intrahepatic recurrence of solitary hepatocellular carcinoma after curative resection. HPB (Oxford), 2015, 17(5): 422-427.
38. Xing H, Sun LY, Yan WT, et al. Repeat hepatectomy for patients with early and late recurrence of hepatocellular carcinoma: A multicenter propensity score matching analysis. Surgery, 2019: S0039-6060(19)30741-X.
39. Jung SM, Kim JM, Choi GS, et al. Characteristics of early recurrence after curative liver resection for solitary hepatocellular carcinoma. J Gastrointest Surg, 2019, 23(2): 304-311.
40. Hu Z, Zhou J, Li Z, et al. Time interval to recurrence as a predictor of overall survival in salvage liver transplantation for patients with hepatocellular carcinoma associated with hepatitis B virus. Surgery, 2015, 157(2): 239-248.
41. Portolani N, Coniglio A, Ghidoni S, et al. Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann Surg, 2006, 243(2): 229-235.

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Status and progress of surgical treatment of postoperative recurrent hepatocellular carcinoma

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