Recurrence pattern after laparoscopic <i>versus</i> open hepatectomy for hepatocellular carcinoma: a propensity score matching analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

PAN Yi ,  WEI Yonggang

Department of Liver Surgery & Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

WEI Yonggang, Email: drweiyg@163.com

Keywords：

hepatocellular carcinoma; laparoscopic hepatectomy; recurrence; relapse free survival rate

DOI：

10.7507/1007-9424.202111027

Video：

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Objective To compare the long-term outcomes of laparoscopic hepatectomy (LH) and open hepatectomy (OH) in the treatment of hepatocellular carcinoma (HCC), and to discuss the recurrence patterns of HCC after surgery. Methods Patients with HCC who underwent hepatectomy and met inclusion and exclusion criteria from January 2015 to December 2018 were retrospectively enrolled, then were divided into LH and OH groups according to surgical methods. The results of HCC recurrence after LH and OH were compared after 1∶1 propensity score matching between the two groups. The potential risk factors for recurrence were assessed by Cox proportional hazards regression and a nomogram was constructed. Results A total of 977 patients with HCC who underwent hepatectomy were enrolled. Of these, 385 underwent LH and 592 underwent OH. After 1∶1 propensity score matching, 323 patients were enrolled in each group for analysis. The tumor recurrences were found in 124 patients (38.4%) and 118 patients (36.5%) and the median tumor free survival time was 10 months and 9 months in the LH group and OH group, respectively. The most common recurrence pattern was the intrahepatic recurrence, and the most common treatment was the transarterial chemoembolization. There was no significant difference of the relapse free survival curve between the LH and OH groups (P=0.763). In the entire cohort, no patient had recurrence or metastasis of specimen removal incisions or Trocar pores. No significant differences in the recurrence pattern and treatment between the LH and OH groups (P>0.05). Cox proportional hazards regression analysis showed that the age ≤60 years old, grade 2 of albumin-bilirubin grade, postoperative alpha fetoprotein >8 μg/L, tumor diameter ≥5 cm, multiple tumors, and low differentiation increased the recurrence of HCC after LH (P<0.05). The nomogram including these factors and combining with clinical practice was constructed, its consistent index for predicting the recurrence of HCC after LH was 0.704 [95%CI (0.659, 0.753)]. Conclusion Intrahepatic recurrence is still the most common pattern of postoperative HCC recurrence, and LH doesn’t increase risk of incision recurrence or implantation.

Citation： PAN Yi, WEI Yonggang. Recurrence pattern after laparoscopic versus open hepatectomy for hepatocellular carcinoma: a propensity score matching analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(4): 505-511. doi: 10.7507/1007-9424.202111027 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Vogel A, Cervantes A, Chau I, et al. Hepatocellular carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2019, 30(5): 871-873.
3.	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.
4.	Takahara T, Wakabayashi G, Beppu T, et al. Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci, 2015, 22(10): 721-727.
5.	Witowski J, Rubinkiewicz M, Mizera M, et al. Meta-analysis of short- and long-term outcomes after pure laparoscopic versus open liver surgery in hepatocellular carcinoma patients. Surg Endosc, 2019, 33(5): 1491-1507.
6.	Katz SC, Shia J, Liau KH, et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg, 2009, 249(4): 617-623.
7.	Marukuchi R, Furukawa K, Iwase R, et al. Risk factors for deterioration of remnant liver function after hepatic resection for hepatocellular carcinoma. Anticancer Res, 2019, 39(10): 5755-5760.
8.	Xiang L, Li J, Chen J, et al. Prospective cohort study of laparoscopic and open hepatectomy for hepatocellular carcinoma. Br J Surg, 2016, 103(13): 1895-1901.
9.	中国研究型医院学会肝胆胰外科专业委员会. 腹腔镜肝切除术治疗肝细胞癌中国专家共识(2020版). 中华消化外科杂志, 2020, 19(11): 1119-1134.
10.	Liu F, Xu H, Li Q, et al. Outcomes of pure laparoscopic Glissonian pedicle approach hepatectomy for hepatocellular carcinoma: a propensity score matching analysis. Surg Endosc, 2019, 33(4): 1155-1166.
11.	Xu XF, Xing H, Han J, et al. Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: a multicenter study from China. JAMA Surg, 2019, 154(3): 209-217.
12.	Shah SA, Greig PD, Gallinger S, et al. Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg, 2006, 202(2): 275-283.
13.	Liu F, Zhang J, Lei C, et al. Feasibility of laparoscopic major hepatectomy for hepatic paragonimiasis: two case reports. Medicine (Baltimore), 2016, 95(38): e4939. doi: 10.1097/MD.0000000000004939.
14.	Xu HW, Liu F, Li HY, et al. Outcomes following laparoscopic versus open major hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score-matched analysis. Surg Endosc, 2018, 32(2): 712-719.
15.	Liu F, Wei Y, Chen K, et al. The extrahepatic Glissonian versus hilar dissection approach for laparoscopic formal right and left hepatectomies in patients with hepatocellular carcinoma. J Gastrointest Surg, 2019, 23(12): 2401-2410.
16.	魏永刚, 张渝翰. 腹腔镜肝脏切除术的肝门血流阻断及断肝技巧. 中国普外基础与临床杂志, 2019, 26(2): 137-140.
17.	Liu F, Wei Y, Li H, et al. LigaSure versus CUSA for parenchymal transection during laparoscopic hepatectomy in hepatocellular carcinoma patients with cirrhosis: a propensity score-matched analysis. Surg Endosc, 2018, 32(5): 2454-2465.
18.	Pinato DJ, Sharma R, Allara E, et al. The ALBI grade provides objective hepatic reserve estimation across each BCLC stage of hepatocellular carcinoma. J Hepatol, 2017, 66(2): 338-346.
19.	Ishak K, Baptista A, Bianchi L, et al. Histological grading and staging of chronic hepatitis. J Hepatol, 1995, 22(6): 696-699.
20.	Cucchetti A, Piscaglia F, Caturelli E, et al. Comparison of recurrence of hepatocellular carcinoma after resection in patients with cirrhosis to its occurrence in a surveilled cirrhotic population. Ann Surg Oncol, 2009, 16(2): 413-422.
21.	Jin B, Chen MT, Fei YT, et al. Safety and efficacy for laparoscopic versus open hepatectomy: a meta-analysis. Surg Oncol, 2018, 27(2): A26-A34. doi: 10.1016/j.suronc.2017.06.007.
22.	Abu Hilal M, Aldrighetti L, Dagher I, et al. The Southampton Consensus Guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg, 2018, 268(1): 11-18.
23.	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.
24.	Cai X, Li Z, Zhang Y, et al. Laparoscopic liver resection and the learning curve: a 14-year, single-center experience. Surg Endosc, 2014, 28(4): 1334-1341.
25.	Hung MC, Wu HS, Lee YT, et al. Intraperitoneal metastasis of hepatocellular carcinoma after spontaneous rupture: a case report. World J Gastroenterol, 2008, 14(24): 3927-3931.
26.	Imamura H, Matsuyama Y, Tanaka E, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol, 2003, 38(2): 200-207.
27.	Shim JH, Jun MJ, Han S, et al. Prognostic nomograms for prediction of recurrence and survival after curative liver resection for hepatocellular carcinoma. Ann Surg, 2015, 261(5): 939-946.
28.	Cheung TT, Dai WC, Tsang SH, et al. Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg, 2016, 264(4): 612-620.
29.	Lan X, Li H, Liu F, et al. Does liver cirrhosis have an impact on the results of different hepatic inflow occlusion methods in laparoscopic liver resection? A propensity score analysis. HPB (Oxford), 2019, 21(5): 531-538.
30.	中华人民共和国国家卫生健康委员会医政医管局. 原发性肝癌诊疗规范(2019年版). 传染病信息, 2020, 33(6): 481-500.
31.	Wang Z, Ren Z, Chen Y, et al. Adjuvant transarterial chemoembolization for HBV-related hepatocellular carcinoma after resection: a randomized controlled study. Clin Cancer Res, 2018, 24(9): 2074-2081.
32.	Chen ZH, Zhang XP, Zhou TF, et al. Adjuvant transarterial chemoembolization improves survival outcomes in hepatocellular carcinoma with microvascular invasion: a systematic review and meta-analysis. Eur J Surg Oncol, 2019, 45(11): 2188-2196.
33.	Feng YX, Wang T, Deng YZ, et al. Sorafenib suppresses postsurgical recurrence and metastasis of hepatocellular carcinoma in an orthotopic mouse model. Hepatology, 2011, 53(2): 483-492.
34.	Shariat SF, Capitanio U, Jeldres C, et al. Can nomograms be superior to other prediction tools? BJU Int, 2009, 103(4): 492-495.
35.	Yan Y, Zhou Q, Zhang M, et al. Integrated nomograms for preoperative prediction of microvascular invasion and lymph node metastasis risk in hepatocellular carcinoma patients. Ann Surg Oncol, 2020, 27(5): 1361-1371.
36.	Lei Z, Li J, Wu D, et al. Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the Milan criteria. JAMA Surg, 2016, 151(4): 356-363.
37.	Yang L, Gu D, Wei J, et al. A radiomics nomogram for preoperative prediction of microvascular invasion in hepatocellular carcinoma. Liver Cancer, 2019, 8(5): 373-386.
38.	Hu HT, Wang Z, Huang XW, et al. Ultrasound-based radiomics score: a potential biomarker for the prediction of microvascular invasion in hepatocellular carcinoma. Eur Radiol, 2019, 29(6): 2890-2901.
39.	Xu L, Li L, Wang P, et al. Novel prognostic nomograms for hepatocellular carcinoma patients with microvascular invasion: experience from a single center. Gut Liver, 2019, 13(6): 669-682.

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Vogel A, Cervantes A, Chau I, et al. Hepatocellular carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2019, 30(5): 871-873.
3. 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.
4. Takahara T, Wakabayashi G, Beppu T, et al. Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci, 2015, 22(10): 721-727.
5. Witowski J, Rubinkiewicz M, Mizera M, et al. Meta-analysis of short- and long-term outcomes after pure laparoscopic versus open liver surgery in hepatocellular carcinoma patients. Surg Endosc, 2019, 33(5): 1491-1507.
6. Katz SC, Shia J, Liau KH, et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg, 2009, 249(4): 617-623.
7. Marukuchi R, Furukawa K, Iwase R, et al. Risk factors for deterioration of remnant liver function after hepatic resection for hepatocellular carcinoma. Anticancer Res, 2019, 39(10): 5755-5760.
8. Xiang L, Li J, Chen J, et al. Prospective cohort study of laparoscopic and open hepatectomy for hepatocellular carcinoma. Br J Surg, 2016, 103(13): 1895-1901.
9. 中国研究型医院学会肝胆胰外科专业委员会. 腹腔镜肝切除术治疗肝细胞癌中国专家共识(2020版). 中华消化外科杂志, 2020, 19(11): 1119-1134.
10. Liu F, Xu H, Li Q, et al. Outcomes of pure laparoscopic Glissonian pedicle approach hepatectomy for hepatocellular carcinoma: a propensity score matching analysis. Surg Endosc, 2019, 33(4): 1155-1166.
11. Xu XF, Xing H, Han J, et al. Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: a multicenter study from China. JAMA Surg, 2019, 154(3): 209-217.
12. Shah SA, Greig PD, Gallinger S, et al. Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg, 2006, 202(2): 275-283.
13. Liu F, Zhang J, Lei C, et al. Feasibility of laparoscopic major hepatectomy for hepatic paragonimiasis: two case reports. Medicine (Baltimore), 2016, 95(38): e4939. doi: 10.1097/MD.0000000000004939.
14. Xu HW, Liu F, Li HY, et al. Outcomes following laparoscopic versus open major hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score-matched analysis. Surg Endosc, 2018, 32(2): 712-719.
15. Liu F, Wei Y, Chen K, et al. The extrahepatic Glissonian versus hilar dissection approach for laparoscopic formal right and left hepatectomies in patients with hepatocellular carcinoma. J Gastrointest Surg, 2019, 23(12): 2401-2410.
16. 魏永刚, 张渝翰. 腹腔镜肝脏切除术的肝门血流阻断及断肝技巧. 中国普外基础与临床杂志, 2019, 26(2): 137-140.
17. Liu F, Wei Y, Li H, et al. LigaSure versus CUSA for parenchymal transection during laparoscopic hepatectomy in hepatocellular carcinoma patients with cirrhosis: a propensity score-matched analysis. Surg Endosc, 2018, 32(5): 2454-2465.
18. Pinato DJ, Sharma R, Allara E, et al. The ALBI grade provides objective hepatic reserve estimation across each BCLC stage of hepatocellular carcinoma. J Hepatol, 2017, 66(2): 338-346.
19. Ishak K, Baptista A, Bianchi L, et al. Histological grading and staging of chronic hepatitis. J Hepatol, 1995, 22(6): 696-699.
20. Cucchetti A, Piscaglia F, Caturelli E, et al. Comparison of recurrence of hepatocellular carcinoma after resection in patients with cirrhosis to its occurrence in a surveilled cirrhotic population. Ann Surg Oncol, 2009, 16(2): 413-422.
21. Jin B, Chen MT, Fei YT, et al. Safety and efficacy for laparoscopic versus open hepatectomy: a meta-analysis. Surg Oncol, 2018, 27(2): A26-A34. doi: 10.1016/j.suronc.2017.06.007.
22. Abu Hilal M, Aldrighetti L, Dagher I, et al. The Southampton Consensus Guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg, 2018, 268(1): 11-18.
23. 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.
24. Cai X, Li Z, Zhang Y, et al. Laparoscopic liver resection and the learning curve: a 14-year, single-center experience. Surg Endosc, 2014, 28(4): 1334-1341.
25. Hung MC, Wu HS, Lee YT, et al. Intraperitoneal metastasis of hepatocellular carcinoma after spontaneous rupture: a case report. World J Gastroenterol, 2008, 14(24): 3927-3931.
26. Imamura H, Matsuyama Y, Tanaka E, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol, 2003, 38(2): 200-207.
27. Shim JH, Jun MJ, Han S, et al. Prognostic nomograms for prediction of recurrence and survival after curative liver resection for hepatocellular carcinoma. Ann Surg, 2015, 261(5): 939-946.
28. Cheung TT, Dai WC, Tsang SH, et al. Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg, 2016, 264(4): 612-620.
29. Lan X, Li H, Liu F, et al. Does liver cirrhosis have an impact on the results of different hepatic inflow occlusion methods in laparoscopic liver resection? A propensity score analysis. HPB (Oxford), 2019, 21(5): 531-538.
30. 中华人民共和国国家卫生健康委员会医政医管局. 原发性肝癌诊疗规范(2019年版). 传染病信息, 2020, 33(6): 481-500.
31. Wang Z, Ren Z, Chen Y, et al. Adjuvant transarterial chemoembolization for HBV-related hepatocellular carcinoma after resection: a randomized controlled study. Clin Cancer Res, 2018, 24(9): 2074-2081.
32. Chen ZH, Zhang XP, Zhou TF, et al. Adjuvant transarterial chemoembolization improves survival outcomes in hepatocellular carcinoma with microvascular invasion: a systematic review and meta-analysis. Eur J Surg Oncol, 2019, 45(11): 2188-2196.
33. Feng YX, Wang T, Deng YZ, et al. Sorafenib suppresses postsurgical recurrence and metastasis of hepatocellular carcinoma in an orthotopic mouse model. Hepatology, 2011, 53(2): 483-492.
34. Shariat SF, Capitanio U, Jeldres C, et al. Can nomograms be superior to other prediction tools? BJU Int, 2009, 103(4): 492-495.
35. Yan Y, Zhou Q, Zhang M, et al. Integrated nomograms for preoperative prediction of microvascular invasion and lymph node metastasis risk in hepatocellular carcinoma patients. Ann Surg Oncol, 2020, 27(5): 1361-1371.
36. Lei Z, Li J, Wu D, et al. Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the Milan criteria. JAMA Surg, 2016, 151(4): 356-363.
37. Yang L, Gu D, Wei J, et al. A radiomics nomogram for preoperative prediction of microvascular invasion in hepatocellular carcinoma. Liver Cancer, 2019, 8(5): 373-386.
38. Hu HT, Wang Z, Huang XW, et al. Ultrasound-based radiomics score: a potential biomarker for the prediction of microvascular invasion in hepatocellular carcinoma. Eur Radiol, 2019, 29(6): 2890-2901.
39. Xu L, Li L, Wang P, et al. Novel prognostic nomograms for hepatocellular carcinoma patients with microvascular invasion: experience from a single center. Gut Liver, 2019, 13(6): 669-682.

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Recurrence pattern after laparoscopic versus open hepatectomy for hepatocellular carcinoma: a propensity score matching analysis

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