Skip to main content
Top
Published in: Annals of Surgical Oncology 1/2021

01-01-2021 | Liver Resection | Hepatobiliary Tumors

Major Laparoscopic Versus Open Resection for Hepatocellular Carcinoma: A Propensity Score-Matched Analysis Based on Surgeons’ Learning Curve

Authors: Jonathan Geograpo Navarro, MD, Incheon Kang, MD, Seoung Yoon Rho, MD, Gi Hong Choi, MD, PhD, Dai Hoon Han, MD, PhD, Kyung Sik Kim, MD, PhD, Jin Sub Choi, MD, PhD

Published in: Annals of Surgical Oncology | Issue 1/2021

Login to get access

Abstract

Background

Surgical complications for surgeons still in the learning phase of major laparoscopic liver resection (LLR) have been frequently observed. We aimed to compare perioperative and long-term outcomes of laparoscopic and open surgery based on the surgeons’ learning curve for LLR after propensity score-matched (PSM) analysis.

Methods

This was a retrospective study of all patients with a histologic diagnosis of hepatocellular carcinoma who underwent major hepatectomy between January 2013 and December 2018. A PSM analysis was used to compare the groups of patients who underwent LLR and open major liver resection (OLR) before and after the learning curve was maximized.

Results

Among 405 patients, 106 underwent LLR and 299 underwent OLR. The learning curve was maximized after 42 cases. Compared with OLR, LLR had more liver-related injury and grade III or higher complications during the learning phase. The LLR group had less blood loss, fewer transfusion requirements, and fewer liver-related complications during the ‘experienced’ phase. Hospital stay was significantly shorter during and after maximization of the learning curve in LLR compared with OLR. Operative time was comparable in the two phases. Overall, LLR was associated with less blood loss, fewer complications, and shorter hospital stay compared with open surgery. There was no significant difference in long-term survival outcomes between the two groups.

Conclusions

LLR had a higher incidence of liver-related complications during the surgeon’s learning phase compared with OLR. This association was significantly diminished with surgeon experience. Overall perioperative outcomes such as estimated blood loss, surgical complications, and hospital stay remained better for LLR compared with OLR.
Appendix
Available only for authorised users
Literature
1.
go back to reference Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2804 patients. Ann Surg. 2009;250:831–841.CrossRef Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2804 patients. Ann Surg. 2009;250:831–841.CrossRef
2.
go back to reference Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg. 2009;250:825–830.CrossRef Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg. 2009;250:825–830.CrossRef
3.
go back to reference Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261:619–629.PubMed Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261:619–629.PubMed
4.
go back to reference Ciria R, Cherqui D, Geller DA, Briceno J, Wakabayashi G. Comparative short-term benefits of laparoscopic liver resection: 9000 cases and climbing. Ann Surg. 2016;263:761–777.CrossRef Ciria R, Cherqui D, Geller DA, Briceno J, Wakabayashi G. Comparative short-term benefits of laparoscopic liver resection: 9000 cases and climbing. Ann Surg. 2016;263:761–777.CrossRef
5.
go back to reference Brown KM, Geller DA. What is the learning curve for laparoscopic major hepatectomy? J Gastrointest Surg. 2016;20:1065–1071.CrossRef Brown KM, Geller DA. What is the learning curve for laparoscopic major hepatectomy? J Gastrointest Surg. 2016;20:1065–1071.CrossRef
6.
go back to reference Berardi G, Aghayan D, Fretland AA, et al. Multicentre analysis of the learning curve for laparoscopic liver resection of the posterosuperior segments. Br J Surg. 2019;106(11):1512–1522.CrossRef Berardi G, Aghayan D, Fretland AA, et al. Multicentre analysis of the learning curve for laparoscopic liver resection of the posterosuperior segments. Br J Surg. 2019;106(11):1512–1522.CrossRef
7.
go back to reference van der Poel MJ, Besselink MG, Cipriani F, et al. Outcome and learning curve in 159 consecutive patients undergoing total laparoscopic hemihepatectomy. JAMA Surg. 2016;151:923–928.CrossRef van der Poel MJ, Besselink MG, Cipriani F, et al. Outcome and learning curve in 159 consecutive patients undergoing total laparoscopic hemihepatectomy. JAMA Surg. 2016;151:923–928.CrossRef
8.
go back to reference Berardi G, Van Cleven S, Fretland AA, et al. Evolution of laparoscopic liver surgery from innovation to implementation to mastery: perioperative and oncologic outcomes of 2238 patients from 4 European specialized centers. J Am Coll Surg. 2017;225:639–649.CrossRef Berardi G, Van Cleven S, Fretland AA, et al. Evolution of laparoscopic liver surgery from innovation to implementation to mastery: perioperative and oncologic outcomes of 2238 patients from 4 European specialized centers. J Am Coll Surg. 2017;225:639–649.CrossRef
9.
go back to reference Thornblade LW, Shi X, Ruiz A, Flum DR, Park JO. Comparative effectiveness of minimally invasive surgery and conventional approaches for major or challenging hepatectomy. J Am Coll Surg. 2017;224:851–861.CrossRef Thornblade LW, Shi X, Ruiz A, Flum DR, Park JO. Comparative effectiveness of minimally invasive surgery and conventional approaches for major or challenging hepatectomy. J Am Coll Surg. 2017;224:851–861.CrossRef
10.
go back to reference Guro H, Cho JY, Han HS, et al. Outcomes of major laparoscopic liver resection for hepatocellular carcinoma. Surg Oncol. 2018;27:31–35.CrossRef Guro H, Cho JY, Han HS, et al. Outcomes of major laparoscopic liver resection for hepatocellular carcinoma. Surg Oncol. 2018;27:31–35.CrossRef
11.
go back to reference Fretland AA, Dagenborg VJ, Bjornelv GMW, et al. Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET randomized controlled trial. Ann Surg. 2018;267:199–207.CrossRef Fretland AA, Dagenborg VJ, Bjornelv GMW, et al. Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET randomized controlled trial. Ann Surg. 2018;267:199–207.CrossRef
12.
go back to reference Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg. 2005;12:351–355.CrossRef Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg. 2005;12:351–355.CrossRef
13.
go back to reference Coles SR, Besselink MG, Serin KR, et al. Total laparoscopic management of lesions involving liver segment 7. Surg Endosc 2015;29:3190–3195.CrossRef Coles SR, Besselink MG, Serin KR, et al. Total laparoscopic management of lesions involving liver segment 7. Surg Endosc 2015;29:3190–3195.CrossRef
14.
go back to reference Martinez-Cecilia D, Fontana M, Siddiqi NN, Halls M, Barbaro S, Abu-Hilal M. Laparoscopic parenchymal sparing resections in segment 8: techniques for a demanding and infrequent procedure. Surg Endosc. 2018;32:2012–2019.CrossRef Martinez-Cecilia D, Fontana M, Siddiqi NN, Halls M, Barbaro S, Abu-Hilal M. Laparoscopic parenchymal sparing resections in segment 8: techniques for a demanding and infrequent procedure. Surg Endosc. 2018;32:2012–2019.CrossRef
15.
go back to reference Choi SH, Choi GH, Han DH, Choi JS. Laparoscopic liver resection using a rubber band retraction technique: usefulness and perioperative outcome in 100 consecutive cases. Surg Endosc 2015;29:387–397.CrossRef Choi SH, Choi GH, Han DH, Choi JS. Laparoscopic liver resection using a rubber band retraction technique: usefulness and perioperative outcome in 100 consecutive cases. Surg Endosc 2015;29:387–397.CrossRef
16.
go back to reference Gombay E, Hussein AA, Steiner SH. Monitoring binary outcomes using risk-adjusted charts: a comparative study. Stat Med. 2011;30:2815–2826.CrossRef Gombay E, Hussein AA, Steiner SH. Monitoring binary outcomes using risk-adjusted charts: a comparative study. Stat Med. 2011;30:2815–2826.CrossRef
17.
go back to reference Park EJ, Kim CW, Cho MS, et al. Multidimensional analyses of the learning curve of robotic low anterior resection for rectal cancer: 3-phase learning process comparison. Surg Endosc 2014;28:2821–2831.CrossRef Park EJ, Kim CW, Cho MS, et al. Multidimensional analyses of the learning curve of robotic low anterior resection for rectal cancer: 3-phase learning process comparison. Surg Endosc 2014;28:2821–2831.CrossRef
18.
go back to reference Xiangfei M, Yinzhe X, Yingwei P, Shichun L, Weidong D. Open versus laparoscopic hepatic resection for hepatocellular carcinoma: a systematic review and meta-analysis. Surg Endosc. 2019;33:2396–2418.CrossRef Xiangfei M, Yinzhe X, Yingwei P, Shichun L, Weidong D. Open versus laparoscopic hepatic resection for hepatocellular carcinoma: a systematic review and meta-analysis. Surg Endosc. 2019;33:2396–2418.CrossRef
19.
go back to reference Ciria R, Gomez-Luque I, Ocana S, et al. A systematic review and meta-analysis comparing the short- and long-term outcomes for laparoscopic and open liver resections for hepatocellular carcinoma: updated results from the European guidelines meeting on laparoscopic liver surgery, Southampton, UK, 2017. Ann Surg Oncol. 2019;26:252–263.CrossRef Ciria R, Gomez-Luque I, Ocana S, et al. A systematic review and meta-analysis comparing the short- and long-term outcomes for laparoscopic and open liver resections for hepatocellular carcinoma: updated results from the European guidelines meeting on laparoscopic liver surgery, Southampton, UK, 2017. Ann Surg Oncol. 2019;26:252–263.CrossRef
20.
go back to reference Shang HT, Bao JH, Zhang XB, Wang HB, Zhang HT, Li ZL. Comparison of clinical efficacy and complications between laparoscopic partial and open partial hepatectomy for liver carcinoma: a meta-analysis. J Laparoendosc Adv Surg Tech A. 2019;29:225–232.CrossRef Shang HT, Bao JH, Zhang XB, Wang HB, Zhang HT, Li ZL. Comparison of clinical efficacy and complications between laparoscopic partial and open partial hepatectomy for liver carcinoma: a meta-analysis. J Laparoendosc Adv Surg Tech A. 2019;29:225–232.CrossRef
21.
go back to reference Cai W, Liu Z, Xiao Y, et al. Comparison of clinical outcomes of laparoscopic versus open surgery for recurrent hepatocellular carcinoma: a meta-analysis. Surg Endosc. 2019;33(11):3550–3557.CrossRef Cai W, Liu Z, Xiao Y, et al. Comparison of clinical outcomes of laparoscopic versus open surgery for recurrent hepatocellular carcinoma: a meta-analysis. Surg Endosc. 2019;33(11):3550–3557.CrossRef
22.
go back to reference Vigano L, Laurent A, Tayar C, Tomatis M, Ponti A, Cherqui D. The learning curve in laparoscopic liver resection: improved feasibility and reproducibility. Ann Surg. 2009;250:772–782.CrossRef Vigano L, Laurent A, Tayar C, Tomatis M, Ponti A, Cherqui D. The learning curve in laparoscopic liver resection: improved feasibility and reproducibility. Ann Surg. 2009;250:772–782.CrossRef
23.
go back to reference Choi SH, Choi GH, Han DH, Kwon SW, Choi JS. Laparoscopic right hepatectomy: toward protocolization and simplification. Ann Surg Oncol. 2017;24:554–555.CrossRef Choi SH, Choi GH, Han DH, Kwon SW, Choi JS. Laparoscopic right hepatectomy: toward protocolization and simplification. Ann Surg Oncol. 2017;24:554–555.CrossRef
24.
go back to reference Aldrighetti L, Cipriani F, Fiorentini G, Catena M, Paganelli M, Ratti F. A stepwise learning curve to define the standard for technical improvement in laparoscopic liver resections: complexity-based analysis in 1032 procedures. Updates Surg. 2019;71:273–283.CrossRef Aldrighetti L, Cipriani F, Fiorentini G, Catena M, Paganelli M, Ratti F. A stepwise learning curve to define the standard for technical improvement in laparoscopic liver resections: complexity-based analysis in 1032 procedures. Updates Surg. 2019;71:273–283.CrossRef
25.
go back to reference Di Fabio F, Samim M, Di Gioia P, Godeseth R, Pearce NW, Abu Hilal M. Laparoscopic major hepatectomies: clinical outcomes and classification. World J Surg. 2014;38:3169–3174.CrossRef Di Fabio F, Samim M, Di Gioia P, Godeseth R, Pearce NW, Abu Hilal M. Laparoscopic major hepatectomies: clinical outcomes and classification. World J Surg. 2014;38:3169–3174.CrossRef
27.
go back to reference Guilbaud T, Birnbaum DJ, Berdah S, Farges O, Beyer Berjot L. Learning curve in laparoscopic liver resection, educational value of simulation and training programmes: a systematic review. World J Surg. 2019;43:2710–2719.CrossRef Guilbaud T, Birnbaum DJ, Berdah S, Farges O, Beyer Berjot L. Learning curve in laparoscopic liver resection, educational value of simulation and training programmes: a systematic review. World J Surg. 2019;43:2710–2719.CrossRef
28.
go back to reference Halls MC, Cipriani F, Berardi G, et al. Conversion for unfavorable intraoperative events results in significantly worse outcomes during laparoscopic liver resection: lessons learned from a multicenter review of 2861 cases. Ann Surg. 2018;268:1051–1057.CrossRef Halls MC, Cipriani F, Berardi G, et al. Conversion for unfavorable intraoperative events results in significantly worse outcomes during laparoscopic liver resection: lessons learned from a multicenter review of 2861 cases. Ann Surg. 2018;268:1051–1057.CrossRef
29.
go back to reference Nomi T, Fuks D, Kawaguchi Y, Mal F, Nakajima Y, Gayet B. Learning curve for laparoscopic major hepatectomy. Br J Surg 2015;102:796–804.CrossRef Nomi T, Fuks D, Kawaguchi Y, Mal F, Nakajima Y, Gayet B. Learning curve for laparoscopic major hepatectomy. Br J Surg 2015;102:796–804.CrossRef
30.
go back to reference Kluger MD, Vigano L, Barroso R, Cherqui D. The learning curve in laparoscopic major liver resection. J Hepatobiliary Pancreat Sci. 2013;20:131–136.CrossRef Kluger MD, Vigano L, Barroso R, Cherqui D. The learning curve in laparoscopic major liver resection. J Hepatobiliary Pancreat Sci. 2013;20:131–136.CrossRef
31.
go back to reference Yamada S, Shimada M, Imura S, et al. Effective stepwise training and procedure standardization for young surgeons to perform laparoscopic left hepatectomy. Surg Endosc. 2017;31:2623–2629.CrossRef Yamada S, Shimada M, Imura S, et al. Effective stepwise training and procedure standardization for young surgeons to perform laparoscopic left hepatectomy. Surg Endosc. 2017;31:2623–2629.CrossRef
32.
go back to reference Gani F, Ejaz A, Dillhoff M, et al. A national assessment of the utilization, quality and cost of laparoscopic liver resection. HPB (Oxford). 2019;21(10):1327–1335.CrossRef Gani F, Ejaz A, Dillhoff M, et al. A national assessment of the utilization, quality and cost of laparoscopic liver resection. HPB (Oxford). 2019;21(10):1327–1335.CrossRef
33.
go back to reference Franken C, Lau B, Putchakayala K, DiFronzo LA. Comparison of short-term outcomes in laparoscopic versus open hepatectomy. JAMA Surg. 2014;149:941–946.CrossRef Franken C, Lau B, Putchakayala K, DiFronzo LA. Comparison of short-term outcomes in laparoscopic versus open hepatectomy. JAMA Surg. 2014;149:941–946.CrossRef
34.
go back to reference Heinrich S, Tripke V, Huber T, Mittler J, Lang H. A match-pair analysis of open versus laparoscopic liver surgery. JSLS. 2017;21:e2017.00061. Heinrich S, Tripke V, Huber T, Mittler J, Lang H. A match-pair analysis of open versus laparoscopic liver surgery. JSLS. 2017;21:e2017.00061.
35.
go back to reference Kasai M, Cipriani F, Gayet B, et al. Laparoscopic versus open major hepatectomy: a systematic review and meta-analysis of individual patient data. Surgery. 2018;163:985–995.CrossRef Kasai M, Cipriani F, Gayet B, et al. Laparoscopic versus open major hepatectomy: a systematic review and meta-analysis of individual patient data. Surgery. 2018;163:985–995.CrossRef
36.
go back to reference Abu Hilal M, Aldrighetti L, Dagher I, et al. The southampton consensus guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg. 2018;268:11–18.CrossRef Abu Hilal M, Aldrighetti L, Dagher I, et al. The southampton consensus guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg. 2018;268:11–18.CrossRef
37.
go back to reference Navarro JG, Kang CM. Pitfalls for laparoscopic pancreaticoduodenectomy: need for a stepwise approach. Ann Gastroenterol Surg. 2019;3:254–268.CrossRef Navarro JG, Kang CM. Pitfalls for laparoscopic pancreaticoduodenectomy: need for a stepwise approach. Ann Gastroenterol Surg. 2019;3:254–268.CrossRef
38.
go back to reference Yoon YI, Kim KH, Cho HD, et al. Long-term perioperative outcomes of pure laparoscopic liver resection versus open liver resection for hepatocellular carcinoma: a retrospective study. Surg Endosc. 2020;34(2):796–805.CrossRef Yoon YI, Kim KH, Cho HD, et al. Long-term perioperative outcomes of pure laparoscopic liver resection versus open liver resection for hepatocellular carcinoma: a retrospective study. Surg Endosc. 2020;34(2):796–805.CrossRef
39.
go back to reference Yin Z, Fan X, Ye H, Yin D, Wang J. Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol. 2013;20:1203–1215.CrossRef Yin Z, Fan X, Ye H, Yin D, Wang J. Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol. 2013;20:1203–1215.CrossRef
40.
go back to reference Ban D, Kudo A, Ito H, et al. The difficulty of laparoscopic liver resection. Updates Surg. 2015;67:123–128.CrossRef Ban D, Kudo A, Ito H, et al. The difficulty of laparoscopic liver resection. Updates Surg. 2015;67:123–128.CrossRef
Metadata
Title
Major Laparoscopic Versus Open Resection for Hepatocellular Carcinoma: A Propensity Score-Matched Analysis Based on Surgeons’ Learning Curve
Authors
Jonathan Geograpo Navarro, MD
Incheon Kang, MD
Seoung Yoon Rho, MD
Gi Hong Choi, MD, PhD
Dai Hoon Han, MD, PhD
Kyung Sik Kim, MD, PhD
Jin Sub Choi, MD, PhD
Publication date
01-01-2021
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 1/2021
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-020-08764-4

Other articles of this Issue 1/2021

Annals of Surgical Oncology 1/2021 Go to the issue