Comparison of laparoscopic versus open liver resection for hepatocellular carcinoma using propensity score matching
Review Article

Comparison of laparoscopic versus open liver resection for hepatocellular carcinoma using propensity score matching

Yuki Koga1,2, Toru Beppu1,2,3, Katsutaka Kuramoto1,2, Koichi Kinoshita1,2, Yasushi Yoshida1,2, Katsunori Imai2, Takeshi Takahara3, Masafumi Nakamura3, Go Wakabayashi3, Hideo Baba2

1Department of Surgery, Yamaga City Medical Center, Kumamoto, Japan; 2Department of Gastroenterological Surgery, Graduate School of Life Sciences, Kumamoto University, Kumamoto, Japan; 3“Project Committee of the Endoscopic Surgery” of the Japanese Society of Hepato-Biliary-Pancreatic Surgery, Tokyo, Japan

Contributions: (I) Conception and design: Y Koga, T Beppu; (II) Administrative support: All authors; (III) Provision of study materials or patients: None; (IV) Collection and assembly of data: Y Koga, K Kuramoto, K Imai; (V) Data analysis and interpretation: T Beppu, T Takahara, M Nakamura, G Wakabayashi, H Baba; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Toru Beppu, MD, PhD, FACS. Department of Surgery, Yamaga City Medical Center, Kumamoto, 511 Yamaga, Kumamoto 861-0593, Japan. Email: tbeppu@kumamoto-u.ac.jp.

Abstract: Laparoscopic liver resection (LLR) has become one of standard treatments for hepatocellular carcinoma (HCC). Numerous reports have demonstrated that LLR might be less invasive and provide better short-term results and identical oncological outcome compared to conventional open liver resection (OLR); however almost reports in the past were not conclusive. Propensity score matching (PSM) is a quite useful tool to match different background factors in the two groups; therefore, we reviewed papers assessing laparoscopic and OLR using PSM. We have already published the largest study of LLR for HCC from the “Project Committee of the Endoscopic Surgery” of the Japanese Society of Hepato-Biliary-Pancreatic Surgery. We summarized 10 documents including this paper. After PSM, maximum 387 patients undergoing laparoscopic and OLR were investigated. Less intraoperative blood loss or low rate of blood transfusion, and shorter hospital stay are solid advantageous results of LLR. Long-term outcome was quite equivalent in the two groups and special recurrence pattern in the LLR was rarely observed. These PSM studies clearly demonstrated that LLR can provide excellent perioperative benefits without oncologic disadvantages; therefore, we can strongly recommend LLR as a standard practice for properly selected patients with HCC.

Keywords: Laparoscopic liver resection (LLR); open liver resection (OLR); hepatocellular carcinoma (HCC); propensity score matching analysis (PSM analysis)

Received: 14 March 2017; Accepted: 08 May 2017; Published: 19 June 2017.

doi: 10.21037/ales.2017.05.11

Introduction

Laparoscopic liver resection (LLR) become a gold standard for not only benign liver tumors but also malignant tumors, including hepatocellular carcinoma (HCC) and colorectal liver metastases (CRLM) (1-3). Many papers have demonstrated that LLR is less invasive and can provide better short-term results and identical oncological outcome compared to conventional open liver resection (OLR) (4-8). However, these reports in the early period were based on the examinations of retrospective case-matched studies or meta-analysis of non-randomized studies. In clinical situation, numerous selection biases can exist with regard to selecting LLR; therefore, the previous results are not definitive. Unfortunately, there has been no conclusive randomized control trial in this field (3,9). More recently, ORANGE II study was closed due to slow patients’ collection (10). This randomized control trial was conducted to compare open versus laparoscopic left lateral sectionectomy in terms of an enhanced recovery after surgery program.

Propensity score matching (PSM) is a quite useful tool to compare the usefulness in the two groups with different backgrounds. The treatment effects assessed by well-designed PSM study were similar to those obtained by randomized control trial (11). We have previously reported the results of PSM study for CRLM patients undergoing LLR and OLR in the recent issue of “Annals of Laparoscopic and Endoscopic Surgery” (12).

In this paper, we reviewed the surgical results of LLR compared to OLR for HCC patients.

LLR versus OLR for HCC using PSM

We have published the two largest study of LLR for HCC and CRLM from the “Project Committee of the Endoscopic Surgery” of the Japanese Society of Hepato-Biliary-Pancreatic Surgery (13,14). In a HCC study, we retrospectively analyzed 3,405 patients undergoing initial liver resection for HCC from 31 specialized centers all over Japan between 2000 and 2010. Among them, after PSM, 774 (387 LLR and 387 OLR) patients were selected. The receiver operating characteristic area under the curve of the propensity score for undergoing LLR was excellent; 0.786. LLR for patients with HCC showed similar long-term outcomes, associated with less blood loss, fewer postoperative complications, and shorter hospital stay compared with OLR. In PSM, it is quite important what is selected as a matching item. In that study, we examined difficult location or not; posterosuperior segments or anterolateral segments (15). In 3 papers in Table 1, difficult tumor location was currently assessed and used for PSM analysis. Tumor location (superficial or deeper position) and proximity to the large vessels were also important points. We investigated all these subjects for PSM in Kumamoto University study (17).

Table 1

Perioperative findings and outcomes in HCC patients undergoing LLR and OLR using PSM

First author year Patients’ number, LLR/OLR Operation time Blood loss Morbidity Mortality Hospital stay RFS, DFS OS
Kim, 2014 (16) 29/29 Equal LLR# less LLR M-less, P=0.065 Equal LLR shorter Equal Equal
Takahara, 2015 (13) 387/387 LLR longer LLR less LLR less Equal LLR shorter Equal Equal
Beppu, 2015 (17) 52/52 Equal LLR less Equal Equal LLR shorter Equal Equal
Meguro, 2015 (18) 35/35 Equal LLR less Equal Equal NA Equal Equal
Han, 2015 (19) 88/88 LLR M-longer, P=0.07 LLR M-less, P=0.08 LLR less Equal LLR shorter Equal Equal
Yoon#2, 2015 (20) 58/174 LLR shorter LLR less LLR less NA LLR shorter Equal Equal
Sposito, 2016 (21) 43/43 Equal Equal LLR less Equal LLR shorter Equal Equal
Han#3, 2016 (22) 99/198 LLR M-longer, P=0.085 LLR less LLR less Equal LLR shorter Equal Equal
Cheung#4, 2016 (23) 110/330 LLR shorter LLR less Equal Equal LLR shorter Equal LLR better
Yoon#5, 2016 (24) 33/33 LLR longer Equal Equal NA LLR shorter Equal Equal

#, blood transfusion rate; #2, limited to HCC smaller than 5 cm; #3, robot operation; #4, limited to patients with liver cirrhosis; #5, limited to right hepatectomy. HCC, hepatocellular carcinoma; PSM, propensity score matching; LLR, laparoscopic liver resection; OLR, open liver resection; RFS, recurrence-free survival; DFS, disease-free survival; OS, overall survival; NA, not available; M-, marginally.

From 2014 ten PSM studies have published comparing LLR and OLR limited to HCC patients (Table 1) (13,16-24). One to one, one to two and one to three PSM was performed. After PSM, 29–387 LLR patients and 29–387 OLR patients were investigated. One study included only robot operation (22). In terms of perioperative parameters, the operation time for LLR was similar in 6 studies, longer in two, and shorter in two compared with OLR and the blood loss amount or blood transfusion rate was less in 7 of 10 studies. Morbidity was equal in 5 studies and less in 5 for LLR compared to OLR and mortality was comparable in all studies. HCC patients with live cirrhosis could have specific advantages, including postoperative fluid collection (16). LLR and can be completed through a minimal wound and can avoid massive liver mobilization and can preserve collateral vessels (25,26). General morbidity, not surgical one was less in LLR (23) and low severity of morbidity was observed in LLR (24). In HCC patients requiring repeated treatments, reduced post-operative adhesion may allow successful laparoscopic radio-frequency ablation or LLR for the future recurrence (27). The hospital stay was shorter in all papers that were mentioned. Regarding to long-term outcome, disease-free or recurrence-free survival and overall survival were comparable in almost all studies. In one paper, overall survival was better in LLR compared to OLR and the better long-term survival was explained by significantly less blood loss and high frequency of non-touch anterior approach in LLR (23).

Less intraoperative blood loss or low rate of blood transfusion, and shorter hospital stay are solid beneficial advantages of LLR. Additionally, postoperative complication rates were significantly lower in a half of the patients compared to those in OLR. These less invasive futures of LLR can decrease the recurrence rates and can allow adequate treatment for the recurrence because of preserved liver function (28-32). Long-term outcome was quite equivalent in the two groups and special recurrence pattern in the LLR was rarely observed; therefore, LLR might have no obvious oncological disadvantages compared to OLR (13,16-24). Nevertheless, the utility of laparoscopic systematic resection or laparoscopic major resection was not fully understood.

These PSM studies clearly demonstrated that LLR can provide excellent perioperative benefits without oncologic disadvantages; therefore, LLR is strongly recommended as a standard practice for properly selected patients with HCC. In the future, advantages of LLR should be assessed minutely in consideration of the tumor location assessment (difficult location or not) or difficulty scoring system (15,17,33).

Acknowledgments

The authors give special thanks to the members of the “Project Committee of the Endoscopic Surgery” of the Japanese Society of Hepato-Biliary-Pancreatic Surgery for their tremendous contribution to data collection.

Funding: None.

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/ales.2017.05.11). Go Wakabayashi serves as an unpaid editorial board member of Annals of Laparoscopic and Endoscopic Surgery from Jun 2016 to May 2018. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

  1. Buell JF, Cherqui D, Geller DA, et al. World Consensus Conference on Laparoscopic Surgery. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 2009;250:825-30. [Crossref] [PubMed]
  2. Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection - 2,804 patients. Ann Surg 2009;250:831-41. [Crossref] [PubMed]
  3. Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic liver resection: A report from the 2nd International Consensus Conference Held in Morioka. Ann Surg 2015;261:619-29. [PubMed]
  4. Castaing D, Vibert E, Ricca L, et al. Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg 2009;250:849-55. [Crossref] [PubMed]
  5. Kazaryan AM, Marangos IP, Rosok BI, et al. Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome. Ann Surg 2010;252:1005-12. [Crossref] [PubMed]
  6. Vanounou T, Steel JL, Nguyen KT, et al. Comparing the clinical and economic impact of laparoscopic versus open liver resection. Ann Surg Oncol 2010;17:998-1009. [Crossref] [PubMed]
  7. Rao A, Rao G, Ahmed I. Laparoscopic or open liver resection? Let systematic review decide it. Am J Surg 2012;204:222-31. [Crossref] [PubMed]
  8. Parks KR, Kuo YH, Davis JM, et al. Laparoscopic versus open liver resection: a meta-analysis of long-term outcome. HPB (Oxford) 2014;16:109-18. [Crossref] [PubMed]
  9. Fretland ÅA, Kazaryan AM, Bjørnbeth BA, et al. Open versus laparoscopic liver resection for colorectal liver metastases (the Oslo-CoMet Study): study protocol for a randomized controlled trial. Trials 2015;16:73. [Crossref] [PubMed]
  10. Wong-Lun-Hing EM, van Dam RM, van Breukelen GJ, et al. Randomized clinical trial of open versus laparoscopic left lateral hepatic sectionectomy within an enhanced recovery after surgery programme (ORANGE II study). Br J Surg 2017; [Epub ahead of print]. [Crossref] [PubMed]
  11. Lonjon G, Boutron I, Trinquart L, et al. Comparison of treatment effect estimates from prospective nonrandomized studies with propensity score analysis and randomized controlled trials of surgical procedures. Ann Surg 2014;259:18-25. [Crossref] [PubMed]
  12. Beppu T, Imai K, Sakamoto Y, et al. Comparison of laparoscopic versus open liver resection for colorectal liver metastases using propensity score matching. Ann Laparosc Endosc Surg 2017;1:50. [Crossref]
  13. 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;22:721-7. [Crossref] [PubMed]
  14. Beppu T, Wakabayashi G, Hasegawa K, et al. Longterm and perioperative outcomes of laparoscopic versus open liver resection for colorectal liver metastases with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci 2015;22:711-20. [Crossref] [PubMed]
  15. Cho JY, Han HS, Yoon YS, et al. Feasibility of laparoscopic liver resection for tumors located in the posterosuperior segments of the liver, with a special reference to overcoming current limitations on tumor location. Surgery 2008;144:32-8. [Crossref] [PubMed]
  16. Kim H, Suh KS, Lee KW, et al. Long-term outcome of laparoscopic versus open liver resection for hepatocellular carcinoma: a case-controlled study with propensity score matching. Surg Endosc 2014;28:950-60. [Crossref] [PubMed]
  17. Beppu T, Hayashi H, Okabe H, et al. Hybrid-including endoscopic versus open hepatic resection for patients with hepatocellular carcinoma meeting the Milan criteria: a propensity case-matched analysis. Anticancer Res 2015;35:1583-90. [PubMed]
  18. Meguro M, Mizuguchi T, Kawamoto M, et al. Clinical comparison of laparoscopic and open liver resection after propensity matching selection. Surgery 2015;158:573-87. [Crossref] [PubMed]
  19. Han HS, Shehta A, Ahn S, et al. Laparoscopic versus open liver resection for hepatocellular carcinoma: Case-matched study with propensity score matching. J Hepatol 2015;63:643-50. [Crossref] [PubMed]
  20. Yoon SY, Kim KH, Jung DH, et al. Oncological and surgical results of laparoscopic versus open liver resection for HCC less than 5 cm: case-matched analysis. Surg Endosc 2015;29:2628-34. [Crossref] [PubMed]
  21. Sposito C, Battiston C, Facciorusso A, et al. Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg 2016;103:871-80. [Crossref] [PubMed]
  22. Han DH, Choi SH, Park EJ, et al. Surgical outcomes after laparoscopic or robotic liver resection in hepatocellular carcinoma: a propensity-score matched analysis with conventional open liver resection. Int J Med Robot 2016;12:735-42. [Crossref] [PubMed]
  23. 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;264:612-20. t. [Crossref] [PubMed]
  24. Yoon YI, Kim KH, Kang SH, et al. Pure Laparoscopic Versus Open Right Hepatectomy for Hepatocellular Carcinoma in Patients With Cirrhosis: A Propensity Score Matched Analysis. Ann Surg 2017;265:856-63. [Crossref] [PubMed]
  25. Kanazawa A, Tsukamoto T, Shimizu S, et al. Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc 2013;27:2592-7. [Crossref] [PubMed]
  26. Morise Z, Kawabe N, Kawase J, et al. Pure laparoscopic hepatectomy for hepatocellular carcinoma with chronic liver disease. World J Hepatol 2013;5:487-95. [Crossref] [PubMed]
  27. Doi K, Beppu T, Ishiko T, et al. Endoscopic radiofrequency ablation in elderly patients with hepatocellular carcinoma. Anticancer Res 2015;35:3033-40. [PubMed]
  28. Johnstone PA, Rohde DC, Swartz SE, et al. Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol 1996;14:1950-6. [Crossref] [PubMed]
  29. Gutt CN, Riemer V, Kim ZG, et al. Impact of laparoscopic surgery on experimental hepatic metastases. Br J Surg 2001;88:371-5. [Crossref] [PubMed]
  30. Chikamoto A, Beppu T, Masuda T, et al. Amount of operative blood loss affects the long-term outcome after liver resection for hepatocellular carcinoma. Hepatogastroenterology 2012;59:1213-6. [PubMed]
  31. Liu L, Miao R, Yang H, et al. Prognostic factors after liver resection for hepatocellular carcinoma: a single-center experience from China. Am J Surg 2012;203:741-50. [Crossref] [PubMed]
  32. Harimoto N, Shirabe K, Ikegami T, et al. Postoperative complications are predictive of poor prognosis in hepatocellular carcinoma. J Surg Res 2015;199:470-7. [Crossref] [PubMed]
  33. Ban D, Tanabe M, Ito H, et al. A novel difficulty scoring system for laparoscopic liver resection. J Hepatobiliary Pancreat Sci 2014;21:745-53. [Crossref] [PubMed]
doi: 10.21037/ales.2017.05.11
Cite this article as: Koga Y, Beppu T, Kuramoto K, Kinoshita K, Yoshida Y, Imai K, Takahara T, Nakamura M, Wakabayashi G, Baba H. Comparison of laparoscopic versus open liver resection for hepatocellular carcinoma using propensity score matching. Ann Laparosc Endosc Surg 2017;2:105.

Article Options

Download Citation

Share