Advertisement
Hepatic| Volume 171, ISSUE 5, P1290-1302, May 2022

Laparoscopic versus open liver resection for intrahepatic cholangiocarcinoma: Report of an international multicenter cohort study with propensity score matching

Published:September 14, 2021DOI:https://doi.org/10.1016/j.surg.2021.08.015

      Abstract

      Background

      Intrahepatic cholangiocarcinoma is a rare disease with a poor prognosis. In patients where surgical resection is possible, outcome is influenced by perioperative morbidity and lymph node status. Laparoscopic liver resection is associated with improved clinical and oncological outcomes in primary and metastatic liver cancer compared with open liver resection, but evidence on intrahepatic cholangiocarcinoma is still insufficient.
      The primary aim of this study was to compare overall survival for a large series of patients treated for intrahepatic cholangiocarcinoma by open or laparoscopic approach. Secondary objectives were to compare disease-free survival, predictors of death, and recurrence.

      Methods

      Patients treated with laparoscopic or open liver resection for intrahepatic cholangiocarcinoma from 2000 to 2018 from 3 large international databases were analyzed retrospectively. Each patient in the laparoscopic resection group (case) was matched with 1 open resection control (1:1 ratio), through a propensity score calculated on clinically relevant preoperative covariates. Overall and disease-free survival were compared between the matched groups. Predictors of mortality and recurrence were analyzed with Cox regression, and the Textbook Outcomes were described.

      Results

      During the study period, 855 patients met the inclusion criteria (open liver resection = 709, 82.9%; laparoscopic liver resection = 146, 17.1%). Two groups of 89 patients each were analyzed after propensity score matching, with no significant difference regarding pre- and postoperative variables. Overall survival at 1, 3, and 5 years was 92%, 75%, and 63% in the laparoscopic liver resection group versus 92%, 58%, and 49% in the open liver resection group (P = .0043). Adjusted Cox regression revealed severe postoperative complications (hazard ratio: 10.5, 95% confidence interval [1.01–109] P = .049) and steatosis (hazard ratio: 13.8, 95% confidence interval [1.23–154] P = .033) as predictors of death, and transfusion (hazard ratio: 19.2, 95% confidence interval [4.04–91.4] P < .001) and severe postoperative complications (hazard ratio: 4.07, 95% confidence interval [1.15–14.4] P = .030) as predictors of recurrence.

      Conclusion

      The survival advantage of laparoscopic liver resection over open liver resection for intrahepatic cholangiocarcinoma is equivocal, given historical bias and missing data.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Razumilava N.
        • Gores G.J.
        Cholangiocarcinoma.
        Lancet (London, England). 2014; 383: 2168-2179
        • Mavros M.N.
        • Economopoulos K.P.
        • Alexiou V.G.
        • Pawlik T.M.
        Treatment and prognosis for patients with intrahepatic cholangiocarcinoma.
        JAMA Surg. 2014; 149: 565
        • Shaib Y.
        • El-Serag H.
        The epidemiology of cholangiocarcinoma.
        Semin Liver Dis. 2004; 24: 115-125
        • DeOliveira M.L.
        • Cunningham S.C.
        • Cameron J.L.
        • et al.
        Cholangiocarcinoma: thirty-one-year experience with 564 patients at a single institution.
        Ann Surg. 2007; 245: 755-762
        • Brustia R.
        • Langella S.
        • Kawai T.
        • et al.
        Preoperative risk score for prediction of long-term outcomes after hepatectomy for intrahepatic cholangiocarcinoma: report of a collaborative, international-based, external validation study.
        Eur J Surg Oncol. November 2020; 46: 560-571
        • Bagante F.
        • Spolverato G.
        • Cucchetti A.
        • et al.
        Defining when to offer operative treatment for intrahepatic cholangiocarcinoma: a regret-based decision curves analysis.
        Surgery. 2016; 160: 106-117
        • Spolverato G.
        • Kim Y.
        • Alexandrescu S.
        • et al.
        Is hepatic resection for large or multifocal intrahepatic cholangiocarcinoma justified? Results from a multi-institutional collaboration.
        Ann Surg Oncol. 2015; 22: 2218-2225
        • Spolverato G.
        • Yakoob M.Y.
        • Kim Y.
        • et al.
        The impact of surgical margin status on long-term outcome after resection for intrahepatic cholangiocarcinoma.
        Ann Surg Oncol. 2015; 22: 4020-4028
        • Bektas H.
        • Yeyrek C.
        • Kleine M.
        • et al.
        Surgical treatment for intrahepatic cholangiocarcinoma in Europe: a single center experience.
        J Hepatobiliary Pancreat Sci. 2015; 22: 131-137
        • 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
        • Kim J.M.
        • Kwon C.H.D.
        • Yoo H.
        • et al.
        Which approach is preferred in left hepatocellular carcinoma? Laparoscopic versus open hepatectomy using propensity score matching.
        BMC Cancer. 2018; 18
        • Komatsu S.
        • Brustia R.
        • Goumard C.
        • Perdigao F.
        • Soubrane O.
        • Scatton O.
        Laparoscopic versus open major hepatectomy for hepatocellular carcinoma: a matched pair analysis.
        Surg Endosc Other Interv Tech. 2016; 30
        • Beppu T.
        • Wakabayashi G.
        • Hasegawa K.
        • et al.
        Long-term 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: 711-720
        • Nachmany I.
        • Pencovich N.
        • Zohar N.
        • et al.
        Laparoscopic versus open liver resection for metastatic colorectal cancer.
        Eur J Surg Oncol. 2015; 41: 1615-1620
        • 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
        • Syn N.L.
        • Kabir T.
        • Koh Y.X.
        • et al.
        Survival advantage of laparoscopic versus open resection for colorectal liver metastases: a meta-analysis of individual patient data from randomized trials and propensity-score matched studies.
        Ann Surg. 2019; 22: 22
        • Aghayan D.L.
        • Kazaryan A.M.
        • Dagenborg V.J.
        • et al.
        Long-term oncologic outcomes after laparoscopic versus open resection for colorectal liver metastases: a randomized trial.
        Ann Intern Med. 2021; 174: 175-182
        • El-Gendi A.
        • El-Shafei M.
        • El-Gendi S.
        • Shawky A.
        Laparoscopic versus open hepatic resection for solitary hepatocellular carcinoma less than 5 cm in cirrhotic patients: a randomized controlled study.
        J Laparoendosc Adv Surg Tech A. 2018; 28: 302-310
        • Wei F.
        • Wang G.
        • Ding J.
        • Dou C.
        • Yu T.
        • Zhang C.
        Is it time to consider laparoscopic hepatectomy for intrahepatic cholangiocarcinoma? A meta-analysis.
        J Gastrointest Surg. 2020; 24: 2244-2250
        • Hobeika C.
        • Nault J.C.
        • Barbier L.
        • et al.
        Influence of surgical approach and quality of resection on the probability of cure for early-stage HCC occurring in cirrhosis.
        JHEP Reports. 2020; 2100153
        • Tsilimigras D.I.
        • Mehta R.
        • Merath K.
        • et al.
        Hospital variation in textbook outcomes following curative-intent resection of hepatocellular carcinoma: an international multi-institutional analysis.
        HPB. 2020; 22: 1305-1313
        • Farges O.
        • Fuks D.
        • Le Treut Y.P.
        • et al.
        AJCC 7th edition of TNM staging accurately discriminates outcomes of patients with resectable intrahepatic cholangiocarcinoma.
        Cancer. 2011; 117: 2170-2177
        • von Elm E.
        • Altman D.G.
        • Egger M.
        • et al.
        The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies.
        Lancet. 2007; 370: 1453-1457
        • Merath K.
        • Chen Q.
        • Bagante F.
        • et al.
        A multi-institutional international analysis of textbook outcomes among patients undergoing curative-intent resection of intrahepatic cholangiocarcinoma.
        JAMA Surg. 2019; 154
        • Kawaguchi Y.
        • Hasegawa K.
        • Tzeng C.W.D.
        • et al.
        Performance of a modified three-level classification in stratifying open liver resection procedures in terms of complexity and postoperative morbidity.
        Br J Surg. 2020; 107: 258-267
        • Kawaguchi Y.
        • Fuks D.
        • Kokudo N.
        • Gayet B.
        Difficulty of laparoscopic liver resection.
        Ann Surg. 2018; 267: 13-17
        • Bridgewater J.
        • Galle P.R.
        • Khan S.A.
        • et al.
        Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma.
        J Hepatol. 2014; 60: 1268-1289
      1. Amin M. Edge S. Greene F. AJCC Cancer Staging Manual. 8th Edition. Springer International Publishing: American Joint Commission on Cancer, 2017
        • Zhang X.F.
        • Chakedis J.
        • Bagante F.
        • et al.
        Trends in use of lymphadenectomy in surgery with curative intent for intrahepatic cholangiocarcinoma.
        Br J Surg. 2018; 105: 857-866
        • Dindo D.
        • Demartines N.
        • Clavien P.A.
        Classification of surgical complications.
        Ann Surg. 2004; 240: 205-213
        • Kang S.H.
        • Choi Y.R.
        • Lee W.
        • et al.
        Laparoscopic liver resection versus open liver resection for intrahepatic cholangiocarcinoma: 3-year outcomes of a cohort study with propensity score matching.
        Surg Oncol. 2020; 33: 63-69
        • Chen K.
        • Pan Y.
        • Zhang B.
        • Liu X.L.
        • Maher H.
        • Zheng X.Y.
        Laparoscopic versus open surgery for hepatocellular carcinoma: a meta-analysis of high-quality case-matched studies.
        Can J Gastroenterol Hepatol. 2018; 2018: 1746895
        • Yamamoto M.
        • Kobayashi T.
        • Oshita A.
        • et al.
        Laparoscopic versus open limited liver resection for hepatocellular carcinoma with liver cirrhosis: a propensity score matching study with the Hiroshima Surgical study group of Clinical Oncology (HiSCO).
        Surg Endosc. 2020; 34: 5055-5061
        • Wang Z.Y.
        • Chen Q.L.
        • Sun L.L.
        • et al.
        Laparoscopic versus open major liver resection for hepatocellular carcinoma: systematic review and meta-analysis of comparative cohort studies.
        BMC Cancer. 2019; 19: 1047
        • Brustia R.
        • Fleres F.
        • Tamby E.
        • et al.
        Postoperative collections after liver surgery: risk factors and impact on long-term outcomes.
        J Visc Surg. 2020; 157: 199-209
        • Margonis G.A.
        • Sasaki K.
        • Andreatos N.
        • et al.
        Prognostic impact of complications after resection of early stage hepatocellular carcinoma.
        J Surg Oncol. 2017; 115: 791-804
        • Sasaki K.
        • Margonis G.A.
        • Andreatos N.
        • et al.
        Preoperative risk score and prediction of long-term outcomes after hepatectomy for intrahepatic cholangiocarcinoma.
        J Am Coll Surg. 2018; 226: 393-403
        • Martin S.P.
        • Drake J.
        • Wach M.M.
        • et al.
        Laparoscopic approach to intrahepatic cholangiocarcinoma is associated with an exacerbation of inadequate nodal staging.
        Ann Surg Oncol. 2019; 26: 1851-1857
        • Yoh T.
        • Cauchy F.
        • Le Roy B.
        • et al.
        Prognostic value of lymphadenectomy for long-term outcomes in node-negative intrahepatic cholangiocarcinoma: a multicenter study.
        Surgery. 2019; 166: 975-982
        • Feng L.F.
        • Yan P.J.
        • Chu X.J.
        • et al.
        A scientometric study of the top 100 most-cited publications based on Web of Science of robotic surgery versus laparoscopic surgery.
        Asian J Surg. 2021; 44: 440-451
        • Byun Y.
        • Choi Y.J.
        • Kang J.S.
        • et al.
        Early outcomes of robotic extended cholecystectomy for the treatment of gallbladder cancer.
        J Hepatobiliary Pancreat Sci. 2020; 27: 324-330
        • Byun Y.
        • Choi Y.J.
        • Kang J.S.
        • et al.
        Robotic extended cholecystectomy in gallbladder cancer.
        Surg Endosc. 2020; 34: 3256-3261
        • Napoli N.
        • Kauffmann E.F.
        • Menonna F.
        • Iacopi S.
        • Cacace C.
        • Boggi U.
        Robot-assisted radical antegrade modular pancreatosplenectomy including resection and reconstruction of the spleno-mesenteric junction.
        J Vis Exp. 2020; 3
        • Hameed I.
        • Aggarwal P.
        • Weiser M.R.
        Robotic extended right hemicolectomy with complete mesocolic excision and D3 lymph node dissection.
        Ann Surg Oncol. 2019; 26: 3990-3991
        • Chong E.H.
        • Choi S.H.
        Hybrid laparoscopic and robotic hepatopancreaticoduodenectomy for cholangiocarcinoma.
        J Gastrointest Surg. 2019; 23: 1947-1948
        • Amini N.
        • Margonis G.A.
        • Kim Y.
        • Wilson A.
        • Gani F.
        • Pawlik T.M.
        Complication timing impacts 30-d mortality after hepatectomy.
        J Surg Res. 2016; 203: 495-506
        • Matsuda A.
        • Matsumoto S.
        • Seya T.
        • et al.
        Does postoperative complication have a negative impact on long-term outcomes following hepatic resection for colorectal liver metastasis?: a meta-analysis.
        Ann Surg Oncol. 2013; 20: 2485-2492
        • Melloul E.
        • Hübner M.
        • Scott M.
        • et al.
        Guidelines for perioperative care for liver surgery: Enhanced Recovery After Surgery (ERAS) Society recommendations.
        World J Surg. 2016; 40: 2425-2440
        • Ljungqvist O.
        • Scott M.
        • Fearon K.C.
        Enhanced recovery after surgery.
        JAMA Surg. 2017; 152: 292
        • Chalmers I.
        • Glasziou P.
        Avoidable waste in the production and reporting of research evidence.
        Lancet. 2009; 374: 86-89
        • Yordanov Y.
        • Dechartres A.
        • Atal I.
        • et al.
        Avoidable waste of research related to outcome planning and reporting in clinical trials.
        BMC Med. 2018; 16: 87
        • Mansukhani N.A.
        • Patti M.G.
        • Kibbe M.R.
        Rebranding “the lab years” as “professional development” in order to redefine the modern surgeon scientist.
        Ann Surg. 2017; 266: 937-938