Laparoscopic Parenchymal-Sparing Hepatectomy for Multiple Colorectal Liver Metastases Improves Outcomes and Salvageability: A Propensity Score-Matched Analysis

  • Shinya Okumura
  • Nicolas Tabchouri
  • Universe Leung
  • Pascale Tinguely
  • Christophe Louvet
  • Marc Beaussier
  • Brice Gayet
  • David FuksEmail author
Hepatobiliary Tumors



Parenchymal-sparing hepatectomy (PSH) is regarded as the standard of care for colorectal liver metastases (CRLMs) in open surgery. However, the surgical and oncological benefits of laparoscopic PSH compared with laparoscopic major hepatectomy (MH) have not been fully documented.


A total of 269 patients who underwent initial laparoscopic liver resections with curative intent for CRLMs between 2004 and 2017 were enrolled. Preoperative patient characteristics and tumor burden were adjusted with propensity score matching, and laparoscopic PSH was compared with laparoscopic MH after matching.


PSH was performed in 148 patients, while MH was performed in 121 patients. After propensity score matching, 82 PSH and 82 MH patients showed similar preoperative characteristics. PSH was associated with lower rates of major postoperative complications compared with MH (6.1 vs. 15.9%; p = 0.046). Recurrence-free survival (RFS) and liver-specific RFS rates were comparable between both groups (p = 0.595 and 0.683). Repeat hepatectomy for liver recurrence was more frequently performed in the PSH group (63.9 vs. 36.4%; p = 0.022), and the PSH group also showed a trend toward a higher overall survival (OS) rate (5-year OS 79.4 vs. 64.3%; p = 0.067). Multivariate analyses revealed that initial MH was one of the risk factors to preclude repeat hepatectomy after liver recurrence (hazard ratio 2.39, p = 0.047).


Laparoscopic PSH provided surgical and oncological benefits for CRLMs, with less complications, similar recurrence rates, and increased salvageability through repeat hepatectomy, compared with laparoscopic MH. PSH should be the standard approach, even in laparoscopic procedures.



No financial support was received from any sources for this study.


Shinya Okumura, Nicolas Tabchouri, Universe Leung, Pascale Tinguely, Christophe Louvet, Marc Beaussier, Brice Gayet, and David Fuks have no conflicts of interest to declare in relation to this study.


  1. 1.
    Adam R, De Gramont A, Figueras J, Guthrie A, Kokudo N, Kunstlinger F, et al. The oncosurgery approach to managing liver metastases from colorectal cancer: a multidisciplinary international consensus. The oncologist 2012; 17: 1225–39.CrossRefGoogle Scholar
  2. 2.
    Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, et al. Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 2002; 235: 759–66.CrossRefGoogle Scholar
  3. 3.
    Adams RB, Aloia TA, Loyer E, Pawlik TM, Taouli B, Vauthey JN. Selection for hepatic resection of colorectal liver metastases: expert consensus statement. HPB (Oxford). 2013; 15: 91–103.CrossRefGoogle Scholar
  4. 4.
    Mise Y, Aloia TA, Brudvik KW, Schwarz L, Vauthey JN, Conrad C. Parenchymal-sparing hepatectomy in colorectal liver metastasis improves salvageability and survival. Ann Surg 2016; 263: 146–52.CrossRefGoogle Scholar
  5. 5.
    Hosokawa I, Allard MA, Mirza DF, Kaiser G, Barroso E, Lapointe R, et al. Outcomes of parenchyma-preserving hepatectomy and right hepatectomy for solitary small colorectal liver metastasis: A LiverMetSurvey study. Surgery 2017; 162: 223–32.CrossRefGoogle Scholar
  6. 6.
    Andreou A, Brouquet A, Abdalla EK, Aloia TA, Curley SA, Vauthey JN. Repeat hepatectomy for recurrent colorectal liver metastases is associated with a high survival rate. HPB Oxford. 2011; 13: 774–82.CrossRefGoogle Scholar
  7. 7.
    Butte JM, Gonen M, Allen PJ, Peter Kingham T, Sofocleous CT, DeMatteo RP, et al. Recurrence after partial hepatectomy for metastatic colorectal cancer: potentially curative role of salvage repeat resection. Ann Surg Oncol 2015; 22: 2761–71.CrossRefGoogle Scholar
  8. 8.
    Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, et al. The international position on laparoscopic liver surgery: the Louisville Statement, 2008. Ann Surg 2009; 250: 825–30.CrossRefGoogle Scholar
  9. 9.
    Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg 2009; 250: 831–41.CrossRefGoogle Scholar
  10. 10.
    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 2015; 261: 619–29.PubMedGoogle Scholar
  11. 11.
    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: 761–77.CrossRefGoogle Scholar
  12. 12.
    Fretland AA, Dagenborg VJ, Bjornelv GMW, Kazaryan AM, Kristiansen R, Fagerland MW, et al. Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET randomized controlled trial. Ann Surg 2018; 267: 199–207.CrossRefGoogle Scholar
  13. 13.
    Cui CH, Huang SX, Qi J, Zhu HJ, Huang ZH, Yu JL. Neoadjuvant chemotherapy (NCT) plus targeted agents versus NCT alone in colorectal liver metastases patients: a systematic review and meta-analysis. Oncotarget 2015; 6: 44005–18.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Couinaud C. Liver anatomy: portal (and suprahepatic) or biliary segmentation. Dig Surg 1999; 16: 459–67.CrossRefGoogle Scholar
  15. 15.
    Ogiso S, Conrad C, Araki K, Nomi T, Anil Z, Gayet B. Laparoscopic transabdominal with transdiaphragmatic access improves resection of difficult posterosuperior liver lesions. Ann Surg 2015; 262: 358–65.CrossRefGoogle Scholar
  16. 16.
    Fuks D, Gayet B. Laparoscopic surgery of postero-lateral segments: a comparison between transthoracic and abdominal approach. Updat Surg 2015; 67: 141–5.CrossRefGoogle Scholar
  17. 17.
    Araki K, Conrad C, Ogiso S, Kuwano H, Gayet B. Intraoperative ultrasonography of laparoscopic hepatectomy: key technique for safe liver transection. J Am Coll Surg 2014; 218: e37–41.CrossRefGoogle Scholar
  18. 18.
    Ishizawa T, Gumbs AA, Kokudo N, Gayet B. Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 2012; 256: 959–64.CrossRefGoogle Scholar
  19. 19.
    Gayet B, Cavaliere D, Vibert E, Perniceni T, Levard H, Denet C, et al. Totally laparoscopic right hepatectomy. Am J Surg 2007; 194: 685–9.CrossRefGoogle Scholar
  20. 20.
    Ogiso S, Nomi T, Araki K, Conrad C, Hatano E, Uemoto S, et al. Laparoscopy-specific surgical concepts for hepatectomy based on the laparoscopic caudal view: a key to reboot surgeons’ minds. Ann Surg Oncol 2015; 22 Suppl 3: S327–33.CrossRefGoogle Scholar
  21. 21.
    Dindo D, Demartines N, Clavien P-A. Classification of surgical complications. Ann Surg 2004; 240: 205–13.CrossRefGoogle Scholar
  22. 22.
    Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien PA. The comprehensive complication index: a novel continuous scale to measure surgical morbidity. Ann Surg 2013; 258: 1–7.CrossRefGoogle Scholar
  23. 23.
    Rahbari NN, Garden OJ, Padbury R, Brooke-Smith M, Crawford M, Adam R, et al. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 2011; 149: 713–24.CrossRefGoogle Scholar
  24. 24.
    Ishizawa T, Hasegawa K, Kokudo N, Sano K, Imamura H, Beck Y, et al. Risk factors and management of ascites after liver resection to treat hepatocellular carcinoma. Arch Surg 2009; 144: 46–51.CrossRefGoogle Scholar
  25. 25.
    Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, et al. Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery 2011; 149: 680–8.CrossRefGoogle Scholar
  26. 26.
    Lemeshow S, Hosmer DW Jr. A review of goodness of fit statistics for use in the development of logistic regression models. Am J Epidemiol 1982; 115: 92–106.CrossRefGoogle Scholar
  27. 27.
    Gold JS, Are C, Kornprat P, Jarnagin WR, Gonen M, Fong Y, et al. Increased use of parenchymal-sparing surgery for bilateral liver metastases from colorectal cancer is associated with improved mortality without change in oncologic outcome: trends in treatment over time in 440 patients. Ann Surg 2008; 247: 109–17.CrossRefGoogle Scholar
  28. 28.
    Kokudo N, Tada K, Seki M, Ohta H, Azekura K, Ueno M, et al. Anatomical major resection versus nonanatomical limited resection for liver metastases from colorectal carcinoma. Am J Surg 2001; 181: 153–9.CrossRefGoogle Scholar
  29. 29.
    Lalmahomed ZS, Ayez N, van der Pool AEM, Verheij J, IJzermans JNM, et al. Anatomical versus nonanatomical resection of colorectal liver metastases: Is there a difference in surgical and oncological outcome?. World J Surg 2011; 35: 656–61.CrossRefGoogle Scholar
  30. 30.
    Cipriani F, Shelat VG, Rawashdeh M, Francone E, Aldrighetti L, Takhar A, et al. Laparoscopic parenchymal-sparing resections for nonperipheral liver lesions, the diamond technique: technical aspects, clinical outcomes, and oncologic efficiency. J Am Coll Surg 2015; 221: 265–72.CrossRefGoogle Scholar
  31. 31.
    Kawaguchi Y, Fuks D, Kokudo N, Gayet B. Difficulty of laparoscopic liver resection: proposal for a new classification. Ann Surg 2018; 267: 13–7.CrossRefGoogle Scholar
  32. 32.
    Hasegawa Y, Wakabayashi G, Nitta H, Takahara T, Katagiri H, Umemura A, et al. A novel model for prediction of pure laparoscopic liver resection surgical difficulty. Surg Endosc 2017; 31: 5356–63.CrossRefGoogle Scholar
  33. 33.
    Conrad C, Ogiso S, Inoue Y, Shivathirthan N, Gayet B. Laparoscopic parenchymal-sparing liver resection of lesions in the central segments: feasible, safe, and effective. Surg Endosc 2015; 29: 2410–7.CrossRefGoogle Scholar
  34. 34.
    Cady B, Jenkins RL, Steele GD Jr, Lewis WD, Stone MD, McDermott WV, et al. Surgical margin in hepatic resection for colorectal metastasis: a critical and improvable determinant of outcome. Ann Surg 1998; 227: 566–71.CrossRefGoogle Scholar
  35. 35.
    Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, et al. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Francaise de Chirurgie. Cancer 1996; 77: 1254–62.CrossRefGoogle Scholar
  36. 36.
    Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C, et al. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 2005; 241: 715–22 (discussion 722–14)CrossRefGoogle Scholar
  37. 37.
    Muratore A, Ribero D, Zimmitti G, Mellano A, Langella S, Capussotti L. Resection margin and recurrence-free survival after liver resection of colorectal metastases. Ann Surg Oncol 2010; 17: 1324–29.CrossRefGoogle Scholar
  38. 38.
    Hamady ZZ, Lodge JP, Welsh FK, Toogood GJ, White A, John T, et al. One-millimeter cancer-free margin is curative for colorectal liver metastases: a propensity score case-match approach. Ann Surg 2014; 259: 543–8.CrossRefGoogle Scholar
  39. 39.
    Yamashita S, Venkatesan A, Mizuno T, Aloia T, Chun Y, Lee J et al. Remnant liver ischemia as a prognostic factor for cancer-specific survival after resection of colorectal liver metastases. JAMA Surg 2017; 152(10):e172986.CrossRefGoogle Scholar
  40. 40.
    Moris D, Ronnekleiv-Kelly S, Rahnemai-Azar AA, Felekouras E, Dillhoff M, Schmidt C, et al. Parenchymal-sparing versus anatomic liver resection for colorectal liver metastases: a systematic review. J Gastrointest Surg 2017; 21: 1076–85.CrossRefGoogle Scholar
  41. 41.
    41. Vigano L, Procopio F, Cimino M, Donadon M, Gatti A, Costa G et al. Is tumor detachment from vascular structures equivalent to R0 resection in surgery for colorectal liver metastases? An observational cohort. Ann Surg Oncol 2016; 23:1352–60CrossRefGoogle Scholar
  42. 42.
    Margonis G, Sasaki K, Andreatos N, Kim Y, Merath K, Wagner D et al. KRAS mutation status dictates optimal surgical margin width in patients undergoing resection of colorectal liver metastases. Ann Surg Oncol 2017; 24(1):264–71.CrossRefGoogle Scholar
  43. 43.
    Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M. Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer 2006; 94: 982–99.CrossRefGoogle Scholar
  44. 44.
    Narita M, Oussoultzoglou E, Bachellier P, Jaeck D, Uemoto S. Post-hepatectomy liver failure in patients with colorectal liver metastases. Surg Today 2015; 45: 1218–26.CrossRefGoogle Scholar
  45. 45.
    Yamashita S, Shindoh J, Mizuno T, Chun YS, Conrad C, Aloia TA, et al. Hepatic atrophy following preoperative chemotherapy predicts hepatic insufficiency after resection of colorectal liver metastases. J Hepatol 2017; 67: 56–64.CrossRefGoogle Scholar
  46. 46.
    Aloia TA, Vauthey JN, Loyer EM, Ribero D, Pawlik TM, Wei SH, et al. Solitary colorectal liver metastasis: resection determines outcome. Arch Surg 2006; 141: 460–466 (discussion 466–7)CrossRefGoogle Scholar
  47. 47.
    Ratti F, Fiorentini G, Cipriani F, Catena M, Paganelli M, Aldrighetti L. Laparoscopic vs open surgery for colorectal liver metastases. JAMA Surg 2018; 153(11): 1028–35.CrossRefGoogle Scholar
  48. 48.
    Hallet J, Sa Cunha A, Adam R, Goéré D, Bachellier P, Azoulay D, et al. Factors influencing recurrence following initial hepatectomy for colorectal liver metastases. Br J Surg 2016; 103:1366–76CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2019

Authors and Affiliations

  • Shinya Okumura
    • 1
  • Nicolas Tabchouri
    • 1
  • Universe Leung
    • 1
  • Pascale Tinguely
    • 1
  • Christophe Louvet
    • 2
  • Marc Beaussier
    • 3
  • Brice Gayet
    • 1
  • David Fuks
    • 1
    Email author
  1. 1.Department of Digestive, Oncologic and Metabolic Surgery, Institut Mutualiste MontsourisUniversity of ParisParisFrance
  2. 2.Department of OncologyInstitut Mutualiste MontsourisParisFrance
  3. 3.Department of AnesthesiologyInstitut Mutualiste MontsourisParisFrance

Personalised recommendations