Surgical Endoscopy

, Volume 32, Issue 12, pp 4788–4797 | Cite as

Recurrence patterns after laparoscopic resection of colorectal liver metastases

  • Nicolas Tabchouri
  • Brice Gayet
  • Shinya Okumura
  • Gianfranco Donatelli
  • Marc Beaussier
  • Mostefa Bennamoun
  • Christophe Louvet
  • David FuksEmail author



The major issue after liver resection for colorectal liver metastases (CRLM) is the high incidence of recurrence. Unlike open liver resection (OLR), recurrence following laparoscopic liver resection (LLR) is not well documented. The aim of this study was to analyze recurrence patterns and treatment following LLR for CRLM.

Study design

All patients who underwent LLR for CRLM from 2000 to 2016 were reviewed. Patients who presented with recurrence were compared to those who did not. Recurrence-free survival (RFS), overall survival (OS), and risk of recurrence and survival prognostic factors were analyzed.


Overall, 273 patients were included, of which 157 (57.5%) were treated for one liver metastasis (LM). Median follow-up was 41 (12–187) months and associated extrahepatic disease was present in 27% of patients (mainly pulmonary, 65%). After a median of 16 (3–151) months, 197 (72%) patients presented with recurrence. Recurrences were early (< 6 months) in 22.8% of cases, occured in a single site in 66% and were intrahepatic, extrahepatic, or both in 44, 30, and 26%, respectively. Recurrences were treated with surgery or chemotherapy only in 45 and 47%, respectively. 3-, 5-, and 10-year OS was 82, 71, and 43%, respectively. Independent risk factors for recurrence were node-positive primary tumor, extrahepatic disease before hepatectomy, and R1 resection.


LLR for CRLM does not seem to be associated with distinctive recurrence patterns. LLR for CRLM yielded satisfying RFS and OS and should therefore be considered whenever possible.


Colorectal liver metastases Laparoscopic liver resection Recurrence Management 



Colorectal liver metastases


Overall survival


Radiofrequency ablation


Laparoscopic liver resection


Open liver resection


Comprehensive complication index


Recurrence-free survival


Extrahepatic disease


Computerized tomography scanner


Magnetic resonance imaging


Compliance with ethical standards


The authors Nicolas Tabchouri, Brice Gayet, Shinya Okumura, Gianfranco Donatelli, Marc Beaussier, Mostefa Bennamoun, Christophe Louvet, and David Fuks have nothing to declare.


  1. 1.
    McMillan DC, McArdle CS (2007) Epidemiology of colorectal liver metastases. Surg Oncol 16(1):3–5CrossRefGoogle Scholar
  2. 2.
    Beamish P, Lemke M, Li J, Dixon E, Abraham MT, Alejandro RH et al (2017) Validation of clinical risk score for colorectal liver metastases resected in a contemporary multicenter cohort. HPB [Internet]. Accessed 5 Jul 2017
  3. 3.
    Jones RP, Kokudo N, Folprecht G, Mise Y, Unno M, Malik HZ et al (2017) Colorectal liver metastases: a critical review of state of the art. Liver Cancer 6(1):66–71CrossRefGoogle Scholar
  4. 4.
    Neal CP, Nana GR, Jones M, Cairns V, Ngu W, Isherwood J et al (2017 Feb) Repeat hepatectomy is independently associated with favorable long-term outcome in patients with colorectal liver metastases. Cancer Med 6(2):331–338CrossRefGoogle Scholar
  5. 5.
    Viganò L, Capussotti L, Lapointe R, Barroso E, Hubert C, Giuliante F et al (2014) Early recurrence after liver resection for colorectal metastases: risk factors, prognosis, and treatment. A LiverMetSurvey-based study of 6,025 patients. Ann Surg Oncol 21(4):1276–1286CrossRefGoogle Scholar
  6. 6.
    Hallet J, Sa Cunha A, Adam R, Goéré D, Bachellier P, Azoulay D et al (2016 ) Factors influencing recurrence following initial hepatectomy for colorectal liver metastases: recurrence following initial hepatectomy for colorectal liver metastases. Br J Surg 103(10):1366–1376CrossRefGoogle Scholar
  7. 7.
    Nomi T, Fuks D, Ogiso S, Nakajima Y, Louvet C, Gayet B (2016) Second and third laparoscopic liver resection for patients with recurrent colorectal liver metastases. Ann Surg 263(5):e68–e72CrossRefGoogle Scholar
  8. 8.
    Malik HZ, Gomez D, Wong V, Al-Mukthar A, Toogood GJ, Lodge JPA et al (2007) Predictors of early disease recurrence following hepatic resection for colorectal cancer metastasis. Eur J Surg Oncol EJSO 33(8):1003–1009CrossRefGoogle Scholar
  9. 9.
    Takahashi M, Hasegawa K, Oba M, Aoki T, Sakamoto Y, Sugawara Y et al (2015) Repeat resection leads to long-term survival: analysis of 10-year follow-up of patients with colorectal liver metastases. Am J Surg 210(5):904–910CrossRefGoogle Scholar
  10. 10.
    Zhang X-L, Liu R-F, Zhang D, Zhang Y-S, Wang T (2017) Laparoscopic versus open liver resection for colorectal liver metastases: a systematic review and meta-analysis of studies with propensity score-based analysis. Int J Surg 44:191–203CrossRefGoogle Scholar
  11. 11.
    Martínez-Cecilia D, Cipriani F, Vishal S, Ratti F, Tranchart H, Barkhatov L et al (2017) Laparoscopic versus open liver resection for colorectal metastases in elderly and octogenarian patients: a multicenter propensity score based analysis of short- and long-term outcomes. Ann Surg 265(6):1192–1200CrossRefGoogle Scholar
  12. 12.
    Scuderi V, Barkhatov L, Montalti R, Ratti F, Cipriani F, Pardo F et al (2017) Outcome after laparoscopic and open resections of posterosuperior segments of the liver: Laparoscopic versus open resection of posterosuperior hepatic segments. Br J Surg 104(6):751–759CrossRefGoogle Scholar
  13. 13.
    Allard M-A, Cunha AS, Gayet B, Adam R, Goere D, Bachellier P et al (2015) Early and long-term oncological outcomes after laparoscopic resection for colorectal liver metastases: a propensity score-based analysis. Ann Surg 262(5):794–802CrossRefGoogle Scholar
  14. 14.
    Xie S-M, Xiong J-J, Liu X-T, Chen H-Y, Iglesia-García D, Altaf K et al (2017). Laparoscopic versus open liver resection for colorectal liver metastases: a comprehensive systematic review and meta-analysis. Sci Rep 7(1):1012. Accessed 5 Jul 2017
  15. 15.
    Fretland AA, Dagenborg VJ, Bjornelv GMW, Kazaryan AM, Kristiansen R, Fagerlang MW et al (2017) Laparoscopic versus open resection for colorectal liver metastases. Ann Surg 267:199–207CrossRefGoogle Scholar
  16. 16.
    House MG (2016) Laparoscopic resection for recurrent hepatic colorectal metastases. Ann Surg 263(5):e73CrossRefGoogle Scholar
  17. 17.
    Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH (1999) Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 230(3):309CrossRefGoogle Scholar
  18. 18.
    Matsuda A, Matsumoto S, Seya T, Matsutani T, Kishi T, Yokoi K et al (2013) Does postoperative complication have a negative impact on long-term outcomes following hepatic resection for colorectal liver metastasis?: A meta-analysis. Ann Surg Oncol 20(8):2485–2492CrossRefGoogle Scholar
  19. 19.
    Okimoto S, Kobayashi T, Tashiro H, Kuroda S, Ishiyama K, Ide K et al (2017) Significance of the glasgow prognostic score for patients with colorectal liver metastasis. Int J Surg 42:209–214CrossRefGoogle Scholar
  20. 20.
    Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357(9255):539–545CrossRefGoogle Scholar
  21. 21.
    Moon Y-J, Jun I-G, Kim K-H, Kim S-O, Song J-G, Hwang G-S (2017) Comparison of acute kidney injury between open and laparoscopic liver resection: propensity score analysis. PLoS ONE 12(10):e0186336CrossRefGoogle Scholar
  22. 22.
    Welsh FKS, Tekkis PP, John TG, Rees M (2008) Predictive models in colorectal liver metastases—can we personalize treatment and outcome? Dig Surg 25(6):406–412CrossRefGoogle Scholar
  23. 23.
    Nomi T, Fuks D, Kawaguchi Y, Mal F, Nakajima Y, Gayet B (2015) Laparoscopic major hepatectomy for colorectal liver metastases in elderly patients: a single-center, case-matched study. Surg Endosc 29(6):1368–1375CrossRefGoogle Scholar
  24. 24.
    Nomi T, Fuks D, Govindasamy M, Mal F, Nakajima Y, Gayet B (2015) Risk factors for complications after laparoscopic major hepatectomy. Br J Surg 102(3):254–260CrossRefGoogle Scholar
  25. 25.
    Nomi T, Fuks D, Kawaguchi Y, Mal F, Nakajima Y, Gayet B (2015) Learning curve for laparoscopic major hepatectomy. Br J Surg 102(7):796–804CrossRefGoogle Scholar
  26. 26.
    Nomi T, Fuks D, Agrawal A, Govindasamy M, Araki K, Gayet B (2015) Modified pringle maneuver for laparoscopic liver resection. Ann Surg Oncol 22(3):852–852CrossRefGoogle Scholar
  27. 27.
    Nomi T, Fuks D, Agrawal A, Kawaguchi Y, Ogiso S, Gayet B (2015) Totally laparoscopic right hepatectomy combined with resection of the inferior vena cava by anterior approach. Ann Surg Oncol 22(3):851–851CrossRefGoogle Scholar
  28. 28.
    Gumbs AA, Gayet B (2008) Totally laparoscopic central hepatectomy. J Gastrointest Surg 12(7):1153–1153CrossRefGoogle Scholar
  29. 29.
    Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256(6):959–964CrossRefGoogle Scholar
  30. 30.
    Strasberg SM, Belghiti J, Clavien P-A, Gadzijev E, Garden JO, Lau W-Y et al (2000) The Brisbane 2000 terminology of liver anatomy and resections. Hpb 2(3):333–339CrossRefGoogle Scholar
  31. 31.
    Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213CrossRefGoogle Scholar
  32. 32.
    Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien P-A (2013) The comprehensive complication index: a novel continuous scale to measure surgical morbidity. Ann Surg 258(1):1–7CrossRefGoogle Scholar
  33. 33.
    Balzan S, Belghiti J, Farges O, Ogata S, Sauvanet A, Delefosse D et al (2005) The “50–50 criteria” on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 242(6):824–829CrossRefGoogle Scholar
  34. 34.
    Adam R, Imai K, Castro Benitez C, Allard M-A, Vibert E, Sa Cunha A et al (2016) Outcome after associating liver partition and portal vein ligation for staged hepatectomy and conventional two-stage hepatectomy for colorectal liver metastases. Br J Surg 103(11):1521–1529CrossRefGoogle Scholar
  35. 35.
    Galjart B, van der Stok EP, Rothbarth J, Grünhagen DJ, Verhoef C (2016) Posttreatment surveillance in patients with prolonged disease-free survival after resection of colorectal liver metastasis. Ann Surg Oncol 23(12):3999–4007CrossRefGoogle Scholar
  36. 36.
    Imai K, Allard M-A, Benitez CC, Vibert E, Cunha AS, Cherqui D et al (2016 ) Early recurrence after hepatectomy for colorectal liver metastases: what optimal definition and what predictive factors? Oncologist 21:887–894CrossRefGoogle Scholar
  37. 37.
    Kulaylat AN, Schubart JR, Stokes AL, Bhayani NH, Wong J, Kimchi ET et al (2014) Overall survival by pattern of recurrence following curative intent surgery for colorectal liver metastasis: CRLM patterns of recurrence. J Surg Oncol 110(8):1011–1015CrossRefGoogle Scholar
  38. 38.
    Bredt LC, Rachid AF (2014) Predictors of recurrence after a first hepatectomy for colorectal cancer liver metastases: a retrospective analysis. World J Surg Oncol 12(1):391CrossRefGoogle Scholar
  39. 39.
    Imai K, Allard M-A, Castro Benitez C, Vibert E, Sa Cunha A, Cherqui D et al (2017) Long-term outcomes of radiofrequency ablation combined with hepatectomy compared with hepatectomy alone for colorectal liver metastases: radiofrequency ablation with hepatectomy for colorectal liver metastases. Br J Surg 104(5):570–579CrossRefGoogle Scholar
  40. 40.
    Hashimoto M, Kobayashi T, Ishiyama K, Ide K, Ohira M, Tahara H et al (2016) Efficacy of repeat hepatectomy for recurrence following curative hepatectomy for colorectal liver metastases: a Retrospective Cohort Study of 128 patients. Int J Surg 36:96–103CrossRefGoogle Scholar
  41. 41.
    Shafaee Z, Kazaryan AM, Marvin MR, Cannon R, Buell JF, Edwin B et al (2011) Is laparoscopic repeat hepatectomy feasible? A tri-institutional analysis. J Am Coll Surg 212(2):171–179CrossRefGoogle Scholar
  42. 42.
    Montalti R, Berardi G, Laurent S, Sebastiani S, Ferdinande L, Libbrecht LJ et al (2014) Laparoscopic liver resection compared to open approach in patients with colorectal liver metastases improves further resectability: oncological outcomes of a case-control matched-pairs analysis. Eur J Surg Oncol EJSO 40(5):536–544CrossRefGoogle Scholar
  43. 43.
    Dupré A, Rehman A, Jones RP, Parker A, Diaz-Nieto R, Fenwick SW et al (2018) Validation of clinical prognostic scores for patients treated with curative-intent for recurrent colorectal liver metastases. J Surg Oncol. CrossRefPubMedGoogle Scholar
  44. 44.
    Bellier J, De Wolf J, Hebbar M, Amrani ME, Desauw C, Leteurtre E et al (2017) Repeated resections of hepatic and pulmonary metastases from colorectal cancer provide long-term survival. World J Surg. CrossRefPubMedGoogle Scholar
  45. 45.
    Moroni M, Veronese S, Benvenuti S, Marrapese G, Sartore-Bianchi A, Di Nicolantonio F et al (2005) Gene copy number for epidermal growth factor receptor (EGFR) and clinical response to antiEGFR treatment in colorectal cancer: a cohort study. Lancet Oncol 6(5):279–286CrossRefGoogle Scholar
  46. 46.
    Sasaki K, Margonis GA, Wilson A, Kim Y, Buettner S, Andreatos N et al (2016) Prognostic implication of KRAS status after hepatectomy for colorectal liver metastases varies according to primary colorectal tumor location. Ann Surg Oncol 23(11):3736–3743CrossRefGoogle Scholar
  47. 47.
    Brudvik KW, Kopetz SE, Li L, Conrad C, Aloia TA, Vauthey J-N (2015) Meta-analysis of KRAS mutations and survival after resection of colorectal liver metastases: KRAS status and survival after resection of colorectal liver metastases. Br J Surg 102(10):1175–1183CrossRefGoogle Scholar
  48. 48.
    Kim CG, Ahn JB, Jung M, Beom SH, Kim C, Kim JH et al (2016) Effects of microsatellite instability on recurrence patterns and outcomes in colorectal cancers. Br J Cancer 115(1):25–33CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Nicolas Tabchouri
    • 1
    • 2
  • Brice Gayet
    • 1
  • Shinya Okumura
    • 1
  • Gianfranco Donatelli
    • 1
  • Marc Beaussier
    • 1
  • Mostefa Bennamoun
    • 3
  • Christophe Louvet
    • 3
  • David Fuks
    • 1
    Email author
  1. 1.Department of Digestive Disease, Institut Mutualiste MontsourisUniversité Paris DescartesParisFrance
  2. 2.Department of Digestive SurgeryTrousseau HospitalChambray-lès-ToursFrance
  3. 3.Department of OncologyInstitut Mutualiste MontsourisParisFrance

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