Open versus minimally invasive liver surgery for colorectal liver metastases (LapOpHuva): a prospective randomized controlled trial

Abstract

Objective

To present surgical and oncological outcomes using a prospective and randomized trial (LapOpHuva, NCT02727179) comparing minimally invasive liver resection (LLR) versus open liver resection (OLR) in patients with colorectal liver metastases (CRLM).

Methods

Between February 2005 and March 2016, 204 selected patients with CRLM were randomized and 193 were included: LLR (n = 96) and OLR (n = 97). The primary endpoint was to compare postoperative morbidity. Other secondary endpoints were oncological outcomes, use of the Pringle maneuver, surgical time, blood losses, transfusions, hospital stay, mortality and OS, and disease-free survival (DFS) at 3, 5, and 7 years.

Results

LLR presented with lower global morbidity (11.5% vs. 23.7%, p = 0.025) but with similar severe complications. Long-term survival outcomes were similar in both groups. The cumulative 1-, 3-, 5-, 7-year OS for LLR and OLR were 92.5%, 71.5%, 49.3%, 35.6% versus 93.6%, 69.7%, 47.4%, 35.5%, respectively (log-rank = 0.047, p = 0.82). DFS for LLR and OLR was 72.7%, 33.5%, 22.7%, and 20.8% versus 61.6%, 27.2%, 23.9%, and 17.9%, respectively (log-rank = 1.427, p = 0.23). LLR involved more use of the Pringle maneuver (15.5% vs. 30.2%, p = 0.025) and a shorter hospital stay (4 vs. 6 days, p < 0.001). There were no differences regarding surgical time, blood losses, transfusion, and mortality.

Conclusions

In selected patients with CRLM, LLR presents similar oncological outcomes with the advantages of the short-term results associated with LLR.

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References

  1. 1.

    Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P et al (2013) Perioperative FOLFOX4 chemotherapy and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC 40983): long-term results of a randomised, controlled, phase 3 trial. Lancet Oncol 14(12):1208–1215

    CAS  PubMed  Google Scholar 

  2. 2.

    Kopetz S, Chang GJ, Overman MJ, Eng C, Sargent DJ, Larson DW et al (2009) Improved survival in metastatic colorectal cancer is associated with adoption of hepatic resection and improved chemotherapy. J Clin Oncol 27(22):3677–3683

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    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):309–318; discussion 318–321

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Adam R, Delvart V, Pascal G, Valeanu A, Castaing D, Azoulay D et al (2004) Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg 240(4):644–657; discussion 657–648

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Cherqui D, Husson E, Hammoud R, Malassagne B, Stephan F, Bensaid S et al (2000) Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg 232(6):753–762

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I et al (2009) The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 250(5):825–830

    PubMed  Google Scholar 

  7. 7.

    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS et al (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261(4):619–629

    PubMed  Google Scholar 

  8. 8.

    Mala T, Edwin B, Gladhaug I, Fosse E, Soreide O, Bergan A et al (2002) A comparative study of the short-term outcome following open and laparoscopic liver resection of colorectal metastases. Surg Endosc 16(7):1059–1063

    CAS  PubMed  Google Scholar 

  9. 9.

    Castaing D, Vibert E, Ricca L, Azoulay D, Adam R, Gayet B (2009) Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg 250(5):849–855

    PubMed  Google Scholar 

  10. 10.

    Cannon RM, Scoggins CR, Callender GG, McMasters KM, Martin RC 2nd (2012) Laparoscopic versus open resection of hepatic colorectal metastases. Surgery 152(4):567–573; discussion 573–564

    PubMed  Google Scholar 

  11. 11.

    Cheung TT, Poon RT, Yuen WK, Chok KS, Tsang SH, Yau T et al (2013) Outcome of laparoscopic versus open hepatectomy for colorectal liver metastases. ANZ J Surg 83(11):847–852

    PubMed  Google Scholar 

  12. 12.

    Guerron AD, Aliyev S, Agcaoglu O, Aksoy E, Taskin HE, Aucejo F et al (2013) Laparoscopic versus open resection of colorectal liver metastasis. Surg Endosc 27(4):1138–1143

    PubMed  Google Scholar 

  13. 13.

    Qiu J, Chen S, Pankaj P, Wu H (2014) Laparoscopic hepatectomy is associated with considerably less morbidity and a long-term survival similar to that of the open procedure in patients with hepatic colorectal metastases. Surg Laparosc Endosc Percutan Tech 24(6):517–522

    PubMed  Google Scholar 

  14. 14.

    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 40(5):536–544

    CAS  PubMed  Google Scholar 

  15. 15.

    Kubota Y, Otsuka Y, Tsuchiya M, Katagiri T, Ishii J, Maeda T et al (2014) Efficacy of laparoscopic liver resection in colorectal liver metastases and the influence of preoperative chemotherapy. World J Surg Oncol 12:351

    PubMed  PubMed Central  Google Scholar 

  16. 16.

    Iwahashi S, Shimada M, Utsunomiya T, Imura S, Morine Y, Ikemoto T et al (2014) Laparoscopic hepatic resection for metastatic liver tumor of colorectal cancer: comparative analysis of short- and long-term results. Surg Endosc 28(1):80–84

    PubMed  Google Scholar 

  17. 17.

    Hasegawa Y, Nitta H, Sasaki A, Takahara T, Itabashi H, Katagiri H et al (2015) Long-term outcomes of laparoscopic versus open liver resection for liver metastases from colorectal cancer: a comparative analysis of 168 consecutive cases at a single center. Surgery 157(6):1065–1072

    PubMed  Google Scholar 

  18. 18.

    Nachmany I, Pencovich N, Zohar N, Ben-Yehuda A, Binyamin C, Goykhman Y et al (2015) Laparoscopic versus open liver resection for metastatic colorectal cancer. Eur J Surg Oncol 41(12):1615–1620

    CAS  PubMed  Google Scholar 

  19. 19.

    Allard MA, 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):794–802

    PubMed  Google Scholar 

  20. 20.

    de’Angelis N, Eshkenazy R, Brunetti F, Valente R, Costa M, Disabato M et al (2015) Laparoscopic versus open resection for colorectal liver metastases: a single-center study with propensity score analysis. J Laparoendosc Adv Surg Tech A 25(1):12–20

    PubMed  Google Scholar 

  21. 21.

    Beppu T, Wakabayashi G, Hasegawa K, Gotohda N, Mizuguchi T, Takahashi Y et al (2015) 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 22(10):711–720

    PubMed  Google Scholar 

  22. 22.

    Cipriani F, Rawashdeh M, Stanton L, Armstrong T, Takhar A, Pearce NW et al (2016) Propensity score-based analysis of outcomes of laparoscopic versus open liver resection for colorectal metastases. Br J Surg 103(11):1504–1512

    CAS  PubMed  Google Scholar 

  23. 23.

    Untereiner X, Cagniet A, Memeo R, Tzedakis S, Piardi T, Severac F et al (2016) Laparoscopic hepatectomy versus open hepatectomy for colorectal cancer liver metastases: comparative study with propensity score matching. Hepatobiliary Surg Nutr 5(4):290–299

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Lewin JW, O’Rourke NA, Chiow AKH, Bryant R, Martin I, Nathanson LK et al (2016) Long-term survival in laparoscopic vs open resection for colorectal liver metastases: inverse probability of treatment weighting using propensity scores. HPB (Oxford) 18(2):183–191

    Google Scholar 

  25. 25.

    Zeng Y, Tian M (2016) Laparoscopic versus open hepatectomy for elderly patients with liver metastases from colorectal cancer. J Buon 21(5):1146–1152

    PubMed  Google Scholar 

  26. 26.

    Martinez-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):1192–1200

    PubMed  Google Scholar 

  27. 27.

    Hallet J, Sa Cunha A, Cherqui D, Gayet B, Goere D, Bachellier P et al (2017) Laparoscopic compared to open repeat hepatectomy for colorectal liver metastases: a multi-institutional propensity-matched analysis of short- and long-term outcomes. World J Surg 41(12):3189–3198

    PubMed  Google Scholar 

  28. 28.

    Robles R, Marin C, Abellan B, Lopez A, Pastor P, Parrilla P (2008) A new approach to hand-assisted laparoscopic liver surgery. Surg Endosc 22(11):2357–2364

    PubMed  Google Scholar 

  29. 29.

    Robles R, Marin C, Parrilla P (2008) Laparoscopic liver resection for metastatic disease. Minerva Chir 63(6):441–453

    CAS  PubMed  Google Scholar 

  30. 30.

    Fretland AA, Dagenborg VJ, Bjornelv GMW, Kazaryan AM, Kristiansen R, Fagerland MW et al (2017) Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET Randomized Controlled Trial. Ann Surg 267(2):199–207

    Google Scholar 

  31. 31.

    The Brisbane (2000) Terminology of liver anatomy and resections. HPB 2(3):333–339

    Google Scholar 

  32. 32.

    Ban D, Tanabe M, Ito H et al (2014) A novel difficulty scoring system for laparoscopic liver resection. J Hepatobiliary Pancreat Sci 21(10):745–753

    PubMed  Google Scholar 

  33. 33.

    Lee MK, Gao F, Strasberg SM (2016) Completion of a liver surgery complexity score and classification based on an international survey of experts. J Am Coll Surg 223(2):332–342

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Antonetti MC, Killelea B, Orlando R (2002) 3rd. Hand-assisted laparoscopic liver surgery. Arch Surg 137(4):407–411; discussion 412

    PubMed  Google Scholar 

  35. 35.

    Hariharan D, Constantinides V, Kocher HM, Tekkis PP (2012) The role of laparoscopy and laparoscopic ultrasound in the preoperative staging of patients with resectable colorectal liver metastases: a meta-analysis. Am J Surg 204(1):84–92

    PubMed  Google Scholar 

  36. 36.

    Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications. Ann Surg 240(2):205–213

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    Rennie D (2001) CONSORT revised-improving the reporting of randomized trials. JAMA 285(15):2006–2007

    CAS  PubMed  Google Scholar 

  38. 38.

    Zhang XL, Liu RF, Zhang D, Zhang YS, 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 44:191–203

    PubMed  Google Scholar 

  39. 39.

    Kazaryan AM, Marangos IP, Rosok BI, Rosseland AR, Villanger O, Fosse E et al (2010) Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic outcome. Ann Surg 252(6):1005–1012

    PubMed  Google Scholar 

  40. 40.

    Hallet J, Beyfuss K, Memeo R, Karanicolas PJ, Marescaux J, Pessaux P (2016) Short and long-term outcomes of laparoscopic compared to open liver resection for colorectal liver metastases. Hepatobiliary Surg Nutr 5(4):300–310

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Tian ZQ, Su XF, Lin ZY, Wu MC, Wei LX, He J (2016) Meta-analysis of laparoscopic versus open liver resection for colorectal liver metastases. Oncotarget 7(51):84544–84555

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Zhou Y, Xiao Y, Wu L, Li B, Li H (2013) Laparoscopic liver resection as a safe and efficacious alternative to open resection for colorectal liver metastasis: a meta-analysis. BMC Surg 13:44

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Schiffman SC, Kim KH, Tsung A, Marsh JW, Geller DA (2015) Laparoscopic versus open liver resection for metastatic colorectal cancer: a metaanalysis of 610 patients. Surgery 157(2):211–222

    PubMed  Google Scholar 

  44. 44.

    Cheng Y, Zhang L, Li H, Wang L, Huang Y, Wu L et al (2017) Laparoscopic versus open liver resection for colorectal liver metastases: a systematic review. J Surg Res 220:234–246

    PubMed  Google Scholar 

  45. 45.

    Luo LX, Yu ZY, Bai YN (2014) Laparoscopic hepatectomy for liver metastases from colorectal cancer: a meta-analysis. J Laparoendosc Adv Surg Tech A 24(4):213–222

    PubMed  Google Scholar 

  46. 46.

    Wei M, He Y, Wang J, Chen N, Zhou Z, Wang Z (2014) Laparoscopic versus open hepatectomy with or without synchronous colectomy for colorectal liver metastasis: a meta-analysis. PLoS ONE 9(1):e87461

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Kawai T, Goumard C, Jeune F, Savier E, Vaillant JC, Scatton O (2018) Laparoscopic liver resection for colorectal liver metastasis patients allows patients to start adjuvant chemotherapy without delay: a propensity score analysis. Surg Endosc 32(7):3273–3281

    PubMed  Google Scholar 

  48. 48.

    Tohme S, Goswami J, Han K, Chidi AP, Geller DA, Reddy S et al (2015) Minimally invasive resection of colorectal cancer liver metastases leads to an earlier initiation of chemotherapy compared to open surgery. J Gastrointest Surg 19(12):2199–2206

    PubMed  PubMed Central  Google Scholar 

  49. 49.

    Fretland AA, Sokolov A, Postriganova N, Kazaryan AM, Pischke SE, Nilsson PH et al (2015) Inflammatory response after laparoscopic versus open resection of colorectal liver metastases: data from the Oslo-CoMet Trial. Medicine (Baltimore) 94(42):e1786

    CAS  Google Scholar 

  50. 50.

    Vigano L, Laurent A, Tayar C, Tomatis M, Ponti A, Cherqui D (2009) The learning curve in laparoscopic liver resection: improved feasibility and reproducibility. Ann Surg 250(5):772–782

    PubMed  Google Scholar 

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Acknowledgements

The authors would like to express their gratitude to Mrs. Guadalupe Ruiz and Mr. José J. López-Espín, for the statistical support.

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Correspondence to Ricardo Robles-Campos.

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R. Robles, V. Lopez-Lopez, R. Brusadin. A. Lopez-Conesa, P. Gil, A. Navarro, and P. Parrilla have no conflicts of interest or financial ties to disclose.

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Robles-Campos, R., Lopez-Lopez, V., Brusadin, R. et al. Open versus minimally invasive liver surgery for colorectal liver metastases (LapOpHuva): a prospective randomized controlled trial. Surg Endosc 33, 3926–3936 (2019). https://doi.org/10.1007/s00464-019-06679-0

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Keywords

  • Minimally invasive liver surgery
  • Open liver resection
  • Colorectal cancer
  • Colorectal liver metastases
  • Hepatectomy