Annals of Surgical Oncology

, Volume 23, Issue 4, pp 1352–1360 | Cite as

Is Tumor Detachment from Vascular Structures Equivalent to R0 Resection in Surgery for Colorectal Liver Metastases? An Observational Cohort

  • Luca Viganò
  • Fabio Procopio
  • Matteo Maria Cimino
  • Matteo Donadon
  • Andrea Gatti
  • Guido Costa
  • Daniele Del Fabbro
  • Guido Torzilli
Hepatobiliary Tumors



R0 resection is the standard for colorectal liver metastases (CLMs). Adequacy of R1 resections is debated. Detachment of CLMs from vessels has been proposed to prioritize parenchyma sparing and increase resectability, but outcomes are still to be elucidated. The present study aimed to clarify the outcomes of R1 surgery (margin <1 mm) in patients with CLMs, distinguishing standard R1 resection (parenchymal margin, R1Par) and R1 resection with detachment of CLMs from major intrahepatic vessels (R1Vasc).


All patients undergoing first resection between 2004 and June 2013 were prospectively considered. R0, R1Par, and R1Vasc were compared in per-patient and per-resection area analyses.


The study included 627 resection areas in 226 consecutive patients. Fifty-one (8.1 %) resections in 46 (20.4 %) patients were R1Vasc, and 177 (28.2 %) resections in 107 (47.3 %) patients were R1Par. Thirty-two (5.1 %) surgical margin recurrences occurred in 28 (12.4 %) patients. Local recurrence risk was similar between the R0 and R1Vasc groups (per-patient analysis 5.3 vs. 4.3 %; per-resection area analysis 1.5 vs. 3.9 %, p = n.s.) but increased in the R1Par group (19.6 and 13.6 %, p < 0.05 for both). The R1Par group had a higher rate of hepatic-only recurrences (49.5 vs. 36.1 %, p = 0.042). On multivariate analysis, R1Par was an independent negative prognostic factor of overall survival (p = 0.034, median follow-up 33 months); conversely R1Vasc versus R0 had no significant differences.


R1Par resection is not adequate for CLMs. R1Vasc surgery achieves outcomes equivalent to R0 resection. CLM detachment from intrahepatic vessels can be pursued to increase patient resectability and resection safety (parenchymal sparing).


Overall Survival Local Recurrence Liver Resection Major Hepatectomy Resection Area 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Conflict of interest

None to declare.

Supplementary material

10434_2015_5009_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 13 kb)


  1. 1.
    Charnsangavej C, Clary B, Fong Y, et al. Selection of patients for resection of hepatic colorectal metastases: expert consensus statement. Ann Surg Oncol. 2006;13:1261–8.CrossRefPubMedGoogle Scholar
  2. 2.
    Schmoll HJ, Van Cutsem E, Stein A, et al. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Ann Oncol. 2012;23:2479–516.CrossRefPubMedGoogle Scholar
  3. 3.
    Minagawa M, Makuuchi M, Torzilli G, et al. Extension of the frontiers of surgical indications in the treatment of liver metastases from colorectal cancer: long-term results. Ann Surg. 2000;231:487–99.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Poultsides GA, Schulick RD, Pawlik TM. Hepatic resection for colorectal metastases: the impact of surgical margin status on outcome. HPB. 2010;12:43–9.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    de Haas RJ, Wicherts DA, Flores E, et al. R1 resection by necessity for colorectal liver metastases: is it still a contraindication to surgery? Ann Surg. 2008;248:626–37.PubMedGoogle Scholar
  6. 6.
    Nuzzo G, Giuliante F, Ardito F, et al. Influence of surgical margin on type of recurrence after liver resection for colorectal metastases: a single-center experience. Surgery. 2008;143:384–93.CrossRefPubMedGoogle Scholar
  7. 7.
    Kokudo N, Miki Y, Sugai S, et al. Genetic and histological assessment of surgical margins in resected liver metastases from colorectal carcinoma: minimum surgical margins for successful resection. Arch Surg. 2002;137:833–40.CrossRefPubMedGoogle Scholar
  8. 8.
    Pawlik TM, Scoggins CR, Zorzi D, 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.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Yokoyama N, Shirai Y, Ajioka Y, et al. Immunohistochemically detected hepatic micrometastases predict a high risk of intrahepatic recurrence after resection of colorectal carcinoma liver metastases. Cancer. 2002;94:1642–7.CrossRefPubMedGoogle Scholar
  10. 10.
    Wakai T, Shirai Y, Sakata J, et al. Appraisal of 1 cm hepatectomy margins for intrahepatic micrometastases in patients with colorectal carcinoma liver metastasis. Ann Surg Oncol. 2008;15:2472–81.CrossRefPubMedGoogle Scholar
  11. 11.
    Viganò L, Capussotti L, De Rosa G, et al. Liver resection for colorectal metastases after chemotherapy: impact of chemotherapy-related liver injuries, pathological tumor response, and micrometastases on long-term survival. Ann Surg. 2013;258:731–40.CrossRefPubMedGoogle Scholar
  12. 12.
    Mentha G, Terraz S, Morel P, et al. Dangerous halo after neoadjuvant chemotherapy and two-step hepatectomy for colorectal liver metastases. Br J Surg. 2009;96:95–103.CrossRefPubMedGoogle Scholar
  13. 13.
    Yamashita S, Hasegawa K, Takahashi M, et al. One-stage hepatectomy following portal vein embolization for colorectal liver metastasis. World J Surg. 2013;37:622–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Adam R, Delvart V, Pascal G, et al. Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg. 2004;240:644–57.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Viganò L, Capussotti L, Majno P, et al. Liver resection in patients with eight or more colorectal liver metastases. Br J Surg. 2015;102:92–101.CrossRefPubMedGoogle Scholar
  16. 16.
    Kornprat P, Jarnagin WR, Gonen M, et al. Outcome after hepatectomy for multiple (four or more) colorectal metastases in the era of effective chemotherapy. Ann Surg Oncol. 2007;14:1151–60.CrossRefPubMedGoogle Scholar
  17. 17.
    Malik HZ, Hamady ZZ, Adair R, et al. Prognostic influence of multiple hepatic metastases from colorectal cancer. Eur J Surg Oncol. 2007;33:468–73.CrossRefPubMedGoogle Scholar
  18. 18.
    van Dam RM, Lodewick TM, van den Broek MA, et al. Outcomes of extended versus limited indications for patients undergoing a liver resection for colorectal cancer liver metastases. HPB. 2014;16:550–9.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Andreou A, Aloia TA, Brouquet A, et al. Margin status remains an important determinant of survival after surgical resection of colorectal liver metastases in the era of modern chemotherapy. Ann Surg. 2013;257:1079–88.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Tranchart H, Chirica M, Faron M, et al. Prognostic impact of positive surgical margins after resection of colorectal cancer liver metastases: reappraisal in the era of modern chemotherapy. World J Surg. 2013;37:2647–54.CrossRefPubMedGoogle Scholar
  21. 21.
    Ayez N, Lalmahomed ZS, Eggermont AM, et al. Outcome of microscopic incomplete resection (R1) of colorectal liver metastases in the era of neoadjuvant chemotherapy. Ann Surg Oncol. 2012;19:1618–27.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Eveno C, Karoui M, Gayat E, et al. Liver resection for colorectal liver metastases with peri-operative chemotherapy: oncological results of R1 resections. HPB. 2013;15:359–64.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Pandanaboyana S, White A, Pathak S, et al. Impact of margin status and neoadjuvant chemotherapy on survival, recurrence after liver resection for colorectal liver metastasis. Ann Surg Oncol. 2015;22:173–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Torzilli G, Montorsi M, Donadon M, et al. “Radical but conservative” is the main goal for ultrasonography-guided liver resection: prospective validation of this approach. J Am Coll Surg. 2005;201:517–28.CrossRefPubMedGoogle Scholar
  25. 25.
    Torzilli G. Ultrasound-guided liver surgery: an atlas. 1 edn. Milan: Springer; 2014.CrossRefGoogle Scholar
  26. 26.
    Torzilli G, Procopio F, Botea F, et al. One-stage ultrasonographically guided hepatectomy for multiple bilobar colorectal metastases: a feasible and effective alternative to the 2-stage approach. Surgery. 2009;146:60–71.CrossRefPubMedGoogle Scholar
  27. 27.
    Torzilli G, Montorsi M, Del Fabbro D, et al. Ultrasonographically guided surgical approach to liver tumours involving the hepatic veins close to the caval confluence. Br J Surg. 2006;93:1238–46.CrossRefPubMedGoogle Scholar
  28. 28.
    Therasse P, Arbuck SG, Eisenhauer EA, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst. 2000;92:205–16.CrossRefPubMedGoogle Scholar
  29. 29.
    Cady B, McDermott WV. Major hepatic resection for metachronous metastases from colon cancer. Ann Surg. 1985;201:204–9.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Elias D, Cavalcanti A, Sabourin JC, et al. Resection of liver metastases from colorectal cancer: the real impact of the surgical margin. Eur J Surg Oncol. 1998;24:174–9.CrossRefPubMedGoogle Scholar
  31. 31.
    Holdhoff M, Schmidt K, Diehl F, et al. Detection of tumor DNA at the margins of colorectal cancer liver metastasis. Clin Cancer Res. 2011;17:3551–7.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Fong Y, Fortner J, Sun RL, et al. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230:309–18.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Margonis GA, Spolverato G, Kim Y, et al. Intraoperative surgical margin re-resection for colorectal liver metastasis: is it worth the effort? J Gastrointest Surg. 2015; 19:699–707.CrossRefPubMedGoogle Scholar
  34. 34.
    Portier G, Elias D, Bouche O, et al. Multicenter randomized trial of adjuvant fluorouracil and folinic acid compared with surgery alone after resection of colorectal liver metastases: FFCD ACHBTH AURC 9002 trial. J Clin Oncol. 2006;24:4976–82.CrossRefPubMedGoogle Scholar
  35. 35.
    Mitry E, Fields A, Bleiberg H, et al. Adjuvant chemotherapy after potentially curative resection of metastases from colorectal cancer. A meta-analysis of two randomized trials. J Clin Oncol. 2008;26:4906–11.CrossRefPubMedGoogle Scholar

Copyright information

© Society of Surgical Oncology 2015

Authors and Affiliations

  • Luca Viganò
    • 1
  • Fabio Procopio
    • 1
  • Matteo Maria Cimino
    • 1
  • Matteo Donadon
    • 1
  • Andrea Gatti
    • 1
  • Guido Costa
    • 1
  • Daniele Del Fabbro
    • 1
  • Guido Torzilli
    • 1
  1. 1.Department of Hepatobiliary & General Surgery, Humanitas Clinical and Research Center - IRCCSHumanitas UniversityRozzanoItaly

Personalised recommendations