Skip to main content
Log in

R1 Resection for Colorectal Liver Metastases: a Survey Questioning Surgeons about Its Incidence, Clinical Impact, and Management

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery

Abstract

Background

A ≥ 1-mm margin is standard for resection of colorectal liver metastases (CLM). However, R1 resection is not rare (10–30%), and chemotherapy could mitigate its impact. The possibility of detaching CLM from vessels (R1 vascular margin) has been described. A reappraisal of R1 resection is needed.

Methods

A 19-question survey regarding R1 resection for CLM was sent to hepatobiliary surgeons worldwide. Seven clinical cases were included.

Results

In total, 276 surgeons from 52 countries completed the survey. Ninety percent reported a negative impact of R1 resection (74% local recurrence, 31% hepatic recurrence, and 36% survival), but 50% considered it sometimes required for resectability. Ninety-one percent of responders suggested that the impact of R1 resection is modulated by the response to chemotherapy and/or CLM characteristics. Half considered the risk of R1 resection to be an indication for preoperative chemotherapy in patients who otherwise underwent upfront resection, and 40% modified the chemotherapy regimen when the tumor response did not guarantee R0 resection. Nevertheless, 80% scheduled R1 resection for multiple bilobar CLM that responded to chemotherapy. Forty-five percent considered the vascular margin equivalent to R0 resection. However, for lesions in contact with the right hepatic vein, right hepatectomy remained the standard. Detachment from the vein was rarely considered (10%), but 27% considered detachment in the presence of multiple bilobar CLM.

Conclusions

A negative margin is still standard for CLM, but R1 resection is no longer just a technical error. R1 resection should be part of the modern multidisciplinary, aggressive approach to CLM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kopetz S, Chang GJ, Overman MJ, Eng C, Sargent DJ, Larson DW, Grothey A, Vauthey JN, Nagorney DM, McWilliams RR. Improved survival in metastatic colorectal cancer is associated with adoption of hepatic resection and improved chemotherapy. J Clin Oncol 2009;27:3677–3683.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Schmoll HJ, Van Cutsem E, Stein A, Valentini V, Glimelius B, Haustermans K, Nordlinger B, van de Velde CJ, Balmana J, Regula J, Nagtegaal ID, Beets-Tan RG, Arnold D, Ciardiello F, Hoff P, Kerr D, Köhne CH, Labianca R, Price T, Scheithauer W, Sobrero A, Tabernero J, Aderka D, Barroso S, Bodoky G, Douillard JY, El Ghazaly H, Gallardo J, Garin A, Glynne-Jones R, Jordan K, Meshcheryakov A, Papamichail D, Pfeiffer P, Souglakos I, Turhal S, Cervantes A. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Ann Oncol 2012;23:2479–2516.

    Article  CAS  PubMed  Google Scholar 

  3. Adam R, de Gramont A, Figueras J, Kokudo N, Kunstlinger F, Loyer E, Poston G, Rougier P, Rubbia-Brandt L, Sobrero A, Teh C, Tejpar S, Van Cutsem E, Vauthey JN, Påhlman L; of the EGOSLIM (Expert Group on OncoSurgery management of LIver Metastases) group. Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus. Cancer Treat Rev 2015;41:729–741.

    Article  Google Scholar 

  4. Viganò L, Russolillo N, Ferrero A, Langella S, Sperti E, Capussotti L. Evolution of long-term outcome of liver resection for colorectal metastases: analysis of actual 5-year survival rates over two decades. Ann Surg Oncol 2012;19:2035–2044.

    Article  PubMed  Google Scholar 

  5. Cady B, McDermott WV. Major hepatic resection for metachronous metastases from colon cancer. Ann Surg 1985;201:204–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Elias D, Cavalcanti A, Sabourin JC, Lassau N, Pignon JP, Ducreux M, Coyle C, Lasser P. Resection of liver metastases from colorectal cancer: the real impact of the surgical margin. Eur J Surg Oncol 1998;24:174–179.

    Article  CAS  PubMed  Google Scholar 

  7. Holdhoff M, Schmidt K, Diehl F, Aggrawal N, Angenendt P, Romans K, Edelstein DL, Torbenson M, Kinzler KW, Vogelstein B, Choti MA, Diaz LA Jr Detection of tumor DNA at the margins of colorectal cancer liver metastasis. Clin Cancer Res 2011;17:3551–3557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kokudo N, Miki Y, Sugai S, Yanagisawa A, Kato Y, Sakamoto Y, Yamamoto J, Yamaguchi T, Muto T, Makuuchi M. Genetic and histological assessment of surgical margins in resected liver metastases from colorectal carcinoma: minimum surgical margins for successful resection. Arch Surg 2002;137:833–840.

    Article  PubMed  Google Scholar 

  9. Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C, Curley SA, Loyer EM, Muratore A, Mentha G, Capussotti L, Vauthey JN. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 2005;241:715–22.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hamady ZZ, Lodge JP, Welsh FK, Toogood GJ, White A, John T, Rees M. One-millimeter cancer-free margin is curative for colorectal liver metastases: a propensity score case-match approach. Ann Surg 2014;259:543–8.

    Article  PubMed  Google Scholar 

  11. Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 1999;230:309–318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Poultsides GA, Schulick RD, Pawlik TM. Hepatic resection for colorectal metastases: the impact of surgical margin status on outcome. HPB (Oxford) 2010;12:43–49.

    Article  Google Scholar 

  13. de Haas RJ, Wicherts DA, Andreani P, Pascal G, Saliba F, Ichai P, Adam R, Castaing D, Azoulay D. Impact of expanding criteria for resectability of colorectal metastases on short- and long-term outcomes after hepatic resection. Ann Surg 2011;253:1069–1079.

    Article  PubMed  Google Scholar 

  14. van Dam RM, Lodewick TM, van den Broek MA, de Jong MC, Greve JW, Jansen RL, Bemelmans MH, Neumann UP, Olde Damink SW, Dejong CH. Outcomes of extended versus limited indications for patients undergoing a liver resection for colorectal cancer liver metastases. HPB (Oxford) 2014;16:550–559.

    Google Scholar 

  15. Torzilli G, Adam R, Viganò L, Imai K, Goransky J, Fontana A, Toso C, Majno P, de Santibañes E. Surgery of Colorectal Liver Metastases: Pushing the Limits. Liver Cancer 2016;6:80–89.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Viganò L, Capussotti L, Majno P, Toso C, Ferrero A, De Rosa G, Rubbia-Brandt L, Mentha G. Liver resection in patients with eight or more colorectal liver metastases. Br J Surg 2015;102:92–101.

    Article  PubMed  Google Scholar 

  17. Andreou A, Aloia TA, Brouquet A, Dickson PV, Zimmitti G, Maru DM, Kopetz S, Loyer EM, Curley SA, Abdalla EK, Vauthey JN. Margin status remains an important determinant of survival after surgical resection of colorectal liver metastases in the era of modern chemotherapy. Ann Surg 2013;257:1079–1088.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Sadot E, Groot Koerkamp B, Leal JN, Shia J, Gonen M, Allen PJ, DeMatteo RP, Kingham TP, Kemeny N, Blumgart LH, Jarnagin WR, DʼAngelica MI. Resection margin and survival in 2368 patients undergoing hepatic resection for metastatic colorectal cancer: surgical technique or biologic surrogate? Ann Surg 2015;262:476–85.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Pandanaboyana S, White A, Pathak S, Hidalgo EL, Toogood G, Lodge JP, Prasad KR. Impact of margin status and neoadjuvant chemotherapy on survival, recurrence after liver resection for colorectal liver metastasis. Ann Surg Oncol 2015;22:173–179.

    Article  PubMed  Google Scholar 

  20. Viganò L, Procopio F, Cimino MM, Donadon M, Gatti A, Costa G, Del Fabbro D, Torzilli G. Is Tumor Detachment from Vascular Structures Equivalent to R0 Resection in Surgery for Colorectal Liver Metastases? An Observational Cohort. Ann Surg Oncol 2016;23:1352–1360.

    Article  PubMed  Google Scholar 

  21. Eveno C, Karoui M, Gayat E, Luciani A, Auriault ML, Kluger MD, Baumgaertner I, Baranes L, Laurent A, Tayar C, Azoulay D, Cherqui D. Liver resection for colorectal liver metastases with peri-operative chemotherapy: oncological results of R1 resections. HPB (Oxford) 2013;15:359–364.

    Article  Google Scholar 

  22. Kornprat P, Jarnagin WR, Gonen M, DeMatteo RP, Fong Y, Blumgart LH, D'Angelica M. Outcome after hepatectomy for multiple (four or more) colorectal metastases in the era of effective chemotherapy. Ann Surg Oncol 2007;14:1151–1160.

    Article  PubMed  Google Scholar 

  23. Malik HZ, Hamady ZZ, Adair R, Finch R, Al-Mukhtar A, Toogood GJ, Prasad KR, Lodge JP. Prognostic influence of multiple hepatic metastases from colorectal cancer. Eur J Surg Oncol 2007;33:468–473.

    Article  CAS  PubMed  Google Scholar 

  24. Tanaka K, Shimada H, Ueda M, Matsuo K, Endo I, Togo S. Role of hepatectomy in treating multiple bilobar colorectal cancer metastases. Surgery 2008;143:259–270.

    Article  PubMed  Google Scholar 

  25. Adam R, Delvart V, Pascal G, Valeanu A, Castaing D, Azoulay D, Giacchetti S, Paule B, Kunstlinger F, Ghémard O, Levi F, Bismuth H. Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg 2004;240:644–657.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Yamashita S, Hasegawa K, Takahashi M, Inoue Y, Sakamoto Y, Aoki T, Sugawara Y, Kokudo N. One-stage hepatectomy following portal vein embolization for colorectal liver metastasis. World J Surg 2013;37:622–628.

    Article  PubMed  Google Scholar 

  27. Torzilli G, Procopio F, Costa G. Adjuncts to hepatic resection: ultrasound and intraoperative navigation. In Jarnagin WR, ed. Blumgart's Surgery of the Liver, Biliary Tract and Pancreas, vol. 2, 6th ed. Philadelphia: Elservier, 2017, pp 1684–1724.

    Google Scholar 

  28. Torzilli G. Ultrasound-Guided Liver Surgery: An Atlas, 1st ed. Milan: Springer-Verlag, 2014.

    Book  Google Scholar 

  29. de Haas RJ, Wicherts DA, Flores E, Azoulay D, Castaing D, Adam R. R1 resection by necessity for colorectal liver metastases: is it still a contraindication to surgery? Ann Surg 2008;248:626–637.

    PubMed  Google Scholar 

  30. Ayez N, Lalmahomed ZS, Eggermont AM, Ijzermans JN, de Jonge J, van Montfort K, Verhoef C. Outcome of microscopic incomplete resection (R1) of colorectal liver metastases in the era of neoadjuvant chemotherapy. Ann Surg Oncol 2012;19:1618–1627.

    Article  PubMed  Google Scholar 

  31. Torzilli G, Vauthey JN, Belghiti J, Makuuchi M, Donadon M, Viganò L, Kokudo N. EWALT: East Meets West in a Multidisciplinary Setting to Improve the Management of Liver Tumors. Liver Cancer 2016;6:13–15.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Yokoyama N, Shirai Y, Ajioka Y, Nagakura S, Suda T, Hatakeyama K. Immunohistochemically detected hepatic micrometastases predict a high risk of intrahepatic recurrence after resection of colorectal carcinoma liver metastases. Cancer 2002;94:1642–1647.

    Article  PubMed  Google Scholar 

  33. Wakai T, Shirai Y, Sakata J, Valera VA, Korita PV, Akazawa K, Ajioka Y, Hatakeyama K. Appraisal of 1 cm hepatectomy margins for intrahepatic micrometastases in patients with colorectal carcinoma liver metastasis. Ann Surg Oncol 2008;15:2472–2481.

    Article  PubMed  Google Scholar 

  34. Viganò L, Capussotti L, De Rosa G, De Saussure WO, Mentha G, Rubbia-Brandt L. 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;258:731–740.

    Article  PubMed  Google Scholar 

  35. Mentha G, Terraz S, Morel P, Andres A, Giostra E, Roth A, Rubbia-Brandt L, Majno P. Dangerous halo after neoadjuvant chemotherapy and two-step hepatectomy for colorectal liver metastases. Br J Surg 2009;96:95–103.

    Article  CAS  PubMed  Google Scholar 

  36. Torzilli G, Montorsi M, Donadon M, Palmisano A, Del Fabbro D, Gambetti A, Olivari N, Makuuchi M. "Radical but conservative" is the main goal for ultrasonography-guided liver resection: prospective validation of this approach. J Am Coll Surg 2005;201:517–528.

    Article  PubMed  Google Scholar 

  37. Torzilli G, Procopio F, Botea F, Marconi M, Del Fabbro D, Donadon M, Palmisano A, Spinelli A, Montorsi M. 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.

    Article  PubMed  Google Scholar 

  38. Torzilli G, Montorsi M, Del Fabbro D, Palmisano A, Donadon M, Makuuchi M. Ultrasonographically guided surgical approach to liver tumours involving the hepatic veins close to the caval confluence. Br J Surg 2006;93:1238–1246.

    Article  CAS  PubMed  Google Scholar 

  39. Saiura A, Yamamoto J, Hasegawa K, Koga R, Sakamoto Y, Hata S, Makuuchi M, Kokudo N. Liver resection for multiple colorectal liver metastases with surgery up-front approach: bi-institutional analysis of 736 consecutive cases. World J Surg 2012;36:2171–2178.

    Article  PubMed  Google Scholar 

  40. Tranchart H, Chirica M, Faron M, Balladur P, Lefevre LB, Svrcek M, de Gramont A, Tiret E, Paye F. Prognostic impact of positive surgical margins after resection of colorectal cancer liver metastases: reappraisal in the era of modern chemotherapy. World J Surg 2013;37:2647–2654.

    Article  PubMed  Google Scholar 

  41. Nuzzo G, Giuliante F, Ardito F, Vellone M, Giovannini I, Federico B, Vecchio FM. Influence of surgical margin on type of recurrence after liver resection for colorectal metastases: a single-center experience. Surgery 2008;143:384–393.

    Article  PubMed  Google Scholar 

  42. Truant S, Séquier C, Leteurtre E, Boleslawski E, Elamrani M, Huet G, Duhamel A, Hebbar M, Pruvot FR. Tumour biology of colorectal liver metastasis is a more important factor in survival than surgical margin clearance in the era of modern chemotherapy regimens. HPB (Oxford) 2015;17:176–184.

    Article  Google Scholar 

  43. Viganò L, Torzilli G, Cimino M, Imai K, Vibert E, Donadon M, Castaing D, Adam R. Drop-out between the two liver resections of two-stage hepatectomy. Patient selection or loss of chance? Eur J Surg Oncol 2016;42:1385–93.

    Article  PubMed  Google Scholar 

  44. Margonis GA, Spolverato G, Kim Y, Ejaz A, Pawlik TM. Intraoperative surgical margin re-resection for colorectal liver metastasis: is it worth the effort? J Gastrointest Surg 2015;19:699–707.

    Article  PubMed  Google Scholar 

  45. Hosokawa I, Allard MA, Mirza DF, Kaiser G, Barroso E, Lapointe R, Laurent C, Ferrero A, Miyazaki M, Adam R. Outcomes of parenchyma-preserving hepatectomy and right hepatectomy for solitary small colorectal liver metastasis: A LiverMetSurvey study. Surgery 2017;162:223–232.

    Article  PubMed  Google Scholar 

  46. Parikh AA, Gentner B, Wu TT, Curley SA, Ellis LM, Vauthey JN. Perioperative complications in patients undergoing major liver resection with or without neoadjuvant chemotherapy. J Gastrointest Surg 2003;7:1082–1088.

    Article  PubMed  Google Scholar 

  47. Adam R, Bhangui P, Poston G, Mirza D, Nuzzo G, Barroso E, Ijzermans J, Hubert C, Ruers T, Capussotti L, Ouellet JF, Laurent C, Cugat E, Colombo PE, Milicevic M. Is perioperative chemotherapy useful for solitary, metachronous, colorectal liver metastases? Ann Surg 2010;252:774–787.

    Article  PubMed  Google Scholar 

  48. Gold JS, Are C, Kornprat P, Jarnagin WR, Gönen M, Fong Y, DeMatteo RP, Blumgart LH, D'Angelica M. 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;247:109–117.

    Article  PubMed  Google Scholar 

  49. Kokudo N, Tada K, Seki M, Ohta H, Azekura K, Ueno M, Matsubara T, Takahashi T, Nakajima T, Muto T. Anatomical major resection versus nonanatomical limited resection for liver metastases from colorectal carcinoma. Am J Surg 2001;181:153–159.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank all the colleagues that completed the survey for their precious contribution to this study.

Author information

Authors and Affiliations

Authors

Contributions

• Substantial contributions to the conception or design of the work: Viganò, Belghiti, Kokudo, Makuuchi, Vauthey, Torzilli

• Acquisition, analysis, or interpretation of data for the work: Costa, Cimino, Procopio, Donadon, Del Fabbro

• Drafting the work: Viganò, Costa, Cimino, Procopio, Donadon, Del Fabbro

• Revising it critically for important intellectual content: Viganò, Belghiti, Kokudo, Makuuchi, Vauthey, Torzilli

• Final approval of the version to be published: all the authors

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: all the authors

Corresponding author

Correspondence to Guido Torzilli.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Viganò, L., Costa, G., Cimino, M.M. et al. R1 Resection for Colorectal Liver Metastases: a Survey Questioning Surgeons about Its Incidence, Clinical Impact, and Management. J Gastrointest Surg 22, 1752–1763 (2018). https://doi.org/10.1007/s11605-018-3820-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-018-3820-z

Keywords

Navigation