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Impact of RAS Mutations in Metastatic Colorectal Cancer After Potentially Curative Resection: Does Site of Metastases Matter?

  • Colorectal Cancer
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

RAS mutation status is an important prognostic factor after resection of liver metastases (LiM) from colorectal cancer (CRC). The prognostic significance of RAS after resection of lung (LuM) and peritoneal (PM) metastases from CRC is unknown.

Methods

Between 2005 and 2014, all consecutive patients with known RAS status who underwent potentially curative resection for LiM, LuM, or PM were evaluated.

Results

A total of 720 patients with known RAS status underwent resection of LiM (n = 468), LuM (n = 102), and PM (n = 150). RAS mutations were identified in 63 and 58% of patients with LuM and PM, respectively, compared with 41% of patients with LiM (p < 0.001). Five-year overall survival (OS) after resection of PM was 45%, compared with 52% after resection of LiM (p = 0.018) and 64% after resection of LuM (p = 0.005). RAS mutations were associated with significantly worse OS after resection of LiM (p < 0.001), but did not affect OS among patients undergoing resection of LuM (p = 0.41) and PM (p = 0.65).

Conclusions

RAS mutations are more prevalent among patients undergoing resection of LuM and PM than LiM but do not affect survival after lung and peritoneal metastasectomy, as they do after hepatectomy. These results suggest that the prognostic significance of RAS mutations after resection of metastatic CRC depends on the specific site of metastases.

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Acknowledgment

The members of the BIG-RENAPE Working Group include: Julio Abba, MD (Department of Digestive Surgery, Grenoble University Hospital, Grenoble, France); KarineAbboud, MD (Department of General Surgery, St Etienne University Hospital, St Etienne, France); Mohammad Alyami, MD (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Catherine Arvieux, MD, PhD (Department of Digestive Surgery, Grenoble University Hospital, Grenoble, France); Amani Asnacios, MD (Department of Gastroenterology, Curie Institute, Paris, France); Gerlinde Averous, MD (Department of Pathology, Hautepierre University Hospital, Strasbourg, France); Naoual Bakrin, MD, PhD (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Armelle Bardier, MD (Department of Pathology, La Pitié-Salpétriêre University Hospital, Paris, France); Houda Ben Rejeb, MD (Department of Pathology, Bergonie Institute, Bordeaux, France); Jean-Marc Bereder, MD, PhD (Department of Digestive Surgery, Archet 2 University Hospital, Nice, France); Jean-Louis Bernard, MD (Department of Digestive Surgery, Archet 2 University Hospital, Nice, France); Frédéric Bibeau, MD, PhD (Department of Pathology, Caen University Hospital, Caen, France); Isabelle Bonnefoy (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Christophe Borg, MD, PhD (Department of Medical Oncology, Jean Minjoz University Hospital, Besançon, France); Gilles Boschetti, MD, PhD (Department of Gastroenterology, Lyon-Sud University Hospital, Lyon, France); Nadia Bouarioua, MD (Department of Gastroenterology, St Etienne University Hospital, St Etienne, France); Olivier Bouche, MD, PhD (Department of Gastroenterology, Robert Debré University Hospital, Reims, France); Dominique Bouzard, MD (Department of Digestive Surgery, Louis Mourier University Hospital, Colombes, France); Cécile Brigand, MD, PhD (Department of Digestive Surgery, Hautepierre University Hospital, Strasbourg, France); Wulfran Cacheux, MD (Department of Gastroenterology, Curie Institute, Paris, France); Olivier Capitain, MD (Department of Medical Oncology, ICO Paul Papin Cancer Center, Angers, France); Sébastien Carrère, MD (Department of Surgical Oncology, Val d’Aurelle Montpellier Cancer Center, Montpellier, France); Michel Carretier, MD, PhD (Department of Digestive Surgery, Poitiers University Hospital, Poitiers, France); Benjamin Castel, MD (Department of Digestive Surgery, Louis Mourier University Hospital, Colombes, France); Marion Chauvenet, MD, PhD (Department of Gastroenterology, Lyon-Sud University Hospital, Lyon, France); Anne Chevallier, MD (Department of Pathology, Archet 2 University Hospital, Nice, France); Benoît Coffin, MD (Department of Gastroenterology, Louis Mourier University Hospital, Colombes, France); Cristina Costan, MD (Department of Medical Oncology, Grenoble University Hospital, Grenoble, France); Eddy Cotte, MD, PhD (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Thomas Courvoisier, MD (Department of Digestive Surgery, Poitiers University Hospital, Poitiers, France); Laetitia Dahan, MD (Department of Medical Oncology, Timône University Hospital, Marseille, France); Peggy Dartigues, MD (Department of Pathology, Gustave Roussy Institute, Villejuif, France); Cécile De Chaisemartin, MD (Department of Surgical Oncology, Paoli Calmettes Institute, Marseille, France); Pierre Dechelotte, MD, PhD (Department of Pathology, Estaing University Hospital, Clermont-Ferrand, France); Sophie Deguelte-Lardière, MD (Department of Digestive Surgery, Robert Debré University Hospital, Reims, France); Jean-Robert Delpero, MD (Department of Surgical Oncology, Paoli Calmettes Institute, Marseille, France); Jean Del Grande, MD (Department of Pathology, Timône University Hospital, Marseille, France); Martin Demarchi, MD (Department of Medical Oncology, Jean Minjoz University Hospital, Besançon, France); Emmanuel Desandes, MD (Department of Medical Oncology, Lorraine Cancer Institute, Vandoeuvre-les-Nancy France); Grégoire Desolneux, MD (Department of Surgical Oncology, Bergonie Institute, Bordeaux, France); Patrick Dufour, MD (Department of Medical Oncology, Paul Strauss Comprehensive Cancer Center, Strasbourg, France); Frédéric Dumont, MD (Department of Surgical Oncology, ICO René Gauducheau Cancer Center, Saint-Herblain, France); Sylvaine Durand-Fontanier, MD (Department of Visceral Surgery and Transplantation, Dupuytren University Hospital, Limoges, France); Clarisse Eveno, MD, PhD (Surgical Oncologic & Digestive Unit, Lariboisière University Hospital, Paris, France); Serge Evrard, MD, PhD (Department of Surgical Oncology, Bergonie Institute, Bordeaux, France); Olivier Facy, MD, PhD (Department of Digestive Surgical Oncology, University Hospital of Dijon, Dijon, France); Fereshteh Farkhondeh, MD (Department of Pathology, Curie Institute, Paris, France); Juliette Fontaine, MD (Department of Pathology, Lyon-Sud University Hospital, Lyon, France); Johan Gagniere, MD (Department of Digestive Surgery, Estaing University Hospital, Clermont-Ferrand, France); Marie-Pierre Galais, MD (Department of Medical Oncology, François Baclesse Comprehensive Cancer, Caen, France); Laurent Ghouti, MD (Department of Digestive Surgery, Purpan University Hospital, Toulouse, France); François-Noël Gilly, MD, PhD (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Nicolas Goasguen, MD (Department of General Surgery, Diaconesses Croix Saint Simon Group Hospital, Paris, France); Jean-Marc Gornet, MD, PhD (Department of Medical Oncology, Saint Louis University Hospital, Paris, France); Pierre Gourdiole, MD (Department of Digestive Surgery, Grenoble University Hospital, Grenoble, France); Véronique Guerin-Meyer, MD (Department of Medical Oncology, ICO Paul Papin Cancer Center, Angers, France); Jean-Marc Guilloit, MD (Department of Surgical Oncology, François Baclesse Comprehensive Cancer, Caen, France); Rosine Guimbaud, MD, PhD (Department of Medical Oncology, Rangueil University Hospital, Toulouse, France); Frédéric Guyon, MD (Department of Surgical Oncology, Bergonie Institute, Bordeaux, France); Bruno Heyd, MD, PhD (Department of Digestive Surgery, Jean Minjoz University Hospital, Besançon, France); Marie-Françoise Heymann, MD (Department of Pathology, Nantes University Hospital, Nantes, France); Sylvie Isaac, MD (Department of Pathology, Lyon-Sud University Hospital, Lyon, France); Pauline Jouet, MD (Department of Gastroenterology, Louis Mourier University Hospital, Colombes, France); Peggy Jourdan-Enfer (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Jean-Louis Jouve, MD (Department of Gastroenterology, University Hospital of Dijon, Dijon, France); Rachid Kaci, MD (Department of Pathology, Lariboisière University Hospital, Paris, France); Mehdi Karoui, MD, PhD (Department of Surgery, La Pitié-Salpétriêre University Hospital, Paris, France); Reza Kianmanesh, MD, PhD (Department of Digestive Surgery, Robert Debré University Hospital, Reims, France); Sylvain Kirzin, MD, PhD (Department of Digestive Surgery, Purpan University Hospital, Toulouse, France); Jean-Emmanuel Kurtz, MD, PhD (Department of Medical Oncology, Hautepierre University Hospital, Strasbourg, France); François Labrousse, MD, PhD (Department of Pathology, Dupuytren University Hospital, Limoges, France); Valérie Lebrun-Ly, MD (Department of Medical Oncology, Dupuytren University Hospital, Limoges, France); Jérémie Lefevre, MD, PhD (Department of Digestive Surgery, University Hospital Saint Antoine, Paris, France); Bernard Lelong, MD (Department of Surgical Oncology, Paoli Calmettes Institute, Marseille, France); Anne-Elisabeth Lemaistre, MD (Department of Pathology, Léon Bérard Comprehensive Cancer Center, Lyon, France); Agnès Leroux-Broussier, MD (Department of Pathology, Lorraine Institute of Oncology, Vandoeuvre-les-Nancy, France); Pierre Levillain, MD, PhD (Department of Pathology, Poitiers University Hospital, Poitiers, France); Benjamin Linot, MD (Department of Medical Oncology, ICO Paul Papin Cancer Center, Angers, France); Réa Lo Dico, MD (Surgical Oncologic & Digestive Unit, Lariboisière University Hospital, Paris, France); Valéria Loi, MD (Department of Digestive Surgery, Tenon University Hospital, Paris, France); Gérard Lorimier, MD (Department of Digestive Surgery, University Hospital, Angers, France); Abakar Mahammat, MD (Department of Medical Oncology, Archet 2 University Hospital, Nice, France); David Malka, MD (Department of Medical Oncology, Gustave Roussy Institute, Villejuif, France); Frédéric Marchal, MD, PhD (Department of Surgical Oncology, Lorraine Cancer Institute, Vandoeuvre-les-Nancy France); Antoine Mariani, MD (Department of Surgery, La Pitié-Salpétriêre University Hospital, Paris, France); Pascale Mariani, MD (Department of Surgical Oncology, Curie Institute, Paris, France); Christophe Mariette, MD, PhD (Department of Digestive and Oncological Surgery, University Hospital Claude Huriez, Lille, France); Laurent Martin, MD, PhD (Department of Pathology, University Hospital of Dijon, Dijon, France); Pierre Meeus, MD (Department of Surgery, Léon Bérard Comprehensive Cancer Center, Lyon, France); Jean-Luc Meffert, MD (Department of Digestive Surgery, Robert Debré University Hospital, Reims, France); Mathieu Messager, MD, PhD (Department of Digestive and Oncological Surgery, University Hospital Claude Huriez, Lille, France); Pierre Michel, MD, PhD (Department of Gastroenterology, Charles Nicolle University Hospital, Rouen, France); Simon Msika, MD, PhD (Department of Digestive Surgery, Louis Mourier University Hospital, Colombes, France); Thierry Muron, MD (Department of Medical Oncology, Cancer Loire Cancer Institute, Saint Priest-en-Jarez, France); Georges Noel, MD (Department of Medical Oncology, Paul Strauss Comprehensive Cancer Center, Strasbourg, France); Pablo Ortega-Deballon, MD, PhD (Department of Digestive Surgical Oncology, University Hospital of Dijon, Dijon, France); Brice Paquette, MD (Department of Digestive Surgery, Jean Minjoz University Hospital, Besançon, France); Michel Peoc’h, MD, PhD (Department of Pathology, St Etienne University Hospital, St Etienne, France); Caroline Petorin, MD (Department of Digestive Surgery, Estaing University Hospital, Clermont-Ferrand, France); Patrice Peyrat, MD (Department of Surgery, Léon Bérard Comprehensive Cancer Center, Lyon, France); Denis Pezet, MD, PhD (Department of Digestive Surgery, Estaing University Hospital, Clermont-Ferrand, France); Guillaume Piessen, MD, PhD (Department of Digestive and Oncological Surgery, University Hospital Claude Huriez, Lille, France); Nicolas Pirro, MD, PhD (Department of Digestive Surgery, Timône University Hospital, Marseille, France); Marc Pocard, MD, PhD (Surgical Oncologic & Digestive Unit, Lariboisière University Hospital, Paris, France); Flora Poizat, MD (Department of Pathology, Paoli Calmettes Institute, Marseille, France); Jack Porcheron, MD, PhD (Department of Digestive Surgery, St Etienne University Hospital, St Etienne, France); Anaïs Poulet, PhD (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Fabienne Portales, MD (Department of Medical Oncology, Montpellier Cancer Institute, Montpellier, France); Justine Prost a la Denise, MD (Department of Digestive Surgery, Georges Pompidou University Hospital, Paris, France); François Quenet, MD (Department of Surgical Oncology, Montpellier Cancer Institute, Montpellier, France); Patrick Rat, MD, PhD (Department of Digestive Surgical Oncology, University Hospital of Dijon, Dijon, France); Christine Rebischung, MD, PhD (Department of Medical Oncology, Grenoble University Hospital, Grenoble, France); Jean-Marc Regimbeau, MD, PhD (Department of Digestive Surgery, University Hospital of Amiens, Amiens, France); Romain Rivoirard, MD (Department of Medical Oncology, Cancer Loire Cancer Institute, Saint Priest-en-Jarez, France); Serge Rohr, MD, PhD (Department of Digestive Surgery, Hautepierre University Hospital, Strasbourg, France); Philippe Rougier, MD, PhD (Department of Medical Oncology, Georges Pompidou University Hospital, Paris, France); Pierre Rousselot, MD (Department of Pathology, Francois Baclesse Comprehensive Cancer Center, Caen, France); Léa Saban-Roche, MD (Department of Medical Oncology, Cancer Loire Cancer Institute, Saint Priest-en-Jarez, France); Jean-Marc Sabate, MD, PhD (Department of Gastroenterology, Louis Mourier University Hospital, Colombes, France); Charles Sabbagh, MD (Department of Digestive Surgery, University Hospital of Amiens, Amiens, France); Jean-Christophe Sabourin, MD, PhD (Department of Pathology, Charles Nicolle University Hospital, Rouen, France); Emmanuelle Samalin-Scalzi, MD (Department of Medical Oncology, Montpellier Cancer Institute, Montpellier, France); Jean-François Seitz, MD, PhD (Department of Digestive Surgery, Timône University Hospital, Marseille, France); Janick Selves, MD, PhD (Department of Pathology, Toulouse University Hospital, Toulouse, France); Helène Senellart, MD (Department of Medical Oncology, ICO René Gauducheau Cancer Center, Saint-Herblain, France); Martine Serrano (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Olivia Sgabura, MD (Department of Surgical Oncology, Montpellier Cancer Institute, Montpellier, France); Igor Sielezneff, MD, PhD (Department of Digestive Surgery, Timône University Hospital, Marseille, France); Magali Svrcek, MD, PhD (Department of Pathology, Saint Antoine University Hospital, Paris, France); Abdelkader Taibi, MD (Department of Visceral Surgery and Transplantation, Dupuytren University Hospital, Limoges, France); Julien Taieb, MD, PhD (Department of Medical Oncology, Georges Pompidou University Hospital, Paris, France); Emilie Thibaudeau, MD (Department of Surgical Oncology, ICO René Gauducheau Cancer Center, Saint-Herblain, France); David Tougeron, MD (Department of Gastroenterology, Poitiers University Hospital, Poitiers, France); Jean-Jacques Tuech, MD, PhD (Department of Digestive Surgery, Charles Nicolle University Hospital, Rouen, France); Séverine Valmary-Degano, MD, PhD (Department of Pathology, Jean Minjoz University Hospital, Besançon, France); Delphine Vaudoyer, MD (Department of Digestive Surgery, Lyon-Sud University Hospital, Lyon, France); Véronique Verriele-Beurrier, MD (Department of Pathology, ICO Paul Papin Cancer Center, Angers, France); Laurent Villeneuve (Hospices Civils de Lyon, Pôle Information Médicale Evaluation Recherche, Unité de Recherche Clinique, Lyon, France); Julien Volet, MD (Department of Gastroenterology, Robert Debré University Hospital, Reims, France); Romuald Wernert, MD (Department of Surgical Oncology, ICO Paul Papin Cancer Center, Angers, France); Marc Ychou, MD, PhD (Department of Medical Oncology, Montpellier Cancer Institute, Montpellier, France); Benoît You, MD, PhD (Department of Medical Oncology, Lyon-Sud University Hospital, Lyon, France); Aziz Zaanan, MD (Department of Medical Oncology, Georges Pompidou University Hospital, Paris, France); Franck Zinzindohoue, MD, PhD (Department of Digestive Surgery, Georges Pompidou University Hospital, Paris, France)

Funding

This research was supported in part by the National Institutes of Health through MD Anderson’s Cancer Center Support Grant, CA016672. Dr. Passot was supported by the French Association of Surgery (AFC).

Disclosure

Guillaume Passot, Bradford J. Kim, Olivier Glehen, Reza J. Mehran, Scott E. Kopetz, Diane Goere, Michael J. Overman, Marc Pocard, Frédéric Marchal, Claudius Conrad, Thomas A. Aloia, Jean-Nicolas Vauthey, and Yun Shin Chun report no conflicts of interest relevant to this article.

Author information

Authors and Affiliations

  1. Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Guillaume Passot MD, PhD, Bradford J. Kim MD, MHS, Claudius Conrad MD, PhD, Thomas A. Aloia MD, Jean-Nicolas Vauthey MD & Yun Shin Chun MD

  2. Department of Surgical Oncology, Hospices Civils de Lyon, CH Lyon Sud, EMR 37-38 University Lyon 1, Lyon, France

    Guillaume Passot MD, PhD & Olivier Glehen MD, PhD

  3. Department of Thoracic and Cardiovascular Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Reza J. Mehran MD

  4. Department of Gastrointestinal Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Scott E. Kopetz MD & Michael J. Overman MD

  5. Department of Surgical Oncology, CLCC Institut Gustave Roussy, Villejuif, France

    Diane Goere MD, PhD

  6. Department of General Surgery and Surgical Oncology, Assistance Publique des Hopitaux de Paris, Paris, France

    Marc Pocard MD, PhD

  7. Department of Surgical Oncology, Lorraine Cancer Institute, Vandoeuvre-les-Nancy, France

    Frédéric Marchal MD, PhD

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  1. Guillaume Passot MD, PhD
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  2. Bradford J. Kim MD, MHS
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  3. Olivier Glehen MD, PhD
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  5. Scott E. Kopetz MD
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  11. Thomas A. Aloia MD
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  12. Jean-Nicolas Vauthey MD
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  13. Yun Shin Chun MD
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Consortia

on behalf of the BIG-RENAPE Working Group

  • Julio Abba
  • , Karine Abboud
  • , Mohammad Alyami
  • , Catherine Arvieux
  • , Amani Asnacios
  • , Gerlinde Averous
  • , Naoual Bakrin
  • , Armelle Bardier
  • , Houda Ben Rejeb
  • , Jean-Marc Bereder
  • , Jean-Louis Bernard
  • , Frédéric Bibeau
  • , Isabelle Bonnefoy
  • , Christophe Borg
  • , Gilles Boschetti
  • , Nadia Bouarioua
  • , Olivier Bouche
  • , Dominique Bouzard
  • , Cécile Brigand
  • , Wulfran Cacheux
  • , Olivier Capitain
  • , Sébastien Carrère
  • , Michel Carretier
  • , Benjamin Castel
  • , Marion Chauvenet
  • , Anne Chevallier
  • , Benoît Coffin
  • , Cristina Costan
  • , Eddy Cotte
  • , Thomas Courvoisier
  • , Laetitia Dahan
  • , Peggy Dartigues
  • , Cécile De Chaisemartin
  • , Pierre Dechelotte
  • , Sophie Deguelte-Lardière
  • , Jean-Robert Delpero
  • , Jean Del Grande
  • , Martin Demarchi
  • , Emmanuel Desandes
  • , Grégoire Desolneux
  • , Patrick Dufour
  • , Frédéric Dumont
  • , Sylvaine Durand-Fontanier
  • , Clarisse Eveno
  • , Serge Evrard
  • , Olivier Facy
  • , Fereshteh Farkhondeh
  • , Juliette Fontaine
  • , Johan Gagniere
  • , Marie-Pierre Galais
  • , Laurent Ghouti
  • , François-Noël Gilly
  • , Nicolas Goasguen
  • , Jean-Marc Gornet
  • , Pierre Gourdiole
  • , Véronique Guerin-Meyer
  • , Jean-Marc Guilloit
  • , Rosine Guimbaud
  • , Frédéric Guyon
  • , Bruno Heyd
  • , Marie-Françoise Heymann
  • , Sylvie Isaac
  • , Pauline Jouet
  • , Peggy Jourdan-Enfer
  • , Jean-Louis Jouve
  • , Rachid Kaci
  • , Mehdi Karoui
  • , Reza Kianmanesh
  • , Sylvain Kirzin
  • , Jean-Emmanuel Kurtz
  • , François Labrousse
  • , Valérie Lebrun-Ly
  • , Jérémie Lefevre
  • , Bernard Lelong
  • , Anne-Elisabeth Lemaistre
  • , Agnès Leroux-Broussier
  • , Pierre Levillain
  • , Benjamin Linot
  • , Réa Lo Dico
  • , Valéria Loi
  • , Gérard Lorimier
  • , Abakar Mahammat
  • , David Malka
  • , Frédéric Marchal
  • , Antoine Mariani
  • , Pascale Mariani
  • , Christophe Mariette
  • , Laurent Martin
  • , Pierre Meeus
  • , Jean-Luc Meffert
  • , Mathieu Messager
  • , Pierre Michel
  • , Simon Msika
  • , Thierry Muron
  • , Georges Noel
  • , Pablo Ortega-Deballon
  • , Brice Paquette
  • , Michel Peoc’h
  • , Caroline Petorin
  • , Patrice Peyrat
  • , Denis Pezet
  • , Guillaume Piessen
  • , Nicolas Pirro
  • , Marc Pocard
  • , Flora Poizat
  • , Jack Porcheron
  • , Anaïs Poulet
  • , Fabienne Portales
  • , Justine Prost a la Denise
  • , François Quenet
  • , Patrick Rat
  • , Christine Rebischung
  • , Jean-Marc Regimbeau
  • , Romain Rivoirard
  • , Serge Rohr
  • , Philippe Rougier
  • , Pierre Rousselot
  • , Léa Saban-Roche
  • , Jean-Marc Sabate
  • , Charles Sabbagh
  • , Jean-Christophe Sabourin
  • , Emmanuelle Samalin-Scalzi
  • , Jean-François Seitz
  • , Janick Selves
  • , Helène Senellart
  • , Martine Serrano
  • , Olivia Sgabura
  • , Igor Sielezneff
  • , Magali Svrcek
  • , Abdelkader Taibi
  • , Julien Taieb
  • , Emilie Thibaudeau
  • , David Tougeron
  • , Jean-Jacques Tuech
  • , Séverine Valmary-Degano
  • , Delphine Vaudoyer
  • , Véronique Verriele-Beurrier
  • , Laurent Villeneuve
  • , Julien Volet
  • , Romuald Wernert
  • , Marc Ychou
  • , Benoît You
  • , Aziz Zaanan
  •  & Franck Zinzindohoue

Corresponding author

Correspondence to Yun Shin Chun MD.

Additional information

Collaborators of the BIG-RENAPE Working Group are listed in the “Acknowledgment”.

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Passot, G., Kim, B.J., Glehen, O. et al. Impact of RAS Mutations in Metastatic Colorectal Cancer After Potentially Curative Resection: Does Site of Metastases Matter?. Ann Surg Oncol 25, 179–187 (2018). https://doi.org/10.1245/s10434-017-6141-7

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