Machine learning evaluation of immune infiltrate through digital tumour score allows prediction of survival outcome in a pooled analysis of three international stage III colon cancer cohortsResearch in context
Julie Lecuelle,
Caroline Truntzer,
Debora Basile,
Luigi Laghi,
Luana Greco,
Alis Ilie,
David Rageot,
Jean-François Emile,
Fréderic Bibeau,
Julien Taïeb,
Valentin Derangere,
Come Lepage,
François Ghiringhelli
Affiliations
Julie Lecuelle
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; Cancer Biology Transfer Platform, Centre Georges-François Leclerc, Dijon, France
Caroline Truntzer
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; Cancer Biology Transfer Platform, Centre Georges-François Leclerc, Dijon, France; Genetic and Immunology Medical Institute, Dijon, France
Debora Basile
Department of Medical Oncology, San Giovanni di Dio Hospital, Crotone, Italy
Luigi Laghi
Department of Medicine and Surgery, University of Parma, Parma, Italy; Molecular Gastroenterology Laboratory, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
Luana Greco
Molecular Gastroenterology Laboratory, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
Alis Ilie
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; Cancer Biology Transfer Platform, Centre Georges-François Leclerc, Dijon, France
David Rageot
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; Cancer Biology Transfer Platform, Centre Georges-François Leclerc, Dijon, France
Jean-François Emile
Paris-Saclay University, Versailles SQY University (UVSQ), EA4340-BECCOH, Assistance Publique-Hôpitaux de Paris (AP-HP), Ambroise Paré Hospital, Smart Imaging, Service de Pathologie, Boulogne, France
Fréderic Bibeau
Service d'Anatomie et Cytologie Pathologiques, CHU Côte de Nacre, Normandie Université, Caen, France; Department of Pathology, Besançon University Hospital, Besançon, France
Julien Taïeb
Institut du Cancer Paris Cancer Research for Personalized Medicine, Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpital Européen Georges Pompidou, Paris, France; Centre de Recherche des Cordeliers, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre National de la Recherche Scientifique, Sorbonne Université, Université Sorbonne Paris Cité, Université de Paris, Paris, France; Department of Gastroenterology and Digestive Oncology, Georges Pompidou European Hospital, AP-HP Centre, Université Paris Cité, Paris, France
Valentin Derangere
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; Cancer Biology Transfer Platform, Centre Georges-François Leclerc, Dijon, France; Genetic and Immunology Medical Institute, Dijon, France; University of Burgundy Franche-Comté, Dijon, France
Come Lepage
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; University of Burgundy Franche-Comté, Dijon, France; Fédération Francophone de Cancérologie Digestive, Centre de Randomisation Gestion Analyse, EPICAD LNC 1231, Dijon, France; Service d'Hépato-gastroentérologie et Oncologie digestive, CHU de Dijon, France
François Ghiringhelli
Centre de Recherche INSERM LNC-UMR1231, Dijon, France; Cancer Biology Transfer Platform, Centre Georges-François Leclerc, Dijon, France; Genetic and Immunology Medical Institute, Dijon, France; University of Burgundy Franche-Comté, Dijon, France; Department of Medical Oncology, Centre Georges-François Leclerc, Dijon, France; Corresponding authors. Centre de Recherche INSERM LNC-UMR1231, Dijon, France.
Summary: Background: T-cell immune infiltrates are robust prognostic variables in localised colon cancer. Evaluation of prognosis using artificial intelligence is an emerging field. We evaluated whether machine learning analysis improved prediction of patient outcome in comparison with analysis of T cell infiltrate only or in association with clinical variables. Methods: We used data from two phase III clinical trials (Prodige-13 and PETACC08) and one retrospective Italian cohort (HARMONY). Cohorts were split into training (N = 692), internal validation (N = 297) and external validation (N = 672) sets. Tumour slides were stained with CD3mAb. CD3 Machine Learning (CD3ML) score was computed using graphical parameters within the tumour tiles obtained from CD3 slides. CD3 infiltrates in tumour core and invasive margin were automatically detected. Associations of CD3 infiltrates and CD3ML with 5-year Disease-Free Survival (DFS) were examined using univariate and multivariable survival models by Cox regression. Findings: CD3 density both in the invasive margin and the tumour core were significantly associated with DFS in the different sets. Similarly, CD3ML score was significantly associated with DFS in all sets. CD3 assessment did not provide added value on top of CD3ML assessment (Likelihood Ratio Test (LRT), p = 0.13). In contrast, CD3ML improved prediction of DFS when combined with a clinical risk stage (LRT, p = 0.001). Stratified by clinical risk score (High or Low), patients with low CD3ML score had better DFS. Interpretation: In all tested sets, machine learning analysis of tumour cells improved prediction of prognosis compared to clinical parameters. Adding tumour-infiltrating lymphocytes assessment did not improve prognostic determination. Funding: This research received no external funding.