Deep learning-based phenotyping reclassifies combined hepatocellular-cholangiocarcinoma

Julien Calderaro (), Narmin Ghaffari Laleh, Qinghe Zeng, Pascale Maille, Loetitia Favre, Anaïs Pujals, Christophe Klein, Céline Bazille, Lara R. Heij, Arnaud Uguen, Tom Luedde, Luca Tommaso, Aurélie Beaufrère, Augustin Chatain, Delphine Gastineau, Cong Trung Nguyen, Hiep Nguyen-Canh, Khuyen Nguyen Thi, Viviane Gnemmi, Rondell P. Graham, Frédéric Charlotte, Dominique Wendum, Mukul Vij, Daniela S. Allende, Federico Aucejo, Alba Diaz, Benjamin Rivière, Astrid Herrero, Katja Evert, Diego Francesco Calvisi, Jérémy Augustin, Wei Qiang Leow, Howard Ho Wai Leung, Emmanuel Boleslawski, Mohamed Rela, Arnaud François, Anthony Wing-Hung Cha, Alejandro Forner, Maria Reig, Manon Allaire, Olivier Scatton, Denis Chatelain, Camille Boulagnon-Rombi, Nathalie Sturm, Benjamin Menahem, Eric Frouin, David Tougeron, Christophe Tournigand, Emmanuelle Kempf, Haeryoung Kim, Massih Ningarhari, Sophie Michalak-Provost, Purva Gopal, Raffaele Brustia, Eric Vibert, Kornelius Schulze, Darius F. Rüther, Sören A. Weidemann, Rami Rhaiem, Jean-Michel Pawlotsky, Xuchen Zhang, Alain Luciani, Sébastien Mulé, Alexis Laurent, Giuliana Amaddeo, Hélène Regnault, Eleonora Martin, Christine Sempoux, Pooja Navale, Maria Westerhoff, Regina Cheuk-Lam Lo, Jan Bednarsch, Annette Gouw, Catherine Guettier, Marie Lequoy, Kenichi Harada, Pimsiri Sripongpun, Poowadon Wetwittayaklang, Nicolas Loménie, Jarukit Tantipisit, Apichat Kaewdech, Jeanne Shen, Valérie Paradis, Stefano Caruso and Jakob Nikolas Kather ()
Additional contact information
Julien Calderaro: Université Paris Est Créteil, INSERM, IMRB
Narmin Ghaffari Laleh: Technical University Dresden
Qinghe Zeng: Centre d’Histologie, d’Imagerie et de Cytométrie (CHIC), Centre de Recherche des Cordeliers
Pascale Maille: Université Paris Est Créteil, INSERM, IMRB
Loetitia Favre: Université Paris Est Créteil, INSERM, IMRB
Anaïs Pujals: Université Paris Est Créteil, INSERM, IMRB
Christophe Klein: Centre d’Histologie, d’Imagerie et de Cytométrie (CHIC), Centre de Recherche des Cordeliers
Céline Bazille: Caen University Hospital, Department of Pathology
Lara R. Heij: University Hospital RWTH Aachen
Arnaud Uguen: CHRU Brest, Department of Pathology
Tom Luedde: University Hospital Düsseldorf, Medical Faculty of Heinrich Heine University Düsseldorf
Luca Tommaso: Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano
Aurélie Beaufrère: Beaujon University Hospital, Department of Pathology
Augustin Chatain: Inserm, U955, Team 18
Delphine Gastineau: Inserm, U955, Team 18
Cong Trung Nguyen: Hanoi Medical University
Hiep Nguyen-Canh: Pathology Center, Bachmai Hospital
Khuyen Nguyen Thi: Pathology and Molecular biology Center, National Cancer Hospital
Viviane Gnemmi: University Lille, UMR9020-U1277, Cancer Heterogeneity Plasticity and Resistance to Therapies
Rondell P. Graham: Mayo Clinic Rochester
Frédéric Charlotte: Pitié-Salpêtrière University Hospital, Department of Pathology
Dominique Wendum: Saint-Antoine University Hospital, Department of Pathology
Mukul Vij: Bharath Institute of Higher Education and Research
Daniela S. Allende: Cleveland Clinic Foundation
Federico Aucejo: Cleveland Clinic Foundation
Alba Diaz: Universitat de Barcelona
Benjamin Rivière: Gui-de-Chauliac University Hospital, 80
Astrid Herrero: Gui-de-Chauliac University Hospital, 80
Katja Evert: University of Regensburg, Franz-Josef-Strauß-Allee 11
Diego Francesco Calvisi: University of Regensburg, Franz-Josef-Strauß-Allee 11
Jérémy Augustin: Université Paris Est Créteil, INSERM, IMRB
Wei Qiang Leow: Singapore General Hospital
Howard Ho Wai Leung: The Chinese University of Hong Kong
Emmanuel Boleslawski: CHU Lille, Department of Digestive and Hepatobiliary Surgery
Mohamed Rela: Dr Rela Institute and Medical Centre, Bharath Institute of Higher Education and Research
Arnaud François: Rouen University Hospital, Department of Pathology
Anthony Wing-Hung Cha: The Chinese University of Hong Kong
Alejandro Forner: Universidad de Barcelona
Maria Reig: Universidad de Barcelona
Manon Allaire: Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière University Hospital, Department of Hepatology
Olivier Scatton: Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière University Hospital, Department of Digestive and Hepatobiliary Surgery
Denis Chatelain: Centre Hospitalier Universitaire d’Amiens, Département de Pathologie
Camille Boulagnon-Rombi: Reims University Hospital, Department of Pathology
Nathalie Sturm: University Hospital
Benjamin Menahem: Caen University Hospital, Department of Digestive and Hepatobiliary Surgery
Eric Frouin: Poitiers University Hospital, Department of Pathology
David Tougeron: Poitiers University Hospital, Department of Hepatogastroenterology and Oncology
Christophe Tournigand: Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Medical Oncology
Emmanuelle Kempf: Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Medical Oncology
Haeryoung Kim: Seoul National University Hospital, Seoul National University College of Medicine
Massih Ningarhari: CHU Lille, Department of Hepatology
Sophie Michalak-Provost: Angers University Hospital, Department of Pathology
Purva Gopal: Department of Pathology, UT Southwestern Medical Center
Raffaele Brustia: Assistance Publique-Hôpitaux de Paris, Henri Mondor University Hospital, Department of Digestive and Hepatobiliary Surgery
Eric Vibert: Paul Brousse University Hospital, Department of Digestive and Hepatobiliary Surgery
Kornelius Schulze: University Medical Center Hamburg-Eppendorf
Darius F. Rüther: University Medical Center Hamburg-Eppendorf
Sören A. Weidemann: University Medical Center Hamburg-Eppendorf
Rami Rhaiem: Reims University Hospital, Department of Digestive and Hepatobiliary Surgery
Jean-Michel Pawlotsky: Université Paris Est Créteil, INSERM, IMRB
Xuchen Zhang: Yale University School of Medicine
Alain Luciani: Henri Mondor University Hospital, Department of Medical Imaging
Sébastien Mulé: Henri Mondor University Hospital, Department of Medical Imaging
Alexis Laurent: Assistance Publique-Hôpitaux de Paris, Henri Mondor University Hospital, Department of Digestive and Hepatobiliary Surgery
Giuliana Amaddeo: Henri Mondor University Hospital, Department of Hepatology
Hélène Regnault: Henri Mondor University Hospital, Department of Hepatology
Eleonora Martin: Paul Brousse University Hospital, Department of Hepatology
Christine Sempoux: Lausanne University Hospital (CHUV), University of Lausanne (UNIL)
Pooja Navale: Washington University in St. Louis
Maria Westerhoff: Department of Pathology University of Michigan
Regina Cheuk-Lam Lo: The University of Hong Kong, Pok Fu Lam
Jan Bednarsch: University Hospital RWTH Aachen
Annette Gouw: University Medical Center Groningen
Catherine Guettier: University Hospital RWTH Aachen
Marie Lequoy: Assistance Publique-Hôpitaux de Paris, Saint Antoine University Hospital, Department of Hepatology
Kenichi Harada: Kanazawa University Graduate School of Medicine
Pimsiri Sripongpun: Prince of Songkla University
Poowadon Wetwittayaklang: Prince of Songkla University, Department of Pathology
Nicolas Loménie: Université Paris Cité
Jarukit Tantipisit: Prince of Songkla University, Department of Pathology
Apichat Kaewdech: Prince of Songkla University
Jeanne Shen: Stanford University
Valérie Paradis: Beaujon University Hospital, Department of Pathology
Stefano Caruso: Université Paris Est Créteil, INSERM, IMRB
Jakob Nikolas Kather: Technical University Dresden

Nature Communications, 2023, vol. 14, issue 1, 1-10

Abstract: Abstract Primary liver cancer arises either from hepatocytic or biliary lineage cells, giving rise to hepatocellular carcinoma (HCC) or intrahepatic cholangiocarcinoma (ICCA). Combined hepatocellular- cholangiocarcinomas (cHCC-CCA) exhibit equivocal or mixed features of both, causing diagnostic uncertainty and difficulty in determining proper management. Here, we perform a comprehensive deep learning-based phenotyping of multiple cohorts of patients. We show that deep learning can reproduce the diagnosis of HCC vs. CCA with a high performance. We analyze a series of 405 cHCC-CCA patients and demonstrate that the model can reclassify the tumors as HCC or ICCA, and that the predictions are consistent with clinical outcomes, genetic alterations and in situ spatial gene expression profiling. This type of approach could improve treatment decisions and ultimately clinical outcome for patients with rare and biphenotypic cancers such as cHCC-CCA.

Date: 2023
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DOI: 10.1038/s41467-023-43749-3

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