Artificial intelligence predicts immune and inflammatory gene signatures directly from hepatocellular carcinoma histology.

artificial intelligence deep learning immune gene signatures pathology whole slide image

Journal

Journal of hepatology
ISSN: 1600-0641
Titre abrégé: J Hepatol
Pays: Netherlands
ID NLM: 8503886

Informations de publication

Date de publication:
07 2022
Historique:
received: 29 07 2021
revised: 17 12 2021
accepted: 17 01 2022
pubmed: 11 2 2022
medline: 22 6 2022
entrez: 10 2 2022
Statut: ppublish

Résumé

Patients with hepatocellular carcinoma (HCC) displaying overexpression of immune gene signatures are likely to be more sensitive to immunotherapy, however, the use of such signatures in clinical settings remains challenging. We thus aimed, using artificial intelligence (AI) on whole-slide digital histological images, to develop models able to predict the activation of 6 immune gene signatures. AI models were trained and validated in 2 different series of patients with HCC treated by surgical resection. Gene expression was investigated using RNA sequencing or NanoString technology. Three deep learning approaches were investigated: patch-based, classic MIL and CLAM. Pathological reviewing of the most predictive tissue areas was performed for all gene signatures. The CLAM model showed the best overall performance in the discovery series. Its best-fold areas under the receiver operating characteristic curves (AUCs) for the prediction of tumors with upregulation of the immune gene signatures ranged from 0.78 to 0.91. The different models generalized well in the validation dataset with AUCs ranging from 0.81 to 0.92. Pathological analysis of highly predictive tissue areas showed enrichment in lymphocytes, plasma cells, and neutrophils. We have developed and validated AI-based pathology models able to predict the activation of several immune and inflammatory gene signatures. Our approach also provides insights into the morphological features that impact the model predictions. This proof-of-concept study shows that AI-based pathology could represent a novel type of biomarker that will ease the translation of our biological knowledge of HCC into clinical practice. Immune and inflammatory gene signatures may be associated with increased sensitivity to immunotherapy in patients with advanced hepatocellular carcinoma. In the present study, the use of artificial intelligence-based pathology enabled us to predict the activation of these signatures directly from histology.

Sections du résumé

BACKGROUND & AIMS
Patients with hepatocellular carcinoma (HCC) displaying overexpression of immune gene signatures are likely to be more sensitive to immunotherapy, however, the use of such signatures in clinical settings remains challenging. We thus aimed, using artificial intelligence (AI) on whole-slide digital histological images, to develop models able to predict the activation of 6 immune gene signatures.
METHODS
AI models were trained and validated in 2 different series of patients with HCC treated by surgical resection. Gene expression was investigated using RNA sequencing or NanoString technology. Three deep learning approaches were investigated: patch-based, classic MIL and CLAM. Pathological reviewing of the most predictive tissue areas was performed for all gene signatures.
RESULTS
The CLAM model showed the best overall performance in the discovery series. Its best-fold areas under the receiver operating characteristic curves (AUCs) for the prediction of tumors with upregulation of the immune gene signatures ranged from 0.78 to 0.91. The different models generalized well in the validation dataset with AUCs ranging from 0.81 to 0.92. Pathological analysis of highly predictive tissue areas showed enrichment in lymphocytes, plasma cells, and neutrophils.
CONCLUSION
We have developed and validated AI-based pathology models able to predict the activation of several immune and inflammatory gene signatures. Our approach also provides insights into the morphological features that impact the model predictions. This proof-of-concept study shows that AI-based pathology could represent a novel type of biomarker that will ease the translation of our biological knowledge of HCC into clinical practice.
LAY SUMMARY
Immune and inflammatory gene signatures may be associated with increased sensitivity to immunotherapy in patients with advanced hepatocellular carcinoma. In the present study, the use of artificial intelligence-based pathology enabled us to predict the activation of these signatures directly from histology.

Identifiants

pubmed: 35143898
pii: S0168-8278(22)00031-9
doi: 10.1016/j.jhep.2022.01.018
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

116-127

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflicts of interest JC consults for Crosscope, Keen Eye, and has received research funding from Fondation Bristol Myers Squibb pour la Recherche en Immuno-Oncologie. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Qinghe Zeng (Q)

Centre d'Histologie, d'Imagerie et de Cytométrie (CHIC), Centre de Recherche des Cordeliers, INSERM, Sorbonne Université, Université de Paris, Paris, France; Laboratoire d'Informatique Paris Descartes (LIPADE), Université de Paris, Paris, France.

Christophe Klein (C)

Centre d'Histologie, d'Imagerie et de Cytométrie (CHIC), Centre de Recherche des Cordeliers, INSERM, Sorbonne Université, Université de Paris, Paris, France.

Stefano Caruso (S)

INSERM UMR-1162, Functional Genomics of Solid Tumors, Paris, France.

Pascale Maille (P)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Pathology, Créteil, France; Université Paris Est Créteil, INSERM, IMRB, F-94010 Créteil, France; INSERM, Unit U955, Team 18, Créteil, France.

Narmin Ghaffari Laleh (NG)

Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany; Medical Oncology, National Center for Tumor Diseases (NCT), University Hospital Heidelberg, Heidelberg, Germany.

Daniele Sommacale (D)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Digestive and Hepatobiliary Surgery, Créteil, France.

Alexis Laurent (A)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Digestive and Hepatobiliary Surgery, Créteil, France.

Giuliana Amaddeo (G)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Hepatology, Créteil, France.

David Gentien (D)

Institut Curie, PSL Research University, Translational Research Department, Genomics Platform, Paris, F-75248 France.

Audrey Rapinat (A)

Institut Curie, PSL Research University, Translational Research Department, Genomics Platform, Paris, F-75248 France.

Hélène Regnault (H)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Hepatology, Créteil, France.

Cécile Charpy (C)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Pathology, Créteil, France.

Cong Trung Nguyen (CT)

Université Paris Est Créteil, INSERM, IMRB, F-94010 Créteil, France; INSERM, Unit U955, Team 18, Créteil, France.

Christophe Tournigand (C)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Medical Oncology, Créteil, France.

Raffaele Brustia (R)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Digestive and Hepatobiliary Surgery, Créteil, France.

Jean Michel Pawlotsky (JM)

Université Paris Est Créteil, INSERM, IMRB, F-94010 Créteil, France; INSERM, Unit U955, Team 18, Créteil, France.

Jakob Nikolas Kather (JN)

Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany; Medical Oncology, National Center for Tumor Diseases (NCT), University Hospital Heidelberg, Heidelberg, Germany.

Maria Chiara Maiuri (MC)

Centre d'Histologie, d'Imagerie et de Cytométrie (CHIC), Centre de Recherche des Cordeliers, INSERM, Sorbonne Université, Université de Paris, Paris, France.

Nicolas Loménie (N)

Laboratoire d'Informatique Paris Descartes (LIPADE), Université de Paris, Paris, France.

Julien Calderaro (J)

Assistance Publique-Hôpitaux de Paris, Henri Mondor-Albert Chenevier University Hospital, Department of Pathology, Créteil, France; Université Paris Est Créteil, INSERM, IMRB, F-94010 Créteil, France; INSERM, Unit U955, Team 18, Créteil, France. Electronic address: juliencalderaro@yahoo.fr.

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