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Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning

OBJECTIVE: Complex phenotypes captured on histological slides represent the biological processes at play in individual cancers, but the link to underlying molecular classification has not been clarified or systematised. In colorectal cancer (CRC), histological grading is a poor predictor of disease...

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Autores principales: Sirinukunwattana, Korsuk, Domingo, Enric, Richman, Susan D, Redmond, Keara L, Blake, Andrew, Verrill, Clare, Leedham, Simon J, Chatzipli, Aikaterini, Hardy, Claire, Whalley, Celina M, Wu, Chieh-hsi, Beggs, Andrew D, McDermott, Ultan, Dunne, Philip D, Meade, Angela, Walker, Steven M, Murray, Graeme I, Samuel, Leslie, Seymour, Matthew, Tomlinson, Ian, Quirke, Phil, Maughan, Timothy, Rittscher, Jens, Koelzer, Viktor H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BMJ Publishing Group 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7873419/
https://www.ncbi.nlm.nih.gov/pubmed/32690604
http://dx.doi.org/10.1136/gutjnl-2019-319866
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author Sirinukunwattana, Korsuk
Domingo, Enric
Richman, Susan D
Redmond, Keara L
Blake, Andrew
Verrill, Clare
Leedham, Simon J
Chatzipli, Aikaterini
Hardy, Claire
Whalley, Celina M
Wu, Chieh-hsi
Beggs, Andrew D
McDermott, Ultan
Dunne, Philip D
Meade, Angela
Walker, Steven M
Murray, Graeme I
Samuel, Leslie
Seymour, Matthew
Tomlinson, Ian
Quirke, Phil
Maughan, Timothy
Rittscher, Jens
Koelzer, Viktor H
author_facet Sirinukunwattana, Korsuk
Domingo, Enric
Richman, Susan D
Redmond, Keara L
Blake, Andrew
Verrill, Clare
Leedham, Simon J
Chatzipli, Aikaterini
Hardy, Claire
Whalley, Celina M
Wu, Chieh-hsi
Beggs, Andrew D
McDermott, Ultan
Dunne, Philip D
Meade, Angela
Walker, Steven M
Murray, Graeme I
Samuel, Leslie
Seymour, Matthew
Tomlinson, Ian
Quirke, Phil
Maughan, Timothy
Rittscher, Jens
Koelzer, Viktor H
author_sort Sirinukunwattana, Korsuk
collection PubMed
description OBJECTIVE: Complex phenotypes captured on histological slides represent the biological processes at play in individual cancers, but the link to underlying molecular classification has not been clarified or systematised. In colorectal cancer (CRC), histological grading is a poor predictor of disease progression, and consensus molecular subtypes (CMSs) cannot be distinguished without gene expression profiling. We hypothesise that image analysis is a cost-effective tool to associate complex features of tissue organisation with molecular and outcome data and to resolve unclassifiable or heterogeneous cases. In this study, we present an image-based approach to predict CRC CMS from standard H&E sections using deep learning. DESIGN: Training and evaluation of a neural network were performed using a total of n=1206 tissue sections with comprehensive multi-omic data from three independent datasets (training on FOCUS trial, n=278 patients; test on rectal cancer biopsies, GRAMPIAN cohort, n=144 patients; and The Cancer Genome Atlas (TCGA), n=430 patients). Ground truth CMS calls were ascertained by matching random forest and single sample predictions from CMS classifier. RESULTS: Image-based CMS (imCMS) accurately classified slides in unseen datasets from TCGA (n=431 slides, AUC)=0.84) and rectal cancer biopsies (n=265 slides, AUC=0.85). imCMS spatially resolved intratumoural heterogeneity and provided secondary calls correlating with bioinformatic prediction from molecular data. imCMS classified samples previously unclassifiable by RNA expression profiling, reproduced the expected correlations with genomic and epigenetic alterations and showed similar prognostic associations as transcriptomic CMS. CONCLUSION: This study shows that a prediction of RNA expression classifiers can be made from H&E images, opening the door to simple, cheap and reliable biological stratification within routine workflows.
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spelling pubmed-78734192021-02-18 Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning Sirinukunwattana, Korsuk Domingo, Enric Richman, Susan D Redmond, Keara L Blake, Andrew Verrill, Clare Leedham, Simon J Chatzipli, Aikaterini Hardy, Claire Whalley, Celina M Wu, Chieh-hsi Beggs, Andrew D McDermott, Ultan Dunne, Philip D Meade, Angela Walker, Steven M Murray, Graeme I Samuel, Leslie Seymour, Matthew Tomlinson, Ian Quirke, Phil Maughan, Timothy Rittscher, Jens Koelzer, Viktor H Gut Artificial Intelligence/Machine Learning OBJECTIVE: Complex phenotypes captured on histological slides represent the biological processes at play in individual cancers, but the link to underlying molecular classification has not been clarified or systematised. In colorectal cancer (CRC), histological grading is a poor predictor of disease progression, and consensus molecular subtypes (CMSs) cannot be distinguished without gene expression profiling. We hypothesise that image analysis is a cost-effective tool to associate complex features of tissue organisation with molecular and outcome data and to resolve unclassifiable or heterogeneous cases. In this study, we present an image-based approach to predict CRC CMS from standard H&E sections using deep learning. DESIGN: Training and evaluation of a neural network were performed using a total of n=1206 tissue sections with comprehensive multi-omic data from three independent datasets (training on FOCUS trial, n=278 patients; test on rectal cancer biopsies, GRAMPIAN cohort, n=144 patients; and The Cancer Genome Atlas (TCGA), n=430 patients). Ground truth CMS calls were ascertained by matching random forest and single sample predictions from CMS classifier. RESULTS: Image-based CMS (imCMS) accurately classified slides in unseen datasets from TCGA (n=431 slides, AUC)=0.84) and rectal cancer biopsies (n=265 slides, AUC=0.85). imCMS spatially resolved intratumoural heterogeneity and provided secondary calls correlating with bioinformatic prediction from molecular data. imCMS classified samples previously unclassifiable by RNA expression profiling, reproduced the expected correlations with genomic and epigenetic alterations and showed similar prognostic associations as transcriptomic CMS. CONCLUSION: This study shows that a prediction of RNA expression classifiers can be made from H&E images, opening the door to simple, cheap and reliable biological stratification within routine workflows. BMJ Publishing Group 2021-03 2020-07-20 /pmc/articles/PMC7873419/ /pubmed/32690604 http://dx.doi.org/10.1136/gutjnl-2019-319866 Text en © Author(s) (or their employer(s)) 2021. Re-use permitted under CC BY. Published by BMJ. https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See: https://creativecommons.org/licenses/by/4.0/.
spellingShingle Artificial Intelligence/Machine Learning
Sirinukunwattana, Korsuk
Domingo, Enric
Richman, Susan D
Redmond, Keara L
Blake, Andrew
Verrill, Clare
Leedham, Simon J
Chatzipli, Aikaterini
Hardy, Claire
Whalley, Celina M
Wu, Chieh-hsi
Beggs, Andrew D
McDermott, Ultan
Dunne, Philip D
Meade, Angela
Walker, Steven M
Murray, Graeme I
Samuel, Leslie
Seymour, Matthew
Tomlinson, Ian
Quirke, Phil
Maughan, Timothy
Rittscher, Jens
Koelzer, Viktor H
Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
title Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
title_full Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
title_fullStr Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
title_full_unstemmed Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
title_short Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
title_sort image-based consensus molecular subtype (imcms) classification of colorectal cancer using deep learning
topic Artificial Intelligence/Machine Learning
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7873419/
https://www.ncbi.nlm.nih.gov/pubmed/32690604
http://dx.doi.org/10.1136/gutjnl-2019-319866
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