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Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study

Deep learning (DL) can accelerate the prediction of prognostic biomarkers from routine pathology slides in colorectal cancer (CRC). However, current approaches rely on convolutional neural networks (CNNs) and have mostly been validated on small patient cohorts. Here, we develop a new transformer-bas...

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Autores principales: Wagner, Sophia J., Reisenbüchler, Daniel, West, Nicholas P., Niehues, Jan Moritz, Zhu, Jiefu, Foersch, Sebastian, Veldhuizen, Gregory Patrick, Quirke, Philip, Grabsch, Heike I., van den Brandt, Piet A., Hutchins, Gordon G.A., Richman, Susan D., Yuan, Tanwei, Langer, Rupert, Jenniskens, Josien C.A., Offermans, Kelly, Mueller, Wolfram, Gray, Richard, Gruber, Stephen B., Greenson, Joel K., Rennert, Gad, Bonner, Joseph D., Schmolze, Daniel, Jonnagaddala, Jitendra, Hawkins, Nicholas J., Ward, Robyn L., Morton, Dion, Seymour, Matthew, Magill, Laura, Nowak, Marta, Hay, Jennifer, Koelzer, Viktor H., Church, David N., Matek, Christian, Geppert, Carol, Peng, Chaolong, Zhi, Cheng, Ouyang, Xiaoming, James, Jacqueline A., Loughrey, Maurice B., Salto-Tellez, Manuel, Brenner, Hermann, Hoffmeister, Michael, Truhn, Daniel, Schnabel, Julia A., Boxberg, Melanie, Peng, Tingying, Kather, Jakob Nikolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507381/
https://www.ncbi.nlm.nih.gov/pubmed/37652006
http://dx.doi.org/10.1016/j.ccell.2023.08.002
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author Wagner, Sophia J.
Reisenbüchler, Daniel
West, Nicholas P.
Niehues, Jan Moritz
Zhu, Jiefu
Foersch, Sebastian
Veldhuizen, Gregory Patrick
Quirke, Philip
Grabsch, Heike I.
van den Brandt, Piet A.
Hutchins, Gordon G.A.
Richman, Susan D.
Yuan, Tanwei
Langer, Rupert
Jenniskens, Josien C.A.
Offermans, Kelly
Mueller, Wolfram
Gray, Richard
Gruber, Stephen B.
Greenson, Joel K.
Rennert, Gad
Bonner, Joseph D.
Schmolze, Daniel
Jonnagaddala, Jitendra
Hawkins, Nicholas J.
Ward, Robyn L.
Morton, Dion
Seymour, Matthew
Magill, Laura
Nowak, Marta
Hay, Jennifer
Koelzer, Viktor H.
Church, David N.
Matek, Christian
Geppert, Carol
Peng, Chaolong
Zhi, Cheng
Ouyang, Xiaoming
James, Jacqueline A.
Loughrey, Maurice B.
Salto-Tellez, Manuel
Brenner, Hermann
Hoffmeister, Michael
Truhn, Daniel
Schnabel, Julia A.
Boxberg, Melanie
Peng, Tingying
Kather, Jakob Nikolas
author_facet Wagner, Sophia J.
Reisenbüchler, Daniel
West, Nicholas P.
Niehues, Jan Moritz
Zhu, Jiefu
Foersch, Sebastian
Veldhuizen, Gregory Patrick
Quirke, Philip
Grabsch, Heike I.
van den Brandt, Piet A.
Hutchins, Gordon G.A.
Richman, Susan D.
Yuan, Tanwei
Langer, Rupert
Jenniskens, Josien C.A.
Offermans, Kelly
Mueller, Wolfram
Gray, Richard
Gruber, Stephen B.
Greenson, Joel K.
Rennert, Gad
Bonner, Joseph D.
Schmolze, Daniel
Jonnagaddala, Jitendra
Hawkins, Nicholas J.
Ward, Robyn L.
Morton, Dion
Seymour, Matthew
Magill, Laura
Nowak, Marta
Hay, Jennifer
Koelzer, Viktor H.
Church, David N.
Matek, Christian
Geppert, Carol
Peng, Chaolong
Zhi, Cheng
Ouyang, Xiaoming
James, Jacqueline A.
Loughrey, Maurice B.
Salto-Tellez, Manuel
Brenner, Hermann
Hoffmeister, Michael
Truhn, Daniel
Schnabel, Julia A.
Boxberg, Melanie
Peng, Tingying
Kather, Jakob Nikolas
author_sort Wagner, Sophia J.
collection PubMed
description Deep learning (DL) can accelerate the prediction of prognostic biomarkers from routine pathology slides in colorectal cancer (CRC). However, current approaches rely on convolutional neural networks (CNNs) and have mostly been validated on small patient cohorts. Here, we develop a new transformer-based pipeline for end-to-end biomarker prediction from pathology slides by combining a pre-trained transformer encoder with a transformer network for patch aggregation. Our transformer-based approach substantially improves the performance, generalizability, data efficiency, and interpretability as compared with current state-of-the-art algorithms. After training and evaluating on a large multicenter cohort of over 13,000 patients from 16 colorectal cancer cohorts, we achieve a sensitivity of 0.99 with a negative predictive value of over 0.99 for prediction of microsatellite instability (MSI) on surgical resection specimens. We demonstrate that resection specimen-only training reaches clinical-grade performance on endoscopic biopsy tissue, solving a long-standing diagnostic problem.
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spelling pubmed-105073812023-09-20 Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study Wagner, Sophia J. Reisenbüchler, Daniel West, Nicholas P. Niehues, Jan Moritz Zhu, Jiefu Foersch, Sebastian Veldhuizen, Gregory Patrick Quirke, Philip Grabsch, Heike I. van den Brandt, Piet A. Hutchins, Gordon G.A. Richman, Susan D. Yuan, Tanwei Langer, Rupert Jenniskens, Josien C.A. Offermans, Kelly Mueller, Wolfram Gray, Richard Gruber, Stephen B. Greenson, Joel K. Rennert, Gad Bonner, Joseph D. Schmolze, Daniel Jonnagaddala, Jitendra Hawkins, Nicholas J. Ward, Robyn L. Morton, Dion Seymour, Matthew Magill, Laura Nowak, Marta Hay, Jennifer Koelzer, Viktor H. Church, David N. Matek, Christian Geppert, Carol Peng, Chaolong Zhi, Cheng Ouyang, Xiaoming James, Jacqueline A. Loughrey, Maurice B. Salto-Tellez, Manuel Brenner, Hermann Hoffmeister, Michael Truhn, Daniel Schnabel, Julia A. Boxberg, Melanie Peng, Tingying Kather, Jakob Nikolas Cancer Cell Article Deep learning (DL) can accelerate the prediction of prognostic biomarkers from routine pathology slides in colorectal cancer (CRC). However, current approaches rely on convolutional neural networks (CNNs) and have mostly been validated on small patient cohorts. Here, we develop a new transformer-based pipeline for end-to-end biomarker prediction from pathology slides by combining a pre-trained transformer encoder with a transformer network for patch aggregation. Our transformer-based approach substantially improves the performance, generalizability, data efficiency, and interpretability as compared with current state-of-the-art algorithms. After training and evaluating on a large multicenter cohort of over 13,000 patients from 16 colorectal cancer cohorts, we achieve a sensitivity of 0.99 with a negative predictive value of over 0.99 for prediction of microsatellite instability (MSI) on surgical resection specimens. We demonstrate that resection specimen-only training reaches clinical-grade performance on endoscopic biopsy tissue, solving a long-standing diagnostic problem. Cell Press 2023-09-11 /pmc/articles/PMC10507381/ /pubmed/37652006 http://dx.doi.org/10.1016/j.ccell.2023.08.002 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Wagner, Sophia J.
Reisenbüchler, Daniel
West, Nicholas P.
Niehues, Jan Moritz
Zhu, Jiefu
Foersch, Sebastian
Veldhuizen, Gregory Patrick
Quirke, Philip
Grabsch, Heike I.
van den Brandt, Piet A.
Hutchins, Gordon G.A.
Richman, Susan D.
Yuan, Tanwei
Langer, Rupert
Jenniskens, Josien C.A.
Offermans, Kelly
Mueller, Wolfram
Gray, Richard
Gruber, Stephen B.
Greenson, Joel K.
Rennert, Gad
Bonner, Joseph D.
Schmolze, Daniel
Jonnagaddala, Jitendra
Hawkins, Nicholas J.
Ward, Robyn L.
Morton, Dion
Seymour, Matthew
Magill, Laura
Nowak, Marta
Hay, Jennifer
Koelzer, Viktor H.
Church, David N.
Matek, Christian
Geppert, Carol
Peng, Chaolong
Zhi, Cheng
Ouyang, Xiaoming
James, Jacqueline A.
Loughrey, Maurice B.
Salto-Tellez, Manuel
Brenner, Hermann
Hoffmeister, Michael
Truhn, Daniel
Schnabel, Julia A.
Boxberg, Melanie
Peng, Tingying
Kather, Jakob Nikolas
Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study
title Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study
title_full Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study
title_fullStr Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study
title_full_unstemmed Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study
title_short Transformer-based biomarker prediction from colorectal cancer histology: A large-scale multicentric study
title_sort transformer-based biomarker prediction from colorectal cancer histology: a large-scale multicentric study
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507381/
https://www.ncbi.nlm.nih.gov/pubmed/37652006
http://dx.doi.org/10.1016/j.ccell.2023.08.002
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