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Swarm learning for decentralized artificial intelligence in cancer histopathology

Oliver Lester Saldanha, Philip Quirke, Nicholas P. West, Jacqueline A. James, Maurice B. Loughrey, Heike I. Grabsch, Manuel Salto-Tellez, Elizabeth Alwers, Didem Cifci, Narmin Ghaffari Laleh, Tobias Seibel, Richard Gray, Gordon G. A. Hutchins, Hermann Brenner, Tanwei Yuan, Titus J. Brinker, Jenny Chang-Claude, Firas Khader, Andreas Schuppert, Tom Luedde, Sebastian Foersch, Hannah Sophie Muti, Christian Trautwein, Michael Hoffmeister, Daniel Truhn, View ORCID ProfileJakob Nikolas Kather
doi: https://doi.org/10.1101/2021.11.19.469139
Oliver Lester Saldanha
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Philip Quirke
2Pathology & Data Analytics, Leeds Institute of Medical Research at St James’s, University of Leeds, Leeds, United Kingdom
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Nicholas P. West
2Pathology & Data Analytics, Leeds Institute of Medical Research at St James’s, University of Leeds, Leeds, United Kingdom
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Jacqueline A. James
3Precision Medicine Centre of Excellence, Health Sciences Building, The Patrick G Johnston Centre for Cancer Research, Queen’s University Belfast, United Kingdom
4Regional Molecular Diagnostic Service, Belfast Health and Social Care Trust, Belfast, United Kingdom
5The Patrick G Johnston Centre for Cancer Research, Queen’s University Belfast, United Kingdom
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Maurice B. Loughrey
5The Patrick G Johnston Centre for Cancer Research, Queen’s University Belfast, United Kingdom
6Department of Cellular Pathology, Belfast Health and Social Care Trust, Belfast, United Kingdom
7Centre for Public Health, Queen’s University Belfast, United Kingdom
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Heike I. Grabsch
2Pathology & Data Analytics, Leeds Institute of Medical Research at St James’s, University of Leeds, Leeds, United Kingdom
8Pathology and GROW School for Oncology and Developmental Biology, Maastricht University Medical Center+, Maastricht, The Netherlands
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Manuel Salto-Tellez
3Precision Medicine Centre of Excellence, Health Sciences Building, The Patrick G Johnston Centre for Cancer Research, Queen’s University Belfast, United Kingdom
4Regional Molecular Diagnostic Service, Belfast Health and Social Care Trust, Belfast, United Kingdom
5The Patrick G Johnston Centre for Cancer Research, Queen’s University Belfast, United Kingdom
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Elizabeth Alwers
9Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Didem Cifci
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Narmin Ghaffari Laleh
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Tobias Seibel
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Richard Gray
10Clinical Trial Service Unit, University of Oxford, Oxford, United Kingdom
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Gordon G. A. Hutchins
2Pathology & Data Analytics, Leeds Institute of Medical Research at St James’s, University of Leeds, Leeds, United Kingdom
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Hermann Brenner
9Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
11Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany
12German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany
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Tanwei Yuan
9Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Titus J. Brinker
13Digital Biomarkers for Oncology Group (DBO), National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany
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Jenny Chang-Claude
14Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
15Cancer Epidemiology Group, University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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Firas Khader
16Department of Diagnostic and Interventional Radiology, University Hospital RWTH Aachen, Aachen, Germany
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Andreas Schuppert
17Institute for Computational Biomedicine, JRC for Computational Biomedicine, RWTH Aachen University, University Hospital Aachen, Aachen, Germany
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Tom Luedde
18Department of Gastroenterology, Hepatology and Infectious Diseases, Medical Faculty of Heinrich Heine University Düsseldorf, University Hospital Düsseldorf, Düsseldorf, Germany
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Sebastian Foersch
19Institute of Pathology, University Medical Center Mainz, Mainz, Germany
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Hannah Sophie Muti
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Christian Trautwein
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Michael Hoffmeister
9Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Daniel Truhn
16Department of Diagnostic and Interventional Radiology, University Hospital RWTH Aachen, Aachen, Germany
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Jakob Nikolas Kather
1Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany
2Pathology & Data Analytics, Leeds Institute of Medical Research at St James’s, University of Leeds, Leeds, United Kingdom
12German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany
20Medical Oncology, National Center for Tumor Diseases (NCT), University Hospital Heidelberg, Heidelberg, Germany
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  • ORCID record for Jakob Nikolas Kather
  • For correspondence: jakob.kather@gmail.com
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Abstract

Artificial Intelligence (AI) can extract clinically actionable information from medical image data. In cancer histopathology, AI can be used to predict the presence of molecular alterations directly from routine histopathology slides. However, training robust AI systems requires large datasets whose collection faces practical, ethical and legal obstacles. These obstacles could be overcome with swarm learning (SL) where partners jointly train AI models, while avoiding data transfer and monopolistic data governance. Here, for the first time, we demonstrate the successful use of SL in large, multicentric datasets of gigapixel histopathology images comprising over 5000 patients. We show that AI models trained using Swarm Learning can predict BRAF mutational status and microsatellite instability (MSI) directly from hematoxylin and eosin (H&E)-stained pathology slides of colorectal cancer (CRC). We trained AI models on three patient cohorts from Northern Ireland, Germany and the United States of America and validated the prediction performance in two independent datasets from the United Kingdom using SL-based AI models. Our data show that SL enables us to train AI models which outperform most locally trained models and perform on par with models which are centrally trained on the merged datasets. In addition, we show that SL-based AI models are data efficient and maintain a robust performance even if only subsets of local datasets are used for training. In the future, SL can be used to train distributed AI models for any histopathology image analysis tasks, overcoming the need for data transfer and without requiring institutions to give up control of the final AI model.

Competing Interest Statement

JNK declares consulting services for Owkin, France and Panakeia, UK. PQ and NW declare research funding from Roche and PQ consulting and speaker services for Roche. MST has recently received honoraria for advisory work in relation to the following companies: Incyte, MindPeak, MSD, BMS and Sonrai; these are all unrelated to this work. No other potential conflicts of interest are reported by any of the authors. The authors received advice from the customer support team of Hewlett Packard Enterprise (HPE) when performing this study, but HPE did not have any role in study design, conducting the experiments, interpretation of the results or decision to submit for publication.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted November 20, 2021.
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Swarm learning for decentralized artificial intelligence in cancer histopathology
Oliver Lester Saldanha, Philip Quirke, Nicholas P. West, Jacqueline A. James, Maurice B. Loughrey, Heike I. Grabsch, Manuel Salto-Tellez, Elizabeth Alwers, Didem Cifci, Narmin Ghaffari Laleh, Tobias Seibel, Richard Gray, Gordon G. A. Hutchins, Hermann Brenner, Tanwei Yuan, Titus J. Brinker, Jenny Chang-Claude, Firas Khader, Andreas Schuppert, Tom Luedde, Sebastian Foersch, Hannah Sophie Muti, Christian Trautwein, Michael Hoffmeister, Daniel Truhn, Jakob Nikolas Kather
bioRxiv 2021.11.19.469139; doi: https://doi.org/10.1101/2021.11.19.469139
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Swarm learning for decentralized artificial intelligence in cancer histopathology
Oliver Lester Saldanha, Philip Quirke, Nicholas P. West, Jacqueline A. James, Maurice B. Loughrey, Heike I. Grabsch, Manuel Salto-Tellez, Elizabeth Alwers, Didem Cifci, Narmin Ghaffari Laleh, Tobias Seibel, Richard Gray, Gordon G. A. Hutchins, Hermann Brenner, Tanwei Yuan, Titus J. Brinker, Jenny Chang-Claude, Firas Khader, Andreas Schuppert, Tom Luedde, Sebastian Foersch, Hannah Sophie Muti, Christian Trautwein, Michael Hoffmeister, Daniel Truhn, Jakob Nikolas Kather
bioRxiv 2021.11.19.469139; doi: https://doi.org/10.1101/2021.11.19.469139

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