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Whole-Slide Mitosis Detection in H&E Breast Histology Using PHH3 as a Reference to Train Distilled Stain-Invariant Convolutional Networks

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Tellez, David, Balkenhol, Maschenka, Otte-Höller, Irene, van de Loo, Rob, Vogels, Rob, Bult, Peter, Wauters, Carla, Vreuls, Willem, Mol, Suzanne, Karssemeijer, Nico, Litjens, Geert, van der Laak, Jeroen, Ciompi, Francesco·2018·IEEE Transactions on Medical Imaging

DOI 10.1109/tmi.2018.2820199

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Abstract

Manual counting of mitotic tumor cells in tissue sections constitutes one of the strongest prognostic markers for breast cancer. This procedure, however, is time-consuming and error-prone. We developed a method to automatically detect mitotic figures in breast cancer tissue sections based on convolutional neural networks (CNNs). Application of CNNs to hematoxylin and eosin (H&E) stained histological tissue sections is hampered by noisy and expensive reference standards established by pathologists, lack of generalization due to staining variation across laboratories, and high computational requirements needed to process gigapixel whole-slide images (WSIs). In this paper, we present a method to train and evaluate CNNs to specifically solve these issues in the context of mitosis detection in breast cancer WSIs. First, by combining image analysis of mitotic activity in phosphohistone-H3 restained slides and registration, we built a reference standard for mitosis detection in entire H&E WSIs requiring minimal manual annotation effort. Second, we designed a data augmentation strategy that creates diverse and realistic H&E stain variations by modifying H&E color channels directly. Using it during training combined with network ensembling resulted in a stain invariant mitosis detector. Third, we applied knowledge distillation to reduce the computational requirements of the mitosis detection ensemble with a negligible loss of performance. The system was trained in a single-center cohort and evaluated in an independent multicenter cohort from the cancer genome atlas on the three tasks of the tumor proliferation assessment challenge. We obtained a performance within the top three best methods for most of the tasks of the challenge.

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Authors: Tellez, D., Balkenhol, M., Otte-Höller, I., van de Loo, R., Vogels, R., Bult, P., Wauters, C., Vreuls, W., Mol, S., Karssemeijer, N., Litjens, G., van der Laak, J., & Ciompi, F.
Affiliations: Radboud University Medical Center (NL)
Canisius-Wilhelmina Ziekenhuis (NL)
Jeroen Bosch Ziekenhuis (NL)
ORCID: Tellez, David
Vreuls, Willem
Litjens, Geert
van der Laak, Jeroen
Ciompi, Francesco
Venue: IEEE Transactions on Medical Imaging
Publisher: Institute of Electrical and Electronics Engineers (IEEE)
Published: 2018-09
Volume: 37
Issue: 9
Pages: 2126-2136
ISSN: 0278-0062 (ISSN-L)
1558-254X
DOI: 10.1109/tmi.2018.2820199
OpenAlex: W2794616003
Cited by: 288
References: 27
Citations by year: 2026: 16 · 2025: 27 · 2024: 49 · 2023: 41 · 2022: 47 · 2021: 41 · 2020: 39 · 2019: 24 · 2018: 3
FWCI: 15.06
Type: journal article
Language: en
Open access: green
arxiv.org
Licence: ieeexplore.ieee.org/Xplorehelp/downloads/license-information/IEEE.html (vor)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
Locations: IEEE Transactions on Medical Imaging (publishedVersion)
PubMed (publishedVersion)
arXiv (Cornell University) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion, other-oa)
arXiv (Cornell University)
Funders: Radboud Universitair Medisch Centrum
Topics: Physical Sciences › Computer Science › Artificial Intelligence › AI in cancer detection
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Cell Image Analysis Techniques
Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Digital Imaging for Blood Diseases
Keywords: mitosis detection, breast cancer, whole slide images, H&E staining, knowledge distillation, data augmentation, image registration, tumor cell proliferation, histopathology, convolutional neural networks

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Whole-Slide Mitosis Detection in H&E Breast Histology Using PHH3 as a Reference to Train Distilled Stain-Invariant Convolutional Networks

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