Data-efficient and weakly supervised computational pathology on whole-slide images

被引:982
作者
Lu, Ming Y. [1 ,2 ,3 ]
Williamson, Drew F. K. [1 ]
Chen, Tiffany Y. [1 ]
Chen, Richard J. [1 ,4 ]
Barbieri, Matteo [1 ]
Mahmood, Faisal [1 ,2 ,3 ]
机构
[1] Harvard Med Sch, Brigham & Womens Hosp, Dept Pathol, Boston, MA 02115 USA
[2] Broad Inst Harvard & MIT, Canc Program, Cambridge, MA 02142 USA
[3] Dana Farber Canc Inst, Canc Data Sci, Boston, MA 02115 USA
[4] Harvard Med Sch, Dept Biomed Informat, Boston, MA 02115 USA
关键词
PROSTATE-CANCER; DEEP; BIOPSIES; SYSTEM;
D O I
10.1038/s41551-020-00682-w
中图分类号
R318 [生物医学工程];
学科分类号
0831 ;
摘要
Deep-learning methods for computational pathology require either manual annotation of gigapixel whole-slide images (WSIs) or large datasets of WSIs with slide-level labels and typically suffer from poor domain adaptation and interpretability. Here we report an interpretable weakly supervised deep-learning method for data-efficient WSI processing and learning that only requires slide-level labels. The method, which we named clustering-constrained-attention multiple-instance learning (CLAM), uses attention-based learning to identify subregions of high diagnostic value to accurately classify whole slides and instance-level clustering over the identified representative regions to constrain and refine the feature space. By applying CLAM to the subtyping of renal cell carcinoma and non-small-cell lung cancer as well as the detection of lymph node metastasis, we show that it can be used to localize well-known morphological features on WSIs without the need for spatial labels, that it overperforms standard weakly supervised classification algorithms and that it is adaptable to independent test cohorts, smartphone microscopy and varying tissue content. A data-efficient and interpretable deep-learning method for the multi-class classification of whole-slide images that relies only on slide-level labels is applied to the detection of lymph node metastasis and to cancer subtyping.
引用
收藏
页码:555 / +
页数:19
相关论文
共 47 条
[1]   Systematic Analysis of Breast Cancer Morphology Uncovers Stromal Features Associated with Survival [J].
Beck, Andrew H. ;
Sangoi, Ankur R. ;
Leung, Samuel ;
Marinelli, Robert J. ;
Nielsen, Torsten O. ;
van de Vijver, Marc J. ;
West, Robert B. ;
van de Rijn, Matt ;
Koller, Daphne .
SCIENCE TRANSLATIONAL MEDICINE, 2011, 3 (108)
[2]   Diagnostic Assessment of Deep Learning Algorithms for Detection of Lymph Node Metastases in Women With Breast Cancer [J].
Bejnordi, Babak Ehteshami ;
Veta, Mitko ;
van Diest, Paul Johannes ;
van Ginneken, Bram ;
Karssemeijer, Nico ;
Litjens, Geert ;
van der Laak, Jeroen A. W. M. .
JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION, 2017, 318 (22) :2199-2210
[3]   Adversarial Stain Transfer for Histopathology Image Analysis [J].
BenTaieb, Aicha ;
Hamarneh, Ghassan .
IEEE TRANSACTIONS ON MEDICAL IMAGING, 2018, 37 (03) :792-802
[4]   Artificial intelligence in digital pathology - new tools for diagnosis and precision oncology [J].
Bera, Kaustav ;
Schalper, Kurt A. ;
Rimm, David L. ;
Velcheti, Vamsidhar ;
Madabhushi, Anant .
NATURE REVIEWS CLINICAL ONCOLOGY, 2019, 16 (11) :703-715
[5]   Automated deep-learning system for Gleason grading of prostate cancer using biopsies: a diagnostic study [J].
Bulten, Wouter ;
Pinckaers, Hans ;
van Boven, Hester ;
Vink, Robert ;
de Bel, Thomas ;
van Ginneken, Bram ;
van der Laak, Jeroen ;
Hulsbergen-van de Kaa, Christina ;
Litjens, Geert .
LANCET ONCOLOGY, 2020, 21 (02) :233-241
[6]   Clinical-grade computational pathology using weakly supervised deep learning on whole slide images [J].
Campanella, Gabriele ;
Hanna, Matthew G. ;
Geneslaw, Luke ;
Miraflor, Allen ;
Silva, Vitor Werneck Krauss ;
Busam, Klaus J. ;
Brogi, Edi ;
Reuter, Victor E. ;
Klimstra, David S. ;
Fuchs, Thomas J. .
NATURE MEDICINE, 2019, 25 (08) :1301-+
[7]   An augmented reality microscope with real-time artificial intelligence integration for cancer diagnosis [J].
Chen, Po-Hsuan Cameron ;
Gadepalli, Krishna ;
MacDonald, Robert ;
Liu, Yun ;
Kadowaki, Shiro ;
Nagpal, Kunal ;
Kohlberger, Timo ;
Dean, Jeffrey ;
Corrado, Greg S. ;
Hipp, Jason D. ;
Mermel, Craig H. ;
Stumpe, Martin C. .
NATURE MEDICINE, 2019, 25 (09) :1453-+
[8]  
Chen RJ, 2022, IEEE T MED IMAGING, V41, P757, DOI [10.1109/TMI.2020.3021387, 10.1109/TITS.2020.3030218]
[9]   Classification and mutation prediction from non-small cell lung cancer histopathology images using deep learning [J].
Coudray, Nicolas ;
Ocampo, Paolo Santiago ;
Sakellaropoulos, Theodore ;
Narula, Navneet ;
Snuderl, Matija ;
Fenyo, David ;
Moreira, Andre L. ;
Razavian, Narges ;
Tsirigos, Aristotelis .
NATURE MEDICINE, 2018, 24 (10) :1559-+
[10]   Multiple Instance Learning for Heterogeneous Images: Training a CNN for Histopathology [J].
Couture, Heather D. ;
Marron, J. S. ;
Perou, Charles M. ;
Troester, Melissa A. ;
Niethammer, Marc .
MEDICAL IMAGE COMPUTING AND COMPUTER ASSISTED INTERVENTION - MICCAI 2018, PT II, 2018, 11071 :254-262