Journal Article
. 2018 Apr; 23(1):181-193.e7.
doi: 10.1016/j.celrep.2018.03.086.

Spatial Organization and Molecular Correlation of Tumor-Infiltrating Lymphocytes Using Deep Learning on Pathology Images

Joel Saltz 1 Rajarsi Gupta 2 Le Hou 3 Tahsin Kurc 4 Pankaj Singh 5 Vu Nguyen 3 Dimitris Samaras 3 Kenneth R Shroyer 6 Tianhao Zhao 6 Rebecca Batiste 6 John Van Arnam 7 Cancer Genome Atlas Research Network  Ilya Shmulevich 8 Arvind U K Rao 9 Alexander J Lazar 10 Ashish Sharma 11 Vésteinn Thorsson 12 
Affiliations
  • PMID: 29617659
  •     37 References
  •     143 citations

Abstract

Beyond sample curation and basic pathologic characterization, the digitized H&E-stained images of TCGA samples remain underutilized. To highlight this resource, we present mappings of tumor-infiltrating lymphocytes (TILs) based on H&E images from 13 TCGA tumor types. These TIL maps are derived through computational staining using a convolutional neural network trained to classify patches of images. Affinity propagation revealed local spatial structure in TIL patterns and correlation with overall survival. TIL map structural patterns were grouped using standard histopathological parameters. These patterns are enriched in particular T cell subpopulations derived from molecular measures. TIL densities and spatial structure were differentially enriched among tumor types, immune subtypes, and tumor molecular subtypes, implying that spatial infiltrate state could reflect particular tumor cell aberration states. Obtaining spatial lymphocytic patterns linked to the rich genomic characterization of TCGA samples demonstrates one use for the TCGA image archives with insights into the tumor-immune microenvironment.

Keywords: artificial intelligence; bioinformatics; computer vision; deep learning; digital pathology; immuno-oncology; lymphocytes; machine learning; tumor microenvironment; tumor-infiltrating lymphocytes.

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Nat Commun, 2020 Aug 05; 11(1). PMID: 32747659    Free PMC article.
An annotated fluorescence image dataset for training nuclear segmentation methods.
Florian Kromp, Eva Bozsaky, +11 authors, Sabine Taschner-Mandl.
Sci Data, 2020 Aug 13; 7(1). PMID: 32782410    Free PMC article.
Prognostic Significance of Immune Cell Populations Identified by Machine Learning in Colorectal Cancer Using Routine Hematoxylin and Eosin-Stained Sections.
Juha P Väyrynen, Mai Chan Lau, +24 authors, Jonathan A Nowak.
Clin Cancer Res, 2020 May 23; 26(16). PMID: 32439699    Free PMC article.
Digital pathology and computational image analysis in nephropathology.
Laura Barisoni, Kyle J Lafata, +2 authors, Ulysses G J Balis.
Nat Rev Nephrol, 2020 Aug 28; 16(11). PMID: 32848206    Free PMC article.
Review.
Tumor Infiltrating Lymphocytes in Pet Rabbit Mammary Carcinomas: A Study with Relevance to Comparative Pathology.
Sandra Schöniger, Sophie Degner, +4 authors, Heinz-Adolf Schoon.
Animals (Basel), 2020 Aug 23; 10(8). PMID: 32824521    Free PMC article.
Artificial Intelligence to Decode Cancer Mechanism: Beyond Patient Stratification for Precision Oncology.
Sandip Kumar Patel, Bhawana George, Vineeta Rai.
Front Pharmacol, 2020 Sep 10; 11. PMID: 32903628    Free PMC article.
Review.
Molecular, clinicopathological, and immune correlates of LAG3 promoter DNA methylation in melanoma.
Anne Fröhlich, Judith Sirokay, +19 authors, Dimo Dietrich.
EBioMedicine, 2020 Aug 30; 59. PMID: 32861198    Free PMC article.
Tumor immune profiles noninvasively estimated by FDG PET with deep learning correlate with immunotherapy response in lung adenocarcinoma.
Changhee Park, Kwon Joong Na, +14 authors, Dae Seog Heo.
Theranostics, 2020 Sep 16; 10(23). PMID: 32929383    Free PMC article.
Artificial Intelligence and Digital Pathology: Challenges and Opportunities.
Hamid Reza Tizhoosh, Liron Pantanowitz.
J Pathol Inform, 2019 Jan 05; 9. PMID: 30607305    Free PMC article.
Highly Cited. Review.
Sparse Autoencoder for Unsupervised Nucleus Detection and Representation in Histopathology Images.
Le Hou, Vu Nguyen, +8 authors, Joel H Saltz.
Pattern Recognit, 2019 Jan 12; 86. PMID: 30631215    Free PMC article.
Integrative Analysis of Novel Metabolic Subtypes in Pancreatic Cancer Fosters New Prognostic Biomarkers.
Laura Follia, Giulio Ferrero, +12 authors, Francesca Cordero.
Front Oncol, 2019 Mar 16; 9. PMID: 30873387    Free PMC article.
Segmentation of Glomeruli Within Trichrome Images Using Deep Learning.
Shruti Kannan, Laura A Morgan, +9 authors, Vijaya B Kolachalama.
Kidney Int Rep, 2019 Jul 19; 4(7). PMID: 31317118    Free PMC article.
Survival outcome prediction in cervical cancer: Cox models vs deep-learning model.
Koji Matsuo, Sanjay Purushotham, +4 authors, Lynda D Roman.
Am J Obstet Gynecol, 2018 Dec 26; 220(4). PMID: 30582927    Free PMC article.
Do innate killing mechanisms activated by inflammasomes have a role in treating melanoma?
Abdullah Al Emran, Hsin-Yi Tseng, +6 authors, Peter Hersey.
Pigment Cell Melanoma Res, 2020 Feb 07; 33(5). PMID: 32027447    Free PMC article.
Review.
Tumor-Infiltrating Lymphocytes and Their Prognostic Value in Cutaneous Melanoma.
Fabienne Maibach, Hassan Sadozai, +2 authors, Mirjam Schenk.
Front Immunol, 2020 Oct 06; 11. PMID: 33013886    Free PMC article.
Review.
Prognostic significance of spatial immune profiles in human solid cancers.
Takahiro Tsujikawa, Junichi Mitsuda, +4 authors, Shigeru Hirano.
Cancer Sci, 2020 Jul 30; 111(10). PMID: 32726495    Free PMC article.
Review.
Development and interpretation of a pathomics-based model for the prediction of microsatellite instability in Colorectal Cancer.
Rui Cao, Fan Yang, +17 authors, Zhong-Yi Dong.
Theranostics, 2020 Oct 13; 10(24). PMID: 33042271    Free PMC article.
Predicting Relapse in Patients With Triple Negative Breast Cancer (TNBC) Using a Deep-Learning Approach.
Guangyuan Yu, Xuefei Li, +12 authors, Herbert Levine.
Front Physiol, 2020 Oct 20; 11. PMID: 33071806    Free PMC article.
Driverless artificial intelligence framework for the identification of malignant pleural effusion.
Yuan Li, Shan Tian, Yajun Huang, Weiguo Dong.
Transl Oncol, 2020 Oct 13; 14(1). PMID: 33045678    Free PMC article.
Tumor Infiltrating Lymphocytes Signature as a New Pan-Cancer Predictive Biomarker of Anti PD-1/PD-L1 Efficacy.
Elise Ballot, Sylvain Ladoire, +2 authors, François Ghiringhelli.
Cancers (Basel), 2020 Aug 30; 12(9). PMID: 32858956    Free PMC article.
Spatial and Temporal Changes in PD-L1 Expression in Cancer: The Role of Genetic Drivers, Tumor Microenvironment and Resistance to Therapy.
Elena Shklovskaya, Helen Rizos.
Int J Mol Sci, 2020 Oct 01; 21(19). PMID: 32992658    Free PMC article.
Review.
Combining multiple spatial statistics enhances the description of immune cell localisation within tumours.
Joshua A Bull, Philip S Macklin, +4 authors, Helen M Byrne.
Sci Rep, 2020 Oct 31; 10(1). PMID: 33122646    Free PMC article.
Using deep learning to predict anti-PD-1 response in melanoma and lung cancer patients from histopathology images.
Jing Hu, Chuanliang Cui, +4 authors, Yan Kong.
Transl Oncol, 2020 Nov 01; 14(1). PMID: 33129113    Free PMC article.
Review.
Spatial transcriptomics inferred from pathology whole-slide images links tumor heterogeneity to survival in breast and lung cancer.
Alona Levy-Jurgenson, Xavier Tekpli, Vessela N Kristensen, Zohar Yakhini.
Sci Rep, 2020 Nov 04; 10(1). PMID: 33139755    Free PMC article.
ImageBox 2 - Efficient and Rapid Access of Image Tiles from Whole-Slide Images Using Serverless HTTP Range Requests.
Erich Bremer, Joel Saltz, Jonas S Almeida.
J Pathol Inform, 2020 Nov 10; 11. PMID: 33163255    Free PMC article.
Zeb1 expression by tumor or stromal cells is associated with spatial distribution patterns of CD8+ tumor-infiltrating lymphocytes: a hypothesis-generating study on 113 triple negative breast cancers.
Mona Ouled Dhaou, Myriam Kossai, +4 authors, Nina Radosevic-Robin.
Am J Cancer Res, 2020 Nov 10; 10(10). PMID: 33163276    Free PMC article.
A prognostic model for overall survival of patients with early-stage non-small cell lung cancer: a multicentre, retrospective study.
Cheng Lu, Kaustav Bera, +14 authors, Anant Madabhushi.
Lancet Digit Health, 2020 Nov 10; 2(11). PMID: 33163952    Free PMC article.
CRI iAtlas: an interactive portal for immuno-oncology research.
James A Eddy, Vésteinn Thorsson, +9 authors, Justin Guinney.
F1000Res, 2020 Nov 21; 9. PMID: 33214875    Free PMC article.
Precision immunoprofiling by image analysis and artificial intelligence.
Viktor H Koelzer, Korsuk Sirinukunwattana, Jens Rittscher, Kirsten D Mertz.
Virchows Arch, 2018 Nov 25; 474(4). PMID: 30470933    Free PMC article.
Review.
Joint reconstruction and classification of tumor cells and cell interactions in melanoma tissue sections with synthesized training data.
Alexander Effland, Erich Kobler, +6 authors, Martin Rumpf.
Int J Comput Assist Radiol Surg, 2019 Feb 20; 14(4). PMID: 30779021    Free PMC article.
Artificial intelligence at the intersection of pathology and radiology in prostate cancer.
Stephnie A Harmon, Sena Tuncer, +2 authors, Barış Türkbey.
Diagn Interv Radiol, 2019 May 08; 25(3). PMID: 31063138    Free PMC article.
Review.
Reimagining T Staging Through Artificial Intelligence and Machine Learning Image Processing Approaches in Digital Pathology.
Kaustav Bera, Ian Katz, Anant Madabhushi.
JCO Clin Cancer Inform, 2020 Nov 10; 4. PMID: 33166198    Free PMC article.
Density of CD3+ and CD8+ cells in gingivo-buccal oral squamous cell carcinoma is associated with lymph node metastases and survival.
Geetashree Mukherjee, Swarnendu Bag, +7 authors, Suparna Dutt.
PLoS One, 2020 Nov 20; 15(11). PMID: 33211709    Free PMC article.
Single-Cell Spatial Analysis of Tumor and Immune Microenvironment on Whole-Slide Image Reveals Hepatocellular Carcinoma Subtypes.
Haiyue Wang, Yuming Jiang, +3 authors, Ruijiang Li.
Cancers (Basel), 2020 Dec 03; 12(12). PMID: 33260561    Free PMC article.
Tumour Stroma Ratio Assessment Using Digital Image Analysis Predicts Survival in Triple Negative and Luminal Breast Cancer.
Ewan Ka Millar, Lois H Browne, +4 authors, Peter H Graham.
Cancers (Basel), 2020 Dec 17; 12(12). PMID: 33322174    Free PMC article.
Integrative analysis of histopathological images and chromatin accessibility data for estrogen receptor-positive breast cancer.
Siwen Xu, Zixiao Lu, +6 authors, Yunlong Liu.
BMC Med Genomics, 2020 Dec 30; 13(Suppl 11). PMID: 33371906    Free PMC article.
A new precision medicine initiative at the dawn of exascale computing.
Ruth Nussinov, Hyunbum Jang, +2 authors, Feixiong Cheng.
Signal Transduct Target Ther, 2021 Jan 07; 6(1). PMID: 33402669    Free PMC article.
Review.
A template to quantify the location and density of CD3 + and CD8 + tumor-infiltrating lymphocytes in colon cancer by digital pathology on whole slides for an objective, standardized immune score assessment.
Dordi Lea, Martin Watson, +4 authors, Kjetil Søreide.
Cancer Immunol Immunother, 2021 Jan 14; 70(7). PMID: 33439293
Increased VEGF-A in solid type of lung adenocarcinoma reduces the patients' survival.
Woon Yong Jung, Kyueng-Whan Min, Young Ha Oh.
Sci Rep, 2021 Jan 16; 11(1). PMID: 33446784    Free PMC article.
Tumor infiltrating lymphocyte clusters are associated with response to immune checkpoint inhibition in BRAF V600E/K mutated malignant melanomas.
Sebastian Klein, Cornelia Mauch, +5 authors, Doris Helbig.
Sci Rep, 2021 Jan 21; 11(1). PMID: 33469107    Free PMC article.
Artificial intelligence and computational pathology.
Miao Cui, David Y Zhang.
Lab Invest, 2021 Jan 18; 101(4). PMID: 33454724    Free PMC article.
Review.
Designing deep learning studies in cancer diagnostics.
Andreas Kleppe, Ole-Johan Skrede, +3 authors, Håvard E Danielsen.
Nat Rev Cancer, 2021 Jan 31; 21(3). PMID: 33514930
Review.
Automated digital TIL analysis (ADTA) adds prognostic value to standard assessment of depth and ulceration in primary melanoma.
Michael R Moore, Isabel D Friesner, +26 authors, Yvonne M Saenger.
Sci Rep, 2021 Feb 04; 11(1). PMID: 33531581    Free PMC article.
Feature-driven local cell graph (FLocK): New computational pathology-based descriptors for prognosis of lung cancer and HPV status of oropharyngeal cancers.
Cheng Lu, Can Koyuncu, +8 authors, Anant Madabhushi.
Med Image Anal, 2020 Dec 23; 68. PMID: 33352373    Free PMC article.
Artificial Intelligence for Histology-Based Detection of Microsatellite Instability and Prediction of Response to Immunotherapy in Colorectal Cancer.
Lindsey A Hildebrand, Colin J Pierce, +2 authors, Asaf Maoz.
Cancers (Basel), 2021 Jan 27; 13(3). PMID: 33494280    Free PMC article.
Review.

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Next Generation Imaging Techniques to Define Immune Topographies in Solid Tumors.
Violena Pietrobon, Alessandra Cesano, Francesco Marincola, Jakob Nikolas Kather.
Front Immunol, 2021 Feb 16; 11. PMID: 33584676    Free PMC article.
Review.

;. PMID: 33594213
Optimization of an automated tumor-infiltrating lymphocyte algorithm for improved prognostication in primary melanoma.
Margaret Chou, Irineu Illa-Bochaca, +8 authors, Hua Zhong.
Mod Pathol, 2020 Oct 03; 34(3). PMID: 33005020    Free PMC article.
Protein-based immune profiles of basal-like vs. luminal breast cancers.
Andrea Walens, Linnea T Olsson, +11 authors, Benjamin C Calhoun.
Lab Invest, 2021 Feb 25; 101(6). PMID: 33623115    Free PMC article.
Computational Staining of Pathology Images to Study the Tumor Microenvironment in Lung Cancer.
Shidan Wang, Ruichen Rong, +15 authors, Guanghua Xiao.
Cancer Res, 2020 Jan 10; 80(10). PMID: 31915129    Free PMC article.
Tumor immune microenvironment-based classifications of bladder cancer for enhancing the response rate of immunotherapy.
Jialin Meng, Xiaofan Lu, +7 authors, Chaozhao Liang.
Mol Ther Oncolytics, 2021 Mar 06; 20. PMID: 33665361    Free PMC article.
KRAS drives immune evasion in a genetic model of pancreatic cancer.
Irene Ischenko, Stephen D'Amico, +5 authors, Nancy C Reich.
Nat Commun, 2021 Mar 07; 12(1). PMID: 33674596    Free PMC article.
GestAltNet: aggregation and attention to improve deep learning of gestational age from placental whole-slide images.
Pooya Mobadersany, Lee A D Cooper, Jeffery A Goldstein.
Lab Invest, 2021 Mar 07;. PMID: 33674784    Free PMC article.
Human-interpretable image features derived from densely mapped cancer pathology slides predict diverse molecular phenotypes.
James A Diao, Jason K Wang, +19 authors, Amaro Taylor-Weiner.
Nat Commun, 2021 Mar 14; 12(1). PMID: 33712588    Free PMC article.
Predicting gastric cancer outcome from resected lymph node histopathology images using deep learning.
Xiaodong Wang, Ying Chen, +15 authors, Guanzhen Yu.
Nat Commun, 2021 Mar 14; 12(1). PMID: 33712598    Free PMC article.
Clinical Potential of Kinase Inhibitors in Combination with Immune Checkpoint Inhibitors for the Treatment of Solid Tumors.
Ryuhjin Ahn, Josie Ursini-Siegel.
Int J Mol Sci, 2021 Apr 04; 22(5). PMID: 33807608    Free PMC article.
Review.
Artificial Intelligence in Cancer Research and Precision Medicine.
Bhavneet Bhinder, Coryandar Gilvary, Neel S Madhukar, Olivier Elemento.
Cancer Discov, 2021 Apr 04; 11(4). PMID: 33811123    Free PMC article.
Review.
A deep learning model for the classification of indeterminate lung carcinoma in biopsy whole slide images.
Fahdi Kanavati, Gouji Toyokawa, +6 authors, Masayuki Tsuneki.
Sci Rep, 2021 Apr 16; 11(1). PMID: 33854137    Free PMC article.
Computational Image Analysis Identifies Histopathological Image Features Associated With Somatic Mutations and Patient Survival in Gastric Adenocarcinoma.
Jun Cheng, Yuting Liu, +7 authors, Jie Zhang.
Front Oncol, 2021 Apr 20; 11. PMID: 33869007    Free PMC article.
A deep learning model to detect pancreatic ductal adenocarcinoma on endoscopic ultrasound-guided fine-needle biopsy.
Yoshiki Naito, Masayuki Tsuneki, +25 authors, Hirohisa Yano.
Sci Rep, 2021 Apr 21; 11(1). PMID: 33875703    Free PMC article.
RB1 and TP53 co-mutations correlate strongly with genomic biomarkers of response to immunity checkpoint inhibitors in urothelial bladder cancer.
Ramon Gonzalez Manzano, Ana Catalan-Latorre, Antonio Brugarolas.
BMC Cancer, 2021 Apr 22; 21(1). PMID: 33879103    Free PMC article.
Prognostic Modeling of Patients Undergoing Surgery Alone for Esophageal Squamous Cell Carcinoma: A Histopathological and Computed Tomography Based Quantitative Analysis.
Lei-Lei Wu, Jin-Long Wang, +11 authors, Guo-Wei Ma.
Front Oncol, 2021 Apr 30; 11. PMID: 33912439    Free PMC article.
Tumor microenvironment as a therapeutic target in cancer.
Yi Xiao, Dihua Yu.
Pharmacol Ther, 2020 Dec 02; 221. PMID: 33259885    Free PMC article.
Review.
ImmunoAIzer: A Deep Learning-Based Computational Framework to Characterize Cell Distribution and Gene Mutation in Tumor Microenvironment.
Chang Bian, Yu Wang, +5 authors, Jie Tian.
Cancers (Basel), 2021 May 01; 13(7). PMID: 33916145    Free PMC article.
Artificial Intelligence & Tissue Biomarkers: Advantages, Risks and Perspectives for Pathology.
Cesare Lancellotti, Pierandrea Cancian, +4 authors, Luca Di Tommaso.
Cells, 2021 May 01; 10(4). PMID: 33918173    Free PMC article.
Review.
Radiomic biomarkers of tumor immune biology and immunotherapy response.
Jarey H Wang, Kareem A Wahid, +3 authors, Clifton David Fuller.
Clin Transl Radiat Oncol, 2021 May 04; 28. PMID: 33937530    Free PMC article.
Review.
Immune response drives outcomes in prostate cancer: implications for immunotherapy.
Jialin Meng, Yujie Zhou, +7 authors, Chaozhao Liang.
Mol Oncol, 2020 Dec 19; 15(5). PMID: 33338321    Free PMC article.
College of American Pathologists Tumor Regression Grading System for Long-Term Outcome in Patients with Locally Advanced Rectal Cancer.
Hai-Yang Chen, Li-Li Feng, +24 authors, Xiang-Bo Wan.
Oncologist, 2021 Feb 06; 26(5). PMID: 33543577    Free PMC article.
Deep learning in histopathology: the path to the clinic.
Jeroen van der Laak, Geert Litjens, Francesco Ciompi.
Nat Med, 2021 May 16; 27(5). PMID: 33990804
Review.
Deep Learning Based on Standard H&E Images of Primary Melanoma Tumors Identifies Patients at Risk for Visceral Recurrence and Death.
Prathamesh M Kulkarni, Eric J Robinson, +19 authors, Yvonne M Saenger.
Clin Cancer Res, 2019 Oct 23; 26(5). PMID: 31636101    Free PMC article.
[Research Progress of Single Cell Sequencing in Lung Cancer].
Mengjun Yu, Jinjing Tan, Jinghui Wang.
Zhongguo Fei Ai Za Zhi, 2021 Apr 30; 24(4). PMID: 33910276    Free PMC article.
Single-cell transcriptomics reveals the effect of PD-L1/TGF-β blockade on the tumor microenvironment.
Yoong Wearn Lim, Garry L Coles, +3 authors, Erica L Stone.
BMC Biol, 2021 May 26; 19(1). PMID: 34030676    Free PMC article.
State of machine and deep learning in histopathological applications in digestive diseases.
Soma Kobayashi, Joel H Saltz, Vincent W Yang.
World J Gastroenterol, 2021 Jun 08; 27(20). PMID: 34092975    Free PMC article.
Review.
How can artificial intelligence models assist PD-L1 expression scoring in breast cancer: results of multi-institutional ring studies.
Xinran Wang, Liang Wang, +15 authors, Yueping Liu.
NPJ Breast Cancer, 2021 May 28; 7(1). PMID: 34039982    Free PMC article.
Machine learning analyses of antibody somatic mutations predict immunoglobulin light chain toxicity.
Maura Garofalo, Luca Piccoli, +12 authors, Andrea Cavalli.
Nat Commun, 2021 Jun 12; 12(1). PMID: 34112780