Evidence map›Paper›PMID 37608771›Full record

ReviewThe Journal of pathology2023

Spatial analyses of immune cell infiltration in cancer: current methods and future directions: A report of the International Immuno-Oncology Biomarker Working Group on Breast Cancer.

David B Page, Glenn Broeckx, Chowdhury Arif Jahangir, Sara Verbandt, Rajarsi R Gupta, Jeppe Thagaard, Reena Khiroya, Zuzana Kos, Khalid Abduljabbar, Gabriela Acosta Haab and 124 more

Open access · bronzeAbstract readReview
In one paragraph

Review in The Journal of pathology, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 30 papers.

0numbers the graph read from it
0cells of the map it votes in
30citing papers in PubMed
9.4field-weighted citation impact, top 2% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

30 citing papers in PubMed, 45 citations in OpenAlex.

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  13. Advancements and future trends in machine learning for lung cancer: a comprehensive bibliometric analysis.Clinical & translational oncology : official publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico · 2025
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4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

134 authors at 20 institutions in 33 countries.

David B PageEarle A Chiles Research Institute, Providence Cancer Institute, Portland, OR, USA.ORCID 0000-0001-9264-4628
Glenn BroeckxDepartment of Pathology, GZA-ZNA Hospitals, Antwerp, Belgium.
Chowdhury Arif JahangirUCD School of Biomolecular and Biomedical Science, University College Dublin, Dublin, Ireland.ORCID 0000-0002-5389-7275
Sara VerbandtDigestive Oncology, Department of Oncology, KU Leuven, Leuven, Belgium.
Rajarsi R GuptaDepartment of Biomedical Informatics, Stony Brook University, Stony Brook, NY, USA.ORCID 0000-0002-1577-8718
Jeppe ThagaardTechnical University of Denmark, Kongens Lyngby, Denmark.
Reena KhiroyaDepartment of Cellular Pathology, University College Hospital, London, UK.
Zuzana KosDepartment of Pathology and Laboratory Medicine, BC Cancer Vancouver Centre, University of British Columbia, Vancouver, BC, Canada.
Khalid AbduljabbarCentre for Evolution and Cancer, The Institute of Cancer Research, London, UK.
Gabriela Acosta HaabHospital Maria Curie, Buenos Aires, Argentina.
Balazs AcsDepartment of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden.
Guray AkturkTranslational Molecular Biomarkers, Merck & Co Inc, Kenilworth, NJ, USA.
Jonas S AlmeidaNational Cancer Institute, Division of Cancer Epidemiology and Genetics (DCEG), Rockville, MD, USA.
Isabel Alvarado-CabreroOncology Hospital, Star Medica Centro, Mexico.
Farid Azmoudeh-ArdalanTehran University of Medical Sciences, Tehran, Iran.
Sunil BadvePathology and Laboratory Medicine, Emory University School of Medicine, Emory University Winship Cancer Institute, Atlanta, GA, USA.
Nurkhairul Bariyah BaharunThe National University of Malaysia, Kuala Lumpur, Malaysia.
Enrique R BellolioDepartamento de Anatomía Patológica, Facultad de Medicina, Universidad de La Frontera, Temuco, Chile.
Vydehi BheemarajuDepartment of Pathology, Narayana Medical College, Nellore, India.
Kim Rm BlenmanInternal Medicine Section of Medical Oncology and Yale Cancer Center, Yale School of Medicine, New Haven, CT, USA.
Luciana Botinelly Mendonça FujimotoAmazonas Federal University, Manaus, Brazil.
Najat BouchmaaInstitute of Biological Sciences, Faculty of Medical Sciences, Mohammed VI Polytechnic University (UM6P), Ben-Guerir, Morocco.
Octavio BurguesPathology Department, Hospital Cliníco Universitario de Valencia/Incliva, Valencia, Spain.
Maggie Chon U CheangHead of Integrative Genomics Analysis in Clinical Trials, ICR-CTSU, Division of Clinical Studies, Institute of Cancer Research, London, UK.
Francesco CiompiRadboud University Medical Center, Department of Pathology, Nijmegen, The Netherlands.
Lee Ad CooperDepartment of Pathology, Northwestern Feinberg School of Medicine, Chicago, IL, USA.
An CoosemansDepartment of Oncology, Laboratory of Tumor Immunology and Immunotherapy, KU Leuven, Leuven, Belgium.
Germán CorredorBiomedical Engineering Department, Emory University, Atlanta, GA, USA.
Flavio Luis Dantas PortelaHospital Universitário Getúlio Vargas, Manaus, Brazil.ORCID 0000-0003-0188-3709
Frederik DemanDepartment of Pathology, GZA-ZNA Hospitals, Antwerp, Belgium.
Sandra DemariaDepartment of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA.
Sarah N DudgeonConputational Biology and Bioinformatics, Yale University, New Haven, CT, USA.
Mahmoud ElghazawyUniversity of Surrey, Guildford, UK.ORCID 0000-0002-3100-7606
Scott ElyTranslational Pathology, Translational Sciences and Diagnostics/Translational Medicine/R&D, Bristol Myers Squibb, Princeton, NJ, USA.
Claudio Fernandez-MartínInstituto Universitario de Investigación en Tecnología Centrada en el Ser Humano, HUMAN-tech, Universitat Politècnica de València, Valencia, Spain.
Susan FinebergMontefiore Medical Center and the Albert Einstein College of Medicine, New York, NY, USA.
Stephen B FoxDepartment of Pathology, Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, VIC, Australia.
William M GallagherUCD School of Biomolecular and Biomedical Science, University College Dublin, Dublin, Ireland.
Jennifer M GiltnaneGenentech, South San Francisco, CA, USA.
Sacha GnjaticDepartment of Oncological Sciences, Medicine Hem/Onc, and Pathology, Tisch Cancer Institute - Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Paula I Gonzalez-EricssonDepartment of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.ORCID 0000-0002-6292-6963
Anita GrigoriadisCancer Bioinformatics, School of Cancer & Pharmaceutical Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.ORCID 0000-0003-3434-201X
Niels HalamaTranslational Immunotherapy, German Cancer Research Center, Heidelberg, Germany.
Matthew G HannaMemorial Sloan Kettering Cancer Center, New York, NY, USA.
Aparna HarbhajankaCase Western University, Cleveland, OH, USA.
Alexandros HardasPathobiology & Population Sciences, The Royal Veterinary College, London, UK.ORCID 0000-0001-9906-7552
Steven N HartLaboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.ORCID 0000-0001-7714-2734
Johan HartmanClinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.ORCID 0000-0002-6500-8527
Stephen HewittDepartment of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Akira I HidaDepartment of Pathology, Matsuyama Shimin Hospital, Matsuyama, Japan.
Hugo M HorlingsDivision of Pathology, Netherlands Cancer Institute (NKI), Amsterdam, The Netherlands.
Zaheed HusainPraava Health, Dhaka, Bangladesh.
Evangelos HytopoulosiRhythm Technologies Inc., San Francisco, CA, USA.
Sheeba IrshadKing's College London & Guy's & St Thomas' NHS Trust, London, UK.
Emiel Am JanssenDepartment of Pathology, Stavanger University Hospital, Stavanger, Norway.
Mohamed KahilaDepartment of Pathology, Yale University School of Medicine, New Haven, CT, USA.
Tatsuki R KataokaDepartment of Pathology, Iwate Medical University, Iwate, Japan.ORCID 0000-0003-3095-8976
Kosuke KawaguchiDepartment of Breast Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.
Durga KharidehalDepartment of Pathology, Narayana Medical College, Nellore, India.
Andrey I KhramtsovPathology and Laboratory Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA.
Umay KirazDepartment of Pathology, Stavanger University Hospital, Stavanger, Norway.
Pawan KirtaniDepartment of Histopathology, Aakash Healthcare Super Speciality Hospital, New Delhi, India.
Liudmila L KodachDepartment of Pathology, Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
Konstanty KorskiData, Analytics and Imaging, Product Development, F.Hoffmann-La Roche AG, Basel, Switzerland.
Anikó KovácsDepartment of Clinical Pathology, Sahlgrenska University Hospital, Gothenburg, Sweden.
Anne-Vibeke LaenkholmSurgical Pathology, Zealand University Hospital, Roskilde, Denmark.
Corinna Lang-SchwarzInstitute of Pathology, Klinikum Bayreuth GmbH, Friedrich-Alexander-University Erlangen-Nuremberg, Bayreuth, Germany.
Denis LarsimontInstitut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.
Jochen K LennerzCenter for Integrated Diagnostics, Massachusetts General Hospital/Harvard Medical School, Boston, MA, USA.
Marvin LerousseauCentre for Computational Biology (CBIO), Mines Paris, PSL University, Paris, France.
Xiaoxian LiPathology and Laboratory Medicine, Emory University, Atlanta, GA, USA.
Amy LyDepartment of Pathology, Massachusetts General Hospital, Boston, MA, USA.
Anant MadabhushiBiomedical Engineering, Radiology and Imaging Sciences, Biomedical Informatics, Pathology, Georgia Institute of Technology and Emory University, Atlanta, GA, USA.
Sai K MaleyNRG Oncology/NSABP Foundation, Pittsburgh, PA, USA.
Vidya Manur NarasimhamurthyManipal Hospitals, Bangalore, India.
Douglas K MarksPerlmutter Cancer Center, NYU Langone Health, New York, NY, USA.
Elizabeth S McDonaldBreast Cancer Translational Research Group, University of Pennsylvania, Philadelphia, PA, USA.
Ravi MehrotraIndian Cancer Genome Atlas, Pune, India.
Stefan MichielsOffice of Biostatistics and Epidemiology, Gustave Roussy, Oncostat U1018, Inserm, University Paris-Saclay, Ligue Contre le Cancer labeled Team, Villejuif, France.
Fayyaz Ul Amir Afsar MinhasTissue Image Analytics Centre, Warwick Cancer Research Centre, PathLAKE Consortium, Department of Computer Science, University of Warwick, Coventry, UK.
Shachi MittalDepartment of Chemical Engineering, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA, USA.
David A MooreCRUK Lung Cancer Centre of Excellence, UCLH, London, UK.
Shamim MushtaqDepartment of Biochemistry, Ziauddin University, Karachi, Pakistan.
Hussain NighatPathology and Laboratory Medicine, All India Institute of Medical Sciences, Raipur, India.
Thomas PapathomasInstitute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK.
Frederique Penault-LlorcaCentre Jean Perrin, INSERM U1240, Imagerie Moléculaire et Stratégies Théranostiques, Université Clermont Auvergne, Clermont-Ferrand, France.
Rashindrie D PereraSchool of Electrical, Mechanical and Infrastructure Engineering, University of Melbourne, Melbourne, VIC, Australia.
Christopher J PinardRadiogenomics Laboratory, Sunnybrook Health Sciences Centre, Toronto, ON, Canada.
Juan Carlos Pinto-CardenasDiagnostico de Salud Animal SA, Ciudad de México, Mexico.
Giancarlo PruneriDepartment of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
Lajos PusztaiYale Cancer Center, New Haven, CT, USA.
Arman RahmanUCD School of Biomolecular and Biomedical Science, University College Dublin, Dublin, Ireland.
Nasir Mahmood RajpootUniversity of Warwick, Warwick, UK.
Bernardo Leon RapoportThe Medical Oncology Centre of Rosebank, Johannesburg, South Africa.
Tilman T RauInstitute of Pathology, University Hospital Düsseldorf and Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany.ORCID 0000-0002-1251-950X
Jorge S Reis-FilhoPathology and Laboratory Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0003-2969-3173
Joana M RibeiroDépartement de Médecine Oncologique, Institute Gustave Roussy, Villejuif, France.
David RimmDepartment of Pathology, Yale University School of Medicine, New Haven, CT, USA.ORCID 0000-0001-5820-4397
Anne Vincent-SalomonDepartment of Diagnostic and Theranostic Medicine, Institut Curie, University Paris-Sciences et Lettres, Paris, France.
Manuel Salto-TellezIntegrated Pathology Unit, Institute of Cancer Research, London, UK.
Joel SaltzDepartment of Biomedical Informatics, Stony Brook Medicine, New York, NY, USA.
Shahin SayedDepartment of Pathology, Aga Khan University, Nairobi, Kenya.
Kalliopi P SiziopikouDepartment of Pathology, Section of Breast Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
Christos SotiriouBreast Cancer Translational Research Laboratory J.-C. Heuson, Institut Jules Bordet, Hôpital Universitaire de Bruxelles (HUB), Université Libre de Bruxelles (ULB), Brussels, Belgium.
Albrecht StenzingerInstitute of Pathology, University Hospital Heidelberg, Centers for Personalized Medicine (ZPM), Heidelberg, Germany.
Maher A SughayerKing Hussein Cancer Center, Amman, Jordan.
Daniel SurDepartment of Medical Oncology, University of Medicine and Pharmacy "Iuliu Hatieganu", Cluj-Napoca, Romania.
Fraser SymmansUniversity of Texas MD Anderson Cancer Center, Houston, TX, USA.
Sunao TanakaKyoto University, Kyoto, Japan.
Timothy TaxterTempus Labs, Chicago, IL, USA.
Sabine TejparDigestive Oncology, Department of Oncology, KU Leuven, Leuven, Belgium.
Jonas TeuwenAI for Oncology Lab, Netherlands Cancer Institute, Amsterdam, The Netherlands.
E Aubrey ThompsonMayo Clinic, Jacksonville, FL, USA.
Trine TrammPathology, and Institute of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark.
William T TranDepartment of Radiation Oncology, University of Toronto and Sunnybrook Health Sciences Centre, Toronto, ON, Canada.
Jeroen van der LaakDepartment of Pathology, Radboud University Medical Center, Nijmegen, The Netherlands.
Paul J van DiestDepartment of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands.
Gregory E VergheseCancer Bioinformatics, School of Cancer & Pharmaceutical Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.ORCID 0009-0006-7638-6431
Giuseppe VialeDepartment of Pathology, European Institute of Oncology & University of Milan, Milan, Italy.
Michael ViethInstitute of Pathology, Klinikum Bayreuth GmbH, Friedrich-Alexander-University Erlangen-Nuremberg, Bayreuth, Germany.
Noorul WahabTissue Image Analytics Centre, Department of Computer Science, University of Warwick, Coventry, UK.ORCID 0000-0002-1251-1559
Thomas WalterCentre for Computational Biology (CBIO), Mines Paris, PSL University, Paris, France.
Yannick WaumansCellCarta NV, Antwerp, Belgium.
Hannah Y WenMemorial Sloan Kettering Cancer Center, New York, NY, USA.
Wentao YangFudan Medical University Shanghai Cancer Center, Shanghai, PR China.
Yinyin YuanTranslational Molecular Pathology, Division of Pathology and Laboratory Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Sylvia AdamsPerlmutter Cancer Center, NYU Langone Health, New York, NY, USA.
John Mark Seaverns BartlettUniversity of Edinburgh, Edinburgh, UK.
Sibylle LoiblDepartment of Medicine and Research, German Breast Group, Neu-Isenburg, Germany.
Carsten DenkertInstitut für Pathologie, Philipps-Universität Marburg und Universitätsklinikum Marburg, Marburg, Germany.
Peter SavasDivision of Cancer Research, Peter MacCallum Cancer Centre, Melbourne, VIC, Australia.
Sherene LoiDivision of Cancer Research, Peter MacCallum Cancer Centre, Melbourne, VIC, Australia.
Roberto SalgadoDepartment of Pathology, GZA-ZNA Hospitals, Antwerp, Belgium.
Elisabeth Specht StovgaardDepartment of Pathology, Herlev and Gentofte Hospital, Herlev, Denmark.
Inserm · FRThe University of Melbourne · AUEmory University · USKing's College London · GBMemorial Sloan Kettering Cancer Center · USThe Netherlands Cancer Institute · NLUniversity College Dublin · IEUniversity of Warwick · GBYale University · USBayreuth Medical Center · DEInstitute of Cancer Research · GBKarolinska University Hospital · SEKU Leuven · BEKyoto University · JPNarayana Dental College and Hospital · INNorthwestern University · USNYU Langone Health · USRadboud University Nijmegen · NLStavanger University Hospital · NOSunnybrook Health Science Centre · CA

Funding

The Role of CHFR in Tumorigenesis and Paclitaxel-Sensitivity in Breast CancerP50CA116201 · NCI · MAYO CLINIC ROCHESTER · PI Fergus Joseph Couch · 2005 to 2026
$49.9M
THE TISCH CANCER INSTITUTE - CANCER CENTER SUPPORT GRANTP30CA196521 · NCI · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI Ramon E Parsons · 2015 to 2026
$35.4M
High-Dimensional Immune Monitoring of NCI-Supported Immunotherapy TrialsU24CA224319 · NCI · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI Sacha Gnjatic, Seunghee Kim-Schulze · 2017 to 2026
$21.5M
Targeting Polθ to Overcome PARP Inhibitor Resistance in Homologous Recombination Deficient Breast CancerP50CA247749 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI Simon N. Powell · 2020 to 2026
$16.3M
TCIA Sustainment and Scalability - Platforms for Quantitative Imaging Informatics in Precision MedicineU24CA215109 · NCI · UNIV OF ARKANSAS FOR MED SCIS · PI BANERJEE, IMON, PRIOR, FRED WILLIAM · 2017 to 2021
$8.5M
Pathology CoreU54CA254566 · NCI · CASE WESTERN RESERVE UNIVERSITY · PI MADABHUSHI, ANANT · 2020 to 2024
$5.0M
Computer-Assisted Histologic Evaluation of Cardiac Allograft RejectionR01HL151277 · NHLBI · UNIVERSITY OF PENNSYLVANIA · PI MADABHUSHI, ANANT, MARGULIES, KENNETH BER · 2020 to 2023
$3.2M
Oral Cavity Quantitative Histomorphometric Risk Classifier (OHbIC) in Oral Cavity Squamous Cell Carcinoma (OC-SCC)R01CA249992 · NCI · EMORY UNIVERSITY · PI LEWIS, JAMES, MADABHUSHI, ANANT · 2021 to 2025
$3.2M
Computerized histologic image predictor of cancer outcomeR01CA202752 · NCI · CASE WESTERN RESERVE UNIVERSITY · PI FELDMAN, MICHAEL D, GANESAN, SHRIDAR · 2016 to 2020
$3.1M
Prostate cancer risk stratification via computational 3D pathologyR01CA268207 · NCI · UNIVERSITY OF WASHINGTON · PI Jonathan T.C. Liu, Anant Madabhushi · 2022 to 2026
$3.1M
Quantitative Histomorphometric Risk Classifier (QuHbIC) in HPV + Oropharyngeal CarcinomaR01CA220581 · NCI · CASE WESTERN RESERVE UNIVERSITY · PI KOYFMAN, SHLOMO, LEWIS, JAMES · 2018 to 2023
$3.1M
Computerized Histologic Risk Predictor (CHiRP) for Early Stage Lung CancersR01CA216579 · NCI · EMORY UNIVERSITY · PI FU, PINGFU, LLOYD, MARK · 2018 to 2023
$3.1M
BLRD VA I01 BX004121Cancer Research UK C45982/A21808Cancer Research UK CRUK/07/012Cancer Research UK KCL-BCN-Q3NCI NIH HHS P30 CA196521NCI NIH HHS P50 CA116201NCI NIH HHS P50 CA247749NCI NIH HHS R01 CA202752NCI NIH HHS R01 CA208236NCI NIH HHS R01 CA216579NCI NIH HHS R01 CA220581NCI NIH HHS R01 CA249992NCI NIH HHS R01 CA257612NCI NIH HHS R01 CA268207NCI NIH HHS R01 CA268287NCI NIH HHS R33 CA263705NCI NIH HHS R37 CA225655NCI NIH HHS U01 CA239055NCI NIH HHS U01 CA248226NCI NIH HHS U01 CA269181NCI NIH HHS U24 CA215109NCI NIH HHS U24 CA224319NCI NIH HHS U54 CA254566NCI NIH HHS UH3 CA225021NHLBI NIH HHS R01 HL151277NHLBI NIH HHS R01 HL158071NIBIB NIH HHS R43 EB028736NIDDK NIH HHS U01 DK124165
6 · The paper itself

Abstract

Modern histologic imaging platforms coupled with machine learning methods have provided new opportunities to map the spatial distribution of immune cells in the tumor microenvironment. However, there exists no standardized method for describing or analyzing spatial immune cell data, and most reported spatial analyses are rudimentary. In this review, we provide an overview of two approaches for reporting and analyzing spatial data (raster versus vector-based). We then provide a compendium of spatial immune cell metrics that have been reported in the literature, summarizing prognostic associations in the context of a variety of cancers. We conclude by discussing two well-described clinical biomarkers, the breast cancer stromal tumor infiltrating lymphocytes score and the colon cancer Immunoscore, and describe investigative opportunities to improve clinical utility of these spatial biomarkers. © 2023 The Pathological Society of Great Britain and Ireland.

Indexed as

Colonic NeoplasmsBenchmarkingBiomarkersHumansLymphocytes, Tumor-InfiltratingSpatial AnalysisTumor MicroenvironmentBiomarkersImmunoscoremultispectral immunofluorescencespatial heterogeneityspatial statisticssTIL scoreTILtumor infiltrating lymphocytes

Identifiers

PMID37608771
PMCPMC11288334
OpenAlexW4386084933

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Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.