Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer

Chowdhury Arif Jahangir¹, David B Page², Glenn Broeckx^{3

4}, Claudia A Gonzalez¹, Caoimbhe Burke¹, Clodagh Murphy¹, Jorge S Reis-Filho⁵, Amy Ly⁶, Paul W Harms⁷, Rajarsi R Gupta⁸, Michael Vieth⁹, Akira I Hida¹⁰, Mohamed Kahila¹¹, Zuzana Kos¹², Paul J van Diest^{13

14}, Sara Verbandt¹⁵, Jeppe Thagaard^{16

17}, Reena Khiroya¹⁸, Khalid Abduljabbar¹⁹, Gabriela Acosta Haab²⁰, Balazs Acs^{21

22}, Sylvia Adams^{23

24}, Jonas S Almeida²⁵, Isabel Alvarado-Cabrero²⁶, Farid Azmoudeh-Ardalan²⁷, Sunil Badve²⁸, Nurkhairul Bariyah Baharun²⁹, Enrique R Bellolio³⁰, Vydehi Bheemaraju³¹, Kim Rm Blenman^{32

33}, Luciana Botinelly Mendonça Fujimoto³⁴, Octavio Burgues³⁵, Alexandros Chardas³⁶, Maggie Chon U Cheang³⁷, Francesco Ciompi³⁸, Lee Ad Cooper³⁹, An Coosemans⁴⁰, Germán Corredor⁴¹, Flavio Luis Dantas Portela⁴², Frederik Deman³, Sandra Demaria^{43

44}, Sarah N Dudgeon⁴⁵, Mahmoud Elghazawy^{46

47}, Claudio Fernandez-Martín⁴⁸, Susan Fineberg⁴⁹, Stephen B Fox⁵⁰, Jennifer M Giltnane⁵¹, Sacha Gnjatic⁵², Paula I Gonzalez-Ericsson⁵³, Anita Grigoriadis^{54

55}, Niels Halama⁵⁶, Matthew G Hanna⁵⁷, Aparna Harbhajanka⁵⁸, Steven N Hart⁵⁹, Johan Hartman^{22

60}, Stephen Hewitt⁶¹, Hugo M Horlings⁶², Zaheed Husain⁶³, Sheeba Irshad⁶⁴, Emiel Am Janssen^{65

66}, Tatsuki R Kataoka⁶⁷, Kosuke Kawaguchi⁶⁸, Andrey I Khramtsov⁶⁹, Umay Kiraz^{65

66}, Pawan Kirtani⁷⁰, Liudmila L Kodach⁷¹, Konstanty Korski⁷², Guray Akturk⁷³, Ely Scott⁷⁴, Anikó Kovács^{75

76}, Anne-Vibeke Laenkholm^{77

78}, Corinna Lang-Schwarz⁹, Denis Larsimont⁷⁹, Jochen K Lennerz⁸⁰, Marvin Lerousseau^{81

82

83}, Xiaoxian Li⁸⁴, Anant Madabhushi⁸⁵, Sai K Maley⁸⁶, Vidya Manur Narasimhamurthy⁸⁷, Douglas K Marks²³, Elizabeth S McDonald⁸⁸, Ravi Mehrotra^{89

90}, Stefan Michiels⁹¹, Durga Kharidehal⁹², Fayyaz Ul Amir Afsar Minhas⁹³, Shachi Mittal⁹⁴, David A Moore⁹⁵, Shamim Mushtaq⁹⁶, Hussain Nighat⁹⁷, Thomas Papathomas^{98

99}, Frederique Penault-Llorca¹⁰⁰, Rashindrie D Perera^{101

102}, Christopher J Pinard^{103

104

105

106}, Juan Carlos Pinto-Cardenas¹⁰⁷, Giancarlo Pruneri^{108

109}, Lajos Pusztai^{110

111}, Nasir Mahmood Rajpoot¹¹², Bernardo Leon Rapoport^{113

114}, Tilman T Rau¹¹⁵, Joana M Ribeiro¹¹⁶, David Rimm^{117

118}, Anne Vincent-Salomon¹¹⁹, Joel Saltz¹²⁰, Shahin Sayed¹²¹, Evangelos Hytopoulos^{121

122}, Sarah Mahon¹²³, Kalliopi P Siziopikou¹²⁴, Christos Sotiriou^{125

126}, Albrecht Stenzinger¹²⁷, Maher A Sughayer¹²⁸, Daniel Sur¹²⁹, Fraser Symmans¹³⁰, Sunao Tanaka¹³¹, Timothy Taxter¹³², Sabine Tejpar¹⁵, Jonas Teuwen¹³³, E Aubrey Thompson¹³⁴, Trine Tramm¹³⁵, William T Tran¹³⁶, Jeroen van der Laak³⁷, Gregory E Verghese^{54

55}, Giuseppe Viale¹³⁷, Noorul Wahab¹³⁸, Thomas Walter^{81

82

83}, Yannick Waumans¹³⁹, Hannah Y Wen⁵⁷, Wentao Yang¹⁴⁰, Yinyin Yuan¹⁴¹, John Bartlett¹⁴², Sibylle Loibl¹⁴³, Carsten Denkert¹⁴⁴, Peter Savas^{102

145}, Sherene Loi^{102

146}, Elisabeth Specht Stovgaard¹⁴⁷, Roberto Salgado^{3

102}, William M Gallagher¹, Arman Rahman¹⁴⁸

Affiliations

¹ UCD School of Biomolecular and Biomedical Science, UCD Conway Institute, University College Dublin, Dublin, Ireland.
² Earle A Chiles Research Institute, Providence Cancer Institute, Portland, OR, USA.
³ Department of Pathology PA2, GZA-ZNA Hospitals, Antwerp, Belgium.
⁴ Centre for Oncological Research (CORE), MIPPRO, Faculty of Medicine, Antwerp University, Antwerp, Belgium.
⁵ Department of Pathology and Laboratory Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
⁶ Department of Pathology, Massachusetts General Hospital, Boston, MA, USA.
⁷ Departments of Pathology and Dermatology, University of Michigan, Ann Arbor, MI, USA.
⁸ Department of Biomedical Informatics, Stony Brook University, Stony Brook, NY, USA.
⁹ Institute of Pathology, Klinikum Bayreuth GmbH, Friedrich-Alexander-University Erlangen-Nuremberg, Bayreuth, Germany.
¹⁰ Department of Pathology, Matsuyama Shimin Hospital, Matsuyama, Japan.
¹¹ Department of Pathology, Yale School of Medicine, New Haven, CT, USA.
¹² Department of Pathology and Laboratory Medicine, University of British Columbia, BC Cancer, Vancouver, British Columbia, Canada.
¹³ Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands.
¹⁴ Johns Hopkins Oncology Center, Baltimore, MD, USA.
¹⁵ Digestive Oncology, Department of Oncology, KU Leuven, Leuven, Belgium.
¹⁶ Technical University of Denmark, Kgs. Lyngby, Denmark.
¹⁷ Visiopharm A/S, Hørsholm, Denmark.
¹⁸ Department of Cellular Pathology, University College Hospital, London, UK.
¹⁹ Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK.
²⁰ Hospital Maria Curie, Buenos Aires, Argentina.
²¹ Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden.
²² Department of Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.
²³ Perlmutter Cancer Center, NYU Langone Health, New York, NY, USA.
²⁴ Department of Medicine, NYU Grossman School of Medicine, Manhattan, NY, USA.
²⁵ Division of Cancer Epidemiology and Genetics (DCEG), National Cancer Institute (NCI), Rockville, MD, USA.
²⁶ Oncology Hospital, Star Medica Centro, Juarez City, Mexico.
²⁷ Tehran University of Medical Sciences, Tehran, Iran.
²⁸ Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Emory University Winship Cancer Institute, Atlanta, GA, USA.
²⁹ The National University of Malaysia, Kuala Lumpur, Malaysia.
³⁰ Departamento de Anatomía Patológica, Facultad de Medicina, Universidad de La Frontera, Temuco, Chile.
³¹ Department of Pathology, Narayana Medical College, Nellore, India.
³² Department of Internal Medicine Section of Medical Oncology and Yale Cancer Center, Yale School of Medicine, New Haven, CT, USA.
³³ Department of Computer Science, Yale School of Engineering and Applied Science, New Haven, CT, USA.
³⁴ Amazonas Federal University, Manaus, Brazil.
³⁵ Pathology Department, Hospital Cliníco Universitario de Valencia/Incliva, Valencia, Spain.
³⁶ Department of Pathobiology & Population Sciences, The Royal Veterinary College, London, UK.
³⁷ Head of Integrative Genomics Analysis in Clinical Trials, ICR-CTSU, Division of Clinical Studies, The Institute of Cancer Research, London, UK.
³⁸ Department of Pathology, Radboud University Medical Center, Nijmegen, The Netherlands.
³⁹ Department of Pathology, Northwestern Feinberg School of Medicine, Chicago, IL, USA.
⁴⁰ Department of Oncology, Laboratory of Tumor Immunology and Immunotherapy, KU Leuven, Leuven, Belgium.
⁴¹ Biomedical Engineering Department, Emory University, Atlanta, GA, USA.
⁴² Hospital Universitário Getúlio Vargas, Manaus, Brazil.
⁴³ Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA.
⁴⁴ Department of Pathology, Weill Cornell Medicine, New York, NY, USA.
⁴⁵ Computational Biology and Bioinformatics, Yale University, New Haven, CT, USA.
⁴⁶ University of Surrey, Guildford, UK.
⁴⁷ Ain Shams University, Cairo, Egypt.
⁴⁸ Instituto Universitario de Investigación en Tecnología Centrada en el Ser Humano, HUMAN-tech, Universitat Politècnica de València, Valencia, Spain.
⁴⁹ Montefiore Medical Center and the Albert Einstein College of Medicine, New York, NY, USA.
⁵⁰ Pathology, Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, Victoria, Australia.
⁵¹ Genentech, San Francisco, CA, USA.
⁵² Department 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.
⁵³ Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
⁵⁴ Cancer Bioinformatics, Faculty of Life Sciences and Medicine, School of Cancer & Pharmaceutical Sciences, King's College London, London, UK.
⁵⁵ The Breast Cancer Now Research Unit, Faculty of Life Sciences and Medicine, School of Cancer and Pharmaceutical Sciences, King's College London, London, UK.
⁵⁶ Department of Translational Immunotherapy, German Cancer Research Center, Heidelberg, Germany.
⁵⁷ Memorial Sloan Kettering Cancer Center, New York, NY, USA.
⁵⁸ Case Western University, Cleveland, OH, USA.
⁵⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁶⁰ Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden.
⁶¹ Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
⁶² Division of Pathology, Netherlands Cancer Institute (NKI), Amsterdam, The Netherlands.
⁶³ Praava Health, Dhaka, Bangladesh.
⁶⁴ King's College London & Guys & St Thomas NHS Trust, London, UK.
⁶⁵ Department of Pathology, Stavanger University Hospital, Stavanger, Norway.
⁶⁶ Department of Chemistry, Bioscience and Environmental Technology, University of Stavanger, Stavanger, Norway.
⁶⁷ Department of Pathology, Iwate Medical University, Morioka, Japan.
⁶⁸ Department of Breast Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.
⁶⁹ Department of Pathology and Laboratory Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA.
⁷⁰ Histopathology, Aakash Healthcare Super Speciality Hospital, New Delhi, India.
⁷¹ Department of Pathology, Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
⁷² Data, Analytics and Imaging, Product Development, F. Hoffmann-La Roche AG, Basel, Switzerland.
⁷³ Translational Molecular Biomarkers, Merck & Co., Inc., Kenilworth, NJ, USA.
⁷⁴ Translational Medicine, Bristol Myers Squibb, Princeton, NJ, USA.
⁷⁵ Department of Clinical Pathology, Sahlgrenska University Hospital, Gothenburg, Sweden.
⁷⁶ Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
⁷⁷ Department of Surgical Pathology, Zealand University Hospital, Roskilde, Denmark.
⁷⁸ Department of Surgical Pathology, University of Copenhagen, Copenhagen, Denmark.
⁷⁹ Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.
⁸⁰ Center for Integrated Diagnostics, Massachusetts General Hospital/Harvard Medical School, Boston, MA, USA.
⁸¹ Centre for Computational Biology (CBIO), Mines Paris, PSL University, Paris, France.
⁸² Institut Curie, PSL University, Paris, France.
⁸³ INSERM U900, Paris, France.
⁸⁴ Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA.
⁸⁵ Department of Biomedical Engineering, Radiology and Imaging Sciences, Biomedical Informatics, Pathology, Georgia Institute of Technology and Emory University, Atlanta, GA, USA.
⁸⁶ NRG Oncology/NSABP Foundation, Pittsburgh, PA, USA.
⁸⁷ Manipal Hospitals, Bangalore, India.
⁸⁸ Breast Cancer Translational Research Group, University of Pennsylvania, Philadelphia, PA, USA.
⁸⁹ Indian Cancer Genomic Atlas, Pune, India.
⁹⁰ Centre for Health, Innovation and Policy Foundation, Noida, India.
⁹¹ Office of Biostatistics and Epidemiology, Gustave Roussy, Oncostat U1018, Inserm, University Paris-Saclay, Ligue Contre le Cancer labeled Team, Villejuif, France.
⁹² Department of Pathology, Narayana Medical College and Hospital, Nellore, India.
⁹³ Tissue Image Analytics Centre, Warwick Cancer Research Centre, PathLAKE Consortium, Department of Computer Science, University of Warwick, Coventry, UK.
⁹⁴ Department of Chemical Engineering, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, USA.
⁹⁵ CRUK Lung Cancer Centre of Excellence, UCL and Cellular Pathology Department, UCLH, London, UK.
⁹⁶ Department of Biochemistry, Ziauddin University, Karachi, Pakistan.
⁹⁷ Pathology and Laboratory Medicine, All India Institute of Medical Sciences, Raipur, India.
⁹⁸ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK.
⁹⁹ Department of Clinical Pathology, Drammen Sykehus, Vestre Viken HF, Drammen, Norway.
¹⁰⁰ Service de Pathologie et Biopathologie, Centre Jean PERRIN, INSERM U1240 Imagerie Moléculaire et Stratégies Théranostiques (IMoST), Université Clermont Auvergne, Clermont-Ferrand, France.
¹⁰¹ School of Electrical, Mechanical and Infrastructure Engineering, University of Melbourne, Melbourne, Victoria, Australia.
¹⁰² Division of Cancer Research, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
¹⁰³ Radiogenomics Laboratory, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada.
¹⁰⁴ Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada.
¹⁰⁵ Department of Oncology, Lakeshore Animal Health Partners, Mississauga, Ontario, Canada.
¹⁰⁶ Centre for Advancing Responsible and Ethical Artificial Intelligence (CARE-AI), University of Guelph, Guelph, Ontario, Canada.
¹⁰⁷ Diagnostico de Salud Animal SA, Ciudad de México, Mexico.
¹⁰⁸ Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
¹⁰⁹ Faculty of Medicine and Surgery, University of Milan, Milan, Italy.
¹¹⁰ Yale Cancer Center, Yale University, New Haven, CT, USA.
¹¹¹ Department of Medical Oncology, Yale School of Medicine, Yale University, New Haven, CT, USA.
¹¹² University of Warwick, Coventry, UK.
¹¹³ The Medical Oncology Centre of Rosebank, Johannesburg, South Africa.
¹¹⁴ Department of Immunology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa.
¹¹⁵ Institute of Pathology, University Hospital Düsseldorf and Heinrich-Heine-University, Düsseldorf, Germany.
¹¹⁶ Breast Unit, Institute Gustave Roussy, Villejuif, France.
¹¹⁷ Department of Pathology, Yale University School of Medicine, New Haven, CT, USA.
¹¹⁸ Department of Medicine, Yale University School of Medicine, New Haven, CT, USA.
¹¹⁹ Department of Diagnostic and Theranostic Medicine, Institut Curie, University Paris-Sciences et Lettres, Paris, France.
¹²⁰ Department of Biomedical Informatics, Stony Brook Medicine, New York, NY, USA.
¹²¹ Department of Pathology, Aga Khan University, Nairobi, Kenya.
¹²² iRhythm Technologies Inc., San Francisco, CA, USA.
¹²³ Mater Misericordiae University Hospital, Dublin, Ireland.
¹²⁴ Department of Pathology, Section of Breast Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
¹²⁵ Breast Cancer Translational Research Laboratory J.-C. Heuson, Institut Jules Bordet, Hôpital Universitaire de Bruxelles (H.U.B), Université Libre de Bruxelles (ULB), Brussels, Belgium.
¹²⁶ Medical Oncology Department, Institut Jules Bordet, Hôpital Universitaire de Bruxelles (H.U.B), Université Libre de Bruxelles (ULB), Brussels, Belgium.
¹²⁷ Institute of Pathology, University Hospital Heidelberg, Centers for Personalized Medicine (ZPM), Heidelberg, Germany.
¹²⁸ King Hussein Cancer Center, Amman, Jordan.
¹²⁹ Department of Medical Oncology, University of Medicine and Pharmacy "Iuliu Hatieganu", Cluj-Napoca, Romania.
¹³⁰ University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹³¹ Kyoto University, Kyoto, Japan.
¹³² Tempus Labs, Chicago, IL, USA.
¹³³ AI for Oncology Lab, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
¹³⁴ Mayo Clinic, Jacksonville, FL, USA.
¹³⁵ Department of Pathology, Institute of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark.
¹³⁶ Department of Radiation Oncology, University of Toronto and Sunnybrook Health Sciences Centre, Toronto, Canada.
¹³⁷ Department of Pathology, European Institute of Oncology & University of Milan, Milan, Italy.
¹³⁸ Tissue Image Analytics Centre, Department of Computer Science, University of Warwick, Coventry, UK.
¹³⁹ CellCarta NV, Antwerp, Belgium.
¹⁴⁰ Fudan Medical University Shanghai Cancer Center, Shanghai, PR China.
¹⁴¹ Department of Translational Molecular Pathology, Division of Pathology and Laboratory Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴² University of Edinburgh, Edinburgh, UK.
¹⁴³ Department of Medicine and Research, German Breast Group, Neu-Isenburg, Germany.
¹⁴⁴ Institut für Pathologie, Philipps-Universität Marburg und Universitätsklinikum Marburg, Marburg, Germany.
¹⁴⁵ The Sir Peter MacCallum Department of Medical Oncology, University of Melbourne, Melbourne, Victoria, Australia.
¹⁴⁶ Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁴⁷ Department of Pathology, Herlev and Gentofte Hospital, Herlev, Denmark.
¹⁴⁸ UCD School of Medicine, UCD Conway Institute, University College Dublin, Dublin, Ireland.

PMID: 38230434
PMCID: PMC11288342
DOI: 10.1002/path.6238

Review

Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer

Chowdhury Arif Jahangir et al. J Pathol. 2024 Mar.

. 2024 Mar;262(3):271-288.

doi: 10.1002/path.6238. Epub 2024 Jan 17.

Authors

Affiliations

¹ UCD School of Biomolecular and Biomedical Science, UCD Conway Institute, University College Dublin, Dublin, Ireland.
² Earle A Chiles Research Institute, Providence Cancer Institute, Portland, OR, USA.
³ Department of Pathology PA2, GZA-ZNA Hospitals, Antwerp, Belgium.
⁴ Centre for Oncological Research (CORE), MIPPRO, Faculty of Medicine, Antwerp University, Antwerp, Belgium.
⁵ Department of Pathology and Laboratory Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
⁶ Department of Pathology, Massachusetts General Hospital, Boston, MA, USA.
⁷ Departments of Pathology and Dermatology, University of Michigan, Ann Arbor, MI, USA.
⁸ Department of Biomedical Informatics, Stony Brook University, Stony Brook, NY, USA.
⁹ Institute of Pathology, Klinikum Bayreuth GmbH, Friedrich-Alexander-University Erlangen-Nuremberg, Bayreuth, Germany.
¹⁰ Department of Pathology, Matsuyama Shimin Hospital, Matsuyama, Japan.
¹¹ Department of Pathology, Yale School of Medicine, New Haven, CT, USA.
¹² Department of Pathology and Laboratory Medicine, University of British Columbia, BC Cancer, Vancouver, British Columbia, Canada.
¹³ Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands.
¹⁴ Johns Hopkins Oncology Center, Baltimore, MD, USA.
¹⁵ Digestive Oncology, Department of Oncology, KU Leuven, Leuven, Belgium.
¹⁶ Technical University of Denmark, Kgs. Lyngby, Denmark.
¹⁷ Visiopharm A/S, Hørsholm, Denmark.
¹⁸ Department of Cellular Pathology, University College Hospital, London, UK.
¹⁹ Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK.
²⁰ Hospital Maria Curie, Buenos Aires, Argentina.
²¹ Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden.
²² Department of Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.
²³ Perlmutter Cancer Center, NYU Langone Health, New York, NY, USA.
²⁴ Department of Medicine, NYU Grossman School of Medicine, Manhattan, NY, USA.
²⁵ Division of Cancer Epidemiology and Genetics (DCEG), National Cancer Institute (NCI), Rockville, MD, USA.
²⁶ Oncology Hospital, Star Medica Centro, Juarez City, Mexico.
²⁷ Tehran University of Medical Sciences, Tehran, Iran.
²⁸ Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Emory University Winship Cancer Institute, Atlanta, GA, USA.
²⁹ The National University of Malaysia, Kuala Lumpur, Malaysia.
³⁰ Departamento de Anatomía Patológica, Facultad de Medicina, Universidad de La Frontera, Temuco, Chile.
³¹ Department of Pathology, Narayana Medical College, Nellore, India.
³² Department of Internal Medicine Section of Medical Oncology and Yale Cancer Center, Yale School of Medicine, New Haven, CT, USA.
³³ Department of Computer Science, Yale School of Engineering and Applied Science, New Haven, CT, USA.
³⁴ Amazonas Federal University, Manaus, Brazil.
³⁵ Pathology Department, Hospital Cliníco Universitario de Valencia/Incliva, Valencia, Spain.
³⁶ Department of Pathobiology & Population Sciences, The Royal Veterinary College, London, UK.
³⁷ Head of Integrative Genomics Analysis in Clinical Trials, ICR-CTSU, Division of Clinical Studies, The Institute of Cancer Research, London, UK.
³⁸ Department of Pathology, Radboud University Medical Center, Nijmegen, The Netherlands.
³⁹ Department of Pathology, Northwestern Feinberg School of Medicine, Chicago, IL, USA.
⁴⁰ Department of Oncology, Laboratory of Tumor Immunology and Immunotherapy, KU Leuven, Leuven, Belgium.
⁴¹ Biomedical Engineering Department, Emory University, Atlanta, GA, USA.
⁴² Hospital Universitário Getúlio Vargas, Manaus, Brazil.
⁴³ Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA.
⁴⁴ Department of Pathology, Weill Cornell Medicine, New York, NY, USA.
⁴⁵ Computational Biology and Bioinformatics, Yale University, New Haven, CT, USA.
⁴⁶ University of Surrey, Guildford, UK.
⁴⁷ Ain Shams University, Cairo, Egypt.
⁴⁸ Instituto Universitario de Investigación en Tecnología Centrada en el Ser Humano, HUMAN-tech, Universitat Politècnica de València, Valencia, Spain.
⁴⁹ Montefiore Medical Center and the Albert Einstein College of Medicine, New York, NY, USA.
⁵⁰ Pathology, Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, Victoria, Australia.
⁵¹ Genentech, San Francisco, CA, USA.
⁵² Department 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.
⁵³ Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
⁵⁴ Cancer Bioinformatics, Faculty of Life Sciences and Medicine, School of Cancer & Pharmaceutical Sciences, King's College London, London, UK.
⁵⁵ The Breast Cancer Now Research Unit, Faculty of Life Sciences and Medicine, School of Cancer and Pharmaceutical Sciences, King's College London, London, UK.
⁵⁶ Department of Translational Immunotherapy, German Cancer Research Center, Heidelberg, Germany.
⁵⁷ Memorial Sloan Kettering Cancer Center, New York, NY, USA.
⁵⁸ Case Western University, Cleveland, OH, USA.
⁵⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁶⁰ Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden.
⁶¹ Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
⁶² Division of Pathology, Netherlands Cancer Institute (NKI), Amsterdam, The Netherlands.
⁶³ Praava Health, Dhaka, Bangladesh.
⁶⁴ King's College London & Guys & St Thomas NHS Trust, London, UK.
⁶⁵ Department of Pathology, Stavanger University Hospital, Stavanger, Norway.
⁶⁶ Department of Chemistry, Bioscience and Environmental Technology, University of Stavanger, Stavanger, Norway.
⁶⁷ Department of Pathology, Iwate Medical University, Morioka, Japan.
⁶⁸ Department of Breast Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.
⁶⁹ Department of Pathology and Laboratory Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA.
⁷⁰ Histopathology, Aakash Healthcare Super Speciality Hospital, New Delhi, India.
⁷¹ Department of Pathology, Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
⁷² Data, Analytics and Imaging, Product Development, F. Hoffmann-La Roche AG, Basel, Switzerland.
⁷³ Translational Molecular Biomarkers, Merck & Co., Inc., Kenilworth, NJ, USA.
⁷⁴ Translational Medicine, Bristol Myers Squibb, Princeton, NJ, USA.
⁷⁵ Department of Clinical Pathology, Sahlgrenska University Hospital, Gothenburg, Sweden.
⁷⁶ Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
⁷⁷ Department of Surgical Pathology, Zealand University Hospital, Roskilde, Denmark.
⁷⁸ Department of Surgical Pathology, University of Copenhagen, Copenhagen, Denmark.
⁷⁹ Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.
⁸⁰ Center for Integrated Diagnostics, Massachusetts General Hospital/Harvard Medical School, Boston, MA, USA.
⁸¹ Centre for Computational Biology (CBIO), Mines Paris, PSL University, Paris, France.
⁸² Institut Curie, PSL University, Paris, France.
⁸³ INSERM U900, Paris, France.
⁸⁴ Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA.
⁸⁵ Department of Biomedical Engineering, Radiology and Imaging Sciences, Biomedical Informatics, Pathology, Georgia Institute of Technology and Emory University, Atlanta, GA, USA.
⁸⁶ NRG Oncology/NSABP Foundation, Pittsburgh, PA, USA.
⁸⁷ Manipal Hospitals, Bangalore, India.
⁸⁸ Breast Cancer Translational Research Group, University of Pennsylvania, Philadelphia, PA, USA.
⁸⁹ Indian Cancer Genomic Atlas, Pune, India.
⁹⁰ Centre for Health, Innovation and Policy Foundation, Noida, India.
⁹¹ Office of Biostatistics and Epidemiology, Gustave Roussy, Oncostat U1018, Inserm, University Paris-Saclay, Ligue Contre le Cancer labeled Team, Villejuif, France.
⁹² Department of Pathology, Narayana Medical College and Hospital, Nellore, India.
⁹³ Tissue Image Analytics Centre, Warwick Cancer Research Centre, PathLAKE Consortium, Department of Computer Science, University of Warwick, Coventry, UK.
⁹⁴ Department of Chemical Engineering, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, USA.
⁹⁵ CRUK Lung Cancer Centre of Excellence, UCL and Cellular Pathology Department, UCLH, London, UK.
⁹⁶ Department of Biochemistry, Ziauddin University, Karachi, Pakistan.
⁹⁷ Pathology and Laboratory Medicine, All India Institute of Medical Sciences, Raipur, India.
⁹⁸ Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK.
⁹⁹ Department of Clinical Pathology, Drammen Sykehus, Vestre Viken HF, Drammen, Norway.
¹⁰⁰ Service de Pathologie et Biopathologie, Centre Jean PERRIN, INSERM U1240 Imagerie Moléculaire et Stratégies Théranostiques (IMoST), Université Clermont Auvergne, Clermont-Ferrand, France.
¹⁰¹ School of Electrical, Mechanical and Infrastructure Engineering, University of Melbourne, Melbourne, Victoria, Australia.
¹⁰² Division of Cancer Research, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
¹⁰³ Radiogenomics Laboratory, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada.
¹⁰⁴ Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada.
¹⁰⁵ Department of Oncology, Lakeshore Animal Health Partners, Mississauga, Ontario, Canada.
¹⁰⁶ Centre for Advancing Responsible and Ethical Artificial Intelligence (CARE-AI), University of Guelph, Guelph, Ontario, Canada.
¹⁰⁷ Diagnostico de Salud Animal SA, Ciudad de México, Mexico.
¹⁰⁸ Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
¹⁰⁹ Faculty of Medicine and Surgery, University of Milan, Milan, Italy.
¹¹⁰ Yale Cancer Center, Yale University, New Haven, CT, USA.
¹¹¹ Department of Medical Oncology, Yale School of Medicine, Yale University, New Haven, CT, USA.
¹¹² University of Warwick, Coventry, UK.
¹¹³ The Medical Oncology Centre of Rosebank, Johannesburg, South Africa.
¹¹⁴ Department of Immunology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa.
¹¹⁵ Institute of Pathology, University Hospital Düsseldorf and Heinrich-Heine-University, Düsseldorf, Germany.
¹¹⁶ Breast Unit, Institute Gustave Roussy, Villejuif, France.
¹¹⁷ Department of Pathology, Yale University School of Medicine, New Haven, CT, USA.
¹¹⁸ Department of Medicine, Yale University School of Medicine, New Haven, CT, USA.
¹¹⁹ Department of Diagnostic and Theranostic Medicine, Institut Curie, University Paris-Sciences et Lettres, Paris, France.
¹²⁰ Department of Biomedical Informatics, Stony Brook Medicine, New York, NY, USA.
¹²¹ Department of Pathology, Aga Khan University, Nairobi, Kenya.
¹²² iRhythm Technologies Inc., San Francisco, CA, USA.
¹²³ Mater Misericordiae University Hospital, Dublin, Ireland.
¹²⁴ Department of Pathology, Section of Breast Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
¹²⁵ Breast Cancer Translational Research Laboratory J.-C. Heuson, Institut Jules Bordet, Hôpital Universitaire de Bruxelles (H.U.B), Université Libre de Bruxelles (ULB), Brussels, Belgium.
¹²⁶ Medical Oncology Department, Institut Jules Bordet, Hôpital Universitaire de Bruxelles (H.U.B), Université Libre de Bruxelles (ULB), Brussels, Belgium.
¹²⁷ Institute of Pathology, University Hospital Heidelberg, Centers for Personalized Medicine (ZPM), Heidelberg, Germany.
¹²⁸ King Hussein Cancer Center, Amman, Jordan.
¹²⁹ Department of Medical Oncology, University of Medicine and Pharmacy "Iuliu Hatieganu", Cluj-Napoca, Romania.
¹³⁰ University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹³¹ Kyoto University, Kyoto, Japan.
¹³² Tempus Labs, Chicago, IL, USA.
¹³³ AI for Oncology Lab, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
¹³⁴ Mayo Clinic, Jacksonville, FL, USA.
¹³⁵ Department of Pathology, Institute of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark.
¹³⁶ Department of Radiation Oncology, University of Toronto and Sunnybrook Health Sciences Centre, Toronto, Canada.
¹³⁷ Department of Pathology, European Institute of Oncology & University of Milan, Milan, Italy.
¹³⁸ Tissue Image Analytics Centre, Department of Computer Science, University of Warwick, Coventry, UK.
¹³⁹ CellCarta NV, Antwerp, Belgium.
¹⁴⁰ Fudan Medical University Shanghai Cancer Center, Shanghai, PR China.
¹⁴¹ Department of Translational Molecular Pathology, Division of Pathology and Laboratory Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴² University of Edinburgh, Edinburgh, UK.
¹⁴³ Department of Medicine and Research, German Breast Group, Neu-Isenburg, Germany.
¹⁴⁴ Institut für Pathologie, Philipps-Universität Marburg und Universitätsklinikum Marburg, Marburg, Germany.
¹⁴⁵ The Sir Peter MacCallum Department of Medical Oncology, University of Melbourne, Melbourne, Victoria, Australia.
¹⁴⁶ Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁴⁷ Department of Pathology, Herlev and Gentofte Hospital, Herlev, Denmark.
¹⁴⁸ UCD School of Medicine, UCD Conway Institute, University College Dublin, Dublin, Ireland.

PMID: 38230434
PMCID: PMC11288342
DOI: 10.1002/path.6238

Abstract

Recent advances in the field of immuno-oncology have brought transformative changes in the management of cancer patients. The immune profile of tumours has been found to have key value in predicting disease prognosis and treatment response in various cancers. Multiplex immunohistochemistry and immunofluorescence have emerged as potent tools for the simultaneous detection of multiple protein biomarkers in a single tissue section, thereby expanding opportunities for molecular and immune profiling while preserving tissue samples. By establishing the phenotype of individual tumour cells when distributed within a mixed cell population, the identification of clinically relevant biomarkers with high-throughput multiplex immunophenotyping of tumour samples has great potential to guide appropriate treatment choices. Moreover, the emergence of novel multi-marker imaging approaches can now provide unprecedented insights into the tumour microenvironment, including the potential interplay between various cell types. However, there are significant challenges to widespread integration of these technologies in daily research and clinical practice. This review addresses the challenges and potential solutions within a structured framework of action from a regulatory and clinical trial perspective. New developments within the field of immunophenotyping using multiplexed tissue imaging platforms and associated digital pathology are also described, with a specific focus on translational implications across different subtypes of cancer. © 2024 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.

Keywords: cancer prognosis; clinical integration; digital image analysis; multiplex imaging; multiplex immunofluorescence; multiplex immunohistochemistry; therapy response; tumour immune profiling; tumour infiltrating lymphocytes.

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Conflict of interest statement

DBP: Speaker’s Bureau: Genentech, Novartis, Clinical Care Options, Oncocyte; research support: WindMIL, Brooklyn Immunotherapeutics, Merck, Bristol Myers Squibb, IMV; consulting: Merck, Biotheranostics, Puma, Gilead, Lilly, Sanofi, NGM Bio, Sanford Burnham Prebys, AstraZeneca. GB: Speaker’s fee from MSD and Novartis, advisory boards for Roche and MSD, consultant for MSD, Novartis, and Roche, travel and conference support from Roche, MSD, and Gilead. JSR-F is an Associate Editor of The Journal of Pathology and has received personal/consultancy fees from Goldman Sachs, Bain Capital, REPARE Therapeutics, Saga Diagnostics, and PaigeAl, membership of the scientific advisory boards of VolitionRx, REPARE Therapeutics, and Paige. Al, membership of the Board of Directors of Grupo Oncoclinicas, and ad hoc membership of the scientific advisory boards of AstraZeneca, Merck Daiichi Sankyo, Roche Tissue Diagnostics, and Personalis, outside the scope of this study. AIH: Research fund from Visiopharm A/S. ZK: Paid advisory role for Eli Lilly and AstraZeneca Canada. JT: Employee of Visiopharm A/S. KRMB: Scientific Advisory Board for CDI Labs, research funding form Carevive. FC: Chair of the Scientific and Medical Advisory Board of TRIBVN Healthcare, France, and advisory board fees from TRIBVN Healthcare, France in the last 5 years. Shareholder of Aiosyn BV, the Netherlands. LADC: Participation in the Tempus Algorithm Advisors program. AC: Contracted researcher for Oncoinvent AS and Novocure and a consultant for Sotio a.s. and Epics Therapeutics SA. ME: Egyptian missions sector. SBF: Expert advisory panel for AXDEV Group. JMG: Employee and stockholder of Roche/Genentech. SG: Research funding from Regeneron Pharmaceuticals, Boehringer Ingelheim, Bristol Myers Squibb, Celgene, Genentech, EMD Serono, Pfizer, and Takeda, unrelated to the current work; named co-inventor on an issued patent for multiplex immunohistochemistry to characterise tumours and treatment responses. The technology is filed through Icahn School of Medicine at Mount Sinai (ISMMS) and is currently unlicensed. NH: Patent on a technology to measure immune infiltration in cancer to predict treatment outcome (W02012038068A2). MGH: Consultant for PaigeAl, VolastraTx, and advisor for PathPresenter. JH: Speaker’s honoraria or advisory board remunerations from Roche, Novartis, AstraZeneca, Eli Lilly, and MSD. Co-founder and shareholder of Stratipath AB. KK Employee and stockholder of Roche. GA: Employee of Merck & Co Inc. AIK: Honorarium from Roche, MSD, and Pfizer, member of the Advisory Board of Pfizer. A-VL Institutional grants from AstraZeneca and personal grants from AstraZeneca (travel and honorarium from advisory board), MSD (honorarium from advisory board), and Daiichi Sankyo (travel). XL: Eli Lilly Company, Advisor, Cancer Expert Now, Advisor, Champions Oncology, Research fund. AM: Equity holder in Picture Health, Elucid Bioimaging and Inspirata Inc, advisory board of Picture Health, Aiforia Inc and SimBioSys, consultant for SimBioSys, sponsored research agreements with AstraZeneca, Boehringer-lngelheim, Eli-Lilly, and Bristol Myers Squibb, technology licensed to Picture Health and Elucid Bioimaging involvement in three different R01 grants with Inspirata Inc DKM: Consulting: Astrazeneca, Lilly USA LLC Hologic. Sponsored Research: Merck Agendia. SM: Scientific Committee Study member. Roche, data and safety monitoring member of clinical trials: Sensorion, Biophytis, Servier, IQVIA, Yuhan, Kedrion. FuAAM: Research studentship funding from GSK DAM: Speaker fees from AstraZeneca, Eli Lilly, and Takeda, consultancy fees from AstraZeneca, Thermo Fisher, Takeda, Amgen, Janssen, M/M Software, Bristol Myers Squibb, and Eli Lilly, educational support from Takeda and Amgen. FP-L: Personal financial interests: AbbVie, Agendia, Amgen, Astellas, AstraZeneca, Bayer, BMS, Daiichi-Sankyo, Eisai, Exact Science, GSK lllumina, Incyte, Janssen, Lilly, MERCK lifa, Merck-MSD, Myriad, Novartis, Pfizer, Pierre-Fabre, Roche, Sanofi, Seagen, Takeda, Veracyte, Servier. Institutional financial interests: AstraZeneca, Bayer, BMS, MSD, Myriad, Roche, Veracyte. Congress invitations: AbbVie, Amgen, AstraZeneca, Bayer, BMS, Gilead, MSD, Novartis, Roche, Lilly, Pfizer. NMR: Co-Founder, Director and CSO of Histofy Ltd, UK AS: Advisory Board/Speaker’s Bureau: Aignostics, AstraZeneca, Bayer, BMS, Eli Lilly, lllumina, Incyte, Janssen, MSD, Novartis, Pfizer, Roche, Seagen, Takeda, and Thermo Fisher; grants from Bayer, Bristol Meyers Squibb, Chugai, and Incyte. TT: Employee of Tempus Labs. JT: Shareholder of EllogonAI BV. TT: Speaker’s fee from Pfizer. JvdL: Member of the advisory boards of Philips, the Netherlands and ContextVision, Sweden, research funding from Philips, the Netherlands, ContextVision, Sweden, and Sectra, Sweden in the last 5 years. Chief scientific officer and shareholder of Aiosyn BV, the Netherlands. TW: Collaboration with TRIBUN Health on automatic grading of biopsies for head and neck cancer, patent on the prediction of homologous recombination deficiency in breast cancer. YW: Employee of CellCarta. HYW: Advisory faculty of AstraZeneca. YY: Speaker/consultant for Roche and Merck PS: Consultant (uncompensated) to Roche-Genentech. SL Research funding to institution from Novartis, Bristol Meyers Squibb, Merck Puma Biotechnology, Eli Lilly, Nektar Therapeutics, AstraZeneca, Roche-Genentech, and Seattle Genetics. Consultant (not compensated) to Seattle Genetics, Novartis, Bristol Meyers Squibb, Merck, AstraZeneca, Eli Lilly, Pfizer, and Roche-Genentech. Consultant (paid to her institution) to Aduro Biotech, Novartis, GlaxoSmithKline, Roche-Genentech, AstraZeneca, Silverback Therapeutics, GI Therapeutics, PUMA Biotechnologies, Pfizer, Gilead Therapeutics, Seattle Genetics, Daiichi-Sankyo, Amunix, Tallac therapeutics, Eli Lilly, and Bristol Meyers Squibb. RS: Non-financial support from Merck and Bristol Myers Squibb, research support from Merck Puma Biotechnology and Roche; personal fees from Roche, Bristol Myers Squibb and Exact Sciences for advisory boards. WMG: Co-founder, shareholder and part-time Chief Scientific Officer of OncoAssure Limited, shareholder in Deciphex and member of the Scientific Advisory Board of Carrick Therapeutics.

Figures

**Figure 1.**
mIF staining of a panel of five immune markers plus one epithelial marker. (A and B) A breast cancer TMA core showing composite staining of each of the six markers in the mIF panel (CD4, CD8, F0XP3, CD68, CD68, and PanCK) together with DAPI. (C–H) Individual images of CD4 (green), CD8 (yellow), F0XP3 (orange), CD68 (red), CD20 (white), and PanCK (purple) with DAPI counterstain.

**Figure 2.**
Comparison of experimental design between conventional chromogenic IHC and mIF. (A) In conventional chromogenic IHC, each marker requires a separate slide. Although multiplexing with chromogenic IHC is possible, it is severely restricted in terms of the number of markers that can be simultaneously stained. (B) With mIF, one section is enough to examine multiple markers. The figure was partly created using BioRender.com.

**Figure 3.**
TIL profiling with H&E versus conventional chromogenic IHC versus mIF. (A) H&E staining enables the measurement of total TILs in tissue, whereas, with conventional IHC, a specific immune population can be profiled based on a single protein marker. (B) mIF staining allows the total TIL population to be subtyped based on multiple markers. It is also possible to further characterise cells based on marker colocalisation. With an epithelial or tumour differentiation marker, it is possible to automate tumour-stroma segmentation with image analysis software. Furthermore, multiplex images can be used to map spatial distributions of different cell phenotypes and examine their proximal associations, and further identify distinct cellular neighbourhoods. Created with BioRender.com.

**Figure 4.**
DIA workflow for mIF. (A) First, raw images are generated by scanning stained tissue slides. (B) Spectral unmixing and autofluorescence removal are performed with the software to extract the true signals from each marker. (C) A tissue segmentation algorithm is run to segment tumour and stromal areas. (D) Cell segmentation followed by cell phenotyping is performed to classify all cells based on the marker panel used. (E) Finally, spatial mapping of all cell classes is carried out for further proximity analysis. The images were generated using inForm^® image analysis software, Akoya Bioscience.

See this image and copyright information in PMC

References

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Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer

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Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer

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