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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

Jahangir CA 1 , Page DB 2 , Broeckx G 3 , Gonzalez CA 1 , Burke C 1 , Murphy C 1 Show all authors , Reis-Filho JS 4 , Ly A 5 , Harms PW 6 , Gupta RR 7 , Vieth M 8 , Hida AI 9 , Kahila M 10 , Kos Z 11 , van Diest PJ 12 , Verbandt S 13 , Thagaard J 14 , Khiroya R 15 , Abduljabbar K 16 , Acosta Haab G 17 , Acs B 18 , Adams S 19 , Almeida JS 20 , Alvarado-Cabrero I 21 , Azmoudeh-Ardalan F 22 , Badve S 23 , Baharun NB 24 , Bellolio ER 25 , Bheemaraju V 26 , Blenman KR 27 , Botinelly Mendonça Fujimoto L 28 , Burgues O 29 , Chardas A 30 , Cheang MCU 31 , Ciompi F 32 , Cooper LA 33 , Coosemans A 34 , Corredor G 35 , Dantas Portela FL 36 , Deman F 3 , Demaria S 37 , Dudgeon SN 38 , Elghazawy M 39 , Fernandez-Martín C 40 , Fineberg S 41 , Fox SB 42 , Giltnane JM 43 , Gnjatic S 44 , Gonzalez-Ericsson PI 45 , Grigoriadis A 46 , Halama N 47 , Hanna MG 48 , Harbhajanka A 49 , Hart SN 50 , Hartman J 51 , Hewitt S 52 , Horlings HM 53 , Husain Z 54 , Irshad S 55 , Janssen EA 56 , Kataoka TR 57 , Kawaguchi K 58 , Khramtsov AI 59 , Kiraz U 56 , Kirtani P 60 , Kodach LL 61 , Korski K 62 , Akturk G 63 , Scott E 64 , Kovács A 65 , Laenkholm AV 66 , Lang-Schwarz C 8 , Larsimont D 67 , Lennerz JK 68 , Lerousseau M 69 , Li X 70 , Madabhushi A 71 , Maley SK 72 , Manur Narasimhamurthy V 73 , Marks DK 19 , McDonald ES 74 , Mehrotra R 75 , Michiels S 76 , Kharidehal D 77 , Minhas FUAA 78 , Mittal S 79 , Moore DA 80 , Mushtaq S 81 , Nighat H 82 , Papathomas T 83 , Penault-Llorca F 84 , Perera RD 85 , Pinard CJ 86 , Pinto-Cardenas JC 87 , Pruneri G 88 , Pusztai L 89 , Rajpoot NM 90 , Rapoport BL 91 , Rau TT 92 , Ribeiro JM 93 , Rimm D 94 , Vincent-Salomon A 95 , Saltz J 96 , Sayed S 97 , Hytopoulos E 97 , Mahon S 98 , Siziopikou KP 99 , Sotiriou C 100 , Stenzinger A 101 , Sughayer MA 102 , Sur D 103 , Symmans F 104 , Tanaka S 105 , Taxter T 106 , Tejpar S 13 , Teuwen J 107 , Thompson EA 108 , Tramm T 109 , Tran WT 110 , van der Laak J 31 , Verghese GE 46 , Viale G 111 , Wahab N 112 , Walter T 69 , Waumans Y 113 , Wen HY 48 , Yang W 114 , Yuan Y 115 , Bartlett J 116 , Loibl S 117 , Denkert C 118 , Savas P 119 , Loi S 119 , Specht Stovgaard E 120 , Salgado R 3 , Gallagher WM 1 , Rahman A 121

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 Department of Pathology and Laboratory Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA
  • 5 Department of Pathology, Massachusetts General Hospital, Boston, MA, USA
  • 6 Departments of Pathology and Dermatology, University of Michigan, Ann Arbor, MI, USA
  • 7 Department of Biomedical Informatics, Stony Brook University, Stony Brook, NY, USA
  • 8 Institute of Pathology, Klinikum Bayreuth GmbH, Friedrich-Alexander-University Erlangen-Nuremberg, Bayreuth, Germany
  • 9 Department of Pathology, Matsuyama Shimin Hospital, Matsuyama, Japan
  • 10 Department of Pathology, Yale School of Medicine, New Haven, CT, USA
  • 11 Department of Pathology and Laboratory Medicine, University of British Columbia, BC Cancer, Vancouver, British Columbia, Canada
  • 12 Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands
  • 13 Digestive Oncology, Department of Oncology, KU Leuven, Leuven, Belgium
  • 14 Technical University of Denmark, Kgs. Lyngby, Denmark
  • 15 Department of Cellular Pathology, University College Hospital, London, UK
  • 16 Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK
  • 17 Hospital Maria Curie, Buenos Aires, Argentina
  • 18 Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden
  • 19 Perlmutter Cancer Center, NYU Langone Health, New York, NY, USA
  • 20 Division of Cancer Epidemiology and Genetics (DCEG), National Cancer Institute (NCI), Rockville, MD, USA
  • 21 Oncology Hospital, Star Medica Centro, Juarez City, Mexico
  • 22 Tehran University of Medical Sciences, Tehran, Iran
  • 23 Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Emory University Winship Cancer Institute, Atlanta, GA, USA
  • 24 The National University of Malaysia, Kuala Lumpur, Malaysia
  • 25 Departamento de Anatomía Patológica, Facultad de Medicina, Universidad de La Frontera, Temuco, Chile
  • 26 Department of Pathology, Narayana Medical College, Nellore, India
  • 27 Department of Internal Medicine Section of Medical Oncology and Yale Cancer Center, Yale School of Medicine, New Haven, CT, USA
  • 28 Amazonas Federal University, Manaus, Brazil
  • 29 Pathology Department, Hospital Cliníco Universitario de Valencia/Incliva, Valencia, Spain
  • 30 Department of Pathobiology & Population Sciences, The Royal Veterinary College, London, UK
  • 31 Head of Integrative Genomics Analysis in Clinical Trials, ICR-CTSU, Division of Clinical Studies, The Institute of Cancer Research, London, UK
  • 32 Department of Pathology, Radboud University Medical Center, Nijmegen, The Netherlands
  • 33 Department of Pathology, Northwestern Feinberg School of Medicine, Chicago, IL, USA
  • 34 Department of Oncology, Laboratory of Tumor Immunology and Immunotherapy, KU Leuven, Leuven, Belgium
  • 35 Biomedical Engineering Department, Emory University, Atlanta, GA, USA
  • 36 Hospital Universitário Getúlio Vargas, Manaus, Brazil
  • 37 Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA
  • 38 Computational Biology and Bioinformatics, Yale University, New Haven, CT, USA
  • 39 University of Surrey, Guildford, UK
  • 40 Instituto Universitario de Investigación en Tecnología Centrada en el Ser Humano, HUMAN-tech, Universitat Politècnica de València, Valencia, Spain
  • 41 Montefiore Medical Center and the Albert Einstein College of Medicine, New York, NY, USA
  • 42 Pathology, Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, Victoria, Australia
  • 43 Genentech, San Francisco, CA, USA
  • 44 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
  • 45 Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
  • 46 Cancer Bioinformatics, Faculty of Life Sciences and Medicine, School of Cancer & Pharmaceutical Sciences, King's College London, London, UK
  • 47 Department of Translational Immunotherapy, German Cancer Research Center, Heidelberg, Germany
  • 48 Memorial Sloan Kettering Cancer Center, New York, NY, USA
  • 49 Case Western University, Cleveland, OH, USA
  • 50 Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA
  • 51 Department of Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden
  • 52 Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
  • 53 Division of Pathology, Netherlands Cancer Institute (NKI), Amsterdam, The Netherlands
  • 54 Praava Health, Dhaka, Bangladesh
  • 55 King's College London & Guys & St Thomas NHS Trust, London, UK
  • 56 Department of Pathology, Stavanger University Hospital, Stavanger, Norway
  • 57 Department of Pathology, Iwate Medical University, Morioka, Japan
  • 58 Department of Breast Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan
  • 59 Department of Pathology and Laboratory Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA
  • 60 Histopathology, Aakash Healthcare Super Speciality Hospital, New Delhi, India
  • 61 Department of Pathology, Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands
  • 62 Data, Analytics and Imaging, Product Development, F. Hoffmann-La Roche AG, Basel, Switzerland
  • 63 Translational Molecular Biomarkers, Merck & Co., Inc., Kenilworth, NJ, USA
  • 64 Translational Medicine, Bristol Myers Squibb, Princeton, NJ, USA
  • 65 Department of Clinical Pathology, Sahlgrenska University Hospital, Gothenburg, Sweden
  • 66 Department of Surgical Pathology, Zealand University Hospital, Roskilde, Denmark
  • 67 Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium
  • 68 Center for Integrated Diagnostics, Massachusetts General Hospital/Harvard Medical School, Boston, MA, USA
  • 69 Centre for Computational Biology (CBIO), Mines Paris, PSL University, Paris, France
  • 70 Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA
  • 71 Department of Biomedical Engineering, Radiology and Imaging Sciences, Biomedical Informatics, Pathology, Georgia Institute of Technology and Emory University, Atlanta, GA, USA
  • 72 NRG Oncology/NSABP Foundation, Pittsburgh, PA, USA
  • 73 Manipal Hospitals, Bangalore, India
  • 74 Breast Cancer Translational Research Group, University of Pennsylvania, Philadelphia, PA, USA
  • 75 Indian Cancer Genomic Atlas, Pune, India
  • 76 Office of Biostatistics and Epidemiology, Gustave Roussy, Oncostat U1018, Inserm, University Paris-Saclay, Ligue Contre le Cancer labeled Team, Villejuif, France
  • 77 Department of Pathology, Narayana Medical College and Hospital, Nellore, India
  • 78 Tissue Image Analytics Centre, Warwick Cancer Research Centre, PathLAKE Consortium, Department of Computer Science, University of Warwick, Coventry, UK
  • 79 Department of Chemical Engineering, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, Washington, USA
  • 80 CRUK Lung Cancer Centre of Excellence, UCL and Cellular Pathology Department, UCLH, London, UK
  • 81 Department of Biochemistry, Ziauddin University, Karachi, Pakistan
  • 82 Pathology and Laboratory Medicine, All India Institute of Medical Sciences, Raipur, India
  • 83 Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK
  • 84 Service de Pathologie et Biopathologie, Centre Jean PERRIN, INSERM U1240 Imagerie Moléculaire et Stratégies Théranostiques (IMoST), Université Clermont Auvergne, Clermont-Ferrand, France
  • 85 School of Electrical, Mechanical and Infrastructure Engineering, University of Melbourne, Melbourne, Victoria, Australia
  • 86 Radiogenomics Laboratory, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada
  • 87 Diagnostico de Salud Animal SA, Ciudad de México, Mexico
  • 88 Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
  • 89 Yale Cancer Center, Yale University, New Haven, CT, USA
  • 90 University of Warwick, Coventry, UK
  • 91 The Medical Oncology Centre of Rosebank, Johannesburg, South Africa
  • 92 Institute of Pathology, University Hospital Düsseldorf and Heinrich-Heine-University, Düsseldorf, Germany
  • 93 Breast Unit, Institute Gustave Roussy, Villejuif, France
  • 94 Department of Pathology, Yale University School of Medicine, New Haven, CT, USA
  • 95 Department of Diagnostic and Theranostic Medicine, Institut Curie, University Paris-Sciences et Lettres, Paris, France
  • 96 Department of Biomedical Informatics, Stony Brook Medicine, New York, NY, USA
  • 97 Department of Pathology, Aga Khan University, Nairobi, Kenya
  • 98 Mater Misericordiae University Hospital, Dublin, Ireland
  • 99 Department of Pathology, Section of Breast Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
  • 100 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
  • 101 Institute of Pathology, University Hospital Heidelberg, Centers for Personalized Medicine (ZPM), Heidelberg, Germany
  • 102 King Hussein Cancer Center, Amman, Jordan
  • 103 Department of Medical Oncology, University of Medicine and Pharmacy "Iuliu Hatieganu", Cluj-Napoca, Romania
  • 104 University of Texas MD Anderson Cancer Center, Houston, TX, USA
  • 105 Kyoto University, Kyoto, Japan
  • 106 Tempus Labs, Chicago, IL, USA
  • 107 AI for Oncology Lab, The Netherlands Cancer Institute, Amsterdam, The Netherlands
  • 108 Mayo Clinic, Jacksonville, FL, USA
  • 109 Department of Pathology, Institute of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark
  • 110 Department of Radiation Oncology, University of Toronto and Sunnybrook Health Sciences Centre, Toronto, Canada
  • 111 Department of Pathology, European Institute of Oncology & University of Milan, Milan, Italy
  • 112 Tissue Image Analytics Centre, Department of Computer Science, University of Warwick, Coventry, UK
  • 113 CellCarta NV, Antwerp, Belgium
  • 114 Fudan Medical University Shanghai Cancer Center, Shanghai, PR China
  • 115 Department of Translational Molecular Pathology, Division of Pathology and Laboratory Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
  • 116 University of Edinburgh, Edinburgh, UK
  • 117 Department of Medicine and Research, German Breast Group, Neu-Isenburg, Germany
  • 118 Institut für Pathologie, Philipps-Universität Marburg und Universitätsklinikum Marburg, Marburg, Germany
  • 119 Division of Cancer Research, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia
  • 120 Department of Pathology, Herlev and Gentofte Hospital, Herlev, Denmark
  • 121 UCD School of Medicine, UCD Conway Institute, University College Dublin, Dublin, Ireland
J Pathol, 2024 Mar;262(3):271-288.
PMID: 38230434 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.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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