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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 Publisher Pubmed



Jahangir CA1 ; Page DB2 ; Broeckx G3, 4 ; Gonzalez CA1 ; Burke C1 ; Murphy C1 ; Reisfilho JS5 ; Ly A6 ; Harms PW7 ; Gupta RR8 ; Vieth M9 ; Hida AI10 ; Kahila M11 ; Kos Z12 Show All Authors
Authors
  1. Jahangir CA1
  2. Page DB2
  3. Broeckx G3, 4
  4. Gonzalez CA1
  5. Burke C1
  6. Murphy C1
  7. Reisfilho JS5
  8. Ly A6
  9. Harms PW7
  10. Gupta RR8
  11. Vieth M9
  12. Hida AI10
  13. Kahila M11
  14. Kos Z12
  15. Van Diest PJ13, 14
  16. Verbandt S15
  17. Thagaard J16, 17
  18. Khiroya R18
  19. Abduljabbar K19
  20. Acosta Haab G20
  21. Acs B21, 22
  22. Adams S23, 24
  23. Almeida JS25
  24. Alvaradocabrero I26
  25. Azmoudehardalan F27
  26. Badve S28
  27. Baharun NB29
  28. Bellolio ER30
  29. Bheemaraju V31
  30. Blenman KRM32, 33
  31. Botinelly Mendonca Fujimoto L34
  32. Burgues O35
  33. Chardas A36
  34. Cheang MCU37
  35. Ciompi F38
  36. Cooper LAD39
  37. Coosemans A40
  38. Corredor G41
  39. Dantas Portela FL42
  40. Deman F3
  41. Demaria S43, 44
  42. Dudgeon SN45
  43. Elghazawy M46, 47
  44. Fernandezmartin C48
  45. Fineberg S49
  46. Fox SB50
  47. Giltnane JM51
  48. Gnjatic S52
  49. Gonzalezericsson PI53
  50. Grigoriadis A54, 55
  51. Halama N56
  52. Hanna MG57
  53. Harbhajanka A58
  54. Hart SN59
  55. Hartman J22, 60
  56. Hewitt S61
  57. Horlings HM62
  58. Husain Z63
  59. Irshad S64
  60. Janssen EAM65, 66
  61. Kataoka TR67
  62. Kawaguchi K68
  63. Khramtsov AI69
  64. Kiraz U65, 66
  65. Kirtani P70
  66. Kodach LL71
  67. Korski K72
  68. Akturk G73
  69. Scott E74
  70. Kovacs A75, 76
  71. Laenkholm AV77, 78
  72. Langschwarz C9
  73. Larsimont D79
  74. Lennerz JK80
  75. Lerousseau M81, 82, 83
  76. Li X84
  77. Madabhushi A85
  78. Maley SK86
  79. Manur Narasimhamurthy V87
  80. Marks DK23
  81. Mcdonald ES88
  82. Mehrotra R89, 90
  83. Michiels S91
  84. Kharidehal D92
  85. Minhas FUAA93
  86. Mittal S94
  87. Moore DA95
  88. Mushtaq S96
  89. Nighat H97
  90. Papathomas T98, 99
  91. Penaultllorca F100
  92. Perera RD101, 102
  93. Pinard CJ103, 104, 105, 106
  94. Pintocardenas JC107
  95. Pruneri G108, 109
  96. Pusztai L110, 111
  97. Rajpoot NM112
  98. Rapoport BL113, 114
  99. Rau TT115
  100. Ribeiro JM116
  101. Rimm D117, 118
  102. Vincentsalomon A119
  103. Saltz J120
  104. Sayed S121
  105. Hytopoulos E121, 122
  106. Mahon S123
  107. Siziopikou KP124
  108. Sotiriou C125, 126
  109. Stenzinger A127
  110. Sughayer MA128
  111. Sur D129
  112. Symmans F130
  113. Tanaka S131
  114. Taxter T132
  115. Tejpar S15
  116. Teuwen J133
  117. Thompson EA134
  118. Tramm T135
  119. Tran WT136
  120. Van Der Laak J37
  121. Verghese GE54, 55
  122. Viale G137
  123. Wahab N138
  124. Walter T81, 82, 83
  125. Waumans Y139
  126. Wen HY57
  127. Yang W140
  128. Yuan Y141
  129. Bartlett J142
  130. Loibl S143
  131. Denkert C144
  132. Savas P102, 145
  133. Loi S102, 146
  134. Specht Stovgaard E147
  135. Salgado R3, 102
  136. Gallagher WM1
  137. Rahman A148
Show Affiliations
Authors Affiliations
  1. 1. UCD School of Biomolecular and Biomedical Science, UCD Conway Institute, University College Dublin, Dublin, Ireland
  2. 2. Earle A Chiles Research Institute, Providence Cancer Institute, Portland, OR, United States
  3. 3. Department of Pathology PA2, GZA-ZNA Hospitals, Antwerp, Belgium
  4. 4. Centre for Oncological Research (CORE), MIPPRO, Faculty of Medicine, Antwerp University, Antwerp, Belgium
  5. 5. Department of Pathology and Laboratory Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, United States
  6. 6. Department of Pathology, Massachusetts General Hospital, Boston, MA, United States
  7. 7. Departments of Pathology and Dermatology, University of Michigan, Ann Arbor, MI, United States
  8. 8. Department of Biomedical Informatics, Stony Brook University, Stony Brook, NY, United States
  9. 9. Institute of Pathology, Klinikum Bayreuth GmbH, Friedrich-Alexander-University Erlangen-Nuremberg, Bayreuth, Germany
  10. 10. Department of Pathology, Matsuyama Shimin Hospital, Matsuyama, Japan
  11. 11. Department of Pathology, Yale School of Medicine, New Haven, CT, United States
  12. 12. Department of Pathology and Laboratory Medicine, University of British Columbia, BC Cancer, Vancouver, BC, Canada
  13. 13. Department of Pathology, University Medical Center Utrecht, Utrecht, Netherlands
  14. 14. Johns Hopkins Oncology Center, Baltimore, MD, United States
  15. 15. Digestive Oncology, Department of Oncology, KU Leuven, Leuven, Belgium
  16. 16. Technical University of Denmark, Kgs. Lyngby, Denmark
  17. 17. Visiopharm A/S, Horsholm, Denmark
  18. 18. Department of Cellular Pathology, University College Hospital, London, United Kingdom
  19. 19. Centre for Evolution and Cancer, The Institute of Cancer Research, London, United Kingdom
  20. 20. Hospital Maria Curie, Buenos Aires, Argentina
  21. 21. Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden
  22. 22. Department of Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden
  23. 23. Perlmutter Cancer Center, NYU Langone Health, New York, NY, United States
  24. 24. Department of Medicine, NYU Grossman School of Medicine, Manhattan, NY, United States
  25. 25. Division of Cancer Epidemiology and Genetics (DCEG), National Cancer Institute (NCI), Rockville, MD, United States
  26. 26. Oncology Hospital, Star Medica Centro, Juarez City, Mexico
  27. 27. Tehran University of Medical Sciences, Tehran, Iran
  28. 28. Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Emory University Winship Cancer Institute, Atlanta, GA, United States
  29. 29. The National University of Malaysia, Kuala Lumpur, Malaysia
  30. 30. Departamento de Anatomia Patologica, Facultad de Medicina, Universidad de La Frontera, Temuco, Chile
  31. 31. Department of Pathology, Narayana Medical College, Nellore, India
  32. 32. Department of Internal Medicine Section of Medical Oncology and Yale Cancer Center, Yale School of Medicine, New Haven, CT, United States
  33. 33. Department of Computer Science, Yale School of Engineering and Applied Science, New Haven, CT, United States
  34. 34. Amazonas Federal University, Manaus, Brazil
  35. 35. Pathology Department, Hospital Clinico Universitario de Valencia/Incliva, Valencia, Spain
  36. 36. Department of Pathobiology & Population Sciences, The Royal Veterinary College, London, United Kingdom
  37. 37. Head of Integrative Genomics Analysis in Clinical Trials, ICR-CTSU, Division of Clinical Studies, The Institute of Cancer Research, London, United Kingdom
  38. 38. Department of Pathology, Radboud University Medical Center, Nijmegen, Netherlands
  39. 39. Department of Pathology, Northwestern Feinberg School of Medicine, Chicago, IL, United States
  40. 40. Department of Oncology, Laboratory of Tumor Immunology and Immunotherapy, KU Leuven, Leuven, Belgium
  41. 41. Biomedical Engineering Department, Emory University, Atlanta, GA, United States
  42. 42. Hospital Universitario Getulio Vargas, Manaus, Brazil
  43. 43. Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, United States
  44. 44. Department of Pathology, Weill Cornell Medicine, New York, NY, United States
  45. 45. Computational Biology and Bioinformatics, Yale University, New Haven, CT, United States
  46. 46. University of Surrey, Guildford, United Kingdom
  47. 47. Ain Shams University, Cairo, Egypt
  48. 48. Instituto Universitario de Investigacion en Tecnologia Centrada en el Ser Humano, HUMAN-tech, Universitat Politecnica de Valencia, Valencia, Spain
  49. 49. Montefiore Medical Center and the Albert Einstein College of Medicine, New York, NY, United States
  50. 50. Pathology, Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, VIC, Australia
  51. 51. Genentech, San Francisco, CA, United States
  52. 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, United States
  53. 53. Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, United States
  54. 54. Cancer Bioinformatics, Faculty of Life Sciences and Medicine, School of Cancer & Pharmaceutical Sciences, King's College London, London, United Kingdom
  55. 55. The Breast Cancer Now Research Unit, Faculty of Life Sciences and Medicine, School of Cancer and Pharmaceutical Sciences, King's College London, London, United Kingdom
  56. 56. Department of Translational Immunotherapy, German Cancer Research Center, Heidelberg, Germany
  57. 57. Memorial Sloan Kettering Cancer Center, New York, NY, United States
  58. 58. Case Western University, Cleveland, OH, United States
  59. 59. Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, United States
  60. 60. Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden
  61. 61. Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States
  62. 62. Division of Pathology, Netherlands Cancer Institute (NKI), Amsterdam, Netherlands
  63. 63. Praava Health, Dhaka, Bangladesh
  64. 64. King's College London & Guys & St Thomas NHS Trust, London, United Kingdom
  65. 65. Department of Pathology, Stavanger University Hospital, Stavanger, Norway
  66. 66. Department of Chemistry, Bioscience and Environmental Technology, University of Stavanger, Stavanger, Norway
  67. 67. Department of Pathology, Iwate Medical University, Morioka, Japan
  68. 68. Department of Breast Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan
  69. 69. Department of Pathology and Laboratory Medicine, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, United States
  70. 70. Histopathology, Aakash Healthcare Super Speciality Hospital, New Delhi, India
  71. 71. Department of Pathology, Netherlands Cancer Institute – Antoni van Leeuwenhoek Hospital, Amsterdam, Netherlands
  72. 72. Data, Analytics and Imaging, Product Development, F. Hoffmann-La Roche AG, Basel, Switzerland
  73. 73. Translational Molecular Biomarkers, Merck & Co., Inc., Kenilworth, NJ, United States
  74. 74. Translational Medicine, Bristol Myers Squibb, Princeton, NJ, United States
  75. 75. Department of Clinical Pathology, Sahlgrenska University Hospital, Gothenburg, Sweden
  76. 76. Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
  77. 77. Department of Surgical Pathology, Zealand University Hospital, Roskilde, Denmark
  78. 78. Department of Surgical Pathology, University of Copenhagen, Copenhagen, Denmark
  79. 79. Institut Jules Bordet, Universite Libre de Bruxelles, Brussels, Belgium
  80. 80. Center for Integrated Diagnostics, Massachusetts General Hospital/Harvard Medical School, Boston, MA, United States
  81. 81. Centre for Computational Biology (CBIO), Mines Paris, PSL University, Paris, France
  82. 82. Institut Curie, PSL University, Paris, France
  83. 83. INSERM U900, Paris, France
  84. 84. Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, United States
  85. 85. Department of Biomedical Engineering, Radiology and Imaging Sciences, Biomedical Informatics, Pathology, Georgia Institute of Technology and Emory University, Atlanta, GA, United States
  86. 86. NRG Oncology/NSABP Foundation, Pittsburgh, PA, United States
  87. 87. Manipal Hospitals, Bangalore, India
  88. 88. Breast Cancer Translational Research Group, University of Pennsylvania, Philadelphia, PA, United States
  89. 89. Indian Cancer Genomic Atlas, Pune, India
  90. 90. Centre for Health, Innovation and Policy Foundation, Noida, India
  91. 91. Office of Biostatistics and Epidemiology, Gustave Roussy, Oncostat U1018, Inserm, University Paris-Saclay, Ligue Contre le Cancer labeled Team, Villejuif, France
  92. 92. Department of Pathology, Narayana Medical College and Hospital, Nellore, India
  93. 93. Tissue Image Analytics Centre, Warwick Cancer Research Centre, PathLAKE Consortium, Department of Computer Science, University of Warwick, Coventry, United Kingdom
  94. 94. Department of Chemical Engineering, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA, United States
  95. 95. CRUK Lung Cancer Centre of Excellence, UCL and Cellular Pathology Department, UCLH, London, United Kingdom
  96. 96. Department of Biochemistry, Ziauddin University, Karachi, Pakistan
  97. 97. Pathology and Laboratory Medicine, All India Institute of Medical Sciences, Raipur, India
  98. 98. Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, United Kingdom
  99. 99. Department of Clinical Pathology, Drammen Sykehus, Vestre Viken HF, Drammen, Norway
  100. 100. Service de Pathologie et Biopathologie, Centre Jean PERRIN, INSERM U1240 Imagerie Moleculaire et Strategies Theranostiques (IMoST), Universite Clermont Auvergne, Clermont-Ferrand, France
  101. 101. School of Electrical, Mechanical and Infrastructure Engineering, University of Melbourne, Melbourne, VIC, Australia
  102. 102. Division of Cancer Research, Peter MacCallum Cancer Centre, Melbourne, VIC, Australia
  103. 103. Radiogenomics Laboratory, Sunnybrook Health Sciences Centre, Toronto, ON, Canada
  104. 104. Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada
  105. 105. Department of Oncology, Lakeshore Animal Health Partners, Mississauga, ON, Canada
  106. 106. Centre for Advancing Responsible and Ethical Artificial Intelligence (CARE-AI), University of Guelph, Guelph, ON, Canada
  107. 107. Diagnostico de Salud Animal SA, Ciudad de Mexico, Mexico
  108. 108. Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
  109. 109. Faculty of Medicine and Surgery, University of Milan, Milan, Italy
  110. 110. Yale Cancer Center, Yale University, New Haven, CT, United States
  111. 111. Department of Medical Oncology, Yale School of Medicine, Yale University, New Haven, CT, United States
  112. 112. University of Warwick, Coventry, United Kingdom
  113. 113. The Medical Oncology Centre of Rosebank, Johannesburg, South Africa
  114. 114. Department of Immunology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa
  115. 115. Institute of Pathology, University Hospital Dusseldorf and Heinrich-Heine-University, Dusseldorf, Germany
  116. 116. Breast Unit, Institute Gustave Roussy, Villejuif, France
  117. 117. Department of Pathology, Yale University School of Medicine, New Haven, CT, United States
  118. 118. Department of Medicine, Yale University School of Medicine, New Haven, CT, United States
  119. 119. Department of Diagnostic and Theranostic Medicine, Institut Curie, University Paris-Sciences et Lettres, Paris, France
  120. 120. Department of Biomedical Informatics, Stony Brook Medicine, New York, NY, United States
  121. 121. Department of Pathology, Aga Khan University, Nairobi, Kenya
  122. 122. iRhythm Technologies Inc., San Francisco, CA, United States
  123. 123. Mater Misericordiae University Hospital, Dublin, Ireland
  124. 124. Department of Pathology, Section of Breast Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, United States
  125. 125. Breast Cancer Translational Research Laboratory J.-C. Heuson, Institut Jules Bordet, Hopital Universitaire de Bruxelles (H.U.B), Universite Libre de Bruxelles (ULB), Brussels, Belgium
  126. 126. Medical Oncology Department, Institut Jules Bordet, Hopital Universitaire de Bruxelles (H.U.B), Universite Libre de Bruxelles (ULB), Brussels, Belgium
  127. 127. Institute of Pathology, University Hospital Heidelberg, Centers for Personalized Medicine (ZPM), Heidelberg, Germany
  128. 128. King Hussein Cancer Center, Amman, Jordan
  129. 129. Department of Medical Oncology, University of Medicine and Pharmacy “Iuliu Hatieganu�, Cluj-Napoca, Romania
  130. 130. University of Texas MD Anderson Cancer Center, Houston, TX, United States
  131. 131. Kyoto University, Kyoto, Japan
  132. 132. Tempus Labs, Chicago, IL, United States
  133. 133. AI for Oncology Lab, The Netherlands Cancer Institute, Amsterdam, Netherlands
  134. 134. Mayo Clinic, Jacksonville, FL, United States
  135. 135. Department of Pathology, Institute of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark
  136. 136. Department of Radiation Oncology, University of Toronto and Sunnybrook Health Sciences Centre, Toronto, Canada
  137. 137. Department of Pathology, European Institute of Oncology & University of Milan, Milan, Italy
  138. 138. Tissue Image Analytics Centre, Department of Computer Science, University of Warwick, Coventry, United Kingdom
  139. 139. CellCarta NV, Antwerp, Belgium
  140. 140. Fudan Medical University Shanghai Cancer Center, Shanghai, China
  141. 141. Department of Translational Molecular Pathology, Division of Pathology and Laboratory Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, United States
  142. 142. University of Edinburgh, Edinburgh, United Kingdom
  143. 143. Department of Medicine and Research, German Breast Group, Neu-Isenburg, Germany
  144. 144. Institut fur Pathologie, Philipps-Universitat Marburg und Universitatsklinikum Marburg, Marburg, Germany
  145. 145. The Sir Peter MacCallum Department of Medical Oncology, University of Melbourne, Melbourne, VIC, Australia
  146. 146. Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, VIC, Australia
  147. 147. Department of Pathology, Herlev and Gentofte Hospital, Herlev, Denmark
  148. 148. UCD School of Medicine, UCD Conway Institute, University College Dublin, Dublin, Ireland

Source: Journal of Pathology Published:2024


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. © 2024 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.
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