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
(1, 2)
,
David B Page
(3)
,
Glenn Broeckx
(4, 5)
,
Claudia A Gonzalez
(1, 2)
,
Caoimbhe Burke
(1, 2)
,
Clodagh Murphy
(1, 2)
,
Jorge S Reis‐filho
(6)
,
Amy Ly
(7)
,
Paul W Harms
(8)
,
Rajarsi R Gupta
(9)
,
Michael Vieth
(10)
,
Akira I Hida
(11)
,
Mohamed Kahila
(12)
,
Zuzana Kos
(13)
,
Paul J van Diest
(14, 15)
,
Sara Verbandt
(16)
,
Jeppe Thagaard
(17)
,
Reena Khiroya
(18)
,
Khalid Abduljabbar
(19)
,
Gabriela Acosta Haab
(20)
,
Balazs Acs
(21, 22)
,
Sylvia Adams
(23, 24)
,
Jonas S Almeida
(25)
,
Isabel Alvarado‐cabrero
(26)
,
Farid Azmoudeh‐ardalan
(27)
,
Sunil Badve
(28)
,
Nurkhairul Bariyah Baharun
(29)
,
Enrique R Bellolio
(30)
,
Vydehi Bheemaraju
(31)
,
Kim Rm Blenman
(12, 32)
,
Luciana Botinelly Mendonça Fujimoto
(33)
,
Octavio Burgues
(34)
,
Alexandros Chardas
(35)
,
Maggie Chon U Cheang
(19)
,
Francesco Ciompi
(36)
,
Lee Ad Cooper
(37)
,
An Coosemans
(16)
,
Germán Corredor
(38)
,
Flavio Luis Dantas Portela
(39)
,
Frederik Deman
(4)
,
Sandra Demaria
(40, 41)
,
Sarah N Dudgeon
(42)
,
Mahmoud Elghazawy
(43, 44)
,
Claudio Fernandez‐martín
(45)
,
Susan Fineberg
(46)
,
Stephen B Fox
(47, 48)
,
Jennifer M Giltnane
(49)
,
Sacha Gnjatic
(50)
,
Paula I Gonzalez‐ericsson
(51)
,
Anita Grigoriadis
(52)
,
Niels Halama
(53)
,
Matthew G Hanna
(6)
,
Aparna Harbhajanka
(54)
,
Steven N Hart
(55)
,
Johan Hartman
(56, 21)
,
Stephen Hewitt
(57)
,
Hugo M Horlings
(58)
,
Zaheed Husain
(59)
,
Sheeba Irshad
(52, 60)
,
Emiel Am Janssen
(61, 62)
,
Tatsuki R Kataoka
(63)
,
Kosuke Kawaguchi
(64)
,
Andrey I Khramtsov
(65)
,
Umay Kiraz
(61, 62)
,
Pawan Kirtani
(66)
,
Liudmila L Kodach
(67)
,
Konstanty Korski
(68)
,
Guray Akturk
(69)
,
Ely Scott
(70)
,
Anikó Kovács
(71, 72)
,
Anne‐vibeke Lænkholm
(73, 74)
,
Corinna Lang‐schwarz
(10)
,
Denis Larsimont
(75, 76)
,
Jochen K Lennerz
(7, 77)
,
Marvin Lerousseau
(78, 79)
,
Xiaoxian Li
(38)
,
Anant Madabhushi
(80, 38)
,
Sai K Maley
(81, 82)
,
Vidya Manur Narasimhamurthy
(83)
,
Douglas K Marks
(84, 23)
,
Elizabeth S Mcdonald
(85, 86)
,
Ravi Mehrotra
(87)
,
Stefan Michiels
(88, 89)
,
Durga Kharidehal
(31)
,
Fayyaz Ul Amir Afsar Minhas
(90)
,
Shachi Mittal
(91)
,
David A Moore
(92)
,
Shamim Mushtaq
(93)
,
Hussain Nighat
(94)
,
Thomas Papathomas
(95)
,
Frederique Penault‐llorca
(96)
,
Rashindrie D Perera
(48, 97)
,
Christopher J Pinard
(98, 99)
,
Juan Carlos Pinto‐cardenas
(100)
,
Giancarlo Pruneri
(101, 102)
,
Lajos Pusztai
(42, 12)
,
Nasir Mahmood Rajpoot
(90)
,
Bernardo Leon Rapoport
(103)
,
Tilman T Rau
(104, 105)
,
Joana M Ribeiro
(89)
,
David Rimm
(42, 12)
,
Anne Vincent‐salomon
(79)
,
Joel Saltz
(106)
,
Shahin Sayed
(107)
,
Evangelos Hytopoulos
(107)
,
Sarah Mahon
(108)
,
Kalliopi P Siziopikou
(109, 110)
,
Christos Sotiriou
(75, 76, 111)
,
Albrecht Stenzinger
(112)
,
Maher A Sughayer
(113)
,
Daniel Sur
(114)
,
Fraser Symmans
(115)
,
Sunao Tanaka
(64)
,
Timothy Taxter
(116)
,
Sabine Tejpar
(16)
,
Jonas Teuwen
(58)
,
E Aubrey Thompson
(117)
,
Trine Tramm
(118)
,
William T Tran
(119, 99)
,
Jeroen van der Laak
(19)
,
Gregory E Verghese
(52)
,
Giuseppe Viale
(102)
,
Noorul Wahab
(90)
,
Thomas Walter
(78)
,
Yannick Waumans
(120)
,
Hannah Y Wen
(6)
,
Wentao Yang
(121, 122)
,
Yinyin Yuan
(115)
,
John Bartlett
(123)
,
Sibylle Loibl
(124)
,
Carsten Denkert
(125, 126)
,
Peter Savas
(97, 48)
,
Sherene Loi
(97, 48)
,
Elisabeth Specht Stovgaard
(127)
,
Roberto Salgado
(97, 4)
,
William M Gallagher
(128, 1)
,
Arman Rahman
(128, 1)
1
UCD -
University College Dublin [Dublin]
2 UCD Conway Institute
3 Earle A. Chiles Research Institute [Portland, OR, USA]
4 UZA - Antwerp University Hospital [Edegem]
5 UA - University of Antwerp
6 Memorial Sloane Kettering Cancer Center [New York]
7 Massachusetts General Hospital [Boston]
8 University of Michigan [Ann Arbor]
9 SBU - Stony Brook University [SUNY]
10 FAU - Friedrich-Alexander Universität Erlangen-Nürnberg = University of Erlangen-Nuremberg
11 MSH - Matsuyama Shimin Hospital [Matsuyama, Japan]
12 YSM - Yale School of Medicine [New Haven, Connecticut]
13 UBC - University of British Columbia
14 UMCU - University Medical Center [Utrecht]
15 Johns Hopkins University School of Medicine [Baltimore]
16 KU Leuven - Catholic University of Leuven = Katholieke Universiteit Leuven
17 Department of Health Technology, Technical University of Denmark
18 UCLH - University College London Hospitals
19 The institute of cancer research [London]
20 Hospital Maria Curie [Buenos Aires, Argentina]
21 Karolinska Institutet [Stockholm]
22 Karolinska University Hospital [Stockholm]
23 NYU Langone Health [New York]
24 NYU Grossman School of Medicine - New York University School of Medicine
25 NCI-NIH - National Cancer Institute [Bethesda]
26 Star Medical Diagnostic Center
27 IUMS - Iran University of Medical Sciences [Tehran, Iran]
28 Emory University School of Medicine
29 UKM - National University of Malaysia [Bandar Baru Bangi]
30 UFRO - Universidad de la frontera [Tecumo, Chile] = University of La Frontera [Tecumo, Chile] = Université de La Frontera [Tecumo, Chili]
31 Narayana Medical College [Nellore, India]
32 Yale school of Engineering [New Haven]
33 Federal University of Amazonas
34 Hospital Clínico Universitario, Valencia
35 The Royal Veterinary College
36 Radboud University Medical Center [Nijmegen]
37 Department of Pediatrics [Feinberg School of Medicine, Northwestern University]
38 Emory University [Atlanta, GA]
39 Fundação Getúlio Vargas [San Paulo]
40 Weill Medical College of Cornell University [New York]
41 Sandra and Edward Meyer Cancer Center [New-York]
42 Yale University [New Haven]
43 UNIS - University of Surrey
44 ASU - Ain Shams University
45 UPV - Universitat Politècnica de València = Universitad Politecnica de Valencia = Polytechnic University of Valencia
46 Albert Einstein College of Medicine [New York]
47 Peter MacCallum Cancer Centre
48 University of Melbourne
49 Genentech, Inc. [San Francisco]
50 MSSM - Icahn School of Medicine at Mount Sinai [New York]
51 Vanderbilt University Medical Center [Nashville]
52 King‘s College London
53 DKFZ - German Cancer Research Center - Deutsches Krebsforschungszentrum [Heidelberg]
54 Case Western Reserve University [Cleveland]
55 Mayo Clinic [Rochester]
56 TUMS - Tehran University of Medical Sciences
57 NIH - National Institutes of Health [Bethesda, MD, USA]
58 NKI - Netherlands Cancer Institute
59 Praava Health [Dhaka, Bangladesh]
60 Guy's and St Thomas' NHS Foundation Trust [London, UK]
61 Stavanger University Hospital
62 University of Stavanger
63 Iwate Medical University
64 Kyoto University
65 Ann & Robert H. Lurie Children's Hospital of Chicago
66 Associate Consultant- Cardiology, Aakash Healthcare Pvt. Ltd., Dwarka, New Delhi, India
67 Antoni van Leeuwenhoek Hospital
68 Data, Analytics and Imaging, F. Hoffmann-La Roche AG [ Basel, Switzerland]
69 Translational Molecular Biomarkers [Kenilworth, USA]
70 Bristol-Myers Squibb [Princeton]
71 Sahlgrenska University Hospital [Gothenburg]
72 GU - Göteborgs Universitet = University of Gothenburg
73 Zealand University Hospital [Roskilde, Denmark]
74 UCPH - University of Copenhagen = Københavns Universitet
75 Institut Jules Bordet [Bruxelles]
76 ULB - Université libre de Bruxelles
77 HMS - Harvard Medical School [Boston]
78 Cancer et génome: Bioinformatique, biostatistiques et épidémiologie d'un système complexe
79 Institut Curie [Paris]
80 Georgia Institute of Technology [Atlanta]
81 NRG Oncology [Pittsburgh, USA]
82 NSABP - National Surgical Adjuvant Breast and Bowel Project [Pittsburgh, USA]
83 Melaka Manipal Medical College (Manipal Campus), Manipal University, Karnataka State, India
84 NYUP2C - NYU Perlmutter Cancer Center [New York, NY, USA]
85 Breast Cancer Translational Research Laboratory
86 University of Pennsylvania
87 Indian Cancer Genomic Atlas [Pune, India]
88 U1018 (Équipe 2) - Oncostat
89 IGR - Institut Gustave Roussy
90 University of Warwick [Coventry]
91 University of Washington [Seattle]
92 CRUK Lung Cancer Centre of Excellence [london, United Kingdom]
93 Ziauddin University [Karachi, Pakistan]
94 All India Institute of Medical Sciences [New Delhi]
95 University of Birmingham [Birmingham]
96 IMoST - Imagerie Moléculaire et Stratégies Théranostiques
97 Peter MacCallum Cancer Centre
98 University of Guelph
99 Sunnybrook - Sunnybrook Health Sciences Centre [Toronto]
100 UACM - Universidad Autónoma de la Ciudad de México
101 Human Tumor Immunobiology Unit [Fondazione IRCCS Istituto Nazionale dei Tumori, Milan]
102 UNIMI - Università degli Studi di Milano = University of Milan
103 University of Pretoria [South Africa]
104 University Hospital Düsseldorf
105 Heinrich Heine Universität Düsseldorf = Heinrich Heine University [Düsseldorf]
106 School of Dental Medicine - Department of Oral Biology and Pathology [Stony Brook, NY, USA]
107 Aga Khan University Hospital (AKUH), Nairobi
108 The Mater Hospital - Mater Misericordiae University Hospital
109 Northwestern University [Evanston]
110 [Northwestern University Medical School] - Feinberg School of Medicine [Northwestern University, Evanston]
111 Université de Bruxelles
112 Heidelberg University Hospital [Heidelberg]
113 KH2C - King Hussein Cancer Center [Amman, Jordan]
114 UMF - Iuliu Haţieganu University of Medicine and Pharmacy of Cluj-Napoca = Universitatea de Medicină şi Farmacie Iuliu Haţieganu din Cluj-Napoca
115 The University of Texas M.D. Anderson Cancer Center [Houston]
116 Tempus Labs [ Chicago, USA]
117 Mayo Clinic [Jacksonville]
118 Aarhus University Hospital
119 University of Toronto
120 CellCarta [Antwerp, Belgium]
121 Shanghai University
122 Shanghai Medical College of Fudan University
123 Edin. - University of Edinburgh
124 GBG - German Breast Group
125 Philipps Universität Marburg = Philipps University of Marburg
126 Universitatsklinikum Giessen und Marburg [Marburg,Germany]
127 Herlev and Gentofte Hospital
128 UCD Conway Institute
2 UCD Conway Institute
3 Earle A. Chiles Research Institute [Portland, OR, USA]
4 UZA - Antwerp University Hospital [Edegem]
5 UA - University of Antwerp
6 Memorial Sloane Kettering Cancer Center [New York]
7 Massachusetts General Hospital [Boston]
8 University of Michigan [Ann Arbor]
9 SBU - Stony Brook University [SUNY]
10 FAU - Friedrich-Alexander Universität Erlangen-Nürnberg = University of Erlangen-Nuremberg
11 MSH - Matsuyama Shimin Hospital [Matsuyama, Japan]
12 YSM - Yale School of Medicine [New Haven, Connecticut]
13 UBC - University of British Columbia
14 UMCU - University Medical Center [Utrecht]
15 Johns Hopkins University School of Medicine [Baltimore]
16 KU Leuven - Catholic University of Leuven = Katholieke Universiteit Leuven
17 Department of Health Technology, Technical University of Denmark
18 UCLH - University College London Hospitals
19 The institute of cancer research [London]
20 Hospital Maria Curie [Buenos Aires, Argentina]
21 Karolinska Institutet [Stockholm]
22 Karolinska University Hospital [Stockholm]
23 NYU Langone Health [New York]
24 NYU Grossman School of Medicine - New York University School of Medicine
25 NCI-NIH - National Cancer Institute [Bethesda]
26 Star Medical Diagnostic Center
27 IUMS - Iran University of Medical Sciences [Tehran, Iran]
28 Emory University School of Medicine
29 UKM - National University of Malaysia [Bandar Baru Bangi]
30 UFRO - Universidad de la frontera [Tecumo, Chile] = University of La Frontera [Tecumo, Chile] = Université de La Frontera [Tecumo, Chili]
31 Narayana Medical College [Nellore, India]
32 Yale school of Engineering [New Haven]
33 Federal University of Amazonas
34 Hospital Clínico Universitario, Valencia
35 The Royal Veterinary College
36 Radboud University Medical Center [Nijmegen]
37 Department of Pediatrics [Feinberg School of Medicine, Northwestern University]
38 Emory University [Atlanta, GA]
39 Fundação Getúlio Vargas [San Paulo]
40 Weill Medical College of Cornell University [New York]
41 Sandra and Edward Meyer Cancer Center [New-York]
42 Yale University [New Haven]
43 UNIS - University of Surrey
44 ASU - Ain Shams University
45 UPV - Universitat Politècnica de València = Universitad Politecnica de Valencia = Polytechnic University of Valencia
46 Albert Einstein College of Medicine [New York]
47 Peter MacCallum Cancer Centre
48 University of Melbourne
49 Genentech, Inc. [San Francisco]
50 MSSM - Icahn School of Medicine at Mount Sinai [New York]
51 Vanderbilt University Medical Center [Nashville]
52 King‘s College London
53 DKFZ - German Cancer Research Center - Deutsches Krebsforschungszentrum [Heidelberg]
54 Case Western Reserve University [Cleveland]
55 Mayo Clinic [Rochester]
56 TUMS - Tehran University of Medical Sciences
57 NIH - National Institutes of Health [Bethesda, MD, USA]
58 NKI - Netherlands Cancer Institute
59 Praava Health [Dhaka, Bangladesh]
60 Guy's and St Thomas' NHS Foundation Trust [London, UK]
61 Stavanger University Hospital
62 University of Stavanger
63 Iwate Medical University
64 Kyoto University
65 Ann & Robert H. Lurie Children's Hospital of Chicago
66 Associate Consultant- Cardiology, Aakash Healthcare Pvt. Ltd., Dwarka, New Delhi, India
67 Antoni van Leeuwenhoek Hospital
68 Data, Analytics and Imaging, F. Hoffmann-La Roche AG [ Basel, Switzerland]
69 Translational Molecular Biomarkers [Kenilworth, USA]
70 Bristol-Myers Squibb [Princeton]
71 Sahlgrenska University Hospital [Gothenburg]
72 GU - Göteborgs Universitet = University of Gothenburg
73 Zealand University Hospital [Roskilde, Denmark]
74 UCPH - University of Copenhagen = Københavns Universitet
75 Institut Jules Bordet [Bruxelles]
76 ULB - Université libre de Bruxelles
77 HMS - Harvard Medical School [Boston]
78 Cancer et génome: Bioinformatique, biostatistiques et épidémiologie d'un système complexe
79 Institut Curie [Paris]
80 Georgia Institute of Technology [Atlanta]
81 NRG Oncology [Pittsburgh, USA]
82 NSABP - National Surgical Adjuvant Breast and Bowel Project [Pittsburgh, USA]
83 Melaka Manipal Medical College (Manipal Campus), Manipal University, Karnataka State, India
84 NYUP2C - NYU Perlmutter Cancer Center [New York, NY, USA]
85 Breast Cancer Translational Research Laboratory
86 University of Pennsylvania
87 Indian Cancer Genomic Atlas [Pune, India]
88 U1018 (Équipe 2) - Oncostat
89 IGR - Institut Gustave Roussy
90 University of Warwick [Coventry]
91 University of Washington [Seattle]
92 CRUK Lung Cancer Centre of Excellence [london, United Kingdom]
93 Ziauddin University [Karachi, Pakistan]
94 All India Institute of Medical Sciences [New Delhi]
95 University of Birmingham [Birmingham]
96 IMoST - Imagerie Moléculaire et Stratégies Théranostiques
97 Peter MacCallum Cancer Centre
98 University of Guelph
99 Sunnybrook - Sunnybrook Health Sciences Centre [Toronto]
100 UACM - Universidad Autónoma de la Ciudad de México
101 Human Tumor Immunobiology Unit [Fondazione IRCCS Istituto Nazionale dei Tumori, Milan]
102 UNIMI - Università degli Studi di Milano = University of Milan
103 University of Pretoria [South Africa]
104 University Hospital Düsseldorf
105 Heinrich Heine Universität Düsseldorf = Heinrich Heine University [Düsseldorf]
106 School of Dental Medicine - Department of Oral Biology and Pathology [Stony Brook, NY, USA]
107 Aga Khan University Hospital (AKUH), Nairobi
108 The Mater Hospital - Mater Misericordiae University Hospital
109 Northwestern University [Evanston]
110 [Northwestern University Medical School] - Feinberg School of Medicine [Northwestern University, Evanston]
111 Université de Bruxelles
112 Heidelberg University Hospital [Heidelberg]
113 KH2C - King Hussein Cancer Center [Amman, Jordan]
114 UMF - Iuliu Haţieganu University of Medicine and Pharmacy of Cluj-Napoca = Universitatea de Medicină şi Farmacie Iuliu Haţieganu din Cluj-Napoca
115 The University of Texas M.D. Anderson Cancer Center [Houston]
116 Tempus Labs [ Chicago, USA]
117 Mayo Clinic [Jacksonville]
118 Aarhus University Hospital
119 University of Toronto
120 CellCarta [Antwerp, Belgium]
121 Shanghai University
122 Shanghai Medical College of Fudan University
123 Edin. - University of Edinburgh
124 GBG - German Breast Group
125 Philipps Universität Marburg = Philipps University of Marburg
126 Universitatsklinikum Giessen und Marburg [Marburg,Germany]
127 Herlev and Gentofte Hospital
128 UCD Conway Institute
Chowdhury Arif Jahangir
- Fonction : Auteur
- PersonId : 1284895
- ORCID : 0000-0002-5389-7275
David B Page
- Fonction : Auteur
- PersonId : 1284894
- ORCID : 0000-0001-9264-4628
Jorge S Reis‐filho
- Fonction : Auteur
- PersonId : 1284903
- ORCID : 0000-0003-2969-3173
Rajarsi R Gupta
- Fonction : Auteur
- PersonId : 1284896
- ORCID : 0000-0002-1577-8718
Alexandros Chardas
- Fonction : Auteur
- PersonId : 1284900
- ORCID : 0000-0001-9906-7552
Flavio Luis Dantas Portela
- Fonction : Auteur
- PersonId : 1284897
- ORCID : 0000-0003-0188-3709
Mahmoud Elghazawy
- Fonction : Auteur
- PersonId : 1284898
- ORCID : 0000-0002-3100-7606
Paula I Gonzalez‐ericsson
- Fonction : Auteur
- PersonId : 1230968
- ORCID : 0000-0002-6292-6963
Anita Grigoriadis
- Fonction : Auteur
- PersonId : 1284899
- ORCID : 0000-0003-3434-201X
Steven N Hart
- Fonction : Auteur
- PersonId : 826520
- ORCID : 0000-0001-7714-2734
Johan Hartman
- Fonction : Auteur
- PersonId : 1188518
- ORCID : 0000-0002-6500-8527
Tatsuki R Kataoka
- Fonction : Auteur
- PersonId : 1284901
- ORCID : 0000-0003-3095-8976
Tilman T Rau
- Fonction : Auteur
- PersonId : 1284902
- ORCID : 0000-0002-1251-950X
David Rimm
- Fonction : Auteur
- PersonId : 785541
- ORCID : 0000-0001-5820-4397
Gregory E Verghese
- Fonction : Auteur
- PersonId : 1284904
- ORCID : 0009-0006-7638-6431
Noorul Wahab
- Fonction : Auteur
- PersonId : 1284905
- ORCID : 0000-0002-1251-1559
Roberto Salgado
- Fonction : Auteur
Résumé
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.
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