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; David B. Page; Glenn Broeckx; Claudia A. Gonzalez; Caoimbhe Burke; Clodagh Murphy; Jorge S. Reis-Filho; Amy Ly; Paul W. Harms; Rajarsi R. Gupta; Michael Vieth; Akira I. Hida; Mohamed Kahila; Zuzana Kos; Paul J. van Diest; Sara Verbandt; Jeppe Thagaard; Reena Khiroya; Khalid Abduljabbar; Gabriela Acosta Haab; Balazs Acs; Sylvia Adams; Jonas S. Almeida; Isabel Alvarado-Cabrero; Farid Azmoudeh-Ardalan; Sunil Badve; Nurkhairul Bariyah Baharun; Enrique R. Bellolio; Vydehi Bheemaraju; Kim R.M. Blenman; Luciana Botinelly Mendonça Fujimoto; Octavio Burgues; Alexandros Chardas; Maggie Chon U. Cheang; Francesco Ciompi; Lee A.D. Cooper; An Coosemans; Germán Corredor; Flavio Luis Dantas Portela; Frederik Deman; Sandra Demaria; Sarah N. Dudgeon; Mahmoud Elghazawy; Claudio Fernandez-Martín; Susan Fineberg; Stephen B. Fox; Jennifer M. Giltnane; Sacha Gnjatic; Paula I. Gonzalez-Ericsson; Anita Grigoriadis; Niels Halama; Matthew G. Hanna; Aparna Harbhajanka; Steven N. Hart; Johan Hartman; Stephen Hewitt; Hugo M. Horlings; Zaheed Husain; Sheeba Irshad; Emiel A.M. Janssen; Tatsuki R. Kataoka; Kosuke Kawaguchi; Andrey I. Khramtsov; Umay Kiraz; Pawan Kirtani; Liudmila L. Kodach; Konstanty Korski; Guray Akturk; Ely Scott; Anikó Kovács; Anne Vibeke Lænkholm; Corinna Lang-Schwarz; Denis Larsimont; Jochen K. Lennerz; Marvin Lerousseau; Xiaoxian Li; Anant Madabhushi; Sai K. Maley; Vidya Manur Narasimhamurthy; Douglas K. Marks; Elizabeth S. McDonald; Ravi Mehrotra; Stefan Michiels; Durga Kharidehal; Fayyaz ul Amir Afsar Minhas; Shachi Mittal; David A. Moore; Shamim Mushtaq; Hussain Nighat; Thomas Papathomas; Frederique Penault-Llorca; Rashindrie D. Perera; Christopher J. Pinard; Juan Carlos Pinto-Cardenas; Giancarlo Pruneri; Lajos Pusztai; Nasir Mahmood Rajpoot; Bernardo Leon Rapoport; Tilman T. Rau; Joana M. Ribeiro; David Rimm; Anne Vincent-Salomon; Joel Saltz; Shahin Sayed; Evangelos Hytopoulos; Sarah Mahon; Kalliopi P. Siziopikou; Christos Sotiriou; Albrecht Stenzinger; Maher A. Sughayer; Daniel Sur; Fraser Symmans; Sunao Tanaka; Timothy Taxter; Sabine Tejpar; Jonas Teuwen; E. Aubrey Thompson; Trine Tramm; William T. Tran; Jeroen van der Laak; Gregory E. Verghese; Giuseppe Viale; Noorul Wahab; Thomas Walter; Yannick Waumans; Hannah Y. Wen; Wentao Yang; Yinyin Yuan; John Bartlett; Sibylle Loibl; Carsten Denkert; Peter Savas; Sherene Loi; Elisabeth Specht Stovgaard; Roberto Salgado; William M. Gallagher; Arman Rahman

doi:10.1002/path.6238

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, David B. Page, Glenn Broeckx, Claudia A. Gonzalez, Caoimbhe Burke, Clodagh Murphy, Jorge S. Reis-Filho, Amy Ly, Paul W. Harms, Rajarsi R. Gupta, Michael Vieth, Akira I. Hida, Mohamed Kahila, Zuzana Kos, Paul J. van Diest, Sara Verbandt, Jeppe Thagaard, Reena Khiroya, Khalid Abduljabbar, Gabriela Acosta HaabBalazs Acs, Sylvia Adams, Jonas S. Almeida, Isabel Alvarado-Cabrero, Farid Azmoudeh-Ardalan, Sunil Badve, Nurkhairul Bariyah Baharun, Enrique R. Bellolio, Vydehi Bheemaraju, Kim R.M. Blenman, Luciana Botinelly Mendonça Fujimoto, Octavio Burgues, Alexandros Chardas, Maggie Chon U. Cheang, Francesco Ciompi, Lee A.D. Cooper, An Coosemans, Germán Corredor, Flavio Luis Dantas Portela, Frederik Deman, Sandra Demaria, Sarah N. Dudgeon, Mahmoud Elghazawy, Claudio Fernandez-Martín, Susan Fineberg, Stephen B. Fox, Jennifer M. Giltnane, Sacha Gnjatic, Paula I. Gonzalez-Ericsson, Anita Grigoriadis, Niels Halama, Matthew G. Hanna, Aparna Harbhajanka, Steven N. Hart, Johan Hartman, Stephen Hewitt, Hugo M. Horlings, Zaheed Husain, Sheeba Irshad, Emiel A.M. Janssen, Tatsuki R. Kataoka, Kosuke Kawaguchi, Andrey I. Khramtsov, Umay Kiraz, Pawan Kirtani, Liudmila L. Kodach, Konstanty Korski, Guray Akturk, Ely Scott, Anikó Kovács, Anne Vibeke Lænkholm, Corinna Lang-Schwarz, Denis Larsimont, Jochen K. Lennerz, Marvin Lerousseau, Xiaoxian Li, Anant Madabhushi, Sai K. Maley, Vidya Manur Narasimhamurthy, Douglas K. Marks, Elizabeth S. McDonald, Ravi Mehrotra, Stefan Michiels, Durga Kharidehal, Fayyaz ul Amir Afsar Minhas, Shachi Mittal, David A. Moore, Shamim Mushtaq, Hussain Nighat, Thomas Papathomas, Frederique Penault-Llorca, Rashindrie D. Perera, Christopher J. Pinard, Juan Carlos Pinto-Cardenas, Giancarlo Pruneri, Lajos Pusztai, Nasir Mahmood Rajpoot, Bernardo Leon Rapoport, Tilman T. Rau, Joana M. Ribeiro, David Rimm, Anne Vincent-Salomon, Joel Saltz, Shahin Sayed, Evangelos Hytopoulos, Sarah Mahon, Kalliopi P. Siziopikou, Christos Sotiriou, Albrecht Stenzinger, Maher A. Sughayer, Daniel Sur, Fraser Symmans, Sunao Tanaka, Timothy Taxter, Sabine Tejpar, Jonas Teuwen, E. Aubrey Thompson, Trine Tramm, William T. Tran, Jeroen van der Laak, Gregory E. Verghese, Giuseppe Viale, Noorul Wahab, Thomas Walter, Yannick Waumans, Hannah Y. Wen, Wentao Yang, Yinyin Yuan, John Bartlett, Sibylle Loibl, Carsten Denkert, Peter Savas, Sherene Loi, Elisabeth Specht Stovgaard, Roberto Salgado, William M. Gallagher, Arman Rahman^*

^*Corresponding author for this work

Pathology

Research output: Contribution to journal › Review article › peer-review

7 Scopus citations

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.

Original language	English (US)
Pages (from-to)	271-288
Number of pages	18
Journal	Journal of Pathology
Volume	262
Issue number	3
DOIs	https://doi.org/10.1002/path.6238
State	Published - Mar 2024

Funding

GB was funded by the Gilead Breast Cancer Research Grant 2023. JSR\u2010F was funded in part by the Breast Cancer Research Foundation, a Susan G Komen Leadership Grant, and NIH/NCI P50 CA247749 01 grant. SV was supported by Interne Fondsen KU Leuven/Internal Funds KU Leuven. BA received the Swedish Society for Medical Research (Svenska S\u00E4llskapet f\u00F6r Medicinsk Forskning) Postdoctoral Grant and the Swedish Breast Cancer Association (Br\u00F6stcancerf\u00F6rbundet) Research Grant 2021. GC was supported by the Peer Reviewed Cancer Research Program (Award W81XWH\u201021\u20101\u20100160) from the US Department of Defense and the Mayo Clinic Breast Cancer SPORE Grant P50 CA116201 from the NIH. CF\u2010M was funded by the Horizon 2020 European Union research and innovation programme under the Marie Sklodowska Curie grant agreement no. 860627 (CLARIFY Project). SBF: NHMRC GNT1193630. SG was partially supported by NIH Grant CA224319, DK124165, CA263705, and CA196521. AG was supported by Breast Cancer Now (and their legacy charity Breakthrough Breast Cancer) and Cancer Research UK (CRUK/07/012, KCL\u2010BCN\u2010Q3). TRK: Japan Society for the Promotion of Science (JSPS) KAKENHI (21K06909). UK was funded by the Horizon 2020 European Union Research and Innovation Programme under the Marie Sk\u0142odowska\u2010Curie grant agreement no. 860627 (CLARIFY Project). JKL was in part supported by National Institutes of Health (NIH) (R37 CA225655). AM was supported by the National Cancer Institute under award numbers R01CA268287A1, U01CA269181, R01CA26820701A1, R01CA249992\u201001A1, R01CA202752\u201001A1, R01CA208236\u201001A1, R01CA216579\u201001A1, R01CA220581\u201001A1, R01CA257612\u201001A1, 1U01CA239055\u201001, 1U01CA248226\u201001, 1U54CA254566\u201001, National Heart, Lung and Blood Institute 1R01HL15127701A1, R01HL15807101A1, National Institute of Biomedical Imaging and Bioengineering 1R43EB028736\u201001, VA Merit Review Award IBX004121A from the US Department of Veterans Affairs Biomedical Laboratory Research and Development Service the Office of the Assistant Secretary of Defense for Health Affairs, through the Breast Cancer Research Program (W81XWH\u201019\u20101\u20100668), the Prostate Cancer Research Program (W81XWH\u201020\u20101\u20100851), the Lung Cancer Research Program (W81XWH\u201018\u20101\u20100440, W81XWH\u201020\u20101\u20100595), the Peer Reviewed Cancer Research Program (W81XWH\u201018\u20101\u20100404, W81XWH\u201021\u20101\u20100345, W81XWH\u201021\u20101\u20100160), the Kidney Precision Medicine Project (KPMP) Glue Grant and sponsored research agreements from Bristol Myers Squibb, Boehringer\u2010Ingelheim, Eli Lilly and AstraZeneca. SKM thanks Kay Pogue\u2010Geile, Director of Molecular Profiling at NSABP for her constant support and encouragement, Roberto Salgado, for getting me initiated into the wonderful subject of immuno\u2010oncology and its possibilities. FuAM received funding from EPSRC EP/W02909X/1 and PathLAKE consortium. FP\u2010L received research grants from Fondation ARC, La Ligue contre le Cancer. RDP received the Melbourne Research Scholarship and a scholarship from the Peter MacCallum Cancer Centre. JS: UH3CA225021, U24CA215109. ST was supported by Interne Fondsen KU Leuven/Internal Funds KU Leuven. JT was supported by institutional grants of the KWF Kankerbestrijding and the Dutch Ministry of Health, Welfare and Sport. EAT received the Breast Cancer Research Foundation Grant 22\u2010161. GEV was supported by Breast Cancer Now (and their legacy charity Breakthrough Breast Cancer) and Cancer Research UK (CRUK/07/012, KCL\u2010BCN\u2010Q3). TW was supported by the French Government under management of Agence Nationale de la Recherche as part of the \u2018Investissements d'avenir\u2019 program, reference ANR\u201019\u2010P3IA\u20100001 (PRAIRIE 3IA Institute) and by Q\u2010Life (ANR\u201017\u2010CONV\u20100005). HYW was funded in part by the NIH/NCI P50 CA247749 01 grant. YY received funding from Cancer Research UK Career Establishment Award (CRUK C45982/A21808). PS received funding support from the National Health and Medical Research Council, Australia. SL was supported by the National Breast Cancer Foundation of Australia (NBCF) (APP ID: EC\u201017\u2010001), the Breast Cancer Research Foundation, New York (BCRF (APP ID: BCRF\u201021\u2010102), and a National Health and Medical Council of Australia (NHMRC) Investigator Grant (APP ID: 1162318). RS was supported by the Breast Cancer Research Foundation (BCRF, grant no. 17\u2010194). WMG was supported by the North\u2013South Research Programme administered by the Higher Education Authority on behalf of the Department of Further and Higher Education, Research, Innovation and Science and the Shared Island Fund (AICRIstart: A Foundation Stone for the All\u2010Island Cancer Research Institute (AICRI): Building Critical Mass in Precision Cancer Medicine https://www.aicri.org/aicristart ), Irish Cancer Society (Collaborative Cancer Research Centre BREAST\u2010PREDICT; CCRC13GAL; https://www.breastpredict.com ), the Science Foundation Ireland Investigator Programme (OPTi\u2010PREDICT; 15/IA/3104), the Science Foundation Ireland Strategic Partnership Programme (Precision Oncology Ireland; 18/SPP/3522; https://www.precisiononcology.ie ). Open access funding provided by IReL. GB was funded by the Gilead Breast Cancer Research Grant 2023. JSR-F was funded in part by the Breast Cancer Research Foundation, a Susan G Komen Leadership Grant, and NIH/NCI P50 CA247749 01 grant. SV was supported by Interne Fondsen KU Leuven/Internal Funds KU Leuven. BA received the Swedish Society for Medical Research (Svenska S\u00E4llskapet f\u00F6r Medicinsk Forskning) Postdoctoral Grant and the Swedish Breast Cancer Association (Br\u00F6stcancerf\u00F6rbundet) Research Grant 2021. GC was supported by the Peer Reviewed Cancer Research Program (Award W81XWH-21-1-0160) from the US Department of Defense and the Mayo Clinic Breast Cancer SPORE Grant P50 CA116201 from the NIH. CF-M was funded by the Horizon 2020 European Union research and innovation programme under the Marie Sklodowska Curie grant agreement no. 860627 (CLARIFY Project).

Keywords

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

ASJC Scopus subject areas

Pathology and Forensic Medicine

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1002/path.6238

Cite this

Jahangir, C. A., Page, D. B., Broeckx, G., Gonzalez, C. A., Burke, C., Murphy, C., Reis-Filho, J. S., Ly, A., Harms, P. W., Gupta, R. R., Vieth, M., Hida, A. I., Kahila, M., Kos, Z., van Diest, P. J., Verbandt, S., Thagaard, J., Khiroya, R., Abduljabbar, K., ... Rahman, A. (2024). Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer. Journal of Pathology, 262(3), 271-288. https://doi.org/10.1002/path.6238

@article{739f097f0bd0432c89aba0feefc8f750,

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

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.",

keywords = "cancer prognosis, clinical integration, digital image analysis, multiplex imaging, multiplex immunofluorescence, multiplex immunohistochemistry, therapy response, tumour immune profiling, tumour infiltrating lymphocytes",

author = "Jahangir, {Chowdhury Arif} and Page, {David B.} and Glenn Broeckx and Gonzalez, {Claudia A.} and Caoimbhe Burke and Clodagh Murphy and Reis-Filho, {Jorge S.} and Amy Ly and Harms, {Paul W.} and Gupta, {Rajarsi R.} and Michael Vieth and Hida, {Akira I.} and Mohamed Kahila and Zuzana Kos and {van Diest}, {Paul J.} and Sara Verbandt and Jeppe Thagaard and Reena Khiroya and Khalid Abduljabbar and {Acosta Haab}, Gabriela and Balazs Acs and Sylvia Adams and Almeida, {Jonas S.} and Isabel Alvarado-Cabrero and Farid Azmoudeh-Ardalan and Sunil Badve and Baharun, {Nurkhairul Bariyah} and Bellolio, {Enrique R.} and Vydehi Bheemaraju and Blenman, {Kim R.M.} and {Botinelly Mendon{\c c}a Fujimoto}, Luciana and Octavio Burgues and Alexandros Chardas and Cheang, {Maggie Chon U.} and Francesco Ciompi and Cooper, {Lee A.D.} and An Coosemans and Germ{\'a}n Corredor and {Dantas Portela}, {Flavio Luis} and Frederik Deman and Sandra Demaria and Dudgeon, {Sarah N.} and Mahmoud Elghazawy and Claudio Fernandez-Mart{\'i}n and Susan Fineberg and Fox, {Stephen B.} and Giltnane, {Jennifer M.} and Sacha Gnjatic and Gonzalez-Ericsson, {Paula I.} and Anita Grigoriadis and Niels Halama and Hanna, {Matthew G.} and Aparna Harbhajanka and Hart, {Steven N.} and Johan Hartman and Stephen Hewitt and Horlings, {Hugo M.} and Zaheed Husain and Sheeba Irshad and Janssen, {Emiel A.M.} and Kataoka, {Tatsuki R.} and Kosuke Kawaguchi and Khramtsov, {Andrey I.} and Umay Kiraz and Pawan Kirtani and Kodach, {Liudmila L.} and Konstanty Korski and Guray Akturk and Ely Scott and Anik{\'o} Kov{\'a}cs and L{\ae}nkholm, {Anne Vibeke} and Corinna Lang-Schwarz and Denis Larsimont and Lennerz, {Jochen K.} and Marvin Lerousseau and Xiaoxian Li and Anant Madabhushi and Maley, {Sai K.} and {Manur Narasimhamurthy}, Vidya and Marks, {Douglas K.} and McDonald, {Elizabeth S.} and Ravi Mehrotra and Stefan Michiels and Durga Kharidehal and Minhas, {Fayyaz ul Amir Afsar} and Shachi Mittal and Moore, {David A.} and Shamim Mushtaq and Hussain Nighat and Thomas Papathomas and Frederique Penault-Llorca and Perera, {Rashindrie D.} and Pinard, {Christopher J.} and Pinto-Cardenas, {Juan Carlos} and Giancarlo Pruneri and Lajos Pusztai and Rajpoot, {Nasir Mahmood} and Rapoport, {Bernardo Leon} and Rau, {Tilman T.} and Ribeiro, {Joana M.} and David Rimm and Anne Vincent-Salomon and Joel Saltz and Shahin Sayed and Evangelos Hytopoulos and Sarah Mahon and Siziopikou, {Kalliopi P.} and Christos Sotiriou and Albrecht Stenzinger and Sughayer, {Maher A.} and Daniel Sur and Fraser Symmans and Sunao Tanaka and Timothy Taxter and Sabine Tejpar and Jonas Teuwen and Thompson, {E. Aubrey} and Trine Tramm and Tran, {William T.} and {van der Laak}, Jeroen and Verghese, {Gregory E.} and Giuseppe Viale and Noorul Wahab and Thomas Walter and Yannick Waumans and Wen, {Hannah Y.} and Wentao Yang and Yinyin Yuan and John Bartlett and Sibylle Loibl and Carsten Denkert and Peter Savas and Sherene Loi and {Specht Stovgaard}, Elisabeth and Roberto Salgado and Gallagher, {William M.} and Arman Rahman",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.",

year = "2024",

month = mar,

doi = "10.1002/path.6238",

language = "English (US)",

volume = "262",

pages = "271--288",

journal = "Journal of Pathology",

issn = "0022-3417",

publisher = "John Wiley and Sons Ltd",

number = "3",

}

Jahangir, CA, Page, DB, Broeckx, G, Gonzalez, CA, Burke, C, Murphy, C, Reis-Filho, JS, Ly, A, Harms, PW, Gupta, RR, Vieth, M, Hida, AI, Kahila, M, Kos, Z, van Diest, PJ, Verbandt, S, Thagaard, J, Khiroya, R, Abduljabbar, K, Acosta Haab, G, Acs, B, Adams, S, Almeida, JS, Alvarado-Cabrero, I, Azmoudeh-Ardalan, F, Badve, S, Baharun, NB, Bellolio, ER, Bheemaraju, V, Blenman, KRM, Botinelly Mendonça Fujimoto, L, Burgues, O, Chardas, A, Cheang, MCU, Ciompi, F, Cooper, LAD, Coosemans, A, Corredor, G, Dantas Portela, FL, Deman, F, Demaria, S, Dudgeon, SN, Elghazawy, M, Fernandez-Martín, C, Fineberg, S, Fox, SB, Giltnane, JM, Gnjatic, S, Gonzalez-Ericsson, PI, Grigoriadis, A, Halama, N, Hanna, MG, Harbhajanka, A, Hart, SN, Hartman, J, Hewitt, S, Horlings, HM, Husain, Z, Irshad, S, Janssen, EAM, Kataoka, TR, Kawaguchi, K, Khramtsov, AI, Kiraz, U, Kirtani, P, Kodach, LL, Korski, K, Akturk, G, Scott, E, Kovács, A, Lænkholm, AV, Lang-Schwarz, C, Larsimont, D, Lennerz, JK, Lerousseau, M, Li, X, Madabhushi, A, Maley, SK, Manur Narasimhamurthy, V, Marks, DK, McDonald, ES, Mehrotra, R, Michiels, S, Kharidehal, D, Minhas, FUAA, Mittal, S, Moore, DA, Mushtaq, S, Nighat, H, Papathomas, T, Penault-Llorca, F, Perera, RD, Pinard, CJ, Pinto-Cardenas, JC, Pruneri, G, Pusztai, L, Rajpoot, NM, Rapoport, BL, Rau, TT, Ribeiro, JM, Rimm, D, Vincent-Salomon, A, Saltz, J, Sayed, S, Hytopoulos, E, Mahon, S, Siziopikou, KP, Sotiriou, C, Stenzinger, A, Sughayer, MA, Sur, D, Symmans, F, Tanaka, S, Taxter, T, Tejpar, S, Teuwen, J, Thompson, EA, Tramm, T, Tran, WT, van der Laak, J, Verghese, GE, Viale, G, Wahab, N, Walter, T, Waumans, Y, Wen, HY, Yang, W, Yuan, Y, Bartlett, J, Loibl, S, Denkert, C, Savas, P, Loi, S, Specht Stovgaard, E, Salgado, R, Gallagher, WM & Rahman, A 2024, 'Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer', Journal of Pathology, vol. 262, no. 3, pp. 271-288. https://doi.org/10.1002/path.6238

Image-based multiplex immune profiling of cancer tissues: translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer. / Jahangir, Chowdhury Arif; Page, David B.; Broeckx, Glenn et al.
In: Journal of Pathology, Vol. 262, No. 3, 03.2024, p. 271-288.

Research output: Contribution to journal › Review article › peer-review

TY - JOUR

T1 - Image-based multiplex immune profiling of cancer tissues

T2 - translational implications. A report of the International Immuno-oncology Biomarker Working Group on Breast Cancer

AU - Jahangir, Chowdhury Arif

AU - Page, David B.

AU - Broeckx, Glenn

AU - Gonzalez, Claudia A.

AU - Burke, Caoimbhe

AU - Murphy, Clodagh

AU - Reis-Filho, Jorge S.

AU - Ly, Amy

AU - Harms, Paul W.

AU - Gupta, Rajarsi R.

AU - Vieth, Michael

AU - Hida, Akira I.

AU - Kahila, Mohamed

AU - Kos, Zuzana

AU - van Diest, Paul J.

AU - Verbandt, Sara

AU - Thagaard, Jeppe

AU - Khiroya, Reena

AU - Abduljabbar, Khalid

AU - Acosta Haab, Gabriela

AU - Acs, Balazs

AU - Adams, Sylvia

AU - Almeida, Jonas S.

AU - Alvarado-Cabrero, Isabel

AU - Azmoudeh-Ardalan, Farid

AU - Badve, Sunil

AU - Baharun, Nurkhairul Bariyah

AU - Bellolio, Enrique R.

AU - Bheemaraju, Vydehi

AU - Blenman, Kim R.M.

AU - Botinelly Mendonça Fujimoto, Luciana

AU - Burgues, Octavio

AU - Chardas, Alexandros

AU - Cheang, Maggie Chon U.

AU - Ciompi, Francesco

AU - Cooper, Lee A.D.

AU - Coosemans, An

AU - Corredor, Germán

AU - Dantas Portela, Flavio Luis

AU - Deman, Frederik

AU - Demaria, Sandra

AU - Dudgeon, Sarah N.

AU - Elghazawy, Mahmoud

AU - Fernandez-Martín, Claudio

AU - Fineberg, Susan

AU - Fox, Stephen B.

AU - Giltnane, Jennifer M.

AU - Gnjatic, Sacha

AU - Gonzalez-Ericsson, Paula I.

AU - Grigoriadis, Anita

AU - Halama, Niels

AU - Hanna, Matthew G.

AU - Harbhajanka, Aparna

AU - Hart, Steven N.

AU - Hartman, Johan

AU - Hewitt, Stephen

AU - Horlings, Hugo M.

AU - Husain, Zaheed

AU - Irshad, Sheeba

AU - Janssen, Emiel A.M.

AU - Kataoka, Tatsuki R.

AU - Kawaguchi, Kosuke

AU - Khramtsov, Andrey I.

AU - Kiraz, Umay

AU - Kirtani, Pawan

AU - Kodach, Liudmila L.

AU - Korski, Konstanty

AU - Akturk, Guray

AU - Scott, Ely

AU - Kovács, Anikó

AU - Lænkholm, Anne Vibeke

AU - Lang-Schwarz, Corinna

AU - Larsimont, Denis

AU - Lennerz, Jochen K.

AU - Lerousseau, Marvin

AU - Li, Xiaoxian

AU - Madabhushi, Anant

AU - Maley, Sai K.

AU - Manur Narasimhamurthy, Vidya

AU - Marks, Douglas K.

AU - McDonald, Elizabeth S.

AU - Mehrotra, Ravi

AU - Michiels, Stefan

AU - Kharidehal, Durga

AU - Minhas, Fayyaz ul Amir Afsar

AU - Mittal, Shachi

AU - Moore, David A.

AU - Mushtaq, Shamim

AU - Nighat, Hussain

AU - Papathomas, Thomas

AU - Penault-Llorca, Frederique

AU - Perera, Rashindrie D.

AU - Pinard, Christopher J.

AU - Pinto-Cardenas, Juan Carlos

AU - Pruneri, Giancarlo

AU - Pusztai, Lajos

AU - Rajpoot, Nasir Mahmood

AU - Rapoport, Bernardo Leon

AU - Rau, Tilman T.

AU - Ribeiro, Joana M.

AU - Rimm, David

AU - Vincent-Salomon, Anne

AU - Saltz, Joel

AU - Sayed, Shahin

AU - Hytopoulos, Evangelos

AU - Mahon, Sarah

AU - Siziopikou, Kalliopi P.

AU - Sotiriou, Christos

AU - Stenzinger, Albrecht

AU - Sughayer, Maher A.

AU - Sur, Daniel

AU - Symmans, Fraser

AU - Tanaka, Sunao

AU - Taxter, Timothy

AU - Tejpar, Sabine

AU - Teuwen, Jonas

AU - Thompson, E. Aubrey

AU - Tramm, Trine

AU - Tran, William T.

AU - van der Laak, Jeroen

AU - Verghese, Gregory E.

AU - Viale, Giuseppe

AU - Wahab, Noorul

AU - Walter, Thomas

AU - Waumans, Yannick

AU - Wen, Hannah Y.

AU - Yang, Wentao

AU - Yuan, Yinyin

AU - Bartlett, John

AU - Loibl, Sibylle

AU - Denkert, Carsten

AU - Savas, Peter

AU - Loi, Sherene

AU - Specht Stovgaard, Elisabeth

AU - Salgado, Roberto

AU - Gallagher, William M.

AU - Rahman, Arman

PY - 2024/3

Y1 - 2024/3

N2 - 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.

AB - 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.

KW - cancer prognosis

KW - clinical integration

KW - digital image analysis

KW - multiplex imaging

KW - multiplex immunofluorescence

KW - multiplex immunohistochemistry

KW - therapy response

KW - tumour immune profiling

KW - tumour infiltrating lymphocytes

UR - http://www.scopus.com/inward/record.url?scp=85182480446&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85182480446&partnerID=8YFLogxK

U2 - 10.1002/path.6238

DO - 10.1002/path.6238

M3 - Review article

C2 - 38230434

AN - SCOPUS:85182480446

SN - 0022-3417

VL - 262

SP - 271

EP - 288

JO - Journal of Pathology

JF - Journal of Pathology

IS - 3

ER -

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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