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

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 immun...

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Published in:The Journal of pathology Vol. 262; no. 3; pp. 271 - 288
Main Authors: Jahangir, Chowdhury Arif, Page, David B, Broeckx, Glenn, Gonzalez, Claudia A, Burke, Caoimbhe, Reis‐Filho, Jorge S, Ly, Amy, Harms, Paul W, Vieth, Michael, Kos, Zuzana, Diest, Paul J, Thagaard, Jeppe, Khiroya, Reena, Acosta Haab, Gabriela, Acs, Balazs, Adams, Sylvia, Almeida, Jonas S, Alvarado‐Cabrero, Isabel, Azmoudeh‐Ardalan, Farid, Badve, Sunil, Baharun, Nurkhairul Bariyah, Bellolio, Enrique R, Blenman, Kim RM, Cheang, Maggie Chon U, Ciompi, Francesco, Cooper, Lee AD, Coosemans, An, Corredor, Germán, Dantas Portela, Flavio Luis, Demaria, Sandra, Dudgeon, Sarah N, Elghazawy, Mahmoud, Fernandez‐Martín, Claudio, Fineberg, Susan, Fox, Stephen B, Giltnane, Jennifer M, Gnjatic, Sacha, Grigoriadis, Anita, Hanna, Matthew G, Harbhajanka, Aparna, Hart, Steven N, Hartman, Johan, Hewitt, Stephen, Irshad, Sheeba, Janssen, Emiel AM, Kataoka, Tatsuki R, Kawaguchi, Kosuke, Khramtsov, Andrey I, Kiraz, Umay, Kirtani, Pawan, Kodach, Liudmila L, Korski, Konstanty, Akturk, Guray, Scott, Ely, Lænkholm, Anne‐Vibeke, Lennerz, Jochen K, Lerousseau, Marvin, Li, Xiaoxian, Maley, Sai K, Manur Narasimhamurthy, Vidya, Marks, Douglas K, Mehrotra, Ravi, Michiels, Stefan, Minhas, Fayyaz ul Amir Afsar, Moore, David A, Mushtaq, Shamim, Nighat, Hussain, Papathomas, Thomas, Penault‐Llorca, Frederique, Pinard, Christopher J, Pinto‐Cardenas, Juan Carlos, Pruneri, Giancarlo, Rau, Tilman T, Rimm, David, Vincent‐Salomon, Anne, Saltz, Joel, Sayed, Shahin, Hytopoulos, Evangelos, Sotiriou, Christos, Sur, Daniel, Tanaka, Sunao, Taxter, Timothy, Tejpar, Sabine, Teuwen, Jonas, Thompson, E Aubrey, Tramm, Trine, Tran, William T, Laak, Jeroen, Verghese, Gregory E, Viale, Giuseppe, Wahab, Noorul, Walter, Thomas, Wen, Hannah Y, Bartlett, John, Loibl, Sibylle, Denkert, Carsten, Savas, Peter, Loi, Sherene, Specht Stovgaard, Elisabeth, Rahman, Arman
Format: Journal Article
Language:English
Published: Chichester, UK John Wiley & Sons, Ltd 01.03.2024
Wiley Subscription Services, Inc
Wiley
Subjects:
Biomarkers
Breast cancer
Cancer
cancer prognosis
clinical integration
digital image analysis
Humanities and Social Sciences
Immunofluorescence
Immunohistochemistry
Life Sciences
Methodology
Methods and statistics
multiplex imaging
multiplex immunofluorescence
multiplex immunohistochemistry
Oncology
Other Statistics
Pathology
Phenotypes
Statistics
therapy response
Translation
Tumor microenvironment
Tumors
tumour immune profiling
tumour infiltrating lymphocytes
multiplex immunohistochemistry
tumour infiltrating lymphocytes
multiplex immunofluorescence
therapy response
multiplex imaging
cancer prognosis
digital image analysis
clinical integration
tumour immune profiling
ISSN:0022-3417, 1096-9896, 1096-9896
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Summary: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.
Bibliography: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
and has received personal/consultancy fees from Goldman Sachs, Bain Capital, REPARE Therapeutics, Saga Diagnostics, and Paige.AI, membership of the scientific advisory boards of VolitionRx, REPARE Therapeutics, and Paige.AI, 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 (WO2012038068A2). MGH: Consultant for Paige.AI, 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‐Ingelheim, 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, MIM 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, Illumina, 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, Illumina, 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 Ellogon.AI 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, G1 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.
The Journal of Pathology
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PMCID: PMC11288342
CAJ, AR, and WMG conceptualised, developed the methodology and wrote the original draft. DBP was also involved in writing. AR, WMG, and RS were responsible for conceptualising, designing, editing the article and supervising. All remaining authors have provided critical revisions and agreed to publish the final version of the manuscript.
Author contributions statement
ISSN:0022-3417
1096-9896
1096-9896
DOI:10.1002/path.6238