Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy

Background: Anthracycline-based neoadjuvant chemotherapy (NAC) may modify tumour immune infiltrate. This study characterized immune infiltrate spatial distribution after NAC in primary high-risk soft tissue sarcomas (STS) and investigate association with prognosis. Methods: The ISG-STS 1001 trial ra...

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Autores: Pasquali, Sandro|||0000-0003-4815-6293, Vallacchi, Viviana|||0000-0002-2819-0630, Lalli, Luca|||0000-0002-4472-628X, Collini, Paola|||0000-0002-6158-210X, Barisella, Marta|||0000-0001-9728-3120, Romagosa, Cleofé, Bagué Rosell, Sílvia|||0000-0001-9980-7231, Coindre, Jean Michel|||0000-0001-8039-6786, Dei Tos, Angelo|||0000-0002-1228-8940, Palmerini, Emanuela|||0000-0003-3406-6705, Quagliuolo, Vittorio, Martín-Broto, Javier|||0000-0001-7350-6916, López Pousa, Antonio, Grignani, Giovanni|||0000-0001-5515-569X, Blay, Jean-Yves|||0000-0001-7190-120X, Diaz Beveridge, Robert, Casiraghi, Elena, Brich, Silvia|||0000-0002-6359-1712, Renne, Salvatore Lorenzo, Bergamaschi, Laura, Vergani, Barbara, Sbaraglia, Marta, Casali, Paolo Giovanni|||0000-0003-4056-8023, Rivoltini, Licia, Stacchiotti, Silvia|||0000-0002-1742-8666, Gronchi, Alessandro|||0000-0002-4703-3534
Tipo de recurso: artículo
Fecha de publicación:2024
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:299788
Acceso en línea:https://ddd.uab.cat/record/299788
https://dx.doi.org/urn:doi:10.1016/j.ebiom.2024.105220
Access Level:acceso abierto
Palabra clave:Anthracycline
Neoadjuvant chemotherapy
Soft tissue sarcomas
Tumour immune microenvironment
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spelling Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapyPasquali, Sandro|||0000-0003-4815-6293Vallacchi, Viviana|||0000-0002-2819-0630Lalli, Luca|||0000-0002-4472-628XCollini, Paola|||0000-0002-6158-210XBarisella, Marta|||0000-0001-9728-3120Romagosa, CleoféBagué Rosell, Sílvia|||0000-0001-9980-7231Coindre, Jean Michel|||0000-0001-8039-6786Dei Tos, Angelo|||0000-0002-1228-8940Palmerini, Emanuela|||0000-0003-3406-6705Quagliuolo, VittorioMartín-Broto, Javier|||0000-0001-7350-6916López Pousa, AntonioGrignani, Giovanni|||0000-0001-5515-569XBlay, Jean-Yves|||0000-0001-7190-120XDiaz Beveridge, RobertCasiraghi, ElenaBrich, Silvia|||0000-0002-6359-1712Renne, Salvatore LorenzoBergamaschi, LauraVergani, BarbaraSbaraglia, MartaCasali, Paolo Giovanni|||0000-0003-4056-8023Rivoltini, LiciaStacchiotti, Silvia|||0000-0002-1742-8666Gronchi, Alessandro|||0000-0002-4703-3534AnthracyclineNeoadjuvant chemotherapySoft tissue sarcomasTumour immune microenvironmentBackground: Anthracycline-based neoadjuvant chemotherapy (NAC) may modify tumour immune infiltrate. This study characterized immune infiltrate spatial distribution after NAC in primary high-risk soft tissue sarcomas (STS) and investigate association with prognosis. Methods: The ISG-STS 1001 trial randomized STS patients to anthracycline plus ifosfamide (AI) or a histology-tailored (HT) NAC. Four areas of tumour specimens were sampled: the area showing the highest lymphocyte infiltrate (HI) at H&E; the area with lack of post-treatment changes (highest grade, HG); the area with post-treatment changes (lowest grade, LG); and the tumour edge (TE). CD3, CD8, PD-1, CD20, FOXP3, and CD163 were analyzed at immunohistochemistry and digital pathology. A machine learning method was used to generate sarcoma immune index scores (SIS) that predict patient disease-free and overall survival (DFS and OS). Findings: Tumour infiltrating lymphocytes and PD-1+ cells together with CD163+ cells were more represented in STS histologies with complex compared to simple karyotype, while CD20+ B-cells were detected in both these histology groups. PD-1+ cells exerted a negative prognostic value irrespectively of their spatial distribution. Enrichment in CD20+ B-cells at HI and TE areas was associated with better patient outcomes. We generated a prognostic SIS for each tumour area, having the HI-SIS the best performance. Such prognostic value was driven by treatment with AI. Interpretation: The different spatial distribution of immune populations and their different association with prognosis support NAC as a modifier of tumour immune infiltrate in STS.Universitat Autònoma de Barcelona 22024-01-0120242024-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/299788https://dx.doi.org/urn:doi:10.1016/j.ebiom.2024.105220reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengopen accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, sempre que no sigui amb finalitats comercials, i sempre que es reconegui l'autoria de l'obra original.https://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:2997882026-06-06T12:50:31Z
dc.title.none.fl_str_mv Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
title Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
spellingShingle Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
Pasquali, Sandro|||0000-0003-4815-6293
Anthracycline
Neoadjuvant chemotherapy
Soft tissue sarcomas
Tumour immune microenvironment
title_short Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
title_full Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
title_fullStr Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
title_full_unstemmed Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
title_sort Spatial distribution of tumour immune infiltrate predicts outcomes of patients with high-risk soft tissue sarcomas after neoadjuvant chemotherapy
dc.creator.none.fl_str_mv Pasquali, Sandro|||0000-0003-4815-6293
Vallacchi, Viviana|||0000-0002-2819-0630
Lalli, Luca|||0000-0002-4472-628X
Collini, Paola|||0000-0002-6158-210X
Barisella, Marta|||0000-0001-9728-3120
Romagosa, Cleofé
Bagué Rosell, Sílvia|||0000-0001-9980-7231
Coindre, Jean Michel|||0000-0001-8039-6786
Dei Tos, Angelo|||0000-0002-1228-8940
Palmerini, Emanuela|||0000-0003-3406-6705
Quagliuolo, Vittorio
Martín-Broto, Javier|||0000-0001-7350-6916
López Pousa, Antonio
Grignani, Giovanni|||0000-0001-5515-569X
Blay, Jean-Yves|||0000-0001-7190-120X
Diaz Beveridge, Robert
Casiraghi, Elena
Brich, Silvia|||0000-0002-6359-1712
Renne, Salvatore Lorenzo
Bergamaschi, Laura
Vergani, Barbara
Sbaraglia, Marta
Casali, Paolo Giovanni|||0000-0003-4056-8023
Rivoltini, Licia
Stacchiotti, Silvia|||0000-0002-1742-8666
Gronchi, Alessandro|||0000-0002-4703-3534
author Pasquali, Sandro|||0000-0003-4815-6293
author_facet Pasquali, Sandro|||0000-0003-4815-6293
Vallacchi, Viviana|||0000-0002-2819-0630
Lalli, Luca|||0000-0002-4472-628X
Collini, Paola|||0000-0002-6158-210X
Barisella, Marta|||0000-0001-9728-3120
Romagosa, Cleofé
Bagué Rosell, Sílvia|||0000-0001-9980-7231
Coindre, Jean Michel|||0000-0001-8039-6786
Dei Tos, Angelo|||0000-0002-1228-8940
Palmerini, Emanuela|||0000-0003-3406-6705
Quagliuolo, Vittorio
Martín-Broto, Javier|||0000-0001-7350-6916
López Pousa, Antonio
Grignani, Giovanni|||0000-0001-5515-569X
Blay, Jean-Yves|||0000-0001-7190-120X
Diaz Beveridge, Robert
Casiraghi, Elena
Brich, Silvia|||0000-0002-6359-1712
Renne, Salvatore Lorenzo
Bergamaschi, Laura
Vergani, Barbara
Sbaraglia, Marta
Casali, Paolo Giovanni|||0000-0003-4056-8023
Rivoltini, Licia
Stacchiotti, Silvia|||0000-0002-1742-8666
Gronchi, Alessandro|||0000-0002-4703-3534
author_role author
author2 Vallacchi, Viviana|||0000-0002-2819-0630
Lalli, Luca|||0000-0002-4472-628X
Collini, Paola|||0000-0002-6158-210X
Barisella, Marta|||0000-0001-9728-3120
Romagosa, Cleofé
Bagué Rosell, Sílvia|||0000-0001-9980-7231
Coindre, Jean Michel|||0000-0001-8039-6786
Dei Tos, Angelo|||0000-0002-1228-8940
Palmerini, Emanuela|||0000-0003-3406-6705
Quagliuolo, Vittorio
Martín-Broto, Javier|||0000-0001-7350-6916
López Pousa, Antonio
Grignani, Giovanni|||0000-0001-5515-569X
Blay, Jean-Yves|||0000-0001-7190-120X
Diaz Beveridge, Robert
Casiraghi, Elena
Brich, Silvia|||0000-0002-6359-1712
Renne, Salvatore Lorenzo
Bergamaschi, Laura
Vergani, Barbara
Sbaraglia, Marta
Casali, Paolo Giovanni|||0000-0003-4056-8023
Rivoltini, Licia
Stacchiotti, Silvia|||0000-0002-1742-8666
Gronchi, Alessandro|||0000-0002-4703-3534
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universitat Autònoma de Barcelona
dc.subject.none.fl_str_mv Anthracycline
Neoadjuvant chemotherapy
Soft tissue sarcomas
Tumour immune microenvironment
topic Anthracycline
Neoadjuvant chemotherapy
Soft tissue sarcomas
Tumour immune microenvironment
description Background: Anthracycline-based neoadjuvant chemotherapy (NAC) may modify tumour immune infiltrate. This study characterized immune infiltrate spatial distribution after NAC in primary high-risk soft tissue sarcomas (STS) and investigate association with prognosis. Methods: The ISG-STS 1001 trial randomized STS patients to anthracycline plus ifosfamide (AI) or a histology-tailored (HT) NAC. Four areas of tumour specimens were sampled: the area showing the highest lymphocyte infiltrate (HI) at H&E; the area with lack of post-treatment changes (highest grade, HG); the area with post-treatment changes (lowest grade, LG); and the tumour edge (TE). CD3, CD8, PD-1, CD20, FOXP3, and CD163 were analyzed at immunohistochemistry and digital pathology. A machine learning method was used to generate sarcoma immune index scores (SIS) that predict patient disease-free and overall survival (DFS and OS). Findings: Tumour infiltrating lymphocytes and PD-1+ cells together with CD163+ cells were more represented in STS histologies with complex compared to simple karyotype, while CD20+ B-cells were detected in both these histology groups. PD-1+ cells exerted a negative prognostic value irrespectively of their spatial distribution. Enrichment in CD20+ B-cells at HI and TE areas was associated with better patient outcomes. We generated a prognostic SIS for each tumour area, having the HI-SIS the best performance. Such prognostic value was driven by treatment with AI. Interpretation: The different spatial distribution of immune populations and their different association with prognosis support NAC as a modifier of tumour immune infiltrate in STS.
publishDate 2024
dc.date.none.fl_str_mv 2
2024-01-01
2024
2024-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/299788
https://dx.doi.org/urn:doi:10.1016/j.ebiom.2024.105220
url https://ddd.uab.cat/record/299788
https://dx.doi.org/urn:doi:10.1016/j.ebiom.2024.105220
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by-nc/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
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repository.mail.fl_str_mv
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