Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients

Abstract Changes in the oral microbiome, particularly Fusobacterium nucleatum, are associated with oral squamous cell carcinoma (OSCC). F. nucleatum has been reported to modulate local immunity in cancers. We aimed to assess the association between intratumoral F. nucleatum and clinico-pathological...

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Autores principales:	Cindy Neuzillet, Manon Marchais, Sophie Vacher, Marc Hilmi, Anne Schnitzler, Didier Meseure, Renaud Leclere, Charlotte Lecerf, Coraline Dubot, Emmanuelle Jeannot, Jerzy Klijanienko, Odette Mariani, Valentin Calugaru, Caroline Hoffmann, Maria Lesnik, Nathalie Badois, Edith Borcoman, Eliane Piaggio, Maud Kamal, Christophe Le Tourneau, Ivan Bieche
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/cc1d246718cc4eb6b4c35b1ab82d6872
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spelling	oai:doaj.org-article:cc1d246718cc4eb6b4c35b1ab82d68722021-12-02T14:26:13ZPrognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients10.1038/s41598-021-86816-92045-2322https://doaj.org/article/cc1d246718cc4eb6b4c35b1ab82d68722021-04-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-86816-9https://doaj.org/toc/2045-2322Abstract Changes in the oral microbiome, particularly Fusobacterium nucleatum, are associated with oral squamous cell carcinoma (OSCC). F. nucleatum has been reported to modulate local immunity in cancers. We aimed to assess the association between intratumoral F. nucleatum and clinico-pathological features, relapse, and overall survival (OS) in two independent cohorts of patients with OSCC, and to explore the interplay with immune-related genes. We retrospectively analyzed tissue samples from a first cohort of 122 patients with head and neck squamous cell carcinoma, including 61 OSCC (cohort #1), and a second cohort of 90 additional OSCC (cohort #2). We then performed a sensitivity analysis on the merged cohort of OSCC patients (N = 151). F. nucleatum 16S rRNA gene sequences were quantified using real-time quantitative PCR. The presence of gram-negative bacteria and macrophages was confirmed by LPS and CD163 immunostainings, respectively. F. nucleatum positivity was associated with older age, less alcohol and combined alcohol plus tobacco consumption, and less frequent lymph node invasion. There was a trend for a lower recurrence rate in F. nucleatum-positive cases, with less metastatic relapses compared to F. nucleatum-negative tumors, and significantly longer OS, relapse-free and metastasis-free survival. F. nucleatum status was independently associated with OS in multivariate analysis. Immune-related gene and immunohistochemistry analyses showed that gram-negative bacteria load inversely correlated with M2 macrophages. F. nucleatum-associated OSCC has a specific immune microenvironment, is more frequent in older, non-drinking patients, and associated with a favorable prognosis.Cindy NeuzilletManon MarchaisSophie VacherMarc HilmiAnne SchnitzlerDidier MeseureRenaud LeclereCharlotte LecerfCoraline DubotEmmanuelle JeannotJerzy KlijanienkoOdette MarianiValentin CalugaruCaroline HoffmannMaria LesnikNathalie BadoisEdith BorcomanEliane PiaggioMaud KamalChristophe Le TourneauIvan BiecheNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-13 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Cindy Neuzillet Manon Marchais Sophie Vacher Marc Hilmi Anne Schnitzler Didier Meseure Renaud Leclere Charlotte Lecerf Coraline Dubot Emmanuelle Jeannot Jerzy Klijanienko Odette Mariani Valentin Calugaru Caroline Hoffmann Maria Lesnik Nathalie Badois Edith Borcoman Eliane Piaggio Maud Kamal Christophe Le Tourneau Ivan Bieche Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
description	Abstract Changes in the oral microbiome, particularly Fusobacterium nucleatum, are associated with oral squamous cell carcinoma (OSCC). F. nucleatum has been reported to modulate local immunity in cancers. We aimed to assess the association between intratumoral F. nucleatum and clinico-pathological features, relapse, and overall survival (OS) in two independent cohorts of patients with OSCC, and to explore the interplay with immune-related genes. We retrospectively analyzed tissue samples from a first cohort of 122 patients with head and neck squamous cell carcinoma, including 61 OSCC (cohort #1), and a second cohort of 90 additional OSCC (cohort #2). We then performed a sensitivity analysis on the merged cohort of OSCC patients (N = 151). F. nucleatum 16S rRNA gene sequences were quantified using real-time quantitative PCR. The presence of gram-negative bacteria and macrophages was confirmed by LPS and CD163 immunostainings, respectively. F. nucleatum positivity was associated with older age, less alcohol and combined alcohol plus tobacco consumption, and less frequent lymph node invasion. There was a trend for a lower recurrence rate in F. nucleatum-positive cases, with less metastatic relapses compared to F. nucleatum-negative tumors, and significantly longer OS, relapse-free and metastasis-free survival. F. nucleatum status was independently associated with OS in multivariate analysis. Immune-related gene and immunohistochemistry analyses showed that gram-negative bacteria load inversely correlated with M2 macrophages. F. nucleatum-associated OSCC has a specific immune microenvironment, is more frequent in older, non-drinking patients, and associated with a favorable prognosis.
format	article
author	Cindy Neuzillet Manon Marchais Sophie Vacher Marc Hilmi Anne Schnitzler Didier Meseure Renaud Leclere Charlotte Lecerf Coraline Dubot Emmanuelle Jeannot Jerzy Klijanienko Odette Mariani Valentin Calugaru Caroline Hoffmann Maria Lesnik Nathalie Badois Edith Borcoman Eliane Piaggio Maud Kamal Christophe Le Tourneau Ivan Bieche
author_facet	Cindy Neuzillet Manon Marchais Sophie Vacher Marc Hilmi Anne Schnitzler Didier Meseure Renaud Leclere Charlotte Lecerf Coraline Dubot Emmanuelle Jeannot Jerzy Klijanienko Odette Mariani Valentin Calugaru Caroline Hoffmann Maria Lesnik Nathalie Badois Edith Borcoman Eliane Piaggio Maud Kamal Christophe Le Tourneau Ivan Bieche
author_sort	Cindy Neuzillet
title	Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
title_short	Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
title_full	Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
title_fullStr	Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
title_full_unstemmed	Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
title_sort	prognostic value of intratumoral fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/cc1d246718cc4eb6b4c35b1ab82d6872
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Prognostic value of intratumoral Fusobacterium nucleatum and association with immune-related gene expression in oral squamous cell carcinoma patients

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