Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)

Mycobacterium bovis (M. bovis) is the primary agent of bovine tuberculosis (TB) in Mediterranean buffalo, which has a negative economic impact on buffalo herds. Improving TB diagnostic performance in this species represents a key step to eradicate efficiently this disease. We have recently shown the...

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Main Authors: Giulia Franzoni, Federica Signorelli, Piera Mazzone, Anna Donniacuo, Giovanna De Matteis, Francesco Grandoni, Lorena Schiavo, Susanna Zinellu, Silvia Dei Giudici, Javier Bezos, Esterina De Carlo, Giorgio Galiero, Francesco Napolitano, Alessandra Martucciello
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Veterinary Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2024.1512571/full
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author Giulia Franzoni
Federica Signorelli
Piera Mazzone
Anna Donniacuo
Giovanna De Matteis
Francesco Grandoni
Lorena Schiavo
Susanna Zinellu
Silvia Dei Giudici
Javier Bezos
Javier Bezos
Esterina De Carlo
Giorgio Galiero
Francesco Napolitano
Alessandra Martucciello
author_facet Giulia Franzoni
Federica Signorelli
Piera Mazzone
Anna Donniacuo
Giovanna De Matteis
Francesco Grandoni
Lorena Schiavo
Susanna Zinellu
Silvia Dei Giudici
Javier Bezos
Javier Bezos
Esterina De Carlo
Giorgio Galiero
Francesco Napolitano
Alessandra Martucciello
author_sort Giulia Franzoni
collection DOAJ
description Mycobacterium bovis (M. bovis) is the primary agent of bovine tuberculosis (TB) in Mediterranean buffalo, which has a negative economic impact on buffalo herds. Improving TB diagnostic performance in this species represents a key step to eradicate efficiently this disease. We have recently shown the utility of the IFN-γ assay in the diagnosis of M. bovis infection in Mediterranean buffaloes (Bubalus bubalis), but other cytokines might be useful immunological biomarkers of this infection. We therefore investigated the utility of key immune cytokines as diagnostic biomarkers of M. bovis infection in this species. Thirty-six Italian Mediterranean buffaloes were used in this study: healthy animals (N = 11), infected (IFN-γ test positive, no post-mortem lesions, no M. bovis detection; N = 14), and affected (IFN-γ test positive, visible post-mortem lesions; N = 11). Heparin blood samples were stimulated with bovine purified protein derivative (PPD-B), alongside controls, and 18–24 h later plasma were collected. Levels of 14 key cytokines were measured: IFN-γ, IL-17, IL-4, IL-10, TNF, IL-1α, IL-1β, IL-6, IP-10, MIP-1α, MIP-1β, MCP-1, IL-36Ra, and VEGF-A. We observed that both infected and affected animals released higher levels of IFN-γ, IL-17, IL-10, TNF, IL-1α, IL-6, MIP-1β, in response to PPD-B compared to healthy subjects. Mycobacterium bovis infected animals released also higher levels of IL-1β and IP-10 in response to PPD-B compared to healthy subjects, whereas only tendencies were detected in affected animals. Affected animals only released MIP-1α in response to PPD-B compared to healthy subjects and in this group higher values of PPD-B specific TNF was also observed. Finally, canonical discriminant analysis (CDA) was used to generate predictive cytokine profiles by groups. Our data suggest that IL-10, TNF, IL-1α, IL-6, MIP-1β could be useful biomarkers of TB in Mediterranean Buffalo and can improve the TB diagnostic performance in this specie.
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spelling doaj-art-b1853ad5f4ca49bfa1c79f0b2c4045822025-08-20T02:00:06ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692024-12-011110.3389/fvets.2024.15125711512571Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)Giulia Franzoni0Federica Signorelli1Piera Mazzone2Anna Donniacuo3Giovanna De Matteis4Francesco Grandoni5Lorena Schiavo6Susanna Zinellu7Silvia Dei Giudici8Javier Bezos9Javier Bezos10Esterina De Carlo11Giorgio Galiero12Francesco Napolitano13Alessandra Martucciello14Department of Animal Health, Istituto Zooprofilattico Sperimentale della Sardegna, Sassari, ItalyCREA-Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di ricerca Zootecnia e Acquacoltura (Research Centre for Animal Production and Aquaculture), Monterotondo (RM), ItalyIstituto Zooprofilattico Sperimentale dell’Umbria e delle Marche “Togo Rosati”, Perugia, ItalyNational Reference Centre for Hygiene and Technologies of Mediterranean Buffalo Farming and Productions, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Salerno, ItalyCREA-Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di ricerca Zootecnia e Acquacoltura (Research Centre for Animal Production and Aquaculture), Monterotondo (RM), ItalyCREA-Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di ricerca Zootecnia e Acquacoltura (Research Centre for Animal Production and Aquaculture), Monterotondo (RM), ItalyNational Reference Centre for Hygiene and Technologies of Mediterranean Buffalo Farming and Productions, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Salerno, ItalyDepartment of Animal Health, Istituto Zooprofilattico Sperimentale della Sardegna, Sassari, ItalyDepartment of Animal Health, Istituto Zooprofilattico Sperimentale della Sardegna, Sassari, ItalyVISAVET Health Surveillance Centre, Complutense University of Madrid, Madrid, SpainFacultad de Veterinaria, Departamento de Sanidad Animal, Universidad Complutense de Madrid, Madrid, SpainNational Reference Centre for Hygiene and Technologies of Mediterranean Buffalo Farming and Productions, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Salerno, ItalyNational Reference Centre for Hygiene and Technologies of Mediterranean Buffalo Farming and Productions, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Salerno, ItalyCREA-Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di ricerca Zootecnia e Acquacoltura (Research Centre for Animal Production and Aquaculture), Monterotondo (RM), ItalyNational Reference Centre for Hygiene and Technologies of Mediterranean Buffalo Farming and Productions, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Salerno, ItalyMycobacterium bovis (M. bovis) is the primary agent of bovine tuberculosis (TB) in Mediterranean buffalo, which has a negative economic impact on buffalo herds. Improving TB diagnostic performance in this species represents a key step to eradicate efficiently this disease. We have recently shown the utility of the IFN-γ assay in the diagnosis of M. bovis infection in Mediterranean buffaloes (Bubalus bubalis), but other cytokines might be useful immunological biomarkers of this infection. We therefore investigated the utility of key immune cytokines as diagnostic biomarkers of M. bovis infection in this species. Thirty-six Italian Mediterranean buffaloes were used in this study: healthy animals (N = 11), infected (IFN-γ test positive, no post-mortem lesions, no M. bovis detection; N = 14), and affected (IFN-γ test positive, visible post-mortem lesions; N = 11). Heparin blood samples were stimulated with bovine purified protein derivative (PPD-B), alongside controls, and 18–24 h later plasma were collected. Levels of 14 key cytokines were measured: IFN-γ, IL-17, IL-4, IL-10, TNF, IL-1α, IL-1β, IL-6, IP-10, MIP-1α, MIP-1β, MCP-1, IL-36Ra, and VEGF-A. We observed that both infected and affected animals released higher levels of IFN-γ, IL-17, IL-10, TNF, IL-1α, IL-6, MIP-1β, in response to PPD-B compared to healthy subjects. Mycobacterium bovis infected animals released also higher levels of IL-1β and IP-10 in response to PPD-B compared to healthy subjects, whereas only tendencies were detected in affected animals. Affected animals only released MIP-1α in response to PPD-B compared to healthy subjects and in this group higher values of PPD-B specific TNF was also observed. Finally, canonical discriminant analysis (CDA) was used to generate predictive cytokine profiles by groups. Our data suggest that IL-10, TNF, IL-1α, IL-6, MIP-1β could be useful biomarkers of TB in Mediterranean Buffalo and can improve the TB diagnostic performance in this specie.https://www.frontiersin.org/articles/10.3389/fvets.2024.1512571/fullMycobacterium bovisbiomarkersinterleukinschemokinesMediterranean buffaloes
spellingShingle Giulia Franzoni
Federica Signorelli
Piera Mazzone
Anna Donniacuo
Giovanna De Matteis
Francesco Grandoni
Lorena Schiavo
Susanna Zinellu
Silvia Dei Giudici
Javier Bezos
Javier Bezos
Esterina De Carlo
Giorgio Galiero
Francesco Napolitano
Alessandra Martucciello
Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)
Frontiers in Veterinary Science
Mycobacterium bovis
biomarkers
interleukins
chemokines
Mediterranean buffaloes
title Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)
title_full Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)
title_fullStr Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)
title_full_unstemmed Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)
title_short Cytokines as potential biomarkers for the diagnosis of Mycobacterium bovis infection in Mediterranean buffaloes (Bubalus bubalis)
title_sort cytokines as potential biomarkers for the diagnosis of mycobacterium bovis infection in mediterranean buffaloes bubalus bubalis
topic Mycobacterium bovis
biomarkers
interleukins
chemokines
Mediterranean buffaloes
url https://www.frontiersin.org/articles/10.3389/fvets.2024.1512571/full
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