Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar

David Risco; Emmanuel Serrano; Pedro Fernández-Llario; Jesús M. Cuesta; Pilar Gonçalves; Waldo L. Garcia-Jiménez; Remigio Martinez; Rosario Cerrato; Roser Velarde; Luis Gómez; Joaquim Segalés; Javier Hermoso De Mendoza

doi:10.1371/journal.pone.0110123

Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar

David Risco, Emmanuel Serrano, Pedro Fernández-Llario, Jesús M. Cuesta, Pilar Gonçalves, Waldo L. Garcia-Jiménez, Remigio Martinez, Rosario Cerrato, Roser Velarde, Luis Gómez, Joaquim Segalés, Javier Hermoso De Mendoza

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Resum

Les coinfeccions amb paràsits o virus impulsen la dinàmica de la tuberculosi en humans, però se sap poc sobre els seus efectes en altres hostes no humans. Aquest treball pretén investigar la relació entre la infecció per Mycobacterium bovis i altres patògens en senglars (Sus scrofa), un reservori reconegut de tuberculosi bovina (bTB) en ecosistemes mediterranis. Per a això, s'ha avaluat si els contactes amb patògens concomitants comuns estan associats al desenvolupament de lesions greus per TBB en 165 senglars del mig oest d'Espanya. S'ha avaluat la presència de lesions per TBB que afecten només una localització anatòmica (ganglis limfàtics cervicals), o patrons més severs que afecten més d'una localització (principalment ganglis limfàtics cervicals i pulmons) en animals infectats. A més, s'ha avaluat l'existència de contactes amb altres patògens com ara el circovirus porcí tipus 2 (PCV2), la malaltia d'Aujeszky (ADV), el virus de la grip porcina, el virus del síndrome reproductiu i respiratori porcí (PRRSV), Mycoplasma hyopneumoniae, Actinobacillus pleuropneumoniae, Haemophilus parasuis i Metastrongylus spp. mitjançant tècniques serològiques, microbiològiques i parasitològiques. L'existència de contactes amb una comunitat estructurada de patògens en senglars infectats per M. bovis s'ha investigat estadísticament mitjançant models nuls. S'ha examinat l'associació entre aquesta comunitat de patògens i la gravetat de la TBB utilitzant un enfocament de regressió parcial dels mínims quadrats. Els resultats han mostrat que els senglars adults infectats per M. bovis havien contactat amb algunes combinacions específiques, no aleatòries, de patògens. El contacte amb PCV2, ADV i infeccions per Metastrongylus spp s'ha correlacionat positivament amb la gravetat de la tuberculosi. Per tant, les mesures contra aquests patògens concomitants com ara vacunació o desparasitacions podrien ser d'utilitat en els programes de control de la tuberculosi en senglars. No obstant això, donades les conseqüències inesperades que pot tenir alterar qualsevol comunitat d'organismes, s'hauria d'avaluar l'impacte d'aquestes mesures sota condicions controlades. A més, es necessita una investigació addicional incloent altres patògens importants com els nematodes gastrointestinals per completar aquest quadre. © 2014 Risco et al

Idioma original	Anglès
Número d’article	e110123
Revista	PLoS ONE
Volum	9
Número	10
DOIs	https://doi.org/10.1371/journal.pone.0110123
Estat de la publicació	Publicada - 28 d’oct. 2014

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Risco, D., Serrano, E., Fernández-Llario, P., Cuesta, J. M., Gonçalves, P., Garcia-Jiménez, W. L., Martinez, R., Cerrato, R., Velarde, R., Gómez, L., Segalés, J., & De Mendoza, J. H. (2014). Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar. PLoS ONE, 9(10), Article e110123. https://doi.org/10.1371/journal.pone.0110123

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title = "Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar",

abstract = "{\textcopyright} 2014 Risco et al. Co-infections with parasites or viruses drive tuberculosis dynamics in humans, but little is known about their effects in other non-human hosts. This work aims to investigate the relationship between Mycobacterium bovis infection and other pathogens in wild boar (Sus scrofa), a recognized reservoir of bovine tuberculosis (bTB) in Mediterranean ecosystems. For this purpose, it has been assessed whether contacts with common concomitant pathogens are associated with the development of severe bTB lesions in 165 wild boar from mid-western Spain. The presence of bTB lesions affecting only one anatomic location (cervical lymph nodes), or more severe patterns affecting more than one location (mainly cervical lymph nodes and lungs), was assessed in infected animals. In addition, the existence of contacts with other pathogens such as porcine circovirus type 2 (PCV2), Aujeszky's disease virus (ADV), swine influenza virus, porcine reproductive and respiratory syndrome virus, Mycoplasma hyopneumoniae, Actinobacillus pleuropneumoniae, Haemophilus parasuis and Metastrongylus spp, was evaluated by means of serological, microbiological and parasitological techniques. The existence of contacts with a structured community of pathogens in wild boar infected by M. bovis was statistically investigated by null models. Association between this community of pathogens and bTB severity was examined using a Partial Least Squares regression approach. Results showed that adult wild boar infected by M. bovis had contacted with some specific, non-random pathogen combinations. Contact with PCV2, ADV and infection by Metastrongylus spp, was positively correlated to tuberculosis severity. Therefore, measures against these concomitant pathogens such as vaccination or deworming, might be useful in tuberculosis control programmes in the wild boar. However, given the unexpected consequences of altering any community of organisms, further research should evaluate the impact of such measures under controlled conditions. Furthermore, more research including other important pathogens, such as gastro-intestinal nematodes, will be necessary to complete this picture.",

author = "David Risco and Emmanuel Serrano and Pedro Fern{\'a}ndez-Llario and Cuesta, \{Jes{\'u}s M.\} and Pilar Gon{\c c}alves and Garcia-Jim{\'e}nez, \{Waldo L.\} and Remigio Martinez and Rosario Cerrato and Roser Velarde and Luis G{\'o}mez and Joaquim Segal{\'e}s and \{De Mendoza\}, \{Javier Hermoso\}",

year = "2014",

month = oct,

day = "28",

doi = "10.1371/journal.pone.0110123",

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volume = "9",

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TY - JOUR

T1 - Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar

AU - Risco, David

AU - Serrano, Emmanuel

AU - Fernández-Llario, Pedro

AU - Cuesta, Jesús M.

AU - Gonçalves, Pilar

AU - Garcia-Jiménez, Waldo L.

AU - Martinez, Remigio

AU - Cerrato, Rosario

AU - Velarde, Roser

AU - Gómez, Luis

AU - Segalés, Joaquim

AU - De Mendoza, Javier Hermoso

PY - 2014/10/28

Y1 - 2014/10/28

N2 - © 2014 Risco et al. Co-infections with parasites or viruses drive tuberculosis dynamics in humans, but little is known about their effects in other non-human hosts. This work aims to investigate the relationship between Mycobacterium bovis infection and other pathogens in wild boar (Sus scrofa), a recognized reservoir of bovine tuberculosis (bTB) in Mediterranean ecosystems. For this purpose, it has been assessed whether contacts with common concomitant pathogens are associated with the development of severe bTB lesions in 165 wild boar from mid-western Spain. The presence of bTB lesions affecting only one anatomic location (cervical lymph nodes), or more severe patterns affecting more than one location (mainly cervical lymph nodes and lungs), was assessed in infected animals. In addition, the existence of contacts with other pathogens such as porcine circovirus type 2 (PCV2), Aujeszky's disease virus (ADV), swine influenza virus, porcine reproductive and respiratory syndrome virus, Mycoplasma hyopneumoniae, Actinobacillus pleuropneumoniae, Haemophilus parasuis and Metastrongylus spp, was evaluated by means of serological, microbiological and parasitological techniques. The existence of contacts with a structured community of pathogens in wild boar infected by M. bovis was statistically investigated by null models. Association between this community of pathogens and bTB severity was examined using a Partial Least Squares regression approach. Results showed that adult wild boar infected by M. bovis had contacted with some specific, non-random pathogen combinations. Contact with PCV2, ADV and infection by Metastrongylus spp, was positively correlated to tuberculosis severity. Therefore, measures against these concomitant pathogens such as vaccination or deworming, might be useful in tuberculosis control programmes in the wild boar. However, given the unexpected consequences of altering any community of organisms, further research should evaluate the impact of such measures under controlled conditions. Furthermore, more research including other important pathogens, such as gastro-intestinal nematodes, will be necessary to complete this picture.

AB - © 2014 Risco et al. Co-infections with parasites or viruses drive tuberculosis dynamics in humans, but little is known about their effects in other non-human hosts. This work aims to investigate the relationship between Mycobacterium bovis infection and other pathogens in wild boar (Sus scrofa), a recognized reservoir of bovine tuberculosis (bTB) in Mediterranean ecosystems. For this purpose, it has been assessed whether contacts with common concomitant pathogens are associated with the development of severe bTB lesions in 165 wild boar from mid-western Spain. The presence of bTB lesions affecting only one anatomic location (cervical lymph nodes), or more severe patterns affecting more than one location (mainly cervical lymph nodes and lungs), was assessed in infected animals. In addition, the existence of contacts with other pathogens such as porcine circovirus type 2 (PCV2), Aujeszky's disease virus (ADV), swine influenza virus, porcine reproductive and respiratory syndrome virus, Mycoplasma hyopneumoniae, Actinobacillus pleuropneumoniae, Haemophilus parasuis and Metastrongylus spp, was evaluated by means of serological, microbiological and parasitological techniques. The existence of contacts with a structured community of pathogens in wild boar infected by M. bovis was statistically investigated by null models. Association between this community of pathogens and bTB severity was examined using a Partial Least Squares regression approach. Results showed that adult wild boar infected by M. bovis had contacted with some specific, non-random pathogen combinations. Contact with PCV2, ADV and infection by Metastrongylus spp, was positively correlated to tuberculosis severity. Therefore, measures against these concomitant pathogens such as vaccination or deworming, might be useful in tuberculosis control programmes in the wild boar. However, given the unexpected consequences of altering any community of organisms, further research should evaluate the impact of such measures under controlled conditions. Furthermore, more research including other important pathogens, such as gastro-intestinal nematodes, will be necessary to complete this picture.

UR - https://www.scopus.com/pages/publications/84908565207

U2 - 10.1371/journal.pone.0110123

DO - 10.1371/journal.pone.0110123

M3 - Article

SN - 1932-6203

VL - 9

JO - PLoS ONE

JF - PLoS ONE

IS - 10

M1 - e110123

ER -

Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar

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