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Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland

Bovine tuberculosis (bTB) is a costly, epidemiologically complex, multi-host, endemic disease. Lack of understanding of transmission dynamics may undermine eradication efforts. Pathogen whole-genome sequencing improves epidemiological inferences, providing a means to determine the relative importanc...

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Autores principales: Akhmetova, Assel, Guerrero, Jimena, McAdam, Paul, Salvador, Liliana C. M., Crispell, Joseph, Lavery, John, Presho, Eleanor, Kao, Rowland R., Biek, Roman, Menzies, Fraser, Trimble, Nigel, Harwood, Roland, Pepler, P. Theo, Oravcova, Katarina, Graham, Jordon, Skuce, Robin, du Plessis, Louis, Thompson, Suzan, Wright, Lorraine, Byrne, Andrew W., Allen, Adrian R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272874/
https://www.ncbi.nlm.nih.gov/pubmed/37227264
http://dx.doi.org/10.1099/mgen.0.001023
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author Akhmetova, Assel
Guerrero, Jimena
McAdam, Paul
Salvador, Liliana C. M.
Crispell, Joseph
Lavery, John
Presho, Eleanor
Kao, Rowland R.
Biek, Roman
Menzies, Fraser
Trimble, Nigel
Harwood, Roland
Pepler, P. Theo
Oravcova, Katarina
Graham, Jordon
Skuce, Robin
du Plessis, Louis
Thompson, Suzan
Wright, Lorraine
Byrne, Andrew W.
Allen, Adrian R.
author_facet Akhmetova, Assel
Guerrero, Jimena
McAdam, Paul
Salvador, Liliana C. M.
Crispell, Joseph
Lavery, John
Presho, Eleanor
Kao, Rowland R.
Biek, Roman
Menzies, Fraser
Trimble, Nigel
Harwood, Roland
Pepler, P. Theo
Oravcova, Katarina
Graham, Jordon
Skuce, Robin
du Plessis, Louis
Thompson, Suzan
Wright, Lorraine
Byrne, Andrew W.
Allen, Adrian R.
author_sort Akhmetova, Assel
collection PubMed
description Bovine tuberculosis (bTB) is a costly, epidemiologically complex, multi-host, endemic disease. Lack of understanding of transmission dynamics may undermine eradication efforts. Pathogen whole-genome sequencing improves epidemiological inferences, providing a means to determine the relative importance of inter- and intra-species host transmission for disease persistence. We sequenced an exceptional data set of 619 Mycobacterium bovis isolates from badgers and cattle in a 100 km(2) bTB ‘hotspot’ in Northern Ireland. Historical molecular subtyping data permitted the targeting of an endemic pathogen lineage, whose long-term persistence provided a unique opportunity to study disease transmission dynamics in unparalleled detail. Additionally, to assess whether badger population genetic structure was associated with the spatial distribution of pathogen genetic diversity, we microsatellite genotyped hair samples from 769 badgers trapped in this area. Birth death models and TransPhylo analyses indicated that cattle were likely driving the local epidemic, with transmission from cattle to badgers being more common than badger to cattle. Furthermore, the presence of significant badger population genetic structure in the landscape was not associated with the spatial distribution of M. bovis genetic diversity, suggesting that badger-to-badger transmission is not playing a major role in transmission dynamics. Our data were consistent with badgers playing a smaller role in transmission of M. bovis infection in this study site, compared to cattle. We hypothesize, however, that this minor role may still be important for persistence. Comparison to other areas suggests that M. bovis transmission dynamics are likely to be context dependent, with the role of wildlife being difficult to generalize.
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spelling pubmed-102728742023-06-17 Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland Akhmetova, Assel Guerrero, Jimena McAdam, Paul Salvador, Liliana C. M. Crispell, Joseph Lavery, John Presho, Eleanor Kao, Rowland R. Biek, Roman Menzies, Fraser Trimble, Nigel Harwood, Roland Pepler, P. Theo Oravcova, Katarina Graham, Jordon Skuce, Robin du Plessis, Louis Thompson, Suzan Wright, Lorraine Byrne, Andrew W. Allen, Adrian R. Microb Genom Research Articles Bovine tuberculosis (bTB) is a costly, epidemiologically complex, multi-host, endemic disease. Lack of understanding of transmission dynamics may undermine eradication efforts. Pathogen whole-genome sequencing improves epidemiological inferences, providing a means to determine the relative importance of inter- and intra-species host transmission for disease persistence. We sequenced an exceptional data set of 619 Mycobacterium bovis isolates from badgers and cattle in a 100 km(2) bTB ‘hotspot’ in Northern Ireland. Historical molecular subtyping data permitted the targeting of an endemic pathogen lineage, whose long-term persistence provided a unique opportunity to study disease transmission dynamics in unparalleled detail. Additionally, to assess whether badger population genetic structure was associated with the spatial distribution of pathogen genetic diversity, we microsatellite genotyped hair samples from 769 badgers trapped in this area. Birth death models and TransPhylo analyses indicated that cattle were likely driving the local epidemic, with transmission from cattle to badgers being more common than badger to cattle. Furthermore, the presence of significant badger population genetic structure in the landscape was not associated with the spatial distribution of M. bovis genetic diversity, suggesting that badger-to-badger transmission is not playing a major role in transmission dynamics. Our data were consistent with badgers playing a smaller role in transmission of M. bovis infection in this study site, compared to cattle. We hypothesize, however, that this minor role may still be important for persistence. Comparison to other areas suggests that M. bovis transmission dynamics are likely to be context dependent, with the role of wildlife being difficult to generalize. Microbiology Society 2023-05-25 /pmc/articles/PMC10272874/ /pubmed/37227264 http://dx.doi.org/10.1099/mgen.0.001023 Text en © 2023 Crown Copyright https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License.
spellingShingle Research Articles
Akhmetova, Assel
Guerrero, Jimena
McAdam, Paul
Salvador, Liliana C. M.
Crispell, Joseph
Lavery, John
Presho, Eleanor
Kao, Rowland R.
Biek, Roman
Menzies, Fraser
Trimble, Nigel
Harwood, Roland
Pepler, P. Theo
Oravcova, Katarina
Graham, Jordon
Skuce, Robin
du Plessis, Louis
Thompson, Suzan
Wright, Lorraine
Byrne, Andrew W.
Allen, Adrian R.
Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland
title Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland
title_full Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland
title_fullStr Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland
title_full_unstemmed Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland
title_short Genomic epidemiology of Mycobacterium bovis infection in sympatric badger and cattle populations in Northern Ireland
title_sort genomic epidemiology of mycobacterium bovis infection in sympatric badger and cattle populations in northern ireland
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272874/
https://www.ncbi.nlm.nih.gov/pubmed/37227264
http://dx.doi.org/10.1099/mgen.0.001023
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