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Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data

When studying the dynamics of a pathogen in a host population, one crucial question is whether it transitioned from an epidemic (i.e., the pathogen population and the number of infected hosts are increasing) to an endemic stable state (i.e., the pathogen population reached an equilibrium). For slow-...

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Autores principales: Rossi, Gianluigi, Shih, Barbara Bo-Ju, Egbe, Nkongho Franklyn, Motta, Paolo, Duchatel, Florian, Kelly, Robert Francis, Ndip, Lucy, Sander, Melissa, Tanya, Vincent Ngwang, Lycett, Samantha J., Bronsvoort, Barend Mark, Muwonge, Adrian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10230100/
https://www.ncbi.nlm.nih.gov/pubmed/37266384
http://dx.doi.org/10.3389/fvets.2023.1086001
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author Rossi, Gianluigi
Shih, Barbara Bo-Ju
Egbe, Nkongho Franklyn
Motta, Paolo
Duchatel, Florian
Kelly, Robert Francis
Ndip, Lucy
Sander, Melissa
Tanya, Vincent Ngwang
Lycett, Samantha J.
Bronsvoort, Barend Mark
Muwonge, Adrian
author_facet Rossi, Gianluigi
Shih, Barbara Bo-Ju
Egbe, Nkongho Franklyn
Motta, Paolo
Duchatel, Florian
Kelly, Robert Francis
Ndip, Lucy
Sander, Melissa
Tanya, Vincent Ngwang
Lycett, Samantha J.
Bronsvoort, Barend Mark
Muwonge, Adrian
author_sort Rossi, Gianluigi
collection PubMed
description When studying the dynamics of a pathogen in a host population, one crucial question is whether it transitioned from an epidemic (i.e., the pathogen population and the number of infected hosts are increasing) to an endemic stable state (i.e., the pathogen population reached an equilibrium). For slow-growing and slow-evolving clonal pathogens such as Mycobacterium bovis, the causative agent of bovine (or animal) and zoonotic tuberculosis, it can be challenging to discriminate between these two states. This is a result of the combination of suboptimal detection tests so that the actual extent of the pathogen prevalence is often unknown, as well as of the low genetic diversity, which can hide the temporal signal provided by the accumulation of mutations in the bacterial DNA. In recent years, the increased availability, efficiency, and reliability of genomic reading techniques, such as whole-genome sequencing (WGS), have significantly increased the amount of information we can use to study infectious diseases, and therefore, it has improved the precision of epidemiological inferences for pathogens such as M. bovis. In this study, we use WGS to gain insights into the epidemiology of M. bovis in Cameroon, a developing country where the pathogen has been reported for decades. A total of 91 high-quality sequences were obtained from tissue samples collected in four abattoirs, 64 of which were with complete metadata. We combined these with environmental, demographic, ecological, and cattle movement data to generate inferences using phylodynamic models. Our findings suggest M. bovis in Cameroon is slowly expanding its epidemiological range over time; therefore, endemic stability is unlikely. This suggests that animal movement plays an important role in transmission. The simultaneous prevalence of M. bovis in co-located cattle and humans highlights the risk of such transmission being zoonotic. Therefore, using genomic tools as part of surveillance would vastly improve our understanding of disease ecology and control strategies.
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spelling pubmed-102301002023-06-01 Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data Rossi, Gianluigi Shih, Barbara Bo-Ju Egbe, Nkongho Franklyn Motta, Paolo Duchatel, Florian Kelly, Robert Francis Ndip, Lucy Sander, Melissa Tanya, Vincent Ngwang Lycett, Samantha J. Bronsvoort, Barend Mark Muwonge, Adrian Front Vet Sci Veterinary Science When studying the dynamics of a pathogen in a host population, one crucial question is whether it transitioned from an epidemic (i.e., the pathogen population and the number of infected hosts are increasing) to an endemic stable state (i.e., the pathogen population reached an equilibrium). For slow-growing and slow-evolving clonal pathogens such as Mycobacterium bovis, the causative agent of bovine (or animal) and zoonotic tuberculosis, it can be challenging to discriminate between these two states. This is a result of the combination of suboptimal detection tests so that the actual extent of the pathogen prevalence is often unknown, as well as of the low genetic diversity, which can hide the temporal signal provided by the accumulation of mutations in the bacterial DNA. In recent years, the increased availability, efficiency, and reliability of genomic reading techniques, such as whole-genome sequencing (WGS), have significantly increased the amount of information we can use to study infectious diseases, and therefore, it has improved the precision of epidemiological inferences for pathogens such as M. bovis. In this study, we use WGS to gain insights into the epidemiology of M. bovis in Cameroon, a developing country where the pathogen has been reported for decades. A total of 91 high-quality sequences were obtained from tissue samples collected in four abattoirs, 64 of which were with complete metadata. We combined these with environmental, demographic, ecological, and cattle movement data to generate inferences using phylodynamic models. Our findings suggest M. bovis in Cameroon is slowly expanding its epidemiological range over time; therefore, endemic stability is unlikely. This suggests that animal movement plays an important role in transmission. The simultaneous prevalence of M. bovis in co-located cattle and humans highlights the risk of such transmission being zoonotic. Therefore, using genomic tools as part of surveillance would vastly improve our understanding of disease ecology and control strategies. Frontiers Media S.A. 2023-05-17 /pmc/articles/PMC10230100/ /pubmed/37266384 http://dx.doi.org/10.3389/fvets.2023.1086001 Text en Copyright © 2023 Rossi, Shih, Egbe, Motta, Duchatel, Kelly, Ndip, Sander, Tanya, Lycett, Bronsvoort and Muwonge. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Veterinary Science
Rossi, Gianluigi
Shih, Barbara Bo-Ju
Egbe, Nkongho Franklyn
Motta, Paolo
Duchatel, Florian
Kelly, Robert Francis
Ndip, Lucy
Sander, Melissa
Tanya, Vincent Ngwang
Lycett, Samantha J.
Bronsvoort, Barend Mark
Muwonge, Adrian
Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
title Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
title_full Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
title_fullStr Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
title_full_unstemmed Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
title_short Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
title_sort unraveling the epidemiology of mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
topic Veterinary Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10230100/
https://www.ncbi.nlm.nih.gov/pubmed/37266384
http://dx.doi.org/10.3389/fvets.2023.1086001
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