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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Main Authors: Gianluigi Rossi, Barbara Bo-Ju Shih, Nkongho Franklyn Egbe, Paolo Motta, Florian Duchatel, Robert Francis Kelly, Lucy Ndip, Melissa Sander, Vincent Ngwang Tanya, Samantha J. Lycett, Barend Mark Bronsvoort, Adrian Muwonge
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Veterinary Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2023.1086001/full
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author Gianluigi Rossi
Gianluigi Rossi
Barbara Bo-Ju Shih
Nkongho Franklyn Egbe
Paolo Motta
Florian Duchatel
Robert Francis Kelly
Lucy Ndip
Lucy Ndip
Melissa Sander
Vincent Ngwang Tanya
Samantha J. Lycett
Samantha J. Lycett
Barend Mark Bronsvoort
Barend Mark Bronsvoort
Adrian Muwonge
author_facet Gianluigi Rossi
Gianluigi Rossi
Barbara Bo-Ju Shih
Nkongho Franklyn Egbe
Paolo Motta
Florian Duchatel
Robert Francis Kelly
Lucy Ndip
Lucy Ndip
Melissa Sander
Vincent Ngwang Tanya
Samantha J. Lycett
Samantha J. Lycett
Barend Mark Bronsvoort
Barend Mark Bronsvoort
Adrian Muwonge
author_sort Gianluigi Rossi
collection DOAJ
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 doaj.art-f9bd07061a5848e4be5335952bcc43a82023-05-17T05:40:20ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692023-05-011010.3389/fvets.2023.10860011086001Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic dataGianluigi Rossi0Gianluigi Rossi1Barbara Bo-Ju Shih2Nkongho Franklyn Egbe3Paolo Motta4Florian Duchatel5Robert Francis Kelly6Lucy Ndip7Lucy Ndip8Melissa Sander9Vincent Ngwang Tanya10Samantha J. Lycett11Samantha J. Lycett12Barend Mark Bronsvoort13Barend Mark Bronsvoort14Adrian Muwonge15The Roslin Institute, R(D)SVS, University of Edinburgh – Easter Bush Campus, Midlothian, United KingdomCentre of Expertise on Animal Diseases Outbreaks, EPIC, Edinburgh, United KingdomThe Roslin Institute, R(D)SVS, University of Edinburgh – Easter Bush Campus, Midlothian, United KingdomSchool of Life Sciences, University of Lincoln, Brayford Pool, Lincoln, United KingdomThe Food and Agriculture Organization of the United Nations, Regional Office for Asia and the Pacific, Bangkok, ThailandThe Roslin Institute, R(D)SVS, University of Edinburgh – Easter Bush Campus, Midlothian, United KingdomRoyal (Dick) School of Veterinary Studies and the Roslin Institute, University of Edinburgh, Easter Bush, Midlothian, United KingdomLaboratory for Emerging Infectious Diseases, University of Buea, Buea, CameroonDepartment of Biomedical Sciences, Faculty of Health Sciences, University of Buea, Buea, CameroonTuberculosis Reference Laboratory, Bamenda, CameroonCameroon Academy of Sciences, Yaoundé, CameroonThe Roslin Institute, R(D)SVS, University of Edinburgh – Easter Bush Campus, Midlothian, United KingdomCentre of Expertise on Animal Diseases Outbreaks, EPIC, Edinburgh, United KingdomThe Roslin Institute, R(D)SVS, University of Edinburgh – Easter Bush Campus, Midlothian, United KingdomCentre of Expertise on Animal Diseases Outbreaks, EPIC, Edinburgh, United KingdomThe Roslin Institute, R(D)SVS, University of Edinburgh – Easter Bush Campus, Midlothian, United KingdomWhen 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.https://www.frontiersin.org/articles/10.3389/fvets.2023.1086001/fullMycobacterium boviswhole genome sequencing (WGS)genomic surveillancezoonotic tuberculosisphylodynamicsphylogeography
spellingShingle Gianluigi Rossi
Gianluigi Rossi
Barbara Bo-Ju Shih
Nkongho Franklyn Egbe
Paolo Motta
Florian Duchatel
Robert Francis Kelly
Lucy Ndip
Lucy Ndip
Melissa Sander
Vincent Ngwang Tanya
Samantha J. Lycett
Samantha J. Lycett
Barend Mark Bronsvoort
Barend Mark Bronsvoort
Adrian Muwonge
Unraveling the epidemiology of Mycobacterium bovis using whole-genome sequencing combined with environmental and demographic data
Frontiers in Veterinary Science
Mycobacterium bovis
whole genome sequencing (WGS)
genomic surveillance
zoonotic tuberculosis
phylodynamics
phylogeography
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 Mycobacterium bovis
whole genome sequencing (WGS)
genomic surveillance
zoonotic tuberculosis
phylodynamics
phylogeography
url https://www.frontiersin.org/articles/10.3389/fvets.2023.1086001/full
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