A new phylodynamic model of Mycobacterium bovis transmission in a multi-host system uncovers the role of the unobserved reservoir

Autor: Stanley W. J. McDowell, David Wright, Robin A. Skuce, Hannah Trewby, Anthony O'Hare, Daniel Balaz, Rowland R. Kao, Carl McCormick
Jazyk: angličtina
Rok vydání: 2021
Předmět:
0301 basic medicine
Badger
Epidemiology
Single Nucleotide Polymorphisms
Pathology and Laboratory Medicine
law.invention
0403 veterinary science
Medical Conditions
law
Medicine and Health Sciences
Biology (General)
Phylogeny
Animal Management
Mammals
Mycobacterium bovis
education.field_of_study
biology
Ecology
Eukaryota
Agriculture
04 agricultural and veterinary sciences
Ruminants
3. Good health
Transmission (mechanics)
Infectious Diseases
Computational Theory and Mathematics
Modeling and Simulation
Genetic Epidemiology
Vertebrates
Livestock
Pathogens
Research Article
Exploit
Ecological Metrics
040301 veterinary sciences
QH301-705.5
Ecology (disciplines)
Population
Infectious Disease Epidemiology
03 medical and health sciences
Cellular and Molecular Neuroscience
SDG 3 - Good Health and Well-being
Bovines
biology.animal
Mustelidae
Genetics
Animals
Computer Simulation
education
Molecular Biology
Ecology
Evolution
Behavior and Systematics

Disease Reservoirs
business.industry
Host (biology)
Ecology and Environmental Sciences
Organisms
Biology and Life Sciences
Species Diversity
biology.organism_classification
030104 developmental biology
Evolutionary biology
Amniotes
Cattle
business
Tuberculosis
Bovine

Zoology
Badgers
Zdroj: PLoS Computational Biology, Vol 17, Iss 6, p e1009005 (2021)
O'Hare, A, Balaz, D, Wright, D M, McCormick, C, McDowell, S W J, Skuce, R & Kao, R 2021, ' A new phylodynamic model of Mycobacterium bovis transmission in a multi-host system uncovers the role of the unobserved reservoir ', PLoS Computational Biology . https://doi.org/10.1371/journal.pcbi.1009005
PLoS Computational Biology
O’Hare, A, Balaz, D, Wright, D M, McCormick, C, McDowell, S, Trewby, H, Skuce, R A & Kao, R R 2021, ' A new phylodynamic model of Mycobacterium bovis transmission in a multi-host system uncovers the role of the unobserved reservoir ', PLoS Computational Biology, vol. 17, no. 6, e1009005 . https://doi.org/10.1371/journal.pcbi.1009005
ISSN: 1553-7358
DOI: 10.1371/journal.pcbi.1009005
Popis: Multi-host pathogens are particularly difficult to control, especially when at least one of the hosts acts as a hidden reservoir. Deep sequencing of densely sampled pathogens has the potential to transform this understanding, but requires analytical approaches that jointly consider epidemiological and genetic data to best address this problem. While there has been considerable success in analyses of single species systems, the hidden reservoir problem is relatively under-studied. A well-known exemplar of this problem is bovine Tuberculosis, a disease found in British and Irish cattle caused by Mycobacterium bovis, where the Eurasian badger has long been believed to act as a reservoir but remains of poorly quantified importance except in very specific locations. As a result, the effort that should be directed at controlling disease in badgers is unclear. Here, we analyse densely collected epidemiological and genetic data from a cattle population but do not explicitly consider any data from badgers. We use a simulation modelling approach to show that, in our system, a model that exploits available cattle demographic and herd-to-herd movement data, but only considers the ability of a hidden reservoir to generate pathogen diversity, can be used to choose between different epidemiological scenarios. In our analysis, a model where the reservoir does not generate any diversity but contributes to new infections at a local farm scale are significantly preferred over models which generate diversity and/or spread disease at broader spatial scales. While we cannot directly attribute the role of the reservoir to badgers based on this analysis alone, the result supports the hypothesis that under current cattle control regimes, infected cattle alone cannot sustain M. bovis circulation. Given the observed close phylogenetic relationship for the bacteria taken from cattle and badgers sampled near to each other, the most parsimonious hypothesis is that the reservoir is the infected badger population. More broadly, our approach demonstrates that carefully constructed bespoke models can exploit the combination of genetic and epidemiological data to overcome issues of extreme data bias, and uncover important general characteristics of transmission in multi-host pathogen systems.
Author summary For single host pathogens, pathogen genetic data have been transformative for understanding the transmission and control of many diseases, particuarly rapidly evolving RNA viruses. However garnering similar insights where pathogens are multi-host is more challenging, particularly when the evolution of the pathogen is slower and pathogen sampling often heavily biased. This is the case for Mycobacterium bovis, the causative agent of bovine Tuberculosis (bTB) and for which the Eurasian badger plays an as yet poorly understood role in transmission and spread. Here we have developed a computational model that incorporates M. bovis genetic data from cattle only with a highly abstracted model of an unobserved reservoir. Our research shows that a model in which the reservoir does not contribute to pathogen diversity, but is a source of infection in spatially localised areas around each farm, better describes the patterns of outbreaks observed in a population-level sample of a single M. bovis genotype in Northern Ireland over a period of 15 years, compared to models in which either the reservoir has no role, disease spread is spatially extensive, or where they generate considerable diversity on their own. While this reservoir model is not explicitly a model of badgers, its characteristics are consistent with other data that would suggest a reservoir consisting of infected badgers that contribute substantially to cattle infection, but could not maintain disease on their own.
Databáze: OpenAIRE