Genomic epizootiology of a Brucella abortus outbreak in Northern Ireland (1997-2012).


Journal

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases
ISSN: 1567-7257
Titre abrégé: Infect Genet Evol
Pays: Netherlands
ID NLM: 101084138

Informations de publication

Date de publication:
07 2020
Historique:
received: 10 10 2019
revised: 28 01 2020
accepted: 04 02 2020
pubmed: 9 2 2020
medline: 29 6 2021
entrez: 9 2 2020
Statut: ppublish

Résumé

In the recent past (1997-2012), Northern Ireland in the United Kingdom suffered an outbreak of Brucella abortus, which at its height affected over 200 cattle herds. Initially, isolates were characterized using multi-locus variable number tandem repeats analysis (MLVA). While informative in this setting, hyper-variability in some loci limited the resolution necessary to infer fine-scale disease transmission networks. Consequently, we applied whole-genome sequencing to isolates from this outbreak to evaluate higher resolution markers for disease epizootiology. Phylogenetic analysis revealed that the B. abortus outbreak in Northern Ireland was caused by two distinct pathogen lineages. One contained isolates consistent with the 1997-2012 outbreak being linked to a previous endemic infection thought eradicated. The dominant second lineage exhibited little genetic diversity throughout the recrudescent outbreak, with limited population sub-structure evident. This finding was inconsistent with prior MLVA molecular characterizations that suggested the presence of seven clonal complexes. Spatio-temporal modeling revealed a significant association of pairwise SNP differences between isolates and geographic distances. However, effect sizes were very small due to reduced pathogen diversity. Genome sequence data suggested that hyper-variability in some MLVA loci contributed to an overestimate of pathogen diversity in the most recent outbreak. The low diversity observed in our genomic dataset made it inappropriate to apply phylodynamic methods to these data. We conclude that maintaining data repositories of genome sequence data will be invaluable for source attribution/epizootiological inference should recrudescence ever re-occur. However genomic epizootiological methods may have limited utility in some settings, such as when applied to recrudescent/re-emergent infections of slowly-evolving bacterial pathogens.

Sections du résumé

BACKGROUND
In the recent past (1997-2012), Northern Ireland in the United Kingdom suffered an outbreak of Brucella abortus, which at its height affected over 200 cattle herds. Initially, isolates were characterized using multi-locus variable number tandem repeats analysis (MLVA). While informative in this setting, hyper-variability in some loci limited the resolution necessary to infer fine-scale disease transmission networks. Consequently, we applied whole-genome sequencing to isolates from this outbreak to evaluate higher resolution markers for disease epizootiology.
RESULTS
Phylogenetic analysis revealed that the B. abortus outbreak in Northern Ireland was caused by two distinct pathogen lineages. One contained isolates consistent with the 1997-2012 outbreak being linked to a previous endemic infection thought eradicated. The dominant second lineage exhibited little genetic diversity throughout the recrudescent outbreak, with limited population sub-structure evident. This finding was inconsistent with prior MLVA molecular characterizations that suggested the presence of seven clonal complexes. Spatio-temporal modeling revealed a significant association of pairwise SNP differences between isolates and geographic distances. However, effect sizes were very small due to reduced pathogen diversity.
CONCLUSIONS
Genome sequence data suggested that hyper-variability in some MLVA loci contributed to an overestimate of pathogen diversity in the most recent outbreak. The low diversity observed in our genomic dataset made it inappropriate to apply phylodynamic methods to these data. We conclude that maintaining data repositories of genome sequence data will be invaluable for source attribution/epizootiological inference should recrudescence ever re-occur. However genomic epizootiological methods may have limited utility in some settings, such as when applied to recrudescent/re-emergent infections of slowly-evolving bacterial pathogens.

Identifiants

pubmed: 32035245
pii: S1567-1348(20)30067-8
doi: 10.1016/j.meegid.2020.104235
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

104235

Informations de copyright

Crown Copyright © 2020. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest All authors declare no conflict of interest.

Auteurs

Adrian R Allen (AR)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.. Electronic address: Adrian.Allen@afbini.gov.uk.

Georgina Milne (G)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.

Kevin Drees (K)

University of New Hampshire, Department of Molecular, Cellular and Biomedical Sciences, Rudman Hall, 46 College Road, Durham, NH, USA.

Eleanor Presho (E)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.

Jordon Graham (J)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.

Paul McAdam (P)

Fios Genomics, Nine Edinburgh Bioquarter, 9 Little France Road, Edinburgh, United Kingdom.

Kerri Jones (K)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.

Lorraine Wright (L)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.

Robin Skuce (R)

Agri Food and Biosciences Institute (AFBI), AFBI Stormont, Bacteriology Branch, Stoney Road, Belfast, United Kingdom.

Adrian M Whatmore (AM)

Department of Bacteriology, Animal and Plant Health Agency (APHA), New Haw, Addlestone, Surrey, United Kingdom.

Judith Graham (J)

Department of Agriculture, Environment and Rural Affairs, Veterinary Service, Belfast, Northern Ireland, United Kingdom.

Jeffrey T Foster (JT)

University of New Hampshire, Department of Molecular, Cellular and Biomedical Sciences, Rudman Hall, 46 College Road, Durham, NH, USA.

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Classifications MeSH