Molecular Epidemiology of Brucella abortus in Northern Ireland—1991 to 2012

RESEARCH ARTICLE Molecular Epidemiology of Brucella abortus in Northern Ireland—1991 to 2012 Adrian Allen1☯*, Eleanor Breadon1☯, Andrew Byrne1, Thomas Mallon1, Robin Skuce1,2, Pauline Groussaud3, Amanda Dainty3, Judith Graham4, Kerri Jones1, Lorraine Pollock1, Adrian Whatmore3 1 Agri-Food and Biosciences Institute (AFBI), AFBI Stormont, Belfast, United Kingdom, 2 School of Biological Sciences, Queens University, Belfast, United Kingdom, 3 OIE/WHO/FAO Reference Laboratory for Brucellosis, Department of Bacteriology, Animal and Plant Health Agency (APHA), New Haw, Addlestone, Surrey, United Kingdom, 4 Department of Agriculture and Rural Development, Veterinary Service, Belfast, Northern Ireland ☯ These authors contributed equally to this work. * Abstract OPEN ACCESS Citation: Allen A, Breadon E, Byrne A, Mallon T, Skuce R, Groussaud P, et al. (2015) Molecular Epidemiology of Brucella abortus in Northern Ireland —1991 to 2012. PLoS ONE 10(9): e0136721. doi:10.1371/journal.pone.0136721 Editor: Axel Cloeckaert, Institut National de la Recherche Agronomique, FRANCE Received: October 3, 2014 Background Brucellosis is the most common bacterial zoonoses worldwide. Bovine brucellosis caused by Brucella abortus has far reaching animal health and economic impacts at both the local and national levels. Alongside traditional veterinary epidemiology, the use of molecular typing has recently been applied to inform on bacterial population structure and identify epidemiologically-linked cases of infection. Multi-locus variable number tandem repeat VNTR analysis (MLVA) was used to investigate the molecular epidemiology of a well-characterised Brucella abortus epidemic in Northern Ireland involving 387 herds between 1991 and 2012. Accepted: August 7, 2015 Published: September 1, 2015 Results Copyright: © 2015 Allen et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. MLVA identified 98 unique B. abortus genotypes from disclosing isolates in the 387 herds involved in the epidemic. Clustering algorithms revealed the relatedness of many of these genotypes. Combined with epidemiological information on chronology of infection and geographic location, these genotype data helped to identify 7 clonal complexes which underpinned the outbreak over the defined period. Hyper-variability of some VNTR loci both within herds and individual animals led to detection of multiple genotypes associated with single outbreaks. However with dense sampling, these genotypes could still be associated with specific clonal complexes thereby permitting inference of epidemiological links. MLVAbased epidemiological monitoring data were congruent with an independent classical veterinary epidemiology study carried out in the same territory. Data Availability Statement: All genotype data for brucella strains is contained within the general and supplementary tables supplied along with the manuscript. Herd location for diseased animals is supplied on the map figure, however supplying exact co-ordinates for the farms involved is not possible as it would involve a breach of confidentiality between the enterprises involved and the Department of Agriculture and Rural Development, Northern Ireland. Funding: This work was funded by the Department of Agriculture and Rural Development, Northern Ireland www.dardni.gov.uk, and the Department of Conclusions MLVA is a useful tool in ongoing disease surveillance of B. abortus outbreaks, especially when combined with accurate epidemiological information on disease tracings, geographical clustering of cases and chronology of infection. PLOS ONE | DOI:10.1371/journal.pone.0136721 September 1, 2015 1 / 23 Brucella abortus in N. Ireland—Molecular Epidemiology Environment, Food and Rural Affairs (DEFRA) under projects SE0311, SE0313 and SB1400 www. Competing Interests: The authors have declared that no competing interests exist. Introduction Bovine brucellosis, the most common bacterial zoonoses worldwide [1,2], caused by the bacterium Brucella abortus, is a major public and animal health issue worldwide. The disease can cause chronic and debilitating infection in humans and reproductive losses / abortion in cattle [3,4]. Aborted foetuses and amniotic fluids from infected animals are highly infectious [5] and are thought to be a major transmission route to new susceptible hosts [6]. The nasal and oral mucosae of animals are considered the most likely site of entry for the pathogen to new hosts [7,8]. The B. abortus bacterium is a facultative intracellular pathogen [9] but can remain viable in the environment for long periods provided there is an adequate moisture level. Conversely, strong sunlight and an arid climate can reduce the survival of the bacterium in the environment [7,9]. Further elucidation of the epidemiology of the pathogen has been gained by use of data from the greater Yellowstone area of the western United States where both elk and bison are known wildlife reservoirs. In this setting, animal density has been observed to play a crucial role in the likely outcome of a disease outbreak. Both elk and bison populations are at considerably greater risk of developing widespread infection if abortions occur during the winter period when grazing land is scarce leading to higher animal density [9]. In intensively farmed agricultural settings, such as Northern Ireland, dense populations of domesticated bovine animals are therefore at a considerable risk of becoming infected in the event of brucellosis mediated abortion within their herd. Eradication of bovine brucellosis is undertaken using a test and slaughter protocol that makes use of internationally standardised bacterial culture and diagnostic tests. In addition, vaccination to agreed international standards is routinely deployed in some parts of the world [2, 10–12]. Whilst B. abortus eradication programmes have been effective in much of the developed world [13], including in Great Britain, the Republic of Ireland, Australia, New Zealand and most of North America [6,14], in many other locations, the disease remains a costly and challenging issue. Gaining and maintaining officially brucellosis free (OBF) status is economically desirable for nations since being free from disease increases herd productivity and opportunities for trade whilst reducing expenditure on control and/or eradication. Despite initial success in disease eradication in Northern Ireland throughout the 1980s [15], three major sporadic outbreaks in 1997 [16] led to regional recrudescence [15]. The cost of the Northern Ireland eradication scheme between 1999 and 2013 has amounted to approximately £150 million sterling. At the molecular level, the Brucella genus is characterised by a high level of nucleotide similarity [1,5,17]. The latter has, until relatively re (...truncated)