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      Bovine tuberculosis breakdown duration in cattle herds: an investigation of herd, host, pathogen and wildlife risk factors

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          Abstract

          Background

          Despite rigorous controls placed on herds which disclose ante-mortem test positive cattle to bovine tuberculosis, caused by the infection of Mycobacterium bovis, many herds in Northern Ireland (NI) experience prolonged breakdowns. These herds represent a considerable administrative and financial burden to the State and farming community.

          Methods

          A retrospective observational study was conducted to better understand the factors associated with breakdown duration, which was modelled using both negative binomial and ordinal regression approaches.

          Results

          Six explanatory variables were important predictors of breakdown length in both models; herd size, the number of reactors testing positive in the initial SICCT test, the presence of a lesioned animal at routine slaughter (LRS), the count of M. bovis genotypes during the breakdown (MLVA richness), the local herd-level bTB prevalence, and the presence of herds linked via management factors (associated herds). We report that between 2008 and 2014, mean breakdown duration in NI was 226 days (approx. seven months; median: 188 days). In the same period, however, more than 6% of herds in the region remained under movement restriction for more than 420 days (13 months); almost twice as long as the mean. The MLVA richness variable was a particularly important predictor of breakdown duration. We contend that this variable primarily represents a proxy for beef fattening herds, which can operate by purchasing cattle and selling animals straight to slaughter, despite prolonged trading restrictions. For other herd types, the model supports the hypothesis that prolonged breakdowns are a function of both residual infection within the herd, and infection from the environment (e.g. infected wildlife, contiguous herds and/or a contaminated environment). The impact of badger density on breakdown duration was assessed by including data on main sett (burrow) density. Whilst a positive association was observed in the univariate analysis, confounding with other variables means that the contribution of badgers to prolonged breakdowns was not clear from our study. We do not fully reject the hypothesis that badgers are implicated in prolonging bTB breakdowns via spillback infection, but given our results, we posit that increased disease risk from badgers is unlikely to simply be a function of increasing badger density measured using sett metrics.

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          Most cited references 45

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          Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

          From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.
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            Regression models for ordinal responses: a review of methods and applications.

            Epidemiologists are often interested in estimating the risk of several related diseases as well as adverse outcomes, which have a natural ordering of severity or certainty. While most investigators choose to model several dichotomous outcomes (such as very low birthweight versus normal and moderately low birthweight versus normal), this approach does not fully utilize the available information. Several statistical models for ordinal responses have been proposed, but have been underutilized. In this paper, we describe statistical methods for modelling ordinal response data, and illustrate the fit of these models to a large database from a perinatal health programme. Models considered here include (1) the cumulative logit model, (2) continuation-ratio model, (3) constrained and unconstrained partial proportional odds models, (4) adjacent-category logit model, (5) polytomous logistic model, and (6) stereotype logistic model. We illustrate and compare the fit of these models on a perinatal database, to study the impact of midline episiotomy procedure on perineal lacerations during labour and delivery. Finally, we provide a discussion on graphical methods for the assessment of model assumptions and model constraints, and conclude with a discussion on the choice of an ordinal model. The primary focus in this paper is the formulation of ordinal models, interpretation of model parameters, and their implications for epidemiological research. This paper presents a synthesized review of generalized linear regression models for analysing ordered responses. We recommend that the analyst performs (i) goodness-of-fit tests and an analysis of residuals, (ii) sensitivity analysis by fitting and comparing different models, and (iii) by graphically examining the model assumptions.
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              Contact Networks in a Wildlife-Livestock Host Community: Identifying High-Risk Individuals in the Transmission of Bovine TB among Badgers and Cattle

              Background The management of many pathogens, which are of concern to humans and their livestock, is complicated by the pathogens' ability to cross-infect multiple host species, including wildlife. This has major implications for the management of such diseases, since the dynamics of infection are dependent on the rates of both intra- and inter-specific transmission. However, the difficulty of studying transmission networks in free-living populations means that the relative opportunities for intra- versus inter-specific disease transmission have not previously been demonstrated empirically within any wildlife-livestock disease system. Methodology/Principal Findings Using recently-developed proximity data loggers, we quantify both intra-and inter-specific contacts in a wildlife-livestock disease system, using bovine tuberculosis (bTB) in badgers and cattle in the UK as our example. We assess the connectedness of individuals within the networks in order to identify whether there are certain ‘high-risk’ individuals or groups of individuals for disease transmission within and between species. Our results show that contact patterns in both badger and cattle populations vary widely, both between individuals and over time. We recorded only infrequent interactions between badger social groups, although all badgers fitted with data loggers were involved in these inter-group contacts. Contacts between badgers and cattle occurred more frequently than contacts between different badger groups. Moreover, these inter-specific contacts involved those individual cows, which were highly connected within the cattle herd. Conclusions/Significance This work represents the first continuous time record of wildlife-host contacts for any free-living wildlife-livestock disease system. The results highlight the existence of specific individuals with relatively high contact rates in both livestock and wildlife populations, which have the potential to act as hubs in the spread of disease through complex contact networks. Targeting testing or preventive measures at high-contact groups and individuals within livestock populations would enhance the effectiveness and efficiency of disease management strategies.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Diego, USA )
                2167-8359
                3 February 2020
                2020
                : 8
                Affiliations
                [1 ]Veterinary Sciences Division, Agri-food and Biosciences Institute , Belfast, United Kingdom
                [2 ]Department of Agriculture, Environment, and Rural Affairs , Coleraine, United Kingdom
                [3 ]School of Biological Sciences, Queen’s University Belfast , Belfast, United Kingdom
                [4 ]One-Health Scientific Support Unit, Department of Agriculture, Food and the Marine , Dublin, Ireland
                Article
                8319
                10.7717/peerj.8319
                7003687
                ©2020 Milne et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                Funding
                Funded by: Department of Agriculture, Environment and Rural Affairs (DAERA)
                Award ID: 48005 (122035): 15/3/10
                This work was supported by Department of Agriculture, Environment and Rural Affairs (DAERA) (Grant: 48005 (122035): 15/3/10 “The evaluation of the role of multiple reactor and chronic breakdown herds in the epidemiology of bovine tuberculosis in Northern Ireland”). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Agricultural Science
                Ecology
                Veterinary Medicine

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