Bovine tuberculosis: Within-herd transmission models to support and direct the decision-making process

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Abstract

Use of mathematical models to study the transmission dynamics of infectious diseases is becoming increasingly common in veterinary sciences. However, modeling chronic infectious diseases such as bovine tuberculosis (bTB) is particularly challenging due to the substantial uncertainty associated with the epidemiology of the disease. Here, the methodological approaches used to model bTB and published in the peer-reviewed literature in the last decades were reviewed with a focus on the impact that the models’ assumptions may have had on their results, such as the assumption of density vs. frequency-dependent transmission, the existence of non-infectious and non-detectable stages, and the effect of extrinsic sources of infection (usually associated with wildlife reservoirs). Although all studies suggested a relatively low rate of within-herd transmission of bTB when test-and-cull programs are in place, differences in the estimated length of the infection stages, sensitivity and specificity of the tests used and probable type of transmission (density or frequency dependent) were observed. Additional improvements, such as exploring the usefulness of contact-networks instead of assuming homogeneous mixing of animals, may help to build better models that can help to design, evaluate and monitor control and eradication strategies against bTB.

Introduction

Although mathematical models of disease dynamics have been extensively used in human medicine since the eighteenth century and particularly from the 1900s onward (Keeling and Rohani, 2008), their use in veterinary medicine has been quite limited until the end of the twentieth century. However, in recent decades, the number of animal disease mathematical models published in the peer-reviewed literature has substantially increased. In the field of animal health, different types of disease models of varying complexity have been useful tools for development of policy, design and evaluation of surveillance systems and the prediction of consequences due to introduction of new diseases and the expected impact of control strategies (Garner, Hamilton, 2011, Willeberg et al, 2011a, Willeberg et al, 2011b). In the case of bovine tuberculosis (bTB), modeling has been used to provide estimates of (i) within- and between-herd transmission rates (Alvarez et al, 2012, Barlow et al, 1997, Griffin et al, 2000, Kao et al, 1997, Kean et al, 1999, Perez et al, 2002a), (ii) the duration of the period between infection and detection/shedding of the pathogen (commonly referred to as ‘latency’) (Conlan et al, 2012, Fischer et al, 2005, Kao et al, 1997, Perez et al, 2002a, Smith et al, 2013a), (iii) bTB diagnostic technique reliability (sensitivity and specificity) (Conlan et al, 2012, Fischer et al, 2005, Smith et al, 2013a), (iv) disease dynamics in wildlife and contribution of wildlife reservoirs in disease incidence and/or persistence in livestock (Anderson et al, 2013, Barlow, 2000, Delahay et al, 2013, Graham et al, 2013, Kean et al, 1999), and (v) the effectiveness of alternative control measures in cattle and wildlife reservoirs (Fischer et al, 2005, Hardstaff et al, 2013, Kao, Roberts, 1999, Perez et al, 2002b, Smith et al, 2013b). Here, we offer a comprehensive review of models assessing bTB within-herd transmission, including a simplified description of the methodologies and assumptions adopted to formulate the models, a summary of the values used to parameterize or obtained from the modeling exercises, and a discussion on the most important conclusions that may be extracted from existing knowledge. We emphasize the review of studies published since the last review of the subject was published more than 10 years ago (Goodchild and Clifton-Hadley, 2001).

Section snippets

Model formulation and basic parameterization

Models of bTB within-herd transmission typically assume different mutually exclusive states between which individuals move through transitions with a given probability, which are referred to as ‘state transition models’ (Fig. 1). All models consider a ‘susceptible (S)’ state (non-infected animals that become infected after an adequate contact) and an ‘infectious (I)’ state (infected animals shedding the pathogen that, when in contact with susceptible cattle, may infect them). However, certain

Lessons learned from bTB within-herd transmission modeling

Modeling has received criticism in the past, often due to a misunderstanding about the potential benefits that could be gained from modeling disease dynamics in animal populations (de Jong, 1995). As reviewed in the previous sections, alternative modeling approaches and assumptions may be applied to one single disease and epidemiological setting, eventually leading to a wide range of estimates for a number of parameters, and thus demonstrating the impact that the different assumptions may have

Knowledge gaps and model limitations

Although tuberculosis is arguably one of the infectious diseases that has been studied more extensively in the history of human and veterinary medicine, many aspects of its pathogenesis are yet to be elucidated, which limits the formulation and parameterization of transmission models. The way those uncertainties are handled in mathematical models, usually in the form of more or less flexible assumptions, may have a critical impact on model outcomes, as recently suggested (Conlan et al., 2012).

Future uses of bTB modeling

The global situation of bTB has changed considerably in the last century. The disease has been eradicated from certain regions while its prevalence is declining in most developed countries in which ad hoc programs are in place, thus providing evidence of the usefulness of the currently available diagnostic strategies in certain settings (Cousins, Roberts, 2001, Olmstead, Rhode, 2004, Reviriego Gordejo, Vermeersch, 2006). In addition, several developing countries have initiated control and

Acknowledgments

This study was supported by Agriculture and Food Research Initiative Competitive Grant no. 2013-67015-21244 from the USDA National Institute of Food and Agriculture.

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