The use of digital infrared thermography and measurement of oxidative stress biomarkers as tools to diagnose foot lesions in sheep
Introduction
Lameness is a common cause of welfare and economic concerns in sheep-keeping countries (Winter, 2008). The most important infectious agents that can induce foot lesions and lameness in sheep are footrot and interdigital dermatitis (Egerton et al., 1989). Dichelobacter nodosus is the essential organism for causing footrot, while interdigital dermatitis is caused by Fusobacterium necrophorum, which is also thought to play an important role in the pathogenesis of footrot (Egerton et al., 1989). Pathogenesis, clinical appearance, differential diagnosis and control measures of interdigital dermatitis and footrot have been recently reviewed (Winter, 2008, Raadsma and Egerton, 2013, Allworth, 2014). While methods of treatment and control of these diseases are readily available, the need to make a rapid and simple diagnosis remains a key feature in treating and controlling lameness in sheep flocks. For example, a rapid and sensitive competitive real-time PCR method for early detection of D. nodosus directly from interdigital swabs of sheep has been developed (Stäuble et al., 2014). Prevention of lameness should be considered a priority economically as the control cost comprises only 3% of the total expenses for an outbreak. Moreover, the response rate to treatment is higher when lameness is treated at a very early stage (Winter, 2009).
Currently, the most common method employed by researchers and clinicians in detection of interdigital dermatitis and footrot is the visual observation of interdigital space. Visual diagnosis involves the use of a system to score the severity of the footrot lesion. A commonly used system to score footrot in small ruminants is an Australian system with five ordinal scores (Egerton and Roberts, 1971). However, this approach can be time consuming, subjective, depends on the experience of the observer and requires regular observation that is both logistically and economically challenging. Therefore, reliable, practical and non-invasive methods to monitor frequently and rapidly the presence of foot lesions are needed. In this circumstance, infrared thermography (IRT) might be useful for rapid screening of foot lesions in sheep. In veterinary medicine, IRT has been successfully used in various applications such as for the detection of bovine viral diarrhoea (Schaefer et al., 2004), bovine respiratory disease (Schaefer et al., 2007, Schaefer et al., 2012), foot-and-mouth disease (Rainwater-Lovett et al., 2009), bluetongue (Pérez de Diego et al., 2013) and clinical mastitis (Hovinen et al., 2008, Polat et al., 2010, Martins et al., 2013) and to test for detection of oestrus in dairy cows (Talukder et al., 2014b). Infrared thermography has also been applied to diagnose hoof and foot lesions in horses and cattle (Alsaaod and Büscher, 2012, Main et al., 2012, Stokes et al., 2012, Alsaaod et al., 2014). It has been reported the IRT is able to detect circadian changes of foot temperature in sheep (D’Alterio et al., 2011) and that it can measure differences between hooves temperature of healthy and footrot affected herds (Lehugeur, 2012), however in the same study, Lehugeur was not able to detect difference in temperature of different foot scores. Therefore, further studies are needed to evaluate IRT as a tool to diagnose foot lesions in sheep.
Oxidative stress, the result of an imbalance between pro-oxidants and antioxidants, is an active field of research in ruminant medicine and has been implicated in numerous disease processes including sepsis, mastitis, acidosis, ketosis, enteritis, pneumonia, respiratory, and joint diseases (Lykkesfeldt and Svendsen, 2007, Celi, 2010, Celi, 2011b). In veterinary medicine the most investigated causes of excessive free radical production, which then results in oxidative stress, are represented by metabolic and environmental cues (Celi, 2010, Celi, 2011b) and inflammatory events (Sordillo and Aitken, 2009). Selenium is an essential element in the diet of animals and is important in host antioxidant defense (Rivera et al., 2005). Recently, it has been shown that whole-blood selenium is decreased in footrot-affected sheep and that parenteral selenium supplementation accelerates recovery from footrot (Hall et al., 2009). Therefore, it seems that footrot could induce oxidative stress, leading to increase in formation of free radicals.
We hypothesised that rams affected by foot lesions will have higher interdigital space temperatures and higher oxidative stress compared to healthy rams. Therefore, the aim of this study was to assess the potential use of IRT and oxidative stress biomarkers as tools to diagnose foot lesions in sheep.
Section snippets
Animals and classification of feet lesions
In this study 15 cross bred (Merino × Dorset) rams (3 ± 1 years) were used from a farm located near Camden, NSW (34.0544° S, 150.6958° E). This region has been identified as an area with medium-high rainfall (764 mm/year) which is thought to be a predisposing factor for footrot and interdigital dermatitis. Rams were kept in a single paddock were they grazed native pasture and had ad libitum access to water. Rams were inspected and awarded a score of 0 (healthy) to 4 (severe footrot) for each hoof, as
Results
In the current study, significant (P < 0.05) differences between maximum IRT temperatures were observed between HG and FL groups (Table 1, Fig. 1). The highest maximum IRT temperature noted in rams with foot lesions was 1.3 °C greater than that of healthy rams. In addition, average IRT temperature was greater in FL rams compared to their healthy flock mates. The ability of IRT in detecting foot rot was further compared with the foot scoring system (as a reference test) using ROC curves. The
Discussion
In the current study, interdigital space temperature was significantly higher in rams with foot lesions compared to rams without any foot lesions; IRT was able to detect elevated temperature associated with foot lesions. These finding are in agreement with those of Alsaaod and Büscher (2012), Main et al. (2012), Stokes et al. (2012) and Alsaaod et al. (2014) who observed foot temperature difference between infected and healthy cattle. Stokes et al. (2012) used the maximum foot temperature to
Conclusion
The data gathered in this study suggest that measuring IRT interdigital space temperatures and oxidative stress biomarkers in sheep may help in the diagnosis of foot lesions on endemic farms, however its potential as diagnostic tool needs further evaluation before the practical benefits and on-farm adoption of this technology can be considered. Longitudinal studies investigating the progression or regression of foot lesions in a larger population of affected sheep are required to determine in
Conflict of interest statement
None of the authors are personally or professionally affiliated with other people or organisations that could inappropriately influence the content of the paper.
Acknowledgments
The authors are grateful to Craig Kristo for assistance in the scoring and classification of foot lesions and to the University of Sydney Poultry Research Foundation for providing the use of the infrared camera. The authors wish to acknowledge the Honda Foundation for providing financial support to purchase the FREE Carpe Diem.
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