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The Veterinary Journal xxx (2014) xxxxxx

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The Veterinary Journal


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A eld trial of infrared thermography as a non-invasive diagnostic tool for early detection of digital dermatitis in dairy cows
M. Alsaaod a,, C. Syring a, J. Dietrich a, M.G. Doherr b, T. Gujan c, A. Steiner a
a

Clinic for Ruminants, Vetsuisse-Faculty, University of Bern, Switzerland Veterinary Public Health Institute, Vetsuisse-Faculty, University of Bern, Switzerland c Institute of Agricultural Sciences, Swiss Federal Technical School of Zrich, Switzerland
b

a r t i c l e

i n f o

a b s t r a c t
Infrared thermography (IRT) was used to detect digital dermatitis (DD) prior to routine claw trimming. A total of 1192 IRT observations were collected from 149 cows on eight farms. All cows were housed in tiestalls. The maximal surface temperatures of the coronary band (CB) region and skin (S) of the fore and rear feet (mean value of the maximal surface temperatures of both digits for each foot separately, CBmax and Smax) were assessed. Grouping was performed at the foot level (presence of DD, n = 99; absence, n = 304), or at the cow level (all four feet healthy, n = 24) or where there was at least one DD lesion on the rear feet, n = 37). For individual cows (n = 61), IRT temperature difference was determined by subtracting the mean sum of CBmax and Smax of the rear feet from that of the fore feet. Feet with DD had higher CBmax and Smax (P < 0.001) than healthy feet. Smax was signicantly higher in feet with infectious DD lesions (M-stage: M2 + M4; n = 15) than in those with non-infectious M-lesions (M1 + M3; n = 84) (P = 0.03), but this was not the case for CBmax (P = 0.12). At the cow level, an optimal cut-off value for detecting DD of 0.99 C (IRT temperature difference between rear and front feet) yielded a sensitivity of 89.1% and a specicity of 66.6%. The results indicate that IRT may be a useful non-invasive diagnostic tool to screen for the presence of DD in dairy cows by measuring CBmax and Smax. 2013 Elsevier Ltd. All rights reserved.

Article history: Accepted 30 November 2013 Available online xxxx Keywords: Infrared thermography Dairy cow Coronary band Digital dermatitis

Introduction Digital dermatitis (DD) is a dynamic infectious foot disease with increasing prevalence in many countries (Somers et al., 2003; Capion et al., 2008; Logue, 2011; Becker et al., in press). It is considered a major cause of lameness in dairy cattle, with an important effect both in terms of economics and as a welfare issue (Somers et al., 2005; Cha et al., 2010; Ettema et al., 2010). DD is a multifactorial disease, but spirochetes play an important role in its aetiopathogenesis (Walker et al., 1995; Read and Walker, 1998; Yano et al., 2010). Other factors include environmental conditions and farm management, i.e. poor foot hygiene (Shearer and Hernandez, 2000; Chapinal et al., 2013) and individual animal factors (Rodriguez-Lainz et al., 1999; Onyiro et al., 2008). Diagnosis of DD is often carried out by lifting the foot in a claw-trimming chute during routine claw trimming (Manske et al., 2002; Holzhauer et al., 2006; Thomsen et al., 2008b). Several studies have evaluated the direct inspection of DD during standing

Corresponding author. Tel.: +41 31 631 29 40.


E-mail address: maher.alsaaod@vetsuisse.unibe.ch (M. Alsaaod). 1090-0233/$ - see front matter 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.11.028

in the milking parlour, i.e. using a swivelling mirror or a rigid borescope (Rodriguez-Lainz et al., 1998; Thomsen et al., 2008a; Relun et al., 2011). Locomotion scoring is a subjective approach to assess lameness in dairy cattle (Sprecher et al., 1997; Flower and Weary, 2006), is time-consuming and may not be sensitive enough to detect hoof lesions (Tadich et al., 2010). Moreover, DD can be present without any sign of lameness, and so lameness does not appear until the DD lesion is severe (Laven and Proven, 2000; Stokes et al., 2009). Early detection of DD is therefore likely to be valuable in the prevention of further progression and in early effective treatment (Shearer and Hernandez, 2000; Dpfer et al., 2012). Reliable, practical and non-invasive methods to screen frequently and rapidly for the presence of DD in real time at foot and cow level are needed. Infrared thermography (IRT) is a non-invasive diagnostic tool that measures surface temperature of an object and represents it in a thermal colour map (colour-scale). Inammation or infectious conditions usually lead to a localized increase in the surface temperature of the affected areas (Purohit and McCoy, 1980; Turner, 1991). This is caused by an increase in the underlying circulation and tissue metabolism rate (Berry et al., 2003) and may further be inuenced by individual differences between cows

Please cite this article in press as: Alsaaod, M., et al. A eld trial of infrared thermography as a non-invasive diagnostic tool for early detection of digital dermatitis in dairy cows. The Veterinary Journal (2014), http://dx.doi.org/10.1016/j.tvjl.2013.11.028

M. Alsaaod et al. / The Veterinary Journal xxx (2014) xxxxxx

or environmental conditions (Nikkhah et al., 2005; Bowers et al., 2009; Alsaaod and Bscher, 2012). IRT may potentially be used to detect inammation non-invasively by comparing the affected area with healthy contralateral anatomical structures (Eddy et al., 2001; Van Hoogmoed and Snyder, 2002). In horses, IRT has been described for several years as a diagnostic tool to detect lameness associated with inammatory conditions (Eddy et al., 2001; Van Hoogmoed and Snyder, 2002). In dairy cattle, IRT has been used to detect infectious diseases, including bovine viral diarrhoea (Schaefer et al., 2004), bovine respiratory disease (Schaefer et al., 2007), foot-and-mouth disease (Rainwater-Lovett et al., 2009) and clinical mastitis (Hovinen et al., 2008; Polat et al., 2010). Previous studies using IRT in dairy cows have shown that both coronary band (CB) temperature (Munsell, 2004; Alsaaod and Bscher, 2012) and the temperature of the plantar aspect of the limb (Stokes et al., 2012) are increased in the presence of a foot lesion, but the reliability of IRT in detecting DD has not been assessed. The aim of this experimental study was to evaluate IRT as a tool for the detection of DD lesions in dairy cows and to determine an optimal temperature cut-off value.
Materials and methods Farms and cows The study was carried out in March/April 2013 in 149 cows (median age 4.7 years, range 2.115.2) from eight tie-stall dairy farms. The farms were a convenience sample of the farms which used the routine herd health management service provided by the Clinic for Ruminants, Vetsuisse-Faculty, University of Bern. The next eight farms where routine claw-trimming was scheduled were selected for the study. In six of these eight farms claw-trimming was performed by professional claw trimmers and in the remaining two farms by the herdsman himself. The frequency of claw trimming on the selected farms ranged from one to three times per year. The median number of cows per farm was 18 (range 728). The breeds involved were Red Holstein (n = 106; 71.1%), Holstein Friesian (n = 34; 22.8%) and Swiss Fleckvieh (n = 9; 6%). Median 305-day milk yield was 8354 L (range 70569037 L). Clinical diagnosis Clinical diagnoses of foot lesions was undertaken during routine claw-trimming by two of the authors (JD and TG) and served as reference for the detection of DD and other foot lesions. To optimize inter-observer agreement, the two participants were trained in dening DD status and scoring DD stages with pictures at repeated training sessions held before the start of the study. The foot lesions of the fore and rear legs were recorded, using the software Klauenmanager Version 3.1 (SEG Informationstechnik). The software stored information about the farm number, ear tag number, specic foot lesions (presence/ absence), and the score and location of foot lesions present. The recorded data were exported to an Excel database (Microsoft) for further analysis. Classication of digital dermatitis lesions DD lesions were scored using the 5-point M0M4 scale (Dpfer et al., 1997). Briey, M0 referred to feet with no DD lesion; M1 early stage of DD, <2 cm in diameter; M2 the classic ulcerative stage with a diameter >2 cm; M3 the healing stage, and M4 the late chronic stage. For the present study, M2 and M4 lesions were considered as infectious stages, while M1 and M3 were deemed non-infectious (Holzhauer et al., 2008; Dpfer et al., 2012). If different stages of DD were present in the same foot, the most dominant stage was chosen to describe the individual foot (M2 > M4 > M1 > M3). Infrared thermography imaging IRT images were collected immediately before the cows walked into the trimming chute. To minimize confounding factors, all IRT scans were acquired in a closed, indoor environment, while the animals were restrained in the stall in a standing position. Mean ambient temperature at the time of taking the scans was 11.3 C (range 9.614.7 C). The IRT images were obtained with a Ti25 Thermal Imager (Fluke IR-Fusion Technology), which had a precision of 0.01 C. Emissivity (e) was set at 0.95 based on the ability of the skin surface to emit radiation (Gloster et al., 2011). All images of the lateral claw were taken with the camera held in the hand at a distance of 0.5 m

Fig. 1. Infrared thermography image of the right rear foot of a 5-year-old cow (lateral-aspect). R1 is the area of interest for measurement of the maximal temperature of the coronary band, dened as the hottest pixel measured by IRT in the junction between the skin and the horn of the claw; R2 is the area of interest for measurement of the maximal temperature of the skin, dened as the hottest pixel measured by IRT in the skin area, neighbouring R1 proximally.

in a lateral 45 dorsal-mediodistal oblique direction, perpendicular to the abaxial claw wall, ensuring that the CB appeared clearly in the centre of the images for the lateral claw (Fig. 1). For the medial claw the camera was similarly held but perpendicular to the axial claw wall. The analysis of temperature was undertaken using SmartView 3.1.82.0 (Fluke IR-Fusion Technology). Two areas were measured on each image. Area 1 was laid over the CB (junction between the skin and the horn of the claw), and area 2 was laid over the skin (S), immediately neighbouring area 1 proximally (Fig. 1). The maximal temperatures of both areas (CBmax and Smax) were determined. Data analysis and statistics The complete data set consisted of a total of 1192 IRT observations for CBmax and Smax collected from 149 cows. The feet of 16 cows (10.7%) were dirty and consequently excluded from this study. A total of 532 IRT values ([CBmax lateral + CBmax medial]/2); [Smax lateral + Smax medial]/2) from 133 cows at foot level were used for the analysis. The rst analysis (data subset 1) was at the foot level. It included all healthy feet (n = 304) and all feet affected with DD (n = 99), using the absolute values of CBmax and Smax. One-way analysis of variance (ANOVA) was performed to compare: (1) rear versus front feet of healthy feet and feet affected with DD separately; (2) feet with DD versus healthy feet; and (3) infectious M-stages (M2, n = 7; and M4, n = 8) versus non-infectious M-stages (M1, n = 77; and M3, n = 7). The second and third analyses (data subsets 2 and 3) were both at the cow level. Data subset 2 included all cows with four healthy feet (n = 24) and all cows affected with DD on at least one rear foot, but which had two healthy front feet (n = 37). Data subset 3 included all cows with 4 healthy feet (n = 24) and all cows affected with DD on at least one rear foot and one front foot (n = 5). The individual temperature differences between rear and front feet were determined, by subtracting the sum of CBmax and Smax of the front feet (FF) from the rear feet (RF) of each individual cow [CBmax RF + Smax RF] [CBmax FF + Smax FF]. A one-way ANOVA was used to compare between the healthy and the DD group. A receiver operator characteristic analysis (ROC) was used to compare the diagnostic performance of IRT at the cow level and calculate the optimal threshold values for skin temperature (Dohoo et al., 2009). Statistical analysis were undertaken using NCSS 2007.

Results The prevalence of DD was 44.8 % (n = 67) at cow level and 87.5% (n = 7) at herd level. The number of cows in which DD lesions occurred in the rear feet only was 54, there were ve with lesions in the rear and front feet, and none had lesions in the front feet only. The within-herd prevalence in the eight farms ranged from 0% to 91.6%. Foot level The maximal temperatures of CB and S were signicantly higher in healthy rear feet compared to healthy front feet (P < 0.001),

Please cite this article in press as: Alsaaod, M., et al. A eld trial of infrared thermography as a non-invasive diagnostic tool for early detection of digital dermatitis in dairy cows. The Veterinary Journal (2014), http://dx.doi.org/10.1016/j.tvjl.2013.11.028

M. Alsaaod et al. / The Veterinary Journal xxx (2014) xxxxxx Table 1 Maximal temperature of coronary band (CBmax) and skin (Smax) of all healthy feet and all feet with DD, as measured by infrared thermography. Location Mean CBmax (C) Smax (C) 30.09 28.25 Rear feet (n = 95) Mean CBmax (C) Smax (C) 31.41 29.30 SD 0.34 0.31 Healthy feet (n = 304) SD 0.18 0.16 Front feet (n = 209) Mean 29.48 27.77 SD 0.23 0.21 <0.001 <0.001 P-value Mean 32.64 30.74 Rear feet (n = 91) Mean 32.70 30.79 SD 0.18 0.19 Feet with DD (n = 99) SD 0.31 0.28 Front feet (n = 8) Mean 31.85 30.13 SD 0.60 0.66 0.18 0.34 <0.001 <0.001 P-value P-value

SD, standard deviation.

Table 2 Comparison of maximum temperature of coronary band (CBmax) and skin (Smax) of infectious M-stages (M2, n = 7; and M4, n = 8) and non-infectious M-stages (M1, n = 77; and M3, n = 7). Location Infectious M-stages M2 + M4 (n = 15) Mean CBmax (C) Smax (C) 33.28 31.70 SD 0.44 0.47 Non-infectious M-stages M1 + M3 (n = 84) Mean 32.52 30.57 SD 0.19 0.20 0.12 0.03 P-value

Fig. 3. Receiver operator characteristic (ROC) curve for the temperature difference of healthy front feet and rear feet affected with DD by subtracting the sum of CBmax and Smax of the rear feet from the front feet for each individual cow (n = 61). The true positive rate (sensitivity) is plotted as function of the false positive rate (1specicity) for different thresholds. The area under the ROC curve for IRT was 0.842 (z-value = 6.79; P < 0.001). Fig. 2. Box plot of the temperature differences between rear and front feet after summation of coronary band (CBmax) and skin (Smax) temperature of each foot, comparing cows with four healthy feet (0; n = 24) and cows with digital dermatitis (1; n = 37) on at least one rear foot and with two healthy front feet (P < 0.001).

Discussion The results of this study show that feet with DD had signicantly higher CBmax and Smax than healthy feet. Using a threshold of 0.99 C for the difference in CBmax + Smax between rear and front feet, cows were detected with DD of the rear feet only with a sensitivity of 89.1% and a specicity of 66.6%. In cows with lesions of the front feet, detection of DD in the rear feet was less accurate (sensitivity 60%, specicity 62.5%). However, rear feet are affected by DD much more frequently than the front feet (Read and Walker, 1998; Rodriguez-Lainz et al., 1999; Berry et al., 2004; Speijers et al., 2012), and front feet are usually only affected in cattle that have lesions also in the rear feet (Read and Walker, 1998). Indeed in this study, <10% of the cows with DD had lesions in the front feet and none of these had DD in the front feet only. Therefore our signicant ndings for cows with DD in the rear but not the front feet apply to the great majority of cows with DD. IRT can be affected by several factors such as lactation, ambient temperature and individual body temperature (Nikkhah et al., 2005; Alsaaod and Bscher, 2012). A controlled environment is therefore essential to ensure the reliability of thermography

while no difference was found for CBmax and Smax between rear and front feet affected with DD (Table 1). Feet with DD had signicantly higher CBmax and Smax than healthy feet (P < 0.001; Table 1). Smax was signicantly higher in feet with infectious as compared to non-infectious M-lesions (P = 0.03); such a difference was not evident for CBmax (Table 2).

Cow level Within data subset 2, mean (CBmax) and skin (Smax) temperature was 0.74 C higher in healthy cows and 5.6 C for cows with DD (P < 0.001; Fig. 2). The optimal cut-off value for identifying DD in the rear feet of cows without DD in the front feet was 0.99 C. This gave a sensitivity of 89.1%, a specicity of 66.6%, and positive and negative predictive values of 80.5% and 80%, respectively (Fig. 3). The optimal cut-off value from cows with DD in both rear and front feet (data subset 3) was 0.85 C (sensitivity 60%, specicity 62.5%).

Please cite this article in press as: Alsaaod, M., et al. A eld trial of infrared thermography as a non-invasive diagnostic tool for early detection of digital dermatitis in dairy cows. The Veterinary Journal (2014), http://dx.doi.org/10.1016/j.tvjl.2013.11.028

M. Alsaaod et al. / The Veterinary Journal xxx (2014) xxxxxx

imaging (Eddy et al., 2001; Alsaaod and Bscher, 2012). In our study, all measurements were done at the same point in time relative to claw trimming, within a thermally neutral zone (TNZ). Furthermore, in order to account for individual temperature differences within cows, the temperature of both rear and front feet were calculated, with the front feet being used as controls to establish the optimal cut-off values for detecting cows with DD of the hind feet. CBmax and Smax were used as several previous studies have reported that the maximal temperature measured by IRT is more reliable than the mean or minimum (Whay et al., 2004; Rainwater-Lovett et al., 2009; Stokes et al., 2012). The surface temperature was measured at CB and S for many reasons: (1) CB is a well vascularized area which optimally reects the blood circulation of the claws, so that any inammation caused by DD may be mirrored in temperature elevation at CB and S; (2) the thermal scans of CB and S can be done without physical animal contact, quickly, and with minimal stress during examination; and (3) the CB can easily and clearly be detected by IRT, because the hair coat in this area is sparse and does not completely cover the CB. Hair insulates the emission of infrared radiation to some degree (Eddy et al., 2001). The IRT data indicated that healthy rear feet had higher CBmax and Smax than healthy front feet. The reason for this remains unclear; it may be a real effect or the apparently healthy rear feet may have been affected by a subclinical disease process. Stokes et al. (2012) measured the temperature of the plantar aspect of the foot, with and without lifting, and found that IRT reliably detected the elevated foot temperature associated with foot lesions. However, the technique was not sensitive enough for lesion-specic detection. In contrast, we found that we could detect DD in most affected cows by measuring CBmax and Smax. It is likely that the increased sensitivity of the current study is due to measuring differences between feet rather than absolute temperatures and measuring the temperature of CB and S rather than that of the plantar surface of the hoof. The increases in CBmax and Smax seen in the current study are probably associated with the inammation present in the skin and foot of cows with DD lesions. Indeed we found a higher Smax in feet with infectious (M2 + M4) as compared to non-infectious M-lesions. Spirochetes are mainly present near the cutaneous surface of the lesions during M2 and M4 stages (Mumba et al., 1999; Holzhauer et al., 2008; Dpfer et al., 2012) but further longitudinal studies are required to establish whether there is a useful correlation. In this study, IRT images were taken without prior foot cleaning as the proportion of dirty feet was very low in these tie-stall cows. If the feet are dirty this has an effect on both surface temperature measured by IRT (Stokes et al., 2012) and on the emissivity value of the measured surface (Wilhelm, 2010). Further investigation of combined washing and IRT is required in order for this system to be benecial for the management of cows kept in free stalls (cubicles).

Conict of interest statement None of the authors has any nancial or personal relationships that could inappropriately inuence or bias the content of the paper.

Acknowledgements This study was generously supported by a grant of the Fondation sur-la-croix, Switzerland. We thank the Institute of Virology and Immunology IVI, Mittelhusern, Switzerland for loaning the IRT camera for this project.

References
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Conclusions The results of this eld study showed that IRT is a promising diagnostic tool in screening for the presence of DD in dairy cows by measuring the temperature difference of CBmax and Smax between rear and front feet. However for the techniques to be successful the feet have to be clean. The development of an early warning system to detect DD using IRT might help producers to select and treat affected cattle more rapidly at an early stage of the disease. This, in turn, would improve animal welfare and reduce losses associated with DD.

Please cite this article in press as: Alsaaod, M., et al. A eld trial of infrared thermography as a non-invasive diagnostic tool for early detection of digital dermatitis in dairy cows. The Veterinary Journal (2014), http://dx.doi.org/10.1016/j.tvjl.2013.11.028

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Please cite this article in press as: Alsaaod, M., et al. A eld trial of infrared thermography as a non-invasive diagnostic tool for early detection of digital dermatitis in dairy cows. The Veterinary Journal (2014), http://dx.doi.org/10.1016/j.tvjl.2013.11.028

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