Access the full text.
Sign up today, get DeepDyve free for 14 days.
Loading next page...
/lp/springer-journals/technological-environmental-and-biological-factors-referent-variance-H4DYEgtEhm
- Publisher
- Springer Journals
- Copyright
- Copyright © 2015 by Montanholi et al.
- Subject
- Life Sciences; Agriculture; Biotechnology; Food Science; Animal Genetics and Genomics; Animal Physiology
- eISSN
- 2049-1891
- DOI
- 10.1186/s40104-015-0027-y
- pmid
- 26217486
- Publisher site
- See Article on Publisher Site
Abstract
Background: Despite its variety of potential applications, the wide implementation of infrared technology in cattle production faces technical, environmental and biological challenges similar to other indicators of metabolic state. Nine trials, divided into three classes (technological, environmental and biological factors) were conducted to illustrate the influence of these factors on body surface temperature assessed through infrared imaging. Results: Evaluation of technological factors indicated the following: measurements of body temperatures were strongly repeatable when taken within 10 s; appropriateness of differing infrared camera technologies was influenced by distance to the target; and results were consistent when analysis of thermographs was compared between judges. Evaluation of environmental factors illustrated that wind and debris caused decreases in body surface temperatures without affecting metabolic rate; additionally, body surface temperature increased due to sunlight but returned to baseline values within minutes of shade exposure. Examination/investigation/exploration of animal factors demonstrated that exercise caused an increase in body surface temperature and metabolic rate. Administration of sedative and anti-sedative caused changes on body surface temperature and metabolic rate, and during late pregnancy a foetal thermal imprint was visible through abdominal infrared imaging. Conclusion: The above factors should be considered in order to standardize operational procedures for taking thermographs, thereby optimizing the use of such technology in cattle operations. Keywords: Body heat loss, Convective heat loss, Infrared imaging, Oxygen consumption, Pharmacodynamics Background in the study of wild and domestic animals. In wild Infrared radiation refers to radiation that has a longer animals this technology has been used to determine wavelength than visible light. Its history began in 1800, dorsal fin surface temperatures of dolphins [2], optimize when Sir William Herschel discovered heat rays that the counts of white tailed deer via aerial appraisal [3], went beyond the scope of the visible red colour in the evaluate heat exchange patterns in African elephants [4], electromagnetic spectrum [1]. This discovery culminated and determine metabolic heat loss in birds [5]. in the development of several infrared radiation based A comprehensive collection of infrared imaging appli- applications, including infrared imaging. Infrared im- cations in livestock animals is described by Luzi et al. aging technology, which is noted for its non-contact op- [6]. Applications in the livestock sector, particularly in eration, has evolved from its initial military use in the bovine operations, include early detection of inflam- 1950’s to a multitude of applications, including several matory illness including mastitis [7], lameness [8] and bovine respiratory disease virus [9]; assessment of animal welfare issues such as tail docking sensitivity [10] and * Correspondence: Yuri.Montanholi@dal.ca Department of Animal and Poultry Science, University of Guelph, Guelph, reactivity to stress [11]; determination of the appropri- ON N1G 2W1, Canada ateness of milking equipment [12]; assessment of prod- Department of Plant and Animal Sciences, Dalhousie University, Truro, NS uctivity, including of heat and methane production [13] B2N 5E3, Canada Full list of author information is available at the end of the article © 2015 Montanholi et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 2 of 16 and feed efficiency [14]; evaluation of fertility traits, such (1) technological factors (imaging repeatability, infrared as scrotum temperature patterns [15] and body condi- camera comparison, and judge comparison trials); (2) tion score [16]; and appraisal of meat quality [17]. environmental factors (wind, debris on body surface, and Despite the myriad of potential applications, the use of sunlight exposure); and (3) biological factors (physical infrared imaging in commercial cattle husbandry is not exercise, drug response, and pregnancy status). Trials widespread. There is, however, great potential for expan- were conducted at the Elora Beef and Dairy Research sion as reviewed by Mitchell [18]. As with other highly Centres (University of Guelph). The animal care proto- sensitive measures, radiant heat loss poses challenges col and experimental procedures in this study were ap- related to adequacy of equipment, as well as environ- proved by the University of Guelph Animal Care mental and biological factors that can alter thermograph Committee. A number of animals (2 beef heifers, 128 readings. The choice of the infrared camera based on beef calves, 3 beef cows and 1 dairy cow) were used to the available technological options should be considered accomplish the different trials, as detailed in Table 1. For [19]. Environmental and animal factors may mask the the physical exercise, sedative response, wind, and debris underlying biological target by causing uncontrolled on body surface trials, an indirect calorimeter based on changes in the patterns of radiation detected by the infra- gas exchange, similar to the system described by Odongo red camera. In the case of livestock species, infrared im- et al. [24], was used to assess real-time metabolic rate aging detects small changes in body surface temperature with measures of oxygen consumption obtained every patterns caused by biological phenomena [11, 13], making 1 s during sampling. For infrared camera comparison, the infrared imaging assessment subject to artifacts. wind, debris on body surface, physical exercise, drug Environmental factors include debris covering the animal response and pregnancy status trials, temperature and which blocks the normal infrared radiation emissions from humidity were monitored every 5 min (Hobo Pro U14, the body surface. Additionally, weather conditions such as U.S.A.). Additionally, a shaved patch of 5 by 5 cm, sunlight exposure and air movement [20] can also skew located at the dorso-caudal portion of the flank, was infrared analyses by interfering with the radiation emitted made on the beef heifers for skin surface assessment. by the animal’s body surface. A few examples of biological Assessment of respiration rate during the physical effects on metabolic rate, and consequently body tem- exercise and sunlight trials was performed by counting perature, include physical activity [21], physiological states flank movements over a period of 1 min during each such as pregnancy [22], and pharmacodynamics [23]. assessment, in accordance with the method previously Since infrared radiation emissions captured from ani- described by Gaughan et al. [25]. mals through infrared images may be largely influenced by several factors, it is important to characterize and Infrared imaging and image analysis consider these potential effects to ensure reliable and Infrared images from different body locations were taken accurate infrared imaging assessments. Our objectives (Fig. 1) with one or all of the following infrared cameras: were several fold: a) to compare the types of infrared FLIR i40, FLIR T250 and FLIR SC2000 (FLIR Systems, technology and measure the consistency of imaging Inc., U.S.A.). The FLIR i40 represents the simplest tech- analysis; b) to demonstrate the effects of environmental nology, with a temperature range of −20 to 350 °C, and artifacts (wind, debris on body surface, and sunlight resolution of 120 × 120 pixels. The FLIR T250 represents exposure) on infrared imaging; and c) to illustrate the technology of intermediate quality, with a temperature effects of biological factors (physical exercise, drug re- range of −20 to 350 °C, and a resolution of 240 × sponse, and pregnancy) on thermographs. 180 pixels. The FLIR SC2000 is of scientific grade, has a temperature range of −40 to 1500 °C, a resolution of Methods 320 × 240 pixels, and also multiple options for lenses General information about research trials and animals (12, 24 and 45° lenses). The study was divided into three classes with a total of Analyses of the thermographs were performed using nine research trials. The classes included the following: the ThermaCAM Researcher Pro 2.8 SR-1 software Table 1 Description of the animals used over the different research trial Animals Age, d Weight, kg Status Breed composition Beef heifer A 487 496 Non-pregnant 50 % Piedmontese, 35 % Angus 15 % Simmental, Beef heifer B 453 492 Non-pregnant 50 % Piedmontese, 50 % Simmental 128 Calves 194 ± 21 260 ± 40.2 Weaned 45 % Angus, 40 % Simmental, 15 % Piedmontese; 3 Beef cows 5079 ± 440 689 ± 63.7 Post-partum, nursing 33 % Angus, 33 % Piedmontese, 17 % Simmental, 17 % other breeds Dairy heifer 738 560 Pre-calving 100 % Holstein Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 3 of 16 Fig. 1 Infrared images of the body locations evaluated throughout the trials; (a): flank (k), shaved patch (j), (b): eyeball (l), whole eye (m), cheek area (n), (c): hind area using a rectangle (o), hind area using a circle (p), (d): rear view of the foot, (e): lumbar region, (f): trunk, (g): coronary band, (h)snout, (i) rear view of the ear. The shapes drawn on the images delimit the portion of the image used to access the temperature during imaging analyses (FLIR Systems, Inc., U.S.A.). The emissivity value was set animal was infrared imaged and its body weight assessed at 0.98 for all infrared imaging analyses. Images were while calves were restrained in a squeeze chute (Silencer captured and analyzed using the iron palette for all trials Hydraulic Squeeze Chute; Moly Manufacturing Inc., except for the pregnancy status trial, where the rain 10 U.S.A.) located indoors. Two head thermographs were palette was used. Both the iron and rain 10 palettes taken consecutively (within 10 s) with the FLIR SC2000 display black and white colors indicating the coldest and camera. All calves were submitted to the same sampling warmest temperatures respectively, with other colors in- regime 72 h later. The images were taken between 1400 dicating intermediary temperatures. For the iron palette and 1600 h. The repeatability of the eye and the snout the color pattern is continuous from pixel to pixel, while analysis, for both average and maximum temperatures, in the rain 10 palette the whole temperature distribution was then accessed (Fig. 1; bm, h). of the image is divided in ten ranges with each receiving a different color. After an appropriate shape was drawn Distance and infrared cameras comparison trial on each image to outline the body sub-location, the Images were taken of the shaved square patch located maximum and average temperatures of the selected region on the left flank (Fig. 1; aj) of the beef heifer A (Table 1). were computed (Fig. 1). The shapes were determined Images were taken from seven distances (1.0, 1.5, 3.5, based on anatomical landmarks as well as biological rele- 5.5, 9.5, 11.5 and 15.5 m) with the three infrared cam- vance for body temperature control [26], and were based eras, and with the three different lenses for the SC2000 on previous studies on body surface temperature assess- camera. The heifer was tied to a post indoors using a ment using infrared imaging in the bovine [11, 13]. halter and allowed to acclimatize to the environment be- fore the imaging procedure. All images were taken Technological factors within 40 min with the heifer standing still. Imaging repeatability trial The imaging repeatability trial used beef calves (Table 1). Judge comparison trial Calves were divided into two groups (with 69 calves in Two trained judges who were experienced with infrared the first group and 59 calves in the second), and groups imaging interpretation analyzed the images, which were were sampled on two consecutive weeks. Each individual all taken 1 m from the animal surface. Images of the Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 4 of 16 foot, eye, snout and hind area, as well as the images of adding shavings (cooled to 10 °C) on top of the animal’s the shaved square patch were taken for use in this trial. back, and a fifth image being taken immediately after Body surface landmarks were established beforehand to the shavings were put on. Shavings remained on the ensure consistency between temperature readings from animal for 40 min, with one image taken every 20 min the infrared images among the two judges. For the flank, for a total of two images. Shavings were then removed an irregular hexagon was drawn following the anatom- from the animal with a soft brush and a final image was ical landmarks delimiting the flank region (Fig. 1; ak). taken 20 min later under the same conditions as the The foot was analyzed via a rectangle placed below the previous images. dew claw and immediately above the hoof (Fig. 1; d). The coronary band temperature was measured via a line Sunlight exposure trial drawn at the lateral view of the outer hoof (Fig. 1; g). To A sunlight exposure trial was conducted using three beef measure eye temperature, a circle was drawn to cover cows (Table 1). Infrared images were taken using the the entire eye and surrounding area; the diameter of the FLIR SC2000 camera with the 24° lens at a distance of circle was equal to the width of the eye plus distance be- 1.0 to 1.5 m from the object. Images were taken from tween the eye medial canthus and the end of the warm- the flank, the hind area, the eyeball, the snout and the est region medial to the canthus (Fig. 1; bm). A polygon back of the ear (Fig. 1; ak, co, bl, h, i). The solar radi- spanning the lower edge of the nostril and across the ation was measured by a light meter (Li-Cor LI-189, top of the upper lip was created to analyze the snout U.S.A.). The temperature and relative humidity were (Fig. 1; h). Lastly, the hind area was analyzed using a cir- assessed using a thermometer and humidity data logger cle with a diameter equal to the width of the tail at its (Hobo Pro v2 U23-002, U.S.A.), and wind speed was insertion and placed immediately dorsolateral to the measured using an anemometer (Sims DIC-3, Simerl vulva (Fig. 1; cp). Instruments, U.S.A.). An adapted heart rate monitor (Polar WearLink W.I.N.D. transmitter, Polar Electro Oy, Environmental factors U.S.A.) was attached to the animal via a leather belt Wind trial strapped around the girth of the animal, and respiration Heifer B (Table 1) was used in this trial and infrared im- frequency assessed as previously described every 7 min ages were taken using the FLIR SC2000 camera with the for a total of 15 times. Measurements of heart rate and 45° lens at a distance of 0.8 m. Images were taken of the environmental temperature were taken every 5 and 60 s hind foot, trunk, flank and clipped square on both sides respectively, and averaged over 7 min intervals for the of the animal (Fig. 1; d, f, ak and aj). A set of baseline entire duration of the trial. Cows were housed in indi- images were taken, and 20 min later a fan (Protemp vidual and neighboring pens and were supervised by one PT-36-BDF-AF, Pinnacle Products International, Inc., herdsman per cow to ensure minimal physical activity U.S.A.) was turned on at a wind speed of 17 km/h, during this trial. Cows were initially confined to a measured using an anemometer (La Crosse Technology shaded area for 30 min of standing with minimum phys- EA-3010U, U.S.A.). The wind was directed at the left ical activity; this was then followed by a set of baseline side of the animal from a distance of 0.9 m from the images taken for a total of three sets every 7 min. The trunk of the heifer, while the head of the animal was three cows were then moved and kept in a sunny area, held in the calorimetric chamber. Images were taken as where a set of images was taken every 7 min for a total soon as the fan was turned on and every 20 min there- of six sets, before being led back to the shaded area after, for a total of four sets. The fan was then turned off where another set of images were taken every 7 min for and images were taken every 20 min for a total of three a total of six sets. additional sets. Biological factors Debris on body surface trial Physical exercise trial Heifer B (Table 1) was used in this trial and infrared im- Heifer A (Table 1) was used in this trial and infrared im- ages were taken using the FLIR SC2000 camera with the ages were taken using the T250 camera at a distance of 45° lens at a distance of 0.8 m. The debris on body sur- 0.8 m. Information was gathered for heat production face trial was conducted by placing dried wood shavings with images taken of the clipped left flank area, the front on the back while the head of the animal was held in the foot, eyeball, cheek and snout (Fig. 1; aj, d, bn and h). indirect calorimeter. Unlike the other trials, only one Following three sets of baseline images and concurrent specific body location, a top view of the lumbar region, metabolic rate assessments, the heifer was then subjected to was the focus for this trial (Fig. 1; e). One image was 15 min of exercise which consisted of chasing the heifer to taken as a baseline every 20 min for a total of four im- run across a covered barn of 80 m in length. The entire ex- ages, with the fourth image taken immediately before ercise portion took a total of 20 min; 15 min for the exercise Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 5 of 16 trial and 5 min to set the heifer back up in the calorimeter). the sunlight exposure trial, the average across different A later set of post-exercise images and calorimetry assess- cows was calculated. Additionally, in the infrared camera ments were taken every 5 min after exercising for three sets. comparison trial, means of all of equipment used were Respiration rate was also assessed during the baseline and calculated at each distance. For the imaging repeatability post-exercise periods. trial, correlations between images taken consecutively and across different days, as well as between body weight Drug response trial assessed on different days, were determined. Similarly, The drug response trial was separated into two portions. correlations between judges across different body locations Heifer B was used in the first portion and Heifer A was and by determinations of the average or maximum used in the second portion (Table 1). Infrared images temperature were also calculated. were taken from the right flank, the coronary band, the foot, and the hind area (Fig. 1; ak, g, d, co). In the first Results portion, where only xylazine (Rompun, Bayer) was uti- Technological factors lized, baseline images were taken every 7.5 min for three Imaging repeatability trial sets with the FLIR SC2000 camera at a distance of Table 2 shows the infrared imaging results of the repeat- 0.8 m. The animal was then injected with 0.02 mg/kg of ability trial. For the four days of assessment (with two xylazine (Rompun, Bayer) intravenously to obtain mild days for each group of calves), strong correlations were sedation while maintained in the calorimetric chamber, observed between images taken consecutively at both and a subsequent set of images were taken after this in- body locations (snout and eye) and for both analyses jection every 7.5 min for a total of 12 sets. The second (average and maximum temperatures). Correlations be- portion of the trial involved xylazine and atipamezole tween days for both groups were weak, with average (Antisedan, Pfizer), with xylazine first administered to temperatures for both locations displaying better repeat- the animal (0.02 mg/kg; IV), followed by atipamezole ability than maximum temperatures (Table 2). Average (0.10 mg/kg; IV) 40 min after the xylazine. A set of base- temperatures also presented more consistent correla- line images was taken every 20 min for three sets, followed tions between the two groups over maximum tempera- by the xylazine injection. A set of images was then taken tures. A strong correlation between body weights of every 20 min following the xylazine injection for two more animals at the two different weight assessments was also sets, and after injection of atipamezole, two additional sets observed for both groups; correlations were 0.97 and of images were taken every 20 min. Calorimetry measures 0.89 for groups 1 and 2, respectively (P < 0.01). were taken for the animals throughout the trial, with infor- mation gathered for heat production. Distance and infrared cameras comparison trial The average relative humidity was 69.8 ± 1.7 % and the Pregnancy status trial average temperature was 22.9 ± 0.5 °C for the duration A pregnant dairy heifer was imaged for this trial (Table 1) of the infrared cameras comparison trial. Figure 2 shows using the SC2000 camera, equipped with the 45° lens, at the temperature of the shaven patch obtained using five a distance of 4.0 m. The heifer was housed indoors in an infrared imaging technologies from seven distances. The individual free-stall where the images were also taken. overall mean ± SD, for each technology and across differ- Infrared images were taken of the left and right sides of ent distances, for the i40, T250, SC2000-12°, SC2000-24° the trunk of the animal (Fig. 9), upon ensuring the heifer and SC2000-45° was 34.4 ± 1.2, 35.2 ± 0.7, 35.5 ± 0.5, was standing for 30 min and had a dry hair coat free of 35.7 ± 0.7, and 35.7 ± 0.9 °C respectively. The overall debris. mean ± SD for each distance, namely 1.0, 1.5, 3.5, 5.5, 9.5, 11.5 and 15.5 m from the targeted body location Data analysis was 36.1 ± 0.7, 36.2 ± 0.6, 35.5 ± 0.1, 35.3 ± 0.6, 35.0 ± 0.7, Descriptive statistics (average, standard deviation, max- 34.7 ± 0.8 and 34.2 ± 1.4. imum and minimum values) and Pearson correlation analysis for all the nine trials, except pregnancy status, were conducted using the means and correlation proce- Judge comparison trial dures of the statistical analysis system (version 9.1, SAS Results indicate a strong association between the in- Institute, U.S.A.). The mean procedure was employed on frared imaging results obtained by each of the two the dataset of the following trials: physical exercise, drug judges, with a correlation of 0.96 and 0.98 (P < 0.05) response, wind, debris on body surface, and sunlight between the judges for the average and maximum tem- exposure; in order to calculate the descriptive statistics peratures respectively, across the six body locations of the distinct events within each of these trials (i.e. base- studied (coronary band, eye, hind foot, hind area, right line readings and experimental treatment responses). For flank and snout) (Fig. 3). Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 6 of 16 Table 2 Correlations between infrared imaging measures (average and maximum temperatures) taken from snout and eye Group Comparison Snout Eye Maximum Average Maximum Average Group 1 Images 1 and 2 (day 1) 0.97* 0.99* 0.95* 0.96* Images 1 and 2 (day 2) 0.91* 0.99* 0.82* 0.97* Average day 1 and 2 0.28** 0.34* 0.13 0.37* Group 2 Image 1 and 2 (day 1) 0.76* 0.98* 0.79* 0.96* Image 1 and 2 (day 2) 0.91* 0.93* 0.87* 0.95* Average day 1 and 2 0.16 0.31** 0.22 0.45* *P < 0.05; ** 0.05 < P ≤ 0.10 Images were taken from two groups of calves (Group 1 and Group 2) on two different days (Day 1 and Day 2), with two consecutive images in each day (Image 1 and Image 2) Environmental factors Debris on body surface trial Wind trial The average relative humidity was 79.1 ± 1.6 % and the The average relative humidity was 62.8 ± 2.2 % and the average temperature was 22.7 ± 0.4 °C during evaluation average temperature was 25.4 ± 0.3 °C for the duration of the effects of debris on the body surface. The four sets of the wind trial. The wind, directed to the left side of of infrared images and heat production data collected the animal, caused an immediate and abrupt decrease in prior to adding shavings indicate a similarity between the body surface temperature at the four body locations the values of these two measures (Fig. 5). Immediately evaluated (Fig. 4a). A similar response was also observed after adding shavings, heat production was unaffected on the right side, but of a lower magnitude (Fig. 4b). but the temperature of the lumbar region drastically de- The temperature of the left and right trunk decreased creased from 32.3 to 19.0 °C (Fig. 5). The temperature of from 36.5 to 31.9 °C and 36.2 to 33.4 °C, respectively, in the lumbar region subsequently rose to 28.6 °C after response to the wind. Figure 4 illustrates a lack of asso- 20 min, and continued to increase at a slower pace until ciation between heat production and infrared traits dur- 40 min after when the shavings were brushed off. After ing the period that the animal was subjected to wind on brushing, the temperature of the lumbar region was the its left side, and a re-establishment of such association highest observed throughout the entire trial, and showed after the fan was turned off. a significant mismatch with heat production (Fig. 5). Fig. 2 Infrared imaging measures by different camera types and lenses and at different distances from the flank clipped area Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 7 of 16 Fig. 3 Infrared imaging measures by two judges for maximum (solid shapes) and average (open shapes) temperatures at six body locations Sunlight exposure trial the right flank (changing from 38.1 to 41.4 °C) and smallest During the sunlight exposure trial the average solar ra- change at the eyeball (changing from 37.2 to 38.1 °C). diation was 1024.8 ± 80.6 μmol/m s, the average relative humidity was 51.6 ± 1.4 %, the average temperature was Biological factors 35.1 ± 0.7 °C and the air was still (wind speed was 0 km/h). Physical exercise trial Figure 6 shows the averages of heart rate, respiration rate The average relative humidity was 73.2 ± 2.7 % and the and infrared traits over the three portions of the trial (base- average temperature was 20.9 ± 0.1 °C during the phys- line, sunlight exposure, and shade period), as well as the ical exercise trial. The exercise trial revealed a notice- environment temperature. The weather parameters of solar able increase in heat production and temperature for all radiation, relative humidity, wind speed, and temperature body locations studied following the exercise treatment all remained stable throughout the trial. Heart rate aver- (Fig. 7). For example, the clipped left flank increased aged 72.8 ± 16, 69.5 ± 22, and 70.5 ± 14 beats/min during from 34.4 to 38.0 °C right after exercise. Respiration rate the baseline, sunlight exposure and shade period respect- at baseline was 29.2 counts/min and increased to 80.1 ively. The respiration rate averaged 36.3 ± 7.3, 51.5 ± 13.4 counts/min immediately post-exercise. Changes in and 48.9 ± 12.1 counts/min during the baseline, sunlight body surface temperature due to physical exercise were exposure and shade period respectively, with the highest mirrored by heat production; the strongest association respiration ratefor thesunlightexposureperiodobserved was observed with the snout, which increased in shortly after moving the cows into sunlight (Fig. 6). The temperature from 32.6 to 33.5 °C when heat produc- values for all infrared imaging traits increased immediately tion increased. The weakest association was observed following exposure to sunlight. About 7 min after moving with the eyeball, which decreased in temperature from the animals to the shade, values returned to approximately 34.2 to 32.8 °C as heat production increased (Fig. 7). At those observed during the baseline portion, while the res- 5.0 min post-exercise, the increased heat production piration rate remained elevated (Fig. 6). Sunlight exposure returned to values similar to those observed during the caused the greatest change in body surface temperature at baseline assessment. Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 8 of 16 Fig. 4 Infrared imaging measures and heat production in response to wind. (a) left and (b) right sides of the animal in response to a wind being blown on the left side of the animal. The solid and open arrows denote the fan being turned on and off Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 9 of 16 Fig. 5 Infrared imaging measures and heat production in response to shavings partially covering the animal skin surface. The solid and open arrows denote the spread and removal of shavings on the lumbar region of the animal Drug response trial side having a well-delimited warmer region. The average During the conduction of the first and second portions of temperatures on the warmer region and the adjacent re- the drug trial, the average relative humidity was 73.8 ± gion to this right side were 30.3 °C (maximum = 31.2 °C, 2.9 % and 74.2 ± 2.6 % and the average temperature was minimum = 29.3 °C, SD = 0.5) and 28.7 °C (maximum = 23.9 ± 0.7 and 22.6 ± 0.6 °C, respectively. The first portion 29.4 °C, minimum = 27.1 °C, SD = 0.3), respectively. of the drug trial using xylazine only is illustrated in Fig. 8a. Heat production, upon administration of xylazine, de- Discussion creased from 376.6 to 359.4 W. A greater decrease in heat Technological factors production was observed in the second portion of the Imaging repeatability trial drug trial (Fig. 8b), where heat production decreased from As expected, the first study indicates a low association 429.5 to 319.4 W with xylazine administration. Addition- between infrared images taken on different days. This ally, the effect of xylazine on metabolic rate was reversed suggests that infrared imaging does not exhibit the strong by administration of atipamezole, as heat production repeatability of traditional routine practices employed values returned to values similar to those at baseline within commercial (beef) cattle operations for assessing (Fig. 8b). Changes in body surface temperature due to production characteristics, such as ultrasound for body drug administration were similar to the heat production composition [27, 28] and body weight [29]. This obser- pattern, with the strongest associations observed for the vation reflects the sensitivity of infrared imaging to right flank and weakest for the coronary band (Fig. 8a, b). metabolic state and environmental conditions, which would affect long term repeatability of other assessments (i.e. heart Pregnancy status trial and respiration rate) rooted in the metabolic state. This Infrared assessment of pregnancy status was conducted at lack of consistency was not observed when consecutive 20.4°Cand with arelativehumidityof54%.Figure9shows images (within 10 s) were taken; suggesting that con- images of the right and left sides of the Holstein heifer 2 d straints should be defined for proper infrared assess- before calving. A noticeable temperature difference at the ment over longer time periods. For example, factors ventro-caudal portion of the trunk was observed when left such as ambient conditions [30] and familiarization with and right sides were compared (Fig. 9a, b), with the right handling and management practices [31], were relatively Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 10 of 16 Fig. 6 Infrared imaging measures, ambient temperature, heart and respiration rates of beef cows in response to sun or shade exposure. The solid and open arrows denote the start and end of the sun light exposure uncontrolled in this study and may easily cause bias in measureanobjectfromagivendistance[33].Despite thethermographs. Theexposureofcattletoa several variation between infrared imaging technologies across uncontrolled infrared imaging artifacts, including rou- different distances to the target (shaven patch), the ob- tine cattle handling and housing in commercial settings, servation that all the different equipment had consistent may skew assessments by impairing regular radiation results for images taken up to 1.5 m from the target was emission patterns from the body surface [32]. In es- remarkable. Such an observation indicates the possibil- sence, this initial study provides perspective for a series ity of using simpler technologies for performing infrared of eight studies aimed to further illustrate the boundar- imaging in animals at close distances, which would be ies of using infrared imaging for monitoring cattle in feasible in commercial operation set-ups (i.e. infrared commercial operations. devices mounted onto feeding stations), and improve economical reach and use of this technology. Similarly, Distance and infrared cameras comparison trial infrared assessments at known distances to the object Distance to the object is an influential factor on the results may aid in avoiding bias due to variation in distance and of an infrared imaging assessment due the effects on the may be easily implemented with automated infrared im- captured radiation by infrared imaging devices [19]. Our re- aging devices. Schaefer et al. [9] presented an intriguing sults indicate an overall decrease in temperature (Fig. 2) as example of an automated infrared imaging system distance to the 5 by 5 cm shaven patch on the flank of the which accommodated distance, resolution and other heifer increased (Fig. 1aj). This effect was due to the de- imaging issues to aid in early detection of an inflamma- creased number of pixels encompassing the targeted tory respiratory disease in cattle at the feeding station. patch as a result of the increased distance, and was more prominent in the equipment with the lowest infra- red imaging range (the i40; Fig. 2). Indeed, the fewer the Judge comparison trial pixels, as for camera i40 images, the lower the spot:size Infrared imaging evaluation is another key aspect of ratio that indicates the ability of an infrared camera to a promising thermographic assessment program. The Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 11 of 16 Fig. 7 Infrared imaging measures, heat production and respiration rate in response to physical exercise. The solid and open arrows denote the start and end of the exercise challenge current study demonstrated an outstanding agreement [36]. At the thermal neutral zone, heat production between analyses of thermographs made by two judges through radiation is at a maximum, increasing the cap- in six body locations, following a pre-established im- acity to make inferences on total heat production through aging protocol. The benefits of a pre-established infra- detection of emitted radiation via infrared imaging. In our red imaging analysis protocol were also demonstrated study, the room temperature was above the Bos taurus by Ammer [34] when comparing studies that analyzed thermoneutral zone. For high-producing cattle with high the same body locations and concluded that variations intakes of metabolizable energy, such as those used in this of shapes and sizes of the measurement areas affected study, the upper temperature limit may be closer to 20 °C the precision of the body surface temperature readings. [37]. However, the room temperature was still within the Similarly, a standardized landmark protocol established range where radiant heat loss is significantly important to for capturing a series of thermographs over the entire regulate body temperature [38]. The wind caused an in- human body yielded consistent results [1]. In contrast, crease in convective heat loss that is primarily dependent analysis of magnetic resonance images compared across on the movement of the air, which has been reported to judges without a pre-defined imaging analysis protocol affect body surface temperature in cattle [30]. Similarly, resulted in repeatability values of 0.4 [35]. This evidence while studying heat loss in emu, Maloney & Dawson [39] reinforces the benefits of establishing imaging analysis observed that increased wind speeds decreased heat load protocols. Such protocols should be repeatable across from radiation. In our study, wind caused a cooling effect judges and may eventually be incorporated within auto- on the body surface that contradicted the close association mated imaging analysis as part of a user-friendly tech- between heat production and radiant heat captured by the nology for commercial operations. infrared camera under still air conditions. Therefore, wind drafts that are a common event in handling facilities may Environmental factors mask the association between infrared measures and Wind trial metabolic rate. The fact that the strong association be- Physical properties of heat loss in response to ambient tween infrared imaging readings and metabolic rate was conditions are important factors to consider when evalu- quickly re-established after ceasing the wind (Fig. 4) indi- ating heat loss and body surface temperature patterns cates that minimizing the effects of wind might be Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 12 of 16 Fig. 8 Infrared imaging measures and heat production in response to drugs. (a) Response to xylazine administration (only). (b) Response to xylazine followed by atipamezole administration. The solid and open arrows denote the injection of xylazine and atipamezole Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 13 of 16 Fig. 9 Infrared images of the left (a) and right (b) sides of the trunk of a pregnant cow. Arrows are pointing to the lower abdomen on both sides. The thermal print of the fetus on the right side is noticeable achieved through simple management adjustments and increase in local heat dissipation [43]. Thus, our observa- practices (i.e. wind breaks) at locations where the infrared tion likely reflects this local heating generated by increased images are taken. blood flow. This will have implications for infrared im- aging in commercial set-ups, since cattle may rub their Debris on body surface trial bodies during handling or as part of their general behav- Similar to the wind trial, the shavings affected body ior. This can generate similar stimuli within the skin, surface temperatures with no corresponding fluctuations resulting in unexpected and increased local heat dissipa- in heat production. Interestingly, shavings resulted in a tion inconsistent with metabolic state. conductive cooling effect with heat being transferred from the higher temperature (animal) to lower tempera- Sunlight exposure trial tures (cooled shavings) through contact [36]. Even The total infrared radiation captured through infrared im- though heat loss through conduction is a minor con- aging from an object represents the sum of emitted, trans- tributor to the total heat loss in standing animals [40], mitted and reflected radiation [39]. In the context of these results indicate possible impairments in emitted infrared imaging in animals, a combination of emitted plus radiation by the animal, at least temporarily. It is also reflected radiation is obtained when thermographs are taken important to highlight the fast return of an association under direct sunlight. In the present study, cattle were between body surface temperature and heat production a exposed to sunlight at both high humidity and ambient few minutes after spreading cooled debris, indicating an temperature. These factors combined altered the emitted area for optimizing handling practices. It is common to radiation due to thermoregulatory adaptations by the ani- observe debris on cattle and there are studies demonstrat- mal, as demonstrated by the increase in respiration rate, ing substantial effects of the amount of body coverage on indicating a greater heat loss as evaporative heat [44]. Inter- thermoregulation and nutritional requirements [41]. Add- estingly, heart rate, a measure that can also indicate meta- itionally, the type of debris should also be considered in bolic changes, was unaffected by sunlight exposure. As relation to thermo-imaging properties. A study by van reviewed by Brosh [45], an increase in heart rate is expected Liere [42] involving plumage in dust-bathing birds, found in cattle kept under extreme and prolonged heat load, which differences in temperature of the birds depending on the is a more severe scenario than the conditions of our study. type of litter used for dust-bathing. Regarding changes in reflected radiation, moving the ani- When the shavings were brushed off the animal there mal from shade to sunlight caused the body surface to re- was a noticeable increase in the local temperature, which flect solar radiation in addition to the emitted radiation was unaccompanied by an increase in heat production from the animal, both of which were captured in the ther- (Fig. 5). It has been demonstrated that scratching causes mographs. This resulted in a thermal imaging artifact where an increase in peripheral blood flow, resulting in an body surface temperature was apparently increased and Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 14 of 16 subsequently decreased with sunlight and shade exposure sedative effects we observed in the animals were com- respectively. Our study also indicated a rapid return to body parable to other studies [50]. Conversely, atipamezole is surface temperatures similar to those observed during the known to provide a rapid reversal of xylazine-induced baseline readings, upon 7 min of returning the cows to the sedation and immobilization [51, 52]. Other studies shaded area. Similarly, dairy cows that chose shaded areas have investigated the effects of drugs on the metabolic to rest were found to have decreased surface temperature rate and skin temperature in the bovine [23], as well as after 10 min of staying in the shade [30]. It is also interest- the potential of anti-sedatives to reverse the metabolic ing to observe that the snout temperature decreased below effects of sedatives [53, 54]. Our study highlights the the baseline readings after returning the cows to the shade. need to consider the significant effects of drugs on ani- This biological response is probably due to changes in the mal heat and temperature patterns while performing peripheral vascularization patterns during heat dissipation, procedures that require chemical restriction, as well as as illustrated elsewhere [26]. Considering the dramatic ef- use of infrared imaging in research models to evaluate fects of solar loading on captured radiation from the body the metabolic effects of administered drugs. surface, this potential for bias should be considered in the thermography assessment of cattle subjected to sunlight ex- Pregnancy status trial posure prior to infrared imaging. The reflected environ- Pregnancy is a biological phenomenon that may be de- mental radiation could also be largely accounted for, which tected through infrared imaging due to the considerably is an alternative to minimizing the effects of solar load on higher metabolic rate of the fetus relative to that of the the thermographs (i.e. by protocols and management prior dam [55]. This discrepancy results in heat transfer by to the imaging). conduction through the tissue layers to the body surface, resulting in a comparatively warmer region detectable Biological factors through infrared imaging. Remarkably, other studies Physical exercise trial have reported similar uses in a diversity of species such Physical exercise is known to produce an increase in as giant pandas [56] and horses [22]. These studies, metabolic rate [46], affecting the amount of heat pro- along with our own, indicate the potential for identifying duced and the means employed to dissipate heat [36]. pregnancy at its later stages, where the substantial meta- Herein we note a substantial increase in heat production bolic output of the fetus is capable of producing enough in response to exercise which is consistent with results heat to form thermal print. In our study, the observation observed by Folkow & Mercer [47] across different am- of a thermal print on the right side of the cow likely bient temperatures and climate conditions. Similarly, el- indicated that the fetus was located within the right horn evated respiration rate in response to exercise is a of the uterus, which may be a frequent occurrence [57, 58]. known indicator of increased metabolic rate, as reported While pregnancy status may be predicted using infrared elsewhere [21, 48]. The association between heat pro- imaging, these observations suggest that the use of duction and infrared imaging measures in cattle is infrared imaging for pregnancy checks should be further known [13], as well as the ability of body extremities to evaluated to determine the earliest gestational stage for regulate body temperature [13, 26]. This evidence sup- such an assessment. Jones et al. [59] conducted a ports the close association observed between infrared preliminary study applying infrared imaging to detect measures of extremities and fluctuations in metabolic pregnancy in dairy heifers and concluded that this form rate. Considering the tremendous variation in cattle of assessment was confounded with ambient tem- temperament during handling [31] and the respective perature and considered questionable; gestational stage, effects of exercising on metabolic rate, physical exercise however, was not described. can be considered a major bias while assessing metabolic rate. However, the observation that the metabolic rate Conclusion returned to similar values as observed during the base- The three categories of factors influencing infrared im- line readings indicates the potential for avoiding this aging in cattle considered here illustrated both the oc- confounding factor by standardizing the infrared im- currence of biases that can skew quality of the infrared aging procedure in handled and restrained cattle. imaging and possibilities for creating undesirable effects on infrared assessment. The use of such technology under Drug response trial relatively random conditions can result in misleading as- The decrease and re-establishment of body surface sessments, similar to the use of other biologically-sensitive temperature and metabolic rate upon administration of measures. Indeed, the proper choice of equipment for a a sedative and an anti-sedative were expected (Fig. 8a; b). given application and imaging analyses plan, as well as the Xylazine causes sedation and is associated with a avoidance of environmental or biological biases, may hypothermic response in animals [49]. The duration of maximize the successful application of infrared imaging in Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 15 of 16 livestock production systems. Infrared imaging has tre- 12. Paulrud CO, Clausen S, Andersen PE, Rasmussen MD. Infrared thermography and ultrasonography to indirectly monitor the influence of liner type and mendous potential for assessing aspects of bovine physi- overmilking on teat tissue recovery. Acta Vet Scand. 2005;46:137–47. ology related to health and productivity, which could 13. Montanholi YR, Odongo NE, Swanson KC, Schenkel FS, McBride BW, Miller SP. ultimately bring benefits to the livestock industry. Application of infrared thermography as an indicator of heat and methane production and its use in the study of skin temperature in response to physiological events in dairy cattle (Bos taurus). J Therm Biol. 2008;33:468–75. Competing interests 14. Montanholi YR, Swanson KC, Schenkel FS, McBride BW, Caldwell TR, Miller The authors declare that they have no competing interests. SP. On the determination of residual feed intake and associations of infrared thermography with efficiency and ultrasound traits in beef bulls. Livest Sci. 2009;125:22–30. Authors’ contributions 15. Coulter GH, Senger PL, Bailey DRC. Relationship of scrotal surface The research trials were planned and conducted by YM, BS, AM, ML and KG. temperature measured by infrared thermography to subcutaneous and The dry lab work was conducted by BS, ML and KG. SM and KS provided deep testicular temperature in the ram. J Reprod Fertil. 1988;84:417–23. mentorship on the infrared camera utilization and helped with the support 16. Halachmi I, Polak P, Roberts DJ, Klopcic M. Cow body shape and for administrating and developing the study. YM, ML, BS, AM and KG prepared automation of condition scoring. J Dairy Sci. 2008;91:4444–51. the manuscript. All authors assisted with editions on the manuscript and 17. Tong AL, Schaefer AL, Jones SDM. Detection of poor quality beef using approved the final manuscript. infrared thermography. Meat Focus Int. 1995;4:443–5. 18. Mitchell M. Thermal imaging: thermoregulation in relation to animal Acknowledgments production and welfare. In: Luzi F, Mitchell M, Nanni Costa L, Redaelli V, We would like to thank the Beef Producers of Ontario, Ontario Ministry of editors. Thermography: current status and advances in livestock animals and Agriculture and Rural Affairs, Beef Cattle Research Council and Agri-Food in veterinary medicine. Brescia, Italy: Fondazione Iniziative Zooprofilattiche e Canada for financial support. The support of the staff at Elora Beef Research Zootecniche; 2013. p. 147–62. Center and the staff at Elora Dairy Research Center is also acknowledged. 19. Minkina W, Dudzik S. Infrared thermography errors and uncertainties. United States: Natick; 2009. Author details 20. Schutz KE, Rogers AR, Cox NR, Webster JR, Tucker CB. Dairy cattle prefer shade Department of Animal and Poultry Science, University of Guelph, Guelph, over sprinklers: effects on behavior and physiology. J Dairy Sci. 2011;94:273–83. ON N1G 2W1, Canada. Department of Plant and Animal Sciences, Dalhousie 21. Ueno T, Takemura Y, Shijimaya K, Ohtani F, Furukawa R. Effects of high University, Truro, NS B2N 5E3, Canada. Monsanto, Headingley, MB R3T 6E3, environmental temperature and exercise on cardiorespiratory function and Canada. Agriculture and Agri-Food Canada, Lethbridge, AB T1J 4B1, Canada. metabolic responses to stress. Jpn Agric Res Q. 2001;35:137–44. Faculty of Veterinary Medicine, University of Calgary, Calgary, AB T2N 4Z6, 22. Bowers S, Gandy S, Anderson B, Ryan P, Willard S. Assessment of pregnancy Canada. Invermay Agricultural Centre, AgResearch Limited, Mosgiel 9053, in the late-gestation mare using digital infrared thermography. Therigenology. New Zealand. 2009;72:372–7. 23. Findlay JD, Robertshaw D. The mechanism of body temperature changes Received: 16 February 2015 Accepted: 10 June 2015 induced by intraventricular injections of adrenaline, noradrenaline and 5-hyodropytryptanime in the ox (Bos taurus). J Physiol. 1967;189:329–36. 24. Odongo NE, AlZahal O, Las JE, Kramer A, Kerrigan B, Kebreab E, et al. Data capture: development of a mobile open-circuit ventilated hood system for References measuring real-time gaseous exchange in cattle. In: France J, Kebreab E, 1. Ring EFJ. The historical development of temperature measurement in editors. Mathematical modelling in animal nutrition. Wallingford, United medicine. Infrared Phys Technol. 2004;49:297–301. Kingdom: CABI Publishing; 2008. p. 225–40. 2. Barbieri BB, McLellan WA, Wells RS, Blum JE, Hofmann S, Gannon J, et al. 25. Gaughan JB, Holt SM, Hahn GL, Mader TL, Eigenberg R. Respiration rate–is it Using infrared thermography to assess seasonal trends in dorsal fin surface a good measure of heat stress in cattle? Asian-Australas J Anim Sci. temperatures of free-swimming bottlenose dolphins (Tursiops truncatus)in 2000;13(Suppl C):329–32. Sarasota Bay, Florida. Mar Mamm Sci. 2010;26:53–66. 26. Whittow GC. The significance of the extremities of the ox (Bos taurus)in 3. Koerth BH, McKown CD, Kroll JC. Infrared-triggered camera versus helicopter thermoregulation. J Agric Sci. 1962;58:109–20. counts of White-tailed deer. Wildl Soc Bull. 1997;25:557–62. 27. Hassen A, Wilson DE, Willham RL, Rouse GH, Trenkle AH. Evaluation of ultrasound 4. Weissenbock NM, Weiss CM, Scwammer HM, Kratochvil H. Thermal windows measurements of fat thickness and longissimus muscle area in feedlot cattle: on the body surface of African elephants (Loxodonta africana) studied by assessment of accuracy and repeatability. Can J Anim Sci. 1998;78:277–85. infrared thermography. J Therm Biol. 2010;35:182–8. 28. Brethour JR. The repeatability and accuracy of ultrasound in measuring 5. McCafferty DJ, Gilbert C, Paterson W, Pomeroy PP, Thompson D, Currie JI, backfat of cattle. J Anim Sci. 1992;70:1039–44. et al. Estimating metabolic heat loss in birds and mammals by combining 29. Roche JR, Macdonald KA, Burke CR, Lee JM, Berry DP. Associations among infrared thermography with biophysical modelling. Comp Biochem Physiol. body condition score, body weight, and reproductive performance in 2011;158:337–45. seasonal-calving dairy cattle. J Dairy Sci. 2007;90:376–91. 6. Luzi F, Mitchell M, Nanni Costa L, Redaelli V. Thermography: current status 30. Schutz KE, Rogers AR, Poulouin YA, Cox NR, Tucker CB. The amount of and advances in livestock animals and in veterinary medicine. Brescia, Italy: shade influences the behavior and physiology of dairy cattle. J Dairy Sci. Fondazione Iniziative Zooprofilattiche e Zootecniche; 2013. 2010;93:125–33. 7. Colak A, Polat B, Okumus Z, Kaya M, Yanmaz LE, Hayirli A. Early detection of 31. Grandin T. Assessment of stress during handling and transport. J Anim Sci. mastitis using infrared thermography in dairy cows. J Dairy Sci. 1997;75:249–57. 2008;91:4244–8. 32. Ludwig N. Infrared history and applications. In: Luzi F, Mitchell M, Nanni 8. Nikkhah A, Plaizier JC, Einarson MS, Berry RJ, Scott SL, Kennedy AD. Infrared Costa L, Redaelli V, editors. Thermography: current status and advances in thermography and visual examination of hooves of dairy cows in two livestock animals and in veterinary medicine. Brescia, Italy: Fondazione stages of lactation. J Dairy Sci. 2005;88:2749–53. Iniziative Zooprofilattiche e Zootecniche; 2013. p. 27–36. 9. Schaefer AL, Cook NJ, Bench C, Chabot JB, Colyn J, Liu T, et al. The non-invasive 33. Redaelli V, Caglio S. Thermal imaging theory. In: Luzi F, Mitchell M, Nanni and automated detection of bovine respiratory disease onset in receiver calves Costa L, Redaelli V, editors. Thermography: current status and advances in using infrared thermography. Res Vet Sci. 2012;93:928–35. livestock animals and in veterinary medicine. Brescia, Italy: Fondazione 10. Eicher SD, Cheng HW, Sorreells AD, Schutz MM. Behavioral and Iniziative Zooprofilattiche e Zootecniche; 2013. p. 41–6. physiological indicators of sensitivity of chronic pain following tail dockings. 34. Ammer K. Influence of imaging and object conditions on temperature J Dairy Sci. 2006;89:3047–51. readings from medical infrared images. Pol J Environ Stud. 2006;15:117–9. 11. Stewart M, Schaefer AL, Haley DB, Colyn J, Cook N, Stafford KJ, et al. Infrared thermography as a non-invasive method for detecting fear-related responses 35. Colagrande S, Pasquinelli F, Mazooni LN, Belli G, Virgili G. MR-diffusion weighted of cattle to handling procedures. Anim Welf. 2008;17:387–93. imaging of healthy liver parenchyma: repeatability and reproducibility of Montanholi et al. Journal of Animal Science and Biotechnology (2015) 6:27 Page 16 of 16 apparent diffusion coefficient measurement. J Magn Reson Imaging. 2010;31:912–20. 36. Kleiber M. The fire of life. New York, United States: John Wiley & Sons, Inc; 1961. 37. Brown-Brandl TM, Eigenberg RA, Nienaber JA. Heat stress factors of feedlot heifers. Livest Sci. 2006;105:57–68. 38. Robertshaw D. Heat loss of cattle. In: Yousef MK, editor. Stress physiology in livestock. Vol. I. Basic principles. Boca Raton, FL, USA: CRC Press; 1985. p. 55–66. 39. Maloney SK, Dawson TJ. The heat load from solar radiation on large, diurnally active bird, the emu (Dromaius novaehollandiae). J Therm Biol. 1995;20:381–7. 40. Cunningham JG. Textbook of veterinary physiology. Philadelphia, United States: The Curtis Center; 2002. 41. NRC. Nutrient requirements of beef cattle. Washington, United States: National Academy Press; 1996. 42. van Liere DW. The significance of fowls’ bathing in dust. Anim Welf. 1992;1:187–202. 43. Yosipovitch G, Fast K, Bernhard JD. Noxious heat and scratching decrease histamine-induced itch and skin blood flow. J Investig Dermatol. 2005;125:1268–72. 44. Hales JRS. Interactions between respiratory and thermoregulatory systems of domestic animals in hot environments. Prog Biometeorol. 1976;1:123–31. 45. Brosh A. Heart rate measurements as an index of energy expenditure and energy balance in ruminants: a review. J Anim Sci. 2007;85:1213–27. 46. McLean JA, Tobin G. Animal and human calorimetry. Melbourne, Australia: Cambridge University Press; 1987. 47. Folkow LP, Mercer JB. Partition of heat loss in resting and exercising winter- and summer insulated reindeer. Am J Physiol Regul Integr Comp Physiol. 1986;251:32–40. 48. Ingram DL, Whittow GC. The effects of variations in respiratory activity and in the skin temperatures of the ears on the temperature of the blood in the external jugular vein of the ox (Bos taurus). J Physiol. 1962;163:211–21. 49. Livingston A, Low J, Morris B. Effects of clonidine and xylazine on body temperature in the rat. Br J Pharmacol. 1984;81:189–93. 50. St Jean G, Skarda RT, Muir WW, Hoffsis GF. Caudal epidural analgesia induced by xylazine administration in cows. Am J Vet Res. 1990;51:1232–6. 51. Arnemo JM, Soli NE. Reversal of xylazine-induced sedation in dairy calves with atipamezole: a field trial. Vet Res Commun. 1993;17:305–12. 52. Lee I, Yamagishi N, Oboshi K, Yamada H. Antagonistic effects of intravenous or epidural atipamezole on xylazine-induced dorsolumbar epidural analgesia in cattle. Vet J. 2003;166:194–7. 53. Clarke KW, England GCW. Medetomidine, a new sedative-analgesic for use in the dog and its reversal with atipamezole. J Small Anim Prac. 1989;30:343–8. 54. Skarda RT, Jean GS, Muir WW. Influence of tolazoline on caudal epidural administration of xylazine in cattle. Am J Vet Res. 1990;51:556–60. 55. Ferrell CL, Reynolds LP. Uterine and umbilical blood flows and net nutrient uptake by fetuses and uteroplacental tissues of cows gravid with either single or twin fetuses. J Anim Sci. 1992;70:426–33. 56. Durrant BS, Ravida N, Spady T, Cheng A. New technologies for the study of carnivore reproduction. Theriogenology. 2006;66:1729–36. 57. Aubry P, Warnick LD, DesCoteaux L, Bouchard E. A study of 55 field cases of uterine torsion in dairy cattle. Can Vet J. 2008;49:366–72. 58. Frazer GS, Perkins NR, Constable PD. Bovine uterine torsion: 164 hospital referral cases. Theriogenology. 1996;46:739–58. 59. Jones M, Denson A, Williams E, Graves K, Dos Santos A, Kouba A, et al. Assessing pregnancy status using digital infrared thermal imaging in Holstein dairy heifers. J Anim Sci. 2005;88:40–1. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit
Journal
Journal of Animal Science and Biotechnology – Springer Journals
Published: Jun 12, 2015