Comparison of Rectal and Infrared Thermometry Temperatures in Anesthetized Swine (Sus Scrofa)

Comparison of Rectal and Infrared Thermometry Temperatures in Anesthetized Swine (Sus scrofa)

Kerrie L Farrar,1,* Amy E Field,3 Sarah L Norris,2 and Kenneth O Jacobsen1

Infrared thermometry (IRTM) is a noncontact method to measure temperature. The purpose of this study was to compare rectal temperature and IRTM in healthy anesthetized swine, with the hypothesis that IRTM would be an accurate, noninvasive alternative for rectal temperature measurement. Two groups of female Yorkshire-cross swine (n = 14 and n = 12) were sedated with Tiletamine–zolazepam (0.5 mg/kg) for blood collection during a routine physical examination. While sedated, rectal temperatures were measured using a SureTemp Plus 690 (Welch Allyn) and IRTM measurements were taken using a FLIR E5 thermal imaging camera. The 2 anatomic sites used for thermography measurements were the area surrounding the eye and the neck at the base of the ear. The distance from the imaging camera and the animal during IRTM measurements was 24 to 32 inches, a distance that would allow camera access in a standard swine enclosure. The infrared imaging camera’s surface temperature measurement exhibited a proportional bias when compared with the rectal temperature. All rectal temperature measurements were between 98.7 °F to 101.3 °F, with a mean temperature of 100.4 °F. IRTM tended to underestimate rectal temperatures at lower values, and overestimate rectal temperatures at higher values by approximately (+) or (-) 0.8 °F of rectal temperature. Infrared thermometry can provide a quick noninvasive assessment of the body surface temperature, without the need for animal handling or restraint, but should not be considered an accurate replacement for rectal temperature measurement.

Abbreviations: IRTM, infrared thermometry; IRT, infrared thermography

DOI: 10.30802/AALAS-JAALAS-19-000119

Body temperature is an important vital parameter in the thermography has been found to provide useful information veterinary assessment of an animal’s health status. One of the on tissue perfusion with flap reconstructions.11 It has also most frequently used methods of assessing body temperature in been found useful as a method to add functional information veterinary medicine is through rectal temperature measurement. for conditions such as inflammatory arthritis, muscle injury, While generally innocuous, depending on the temperament or complex regional pain syndrome, peripheral circulation, fever condition of the animal this can be both a stressful and poten- screening, tumor development, and evaluation of specific der- tially harmful procedure.18 Since stress from handling alone matological conditions.7,9,16 However, limitations to the use of can alter both core and surface body temperature, a noncontact IRTM have also been described in the literature. These include method would represent a technical refinement.4,6,8,18 Infrared variability in readings depending on ambient temperature, thermometry (IRTM), or infrared thermography (IRT), is a variability in readings based on the equipment, and variation noninvasive, noncontact method to measure body temperature in surface temperature based on the anatomic location used for that may offer a viable alternative for attaining an accurate measurement.1,17 temperature measurement in swine. IRTM based temperature recording in pigs has been in- The medical implications of having a noninvasive and non- vestigated in studies of heat stress, neonatal survival, and contact method for estimating temperature are both significant production.5,12,15,17 Currently, IRTM and rectal temperature have and varied. In swine IRTM was found to be a reliable method not been compared in healthy unstressed pig populations. The to assess thermal status in piglets,12 to estimate the rectal tem- purpose of this study was to evaluate the accuracy of infrared perature in gnotobiotic piglets,4 to detect febrile behavioral thermometry in comparison to rectal temperature in healthy differences in groups of weaned piglets,5 and as an imaging anesthetized swine. The hypothesis of this study was that IRTM technique for the diagnosis of respiratory infection.14 Renal is an accurate noninvasive alternative for rectal temperature surgery using the swine model also found IRT to be accurate measurement in swine. in renal temperature monitoring.13 In small rodents, body temperature has been used to make recommendations regard- Materials and Methods ing the humane endpoint of studies, which makes access to a Animals. Juvenile female Yorkshire-cross swine (n = 26) rapid, noninvasive method of body temperature measurement were obtained from Midwest Research Swine (Gibbon, MN). 6 of particular interest. In human medicine, dynamic infrared Pigs were all approximately 12 to 15 wk of age and weighed approximately 30 to 45 pounds. The source herd was free of pseudorabies, brucellosis, porcine respiratory and reproductive Received: 13 Aug 2019. Revision requested: 23 Sep 2019. Accepted: 29 Oct 2019. 1Veterinary Medicine Division, 2Statistics Division, United States Army Medical Research syndrome, swine influenza, swine dysentery, erysipelas, and Institute of Infectious Diseases, Fort Detrick, Maryland; 3Research Support Division, US Bordetella bronchiseptica. The pigs were housed in indoor runs Army Institute of Surgical Research, JBSA Fort Sam Houston, Texas and fed a standard laboratory diet (Lab Diet 5081, St Louis, MO) *Corresponding author. Email: [email protected]

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Figure 1. 3D Computed tomography scan of a pig head showing vasculature in association with skeletal structures. IRTM measurement locations were selected based on prominent vasculature, which in turn corresponded to the spot-meter locations highlighted by the thermography camera. with water provided from an automated watering system ad base of the ear (Figure 2 B). The temperature in both locations libitum. The pigs were sedated with Tiletamine–zolazepam (0.5 was attained using the IRTM camera feature that measures the mg/kg) for routine physical examination and blood collection. most consistent highest temperature recording within an area. During the examination, both rectal and IRTM temperatures This is visible within the field of view in a moving spot-meter. were measured and recorded, concurrently. Research was Rectal temperature measurements were taken using a conducted in compliance with the Animal Welfare Act,2 the SureTemp Plus 690 (Welch Allyn) thermometer. This model of implementing Animal Welfare Regulations,3 and the principles thermometer has a calibration accuracy of ± 0.2 °F (± 0.1 °C), of the Guide for the Care and Use of Laboratory Animals.10 The ambient temperature range of 50 °F (10 °C) to 104 °F (40 °C), and facility’s Institutional Animal Care and Use Committee ap- a patient temperature range of 80 °F (26.7 °C) to 110 °F (43.3 °C). proved all research conducted in this study. The facility where The temperature probe was inserted approximately 10 cm into this research was conducted is fully accredited by AAALAC. the rectum of the sedated pig and held for approximately 10 to Temperature measurement. The IRTM measurements were 13 s until a temperature reading was taken. The thermometer taken using a FLIR E5 thermal imaging camera. This specified calibration was verified prior to use using a Welch Allyn 9600 camera has 10,800 pixels (120 × 90), a temperature range of -4 Plus Calibration Tester (Welch Allyn, Skaneateles Falls, NY). (-20 °C) to 482 °F (250 °C), and thermal sensitivity of less than Data Analysis. Routine physical exam occurred in 2 groups 0.18 °F (<0.10 °C). Thermal measurements were taken with the of swine (14 and 12 animals) on different days. Ambient tem- thermal imaging camera located between 24 and 32 in. from the perature was comparable for both data collection dates. Data animal. This distance allowed for camera access in a standard consisted of temperature readings taken rectally and via IRTM at 48 by 72 in. individual swine enclosure. Three-dimensional the eye and neck. There was a recording error in which the eye Computed Tomography (CT) scan imaging was performed thermometry readings for 2 swine was missed. Only samples in several pigs demonstrating prominent vasculature in asso- that had rectal-eye or rectal-neck paired results were used in ciation with skeletal structures (Figure 1). Two anatomic sites the analyses. The analyses conducted were Pearson product- were selected for thermal measurements based on the 3D CT moment correlation to evaluate the strength of association images of prominent vasculature. The first location “Eye” was between rectal and infrared temperature, and Bland-Altman the tissue located next to the lateral canthus of the eye (Figure plots to describe the agreement between temperature measure- 2 A). The second location “Neck” was taken on the neck at the ments by constructing limits of agreement. A Deming regression

222 Use of infrared thermography in swine

Table 1. Correlation of rectal temperature and thermography temperature values Number of Correlation Comparison pairs (n) coefficient r( ) P value Rectal compared with eye 24 0.359 0.0845 Rectal compared with neck 26 0.432 0.0275

Figure 2. Two IRTM temperature measurement locations. (A) The first measurement was taken on the tissue at the lateral canthus of eye, and (B) the second measurement was taken at the base of the ear on the neck. The spot-meter for the hottest temperature is indicated by the black arrows. analysis was also explored, but the results were inconclusive due to the small sample size. Statistical significance was defined as a P value less than 0.05 for all tests. All analysis was performed Figure 3. Linear relationship between the between temperature read- using SAS 9.4 and Sigmaplot 13.0 statistical programs. ings. (A) Demonstrates the linear relationship for eye temperature compared with rectal temperature. (B) Demonstrates the linear relationship for neck temperature compared with rectal temperature. Results Ideal linear function of perfect correlation (red line). Observed linear The baseline rectal temperature readings for all swine function corresponding to the r value (black line). 95% confidence in- evaluated were between 98.7 °F to 101.3 °F, with an mean rectal terval around the linear function (blue line). temperature of 100.4 °F. Results from Pearson product-moment correlation of rectal and IRTM temperature values showed weak were then plotted against each other. Ideally, the mean difference correlation, (r) = 0.359 and (r) = 0.432, for both the eye and neck (bias) between the values should be close to zero, and 95% of locations of IRTM temperature measurement respectively (Table the data points should fall within 1.96 standard deviations of 1). The correlation coefficients (r) and associated P value were the mean difference (within the limits of agreement). The data statistically significant (P = 0.0275) only for the neck-based IRTM points also should show no discernable pattern of systematic temperature collection method. The scatterplot illustrates the differences, either constant or proportional. weak linear relationship between the corresponding tempera- For each of the Bland-Altman graphs, only 92% of data points ture readings (Figure 3). fall within 1.96 standard deviation of the mean difference (Fig- The Bland-Altman plots show the relationship of the differ- ure 4 and 5). Although the bias estimates are below 0 for both ences between a pair of temperature measurements and the eye and neck methods, the limits of agreement contain zero average of a pair of temperature measurements. For each sub- (Table 2). Therefore, constant bias cannot be assumed. Most ject, the difference between rectal temperature values and eye notably, a discernable pattern of proportional bias exists in both or neck temperature values was calculated. The average of the graphs. IRTM temperatures are more likely to be lower than rectal temperature values and eye (Figure 4) or neck (Figure 5) rectal temperatures until around 100.5 °F, at which point, IRTM temperature values was also calculated. These average values temperatures tend to be higher than rectal temperatures. Even

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Table 2. Bland-Altman plot relationship concerning the difference between rectal and IRTM paired temperatures. Upper limit of Standard Limits of Lower limit of agreement CI Comparison Bias deviation agreement Bias CI (95% CI) agreement CI (95% CI) (95% CI) Rectal and eye −0.78 1.23 −3.17, 1.61 −1.30 to -0.26 −4.06 to -2.27 0.72 to 2.51 Rectal and neck −0.80 1.11 −2.98, 1.39 −1.25 to -0.35 −3.76 to -2.20 0.61 to 2.17 with the proportional bias, IRTM temperatures were generally been published with extremely varied results.4,5,7,9,12,13,14,17,19 within (+) or (-) 0.8 °F of the corresponding rectal temperature. For example, in gnotobiotic piglets, where excessive handling is a particular concern, the surface temperature of several ana- Discussion tomic locations had significant linear relationships with rectal The results indicate that a proportional bias exists between the temperature measurement, making IRTM a potentially ideal 4 rectal temperature and IRTM temperature readings. Tempera- method of temperature evaluation. On the other hand, in some tures taken at both the eye and neck tended to underestimate cases skin surface temperature has varied greatly from core body 17,19 temperatures at lower values, and overestimate temperatures at temperature. For example, this occurs after acute heat stress higher values, in comparison to the corresponding rectal tem- in swine. When swine that have experienced acute heat stress are peratures. Although larger sample sizes may have yielded more put into thermoneutral conditions, the skin temperature cools 17 definitive results, a plethora of articles on the value of IRTM rapidly while the core body temperature can still increase. across a wide array of both human and animal medicine have Another instance of great temperature variation occurs in pigs with fever, in which the temperature of the skin increases at extremely varied degrees across the surface of the pig.19 IRTM strictly allows for a measurement of the temperature of the body surface, which exposes important limitations to this technique. One of the major limitations of IRTM involves the depth of penetration, which is generally limited to just 2 to 3 mm from the surface.7 This means that any alteration to the skin, such as scarring, sclerosis, or scabs, could affect the temperature reading.7 This form of temperature measurement would potentially be more accurate when used on animals with greater surface area to mass ratio. While newborn piglets have almost uniform skin temperature, the ability of pigs to thermoregulate increases with age.19 This has implications when IRTM is used in studies dealing with larger swine, where the reliability of paral- lel anatomic locations for temperature analysis may decrease. Another limitation of this study is the exceptionally controlled nature of the data collection. All temperature measurements were taken under sedation. This allowed very precise position- ing of the camera. If the true goal is to have a valid, noncontact, Figure 4. Bland-Altman plot showing the relationship between the dif- noninvasive temperature measurement option, then IRTM ferences between paired eye and rectal temperature. would only meet that goal if it is able to be accurately repeated in conscious pigs. Therefore, a comparison of rectal and IRTM methods, while also evaluating if the precision of measurement of temperature at a specific location could be adequately achieved in an awake, unrestrained animal is a valid area for further study. Only the answer to that question can allow us to determine the practicality of getting an accurate temperature reading on a potentially moving target and whether a consistent proportional bias in temperature difference would allow IRTM to be used to accurately estimate rectal temperature. This study was designed to evaluate the accuracy of IRTM temperature measurements compared with standard rectal temperature measurement in healthy anesthetized swine. IRTM, as a noninvasive alternative for temperature measurement, can provide an approximation of body temperature within (+) or (-) 0.8 °F of the rectal temperature. Our hypothesis that IRTM would be an accurate noninvasive alternative for rectal temperature measurement in swine was false due to the proportional bias and should not be considered an accurate replacement for rectal temperature measurement. However, this study does demonstrate IRTM may potentially be used as a quick, noninva- Figure 5. Bland-Altman plot showing the relationship between the dif- sive temperature screening tool for swine in a research setting. ferences between paired neck and rectal temperature.

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