Measurement of body temperature is essential to the evaluation of health status of animals in both clinical and research settings.1 Body temperature can be measured by several methods that are typically classified according to the invasiveness of the procedure, thermometer location, the extent of contact between the probe and the patient, and thermometer type.2–5 Invasive methods of temperature monitoring include arterial catheterization, urinary bladder catheterization, and insertion of esophageal probes.2,6,7 These methods require adequate patient sedation or restraint and technical skills to obtain temperature measurements.4,5 Whereas these invasive techniques provide the most accurate measurements of core body temperature, they are not practical for routine temperature measurement and are typically reserved for monitoring of critical patients and research settings.2,7
Rectal thermometry is currently the most clinically acceptable and relatively noninvasive method to obtain body temperature measurements in animals. Glass mercury thermometers, digital thermometers, or predictive thermometers that are in contact with the rectal mucosa for various time periods are routinely used.2,7 Glass thermometers are used less often and require a longer time to equilibrate to body temperature. Digital thermometers require less time than glass thermometers, but still typically require 45 to 60 seconds to measure rectal temperatures. Digital predictive thermometers require the shortest measurement time because they use the initial rate of temperature change to predict the final temperature reading.2,3
In veterinary medicine, rectal temperature measurement is the typical method used to estimate core body temperature.3–6,8,9 However, measurement of rectal temperature requires adequate manual restraint and, therefore, can cause stress to animals, particularly those not accustomed to manual restraint.10,11 This effect may be amplified in a research setting,8 where a study protocol may require frequent measurements.8 Furthermore, stress associated with restraint and temperature measurement may have negative physiologic effects on the animal, increasing core body temperature and potentially leading to false assumptions regarding the overall health status of the animal.7–10 A study12 of hospitalized dogs indicated that the magnitude of tachycardia and other behavioral indicators of stress were greater when temperature was measured with rectal thermometry versus other methods. Furthermore, gastrointestinal variables (eg, peristalsis and volume of fecal material) may affect temperature measurements obtained with a rectal thermometer.3–5 Because of these factors, there has been increasing interest in noncontact, noninvasive measurement techniques for estimating core body temperature in animals.
The use of infrared tympanic thermometers has been investigated.4,5 This method provides for relatively rapid acquisition of a temperature measurement from a relatively easily accessible anatomic site.2,6,9 Infrared thermometers measure the amount of radiation emitted from the tympanic membrane via a sensor probe.13 The probe detects the thermal source, and the infrared radiation is converted to an electric signal and calibrated to display a temperature reading.6,14 Because the tympanic membrane shares its blood supply with the hypothalamus via the carotid artery, core body temperature can be approximated from this measurement.2,9,15 However, because tympanic membrane temperature is variably cooler than core body (hypothalamic) temperature, tympanic thermometers have a built-in offset that converts the measured temperature to core body or rectal temperature to compensate for this difference.15,16
Tympanic thermometry is currently widely used in human patients because of the ease and rapidity of use.13,14,16,17 Tympanic thermometry in veterinary medicine has been evaluated in several species, including cats,5,8 dogs,2–4,12,18 rabbits,6 guinea pigs,7 monkeys,9 goats,19 sheep,19 cows,20 and horses.19 However, results have varied greatly between species and between studies, with some studies2,5,9,18,19 finding close agreement between tympanic and rectal temperature measurements, whereas other studies3,4,6,7,19 report a lack of agreement. Aside from species differences, various studies have also compared tympanic thermometer measurements with various gold standards. Although some investigators have used invasive methods as the gold standard,2,3,8 others have used commercial rectal thermometers with various rectal insertion depths.4–7,9,18 Therefore, differences in the procedures and methods of comparison may also have affected the conclusions of previous studies.
Tympanic thermometers designed for human use have been studied and used in veterinary medicine.4–6,9 However, because of the differences in the anatomy of the ear canal between veterinary species, tympanic thermometers specifically designed for companion animals have recently been developed.3,6,9,18 The latter devices have a smaller probe, allowing for more precise placement into the ear canal.9,18 The ear canal in dogs and cats consists of horizontal and vertical canals that need to be traversed to reach the tympanic membrane.9 This differs from the relatively straight ear canal in human patients, which generally allows for easier positioning of the tympanic thermometer probe when recording tympanic temperature.21 The ear canal in chinchillas lies in a dorsal to ventral direction, parallel to the tympanic membrane.22,23
We are not aware of prior studies evaluating the use of tympanic thermometers in chinchillas. In addition to being pets, chinchillas are used extensively in experimental studies of otitis media and hearing loss and as an experimental model of ototoxicosis.23–29 Because measurement of rectal temperature can be time consuming and stressful, tympanic thermometry may offer a suitable alternative for measurement of body temperature in chinchillas. Therefore, the objectives of the study reported here were to assess the clinical practicality and reliability of tympanic thermometry in chinchillas, evaluate the effects of restraint time and thermometer insertion depth on rectal temperature measurements, and determine the extent of agreement between temperature measured with 2 tympanic and a rectal thermometer. It was our hypothesis that there would be good agreement between the results of tympanic and rectal thermometry in chinchillas.
Materials and Methods
Animals
Forty-seven chinchillas (Chinchilla lanigera; 17 males and 30 females) ranging between 4 months and 8 years of age and weighing between 360 and 1,240 g (0.8 to 1.7 lb; mean ± SD, 0.68 ± 0.16 kg [0.31 ± 0.07 lb]) were evaluated in 3 separate experiments. One group (n = 17; 8 males and 9 females) was obtained from a commercial breedera and housed at the University of Wisconsin-Madison for several studies. The other group (n = 30; 9 males and 21 females) was housed at a local breeding facility. The chinchillas in both groups were maintained in individual cages in climate-controlled rooms with a light cycle of 12 hours. Rooms were maintained at a temperature of 21.1° to 23.3°C (70° to 74°F) and 35% to 60% relative humidity. The chinchillas were fed a commercial pelleted diet. All animals enrolled in the study were determined to be initially healthy on the basis of results of a physical examination performed by a veterinarian, and had no abnormalities noted on otoscopic examination, including examination of the tympanic membranes. Animals with auricular abnormalities were excluded from the study. The study protocol was approved by the Institutional Animal Care and Use Committee of the School of Veterinary Medicine, University of Wisconsin-Madison.
Thermometers
Rectal temperature measurements were obtained with a predictive digital thermometer.b The rectal thermometer had a temperature range of 32.2° to 43.2°C (90° to 108°F) and an accuracy of ± 0.1°C (± 0.2°F) and displayed temperature values within 10 to 20 seconds. The rectal thermometer was validated against a reference digital thermometer traceable to the National Institute of Standards and Technologyc in a water bath over a temperature range of 32° to 41.3°C (89.6° to 106.3°F) 3 times throughout the duration of the study. The rectal thermometer was found to measure a mean of 0.09°C (0.16°F) lower than the reference thermometer (−0.09°C [−0.16°F]; 95% limits of agreement, −0.34° to 0.12°C [–0.61° to 0.22°F]). In this study we used the rectal thermometer as our gold standard because of the small difference between temperatures measured with the rectal and reference thermometers.
Tympanic temperature measurements were obtained with both a humand and a veterinarye infrared thermometer. The human thermometer displayed temperatures ranging from 34° to 42.2°C (93.2° to 108°F), with a manufacturer-reported accuracy of ± 0.2°C (0.4°F) for 36° to 39°C (96.8° to 102.2°F) and an accuracy of ± 0.3°C (0.5°F) outside this range. Measurement time was < 1 second. The veterinary tympanic thermometer had the same manufacturer-reported values for temperature range and accuracy and a measurement time of < 1 second.
Effect of thermometer insertion depth on rectal temperature
To evaluate the effect of rectal insertion depth on temperature measurements obtained with the rectal thermometer, single rectal temperature measurements were obtained at a rectal insertion depth of 1 or 2 cm in 13 chinchillas. Each chinchilla was positioned in ventral recumbency with all 4 feet resting on the handler's arm and its head pointed toward the handler. A single observer was responsible for acquiring all rectal temperature measurements. The rectal thermometer was lubricated with sterile lubricant, and duplicate rectal temperature measurements were obtained for each chinchilla at 1- and 2-cm insertion depths in a randomized fashion. Randomization was performed with a computer program.f Both measurements were completed in < 1 minute in each animal during a single restraint period.
Effect of manual restraint on rectal temperature
To evaluate the effect of short-term manual restraint on rectal temperature measurements, 17 chinchillas were manually restrained for a single 5-minute period between the hours of 10:00 am and 12:30 pm. Each chinchilla was positioned in ventral recumbency with all 4 feet resting on the handler's arm and its head pointed toward the handler. Between temperature readings, the animal was held close to the handler's chest in a more secure manner. Rectal temperature was measured at an insertion depth of 2 cm. Following the initial temperature measurement, rectal temperature was measured in an identical manner at 1-minute intervals for the entire 5-minute restraint period.
Tympanic versus rectal thermometry
Temperature measurements obtained with the 2 tympanic thermometersd,e were compared with data obtained with the rectal thermometer in a total of 47 chinchillas. All measurements were collected between the hours of 9:30 am and 12:30 pm. Temperature data acquired with all 3 methods were collected within 88 to 200 seconds (mean ± SD, 127 ± 25 seconds) after the beginning of manual restraint. Temperature measurements were obtained in duplicate for each method, and the sequence of measurements was randomizedf for each animal. Two observers (1 left handed and 1 right handed) were responsible for all measurements, and the animals were randomlyf assigned to each observer, with 1 observer assessing 24 animals and the other assessing 23.
Rectal temperatures were assessed as described at an insertion depth of 2 cm. Tympanic temperatures were measured in the left ear to avoid potential confounding between ears within an animal. Disposable probe covers were applied to each thermometer prior to use. The pinna was gently lifted to aid in visualization of the ear canal. The probe was then placed into the ear canal and positioned toward the rostral aspect of the base of the opposite ear. This led to the most consistent positioning of the probe in the ear canal and near the tympanic membrane. The thermometer was removed completely from the ear to record the temperature reading before the duplicate measurement was obtained.
Statistical analysis
Bias (rectal vs tympanic thermometer) was modeled with a linear mixed-model procedure, with animal (chinchilla) as the random effect and method (type of thermometer) and order as fixed effects. The mean systematic bias was equivalent to the intercept of the model. Temperatures measured with the rectal thermometer (ie, the gold standard) were included as a fixed covariable to assess for the presence of proportional bias. Residuals were tested for normality and homoscedasticity on the basis of quantile and residual plots. To assess method variability, a linear mixed-model procedure was also implemented with tympanic thermometer types, replicates, and chinchillas as random variables. For this latter model, a heterogeneous variance model was also implemented to assess the difference in variance between the 2 thermometers and was compared with the homogeneous variance model by means of a likelihood ratio test. The coefficient of reliability was calculated for each method as SDchinchilla/SDTotal as a measure of consistency of measurement.30 The limits of agreement were calculated on the basis of the variance obtained from the mixed model as ± 1.96 • SDTotal.
The effect of restraint duration on rectal temperature was evaluated with a linear mixed-model procedure with time as a fixed effect and animal (chinchilla) as a random effect. Assumptions were checked as described. First-order autocorrelation over time was also checked with assessment of the autocorrelation function. Post-hoc comparisons of the various time points were made with Tukey adjustments.
Rectal temperatures obtained at a 1- versus 2-cm depth of insertion were compared with 2-tailed paired Student t tests, checking for normality and homoscedasticity of the data. For all analyses, values of P < 0.05 were considered significant. All analyses were performed with statistical software.g,h
Results
Effect of rectal insertion depth on rectal temperature
Inserting the rectal thermometer at a 1-cm insertion depth resulted in a mean ± SD rectal temperature of 35.3 ± 0.94°C (95.5° ± 1.69°F), whereas at a 2-cm insertion depth, the mean ± SD rectal temperature was 36.4 ± 0.77°C (97.5° ± 1.39°F). The mean difference between the 2 readings was 1.14 ± 0.77°C (2.05° ± 1.39°F), with insertion of the thermometer to a depth of 2 cm resulting in significantly (P < 0.001) higher temperatures than insertion to a depth of 1 cm. The 95% reference interval (mean ± 2SD, Gaussian distribution) for rectal measurements in chinchillas obtained at a 2-cm insertion depth was calculated as 34.9° to 37.9°C (94.8° to 100.2°F).
Effect of manual restraint on rectal temperature
Manual restraint of chinchillas had a significant (P < 0.001) effect on rectal temperature over time. Rectal temperature increased significantly (P = 0.029) beginning at 3 minutes of restraint by a mean ± SEM of 0.22 ± 0.07°C (0.40° ± 0.13°F). At 5 minutes of restraint, the mean ± SEM temperature increase, compared with the baseline temperature, was 0.35 ± 0.07°C (0.63° ± 0.13°F; P < 0.001).
Tympanic versus rectal thermometry
Temperatures acquired with both the humand and veterinarye tympanic infrared thermometers had significant systematic bias (0.42° ± 0.12°C [0.76° ± 0.22°F]; P < 0.001). The veterinary tympanic thermometer systematic bias was higher than that for the human tympanic thermometer by a mean ± SEM of 0.17° ± 0.08°C (0.31° ± 0.14°F; P = 0.038). The margin of error around the bias was 1.73°C (3.11°F; 95% limits of agreement = bias ± margin of error; Figure 1). There was also significant proportional bias (0.88° ± 0.14°C [1.58° ± 0.25°F]; P < 0.001), such that for each 1°C (1.8°F) increment of body temperature, the bias increased by 0.88°C. The magnitude of proportional bias was similar between thermometers (ie, the thermometer × temperature interaction effect was not significant). There was no significant difference in the variances for the 2 tympanic thermometers (P = 0.3). The coefficients of reliability for the rectal thermometer, the human tympanic thermometer, and the veterinary tympanic thermometer were 0.86, 0.85, and 0.69, respectively.
Differential plot illustrating the extent of bias between temperature measured with rectal thermometry versus 2 tympanic thermometers in 47 chinchillas. Plots were constructed with the bias as the y-axis and the rectal temperature (ie, reference standard) as the x-axis. LOA = Limits of agreement.
Citation: Journal of the American Veterinary Medical Association 251, 5; 10.2460/javma.251.5.552
Differential plot illustrating the extent of bias between temperature measured with rectal thermometry versus 2 tympanic thermometers in 47 chinchillas. Plots were constructed with the bias as the y-axis and the rectal temperature (ie, reference standard) as the x-axis. LOA = Limits of agreement.
Citation: Journal of the American Veterinary Medical Association 251, 5; 10.2460/javma.251.5.552
Differential plot illustrating the extent of bias between temperature measured with rectal thermometry versus 2 tympanic thermometers in 47 chinchillas. Plots were constructed with the bias as the y-axis and the rectal temperature (ie, reference standard) as the x-axis. LOA = Limits of agreement.
Citation: Journal of the American Veterinary Medical Association 251, 5; 10.2460/javma.251.5.552
Discussion
In the present study, we documented a significant and clinically important difference in temperature measurements when inserting a rectal thermometer at 2 different depths in chinchillas. By increasing the thermometer insertion depth from 1 to 2 cm, the rectal thermometer obtained a significantly higher reading. Other studies20,31 have also reported that rectal thermometer insertion depth affects measurements.20,31 Previous studies3–9 in various species comparing tympanic thermometers with rectal thermometers have used various depths ranging from 1 to 3 cm when obtaining rectal temperature. However, some authors18 did not report the rectal thermometer insertion depth.
Manual restraint of chinchillas resulted in a significant increase in rectal temperature within the first 3 minutes of restraint. Whereas the increase in rectal temperature may or may not be clinically relevant, prolonged handling and restraint should be avoided if rectal temperature is to be recorded. Furthermore, we suggest that the increase in rectal temperature might affect the accuracy of comparisons between devices when the time taken to collect measurements nears the 3- to 5-minute mark. It has been reported10,11,32 previously that acute stress secondary to manual restraint leads to an increase in body temperature in many species. A study32 in silver foxes indicated that stress-induced hyperthermia was evident within 5 minutes after capture and that temperature continued to increase during a 1-hour period of restraint. As such, it is advisable that temperature be measured relatively early during a physical examination, before the animal is restrained for a longer period, to acquire a temperature measurement that is most reflective of the animal's health status.33 Chinchillas are particularly sensitive to vigorous manual restraint and often struggle more with increasing pressure application. Stress can be minimized by providing adequate support for the animal without increasing restraint and by keeping restraint times minimal.33
The effect of manual restraint on rectal temperature highlights the importance of efficient data collection when comparing thermometry devices. If data collection is prolonged, false assumptions may be made about the relative accuracy and reliability of devices, especially if the order of temperature measurements is not randomized. Previous studies often did not highlight the importance of restraint time and whether an increase in temperature occurred with restraint. One study6 in rabbits noted that the temperature measurements did not increase with restraint and that the duration of temperature measurements ranged from 5.5 to 9.5 minutes. Previous studies evaluating tympanic thermometers in other species also varied greatly in the data collection duration as well as whether data collection methods were randomized. In the present study, when comparing tympanic and rectal thermometry, we attempted to minimize the effect of stress-induced hyperthermia on our results by limiting restraint times to < 200 seconds.
In the present study, tympanic temperature measurements acquired with both human and veterinary tympanic thermometers were not in agreement with results of rectal thermometry in chinchillas. However, rectal thermometry has not been validated in chinchillas by comparing it with results of core body temperature measurement. Rectal thermometry is currently the clinically accepted standard method for measurement of body temperature in chinchillas; therefore, it was used in this study as the gold standard. For devices to be used interchangeably, the new device must have an acceptable level of accuracy and analytic agreement with the preexisting method. Whereas a noninvasive method of temperature measurement in this species would be desirable to decrease stress in both clinical and research settings, the overall difference in temperature data for tympanic thermometry versus rectal thermometry was too large, precluding clinical use. We documented significant systematic bias as well as proportional bias, with the veterinary tympanic thermometer having higher bias than the human device. The margin of error was relatively wide (1.7°C [3.1°F]), indicating that tympanic thermometers may under- or overestimate rectal temperatures by up to 1.7°C in some animals. In addition, there was a tendency for larger clinical discrepancies at both ends of the temperature ranges investigated.
In the present study, the coefficient of reliability was also lower for the veterinary tympanic thermometer (0.69) than for the human tympanic (0.85) and rectal thermometers (0.86). This suggested that repeated measurements obtained with the veterinary tympanic thermometer may not be consistent. As such, we cannot recommend veterinary tympanic thermometry for monitoring body temperature in chinchillas, whereas the reliability of the human tympanic thermometer was comparable to that of the rectal thermometer.
The positive bias noted in the present study indicated that both tympanic thermometers tended to record temperatures that were lower than values obtained with rectal thermometry. Prior studies have reported similar results. In anesthetized cats and monkeys, temperatures obtained with tympanic thermometry were lower than hypothalamic temperatures, but correlated well.15 A study6 in rabbits also concluded that tympanic thermometry recorded lower temperatures than rectal thermometry. The lower tympanic temperature may be attributed to the relative proximity of the probe to the environment, compared with other methods, and the lack of insulating tissues surrounding the ear canal. Positioning and anatomic differences of the chinchilla ear canal may also contribute to the lower temperature readings with tympanic thermometers.
Differences in the anatomy of the ear canal as well as positioning of the probe may also have contributed to the overall lack of agreement between thermometry methods in chinchillas in the present study. A study9 in squirrel monkeys found good agreement between human tympanic thermometers and rectal thermometers. This may have been because the straight ear canal of a squirrel monkey more closely resembles the ear canal of a human infant.9 However, a study in rabbits6 found a lack of agreement between temperature data acquired with human, veterinary, and rectal thermometers; this may have been because of the presence of a blind diverticulum cranial to the ear canal as well as the long vertical portion of the canal in rabbits, which differs from the anatomy in humans as well as other species.6 A study7 in guinea pigs also found poor agreement when comparing measurements obtained with a veterinary tympanic thermometer versus with a rectal thermometer. As such, we would emphasize that it cannot be assumed that veterinary or human tympanic thermometers are appropriate for use in all species.
Although rectal temperatures recorded at a depth of 2 cm were used as the reference (gold) standard in the present study, it is important to note there is a lack of substantial data regarding normal body temperatures in chinchillas. Most resources list ranges of temperatures but do not disclose the depth of thermometer insertion used to validate these parameters. Reference ranges for body temperature reported in the literature include 36.1° to 37.8°C (97° to 100°F),34 35.5° to 37.2°C (96° to 99°F),33 and 37° to 38°C (98.6° to 100.4°F).35 The reference interval established on the basis of our data at an insertion depth of 2 cm was 34.9° to 37.9°C, which was similar to the previously reported reference intervals for chinchillas. However, it should be noted that, in 2 studies,33,34 the reported reference range indicated a temperature of > 36°C as the lower limit, whereas the reference range calculated on the basis of our measurements had a lower limit of 34.9°C.
All animals enrolled in the present study were considered healthy and euthermic. Therefore, the results of the present study should be interpreted with caution because the performance of the evaluated thermometers may differ in chinchillas with abnormal body temperatures. Further studies investigating and validating the use of rectal and tympanic thermometry in chinchillas in both healthy and disease states are indicated.
Footnotes
R & R Chinchilla Inc, Jenera, Ohio.
Vet-Temp Rapid Digital Thermometer DT-10, Advanced Monitors Corp, San Diego, Calif.
Traceable Digital Thermometer 15-077-8, Fisher Scientific, Pittsburgh, Pa.
Thermoscan IRT 4520, Braun, Southborough, Mass.
Vet-Temp VT-150, Advanced Monitors Corp, San Diego, Calif.
Research Randomizer, version 4.0, Geoffrey C. Urbaniak and Scott Plous, Middletown, Conn. Available at: www.randomizer.org. Accessed Nov 5, 2015.
R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. Available at: www.r-project.org. Accessed Nov 5, 2015.
nlme: Linear and Nonlinear Mixed Effects Models, R package, version 3.1-103, José Pinheiro, Douglas Bates, Saikat DebRoy, Deepayan Sarkar, and the R core team, Vienna, Austria. Available at: cran.r-project.org/web/packages/nlme/index.html. Accessed Nov 5, 2015.
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