Introduction
Assessment of body temperature is a fundamental component of the physical examination in veterinary patients, and the information obtained often guides clinical decisions. Invasive contact devices, such as esophageal and pulmonary thermistors, are the gold standard for assessing core body temperature, but these techniques can be used only on anesthetized animals.1–3 Instead, rectal thermometer (RT) is used to assess body temperature in conscious animals, and there is good agreement between rectal and core body temperature in dogs.2,3 Similar studies are yet to be performed in cats. However, the technique of using contact thermometers against the rectal mucosa can be difficult to perform, as it is particularly stressful for fractious animals as well as a potential source of cross-contamination if appropriate hygienic measures are not taken.4,5 There is also the possibility of further rectal injury and discomfort in patients with preexisting anorectal and pelvic disease.2,3 Moreover, despite its relatively good agreement with core body temperature, the accuracy and repeatability of RT can be negatively impacted by the depth of the probe, presence of feces, air, and local blood flow.3,4 As a result, several veterinary studies2–13 have reported alternative, often less-invasive techniques to measure body temperature. For example, axillary and auricular temperature measurements have been compared, the latter mostly by use of pyroelectric sensors to measure infrared radiation emanating from the tympanic membrane, with conflicting results.4–6,8–11 However, the consensus is that tympanic membrane and axillary temperatures should not be used interchangeably with rectal temperature in dogs and cats.
Noncontact infrared thermometers (NCITs) use pyroelectric sensors to measure infrared radiation emanating from the skin or forehead supplied by the temporal artery. They have gained popularity in human medicine in 2020 largely as a result of the SARS-COV2 pandemic14,15; this is a rapid, cheap, noninvasive method not requiring contact, sterilization, or disposal and therefore has been widely used to screen for febrile individuals in various settings (eg, international travel).16 However, data on their use in the clinical human medical setting are mixed.17 A systematic review on the use of NCIT for fever screening at airports reported sensitivities for detecting fever ranging from 4% to 89%, with specificities ranging from 75% to 99%.18 As such, the authors highlighted the poor scientific evidence available for utilization of this technique. Conflicting results persist in the clinical setting of pediatric medicine with studies on children reporting sensitivity ranges of 83% to 99%.16,19,20
Veterinary use of noncontact infrared technology at locations other than the tympanic membrane are limited, with most studies21–25 having been performed in monkeys, guinea pigs, and horses, all with poor results. Two previous studies26,27 have been performed in dogs and cats. The first study used NCIT applied to the cornea in dogs and compared it with RT, and the second study compared NCIT readings from the pinna, gingiva, and perineum with the RT in a population of cats. Neither study assessed the effect of variables such skin color or disease states (eg, hypovolemia) on measurements, and both demonstrated poor agreement between NCIT measurements and RT.
The aim of this study was to compare the agreement of standard RT measurements and the temperature measured with an NCIT in a population of privately owned dogs and cats. For this study, we hypothesized that there would be good agreement and correlation between body temperature measurements taken with the NCIT and RT.
Materials and Methods
Study population and ethics
This was a prospective multicenter study of privately owned dogs and cats referred to the internal medicine and intensive care services of Ospedale Veterinario San Francesco (Milan, Italy), Clinica Veterinaria Gran Sasso (Milan, Italy), and the University of Liverpool Small Animal Teaching Hospital (Liverpool, UK) for any medical condition during a 6-month period from July 2020 to December 2020. The University of Liverpool Committee on Research Ethics granted ethical approval prior to the study at each center. Prior to enrollment, owners were informed of the research protocol and provided informed written consent. Animals were recruited at each center whenever the investigators (1 from each center) and staff were available to perform the measurements required. Animals were included only once; animals with an illness or injury that could be exacerbated or could influence the NCIT or RT measurements were excluded. Examples included animals with conditions affecting their peripheral perfusion (hypovolemic shock, sepsis, and anaphylaxis), ear disease including diffuse dermatologic conditions affecting the pinna, and rectal, pelvic, and perineal diseases. Animals with a demeanor that prevented acquisition of any of the temperature readings were also excluded.
Data recording
Ambient room temperature, age, breed, sex, neuter status, weight, skin color, and coat color were all recorded, as was the presence of icterus, reason for presentation, and diagnosis if known. For the purposes of analysis, animals were classified as normothermic if their body temperature was within reference interval (38 to 39.2 °C), hyperthermic if body temperature was > 39.2 °C, and hypothermic if body temperature was < 38 °C
Measurement of body temperature
All body temperature measurements were taken by staff, students or clinicians involved in the care of the individual animal; body temperature measurements were first taken by use of an NCIT to minimize stress to the animal, with measurements taken with a rectal thermometer immediately afterwards. The thermometer used was a single cutaneous NCIT (PC868 Infrared Thermometer; Shenzhen Pacom Medical Instruments Co Ltd), and triplicate measurements were taken in immediate succession at a distance of 3 to 5 cm from the hairless skin of the medial aspect of the pinna. The rectal thermometer used to obtain RT was a standard digital thermometer (PIC Solution) and was placed in a single-use, disposable probe cover (Supvox; Shenzhenshi Yunasheng Technology Co Ltd) and lubricated (Luan gel 1%; Molteni Farmaceutici) before inserting 2 cm into the rectum, ensuring that it was positioned in contact with the rectal mucosa until the final reading was displayed. The ambient room temperature was recorded at the time that the measurements were taken. All thermometers were precalibrated by the manufacturers.
Statistical analysis
To evaluate differences in body temperature readings between NCIT and RT, the rectal noncontact infrared thermometer gradient (RNITG) was calculated for each animal by subtracting the mean NCIT measurements of 3 readings from the RT measurement, ranking the values in ascending order and obtaining the median value. Based on previous veterinary studies comparing methods of temperature measurement,6,9,11 a difference in temperature > 0.5 °C was considered to be clinically important. To assess repeatability of measurements, the coefficient of variation of the triplicate NCIT readings was calculated for each animal and the mean of the population calculated. Statistical analysis was then performed using statistical software packages (JMP version 14.2.0; SAS Institute Inc; Prism for Mac version 8.10; Graph Pad Software Inc). Deming regression and Kendall rank correlation coefficient were used to compare associations between RT and NCIT measurements, while Bland-Altman analysis and Cohen kappa coefficients were used to further assess the agreement between RT and NCIT measurements. Categorical data are reported as numbers or proportions with percentages in brackets, while continuous data are reported as mean ± SD or median (range), as indicated. The level of statistical significance was set at P < 0.05 for 2-sided analyses.
Results
Dogs
One hundred sixty-eight dogs were recruited, 86 (51%) of which were male and 82 (49%) were female. Forty-one of 86 (48%) male and 72 of 82 (88%) female dogs, respectively were neutered. Median age was 8 years (range, 4 weeks to 17 years) and median weight was 12.9 kg (range, 0.4 to 60.0 kg). Fifty-one breeds were represented, the most common of which were mixed-breed dogs (n = 46) followed by Border Collie (9), Jack Russell Terrier (8), Labrador Retriever (7), and Cavalier King Charles Spaniel (6). A total of 504 NCIT measurements and 168 RT measurements were performed on these dogs, with the room temperature ranging from 22.1 to 24.1 °C.
Median (range) body temperature reflected by RT and NCIT measurements was 38.4 °C (33.4 to 40.3 °C) and 36.3°C (30.8 to 40.0 °C), respectively. In all, 18 of 168 dogs (11%) were hyperthermic by RT, compared with 5 of 168 (3%) by NCIT, while 35 of 168 (21%) dogs were hypothermic by RT, compared with 153 of 168 (91%) by NCIT. The mean coefficient of variation for the triplicate NCIT readings was 0.6 °C (0.0 to 4.6 °C). Deming regression analysis identified a weak positive association between body temperature measured with the NCIT and RT in dogs (P = 0.004; Figure 1) supported by Kendall tau = 0.154 (P = 0.004). Kappa analysis revealed only weak agreement between the 2 measurements (Kappa value, 0.05; P < 0.001). Bland-Altman analysis demonstrated a mean ± SD bias of –2.2 ± 1.51 °C (P < 0.001) and a tendency for the NCIT to underread body temperature, in comparison to the RT, with the degree of low measurements lessening as body temperature increased (Figure 2). Median RNITG was 2.1 °C (–1.1 to 7.3 °C). A positive RNITG (RT greater than NCIT) was present in 159 of 168 (94.6%) dogs. In 1 of 168 (< 1%) dogs, the RNITG was neutral. A negative RNITG (RT less than NCIT) was present in 8 of 168 (5.0%) dogs. Only 15 of 168 (8.9%) dogs had an RNITG ≤ 0.5 °C. Ambient room temperature, age, breed, sex, neuter status, weight, skin color and coat color, presence of icterus, reason for presentation, and diagnosis if known were initially evaluated to assess if these factors could influence the accuracy of NCIT measurements. However, due to the poor association and correlation of NCIT with RT, the influence of these factors was not evaluated because of doubts in the significance of any 1 result in the context of the poor reliability of the device.
Deming regression plot depicting the relationship between body temperature measured with a rectal thermometer (RT) and noncontact infrared thermometer (NCIT) in 168 dogs. The points represent results for individual dogs, while the dotted line represents the line from Deming regression.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Deming regression plot depicting the relationship between body temperature measured with a rectal thermometer (RT) and noncontact infrared thermometer (NCIT) in 168 dogs. The points represent results for individual dogs, while the dotted line represents the line from Deming regression.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Deming regression plot depicting the relationship between body temperature measured with a rectal thermometer (RT) and noncontact infrared thermometer (NCIT) in 168 dogs. The points represent results for individual dogs, while the dotted line represents the line from Deming regression.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Bland-Altman plot depicting agreement between body temperature measured with the RT and NCIT in 168 dogs. The y- and x-axes depict the difference between and the average of the RT and NCIT measurements, respectively. The points represent results for individual dogs, the solid line depicts the average bias, the dotted lines depict the 95% confidence limits to the agreement, and the dashed line represents the trendline from linear regression analysis.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Bland-Altman plot depicting agreement between body temperature measured with the RT and NCIT in 168 dogs. The y- and x-axes depict the difference between and the average of the RT and NCIT measurements, respectively. The points represent results for individual dogs, the solid line depicts the average bias, the dotted lines depict the 95% confidence limits to the agreement, and the dashed line represents the trendline from linear regression analysis.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Bland-Altman plot depicting agreement between body temperature measured with the RT and NCIT in 168 dogs. The y- and x-axes depict the difference between and the average of the RT and NCIT measurements, respectively. The points represent results for individual dogs, the solid line depicts the average bias, the dotted lines depict the 95% confidence limits to the agreement, and the dashed line represents the trendline from linear regression analysis.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Cats
Sixty-one cats were included in the study, of which 28 (46%) were neutered males, 16 (26%) were neutered females, 14 (23%) were sexually intact males, and 3 (5%) were sexually intact females. Median age was 6 years (range, 1 month to 18 years), and median weight was 4.4 kg (range, 1.3 to 9.0 kg). Thirteen different breeds were represented, the most common of which was the domestic shorthair (n = 37), followed by Maine Coon (4), Ragdoll (3), Siamese (3), and British Shorthair (3). A total of 183 NCIT measurements and 61 RT measurements were performed on these cats, with the room temperature ranging from 19.3 to 23.7 °C.
Median (range) body temperature reflected by RT and NCIT measurements was 38.3 °C (36.2 to 40.0 °C) and 35.7°C (31.8 to 38.0 °C), respectively. Of the 61 cats, 4 (7%) were hyperthermic on RT. No cat was hyperthermic on readings taken with the NCIT. Nineteen (31%) and 60 (98%) cats were hypothermic on the basis of RT and NCIT measurements, respectively. The mean coefficient of variation for the triplicate NCIT readings was 0.9 °C (0.0 to 5.8 °C). There was no correlation (Deming regression [P = 0.932]; Kendall tau = –0.01 [P = 0.91]) or agreement (Kappa value, –0.08 [P = 0.704]) between NCIT and RT measurements in cats (Figure 3). Similar to dogs, Bland-Altman analysis demonstrated a mean bias of –2.7 ± 1.44 °C (P < 0.001) and a tendency for the NCIT to underread body temperature (with the degree of low measurements lessening as body temperature increased; Figure 4). The median RNITG was 2.4 °C (0.0 to 7.0 °C). A positive RNITG (RT greater than NCIT) was present in 60 of 61 (98.3%) cats, while 1 cat had a neutral RNITG (1.6%) and none of the cats had a negative RNITG. The RNITG was ≤ 0.5 °C in 3 of 61 (5.0%) cats. Similar for dogs, the influence of external factors (ie, coat length and skin color) was not pursued because of the inherent poor reliability of both NCIT measurements taken within the same individual and when compared with RT.
Deming regression plot depicting the relationship between body temperature measured with the RT and NCIT in 61 cats. The points represent individual cats, while the dotted line represents the line from Deming regression.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Deming regression plot depicting the relationship between body temperature measured with the RT and NCIT in 61 cats. The points represent individual cats, while the dotted line represents the line from Deming regression.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Deming regression plot depicting the relationship between body temperature measured with the RT and NCIT in 61 cats. The points represent individual cats, while the dotted line represents the line from Deming regression.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Bland-Altman plot depicting agreement between body temperature measured with the RT and NCIT in 61 cats. The y- and x-axes depict the difference between and the average of the RT and NCIT measurements, respectively. The points represent results for individual cats, the solid line depicts the average bias, the dotted lines depict the 95% confidence limits to the agreement, and the dashed line represents the trendline from linear regression analysis.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Bland-Altman plot depicting agreement between body temperature measured with the RT and NCIT in 61 cats. The y- and x-axes depict the difference between and the average of the RT and NCIT measurements, respectively. The points represent results for individual cats, the solid line depicts the average bias, the dotted lines depict the 95% confidence limits to the agreement, and the dashed line represents the trendline from linear regression analysis.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Bland-Altman plot depicting agreement between body temperature measured with the RT and NCIT in 61 cats. The y- and x-axes depict the difference between and the average of the RT and NCIT measurements, respectively. The points represent results for individual cats, the solid line depicts the average bias, the dotted lines depict the 95% confidence limits to the agreement, and the dashed line represents the trendline from linear regression analysis.
Citation: Journal of the American Veterinary Medical Association 260, 7; 10.2460/javma.21.09.0403
Discussion
Measurement of body temperature is an important part of the clinical examination of veterinary patients. Accuracy is essential since findings will often determine the course of clinical decisions and diagnostic investigations. Body temperature in dogs and cats can be impacted by stress, with temperatures reaching as high as 39.7 °C in healthy individuals in the consulting room.28,29 While rectal temperature is considered to be the standard measurement to assess body temperature in conscious animals, it can be stressful to perform. Our study attempted to compare a correlation and agreement between RT and temperature taken from the medial aspect of the pinna using a noninvasive, NCIT.
Results of this study indicated a poor correlation in body temperature measured by NCIT and RT in both species, which is consistent with results from 2 previous studies26,27 that compared RT and NCIT measurements taken from 3 different anatomic sites in a population of cats and from the cornea in dogs, respectively. In our study, the median temperature difference in both species (dogs, 2.1 °C; cats, 2.4 °C) was outside the clinically acceptable range (≤ 0.5 °C), with only 8.9% of dogs and 4.9% of cats, respectively, having a median temperature difference (RNITG) ≤ 0.5 °C. Due to the poor correlation and agreement between RT and NCIT measurements, a correction factor could not be calculated for NCIT measurements which is therefore not considered a reliable surrogate for RT in dogs and cats.
In the present study, measurements obtained by NCIT underestimated body temperature, compared with RT, in both dogs and cats by a mean of 2.2 and 2.7 °C, respectively. This is not dissimilar to a study30 that compared RT and NCIT measurements in children. Interestingly, the degree of underestimation in both dogs and cats lessened as body temperature increased in the present study. These results are in contrast to a study30 of children in which infrared thermometry tended to overestimate hypothermia and underestimate hyperthermia.
In the early phase of pyrexia, pyrogens inhibit preoptic neurons that would normally facilitate heat loss and suppress heat production. This activates cold defenses, such as vasoconstriction and shivering, leading to discrepancies between core temperature and surface temperature. Once pyrogen concentrations decrease, the set point temperature returns toward normal, triggering active vasodilation and sweating, which increases heat loss from the skin surface.31 It is possible that some hyperthermic individuals in our study were in this latter vasodilatory phase, increasing peripheral surface temperatures in line with core temperature. Unfortunately, the duration of hyperthermia was not a recorded variable in this study and represents a possible limitation.
The reason for poor correlation of NCIT with RT is difficult to determine. A previous study27 on the use of NCIT in a shelter population of cats found that skin temperatures varied widely, even within the same individual over a short period of time. The poor correlation seen in the present study may therefore be related to possible natural variation in skin temperatures of dogs and cats. Indeed, the coefficient of variation of the triplicate NCIT readings from dogs and cats showed a mean variation of 0.6 and 0.9 °C, respectively. However, since NCIT readings were taken in immediate succession, it would seem more likely that this is the result of an inherently poor precision and repeatability in the measurements taken by the NCIT device.
Alternatively, an inherent underreading of superficial temperature with NCIT when compared with RT may explain the discrepancies between the 2 methods. Previous studies6,7,9 that compared temperature measurements obtained at peripheral sites with RT measurements have demonstrated they are often lower than RT. For example, a study32 of adults suggested the cutoff for fever when forehead temperature is taken with the NCIT should be 2 °C below that of other body temperature measurements due to underreading. Of note, this is not a dissimilar temperature to the underreading reported when using the NCIT in dogs in this study. Therefore, the authors attempted to ascertain whether a correction factor could be applied to the NCIT. Unfortunately, this was not achievable since the poor correlation and systemic bias identified by Bland-Altman plots indicate the limitations when using NCIT measurements are not simply due to underreading but also to unacceptable low levels of accuracy and precision. Finally, the fact that NCIT devices are designed for human use may mean that other factors not assessed in this study, such as potential differences in arterial blood flow, skin emissivity, and skin pigmentation, in dogs and cats, compared with factors in humans, may have played a greater role.
Limitations of this study include data collection, which was performed by multiple personnel including clinicians, nursing staff, and veterinary students. This may have increased variation in the data, although a standardized method of acquisition of temperatures was taught to all participants. It is also possible that relative user inexperience with the NCIT device may represent a disadvantage and source of bias. Regardless, the way the readings were obtained is consistent with a clinical practice setting.
The low prevalence of pyrexia in dogs (11%) and cats (7%) is an additional limitation of this study, particularly since the degree of underestimation of NCIT, compared with RT, lessened as body temperature increased. Further study is required to investigate whether there is a place for the noninvasive nature of NCIT to be used in the monitoring of pyrexia in dogs and cats.
Since all animals were conscious, invasive core temperature measurement by use of pulmonary artery thermistors was not used. It could be argued that a suitable gold standard with which to compare the test device was therefore not adopted. The limitations of using rectal temperature as a surrogate for core temperature are that it tends to lag behind changes in core temperature in both humans and dogs by up to 90 minutes.33,34 Its accuracy can also be affected by local blood flow or the presence of feces or air in the rectum.35,36 That being said, the use of RT is considered the reference standard for clinically assessing body temperature in conscious veterinary patients because of the overall good agreement with core temperature.2,3
Animals with underlying conditions that may have led to aberrant peripheral temperature measurements were excluded from the study. However, it is possible that alterations in peripheral perfusion not identified in this study could have affected peripheral measurements. Finally, it is possible that immeasurable selection bias against the test device was present, although we did not find any evidence in our analysis to suggest as much.
Results of this study show a clinically unacceptable difference between body temperature measurements made by NCIT and rectal thermometer. This, in accordance with a poor correlation and agreement between the 2 measurements, prevents the development of a standardized correction equation to improve the accuracy of NCIT measurement. Therefore, the use of NCIT in dogs and cats cannot be recommended at the current time.
Acknowledgments
No external funding was used in this study. The authors declare that there were no conflicts of interest.
Dr. German is an employee of the University of Liverpool, but his post is financially supported by Royal Canin. Dr. German has also received financial remuneration for providing educational material, speaking at conferences, and consultancy work from this company; all such remuneration has been for projects unrelated to the work reported in this manuscript.
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