1. Introduction
Temperature is one of the vital assessments used to objectively examine a veterinary patient, the results of which can have significant implications on the health status of that patient [
1,
2,
3]. Predictive rectal thermometry is the most common form of thermometry used in veterinary clinical practice despite 30 years of research on alternative modalities [
4,
5,
6]. Research on alternatives to rectal thermometry have primarily focused on corelating the temperature values of these alternative methods to either rectal temperatures or a core body temperature [
4,
5,
7,
8,
9].
Some of the discussed motivation to identify alternative modalities to rectal thermometry has been; the difficulty in obtaining rectal temperatures in uncooperative or fractious animals, the influence of feces or perianal disease processes (i.e. fistulas, tumors, etc.) falsifying results and the potential increase in the risk of nosocomial infections with shared instrument usage and handling [
4,
10,
11,
12]. Rectal thermometry may be more stressful than potential alternatives. Gomart and colleagues (2014) looked at heart rate and graded stress behaviors (vocalization, lip licking, shaking, panting and defensive behaviors) in 250 dogs following rectal, auricular and axillary temperature readings. They found that heart rate and stress behavior scores were both significantly increased following rectal thermometry compared with the other methods [
13]. In cats, it has been noted, that the stress of rectal temperature measurement alone may be enough to elevate rectal temperature [
3].
Stress in the clinical environment can negatively influence not only the current visit but subsequent visits [
14,
15]. Some inherent stress may be from interactions with practitioners in the clinical setting, this is often referred to as a “white-coat effect” and has been described in both dogs and cats [
1,
3,
16]. Another potential stressor in the clinical environment may be an appointment’s duration. In the human literature, one of the main factors adversely affecting patient satisfaction is time spent in a clinic [
17,
18]. In veterinary medicine it is widely regarded that minimizing the duration of a procedure helps to minimize stress [
19,
20]. When feasible the minimal duration of restrain that can be used for immobilization should be used [
14]. Despite the importance of minimizing appointment duration, handling and procedure time; an analysis on how the method of thermometry affects the duration of restrain and appointment time for dogs and cats has not been investigated.
Here we compare the time associated with approaching, restraining and recording the temperature of canine and feline patients with a digital predicative rectal thermometer and a digital axillary thermometer. The instrument duration was kept constant to focus on the temporal aspect of restraining with either method. Innovations and technology continue to advance the speed and quality of instrumentation. Rather than focusing on the type of thermometer our aim was to compare the temporal aspects of the procedure at each location.
We hypothesize that there would be an increased duration of restraint with rectal thermometry which would provide at least a partial explanation on the increased stress reported between that and axillary thermometry. This information will not only provide insight on an uncontrolled factor in thermometry research it will also provide information that can be used to minimize the duration of clinical visits overall.
2. Materials and Methods
Data was collected approximately weekly between November 2021 and May 2022 at a small animal hospital. Canine and feline pet owners with appointments for routine veterinary wellness care were approached and provided with information about the study. Confirmation of each animal’s wellness status and written owner consent to participate in the study was provided. Participation required acclimation to the clinic environment (22.14 ° ± 0.56 ° C) for 15 minutes before initiating the study. Owners could elect to withdraw their pet at any point. Three canines and one feline were withdrawn prior to completing the full study at their owner’s request, this data was omitted. Participating pets (n = 186) included 114 canines and 72 felines.
Animal demographic information is included in
Table 1. Canine participants included 45 spayed females and 69 males, 12 of which were intact. All canine participants were at least 1 year of age, the average age was 6.01 years ± 3.87 years old (range 1.2 – 13.18 years). Canine breeds included twenty-five different pure and mixed breeds that varied from Chihuahua to Saint Bernard. Retriever and retriever crosses were the largest breed group represented (33/114). Average canine weight was 22.57 kg ± 13.90 kg (range 3.58 - 54.88 kg). Animal body condition was scored on a 9-point scale. The average canine body condition score (BCS) was 6.02 ± 0.94 (range 4-8). Feline participant average age was 5.91 y ± 4.49 (range 1.01 - 15.69y). Forty-nine out of 72 cats were classified as a domestic short-haired breed, 10 as domestic long-haired, 6 as domestic medium-haired, 5 as Siamese and 2 as a Scottish Fold breed. Feline weight was 4.70 ± 1.25kg (range 2.81 – 7.71 kg); BCS 5.83 ± 1.15 (range 4-8). Animal body confirmation/chest size was classified as either small (< 10kg), barrel chested or keel chested. Animal coat type was also classified as either smooth, short, medium, or long haired for both canines and felines.
Using a crossover design both rectal and axillary thermometry was performed successively on each pet. Each animal was randomly assigned to receive rectal or axillary thermometry first. Rectal thermometry was performed using a commercial digital thermometer (Vicks V912US; Proctor and Gamble, Cincinnati Ohio), Axillary Thermometry was performed using a veterinary digital axillary thermometer (Mella Pro; Mella Pet Care, Chicago Illinois). Pets were brought into a 1400 ft examination room (22.14 ° ± 0.56 ° C) individually by their owner, who remained in the room throughout the study. See
Figure 1 for a schematic of the study design area. Canines remained on a lead on the floor and felines were removed from carriers and lightly restrained on an examination table. The same veterinarian and licensed technician performed all the animal handling and thermometry. A third investigator remained near the door to monitor and record timing. Markers on the floor indicated the veterinarian and technician’s starting location. The veterinarian would verbally signal timing should commence, and both the technician and veterinarian would approach the pet. The technician would restrain the animal in whatever fashion seemed most appropriate given the animal’s size and demeanor and the veterinarian would perform the thermometry (rectal or axillary). As soon at the thermometer was positioned the veterinarian would signal verbally to the timer, and the timing would stop. This was recorded as a Pre-temperature time (Pre-TempT).
After the thermometry was completed, the veterinarian would provide another verbal cue indicating they were done. Recording would commence again, the thermometer was removed from its position, the technician would return handling of the pet to the owner and the veterinarian would travel to the digital record system and enter the temperature into the record. Once the record was entered, they would again verbally signal that recording should stop. This was recorded as a Post-temperature time (Post-TempT). The measurement time for each device varied, for that reason the measurement time was not recorded. For analysis purposes a standard 6 seconds was used as the recording time and was added to the Pre-Temp and Post-Temp times to determine a presumptive total time (TTime). Once time values were recorded all parties returned to their starting location and the process was immediately repeated. Pets who initially were randomly selected to receive rectal thermometry, received axillary thermometry for the second round and vice versa.
Statistical analysis was performed as an aggregate for all pet participants and for canines and felines separately using a statistical software package (SigmaStat, San Jose, CA). Normal distribution was confirmed using a Shapiro-Wilk normality test. Paired two-tailed t-tests were used to compare times (Pre-TempT, Post-TempT and TTime) between rectal and axillary trials. Two-way repeated-measure analysis of variance (ANOVA) was performed where one variable remained the trial type (rectal or axillary) and the other tested the significance of trial order, breed type, BCS, sex, body confirmation and hair type on each time value (Pre-TempT, Post-TempT and TTime). Significance level was set at P values < 0.05. In the event of significance, a Bonferroni post-hoc multiple comparison test evaluated all pairwise interactions. All data reported are mean values ± standard deviation.
3. Results
Results for canine and felines combined are indicted in
Figure 2 and are separated by species in
Figure 3. For all pets the Pre-TempT was shorter with the axillary trial (17.67 sec ± 2.34 sec) than the rectal trial (20.15 sec ± 2.38 sec; P < 0.001). For canines the axillary Pre-TempT was 17.51 sec ± 2.19 sec and the rectal Pre-TempT was 19.43 ± 2.45 sec and for felines the axillary Pre-TempT was 17.92 sec ± 2.57 sec and the rectal Pre-TempT was 21.29 ± 1.69 sec (P < 0.001 for both). For all pets the Post-TempT was not significantly different between the axillary and rectal trails (12.45 sec ± 2.37 sec and 12.06 sec ± 3.20 sec respectively; P = 0.103) For canines the Post-TempT for the axillary trial was 12.31 sec ± 2.46 sec and Post-TempT for the rectal trial was 12.27 sec ± 3.31 sec (P = 0.887). For felines only the Post-TempT for the axillary trial was significantly longer at 12.67 sec ± 2.22 sec than the rectal Post-TempT (11.74 sec ± 3.08 sec; P = 0.004). With a standardized measurement duration of 6 sec, the TTime for all pets was shorter with the axillary trial (36.12 sec ± 3.24 sec) than the rectal trial (38.22 sec ± 3.46 sec; P < 0.001). For canines the TTime for the axillary trials (35.82 sec ± 3.13 sec) was shorter than the rectal trial (37.70 sec ± 3.61 sec; P < 0.001). Similarly, for felines the TTime was 36.59 sec ± 3.39 sec for the axillary trials and significantly longer at 39.03 sec ± 3.08 sec for the rectal trials (P < 0.001).
The order with which the trials took place did not significantly impact Pre-TempT, Post-TempT or TTime for canines, felines or all pets collectively (P > 0.05 for all). Canine participants were on the floor and felines on examination tables, making direct comparison difficult. Rectal Pre-TempT was shorter in canines than felines (P < 0.001), consequently the rectal TTime was also significantly shorter (P = 0.011). No other difference in timing was significantly different between canines and felines (P > 0.05 for rectal Post-TempT and all axillary times). Across all participants and within canine and felines individually animal reproductive status (sex and intact vs spayed) did not significantly affect Pre-TempT, Post-TempT or TTime. Body condition score (BCS; 5.95 ± 1) did not differ significantly between canine (BCS 5.83 ± 1.15; range 4-8) and feline (BCS 6.02 ± 0.94; range 4-8) participants nor did it significantly impact Pre-TempT, Post-TempT or TTime for canines, felines of all pets collectively (P > 0.05 for all).
Canine breed variation and small sample size of certain breeds made direct comparisons between breeds difficult. Body confirmation/ chest classification as either small (< 10kg), barrel chested or keel chested did not significantly impact Pre-TempT, Post-TempT or TTime within or between rectal and axillary trials nor did the designation of canine coat type as either smooth, short, medium, or long haired (P > 0.05 for all). Similar results were determined for feline participants with a few exceptions. Using post-hoc Bonferonni comparisons based on breed. All feline breed types demonstrated significant reductions in axillary Pre-TempT and TTime except the two felines designated as Scottish Fold breed (P = 0.51 and 0.76 for axillary vs rectal Pre-TempT and TTime respectively). Within the feline rectal trials the TTime of domestic-long hair breeds (41.91 sec ± 0.93 sec) was significantly longer than domestic-short hair breeds (38.11 sec ± 1.91 sec; P = 0.019). No other difference was noted between breeds within or between the rectal and axillary trails. All feline participants were under 10 kg, and consequentially classified as small confirmation/chest size. Despite variation in breed designation, no difference was identified in or between felines with coats classified as either smooth, short, medium, or long haired (P > 0.05 for all).
4. Discussion
The total time (TTime) associated with axillary thermometry was shorter than that for rectal thermometry in both canine and feline participants. This is because in both species groups the time leading up to the temperature measurement (Pre-TempT) was significantly shorter in the axillary temperature trials than the rectal temperature trials. For canine participants the duration after the temperature was taken, until it was recorded (Post-TempT) did not differ between axillary and rectal trials. In felines the Post-TempT was actually shorter in the rectal trials, but not enough to compensate for the significant reduction in axillary Pre-TempT.
A number of factors could influence Pre-TempT. Pre-TempT was prior to thermometry when the pet was approached and restrained for either thermometry method. In this study, effort was made to control for the space and distance traveled within species. Each clinic would likely have different results based on size and arrangement of that facility. The personnel performing the measurements also remained constant. Presumably in the average clinical environment, there would be some consistency in personnel and clinical spacing. Pet handling and restraint varied inherently based on, breed, size, and animal demeanor. The crossover design was meant to minimize the effect of individual variation to the extent possible. The experimental design was meant to provide insight on how duration of handling for axillary thermometry differed from that of rectal thermometry. It Is interesting that regardless of species, body confirmation, sex, coat type and BCS the axillary Pre-TempT was significantly shorter than rectal Pre-TempT. Presumably this is due to shorter restraint and handling time with axillary thermometry. Pre-TempT time for domestic-long haired breeds was longer than domestic-short haired breeds, this may have been due to extra time being needed to identify the anus which may be visually obscured in longer haired animals.
Feline participants were restrained on an examination table and canine patients were on the floor. The location in the room and difference in restraint technique (extrinsic factors) may have contributed to the shorter Pre-TimeT and TTime for feline rectal thermometry than for canines. This difference may also be due to species variation. It is interesting that despite variation in rectal thermometry between canine and felines, no difference was seen in axillary thermometry. In both species however, axillary thermometry took significantly less time than rectal thermometry.
In all cases restraint served to maintain instrument position and stability. In rectal thermometry, restraint involved preventing cranial movement away from the thermometer, shifting the tail (as needed) and maintaining animal stability in the lateral and dorsal-ventral planes. Moving forward away from the instrument is a common action, which can require additional force to prevent. Axillary thermometry involved abducting the forelimb enough to facilitate instrument placement after which the pet is allowed to maintain a static position with stabilizing support. The time associated with maintaining additional movement restriction and tail handling may have contributed to the longer rectal thermometry time.
Research on the effect of appointment duration is limited in veterinary medicine [
21,
22]. In dental literature examination time is strong predictor of appointment duration [
23]. The clinical value of thermometry makes it a standard in most veterinary examinations and a likely contributor to appointment duration. Appointment duration not only impacts patient satisfaction, it can also effect clinician time, the wait time for subsequent appointments and the number of patients that can be seen in a given time [
17,
18,
21,
22]. In this study, animal restraint was performed by a licensed technologist and thermometry by a veterinarian. In many clinics thermometry is performed by a single individual with or without the support of an owner. The handling time would likely be increased for both axillary and rectal thermometry without the benefit of supportive restraint.
Efforts that minimize stress in the veterinary clinic is an active area of research [
14,
15]. Patients that have negative experiences are more fearful in subsequent veterinary appointments and prolonged stress can adversely affect patient health [
1,
3,
13,
15]. Struggling and volatilization are likely to increase a patient’s sympathetic tone effecting epinephrine, cortisol and glucose levels that may alter normal vital assessment parameters [
16,
19]. The extent to which variation in thermometry methods influence animal stress is unknown and outside the scope of this study. However, given the significant difference in duration between thermometry methods this is an area of future research that should be considered.
This study has a number of limitations. Conducting the study at one location, as one prospective study, requiring continued owner approval, creates some selection bias. These results may not represent results at other locations or with other pets. The study took place on the same day of the week, based on investigator availability, and at relatively the same time. The crossover design of the study was meant to minimize individual variation. Although patients were randomly assigned the order of their measurements the investigators were not able to be blinded. Comparing a random sampling of subgroups from either the rectal or axillary data produced similar results and the level of significance in the data is compelling, however we cannot eliminate the possibility of observer bias in this study.
Device measurement time was standardized as 6-seconds but can vary between commercial devices. With technology changes the advantage of this standardization was to focus on factors outside of the specific instrumentation used. This does not minimize the importance of device selection, which should be considered in the timing of thermometry.
Duration and handling are not the only things to consider when selecting a thermometer. Accuracy is especially important [
4,
13]. Both thermometers used in this study meet federal accuracy standards in reporting the temperature at the sight of measurement. By convention, rectal thermometry is often used as an indication of “core temperature” with clear parameters on the clinical significance of values at that location [
4,
5,
13]. Studies have looked at corelating axillary thermometry to rectal temperatures in pets [
24,
25,
26,
27,
28]. It may be that conversion factors are needed to interpret axillary temperatures or relate them to rectal or core temperature. The effort to correlate alternate thermometry locations with rectal temperature may be replaced with studies determining the clinical significance of values at locations like the axilla. The purpose of this study was not to interpret the quality of the thermometer or the temperature values at a specific location, but rather to consider how the method of thermometry potentially effects handling and appointment duration.
5. Conclusions
In a standardized clinical scenario, we found that TTime associated with axillary thermometry was less than that of rectal thermometry in both canine and felines pets. This was due to the time associated with animal approach and restraint (Pre-TempT). This may have implications when considering clinic workflow, appointment duration and patient handling time.
Author Contributions
Conceptualization, methodology, resources, and writing were contributed by: C.B.; investigation, data curation and formal analysis was contributed by: C.B., O.B. and A.L All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
The animal study protocol was approved by the Institutional Review Board (or Ethics Committee) of the University of Wisconsin La Crosse (protocol code 5-21, approved October 2021).
Informed Consent Statement
This study involved no human subjects. Informed consent was obtained from all clients prior to including their pet in the study.
Data Availability Statement
Not applicable.
Acknowledgments
The authors would like to acknowledge the patient owners and clinic staff for their participation and support of this study.
Conflicts of Interest
The axillary thermometers used in this study were donated by Mella Pet Care, Chicago Illinois. The authors declare no other conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
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