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. 2014 Oct;55(10):939–945.

Comparison between core temperatures measured telemetrically using the CorTemp® ingestible temperature sensor and rectal temperature in healthy Labrador retrievers

Stephanie Osinchuk 1,✉, Susan M Taylor 1, Cindy L Shmon 1, John Pharr 1, John Campbell 1
PMCID: PMC4187377  PMID: 25320380

Abstract

This study evaluated the CorTemp® ingestible telemetric core body temperature sensor in dogs, to establish the relationship between rectal temperature and telemetrically measured core body temperature at rest and during exercise, and to examine the effect of sensor location in the gastrointestinal (GI) tract on measured core temperature. CorTemp® sensors were administered orally to fasted Labrador retriever dogs and radiographs were taken to document sensor location. Core and rectal temperatures were monitored throughout the day in 6 resting dogs and during a 10-minute strenuous retrieving exercise in 6 dogs. Time required for the sensor to leave the stomach (120 to 610 min) was variable. Measured core temperature was consistently higher than rectal temperature across all GI locations but temperature differences based on GI location were not significant (P = 0.5218). Resting dogs had a core temperature that was on average 0.4°C above their rectal temperature with 95% limits of agreement (LoA) between 1.2°C and −0.5°C. Core temperature in exercising dogs was on average 0.3°C higher than their concurrent rectal temperature, with LoA of +1.6°C and −1.1°C.

Introduction

Increases in body temperature and heat stress play a role in numerous canine exercise intolerance syndromes (1–6). However, it is difficult to measure temperature during exercise in the field. In canine sporting settings, the use of a rectal thermometer requires disruption of the activity, requires restraint, and may be influenced by feces in the rectum (7,8).

Ingestible internal temperature sensors have been used in human athletes as a non-invasive means for early recognition of heat stress, in assessing the effectiveness of cooling treatments and as a tool in the prevention of heat stroke. Research on the CorTemp® system (COR-100; Human Technologies, St. Petersburg, Florida, USA) has shown that the ingestible temperature pill telemetry system provides a safe and valid measure of core temperature during rest and exercise in humans. Studies have shown a bias between rectal and core temperature measurements varying in direction and magnitude, thought to be related to the position of the sensor within the gastrointestinal (GI) tract (9).

The CorTemp® ingestible sensor has been evaluated for the measurement of core temperature in humans, horses, and livestock but limited research has been reported in dogs (9–13). Rectal temperature has been considered the standard measurements for core body temperature in dogs (3,14). Although these measurements can be obtained continuously in chronically instrumented dogs trained to run on a treadmill they are not useful methods for evaluating individual exercise intolerant dogs. For exercise applications in the field the esophageal thermometer is impractical and invasive and rectal thermometry requires periodic halting of exercise. Telemetric measurement of core temperature may be useful in the evaluation of exercise intolerance syndromes in dogs in which increases in body temperature are thought to correlate with severity of clinical signs.

The objective of this study was to evaluate the use of the CorTemp® system for its reliability and accuracy in monitoring body temperature in dogs. Our study aimed to establish the relationship between rectal temperature and telemetrically measured core body temperature at rest and during exercise, to examine the effect of gastrointestinal tract location of the CorTemp® sensor on measured core temperature, and to determine the time required for the ingested CorTemp® sensor to exit the stomach and traverse the entire GI tract in dogs.

Materials and methods

Thermometer calibration

Thermometers were calibrated (15) for the evaluation of dogs at rest. Each sensor (COR-100 ingestible temperature sensor) and the rectal thermometer (BD compact contact temperature probe) were immersed in a water bath over a series of 10 temperatures between 35°C and 45°C (1.0°C increments). The water bath was maintained at each temperature for 4 min prior to taking readings from both the rectal and the CorTemp® thermometers (CorTemp® CT2000).

Prior to use in the exercising dog study, each CorTemp® sensor and the rectal thermometer were calibrated in a water bath through a range of temperatures (35°C to 45°C). Temperatures were increased incrementally by 1°C and temperature recordings were taken every 30 s for 10 min.

Temperature in resting dogs

Healthy adult purebred Labrador retriever dogs (n = 6) between the ages of 2 and 10 y were recruited to participate. Dogs had normal physical and neurologic examinations and a body condition score of 2 to 4.5/5. Dogs weighed 20.0 kg to 34.8 kg (median 30.1 kg). No dog had a history of diarrhea or constipation in the preceding 5 d. Dogs were fasted for 8 h prior to sensor administration and had access to water until 2 h prior. A COR-100 ingestible temperature sensor was administered orally with 2 tablespoons of canned dog food in the form of a meatball.

Rectal temperature was measured every 15 min for the first hour after capsule ingestion with simultaneous recording of core temperature (CorTemp CT2000). After the first hour, core temperature was measured every 15 min and rectal temperature was measured every 30 min until the sensor was determined to be in the descending colon. The increased time interval between rectal temperature measurements after the first hour was intended to minimize stress and rectal irritation in the dogs.

Abdominal radiographs were taken immediately after capsule ingestion, every 60 min until the capsule left the stomach (the first radiograph with the capsule in the small intestine), and then every 120 min until the capsule was in the descending colon. The dogs were walked outside every 2 h throughout all data collection. Every 4 h after the capsule left the stomach the dog was offered 500 mL of room temperature water to drink. Rectal temperature and core temperature were taken before ingestion of the water and then again 15 min after. At 8 h after capsule ingestion, the dogs were fed their regular diet. The time for the ingested temperature sensor to reach each portion of the GI tract was recorded. The relationship between core and rectal temperature throughout the day in resting dogs was studied, and changes in measured core temperature based on sensor location in different portions of the GI tract were analyzed.

Temperature during exercise

A second group of healthy purebred Labrador retriever dogs (n = 6) between the ages of 2 and 7 y were recruited to participate. This group had an additional requirement that they must be accustomed to at least 20 min of exercise (running or retrieving) at least 3 times weekly during the 2 mo prior to participation in the study. Dogs had normal physical, orthopedic, and neurologic examinations and a body condition score of 2 to 4/5. Dogs weighed 22.8 kg to 34 kg (median 29.6 kg). Criteria for participation in the study included no vomiting or diarrhea in the previous 5 d, test negative for dynamin-1 mutation causing dynamin-associated exercise induced collapse (dEIC), normal complete blood (cell) count (CBC), serum biochemical profile and blood gas. Dogs were fasted for 8 h prior to sensor administration and had access to water until 2 h prior. A COR-100 ingestible temperature sensor was administered orally inside a meatball of 2 tablespoons of canned dog food. Abdominal radiographs were taken hourly and the exercise protocol was initiated within 30 min after the sensor had left the stomach. The ambient temperature and humidity were measured before exercise was initiated for each dog. Rectal temperature and core temperature were measured every 5 min during the 15 min before the retrieving exercise began. Gait and neurologic examination were videotaped before, during, and after exercise for evaluation and for pace analysis. Dogs were exercised by having them repeatedly retrieve a soft plastic tube (retrieving dummy) thrown 35 to 40 m. Dogs were exercised in this manner for ten 60 s periods. Dogs typically sprinted at full speed to retrieve the dummy each time it was thrown and then ran back to the handler at a slightly slower pace. Strenuous exercise was interspersed with brief (< 5 s) pauses as the dummy was re-thrown. Following each 60 s exercise period during which they repeatedly retrieved the thrown bumper, dogs were restrained for the short period of time (mean 24 s) required to take core and rectal temperature recordings. Average speed for each dog during the retrieving exercise was calculated by dividing the distance run (number of retrieves × length of retrieve) during the 10 min of exercise. The time taken to re-throw the dummy for each retrieve (< 5 s) was not taken into consideration, so this calculation underestimates the actual speed of the dog but allows comparison to similar previously established strenuous exercise retrieving protocols (4). Following exercise, the dogs were walked on a leash for 20 min and temperature measurements were recorded at 1-minute intervals. The location of the sensor within the GI tract was determined radiographically at the end of the walking period.

Results

Sensor calibration

Resting dog study

A linear regression was developed for each sensor across all temperatures. The R2 was > 98% for every sensor so no adjustment of data was required. A discrepancy between the response time (calibration time) of the thermometers was noted, with the CorTemp® sensor being slower to detect temperature changes, but this delay was not considered important in dogs at rest without extreme temperature fluctuations.

Exercise study

The rectal thermometer was faster to detect the change in water bath temperature and reached equilibrium sooner. The period during the water bath calibration in which the difference between readings was > 0.2°C was considered the lag phase of the CorTemp® thermometer, which was on average 2.5 min long (Figure 1). At each time point the CorTemp thermometer was reporting the temperature that had been surrounding its sensor 2 to 4.5 min earlier. Due to these findings, a 2-minute delay was applied to all of the CorTemp temperature measurements for each exercise trial. At each time point the rectal temperature reported was the rectal temperature recorded at that time and the core temperature reported was the CorTemp reading 2 min later.

Figure 1.

Figure 1

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Difference between rectal thermometer reading and CorTemp® sensor reading in the 10-minute period after water bath temperature was increased 1°C. Temperatures were recorded every 30 s with both devices. There was a 2.5-minute lag period (between 2 and 4 min after the temperature change) during which rectal thermometer readings and CorTemp® sensor readings differed by > 0.1°C.

Tolerance

Administration of the CorTemp® sensor was achieved without complications in all dogs. No adverse effects were observed as the sensor passed through the GI tract. Telemetric core temperature monitoring was well-tolerated while most dogs mildly resisted each insertion of the rectal thermometer.

Sensor location and time

The time required for the sensor to reach the stomach following oral administration was less than the time required to position each dog for radiographs. The minimum time (earliest radiograph) for the sensor to be detected in the small intestine was 240 min (4/6 dogs) and the maximum time was 360 min (2/6 dogs). The median time to be detected in the small intestine was 240 min. Time required for the sensor to reach the transverse colon was from 360 to 600 min. Time required for the sensor to reach the descending colon was from 480 to 840 min (median 600 min). Dogs were released to owners following observation of the sensor in their descending colon, and owners were relied upon for observing the time the sensor was passed. Mean total transit time was 2187 +/− 1247 (SD) min, with a range of 840 to 4290 min.

Relationship between core temperature and rectal temperature

Bland-Altman’s limits of agreement method was used to quantitatively assess the agreement between rectal temperature and deep core temperature. The data collected had a bias of 0.4°C, with core temperature measuring higher than rectal temperature. The 95% limits of agreement fell between 1.2°C above and 0.5°C below rectal temperature (Figure 2).

Figure 2.

Figure 2

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Bland and Altman plots of the difference between rectal temperature and telemetrically measured deep core temperature in dogs at rest.

Relationship between sensor location and temperature in dogs at rest

Throughout the day, subjects were confined to a kennel and temperatures were monitored. Measured core temperature was consistently higher than measured rectal temperature, regardless of location of the sensor in the GI tract (Figure 3). The greatest difference between core temperature and rectal temperature occurred when the CorTemp® sensor was located in the descending colon, with the ingested sensor reading an average of 0.56°C higher than rectal temperature. The smallest difference between core temperature and rectal temperature was observed when the sensor was in the transverse colon, where the difference was 0.31°C. An analysis of variance (ANOVA) showed that temperature differences based on GI location were not significant (P = 0.5218).

Figure 3.

Figure 3

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Average temperatures observed across 4 gastrointestinal locations and their concurrent rectal temperature readings.

Exercising Labrador retriever dogs

The ambient temperature ranged from 22.0°C to 24.6°C and humidity ranged from 54% to 77% in the exercise area.

Exercise speed

All 6 dogs successfully completed the 10 min retrieving strenuous exercise protocol without exhibiting ataxia, lameness, or collapse. The median speed of the dogs during exercise was 171 m/min and the range was 145 to 182 m/min.

Sensor location in exercising dogs

The exercise protocol was initiated within 30 min of the time the sensor was first documented in the small intestine, which ranged from 232 to 610 min after ingestion with a mean of 394 min. Following completion of the exercise protocol and the post-exercise 20 min of walking, sensor location was documented radiographically to be in the small intestine (2 dogs) transverse colon (1 dog) or the ascending colon (3 dogs).

Relationship between core temperature and rectal temperature in exercising Labrador retriever dogs

Rectal and core temperatures were graphed against time over the 10-minute exercise protocol and during the 20-minute cool down period. Core temperature had less variation than measured rectal temperature, as illustrated by the smoother curve in Figure 4.

Figure 4.

Figure 4

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Graph of a single dog’s rectal (BD Temp) and core temperature (CoreTemp®) readings throughout the entire exercise protocol. The rectal temperature readings had more variation between points compared to the core temperature. This data has not been adjusted for the 2-minute CorTemp® sensor delay.

Rectal temperature and core temperature raw data and data corrected for the 2-minute CorTemp® response time delay were analyzed using the Bland and Altman Limits of Agreement method. Raw data analysis revealed that core temperature was on average 0.2°C higher than rectal temperature during the exercise protocol. The data showed that 95% of core temperature readings fell between 1.3°C above and 0.9°C below measured rectal temperature (Figure 5).

Figure 5.

Figure 5

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Bland Altman Limits of Agreements graph indicating core temperature was on average 0.2°C higher than rectal temperature, and between +1.3°C and −0.9°C for 95% of the readings in exercising dogs. Raw data not corrected for 2-minute CorTemp® sensor delay.

Data corrected for the 2-minute response time discrepancy between thermometers indicated that core temperature was on average 0.3°C higher than rectal temperature in the exercised dogs. The core temperature reading fell within 1.6°C above and 1.1°C below rectal temperature 95% of the time (Figure 6). Temperatures measured at the beginning and end of the 5-minute measurement intervals could not be adjusted by the 2-minute delay interval and were therefore excluded from these calculations.

Figure 6.

Figure 6

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Bland Altman Limits of Agreement Graph showing core temperature to be 0.3°C higher than rectal temperature and between +1.6°C and −1.1°C 95% of the time in exercising dog protocol. Data corrected for the 2-minute discrepancy between thermometers.

Analysis of core and rectal temperatures over time during the exercise protocol showed that core temperature was faster to rise and fall than rectal temperature, and that maximum core temperature measured in exercising dogs (range: 39.0°C to 42.5°C, median 40.5°C) was higher than maximum rectal temperature (range: 37.9°C to 42.5°C, median 40.3°C).

Discussion

When monitoring rectal temperature in the field, exercise must be halted periodically to restrain the dog and obtain the measurement (6,16–20). This is a limitation to the monitoring of dogs with exercise intolerance manifested during continuous strenuous exercise. Increasing body temperature during exercise may be important in initiating collapse or other signs in dogs with exercise intolerance. Simultaneous evaluation of core and rectal temperature has been performed in experimental dogs chronically instrumented and trained to run on a treadmill, but these invasive protocols cannot be applied in the evaluation of exercise intolerance in individual owned dogs (21–24).

The CorTemp® sensor was easily ingested by all dogs in a canned dog food meatball and passed through the gastrointestinal tract without complication. The dogs in this study were medium to large in size (20.0 kg to 34.8 kg). The CorTemp® ingestible temperature sensor measures 22.4 mm × 10.9 mm, so although useful for monitoring core temperature in Labrador retriever dogs there may be a safety issue using the pill in smaller breeds because of the pill size.

Measured core temperature was consistently higher than measured rectal temperature in the resting dogs. Studies in humans at rest have reported variable results on the relationship between core temperature measured using an ingested telemetric sensor (Tin) and rectal temperature. Lee et al (25) reported Tin to be higher than rectal temperature in the initial part of their 20-minute resting period but not significantly different toward the end. Other authors reported rectal temperature to be higher than Tin during rest periods of 15 or 10 min (26–27). The difference in results can likely be attributed to differences in study design, and especially to the variability in the length of the rest period. The resting dogs in this study had temperature monitored from sensor ingestion until it was visualized radiographically in the descending colon; the median time being 600 min. This is significantly longer than the 20-, 15-, and 10-minute rest periods reported in these human literature examples. In 1 study, human subjects carried out normal daily activities over 24 h, and Tin was consistently 0.2°C higher than rectal temperature (28). The authors hypothesized that rectal temperature may be influenced by cooled blood returning from the lower limbs through the pelvis in conjunction with effects of local temperature at the anal sphincter, making rectal temperatures consistently lower (28).

Studies evaluating ingestible temperature sensors in human subjects typically recommend waiting until the sensor has exited the stomach before commencing measurements (approximately 360 min). This is primarily to reduce the effects of drinking fluids, food, and aerophagia on temperature readings. The current investigation found canine gastric emptying times for the CorTemp® sensor to vary between 232 and 610 min. Canine gastric emptying time is known to be variable. One report found canine gastric emptying time for a sensor similar in size to the CorTemp® sensor varied between 380 and 897 min (29). The unpredictability of the time required for the sensor to leave the stomach makes it necessary to take radiographs to identify sensor location prior to use if temperature measurements from the stomach are undesirable. Tracking the sensor radiographically is associated with increased cost and time for the investigator and may not be available in some field situations. In this study of 6 dogs at rest, core temperature measured when the sensor was in the stomach was not different from core temperature measured in different regions of the GI tract. Total transit times before the sensor was passed in the feces varied between 840 min and 4290 min in our study.

Differences between core and rectal temperature varying in direction and magnitude have been recorded in resting and exercising humans and in anesthetised dogs (9,12,30–31). It has been speculated that these varying biases are due to a physiologic gastrointestinal temperature gradient (9). Surgically placed temperature sensors in the stomach, duodenum, ileum, large intestine, and rectum were used to measure core temperatures in dogs anesthetized with sodium pentobarbitone. Regional variances in gastrointestinal temperature were identified, with the warmest region of the gastrointestinal tract being the lumen of the duodenum and ileum while the stomach, large bowel, and rectum temperatures were significantly lower (12). In our study the dogs had been fasted prior to administration of the sensor so that there would not be a large amount of food in the stomach. It is possible that we falsely increased or decreased the measured core temperature in the stomach by administering the sensor in a small meatball of canned dog food. No statistically significant differences in temperature between GI locations were found in the resting dogs in this study. Because the sensors were administered with a dog food meat ball, it is possible that the core temperature reading in this study could have also been affected by digestive processes.

A discrepancy in response time of the thermometers was noted during calibration. The discrepancy between response times of the thermometers was, on average, 2.5 min, with the rectal thermometer recording the altered temperature of the water bath before the CorTemp® sensor. During exercise and recovery, when temperatures are rapidly changing, using a temperature sensor device with a delay could lead to an inability to accurately measure core temperature at specific time points. In exercise intolerance disorders where clinical signs are correlated with body temperature, this delay could result in inaccurate interpretation of findings. The CorTemp® system uses a temperature sensitive quartz oscillator in which the telemetered signal is inductively coupled by a radiofrequency coil system to a receiver. Research evaluating this system has demonstrated that the time to achieve 90% response during a temperature increase of 5°C is 115 +/− 8 s, and time to cool down to 10% of initial temperature is 114 +/− 4 s (32). This response time, which is larger than with conventional probes in which times are in the order of milliseconds, is primarily due to the large thermal capacity of the silicon-encapsulated sensor rather than the limitations of the electric circuitry used (32).

The data from this investigation indicate that rectal temperature change lags behind core body temperature change in dogs undergoing strenuous exercise followed by a cool-down period. These findings are in agreement with the human literature in which a similar lag in rectal temperature change has been documented (9,13,26,33). The 95% LoA in this study had a larger range (more than double) than the 95% LoA seen in similar studies on exercising humans. Sparling et al (27), Lee et al (25), and Gant et al (31), reported LoA of +0.08°C/+1.44°C, −0.07°C, −0.41°C/+0.27°C, and −0.37°C/+0.07°C, respectively. This difference may be due to a difference in rectal thermometers, recording protocol, and interspecies differences between humans and canines with respect to maximum temperatures achieved during exercise. None of the human studies identified a delay between rectal and CorTemp® thermometer readings during calibration and therefore did not account for this delay in their readings.

There is no consensus in the veterinary literature regarding what degree of bias and level of agreement is acceptable when evaluating 2 methods of temperature monitoring. A few validation studies in humans have delimited an acceptable level of agreement between methods, such as < 0.1°C with 95% LoA between +/− 0.3°C (31) and < 0.1°C and 95% LoA within +/− 0.4°C (9). The authors believe acceptable limits of agreement for evaluating veterinary patients fall between +/− 0.5°C because temperature differences of > 0.5°C could affect diagnostic and treatment decisions made based on a patient’s thermal status. The data in our study show a greater systemic bias and higher LoA both at rest and during exercise than deemed acceptable in the human literature and by the standard of the authors. The large variability between sequential rectal temperature readings (Figure 4) is likely an important contributing factor to the larger range of LoA observed in this study compared with similar human studies that used indwelling rectal thermometers. Measured core temperature had less variation than measured rectal temperature during exercise and cool-down. This variability could be a reflection of minor inaccuracy in the rectal thermometer designed for clinical rather than research use, but calibration in the water bath suggested that the readings were accurate. The variability of rectal temperature recordings was most likely caused by the presence of feces in the rectum and the potentially changing proximity of the temperature probe to the rectal wall with each reading as previously reported (7,8,14).

We conclude that telemetric measurement of core temperature using an ingested sensor and the CorTemp® system is well-tolerated by dogs and allows temperature measurement without halting exercise. Core temperature was higher than rectal temperature in resting and exercising dogs. The limits of agreement between the rectal and core body temperature in this study fell outside limits deemed acceptable by the authors of this study (+/− 0.5°C) in both resting and exercising dogs, potentially limiting the usefulness of this technology when frequent temperature measurements are needed in a small time window or when body temperature is rapidly changing. The rectal thermometer has increased variability between concurrent readings compared to the CorTemp® system and measured rectal temperature lags behind changes in core body temperature. CVJ

Acknowledgments

This study was supported by grants from the WCVM Companion Animal Health Research Fund, the WCVM Interprovincial Summer Undergraduate Research Program, and Hills Pet Nutrition Canada, Inc.

Footnotes

Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.

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