Measurement of body temperature is an important diagnostic and monitoring tool in veterinary medicine but when compared with human medicine there are limited methods available. In human medicine tympanic membrane thermometry has become popular (Haugan et al, 2013). The technique provides an accurate estimation of core body temperature as the tympanic membrane shares a blood supply with the brain via the carotid artery (Bock et al, 2005).
There has been recent interest in the use of tympanic membrane thermometers in both dogs and cats (Sousa et al, 2011; Sousa et al, 2013). Veterinary-specific tympanic membrane thermometers have been designed and marketed to practices. Studies on the accuracy and effectiveness of tympanic membrane thermometry in both the dog (Southward et al, 2006; Greer et al, 2007; Sousa et al, 2011; Lamb and McBrearty, 2013) and cat (Kunkle et al, 2004; Sousa et al, 2013) in experimental settings (Kunkle et al, 2004; Southward et al, 2006; Greer et al, 2007; Sousa et al, 2011; Sousa et al, 2013) have been published with variable results.
The aim of this study was to evaluate a veterinary-specific device in a population of client-owned cats undergoing general anaesthesia and to compare the temperature values obtained with oesophageal and rectal thermometers. It was hypothesised that a veterinary-specific device would provide readings that were as reliable and comparable to oesophageal temperature in a clinical setting.
Materials and methods
The study took place in a first opinion veterinary practice where a convenience sample of 20 cats that were scheduled for elective general anaesthesia and routine surgery during a 4-month period was selected. The study was approved by an appropriate Ethics and Welfare Committee and the participating veterinary practice. The owners of cats included in the study gave their informed written consent for inclusion into the study. Each cat was assessed by the attending veterinary surgeon as clinically normal and in good general health, other than their reason for surgery, prior to inclusion in the study.
The cats were premedicated using a regimen which was dependent on the procedure being performed and individual assessment (Table 1). An intravenous catheter was placed and general anaesthesia induced with propofol (Propoflo Plus, Abbott Animal Health), prior to endotracheal intubation and maintenance of anaesthesia with isoflurane (Isoflo, Abbott Animal Health) in oxygen. The surgical area was clipped and aseptically prepared before the cat was moved into the operating theatre and positioned as required for the procedure. Once the cat was stable under anaesthesia, temperature readings using the three different devices were recorded. Following data collection the planned surgical procedure was carried out and the patients were recovered.
| Premedication | Frequency | Percentage (%) |
|---|---|---|
| Acepromazine + buprenorphine | 12 | 60% |
| Acepromazine, ketamine + methadone | 1 | 5% |
| Buprenorphine + diazepam | 5 | 25% |
| Buprenorphine + medetomidine | 2 | 10% |
Temperature measurement
Oesophageal temperature measurements were taken in Celsius with an oesophageal probe (VetSpecs VSM8 ECG and Core Body Temperature Probe; VetSpec®, Georgia, USA) (OT) which gave a continuous temperature measurement via a digital display to one decimal place. The probe was measured against the body of the cat so that the distal metal ring and middle metal ring were positioned over the heart, a mark was made with tape at the level of the mouth and the probe inserted to this level before being secured to the endotracheal tube. OT was allowed to stabilise until readings no longer changed frequently before data collection commenced.
Tympanic membrane temperature measurements were taken with a veterinary-specific tympanic membrane thermometer (Vet-Temp VT-150, Vet-Direct, Newcastle upon Tyne, UK) (TT) (Figure 1) from the most accessible ear. A plastic cover was used for every temperature measurement as per the manufacturer's instructions. The thermometer was directed down the external ear canal while gently pulling on the pinna to straighten the canal and access the tympanic membrane. Visual confirmation of the probe reaching the tympanic membrane was not achievable. The TT measurements were recorded in Fahrenheit (°F) to one decimal place and later converted to Celsius (°C) during data analysis shown to two decimal places to maximise accuracy.
Rectal temperature measurements were taken in Celsius with a rectal thermometer (Tro-Digitherm Digital Thermometer, Troge, Hamburg, Germany) (RT) to one decimal place. The RT was inserted approximately 2 cm into the rectum and held in the same position for each of the five temperature recordings.
Temperature measurements were obtained from all patients prior to surgery, in the same operating theatre using the same equipment throughout. The measurements were taken by chief researcher (FW) and one other RVN. The RT and TT were recorded alternately and consecutively at minute intervals, until five measurements had been obtained with each thermometer over a 5 minute period. The OT was displayed continuously on a monitor and recorded at the same measurement times as RT and TT. All measurements were taken by a registered veterinary nurse who was familiar with the equipment.
Both the tympanic membrane and rectal thermometers were new and only used for data collection during the study. The oesophageal probe was owned by the practice and used for all surgical patients whether included in the study or not. The cats were all placed on a heated surgical table and covered with a blanket.
Data analysis
The raw data were entered into a Microsoft Office Excel 2007 spreadsheet. Descriptive statistics and assessment of normality via the Kolmogorov-Smirnov test were made using the IBM SPSS Statistics Version 20. Agreement between each method of temperature measurement was assessed using the modified Bland and Altman test of agreement (Bland and Altman, 1999) accounting for multiple measurements within each subject. Limits of agreement, mean differences and Bland-Altman graphs were produced using MedCalc and GraphPad Prism 7. Statistical significance was set at p< 0.05 for all hypothesis tests.
Results
Twenty client-owned cats were recruited to the study. Six were male and 14 were female. Age ranged from 0.50 years to 16.91 years (median = 1.04 years) and bodyweight from 2.28 kg to 6.09 kg (median = 3.00 kg). Breeds included 18 domestic short hairs, one domestic long hair and one Siberian. Thirteen (65%) cats were anaesthetised for ovariohysterectomy, two (10%) for lump removal, two (10%) for thyroidectomy, one (5%) for wound repair, one (5%) for cyst removal and one (5%) for luxating patella surgery. Two cats (10%) were receiving carbimazole (Vidalta, MSD Animal Health).
Five temperature measurements from each device were obtained from each cat. There were no missing values giving a total of 300 readings. The majority of measurements (90%) were made by the chief researcher (FCEW). Eighty of 100 (80%) tympanic membrane temperatures were taken from the right ear.
OT measurements ranged from 36.80°C and 39.40°C (median = 37.80°C, range = 2.60°C), TT measurements ranged from 35.61°C and 38.39°C (median = 37.33°C, range = 2.78°C) and RT measurements ranged from 37.00°C to 39.40°C (median = 37.80°C, range = 2.40°C). These results are summarised in a box and whisker plot of temperature measurement in Figure 1. Bland-Altman plots were plotted to illustrate the agreement between TT and OT, RT and OT and for TT and RT (Figures 3, 4 and 5).
The mean difference for the TT was -0.86°C (SD = 0.62°C, 95% CI [-2.39°C, 0.67°C]) when compared with OT. Approximately 9% (n=9) lay within 0.20°C and 27% (n=27) lay within 0.50°C of OT. The mean difference for the RT compared with OT was 0.06°C (SD = 0.28°C, 95% CI [-0.56, 0.67]). Fifty-five percent (n=55) lay within 0.25°C and 94% (n=94) lay within 0.50°C of perfect agreement with OT.
The agreement between TT and the RT was evaluated in order to assess whether or not they could be used interchangeably within practice. The mean difference was -0.93°C (SD = 0.57°C, 95% CI [-2.27, 0.44]).
Discussion
This study confirmed that the veterinary-specific tympanic membrane thermometer used in this study, gave a wider range of measurements, poorer agreement and lower measured temperatures than either the rectal thermometer or oesophageal probe thermometer when used simultaneously in the same anaesthetised cats.
Throughout related veterinary literature, clinically acceptable mean temperature differences have been cited as ±0.20°C (Childs et al, 1999) to ±0.50°C (Southward et al, 2006; Greer et al, 2007, Sousa et al, 2011). It could be argued that a difference of 0.50°C would be clinically unacceptable as a rise or fall in temperature to this degree could affect clinical judgement. An agreement of ±0.20°C would be necessary to ensure that correct decisions are made in the continuing care of an animal patient and ensure that high standards are upheld in the search to find accurate and reliable thermometers. In this study only 9% of TT results lay within 0.20°C of OT. In comparison, 56% of RT results lay within 0.20°C of OT. For the purpose of this study a mean difference within 0.20°C will be viewed as clinically acceptable. The TT fails to meet these standards, but the RT has a mean difference <0.20°C and far exceeds the standards set.
Ninety five percent of TT measurements underestimated those taken simultaneously by OT. There are few other veterinary studies that compare a veterinary-specific tympanic membrane thermometer with core temperature; most researchers have compared tympanic temperature with rectal temperature in conscious animals. Southward et al (2006) used eight experimental bitches to test correlation between tympanic membrane, rectal and pulmonary artery temperatures during general anaesthesia-induced hypothermia. A strong correlation between all three methods was found (r ≥ 0.846 and p < 0.001). Correlation is not as appropriate as Bland-Altman analysis as two methods measuring the same variable are likely to be highly correlated (Hartnack 2014). In agreement with this study, the tympanic-membrane thermometer consistently underestimated pulmonary artery temperature. Greer et al (2007) tested a veterinary-specific tympanic membrane thermometer on eight experimental dogs. They found that the tympanic membrane thermometer measured lower than pulmonary artery temperature values (mean = -0.30°C). This study found a more exaggerated underestimation of core body temperature, which may be due to the use of cats, the use of client-owned animals, the clinical setting or the use of an oesophageal probe to measure core body temperature.
As noted by Greer et al (2007) the underestimation of OT by TT is most likely to do with the complex, ‘L’-shape, anatomy of the ear canal, which makes the tympanic membrane difficult to access with the thermometer. Despite veterinary-specific tympanic membrane thermometers being designed to combat these issues, such as having a longer probe at the end, it is not easier to navigate the external ear canal. The manufacturer recommends pulling the pinna in order to straighten the ear canal; which was done throughout the data collection in this study. It is likely that the TT is accurate but that the temperature measured is actually that of the ear canal rather than the tympanic membrane, giving a lower temperature measurement than the true core temperature.
Human research has found that rectal temperature lags behind core temperature as temperature changes take place throughout the body (Robinson et al, 1998; Lu et al, 2010; Carr et al, 2011; Shin et al, 2013). Therefore, during general anaesthesia, when the patient's core temperature is expected to decrease as a result of lower environmental temperature, redistribution of heat from the core to the periphery and the inability to thermoregulate (Kurz, 2008), it might be predicted that rectal temperatures would be higher than the observed core body temperature. The mean difference of the RT compared with the OT does support this theory, as the mean difference was a positive result (0.06°C), however, in agreement with work by Greer et al (2007), the results were relatively evenly spread about the 0.00°C mark. Sousa et al (2011) listed problems involved in collecting accurate rectal temperatures including the presence of faeces and poor anal sphincter tone during general anaesthesia, which could all cause inadequate contact with the rectal mucosa. These factors could have caused slight inaccuracies within the results causing some measurements to be lower than they might otherwise have been.
Limitations
A limitation of this study is that not all measurements were made by the same researcher. Other members of the team who took temperature measurements were already familiar with the methods of measuring OT and RT, and were trained to use the tympanic membrane thermometer. Other limitations include the differing ear used to measure tympanic membrane temperatures. For optimum results two studies (Heusch and McCarthy, 2005; Smitz et al, 2009) suggest measuring the temperature in both ears and recording the highest, while two other studies (Stavem et al, 1997; Nordås et al, 2005) suggest taking an average of both ear temperatures.
Premedication was prescribed based on individual patient health and analgesia requirements so varied throughout the study. As seen in Table 1 some patients did receive medetomidine, an alpha-2-adrenergic agonist, as a premedicant which could have caused peripheral vasoconstriction (Ramsey et al, 2011) and therefore limited the blood flow to the extremities such as the ear and rectum which could, in turn, alter temperature at these sites. Equally, others received acepromazine, a phenothiazine with vasodilatory properties (Ramsey et al, 2011) that may also have affected regional blood flow and hence temperature recordings. Environmental variation was not controlled or recorded, thermometers were not calibrated and the results of this study are not representative of hyperthermic temperatures or anything more than mild hypothermia. Repeated measures taken from the same patient were used in this study in order to increase results; this can cause limitations as one patient´s measurements are likely to agree more closely to its own other readings than to readings from another patient (Bland and Altman, 1999). This limitation was accounted for in this paper by using a modified Bland Altman test for agreement. Finally, this research is only relevant in normothermic and hypothermic cats within the range of hypothermia observed and no major comment in relation to hyperthermia can be made.
Conclusion
This study has shown that rectal thermometry appears to give an accurate representation of core body temperature with relatively narrow limits of agreement and clinically acceptable variation in client-owned cats under general anaesthesia. Despite ease of use and rapid measurement, the tympanic membrane thermometer underestimated core body temperature to such a degree that it cannot currently be considered clinically useful and should not be used to direct clinical decisions. The tympanic membrane ear thermometer cannot be recommended at present to reliably measure oesophageal temperature in the cat.
Further study is required of tympanic membrane thermometers before they can be recommended for clinical use in cats; developments should be observed and new equipment tested for improved reliability of measurement. Further studies considering the limitations of this paper and with larger sample sizes should be carried out.