Influence of low ambient temperature on epitympanic temperature measurement: a prospective randomized clinical study
© Strapazzon et al. 2015
Received: 22 April 2015
Accepted: 28 October 2015
Published: 5 November 2015
Epitympanic temperature (Tty) measured with thermistor probes correlates with core body temperature (Tcore), but the reliability of measurements at low ambient temperature is unknown. The aim of this study was to determine if commercially-available thermistor-based Tty reflects Tcore in low ambient temperature and if Tty is influenced by insulation of the ear.
Thirty-one participants (two females) were exposed to room (23.2 ± 0.4 °C) and low (−18.7 ± 1.0 °C) ambient temperature for 10 min using a randomized cross-over design. Tty was measured using an epitympanic probe (M1024233, GE Healthcare Finland Oy) and oesophageal temperature (Tes) with an oesophageal probe (M1024229, GE Healthcare Finland Oy) inserted into the lower third of the oesophagus. Ten participants wore ear protectors (Arton 2200, Emil Lux GmbH & Co. KG, Wermelskirchen, Switzerland) to insulate the ear from ambient air.
During exposure to room temperature, mean Tty increased from 33.4 ± 1.5 to 34.2 ± 0.8 °C without insulation of the ear and from 35.0 ± 0.8 to 35.5 ± 0.7 °C with insulation. During exposure to low ambient temperature, mean Tty decreased from 32.4 ± 1.6 to 28.5 ± 2.0 °C without insulation and from 35.6 ± 0.6 to 35.2 ± 0.9 °C with insulation. The difference between Tty and Tes at low ambient temperature was reduced by 82 % (from 7.2 to 1.3 °C) with insulation of the ear.
Epitympanic temperature measurements are influenced by ambient temperature and deviate from Tes at room and low ambient temperature. Insulating the ear with ear protectors markedly reduced the difference between Tty and Tes and improved the stability of measurements. The use of models to correct Tty may be possible, but results should be validated in larger studies.
Accurate measurement of core body temperature (Tcore) can be fundamental for guiding treatment and triage decisions in emergency care of patients. Although invasive techniques remain the gold standard for Tcore measurement (pulmonary artery or lower third of the oesophagus) these sites are not practical in emergency situations .
Temperature at the tympanic membrane was originally proposed as a less invasive alternative for estimation of Tcore [2, 3]. Previous investigations have shown that with precise placement in the lower anterior quadrant of the tympanic membrane, tympanic temperature is highly correlated with intracranial temperature and changes in temperature  and, importantly, that tympanic temperature is independent from the influence of changes in skin temperature . Epitympanic temperature (Tty) measured with a thermistor probe in the ear canal correlates with Tcore in hypothermic patients [5, 6] and may be a non-invasive alternative for diagnosing the severity of hypothermia in victims of accidental hypothermia [7, 8]. Case reports of deep hypothermic patients have shown that Tty measured prehospitally was comparable to Tcore measured invasively at hospital admission [9–11], but there is still a lack of data on the reliability of epitympanic measurements at low ambient temperature. Early studies compared Tty to oesophageal temperature (Tes) during exposure to moderately low temperatures (between 0 and 10 °C) [3, 12, 13], though ambient conditions in many prehospital situations are commonly much colder with confounding environmental factors. Only two case series (five participants each) describe Tty measured with self-made devices during cold exposure (between −20 and −32 °C) [5, 14]. Pre-hospital use of commercially-available thermometers falls outside the tested operating conditions, since standard probes are validated in-hospital under relatively stable conditions . The aim of this study was to determine if commercially-available thermistor-based Tty reflects Tcore in low ambient temperature and if Tty is influenced by insulation of the ear.
Design, setting and participants
Volunteers were recruited from the local mountain rescue organization. Written informed consent was obtained from all participants prior to participation in the study. The study was approved by the Ethics Committee of the Regional Hospital of Bolzano, Italy. Participants were in good cardiopulmonary health; a clinical history and medical examination were conducted to exclude acute or chronic conditions or abnormalities of the ear canal or upper airways. Cerumen was removed from the ear canal if necessary. Participants were instructed to fast for at least 6 h prior to testing.
We used a randomized cross-over design. Participants were randomly assigned to group A or B; group A was exposed to low temperature first followed by room temperature (n = 15); group B was exposed to room temperature first followed by low temperature (n = 16). A climate chamber with controlled temperature settings was used for the low temperature setting and a medical examination office for the room temperature setting.
An oesophageal probe (9F general purpose sterile probe M1024229, GE Healthcare Finland Oy) was inserted via the naris into the lower third of the oesophagus  after anesthesia of the nasal and pharyngeal mucosa with topical 2 % lidocaine solution. An epitympanic probe (M1024233, GE Healthcare Finland Oy) was inserted according to the product instructions into the right ear and fixed to the lobe using standard surgical tape to prevent displacement. Ten participants additionally used industrial ear protectors (Arton 2200, Emil Lux GmbH & Co. KG, Wermelskirchen, Switzerland) to insulate the ear from ambient air. After successful insertion, the probes were connected to an intensive care monitor (Compact Anesthesia Monitor, GE Healthcare Finland Oy).
Probes were placed after at least 30 min of rest. After placement of the probes in the medical examination office, participants were guided to the first test setting. Measurements were recorded every 5 s for a total duration of 10 min for each location (participants were in a seated position for the testing duration). The interval to transfer to the second test setting and commence data recording was between 3 and 5 min. Complete winter clothing including a hat was allowed during measurements at low temperature but was removed during measurements at room temperature.
Descriptive data are reported as mean ± standard deviation unless otherwise indicated. The Wilcoxon signed-rank test was used to compare (i) Tes and Tty in the same person at a specified duration of exposure and (ii) Tes or Tty in the same person between the first and last measurement. The Wilcoxon-Mann–Whitney test was used to compare Tes or Tty between groups A and B and the Pearson coefficient to correlate differences between Tes or Tty in the room and low temperature setting. The Bland-Altman plot and concordance correlation coefficient (CCC)  were used to quantify the agreement between Tes and Tty. A model to correct Tty was developed using a linear regression. The statistical analyses were performed using SPSS software (Version 22.214.171.124, SPSS Inc., Chicago, IL, USA); the Bland-Altman plot and CCC were calculated using MedCalc (Version 126.96.36.199, MedCalc Software, Ostend, Belgium). P <0.05 was considered significant.
There were 31 participants (two females) with mean age 38 ± 12 years (range 22–61 years). The ambient air temperature in the room temperature setting was 23.2 ± 0.4 °C and in the low temperature setting was −18.7 ± 1.0 °C. In one participant the oesophageal probe was displaced after 5 min at room temperature and the last 5 min of measurements had to be excluded from the analysis. In one participant the monitor data was not stored and manually recorded measurements were used for the last 4 min at low temperature.
Measurements at room temperature
In the room temperature setting, Tty without insulation of the ear was lower at 0 min in group A (32.0 ± 0.9 °C; n = 10) compared to B (34.6 ± 0.7 °C; n = 11, p <0.001), but was not different with insulation of the ear (p = 0.476).
Measurements at low temperature
Temperature measurements during testing at low temperature are shown in Fig. 1b. Mean Tes was 36.7 ± 0.4 °C at 0 min and 36.8 ± 0.4 °C at 9:15 min (n = 31, p = 0.001). Without insulation of the ear, mean Tty decreased from 32.4 ± 1.6 °C at 0 min to 28.5 ± 2.0 °C at 9:15 min (n = 21, p <0.001). With insulation of the ear, mean Tty decreased from 35.6 ± 0.6 °C at 0 min to 35.2 ± 0.9 °C at 9:15 min (n = 10, p = 0.007).
Based on a Bland-Altman plot (Fig. 2), the mean difference between Tty without insulation of the ear and Tes was 7.2 °C and the correlation was not significant (CCC = 0, 95 % CI −0.01–0.01, n = 21). The mean difference was less with insulation of the ear (1.3 °C), which was similar to the mean difference at room temperature (1.5 °C). The correlation between Tty with insulation of the ear and Tes was not significant (CCC = 0.18, 95 % CI −0.02–0.37, n = 10).
In the low temperature setting, Tty without insulation of the ear was lower at 0 min in group A (31.5 ± 1.4 °C; n = 10) compared to B (33.3 ± 1.3 °C; n = 11, p = 0.008), but was not different with insulation of the ear (p = 0.352).
Individual variability in temperature
To understand the influence of inter-individual variability, the difference between Tty and Tes at 3 min at room temperature was correlated to the difference between Tty and Tes at 3 min at low temperature for each individual. We chose 3 min to reduce the variability seen in some measurements in the first minutes after exposure. The measurements were correlated, suggesting that individuals with a large deviation between Tty and Tes in one setting also had a large deviation in the other setting. The correlation was stronger with insulation of the ear (r = 0.907, n = 10, p <0.001) compared to without (r = 0.446, n = 21, p = 0.043).
Model for predicting core temperature
We report the influence of low ambient temperature and individual factors on temperature measured epitympanically using a thermistor-based probe. We found a deviation from the reference Tcore that was markedly reduced with insulation of the ear from ambient air using an ear protector. We also propose a model to correct Tty. Nevertheless, inter-individual variability remained and variations in probe placement likely account for some of the variability.
Influence of ambient temperature
Epitympanic measurements were influenced by ambient temperature. During exposure to room temperature, mean Tty increased by 0.8 °C, whereas it decreased by 3.9 °C during exposure to low temperature. Similarly, mean deviation from Tes was >50 % higher in the low temperature setting compared to the room temperature setting. However, it is interesting that the difference to Tes in our data was reduced with simple external insulation with an ear protector; with insulation the mean difference to Tes was reduced by 52 % in the room temperature setting (difference of 2.9 to 1.5 °C) and by 82 % in the low temperature setting (7.2 to 1.3 °C; Fig. 2). This suggests that the ear cover limits exchange of ambient air, thus creating a “microclimate” in the ear canal, though the influence of ambient temperature on Tty was not completely removed. Moreover, previous studies of Tty that also insulated the ear or ear canal reported that measurements required several minutes to stabilize [5, 12, 13], even if an external device was used to heat the ear protector . In our study, Tty without insulation of the ear did not stabilize and showed rapid and constant decreases over 10 min in low ambient temperature. This explains the differences in Tty at baseline between group A and B—for example, in the room temperature setting mean Tty at 0 min was lower in group A than B because they had already been exposed to low ambient temperature and adaptation to the warmer temperature was still occurring in the first minutes.
We found that the degree of deviation of Tty from Tes in both ambient air settings was different between individuals, i.e. individuals with a large deviation in one setting also had a large deviation in the other setting. This is partially due to differences in placement of the probe. Temperature in the ear canal seems to decrease with increasing distance from the tympanic membrane [17, 18], and thus Tty will be less reflective of Tcore with increasing distance. The distance between the sensor and the tympanic membrane will vary slightly between individuals because of differences in anatomy (length, width, shape) that affect insertion depth. Additionally, there may be other unknown physiological factors such as individual differences in the vascular anatomy of the ear and thermal conductivity and perfusion of the tissues that could influence the absolute difference between Tty and Tcore in an individual.
Measuring Tcore is the only way to accurately assess the severity of hypothermia. There are other commonly used scales to stage hypothermia based on clinical signs and symptoms, but these are not always reliable since there are differences in consciousness among patients at a given Tcore . Patients with mild hypothermia (Tcore 35 to 32 °C) can be treated in the field if they are uninjured or transported to the closest hospital if in-field rewarming is not possible, whereas patients with moderate hypothermia (Tcore <32 °C) should be transported to the most appropriate hospital on the basis of cardiac stability . The results of our study show a large difference (7.2 °C) between mean Tty and Tcore at low temperature, which in practical terms could lead to wrong triage and transport even of normothermic patients. These results also suggest that Tty without insulation of the ear does not stabilize within 10 min, and thus is impractical for applications that require rapid measurement and/or accurate monitoring of changes in Tcore.
The models to correct Tty seem to give a valid estimation of Tes for measurements at room temperature without insulation of the ear and at low temperature with insulation. It was unexpected that the correlation between Tty_c and Tes at room temperature with insulation was low and non-significant, though this is probably due to the small sample size (n = 10). In comparison to these three conditions, it was not possible to create a realistic model for measurements at low temperature without insulation. Thus in order to reliably predict Tcore from epitympanic temperature, modification of currently available devices (i.e. ear cover) and development of an appropriate model to correct for ambient temperature may be necessary. Thermistor-based Tty probes are non-invasive and easy to use and could be used with standard patient monitors. This would also allow continuous monitoring of ECG and Tcore, as recommended in international guidelines for pre-hospital management of accidental and therapeutic hypothermia .
Limitations and further research
The results are based on measurements in healthy, normothermic volunteers at rest in the two reported ambient temperatures and may not be applicable for other populations (e.g. patients in cardiac arrest, trauma) or ambient conditions. The models to correct Tty should be validated with a larger sample size. The lack of correlation between Tes and Tty (or Tty_c) at room temperature with insulation may be due to the small sample size (n = 10). Further investigations are needed to understand if models could account for other factors characteristic of the prehospital environment such as rapidly changing conditions and wind.
Epitympanic temperature measurements are influenced by ambient temperature and deviate from Tes at room temperature and low ambient temperature. Insulating the ear with standard industrial ear protectors markedly reduced the difference between Tty and Tes and improved the stability of measurements over the testing duration. The use of models to correct Tty may be possible, but results should be validated in larger studies.
Ethics, consent and permissions
The study was approved by the Ethics Committee of the Regional Hospital of Bolzano, Italy. Written informed consent was obtained from all participants prior to participation in the study.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Strapazzon G, Procter E, Paal P, Brugger H. Pre-hospital core temperature measurement in accidental and therapeutic hypothermia. High Alt Med Biol. 2014;15(2):104–11.View ArticlePubMedGoogle Scholar
- Benzinger TH. On physical heat regulation and the sense of temperature in man. Proc Natl Acad Sci U S A. 1959;45(4):645–59.PubMed CentralView ArticlePubMedGoogle Scholar
- Brinnel H, Cabanac M. Tympanic temperature is a core temperature in humans. J Therm Biol. 1989;14(1):47–53.View ArticleGoogle Scholar
- Mariak Z, White MD, Lyson T, Lewko J. Tympanic temperature reflects intracranial temperature changes in humans. Pflugers Arch. 2003;446(2):279–84.PubMedGoogle Scholar
- Walpoth BH, Galdikas J, Leupi F, Muehlemann W, Schlaepfer P, Althaus U. Assessment of hypothermia with a new “tympanic” thermometer. J Clin Monit. 1994;10(2):91–6.View ArticlePubMedGoogle Scholar
- Shin J, Kim J, Song K, Kwak Y. Core temperature measurement in therapeutic hypothermia according to different phases: comparison of bladder, rectal, and tympanic versus pulmonary artery methods. Resuscitation. 2013;84(6):810–17.View ArticlePubMedGoogle Scholar
- Brown DJ, Brugger H, Boyd J, Paal P. Accidental hypothermia. N Engl J Med. 2012;367(20):1930–38.View ArticlePubMedGoogle Scholar
- Brugger H, Durrer B, Elsensohn F, Paal P, Strapazzon G, Winterberger E, et al. Resuscitation of avalanche victims: evidence-based guidelines of the international commission for mountain emergency medicine (ICAR MEDCOM): intended for physicians and other advanced life support personnel. Resuscitation. 2013;84(5):539–46.View ArticlePubMedGoogle Scholar
- Oberhammer R, Beikircher W, Hörmann C, Lorenz I, Pycha R, Adler-Kastner L, et al. Full recovery of an avalanche victim with profound hypothermia and prolonged cardiac arrest treated by extracorporeal re-warming. Resuscitation. 2008;76(3):474–80.View ArticlePubMedGoogle Scholar
- Koppenberg J, Brugger H, Esslinger A, Albrecht R. Life-saving air supported avalanche mission at night in high alpine terrain. Anaesthesist. 2012;61(10):892–900.View ArticlePubMedGoogle Scholar
- Strapazzon G, Nardin M, Zanon P, Kaufmann M, Kritzinger M, Brugger H. Respiratory failure and spontaneous hypoglycemia during noninvasive rewarming from 24.7 degrees C (76.5 degrees F) core body temperature after prolonged avalanche burial. Ann Emerg Med. 2012;60(2):193–96.View ArticlePubMedGoogle Scholar
- Keatinge WR, Sloan RE. Deep body temperature from aural canal with servo-controlled heating to outer ear. J Appl Physiol. 1975;38(5):919–21.PubMedGoogle Scholar
- Teunissen LP, de Haan A, de Koning JJ, Clairbois HE, Daanen HA. Limitations of temperature measurement in the aural canal with an ear mould integrated sensor. Physiol Meas. 2011;32(9):1403–16.View ArticlePubMedGoogle Scholar
- Livingstone SD, Grayson J, Frim J, Allen CL, Limmer RE. Effect of cold exposure on various sites of core temperature measurements. J Appl Physiol Respir Environ Exerc Physiol. 1983;54(4):1025–31.PubMedGoogle Scholar
- Hu EW, Wakamatsu BK, Smith DD. Emergency procedures. In: Roppolo L, Davis D, Kelly S, Rosen P, editors. Emergency medicine handbook; critical concepts for clinical practice. Edinburgh: Elsevier Mosby; 2007. p. 1223–75.Google Scholar
- Lin LI. A concordance correlation coefficient to evaluate reproducibility. Biometrics. 1989;45(1):255–68.View ArticlePubMedGoogle Scholar
- Procter E, Strapazzon G, Rilk C, Überbacher N, Brugger H. Temperature gradient in the inner ear canal and implications for epitympanic temperature measurement. High Alt Med Biol. 2014;15:A-281.Google Scholar
- Cooper KE, Cranston WI, Snell ES. Temperature in the external auditory meatus as an index of central temperature changes. J Appl Physiol. 1964;19:1032–35.PubMedGoogle Scholar
- Pasquier M, Zurron N, Weith B, Turini P, Dami F, Carron PN, et al. Deep accidental hypothermia with core temperature below 24 °C presenting with vital signs. High Alt Med Biol. 2013;15(1):58–63.View ArticleGoogle Scholar