Tympanic temperature reflects intracranial temperature changes in humans
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- Mariak, Z., White, M.D., Lyson, T. et al. Pflugers Arch - Eur J Physiol (2003) 446: 279. doi:10.1007/s00424-003-1021-3
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The purpose of the study was to identify extracranial locations in which temperature changes in humans reflect those of intracranial temperature in a reliable and repeatable way. This was achieved by subjecting 14 non-anaesthetized patients after neurosurgery to face fanning while intracranial and extracranial temperatures were continuously measured. In all patients the cranium was closed and the group included both febrile and non-febrile as well as hyperthermic and normothermic patients. The patients' faces were fanned for 20–30 min, with a small fan at an air speed of 3.25 m s−1. This gave intracranial temperature changes measured in the subdural space (Tsd) that were highly and significantly correlated (r=0.91, P<0.05, n=14) with changes in tympanic temperatures (Tty). A low, statistically insignificant correlation (r=0.40, P>0.05, n=12) was found between Tsd and oesophageal temperatures. In conclusion, intracranial temperature changes, induced by face fanning, were reliably reflected by the changes in Tty.
KeywordsBrain temperatureFace fanningHumansTympanic temperature
Measurement of intracranial temperature in humans is normally not feasible. To estimate brain temperature both physiologists and clinicians either rely on trunk core temperatures (e.g. oesophageal, Tes) or use extracranial temperatures in other specific sites, such as the tympanic membrane (Tty). However, there exist data suggesting that trunk core temperatures in many situations may substantially deviate from true intracranial temperature [11, 16, 22, 25] (for review see ). Also the validity of Tty as an index of brain temperature has been subject to dispute [1, 4, 5, 20, 25], despite the increasing use of infrared thermometry of the tympanic membrane . Consequently, it is still not evident which extracranial site of the body, if any, can reliably represent brain temperature.
Intracranial temperatures are now measured more often following neurosurgery [10, 11, 14, 16, 19, 22], since it has been shown that the ischaemic brain is very sensitive to relatively small increases in temperature . This has provided us with an opportunity to directly explore relationships between intracranial and extracranial temperatures during controlled changes in brain temperature. In an earlier study from this group, performed during neurosurgical operations, brain temperature fluctuations in patients with open cranium were closely followed by changes in Tty, but not by Tes . Shiraki et al. found no relationship between temperature in the brain lateral ventricle/parenchyma and Tty when an unanaesthetized normothermic neurosurgical patient's face was fanned . This case study has been repeatedly cited since 1988 as an argument against the validity of Tty, despite the fact that Shiraki's interpretation of his results was later questioned . Since the publication of Shiraki et al.'s study  there has been no attempt to replicate their protocol in an expanded group of patients.
In the present study we analysed intracranial and extracranial temperatures in unanaesthetized patients following cranial surgery. The purpose of this investigation was to determine whether changes in intracranial temperatures, evoked by face fanning, are more closely followed by the Tty than by a trunk core (oesophageal or rectal) temperature. Face fanning has typically been used in experiments concerning hypothesized selective brain cooling (SBC) in humans [5, 7, 13, 18, 20]. Nevertheless, it needs to be emphasized that our study does not address the effect of facial fanning on brain temperatures because our patients were in different thermoregulatory and clinical states. As previous studies have shown, SBC occurs only in some orders of physiologically hyperthermic mammals , but not in feverish patients  and not in normothermic, non-feverish humans [4, 5, 7]. Additionally, for clinical reasons of patient comfort, we were not able to keep a strictly standardized protocol of fanning.
Materials and methods
The direct measurement of brain temperature during neurosurgical operative procedures and in the immediate postoperative period has been carried out in Bialystok since 1993 . Out of 85 patients examined, a group of 14 (5 women and 9 men, aged between 28 and 70 years of age) were subjected to face fanning while their intra- and extracranial temperatures were monitored. Eight patients underwent surgery for subdural haematoma, 2 for intracerebral haematoma and 4 for brain tumours. Intracranial pressure was monitored in 8 patients. Eight patients were conscious with no neurological signs or symptoms, 4 demonstrated neurological deficits to varying degrees and/or disturbances of consciousness [scores of 9 to 14 on the Glasgow Coma Scale (GCS)], 2 were unconscious but with brisk tendon reflexes and no posturing (score of 8 in the GCS). All patients were operated on under general anaesthesia with isoflurane. Patients and/or their relatives were provided with information about the purpose and details of the investigation and gave their informed consent. No complications related to measurement of intracranial temperature occurred in the patients.
Teflon-coated, implantable copper-constantan thermocouples (Physitemp, USA) were used for temperature measurements. Intracranial temperature was measured on the brain surface, in the subdural space (Tsd), using a thermocouple placed on the brain convexity. To achieve this, a flexible miniature (0.2 mm diameter) thermocouple was mounted into the drainage system, or within an intracranial pressure probe, and left within the subdural space on completion of the neurosurgical procedure. In all patients the subdural probe was placed in the temporo-parietal region, with the tip localized 30–40 mm out of the bone opening. It is important to add that the tip of the thermocouple was not in direct contact with any of the dural venous sinuses. The thermocouples were left in place for 4–16 h postoperatively. Tty was measured with a 0.2-mm-diameter thermocouple that was placed by a laryngologist, with an otoscope, on the anterior, lower quarter of the tympanic membrane . The ear canal was filled with cotton and padded. Rectal temperature (Tre) was measured in all subjects using a 1.2-mm-diameter thermocouple that was introduced 50–60 mm into the rectum. For measurement ofTes the thermocouple was introduced through the nostril to a depth of 0.42–0.46 m . Two patients after initial unsuccessful attempts refused insertion of this probe and for this reason Tes was available only in 12 subjects. For face skin temperature (Tsk), a special flat probe was secured to the forehead. The thermocouples were calibrated and read with a BAT10 thermometer (Physitemp, USA) with a precision of absolute temperature reading of 0.1°C. Temperature sampling was carried out with a data-acquisition system and computer which had a sensitivity of 0.01°C (resolution) to the smallest change in temperature.
A period of at least 4 h was allowed after the completion of surgical procedures to have patients free of the influence of anaesthetics. Isoflurane is rapidly eliminated through the respiratory system and patients become conscious several minutes after cessation of administration of the anaesthetic. Concentration of isoflurane in the expired air falls to 22% of the initial value within 5 min and is negligible after 120 min . Only about 2.5% of the administered dose is metabolized and the metabolites have a half-life of 16 h in the human body.
Six patients who were hypothermic in the postoperative recovery room were covered and passively rewarmed with a small (0.36 m×0.46 m) heating pad until the first signs of sweating appeared. On the basis of this sweating, these six patients were considered to be in a state of mild hyperthermia during face fanning. No passive warming was employed in the four normothermic patients nor in the four patients with spontaneous body core temperatures above 38°C. It was not possible in this study to identify with any reliability the phase of the fever (increase, decrease, plateau) in these particular patients. All investigations were carried out with the subject in the supine position and with the head elevated at an angle of 30°. The ambient temperature was 22°C. It is worth noting that all patients had head dressings of different shape and thickness during the experiments.
Face fanning was carried out from a distance of approximately 0.2–0.3 m with the stream of air directed straight on to the face. A small portable fan was used to produce an air stream with a velocity of 3.25 m s−1, which was not increased further in order to avoid any discomfort to the patients. Generally, all patients reported an unpleasant sensation when fanned. The duration of fanning was between 20 and 30 min, depending on the individual patient's tolerance.
Number of patients in whom core body temperatures decreased, increased or remained unchanged during face fanning (Tre rectal, Tes oesophageal, Tty tympanic, Tsd subdural, Tsk skin temperature)
Figure 1 gives three representative intracranial and extracranial temperature profiles for three separate patients during face fanning. Profile A is an example of a patient who responded with a decrease in subdural temperature, profile B shows a patient with no response in the subdural temperature to face fanning and profile C is a patient's response that typifies those subjects who responded with an increase in subdural temperatures. Seven patients were representative of profile A, three of profile B and four of profile C. It is worth noting that with face fanning the course of Tty was found to follow intracranial temperature both during its increase and decrease. Where no changes in Tsd were noted, Tty also remained unchanged.
Figure 3 compares the means calculated from changes in Tty, Tes,Tre and intracranial temperatures induced by face fanning. The fall of 0.18±0.19°C (mean±SD) in Tty during face fanning did not differ significantly from the mean decrease of 0.15±0.18°C in intracranial temperature. Both these values were significantly greater than the fall of 0.05±0.09°C in Tes and 0.03±0.07°C in Tre during the same period of face fanning (t=1.86; P<0.05).
In a previous study from our group  it was shown that during open brain surgery a decrease in deep and superficial brain temperature was followed by a decrease in Tty, while Tre and Tes continued to increase. Our study  gives strong support to a relationship between intracranial temperature and extracranial Tty, while brain temperature is decreasing. Nevertheless, the experimental set-up was not typical of any physiological situation, because the patients were under general anaesthesia and the content of the cranium was open to ambient air temperature.
It needs to be stressed that this study was carried out in neurosurgical patients in the environment of the post-operative recovery room and not in healthy volunteers in the laboratory. First and foremost, it was necessary to ensure that the experimental procedures did not interfere with the therapeutic process and did not represent potential harm to the patients or cause excessive discomfort. For these reasons restrictions in the set-up and limitation in interpretation of the results had to be accepted as an unavoidable price for the possibility of direct recording of intracranial temperature during face fanning. Thus fanning could be executed only for subjects in the supine position, with an air stream of only moderate velocity. Moreover, the intensity of fanning (duration and distance from the fan) had to be changed if a patient reported discomfort. It was also generally not possible to identify the thermoregulatory status of the patient (except for the six patients who could be considered to have remained in a very mild degree of hyperthermia; see section on procedure in Materials and methods). Furthermore, patients with various pathological conditions, with craniotomies in different locations and with different types of head dressing were included in this study.
All these factors resulted in a limited degree of cooling with a mean fall in Tsd of 0.15±0.18°C and in Tty of 0.18±0.19°C. Additionally, face Tsk remained unchanged or diminished by a maximum only 2.2°C. The median value of the decrease in Tsk was 0.8°C. Nevertheless, a more serious limitation in our set-up must be explicitly stated as follows: it does not allow conclusions to be drawn about the effect of facial fanning on intracranial temperature. Consequently, only the relationship between Tsd and some extracranial temperatures: Tty, Tes and Tre, could be reliably studied in this experiment, as stated in the Introduction.
It is evident, as mentioned above, that numerous factors can potentially influence the effect of fanning on intracranial temperature. Amongst them are the velocity of the air stream, the thermal status of the patient [5, 16], the body position, the shape of the head dressing , the type of intracranial pathology, etc. Each of these variables and especially their interactions, were of necessity, poorly controlled in this experiment in 14 different subjects with 14 different conditions. On account of these reasons we have not described the characteristics and reactions of the different subjects. Nevertheless, the change in the subdural intracranial temperature was measured directly (in contrast to all previously published studies with face fanning) and safely used as an independent variable for studying changes in intracranial temperature and their relationship to changes in extracranial temperature.
The results illustrate that the Tty measured with a thermocouple placed under visual guidance on the tympanic membrane using an otoscope, gives the best indication of intracranial temperature. These results support our previous conclusion  based on examination of patients with open cranium during brain surgery.
Two comments must be added to the above statement. The first concerns the mechanism for a thermal link between brain temperature and Tty. This is hypothesized to be due to convection of heat with warm venous outflow from the brain to the jugular bulb which abuts the tympanic cavity [7, 15]. This outflow can be compromised by those intracranial pathologies that cause increased intracranial pressure, whereas other pathologies (e.g. arterio-venous malformation, AVM) can potentially augment venous outflow from the brain. Our experiments were carried out immediately after surgical evacuation of mass lesions and no increase in intracranial pressure was recorded during temperature measurements. Also, no cases with cerebral AVM were included in the study. A very high correlation was found between changes in Tsd and Tty despite the potential presence of concomitant factors influencing heat exchange from the head. Thus, it can be expected that in healthy people this correlation will be stronger rather than weaker.
Vascular transfer of heat from the brain to the region of the tympanum implies that Tsd and Tty do not change in parallel, but that Tty lags behind Tsd. In a previous study this time delay was estimated to be of the order of a few minutes . A delay of the same order is observed with careful inspection of temperature plots in Fig. 1B and C.
Another comment concerns the volume of brain tissue that can be cooled by face fanning. In this experiment we measured only the temperature of the brain surface in the parietal region but not the temperature inside the brain. In Shiraki et al.'s experiment, the lateral ventricular temperature fell by 0.1°C as a result of 20 min face fanning in a normothermic subject . It may be expected that different regions of the brain would benefit from this kind of external cooling to a different degree; it is likely that the brain surface benefits more than the brain interior. If so, temperature gradients must inevitably form within the brain and the existence of such gradients has been confirmed by direct temperature measurements (for review see ). On the basis of the present study it would seem that it is not possible to estimate any average brain temperature. Clearly, a study including both intraparenchymal/ventricular and subdural temperatures during face fanning would provide more complete information on the extent of brain cooling. However, there will always be fewer opportunities in a clinical setting to carry out such a complex study.
For the reasons mentioned above, we do not address the debate on SBC in humans in this contribution [1, 5, 7, 13, 20, 21]. Surface cooling of the face and scalp was hypothesized to give a decrease in the temperature of venous blood that drains to the intracranium via valveless emissary veins [6, 9]. This is thought to cool the brain to a temperature lower than the trunk core temperature [5, 9]. This mechanism of convective cooling is believed to function only during hyperthermia when the direction of blood flow in the emissary veins is from the scalp and face toward the intracranium [4, 6, 9, 12]. This study included not only patients with mild hyperthermia but also those who were normothermic, as well as those with fever. Face fanning of normothermic patients would be expected to be less effective, since blood flow in the emissary veins is minimal or directed toward the skin surface [4, 9, 12]. This, we hypothesize, accounts for the situations in which no change in intracranial temperature has been evoked with face fanning (Fig. 1). In those patients in whom core body temperature was actually increasing due to fever (and who could at that time have been in functional normothermia or even hypothermia), both intracranial temperature and Tty continued to rise during face fanning (Fig. 1). This finding is in line with a report from this laboratory  which concluded that during fever, intracranial temperature does not decrease below core trunk temperature.
Patients in different thermoregulatory states and not only those in hyperthermia were deliberately included in the group to allow for the possibility of a decrease, an increase and no change in intracranial temperature to be studied. If in all instances Tty had decreased (even along with a decrease in Tsd), an argument could have been forwarded that this decrease was due to fanning of the skin abutting the tympanum . This potential argument can now be easily refuted, because when Tsd did not decrease as a result of fanning, no decrease in Tty was observed. Moreover, as all core temperatures, including the intracranial temperature increased during the experiment, Tty also increased. This was in spite of face fanning. This last observation makes a strong argument for Tty being a core temperature directly related to intracranial temperature, as it was the only extracranial temperature to be significantly correlated with Tsd.
An important additional remark in relation to this study is that Tty was measured with a thermocouple physically placed by an otologist on the tympanic membrane under visual guidance with an otoscope. Our results do not support the view that Tty may be heavily contaminated by the temperature of adjacent tissues, including the skin temperature of the external auditory meatus [1, 13, 18, 20, 24]. The ear canal in our set-up was filled with cotton wool and the external ear was padded to minimize the risk of direct cooling of these regions by the air-stream. Nevertheless, in many instances we have seen that if the tip of the thermocouple rests just on the tympanic membrane, direct fanning of the ear region does not influence Tty, even with no insulation of the ear canal. On the contrary, a rapid decrease in Tty, with no change in Tsd at the start of fanning was always found to be the result of disconnection of the thermocouple from the tympanic membrane.
During face fanning changes in Tty correlated significantly with changes in intracranial temperature. Tes showed a smaller and statistically insignificant correlation with intracranial temperature changes under the conditions of our study. The results of the present study support the use of Tty as an extracranial estimate of intracranial temperatures.
The investigation was performed with the approval of the Ethical Committee of the Medical Academy in Bialystok.