Monitoring the Core Temperature

A history of clinical thermometry is available¹¹¹ as are good overviews of the assessment of core temperature.^10,32,201 Sites for taking the temperature, in order of increasing invasiveness, include the forehead, axilla, oral cavity, tympanum, rectum, esophagus, bladder, and pulmonary artery. There is no clear-cut choice regarding the best site to monitor; particular situations demand different techniques. Thermometers that have been employed clinically include mercury-in-glass thermometers (which are now obsolete), electronic thermometers, tympanic radiation thermometers, and liquid crystal thermometers. Whatever instrument is used should have an accuracy of ±0.1° C (0.2° F). The handheld electronic thermometer is a good choice for field emergencies.

Measuring Instruments

The handheld electronic thermometer has replaced the mercury-in-glass thermometer, and it has been widely used for many years. Electronic thermometers can make use of either thermistors or thermocouples as sensors; they have the requisite degree of accuracy, and they are very flexible in application. Although an equilibration time of 1 minute is specified for the typical probe, this is largely because of the need for a stiff casing for ease of insertion; smaller probes are available that can equilibrate in seconds. The digital display of these instruments reduces errors, and the probes can be left in place for continuous monitoring. A quality instrument with a wide range of interchangeable probes is important. Even then, these devices are subject to the usual problems inherent with electronic instruments and rarely have a range low enough to monitor skin temperature in cold environments. A second electronic thermometer with a wide temperature range is important for measuring skin temperature and as a backup for the standard clinical thermometer. Alternate probes and spare batteries for both instruments are essential.

Tympanic infrared radiometers are often used in hospital settings. However, even in this relatively predictable environment, some controversy exists regarding their ability to accurately assess core temperature. These instruments monitor the electromagnetic radiation that emanates from the ear canal; various manufacturers make use of different and complicated electronic circuitry to produce a temperature display. An advantage is that the reading takes only a few seconds,³² but questions remain regarding the overall accuracy of the measurement displayed. In a laboratory situation in which the auditory canal is plugged with a sponge and the probe measures only radiation that emanates from the tympanum, infrared tympanic thermometry provides an excellent estimate of the core temperature.¹⁷⁴ In clinical settings, the results are less consistent. In one study, infrared tympanic thermometry produced core temperatures that were much more variable than rectal temperatures. Even after correcting for the higher rectal values (0.5° C [0.9° F]), tympanic measurements still inaccurately displayed one-third of the temperatures that were more than 37.7° C (99° F). An extended training program did not significantly alter the accuracy of the readings.¹⁴⁷

In one instance, a child who arrived at an emergency department presented with tachycardia and skin vasoconstriction. Separate tympanic infrared thermometers gave core temperatures of 36.4° and 37.6° C (97.5° and 99.7° F); the rectal temperature was determined to be 42.2° C (108° F).¹⁵⁸ Alternatively, in a hospital setting with a trained operator and immobile patients, two brands of infrared tympanic thermometers produced readings that were closer to pulmonary artery readings than those obtained from the axilla or the rectum.¹⁵⁵

The potential benefits of a continuous and easily applied core temperature monitor have led to repeated attempts to validate liquid-crystal thermometers, which are typically placed on the head or neck surface. Unfortunately, the temperature readings produced by this method are not reliable.^10,111 Because these measurements are compromised by the thermoregulatory vascular changes associated with heat conservation and heat dissipation and by changes in ambient temperature,⁸⁰ they are particularly unsuited for field emergency measurements.

Measurement Sites

Although the deep internal temperatures of normothermic humans are reasonably similar, no specific anatomic site represents the “official” core temperature. The temperature at each location is a consequence of a combination of the local metabolic rate, local perfusion rate, proximity to the outer shell, and proximity to other locations that have differing rates of metabolism and perfusion. Nevertheless, because of the generally high overall rates of tissue perfusion in mammals, deep core temperatures rarely differ by more than 0.5° C (0.9° F). The temperature of the pulmonary artery is a good reference temperature for the overall status of the thermal core. At steady state, accepted sites for assessing core temperature differ with regard to varying amounts from this temperature. Esophageal and tympanic temperatures are essentially the same as the temperature of the pulmonary artery,^155,166 whereas rectal temperature averages about 0.4° C (0.7° F) higher, and axillary and oral temperatures are about 0.2° C (0.4° F) and 0.4° C (0.7° F) lower, respectively.^10,110,155

Although esophageal temperature is somewhat difficult to obtain, this is the site that is most likely to accurately reflect the temperature of the pulmonary artery. Measurement at this location accurately follows changes in core temperature and is reasonably noninvasive. For placement, the probe is lubricated, and a small amount of local anesthetic is applied. It is then passed via a nasal passage into the distal portion of the esophagus to the level of the heart. The probe can be moved up and down slightly to obtain the highest temperature. Although this procedure is routinely used in physiology experiments, it is somewhat unpleasant for conscious patients. Esophageal temperature is affected by swallowing for about 30 seconds.

Tympanic temperature as an estimation of core temperature has long been controversial. Because the tympanic membrane is highly vascular and supplied by branches of the external and internal carotid arteries, it should be an ideal site. Nevertheless, over the years many studies have indicated that tympanic temperature is affected by ambient temperature and local facial cooling.¹⁶⁶ Conditions under which these complications can be avoided have now been clarified: (1) if the ear canal is insulated; (2) if the thermocouple is made of fine wire and insulated except at the active junction; and (3) if the thermocouple is in direct contact with the tympanum (which causes the patient to “hear” a continuous and low-pitched sound), then alterations in core temperature are detected more rapidly than by an esophageal probe, are not affected by facial skin temperature, and are otherwise identical to esophageal temperature.¹⁶⁶ In fact, if these conditions are adhered to during facial fanning, tympanic temperature provides a better estimate of brain temperature than do measurements made in the esophagus or the rectum.¹¹⁵ Accurate results were also obtained when an insulated probe was used in conjunction with an optical sensor to detect infrared radiation from the tympanum.¹⁷⁴ Whether the conditions met in these carefully controlled studies can be duplicated in the field is unknown.

In steady-state conditions, rectal temperature is a good index of core temperature, and it can also be used to estimate brain temperature.²⁰⁴ However, when the heat content of the body or of the internal thermal compartments is in flux, rectal temperature changes more slowly than temperatures measured in other commonly used sites.¹⁵⁵ There is a thermal gradient along the rectum, so all measurements should be made at a standard depth; 4 cm is recommended.¹⁰ The higher temperatures recorded in this region may be caused by a combination of low perfusion rates, digestive reactions, and bacterial activity, but there is not clear evidence of this.¹¹¹ For assessing core temperature during outdoor exercise in the heat, the National Athletic Trainers’ Association recommends that only rectal temperature be used.²⁹

Oral temperature is an excellent index of core temperature, provided that the mouth is kept closed. The sublingual pocket is well perfused by blood flow, and responds quite rapidly to alterations in core temperature. Mastication, smoking, fluid intake, and mouth breathing can affect sublingual temperature; these should be avoided during the period that immediately precedes the measurement.^10,110,111 The use of an electronic thermometer with a rapidly responding sensor makes this measurement considerably more accurate and rapid than when it is performed with a mercury-in-glass thermometer.

Although axillary temperature does reflect core temperature, it has a number of negative characteristics and should be used only as a last resort. The axillary temperature is affected by local blood flow as well as by thermal and nonthermal sweating.¹⁰ Changes in core temperature are slow to affect the axillary temperature, and there is high interpatient variability.¹⁵⁵ However, this measurement has proved to be particularly useful for assessing core temperature in infants.^10,111

Estimating Mean Body Temperature

Mean body temperature (MBT) provides a mass-weighted average of body tissue temperature and thus can be related to the heat content of the entire body. For a severely hypothermic patient, MBT provides a way to gauge the potential fall in core temperature (afterdrop) after vessel dilation caused by rapid surface warming. Traditionally, estimates of MBT have been made with the use of a formula that combines mean skin temperature and core temperature. Recently, the validity of such estimates was evaluated for patients undergoing various procedures, including cardiac surgery during extracorporeal circulation; these studies included core temperatures as low as 18.5° C (65.3° F).¹⁰⁶ “Peripheral compartment temperatures were estimated using fourth-order regression and integration over volume from 18 intramuscular needle thermocouples, 9 skin temperatures, and ‘deep’ hand and foot temperatures.”¹⁰⁶ The authors concluded that the estimation of MBT from Burton’s original formula²³ “is generally accurate and precise.”¹⁰⁶ That formula is as follows:

Ramanathan¹⁵¹ found that a rough but reasonably accurate estimate of mean skin temperature could be provided by the temperature of the medial thigh, and that a very accurate estimate of mean skin temperature could be made by measuring and weighting the temperature of four skin sites as follows:

Conductive Heat Exchange

Heat transfer between objects that are in direct contact is called conduction (H_d). The direction of heat flow is always from the higher to the lower temperature. Because conduction involves a direct interaction (i.e., contact) between molecules, this type of heat transfer is minimal except under certain circumstances, such as when sitting on a cold rock with a little insulation. Under such conditions, the heat lost to the rock would be similar to that lost from the remainder of the body surface by radiation and convection. Adequate insulation should be placed under patients who are in contact with hot or cold substrates.¹²⁵ The equation that governs heat exchange by conduction is

The thermal conductivity of a number of substances is given in Table 4-1. Note that water has 25 times the conductivity of air but only one fifth that of granite. Muscle tissue has about twice the conductivity of fat tissue. The conduction of heat through a tissue is called thermal diffusivity. This expression is obtained by dividing the thermal conductivity by the product of the density and the specific heat. The specific heats of various substances are also given in Table 4-1. Water and muscle tissue, which consists mostly of water, have particularly high values. However, specific heats can be misleading, so the volumetric heat capacities are also listed in Table 4-1. Although the specific heat of water is four times that of air, it takes about 3500 times as much heat to raise the temperature of a given volume of water by 1° C (1.8° F) as it does to accomplish the same feat with a similar volume of air. For someone in the water, the consequence of these properties is that skin temperature is within 1° C (1.8° F) of water temperature, and heat transfer to or from the environment is greatly facilitated. In cool water during rest, skin blood flow is minimized as a result of peripheral vasoconstriction. Heat loss is importantly determined by the subcutaneous fat layer; an average-size fat person with 36% body fat by weight begins shivering at a water temperature of about 27° C (81° F), whereas a lean person with less than 10% body fat starts shivering at about 33° C (91° F).¹³⁵

TABLE 4-1 Thermal Characteristics of Select Substances

Convective Heat Exchange

Convection (H_c) can be seen as the facilitation of conduction caused by the movement of molecules in a gas or liquid. This movement decreases the functional value of L, which is the denominator in the conduction equation. Convection can be either forced or natural (free). Forced convection results from gas or liquid movement caused by the application of an external force, such as the movement of a fan or the pumping of a heart. Natural convection results from density changes that are produced by heating or cooling molecules adjacent to the body. These density changes cause the molecules to move with respect to the body surface. For humans, natural convection predominates at air speeds of less than 0.2 m/sec (0.7 ft/sec), whereas forced convection is more important at greater air speeds.¹²⁴

The relationships that define heat exchange as a result of convection can be complicated. They depend on surface temperature profiles, surface shape, flow dynamics, density, conductivity, and specific heat. Any factor that impedes the movement of the boundary layer (i.e., the molecules immediately adjacent to the body) greatly retards convective heat transfer.

Brengelmann and Brown¹⁶ have noted that, under relatively neutral conditions (T_a = 29° C [84.2° F], wind velocity = 0.9 m/sec [3 ft/sec]), about 40% of heat loss from a nude human is mediated by convection. Increases in air or fluid velocity greatly increase convective heat transfer. Fanning a minimally clothed patient will greatly augment heat loss in a cool environment.

Radiative Heat Exchange

All objects at temperatures of more than absolute zero emit electromagnetic radiation. This energy transfer occurs through space and does not require an intervening medium. In any given situation, the object is both transmitting and receiving infrared thermal radiation. In some cases, the object also receives solar radiation. The net heat transfer depends on the absolute temperatures, nature of the surfaces involved, and solar input. Surfaces that are effective absorbers of radiation are also effective emitters of radiation. The idealized “black body” illustrates this property; such bodies absorb all and reflect none of the incident radiation. Conversely, poor absorbers (e.g., a polished silver surface) are also poor emitters. Heat transfer that results from infrared (first-term) and solar (second-term) radiation is given by the following equation:

For temperatures in the physiologic range and where (T_sk − T_a) is less than 20° C (68.0° F), several authors have noted that infrared radiation heat exchange is roughly proportional to T_sk − T_a.^14,168 Also of note is that the spectrum of emitted radiation depends on the temperature of the object. At physiologic temperatures, the predominant wavelengths of emitted radiation are longer (infrared), whereas, at higher temperatures (e.g., like that of the sun’s surface), the predominant wavelengths are shorter (visible radiation) and can be detected by the human eye. This difference leads to some important consequences. The middle infrared radiation that is emitted by mammals is maximal, regardless of skin pigmentation or the color of clothing. However, solar radiation peaks in the visible portion of the spectrum and is differentially absorbed. In other words, dark clothes absorb more heat from solar radiation than do light clothes, but both types emit similar amounts of radiation energy.

Incident radiation can vary drastically under different environmental conditions and may severely tax the body’s ability to respond. Heat input from solar radiation on a cloudless day may exceed by several times the heat produced by basal metabolism; on a cloudless night, there is a significant net loss of radiation to the sky. Under the relatively thermoneutral conditions noted earlier by Brengelmann and Brown,¹⁶ radiant heat loss accounts for about 45% of the total.

Peripheral Thermal Sensors

The entire outer surface of the body is well supplied with sensitive thermoreceptive structures. Because one destination of the output of these transducers is the sensory cortex, many properties of the receptors can be gleaned from direct experience. Afferent thermal information produces both hot and cold sensations, and it is particularly rate sensitive. In addition to cortical input that arrives via the medial lemniscus and the ventrobasal thalamus, the brain receives a large amount of thermal information from pathways that synapse in the reticular area.²⁰ Although cortical thermal input is part of the sensory information that is used to reconstruct the external thermal environment, reticular inputs are more important to the behavioral and autonomic regulation of body temperature.⁴³ This distinction was pointed out by Cabanac,²⁶ who found that internal body temperature determined whether a particular surface temperature was perceived as pleasant or unpleasant. However, altered body temperature did not affect the discriminative (cortically mediated) aspects of the thermal stimulus; subjects had no problem correctly identifying the actual peripheral temperature. This study also confirms the intimate relationship between the thermoregulatory network and the pleasure–pain system.¹⁴²

The structure, location, and properties of peripheral thermoreceptors are well documented. Thermal sensors are free nerve endings, and they are categorized as either warm or cold. Cold receptors are found immediately beneath the epidermis, whereas warm receptors are located slightly deeper in the dermis. The hallmark of both types of receptors is their extremely high rate sensitivity (Figure 4-3, online). Although the static firing rate of cold receptors is usually less than 10 impulses per second, under conditions of rapid temperature change, firing rates are often higher by an order of magnitude. Cold receptors are excited by cooling and inhibited by warming, and they have static maxima at about 25° C (77.0° F); these receptors are active from about 10° C (50.0° F) to 40° C (104.0° F). Warm receptors are excited by warming and inhibited by cooling, and they have static maxima at more than 40° C; they are active from about 30° C (86.0° F) to 45° C (113.0° F). At both ends of the spectrum, more extreme temperatures activate neuronal responses that are phenomenologically reported as “cold pain” and “warm pain.”⁷²

FIGURE 4-3 Impulses from a recording that includes a single warm fiber and a single cold fiber. A, In this recording, a shield was periodically placed in front of and then moved away from the skin site that was innervated by the warm fiber. The discharge stops immediately when the skin is shielded from the radiation source. B, In this recording, the shield was simultaneously placed in front of the skin site innervated by both the warm fiber and the cold fiber. This caused excitation of the cold fiber and inhibition of the warm fiber.

(From Hensel H, Kenshalo DR: Warm receptors in the nasal region of cats, J Physiol [Lond] 204:99, 1969.)

Recent work with the use of cloning and ion-channel characterization has elucidated peripheral temperature transduction mechanisms. A family of related temperature-activated transient receptor potential (TRP) ion channels is highly sensitive to temperature. The cloned receptors TRPV3 and TRPV4 respond over a range similar to that of the warm receptors just described, whereas TRPM8 responds similarly to the cool receptors. TRPM8 also responds to menthol, eucalyptol, and icillin.^117,146 TRPV1, TRPV2, and TRPA1 respond similarly to the heat-pain–sensitive and cold-pain–sensitive neurons. The heat-pain channels (vanilloid receptor 1 [VR1]) also respond to low pH, ethanol, and capsaicin, which is the active ingredient in chili peppers.¹⁴⁴ Alternatively, TRPM2, TRPM4, and TRPM5 respond to warm temperatures and involve insulin secretion¹⁸⁷ and taste.¹⁸³ However, they are not regarded as warm receptors for thermal sensation, because sensory neurons have none of those receptors. In addition to TRP channels, TREK-1 and TRAAK channels may also be related to control of warm and cold perception.¹³⁷

Psychophysical and physiologic studies indicate that thermal receptors are not uniformly distributed across the body surface and that there are far more cold receptors.⁷² Cold receptors are abundant in the face and trunk areas, especially in the lips; however, they are less numerous in the feet and lower legs. The face and fingers have a greater number of warm spots.^153,181 Threshold temperature for the perception of thermal sensation follows the anatomic distribution and is not uniform across the body. The face, particularly near the mouth, is exquisitely sensitive, whereas the extremities, by comparison, have poor sensitivity. Other regions of the body are intermediate in sensitivity.¹⁷⁹

Because peripheral thermal input is intimately involved in regulation of body temperature, heating and cooling different body sites can differentially affect the magnitude of the restorative physiologic response produced. In one study, cooling the forehead was found to be more than three times as effective (per unit area) for decreasing ongoing sweating as was cooling the lower leg.⁴¹ A separate study evaluated regional trunk and appendage sensitivity to cooling by assessing the magnitude of the gasping response that occurs at the onset of immersion. In this case, exposing various parts of the body to water at 15° C (59.0° F) indicated that the upper torso had the greatest cold receptor density or sensitivity (or both). The lower torso was somewhat less sensitive, with the arms and legs exhibiting similar but considerably lower sensitivity.²²

Central Thermal Sensors

Many sites within the body are capable of eliciting generalized thermoregulatory responses. Such areas include the abdominal viscera, spinal cord, hypothalamus, and lower portions of the brainstem.^12,69 The genesis of input to the regulator that results from heating or cooling these areas is poorly understood. Some of the effects may result from modulation of synaptic connections rather than from stimulation of specific thermodetectors per se. Input from central detectors is not rate sensitive; rather, it is a direct reflection of the absolute temperature. The area with the highest thermal sensitivity and that has received the greatest amount of experimental attention is the preoptic area/anterior hypothalamus (POAH). Heating or cooling this portion of the brainstem elicits the entire array of autonomic and behavioral heat loss and heat gain responses, respectively.⁶⁸ Neurons in this portion of the brain exhibit both warm sensitivity and cold sensitivity.¹² Recent work on hypothalamic slice preparations with the use of synaptic blockers has indicated that warm sensitivity may be an inherent property of some of the POAH neurons, whereas cold sensitivity in this area of the brain requires synaptic input.^12,45 Figure 4-4, online illustrates the effects of temperature on the firing rates of three representative types of hypothalamic neurons.

FIGURE 4-4 Effects of temperature on the activity of three different types of hypothalamic neurons. A, Low-slope temperature-insensitive neuron. B, Moderate-slope temperature-insensitive neuron. C, Warm-sensitive neuron. The thermosensitivity in each case was 0.06 (A), 0.5 (B), and 1.1 impulses s⁻¹ • ° C⁻¹ (C). All three types of neurons displayed depolarizing prepotentials, and action potentials occurred when the prepotentials reached threshold. As exemplified in C, putative postsynaptic potentials (especially inhibitory ones) were often observed in all neuronal types.

(From Griffin JD, Kaple ML, Chow AR, et al: Cellular mechanisms for neuronal thermosensitivity in the rat hypothalamus, J Physiol 492:231, 1996.)

The high level of temperature sensitivity shown by one of the cells (labeled “C”) results from the temperature-dependent characteristic of the prepotential. Voltage-clamp experiments indicate that the altered rate of depolarization is most likely the result of an effect on hyperpolarizing (K⁺) conductances.⁶⁴ Work involving the use of hypothalamic slices has also established that about one-half of the thermosensitive neurons also respond to nonthermal stimuli such as osmotic pressure, glucose concentration, and steroid hormone concentration. Such neurons could form the basis for the interactions between the homeostatic systems that are described later in this chapter. Figure 4-5, online illustrates the response of a warm-sensitive POAH neuron in a slice preparation. This cell is excited by increased temperature, low glucose, or increased osmotic pressure.¹³ TRPV protein expression has been detected in the POAH; thus, it was proposed that the TRPV channels may underlie the thermosensitivity found in POAH neurons¹⁴⁴ and that both TRPV1 and TRPV2 channels may be active within the physiologic range of temperature.^93,149 However, a large body of evidence is at odds with the proposal of TRPV1 as a thermosensor.¹⁵⁷ Furthermore, TRPV channels respond to warming with persistent inward cationic currents, and this would produce a change in the resting membrane potential. In the POAH, both warm-sensitive neurons and temperature-insensitive neurons show identical membrane potential responses to temperature change.²⁰³ In addition, several in vivo studies have shown that TRPV1, TRPV3, and TRPV4—all of which are expressed in the hypothalamus—are not likely to be involved in thermoregulation in either the heat or the cold.^31,107,118 It is more likely that POAH warm sensitivity is caused by brief ionic currents that determine the rate of change in depolarizing the prepotentials that occur between two successive action potentials.⁶⁴

FIGURE 4-5 The response of a warm-sensitive preoptic nucleus–anterior hypothalamic area neuron to changes in temperature, glucose concentration, and osmotic pressure. The large downward arrows indicate media changes.

(From Boulant JA, Silva NL: Neuronal sensitivities in preoptic tissue slices: Interactions among homeostatic systems, Brain Res Bull 20:871, 1988.)

Regulator

As mentioned previously, the brain is capable of accurately regulating body temperature under a wide range of conditions. Although almost all portions of the central nervous system can potentially be involved, the most critical neuroanatomic structures for thermoregulation include the spinal cord, brainstem, hypothalamus, and septum. The preoptic area and anterior hypothalamus are particularly important for both integration and sensing of internal temperature.^68,70 Recent advances in neurophysiologic and neuroanatomic techniques have been used to extend our understanding of the systems involved in regulation of body temperature; a number of excellent sources document this progress.^11,122,200 Notable advances include demonstration of the relative independence of populations of neurons that control separate effector systems^91,202 and elucidation of a pathway that conveys cold-sensitive afferent (feed-forward) information to the hypothalamus.¹³¹

A schematic model for regulation of body temperature is presented in Figure 4-6. Credit for much of the information and organization in the figure comes from the authors listed in the figure legend as well as from many others in the field. For ease of understanding, many aspects of the system’s complexity have been simplified or modified. Among the many inputs to this system that are not shown include those mentioned in the section about central thermoreceptors (e.g., glucose concentration, osmotic pressure) as well as factors that are covered later in this chapter (e.g., time of day, hormone levels, pyrogen titer, oxygen concentration of the blood). In addition, central thermoreceptors from many locations in the body provide input to this system.

FIGURE 4-6 A simplified schematic diagram of the basic parts of the nervous system responsible for regulating internal body temperature. Details of how this system functions are given in the text. ac, Anterior commissure; GLU, glutaminergic synapse; GABA, GABAergic synapse; oc, optic chiasm.

(Anatomic, neurophysiologic, and conceptual concepts represented in this image are from Boulant JA: Neuronal basis of Hammel’s model for set-point thermoregulation, J Appl Physiol 100:1347, 2006; Hammel HT: Regulation of internal body temperature, Annu Rev Physiol 30:641, 1968; and Morrison SF, Nakamura K, Madden CJ: Central control of thermogenesis in mammals, Exp Physiol 93:773, 2008. These articles should be consulted for a more rigorous explanation of the details of the thermoregulatory system.)

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