Am J Physiol Regul Integr Comp Physiol 292: R167R175, 2007. First published August 24, 2006; doi:10.1152/ajpregu.00338.2006.

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Physiology and Pharmacology of Temperature Regulation

A three-compartment thermometry model for the improved estimation of changes in body heat content
Ollie Jay,1 Louise M. Gariepy,1 Francis D. Reardon,1 Paul Webb,2 Michel B. Ducharme,1,3 Tim Ramsay,4 and Glen P. Kenny1
Laboratory of Human Bioenergetics and Environmental Physiology, School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada; 2Yellow Springs, Ohio; 3Defence R&D Canada, Toronto, Ontario, Canada; and 4Ottawa Health Research Institute, The Ottawa Hospital, General Campus, Ottawa, Ontario, Canada
Submitted 18 May 2006; accepted in nal form 21 August 2006
1

Jay, O, Gariepy LM, Reardon FD, Webb P, Ducharme MB, Ramsay T, Kenny GP. A three-compartment thermometry model for the improved estimation of changes in body heat content. Am J Physiol Regul Integr Comp Physiol 292: R167R175, 2007. First published August 24, 2006; doi:10.1152/ajpregu.00338.2006.The aim of this study was to use whole body calorimetry to directly measure the change in body heat content ( Hb) during steady-state exercise and compare these values with those estimated using thermometry. The thermometry models tested were the traditional twocompartment model of core and shell temperatures, and a threecompartment model of core, muscle, and shell temperatures; with individual compartments within each model weighted for their relative inuence upon Hb by coefcients subject to a nonnegative and a sum-to-one constraint. Fifty-two participants performed 90 min of moderate-intensity exercise (40% of VO2 peak) on a cycle ergometer in the Snellen air calorimeter, at regulated air temperatures of 24C or 30C and a relative humidity of either 30% or 60%. The core compartment was represented by temperatures measured in the esophagus (Tes), rectum (Tre), and aural canal (Tau), while the muscle compartment was represented by regional muscle temperature measured in the vastus lateralis (Tvl), triceps brachii (Ttb), and upper trapezius (Tut). The shell compartment was represented by the weighted mean of 12 skin temperatures (Tsk). The whole body calorimetry data were used to derive optimally tting two- and three-compartment thermometry models. The traditional two-compartment model was found to be statistically biased, systematically underestimating Hb by 15.5% (SD 31.3) at 24C and by 35.5% (SD 21.9) at 30C. The three-compartment model showed no such bias, yielding a more precise estimate of Hb as evidenced by a mean estimation error of 1.1% (SD 29.5) at 24C and 5.4% (SD 30.0) at 30C with an adjusted R2 of 0.48 and 0.51, respectively. It is concluded that a major source of error in the estimation of Hb using the traditional two-compartment thermometry model is the lack of an expression independently representing the heat storage in muscle during exercise. body heat storage; calorimetry; muscle temperature; thermoregulation

THE DERIVATION OF THE CHANGE

in body heat content ( Hb) is of fundamental importance to the physiologist assessing the exposure of the human body to environmental conditions that result in thermal imbalance. In theory, the measurement of body heat exchange using simultaneous measures of direct and

indirect calorimetry is the only method whereby Hb can be directly determined. Thus the difference between metabolic heat production using the stoichiometric relationship of the products and reactants of oxidative metabolism (indirect calorimetry) and the total heat lost from the body can be used to estimate Hb. By denition, Hb is the product of the change of the mean temperature of the tissues of the body ( Tb), the total body mass (bm), and the average specic heat of the tissues of the body (CP). Hence, for a given body mass of a known CP, Tb is an acceptable surrogate measure of Hb. Because of the limited accessibility of direct calorimeters, thermometry is most often used to estimate Tb and thereby derive Hb. The most common thermometry approach is the two-compartment model (4) that estimates Tb by separating the body into a core compartment temperature measured using the change in rectal temperature ( Tre) and a shell compartment temperature measured using the change in mean skin temperature ( Tsk). The relative contribution of each compartment to Tb is determined by a sum-to-one ratio of weighting coefcients that is dependent upon the external environment. Recommended weighting coefcients are variable, however, and for a hot environment, the suggested shell coefcient ranges from as low as 0.05 (40, 41) to as high as 0.2 or 0.3 (5, 11, 20, 26). Previous research has shown that the two-compartmental thermometry model greatly underestimates Tb and therefore Hb (15, 18, 38, 43). Despite this, the two-compartment model is still extensively used for the estimation of Tb and Hb, both as an analytical tool for assessing individual heat load status for a wide range of subpopulations (1, 7, 36, 49) and extensively as a physiological criterion for maximal heat exposure (2, 16, 17, 19, 22). A major source of error in the prediction of Hb may be accounted for by independently considering the thermal inuences of muscle tissue using a three-compartment thermometry model of core, muscle, and shell. Such a model was rst described by Nadel et al. (28) using partitional calorimetry and intermittent intramuscular temperature measurements taken in the quadriceps and later by Webb (45) using suit calorimetery but with no concurrent measurements of muscle temperature. Total body mass is composed of 40% muscle mass compared
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Address for reprint requests and other correspondence: O. Jay, Univ. of Ottawa, School of Human Kinetics, 125 Univ., Montpetit Hall, Rm. 367, Ottawa, Ontario, Canada K1N 6N5 (e-mail: ojay@uottawa.ca). http://www.ajpregu.org

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Table 1. Mean descriptive characteristics for male and female participants

n Age, yr Weight, kg Height, cm BSA, m2 BMI, kg/m2 VO2peak, ml kg
1

min

Male Female

26 26

25.8 (9.0) 5118 23.7 (4.2) 3818

78.8 (12.9) 106.860.1 63.1 (10.0) 97.241.5

179.0 (6.0) 193.0167.6 167.3 (6.2) 180.0154.9

1.97 (0.17) 2.371.69 1.71 (0.14) 2.041.35

24.5 (3.3) 31.819.6 22.7 (3.3) 35.717.3

49.5 (7.3) 63.130.8 40.5 (8.1) 56.728.0

Values given are means, standard deviation (in parentheses), and range (maximumminimum). Body surface area (BSA) is estimated using the equation of DuBois and DuBois (8). BMIs, body mass indices; VO2peak, volume of peak oxygen consumption.

with 5% skin mass (44), and the specic heat capacity of muscle tissue is very similar to that of skin (13). Despite this, temperature of the skin is independently considered in the two-compartment thermometry model (i.e., shell), whereas muscle temperature is not. Furthermore, the traditional twocompartment thermometric approach arbitrarily includes muscle mass as part of the core. However, active muscle tissue can be the primary source of thermogenesis during exercise, and inactive muscle may be a major heat sink during exercise. Therefore, overall muscle tissue temperature is typically subject to a greater change relative to measures of core and skin temperature. The aim of the present study was to compare the change in body heat content, as estimated using a two-compartment thermometry model, and a three-compartment model, incorporating the thermal inuences of muscle mass, with those values directly measured using whole body direct calorimetry. It was hypothesized that the difference between the estimates for change in body heat content by a three-compartment thermometry model relative to direct calorimetry, will be less than by the two-compartment approach.
METHODS

Participants After approval of the experimental protocol from the University of Ottawa Research Ethics Committee, 52 healthy, nonsmoking normotensive participants volunteered (26 males, 26 females) for the study. Of the participants, 22 (10 males, 12 females) were exposed to an air temperature of 30C and relative humidity (RH) of 30%; 6 (3 males, 3 females) to 30C, 60% RH; 14 (9 males, 5 females) to 24C, 30% RH; and 10 (4 males, 6 females) to 24C, 60% RH. The characteristics of the participants are given in Table 1. The body composition of each participant was measured using dual energy X-ray absorptiometry (DEXA) by which the body mass is partitioned into fat tissue mass (mf), lean tissue mass (ml), and bone mass (mb). Lean tissue mass (ml) is further subdivided into muscle mass (51.0% of ml), skin mass (11.0%), white matter, gray matter, eye, nerve, lens, and cartilage mass (12.9%), blood mass (25.0%), and cerebral spinal uid mass (0.1%) (12, 37). Using these components (13), we determined the mean average specic heat of the body (CP) (Table 2). Instrumentation

thermocouple probe (Mon-a-therm General Purpose Temperature Probe) inserted to a minimum of 12 cm past the sphincter. Aural canal temperature (Tau) was measured using a aural canal thermocouple probe (Mon-a-therm Tympanic) placed in the aural canal until resting against the tympanic membrane (determined by the participant reporting an audible scratching sound), following which it was withdrawn slightly. The aural canal probe was held in position and isolated from the external environment with cotton and ear protectors. Skin temperature was measured at 12 points over the body surface using 0.3-mm diameter T-type (copper/constantan) thermocouples integrated into heat ow sensors (Concept Engineering, Old Saybrook, CT). Thermocouples were attached using surgical tape (Blenderm, 3M, St. Paul, MN). Mean skin temperature (Tsk) was calculated using the 12 skin temperatures weighted to the regional proportions, as determined by Hardy and DuBois (14): head 7%, hand 4%, upper back 9.5%, chest 9.5%, lower back 9.5%, abdomen 9.5%, bicep 9%, forearm 7%, quadriceps 9.5%, hamstring 9.5%, front calf 8.5%, and back calf 7.5%. Regional muscle temperature was measured using a exible intramuscular temperature probe (Physitemp Instruments, Clifton, NJ, model IT-17:18, type T, time constant of 0.1 s) inserted into the vastus lateralis (Tvl), triceps brachii (Ttb), and upper trapezius (Tut). Using an aseptic technique, we anesthetized the skin, subcutaneous tissue, and muscle to a maximum depth of 40 mm by inltrating 3 ml of lidocaine with 2% epinephrine. An 18-gauge, 45-mm nonradiopaque FEP polymer catheter (Medex Canada, Toronto, ON, Canada) was then inserted at an angle and parallel to the long axis of the muscle into the anesthetized tract to the required depth ( 3 cm). The catheter stylet was then withdrawn, and the temperature probe was inserted into the catheter shaft. The probe assembly, including the catheter shaft, was secured to the skin with sterile, waterproof dressing (23, 25). The implant site for the vastus lateralis was approximately midway between, and lateral to, a line joining the anterior superior iliac spine and the superior aspect of the centre of the patella (2325). The triceps brachii muscle temperature probe was inserted approximately midway between, and lateral to, a line joining the greater

Table 2. Mean DEXA results for male and female participants

n Lean Mass, kg Fat Mass, kg Bone Mass, kg C p, kJ kg 1 C
1

Male Female

26 26

Esophageal temperature (Tes) was measured by placing a pediatric thermocouple probe of 2 mm in diameter (Mon-a-therm Nasopharyngeal Temperature Probe; Mallinckrodt Medical, St. Louis, MO) through the participants nostril while they were asked to sip water through a straw. The location of the probe tip in the esophagus was estimated to be at the T8/T9 level, in proximity to the left ventricle and aorta. This position is based upon the equation of Mekjavic and Rempel (27). Rectal temperature (Tre) was measured using a pediatric
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61.89 (6.56) 74.0150.48 44.66 (6.14) 58.8133.40

14.96 (8.30) 31.723.24 15.88 (6.26) 38.534.73

3.27 (0.46) 4.022.38 2.59 (0.34) 3.181.91

3.48 (0.05) 3.563.39 3.43 (0.05) 3.533.34

Values given are means, standard deviation (in parentheses) and range (maximumminimum). Specic heat of the human body (Cp) calculated from partitioning total body mass into lean, fat, and bone; and lean mass subdivided into muscle mass (51.0%); skin mass (11.0%) combined white matter, gray matter, eye, nerve, lens, and cartilage mass (12.9%); blood mass (25.0%); and cerebral spinal uid mass (0.1%); and assigning a specic heat for each component (12, 13, 37). DEXA, dual energy X-ray absorptiometry.
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tubercle of the humerus and the superior aspect of the olecranon of the ulna (23, 25). The upper trapezius muscle temperature probe was inserted 3 cm superior to the center point between the acromion process and superior angle of the scapula. All temperature data were collected using a HP Agilent data acquisition module (model 3497A) at 15-s intervals. These data were simultaneously displayed and recorded in spreadsheet format on a personal computer (IBM ThinkCentre M50) with LabVIEW software (Version 7.0, National Instruments, Austin, TX). Direct calorimetry. The modied Snellen whole body air calorimeter was employed for the purpose of measuring whole body changes in evaporative and dry heat loss, yielding an accuracy 2.3 W for the measurement for total body heat loss. A full technical description of the fundamental principles of the original Snellen calorimeter has been published (39), and a further technical report describing all modications and performance characteristics is also available (34). In summary, the calorimeter incorporates a semirecumbent constant load cycle ergometer and is housed within a climatic chamber slightly pressurized ( 8.25 mmHg) to nullify potential air leakage through the calorimeter walls. Differential air temperature and humidity are measured over the calorimeter by sampling the inuent and efuent air. The water content is measured using precision dew point thermometry (model 373H; RH Systems, Albuquerque, NM), while the air temperature is measured using RTD high-precision thermistors ( 0.002C, Black Stack model 1560, Hart Electronics, American Fork, UT). Air mass ow through the calorimeter is estimated by differential thermometry over a known heat source (2 750 W heating elements) placed in the efuent air stream. Differential temperature over the heater is measured using a third aforementioned high-precision thermistor placed downstream from the heater. Air mass ow rate (kg air/min) is continuously measured during each trial. Data from the calorimeter were collected continuously at 8-s intervals throughout the trials. The real-time data were displayed and recorded on a personal computer (Dell OPTIPLEX GX270) with LabVIEW software (Version 7.0, National Instruments). Evaporative heat loss per minute was calculated using the following equation Evaporative Heat Loss Mass flow (Humidityout Humidityin) 2.427 (1)

Metabolic energy expenditure (M) was calculated from minute average values for VO2 and respiratory exchange ratio using the following equation M V O2 RER 0.7 ec 0.3 1 RER ef 0.3 (3)

where ec is the caloric equivalent per liter of oxygen for the oxidation of carbohydrates (21.13 kJ), and ef is the caloric equivalent per liter of oxygen for the oxidation of fat (19.62 kJ). Change in body heat content. Change in body heat content ( Hb) was measured using the temporal summation of metabolic heat production by indirect calorimetry and the net evaporative and dry heat exchange of the body with the environment by direct calorimetry. The cumulative change in heat storage over the exercise period was therefore calculated using the following equation
t

Hb
t 0

W dt

(4)

where M metabolic rate, (R C K) rate of dry heat loss (radiation, convection, and conduction), E rate evaporative heat loss, and W rate of external work being performed. Experimental Protocol All participants volunteered for two separate testing sessions. On the rst day, an incremental cycle ergometer VO2 peak test was performed. On the second day, the calorimetry experimental protocol was performed. Testing days were separated by a minimum of 72 h. All calorimeter trials were performed at the same time of day, with each participant entering the calorimeter at 8:45 AM. Participants were asked to arrive at the laboratory in a fasted state, consuming no tea, coffee, or food that morning, and also avoiding any major thermal stimuli on their way to the laboratory. Participants were also asked to not drink alcohol or exercise for 24 h before experimentation. Following instrumentation, the participant entered the calorimeter regulated to an ambient air temperature of either 24C or 30C and either 30% or 60% relative humidity. The participant, seated in the semirecumbent position, rested for a 45-min habituation period until a steady-state baseline resting condition was achieved. Subsequently, the participant cycled at 40% of their predetermined VO2 peak for a maximum of 90 min. The exercise duration was such that a steadystate condition dened as a rectal temperature stable within 0.1C, a variation of less than 3% for metabolic heat production (M W) and constant total heat loss (dry heat loss evaporative heat loss), would be achieved for at least the nal 10 min of exercise (31, 46 48). For all experimentation, clothing insulation was standardized at 0.2 to 0.3 clo [i.e., cotton underwear, shorts, socks, sports bra (for women) and athletic shoes]. Statistical Analyses

where (Humidityout Humidityin) is the difference in absolute humidity across the calorimeter (g water kg air 1), and 2.427 is the latent heat of vaporization of sweat (kJ kg sweat 1) (50). Dry heat loss per minute from radiation, conduction, and convection was calculated using the following equation Dry Heat Loss Mass flow (Temperatureout Temperaturein) 1.005 (2)

where (Temperatureout Temperaturein) is the difference in air temperature across the calorimeter (C), and 1.005 is the specic heat of air [kJ (kg air C) 1]. Indirect calorimetry. Oxygen consumption (VO2) was measured by the open circuit technique using expired gas samples drawn from a 6-liter uted mixing box. Expired gas was analyzed using calibrated electrochemical gas analyzers (AMETEK model S-3A/1 and CD 3A, Applied Electrochemistry, Pittsburgh, PA). Expired air was recycled back into the calorimeter chamber to account for respiratory conductive and evaporative heat loss. Before each session, gas mixtures of 4% CO2, 17% O2, balance N2 were used to calibrate the gas analyzers and a 3-liter syringe was used to calibrate the turbine ventilometer.
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The data from all participants were pooled and analyzed according to ambient air temperature (24 and 30C). Data were not separated further according to relative humidity due to the confounding effect of a reduced number of data points upon predictive power, and the traditional two-compartment thermometry approach employing weighting coefcients based upon air temperature not relative humidity (4). This also ensures an optimal statistical validity by attaining a wide variation in the calorimetric and thermometric measures between participants, under each air temperature condition. Change in body heat content ( Hb) as measured using calorimetry was solved for mean body temperature ( Tb) using the following equation
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Tb

BODY HEAT CONTENT AND DIRECT CALORIMETRY

Hb/ bm Cp

(5)

where Hb is the change in body heat content by calorimetry (kJ), bm is total body mass (kg), and CP is specic heat of the human body as estimated using DEXA (in kJ kg 1 C 1). Two-compartment thermometry model of mean body temperature. The traditional two-compartment thermometry model (4) for mean body temperature ( Tb) is Tb X Tre 1 X Tsk (6)

overtting. The adjusted R2 statistic, which takes into account the possibility of overtting, is given by the following expression: 1 {[(n 1)SSE]/[(n k j)SSM]}. When k is large relative to n, the adjusted and unadjusted R2 statistics will be somewhat different, with the adjusted R2 statistic being lower. With this in mind, the adjusted R2 statistic is reported in the present study.
RESULTS

Thermometry Data Mean values for mean skin temperature and all of the measurements of core and regional muscle temperature at each air temperature condition are given for baseline preexercise rest and across the nal 10 min of exercise (Table 3). These data show that during the nal 10 min of exercise, rectal temperature (Tre) was 0.24C (SD 0.23) and 0.25C (0.15) higher than esophageal temperature (Tes) and 0.62C (0.23) and 0.45C (0.27) higher than aural canal temperature (Tau) at 24C and 30C, respectively. Active muscle temperature, vastus lateralis (Tvl), was higher than the two inactive muscle temperature sites of the triceps brachii (Ttb) and the upper trapezius (Tut) by 1.23C (0.98) and 0.53C (0.99), respectively, at 24C, and by 0.63C (0.74) and 0.62 (0.87), respectively at 30C. Mean core temperature (Tc), Tes, and Tre was higher than Tvl by 0.29C (0.53), 0.33C (0.59), and 0.57C (0.56), respectively, at 24C, and by 0.08C (0.37), 0.07C (0.42), and 0.32C (0.39), respectively, at 30C. Whereas Tau was 0.03C (0.23) and 0.14C (0.36) lower than Tvl at 24 and 30C, respectively. Comparison of Thermometry with Calorimetry An example of the minute-by-minute calorimetry data with concurrent thermometry data is given in Fig. 1. The mean differences between calorimetry and the two thermometric models for the change in mean body temperature ( Tb) and change in body heat content ( Hb) at 24 and 30C are detailed in Table 4. The optimal coefcients for the estimation of Tb using the traditional two-compartment thermometry model of core represented by Tre and shell represented by Tsk for the direct, whole body calorimetry data measured in the present study were 24 C; Tb 30 C; Tb 0.52 Tre 0.90 Tre 0.48 Tsk Adjusted R-squared: 0.07 0.10 Tsk Adjusted R-squared: 0.37

where Tre is the change in rectal temperature and Tsk is the change in mean skin temperature. The value for X is the proportion of the body representing the body core. The value of X may not exceed 1 or be less than 0. Three-compartment thermometry model of mean body temperature. The three-compartment thermometry model (28, 45) for mean body temperature ( Tb) is Tb X1 Tcore X2 Tsk X3 Tmus (7)

where Tcore is the change in core temperature represented by either rectal (Tre), esophageal (Tes), aural (Tau) temperature or an unweighted mean of the three measurements (Tc); Tsk is the change in mean skin temperature; Tmus is the change in muscle temperature represented by either vastus lateralis (Tvl), upper trapezius (Tut), triceps brachii (Ttb), the unweighted mean of inactive muscle temperature (Tinact), or an unweighted mean of all three measurements (Tm). Values for coefcients X1, X2, and X3 may not exceed 1 or be less than 0, and the sum of all coefcients must equal 1. Derivation of optimal two- and three-compartment models for mean body temperature. The two- and three-compartment thermometry models were individually t to the mean body temperature data obtained using calorimetry with the optimization technique of quadratic programming. In summary, the quadratic programming problem is to derive coefcient values that minimize a quadratic function while simultaneously satisfying the set of linear constraints (32). These constraints were that individual coefcients within each model may not exceed 1, be less than 0, and the sum of all coefcients within each model must equal 1. Quadratic programming was performed using the statistical programming language R (the open-source software R can be downloaded at http://www.r-project.org/). Goodness-of-t. To demonstrate and compare the predictive power of the optimal two- and three-compartment thermometry models for Tb, the goodness-of-t was measured for each by simply adapting the R2 statistic from linear regression. For n observations and k parameters in a given model, the quadratic programming problem incorporates j equality constraints (in the present case, j 1). Let the ith response be denoted by yi (for each thermometry model, yi Tbi), the ith tted value be denoted by yi, and let the mean response be denoted by y. Then the variance of the response about the mean is estimated by SSM [i 18n (yi y)2]/(n 1) and the residual variance, with respect to the quadratic programming model, is estimated by SSE [ (yi yi)2]/(n k j). Dened as the proportion of the variance in the response explained by the model, the R2 statistic is given by the expression [1 (SSE/SSM)]. As with linear regression, the R2 statistic in a quadratic programming model has a maximum value of 1. However, as SSE may be greater than SSM, R2 may be less than 0. It is possible for SSE to be greater than SSM as the model does not contain a constant intercept. In the event of this, the model is considered biased, that is, a systematic under- or overestimation of the response. For a biased model, the average observed response will actually perform better as a predictor than the model itself. In other words, the variance about the mean (SSM) will be less than the variance about the tted values (SSE) and R2 will be negative. As is the case with linear regression, if there are many parameters in the model, it is possible for the R2 statistic to be biased by
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The resultant estimation of Hb using the two-compartment model for Tb shows a very poor predictive capability at 24C and a systematic shortfall compared with calorimetry (as indicated by the negative adjusted R2 value) at 30C. Change in body heat content ( Hb) is below the line of identity between thermometry and calorimetry in 43 of the 52 total participants, and in 26 of the 28 participants at 30C (Fig. 2A). Results for the quadratic programming analyses of the threecompartment model of core, muscle, and skin for the estimation of Tb are detailed for 24C (Table 5) and 30C (Table 6). At 24C, it is evident that in all of the models Tsk has a consistent inuence with a weighting coefcient between
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Table 3. Mean values for skin temperature and all of the measurements of core and regional muscle temperature
Core Temperatures Tre Tau Tc Tvl Ttb Tut Tinact Tm Regional Muscle Temperatures Skin Tsk

Tes

Baseline (24C) Steady-state (24C) Delta ( ) (24C) Baseline (30C) Steady-state (30C) Delta ( ) (30C)

36.64 (0.30) 37.27 (0.25) 0.63 (0.23) 36.81 (0.23) 37.43 (0.39) 0.62 (0.31)

36.82 (0.20) 37.51 (0.25) 0.69 (0.23) 36.98 (0.23) 37.68 (0.37) 0.70 (0.31)

36.48 (0.30) 36.90 (0.32) 0.42 (0.18) 36.74 (0.35) 37.22 (0.41) 0.48 (0.33)

36.65 (0.23) 37.23 (0.22) 0.58 (0.22) 36.84 (0.23) 37.44 (0.36) 0.60 (0.30)

34.17 (0.75) 36.94 (0.64) 2.78 (0.79) 34.97 (0.59) 37.36 (0.39) 2.40 (0.49)

32.77 (0.83) 35.71 (1.12) 2.94 (0.88) 34.58 (0.83) 36.74 (0.83) 2.16 (0.65)

35.11 (0.67) 36.38 (0.76) 1.27 (0.42) 35.78 (0.84) 36.74 (0.87) 0.95 (0.37)

34.01 (0.65) 36.06 (0.82) 2.04 (0.64) 35.18 (0.76) 36.74 (0.75) 1.56 (0.46)

34.08 (0.62) 36.33 (0.65) 2.25 (0.62) 35.11 (0.58) 36.95 (0.56) 1.84 (0.38)

31.29 (0.74) 32.36 (1.02) 1.08 (0.61) 33.20 (0.77) 33.75 (0.88) 0.55 (0.46)

AJP-Regul Integr Comp Physiol VOL Fig. 1. Example of the minute-by-minute whole body direct calorimetry data for total heat gain and heat loss (top) with concurrent thermometry data (bottom) during exercise at 40% VO2 peak.

All values are means, standard deviation (in parentheses) for baseline preexercise rest, nal 10-min of exercise (steady state) and changes between steady state and baseline (Delta ). Data are presented for n 24 at 24C and n 28 at 30C. Core temperature measured in the esophagus (Tes), rectum (Tre), aural canal (Tau), and the unweighted mean of all three measurements (Tc). Regional muscle temperature measured in the vastus lateralis (Tvl), triceps brachii (Ttb), upper trapezius (Tut), an unweighted mean of inactive (Tlb and Tut) muscle temperature (Tinact), and an unweighted mean all muscle temperature measurements (Tm). Skin temperature (Tsk) measured as a weighted mean of 12 sites (14).

30 C; Tb

24 C; Tb

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0.51 Tre

0.63 Tre

0.20 and 0.30. Models employing Tre as a representation of the core yield the higher adjusted R-squared statistics, with muscle effectively represented by Tvl, Ttb, and Tinact. In contrast, the three-compartment models at 30C are minimally inuenced by Tsk; however, Tre again provides the best representation of the core relative to Tes, Tau, and Tc. By incorporating Tre as core, Tvl, Ttb, and Tinact again provide effective representations of the muscle compartment. At both 24 and 30C, all models using Tut as muscle yielded the lowest adjusted R-squared statistics. The optimal three-compartment models for the data in the present study were

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0.03 Tsk

0.24 Tsk

0.13 Tvl

0.46 Tinact

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Adjusted R-squared: 0.51

Adjusted R-squared: 0.48

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Table 4. Comparison of whole body, direct calorimetry, and traditional thermometry

Thermometry Calorimetry Two-compartment Threecompartment

Change in body heat content in kJ, Hb Change in mean body temperature in C, Tb %Difference between thermometry and calorimetry for Hb

24C 30C 24C 30C 24C 30C

260.7 (94.1) 258.7 (95.7) 1.06 (0.36) 1.11 (0.47)

220.0 (108.1) 161.7 (61.1) 0.87 (0.35) 0.68 (0.30) 15.5% (31.3) 35.5% (21.9)

259.6 (109.1) 261.6 (82.6) 1.04 (0.34) 1.09 (0.35) 1.1% (29.5) 5.4% (30.0)

Values for calorimetry obtained using direct whole body calorimetry. Values for thermometry obtained using Hb Tb bm Cp, where bm is total body mass (kg), Cp is specic heat of the human body (kJ kg 1 C 1), and Tb is change in mean body temperature. Optimal two-compartment models: Tb (0.52 Tre) (0.48 Tsk) for 24C, and Tb (0.90 Tre) (0.10 Tsk) for 30C; Optimal three-compartment models: Tb (0.63 Tre) (0.24 Tsk) (0.13 Tvl) for 24C and Tb (0.51 Tre) (0.03 Tsk) (0.46 Tinact) for 30C, where Tre is change in rectal temperature, Tsk is change in mean skin temperature, Tvl is change in vastus lateralis temperature and Tinact is change the unweighted mean of the two inactive muscle sites.

The resultant estimation of Hb using the optimal threecompartment thermometry model for Tb shows an unbiased relationship with calorimetry at both 24 and 30C (Fig. 2B).
DISCUSSION

The main ndings from this study show that the traditional two-compartment thermometry model of core and shell underestimates changes in body heat content ( Hb) during moderate-intensity, steady-state exercise by between 15 and 35%. Upon investigating change in mean body temperature ( Tb) within the two-compartment thermometry model, there was a systematic underestimation of Tb relative to calorimetry. At 30C, the adjusted R-squared statistic for the twocompartment model was negative ( 0.37), indicating a bias, that is, simply using the group mean value for Tb of 1.11C measured using calorimetry provides a better estimation than the two-compartment model. The three-compartment thermometry model of core, muscle, and skin at both 24 and 30C was unbiased and was found to consistently yield a more precise estimate of Tb and therefore Hb than the twocompartment model. The notion of a three-compartment thermometry model for the improved estimation of Hb has been supported for some time. However, the present study, with the exception of Snellen (38), is the rst to use whole body direct air calorimetry to assess such a concept. Nadel et al. (28) developed the following theoretical three-compartment model for the calculation of absolute mean body temperature (Tb) during positive and negative work on a semirecumbent bicycle ergometer, by estimating the mass of working muscles from the data of Stolwijk and Hardy (42) Tb 0.67Tes 0.23Tm 0.10Tsk

where Tes is esophageal temperature; Tm is quadriceps temperature, and Tsk is mean skin temperature. Webb (45) proposed an alternative three-compartment thermometry model for the estimation of change in mean body temperature ( Tb) during level and uphill walking with a suit calorimeter. While muscle temperature was not measured, the estimated weighting coefcients for muscle suggested substantial heat storage during exercise Tb where 0.5 Tre 0.4 Tm 0.1 Tsk Tm is the

Tre is the change in rectal temperature,

change in mean muscle temperature; and Tsk is change in mean skin temperature. The three-compartment models derived in the present study suggest that the role of skin temperature in the estimation of Tb becomes progressively less with increasing ambient air temperature as is the case with the traditional two-compartment approach (4). As such, the model derived at 30C is similar to that proposed by both Webb (45) and Nadel et al. (28). Furthermore, the core weighting coefcient derived by Webb (45) is almost identical to the 30C model in our study, while the weighting coefcient derived by Nadel et al. (28) is closer to that of the 24C model; however, Tre provided the best representation of the core compartment at both 24 and 30C. The muscle compartment weighting coefcient of 0.46 at 30C is very similar to that proposed previously by Webb (45), but the coefcient of 0.13 at 24C is lower than previously suggested with the body shell (i.e., Tsk) having a more prominent effect. Whole body, direct air calorimetry was used by Snellen (38) to develop an improved estimation of Hb and therefore Tb. This was a unique study that incorporated multiple tissue measurements, including the estimation of subcutaneous temperature, for individuals exposed to ambient conditions from 12.3 to 35.0C. However, there were considerable limitations of the methodology, in that only seven young male subjects were tested and subcutaneous temperatures were not directly measured, but estimated, using zero-ux heat devices, which have been since demonstrated not to give a reliable estimate of muscle temperature (3). Furthermore, the multiple linear regression method used for deriving the improved estimating equation for Tb appears statistically unstable due to the number of variables introduced for such a small sample size, potential collinearity between variables, and the use of a nonintercept design, giving disproportionate R-squared statistics. In the case of the present study, a large subject group of 52 was used, ranging in age and physical characteristics; active and inactive muscle temperatures were directly measured using intramuscular probes; and the analytical techniques for deriving an improved estimation of Tb were meticulously considered, so that collinearity between variables was avoided and fallacious R-squared statistics were not attained. Mean body temperature is dened as the average temperature of the tissues of the body (4). In the two-compartment thermometry model, change in mean skin temperature is inde292 JANUARY 2007

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Table 5. Results for quadratic tting of three-compartment model of core ( Tcore), skin ( Tsk) and muscle ( Tmus) for 24C
Measures Tcore Tmus X1 ( Tcore) Optimal Coefcients X2 ( Tsk) X3 ( Tmus) Adjusted R-Squared

Tc Tes

Tre

Tau

Tm Tvl Ttb Tut Tinact Tvl Ttb Tut Tinact Tvl Ttb Tut Tinact

0.58 0.61 0.62 0.31 0.54 0.63 0.64 0.37 0.57 0.58 0.59 0.24 0.49

0.19 0.23 0.24 0.30 0.25 0.24 0.24 0.29 0.24 0.20 0.21 0.30 0.22

0.23 0.16 0.14 0.40 0.22 0.13 0.12 0.34 0.19 0.22 0.20 0.46 0.29

0.48 0.37 0.33 0.22 0.32 0.48 0.47 0.32 0.45 0.44 0.38 0.20 0.36

Data obtained for the model of Tb (X1 Tcore) (X2 Tsk) (X3 Tmus). The term Tcore is represented by esophageal (Tes), rectal (Tre), aural canal temperature (Tau), or the unweighted mean of all three core temperature measures (Tc). The term Tsk is represented by mean skin temperature. The term Tmus is represented by vastus lateralis (Tvl), triceps brachii (Ttb), upper trapezius (Tut) temperature, the unweighted mean of all three measurements (Tm) or the unweighted mean of the two inactive muscle sites (Tinact). Model constraints are the sum of X1, X2 and X3 must equal 1, and all coefcients must be between 0 and 1.

partment is enclosed in the core compartment once muscle becomes well perfused with blood during exercise. However, the data from the present study show that the change in both active and inactive muscle temperature is poorly represented by any measure of core temperature. After 90-min of exercise, change in Tvl, Ttb, and Tut were 4.0, 4.3, and 1.8 times greater that of Tre at 24C; and 3.4, 3.1, and 1.4 times greater than Tre at 30C. Table 6. Results for quadratic tting of three-compartment model of core ( Tcore), skin ( Tsk), and muscle ( Tmus) for 30C
Measures Tcore Tmus X1 ( Tcore) Optimal Coefcients X2 ( Tsk) X3 ( Tmus) Adjusted R-Squared

Tc Tes Fig. 2. A comparison between change in body heat content measured by whole body and direct calorimetry and estimated by thermometry using the optimal two-compartment model (A) and the optimal 3-compartment model (B). Triangle () denotes 24C; Circle (E) denotes 30C. Solid line indicates the line of identity (y x).

Tre

pendently included in the estimation of the change mean body temperature. However, in a typical person, 40% of total body mass is muscle mass, where as only 5% is skin mass (44). The specic heat of muscle (3.639 kJ kg 1 C 1) is very similar to that of skin (3.662 kJ kg 1 C 1), and in the present study, change in mean muscle temperature was 2.08 and 3.35 times greater than the change in mean skin temperature at 24C and 30C, respectively. It therefore seems logical to consider changes in muscle temperature when estimating changes in mean body temperature. It has previously been viewed in the two-compartment thermometry model that the muscle comAJP-Regul Integr Comp Physiol VOL

Tau

Tm Tvl Ttb Tut Tinact Tvl Ttb Tut Tinact Tvl Ttb Tut Tinact

0.49 0.51 0.48 0.00 0.36 0.65 0.63 0.13 0.51 0.51 0.49 0.00 0.37

0.10 0.23 0.20 0.00 0.11 0.12 0.10 0.00 0.03 0.19 0.17 0.00 0.08

0.41 0.27 0.31 1.00 0.52 0.23 0.27 0.87 0.46 0.30 0.35 1.00 0.56

0.45 0.25 0.31 0.17 0.40 0.42 0.48 0.19 0.51 0.32 0.39 0.17 0.45

Data obtained for the model of Tb (X1 Tcore) (X2 Tsk) (X3 Tmus). The term Tcore is represented by esophageal (Tes), rectal (Tre), aural canal temperature (Tau), or the unweighted mean of all three core temperature measures (Tc). The term Tsk is represented by mean skin temperature. The term Tmus is represented by vastus lateralis (Tvl), triceps brachii (Ttb), upper trapezius (Tut) temperature, the unweighted mean of all three measurements (Tm) or the unweighted mean of the two inactive muscle sites (Tinact). Model constraints are the sum of X1, X2, and X3 must equal 1 and all coefcients must be between 0 and 1.
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The ndings of the present study suggest that the source of error observed with the two-compartment thermometry model for the estimation of Tb and therefore Hb is an underestimation of the tissue temperature transients of the body during exercise. The three-compartment model by no means reects the level of complexity of the thermal interactions between various tissues of the body; however, the inclusion of a muscle compartment does give a degree of representation to the considerable inuences of muscle heat load upon body heat content. Indeed, regional muscle temperature at any point in time is the result of regional differences in metabolic rate, conductive heat loss to adjacent tissue, and deep and peripheral convective blood ow (9). Furthermore, the convective transfer of muscle heat load to cooler tissues in the body has been demonstrated to signicantly prolong the elevation of core temperature and presumably body heat content after exercise, with hyperemic previously active musculature considered to have the most profound inuence (23, 25). When using a muscle compartment for the estimation of Tb, the present ndings suggest a minimal predictive role of the shell compartment at warmer ambient temperatures. In addition to the fact that total body mass is composed of a relatively small proportion of skin mass, the contribution of mean skin temperature to the estimation of Tb is further confounded by several factors. Skin temperature is strongly inuenced by skin blood ow, which itself can be signicantly modied independently of whole body thermal state. For example, varying levels of exercise intensity result in different skin-to-muscle perfusion ratios, with increasing blood ow shunted away from skin to working muscle groups with greater levels of exercise (23). Furthermore, factors such as hydration status (29), training status (30), level of acclimatization (10), and the administration of topically applied medications, such as corticosteroids and nicotinates (21), have been demonstrated to alter skin blood ow during exercise. The use of mean skin temperature as an estimate of the thermal status of the skin is itself also subject to potential error. Measurement methods range from as few as four sites (33) to as many as 12 sites (14), and as mean skin temperature is in reality an interface temperature between the body surface with the external environment, factors such as clothing and environmental conditions will also have an inuence. Similarly, as with the two-compartment thermometry model, the data from the present study indicated that Tre was the core measurement that best associated with Tb within the three-compartment thermometry model. Models using Tes as an indicator of core temperature provided the worst association with Tb. This is thought to be a consequence of Tes generally representing the central arterial blood temperature (6). Although a response lag is inevitable with Tre, it is suggested that during steady-state exercise Tre provides a better representation of equilibrated tissue temperatures of the deep visceral/splanchnic region. The use of Tau also provided an acceptable means by which changes in core temperature could be represented in the three-compartment thermometry model; however, Tau was consistently lower than both Tre and Tes, possibly due to insufcient insulation of the probe in the aural canal from the air within the calorimeter and are therefore thought to be less reliable. The present study does have limitations in terms of the range of ambient conditions tested and the employment of only one
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workload. Indeed core and active muscle temperature has been demonstrated to be dependent upon relative workload (35); therefore, thermometry models for Hb may also differ across the range of workloads that steady-state exercise is possible. Furthermore, the employment of the three-compartment thermometry model does require the direct measurement of intramuscular temperature; however, in many cases, such an invasive technique may not be possible. The development of an accurate noninvasive method of estimating muscle temperature using novel zero-heat-ux methods is ongoing (3, 51). Despite the inclusion of a muscle compartment yielding an improved estimation of Tb relative to the traditional twocompartment thermometry model, the optimal models only explained 48% and 51% of the variation found in Tb at 24C and 30C, respectively. Increasing the number of tissue temperature measurements intermediate to the core and shell may further improve the estimation of Tb somewhat; however, the determination of the primary sources of individual variability in body heat content is of paramount importance for its more precise estimation. Further research must therefore be conducted to elucidate the relative effects of factors such as adiposity, age, gender, physical tness, and acclimation upon Hb. In conclusion, whole body direct air calorimetry shows that a two-compartment thermometry model of core and shell for the derivation of Tb underestimates Hb by between 15 and 35% under the conditions tested in this study. A threecompartment thermometry model independently removed the statistical bias seen with the two-compartment model, including the thermal inuences of muscle, and consistently yielded a more precise estimate of Tb and therefore Hb.
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