New evidence suggests that the physiology of human temperature regulation may be different between males and females (9,11,12). Recently, it was demonstrated that young females show a marked reduction in their capacity to dissipate heat compared with young males during exercise in the heat independently of differences in physical characteristics (11). In light of the potential independent effect of sex on temperature regulation, the study of thermoregulatory control and aging should be assessed separately for males and females. The current body of knowledge regarding age-related changes in heat loss capacity, however, is largely based on comparisons made between young and older males (13,14,30,32,33,36,37). As a result, it is unclear how changes in temperature regulation may differ as a function of age between young and older females.
To date, there have been very few published studies that examined age-related changes in the body’s ability to dissipate heat in females. One study by Drinkwater and Horvath (6) examined the effects of chronological age (12–68 yr) on heat tolerance during continuous 50-min exercise performed at approximately 30% V˙O2max in the heat. The authors reported that heat tolerance was reduced in older females as evidenced by elevated rectal temperatures during exercise at both 35°C and 48°C. This was paralleled by marked reductions in sweat production. In contrast, no differences were observed across ages during a mild heat stress exposure (i.e., 28°C). However, the participants differed in their level of fitness, and as a result, the prescribed work intensity would have produced different rates of heat production. Moreover, no specific comparison was performed between distinct age groups. Thus, it is not possible to determine the extent, if any, of the level of impairment in heat loss between young and older females per se. To the best of our knowledge, a study by Anderson and Kenney (1) is the only study that has compared thermoregulatory responses between young (25 ± 4 yr) and older (56 ± 4 yr) females matched for fitness (and therefore heat production) and body surface area during a prolonged 2-h exercise experiment in the heat (48°C, 10% relative humidity [RH]). They reported marked reductions in whole-body sweat rate in older females, which were evident within the first 30 min of exercise and remained lower throughout the 2-h exercise protocol in comparison with young females. This was paralleled by a greater elevation in rectal temperature; however, the separation in the rise in rectal temperature between young and older females was not evident until well after 30 min of exercise. Given that Anderson and Kenney (1) did not report thermal responses in the early stages of exercise (i.e., <30 min), it is unclear if these age-related differences in heat loss were only evidenced at and beyond 30 min of exercise. The fact that differences in core temperature were only observed after 30 min of exercise suggests that differences in thermal responses between age groups were likely not evident in the earlier stages of exercise for the combined metabolic and environmental heat load employed. Otherwise, marked differences in core temperature and therefore heat storage would likely have been measured at 30 min as well.
Despite our growing knowledge of the effects of aging on the body’s physiological capacity to dissipate heat during challenges to human heat balance associated with exercise in the heat, there remain significant gaps in knowledge. First, it is unclear if differences in heat loss capacity occur in the early stages of exercise (<30 min), wherein the rate of heat loss is still increasing to match the rate of heat production. Depending on the heat load, it can take approximately 30–45 min for the rate of heat loss to match the rate of metabolic heat production under compensable heat stress conditions. If the heat load exceeds the individual’s ability to achieve heat balance, the level of sweat production achieved will be driven by the individual’s maximum sweating capacity, hence the differences observed by Anderson and Kenney (1). Second, no study to date has investigated the heat loss responses of older females during the recovery phase of an exercise-induced heat stress. In previous studies involving young adults, it was observed that skin blood flow (SkBF) and sweating were attenuated in the early stages of postexercise recovery despite a sustained elevation in core temperature (20,21). Similar responses have been observed in highly trained middle-age males (45 yr) (25). However, it is unclear if this postexercise disturbance in thermal homeostasis is exacerbated in older females, especially given the growing evidence that young females have a reduced capacity to dissipate heat relative to their male counterparts (12). Finally, no study has examined heat loss responses between young and older females during successive exercise and recovery periods. Factors influencing local and whole-body heat loss responses during successive exercise/recovery cycles have been shown to have pronounced effects on body heat content and therefore core temperature response in young adults (23). How aging may alter this pattern of response remains to be examined.
The previously mentioned studies have only examined impairments in local heat loss responses (i.e., sweating and SkBF) and the consequence on core temperature response. In addition, the overall effect of regional variations in these responses on whole-body heat loss and body heat content is currently unknown. It is generally accepted that the only way to accurately measure whole-body heat loss capacity and changes in body heat content is by performing simultaneous measurements of heat load and heat dissipation by whole-body calorimetry. In the present study, we examined age-related differences in heat balance during thermal transients associated with intermittent exercise in the heat (35°C and 20% RH) in young (24.3 ± 3.6 yr) versus older (51.3 ± 7.5 yr) females by directly measuring the individual components of heat production and heat loss using a whole-body calorimeter. A fixed rate of heat production of 300 W was used during exercise to maintain an equal heat load. We evaluated the hypothesis that older females would demonstrate a reduced rate of whole-body heat loss, and therefore greater change in body heat content, during each of the four successive 15-min exercise bouts. Despite a larger increase in body heat content, it was hypothesized that no differences in whole-body heat loss would be observed during recovery. As a result, older females would demonstrate a greater cumulative increase in body heat content after the 2-h intermittent exercise protocol compared with young females of comparable fitness level, body adiposity, and body surface area.
After receiving approval of the experimental protocol from the University of Ottawa Research Ethics Committee and obtaining written informed consent, 24 healthy and physically active females (11 young and 13 older) volunteered to participate in the study. Before the experimental session, body density and maximal oxygen uptake (V˙O2max) were measured. Body density was measured using the hydrostatic weighing technique, and body fat percentage was calculated using the Siri equation (34). Body surface area was calculated from the measurements of weight and height according to Du Bois and Du Bois (7). V˙O2max was measured during a progressive cycle ergometer protocol, which consisted of a 2-min warm-up at 40 W followed by 20 W increments every minute until the participant could no longer maintain a pedaling cadence of at least 60 rpm. Electrocardiographic monitoring was used on females 50 yr or older during the maximal exercise test. Participant characteristics are given in Table 1. No account was taken of the younger female’s and perimenopausal older female’s (perimenopausal n = 5, postmenopausal n = 8) menstrual cycle phase during the experimental session.
All participants performed one experimental session in a warm/dry (35°C, 20% RH) environment. The experiments were performed at the same time of day. Participants were asked to arrive at the laboratory after eating a small breakfast, to refrain from consuming alcohol and caffeine for 24 h before experimentation, and to avoid major thermal stimuli on their way to the laboratory. Participants were also encouraged to arrive well hydrated as no fluid replacements were provided during the experiment.
After instrumentation, participants entered the whole-body calorimeter and rested in a semirecumbent position for a 30-min habituation period while a steady-state baseline condition was achieved. Participants then performed four 15-min bouts of cycling at a constant rate of metabolic heat production equal to 300 W separated by 15-min inactive periods except the final recovery period, which was 60 min in duration. All participants were dressed in shorts, a sports bra, and sandals for the duration of the experiment. A urine sample was collected before the start of the experiment and immediately after the final 60-min recovery period for the measure of urine specific gravity (Reichert TS 400 total solids refractometer; Reichert Inc., Depew, NY). Venous blood samples were also collected via a single venipuncture at baseline and immediately after the final 60-min recovery period while the participant rested in a semirecumbent position. Changes in blood hemoglobin and hematocrit were used to estimate the percent change in plasma volume (5).
Whole-body direct calorimetry
Whole-body direct calorimetry is the gold standard to accurately measure the rates of whole-body evaporative and dry heat loss as well as the change in body heat content (18,19). For this reason, the modified Snellen direct air calorimeter was used to measure the rate of evaporative (E) and dry heat loss (R [radiant heat exchange] + C [convective heat exchange] + K [conductive heat exchange]) with an accuracy of ±2.3 W for the measurement of total heat loss (THL). A full peer-reviewed technical description of the performance and calibration characteristics of the Snellen whole-body calorimeter is available (31). Data from the direct calorimeter were collected continuously at 8-s intervals during the experimental sessions. Real-time data were displayed and recorded on a personal computer with Lab-VIEW software (version 7.0; National Instruments, Austin, TX). The rate of evaporative heat loss (EHL; in watts) was calculated from the calorimetry data using the following equation:
where mass flow is the rate of air mass (kg air·s−1), humidityout – humidityin is the difference in absolute humidity (g water·kg air−1) between the inflow and outflow of in the calorimeter, and 2426 is the latent heat of vaporization of sweat (J·g sweat−1). The rate of dry heat loss, from radiation, convection, and conduction (W), was calculated from calorimetry data using the following equation:
where mass flow is the rate of air mass (kg air·s−1), (temperatureout – temperaturein) is the difference in inflow–outflow air temperature (°C) of the calorimeter, and 1005 is the specific heat of air [J·(kg air−1°C)−1]. A 6-L fluted mixing box housed within the calorimeter was used to measure metabolic energy expenditure (M). Expired gas was analyzed for oxygen (O2) and carbon dioxide (CO2) concentrations using electrochemical gas analyzers (AMETEK models S-3A/1 and CD 3A, respectively; Applied Electrochemistry, Pittsburg, PA) located outside the calorimeter chamber. Expired air was recycled back into the calorimeter chamber to account for respiratory dry heat loss and EHL. Before each session, gas mixtures of 4% CO2, 17% O2, and balance nitrogen were used to calibrate the gas analyzers, and a 3-L syringe was used to calibrate the turbine ventilometer. The data derived from direct and indirect calorimetry were thereafter used to calculate the change in body heat content (kJ).
Local heat loss responses and HR
Forearm SkBF was estimated using laser Doppler velocimetry (PeriFlux System 5000; Perimed, Stockholm, Sweden) at the left midanterior forearm. The laser Doppler flow probe (model PR 401 Angled Probe; Perimed) was fixed with an adhesive ring and surgical tape to the ventral forearm in a site determined to be free of superficial veins that demonstrated high flux values and pulsatile activity before the start of the experiment. Local skin temperature was raised to 44°C by using a heating element (model PF 5020 Temperature Unit; Perimed) housing the laser Doppler flow probe 15 min after the start of the final 60-min recovery period and remained on until the end of the experiment (i.e., 45 min), at which point a plateau in SkBF was attained for all participants. SkBF data are presented as a percentage of maximum flux values.
The ventilated capsule technique was used to measure local sweat rate. Sweat production on the upper back was measured from a 3.8-cm2 plastic capsule attached to the skin with adhesive rings and topical skin glue (Collodion HV; Mavidon Medical, Lake Worth, FL). Anhydrous compressed air was passed through each capsule at a rate of 1 L·min−1. Water content of the effluent air was measured using high precision dew point mirrors (model 473; RH Systems, Albuquerque, NM). Subsequently, local sweat rate was determined by calculating the difference in water content between effluent and influent air multiplied by the flow rate and normalized for the skin surface area under the capsule.
HR was monitored, recorded continuously, and stored with a Polar Advantage interface and Polar precision Performance software (Polar Electro Oy, Kempele, Finland).
Core and skin temperatures
Rectal temperature was measured by a thermocouple probe (Mon-a-therm General Purpose Temperature Probe; Mallinckrodt Medical, St. Louis, MO) inserted to a minimum of 12 cm past the anal sphincter. A telemetric pill (Vital Sense ingestible capsule thermometer; Mini Mitter Company Inc., Bend, OR) was used to estimate internal body temperature within the lower gut. Skin temperature was measured at four sites using 0.3-mm diameter T-type thermocouples (Concept Engineering, Old Saybrook, CT) attached to the skin with surgical tape. Mean skin temperature was subsequently calculated using four skin temperatures weighted to the following regional proportions: upper back, 30%; chest, 30%; quadriceps, 20%; and back calf, 20%. Temperature data were collected using an HP Agilent data acquisition module (model 3497A) at a sampling rate of 15 s and simultaneously displayed and recorded in spreadsheet format on a personal computer with LabVIEW software (version 7.0; National Instruments).
The differences between young and older females were analyzed separately for heat loss responses during the exercise bouts and rest periods. The primary outcome was the measurements obtained from direct calorimetry (i.e., THL, EHL, dry heat loss, and changes in body heat content). Secondary outcomes included measurements of local sweat rate, SkBF, HR, core (i.e., visceral pill and rectal temperature) temperature and skin temperature. All primary and secondary outcomes were analyzed using repeated-measures ANOVA with the repeated factors of exercise time in minutes (levels: 0, 45 [Ex1], 75 [Ex2], 105 [Ex3], and 135 [Ex4]) and recovery time (0, 60 [R1], 90 [R2], 120 [R3], and 150 [R4]) and a nonrepeated factor of age (levels: young and older). The values for Ex1, Ex2, Ex3 and Ex4 were obtained at the end of each 15-min exercise period by averaging the last minute of exercise. Similarly, the values for R1, R2, and R3 were obtained by averaging the last minute of each 15-min recovery period, whereas the value for R4 is obtained at the 15-min mark of the final 60-min recovery period. Repeated-measures ANOVA (levels: Ex1, Ex2, Ex3, and Ex4 and R1, R2, R3, and R4) were conducted separately for young and older females for post hoc comparisons when a significant main effect of time was observed. Physical characteristics, baseline values for all variables, and cumulative change in body heat content were analyzed using independent sample t-tests. A sample size of 11 young and 13 older females was used in all primary outcome analyses. However, because of technical problems during the experimental session, a reduced sample size of 9 young and 12 older females was used for the analyses of rectal and visceral temperature. Of note, we were unable to directly access the participants to replace faulty rectal probes and/or telemetric pills as it was imperative that the calorimeter door remain closed during the entire experimental session to ensure accurate measurements of heat loss. For all comparisons, an alpha level of 0.05 was considered statistically significant; this was adjusted during multiple comparisons to limit the rate of type 1 error to 5% during Holm–Bonferroni adjustments. The Statistical Package for the Social Sciences (Version 18; SPSS Inc., Chicago, IL) was used for all analyzes.
With the exception of age (P < 0.001), there were no significant differences between groups for height (P = 0.513), weight (P = 0.540), body surface area (P = 0.582), percentage of body fat (P = 0.399), and V˙O2max (P = 0.343) (Table 1). There were also no baseline differences between age groups on any of the dependent variables except mean skin temperature (Tsk) (P = 0.006), which was significantly higher in young females at baseline.
Whole-Body Direct Calorimetry
The results obtained from calorimetry are presented in Table 2. The required evaporation to achieve heat balance (metabolic heat production ± dry heat exchange) (Ereq) and EHL during the experimental session are displayed in Figure 1. There were no differences in Ereq during exercise between young (Ex1: 321.6 ± 10.2; Ex2: 318.1 ± 9.0; Ex3: 316.2 ± 11.0; Ex4: 320.6 ± 11.0 W) and older females (Ex1: 318.6 ± 5.8; Ex2: 318.4 ± 4.6; Ex3: 323.1 ± 5.1; Ex4: 321.7 ± 4.6 W) (P = 0.885). THL significantly increased with successive exercise bouts (P < 0.001). THL was significantly greater during Ex2 compared with Ex1 in both young (P = 0.001) and older females (P < 0.001) as well as between Ex3 versus Ex2 in young females (P = 0.044) only. THL was significantly different between young and older females (P < 0.001). The younger females had greater THL after Ex1 (P < 0.001), Ex2 (P = 0.001), Ex3 (P < 0.001), and Ex4 (P = 0.034). When THL was separated into EHL and dry heat loss (DHL), only EHL significantly increased with each exercise period (P < 0.001). EHL significantly increased between Ex1 and Ex2 in young (P = 0.002) and older females (P < 0.001) and between Ex2 and Ex3 in older females (P = 0.033). EHL was also significantly different between age groups (P = 0.015) such that younger females had greater EHL after Ex1 (P = 0.001), Ex2 (P = 0.023), and Ex3 (P = 0.040), whereas EHL at the end of Ex4 was not significantly different between groups (P = 0.161). DHL did not change from one exercise session to the next (P = 0.149) and was not significantly different between age groups during exercise (P = 0.741).
Ereq during the recovery sessions was not significantly different between groups (P = 0.457). EHL, THL, and DHL were similar between recovery periods and did not significantly differ between groups.
Change in Body Heat Content
The changes in body heat content during the exercise and recovery periods are presented in Figure 2. The amount of heat stored in the body increased with repeated exercises (P < 0.001), whereby a significantly lower amount of heat was stored during Ex2 compared with Ex1 in young (75.4 ± 2.4 [Ex2] vs 114.0 ± 4.9 kJ [Ex1], P = 0.001) and older females (92.3 ± 3.6 [Ex2] vs 135.9 ± 5.2 kJ [Ex1], P = 0.001). No differences in body heat content between Ex2, Ex3, and Ex4 were observed in either group. The change in body heat content was also significantly different between groups (P < 0.001). The older females stored significantly more heat than the younger females at the end of Ex1 (P = 0.004), Ex2 (P = 0.001), and Ex3 (P = 0.017), whereas no significant differences were measured at the end of Ex4 (P = 0.547).
The change in body heat content was significantly different during successive recovery periods (P = 0.001). The older females had a reduced rate of heat storage during R2 compared with R1 (−30.0 ± 7.1 [R2] vs −9.7 ± 5.8 kJ [R1], P = 0.001). A similar trend was observed in young females (−43.0 ± 4.1 [R2] vs −27.5 ± 5.7 kJ [R1], P = 0.068). No differences in the change in body heat content were measured between R2, R3, and R4. Moreover, the changes in body heat content during the recovery periods were not significantly different between age groups (P = 0.126).
Cumulative change in body heat content
The older females had a significantly greater cumulative change in body heat content compared with younger females (269.7 ± 20.1 vs 166.1 ± 20.3 kJ, P = 0.001) after the 2-h intermittent exercise bout.
Results for rectal (Trec) and telemetric pill temperatures (Tpill) during the exercise and rest periods are presented in Table 3. The main effect for the increase in core temperature with successive exercise periods was significant for both Trec (P < 0.001) and Tpill (P < 0.001). The rise in Trec was greater at the end of Ex2 compared with Ex1 in young females (P < 0.001). In older females, the rise in Trec was greater during Ex2 versus Ex1 (P < 0.001), Ex3 versus Ex2 (P < 0.001), and Ex4 versus Ex3 (P = 0.027). Although the rise in Tpill was not found to be significantly different between successive exercises in young females, older females had a greater rise in Tpill at the end of Ex2 versus Ex1 (P < 0.001), Ex3 versus Ex2 (P = 0.037), and Ex4 versus Ex3 (P = 0.049). Trec and Tpill did not significantly differ between young and older females (P = 0.773 and P = 0.814, respectively). The change in Trec from baseline was not significantly different between groups at end of each exercise bout (P = 0.680). Conversely, the change in Tpill from baseline was significantly greater in older females at end of Ex3 (0.58°C ± 0.04°C vs 0.38°C ± 0.06°C, P = 0.023) and Ex4 (0.65°C ± 0.05°C vs 0.43°C ± 0.08°C, P = 0.037), whereas the difference in Tpill at the end of Ex2 was just short of statistical significance (0.51°C ± 0.04°C vs 0.36°C ± 0.06°C, P = 0.056).
The main effect for the increase in core temperature during the rest periods was significant for both Trec and Tpill (both P < 0.001). The rise in Trec was greater at the end of R2 compared with R1 in young females (P = 0.044). In older females, the rise in Trec was greater during R2 versus R1 (P < 0.001), R3 versus R2 (P = 0.002), and R4 versus R3 (P = 0.022). Tpill was only found to be significantly greater at the end of R2 compared with R1 in older females (P < 0.001). The main effect for age group was not significant for either measures of core temperature during the recovery periods (TrecP = 0.426 and TpillP = 0.449). The change in Trec from baseline, however, was significantly greater in older females compared with young females at the end of R3 (0.56°C ± 0.07°C vs 0.36°C ± 0.06°C, P = 0.028) and R4 (0.63°C ± 0.08°C vs 0.40°C ± 0.06°C, P = 0.024). In addition, the change in Tpill from baseline was significantly more elevated in older versus young females at the end of R2 (0.41°C ± 0.04°C vs 0.18°C ± 0.05°C, P = 0.005), R3 (0.44°C ± 0.04°C vs 0.24°C ± 0.06°C, P = 0.018), and R4 (0.46°C ± 0.05°C vs 0.24°C ± 0.08°C, P = 0.014). The difference in Tpill between older and young females at the end of R1 was just short of significance (0.23°C ± 0.02°C vs 0.15°C ± 0.03°C, P = 0.064).
Mean Skin Temperature
Mean skin temperatures throughout the experimental protocol are presented in Table 3. Tsk significantly increased with successive exercise bouts (P = 0.023). However, Tsk was only found to be significantly different at the end of Ex2 compared with Ex1 in older females (P = 0.018). The main effect for age group was also significant (P = 0.019); however, this was likely due to the significantly greater mean skin temperature in younger females at baseline. When Tsk was expressed as a change from baseline (Fig. 3C), the main effect for group was no longer significant (P = 0.537).
Tsk did not significantly change during the recovery periods (P = 0.263), but there was a tendency for mean skin temperature to be different between groups (P = 0.054). When expressed as a change from baseline values, the main effect for age group was no longer significant P = 0.213).
Local Heat Loss Responses and HR
Exercise (local sweat rate)
The results for local sweat rate, SkBF, and HR are presented in Table 3. Three older females were excluded from the analysis of local sweat rate due to failure of the ventilated sweat capsule to remain attached to the participant during the experiment. The data presented are therefore from 11 young females and 10 older females. Local sweat rate measured on the upper back significantly increased with successive exercise periods (P < 0.001). Local sweat rate was greater at the end of Ex2 compared with Ex1 in young (P = 0.004) and older females (P = 0.015) as well as at the end of Ex3 versus Ex2 in older females only (P = 0.041). However, local sweat rate was not significantly different between age groups (P = 0.451). The main effect for age group remained nonsignificant when local sweat rate was expressed as a change from baseline (P = 0.166).
Local sweat rate significantly increased with successive recovery periods (P < 0.001). Local sweat rate was only found to be significantly greater at the end of R2 compared with R1 in older females (P = 0.038). The main effect for age group was not significant (P = 0.708), and this remained true when expressed as a change from baseline (P = 0.831).
SkBF did not significantly increase between exercise periods (P = 0.134) and was not significantly different between groups (P = 0.898). The main effect for age group remained nonsignificant when SkBF was expressed as a change from baseline (P = 0.442).
SkBF did not significantly increase with sequential recovery bouts (P = 0.732) and was not different between age groups (P = 0.777). The change in SkBF from baseline during the rest periods was also not different between young and older females (P = 0.245).
The HR responses of young and older females were analyzed as a percentage of maximal HR (%HR) to account for differences between age groups in maximal HR achieved during the maximal exercise test. However, both absolute HR values and %HR are presented in Table 3. HR significantly increased with repeated exercise periods (P < 0.001). HR response was found to be significantly greater at the end of Ex2 versus Ex1 (P = 0.043) and Ex3 versus Ex2 (P = 0.036) in older females. HR response, however, did not significantly differ between groups (P = 0.733).
HR did not significantly differ between recovery periods (P = 0.283) and was not significantly different between young and older females (P = 0.387).
The main findings of the present study confirm our hypothesis that older females have a reduced rate of whole-body heat loss during short duration intermittent exercise in the heat compared with younger females matched for fitness, body composition, and body surface area. At the end of the 2-h intermittent exercise, the older females had a greater cumulative change in body heat content, which was paralleled by a greater change in core temperature. This was a consequence of a marked reduction in their ability to dissipate heat only during exercise given that both the young and older females showed a similar attenuated rate of whole-body heat loss during the postexercise recovery periods. The observed lower whole-body heat dissipation during exercise was not paralleled by lower local heat loss (sweating and SkBF).
Our knowledge of how aging affects thermoregulatory responses is largely based on studies that compared young and older males (13,14,30,32,33,36,37). Recent evidence suggests that sex may be an important modulator of human temperature regulation during exercise in the heat (9,11,12). Recently, Gagnon and Kenny (12) showed that young females had a reduced capacity to dissipate heat, as evidenced by a marked attenuation in whole-body sudomotor activity, compared with males during exercise in the heat performed at a fixed rate of metabolic heat production exceeding 250 W·m−2. The lower sudomotor activity observed in females was subsequently ascribed to a peripheral modulation at the level of the sweat gland rather than centrally through potential differences in neural activity (8). The extent to which aging may alter this pattern of response is unclear. Some insight may be gleaned by an earlier study by Shoenfeld et al. (33). They reported lower mean sweat rates per body surface area between males and females ranging in age from 18 to 63 yr during a 10-min passive exposure to extreme heat (80°C–90°C). The males had a mean whole-body sweat rate of 287 ± 117 g·m−2, whereas in females, it was 212 ± 89 g·m−2. Although sex comparisons were not performed by age groups, the reported mean sweat rate in older females (167 ± 94 g·m−2) was lower compared with the rates recorded in older males (267 ± 98 g·m−2). Nonetheless, given the short and extreme nature of the passive heat stress, these findings should be interpreted with caution. Ultimately, it remains unclear how responses in older males and females would differ during a thermal challenge associated with exercise in the heat. However, when combined with the findings by Gagnon et al. (8,12), the evidence suggest that age-related differences in thermoregulatory function should be examined separately in males and females.
To date, very few published studies have examined age-related changes in the body’s ability to dissipate heat in females during exercise in the heat. One study by Drinkwater and Horvath (6) examined the effects of chronological age (12–68 yr) on heat tolerance during exercise in the heat by compiling data from four separate studies. On the basis of results from regression analyses, they reported that older females tended to have reduced heat tolerance. Given that no preplanned comparison was performed between a subgroup of young versus older adult females, it is not possible to determine the extent of the age-related impairments in thermoregulatory control, if any. To the best of our knowledge, the study by Anderson and Kenney (1) is the only study to compare thermal responses between young (25 ± 4 yr) and older females (56 ± 4 yr) while exercising at the same rate of heat production. The older females had a more pronounced rise in rectal temperature and greater heat storage than the younger females after 2 h of treadmill walking at 35%–40% V˙O2max in a hot dry environment (48°C, 10% RH). In parallel, they showed that older females had an attenuated sweat production as measured by lower local sweat rate at 30 min of exercise, which was maintained for the duration of the 2-h exercise protocol. Taken together, their observations demonstrated that older females had a reduced sudomotor capacity relative to their younger female counterparts, which was attributed mainly to a lower sweat output per gland. When the maximal evaporation possible within a given environment does not limit an individual’s ability to achieve heat balance, and therefore a stable core temperature, the level of sudomotor activity achieved during exercise is driven by the required evaporation for heat balance (4,17). Thus, given that the older females showed a marked reduction in local sweat rate for the duration of exercise, which was paralleled by a markedly greater rise in core temperature, indicates that the combined metabolic and environmental heat load exceeded the physiological capacity of the older females to dissipate heat. Given that the authors did not report data before what was recorded after the first 30 min of exercise (when the rate of whole-body heat loss is still increasing), it is unclear if these age-related differences in heat loss are only evidenced at and beyond 30 min of exercise when steady-state levels of whole-body sweat production are typically observed (27).
As seen in Figure 1, the rate of metabolic heat production increases immediately at the start of exercise and is not initially offset by an increase in the rate of whole-body heat loss, thus giving rise to a pronounced increase in body heat content during the early stages of exercise (38). Whole-body EHL increases in an exponential fashion during the early stages of exercise (i.e., non–steady-state period), with a time constant of approximately 12 min and reaching steady state after approximately 30 min of continuous exercise under compensable heat stress conditions (27). We show a marked attenuation in whole-body sudomotor activity during the non–steady-state period in the older females relative to their younger counterparts occurring as early as 10 min after the onset of exercise. This pattern of response was consistently observed in Ex1, Ex2, and Ex3 with rates of whole-body EHL reduced by 17%, 9%, and 9%, respectively, in older compared with younger females. This was paralleled by a greater change in body heat content (i.e., Ex1, 16%; Ex2, 18%; and Ex3, 11%). It is important to note that while there was no statistically significant difference between age groups measured in the final exercise bout, the difference in the rate of whole-body EHL was comparable between Ex3 and Ex4 for each group, albeit the separation between groups was marginally reduced (i.e., Ex3 vs Ex4; young, 273.8 ± 11.3 vs 272.4 ± 11.0 W; older, 248.9 ± 4.7 vs 254.2 ± 7.5 W). The greater heat storage measured in older females during the exercise periods resulted in a greater cumulative increase in body heat content during the 2-h intermittent exercise. In keeping with the progressively greater thermal drive, we observed a progressive albeit marginally higher rate of whole-body heat loss measured at the end of each successive 15-min exercise bout.
It is noteworthy that the amount of heat stored after the first exercise bout was reduced to a similar extent in the young (34%) and older (32%) females relative to the second exercise bout. This greater rate of increase in whole-body heat loss during successive exercise bouts is consistent with previous reports demonstrating that the thermal inertia (i.e., the time taken to balance the differential rates of heat production and heat loss) is reduced when core temperature is elevated and the body is already warm and much of the heat already stored during the first exercise/recovery cycle remains (10,23,24). As a result of the enhanced rate of local and whole-body heat loss, the net amount of heat gained during intermittent exercise is significantly reduced in the successive exercise bouts (23). We show that this response, known as the priming effect (10), occurs despite any apparent age-related impairment in thermoregulatory function. As in the case of exercise where the greater thermal drive with successive exercise enhanced the rate of heat loss, a greater decrease in body heat content would have been expected with each successive recovery period. We observed a marked attenuation of whole-body heat loss after the first exercise bout such that only 25% and 7% of the total heat gained during exercise was dissipated during the first 15-min recovery period in the young and older females, respectively. Noteworthy, a greater decrease in body heat content was measured during the second recovery period compared with the first recovery in the older females as shown in Figure 2. Nevertheless, the change in body heat content during the subsequent recovery bouts was not different despite our observation that the cumulative heat storage was greater at the end of each successive exercise bout (Fig. 2). In parallel, we measured a rapid decay in whole-body EHL at the cessation of each exercise bout of similar magnitude in both the young and older females. These observations add to the growing body of evidence that factors of nonthermal origin have an overriding influence on heat loss responses during the postexercise period irrespective of the changes in thermal status of the individual (23–27) and, as evidenced by our study findings, the level of age-related impairment in thermoregulatory function. For a more comprehensive review of the current state of knowledge pertaining to the effects of nonthermal influences on postexercise thermoregulation, the reader is referred to a recent review on this topic (26).
In addition to measuring whole-body heat loss responses and heat storage, we also measured local heat loss responses (i.e., local sweating and SkBF) as well as core and skin temperature responses between young and older females. Although reduced whole-body EHL in older females was measured by whole-body calorimetry, this was not paralleled by similar differences in local heat loss responses. In light of our observations of marked reductions in whole-body heat loss, these results may simply reflect regional differences in local sweat rate and SkBF, consistent with the results reported in previous studies (15,16). Segmental differences in vasomotor and sudomotor function have been well documented during rest and exercise (3,29). These differences are more pronounced with greater levels of hyperthermia (29) and can be exacerbated by the high degree of heterogeneity in local sweating and SkBF responses with aging (15,16) such that these measurements may not accurately reflect changes in whole-body heat loss capacity in older adults. On the other hand, the progressively greater change in body heat content with successive exercises eventually resulted in a significantly greater change in rectal and visceral pill temperature in older females. Differences in the increase in rectal temperature between age groups became apparent by the end of the third recovery period, whereas differences in visceral temperature were seen at the end of the second recovery period and remained significantly greater until the end of the experimental session. As depicted in Figure 3, for those subjects with both measures of body heat content and core temperature (young, n = 9; older, n = 12), the greater cumulative change in body heat content in older females was paralleled by a greater change in both rectal and visceral core temperature at the end of the 2-h experiment compared with young females. Specifically, the change in body heat content measured by calorimetry and the change in rectal temperature were 33% and 38% greater in older females compared with young females. Similarly, the change in both body heat content and visceral temperature were 30% and 48% greater, respectively, in older versus young females. Moreover, as a consequence of a greater increase in body heat content during exercise, both rectal and visceral temperature increased progressively from Ex1 to Ex2, Ex2 to Ex3, and Ex3 to Ex4 in older females. This was paralleled by a progressive elevation in rectal temperature from R1 to R2, R2 to R3, and R3 to R4. In contrast, in young females, rectal temperature was only significantly more elevated at the end of Ex2 compared with Ex1 and R2 compared with R1. No significant differences in core temperature were measured between Ex2, Ex3, and Ex4 as well as R2, R3, and R4. It is likely that with longer exercise bouts, greater series of exercise/recovery cycles, and/or greater heat load (metabolic and/or environment), the differences in core temperature between young and older females would have been even more pronounced.
The older females who volunteered for this study were probably more active and physically fit than the average aging female. As such, thermoregulatory capacity may be further reduced in older females with lower cardiorespiratory fitness or chronic medical conditions (28). We did not attempt in the present study to control for menopause or menstrual cycle. However, we looked at the cumulative change in body heat content between the eight older females that were postmenopausal and the five older females that were perimenopausal and found comparable results. In fact, the overall change in body heat content was 294 ± 26 kJ in perimenopausal women and 258 ± 18 kJ in postmenopausal women. This is in sharp contrast to younger females who had a change in body heat content of 166 ± 20 kJ. The effects of circulating estrogen and progesterone levels are reported to affect baseline core temperatures (2,35). There were no significant differences in baseline Trec (37.20°C ± 0.05°C [Y] and 37.13°C ± 0.12°C [O]) or Tpill (37.36°C ± 0.05°C [Y] and 37.23°C ± 0.07°C [O]) between our age groups. In addition, previous studies have shown that menstrual cycle does not play a major role in a women’s response to exercise in the heat (39,40). Menopause on the other hand is a natural occurrence with aging; thus, it seems irrelevant to control for this when studying the effects of aging on thermoregulatory responses in aging females. It remains evident that older females, postmenopausal or not, have a reduced capacity to dissipate heat relative to younger females. On a different note, it has been suggested that differences in hydration state could account for the differences in sweating capacity and, consequently, EHL in older versus young females (22). We encouraged our participants to hydrate before the experimental session, and no fluid replacement was provided during the session. Urine-specific gravity was not significantly different between groups at baseline (Y, 1.016 ± 0.002; O, 1.012 ± 0.002; P = 0.181) or at the end of the experiment (Y, 1.018 ± 0.002; O, 1.019 ± 0.002; P = 0.767). The percent change in plasma volume was not significantly different between groups (Y, −2.7 ± 0.7%; O, −3.6 ± 0.9%; P = 0.414). Therefore, the observed differences in EHL appear unrelated to differences in hydration state between groups.
Given the intermittent nature of many daily and work-related activities, it was important to determine whether aging females experienced greater thermal strain during short bouts of exercise. Anderson and Kenney (1) showed a marked difference in heat dissipation during prolonged and continuous exercise in a very hot ambient condition (48°C). Both the exercise and ambient conditions used in their study, however, are not representative of typical environmental conditions or activity patterns consistent with everyday life. On the other hand, the present study demonstrated that age-related differences in sudomotor activity were evident as early as 10 min after the start of exercise during moderate heat stress (i.e., ambient temperature of 35°C). As demonstrated in the present study, age-related impairments in heat dissipation during short exercise/rest cycles can result in a substantially greater increase in body heat content and consequently, a greater change in core temperature. This is exacerbated by the fact that older females appear to have a similar attenuation in local and whole-body heat loss shortly after the end of exercise. Taken together, our findings support the notion that older females may be more susceptible to heat-related injury not only during prolonged exercise in the heat as demonstrated in previous studies, but during short intermittent bouts of exercise as well.
In conclusion, whole-body EHL was reduced in older females during the first, second, and third exercise bouts compared with younger females, which led to greater changes in body heat content during exercise. Because a similar attenuation in local and whole-body heat loss during the postexercise periods was observed in both age groups, the greater cumulative change in body heat content measured in older females, which was paralleled by a greater change in body core temperature, was due to reduced sudomotor activity evident in the early stages of exercise. Consequently, older females maybe more susceptible to heat-related injury while performing work or exercise of short duration in the heat compared with younger females.
This project was funded by the Workplace Safety and Insurance Board of Ontario (grant no. 10001) and a Natural Sciences and Engineering Research Council Discovery Grant (RGPIN-298159-2009) (grants held by Dr. G. Kenny).
The authors are indebted to the study participants and to Mr. S. Nagaraja, Ms. N. Baala, Ms. J. Barrera, Mr. M. Poirier, and the entire Human and Environmental Physiology Research Unit team for their contribution to the success of this project.
The authors declare no conflicts of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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