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Older Adults with Type 2 Diabetes Store More Heat during Exercise

KENNY, GLEN P.1; STAPLETON, JILL M.1; YARDLEY, JANE E.1; BOULAY, PIERRE2; SIGAL, RONALD J.3

Medicine & Science in Sports & Exercise: October 2013 - Volume 45 - Issue 10 - p 1906–1914
doi: 10.1249/MSS.0b013e3182940836
BASIC SCIENCES
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Introduction It is unknown if diabetes-related reductions in local skin blood flow (SkBF) and sweating (LSR) measured during passive heat stress translate into greater heat storage during exercise in the heat in individuals with type 2 diabetes (T2D) compared with nondiabetic control (CON) subjects.

Purpose This study aimed to examine the effects of T2D on whole-body heat exchange during exercise in the heat.

Methods Ten adults (6 males and 4 females) with T2D and 10 adults (6 males and 4 females) without diabetes matched for age, sex, body surface area, and body surface area and aerobic fitness cycled continuously for 60 min at a fixed rate of metabolic heat production (∼370 W) in a whole-body direct calorimeter (30°C and 20% relative humidity). Upper back LSR, forearm SkBF, rectal temperature, and heart rate were measured continuously. Whole-body heat loss and changes in body heat content (ΔHb) were determined using simultaneous direct whole-body and indirect calorimetry.

Results Whole-body heat loss was significantly attenuated from 15 min throughout the remaining exercise with the differences becoming more pronounced over time for T2D relative to CON (P = 0.004). This resulted in a significantly greater ΔHb in T2D (367 ± 35; CON, 238 ± 25 kJ, P = 0.002). No differences were measured during recovery (T2D, −79 ± 23; CON, −132 ± 23 kJ, P = 0.083). By the end of the 60-min recovery, the T2D group lost only 21% (79 kJ) of the total heat gained during exercise, whereas their nondiabetic counterparts lost in excess of 55% (131 kJ). No difference were observed in LSR, SkBF, rectal temperature or heart rate during exercise. Similarly, no differences were measured during recovery with the exception that heart rate was elevated in the T2D group relative to CON (p=0.004).

Conclusion Older adults with T2D have a reduced capacity to dissipate heat during exercise, resulting in a greater heat storage and therefore level of thermal strain.

1Human and Environmental Physiology Research Unit, University of Ottawa, Ottawa, CANADA; 2Faculty of Physical Education and Sports, University of Sherbrooke, Sherbrooke, QC, CANADA; and 3Departments of Medicine, Cardiac Sciences and Community Health Sciences, Faculties of Medicine and Kinesiology, University of Calgary, Calgary, AB, CANADA

Address for correspondence: Glen P. Kenny, Ph.D., Human and Environmental Physiology Research Unit, University of Ottawa, Room 367, Montpetit Hall, Ottawa, Ontario K1N 6N5, Canada; E-mail: gkenny@uottawa.ca.

Submitted for publication November 2012.

Submitted for publication March 2013.

Heat wave mortality patterns have shown that older adults are at significantly higher risk for heat illness and/or injury compared with the general population (18). However, individuals with type 2 diabetes mellitus (T2D) are at an even greater risk of suffering a heat-related illness and/or injury compared with nondiabetic individuals of similar age (6,33,34). Epidemiological data show greater rates of hospitalization and/or death for individuals with T2D during heat waves (18,33). Although these findings would indicate that heat tolerance may be reduced to a greater extent in older adults with T2D, the extent that T2D affects the body’s ability to dissipate heat remains unclear.

T2D can have a profound influence on physiological function leading to metabolic, cardiovascular and neurologic disturbances. In recent years, T2D has also been identified as a modulator of human temperature regulation during heat stress, adding thermoregulation to the list of physiological systems affected by the disease. Studies demonstrate that microvascular reactivity is reduced in individuals with diabetes. This is evidenced by a decrease in local sensory nerve vasodilation during local warming (3,39,41) and an altered control of active cutaneous vasodilation during whole-body heating (40,44). The few existing studies assessing sweat rates in T2D individuals have primarily studied sudomotor (sweating) function to test the severity of autonomic neuropathy (7,19) rather than thermoregulatory function. These reports reveal that otherwise healthy individuals with T2D have an attenuated sweat production during different thermal challenges (7,30) (i.e., passive heating, fatiguing isometric hand-grip exercise). This reduction is especially pronounced in the distal regions (7,30). The attenuation in the local heat loss responses of skin blood flow (SkBF) and sweating have been linked to diabetes-related peripheral neuropathy and autonomic dysfunction as well as reduced nitric oxide production/availability and high concentrations of free radicals in blood (9,13,29).

Despite our growing knowledge of the effects of T2D on thermoregulatory function, it remains unclear if dysfunction in the control of heat loss responses of SkBF and sweating can lead to a greater risk of dangerous hyperthermia in individuals with T2D during exercise in the heat. When combined, these diabetes-related impairments in vasomotor and sudomotor function can severely affect even the most basic activities of daily living in individuals with T2D (29). Under circumstances where impairments in heat loss responses prevent the attainment of a sufficient rate of heat loss to offset an increase in heat production (exercise) and/or environmental heat load (elevated ambient temperature and/or humidity), core temperature can continue to increase to dangerously high levels. This can result in major heat-related disorders such as heat cramps, heat exhaustion and heatstroke, each involving varying degrees of thermoregulatory failure.

The following study was conducted to evaluate how T2D affects the body’s physiological capacity to dissipate heat during exercise in a warm environment. To achieve this objective, we examined local and whole-body heat loss during and after 60 min of dynamic exercise performed at a moderate fixed rate of heat production of ∼370 W (representing an equivalent exercise intensity of ∼60% of the participants’ maximal aerobic capacity) under conditions that permit full evaporation (air temperature, 30°C; relative humidity [RH], 20%) in relatively healthy older habitually active adults with and without T2D. This exercise condition was used to ensure that, in combination with the elevated ambient temperature conditions, the exercise would elicit a sufficiently elevated thermal load to challenge the individual’s ability to achieve heat balance without compromising the participant’s health and safety. It was hypothesized that individuals with T2D, matched for age, sex, body surface area, body composition, and aerobic fitness with their healthy counterparts, would demonstrate a lower whole-body heat loss response compared with nondiabetic controls, resulting in greater heat storage during exercise in a warm environment.

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METHODS

Participants

The experimental protocol was approved by the University of Ottawa Health Sciences and Science Research Ethics Board, in accordance with the Declaration of Helsinki. Written informed consent was obtained from all volunteers before their participation in the study.

Ten adults (6 males and 4 females) with T2D and 10 adults (6 males and 4 females) without diabetes volunteered to participate in the study. Participants were matched for age, sex, body composition, body surface area, and aerobic fitness and were all habitually active (no more than 2 d of continuous exercise of less than 20 min in duration). Mean ± SE characteristics of the participants are presented in Table 1. All participants were healthy, weight stable, normotensive, and free of diabetes-related complications (i.e., renal disease, severe peripheral neuropathy, proliferative retinopathy, and unstable cardiac or pulmonary disease) or musculoskeletal complications (i.e., injury, arthritis, etc.). T2D participants had been diagnosed for at least 5 yr and had hemoglobin (Hb) A1c levels lower than 9.9%. All female participants were postmenopausal.

TABLE 1

TABLE 1

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Experimental design

Participants volunteered for one preliminary and one experimental sessions. During the preliminary session, training history, body height, mass, and density as well as maximum oxygen uptake were determined. Training history was assessed by having the participants quantify their physical activity levels using the quantitative (3 months) and 7-d physical activity recall questionnaires proposed by Kohl et al. (21). Body height was determined using a stadiometer (model 2391; Detecto, Webb City, MO), whereas body mass was measured using a digital high-performance weighing terminal (model CBU150X; Mettler Toledo Inc., Mississauga, Ontario, Canada). Body surface area was subsequently calculated from the measurements of body height and mass (4). Body density was measured using the hydrostatic weighing technique and used to calculate body fat percentage (38). Maximum oxygen uptake was determined by measuring expired oxygen (O2) and carbon dioxide (CO2) concentrations (AMETEK model S-3A/1 and CD 3A; Applied Electrochemistry, Pittsburgh, PA) during a progressive incremental stress test performed to volitional fatigue on a semirecumbent cycle ergometer while participants were monitored by electrocardiogram.

All experimental trials were performed at the same time of day for individuals with T2D and their matched controls. 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. Upon arrival at the laboratory, the participants changed into shorts, sandals, and a sports bra for female participants. They subsequently sat quietly for a 60-min instrumentation period at an ambient room temperature of 24°C. After instrumentation, the participant entered a whole-body calorimeter regulated to an ambient air temperature of 30°C and 20% RH with air movement around the subject limited to that provided for in the design of the Snellen whole-body calorimeter (32). Each participant, seated in the upright position, rested for a 30-min habituation period. Subsequently, the participant performed 60 min of continuous upright seated cycling exercise followed by a 60-min recovery period. The exercise period was performed at a fixed rate of metabolic heat production equal to ∼370 W, representative of an average work output of 58 W and equivalent to ∼60% of the participant’s predetermined V˙O2max. This work intensity was chosen based on previous work evaluating the use of aerobic exercise in the management of T2D. This moderate work intensity was previously shown to be performed safely during a 45-min exercise bout in previously sedentary individuals with T2D undergoing a 6-month exercise training program (37). During the final 30 min of the recovery period, local heating of the anterior forearm was performed to determine maximum SkBF (see details in the next section). At the end of the local heating period, the participants exited the calorimeter.

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Measurements

The modified Snellen direct air calorimeter (32) 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). 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 (5) (in watts) was calculated from the calorimetry data using the following equation:

where mass flow is the rate of air mass (kilograms of air per second), (humidityout − humidityin) is the difference in absolute humidity (grams of water per kilogram of air) between the in and out flows of the calorimeter, and 2426 is the latent heat of vaporization of sweat (J·g−1 of sweat). The rate of dry heat loss (DHL) from radiation, convection, and conduction (W) was calculated from calorimetry data using the following equation:

where mass flow is the rate of air mass (kilograms of air per second), (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·°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 O2 and CO2 concentrations using electrochemical gas analyzers (AMETEK models S-3A/1 and CD 3A, respectively; Applied Electrochemistry) located outside the calorimeter chamber. Expired air was recycled back into the calorimeter chamber to account for respiratory dry and evaporative heat loss. 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 contentHb, in kilojoules).

The ventilated capsule technique was used for the purpose of measuring local sudomotor activity. Sweat production on the upper back was measured from 3.8 cm2 plastic capsules attached to the skin with adhesive rings and topical skin glue (Collodion HV; Mavidon Medical Products, 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). Local sweat rate was calculated using 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.

SkBF was estimated using laser Doppler velocimetry (PeriFlux System 5000; Perimed AB, Stockholm, Sweden). Before the start of the experimental trial, the laser Doppler flow probe (PR 401 Angled Probe; Perimed AB) was affixed with an adhesive ring to the anterior forearm in a site without superficial veins that demonstrated pulsatile activity. The probe was not moved from its location throughout the experimental trial. To determine maximum SkBF, a local heating period to 44°C was performed 30 min into recovery. Local heating was continued until maximal skin vasodilation was achieved.

A general purpose thermocouple temperature probe (Mon-a-therm General Purpose Temperature Probe; Mallinckrodt Medical, St. Louis, MO) was self-inserted 12 cm past the anal sphincter to measure rectal temperature. Skin temperature was measured at four different sites and used to calculate a mean skin temperature weighted to the following regional proportions: upper trapezius, 30%; chest, 30%; quadriceps, 20%; and back calf, 20% (31). All temperature data (sampling rate of 15 s) were collected using an HP Agilent data acquisition module (model 3497A) and a personal computer. Data were simultaneously recorded and displayed in a spreadsheet using LabVIEW software V.7.0 (National Instruments).

Heart rate was monitored, recorded continuously, and stored using a Polar coded transmitter, Polar Advantage interface, and Polar Precision Performance software (Polar Electro Oy, Kempele, Finland).

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Data analysis

For all variables, minute averages were performed to carry out the statistical analyses. To account for the relative influence of core and skin temperatures on the activation of heat loss responses (12,26,27), mean body temperature was calculated as: 0.8 × rectal temperature + 0.2 × mean skin temperature (35). The onset threshold and the thermosensitivity of local (sweat rate) and whole-body (evaporative heat loss) sudomotor activity during each exercise period were determined using the linear portion of each response plotted against mean body temperature and analyzed using the segmented regression analysis proposed by Cheuvront et al. (2).

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Statistical analysis

All dependent variables were compared between groups (T2D vs control [CON]) and examined using a two-way ANOVA with nonrepeated measures of groups and repeated measures of time (30, 45, and 60 min of exercise and recovery separately). Paired t-tests were used for single comparisons between groups and for post hoc comparisons upon finding significant main effects. The level of significance for all analyses was set at a level of P ≤ 0.05. Statistical analyses were performed using commercially available statistical software (GraphPad Prism 5.0; GraphPad Software, La Jolla, CA). All values are reported as mean ± SE.

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RESULTS

Participant Characteristics

With the intention of matching our participants as closely as possible on all physical characteristics, there were no differences between groups in age (P = 0.452), height (P = 0.925), body mass (P = 0.937), body surface area (P = 0.689), and maximum oxygen consumption (both in absolute values [P = 0.539] and relative to body mass [P = 0.241]). Subject characteristics are available in Table 1.

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Baseline Resting

Whole-body heat exchange

The rate of metabolic heat production during the 30-min baseline period did not differ between T2D and CON (T2D: 116 ± 8 vs CON: 109 ± 6 W, P = 0.465). Likewise, the rates of total (T2D: 90 ± 10 vs CON: 94 ± 10 W, P = 0.781; Fig. 1A), evaporative (T2D: 59 ± 8 vs CON: 61 ± 11 W, P = 0.868; Fig. 1B), and dry (T2D: 31 ± 5 vs CON: 33 ± 5 W, P = 0.792; Fig. 1B) heat loss was similar between groups before exercise. As such, no differences were observed in the change in body heat content during the 30-min period before the start of exercise (T2D: 58 ± 11 vs CON: 50 ± 7 kJ, P = 0.623; Fig. 2).

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

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Core temperature, local heat loss, and heart rate responses

Rectal temperature was similar between T2D and CON before the start of exercise (P = 0.943) as was mean skin temperature (P = 0.505). Values are presented in Table 2. Local sweat rate did not differ between groups before exercise (T2D: 0.14 ± 0.04 vs CON: 0.15 ± 0.06 mg·min−1·cm−2, P = 0.937). Similarly, local SkBF was comparable between groups at rest (T2D: 23.59 ± 3.31% vs CON: 25.26 ± 3.06%, P = 0.613). Resting heart rate was greater for T2D compared with CON (P = 0.007). Values are presented in Table 2.

TABLE 2

TABLE 2

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Exercise

Whole-body heat exchange

The rates of metabolic heat production and THL (evaporative + dry) are presented in Figure 1A. By design, the rate of metabolic heat production did not differ between groups during the 60-min exercise bout (end exercise values, T2D: 368 ± 24 vs CON: 368 ± 21 W, P = 0.970). There was a main effect of group on the rate of THL during the 60-min exercise period (P = 0.004). THL was greater from CON compared with T2D from 15 min throughout the remainder of exercise. As a result, the change in body heat content during exercise (Fig. 2) was significantly greater for T2D compared with CON (T2D: 367 ± 35 vs CON: 238 ± 25 kJ, P = 0.002). Similar to the rate of THL, there was a main effect of group on the rate of evaporative heat loss (P = 0.043), but not dry heat loss (P = 0.431) (Fig. 1B). Evaporative heat loss was greater for CON compared with T2D from 15 min to the remainder of the 60-min exercise bout. The thermosensitivity of evaporative heat loss was also significantly greater for the control group (T2D: 3270 ± 38 vs 453 ± 38 W·°C−1, P = 0.018), indicating that the individuals with T2D had a slower rate of evaporative heat loss response to increases in mean body temperature. No differences were observed in the onset threshold (P = 0.794).

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Core temperature, local heat loss, and heart rate responses

End exercise values for rectal and mean skin temperature are presented in Table 2. There was no main effect of group on rectal (P = 0.388) or mean skin temperature (P = 0.445) during exercise. There was no main effect of group on local sweat rate during exercise (P = 0.421; Fig. 3A). The mean body temperature onset threshold for local sweat rate was not significantly different between groups (T2D: 36.18 ± 0.13°C vs CON: 36.26 ± 0.12°C, P = 0.588). Likewise, the thermosensitivity of the sweating response on the back was also comparable between groups (0.90 ± 0.14 vs 1.19 ± 0.22 mg·min−1·cm−2·°C−1, P = 0.169). Local SkBF is expressed as percent of maximum. There was no main effect of group on local SkBF during exercise (P = 0.683; Fig. 3B). The onset threshold for local SkBF was not different between groups (T2D: 36.32 ± 0.13°C vs CON: 36.8 ± 0.10°C, P = 0.787). Finally, there was no difference in the thermosensitivity of SkBF on the forearm between groups (T2D: 49.35 ± 11.18% vs CON: 73.20 ± 16.83% of max·°C−1, P = 0.301). During exercise, there was no main effect of group on heart rate (P = 0.179). Values are presented in Table 2.

FIGURE 3

FIGURE 3

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Recovery

Whole-body heat exchange

There was no main effect of group on the rate of THL during the recovery period (P = 0.975). Likewise, the change in body heat content during recovery was similar for T2D compared with CON (T2D: −79 ± 23 vs CON: −132 ± 23 kJ, P = 0.083). Therefore, because of the greater change in body heat content during exercise, the residual amount of heat stored after the recovery period was significantly greater for T2D compared with CON (T2D: 288 ± 46 vs CON: 107 ± 36 kJ, P = 0.010). When breaking down the rate of THL into its components (evaporative + dry), the rates of evaporative (P = 0.527) and dry (P = 0.442) heat loss were not different between groups for the 60-min recovery period.

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Core temperature, local heat loss, and heart rate responses

There were no significant differences in the pattern of response between groups for rectal temperature during recovery (P = 0.391). In addition, mean skin temperature was comparable between groups during the recovery period (P = 0.622). There were no differences between groups for local sweat rate (P = 0.315) or SkBF (P = 0.861) during the 60-min recovery period. There was a main effect of group on heart rate during recovery (P = 0.004). The T2D group had an elevated heart rate compared with CON for the entire 60-min recovery period (Table 2).

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DISCUSSION

Our study demonstrates for the first time that older adults with T2D have reduced capacity to dissipate heat, and they therefore store progressively more heat during exercise in a warm environment. We showed that the cumulative change in body heat content increased over time such that the amount of heat stored was significantly greater from 15 min of exercise onward in the older adults with T2D relative to their nondiabetic counterparts. In contrast to our study hypothesis, the reduction in whole-body heat loss (dry + evaporative) was not paralleled by attenuations in local sweating or SkBF. Further, despite a greater rate of heat storage measured in the individuals with T2D, no differences in core temperature were observed between groups.

Chronic medical conditions such as T2D are thought to cause changes in the body’s normal response to heat as evidenced by the fact that T2D is associated with higher rates of heat illness and death during heat waves when compared with the general population (18). Although these findings would indicate that heat tolerance may be reduced in individuals with T2D, the extent that T2D affects the body’s ability to dissipate heat remains unclear (30,41,44). All but one study (42) has demonstrated that the ability of skin blood vessels to dilate in response to passive heating and/or pharmacological stimuli may be impaired (3,39–41,44) in T2D individuals relative to age-matched controls. However, the level of impairment may be influenced by the level of physical activity (3). Although the impairments in skin vascular responsiveness have been linked to reduced bioavailability of nitric oxide and high concentrations of free radicals in the blood (9,13,29), a recent report suggests that the influence of nitric oxide in the regulation of skin vasodilation response may vary in individuals with diabetes (40). The limited studies assessing sweat production in T2D individuals have primarily studied sudomotor function to test the severity of autonomic neuropathy (7,19) rather than thermoregulatory function. To the best of our knowledge, the study by Petrofsky et al. (30) is the only study to show a reduction in sweat rate during 1) a prolonged passive heat exposure (i.e., ambient air temperature of 39°C) and 2) isometric exercise (two bouts at 40% of maximal voluntary contraction, separated by 5 min of rest) in the heat (32°C) in individuals with type 1 and T2D (HbA1c: 7.7%, ∼40 yr of age). A greater attenuation was observed at higher ambient air temperatures (i.e., 32°C vs 39°C), but sweat rate was more pronounced in the forehead for the individuals with diabetes as compared with controls for all conditions.

In light of the fact that none of the aforementioned studies performed concurrent measurement of changes in core temperature, it was not possible to determine whether diabetes-related impairments and/or abnormalities in skin perfusion (i.e., vascular responsiveness, changes in structure and quality of blood vessels, etc.) and sweating result in reductions in whole-body heat loss and therefore greater levels of body heat storage. To the best of our knowledge, our study is the first to examine the possible effects of diabetes on whole-body heat loss during either rest or exercise. In the present study, participants were only exposed to a mild ambient heat stress (i.e., 30°C) during baseline resting. As expected, we did not observe any differences in local and whole-body heat loss responses during the 30-min preexercise rest period. This is consistent with the observations by Petrofsky et al. (30), who reported that the reduction in sweat production is more pronounced with increases in environmental heat load. However, given previous observations of attenuated local heat loss responses of SkBF and sweating during whole-body heating (40,44), we predicted comparable if not greater reductions in local heat loss responses during exercise (participants exercised at a fixed rate of heat production of ∼370 W) in the heat. Moreover, we surmised that the decrement in local SkBF and sweating would translate into a marked reduction in whole-body (dry + evaporative) heat loss. We observed a significant reduction in whole-body heat loss in the individuals with T2D after the first 15 min of exercise that persisted for the duration of exercise. This attenuation was the result of a marked reduction in whole-body sudomotor activity (evaporative heat loss). Although we observed a similar pattern of response in local sweating, the differences between groups were not significant. Similarly, no differences in local forearm SkBF were observed.

To further examine whether group differences in whole-body sudomotor activity are mediated peripherally and/or centrally, we also examined the onset threshold and thermosensitivity. Although both variables can represent a central and/or peripheral modulation of temperature regulation (11), it is thought that a parallel shift in the onset threshold of all effector responses must occur to be representative of a central modulation (10). As such, changes in the thermosensitivity of an effector response, without parallel changes in the onset threshold, likely imply a peripheral modulation. On this basis, the onset threshold has typically been used to represent a central modification of temperature regulation, whereas the thermosensitivity has been used to represent peripheral adaptations in effector responses (27,28). In the current study, the lower whole-body sudomotor activity in the participants with T2D was paralleled by a lower thermosensitivity of response, with no differences in the onset threshold. The decrease in whole-body sudomotor activity can reflect altered function at any point in the activation of the sweating response manifested as an altered thermoafferent information from peripheral thermoreceptors, an altered neural integration of thermoafferent activity, altered thermoefferent neural activity, and/or an altered thermoeffector response for a given level of thermoefferent activity (22). Taken together, the observed differences in sudomotor thermosensitivity and lack of differences in the onset threshold, combined with the lack of differences in SkBF, suggest a peripheral modulation of the thermoeffector organ. A peripheral modulation of the thermoeffector organ could stem from 1) damage to or changes in physical properties of the sweat gland itself that may occur with diabetic neuropathies (1,24) and/or 2) a change in sensitivity of the sweat gland to a given concentration of neurotransmitters. Although we excluded participants with T2D who had evidence of peripheral or autonomic neuropathy on physical examination, we cannot rule out the possibility that some participants may have had more subtle neuropathies that were undetected by the clinical screening tests. With respect to the latter, sweat production has been linked to the bioavailability of nitric oxide (36). More recently, Welch et al. (43) reported that nitric oxide may play a role in the modulation of sweat rate during exercise in the heat. However, studies show that nitric oxide bioavailability may be blunted with diabetes (41).

As noted earlier, we did not observe parallel differences between groups in local and whole-body heat loss responses during exercise. The lack of difference in local heat loss responses between the T2D and the nondiabetic controls, however, does not rule out thermoregulatory impairment of local sudomotor and vasomotor activity. In light of the preponderance of evidence demonstrating reductions in local SkBF (3,39–41,44) in response to passive heating and/or pharmacological stimuli, we had expected to see marked differences in our local forearm SkBF measurements. Given that the aim of this study was to assess whole-body heat loss, we used a whole-body calorimeter to perform our measurements, which limited our ability to perform measurements at multiple skin sites. Regardless, it is important to note that although a number of recent studies have observed reductions in forearm SkBF (39,40,44), consistent with our observations, Strom et al. (42) recently reported no impairment in local forearm skin vasodilation in relatively healthy individuals with T2D. With respect to the sweating response, only one study has examined sweat production in individuals with diabetes during a passive heat exposure, isometric exercise, and their combination (30). However, the diabetic group in this study included individuals with both type 1 and T2D. As such, it is not possible to determine whether the level of sudomotor impairment differed between those individuals with type 1 and T2D. It has been suggested that the level of impairment in sudomotor function may be more pronounced in individual with type 1 diabetes (7).

It is possible that the lack of difference in local heat loss responses between the T2D and the nondiabetic controls during the exercise bout could be the result of differences in age-related decrements in SkBF and sweating. Inoue et al. (14) reported that age-related reductions in vasomotor and sudomotor function may not occur at a uniform rate over the entire body and can vary between individuals of similar age. Moreover, within the diabetic population, the response (magnitude of change) is heterogeneous (7). In view of the fact that we measured marked reductions in whole-body heat loss, paralleled by greater heat storage, it is possible that differences would have been observed had we measured multiple skin sites and/or used a higher metabolic and/or environmental heat load. In support of this possibility, a recent study by Gagnon and Kenny (8) found that differences in local sweat rates between independent groups (i.e., males and females) for different skin sites varied as a function of the level of heat production (and therefore requirement for heat loss). Local SkBF is ultimately used to indicate changes in thermal conductivity and as an index of dry heat loss, whereas local measurements of sweating are used to indicate changes in evaporation. However, they are only representative of localized changes in sudomotor and vasomotor activity. If local declines in SkBF and sweat production in one region of the body are counterbalanced by increased SkBF and sweat production at other sites due to regional differences in the level of activation, changes in SkBF and sweating may not be reflective of whole-body (dry + evaporative) heat loss. Although the measurements of other skin sites may have yielded differences between groups, we used a gold standard measure (i.e., whole-body calorimetry) to assess the body’s ability to dissipate heat. Our findings provide conclusive evidence that irrespective of regional variations in local heat loss responses, individuals with diabetes have an impaired ability to dissipate heat and store more heat during exercise.

Although we observed markedly greater heat storage during exercise in the individuals with T2D, this was not paralleled by differences in rectal and skin temperatures. It has been demonstrated previously that measurements of core and skin temperature do not accurately represent the magnitude of residual heat storage of exercise (15). In fact, studies show that the use of a two-compartment thermometry model based on core and skin temperature measurements underestimates body heat storage by as much as 35% during exercise in warm (30°C) ambient conditions. The heat transfer/distribution between internal tissues such as visceral organs and skeletal muscle can vary profoundly during exercise (15), and this may be further exacerbated by diabetes-related differences in tissue vascular flow (20,23,40,41). Taken together, our findings demonstrate that measurements of local heat loss and core temperature responses cannot be reliably interpreted when examined between independent groups for the purposes of evaluating differences in the body’s physiological capacity to dissipate heat. The use of whole-body calorimetry to assess changes in whole-body heat loss capacity is one way of eliminating the potential confounding effects of regional variations in local heat loss and tissue heat exchange (16,17).

In contrast to our observations during exercise, we measured similar responses in local and whole-body heat loss during the postexercise recovery period, albeit no differences were measured between groups. After cessation of exercise, we observed a similar rapid decay in both local and whole-body heat loss in both the T2D and control groups. The rapid attenuation in heat loss occurred despite a significant residual heat load measured at end exercise in both groups (i.e., T2D, 367 kJ; CON, 238 kJ), which remained significantly elevated at the end of the 60-min recovery (i.e., T2D, 288 kJ; CON, 107 kJ). Interestingly, despite a greater residual heat load in the T2D group measured at end exercise, both groups showed a rapid decrease in whole-body heat loss to similar levels in the first 5 min of recovery and for the duration of the recovery period. By the end of the 60-min recovery, the T2D group lost only 21% (79 kJ) of the total heat gained during exercise, whereas their nondiabetic counterparts lost in excess of 55% (131 kJ). In view of the significantly greater end exercise heat load measured in the T2D group, a correspondingly higher rate of whole-body heat loss would have been expected. Numerous reports demonstrate that the recovery from dynamic exercise results in significant disturbance of thermoregulatory control (17). Our present findings demonstrate all the hallmarks of a postexercise disturbance in thermal homeostasis, namely, a prolonged elevation in core temperature and a concomitant suppression of thermoeffector activity in the early stages of recovery (17). It is believed that the factors contributing to the alteration in postexercise whole-body homeothermy are those of nonthermal origin. Specifically, sensory end organ modulation of heat loss associated with postexercise baroreceptor, osmoreceptor, and/or metaboreceptor activation (17,25). On the basis of the current findings, however, it is not possible to determine whether the more rapid attenuation of local and whole-body heat loss responses are associated with a diabetes-related impairment of thermoeffector activity, a greater sensory end organ modulation of heat loss, or a combination of the two. Further studies must be conducted to examine the separate and relative influence of nonthermal factors on thermoregulatory function in diabetes.

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Consideration

The current study did not examine local and whole-body heat loss at different levels of thermal stress. 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 whole-body heat loss required to achieve heat balance during exercise, particularly in the heat, is determined by the sum of metabolic and environmental (dry heat gain from the environment) heat load. An exercise-induced increase in metabolic heat production augments the rate at which heat must be dissipated to the environment. So long as the concomitant increase in the rate of whole-body heat loss is sufficient to match the rate of metabolic heat production, heat balance will be reestablished. However, if the rate of metabolic heat production (as occurs with increases in exercise intensity) exceeds the rate of THL, a progressive increase in body heat storage will occur as observed in the present study. The increase can be more pronounced when exercise is performed in hot ambient conditions due to the elevated rate of dry heat gain. Thus, it will be important to conduct further studies to evaluate 1) if diabetes-related differences are evident at progressively greater heat loads, and therefore requirements for heat loss and 2) if the degree of impairment augments with increases in the level of heat stress. Further, it will be important to determine how the response may change with advancing age. Other factors that would need to be considered in advancing our understanding of the effects of diabetes on the body’s physiological capacity to dissipate heat include glycemic control (HbA1c), duration of diabetes, and level of physical activity (i.e., sedentary vs habitually active), among others.

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CONCLUSION

The current study examined differences in local and whole-body heat loss during exercise in older habitually active adults with T2D relative to their well-matched nondiabetic counterparts. The current results demonstrate that older adults with T2D have a reduced capacity to dissipate heat and store more heat during moderate intensity exercise in a warm environment. The lower whole-body evaporative heat loss observed in the participants with diabetes was paralleled by a lower thermosensitivity of the response, without any significant differences in the onset threshold. The present findings demonstrate that older adults with T2D may be at greater risk of developing a heat-related injury during exercise in the heat.

The current work was supported by the Natural Sciences and Engineering Research Council (grant no. RGPIN-298159-2009, held by Dr. Kenny) and Leaders Opportunity Fund from the Canada Foundation for Innovation (grant no. 22529, held by Dr. Kenny). Dr. Glen P. Kenny was supported by a grant from the University of Ottawa Research Chair in Environmental Physiology. The provision of financial support does not in any way infer or imply endorsement of the research findings by either agency. Jill M. Stapleton, Jane E. Yardley, and Glen P. Kenny were working for the University of Ottawa, Human and Environmental Physiology Research Unit. Pierre Boulay was working for the Champlain Diabetes Regional Coordination Centre. Ronald J. Sigal was working for the University of Calgary, Departments of Medicine, Cardiac Sciences and Community Health Sciences, Faculties of Medicine and Kinesiology.

The authors thank all the members of the Human and Environmental Physiology Research Unit who assisted with data collection, with special thanks to Candice Brown for her involvement in participant recruitment and data collection. They also thank all the participants who volunteered for the present study.

The authors declare no conflict of interest.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

AGING; CHRONIC DISEASE; HEAT STRESS; CALORIMETRY; CHANGE IN BODY HEAT CONTENT; CORE TEMPERATURE

© 2013 American College of Sports Medicine