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.
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).
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.
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.
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).
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.
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.
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:© 2013 American College of Sports Medicine
AGING; CHRONIC DISEASE; HEAT STRESS; CALORIMETRY; CHANGE IN BODY HEAT CONTENT; CORE TEMPERATURE