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Performance in the Heat—Physiological Factors of Importance for Hyperthermia‐Induced Fatigue

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Abstract

This article presents a historical overview and an up‐to‐date review of hyperthermia‐induced fatigue during exercise in the heat. Exercise in the heat is associated with a thermoregulatory burden which mediates cardiovascular challenges and influence the cerebral function, increase the pulmonary ventilation, and alter muscle metabolism; which all potentially may contribute to fatigue and impair the ability to sustain power output during aerobic exercise. For maximal intensity exercise, the performance impairment is clearly influenced by cardiovascular limitations to simultaneously support thermoregulation and oxygen delivery to the active skeletal muscle. In contrast, during submaximal intensity exercise at a fixed intensity, muscle blood flow and oxygen consumption remain unchanged and the potential influence from cardiovascular stressing and/or high skin temperature is not related to decreased oxygen delivery to the skeletal muscles. Regardless, performance is markedly deteriorated and exercise‐induced hyperthermia is associated with central fatigue as indicated by impaired ability to sustain maximal muscle activation during sustained contractions. The central fatigue appears to be influenced by neurotransmitter activity of the dopaminergic system, but inhibitory signals from thermoreceptors arising secondary to the elevated core, muscle and skin temperatures and augmented afferent feedback from the increased ventilation and the cardiovascular stressing (perhaps baroreceptor sensing of blood pressure stability) and metabolic alterations within the skeletal muscles are likely all factors of importance for afferent feedback to mediate hyperthermia‐induced fatigue during submaximal intensity exercise. Taking all the potential factors into account, we propose an integrative model that may help understanding the interplay among factors, but also acknowledging that the influence from a given factor depends on the exercise hyperthermia situation. © 2014 American Physiological Society. Compr Physiol 4:657‐689, 2014.

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Figure 1. Figure 1. Integrative model with the potential cardiovascular, respiratory, central nervous system, and peripheral factors that may influence fatigue during prolonged exercise in the heat. Detailed discussion and explanations for the interactions indicated by the arrows are given in the text, but in brief summarized here. Hyperthermia‐induced cardiovascular changes may influence muscle function if cardiac output becomes inadequate to support muscle blood flow and oxygen delivery declines (as observed during exercise eliciting maximal oxygen uptake). Furthermore, cardiovascular changes may also influence cerebral blood flow, substrate and oxygen delivery to the brain, and the cerebral heat balance. The changes in cerebral blood flow are highly dependent on the hypocapnia provoked by the hyperventilation observed during exercise with hyperthermia (see Fig. 8). Central nervous system alterations are focused on neurobiological changes that may influence motor activation (and hence the ability to maintain muscle function) or influence perceived exertion and interact with “psychological factors.” Changes in muscle function when the tissue temperature is elevated or as consequence of impaired oxygen delivery may directly influence peripheral fatigue or it may influence afferent feedback and hence CNS factors of importance for central fatigue. The influence from afferent feedback may also include signals from the elevated skin temperature and the associated cardiovascular stressing.
Figure 2. Figure 2. Effect of local temperature of forearm blood flow during cycle exercise. The skin of the experimental forearm was either heated to 39°C (open circles) or cooled to 27°C (filled circles), and skin of the control arm was maintained at 33°C. Blood flow in the experimental arm is plotted against blood flow measured simultaneously in the control arm. If no effect of local temperature, plotted points would lie on the line of identity. Redrawn with permission from Ref. 316.
Figure 3. Figure 3. The impact of high skin temperature on elevating heart rate during light‐intensity exercise. Reprint, with permission, from Cheuvront et al. (46).
Figure 4. Figure 4. Impact of high skin temperature on cardiovascular responses during light‐intensity exercise. Perfusate temperature is that circulated within the water perfused suit. T sk represents skin temperature; T rectal represents rectal temperature; T blood represents blood temperature; CO represents cardiac output; HR represents heart rate; SV represents stroke volume; CBV represents central blood volume; AoMP represents aortic pressure; RaMP represents right atrium mean pressure; and TPR represents total peripheral resistance. Redrawn, with permission, from Rowell et al. (254).
Figure 5. Figure 5. Power output (kJ) achieved during 3‐min blocks during Time Trial tests in hot (40°C) compensable heat stress and in temperate (21°C) conditions. Asterisk indicates significant difference between trials. Reprinted, with permission, from Ely et al. (64).
Figure 6. Figure 6. (A) force production, (B) voluntary activation level, and (C) rectified integrated surface electromyography (IEMG) from m. vastus lateralis during 2 min of sustained maximal knee extension during hyperthermia (core temperature of ∼40°C) and control (core temperature of 38°C). The subjects were instructed and verbally encouraged to make a maximal effort throughout the contraction and electrical stimulation (EL) was superimposed every 30 s to assess the level of voluntary activation, which was calculated as voluntary force divided by the force elicited when EL was superimposed. Data are means ± SE for eight subjects [error bars not included in Figure 6(A)]. *indicates that all values in this period are significantly lower than control, P< 0.05. Modified from Nybo & Nielsen (204), with permission.
Figure 7. Figure 7. Knee extension maximal isometric force production (MVC; top) and voluntary activation (VA; bottom) during passive heating and cooling. Matching letters indicate significant differences (P < 0.001). During the heating phase, the skin temperature increased rapidly and remained above 39°C from second measure of MVC and throughout the heating phase. During the cooling phase, the mean skin temperature was quickly lowered to 33°C (first MVC measure in the cooling phase) and further to 31°C or below for the remaining of the cooling phase. Reprinted from Morrison et al (181), with permission.
Figure 8. Figure 8. (A) MCA V mean, middle cerebral artery mean blood velocity, (B) arterial carbon dioxide pressure (PaCO2), and (C) ventilation during prolonged exercise with and without hyperthermia. (•) Hyperthermic trial, (○) control trial, and (▴) MCA V mean in the hyperthermic trial when the values are related to the PaCO2 in the control trial. Values represent means ± SEM for eight subjects. *significantly different from 10 min value, P < 0.05. †significally different from control, P < 0.05. Adapted from Nybo and Nielsen (205), with permission.
Figure 9. Figure 9. (A) CBF, cerebral blood flow; (B) avDO2, arterio‐jugular venous difference of oxygen, and (C) CMRO2, cerebral metabolic rate of oxygen, measured during prolonged exercise with and without hyperthermia. Values at t = 0 min represents resting measurements. All values are means ± SE for eight subjects. *significantly different from control (P < 0.05). Adapted from Nybo et al. (203), with permission.
Figure 10. Figure 10. Esophageal, tympanic, arterial, and jugular venous blood temperature responses during cycling with a normal core temperature response (top panel; control trial) and during a similar exercise bout with progressive hyperthermia (lower panel). Values are means of seven subjects. Standard deviations are omitted for simplicity, but the SDs of all temperatures were in the range of 0.1 to 0.3°C. Adapted From Nybo et al. (209), with permission.
Figure 11. Figure 11. Time trial performance during exercise with prior ingestion of bupripion (bup; a combined dopamine and noradrenaline reuptake inhibitor) or placebo (pla) in normal (18°C) and hot (30°C) environments. (B) Time trial performance during exercise with prior ingestion of methylphenidate (mph; a dopamine reuptake inhibitor) or placebo (pla) in normal (18°C) and hot (30°C) environments. The exercise protocol in both studies consisted of 60 min constant load exercise at a workload corresponding to 55%W max, followed by a time trial, which required the subjects to complete a predetermined amount of work equal to 30 min at 75%W max as quickly as possible Values are mean ± SD. Adapted From Watson et al. (314) and Roelands et al. (240), with permission.


Figure 1. Integrative model with the potential cardiovascular, respiratory, central nervous system, and peripheral factors that may influence fatigue during prolonged exercise in the heat. Detailed discussion and explanations for the interactions indicated by the arrows are given in the text, but in brief summarized here. Hyperthermia‐induced cardiovascular changes may influence muscle function if cardiac output becomes inadequate to support muscle blood flow and oxygen delivery declines (as observed during exercise eliciting maximal oxygen uptake). Furthermore, cardiovascular changes may also influence cerebral blood flow, substrate and oxygen delivery to the brain, and the cerebral heat balance. The changes in cerebral blood flow are highly dependent on the hypocapnia provoked by the hyperventilation observed during exercise with hyperthermia (see Fig. 8). Central nervous system alterations are focused on neurobiological changes that may influence motor activation (and hence the ability to maintain muscle function) or influence perceived exertion and interact with “psychological factors.” Changes in muscle function when the tissue temperature is elevated or as consequence of impaired oxygen delivery may directly influence peripheral fatigue or it may influence afferent feedback and hence CNS factors of importance for central fatigue. The influence from afferent feedback may also include signals from the elevated skin temperature and the associated cardiovascular stressing.


Figure 2. Effect of local temperature of forearm blood flow during cycle exercise. The skin of the experimental forearm was either heated to 39°C (open circles) or cooled to 27°C (filled circles), and skin of the control arm was maintained at 33°C. Blood flow in the experimental arm is plotted against blood flow measured simultaneously in the control arm. If no effect of local temperature, plotted points would lie on the line of identity. Redrawn with permission from Ref. 316.


Figure 3. The impact of high skin temperature on elevating heart rate during light‐intensity exercise. Reprint, with permission, from Cheuvront et al. (46).


Figure 4. Impact of high skin temperature on cardiovascular responses during light‐intensity exercise. Perfusate temperature is that circulated within the water perfused suit. T sk represents skin temperature; T rectal represents rectal temperature; T blood represents blood temperature; CO represents cardiac output; HR represents heart rate; SV represents stroke volume; CBV represents central blood volume; AoMP represents aortic pressure; RaMP represents right atrium mean pressure; and TPR represents total peripheral resistance. Redrawn, with permission, from Rowell et al. (254).


Figure 5. Power output (kJ) achieved during 3‐min blocks during Time Trial tests in hot (40°C) compensable heat stress and in temperate (21°C) conditions. Asterisk indicates significant difference between trials. Reprinted, with permission, from Ely et al. (64).


Figure 6. (A) force production, (B) voluntary activation level, and (C) rectified integrated surface electromyography (IEMG) from m. vastus lateralis during 2 min of sustained maximal knee extension during hyperthermia (core temperature of ∼40°C) and control (core temperature of 38°C). The subjects were instructed and verbally encouraged to make a maximal effort throughout the contraction and electrical stimulation (EL) was superimposed every 30 s to assess the level of voluntary activation, which was calculated as voluntary force divided by the force elicited when EL was superimposed. Data are means ± SE for eight subjects [error bars not included in Figure 6(A)]. *indicates that all values in this period are significantly lower than control, P< 0.05. Modified from Nybo & Nielsen (204), with permission.


Figure 7. Knee extension maximal isometric force production (MVC; top) and voluntary activation (VA; bottom) during passive heating and cooling. Matching letters indicate significant differences (P < 0.001). During the heating phase, the skin temperature increased rapidly and remained above 39°C from second measure of MVC and throughout the heating phase. During the cooling phase, the mean skin temperature was quickly lowered to 33°C (first MVC measure in the cooling phase) and further to 31°C or below for the remaining of the cooling phase. Reprinted from Morrison et al (181), with permission.


Figure 8. (A) MCA V mean, middle cerebral artery mean blood velocity, (B) arterial carbon dioxide pressure (PaCO2), and (C) ventilation during prolonged exercise with and without hyperthermia. (•) Hyperthermic trial, (○) control trial, and (▴) MCA V mean in the hyperthermic trial when the values are related to the PaCO2 in the control trial. Values represent means ± SEM for eight subjects. *significantly different from 10 min value, P < 0.05. †significally different from control, P < 0.05. Adapted from Nybo and Nielsen (205), with permission.


Figure 9. (A) CBF, cerebral blood flow; (B) avDO2, arterio‐jugular venous difference of oxygen, and (C) CMRO2, cerebral metabolic rate of oxygen, measured during prolonged exercise with and without hyperthermia. Values at t = 0 min represents resting measurements. All values are means ± SE for eight subjects. *significantly different from control (P < 0.05). Adapted from Nybo et al. (203), with permission.


Figure 10. Esophageal, tympanic, arterial, and jugular venous blood temperature responses during cycling with a normal core temperature response (top panel; control trial) and during a similar exercise bout with progressive hyperthermia (lower panel). Values are means of seven subjects. Standard deviations are omitted for simplicity, but the SDs of all temperatures were in the range of 0.1 to 0.3°C. Adapted From Nybo et al. (209), with permission.


Figure 11. Time trial performance during exercise with prior ingestion of bupripion (bup; a combined dopamine and noradrenaline reuptake inhibitor) or placebo (pla) in normal (18°C) and hot (30°C) environments. (B) Time trial performance during exercise with prior ingestion of methylphenidate (mph; a dopamine reuptake inhibitor) or placebo (pla) in normal (18°C) and hot (30°C) environments. The exercise protocol in both studies consisted of 60 min constant load exercise at a workload corresponding to 55%W max, followed by a time trial, which required the subjects to complete a predetermined amount of work equal to 30 min at 75%W max as quickly as possible Values are mean ± SD. Adapted From Watson et al. (314) and Roelands et al. (240), with permission.
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Lars Nybo, Peter Rasmussen, Michael N. Sawka. Performance in the Heat—Physiological Factors of Importance for Hyperthermia‐Induced Fatigue. Compr Physiol 2014, 4: 657-689. doi: 10.1002/cphy.c130012