Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise

Parkin, J. M., M. F. Carey, S. Zhao, and M. A. Feb- braio. Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise. J. Appl. Physiol. 86(3): 902–908, 1999.—To examine the effect of ambient temperature on metabolism during fatiguing sub- maximal exercise, eight men cycled to exhaustion at a work- load requiring 70% peak pulmonary oxygen uptake on three separate occasions, at least 1 wk apart. These trials were conducted in ambient temperatures of 3°C (CT), 20°C (NT), and 40°C (HT). Although no differences in muscle or rectal temperature were observed before exercise, both muscle and rectal temperature were higher (P 􏱁 0.05) at fatigue in HT compared with CT and NT. Exercise time was longer in CT compared with NT, which, in turn, was longer compared with HT (85 􏱋 8 vs. 60 􏱋 11 vs. 30 􏱋 3 min, respectively; P 􏱁 0.05). Plasma epinephrine concentration was not different at rest or at the point of fatigue when the three trials were compared, but concentrations of this hormone were higher (P 􏱁 0.05) when HT was compared with NT, which in turn was higher (P 􏱁 0.05) compared with CT after 20 min of exercise. Muscle glycogen concentration was not different at rest when the three trials were compared but was higher at fatigue in HT compared with NT and CT, which were not different (299 􏱋 33 vs. 153 􏱋 27 and 116 􏱋 28 mmol/kg dry wt, respectively; P 􏱁 0.01). Intramuscular lactate concentration was not different at rest when the three trials were compared but was higher (P 􏱁 0.05) at fatigue in HT compared with CT. No differences in the concentration of the total intramuscular adenine nucleo- tide pool (ATP 􏱆 ADP 􏱆 AMP), phosphocreatine, or creatine were observed before or after exercise when the trials were compared. Although intramuscular IMP concentrations were not statistically different before or after exercise when the three trials were compared, there was an exercise-induced increase (P 􏱁 0.01) in IMP. These results demonstrate that fatigue during prolonged exercise in hot conditions is not related to carbohydrate availability. Furthermore, the in- creased endurance in CT compared with NT is probably due to a reduced glycogenolyticrate.

FATIGUE during prolonged, submaximal exercise often coincides with glycogen depletion (9, 10, 37), and endur- ance can be increased by providing exogenous carbohy- drate during exercise (7, 10). During prolonged submaxi- mal exercise, glycogen stores within the muscle are lowered, eventually giving rise to reduced glycolytic flux, leading to a fall in pyruvate formation (37) and a reduction in tricarboxylic acid cycle (TCA) intermedi- ates (TCAI) (18). It has been hypothesized that this reduction in flux through the TCA cycle decreases mitochondrial NADH production and energy turnover via oxidative phosphorylation, leading to ATP genera- tion from alternative pathways (40). One such pathway, the adenylate kinase reaction, also results in the formation of AMP, which is rapidly deaminated to IMP. Accordingly, many studies have noted the accumula- tion of IMP at fatigue during prolonged exercise in the presence of low intramuscular glycogen stores (4, 34, 37, 39, 40) but not earlier during exercise when glyco- gen stores are adequate (34, 37). Although exercise in the heat often results in an increase in intramuscular glycogen utilization (13, 14, 16), fatigue, in these circum- stances, appears to be related to factors other than carbohydrate availability. It has been demonstrated that intramuscular glycogen concentration is 􏱃300 mmol/kg dry wt at fatigue during submaximal exercise in the heat (33), whereas carbohydrate supplementa- tion provides no ergogenic benefit in these circum- stances (12). It is likely, therefore, that at fatigue during exercise in the heat there would be no signifi- cant accumulation of IMP, although this has never been investigated.

When the rise in body temperature is attenuated during prolonged exercise by either reducing the ambi- ent temperature (15), providing external cooling (26), or preventing dehydration (20), contracting muscle glycogen utilization is reduced. It is possible that the sparing of glycogen may be due to enhanced lipid oxidation because both plasma free fatty acid mobiliza- tion and fatty acid oxidation increase with cold expo- sure (24). In addition, when the rise in body tempera- ture is attenuated, exercise performance is increased (12, 17, 23, 28). Although no previous studies have examined muscle metabolism at fatigue during pro- longed exercise in cooler ambient temperatures, it is likely that intramuscular glycogen stores would be depleted and IMP elevated because providing exoge- neous carbohydrate in these conditions results in in- creased endurance (15).
The present study examined metabolism during pro- longed submaximal exercise to exhaustion at a range of ambient temperatures: cool (3°C), thermoneutral (20°C), and hot (40°C). We hypothesized that at fatigue during prolonged submaximal exercise in a hot environment, muscle glycogen levels would be adequate, resulting in no significant formation of IMP. In contrast, we ex- pected glycogen to be depleted after prolonged submaxi- mal exercise in both cool and thermoneutral environ- ments, resulting in marked increases in IMP at fatigue, but that exercise duration would be prolonged in the cooler environment due to a reduction in glycolyticrate.

MATERIALS AND METHODS
Subjects. Eight endurance-trained men [age 22.6 􏱋 4.5 (SD) yr; height 176.4 􏱋 4.8 cm; weight 75.9 􏱋 8.5 kg; peak pulmonary oxygen uptake (V ̇O2peak) 4.2 􏱋 0.6 l/min] volun- teered as subjects for this study. The subjects were informed of the purpose and the risks associated with the procedures and were free to withdraw from the study at any time. Written informed consent was obtained from all subjects before they commenced the experiment. The study was approved by the Victoria University of Technology Human Research Ethics Committee.
Experimental procedures. V ̇ O2 peak was determined on a friction-braked bicycle ergometer (Ergomatic 814E, Monark, Varberg, Sweden) by using an incremental cycling exercise test to volitional fatigue at 20–22°C as previously described (13).
At least 7 days after the V ̇ O2 peak test, subjects arrived at the laboratory to participate in one of three trials. Each trial required subjects to cycle at 70% V ̇O2peak in a temperature- and humidity-controlled chamber maintained at tempera- tures of 3°C (CT), 20°C (NT), or 40°C (HT) with a relative humidity of 􏱁50% in each condition. The trials were con- ducted in a counterbalanced fashion to remove any chance of an order effect. The subjects arrived after an overnight fast, having refrained from strenuous exercise, alcohol, caffeine, and tobacco for a period of 24 h. To minimize differences in resting muscle glycogen concentration, subjects completed a 48-h diet and activity log before the first trial and were then instructed to follow the same diet and activities before the second and third trials. To further minimize differences, subjects were provided with a standardized carbohydrate meal, which they consumed the night before each exercise trial.
On arrival at the laboratory, the subjects voided, were weighed nude, and positioned a rectal thermometer (Mono- therm, Mallinckrodt Medical, St. Louis, MO) 10 – 15 cm beyond the anal sphincter. The subjects then moved into the environmental chamber and lay supine. A 20-gauge indwell- ing Teflon catheter (Terumo, Tokyo, Japan) was inserted into an antecubital vein of one arm, and a resting blood sample was obtained. The catheter was kept patent by flushing with 0.5 ml NaCl containing 5 U of heparin after each sample collection. After anesthesia, two incisions were made 􏴗10 and 13 cm proximal to the lateral epicondyle of the femur, and a muscle sample was removed from the vastus lateralis (distal incision) by using the percutaneous needle biopsy technique (1) modified to include suction. The sample was quickly frozen in liquid N2. Muscle temperature (Tmu) was measured imme- diately after the biopsy by using a needle thermistor (YSI 525, Yellow Springs Instruments, Yellow Springs OH) inserted to a depth of 4 cm through the biopsy incision. Subjects then moved to the cycle ergometer, a heart rate monitor (Sports Tester, Polar) was positioned, and exercise commenced. The friction-braked cycle ergometer was interfaced with a com- puter by using a data-acquisition operating system software. Subjects were instructed to cycle at 80 rpm, which allowed for the maintenance of a work rate that was equivalent to 70% V ̇O2peak. Fatigue was defined as the point when subjects were unable to maintain 70 rpm for 20 s consecutively. At the point of fatigue, a muscle biopsy was sampled and immedi- ately frozen in liquid N2, and Tmu was subsequently mea- sured. Blood samples were obtained at 20 min of exercise and at fatigue. Heart rate and rectal temperature (Tre) were recorded at rest; at 5, 10, and 20 min of exercise; and then every 20 min until fatigue. Pulmonary gases were collected at the same time points by using Douglas bags as previously described (13). Subjects wore cycling shorts and shoes during all trials and were not supplied with fluid or circulating air throughout the period of the exercise.

Analytic techniques. Oxygen uptake (V ̇O2) and respiratory exchange ratio (RER) were calculated from expired gases by using standardized equations (8). For sampling, an aliquot (1.5 ml) of whole blood was placed in a tube containing 30 μl of EGTA and reduced glutathione, mixed, and spun at 1,500 rpm at 4°C for 15 min, and the supernatant was stored at 􏱇80°C until analysis. Samples were analyzed for plasma catecholamines by using the single-isotope 3H radioenzy- matic assay as described in the Amersham Catecholamines Research Assay System (code TRK 995). Each muscle sample was divided into two portions and weighed at 􏱇20°C. One portion was extracted, neutralized, and analyzed for NH3 by the flow-injection analysis technique as described by Katz et al. (25). The remaining muscle was subsequently freeze- dried, dissected free of any blood and connective tissue, powdered, and divided into two portions. Glycogen concentra- tion was determined from one portion after acid hydrolysis and neutralization according to the procedure of Passonneau and Lauderdale (35). The second portion was extracted according to the procedure of Harris et al. (21) and analyzed enzymatically for lactate (La), creatine (Cr), and creatine phosphate (PCr) by using fluorometric detection, according to the methods of Lowry and Passonneau (29). Reverse-phase high-performance liquid chromatography was used to quan- tify ATP, ADP, AMP and IMP according to the method of Wynants and Van Belle (43). Muscle NH3 was corrected for water content on the basis of the wet-to-dry weight ratio determined from the freeze-dried sample. Muscle metabo- lites, except for La, glycogen, and NH3 (because of their extracellular presence) were adjusted to peak total Cr for each subject to correct for variability in blood, connective tissue, and other nonmuscle constituents between biopsies.

Statistics. A biomedical statistical software package was used for all statistical calculations. A two-way (time and treatment) ANOVA with repeated measures was used to compare the data collected in the three trials. When the two-way ANOVA revealed a significant interaction, simple main-effects analysis was used to locate the differences. When the analyses indicated a significant difference, a New- man-Keuls post hoc test was used to locate the difference. The level of probability to reject the null hypothesis was set at P 􏱁 0.05. All comparative data are expressed as means 􏱋 SE.

RESULTS
Exercise time was longer (P 􏱁 0.05) in CT compared with NT which, in turn, was longer (P 􏱁 0.05) compared with HT (Fig. 1). Neither V ̇O2 nor RER was different when the three trials were compared at any measure- ment point (data not shown). Mean heart rate during exercise was higher (P 􏱁 0.05) in HT compared with NT and CT. Heart rate was not different in NT compared with CT (181 􏱋 2 vs. 173 􏱋 2 vs. 168 􏱋 2 beats/min for HT, NT, and CT respectively).

Tmu was not different when the three trials were compared at rest, but it was higher (P 􏱁 0.01) at fatigue when compared with rest in all trials. Tmu was higher (P 􏱁 0.05) at fatigue in HT compared with NT and CT (40.7 􏱋 3 vs. 39.4 􏱋 2 vs. 39.4 􏱋 2°C for HT, NT, and CT, respectively). The values at fatigue were not different when the latter two trials were compared (Fig. 2). Tre was not different when the three trials were compared at rest. No differences were observed when NT was compared with CT at any point during exercise. In contrast, Tre was higher (P 􏱁 0.05) at 10 min and thereafter when HT was compared with the other trials (Fig. 2).

Plasma epinephrine concentration was not different at rest when the three trials were compared. The concentration of this hormone was, however, higher (P 􏱁 0.05) after 20 min of exercise in HT compared with NT and CT. Furthermore, the plasma epinephrine concentration was higher (P 􏱁 0.05) in NT compared with CT at this time. No differences were observed in plasma epinephrine concentration at fatigue when the three trials was compared (Fig. 3). Plasma norepineph- rine concentration was not different when the three trials were compared at any point (data not shown).

Concentrations of the total adenine nucleotide pool (ATP 􏱆 ADP 􏱆 AMP) were not different when the three trials were compared. (Table 1). Concentrations of Cr were higher (P 􏱁 0.05) and of PCr lower (P 􏱁 0.05) when resting values were compared with those at fatigue, but the values were not different when the three trials were compared (Table 1). Muscle La concen- trations were not different when the three trials were compared at rest. Concentrations of this metabolite were higher (P 􏱁 0.05) at fatigue in all trials compared with rest. Although there was a graded response in muscle La concentration when the three trials at fatigue were compared, a significant difference (P 􏱁 0.05) at fatigue, was only observed when HT was compared with CT (Table 1). Muscle NH3 concentra- tions were not different when the three trials were compared at rest. Concentrations of this metabolite were higher (P 􏱁 0.05) at fatigue in all trials compared with rest. Postexercise muscle NH3 concentration was greater (P 􏱁 0.05) in CT when compared with NT and HT. Postexercise muscle NH3 concentrations were not different when NT was compared with HT (Table 1). Intramuscular glycogen content was not different when the three trials were compared at rest. Postexercise muscle glycogen content was lower (P 􏱁 0.05) when compared with rest for all trials, although it was greater (P 􏱁 0.05) in HT when compared with both NT and CT. Concentrations of this metabolite were not different between these two trials postexercise (Fig. 4), but the longer exercise duration rendered the glycogen- olytic rate to be greater (P 􏱁 0.05) in NT compared with CT (6.1 􏱋 0.9 vs. 4.3 􏱋 0.5 mmol glucosyl units · kg􏱇1 · min􏱇1 ). Although IMP concentrations were not statistically different before or after exercise when the three trials were compared, there was a main effect (P 􏱁 0.05) for exercise for this metabolite (Fig. 4).

DISCUSSION
The results from this study demonstrate that glyco- gen content within contracting muscle at fatigue dur- ing exercise in the heat is not reduced to the low levels observed during exercise in comfortable ambient tem- peratures, and, therefore, fatigue during exercise in the heat is related to processes other than carbohydrate availability. In addition, the main effect for exercise in IMP within contracting muscle indicates that the accu- mulation of this metabolite during prolonged exercise in the heat is not related to substrate availability. Because no differences were observed in muscle glyco- gen content or energy metabolism when NT was com- pared with CT, the 30% improved performance in CT probably reflects a lower rate of glycogen utilization for the exercise duration.

Several studies have previously demonstrated that attenuating body core temperature by employing a precooling maneuver (3, 23, 28), lowering ambient temperature (12, 17), or cooling with ice packs (26, 27) improves exercise performance. No studies, however, have examined intramuscular metabolism in these circumstances. The data from the present study sug- gest that the reason for the improved performance with cooling is likely to be related to carbohydrate availabil- ity because we observed a lower glycogenolytic rate. The mechanism for such a lower glycogenolytic rate is probably due to the blunted epinephrine concentration observed early during exercise (Fig. 3), because epineph- rine concentration influences glycogen use during sub- maximal exercise in trained men (11). The present data

are consistent with our earlier findings that demon- strated that an attenuated rise in body core tempera- ture was associated with a blunted epinephrine re- sponse and concommitant reductionin glycogen use during exercise in humans (15).
It has been previously demonstrated that prolonged, submaximal exercise to fatigue in comfortable ambient temperatures results in muscle glycogen depletion (2, 4, 10, 22). The reduction in glycogen availability causes a decrease in the TCAI (18, 37), a reduction in flux through the TCA cycle, and a decrease in NADH formation, leading to reduced ADP rephosphorylation (37). As a result, the transient increase in free ADP stimulates the adenylate kinase reaction, resulting in the formation of ATP and AMP. Subsequently, the AMP thus formed activates AMP deaminase, producing IMP and NH3 (4, 25, 34, 39). Results from the present study support these previous observations. Muscle glycogen content was reduced to low levels in both NT and CT (Fig. 3) Accordingly, both IMP and NH3 concentrations were elevated in these trials at fatigue.

Despite the fact that exercise in the heat accelerates the rate of glycogen utilization (13, 14, 16, 26), the muscle glycogen concentration at fatigue in HT, 􏴗300 mmol glucosyl units/kg, was higher compared with CT and NT (Fig. 3). These data support previous findings by Nielsen et al. (33), who have demonstrated that exercise duration in a hot environment is reduced, despite the presence of adequate muscle glycogen stores, and is, therefore, not related to the depletion of this substrate. It is clear, therefore, that factors other than substrate availability are related to fatigue at high ambient temperatures. It has previously been sug- gested that fatigue in these circumstances is related to a diminished central drive to exercise (6). Indeed, Nielsen et al. have demonstrated that when subjects underwent 9 days of heat acclimation they increased their exercise capacity in the heat twofold but fatigued with the same core temperature on each occasion. In addition, when subjects exercised to exhaustion in a hot environment while ingesting various beverages, they also fatigued at the same core temperature (12). The data from the present study, however, suggest that fatigue may be related, at least in part, to metabolic processes. Despite the relatively high concentration of muscle glycogen in HT at fatigue, the main effect for exercise indicates that IMP accumulation was signifi- cantly elevated above rest at this point. During the present study, we did not conduct the trials in an ordered fashion and thus could not compare muscle metabolism at the same time points in each trial. Therefore, we cannot rule out the possibility that IMP was also elevated in the presence of adequate glycogen stores in NT and CT. However, previous research has demonstrated that, during exercise in comfortable am- bient temperatures, IMP is elevated at fatigue in the presence of low glycogen stores (34, 37, 40) but not earlier when glycogen stores are adequate (34, 37). It is unlikely, therefore, that were we to sample muscle earlier in NT and CT the same relationship between IMP and glycogen that we observed in HT would be prevalent. Hence, the theory that the increase in IMP at fatigue during prolonged exercise is related to sub- strate availability appears to be untrue during exercise in hot environments.

There are several possible explanations for the accu- mulation of IMP in the presence of adequate levels of

muscle glycogen in HT at fatigue. It has been suggested (36) that as exercise in the heat progresses the increase in cardiac output is inadequate to meet the demands of increased blood flow to the skin for thermoregulation while maintaining active skeletal muscle blood flow. Potentially, therefore, this could result in a reduction in active skeletal muscle blood flow. In the absence of any rate change in oxygen extraction, it could explain the increase in IMP accumulation. It is unlikely, however, for two reasons, that alterations in blood flow to the active skeletal muscle would explain the present obser- vations. First, active muscle blood flow during exercise in humans has been demonstrated to be unaffected by heat stress (33, 38). In addition, recent data suggest that, even when active muscle blood flow is reduced in the heat with the combination of exercise and dehydra- tion, oxygen extraction is increased such that oxygen availability is not limiting (19).
Our data may suggest a temperature-induced pertur- bation in metabolism during fatiguing exercise in the heat. Brooks et al. (5) studied the phosphorylative efficiency of isolated rat skeletal muscle mitochondria by examining the ADP/O ratio over a range of tempera- tures. They observed a constant ADP/O ratio at tempera- tures ranging from 25 to 40°C; however, above 40°C the ADP/O ratio decreased linearly with increasing tem- perature. This suggests that for a given V ̇O2 the in- crease in ADP rephosphorylation was lower than the rate of ATP degradation. Similarly, Willis and Jackman (42), using rat and rabbit skeletal muscle mitochon- dria, found a 20% reduction in the ADP/O ratio at 43°C when compared with that at 37°C and suggested that the rise in muscle temperature with heavy exercise compromises the permselectivity of the inner mitochon- drial membrane, increasing nonspecific proton leakage back across this membrane and decreasing the ADP/O ratio. Interestingly, in the present study, Tmu was 􏱃40°C after exercise in the HT but was below this temperature in the other trials. Recent findings by Mills et al. (31), who observed an increase in the plasma concentration of lipid hyperoxides, an indicator of oxidative stress, in hyperthermic horses exercising to fatigue, may support the hypothesis that fatigue during exercise and heat stress may cause metabolic dysfunc- tion. Of note, we have previously observed no increase in IMP accumulation after 40 min of submaximal exercise at 40°C, even though Tmu was 􏱃40°C (14). Although speculative, the results from the present study along with previous data (14, 31) suggest that this mitochondrial disruption occurs near to or at fatigue. Further research examining the relationship among mitochondrial function, heat stress, and exer- cise is warranted.

Despite there being no statistical difference in IMP when the three trials were compared at fatigue, intra- muscular NH3 accumulation was higher in CT relative to NT. This result can best be explained by the exercise duration and pathways for NH3 production. The mecha- nisms for contracting skeletal muscle NH3 production during submaximal exercise are related to the activation of AMP deaminase and amino acid catabolism (30, 41). As exercise progresses, so too does NH3 production from amino acid catabolism (30). Because exercise duration in CT was considerably longer relative to the other trials, it is likely that increased amino acid catabolism was responsible for the higher muscle NH3 accumula- tion in this trial.
In summary, our observation of significant IMP accu- mulation at fatigue after submaximal exercise at 40°C, in the presence of adequate glycogen stores, suggests that fatigue under conditions of heat stress could reflect a temperature-induced metabolic perturbation. This may, therefore, influence in part, the reduction in performance during exercise in the heat.

 

 

 

Adaptation to Hot Environmental Conditions: An Exploration of the Performance Basis, Procedures and Future Directions to Optimise Opportunities for Elite Athletes

Abstract 
Extreme environmental conditions present athletes with diverse challenges; however, not all sporting events are limited by thermoregulatory parameters. The purpose of this leading article is to identify specific instances where hot environmental conditions either com- promise or augment performance and, where heat accli- mation appears justified, evaluate the effectiveness of pre- event acclimation processes. To identify events likely to be receptive to pre-competition heat adaptation protocols, we clustered and quantified the magnitude of difference in performance of elite athletes competing in International Association of Athletics Federations (IAAF) World

Championships (1999–2011) in hot environments ([25 °C) with those in cooler temperate conditions (\25 °C). Ath- letes in endurance events performed worse in hot condi- tions (*3 % reduction in performance, Cohen’s d [ 0.8; large impairment), while in contrast, performance in short- duration sprint events was augmented in the heat compared with temperate conditions (*1 % improvement, Cohen’s d [ 0.8; large performance gain). As endurance events were identified as compromised by the heat, we evaluated common short-term heat acclimation (B7 days, STHA) and medium-term heat acclimation (8–14 days, MTHA) pro- tocols. This process identified beneficial effects of heat acclimation on performance using both STHA (2.4 ± 3.5 %) and MTHA protocols (10.2 ± 14.0 %). These effects were differentially greater for MTHA, which also demonstrated larger reductions in both endpoint exercise heart rate (STHA: -3.5 ± 1.8 % vs MTHA: -7.0 ± 1.9 %) and endpoint core temperature (STHA: -0.7 ± 0.7 % vs -0.8 ± 0.3 %). It appears that worth- while acclimation is achievable for endurance athletes via both short-and medium-length protocols but more is gained using MTHA. Conversely, it is also conceivable that heat acclimation may be counterproductive for sprinters. As high-performance athletes are often time-poor, shorter duration protocols may be of practical preference for endurance athletes where satisfactory outcomes can be achieved.

Introduction
It is popularly perceived that performance in the heat is compromised compared with temperate conditions and that pre-competition adaptation to this environment is a necessity [1, 2]. However, this may not be the case for all events, depending on the intensity and duration of perfor- mance. For elite athletes, there are also issues of time efficiencies to be considered when determining event preparation within busy training and performance sched- ules. Therefore, although some recent articles have added some useful information on this underserved area (e.g., [3, 4]), the purpose of this leading article is to now take this issue forward and describe instances where heat adaptation may be useful, to identify protocols which lead to mean- ingful adaptations and finally to suggest future directions for this important area of research.
Endurance events in particular have often been descri- bed as being compromised in the heat [1, 2]. This effect is most likely mediated as an integrated thermoregulatory response associated with exposure to the heat, including increased exercising heart rate (HR), elevated core (Tc) and skin temperatures, greater perception of effort, thermal strain, thirst, and water loss leading to dehydration (for

reviews see [3–5]). It is, therefore, important for athletes to prepare themselves for events that may take place in environmentally challenging conditions. This strategy is particularly important in both team sports [2] and endur- ance events [6], which require performances to be sus- tained for extended periods of time potentially increasing the likelihood of athletes developing substantial dehydra- tion, overheating or a potentially critical Tc [7]. This sce- nario often results in fatigue, down-regulation of effort, performance impairment and, in extreme cases, heat illness [4–6]. However, particular scenarios where heat-induced decrements to performance are most prevalent, and the most effective evidence-based strategies of minimising these effects, are seldom described.
Almost 50 % of the world’s population now live in the Torrid Zone, close to the Earth’s equator where tempera- tures are hotter and more physically challenging than in the Temperate or Frigid Zones [8]. Consequently, many major sporting events are now scheduled to be held in geo- graphical locations that experience hot and humid envi- ronmental conditions. These locations include the 2015 International Association of Athletics Federations (IAAF) World Championships (Beijing, summer), the 2016 Olympic Games (Brazil, summer), and the 2022 Fe ́de ́ration Internationale de Football Association (FIFA) World Cup (Qatar). It is, therefore, critical that competitive athletes are adequately prepared for such competitions, particularly individuals more used to living and exercising in temperate environments and unaccustomed to hot conditions. For athletes not living and regularly training in the Torrid Zone, most would likely require some form of preparatory heat training prior to embarking on competition in this region. It is often reported that 10–14 days of heat expo- sure [3] is ample heat acclimation; however, these exten- ded interventions might not be viable for most sporting programmes. This period may be particularly challenging for time-poor high-performance athletes in terms of avail- ability, timing, training and/or logistical reasons. To com- bat this, there have been recent efforts to evaluate the effectiveness of shorter heat training programmes of 7 days or shorter duration [4, 5]. The priority for coaches and athletes in such cases is determining the minimum number of days of heat training needed to provide some benefit, within their busy training and performance schedules.
Both short- and medium-term heat adaptation protocols can elicit changes in important physiological parameters such as plasma volume (PV) expansion, reductions to exercising HR, Tc, and sweating commences at a lower Tc with a more dilute concentration of metabolites [9], which could be useful for subsequent performances in the heat and also in cool conditions where potential fluid loss is substantial [10]. It is important to understand how these physiological changes occur, and the potential effects they have on athletes’ performances. For example, an expansion of PV can promote improved performance in aerobic events, most likely by reducing plasma protein loss [11, 12] and increasing blood volume, thus mediating a decreased exercising HR in the heat through adaptive gains in central venous return and preload [4, 13, 14]. Consequently, an increase to stroke volume mediated by gains in PV and blood volume lowers cardiac frequency [15, 16]. As heat adaptation increases PV, the body more effectively regu- lates blood pressure in the face of fluid loss as a conse- quence of increased levels of sweat [17]. Collectively these adaptations lower HR, promote reduced thermal strain and more efficient transfer of heat [17]. Therefore, as PV expansion plays an important role in extending endurance exercise performance, heat training programmes promoting greater PV expansion are of benefit. Nevertheless, this adaptive response may only be of relevance for athletes undertaking endurance events, where fluid loss and heat dissipation mechanisms play a meaningful role in race or competition performance. For example, athletes competing in events that require only short bursts of anaerobic power (e.g., 100 m sprint) are unlikely to experience a decrement in performance in hot conditions as they are under sub- stantially less sustained thermal load compared with their endurance counterparts.

Comparison of Running Performances in Hot
and Temperate Conditions: IAAF Track and Field Performances (1999–2011)
Numerous studies have examined the effects of environ- mental conditions on performance in controlled isolated laboratory experiments. However, to fully ascertain whe- ther or not environmental conditions influence elite field- based performance, it is useful to consider the magnitude of change in outcomes of regularly scheduled events over a longitudinal period performed in different conditions. This type of analysis can be performed by examining secondary data from scheduled major events such as those organised by the IAAF. These data are publicly available and facil- itate rapid and meaningful comparisons when appropriately clustered for analysis of data trends. To address the ques- tion of where and which events are most affected by environmental conditions, we collated and analysed the mean of the top ten performances in distance events (top 60 % of track events) and top six performances in sprint performances (top 60 %) for males and females in the 100, 200, 400, 800, 1,500, 5,000, 10,000 m and marathon events from seven consecutive IAAF World Championships (1999–2011). Events were categorised as either temperate (n = 41) or hot (n = 44) conditions, separated using a standardised threshold temperature of 25 °C as an index of

comfortable working temperature [18]. It was determined to utilise 25 °C as it further represented the full cohort (n = 85) mean temperature (24.5 °C) and resulted in a temperate condition mean ± SD of 18.5 ± 3.2 °C (humidity 59.6 ± 7.0 %) and a hot condition mean ± SD temperature of 30 ± 4.3 °C; (humidity 61.3 ± 4.9 %), which are both in range of common specifications for these conditions. Although 25 °C is a relatively high threshold temperature, outdoor exercise benefits to a greater extent from convective cooling than laboratory exercise, meaning a higher temperature is more comfortable outdoors [19]. Therefore, we sought to recognise this in contrast to lab- oratory exercise [20].

Brief analysis of performances identified that the tem- perate conditions (\25 °C) resulted in faster performances in endurance events ([5,000 m) (*2 % mean gain, med- ium effect) (Fig. 1; Table 1). Conversely, the sprint events (B200 m) demonstrated the opposite effect with athletes performing better in hot conditions (*2 % mean gain, medium to large effect) compared with the events in temperate climates. As might be expected, middle-distance events were less affected by ambient conditions and con- siderable variation between performance gains and losses were observed for males and females, probably due to the influence of other factors such as race tactics (Fig. 1). 

The marathon exhibited the largest performance impairment in the heat, with a mean reduction of 3.1 % for males (also a large effect; effect size [ES] = -2.0) and 2.7 % mean change for females (large effect; ES = -2.4) (Table 1). Although inferences from this observation were limited due to absence of knowledge in relation to race tactics, it is most likely that these reductions in perfor- mance were primarily related to the ambient temperature and absolute humidity in which the athletes were competing.
There are logical physiological and behavioural expla- nations for the differential effects of environment on per- formance variations in endurance and sprint events which have been detailed previously [8]. However, the underlying observation that hot conditions do not necessarily com- promise all events is an important consideration for athletes and coaches in their preparation for competition based in the heat. This information should be useful for evidence- based decisions on prescribing appropriate pre-event acclimation for endurance-type activities where perfor- mance is most likely to be impeded in the heat.

Comparison of Short- and Medium-Term Heat Acclimation Models

Defining the optimum length of a heat acclimation protocol will be influenced by two factors: first, in physiological performance terms, the number of sessions needed to attain appropriate adaptations, and, second, the practical issues of logistics related to the competition such as a one-off tournament or an ongoing seasonal competition combined with player availability. Research has primarily focused on the acute effects in response to a single stressor, or in preparation for a one-off event, with little practical rec- ognition of preparatory time restrictions commonly expe- rienced by athletes across a competitive season. In most sports, teams and athletes need to compete in various conditions across a season, and hot condition events might only constitute a short period within the competitive cycle [21]. As such, it is important to consider both the acute effects of acclimation and secondary (residual) factors which might influence the magnitude and time course of benefits.

The majority of heat acclimation research to date has examined either short-term heat acclimation (B7 days, STHA) (Table 2), or medium-term heat acclimation (8–14 days, MTHA) (Table 3) protocols. Clearly, for elite athletes performing in a congested competitive season, a shorter acclimation period would be advantageous and less disruptive to routine training. Therefore, we have made a brief practical comparative analysis to identify the degree of benefit derived from both STHA and MTHA protocols [21]. A representative sample of relevant research papers were included on the basis of acclimation or acclimatisa- tion occurring in conjunction with exercise as well as the reporting of either a performance variable such as a time trial or time to exhaustion, HR, Tc or PV. From these data, pooled percentage change (mean ± 90 % confidence limits [CL]) as well as ES size was calculated.
From this brief comparison of available data, it is evi- dent that there are merits to both STHA and MTHA strategies. Both strategies appear to result in some positive effects on subsequent performance outcome, HR adapta- tions, and reductions to exercising Tc (Table 2). However, it is also evident that MTHA protocols are more beneficial for eliciting plasma volume expansion (*7 % mean gain) when compared with STHA (*3.5% mean gain) (Tables 2, 3, 4). This is also supported by changes in performance outcomes which demonstrate greater gains in response to MTHA compared with STHA protocols. The extent of any possible gain will be acutely meaningful among high-performance athletes for whom the smallest advantage represents a competitive edge (Table 4). It is plausible that elite athletes may also adapt more rapidly to a hot environment and several studies [2, 4] indicate short- term protocols are capable of evoking beneficial adapta- tions to athletic performance, but greater consistency of protocol design and a considerably larger volume of data is required to fully elucidate this area of athletic preparation. The balance between time effectiveness of the protocol and gaining meaningful adaptation should be the focus of future investigations. Nevertheless, it is important for a leading article such as this to identify important current deficiencies in contemporary practice and research litera- ture, and propose areas in which more empirical data is required. 
Based on current evidence and utilising a limited range of protocols, MTHA acclimation periods (8–14 days) are of more benefit for both performance and physiological indices such as PV expansion, lower exercising Tc, and lower end-point exercise HR. These observations are likely to be particularly meaningful for the preparation of athletes competing in particularly long duration events such as marathon or triathlon, which would be most challenging to heat dissipation mechanisms, or athletes required to con- tinue with high-quality training regimens with minimal disruption. For example, hot environmental conditions may diminish training intensity among non-acclimated athletes if they are still acclimating, which could induce a detraining effect. Therefore, the individualised require- ments and periodisation of athletic preparation must be carefully considered.

Preparatory Activities that may Optimise Exercise in the Heat
It is often purported that, for exercise-induced heat accli- mation to be most effective, athletes should employ the

same exercise mode in which they will compete [17]. One way to achieve this is to use high-specification ergometry in a regulated hot and/or humid environment in a sealed heat chamber, utilising the athlete’s common exercise modality. Depending on the expected environmental con- ditions of the targeted athletic event, mere heat exposure in the absence of (elevated) humidity is less appropriate for preparation for hot humid environments [22]. Specific humidity exposure can form part of the acclimation strat- egy if appropriate for the athlete, as high humidity is an aspect of heat exposure that is both extremely challenging and under researched [22]. Responsiveness to these con- ditions requires manipulation of training volume and intensity to ensure that the appropriate exercise and recovery strategies are applied. Quantifying the degree of thermal load throughout training sessions through devices such as ingestible Tc pills can complement this process. Simple submaximal heat stress tests that include physio- logical and performance measures can be used throughout the acclimation process to indicate the level of adaptation reached [23].

Although it has been reported that, following heat acclimation, physiological adaptations may decay after a exposure, although there is currently no systematic evi- dence of this type of strategy being performed. Routine and regular exposure to heat during an acclimation protocol enables the athlete to experience the heat in day-to-day training sessions [17], and athletes can gradually increase passive heat exposure related to daily living as soon as possible (i.e., live hot). Greater research in this area and manipulations of time spent training and passively recov- ering in hot or cool conditions may help ascertain whether residual effects of heat exposure are retained and, once undertaken, whether and how often it should be repeated.

It is possible that to adapt to the heat optimally and in a time efficient way, short-term protocols may best utilise a combination of active acclimation and passive acclimati- sation. This could be achieved by using widely reported and effective heat tolerance training protocols in stand- ardised conditions (acclimation), but also by promoting passive effects of the heat by living in hot conditions over the short- or medium-term period (acclimatisation). Living in the heat could enable athletes to adapt to hot conditions more rapidly while facilitating training in the cooler parts of the day. It has also recently been proposed that heat training may prove a useful preparatory strategy for per- formance in cool and temperate conditions [10], and con- sequently the potential gains from STHA and MTHA could be multi-faceted. Therefore, a combined approach could prove effective and achievable in short-duration protocols (\7 days); however, new research is required to clarify the interactions between STHA and MTHA and the extent to which passive exposure to heat might be useful.
Training intensities in hot or humid conditions, cer- tainly in the short term, should not rely solely on HR or personal best times as effective markers of adaptation as these can be misleading [25]. Consequently, the use of scalar methods such as perceived exertion may be more effective in this context. Effective pacing strategies take time to establish in the heat and athletes should expect a degree of performance decrement in events of prolonged duration, especially when still acclimating. Knowing that elite athletic performance can be reduced by as much as 3 % in endurance events such as the marathon (Table 1), athletes can adjust their pacing strategies to ensure max- imum possible performance, taking into consideration their current level of acclimation, relevant ambient con- ditions (temperature and humidity) and other competitor actions. It seems likely that the shorter time spent accli- mating, the faster the acquired adaptations may diminish [8] and, therefore, it is probable that undertaking pre-event acclimation, top-up sessions, and living hot as soon as practical could facilitate athletes to compete at greater intensities in hot and humid conditions [26]. Potentially, the combination of all three strategies (heat acclimation, top-up sessions and living hot) may yield greater

improvements in performance but this premise remains to be tested and may be best suited to either individual sports or tournament-like competitions that are major features of the athletes’ season.
The adaptations underpinning maintenance of perfor- mance are likely consequent to the cumulative effect of the necessary heat adaptations for that particular individual or event. As discussed above, a 100 m runner may not require a lowered HR or Tc or other body cooling capabilities for optimal performance. It is plausible that physiological factors associated with being non-acclimated to the heat, such as peripheral vasodilation, coupled with elevated pre- race muscle temperatures may actually be beneficial in the context of sprinting performance although this is a concept rarely considered [27]. Minimising heat acclimation adaptations for these athletes could, therefore, be of benefit as it is possible that acclimation could have the opposite of the intended effect. More data are required to determine if it could be counter-productive for sprint athletes to undertake heat acclimation. It is even conceivable that sprinters may gain more from exaggerating the effects of initial heat exposure by undertaking pre-(hot)event cold acclimation to promote immediate ‘fight or flight’ style of responsiveness to the heat so as to up-regulate muscle temperature, elevate HR and Tc as a means of readiness for very short duration events [28]. It is one of the purposes of a leading article to challenge existing concepts and stim- ulate new research; it is our view that new research is required to clarify the issues we have identified.
Conclusion
Athletic performance for males and females participating in endurance events is likely to be impaired in very warm to hot environments. The opposite is the case for athletes competing in short-distance sprint events. Short-term heat acclimation programmes of \7 days provide athletes with modest thermoregulatory adaptations and performance benefits but, based on current evidence, more can be gained from medium-term ([8–14 days) acclimation periods. However, considerable recent evidence suggests STHA may be worthwhile [5] as, given the practical consider- ations of congested training and competition schedules, coaches and athletes will most likely give preference to shorter-term protocols. More efficient shorter-term accli- mation may be achieved through strategies such as manipulations of active and passive periods of heat expo- sure and top-up sessions over the adaptive period.