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SYSTEMATIC REVIEW article

Front. Physiol., 13 February 2019
Sec. Exercise Physiology
This article is part of the Research Topic Towards Tokyo 2020: What will contribute to Optimal Olympic Athlete Performance? View all 29 articles

Efficacy of Heat Mitigation Strategies on Core Temperature and Endurance Exercise: A Meta-Analysis

\r\nSharifah Badriyah Alhadad,,&#x;Sharifah Badriyah Alhadad1,2,3Pearl M. S. Tan&#x;Pearl M. S. Tan4Jason K. W. Lee,,*Jason K. W. Lee2,4,5*
  • 1NUS Graduate School for Integrative Sciences and Engineering, National University of Singapore, Singapore, Singapore
  • 2Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
  • 3Saw Swee Hock School of Public Health, National University of Singapore, Singapore, Singapore
  • 4Defence Medical & Environmental Research Institute, DSO National Laboratories, Singapore, Singapore
  • 5Department of Orthopaedic Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore

Background: A majority of high profile international sporting events, including the coming 2020 Tokyo Olympics, are held in warm and humid conditions. When exercising in the heat, the rapid rise of body core temperature (Tc) often results in an impairment of exercise capacity and performance. As such, heat mitigation strategies such as aerobic fitness (AF), heat acclimation/acclimatization (HA), pre-exercise cooling (PC) and fluid ingestion (FI) can be introduced to counteract the debilitating effects of heat strain. We performed a meta-analysis to evaluate the effectiveness of these mitigation strategies using magnitude-based inferences.

Methods: A computer-based literature search was performed up to 24 July 2018 using the electronic databases: PubMed, SPORTDiscus and Google Scholar. After applying a set of inclusion and exclusion criteria, a total of 118 studies were selected for evaluation. Each study was assessed according to the intervention's ability to lower Tc before exercise, attenuate the rise of Tc during exercise, extend Tc at the end of exercise and improve endurance. Weighted averages of Hedges' g were calculated for each strategy.

Results: PC (g = 1.01) was most effective in lowering Tc before exercise, followed by HA (g = 0.72), AF (g = 0.65), and FI (g = 0.11). FI (g = 0.70) was most effective in attenuating the rate of rise of Tc, followed by HA (g = 0.35), AF (g = −0.03) and PC (g = −0.46). In extending Tc at the end of exercise, AF (g = 1.11) was most influential, followed by HA (g = −0.28), PC (g = −0.29) and FI (g = −0.50). In combination, AF (g = 0.45) was most effective at favorably altering Tc, followed by HA (g = 0.42), PC (g = 0.11) and FI (g = 0.09). AF (1.01) was also found to be most effective in improving endurance, followed by HA (0.19), FI (−0.16) and PC (−0.20).

Conclusion: AF was found to be the most effective in terms of a strategy's ability to favorably alter Tc, followed by HA, PC and lastly, FI. Interestingly, a similar ranking was observed in improving endurance, with AF being the most effective, followed by HA, FI, and PC. Knowledge gained from this meta-analysis will be useful in allowing athletes, coaches and sport scientists to make informed decisions when employing heat mitigation strategies during competitions in hot environments.

Introduction

Exercising in the heat often results in elevation in body core temperature (Tc). This is the cumulative result of more heat being produced by the working muscles than heat loss to the environment coupled with hot and/or humid environmental conditions (Berggren and Hohwu Christensen, 1950; Saltin and Hermansen, 1966). Studies have shown that an accelerated increase in Tc could impair both exercise performance (i.e. time trial) and exercise capacity (i.e., time to exhaustion) (Galloway and Maughan, 1997; Parkin et al., 1999). In ambient temperatures of 4°, 11°, 21°, and 31°C, a compromise in endurance capacity due to thermoregulatory stress was already evident at 21°C (Galloway and Maughan, 1997). Parkin et al. (1999) found that time to exhaustion was longest when cycling in ambient temperatures of 3°C (85 min), followed by 20°C (60 min) and 40°C (30 min).

Elite athletes, however, cannot avoid competing in the heat since a majority of high-profile international sporting events are often held in warm conditions. The 2008 Summer Olympics in Beijing was held in average ambient conditions of 25°C with 81% relative humidity. Similarly, the 2010 Youth Olympic Games in Singapore had temperatures reaching 31°C with relative humidity between 80 and 90%. The upcoming 2020 Olympics held in Tokyo's hot and humid summer period could potentially expose athletes to one of the most challenging environmental conditions observed in the modern history of the Olympic Games, with temperatures upwards of 35°C and above 60% relative humidity. Therefore, athletes have to learn to adapt and perform in these unfavorable environments and whenever possible, incorporate mitigation strategies to counter the negative effects of heat strain to augment performance and health.

Exercise tolerance in the heat can be affected by multiple factors such as the attainment of a critically high Tc (Gonzalez-Alonso et al., 1999b), cardiovascular insufficiency (Gonzalez-Alonso and Calbet, 2003), metabolic disturbances (Febbraio et al., 1994b, 1996; Parkin et al., 1999) and reductions in central nervous system drive to skeletal muscle (Nybo and Nielsen, 2001; Todd et al., 2005). Indeed, a high Tc represents one of the key limiting factors to exercise tolerance in the heat. The development of hyperthermia has been associated with alterations in self-pacing strategies in exercise performance trials or earlier voluntary termination during exercise capacity trials (Nielsen et al., 1993; Gonzalez-Alonso et al., 1999a,b).

In order to optimize exercise tolerance in the heat, exercising individuals often employ strategies to alter Tc. There are various ways in which this can be done, such as aerobic fitness (AF) (Nadel et al., 1974; Cheung and McLellan, 1998b), heat acclimation/acclimatization (HA) (Nielsen et al., 1993; Cotter et al., 1997), pre-exercise cooling (PC) (Gonzalez-Alonso et al., 1999a,b; Cotter et al., 2001) and fluid ingestion (FI) (Greenleaf and Castle, 1971; McConell et al., 1997). These strategies have shown to be effective in improving exercise tolerance in warm conditions through various processes that include alterations in heat dissipation ability, cardiovascular stability and adaptations and changes to the body's heat storage capacity.

Being able to objectively rank these heat mitigation strategies in order of their efficacy will be particularly useful for an athlete preparing to compete in the heat. This knowledge will also be beneficial for coaches, fitness trainers and backroom staff to discern when they consider heat mitigation in warm, humid conditions. With limited amount of time and resources, an evidence-based approach to quantify the efficacy of various heat mitigation strategies will allow selection of the most effective strategy to optimize performance and health and determine the priority in which these strategies should be employed. Furthermore, no comparison of the effect of different heat mitigation strategies have been presented using a meta-analysis thus far.

Therefore, the purpose of this review was to objectively evaluate the efficacy of various heat mitigation strategies using Hedges' g. Each study was analyzed in terms of the degree to which (i) Tc was lowered at the start of exercise; (ii) the rise of Tc is attenuated; (iii) Tc is extended at the end of exercise to safe limits (McLellan and Daanen, 2012) and (iv) endurance are improved. The weighted averages of Hedges' g (Hopkins et al., 2009) were then calculated, and the various heat mitigation strategies ranked in order of effectiveness in terms of both affecting Tc measurements and endurance.

Materials and Methods

Search Strategy

A computer-based literature search was performed using the following electronic databases: PubMed, SPORTDiscus and Google Scholar. The electronic database was searched with the following keywords: “fitness,” “training,” “heat acclimation,” “heat acclimatization,” “precooling,” “pre-cooling,” “cold water immersion,” “cold air,” “cold room,” “cold vest,” “cold jacket,” “ice vest,” “cold fluid,” “cold beverage,” “neck collar,” “neck cooling,” “ice slurry,” “ice slush,” “fluid ingestion,” “fluid intake,” “water ingestion,” “water intake,” “fluid replacement,” “rehydration,” “thermoregulation,” “core temperature,” and “heat mitigation.” Searches were systematically performed by combining the keywords and using Boolean operators “AND” and “OR” to yield the maximum outcome of relevant studies. Where applicable, we applied filters for language (English) and species (Human). In addition, a manual citation tracking of relevant studies and review articles was performed. The last day of the literature search was 24 July 2018.

Inclusion and Exclusion Criteria

Studies were screened and included if they met the following criteria: (i) they investigated the effect of a heat mitigation strategy on Tc in an exercise context; (ii) they were conducted in warm or hot ambient conditions of more than 20°C; and (iii) they included a control condition or a pre-intervention and post-intervention assessment. Studies were excluded based on the following criteria: (i) they reported the use of pharmacological agents to alter Tc due to ethical issues and dangers involved with its use; (ii) they were review articles, abstracts, case studies and editorials; (iii) they involved combined use of different methods; and (iv) they involved children or the elderly.

Data Extraction

The following data were extracted: participant characteristics, sample size, ambient conditions, exercise protocol, intervention method, exercise outcome and Tc measurements. Tc measurements included the type of Tc measure used, Tc at the beginning of exercise, rate of rise of Tc and Tc at the end of exercise. In studies where mean and standard deviation of Tc were not reported in the text, the relevant data was extracted using GetData Graph Digitiser (http://getdata-graph-digitizer.com). In the event that pertinent data were not available, the corresponding authors of the manuscripts were contacted. Studies with missing data that could not be retrieved or provided by the author were excluded from the meta-analysis.

Data Analysis

In the event that rate of rise of Tc was not provided in the study, it was calculated as the difference between the Tc at the end of exercise and Tc at the beginning of exercise divided by the time taken to complete the task. When studies only reported standard errors, standard deviations were calculated by multiplying the standard error by the square root of the sample size.

Standardized mean differences (Hedges' g) and 95% confidence intervals (CIs) were also calculated for each study. This was derived using the mean Tc differences divided by the pooled standard deviation either between the control and intervention groups or between the pre-intervention and post-intervention states. A bias-corrected formula for Hedges' g for all studies was used to correct for positive and small sample bias (Borenstein et al., 2009). Weighted average of Hedges' g for each heat mitigation strategy was calculated and presented in a forest plot. A combined weighted average of Hedges' g values across all three phases for each strategy's effect on altering Tc and on endurance was also calculated, and used as the basis for ranking. The magnitude of the Hedges' g-values were interpreted as follows: < 0.20, trivial; 0.20–0.49, small; 0.50–0.79, moderate; and ≥0.80, large.

Results

Search Results

The initial identification process yielded 5159 references and after removing duplicates and screening for title and abstract, 229 full texts were obtained. Of these, based on the assessment of study relevance and the inclusion and exclusion criteria, 118 were found to be relevant and therefore included in the analysis. The number of studies found for each heat mitigation strategy is as follows: AF (n = 22), HA (n = 35), PC (n = 42), and FI (n = 24) (Figure 1). It should be noted that AF studies may incorporate effects of HA due to the environmental conditions that the AF studies are carried out in. To separate these effects, training periods for “within subjects” AF studies included were conducted at temperatures of 30°C and below. No separation based on temperature was determined for “between subjects” studies as no training was carried out for the subjects prior to the exercise test. Characteristics of the selected studies are summarized in Tables 14.

FIGURE 1
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Figure 1. Flowchart of the study selection process.

TABLE 1
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Table 1. Summary of aerobic fitness studies.

TABLE 2
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Table 2. Summary of heat acclimation/acclimatization studies.

TABLE 3
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Table 3. Summary of pre-event cooling studies.

TABLE 4
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Table 4. Summary of fluid ingestion studies.

Effect of Heat Mitigation Strategies on Tc

PC was found to be the most effective in the lowering of Tc before exercise (Hedge's g = 1.01; 95% Confidence Intervals 0.85–1.17; Figure 2). A moderate effect on lowering of Tc before exercise was observed for HA (0.72; 0.58 to 0.86) and AF (0.65; 0.46 to 0.85) while FI (0.11; −0.08 to 0.31) only exhibited a trivial effect on lowering Tc before exercise.

FIGURE 2
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Figure 2. Forest plot of Hedges' g weighted averages of heat mitigation strategies effect on Tc at different points.

Rate of rise of Tc during exercise was most attenuated by FI (0.70; 0.46 to 0.94), followed by HA (0.35; 0.19 to 0.50). AF (−0.03; −0.24 to 0.18) showed a trivial effect on the rate of rise of Tc while PC (−0.46; −0.63 to −0.28) did not appear to be as effective in lowering the rate of rise of Tc.

AF (1.11; 0.71 to 1.51) exhibited a large effect on extending the limit of Tc at the end of exercise. However, HA (−0.28; −0.52 to −0.04), PC (−0.29; −0.44 to −0.14), and FI (−0.50; −0.74 to −0.27) did not seem as effective in extending the Tc limit at the end of exercise.

In combination, AF was found to be the most effective at favorably altering Tc (0.45; 0.32 to 0.59), followed by HA (0.42; 0.33 to 0.52), PC (0.11; 0.02 to 0.19) and FI (0.09; −0.03 to 0.13) (Figure 3).

FIGURE 3
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Figure 3. Forest plot of combined Hedges' g weighted averages of heat mitigation strategies.

In addition, AF studies included both longitudinal and cross-sectional studies. We sought to determine if there was an effect on Tc variables when comparing “between subjects” and “within subjects” studies. We found that effect sizes were comparable with “between subjects” AF studies (0.45; 0.28 to 0.61) and “within subjects” AF studies (0.38; 0.14 to 0.61). The large overlap in CIs suggest that the inclusion of both study types did not have significantly different effects on Tc variables.

Effect of Heat Mitigation Strategies on Endurance

Of the 118 articles selected and used for analysis of the strategies based on effects on Tc, 45 studies also included measurements of endurance. The number of studies for each heat mitigation strategy is as follows: AF (n = 5), HA (n = 7), PC (n = 24), and FI (n = 9).

We observed that AF was the most effective in improving endurance (1.01; 1.40 to 0.61), followed by HA (0.19; −0.16 to 0.54), FI (−0.16; −0.53 to 0.22), and PC (−0.20; −0.56 to 0.17) (Figure 4).

FIGURE 4
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Figure 4. Forest plot of Hedge's g weighted averages of heat mitigation strategies on endurance.

Discussion

This meta-analysis aimed to evaluate the efficacy of different heat mitigation strategies. Our main findings suggest that AF was most effective in altering Tc, followed by HA, PC and FI. A secondary objective was to evaluate the effect of these strategies on endurance. We observed that aerobic fitness was again the most beneficial, followed by heat acclimation/acclimatization, fluid ingestion and pre-cooling. It is noteworthy that the ranking of the effectiveness of the heat mitigation strategies on favorably altering Tc is similar to their effectiveness in improving endurance (Table 5).

TABLE 5
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Table 5. Ranking of heat mitigation strategies based on Hedges' g weighted averages.

Aerobic Fitness

Individuals with a higher aerobic fitness have been shown to have a lower pre-exercise Tc at rest (Selkirk and McLellan, 2001; Mora-Rodriguez et al., 2010). Aerobic fitness also enhances heat dissipation by lowering the threshold Tc at which both skin vasodilation and sweating occur (Nadel et al., 1974; Ichinose et al., 2009). Kuwahara et al. (2005) found that sweat rates of trained individuals were significantly higher than that of untrained individuals over a 30 min cycling exercise and that the onset of sweating occurred earlier on in the exercise as well. Higher aerobic fitness has also shown to cause an increase in skin blood flow (Fritzsche and Coyle, 2000). The combination of these two effects will lower Tc by enhancing heat dissipation during exercise in the heat. In addition, a greater aerobic fitness elicits a higher Tc attained at the end of exercise (Cheung and McLellan, 1998b; Selkirk and McLellan, 2001). This is corroborated by studies in marathon runners, where highly aerobically trained individuals were able to tolerate greater end Tc without any pathophysiological effects (Maron et al., 1977; Byrne et al., 2006). However, it should be noted that the ability to extend the limit of Tc at the end of exercise may pose as a double-edged sword, as highly motivated individuals may continue to exercise past the limits of acceptable Tc which could cause higher rates of exertional heat related illnesses occurring.

Heat Acclimation/Acclimatization

Heat acclimation/acclimatization refers to the physiological adaptations that occur as a result of prolonged, repeated exposure to heat stress (Armstrong and Maresh, 1991). It is noteworthy that the magnitude and duration of the heat acclimation/acclimatization protocols are important considerations in the development of the above physiological adaptations (Tyler et al., 2016). Previous meta-analysis and studies have shown that effects on cardiovascular efficiency and Tc may be achieved in protocols lasting less than 7 days, while thermoregulatory adaptations and improvements in endurance capacity and performance may require up to 14 days. For the benefits to be maximized, protocols longer than 2 weeks may also be considered (Armstrong and Maresh, 1991; Pandolf, 1998; Tyler et al., 2016). Heat acclimation/acclimatization has been shown to effectively reduce pre-exercise body temperature (Nielsen et al., 1993; Cotter et al., 1997). The physiological adaptations also observed include decreased heart rate (Harrison, 1985; Lorenzo and Minson, 2010), increased cardiac output (Harrison, 1985; Nielsen, 1996) and plasma volume (Mitchell et al., 1976; Lorenzo and Minson, 2010). Most significantly, cutaneous vasodilation occurs at a lower Tc threshold, together with an increase in skin blood flow (Roberts et al., 1977). The onset of sweating also occurs at a lower Tc threshold, resulting in increased sweat rates during exercise (Cotter et al., 1997; Cheung and McLellan, 1998a). Taken together, this helps to reduce the rate of rise of Tc during exercise due to increased cardiovascular efficiency and heat dissipation mechanisms.

However, for tropical natives, heat acclimatization does not lead to more efficient thermoregulation. In a study by Lee and colleagues (Lee et al., 2012), military soldiers native to a warm and humid climate were asked to undergo a 10 day heat acclimatization programme. Although there was an increase in work tolerance following acclimatization, no significant cardiovascular or thermoregulatory adaptations were found. These observations could suggest that thermoregulatory benefits of heat acclimatization are minimized in tropical natives, possibly due to the “partially acquired heat acclimatization status from living and training in a warm and humid climate” (Lee et al., 2012). Alternatively, thermoregulatory benefits from heat acclimatization may also be minimized in tropical natives due to modern behavioral adaptations such as the usage of air conditioning in living spaces and the avoidance of exercise during the hottest periods of the day that reduce the environmental heat stimulus experienced (Bain and Jay, 2011). In addition, evaporative heat loss through sweating is compromised with high relative humidity and therefore results in a higher rate of rise of Tc during exercise (Maughan et al., 2012).

It is also noteworthy that heat acclimation/acclimatization encompasses aerobic fitness as well. In most protocols, there is some form of training in the simulated laboratory settings or in the natural environmental settings. Few studies have attempted to separate the effects of heat acclimation from aerobic fitness. A study by Ravanelli et al. (2018) showed that a greater maximum skin wittedness occurred at the end of aerobic training in temperate conditions (22°C, 30% relative humidity), and this was further augmented by heat acclimation in a hot and humid condition (38°C, 65% relative humidity). This suggests that studies that include aerobic training in the heat acclimation/acclimatization protocols may have had their thermoregulatory effects augmented. However, as there have been few studies that have isolated the effects of heat acclimation/acclimatization from aerobic training or compared exertional vs. passive exposure to heat in heat acclimation/acclimatization protocols, it would be difficult to isolate the effects of heat acclimation/acclimatization from aerobic fitness.

Pre-exercise Cooling

The main intention of pre-exercise cooling is to lower Tc before exercise to extend heat storage capacity in hope to delay the onset of fatigue and in this review, we have observed pre-exercise cooling to be most effective in this aspect compared to the other heat mitigation strategies. For comprehensive reviews on pre-exercise cooling (see Marino, 2002; Quod et al., 2006; Duffield, 2008; Jones et al., 2012; Siegel and Laursen, 2012; Wegmann et al., 2012; Ross et al., 2013). The various pre-exercise cooling methods include cold water immersion (Booth et al., 1997; Kay et al., 1999), cold air exposure (Lee and Haymes, 1995; Cotter et al., 2001), cold vest (Arngrimsson et al., 2004; Bogerd et al., 2010), cold fluid ingestion (Lee et al., 2008; Byrne et al., 2011), and ice slurry ingestion (Siegel et al., 2010; Yeo et al., 2012).

Largely, the methods above have been shown to be effective in lowering Tc pre-exercise, which could consequently reduce thermal strain and therefore enhance endurance performance. Apart from lowering Tc pre-exercise, ice slurry ingestion has shown to increase Tc at the end of exercise. In both laboratory and field studies, Tc was higher at the end of exercise with ice slurry. In the laboratory study by Siegel et al. (2010) oesophageal temperature was higher by 0.31°C, and in the field study by Yeo et al. (2012), gastrointestinal temperature was higher by 0.4°C with the ingestion of ice slurry. Siegel et al. (2010) suggested that the ingestion of ice slurry may have affected thermoreceptors present causing a “physiologically meaningful reduction in brain temperature.” In addition, ice slurry ingestion may have potentially attenuated any afferent feedback that would have resulted in central reduction in muscle activation, allowing tolerance of a greater thermoregulatory load (Lee et al., 2010).

In addition, practitioners should consider the magnitude of pre-exercise cooling strategies being employed. Large volumes of ice slurry/cold water ingestion may blunt heat loss pathways by limiting sweat gland activity. This would reduce evaporative heat loss which may counteract to cause a greater heat storage and higher Tc during exercise which would be unfavorable (Ruddock et al., 2017). However, it should be noted that this potentially negative effect of ice slurry/cold water ingestion may be a greater concern in dry environments as compared to humid environments. In hot and humid environments, despite reductions in evaporative heat loss potential, actual evaporation may not be reduced, and ice slurry/cold water ingestion would still be beneficial in reducing body heat storage. This is due to the attainment of the maximum evaporation potential anyway, and any additional sweat generated would drip off the skin in hot and humid environments (Jay and Morris, 2018). Numerous studies also support the effectiveness of pre-exercise ice slurry/cold water ingestion in lowering Tc and demonstrate that this profile is continued during exercise (Lee et al., 2008; Siegel et al., 2010, 2012; Byrne et al., 2011; Yeo et al., 2012).

The effectiveness of pre-cooling as a strategy in altering Tc may be limited as it is mostly done acutely before exercise. As such, its benefit may not be able to be sustained throughout the exercise duration. To counteract this limitation, considerations can be made to consider per/mid-exercise cooling. Whilst not discussed in the present meta-analysis, previous reviews have shown that per/mid-exercise cooling may be as effective in enhancing exercise performance in hot environments (Bongers et al., 2015, 2017).

Fluid Ingestion

Fluid ingestion is a common strategy used to reduce thermoregulatory strain in the heat. Many studies have shown that when fluid is ingested during exercise, exercise capacity and performance are enhanced (Fallowfield et al., 1996; Cheung and McLellan, 1997; Marino et al., 2004). A more controversial issue is the optimal amount of fluid to be consumed during exercise. Two dominant viewpoints exist—the first is that athletes should prevent fluid loss of >2% body mass (Sawka et al., 1985; Montain and Coyle, 1992a; Sawka and Coyle, 1999; Casa et al., 2010), while the other recommends drinking ad libitum (Noakes, 1995; Beltrami et al., 2008; Lee et al., 2011) due to an increased prevalence of exercise associated hyponatremia, commonly referred to as water intoxication (Noakes, 1995). Even in warm conditions where sweat rates are high, the behavioral drive to ingest fluids could exceed the physiological sweat loss (Lee et al., 2011).

This review analyzed the effects of a (i) low fluid/ad libitum vs. high fluid intake and (ii) no fluid vs. high fluid intake on Tc. All participants began exercise in a euhydrated state. Dugas et al. (2009) found that ad libitum drinking while cycling replaces approximately 55% of fluid losses., while Daries et al. (2000) found that ad libitum drinking during a treadmill run replaces approximately 30% of fluid losses. Hence in this evaluation, a fluid intake trial replacing closest to ~45% of fluid losses was chosen to represent the low fluid/ad libitum condition. It should also be stated that the results in trials in which the control state was no fluid intake may have exaggerated the results of fluid ingestion seen in this meta-analysis. This is especially so when we consider that it is impractical during a competition event to avoid drinking. As such, future hydration studies should consider avoiding a “No fluid” control state.

Ideally, individuals should begin their exercise in a euhydrated state. This could be achieved by drinking 6 mL of water per kg body mass for 2–3 h pre-exercising in a hot environment (Racinais et al., 2015a). During exercise, fluid is largely loss through sweating. Sweat rates may vary depending on individual characteristics, environmental conditions and heat acclimation/acclimatization status (Cheuvront et al., 2007). Practitioners should therefore consider determining their sweat rate prior to exercising in a hot environment to determine the amount of rehydration or fluid intake that is necessary to reduce physiological strain and optimize performance, without increasing body weight. Considerations can also be made to include supplementation with sodium (Casa, 1999; Sawka et al., 2007) and glucose (von Duvillard et al., 2007; Burke et al., 2011).

Practical Implications

Logically, employing a combination of all the different heat mitigation strategies would be most beneficial in extending an athlete's heat storage capacity and in optimizing exercise performance in the heat. However, due to time and resource constraints, it may not be practical for athletes and coaches to employ all these strategies for competition. By knowing which heat mitigation strategy is most effective, an informed decision can be made. Strategies such as aerobic fitness and heat acclimation/acclimatization have to be conducted months and weeks respectively before competition in order to reap its benefits. On the other hand, strategies such as pre-exercise cooling and fluid ingestion can be done immediately before or during competition. Practicality and comfort should be the main focus when deciding which heat mitigation strategy to employ. For example, pre-exercise cooling methods such as cold water immersion may be effective in lowering Tc before exercise begins. However, it may be cumbersome to set up a cold water bath especially during outdoor field events. Furthermore, being immersed in a cold water bath may be an uncomfortable experience for some athletes, and may cool the muscles prior to the event and hence is not practical to be used prior to competition (Quod et al., 2006; Ross et al., 2013). It is noteworthy that there could be inter-individual differences when employing each of these heat mitigation strategies. Athletes and coaches are advised to experiment with these strategies during training before deciding on the appropriate strategy to employ during competition. Finally, the importance of the usage of heat mitigation strategies when competing in hot and humid environments cannot be stressed enough. From this meta-analysis, we have shown that aerobic fitness is the most effective heat mitigation strategy. However, this does not understate the importance of a combination of heat mitigation strategies, nor does it reflect that should an athlete be aerobically fit, other heat mitigation strategies are not necessary. In the 15th International Association of Athletics Federations (IAAF) World Championships held in Beijing (China), mean and maximal temperatures were anticipated to be 26° and 33°C respectively, with relative humidity of ~73%. Despite the expected hot and humid conditions, only 15% of athletes reported having specifically prepared for these conditions. Of these, females and athletes with previous history of exertional heat illnesses (EHI) were more likely to adopt heat mitigation strategies (Périard et al., 2017). Although <2% experienced EHI symptoms, athletes should be more aware of the potential benefits of using one or more heat mitigation strategies in the lead up to competitions in hot and humid environments. As global temperatures continue to rise, the importance of such heat mitigation strategies in enhancing performance and in reducing the likelihood of EHI cannot be understated.

Limitations

The methodology of using a meta-analysis to evaluate effectiveness of different strategies is not without limitation. Publication and language restriction bias may have affected the number of studies that could be included in the analysis. As such, care was taken to ensure to control for such biases, such as a manual tracking of review articles to ensure that studies that were relevant but that did not show up in the initial search of the databases could be included as well. The heterogeneity of the included studies was also controlled for by statistical analysis. In addition, due to the practical difficulty in blinding the participants to the heat mitigation strategy being employed, any beneficial effect arising from the placebo effect could not be eliminated.

This meta-analysis also did not include behavioral alterations that could be undertaken as a mitigation strategy against exertional heat stress. Taking regular breaks during exercise is an effective way to minimize heat strain by preventing an excessive rise of Tc and increasing exercise tolerance in the heat (Minett et al., 2011). Individuals should also avoid exercising during the hottest part of the day. Alternatively, several shorter sessions of exercise can be performed rather than having a single long session, to reduce hyperthermia, while maintaining the quality of the exercise session (Maughan and Shirreffs, 2004). When exercising in the heat, an important consideration is to ensure that the material in the clothing does not prevent the evaporation of sweat from the skin (Maughan and Shirreffs, 2004). Furthermore, black and dark-colored clothing absorb more heat and should not be worn when exercising in the heat. For a review of the thermal characteristics of clothing (see Gonzalez, 1988; Parsons, 2002). One reason for the exclusion is that there is often time pressure to complete a task or race as fast as possible and/or in certain attire that does not permit behavioral alteration during competitions. There are also few studies that looked at the effect of behavioral alterations on endurance that fulfilled our inclusion criteria, which did not allow for the calculation of an effect size to compare effectively with the other heat mitigations strategies.

Although these limitations should be accounted for, this is the first meta-analysis to compare several different heat mitigation strategies and their effects on Tc and endurance. As such, this meta-analysis could provide the information necessary to allow for more informed decision making by coaches, athletes and sports scientists during exercise in hot and/or humid environments.

Conclusion

In conclusion, aerobic fitness was found to be the most effective heat mitigation strategy, followed by heat acclimation/acclimatization, pre-exercise cooling and lastly, fluid ingestion. The similarity in ranking between the ability of each heat mitigation strategy to favorably alter Tc and affect endurance suggest that alteration of heat strain may be a key limiting factor that contributes to endurance. This analysis has practical implications for an athlete preparing for competition in the heat and also allows coaches and sport scientists to make a well-informed and objective decision when choosing which heat mitigation strategy to employ.

Author Contributions

SA and PT realized the research literature. SA, PT, and JL contributed to the writing of the manuscript.

Funding

Funds received for open access publication fees were obtained from Defence Innovative Research Program Grant No. 9015102335, Ministry of Defence, Singapore.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

Armstrong, L. E., Costill, D. L., Fink, W. J., Bassett, D., Hargreaves, M., Nishibata, I., et al. (1985). Effects of dietary sodium on body and muscle potassium content during heat acclimation. Eur. J. Appl. Physiol. Occup. Physiol. 54, 391–397.

PubMed Abstract | Google Scholar

Armstrong, L. E., and Maresh, C. M. (1991). The induction and decay of heat acclimatisation in trained athletes. Sports Med. 12, 302–312.

PubMed Abstract | Google Scholar

Armstrong, L. E., Maresh, C. M., Gabaree, C. V., Hoffman, J. R., Kavouras, S. A., Kenefick, R. W., et al. (1997). Thermal and circulatory responses during exercise: effects of hypohydration, dehydration, and water intake. J. Appl. Physiol. 82, 2028–2035. doi: 10.1152/jappl.1997.82.6.2028

PubMed Abstract | CrossRef Full Text | Google Scholar

Arngrimsson, S. A., Petitt, D. S., Stueck, M. G., Jorgensen, D. K., and Cureton, K. J. (2004). Cooling vest worn during active warm-up improves 5-km run performance in the heat. J. Appl. Physiol. 96, 1867–1874. doi: 10.1152/japplphysiol.00979.2003

PubMed Abstract | CrossRef Full Text | Google Scholar

Bain, A. R., and Jay, O. (2011). Does summer in a humid continental climate elicit an acclimatization of human thermoregulatory responses? Eur. J. Appl. Physiol. 111, 1197–1205. doi: 10.1007/s00421-010-1743-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Bardis, C. N., Kavouras, S. A., Adams, J. D., Geladas, N. D., Panagiotakos, D. B., and Sidossis, L. S. (2017). Prescribed drinking leads to better cycling performance than ad libitum drinking. Med. Sci. Sports Exerc. 49, 1244–1251. doi: 10.1249/mss.0000000000001202

PubMed Abstract | CrossRef Full Text | Google Scholar

Barr, D., Reilly, T., and Gregson, W. (2011). The impact of different cooling modalities on the physiological responses in firefighters during strenuous work performed in high environmental temperatures. Eur. J. Appl. Physiol. 111, 959–967. doi: 10.1007/s00421-010-1714-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Beaudin, A. E., Clegg, M. E., Walsh, M. L., and White, M. D. (2009). Adaptation of exercise ventilation during an actively-induced hyperthermia following passive heat acclimation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R605–R614. doi: 10.1152/ajpregu.90672.2008

PubMed Abstract | CrossRef Full Text | Google Scholar

Beltrami, F. G., Hew-Butler, T., and Noakes, T. D. (2008). Drinking policies and exercise-associated hyponatraemia: is anyone still promoting overdrinking? Br. J. Sports Med. 42:796. doi: 10.1136/bjsm.2008.047944

PubMed Abstract | CrossRef Full Text | Google Scholar

Berggren, G., and Hohwu Christensen, E. (1950). Heart rate and body temperature as indices of metabolic rate during work. Arbeitsphysiologie 14, 255–260.

PubMed Abstract | Google Scholar

Best, S., Thompson, M., Caillaud, C., Holvik, L., Fatseas, G., and Tammam, A. (2014). Exercise-heat acclimation in young and older trained cyclists. J. Sci. Med. Sport 17, 677–682. doi: 10.1016/j.jsams.2013.10.243

PubMed Abstract | CrossRef Full Text | Google Scholar

Bogerd, N., Perret, C., Bogerd, C. P., Rossi, R. M., and Daanen, H. A. (2010). The effect of pre-cooling intensity on cooling efficiency and exercise performance. J. Sports Sci. 28, 771–779. doi: 10.1080/02640411003716942

PubMed Abstract | CrossRef Full Text | Google Scholar

Bongers, C. C., Hopman, M., and Eijsvogels, T. M. (2017). Cooling interventions for athletes: an overview of effectiveness, physiological mechanisms, and practical considerations. Temperature 4, 60–78. doi: 10.1080/23328940.2016.1277003

PubMed Abstract | CrossRef Full Text | Google Scholar

Bongers, C. C. W. G., Thijssen, D. H. J., Veltmeijer, M. T. W., Hopman, M. T. E., and Eijsvogels, T. M. H. (2015). Precooling and percooling (cooling during exercise) both improve performance in the heat: a meta-analytical review. Br. J. Sports Med. 49, 377–384. doi: 10.1136/bjsports-2013-092928

PubMed Abstract | CrossRef Full Text | Google Scholar

Booth, J., Marino, F., and Ward, J. J. (1997). Improved running performance in hot humid conditions following whole body precooling. Med. Sci. Sports Exerc. 29, 943–949.

PubMed Abstract | Google Scholar

Borenstein, M., Hedges, L. V., Higgins, J. P. T., and Rothstein, H. R. (2009). Introduction to Meta-Analysis. West Sussex: John Wiley & Sons, Ltd.

PubMed Abstract | Google Scholar

Brade, C., Dawson, B., and Wallman, K. (2013). Effect of precooling and acclimation on repeat-sprint performance in heat. J. Sports Sci. 31, 779–786. doi: 10.1080/02640414.2012.750006

PubMed Abstract | CrossRef Full Text | Google Scholar

Brade, C., Dawson, B., and Wallman, K. (2014). Effects of different precooling techniques on repeat sprint ability in team sport athletes. Eur. J. Sport Sci. 14, S84–S91. doi: 10.1080/17461391.2011.651491

PubMed Abstract | CrossRef Full Text | Google Scholar

Buono, M. J., Heaney, J. H., and Canine, K. M. (1998). Acclimation to humid heat lowers resting core temperature. Am. J. Physiol. 274(5 Pt 2), R1295–R1299.

PubMed Abstract | Google Scholar

Burdon, C. A., Hoon, M. W., Johnson, N. A., Chapman, P. G., and O'Connor, H. T. (2013). The effect of ice slushy ingestion and mouthwash on thermoregulation and endurance performance in the heat. Int. J. Sport Nutr. Exerc. Metab. 23, 458–469. doi: 10.1123/ijsnem.23.5.458

PubMed Abstract | CrossRef Full Text | Google Scholar

Burk, A., Timpmann, S., Kreegipuu, K., Tamm, M., Unt, E., and Oopik, V. (2012). Effects of heat acclimation on endurance capacity and prolactin response to exercise in the heat. Eur. J. Appl. Physiol. 112, 4091–4101. doi: 10.1007/s00421-012-2371-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Burke, L. M., Hawley, J. A., Wong, S. H. S., and Jeukendrup, A. (2011). Carbohydrates for training and competiton. J. Sports Sci. 29(Supp. 1), S17–S27. doi: 10.1080/02640414.2011.585473

PubMed Abstract | CrossRef Full Text | Google Scholar

Byrne, C., Lee, J. K., Chew, S. A., Lim, C. L., and Tan, E. Y. (2006). Continuous thermoregulatory responses to mass-participation distance running in heat. Med. Sci. Sports Exerc. 38, 803–810. doi: 10.1249/01.mss.0000218134.74238.6a

PubMed Abstract | CrossRef Full Text | Google Scholar

Byrne, C., Owen, C., Cosnefroy, A., and Lee, J. K. (2011). Self-paced exercise performance in the heat after pre-exercise cold-fluid ingestion. J. Athl. Train. 46, 592–599. doi: 10.4085/1062-6050-46.6.592

PubMed Abstract | CrossRef Full Text | Google Scholar

Casa, D. J. (1999). Exercise in the Heat. II. Critical concepts in rehydration, exertional heat illnesses, and maximizing athletic performance. J. Athl. Train 34, 253–262.

PubMed Abstract | Google Scholar

Casa, D. J., Stearns, R. L., Lopez, R. M., Ganio, M. S., McDermott, B. P., Walker Yeargin, S., et al. (2010). Influence of hydration on physiological function and performance during trail running in the heat. J. Athl. Train. 45, 147–156. doi: 10.4085/1062-6050-45.2.147

PubMed Abstract | CrossRef Full Text | Google Scholar

Castle, P. C., Macdonald, A. L., Philp, A., Webborn, A., Watt, P. W., and Maxwell, N. S. (2006). Precooling leg muscle improves intermittent sprint exercise performance in hot, humid conditions. J. Appl. Physiol. 100, 1377–1384. doi: 10.1152/japplphysiol.00822.2005

PubMed Abstract | CrossRef Full Text | Google Scholar

Cheung, S. S., and McLellan, T. M. (1997). Influence of hydration status and fluid replacement on heat tolerance while wearing NBC protective clothing. Eur. J. Appl. Physiol. Occup. Physiol. 77, 139–148.

PubMed Abstract | Google Scholar

Cheung, S. S., and McLellan, T. M. (1998a). Heat acclimation, aerobic fitness, and hydration effects on tolerance during uncompensable heat stress. J. Appl. Physiol. 84, 1731–1739. doi: 10.1152/jappl.1998.84.5.1731

PubMed Abstract | CrossRef Full Text | Google Scholar

Cheung, S. S., and McLellan, T. M. (1998b). Influence of short-term aerobic training and hydration status on tolerance during uncompensable heat stress. Eur. J. Appl. Physiol. Occup. Physiol. 78, 50–58.

PubMed Abstract | Google Scholar

Cheuvront, S., Montain, S., Goodman, D. A., Blanchard, L., and Sawka, M. N. (2007). Evaluation of the limits to accurate sweat loss prediction during prolonged exercise. Eur. J. Appl. Physiol. 101, 215–224. doi: 10.1007/s00421-007-0492-x

PubMed Abstract | CrossRef Full Text | Google Scholar

Clarke, N. D., Duncan, M. J., Smith, M., and Hankey, J. (2017). Pre-cooling moderately enhances visual discrimination during exercise in the heat. J. Sports Sci. 35, 355–360. doi: 10.1080/02640414.2016.1164885

PubMed Abstract | CrossRef Full Text | Google Scholar

Coso, J. D., Estevez, E., Baquero, R. A., and Mora-Rodriguez, R. (2008). Anaerobic performance when rehydrating with water or commercially available sports drinks during prolonged exercise in the heat. Appl. Physiol. Nutr. Metabolism 33, 290–298. doi: 10.1139/H07-188

PubMed Abstract | CrossRef Full Text | Google Scholar

Cotter, J. D., Patterson, M. J., and Taylor, N. A. (1997). Sweat distribution before and after repeated heat exposure. Eur. J. Appl. Physiol. Occup. Physiol. 76, 181–186. doi: 10.1007/s004210050232

PubMed Abstract | CrossRef Full Text | Google Scholar

Cotter, J. D., Sleivert, G. G., Roberts, W. S., and Febbraio, M. A. (2001). Effect of pre-cooling, with and without thigh cooling, on strain and endurance exercise performance in the heat. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 128, 667–677. doi: 10.1016/S1095-6433(01)00273-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Cramer, M. N., Bain, A. R., and Jay, O. (2012). Local sweating on the forehead, but not forearm, is influenced by aerobic fitness independently of heat balance requirements during exercise. Exp. Physiol. 97, 572–582. doi: 10.1113/expphysiol.2011.061374

CrossRef Full Text | Google Scholar

Daries, H. N., Noakes, T. D., and Dennis, S. C. (2000). Effect of fluid intake volume on 2-h running performances in a 25 degrees C environment. Med. Sci. Sports Exerc. 32, 1783–1789. doi: 10.1097/00005768-200010000-00019

PubMed Abstract | CrossRef Full Text | Google Scholar

Dileo, T. D., Powell, J. B., Kang, H. K., Roberge, R. J., Coca, A., and Kim, J. H. (2016). Effect of short-term heat acclimation training on kinetics of lactate removal following maximal exercise. J. Sports Med. Phys. Fitness 56, 70–78. Available online at: https://www.minervamedica.it/en/journals/sports-med-physical-fitness/article.php?cod=R40Y2016N01A0070

PubMed Abstract | Google Scholar

Duffield, R. (2008). Cooling interventions for the protection and recovery of exercise performance from exercise-induced heat stress. Med. Sport Sci. 53, 89–103. doi: 10.1159/000151552

PubMed Abstract | CrossRef Full Text | Google Scholar

Duffield, R., Green, R., Castle, P., and Maxwell, N. (2010). Precooling can prevent the reduction of self-paced exercise intensity in the heat. Med. Sci. Sports Exerc. 42, 577–584. doi: 10.1249/MSS.0b013e3181b675da

PubMed Abstract | CrossRef Full Text | Google Scholar

Dugas, J. P., Oosthuizen, U., Tucker, R., and Noakes, T. D. (2009). Rates of fluid ingestion alter pacing but not thermoregulatory responses during prolonged exercise in hot and humid conditions with appropriate convective cooling. Eur. J. Appl. Physiol. 105, 69–80. doi: 10.1007/s00421-008-0876-6

CrossRef Full Text | Google Scholar

Fallowfield, J. L., Williams, C., Booth, J., Choo, B. H., and Growns, S. (1996). Effect of water ingestion on endurance capacity during prolonged running. J. Sports Sci. 14, 497–502.

PubMed Abstract | Google Scholar

Faulkner, S. H., Hupperets, M., Hodder, S. G., and Havenith, G. (2015). Conductive and evaporative precooling lowers mean skin temperature and improves time trial performance in the heat. Scand. J. Med. Sci. Sports 25, 183–189. doi: 10.1111/sms.12373

PubMed Abstract | CrossRef Full Text | Google Scholar

Febbraio, M. A., Carey, M. F., Snow, R. J., Stathis, C. G., and Hargreaves, M. (1996). Influence of elevated muscle temperature on metabolism during intense, dynamic exercise. Am. J. Physiol. 271(5 Pt 2), R1251–R1255. doi: 10.1152/ajpregu.1996.271.5.R1251

PubMed Abstract | CrossRef Full Text | Google Scholar

Febbraio, M. A., Snow, R. J., Hargreaves, M., Stathis, C. G., Martin, I. K., and Carey, M. F. (1994a). Muscle metabolism during exercise and heat stress in trained men: effect of acclimation. J. Appl. Physiol. 76, 589–597.

PubMed Abstract | Google Scholar

Febbraio, M. A., Snow, R. J., Stathis, C. G., Hargreaves, M., and Carey, M. F. (1994b). Effect of heat stress on muscle energy metabolism during exercise. J. Appl. Physiol. (1985) 77, 2827–2831. doi: 10.1152/jappl.1994.77.6.2827

PubMed Abstract | CrossRef Full Text | Google Scholar

Flouris, A., Poirier, M., Bravi, A., Wright-Beatty, H., Herry, C., Seely, A., et al. (2014). Changes in heart rate variability during the induction and decay of heat acclimation. Eur. J. Appl. Physiol. 114, 2119–2128. doi: 10.1007/s00421-014-2935-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Fritzsche, R. G., and Coyle, E. F. (2000). Cutaneous blood flow during exercise is higher in endurance-trained humans. J. Appl. Physiol. 88, 738–744. doi: 10.1152/jappl.2000.88.2.738

PubMed Abstract | CrossRef Full Text | Google Scholar

Fujii, N., Honda, Y., Ogawa, T., Tsuji, B., Kondo, N., Koga, S., et al. (2012). Short-term exercise-heat acclimation enhances skin vasodilation but not hyperthermic hyperpnea in humans exercising in a hot environment. Eur. J. Appl. Physiol. 112, 295–307. doi: 10.1007/s00421-011-1980-6

CrossRef Full Text | Google Scholar

Gagnon, D., Lynn, A. G., Binder, K., Boushel, R. C., and Kenny, G. P. (2012). Mean arterial pressure following prolonged exercise in the heat: influence of training status and fluid replacement. Scand. J. Med. Sci. Sports 22, e99–e107. doi: 10.1111/j.1600-0838.2012.01506.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Galloway, S. D., and Maughan, R. J. (1997). Effects of ambient temperature on the capacity to perform prolonged cycle exercise in man. Med. Sci. Sports Exerc. 29, 1240–1249.

PubMed Abstract | Google Scholar

Garrett, A. T., Creasy, R., Rehrer, N. J., Patterson, M. J., and Cotter, J. D. (2012). Effectiveness of short-term heat acclimation for highly trained athletes. Eur. J. Appl. Physiol. 112, 1827–1837. doi: 10.1007/s00421-011-2153-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Garrett, A. T., Goosens, N. G., Rehrer, N. J., Patterson, M. J., and Cotter, J. D. (2009). Induction and decay of short-term heat acclimation. Eur. J. Appl. Physiol. 107, 659–670. doi: 10.1007/s00421-009-1182-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Gerrett, N., Jackson, S., Yates, J., and Thomas, G. (2017). Ice slurry ingestion does not enhance self-paced intermittent exercise in the heat. Scand. J. Med. Sci. Sports 27, 1202–1212. doi: 10.1111/sms.12744

CrossRef Full Text | Google Scholar

Gibson, O. R., Mee, J. A., Tuttle, J. A., Taylor, L., Watt, P. W., and Maxwell, N. S. (2015). Isothermic and fixed intensity heat acclimation methods induce similar heat adaptation following short and long-term timescales. J. Therm. Biol. 49-50, 55–65. doi: 10.1016/j.jtherbio.2015.02.005

CrossRef Full Text | Google Scholar

Gonzalez, R. R. (1988). Biophysics of Heat Transfer and Clothing Considerations. Carmel, CA: Cooper.

Google Scholar

Gonzalez-Alonso, J., and Calbet, J. A. (2003). Reductions in systemic and skeletal muscle blood flow and oxygen delivery limit maximal aerobic capacity in humans. Circulation 107, 824–830. doi: 10.1161/01.CIR.0000049746.29175.3F

PubMed Abstract | CrossRef Full Text | Google Scholar

Gonzalez-Alonso, J., Teller, C., Andersen, S. L., Jensen, F. B., Hyldig, T., and Nielsen, B. (1999a). Influence of body tempeature on the development of fatigue during prolonged exercise in the heat. J. Appl. Physiol. 86, 1032–1039.

PubMed Abstract | Google Scholar

Gonzalez-Alonso, J., Teller, C., Andersen, S. L., Jensen, F. B., Hyldig, T., and Nielsen, B. (1999b). Influence of body temperature on the development of fatigue during prolonged exercise in the heat. J. Appl. Physiol. 86, 1032–1039. doi: 10.1152/jappl.1999.86.3.1032

PubMed Abstract | CrossRef Full Text | Google Scholar

Greenleaf, J. E., and Castle, B. L. (1971). Exercise temperature regulation in man during hypohydration and hyperhydration. J. Appl. Physiol. 30, 847–853. doi: 10.1152/jappl.1971.30.6.847

PubMed Abstract | CrossRef Full Text | Google Scholar

Hargreaves, M., Dillo, P., Angus, D., and Febbraio, M. (1996). Effect of fluid ingestion on muscle metabolism during prolonged exercise. J. Appl. Physiol. 80, 363–366.

PubMed Abstract | Google Scholar

Harrison, M. H. (1985). Effects on thermal stress and exercise on blood volume in humans. Physiol. Rev. 65, 149–209. doi: 10.1152/physrev.1985.65.1.149

PubMed Abstract | CrossRef Full Text | Google Scholar

Hasegawa, H., Takatori, T., Komura, T., and Yamasaki, M. (2006). Combined effects of pre-cooling and water ingestion on thermoregulation and physical capacity during exercise in a hot environment. J. Sports Sci. 24, 3–9. doi: 10.1080/02640410400022185

PubMed Abstract | CrossRef Full Text | Google Scholar

Ho, C., Beard, J., Farrell, P., Minson, C., and Kenney, W. (1997). Age, fitness, and regional blood flow during exercise in the heat. J. Appl. Physiol. 82, 1126–1135.

PubMed Abstract | Google Scholar

Hodge, D., Jones, D., Martinez, R., and Buono, M. J. (2013). Time course of the attenuation of sympathetic nervous activity during active heat acclimation. Auton. Neurosci. 177, 101–103. doi: 10.1016/j.autneu.2013.02.017

PubMed Abstract | CrossRef Full Text | Google Scholar

Hopkins, W. G., Marshall, S. W., Batterham, A. M., and Hanin, J. (2009). Progressive statistics for studies in sports medicine and exercise science. Med. Sci. Sports Exerc. 41, 3–13. doi: 10.1249/MSS.0b013e31818cb278

PubMed Abstract | CrossRef Full Text | Google Scholar

Horstman, D. H., and Christensen, E. (1982). Acclimatization to dry heat: active men vs. active women. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 52, 825–831. doi: 10.1152/jappl.1982.52.4.825

PubMed Abstract | CrossRef Full Text | Google Scholar

Ichinose, T., Okazaki, K., Masuki, S., Mitono, H., Chen, M., Endoh, H., et al. (2005). Ten-day endurance training attenuates the hyperosmotic suppression of cutaneous vasodilation during exercise but not sweating. J. Appl. Physiol. 99, 237–243. doi: 10.1152/japplphysiol.00813.2004

CrossRef Full Text | Google Scholar

Ichinose, T. K., Inoue, Y., Hirata, M., Shamsuddin, A. K., and Kondo, N. (2009). Enhanced heat loss responses induced by short-term endurance training in exercising women. Exp. Physiol. 94, 90–102. doi: 10.1113/expphysiol.2008.043810

PubMed Abstract | CrossRef Full Text | Google Scholar

Ikegawa, S., Kamijo, Y., Okazaki, K., Masuki, S., Okada, Y., and Nose, H. (2011). Effects of hypohydration on thermoregulation during exercise before and after 5-day aerobic training in a warm environment in young men. J. Appl. Physiol. 110, 972–980. doi: 10.1152/japplphysiol.01193.2010

PubMed Abstract | CrossRef Full Text | Google Scholar

James, C. A., Richardson, A. J., Watt, P. W., Gibson, O. R., and Maxwell, N. S. (2015). Physiological responses to incremental exercise in the heat following internal and external precooling. Scand. J. Med. Sci. Sports 25 (Suppl. 1), 190–199. doi: 10.1111/sms.12376

PubMed Abstract | CrossRef Full Text | Google Scholar

James, C. A., Richardson, A. J., Watt, P. W., Willmott, A. G. B., Gibson, O. R., and Maxwell, N. S. (2017). Short-term heat acclimation improves the determinants of endurance performance and 5-km running performance in the heat. Appl. Physiol. Nutr. Metabolism 42, 285–294. doi: 10.1139/apnm-2016-0349

PubMed Abstract | CrossRef Full Text | Google Scholar

James, C. A., Richardson, A. J., Watt, P. W., Willmott, A. G. B., Gibson, O. R., and Maxwell, N. S. (2018). Short-term heat acclimation and precooling, independently and combined, improve 5-kmtime trial performance in the heat. J. Strength Cond. Res. 32, 1366–1375. doi: 10.1519/JSC.0000000000001979

PubMed Abstract | CrossRef Full Text | Google Scholar

James, L. J., Moss, J., Henry, J., Papadopoulou, C., and Mears, S. A. (2017). Hypohydration impairs endurance performance: a blinded study. Physiol. Rep. 5:e13315. doi: 10.14814/phy2.13315

PubMed Abstract | CrossRef Full Text | Google Scholar

Jay, O., and Morris, N. B. (2018). Does cold water or ice slurry ingestion during exercise elicit a net body cooling effect in the heat? Sports Med. 48, 17–29. doi: 10.1007/s40279-017-0842-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Jones, P. R., Barton, C., Morrissey, D., Maffulli, N., and Hemmings, S. (2012). Pre-cooling for endurance exercise performance in the heat: a systematic review. BMC Med. 10:166. doi: 10.1186/1741-7015-10-166

PubMed Abstract | CrossRef Full Text | Google Scholar

Kay, D., and Marino, F. E. (2003). Failure of fluid ingestion to improve self-paced exercise performance in moderate-to-warm humid environments. J. Therm. Biol. 28, 29–34. doi: 10.1016/S0306-4565(02)00032-3

CrossRef Full Text | Google Scholar

Kay, D., Taaffe, D. R., and Marino, F. E. (1999). Whole-body pre-cooling and heat storage during self-paced cycling performance in warm humid conditions. J. Sports Sci. 17, 937–944.

PubMed Abstract | Google Scholar

Kenny, G. P., Schissler, A. R., Stapleton, J., Piamonte, M., Binder, K., Lynn, A., et al. (2011). Ice cooling vest on tolerance for exercise under uncompensable heat stress. J. Occup. Environ. Hyg. 8, 484–491. doi: 10.1080/15459624.2011.596043

PubMed Abstract | CrossRef Full Text | Google Scholar

Kobayashi, Y., Ando, Y., Okuda, N., Takaba, S., and Ohara, K. (1980). Effects of endurance training on thermoregulation in females. Med. Sci. Sports Exerc. 12, 361–364.

PubMed Abstract | Google Scholar

Kotze, H. F., van der Walt, W. H., Rogers, G. G., and Strydom, N. B. (1977). Effects of plasma ascorbic acid levels on heat acclimatization in man. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 42, 711–716. doi: 10.1152/jappl.1977.42.5.711.

PubMed Abstract | CrossRef Full Text | Google Scholar

Kuwahara, T., Inoue, Y., Taniguchi, M., Ogura, Y., Ueda, H., and Kondo, N. (2005). Effects of physical training on heat loss responses of young women to passive heating in relation to menstrual cycle. Eur. J. Appl. Physiol. 94, 376–385. doi: 10.1007/s00421-005-1329-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Lee, B. J., Clarke, N. D., Hankey, J., and Thake, C. D. (2018). Whole body precooling attenuates the extracellular HSP72, IL-6 and IL-10 responses after an acute bout of running in the heat. J. Sports Sci. 36, 414–421. doi: 10.1080/02640414.2017.1313441

PubMed Abstract | CrossRef Full Text | Google Scholar

Lee, D. T., and Haymes, E. M. (1995). Exercise duration and thermoregulatory responses after whole body precooling. J. Appl. Physiol. 79, 1971–1976. doi: 10.1152/jappl.1995.79.6.1971

PubMed Abstract | CrossRef Full Text | Google Scholar

Lee, J. K., Nio, A. Q., Ang, W. H., Johnson, C., Aziz, A. R., Lim, C. L., et al. (2011). First reported cases of exercise-associated hyponatremia in Asia. Int. J. Sports Med. 32, 297–302. doi: 10.1055/s-0030-1269929

PubMed Abstract | CrossRef Full Text | Google Scholar

Lee, J. K., Nio, A. Q., Fun, D. C., Teo, Y. S., Von Chia, E., and Lim, C. L. (2012). Effects of heat acclimatisation on work tolerance and thermoregulation in trained tropical natives. J. Therm. Biol. 37, 366–373. doi: 10.1016/j.jtherbio.2012.01.008

CrossRef Full Text | Google Scholar

Lee, J. K. W., Nio, A. Q. X., Chin Leong, L., Teo, E. Y. N., Byrne, C., and Lim, C. L. (2010). Thermoregulation, pacing and fluid balance during mass participation distance running in a warm and humid environment. Eur. J. Appl. Physiol. 109, 887–898. doi: 10.1007/s00421-010-1405-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Lee, J. K. W., Shirreffs, S. M., and Maughan, R. J. (2008). Cold drink ingestion improves exercise endurance capacity in the heat. Med. Sci. Sports Exerc. 40, 1637–1644. doi: 10.1249/MSS.0b013e318178465d

PubMed Abstract | CrossRef Full Text | Google Scholar

Lim, C. L., Pyne, D., Horn, P., Kalz, A., Saunders, P., Peake, J., et al. (2009). The effects of increased endurance training load on biomarkers of heat intolerance during intense exercise in the heat. Appl. Physiol. Nutr. Metab. 34, 616–624. doi: 10.1139/h09-021

PubMed Abstract | CrossRef Full Text | Google Scholar

Lorenzo, S., and Minson, C. T. (2010). Heat acclimation improves cutaneous vascular function and sweating in trained cyclists. J. Appl. Physiol. 109, 1736–1743. doi: 10.1152/japplphysiol.00725.2010

PubMed Abstract | CrossRef Full Text | Google Scholar

Magalhaes Fde, C., Amorim, F. T., Passos, R. L., Fonseca, M. A., Oliveira, K. P., Lima, M. R., et al. (2010). Heat and exercise acclimation increases intracellular levels of Hsp72 and inhibits exercise-induced increase in intracellular and plasma Hsp72 in humans. Cell Stress Chaperones 15, 885–895. doi: 10.1007/s12192-010-0197-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Magalhaes Fde, C., Machado-Moreira, C. A., Vimieiro-Gomes, A. C., Silami-Garcia, E., Lima, N. R., and Rodrigues, L. O. (2006). Possible biphasic sweating response during short-term heat acclimation protocol for tropical natives. J. Physiol. Anthropol. 25, 215–219. doi: 10.2114/jpa2.25.215

PubMed Abstract | CrossRef Full Text | Google Scholar

Marino, F. E. (2002). Methods, advantages, and limitations of body cooling for exercise performance. Br. J. Sports Med. 36, 89–94. doi: 10.1136/bjsm.36.2.89

PubMed Abstract | CrossRef Full Text | Google Scholar

Marino, F. E., Kay, D., and Serwach, N. (2004). Exercise time to fatigue and the critical limiting temperature: effect of hydration. J. Therm. Biol. 29, 21–29. doi: 10.1016/j.jtherbio.2003.08.008

CrossRef Full Text | Google Scholar

Maron, M. B., Wagner, J. A., and Horvath, S. M. (1977). Thermoregulatory responses during competitive marathon running. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 42, 909–914. doi: 10.1152/jappl.1977.42.6.909

PubMed Abstract | CrossRef Full Text | Google Scholar

Maughan, R., and Shirreffs, S. (2004). Exercise in the heat: challenges and opportunities. J. Sports Sci. 22, 917–927. doi: 10.1080/02640410400005909

PubMed Abstract | CrossRef Full Text | Google Scholar

Maughan, R. J., Otani, H., and Watson, P. (2012). Influence of relative humidity on prolonged exercise capacity in a warm environment. Eur. J. Appl. Physiol. 112, 2313–2321. doi: 10.1007/s00421-011-2206-7

PubMed Abstract | CrossRef Full Text | Google Scholar

McConell, G., Burge, C., Skinner, S., and Hargreaves, M. (1997). Influence of ingested fluid volume on physiological responses during prolonged exercise. Acta Physiol. Scand. 160, 149–156.

PubMed Abstract | Google Scholar

McLellan, T., and Daanen, H. (2012). “Heat strain in personal protective clothing: challenges and intervention strategies,” in Intelligent Textiles and Clothing for Ballistic and NBC Protection, eds P. Kiekens and S. Jayaraman (Dordrecht: Springer), 99–118.

Google Scholar

Merry, T. L., Ainslie, P. N., and Cotter, J. D. (2010). Effects of aerobic fitness on hypohydration-induced physiological strain and exercise impairment. Acta Physiol. 198, 179–190. doi: 10.1111/j.1748-1716.2009.02051.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Minett, G. M., Duffield, R. O. B., Marino, F. E., and Portus, M. (2011). Volume-dependent response of precooling for intermittent-sprint exercise in the heat. Med. Sci. Sports Exer. 43, 1760–1769. doi: 10.1249/MSS.0b013e318211be3e

PubMed Abstract | CrossRef Full Text | Google Scholar

Mitchell, D., Senay, L. C., Wyndham, C. H., van Rensburg, A. J., Rogers, G. G., and Strydom, N. B. (1976). Acclimatization in a hot, humid environment: energy exchange, body temperature, and sweating. J. Appl. Physiol. 40, 768–778. doi: 10.1152/jappl.1976.40.5.768

PubMed Abstract | CrossRef Full Text | Google Scholar

Montain, S. J., and Coyle, E. F. (1992a). Fluid ingestion during exercise increases skin blood flow independent of increases in blood volume. J. Appl. Physiol. 73, 903–910. doi: 10.1152/jappl.1992.73.3.903

PubMed Abstract | CrossRef Full Text | Google Scholar

Montain, S. J., and Coyle, E. F. (1992b). Influence of graded dehydration on hyperthermia and cardiovascular drift during exercise. J. Appl. Physiol. 73, 1340–1350. doi: 10.1152/jappl.1992.73.4.1340

PubMed Abstract | CrossRef Full Text | Google Scholar

Mora-Rodriguez, R., Del Coso, J., Hamouti, N., Estevez, E., and Ortega, J. F. (2010). Aerobically trained individuals have greater increases in rectal temperature than untrained ones during exercise in the heat at similar relative intensities. Eur. J. Appl. Physiol. 109, 973–981. doi: 10.1007/s00421-010-1436-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Munoz, C., Carney, K., Schick, M., Coburn, J., Becker, A., and Judelson, D. (2012). Effects of oral rehydration and external cooling on physiology, perception, and performance in hot, dry climates. Scand. J. Med. Sci. Sports 22, e115–e124. doi: 10.1111/j.1600-0838.2012.01510.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Nadel, E. R., Pandolf, K. B., Roberts, M. F., and Stolwijk, J. A. (1974). Mechanisms of thermal acclimation to exercise and heat. J. Appl. Physiol. 37, 515–520. doi: 10.1152/jappl.1974.37.4.515

PubMed Abstract | CrossRef Full Text | Google Scholar

Nielsen, B. (1996). Olympics in Atlanta: a fight against physics. Med. Sci. Sports Exerc. 28, 665–668.

PubMed Abstract | Google Scholar

Nielsen, B., Hales, J. R., Strange, S., Christensen, N. J., Warberg, J., and Saltin, B. (1993). Human circulatory and thermoregulatory adaptations with heat acclimation and exercsie in a hot, dry environment. J. Physiol. 460, 467–485.

PubMed Abstract | Google Scholar

Noakes, T. D. (1995). Dehydration during exercise: what are the real dangers? Clin. J. Sport Med. 5, 123–128.

PubMed Abstract | Google Scholar

Nybo, L., and Nielsen, B. (2001). Hyperthermia and central fatigue during prolonged exercise in the heat. J. Appl. Physiol. 91, 1055–1060. doi: 10.1152/jappl.2001.91.3.1055

CrossRef Full Text | Google Scholar

Olschewski, H., and Bruck, K. (1988). Thermoregulatory, cardiovascular, and muscular factors related to exercise after precooling. J. Appl. Physiol. 64, 803–811. doi: 10.1152/jappl.1988.64.2.803

PubMed Abstract | CrossRef Full Text | Google Scholar

Pandolf, K. B. (1998). Time course of heat acclimation and its decay. Int. J. Sports Med. 19 (Suppl. 2), S157–S160. doi: 10.1055/s-2007-971985

PubMed Abstract | CrossRef Full Text | Google Scholar

Parkin, J. M., Carey, M. F., Zhao, S., and Febbraio, M. A. (1999). Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise. J. Appl. Physiol. 86, 902–908. doi: 10.1152/jappl.1999.86.3.902

PubMed Abstract | CrossRef Full Text | Google Scholar

Parsons, K. (2002). Human Thermal Environments: The Effects of Hot, Moderate and Cold Environments on Human Health, Comfort and Performance. London: Taylor & Francis.

Patterson, M. J., Stocks, J. M., and Taylor, N. A. (2004). Humid heat acclimation does not elicit a preferential sweat redistribution toward the limbs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R512–R518. doi: 10.1152/ajpregu.00359.2003

CrossRef Full Text | Google Scholar

Periard, J. D., Caillaud, C., and Thompson, M. W. (2012). The role of aerobic fitness and exercise intensity on endurance performance in uncompensable heat stress conditions. Eur. J. Appl. Physiol. 112, 1989–1999. doi: 10.1007/s00421-011-2165-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Périard, J. D., Racinais, S., Knez, W. L., Herrera, C. P., Christian, R. J., and Girard, O. (2014). Coping with heat stress during match-play tennis: does an individualised hydration regimen enhance performance and recovery? Br. J. Sports Med. 48, 748–753. doi: 10.1136/bjsports-2013-093242

PubMed Abstract | CrossRef Full Text | Google Scholar

Périard, J. D., Racinais, S., Timpka, T., Dahlström, Ö., Spreco, A., Jacobsson, J., et al. (2017). Strategies and factors associated with preparing for competing in the heat: a cohort study at the 2015 IAAF World Athletics Championships. Br. J. Sports Med. 51, 264–270. doi: 10.1136/bjsports-2016-096579

PubMed Abstract | CrossRef Full Text | Google Scholar

Quod, M. J., Martin, D. T., and Laursen, P. B. (2006). Cooling athletes before competition in the heat: comparison of techniques and practical considerations. Sports Med. 36, 671–682. doi: 10.2165/00007256-200636080-00004

PubMed Abstract | CrossRef Full Text | Google Scholar

Quod, M. J., Martin, D. T., Laursen, P. B., Gardner, A. S., Halson, S. L., Marino, F. E., et al. (2008). Practical precooling: Effect on cycling time trial performance in warm conditions. J. Sports Sci. 26, 1477–1487. doi: 10.1080/02640410802298268

PubMed Abstract | CrossRef Full Text | Google Scholar

Racinais, S., Alonso, J. M., Coutts, A. J., Flouris, A. D., Girard, O., Gonzalez-Alonso, J., et al. (2015a). Consensus recommendations on training and competing in the heat. Br. J. Sports Med. 49, 1164–1173. doi: 10.1136/bjsports-2015-094915

PubMed Abstract | CrossRef Full Text | Google Scholar

Racinais, S., Mohr, M., Buchheit, M., Voss, S. C., Gaoua, N., Grantham, J., et al. (2012). Individual responses to short-term heat acclimatisation as predictors of football performance in a hot, dry environment. Br. J. Sports Med. 46, 810–815. doi: 10.1136/bjsports-2012-091227

PubMed Abstract | CrossRef Full Text | Google Scholar

Racinais, S., Periard, J. D., Karlsen, A., and Nybo, L. (2015b). Effect of heat and heat acclimatization on cycling time trial performance and pacing. Med. Sci. Sports Exerc. 47, 601–606. doi: 10.1249/mss.0000000000000428

PubMed Abstract | CrossRef Full Text | Google Scholar

Ravanelli, N., Coombs, G. B., Imbeault, P., and Jay, O. (2018). Maximum skin wettedness after aerobic training with and without heat acclimation. Med. Sci. Sports Exerc. 50, 299–307. doi: 10.1249/mss.0000000000001439

PubMed Abstract | CrossRef Full Text | Google Scholar

Roberts, M. F., Wenger, C. B., Stolwijk, J. A., and Nadel, E. R. (1977). Skin blood flow and sweating changes following exercise training and heat acclimation. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 43, 133–137. doi: 10.1152/jappl.1977.43.1.133

PubMed Abstract | CrossRef Full Text | Google Scholar

Robinson, T. A., Hawley, J. A., Palmer, G. S., Wilson, G. R., Gray, D. A., Noakes, T. D., et al. (1995). Water ingestion does not improve 1-h cycling performance in moderate ambient temperatures. Eur. J. Appl. Physiol. Occup. Physiol. 71, 153–160.

Google Scholar

Ross, M., Abbiss, C., Laursen, P., Martin, D., and Burke, L. (2013). Precooling methods and their effects on athletic performance. Sports Med. 43, 207–225. doi: 10.1007/s40279-012-0014-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Ruddock, A., Robbins, B., Tew, G., Bourke, L., and Purvis, A. (2017). Practical cooling strategies during continuous exercise in hot environments: a systematic review and meta-analysis. Sports Med. 47, 517–532. doi: 10.1007/s40279-016-0592-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Saat, M., Sirisinghe, R. G., Singh, R., and Tochihara, Y. (2005). Effects of short-term exercise in the heat on thermoregulation, blood parameters, sweat secretion and sweat composition of tropic-dwelling subjects. J. Physiol. Anthropol. Appl. Hum. Sci. 24, 541–549. doi: 10.2114/jpa.24.541

PubMed Abstract | CrossRef Full Text | Google Scholar

Saltin, B., and Hermansen, L. (1966). Esophageal, rectal, and muscle temperature during exercise. J. Appl. Physiol. 21, 1757–1762. doi: 10.1152/jappl.1966.21.6.1757

PubMed Abstract | CrossRef Full Text | Google Scholar

Sawka, M. N., Burke, L. M., Eichner, E. R., Maughan, R. J., Montain, S. J., and Stachenfeld, N. S. (2007). American College of Sports Medicine position stand. Exercise and fluid replacement. Med. Sci. Sports Exerc. 39, 377–390. doi: 10.1249/mss.0b013e31802ca597

PubMed Abstract | CrossRef Full Text | Google Scholar

Sawka, M. N., and Coyle, E. F. (1999). Influence of body water and blood volume on thermoregulation and exercise performance in the heat. Exerc. Sport Sci. Rev. 27, 167–218.

PubMed Abstract | Google Scholar

Sawka, M. N., Young, A. J., Francesconi, R. P., Muza, S. R., and Pandolf, K. B. (1985). Thermoregulatory and blood responses during exercise at graded hypohydration levels. J. Appl. Physiol. 59, 1394–1401. doi: 10.1152/jappl.1985.59.5.1394

PubMed Abstract | CrossRef Full Text | Google Scholar

Selkirk, G. A., and McLellan, T. M. (2001). Influence of aerobic fitness and body fatness on tolerance to uncompensable heat stress. J. Appl. Physiol. 91, 2055–2063. doi: 10.1152/jappl.2001.91.5.2055

PubMed Abstract | CrossRef Full Text | Google Scholar

Shields, C. L., Giesbrecht, G. G., Pierce, G. N., and Ready, A. E. (2004). The effects of a moderate physical activity program on thermoregulatory responses in a warm environment in men. Can. J. Appl. Physiol. 29, 379–394. doi: 10.1139/h04-024

PubMed Abstract | CrossRef Full Text | Google Scholar

Shvartz, E., Magazanik, A., and Glick, Z. (1974). Thermal responses during training in a temperate climate. J. Appl. Physiol. 36, 572–576. doi: 10.1152/jappl.1974.36.5.572

PubMed Abstract | CrossRef Full Text | Google Scholar

Shvartz, E., Shapiro, Y., Magazanik, A., Meroz, A., Birnfeld, H., Mechtinger, A., et al. (1977). Heat acclimation, physical fitness, and responses to exercise in temperate and hot environments. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 43, 678–683. doi: 10.1152/jappl.1977.43.4.678

PubMed Abstract | CrossRef Full Text | Google Scholar

Siegel, R., and Laursen, P. B. (2012). Keeping your cool: possible mechanisms for enhanced exercise performance in the heat with internal cooling methods. Sports Med. 42, 89–98. doi: 10.2165/11596870-000000000-00000

PubMed Abstract | CrossRef Full Text | Google Scholar

Siegel, R., Maté, J., Brearley, M. B., Watson, G., Nosaka, K., and Laursen, P. B. (2010). Ice slurry ingestion increases core temperature capacity and running time in the heat. Med. Sci. Sports Exerc. 42, 717–725. doi: 10.1249/MSS.0b013e3181bf257a

PubMed Abstract | CrossRef Full Text | Google Scholar

Siegel, R., Maté, J., Watson, G., Nosaka, K., and Laursen, P. B. (2012). Pre-cooling with ice slurry ingestion leads to similar run times to exhaustion in the heat as cold water immersion. J. Sports Sci. 30, 155–165. doi: 10.1080/02640414.2011.625968

PubMed Abstract | CrossRef Full Text | Google Scholar

Skein, M., Duffield, R., Cannon, J., and Marino, F. (2012). Self-paced intermittent-sprint performance and pacing strategies following respective pre-cooling and heating. Eur. J. Appl. Physiol. 112, 253–266. doi: 10.1007/s00421-011-1972-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Smith, D. L., Fehling, P. C., Hultquist, E. M., Arena, L., Lefferts, W. K., Haller, J. M., et al. (2013). The effect of precooling on cardiovascular and metabolic strain during incremental exercise. Appl. Physiol. Nutr. Metab. 38, 935–940. doi: 10.1139/apnm-2012-0489

PubMed Abstract | CrossRef Full Text | Google Scholar

Smoljanic, J., Morris, N. B., Dervis, S., and Jay, O. (2014). Running economy, not aerobic fitness, independently alters thermoregulatory responses during treadmill running. J. Appl. Physiol. 117, 1451–1459. doi: 10.1152/japplphysiol.00665.2014

CrossRef Full Text | Google Scholar

Stanley, J., Leveritt, M., and Peake, J. M. (2010). Thermoregulatory responses to ice-slush beverage ingestion and exercise in the heat. Eur. J. Appl. Physiol. 110, 1163–1173. doi: 10.1007/s00421-010-1607-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Stannard, A. B., Brandenburg, J. P., Pitney, W. A., and Lukaszuk, J. M. (2011). Effects of wearing a cooling vest during the warm-up on 10-km run performance. J. Strength Cond. Res. 25, 2018–2024. doi: 10.1519/JSC.0b013e3181e07585

PubMed Abstract | CrossRef Full Text | Google Scholar

Stapleton, J., Gagnon, D., and Kenny, G. P. (2010). Short-term exercise training does not improve whole-body heat loss when rate of metabolic heat production is considered. Eur. J. Appl. Physiol. 109, 437–446. doi: 10.1007/s00421-010-1380-3

CrossRef Full Text | Google Scholar

Stevens, C. J., Kittel, A., Sculley, D. V., Callister, R., Taylor, L., and Dascombe, B. J. (2017). Running performance in the heat is improved by similar magnitude with pre-exercise cold-water immersion and mid-exercise facial water spray. J. Sports Sci. 35, 798–805. doi: 10.1080/02640414.2016.1192294

PubMed Abstract | CrossRef Full Text | Google Scholar

Stevens, C. J., Thoseby, B., Sculley, D. V., Callister, R., Taylor, L., and Dascombe, B. J. (2016). Running performance and thermal sensation in the heat are improved with menthol mouth rinse but not ice slurry ingestion. Scand. J. Med. Sci. Sports 26, 1209–1216. doi: 10.1111/sms.12555

CrossRef Full Text | Google Scholar

Takeno, Y., Kamijo, Y. I., and Nose, H. (2001). Thermoregulatory and aerobic changes after endurance training in a hypobaric hypoxic and warm environment. J. Appl. Physiol. 91, 1520–1528. doi: 10.1152/jappl.2001.91.4.1520

PubMed Abstract | CrossRef Full Text | Google Scholar

Takeshima, K., Onitsuka, S., Xinyan, Z., and Hasegawa, H. (2017). Effect of the timing of ice slurry ingestion for precooling on endurance exercise capacity in a warm environment. J. Therm. Biol. 65, 26–31. doi: 10.1016/j.jtherbio.2017.01.010

PubMed Abstract | CrossRef Full Text | Google Scholar

Todd, G., Butler, J. E., Taylor, J. L., and Gandevia, S. (2005). Hyperthermia: a failure of the motor cortex and the muscle. J. Physiol. 563(Pt 2), 621–631. doi: 10.1113/jphysiol.2004.077115

PubMed Abstract | CrossRef Full Text | Google Scholar

Trangmar, S. J., Chiesa, S. T., Llodio, I., Garcia, B., Kalsi, K. K., Secher, N. H., et al. (2015). Dehydration accelerates reductions in cerebral blood flow during prolonged exercise in the heat without compromising brain metabolism. Am. J. Physiol. Heart Circ. Physiol. 309, H1598–H1607. doi: 10.1152/ajpheart.00525.2015

PubMed Abstract | CrossRef Full Text | Google Scholar

Tsuji, B., Honda, Y., Fujii, N., Kondo, N., and Nishiyasu, T. (2012). Effect of initial core temperature on hyperthermic hyperventilation during prolonged submaximal exercise in the heat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R94–R102. doi: 10.1152/ajpregu.00048.2011

PubMed Abstract | CrossRef Full Text | Google Scholar

Tyler, C. J., Reeve, T., Hodges, G. J., and Cheung, S. S. (2016). The effects of heat adaptation on physiology, perception and exercise performance in the heat: a meta-analysis. Sports Med. 46, 1699–1724. doi: 10.1007/s40279-016-0538-5

CrossRef Full Text | Google Scholar

von Duvillard, S. P., Braun, W. A., Markofski, M., Beneke, R., and Leithäuser, R. (2007). Fluids and hydration in prolonged endurance performance. Nutrition 20, 651–656. doi: 10.1016/j.nut.2004.04.011

PubMed Abstract | CrossRef Full Text | Google Scholar

Wall, B. A., Watson, G., Peiffer, J. J., Abbiss, C. R., Siegel, R., and Laursen, P. B. (2015). Current hydration guidelines are erroneous: dehydration does not impair exercise performance in the heat. Br. J. Sports Med. 49, 1077–1083. doi: 10.1136/bjsports-2013-092417

CrossRef Full Text | Google Scholar

Watkins, A. M., Cheek, D. J., Harvey, A. E., Blair, K. E., and Mitchell, J. B. (2008). Heat acclimation and HSP-72 expression in exercising humans. Int. J. Sports Med. 29, 269–276. doi: 10.1055/s-2007-965331

PubMed Abstract | CrossRef Full Text | Google Scholar

Wegmann, M., Faude, O., Poppendieck, W., Hecksteden, A., Frohlich, M., and Meyer, T. (2012). Pre-cooling and sports performance: a meta-analytical review. Sports Med. 42, 545–564. doi: 10.2165/11630550-000000000-00000

PubMed Abstract | CrossRef Full Text | Google Scholar

Weller, A. S., Linnane, D. M., Jonkman, A. G., and Daanen, H. A. (2007). Quantification of the decay and re-induction of heat acclimation in dry-heat following 12 and 26 days without exposure to heat stress. Eur. J. Appl. Physiol. 102, 57–66. doi: 10.1007/s00421-007-0563-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Willmott, A. G., Gibson, O. R., Hayes, M., and Maxwell, N. S. (2016). The effects of single versus twice daily short term heat acclimation on heat strain and 3000m running performance in hot, humid conditions. J. Therm. Biol. 56, 59–67. doi: 10.1016/j.jtherbio.2016.01.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Wilson, T. E., Johnson, S. C., Petajan, J. H., Davis, S. L., Gappmaier, E., Luetkemeier, M. J., et al. (2002). Thermal regulatory responses to submaximal cycling following lower-body cooling in humans. Eur. J. Appl. Physiol. 88, 67–75. doi: 10.1007/s00421-002-0696-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Wittbrodt, M. T., Millard-Stafford, M., Sherman, R. A., and Cheatham, C. C. (2015). Fluid replacement attenuates physiological strain resulting from mild hypohydration without impacting cognitive performance. Int. J. Sport Nutr. Exerc. Metabolism 25, 439–447. doi: 10.1123/ijsnem.2014-0173

PubMed Abstract | CrossRef Full Text | Google Scholar

Wright, H. E., Selkirk, G. A., Rhind, S. G., and McLellan, T. M. (2012). Peripheral markers of central fatigue in trained and untrained during uncompensable heat stress. Eur. J. Appl. Physiol. 112, 1047–1057. doi: 10.1007/s00421-011-2049-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Yamauchi, M., Matsumoto, T., Ohwatari, N., and Kosaka, M. (1997). Sweating economy by graded control in well-trained athletes. Pflug. Arch. 433, 675–678. doi: 10.1007/s004240050331

PubMed Abstract | CrossRef Full Text | Google Scholar

Yamazaki, F., Fujii, N., Sone, R., and Ikegami, H. (1994). Mechanisms of potentiation in sweating induced by long-term physical training. Eur. J. Appl. Physiol. Occup. Physiol. 69, 228–232.

PubMed Abstract | Google Scholar

Yeargin, S. W., Casa, D. J., Armstrong, L. E., Watson, G., Judelson, D. A., Psathas, E., et al. (2006). Heat acclimatization and hydration status of American football players during initial summer workouts. J. Strength Cond. Res. 20, 463–470. doi: 10.1519/20596.1

PubMed Abstract | CrossRef Full Text | Google Scholar

Yeo, Z. W., Fan, P. W., Nio, A. Q., Byrne, C., and Lee, J. K. (2012). Ice slurry on outdoor running performance in heat. Int. J. Sports Med. 33, 859–866. doi: 10.1055/s-0032-1304643

PubMed Abstract | CrossRef Full Text | Google Scholar

Zimmermann, M., Landers, G., Wallman, K., and Kent, G. (2018). Precooling with crushed ice: as effective as heat acclimation at improving cycling time-trial performance in the heat. Int. J. Sports Physiol. Perform. 13, 228–234. doi: 10.1123/ijspp.2016-0766

PubMed Abstract | CrossRef Full Text | Google Scholar

Zimmermann, M., Landers, G., Wallman, K. E., and Saldaris, J. (2017a). The effects of crushed ice ingestion prior to steady state exercise in the heat. Int. J. Sport Nutr. Exerc. Metabolism 27, 120–127. doi: 10.1123/ijsnem.2016-0215

PubMed Abstract | CrossRef Full Text | Google Scholar

Zimmermann, M., Landers, G. J., and Wallman, K. E. (2017b). Crushed ice ingestion does not improve female cycling time trial performance in the heat. Int. J. Sport Nutr. Exerc. Metab. 27, 67–75. doi: 10.1123/ijsnem.2016-0028

PubMed Abstract | CrossRef Full Text | Google Scholar

Zimmermann, M. R., and Landers, G. J. (2015). The effect of ice ingestion on female athletes performing intermittent exercise in hot conditions. Eur. J. Sport Sci. 15, 407–413. doi: 10.1080/17461391.2014.965751

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: thermoregulation, aerobic fitness, heat acclimation, heat acclimatization, pre-exercise cooling, fluid ingestion

Citation: Alhadad SB, Tan PMS and Lee JKW (2019) Efficacy of Heat Mitigation Strategies on Core Temperature and Endurance Exercise: A Meta-Analysis. Front. Physiol. 10:71. doi: 10.3389/fphys.2019.00071

Received: 03 November 2018; Accepted: 21 January 2019;
Published: 13 February 2019.

Edited by:

Toby Mündel, Massey University, New Zealand

Reviewed by:

Tatsuro Amano, Niigata University, Japan
Oliver R. Gibson, Brunel University London, United Kingdom

Copyright © 2019 Alhadad, Tan and Lee. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Jason K. W. Lee, phsjlkw@nus.edu.sg

These authors have contributed equally to this work

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.