A Matter of Degrees: A Systematic Review of the Ergogenic Effect of Pre-Cooling in Highly Trained Athletes.

The current systematic review evaluated the effects of different pre-cooling techniques on sports performance in highly-trained athletes under high temperature conditions. PubMed/MEDLINE, EMBASE, Web of Science, CENTRAL, Scopus, and SPORTDiscus databases were searched from inception to December 2019. Studies performing pre-cooling interventions in non-acclimatized highly-trained athletes (>55 mL/kg/min of maximal oxygen consumption) under heat conditions (≥30 °C) were included. The searched reported 26 articles. Pre-cooling techniques can be external (exposure to ice water, cold packs, or cooling clothes), internal (intake of cold water or ice), or mixed. Cooling prior to exercise concluded increases in distance covered (1.5–13.1%), mean power output (0.9–6.9%), time to exhaustion (19–31.9%), work (0.1–8.5%), and mean peak torque (10.4–22.6%), as well as reductions in completion time (0.6–6.5%). Mixed strategies followed by cold water immersion seem to be the most effective techniques, being directly related with the duration of cooling and showing the major effects in prolonged exercise protocols. The present review showed that pre-cooling methods are an effective strategy to increase sports performance in hot environments. This improvement is associated with the body surface exposed and its sensibility, as well as the time of application, obtaining the best results in prolonged physical exercise protocols.


Introduction
Nowadays, sport competitions take place in a great diversity of geographical areas characterized by hot environments, such as the 2019 International Association of Athletics Federations (IAAF) World Championships in Doha, the 2020 Olympic Games in Tokyo, and the 2022 Federation International Football Association (FIFA) World Championship in Qatar. This situation constitutes a major challenge for athletic trainers and medical staff due to the impact that heat causes in athletes, mainly in endurance, racket, and team-sport disciplines. The practice of moderate/high-intensity exercise produces large amount of energy, which is eliminated as heat with an associated increase of central temperature [1]. Skin blood flow and sweat rate increments are crucial thermoregulatory mechanisms that favor heat loss [2], although when environmental conditions are extreme, these adjustments are disturbed and cannot avoid the elevation of core body temperature [3]. In this regard, hyperthermia is known main outcomes were total distance covered, power output, completion time, time to exhaustion, and work.

Quality Assessment
The quality of the studies was assessed by two researchers using the PEDro scale for this purpose [16]. This scale is based on 11 items, the first of which refers to external validity, and the remaining 10 to internal validity and the presentation of the statistical analysis. The assessment was nevertheless scored out of 10, as the first item was not taken into account for this purpose. For each item whose criterion was met, one point was awarded, whereas no points were given if the item was not fulfilled [17]. The relationship between the score and the quality of the study was on the following basis: excellent quality (9 or 10 points), good quality (6 to 8 points), fair quality (4 or 5 points), and poor quality (fewer than 4 points).

Studies Included
The search strategy retrieved 2845 records. After duplicates were removed, 1253 studies were excluded from the review process and 1525 were excluded after title and/or abstract analysis; 67 fulltext copies of the remaining studies were obtained and subjected to further evaluation. After reading full-text copies, 41 studies were excluded from this review and 26 articles meeting the eligibility criteria were included for qualitative analysis   (Figure 1).

Participant Characteristics
Overall, 240 subjects were included in the qualitative analysis. The number of participants ranged from 6 [41] to 20 [25]. All the studies assessed only men, except three which used a mix-sex

Mixed-Method Cooling vs. Non-Cooling Strategies
The combination of internal and external strategies was effective in increasing mean power output (3%) and reducing completion time (1.3-5.1%).

Inter-Group Comparisons
Those studies comparing mixed-method cooling vs. internal and/or external strategies did not conclude any significant between-group effects, although there was a trend in favor of mixed methods [31,40,43].

Quality Assessment
Regarding methodological quality, the risk of bias of the included studies is shown in Table 2. Due to their crossover design, none of the studies could conceal allocations and blind participants from the interventions. Moreover, none of them blinded therapists or assessors. Overall, the quality of the studies attained an average of 4.9 in the PEDro scale, which corresponded to a fair quality.
(1) ↑6% and 7% in favor of whole-body COOL (vs. head + hand-COOL and hand-COOL, respectively) EXT Head + hand-COOL (iced towel soaked in water at 5 • C in head and cold water immersion @ 9 • C in hands) EXT Whole-body COOL (iced towel on head and neck @ 5 • C, cold water on hands @ 9 • C, ice vest on torso and ice packs on quadriceps @ −20 • C −20 + 5 rec) EXT 10 + 5 rec of whole-body COOL (iced towel on head and neck @ 5 • C, cold water on hands @ 9 • C, ice vest on torso and ice packs on quadriceps @ −20 • C)

Discussion
Pre-cooling techniques seem to be an effective strategy to enhance sports performance in hot environments. Thus, improvements in terms of time, distance covered, work and power output, and increasing TTE have been shown after applying cooling strategies prior to acute exercise trials.
With regard to external pre-cooling, a combination of methods appears to yield better results than the use of an isolated technique. A reduced mean completion time was observed after a combination of CWI with an ice vest/jacket, compared with ice vest or jacket alone [41]. Minett et al. [27] found that 20 min of whole-body pre-cooling was more effective than head and hands cooling in intermittent sprint bouts, and even larger differences were observed compared to head refreshing alone. However, Maroni et al. [39] did not show any differences in performance when comparing a hand-cooling glove technique with a cooling jacket or a combination of both during high intensity prolonged repeated-sprint efforts in cyclists. Despite this circumstance, all techniques improved thermal sensation when they were applied in isolation. Because none of the cooling techniques assessed were able to reduce Tc values between all trials [39], this factor might play an important role in athletic performance.
The key to reducing the Tc could reside in the parts of the body exposed to cooling devices, suggesting that head and neck are more decisive than the distal parts. Neck is located near the thermoregulatory center, which receives and integrates afferent thermal inputs and coordinates the efferent response to the periphery [46]. Both neck and head present 2-5 times higher alliesthesial thermosensitivity than any other segment during moderate cooling [47] and dominate whole-body temperature perception despite constituting only a small portion of the total skin surface area [48]. In this regard, cooling the neck was observed to significantly extend TTE in untrained individuals performing a treadmill time-trial [49]. Furthermore, the distance covered increased when endurance-trained subjects were cooled prior and during a similar exercise protocol [50]. In addition to this, the specificity in the physiological assessment of performance may have a key role in these findings [51], as cricket players are more familiar with sprints [27] than cyclists, who are not used to performing repeated short-duration sprints (15 s) on a cycle-ergometer [39]. However, the hypothesis that cycling may not benefit from pre-cooling was discarded, as there are a considerable number of studies that have reported positive results using cooling devices prior to simulated cycling tests [18,19,24,25,30,37,38,40,41].
Concerning individual techniques, CWI showed the best results among the external strategies in terms of sports performance, offering significant increases in total distance covered [21,33,37], as well as reductions in completion time [38]. Although these previous results support the fact that cooling a larger body surface area improves performance to a greater extent, the application of ice packs alone on quadriceps and hamstrings also yielded significant positive effects in completion time after performing a 5000m treadmill time-trial [22]. Moreover, cooling hamstrings and quadriceps improved power and work following a sprint-based protocol on a cycle-ergometer [52], even though local cooling slows enzyme activity and nerve conduction, as well as reducing the rate of force development [53]. This reduction in contractile speed shown by the cooled muscles [54] especially affects short and intense efforts, as a consequence of its negative impact on the fast twitch fiber recruitment, essential for an optimal sprint performance [55]. Therefore, although further research is needed, it may be counterproductive to cool lower-limb muscles prior to sprint protocols, as the high pre-activation required by the hamstrings just before ground contact to produce maximum acceleration [56] could be harmed.
Furthermore, and inversely related with intense efforts, prolonged exercise alters thermal homeostasis to a greater extent than shorter exercise protocols, responding better to pre-cooling and highlighting the importance of exercise duration on its effectiveness [57]. Nonetheless, it is worth mentioning that cooling effect may be limited and tends to decrease when exercise exceeds 60 min [11], and thus including the intervention process during exercise breaks (if exist) can help to maintain its effectiveness.
Regarding internal strategies, the ingestion of ice crushed before exercising managed to reduce completion time in both a 40km time-trial [30] and in the running phase of an Olympic-distance triathlon [23], as well as increases in distance covered on a treadmill [35]. Nevertheless, the timing of ice ingestions may be important for enhancing performance. In this regard, a significantly higher TTE was observed when the rest interval between the end of the ice intake and the beginning of the exercise protocol was more prolonged (20 min vs. 5 min) [58]. These results encourage research on the most appropriate time of ingestion in relation with the beginning of the competition to enhance the ergogenic effects of this technique.
Muñoz et al. [43] noted that oral rehydration (7 • C) each 10 min before completing a 5000 m treadmill could reduce a 4.7% time in the race test, although in a non-significant manner. Despite the short duration of the test, this fact might highlight the importance of an adequate pre-hydration level on sports performance, as has been previously described in long-distance runners [59] and cyclists [60,61]. Nevertheless, the deleterious effect of hypohydration is still in doubt, as well-trained cyclists subjected to a dehydration up to −3% did not impair their performance on a 25 km time-trial in hot conditions (33 • C, 40% relative humidity (rh)) [62]. These results may be taken into account, as they have been obtained under real conditions (blinding the cyclists to their hydration status and with a facing air speed at a rate near that of field-based forward cycling speed).
As expected, when internal and external strategies are combined, the effectiveness is enhanced in comparison with the application of both separately. The intake of crushed ice ingestion was significantly more effective than CWI in terms of power output when both were combined separately with a cooling jacket [40], and adding ice slushy to a cooling jacket improved power and work values compared to the external technique alone in team sport athletes [63]. Therefore, it seems that mixed strategies are the best alternative to boost athletic performance under heat stress conditions, although further research studying practical applicability is needed to establish the most feasible techniques.
Despite all the above, this review focused on athletes non-acclimatized to heat, and thus those who perform an adaptation period before competing might not obtain further positive results after pre-cooling aid, as has already been suggested. In this regard, no beneficial effects of pre-cooling were observed in terms of performance in acclimatized amateur trained runners [64]. However, 2 weeks of acclimatization offered similar results compared with cool conditions in terms of time when trained cyclists were subjected to a prolonged time trial, whereas they showed a decrease in power output in the non-acclimatized period [65]. Accordingly, it has been concluded that crushed ice ingestion prior to exercise offered identical improvements in endurance cycling performance compared with a 12 day acclimatization training program [66], being a cost-effective, time-efficient alternative if the acclimatization is not possible. Apart from this, the individual characteristics of each athlete constitute a differential factor concerning their response to heat. The skin temperature of athletes exposed to heat raises at a slower rate, as they sweat earlier than less-trained individuals [67]. This fact has led to suggestions that the application of cooling devices before exercise does not provide any beneficial effects [12]. However, this hypothesis may depend on athletes' morphology. Larger individuals have a lower increase of body temperature, whereas subjects with higher aerobic fitness tended to accumulate more heat for the same relative exercise intensity during cycling in hot conditions, as heat production exceeds its elimination [68].

Future Directions on Heat Management in Athletes
Sport competitions are currently taking place in non-traditional hot countries, and thus the implementation of cooling techniques before, during, and after competitions will become even more important for athletes to cope with the heat. We have concluded that pre-cooling is effective in improving performance parameters in highly trained athletes. However, no solid evidence exists about the implication of cooling strategies on short and intense efforts, as we have mentioned above. Furthermore, it is also important to find the most suitable pre-cooling technique for each sports practice or specific context, as it may occur that the most effective technique in absolute terms is not the most adequate in certain circumstances. In addition, and parallel to these techniques, the development of technology as wearable biosensors capable of monitoring the thermal state and the response to physical exertion in real time will provide additional advantages to medical staff to protect the health of athletes [69,70].

Conclusions
Pre-cooling methods are an effective strategy to reduce core body temperature prior exercise sessions in heat environments. These methods boost athletic performance, generally increasing power, work, covered distance, and time to exhaustion, as well as reducing completion time. Mixed techniques (a combination of internal and external strategies) seem to be the most adequate option to enhance the benefits of this practice, closely followed by cold water immersion, highlighting the influence of the body surface exposed. Additionally, prolonged physical exercise protocols have evidenced better results from the application of pre-cooling than short bouts.

Conflicts of Interest:
The authors declare no conflict of interest.