Journal Logo

BASIC SCIENCES: Special Report

Markers of Muscle Damage and Performance Recovery after Exercise in the Heat


Author Information
Medicine & Science in Sports & Exercise: May 2013 - Volume 45 - Issue 5 - p 860-868
doi: 10.1249/MSS.0b013e31827ded04
  • Free


Heat-related illnesses are a major concern for organizers of endurance events, and excessively high core and muscle temperatures have been considered as potential risk factors for the exercising athlete (31). The large number of “unsuccessful starters” and medical encounters when marathons are held in hot environment signifies the potential risk of competing in the heat (10,36). For marathon races, it has been considered to include a “do not start temperature,” and the international football organization (Fédération Internationale de Football Association [FIFA]) recommend that soccer matches include additional breaks if the environmental settings are likely to cause profound hyperthermia (9,37). However, exercise and competitive sports are conducted all over the world, and several major summer events such as Olympics, FIFA world cups, and prestigious tennis tournaments are conducted in conditions with marked heat stress. It is therefore relevant and of importance to address the physiological consequences of competing in the heat.

Extreme environmental heat stress potentially provokes profound homeostatic disturbances of the athletes electrolyte, water, and temperature balance (12) and induces cardiovascular stress, including reductions in the cerebral perfusion (27), muscle blood flow, and cardiac output (13,29), and it accelerates muscle glycogen metabolism (11,39). In laboratory settings with air temperatures of 30°C–40°C, both intermittent and continuous exercise performance is clearly impaired (13,24,28). However, it appears that trained subjects can exercise to volitional exhaustion without jeopardizing health, and they are able to maintain performance in the heat during consecutive days of controlled submaximal exercise (25). However, in many competitive sport disciplines, prolonged intermittent exercise is conjoined with multiple sprints in an irregular mode. To this point, it is not known how trained athletes recover after such exercise in very hot environments and how competitive exercise in the heat affects muscle fiber damage. Sports with multiple intense actions such as football (soccer) is of special interest because even at normal environmental temperatures (<20°C), the competing athlete can reach high muscle temperatures (20), and the intense nature of the game with frequent sprints, turns, accelerations, and deceleration is associated with marked elevations of markers of muscle damage (18,22). Subsequently, this results in an impaired ability to restore muscle glycogen after competitions (14,17,18). Thus, very high levels of myoglobin and creatine kinase have been reported after a competitive game (18), and because hyperthermia may aggravate or in itself induce rhabdomyolysis (15), it could be speculated that a competitive match in the heat would be of potential risk and influence the requirement for recovery.

To address the abovementioned issues, we evaluated functional performance, hematological markers of muscle damage, and muscle glycogen responses immediately after and for the subsequent 48-h recovery period after a soccer match that was completed in 43°C hot environment (HOT) and compared these responses to those of a match played in a 21°C environment (CON) on an indoor football pitch with a similar setup. Furthermore, responses after the two matches were compared with baseline values measured in a condition with no prior exercise or competition. Creatine kinase and myoglobin were measured as plasma and sera markers, indicating muscle damage and potential rhabdomyolysis (7), whereas muscle glycogen recovery was used as an indicator of muscle metabolic homeostasis. Functional performance was evaluated via repeated sprint tests, neuromuscular testing, and intermittent endurance test.



In total, 22 soccer players took part in each game; however, two subjects were injured before the first match and did not participate in either of the games (they were substituted by local players where we did not obtain blood samples or evaluate recovery), and one subject was injured during a non–soccer-related activity between the two matches and therefore not able to play in match two. Hence, only data from the 17 outfield players that completed full time in both games are reported. These 17 subjects were trained elite male soccer players (age = 27 ± 1 yr, height = 184 ± 1 cm, body mass = 80.1 ± 1.6 kg) and all north European residents. All subjects were informed of potential risks and discomforts associated with the experiments before giving their written consent to participate. None of the participants used muscle building precursors such as creatine or ingested any special recovery drinks during the study. The study was conducted in accordance with the code of Ethics of the World Medical Association (Declaration of Helsinki) and was approved by the research committee from Aspetar, Qatar Orthopaedic and Sports Medicine Hospital.

Experimental Design

Participants were tested for physiological performance, and we obtained muscle and blood samples in a baseline condition (baseline) at least 3 d after any competitive activity and with no physical activity for the last 24 h before testing. Furthermore, tests were completed, and muscle and blood samples were obtained immediately after and 24 and 48 h after competitive soccer matches with or without environmental heat stress. The two experimental games were separated by 6 d and played on artificial grass (Classic series, Mondo, Italia) on two football pitches with similar dimensions. The control match took place at an environmental temperature of 21°C in an air-conditioned indoor facility (CON, 55% RH; wet bulb globe temperature, 18.8°C; Aspire Dome, Doha, Qatar), whereas the second game was played 6 d later outside at an environmental temperature of 43°C (HOT, 12% RH; wet bulb globe temperature, 34.9°C; Aspire Field, Doha, Qatar). The matches were friendly games but with a competitive setup, international FIFA referees, and a (minor) reward to the winning team to secure maximal “competitive” effort by all players. The study was completed in the middle of the competitive season, and all players participated in a normal competitive game (in their regular clubs—with weekly games played at an environmental temperature between 15°C and 20°C for the last 2 months before the study) 5–6 d before the control match. Therefore, the recovery interval before the control match was comparable with the period between the two experimental games. Except for the short test sessions (described in the next section), training during the 48 h after each match was light (similar intensity as indicated by the heart rate response ∼60% of the players maximal HR) and with a fixed duration of 45 min. These sessions as well as the remaining 4 d before the hot match were conducted outside to allow players to get used to the environment and acclimatize to the heat. The subjects were provided with similar diets before each of the two trials/conditions and for 48 h after the two matches. This was carbohydrate-rich diets (meals, snacks, and ad libitum buffets) that aimed at providing the subjects with ∼60 E% from carbohydrates, 15–20 E% from protein, and 20–25 E% from dietary fats.

During the two matches, the movement patterns of all 17 outfield players were observed by three stable, synchronized cameras positioned at a height of 10 m above the pitch and sampled data at a frequency of 25 Hz. Signals and angles obtained by the encoders were sequentially converted into digital data and recorded on a computer for postmatch analyses. From the stored data, the total distance covered was determined by a multiple-camera semiautomatic tracking system (version 1.0.2; Amisco Pro®, Nice, France).

Core temperature responses during the matches were monitored via wireless ingestible thermometer pills (VitalSense, precision 0.01°C; Mini Mitter, Respironics, Herrsching, Germany) swallowed early morning, before breakfast, to maximize the transit time before the experimental games. Heart rate was recorded throughout the games (Polar Team system 2; Polar Electro, Kempele, Finland), and the average heart rate was determined. Changes in body weight were determined by weighing the subjects’ prematch and postmatch. The players were supplied with pure water at the sidelines with ad libitum intake during the games, but no artificial breaks were provided. The intake was registered, and the total volume of ingested water was calculated for each player. The physiological responses and detailed analysis of running patterns during the matches have been reported by Mohr et al. (23) and only briefly presented for background information as the focus of the present article is related to the recovery aspects.

Performance Tests

Repeated sprinting.

The subjects underwent repeated sprint tests consisting of three 30-m sprint interspersed with 25 s of active recovery (20). In all conditions (baseline, ∼5 min after termination of the soccer matches, and 24 and 48 h after the two matches), the sprint test was performed in a temperate environment (∼20°C) on an indoor track. At baseline and at 24 and 48 h postmatch, the sprint test was preceded by 15 min of active warm-up at light to moderate intensity. Each sprint was initiated from a standing position with the arms raised to chest height 20 cm behind the photocell gate, which started a digital timer. Sprint times were determined using photocell gates placed 1 m above ground level (Polifemo Radio Light, Micro Gate, Bolzano, Italy). The cumulated sprint time was calculated as the index of players’ performance.

Neuromuscular testing.

Muscle function was assessed indoors (∼20°C), after the repeated sprint test (i.e., at baseline, ∼30 min after termination of the matches, and 24 and 48 h after the two matches). Neuromuscular test sessions began by eliciting three twitches by electrical stimulation of the tibial nerve at rest separated by 5 s. Thereafter, subjects were instructed to perform three isometric maximal voluntary contractions (MVC) of the plantar flexors, all brief (5 s) and separated by 30 s of rest, with a twitch delivered over the isometric plateau (control twitch) and 4 s after each MVC (potentiated twitch). For all brief MVC trials, participants were carefully instructed to contract as hard and fast as possible from a fully relaxed state. Strong verbal encouragement was given to the subjects during each maximal effort. At baseline 24 and 48 h postmatch, subjects carried out a warm-up, which consisted of ten isometric plantarflexions (alternating 4 s of contraction and 6 s of rest). Stimulations (400 V, rectangular pulse of 0.2 ms) were delivered by a high-voltage stimulator (Digitimer DS7AH; Digitimer, Hertfordshire, UK) via a cathode electrode (diameter of 9 mm) placed in the popliteal cavity and an anode (5 × 10 cm) positioned beneath the patella. The intensity of stimulation was determined before the baseline test session using a passive isometric recruitment curve. Briefly, the stimulation intensity was increased by 10-mA increments until a maximal peak twitch torque was achieved and then a further increased by 50% to ensure a constant supramaximal stimulation throughout the protocol (mean ± SE = 85 ± 22 mA, range = 48–120 mA).

The subject’s seating position was standardized with pelvis, knee, and ankle angulations of 90°, the right foot securely strapped on the pedal by three straps, and a motionless head. The torque was measured using a dynamometric pedal (Captels, St. Mathieu de Treviers, France). The EMG activity of the soleus muscle was recorded via bipolar Ag/AgCl electrodes (Ambu Blue sensor T, Ambu A/S, Denmark) with a diameter of 9 mm and an interelectrode distance of 3 cm fixed lengthwise over the muscle belly. The reference electrode was attached to the left wrist. Low impedance between the two electrodes was obtained by abrading the skin with emery paper and cleaning with alcohol. EMG signals were amplified (gain = 1000), filtered (bandwidth frequency = 30–500 Hz), and recorded (sampling frequency = 2000 Hz) by a commercially available hardware (Biopac MP35; Biopac Systems Inc., Santa Barbara, CA) and its dedicated software (Acknowledge 3.6.7; Biopac Systems Inc.).

The MVC torque was defined as the maximum value recorded for 1 s, and the root mean square (RMS) of the EMG activity was computed during the same 1 s. The voluntary activation (VA) level was estimated as VA (%) = [(1 − (superimposed twitch / potentiated twitch)] × 100). Furthermore, the rate of torque development and soleus EMG rise were derived as the average slopes of the torque time and EMG RMS time, respectively, at 0–200 ms relative to the onset of contraction and normalized relative to maximal MVC torque (%MVC·s−1) and maximal EMG activity (%RMS·s−1) values (1,40). The onset of EMG integration was shifted 50 ms before the onset of contraction to account for the presence of electromechanical delay. The peak twitch torque was determined from the mechanical response of the evoked potential. The mean over three trials was used for subsequent analysis for each parameter.

Intermittent endurance test.

At baseline and 48 h after the two matches (in the two latter conditions after a brief recovery from the repeated sprint tests), the players completed an interval endurance test (Yo-Yo IR1, intermittent recovery test level 1 [16]). The Yo-Yo intermittent recovery test consists of repeated 2 × 20-m runs back and forth between the starting, turning, and finishing line at a progressively increasing speed. Between each running bout, the subjects have a 10-s active rest period. The test was terminated the second time the subjects failed to reach the finishing line in time, and the distance covered was recorded as the overall test result. All players were familiar with this test, and the baseline and the 48-h postmatch tests were completed under similar conditions (indoor, ∼20°C). Yo-Yo IR1 tests were not performed immediately, or 24-h postmatches as this test is associated with maximal exertion and high lactate levels, and the intense exercise could influence the recovery response and the myoglobin and creatine kinase values (16).

Muscular Measures, Samples, and Analysis

In 12 subjects, muscle biopsies were obtained under local anesthesia from the vastus lateralis muscle at baseline, within 5 min after each of the two games and after 24 and 48 h of recovery from CON and HOT. The muscle samples were collected with the subject resting in a supine position, with the needle biopsy technique (6) modified with suction. The biopsies were frozen in liquid nitrogen within 15 s after being obtained and stored at –80°C for subsequent analysis of glycogen content. Muscle glycogen content was determined as glucose residues, after hydrolysis of the muscle specimen in 1 M HCl at 100°C for 2 h, and the glycosyl units were then measured fluorometrically (19). Muscle temperature was measured with a needle thermistor (MKA08050-A; Ellab A/S, Rødovre, Denmark) both at half time and immediately after the two matches in the vastus lateralis muscle at a depth of 3 cm (as previously described by Mohr et al. [20]), and the peak temperature was reported.

Blood Samples and Analysis

Ten milliliters of ethylenediaminetetraacetic acid and Heparin blood (BD Vacutainer, Franklin Lakes, NJ) was obtained from an antecubital vein at rest before the games, immediately after each match and after 24 and 48 h of recovery (n = 17). The blood samples were transported within 10 min under cooled conditions to the laboratory, where the heparin blood was directly centrifuged. Plasma was analyzed to determine lactate and sodium concentrations on a Cobas b221 Blood Gas Analyzer (Roche, Mannheim, Germany). Creatine kinase was analyzed thereafter using the Cobas Integra 400 plus (Roche). Furthermore, serum was obtained from a 3.5-mL SST tube (BD Vacutainer). Serum was frozen at −80°C, and myoglobin levels were assessed later in a batch analysis using a commercially available ELISA kit (BioCheck, Inc., Foster City, CA) according to the manufacturer’s instructions. A standard curve was prepared using reference standards ranging from 0 to 1000 ng·mL−1 myoglobin. All samples were run in duplicate on the same assay plate, and mean values were recorded and reported.

Statistical Analysis

Values are presented as mean ± SD unless otherwise indicated. Differences in sprint and endurance performance, neuromuscular parameters, or changes in physiological variables over time or between baseline, CON, and HOT were determined using an a two-way repeated-measures ANOVA (time × condition). In case of a significant difference between periods, a Tukey post hoc test with Bonferroni correction was used to identify the points of difference. Correlations between physiological changes and performance parameters were tested with simple linear regression. For all parameters, statistical significance was accepted at P < 0.05.


The average heart rate was similar in CON (160 ± 2 beats·min−1) and HOT (158 ± 2 beats·min−1). The players ingested 2.6 ± 0.2 L of water in HOT versus 1.1 ± 0.1 L in CON, and the dehydration level was similar at the end of the two matches (1.9% ± 0.3% body weight loss and a plasma sodium concentration of 142 ± 1 mmol·L−1 in HOT vs 1.8% ± 0.1% body weight loss and plasma sodium of 140 ± 1 mmol·L−1 in CON). Blood lactate concentrations recorded after the matches were not different across the two conditions (on average, 4 mmol·L−1). In contrast, significantly (P < 0.001) higher muscle (40.3°C, range = 39.9°C to 41.1°C) and core temperatures (39.6°C, range = 39.1°C to 40.3°C) were attained in the hot match compared with the control match (where the peak muscle and core temperatures were 39.2°C ± 0.1°C and 38.3°C ± 0.1°C; respectively). Furthermore, the players ran 7% less in the hot environment match (9.6 ± 0.2 km) compared with the CON (10.3 ± 0.2 km), and high-intensity running (speed >14 km·h−1) was reduced by 26% (P < 0.05).

Markers of muscle damage and muscle glycogen.

There was a modest reduction in the vastus lateralis muscle glycogen content during the matches as the levels decreased from 488 ± 25 mmol·kg−1 (dry weight) at baseline to ∼300 mmol·kg−1 after both games with no difference across conditions (see Fig. 1). After 24 h of recovery, muscle glycogen levels increased (P < 0.01) by ∼100 mmol·kg−1 in both conditions but then stagnated at ∼400 mmol·kg−1 with no further recovery in the period from 24 to 48 h postmatches. Hence, muscle glycogen levels remained depressed in both conditions for at least 48 h after HOT and CON.

Vastus lateralis muscle glycogen (per kilogram of dry weight muscle) concentrations at baseline and immediately after the control and hot matches and after 24 and 48 h of recovery after the two matches (n = 12; values are presented as mean ± SD). *Significantly lower than baseline (P < 0.05).

Plasma myoglobin levels increased (P < 0.01) by threefold to fourfold after both matches with no significant differences across the environmental conditions. The myoglobin levels returned to baseline value within 24 h, independently of the match condition (Fig. 2).

Plasma myoglobin values obtained before the control and hot match, immediately after matches, and 24 and 48 h after (n = 17; values represent mean ± SD). *Significantly different from baseline (P < 0.05).

Creatine kinase levels were elevated immediately after the games and increased further (P < 0.05) and peaked 24 h postmatches, with significantly higher levels after CON compared with HOT (see Fig. 3). After 48 h, creatine kinase values were still significantly higher in CON compared with HOT, but in both instances, the values were lower than 24 h postmatch and not significantly different from the prematch values. A moderate but significant positive correlation between the individual changes in high-intensity running (between HOT and CON) and the individual changes postmatch in creatine kinase levels after each of the two matches was observed (r2 = 0.20, P < 0.05).

Serum creatine kinase (CK) values obtained before the control and hot match, immediately after matches, and 24 and 48 h after (n = 17; values represent mean ± SD). *Significantly elevated compared with prematch (P < 0.05). #Significantly lower than control (at similar time point, P < 0.05).
Sprint performance (total time for three 30-m repeated sprint) at baseline and immediately after the control and hot matches and after 24 and 48 h of recovery after the two matches (n = 17). *Significantly slower than baseline (P < 0.05). #Significantly lower than control (at similar time point, P < 0.05).

Recovery of sprint performance, endurance, and neuromuscular parameters.

Repeated sprint performance evaluated as time to complete 30 m three times was impaired by ∼2% immediately after the matches (P < 0.05), with no difference across trials. The recovery was faster after the hot environment match as sprint performance was not different from baseline already 24 h postmatch in HOT but remained impaired at this time point in CON. After 48 h of recovery, there was no difference across trials and repeated sprint performance was similar to the baseline value (Fig. 4).

Compared with baseline, the players’ intermittent endurance capacity, estimated by the Yo-Yo test, was similar 48 h postmatch, with no effect of the condition (see Fig. 5).

Mean and individual Yo-Yo performance (endurance interval running distance) at baseline and 48 h after the control and hot match (n = 17).

MVC torque was reduced by ∼5% after both matches, however, with no significant effect of time (P = 0.15) or condition (P = 0.81; see Fig. 6A). Compared with baseline, VA was reduced (P < 0.05) after both games (−1.4% and −1.6% in CON and HOT, respectively) but returned to baseline values within 24 h after both matches (Fig. 6B). There was a significant (P < 0.05) reduction in peak twitch torque after both matches (Fig. 6C), with no differences across trials. At baseline, the rate of force development (slope of torque-time curve normalized relative to MVC) and the associated soleus EMG rise (slope of EMG-time curve normalized relative to maximal EMG activity) were 66.2 ± 4.6%MVC·s−1 and 13.5 ± 1.0%RMS·s−1. These were not affected by the game irrespectively of the environmental conditions (all P > 0.05).

Time course of plantarflexion maximal isometric voluntary contraction (MVC) torque (A), VA (B), and peak twitch torque (C). Measurements were taken at baseline and 30 min (Post), 24 h (Post24), and 48 h (Post48) after two experimental soccer matches performed in control (black bars) and hot (white bars) environments (n = 17). *Significantly different from baseline. #Significantly different from all other conditions (P < 0.05).


The present study demonstrates that in well-trained athletes, acute physical exercise performance is impaired, but neither markers of muscle damage nor recovery of functional performance are aggravated after competitive exercise under heat stress as compared with a control match in a temperate environment. Myoglobin and creatine kinase levels were elevated twofold to threefold after both matches, but the high muscle temperatures attained in the hot match did not augment indices of rhabdomyolysis. In contrast, the creatine kinase response after the hot match was lower rather than higher compared with the control match. Similarly, the recovery of repeated sprinting performance appeared to be marginally faster after the hot match. The neuromuscular fatigue experienced by the plantar flexors, which appeared to relate to a combination of neural (reduced voluntary muscle activation, which recovered within 24 h) and muscular factors (impaired muscle contractility during an electrically evoked twitch), was modest and not different between conditions. Muscle glycogen levels remained depressed for more than 48 h after both matches, but the responses were similar across environmental conditions, and the incomplete muscle glycogen recovery 2 d after the matches did not limit the player performance in a maximal intermittent endurance test. Furthermore, there was no relation between the incomplete recovery of muscle glycogen and any of the neuromuscular parameters (MVC, rate of force development, or rise of the EMG) or the impaired sprinting ability.

Myoglobin and creatine kinase levels.

On average, the postmatch creatine kinase levels did not approach levels associated with clinical rhabdomyolysis (7,8); however, five of the players reached values higher than 1000 U·L−1 after the control match, whereas only one of those five individuals had plasma levels higher than 1000 U·L−1 after HOT. It was hypothesized that the postexercise responses of these commonly used blood biomarkers of rhabdomyolysis would be exaggerated if the hot match was associated with hyperthermia-induced muscle damage. The changes observed in both myoglobin and CK are comparable with previous postmatch values in trained players after competitive games in temperate settings (18), and because the levels after the hot match were lower rather than higher, it appears unlikely that high muscle temperatures (with values up to ∼41°C) or moderate dehydration (∼2%) will induce exertional rhabdomyolysis in trained soccer players. Rather, it appears that the total amount of running (presumably the distance of high-intensity running, which was ∼25% higher in the control match compared with HOT [23]) is an important factor affecting the creatine kinase response. Thus, a moderate but significant correlation between the individual changes in high-intensity running and the individual changes in creatine kinase levels postmatch was observed. In contrast, neither relative changes nor absolute values of the individual CK levels could predict performance changes after the matches or during the recovery period. However, comparing the recovery of sprint performance with the postmatch CK responses, it seems plausible that the hot match, due to heat-induced fatigue, resulted in a decrease in high-intensity running and a diminished CK response with a slightly faster recovery of the subjects sprinting ability (cf. Fig. 3 with Fig. 4).

The marked elevation of serum myoglobin after both matches indicates that the present type of exercise with several brief efforts and many eccentric muscle contractions is associated with muscle damage, which may explain the slow recovery of performance and muscle glycogen (18,21). Because the postexercise myoglobin response was not aggravated by the hyperthermia developed during the hot match, it appears that the resultant acute muscle damage is caused by the exercise mode rather than the higher muscle temperatures. Very high core or muscle temperatures have been suggested to be potentially harmful (8,31), but these detrimental effects were not observed in the current study despite exercising in adverse environmental conditions. This outcome further highlights the necessity for field-based studies with highly trained athletes (5). The present data and conclusions refer to trained athletes, and it remains possible that untrained individuals exercising in the heat may experience adverse effects that could lead to rhabdomyolysis. Thus, some individuals may be more susceptible to exertional rhabdomyolysis and vulnerable to malignant hyperthermia than the present group of trained athletes, and these individuals should be extra careful when exercising in the heat (8). However, the present group of trained athletes appeared to tolerate intense competitive exercise with marked environmental heat stress with no signs of heat injury. Furthermore, data showed that muscle damage was not significantly different between HOT and CON, which mimics the low-to-moderate environmental conditions experienced during the subjects regular season (all the 17 players were living and competing in the northern Europe with environmental temperatures lower than 20°C for the last 2 month before the study). Hence, on the basis of the present study, the recovery issue should not prevent matches from being placed in countries/conditions with high environmental temperatures.

Muscle glycogen and performance recovery.

The delayed recovery of muscle function and the slow replenishment of muscle glycogen stores after intermittent exercise are comparable with previous observations in well-trained soccer players after competitive matches or simulated games (4,18). The present study compared recovery responses after matches in HOT and CON and did not include an additional control group that did not participate in any match and only completed the exercise tests. However, although the subjects in the present study performed light training, three short sprints and an MVC test postmatch and again 24 h later the recovery response were not different from observations with a complete absence of physical activity during the recovery period (14,26). Thus, it is a general observation that although glycogen degradation during a 90-min soccer match is moderate compared with a prolonged bicycle bout, the recovery period necessary for complete restoration of the glycogen levels is markedly longer (26). Furthermore, it does not appear to be limited by the amount of carbohydrate or protein ingested during the recovery period (14). The slow recovery of muscle glycogen has been ascribed to the eccentric work associated with the many intense actions, such as frequent accelerations and decelerations, which are characteristic for many sports including soccer (21,26). In addition, it is well known that eccentric contractions may induce muscle damage and impair insulin action and muscle glucose transport for several days (3).

During exercise in the heat at a given intensity, it has been demonstrated that muscle glycogen utilization is augmented and that the altered muscle metabolism relates to the increase in intramuscular temperature (11,39). The higher muscle temperatures attained in HOT would therefore be expected to aggravate the degradation of muscle glycogen during the match. However, the temperature effect may have been offset because of total running, and in particular high-intensity running was reduced in the hot match compared with control. In relation to muscle glycogen utilization, the HOT match resulted in a similar response as the CON game. Furthermore, the subsequent recovery response was apparently not altered, although the HOT match had less high-intensity running, and a diminished creatine kinase response during the recovery period that could indicate less muscle damage as consequence of less eccentric exercise.

Interestingly, the ability to perform repeated sprints as well as performance in the high-intensity running (Yo-Yo IR1) test was not impaired 48 h after the games, although muscle glycogen levels still were depressed. The release rate of calcium from the sarcoplasmic reticulum is impaired by fatigue and low muscle glycogen levels (32,33), and the potential relation between impaired sarcoplasmic reticulum function, reduced MVC force, and low subcellular glycogen content has been investigated after intermittent exercise (26). The link is not fully understood, but in the present study, the MVC, the rate of force/torque development, and the athletes’ sprinting ability were fully recovered 48 h after the matches, and it appears that muscle contractile and sarcoplasmic reticulum function recover faster than total muscle glycogen.

In line with sprint and intermittent performance, neuromuscular fatigue evaluated by voluntary and electrical stimulation of the plantar flexors was not fundamentally different when conditions were compared. It is well known that ongoing profound hyperthermia may impair VA and the ability to maintain maximal activation of both exercised and “nonexercised” muscle groups (28); however, this effect of exercise-induced hyperthermia is apparently not present ∼30 min after exercise as the core and brain temperatures will return to normothermic levels within this period (30). Previous studies examining neuromuscular consequences of football matches or comparable prolonged intermittent exercise have primarily focused on the knee extensors, showing significant reductions in maximal voluntary strength and explosive force (i.e., rate of force development [2,35]). Rampinini et al. (35) reported a similar reduction in sprint performance in professional players as observed in the present article; however, they observe marked reductions in MVC, whereas the results in the present study showed that match-related fatigue in the plantar flexors of well-trained soccer players is modest, as evidenced by nonsignificant reduction of 5% in maximal isometric strength and an unaltered rapid force characteristics with an associated postmatch neural drive to the soleus muscle. Although, there may be differences between muscle groups, there are also contrasting results in the literature regarding the recovery of quadriceps muscle function in the days after a soccer match with voluntary strength production capacity either returning to baseline 48 h after the game (18,35) or remaining depressed for more than 72 h (2). In contrast, quadriceps peak twitch force did not change after a 90-min simulated soccer game performed in a laboratory environment, presumably because of the lowered eccentric solicitations on the treadmill (38). However, in the present study, impaired muscle function, as interpreted from the lowered peak twitch torque, persisted at least 48 h after exercise. This peripheral alteration could be attributed to exercise-induced muscle damage as indicated by the large postgame increases in serum myoglobin and plasma creatine kinase values, and as discussed previously, the delayed recovery of muscle glycogen may interfere with sarcoplasmic reticulum function (32,33). However, the relation between the impaired muscle function, muscle damage, and delayed recovery of muscle glycogen is not well understood, and although electrically evoked twitch force remained depressed for 48 h after exercise, functional performance evaluated as MVC and sprint ability was fully recovered.

Hot ambient conditions have previously been observed to affect MVC of the plantar flexors but not the knee extensors (34). However, the current study revealed that the effect of fatigue on the plantar flexor function after the matches was independent of the temperature condition and recovered within 24 h. Hence, the hyperthermia-induced temperature effect on central fatigue persist for less than 30 min and the exercise effects on motor cortex excitability and excitation, descending nervous command toward motoneurons, and motor neuron excitability are recovered within 24 h.

In conclusion, in trained athletes, neither markers of muscle damage nor the recovery of functional performance are aggravated by completing a competitive soccer match under heat stress as compared with a control match in a temperate environment. In the heat as well as the control condition, the matches were associated with elevated levels of creatine kinase and myoglobin, and the functional performance and the recovery of muscle glycogen stores were impaired for a prolonged period after the matches. However, the muscle damage and subsequent slow recovery of performance and glycogen stores seems to relate to exercise-induced factors rather than heat-induced muscle injury.

The authors thank the players for their effort.

The authors thank Dr. Hakim Chalabi and Dr. Pitre Bourdon for the support from Aspetar, Qatar Orthopaedic and Sports Medicine Hospital and Aspire, Academy for Sports Excellence.

The authors thank Dr. Martin Buchheit for the HR analyses and the staff from the Research Education Centre for data collection.

The authors thank the nurses, physiotherapists, and sports medicine physicians from Aspetar for taking care of the players.

The study was funded by Aspetar, Qatar Orthopaedic and Sports Medicine Hospital. The authors have no conflict of interest.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.


1. Aagaard P, Simonsen E, Andersen J, Magnusson P, Dyhre-Poulsen P. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol. 2002; 93: 1318–26.
2. Ascensao A, Rebelo A, Oliveira E, Marques F, Pereira L, Magalhaes J. Biochemical impact of a soccer match—analysis of oxidative stress and muscle damage markers throughout recovery. Clin Biochem. 2008; 41: 841–51.
3. Asp S, Daugaard J, Kristiansen S, Kiens B, Richter EA. Eccentric exercise decreases maximal insulin action in humans: muscle and systemic effects. J Physiol. 1996; 494 (Pt 3): 891–8.
4. Bendiksen M, Bischoff M, Randers MB, et al.. The Copenhagen Soccer Test: physiological response and fatigue development. Med Sci Sports Exerc. 2012; 44 (8): 1595–603.
5. Bergeron M, Bahr R, Bartsch P, et al.. International Olympic Committee consensus statement on thermoregulatory and altitude challenges for high-level athletes. Br J Sports Med. 2012; 46 (11): 770–9.
6. Bergstrom J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967; 71: 140–50.
7. Brancaccio P, Lippi G, Maffulli N. Biochemical markers of muscular damage. Clin Chem Lab Med. 2010; 48: 757–67.
8. Capacchione JF, Muldoon SM. The relationship between exertional heat illness, exertional rhabdomyolysis, and malignant hyperthermia. Anesth Analg. 2009; 109: 1065–9.
9. Dvorak J, Racinais S. Training and playing football in hot environments. Scand J Med Sci Sports. 2010; 20 (Suppl 3): 4–5.
10. Ely MR, Cheuvront S, Roberts WO, Montain SJ. Impact of weather on marathon-running performance. Med Sci Sports Exerc. 2007; 39 (3): 487–93.
11. Febbraio MA, Snow RJ, Stathis CG, Hargreaves M, Carey MF. Effect of heat stress on muscle energy metabolism during exercise. J Appl Physiol. 1994; 77: 2827–31.
12. González-Alonso J, Mora-Rodríguez R, Below PR, Coyle EF. Dehydration markedly impairs cardiovascular function in hyperthermic endurance athletes during exercise. J Appl Physiol. 1997; 82: 1229–36.
13. Gonzalez-Alonso J, Teller C, Andersen S, Jensen F, Hyldig T, Nielsen B. Influence of body temperature on the development of fatigue during prolonged exercise in the heat. J Appl Physiol. 1999; 86: 1032–9.
14. Gunnarsson TP, Bendiksen M, Bischoff R, et al.. Effect of whey protein- and carbohydrate-enriched diet on glycogen resynthesis during the first 48 h after a soccer game. Scand J Med Sci Sports. 2011. doi: 10.1111/j.1600-0838.2011.01418.x.
15. Hawes R, McMorran J, Vallis C. Exertional heat illness in half marathon runners: experiences of the Great North Run. Emerg Med J. 2010; 27: 866–7.
16. Krustrup P, Mohr M, Amstrup T, et al.. The Yo-Yo Intermittent Recovery Test: physiological response, reliability, and validity. Med Sci Sports Exerc. 2003; 35 (4): 697–705.
17. Krustrup P, Mohr M, Steensberg A, Bencke J, Kjaer M, Bangsbo J. Muscle and blood metabolites during a soccer game: implications for sprint performance. Med Sci Sports Exerc. 2006; 38 (6): 1165–74.
18. Krustrup P, Ortenblad N, Nielsen J, et al.. Maximal voluntary contraction force, SR function and glycogen resynthesis during the first 72 h after a high-level competitive soccer game. Eur J Appl Physiol. 2011; 111: 2987–95.
19. Lowry OH, Passonneau JV. Some recent refinements of quantitative histochemical analysis. Curr Probl Clin Biochem. 1971; 3: 63–84.
20. Mohr M, Krustrup P, Nybo L, Nielsen J, Bangsbo J. Muscle temperature and sprint performance during soccer matches—beneficial effect of re-warm-up at half time. Scand J Med Sci Sports. 2003; 14: 156–62.
21. Mohr M, Krustrup P, Bangsbo J. Fatigue in soccer: a brief review. J Sports Sci. 2005; 23: 593–9.
22. Mohr M, Mujika I, Santisteban J, et al.. Examination of fatigue development in elite soccer in a hot environment: a multi-experimental approach. Scand J Med Sci Sports. 2010; 20 (Suppl 3): 125–32.
23. Mohr M, Nybo L, Grantham J, Racinais S. Physiological responses and physical performance during football in the heat. PLoS One. 2012; 7: e39202.
24. Morris JG, Nevill ME, Williams C. Physiological and metabolic responses of female games and endurance athletes to prolonged, intermittent, high-intensity running at 30 degrees and 16 degrees C ambient temperatures. Eur J Appl Physiol. 2000; 81: 84–92.
25. Nielsen B, Hales JRS, Strange NJ, Christensen NJ, Warberg J, Saltin B. Human circulatory and thermoregulatory adaptations with heat acclimation and exercise in a hot, dry environment. J Physiol. 1993; 460: 467–85.
26. Nielsen J, Krustrup P, Nybo L, et al.. Skeletal muscle glycogen content and particle size of distinct subcellular localizations in the recovery period after a high-level soccer match. Eur J Appl Physiol. 2012; 112 (10): 3559–67.
27. Nybo L, Møller K, Volianitis S, Nielsen B, Secher NH. Effects of hyperthermia on cerebral blood flow and metabolism during prolonged exercise in humans. J Appl Physiol. 2002; 93: 58–64.
28. Nybo L, Nielsen B. Hyperthermia and central fatigue during prolonged exercise in humans. J Appl Physiol. 2001; 91: 1055–60.
29. Nybo L, Nielsen B. Middle cerebral artery blood flow velocity is reduced with hyperthermia during prolonged exercise in humans. J Physiol. 2001; 534: 279–86.
30. Nybo L, Secher NH, Nielsen B. Inadequate heat release from the human brain during prolonged exercise with hyperthermia. J Physiol. 2002; 545: 697–704.
31. O’Connor FG, Casa DJ, Bergeron MF, et al.. American College of Sports Medicine roundtable on exertional heat stroke-return to duty/return to play: conference proceedings. Curr Sports Med Rep. 2010; 9: 314–21.
32. Ortenblad N, Nielsen J, Saltin B, Holmberg HC. Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J Physiol. 2011; 589: 711–25.
33. Ortenblad N, Sjogaard G, Madsen K. Impaired sarcoplasmic reticulum Ca(2+) release rate after fatiguing stimulation in rat skeletal muscle. J Appl Physiol. 2000; 89: 210–7.
34. Racinais S, Girard O. Neuromuscular failure is unlikely to explain the early exercise cessation in hot ambient conditions. Psychophysiology. 2012; 49: 853–65.
35. Rampinini E, Bosio A, Ferraresi I, Petruolo A, Morelli A, Sassi A. Match-related fatigue in soccer players. Med Sci Sports Exerc. 2011; 43 (11): 2161–70.
36. Roberts WO. Exercise-associated collapse care matrix in the marathon. Sports Med. 2007; 37: 431–3.
37. Roberts WO. Determining a “do not start” temperature for a marathon on the basis of adverse outcomes. Med Sci Sports Exerc. 2010; 42 (2): 226–32.
38. Robineau J, Jouaux T, Lacroix M, Babault N. Neuromuscular fatigue induced by a 90-minute soccer game modeling. J Strength Cond Res. 2012; 26: 555–62.
39. Starkie RL, Hargreaves M, Lambert DL, Febbraio MA. Effect of temperature on muscle metabolism during submaximal exercise in humans. Exp Physiol. 1999; 84: 775–84.
40. Thorlund JB, Aagaard P, Madsen P. Rapid muscle force capacity changes after soccer match play. Int J Sports Med. 2009; 30: 273–8.


©2013The American College of Sports Medicine