Force and power generation during sustained muscle contraction is limited by fatigue which is one major factor that determines human performance. According to Kluger et al. (33, p. 411), fatigability is defined as “the magnitude or rate of change in a performance criterion relative to a value over a given time of task performance or measure of mechanical output.” This change may involve central (18) and peripheral (16) sites. More specifically, central fatigability includes processes starting from the activation of the motor cortex to the recruitment of motoneuron pool at spinal level, whereas peripheral fatigability includes the action potential transmission along the motor nerve axon, sarcolemma, and T-tubules; the function of the neuromuscular junction; and the efficiency of cross-bridge force production (18). Noninvasive transcutaneous nerve stimulation and EMG combined with voluntary muscle activation can provide an insight to the above-mentioned central and peripheral components. Peripheral deficits are reflected in alterations of the twitch properties of the fatigued muscle, and central fatigability can be evaluated with the twitch interpolation technique as a measure of central activation deficit (17,18).
According to previous studies, fatigability resistance is altered during the developmental ages (48). Preadolescent children are less fatigued than adults when performing maximal isometric (24) or isokinetic contractions (43) and during dynamic actions, such as maximal cycling (47) and short running bouts (49). These studies support the idea that the higher fatigability resistance shown in children could be attributed to peripheral metabolic factors, such as lower blood lactate and proton accumulation (47,49), and to central factors, as revealed by the lower reduction in EMG mean power frequency and amplitude (24,43). These are indications that central and peripheral factors inducing fatigue are different between children and adults. However, there are several central and peripheral parameters that have not been examined during fatigue.
One important parameter that could determine central fatigability is the level of voluntary activation. After sustained or intermittent maximal voluntary contractions (MVC), force output and EMG amplitude become progressively lower due to fatigability (31). This decrease in EMG (amplitude and mean power frequency) is particularly lower in children than in adults (1,24). However, it is still unknown whether this difference in EMG response between the two age groups could be attributed to differences in the level of activation as well. For the knee extensors, it has been shown that the level of activation, as determined by twitch interpolation technique, is lower in children (42) and decreases more during a 2-min MVC compared to adults (51). In contrast, after a fatigue-inducing protocol involving repetitive stretch shortening cycles, young adults had significantly higher level of central fatigability in terms of decrement in level of activation than prepubescent boys (21). Nevertheless, the level of activation (6) or fatigability resistance (2) could be different not only between different fatigue-inducing protocols but also between different muscle groups. Under nonfatigue conditions, the level of activation during plantarflexion tends to increase with age (23), but within an age range of 9 and 13 yr, children have similar levels of activation compared to 15- to 18-yr-old male adolescents and adults (7). However, there are no references in the literature concerning the difference in the level of muscle activation between prepubertal children and adults after a maximal sustained fatigue-inducing protocol. The only relevant study on this issue examined the knee extensors of adults and 12– to 14-yr-old children and showed that children have higher central fatigability than adults (51).
The differences in fatigability between children and adults have been attributed to the children’s lower accumulation of metabolites in their muscle compartments (49) and to their reduced reliance on the glycolytic metabolism (47). These parameters could have consequences for the periphery and, more particularly, for muscle twitch properties. For instance, twitch torque decreases after sustained or intermittent fatigue–inducing protocols in adults (20) and increases with age (7,22). The percent decrease in twitch torque after fatigue is lower in 12- to 14-yr-old children as compared to adults (51). However, we still do not know the extent peak twitch torque and maximum rate of torque development (RTDmax) decrease among 9- to 10-yr-old children and adults. The importance of the examination in this age group is based on the fact that the corticospinal tract is still developing until the age of 11 (34), and significant differences in fatigability rates exist between 11- and 14-yr-old boys (12,46). Furthermore, the propagation of the action potentials from the nerve to the muscle, as examined by the maximum M-wave (Mmax), has not yet been measured in children after fatigue. This issue is still controversial even in adults. While several studies revealed a decrease in Mmax after maximal (9) or submaximal (37) fatiguing tasks, others showed no change during either maximal (35) or submaximal (45) contractions.
Taking the above into account, the purpose of this study was to examine central and peripheral neuromuscular factors that might be responsible for the fatigability differences between adults and prepubertal boys after a maximal sustained fatigue-inducing test. This will enhance our understanding of fatigability in pediatric individuals, which is an essential requirement in developing strategies to cope with fatigue phenomena under athletic, everyday, or pathological conditions.
A total of 10 prepubescent boys and 11 men with no lower limb or back injuries participated voluntarily in the study (Table 1). The participants were nonathletes for the past 2 yr, with boys participating in the physical education class twice a week. Men were students of the local Physical Education and Sports Department and participated in their curriculum activities. All children were examined by a pediatrician and were classified to be at the first stage of sexual maturity according to the Tanner scale (52). Before data collection, all participants and the children’s parents were informed about the purpose and the assessments of the study, and written consent was obtained. The parents were always present during testing, and participants were free to withdraw from the experiment at any time. The experimental protocol was approved by the Ethics Committee of the Aristotle University of Thessaloniki.
The Cybex Norm isokinetic dynamometer (Cybex division of Lumex, Ronkonkoma, NY) was used for the isometric torque measurement and the fatigue–inducing task of plantar flexors muscles. For the EMG, the BTS TELEMG (BTS Bioengineering, Milano, Italy) remote system was used (CMMR > 94 dB, noise < 0.7 μV rms at 1–10,000 Hz). The analog signals were converted to digital (16 bit, at 1-kHz sampling frequency) and were stored for further analysis. Single electrical square pulses (200 μs in duration) were delivered from an isolated constant current stimulator (DS7A; Digitimer Ltd., Hertfordshire, UK).
Soleus, medial gastrocnemius, and the tibialis anterior muscles were selected for the EMG measurement. The gastrocnemius lateralis was excluded to avoid the cross-talk issues from the tibialis anterior muscle (54). The EMG was recorded with bipolar Ag–AgCl surface electrodes (0.8 mm in diameter and 1.2-cm interelectrode distance) covered with conductive paste (Ten20; Weaver and Company). To reduce skin resistance below 2 kΩ, the skin surface was shaved, abraded with sandpaper, and cleaned with alcohol wipes. Each electrode was fixed to the skin with adhesive tape.
EMG electrodes were placed on the dominant foot, determined as the foot preferred to make a kick. Electrode placement was consistent with the SENIAM recommendations (27). The medial gastrocnemius electrodes were set on the most prominent bulk of the muscle defined during a brief muscle contraction while standing. For the soleus muscle, the electrodes were placed at two-thirds the line between the medial condyle of the femur and the medial malleolus. The electrodes for the tibialis anterior were placed parallel to tibia and at two-thirds of the distance between the knee joint cleft and the medial malleolus. Each participant performed manual resistance tests that consisted of isolated movements specific to each muscle to validate the electrode placement. The ground electrode was fixed on the lateral epicondyle.
Supramaximal electrical stimulation (1.5 times above the intensity evoking the Mmax) was applied on the tibial nerve during MVC testing approximately 1 s after the plantarflexion torque reached a plateau. The cathode was located on the poplitea fossa and the anode on the thigh, proximal to the patella. Elastic bandages kept the electrodes in place and ensured the appropriate electrode contact with the skin. To limit the discomfort and due to ethical issues for children, a single stimulus was used rather than multiple stimuli (50).
One week before the measurement, participants visited the laboratory for familiarization with the experimental conditions. For the evaluation session, the anthropometric measurements were assessed (body mass and height), and afterwards, each participant performed a general warm-up including low-intensity cycling on an ergometer and stretching exercises. All tests were performed on the dominant foot, at supine position, with hips flexed at 60°. The knee was set at full extension, and the angle between the plantar surface of the foot and the tibia was set at 90°. The rotation axis of the dynamometer was approximately aligned with the rotation axis of the ankle. Nonelastic Velcro straps stabilized the foot on the platform and the subject’s trunk and thigh on the dynamometer’s chair.
The participants performed 15–20 submaximal isometric contractions with gradually increasing intensity. Twitch torque and Mmax were assessed at relaxed state before the MVC test, which consisted of three to five maximal isometric plantar and dorsal flexions, with a 3-min rest interval. During plantarflexion, superimposed nerve stimulation was performed. Participants were instructed to produce their maximal torque output as fast as possible and maintain it at the highest levels for 5 s. Verbal motivation and visual feedback of the torque output were provided during the tests. The highest torque value was marked on the monitor and was set as the target to overcome for the pending trials. This procedure was repeated until the torque of the three best trials was not less than the 95% of the best one. The trial with the highest torque value was further analyzed and used as the target value for the fatigue-inducing task, which took place 10 min after the end of the MVC tests.
The fatigue-inducing protocol consisted of a sustained plantarflexion at 100% of MVC. The trial was terminated until the individual was not able to reach the 50% of MVC. Within 10 s after the end of the fatigue-inducing protocol, plantarflexion MVC was measured with superimposed nerve stimulation. Furthermore, supramaximal nerve stimulation was applied at rest to record the twitch torque and M-wave.
Measurements and data processing
The EMG signal was band-pass filtered (10–500 Hz) and amplified (×1000). The root mean square was calculated over a window of 20 ms. The antagonistic activity of tibialis anterior was normalized to the tibialis anterior EMG during the prefatigue dorsiflexion MVC. Data captured during fatigue (torque and EMG) were analyzed by calculating the mean value of five equal time windows, representing the 0%–20%, 20%–40%, 40%–60%, 60%–80%, and 80%–100% of the endurance limit.
The activation deficit (AD) was assessed by means of twitch interpolation technique (23), by applying supramaximal stimulation on the tibial nerve and measuring the plantarflexion torque output before and shortly after the stimulation. AD was calculated according to the following formula (23):
Peak twitch torque, RTDmax, and Mmax area were assessed using custom MATLAB scripts (MATLAB 7.0; MathWorks, Inc.). The torque onset was determined at the instance when torque exceeded 1% of the peak twitch torque. RTDmax was defined as the maximum slope of torque during a moving time window of 20 ms. Mmax area was measured beginning from the first point to cross the zero baseline after the stimulus artifact and ending to the last point before the second baseline crossing (11).
All values are presented as mean and SEM, and they were normalized to the prefatigue values. The statistical analysis included two-way ANOVA for repeated measurements for the factor time (measurements before, during, and after the fatigue-inducing protocol). Scheffè post hoc test for multiple comparisons was performed. Furthermore, between-group differences in baseline values and in percent changes relative to the prefatigue values were calculated using unpaired t-test. The level of significance was set at P < 0.05. All statistical tests were performed with Statistica 6.0 (StatSoft, Inc.).
Before the fatigue-inducing protocol, men had significantly higher absolute and relative (i.e., normalized to body mass) torque, peak twitch torque, and RTDmax than boys (P < 0.001; Table 2). In contrast, there was no between-group significant difference in AD and Mmax area for the soleus and medial gastrocnemius muscles (P > 0.05).
During fatigue-inducing protocol
The mean endurance times for the fatigue-inducing task were significantly higher in boys than in men (t = −3.61, P = 0.002). More specifically, boys and men abandoned the fatigue-inducing trial at 126.7 ± 6.4 and 94.1 ± 6.3 s, respectively.
As shown in Figure 1, torque and EMG decreased significantly in both groups during the sustained contraction. More specifically, torque decreased significantly for men and boys at the end of the protocol by 50.4% ± 1.7% and 47.3% ± 1.3%, respectively (F 4,76 = 191.4, P < 0.001). The interaction between the factor group and time was statistically significant (F 4,76 = 5.5, P < 0.001). Compared to the initial values, men showed a significant decrease in torque for the 20%–100% of endurance limit, whereas boys showed a significant decrease in torque for the 40%–100% of endurance limit. Furthermore, men had significantly higher torque deficit than boys during the 20%–40% of the endurance time.
Regarding the soleus EMG amplitude, a significant decrease was observed in men and boys (F 4,76 = 146.1, P < 0.001), decreasing at the end of the protocol relative to the initial value by 41.0% ± 2.6% and 32.4% ± 2.3%, respectively (Fig. 1). Men had significantly lower EMG amplitude than boys (F 1,76 = 7.2, P = 0.015), but the interaction between age and time did not reach the level of significance (F 4,76 = 2.0, P = 0.097).
Similar behavior was observed for the medial gastrocnemius EMG regarding its decreases during fatigue (F 4,76 = 194.0, P < 0.001). Boys had higher EMG amplitude than men (F 1,76 = 5.7, P = 0.027), and the interaction was significant (F 4,76 = 5.9, P < 0.001). Boys had significantly lower medial gastrocnemius EMG relative to the initial value after the 40%–60% of the endurance limit, whereas men revealed significant decrease relative to the initial value after the 20%–40% of the endurance limit. Between-group differences were observed during 20%–60% of the endurance limit (P < 0.05).
Concerning the antagonistic activity, tibialis anterior EMG during plantarflexion showed a gradual decrease during the fatigue-inducing protocol (F 4,76 = 57.0, P < 0.001). Boys revealed significantly higher values than men throughout the whole fatigue-inducing session (F 1,76 = 9.7, P = 0.006). The interaction was significant (F 4,76 = 2.9, P < 0.027), although both groups had statistically significant decrease compared to the initial values after the 40%–60% of the endurance time (P < 0.05).
Prefatigue versus postfatigue comparison
As shown in Figure 2, AD was not significantly different between groups (F 1,19 = 0.1, P = 0.821) but increased significantly after fatigue (F 1,19 = 293.5, P < 0.001), with no significant interaction (F 1,19 = 0.4, P = 0.560). After fatigue, AD reached 9.6% ± 0.6% and 9.5% ± 1.0% for men and boys, respectively, with no significant difference between these values (P > 0.05).
Peak twitch torque decreased significantly (F 1,19 = 44.4, P < 0.001), and the interaction was significant as well (F 1,19 = 18.7, P < 0.001). Men compared to boys had significantly higher decrease in peak twitch torque when expressed as percent change (t = −2.8, P = 0.011; Fig. 3). Similarly, RTDmax showed a significant decrease after fatigue (F 1,19 = 106.8, P < 0.001), and the interaction was significant as well (F 1,19 = 17.8, P < 0.001). RTDmax decreased significantly more in men than in boys when values were expressed as percent change (t = −2.7, P = 0.015; Fig. 3).
Mmax area decreased significantly in both groups for the soleus (F 1,19 = 113.8, P < 0.001) and the medial gastrocnemius (F 1,19 = 279.4, P < 0.001). However, in both muscles, the interaction was not significant (soleus: F 1,19 = 1.0, P = 0.329; medial gastrocnemius: F 1,19 = 1.5, P = 0.234). The decrease in Mmax area expressed as percent change relative to the prefatigue values did not differ statistically significant between the two groups in both muscles (soleus: t = −1.2, P = 0.239; medial gastrocnemius: t = −1.5, P = 0.153; Fig. 3).
In the present study, boys appear more fatigue resistant than men, showing longer endurance limit and delayed torque and agonist EMG decrease. After the end of the fatigue-inducing protocol, both groups showed similar decrease in the level of activation. However, regarding the peripheral parameters that were examined, boys were less affected after fatigue than men in terms of reduction in peak twitch torque, and RTDmax, whereas no differentiation in Mmax area between the two groups was observed.
Our data revealed that both children and adults decreased their torque and agonist EMG during fatigue but children were less prone to fatigue than adults, showing a tendency for slower rate of decrease during the first half of the fatigue–inducing protocol. The slower rate of decrease in boys compared to men was apparent only for the medial gastrocnemius and not for the soleus muscle, which has predominantly Type I fibers and, consequently, is more fatigue resistant (15). The differentiation in fatigability between these muscles has also been shown in previous studies (38,40), but our data suggest further that muscle fiber distribution might determine whether children and adults will be differentiated in the fatigue process in terms of EMG amplitude.
In general, the EMG amplitude decrease during the sustained contraction could be attributed to the number of recruited motor units, their recruitment rate, and their synchronization (28). Moreover, part of this reduction could be explained by the decline in Mmax area observed in both groups for the soleus and medial gastrocnemius muscles. Reduced Mmax area is an indication of failure to maintain neuromuscular propagation at a normal level and/or decline in the sarcolemmal or t-tubule excitability (19). According to our data, this mechanism plays a similar role in both age groups. It has been suggested that, during fatigue, adults rely more on their fast-twitch motor units (24), which, compared to the slow-twitch motor units, are (a) less fatigue resistant, (b) induce action potentials higher in amplitude, and (c) are recruited during high-intensity contractions (26). This could explain the faster decrease in agonist EMG shown in men compared to boys during fatigue.
The higher antagonist activity in boys compared to men, expressed as percent of the maximum EMG produced by the same muscle when acting as agonist, which is in agreement with a previous study (36), could partially explain the boys’ deficit in force output before fatigue. However, the parallel decrease in antagonist EMG during the fatigue-inducing session for both groups (no significant interaction) rules out the contribution of this mechanism for the differences of fatigability between the groups examined. This has also been previously verified for the biceps femoris during knee flexion (1).
Regarding the level of activation, as assessed with the twitch interpolation technique, our results showed that, before fatigue, both groups could recruit their motor units near maximum. This is in agreement with previous studies assessed on the plantar flexors in 9- to 13-yr-old boys (7,23), although children have a decreased level of activation compared to adults for the knee joint (42), which underlines the muscle group specificity on this issue. After fatigue, the decrease in the level of activation was evident in both groups, and the difference between the groups was not significant. This indicates that this central component might not be responsible for the greater fatigability resistance of children compared to adults. This finding is in contrast to a previous study on the knee extensors comparing 12- to 14-yr-old boys with men (51). In this study, the authors indicated that the level of activation decreased significantly more in children after a 2-min MVC. This discrepancy could be attributed to the examined age range and muscle group. More specifically, 11-yr-old boys demonstrated a more fatigue-resistant profile than 14-yr-old boys (12,46). Furthermore, central fatigability associated with sustained isometric contractions may differ according to the muscle group examined (i.e., plantar flexors vs knee extensors) despite similar MVC force reductions (39). A major methodological difference can be also observed in the stimulation properties for examining the level of voluntary activation. Streckis et al. (51) applied a train of 25 supramaximal stimuli at 100 Hz to assess the level of activation, which could have caused discomfort especially in children. In our study, we used a single supramaximal stimulus for the same purpose because of ethical reasons and because it was not possible to get permission from the children’s parents to apply more than one stimulus on the tibial nerve because this was painful in some occasions. This implies that the level of activation could probably be overestimated in the current study. Further in–depth investigation of this issue measuring biochemical components acting globally on the brain and regulating its response to central fatigability, such as noradrenaline (32), might help us better understand the discrepancies between different responses of central fatigability when testing different muscle groups and age groups.
The results of the present study indicate that the differences in fatigability observed between boys and men rely more on peripheral rather than central factors. Even if men had higher peak twitch torque and RTDmax than boys before fatigue, the observed reduction after fatigue was significantly higher in men than in boys, indicating dramatic fatigability on these contractile properties. In general, the decrease in these twitch properties after fatigue is in agreement with previous studies (5), and based on in situ or animal experiments, it could be attributed to the impairment of the excitation–contraction coupling (29), to the decreased activity in myosin ATPase (14), and to a lower contractile kinetics of intracellular Ca2+ release (44). Because of ethical constraints, we cannot conclude whether the abovementioned parameters are differentiated between children and adults. We are confident, however, that children have a lower rate of glycolytic metabolite accumulation (47), and individuals with predominantly Type II fibers demonstrate a greater decrease in peak twitch torque compared to subjects with higher Type I fibers (25). Possibly, adults have a higher Type II fiber composition than children (30), although there are studies revealing no significant differences in muscle-fiber composition between children and adults (8,10,53). Furthermore, children’s oxidative metabolic profile could be associated with a lower recruitment of their Type II muscle fibers during high–intensity exercise (13).
As mentioned above, the single supramaximal stimulus applied on the tibial nerve could potentially overestimate the level of activation compared to a doublet or a tetanic train of stimuli. This inaccuracy has been demonstrated for knee extensors in adults (4) and could possibly occur in children too. Despite the importance of accuracy, some children claimed that they could not afford a second stimulus because of pain, which could have had adverse effects in their performance. Nonetheless, this limitation should be considered in future studies by applying less painful procedures such as magnetic stimulation (41) or even submaximal electrical stimulation (3).
In the present study, we conclude that maximal isometric exercise protocol induces higher fatigability levels in men than in boys. After the fatigue-inducing protocol, the significantly higher decrements in peak twitch torque and RTDmax observed in men compared to boys reflect greater peripheral fatigability in men. On the other hand, a similar increase in the activation deficit indicates similar central fatigability for the two age groups examined. The present findings suggest that the greater fatigability resistance of prepubertal boys during sustained maximal contractions is explained mainly by peripheral rather than central factors.
K. Hatzikotoulas and D. Patikas contributed equally to this work. No external funding was received for this project.
The authors report no conflict of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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