Neuromuscular Differences Between Men and Prepubescent Boys

Pediatric Exercise Science, 2010, 22, 205-217 © 2010 Human Kinetics, Inc.

Neuromuscular Differences Between Men and Prepubescent Boys During a Peak Isometric Knee Extension Intermittent Fatigue Test Vasilios Armatas, Eleni Bassa, Dimitrios Patikas, Ilias Kitsas, Georgios Zangelidis, and Christos Kotzamanidis Aristotle University The aim of this study was to examine the fatigue and recovery in boys and men during a maximal intermittent isometric fatigue test of the knee extensor muscles, by evaluating the electromyogram of vastus lateralis, vastus medialis and biceps femoris. Thirteen boys (10.0 ± 0.8yrs) and 13 men (26.1 ± 4.2yrs) were fatigued until torque reached 50% of its initial value. Three and 6 min after, a maximal isometric knee extension test was assessed. Men had faster torque decline during fatigue and slower torque recovery compared with boys. Agonist activity declined in both groups during fatigue but men had greater extent of reduction. After 6 min boys recovered fully in respect to agonist EMG, whereas this was not the case for the men. The lower level of fatigue and faster recovery in boys could be attributed to the limited inhibition that was observed in the boys’ agonist muscles, whereas the antagonist activity does not seem to play a role in the fatigue or recovery differences between the groups.

Muscular fatigue, defined as the reduction in the force-generating capacity of the neuromuscular system that occurs during sustained activity (3) is affected by many factors, such as the contraction type and intensity (15), the joint type (4) and angle (5), motivation (18), gender (21,26) and age (25). Moreover, the process of recovery from fatigue depends on numerous factors, including ATP and high-energy phosphates resynthesis (46), removal rate of metabolic by-products (22), muscle fiber distribution (16) and gender (9). Although muscle fatigue has been extensively studied in adults, a limited number of studies concerning children’s neuromuscular response to fatigue during intense fatiguing contractions is only available. Comparisons between children and adults have shown that children are more fatigue resistant and recover faster when Armatas, Bassa, Patikas, Zangelidis, and Kotzamanidis are with the Laboratory of Coaching and Sport Performance, Dept. of Physical Education and Sport Sciences, Aristotle University, Thessaloniki, Greece. Kitsas is with the Dept. of Electrical and Computer Engineering, Aristotle University, Thessaloniki, Greece.

205

206 Armatas et al.

fatigue tasks include repeated dynamic contractions, such as Wingate test (22), sprints (36,37), maximal isokinetic (29,33,49) and maximal sustained contractions (18,31). The influence of age in fatigability during high intensity exercise was attributed to various factors, such as the differences in muscle mass, motor unit activation, distribution of motor unit types and metabolites accumulation (18,35,39). On the other hand, when examining the knee extensors during a maximal sustained contraction, no differences in fatigue were detected between children and adults (42). Nonetheless, the agonist and antagonist muscle activity and the recovery process in that study was not evaluated. In this context, the purpose of the current study was to examine the fatigue and recovery in prepubescent boys and men during a maximal intermittent isometric fatigue test of the knee extensor muscles, by evaluating also the agonist and antagonist muscle activity. Our hypothesis is that the torque production and the neuromuscular activation during fatigue and recovery will be influenced by the age group of the participants when the fatigue protocol is consisted of intermittent maximal knee extensions.

Methods Participants Thirteen men and thirteen prepubescent boys, all with right dominant side, participated in this study (Table 1). None of the participants were involved in intensive training, while all of them were healthy, without any lower limb injury history or neuromuscular diseases. All participants, and the boy’s parents as well, obtained the written consent before participation in the experimental procedure. All boys were classified as prepubescent (stage 1,2) by a pediatrician according to Tanner criteria (43). The body fat mass was calculated using a skin-fold caliper and was expressed as percentage of body mass (41). Participants with greater than 25% fat mass were excluded (47). Skin-folds were measured three times and the average value was estimated. The experimental procedures were performed according to the code of ethics of the Aristotle University of Thessaloniki (Greece). Table 1 Participants’ Physical Characteristics Boys (n = 13)

Men (n = 13)

p values

Age (y)

10.0 ± 0.8

26.18 ± 4.2

0.002

Height (m)

1.46 ± 0.06

1.81 ± 0.14

0.030

Body mass (kg)

44.2 ± 6.2

80.1±16.9

94db). The analog signals of the torque and EMG were converted to digital using a 16-bit A/D card with a sample frequency of 1 kHz. All data were stored for further off-line analysis. EMG signal was fully rectified. Torque and EMG activity were expressed as a percentage of their maximum prefatigue values. During the fatigue protocol values were averaged for every 10% of the total protocol duration. The EMG analysis included signal of 1 s duration which included the peak torque of each bout. The average EMG (aEMG) was calculated from the fully rectified EMG. The power spectral density was computed by means of fast-Fourier transform and the mean power frequency (MPF) was calculated as described by Kwatny et al. (30).

Statistics Results are presented as mean values and standard deviation (SD). The dependent variables were the knee extension torque, the aEMG and MPF of the VL, VM and BF muscles, which were normalized to the initial prefatigue value. A two-way analysis of variance (ANOVA) with repeated measurements for time was assessed. Post hoc Scheffé tests were used to examine differences between paired means. The level of significance was set at p < .05. Statistical tests were performed using SPSS v14.0 (LEAD Technologies Inc, USA).

Results During Fatigue Torque was reduced to 50% of MVC after 56.3 ± 8.0 and 34.8 ± 7.6 repetitions in prepubescent boys and men, respectively, and this difference was statistically significant. The ratings of perceived exertion in were significantly lower compared with men (3.2 ± 0.7 vs. 7.2 ± 0.8, respectively) after the fatigue protocol.

Fatiguing Differences Between Men and Prepubertal Boys 209

Torque decreased gradually for both groups during the fatigue protocol, but men had a more rapid reduction than boys. This was revealed by the significant interaction of the analysis of variance. More specifically, men differentiate statistically significant their torque from the initial value earlier than boys (20% and 70% of the total repetitions for men and boys, respectively). The differences between the age groups were statistically significant for most of the part of the fatigue protocol (between the 10% and 80% of repetitions) with the boys having higher mean values (Figure 1). The aEMG of the examined agonist muscles decreased during the fatigue protocol more in men than in boys. More specifically at the end of the protocol the VM activity reached the 58% and 86% of the initial value for men and boys, respectively. The difference between the groups was statistically significant after the 50% of repetitions. Compared with the initial values, only men showed decreased VM amplitude at the second half of the fatigue protocol (Figure 2A). The VL amplitude decreased at 58% of the initial value for the men’s group and at 83% for the boys’ group. The difference between the groups was significant after the 10% of repetitions. Furthermore, men had significantly lower values in respect to the initial after the 20% of repetitions, whereas boys showed significant decrease only at the end of the fatigue protocol (Figure 2B). Regarding the antagonistic

Figure 1 — Change in torque as percentage of the initial in men and boys during the fatigue protocol. *= statistically significant difference of torque between age groups. #= statistically significant difference compared with the initial value.

Figure 2 — Changes in vastus medialis (A), vastus lateralis (B) and biceps femoris (C) average EMG amplitude (as percentage of the initial) for men and boys during the fatigue protocol. *= statistically significant difference of torque between age groups. #= statistically significant difference compared with the initial value.

210


activity, the BF amplitude showed no statistically significant differentiation during the fatigue protocol compared with the initial value. Moreover, boys on average tended to have smaller decrease in amplitude, although no statistical significant difference between the groups was observed (Figure 2C). Concerning MPF, the initial values were not significantly different between men and boys for the VM (97.3 ± 9.7 vs. 90.5 ± 10.6 Hz) and VL (92.8 ± 10.5 vs. 88.3 ± 8.1 Hz). MPF declined for both groups during MIFP for all muscles (Figure 3). More specifically for VM and VL, significant differentiation between groups was shown after the 60% of repetitions, while no significant differences were found for BF during MIFP. Compared with the initial values, the MPF of VM and VL showed significant difference in men after the 60% and 70% of repetitions, respectively. Boys showed significantly lower MPF for the VL only at the end of the MIFP. BF did not show any significant difference.

During Recovery A summary of the results concerning recovery is presented in Table 2. Torque showed a faster recovery in boys than in men. Specifically, after third minute of recovery boys showed almost complete recovery, while men did not fully recover after six minutes. Table 2 Mean ± SD of Torque, Average Electromyogram (aEMG) and Mean Power Frequency (MPF) of the Electromyogram for Men and Boys During Recovery Recovery time Torque aEMG

Men VM VL

MPF

0 min

3 min

6 min

48.3 ± 3.3

84.2 ± 12.0

89.7 ± 7.3

Boys

49.9 ± 0.3

97.9 ± 10.1*

102.4 ± 8.0*

Men

54.1 ± 17.1

75.3 ± 26.4

82.2 ± 27.7

Boys

85.5 ± 16.7

98.6 ± 19.1*

102.6 ± 20.8*

Men

58.3 ± 14.5

80.4 ± 15.3

84.5 ± 16.7

Boys

82.4 ± 12.9

97.5 ± 15.5*

99.9 ± 16.0*

BF

Men

83.4 ± 7.4

96.0 ± 30.6

99.1 ± 29.4

Boys

88.9 ± 21.4

101.7 ± 20.5

104.3 ± 19.2

VM

Men

58.7 ± 6.0

61.9 ± 7.4

68.6 ± 9.1

Boys

90.7 ± 13.8

94.2 ± 16.7*

97.3 ± 11.5*

Men

60.7 ± 8.6

67.2 ± 6.5

69.5 ± 7.7

Boys

82.5 ± 6.7

86.4 ± 10.5

91.9 ± 10.1*

Men Boys

80.8 ± 9.5 94.4 ± 12.7

85.8 ± 11.1 95.5 ± 5.8

89.2 ± 10.2 103.6 ± 13.1

VL BF

Note. Electromyographic data are presented from the vastus medialis (VM), vastus lateralis (VL) and biceps femoris (BF). All values are presented in % of the initial prefatigue value during the MVC. Asterisks indicate significant difference between men and boys.

Figure 3 — Changes in vastus medialis (A), vastus lateralis (B) and biceps femoris (C) mean power frequency (MPF) of the EMG signal (as percentage of the initial) for men and boys during the fatigue protocol. *= statistically significant difference of torque between age groups. #= statistically significant difference compared with the initial value.

212


The VM amplitude was significantly higher in boys during the 3rd and 6th minute of recovery. In contrast with boys, men’s aEMG did not fully recover to the prefatigue ones after 6 min of rest. Similar results were observed for the VL as well. Thereby, boys presented higher VL activation 3 and 6 min after the end of the fatigue protocol compared with men. On the other hand, BF antagonist activity during recovery did not reveal any significant differences between measurements or between groups. During recovery boys presented in general higher MPF values for VM and VL. In particular for the VM, boys showed significantly higher values three and six minutes after MIFP compared with men, whereas for the VL significant differences were only found six minutes after the protocol. No significant differences were found for the BF, although boys presented higher values.

Discussion The present study examined the effects of age during the developmental period in maximal voluntary knee extension torque alteration and agonist-antagonist muscle activation, during an intermittent isometric fatigue test. The main findings indicated that prepubescent boys were less fatigued compared with men during MIFP and had faster recovery.

During Fatigue During MIFP men showed earlier torque reduction than boys. This could be supported by previous studies comparing boys and men during maximal sustained fatigue tests in other joints (18,31) and more specifically during maximal isokinetic ones for the knee extensors (33,49). Similar results were also reported after intermittent maximal protocols performed in cycle ergometer (37) and Wingate test (22). However, in a recent study men and boys had similar rate of fatigue after a 2-min maximal voluntary isometric knee extension (42). Nonetheless, twitch interpolation technique with 100 Hz stimulation which was repeatedly used in this study (42) could have probably caused more discomfort in children and possibly diminished their effort (40). The differences in fatigue between boys and men are attributed to either muscular and/or neural mechanisms. Regarding the former, Van Praagh and Dore (45) claimed that when children and adults perform the same relative work, children generate lower absolute power values and this could explain their greater resistance to fatigue. In other words, given that the muscle mass is correlated with the power output during growth, the greater fatigue resistance in children might be related to the fact that lower muscle mass is involved during exercise (38). Besides, children have a higher proportion of slow type fibers (27), which may explain why children have lower rate of glycolytic metabolite accumulation and pH decrease (11). Children rely less on glycolytic pathways during high-intensity exercise, and hence have lower metabolites accumulation (39,49). In addition, children require less time to replenish the half of the consumed PCr and hence, during the intermittent maximal exercise, the interval between the maximal trials could have a greater recovery effect for the children than for the men (44). Therefore, the prepubescent

214 Armatas et al.

boys of the current study could probably recover faster during the interval between the maximal trials due to the rapid onset of oxidative energy production at the onset of exercise (1,7,8,39). Another finding of the current study, indicative of less fatigability in boys, is that of the rating of perceived exertion is lower in boys and this is in agreement with previous studies (2,36,39,48). However, the physiological underlying mechanisms used to determine the ratings of perceived exertion are not fully understood. Regarding the neuronal mechanisms, agonist activity in the current study showed reduction for both age groups, as it was observed previously in maximal isometric fatigue tasks in men (32,34) and boys (18,31). The reduction was more pronounced in men and this has been observed in previous studies for both maximal sustained contraction for the elbow flexors (18) and isokinetic (33) fatigue tests. An explanation for the decrease in agonist EMG could be based on the assumption that men have more type II motor units, which are more susceptible to fatigue (18). Moreover, the higher metabolite accumulation observed in men compared with boys (39) possibly causes higher presynaptic inhibition on a-motoneurone by activating in a higher extent the type III and IV afferents (12). The lower EMG decrease in the children could be attributed to a possibly incomplete activation of the available motor units, which implies that the high threshold, and more fatigable type II motor units were not recruited. This concept was supported by Halin et al. (17) based on data of fast-Fourier transform analysis for the elbow flexors. However, our data showing no differences in mean power frequency between boys and men, indicating that this issue is possibly muscledependent. Moreover, recent studies using interpolated twitch technique claimed that children and adults have similar level of motor unit activation regarding the plantar flexors (14,19) and the knee extensors (42). Hence, the most plausible cause for the higher agonist EMG decrease in men could be based on metabolic factors. The important role of the metabolic factors is also supported by the higher MPF decrease in the men of the current study, which is in agreement with a previous one (18) and indicates a reduced conduction velocity of the action potentials over the muscle fibers as a result of higher metabolic accumulation in the muscle. The studies in adults related with antagonist activity during maximal isometric fatigue tests are conflicting showing unaltered (34) or decreased (32) amplitude. Hence, this issue requires further research. Regarding children and their antagonistic activity during fatigue, there is only one study in the literature using a maximal isokinetic test (33). This study showed that antagonist activity of adults remained constant throughout fatigue test while children showed an initial increase followed by a decrement and an increment at the end of the test, possibly due to discomfort. In the current study however, antagonist activity did not change in boys and men and hence could not explain their differences in fatigability during an intermittent maximal isometric fatigue test.

During Recovery The results of the torque output during recovery are in accordance with previous studies (6,22,35,49), showing that boys recovered faster than men. In our study boys reached their initial torque values even after three minutes.


The faster torque recovery in boys could be attributed to their higher PCr resynthesis, higher muscle oxidative activity and shorter mean diffusion distance (6). Conversely, men’s torque did not reach initial values even after 6 min of recovery, which is in line with findings about PCr full recovery that is not achieved even 5 min after the fatigue task (23). The activity of the agonist muscles recovered faster in boys compared with men. The full agonist EMG recovery observed in prepubescent boys is in agreement with previous studies (20,29). Although some studies reported that VM and VL are fatigued to a similar extent (13) others support that VL is more fatigable than VM (10,29). These differences can be attributed to various factors such as the different used protocols, the selected sample, and the electrode placement. Concerning antagonist activity during recovery process, there were no significant differences between groups. Antagonist activity of boys remained constant during recovery. Kotzamanidou et al. (29) showed no differences between boys and young adults on the antagonist muscle, 3, 6 and 9 min after an isokinetic fatigue task at 60°/s. Therefore, the obtained results indicate that antagonist activity does not contribute to the faster torque recovery in boys. In conclusion, men and boys respond differently to fatigue and recovery after a repeated intermittent maximal isometric fatigue protocol for the knee extensors. This study gives evidence that prepubescent boys are more fatigue resistant and this fact could be attributed to a more limited inhibition of their agonist muscles, while the antagonist activity was not differentiated between the two groups.

References 1. Armon, Y. D.M., Cooper, R., Flores, S. Zanconato, and T.J. Barstow. Oxygen uptake during high-intensity exercise in children and adults. J. Appl. Physiol. 39:65–76, 1991. 2. Bar-Or, O., and D.S. Ward. Rating of perceived exertion in children. In: Advances in pediatric sports sciences, O. Bar-Or (Ed.). Champaign, IL: Human Kinetics, 1989, pp. 151–168. 3. Bigland-Ritchie, B.R., R.S. Johansson, O.C. Lippold, and J.J. Woods. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J. Neurophysiol. 50(1):313–324, 1983. 4. Clark, B., T. Manini, D. The, N. Doldo, and L. Ploutz-Snyder. Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. J. Appl. Physiol. 94:2263–2272, 2003. 5. Croce, R.V., J.P. Miller, and P. St. Pierre. Effect of ankle position fixation on peak torque and electromyographic activity of the knee flexors and extensors. Electromyogr. Clin. Neurophysiol. 40(6):365–373, 2000. 6. Falk, B., and R. Dotan. Child-adult differences in the recovery from high-intensity exercise. Exerc. Sport Sci. Rev. 34:107–112, 2006. 7. Fawkner, S.G. N., Armstrong, C.R., Potter, and J.R., Welsman. Oxygen uptake kinetics in children and adults after the onset of moderate-intensity exercise. J Sports Sci. 20(4):319–326, 2002. 8. Fawkner, SG., and N., Armstrong. Oxygen uptake kinetic response to exercise in children. Sports Med. 33(9):651–669, 2003. 9. Fulco, C., P. Rock, S. Muza, et al. Slower fatigue and faster recovery of the adductor pollicis in women matched for strength with men. Acta Physiol. Scand. 167:233–239, 1999. 10. Gabriel, Y.F. Comparing fatigue and the rate of recovery between vastus medialis oblique and vastus laterals. Phys. Ther. Sport. 3(3):118–123, 2002.

216 Armatas et al.

11. Gaitanos, G.C., C. Williams, L.H. Boobis, and S. Brooks. Human muscle metabolism during intermittent maximal exercise. J. Appl. Physiol. 75:712–719, 1993. 12. Gandevia, S.C. Spinal and supraspinal factors in human muscle fatigue. Physiol. Rev. 81(4):1725–1789, 2001. 1 3. Grabiner, M.D., T.J. Koh, and G.F. Miller. Fatigue rates of vastus medialis oblique and vastus lateralis during static and dynamic knee extension. J. Orthop. Res. 9:391–397, 1991. 14. Grosset, J., I. Mora, D. Lambertz, and C. Perot. Voluntary activation of the triceps surae in prepubertal children. J. Electromyogr. Kinesiol. 18(3):455–465, 2006. 15. Hakkinen, K. Neuromuscular fatigue and recovery in male and female athletes during heavy resistance exercise. Int. J. Sports Med. 14:53–59, 1993. 16. Hakkinen, K., and E. Myllyla. Acute effects of muscle fatigue and recovery on force production and relaxation in endurance, power and strength athletes. J Sports Med Phys Fitness. 30:5–12, 1990. 17. Halin, R., P. Germain, O. Buttelli, and B. Kapitaniak. Differences in strength and surface electromyogram characteristics between pre-pubertal gymnasts and un-trained boys during brief and maintained isometric voluntary contractions. Eur. J. Appl. Physiol. 87:409–415, 2002. 18. Halin, R., P. Germain, S. Bercier, B. Kapitaniak, and O. Buttelli. Neuromuscular response of young boys versus men during sustained maximal contraction. Med. Sci. Sports Exerc. 35:1042–1048, 2003. 19. Hatzikotoulas, K., D. Patikas, E. Bassa, I. Paraschos, and C. Kotzamanidis. Differences in voluntary activation between adult and prepubertal males. In: Children and exercise XXIV: The Proceedings of the 24th Pediatric Work Physiology Meeting, T. Jurimae, N. Amstrong, and J. Jurimae (Eds.). Oxon: Routledge, 2008, pp. 247-251. 20. Hatzikotoulas, K., E. Bassa, D. Patikas, Y. Koutedakis, L. Hatjileontiadis, and C. Kotzamanidis. Submaximal fatigue and recovery in boys and men. Int. J. Sports Med., in press. 21. Hatzikotoulas, K., T. Siatras, E. Spyropoulou, I. Paraschos, and D. Patikas. Muscle fatigue and electromyographic changes are not different in women and men matched for strength. Eur. J. Appl. Physiol. 92:298–304, 2004. 22. Hebestreit, H., K.I. Mimura, and O. Bar-Or. Recovery of muscle power after highintensity short-term exercise: comparing boys and men. J. Appl. Physiol. 74:2875–2880, 1993. 23. Henriksson, J., A. Katz, and K. Sahlin. Redox state changes in human skeletal muscle after isometric contraction. J. Physiol. 380:441–451, 1986. 24. Hermens, H.J., B. Freriks, R. Merletti, G. Hagg, D. Stegeman, and J. Blok. SENIAM 8: European recommendations for surface electromyography, ISBN: 90-75452-15-2: Roessingh Research and Development, 1999. 25. Hunter, S.K., A. Critchlow, I. Shin, and R.M. Enoka. Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. J. Appl. Physiol. 96:195–202, 2004. 26. Hunter, S.K., and R.M. Enoka. Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J. Appl. Physiol. 91:2686–2694, 2001. 27. Jansson, E. Age-related fiber type changes in human skeletal muscle. In: Biochemistry of Exercise IX, R.J. Maughan and S.M. Shireffs (Eds.). Champaign, IL: Human Kinetics, 1996, pp. 297–307. 28. Kellis, E. Antagonist moment of force during maximal knee extension in pubertal boys: effects of quadriceps fatigue. Eur. J. Appl. Physiol. 89:271–280, 2003. 29. Kotzamanidou, M., I. Michailidis, K. Hatzikotoulas, A. Hasani, E. Bassa, and C. Kotzamanidis. Differences in recovery process between adult and prepubertal males after a maximal isokinetic fatigue task. Isokinet. Exerc. Sci. 13:261–266, 2005. 30. Kwatny, E. D.H., Thomas, and H.G. Kwatny. An application of signal processing techniques to the study of myoelectric signals. IEEE Trans. Biomed. Eng. 17(4):303–313, 1970.


31. Moritani, T., S. Oda, M. Shibata, T. Matsumoto, and F. Mimasa. Myoelectric signal characteristics in lumbar back muscle fatigue among adult males, females and prepuberty boys. J. Sports Med. Sci. 5(1):13–21, 1991. 32. Mullany, H., M. O’Malley, A. St.Clair Gibson, and C. Vaughan. Agonist-antagonist common drive during fatiguing knee extension efforts using surface electromyography. J. Electromyogr. Kinesiol. 12(5):375–384, 2002. 33. Paraschos, I., A. Hassani, E. Bassa, K. Hatzikotoulas, D. Patikas, and C. Kotzamanidis. Differences in neuromuscular activation between adults and prepubertal males during maximal isokinetic knee extension fatigue test. Int. J. Sports Med. 28(11):958–963, 2007. 34. Patikas, D., C. Michailidis, E. Bassa, et al. Electromyographic changes of agonist and antagonist calf muscles during maximum isometric induced fatigue. Int. J. Sports Med. 23:285–289, 2002. 35. Ratel, S., A. Tonson, Y. Le Fur, P. Cozzone, and D. Bendahan. Comparative analysis of skeletal muscle oxidative capacity in children and adults: a 31P-MRS study. Appl. Physiol. Nutr. Metab. 33(4):720–727, 2008. 36. Ratel, S., C.A. Williams, J. Oliver, and N. Armstrong. Effects of age and mode of exercise on power output profiles during repeated sprints. Eur. J. Appl. Physiol. 92:204–210, 2004. 37. Ratel, S., M. Bedu, A. Hennegrave, E. Doré, and P. Duché. Effects of age and recovery duration on peak power output during repeated cycling sprints. Int. J. Sports Med. 23:397–402, 2002. 38. Ratel, S., N. Lazaar, C.A. Williams, M. Bedu, and P. Duché. Age differences in human skeletal muscle fatigue during high-intensity intermittent exercise. Acta Paediatr. 92:1248–1254, 2003. 39. Ratel, S., P. Duché, and C.A. Williams. Muscle fatigue during high intensity exercise in children. Sports Med. 36(12):1031–1065, 2006. 40. Shield, A., and S. Zhou. Assessing voluntary muscle activation with the twitch interpolation technique. Sports Med. 34:253–267, 2004. 41. Slaughter, M.H., T.G. Lohman, R.A. Boileau, et al. Skinfold equations for estimation of body fatness in children and youth. Hum. Biol. 60(5):709–723, 1988. 42. Streckis, V., A. Skurvydas, and A. Ratkevicius. Children are more susceptible to central fatigue than adults. Muscle Nerve. 36:357–363, 2007. 43. Tanner, J.M. Growth at Adolescence, 2nd ed. Oxford: Blackwell Scientific, 1962. 44. Taylor, D.J., G.J. Kemp, C.H. Thompson, and G.K. Radda. Ageing:effects on oxidative capacity function of skeletal muscle in vivo. Mol. Cell. Biochem. 174(1-2):321–324, 1997. 45. Van Praagh, E., and E. Doré. Short-term muscle power during growth and maturation. Sports Med. 32:701–728, 2002. 46. Vollestad, K.K., O.M. Sejersted, R. Bahr, J.J. Woods, and B. Bigland-Ritchie. Motor drive and metabolic responses during repeated submaximal contractions in humans. J. Appl. Physiol. 64:1421–1427, 1988. 47. Williams, D.P., S.B. Going, T.G. Lohman, et al. Body fatness and risk for elevated blood pressure, total cholesterol and serum lipoprotein ratios in children and adolescents. Am. J. Public Health. 83:358–363, 1992. 48. Williams, J.G., R.G. Eston, and B. Furlong. CERT: a perceived exertion scale for young children. Percept. Mot. Skills. 79:1451–1458, 1994. 49. Zafeiridis, A., A. Dalamitros, K. Dipla, V. Manou, N. Galanis, and S. Kellis. Recovery during high-intensity intermittent anaerobic exercise in boys, teens and men. Med. Sci. Sports Exerc. 37:505–512, 2005.