Abstract
Purpose
The purpose of this study was to compare measurements of muscle strength, size, and activation of the forearm flexors in pre- and post-pubescent males and females.
Methods
Forty pre-pubescent (mean ± 95% confidence interval, age = 9.79 ± 0.35 years, n = 10 males, n = 10 females) and post-pubescent (age = 17.23 ± 0.58 years, n = 10 males, n = 10 females) youth participated. Subjects completed maximal voluntary isometric contractions (MVICs) of the forearm flexors, and submaximal isometric step muscle actions at 30, 50, and 70% of the peak MVIC. Percent voluntary activation (VA) was quantified during all isometric muscle actions. Forearm flexor (biceps brachii and brachialis) muscle cross-sectional area (CSA) was quantified from ultrasound images.
Results
MVIC strength was expressed in absolute terms and normalized to CSA. Post-pubertal males were 130% stronger, had 101% greater CSA, and 17% greater maximal VA than pre-pubertal males, while post-pubertal females were 72% stronger, had 54% greater CSA, and 23% greater maximal VA than pre-pubertal females. When MVIC strength was normalized to CSA, the post-pubertal males were still 15% stronger than the pre-pubertal males, while the post-pubertal females were only 12% stronger than the pre-pubertal females. The responses for VA across intensity reflected differences in muscle activation strategies between pre- and post-pubertal males and females.
Conclusion
These results suggest that muscle size may account for a greater proportion of the growth and development-related differences in strength among males, while females may be more affected by changes in muscle activation. Regardless of sex, changes in muscle size and neuromuscular function influence strength increases during growth and development.



Similar content being viewed by others
Availability of data and material
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Code availability
The custom-written software of this study is available from the corresponding author upon reasonable request.
Abbreviations
- ANOVA:
-
Analysis of variance
- BF%:
-
Percent body fat
- CSA:
-
Cross-sectional area
- FFM:
-
Fat-free mass
- MVIC:
-
Maximum voluntary isometric contraction
- PAR-Q:
-
Physical activity readiness questionnaire
- VA:
-
Voluntary activation
References
Allen G, Gandevia S, McKenzie D (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600. https://doi.org/10.1002/mus.880180605
Allen GM, McKenzie DK, Gandevia SC (1998) Twitch interpolation of the elbow flexor muscles at high forces. Muscle Nerve 21:318–328
Bergeron M, Mountjoy M, Armstrong N et al (2015) International Olympic Committee consensus statement on youth athletic development. Br J Sports Med 49:843–851. https://doi.org/10.1136/bjsports-2015-094962
Brozek J, Grande F, Anderson J, Keys A (1963) Densiometric analysis of body composition: revision of some quantitative assumptions. Ann NY Acad Sci 110:113–140
Chalchat E, Piponnier E, Bontemps B et al (2019) Characteristics of motor unit recruitment in boys and men at maximal and submaximal force levels. Exp Brain Res 237:1289–1302
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale, NJ
Fukunaga Y, Takai Y, Yoshimoto T et al (2014) Effect of maturation on muscle quality of the lower limb muscles in adolescent boys. J Physiol Anthopol 33:30. https://doi.org/10.1186/1880-6805-33-30
Gaudet G, Raison M, Maso FD et al (2016) Intra- and intersession reliability of surface electromyography on muscles actuating the forearm during maximum voluntary contractions. J Appl Biomech 32:558–570. https://doi.org/10.1123/jab.2015-0214
Gillen ZM, Shoemaker ME, McKay BD et al (2019) Muscle strength, size, and neuromuscular function before and during adolescence. Eur J Appl Physiol 119:1619–1632. https://doi.org/10.1007/s00421-019-04151-4
Granados A, Gebremariam A, Lee JM (2015) Relationship between timing of peak height velocity and pubertal staging in boys and girls. J Clin Res Pediatr Endocrinol 7:235–237. https://doi.org/10.4274/jcrpe.2007
Gravetter FJ, Wallnau LB (2017) Statistics for the behavioral sciences, 10th edn. Cengage Learning, Boston, MA
Greenhouse SW, Geisser S (1959) On methods in the analysis of profile data. Psychometrika 24:95–112
Grosset JF, Mora I, Lambertz D, Pérot C (2008) Voluntary activation of the triceps surae in prepubertal children. J Electromyogr Kinesiol 18:455–465. https://doi.org/10.1016/j.jelekin.2006.11.002
Hermens HJ (1999) SENIAM 8: European recommendations for surface electromyography, 2nd edn. Roessingh Research and Development, Enschede, the Netherlands
Housh TJ, Stout JR, Housh DJ, Johnson GO (1995a) The covariate influence of muscle mass on isokinetic peak torque in high school wrestlers. Pediatr Exerc Sci 7:176–182. https://doi.org/10.1123/pes.7.2.176
Housh TJ, Stout JR, Weir JP et al (1995b) Relationships of age and muscle mass to peak torque in high school wrestlers. Res Q Exerc Sport 66:256–261. https://doi.org/10.1080/02701367.1995.10608840
Housh TJ, Johnson GO, Housh DJ et al (1996) Validity of skinfold estimates of percent fat in high school female gymnasts. Med Sci Sports Exerc 28:1331–1335. https://doi.org/10.1097/00005768-199610000-00019
Housh TJ, Johnson GO, Housh DJ et al (1997) Isokinetic peak torque and estimated muscle cross-sectional area in high school wrestlers. J Strength Cond Res 11:45–49. https://doi.org/10.1519/00124278-199702000-00010
Housh TJ, Johnson GO, Housh DJ et al (2000) Estimation of body density in young wrestlers. J Strength Cond Res 14:477–482
Jackson AS, Pollock ML (1985) Practical assessment of body composition. Phys Sportsmed 13:76–90. https://doi.org/10.1080/00913847.1985.11708790
Jenkins N, Housh T, Buckner S et al (2016) Neuromuscular adaptations after 2 and 4 weeks of 80% versus 30% 1 repetition maximum resistance training to failure. J Strength Cond Res 30:2174–2185. https://doi.org/10.1519/JSC.0000000000001308
Kanehisa H, Ikegawa S, Tsunoda N, Fukunaga T (1995) Strength and cross-sectional areas of reciprocal muscle groups in the upper arm and thigh during adolescence. Int J Sports Med 16:54–60
Khairullah A, Klein LC, Ingle SM et al (2014) Testosterone trajectories and reference ranges in a large longitudinal sample of male adolescents. PLoS ONE 9:e108838. https://doi.org/10.1371/journal.pone.0108838
Klein KO, Martha PM Jr, Blizzard RM et al (1996) A longitudinal assessment of hormonal and physical alterations during normal puberty in boys. II. Estrogen levels as determined by an ultrasensitive bioassay. J Clin Endocrinol Metab 81:3203–3207. https://doi.org/10.1210/jc.81.9.3203
Kluka V, Martin V, Vicencio SG et al (2015) Effect of muscle length on voluntary activation level in children and adults. Med Sci Sports Exerc 47:718–724. https://doi.org/10.1249/MSS.0000000000000463
Kluka V, Martin V, Vicencio SG et al (2016) Effect of muscle length on voluntary activation of the plantar flexors in boys and men. Eur J Appl Physiol 116:1043–1051. https://doi.org/10.1007/s00421-016-3362-6
Lloyd R, Cronin J, Faigenbaum A et al (2016) National strength and conditioning association position statement on long-term athletic development. J Strength Cond Res 30:1491–1509. https://doi.org/10.1519/JSC.0000000000001387
Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–303. https://doi.org/10.1136/adc.44.235.291
Marshall WA, Tanner JM (1970) Variations in the pattern of pubertal changes in boys. Arch Dis Child 45:13–23. https://doi.org/10.1136/adc.45.239.13
Martin V, Kluka V, Vicencio SG et al (2015) Children have a reduced maximal voluntary activation level of the adductor pollicis muscle compared to adults. Eur J Appl Physiol 115:1485–1491. https://doi.org/10.1007/s00421-015-3132-x
Mirwald RL, Baxter-Jones ADG, Bailey DA, Beunen GP (2002) An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc 34:689–694. https://doi.org/10.1097/00005768-200204000-00020
Morris SB, DeShon RP (2002) Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. Psychol Methods 7:105–125. https://doi.org/10.1037/1082-989x.7.1.105
Neu CM, Rauch F, Rittweger J et al (2002) Influence of puberty on muscle development at the forearm. Am J Physiol Endocrinol Metab 283:103–107. https://doi.org/10.1152/ajpendo.00445.2001
Nielsen CT, Skakkebaek NE, Darling JA et al (1986) Longitudinal study of testosterone and luteinizing hormone (LH) in relation to spermarche, pubic hair, height and sitting height in normal boys. Acta Endocrinol Suppl 279:98–106
O’Brien TD, Reeves ND, Baltzopoulos V et al (2009) The effects of agonist and antagonist muscle activation on the knee extension moment–angle relationship in adults and children. Eur J Appl Physiol 106:849–856. https://doi.org/10.1007/s00421-009-1088-4
O’Brien TD, Reeves ND, Baltzopoulos V, Jones DA (2010) In vivo measurements of muscle specific tension in adults and children. Exp Physiol 95:202–210. https://doi.org/10.1113/expphysiol.2009.048967
Pişkin İE, Gümüş M, Bayraktaroğlu T et al (2018) Growth and pubertal development in adolescent male wrestlers. J Sports Med Phys Fit 58:852–856
Pitcher CA, Elliott CM, Williams SA et al (2012) Childhood muscle morphology and strength: alterations over six months of growth. Muscle Nerve 46:360–366. https://doi.org/10.1002/mus.23326
Round JM, Jones DA, Honour JW, Nevill AM (1999) Hormonal factors in the development of differences in strength between boys and girls during adolescence: a longitudinal study. Ann Hum Biol 26:49–62. https://doi.org/10.1080/030144699282976
Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428
Tonson A, Ratel S, Fur YL et al (2008) Effect of maturation on the relationship between muscle size and force production. Med Sci Sports Exerc 40:918–925. https://doi.org/10.1249/MSS.0b013e3181641bed
Vincent WJ, Weir JP (2012) Statistics in kinesiology, 4th edn. Human Kinetics, Champaign, IL
Warburton DER, Jamnik VK, Bredin SSD, Gledhill N (2011) The physical activity readiness questionnaire for everyone (PAR-Q+) and electronic physical activity readiness medical examination (ePARmed-X+). Health Fit J Can 4:3–23
Weir JP (2005) Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res 19:231–240
Wood LE, Dixon S, Grant C, Armstrong N (2004) Elbow flexion and extension strength relative to body or muscle size in children. Med Sci Sports Exerc 36:1977–1984. https://doi.org/10.1249/01.MSS.0000145453.02598.7E
Wood LE, Dixon S, Grant C, Armstrong N (2006) Elbow flexor strength, muscle size, and moment arms in prepubertal boys and girls. Pediatr Exerc Sci 18:457–469. https://doi.org/10.1123/pes.18.4.457
Zacharias L, Rand WM (1983) Adolescent growth in height and its relation to menarche in contemporary American girls. Ann Hum Biol 10:209–222. https://doi.org/10.1080/03014468300006381
Acknowledgements
We would like to thank the National Strength and Conditioning Association, the University of Nebraska Agriculture Research Division, and Abbott Nutrition for funding this study. We would also like to thank Nicholas Bohannon and Sydney Gibson for their help conducting the study, as well as each of the subjects for their participation.
Funding
Efforts for this study were funded, in part, by a National Strength and Conditioning Association Foundation (NSCAF) Graduate Research Doctoral Grant, the University of Nebraska Agriculture Research Division with funds provided by the Hatch Act (Agency: U.S. Department of Agriculture, National Institute of Food and Agriculture; Accession No: 1000080; Project No: NEB-36-078), and a grant from Abbott Nutrition, Columbus, OH.
Author information
Authors and Affiliations
Contributions
ZMG was a substantial contributor to the study concept and design, carried out data acquisition, analysis, and interpretation, and wrote the manuscript. TJH, RJS, TJH, and RJDA contributed to the study concept and design, and manuscript revision. MES contributed to data acquisition and manuscript revision. JTC was the primary manuscript reviser and a substantial contributor to the study concept, design, and interpretation. All authors provided critical feedback and approved the final version of the manuscript. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed. All the authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to report.
Ethical approval
This study was approved by the University of Nebraska-Lincoln’s Institutional Review Board (IRB) for the protection of human subjects (IRB Approval #: 20190719446FB, Title: Muscle Strength, Size, and Neuromuscular Function in Pre-pubescent and Post-pubescent Boys and Girls).
Informed consent
Before any data collection, pre-pubescent subjects signed an approved child assent form, while post-pubescent subjects signed an approved youth assent form, and one parent or legal guardian signed an approved parental consent form. Each subject, with the assistance from their parent or legal guardian, completed the PAR-Q + 2015 and was included in this study if questions 1–7 were answered “no” or all of the follow-up questions of the PAR-Q + 2015 were answered “no.”
Additional information
Communicated by William J. Kraemer.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gillen, Z.M., Housh, T.J., Schmidt, R.J. et al. Comparisons of muscle strength, size, and voluntary activation in pre- and post-pubescent males and females. Eur J Appl Physiol 121, 2487–2497 (2021). https://doi.org/10.1007/s00421-021-04717-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-021-04717-1