Advertisement

European Journal of Applied Physiology

, Volume 119, Issue 7, pp 1619–1632 | Cite as

Muscle strength, size, and neuromuscular function before and during adolescence

  • Zachary M. Gillen
  • Marni E. Shoemaker
  • Brianna D. McKay
  • Nicholas A. Bohannon
  • Sydney M. Gibson
  • Joel T. CramerEmail author
Original Article

Abstract

Purpose

To compare measurements of muscle strength, size, and neuromuscular function among pre-adolescent and adolescent boys and girls with distinctly different strength capabilities.

Methods

Fifteen boys (mean age ± confidence interval: 13.0 ± 1.0 years) and 13 girls (12.9 ± 1.1 years) were categorized as low strength (LS, n = 14) or high strength (HS, n = 14) based on isometric maximal voluntary contraction strength of the leg extensors. Height (HT), seated height, and weight (WT) determined maturity offset, while percent body fat and fat-free mass (FFM) were estimated from skinfold measurements. Quadriceps femoris muscle cross-sectional area (CSA) was assessed from ultrasound images. Isometric ramp contractions of the leg extensors were performed while surface electromyographic amplitude (EMGRMS) and mechanomyographic amplitude (MMGRMS) were recorded for the vastus lateralis (VL). Neuromuscular efficiency from the EMG and MMG signals (NMEEMG and NMEMMG, respectively) and log-transformed EMG and MMG vs. torque relationships were also used to examine neuromuscular responses.

Results

HS was 99–117% stronger, 2.3–2.8  years older, 14.0–15.7 cm taller, 20.9–22.3 kg heavier, 2.3–2.4 years more biologically mature, and exhibited 39–43% greater CSA than LS (p ≤ 0.001). HS exhibited 74–81% higher NMEEMG than LS (p ≤ 0.022), while HS girls exhibited the highest NMEMMG (p ≤ 0.045). Even after scaling for HT, WT, CSA, and FFM, strength was still 36–90% greater for HS than LS (p ≤ 0.031). The MMGRMS patterns in the LS group displayed more type I motor unit characteristics.

Conclusions

Neuromuscular adaptations likely influence strength increases from pre-adolescence to adolescence, particularly when examining large, force-producing muscles and large strength differences explained by biological maturity, rather than simply age.

Keywords

Electromyography Mechanomyography Isometric strength Youth 

Abbreviations

BF

Biceps femoris

BF%

Body fat percent

CSA

Cross-sectional area

EMG

Electromyography

FFM

Fat-free mass

HS

High strength

HT

Height

LS

Low strength

MMG

Mechanomyography

MVC

Maximum voluntary contraction

NME

Neuromuscular efficiency

VL

Vastus lateralis

WT

Weight

Notes

Acknowledgements

Efforts for this study were funded, in part, by 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 contributions

All authors conceived and designed the research. ZMG, MES, BDM, NAB, and SMG contributed to the data collection and analysis. ZMG and JTC wrote the manuscript. MES, BDM, NAB, SMG, and JTC contributed edits, feedback, and suggestions for the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interest.

References

  1. Akataki K, Mita K, Watakabe M, Itoh K (2003) Mechanomyographic responses during voluntary ramp contractions of the human first dorsal interosseous muscle. Eur J Appl Physiol 89:520–525Google Scholar
  2. Akataki K, Mita K, Watakabe M (2004) Electromyographic and mechanomyographic estimation of motor unit activation strategy in voluntary force production. Electromyogr Clin Neurophysiol 44:489–496Google Scholar
  3. Arabadzhiev TI, Dimitrov VG, Dimitrova NA, Dimitrov GV (2010) Interpretation of EMG integral or RMS and estimates of "neuromuscular efficiency" can be misleading in fatiguing contraction. J Electromyogr Kinesiol 20:223–232Google Scholar
  4. Barry DT, Cole NM (1990) Muscle sounds are emitted at the resonant frequencies of skeletal muscle. IEEE Trans Biomed Eng 37:525–531Google Scholar
  5. Beck TW, Housh TJ, Johnson GO, Weir JP, Cramer JT, Coburn JW, Malek MH (2006) Mechanomyographic and electromyographic responses during submaximal to maximal eccentric isokinetic muscle actions of the biceps Brachii. J Strength Cond Res 20:184–191Google Scholar
  6. Birat A, Bourdier P, Piponnier E, Blazevich AJ, Maciejewski H, Duché P, Ratel S (2018) Metabolic and fatigue profiles are comparable between prepubertal children and well-trained adult endurance athletes. Front Physiol 9:387Google Scholar
  7. Bouchant A, Martin V, Maffiuletti NA, Ratel S (2011) Can muscle size fully account for strength differences between children and adults? J Appl Physiol (1985) 110:1748–1749Google Scholar
  8. Brozek J, Grande F, Anderson JT, Keys A (1963) Densiometric analysis of body composition: revision of some quantitative assumptions. Ann N Y Acad Sci 110:113–140Google Scholar
  9. Castaingts V, Martin A, Van Hoecke J, Pérot C (2004) Neuromuscular efficiency of the triceps Surae in induced and voluntary contractions: morning and evening evaluations. Chronobiol Int 21:631–643Google Scholar
  10. Chaves SF, Marques NP, Silva RLE, Rebouças NS, de Freitas LM, de Paula Lima PO, de Oliveira RR (2012) Neuromuscular efficiency of the vastus medialis obliquus and postural balance in professional soccer athletes after anterior cruciate ligament reconstruction. Muscles Ligam Tend J 2:121–126Google Scholar
  11. Coburn JW, Housh TJ, Cramer JT, Weir JP, Miller JM, Beck TW, Malek MH, Johnson GO (2005) Mechanomyographic and electromyographic responses of the vastus medialis muscle during isometric and concentric muscle actions. J Strength Cond Res 19:412–420Google Scholar
  12. De Luca CJ (1997) The use of surface electromyography in biomechanics. J Appl Biomech 13:135–163Google Scholar
  13. De Ste Croix M (2007) Advances in paediatric strength assessment: changing our perspective on strength development. J Sports Sci Med 6(3):292–304Google Scholar
  14. De Luca CJ, Hostage EC (2010) Relationship between firing rate and recruitment threshold of motoneurons in voluntary isometric contractions. J Neurophysiol 104:1034–1046Google Scholar
  15. De Luca CJ, Kline JC (2012) Influence of proprioceptive feedback on the firing rate and recruitment of motoneurons. J Neural Eng 9(1):016007Google Scholar
  16. De Luca CJ, LeFever RS, McCue MP, Xenakis AP (1982) Behaviour of human motor units in different muscles during linearly varying contractions. J Physiol 329:113–128Google Scholar
  17. Deschenes MR, Giles JA, McCoy RW, Volek JS (2002) Neural factors account for strength decrements observed after short-term muscle unloading. Am J Physiol Regul Integr Comp Physiol 282:578–583Google Scholar
  18. DeVries HA (1968) "Efficiency of electrical activity" as a physiological measure of the functional state of muscle tissue. Am J Phys Med 47:11–22Google Scholar
  19. Doix AM, Gulliksen A, Brændvik SM, Roeleveld K (2013) Fatigue and muscle activation during submaximal elbow flexion in children with cerebral palsy. J Electromyogr Kinesiol 23:721–726Google Scholar
  20. Eriksson BO, Karlsson J, Saltin B (1971) Muscle metabolites during exercise in pubertal boys. Acta Paediatr Scand Suppl 217:154–157Google Scholar
  21. Eriksson BO, Gollnick PD, Saltin B (1973) Muscle metabolism and enzyme activities after training in boys 11–13 years old. Acta Physiol Scand 87:485–497Google Scholar
  22. Farina D, Merletti R, Enoka RM (2004) The extraction of neural strategies from the surface EMG. J Appl Physiol 96:1486–1495Google Scholar
  23. Fukunaga Y, Takai Y, Yoshimoto T, Fujita E, Yamamoto M, Kanehisa H (2014) Effect of maturation on muscle quality of the lower limb muscles in adolescent boys. J Physiol Anthropol 33(1):30Google Scholar
  24. Goldberg LJ, Derfler B (1977) Relationship among recruitment order, spike amplitude, and twitch tension of single motor units in human masseter muscle. J Neurophysiol 40(4):879–890Google Scholar
  25. Granacher U, Goesele A, Roggo K, Wischer T, Fischer S, Zuerny C, Gollhofer A, Kriemler S (2011) Effects and mechanisms of strength training in children. Int J Sports Med 32:357–364Google Scholar
  26. Grosset JF, Mora I, Lambertz D, Pérot C (2008) Voluntary activation of the triceps surae in prepubertal children. J Electromyogr Kinesiol 18(3):455–465Google Scholar
  27. Häkkinen K, Komi PV (1983) Electromyographic changes during strength training and detraining. Med Sci Sports Exerc 15:455–460Google Scholar
  28. Herda T, Cooper M (2015) Muscle-related differences in mechanomyography frequency–force relationships are model dependent. Med Biol Eng Comput 53:689–697Google Scholar
  29. Herda TJ, Weir JP, Ryan ED, Walter AA, Costa PB, Hoge KM, Beck TW, Stout JR, Cramer JT (2009) Reliability of absolute versus log-transformed regression models for examining the torque-related patterns of response for mechanomyographic amplitude. J Neurosci Methods 179:240–246Google Scholar
  30. Herda TJ, Housh TJ, Fry AC, Weir JP, Schilling BK, Ryan ED, Cramer JT (2010) A noninvasive, log-transform method for fiber type discrimination using mechanomyography. J Electromyogr Kinesiol 20:787–794Google Scholar
  31. Herda TJ, Walter AA, Costa PB, Ryan ED, Stout JR, Cramer JT (2011) Differences in the log-transformed electromyographic–force relationships of the plantar flexors between high- and moderate-activated subjects. J Electromyogr Kinesiol 21:841–846Google Scholar
  32. Herda TJ, Siedlik JA, Trevino MA, Cooper MA, Weir JP (2015) Motor unit control strategies of endurance- versus resistance-trained individuals. Muscle Nerve 52:832–843Google Scholar
  33. Herda TJ, Trevino MA, Sterczala AJ, Miller JD, Wray ME, Dimmick HL, Gallagher PM, Fry AC (2019) Muscular strength and power are correlated with motor unit action potential amplitudes, but not myosin heavy chain isoforms in sedentary males and females. J Biomech 86:251–255Google Scholar
  34. Hermens HJ (1999) SENIAM 8: European recommendations for surface electromyography. Roessingh Research and Development, Enschede, pp 45–46Google Scholar
  35. Housh TJ, Johnson GO, Housh DJ, Stout JR, Weir JP, Weir LL, Eckerson JM (1996) Isokinetic peak torque in young wrestlers. Pediatr Exerc Sci 8:143–155Google Scholar
  36. Housh TJ, Johnson GO, Housh DJ, Stout JR, Eckerson JM (2000) Estimation of body density in young wrestlers. J Strength Cond Res 14(4):477–482Google Scholar
  37. Jackson AS, Pollock ML (1985) Practical assessment of body composition. Phys Sportsmed 13(5):76–90Google Scholar
  38. Jakobi JM, Cafarelli E (1998) Neuromuscular drive and force production are not altered during bilateral contractions. J Appl Physiol 84:200–206Google Scholar
  39. Jenkins N, Housh T, Bergstrom H, Cochrane K, Hill E, Smith C, Johnson G, Schmidt R, Cramer J (2015) Muscle activation during three sets to failure at 80 vs. 30 % 1RM resistance exercise. Eur J Appl Physiol 115(11):2335–2347Google Scholar
  40. Jenkins ND, Miramonti AA, Hill EC, Smith CM, Cochrane-Snyman KC, Housh TJ, Cramer JT (2017) Greater neural adaptations following high- vs. low-load resistance training. Front Physiol 8:331Google Scholar
  41. Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles: an autopsy study. J Neurol Sci 18:111–129Google Scholar
  42. Kanehisa H, Ikegawa S, Tsunoda N, Fukunaga T (1995) Strength and cross-sectional areas of reciprocol muscle groups in the upper arm and thigh during adolescence. Int J Sports Med 16(1):54–60Google Scholar
  43. Kluka V, Martin V, Vicencio SG, Jegu A, Cardenoux C, Morio C, Coudeyre E, Ratel S (2015) Effect of muscle length on voluntary activation level in children and adults. Med Sci Sports Exerc 47(4):718–724Google Scholar
  44. Lambertz D, Mora I, Grosset J, Pérot C (2003) Evaluation of musculotendinous stiffness in prepubertal children and adults, taking into account muscle activity. J Appl Physiol 95(1):64–72Google Scholar
  45. Lawrence JH, De Luca CJ (1983) Myoelectric signal versus force relationship in different human muscles. J Appl Physiol 54:1653–1659Google Scholar
  46. MacIntosh BR, Gardiner PF, MacComas AJ (2006) Skeletal muscle. Human Kinetics, Champaign, pp 175–207Google Scholar
  47. Madeleine P, Bajaj P, Søgaard K, Arendt-Nielsen L (2001) Mechanomyography and electromyography force relationships during concentric, isometric and eccentric contractions. J Electromyogr Kinesiol 11:113–121Google Scholar
  48. Martin V, Kluka V, Garcia Vicencio S, Maso F, Ratel S (2015) Children have a reduced maximal voluntary activation level of the adductor pollicis muscle compared to adults. Eur J Appl Physiol 115(7):1485–1491Google Scholar
  49. Milner-Brown HS, Stein RB (1975) The relation between the surface electromyogram and muscular force. J Physiol 246(3):549–569Google Scholar
  50. Milner-Brown HS, Mellenthin M, Miller RG (1986) Quantifying human muscle strength, endurance and fatigue. Arch Phys Med Rehabil 67:530–535Google Scholar
  51. Mirwald RL, Baxter-Jones ADG, Bailey DA, Beunen GP (2002) An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc 34(4):689–694Google Scholar
  52. Moritani T, DeVries HA (1979) Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58:115–130Google Scholar
  53. Neu CM, Rauch F, Rittweger J, Manz F, Schoenau E (2002) Influence of puberty on muscle development at the forearm. Am J Physiol Endocrinol Metab 283(1):103–107Google Scholar
  54. O'Brien TD, Reeves ND, Baltzopoulos V, Jones DA (2010) In vivo measurements of muscle specific tension in adults and children. Exp Physiol 95(1):202–210Google Scholar
  55. Orizio C (1993) Muscle sound: bases for the introduction of a mechanomyographic signal in muscle studies. Crit Rev Biomed Eng 21:201–243Google Scholar
  56. Orizio C, Gobbo M, Diemont B, Esposito F, Veicsteinas A (2003) The surface mechanomyogram as a tool to describe the influence of fatigue on biceps brachii motor unit activation strategy. Historical basis and novel evidence. Eur J Appl Physiol 90:326–336Google Scholar
  57. Ozmun JC, Mikesky AE, Surburg PR (1994) Neuromuscular adaptations following prepubescent strength training. Med Sci Sports Exerc 26:510–514Google Scholar
  58. Pitcher CA, Elliott CM, Williams SA, Licari MK, Kuenzel A, Shipman PJ, Valentine JP, Reid SL (2012) Childhood muscle morphology and strength: Alterations over six months of growth. Muscle Nerve 46(3):360–366Google Scholar
  59. Pope ZK, Hester GM, Benik FM, DeFreitas JM (2016) Action potential amplitude as a noninvasive indicator of motor unit-specific hypertrophy. J Neurophysiol 115:2608–2614Google Scholar
  60. Ramsay JA, Blimkie CJ, Smith K, Garner S, MacDougall JD, Sale DG (1990) Strength training effects in prepubescent boys. Med Sci Sports Exerc 22:605–614Google Scholar
  61. Ratel S, Tonson A, Le Fur Y, Cozzone P, Bendahan D (2008) Comparative analysis of skeletal muscle oxidative capacity in children and adults: a 31P-MRS study. Appl Physiol Nutr Metab 33:720–727Google Scholar
  62. Rose J, McGill KC (2005) Neuromuscular activation and motor-unit firing characteristics in cerebral palsy. Dev Med Child Neurol 47:329–336Google Scholar
  63. Ryan ED, Cramer JT, Housh TJ, Beck TW, Herda TJ, Hartman MJ, Stout JR (2007) Inter-individual variability among the mechanomyographic and electromyographic amplitude and mean power frequency responses during isometric ramp muscle actions. Electromyogr Clin Neurophysiol 47:161Google Scholar
  64. Ryan ED, Cramer JT, Egan AD, Hartman MJ, Herda TJ (2008) Time and frequency domain responses of the mechanomyogram and electromyogram during isometric ramp contractions: a comparison of the short-time Fourier and continuous wavelet transforms. J Electromyogr Kinesiol 18:54–67Google Scholar
  65. Ryan ED, Thompson BJ, Herda TJ, Sobolewski EJ, Costa PB, Walter AA, Cramer JT (2011) The relationship between passive stiffness and evoked twitch properties: the influence of muscle CSA normalization. Physiol Meas 32(6):677–686Google Scholar
  66. Seger JY, Thorstensson A (2000) Muscle strength and electromyogram in boys and girls followed through puberty. Eur J Appl Physiol 81(1):54–61Google Scholar
  67. Stokes MJ, Dalton PA (1993) Acoustic myography: applications and considerations in measuring muscle performance. Isokinet Exerc Sci 3:4–15Google Scholar
  68. Tonson A, Ratel S, Le Fur Y, Cozzone P, Bendahan D (2008) Effect of maturation on the relationship between muscle size and force production. Med Sci Sports Exerc 40(5):918–925Google Scholar
  69. Trevino MA, Sterczala AJ, Miller JD, Wray ME, Dimmick HL, Ciccone AB, Weir JP, Gallagher PM, Fry AC, Herda TJ (2018) Sex-related differences in muscle size explained by amplitudes of higher-threshold motor unit action potentials and muscle fibre typing. Acta Physiol (Oxf) 225:e13151Google Scholar
  70. 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(2):3–23Google Scholar
  71. Weir JP, Housh TJ, Johnson GO, Housh DJ, Ebersole KT (1999) Allometric scaling of isokinetic peak torque: The nebraska wrestling study. Eur J Appl Physiol 80(3):240–248Google Scholar
  72. 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(11):1977–1984Google Scholar
  73. Xu K, He L, Mai J, Yan X, Chen Y (2015) Muscle recruitment and coordination following constraint-induced movement therapy with electrical stimulation on children with hemiplegic cerebral palsy: a randomized controlled trial. PLoS ONE 10:e0138608Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zachary M. Gillen
    • 1
  • Marni E. Shoemaker
    • 1
  • Brianna D. McKay
    • 1
  • Nicholas A. Bohannon
    • 1
  • Sydney M. Gibson
    • 1
  • Joel T. Cramer
    • 1
    Email author
  1. 1.Department of Nutrition and Health SciencesUniversity of Nebraska-LincolnLincolnUSA

Personalised recommendations