Are Prepubertal Children Metabolically Comparable to Well-Trained Adult Endurance Athletes?

Abstract

It is well acknowledged that prepubertal children have smaller body dimensions and a poorer mechanical (movement) efficiency, and thus a lower work capacity than adults. However, the scientific evidence indicates that prepubertal children have a greater net contribution of energy derived from aerobic metabolism in exercising muscle and reduced susceptibility to muscular fatigue, which makes them metabolically comparable to well-trained adult endurance athletes. For example, the relative energy contribution from oxidative and non-oxidative (i.e. anaerobic) sources during moderate-to-intense exercise, the work output for a given anaerobic energy contribution and the rate of acceleration of aerobic metabolic machinery in response to submaximal exercise are similar between prepubertal children and well-trained adult endurance athletes. Similar conclusions can be drawn on the basis of experimental data derived from intra-muscular measurements such as type I fibre percentage, succinate dehydrogenase enzyme activity, mitochondrial volume density, post-exercise phosphocreatine re-synthesis rate and muscle by-product clearance rates (i.e. H+ ions). On a more practical level, prepubertal children also experience similar decrements in peak power output as well-trained adult endurance athletes during repeated maximal exercise bouts. Therefore, prepubertal children have a comparable relative oxidative contribution to well-trained adult endurance athletes, but a decrease in this relative contribution occurs from childhood through to early adulthood. In a clinical context, this understanding may prove central to the development of exercise-based strategies for the prevention and treatment of many metabolic diseases related to mitochondrial oxidative dysfunction (e.g. in obese, insulin-resistant and diabetic patients), which are often accompanied by muscular deconditioning during adolescence and adulthood.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    Bailey RC, Olson J, Pepper SL, et al. The level and tempo of children’s physical activities: an observational study. Med Sci Sports Exerc. 1995;27:1033–41.

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Frost G, Dowling J, Dyson K, et al. Cocontraction in three age groups of children during treadmill locomotion. J Electromyogr Kinesiol. 1997;7:179–86.

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Moritani T, Oddsson L, Thorstensson A, et al. Neural and biomechanical differences between men and young boys during a variety of motor tasks. Acta Physiol Scand. 1989;137:347–55.

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Cooper DM, Kaplan MR, Baumgarten L, et al. Coupling of ventilation and CO2 production during exercise in children. Pediatr Res. 1987;21:568–72.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Van Praagh E, Dore E. Short-term muscle power during growth and maturation. Sports Med. 2002;32:701–28.

    Article  PubMed  Google Scholar 

  6. 6.

    Vinet A, Nottin S, Lecoq AM, et al. Cardiovascular responses to progressive cycle exercise in healthy children and adults. Int J Sports Med. 2002;23:242–6.

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Pesta D, Paschke V, Hoppel F, et al. Different metabolic responses during incremental exercise assessed by localized 31P MRS in sprint and endurance athletes and untrained individuals. Int J Sports Med. 2013;34:669–75.

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Bogdanis GC, Nevill ME, Boobis LH, et al. Recovery of power output and muscle metabolites following 30 s of maximal sprint cycling in man. J Physiol. 1995;482(Pt 2):467–80.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Garrandes F, Colson SS, Pensini M, et al. Neuromuscular fatigue profile in endurance-trained and power-trained athletes. Med Sci Sports Exerc. 2007;39:149–58.

    Article  PubMed  Google Scholar 

  10. 10.

    Ratel S, Kluka V, Vicencio SG, et al. Insights into the mechanisms of neuromuscular fatigue in boys and men. Med Sci Sports Exerc. 2015;47:2319–28.

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Ekblom B, Hermansen L. Cardiac output in athletes. J Appl Physiol. 1968;25:619–25.

    CAS  PubMed  Google Scholar 

  12. 12.

    Astorino TA, White AC. Assessment of anaerobic power to verify VO2max attainment. Clin Physiol Funct Imaging. 2010;30:294–300.

    Article  PubMed  Google Scholar 

  13. 13.

    Bell W, Cooper SM, Cobner D, et al. Physiological changes arising from a training programme in under-21 international netball players. Ergonomics. 1994;37:149–57.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    MacDougall JD, Hicks AL, MacDonald JR, et al. Muscle performance and enzymatic adaptations to sprint interval training. J Appl Physiol. 1985;1998(84):2138–42.

    Google Scholar 

  15. 15.

    Rivera-Brown AM, Alvarez M, Rodriguez-Santana JR, et al. Anaerobic power and achievement of VO2 plateau in pre-pubertal boys. Int J Sports Med. 2001;22:111–5.

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Rotstein A, Dotan R, Bar-Or O, et al. Effect of training on anaerobic threshold, maximal aerobic power and anaerobic performance of preadolescent boys. Int J Sports Med. 1986;7:281–6.

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Hostrup M, Kalsen A, Auchenberg M, et al. Effects of acute and 2-week administration of oral salbutamol on exercise performance and muscle strength in athletes. Scand J Med Sci Sports. 2016;26:8–16.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Meeuwisse WH, McKenzie DC, Hopkins SR, et al. The effect of salbutamol on performance in elite nonasthmatic athletes. Med Sci Sports Exerc. 1992;24:1161–6.

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Léger L. Aerobic performance. In: Docherty D, editor. Measurement in pediatric exercise science. Champaign: Human Kinetics; 1996. p. 183–223.

    Google Scholar 

  20. 20.

    Tanaka H, Shindo M. Running velocity at blood lactate threshold of boys aged 6–15 years compared with untrained and trained young males. Int J Sports Med. 1985;6:90–4.

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Reybrouck T, Weymans M, Stijns H, et al. Ventilatory anaerobic threshold in healthy children: age and sex differences. Eur J Appl Physiol Occup Physiol. 1985;54:278–84.

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Seiler S, Haugen O, Kuffel E. Autonomic recovery after exercise in trained athletes: intensity and duration effects. Med Sci Sports Exerc. 2007;39:1366–73.

    Article  PubMed  Google Scholar 

  23. 23.

    Fawkner SG, Armstrong N, Potter CR, et al. Oxygen uptake kinetics in children and adults after the onset of moderate-intensity exercise. J Sports Sci. 2002;20:319–26.

    Article  PubMed  Google Scholar 

  24. 24.

    Cleuziou C, Perrey S, Borrani F, et al. Dynamic responses of O2 uptake at the onset and end of exercise in trained subjects. Can J Appl Physiol. 2003;28:630–41.

    Article  PubMed  Google Scholar 

  25. 25.

    Ratel S, Tonson A, Le Fur Y, et al. Comparative analysis of skeletal muscle oxidative capacity in children and adults: a 31P-MRS study. Appl Physiol Nutr Metab. 2008;33:720–7.

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Taylor DJ, Kemp GJ, Thompson CH, et al. Ageing: effects on oxidative function of skeletal muscle in vivo. Mol Cell Biochem. 1997;174:321–4.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Tonson A, Ratel S, Le Fur Y, et al. Muscle energetics changes throughout maturation: a quantitative 31P-MRS analysis. J Appl Physiol. 1985;2010(109):1769–78.

    Google Scholar 

  28. 28.

    Kriketos AD, Baur LA, O’Connor J, et al. Muscle fibre type composition in infant and adult populations and relationships with obesity. Int J Obes Relat Metab Disord. 1997;21:796–801.

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Lexell J, Sjostrom M, Nordlund AS, et al. Growth and development of human muscle: a quantitative morphological study of whole vastus lateralis from childhood to adult age. Muscle Nerve. 1992;15:404–9.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Metaxas TI, Mandroukas A, Vamvakoudis E, et al. Muscle fiber characteristics, satellite cells and soccer performance in young athletes. J Sports Sci Med. 2014;13:493–501.

    PubMed  PubMed Central  Google Scholar 

  31. 31.

    Oertel G. Morphometric analysis of normal skeletal muscles in infancy, childhood and adolescence: an autopsy study. J Neurol Sci. 1988;88:303–13.

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Jansson E. Age-related fiber type changes in human skeletal muscle. In: Maughan R, Shireffs S, editors. Biochemistry of exercise IX. Champaign: Human Kinetics; 1996. p. 297–307.

    Google Scholar 

  33. 33.

    Berg A, Keul J. Biochemical changes during exercise in children. In: Malina R, editor. Young athletes/biological, psychological and educational perspectives. Champaign: Human Kinetics; 1988. p. 61–77.

    Google Scholar 

  34. 34.

    Berg A, Kim SS, Keul J. Skeletal muscle enzyme activities in healthy young subjects. Int J Sports Med. 1986;7:236–9.

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Eriksson BO, Gollnick PD, Saltin B. Muscle metabolism and enzyme activities after training in boys 11–13 years old. Acta Physiol Scand. 1973;87:485–97.

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Haralambie G. Enzyme activities in skeletal muscle of 13–15 years old adolescents. Bull Eur Physiopathol Respir. 1982;18:65–74.

    CAS  PubMed  Google Scholar 

  37. 37.

    Bell RD, MacDougall JD, Billeter R, et al. Muscle fiber types and morphometric analysis of skeletal msucle in six-year-old children. Med Sci Sports Exerc. 1980;12:28–31.

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Hoppeler H, Luthi P, Claassen H, et al. The ultrastructure of the normal human skeletal muscle: a morphometric analysis on untrained men, women and well-trained orienteers. Pflugers Arch. 1973;344:217–32.

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Tesch PA, Karlsson J. Muscle fiber types and size in trained and untrained muscles of elite athletes. J Appl Physiol. 1985;1985(59):1716–20.

    Google Scholar 

  40. 40.

    Vandenborne K, Walter G, Ploutz-Snyder L, et al. Energy-rich phosphates in slow and fast human skeletal muscle. Am J Physiol. 1995;268:C869–76.

    CAS  PubMed  Google Scholar 

  41. 41.

    Bernus G, Gonzalez de Suso JM, Alonso J, et al. 31P-MRS of quadriceps reveals quantitative differences between sprinters and long-distance runners. Med Sci Sports Exerc. 1993;25:479–84.

    CAS  PubMed  Google Scholar 

  42. 42.

    Gollnick PD, Armstrong RB, Saubert CW 4th, et al. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol. 1972;33:312–9.

    CAS  PubMed  Google Scholar 

  43. 43.

    Johansen L, Quistorff B. 31P-MRS characterization of sprint and endurance trained athletes. Int J Sports Med. 2003;24:183–9.

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Fleischman A, Makimura H, Stanley TL, et al. Skeletal muscle phosphocreatine recovery after submaximal exercise in children and young and middle-aged adults. J Clin Endocrinol Metab. 2010;95:E69–74.

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Hug F, Bendahan D, Le Fur Y, et al. Metabolic recovery in professional road cyclists: a 31P-MRS study. Med Sci Sports Exerc. 2005;37:846–52.

    Article  Google Scholar 

  46. 46.

    Emmett B, Hochachka PW. Scaling of oxidative and glycolytic enzymes in mammals. Respir Physiol. 1981;45:261–72.

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Cumming GR. Recirculation times in exercising children. J Appl Physiol Respir Environ Exerc Physiol. 1978;45:1005–8.

    CAS  PubMed  Google Scholar 

  48. 48.

    Hebestreit H, Mimura K, Bar-Or O. Recovery of muscle power after high-intensity short-term exercise: comparing boys and men. J Appl Physiol. 1985;1993(74):2875–80.

    Google Scholar 

  49. 49.

    Ratel S, Williams CA, Oliver J, et al. Effects of age and mode of exercise on power output profiles during repeated sprints. Eur J Appl Physiol. 2004;92:204–10.

    Article  PubMed  Google Scholar 

  50. 50.

    Harbili S. The effect of different recovery duration on repeated anaerobic performance in elite cyclists. J Hum Kinet. 2015;49:171–8.

    Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Berger NJ, Jones AM. Pulmonary O2 uptake on-kinetics in sprint- and endurance-trained athletes. Appl Physiol Nutr Metab. 2007;32:383–93.

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Kappenstein J, Ferrauti A, Runkel B, et al. Changes in phosphocreatine concentration of skeletal muscle during high-intensity intermittent exercise in children and adults. Eur J Appl Physiol. 2013;113:2769–79.

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev. 2008;88:287–332.

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Short KR, Sedlock DA. Excess postexercise oxygen consumption and recovery rate in trained and untrained subjects. J Appl Physiol. 1985;1997(83):153–9.

    Google Scholar 

  55. 55.

    Ohuchi H, Suzuki H, Yasuda K, et al. Heart rate recovery after exercise and cardiac autonomic nervous activity in children. Pediatr Res. 2000;47:329–35.

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Dixon EM, Kamath MV, McCartney N, et al. Neural regulation of heart rate variability in endurance athletes and sedentary controls. Cardiovasc Res. 1992;26:713–9.

    CAS  Article  PubMed  Google Scholar 

  57. 57.

    Armon Y, Cooper DM, Flores R, et al. Oxygen uptake dynamics during high-intensity exercise in children and adults. J Appl Physiol. 1985;1991(70):841–8.

    Google Scholar 

  58. 58.

    Eisenmann JC. Aerobic fitness, fatness and the metabolic syndrome in children and adolescents. Acta Paediatr. 2007;96:1723–9.

    Article  PubMed  Google Scholar 

  59. 59.

    Moran A, Jacobs DR Jr, Steinberger J, et al. Insulin resistance during puberty: results from clamp studies in 357 children. Diabetes. 1999;48:2039–44.

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Brandou F, Savy-Pacaux AM, Marie J, et al. Impact of high- and low-intensity targeted exercise training on the type of substrate utilization in obese boys submitted to a hypocaloric diet. Diabetes Metab. 2005;31:327–35.

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    Ratel S, Lazaar N, Dore E, et al. High-intensity intermittent activities at school: controversies and facts. J Sports Med Phys Fit. 2004;44:272–80.

    CAS  Google Scholar 

  62. 62.

    Falgairette G, Bedu M, Fellmann N, et al. Bio-energetic profile in 144 boys aged from 6 to 15 years with special reference to sexual maturation. Eur J Appl Physiol Occup Physiol. 1991;62:151–6.

    CAS  Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sébastien Ratel.

Ethics declarations

Funding

The authors have no funding sources to declare.

Conflicts of interest

Sébastien Ratel and Anthony Blazevich declare that they have no conflicts of interest with the content of this review.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ratel, S., Blazevich, A.J. Are Prepubertal Children Metabolically Comparable to Well-Trained Adult Endurance Athletes?. Sports Med 47, 1477–1485 (2017). https://doi.org/10.1007/s40279-016-0671-1

Download citation

Keywords

  • Maximal Voluntary Muscle Contraction
  • Ventilatory Threshold
  • Heart Rate Recovery
  • Prepubertal Child
  • Peripheral Fatigue