European Journal of Applied Physiology

, Volume 98, Issue 6, pp 556–565 | Cite as

Reliability of 31P-magnetic resonance spectroscopy during an exhaustive incremental exercise test in children

  • Alan Barker
  • Joanne Welsman
  • Deborah Welford
  • Jonathan Fulford
  • Craig Williams
  • Neil Armstrong
Original Article


This study examined the reliability of 31P-magnetic resonance spectroscopy (MRS) to measure parameters of muscle metabolic function in children. On separate days, 14 children (7 boys and 7 girls) completed three knee-extensor incremental tests to exhaustion inside a whole-body scanner (1.5 T, Phillips). The dynamic changes in the ratio of inorganic phosphate to phosphocreatine (Pi/PCr) and intracellular muscle pH were resolved every 30 s. Using plots of Pi/PCr and pH against power output (W), intracellular thresholds (ITs) for each variable were determined using both subjective and objective procedures. The ITPi/PCr and ITpH were observed subjectively in 93 and 81% of their respective plots, whereas the objective method identified the ITPi/PCr in 88% of the plots. The ITpH was undetectable using the objective method. End exercise (END) ENDPi/PCr, ENDpH, ITPi/PCr and ITpH were examined using typical error statistics expressed as a % coefficient of variation (CV) across all three exercise tests. The CVs for the power output at the subjectively determined ITPi/PCr and ITpH were 10.6 and 10.3%, respectively. Objective identification of the ITPi/PCr had a CV of 16.3%. CVs for ENDpH and ENDPi/PCr were 0.9 and 50.0%, respectively. MRS provides a valuable window into metabolic changes during exercise in children. During knee-extensor exercise to exhaustion, ENDpH and the subjectively determined ITPi/PCr and ITpH demonstrate good reliability and thus stable measures for the future study of developmental metabolism. However, the objectively determined ITPi/PCr and ENDPi/PCr displayed poor reliability.


MRS Muscle metabolism Intracellular threshold Developmental 



We would like to express our gratitude to the subjects from Wynstream primary school that participated in this study. Furthermore, the technical expertise provided by David Childs in designing the ergometer and analysis software was most appreciated. The study was funded by the Darlington Trust.


  1. Atkinson G, Nevill AM (1998) Statistical methods for assessing measurement error (reliability) in variables relevant to sports medicine. Sports Med 26:217–238PubMedCrossRefGoogle Scholar
  2. Barstow TJ, Buchthal SD, Zanconato S, Cooper DM (1994) Changes in potential controllers of human skeletal muscle respiration during incremental calf exercise. J Appl Physiol 77:2169–2176PubMedGoogle Scholar
  3. Bendahan D, Mattei JP, Ghattas B, Confort-Gouny S, Le Guern ME, Cozzone PJ (2005) Citrulline/malate promotes aerobic energy production in human exercising muscle. Br J Sports Med 36:282–289CrossRefGoogle Scholar
  4. Boisseau N, Delamarche P (2000) Metabolic and hormonal responses to exercise in children and adolescents. Sports Med 30:405–422PubMedCrossRefGoogle Scholar
  5. Chance B, Leigh JS Jr, Clark BJ, Maris J, Kent J, Nioka S, Smith D (1985) Control of oxidative metabolism and oxygen delivery in human skeletal muscle: a steady-state analysis of the work/energy cost transfer function. Proc Natl Acad Sci USA 82:8384–8388PubMedCrossRefGoogle Scholar
  6. Chilibeck PD, McCreary CR, Marsh GD, Paterson DH, Noble EG, Taylor AW, Thompson RT (1998) Evaluation of muscle oxidative potential by 31P-MRS during incremental exercise in old and young humans. Eur J Appl Physiol 78:460–465CrossRefGoogle Scholar
  7. Conley KE, Jubrias SA, Esselman PC (2000) Oxidative capacity and ageing in human muscle. J Physiol 526:203–210PubMedCrossRefGoogle Scholar
  8. DeVries DA, Marsh GD, Rodger NW, Thompson RT (1996) Metabolic response of forearm muscle to graded exercise in type II diabetes mellitus: effect of endurance training. Can J Appl Physiol 21:120–133PubMedGoogle Scholar
  9. Eriksson BO (1980) Muscle metabolism in children: a review. Acta Paediatr Scand 283:20–28Google Scholar
  10. Fawkner SG, Armstrong N, Childs DJ, Welsman JR (2002) Reliability of the visually identified ventilatory threshold and v-slope in children. Pediatr Exerc Sci 14:181–192Google Scholar
  11. Fowler MD, Ryschon TW, Wysong RE, Combs CA, Balaban RS (1997) Normalized metabolic stress for 31P-MR spectroscopy studies of human skeletal muscle: MVC vs. muscle volume. J Appl Physiol 83:875–883Google Scholar
  12. Haralambie G (1982) Enzyme activities in skeletal muscle of 13–15 years old adolescents. Bull Eur Physiopathol Respir 18:65–74PubMedGoogle Scholar
  13. Hopkins WG (2000a) Measures of reliability in sports medicine and science. Sports Med 30:1–15CrossRefGoogle Scholar
  14. Hopkins WG (2000b) A new view of statistics. Internet Society for Sport Science. Scholar
  15. Kent-Braun JA, McCully KK, Chance B (1990) Metabolic effects of training in humans: a 31P-MRS study. J Appl Physiol 69:1165–1170PubMedGoogle Scholar
  16. Kent-Braun JA, Miller RG, Weiner MW (1993) Phases of metabolism during progressive exercise to fatigue in human skeletal muscle. J Appl Physiol 75:573–580PubMedGoogle Scholar
  17. Kowalchuk JM, Smith SA, Weening BS, Marsh GD, Paterson DH (2000) Forearm muscle metabolism studied using (31)P-MRS during progressive exercise to fatigue after Acz administration. J Appl Physiol 89:200–209PubMedGoogle Scholar
  18. Kuno S, Miyamaru M, Itai Y (1993) Muscle energetics during exercise of elite sprinter in children by 31P NMR. Med Sci Sports Exerc 25:S147Google Scholar
  19. Kuno S, Takahashi H, Fujimoto K, Akima H, Miyamaru M, Nemoto I, Itai Y, Katsuta S (1995) Muscle metabolism during exercise using phosphorus-31 nuclear magnetic resonance spectroscopy in adolescents. Eur J Appl Physiol Occup Physiol 70:301–304PubMedCrossRefGoogle Scholar
  20. Larson-Meyer DE, Newcomer BR, Hunter GR, Hetherington HP, Weinsier RL (2000) 31P MRS measurement of mitochondrial function in skeletal muscle: reliability, force-level sensitivity and relation to whole body maximal oxygen uptake. NMR Biomed 13:14–27PubMedCrossRefGoogle Scholar
  21. Madden A, Leach MO, Sharp JC, Collins DJ, Easton D (1991) A quantitative analysis of the accuracy of in vivo pH measurements with 31P NMR spectroscopy: assessment of pH measurement methodology. NMR Biomed 4:1–11PubMedGoogle Scholar
  22. Marsh GD, Paterson DH, Thompson RT, Driedger AA (1991) Coincident thresholds in intracellular phosphorylation potential and pH during progressive exercise. J Appl Physiol 71:1076–1081PubMedGoogle Scholar
  23. Miller RG, Carson PJ, Moussavi RS, Green A, Baker A, Boska MD, Weiner MW (1995) Factors which influence alterations of phosphates and pH in exercising human skeletal muscle: measurement error, reproducibility, and effects of fasting, carbohydrate loading, and metabolic acidosis. Muscle Nerve 18:60–67PubMedCrossRefGoogle Scholar
  24. Mizuno M, Secher NH, Quistorff B (1994) 31P-NMR spectroscopy, rsEMG, and histochemical fiber types of human wrist flexor muscles. J Appl Physiol 76:531–538PubMedGoogle Scholar
  25. Morris NM, Udry JR (1980) Validation of a self-administered instrument to assess stage of adolescent development. J Youth Adolesc 9:271–280CrossRefGoogle Scholar
  26. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D (2001) Java-based graphical user interface for the MRUI quantitation package. MAGMA 12:141–152PubMedGoogle Scholar
  27. Petersen SR, Gaul CA, Stanton MM, Hanstock CC (1999) Skeletal muscle metabolism during short-term, high-intensity exercise in prepubertal and pubertal girls. J Appl Physiol 87:2151–2156PubMedGoogle Scholar
  28. Potwarka JJ, Drost DJ, Williamson PC (1995) Time domain quantification of 31P brain spectra. Magn Reson Med 3:1986Google Scholar
  29. Rossiter HB, Howe FA, Ward SA, Kowalchuk JM, Griffiths JR, Whipp BJ (2000) Intersample fluctuations in phosphocreatine concentration determined by 31P-magnetic resonance spectroscopy and parameter estimation of metabolic responses to exercise in humans. J Physiol 528:359–369PubMedCrossRefGoogle Scholar
  30. Rossiter HB, Whipp BJ, Ward SA, McIntyre DJ, Griffiths JR, Howe FA (2004) The heterogeneity of intramuscular metabolism using simultaneous 31P2D-CSI and pulmonary oxygen uptake (VO2) during incremental knee-extensor exercise in humans. Magn Reson Med 12:773Google Scholar
  31. Selvadurai HC, Allen J, Sachinwalla T, Macauley J, Blimkie CJ, Van Asperen PP (2003) Muscle function and resting energy expenditure in female athletes with cystic fibrosis. Am J Respir Crit Care Med 168:1476–1480PubMedCrossRefGoogle Scholar
  32. Systrom DM, Kanerek DJ, Kohler SJ, Kazemi H (1990) 31P nuclear magnetic resonance spectroscopy study of the anaerobic threshold in humans. J Appl Physiol 68:2060–2066PubMedGoogle Scholar
  33. Taylor DJ, Bore PJ, Styles P, Gadian DG, Radda GK (1983) Bioenergetics of intact human muscle: a 31P nuclear magnetic resonance study. Mol Biol Med 1:77–94PubMedGoogle Scholar
  34. Taylor DJ, Kemp GJ, Thompson CH, Radda GK (1997) Ageing: effects on oxidative function of skeletal muscle in vivo. Mol Cell Biochem 174:321–324PubMedCrossRefGoogle Scholar
  35. Vanhamme L, van den Boogaart A, Van Huffel S (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129:35–43PubMedCrossRefGoogle Scholar
  36. Veith E (1989) Fitting piecewise linear regression functions to biological responses. J Appl Physiol 67:390–396Google Scholar
  37. Yoshida T, Watari H (1993) 31P-nuclear magnetic resonance spectroscopy study of the time course of energy metabolism during exercise and recovery. Eur J Appl Physiol Occup Physiol 66:494–499PubMedCrossRefGoogle Scholar
  38. Yoshida T, Watari H (1997) Effect of circulatory occlusion on human muscle metabolism during exercise and recovery. Eur J Appl Physiol Occup Physiol 75:200–205PubMedCrossRefGoogle Scholar
  39. Zanconato S, Buchthal S, Barstow TJ, Cooper DM (1993) 31P-magnetic resonance spectroscopy of leg muscle metabolism during exercise in children and adults. J Appl Physiol 74:2214–2218PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Alan Barker
    • 1
  • Joanne Welsman
    • 1
  • Deborah Welford
    • 1
  • Jonathan Fulford
    • 1
  • Craig Williams
    • 1
  • Neil Armstrong
    • 1
  1. 1.Children’s Health, Exercise Research Centre, St Luke’s CampusUniversity of ExeterExeterUK

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