Abstract
According to the literature the steady-state level of phosphocreatine (PCr) has a linear relationship to the workload during muscle exercise intensities below the lactate threshold, whereas this linearity is impaired during exercise intensities above the lactate threshold. The purpose of this study was to investigate the linearity between PCr kinetics and workload during two bouts of isotonic incremental calf exercise with transitions from moderate- to high-intensity as well as from high- to moderate-intensity work rates. Using a whole-body 1.5 T MR scanner and a self-built exercise bench, we performed serial phosphorus-31 magnetic resonance spectroscopy (31P-MRS) with a time resolution of 30 s in nine healthy male volunteers. Changes in PCr, inorganic phosphate (Pi) and pH were statistically evaluated in comparison to the baseline. The exercise protocol started with a 4.5 W interval of 6 min followed by two bouts of 1.5 W increments. The workload was increased in 2-min intervals up to 9 W during the first bout and up to 7.5 W during the second bout. The second bout was preceded by a 4.5 W interval of 2 min and followed by a 4.5 W interval of 4 min. PCr hydrolysis achieved a steady state during each increment and was highly linear to the work rate (r 2, −0.796; P <0.001). Pi accumulated during each bout, whereas the pH decreased continuously during the first bout and did not exhibit any substantial decrease during the second bout. The metabolite levels and pH were expressed as the median value and the range. Our study confirms that steady-state PCr levels also have a linear relationship to work intensities above the lactate threshold, while pH changes do not have any impact on PCr degradation. The lack of substantial changes in pH during the second exercise bout indicates that prior high-intensity exercise leads to an activation of oxidative phosphorylation.
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References
Bangsbo J, Gollnick PD, Graham TE, Juel C, Kiens B, Mizuno M, Saltin B (1990) Anaerobic energy production and O2 deficit-debt relationship during exhaustive exercise in humans. J Physiol (Lond) 422:539–559
Bangsbo J, Johansen L, Quistorff B, Saltin B (1993) NMR and analytic biochemical evaluation of CrP and nucleotides in the human calf during muscle contraction. J Appl Physiol 74:2034–2039
Barstow TJ, Buchthal S, Zanconato S, Cooper DM (1994a) Muscle energetics and pulmonary oxygen uptake kinetics during moderate exercise. J Appl Physiol 77:1742–1749
Barstow TJ, Buchthal SD, Zanconato S, Cooper DM (1994b) Changes in potential controllers of human skeletal muscle respiration during incremental calf exercise. J Appl Physiol 77:2169–2176
Binzoni T, Ferretti G, Schenker K, Cerretelli P (1992) Phosphocreatine hydrolysis by 31P-NMR at the onset of constant-load exercise in humans. J Appl Physiol 73:1644–1649
Bohnert B, Ward SA, Whipp BJ (1998) Effects of prior arm exercise on pulmonary gas exchange kinetics during high-intensity leg exercise in humans. Exp Physiol 83:557–570
Brosseau OE, Mahdjoub R, Seurin MJ, Thiriet P, Gozal D, Briguet A (2003) Kinetics of anaerobic metabolism in human skeletal muscle: influence of repetitive high-intensity exercise on sedentary dominant and non-dominant forearm. A 31P-NMR study. Biochimie 85:885–890
Chin ER, Allen DG (1998) The contribution of pH-dependent mechanisms to fatigue at different intensities in mammalian single muscle fibres. J Physiol (Lond) 512:831–840
Chwalbinska-Moneta J, Robergs RA, Costill DL, Fink WJ (1989) Threshold for muscle lactate accumulation during progressive exercise. J Appl Physiol 66:2710–2716
Di Prampero PE (1981) Energetics of muscular exercise. Rev Physiol Biochem Pharmacol 89:143–222
Di Prampero PE, Margaria R (1968) Relationship between O2 consumption, high energy phosphates and the kinetics of the O2 debt in exercise. Pflugers Arch 304:11–19
Di Prampero PE, Francescato MP, Cettolo V (2003) Energetics of muscular exercise at work onset: the steady-state approach. Pflugers Arch 445:741–746
Endo M, Usui S, Fukuoka Y, Miura A, Rossiter HB, Fukuba Y (2004) Effects of priming exercise intensity on the dynamic linearity of the pulmonary V̇O2 response during heavy exercise. Eur J Appl Physiol 91:545–554
Francescato MP, Cettolo V, Di Prampero PE (2003) Relationships between mechanical power, O2 consumption, O2 deficit and high-energy phosphates during calf exercise in humans. Pflugers Arch 445:622–628
Gerbino A, Ward SA, Whipp BJ (1996) Effects of prior exercise on pulmonary gas-exchange kinetics during high-intensity exercise in humans. J Appl Physiol 80:99–107
Grassi B (2000) Skeletal muscle V̇O2 on-kinetics: set by O2 delivery or by O2 utilization? New insights into an old issue. Med Sci Sports Exerc 32:108–116
Grassi B (2003) Oxygen uptake kinetics: old and recent lessons from experiments on isolated muscle in situ. Eur J Appl Physiol 90:242–249
Knuttgen HG, Saltin B (1972) Muscle metabolites and oxygen uptake in short-term submaximal exercise in man. J Appl Physiol 32:690–694
Macdonald M, Pedersen PK, Hughson RL (1997) Acceleration of V̇O2 kinetics in heavy submaximal exercise by hyperoxia and prior high-intensity exercise. J Appl Physiol 83:1318–1325
Mahler M (1985) First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between Q O2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol 86:135–165
Marsh GD, Paterson DH, Thompson RT, Driedger AA (1991) Coincident thresholds in intracellular phosphorylation potential and pH during progressive exercise. J Appl Physiol 71:1076–1081
Marsh GD, Paterson DH, Potwarka JJ, Thompson RT (1993) Transient changes in muscle high-energy phosphates during moderate exercise. J Appl Physiol 75:648–656
McCann DJ, Mole PA, Caton JR (1995) Phosphocreatine kinetics in humans during exercise and recovery. Med Sci Sports Exerc 27:378–389
McCreary CR, Chilibeck PD, Marsh GD, Paterson DH, Cunningham DA, Thompson RT (1996) Kinetics of pulmonary oxygen uptake and muscle phosphates during moderate-intensity calf exercise. J Appl Physiol 81:1331–1338
Meyer RA (1988) A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol 254:C548–C553
Newcomer BR, Boska MD, Hetherington HP (1999) Non-P(i) buffer capacity and initial phosphocreatine breakdown and resynthesis kinetics of human gastrocnemius/soleus muscle groups using 0.5 s time-resolved 31P-MRS at 4.1 T. NMR Biomed 12:545–551
Petroff OA, Prichard JW, Behar KL, Alger JR, den Hollander JA, Shulman RG (1985) Cerebral intracellular pH by 31P-nuclear magnetic resonance spectroscopy. Neurology 35:781–788
Price TB, Kamen G, Damon BM, Knight CA, Applegate B, Gore JC, Eward K, Signorile JF (2003) Comparison of MRI with EMG to study muscle activity associated with dynamic plantar flexion. Magn Reson Imaging 21:853–861
Rico-Sanz J (2003) Progressive decrease of intramyocellular accumulation of H+ and Pi in human skeletal muscle during repeated isotonic exercise. Am J Physiol Cell Physiol 284:C1490–1496
Rossiter HB, Ward SA, Kowalchuk JM, Howe FA, Griffiths JR, Whipp BJ (2001) Effects of prior exercise on oxygen uptake and phosphocreatine kinetics during high-intensity knee-extension exercise in humans. J Physiol (Lond) 537:291–303
Rossiter HB, Ward SA, Kowalchuk JM, Howe FA, Griffiths JR, Whipp BJ (2002) Dynamic asymmetry of phosphocreatine concentration and O2 uptake between the on- and off-transients of moderate- and high-intensity exercise in humans. J Physiol 541:991–1002
Russ DW, Vandenborne K, Walter GA, Elliott M, Binder-Macleod SA (2002) Effects of muscle activation on fatigue and metabolism in human skeletal muscle. J Appl Physiol 92:1978–1986
Sairyo K, Iwanaga K, Yoshida N, Mishiro T, Terai T, Sasa T, Ikata T (2003) Effects of active recovery under a decreasing work load following intense muscular exercise on intramuscular energy metabolism. Int J Sports Med 24:179–182
Schocke MF, Metzler B, Wolf C, Steinboeck P, Kremser C, Pachinger O, Jaschke W, Lukas P (2003) Impact of aging on cardiac high-energy phosphate metabolism determined by phosphorus-31 2-dimensional chemical shift imaging (31P-2D CSI). Magn Reson Imaging 21:553–559
Schocke MF, Esterhammer R, Kammerlander C, Rass A, Kremser C, Fraedrich G, Jaschke WR, Greiner A (2004a) High-energy phosphate metabolism during incremental calf exercise in humans measured by 31Phosphorus Magnetic Resonance Spectroscopy (31P-MRS). Magn Reson Imaging 22:109–115
Schocke MF, Zoller H, Vogel W, Wolf C, Kremser C, Steinboeck P, Poelzl G, Pachinger O, Jaschke WR, Metzler B (2004b) Cardiac phosphorus-31 two-dimensional chemical shift imaging in patients with hereditary hemochromatosis. Magn Reson Imaging 22:515–521
Schunk K, Losch O, Kreitner KF, Kersjes W, Schadmand-Fischer S, Thelen M (1999) Contributions of dynamic phosphorus-31 magnetic resonance spectroscopy to the analysis of muscle fiber distribution. Invest Radiol 34:348–356
Street D, Bangsbo J, Juel C (2001) Interstitial pH in human skeletal muscle during and after dynamic graded exercise. J Physiol (Lond) 537:993–998
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 1:77–94
Vandenborne K, Walter G, Ploutz-Snyder L, Dudley G, Elliott MA, De Meirleir K (2000) Relationship between muscle T2* relaxation properties and metabolic state: a combined localized 31P-spectroscopy and 1H-imaging study. Eur J Appl Physiol 82:76–82
Westerblad H, Allen DG, Lannergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17:17–21
Yoshida T (2002) The rate of phosphocreatine hydrolysis and resynthesis in exercising muscle in humans using 31P-MRS. J Physiol Anthropol Appl Human Sci 21:247–255
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Schocke, M.F.H., Esterhammer, R., Arnold, W. et al. High-energy phosphate metabolism during two bouts of progressive calf exercise in humans measured by phosphorus-31 magnetic resonance spectroscopy. Eur J Appl Physiol 93, 469–479 (2005). https://doi.org/10.1007/s00421-004-1233-z
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DOI: https://doi.org/10.1007/s00421-004-1233-z