Muscle damage alters the metabolic response to dynamic exercise in humans: A 31P-MRS study

Journal of Applied Physiology

Volumn 111, Issue 3, 2011, Pages 782-790

  Davies, Rosemary C ^a   Eston, Roger G ^a,b   Fulford, Jonathan ^a   Rowlands, Ann V ^a   Jones, Andrew M ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

31P magnetic resonance spectroscopy exercise induced muscle damage; Creatine kinase; Delayed onset muscle soreness; Muscle energetics

Indexed keywords

BIOLOGICAL MARKER; CREATINE KINASE MM; CREATINE PHOSPHATE; PHOSPHATE; PHOSPHORUS;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ARTICLE; BIOMECHANICS; BLOOD; ENERGY METABOLISM; EXERCISE; EXERCISE TOLERANCE; HUMAN; MALE; METABOLISM; MUSCLE CONTRACTION; MUSCLE DISEASE; MUSCLE FATIGUE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PAIN; PAIN ASSESSMENT; PATHOPHYSIOLOGY; PH; SKELETAL MUSCLE; TIME; TORQUE;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; BIOLOGICAL MARKERS; BIOMECHANICS; CREATINE KINASE, MM FORM; ENERGY METABOLISM; EXERCISE; EXERCISE TOLERANCE; HUMANS; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; MUSCULAR DISEASES; PAIN; PAIN MEASUREMENT; PHOSPHATES; PHOSPHOCREATINE; PHOSPHORUS ISOTOPES; TIME FACTORS; TORQUE; YOUNG ADULT;

EID: 80052976181     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01021.2010     Document Type: Article

References (55)

1. Armstrong RB. Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc 16: 529-538, 1984. (Pubitemid 15178312)
2. Asp S, Daugaard JR, Kristiansen S, Kiens B, Richter EA. Exercise metabolism in human skeletal muscle exposed to prior eccentric exercise. J Physiol 509: 305-313, 1998. (Pubitemid 28252032)
3. Asp S, Daugaard JR, Richter EA. Eccentric exercise decreases glucose transporter GLUT4 protein in human skeletal muscle. J Physiol 482: 705-712, 1995.
4. Barstow TJ, Buchthal S, Zanconato S, Cooper DM. Muscle energetics and pulmonary oxygen uptake kinetics during moderate exercise. J Appl Physiol 77: 1742-1749, 1994. (Pubitemid 24322429)
5. Bendahan D, Confort-Gouney S, Kozak-Reiss G, Cozzone PJ. Pi trapping in glycogenolytic pathway can explain transient Pi disappearance during recovery from muscular exercise. FEBS Lett 269: 402-405, 1990. (Pubitemid 20273835)
6. Braun WA, Dutto DJ. The effects of a single bout of downhill running and ensuing delayed onset of muscle soreness on running economy performed 48 h later. Eur J Appl Physiol 90: 29-34, 2003. (Pubitemid 37369491)
7. Byrne C, Eston R. The effect of exercise-induced muscle damage on isometric and dynamic knee extensor strength and vertical jump performance. J Sports Sci 20: 417-425, 2002. (Pubitemid 34516477)
8. Byrne C, Eston R. Maximal-intensity isometric and dynamic exercise performance after eccentric muscle actions. J Sports Sci 20: 951-959, 2002. (Pubitemid 35373417)
9. Carmichael MD, Davis JM, Murphy EA, Brown AS, Carson JA, Eugene MB, Ghaffar A. Recovery of running performance following muscle-damaging exercise: Relationship to brain IL-1 beta. Brain Behav Immun 19: 445-452, 2005. (Pubitemid 41074783)
10. Carmichael MD, Davis JM, Murphy EA, Brown AS, Carson JA, Mayer EP, Ghaffar A. Role of brain IL-1 beta on fatigue after exerciseinduced muscle damage. Am J Physiol Regul Integr Comp Physiol 291: R1344-R1348, 2006.
11. Cettolo V, Piorico C, Francescato MP. T1 measurement of 31P metabolites at rest and during steady-state dynamic exercise using a clinical nuclear magnetic resonance scanner. Magn Reson Med 55: 498-505, 2006. (Pubitemid 43352547)
12. Chen TC, Nosaka K, Tu JH. Changes in running economy following downhill running. J Sports Sci 25: 55-63, 2007. (Pubitemid 44824380)
13. Clarkson PM, Nosaka K, Braun B. Muscle function after exerciseinduced muscle damage and rapid adaptation. Med Sci Sport Exerc 24: 512-520, 1992.
14. Davies RC, Eston RG, Poole DC, Rowlands AV, Dimenna F, Wilkerson DP, Twist C, Jones AM. Effect of eccentric exercise-induced muscle damage on the dynamics of muscle oxygenation and pulmonary oxygen uptake. J Appl Physiol 105: 1413-1421, 2008.
15. Davies RC, Rowlands AV, Eston RG. Effect of exercise-induced muscle damage on ventilatory and perceived exertion responses to moderate and severe intensity cycle exercise. Eur J Appl Physiol 107: 11-19, 2009.
16. Debold EP, Romatowski J, Fitts RH. The depressive effect of Pi on the force calcium relationship in skinned single muscle fibers is temperature dependent. Am J Physiol Cell Physiol 290: C1041-C1050, 2006.
17. Fridén J, Lieber RL. Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand 171: 321-326, 2001. (Pubitemid 32823799)
18. Gleeson M, Blannin AK, Walsh NP, Field CN, Pritchard JC. Effect of exercise-induced muscle damage on the blood lactate response to incremental exercise in humans. Eur J Appl Physiol Occup Physiol 77: 292-295, 1998. (Pubitemid 28107801)
19. Gleeson M, Blannin AK, Zhu B, Brooks S, Cave R. Cardiorespiratory, hormonal and haematological responses to submaximal cycling performed 2 days after eccentric or concentric exercise bouts. J Sports Sci 13: 471-479, 1995. (Pubitemid 26021971)
20. Hogan MC, Richardson RS, Haseler LJ. Human muscle performance and PCr hydrolysis with varied inspired oxygen fractions: a 31P-MRS study. J Appl Physiol 86: 1367-73, 1999. (Pubitemid 29172173)
21. Hortobágyi T, Denahan T. Variability in creatine-kinase- methodological, exercise, and clinically related factors. Int J Sports Med 10: 69-80, 1989. (Pubitemid 19105547)
22. Jones AM, Wilkerson DP, Berger NJ, Fulford J. Influence of endurance training on muscle [PCr] kinetics during high-intensity exercise. Am J Physiol Regul Integr Comp Physiol 293: R392-R401, 2007. (Pubitemid 47092198)
23. Kano Y, Padilla DJ, Behnke BJ, Hageman KS, Musch TI, Poole DC. Effects of eccentric exercise on microcirculation and microvascular oxygen pressures in rat spinotrapezius muscle. J Appl Physiol 99: 1516-1522, 2005. (Pubitemid 43014362)
24. Kano Y, Sampei K, Matsudo H. Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise. Acta Physiol Scand 180: 291-299, 2004. (Pubitemid 38299640)
25. Kemp GJ, Roussel M, Bendahan D, Le Fur Y, Cozzone PY. Interrelations of ATP synthesis and proton handling in ischaemically exercising human forearm muscle studied by 31P magnetic resonance spectroscopy. J Physiol 535: 901-928, 2001. (Pubitemid 32894498)
26. Lund H, Vestergaard-Poulsen P, Kanstrup IL, Sejrsen P. The effect of passive stretching on delayed onset muscle soreness, and other detrimental effects following eccentric exercise. Scand J Med Sci Sports 8: 216-221, 1998. (Pubitemid 128531127)
27. Lund H, Vestergaard-Poulsen P, Kanstrup IL, Sejrsen P. Isokinetic eccentric exercise as a model to induce and reproduce pathophysiological alterations related to delayed onset muscle soreness. Scand J Med Sci Sports 8: 208-215, 1998. (Pubitemid 128531126)
28. MacIntyre DL, Reid WD, Lyster DM, Szasz IJ, McKenzie DC. Presence of WBC, decreased strength, and delayed soreness in muscle after eccentric exercise. J Appl Physiol 80: 1006-1013, 1996. (Pubitemid 26087269)
29. Mahler M. First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol 86: 135-165, 1985. (Pubitemid 15073068)
30. Marcora SM, Bosio A. Effect of exercise-induced muscle damage on endurance running performance in humans. Scand J Med Sci Sports 17: 662-671, 2007.
31. Marsh GD, Paterson DH, Potwarka JJ, Thompson RT. Transient changes in muscle high-energy phosphates during moderate exercise. J Appl Physiol 75: 648-656, 1993. (Pubitemid 23260203)
32. Marsh GD, Paterson DH, Thompson RT, Driedger AA. Coincident thresholds in intracellular phosphorylation potential and pH during progressive exercise. J Appl Physiol 71: 1076-1081, 1991.
33. McCully K, Shellock FG, Bank WJ, Posner JD. The use of nuclear magnetic resonance to evaluate muscle injury. Med Sci Sports Exerc 24: 537-542, 1992.
34. Meyer RA. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol Cell Physiol 254: C548-C553, 1988.
35. Moon RB, Richards JH. Determination of intracellular pH by 31P magnetic resonance. J Biol Chem 248: 7276-7278, 1973.
36. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D. Java-based graphical user interface for the MRUI quantitation package. MAGMA 12: 141-152, 2001. (Pubitemid 32510133)
37. Pathare N, Vandenborne K, Liu M, Stevens JE, Li Y, Frimel TN, Walter GA. Alterations in inorganic phosphate in mouse hindlimb muscles during limb disuse. NMR Biomed 21: 101-110, 2008. (Pubitemid 351351002)
38. Pathare N, Walter GA, Stevens JE, Yang Z, Okerke E, Gibbs JD, Esterhai JL, Scarborough MT, Gibbs CP, Sweeney HL, Vandenborne K. Changes in inorganic phosphate and force production in human skeletal muscle after cast immobilization. J Appl Physiol 98: 307-314, 2005. (Pubitemid 40041261)
39. Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537: 333-345, 2001. (Pubitemid 33130492)
40. Robergs RA, Ghiasvand F, Parker D. Biochemistry of exercise-induced metabolic acidosis. Am J Physiol Regul Integr Comp Physiol 287: R502-R516, 2004. (Pubitemid 39095921)
41. Rodenburg JB, Degroot MCH, Vanechteld CJA, Jongsma HJ, Bar PR. Phosphate-metabolism of prior eccentrically loaded vastus medialis muscle during exercise in humans. Acta Physiol Scand 153: 97-108, 1995.
42. Rossiter HB, Ward SA, Doyle VL, Howe FA, Griffiths JR, Whipp BJ. Inferences from pulmonary O2 uptake with respect to intramuscular [phosphocreatine] kinetics during moderate exercise in humans. J Physiol 518: 921-932, 1999. (Pubitemid 29387258)
43. Schneider DA, Berwick JP, Sabapathy S, Minahan CL. Delayed onset muscle soreness does not alter O2 uptake kinetics during heavy-intensity cycling in humans. Int J Sports Med 28: 550-556, 2007. (Pubitemid 47080134)
44. Sharma U, Kumar V, Wadhwa S, Jagannathan NR. In vivo (31)P MRS study of skeletal muscle metabolism in patients with postpolio residual paralysis. Magn Reson Imaging 25: 244-249, 2007. (Pubitemid 46162051)
45. St Clair Gibson A, Baden DA, Lambert MI, Lambert EV, Harley YX, Hampson D, Russell VA, Noakes TD. The conscious perception of the sensation of fatigue. Sports Med 33: 167-176, 2003. (Pubitemid 36433825)
46. Szasz G, Gruber W, Bernt E. Creatine-kinase in serum. 1. Determination of optimum reaction conditions. Clin Chem 22: 650-656, 1976.
47. Twist C, Eston R. The effects of exercise-induced muscle damage on maximal intensity intermittent exercise performance. Eur J Appl Physiol 94: 652-658, 2005. (Pubitemid 41136067)
48. Twist C, Eston RG. The effect of exercise-induced muscle damage on perceived exertion and cycling endurance performance. Eur J Appl Physiol 105: 559-567, 2009.
49. van den Broek NMA, De Feyters HMML, de Graaf L, Nicolay K, Prompers JJ. Intersubject differences in the effect of acidosis on phospocreatine recovery kinetics in muscle after exercise are due to proton efflux rates. Am J Physiol Cell Physiol 293: C228-C237, 2007. (Pubitemid 47105047)
50. Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129: 35-43, 1997. (Pubitemid 127454051)
51. Vanhatalo A, Fulford J, DiMenna FJ, Jones AM. Influence of hyperoxia on muscle metabolic responses and the power-duration relationship during severe-intensity exercise in humans: a 31P magnetic resonance spectroscopy study. Exp Physiol 95: 528-540, 2010.
52. Westerblad H, Allen DG, Lännergren J. Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17: 17-2002.
53. Wilson JR, McCully KK, Mancini DM, Boden B, Chance B. Relationship of muscular fatigue to pH and diprotonated Pi in humans: a 31P-NMR study. J Appl Physiol 64: 2333-2339, 1988.
54. Yu JG, Malm C, Thornell LE. Eccentric contractions leading to DOMS do not cause loss of desmin nor fibre necrosis in human muscle. Histochem Cell Biol 118: 29-34, 2002. (Pubitemid 34762316)
55. Yu JG, Thornell LE. Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem Cell Biol 118: 171-179, 2002.