Fibre-type-specific and Mitochondrial Biomarkers of Muscle Damage after Mountain Races

Abstract

Consequences of running mountain races on muscle damage were investigated by analysing serum muscle enzymes and fibre-type-specific sarcomere proteins. We studied 10 trained amateur and 6 highly trained runners who ran a 35 km and 55 km mountain trail race (MTR), respectively. Levels of creatine kinase (CK), CK-MB isoform (CK-MB), sarcomeric mitochondrial CK (sMtCK), transaminases (AST and ALT), cardiac troponin I (cTnI) and fast (FM) and slow myosin (SM) isoforms, were assessed before, 1 h, 24 h and 48 h after the beginning of MTR. Significant SM increases were found at 24 h in the 55 km group. Levels of CK, CK-MB, AST and cTnI were significantly elevated in both groups following MTR, but in the 55 km group they tended to stabilize in at 48 h. Using pooled data, time-independent serum peaks of SM and CK-MB were significantly correlated. Moreover, concentration of sMtCK was significantly elevated at 1 and 24 h after the race in the 35 km group. Although training volume could confer protection on the mitochondria, the increase in serum CK-MB and SM in the 55 km group might be related to damage to the contractile apparatus type I fibres. Competing in long-distance MTRs might be related to deeper type I muscle fibre damage, even in highly trained individuals

Key words

eccentric exercise - downhill running - myosin isoforms - creatine kinase - cardiac troponin I

• References

• 1 Agarkova I, Perriard JC. The M-band: An elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 2005; 15: 477-485
• 2 Allen DG, Whitehead NP, Yeung EW. Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: Role of ionic changes. J Physiol 2005; 567: 723-735
• 3 Apple FS, Tesch PA. CK and LD isozymes in human single muscle fibers in trained athletes. J Appl Physiol 1989; 66: 2717-2720
• 4 Baird MF, Graham SM, Baker JS, Bickerstaff GF. Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J Nutr Metab 2012; 2012: 960363
• 5 Bonner HW, Leslie SW, Combs AB, Tate CA. Effects of exercise training and exhaustion on 45Ca uptake by rat skeletal muscle mitochondria and sarcoplasmic reticulum. Res Commun Chem Pathol Pharmacol 1976; 14: 767-770
• 6 Brancaccio P, Lippi G, Maffulli N. Biochemical markers of muscular damage. Clin Chem Lab Med 2010; 48: 757-767
• 7 Carmona G, Guerrero M, Cusso R, Padulles JM, Moras G, Lloret M, Bedini JL, Cadefau JA. Muscle enzyme and fiber type-specific sarcomere protein increases in serum after inertial concentric-eccentric exercise. Scand J Med Sci Sports 2015; 25: e547-e557
• 8 Carmona G, Mendiguchia J, Alomar X, Padulles JM, Serrano D, Nescolarde L, Rodas G, Cusso R, Balius R, Cadefau JA. Time course and association of functional and biochemical markers in severe semitendinosus damage following intensive eccentric leg curls: Differences between and within Subjects. Front Physiol 2018; 9: 54
• 9 Carmona G, Roca E, Guerrero M, Cusso R, Irurtia A, Nescolarde L, Brotons D, Bedini JL, Cadefau JA. Sarcomere disruptions of slow fiber resulting from mountain ultramarathon. Int J Sports Physiol Perform 2015; 10: 1041-1047
• 10 Chen Y, Serfass RC, Apple FS. Alterations in the expression and activity of creatine kinase-M and mitochondrial creatine kinase subunits in skeletal muscle following prolonged intense exercise in rats. Eur J Appl Physiol 2000; 81: 114-119
• 11 Clarke MS, Caldwell RW, Chiao H, Miyake K, McNeil PL. Contraction-induced cell wounding and release of fibroblast growth factor in heart. Circ Res 1995; 76: 927-934
• 12 Colombini A, Corsetti R, Machado M, Graziani R, Lombardi G, Lanteri P, Banfi G. Serum creatine kinase activity and its relationship with renal function indices in professional cyclists during the Giro d'Italia 3-week stage race. Clin J Sport Med 2012; 22: 408-413
• 13 Del Coso J, Fernandez de Velasco D, Abian-Vicen J, Salinero JJ, Gonzalez-Millan C, Areces F, Ruiz D, Gallo C, Calleja-Gonzalez J, Perez-Gonzalez B. Running pace decrease during a marathon is positively related to blood markers of muscle damage. PLoS One 2013; 8: e57602
• 14 Easthope CS, Hausswirth C, Louis J, Lepers R, Vercruyssen F, Brisswalter J. Effects of a trail running competition on muscular performance and efficiency in well-trained young and master athletes. Eur J Appl Physiol 2010; 110: 1107-1116
• 15 Eston RG, Mickleborough J, Baltzopoulos V. Eccentric activation and muscle damage: Biomechanical and physiological considerations during downhill running. Br J Sports Med 1995; 29: 89-94
• 16 Feasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, Denis C. Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 2002; 543: 297-306
• 17 Friden J, Lieber RL. Serum creatine kinase level is a poor predictor of muscle function after injury. Scand J Med Sci Sports 2001; 11: 126-127
• 18 Giandolini M, Horvais N, Rossi J, Millet GY, Morin JB, Samozino P. Effects of the foot strike pattern on muscle activity and neuromuscular fatigue in downhill trail running. Scand J Med Sci Sports 2016;
• 19 Gissel H, Clausen T. Excitation-induced Ca2+influx and skeletal muscle cell damage. Acta Physiol Scand 2001; 171: 327-334
• 20 Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 2003; 83: 731-801
• 21 Harber M, Trappe S. Single muscle fiber contractile properties of young competitive distance runners. J Appl Physiol 2008; 105: 629-636
• 22 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 update. Int J Sports Med 2017; 38: 1126-1131
• 23 Hoffman BW, Cresswell AG, Carroll TJ, Lichtwark GA. Protection from muscle damage in the absence of changes in muscle mechanical behavior. Med Sci Sports Exerc 2016; 48: 1495-1505
• 24 Hoffman MD. State of the science – ultraendurance sports. Int J Sports Physiol Perform 2016; 11: 831-832
• 25 Hoffman MD, Ingwerson JL, Rogers IR, Hew-Butler T, Stuempfle KJ. Increasing creatine kinase concentrations at the 161-km Western States Endurance Run. Wilderness Environ Med 2012; 23: 56-60
• 26 Hornemann T, Kempa S, Himmel M, Hayess K, Furst DO, Wallimann T. Muscle-type creatine kinase interacts with central domains of the M-band proteins myomesin and M-protein. J Mol Biol 2003; 332: 877-887
• 27 Hu LY, Ackermann MA, Kontrogianni-Konstantopoulos A. The sarcomeric M-region: A molecular command center for diverse cellular processes. Biomed Res Int 2015; 2015: 714197
• 28 Hyldahl RD, Hubal MJ. Lengthening our perspective: Morphological, cellular and molecular responses to eccentric exercise. Muscle Nerve 2014; 49: 155-170
• 29 Koller A, Schobersberger W. Post-exercise release of cardiac troponins. J Am Coll Cardiol 2009; 53: 1341 author reply 1341–1342
• 30 Kupchak BR, Kraemer WJ, Hoffman MD, Phinney SD, Volek JS. The impact of an ultramarathon on hormonal and biochemical parameters in men. Wilderness Environ Med 2014; 25: 278-288
• 31 McHugh MP. Recent advances in the understanding of the repeated bout effect: The protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 2003; 13: 88-97
• 32 McNeil PL, Khakee R. Disruptions of muscle fiber plasma membranes. Role in exercise-induced damage. Am J Pathol 1992; 140: 1097-1109
• 33 Mehta R, Gaze D, Mohan S, Williams KL, Sprung V, George K, Jeffries R, Hudson Z, Perry M, Shave R. Post-exercise cardiac troponin release is related to exercise training history. Int J Sports Med 2012; 33: 333-337
• 34 Mikkelsen UR, Fredsted A, Gissel H, Clausen T. Excitation-induced Ca2+influx and muscle damage in the rat: loss of membrane integrity and impaired force recovery. J Physiol 2004; 559: 271-285
• 35 Millet GP, Millet GY. Ultramarathon is an outstanding model for the study of adaptive responses to extreme load and stress. BMC Med 2012; 10: 77
• 36 Millet GY, Tomazin K, Verges S, Vincent C, Bonnefoy R, Boisson RC, Gergele L, Feasson L, Martin V. Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS One 2011; 6: e17059
• 37 Mingels A, Jacobs L, Michielsen E, Swaanenburg J, Wodzig W, van Dieijen-Visser M. Reference population and marathon runner sera assessed by highly sensitive cardiac troponin T and commercial cardiac troponin T and I assays. Clin Chem 2009; 55: 101-108
• 38 Noakes TD. Effect of exercise on serum enzyme activities in humans. Sports Med 1987; 4: 245-267
• 39 Overgaard K, Fredsted A, Hyldal A, Ingemann-Hansen T, Gissel H, Clausen T. Effects of running distance and training on Ca2+content and damage in human muscle. Med Sci Sports Exerc 2004; 36: 821-829
• 40 Overgaard K, Lindstrom T, Ingemann-Hansen T, Clausen T. Membrane leakage and increased content of Na+-K+pumps and Ca2+in human muscle after a 100-km run. J Appl Physiol ( 1985; ); 2002 92: 1891-1898
• 41 Rattray B, Thompson M, Ruell P, Caillaud C. Specific training improves skeletal muscle mitochondrial calcium homeostasis after eccentric exercise. Eur J Appl Physiol 2013; 113: 427-436
• 42 Saugy J, Place N, Millet GY, Degache F, Schena F, Millet GP. Alterations of neuromuscular function after the world's most challenging mountain ultra-marathon. PLoS One 2013; 8: e65596
• 43 Secher NH, Mizuno M, Saltin B. Adaptation of skeletal muscles to training. Bull Eur Physiopathol Respir 1984; 20: 453-457
• 44 Shave R, Baggish A, George K, Wood M, Scharhag J, Whyte G, Gaze D, Thompson PD. Exercise-induced cardiac troponin Elevation: Evidence, mechanisms, and implications. J Am Coll Cardiol 2010; 56: 169-176
• 45 Siekmann L, Bonora R, Burtis CA, Ceriotti F, Clerc-Renaud P, Ferard G, Ferrero CA, Forest JC, Franck PF, Gella FJ, Hoelzel W, Jorgensen PJ, Kanno T, Kessner A, Klauke R, Kristiansen N, Lessinger JM, Linsinger TP, Misaki H, Mueller MM, Panteghini M, Pauwels J, Schiele F, Schimmel HG, Vialle A, Weidemann G, Schumann G. IFCC primary reference procedures for the measurement of catalytic activity concentrations of enzymes at 37 degrees C. Part 1. The concept of reference procedures for the measurement of catalytic activity concentrations of enzymes. Clin Chem Lab Med 2002; 40: 631-634
• 46 Venditti P, Di Meo S. Effect of training on antioxidant capacity, tissue damage, and endurance of adult male rats. Int J Sports Med 1997; 18: 497-502
• 47 Waskiewicz Z, Klapcinska B, Sadowska-Krepa E, Czuba M, Kempa K, Kimsa E, Gerasimuk D. Acute metabolic responses to a 24-h ultra-marathon race in male amateur runners. Eur J Appl Physiol 2012; 112: 1679-1688
• 48 Yamashita K, Yoshioka T. Profiles of creatine kinase isoenzyme compositions in single muscle fibres of different types. J Muscle Res Cell Motil 1991; 12: 37-44