Insights into the molecular etiology of exercise-induced inflammation: opportunities for optimizing performance

Ioannis G Fatouros, Athanasios Z Jamurtas, Ioannis G Fatouros, Athanasios Z Jamurtas

Abstract

The study of exercise-induced muscle damage (EIMD) is of paramount importance not only because it affects athletic performance but also because it is an excellent model to study the mechanisms governing muscle cachexia under various clinical conditions. Although, a large number of studies have investigated EIMD and its associated inflammatory response, several aspects of skeletal muscles responses remain unclear. In the first section of this article, the mechanisms of EIMD are reviewed in an attempt to follow the events that result in functional and structural alterations of skeletal muscle. In the second section, the inflammatory response associated with EIMD is presented with emphasis in leukocyte accumulation through mechanisms that are largely coordinated by pro- and anti-inflammatory cytokines released either by injured muscle itself or other cells. The practical applications of EIMD and the subsequent inflammatory response are discussed with respect to athletic performance. Specifically, the mechanisms leading to performance deterioration and development of muscle soreness are discussed. Emphasis is given to the factors affecting individual responses to EIMD and the resulting interindividual variability to this phenomenon.

Keywords: aseptic inflammation; exercise; immune system; muscle damage; recovery; redox status.

Conflict of interest statement

The authors report no conflicts of interest in this work.

References

    1. Peake J, Nosaka K, Suzuki K. Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev. 2005;11:64–85.
    1. Proske U, Allen TJ. Damage to skeletal muscle from eccentric exercise. Exerc Sport Sci Rev. 2005;33:98–104.
    1. Fehrenbach E, Schneider ME. Trauma-induced systemic inflammatory response versus exercise-induced immunomodulatory effects. Sports Med. 2006;36:373–384.
    1. Smith C, Kruger MJ, Smith RM, Myburgh KH. The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med. 2008;38:947–969.
    1. Tidball JG, Villalta SA. Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integr Comp Physiol. 2010;298:R1173–R1187.
    1. Gomez-Cabrera MC, Borras C, Pallardo FV, Sastre J, Li LJ, Vina J. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol. 2005;567:113–120.
    1. Michailidis Y, Karagounis LG, Terzis G, et al. Evidence of potential redox-sensitive regulation of human skeletal muscle’s performance and intracellular signaling following aseptic inflammation induced by damaging exercise. Am J Clin Nutr. 2013;98:233–245.
    1. Paulsen G, Mikkelsen UR, Raastad T, Peake JM. Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exerc Immunol Rev. 2012;18:42–97.
    1. Asmussen E. Observations on experimental muscular soreness. Acta Rheumatol Scand. 1956;2:109–116.
    1. Hough T. Ergographic studies in muscular soreness. Am J Physiol – Legacy Content. 1902;7:76–92.
    1. Clarkson PM, Tremblay I. Exercise-induced muscle damage, repair, and adaptation in humans. J Appl Physiol. 1988;65:1–6.
    1. Givli S. Contraction induced muscle injury: towards personalized training and recovery programs. Ann Biomed Eng. 2015;43(2):388–403.
    1. Petrof BJ. The molecular basis of activity-induced muscle injury in Duchenne muscular dystrophy. Mol Cell Biochem. 2001;179:111–123.
    1. Andersen SP, Sveen ML, Hansen RS, et al. Creatine kinase response to high-intensity aerobic exercise in adult-onset muscular dystrophy. Muscle Nerve. 2013;48(6):897–901.
    1. Koskinen SO, Höyhtyä M, Turpeenniemi-Hujanen T, et al. Serum concentrations of collagen degrading enzymes and their inhibitors after downhill running. Scand J Med Sci Sports. 2001;11(1):9–15.
    1. Buono R, Vantaggiato C, Pisa V, et al. Nitric oxide sustains long-term skeletal muscle regeneration by regulating fate of satellite cells via signaling pathways requiring Vangl2 and cyclic GMP. Stem Cells. 2012;30(2):197–209.
    1. Sciorati C, Buono R, Azzoni E, et al. Co-administration of ibuprofen and nitric oxide is an effective experimental therapy for muscular dystrophy, with immediate applicability to humans. Br J Pharmacol. 2010;160(6):1550–1560.
    1. Nunes VA, Gozzo AJ, Cruz-Silva I, et al. Vitamin E prevents cell death induced by mild oxidative stress in chicken skeletal muscle cells. Comp Biochem Physiol C Toxicol Pharmacol. 2005;141(3):225–240.
    1. Stavropoulos-Kalinoglou A, Metsios GS, Koutedakis Y, et al. Redefining overweight and obesity in rheumatoid arthritis patients. Ann Rheum Dis. 2007;66(10):1316–1321.
    1. Joosten LA, Abdollahi-Roodsaz S, Dinarello CA, O’Neill L, Netea MG. Toll-like receptors and chronic inflammation in rheumatic diseases: new developments. Nat Rev Rheumatol. 2016;12(6):344–357.
    1. Newham D, Jones D, Edwards R. Large delayed plasma creatine kinase changes after stepping exercise. Muscle Nerve. 1983;6:380–385.
    1. Mohr M, Draganidis D, Chatzinikolaou A, et al. Muscle damage, inflammatory, immune and performance responses to three football games in one week in competitive male players. Eur J Appl Physiol. 2016;116(1):179–193.
    1. Friden J, Sjostrom M, Ekblom B. A morphological study of delayed muscle soreness. Experientia. 1981;37:506–507.
    1. Raastad T, Owe SG, Paulsen G, et al. Changes in calpain activity, muscle structure, and function after eccentric exercise. Med Sci Sports Exerc. 2010;42:86–95.
    1. Hamer P, McGeachie J, Davies M, Grounds M. Evans blue dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J Anat. 2002;200:69–79.
    1. Crameri RM, Langberg H, Magnusson P, et al. Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol. 2004;558:333–340.
    1. Stauber WT, Clarkson PM, Fritz VK, Evans WJ. Extracellular matrix disruption and pain after eccentric muscle action. J Appl Physiol. 1990;69:868–874.
    1. Allen DG, Gervasio OL, Yeung EW, Whitehead NP. Calcium and the damage pathways in muscular dystrophy. Can J Physiol Pharmacol. 2010;88:83–91.
    1. Whitehead NP, Pham C, Gervasio OL, Allen DG. N-Acetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice. J Physiol. 2008;586:2003–2014.
    1. Lauritzen F, Paulsen G, Raastad T, Bergersen LH, Owe SG. Gross ultrastructural changes and necrotic fiber segments in elbow flexor muscles after maximal voluntary eccentric action in humans. J Appl Physiol. 2009;107:1923–1934.
    1. Yu JG, Liu JX, Carlsson L, Thornell LE, Stal PS. Re-evaluation of sarcolemma injury and muscle swelling in human skeletal muscles after eccentric exercise. PLoS One. 2013;8:e62056.
    1. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M. Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol. 2007;583:365–380.
    1. Newham DJ, McPhail G, Mills KR, Edwards RH. Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci. 1983;61:109–122.
    1. Lieber RL, Thornell LE, Friden J. Muscle cytoskeletal disruption occurs within the first 15 min of cyclic eccentric contraction. J Appl Physiol. 1996;80:278–284.
    1. Beaton LJ, Tarnopolsky MA, Phillips SM. Contraction-induced muscle damage in humans following calcium channel blocker administration. J Physiol. 2002;544:849–859.
    1. Lovering RM, De Deyne PG. Contractile function, sarcolemma integrity, and the loss of dystrophin after skeletal muscle eccentric contraction-induced injury. Am J Physiol Cell Physiol. 2004;286:C230–C238.
    1. Trump BF, Laiho KA, Mergner WJ, Arstila AU. Studies on the subcellular pathophysiology of acute lethal cell injury. Beitr Pathol. 1974;152:243–271.
    1. Paulsen G, Egner IM, Drange M, et al. A COX-2 inhibitor reduces muscle soreness, but does not influence recovery and adaptation after eccentric exercise. Scand J Med Sci Sports. 2010;20:e195–e207.
    1. Cavassani KA, Ishii M, Wen H, et al. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med. 2008;205:2609–2621.
    1. Mathes AL, Lafyatis R. Role for Toll-like receptor 3 in muscle regeneration after cardiotoxin injury. Muscle Nerve. 2011;43:733–740.
    1. Jarvinen TA, Jarvinen TL, Kaariainen M, Kalimo H, Jarvinen M. Muscle injuries: biology and treatment. Am J Sports Med. 2005;33:745–764.
    1. Lieber RL, Friden J. Mechanisms of muscle injury gleaned from animal models. Am J Phys Med Rehabil. 2002;81:S70–S79.
    1. Stauber WT, Smith CA. Cellular responses in exertion-induced skeletal muscle injury. Mol Cell Biochem. 1998;179:189–196.
    1. Yu JG, Carlsson L, Thornell LE. Evidence for myofibril remodelling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol. 2004;121:219–227.
    1. Malm C, Sjodin TLB, Sjoberg B, et al. Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol. 2004;556:983–1000.
    1. Hyldahl RD, Hubal MJ. Lengthening our perspective: morphological, cellular, and molecular responses to eccentric exercise. Muscle Nerve. 2014;49:155–170.
    1. Jamurtas AZ, Theocharis V, Tofas T, et al. Comparison between leg and arm eccentric exercises of the same relative intensity on indices of muscle damage. Eur J Appl Physiol. 2005;95(2–3):179–185.
    1. Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004;84:649–698.
    1. Heinemeier KM, Olesen JL, Haddad F, et al. Expression of collagen and related growth factors in rat tendon and skeletal muscle in response to specific contraction types. J Physiol. 2007;582:1303–1316.
    1. Tofas T, Jamurtas AZ, Fatouros I, et al. The effects of plyometric exercise on muscle performance, muscle damage and collagen breakdown. J Strength Cond Res. 2008;22(2):490–496.
    1. Husmann I, Soulet L, Gautron J, Martelly I, Barritault D. Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev. 1996;7:249–258.
    1. Tidball J. Inflammatory processes in muscle injury and repair. Am J Physiol. 2005;288:R345–R353.
    1. Hyldahl RD, Xin L, Hubal MJ, Moeckel-Cole S, Chipkin S, Clarkson PM. Activation of nuclear factor-fkappagB following muscle eccentric contractions in humans is localized primarily to skeletal muscleresiding pericytes. FASEB J. 2011;25:2956–2966.
    1. Hyldahl RD, Schwartz LM, Clarkson PM. NF-KB activity functions in primary pericytes in a cell- and non-cell-autonomous manner to affect myotube formation. Muscle Nerve. 2013;47:522–531.
    1. Li H, Malhotra S, Kumar A. Nuclear factor-kappa B signalling in skeletal muscle atrophy. J Mol Med. 2008;86:1113–1126.
    1. Clarkson PM, Dedrick ME. Exercise-induced muscle damage, repair, and adaptation in old and young subjects. J Gerontol. 1988;43:M91–M96.
    1. Draganidis D, Chatzinikolaou A, Avloniti A, et al. Flexor and extensor strength after a football match. PLoS One. 2015;10(6):e0128072.
    1. Clarkson PM, Hubal MJ. Exercise-induced muscle damage in humans. Am J Phys Med Rehabil. 2002;81:S52–S69.
    1. Chatzinikolaou A, Christoforidis C, Avloniti A, et al. A microcycle of inflammation following a team-handball game. J Strength Cond Res. 2013;28(7):1981–1994.
    1. Morgan DL. New insights into the behavior of muscle during active lengthening. Biophys J. 1990;57:209–221.
    1. Komazaki S, Ito K, Takeshima H, Nakamura H. Deficiency of triad formation in developing skeletal muscle cells lacking junctophilin type 1. FEBS Lett. 2002;524:225–229.
    1. Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP. Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol Cell Physiol. 2010;298:C365–C376.
    1. Balnave CD, Allen DG. Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J Physiol. 1995;488:25–36.
    1. Balnave CD, Davey DF, Allen DG. Distribution of sarcomere length and intracellular calcium in mouse skeletal muscle following stretch-induced injury. J Physiol. 1997;502:649–659.
    1. Warren GL, Ingalls CP, Lowe DA, Armstrong RB. What mechanisms contribute to the strength loss that occurs during and in the recovery from skeletal muscle injury? J Orthop Sports Phys Ther. 2002;32:58–64.
    1. Murphy RM, Dutka TL, Horvath D, Bell JR, Delbridge LM, Lamb GD. Ca21-dependent proteolysis of junctophilin-1 and junctophilin-2 in skeletal and cardiac muscle. J Physiol. 2013;591:719–729.
    1. Chan S, Head SI, Morley JW. Branched fibers in dystrophic mdx muscle are associated with a loss of force following lengthening contractions. Am J Physiol Cell Physiol. 2007;293:C985–C992.
    1. Whitehead N, Streamer M, Lusambili L, Sachs F, Allen D. Streptomycin reduces stretch-induced membrane permeability in muscles from mdx mice. Neuromuscul Disord. 2006;16:845–854.
    1. Yeung EW, Whitehead NP, Suchyna TM, Gottlieb PA, Sachs F, Allen DG. Effects of stretch-activated channel blockers on [Ca21]i and muscle damage in the mdx mouse. J Physiol. 2005;562:367–380.
    1. Butterfield TA, Best TM. Stretch-activated ion channel blockade attenuates adaptations to eccentric exercise. Med Sci Sports Exerc. 2009;41:351–356.
    1. Clarkson PM, Devaney JM, Gordish-Dressman H, et al. ACTN3 genotype is associated with increases in muscle strength in response to resistance training in women. J Appl Physiol. 2005;99:154–163.
    1. Seto JT, Lek M, Quinlan KGR, et al. Deficiency of falphag-actinin-3 is associated with increased susceptibility to contraction-induced damage and skeletal muscle remodeling. Hum Mol Genet. 2011;20:2914–2927.
    1. Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc. 1992;24:512–520.
    1. Chatzinikolaou A, Draganidis D, Avloniti A, et al. The microcycle of inflammation and performance changes after a basketball match. J Sports Sci. 2013;32(9):870–882.
    1. Armstrong RB. Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc. 1984;16:529–538.
    1. Radak Z, Naito H, Taylor AW, Goto S. Nitric oxide: is it the cause of muscle soreness? Nitric Oxide. 2012;26(2):89–94.
    1. Murase S, Terazawa E, Queme F, et al. Bradykinin and nerve growth factor play pivotal roles in muscular mechanical hyperalgesia after exercise (delayed-onset muscle soreness) J Neurosci. 2010;30:3752–3761.
    1. Nie H, Madeleine P, Arendt-Nielsen L, Graven-Nielsen T. Temporal summation of pressure pain during muscle hyperalgesia evoked by nerve growth factor and eccentric contractions. Eur J Pain. 2009;13:704–710.
    1. Sewright K, Hubal M, Kearns A, Holbrook M, Clarkson P. Sex differences in response to maximal eccentric exercise. Med Sci Sports Exerc. 2008;40:242–251.
    1. Clarkson P, Hubal M. Are women less susceptible to exercise induced muscle damage? Curr Opin Clin Nutr Metab Care. 2001;4:527–531.
    1. Enns D, Iqbal S, Tiidus P. Oestrogen receptors mediate oestrogen-induced increases in post-exercise rat skeletal muscle satellite cells. Acta Physiol (Oxf) 2008;194:81–93.
    1. Iqbal S, Thomas A, Bunyan K, Tiidus P. Progesterone and estrogen influence postexercise leukocyte infiltration in overiectomized female rats. Appl Physiol Nutr Metab. 2008;33:1207–1212.
    1. Sonobe T, Inagaki T, Sudo M, Poole DC, Kano Y. Sex differences in intracellular Ca(21) accumulation following eccentric contractions of rat skeletal muscle in vivo. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1006–R1012.
    1. McGinley C, Shafat A, Donnelly A. Does antioxidant vitamin supplementation protect against muscle damage? Sports Med. 2009;39:1011–1032.
    1. Cooke M, Rybalka E, Williams A, Cribb P, Hayes A. Creatine supplementation enhances muscle force recovery after eccentrically induced muscle damage in healthy individuals. Int Soc Sports Nutr. 2009;6:13.
    1. Howatson G, Hoad M, Goodall S, Tallent J, Bell PG, French DN. Exercise-induced muscle damage is reduced in resistance-trained males by branched chain amino acids: a randomized, double-blind, placebo controlled study. J Int Soc Sports Nutr. 2012;9:20.
    1. Bowtell JL, Sumners DP, Dyer A, Fox P, Mileva KN. Montmorency cherry juice reduces muscle damage caused by intensive strength exercise. Med Sci Sports Exerc. 2011;43:1544–1551.
    1. Trombold JR, Reinfeld AS, Casler JR, Coyle EF. The effect of pomegranate juice supplementation on strength and soreness after eccentric exercise. J Strength Cond Res. 2011;25:1782–1788.
    1. Connolly DJ, McHugh MP, Padilla-Zakour OI. Efficacy of a tart cherry juice blend in preventing the symptoms of muscle damage. Br J Sports Med. 2006;40:679–683.
    1. Rosene J, Matthews T, Ryan C, et al. Short and longer-term effects of creatine supplementation on exercise induced muscle damage. J Sports Sci Med. 2009;8:89–96.
    1. Kim J, Lee J, Kim S, Yoon D, Kim J, Sung DJ. Role of creatine supplementation in exercise-induced muscle damage: a mini review. J Exerc Rehab. 2015;11(5):244–250.
    1. Sousa M, Teixeira VH, Soares J. Dietary strategies to recover from exercise-induced muscle damage. Int J Food Sci Nutr. 2014;65(2):151–163.
    1. Theodorou AA, Nikolaidis MG, Paschalis V, et al. No effect of antioxidant supplementation on muscle performance and blood redox status adaptations to eccentric training. Am J Clin Nutr. 2011;93:1373–1383.
    1. 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. 1996;80:1006–1013.
    1. Malm C, Nyberg P, Engstrom M, et al. Immunological changes in human skeletal muscle and blood after eccentric exercise and multiple biopsies. J Physiol. 2000;529:243–262.
    1. Raastad T, Risoy BA, Benestad HB, Fjeld JG, Hallen J. Temporal relation between leukocyte accumulation in muscles and halted recovery 10–20 h after strength exercise. J Appl Physiol. 2003;95:2503–2509.
    1. Hamada K, Vannier E, Sacheck JM, Witsell AL, Roubenoff R. Senescence of human skeletal muscle impairs the local inflammatory cytokine response to acute eccentric exercise. FASEB J. 2005;19:264–266.
    1. Cannon JG, St Pierre BA. Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem. 1998;179:159–167.
    1. Nguyen HX, Tidball JG. Null mutation of gp91phox reduces muscle membrane lysis during muscle inflammation in mice. J Physiol. 2003;553:833–841.
    1. Peake JM. Exercise-induced alterations in neutrophil degranulation and respiratory burst activity: possible mechanisms of action. Exerc Immunol Rev. 2002;8:49–100.
    1. Fielding R, Manfredi T, Ding W, Fiatarone M, Evans W, Cannon J. Acute phase response in exercise III. Neutrophil and IL-beta accumulation in skeletal muscle. Am J Physiol. 1993;265:R166–R172.
    1. Arnaout MA. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood. 1990;75:1037–1050.
    1. Petridou A, Chatzinikolaou A, Fatouros IG, et al. Resistance exercise does not affect the serum concentrations of cell adhesion molecules. Br J Sports Med. 2007;41:76–79.
    1. Cannon J, Orencole S, Fielding R, et al. Acute phase response in exercise: interaction of age and vitamin E on neutrophils and muscle enzyme release. Am J Physiol. 1990;259:R1214–R1219.
    1. Barbas I, Fatouros IG, Douroudos II, et al. Physiological and performance adaptations of elite Greco-Roman wrestlers during a one-day tournament. Eur J Appl Physiol. 2011;111(7):1421–1436.
    1. Nieman DC, Davis JM, Henson DA, et al. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol. 2003;94:1917–1925.
    1. Trappe TA, White F, Lambert CP, Cesar D, Hellerstein M, Evans WJ. Effect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am J Physiol Endocrinol Metab. 2002;282:E551–556.
    1. Paulsen G, Crameri R, Benestad HB, et al. Time course of leukocyte accumulation in human muscle after eccentric exercise. Med Sci Sports Exerc. 2010;42:75–85.
    1. Round JM, Jones DA, Cambridge G. Cellular infiltrates in human skeletal muscle: exercise induced damage as a model for inflammatory muscle disease? J Neurol Sci. 1987;82:1–11.
    1. Peake JM, Suzuki K, Wilson G, et al. Exercise-induced muscle damage, plasma cytokines and markers of neutrophil activation. Med Sci Sports Exerc. 2005;37:737–745.
    1. Pizza FX, Davis BH, Henrickson SD, et al. Adaptation to eccentric exercise: effect on CD64 and CD11b/CD18 expression. J Appl Physiol. 1996;80:47–55.
    1. Draganidis D, Chatzinikolaou A, Jamurtas AZ, et al. The time-frame of acute resistance exercise effects on football skill performance: the impact of exercise intensity. J Sport Sci. 2013;31(7):714–722.
    1. Malm C, Lenkei R, Sjodin B. Effects of eccentric exercise on the immune system in men. J Appl Physiol. 1999;86:461–468.
    1. Fatouros IG, Chatzinikolaou A, Paltoglou G, et al. Stress of acute resistance exercise results in catecholaminergic 1 rather than hypothalamic-pituitary-adrenal axis stimulation. Stress. 2010;13(6):461–468.
    1. Fatouros IG, Chatzinikolaou A, Douroudos II, et al. Time-course of changes in oxidative stress and antioxidant status responses following a soccer game. J Strength Cond Res. 2010;24(12):3278–3286.
    1. Theodorou AA, Nikolaidis MG, Paschalis V, et al. Comparison between G6PD-deficient and normal individuals after eccentric exercise. Med Sci Sports Exerc. 2010;42(6):1113–1121.
    1. Chatzinikolaou A, Fatouros IG, Gourgoulis V, et al. Time course of responses in performance and inflammatory responses following acute plyometric exercise. J Strength Cond Res. 2010;24(5):1389–1398.
    1. Ispirlidis I, Fatouros IG, Jamurtas AZ, et al. Time-course of changes in performance and inflammatory responses following a football game. Clin J Sports Med. 2008;18(5):423–431.
    1. Margonis K, Fatouros IG, Jamourtas AZ, et al. Oxidative stress bio-markers responses to physical overtraining: implications for diagnosis. Free Rad Biol Med. 2007;43:901–910.
    1. Michailidis Y, Jamurtas AZ, Nikolaidis MG, et al. Sampling time is crucial for measurement of exercise-induced oxidative stress markers. Med Sci Sports Exerc. 2007;39(7):1107–1113.
    1. Brenner IK, Natale VM, Vasiliou P, Moldoveanu AI, Shek PN, Shephard RJ. Impact of three different types of exercise on components of the inflammatory response. Eur J Appl Physiol. 1999;80:452–460.
    1. Suzuki K, Nakaji S, Yamada M, Totsuka M, Sato K, Sugawara K. Systemic inflammatory response to exhaustive exercise. Cytokine kinetics. Exerc Immunol Rev. 2002;8:6–48.
    1. Toft AD, Jensen LB, Bruunsgaard H, et al. Cytokine response to eccentric exercise in young and elderly humans. Am J Physiol. 2002;283:C289–C295.
    1. Smith L, Anwar A, Fragen M, Rananto C, Johnson R, Holbert D. Cytokines and cell adhesion molecules associated with high-intensity eccentric exercise. Eur J Appl Physiol. 2000;82:61–67.
    1. Phillips T, Childs AC, Dreon DM, Phinney S, Leeuwenburgh C. A dietary supplement attenuates IL-6 and CRP after eccentric exercise in untrained males. Med Sci Sports Exerc. 2003;35:2032–2037.
    1. Childs A, Jacobs C, Kaminski T, Halliwell B, Leeuwenburgh C. Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after an acute muscle injury induced by eccentric exercise. Free Radic Biol Med. 2001;31:745–753.
    1. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98:1154–1162.
    1. Wright CR, Della-Gatta PA, Fatouros IG, et al. The role and regulation of G-CSF and its receptor in skeletal muscle inflammation. J Interf Cytokine Res. 2015;35(9):710–719.
    1. Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol. 1999;515:287–291.
    1. Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol. 2003;285:E433–E437.
    1. Bogdan C, Paik J, Vodovotz Y, Nathan C. Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-beta and interleukin-10. J Biol Chem. 1992;267:23301–23308.
    1. Wang P, Wu P, Siegel MI, Egan RW, Billah MM. IL-10 inhibits transcription of cytokine genes in human peripheral blood mononuclear cells. J Immunol. 1994;153:811–816.
    1. Dinarello CA. The role of the interleukin-1-receptor antagonist in blocking inflammation mediated by interleukin-1. N Engl J Med. 2000;343:732–734.
    1. Bruunsgaard H, Galbo H, Halkjaer-Kristensen J, Johansen TL, MacLean DA, Pedersen BK. Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J Physiol. 1997;499(Pt 3):833–841.
    1. Hirose L, Nosaka K, Newton M, et al. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc Immunol Rev. 2004;10:75–90.
    1. Nieman DC, Dumke CL, Henson DA, McAnulty SR, Gross SJ, Lind RH. Muscle damage is linked to cytokine changes following a 160-km race. Brain Behav Immun. 2005;19:398–403.
    1. Steensberg A, Keller C, Starkie RL, Osada T, Febbraio MA, Pedersen BK. IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle. Am J Physiol Endocrinol Metab. 2002;283:E1272–E1278.
    1. Warren GL, O’farrell L, Summan M, et al. Role of CC chemokines in skeletal muscle functional restoration after injury. Am J Physiol Cell Physiol. 2004;286:C1031–C1036.
    1. Shireman PK, Contreras-Shannon V, Ochoa O, Karia BP, Michalek JE, McManus LM. MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J Leukoc Biol. 2007;81:775–785.
    1. Warren GL, Hulderman T, Jensen N, et al. Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J. 2002;16:1630–1632.
    1. Serrano AL, Baeza-Raja B, Perdiguero E, Jardi M, Munoz-Canoves P. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 2008;7:33–44.
    1. Baeza-Raja B, Munoz-Canoves P. p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: role of interleukin-6. Mol Biol Cell. 2004;15:2013–2026.
    1. Byrne C, Twist C, Eston R. Neuromuscular function after exercise-induced muscle damage: theoretical and applied implications. Sports Med. 2004;34:49–69.
    1. Friden J, Lieber RL. Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand. 2001;171:321–326.
    1. Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol. 2001;537:333–345.
    1. Brooks SV, Zerba E, Faulkner JA. Injury to muscle fibres after single stretches of passive and maximally stimulated muscles in mice. J Physiol. 1995;488(Pt 2):459–469.
    1. Gregory JE, Morgan DL, Allen TJ, Proske U. The shift in muscle’s length-tension relation after exercise attributed to increased series compliance. Eur J Appl Physiol. 2007;99:431–441.
    1. Lieber RL, Friden J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol. 1993;74:520–526.
    1. Lieber RL, Woodburn TM, Friden J. Muscle damage induced by eccentric contractions of 25% strain. J Appl Physiol. 1991;70:2498–2507.
    1. Talbot JA, Morgan DL. Quantitative analysis of sarcomere non-uniformities in active muscle following a stretch. J Muscle Res Cell Motil. 1996;17:261–268.
    1. Talbot JA, Morgan DL. The effects of stretch parameters on eccentric exercise-induced damage to toad skeletal muscle. J Muscle Res Cell Motil. 1998;19:237–245.
    1. Nosaka K, Newton M, Sacco P. Delayed-onset muscle soreness does not reflect the magnitude of eccentric exercise-induced muscle damage. Scand J Med Sci Sports. 2002;12:337–346.
    1. Nosaka K, Sakamoto K, Newton M, Sacco P. The repeated bout effect of reduced-load eccentric exercise on elbow flexor muscle damage. Eur J Appl Physiol. 2001;85:34–40.
    1. Chapman D, Newton M, Sacco P, Nosaka K. Greater muscle damage induced by fast versus slow velocity eccentric exercise. Int J Sports Med. 2006;27:591–598.
    1. Chapman DW, Newton M, McGuigan M, Nosaka K. Effect of lengthening contraction velocity on muscle damage of the elbow flexors. Med Sci Sports Exerc. 2008;40:926–933.
    1. Paddon-Jones D, Keech A, Lonergan A, Abernethy P. Differential expression of muscle damage in humans following acute fast and slow velocity eccentric exercise. J Sci Med Sport. 2005;8:255–263.
    1. Nedelec M, McCall A, Carling C, Legall F, Berthoin S, Dupont G. Recovery in soccer: part I—post-match fatigue and time course of recovery. Sports Med. 2012;42(12):997–1015.
    1. Hubal MJ, Chen TC, Thompson PD, Clarkson PM. Inflammatory gene changes associated with the repeated-bout effect. Am J Physiol Regul Integr Comp Physiol. 2008;294:R1628–R1637.
    1. Stupka N, Tarnopolsky MA, Yardley NJ, Phillips SM. Cellular adaptation to repeated eccentric exercise-induced muscle damage. J Appl Physiol. 2001;91:1669–1678.
    1. 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.
    1. Manfredi TG, Fielding RA, O’Reilly KP, Meredith CN, Lee HY, Evans WJ. Plasma creatine kinase activity and exercise-induced muscle damage in older men. Med Sci Sports Exerc. 1991;23:1028–1034.
    1. Sorichter S, Puschendorf B, Mair J. Skeletal muscle injury induced by eccentric muscle action: muscle proteins as markers of muscle fiber injury. Exerc Immunol Rev. 1999;5:5–21.
    1. Nosaka K, Clarkson PM. Variability in serum creatine kinase response after eccentric exercise of the elbow flexors. Int J Sports Med. 1996;17:120–127.
    1. Jones DA, Newham DJ, Round JM, Tolfree SE. Experimental human muscle damage: morphological changes in relation to other indices of damage. J Physiol. 1986;375:435–448.
    1. Clarkson PM, Newham DJ. Associations between muscle soreness, damage, and fatigue. Adv Exp Med Biol. 1995;384:457–469.
    1. Sayers SP, Clarkson PM. Force recovery after eccentric exercise in males and females. Eur J Appl Physiol. 2001;84:122–126.
    1. Foley JM, Jayaraman RC, Prior BM, Pivarnik JM, Meyer RA. MR measurements of muscle damage and adaptation after eccentric exercise. J Appl Physiol. 1999;87:2311–2318.
    1. Bishop PA, Jones E, Woods AK. Recovery from training: a brief review. J Strength Cond Res. 2008;22(3):1015–1024.
    1. Howatson F, van Someren KA. The prevention and treatment of exercise-induced muscle damage. Sports Med. 2008;38(6):483–503.
    1. Connolly DAJ, Sayers SP, McHugh MP. Treatment and prevention of delayed onset muscle soreness. J Strength Cond Res. 2003;17(1):197–208.
    1. Cheung K, Hume PA, Maxwell L. Delayed onset muscle soreness treatment strategies and performance factors. Sports Med. 2003;33(2):145–164.
    1. Gomez-Cabrera MC, Domenech E, Romagnoli M, et al. Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr. 2008;87:142–149.
    1. Chen TC. Variability in muscle damage after eccentric exercise and the repeated bout effect. Res Q Exerc Sport. 2006;77:362–371.
    1. Hubal MJ, Rubinstein SR, Clarkson PM. Mechanisms of variability in strength loss after muscle-lengthening actions. Med Sci Sports Exerc. 2007;39:461–468.
    1. Sayers SP, Knight CA, Clarkson PM. Neuromuscular variables affecting the magnitude of force loss after eccentric exercise. J Sports Sci. 2003;21:403–410.
    1. Lavender AP, Nosaka K. Responses of old men to repeated bouts of eccentric exercise of the elbow flexors in comparison with young men. Eur J Appl Physiol. 2006;97:619–626.
    1. Zalavras A, Fatouros IG, Deli CK, et al. Age-related responses in circulating markers of redox status in healthy adolescents and adults during the course of a training macrocycle. Oxid Med Cell Longev. 2015 article ID 283921.
    1. Nosaka K, Sakamoto K, Newton M, Sacco P. How long does the protective effect on eccentric exercise-induced muscle damage last? Med Sci Sports Exerc. 2001;33:1490–1495.
    1. 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.
    1. Jamurtas AZ, Fatouros IG, Buckenmeyer PJ, et al. Effects of plyo-metric exercise on muscle soreness and creatine kinase levels and its comparison to eccentric and concentric exercise. J Strength Cond Res. 2000;14(1):68–74.
    1. Yamin C, Duarte JA, Oliveira JM, et al. IL6 (-174) and TNFA (-308) promoter polymorphisms are associated with systemic creatine kinase response to eccentric exercise. Eur J Appl Physiol. 2008;104:579–586.
    1. Hubal MJ, Devaney JM, Hoffman EP, et al. CCL2 and CCR2 polymorphisms are associated with markers of exercise-induced skeletal muscle damage. J Appl Physiol. 2010;108:1651–1658.
    1. Appell HJ, Soares JM, Duarte JA. Exercise, muscle damage and fatigue. Sports Med. 1992;13:108–115.
    1. Falvo MJ, Bloomer RJ. Review of exercise-induced muscle injury: relevance for athletic populations. Res Sports Med. 2006;14:65–82.
    1. Gibala MJ, Interisano SA, Tarnopolsky MA, et al. Myofibrillar disruption following acute concentric and eccentric resistance exercise in strength-trained men. Can J Physiol Pharmacol. 2000;78:656–661.
    1. Chen CH, Nosaka K, Chen HL, Lin MJ, Tseng KW, Chen TC. Effects of flexibility training on eccentric exercise-induced muscle damage. Med Sci Sports Exerc. 2011;43(3):491–500.
    1. Nikolaidis MG, Paschalis V, Giakas G, et al. Decreased blood oxidative stress after repeated eccentric exercise. Med Sci Sports Exerc. 2007;39(7):1080–1089.
    1. Pizza FX, Baylies H, Mitchell JB. Adaptation to eccentric exercise: neutrophils and E-selectin during early recovery. Can J Appl Physiol. 2001;26:245–253.

Source: PubMed

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