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Muscle function after exercise-induced muscle damage and rapid adaptation
Abstract
This brief review focuses on the time course of changes in muscle function and other correlates of muscle damage following maximal effort eccentric actions of the forearm flexor muscles. Data on 109 subjects are presented to describe an accurate time course of these changes and attempt to establish relationships among the measures. Peak soreness is experienced 2-3 d postexercise while peak swelling occurs 5 d postexercise. Maximal strength and the ability to fully flex the arm show the greatest decrements immediately after exercise with a linear restoration of these functions over the next 10 d. Blood creatine kinase (CK) levels increase precipitously at 2 d after exercise which is also the time when spontaneous muscle shortening is most pronounced. Whether the similarity in the time courses of some of these responses implies that they are caused by similar factors remains to be determined. Performance of one bout of eccentric exercise produces an adaptation such that the muscle is more resistant to damage from a subsequent bout of exercise. The length of the adaptation differs among the measures such that when the exercise regimens are separated by 6 wk, all measures show a reduction in response on the second, compared with the first, bout. After 10 wk, only CK and muscle shortening show a reduction in response. After 6 months only the CK response is reduced. A combination of cellular factors and neurological factors may be involved in the adaptation process.
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“Recall that the greatest declines in muscle function occur immediately following eccentric contraction-induced injury, yet markers of muscle damage are not fully apparent until 1–2 days after injury (34, 47, 52).”
From Phytoecdysteroids Accelerate Recovery of Skeletal Muscle Function Following in vivo Eccentric Contraction-Induced Injury in Adult and Old Mice (2021) · cites this paper as [52]
In the citing paper
“However, there is a dissociation between muscle function and histological markers of muscle damage that disputes the latter causal relationship.”
From Phytoecdysteroids Accelerate Recovery of Skeletal Muscle Function Following in vivo Eccentric Contraction-Induced Injury in Adult and Old Mice (2021) · cites this paper as [52]
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Kim, H. J., Lee, Y. H., & Kim, C. K. (2009) · European Journal of Applied Physiology · doi:10.1007/s00421-008-0961-x · Cited by 127
“Plasma activities of creatine phosphokinase (CPK) and high-sensitivity C-reactive protein (hs-CRP), on the other hand, are widely used as a marker of muscle damage and inXammation (Clarkson et al. 1992; Kuipers 1994; Noakes 1987).”
BackgroundContraction‐induced muscle damage in humans following calcium channel blocker administration
Beaton, L. J., Tarnopolsky, M. A., & Phillips, S. M. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.022350 · Cited by 122
“…cells (Duncan, 1987), increased resting intracellular calcium concentration (Duan et al. 1990; Warren et al. 1993; Lowe et al. 1994), muscle enzyme release (Clarkson et al. 1992; Sayers et al. 2000), muscle soreness and a profound loss of both voluntary and involuntary force (Gibala et al. 1995).”
BackgroundThe Effect of a High Resistance Exercise Program in Slowly Progressive Neuromuscular Disease
Kilmer, D. D., McCrory, M. A., Wright, N. C., Aitkens, S. G., & Bernauer, E. M. (1994) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/s0003-9993(21)01620-8 · Cited by 122
Slater, G. J., & Jenkins, D. (2000) · Sports Medicine · doi:10.2165/00007256-200030020-00004 · Cited by 120
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Self-citationAndonian, P., Viallon, M., Goff, C. M. L., de Bourguignon, C., Tourel, C., Morel, J., Giardini, G., Gergelé, L., Millet, G. P., & Croisille, P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161855 · Cited by 122
Oxidative Stress Response in Trained Men following Repeated Squats or Sprints
Bloomer, R. J., Falvo, M. J., Fry, A. C., Schilling, B. K., Smith, W. A., & Moore, C. A. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000227408.91474.77 · Cited by 118
“Subjects completed a subjective rating of muscle soreness felt during body weight only squatting using a 10-cm visual analog scale as previously described (8).”
MethodResponse of males and females to high-force eccentric exercise
Rinard, J., Clarkson, P. M., SMITH, L. L., & Grossman, M. (2000) · Journal of Sports Sciences · doi:10.1080/026404100364965 · Cited by 117
“Maximal voluntary force production and range of motion provide less variable and more reliable methods for assessing exercise-induced muscle injury than serum creatine kinase activity (Clarkson et al., 1992; Warren et al., 1999).”
BackgroundMethodInfluentialSelf-citationMuscle damage and soreness after endurance exercise of the elbow flexors
Nosaka, K., Newton, M. J., & Sacco, P. (2002) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200206000-00003 · Cited by 118
“After maximal eccentric exercise or resistance training containing eccentric loading, soreness tends to have an onset delay of some 8–12 h, and peaks 1–3 d after exercise (6,7).”
BackgroundInfluentialSelf-citationEffect of bench press exercise intensity on muscle soreness and inflammatory mediators
Uchida, M. C., Nosaka, K., Ugrinowitsch, C., Yamashita, A. S., Martins, E., Moriscot, A. S., & Aoki, M. S. (2009) · Journal of Sports Sciences · doi:10.1080/02640410802632144 · Cited by 114
“In the present study, only plasma creatine kinase activity was used as a marker of muscle damage, and it has been questioned whether creatine kinase activity in the blood can be used as a quantitative marker of muscle damage, mainly because of a large variability in the creatine kinase response (Clarkson et al., 1992).”
MethodSelf-citationAssociations Between Muscle Soreness, Damage, and Fatigue
CLARKSON, P. M., & Newham, D. J. (1995) · Advances in experimental medicine and biology · doi:10.1007/978-1-4899-1016-5_35 · Cited by 116
Self-citationEvidence of a contralateral repeated bout effect after maximal eccentric contractions
Howatson, G., & van Someren, K. A. (2007) · European Journal of Applied Physiology · doi:10.1007/s00421-007-0489-5 · Cited by 115
“…to performance and subsequent training bouts and is typically manifested as an increase in concentrations of intramuscular protein in serum, reduced torque production and range of motion (ROM), increased limb girth and pain (Clarkson et al. 1992; McHugh et al. 2000; Nosaka and Newton 2002).”
BackgroundResultInfluentialDecreased EMG median frequency during a second bout of eccentric contractions
Warren, G. L., HERMANN, K. M., Ingalls, C. P., Masselli, M. R., & Armstrong, R. B. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200004000-00015 · Cited by 114
Marqués-Jiménez, D., Calleja-González, J., Arratibel-Imaz, I., Delextrat, A. A., & Terrados, N. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.10.027 · Cited by 116
Effect of a carbohydrate mouthwash on running time-trial performance
Whitham, M., & McKinney, J. (2007) · Journal of Sports Sciences · doi:10.1080/02640410601113676 · Cited by 113
“Participants were asked to rate their gastrointestinal symptoms and thirst using a visual analogue scale (Clarkson, Nosaka, & Braun, 1992 ; Peters et al , 1993 ) at the beginning and end of each trial.”
MethodRecovery of skeletal muscle contractility after high- and moderate-intensity strength exercise
Raastad, T., & Hallén, J. (2000) · European Journal of Applied Physiology · doi:10.1007/s004210050673 · Cited by 124
“Creatine kinase (CK) has been used as a marker of skeletal muscle damage after eccentric exercise (Clarkson et al. 1992; Nosaka and Clarkson 1995).”
MethodAttenuation of indirect markers of eccentric exercise-induced muscle damage by curcumin
Tanabe, Y., Maeda, S., Akazawa, N., Zempo‐Miyaki, A., Choi, Y., Ra, S., Imaizumi, A., Otsuka, Y., & Nosaka, K. (2015) · European Journal of Applied Physiology · doi:10.1007/s00421-015-3170-4 · Cited by 117
“Unaccustomed exercise, especially that consists of highintensity and/or large number of eccentric (lengthening) contractions, induces muscle damage (Clarkson et al. 1992).”
BackgroundSelf-citationKraemer, W. J., Bush, J. A., WICKHAM, R. B., Denegar, C. R., Gómez, A. L., Gotshalk, L. A., Duncan, N. D., Volek, J. S., Newton, R. U., Putukian, M., et al. (2001) · Journal of Sport Rehabilitation · doi:10.1123/jsr.10.1.11 · Cited by 111
West, D., Abou Sawan, S., Mazzulla, M., Williamson, E., & Moore, D. (2017) · Nutrients · doi:10.3390/nu9070735 · Cited by 112
“While this acute loss of performance, potentially mediated by exercise-induced muscle damage [19,20], may be considered a normal byproduct of any training program, the rapid resolution of these negative effects could ultimately facilitate a higher quality training stimulus during in-season trainig and/or sport perform…”
BackgroundLavender, A. P., & Nosaka, K. (2005) · European Journal of Applied Physiology · doi:10.1007/s00421-005-0069-5 · Cited by 111
“Indicators of muscle damage Several indirect markers of muscle damage used in previous studies (Clarkson et al. 1992; Nosaka and Newton 2002; Nosaka et al. 2005) were measured before, immediately and 1 h after, and 1–5 days following exercise.”
BackgroundMethodSelf-citationA sport-physiological perspective on bird migration: evidence for flight-induced muscle damage
Guglielmo, C. G., Piersma, T., & Williams, T. D. (2001) · Journal of Experimental Biology · doi:10.1242/jeb.204.15.2683 · Cited by 111
Aging, Functional Capacity and Eccentric Exercise Training
Gault, M. L. (2013) · Aging and Disease · doi:10.14336/ad.2013.0400351 · Cited by 110
“maximal force production and serum levels of skeletal muscle enzymes or proteins such as creatine kinase [79-81].”
BackgroundBartolomei, S., Sadres, E., Church, D. D., Arroyo, E., Gordon, J. A., Varanoske, A. N., Wang, R., Beyer, K. S., Oliveira, L., Stout, J. R., et al. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3598-9 · Cited by 111
“The continued increase in CSA at P-24 h, P-48 h, and P-72 h may be related to the reactive hyperemia and to a delayed onset of muscle swelling (Clarkson et al. 1992) that was not detected following the HI protocol.”
BackgroundPrasartwuth, O., Allen, T., Butler, J. E., Gandevia, S. C., & Taylor, J. L. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.101600 · Cited by 110
“Unaccustomed eccentric exercise commonly results in muscle damage, characterized by a prolonged reduction in voluntary force and delayed muscle soreness (Newham et al. 1983; Newham et al. 1987; Clarkson et al. 1992; Howell et al. 1993; Prasartwuth et al. 2005).”
BackgroundMuscle damage induced by electrical stimulation
Nosaka, K., Aldayel, A. A., Jubeau, M., & Chen, T. C. (2011) · European Journal of Applied Physiology · doi:10.1007/s00421-011-2086-x · Cited by 111
“cise, the subsequent bout of the same exercise performed within several weeks later results in less muscle damage, and this phenomenon is known as the “repeated bout eVect” (Clarkson et al. 1992; McHugh 2003).”
BackgroundMethodInfluentialSelf-citationChen, T. C., Chen, H.-L., Lin, M.-J., Wu, C.-J., & Nosaka, K. (2009) · European Journal of Applied Physiology · doi:10.1007/s00421-009-1016-7 · Cited by 110
“A bout of unaccustomed eccentric exercise induces skeletal muscle damage that is characterised by a long-lasting decrease in muscle strength and range of motion (ROM) of the joint, delayed onset muscle soreness, swelling of the muscle, and increases in muscle-speciWc proteins such as creatine kinase (CK) and myoglobin…”
BackgroundResultInfluentialSelf-citationHormonal Responses from Concentric and Eccentric Muscle Contractions
DURAND, R. J., Castracane, V. D., HOLLANDER, D. B., Tryniecki, J. L., Bamman, M. M., NEAL, S. O., HEBERT, E. P., & Kraemer, R. R. (2003) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000069522.38141.0b · Cited by 110
“It has been documented that maximal ECC resistance training increases muscular strength (3,4) and produces muscle hypertrophy (13,15).”
BackgroundPerformance, biochemical, and endocrine changes during a competitive football game
Hoffman, J. R., Maresh, C. M., Newton, R. U., Rubin, M. R., French, D. N., Volek, J. S., Sutherland, J. W., ROBERTSON, M., mez, A. L. G., Ratamess, N. A., et al. (2002) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200211000-00023 · Cited by 109
van Someren, K. A., Edwards, A., & Howatson, G. (2005) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.15.4.413 · Cited by 109
“Creatine kinase activity in blood, which is a commonly used marker of sarcolemmal damage (4, 19, 23), has also been shown to be reduced by HMB supplementation following resistance training (9, 13, 20, 25) and prolonged running (14).”
BackgroundShort-Term Immobilization after Eccentric Exercise. Part II: Creatine Kinase and Myoglobin
Sayers, S. P., & Clarkson, P. M. (2003) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000064933.43824.ed · Cited by 108
Self-citationSuski, C. D., Killen, S. S., Morrissey, M. B., et al. (2003) · North American Journal of Fisheries Management · doi:10.1577/m02-042 · Cited by 106
“activity in largemouth bass following tournaments was much less than that which has been shown to occur in other species following severe disturbances (Powell et al. 1974; Clarkson et al. 1992).”
BackgroundChen, T. C. (2003) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0791-1 · Cited by 107
“, strength, range of motion (ROM), muscle soreness, swelling, and circulating levels of muscle proteins] following subsequent bouts of the same eccentric exercise (Newham et al. 1987; Clarkson and Tremblay 1988; Clarkson et al. 1992; Nosaka and Clarkson 1995; Nosaka and Newton 2002).”
BackgroundResultInfluentialDAWSON, B., VLADICH, T., & BLANKSBY, B. A. (2002) · Journal of Strength and Conditioning Research · doi:10.1519/00124278-200211000-00001 · Cited by 41
Self-citationApoptosis of myofibres and satellite cells: exercise‐induced damage in skeletal muscle of the mouse
Podhorska‐Okolow, Sandri, Zampieri, Brun, Rossini, & Carraro, U. (1998) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.1998.00149.x · Cited by 103
Easthope, C. A., Hausswirth, C., Louis, J. B., Lepers, R., Vercruyssen, F., & Brisswalter, J. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1597-1 · Cited by 121
“Intracellular enzymes such CK and LDH indicate that the muscle injury arises from myofibrillar disruption (Clarkson et al. 1992; Noakes 1987), and are classically used to assess the loss of sarcolemmal integrity after strenuous exercices (Overgaard et al.”
BackgroundSkeletal Muscle Damage with Exercise and Aging
Close, G. L., Kayani, A. C., Vasilaki, A., & McArdle, A. (2005) · Sports Medicine · doi:10.2165/00007256-200535050-00004 · Cited by 104
Child, R. B., Saxton, J., & Donnelly, A. (1998) · Journal of Sports Sciences · doi:10.1080/02640419808559358 · Cited by 103
Lavender, A. P., & Nosaka, K. (2007) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2007.03.005 · Cited by 104
Self-citationChanges in running economy at different intensities following downhill running
Chen, T. C., Nosaka, K., Lin, M.-J., et al. (2009) · Journal of Sports Sciences · doi:10.1080/02640410903062027 · Cited by 102
“Exercise-induced muscle damage is characterized by a prolonged decrease in muscle strength, delayed-onset muscle soreness, and increases in muscle proteins such as creatine kinase (Clarkson, Nosaka & Braun, 1992 ).”
BackgroundSelf-citationProtective role of α-actinin-3 in the response to an acute eccentric exercise bout
Vincent, B., Windelinckx, A., Nielens, H., et al. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01007.2009 · Cited by 102
Changes in the angle-force curve of human elbow flexors following eccentric and isometric exercise
Philippou, Α., Bogdanis, G. C., Nevill, A. M., & Maridaki, M. D. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-004-1209-z · Cited by 102
“During the preliminary measurements (day 0), muscle shortening ability and spontaneous muscle shortening were evaluated first by measuring flexed (FANG) and relaxed (RANG) elbow angle, respectively (Clarkson et al. 1992).”
BackgroundMethodResultInfluentialDeterminants of Olympic Fencing Performance and Implications for Strength and Conditioning Training
Turner, A. P., James, N., Dimitriou, L., Greenhalgh, A., Moody, J. A., Fulcher, D., Mias, E., & Kilduff, L. P. (2014) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000000478 · Cited by 113
Cooke, M. B., Rybalka, E., Stathis, C. G., Cribb, P. J., & Hayes, A. (2010) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-7-30 · Cited by 101
“Although CK is used as an indirect marker of muscle damage, there is a larger inter- and intraparticipant variability in the CK response after exercise because blood concentrations reflect what is being released from damaged tissue as well as what is taken up by the reticuloendothelial system [39,40].”
BackgroundTartibian, B., Maleki, B. H., & Abbasi, A. (2011) · Clinical Journal of Sport Medicine · doi:10.1097/jsm.0b013e31820f8c2f · Cited by 99
Effects of Flexibility Training on Eccentric Exercise-Induced Muscle Damage
Chen, C., Nosaka, K., Chen, H.-L., Lin, M.-J., Tseng, K., & Chen, T. C. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181f315ad · Cited by 97
“This type of muscle adaptation is often called the repeated bout effect (7,8,33,37).”
BackgroundInfluentialSelf-citationHesselink, M. K. C., Kuipers, H., Geurten, P., & van Straaten, H. W. M. (1996) · Journal of Muscle Research and Cell Motility · doi:10.1007/bf00240930 · Cited by 97
“Eccentric exercise has previously been shown to induce decreased muscle strength in animal models as well (McCully & Faulkner, 1985; Lieber & Friden, 1993) as in humans (Clarkson et al., 1992; Cleak & Eston, 1992; Rodenburg et al., 1993).”
Do Small Heat Shock Proteins Protect Skeletal Muscle from Injury?
Koh, T. J. (2002) · Exercise and Sport Sciences Reviews · doi:10.1097/00003677-200207000-00005 · Cited by 96
“Fortunately, exercise training can protect skeletal muscle from eccentric-contraction–induced injury (3).”
BackgroundRussell, M. A., Sparkes, W., Northeast, J., Cook, C. J., Bracken, R. M., & Kilduff, L. P. (2015) · Human Movement Science · doi:10.1016/j.humov.2015.11.011 · Cited by 100
Are women less susceptible to exercise-induced muscle damage?
Clarkson, P. M., & Hubal, M. J. (2001) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200111000-00011 · Cited by 93
Self-citationSaxton, J., Donnelly, A., & Roper, H. (1994) · European Journal of Applied Physiology · doi:10.1007/bf00376765 · Cited by 94
“The delayed release of CK into the blood following maximum voluntary eccentric work was consistent with previous studies (Clarkson et al. 1992).”
ResultRaeder, C., Wiewelhove, T., Símola, R. Á. D. P., Kellmann, M., Meyer, T., Pfeiffer, M., & Ferrauti, A. (2016) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000001427 · Cited by 93
“A single bout of high-intensity muscle action results in decreased neuromuscular performance in addition to increased muscle damage and discomfort lasting for many days, especially when eccentric overload strategies are used (3,5,10,11).”
BackgroundResultBiochemical and Hormonal Responses during an Intercollegiate Football Season
Hoffman, J. R., Kang, J., Ratamess, N. A., et al. (2005) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000170068.97498.26 · Cited by 93
Gibala, M. J., Interisano, S. A., Tarnopolsky, M. A., Roy, B. D., MacDonald, J. R., Yarasheski, K. E., & MacDougall, J. D. (2000) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y00-036 · Cited by 98
“…1989) and that even a single bout of resistance exercise can exert a protective effect on the muscle, such that strength loss, muscle soreness, and muscle-specific enzyme release are markedly attenuated following a subsequent exercise bout (Ebbeling and Clarkson 1990; Clarkson et al. 1992).”
BackgroundResultInfluentialNeuromuscular Damage and Repair after Dry Needling in Mice
Domingo, A., del Moral, O. M., Monterde, S., et al. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/260806 · Cited by 92
“However, in the newly regenerated area, some inflammatory cells persist for some time [29].”
BackgroundMagal, M., Dumke, C. L., Urbiztondo, Z. G., Cavill, M. J., Triplett, N. T., Quindry, J. C., McBride, J. M., & Epstein, Y. (2010) · Journal of Sports Sciences · doi:10.1080/02640410903440892 · Cited by 90
“, 2003), peak values of enzymatic damage markers in the present investigation were substantially lower than those in studies that used eccentric contractions of the elbow flexors (Clarkson et al., 1992; Nosaka & Clarkson, 1996).”
ResultStatin myopathy: Incidence, risk factors, and pathophysiology
Sewright, K. A., Clarkson, P. M., & Thompson, P. D. (2007) · Current Atherosclerosis Reports · doi:10.1007/s11883-007-0050-3 · Cited by 90
“In addition, physicians should appreciate that the increases in CK levels with eccentric exercise, in which the muscle is forced to contract while being stretched, can produce remarkable increases in CK levels [ 41 ].”
BackgroundSelf-citationTsuchiya, Y., Yanagimoto, K., Nakazato, K., Hayamizu, K., & Ochi, E. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-016-3373-3 · Cited by 97
“Serum Mb and CK are known markers that indicate large differences in individuals (Clarkson et al. 1992).”
BackgroundInfluentialAttenuation of Eccentric Exercise–Induced Muscle Damage by Preconditioning Exercises
Chen, T. C., Chen, H.-L., Pearce, A. J., & Nosaka, K. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31825f69f3 · Cited by 91
Self-citationProlonged recovery and reduced adaptation in aged rat muscle following eccentric exercise
McBride, T. A., Gorin, F. A., & Carlsen, R. C. (1995) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(95)01629-e · Cited by 89
Effect of Vibration Treatment on Symptoms Associated with Eccentric Exercise-Induced Muscle Damage
Lau, W. Y., & Nosaka, K. (2011) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e3182063ac8 · Cited by 89
“Other symptoms include a prolonged impairment of muscle function and swelling, persisting for several days after exercise.(4,5) These symptoms affect daily activities and athletic performance; therefore, interventions to reduce the symptoms and enhance recovery from muscle damage are necessary.”
BackgroundSelf-citationTime Course of Strength and Echo Intensity Recovery After Resistance Exercise in Women
Radaelli, R., Bottaro, M., Wilhelm, E. N., Wagner, D. R., & Pinto, R. S. (2011) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31823dae96 · Cited by 90
“increases in levels of blood creatine kinase and potassium (11,22).”
BackgroundAre similar inflammatory factors involved in strenuous exercise and sepsis?
Camus, G., Deby-Dupont, G. P., Duchateau, J., Deby, C. M. T., Pincemail, J., & Lamy, M. (1994) · Intensive Care Medicine · doi:10.1007/bf01705731 · Cited by 86
“Under comparable work loads, eccentric contractions produce higher tension on the muscle fibres than concentric contractions [27, 28 ].”
BackgroundInfluentialTanabe, Y., Chino, K., Ohnishi, T., Ozawa, H., Sagayama, H., Maeda, S., & Takahashi, H. (2018) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13373 · Cited by 88
Effects of eccentric treadmill exercise on inflammatory gene expression in human skeletal muscle
Buford, T. W., Cooke, M. B., Shelmadine, B., Hudson, G. M., Redd, L., & Willoughby, D. S. (2009) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-067 · Cited by 91
“These events lead to decreases in muscle force production and delayed-onset muscle soreness that typically peak 2–3 days following the muscle injury (Clarkson et al. 1992; Ebbeling and Clarkson.”
InfluentialLynch, G. S., Fary, C., & Williams, D. A. (1997) · Cell Calcium · doi:10.1016/s0143-4160(97)90022-1 · Cited by 87
Saxton, J., & Donnelly, A. (1996) · Clinical Science · doi:10.1042/cs0900119 · Cited by 88
Adaptation to eccentric exercise: effect on CD64 and CD11b/CD18 expression
Pizza, F. X., Davis, B. H., Henrickson, S. D., Mitchell, J. B., Pace, J. F., Bigelow, N. C., DiLauro, P. C., & Naglieri, T. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.1.47 · Cited by 88
Baker, J., Bailey, D., Hullin, D. A., et al. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-004-1090-9 · Cited by 87
“Exercise-induced muscle damage has been widely reported following different types of eccentric exercise in humans (Balnave and Thompson 1993; Cerny et al. 1983; Clarkson et al. 1993 ).”
BackgroundAdverse events associated with eccentric exercise protocols: six case studies
Sayers, S. P., Clarkson, P. M., ROUZIER, P. A., & Kamen, G. (1999) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199912000-00002 · Cited by 85
Self-citationMeasuring changes in muscle stiffness after eccentric exercise using elastography
Green, M. A., Sinkus, R., Gandevia, S. C., Herbert, R., & Bilston, L. E. (2012) · NMR in Biomedicine · doi:10.1002/nbm.1801 · Cited by 84
Exercise-induced muscle damage and the repeated bout effect: evidence for cross transfer
Starbuck, C., & Eston, R. G. (2011) · European Journal of Applied Physiology · doi:10.1007/s00421-011-2053-6 · Cited by 84
“The symptoms include an increase in muscle soreness (Jones et al. 1987; Armstrong et al. 1991; Nosaka and Newton 2002), increase in plasma creatine kinase (CK; Nosaka and Clarkson 1995; Byrne et al. 2001; Byrne and Eston 2002a, b), strength loss (Cleak and Eston 1992; Clarkson et al. 1992; Byrne et al. 2001; Byrne and…”
BackgroundThe effect of eccentric exercise on position sense and joint reaction angle of the lower limbs
Paschalis, V., Nikolaidis, M. G., Giakas, G., et al. (2007) · Muscle & Nerve · doi:10.1002/mus.20723 · Cited by 84
Hormonal responses during a prolonged military field exercise with variable exercise intensity
Kyröläinen, H., Karinkanta, J., Santtila, M., Koski, H., Mäntysaari, M., & Pullinen, T. (2007) · European Journal of Applied Physiology · doi:10.1007/s00421-007-0619-0 · Cited by 84
“This so-called repeated bout eVect can last for several months (Clarkson et al. 1992; McHugh et al. 1999; McHugh 2003) In addition to these explanations, increased clearance of CK as an adaptation to continued exercise might explain the decreasing CK during the latter part of the training course in…”
BackgroundThe effects of muscle damage following eccentric exercise on gait biomechanics
Paschalis, V., Giakas, G., Baltzopoulos, V., et al. (2006) · Gait & Posture · doi:10.1016/j.gaitpost.2006.04.002 · Cited by 84
Tauler, P., Sureda, A., Cases, N., Aguiló, A., Marroyo, J. A. R., Villa, G., Tur, J. A., & Pons, A. (2005) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2005.10.013 · Cited by 84
High plasma creatine kinase: review of the literature and proposal for a diagnostic algorithm
Morandi, L. O., Angelini, C. I., Prelle, A. C., Pini, A., Grassi, B., Bernardi, G., Politano, L., Bruno, C., Grandis, D. D., Cudia, P., et al. (2006) · Neurological Sciences · doi:10.1007/s10072-006-0701-0 · Cited by 82
“[24] compared CK levels after eccentric exercise in trained and in sedentary students.”
BackgroundRahimi, M. H., Shab-Bidar, S., Mollahosseini, M., & Djafarian, K. (2017) · Nutrition · doi:10.1016/j.nut.2017.05.005 · Cited by 81
Effects of prior concentric training on eccentric exercise induced muscle damage
Gleeson, N., Eston, R. G., Marginson, V., & McHugh, M. P. (2003) · British Journal of Sports Medicine · doi:10.1136/bjsm.37.2.119 · Cited by 81
Sonobe, T., Inagaki, T., Poole, D. C., & Kano, Y. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00815.2007 · Cited by 80
“It is well known that eccentric (ECC) contractions induce muscle damage (8, 26, 44), and it has been suggested that one principal cause of that damage is high [Ca]i (1, 17).”
BackgroundSEMARK, A., Noakes, T. D., Gibson, A. S. C., et al. (1999) · Journal of Sports Sciences · doi:10.1080/026404199366091 · Cited by 80
Itoh, K., Okada, K., & Kawakita, K. (2004) · Acupuncture in Medicine · doi:10.1136/aim.22.1.2 · Cited by 80
Sex Differences in Exercise-Induced Muscle Pain and Muscle Damage
Dannecker, E. A., Liu, Y., Rector, R. S., Thomas, T. R., Fillingim, R. B., & Robinson, M. E. (2012) · Journal of Pain · doi:10.1016/j.jpain.2012.09.014 · Cited by 78
Responses of human elbow flexor muscles to electrically stimulated forced lengthening exercise
Nosaka, K., NEWTON, M., & Sacco, P. (2002) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2002.00936.x · Cited by 79
Self-citationNeuromuscular disturbance outlasts other symptoms of exercise-induced muscle damage
Deschenes, M. R., Brewer, R. E., Bush, J. A., McCoy, R. W., Volek, J. S., & Kraemer, W. J. (2000) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(00)00258-6 · Cited by 76
Dousset, E., Avela, J., Ishikawa, M., Kallio, J., Kuitunen, S., Kyröläinen, H., Linnamo, V., & Komi, P. V. (2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31802dd74e · Cited by 78
“The first stage is characterized by increased muscle stiffness (7), altered force and position sense (6), swelling (9), and muscle structure damage (13), Address for correspondence: Erick Dousset, Ph.”
BackgroundCORP: Measurement of upper and lower limb muscle strength and voluntary activation
Nuzzo, J. L., Taylor, J. L., & Gandevia, S. C. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00569.2018 · Cited by 77
Factors involved in strain-induced injury in skeletal muscles and outcomes of prolonged exposures
Stauber, W. T. (2003) · Journal of Electromyography and Kinesiology · doi:10.1016/j.jelekin.2003.09.010 · Cited by 77
“training effect) [13,22].”
BackgroundFunctional Polymorphisms Associated with Human Muscle Size and Strength
Thompson, P. D., Moyna, N. M., Seip, R. L., Price, T. B., Clarkson, P. M., Angelopoulos, T. J., Gordon, P. M., Pescatello, L. S., Visich, P. S., Zoeller, R. F., et al. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000132274.26612.23 · Cited by 77
Self-citationKano, Y., Padilla, D. J., Behnke, B. J., et al. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00069.2005 · Cited by 77
Early assessment of exercise induced skeletal muscle injury using plasma fatty acid binding protein.
Sorichter, S., Mair, J. M., Koller, A., et al. (1998) · British Journal of Sports Medicine · doi:10.1136/bjsm.32.2.121 · Cited by 77
Potent Protective Effect Conferred by Four Bouts of Low-Intensity Eccentric Exercise
Chen, T. C., Chen, H.-L., Lin, M.-J., Wu, C.-J., & Nosaka, K. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181c0a818 · Cited by 75
Self-citationPlyometric Exercise Increases Serum Indices of Muscle Damage and Collagen Breakdown
Tofas, T., Jamurtas, A. Z., Fatouros, I. G., Nikolaidis, M. G., Koutedakis, Y., Sinouris, E. A., Papageorgakopoulou, N., & Theocharis, D. A. (2008) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31816605a0 · Cited by 77
“Eccentric contractions induce long-lasting decreases in muscle force generation and range of motion (ROM), muscle swelling, and soreness, as well as increased levels of muscle damage indices in the blood (7,14,20).”
BackgroundHeavens, K. R., Szivak, T., Hooper, D., Dunn-Lewis, C., Comstock, B. A., Flanagan, S. D., Looney, D. P., Kupchak, B., Maresh, C., Volek, J., et al. (2014) · Journal of Strength and Conditioning Research · doi:10.1097/jsc.0000000000000236 · Cited by 73
“Damage to muscle fibers can occur during intense exercise bouts, which can include the disruption of the sarcolemma, swelling or disruption of the sarcotubular system, distortion of the contractile components of myofibrils, cytoskeletal damage, extracellular matrix changes, and release of cellular proteins (5,6).”
BackgroundRighi, N. C., Schuch, F. B., Nardi, A. T. D., Pippi, C. M., Righi, G. D. A., Puntel, G. O., da Silva, A. M. V., & Signori, L. U. (2020) · European Journal of Nutrition · doi:10.1007/s00394-020-02215-2 · Cited by 82
“Such damage is shown, among other forms, by the presence of intramuscular enzymes, mainly CK, in the blood plasma [55, 56], which shows the peak of its activity 24 h after the exercises [57].”
BackgroundNosaka, K., Muthalib, M., Lavender, A. P., & Laursen, P. B. (2006) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0331-5 · Cited by 75
“These symptoms are attenuated however when the same eccentric exercise is performed several weeks beforehand ( Clarkson et al. 1992; Nosaka et al. 2005).”
BackgroundMethodResultInfluentialSelf-citationAsymptomatic/pauci‐symptomatic creatine kinase elevations (hyperckemia)
Silvestri, N. J., & Wolfe, G. I. (2012) · Muscle & Nerve · doi:10.1002/mus.23755 · Cited by 74
“CK levels may ascend as high as 30 times the ULN within 24 hours of activity; levels slowly decline over the course of 7–10 days.(35,36) The degree of CK”
BackgroundElectromyographic analysis of exercise resulting in symptoms of muscle damage
McHugh, M. P., Connolly, D., Eston, R. G., et al. (2000) · Journal of Sports Sciences · doi:10.1080/026404100365063 · Cited by 75
“, 1996) or voluntary exercise in humans (FridŠn et al., 1983; FridŠn, 1984; Clarkson et al., 1992) have consistently demonstrated that untrained skeletal muscle is susceptible to damage by eccentric contractions.”
BackgroundACE ID genotype affects blood creatine kinase response to eccentric exercise
Yamin, C., Amir, O., Sagiv, M., Attias, E., Meckel, Y., Eynon, N., Sagiv, M. S., & Amir, R. E. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00867.2007 · Cited by 75
“Eccentric (muscle lengthening) exercise-induced rhabdomyolysis has been well described ( 9 , 14).”
BackgroundFatigue and Recovery in Soccer: Evidence and Challenges
Marqués-Jiménez, D., Calleja-González, J., Arratibel-Imaz, I., Delextrat, A. A., & Terrados, N. (2017) · The Open Sports Sciences Journal · doi:10.2174/1875399x01710010052 · Cited by 98
Metadata
- Authors
- CLARKSON, P. M., NOSAKA, K., & BRAUN, B.
- Affiliations
- University of Massachusetts Amherst (US)
- Venue
- Medicine & Science in Sports & Exercise
- Published
- 1992-05
- Volume
- 24
- Issue
- 5
- Pages
- 512???520
- ISSN
- 0195-9131 (ISSN-L)
- OpenAlex
- W2093625864
- Cited by
- 970
- References
- 0
- Citations by year
- 2026: 10 · 2025: 21 · 2024: 25 · 2023: 18 · 2022: 34 · 2021: 35 · 2020: 28 · 2019: 38 · 2018: 32 · 2017: 43 · 2016: 33 · 2015: 41 · 2014: 38 · 2013: 49 · 2012: 45
- FWCI
- 13.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Medicine & Science in Sports & Exercise (publishedVersion)
- PubMed (publishedVersion)
- ScholarWorks@UMassAmherst (University of Massachusetts Amherst) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Keywords
- exercise-induced muscle damage, eccentric exercise, forearm flexor muscles, muscle soreness, muscle swelling, maximal strength, creatine kinase, muscle shortening, recovery time course, neuromuscular factors
- MeSH terms
- Adaptation, Physiological, Creatine Kinase, Humans, Movement, Muscle Contraction, Muscles, Tensile Strength, Time Factors, Exercise
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