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The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis (2018)

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  • USP affiliated authors: UGRINOWITSCH, CARLOS - EEFE
  • USP Schools: EEFE
  • DOI: 10.1007%2Fs00421-017-3792-9
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  • Language: Inglês
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    Informações sobre o DOI: 10.1007%2Fs00421-017-3792-9 (Fonte: oaDOI API)
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    Título do periódico: European Journal of Applied Physiology

    ISSN: 1439-6319,1439-6327

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  • Título: European Journal of Applied Physiology

    ISSN: 1439-6319

    Citescore - 2017: 2.45

    SJR - 2017: 1.186

    SNIP - 2017: 1.215

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    • ABNT

      DAMAS, Felipe; LIBARDI, Cleiton A; UGRINOWITSCH, Carlos. The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis. European Journal of Applied Physiology, Berlin, v. 118, n. 3, p. 485-500, 2018. Disponível em: < > DOI: 10.1007%2Fs00421-017-3792-9.
    • APA

      Damas, F., Libardi, C. A., & Ugrinowitsch, C. (2018). The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis. European Journal of Applied Physiology, 118( 3), 485-500. doi:10.1007%2Fs00421-017-3792-9
    • NLM

      Damas F, Libardi CA, Ugrinowitsch C. The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis [Internet]. European Journal of Applied Physiology. 2018 ; 118( 3): 485-500.Available from:
    • Vancouver

      Damas F, Libardi CA, Ugrinowitsch C. The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis [Internet]. European Journal of Applied Physiology. 2018 ; 118( 3): 485-500.Available from:

    Referências citadas na obra
    Abraham WM (1977) Factors in delayed muscle soreness. Med Sci Sports 9:11–20
    Ackley BJ, Swan BA, Ladwig G, Tucker S (2008) Evidence-based nursing care guidelines: medical-surgical interventions. Mosby Elsevier, St. Louis
    Ahtiainen JP, Pakarinen A, Kraemer WJ, Hakkinen K (2003) Acute hormonal and neuromuscular responses and recovery to forced vs maximum repetitions multiple resistance exercises. Int J Sports Med 24:410–418.
    Ahtiainen JP, Pakarinen A, Alen M, Kraemer WJ, Hakkinen K (2005) Short vs. long rest period between the sets in hypertrophic resistance training: influence on muscle strength, size, and hormonal adaptations in trained men. J Strength Cond Res 19:572–582
    Ahtiainen JP, Hoffren M, Hulmi JJ, Pietikainen M, Mero AA, Avela J, Hakkinen K (2010) Panoramic ultrasonography is a valid method to measure changes in skeletal muscle cross-sectional area. Eur J Appl Physiol 108:273–279.
    Alexakis C, Partridge T, Bou-Gharios G (2007) Implication of the satellite cell in dystrophic muscle fibrosis: a self-perpetuating mechanism of collagen overproduction. Am J Physiol Cell Physiol 293:C661–C669.
    Andersen LL, Andersen JL, Suetta C, Kjaer M, Sogaard K, Sjogaard G (2009) Effect of contrasting physical exercise interventions on rapid force capacity of chronically painful muscles. J Appl Physiol (1985) 107:1413–1419.
    Arts IM et al (2012) Intramuscular fibrous tissue determines muscle echo intensity in amyotrophic lateral sclerosis. Muscle Nerve 45:449–450.
    Aschenbach WG, Sakamoto K, Goodyear LJ (2004) 5′ adenosine monophosphate-activated protein kinase, metabolism and exercise. Sports Med 34:91–103
    Atherton PJ, Smith K (2012) Muscle protein synthesis in response to nutrition and exercise. J Physiol 590:1049–1057.
    Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H (2005) Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19:786–788.
    Bamman MM, Roberts BM, Adams GR (2017) Molecular regulation of exercise-induced muscle fiber hypertrophy. Cold Spring Harb Perspect Med.
    Beaton LJ, Tarnopolsky MA, Phillips SM (2002a) Contraction-induced muscle damage in humans following calcium channel blocker administration. J Physiol 544:849–859 pii]
    Beaton LJ, Tarnopolsky MA, Phillips SM (2002b) Variability in estimating eccentric contraction-induced muscle damage and inflammation in humans. Can J Appl Physiol 27:516–526
    Bellamy LM et al (2014) The acute satellite cell response and skeletal muscle hypertrophy following resistance training. PLoS One 9:e109739.
    Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR (1995) Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 268:E514–E520
    Biolo G, Tipton KD, Klein S, Wolfe RR (1997) An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 273:E122–E129
    Blazevich AJ, Cannavan D, Coleman DR, Horne S (2007) Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol (1985) 103:1565–1575.
    Bodine SC (2006) mTOR signaling and the molecular adaptation to resistance exercise. Med Sci Sports Exerc 38:1950–1957.
    Bolster DR, Crozier SJ, Kimball SR, Jefferson LS (2002) AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277:23977–23980.
    Brandenburg JP, Docherty D (2002) The effects of accentuated eccentric loading on strength, muscle hypertrophy, and neural adaptations in trained individuals. J Strength Cond Res 16:25–32
    Brook MS et al (2015) Skeletal muscle hypertrophy adaptations predominate in the early stages of resistance exercise training, matching deuterium oxide-derived measures of muscle protein synthesis and mechanistic target of rapamycin complex 1 signaling. FASEB J 29:4485–4496.
    Buckner SL et al (2017) Differentiating swelling and hypertrophy through indirect assessment of muscle damage in untrained men following repeated bouts of resistance exercise. Eur J Appl Physiol 117:213–224.
    Butterfield TA (2010) Eccentric exercise in vivo: strain-induced muscle damage and adaptation in a stable system. Exerc Sport Sci Rev 38:51–60.
    Cao Y, Zhao Z, Gruszczynska-Biegala J, Zolkiewska A (2003) Role of metalloprotease disintegrin ADAM12 in determination of quiescent reserve cells during myogenic differentiation in vitro. Mol Cell Biol 23:6725–6738
    Chapman DW, Newton MJ, McGuigan MR, Nosaka K (2011) Effect of slow-velocity lengthening contractions on muscle damage induced by fast-velocity lengthening contractions. J Strength Cond Res 25:211–219.
    Cheek DB (1985) The control of cell mass and replication. The DNA unit—a personal 20-year study. Early Hum Dev 12:211–239
    Chen TC, Nosaka K (2006) Responses of elbow flexors to two strenuous eccentric exercise bouts separated by three days. J Strength Cond Res 20:108–116.
    Chen TC, Chen HL, Lin MJ, Wu CJ, Nosaka K (2009) Muscle damage responses of the elbow flexors to four maximal eccentric exercise bouts performed every 4 weeks. Eur J Appl Physiol 106:267–275.
    Chen HL, Nosaka K, Pearce AJ, Chen TC (2012a) Two maximal isometric contractions attenuate the magnitude of eccentric exercise-induced muscle damage. Appl Physiol Nutr Metab 37:680–689.
    Chen TC, Chen HL, Pearce AJ, Nosaka K (2012b) Attenuation of eccentric exercise-induced muscle damage by preconditioning exercises. Med Sci Sports Exerc 44:2090–2098.
    Chen TC, Chen HL, Lin MJ, Chen CH, Pearce AJ, Nosaka K (2013) Effect of two maximal isometric contractions on eccentric exercise-induced muscle damage of the elbow flexors. Eur J Appl Physiol 113:1545–1554.
    Clarkson PM, Hubal MJ (2002) Exercise-induced muscle damage in humans. Am J Phys Med Rehabil 81:S52–S69.
    Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, Hawley JA (2006) Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J 20:190–192.
    Conceicao MS et al (2012) Effects of eccentric exercise on systemic concentrations of pro- and anti-inflammatory cytokines and prostaglandin (E2): comparison between young and postmenopausal women. Eur J Appl Physiol 112:3205–3213.
    Counts BR, Buckner SL, Mouser JG, Dankel SJ, Jessee MB, Mattocks KT, Loenneke JP (2017) Muscle growth: to infinity and beyond? Muscle Nerve.
    Cramer JT, Palmer IJ, Ryan ED, Herda TJ, Bemben DA, Bemben MG, Stratemeier PH (2007) Validity and reliability of a peripheral quantitative computed tomography scanner for measuring muscle cross-sectional area. Annual Meeting of the American College of Sports Medicine, Medicine and Science in Sports and Exercise 39(Supplement), New Orleans
    Damas F, Phillips S, Vechin FC, Ugrinowitsch C (2015) A review of resistance training-induced changes in skeletal muscle protein synthesis and their contribution to hypertrophy. Sports Med 45:801–807.
    Damas F, Nosaka K, Libardi CA, Chen TC, Ugrinowitsch C (2016a) Susceptibility to exercise-induced muscle damage: a cluster analysis with a large sample. Int J Sports Med 37:633–640.
    Damas F et al (2016b) Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J Physiol 594:5209–5222.
    Damas F et al (2016c) Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling. Eur J Appl Physiol 116:49–56.
    Damas F et al (2016d) An inability to distinguish edematous swelling from true hypertrophy still prevents a completely accurate interpretation of the time course of muscle hypertrophy. Eur J Appl Physiol 116:445–446.
    Damas F et al (under review) Early- and later-phases satellite cell responses and myonuclear content with resistance training in young men
    DeFreitas JM, Beck TW, Stock MS, Dillon MA, Kasishke PR 2nd (2011) An examination of the time course of training-induced skeletal muscle hypertrophy. Eur J Appl Physiol 111:2785–2790.
    DeFreitas JM, Beck TW, Stock MS (2016) The findings of Damas et al. have not influenced the previously proposed time course of skeletal muscle hypertrophy. Eur J Appl Physiol 116:443–444.
    Doma K, Leicht A, Sinclair W, Schumann M, Damas F, Burt D, Woods C (2017) The impact of exercise-induced muscle damage on performance test outcomes in elite female basketball players. J Strength Cond Res.
    Douglas J, Pearson S, Ross A, McGuigan M (2017) Chronic adaptations to eccentric training: a systematic review. Sports Med 47:917–941.
    Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB (2006) Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol 576:613–624.
    Egner IM, Bruusgaard JC, Gundersen K (2016) Satellite cell depletion prevents fiber hypertrophy in skeletal muscle. Development 143:2898–2906.
    Eriksson A, Lindstrom M, Carlsson L, Thornell LE (2006) Hypertrophic muscle fibers with fissures in power-lifters; fiber splitting or defect regeneration? Histochem Cell Biol 126:409–417.
    Farthing JP, Chilibeck PD (2003) The effects of eccentric and concentric training at different velocities on muscle hypertrophy. Eur J Appl Physiol 89:578–586.
    Farup J, Rahbek SK, Riis S, Vendelbo MH, Paoli F, Vissing K (2014a) Influence of exercise contraction mode and protein supplementation on human skeletal muscle satellite cell content and muscle fiber growth. J Appl Physiol (1985) 117:898–909.
    Farup J et al (2014b) Whey protein hydrolysate augments tendon and muscle hypertrophy independent of resistance exercise contraction mode. Scand J Med Sci Sports 24:788–798.
    Faulkner JA, Opiteck JA, Brooks SV (1992) Injury to skeletal muscle during altitude training: induction and prevention. Int J Sports Med 13 Suppl 1:S160–S162.
    Flann KL, LaStayo PC, McClain DA, Hazel M, Lindstedt SL (2011) Muscle damage and muscle remodeling: no pain, no gain? J Exp Biol 214:674–679.
    Foley JM, Jayaraman RC, Prior BM, Pivarnik JM, Meyer RA (1999) MR measurements of muscle damage and adaptation after eccentric exercise. J Appl Physiol (1985) 87:2311–2318
    Folland JP, Williams AG (2007) The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med 37:145–168
    Folland JP, Chong J, Copeman EM, Jones DA (2001) Acute muscle damage as a stimulus for training-induced gains in strength. Med Sci Sports Exerc 33:1200–1205
    Gibala MJ, MacDougall JD, Tarnopolsky MA, Stauber WT, Elorriaga A (1995) Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J Appl Physiol (1985) 78:702–708
    Gibala MJ, Interisano SA, Tarnopolsky MA, Roy BD, MacDonald JR, Yarasheski KE, MacDougall JD (2000) Myofibrillar disruption following acute concentric and eccentric resistance exercise in strength-trained men. Can J Physiol Pharmacol 78:656–661
    Glynn EL, Fry CS, Drummond MJ, Dreyer HC, Dhanani S, Volpi E, Rasmussen BB (2010) Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. Am J Physiol Regul Integr Comp Physiol 299:R533–R540.
    Gonzalez-Izal M, Lusa Cadore E, Izquierdo M (2014) Muscle conduction velocity, surface electromyography variables, and echo intensity during concentric and eccentric fatigue. Muscle Nerve 49:389–397
    Goreham C, Green HJ, Ball-Burnett M, Ranney D (1999) High-resistance training and muscle metabolism during prolonged exercise. Am J Physiol 276:E489–E496
    Green H, Goreham C, Ouyang J, Ball-Burnett M, Ranney D (1999) Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol 276:R591–R596
    Greenhaff PL et al (2008) Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am J Physiol Endocrinol Metab 295:E595–E604.
    Guerin CW, Holland PC (1995) Synthesis and secretion of matrix-degrading metalloproteases by human skeletal muscle satellite cells. Dev Dyn 202:91–99.
    Halkjaer-Kristensen J, Ingemann-Hansen T (1981) Variations in single fibre areas and fibre composition in needle biopsies from the human quadriceps muscle. Scand J Clin Lab Invest 41:391–395
    Hess DR (2004) What is evidence-based medicine and why should I care? Respir Care 49:730–741
    Hill JC, Millan IS (2014) Validation of musculoskeletal ultrasound to assess and quantify muscle glycogen content. A novel approach. Phys Sportsmed 42:45–52.
    Hortobagyi T, Hill JP, Houmard JA, Fraser DD, Lambert NJ, Israel RG (1996) Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol (1985) 80:765–772
    Hough T (1900) Ergographic studies in muscular fatigue and soreness. J Boston Soc Med Sci 5:81–92
    Hyldahl RD, Hubal MJ (2014) Lengthening our perspective: morphological, cellular, and molecular responses to eccentric exercise. Muscle Nerve 49:155–170.
    Hyldahl RD, Olson T, Welling T, Groscost L, Parcell AC (2014) Satellite cell activity is differentially affected by contraction mode in human muscle following a work-matched bout of exercise. Front Physiol 5:485.
    Hyldahl RD et al (2015) Extracellular matrix remodeling and its contribution to protective adaptation following lengthening contractions in human muscle. FASEB J 29:2894–2904.
    Jenkins ND et al (2016) Neuromuscular adaptations after 2 and 4 weeks of 80% versus 30% 1 repetition maximum resistance training to failure. J Strength Cond Res 30:2174–2185.
    Jenkins NDM, Miramonti AA, Hill EC, Smith CM, Cochrane-Snyman KC, Housh TJ, Cramer JT (2017) Greater neural adaptations following high- vs. low-load resistance training. Front Physiol 8:331.
    Kadi F, Schjerling P, Andersen LL, Charifi N, Madsen JL, Christensen LR, Andersen JL (2004) The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J Physiol 558:1005–1012.
    Kamen G, Knight CA (2004) Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol A Biol Sci Med Sci 59:1334–1338
    Keefe G, Wright C (2016) An intricate balance of muscle damage and protein synthesis: the key players in skeletal muscle hypertrophy following resistance training. J Physiol 594:7157–7158.
    Kim PL, Staron RS, Phillips SM (2005) Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. J Physiol 568:283–290.
    Kumar V, Atherton P, Smith K, Rennie MJ (2009) Human muscle protein synthesis and breakdown during and after exercise. J Appl Physiol (1985) 106:2026–2039.
    Lauritzen F, Paulsen G, Raastad T, Bergersen LH, Owe SG (2009) Gross ultrastructural changes and necrotic fiber segments in elbow flexor muscles after maximal voluntary eccentric action in humans. J Appl Physiol (1985) 107:1923–1934.
    Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646.
    Levels of Evidence (2009) Oxford Centre for Evidence-Based Medicine. . Accessed Mar 2009
    Lixandrao ME et al (2014) Vastus lateralis muscle cross-sectional area ultrasonography validity for image fitting in humans. J Strength Cond Res 28:3293–3297.
    Lixandrao ME et al (2016) Time course of resistance training-induced muscle hypertrophy in the elderly. J Strength Cond Res 30:159–163.
    Loenneke JP, Rossow LM, Fahs CA, Thiebaud RS, Grant Mouser J, Bemben MG (2017) Time-course of muscle growth, and its relationship with muscle strength in both young and older women. Geriatr Gerontol Int.
    Mackey AL, Andersen LL, Frandsen U, Sjogaard G (2011a) Strength training increases the size of the satellite cell pool in type I and II fibres of chronically painful trapezius muscle in females. J Physiol 589:5503–5515.
    Mackey AL et al (2011b) Sequenced response of extracellular matrix deadhesion and fibrotic regulators after muscle damage is involved in protection against future injury in human skeletal muscle. FASEB J 25:1943–1959.
    Mackey AL, Holm L, Reitelseder S, Pedersen TG, Doessing S, Kadi F, Kjaer M (2011c) Myogenic response of human skeletal muscle to 12 weeks of resistance training at light loading intensity. Scand J Med Sci Sports 21:773–782.
    Mahon M, Toman A, Willan PL, Bagnall KM (1984) Variability of histochemical and morphometric data from needle biopsy specimens of human quadriceps femoris muscle. J Neurol Sci 63:85–100
    Malm C, Sjodin TL, Sjoberg B, Lenkei R, Renstrom P, Lundberg IE, Ekblom B (2004) Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol 556:983–1000.
    Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
    Mayhew DL, Kim JS, Cross JM, Ferrando AA, Bamman MM (2009) Translational signaling responses preceding resistance training-mediated myofiber hypertrophy in young and old humans. J Appl Physiol (1985) 107:1655–1662.
    McCarthy JJ, Esser KA (2007) Counterpoint: satellite cell addition is not obligatory for skeletal muscle hypertrophy. J Appl Physiol (1985) 103:1100–1102. (discussion 1102–1103)
    McCarthy JJ, Dupont-Versteegden EE, Fry CS, Murach KA, Peterson CA (2017) Methodological issues limit interpretation of negative effects of satellite cell depletion on adult muscle hypertrophy. Development 144:1363–1365.
    McKay BR, O’Reilly CE, Phillips SM, Tarnopolsky MA, Parise G (2008) Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. J Physiol 586:5549–5560.
    McKay BR, De Lisio M, Johnston AP, O’Reilly CE, Phillips SM, Tarnopolsky MA, Parise G (2009) Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans. PLoS One 4:e6027.
    McKay BR, Toth KG, Tarnopolsky MA, Parise G (2010) Satellite cell number and cell cycle kinetics in response to acute myotrauma in humans: immunohistochemistry versus flow cytometry. J Physiol 588:3307–3320.
    McKeon PO, Medina JM, Hertel J (2006) Hierarchy of research design in evidence-based sports medicine. Int J Athl Ther Train 11:42–45
    Mitchell CJ et al (2014) Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS One 9:e89431.
    Mitchell CJ, Churchward-Venne TA, Cameron-Smith D, Phillips SM (2015) What is the relationship between the acute muscle protein synthesis response and changes in muscle mass? J Appl Physiol (1985) 118:495–497.
    Moore DR, Phillips SM, Babraj JA, Smith K, Rennie MJ (2005) Myofibrillar and collagen protein synthesis in human skeletal muscle in young men after maximal shortening and lengthening contractions. Am J Physiol Endocrinol Metab 288:E1153–E1159.
    Moore DR, Tang JE, Burd NA, Rerecich T, Tarnopolsky MA, Phillips SM (2009) Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. J Physiol 587:897–904.
    Moore DR, Young M, Phillips SM (2012) Similar increases in muscle size and strength in young men after training with maximal shortening or lengthening contractions when matched for total work. Eur J Appl Physiol 112:1587–1592.
    Moritani T, deVries HA (1979) Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58:115–130
    Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G (2011) Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138:3625–3637.
    Murphy-Ullrich JE (2001) The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J Clin Invest 107:785–790.
    Nederveen JP et al (2017) Altered muscle satellite cell activation following 16 week of resistance training in young men. Am J Physiol Regul Integr Comp Physiol 312:R85-R92.
    Newton MJ, Morgan GT, Sacco P, Chapman DW, Nosaka K (2008) Comparison of responses to strenuous eccentric exercise of the elbow flexors between resistance-trained and untrained men. J Strength Cond Res 22:597–607.
    Nosaka K, Clarkson PM (1996) Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exerc 28:953–961
    Nosaka K, Newton M (2002) Concentric or eccentric training effect on eccentric exercise-induced muscle damage. Med Sci Sports Exerc 34:63–69
    Nosaka K, Sakamoto K (2001) Effect of elbow joint angle on the magnitude of muscle damage to the elbow flexors. Med Sci Sports Exerc 33:22–29
    Nosaka K, Clarkson PM, McGuiggin ME, Byrne JM (1991) Time course of muscle adaptation after high force eccentric exercise. Eur J Appl Physiol Occup Physiol 63:70–76
    Nosaka K, Newton M, Sacco P (2002) Delayed-onset muscle soreness does not reflect the magnitude of eccentric exercise-induced muscle damage. Scand J Med Sci Sports 12:337–346
    Nosaka K, Lavender A, Newton M, Sacco P (2003) Muscle damage in resistance training—is muscle damage necessary for strength gain and muscle hypertrophy? Int J Sport Health Sci 1:1–8
    Nosaka K, Newton MJ, Sacco P (2005) Attenuation of protective effect against eccentric exercise-induced muscle damage. Can J Appl Physiol 30:529–542
    O’Connor RS, Pavlath GK (2007) Point:counterpoint: satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol (1985) 103:1099–1100.
    O’Reilly C, McKay B, Phillips S, Tarnopolsky M, Parise G (2008) Hepatocyte growth factor (HGF) and the satellite cell response following muscle lengthening contractions in humans. Muscle Nerve 38:1434–1442.
    Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF (1997) Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385:537–540.
    Paulsen G, Mikkelsen UR, Raastad T, Peake JM (2012) Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exerc Immunol Rev 18:42–97
    Peake J, Nosaka K, Suzuki K (2005) Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev 11:64–85
    Petrella JK, Kim JS, Cross JM, Kosek DJ, Bamman MM (2006) Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol Endocrinol Metab 291:E937–E946.
    Petrella JK, Kim JS, Mayhew DL, Cross JM, Bamman MM (2008) Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol (1985) 104:1736–1742.
    Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273:E99–E107
    Phillips SM, Tipton KD, Ferrando AA, Wolfe RR (1999) Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am J Physiol 276:E118–E124
    Phillips SM, Parise G, Roy BD, Tipton KD, Wolfe RR, Tamopolsky MA (2002) Resistance-training-induced adaptations in skeletal muscle protein turnover in the fed state. Can J Physiol Pharmacol 80:1045–1053
    Phillips BE, Hill DS, Atherton PJ (2012) Regulation of muscle protein synthesis in humans. Curr Opin Clin Nutr Metab Care 15:58–63.
    Pillen S et al (2009) Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol 35:443–446.
    Proske U, Morgan DL (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537:333–345
    Puddy RW, Wilkins N (2011) Understanding evidence Part 1: best available research evidence. A Guide to the Continuum of Evidence of Efectiveness, Atlanta
    Raastad T et al (2010) Changes in calpain activity, muscle structure, and function after eccentric exercise. Med Sci Sports Exerc 42:86–95
    Rahbek SK, Farup J, Moller AB, Vendelbo MH, Holm L, Jessen N, Vissing K (2014) Effects of divergent resistance exercise contraction mode and dietary supplementation type on anabolic signalling, muscle protein synthesis and muscle hypertrophy. Amino Acids 46:2377–2392.
    Rosenberg JG, Ryan ED, Sobolewski EJ, Scharville MJ, Thompson BJ, King GE (2014) Reliability of panoramic ultrasound imaging to simultaneously examine muscle size and quality of the medial gastrocnemius. Muscle Nerve 49:736–740.
    Sale DG (1988) Neural adaptation to resistance training. Med Sci Sports Exerc 20:S135–S145
    Sambasivan R et al (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138:3647–3656.
    Sayers SP, Clarkson PM (2001) Force recovery after eccentric exercise in males and females. Eur J Appl Physiol 84:122–126.
    Schoenfeld BJ, Ogborn DI, Vigotsky AD, Franchi MV, Krieger JW (2017) Hypertrophic effects of concentric vs. eccentric muscle actions: a systematic review and meta-analysis. J Strength Cond Res 31:2599–2608.
    Seynnes OR, de Boer M, Narici MV (2007) Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol (1985) 102:368–373.
    Shepstone TN, Tang JE, Dallaire S, Schuenke MD, Staron RS, Phillips SM (2005) Short-term high- vs. low-velocity isokinetic lengthening training results in greater hypertrophy of the elbow flexors in young men. J Appl Physiol (1985) 98:1768–1776.
    Smeuninx B, McKendry J (2016) Mechanisms of resistance exercise-induced muscle hypertrophy: ‘You can’t make an omelette without breaking eggs’. J Physiol 594:7159–7160.
    Smith LL, Anwar A, Fragen M, Rananto C, Johnson R, Holbert D (2000) Cytokines and cell adhesion molecules associated with high-intensity eccentric exercise. Eur J Appl Physiol 82:61–67.
    Snijders T, Smeets JS, van Kranenburg J, Kies AK, van Loon LJ, Verdijk LB (2016) Changes in myonuclear domain size do not precede muscle hypertrophy during prolonged resistance-type exercise training. Acta Physiol (Oxf) 216:231–239.
    Sorichter S, Puschendorf B, Mair J (1999) Skeletal muscle injury induced by eccentric muscle action: muscle proteins as markers of muscle fiber injury. Exerc Immunol Rev 5:5–21
    Stock MS et al (2017) The time course of short-term hypertrophy in the absence of eccentric muscle damage. Eur J Appl Physiol 117:989–1004.
    Tang JE, Perco JG, Moore DR, Wilkinson SB, Phillips SM (2008) Resistance training alters the response of fed state mixed muscle protein synthesis in young men. Am J Physiol Regul Integr Comp Physiol 294:R172–R178.
    Tesch P (1980) Muscle fatigue in man. With special reference to lactate accumulation during short term intense exercise. Acta Physiol Scand Suppl 480:1–40
    Twist C, Eston RG (2009) The effect of exercise-induced muscle damage on perceived exertion and cycling endurance performance. Eur J Appl Physiol 105:559–567.
    Wang YX, Rudnicki MA (2011) Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 13:127–133.
    Warren GL, Lowe DA, Armstrong RB (1999) Measurement tools used in the study of eccentric contraction-induced injury. Sports Med 27:43–59
    Warren GL, Ingalls CP, Lowe DA, Armstrong RB (2002) What mechanisms contribute to the strength loss that occurs during and in the recovery from skeletal muscle injury? J Orthop Sports Phys Ther 32:58–64.
    Wernbom M, Augustsson J, Thomee R (2007) The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Med 37:225–264
    Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, Rennie MJ (2008) Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586:3701–3717.
    Young A, Hughes I, Round JM, Edwards RH (1982) The effect of knee injury on the number of muscle fibres in the human quadriceps femoris. Clin Sci (Lond) 62:227–234
    Yu JG, Carlsson L, Thornell LE (2004) Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol 121:219–227.
    Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357.
    Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ, Shulman GI (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA 99:15983–15987.