Monitoring exercise-induced muscle damage indicators and myoelectric activity during two weeks of knee extensor exercise training in young and old men

Autoři: Zoltán Heckel aff001;  Tamás Atlasz aff002;  Éva Tékus aff002;  Tamás Kőszegi aff003;  József Laczkó aff005;  Márk Váczi aff006
Působiště autorů: Doctoral School of Health Sciences, Faculty of Health Sciences, University of Pécs, Pécs, Hungary aff001;  Department of Sportbiology, Institute of Sport Sciences and Physical Education, University of Pécs, Pécs, Hungary aff002;  János Szentágothai Research Centre, University of Pécs, Pécs, Hungary aff003;  Department of Laboratory Medicine, Medical School, University of Pécs, Pécs, Hungary aff004;  Department of Informatics and Biorobotics, Institute of Mathematics and Informatics, University of Pécs, Pécs, Hungary aff005;  Department of Theory and Practice of Sports, Institute of Sport Sciences and Physical Education, University of Pécs, Pécs, Hungary aff006
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224866


This study considered the effects of repeated bouts of short-term resistive exercise in old (age: 64.5±5.5 years; n = 10) and young men (age: 25.1±4.9 years; n = 10) who performed six knee extension exercise bouts over two weeks using various markers of exercise-induced muscle damage and electromyographic activity. We found that time-course changes in quadriceps isometric torque, creatine kinase activity, and muscle soreness in the two groups were similar. However, recovery in the acute torque deficit was mediated by more favourable electromyographic activity changes in the young group than in the older adults group. Muscle elastic energy storage and re-use assessed with dynamometry was selectively improved in the young group by the end of the protocol. Serum myoglobin concentration increased selectively in old group, and remained elevated with further bouts, suggesting higher sarcolemma vulnerability and less effective metabolic adaptation in the older adults, which, however, did not affect muscle contractility.

Klíčová slova:

Elderly – Electromyography – Exercise – Knees – Muscle analysis – Muscle contraction – Strength training – Torque


1. Porter MM, Vandervoort AA, Lexell J. Aging of human muscle: structure, function and adaptability. Scand J Med Sci Sports. 1995;5(3):129–142. 7552755

2. Skelton DA, Greig CA, Davies JM, Young A. Strength, Power and Related Functional Ability of Healthy People Aged 65–89 Years. Age Ageing. 1994;23(5):371–377. doi: 10.1093/ageing/23.5.371 7825481

3. Ploutz-Snyder LL, Giamis EL, Formikell M, Rosenbaum AE. Resistance training reduces susceptibility to eccentric exercise-induced muscle dysfunction in older women. J Gerontol Biol Sci. 2001;56(9):B384–B390.

4. Váczi M, Nagy SzA, Kőszegi T, Ambrus M, Bogner P, Perlaki G, et al. Mechanical, hormonal, and hypertrophic adaptations to 10 weeks of eccentric and stretch-shortening cycle exercise training in old males. Exp Gerontol. 2014;58:69–77. doi: 10.1016/j.exger.2014.07.013 25064038

5. Nosaka K, Newton M. Concentric or eccentric training effect on eccentric exercise-induced muscle damage. Med Sci Sports Exerc. 2002;34(1):63–69. doi: 10.1097/00005768-200201000-00011 11782649

6. Newham DJ, Jones DA, Clarkson PM. Repeated high force eccentric exercise: effects on muscle pain and damage. J Appl Physiol. 1987;63(4):1381–1386. doi: 10.1152/jappl.1987.63.4.1381 3693172

7. Clarkson PM, Dedrick ME. Exercise-induced muscle damage, repair, and adaptation in old and young subjects. J Gerontol. 1988;43(4):M91–M96. doi: 10.1093/geronj/43.4.m91 3385145

8. Eston RG, Finney S, Baker S, Baltzopoulos V. Muscle tenderness and peak torque changes after downhill running following a prior bout of isokinetic eccentric exercise. J Sports Sci. 1996;14(4):291–299. doi: 10.1080/02640419608727714 8887208

9. Hortobagyi T, Houmard J, Fraser D, Dudek R, Lambert J, Tracy J. Normal forces and myofibrillar disruption after repeated eccentric exercise. J Appl Physiol. 1998;84(2):492–498. doi: 10.1152/jappl.1998.84.2.492 9475858

10. Lieber RL, Friden J. Mechanisms of muscle injury after eccentric contraction. J Sci Med Sports. 1999;2(3):253–265.

11. Mair J, Mayr M, Müller E, Koller A, Haid C, Artner-Dworzak E, et al. Rapid adaptation to eccentric exercise-induced muscle damage. Int J Sports Med. 1995;16(6):352–356. doi: 10.1055/s-2007-973019 7591384

12. Conceiçăo MS, Libardi CA, Nogueira FRD, Bonganha V, Gáspari AF, Chacon-Mikahil MPT, et al. 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. 2012;112(9):3205–3213. doi: 10.1007/s00421-011-2292-6 22227852

13. Peake J, Della-Gatta P, Cameron-Smith D. Aging and its effects on inflammation in skeletal muscle at rest and following exercise-induced muscle injury. Am J Physiol Regul Integr Comp Physiol. 2010;298(6):R1485–R1495. doi: 10.1152/ajpregu.00467.2009 20393160

14. Gorianovas G, Skurvydas A, Streckis V, Brazaitis M, Kamandulis S, McHugh MP. Repeated bout effect was more expressed in young adult males than in elderly males and boys. BioMed Res Int. 2013;218970. doi: 10.1155/2013/218970 23484095

15. 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(5):619–626. doi: 10.1007/s00421-006-0224-7 16767435

16. 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. 2001a;33(9):1490–1495.

17. 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. 2001b;85(1–2):34–40.

18. Nosaka K, Clarkson PM. Muscle damage following repeated bouts of high force eccentric exercise. Med Sci Sports Exerc. 1995;27(9):1263–1269. 8531624

19. Hortobagyi T, Barrier J, Beard D, Braspennincx J, Koens P, Devita P, et al. Greater initial adaptation to submaximal muscle lengthening than shortening. J Appl Physiol. 1996;81(4):1677–1682. doi: 10.1152/jappl.1996.81.4.1677 8904586

20. Gordon PM, Liu D, Sartor MA, IglayReger HB, Pistilli EE, Gutmann L, et al. Resistance exercise training influences skeletal muscle immune activation: a microarray analysis. J Appl Physiol. 2012;112(3):443–453. doi: 10.1152/japplphysiol.00860.2011 22052873

21. Mackey AL, Brandstetter S, Schjerling P, Bojsen-Moller J, Qvortrup K, Pedersen MM, et al. 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. 2011;25(6):1943–1959. doi: 10.1096/fj.10-176487 21368102

22. Váczi M, Tihanyi J, Hortobágyi T, Rácz L, Csende Z, Costa A, et al. Mechanical, biochemical, and EMG responses to short-term eccentric-concentric knee extensor training in humans. J Strength Cond Res. 2011;25(4):922–932. doi: 10.1519/JSC.0b013e3181c1fa47 20651608

23. Roth SM, Martel GF, Ivey FM, Lemmer JT, Metter EJ, Hurley BF, et al. High-volume, heavy-resistance strength training and muscle damage in young and older women. J Appl Physiol. 2000;88(3):1112–1118. doi: 10.1152/jappl.2000.88.3.1112 10710410

24. Kosek DJ, Kim J, Petrella JK, Cross JM, Bamman MM. Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J Appl Physiol. 2006;101(2):531–544. doi: 10.1152/japplphysiol.01474.2005 16614355

25. Ehsani F, Nodehi-Moghadam A, Ghandali H, Ahmadizade Z. The comparison of cross–education effect in young and elderly females from unilateral training of the elbow flexors. Med J Islam Repub Iran. 2014;28:138. 25694996

26. Frontera WR, Hughes VA, Krivickas LS, Kim SK, Foldvari M, Roubenoff R. Strength training in older women: early and late changes in whole muscle and single cells. Muscle Nerve. 2003;28(5):601–608. doi: 10.1002/mus.10480 14571463

27. Jenkins NDM, Buckner L, Cochrane KC, Bergstrom HC, Palmer TB, Johnson OG, et al. Age-related differences in rates of torque development and rise in EMG are eliminated by normalization. Exp Gerontol. 2014;57:18–28. doi: 10.1016/j.exger.2014.04.015 24806786

28. Váczi M, Rácz L, Hortobágyi T, Tihanyi J. Dynamic contractility and efficiency impairments in stretch-shortening cycle are stretch-load-dependent after training-induced muscle damage. J Strength Cond Res. 2013;27(8):2171–2179. doi: 10.1519/JSC.0b013e31827da32c 23207890

29. Harrison AJ, Gaffney SD. Effects of muscle damage on stretch shortening cycle function and muscle stiffness control. J Strength Cond Res. 2004;18(4):771–776. doi: 10.1519/14343.1 15574081

30. Avlund K, Schroll M, Davidsen M, Lovborg B, Rantanen T. Maximal isometric muscle strength and functional ability in daily activities among 75-year-old men and women. Scand J Med Sci Sports 1994;4(1):32–40.

31. Abellan van Kan G, Rolland Y, Andrieu S, Bauer J, Beauchet O, Bonnefoy M, et al. Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an International Academy on Nutrition and Aging (IANA). J Nutr Health Aging. 2009;13(10):881–889. 19924348

32. Hardy SE, Perera S, Roumani YF, Chandler JM, Studenski SA. Improvement in usual gait speed predicts better survival in older adults. J Am Geriatr Soc. 2007;55(11):1727–1734. doi: 10.1111/j.1532-5415.2007.01413.x 17916121

33. Hvid LG, Suetta C, Nielsen JH, Jensen MM, Frandsen U, Ørtenblad N, et al. Aging impairs the recovery in mechanical muscle function following 4 days of disuse. Exp Gerontol. 2014;52:1–8. doi: 10.1016/j.exger.2014.01.012 24447828

34. Kyröläinen H, Takala TES, Komi PV. Muscle damage induced by stretch-shortening cycle exercise. Med Sci Sports Exerc. 1998;30(3):415–420. doi: 10.1097/00005768-199803000-00012 9526888

35. Campbell MJ, McComas AJ, Petito F. Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry. 1973;36(2):174–182. doi: 10.1136/jnnp.36.2.174 4708452

36. Lexell J, Henriksson-Larsen K, Winblad B, Sjöström M. Distribution of different fiber types in human skeletal muscles: effects of aging studied in whole muscle cross sections. Muscle Nerve. 1983;6(8):588–595. doi: 10.1002/mus.880060809 6646161

37. Clark BC, Manini TM. Sarkopenia ≠ Dynapenia. J Gerontol A Biol Sci Med Sci. 2008;63(8):829–834. doi: 10.1093/gerona/63.8.829 18772470

38. Roig M, Macinyre DL, Eng JJ, Narici MV, Maganaris CN, Reid WD. Preservation of eccentric strength in older adults: evidence, mechanisms and implications for training and rehabilitation. Exp Gerontol. 2010;45(6):400–409. doi: 10.1016/j.exger.2010.03.008 20303404

39. Ebbeling CB, Clarkson PM. Muscle adaptation prior to recovery following eccentric exercise. Eur J Appl Physiol. 1990;60(1):26–31.

40. Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc. 1992;24(5):512–520. 1569847

41. McHugh MP, Connolly DAJ, Eston RG, Gleim GW. Electromyographic analysis of exercise resulting in symptoms of muscle damage. J Sports Sci. 2000;18(3):163–172. doi: 10.1080/026404100365063 10737267

42. McHugh MP, Connolly DAJ, Eston RG, Gleim GW. Electromyographic analysis of repeated bouts of eccentric exercise. J Sports Sci. 2001;19(3):163–170. doi: 10.1080/026404101750095295 11256821

43. Ferri A, Narici M, Grassi B, Pousson M. Neuromuscular recovery after a strength training session in elderly people. Eur J Appl Physiol. 2006;97(3):272–279. doi: 10.1007/s00421-006-0168-y 16572331

44. Takekura H, Fujinami N, Nishizawa T, Ogasawara H, Kasuga N. Eccentric exercise-induced morphological changes in the membrane systems involved in excitation-contraction coupling in rat skeletal muscle. J Physiol. 2001;533(2):571–583.

45. Strojnik V, Komi PV. Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol. 1998;84(1):344–350. doi: 10.1152/jappl.1998.84.1.344 9451655

46. Nosaka K, Newton M, Sacco P. Delayed-onset muscle soreness does notreflect the magnitude of eccentric exercise-induced muscle damage. Scand J Med Sci Sports. 2002;12(6):337–346. 12453160

47. Cooper ST, McNeil PL. Membrane repair: mechanisms and pathophysiology. Physiol Rev. 2015;95:1205–1240. doi: 10.1152/physrev.00037.2014 26336031

48. Larsson L. Morphological and functional characteristics of the ageing skeletal muscle in man. A cross-sectional study. Acta Physiol Scand Suppl. 1978;457:1–36. 281113

49. Nilwik R, Snijders T, Leenders M, Groen BBL, Kranenburg J, Verdijk LB, Loon LJC. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol. 2013;48(5):492–498. doi: 10.1016/j.exger.2013.02.012 23425621

50. Power GA, Dalton HB, Rice LC, Vandervoort AA. Power loss is greater following lengthening contractions in old versus young women. Age. 2012;34(3):737–750. doi: 10.1007/s11357-011-9263-z 21559865

51. Egan B, Zierath JR. Exercise Metabolism and the Molecular Regulation of Skeletal Muscle Adaptation. Cell Metab. 2013;17(2):162–184. doi: 10.1016/j.cmet.2012.12.012 23395166

52. Chen TC, Hsieh SS. Effects of a 7-day eccentric training period on muscle damage and inflammation. Med Sci Sports Exerc. 2001;33(10):1732–1738. doi: 10.1097/00005768-200110000-00018 11581559

53. Gabriel DA, Basford JR, An KN. Neural adaptations to fatigue: Implications for muscle strength and training. Med Sci Sports Exerc. 2001;33(8):1354–1360. doi: 10.1097/00005768-200108000-00017 11474338

54. Caserotti P, Aagaard P, Simonsen BE, Puggaard L. Contraction-specific differences in maximal muscle power during stretch-shortening cycle movements in elderly males and females. Eur J Appl Physiol. 2001;84(3):206–212. doi: 10.1007/s004210170006 11320637

55. Seger JY, Arvidsson B, Thorstensson A. Specific effects of eccentric and concentric training on muscle strength and morphology in humans. Eur J Appl Physiol. 1998;79(1):49–57.

56. Hortobagyi T, Hill J, Lambert N, Israel R. Force and EMG responses to eccentric and concentric resistive exercise training. Med Sci Sports Exerc. 1994;26:S31

57. Duncan PW, Chandler JM, Cavanaugh DK, Johnson KR, Buehler AG. Mode and speed specificity of eccentric and concentric exercise training. J Orthop Sports Phys Ther. 1989;11(2):70–75. 18796927

Článek vyšel v časopise


2019 Číslo 11