Skip to main content

Advertisement

SpringerLink
Log in

The magnitude of muscle strain does not influence serial sarcomere number adaptations following eccentric exercise

  • Skeletal Muscle
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

It is generally accepted that eccentric exercise, when performed by a muscle that is unaccustomed to that type of contraction, results in a delayed onset of muscle soreness (DOMS). A prolonged exposure to eccentric exercise leads to the disappearance of the signs and symptoms associated with DOMS, which has been referred to as the repeated bout effect (RBE). Although the mechanisms underlying the RBE remain unclear, several mechanisms have been proposed, including the serial sarcomere number addition following exercise induced muscle damage. In the traditional DOMS and RBE protocols, muscle injury has been treated as a global parameter, with muscle force and strain assumed to be uniform throughout the muscle. To assess the effects of muscle-tendon unit strain, fiber strain, torque and injury on serial sarcomere number adaptations, three groups of New Zealand White (NZW) rabbits were subjected to chronic repetitive eccentric exercise bouts of the ankle dorsiflexors for 6 weeks. These eccentric exercise protocols consisted of identical muscle tendon unit (MTU) strain, but other mechanical factors were systematically altered. Following chronic eccentric exercise, serial sarcomere number adaptations were not identical between the three eccentric exercise protocols, and serial sarcomere number adaptations were not uniform across all regions of the muscle. Peak torque and relaxation fiber strain were the best predictors of serial sarcomere number across all three protocols. Therefore, MTU strain does not appear to be the primary cause for sarcomerogenesis, and differential adaptations within the muscle may be explained by the nonuniform architecture of the muscle, resulting in differential local fiber strains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Barash IA, Mathew L, Ryan AF, Chen J, Lieber RL (2003) Rapid muscle-specific gene expression changes after a single bout of eccentric contractions in the mouse. Am J Physiol Cell Physiol

  2. Barash IA, Peters D, Friden J, Lutz GJ, Lieber RL (2002) Desmin cytoskeletal modifications after a bout of eccentric exercise in the rat. Am J Physiol Regul Integr Comp Physiol 283:R958–R963

    Google Scholar 

  3. Brockett CL, Morgan DL, Gregory JE, Proske U (2002) Damage to different motor units from active lengthening of the medial gastrocnemius muscle of the cat. J Appl Physiol 92:1104–1110

    Google Scholar 

  4. Brown SJ, Child RB, Day SH, Donnelly AE (1997) Exercise-induced skeletal muscle damage and adaptation following repeated bouts of eccentric muscle contractions. J Sports Sci 15:215–222

    Article  PubMed  Google Scholar 

  5. Burkholder TJ (2001) Age does not influence muscle fiber length adaptation to increased excursion. J Appl Physiol 91:2466–2470

    Google Scholar 

  6. Burkholder TJ, Lieber RL (1998) Sarcomere number adaptation after retinaculum transection in adult mice. J Exp Biol 201(Part 3):309–316

    Google Scholar 

  7. Butterfield TA, Herzog W (2004) Is the force–length relationship a useful indicator of contractile element damage following eccentric exercise? J Biomech 38(9):1932–1937

    Article  Google Scholar 

  8. Butterfield TA, Herzog W (2005a) Alterations in the starting length and activation timing of muscle influence fiber strain and muscle injury. J Appl Physiol—in revision JAP00524-2005

  9. Butterfield TA, Herzog W (2005b) Differential serial sarcomere number adaptations in knee extensor muscles of rats is contraction type dependent. J Appl Physiol doi:10.1152/japplphysiol.00481.2005

    Google Scholar 

  10. Butterfield TA, Herzog W (2005c) Quantification of muscle fiber strain during in-vivo repetitive stretch-shortening cycles. J Appl Physiol 99:593–602

    Article  PubMed  Google Scholar 

  11. De Deyne PG (2001) Application of passive stretch and its implications for muscle fibers. Phys Ther 81:819–827

    PubMed  Google Scholar 

  12. Goldspink G (1998) Cellular and molecular aspects of muscle growth, adaptation and ageing. Gerodontology 15:35–43

    Article  PubMed  Google Scholar 

  13. Goldspink G, Tabary C, Tabary JC, Tardieu C, Tardieu G (1974) Effect of denervation on the adaptation of sarcomere number and muscle extensibility to the functional length of the muscle. J Physiol 236:733–742

    PubMed  Google Scholar 

  14. Hortobagyi T, Barrier J, Beard D, Braspennincx J, Koens P, Devita P, Dempsey L, Lambert J (1996) Greater initial adaptations to submaximal muscle lengthening than maximal shortening. J Appl Physiol 81:1677–1682

    Google Scholar 

  15. Hortobagyi T, Houmard J, Fraser D, Dudek R, Lambert J, Tracy J (1998) Normal forces and myofibrillar disruption after repeated eccentric exercise. J Appl Physiol 84:492–498

    Google Scholar 

  16. Hough T (1902) Ergographic Studies in Muscle Soreness. Am J Physiol 7:76–92

    Google Scholar 

  17. Jones C, Allen T, Talbot J, Morgan DL, Proske U (1997) Changes in the mechanical properties of human and amphibian muscle after eccentric exercise. Eur J Appl Physiol Occup Physiol 76:21–31

    Article  PubMed  Google Scholar 

  18. Koh TJ, Brooks SV (2001) Lengthening contractions are not required to induce protection from contraction-induced muscle injury. Am J Physiol Regul Integr Comp Physiol 281:R155–R161

    Google Scholar 

  19. Koh TJ, Herzog W (1998a) Eccentric training does not increase sarcomere number in rabbit dorsiflexor muscles. J Biomech 31:499–501

    Article  PubMed  Google Scholar 

  20. Koh TJ, Herzog W (1998b) Excursion is important in regulating sarcomere number in the growing rabbit tibialis anterior. J Physiol 508(Part 1):267–280

    PubMed  Google Scholar 

  21. Koh TJ, Herzog W (1998c) Increasing the moment arm of the tibialis anterior induces structural and functional adaptation: implications for tendon transfer. J Biomech 31:593–599

    Article  PubMed  Google Scholar 

  22. Koh TJ, Leonard TR (1996) An implantable electrical interface for in vivo studies of the neuromuscular system. J Neurosci Methods 70:27–32

    Article  PubMed  Google Scholar 

  23. Koh TJ, Peterson JM, Pizza FX, Brooks SV (2003) Passive stretches protect skeletal muscle of adult and old mice from lengthening contraction-induced injury. J Gerontol A Biol Sci Med Sci 58:592–597

    PubMed  Google Scholar 

  24. Lapier TK, Burton HW, Almon R, Cerny F (1995) Alterations in intramuscular connective tissue after limb casting affect contraction-induced muscle injury. J Appl Physiol 78:1065–1069

    Google Scholar 

  25. Lieber RL, Friden J (2002) Morphologic and mechanical basis of delayed-onset muscle soreness. J Am Acad Orthop Surg 10:67–73

    PubMed  Google Scholar 

  26. Lieber RL, Woodburn TM, Friden J (1991) Muscle damage induced by eccentric contractions of 25% strain. J Appl Physiol 70:2498–2507

    Google Scholar 

  27. Lieber RL, Yeh Y, Baskin RJ (1984) Sarcomere length determination using laser diffraction Effect of beam and fiber diameter. Biophys J 45:1007–1016

    PubMed  Google Scholar 

  28. Lindsey CA, Makarov MR, Shoemaker S, Birch JG, Buschang PH, Cherkashin AM, Welch RD, Samchukov ML (2002) The effect of the amount of limb lengthening on skeletal muscle. Clin Orthop 278–287

  29. Lund H, Vestergaard-Poulsen P, Kanstrup IL, Sejrsen P (1998) Isokinetic eccentric exercise as a model to induce and reproduce pathophysiological alterations related to delayed onset muscle soreness. Scand J Med Sci Sports 8:208–215

    PubMed  Google Scholar 

  30. Lynn R, Morgan DL (1994) Decline running produces more sarcomeres in rat vastus intermedius muscle fibers than does incline running. J Appl Physiol 77:1439–1444

    PubMed  Google Scholar 

  31. Lynn R, Talbot JA, Morgan DL (1998) Differences in rat skeletal muscles after incline and decline running. J Appl Physiol 85:98–104

    Google Scholar 

  32. Malm C (2001) Exercise-induced muscle damage and inflammation: fact or fiction? Acta Physiol Scand 171:233–239

    Article  PubMed  Google Scholar 

  33. McHugh MP, Connolly DA, Eston RG, Gartman EJ, Gleim GW (2001) Electromyographic analysis of repeated bouts of eccentric exercise. J Sports Sci 19:163–170

    Article  PubMed  Google Scholar 

  34. McHugh MP, Connolly DA, Eston RG, Gleim GW (1999) Exercise-induced muscle damage and potential mechanisms for the repeated bout effect. Sports Med 27:157–170

    PubMed  Google Scholar 

  35. McHugh MP, Tetro DT (2003) Changes in the relationship between joint angle and torque production associated with the repeated bout effect. J Sports Sci 21:927–932

    Article  PubMed  Google Scholar 

  36. McKay SG, Morck DW, Merrill JK, Olson ME, Chan SC, Pap KM (1996) Use of tilmicosin for treatment of pasteurellosis in rabbits. Am J Vet Res 57:1180–1184

    PubMed  Google Scholar 

  37. Mendez J, Keys A (1960) Density and composition of mammalian muscle. Metabolism 9:184–188

    Google Scholar 

  38. Morgan DL, Proske U (2004) Popping sarcomere hypothesis explains stretch-induced muscle damage. Clin Exp Pharmacol Physiol 31:541–545

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  40. Patel TJ, Lieber RL (1997) Force transmission in skeletal muscle: from actomyosin to external tendons. Exerc Sport Sci Rev 25:321–363

    PubMed  Google Scholar 

  41. Peters D, Barash I, Burdi M, Yuan PS, Mathew L, Friden J, Lieber RL (2003) Asynchronous functional, cellular and transcriptional changes after a bout of eccentric exercise in the rat. J Physiol

  42. Proske U, Morgan DL (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537:333–345

    Article  PubMed  Google Scholar 

  43. Proske U, Morgan DL, Brockett CL, Percival P (2004) Identifying athletes at risk of hamstring strains and how to protect them. Clin Exp Pharmacol Physiol 31:546–550

    Google Scholar 

  44. Prou E, Guevel A, Benezet P, Marini JF (1999) Exercise-induced muscle damage: absence of adaptive effect after a single session of eccentric isokinetic heavy resistance exercise. J Sports Med Phys Fitness 39:226–232

    PubMed  Google Scholar 

  45. Schwane JA, Armstrong RB (1983) Effect of training on skeletal muscle injury from downhill running in rats. J Appl Physiol 55:969–975

    PubMed  Google Scholar 

  46. Smith LL (1991) Acute inflammation: the underlying mechanism in delayed onset muscle soreness? Med Sci Sports Exerc 23:542–551

    PubMed  Google Scholar 

  47. Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114:346–364

    Article  PubMed  Google Scholar 

  48. Tabary JC, Tabary C, Tardieu C, Tardieu G, Goldspink G (1972) Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. J Physiol 224:231–244

    PubMed  Google Scholar 

  49. Tabary JC, Tardieu C, Tardieu G, Tabary C (1981) Experimental rapid sarcomere loss with concomitant hypoextensibility. Muscle Nerve 4:198–203

    Article  PubMed  Google Scholar 

  50. Tabary JC, Tardieu C, Tardieu G, Tabary C, Gagnard L (1976) Functional adaptation of sarcomere number of normal cat muscle. J Physiol (Paris) 72:277–291

    Google Scholar 

  51. Taber LA (1998) Biomechanical growth laws for muscle tissue. J Theor Biol 193:201–213

    Article  PubMed  Google Scholar 

  52. Tardieu C, Tabary JC, Gagnard L, Lombard M, Tabary C, Tardieu G (1974) Change in the number of sarcomeres and in isometric tetanic tension after immobilization of the cat anterior tibialis muscle at different lengths. J Physiol (Paris) 68:205–218

    Google Scholar 

  53. Whitehead NP, Morgan DL, Gregory JE, Proske U (2003) Rises in whole muscle passive tension of mammalian muscle after eccentric contractions at different lengths. J Appl Physiol 95:1224–1234

    Google Scholar 

  54. Williams P, Watt P, Bicik V, Goldspink G (1986) Effect of stretch combined with electrical stimulation on the type of sarcomeres produced at the ends of muscle fibers. Exp Neurol 93:500–509

    Article  PubMed  Google Scholar 

  55. Williams PE (1988) Effect of intermittent stretch on immobilised muscle. Ann Rheum Dis 47:1014–1016

    PubMed  Google Scholar 

  56. Williams PE (1990) Use of intermittent stretch in the prevention of serial sarcomere loss in immobilised muscle. Ann Rheum Dis 49:316–317

    PubMed  Google Scholar 

  57. Williams PE, Catanese T, Lucey EG, Goldspink G (1988) The importance of stretch and contractile activity in the prevention of connective tissue accumulation in muscle. J Anat 158:109–114

    PubMed  Google Scholar 

  58. Williams PE, Goldspink G (1971) Longitudinal growth of striated muscle fibres. J Cell Sci 9:751–767

    PubMed  Google Scholar 

  59. Williams PE, Goldspink G (1973) The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat 116:45–55

    PubMed  Google Scholar 

  60. Wren TA (2003) A computational model for the adaptation of muscle and tendon length to average muscle length and minimum tendon strain. J Biomech 36:1117–1124

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Tim Leonard, Hoa Nguyen for their technical assistance, Dr. Motoshi Kaya, the CIHR Training Program in Bone and Joint Health, NSERC of Canada, and the CIHR Research Chair Program.

Author information

Authors and Affiliations

  1. Faculty of Kinesiology, University of Calgary, T2 N 1N4, Calgary, AB, Canada

    Timothy A. Butterfield & Walter Herzog

Authors
  1. Timothy A. Butterfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Walter Herzog
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Walter Herzog.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Butterfield, T.A., Herzog, W. The magnitude of muscle strain does not influence serial sarcomere number adaptations following eccentric exercise. Pflugers Arch - Eur J Physiol 451, 688–700 (2006). https://doi.org/10.1007/s00424-005-1503-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-005-1503-6

Keywords

Search

Navigation