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. 1993 May;464:477–489. doi: 10.1113/jphysiol.1993.sp019646

Materials fatigue initiates eccentric contraction-induced injury in rat soleus muscle.

G L Warren 1, D A Hayes 1, D A Lowe 1, B M Prior 1, R B Armstrong 1
PMCID: PMC1175397  PMID: 8229814

Abstract

1. The initiation of exercise-induced muscle injury is thought to be the result of high tensile stresses produced in the muscle during eccentric contractions. Materials science theory suggests that high tensile stresses could initiate the injury during the first eccentric contraction (normal stress theory) or after multiple eccentric contractions (materials fatigue). It was the objective of this study to investigate the two possibilities. 2. Rat soleus muscles (n = 66; 11 protocols with 6 muscles per protocol) were isolated, placed in an oxygenated Krebs-Ringer buffer at 37 degrees C, and baseline measurements were made. The muscle then performed an injury protocol which consisted of between zero and ten eccentric contractions (muscle starting length = 0.90 soleus muscle length, L0; length change = 0.25 L0; velocity = 1.5 L0/s; peak force = 180% maximal isometric tetanic tension (P0); time between contractions = 4 min; total duration of the injury protocol = 40 min). At the end of the injury protocol, the muscle was incubated in buffer for 1 h; every 15 min, an isometric twitch and tetanus were performed and lactate dehydrogenase (LDH) release was measured. Total muscle [Ca2+] was measured at the end of the incubation. 3. Change-point regression analysis indicates that at 0 min into the incubation, declines in P0, maximal rate of tension development (+dP/dt), maximal rate of relaxation (-dP/dt), and muscle stiffness (dP/dx) became significantly greater after eight eccentric contractions (p < or = 0.05). No relation was found between the number of eccentric contractions performed and the LDH activity at 0 min into the incubation, although after 60 min of incubation, LDH activity in the buffer was linearly related to eccentric contraction number (p = 0.01). There was no relationship between total muscle [Ca2+] and eccentric contraction number. These findings support the materials fatigue hypothesis of exercise-induced muscle injury.

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Selected References

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  1. Armstrong R. B., Ogilvie R. W., Schwane J. A. Eccentric exercise-induced injury to rat skeletal muscle. J Appl Physiol Respir Environ Exerc Physiol. 1983 Jan;54(1):80–93. doi: 10.1152/jappl.1983.54.1.80. [DOI] [PubMed] [Google Scholar]
  2. Armstrong R. B., Warren G. L., Warren J. A. Mechanisms of exercise-induced muscle fibre injury. Sports Med. 1991 Sep;12(3):184–207. doi: 10.2165/00007256-199112030-00004. [DOI] [PubMed] [Google Scholar]
  3. Claflin D. R., Faulkner J. A. Shortening velocity extrapolated to zero load and unloaded shortening velocity of whole rat skeletal muscle. J Physiol. 1985 Feb;359:357–363. doi: 10.1113/jphysiol.1985.sp015589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ebbeling C. B., Clarkson P. M. Exercise-induced muscle damage and adaptation. Sports Med. 1989 Apr;7(4):207–234. doi: 10.2165/00007256-198907040-00001. [DOI] [PubMed] [Google Scholar]
  5. Fridén J., Kjörell U., Thornell L. E. Delayed muscle soreness and cytoskeletal alterations: an immunocytological study in man. Int J Sports Med. 1984 Feb;5(1):15–18. doi: 10.1055/s-2008-1025873. [DOI] [PubMed] [Google Scholar]
  6. Furuno K., Goldberg A. L. The activation of protein degradation in muscle by Ca2+ or muscle injury does not involve a lysosomal mechanism. Biochem J. 1986 Aug 1;237(3):859–864. doi: 10.1042/bj2370859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Garrett W. E., Jr, Nikolaou P. K., Ribbeck B. M., Glisson R. R., Seaber A. V. The effect of muscle architecture on the biomechanical failure properties of skeletal muscle under passive extension. Am J Sports Med. 1988 Jan-Feb;16(1):7–12. doi: 10.1177/036354658801600102. [DOI] [PubMed] [Google Scholar]
  8. Garrett W. E., Jr, Safran M. R., Seaber A. V., Glisson R. R., Ribbeck B. M. Biomechanical comparison of stimulated and nonstimulated skeletal muscle pulled to failure. Am J Sports Med. 1987 Sep-Oct;15(5):448–454. doi: 10.1177/036354658701500504. [DOI] [PubMed] [Google Scholar]
  9. Jackson M. J., Jones D. A., Edwards R. H. Measurements of calcium and other elements in muscle biopsy samples from patients with Duchenne muscular dystrophy. Clin Chim Acta. 1985 Apr 30;147(3):215–221. doi: 10.1016/0009-8981(85)90202-5. [DOI] [PubMed] [Google Scholar]
  10. Jones R. H., Molitoris B. A. A statistical method for determining the breakpoint of two lines. Anal Biochem. 1984 Aug 15;141(1):287–290. doi: 10.1016/0003-2697(84)90458-5. [DOI] [PubMed] [Google Scholar]
  11. Katz B. The relation between force and speed in muscular contraction. J Physiol. 1939 Jun 14;96(1):45–64. doi: 10.1113/jphysiol.1939.sp003756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. McCully K. K., Faulkner J. A. Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J Appl Physiol (1985) 1986 Jul;61(1):293–299. doi: 10.1152/jappl.1986.61.1.293. [DOI] [PubMed] [Google Scholar]
  13. Ogilvie R. W., Armstrong R. B., Baird K. E., Bottoms C. L. Lesions in the rat soleus muscle following eccentrically biased exercise. Am J Anat. 1988 Aug;182(4):335–346. doi: 10.1002/aja.1001820405. [DOI] [PubMed] [Google Scholar]
  14. SHONK C. E., BOXER G. E. ENZYME PATTERNS IN HUMAN TISSUES. I. METHODS FOR THE DETERMINATION OF GLYCOLYTIC ENZYMES. Cancer Res. 1964 May;24:709–721. [PubMed] [Google Scholar]
  15. Segal S. S., Faulkner J. A. Temperature-dependent physiological stability of rat skeletal muscle in vitro. Am J Physiol. 1985 Mar;248(3 Pt 1):C265–C270. doi: 10.1152/ajpcell.1985.248.3.C265. [DOI] [PubMed] [Google Scholar]
  16. Stauber W. T., Clarkson P. M., Fritz V. K., Evans W. J. Extracellular matrix disruption and pain after eccentric muscle action. J Appl Physiol (1985) 1990 Sep;69(3):868–874. doi: 10.1152/jappl.1990.69.3.868. [DOI] [PubMed] [Google Scholar]
  17. Stauber W. T. Eccentric action of muscles: physiology, injury, and adaptation. Exerc Sport Sci Rev. 1989;17:157–185. [PubMed] [Google Scholar]
  18. Street S. F., Ramsey R. W. Sarcolemma: transmitter of active tension in frog skeletal muscle. Science. 1965 Sep 17;149(3690):1379–1380. doi: 10.1126/science.149.3690.1379. [DOI] [PubMed] [Google Scholar]
  19. Tidball J. G. Myotendinous junction injury in relation to junction structure and molecular composition. Exerc Sport Sci Rev. 1991;19:419–445. [PubMed] [Google Scholar]
  20. Trotter J. A. Interfiber tension transmission in series-fibered muscles of the cat hindlimb. J Morphol. 1990 Dec;206(3):351–361. doi: 10.1002/jmor.1052060312. [DOI] [PubMed] [Google Scholar]
  21. Waterman-Storer C. M. The cytoskeleton of skeletal muscle: is it affected by exercise? A brief review. Med Sci Sports Exerc. 1991 Nov;23(11):1240–1249. [PubMed] [Google Scholar]

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