Sports Medicine

, Volume 32, Issue 2, pp 103–123 | Cite as

Exercise-Induced Muscle Damage and the Potential Protective Role of Estrogen

Review Article

Abstract

Exercise-induced muscle damage is a well documented phenomenon that often follows unaccustomed and sustained metabolically demanding activities. This is a well researched, but poorly understood area, including the actual mechanisms involved in the muscle damage and repair cycle. An integrated model of muscle damage has been proposed by Armstrong and is generally accepted.

A more recent aspect of exercise-induced muscle damage to be investigated is the potential of estrogen to have a protective effect against skeletal muscle damage. Estrogen has been demonstrated to have a potent antioxidant capacity that plays a protective role in cardiac muscle, but whether this antioxidant capacity has the ability to protect skeletal muscle is not fully understood.

In both human and rat studies, females have been shown to have lower creatine kinase (CK) activity following both eccentric and sustained exercise compared with males. As CK is often used as an indirect marker of muscle damage, it has been suggested that female muscle may sustain less damage. However, these findings may be more indicative of the membrane stabilising effect of estrogen as some studies have shown no histological differences in male and female muscle following a damaging protocol.

More recently, investigations into the potential effect of estrogen on muscle damage have explored the possible role that estrogen may play in the inflammatory response following muscle damage. In light of these studies, it may be suggested that if estrogen inhibits the vital inflammatory response process associated with the muscle damage and repair cycle, it has a negative role in restoring normal muscle function after muscle damage has occurred.

This review is presented in two sections: firstly, the processes involved in the muscle damage and repair cycle are reviewed; and secondly, the possible effects that estrogen has upon these processes and muscle damage in general is discussed. The muscle damage and repair cycle is presented within a model, with particular emphasis on areas that are important to understanding the potential effect that estrogen has upon these processes.

References

  1. 1.
    Newham DJ, Mills KR, Quigley BM, et al. Pain and fatigue after concentric and eccentric muscle contractions. Clin Sci (Lond) 1983; 64: 55–62Google Scholar
  2. 2.
    Armstrong RB. Mechanisms of exercise-induced delayed onset muscle soreness: a brief review. Med Sci Sports Exerc 1984; 16: 529–38PubMedGoogle Scholar
  3. 3.
    Clarkson PM, Newham DJ. Associations between muscle soreness, damage and fatigue. In: Gandevia SC, Enoka RM, McComas AJ, et al., editors. Fatigue: neural and Muscular Mechanisms. New York (NY): Plenum, 1994: 457–69Google Scholar
  4. 4.
    Pyne DB. Regulation of neutrophil function during exercise. Sports Med 1994; 17: 245–58PubMedCrossRefGoogle Scholar
  5. 5.
    Wilmore JH, Costill DL. Physiology of sport and exercise. Champagne (IL): Human Kinetics, 1994Google Scholar
  6. 6.
    Hortobagyi T, Hill JP, Houmard JA, et al. Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol 1996; 80: 765–72PubMedGoogle Scholar
  7. 7.
    Lastayo PC, Reich TE, Urquhart M, et al. Chronic eccentric exercise improvements in muscle strength can occur with little demand for oxygen. Am J Physiol 1999; 276: R611–5Google Scholar
  8. 8.
    Bär PR, Reijneveld JC, Wokke JHJ, et al. Muscle damage induced by exercise: nature, prevention, and repair. In: Salmon S, editor. Muscle damage. New York (NY): Oxford Medical Publications, 1997: 1–27Google Scholar
  9. 9.
    Enoka RM. Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol 1996; 81: 2339–46PubMedGoogle Scholar
  10. 10.
    McComas AJ. Skeletal muscle: form and function. Champagne (IL): Human Kinetics, 1996Google Scholar
  11. 11.
    Friden J, Leiber RL. Structural and mechanical basis of exercise-induced muscle injury. Med Sci Sports Exerc 1992; 24: 521–30PubMedGoogle Scholar
  12. 12.
    Talag T. Residual muscle soreness as influenced by concentric, eccentric and static contractions. Res Q 1973; 44: 458–69PubMedGoogle Scholar
  13. 13.
    Howell JN, Chlebourn G, Conatser R. Muscle stiffness, strength loss, swelling and soreness following exercise-induced injury in humans. J Physiol 1993; 464: 183–96PubMedGoogle Scholar
  14. 14.
    Cleak MJ, Eston R. Delayed onset muscle soreness: mechanisms and management. J Sports Sci 1992; 10: 325–41PubMedCrossRefGoogle Scholar
  15. 15.
    Eston R, Peters D. Effects of cold water immersion on the symptoms of exercise-induced muscle damage. J Sports Sci 1999; 17: 231–8PubMedCrossRefGoogle Scholar
  16. 16.
    Yackzan L, Adams C, Francis KT. The effects of ice massage on delayed onset muscle soreness. AmJ Sports Med 1984; 12: 159–65CrossRefGoogle Scholar
  17. 17.
    Eston RG, Finney S, Baker S, et al. Muscle tenderness and peak torque changes after downhill running following a prior bout of isokinetic eccentric exercise. J Sports Sci 1996; 14: 291–9PubMedCrossRefGoogle Scholar
  18. 18.
    Jones DA, Newham DJ, Round JM, et al. Experimental human muscle damage: morphological changes in relation to other indices of damage. J Physiol 1986; 375: 435–48PubMedGoogle Scholar
  19. 19.
    Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 1992; 24: 512–20PubMedGoogle Scholar
  20. 20.
    Child RB, Saxton JM, Donnelly AE. Comparison of eccentric knee extensor muscle actions at two muscle lengths on indices of damage and angle-specific force production in humans. J Sports Sci 1998; 16: 301–8PubMedCrossRefGoogle Scholar
  21. 21.
    Cleak MJ, Eston R. Muscle soreness, swelling, stiffness and strength loss after intense eccentric exercise. Br J Sports Med 1992; 26: 267–72PubMedCrossRefGoogle Scholar
  22. 22.
    Nosaka K, Clarkson PM. Muscle damage following repeated bouts of high force eccentric exercise. Med Sci Sports Exerc 1995; 27: 1263–9PubMedGoogle Scholar
  23. 23.
    Jones DA, Round JM. Skeletal muscle in health and disease. Manchester: Manchester University Press, 1990Google Scholar
  24. 24.
    Armstrong RB. Initial events in exercise-induced muscular injury. Med Sci Sports Exerc 1990; 22: 429–35PubMedGoogle Scholar
  25. 25.
    McArdle A, Jackson MJ. Intracellular mechanisms involved in skeletal muscle damage. In: Salmon S, editor. Muscle damage. New York (NY): Oxford Medical Publications, 1997: 90–106Google Scholar
  26. 26.
    Jenkins RR. Free radical chemistry: relationship to exercise. Sports Med 1988; 5: 156–20PubMedCrossRefGoogle Scholar
  27. 27.
    Karlsson J. Antioxidants and exercise. Champagne (IL): Human Kinetics, 1997Google Scholar
  28. 28.
    Niess AM, Dickhuth H, Northoff H, et al. Free radicals and oxidative stress in exercise-immunological aspects. Exerc Immunol Rev 1999; 5: 22–56PubMedGoogle Scholar
  29. 29.
    Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide. Biochem J 1973; 128: 617–30Google Scholar
  30. 30.
    Crane FL, Sun IL, Clark MG, et al. Transplasma-membrane redox systems in growth and development. Biochim Biophys Acta 1985; 811: 233–64PubMedCrossRefGoogle Scholar
  31. 31.
    Font B, Vial C, Goldschmidt D. Metabolic levels and enzyme release in the ischaemic myocardium. J Mol Med 1977; 2: 291–7Google Scholar
  32. 32.
    Hellsten Y, Frandsen V, Orthenblad N, et al. Xanthine oxidase in human skeletal muscle following eccentric exercise: a role in inflammation. J Physiol 1997; 498: 239–48PubMedGoogle Scholar
  33. 33.
    Tiidus PM. Radical species in inflammation and overtraining. Can J Physiol Pharmacol 1998; 76: 533–8PubMedCrossRefGoogle Scholar
  34. 34.
    Davies KJA, Quintanilha AT, Brooks GA, et al. Free radicals and tissue damage produced by exercise. Biochim Biophys Res Com 1982; 107: 1198–205CrossRefGoogle Scholar
  35. 35.
    Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Oxford: Claredon Press, 1985Google Scholar
  36. 36.
    Best TM, Fiebig R, Corr DT, et al. Free radical activity, antioxidant enzyme, and glutathione changes with muscle stretch injury in rabbits. J Appl Physiol 1999; 87: 74–82PubMedGoogle Scholar
  37. 37.
    Eston R, Jackson M, Pears J. Association between the production of thiobarbituric reactive substances (malondialdehyde) and markers of muscle damage induced by uphill and downhill running [abstract]. J Sports Sci 1996; 14: 80CrossRefGoogle Scholar
  38. 38.
    Lowe DA, Warren GL, Ingalls CP, et al. Muscle function and protein metabolism after initiation of eccentric contraction-induced injury. J Appl Physiol 1995; 79: 1260–70PubMedGoogle Scholar
  39. 39.
    Byrd SK. Alterations in the sarcoplasmic reticulum, a possible link to exercise-induced muscle damage. Med Sci Sports Exerc 1992; 24: 531–6PubMedGoogle Scholar
  40. 40.
    Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 1991; 12: 184–207PubMedCrossRefGoogle Scholar
  41. 41.
    Lieber RL, Friden J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol 1993: 526Google Scholar
  42. 42.
    Duncan CJ. Role of intracellular calcium in promoting muscle damage: a strategy for controlling the dystrophic condition. Experientia 1978; 34: 1531–5PubMedCrossRefGoogle Scholar
  43. 43.
    Amelink GJ, van der Kallen CJM, Wokke JHJ, et al. Dantrolene sodium diminishes exercise-induced muscle damage in he rat. Eur J Pharmacol 1990; 179: 187–92PubMedCrossRefGoogle Scholar
  44. 44.
    Clarkson PM, Sayers SP. Etiology of exercise-induced muscle damage. Can J Appl Physiol 1999; 24: 234–48PubMedCrossRefGoogle Scholar
  45. 45.
    Belcastro AN, Shewchuk LD, Raj DA. Exercise-induced muscle injury; a calpain hypothesis. Mol Cell Biochem; 1998 179: 135–45PubMedCrossRefGoogle Scholar
  46. 46.
    Ingalls CP, Warren GL, Williams JH, et al. E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 1998; 85: 58–67PubMedGoogle Scholar
  47. 47.
    Tidball JG. Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc 1995; 27: 1022–32PubMedCrossRefGoogle Scholar
  48. 48.
    Evans WJ, Cannon JG. The metabolic effects of exercise-induced muscle damage. Exerc Sport Sci Rev 1991; 19: 99–125PubMedCrossRefGoogle Scholar
  49. 49.
    MacIntyre DL, Reid WD, McKenzie DC. The inflammatory response to muscle injury and its clinical implications. Sports Med 1995; 20: 24–40PubMedCrossRefGoogle Scholar
  50. 50.
    Bagby GJ, Larry CD, Shepherd RE. Exercise and cytokines: spontaneous and elicited responses. In: Hoffman-Goetz L, editor. Exercise and immune function. Boca Raton (FL): CRC Press, 1996: 55–79Google Scholar
  51. 51.
    Imura H, Fukata J, Mori T. Cytokines and endocrine function: an interaction between the immune and neuroendocrine systems. Clin Endocrinol 1996; 35: 107–15CrossRefGoogle Scholar
  52. 52.
    St Pierre Schneider B, Correia LA, Cannon JG. Sex differences in leukocyte invasion in injured murine skeletal muscle. Res Nurs Health 1996; 22: 243–51CrossRefGoogle Scholar
  53. 53.
    McCord J. Superoxide radical: controversies, contradictions, and paradoxes. Proc Soc Exp Biol Med 1995; 209: 112–7PubMedGoogle Scholar
  54. 54.
    Cantini M, Carraro U. Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J Neuropathol Exp Neurol 1995; 54: 121–8PubMedCrossRefGoogle Scholar
  55. 55.
    Merly F, Lescaudron L, Rouaud T, et al. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 1999; 22: 724–32PubMedCrossRefGoogle Scholar
  56. 56.
    Lescaudron L, Peltekian E, Fontaine-Perus J, et al. Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul Disord 1999; 9: 72–80PubMedCrossRefGoogle Scholar
  57. 57.
    Stumpf W, Sar M, Aumuller G. The heart: a target organ for estradiol. Science 1977; 196: 319–20PubMedCrossRefGoogle Scholar
  58. 58.
    Bush TL, Barret-Conner E, Cowan LD. Cardiovascular mortality and non-contractile estrogen use in women; results from the lipid research clinics program follow up study. Circulation 1987; 75: 1002–9CrossRefGoogle Scholar
  59. 59.
    Gruchow HW, Anderson AJ, Barbarak JJ. Postmenopausal use of estrogen and occlusion of coronary arteries. Am Heart J 1988; 115: 954–63PubMedCrossRefGoogle Scholar
  60. 60.
    Barret-Connor E, Bush T. Estrogen and coronary heart disease in women. JAMA 1991; 265: 1861–5CrossRefGoogle Scholar
  61. 61.
    Chisholm G. Antioxidants and atherosclerosis: a current assessment. Clin Cardiol 1991; 12: 125–30Google Scholar
  62. 62.
    Stampfer MJ, Colditz GA, Willet WC. Postmenopausal estrogen therapy and cardiovascular disease. N Engl J Med 1991; 325: 756–62PubMedCrossRefGoogle Scholar
  63. 63.
    Tiidus PM. Can estrogens diminish exercise induced muscle damage? Can J Appl Physiol 1995; 20: 26–38PubMedCrossRefGoogle Scholar
  64. 64.
    Bunt J. Metabolic actions of estradiol: significance for acute and chronic exercise response. Med Sci Sports Exerc 1990; 22: 286–90PubMedGoogle Scholar
  65. 65.
    Tiidus PM. Nutritional implications of gender differences in metabolism: estrogen and oxygen radicals: oxidative damage, inflammation and muscle function. In: Tarnopolsky M, editor. Gender differences in metabolism: practical and nutritional implications. Boca Raton (FL): CRC Press, 1999: 265–81Google Scholar
  66. 66.
    Wiseman H, O’Reilly J. Oestrogen as antioxidant cardio-protectants. Biochem Soc Trans 1997; 25: 54–9PubMedGoogle Scholar
  67. 67.
    Yagi K, Komura S. Inhibitory effect of female hormones on lipid peroxidation. Biochem Int 1986; 13: 1051–5PubMedGoogle Scholar
  68. 68.
    Sugioka K, Shimosegawa Y, Nakano M. Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Lett 1987; 210: 37–9PubMedCrossRefGoogle Scholar
  69. 69.
    Huber L, Scheffler E, Poll T, et al. 17β-estradiol inhibits LDL oxidation and cholesteryl ester formation in cultured macrophages. Free Radic Res Commun 1990; 8: 167–75PubMedCrossRefGoogle Scholar
  70. 70.
    Mooradian AD. Antioxidant properties of steroids. Biochem Mol Biol 1993; 45: 509–11Google Scholar
  71. 71.
    Subbiah M, Kessel B, Agrawal M, et al. Antioxidant potential of specific estrogens on lipid peroxidation. J Clin Endocrinol Metabol 1993; 77: 1095–7CrossRefGoogle Scholar
  72. 72.
    Ayres S, Tang M, Subbiah MTR. Estradiol 17β as an antioxidant: some distinct features when compared with common fat-soluble antioxidants. J Lab Clin Med 1996; 128 (4): 367–75PubMedCrossRefGoogle Scholar
  73. 73.
    Ayres S, Abplanalp W, Liu JH, et al. Mechanisms involved in the protective effect of estradiol-17/β on lipid peroxidation and DNA damage. Am J Physiol 1998; 274: E1002–8Google Scholar
  74. 74.
    Ruehlmann DO, Mann GE. Actions of oestrogen on vascular endothelial and smooth muscle cells. Biochem Soc Trans 1997; 25: 40–5PubMedGoogle Scholar
  75. 75.
    Bär PR, Amelink GJ. Protection against muscle damage exerted by oestrogen; hormonal or antioxidant action? Biochem Soc Trans 1997; 25: 50–4PubMedGoogle Scholar
  76. 76.
    Persky AM, Green PS, Stubley L, et al. Protective effect of estrogen against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 2000; 223: 59–66PubMedCrossRefGoogle Scholar
  77. 77.
    Bowles D, Torgan C, Ebner S, et al. Effects of acute submaximal exercise on skeletal muscle vitamin E. Free Radic Res Commun 1991; 14: 138–43Google Scholar
  78. 78.
    Sen CK, Atalay M, Agren J, et al. Fish oil and vitamin E supplementation in oxidative stress at rest and after physical exercise. J Appl Physiol 1997: 95Google Scholar
  79. 79.
    Tiidus PM, Houston ME. Vitamin E status does not affect the responses to exercise training and acute exercise in female rats. J Nutr 1993: 840Google Scholar
  80. 80.
    Wiseman H, Quinn P, Halliwell B. Tamoxifen and related compounds decrease membrane fluidity in liposomes: mechanism for the antioxidant action of tamoxifen and relevance to its anticancer and cardio protective actions? FEBS Lett 1993; 330: 53–6PubMedCrossRefGoogle Scholar
  81. 81.
    Wiseman H, Quinn P. The antioxidant action of synthetic oestrogens involves decreased membrane fluidity: relevance to their potential use as an anticancer and cardioprotective agents compared to tamoxifen. Free RadicRes 1994; 21: 187–94CrossRefGoogle Scholar
  82. 82.
    Whiting KP, Restall CJ, Brain PF. Steroid hormone-induced effects on membrane fluidity and their potential roles in nongenomic mechanisms. Life Sci 2000; 67: 743–57PubMedCrossRefGoogle Scholar
  83. 83.
    Esperson GT, Elbeak A, Ernst E, et al. Effects of physical exercise on cytokines and lymphocyte subpopulations in human peripheral blood. APMIS 1990; 98: 395–400CrossRefGoogle Scholar
  84. 84.
    Fielding RA, Manfredi TJ, Ding W, et al. Acute phase response in exercise III: neutrophil and IL-1β accumulation in skeletal muscle. Am J Physiol 1993; 265: R166–72Google Scholar
  85. 85.
    Bruunsgaard H, Galbo H, Halkjaer-Kristensen J, et al. Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J Physiol 1997; 499: 833–41PubMedGoogle Scholar
  86. 86.
    Pedersen BK, Bruunsgaard H, Klokker M, et al. Exercise-induced immunomodulation: possible roles of neuroendocrine and metabolic factors. Int J Sports Med 1997; 18: S2–7CrossRefGoogle Scholar
  87. 87.
    Suzuki K, Totsuka M, Nakaji MY, et al. Endurance exercise causes interaction among stress hormones, cytokine, neutrophil dynamics and muscle damage. J Appl Physiol 1999; 87: 1360–7PubMedGoogle Scholar
  88. 88.
    Smith LL, Anwar A, Fragen M, et al. Cytokines and cell adhesion molecules associated with high intensity eccentric exercise. Eur J Appl Physiol 2000; 82: 61–7PubMedCrossRefGoogle Scholar
  89. 89.
    Montgomery KF, Osborn L, Hession C, et al. Activation of endothelial- leukocyte adhesion molecule 1 (ELAM-1) gene transcription. Proc Natl Acad Sci U S A 1991; 88: 6523–7PubMedCrossRefGoogle Scholar
  90. 90.
    Degitz K, Lian-Jie L, Caughman SW. Cloning and characterization of the 5’transcriptional regulatory region of the human intercellular adhesion molecule 1 gene. J Biol Chem 1991; 266: 14024–30PubMedGoogle Scholar
  91. 91.
    Iadermarco M, McQuillan J, Rosen G, et al. Characterization of the promoter for vascular cell adhesion molecule-1 (VCAM- 1). J Biol Chem 1992; 267: 16323–9Google Scholar
  92. 92.
    Yoshikawa T, Yoshida N. Vitamin E and leukocyte endothelial cell interactions. Antioxid Redox Signal 2000; 2: 821–5PubMedCrossRefGoogle Scholar
  93. 93.
    Sen CK. Antioxidant and redox regulation of cellular signalling: introduction. Med Sci Sports Exercise 2001; 33: 368–70CrossRefGoogle Scholar
  94. 94.
    Sen CK, Roy S. Antioxidant regulation of cell adhesion. Med Sci Sports Exerc 2001; 33: 377–81PubMedCrossRefGoogle Scholar
  95. 95.
    Caulin-Glaser T, Watson CA, Pardi R, et al. Effects of 17β-estradiol on cytokine-induced endothelial cell adhesion molecule expression. J Clin Invest 1996; 98: 36–42PubMedCrossRefGoogle Scholar
  96. 96.
    Beato M. Gene regulation by steroid hormones. Cell 1989; 56: 335–44PubMedCrossRefGoogle Scholar
  97. 97.
    Gaub MP, Bellard M, Scheuer I, et al. Activation of the ovalbumin gene by the estrogen receptor involves the fos-jun complex. Cell 1990; 63: 1267–76PubMedCrossRefGoogle Scholar
  98. 98.
    Shyamala G, Guiot MC. Activation of Kβ-specific proteins by estradiol. Proc Natl Acad Sci U S A 1992; 89: 10628–32PubMedCrossRefGoogle Scholar
  99. 99.
    Warren GL, Lowe DA, Armstrong RB. Measurement tools used in the study of eccentric contraction-induced injury. Sports Med 1999; 27: 43–59PubMedCrossRefGoogle Scholar
  100. 100.
    Meltzer HY. Factors affecting serum creatine phosphokinase levels in the general population: the role of race, activity and sex. Clin Chim Acta 1971; 33: 165–72PubMedCrossRefGoogle Scholar
  101. 101.
    Shumate JB, Brooke MH, Carroll JE, et al. Increased serum creatine kinase after exercise: a sex-linked phenomenon. Neurology 1979; 29: 902–4PubMedCrossRefGoogle Scholar
  102. 102.
    Berg A, Keul J. Physiological and metabolic responses of female athletes during laboratory and field exercise. Med Sport 1981; 14: 77–96Google Scholar
  103. 103.
    Rogers MA, Stull GA, Apple FS. Creatine kinase isoenzyme activities in men and women following a marathon race. Med Sci Sports Exerc 1985; 17: 679–82PubMedCrossRefGoogle Scholar
  104. 104.
    Bär PR, Amelink GJ, Oldenberg B, et al. Prevention of exercise-induced muscle membrane damage by oestradiol. Life Sci 1988; 42: 2677–81PubMedCrossRefGoogle Scholar
  105. 105.
    Amelink GJ, Bär PR. Exercise-induced muscle protein leakage in the rat: effects of hormonal manipulation. J Neurol Sci 1986; 76: 61–8PubMedCrossRefGoogle Scholar
  106. 106.
    Van der Meulen JH, Kuipers H, Drukker J. Relationship between exercise-induced muscle damage and enzyme release in rats. J Appl Physiol 1991; 71: 999–1004PubMedGoogle Scholar
  107. 107.
    Dumke CL. Protective mechanism of estradiol on eccentrically induced muscle damage [thesis]. Eugen (OR): University of Oregon, 1996Google Scholar
  108. 108.
    Reijneveld JC, Ferrington DA, Amelink GJ, et al. Estradiol treatment reduces structural muscle damage after exercise in male rats [abstract]. Med Sci Sports Exerc 1994; 25 Suppl.: S72Google Scholar
  109. 109.
    Buckley-Bleiler R, Maughan RJ, Clarkson PM, et al. Serum creatine kinase activity after isometric exercise in pre-menopausal and post-menopausal women. Exp Aging Res 1989; 15: 195–8PubMedCrossRefGoogle Scholar
  110. 110.
    Thompson HS, Hyatt JP, De Souza MJ, et al. The effects of oral contraceptives on delayed onset muscle soreness following exercise. Contraception 1997; 56: 59–65PubMedCrossRefGoogle Scholar
  111. 111.
    Kendall BK, Eston RG. The effect of menstrual cycle status and oral contraceptive use on exercise-induced muscle damage [abstract]. J Sports Sci. In PressGoogle Scholar
  112. 112.
    Rinard J, Clarkson PM, Smith L, et al. Response of males and females to high-force eccentric exercise. J Sports Sci 2000; 18: 229–36PubMedCrossRefGoogle Scholar
  113. 113.
    Tiidus PM, Bombardier F. Oestrogen attenuates post exercise myeloperoxide activity in skeletal muscle of male rats. Acta Physiol Scand 1999; 166: 85–90PubMedCrossRefGoogle Scholar
  114. 114.
    Komulainen J, Koskinen SO, Kalliokoski R, et al. Gender differences in skeletal muscle fibre damage after eccentrically biased downhill running in rats. Acta Physiol Scand 1999; 165: 57–63PubMedCrossRefGoogle Scholar
  115. 115.
    Cannon JG, Meydani SM, Fielding R, et al. Acute phase response in exercise II: associations between vitamin E, cytokines, and muscle proteolysis. Am J Physiol 1991; 260: R1235–40Google Scholar
  116. 116.
    Stupka N, Lowther S, Chorneyka K, et al. Gender differences in muscle inflammation after eccentric exercise. J Appl Physiol 2000; 89: 2325–32PubMedGoogle Scholar
  117. 117.
    MacIntyre DL, Reid WD, Lyster DM, et al. Different effects of strenuous eccentric exercise on the accumulation of neutrophils in muscle in women and men. Eur J Appl Physiol 2000; 81: 57–3CrossRefGoogle Scholar
  118. 118.
    Prakash YS, Togaibayeva AA, Kannan MS, et al. Estrogen increases Ca2+ efflux from female porcine coronary arterial smooth muscle. Am J Physiol 1999; 276: H926–34Google Scholar
  119. 119.
    Jovanovic S, Jovanovic A, Shen WK, et al. Low concentrations of 17β-estradiol protect single cardiac cells against metabolic stress-induced Ca2+ loading. J Am Coll Cardiol 2000; 36: 948–52PubMedCrossRefGoogle Scholar
  120. 120.
    Tiidus PM, Holden D, Bombardier E, et al. Estrogen effect on post-exercise skeletal muscle neutrophil infiltration and calpain activity. Can J Physiol Pharmacol 2001; 79: 400–6PubMedCrossRefGoogle Scholar
  121. 121.
    Cid MC, Kleinman HK, Grant DS, et al. Estradiol enhances leukocyte binding to tumor necrosis factor (TNF)-stimulated endothelial cells via an increase in TNF-induced adhesion molecules E-selectin, intercellular adhesion molecule type 1, and vascular cell adhesion molecule type 1. J Clin Invest 1994; 93: 17–25PubMedCrossRefGoogle Scholar
  122. 122.
    Chao TZ, Van Alten PJ, Greager JA, et al. Steroid sex hormones regulate the release of tumor necrosis factor by macrophages. Cell Immunol 1995; 160: 43–9PubMedCrossRefGoogle Scholar
  123. 123.
    Rider V, Foster RT, Evans M, et al. Gender differences in autoimmune diseases: estrogen increases calcineurin expression in systemic lupus erythematosus. Clin Immunol Immunopathol 1998; 89: 171–80PubMedCrossRefGoogle Scholar
  124. 124.
    Ahmed SA, Hissong BD, Verthelyi D, et al. Gender and risk of autoimmune diseases: possible role of estrogenic compounds. Environ Health Perspect 1999; 107: 681–6PubMedGoogle Scholar
  125. 125.
    Tornwall J, Carey AB, Fox RI, et al. Estrogen in autoimmunity; expression of estrogen receptors in thymic and autoimmune T cells. J Gend Specif Med 1999; 2: 33–40PubMedGoogle Scholar
  126. 126.
    Marui N, Offerman M, Swerlick R, et al. Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J Clin Invest 1993; 92: 1866–74PubMedCrossRefGoogle Scholar
  127. 127.
    Zuckerman SH, Ahmari SE, Bryan-Poole N, et al. Estriol: a potent regulator of TNF and IL-6 expression in a murine model of endotoxemia. Inflammation 1996; 20: 581–97PubMedCrossRefGoogle Scholar
  128. 128.
    Schwarz E, Schafer C, Bode JC, et al. Influence of the menstrual cycle on the LPS-induced cytokine response of monocytes. Cytokine 2000; 12: 413–6PubMedCrossRefGoogle Scholar
  129. 129.
    Angstwurm MWA, Gärtner R, Ziegler-Heitbrock HWL. Cyclic plasma IL-6 levels during normal menstrual cycle. Cytokine 1997; 9: 370–4PubMedCrossRefGoogle Scholar
  130. 130.
    Pottratz ST, Bellido T, Macharla H, et al. 17β-estradiol inhibits expression of human interleukin-6 promoter-reporter constructs by a receptor-dependent mechanism. J Clin Invest 1994; 93: 944–50PubMedCrossRefGoogle Scholar
  131. 131.
    Mishra DK, Friden J, Schmitz MC, et al. Anti-inflammatory medication after muscle injury. A treatment resulting in short term improvement but subsequent loss of muscle function. J Bone Joint Surg Am 1997; 79: 1270–1Google Scholar
  132. 132.
    Thorsson O, Rantanen J, Hurme T, et al. Effects of non-steroidal anti-inflammatory medications on satellite cell proliferation during muscle regeneration. Am J Sports Med 1998; 26: 172–6PubMedGoogle Scholar
  133. 133.
    Bethea CL, Pecins-Thompson M, Schutzer WE, et al. Ovarian steroids and serotonin neural function. Mol Neurobiol 1998; 18: 87–123PubMedCrossRefGoogle Scholar
  134. 134.
    Riley JL, Robinson ME, Wise EA, et al. A meta-analytic review of pain perception across the menstrual cycle. Pain 1999; 81: 225–35PubMedCrossRefGoogle Scholar
  135. 135.
    Martinez-Gomez M, Cruz Y, Salas M, et al. Assessing pain thresholds in the rat: changes with estrus and time of day. Physiol Behav 1994; 55: 651–7PubMedCrossRefGoogle Scholar
  136. 136.
    Rao SS, Ranganekar AG, Saifi AQ. Pain thresholds in relation to sex hormones. Indian J Physiol Pharmacol 1987; 31: 250–4PubMedGoogle Scholar
  137. 137.
    Thomas VN. Pain: its nature and management. London: Bailliere Tindall, 1997Google Scholar
  138. 138.
    Macintyre PE, Ready LB. Acute pain management: a practical guide. London: WB Saunders Co. LTD, 1996Google Scholar
  139. 139.
    Gintzler AR. Endorphin-mediated increase in pain threshold during pregnancy. Science 1980; 210: 193–5PubMedCrossRefGoogle Scholar
  140. 140.
    Kristal MB, Thompson AC, Abbott P, et al. Amniotic-fluid ingestion by parturient rats enhances pregnancy-mediated analgesia. Life Sci 1990; 46: 693–8PubMedCrossRefGoogle Scholar
  141. 141.
    Iwasaki H, Collins JG, Saito Y, et al. Naloxene-sensitive pregnancy-induced changes in behavioural responses to colorectal distension: pregnancy-induced analgesia to visceral stimulation. Anesthesiology 1991; 74: 927–33PubMedCrossRefGoogle Scholar
  142. 142.
    Cogan R, Spinnato JA. Pain and discomfort thresholds in late pregnancy. Pain 1986; 27: 63–8PubMedCrossRefGoogle Scholar
  143. 143.
    Whipple B, Josimovich JB, Komisaruk BR. Sensory threshold during the antepartum, intrapartum, and postpartum periods. Int J Nurs Stud 1990; 27: 213–21PubMedCrossRefGoogle Scholar
  144. 144.
    Gintzler AR, Bohan MC. Pain thresholds are elevated during pseudopregnancy. Brain Res 1990; 507: 312–6PubMedCrossRefGoogle Scholar
  145. 145.
    Dawson-Basoa ME, Gintzler AR. Estrogen and progesterone activate spinal kappa-opiate receptor analgesic mechanisms. Pain 1996; 64: 607–15CrossRefGoogle Scholar
  146. 146.
    Dawson-Basoa ME, Gintzler AR. Gestational and ovarian sex steroids antinociception: synergy between spinal κ and δ opioid systems. Brain Res 1998; 794: 61–7PubMedCrossRefGoogle Scholar
  147. 147.
    Liu N, Gintzler AA. Prolonged ovarian sex steroid treatment of male rats produces antinociception: identification of sex based divergent analgesic mechanisms. Pain 2000; 85: 273–81PubMedCrossRefGoogle Scholar
  148. 148.
    Gordon FT, Solimon MRI. The effects of estradiol and progesterone on pain sensitivity and brain opioid receptors in ovariectomized rats. Horm Behav 1996; 30: 244–50PubMedCrossRefGoogle Scholar
  149. 149.
    Dina OA, Aley KO, Isenberg W, et al. Sex hormones regulate the contribution of PKC and PKA signalling in inflammatory pain in the rat. Eur J Neuro Sci 2001; 13: 2227–33CrossRefGoogle Scholar
  150. 150.
    Amandusson A, Hallbeck M, Hallbeck AL, et al. Estrogen-induced alterations of spinal cord enkaphalin gene expression. Pain 1999; 83: 243–8PubMedCrossRefGoogle Scholar
  151. 151.
    Amandusson A, Blomqvist A. Estrogen receptors can regulate pain sensitivity. Lakartidningen 2001; 15: 1774–8Google Scholar
  152. 152.
    Phillips SK, Rook KM, Siddle NC, et al. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci 1993; 84: 95–8PubMedGoogle Scholar
  153. 153.
    Naessen T, Linmark B, Larsen HC. Better postural balance in elderly women receiving estrogens. Am J Obstet Gynecol 1997; 177: 412–6PubMedCrossRefGoogle Scholar
  154. 154.
    Seeley DG, Cauley JA, Grady D, et al. Is postmenopausal estrogen therapy associated with neuromuscular function or falling in elderly women?. Study of osteoporotic fractures research group. Arch Int Med 1995; 155: 293–9CrossRefGoogle Scholar
  155. 155.
    Taaffe DR, Luz Villa M, Delay R, et al. Maximal muscle strength of elderly women is not influenced by oestrogen status. Age Ageing 1995; 24: 329–33PubMedCrossRefGoogle Scholar
  156. 156.
    Armstrong AL, Oborne J, Coupland CA, et al. Effects of hormone replacement therapy on muscle performance and balance in post-menopausal women. Clin Sci 1996; 91: 685–90PubMedGoogle Scholar
  157. 157.
    Brooke-Wavell K, Prelevic GM, Bakridan C, et al. Effects of physical activity and menopausal hormone replacement therapy on postural stability in postmenopausal women: a cross sectional study. Maturitas 2001; 37 (3): 167–72PubMedCrossRefGoogle Scholar

Copyright information

© Adis International Limited 2002

Authors and Affiliations

  1. 1.School of Sport, Health and Exercise SciencesUniversity of WalesBangorUK

Personalised recommendations