Skip to main content

Advertisement

SpringerLink
Log in

Exercise-Induced Oxidative Stress

Myths, Realities and Physiological Relevance

  • Review Article
  • Published:
Sports Medicine Aims and scope Submit manuscript

Abstract

Although assays for the most popular markers of exercise-induced oxidative stress may experience methodological flaws, there is sufficient credible evidence to suggest that exercise is accompanied by an increased generation of free radicals, resulting in a measurable degree of oxidative modifications to various molecules. However, the mechanisms responsible are unclear. A common assumption that increased mitochondrial oxygen consumption leads per se to increased reactive oxygen species (ROS) production is not supported by in vitro and in vivo data. The specific contributions of other systems (xanthine oxidase, inflammation, haem protein auto-oxidation) are poorly characterised. It has been demonstrated that ROS have the capacity to contribute to the development of muscle fatigue in situ, but there is still a lack of convincing direct evidence that ROS impair exercise performance in vivo in humans. It remains unclear whether exercise-induced oxidative modifications have little significance, induce harmful oxidative damage, or are an integral part of redox regulation. It is clear that ROS play important roles in numerous physiological processes at rest; however, the detailed physiological functions of ROS in exercise remain to be elucidated.

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

Table I
Table II
Table III
Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Knight JA. Review: free radicals, antioxidants, and the immune system. Ann Clin Lab Sci 2000; 30 (2): 145–158

    PubMed  CAS  Google Scholar 

  2. Turpaev KT. Reactive oxygen species and regulation of gene expression. Biochemistry (Mosc) 2002; 67 (3): 281–292

    CAS  Google Scholar 

  3. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 2000; 279 (6): L1005–L1028

    PubMed  CAS  Google Scholar 

  4. Cooper CE. Ferryl states and protein free radicals. In: Rice-Evans CA, Burdon RH, editors. Free radical damage and its control. Amsterdam: Elsevier, 1993: 67–111

    Google Scholar 

  5. Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 1993; 57 (5 Suppl.): 715S–724S

    PubMed  CAS  Google Scholar 

  6. Golden TR, Hinerfeld DA, Melov S. Oxidative stress and aging: beyond correlation. Aging Cell 2002; 1 (2): 117–123

    PubMed  CAS  Google Scholar 

  7. Dillard CJ, Litov RE, Savin WM, et al. Effects of exercise, vitamin E, and ozone on pulmonary function and lipid peroxidation. J Appl Physiol 1978; 45 (6): 927–932

    PubMed  CAS  Google Scholar 

  8. Davies KJ, Quintanilha AT, Brooks GA, et al. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 1982; 107 (4): 1198–1205

    PubMed  CAS  Google Scholar 

  9. Ashton T, Rowlands CC, Jones E, et al. Electron spin resonance spectroscopic detection of oxygen-centred radicals in human serum following exhaustive exercise. Eur J Appl Physiol Occup Physiol 1998; 77 (6): 498–502

    PubMed  CAS  Google Scholar 

  10. Ashton T, Young IS, Peters JR, et al. Electron spin resonance spectroscopy, exercise, and oxidative stress: an ascorbic acid intervention study. J Appl Physiol 1999; 87 (6): 2032–2036

    PubMed  CAS  Google Scholar 

  11. Bailey DM, Davies B, Young IS, et al. EPR spectroscopic detection of free radical outflow from an isolated muscle bed in exercising humans. J Appl Physiol 2003; 94 (5): 1714–1718

    PubMed  CAS  Google Scholar 

  12. Bailey DM, Young IS, McEneny J, et al. Regulation of free radical outflow from an isolated muscle bed in exercising humans. Am J Physiol Heart Circ Physiol 2004; 287 (4): H1689–H1699

    PubMed  CAS  Google Scholar 

  13. Groussard C, Rannou-Bekono F, Machefer G, et al. Changes in blood lipid peroxidation markers and antioxidants after a single sprint anaerobic exercise. Eur J Appl Physiol 2003; 89 (1): 14–20

    PubMed  CAS  Google Scholar 

  14. Viinikka L, Vuori J, Ylikorkala O. Lipid peroxides, prostacyclin, and thromboxane A2 in runners during acute exercise. Med Sci Sports Exerc 1984; 16 (3): 275–277

    PubMed  CAS  Google Scholar 

  15. Maughan RJ, Donnelly AE, Gleeson M, et al. Delayed-onset muscle damage and lipid peroxidation in man after a downhill run. Muscle Nerve 1989; 12 (4): 332–336

    PubMed  CAS  Google Scholar 

  16. Duthie GG, Robertson JD, Maughan RJ, et al. Blood antioxidant status and erythrocyte lipid peroxidation following distance running. Arch Biochem Biophys 1990; 282 (1): 78–83

    PubMed  CAS  Google Scholar 

  17. Sahlin K, Ekberg K, Cizinsky S. Changes in plasma hypoxanthine and free radical markers during exercise in man. Acta Physiol Scand 1991; 142 (2): 275–281

    PubMed  CAS  Google Scholar 

  18. Hartmann A, Niess AM, Grunert-Fuchs M, et al. Vitamin E prevents exercise-induced DNA damage. Mutat Res 1995; 346 (4): 195–202

    PubMed  CAS  Google Scholar 

  19. Vasankari T, Kujala U, Heinonen O, et al. Measurement of serum lipid peroxidation during exercise using three different methods: diene conjugation, thiobarbituric acid reactive material and fluorescent chromolipids. Clin Chim Acta 1995; 234 (1–2): 63–69

    PubMed  CAS  Google Scholar 

  20. Niess AM, Hartmann A, Grunert-Fuchs M, et al. DNA damage after exhaustive treadmill running in trained and untrained men. Int J Sports Med 1996; 17 (6): 397–403

    PubMed  CAS  Google Scholar 

  21. Dufaux B, Heine O, Kothe A, et al. Blood glutathione status following distance running. Int J Sports Med 1997; 18 (2): 89–93

    PubMed  CAS  Google Scholar 

  22. Margaritis I, Tessier F, Richard MJ, et al. No evidence of oxidative stress after a triathlon race in highly trained competitors. Int J Sports Med 1997; 18 (3): 186–190

    PubMed  CAS  Google Scholar 

  23. Chung SC, Goldfarb AH, Jamurtas AZ, et al. Effect of exercise during the follicular and luteal phases on indices of oxidative stress in healthy women. Med Sci Sports Exerc 1999; 31 (3): 409–413

    PubMed  CAS  Google Scholar 

  24. Leaf DA, Kleinman MT, Hamilton M, et al. The effect of exercise intensity on lipid peroxidation. Med Sci Sports Exerc 1997; 29 (8): 1036–1039

    PubMed  CAS  Google Scholar 

  25. Surmen-Gur E, Ozturk E, Gur H, et al. Effect of vitamin E supplementation on post-exercise plasma lipid peroxidation and blood antioxidant status in smokers: with special reference to haemoconcentration effect. Eur J Appl Physiol Occup Physiol 1999; 79 (6): 472–478

    PubMed  CAS  Google Scholar 

  26. Alessio HM, Hagerman AE, Fulkerson BK, et al. Generation of reactive oxygen species after exhaustive aerobic and isometric exercise. Med Sci Sports Exerc 2000; 32 (9): 1576–1581

    PubMed  CAS  Google Scholar 

  27. Sacheck JM, Decker EA, Clarkson PM. The effect of diet on vitamin E intake and oxidative stress in response to acute exercise in female athletes. Eur J Appl Physiol 2000; 83 (1): 40–46

    PubMed  CAS  Google Scholar 

  28. Akova B, Surmen-Gur E, Gur H, et al. Exercise-induced oxidative stress and muscle performance in healthy women: role of vitamin E supplementation and endogenous oestradiol. Eur J Appl Physiol 2001; 84 (1–2): 141–147

    PubMed  CAS  Google Scholar 

  29. Quindry JC, Stone WL, King J, et al. The effects of acute exercise on neutrophils and plasma oxidative stress. Med Sci Sports Exerc 2003; 35 (7): 1139–1145

    PubMed  CAS  Google Scholar 

  30. Sacheck JM, Milbury PE, Cannon JG, et al. Effect of vitamin E and eccentric exercise on selected biomarkers of oxidative stress in young and elderly men. Free Radic Biol Med 2003; 34 (12): 1575–1588

    PubMed  CAS  Google Scholar 

  31. Ramel A, Wagner KH, Elmadfa I. Plasma antioxidants and lipid oxidation after submaximal resistance exercise in men. Eur J Nutr 2004; 43 (1): 2–6

    PubMed  CAS  Google Scholar 

  32. Lovlin R, Cottle W, Pyke I, et al. Are indices of free radical damage related to exercise intensity? Eur J Appl Physiol Occup Physiol 1987; 56 (3): 313–316

    PubMed  CAS  Google Scholar 

  33. Kretzschmar M, Muller D, Hubscher J, et al. Influence of aging, training and acute physical exercise on plasma glutathione and lipid peroxides in man. Int J Sports Med 1991; 12 (2): 218–222

    PubMed  CAS  Google Scholar 

  34. Bird RP, Draper HH. Comparative studies on different methods of malonaldehyde determination. Methods Enzymol 1984; 105: 299–305

    PubMed  CAS  Google Scholar 

  35. Lepage G, Munoz G, Champagne J, et al. Preparative steps necessary for the accurate measurement of malondialdehyde by high-performance liquid chromatography. Anal Biochem 1991; 197 (2): 277–283

    PubMed  CAS  Google Scholar 

  36. Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Oxford: University Press, 1998

    Google Scholar 

  37. Kanter MM, Lesmes GR, Kaminsky LA, et al. Serum creatine kinase and lactate dehydrogenase changes following an eighty kilometer race: relationship to lipid peroxidation. Eur J Appl Physiol Occup Physiol 1988; 57 (1): 60–63

    PubMed  CAS  Google Scholar 

  38. Kanter MM, Eddy DE. Effects of antioxidants supplementation on serum markers of lipid peroxidation and skeletal muscle damage following eccentric exercise [abstract]. Med Sci Sports Exerc 1992; 24 (5): S17

    Google Scholar 

  39. Rokitzki L, Logemann E, Sagredos AN, et al. Lipid peroxidation and antioxidative vitamins under extreme endurance stress. Acta Physiol Scand 1994; 151 (2): 149–158

    PubMed  CAS  Google Scholar 

  40. Marzatico F, Pansarasa O, Bertorelli L, et al. Blood free radical antioxidant enzymes and lipid peroxides following long-distance and lactacidemic performances in highly trained aerobic and sprint athletes. J Sports Med Phys Fitness 1997; 37 (4): 235–239

    PubMed  CAS  Google Scholar 

  41. Hessel E, Haberland A, Muller M, et al. Oxygen radical generation of neutrophils: a reason for oxidative stress during marathon running? Clin Chim Acta 2000; 298 (1–2): 145–156

    PubMed  CAS  Google Scholar 

  42. Ji LL. Antioxidant enzyme response to exercise and aging. Med Sci Sports Exerc 1993; 25 (2): 225–231

    PubMed  CAS  Google Scholar 

  43. Largilliere C, Melancon SB. Free malondialdehyde determination in human plasma by high-performance liquid chromatography. Anal Biochem 1988; 170 (1): 123–126

    PubMed  CAS  Google Scholar 

  44. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978; 52: 302–310

    PubMed  CAS  Google Scholar 

  45. Esterbauer H, Cheeseman KH. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 1990; 186: 407–421

    PubMed  CAS  Google Scholar 

  46. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978; 86 (1): 271–278

    PubMed  CAS  Google Scholar 

  47. Carbonneau MA, Peuchant E, Sess D, et al. Free and bound malondialdehyde measured as thiobarbituric acid adduct by HPLC in serum and plasma. Clin Chem 1991; 37 (8): 1423–1429

    PubMed  CAS  Google Scholar 

  48. Hong YL, Yeh SL, Chang CY, et al. Total plasma malondialdehyde levels in 16 Taiwanese college students determined by various thiobarbituric acid tests and an improved high-performance liquid chromatography-based method. Clin Biochem 2000; 33 (8): 619–625

    PubMed  CAS  Google Scholar 

  49. Maxwell SR, Jakeman P, Thomason H, et al. Changes in plasma antioxidant status during eccentric exercise and the effect of vitamin supplementation. Free Radic Res Commun 1993; 19 (3): 191–202

    PubMed  CAS  Google Scholar 

  50. Sen CK, Rankinen T, Vaisanen S, et al. Oxidative stress after human exercise: effect of N-acetylcysteine supplementation. J Appl Physiol 1994; 76 (6): 2570–2577

    PubMed  CAS  Google Scholar 

  51. Vasankari TJ, Kujala UM, Vasankari TM, et al. Effects of acute prolonged exercise on-serum and LDL oxidation and antioxidant defences. Free Radic Biol Med 1997; 22 (3): 509–513

    PubMed  CAS  Google Scholar 

  52. Alessio HM, Goldfarb AH, Cao G. Exercise-induced oxidative stress before and after vitamin C supplementation. Int J Sport Nutr 1997; 7 (1): 1–9

    PubMed  CAS  Google Scholar 

  53. Child RB, Wilkinson DM, Fallowfield JL, et al. Elevated serum antioxidant capacity and plasma malondialdehyde concentration in response to a simulated half-marathon run. Med Sci Sports Exerc 1998; 30 (11): 1603–1607

    PubMed  CAS  Google Scholar 

  54. Szczesniak L, Karolkiewicz J, Deskur E, et al. The influence of exercise-induced oxidative stress on binding and degradation of 125I-insulin by the receptors on erythrocytes. J Physiol Pharmacol 1998; 49 (3): 421–432

    PubMed  CAS  Google Scholar 

  55. Borsheim E, Knardahl S, Hostmark AT. Short-term effects of exercise on plasma very low density lipoproteins (VLDL) and fatty acids. Med Sci Sports Exerc 1999; 31 (4): 522–530

    PubMed  CAS  Google Scholar 

  56. Laaksonen DE, Atalay M, Niskanen L, et al. Blood glutathione homeostasis as a determinant of resting and exercise-induced oxidative stress in young men. Redox Rep 1999; 4 (1–2): 53–59

    PubMed  CAS  Google Scholar 

  57. Leaf DA, Kleinman MT, Hamilton M, et al. The exercise-induced oxidative stress paradox: the effects of physical exercise training. Am J Med Sci 1999; 317 (5): 295–300

    PubMed  CAS  Google Scholar 

  58. Child RB, Wilkinson DM, Fallowfield JL. Effects of a training taper on tissue damage indices, serum antioxidant capacity and half-marathon running performance. Int J Sports Med 2000; 21 (5): 325–331

    PubMed  CAS  Google Scholar 

  59. Roberts LJ, Morrow JD. Products of the isoprostane pathway: unique bioactive compounds and markers of lipid peroxidation. Cell Mol Life Sci 2002; 59 (5): 808–820

    PubMed  CAS  Google Scholar 

  60. Fam SS, Morrow JD. The isoprostanes: unique products of arachidonic acid oxidation — a review. Curr Med Chem 2003; 10 (17): 1723–1740

    PubMed  CAS  Google Scholar 

  61. Waring WS, Convery A, Mishra V, et al. Uric acid reduces exercise-induced oxidative stress in healthy adults. Clin Sci (Lond) 2003; 105 (4): 425–430

    CAS  Google Scholar 

  62. McAnulty SR, McAnulty LS, Nieman DC, et al. Influence of carbohydrate ingestion on oxidative stress and plasma antioxidant potential following a 3h run. Free Radic Res 2003; 37 (8): 835–840

    PubMed  CAS  Google Scholar 

  63. Mastaloudis A, Leonard SW, Traber MG. Oxidative stress in athletes during extreme endurance exercise. Free Radic Biol Med 2001; 31 (7): 911–922

    PubMed  CAS  Google Scholar 

  64. Mastaloudis A, Morrow JD, Hopkins DW, et al. Antioxidant supplementation prevents exercise-induced lipid peroxidation, but not inflammation, in ultramarathon runners. Free Radic Biol Med 2004; 36 (10): 1329–1341

    PubMed  CAS  Google Scholar 

  65. Nieman DC, Henson DA, McAnulty SR, et al. Influence of vitamin C supplementation on oxidative and immune changes after an ultramarathon. J Appl Physiol 2002; 92 (5): 1970–1977

    PubMed  CAS  Google Scholar 

  66. Steensberg A, Morrow J, Toft AD, et al. Prolonged exercise, lymphocyte apoptosis and F2-isoprostanes. Eur J Appl Physiol 2002; 87 (1): 38–42

    PubMed  CAS  Google Scholar 

  67. Bailey DM, Davies B, Young IS. Intermittent hypoxic training: Implications for lipid peroxidation induced by acute normoxic exercise in active men. Clin Sci (Lond) 2001; 101 (5): 465–475

    CAS  Google Scholar 

  68. Pincemail J, Camus G, Roesgen A, et al. Exercise induces pentane production and neutrophil activation in humans: effect of propranolol. Eur J Appl Physiol Occup Physiol 1990; 61 (3–4): 319–322

    PubMed  CAS  Google Scholar 

  69. Kanter MM, Nolte LA, Holloszy JO. Effects of an antioxidant vitamin mixture on lipid peroxidation at rest and postexercise. J Appl Physiol 1993; 74 (2): 965–969

    PubMed  CAS  Google Scholar 

  70. Liu ML, Bergholm R, Bergholm R, et al. A marathon run increases the susceptibility of LDL to oxidation in vitro and modifies plasma antioxidants. Am J Physiol 1999; 276: E1083–E1091

    PubMed  CAS  Google Scholar 

  71. Case D, Baer JT, Subbiah MT. The effect of prolonged exercise on lipid peroxidation in eumenorrheic female runners. Med Sci Sports Exerc 2004; 31 (10): 1390–1393

    Google Scholar 

  72. Ginsburg GS, Agil A, O’Toole M, et al. Effects of a single bout of ultraendurance exercise on lipid levels and susceptibility of lipids to peroxidation in triathletes. JAMA 1996; 276 (3): 221–225

    PubMed  CAS  Google Scholar 

  73. Viguie CA, Frei B, Shigenaga MK, et al. Antioxidant status and indexes of oxidative stress during consecutive days of exercise. J Appl Physiol 1993; 75 (2): 566–572

    PubMed  CAS  Google Scholar 

  74. Hartmann A, Pfuhler S, Dennog C, et al. Exercise-induced DNA effects in human leukocytes are not accompanied by increased formation of 8-hydroxy-2’-deoxyguanosine or induction of micronuclei. Free Radic Biol Med 1998; 24 (2): 245–251

    PubMed  CAS  Google Scholar 

  75. Nielsen HB, Hanel B, Loft S, et al. Restricted pulmonary diffusion capacity after exercise is not an ARDS-like injury. J Sports Sci 1995; 13 (2): 109–113

    PubMed  CAS  Google Scholar 

  76. Witt EH, Reznick AZ, Viguie CA, et al. Exercise, oxidative damage and effects of antioxidant manipulation. J Nutr 1992; 122 (3 Suppl.): 766–773

    PubMed  CAS  Google Scholar 

  77. Mastaloudis A, Yu TW, O’Donnell RP, et al. Endurance exercise results in DNA damage as detected by the comet assay. Free Radic Biol Med 2004; 36 (8): 966–975

    PubMed  CAS  Google Scholar 

  78. Hartmann A, Plappert U, Raddatz K, et al. Does physical activity induce DNA damage? Mutagenesis 1994; 9 (3): 269–272

    PubMed  CAS  Google Scholar 

  79. Radak Z, Ogonovszky H, Dubecz J, et al. Super-marathon race increases serum and urinary nitrotyrosine and carbonyl levels. Eur J Clin Invest 2003; 33 (8): 726–730

    PubMed  CAS  Google Scholar 

  80. Chevion S, Moran DS, Heled Y, et al. Plasma antioxidant status and cell injury after severe physical exercise. Proc Natl Acad Sci U S A 2003; 100 (9): 5119–5123

    PubMed  CAS  Google Scholar 

  81. Gohil K, Viguie C, Stanley WC, et al. Blood glutathione oxidation during human exercise. J Appl Physiol 1988; 64 (1): 115–119

    PubMed  CAS  Google Scholar 

  82. Camus G, Felekidis A, Pincemail J, et al. Blood levels of reduced/oxidized glutathione and plasma concentration of ascorbic acid during eccentric and concentric exercises of similar energy cost. Arch Int Physiol Biochim Biophys 1994; 102 (1): 67–70

    PubMed  CAS  Google Scholar 

  83. Laires MJ, Madeira F, Sergio J, et al. Preliminary study of the relationship between plasma and erythrocyte magnesium variations and some circulating pro-oxidant and antioxidant indices in a standardized physical effort. Magnes Res 1993; 6 (3): 233–238

    PubMed  CAS  Google Scholar 

  84. Lee J, Goldfarb AH, Rescino MH, et al. Eccentric exercise effect on blood oxidative-stress markers and delayed onset of muscle soreness. Med Sci Sports Exerc 2002; 34 (3): 443–448

    PubMed  CAS  Google Scholar 

  85. Rossi R, Milzani A, Dalle-Donne I, et al. Blood glutathione disulfide: in vivo factor or in vitro artifact? Clin Chem 2002; 48 (5): 742–753

    PubMed  CAS  Google Scholar 

  86. Sastre J, Asensi M, Gasco E, et al. Exhaustive physical exercise causes oxidation of glutathione status in blood: prevention by antioxidant administration. Am J Physiol 1992; 263 (5 Pt 2): R992–R995

    PubMed  CAS  Google Scholar 

  87. Vina J, Sastre J, Asensi M, et al. Assay of blood glutathione oxidation during physical exercise. Methods Enzymol 1995; 251: 237–243

    PubMed  CAS  Google Scholar 

  88. Pincemail J, Deby C, Camus G, et al. Tocopherol mobilization during intensive exercise. Eur J Appl Physiol Occup Physiol 1988; 57 (2): 189–191

    PubMed  CAS  Google Scholar 

  89. Kawai Y, Iwane H, Takanami Y. Vitamin E is mobilized in relation to lipolysis after strenuous endurance exercise [abstract]. Med Sci Sports Exerc 1994; 26 (5): S7

    Google Scholar 

  90. Kawai Y, Iwane H, Takanami Y. Mechanisms of the increase in serum vitamin E level through strenuous endurance exercise [abstract]. Med Sci Sports Exerc 1995; 27 (5): S9

    Google Scholar 

  91. Camus G, Pincemail J, Roesgen A, et al. Tocopherol mobilization during dynamic exercise after beta-adrenergic blockade. Arch Int Physiol Biochim 1990; 98 (1): 121–126

    PubMed  CAS  Google Scholar 

  92. Kawai Y, Shimomitsu T, Takanami Y, et al. Vitamin E level changes in serum and red blood cells due to acute exhaustive exercise in collegiate women. J Nutr Sci Vitaminol (Tokyo) 2000; 46 (3): 119–124

    CAS  Google Scholar 

  93. Schneider M, Niess AM, Rozario F, et al. Vitamin E supplementation does not increase the vitamin C radical concentration at rest and after exhaustive exercise in healthy male subjects. Eur J Nutr 2003; 42 (4): 195–200

    PubMed  CAS  Google Scholar 

  94. Garry PJ, Appenzeller O. Vitamins A and C and endurance races. Ann Sports Med 1983; 1: 82–84

    Google Scholar 

  95. Gleeson M, Robertson JD, Maughan RJ. Influence of exercise on ascorbic acid status in man. Clin Sci (Colch) 1987; 73 (5): 501–505

    CAS  Google Scholar 

  96. Inoue T, Mu Z, Sumikawa K, et al. Effect of physical exercise on the content of 8-hydroxydeoxyguanosine in nuclear DNA prepared from human lymphocytes. Jpn J Cancer Res 1993; 84 (7): 720–725

    PubMed  CAS  Google Scholar 

  97. Poulsen HE, Loft S, Vistisen K. Extreme exercise and oxidative DNA modification. J Sports Sci 1996; 14 (4): 343–346

    PubMed  CAS  Google Scholar 

  98. Koyama K, Kaya M, Ishigaki T, et al. Role of xanthine oxidase in delayed lipid peroxidation in rat liver induced by acute exhausting exercise. Eur J Appl Physiol Occup Physiol 1999; 80 (1): 28–33

    PubMed  CAS  Google Scholar 

  99. Liu J, Yeo HC, Overvik-Douki E, et al. Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 2000; 89 (1): 21–28

    PubMed  CAS  Google Scholar 

  100. Boveris A, Oshino N, Chance B. The cellular production of hydrogen peroxide. Biochem J 1972; 128 (3): 617–630

    PubMed  CAS  Google Scholar 

  101. Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochem J 1973; 134 (3): 707–716

    PubMed  CAS  Google Scholar 

  102. Herrero A, Barja G. ADP-regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism. J Bioenerg Biomembr 1997; 29 (3): 241–249

    PubMed  CAS  Google Scholar 

  103. Murphy MP, Echtay KS, Blaikie FH, et al. Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: studies using a mitochondria-targeted spin trap derived from alpha-phenyl-N-tert-butylnitrone. J Biol Chem 2003; 278 (49): 48534–48545

    PubMed  CAS  Google Scholar 

  104. Richardson RS, Leigh JS, Wagner PD, et al. Cellular pO2 as a determinant of maximal mitochondrial (2) consumption in trained human skeletal muscle. J Appl Physiol 1999; 87 (1): 325–331

    PubMed  CAS  Google Scholar 

  105. Richardson RS, Newcomer SC, Noyszewski EA. Skeletal muscle intracellular P (2) assessed by myoglobin desaturation: response to graded exercise. J Appl Physiol 2001; 91 (6): 2679–2685

    PubMed  CAS  Google Scholar 

  106. Bailey DM. What regulates exercise-induced reactive oxidant generation: mitochondrial (2) flux or PO(2)? Med Sci Sports Exerc 2001; 33 (4): 681–682

    PubMed  CAS  Google Scholar 

  107. Drahota Z, Chowdhury SK, Floryk D, et al. Glycerophosphate-dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J Bioenerg Biomembr 2002; 34: 105–113

    PubMed  CAS  Google Scholar 

  108. Miwa S, St-Pierre J, Partridge L, et al. Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Rad Biol Med 2003; 35 (8): 938–948

    PubMed  CAS  Google Scholar 

  109. MacDonald MJ, Brown LJ. Calcium activation of mitochondrial glycerol phosphate dehydrogenase restudied. Arch Biochem Biophys 1996; 326 (1): 79–84

    PubMed  CAS  Google Scholar 

  110. Rasmussen UF, Krustrup P, Bangsbo J, et al. The effect of high-intensity exhaustive exercise studied in isolated mitochondria from human skeletal muscle. Pflugers Arch 2001; 443 (2): 180–187

    PubMed  CAS  Google Scholar 

  111. Jesina P, Kholova D, Bolehovska R, et al. Glycerophosphate-dependent hydrogen peroxide production by rat liver mitochondria. Physiol Res 2004; 53 (3): 305–310

    PubMed  CAS  Google Scholar 

  112. Packer L. Oxidants, antioxidant nutrients and the athlete. J Sports Sci 1997; 15 (3): 353–363

    PubMed  CAS  Google Scholar 

  113. Roy RS, McCord JM. Superoxide and ischemia: conversion of xanthine dehydrogenase to xanthine oxidase. In: Greenvald R, Cohen G, editors. Oxy radicals and their scavenger systems. New York: Elsevier Science Publishing, 1983: 145–153

    Google Scholar 

  114. Volek JS, Kraemer WJ, Rubin MR, et al. L-carnitine L-tartrate supplementation favorably affects markers of recovery from exercise stress. Am J Physiol Endocrinol Metab 2002; 282 (2): E474–E482

    PubMed  CAS  Google Scholar 

  115. Hellsten Y, Hansson HA, Johnson L, et al. Increased expression of xanthine oxidase and insulin-like growth factor I (IGF-I) immunoreactivity in skeletal muscle after strenuous exercise in humans. Acta Physiol Scand 1996; 157 (2): 191–197

    PubMed  CAS  Google Scholar 

  116. Hellsten Y, Frandsen U, Orthenblad N, et al. Xanthine oxidase in human skeletal muscle following eccentric exercise: a role in inflammation. J Physiol 1997; 498 (Pt 1): 239–248

    PubMed  CAS  Google Scholar 

  117. Xia Y, Zweier JL. Substrate control of free radical generation from xanthine oxidase in the postischemic heart. J Biol Chem 1995; 270 (32): 18797–18803

    PubMed  CAS  Google Scholar 

  118. Bangsbo J, Sjodin B, Hellsten-Westing Y. Exchange of hypoxanthine in muscle during intense exercise in man. Acta Physiol Scand 1992; 146 (4): 549–550

    PubMed  CAS  Google Scholar 

  119. Hellsten-Westing Y, Kaijser L, Ekblom B, et al. Exchange of purines in human liver and skeletal muscle with short-term exhaustive exercise. Am J Physiol 1994; 266 (1 Pt 2): R81–R86

    PubMed  CAS  Google Scholar 

  120. Hellsten Y, Ahlborg G, Jensen-Urstad M, et al. Indication of in vivo xanthine oxidase activity in human skeletal muscle during exercise. Acta Physiol Scand 1988; 134 (1): 159–160

    PubMed  CAS  Google Scholar 

  121. Vina J, Gimeno A, Sastre J, et al. Mechanism of free radical production in exhaustive exercise in humans and rats; role of xanthine oxidase and protection by allopurinol. IUBMB Life 2000; 49 (6): 539–544

    PubMed  CAS  Google Scholar 

  122. Heunks LM, Vina J, van Herwaarden CL, et al. Xanthine oxidase is involved in exercise-induced oxidative stress in chronic obstructive pulmonary disease. Am J Physiol 1999; 277 (6 Pt 2): R1697–R1704

    PubMed  CAS  Google Scholar 

  123. Pyne DB. Exercise-induced muscle damage and inflammation: a review. Aust J Sci Med Sport 1994; 26 (3–4): 49–58

    PubMed  CAS  Google Scholar 

  124. Morozov VI, Pryatkin SA, Kalinski MI, et al. Effect of exercise to exhaustion on myeloperoxidase and lysozyme release from blood neutrophils. Eur J Appl Physiol 2003; 89 (3–4): 257–262

    PubMed  CAS  Google Scholar 

  125. Yamada M, Suzuki K, Kudo S, et al. Effect of exhaustive exercise on human neutrophils in athletes. Luminescence 2000; 15 (1): 15–20

    PubMed  CAS  Google Scholar 

  126. Suzuki K, Nakaji S, Yamada M, et al. Impact of a competitive marathon race on systemic cytokine and neutrophil responses. Med Sci Sports Exerc 2003; 35 (2): 348–355

    PubMed  CAS  Google Scholar 

  127. Suzuki K, Sato H, Kikuchi T, et al. Capacity of circulating neutrophils to produce reactive oxygen species after exhaustive exercise. J Appl Physiol 1996; 81 (3): 1213–1222

    PubMed  CAS  Google Scholar 

  128. Bury TB, Pirnay F. Effect of prolonged exercise on neutrophil myeloperoxidase secretion. Int J Sports Med 1995; 16 (6): 410–412

    PubMed  CAS  Google Scholar 

  129. Camus G, Pincemail J, Ledent M, et al. Plasma levels of polymorphonuclear elastase and myeloperoxidase after uphill walking and downhill running at similar energy cost. Int J Sports Med 1992; 13 (6): 443–446

    PubMed  CAS  Google Scholar 

  130. Wetzstein CJ, Shern-Brewer RA, Santanam N, et al. Does acute exercise affect the susceptibility of low density lipoprotein to oxidation? Free Radic Biol Med 1998; 24 (4): 679–682

    PubMed  CAS  Google Scholar 

  131. Niess AM, Sommer M, Schlotz E, et al. Expression of the inducible nitric oxide synthase (iNOS) in human leukocytes: responses to running exercise. Med Sci Sports Exerc 2000; 32 (7): 1220–1225

    PubMed  CAS  Google Scholar 

  132. Childs A, Jacobs C, Kaminski T, et al. Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after an acute muscle injury induced by eccentric exercise. Free Radic Biol Med 2001; 31 (6): 745–753

    PubMed  CAS  Google Scholar 

  133. Cooper CE, Vollaard NB, Choueiri T, et al. Exercise, free radicals and oxidative stress. Biochem Soc Trans 2002; 30 (2): 280–284

    PubMed  CAS  Google Scholar 

  134. Emerit J, Beaumont C, Trivin F. Iron metabolism, free radicals, and oxidative injury. Biomed Pharmacother 2001; 55 (6): 333–339

    PubMed  CAS  Google Scholar 

  135. Gibson JF, Ingram DJ, Perutz MF. Orientation of the four haem groups in haemoglobin. Nature 1956; 178 (4539): 906–908

    PubMed  CAS  Google Scholar 

  136. Svistunenko DA, Patel RP, Voloshchenko SV, et al. The globin-based free radical of ferryl hemoglobin is detected in normal human blood. J Biol Chem 1997; 272 (11): 7114–7121

    PubMed  CAS  Google Scholar 

  137. Balagopalakrishna C, Manoharan PT, Abugo OO, et al. Production of superoxide from hemoglobin-bound oxygen under hypoxic conditions. Biochemistry 1996; 35 (20): 6393–6398

    PubMed  CAS  Google Scholar 

  138. Vollaard NBJ, Reeder BJ, Shearman JP, et al. A new sensitive assay reveals that hemoglobin is oxidatively modified in vivo. Free Radic Biol Med 2005; 39 (9): 1216–1228

    PubMed  CAS  Google Scholar 

  139. Kanter M. Free radicals, exercise and antioxidant supplementation. Proc Nutr Soc 1998; 57 (1): 9–13

    PubMed  CAS  Google Scholar 

  140. Elosua R, Molina L, Fito M, et al. Response of oxidative stress biomarkers to a 16-week aerobic physical activity program, and to acute physical activity, in healthy young men and women. Atherosclerosis 2003; 167 (2): 327–334

    PubMed  CAS  Google Scholar 

  141. Criswell D, Powers S, Dodd S, et al. High intensity training-induced changes in skeletal muscle antioxidant enzyme activity. Med Sci Sports Exerc 1993; 25 (10): 1135–1140

    PubMed  CAS  Google Scholar 

  142. Higuchi M, Cartier LJ, Chen M, et al. Superoxide dismutase and catalase in skeletal muscle: adaptive response to exercise. J Gerontol 1985; 40 (3): 281–286

    PubMed  CAS  Google Scholar 

  143. Leeuwenburgh C, Fiebig R, Chandwaney R, et al. Aging and exercise training in skeletal muscle: responses of glutathione and antioxidant enzyme systems. Am J Physiol 1994; 267 (2 Pt 2): R439–R445

    PubMed  CAS  Google Scholar 

  144. Powers SK, Criswell D, Lawler J, et al. Influence of exercise and fiber type on antioxidant enzyme activity in rat skeletal muscle. Am J Physiol 1994; 266 (2 Pt 2): R375–R380

    PubMed  CAS  Google Scholar 

  145. Powers SK, Lawler J, Criswell D, et al. Aging and respiratory muscle metabolic plasticity: effects of endurance training. J Appl Physiol 1992; 72 (3): 1068–1073

    PubMed  CAS  Google Scholar 

  146. Oh-ishi S, Kizaki T, Nagasawa J, et al. Effects of endurance training on superoxide dismutase activity, content and mRNA expression in rat muscle. Clin Exp Pharmacol Physiol 1997; 24 (5): 326–332

    PubMed  CAS  Google Scholar 

  147. Oh-ishi S, Kizaki T, Ookawara T, et al. Endurance training improves the resistance of rat diaphragm to exercise-induced oxidative stress. Am J Respir Crit Care Med 1997; 156 (5): 1579–1585

    PubMed  CAS  Google Scholar 

  148. Somani SM, Husain K. Exercise training alters kinetics of antioxidant enzymes in rat tissues. Biochem Mol Biol Int 1996; 38 (3): 587–595

    PubMed  CAS  Google Scholar 

  149. Halliwell B. Free radicals, proteins and DNA: oxidative damage versus redox regulation. Biochem Soc Trans 1996; 24 (4): 1023–1027

    PubMed  CAS  Google Scholar 

  150. Evelson P, Travacio M, Repetto M, et al. Evaluation of total reactive antioxidant potential (TRAP) of tissue homogenates and their cytosols. Arch Biochem Biophys 2001; 388 (2): 261–266

    PubMed  CAS  Google Scholar 

  151. Di Meo S, Venditti P, De Leo T. Tissue protection against oxidative stress. Experientia 1996; 52 (8): 786–794

    Google Scholar 

  152. Cao G, Giovanoni M, Prior RL. Antioxidant capacity in different tissues of young and old rats. Proc Soc Exp Biol Med 1996; 211 (4): 359–365

    PubMed  CAS  Google Scholar 

  153. Xu KY, Zweier JL, Becker LC. Hydroxyl radical inhibits sarcoplasmic reticulum C (2+)-ATPase function by direct attack on the ATP binding site. Circ Res 1997; 80 (1): 76–81

    PubMed  CAS  Google Scholar 

  154. Morris TE, Sulakhe PV. Sarcoplasmic reticulum C (2+)-pump dysfunction in rat cardiomyocytes briefly exposed to hydroxyl radicals. Free Radic Biol Med 1997; 22 (1-2): 37–47

    PubMed  CAS  Google Scholar 

  155. Scherer NM, Deamer DW. Oxidation of thiols in the Ca2+-ATPase of sarcoplasmic reticulum microsomes. Biochim Biophys Acta 1986; 862 (2): 309–317

    PubMed  CAS  Google Scholar 

  156. Scherer NM, Deamer DW. Oxidative stress impairs the function of sarcoplasmic reticulum by oxidation of sulfhydryl groups in the Ca2+-ATPase. Arch Biochem Biophys 1986; 246 (2): 589–601

    PubMed  CAS  Google Scholar 

  157. Lawler JM, Hu Z, Barnes WS. Effect of reactive oxygen species on K+ contractures in the rat diaphragm. J Appl Physiol 1998; 84 (3): 948–953

    PubMed  CAS  Google Scholar 

  158. Sen CK, Kolosova I, Hanninen O, et al. Inward potassium transport systems in skeletal muscle derived cells are highly sensitive to oxidant exposure. Free Radic Biol Med 1995; 18 (4): 795–800

    PubMed  CAS  Google Scholar 

  159. Haycock JW, Jones P, Harris JB, et al. Differential susceptibility of human skeletal muscle proteins to free radical induced oxidative damage: a histochemical, immunocytochemical and electron microscopical study in vitro. Acta Neuropathol (Berl) 1996; 92 (4): 331–340

    CAS  Google Scholar 

  160. Lamb GD, Posterino GS. Effects of oxidation and reduction on contractile function in skeletal muscle fibres of the rat. J Physiol 2003; 546 (Pt 1): 149–163

    PubMed  CAS  Google Scholar 

  161. Oba T, Koshita M, Yamaguchi M. H2O2 modulates twitch tension and increases Po of Ca2+ release channel in frog skeletal muscle. Am J Physiol 1996; 271 (3 Pt 1): C810–C818

    PubMed  CAS  Google Scholar 

  162. Reid MB, Khawli FA, Moody MR. Reactive oxygen in skeletal muscle III: contractility of unfatigued muscle. J Appl Physiol 1993; 75 (3): 1081–1087

    PubMed  CAS  Google Scholar 

  163. Barclay JK, Hansel M. Free radicals may contribute to oxidative skeletal muscle fatigue. Can J Physiol Pharmacol 1991; 69 (2): 279–284

    PubMed  CAS  Google Scholar 

  164. Andrade FH, Reid MB, Allen DG, et al. Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol 1998; 509: 565–575

    PubMed  CAS  Google Scholar 

  165. Reid MB. Invited review: redox modulation of skeletal muscle contraction: what we know and what we don’t. J Appl Physiol 2001; 90 (2): 724–731

    PubMed  CAS  Google Scholar 

  166. Novelli GP, Bracciotti G, Falsini S. Spin-trappers and vitamin E prolong endurance to muscle fatigue in mice. Free Radic Biol Med 1990; 8 (1): 9–13

    PubMed  CAS  Google Scholar 

  167. Novelli GP, Falsini S, Bracciotti G. Exogenous glutathione increases endurance to muscle effort in mice. Pharmacol Res 1991; 23 (2): 149–155

    PubMed  CAS  Google Scholar 

  168. Leeuwenburgh C, Ji LL. Glutathone and glutathione ethyl ester supplementation of mice alter glutathione homeostasis during exercise. J Nutr 1998; 128 (12): 2420–2426

    PubMed  CAS  Google Scholar 

  169. Travaline MJ, Sudarshan S, Roy BG, et al. Effect of N-acetylcysteine on human diaphragm strength and fatigability. Am J Respir Crit Care Med 1997; 156 (5): 1567–1571

    PubMed  CAS  Google Scholar 

  170. Reid MB, Stokic DS, Koch SM, et al. N-acetylcysteine inhibits muscle fatigue in humans. J Clin Invest 1994; 94 (6): 2468–2474

    PubMed  CAS  Google Scholar 

  171. Medved I, Brown MJ, Bjorksten AR, et al. N-acetylcysteine infusion alters blood redox status but not time to fatigue during intense exercise in humans. J Appl Physiol 2003; 94 (4): 1572–1582

    PubMed  CAS  Google Scholar 

  172. Medved I, Brown MJ, Bjorksten AR, et al. Effects of intravenous N-acetylcysteine infusion on time to fatigue and potassium regulation during prolonged exercise. J Appl Physiol 2003; 96 (1): 211–217

    PubMed  Google Scholar 

  173. Shephard RJ, Campbell R, Pimm P, et al. Vitamin E, exercise, and the recovery from physical activity. Eur J Appl Physiol Occup Physiol 1974; 33 (2): 119–126

    PubMed  CAS  Google Scholar 

  174. Watt T, Romet TT, McFarlane I, et al. Vitamin E and oxygen consumption [letter]. Lancet 1974; II (7876): 354–355

    Google Scholar 

  175. Lawrence JD, Bower RC, Riehl WP, et al. Effects of alpha-tocopherol acetate on the swimming endurance of trained swimmers. Am J Clin Nutr 1975; 28 (3): 205–208

    PubMed  CAS  Google Scholar 

  176. Sharman IM, Down MG, Norgan NG. The effects of vitamin E on physiological function and athletic performance of trained swimmers. J Sports Med Phys Fitness 1976; 16 (3): 215–225

    PubMed  CAS  Google Scholar 

  177. Braun B, Clarkson PM, Freedson PS, et al. Effects of coenzyme Q10 supplementation on exercise performance, VO2max, and lipid peroxidation in trained cyclists. Int J Sport Nutr 1991; 1 (4): 353–365

    PubMed  CAS  Google Scholar 

  178. Snider IP, Bazzarre TL, Murdoch SD, et al. Effects of coenzyme athletic performance system as an ergogenic aid on endurance performance to exhaustion. Int J Sport Nutr 1992; 2 (3): 272–286

    PubMed  CAS  Google Scholar 

  179. Rokitzki L, Logemann E, Huber G, et al. Alpha-tocopherol supplementation in racing cyclists during extreme endurance training. Int J Sport Nutr 1994; 4 (3): 253–264

    PubMed  CAS  Google Scholar 

  180. Laaksonen R, Fogelholm M, Himberg JJ, et al. Ubiquinone supplementation and exercise capacity in trained young and older men. Eur J Appl Physiol Occup Physiol 1995; 72 (1–2): 95–100

    PubMed  CAS  Google Scholar 

  181. Malm C, Svensson M, Ekblom B, et al. Effects of ubiquinone-10 supplementation and high intensity training on physical performance in humans. Acta Physiol Scand 1997; 161 (3): 379–384

    PubMed  CAS  Google Scholar 

  182. Weston SB, Zhou S, Weatherby RP, et al. Does exogenous coenzyme Q10 affect aerobic capacity in endurance athletes? Int J Sport Nutr 1997; 7 (3): 197–206

    PubMed  CAS  Google Scholar 

  183. Itoh H, Ohkuwa T, Yamazaki Y, et al. Vitamin E supplementation attenuates leakage of enzymes following 6 successive days of running training. Int J Sports Med 2000; 21 (5): 369–374

    PubMed  CAS  Google Scholar 

  184. Patwell DM, Jackson MJ. Contraction-induced oxidants as mediators of adaptation and damage in skeletal muscle. Exerc Sport Sci Rev 2004; 32 (1): 14–18

    Google Scholar 

  185. Jackson MJ. Free radicals in skin and muscle: damaging agents or signals for adaptation? Proc Nutr Soc 1999; 58 (3): 673–676

    PubMed  CAS  Google Scholar 

  186. Iwai K, Drake SK, Wehr NB, et al. Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein 2: implications for degradation of oxidized proteins. Proc Natl Acad Sci U S A 1998; 95 (9): 4924–4928

    PubMed  CAS  Google Scholar 

  187. Kang DK, Jeong J, Drake SK, et al. Iron regulatory protein 2 as iron sensor: iron-dependent oxidative modification of cysteine. J Biol Chem 2003; 278 (17): 14857–14864

    PubMed  CAS  Google Scholar 

  188. Zhu H, Bunn HF. Signal transduction: how do cells sense oxygen? Science 2001; 292 (5516): 449–451

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Niels B.J. Vollaard is grateful for a studentship provided by the Department of Biological Sciences, University of Essex, Essex, UK. The authors have no conflicts of interest that are directly relevant to the content of this review.

Author information

Authors and Affiliations

  1. School of Life Sciences, Heriot-Watt University, Riccarton, Edinburgh, EH14 4AS, UK

    Niels B. J. Vollaard

  2. Department of Biological Sciences, University of Essex, Essex, UK

    Jerry P. Shearman & Chris E. Cooper

Authors
  1. Niels B. J. Vollaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jerry P. Shearman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris E. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Niels B. J. Vollaard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vollaard, N.B.J., Shearman, J.P. & Cooper, C.E. Exercise-Induced Oxidative Stress. Sports Med 35, 1045–1062 (2005). https://doi.org/10.2165/00007256-200535120-00004

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2165/00007256-200535120-00004

Keywords

Search

Navigation