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Sports Medicine

, Volume 45, Issue 3, pp 379–409 | Cite as

Alterations in Redox Homeostasis in the Elite Endurance Athlete

  • Nathan A. Lewis
  • Glyn Howatson
  • Katie Morton
  • Jessica Hill
  • Charles R. Pedlar
Systematic Review

Abstract

Background

The production of reactive oxygen (ROS) and nitrogen species (RNS) is a fundamental feature of mammalian physiology, cellular respiration and cell signalling, and essential for muscle function and training adaptation. Aerobic and anaerobic exercise results in alterations in redox homeostasis (ARH) in untrained, trained and well trained athletes. Low to moderate doses of ROS and RNS play a role in muscle adaptation to endurance training, but an overwhelming increase in RNS and ROS may lead to increased cell apoptosis and immunosuppression, fatigued states and underperformance.

Objectives

The objectives of this systematic review are: (a) to test the hypotheses that ARH occur in elite endurance athletes; following an acute exercise bout, in an endurance race or competition; across a micro-, meso- or macro-training cycle; following a training taper; before, during and after altitude training; in females with amenorrhoea versus eumenorrhoea; and in non-functional over-reaching (NFOR) and overtraining states (OTS); (b) to report any relationship between ARH and training load and ARH and performance; and (c) to apply critical difference values for measures of oxidative stress/ARH to address whether there is any evidence of ARH being of physiological significance (not just statistical) and thus relevant to health and performance in the elite athlete.

Methods

Electronic databases, Embase, MEDLINE, and SPORTDiscus were searched for relevant articles. Only studies that were observational articles of cross-sectional or longitudinal design, and included elite athletes competing at national or international level in endurance sports were included. Studies had to include biomarkers of ARH; oxidative damage, antioxidant enzymes, antioxidant capacity, and antioxidant vitamins and nutrients in urine, serum, plasma, whole blood, red blood cells (RBCs) and white blood cells (WBCs). A total of 3,057 articles were identified from the electronic searches. Twenty-eight articles met the inclusion criteria and were included in the review.

Results

ARH occurs in elite endurance athletes, after acute exercise, a competition or race, across training phases, and with natural or simulated altitude. A reduction in ARH occurs across the season in elite athletes, with marked variation around intensified training phases, between individuals, and the greatest disturbances (of physiological significance) occurring with live-high-train-low techniques, and in athletes competing. A relationship with ARH and performance and illness exists in elite athletes. There was considerable heterogeneity across the studies for the biomarkers and assays used; the sport; the blood sampling time points; and the phase in the annual training cycle and thus baseline athlete fitness. In addition, there was a consistent lack of reporting of the analytical variability of the assays used to assess ARH.

Conclusions

The reported biochemical changes around ARH in elite athletes suggest that it may be of value to monitor biomarkers of ARH at rest, pre- and post-simulated performance tests, and before and after training micro- and meso-cycles, and altitude camps, to identify individual tolerance to training loads, potentially allowing the prevention of non-functionally over-reached states and optimisation of the individual training taper and training programme.

Keywords

Total Antioxidant Capacity Trolox Equivalent Antioxidant Capacity Elite Athlete Endurance Athlete Hypobaric Hypoxia 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

No sources of funding were used to assist in the preparation of this review. The authors have no potential conflicts of interest that are directly relevant to the content of this review.

References

  1. 1.
    Sies H. What is oxidative Stress? Developments in cardiovascular medicine. Boston: Springer; 2000. p. 8.Google Scholar
  2. 2.
    Jones DP. Redefining oxidative stress. Antioxid Redox Signal. 2006;8:1865–79.PubMedGoogle Scholar
  3. 3.
    Powers SK, Duarte J, Kavazis AN, et al. Reactive oxygen species are signalling molecules for skeletal muscle adaptation. Exp Physiol. 2010;95:1–9.PubMedCentralPubMedGoogle Scholar
  4. 4.
    Nikolaidis MG, Kyparos A, Spanou C, et al. Redox biology of exercise: an integrative and comparative consideration of some overlooked issues. J Exp Biol. 2012;215:1615–25.PubMedGoogle Scholar
  5. 5.
    Reid MB. Plasticity in skeletal, cardiac, and smooth muscle. Invited Review: Redox modulation of skeletal muscle contraction: what we know and what we don’t. J Appl Physiol. 2001;90:724–31.PubMedGoogle Scholar
  6. 6.
    Gomez-Cabrera M-C, Domenech E, Romagnoli M, et al. Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr. 2008;87:142–9.PubMedGoogle Scholar
  7. 7.
    Katz A. Modulation of glucose transport in skeletal muscle by reactive oxygen species. J Appl Physiol. 2006;102:1671–6.PubMedGoogle Scholar
  8. 8.
    Ristow M, Zarse K, Oberbach A, et al. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci. 2009;106:8665–70.PubMedCentralPubMedGoogle Scholar
  9. 9.
    Handayaningsih A-E, Iguchi G, Fukuoka H, et al. Reactive oxygen species play an essential role in IGF-I signaling and IGF-I-induced myocyte hypertrophy in C2C12 myocytes. Endocrinology. 2011;152:912–21.PubMedGoogle Scholar
  10. 10.
    Richardson RS, Donato AJ, Uberoi A, et al. Exercise-induced brachial artery vasodilation: role of free radicals. Am J Physiol Heart Circ Physiol. 2006;292:H1516–22.PubMedGoogle Scholar
  11. 11.
    Yfanti C, Åkerström T, Nielsen S, et al. Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc. 2010;42(7):1388–95.PubMedGoogle Scholar
  12. 12.
    Yfanti C, Nielsen AR, Akerstrom T, et al. Effect of antioxidant supplementation on insulin sensitivity in response to endurance exercise training. Am J Physiol Endocrinol Metab. 2011;300:E761–70.PubMedGoogle Scholar
  13. 13.
    Roberts LA, Beattie K, Close GL, et al. Vitamin C consumption does not impair training-induced improvements in exercise performance. Int J Sports Physiol Perform. 2011;6(1):58–69.PubMedGoogle Scholar
  14. 14.
    Higashida K, Kim SH, Higuchi M, et al. Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab. 2011;301:E779–84.PubMedCentralPubMedGoogle Scholar
  15. 15.
    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;94:1714–8.PubMedGoogle Scholar
  16. 16.
    Bailey DM. Regulation of free radical outflow from an isolated muscle bed in exercising humans. Am J Physiol Heart Circ Physiol. 2004;287:H1689–99.PubMedGoogle Scholar
  17. 17.
    Bailey DM, Lawrenson L, Mceneny J, et al. Electron paramagnetic spectroscopic evidence of exercise-induced free radical accumulation in human skeletal muscle. Free Radic Res. 2007;41:182–90.PubMedGoogle Scholar
  18. 18.
    Knez WL, Jenkins DG, Coombes JS. Oxidative Stress in half and full ironman triathletes. Med Sci Sports Exerc. 2007;39:283–8.PubMedGoogle Scholar
  19. 19.
    Mastaloudis A, Leonard SW, Traber MG. Oxidative stress in athletes during extreme endurance exercise. Free Radic Biol Med. 2001;31:911–22.PubMedGoogle Scholar
  20. 20.
    Kabasakalis A, Kyparos A, Tsalis G, et al. Blood oxidative stress markers after ultramarathon swimming. J Strength Cond Res. 2011;25:805–11.PubMedGoogle Scholar
  21. 21.
    Finaud J, Lac G, Filaire E. Oxidative stress: relationship with exercise and training. Sports Med. 2006;36:327–58.PubMedGoogle Scholar
  22. 22.
    Finaud J, Scislowski V, Lac G, et al. Antioxidant status and oxidative stress in professional rugby players: evolution throughout a season. Int J Sports Med. 2006;27:87–93.PubMedGoogle Scholar
  23. 23.
    Bloomer RJ, Fisher-Wellman KH. Blood oxidative stress biomarkers: influence of sex, exercise training status, and dietary intake. Gend Med. 2008;5:218–28.PubMedGoogle Scholar
  24. 24.
    Skarpańska-Stejnborn A, Pilaczyńska-Szcześniak Ł, Basta P, et al. Changes in prooxidative–antioxidative balance in rowers following ergometric exercise test of maximal intensity. Stud Phys Cult Tour. 2009;16:361–7.Google Scholar
  25. 25.
    Kyparos A, Vrabas IS, Nikolaidis MG, et al. Increased oxidative stress blood markers in well-trained rowers following two thousand-meter rowing ergometer race. J Strength Cond Res. 2009;23:1418–26.PubMedGoogle Scholar
  26. 26.
    Knez WL, Jenkins DG, Coombes JS. The effect of an increased training volume on oxidative stress. Int J Sports Med. 2014;35(01):8–13.PubMedGoogle Scholar
  27. 27.
    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:R375–80.PubMedGoogle Scholar
  28. 28.
    Aguiló A, Tauler P, Fuentespina E, et al. Antioxidant response to oxidative stress induced by exhaustive exercise. Physiol Behav. 2005;84:1–7.PubMedGoogle Scholar
  29. 29.
    Gomez-Cabrera M-C, Domenech E, Viña J. Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med. 2008;44:126–31.PubMedGoogle Scholar
  30. 30.
    Elokda AS, Nielsen DH. Effects of exercise training on the glutathione antioxidant system. Eur J Cardiovasc Prev Rehabil. 2007;14:630–7.PubMedGoogle Scholar
  31. 31.
    Koury JC, de Olilveria AV, Portella ES, et al. Zinc and copper biochemical indices of antioxidant status in elite athletes of different modalities. Int J Sport Nutr Exerc Metab. 2004;14:358–72.PubMedGoogle Scholar
  32. 32.
    Gliemann L, Nyberg M, Hellsten Y. Nitric oxide and reactive oxygen species in limb vascular function: what is the effect of physical activity? Free Radic Res. 2014;48:71–83.PubMedGoogle Scholar
  33. 33.
    Harris MB, Mitchell BM, Sood SG, et al. Increased nitric oxide synthase activity and Hsp90 association in skeletal muscle following chronic exercise. Eur J Appl Physiol. 2008;104:795–802.PubMedGoogle Scholar
  34. 34.
    Warburton DER. Health benefits of physical activity: the evidence. Can Med Assoc J. 2006;174:801–9.Google Scholar
  35. 35.
    Nelson ME, Rejeski WJ, Blair SN, et al. Physical activity and public health in older adults: recommendation from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc. 2007;39:1435–45.PubMedGoogle Scholar
  36. 36.
    Powers SK, Talbert EE, Adhihetty PJ. Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol. 2011;589:2129–38.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Levada-Pires AC, Cury-Boaventura MF, Gorjao R, et al. Induction of lymphocyte death by short- and long-duration triathlon competitions. Med Sci Sports Exerc. 2009;41:1896–901.PubMedGoogle Scholar
  38. 38.
    Levada-Pires AC, Cury-Boaventura MF, Gorjao R, et al. Neutrophil death induced by a triathlon competition in elite athletes. Med Sci Sports Exerc. 2008;40:1447–54.PubMedGoogle Scholar
  39. 39.
    Quadrilatero J, Hoffman-Goetz L. N-acetyl-l-cysteine protects intestinal lymphocytes from apoptotic death after acute exercise in adrenalectomized mice. Am J Physiol Regul Integr Comp Physiol. 2005;288:R1664–72.PubMedGoogle Scholar
  40. 40.
    Tanskanen M, Uusitalo A, Kinnunen H, et al. Association of military training with oxidative stress and overreaching. Med Sci Sports Exerc. 2011;43:1552–60.PubMedGoogle Scholar
  41. 41.
    Margonis K, Fatouros IG, Jamurtas AZ, et al. Oxidative stress biomarkers responses to physical overtraining: implications for diagnosis. Free Radic Biol Med. 2007;43:901–10.PubMedGoogle Scholar
  42. 42.
    Tanskanen M, Atalay M, Uusitalo A. Altered oxidative stress in overtrained athletes. J Sports Sci. 2010;28:309–17.PubMedGoogle Scholar
  43. 43.
    Fearon IM, Faux SP. Oxidative stress and cardiovascular disease: novel tools give (free) radical insight. J Mol Cell Cardiol. 2009;47:372–81.PubMedGoogle Scholar
  44. 44.
    Maritim AC, Sanders RA, Watkins JB. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol. 2003;17:24–38.PubMedGoogle Scholar
  45. 45.
    Butterfield DA, Perluigi M, Sultana R. Oxidative stress in Alzheimer’s disease brain: new insights from redox proteomics. Eur J Pharmacol. 2006;545:39–50.PubMedGoogle Scholar
  46. 46.
    Beneke R, Bihn D, Hütler M, et al. Haemolysis caused by alterations of α- and β-spectrin after 10 to 35 min of severe exercise. Eur J Appl Physiol. 2005;95:307–12.PubMedGoogle Scholar
  47. 47.
    Martinovic J, Dopsaj V, Kotur-Stevuljevic J, et al. Oxidative stress status in elite female volleyball athletes with depleted iron stores. Br J Sports Med. 2011;45:534–5.Google Scholar
  48. 48.
    Hillman AR, Vince RV, Taylor L, et al. Exercise-induced dehydration with and without environmental heat stress results in increased oxidative stress. Appl Physiol Nutr Metab. 2011;36:698–706.PubMedGoogle Scholar
  49. 49.
    Pialoux V, Brugniaux JV, Rock E, et al. Antioxidant status of elite athletes remains impaired 2 weeks after a simulated altitude training camp. Eur J Nutr. 2009;49:285–92.PubMedGoogle Scholar
  50. 50.
    Marrot L, Meunier J-R. Skin DNA photodamage and its biological consequences. J Am Acad Dermatol. 2008;58:S139–48.PubMedGoogle Scholar
  51. 51.
    McAnulty SR, McAnulty L, Pascoe DD, et al. Hyperthermia increases exercise-induced oxidative stress. Int J Sports Med. 2005;26:188–92.PubMedGoogle Scholar
  52. 52.
    Watson TA, Callister R, Taylor RD, et al. Antioxidant restriction and oxidative stress in short-duration exhaustive exercise. Med Sci Sports Exerc. 2005;37:63–71.PubMedGoogle Scholar
  53. 53.
    Huang C-J, Webb HE, Evans RK, et al. Psychological stress during exercise: immunoendocrine and oxidative responses. Exp Biol Med. 2010;235:1498–504.Google Scholar
  54. 54.
    Sivoňová M, Žitňanová I, Hlinčíková L, et al. Oxidative stress in university students during examinations. Stress. 2004;7:183–8.PubMedGoogle Scholar
  55. 55.
    Schwarz KB. Oxidative stress during viral infection: a review. Free Radic Biol Med. 1996;21:641–9.PubMedGoogle Scholar
  56. 56.
    Jammes Y, Steinberg JG, Delliaux S. Chronic fatigue syndrome: acute infection and history of physical activity affect resting levels and response to exercise of plasma oxidant/antioxidant status and heat shock proteins. J Intern Med. 2012;272:74–84.PubMedGoogle Scholar
  57. 57.
    McAnulty S, McAnulty L, Nieman D, et al. Effect of NSAID on muscle injury and oxidative stress. Int J Sports Med. 2007;28:909–15.PubMedGoogle Scholar
  58. 58.
    Nikolaidis MG, Kyparos A, Dipla K, et al. Exercise as a model to study redox homeostasis in blood: the effect of protocol and sampling point. Biomarkers. 2012;17:28–35.PubMedGoogle Scholar
  59. 59.
    Nikolaidis MG, Jamurtas AZ, Paschalis V, et al. The effect of muscle-damaging exercise on blood and skeletal muscle oxidative stress. Sports Med. 2008;38:579–606.PubMedGoogle Scholar
  60. 60.
    Everson CA. Antioxidant defense responses to sleep loss and sleep recovery. Am J Physiol Regul Integr Comp Physiol. 2004;288:R374–83.PubMedGoogle Scholar
  61. 61.
    Siegel JM. Clues to the functions of mammalian sleep. Nature. 2005;437:1264–71.PubMedGoogle Scholar
  62. 62.
    Pejovic S, Basta M, Vgontzas AN, et al. Effects of recovery sleep after one work week of mild sleep restriction on interleukin-6 and cortisol secretion and daytime sleepiness and performance. Am J Physiol Endocrinol Metab. 2013;305:E890–6.PubMedCentralPubMedGoogle Scholar
  63. 63.
    Vollaard NBJ, Shearman JP, Cooper CE. Exercise-induced oxidative stress: myths, realities and physiological relevance. Sports Med. 2005;35:1045–62.PubMedGoogle Scholar
  64. 64.
    Sakellariou GK, Jackson MJ, Vasilaki A. Redefining the major contributors to superoxide production in contracting skeletal muscle. The role of NAD(P)H oxidases. Free Radic Res. 2014;48:12–29.PubMedGoogle Scholar
  65. 65.
    Fraser CG. Reference change values. Clin Chem Lab Med. 2012;50(5):807–12.Google Scholar
  66. 66.
    Davison GW, Ashton T, Mceneny J, et al. Critical difference applied to exercise-induced oxidative stress: the dilemma of distinguishing biological from statistical change. J Physiol Biochem. 2012;68:377–84.PubMedGoogle Scholar
  67. 67.
    Peternelj T-T, Coombes JS. Antioxidant supplementation during exercise training. Sports Med. 2011;41:1043–69.PubMedGoogle Scholar
  68. 68.
    Beedie CJ, Foad AJ. The placebo effect in sports performance: a brief review. Sports Med. 2009;39:313–29.PubMedGoogle Scholar
  69. 69.
    Meeusen R, Duclos M, Gleeson M, et al. Prevention, diagnosis and treatment of the overtraining syndrome. Eur J Sport Sci. 2006;6:1–14.Google Scholar
  70. 70.
    Halson SL, Lancaster G, Jeukendrup AE, et al. Immunological responses to overreaching in cyclists. Med Sci Sports Exerc. 2003;35:854–61.PubMedGoogle Scholar
  71. 71.
    ACSM. Prevention, diagnosis, and treatment of the overtraining syndrome. Med Sci Sports Exerc. 2013;45:186–205.Google Scholar
  72. 72.
    NA. The female athlete triad. Med Sci Sports Exerc. 2007;39:1867–82.Google Scholar
  73. 73.
    Wozniak A, Drewa G, Chesy G, et al. Effect of altitude training on the peroxidation and antioxidant enzymes in sportsmen. Med Sci Sports Exerc. 2001;33:1109–13.PubMedGoogle Scholar
  74. 74.
    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;234:63–9.PubMedGoogle Scholar
  75. 75.
    Pihl E, Zilmer K, Kullisaar T, et al. Atherogenic inflammatory and oxidative stress markers in relation to overweight values in male former athletes. Int J Obes Relat Metab Disord. 2005;30:141–6.Google Scholar
  76. 76.
    Pihl E, Zilmer K, Kullisaar T, et al. High-sensitive C-reactive protein level and oxidative stress-related status in former athletes in relation to traditional cardiovascular risk factors. Atherosclerosis. 2003;171:321–6.PubMedGoogle Scholar
  77. 77.
    Unt E, Zilmer K, Mägi A, et al. Homocysteine status in former top-level male athletes: possible effect of physical activity and physical fitness. Scand J Med Sci Sports. 2008;18:360–6.PubMedGoogle Scholar
  78. 78.
    Brites F, Zago V, Verona J, et al. HDL capacity to inhibit LDL oxidation in well-trained triathletes. Life Sci. 2006;78:3074–81.PubMedGoogle Scholar
  79. 79.
    Choi Y, Maeda S, Otsuki T, et al. Oxidative stress and arterial stiffness in strength- and endurance-trained athletes. Artery Res. 2010;4:52–8.Google Scholar
  80. 80.
    Conti V, Corbi G, Russomanno G, et al. Oxidative stress effects on endothelial cells treated with different athletes’ sera. Med Sci Sports Exerc. 2012;44:39–49.PubMedGoogle Scholar
  81. 81.
    Palazzetti S, Richard M-J, Favier A, et al. Overloaded training increases exercise-induced oxidative stress and damage. Can J Appl Physiol. 2003;28:588–604.PubMedGoogle Scholar
  82. 82.
    Heinicke I, Boehler A, Rechsteiner T, et al. Moderate altitude but not additional endurance training increases markers of oxidative stress in exhaled breath condensate. Eur J Appl Physiol. 2009;106:599–604.PubMedGoogle Scholar
  83. 83.
    Gonçalves MC, Bezerra FF, Eleutherio EC, et al. Organic grape juice intake improves functional capillary density and postocclusive reactive hyperemia in triathletes. Clinics. 2011;66:1537–41.PubMedCentralPubMedGoogle Scholar
  84. 84.
    Cubrilo D, Djordjevic D, Zivkovic V, et al. Oxidative stress and nitrite dynamics under maximal load in elite athletes: relation to sport type. Mol Cell Biochem. 2011;355:273–9.PubMedGoogle Scholar
  85. 85.
    Zembron-Lacny A, Szyszka K, Sobanska B, et al. Prooxidant-antioxidant equilibrium in rowers: effect of a single dose of vitamin E. J Sports Med Phys Fitness. 2006;46:257–64.PubMedGoogle Scholar
  86. 86.
    Teixeira V, Valente H, Casal S, et al. Antioxidant status, oxidative stress, and damage in elite trained kayakers and canoeists and sedentary controls. Int J Sport Nutr Exerc Metab. 2009;19:443–56.PubMedGoogle Scholar
  87. 87.
    Tian Y, Nie J, Tong TK, et al. Serum oxidant and antioxidant status during early and late recovery periods following an all-out 21-km run in trained adolescent runners. Eur J Appl Physiol. 2010;110:971–6.PubMedGoogle Scholar
  88. 88.
    Rousseau AS, Hininger I, Palazzetti S. Antioxidant vitamin status in high exposure to oxidative stress in competitive athletes. Br J Nutr. 2004;92(03):461–8.PubMedGoogle Scholar
  89. 89.
    Yan B, A J, Wang G, Lu H, et al. Metabolomic investigation into variation of endogenous metabolites in professional athletes subject to strength-endurance training. J Appl Physiol. 2008;106:531–8.PubMedGoogle Scholar
  90. 90.
    Sureda A, Córdova A, Ferrer MD, et al. l-Citrulline-malate influence over branched chain amino acid utilization during exercise. Eur J Appl Physiol. 2010;110:341–51.PubMedGoogle Scholar
  91. 91.
    Lekhi C, Gupta PH, Singh B. Influence of exercise on oxidant stress products in elite Indian cyclists. Br J Sports Med. 2007;41:691–3.PubMedCentralPubMedGoogle Scholar
  92. 92.
    McAnulty SR, McAnulty LS, Nieman DC, et al. Effect of alpha-tocopherol supplementation on plasma homocysteine and oxidative stress in highly trained athletes before and after exhaustive exercise. J Nutr Biochem. 2005;16:530–7.PubMedGoogle Scholar
  93. 93.
    Nieman DC, Henson DA, McAnulty SR, et al. Vitamin E and immunity after the kona triathlon world championship. Med Sci Sports Exerc. 2004;36:1328–35.PubMedGoogle Scholar
  94. 94.
    Knab AM, Nieman DC, Gillitt ND, et al. Effects of a flavonoid-rich juice on inflammation, oxidative stress, and immunity in elite swimmers: a metabolomics-based approach. Int J Sport Nutr Exerc Metab. 2013;23:150–60.PubMedGoogle Scholar
  95. 95.
    Margaritis I, Palazzetti S, Rousseau A-S, et al. Antioxidant supplementation and tapering exercise improve exercise-induced antioxidant response. J Am Coll Nutr. 2003;22:147–56.PubMedGoogle Scholar
  96. 96.
    Morillas-Ruiz J, Zafrilla P, Almar M, et al. The effects of an antioxidant-supplemented beverage on exercise-induced oxidative stress: results from a placebo-controlled double-blind study in cyclists. Eur J Appl Physiol. 2005;95:543–9.PubMedGoogle Scholar
  97. 97.
    Skarpanska-Stejnborn A, Pilaczynska-Szczesniak L, Basta P, et al. Effects of oral supplementation with plant superoxide dismutase extract on selected redox parameters and an inflammatory marker in a 2,000-m rowing-ergometer test. Int J Sport Nutr Exerc Metab. 2011;21:124–34.PubMedGoogle Scholar
  98. 98.
    Skarpańska-Stejnborn A, Basta P, Pilaczyńska-Szcześniak Ł, et al. Grape extract supplementation attenuates blood oxidative stress in response to acute exercise. Biol Sport. 2010;27:41–6.Google Scholar
  99. 99.
    Skarpanska-Stejnborn A, Pilaczynska-Szczesniak L, Basta P, et al. The influence of supplementation with Rhodiola rosea L. extract on selected redox parameters in professional rowers. Int J Sport Nutr Exerc Metab. 2009;19:186–99.PubMedGoogle Scholar
  100. 100.
    Skarpanska-Stejnborn A, Basta P, Pilaczyńska-Szcześniak Ł. The influence of supplementation with the black currant (Ribes nigrum) extract on selected prooxidative-antioxidative balance parameters in rowers. Stud Phys Cult Tour. 2006;13:51–8.Google Scholar
  101. 101.
    Skarpanska-Stejnborn A, Pilaczynska-Szczesniak L, Basta P, et al. The influence of supplementation with artichoke (Cynara scolymus L.) extract on selected redox parameters in rowers. Int J Sport Nutr Exerc Metab. 2008;18:313–27.PubMedGoogle Scholar
  102. 102.
    von Elm E, Altman DG, Egger M, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008;61:344–9.Google Scholar
  103. 103.
    Vandenbroucke JP. Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. Ann Intern Med. 2007;147(8):W-163.Google Scholar
  104. 104.
    Maher CG, Sherrington C, Herbert RD, Elkins M, et al. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83:713–21.PubMedGoogle Scholar
  105. 105.
    Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52:377–84.PubMedCentralPubMedGoogle Scholar
  106. 106.
    Verhagen AP, de Vet HC, de Bie RA, et al. The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol. 1998;51:1235–41.PubMedGoogle Scholar
  107. 107.
    Kyparos A, Riganas C, Nikolaidis MG, et al. The effect of exercise-induced hypoxemia on blood redox status in well-trained rowers. Eur J Appl Physiol. 2011;112:2073–83.PubMedGoogle Scholar
  108. 108.
    Pittaluga M, Parisi P, Sabatini S, et al. Cellular and biochemical parameters of exercise-induced oxidative stress: relationship with training levels. Free Radic Res. 2006;40:607–14.PubMedGoogle Scholar
  109. 109.
    Cuevas MJ, Almar M, García-Glez JC, et al. Changes in oxidative stress markers and NF-κB activation induced by sprint exercise. Free Radic Res. 2005;39:431–9.PubMedGoogle Scholar
  110. 110.
    Deminice R, Trindade CS, Degiovanni GC, et al. Oxidative stress biomarkers response to high intensity interval training and relation to performance in competitive swimmers. J Sports Med Phys Fitness. 2010;50:356–62.PubMedGoogle Scholar
  111. 111.
    Dane S, Taysi S, Gul M, et al. Acute exercise induced oxidative stress is prevented in erythrocytes of male long distance athletes. Biol Sport. 2008;25:115.Google Scholar
  112. 112.
    Ginsburg GS, O’Toole M, Rimm E, et al. Gender differences in exercise-induced changes in sex hormone levels and lipid peroxidation in athletes participating in the Hawaii Ironman triathlon. Ginsburg-gender and exercise-induced lipid peroxidation. Clin Chim Acta. 2001;305:131–9.PubMedGoogle Scholar
  113. 113.
    Corsetti R, Villa M, Pasturenzi M, et al. Redox state in professional cyclists following competitive sports activity. Open Access J Sports Med. 2012;6:34–41.Google Scholar
  114. 114.
    Cases N, Sureda A, Maestre I, et al. Response of antioxidant defences to oxidative stress induced by prolonged exercise: antioxidant enzyme gene expression in lymphocytes. Eur J Appl Physiol. 2006;98:263–9.PubMedGoogle Scholar
  115. 115.
    Mena P, Maynar M, Gutierrez JM, et al. Erythrocyte free radical scavenger enzymes in bicycle professional racers. Adaptation to training. Int J Sports Med. 1991;12:563–6.PubMedGoogle Scholar
  116. 116.
    Serrano E, Venegas C, Escames G, et al. Antioxidant defence and inflammatory response in professional road cyclists during a 4-day competition. J Sports Sci. 2010;28:1047–56.PubMedGoogle Scholar
  117. 117.
    Sureda A, Tauler P, Aguiló A, et al. Relation between oxidative stress markers and antioxidant endogenous defences during exhaustive exercise. Free Radic Res. 2005;39:1317–24.PubMedGoogle Scholar
  118. 118.
    Tauler P, Sureda A, Cases N, et al. Increased lymphocyte antioxidant defences in response to exhaustive exercise do not prevent oxidative damage. J Nutr Biochem. 2006;17:665–71.PubMedGoogle Scholar
  119. 119.
    Sureda A, Ferrer MD, Tauler P, et al. Intense physical activity enhances neutrophil antioxidant enzyme gene expression. Immunocytochemistry evidence for catalase secretion. Free Radic Res. 2007;41:874–83.PubMedGoogle Scholar
  120. 120.
    Tauler P, Ferrer MD, Romaguera D, et al. Antioxidant response and oxidative damage induced by a swimming session: Influence of gender. J Sports Sci. 2008;26:1303–11.PubMedGoogle Scholar
  121. 121.
    Almar M, Villa JG, Cuevas MJ, Rodríguez-Marroyo JA, et al. Urinary levels of 8-hydroxydeoxyguanosine as a marker of oxidative damage in road cycling. Free Radic Res. 2002;36:247–53.PubMedGoogle Scholar
  122. 122.
    Tauler P, Aguiló A, Cases N, et al. Acute phase immune response to exercise coexists with decreased neutrophil antioxidant enzyme defences. Free Radic Res. 2002;36:1101–7.PubMedGoogle Scholar
  123. 123.
    Pialoux V, Mounier R, Rock E, et al. Effects of the “live high–train low” method on prooxidant/antioxidant balance on elite athletes. Eur J Clin Nutr. 2008;63:756–62.PubMedGoogle Scholar
  124. 124.
    Pialoux V, Mounier R, Brugniaux JV, et al. Thirteen days of “live high–train low” does not affect prooxidant/antioxidant balance in elite swimmers. Eur J Appl Physiol. 2009;106:517–24.PubMedGoogle Scholar
  125. 125.
    Schippinger G, Fankhauser F, Abuja PM, et al. Competitive and seasonal oxidative stress in elite alpine ski racers. Scand J Med Sci Sports. 2008;19:206–12.PubMedGoogle Scholar
  126. 126.
    Subudhi AW, Davis SL, Kipp RW, et al. Antioxidant status and oxidative stress in elite alpine ski racers. Int J Sport Nutr Exerc Metab. 2001;11:32–41.PubMedGoogle Scholar
  127. 127.
    Medina S, Dominguez-Perles R, Cejuela-Anta R, Villano D, Martinez-Sanz JM, Gil P, et al. Assessment of oxidative stress markers and prostaglandins after chronic training of triathletes. Prostaglandins Other Lipid Mediat. 2012;99:79–86.PubMedGoogle Scholar
  128. 128.
    Valimaki IA. Low intensity training and good maximal oxygen uptake associate with decreased oxidative stress in endurance runners. Gazz Med Ital-Arch Sci Med. 2010;169:1–2.Google Scholar
  129. 129.
    Teixeira V, Valente H, Casal S, et al. Antioxidant status, oxidative stress, and damage in elite kayakers after 1 year of training and competition in 2 seasons. Appl Physiol Nutr Metab. 2009;34:716–24.PubMedGoogle Scholar
  130. 130.
    Vasankari TJ, Kujala UM, Vasankari TM, et al. Increased serum and low-density-lipoprotein antioxidant potential after antioxidant supplementation in endurance athletes. Am J Clin Nutr. 1997;65:1052–6.PubMedGoogle Scholar
  131. 131.
    Pialoux V, Mounier R, Rock E, et al. Effects of acute hypoxic exposure on prooxidant/antioxidant balance in elite endurance athletes. Int J Sports Med. 2009;30:87–93.PubMedGoogle Scholar
  132. 132.
    Fatouros IG, Jamurtas AZ, Villiotou V, et al. Oxidative stress responses in older men during endurance training and detraining. Med Sci Sports Exerc. 2004;36:2065–72.PubMedGoogle Scholar
  133. 133.
    Caimi G, Canino B, Amodeo G, et al. Lipid peroxidation and total antioxidant status in unprofessional athletes before and after a cardiopulmonary test. Clin Hemorheol Microcirc. 2009;43:235–41.PubMedGoogle Scholar
  134. 134.
    Falone S, Mirabilio A, Passerini A, et al. Aerobic performance and antioxidant protection in runners. Int J Sports Med. 2009;30:782–8.PubMedGoogle Scholar
  135. 135.
    Michailidis Y, Jamurtas AZ, Nikolaidis MG, et al. Sampling time is crucial for measurement of aerobic exercise-induced oxidative stress. Med Sci Sports Exerc. 2007;39:1107–13.PubMedGoogle Scholar
  136. 136.
    Farney TM, Mccarthy CG, Canale RE, et al. Absence of blood oxidative stress in trained men after strenuous exercise. Med Sci Sports Exerc. 2012;44:1855–63.PubMedGoogle Scholar
  137. 137.
    Bird SR, Linden M, Hawley JA. Acute changes to biomarkers as a consequence of prolonged strenuous running. Ann Clin Biochem. 2014;51:137–50.PubMedGoogle Scholar
  138. 138.
    Powers SK, Smuder AJ, Kavazis AN, et al. Experimental guidelines for studies designed to investigate the impact of antioxidant supplementation on exercise performance. Int J Sport Nutr Exerc Metab. 2010;20:2.PubMedCentralPubMedGoogle Scholar
  139. 139.
    Moore K, Roberts LJ. Measurement of lipid peroxidation. Free Radic Res. 1998;28:659–71.PubMedGoogle Scholar
  140. 140.
    Halliwell B, Whiteman M. Measuring reactive species and oxidative damage in vivoand in cell culture: how should you do it and what do the results mean? Br J Pharmacol. 2004;142:231–55.PubMedCentralPubMedGoogle Scholar
  141. 141.
    Meagher EA, FitzGerald GA. Indices of lipid peroxidation in vivo: strengths and limitations. Free Radic Biol Med. 2000;28:1745–50.PubMedGoogle Scholar
  142. 142.
    Lucia A, Hoyos J, Chicharro JL. Physiology of professional road cycling. Sports Med. 2001;31:325–37.PubMedGoogle Scholar
  143. 143.
    Horn PL, Pyne DB, Hopkins WG, et al. Lower white blood cell counts in elite athletes training for highly aerobic sports. Eur J Appl Physiol. 2010;110:925–32.PubMedGoogle Scholar
  144. 144.
    Parisotto R, Pyne D, Martin D, et al. Neutropenia in elite male cyclists. Clin J Sport Med. 2003;13:303–5.PubMedGoogle Scholar
  145. 145.
    Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med. 2000;29:323–33.PubMedGoogle Scholar
  146. 146.
    Chandra J, Orrenius S. Mitochondria, oxygen metabolism and the regulation of cell death. In: International Congress Series. vol 1233; 2002. p. 259–272.Google Scholar
  147. 147.
    Du Y, Guo H, Lou H. Grape seed polyphenols protect cardiac cells from apoptosis via induction of endogenous antioxidant enzymes. J Agric Food Chem. 2007;55:1695–701.PubMedGoogle Scholar
  148. 148.
    Vollaard NBJ, Copper CE, Shearman JP. Exercise-induced oxidative stress in overload training and tapering. Med Sci Sports Exerc. 2006;38:1335–41.PubMedGoogle Scholar
  149. 149.
    Jones AM. The physiology of the world record holder for the women’s marathon. Int J Sports Sci Coach. 2006;1:101–16.Google Scholar
  150. 150.
    Ingham SA, Fudge BW, Pringle JS. Training distribution, physiological profile, and performance for a male international 1500-m runner. Int J Sports Physiol Perform. 2012;7:193–5.PubMedGoogle Scholar
  151. 151.
    Pedlar CR, Whyte GP, Burden R, et al. A case study of an iron-deficient female Olympic 1,500-m runner. Int J Sports Physiol Perform. 2013;8:695–8.PubMedGoogle Scholar
  152. 152.
    Stellingwerf T. Case study: nutrition and training periodization in three elite marathon runners. Int J Sport Nutr Exerc Metab. 2012;22:392–400.PubMedGoogle Scholar
  153. 153.
    Stellingwerff T. Contemporary nutrition approaches to optimize elite marathon performance. Int J Sports Physiol Perform. 2013;8:573–8.PubMedGoogle Scholar
  154. 154.
    Gore CJ, Clark SA, Saunders PU. Nonhematological mechanisms of improved sea-level performance after hypoxic exposure. Med Sci Sports Exerc. 2007;39:1600–9.PubMedGoogle Scholar
  155. 155.
    Bonetti DL, Hopkins WG. Sea-level exercise performance following adaptation to hypoxia. Sports Med. 2009;39:107–27.PubMedGoogle Scholar
  156. 156.
    Lundby C, Millet GP, Calbet JA, et al. Does “altitude training” increase exercise performance in elite athletes? Br J Sports Med. 2012;46:792–5.PubMedGoogle Scholar
  157. 157.
    Kerksick C, Taylor L IV, Harvey A, et al. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc. 2008;40:1772–80.PubMedGoogle Scholar
  158. 158.
    Robach P, Schmitt L, Brugniaux JV, et al. Living high–training low: effect on erythropoiesis and aerobic performance in highly-trained swimmers. Eur J Appl Physiol. 2005;96:423–33.PubMedGoogle Scholar
  159. 159.
    Robach P, Schmitt L, Brugniaux JV, et al. Living high–training low: effect on erythropoiesis and maximal aerobic performance in elite Nordic skiers. Eur J Appl Physiol. 2006;97:695–705.PubMedGoogle Scholar
  160. 160.
    Brugniaux JV. Eighteen days of “living high, training low” stimulate erythropoiesis and enhance aerobic performance in elite middle-distance runners. J App Physiol. 2006;100:203–11.Google Scholar
  161. 161.
    Plunkett BA, Callister R, Watson TA, et al. Dietary antioxidant restriction affects the inflammatory response in athletes. Br J Nutr. 2009;103:1179–84.PubMedGoogle Scholar
  162. 162.
    VanHeest JL, Rodgers CD, Mahoney CE, et al. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc. 2014;46:156–66.PubMedGoogle Scholar
  163. 163.
    Kendall B, Eston R. Exercise-induced muscle damage and the potential protective role of estrogen. Sports Med. 2002;32:103–23.PubMedGoogle Scholar
  164. 164.
    Strehlow K. Modulation of antioxidant enzyme expression and function by estrogen. Circ Res. 2003;93:170–7.PubMedGoogle Scholar
  165. 165.
    Ayres S, Baer J, Ravi Subbiah MT. Exercised-induced increase in lipid peroxidation parameters in amenorrhelc female athletes. Fertil Steril. 1998;69:73–7.PubMedGoogle Scholar
  166. 166.
    Kanaley JA, Ji LL. Antioxidant enzyme activity during prolonged exercise in amenorrheic and eumenorrheic athletes. Metab Clin Exp. 1991;40:88–92.PubMedGoogle Scholar
  167. 167.
    Joo HM. Influence of exercise training on resting blood oxidative stress markers in young women with the different menstrual cycle status. Adv Exerc Sports Physiol. 2006;12(1):23–8.Google Scholar
  168. 168.
    Meeusen R, Nederhof E, Buyse L, Roelands B, de Schutter G, Piacentini MF. Diagnosing overtraining in athletes using the two-bout exercise protocol. Br J Sports Med. 2010;44:642–8.PubMedGoogle Scholar
  169. 169.
    Vecchiet J, Cipollone F, Falasca K, et al. Relationship between musculoskeletal symptoms and blood markers of oxidative stress in patients with chronic fatigue syndrome. Neurosci Lett. 2003;335:151–4.PubMedGoogle Scholar
  170. 170.
    Kennedy G, Spence VA, McLaren M, Hill A, Underwood C, Belch JJF. Oxidative stress levels are raised in chronic fatigue syndrome and are associated with clinical symptoms. Free Radic Biol Med. 2005;39:584–9.PubMedGoogle Scholar
  171. 171.
    Richards RS, Roberts TK, McGregor NR, et al. Blood parameters indicative of oxidative stress are associated with symptom expression in chronic fatigue syndrome. Redox Rep. 2000;5:35–41.PubMedGoogle Scholar
  172. 172.
    Jammes Y, Steinberg JG, Delliaux S, et al. Chronic fatigue syndrome combines increased exercise-induced oxidative stress and reduced cytokine and Hsp responses. J Intern Med. 2009;266:196–206.PubMedGoogle Scholar
  173. 173.
    Fulle S, Mecocci P, Fanò G, et al. Specific oxidative alterations in vastus lateralis muscle of patients with the diagnosis of chronic fatigue syndrome. Free Radic Biol Med. 2000;29:1252–9.PubMedGoogle Scholar
  174. 174.
    Robinson M, Gray SR, Watson MS, et al. Plasma IL-6, its soluble receptors and F2-isoprostanes at rest and during exercise in chronic fatigue syndrome. Scand J Med Sci Sports. 2009;20:282–90.PubMedGoogle Scholar
  175. 175.
    Bailey SJ, Winyard PG, Blackwell JR, et al. Influence of N-acetylcysteine administration on pulmonary O2 uptake kinetics and exercise tolerance in humans. Respir Physiol Neurobiol. 2011;175:121–9.PubMedGoogle Scholar
  176. 176.
    Margaritis I, Tessier F, Richard M-J, et al. No evidence of oxidative stress after a triathlon race in highly trained competitors. Int J Sports Med. 1997;18:186–90.PubMedGoogle Scholar
  177. 177.
    Davison RCR, van Someren KA, Jones AM. Physiological monitoring of the Olympic athlete. J Sports Sci. 2009;27:1433–42.PubMedGoogle Scholar
  178. 178.
    Meeusen R, Piacentini MF, Busschaert B, et al. Hormonal responses in athletes: the use of a two bout exercise protocol to detect subtle differences in (over)training status. Eur J Appl Physiol. 2004;91:140–6.PubMedGoogle Scholar
  179. 179.
    Coutts A, Wallace L, Slattery K. Monitoring changes in performance, physiology, biochemistry, and psychology during overreaching and recovery in triathletes. Int J Sports Med. 2007;28:125–34.PubMedGoogle Scholar
  180. 180.
    Uusitalo AL, Huttunen P, Hanin Y, et al. Hormonal responses to endurance training and overtraining in female athletes. Clin J Sport Med. 1998;8:178–86.PubMedGoogle Scholar
  181. 181.
    Le Meur Y, Louis J, Aubry A, Gueneron J, et al. Maximal exercise limitation in functionally overreached triathletes: role of cardiac adrenergic stimulation. J App Physiol. 2014;117:214–22.Google Scholar
  182. 182.
    Bagger M, Petersen PH, Pedersen PK. Biological variation in variables associated with exercise training. Int J Sports Med. 2003;24:433–40.PubMedGoogle Scholar
  183. 183.
    Dill DB, Costill DL. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol. 1974;37:247–8.PubMedGoogle Scholar
  184. 184.
    Fraser CG, Cummings ST, Wilkinson SP, et al. Biological variability of 26 clinical chemistry analytes in elderly people. Clin Chem. 1989;35:783–6.PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Nathan A. Lewis
    • 1
    • 2
  • Glyn Howatson
    • 3
    • 4
  • Katie Morton
    • 2
    • 5
  • Jessica Hill
    • 2
  • Charles R. Pedlar
    • 2
  1. 1.English Institute of SportBathUK
  2. 2.St Mary’s UniversityLondonUK
  3. 3.Northumbria UniversityNewcastleUK
  4. 4.Water Research GroupSchool of Environmental Sciences and Development, Northwest UniversityPotchefstroomSouth Africa
  5. 5.University of CambridgeCambridgeUK

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