Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Effects of exercise and training in hypoxia on antioxidant/pro-oxidant balance

Abstract

Objective:

The aim was to investigate the effects of acute exercise under hypoxic condition and the repetition of such exercise in a ‘living low-training high’ training on the antioxidant/prooxidant balance.

Design:

Randomized, repeated measures design.

Setting:

Faculté de Médecine, Clermont-Ferrand, France.

Subjects:

Fourteen runners were randomly divided into two groups. A 6-week endurance training protocol integrated two running sessions per week at the second ventilatory threshold into the usual training.

Intervention:

A 6-week endurance training protocol integrated two running sessions per week at the second ventilatory threshold into the usual training. The first hypoxic group (HG, n=8) carried out these sessions under hypoxia (3000 m simulated altitude) and the second normoxic group (NG, n=6) in normoxia. In control period, the runners were submitted to two incremental cycling tests performed in normoxia and under hypoxia (simulated altitude of 3000 m). Plasma levels of advanced oxidation protein products (AOPP), malondialdehydes (MDA) and lipid oxidizability, ferric-reducing antioxidant power (FRAP), lipid-soluble antioxidants (α-tocopherol and β-carotene) normalized for triacyglycerols and cholesterol were measured before and after the two incremental tests and at rest before and after training.

Results:

No significant changes of MDA and AOPP level were observed after normoxic exercise, whereas hypoxic exercise induced a 56% rise of MDA and a 44% rise of AOPP. Plasma level of MDA and arterial oxygen hemoglobin desaturations after the acute both exercises were highly correlated (r=0.73). α-Tocopherol normalized for cholesterol and triacyglycerols increased only after hypoxic exercise (10–12%, P<0.01). After training, FRAP resting values (−21%, P<0.05) and α-tocopherol/triacyglycerols ratio (−24%, P<0.05) were diminished for HG, whereas NG values remained unchanged.

Conclusions:

Intense exercise and hypoxia exposure may have a cumulative effect on oxidative stress. As a consequence, the repetition of such exercise characterizing the ‘living low-training high’ model has weakened the antioxidant capacities of the athletes.

Sponsorship:

International Olympic Committee and the Direction Régionale de la Jeunesse et des Sports de la Région Auvergne.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Alessio HM (1993). Exercise-induced oxidative stress. Med Sci Sports Exerc 25, 218–224.

    Article  CAS  Google Scholar 

  • Askew EW (2002). Work at high altitude and oxidative stress: antioxidant nutrients. Toxicology 180, 107–119.

    Article  CAS  Google Scholar 

  • Bailey DM, Davies B, Romer L, Castell L, Newsholme E, Gandy G (1998). Implications of moderate altitude training for sea-level endurance in elite distance runners. Eur J Appl Physiol Occup Physiol 78, 360–368.

    Article  CAS  Google Scholar 

  • Bailey DM, Davies B, Young IS (2001b). Intermittent hypoxic training: implications for lipid peroxidation induced by acute normoxic exercise in active men. Clin Sci (London) 101, 465–475.

    Article  CAS  Google Scholar 

  • Bailey DM, Davies B, Young IS, Hullin DA, Seddon PS (2001a). A potential role for free radical-mediated skeletal muscle soreness in the pathophysiology of acute mountain sickness. Aviat Space Environ Med 72, 513–521.

    CAS  PubMed  Google Scholar 

  • Benzie IF, Strain JJ (1996). The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay. Anal Biochem 239, 70–76.

    Article  CAS  Google Scholar 

  • Burke LM, Slater G, Broad EM, Haukka J, Modulon S, Hopkins WG (2003). Eating patterns and meal frequency of elite Australian athletes. Int J Sport Nutr Exerc Metab 13, 521–538.

    Article  Google Scholar 

  • Chao WH, Askew EW, Roberts DE, Wood SM, Perkins JB (1999). Oxidative stress in humans during work at moderate altitude. J Nutr 129, 2009–2012.

    Article  CAS  Google Scholar 

  • Clarkson PM, Thompson HS (2000). Antioxidants: what role do they play in physical activity and health? Am J Clin Nutr 72 (2 Suppl), 637–646.

    Article  Google Scholar 

  • Dernbach AR, Sherman WM, Simonsen JC, Flowers KM, Lamb DR (1993). No evidence of oxidant stress during high-intensity rowing training. J Appl Physiol 74, 2140–2145.

    Article  CAS  Google Scholar 

  • Di Massimo C, Scarpelli P, Penco M, Tozzi-Ciancarelli MG (2004). Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans. Eur J Appl Physiol 91, 406–412.

    Article  CAS  Google Scholar 

  • Dill DB, Costill DL (1974). Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37, 247–248.

    Article  CAS  Google Scholar 

  • Emonson DL, Aminuddin AH, Wight RL, Scroop GC, Gore CJ (1997). Training-induced increases in sea level VO2max and endurance are not enhanced by acute hypobaric exposure. Eur J Appl Physiol Occup Physiol 76, 8–12.

    Article  CAS  Google Scholar 

  • Hitka P, Vizek M, Wilhelm J (2003). Hypoxia and reoxygenation increase H2O2 production in rats. Exp Lung Res 29, 585–592.

    Article  CAS  Google Scholar 

  • Jefferson JA, Simoni J, Escudero E, Hurtado ME, Swenson ER, Wesson DE et al. (2004). Increased oxidative stress following acute and chronic high altitude exposure. High Alt Med Biol 5, 61–69.

    Article  CAS  Google Scholar 

  • Ji LL (1996). Exercise, oxidative stress, and antioxidants. Am J Sports Med 24, S20–24.

    Article  CAS  Google Scholar 

  • Joanny P, Steinberg J, Robach P, Richalet JP, Gortan C, Gardette B et al. (2001). Operation everest III (Comex'97): the effect of simulated sever hypobaric hypoxia on lipid peroxidation and antioxidant defence systems in human blood at rest and after maximal exercise. Resuscitation 49, 307–314.

    Article  CAS  Google Scholar 

  • Kanter MM (1994). Free radicals, exercise, and antioxidant supplementation. Int J Sport Nutr 4, 205–220.

    Article  CAS  Google Scholar 

  • Kawai Y, Iwane H, Takanami Y, Shimomitsu T, Katsumura T, Fujinami J (1994). Vitamin E is mobilized in relation to lipolysis after strenuous endurance exercise. Med Sci Sports Exerc 26, S27.

    Article  Google Scholar 

  • Kehrer JP, Lund LG (1994). Cellular reducing equivalents and oxidative stress. Free Radical Biol Med 17, 65–75.

    Article  CAS  Google Scholar 

  • Levine BD, Stray-Gundersen J (1992). A practical approach to altitude training: where to live and train for optimal performance enhancement. Int J Sports Med 13, S209–S212.

    Article  Google Scholar 

  • Levine BD, Stray-Gundersen J, Duhaime G, Schell PG, Friedman DB (1991). ‘Living high-training low’: the effect of altitude acclimatization/normoxic training in trained runners. Med Sci Sports Exerc 23, S25.

    Google Scholar 

  • Lyan B, Azais-Braesco V, Cardinault N, Tyssandier V, Borel P, Alexandre-Gouabau MC et al. (2001). Simple metho for clinical determination of 13 carotenoids in human plasma using an isocratic high-performance liquid chromatographic method. J Chromatogr B Biomed Sci Appl 751, 297–303.

    Article  CAS  Google Scholar 

  • Margaritis I, Tessier F, Richard MJ, Marconnet P (1997). No evidence of oxidative stress after a triathlon race in highly trained competitors. Int J Sports Med 18, 186–190.

    Article  CAS  Google Scholar 

  • Mazzeo RS, Child A, Butterfield GE, Mawson JT, Zamudio S, Moore LG (1998). Catecholamine response during 12 days of high-altitude exposure (4300 m) in women. J Appl Physiol 84, 1151–1157.

    Article  CAS  Google Scholar 

  • Miyazaki H, Oh-ishi S, Ookawara T, Kizaki T, Toshinai K, Ha S et al. (2001). Strenuous endurance training in humans reduces oxidative stress following exhausting exercise. Eur J Appl Physiol 84, 1–6.

    Article  CAS  Google Scholar 

  • Mohanraj P, Merola AJ, Wright VP, Clanton TL (1998). Antioxidants protect rat diaphragmatic muscle function under hypoxic conditions. J Appl Physiol 84, 1960–1966.

    Article  CAS  Google Scholar 

  • Moller P, Loft S, Lundby C, Olsen NV (2001). Acute hypoxia and hypoxic exercise induce DNA strand breaks and oxidative DNA damage in humans. FASEB J 15, 1181–1186.

    Article  CAS  Google Scholar 

  • Moran M, Delgado J, Gonzalez B, Manso R, Megias A (2004). Responses of rat myocardial antioxidant defences and heat shock protein. HSP72 induced by 12 and 24-week treadmill training. Acta Physiol Scand 180, 157–166.

    Article  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95, 351–358.

    Article  CAS  Google Scholar 

  • Ohno H, Yahata T, Sato Y, Yamamura K, Taniguchi N (1988). Physical training and fasting erythrocyte activities of free radical scavenging enzyme systems in sedentary men. Eur J Appl Physiol Occup Physiol 57, 173–176.

    Article  CAS  Google Scholar 

  • Pincemail J, Deby C, Camus G, Pirnay F, Bouchez R, Massaux L et al. (1988). Tocopherol mobilization during intensive exercise. Eur J Appl Physiol Occup Physiol 57, 189–191.

    Article  CAS  Google Scholar 

  • Radak Z, Ogonovszky H, Dubecz J, Pavlik G, Sasvari M, Pucsok J et al. (2003). Super-marathon race increases serum and urinary nitrotyrosine and carbonyl levels. Eur J Clin Invest 33, 726–730.

    Article  CAS  Google Scholar 

  • Rayssiguier Y, Gueux E, Bussiere L, Mazur A (1993). Copper deficiency increases the susceptibility of lipoproteins and tissues to peroxidation in rats. J Nutr 123, 1343–1348.

    CAS  PubMed  Google Scholar 

  • Robertson JD, Maughan RJ, Duthie GG, Morrice PC (1991). Increased blood antioxidant systems of runners in response to training load. Clin Sci (London) 80, 611–618.

    Article  CAS  Google Scholar 

  • Sen CK (1995). Oxidants and antioxidants in exercise. J Appl Physiol 79, 675–686.

    Article  CAS  Google Scholar 

  • Sen CK (2001). Antioxidants in exercise nutrition. Sports Med 31, 891–908.

    Article  CAS  Google Scholar 

  • Sen CK, Khanna S, Reznick AZ, Roy S, Packer L (1997). Glutathione regulation of tumor necrosis factor-alpha-induced NF-kappa B activation in skeletal muscle-derived L6 cells. Biochem Biophys Res Commun 28, 645–649.

    Article  Google Scholar 

  • Simon-Schnass I (1996). Oxidative stress at high altitude and effects of vitamin E. In: Marriott BM, Carlson SJ (eds). Nutritional Needs in Cold and in High Altitude Environments. National Academy Press: Washington DC, pp 393–418.

    Google Scholar 

  • Subudhi AW, Davis SL, Kipp RW, Askew EW (2001). Antioxidant status and oxidative stress in elite alpine ski racers. Int J Sport Nutr Exerc Metab 1, 32–41.

    Article  Google Scholar 

  • Toskulkao C, Glinsukon T (1996). Endurance exercise and muscle damage: relationship to lipid peroxidation and scavenging enzymes in short and long distance runners. Jpn Phys Fitness Sports Med 46, 63–70.

    Article  Google Scholar 

  • Vasankari TJ, Kujala UM, Rusko H, Sarna S, Ahotupa M (1997). The effect of endurance exercise at moderate altitude on serum lipid peroxidation and antioxidative functions in humans. Eur J Appl Physiol Occup Physiol 75, 396–399.

    Article  CAS  Google Scholar 

  • Wasserman K (1987). Determinants and detection of anaerobic threshold and consequences of exercise above it. Circulation 76, VI29–VI39.

    CAS  PubMed  Google Scholar 

  • Wing SL, Askew EW, Luetkemeier MJ, Ryujin DT, Kamimori GH, Grissom CK (2003). Lack of effect of Rhodiola or oxygenated water supplementation on hypoxemia and oxidative stress. Wilderness Environ Med 14, 9–16.

    Article  Google Scholar 

  • Winklhofer-Roob BM, Khoschsorur G, Meinitzer A, Maritschnegg M, Hiller D; Wuga S, Wonisch W et al. (2003). Effects of vitamin E depletion/repletion on vitamin E status and oxidative stress in healthy volunteers. Clin Nutr 22, S33.

    Article  Google Scholar 

  • Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J et al. (1996). Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 49, 1304–1313.

    Article  CAS  Google Scholar 

  • Yagi K (1992). Lipids peroxides and exercise. Med Sport Sci 37, 40–42.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the subjects for their contribution. We also thank Eric Clottes for reviewing the manuscript and Clark Ellice and English review of the manuscript.

This study was funded by the ‘International Olympic Committee’ and the ‘Direction Régionale de la Jeunesse et des Sports de la Région Auvergne’.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V Pialoux.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pialoux, V., Mounier, R., Ponsot, E. et al. Effects of exercise and training in hypoxia on antioxidant/pro-oxidant balance. Eur J Clin Nutr 60, 1345–1354 (2006). https://doi.org/10.1038/sj.ejcn.1602462

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.ejcn.1602462

Keywords

This article is cited by

Search

Quick links