Abstract
Although exercise-induced oxidative stress receives considerable scientific attention, there is still little information available regarding exercise-induced adaptations of the antioxidant defence system in adolescent and child athletes. The aim of our study was to establish the effects of long-term exercise training on the redox state of adolescents, and to find correlations between elements of redox homeostasis and aerobic power. Thirty-three handball players and 14 non-athletes, 16–19-years old, were subjected to blood sampling to measure levels of nitric oxide (NO; estimated through nitrites (NO2 –)), superoxide anion radical (O2 –), hydrogen peroxide (H2O2), lipid peroxidation (estimated through TBARS), superoxide dismutase (SOD) and catalase (CAT). Subjects were also subjected to maximal progressive exercise test to estimate their maximal oxygen consumption (\( {{{\text{VO}}_{ 2} { \max }}} \)). Athletes had significantly (P < 0.05) higher SOD activity and lower CAT activity compared with non-athletes (SOD: 2175.52 ± 362.07 compared with 1172.16 ± 747.40 U/g of hemoglobin × 10 3, and CAT: 2.19 ± 0.31 compared with 3.08 ± 0.47 U/g of hemoglobin × 103). These differences were the most obvious when comparing non-athletes and athletes with poor/average aerobic power. H2O2 and TBARS levels differed among subjects with poor, average or good aerobic power (P < 0.01, and P < 0.05, respectively). Sports engagament and aerobic capacity are important factors in inducing changes in redox status.
Similar content being viewed by others
References
Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295
Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52(4):601–623
Kojdaa G, Harrison D (1999) Interactions between NO and reactive oxygen species: pathophysiological importance in atherosclerosis, hypertension, diabetes and heart failure. Cardiovasc Res 43:562–571
Fisher-Wellman K, Bloomer RJ (2009) Acute exercise and oxidative stress: a 30 year history. Dyn Med 8:1–25
Finaud J, Lac G, Filaire E (2006) Oxidative stress: relationship with exercise and training. Sports Med 36(4):327–358
Tanskanen M, Atalay M, Uusitalo A (2010) Altered oxidative stress in overtrained athletes. J Sports Sci 28(3):309–317
Dillard CJ, Litov RE, Savin WM (1978) Effects of exercise, vitamin E, and ozone on pulmonary function and lipid peroxidation. J Appl Physiol 45:927–932
Vollaard NB, Shearman JP, Cooper CE (2005) Exercise-induced oxidative stress: myths, realities and physiological relevance. Sports Med 35(12):1045–1062
Elosua R, Molina L, Fito M et al (2003) 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 167(2):327–334
Fatouros IG, Jamurtas AZ, Villiotou V et al (2004) Oxidative stress responses in older men during endurance training and detraining. Med Sci Sports Exerc 36(12):2065–2072
Warburton DE, Nicol CW, Bredin SS (2006) Health benefits of physical activity: the evidence. CMAJ 174:801–809
Melzer K, Kayser B, Pichard C (2004) Physical activity: the health benefits outweigh the risks. Curr Opin Clin Nutr Metab Care 7:641–647
Radak Z, Chung HY, Goto S (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44(2):153–159
Evelson P, Gambino G, Travacio M et al (2002) Higher antioxidant defences in plasma and low density lipoproteins from rugby players. Eur J Clin Investig 32(11):818–825
Radak Z, Chung HY, Koltai E, Taylor AW, Goto S (2008) Exercise, oxidative stress and hormesis. Ageing Res Rev 7(1):34–42
Marzatiko F, Pansarasa O, Bertorelli L et al (1997) 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 Fit 37:235–239
Hellsten Y, Apple FS, Sjodin B (1996) Effect of sprint cycle training on activities of antioxidant enzymes in human skeletal muscle. J Appl Physiol 81(4):1484–1487
Selamoglu S, Turgay F, Kayatekin BM et al (2000) Aerobic and anaerobic training effects on the antioxidant enzymes in the blood. Acta Physiol Hung 87(3):267–273
Miyazaki H, Oh-ishi S, Ookawara T et al (2001) Strenuous endurance training in humans reduces oxidative stress following exhausting exercise. Eur J Appl Physiol 84(1–2):1–6
Lekhi C, Gupta PH, Singh B (2007) Influence of exercise on oxidant stress products in elite Indian cyclists. Br J Sports Med 41(10):691–693
Powers SK, Ji LL, Leewenburg C (1999) Exercise-training induced alterations in skeletal muscle antioxidant capacity: a brief review. Med Sci Sports Exerc 31(7):987–997
Cazzola R, Russo-Volpe S, Cervato G, Cestaro B (2003) Biochemical assessments of oxidative stress, erythrocyte membrane fluidity and antioxidant status in professional soccer players and sedentary controls. Eur J Clin Investig 33(10):924–930
Chang CK, Tseng HF, Hsuuw YD et al (2002) Higher LDL oxidation at rest and after a rugby game in weekend warriors. Ann Nutr Metab 46:103–107
Metin G, Gumustas MK, Uslu E et al (2003) Effect of regular training on plasma thiols, malondialdehyde and carnitine concentrations in young soccer players. Chin J Physiol 46(1):35–39
Cooper DM, Nemet D, Galassetti P (2004) Exercise, stress, and inflammation in the growing child: from the bench to the playground. Curr Opin Pediatr 16(3):286–292
Armstrong N, McManus AM, Welsman JR (2008) Aerobic fitness. In: Armstrong N, Mechelen W (eds) Paediatric exercise science and medicine. Oxford University Press, Oxford, pp 269–282
Boisseau N, Delamarche P (2000) Metabolic and hormonal responses to exercise in children and adolescents. Sports Med 30(6):405–422
Cooper CB (2004) Classification of cardiorespiratory fitness based on maximum oxygen uptake. In: Cooper CB, Storer TW (eds) Exercise testing and interpretation—a practical approach. Cambridge University Press, Cambridge, p 239
Howley ET, Bassett DR Jr, Welch HG (1995) Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 27(9):1292–1301
McCord JM, Fridovich I (1969) The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J Biol Chem 244(22):6056–6063
Beutler E (1982) Catalase. In: Beutler E (ed) Red cell metabolism, a manual of biochemical methods. Grune and Stratton, New York, pp 105–106
Tsuchihashi M (1923) Zur Kernntnis der blutkatalase. Biochem Z 140:65–72
Misra HP, Fridovich I (1972) The role of superoxide-anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175
Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite and [15 N] nitrate in biological fluids. Anal Biochem 126:131–138
Auclair C, Voisin E (1985) Nitroblue tetrazolium reduction. In: Greenvvald RA (ed) Handbook of methods for oxygen radical research. CRC Press Ine., Boca Raton, pp 123–132
Pick E, Keisari Y (1980) A simple colorimetric method for the measurement of hydrogen peroxide produced by cells in culture. J Immunol Methods 38:161–170
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
Naghizadeh H, Afzalpour ME, Zarban A (2009) The comparison of antioxidant status and lipid profile of karate athletes with non-athletes. J Birjand Univ Med Sci 16(3):54–61
Brites FD, Evelson PA, Christiansen MG, Nicol MF, Basílico MJ, Wikinski RW, Llesuy SF (1999) Soccer players under regular training show oxidative stress but an improved plasma antioxidant status. Clin Sci 96(4):381–385
Ortenblad N, Madsen K, Djurhuus MS (1997) Antioxidant status and lipid peroxidation after short-term maximal exercise in trained and untrained humans. Am J Physiol 272(4):R1258–R1263
Balakrishnan SD, Anuradh CV (1998) Exercise, depletion of antioxidants and antioxidant manipulation. Cell Biochem Funct 16:269–275
Djujic I, Jozanov-Stankov O, Demajo M (2003) Oxidative stress and antioxidant defense markers in the population of Serbia and Montenegro. Physiol Pharmacol Acta 39:121–128
Nikolic-Kokic A, Stevic Z, Blagojevic D, Davidovic D, Jones DR, Spasic MB (2006) Alterations in anti-oxidative defence enzymes in erythrocytes from sporadic amyotrophic lateral sclerosis (SALS) and familial ALS patients. Clin Chem Lab Med 44:589–593
Djordjevic D, Cubrilo D, Zivkovic V, Barudzic N, Vuletic M, Jakovljevic V (2010) Pre-exercise superoxide dismutase activity affects the pro/antioxidant response to acute exercise. Ser J Exp Clin Res 11(4):145–153
Kingwell BA, Sherrard B, Jennings GL, Dart AM (1997) Four weeks of cycle training increases basal production of nitric oxide from the forearm. Am J Physiol 272(3 Pt 2):H1070–H1077
Jungersten L, Ambring A, Wall B, Wennmalm A (1997) Both physical fitness and acute exercise regulate nitric oxide formation in healthy humans. J Appl Physiol 82:760–764
Poveda JJ, Riestra A, Salas E, Cagigas ML, López-Somoza C, Amado JA, Berrazueta JR (1997) Contribution of nitric oxide to exercise-induced changes in healthy volunteers: effects of acute exercise and long-term physical training. Eur J Clin Investiig 27(11):967–971
Banfi G, Malavazos A, Iorio E, Dolci A, Doneda L, Verna R, Corsi MM (2006) Plasma oxidative stress biomarkers, nitric oxide and heat shock protein 70 in trained elite soccer players. Eur J Appl Physiol 96(5):483–486
Maeda S, Miyauchi T, Kakiyama T et al (2001) Effects of exercise training of 8 weeks and detraining on plasma levels of endothelium-derived factors, endothelin-1 and nitric oxide, in healthy young humans. Life Sci 69(9):1005–1016
Maiorana A, O’Driscoll G, Taylor R, Green D (2003) Exercise and the nitric oxide vasodilator system. Sports Med 33(14):1013–1035
Green DJ, Maiorana A, O’Driscoll G, Taylor R (2004) Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol 561:1–25
Lewis T, Dart AM, Chin-Dusting JPF, Kingwell BA (1999) Exercise training increases basal nitric oxide production from the forearm in hypercholesterolemic patients. Arterioscler Thromb Vasc Biol 19:2782–2787
Mendes-Ribeiro AC, Mann GE, de Meirelles LR, Moss MB, Matsuura C, Brunini TMC (2009) The Role of Exercise on l-arginine nitric oxide pathway in chronic heart failure. Open Biochem J 3:55–65
Djordjevic D, Jakovljevic V, Cubrilo D, Zlatkovic M, Zivković V, Djuric D (2010) Coordination between nitric oxide and superoxide anion radical during progressive exercise in elite soccer players. Open Biochem J 4:100–106
Rassaf T, Lauer T, Heiss C et al (2007) Nitric oxide synthase-derived plasma nitrite predicts exercise capacity. Br J Sports Med 41:669–673
Allen JD, Cobb FR, Kraus WE, Gow AJ (2006) Total nitrogen oxide following exercise testing reflects endothelial function and discriminates health status. Free Radic Biol Med 41:740–747
Hambrecht R, Fiehn E, Weigl C et al (1998) Regular physical exercise corrects endothelial dysfunction and improves exercise capacity in patients with chronic heart failure. Circulation 98:2709–2715
Moyna NM, Thompson PD (2004) The effect of physical activity on endothelial function in man. Acta Physiol Scand 180:113–123
Tinken TM, Thijssen DHJ, Black MA, Cable NT, Green DJ (2008) Time course of change in vasodilator function and capacity in response to exercise training in humans. J Physiol 586:5003–5012
Kingwell BA (2000) Nitric oxide-mediated metabolic regulation during exercise: effects of training in health and cardiovascular disease. FASEB J 14:1685–1696
Ziv G, Lidor R (2009) Physical characteristics, physiological attributes, and on-court performances of handball players: a review. Eur J Sport Sci 9(6):375–386
Carlsohn A, Rohn S, Bittmann F, Raila J, Mayer F, Schweigert FJ (2008) Exercise increases the plasma antioxidant capacity of adolescent athletes. Ann Nutr Metab 53(2):96–103
Acknowledgments
This work was supported by Grant No. 175043 from the Ministry of Science and Technical Development of the Republic of Serbia.
Conflict of interest
The authors declare that they have no conflict of interests.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Djordjevic, D., Cubrilo, D., Macura, M. et al. The influence of training status on oxidative stress in young male handball players. Mol Cell Biochem 351, 251–259 (2011). https://doi.org/10.1007/s11010-011-0732-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-011-0732-6