Abstract
It is well known that exercise training can deeply affect redox homeostasis by enhancing antioxidant defenses. However, exhaustive exercise can induce excessive reactive oxygen species (ROS) production, leading to oxidative stress-related tissue injury and impaired muscle contractility. Hence, ROS represent important signaling molecules whose level has to be maintained to preserve normal cellular function, but which can also accumulate in response to repetitive muscle contraction. In fact, low levels of oxidants have been suggested to be essential for muscle contraction. Both aerobic and anaerobic exercise induce ROS production from several sources (mitochondria, NADPH oxidases and xanthine oxidases); however, the exact mechanisms underlying exercise-induced oxidative stress remain undefined. Professional athletes show a high risk for oxidative stress, and consequently muscle injury or decreased performance. Based on this background, we investigated leukocyte redox homeostasis alterations during the soccer season in élite soccer players. Overall blood redox status was investigated in twenty-seven male soccer players from primary division (Italian “Serie A” team) at four critical time points during the soccer season: T0: just before the first team training session; T1: at the beginning of the season; T2: in the middle of the season and T3: at the end of the season. The main markers of muscular damage (CK, myoglobin, LDH), assessed by standard routine methods, are significantly altered at the considered time points (T0 vs T1 P < 0.01). In peripheral leukocyte subpopulations, ROS production shows significant alterations at the considered time points during the soccer season, and strictly and significantly correlates with CK values at every considered time point. Our experimental data indicate that deep redox homeostasis alterations are evident during the soccer season in élite soccer players, and that oxidative stress can be easily monitored, besides using the standard plasma biochemical parameters, by leukocyte ROS production analysis.
Similar content being viewed by others
References
Vollaard NB, Shearman JP, Cooper CE (2005) Exercise-induced oxidative stress: myths, realities and physiological relevance. Sports Med 35:1045–1062
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 (Lond) 96:381–385
Schmikli SL, de Vries WR, Brink MS, Backx FJ (2012) Monitoring performance, pituitary-adrenal hormones and mood profiles: how to diagnose non-functional over-reaching in male elite junior soccer players. Br J Sports Med 46:1019–1023
Lippi G, Schena F, Montagnana M, Salvagno GL, Guidi GC (2008) Influence of acute physical exercise on emerging muscular biomarkers. Clin Chem Lab Med 46:1313–1318
Hammouda O, Chtourou H, Chahed H, Ferchichi S, Chaouachi A, Kallel C, Miled A, Chamari K, Souissi N (2012) High intensity exercise affects diurnal variation of some biological markers in trained subjects. Int J Sports Med 33:886–891
Hambrecht R, Gielen S (2014) Essay: hunter-gatherer to sedentary lifestyle. Lancet 366:S60–S61
Sanchis-Gomar F, Lippi G (2014) Physical activity—an important preanalytical variable. Biochem Med (Zagreb) 24:68–79
Budgett R, Hiscock N, Arida RM, Castell LM (2010) The effects of the 5-HT2C agonist m-chlorophenylpiperazine on elite athletes with unexplained underperformance syndrome (overtraining). Br J Sports Med 44:280–283
Meister S, Faude O, Ammann T, Schnittker R, Meyer T (2013) Indicators for high physical strain and overload in elite football players. Scand J Med Sci Sports 23:156–163
Faude O, Kellmann M, Ammann T, Schnittker R, Meyer T (2011) Seasonal changes in stress indicators in high level football. Int J Sports Med 32:259–265
Banfi G, Malavazos A, Iorio E, Dolci A, Doneda L, Verna R, Corsi MM (2005) Plasma oxidative stress biomarkers, nitric oxide and heat shock protein 70 in trained elite soccer players. Eur J Appl Physiol 96:483–486
Gomez-Cabrera MC, Domenech E, Vina J (2008) Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44:126–131
Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Blüher M (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci 106:8665–8670
Chang CK, Huang HY, Tseng HF, Hsuuw YD, Tso TK (2007) Interaction of vitamin E and exercise training on oxidative stress and antioxidant enzyme activities in rat skeletal muscles. J Nutr Biochem 18:39–45
Knez WL, Jenkins DG, Coombes JS (2007) Oxidative stress in half and full Ironman triathletes. Med Sci Sports Exerc 39:283–288
Impellizzeri FM, Rampinini E, Coutts AJ (2004) Use of RPE-based training load in soccer. Med Sci Sports Exerc 36:1042–1047
Foster C (1998) Monitoring training in athletes with reference to overtraining syndrome. Med Sci Sports Exerc 30:1164–1168
American Dietetic Association, Dietitians of Canada, American College of Sports Medicine, Rodriguez NR, Di Marco NM, Langley S (2009) American College of Sports Medicine position stand. Nutrition and athletic performance. Med Sci Sports Exerc 41:709–731
Becatti M, Fiorillo C, Gori AM, Marcucci R, Paniccia R, Giusti B, Violi F, Pignatelli P, Gensini GF, Abbate R (2013) Platelet and leukocyte ROS production and lipoperoxidation are associated with high platelet reactivity in Non-ST elevation myocardial infarction (NSTEMI) patients on dual antiplatelet treatment. Atherosclerosis 231:392–400
Barygina VV, Becatti M, Soldi G, Prignano F, Lotti T, Nassi P, Wright D, Taddei N, Fiorillo C (2013) Altered redox status in the blood of psoriatic patients: involvement of NADPH oxidase and role of anti-TNF-α therapy. Redox Rep 18:100–106
Becatti M, Marcucci R, Bruschi G, Taddei N, Bani D, Gori AM, Giusti B, Gensini GF, Abbate R, Fiorillo C (2014) Oxidative modification of fibrinogen is associated with altered function and structure in the subacute phase of myocardial infarction. Arterioscler Thromb Vasc Biol 34:1355–1361
Becatti M, Emmi G, Silvestri E, Bruschi G, Ciucciarelli L, Squatrito D, Vaglio A, Taddei N, Abbate R, Emmi L, Goldoni M, Fiorillo C, Prisco D (2016) Neutrophil activation promotes fibrinogen oxidation and thrombus formation in Behçet disease. Circulation 133:302–311
Ji LL (2008) Modulation of skeletal muscle antioxidant defense by exercise: role of redox signaling. Free Radic Biol Med 44:142–152
Ji LL, Gomez-Cabrera MC, Vina J (2006) Exercise and hormesis: activation of cellular antioxidant signaling pathway. Ann N Y Acad Sci 1067:425–435
Bloomer RJ, Fisher-Wellman KH (2008) Blood oxidative stress biomarkers: influence of sex, exercise training status, and dietary intake. Gend Med 5:218–228
Falone S, Mirabilio A, Pennelli A, Cacchio M, Di Baldassarre A, Gallina S et al (2010) Differential impact of acute bout of exercise on redox- and oxidative damage-related profiles between untrained subjects and amateur runners. Physiol Res 59:953–961
Ascensão A, Rebelo A, Oliveira E, Marques F, Pereira L, Magalhães J (2008) Biochemical impact of a soccer match—analysis of oxidative stress and muscle damage markers throughout recovery. Clin Biochem 41:841–851
Le Moal E, Groussard C, Paillard T, Chaory K, Le Bris R, Plantet K, Pincemail J, Zouhal H (2016) Redox status of professional soccer players is influenced by training load throughout a season. Int J Sports Med 37:680–686
Teixeira V, Valente H, Casal S, Pereira L, Marques F, Moreira P (2009) Antioxidant status, oxidative stress, and damage in elite kayakers after 1 year of training and competition in 2 seasons. Appl Physiol Nutr Metab 34:716–724
Finaud J, Scislowski V, Lac G, Durand D, Vidalin H, Robert A, Filaire E (2006) Antioxidant status and oxidative stress in professional rugby players: evolution throughout a season. Int J Sports Med 27:87–93
Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8:1865–1879
Elokda AS, Nielsen DH (2007) Effects of exercise training on the glutathione antioxidant system. Eur J Cardiovasc Prev Rehabil 14:630–637
Kumral ZN, Sener G, Ozgur S, Koc M, Suleymanoglu S, Hurdag C, Yegen BC (2016) Regular exercise alleviates renovascular hypertension-induced cardiac/endothelial dysfunction and oxidative injury in rats. J Physiol Pharmacol 67:45–55
Margonis K, Fatouros IG, Jamurtas AZ, Nikolaidis MG, Douroudos I, Chatzinikolaou A, Mitrakou A, Mastorakos G, Papassotiriou I, Taxildaris K, Kouretas D (2007) Oxidative stress biomarkers responses to physical overtraining: implications for diagnosis. Free Radic Biol Med 43:901–910
Seifi-Skishahr F, Damirchi A, Farjaminezhad M, Babaei P (2016) Physical training status determines oxidative stress and redox changes in response to an acute aerobic exercise. Biochem Res Int 2016:3757623
Djordjević VB (2004) Free radicals in cell biology. Int Rev Cytol 237:57–89
Irrcher I, Adhihetty PJ, Joseph AM, Ljubicic V, Hood DA (2003) Regulation of mitochondrial biogenesis in muscle by endurance exercise. Sports Med 33:783–793
St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jäger S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397–408
Aquilano K, Baldelli S, Pagliei B, Cannata SM, Rotilio G, Ciriolo MR (2013) p53 orchestrates the PGC-1alpha-mediated antioxidant response upon mild redox and metabolic imbalance. Antioxid Redox Signal 18:386–399
Margaritelis NV, Cobley JN, Paschalis V, Veskoukis AS, Theodorou AA, Kyparos A, Nikolaidis MG (2016) Going retro: oxidative stress biomarkers in modern redox biology. Free Radic Biol Med 98:2–12
Belia S, Santilli F, Beccafico S, De Feudis L, Morabito C, Davi G, Fanò G, Mariggiò MA (2009) Oxidative-induced membrane damage in diabetes lymphocytes: effects on intracellular Ca(2+) homeostasis. Free Radic Res 43:138–148
Nagaeva O, Bondestam K, Olofsson J, Damber MG, Mincheva-Nilsson L (2002) An optimized technique for separation of human decidual leukocytes for cellular and molecular analyses. Am J Reprod Immunol 47:203–212
Balakrishnan S, Rao SB (1999) Cytogenetic analysis of peripheral blood lymphocytes of occupational workers exposed to low levels of ionising radiation. Mutat Res 442:37–42
Sureda A, Ferrer MD, Tauler P, Romaguera D, Drobnic F, Pujol P, Tur JA, Pons A (2009) Effects of exercise intensity on lymphocyte H2O2 production and antioxidant defences in soccer players. Br J Sports Med 43:186–190
Zuo L, Zhou T, Pannell BK, Ziegler AC, Best TM (2015) Biological and physiological role of reactive oxygen species—the good, the bad and the ugly. Acta Physiol (Oxf) 214:329–348
Gleeson M (2007) Immune function in sport and exercise. J Appl Physiol 103:693–699
Petibois C, Cazorla G, Poortmans JR, Déléris G (2002) Biochemical aspects of overtraining in endurance sports: a review. Sports Med 32:867–878
Syu GD, Chen HI, Jen CJ (2011) Severe exercise and exercise training exert opposite effects on human neutrophil apoptosis via altering the redox status. PLoS One 6:e24385
Mitra S, Abraham E (2006) Participation of superoxide in neutrophil activation and cytokine production. Biochim Biophys Acta 1762:732–741
Brancaccio P, Maffulli N, Limongelli FM (2007) Creatine kinase monitoring in sport medicine. Br Med Bull 81:209–230
Lippi G, Banfi G (2008) Distribution of creatine kinase in sedentary and physically active individuals. Am Heart J 155:e51
Mougios V (2007) Reference intervals for serum creatine kinase in athletes. Br J Sports Med 41:674–678
Clarkson PM, Hubal MJ (2002) Exercise-induced muscle damage in humans. Am J Phys Med Rehabil 81:S52–S69
Kratz A, Lewandrowski KB, Siegel AJ, Chun KY, Flood JG, van Cott EM et al (2002) Effect of marathon running on hematologic and biochemical laboratory parameters, including cardiac markers. Am J Clin Pathol 118:856–863
Vincent HK, Vincent KR (1997) The effect of training status on the serum creatine kinase response, soreness and muscle function following resistance exercise. Int J Sports Med 18:431–437
Margaritis I, Tessier F, Verdera F, Bermon S, Marconnet P (1999) Muscle enzyme release does not predict muscle function impairment after triathlon. J Sports Med Phys Fit 39:133–139
Banfi G, Morelli P (2008) Relation between body mass index and serum aminotransferases concentrations in professional athletes. J Sports Med Phys Fit 48:197–200
Zieliński J, Rychlewski T, Kusy K, Domaszewska K, Laurentowska M (2009) The effect of endurance training on changes in purine metabolism: a longitudinal study of competitive long-distance runners. Eur J Appl Physiol 106:867–876
Filaire E, Lac G, Pequignot JM (2003) Biological, hormonal, and psychological parameters in professional soccer players throughout a competitive season. Percept Mot Skills 97:1061–1072
Heisterberg MF, Fahrenkrug J, Krustrup P, Storskov A, Kjær M, Andersen JL (2013) Extensive monitoring through multiple blood samples in professional soccer players. J Strength Cond Res 27:1260–1271
Reinke S, Karhausen T, Doehner W, Taylor W, Hottenrott K, Duda GN, Reinke P, Volk HD, Anker SD (2009) The influence of recovery and training phases on body composition, peripheral vascular function and immune system of professional soccer players. PLoS One 4:e4910
Karakoc Y, Duzova H, Polat A, Emre MH, Arabaci I (2005) Effects of training period on haemorheological variables in regularly trained footballers. Br J Sports Med 39:e4
Meyer T, Meister S (2011) Routine blood parameters in elite soccer players. Int J Sports Med 32:875–881
Ostojic SM, Ahmetovic Z (2008) Weekly training volume and hematological status in female top-level athletes of different sports. J Sports Med Phys Fit 48:398–403
Acknowledgements
Funding was provided by Università degli Studi di Firenze.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The Authors declare that they have no conflict of interest.
Statement of human and animal rights
The study was conducted according to policy statement set forth in the Declaration of Helsinki, and was approved by the local Ethics Committee of the University of Florence, Italy.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Becatti, M., Mannucci, A., Barygina, V. et al. Redox status alterations during the competitive season in élite soccer players: focus on peripheral leukocyte-derived ROS. Intern Emerg Med 12, 777–788 (2017). https://doi.org/10.1007/s11739-017-1653-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11739-017-1653-5