Redox status alterations during the competitive season in élite soccer players: focus on peripheral leukocyte-derived ROS

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.

[1]  Rosanna Abbate,et al.  Neutrophil Activation Promotes Fibrinogen Oxidation and Thrombus Formation in Behçet Disease , 2016, Circulation.

[2]  A. Jamurtas,et al.  Oxidative stress biomarkers responses to physical overtraining: implications for diagnosis. , 2007, Free radical biology & medicine.

[3]  B. Yeğen,et al.  Regular exercise alleviates renovascular hypertension-induced cardiac/endothelial dysfunction and oxidative injury in rats. , 2016, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[4]  A. Sureda,et al.  Effects of exercise intensity on lymphocyte H2O2 production and antioxidant defences in soccer players , 2007, British Journal of Sports Medicine.

[5]  O. Faude,et al.  Indicators for high physical strain and overload in elite football players , 2013, Scandinavian journal of medicine & science in sports.

[6]  D. Hood,et al.  Regulation of Mitochondrial Biogenesis in Muscle by Endurance Exercise , 2003, Sports medicine.

[7]  F. Santilli,et al.  Oxidative-induced membrane damage in diabetes lymphocytes: Effects on intracellular Ca2 + homeostasis , 2009, Free radical research.

[8]  P. Krustrup,et al.  Extensive Monitoring Through Multiple Blood Samples in Professional Soccer Players , 2013, Journal of strength and conditioning research.

[9]  G. Cazorla,et al.  Biochemical Aspects of Overtraining in Endurance Sports , 2002, Sports medicine.

[10]  A. Damirchi,et al.  Physical Training Status Determines Oxidative Stress and Redox Changes in Response to an Acute Aerobic Exercise , 2016, Biochemistry research international.

[11]  T. Meyer,et al.  Routine Blood Parameters in Elite Soccer Players , 2011, International Journal of Sports Medicine.

[12]  Betti Giusti,et al.  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. , 2013, Atherosclerosis.

[13]  S. Bermon,et al.  Muscle enzyme release does not predict muscle function impairment after triathlon. , 1999, The Journal of sports medicine and physical fitness.

[14]  E. Filaire,et al.  Antioxidant status and oxidative stress in professional rugby players: evolution throughout a season. , 2006, International journal of sports medicine.

[15]  E. Filaire,et al.  Biological, Hormonal, and Psychological Parameters in Professional Soccer Players Throughout a Competitive Season , 2003, Perceptual and motor skills.

[16]  Y. Karakoç,et al.  Effects of training period on haemorheological variables in regularly trained footballers , 2005, British Journal of Sports Medicine.

[17]  D. Nielsen,et al.  Effects of exercise training on the glutathione antioxidant system , 2007, European journal of cardiovascular prevention and rehabilitation : official journal of the European Society of Cardiology, Working Groups on Epidemiology & Prevention and Cardiac Rehabilitation and Exercise Physiology.

[18]  R. Arida,et al.  The effects of the 5-HT2C agonist m-chlorophenylpiperazine on elite athletes with unexplained underperformance syndrome (overtraining) , 2008, British Journal of Sports Medicine.

[19]  Nicola Maffulli,et al.  Creatine kinase monitoring in sport medicine. , 2007, British medical bulletin.

[20]  E. Abraham,et al.  Participation of superoxide in neutrophil activation and cytokine production. , 2006, Biochimica et biophysica acta.

[21]  V. Mougios,et al.  Reference intervals for serum creatine kinase in athletes , 2007, British Journal of Sports Medicine.

[22]  S. Casal,et al.  Antioxidant status, oxidative stress, and damage in elite kayakers after 1 year of training and competition in 2 seasons. , 2009, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme.

[23]  G. Banfi,et al.  Plasma oxidative stress biomarkers, nitric oxide and heat shock protein 70 in trained elite soccer players , 2006, European Journal of Applied Physiology.

[24]  P. Evelson,et al.  Soccer players under regular training show oxidative stress but an improved plasma antioxidant status , 1999 .

[25]  Michael Stumvoll,et al.  Antioxidants prevent health-promoting effects of physical exercise in humans , 2009, Proceedings of the National Academy of Sciences.

[26]  L. Ji Modulation of skeletal muscle antioxidant defense by exercise: Role of redox signaling. , 2008, Free radical biology & medicine.

[27]  Franco M Impellizzeri,et al.  Use of RPE-based training load in soccer. , 2004, Medicine and science in sports and exercise.

[28]  José Magalhães,et al.  Biochemical impact of a soccer match - analysis of oxidative stress and muscle damage markers throughout recovery. , 2008, Clinical biochemistry.

[29]  H. Vincent,et al.  The Effect of Training Status on the Serum Creatine Kinase Response, Soreness and Muscle Function Following Resistance Exercise , 1997, International journal of sports medicine.

[30]  V. Djordjević Free radicals in cell biology. , 2004, International review of cytology.

[31]  N. Taddei,et al.  Altered redox status in the blood of psoriatic patients: involvement of NADPH oxidase and role of anti-TNF-α therapy , 2013, Redox report : communications in free radical research.

[32]  R. Bloomer,et al.  Blood oxidative stress biomarkers: influence of sex, exercise training status, and dietary intake. , 2008, Gender medicine.

[33]  S. Gielen,et al.  Essay: Hunter-gatherer to sedentary lifestyle , 2005, The Lancet.

[34]  M. Cacchio,et al.  Differential impact of acute bout of exercise on redox- and oxidative damage-related profiles between untrained subjects and amateur runners. , 2010, Physiological research.

[35]  A. Veskoukis,et al.  Going retro: Oxidative stress biomarkers in modern redox biology. , 2016, Free radical biology & medicine.

[36]  N. Rodriguez,et al.  Position of the American Dietetic Association, Dietitians of Canada, and the American College of Sports Medicine: Nutrition and athletic performance. , 2009, Journal of the American Dietetic Association.

[37]  L. Jaeger Immune Function In Sport And Exercise , 2016 .

[38]  K. Domaszewska,et al.  The effect of endurance training on changes in purine metabolism: a longitudinal study of competitive long-distance runners , 2009, European Journal of Applied Physiology.

[39]  P. Clarkson,et al.  Exercise-induced muscle damage in humans. , 2002, American journal of physical medicine & rehabilitation.

[40]  Dean P. Jones Redefining oxidative stress. , 2006, Antioxidants & redox signaling.

[41]  A. Kratz,et al.  Effect of marathon running on hematologic and biochemical laboratory parameters, including cardiac markers. , 2002, American journal of clinical pathology.

[42]  A. Jamurtas,et al.  Corrigendum to “Oxidative stress biomarkers responses to physical overtraining: Implications for diagnosis” [Free Radic. Biol. Med. 43 (2007) 901-910] , 2008 .

[43]  S. B. Rao,et al.  Cytogenetic analysis of peripheral blood lymphocytes of occupational workers exposed to low levels of ionising radiation. , 1999, Mutation research.

[44]  A. Chaouachi,et al.  High Intensity Exercise Affects Diurnal Variation of Some Biological Markers in Trained Subjects , 2012, International Journal of Sports Medicine.

[45]  W. Knez,et al.  Oxidative stress in half and full Ironman triathletes. , 2007, Medicine and science in sports and exercise.

[46]  S. Ostojić,et al.  Weekly training volume and hematological status in female top-level athletes of different sports. , 2008, The Journal of sports medicine and physical fitness.

[47]  F. Backx,et al.  Monitoring performance, pituitary–adrenal hormones and mood profiles: how to diagnose non-functional over-reaching in male elite junior soccer players , 2011, British Journal of Sports Medicine.

[48]  L. Mincheva-Nilsson,et al.  An Optimized Technique for Separation of Human Decidual Leukocytes for Cellular and Molecular Analyses , 2002, American journal of reproductive immunology.

[49]  W. Taylor,et al.  The Influence of Recovery and Training Phases on Body Composition, Peripheral Vascular Function and Immune System of Professional Soccer Players , 2009, PloS one.

[50]  C. Foster,et al.  Monitoring training in athletes with reference to overtraining syndrome. , 1998, Medicine and science in sports and exercise.

[51]  Chen-Kang Chang,et al.  Interaction of vitamin E and exercise training on oxidative stress and antioxidant enzyme activities in rat skeletal muscles. , 2007, The Journal of nutritional biochemistry.

[52]  G. Rotilio,et al.  p53 orchestrates the PGC-1α-mediated antioxidant response upon mild redox and metabolic imbalance. , 2013, Antioxidants & redox signaling.

[53]  J. Viña,et al.  Exercise and Hormesis , 2006, Annals of the New York Academy of Sciences.

[54]  P. Evelson,et al.  Soccer players under regular training show oxidative stress but an improved plasma antioxidant status. , 1999, Clinical science.

[55]  H. Chen,et al.  Severe Exercise and Exercise Training Exert Opposite Effects on Human Neutrophil Apoptosis via Altering the Redox Status , 2011, PloS one.

[56]  O. Faude,et al.  Seasonal Changes in Stress Indicators in High Level Football , 2011, International journal of sports medicine.

[57]  A. C. Ziegler,et al.  Biological and physiological role of reactive oxygen species – the good, the bad and the ugly , 2015, Acta physiologica.

[58]  G. Banfi,et al.  Relation between body mass index and serum aminotransferases concentrations in professional athletes. , 2008, The Journal of sports medicine and physical fitness.

[59]  G. Lippi,et al.  Distribution of creatine kinase in sedentary and physically active individuals. , 2008, American heart journal.

[60]  G. Lippi,et al.  Physical activity - an important preanalytical variable , 2014, Biochemia medica.

[61]  Jiandie D. Lin,et al.  Suppression of Reactive Oxygen Species and Neurodegeneration by the PGC-1 Transcriptional Coactivators , 2006, Cell.

[62]  Chris E Cooper,et al.  Exercise-Induced Oxidative Stress , 2005, Sports medicine.

[63]  G. Lippi,et al.  Influence of acute physical exercise on emerging muscular biomarkers , 2008, Clinical chemistry and laboratory medicine.

[64]  J. Viña,et al.  Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. , 2008, Free radical biology & medicine.

[65]  Betti Giusti,et al.  Oxidative Modification of Fibrinogen Is Associated With Altered Function and Structure in the Subacute Phase of Myocardial Infarction , 2014, Arteriosclerosis, thrombosis, and vascular biology.

[66]  J. Pincemail,et al.  Redox Status of Professional Soccer Players is Influenced by Training Load Throughout a Season , 2016, International Journal of Sports Medicine.