Abstract
Background
Physical activity has been associated with reduced oxidative stress (OS) in observational studies and clinical trials.
Objective
The purpose of this systematic review and meta-analysis of controlled trials was to determine the effect of physical exercise on OS parameters.
Methods
We conducted a systematic review of the literature up to March 2016 that included the following databases: PubMed, SCOPUS, and Web of Science. A keyword combination referring to exercise training and OS was included as part of a more thorough search process. We also manually searched the reference lists of the articles. From an initial 1573 references, we included 30 controlled trials (1346 participants) in the qualitative analysis, 19 of which were included in the meta-analysis. All trials were conducted in humans and had at least one exercise intervention and a paired control group. Using a standardized protocol, two investigators independently abstracted data on study design, sample size, participant characteristics, intervention, follow-up duration, outcomes, and quantitative data for the meta-analysis. Thus, the investigators independently assigned quality scores with a methodological quality assessment (MQA).
Results
The agreement level between the reviewers was 85.3 %. Discrepancies were solved in a consensus meeting. The MQA showed a total score in the quality index between 40 and 90 % and a mean quality of 55 %. Further, in a random-effects model, data from each trial were pooled and weighted by the inverse of the total variance. Physical training was associated with a significant reduction in pro-oxidant parameters (standard mean difference [SMD] –1.08; 95 % confidence interval [CI] –1.57 to –0.58; p < 0.001) and an increase in antioxidant capacity (SMD 1.45; 95 % CI 0.83–2.06; p < 0.001).
Conclusion
The pooled analysis revealed that regardless of intensity, volume, type of exercise, and studied population, the antioxidant indicators tended to increase and pro-oxidant indicators tended to decrease after training. Therefore, we conclude that exercise training seems to induce an antioxidant effect. Thus, it is suggested that people practice some kind of exercise to balance the redox state, regardless of their health status, to improve health-related outcomes.
Similar content being viewed by others
References
Hallal PC, Andersen LB, Bull FC, et al. Global physical activity levels: surveillance progress, pitfalls, and prospects. Lancet. 2012;380(9838):247–57. doi:10.1016/S0140-6736(12)60646-1.
Blair SN, Kampert JB, Kohl HW 3rd, et al. Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA. 1996;276(3):205–10.
Kokkinos P, Myers J. Exercise and physical activity: clinical outcomes and applications. Circulation. 2010;122(16):1637–48. doi:10.1161/CIRCULATIONAHA.110.948349.
Vincent HK, Innes KE, Vincent KR. Oxidative stress and potential interventions to reduce oxidative stress in overweight and obesity. Diabetes Obes Metab. 2007;9(6):813–39. doi:10.1111/j.1463-1326.2007.00692.x.
Larsen BA, Martin L, Strong DR. Sedentary behavior and prevalent diabetes in Non-Latino Whites, Non-Latino Blacks and Latinos: findings from the National Health Interview Survey. J Public Health (Oxf). 2015;37(4):634–40. doi:10.1093/pubmed/fdu103.
Beunza JJ, Martinez-Gonzalez MA, Ebrahim S, et al. Sedentary behaviors and the risk of incident hypertension: the SUN Cohort. Am J Hypertens. 2007;20(11):1156–62. doi:10.1016/j.amjhyper.2007.06.007.
Hamer M, Venuraju SM, Urbanova L, et al. Physical activity, sedentary time, and pericardial fat in healthy older adults. Obesity (Silver Spring). 2012;20(10):2113–7. doi:10.1038/oby.2012.61.
Myers J, Prakash M, Froelicher V, et al. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002;346(11):793–801.
Metter EJ, Talbot LA, Schrager M, et al. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci. 2002;57(10):B359–65.
Blair SN, Cheng Y, Holder JS. Is physical activity or physical fitness more important in defining health benefits? Med Sci Sports Exerc. 2001;33(6):379–99.
Mathis D, Shoelson SE. Immunometabolism: an emerging frontier. Nat Rev Immunol. 2011;11(2):81–3.
Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–7. doi:10.1038/nature05485.
Bonnard C, Durand A, Peyrol S, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest. 2008;118(2):789–800. doi:10.1172/JCI32601.
Radak Z, Chung HY, Goto S. Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med. 2008;44(2):153–9. doi:10.1016/j.freeradbiomed.2007.01.029.
Powers SK, Talbert EE, Adhihetty PJ. Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol. 2011;589(9):2129–38.
Fischer R, Maier O. Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxid Med Cell Longev. 2015;2015:610813. doi:10.1155/2015/610813.
Siti HN, Kamisah Y, Kamsiah J. The role of oxidative stress, antioxidants and vascular inflammation in cardiovascular disease (a review). Vascul Pharmacol. 2015;71:40–56. doi:10.1016/j.vph.2015.03.005.
Sarmiento D, Montorfano I, Cerda O, et al. Increases in reactive oxygen species enhance vascular endothelial cell migration through a mechanism dependent on the transient receptor potential melastatin 4 ion channel. Microvasc Res. 2015;98:187–96. doi:10.1016/j.mvr.2014.02.001.
Schepers E, Glorieux G, Dhondt A, et al. Role of symmetric dimethylarginine in vascular damage by increasing ROS via store-operated calcium influx in monocytes. Nephrol Dial Transplant. 2009;24(5):1429–35. doi:10.1093/ndt/gfn670.
Pratico D, Iuliano L, Mauriello A, et al. Localization of distinct F2-isoprostanes in human atherosclerotic lesions. J Clin Invest. 1997;100(8):2028–34. doi:10.1172/JCI119735.
Yla-Herttuala S, Palinski W, Rosenfeld ME, et al. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest. 1989;84(4):1086–95. doi:10.1172/JCI114271.
Maritim AC, Sanders RA, Watkins JB 3rd. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol. 2003;17(1):24–38. doi:10.1002/jbt.10058.
Totter JR. Spontaneous cancer and its possible relationship to oxygen metabolism. Proc Natl Acad Sci. 1980;77(4):1763–7.
Wu JD, Lin DW, Page ST, et al. Oxidative DNA damage in the prostate may predispose men to a higher risk of prostate cancer. Transl Oncol. 2009;2(1):39–45.
Christen Y. Oxidative stress and Alzheimer disease. Am J Clin Nutr. 2000;71(2):621S–9S.
Gjevestad GO, Holven KB, Ulven SM. Effects of exercise on gene expression of inflammatory markers in human peripheral blood cells: a systematic review. Curr Cardiovasc Risk Rep. 2015;9(7):34. doi:10.1007/s12170-015-0463-4.
Gleeson M, Bishop NC, Stensel DJ, et al. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607–15. doi:10.1038/nri3041.
Dias RG, Silva MS, Duarte NE, et al. PBMCs express a transcriptome signature predictor of oxygen uptake responsiveness to endurance exercise training in men. Physiol Genomics. 2015;47(2):13–23. doi:10.1152/physiolgenomics.00072.2014.
Radom-Aizik S, Zaldivar FP Jr, Haddad F, et al. Impact of brief exercise on circulating monocyte gene and microRNA expression: implications for atherosclerotic vascular disease. Brain Behav Immun. 2014;39:121–9. doi:10.1016/j.bbi.2014.01.003.
Fernandez-Gonzalo R, De Paz JA, Rodriguez-Miguelez P, et al. Effects of eccentric exercise on toll-like receptor 4 signaling pathway in peripheral blood mononuclear cells. J Appl Physiol (1985). 2012;112(12):2011–8. doi:10.1152/japplphysiol.01499.2011.
Puterman E, Lin J, Blackburn E, et al. The power of exercise: buffering the effect of chronic stress on telomere length. PLoS One. 2010;5(5):e10837. doi:10.1371/journal.pone.0010837.
Gordon B, Chen S, Durstine JL. The effects of exercise training on the traditional lipid profile and beyond. Curr Sports Med Rep. 2014;13(4):253–9. doi:10.1249/JSR.0000000000000073.
Roque FR, Hernanz R, Salaices M, et al. Exercise training and cardiometabolic diseases: focus on the vascular system. Curr Hypertens Rep. 2013;15(3):204–14. doi:10.1007/s11906-013-0336-5.
Halliwell B, Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol. 2004;142(2):231–55. doi:10.1038/sj.bjp.0705776.
Fisher-Wellman K, Bloomer RJ. Acute exercise and oxidative stress: a 30 year history. Dyn Med. 2009;8:1. doi:10.1186/1476-5918-8-1.
Camiletti-Moirón D, Aparicio VA, Aranda P, et al. Does exercise reduce brain oxidative stress? A systematic review. Scand J Med Sci Sports. 2013;23(4):e202–12.
Bouzid MA, Filaire E, McCall A, et al. Radical oxygen species, exercise and aging: an update. Sports Med. 2015;45(9):1245–61. doi:10.1007/s40279-015-0348-1.
Edwards DG, Schofield RS, Lennon SL, et al. Effect of exercise training on endothelial function in men with coronary artery disease. Am J Cardiol. 2004;93(5):617–20. doi:10.1016/j.amjcard.2003.11.032.
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(6):377–84.
Ruiz JR, Castro-Pinero J, Artero EG, et al. Predictive validity of health-related fitness in youth: a systematic review. Br J Sports Med. 2009;43(12):909–23. doi:10.1136/bjsm.2008.056499.
Borenstein M, Hedges LV, Higgins JPT, et al. Introduction to meta-analysis. West Sussex: Wiley; 2011.
Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60. doi:10.1136/bmj.327.7414.557.
Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.
Cohen J. Statistical power analysis for the behavioral sciences. Cambridge: Academic Press; 2013.
Faul F, Erdfelder E, Lang AG, et al. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–91.
Linke A, Adams V, Schulze PC, et al. Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation. 2005;111(14):1763–70. doi:10.1161/01.CIR.0000165503.08661.E5.
Kelly AS, Steinberger J, Olson TP, et al. In the absence of weight loss, exercise training does not improve adipokines or oxidative stress in overweight children. Metabolism. 2007;56(7):1005–9. doi:10.1016/j.metabol.2007.03.009.
Onur E, Kabaroglu C, Gunay O, et al. The beneficial effects of physical exercise on antioxidant status in asthmatic children. Allergol Immunopathol (Madr). 2011;39(2):90–5. doi:10.1016/j.aller.2010.04.006.
Dennis BA, Ergul A, Gower BA, et al. Oxidative stress and cardiovascular risk in overweight children in an exercise intervention program. Child Obes. 2013;9(1):15–21. doi:10.1089/chi.2011.0092.
Garcia-Lopez D, Hakkinen K, Cuevas MJ, et al. Effects of strength and endurance training on antioxidant enzyme gene expression and activity in middle-aged men. Scand J Med Sci Sports. 2007;17(5):595–604. doi:10.1111/j.1600-0838.2006.00620.x.
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(12):2065–72.
Azizbeigi K, Azarbayjani MA, Peeri M, et al. The effect of progressive resistance training on oxidative stress and antioxidant enzyme activity in erythrocytes in untrained men. Int J Sport Nutr Exerc Metab. 2013;23(3):230–8.
Karabolut AB, Kafkas ME, Kafkas AS, et al. The effect of regular exercise and massage on oxidant and antioxidant parameters. Indian J Physiol Pharmacol. 2013;57(4):6.
Beltran Valls MR, Dimauro I, Brunelli A, et al. Explosive type of moderate-resistance training induces functional, cardiovascular, and molecular adaptations in the elderly. Age (Dordr). 2014;36(2):759–72. doi:10.1007/s11357-013-9584-1.
Sallam N, Laher I. Exercise modulates oxidative stress and inflammation in aging and cardiovascular diseases. Oxid Med Cell Longev. 2016;2016:7239639. doi:10.1155/2016/7239639.
Konopka AR, Sreekumaran Nair K. Mitochondrial and skeletal muscle health with advancing age. Mol Cell Endocrinol. 2013;379(1–2):19–29. doi:10.1016/j.mce.2013.05.008.
Bejma J, Ji LL. Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol (1985). 1999;87(1):465–70.
Malbut KE, Dinan S, Young A. Aerobic training in the ‘oldest old’: the effect of 24 weeks of training. Age Ageing. 2002;31(4):255–60.
Kallinen M, Sipila S, Alen M, et al. Improving cardiovascular fitness by strength or endurance training in women aged 76–78 years. A population-based, randomized controlled trial. Age Ageing. 2002;31(4):247–54.
Bacon AP, Carter RE, Ogle EA, et al. VO2max trainability and high intensity interval training in humans: a meta-analysis. PLoS One. 2013;8(9):e73182. doi:10.1371/journal.pone.0073182.
Vincent HK, Bourguignon C, Vincent KR. Resistance training lowers exercise-induced oxidative stress and homocysteine levels in overweight and obese older adults. Obesity (Silver Spring). 2006;14(11):1921–30. doi:10.1038/oby.2006.224.
Jain SK, McVie R. Effect of glycemic control, race (white versus black), and duration of diabetes on reduced glutathione content in erythrocytes of diabetic patients. Metabolism. 1994;43(3):306–9.
Obrosova IG, Van Huysen C, Fathallah L, et al. An aldose reductase inhibitor reverses early diabetes-induced changes in peripheral nerve function, metabolism, and antioxidative defense. FASEB J. 2002;16(1):123–5. doi:10.1096/fj.01-0603fje.
Mitranun W, Deerochanawong C, Tanaka H, et al. Continuous vs interval training on glycemic control and macro- and microvascular reactivity in type 2 diabetic patients. Scand J Med Sci Sports. 2014;24(2):e69–76. doi:10.1111/sms.12112.
Kurban S, Mehmetoglu I, Yerlikaya HF, et al. Effect of chronic regular exercise on serum ischemia-modified albumin levels and oxidative stress in type 2 diabetes mellitus. Endocr Res. 2011;36(3):116–23. doi:10.3109/07435800.2011.566236.
Gordon LA, Morrison EY, McGrowder DA, et al. Effect of exercise therapy on lipid profile and oxidative stress indicators in patients with type 2 diabetes. BMC Complement Altern Med. 2008;8:21. doi:10.1186/1472-6882-8-21.
de Oliveira VN, Bessa A, Jorge ML, et al. The effect of different training programs on antioxidant status, oxidative stress, and metabolic control in type 2 diabetes. Appl Physiol Nutr Metab. 2012;37(2):334–44. doi:10.1139/h2012-004.
Gomes VA, Casella-Filho A, Chagas AC, et al. Enhanced concentrations of relevant markers of nitric oxide formation after exercise training in patients with metabolic syndrome. Nitric Oxide. 2008;19(4):345–50. doi:10.1016/j.niox.2008.08.005.
Rosety-Rodríguez M, Díaz-Ordonez A, Rosety I, et al. Mejora de defensas antioxidantes mediante ejercicio aeróbico en mujeres con síndrome metabólico [Aerobic training improves antioxidant defense system in women with metabolic syndrome]. Medicina. 2012;72(1):4.
Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(6):1615–25.
Maechler P, Jornot L, Wollheim CB. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J Biol Chem. 1999;274(39):27905–13.
Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes. 2015;6(3):456–80. doi:10.4239/wjd.v6.i3.456.
Braith RW, Schofield RS, Hill JA, et al. Exercise training attenuates progressive decline in brachial artery reactivity in heart transplant recipients. J Heart Lung Transplant. 2008;27(1):52–9. doi:10.1016/j.healun.2007.09.032.
Beck DT, Martin JS, Casey DP, et al. Exercise training improves endothelial function in resistance arteries of young prehypertensives. J Hum Hypertens. 2014;28(5):303–9. doi:10.1038/jhh.2013.109.
Luk TH, Dai YL, Siu CW, et al. Effect of exercise training on vascular endothelial function in patients with stable coronary artery disease: a randomized controlled trial. Eur J Prev Cardiol. 2012;19(4):830–9. doi:10.1177/1741826711415679.
Grossman E. Does increased oxidative stress cause hypertension? Diabetes Care. 2008;31(Suppl 2):S185–9. doi:10.2337/dc08-s246.
Ghoreishian H, Tohidi M, Derakhshan A, et al. Presence of hypertension modifies the impact of insulin resistance on incident cardiovascular disease in a Middle Eastern population: the Tehran Lipid and Glucose Study. Diabet Med. 2015;32(10):1311–8. doi:10.1111/dme.12733.
Schiffrin EL, Canadian Institutes of Health Research Multidisciplinary Research Group on Hypertension. Beyond blood pressure: the endothelium and atherosclerosis progression. Am J Hypertens. 2002;15(10 Pt 2):115S–22S.
López-Suárez A, Bascuñana-Quirell A, Beltrán-Robles M, et al. Metabolic syndrome does not improve the prediction of 5-year cardiovascular disease and total mortality over standard risk markers. Prospective population based study. Medicine. 2014;93(27):e212.
Bastani NE, Kostovski E, Sakhi AK, et al. Reduced antioxidant defense and increased oxidative stress in spinal cord injured patients. Arch Phys Med Rehabil. 2012;93(12):2223–8 e2. doi:10.1016/j.apmr.2012.06.021.
LaVela SL, Evans CT, Prohaska TR, et al. Males aging with a spinal cord injury: prevalence of cardiovascular and metabolic conditions. Arch Phys Med Rehabil. 2012;93(1):90–5. doi:10.1016/j.apmr.2011.07.201.
Ordonez FJ, Rosety MA, Camacho A, et al. Arm-cranking exercise reduced oxidative damage in adults with chronic spinal cord injury. Arch Phys Med Rehabil. 2013;94(12):2336–41. doi:10.1016/j.apmr.2013.05.029.
Wadley AJ, Veldhuijzen van Zanten JJ, Stavropoulos-Kalinoglou A, et al. Three months of moderate-intensity exercise reduced plasma 3-nitrotyrosine in rheumatoid arthritis patients. Eur J Appl Physiol. 2014;114(7):1483–92. doi:10.1007/s00421-014-2877-y.
Lee DM, Weinblatt ME. Rheumatoid arthritis. Lancet. 2001;358(9285):903–11. doi:10.1016/S0140-6736(01)06075-5.
Wadley AJ, Veldhuijzen van Zanten JJ, Aldred S. The interactions of oxidative stress and inflammation with vascular dysfunction in ageing: the vascular health triad. Age (Dordr). 2013;35(3):705–18. doi:10.1007/s11357-012-9402-1.
Hakkinen A, Sokka T, Kautiainen H, et al. Sustained maintenance of exercise induced muscle strength gains and normal bone mineral density in patients with early rheumatoid arthritis: a 5 year follow up. Ann Rheum Dis. 2004;63(8):910–6. doi:10.1136/ard.2003.013003.
Jenner P. Oxidative stress in Parkinson’s disease. Ann Neurol. 2003;53(Suppl 3):S26–36. doi:10.1002/ana.10483 (discussion S-8).
Tuon T, Valvassori SS, Lopes-Borges J, et al. Physical training exerts neuroprotective effects in the regulation of neurochemical factors in an animal model of Parkinson’s disease. Neuroscience. 2012;227:305–12. doi:10.1016/j.neuroscience.2012.09.063.
Maes M, Galecki P, Chang YS, et al. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35(3):676–92. doi:10.1016/j.pnpbp.2010.05.004.
Schuch FB, Vasconcelos-Moreno MP, Borowsky C, et al. The effects of exercise on oxidative stress (TBARS) and BDNF in severely depressed inpatients. Eur Arch Psychiatry Clin Neurosci. 2014;264(7):605–13. doi:10.1007/s00406-014-0489-5.
Bloomer RJ, Schilling BK, Karlage RE, et al. Effect of resistance training on blood oxidative stress in Parkinson disease. Med Sci Sports Exerc. 2008;40(8):1385–9. doi:10.1249/MSS.0b013e31816f1550.
Arikawa AY, Thomas W, Gross M, et al. Aerobic training reduces systemic oxidative stress in young women with elevated levels of F2-isoprostanes. Contemp Clin Trials. 2013;34(2):212–7. doi:10.1016/j.cct.2012.11.003.
Chandwaney R, Leichtweis S, Leeuwenburgh C, et al. Oxidative stress and mitochondrial function in skeletal muscle: effects of aging and exercise training. Age (Omaha). 1998;21(3):109–17. doi:10.1007/s11357-998-0017-5.
Daussin FN, Rasseneur L, Bouitbir J, et al. Different timing of changes in mitochondrial functions following endurance training. Med Sci Sports Exerc. 2012;44(2):217–24. doi:10.1249/MSS.0b013e31822b0bd4.
Phillips SM, Winett RA. Uncomplicated resistance training and health-related outcomes: evidence for a public health mandate. Curr Sports Med Rep. 2010;9(4):208–13. doi:10.1249/JSR.0b013e3181e7da73.
Holviala J, Kraemer WJ, Sillanpaa E, et al. Effects of strength, endurance and combined training on muscle strength, walking speed and dynamic balance in aging men. Eur J Appl Physiol. 2012;112(4):1335–47. doi:10.1007/s00421-011-2089-7.
Li JX, Hong Y, Chan KM. Tai chi: physiological characteristics and beneficial effects on health. Br J Sports Med. 2001;35(3):148–56.
Elwy AR, Groessl EJ, Eisen SV, et al. A systematic scoping review of yoga intervention components and study quality. Am J Prev Med. 2014;47(2):220–32. doi:10.1016/j.amepre.2014.03.012.
Pescatello LS, Arena R, Riebe D, Thompson PD, editors. ACSM’s guidelines for exercise testing and prescription. American College of Sports Medicine. Baltimore: Lippincott Williams & Wilkins; 2013.
Goon JA, Aini AH, Musalmah M, et al. Effect of tai chi exercise on DNA damage, antioxidant enzymes, and oxidative stress in middle-age adults. J Phys Act Health. 2009;6(1):43–54.
Rosado-Pérez J, Santiago-Osorio E, Ortiz R, et al. Tai chi diminishes oxidative stress in Mexican older adults. J Nutr Health Aging. 2012;16(7):5.
Buttle H. Measuring a journey without goal: meditation, spirituality, and physiology. Biomed Res Int. 2015;2015:891671. doi:10.1155/2015/891671.
Kabat-Zinn J, Massion AO, Kristeller J, et al. Effectiveness of a meditation-based stress reduction program in the treatment of anxiety disorders. Am J Psychiatry. 1992;149(7):936–43.
Rahal A, Kumar A, Singh V, et al. Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int. 2014;2014:761264. doi:10.1155/2014/761264.
Hamberg-van Reenen HH, Ariëns GAM, Blatter BM, et al. A systematic review of the relation between physical capacity and future low back and neck/shoulder pain. Pain. 2007;130(1):93–107.
Vinetti G, Mozzini C, Desenzani P, et al. Supervised exercise training reduces oxidative stress and cardiometabolic risk in adults with type 2 diabetes: a randomized controlled trial. Sci Rep. 2015;5:9238. doi:10.1038/srep09238.
Soares JP, Silva AM, Oliveira MM, et al. Effects of combined physical exercise training on DNA damage and repair capacity: role of oxidative stress changes. Age (Dordr). 2015;37(3):9799. doi:10.1007/s11357-015-9799-4.
Johnson ML, Irving BA, Lanza IR, et al. Differential effect of endurance training on mitochondrial protein damage, degradation, and acetylation in the context of aging. J Gerontol A Biol Sci Med Sci. 2015;70(11):1386–93. doi:10.1093/gerona/glu221.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
The authors are thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting scholarships at undergraduate research (CNPq), MSc (CAPES), and PhD (CAPES) levels. No specific sources of funding were used to assist in the preparation of this article.
Conflict of interest
Caio Victor de Sousa, Marcelo Magalhães Sales, Thiago Santos Rosa, John Eugene Lewis, Rosangela Vieira de Andrade, and Herbert Gustavo Simões have no conflicts of interest relevant to the content of this review.
Additional information
C. V. de Sousa and M. M. Sales contributed equally to this work.
Rights and permissions
About this article
Cite this article
de Sousa, C.V., Sales, M.M., Rosa, T.S. et al. The Antioxidant Effect of Exercise: A Systematic Review and Meta-Analysis. Sports Med 47, 277–293 (2017). https://doi.org/10.1007/s40279-016-0566-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40279-016-0566-1