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Bosn J Basic Med Sci 2014; 14 (2): 57-62

ALMIRA HADOVI DUVO E AL.: OXIDA IVE S RESS S A US IN ELI E A HLE ES ENGAGED IN DIFFEREN SPOR DISCIPLINES

sary for important physiological functions such ascell signaling, immune response, and apoptosis [ ].Many studies have shown that exercise induces oxidativestress and causes adaptations in antioxidant defences [ , ].raining can have positive or negative effects on oxidativestress depending on training load, training specificity andthe basal level of training. Data suggest that regular longterm training can induce antioxidant response to the oxida-tive stress. Te results of a study which investigated the rela-tionship between oxidative stress and exercise overtraining/overreaching support the possibility that the beneficial ef-fect of physical exercise on oxidative stress might be associ-ated with increased antioxidant defences [ ]. It is also wellknown that active and non active skeletal muscles producereactive oxygen and nitrogen species although it is not quiteclear where oxidants originate during physical activity [ ].Te degree of oxidative damage, as well as the time coursefor elevation in oxidative stress markers has varied acrossstudies, and appears to be dependent, among all, on thetype, intensity, volume and duration of exercise [ ].his leads to differences in oxidative status betweenathletes in different sport disciplines, but the resultsof the previous studies are inconsistent. herefore theaim of our study was to estimate oxidative stress statusin elite athletes engaged in different sports disciplines.

MATERIALS AND METHODS

Subjectshe study was performed on young ( . . yearsold) male elite players. All the athletes were highly skilledprofessional competitors with international experience(two Olympic players) in three sport disciplines: wres-tlers, soccer players and basketball players. All par-ticipants underwent routine health checks and gave writ-ten informed consent to participate in the study. Allparticipants completed a questionnaire assessing their dailyand weekly training workload, duration of professionalsports involvement. Any participant with suspect patho-logical findings during physical examination, recent his-tory of disease or injuries, intake of medications that mighthave had influence on oxidative markers were excluded.All study procedures were in accordance with the Helsinkideclaration. he study was approved by the Ethical com-mittee of the Faculty of Medicine, University of Sarajevo.

Procedures

wo days prior to taking part in the study all participants re-frained from strenuous physical training. One month prior toblood sampling, the athletes were instructed to abstain fromany vitamin or antioxidant dietary supplementation. All par-

ticipants were nonsmokers. Before the beginning of the study,athletes passed standard sports-medicine examination thatincluded a health questionnaire, electrocardiographic exami-nation, blood pressure and anthropometrical measurement.BMI for each subject was calculated (weight in kilogramsdivided by height in meters squared). Height was measuredwith stadiometer and weight was measured with oledoself-zeroing electronic digital scale (Mettler- oledo, Inc.,Worthington, OH.). rained persons measured blood pres-sure using a mercury sphygmomanometer (MD XX, MEDI,Shanghai, China) on the right arm after at least a -min rest.

Biochemical analysisBlood samples were taken from athletes in order todetermine the redox state. As the markers of oxida-tive stress we used advanced oxidation protein prod-ucts (AOPP) and malondialdechyde (MDA) andImAnOx as marker of total antioxidative capacity.Blood samples were taken from an antecubital vein intoVacutainer test ED A tube and stored immediately.

AOPP Assay Determination of AOPP was based on spectroscopicanalysis of modified proteins using AOPP assay kit (Im-munodiagnostic AG). Standards, controls and samplesassayed for AOPP were placed in each well of a -well

microtiter plate. Te absorbance at nm was measuredat microplate reader (Statfax , USA). Concentra-tion of AOPP is expressed in hloramine units (mol/l).

MDA Assay Level of malondialdehyde in plasma was determined by us-ing ELISA assay kit for MDA (Uscn Life Science Inc.). Tisassay employs the competitive enzyme immunoassay tech-nique. A monoclonal antibody specic for MDA has beenpre-coated onto a microplate. A competitive inhibitionreaction is launched between biotin labeled MDA and un-labeled MDA (standards and samples) with the pre-coatedantibody specic for MDA. After incubation the unboundconjugate is washed off. Avidin conjugated to Horserad-ish Peroxidase (HRP) is added to each microplate well andincubated. Te amount of bound HRP conjugate is reverseproportional concentration of MDA in the sample. Af-ter addition of the substrate solution, the intensity of colordeveloped was reverse proportional to the concentrationof MDA in sample. he absorbance was read at nm.

ImAnOx (Total antioxidative capacity-TAC)Te determination of the total antioxidative capacity is per-formed by photometric test system ImAnOX (Immuno-diagnostic AG, Bensheim). Te antioxidants in the sample


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ALMIRA HADOVI DUVO E AL.: OXIDAIVE S RESS S AUS IN ELI E A HLE ES ENGAGED IN DIFFEREN SPOR DISCIPLINES

reacted with the dened amount of exogenously providedhydrogen peroxide (H O ) and eliminated a certain amount.Te residual H O is determined photometrically by an en-zymatic reaction. Te absorbance was measured at nm.

Statistical analysisValues are expressed as meanSEM or median and inter-quartile range depending on data distribution. Normaldistribution of continuous variables was tested using Sha-piro-Wilk test. Differences in mean between groups weretested using ANOVA followed by post hoc uckey testand differences in median between the groups were testedby use of Kruskal-Wallis test followed by Mann-Whitneystest. Associations between continuous variables were test-ed with Spearmans rank or Pearson correlation analysis.

RESULTS

Baseline characteristics of the male elite athletes aregiven in able . here was no significant difference inage and training habits between soccer players, wres-tlers or basketball players. However, mean weight wasfound to be significantly higher in basketball compared

to soccer players, while mean BMI was significantlyhigher in wrestlers compared to soccer players ( able .).he mean AOPP concentration in soccer players was. . mol/L, in wrestlers . . mol/L and. . mol/L in basketball players, but the dif-

ference was not significant ( p= . , NS)(Figure ).Te mean ImAnOX concentration was . . mol/L insoccer players, . . mol/L in wrestlers and . .

FIGURE 1. AOPP concentration in male elite athletes.Concentration of AOPP is expressed in chloramine units (mol/l).

FIGURE 2. ImAnOx concentration in male elite athletes.

FIGURE 3. MDA concentration in male elite athletes.* soccer playersvs . wrestlers**wrestlersvs . basketball players*** soccer playersvs . basketball players

Soccerplayers Wrestlers Basketballplayers P value

Age (y) 22.14.4 21.76.0 20.22.3 NSWeight (kg) 74.99.4 85.916.6 93.011.3 ** p=0.004BMI (kg/m2) 22.61.8 26.34.4 23.61.5 * p=0.024Duration of training (y) 13.24.112.35.6 10.53.1 NSraining frequency(nr/week) 6.20.8 6.01.0 9.80.8 NS

TABLE 1. Baseline characteristics of male elite athletes.

* soccer playersvs . wrestlers** soccer playersvs . basketball players

AOPP ImAnOx MDAAge (y) r=-0.19 r=0.33 r=-0.07Weight (kg) r=-0.2 r=0.11 r=-0.1BMI (kg/m2) r=-0.35 r=0.18 r=-0.1Duration of training (y) r=-0.15 r=0.12 r=-0.17

TABLE 2. Correlation coeffi cients between age, antropometricparameters, duration of training and oxidant/antioxidant markersin soccer players


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mol/L in basketball players ( p= . ; NS)(Figure ).Mean MDA concentration was signicantly higher in bas-ketball players ( . . ng/mL) compared to soccerplayers ( . . ng/mL)( p= . ). here was no sig-nicant difference in MDA concentration between wrestlers( . . ng/mL), soccer or basketball players (Figure ).Tere was no signicant correlation of AOPP, ImanOx, MDAwith age and anthropometric characteristic in soccer play-ers, wrestlers and basketball players ( able , able , able). Duration of training was signicantly positively associatedwith MDA levers in basketball players (r= . ; p< . ) ( able, Figure ). here was no significant correlation betweenAOPP, ImAnOx and MDA levels in soccer players, wrestlersor basketball players ( able ). Tere was no signicant dif-ferences in AOPP, ImAnOx and MDA concentration in maleathlete players with or without supplement ( able ) and inmale elite athletes without supplement in different sport dis-ciplines ( able ).

DISCUSSION

While ROS are constantly produced in small quantities with-in biological systems, their presence increases when exposedto both environmental and physical stressors [ ]. Exerciseis one such stressor. Simply stated, any situation in whichthe consumption of oxygen is increased, as during physi-cal exercise, could result in an acute state of oxidative stress.In our study we evaluated oxidative stress status in elite ath-letes engaged in different sports disciplines including soccer,basketball and wrestling. We used AOPP (advanced oxida-tion protein products) and MDA (secondary product of lipidperoxidation) as markers of oxidative stress and ImAnOxas marker of total antioxidative capacity ( AC) which isdened as the sum of antioxidant activities of the nonspe-cic pool of antioxidants, consisting of antioxidant enzymes(GPX, catalase, superoxide dismutase), metal chelators, andnonspecic antioxidants (GSH, ascorbic acid, albumin, uricacid, tocopheroles, carotenoids, coenzyme-Q, bilirubin, andamino acids (cystein, methionine, tyrosine) [ ]. he re-sults of our study show that mean oxidative stress markers

levels, both AOPP and MDA and total antioxidant capac-ity in elite athletes included in the study were increasedcompared to referral values provided by the manufacturersuggesting that physical activity leads to increased ROS fol-

FIGURE 4. Relationship between duration of training and MDAconcentration in basketball players.

AOPP ImAnOx MDAAge (y) r=0.49 r=-0.1 r=-0.35Weight (kg) r=0.34 r=-0.04 r=-0.33BMI (kg/m2) r=0.28 r=-0.19 r=-0.32Duration of training (y) r=0.33 r=0.0 r=-0.37

TABLE 3. Correlation coeffi cients between age, antropometricparameters, duration of training and oxidant/antioxidant markersin wrestlers

AOPP ImAnOx MDAAge (y) r=-0.19 r=-0.1 r=-0.03Weight (kg) r=-0.2 r=-0.3 r=-0.47BMI (kg/m2) r=-0.35 r=-0.03 r=-0.1Duration of training (y) r=-0.15 r=0.4 r=0.58*

TABLE 4. Correlation coeffi cients between age, antropometricparameters, duration of training and oxidant/antioxidant markersin basketball players

* p


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lowed by increased antioxidant capacity in order to counterfight oxidative stress. Evidence for increased reactive oxy-gen and nitrogen species (RONS) production during andfollowing exercise is provided by numerous investigationsnoting an increase in various oxidative stress biomarkersfollowing both acute aerobic and anaerobic exercise [ ].In healthy males a period of intensified training elic-ited a biphasic AC response, a significant increase afterlow- and high-volume training, and a decline after very-high-volume training [ ]. he increase in AC suggeststhat the bodys antioxidant defense system is activatedduring exercise. Mobilization of antioxidant tissue storesmay help to maintain the antioxidant status if needed [ ].he results in other researches [ , ] where oxidativestress was assessed in elite soccer layers showed increasedlevels of oxidative stress but also an improved plasma anti-oxidant status together with more fluid erythrocyte mem-brane status, so they concluded that elevation in plasmaactivities of antioxidant enzymes and the higher levels offree radical scavengers of low molecular mass may com-pensate the oxidative stress caused by physical activity.Primary RONS generation in response to acute exercise canoccur via several pathways. hese include mitochondrialrespiration (electron leakage from electron transport chainand subsequent production of the superoxide radical), pros-tanoid metabolism, the autooxidation of catecholoamines,

and oxidase enzymatic activity (NAD(P)H oxidase, xanthineoxidase) [ ]. Te initial increase in RONS during exercise,as well as following cessation of the work bout can lead toadditional secondary generation of prooxidants via phago-cytic respiratory burst, a loss of calcium homeostasis and/or the destruction of iron-containing proteins. Moreover,while the pathways listed above represent potential sourcesof RONS during exercise, specic RONS generation likelydepends on the mode (aerobic, anaerobic), intensity, and du-ration of exercise, as varying types of exercise differ in theirrespective energy requirements, levels of oxygen consump-tion, and mechanical stresses imposed on the tissues [ ].Both acute aerobic and anaerobic exercise has the poten-tial to result in increased free radical production, whichmay or may not result in acute oxidative stress [ ]. In or-der for oxidative stress to occur, the ROS produced dur-ing exercise must exceed the antioxidant defense systempresent, thereby resulting in oxidative damage to specificbiomolecules. Different exercise protocols may induce varying levels of RONS production, as oxidative damagehas been shown to be both intensity and duration depen-

dent [ , ]. During low-intensity and duration protocols,antioxidant defenses appear sufficient to meet the RONSproduction, but as intensity and/or duration of exercise in-creases, these defenses are no longer adequate, potentially

resulting in oxidative damage to surrounding tissues [ ].Neubauer et al. [ ] showed in their study that in well trainedmen, competetors in triatlon, increased levels of analyzedbiomarkers of oxidative stress return to basal levels ve daysafter competetion and that there is also connection betweentraining state, markers of oxidative stress and activity of an-tioxidant enzymes. herefore, alternatives of antioxidantsystem defense in this trained population prevent appear-ance of long-term oxidative stress after intense exertion.Te results of studies which determined oxidative stress bio-markers and antioxidant status in different sport disciplinesshowed mostly increased levels of oxidative stress mark-ers but also more effective antioxidant protection. How-ever, there are only few studies which compared the levelsof oxidative stress markers among various sport disciplines.Our results showed no signicant differences in the levelsof oxidative stress status markers among various elite sportsathletes. Te difference in the mean concentrations of AOPPand ImAnOx between players of different sport disciplineswas not signicant. Mean MDA concentration was signi-cantly higher in basketball players comparing to soccer play-ers while there was no signicant difference in MDA con-centration between wrestlers, soccer or basketball players .Tese results are consistent with the results of Cubrilo et al.[ ] who assessed oxidative stress and nitrite dynamics un-der maximal load in elite athletes in relation to sport type

(aerobic, anaerobic and aerobic/anaerobic) measuring con-centration of lactates, nitric oxide and thiobarbituric reactivesubstances ( BARS) as index of lipid peroxidation. Teir re-sults showed long term different training strategies establishdifferent basal nitrites and lipid peroxidation levels in athleteswhich can be explained with different mechanisms of ROSinduction by aerobic and anaerobic exercise. Neverthelessthey found no statistically signicant difference in oxidativestress parameters regardless of sport type although averageconcentrations (tests instructions proposed values) indicatedhigh level of oxidative stress accompanied with increasedantioxidative response in all groups. Tis can be explainedwith the fact that aero-anaerobic type of physical activity in-cludes more mechanisms for production of oxidative stress.he results of a study by Stankovic et al. [ ] suggestedthat increased production of RONS, as well as oxidativestress occurs in top-quality sportsmen under maximalphysical exertion is independent of energetic require-ment of sport type (aerobic, anaerobic, aero-anaerobic).Te ndings of Shi et al. [ ] who in their study investigat-ed the differences in oxidative stress caused by aerobic and

anaerobic exercise due to different mechanisms suggestthat similar workloads of anaerobic and aerobic exerciseinduce ROS differently: aerobic exercise seems to initiallygenerate more ROS, whereas anaerobic exercise may in-


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duce prolonged ROS generation. Although more oxygenwas consumed during aerobic exercise, the generated ROSdid not induce significant oxidative damage, so they con-cluded that oxygen consumption per se may not be the ma- jor cause of exercise-induced oxidative damage. Te resultsof another study showed that aerobic training increasedGPx activity in erythrocytes with a subsequent decrease inplasma BARS (thiobarbituric reactive supstances) levelsbut anaerobic training had no effect on this process [ ].Different impact on oxidative stress during acute and pro-longed training was also shown by some studies. Pesic et al.[ ] evaluated oxidative status in elite karate players duringtraining session and their results showed that prolongedprogrammed physical exercise doesnt emphasize occur-rence of oxidative stress unlike acute maximal physical ex-ertion. Stankovic et al. [ ] monitored changes of particularbiomarkers of oxidative stress during tae-bo training andpilates training, where statistically significant increase oftotal antioxidant status was determined after tae-bo train-ing, as well as catalase activity in plasma after pilates train-ing. he authors suggested that sport athletes during lon-ger period of exercise develop more effective antioxidantdefence, respectively natural antioxidant defences of thebody respond adequately to complex training program.When interpreting our results and the results from our study,it is important to consider other factors which impact the

degree of antioxidant defences, including age, training status,and dietary intake [ ]. If oxidative stress does occur, detec-tion depends to a large degree on the tissue sampled, thetiming of a given sample, as well as the sensitivity and spec-icity of the biomarker chosen [ ]. In our study we chosetwo oxidative stress markers to analyse AOPP and MDAand found no difference in the average levels between dif-ferent sport types. Oxidative stress has also been assessedby way of a variety of other miscellaneous markers. Assess-ment of lipid peroxidation, with MDA and BARS are themost commonly used assays. the majority of authors havenoted an increase in BARS following a variety of exerciseprotocols, whereas null findings appear much more com-mon when measuring MDA or isoprostanes specificallysuggesting that BARS lack of specicity of the assay whichmight explain possible discrepancies of the results [ ].From work over the past three decades, it is clear that exer-cise of suffi cient volume, intensity, and duration can lead toan increase in RONS production, which may lead to the oxi-dation of several biological molecules (lipids, proteins, nucleicacids). Whether or not this condition is indicative of a harm-

ful stimulus however, remains a topic of debate [ ]. Tatis, due to the potential role of RONS in impairing exerciseperformance via altering contractile function and/or accel-erating muscle damage/fatigue (secondary to the oxidation

of contractile and/or mitochondrial enzymes), coupled withtheir association with human disease [ ], exercise-inducedRONS have commonly been viewed as a detriment to physi-ological function. Hence, methods to reduce radical produc-tion and subsequent oxidative damage during and followingphysical exercise have been a priority of much research activ-ity. While excessive prooxidant production, arising from anyform of extreme aerobic or anaerobic exercise (i.e., marathon,aerobic/anaerobic overtraining) may have the potential toresult in signicant cellular disruption, there presently existno "cause and effect" data to indicate that such an increasein RONS resulting from acute exercise actually causes ill-health and disease [ ]. o the contrary, and in accordancewith the principle of hormesis, a low grade oxidative stressappears necessary for various physiological adaptations [ ].Such a repeated exposure of the system to increased RONSproduction from chronic exercise training leads to an up-regulation in the body's antioxidant defense system andassociated shift in redox balance in favor of a more reduc-ing environment, thus providing adaptive protection fromRONS during subsequent training sessions, as well as whenexposed to non-exercise related conditions [ , ]. akentogether, exercise-induced oxidative stress may operate ina similar fashion to all other principles of exercise science.Tat is, in order for an adaptation to occur (e.g., increasedantioxidant defence, hypertrophy, strength), the physiologi-

cal stimulus applied (in this case RONS production) mustexceed a certain minimal threshold, effectively overload-ing the system. If overload is achieved, the physiologicalcapacity of the body will expand or adapt; ultimately lead-ing to improvements in health and/or human performance.

CONCLUSION

ype of sports (soccer, wrestler or basketball) have no impacton the levels of oxidative status markers. Elite sports engage-ment is a potent stimulus of oxidative stress that leads to thelarge recruitment of antioxidative defense implicating thatoxidative stress status should be monitored. Consumptionof antioxidants is recommended as a part of training regime.

DECLARATION OF INTEREST

he authors declare no conflict of interest for this study.

ACKNOWLEDGMENTS

his study was financed by Federal Ministry of Edu-cation and Science, project titled Impact of train-ing type on oxidative status in elithe sport (Agree-ment between University of Sarajevo and Federal


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Ministry of Education and Science No - - - / ).he part of the results were presented at th An-uual Congress of the European College of Sport Sci-ence, which was held in Barcelona th- th June, .

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