Research ArticleEffects of Concurrent Training on Oxidative Stress and InsulinResistance in Obese Individuals

Niara da Silva Medeiros Fabiana Guichard de AbreuAlana Schraiber Colato Leandro Silva de Lemos Thiago Rozales RamisGilson Pires Dorneles Claacuteudia Funchal and Caroline Dani

Centro Universitario Metodista IPA 90420-060 Porto Alegre RS Brazil

Correspondence should be addressed to Caroline Dani carolinedaniyahoocombr

Received 19 November 2014 Revised 7 January 2015 Accepted 15 January 2015

Academic Editor Vladimir Jakovljevic

Copyright copy 2015 Niara da Silva Medeiros et alThis is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Obesity is associated with insulin resistance (IR) and increased oxidative stress Thus the present study aimed to evaluateanthropometric parameters IR and oxidative stress in obese individuals subjected to two types of concurrent training at the sameintensity but differing in frequency Accordingly 25 individuals were divided into two groups concurrent training 1 (CT1) (5 dwk)and concurrent training 2 (CT2) (3 dwk) both with moderate intensity Anthropometric parameters IR and oxidative stress wereanalyzed before and after 26 sessions of training Both groups had reduced body weight and body mass index (119875 lt 005) but onlyCT1 showed lower body fat percentage and increased basal metabolic rate (119875 lt 005) Moreover CT1 had increased HOMA-IRand decreased protein damage (carbonyl level) and CT2 had decreased HOMA-IR and increased lipid peroxidation (TBARS level)(119875 lt 005) On the other hand both training protocols reduced the GPx activity It can be concluded that both types of concurrenttraining could be an alternative for lowering body weight and BMI Also it was observed that concurrent training depending onthe frequency can contribute to reducing body fat oxidative damage (protein oxidation) and IR but can induce oxidative damageto lipids More studies are needed to elucidate the mechanisms involved

1 Introduction

Sedentary lifestyle contributes to an increase in the inci-dence of obesity in most countries [1] Obesity is definedas a chronic and multifactorial disease which is associatedwith high mortality especially in industrialized areas [1]This disease is associated with many comorbidities such ascardiovascular complications hypertension atherosclerosischronic inflammation dyslipidemia insulin resistance (IR)diabetes mellitus (DM) and other metabolic disorders [1 2]

Furthermore studies show that obesity can cause in-creased reactive species production and a depletion of antiox-idant defenses leading to oxidative stress This conditioninduces oxidative damage to proteins lipids and DNA [3 4]Oxidative stress can be reduced by physical exercise withadequate frequency and intensity which can provide adaptivechanges to the regulation of antioxidant defenses resulting inless oxidative cell damage [5ndash7]

The benefits of regular physical exercise are well docu-mented [5] However there are few studies that approachthe benefits of concurrent training (aerobic plus strength)in the obese population Data demonstrate that this trainingcan help to lose weight and body fat and to gain lean bodymass [7 8] However it is still unclear how concurrenttraining modulates parameters of IR and oxidative stressin obese individuals Thus this study aimed to evaluateanthropometric parameters IR and oxidative stress in obeseindividuals subjected to concurrent training of moderateintensity but differing in frequency

2 Materials and Methods

21 Experimental Approach to the Problem Concurrenttraining consisted in aerobic exercise combinedwith strengthexercises The training was divided into two groups con-current training 1 (CT1) and concurrent training 2 (CT2)

Hindawi Publishing CorporationOxidative Medicine and Cellular LongevityVolume 2015 Article ID 697181 6 pageshttpdxdoiorg1011552015697181

2 Oxidative Medicine and Cellular Longevity

Table 1 Schedule of concurrent training

Sessions1ndash3lowast 4ndash9 10ndash15 16ndash21 22ndash24 25-26

Strength exercisesNumber of series 3 3 3 3 3Number of reps 15 12 10 08 15Intensity ( 1RM) 50 60 70 75 50Volume per session 45 36 30 24 45Recovery time 6010158401015840 9010158401015840 9010158401015840 9010158401015840 6010158401015840

Aerobic exercisesVolumetime 301015840 301015840 301015840 301015840 301015840

Intensity VO2peak 50 60 70 75 50Stage Borg scale 12 13 14 15 12lowastFirst 3 sessions to adapt to the exercises

In both training protocols the participants were subjectedto 26 sessions of 70 minutes each with the same progressiveintensity of 50ndash75 VO

2peak monitored by the Borg scale(Table 1) Each training session was divided into five minutesof initial warm-up 30 minutes of walking 30 minutes ofstrength exercises and five minutes of stretching CT1 wasperformed five days per week and CT2 three days per weekThese different training frequencies were used to check forchanges of oxidative profile and insulin resistance in obesesedentary individuals

22 Subjects The study was conducted in the Centro Univer-sitario Metodista IPA in southern Brazil The study includedindividuals gt18 years of age sedentary (no more than 150minutes of exercise per week) [9] with body mass index(BMI) of 30ndash40 kgm2

Thus this study consisted of 25 individuals 18women and7 menThe CT1 group was composed of 8 women and 4 menwith age of 4533plusmn1046 years and height of 16158plusmn619 cmThe CT2 group was composed of 10 women and 3 men withage of 4915plusmn 947 years and height of 16346plusmn 1043 cmThetwo groups did not differ statistically in baseline values of ageheight and BMI (119875 gt 005) indicating homogeneous groups

The exclusion criteria were subjects who reported a his-tory of autoimmune diseases cancer smoking and diseasesthat make it impossible to engage in physical exercise andorhad contraindications All participants read and signed aninformed consent form and also had a doctorrsquos permissionto perform physical exercise This study was approved bythe Research Ethics Committee of the Centro UniversitarioMetodista IPA under protocol 3712

23 Procedures Before the beginning of the training periodall individuals had a cardiorespiratory test which con-sisted of a progressive test until exhaustion on a treadmill(ATL Inbramed Millennium Porto Alegre Brazil) with anergospirometer (V02000 Medgraphics St Paul MinnesotaUSA) The test was conducted according to the modifiedBruce protocol [9] The Borg scale was used to monitor

the intensity of the test so that the intensity could be repro-duced during physical training To determine the intensity ofexercise and follow a progressive linear intensity the highestmean oxygen uptake (VO

2) during 30 seconds was expressed

as the peak oxygen uptake (VO2peak) because a VO2 plateau

was invariably not observed during the test although othercriteria for VO

2max given in the literature (ie RER gt 11and maximum HR within 10 beats of the age-appropriatereference value) were fulfilled [10]

To monitor the intensity of strength exercise maximaldynamic strength was assessed by the one repetition max-imum test (1RM) (following a progressive intensity of 50ndash75) [11] The 1RM test was performed for lower body bysquat exercise and for upper body by supine exercise with freeweights before starting the training period

Strength training was based on the method of alternatingsegments with the following exercises bench press withdumbbells plan squats shoulder abduction plantar flexionhorizontal pulley and abdominal crunch During trainingwe applied progressive intensity (50ndash75 1RM) as well asdecreased volume of repetitions in all exercises except forabdominal and plantar flexion The abdominal and plantarflexion exercises were performed with no load and fixed in 15repetitions

Anthropometric measurements were assessed before andafter the training period including body weight (kg) (Welmysemianalytical balance) height (cm) (Welmy stadiometer)BMI (defined as the weight (kg) divided by height (m)squared kgm2) abdomen waist and hip circumferences(cm) free fat mass (kg) body fat percentage () and basalmetabolic rate (kcal) by the bioelectrical impedance method(Byodinamics BIA 310e)

Moreover before and after the training period samples ofvenous blood were collected (10mL) without anticoagulantafter an overnight fast of 8 hours Serum was separated bycentrifugation at 1000 g for 10 minutes aliquoted and frozenat minus20∘C for further analysis

We analyzed fasting glucose (automatedmethod COBASC111 mgdL) fasting insulin (DRG Insulin ELISA Kit120583IUmL) and HOMA-IR (homeostasis model of IR) cal-culated by the formula (fasting insulin (120583IUmL) times fastingglucose (mmolL)225)

To evaluate the oxidative profile of the participantslipid peroxidation was determined by the thiobarbituric acidreactive substances (TBARS)method described byWills [12]Protein carbonyl levels were measured to determine proteinoxidation as described by Reznick and Packer [13] Totalsulfhydryl groups were assayed by the technique describedby Aksenov and Markesbery [14] We also determined theactivities of the antioxidant enzymes catalase (CAT) [15]superoxide dismutase (SOD) [16] and glutathione peroxidase(GPx) [17]

24 Statistical Analysis All variables were tested for normal-ity of distribution by the Shapiro-Wilk test For those thatshowed normality we used the paired 119905-test for comparisonof before and after training (mean plusmn standard error) Allanalyses were performed by the Statistical Package for Social

Oxidative Medicine and Cellular Longevity 3

Table 2 Anthropometric parameters of obese individuals before and after concurrent training with different frequencies

Anthropometric CT1 CT2parameters Before After 119875 Before After 119875

Body weight (kg) 9606 plusmn 432 9334 plusmn 426 lt0001 8998 plusmn 464 8720 plusmn 430 0013BMI (kgm2) 3673 plusmn 160 3568 plusmn 155 lt0001 3353 plusmn 103 3255 plusmn 100 0011FFM (kg) 5959 plusmn 290 6174 plusmn 325 0021 5641 plusmn 368 5727 plusmn 427 0541BF () 3735 plusmn 157 3378 plusmn 191 lt0001 3811 plusmn 098 3668 plusmn 139 0062WC (cm) 10294 plusmn 294 10191 plusmn 287 0177 9777 plusmn 255 9511 plusmn 268 0077AC (cm) 11327 plusmn 315 11114 plusmn 279 0074 10533 plusmn 169 10126 plusmn 125 0026HC (cm) 11755 plusmn 227 11323 plusmn 199 lt0001 11379 plusmn 201 11116 plusmn 180 0007BMR (kcal) 182582 plusmn 8700 187236 plusmn 9931 0033 171577 plusmn 11194 173554 plusmn 12926 0651Variables presented as mean plusmn standard error CT1 concurrent training 5 times per week CT2 concurrent training 3 times per week BMI body mass indexFFM free fat mass BF body fat percentage WC waist circumference AC abdominal circumference HC hip circumference BMR basal metabolic rate119875 lt 005 (significantly different) Paired 119905-test was utilized to compare before and after training in the same group

Table 3 Comparison of markers of insulin resistance and oxidative stress in obese individuals before and after concurrent training

CT1 CT2Before After 119875 Before After 119875

Insulin resistance markersFasting glucose (mgdL) 9650 plusmn 385 8566 plusmn 413 0096 10096 plusmn 376 8569 plusmn 413 0001Fasting insulin (uUImL) 1054 plusmn 084 1429 plusmn 077 0002 955 plusmn 077 854 plusmn 064 0293HOMA-IR 256 plusmn 026 377 plusmn 035 0005 234 plusmn 056 179 plusmn 052 0009

Oxidative stress markersTBARS (nmolmL) 369 plusmn 031 369 plusmn 011 0987 470 plusmn 017 635 plusmn 0049 0015Carbonyl (nmol DNPHmg) 11636 plusmn 1836 3445 plusmn 746 0012 2496 plusmn 967 2439 plusmn 857 0965Sulfhydryl (120583Mmg) 1183 plusmn 1103 903 plusmn 123 0145 520 plusmn 104 409 plusmn 041 0169CAT (UCATmg) 279 plusmn 066 473 plusmn 124 0281 326 plusmn 063 183 plusmn 028 0074SOD (USODmg 185 plusmn 050 240 plusmn 086 0667 129 plusmn 046 307 plusmn 138 0235GPx (UGPxmg) 386 plusmn 040 337 plusmn 037 lt0001 457 plusmn 045 422 plusmn 042 0002

Variables presented as mean plusmn standard error CT1 concurrent training 5 times per week CT2 concurrent training 3 times per week HOMA-IR homeostasismodel of insulin resistance TBARS thiobarbituric acid reactive substances CAT catalase activity SOD superoxide dismutase activity GPx glutathioneperoxidase activity119875 lt 005 (significantly different) Paired 119905-test was utilized to compare before and after training in the same group

Sciences (SPSS) program version 180 All statistical tests weretwo-tailed and performed using a significance level of 120572 =005

3 Results

It was observed that both training protocols were able toreduce body weight and BMI (Table 2) But only CT1 showedsignificantly decreased body fat percentage and increasedfree fat mass and BMR after the training period Regardingthe circumference measurements hip circumference wasdecreased in CT1 and abdomen and hip circumferences weredecreased in CT2 (Table 2)

With regard to IR parameters the CT1 group showed asignificant increase in fasting insulin level andHOMA-IR andno change in fasting glucoseHowever theCT2 group showeda significant decrease in fasting glucose level and HOMA-IRwith no change in fasting insulin (Table 3)

Finally for oxidative stress markers only carbonyls andGPx activity were reduced in the CT1 group while in theCT2 group the TBARS levels increased and GPx activitydecreased (Table 3)

4 Discussion

Exercise is a strong ally in the treatment of obesity andwhen performed with adequate intensity and frequency itcould provide protection against comorbidities of obesityThis includes improvement in the cardiovascular system(reduced blood pressure increased peripheral blood flowreduced atherosclerosis progression and decreased oxygendemand of the myocardium) reduced risk of developingtype 2 DM (by reducing IR) anxiety and depression andincreased metabolic rate [18ndash20]

It is known that aerobic exercise is beneficial in weightloss modulation of oxidative stress and reduction of IR inobese individuals [21 22] But there are few studies applyingthe strength exercise associated with aerobic exercise (con-current training) in this populationThis training can help toreduce body weight and fat mass by increasing lean mass andbasal metabolic rate [23ndash26]

These benefitswere observed in this study and both formsof concurrent trainings were able to reduce body weight andBMI CT1 (5xweek) also reduced the body fat percentage andhip circumference and even increased basal metabolic rateThese findings were also shown in a study by Willis et al [7]

4 Oxidative Medicine and Cellular Longevity

whodemonstrated a reduction inweight body fat percentageandwaist circumference in overweight adults who performedconcurrent training 3xweek with an intensity of 65ndash80VO2peakAnother study also showed that overweight individ-

uals who performed concurrent training for 12 weeks 5daysweek had a decrease in weight BMI body fat percent-age and waist circumference However in this same studytwo other groups that performed strength training or aerobictraining only had a decrease in waist circumference showingthe relevance of the type of training [6]

Our study also demonstrated a significant increase infree fat mass in CT1 which can result in neuromuscularadaptations such as increased muscle mass and maximalstrength dynamic capacity and can improve basal metabolicrate in obese individuals Also other studies have shown thatconcurrent training has positive effects in the development ofstrength and muscle mass in both healthy young individuals[27] and overweight dyslipidemic individuals [28]

Furthermore according to the IR data presented the CT1group showed an increase in fasting insulin level andHOMA-IR although this increase was still within normal range(2ndash25120583IUmL) On the other hand CT2 reduced glucoselevels and HOMA-IR but did not alter fasting insulin Inthe literature there are few studies demonstrating the roleof concurrent training in obese nondiabetics But a study ofsubjects with metabolic syndrome and type 2 DM showedthat concurrent training for 20 weeks at 70ndash80 VO

2peakreducedHOMA-IR as well as weight andwaist circumference[29] starting on the third week thereby corroborating ourfindings

Studies have shown a direct relationship between exerciseand insulin sensitivity [29 30] However a short time ofphysical activity is associated with low insulin sensitivityand a few days of rest are associated with increased IR [29ndash31] Thus regular exercise can improve insulin sensitivity inhealthy subjects and obese nondiabetics [19 32ndash34] Notablythe positive effect of exercise on insulin sensitivity has beendemonstrated 12ndash48 hours after the last session of exercisebut preexercise levels return in three or five days [35]highlighting the importance of regular exercise

IR is associated with obesity and both are related tooxidative stress Clinical and animal models studies haveshown that oxidative stress is a potential mediator of IRparticularly in skeletal muscle because there is an inverserelationship between oxidative stress and insulin action [36ndash38] Prolonged exposure to low levels of oxidative stressreduces insulin sensitivity (reduction in GLUT-4) [39] caus-ing defects in its signaling [40 41]

According to a study in a rat model of insulin-resistantobesity (Zucker) endurance training reduced protein oxida-tion (carbonyl) levels after training [36] This research groupalso reported that this exercise improved insulin action andglucose transport in the soleus plantar and cardiac muscles[37] These results are in line with our findings in concurrenttraining that is reduced damage to proteins (carbonyls)Furthermore another study with Wistar rats showed adecrease in lipid peroxidation (TBARS) increase in antioxi-dant enzyme SODactivity and reduction in triglyceride levels

when concurrent trainingwas performed 5xweek It was alsoobserved that this improvement in the antioxidant systemwas similar in the groups that performed exclusively aerobicor strength training [42]

Furthermore the CT2 group showed lower GPx activityand a trend (119875 = 007) towards a reduction in CAT activitybut no change in SOD activity and sulfhydryl level whichmay have contributed to the increase in TBARS in thisgroup It is well known that exercise promotes increasedoxidative stress because during exercise the rate of oxygenconsumption increases about 20 times and in exhaustiveexercise glutathione activity can be reduced [43] Perhapsthe intensity and frequency of CT2 were not sufficientto modulate antioxidant defenses and thereby induce thenecessary adjustments to reduce damage to lipids

Many tissues can produce reactive oxygen species duringphysical exercise Studies have investigated which organs areprimarily responsible for reactive oxygen species productionin exercising humans The lack of in vivo studies on thistopic is due to the difficulty of investigating the multifacetednature of exercise which involves several organ systems andthese organs are connecting through the increased energyrequirement of contracting skeletal muscles [44] Investiga-tors have assumed that skeletal muscle provides the majorsource of free radical and reactive oxygen species generationduring exercise [44] Nonetheless other tissues such as theheart lungs or blood may also contribute to the total bodygeneration of reactive oxygen species during exercise [44 45]

Studies have shown that prolonged or intense contractileactivity alters the physiological environment in muscle fibersresulting in conditions that predispose these fibers to higherrates of reactive oxygen species production Increased oxygenconsumption in muscle fibers lowers intracellular oxygentension during exercise which can promote increased reac-tive oxygen species production [46] Further a rise in muscletemperature increased CO

2tension and decreased cellular

pH are other exercise-related changes that can stimulate reac-tive oxygen species production in muscleThese contraction-induced changes can stimulate superoxide production atmultiple subcellular sites [46 47]

On the basis of this study concurrent training may be analternative to lowering weight and BMI but when training isperformed more frequently (5 times a week) these benefitscan be enhanced by reducing body fat and protein damageas well On the other hand the effects of such training onoxidative stress parameters and IR were contradictory andthus more studies are needed to elucidate the mechanisms ofconcurrent training in this population

Conflict of Interests

The authors have no conflict of interests to disclose in thisstudy

Acknowledgments

The authors are grateful to the study participants fortheir cooperation and collaborators for their dedication

Oxidative Medicine and Cellular Longevity 5

The financial support was provided by Centro UniversitarioMetodista do IPA and Coordenacao de Aperfeicoamento dePessoal de Nıvel Superior (CAPES) Dr A Leyva helped withEnglish editing of the paper

References

[1] S Jebb ldquoObesity causes and consequencesrdquo Womenrsquos HealthMedicine vol 1 no 1 pp 38ndash41 2004

[2] F Amirkhizi F Siassi M Djalali and A R ForoushanildquoEvaluation of oxidative stress and total antioxidant capacity inwomenwith general and abdominal adiposityrdquoObesity Researchand Clinical Practice vol 4 no 3 pp e209ndashe216 2010

[3] I Grattagliano V O Palmieri P Portincasa A Moschetta andG Palasciano ldquoOxidative stress-induced risk factors associatedwith the metabolic syndrome a unifying hypothesisrdquo TheJournal of Nutritional Biochemistry vol 19 no 8 pp 491ndash5042008

[4] S Furukawa T FujitaM Shimabukuro et al ldquoIncreased oxida-tive stress in obesity and its impact onmetabolic syndromerdquoTheJournal of Clinical Investigation vol 114 no 12 pp 1752ndash17612004

[5] R E Andersen and J M Jakicic ldquoInterpreting the physicalactivity guidelines for health and weight managementrdquo Journalof Physical Activity and Health vol 6 no 5 pp 651ndash656 2009

[6] S S Ho S S Dhaliwal A P Hills and S Pal ldquoThe effect of12 weeks of aerobic resistance or combination exercise trainingon cardiovascular risk factors in the overweight and obese in arandomized trialrdquo BMC Public Health vol 12 article 704 2012

[7] L H Willis C A Slentz L A Bateman et al ldquoEffects ofaerobic andor resistance training on bodymass and fat mass inoverweight or obese adultsrdquo Journal of Applied Physiology vol113 no 12 pp 1831ndash1837 2012

[8] E Ghahramanloo A W Midgley and D J Bentley ldquoThe effectof concurrent training on blood lipid profile and anthropomet-rical characteristics of previously untrained menrdquo Journal ofPhysical Activity and Health vol 6 no 6 pp 760ndash766 2009

[9] American College of Sports Medicine (ACSM) ACSMrsquos Guide-lines for Exercise Testing and Prescription Lippincott WilliamsampWilkins Baltimore Md USA 8th edition 2009

[10] E T Howley D R Bassett Jr and H G Welch ldquoCriteria formaximal oxygen uptake review and commentaryrdquo Medicineand Science in Sports and Exercise vol 27 no 9 pp 1292ndash13011995

[11] L A Brown C J Kerr P Whiting N Finer J McEneny and TAshton ldquoOxidant stress in healthy normal-weight overweightand obese individualsrdquoObesity vol 17 no 3 pp 460ndash466 2009

[12] E D Wills ldquoMechanisms of lipid peroxide formation in animaltissuesrdquo Biochemical Journal vol 99 no 3 pp 667ndash676 1966

[13] A Z Reznick and L Packer ldquoOxidative damage to proteinsspectrophotometric method for carbonyl assayrdquo Methods inEnzymology vol 233 pp 357ndash363 1994

[14] M Y Aksenov and W R Markesbery ldquoChanges in thiolcontent and expression of glutathione redox system genesin the hippocampus and cerebellum in Alzheimerrsquos diseaserdquoNeuroscience Letters vol 302 no 2-3 pp 141ndash145 2001

[15] H Aebi ldquo[13] Catalase in vitrordquo Methods in Enzymology vol105 pp 121ndash126 1984

[16] H PMisra and I Fridovich ldquoThe role of superoxide anion in theautoxidation of epinephrine and a simple assay for superoxide

dismutaserdquoThe Journal of Biological Chemistry vol 247 no 10pp 3170ndash3175 1972

[17] A Wendel ldquoGlutathione peroxidaserdquo Methods in Enzymologyvol 77 pp 325ndash333 1981

[18] T S Church C P Earnest J S Skinner and S N Blair ldquoEffectsof different doses of physical activity on cardiorespiratoryfitness among sedentary overweight or obese postmenopausalwomen with elevated blood pressurerdquo The Journal of theAmerican Medical Association vol 297 no 19 pp 2081ndash20912007

[19] D M Okay P V Jackson MMarcinkiewicz andM N PapinoldquoExercise and obesityrdquo Primary CaremdashClinics in Office Practicevol 36 no 2 pp 379ndash393 2009

[20] D E R Warburton C W Nicol and S S D Bredin ldquoHealthbenefits of physical activity the evidencerdquo Canadian MedicalAssociation Journal vol 174 no 6 pp 801ndash809 2006

[21] M F F Mediano and R Sichieri ldquoInsulin resistance influencesweight loss in non-obese women who followed a home-based exercise program and slight caloric restrictionrdquo DiabetesResearch and Clinical Practice vol 92 no 3 pp 361ndash367 2011

[22] G Murdolo M Piroddi F Luchetti et al ldquoOxidative stress andlipid peroxidation by-products at the crossroad between adi-pose organ dysregulation and obesity-linked insulin resistancerdquoBiochimie vol 95 no 3 pp 585ndash594 2013

[23] A Chatzinikolaou I Fatouros A Petridou et al ldquoAdiposetissue lipolysis is upregulated in lean and obese men duringacute resistance exerciserdquo Diabetes Care vol 31 no 7 pp 1397ndash1399 2008

[24] M J Ormsbee D C Myung J K Medlin et al ldquoRegulation offat metabolism during resistance exercise in sedentary lean andobese menrdquo Journal of Applied Physiology vol 106 no 5 pp1529ndash1537 2009

[25] H T Rabelo L A Bezerra D F Terra et al ldquoEffects of 24 weeksof progressive resistance training on knee extensors peak torqueand fat-free mass in older womenrdquoThe Journal of Strength andConditioning Research vol 25 no 8 pp 2298ndash2303 2011

[26] R AWashburn E P Kirk B K Smith et al ldquoOne set resistancetraining effect on body composition in overweight youngadultsrdquo Journal of Sports Medicine and Physical Fitness vol 52no 3 pp 273ndash279 2012

[27] S P Glowacki S E Martin AMaurerW Baek J S Green andS F Crouse ldquoEffects of resistance endurance and concurrentexercise on training outcomes in menrdquoMedicine and Science inSports and Exercise vol 36 no 12 pp 2119ndash2127 2004

[28] M I Schaun T Dipp J S Rossato et al ldquoThe effects ofperiodized concurrent and aerobic training on oxidative stressparameters endothelial function and immune response insedentary male individuals of middle agerdquo Cell Biochemistryand Function vol 29 no 7 pp 534ndash542 2011

[29] S Balducci S Zanuso A Nicolucci et al ldquoAnti-inflammatoryeffect of exercise training in subjects with type 2 diabetes andthe metabolic syndrome is dependent on exercise modalitiesand independent of weight lossrdquo Nutrition Metabolism andCardiovascular Diseases vol 20 no 8 pp 608ndash617 2010

[30] K L Rennie N McCarthy S Yazdgerdi M Marmot and EBrunner ldquoAssociation of the metabolic syndrome with bothvigorous and moderate physical activityrdquo International Journalof Epidemiology vol 32 no 4 pp 600ndash606 2003

[31] T A Lakka D E Laaksonen H-M Lakka et al ldquoSedentarylifestyle poor cardiorespiratory fitness and the metabolicsyndromerdquo Medicine and Science in Sports amp Exercise vol 35no 8 pp 1279ndash1286 2003

6 Oxidative Medicine and Cellular Longevity

[32] S E Kahn V G Larson J C Beard et al ldquoEffect of exerciseon insulin action glucose tolerance and insulin secretion inagingrdquoTheAmerican Journal of PhysiologymdashEndocrinology andMetabolism vol 258 no 6 pp E937ndashE943 1990

[33] J P Kirwan W M Kohrt D M Wojta R E Bourey andJ O Holloszy ldquoEndurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-oldmen andwomenrdquoThe Journals of Gerontology vol 48 no 3 pp M84ndashM90 1993

[34] J P Miller R E Pratley A P Goldberg et al ldquoStrengthtraining increases insulin action in healthy 50- to 65-yr-oldmenrdquo Journal of Applied Physiology vol 77 no 3 pp 1122ndash11271994

[35] J Eriksson S Taimela and V A Koivisto ldquoExercise and themetabolic syndromerdquo Diabetologia vol 40 no 2 pp 125ndash1351997

[36] V Saengsirisuwan T R Kinnick M B Schmit and E JHenriksen ldquoInteractions of exercise training and lipoic acid onskeletal muscle glucose transport in obese Zucker ratsrdquo Journalof Applied Physiology vol 91 no 1 pp 145ndash153 2001

[37] M K Teachey Z C Taylor T Maier et al ldquoInteractions ofconjugated linoleic acid and lipoic acid on insulin action in theobese Zucker ratrdquo Metabolism Clinical and Experimental vol52 no 9 pp 1167ndash1174 2003

[38] H Urakawa A Katsuki Y Sumida et al ldquoOxidative stress isassociated with adiposity and insulin resistance in menrdquo TheJournal of Clinical Endocrinology and Metabolism vol 88 no10 pp 4673ndash4676 2003

[39] A RudichN Kozlovsky R Potashnik andN Bashan ldquoOxidantstress reduces insulin responsiveness in 3T3-L1 adipocytesrdquoThe American Journal of PhysiologymdashEndocrinology andMetabolism vol 272 no 5 pp E935ndashE940 1997

[40] B A Maddux W See J C Lawrence Jr A L Goldfine I DGoldfine and J L Evans ldquoProtection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolarconcentrations of120572-lipoic acidrdquoDiabetes vol 50 no 2 pp 404ndash410 2001

[41] A Rudich A Tlrosh R Potashnik R Hemi H Kanety andN Bashan ldquoProlonged oxidative stress impairs insulin-inducedGLUT4 translocation in 3T3-L1 adipocytesrdquo Diabetes vol 47no 10 pp 1562ndash1569 1998

[42] J D Botezelli L T Cambri A C Ghezzi et al ldquoDifferentexercise protocols improvemetabolic syndromemarkers tissuetriglycerides content and antioxidant status in ratsrdquoDiabetologyand Metabolic Syndrome vol 3 no 1 article 35 2011

[43] L L Ji and R Fu ldquoResponses of glutathione system andantioxidant enzymes to exhaustive exercise and hydroperoxiderdquoThe Journal of Applied Physiology vol 72 no 2 pp 549ndash5541992

[44] S K Powers and M J Jackson ldquoExercise-induced oxidativestress cellularmechanisms and impact onmuscle force produc-tionrdquo Physiological Reviews vol 88 no 4 pp 1243ndash1276 2008

[45] MGNikolaidis andA Z Jamurtas ldquoBlood as a reactive speciesgenerator and redox status regulator during exerciserdquo Archivesof Biochemistry and Biophysics vol 490 no 2 pp 77ndash84 2009

[46] L F Ferreira and M B Reid ldquoMuscle-derived ROS and thiolregulation in muscle fatiguerdquo Journal of Applied Physiology vol104 no 3 pp 853ndash860 2008

[47] S K Powers W B Nelson and M B Hudson ldquoExercise-induced oxidative stress in humans cause and consequencesrdquoFree Radical BiologyampMedicine vol 51 no 5 pp 942ndash950 2011

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

2 Oxidative Medicine and Cellular Longevity

Table 1 Schedule of concurrent training

Sessions1ndash3lowast 4ndash9 10ndash15 16ndash21 22ndash24 25-26

Strength exercisesNumber of series 3 3 3 3 3Number of reps 15 12 10 08 15Intensity ( 1RM) 50 60 70 75 50Volume per session 45 36 30 24 45Recovery time 6010158401015840 9010158401015840 9010158401015840 9010158401015840 6010158401015840

Aerobic exercisesVolumetime 301015840 301015840 301015840 301015840 301015840

Intensity VO2peak 50 60 70 75 50Stage Borg scale 12 13 14 15 12lowastFirst 3 sessions to adapt to the exercises

In both training protocols the participants were subjectedto 26 sessions of 70 minutes each with the same progressiveintensity of 50ndash75 VO

2peak monitored by the Borg scale(Table 1) Each training session was divided into five minutesof initial warm-up 30 minutes of walking 30 minutes ofstrength exercises and five minutes of stretching CT1 wasperformed five days per week and CT2 three days per weekThese different training frequencies were used to check forchanges of oxidative profile and insulin resistance in obesesedentary individuals

22 Subjects The study was conducted in the Centro Univer-sitario Metodista IPA in southern Brazil The study includedindividuals gt18 years of age sedentary (no more than 150minutes of exercise per week) [9] with body mass index(BMI) of 30ndash40 kgm2

Thus this study consisted of 25 individuals 18women and7 menThe CT1 group was composed of 8 women and 4 menwith age of 4533plusmn1046 years and height of 16158plusmn619 cmThe CT2 group was composed of 10 women and 3 men withage of 4915plusmn 947 years and height of 16346plusmn 1043 cmThetwo groups did not differ statistically in baseline values of ageheight and BMI (119875 gt 005) indicating homogeneous groups

The exclusion criteria were subjects who reported a his-tory of autoimmune diseases cancer smoking and diseasesthat make it impossible to engage in physical exercise andorhad contraindications All participants read and signed aninformed consent form and also had a doctorrsquos permissionto perform physical exercise This study was approved bythe Research Ethics Committee of the Centro UniversitarioMetodista IPA under protocol 3712

23 Procedures Before the beginning of the training periodall individuals had a cardiorespiratory test which con-sisted of a progressive test until exhaustion on a treadmill(ATL Inbramed Millennium Porto Alegre Brazil) with anergospirometer (V02000 Medgraphics St Paul MinnesotaUSA) The test was conducted according to the modifiedBruce protocol [9] The Borg scale was used to monitor

the intensity of the test so that the intensity could be repro-duced during physical training To determine the intensity ofexercise and follow a progressive linear intensity the highestmean oxygen uptake (VO

2) during 30 seconds was expressed

as the peak oxygen uptake (VO2peak) because a VO2 plateau

was invariably not observed during the test although othercriteria for VO

2max given in the literature (ie RER gt 11and maximum HR within 10 beats of the age-appropriatereference value) were fulfilled [10]

To monitor the intensity of strength exercise maximaldynamic strength was assessed by the one repetition max-imum test (1RM) (following a progressive intensity of 50ndash75) [11] The 1RM test was performed for lower body bysquat exercise and for upper body by supine exercise with freeweights before starting the training period

Strength training was based on the method of alternatingsegments with the following exercises bench press withdumbbells plan squats shoulder abduction plantar flexionhorizontal pulley and abdominal crunch During trainingwe applied progressive intensity (50ndash75 1RM) as well asdecreased volume of repetitions in all exercises except forabdominal and plantar flexion The abdominal and plantarflexion exercises were performed with no load and fixed in 15repetitions

Anthropometric measurements were assessed before andafter the training period including body weight (kg) (Welmysemianalytical balance) height (cm) (Welmy stadiometer)BMI (defined as the weight (kg) divided by height (m)squared kgm2) abdomen waist and hip circumferences(cm) free fat mass (kg) body fat percentage () and basalmetabolic rate (kcal) by the bioelectrical impedance method(Byodinamics BIA 310e)

Moreover before and after the training period samples ofvenous blood were collected (10mL) without anticoagulantafter an overnight fast of 8 hours Serum was separated bycentrifugation at 1000 g for 10 minutes aliquoted and frozenat minus20∘C for further analysis

We analyzed fasting glucose (automatedmethod COBASC111 mgdL) fasting insulin (DRG Insulin ELISA Kit120583IUmL) and HOMA-IR (homeostasis model of IR) cal-culated by the formula (fasting insulin (120583IUmL) times fastingglucose (mmolL)225)

To evaluate the oxidative profile of the participantslipid peroxidation was determined by the thiobarbituric acidreactive substances (TBARS)method described byWills [12]Protein carbonyl levels were measured to determine proteinoxidation as described by Reznick and Packer [13] Totalsulfhydryl groups were assayed by the technique describedby Aksenov and Markesbery [14] We also determined theactivities of the antioxidant enzymes catalase (CAT) [15]superoxide dismutase (SOD) [16] and glutathione peroxidase(GPx) [17]

24 Statistical Analysis All variables were tested for normal-ity of distribution by the Shapiro-Wilk test For those thatshowed normality we used the paired 119905-test for comparisonof before and after training (mean plusmn standard error) Allanalyses were performed by the Statistical Package for Social

Oxidative Medicine and Cellular Longevity 3

Table 2 Anthropometric parameters of obese individuals before and after concurrent training with different frequencies

Anthropometric CT1 CT2parameters Before After 119875 Before After 119875

Body weight (kg) 9606 plusmn 432 9334 plusmn 426 lt0001 8998 plusmn 464 8720 plusmn 430 0013BMI (kgm2) 3673 plusmn 160 3568 plusmn 155 lt0001 3353 plusmn 103 3255 plusmn 100 0011FFM (kg) 5959 plusmn 290 6174 plusmn 325 0021 5641 plusmn 368 5727 plusmn 427 0541BF () 3735 plusmn 157 3378 plusmn 191 lt0001 3811 plusmn 098 3668 plusmn 139 0062WC (cm) 10294 plusmn 294 10191 plusmn 287 0177 9777 plusmn 255 9511 plusmn 268 0077AC (cm) 11327 plusmn 315 11114 plusmn 279 0074 10533 plusmn 169 10126 plusmn 125 0026HC (cm) 11755 plusmn 227 11323 plusmn 199 lt0001 11379 plusmn 201 11116 plusmn 180 0007BMR (kcal) 182582 plusmn 8700 187236 plusmn 9931 0033 171577 plusmn 11194 173554 plusmn 12926 0651Variables presented as mean plusmn standard error CT1 concurrent training 5 times per week CT2 concurrent training 3 times per week BMI body mass indexFFM free fat mass BF body fat percentage WC waist circumference AC abdominal circumference HC hip circumference BMR basal metabolic rate119875 lt 005 (significantly different) Paired 119905-test was utilized to compare before and after training in the same group

Table 3 Comparison of markers of insulin resistance and oxidative stress in obese individuals before and after concurrent training

CT1 CT2Before After 119875 Before After 119875

Insulin resistance markersFasting glucose (mgdL) 9650 plusmn 385 8566 plusmn 413 0096 10096 plusmn 376 8569 plusmn 413 0001Fasting insulin (uUImL) 1054 plusmn 084 1429 plusmn 077 0002 955 plusmn 077 854 plusmn 064 0293HOMA-IR 256 plusmn 026 377 plusmn 035 0005 234 plusmn 056 179 plusmn 052 0009

Oxidative stress markersTBARS (nmolmL) 369 plusmn 031 369 plusmn 011 0987 470 plusmn 017 635 plusmn 0049 0015Carbonyl (nmol DNPHmg) 11636 plusmn 1836 3445 plusmn 746 0012 2496 plusmn 967 2439 plusmn 857 0965Sulfhydryl (120583Mmg) 1183 plusmn 1103 903 plusmn 123 0145 520 plusmn 104 409 plusmn 041 0169CAT (UCATmg) 279 plusmn 066 473 plusmn 124 0281 326 plusmn 063 183 plusmn 028 0074SOD (USODmg 185 plusmn 050 240 plusmn 086 0667 129 plusmn 046 307 plusmn 138 0235GPx (UGPxmg) 386 plusmn 040 337 plusmn 037 lt0001 457 plusmn 045 422 plusmn 042 0002

Variables presented as mean plusmn standard error CT1 concurrent training 5 times per week CT2 concurrent training 3 times per week HOMA-IR homeostasismodel of insulin resistance TBARS thiobarbituric acid reactive substances CAT catalase activity SOD superoxide dismutase activity GPx glutathioneperoxidase activity119875 lt 005 (significantly different) Paired 119905-test was utilized to compare before and after training in the same group

Sciences (SPSS) program version 180 All statistical tests weretwo-tailed and performed using a significance level of 120572 =005

3 Results

It was observed that both training protocols were able toreduce body weight and BMI (Table 2) But only CT1 showedsignificantly decreased body fat percentage and increasedfree fat mass and BMR after the training period Regardingthe circumference measurements hip circumference wasdecreased in CT1 and abdomen and hip circumferences weredecreased in CT2 (Table 2)

With regard to IR parameters the CT1 group showed asignificant increase in fasting insulin level andHOMA-IR andno change in fasting glucoseHowever theCT2 group showeda significant decrease in fasting glucose level and HOMA-IRwith no change in fasting insulin (Table 3)

Finally for oxidative stress markers only carbonyls andGPx activity were reduced in the CT1 group while in theCT2 group the TBARS levels increased and GPx activitydecreased (Table 3)

4 Discussion

Exercise is a strong ally in the treatment of obesity andwhen performed with adequate intensity and frequency itcould provide protection against comorbidities of obesityThis includes improvement in the cardiovascular system(reduced blood pressure increased peripheral blood flowreduced atherosclerosis progression and decreased oxygendemand of the myocardium) reduced risk of developingtype 2 DM (by reducing IR) anxiety and depression andincreased metabolic rate [18ndash20]

It is known that aerobic exercise is beneficial in weightloss modulation of oxidative stress and reduction of IR inobese individuals [21 22] But there are few studies applyingthe strength exercise associated with aerobic exercise (con-current training) in this populationThis training can help toreduce body weight and fat mass by increasing lean mass andbasal metabolic rate [23ndash26]

These benefitswere observed in this study and both formsof concurrent trainings were able to reduce body weight andBMI CT1 (5xweek) also reduced the body fat percentage andhip circumference and even increased basal metabolic rateThese findings were also shown in a study by Willis et al [7]

4 Oxidative Medicine and Cellular Longevity

whodemonstrated a reduction inweight body fat percentageandwaist circumference in overweight adults who performedconcurrent training 3xweek with an intensity of 65ndash80VO2peakAnother study also showed that overweight individ-

uals who performed concurrent training for 12 weeks 5daysweek had a decrease in weight BMI body fat percent-age and waist circumference However in this same studytwo other groups that performed strength training or aerobictraining only had a decrease in waist circumference showingthe relevance of the type of training [6]

Our study also demonstrated a significant increase infree fat mass in CT1 which can result in neuromuscularadaptations such as increased muscle mass and maximalstrength dynamic capacity and can improve basal metabolicrate in obese individuals Also other studies have shown thatconcurrent training has positive effects in the development ofstrength and muscle mass in both healthy young individuals[27] and overweight dyslipidemic individuals [28]

Furthermore according to the IR data presented the CT1group showed an increase in fasting insulin level andHOMA-IR although this increase was still within normal range(2ndash25120583IUmL) On the other hand CT2 reduced glucoselevels and HOMA-IR but did not alter fasting insulin Inthe literature there are few studies demonstrating the roleof concurrent training in obese nondiabetics But a study ofsubjects with metabolic syndrome and type 2 DM showedthat concurrent training for 20 weeks at 70ndash80 VO

2peakreducedHOMA-IR as well as weight andwaist circumference[29] starting on the third week thereby corroborating ourfindings

Studies have shown a direct relationship between exerciseand insulin sensitivity [29 30] However a short time ofphysical activity is associated with low insulin sensitivityand a few days of rest are associated with increased IR [29ndash31] Thus regular exercise can improve insulin sensitivity inhealthy subjects and obese nondiabetics [19 32ndash34] Notablythe positive effect of exercise on insulin sensitivity has beendemonstrated 12ndash48 hours after the last session of exercisebut preexercise levels return in three or five days [35]highlighting the importance of regular exercise

IR is associated with obesity and both are related tooxidative stress Clinical and animal models studies haveshown that oxidative stress is a potential mediator of IRparticularly in skeletal muscle because there is an inverserelationship between oxidative stress and insulin action [36ndash38] Prolonged exposure to low levels of oxidative stressreduces insulin sensitivity (reduction in GLUT-4) [39] caus-ing defects in its signaling [40 41]

According to a study in a rat model of insulin-resistantobesity (Zucker) endurance training reduced protein oxida-tion (carbonyl) levels after training [36] This research groupalso reported that this exercise improved insulin action andglucose transport in the soleus plantar and cardiac muscles[37] These results are in line with our findings in concurrenttraining that is reduced damage to proteins (carbonyls)Furthermore another study with Wistar rats showed adecrease in lipid peroxidation (TBARS) increase in antioxi-dant enzyme SODactivity and reduction in triglyceride levels

when concurrent trainingwas performed 5xweek It was alsoobserved that this improvement in the antioxidant systemwas similar in the groups that performed exclusively aerobicor strength training [42]

Furthermore the CT2 group showed lower GPx activityand a trend (119875 = 007) towards a reduction in CAT activitybut no change in SOD activity and sulfhydryl level whichmay have contributed to the increase in TBARS in thisgroup It is well known that exercise promotes increasedoxidative stress because during exercise the rate of oxygenconsumption increases about 20 times and in exhaustiveexercise glutathione activity can be reduced [43] Perhapsthe intensity and frequency of CT2 were not sufficientto modulate antioxidant defenses and thereby induce thenecessary adjustments to reduce damage to lipids

Many tissues can produce reactive oxygen species duringphysical exercise Studies have investigated which organs areprimarily responsible for reactive oxygen species productionin exercising humans The lack of in vivo studies on thistopic is due to the difficulty of investigating the multifacetednature of exercise which involves several organ systems andthese organs are connecting through the increased energyrequirement of contracting skeletal muscles [44] Investiga-tors have assumed that skeletal muscle provides the majorsource of free radical and reactive oxygen species generationduring exercise [44] Nonetheless other tissues such as theheart lungs or blood may also contribute to the total bodygeneration of reactive oxygen species during exercise [44 45]

Studies have shown that prolonged or intense contractileactivity alters the physiological environment in muscle fibersresulting in conditions that predispose these fibers to higherrates of reactive oxygen species production Increased oxygenconsumption in muscle fibers lowers intracellular oxygentension during exercise which can promote increased reac-tive oxygen species production [46] Further a rise in muscletemperature increased CO

2tension and decreased cellular

pH are other exercise-related changes that can stimulate reac-tive oxygen species production in muscleThese contraction-induced changes can stimulate superoxide production atmultiple subcellular sites [46 47]

On the basis of this study concurrent training may be analternative to lowering weight and BMI but when training isperformed more frequently (5 times a week) these benefitscan be enhanced by reducing body fat and protein damageas well On the other hand the effects of such training onoxidative stress parameters and IR were contradictory andthus more studies are needed to elucidate the mechanisms ofconcurrent training in this population

Conflict of Interests

The authors have no conflict of interests to disclose in thisstudy

Acknowledgments

The authors are grateful to the study participants fortheir cooperation and collaborators for their dedication

Oxidative Medicine and Cellular Longevity 5

The financial support was provided by Centro UniversitarioMetodista do IPA and Coordenacao de Aperfeicoamento dePessoal de Nıvel Superior (CAPES) Dr A Leyva helped withEnglish editing of the paper

References

[1] S Jebb ldquoObesity causes and consequencesrdquo Womenrsquos HealthMedicine vol 1 no 1 pp 38ndash41 2004

[2] F Amirkhizi F Siassi M Djalali and A R ForoushanildquoEvaluation of oxidative stress and total antioxidant capacity inwomenwith general and abdominal adiposityrdquoObesity Researchand Clinical Practice vol 4 no 3 pp e209ndashe216 2010

[3] I Grattagliano V O Palmieri P Portincasa A Moschetta andG Palasciano ldquoOxidative stress-induced risk factors associatedwith the metabolic syndrome a unifying hypothesisrdquo TheJournal of Nutritional Biochemistry vol 19 no 8 pp 491ndash5042008

[4] S Furukawa T FujitaM Shimabukuro et al ldquoIncreased oxida-tive stress in obesity and its impact onmetabolic syndromerdquoTheJournal of Clinical Investigation vol 114 no 12 pp 1752ndash17612004

[5] R E Andersen and J M Jakicic ldquoInterpreting the physicalactivity guidelines for health and weight managementrdquo Journalof Physical Activity and Health vol 6 no 5 pp 651ndash656 2009

[6] S S Ho S S Dhaliwal A P Hills and S Pal ldquoThe effect of12 weeks of aerobic resistance or combination exercise trainingon cardiovascular risk factors in the overweight and obese in arandomized trialrdquo BMC Public Health vol 12 article 704 2012

[7] L H Willis C A Slentz L A Bateman et al ldquoEffects ofaerobic andor resistance training on bodymass and fat mass inoverweight or obese adultsrdquo Journal of Applied Physiology vol113 no 12 pp 1831ndash1837 2012

[8] E Ghahramanloo A W Midgley and D J Bentley ldquoThe effectof concurrent training on blood lipid profile and anthropomet-rical characteristics of previously untrained menrdquo Journal ofPhysical Activity and Health vol 6 no 6 pp 760ndash766 2009

[9] American College of Sports Medicine (ACSM) ACSMrsquos Guide-lines for Exercise Testing and Prescription Lippincott WilliamsampWilkins Baltimore Md USA 8th edition 2009

[10] E T Howley D R Bassett Jr and H G Welch ldquoCriteria formaximal oxygen uptake review and commentaryrdquo Medicineand Science in Sports and Exercise vol 27 no 9 pp 1292ndash13011995

[11] L A Brown C J Kerr P Whiting N Finer J McEneny and TAshton ldquoOxidant stress in healthy normal-weight overweightand obese individualsrdquoObesity vol 17 no 3 pp 460ndash466 2009

[12] E D Wills ldquoMechanisms of lipid peroxide formation in animaltissuesrdquo Biochemical Journal vol 99 no 3 pp 667ndash676 1966

[13] A Z Reznick and L Packer ldquoOxidative damage to proteinsspectrophotometric method for carbonyl assayrdquo Methods inEnzymology vol 233 pp 357ndash363 1994

[14] M Y Aksenov and W R Markesbery ldquoChanges in thiolcontent and expression of glutathione redox system genesin the hippocampus and cerebellum in Alzheimerrsquos diseaserdquoNeuroscience Letters vol 302 no 2-3 pp 141ndash145 2001

[15] H Aebi ldquo[13] Catalase in vitrordquo Methods in Enzymology vol105 pp 121ndash126 1984

[16] H PMisra and I Fridovich ldquoThe role of superoxide anion in theautoxidation of epinephrine and a simple assay for superoxide

dismutaserdquoThe Journal of Biological Chemistry vol 247 no 10pp 3170ndash3175 1972

[17] A Wendel ldquoGlutathione peroxidaserdquo Methods in Enzymologyvol 77 pp 325ndash333 1981

[18] T S Church C P Earnest J S Skinner and S N Blair ldquoEffectsof different doses of physical activity on cardiorespiratoryfitness among sedentary overweight or obese postmenopausalwomen with elevated blood pressurerdquo The Journal of theAmerican Medical Association vol 297 no 19 pp 2081ndash20912007

[19] D M Okay P V Jackson MMarcinkiewicz andM N PapinoldquoExercise and obesityrdquo Primary CaremdashClinics in Office Practicevol 36 no 2 pp 379ndash393 2009

[20] D E R Warburton C W Nicol and S S D Bredin ldquoHealthbenefits of physical activity the evidencerdquo Canadian MedicalAssociation Journal vol 174 no 6 pp 801ndash809 2006

[21] M F F Mediano and R Sichieri ldquoInsulin resistance influencesweight loss in non-obese women who followed a home-based exercise program and slight caloric restrictionrdquo DiabetesResearch and Clinical Practice vol 92 no 3 pp 361ndash367 2011

[22] G Murdolo M Piroddi F Luchetti et al ldquoOxidative stress andlipid peroxidation by-products at the crossroad between adi-pose organ dysregulation and obesity-linked insulin resistancerdquoBiochimie vol 95 no 3 pp 585ndash594 2013

[23] A Chatzinikolaou I Fatouros A Petridou et al ldquoAdiposetissue lipolysis is upregulated in lean and obese men duringacute resistance exerciserdquo Diabetes Care vol 31 no 7 pp 1397ndash1399 2008

[24] M J Ormsbee D C Myung J K Medlin et al ldquoRegulation offat metabolism during resistance exercise in sedentary lean andobese menrdquo Journal of Applied Physiology vol 106 no 5 pp1529ndash1537 2009

[25] H T Rabelo L A Bezerra D F Terra et al ldquoEffects of 24 weeksof progressive resistance training on knee extensors peak torqueand fat-free mass in older womenrdquoThe Journal of Strength andConditioning Research vol 25 no 8 pp 2298ndash2303 2011

[26] R AWashburn E P Kirk B K Smith et al ldquoOne set resistancetraining effect on body composition in overweight youngadultsrdquo Journal of Sports Medicine and Physical Fitness vol 52no 3 pp 273ndash279 2012

[27] S P Glowacki S E Martin AMaurerW Baek J S Green andS F Crouse ldquoEffects of resistance endurance and concurrentexercise on training outcomes in menrdquoMedicine and Science inSports and Exercise vol 36 no 12 pp 2119ndash2127 2004

[28] M I Schaun T Dipp J S Rossato et al ldquoThe effects ofperiodized concurrent and aerobic training on oxidative stressparameters endothelial function and immune response insedentary male individuals of middle agerdquo Cell Biochemistryand Function vol 29 no 7 pp 534ndash542 2011

[29] S Balducci S Zanuso A Nicolucci et al ldquoAnti-inflammatoryeffect of exercise training in subjects with type 2 diabetes andthe metabolic syndrome is dependent on exercise modalitiesand independent of weight lossrdquo Nutrition Metabolism andCardiovascular Diseases vol 20 no 8 pp 608ndash617 2010

[30] K L Rennie N McCarthy S Yazdgerdi M Marmot and EBrunner ldquoAssociation of the metabolic syndrome with bothvigorous and moderate physical activityrdquo International Journalof Epidemiology vol 32 no 4 pp 600ndash606 2003

[31] T A Lakka D E Laaksonen H-M Lakka et al ldquoSedentarylifestyle poor cardiorespiratory fitness and the metabolicsyndromerdquo Medicine and Science in Sports amp Exercise vol 35no 8 pp 1279ndash1286 2003

6 Oxidative Medicine and Cellular Longevity

[32] S E Kahn V G Larson J C Beard et al ldquoEffect of exerciseon insulin action glucose tolerance and insulin secretion inagingrdquoTheAmerican Journal of PhysiologymdashEndocrinology andMetabolism vol 258 no 6 pp E937ndashE943 1990

[33] J P Kirwan W M Kohrt D M Wojta R E Bourey andJ O Holloszy ldquoEndurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-oldmen andwomenrdquoThe Journals of Gerontology vol 48 no 3 pp M84ndashM90 1993

[34] J P Miller R E Pratley A P Goldberg et al ldquoStrengthtraining increases insulin action in healthy 50- to 65-yr-oldmenrdquo Journal of Applied Physiology vol 77 no 3 pp 1122ndash11271994

[35] J Eriksson S Taimela and V A Koivisto ldquoExercise and themetabolic syndromerdquo Diabetologia vol 40 no 2 pp 125ndash1351997

[36] V Saengsirisuwan T R Kinnick M B Schmit and E JHenriksen ldquoInteractions of exercise training and lipoic acid onskeletal muscle glucose transport in obese Zucker ratsrdquo Journalof Applied Physiology vol 91 no 1 pp 145ndash153 2001

[37] M K Teachey Z C Taylor T Maier et al ldquoInteractions ofconjugated linoleic acid and lipoic acid on insulin action in theobese Zucker ratrdquo Metabolism Clinical and Experimental vol52 no 9 pp 1167ndash1174 2003

[38] H Urakawa A Katsuki Y Sumida et al ldquoOxidative stress isassociated with adiposity and insulin resistance in menrdquo TheJournal of Clinical Endocrinology and Metabolism vol 88 no10 pp 4673ndash4676 2003

[39] A RudichN Kozlovsky R Potashnik andN Bashan ldquoOxidantstress reduces insulin responsiveness in 3T3-L1 adipocytesrdquoThe American Journal of PhysiologymdashEndocrinology andMetabolism vol 272 no 5 pp E935ndashE940 1997

[40] B A Maddux W See J C Lawrence Jr A L Goldfine I DGoldfine and J L Evans ldquoProtection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolarconcentrations of120572-lipoic acidrdquoDiabetes vol 50 no 2 pp 404ndash410 2001

[41] A Rudich A Tlrosh R Potashnik R Hemi H Kanety andN Bashan ldquoProlonged oxidative stress impairs insulin-inducedGLUT4 translocation in 3T3-L1 adipocytesrdquo Diabetes vol 47no 10 pp 1562ndash1569 1998

[42] J D Botezelli L T Cambri A C Ghezzi et al ldquoDifferentexercise protocols improvemetabolic syndromemarkers tissuetriglycerides content and antioxidant status in ratsrdquoDiabetologyand Metabolic Syndrome vol 3 no 1 article 35 2011

[43] L L Ji and R Fu ldquoResponses of glutathione system andantioxidant enzymes to exhaustive exercise and hydroperoxiderdquoThe Journal of Applied Physiology vol 72 no 2 pp 549ndash5541992

[44] S K Powers and M J Jackson ldquoExercise-induced oxidativestress cellularmechanisms and impact onmuscle force produc-tionrdquo Physiological Reviews vol 88 no 4 pp 1243ndash1276 2008

[45] MGNikolaidis andA Z Jamurtas ldquoBlood as a reactive speciesgenerator and redox status regulator during exerciserdquo Archivesof Biochemistry and Biophysics vol 490 no 2 pp 77ndash84 2009

[46] L F Ferreira and M B Reid ldquoMuscle-derived ROS and thiolregulation in muscle fatiguerdquo Journal of Applied Physiology vol104 no 3 pp 853ndash860 2008

[47] S K Powers W B Nelson and M B Hudson ldquoExercise-induced oxidative stress in humans cause and consequencesrdquoFree Radical BiologyampMedicine vol 51 no 5 pp 942ndash950 2011

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Oxidative Medicine and Cellular Longevity 3

Table 2 Anthropometric parameters of obese individuals before and after concurrent training with different frequencies

Anthropometric CT1 CT2parameters Before After 119875 Before After 119875

Body weight (kg) 9606 plusmn 432 9334 plusmn 426 lt0001 8998 plusmn 464 8720 plusmn 430 0013BMI (kgm2) 3673 plusmn 160 3568 plusmn 155 lt0001 3353 plusmn 103 3255 plusmn 100 0011FFM (kg) 5959 plusmn 290 6174 plusmn 325 0021 5641 plusmn 368 5727 plusmn 427 0541BF () 3735 plusmn 157 3378 plusmn 191 lt0001 3811 plusmn 098 3668 plusmn 139 0062WC (cm) 10294 plusmn 294 10191 plusmn 287 0177 9777 plusmn 255 9511 plusmn 268 0077AC (cm) 11327 plusmn 315 11114 plusmn 279 0074 10533 plusmn 169 10126 plusmn 125 0026HC (cm) 11755 plusmn 227 11323 plusmn 199 lt0001 11379 plusmn 201 11116 plusmn 180 0007BMR (kcal) 182582 plusmn 8700 187236 plusmn 9931 0033 171577 plusmn 11194 173554 plusmn 12926 0651Variables presented as mean plusmn standard error CT1 concurrent training 5 times per week CT2 concurrent training 3 times per week BMI body mass indexFFM free fat mass BF body fat percentage WC waist circumference AC abdominal circumference HC hip circumference BMR basal metabolic rate119875 lt 005 (significantly different) Paired 119905-test was utilized to compare before and after training in the same group

Table 3 Comparison of markers of insulin resistance and oxidative stress in obese individuals before and after concurrent training

CT1 CT2Before After 119875 Before After 119875

Insulin resistance markersFasting glucose (mgdL) 9650 plusmn 385 8566 plusmn 413 0096 10096 plusmn 376 8569 plusmn 413 0001Fasting insulin (uUImL) 1054 plusmn 084 1429 plusmn 077 0002 955 plusmn 077 854 plusmn 064 0293HOMA-IR 256 plusmn 026 377 plusmn 035 0005 234 plusmn 056 179 plusmn 052 0009

Oxidative stress markersTBARS (nmolmL) 369 plusmn 031 369 plusmn 011 0987 470 plusmn 017 635 plusmn 0049 0015Carbonyl (nmol DNPHmg) 11636 plusmn 1836 3445 plusmn 746 0012 2496 plusmn 967 2439 plusmn 857 0965Sulfhydryl (120583Mmg) 1183 plusmn 1103 903 plusmn 123 0145 520 plusmn 104 409 plusmn 041 0169CAT (UCATmg) 279 plusmn 066 473 plusmn 124 0281 326 plusmn 063 183 plusmn 028 0074SOD (USODmg 185 plusmn 050 240 plusmn 086 0667 129 plusmn 046 307 plusmn 138 0235GPx (UGPxmg) 386 plusmn 040 337 plusmn 037 lt0001 457 plusmn 045 422 plusmn 042 0002

Variables presented as mean plusmn standard error CT1 concurrent training 5 times per week CT2 concurrent training 3 times per week HOMA-IR homeostasismodel of insulin resistance TBARS thiobarbituric acid reactive substances CAT catalase activity SOD superoxide dismutase activity GPx glutathioneperoxidase activity119875 lt 005 (significantly different) Paired 119905-test was utilized to compare before and after training in the same group

Sciences (SPSS) program version 180 All statistical tests weretwo-tailed and performed using a significance level of 120572 =005

3 Results

It was observed that both training protocols were able toreduce body weight and BMI (Table 2) But only CT1 showedsignificantly decreased body fat percentage and increasedfree fat mass and BMR after the training period Regardingthe circumference measurements hip circumference wasdecreased in CT1 and abdomen and hip circumferences weredecreased in CT2 (Table 2)

With regard to IR parameters the CT1 group showed asignificant increase in fasting insulin level andHOMA-IR andno change in fasting glucoseHowever theCT2 group showeda significant decrease in fasting glucose level and HOMA-IRwith no change in fasting insulin (Table 3)

Finally for oxidative stress markers only carbonyls andGPx activity were reduced in the CT1 group while in theCT2 group the TBARS levels increased and GPx activitydecreased (Table 3)

4 Discussion

Exercise is a strong ally in the treatment of obesity andwhen performed with adequate intensity and frequency itcould provide protection against comorbidities of obesityThis includes improvement in the cardiovascular system(reduced blood pressure increased peripheral blood flowreduced atherosclerosis progression and decreased oxygendemand of the myocardium) reduced risk of developingtype 2 DM (by reducing IR) anxiety and depression andincreased metabolic rate [18ndash20]

It is known that aerobic exercise is beneficial in weightloss modulation of oxidative stress and reduction of IR inobese individuals [21 22] But there are few studies applyingthe strength exercise associated with aerobic exercise (con-current training) in this populationThis training can help toreduce body weight and fat mass by increasing lean mass andbasal metabolic rate [23ndash26]

These benefitswere observed in this study and both formsof concurrent trainings were able to reduce body weight andBMI CT1 (5xweek) also reduced the body fat percentage andhip circumference and even increased basal metabolic rateThese findings were also shown in a study by Willis et al [7]

4 Oxidative Medicine and Cellular Longevity

whodemonstrated a reduction inweight body fat percentageandwaist circumference in overweight adults who performedconcurrent training 3xweek with an intensity of 65ndash80VO2peakAnother study also showed that overweight individ-

uals who performed concurrent training for 12 weeks 5daysweek had a decrease in weight BMI body fat percent-age and waist circumference However in this same studytwo other groups that performed strength training or aerobictraining only had a decrease in waist circumference showingthe relevance of the type of training [6]

Our study also demonstrated a significant increase infree fat mass in CT1 which can result in neuromuscularadaptations such as increased muscle mass and maximalstrength dynamic capacity and can improve basal metabolicrate in obese individuals Also other studies have shown thatconcurrent training has positive effects in the development ofstrength and muscle mass in both healthy young individuals[27] and overweight dyslipidemic individuals [28]

Furthermore according to the IR data presented the CT1group showed an increase in fasting insulin level andHOMA-IR although this increase was still within normal range(2ndash25120583IUmL) On the other hand CT2 reduced glucoselevels and HOMA-IR but did not alter fasting insulin Inthe literature there are few studies demonstrating the roleof concurrent training in obese nondiabetics But a study ofsubjects with metabolic syndrome and type 2 DM showedthat concurrent training for 20 weeks at 70ndash80 VO

2peakreducedHOMA-IR as well as weight andwaist circumference[29] starting on the third week thereby corroborating ourfindings

Studies have shown a direct relationship between exerciseand insulin sensitivity [29 30] However a short time ofphysical activity is associated with low insulin sensitivityand a few days of rest are associated with increased IR [29ndash31] Thus regular exercise can improve insulin sensitivity inhealthy subjects and obese nondiabetics [19 32ndash34] Notablythe positive effect of exercise on insulin sensitivity has beendemonstrated 12ndash48 hours after the last session of exercisebut preexercise levels return in three or five days [35]highlighting the importance of regular exercise

IR is associated with obesity and both are related tooxidative stress Clinical and animal models studies haveshown that oxidative stress is a potential mediator of IRparticularly in skeletal muscle because there is an inverserelationship between oxidative stress and insulin action [36ndash38] Prolonged exposure to low levels of oxidative stressreduces insulin sensitivity (reduction in GLUT-4) [39] caus-ing defects in its signaling [40 41]

According to a study in a rat model of insulin-resistantobesity (Zucker) endurance training reduced protein oxida-tion (carbonyl) levels after training [36] This research groupalso reported that this exercise improved insulin action andglucose transport in the soleus plantar and cardiac muscles[37] These results are in line with our findings in concurrenttraining that is reduced damage to proteins (carbonyls)Furthermore another study with Wistar rats showed adecrease in lipid peroxidation (TBARS) increase in antioxi-dant enzyme SODactivity and reduction in triglyceride levels

when concurrent trainingwas performed 5xweek It was alsoobserved that this improvement in the antioxidant systemwas similar in the groups that performed exclusively aerobicor strength training [42]

Furthermore the CT2 group showed lower GPx activityand a trend (119875 = 007) towards a reduction in CAT activitybut no change in SOD activity and sulfhydryl level whichmay have contributed to the increase in TBARS in thisgroup It is well known that exercise promotes increasedoxidative stress because during exercise the rate of oxygenconsumption increases about 20 times and in exhaustiveexercise glutathione activity can be reduced [43] Perhapsthe intensity and frequency of CT2 were not sufficientto modulate antioxidant defenses and thereby induce thenecessary adjustments to reduce damage to lipids

Many tissues can produce reactive oxygen species duringphysical exercise Studies have investigated which organs areprimarily responsible for reactive oxygen species productionin exercising humans The lack of in vivo studies on thistopic is due to the difficulty of investigating the multifacetednature of exercise which involves several organ systems andthese organs are connecting through the increased energyrequirement of contracting skeletal muscles [44] Investiga-tors have assumed that skeletal muscle provides the majorsource of free radical and reactive oxygen species generationduring exercise [44] Nonetheless other tissues such as theheart lungs or blood may also contribute to the total bodygeneration of reactive oxygen species during exercise [44 45]

Studies have shown that prolonged or intense contractileactivity alters the physiological environment in muscle fibersresulting in conditions that predispose these fibers to higherrates of reactive oxygen species production Increased oxygenconsumption in muscle fibers lowers intracellular oxygentension during exercise which can promote increased reac-tive oxygen species production [46] Further a rise in muscletemperature increased CO

2tension and decreased cellular

pH are other exercise-related changes that can stimulate reac-tive oxygen species production in muscleThese contraction-induced changes can stimulate superoxide production atmultiple subcellular sites [46 47]

On the basis of this study concurrent training may be analternative to lowering weight and BMI but when training isperformed more frequently (5 times a week) these benefitscan be enhanced by reducing body fat and protein damageas well On the other hand the effects of such training onoxidative stress parameters and IR were contradictory andthus more studies are needed to elucidate the mechanisms ofconcurrent training in this population

Conflict of Interests

The authors have no conflict of interests to disclose in thisstudy

Acknowledgments

The authors are grateful to the study participants fortheir cooperation and collaborators for their dedication

Oxidative Medicine and Cellular Longevity 5

The financial support was provided by Centro UniversitarioMetodista do IPA and Coordenacao de Aperfeicoamento dePessoal de Nıvel Superior (CAPES) Dr A Leyva helped withEnglish editing of the paper

References

[1] S Jebb ldquoObesity causes and consequencesrdquo Womenrsquos HealthMedicine vol 1 no 1 pp 38ndash41 2004

[2] F Amirkhizi F Siassi M Djalali and A R ForoushanildquoEvaluation of oxidative stress and total antioxidant capacity inwomenwith general and abdominal adiposityrdquoObesity Researchand Clinical Practice vol 4 no 3 pp e209ndashe216 2010

[3] I Grattagliano V O Palmieri P Portincasa A Moschetta andG Palasciano ldquoOxidative stress-induced risk factors associatedwith the metabolic syndrome a unifying hypothesisrdquo TheJournal of Nutritional Biochemistry vol 19 no 8 pp 491ndash5042008

[4] S Furukawa T FujitaM Shimabukuro et al ldquoIncreased oxida-tive stress in obesity and its impact onmetabolic syndromerdquoTheJournal of Clinical Investigation vol 114 no 12 pp 1752ndash17612004

[5] R E Andersen and J M Jakicic ldquoInterpreting the physicalactivity guidelines for health and weight managementrdquo Journalof Physical Activity and Health vol 6 no 5 pp 651ndash656 2009

[6] S S Ho S S Dhaliwal A P Hills and S Pal ldquoThe effect of12 weeks of aerobic resistance or combination exercise trainingon cardiovascular risk factors in the overweight and obese in arandomized trialrdquo BMC Public Health vol 12 article 704 2012

[7] L H Willis C A Slentz L A Bateman et al ldquoEffects ofaerobic andor resistance training on bodymass and fat mass inoverweight or obese adultsrdquo Journal of Applied Physiology vol113 no 12 pp 1831ndash1837 2012

[8] E Ghahramanloo A W Midgley and D J Bentley ldquoThe effectof concurrent training on blood lipid profile and anthropomet-rical characteristics of previously untrained menrdquo Journal ofPhysical Activity and Health vol 6 no 6 pp 760ndash766 2009

[9] American College of Sports Medicine (ACSM) ACSMrsquos Guide-lines for Exercise Testing and Prescription Lippincott WilliamsampWilkins Baltimore Md USA 8th edition 2009

[10] E T Howley D R Bassett Jr and H G Welch ldquoCriteria formaximal oxygen uptake review and commentaryrdquo Medicineand Science in Sports and Exercise vol 27 no 9 pp 1292ndash13011995

[11] L A Brown C J Kerr P Whiting N Finer J McEneny and TAshton ldquoOxidant stress in healthy normal-weight overweightand obese individualsrdquoObesity vol 17 no 3 pp 460ndash466 2009

[12] E D Wills ldquoMechanisms of lipid peroxide formation in animaltissuesrdquo Biochemical Journal vol 99 no 3 pp 667ndash676 1966

[13] A Z Reznick and L Packer ldquoOxidative damage to proteinsspectrophotometric method for carbonyl assayrdquo Methods inEnzymology vol 233 pp 357ndash363 1994

[14] M Y Aksenov and W R Markesbery ldquoChanges in thiolcontent and expression of glutathione redox system genesin the hippocampus and cerebellum in Alzheimerrsquos diseaserdquoNeuroscience Letters vol 302 no 2-3 pp 141ndash145 2001

[15] H Aebi ldquo[13] Catalase in vitrordquo Methods in Enzymology vol105 pp 121ndash126 1984

[16] H PMisra and I Fridovich ldquoThe role of superoxide anion in theautoxidation of epinephrine and a simple assay for superoxide

dismutaserdquoThe Journal of Biological Chemistry vol 247 no 10pp 3170ndash3175 1972

[17] A Wendel ldquoGlutathione peroxidaserdquo Methods in Enzymologyvol 77 pp 325ndash333 1981

[18] T S Church C P Earnest J S Skinner and S N Blair ldquoEffectsof different doses of physical activity on cardiorespiratoryfitness among sedentary overweight or obese postmenopausalwomen with elevated blood pressurerdquo The Journal of theAmerican Medical Association vol 297 no 19 pp 2081ndash20912007

[19] D M Okay P V Jackson MMarcinkiewicz andM N PapinoldquoExercise and obesityrdquo Primary CaremdashClinics in Office Practicevol 36 no 2 pp 379ndash393 2009

[20] D E R Warburton C W Nicol and S S D Bredin ldquoHealthbenefits of physical activity the evidencerdquo Canadian MedicalAssociation Journal vol 174 no 6 pp 801ndash809 2006

[21] M F F Mediano and R Sichieri ldquoInsulin resistance influencesweight loss in non-obese women who followed a home-based exercise program and slight caloric restrictionrdquo DiabetesResearch and Clinical Practice vol 92 no 3 pp 361ndash367 2011

[22] G Murdolo M Piroddi F Luchetti et al ldquoOxidative stress andlipid peroxidation by-products at the crossroad between adi-pose organ dysregulation and obesity-linked insulin resistancerdquoBiochimie vol 95 no 3 pp 585ndash594 2013

[23] A Chatzinikolaou I Fatouros A Petridou et al ldquoAdiposetissue lipolysis is upregulated in lean and obese men duringacute resistance exerciserdquo Diabetes Care vol 31 no 7 pp 1397ndash1399 2008

[24] M J Ormsbee D C Myung J K Medlin et al ldquoRegulation offat metabolism during resistance exercise in sedentary lean andobese menrdquo Journal of Applied Physiology vol 106 no 5 pp1529ndash1537 2009

[25] H T Rabelo L A Bezerra D F Terra et al ldquoEffects of 24 weeksof progressive resistance training on knee extensors peak torqueand fat-free mass in older womenrdquoThe Journal of Strength andConditioning Research vol 25 no 8 pp 2298ndash2303 2011

[26] R AWashburn E P Kirk B K Smith et al ldquoOne set resistancetraining effect on body composition in overweight youngadultsrdquo Journal of Sports Medicine and Physical Fitness vol 52no 3 pp 273ndash279 2012

[27] S P Glowacki S E Martin AMaurerW Baek J S Green andS F Crouse ldquoEffects of resistance endurance and concurrentexercise on training outcomes in menrdquoMedicine and Science inSports and Exercise vol 36 no 12 pp 2119ndash2127 2004

[28] M I Schaun T Dipp J S Rossato et al ldquoThe effects ofperiodized concurrent and aerobic training on oxidative stressparameters endothelial function and immune response insedentary male individuals of middle agerdquo Cell Biochemistryand Function vol 29 no 7 pp 534ndash542 2011

[29] S Balducci S Zanuso A Nicolucci et al ldquoAnti-inflammatoryeffect of exercise training in subjects with type 2 diabetes andthe metabolic syndrome is dependent on exercise modalitiesand independent of weight lossrdquo Nutrition Metabolism andCardiovascular Diseases vol 20 no 8 pp 608ndash617 2010

[30] K L Rennie N McCarthy S Yazdgerdi M Marmot and EBrunner ldquoAssociation of the metabolic syndrome with bothvigorous and moderate physical activityrdquo International Journalof Epidemiology vol 32 no 4 pp 600ndash606 2003

[31] T A Lakka D E Laaksonen H-M Lakka et al ldquoSedentarylifestyle poor cardiorespiratory fitness and the metabolicsyndromerdquo Medicine and Science in Sports amp Exercise vol 35no 8 pp 1279ndash1286 2003

6 Oxidative Medicine and Cellular Longevity

[32] S E Kahn V G Larson J C Beard et al ldquoEffect of exerciseon insulin action glucose tolerance and insulin secretion inagingrdquoTheAmerican Journal of PhysiologymdashEndocrinology andMetabolism vol 258 no 6 pp E937ndashE943 1990

[33] J P Kirwan W M Kohrt D M Wojta R E Bourey andJ O Holloszy ldquoEndurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-oldmen andwomenrdquoThe Journals of Gerontology vol 48 no 3 pp M84ndashM90 1993

[34] J P Miller R E Pratley A P Goldberg et al ldquoStrengthtraining increases insulin action in healthy 50- to 65-yr-oldmenrdquo Journal of Applied Physiology vol 77 no 3 pp 1122ndash11271994

[35] J Eriksson S Taimela and V A Koivisto ldquoExercise and themetabolic syndromerdquo Diabetologia vol 40 no 2 pp 125ndash1351997

[36] V Saengsirisuwan T R Kinnick M B Schmit and E JHenriksen ldquoInteractions of exercise training and lipoic acid onskeletal muscle glucose transport in obese Zucker ratsrdquo Journalof Applied Physiology vol 91 no 1 pp 145ndash153 2001

[37] M K Teachey Z C Taylor T Maier et al ldquoInteractions ofconjugated linoleic acid and lipoic acid on insulin action in theobese Zucker ratrdquo Metabolism Clinical and Experimental vol52 no 9 pp 1167ndash1174 2003

[38] H Urakawa A Katsuki Y Sumida et al ldquoOxidative stress isassociated with adiposity and insulin resistance in menrdquo TheJournal of Clinical Endocrinology and Metabolism vol 88 no10 pp 4673ndash4676 2003

[39] A RudichN Kozlovsky R Potashnik andN Bashan ldquoOxidantstress reduces insulin responsiveness in 3T3-L1 adipocytesrdquoThe American Journal of PhysiologymdashEndocrinology andMetabolism vol 272 no 5 pp E935ndashE940 1997

[40] B A Maddux W See J C Lawrence Jr A L Goldfine I DGoldfine and J L Evans ldquoProtection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolarconcentrations of120572-lipoic acidrdquoDiabetes vol 50 no 2 pp 404ndash410 2001

[41] A Rudich A Tlrosh R Potashnik R Hemi H Kanety andN Bashan ldquoProlonged oxidative stress impairs insulin-inducedGLUT4 translocation in 3T3-L1 adipocytesrdquo Diabetes vol 47no 10 pp 1562ndash1569 1998

[42] J D Botezelli L T Cambri A C Ghezzi et al ldquoDifferentexercise protocols improvemetabolic syndromemarkers tissuetriglycerides content and antioxidant status in ratsrdquoDiabetologyand Metabolic Syndrome vol 3 no 1 article 35 2011

[43] L L Ji and R Fu ldquoResponses of glutathione system andantioxidant enzymes to exhaustive exercise and hydroperoxiderdquoThe Journal of Applied Physiology vol 72 no 2 pp 549ndash5541992

[44] S K Powers and M J Jackson ldquoExercise-induced oxidativestress cellularmechanisms and impact onmuscle force produc-tionrdquo Physiological Reviews vol 88 no 4 pp 1243ndash1276 2008

[45] MGNikolaidis andA Z Jamurtas ldquoBlood as a reactive speciesgenerator and redox status regulator during exerciserdquo Archivesof Biochemistry and Biophysics vol 490 no 2 pp 77ndash84 2009

[46] L F Ferreira and M B Reid ldquoMuscle-derived ROS and thiolregulation in muscle fatiguerdquo Journal of Applied Physiology vol104 no 3 pp 853ndash860 2008

[47] S K Powers W B Nelson and M B Hudson ldquoExercise-induced oxidative stress in humans cause and consequencesrdquoFree Radical BiologyampMedicine vol 51 no 5 pp 942ndash950 2011

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

4 Oxidative Medicine and Cellular Longevity

whodemonstrated a reduction inweight body fat percentageandwaist circumference in overweight adults who performedconcurrent training 3xweek with an intensity of 65ndash80VO2peakAnother study also showed that overweight individ-

uals who performed concurrent training for 12 weeks 5daysweek had a decrease in weight BMI body fat percent-age and waist circumference However in this same studytwo other groups that performed strength training or aerobictraining only had a decrease in waist circumference showingthe relevance of the type of training [6]

Our study also demonstrated a significant increase infree fat mass in CT1 which can result in neuromuscularadaptations such as increased muscle mass and maximalstrength dynamic capacity and can improve basal metabolicrate in obese individuals Also other studies have shown thatconcurrent training has positive effects in the development ofstrength and muscle mass in both healthy young individuals[27] and overweight dyslipidemic individuals [28]

Furthermore according to the IR data presented the CT1group showed an increase in fasting insulin level andHOMA-IR although this increase was still within normal range(2ndash25120583IUmL) On the other hand CT2 reduced glucoselevels and HOMA-IR but did not alter fasting insulin Inthe literature there are few studies demonstrating the roleof concurrent training in obese nondiabetics But a study ofsubjects with metabolic syndrome and type 2 DM showedthat concurrent training for 20 weeks at 70ndash80 VO

2peakreducedHOMA-IR as well as weight andwaist circumference[29] starting on the third week thereby corroborating ourfindings

Studies have shown a direct relationship between exerciseand insulin sensitivity [29 30] However a short time ofphysical activity is associated with low insulin sensitivityand a few days of rest are associated with increased IR [29ndash31] Thus regular exercise can improve insulin sensitivity inhealthy subjects and obese nondiabetics [19 32ndash34] Notablythe positive effect of exercise on insulin sensitivity has beendemonstrated 12ndash48 hours after the last session of exercisebut preexercise levels return in three or five days [35]highlighting the importance of regular exercise

IR is associated with obesity and both are related tooxidative stress Clinical and animal models studies haveshown that oxidative stress is a potential mediator of IRparticularly in skeletal muscle because there is an inverserelationship between oxidative stress and insulin action [36ndash38] Prolonged exposure to low levels of oxidative stressreduces insulin sensitivity (reduction in GLUT-4) [39] caus-ing defects in its signaling [40 41]

According to a study in a rat model of insulin-resistantobesity (Zucker) endurance training reduced protein oxida-tion (carbonyl) levels after training [36] This research groupalso reported that this exercise improved insulin action andglucose transport in the soleus plantar and cardiac muscles[37] These results are in line with our findings in concurrenttraining that is reduced damage to proteins (carbonyls)Furthermore another study with Wistar rats showed adecrease in lipid peroxidation (TBARS) increase in antioxi-dant enzyme SODactivity and reduction in triglyceride levels

when concurrent trainingwas performed 5xweek It was alsoobserved that this improvement in the antioxidant systemwas similar in the groups that performed exclusively aerobicor strength training [42]

Furthermore the CT2 group showed lower GPx activityand a trend (119875 = 007) towards a reduction in CAT activitybut no change in SOD activity and sulfhydryl level whichmay have contributed to the increase in TBARS in thisgroup It is well known that exercise promotes increasedoxidative stress because during exercise the rate of oxygenconsumption increases about 20 times and in exhaustiveexercise glutathione activity can be reduced [43] Perhapsthe intensity and frequency of CT2 were not sufficientto modulate antioxidant defenses and thereby induce thenecessary adjustments to reduce damage to lipids

Many tissues can produce reactive oxygen species duringphysical exercise Studies have investigated which organs areprimarily responsible for reactive oxygen species productionin exercising humans The lack of in vivo studies on thistopic is due to the difficulty of investigating the multifacetednature of exercise which involves several organ systems andthese organs are connecting through the increased energyrequirement of contracting skeletal muscles [44] Investiga-tors have assumed that skeletal muscle provides the majorsource of free radical and reactive oxygen species generationduring exercise [44] Nonetheless other tissues such as theheart lungs or blood may also contribute to the total bodygeneration of reactive oxygen species during exercise [44 45]

Studies have shown that prolonged or intense contractileactivity alters the physiological environment in muscle fibersresulting in conditions that predispose these fibers to higherrates of reactive oxygen species production Increased oxygenconsumption in muscle fibers lowers intracellular oxygentension during exercise which can promote increased reac-tive oxygen species production [46] Further a rise in muscletemperature increased CO

2tension and decreased cellular

pH are other exercise-related changes that can stimulate reac-tive oxygen species production in muscleThese contraction-induced changes can stimulate superoxide production atmultiple subcellular sites [46 47]

On the basis of this study concurrent training may be analternative to lowering weight and BMI but when training isperformed more frequently (5 times a week) these benefitscan be enhanced by reducing body fat and protein damageas well On the other hand the effects of such training onoxidative stress parameters and IR were contradictory andthus more studies are needed to elucidate the mechanisms ofconcurrent training in this population

Conflict of Interests

The authors have no conflict of interests to disclose in thisstudy

Acknowledgments

The authors are grateful to the study participants fortheir cooperation and collaborators for their dedication

Oxidative Medicine and Cellular Longevity 5

The financial support was provided by Centro UniversitarioMetodista do IPA and Coordenacao de Aperfeicoamento dePessoal de Nıvel Superior (CAPES) Dr A Leyva helped withEnglish editing of the paper

References

[1] S Jebb ldquoObesity causes and consequencesrdquo Womenrsquos HealthMedicine vol 1 no 1 pp 38ndash41 2004

[2] F Amirkhizi F Siassi M Djalali and A R ForoushanildquoEvaluation of oxidative stress and total antioxidant capacity inwomenwith general and abdominal adiposityrdquoObesity Researchand Clinical Practice vol 4 no 3 pp e209ndashe216 2010

[3] I Grattagliano V O Palmieri P Portincasa A Moschetta andG Palasciano ldquoOxidative stress-induced risk factors associatedwith the metabolic syndrome a unifying hypothesisrdquo TheJournal of Nutritional Biochemistry vol 19 no 8 pp 491ndash5042008

[4] S Furukawa T FujitaM Shimabukuro et al ldquoIncreased oxida-tive stress in obesity and its impact onmetabolic syndromerdquoTheJournal of Clinical Investigation vol 114 no 12 pp 1752ndash17612004

[5] R E Andersen and J M Jakicic ldquoInterpreting the physicalactivity guidelines for health and weight managementrdquo Journalof Physical Activity and Health vol 6 no 5 pp 651ndash656 2009

[6] S S Ho S S Dhaliwal A P Hills and S Pal ldquoThe effect of12 weeks of aerobic resistance or combination exercise trainingon cardiovascular risk factors in the overweight and obese in arandomized trialrdquo BMC Public Health vol 12 article 704 2012

[7] L H Willis C A Slentz L A Bateman et al ldquoEffects ofaerobic andor resistance training on bodymass and fat mass inoverweight or obese adultsrdquo Journal of Applied Physiology vol113 no 12 pp 1831ndash1837 2012

[8] E Ghahramanloo A W Midgley and D J Bentley ldquoThe effectof concurrent training on blood lipid profile and anthropomet-rical characteristics of previously untrained menrdquo Journal ofPhysical Activity and Health vol 6 no 6 pp 760ndash766 2009

[9] American College of Sports Medicine (ACSM) ACSMrsquos Guide-lines for Exercise Testing and Prescription Lippincott WilliamsampWilkins Baltimore Md USA 8th edition 2009

[10] E T Howley D R Bassett Jr and H G Welch ldquoCriteria formaximal oxygen uptake review and commentaryrdquo Medicineand Science in Sports and Exercise vol 27 no 9 pp 1292ndash13011995

[11] L A Brown C J Kerr P Whiting N Finer J McEneny and TAshton ldquoOxidant stress in healthy normal-weight overweightand obese individualsrdquoObesity vol 17 no 3 pp 460ndash466 2009

[12] E D Wills ldquoMechanisms of lipid peroxide formation in animaltissuesrdquo Biochemical Journal vol 99 no 3 pp 667ndash676 1966

[13] A Z Reznick and L Packer ldquoOxidative damage to proteinsspectrophotometric method for carbonyl assayrdquo Methods inEnzymology vol 233 pp 357ndash363 1994

[14] M Y Aksenov and W R Markesbery ldquoChanges in thiolcontent and expression of glutathione redox system genesin the hippocampus and cerebellum in Alzheimerrsquos diseaserdquoNeuroscience Letters vol 302 no 2-3 pp 141ndash145 2001

[15] H Aebi ldquo[13] Catalase in vitrordquo Methods in Enzymology vol105 pp 121ndash126 1984

[16] H PMisra and I Fridovich ldquoThe role of superoxide anion in theautoxidation of epinephrine and a simple assay for superoxide

dismutaserdquoThe Journal of Biological Chemistry vol 247 no 10pp 3170ndash3175 1972

[17] A Wendel ldquoGlutathione peroxidaserdquo Methods in Enzymologyvol 77 pp 325ndash333 1981

[18] T S Church C P Earnest J S Skinner and S N Blair ldquoEffectsof different doses of physical activity on cardiorespiratoryfitness among sedentary overweight or obese postmenopausalwomen with elevated blood pressurerdquo The Journal of theAmerican Medical Association vol 297 no 19 pp 2081ndash20912007

[19] D M Okay P V Jackson MMarcinkiewicz andM N PapinoldquoExercise and obesityrdquo Primary CaremdashClinics in Office Practicevol 36 no 2 pp 379ndash393 2009

[20] D E R Warburton C W Nicol and S S D Bredin ldquoHealthbenefits of physical activity the evidencerdquo Canadian MedicalAssociation Journal vol 174 no 6 pp 801ndash809 2006

[21] M F F Mediano and R Sichieri ldquoInsulin resistance influencesweight loss in non-obese women who followed a home-based exercise program and slight caloric restrictionrdquo DiabetesResearch and Clinical Practice vol 92 no 3 pp 361ndash367 2011

[22] G Murdolo M Piroddi F Luchetti et al ldquoOxidative stress andlipid peroxidation by-products at the crossroad between adi-pose organ dysregulation and obesity-linked insulin resistancerdquoBiochimie vol 95 no 3 pp 585ndash594 2013

[23] A Chatzinikolaou I Fatouros A Petridou et al ldquoAdiposetissue lipolysis is upregulated in lean and obese men duringacute resistance exerciserdquo Diabetes Care vol 31 no 7 pp 1397ndash1399 2008

[24] M J Ormsbee D C Myung J K Medlin et al ldquoRegulation offat metabolism during resistance exercise in sedentary lean andobese menrdquo Journal of Applied Physiology vol 106 no 5 pp1529ndash1537 2009

[25] H T Rabelo L A Bezerra D F Terra et al ldquoEffects of 24 weeksof progressive resistance training on knee extensors peak torqueand fat-free mass in older womenrdquoThe Journal of Strength andConditioning Research vol 25 no 8 pp 2298ndash2303 2011

[26] R AWashburn E P Kirk B K Smith et al ldquoOne set resistancetraining effect on body composition in overweight youngadultsrdquo Journal of Sports Medicine and Physical Fitness vol 52no 3 pp 273ndash279 2012

[27] S P Glowacki S E Martin AMaurerW Baek J S Green andS F Crouse ldquoEffects of resistance endurance and concurrentexercise on training outcomes in menrdquoMedicine and Science inSports and Exercise vol 36 no 12 pp 2119ndash2127 2004

[28] M I Schaun T Dipp J S Rossato et al ldquoThe effects ofperiodized concurrent and aerobic training on oxidative stressparameters endothelial function and immune response insedentary male individuals of middle agerdquo Cell Biochemistryand Function vol 29 no 7 pp 534ndash542 2011

[29] S Balducci S Zanuso A Nicolucci et al ldquoAnti-inflammatoryeffect of exercise training in subjects with type 2 diabetes andthe metabolic syndrome is dependent on exercise modalitiesand independent of weight lossrdquo Nutrition Metabolism andCardiovascular Diseases vol 20 no 8 pp 608ndash617 2010

[30] K L Rennie N McCarthy S Yazdgerdi M Marmot and EBrunner ldquoAssociation of the metabolic syndrome with bothvigorous and moderate physical activityrdquo International Journalof Epidemiology vol 32 no 4 pp 600ndash606 2003

[31] T A Lakka D E Laaksonen H-M Lakka et al ldquoSedentarylifestyle poor cardiorespiratory fitness and the metabolicsyndromerdquo Medicine and Science in Sports amp Exercise vol 35no 8 pp 1279ndash1286 2003

6 Oxidative Medicine and Cellular Longevity

[32] S E Kahn V G Larson J C Beard et al ldquoEffect of exerciseon insulin action glucose tolerance and insulin secretion inagingrdquoTheAmerican Journal of PhysiologymdashEndocrinology andMetabolism vol 258 no 6 pp E937ndashE943 1990

[33] J P Kirwan W M Kohrt D M Wojta R E Bourey andJ O Holloszy ldquoEndurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-oldmen andwomenrdquoThe Journals of Gerontology vol 48 no 3 pp M84ndashM90 1993

[34] J P Miller R E Pratley A P Goldberg et al ldquoStrengthtraining increases insulin action in healthy 50- to 65-yr-oldmenrdquo Journal of Applied Physiology vol 77 no 3 pp 1122ndash11271994

[35] J Eriksson S Taimela and V A Koivisto ldquoExercise and themetabolic syndromerdquo Diabetologia vol 40 no 2 pp 125ndash1351997

[36] V Saengsirisuwan T R Kinnick M B Schmit and E JHenriksen ldquoInteractions of exercise training and lipoic acid onskeletal muscle glucose transport in obese Zucker ratsrdquo Journalof Applied Physiology vol 91 no 1 pp 145ndash153 2001

[37] M K Teachey Z C Taylor T Maier et al ldquoInteractions ofconjugated linoleic acid and lipoic acid on insulin action in theobese Zucker ratrdquo Metabolism Clinical and Experimental vol52 no 9 pp 1167ndash1174 2003

[38] H Urakawa A Katsuki Y Sumida et al ldquoOxidative stress isassociated with adiposity and insulin resistance in menrdquo TheJournal of Clinical Endocrinology and Metabolism vol 88 no10 pp 4673ndash4676 2003

[39] A RudichN Kozlovsky R Potashnik andN Bashan ldquoOxidantstress reduces insulin responsiveness in 3T3-L1 adipocytesrdquoThe American Journal of PhysiologymdashEndocrinology andMetabolism vol 272 no 5 pp E935ndashE940 1997

[40] B A Maddux W See J C Lawrence Jr A L Goldfine I DGoldfine and J L Evans ldquoProtection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolarconcentrations of120572-lipoic acidrdquoDiabetes vol 50 no 2 pp 404ndash410 2001

[41] A Rudich A Tlrosh R Potashnik R Hemi H Kanety andN Bashan ldquoProlonged oxidative stress impairs insulin-inducedGLUT4 translocation in 3T3-L1 adipocytesrdquo Diabetes vol 47no 10 pp 1562ndash1569 1998

[42] J D Botezelli L T Cambri A C Ghezzi et al ldquoDifferentexercise protocols improvemetabolic syndromemarkers tissuetriglycerides content and antioxidant status in ratsrdquoDiabetologyand Metabolic Syndrome vol 3 no 1 article 35 2011

[43] L L Ji and R Fu ldquoResponses of glutathione system andantioxidant enzymes to exhaustive exercise and hydroperoxiderdquoThe Journal of Applied Physiology vol 72 no 2 pp 549ndash5541992

[44] S K Powers and M J Jackson ldquoExercise-induced oxidativestress cellularmechanisms and impact onmuscle force produc-tionrdquo Physiological Reviews vol 88 no 4 pp 1243ndash1276 2008

[45] MGNikolaidis andA Z Jamurtas ldquoBlood as a reactive speciesgenerator and redox status regulator during exerciserdquo Archivesof Biochemistry and Biophysics vol 490 no 2 pp 77ndash84 2009

[46] L F Ferreira and M B Reid ldquoMuscle-derived ROS and thiolregulation in muscle fatiguerdquo Journal of Applied Physiology vol104 no 3 pp 853ndash860 2008

[47] S K Powers W B Nelson and M B Hudson ldquoExercise-induced oxidative stress in humans cause and consequencesrdquoFree Radical BiologyampMedicine vol 51 no 5 pp 942ndash950 2011

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Oxidative Medicine and Cellular Longevity 5

The financial support was provided by Centro UniversitarioMetodista do IPA and Coordenacao de Aperfeicoamento dePessoal de Nıvel Superior (CAPES) Dr A Leyva helped withEnglish editing of the paper

References

[1] S Jebb ldquoObesity causes and consequencesrdquo Womenrsquos HealthMedicine vol 1 no 1 pp 38ndash41 2004

[2] F Amirkhizi F Siassi M Djalali and A R ForoushanildquoEvaluation of oxidative stress and total antioxidant capacity inwomenwith general and abdominal adiposityrdquoObesity Researchand Clinical Practice vol 4 no 3 pp e209ndashe216 2010

[3] I Grattagliano V O Palmieri P Portincasa A Moschetta andG Palasciano ldquoOxidative stress-induced risk factors associatedwith the metabolic syndrome a unifying hypothesisrdquo TheJournal of Nutritional Biochemistry vol 19 no 8 pp 491ndash5042008

[4] S Furukawa T FujitaM Shimabukuro et al ldquoIncreased oxida-tive stress in obesity and its impact onmetabolic syndromerdquoTheJournal of Clinical Investigation vol 114 no 12 pp 1752ndash17612004

[5] R E Andersen and J M Jakicic ldquoInterpreting the physicalactivity guidelines for health and weight managementrdquo Journalof Physical Activity and Health vol 6 no 5 pp 651ndash656 2009

[6] S S Ho S S Dhaliwal A P Hills and S Pal ldquoThe effect of12 weeks of aerobic resistance or combination exercise trainingon cardiovascular risk factors in the overweight and obese in arandomized trialrdquo BMC Public Health vol 12 article 704 2012

[7] L H Willis C A Slentz L A Bateman et al ldquoEffects ofaerobic andor resistance training on bodymass and fat mass inoverweight or obese adultsrdquo Journal of Applied Physiology vol113 no 12 pp 1831ndash1837 2012

[8] E Ghahramanloo A W Midgley and D J Bentley ldquoThe effectof concurrent training on blood lipid profile and anthropomet-rical characteristics of previously untrained menrdquo Journal ofPhysical Activity and Health vol 6 no 6 pp 760ndash766 2009

[9] American College of Sports Medicine (ACSM) ACSMrsquos Guide-lines for Exercise Testing and Prescription Lippincott WilliamsampWilkins Baltimore Md USA 8th edition 2009

[10] E T Howley D R Bassett Jr and H G Welch ldquoCriteria formaximal oxygen uptake review and commentaryrdquo Medicineand Science in Sports and Exercise vol 27 no 9 pp 1292ndash13011995

[11] L A Brown C J Kerr P Whiting N Finer J McEneny and TAshton ldquoOxidant stress in healthy normal-weight overweightand obese individualsrdquoObesity vol 17 no 3 pp 460ndash466 2009

[12] E D Wills ldquoMechanisms of lipid peroxide formation in animaltissuesrdquo Biochemical Journal vol 99 no 3 pp 667ndash676 1966

[13] A Z Reznick and L Packer ldquoOxidative damage to proteinsspectrophotometric method for carbonyl assayrdquo Methods inEnzymology vol 233 pp 357ndash363 1994

[14] M Y Aksenov and W R Markesbery ldquoChanges in thiolcontent and expression of glutathione redox system genesin the hippocampus and cerebellum in Alzheimerrsquos diseaserdquoNeuroscience Letters vol 302 no 2-3 pp 141ndash145 2001

[15] H Aebi ldquo[13] Catalase in vitrordquo Methods in Enzymology vol105 pp 121ndash126 1984

[16] H PMisra and I Fridovich ldquoThe role of superoxide anion in theautoxidation of epinephrine and a simple assay for superoxide

dismutaserdquoThe Journal of Biological Chemistry vol 247 no 10pp 3170ndash3175 1972

[17] A Wendel ldquoGlutathione peroxidaserdquo Methods in Enzymologyvol 77 pp 325ndash333 1981

[18] T S Church C P Earnest J S Skinner and S N Blair ldquoEffectsof different doses of physical activity on cardiorespiratoryfitness among sedentary overweight or obese postmenopausalwomen with elevated blood pressurerdquo The Journal of theAmerican Medical Association vol 297 no 19 pp 2081ndash20912007

[19] D M Okay P V Jackson MMarcinkiewicz andM N PapinoldquoExercise and obesityrdquo Primary CaremdashClinics in Office Practicevol 36 no 2 pp 379ndash393 2009

[20] D E R Warburton C W Nicol and S S D Bredin ldquoHealthbenefits of physical activity the evidencerdquo Canadian MedicalAssociation Journal vol 174 no 6 pp 801ndash809 2006

[21] M F F Mediano and R Sichieri ldquoInsulin resistance influencesweight loss in non-obese women who followed a home-based exercise program and slight caloric restrictionrdquo DiabetesResearch and Clinical Practice vol 92 no 3 pp 361ndash367 2011

[22] G Murdolo M Piroddi F Luchetti et al ldquoOxidative stress andlipid peroxidation by-products at the crossroad between adi-pose organ dysregulation and obesity-linked insulin resistancerdquoBiochimie vol 95 no 3 pp 585ndash594 2013

[23] A Chatzinikolaou I Fatouros A Petridou et al ldquoAdiposetissue lipolysis is upregulated in lean and obese men duringacute resistance exerciserdquo Diabetes Care vol 31 no 7 pp 1397ndash1399 2008

[24] M J Ormsbee D C Myung J K Medlin et al ldquoRegulation offat metabolism during resistance exercise in sedentary lean andobese menrdquo Journal of Applied Physiology vol 106 no 5 pp1529ndash1537 2009

[25] H T Rabelo L A Bezerra D F Terra et al ldquoEffects of 24 weeksof progressive resistance training on knee extensors peak torqueand fat-free mass in older womenrdquoThe Journal of Strength andConditioning Research vol 25 no 8 pp 2298ndash2303 2011

[26] R AWashburn E P Kirk B K Smith et al ldquoOne set resistancetraining effect on body composition in overweight youngadultsrdquo Journal of Sports Medicine and Physical Fitness vol 52no 3 pp 273ndash279 2012

[27] S P Glowacki S E Martin AMaurerW Baek J S Green andS F Crouse ldquoEffects of resistance endurance and concurrentexercise on training outcomes in menrdquoMedicine and Science inSports and Exercise vol 36 no 12 pp 2119ndash2127 2004

[28] M I Schaun T Dipp J S Rossato et al ldquoThe effects ofperiodized concurrent and aerobic training on oxidative stressparameters endothelial function and immune response insedentary male individuals of middle agerdquo Cell Biochemistryand Function vol 29 no 7 pp 534ndash542 2011

[29] S Balducci S Zanuso A Nicolucci et al ldquoAnti-inflammatoryeffect of exercise training in subjects with type 2 diabetes andthe metabolic syndrome is dependent on exercise modalitiesand independent of weight lossrdquo Nutrition Metabolism andCardiovascular Diseases vol 20 no 8 pp 608ndash617 2010

[30] K L Rennie N McCarthy S Yazdgerdi M Marmot and EBrunner ldquoAssociation of the metabolic syndrome with bothvigorous and moderate physical activityrdquo International Journalof Epidemiology vol 32 no 4 pp 600ndash606 2003

[31] T A Lakka D E Laaksonen H-M Lakka et al ldquoSedentarylifestyle poor cardiorespiratory fitness and the metabolicsyndromerdquo Medicine and Science in Sports amp Exercise vol 35no 8 pp 1279ndash1286 2003

6 Oxidative Medicine and Cellular Longevity

[32] S E Kahn V G Larson J C Beard et al ldquoEffect of exerciseon insulin action glucose tolerance and insulin secretion inagingrdquoTheAmerican Journal of PhysiologymdashEndocrinology andMetabolism vol 258 no 6 pp E937ndashE943 1990

[33] J P Kirwan W M Kohrt D M Wojta R E Bourey andJ O Holloszy ldquoEndurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-oldmen andwomenrdquoThe Journals of Gerontology vol 48 no 3 pp M84ndashM90 1993

[34] J P Miller R E Pratley A P Goldberg et al ldquoStrengthtraining increases insulin action in healthy 50- to 65-yr-oldmenrdquo Journal of Applied Physiology vol 77 no 3 pp 1122ndash11271994

[35] J Eriksson S Taimela and V A Koivisto ldquoExercise and themetabolic syndromerdquo Diabetologia vol 40 no 2 pp 125ndash1351997

[36] V Saengsirisuwan T R Kinnick M B Schmit and E JHenriksen ldquoInteractions of exercise training and lipoic acid onskeletal muscle glucose transport in obese Zucker ratsrdquo Journalof Applied Physiology vol 91 no 1 pp 145ndash153 2001

[37] M K Teachey Z C Taylor T Maier et al ldquoInteractions ofconjugated linoleic acid and lipoic acid on insulin action in theobese Zucker ratrdquo Metabolism Clinical and Experimental vol52 no 9 pp 1167ndash1174 2003

[38] H Urakawa A Katsuki Y Sumida et al ldquoOxidative stress isassociated with adiposity and insulin resistance in menrdquo TheJournal of Clinical Endocrinology and Metabolism vol 88 no10 pp 4673ndash4676 2003

[39] A RudichN Kozlovsky R Potashnik andN Bashan ldquoOxidantstress reduces insulin responsiveness in 3T3-L1 adipocytesrdquoThe American Journal of PhysiologymdashEndocrinology andMetabolism vol 272 no 5 pp E935ndashE940 1997

[40] B A Maddux W See J C Lawrence Jr A L Goldfine I DGoldfine and J L Evans ldquoProtection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolarconcentrations of120572-lipoic acidrdquoDiabetes vol 50 no 2 pp 404ndash410 2001

[41] A Rudich A Tlrosh R Potashnik R Hemi H Kanety andN Bashan ldquoProlonged oxidative stress impairs insulin-inducedGLUT4 translocation in 3T3-L1 adipocytesrdquo Diabetes vol 47no 10 pp 1562ndash1569 1998

[42] J D Botezelli L T Cambri A C Ghezzi et al ldquoDifferentexercise protocols improvemetabolic syndromemarkers tissuetriglycerides content and antioxidant status in ratsrdquoDiabetologyand Metabolic Syndrome vol 3 no 1 article 35 2011

[43] L L Ji and R Fu ldquoResponses of glutathione system andantioxidant enzymes to exhaustive exercise and hydroperoxiderdquoThe Journal of Applied Physiology vol 72 no 2 pp 549ndash5541992

[44] S K Powers and M J Jackson ldquoExercise-induced oxidativestress cellularmechanisms and impact onmuscle force produc-tionrdquo Physiological Reviews vol 88 no 4 pp 1243ndash1276 2008

[45] MGNikolaidis andA Z Jamurtas ldquoBlood as a reactive speciesgenerator and redox status regulator during exerciserdquo Archivesof Biochemistry and Biophysics vol 490 no 2 pp 77ndash84 2009

[46] L F Ferreira and M B Reid ldquoMuscle-derived ROS and thiolregulation in muscle fatiguerdquo Journal of Applied Physiology vol104 no 3 pp 853ndash860 2008

[47] S K Powers W B Nelson and M B Hudson ldquoExercise-induced oxidative stress in humans cause and consequencesrdquoFree Radical BiologyampMedicine vol 51 no 5 pp 942ndash950 2011

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

6 Oxidative Medicine and Cellular Longevity

[32] S E Kahn V G Larson J C Beard et al ldquoEffect of exerciseon insulin action glucose tolerance and insulin secretion inagingrdquoTheAmerican Journal of PhysiologymdashEndocrinology andMetabolism vol 258 no 6 pp E937ndashE943 1990

[33] J P Kirwan W M Kohrt D M Wojta R E Bourey andJ O Holloszy ldquoEndurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-oldmen andwomenrdquoThe Journals of Gerontology vol 48 no 3 pp M84ndashM90 1993

[34] J P Miller R E Pratley A P Goldberg et al ldquoStrengthtraining increases insulin action in healthy 50- to 65-yr-oldmenrdquo Journal of Applied Physiology vol 77 no 3 pp 1122ndash11271994

[35] J Eriksson S Taimela and V A Koivisto ldquoExercise and themetabolic syndromerdquo Diabetologia vol 40 no 2 pp 125ndash1351997

[36] V Saengsirisuwan T R Kinnick M B Schmit and E JHenriksen ldquoInteractions of exercise training and lipoic acid onskeletal muscle glucose transport in obese Zucker ratsrdquo Journalof Applied Physiology vol 91 no 1 pp 145ndash153 2001

[37] M K Teachey Z C Taylor T Maier et al ldquoInteractions ofconjugated linoleic acid and lipoic acid on insulin action in theobese Zucker ratrdquo Metabolism Clinical and Experimental vol52 no 9 pp 1167ndash1174 2003

[38] H Urakawa A Katsuki Y Sumida et al ldquoOxidative stress isassociated with adiposity and insulin resistance in menrdquo TheJournal of Clinical Endocrinology and Metabolism vol 88 no10 pp 4673ndash4676 2003

[39] A RudichN Kozlovsky R Potashnik andN Bashan ldquoOxidantstress reduces insulin responsiveness in 3T3-L1 adipocytesrdquoThe American Journal of PhysiologymdashEndocrinology andMetabolism vol 272 no 5 pp E935ndashE940 1997

[40] B A Maddux W See J C Lawrence Jr A L Goldfine I DGoldfine and J L Evans ldquoProtection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolarconcentrations of120572-lipoic acidrdquoDiabetes vol 50 no 2 pp 404ndash410 2001

[41] A Rudich A Tlrosh R Potashnik R Hemi H Kanety andN Bashan ldquoProlonged oxidative stress impairs insulin-inducedGLUT4 translocation in 3T3-L1 adipocytesrdquo Diabetes vol 47no 10 pp 1562ndash1569 1998

[42] J D Botezelli L T Cambri A C Ghezzi et al ldquoDifferentexercise protocols improvemetabolic syndromemarkers tissuetriglycerides content and antioxidant status in ratsrdquoDiabetologyand Metabolic Syndrome vol 3 no 1 article 35 2011

[43] L L Ji and R Fu ldquoResponses of glutathione system andantioxidant enzymes to exhaustive exercise and hydroperoxiderdquoThe Journal of Applied Physiology vol 72 no 2 pp 549ndash5541992

[44] S K Powers and M J Jackson ldquoExercise-induced oxidativestress cellularmechanisms and impact onmuscle force produc-tionrdquo Physiological Reviews vol 88 no 4 pp 1243ndash1276 2008

[45] MGNikolaidis andA Z Jamurtas ldquoBlood as a reactive speciesgenerator and redox status regulator during exerciserdquo Archivesof Biochemistry and Biophysics vol 490 no 2 pp 77ndash84 2009

[46] L F Ferreira and M B Reid ldquoMuscle-derived ROS and thiolregulation in muscle fatiguerdquo Journal of Applied Physiology vol104 no 3 pp 853ndash860 2008

[47] S K Powers W B Nelson and M B Hudson ldquoExercise-induced oxidative stress in humans cause and consequencesrdquoFree Radical BiologyampMedicine vol 51 no 5 pp 942ndash950 2011

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom