research article tai chi exercise increases sod activity and total...

Research ArticleTai Chi Exercise Increases SOD Activity and TotalAntioxidant Status in Saliva and Is Linked to an Improvement ofPeriodontal Disease in the Elderly

Viacutector Manuel Mendoza-Nuacutentildeez1 Beatriz Hernaacutendez-Monjaraz1

Edelmiro Santiago-Osorio2 Joseacute Miguel Betancourt-Rule3 and Mirna Ruiz-Ramos1

1 Unidad de Investigacion en Gerontologıa Facultad de Estudios Superiores Zaragoza Universidad Nacional Autonoma de Mexico(UNAM) Guelatao No 66 Delegacion Iztapalapa 09230 Mexico DF Mexico

2 Laboratorio de Biologıa Celular y Molecular del Cancer UIDCC FES-Zaragoza UNAM Mexico DF Mexico3 Departamento de Ciencias de la Salud Universidad Autonoma Metropolitana-Iztapalapa Apartado Postal 55-535 09340 MexicoDF Mexico

Correspondence should be addressed to Vıctor Manuel Mendoza-Nunez mendovicunammx

Received 6 January 2014 Accepted 13 February 2014 Published 26 March 2014

Academic Editor Vladimir Jakovljevic

Copyright copy 2014 Vıctor Manuel Mendoza-Nunez et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The aimof this studywas to determine the effect of Tai Chi on biologicalmarkers of oxidative stress in saliva and its relationshipwithperiodontal disease (PD) in older adults We carried out a quasi-experimental study with a sample of 71 sedentary volunteers withPD who were divided into a control group of 34 subjects and an experimental group of 37 subjects who performed Tai Chi 5 days aweek for a period of 6months PD statuswas characterized using the PeriodontalDisease Index (PDI) Superoxide dismutase (SOD)total antioxidant status (TAS) and TBARS levels of both groups were measured by spectrophotometric methods In additioninflammation markers (TNF-120572 IL-1120573 IL-6 IL-8 and IL-10) were measured by flow cytometry We found a statistically significantincrease in SOD activity (119875 lt 0001) and TAS concentration (119875 lt 005) whereas levels of IL-1120573were significantly lower (119875 lt 001)Likewise a statistically significant decrease in the PDI (119875 lt 005) was observed in subjects who performed Tai Chi during a periodof 6 months Our findings suggest that the practice of Tai Chi has both antioxidant and anti-inflammatory effects that are linked tothe improvement of PD in older adults

1 Introduction

TaiChi (TC) is a traditionalChinese exercise linked tomartialarts that has been shown to have a positive effect on aerobiccapacity muscle strength balance and motor control [1]The practice of TC involves exercises that promote postureflexibility relaxation wellness and mental concentration[2] TC is characterized by extremely slow movementsabsolute continuity without interruption or pause and atotal awareness and focus on its implementation [3] Unlikemany exercises that are characterized by muscle strength andeffort TC movements are slow soft and lightweight [1ndash3]TC is classified as a moderate type of exercise as its intensitydoes not exceed 55 of an individualrsquos maximum oxygen

expenditure and 60 of an individualrsquos maximum heart rate[4]

Recently the practice of TC has been promoted inthe elderly population due to its beneficial health effectsincluding among others the prevention of falls osteoporosishypertension and diabetes mellitus as well as rheumatolog-ical and neurological disorders [2 5 6] Our research grouphas shown that regular practice of TC increases superoxidedismutase activity and total antioxidant status in the serumof the elderly [7 8] We hypothesize that the antioxidanteffect of TC may also be observed in saliva and could havea positive effect on the oral health of the elderly Periodontaldisease (PD) is one of the major chronic oral diseases in theelderly and is characterized by a destructive inflammatory

Hindawi Publishing CorporationOxidative Medicine and Cellular LongevityVolume 2014 Article ID 603853 6 pageshttpdxdoiorg1011552014603853

2 Oxidative Medicine and Cellular Longevity

Participants recruited71

ExcludedDid not comply withinclusion criteria 10Written informed

consent

Periodontal disease index and oral hygiene index

Sample collection

Basic trial and assignment

Control group30 Tai Chi group

31

Followed for six months Followed for

six months

Data analyzed25 Data analyzed

24

Figure 1 General scheme for study tracking

process that affects the supporting tissues of the teeth causingboth alveolar bone resorption and formation of periodontalpockets and eventually leads to tooth loss [9 10] It has beendemonstrated that oxidative stress in the saliva is an etiologicfactor and pathophysiologic of PD [11ndash15] Therefore theaim of this study is to determine the effect of Tai Chi onbiological markers of oxidative stress in the saliva as well asits relationship with periodontal disease in the elderly

2 Methods

21 Design and Subjects A quasi-experimental study wasperformed with a sample size of 71 sedentary volunteerswith a clinical diagnostic of periodontal disease The agerange of the subjects was 60ndash74 years Volunteers takingnutritional supplements or anti-inflammatory medicationswere excluded from the study (119899 = 10) All participants gavetheir written informed consent for inclusion in the studyTheinvestigation protocol was approved by the Ethics Committeeof the Universidad Nacional Autonoma deMexico (UNAM)Zaragoza Campus (IN306213-2)

Subjects were divided into two groups a control group(CG) with 30 subjects who did not exercise and an exper-imental group (EG) with 31 subjects who performed TaiChi (Eight-Form) [16] 5 days a week for 60-minute sessionsunder the supervision of a qualified instructor for 6 months(Figure 1) Twelve subjects (5 from the experimental and

7 from the control group) were excluded from the studyanalysis as they were unable to complete the study

22 Periodontal Health Status The periodontal health statusof each subject was measured using the Periodontal DiseaseIndex (PDI) The examination procedure involved the inser-tion of a graduated periodontal probe between the subjectsrsquoteeth and gums at a standard force to measure pocket depthThese assessments were made for sextants of the dentitionwith the thirdmolars only included if the secondmolars weremissing The final periodontal disease score was determinedby taking the mean of the sextant scores [17]

Oral cleanliness was measured using the Oral HygieneIndex-Simplified (OHI-S) Oral debris and calculus wereestimated by running the side of an explorer along the surfaceof the examined teeth including the upper first molars (teeth16 and 26) the lingual faces of the lower first molars (teeth 36and 46) and the labial faces of the upper right (tooth 11) andlower left (tooth 31) incisors [18]

23 Sample Collection and Preparation Whole unstimulatedsaliva samples were collected from both groups (controland experimental) before (baseline) and after the six-monthperiod The samples were obtained one to two hours afteran eight-hour fasting period and were collected in 15mLpolypropylene tubes Saliva was allowed to pool in the bottomof the mouth and was drained into the collection tube At the

Oxidative Medicine and Cellular Longevity 3

Table 1 Biochemical parameters of the study population by group

Control (119899 = 25) Tai Chi (119899 = 24)Baseline Six months Baseline Six months

HbA1c () 656 plusmn 180 896 plusmn 24 809 plusmn 22 729 plusmn 23Cholesterol (mgdL) 2133 plusmn 392 2096 plusmn 294 2126 plusmn 442 2095 plusmn 366Triglycerides (mgdL) 1751 plusmn 385 2076 plusmn 419 1608 plusmn 764 1958 plusmn 130HDL (mgdL) 3933 plusmn 802 4033 plusmn 35 44375 plusmn 96 5270 plusmn 1198Albumin (gdL) 476 plusmn 005 477 plusmn 012 475 plusmn 020 469 plusmn 025Values are means plusmn SE ANOVA 119875 gt 005 HbA1c glycosylated hemoglobin HDL High-density lipoproteins

Table 2 Oxidative stress markers baseline and postintervention by group


TAS (mmolL) 072 plusmn 035 062 plusmn 029 053 plusmn 033 070 plusmn 035lowast

SOD (UIL) 263 plusmn 18 233 plusmn 11 162 plusmn 083 279 plusmn 16dagger

Lipoperoxides (120583molL) 014 plusmn 014 008 plusmn 009 011 plusmn 007 014 plusmn 009Values are means plusmn SE Repeated measures analysis of variance lowast119875 lt 001 dagger119875 lt 0001 TAS total antioxidant status SOD superoxide dismutase

end of the collection period saliva samples were centrifugedat 2500 rpm for 10 minutes The supernatant fraction wasthen aliquoted into storage vials and kept at minus80∘C untilfurther analysis

24 Saliva TBARS The TBARS assay was performed usingwhole saliva as described by Jentzsch et al (1996) [19] In theTBARS assay one molecule of malondialdehyde reacts withtwomolecules of thiobarbituric acid (TBA) producing a pinkpigment with an absorption peak of 535 nm Amplificationof peroxidation during the assay is prevented by the additionof the chain-breaking antioxidant butylated hydroxytoluene(BHT)

25 Saliva Total Antioxidant Status (TAS) Antioxidant quan-tification was performed by monitoring 221015840-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) (ABTS+) radical forma-tion (Randox Laboratories Ltd Crumlin Co UK) Theantioxidants present suppressed the bluish-green staining ofthe ABTS+ cation which is proportional to the antioxidantconcentration level The reaction kinetics were measuredusing a colorimetric technique in an Autoanalyzer VitalabEclipse Merck (Dieren The Netherlands) [20]

26 Saliva Superoxide Dismutase (SOD) Xanthine and xan-thine oxidase (XOD) were used to generate superoxide rad-icals which react with 2-(4-iodophenyl)-3-(4-nitrophenyl)-5-phenyltetrazolium chloride to produce a red formazan dyeSOD activity was assessed by measuring the degree of inhi-bition of the reaction (Randox Laboratories Ltd CrumlinCo UK) The kinetics of SOD activity were measured usinga colorimetric technique in an Autoanalyzer Vitalab EclipseMerck (Dieren The Netherlands) [21]

27 Quantification of Cytokines Aliquots of each saliva sam-plewere assayed by flow cytometry (CBAKit Human Inflam-matory Cytokine BD Biosciences Becton Dickinson andCompany USA) to determine the levels of interleukin 1-beta(IL-1120573) interleukin 6 (IL6) interleukin 8 (IL-8) interleukin10 (IL-10) and tumor necrosis factor-alpha (TNF-120572) [22]

28 Statistical Analysis Data were analyzed using descriptivestatistics where we determined the mean and standard error(SE) and performed a repeated measures analysis of variance(repeatedmeasures ANOVA) A 119875 value of lt005 was consid-ered statistically significant 119875 values were determined usingthe statistical analysis program SPSS version 160

3 Results

31 Biochemical Characteristics In Table 1 the biochemi-cal values related to glycosylated hemoglobin cholesteroltriglycerides HDL and Albumin for baseline and six monthslater are shown revealing no statistically significant differ-ences between the groups

32 Changes in Oxidative Stress Markers by InterventionWith respect to the oxidative stress markers in saliva asignificant increase in the total antioxidant activity (053 plusmn033mmolL at baseline versus 070 plusmn 035mmolL afterintervention 119875 lt 001) and in SOD activity (162 plusmn 083UILat baseline versus 279 plusmn 16UIL after intervention 119875 lt0001) was found in the group that practiced Tai Chi forsix months No significant differences were observed in thevalues of lipoperoxides (119875 gt 005) (Table 2)

33 Changes in Inflammatory Markers by Intervention Asignificant decrease in the concentration of interleukin 1120573


Table 3 Inflammatory markers baseline and postintervention by group


TNF-120572 (pgmL) 2004 plusmn 150 5325 plusmn 223 05119 plusmn 0009 42410 plusmn 0435IL-1120573 (pgmL) 118018 plusmn 244 135337 plusmn 176 78362 plusmn 1749 62497 plusmn 1967lowast

IL-6 (pgmL) 2080 plusmn 501 5945 plusmn 138 1866 plusmn 725 476 plusmn 193dagger

IL-8 (pgmL) 356053 plusmn 809 321566 plusmn 260 497124 plusmn 835 225242 plusmn 330IL-10 (pgmL) 315 plusmn 066 025 plusmn 021 021 plusmn 25 29 plusmn 15Values are means plusmn SE Repeated measures analysis of variance lowast119875 lt 001 dagger119875 = 009 TNF-120572 tumor necrosis factor alpha IL-1120573 interleukin 1120573 IL-6interleukin 6 IL-8 interleukin 8 IL-10 interleukin 10

Table 4 Oral hygiene index-simplified and periodontal disease index by group


OHIS 243 plusmn 03 245 plusmn 02 245 plusmn 03 246 plusmn 03PDI (mm) 32188 plusmn 06 37960 plusmn 04 36267 plusmn 09 32813 plusmn 08lowast

Values are means plusmn SE Repeated measures analysis of variance lowast119875 lt 005 OHIS oral hygiene index-simplified PDI periodontal disease index

in saliva (78362 plusmn 1749 pgmL at baseline versus 62497 plusmn1967 pgmL after intervention 119875 lt 001) was found in theexperimental group after practicing Tai Chi Additionallya borderline statistically significant decrease in the concen-tration of IL-6 was observed in the same group (1866 plusmn725 pgmL at baseline versus 476 plusmn 193 pgmL after inter-vention 119875 = 009) (Table 3)

34 Changes in Periodontal Disease by Intervention Nosignificant differences were observed in the oral hygieneindex-simplified in any of the groups (119875 gt 005) Howevera statistically significant decrease in the periodontal diseaseindex was observed in the experimental group (362 plusmn 09baseline versus 328 plusmn 08 after intervention 119875 lt 005)(Table 4)

4 Discussion

Oxidative stress (OxS) and chronic inflammation (CI) arebiological changes inherent to aging and are risk factors forseveral chronic degenerative diseases such as periodontaldisease (PD) one of themost prevalent aging-related diseases[23ndash25] Several preventive and therapeutic options havebeen proposed to counteract these biochemical alterationsincluding among others dietary supplementation resultingin antioxidant effects antioxidant vitamins and administra-tion of NSAIDs at low doses [26ndash29] It has also recentlybeen shown that a healthy diet and regular moderate physi-cal exercise have antioxidant and anti-inflammatory effectsreducing the risk of chronic diseases or contributing to itstreatment [30ndash32]Walking and the practice of TC are amongthe modalities of moderate physical exercise recommendedfor the maintenance or improvement of health in the elderly[1 33] Some studies have shown that Tai Chi has positiveeffects on cardiorespiratory function and themusculoskeletalsystem improving a personrsquos ability to control their postureand balance which consequently decreases their frequency

of falls [1ndash3] Likewise it has been shown that the practiceof Tai Chi has a positive effect on the efficiency of theantioxidant system in adult subjects and the elderly Thus ithas been proposed that the practice of Tai Chi could preventand control chronic degenerative diseases that occur withage [7 8 34 35] Additionally it has been observed thatthe regular practice of physical exercise has been linked to asignificantly lower frequency of periodontal disease in adultsubjects [36ndash39]

Our results indicate a statistically significant decrease inthe rate of periodontal disease in subjects practicing Tai ChiThese findings support the proposal that regular physicalexercise promotes biological changes that positively impactthe pathophysiological process of periodontal disease Asignificant increase in the total antioxidant status and SODactivity in the experimental group were found suggestingthat one of the possible mechanisms involved in the improve-ment of periodontal disease is the antioxidant effect broughtabout by the practice of Tai Chi Oxidative stress has beenlinked to the pathophysiology of PD because reactive oxygenspecies (ROS) may selectively damage proteoglycans associ-ated with soft periodontal tissues and the alveolar bone aswell as chains of proline type 1 collagen significantly alteringfibroblast functions such as adhesion and proliferation as wellas their half-life [40ndash43] The excessive production of ROSby neutrophils and fibroblasts in periodontal tissues activatesNF-120581B and triggers the signaling cascade that activatesosteoclasts leading to inflammation [44] Additionally thegeneration of OxS causes an imbalance of metalloproteinasesand their tissue inhibitors leading to the degradation ofperiodontal tissue [45]

It has also been shown that physical exercise lowers thelevels of markers of inflammation [30 46 47] Thus thedecrease of IL-1120573 observed in saliva in the experimentalgroup suggests that the practice of Tai Chi has an anti-inflammatory effect on periodontal tissue The mechanismsof these changes have not been fully elucidated but it has


been proposed that this effect may result from the regulationof cytokine expression caused by muscle contractions duringexercise [48]

Finally it has been noted that the effect of moderatephysical exercise such as Tai Chi on oxidative stress islinked to an adaptive process influenced by the change inthe bodyrsquos redox balance in favor of more alkaline conditionsin the cell The reactive species generated during physicalactivity act as the signal that is necessary for the activationof the MAPK proteins p38 and ERK1ERK2 which in turnactivate the transcription factor sensitive to the redox stateNF-120581B via activation of the kinase that phosphorylates theinhibitor of this factor (I120581B) Once freed of its inhibitor NF-120581B is transported into the nucleus where it can promote thesynthesis of various antioxidant enzymes such as MnSOD[7 8 45 49 50] Our findings suggest that the antioxidanteffect of Tai Chi has a beneficial effect on oral health in theelderly

5 Conclusions

Our results show that the practice of Tai Chi has anantioxidant and anti-inflammatory oral effect supportingthe proposal that the regular practice this type of exercisecan contribute to the prevention and control of periodontaldisease during the aging process Thus our findings supportthe proposal to recommend the regular practice of Tai Chi asa coadjuvant for the prevention and treatment of periodontaldisease in older adults

Conflict of Interests

There are no financial conflict of interests

Acknowledgments

This work was supported by Direccion General de Asuntosdel Personal Academico Universidad Nacional Autonomade Mexico (DGAPA UNAM) PAPIIT IN306213-2 and Pos-grado en Ciencias Biologicas UNAM

References

[1] H Blake and H Hawley ldquoEffects of tai chi exercise on physicaland psychological health of older peoplerdquo Current Aging Sci-ence vol 5 no 1 pp 19ndash27 2012

[2] C Lan S Y Chen J S Lai and A M Wong ldquoTai ChiChuan in medicine and health promotionrdquo Evidence-BasedComplementary and Alternative Medicine vol 2013 Article ID502131 17 pages 2013

[3] R Jahnke L Larkey C Rogers J Etnier and F Lin ldquoAcomprehensive review of health benefits of qigong and tai chirdquoThe American Journal of Health Promotion vol 24 no 6 ppe1ndashe25 2010

[4] J X Li Y Hong and K M Chan ldquoTai chi physiologicalcharacteristics and beneficial effects on healthrdquo British Journalof Sports Medicine vol 35 no 3 pp 148ndash156 2001

[5] Y-K Chang Y-H Nien C-L Tsai and J L Etnier ldquoPhysicalactivity and cognition in older adults the potential of Tai Chi

Chuanrdquo Journal of Aging and Physical Activity vol 18 no 4 pp451ndash472 2010

[6] F Li K J Fisher PHarmerD Irbe RG Tearse andCWeimerldquoTai chi and self-rated quality of sleep and daytime sleepinessin older adults a randomized controlled trialrdquo Journal of theAmerican Geriatrics Society vol 52 no 6 pp 892ndash900 2004

[7] J Rosado-Perez E Santiago-Osorio R Ortiz and V MMendoza-Nunez ldquoTai Chi improves oxidative stress inMexicanolder adultsrdquo The Journal of Nutrition Health amp Aging vol 16pp 642ndash646 2012

[8] J Rosado-Perez R Rocıo Ortiz E Santiago-Osorio and VM Mendoza-Nunez VM ldquoEffect of Tai Chi versus walking onoxidative stress in Mexican older adultsrdquo Oxidative Medicineand Cellular Longevity vol 2013 Article ID 298590 8 pages2013

[9] C M E Champagne W Buchanan M S Reddy J S PreisserJ D Beck and S Offenbacher ldquoPotential for gingival crevicefluid measures as predictors of risk for periodontal diseasesrdquoPeriodontology 2000 vol 31 pp 167ndash180 2003

[10] M Tezal and S Uribe ldquoA lack of consensus in the measurementmethods for and definition of periodontitisrdquo Journal of theAmerican Dental Association vol 142 no 6 pp 666ndash667 2011

[11] P Dahiya R Kamal R Gupta R Bhardwaj K Chaudhary andS Kaur ldquoReactive oxygen species in periodontitisrdquo Journal ofIndian Society of Periodontology vol 17 no 4 pp 411ndash416 2013

[12] I L C Chapple and J B Matthews ldquoThe role of reactive oxygenand antioxidant species in periodontal tissue destructionrdquoPeriodontology 2000 vol 43 no 1 pp 160ndash232 2007

[13] I L C Chapple G I Mason I Garner et al ldquoEnhancedchemiluminescent assay for measuring the total antioxidantcapacity of serum saliva and crevicular fluidrdquoAnnals of ClinicalBiochemistry vol 34 no 4 pp 412ndash421 1997

[14] S-C Kim O-S Kim O-J Kim Y-J Kim and H-J ChungldquoAntioxidant profile of whole saliva after scaling and rootplaning in periodontal diseaserdquo Journal of Periodontal andImplant Science vol 40 no 4 pp 164ndash171 2010

[15] G R Brock C J Butterworth J B Matthews and I L CChapple ldquoLocal and systemic total antioxidant capacity inperiodontitis and healthrdquo Journal of Clinical Periodontology vol31 no 7 pp 515ndash521 2004

[16] F Li K J Fisher PHarmer andM Shirai ldquoA simpler eight-formEasy Tai Chi for elderly adultsrdquo Journal of Aging and PhysicalActivity vol 11 no 2 pp 206ndash218 2003

[17] S P Ramfjord ldquoThe Periodontal Disease Index (PDI)rdquo Journalof Periodontology vol 38 no 6 pp 602ndash610 1967

[18] J C Greene and J R Vermillion ldquoThe simplified oral hygieneindexrdquo Journal of the American Dental Association vol 68 pp7ndash13 1964

[19] A M Jentzsch H Bachmann P Furst and H K BiesalskildquoImproved analysis of malondialdehyde in human body fluidsrdquoFree Radical Biology and Medicine vol 20 no 2 pp 251ndash2561996

[20] V M Mendoza-Nunez M Ruiz-Ramos M A Sanchez-Rodrıguez R Retana-Ugalde and J LMunoz-Sanchez ldquoAging-related oxidative stress in healthy humansrdquoThe Tohoku Journalof Experimental Medicine vol 231 pp 216ndash268 2007

[21] E B Cook J L Stahl L Lowe et al ldquoSimultaneous measure-ment of six cytokines in a single sample of human tears usingmicroparticle-based flow cytometry allergics vs non-allergicsrdquoJournal of Immunological Methods vol 254 no 1-2 pp 109ndash1182001


[22] J A Knight Free Radicals Antioxidants Aging amp DiseaseAACC PRESS Washington DC USA 1999

[23] C FranceschiM Bonafe S Valensin et al ldquoInflamm-aging Anevolutionary perspective on immunosenescencerdquo Annals of theNew York Academy of Sciences vol 908 pp 244ndash254 2000

[24] E S Cannizzo C C Clement R Sahu C Follo and L San-tambrogio ldquoOxidative stress inflamm-aging and immunose-nescencerdquo Journal of Proteomics vol 74 no 11 pp 2313ndash23232011

[25] G Campisi M Chiappelli M De Martinis et al ldquoPathophysi-ology of age-related diseasesrdquo Immunity amp Ageing vol 6 no 122009

[26] W Stahl and H Sies ldquoAntioxidant defense vitamins E and Cand carotenoidsrdquo Diabetes vol 46 no 2 pp S14ndashS18 1997

[27] T-Y Cheng Z Zhu S Masuda and N C Morcos ldquoEffects ofmultinutrient supplementation on antioxidant defense systemsin healthy human beingsrdquo Journal of Nutritional Biochemistryvol 12 no 7 pp 388ndash395 2001

[28] M Faizuddin F Tarannum N Korla and S Swamy ldquoAssocia-tion between long-term aspirin use and periodontal attachmentlevel in humans a cross-sectional investigationrdquo AustralianDental Journal vol 57 no 1 pp 45ndash50 2012

[29] H Zhang and C Zhang ldquoVasoprotection by dietary supple-ments and exercise role of TNF120572 signalingrdquo ExperimentalDiabetes Research vol 2012 Article ID 972679 6 pages 2012

[30] J Rosado-Perez E Santiago-Osorio R Ortiz and V MMendoza-Nunez ldquoModerate physical activity diminishesoxidative stress and the inflammatory process in elderlyrdquoHealthMed Journal vol 5 pp 173ndash179 2011

[31] M Battino and B Mezzetti ldquoUpdate on fruit antioxidantcapacity a key tool for Mediterranean dietrdquo Public healthnutrition vol 9 no 8 pp 1099ndash1103 2006

[32] F El-Khoury B Cassou M A Charles and P Dargent-Molina ldquoThe effect of fall prevention exercise programmeson fall induced injuries in community dwelling older adultssystematic review and meta-analysis of randomised controlledtrialsrdquo British Medical Journal vol 347 Article ID f6234 2013

[33] H A Yeom C Keller and J Fleury ldquoInterventions for promot-ingmobility in community-dwelling older adultsrdquo Journal of theAmerican Academy of Nurse Practitioners vol 21 no 2 pp 95ndash100 2009

[34] J AGoonAHNoorAiniMMusalmahMY YasminAnumWMWanNazaimoon andW ZWanNgah ldquoEffect of Tai Chiexercise on DNA damage antioxidant enzymes and oxidativestress in middle-age adultsrdquo Journal of Physical Activity andHealth vol 6 no 1 pp 43ndash54 2009

[35] A Palasuwan D Suksom I Margaritis S Soogarun and A SRousseau ldquoEffects of tai chi training on antioxidant capacity inpre- and postmenopausal womenrdquo Journal of Aging Researchvol 2011 Article ID 234696 8 pages 2011

[36] A T Merchant W Pitiphat E B Rimm and K JoshipuraldquoIncreased physical activity decreases periodontitis risk inmenrdquo European Journal of Epidemiology vol 18 no 9 pp 891ndash898 2003

[37] A E Sanders G D Slade T R Fitzsimmons and PM BartoldldquoPhysical activity inflammatory biomarkers in gingival crevic-ular fluid and periodontitisrdquo Journal of Clinical Periodontologyvol 36 no 5 pp 388ndash395 2009

[38] H A Bawadi Y S Khader T F HarounM Al-Omari and R FTayyem ldquoThe association between periodontal disease physicalactivity and healthy diet among adults in Jordanrdquo Journal ofPeriodontal Research vol 46 no 1 pp 74ndash81 2011

[39] M S Al-Zahrani E A Borawski and N F Bissada ldquoIncreasedphysical activity reduces prevalence of periodontitisrdquo Journal ofDentistry vol 33 no 9 pp 703ndash710 2005

[40] R JWaddington RMoseley and G Embery ldquoReactive oxygenspecies a potential role in the pathogenesis of periodontaldiseasesrdquo Oral Diseases vol 6 no 3 pp 138ndash151 2000

[41] L Rittie J-C Monboisse M-C Gorisse and P Gillery ldquoMal-ondialdehyde binding to proteins dramatically alters fibroblastfunctionsrdquo Journal of Cellular Physiology vol 191 no 2 pp 227ndash236 2002

[42] D Wei X-L Zhang Y-Z Wang C-X Yang and G ChenldquoLipid peroxidation levels total oxidant status and superoxidedismutase in serum saliva and gingival crevicular fluid inchronic periodontitis patients before and after periodontaltherapyrdquo Australian Dental Journal vol 55 no 1 pp 70ndash782010

[43] S Moore K A C Calder N J Miller and C A Rice-EvansldquoAntioxidant activity of saliva and periodontal diseaserdquo FreeRadical Research vol 21 no 6 pp 417ndash425 1994

[44] E Jimi K Aoki H Saito et al ldquoSelective inhibition of NF-120581B blocks osteoclastogenesis and prevents inflammatory bonedestruction in vivordquoNatureMedicine vol 10 no 6 pp 617ndash6242004

[45] P Pozo M A Valenzuela C Melej et al ldquoLongitudinalanalysis of metalloproteinases tissue inhibitors of metallopro-teinases and clinical parameters in gingival crevicular fluid fromperiodontitis-affected patientsrdquo Journal of Periodontal Researchvol 40 no 3 pp 199ndash207 2005

[46] D R Taaffe T B Harris L Ferrucci J Rowe and T E SeemanldquoCross-sectional and prospective relationships of interleukin-6 and c-reactive protein with physical performance in elderlypersons MacArthur studies of successful agingrdquo Journals ofGerontology A vol 55 no 12 pp M709ndashM715 2000

[47] M R Irwin and R Olmstead ldquoMitigating cellular inflammationin older adults a randomized controlled trial of tai chi chihrdquoTheAmerican Journal of Geriatric Psychiatry vol 20 no 9 pp 746ndash772 2012

[48] B K Pedersen and M A Febbraio ldquoMuscle as an endocrineorgan focus on muscle-derived interleukin-6rdquo PhysiologicalReviews vol 88 no 4 pp 1379ndash1406 2008

[49] M-C Gomez-Cabrera E Domenech and J Vina ldquoModerateexercise is an antioxidant upregulation of antioxidant genes bytrainingrdquo Free Radical Biology and Medicine vol 44 no 2 pp126ndash131 2008

[50] C Leeuwenburgh R Fiebig R Chandwaney and L L JildquoAging and exercise training in skeletal muscle responses ofglutathione and antioxidant enzyme systemsrdquo The AmericanJournal of PhysiologymdashRegulatory Integrative and ComparativePhysiology vol 267 no 2 pp R439ndashR445 1994

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014


MEDIATORSINFLAMMATION

of


Behavioural Neurology

EndocrinologyInternational Journal of



Disease Markers


BioMed Research International

OncologyJournal of



Oxidative Medicine and Cellular Longevity


PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of



Computational and Mathematical Methods in Medicine

OphthalmologyJournal of


Diabetes ResearchJournal of



Research and TreatmentAIDS


Gastroenterology Research and Practice


Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom


Participants recruited71

ExcludedDid not comply withinclusion criteria 10Written informed

consent

Periodontal disease index and oral hygiene index

Sample collection

Basic trial and assignment

Control group30 Tai Chi group

31

Followed for six months Followed for

six months

Data analyzed25 Data analyzed

24

Figure 1 General scheme for study tracking

process that affects the supporting tissues of the teeth causingboth alveolar bone resorption and formation of periodontalpockets and eventually leads to tooth loss [9 10] It has beendemonstrated that oxidative stress in the saliva is an etiologicfactor and pathophysiologic of PD [11ndash15] Therefore theaim of this study is to determine the effect of Tai Chi onbiological markers of oxidative stress in the saliva as well asits relationship with periodontal disease in the elderly

2 Methods

21 Design and Subjects A quasi-experimental study wasperformed with a sample size of 71 sedentary volunteerswith a clinical diagnostic of periodontal disease The agerange of the subjects was 60ndash74 years Volunteers takingnutritional supplements or anti-inflammatory medicationswere excluded from the study (119899 = 10) All participants gavetheir written informed consent for inclusion in the studyTheinvestigation protocol was approved by the Ethics Committeeof the Universidad Nacional Autonoma deMexico (UNAM)Zaragoza Campus (IN306213-2)

Subjects were divided into two groups a control group(CG) with 30 subjects who did not exercise and an exper-imental group (EG) with 31 subjects who performed TaiChi (Eight-Form) [16] 5 days a week for 60-minute sessionsunder the supervision of a qualified instructor for 6 months(Figure 1) Twelve subjects (5 from the experimental and

7 from the control group) were excluded from the studyanalysis as they were unable to complete the study

22 Periodontal Health Status The periodontal health statusof each subject was measured using the Periodontal DiseaseIndex (PDI) The examination procedure involved the inser-tion of a graduated periodontal probe between the subjectsrsquoteeth and gums at a standard force to measure pocket depthThese assessments were made for sextants of the dentitionwith the thirdmolars only included if the secondmolars weremissing The final periodontal disease score was determinedby taking the mean of the sextant scores [17]

Oral cleanliness was measured using the Oral HygieneIndex-Simplified (OHI-S) Oral debris and calculus wereestimated by running the side of an explorer along the surfaceof the examined teeth including the upper first molars (teeth16 and 26) the lingual faces of the lower first molars (teeth 36and 46) and the labial faces of the upper right (tooth 11) andlower left (tooth 31) incisors [18]

23 Sample Collection and Preparation Whole unstimulatedsaliva samples were collected from both groups (controland experimental) before (baseline) and after the six-monthperiod The samples were obtained one to two hours afteran eight-hour fasting period and were collected in 15mLpolypropylene tubes Saliva was allowed to pool in the bottomof the mouth and was drained into the collection tube At the
















3 Results
















4 Discussion








5 Conclusions




Acknowledgments


References


























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of































3 Results
















4 Discussion








5 Conclusions




Acknowledgments


References


























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of




























4 Discussion








5 Conclusions




Acknowledgments


References


























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of



















5 Conclusions




Acknowledgments


References


























































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of



















































of






Disease Markers



OncologyJournal of





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research article tai chi exercise increases sod activity and total...

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