The influence of dental occlusion on the body balance in unstable platform increases after high

Neuroscience Letters 617(2016)116–121Contents lists available at ScienceDirectNeuroscienceLettersj o u r n a l h o m e p a g e :w w w.e l s e v i e r.c o m /l o c a t e /n e u l etResearchpaperThe influence of dental occlusion on the body balance in unstable platform increases after high intensity exerciseSonia Julià-Sánchez a ,∗,Jesús Álvarez-Herms a ,Hannes Gatterer b ,Martin Burtscher b ,Teresa Pagès a ,Ginés Viscor aa Departament de Fisiologia i Immunologia,Universitat de Barcelona (UB),Avda.Diagonal 643,Edifici Ramon Margalef 3A,E-08028Barcelona,Spain bDepartment of Sport Science,Medical Section,University Innsbruck,Fürstenweg 185,6020Innsbruck,Austriah i g h l i g h t s•The relationship between dental occlusion and balance control remains unclear.•10physically active subjects were analyzed prior to and following a maximal exercise.•Body balance was evaluated in stable and unstable levels with occlusion in ICP and CR.•Body balance was significantly better when dental occlusion was set in CR.•Dental occlusion strongly influenced balance control in fatigue.a r t i c l ei n f oArticle history:Received 18October 2015Received in revised form 17January 2016Accepted 2February 2016Available online 11February 2016Keywords:Balance control ExerciseUnstable platform Dental occlusiona b s t r a c tExisting evidence suggests that body balance ability is associated with dental occlusion.The purpose of this study was to determine whether:(i)there are differences in balance between opposed dental occlu-sion (intercuspal position,ICP;cotton rolls,CR)for two extreme levels of stability and (ii)the influence of dental occlusion on the balance control gets stronger under fatigue conditions.To this aim,various mea-sures for assessing postural control in ten physically active subjects were obtained prior to and following a maximal lower limbs exercise consisting in six sets of fifteen seconds stretch-shortening cycle jumping.Balance control at stable and unstable condition was evaluated on an unstable platform Balance System SD for both dental occlusion conditions at random order.Metabolic and psychological measurements ensured the high intensity of the exercise.At unstable level,balance control was significantly improved in the CR condition,for both rest (p =0.03)and fatigue (p <0.001).Whereas at stable level,the influence of dental occlusion only reached significance in fatigue condition (p =0.04).It could be concluded that the sensory information linked to the dental occlusion for the balance control comes strongly into effect when more difficult conditions for the balance control are present (i.e.,unstable conditions,fatigue).©2016Elsevier Ireland Ltd.All rights reserved.1.IntroductionPostural control is a complex system that involves different sen-sory and motor components,such as sensory inputs from the visual,somatosensory and vestibular systems,that must be integrated at the central nervous system in order to regulate orientation and stabilization of the body segments [1].∗Corresponding author.E-mail addresses:soniajulia@ ,soniajulia@ (S.Julià-Sánchez),jesusalvarez@ (J.Álvarez-Herms),hannes.gatterer@uibk.ac.at (H.Gatterer),martin.burtscher@uibk.ac.at (M.Burtscher),tpages@ (T.Pagès),gviscor@ (G.Viscor).Over the last few years,a growing interest has focused on the potential correlation between the stomatognathic system and the body balance.Recently,it has been proposed that the stom-atognathic system may contribute (∼2%)to the postural balance regulation [2].In particular,the presence of some specific mal-occlusal traits seems to negatively influence the balance control [3].From a neurophysiological perspective,the motor influences between the masticatory and cervical muscles may explain the influence of dental occlusion on the body balance [4].The observa-tion of a beneficial effect of balancing occlusion on several postural muscles [5,6]leads to speculate that dental occlusion may affect the whole body.The neuronal links of the trigeminal nerve to the vestibular nuclei,which are responsible of the masticatory function and equilibrium control respectively [7,8],reinforce the argument/10.1016/j.neulet.2016.02.0030304-3940/©2016Elsevier Ireland Ltd.All rights reserved.S.Julià-Sánchez et al./Neuroscience Letters617(2016)116–121117for this relationship.Most literature in the topic have evaluated the influence of proprioceptive information of dental occlusion on the body balance in stable conditions reporting contrasting con-clusions in favor[9–11]or against[12–14].However,less research has focused in assessing the relationship between dental occlusion and balance in unstable conditions,even though unstable platforms are more sensitive[15].Moreover,a different contribution of the afferent signals for the process of balance control occurs depending on the stability of the support base[16],thus evidencing a higher contribution of other sources of sensory information when more difficult conditions for the balance control are present.To data, there is no available literature investigating the influence of den-tal occlusion in fatigue conditions at stable and unstable support surface conditions.Therefore,we hypothesized that dental occlusion may con-tribute differently on the body balance control depending on the stability condition(stable versus unstable)and that influence might be more evident in fatigue conditions due to reorganization of the sensory information sources.Then,the aim of the present study was to determine whether:(i)dental occlusion influences body balance for two extreme levels of stability(stable/unstable),and (ii)the influence of dental occlusion on the balance control comes strongly into effect under fatigue conditions.2.Material and methods2.1.SubjectsTen healthy and physically active male subjects(age, 33.62±4.07year;height, 1.77±0.05m;body mass, 74.38±6.86kg;body mass index,23.75±2.17kg/m2),participated in the study.None of the subjects presented any history of musculoskeletal problems or vestibular impairment.Exclusion criteria were:regu-lar medication,smoking and drinking habits,temporomandibular disorders and pathophysiological factors affecting normal body bal-ance capacity.Subjects were advised to avoid excitant substances (e.g.,caffeine,chocolate...)and strenuous physical activity for72h before the test.All the participants gave their written informed consent according to the updated Declaration of Helsinki and the project protocol was approved by the university’s ethics review board.2.2.Testing apparatusA body balance platform model Balance System SD(Biodex,NY, USA)was used to measure postural control(Fig.1).The Biodex body balance system(BBS)has been widely used for rehabilitation within stability exercise programs[17]and its reliability and applications for clinical testing are well documented[18].The BBS consists in a circular movable platform that provides up to20◦of surface tilt in a360◦arc of motion.Rather than measuring the deviation of COP during static conditions,this device measures the degree of tilt about each axis during dynamic conditions.The amount of stiffness in the platform is controlled mechanically and ranges from stability level8(stiffest)to stability level1(loosest), allowing the examiner to objectively measure the ability of a sub-ject to maintain postural stance under both static and dynamic conditions.An LCD screen provides subjects with visual feedback on the situation of their center of mass in relation to the periphery of the platform[18].The platform provides,as a quantitative data,an overall Stability Index(SI)that represents the variance of foot platform displace-ment in degrees,from a level platform position,in all motions during a test.The SI takes into account the displacement fromlevel Fig.1.BBS platform.This device challenges the individual to maintain balance of the subjects while standing on a moveable platform that tilts a maximum of20◦(from the horizontal plane)in all directions.in the following directions:Anterior/Posterior(A/P)-Sagittal Plane, and Medial/Lateral(M/L)-Frontal Plane;and it is calculated using the following equation,where x represents the M/L plane and y the A/P plane:SI=(0−X)2+(0−Y)2numberofsamplesA high number is indicative of a lot of movement during a test, thus it is associated with poor balance capacity,whereas a low SI indicates little body movement and it is associated with a more stable posture during testing[18].2.3.Testing procedureSubjects reported to the laboratory on three days separated by 72h.Thefirst day was a familiarization session,while the other two were the experimental sessions(Fig.2).The tests were carried out for two dental occlusion conditions: (i)dental contact,setting dental occlusion in Intercuspal Position (ICP)by asking the subject to clench his/her teeth;and(ii)without dental contact,“Cotton Rolls”mandibular position(CR)by using cotton rolls(8mm thick)between the two dental arches placed from the canines to the molars.The testing protocol for each session consisted of two consecutive trials—one for each dental occlusion condition,at random order—with30s of duration each one[19] and afive minutes in between.All measurements were performed with subjects standing barefoot,with their arms unfolded by their sides,shoulders relaxed,and looking at a reference point to eye level placed at one meter distance.The eye-visual target distance was chosen to minimize the retinal shifts of the visual image[20].118S.Julià-Sánchez et al./Neuroscience Letters617(2016)116–121Fig2.Testing procedure scheme for the three days of the study.1st day(familiar-ization session),2nd day(experimental session1),3rd day(experimental session 2).For each trial,subjects were randomly assigned to the dental occlusal condition: CR(Cotton Rolls);ICP(Intercuspal Position).No verbal feedback was given during the testing and the control screen was covered during testing procedures in order to avoid visual feedback.Both dental occlusion conditions were tested on an unstable condition by selecting level2(L2),and on a stable condition by selecting level8(L8)from the eight levels provided by the plat-form,according to the protocol used in previous research[3,19].To avoid repeated measures and potential fatigue masking,the differ-ent stability conditions were tested on two days separated by72h. So that L2was evaluated on thefirst experimental session(S1)and L8was evaluated on the second experimental session(S2).For each experimental session,afirst individual measurement of balance was made at rest.After that,all subjects performed the same exercise protocol aimed to induce lower limbs muscle fatigue.The exercise protocol consisted of six sets offifteen seconds stretch-shortening cycles(SSC)jumping according to Bosco pro-tocol[21]with a three-minute recovery time between successive sets.The exercise was performed on a force platform to evaluate the mechanical power decay along the sets of the exercise.The relia-bility and validity of force platforms to measure force and power output during SSC is well documented[22].A second measurement of balance was then made at fatigue con-dition.Measurements were obtained immediately with no more than10min afterfinishing the exercise,as the effect of fatigue remains present until13min after the exercisefinishes[23].Heart rate was monitored during the exercise with a POLAR RS800CX(POLAR,Kempele,Finland).Blood capillary samples were collected from afinger tip three minutes after the exercise to measure blood lactate concentration(Biosen C-Line analyser,EKF, Barleben,Germany)in order to check the anaerobic character of the exercise.Furthermore,a modified Borg Fatigue Scale,as a sen-sitive method to evaluate fatigue,was used to measure perceived exertion of the subjects after the execution of the exercise.2.4.Statistical analysisTwo-way repeated measures analysis of variance(ANOVA)with Holm-Sidak correction was carried out to determine the effect of the exercise and the dental occlusion on the balance control and to compare the output mechanical power along the sets on the two experimental sessions.Ad hoc paired t-test by groups was used to contrast the differences on heart rate,lactate and effort-perception on both sessions.All values are expressed as mean±SD.A P value <0.05was accepted as the significance level.Statistical analysis was carried out using SigmaPlot version13(SYSTAT Software Inc.,San Jose,CA,USA).3.Results3.1.Stability index and exerciseOverall,the effect of the exercise on the balance control was statistically significant for the level2(p=0.02)and the level8 (p=0.04).The CR condition did not show an impairment of the stability index after the exercise protocol neither for the level2(p=0.07)nor for the level8(p=0.13).While it was detected a statistically signif-icant difference for pre vs post measurements within ICP condition for both level2(p=0.004)and level8(p=0.03)(Table1,Fig.3). 3.2.Stability index and dental occlusionOverall,the mandibular position,disregarding fatigue condition, influenced statistically in the balance control showing a better bal-ance for the CR condition in comparison with ICP for the level2 (p=0.003)and the level8(p=0.048).The detailed analysis of the effect of the mandibular position on the balance control at rest showed statistically significant dif-ferences between CR and ICP for the level2(CR=3.95±1.52vs ICP=4,82±2.0;p=0.03)but not for the level8(CR=2.07±0.52vs ICP=2.36±0.55;p=0.06).Whereas for post-exercise values,bal-ance control was significantly better when dental occlusion was set in CR for both level2(CR=5.10±2.73vs ICP=6.94±3.49;p<0.001) and level8(CR=2.16±0.53vs ICP=2.49±0.58;p=0.04)(Table1, Fig.3).S.Julià-Sánchez et al./Neuroscience Letters617(2016)116–121119Fig.3.Stability index(degrees)for L2and L8when comparing dental occlusion condition in Cotton Rolls(CR)and Intercuspal Position(ICP)for pre-and post-exercise measurements.Values are represented as Mean±SE(n=10).Black bars indicate CR,grey bars indicate ICP condition.*p<0.05;**p<0.005;***p<0.001,NS:non-significant differences.Table1Values of Stabilty Index(Mean±SD)for the two experimental conditions(ICP vs CR)at the two levels of instability measured in the balance platform(L2vs L8).L2L8ICP CR ICP CRPRE 4.82±2.0 3.95±1.5* 2.36±0.6 2.07±0.5NS POST 6.94±3.5 5.10±2.7** 2.49±0.6 2.16±0.5*p-Value(PRE vs POST)0.0040.070.030.13Signs express statistical differences when comparing ICP vs CR conditions for each level tested according to the following schema:NS non significant differences;*p<0.05; **p<0.001.Table2Heart rate,blood lactate,and modified Borg Fatigue Scale values(Mean±SD)for S1(experimental session1)and S2(experimental session2).PRE:before;POST:after the exercise.***p≤0.001for Pre vs Post comparison.NS:non-significant differences for Post S1vs Post S2comparison.S1S2PRE POST PRE POSTHeart rate(bpm)79.8±11.3***144±10.678.5±13.9***143±10.0NS Lactate(mmol/L)–7.7±4.0–7.9±3.0NS Borg Fatigue Scale–8.3±1.4–8.4±2.1NS3.3.Exercise-related measurementsHeart rate,blood lactate,and modified Borg Fatigue Scale are shown in Table2.Heart rate was significantly increased after the exercise for both S1and S2(p<0.001),although not show-ing statistically significant differences among the two experimental sessions neither after nor before the tests.As expected,after the SSC exercise,subjects reached high blood lactate levels although no statistically significant differences were noted among the two post-test conditions.Likewise,values obtained from the modified Borg Fatigue Scale did not show statistically significant differences among the two post-test conditions.The mean of the mechanical power along the six sets of SSC was3187.06±664.745W for S1,while a mean power of 3285.46±745.42W was registered for S2.No statistically signifi-cant difference was found between the mean mechanical power for S1vs S2(p=0.17).Similarly,the decay of mechanical power along the sets for each exercise was not statistically significant neither for S1(p=0.42)nor for S2(p=0.50)(Table3).4.DiscussionThe present study compared the body balance of physically active subjects on unstable platform under opposing dental occlu-sion(ICP/CR)and fatigue(pre-/post-exercise)conditions for two extreme levels of stability(stable/unstable).Measures of the body balance were obtained before and after exhausting lower-limb maximal exercise.The mainfindings were that:(i)the body bal-Table3Values of mechanical power(W)(Mean±SD)along the sets for S1(experimental session1)and S2(experimental session2).N:sample size;S1–S6:sets of SSC.N S1S2S1103228.12±704.063306.72±735.75S2103160.89±665.633210.77±797.68S3103253.89±758.233297.39±778.58S4103189.34±705.713310.67±802.85S5103147.14±652.863326.25±807.38S6103142.98±719.133260.97±800.11120S.Julià-Sánchez et al./Neuroscience Letters617(2016)116–121ance was significantly better when dental occlusion was set in CR; and(ii)the influence of dental occlusion on the balance control came strongly into effect under fatigue conditions.Body balance was affected by the exercise-induced fatigue at both levels of stability tested when comparing the pre-and post-exercise conditions.Previous research has attributed the impairment of body balance after the exercise to an alteration of muscles effectors and proprioception[24].In our study,although fatigue induced impairment in the balance control at both levels tested,the effect of the exercise was further exacerbate at unstable level(L2p=0.02;L8p=0.04).However,we can consider that the level of fatigue reached by the subjects after the exercise was sim-ilar for both experimental sessions,as lactate values,perception of effort reported and mechanical power output were not statis-tically significant between S1and S2.Thus,the magnitude of the impairment on the body balance after the exercise might be mainly attributable to the surface stability condition.Our results agree with Dickin and Doan[25]who reported that muscular fatigue caused an impairment in postural control,which was increased by external postural perturbations.A remarkablefinding of the present study was that dental occlu-sion significantly influenced the balance control of the subjects. However,the influence of dental occlusion on the stability index was different in the two extreme levels of stability tested.Thus,at stable level(L8),the dental occlusion only influenced stability of the subjects for the measurements at fatigue condition(p=0.04);while at the unstable level(L2),differences of balance control between ICP and CR reached significance at both rest(p=0.03)and fatigue (p<0.001)conditions.Thisfinding agrees with previous research reporting that dental occlusion impaired body balance(at rest) in unstable but not in stable conditions[3,26]and contributes to provide more clarity to the lack of scientific agreement in the rela-tionship between dental occlusion and the body balance control which might be influenced by the support surface condition.An interestingfinding in our study was that measurements of balance made in CR were not statistically significant affected by the exercise neither at unstable level2(SI pre:3.95±1.52;SI post: 5.10±2.73,p=0.07)nor at stable level8(SI pre:2.07±0.55;SI post: 2.16±0.53,p=0.13).Whereas an impairment in the balance con-trol was detected after the exercise for the ICP condition at both level2(SI pre:4.82±2.0;SI post:6.94±3.50,p=0.004)and level 8(SI pre:2.36±0.55;SI post:2.49±0.58,p=0.03).It is important to note that balance control registered in CR after the exercise was similar to measurements of balance control obtained in ICP before the exercise at L2or even better at L8.Thus,even in fatigue con-ditions,we can assume that setting dental occlusion in CR allows a better balance control of the subjects,reinforcing the influence of dental occlusion in the balance control.On similar lines,previ-ous research have reported improvements in the neuromuscular coordination[27]and propioception[28]depending on the dental occlusion condition.5.ConclusionsOur mainfindings were that:(i)the body balance was sig-nificantly better when dental occlusion was set in CR,and more especially,at unstable level measurements;and(ii)the influence of dental occlusion on the balance control came strongly into effect under fatigue conditions.These results lead to speculate that the afferent signals from dental occlusion may contribute most effectively in the process of balance control when more external perturbations are present,in this case surface instability and muscle fatigue.Conflict of interestThe authors have no conflicts of interest orfinancial ties to dis-close.AcknowledgementsThe authors are grateful to all the volunteers participating in the study for their hard commitment and enthusiasm.References[1]S.R.Lord,D.L.Sturnieks,The physiology of falling:assessment and preventionstrategies for older people,J.Sci.Med.Sport8(2005)35–42.[2]E.A.Solovykh,O.G.Bugrovetskaya,L.N.Maksimovskaya,Information value offunctional status of the stomatognathic system for postural balanceregulation,Bull.Exp.Biol.Med.153(2012)401–405.[3]S.Julià-Sánchez,J.Álvarez-Herms,H.Gatterer,M.Burtscher,T.Pagès,G.Viscor,Dental occlusion influences the standing balance on an unstableplatform,Motor Control19(2015)341–354.[4]R.W.Pallegama,A.W.Ranasinghe,V.S.Weerasinghe,M.A.Sitheeque,Influence of masticatory muscle pain on electromyographic activities ofcervical muscles in patients with myogenous temporomandibular disorders,J.Oral Rehabil.31(2004)423–429,/10.1111/j.1365-2842.2004.01266.x.[5]M.Bergamini,F.Pierleoni,A.Gizdulich,C.Bergamini,Dental occlusion andbody posture:a surface EMG study,Cranio26(2008)25–32.[6]C.Sforza,G.M.Tartaglia,U.Solimene,V.Morgun,R.R.Kaspranskiy,V.F.Ferrario,Occlusion,sternocleidomastoid muscle activity,and body sway:apilot study in male astronauts,Cranio24(2006)43–49.[7]L.Devoize,S.Domejean,C.Melin,P.Raboisson,A.Artola,R.Dallel,Organization of projections from the spinal trigeminal subnucleus oralis to the spinal cord in the rat:a neuroanatomical substrate for reciprocalorofacial-cervical interactions,Brain Res.1343(2010)75–82,http://dx.doi.org/10.1016/j.brainres.2010.04.076.[8]G.Pinganaud,F.Bourcier,C.Buisseret-Delmas,P.Buisseret,Primarytrigeminal afferents to the vestibular nuclei in the rat:existence of a collateral projection to the vestibulo-cerebellum,Neurosci.Lett.264(1999)133–136. [9]P.Bracco,A.Deregibus,R.Piscetta,Effects of different jaw relations onpostural stability in human subjects,Neurosci.Lett.356(2004)228–230,/10.1016/j.neulet.2003.11.055.[10]K.Sakaguchi,N.R.Mehta,E.F.Abdallah,A.G.Forgione,H.Hirayama,T.Kawasaki,et al.,Examination of the relationship between mandibularposition and body posture,Cranio25(2007)237–249.[11]A.Cuccia,C.Caradonna,The relationship between the stomatognathic systemand body posture,Clinics(Sao Paulo)64(2009)61–66.[12]D.Manfredini,T.Castroflorio,G.Perinetti,L.Guarda-Nardini,Dentalocclusion,body posture and temporomandibular disorders:where we arenow and where we are heading for,J.Oral Rehabil.39(2012)463–471,http:// /10.1111/j.1365-2842.2012.02291.x.[13]G.Perinetti,J.Primozic,D.Manfredini,R.Di Lenarda,L.Contardo,Thediagnostic potential of static body-sway recording in orthodontics:asystematic review,Eur.J.Orthod.35(2013)696–705,/10.1093/ejo/cjs085.[14]A.Baldini,A.Nota,D.Tripodi,S.Longoni,P.Cozza,Evaluation of thecorrelation between dental occlusion and posture using a force platform,Clinics(Sao Paulo)68(2013)45–49.[15]R.W.Baloh,T.D.Fife,L.Zwerling,T.Socotch,K.Jacobson,T.Bell,et al.,Comparison of static and dynamic posturography in young and older normal people,J.Am.Geriatr.Soc.42(1994)405–412.[16]R.J.Peterka,Sensorimotor integration in human postural control,J.Neurophysiol.88(2002)1097–1118.[17]B.Akhbari,I.Ebrahimi Takamjani,M.Salavati,M.Ali Sanjari,A4-week biodexstability exercise program improved ankle musculature onset,peak latency and balance measures in functionally unstable ankles,Phys.Ther.Sport8(2007)117–129,/10.1016/j.ptsp.2007.03.004.[18]M.R.Hinman,Factors affecting reliability of the biodex balance system:asummary of four studies,J.Sport Rehabil.9(2000)240–252.[19]B.L.Arnold,R.J.Schmitz,Examination of balance measures produced by thebiodex stability system,J.Athl.Train.33(1998)323–327.[20]N.Vuillerme,C.Burdet,B.Isableu,S.Demetz,The magnitude of the effect ofcalf muscles fatigue on postural control during bipedal quiet standing with vision depends on the eye-visual target distance,Gait Posture24(2006)169–172,/10.1016/j.gaitpost.2005.07.011.[21]C.Bosco,P.Luhtanen,P.V.Komi,A simple method for measurement ofmechanical power in jumping,Eur.J.Appl.Physiol.Occup.Physiol.50(1983) 273–282.[22]N.Hori,R.U.Newton,N.Kawamori,M.R.McGuigan,W.J.Kraemer,K.Nosaka,Reliability of performance measurements derived from ground reaction force data during countermovement jump and the influence of sampling frequency, J.Strength Cond.Res.23(2009)874–882,/10.1519/JSC.0b013e3181a00ca2.S.Julià-Sánchez et al./Neuroscience Letters617(2016)116–121121[23]Z.G.Fox,J.P.Mihalik,J.T.Blackburn,C.L.Battaglini,K.M.Guskiewicz,Return ofpostural control to baseline after anaerobic and aerobic exercise protocols,J.Athl.Train.43(2008)456–463,/10.4085/1062-6050-43.5.456.[24]N.Vuillerme,F.Hintzy,Effects of a200W-15min cycling exercise on posturalcontrol during quiet standing in healthy young adults,Eur.J.Appl.Physiol.100(2007)169–175,/10.1007/s00421-007-0419-6.[25]D.C.Dickin,J.B.Doan,Postural stability in altered and unaltered sensoryenvironments following fatiguing exercise of lower extremity joints,Scand.J.Med.Sci.Sports18(2008)765–772,/10.1111/j.1600-0838.2007.00760.x.[26]C.Tardieu,M.Dumitrescu,A.Giraudeau,J.L.Blanc,F.Cheynet,L.Borel,Dentalocclusion and postural control in adults,Neurosci.Lett.450(2009)221–224, /10.1016/j.neulet.2008.12.005.[27]V.D’Ermes,M.Basile,A.Rampello,C.Di Paolo,Influence of occlusal splint oncompetitive athletes performances,Ann.Stomatol.(Roma)3(2012)113–118.[28]P.Gangloff,J.P.Louis,P.P.Perrin,Dental occlusion modifies gaze and posturestabilization in human subjects,Neurosci.Lett.293(2000)203–206.。