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www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Temporomandibular

disorder:

otologic

implications

and

its

relationship

to

sleep

bruxism

Bruno

Gama

Magalhães

a

,

Jaciel

Leandro

de

Melo

Freitas

b

,

André

Cavalcanti

da

Silva

Barbosa

a

,

Maria

Cecília

Scheidegger

Neves

Gueiros

a

,

Simone

Guimarães

Farias

Gomes

a

,

Aronita

Rosenblatt

c

,

Arnaldo

de

Franc

¸a

Caldas

Júnior

c,

aUniversidadeFederaldePernambuco(UFPE),ProgramadePós-graduac¸ãoemOdontologia,Recife,PE,Brazil bUniversidadeFederaldePernambuco(UFPE),Odontologia,Recife,PE,Brazil

cUniversidadeFederaldePernambuco(UFPE),Recife,PE,Brazil

Received9June2016;accepted22July2017 Availableonline23August2017

KEYWORDS Bruxism; Temporomandibular disorders; Otologicsymptoms Abstract

Introduction:Temporomandibulardisorderisanumbrellatermfor various clinicalproblems affectingthemusclesofmastication,temporomandibularjointandassociatedstructures.This disorderhasamultifactoretiology,withoralparafunctionalhabitsconsideredanimportant co-factor.Amongsuchhabits,sleepbruxismisconsideredacausalagentinvolvedintheinitiation and/orperpetuationoftemporomandibulardisorder.Thatconditioncanresultinpainotologic symptoms.

Objective:Theaimofthepresentstudywastoinvestigatetherelationshipbetween temporo-mandibulardisorderandbothotologicsymptomsandbruxism.

Methods:Atotalof776individualsaged15yearsorolderfromurbanareasinthecityofRecife (Brazil)registeredatFamilyHealthUnitswereexamined.Thediagnosisoftemporomandibular disorderwasdeterminedusingAxisIoftheResearchDiagnosticCriteriafortemporomandibular disorders,addressingquestionsconcerningmyofascialpainandjointproblems(disk displace-ment,arthralgia,osteoarthritisandosteoarthrosis).Fourexaminershadpreviouslyundergone trainingandcalibrationexercisesfortheadministrationoftheinstrument.Intra-examinerand inter-examineragreementwasdeterminedusingtheKappastatistic.Individualswitha diag-nosisofatleastoneoftheseconditionswereclassifiedashavingtemporomandibulardisorder. Thediagnosisofotologicsymptomsandbruxismwasdefinedusingthesameinstrumentanda clinicalexam.

Pleasecitethisarticleas:MagalhãesBG,FreitasJL,BarbosaAC,GueirosMC,GomesSG,RosenblattA,etal.Temporomandibulardisorder:

otologicimplicationsanditsrelationshiptosleepbruxism.BrazJOtorhinolaryngol.2018;84:614---19.

Correspondingauthor.

E-mail:arnaldo.caldas@ufpe.br(A.F.CaldasJúnior).

PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial. https://doi.org/10.1016/j.bjorl.2017.07.010

1808-8694/©2017Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).

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Results:Amongtheindividualswithtemporomandibulardisorder,58.2%hadatleastone oto-logic symptom and 52% exhibited bruxism. Statistically significant associations were found betweenthedisorderandbothotologicsymptomsandbruxism(p<0.01forbothconditions; OR=2.12and2.3respectively).Otologicsymptomsandbruxismmaintainedstatistical signif-icanceinthebinarylogisticregressionanalysis,whichdemonstrateda1.7foldandtwofold greaterchanceofsuchindividualshavetemporomandibulardisorder,respectively.

Conclusion: Thelogisticregressionanalysisdemonstratedstrongassociationsbetweenthe dis-orderandbothotologicsymptomsandbruxismwhenanalyzedsimultaneously,independently ofpatientageandgender.

© 2017 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Published by Elsevier Editora Ltda. This is an open access article under the CC BY license (http://

creativecommons.org/licenses/by/4.0/).

PALAVRAS-CHAVE

Bruxismo;

Disfunc¸ões temporo-mandibulares; Sintomasotológicos

Disfunc¸ãotemporomandibular:implicac¸õesotológicasesuarelac¸ãocomobruxismo dosono

Resumo

Introduc¸ão: ADisfunc¸ãoTemporomandibularéumtermoqueenglobaváriosproblemas clíni-cos queafetam os músculosda mastigac¸ão,a articulac¸ão temporomandibular e estruturas associadas.Este distúrbiotem umaetiologiamultifatorial,comhábitos parafuncionaisorais considerados umimportantecofator.Entreesseshábitos,obruxismodosonoéconsiderado um agentecausadorenvolvido nodesenvolvimentoe/ouperpetuac¸ãodedisfunc¸ão temporo-mandibular.Esseproblemapoderesultaremsintomasotológicosdolorosos.

Objetivo: Investigararelac¸ãoentredisfunc¸ãotemporomandibulareossintomasotológicose bruxismo.

Método: Foramexaminados 776indivíduos comidade igual ou superior a15 anosde áreas urbanasdacidadedeRecife(Brasil)registradosnasUnidadesdeSaúdedaFamília.Odiagnóstico dadisfunc¸ãofoideterminadoutilizandooEixoIdosCritériosdeDiagnósticodePesquisapara DistúrbiosTemporomandibulares,abordandoquestõesrelativasadormiofascialeproblemas articulares(luxac¸ãodiscal,artralgia,osteoartriteeosteoartrose).Quatroexaminadoresforam treinados para a administrac¸ão do instrumento. A concordância intraexaminador e intere-xaminadorfoideterminadausandoaestatísticaKappa.Osindivíduoscomdiagnósticodepelo menosumadessascondic¸õesforamclassificadoscomotendodisfunc¸ãotemporomandibular.O diagnósticodesintomasotológicosebruxismofoidefinidoutilizandoomesmoinstrumentode diagnósticoeexameclínico.

Resultados: Entreosindivíduoscomadisfunc¸ão,58,2%apresentarampelomenosumsintoma otológicoe52%apresentarambruxismo.Foramencontradasassociac¸õesestatisticamente sig-nificativasentreadisfunc¸ãotemporomandibulareambosossintomasotológicosebruxismo(p <0,01paraambososproblemas,OR=2,12e2,3,respectivamente).Ossintomasotológicose obruxismomantiveramsignificânciaestatísticanaanálisederegressãologísticabinária,oque demonstrouumaprobabilidadede1,7e2vezesmaiorchancedequeessesindivíduostenham disfunc¸ãotemporomandibular,respectivamente.

Conclusão:A análise de regressão logística demonstrou associac¸ões fortes entre disfunc¸ão temporomandibular e sintomas otológicos e bruxismo quandoanalisados simultaneamente, independentementedaidadeesexodopaciente.

© 2017 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Publicado por Elsevier Editora Ltda. Este ´e um artigo Open Access sob uma licenc¸a CC BY (http://

creativecommons.org/licenses/by/4.0/).

Introduction

Temporomandibulardisorder(TMD)isanumbrellatermfor various clinical problems affecting the muscles of mas-tication, temporomandibular joint (TMJ) and associated structures.1This disorderhasamultifactoretiology,2with oral parafunctional habits considered an important co-factor.3 Among suchhabits, sleepbruxism is considered a causalagentinvolvedintheinitiationand/orperpetuation

of TMD.4 Bruxism is the act of grinding or clenching the teethin aparafunctional or unconscious manner.Bruxism causeshyperactivity of themuscles ofmastication due to non-functionalmandibularmovements,whichcanresultin painsymptoms andistherefore animportantcontributing factortochangesintheTMJ.5

TheclinicalsymptomsofTMDincludeclickingor crack-lingsounds in the TMJ, difficultyopening and closing the mouthandpain,thelatterofwhichcanspreadtodifferent

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regionsofthehead,includingthepre-auricularand auric-ular regions.5 A number of studies have suggested an association between otologic symptoms and TMD.6---8 The symptoms most frequently reported in the literature are ringingintheears,otalgia,asensationofearfullness,lossof hearinganddizziness.1,6,7Theassociationofthesesymptoms withTMDisthoughttobe multi-causal,due toanatomic, neurologicandemotionalrelationships.9

Inthis context,thereisalikelyhypothesis that hyper-activity of the muscles of mastication may contract the tensor tympani muscle and tympanic membrane, which wouldresultinauditorytubedysfunction,withsymptomsof asensationofearfullness,lossofbalanceandhearingloss.2 Duetothescarcityofstudies intheliterature,theaimof thepresentstudywastoinvestigatetheassociationbetween TMDandbothotologicsymptomsandsleepbruxism.

Methods

Across-sectionalstudywasconductedwithasampleof776 individualsaged15yearsor older fromurbanareas regis-teredatFamilyHealthUnits.Norestrictionswereimposed regardinggenderorethnicity.Agewascategorizedbasedon anadaptationofthecriteriaoftheWorldHealth Organiza-tion:15---18,19---24,25---44,45---59and60yearsorolder.10

Multi-stagesamplingwasusedtodeterminethesample sizeandobtainarepresentativesampleoftheentire city. First,systematicsamplingwasemployedtodefinethe neigh-borhoodsinthehealthdistrictsthatwouldtakepartinthe study.Systematicsamplingwasthenperformedtoselectthe Primary HealthUnits, fromwhich 776 volunteers at their respectivehealthunitswererandomlyselected.

Thewholeprojectincludingthebothinformedconsent received approval from the Human Research Ethics Com-mittee (n◦ 05650512.9.0000.5208). All participants signed astatementofinformedconsentandthosediagnosedwith TMDwerereferredtoareferencecenterfortreatment.For thoseunder18yearsof age, an informed consentto per-formtheexaminationscamefromtheparentsorguardians properlysigned. This researchhas been conductedin full accordancewiththeWorldMedicalAssociationDeclaration ofHelsinki.11

The diagnosis of TMD was determined using Axis I of the Research Diagnostic Criteria for temporomandibu-lar disorders (RDC/TMD),addressing questions concerning myofascial pain and joint problems (disk displacement, arthralgia,osteoarthritis and osteoarthrosis).The diagno-sis of myofascial pain is based on the report of pain in thetemples,Jaw,face,preauricularareaorinsidetheear atrest orduring function.Painreportedbytheindividual inresponse topalpation ofthree or moremuscle groups. Thereisalsothepresenceofmuscularpainwithorwithout limitationof oralopening. Disk displacement isdiagnosed by opening, closing, lateral excursion, or protruding Jaw movements; reciprocal clicks on the TMJ (disk displace-mentwithreduction),openinglimitation(diskdisplacement withoutreduction),ordiskdisplacementswithoutreduction andwithout signsof limitingmouth opening. Arthralgiais detectedthroughthepresenceof oneormorepain symp-tomsinthejointregion,paininthejointduringthemaximal opening without aid, painin thejoint duringthe opening

withaid,paininthejointduringthelateralexcursionifgross crackling. TMJ osteoarthritis when arthralgia and coarse cracklingandTMJosteoarthrosiswereobservedwhenthere was no evidence of arthralgia and with coarse crackling (Manfredinieixo1).12Individualswithadiagnosisofatleast oneoftheseconditionswereclassifiedashavingTMD.Four examinershadpreviouslyundergonetrainingandcalibration exercises for the administration of the RDC/TMD. Intra-examiner and inter-examiner agreement was determined usingtheKappastatistic(K=0.90and0.82,respectively).

Thepresenceofotologicsymptomswasconsideredwhen at least one of the following was present: tinnitus, otal-gia, ear fullness, dizziness and hearing loss, which were alldiagnosedbypatients’report.Sleepbruxismwas diag-nosed by self-report or report of a family memberabout grindingorclenchingduringsleepusingRDC/TMD(AxisII). Axis II consists of a questionnaire with 31 items, divided intosocio-demographic,socioeconomic,psychological (sub-scalesof depressionandnon-specificphysical symptoms ---painful and non-painful),psychosocial (degree of severity of chronicpain--- intensityof painandrelateddisability); Signs and symptoms related to the patient and the limi-tation scalein mandibularfunction (limitationsrelatedto mandibular functioning).The mean scoreis calculated by summing the score of individual items, allowing patients to be assessed within normal, moderate or severe levels ofdepression,andspecificandnon-specificphysical symp-tom scales. However, for the purpose of this article only relatedrelevantinformationonsleepbruxismandotological symptomswasextracted.13,14

It must be emphasized that all patients with otologic symptomsdidnotknowabout theirdiagnosison temporo-mandibular dysfunction, so they were not on treatment. Furthermore,therearenottreatmentforTMDatthe pub-lichealth centersinthestateofPernambuco.Allpatients properlydiagnosedarereferredtostatedentalcolleges.

Individualswithneurologicaldisorders,thosewitha his-tory of tumor in the head and neck region, those who madecontinuoususeorforatleastthepreviousthreedays ofanti-inflammatoryagents,analgesicorcorticoids,those unabletounderstandorrespondtotheRDC/TMD,thosewho reportedahistoryofrheumaticdisease,thosewithpainof anodontogenicoriginandthosewithaprimaryotalgiawere excluded from the study. This informationwas extracted fromthepatientchartsatthehealthservices.

Forthe statistical analysis, the Statistical Packagefor the SocialSciences (SPSS,version20.0)wasemployedfor thedataentryandstatisticalcalculations.TheShapiro---Wilk was used todetermine the distribution of the data (nor-malor non-normal).Pearson’schi-squaretest wasusedto testassociationsbetweenthedependentandindependent variables.A5%marginoferrorwitha95%significancelevel (p<0.05)wasconsideredforallanalyses.Aregressionmodel wascreatedtoidentifypossibleconfoundingvariablesand explanatoryvariables.

Results

A total of 776 individuals aged 15---85years (mean: 39.88years;median: 39years)participated in thepresent study.The prevalenceof TMDin thesample analyzedwas

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Table1 DistributionofparticipantswithTMDaccordingtootologicsymptomsandbruxism.

Variables TMD

Yesn(%) No n(%) Total(%) Odds(95%CI)

Gender(p=0.029) 1.6(1.04---2.49) Male 243(37) 413(63) 656(100) Female 32(26.7) 88(73.3) 120(100) Age(p=0.32) ---15---18years 10(25.6) 29(74.4) 39(100) 19---24years 29(33.3) 58(66.7) 87(100) 25---44years 132(36.5) 230(63.5) 362(100) 45---59years 87(41) 125(59) 212(100) >59years 17(22.4) 59(77.6) 76(100) Otologicsymptoms(p=0.001) 2.1(1.57---2.87) Yes 160(44.7) 198(55.3) 358(100) No 115(27.5) 303(72.5) 418(100) Sleepbruxism(p=0.001) 2.2(1.70---3.12) Yes 143(47.2) 160(52.8) 303(100) No 132(27.9) 341(72.1) 473(100)

Table2 FinallogisticregressionmodelforTMDaccordingtogender,age,otologicsymptomsandbruxism.

B S.E. Wald df p-value OR 95%CIforOR

Lowerlimit Upperlimit

Gender 0.425 0.229 3.453 1 0.063 1.530 0.977 2.395 Age 0.013 0.082 0.026 1 0.871 1.013 0.863 1.190 Otologicsymptoms 0.556 0.160 12.073 1 0.001 1.744 1.274 2.386 Sleepbruxism 0.702 0.160 19.145 1 0.000 2.018 1.473 2.764 Constant −1.882 0.488 14.862 1 0.000 0.152 Goodnessoffita 0.394

a DeterminedusingHosmer---Lemeshowtest.

35.4%.Amongthe275individualsdiagnosedwithTMD,88.4% werefemale.Theprevalencewasgreaterintheagegroup of45---59years,correspondingto41%of theaffected indi-viduals(Table1).

Among the individuals with TMD, 58.2% had at least one otologic symptom and 52% exhibited sleep bruxism. Pearson’sChi-squaretestdemonstratedstatistically signifi-cantassociationsbetweenTMDandbothotologicsymptoms and sleep bruxism (p<0.01 for both conditions), with an oddsratioof2.12forotologicsymptomsand2.3forsleep bruxism.

Binarylogisticregressionanalysiswasperformedto eval-uatethebehaviorofthecovariablessimultaneouslywiththe outcome(TMD).Otologicsymptomsandsleepbruxism main-tainedstatisticalsignificance,demonstratinga1.7foldand twofoldgreaterchanceofsuchindividualsdevelopingTMD, respectively(Table2).

Discussion

Theaimofthepresentstudywastoinvestigate comorbidi-tiesthatmaybeassociatedwithTMD.Theliteraturereports

associations between this disorder and parafunctional habits.15,16 Thestudiescitedindicatedthatparafunctional habitscanaltertheharmonyofthestomatognathicsystem andarethereforeconsideredasignificantelementinthe eti-ologyandprogressionofmuscleandTMJdisorders.Among suchhabits,thepresentstudyfoundthatsleepbruxismwas associatedwithTMD, whichis in agreement withfindings describedinpreviousstudies.15,16

It is important to note that sleep related movement disorders has also been described in other instruments as in the International Classification of Sleep Disorders (ICSD-3), recognizedas an important clinical text for the diagnosisofsleepdisordersclassifyingsleepdisordersinto six major categories (Insomnia, Sleep Related Breathing Disorders,CentralDisordersofHypersomnolence,Circadian Rhythm Sleep-Wake Disorders, Parasomnias and Sleep Related Movement Disorders). However, the approach of thepresentstudyfocusedontheuseofRDCconsideringits relevanceforepidemiologicalpurposes.17 Bruxismcanlead tomusclehyperactivity,resultinginpaininthemusclesof mastication.Inthepresence ofpainandothersymptoms, thestomatognathicsystem mayperformcompensationsto allowchewing,speakingandswallowingwithefficiencyand

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comfort.However,thiscanhaveanegativeeffectinthelong term; as such compensations are not necessarily healthy andmay contribute tothe progressionof TMD. Moreover, theindiscriminantuseofanalgesicswithoutmedical super-vision, asoften occursin individuals with TMD,can mask symptomsandleadtoanaggravationoftheproblem.18

Theanalysisofthesamplealsoindicatedapositive asso-ciation between otologic symptoms and TMD,which is in agreementwith some reports found in the literature.19,20 Aprevious studyfoundthatsignsofTMDarepredictorsof thedevelopmentofsomeotologicsymptoms,suchasringing intheears.21 However,therelationshipbetween TMDand otologicsymptomshadnotyetbeenfullyclarified. Nonethe-less,thisrelationshiphasbeengroundedonembryological, anatomic and functional relationships in the region that encompassestheTMJ,musclesinnervatedbythetrigeminal nerveandstructuresofthemiddleear.

Among other factors, it has been suggested that mus-clechangesinindividualswithTMD,suchasspasmsinthe lateral pterygoid muscle, cause hypertonia of the tensor tympanimuscle, thereby generating changes in the audi-torytubeandaconsequentreductionintheventilationof themiddle ear.19 Thus, the abnormalactivity of the ten-sortympanimuscle isassociated withotologicsymptoms, suchasa sensationof earfullness,tinnitus,dizzinessand hypo/hyperacusis,withouttheexistenceofanotherillness ofanotologicnature.2

A study conducted by Felício etal.18 suggest that the abnormalsolicitationofthemusclesofmasticationdueto bruxismnotonlycausepain,butcancontributetochangesin theTMJ,therebytriggeringTMD.Moreover,asstatedabove, hyperactivity of the muscles of mastication can result in abnormalactivityofthetensortympanimuscle,leadingto otologicsymptoms.18

It is also important to consider cultural, environmen-talandbiological factorsthatmayplay animportant role inthemaintenanceandprogressionofTMD.22---24 Agreater prevalence rate of TMD was found among females in the presentstudy.AccordingtoPovedaRodaetal.,TMDisfour timesmorefrequentinwomen,whoalsotendtoseek treat-mentthreetimesmorethanmen.25Studieshavesuggested thatestrogenreceptorsmodulatemetabolicfunctionswith regardtotherelaxationofligaments,whichmaycontribute tothe progressionof TMD.25 Inthis context, it shouldbe stressedthat themost affected agegroup corresponds to important hormonal changes, such as menopause, which suggestsparticipation in this process, according to previ-ous studies.26,27 However, both gender and age lost their statistical significance in the logistic regression analysis, whichdemonstratedstrongassociationsbetween TMDand bothotologic symptomsandsleepbruxism whenanalyzed simultaneously,independentlyoftheageandgenderofthe patients. Thus, it is important to considerthe TMD-sleep bruxism-otologicsymptoms triadin clinicaland epidemio-logicaldiagnosticsystemssothatpatientscanbecorrectly diagnosedandtreated.

Conclusion

Thelogisticregressionanalysisdemonstratedstrong associa-tionsbetweenTMDandbothotologicsymptomsandbruxism

whenanalyzedsimultaneously,independentlyofpatientage andgender.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

The authors would like to thank to Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior (CAPES) of theBrazilianMinistryofEducationfortheresearchfunding.

References

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25.Poveda Roda R, Bagan JV, Díaz Fernández JM, Hernández BazánS,JiménezSorianoY.Reviewoftemporomandibularjoint pathology.PartI:Classification,epidemiologyandriskfactors. MedOralPatolOralCirBucal.2007;12:E292---8.

26.ManfrediniD,PiccottiF,Ferronato G, Guarda-Nardini L. Age peaksofdifferentRDC/TMDdiagnosesinapatientpopulation. JDent.2010;38:392---9.

27.Magalhães BG, de-Sousa ST, de Mello VV, da-Silva-Barbosa AC, de-Assis-Morais MP, Barbosa-Vasconcelos MM, et al. Risk factorsfortemporomandibulardisorder:binarylogistic regres-sion analysis. Med Oral Patol Oral Cir Bucal. 2014;19: e232---6.

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