www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
Behavioural
and
objective
vestibular
assessment
in
persons
with
osteoporosis
and
osteopenia:
a
preliminary
investigation
夽
Aditi
Gargeshwari,
Raghav
Hira
Jha
∗,
Niraj
Kumar
Singh,
Prawin
Kumar
AllIndiaInstituteofSpeechandHearing,DepartmentofAudiology,Manasagangothri,Karnataka,India
Received10April2017;accepted26August2017 Availableonline21September2017
KEYWORDS Osteoporosis; Osteopenia;
Bonemineraldensity; cVEMP;
oVEMP;
Balanceassessment
Abstract
Introduction:Calciumisvitalforthefunctioningoftheinnerearhaircellsaswellasforthe neurotransmitterreleasethattriggersthegenerationofanerveimpulse.Areductionincalcium levelcouldthereforeimpair theperiphericvestibularfunctioning.However,theoutcomeof balanceassessmenthasrarelybeenexploredincaseswithosteopeniaandosteoporosis,the medicalconditionsassociatedwithreductionincalciumlevels.
Objective:Thepresentstudyaimedtoinvestigatetheimpactofosteopeniaandosteoporosis ontheoutcomesofbehaviouralandobjectivevestibularassessmenttests.
Methods:Thestudyincluded12individualseachinthehealthycontrolgroupandosteopenia group,and11 individualswere includedintheosteoporosisgroup.Thegroupsweredivided basedonthefindingsofbonemineraldensity.Alltheparticipantsunderwentbehaviouraltests (Fukudastepping,tandemgaitandsubjectivevisualvertical)andobjectiveassessmentusing cervicalandocularvestibularevokedmyogenicpotentials.
Results:Asignificantlyhigherproportionoftheindividualsinthetwoclinicalgroups’ demon-stratedabnormalresultsonthebehaviouralbalanceassessmenttests(p<0.05)thanthecontrol group.However,therewasnosignificantdifferenceinlatenciesoramplitudeofcervical vesti-bularevokedmyogenicpotentialandoVEMPbetweenthegroups.Theproportionofindividuals withabsence ofocular vestibular evokedmyogenicpotentialwas significantlyhigherinthe osteoporosisgroupthantheothertwogroups(p<0.05).
Conclusion:Thefindingsofthepresentstudyconfirmthepresenceofbalance-relateddeficits inindividualswithosteopeniaandosteoporosis.Hencetheclinicalevaluationsshouldinclude balanceassessmentasamandatoryaspectoftheoverallaudiologicalassessmentofindividuals withosteopeniaandosteoporosis.
夽 Pleasecitethisarticleas:GargeshwariA,JhaRH,SinghNK,KumarP.Behaviouralandobjectivevestibularassessmentinpersonswith osteoporosisandosteopenia:apreliminaryinvestigation.BrazJOtorhinolaryngol.2018;84:744---53.
∗Correspondingauthor.
E-mail:raghav.jha415@gmail.com(R.H.Jha).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial. https://doi.org/10.1016/j.bjorl.2017.08.013
1808-8694/©2017Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).
© 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 Osteoporose; Osteopenia; Densidademineral óssea; cVEMP; oVEMP; Avaliac¸ãode equilíbrio
Avaliac¸ãocomportamentalevestibularobjetivaemindivíduoscomosteoporosee osteopenia:umainvestigac¸ãopreliminar
Resumo
Introduc¸ão: O cálcio é vital para o funcionamento das células ciliadas, assim como para a liberac¸ão dos neurotransmissores que desencadeiam um impulso nervoso. Uma reduc¸ão nosníveis decálciopoderia,portanto,prejudicarofuncionamentovestibularperiférico.No entanto, aavaliac¸ãodo equilíbriotem sidoraramenteexplorada emcasos deosteopeniae osteoporose,condic¸õesmédicasassociadasàreduc¸ãodosníveisdecálcio.
Objetivo: O presente estudo teve como objetivo investigar o impacto da osteopenia e da osteoporosenosresultadosdostestesdeavaliac¸ãocomportamentalevestibularobjetiva. Método: Oestudoincluiu12indivíduosnosgruposcontroleegrupodeosteopeniae11indivíduos nogrupodaosteoporose.Osgruposforamdivididoscombasenosachadosdadensidademineral óssea.Todososparticipantesforamsubmetidosatestescomportamentais(ProvadosPassosde Fukuda, MarchaemtandemeVerticalVisual Subjetiva)eàavaliac¸ãoobjetivacomousode potenciaisevocadosmiogênicosvestibularescervicaleocular(cVEMPeoVEMP).
Resultados: Uma proporc¸ão significativamente maior de indivíduos nos dois grupos com condic¸õesclínicasmostrouresultadosanormaisnostestesdeavaliac¸ãocomportamentaledo equilíbrio(p<0,05)doqueogrupocontrole.Emboranãotenhahavidodiferenc¸asignificativa naslatênciasounaamplitudedecVEMPeoVEMPentreosgrupos,aproporc¸ãodeindivíduos comausênciadeoVEMPfoisignificativamentemaiornogrupodaosteoporosedoquenosoutros doisgrupos(p<0,05).
Conclusão:Osresultadosdopresenteestudodemonstramapresenc¸adedéficitsdeequilíbrio emindivíduoscomosteopeniaeosteoporose.Assim,asavaliac¸õesclínicasgeraiseaudiológicas deindivíduoscomosteopeniaeosteoporosedeveriamincluiraavaliac¸ãodoequilíbriocomoum aspectoobrigatório.
© 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
Osteoporosis is a medical condition in which the bones becomebrittleandfragileduetolossoftissue,typicallyas aresultofhormonalchanges,deficiencyofcalciumand/or deficiency of vitamin D.1,2 Osteopenia is also a medical
conditioninwhichtheproteinandmineralcontentofbone tissueisreduced,butlessseverelythaninosteoporosis.1,2
Thesetwopathologiesthusrepresentacontinuumalongthe bonemineraldensitymeasure.
Lossofbone mineralisaphenomenonthattakesplace inallhumanbeings.Thisdailyremovalofsmallamountsof bonemineral,aprocesscalledresorption,mustbebalanced byan equal depositionofnewmineral ifbone strengthis tobepreserved.3Whenthisbalancetipstowardsexcessive
resorption,bonesweakenandcanbecomebrittleandprone tofractureovertime.Thiscontinualresorptionand redepo-sitionof bonemineral,often termedbone remodelling,is intimatelytiedtothepathophysiologyofosteoporosis.3
The balance between bone resorption and bone depo-sition is determined by the activities of two principle celltypes,osteoclastsandosteoblasts.4 Thealterationsin
the intracellular calcium ion (Ca2+) concentrations regu-latedifferentiation andfunctions of osteoclasts.4 Further,
thechangesinintracellularCa2+concentrationsareknown tofunctionasuniversal triggersof diversesignalling path-ways, including enzyme activation, cell survival and cell differentiation.4 This would implythat a reductionin the
Ca2+concentrationisnotonlylikelytoaffectcell differen-tiationandsurvivalbutalsoaffectthefunctioningofvarious neuralpathways.Thiscombinationincreasesthebrittleness ofvariousbonesofthebody.
Accordingtothe InternationalOsteoporosis Foundation (IOF), 40% of women in the world have fractures due to osteoporosisduringtheirlifetime.3Fracturesareassociated
withincreasedmorbidity/mortalityanddiminished quality oflifeinavarietyofways,includingdeclineinphysicaland emotionalfunctioning.5Fallsareresponsiblefor90%ofhip
fractures6andarethesixthleadingcauseofdeathamong
patientsaged65 yearsandolder.7 Inadditiontothe high
mortality,thereareotherdeleteriousconsequencesoffalls, includingrestrictionofmobility,disability,socialisolation, insecurityandfear,ofteninducingacascadeofeventsthat areharmfultohealth and qualityof lifein theelderly.8,9
Researchsuggeststhatalteredbalanceisthegreatest con-tributortowardsfallsintheelderly,withahighcorrelation betweenbalance deficit andincidence offalls.10
been demonstrated to be effective in prevention of falls amongtheelderly,11manyofwhommightbeaffectedwith
lowbonemineraldensity.
It is well documented that calcium is vital for func-tioning of various different organ systems in our body, including the hearing and vestibular systems.12,13
Fur-ther, Madureira et al. observed that the older adults who experienced falls had impaired balance function.14
Since old age is found to be associated with reduc-tion in Ca2+ concentration, there is a likelihood that the impairmentofbalancefunction intheseindividuals might havebeencausedbythedecreasedcalciumconcentration (osteopenia/osteoporosis).3,4 Alternatively, thereare
the-oriessuggesting that reducedvestibularfunctioning could actually be the cause of bone remodelling and thereby osteoporosis,theproofforwhichoriginatesfromthe exper-iments inloweranimals likerats andmice.15,16 Therefore
itappearsthattherecouldbearelationship betweenthe reducedlevelsof calciumand balance sustenanceability. However,thisaspecthasbeenminimallyinvestigated.
Alteredbonecompositionresultsinstructuralchangesof thebonessuchaskyphosis,17whichcanalsoleadtobalance
issues.InastudybyAbreuetal.itwasfoundthatwomen withosteoporosis had worse balance and maximum oscil-lationinevaluationof balanceusingthePolhemussystem infouruprightposturalsituations whencomparedto non-osteoporoticwomen.18Inthegroupwithosteoporosis,Lynn
etal.observedlargerswayamplitudesandinappropriateuse ofbalancemaintenancestrategiesthanthecontrolswhen evaluatedusingthe Computerised Dynamic Posturography (CDP).19 Recentevidencesuggeststhatthedensityof
oto-coniaisreducedinadult femaleosteoporoticrats.20 Since
otoconiaarepresentin theutricleandsaccule,which are vitalforgeneratingtheVestibularevokedMyogenic Poten-tials (VEMP),21,22 impairment of VEMP could be expected
in these patients. However, there are no reports to vali-datethisobservation.Althoughthereissporadicevidence tosuggestthepresenceofvestibulardeficitsinindividuals withosteoporosis, thereis ascarcityofstudiestosuggest whether osteopenia is associated with similar deficits as osteoporosis.Thisthereforehighlightstheneedtostudythe vestibularsystem functioning in individuals with osteope-nia andosteoporosis. Therefore, thepresent study aimed toinvestigate the impact of osteopenia and osteoporosis on the outcomes of behavioural and objective vestibular assessmenttests.
Methods
Participants
Allproceduresperformedinstudiesinvolvinghuman partici-pantswerestrictlyinaccordancewiththeethicalstandards oftheinstitutionalresearchcommittee.Thepresentstudy included 35 participants who had undergone bone min-eral density test. The WHO (2004) has recommended a diagnosis of osteopenia when the T-score (outcome of bone mineral density test) is between −1.1 to −2.5and osteoporosis when the T-score is ≥−2.6 (in the negativ-ity),respectively.23 Those withT-scores better than −1.1
(towards positivity) are considered normal. A total of 37 participantswereincludedinthestudy;however2females, both with osteoporosis, could not maintain eye elevation necessaryfor oVEMP,astheyfoundthe tasktoostraining, blinkedoften, and therefore theywereexcluded. Finally, afterexclusions and based onthe T-scores thestudy had 12individuals each in thehealthy control group (6males
and6females;agerange:42---75years,meanage=58years, SD=10.5)andosteopeniagroup(6malesand6females;age range:45---76years,meanage=64.4,SD=9.6)whereas11 individuals were therein theosteoporosis group (5 males and 6 females; age range:47---76 years,mean age=62.1, SD=8.9).Therewasnosignificantdifferenceinagebetween the groups (p>0.01, MANOVA). Sincethe objective vesti-bularassessmentandconductivepathologiesareknownto causeabsenceofcVEMPandoVEMP,personswithconductive pathologies were excluded. Further,individuals with neu-rological deficits wereexcluded afterconsultation with a neurologist.The screening byan experienced otolaryngol-ogist helpedto exclude personswith other known causes ofvestibularpathologies.Personswithahistoryof occupa-tionalnoiseexposureandexposuretoototoxicmedication werealsoexcluded fromthestudy.Allparticipantsin the studyhadnormallevelsofthyroideventhoughallthefemale participantsinthestudywerepost-menopausal.Noneofthe participantshadundergoneanytreatmentforalteredbone remodelling,astheywererecentlydiagnosed.Themale par-ticipants of the study had an urban sedentary life style, however 5femaleparticipants in eachgroup were house-wives. None of the participants were chronic smokers or alcoholics.Allparticipantssignedtheinformedwritten con-sentformbeforebeingrecruitedtothestudyandtheywere notpaidfortheirparticipationinthestudy.Informed con-sentwasobtainedfromallindividualparticipantsincluded.
Instrumentationandenvironment
Inthepresentstudy,allthebehaviouraltestswerecarried outin awell-illuminatedandair-conditioned room.These includedFukudaSteppingTest(FST),TandemGaitTest(TGT) andSubjectiveVisualVertical(SVV)test.Theobjectivetests werecarriedoutinasound-treatedroomwithnoiselevels well withinthepermissiblelimitsrecommendedby Amer-ican National Standards Institute (ANSIS3.1, 1991).24 The
objectivetests included cervical andocular VEMP (cVEMP andoVEMP).CervicalandOcularVEMPswererecordedusing BiologicNavigatorProversion7.2.1withSINSER-012insert earphones.
Procedure
FortheFST,theparticipantswereinstructedtostretchboth theirarmsinfrontofthemandmarchwiththeireyesclosed at the same place for 50 steps at a rate of 1 step. The angleofdeviation>45◦ ineitherdirectionand/ordistance of deviation >1m was considered abnormal as reported previously.25 Forthe TGT, the participants were asked to
imagine a straight line on the floor and walk heel-to-toe alongitfor30s.Lossofbalanceorraisingofarmstoensure balance sustenancebefore30s was deemedabnormal, as reported previously.26 During the SVV, participants were
handeda bucketwithabrightstrip placedinsideit. They were instructed toplace their head asinside the bucket ascomfortableandalign thepositionof thestrip in their perceivedverticalposition.Thebucketwashandedat dif-ferentanglestotheparticipantsinordertoreducebias.The angleofdeviationfromtheactualverticalwasnotedbya pointerindicatingtheanglesona360◦protractorattached tothebackofthebucket.A>3◦deviationoftheperceived verticalfromthetrueverticalwasdeemedtobeabnormal result.Thisisasperthepreviouslyreportedfindings.27,28
Beforerecording the evoked potentials, the electrode placement sites were scrubbed using a commercially
availableabrasivegel.Thedisctypesurfaceelectrodeswere placedusingcommerciallyavailable conduction pasteand secured in placeusing surgical plaster. The absolute and inter-electrodeimpedancewasmaintainedbelow5kand 2krespectivelyforbothcVEMPandoVEMP.
For the cVEMPrecordings, the electrodes were placed atthesternoclavicularjunction(inverting),superior1/3rd ofsternocleidomastoidmuscle(non-inverting)andforehead (ground).Fortheactivationofthesternocleidomastoid mus-cle, the participants wereasked to turn their head away fromtheearofstimulation.Therecordingwasdonefortone burstsof500Hz,750Hzand1000Hzwith1msrise/falltimes anda2msplateautime.Thetone-burstswerepresentedto theearatan intensityof125dBpeSPLusingastimulation rateof5.1Hz.A1---1500Hzband-passfilterwasusedandthe responseswereaveragedfor200sweeps.Thepre-stimulus rectificationwas usedto control for the effects of varia-tionsintheelectromyographicactivitybetweenthecVEMP recordings.
The oVEMP was obtained by placing the non-inverting electrode on the skin surface 1cm below the centre of thelowereyelid,invertingelectrode2cmbelow the non-invertingandgroundontheforehead,asfoundappropriate and usedpreviously.29,30 The participants were instructed
tomaintaina30◦ upwardcentregazebystaringatastrip placedattheappropriateelevation.Therecordingwasdone usingtone bursts of 500Hz, 750Hz and1000Hz with1ms rise/falltimesanda2msplateautime.Thetoneburstswere deliveredtotheearcanalat anintensity of125dBpeSPL usingarepetitionrateof5.1Hz.A1---1000Hzband-passfilter wasusedandtheresponseswereaveragedfor200sweeps. In order to compare the results of vestibular evalua-tionagainstthebetterknownaudiologicalresultsinpersons withreducedbone-mineraldensity,audiologicalevaluations werecarriedout.Theseincludedpure-toneair-and bone-conductionaudiometry,SpeechReceptionThreshold(SRT), Speech Identification Scores (SIS), immittance evaluation (tympanogramtype,acousticreflexthresholdandresonance frequency)anddistortionproductoto-acousticemissions.
Statisticalanalyses
TheEqualityoftestforproportionswascarriedouttofind the proportionof participants showing abnormal findings. This wasalsodone toinvestigatethebetween groups dif-ference in response rate (number of ears with presence of cVEMP/oVEMP at 500Hz) and frequency tuning. Sepa-rateone-wayrepeatedmeasureANOVAforearswithgroup asthe between subjects factor wasdone for latencies of individualpeaksandpeak-to-peakamplitude.Further, one-way repeated measures ANOVA was done for ears with grouponthebetweensubjectfactorforpure-toneaverage, speechrecognition threshold,speechidentification scores andstaticcompliance.TheEqualityoftestforproportions wasdonetofindthedifferencesifanyintheresponserates of acoustic reflex and DPOAEs. Chi-square analyses were donetoinvestigatetheassociationbetweenthegroupsand theoutcomesofvariousevaluations.
Results
A detailed structured case history was obtained from all theparticipantsin eachof thethreegroups.It wasfound that only one participant in the control group reported vestibularsymptoms(swayingwhile walking).Noneof the other participants in the control group reported of any
vestibular symptom such as vertigo, swaying and imbal-ance.These symptomswerereportedby4 participants(3 vertigoand1imbalance)intheosteopeniagroupand7 par-ticipants(5 vertigo and 2imbalances) in the osteoporosis group.Inordertoinvestigatethestatisticalsignificanceof the above mentioned observations from the case history, the Equality of test for proportions was done. A signif-icantly higher proportion of individuals with osteoporosis werefoundtoexhibitvestibularsymptomsthanthecontrol group(Z=2.78,p=0.005).However,therewasnosignificant differenceinthe proportionof individualswith vestibular symptomsbetween the osteopeniagroup and the control group(Z=1.50,p=0.15)andalsobetweenthe osteopenia groupandtheosteoporosisgroup(Z=1.45,p=0.14).
Comparisonbetweenthegroupsonbehavioural tests
Adeviationoftheperceivedverticalof>3◦oneithersideof theactualverticalhasbeenconsideredanabnormalresult onSVV.27,28Consideringthisnormative,theabnormalresults
werefoundonSVVinasignificantlyhigherproportionof indi-vidualswithosteoporosis(Z=2.40,p=0.01)andosteopenia (Z=1.88, p=0.05)thanthecontrol group.However,there wasnosignificantdifferencebetweentheosteopeniagroup andtheosteoporosisgroup(Z=0.61,p=0.53).
TheresultsonFSTwasconsideredabnormalwhenthere wasadeviationof>45◦ oneithersideand/oradistanceof morethan 1m fromthe starting point.25 Considering this
normative, significantly higher (marginally) proportion of individualswithosteoporosishadabnormalresultsthanthe healthycontrolsonFST,asrevealedbytheEqualityoftest forproportion(Z=1.82,p=0.06).Thecomparisonbetween theothergroupsrevealednosignificantdifference(p>0.1). The inability to perform a balanced heel-to-toe walk (e.g.,tendency tofall, raisinghandsto maintainbalance orstumbling)wasconsideredanabnormalresultonTGT.26
The osteoporosis group had significantly higher propor-tionsofabnormalresultsonTGTthanthehealthycontrols (Z=2.10, p=0.03)or osteopeniagroup(Z=2.59,p=0.09). There was no significant difference between the other
Subjective tests Aff ected individuals (%) FST TGT SVV 80.00 60.00 0.00 20.00 40.00 Control Osteopenia Osteoporosis * * * * * * * *
Figure1 Percentageofparticipantswithabnormalresponses for each of the three subjective tests in each group. One starindicates marginallysignificant difference(0.05>p<0.1) between thegroups and two stars indicate highlysignificant difference(p<0.01)betweenthegroups.
Control group (R) Osteoporosis (L) Osteoporosis (R) Osteopenia (R) Osteopenia (L) Latency (ms) 1.0 -10.0 1.0 12.0 -10 -1.0 1.0 -110 -11.0 -10.0 -210 -210 -210 -210 78.0 67.0 67.0 67.0 67.0 78.0 78.0 78.0 56.0 56.0 56.0 56.0 45.0 34.0 23.0 90 9.0 19.0 19.0 29.0 29.0 39.0 39.0 49.0 49.0 59.0 59.0 69.0 69.0 79.0 79.0 P1 P1 P1 P1 P1 P1 N1 N1 N1 N1 N1 N1 !1.0 -10.0 -10.0 1.0 1.0 12.0 12.0 23.0 23.0 23.0 34.0 34.0 34.0 45.0 45.0 12.0 45.0 Control group (L)
Figure2 RepresentativecVEMPwaveformsobtainedfromoneparticipantwithnormalbonemineraldensity(top-mostpanel)and aparticipanteachwithosteopenia(middlepanel)andosteoporosis(bottom-mostpanel).
groups (p>0.1). Fig. 1 shows the percentage of individ-ualswithabnormalresultsineachgrouponthebehavioural tests.
ComparisonbetweenthegroupsoncVEMP
IpsilateralcVEMPswererecordedfrombothearsofallthe participants in each of the groups. Fig. 2 shows the rep-resentative waveforms of cVEMP from one participant in eachofthethreegroups. Themean,medianandstandard deviationoflatenciesandpeak-to-peakamplitudeof500Hz
tone-burst evoked cVEMP werecalculated and have been mentionedinTable1.
The within and between groups comparison of various parametersofcVEMPwasachievedusingone-wayrepeated measuresANOVAforearswithgroupasthebetweensubjects factor.Eventhoughtherewasatrendforsmalleramplitude inthetwoclinicalgroupsthanthecontrolgroups(smallest amplitudeinosteoporosis),theresultsofone-wayrepeated measures ANOVA revealed no significant main effect for withinandbetweengroupscomparisononanyoftheabove mentionedparametersofcVEMP(p>0.1).
Table1 Mean,medianandstandarddeviationoflatenciesofP1,N1andpeak-to-peakamplitudeof500Hztone-burstevoked cVEMPfromthethreegroupsofparticipants.
cVEMP Controlgroup(n=21) Osteopenia(n=24) Osteoporosis(n=17)
¯ x M SD ¯x M SD ¯x M SD P1 15.80 16.01 1.78 16.06 16.17 1.23 16.12 16.13 1.65 N1 23.81 23.77 2.95 24.26 24.23 1.90 23.69 22.92 2.48 P1N1 12.82 11.38 7.49 12.15 11.09 6.79 9.44 6.13 6.66 ¯
x,mean;M, median;SD,standarddeviation;P1,latencyofP1peakinmilliseconds;N1, latencyofN1peakinmilliseconds;P1N1, peak-to-peakamplitudeofcVEMPinmicrovolts;cVEMP,cervicalvestibularevokedmyogenicpotential.
Control group (L) Control group (R)
Osteopenia (L) Osteopenia (R) Osteoporosis (L) Osteoporosis (R) Latency (ms) N1 N1 N1 N1 N1 N1 P1 P1 P1 P1 P1 P1 56.0 56.0 56.0 56.0 45.0 45.0 45.0 45.0 34.0 34.0 34.0 34.0 23.0 23.0 23.0 23.0 12.0 12.0 12.0 12.0 1.0 1.0 1.0 1.0 -10.0 -10.0 -10.0 -10.0 -21.0 -21.0 -7.0 -13.0 -21.0 -21.0 -13.0 -13.0 47.0 41.0 35.0 29.0 23.0 17.0 11.0 5.0 -1.0 -7. 0 -1.0 5.0 11.0 17.0 23.0 29.0 35.0 41.0 47.0
Figure3 RepresentativeoVEMPwaveformsobtainedfromoneparticipantwithnormalbonemineraldensity(top-mostpanel)and aparticipanteachwithosteopenia(middlepanel)andosteoporosis(bottom-mostpanel).
Table2 Mean,medianandstandarddeviationoflatenciesofN1,P1andpeak-to-peakamplitudeof500Hztone-burstevoked oVEMPfromthethreegroupsofparticipants.
oVEMP Controlgroup(n=21) Osteopenia(n=24) Osteoporosis(n=17)
¯ x M SD ¯x M SD ¯x M SD N1 11.72 11.87 1.40 11.31 11.78 1.92 13.10 12.91 2.38 P1 16.89 16.77 1.94 17.09 17.12 2.81 17.75 17.92 1.03 N1P1 2.41 2.69 1.50 2.28 2.08 2.98 1.45 1.74 3.82 ¯
x,mean;M,median;SD,standarddeviation;N1, latencyofN1peak inmilliseconds;P1,latencyofP1peakinmilliseconds;N1P1, peak-to-peakamplitudeofoVEMPinmicrovolts;oVEMP,ocularvestibularevokedmyogenicpotential.
VEMP (500 Hz) cVEMP oVEMP 0.00 20.00 40.00 60.00 Absent responses (%) Control Osteopenia Osteoporosis * *
Figure4 ResponseratesforcVEMPandoVEMPinthethree groups.Starsindicatehighlysignificantdifference(p<0.01).
ComparisonbetweenthegroupsonoVEMP
IpsilateraloVEMPswererecordedfrombothearsofallthe participants in each of the groups. Fig. 3 shows the rep-resentative waveforms of oVEMP from one participant in eachofthethreegroups. Themean,medianandstandard deviationoflatenciesandpeak-to-peakamplitudeof500Hz tone-burstevoked oVEMP were calculated and have been mentionedinTable2.
There wasatendency for longer latencies andsmaller peak-to-peakamplitudesinthetwoclinicalgroups(longest latenciesandsmallestamplitudeinosteoporosis)thanthe control group. However, the results of one-way repeated measuresANOVA for earswithgroup asthebetween sub-jectsfactor revealednosignificant maineffectofearand grouponanyoftheabove-mentionedparametersofoVEMP (p>0.1).
TheEqualityoftestforproportionwasdoneto investi-gate thebetween thegroups’ differencein responserate (numberofearswithpresenceofcVEMP/oVEMPat500Hz) andfrequency tuning.Therewasnosignificant difference in the response rate of cVEMP and proportions of fre-quencytuningatanyofthefrequencies(p>0.1).However, significantly higher proportions of individuals with osteo-porosis hadcomplete absence of oVEMP than the control group (Z=3.23, p=0.001) and osteopeniagroup (Z=3.54,
p=0.000).Therewasnosignificantdifferenceinresponse rates of oVEMP between osteopenia and control group (Z=0.36,p=0.71).Fig.4showstheresponseratesofcVEMP
andoVEMPacrossthegroupsandtheoutcomeofthe Equal-ityoftestforproportions.
Outcomesofhearingassessment
All the participants underwent pure-tone audiometry, speech audiometry, immittance evaluation and Distortion ProductOto-AcousticEmission(DPOAE).Noneofthe partici-pantshadanyconductivepathology,asthisservedasoneof theexclusioncriteria.Therewasatrendtowardsincrease inPure-Tone Average(PTA),SRT,resonance frequencyand acoustic reflexthreshold and reduction in SIS and DPOAE amplitudeinthetwoclinicalgroupsthanthecontrols; how-ever the groups werenotsignificantly differentonany of these tests(p>0.1). The osteoporosis group revealed sig-nificantly higher proportions of ears withabsent acoustic reflexesanddistortionproductoto-acousticemissionsthan controlgroupandosteopeniagroup(p<0.05).Therewasa significantassociationbetweengroupsandSRT[2(2)=35.7, p=0.000], groups and SIS [2(2)=131.85, p=0.000] and groups and resonance frequency [2(2)=46.49, p=0.001] withmore individualswithhighervalues ofSRTand reso-nancefrequencyandlowervalueofSISintwoclinicalgroups thanthecontrolgroup.
Associationbetweenhearingandbalance
All the individuals in osteopenia and osteoporosis groups underwentaudiologicalandbalanceevaluations.For study-ing the association between hearing and balance related deficits, the PTA of 20dBHL or more was deemed an abnormalresult(personhadhearingloss)whereasthe pres-enceofabnormalfindingsontwoofthethreebehavioural balance assessment tests (Fukuda stepping test, Tandem gait test and subjective visual vertical test) was con-sidered an abnormal result. In terms of the objective vestibularassessment tests,absenceof anyoneof cVEMP or oVEMP or both in one or both sideswasconsidered an abnormal result. The Chi-square test revealed significant associationbetweenpresenceofhearinglossandabnormal resultonbehaviouralbalanceassessmenttests[2(1)=4.82, p=0.028] and marginally significant association between presenceof hearinglossandabnormalresultonobjective vestibularassessment[2(1)=3.45,p=0.063].
Discussion
In the present study significantly a higher proportion of individualswithosteoporosisreportedvestibularsymptoms thanindividuals withosteopeniaor individualsin the con-trol group. These findings are in agreement with those
reportedpreviouslyinthisregard.17,19 Olderagehasbeen
showntobeassociatedwithhigherprevalenceofvestibular symptoms.18,31However,therewasnosignificantdifference
inagebetweenthegroupsofthepresentstudy.Therefore, oldagecannotexplainthesefindings.Thesefindingsmight beattributedtothereductionincalciumcontentwithinthe vestibularsystem.Thecristaampullarispresentattheend ofeachofthesemicircularcanalsandthemaculaepresent ineachoftheotolithorgansconsistoflargevolumesof cal-cium(CaCO3).20Thestudiesonratshaveshownthepresence ofultrastructuralchanges(decreaseddensity)inthe macu-laeofratsthathadosteoporosisthaninthosewhichdidnot. Although therearenohuman studies reportingsuch ultra structuralchanges,similarchangesmightbeassociatedwith osteoporosis,whichcouldinturnaffectthemaintenanceof bodybalance.
Comparisonbetweenthegroupsonbehavioural tests
TheresultsofSVVinthepresentstudydemonstrateda sig-nificantlyhigherproportionofabnormalresultsinthetwo clinicalgroupsthanthecontrolgroup.SVVhasbeenfoundto beasensitivetestfor detectionofutricularpathology.32---34
Thereforetheresultspointtowardsthepresenceof utricu-larpathologyincaseswithosteopeniaandosteoporosis.The utricularpathologyinosteopeniaandosteoporosiscouldbe asa result of thereduction in calcium withinthe utricu-larmacula.The utricularmaculaconsistsoflargeamounts of calcium carbonate crystals (otoconia) which form the majormass of themacula andhave been reportedto be vitalfortheactivation(depolarization)orinhibition(hyper polarization).35Astudyonloweranimalswithosteoporosis
hasshown ultra structuralchanges in theotoconia of the utricle.20 Althoughtherearenostudies ofhumans,a
sim-ilar pattern of ultra structural changes in otoconia might beexpected.Sincetheutricleplaysavitalrolein identi-fyingtheverticalityofanobject,34theanatomicalchanges
causedbyosteoporosisandosteopeniaintheutriclecould havecausedmoredeviationintheperceivedvertical.
The results on other behavioural balance assessment tests(FST andTGT)revealedabnormalresults ina signif-icantly higher proportion of individuals with osteoporosis than osteopenia andthe healthy controls. Although using other tests (CDP, Romberg and standing balance),studies showedhigherswayamplitudesandmoreabnormalresults in individuals withosteoporosis than healthycontrols.19,31
Thusthisshowspresenceofvestibularpathologyin individ-ualswithosteoporosis.Thisagainmightbeattributedtothe ultrastructuralchangesintheperipheralvestibularsystem20
asdescribedabove.
ComparisonbetweenthegroupsoncVEMPand oVEMP
In the present study the results of objective assessment demonstrated a significantly higher proportion of abnor-malresultsinindividualswithosteoporosisthanosteopenia and control group on oVEMP,but not oncVEMP. Although the process of ageing has been shown to be associated withreduction in amplitude and absenceof Cvemp36 and
oVEMP,37,38 this probably couldnot have been the reason
behind suchfinding in the present study asthere wasno significantagedifferencebetweenthethreegroupsofthe presentstudy.Further,thesubjectselectioncriteriaensured thatsubjectswithconductivepathologywerenotincluded
inthestudy.This wasdonebecauseconductivepathology hasbeen knownto adverselyaffect VEMPs.39,40 Therefore
it also unlikely that absence of responses in more num-ber of ears with osteoporosis was because of conductive hearingloss. SinceoVEMP is mediated along the utriculo-occularpathway,andcVEMP alongsacculo-collicpathway, the abnormal results on oVEMP further substantiate the presenceofutricularpathology.Italsopointstowardsmore robustnessandlessersusceptibilityofsacculeandinferior vestibularnervetothedetrimentaleffectsofpathology.The samehasbeenconfirmedthroughthefindingsofcVEMPand oVEMPinothervestibularpathologieslikeBenign Paroxys-malPositionalVertigo,41,42vestibularneuritis43andauditory
neuropathyspectrumdisorders.44
Analternate thoughtworth discussinghereisthat ofa possibility of the vestibular disturbances resulting in the whole process of bone remodelling. Some of the experi-mental evidences from lower animals like rats and mice tend tosuggest that reducedvestibular functioningcould actually be the cause of bone remodelling and thereby osteoporosis.15,16Whether thisistrueinhumanbeingsisa
matterofdebateandneedsfurtherexperimentalstudiesin humanswithvestibularproblems. Nonetheless, thiscould beanimportantresult,iftheevidencesuggests.
Associationbetweenhearingandbalancedeficits
Thefindingsofthepresentstudyrevealedsignificant asso-ciationbetweenthepresenceofhearinglossandpresence of balance deficits. There are no studies, to the best of our knowledge, that have looked at such an association betweenhearing andbalancein individuals with osteope-niaandosteoporosis.This(significantassociation)indicates thatpeoplewithreducedbonemineraldensityhavehearing aswellasbalancerelateddeficitsandthetwoareclosely relatedtoeachother.Thisfurthersignifiestheneedfornot onlyhearingevaluationbutalsoforbalanceassessmentin individualswithosteopeniaandosteoporosis.
Aclosescrutinyoftheoverallresultsofbalancetesting shows a wide variety of results which suggests a spec-trumratherthanasinglegeneralizedcondition.Thiswould suggestaneedformorecomprehensiveassessmentand pro-filingof results on balance assessment in osteopeniaand osteoporosisinordertodevelopaprotocolinfuture.
Overall, thefindings fromthe present study showthat osteopeniaand osteoporosis are associated witha higher prevalence of imbalance in general and vestibular dys-function in particular. However, the study used only 35 participantssplit intothreegroups toarrive at such find-ings.Thisisnotanappropriatesamplesizeconsideringthe prevalence of osteoporosis and osteopenia in the general population.Nonetheless,thestudyisapreliminary investi-gationandthefindingsareencouragingenoughtowarrant continuedexplorationintheareaofbalanceandvestibular functiontestingwithlargersamplesizes.
Conclusion
Findingsofthepresentstudyareatestimonytothepresence of balance-related deficits in individuals with osteopenia and osteoporosis. Therefore, clinical evaluations should includebalance assessment asamandatoryaspect of the overallassessmentsothataholisticmanagement,whichwill beinclusiveofthebalancerelatedrehabilitation,couldbe planned.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
Wewouldalsoliketothankthe DirectorandHOD Audiol-ogy,AllIndiaInstituteofSpeechandHearingforpermitting to carry out the research and providing the necessary infrastructure.
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