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www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Preoperative

vestibular

assessment

protocol

of

cochlear

implant

surgery:

an

analytical

descriptive

study

Roseli

Saraiva

Moreira

Bittar,

Eduardo

Setsuo

Sato

,

Douglas

Jósimo

Silva

Ribeiro,

Robinson

Koji

Tsuji

UniversidadedeSãoPaulo(USP),EscoladeMedicina,DepartamentodeOtorrinolaringologia,SãoPaulo,SP,Brazil

Received2July2015;accepted20June2016 Availableonline31July2016

KEYWORDS

Cochlearimplant; Vestibularfunction; Preoperative diagnosis

Abstract

Introduction:Cochlearimplantsareundeniablyaneffectivemethodfortherecoveryofhearing functioninpatientswithhearingloss.

Objective:Todescribethepreoperativevestibularassessmentprotocolinsubjectswhowillbe submittedtocochlearimplants.

Methods:Ourinstitutionalprotocolprovidesthevestibulardiagnosisthroughsixsimpletests: RombergandFukudatests,assessmentforspontaneousnystagmus,HeadImpulseTest, evalu-ationforHeadShakingNystagmusandcalorictest.

Results:21patientswereevaluatedwithameanageof42.75±14.38years.Only28%ofthe samplehad allnormaltest results.Thepresence ofasymmetricvestibular informationwas documentedthroughthecalorictestin32%ofthesampleandspontaneousnystagmuswasan importantclueforthediagnosis. Bilateralvestibular areflexiawas presentinfoursubjects, unilateralarreflexiainthreeandbilateral hyporeflexiaintwo.TheHeadImpulseTestwasa significantindicatorforthediagnosisofareflexiainthetestedear(p=0.0001).Thesensitized Rombergtestusingafoampadwasable todiagnoseseverevestibular functionimpairment (p=0.003).

Conclusion:Thesixclinicaltestswereabletoidentifythepresenceorabsenceofvestibular functionandfunctionasymmetrybetweentheearsofthesameindividual.

© 2016 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/).

Pleasecitethisarticleas:BittarRS,SatoES,RibeiroDJ, TsujiRK.Preoperativevestibularassessmentprotocolofcochlearimplant

surgery:ananalyticaldescriptivestudy.BrazJOtorhinolaryngol.2017;83:530---5.

Correspondingauthor.

E-mail:esetsuo@icloud.com(E.S.Sato).

PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.

http://dx.doi.org/10.1016/j.bjorl.2016.06.014

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PALAVRAS-CHAVE

Implantecoclear; Func¸ãovestibular; Diagnóstico pré-operatório

Protocolodeavaliac¸ãovestibularpré-operatóriadacirurgiadeimplantecoclear: estudodescritivoanalítico

Resumo

Introduc¸ão: Osimplantescocleares(IC)sãoindiscutivelmenteummétodoeficazderecuperac¸ão dafunc¸ãoauditivadepacientessurdos.

Objetivo: Descreveroprotocolodeavaliac¸ãovestibularpré-operatóriaemsujeitosqueserão submetidosaoIC.

Método: Nossoprotocoloinstitucionalprevêodiagnósticovestibularpormeiodeseistestes simples:testesdeRombergeFukuda,nistagmoespontâneo,HeadImpulseTest,HeadShaking Nistagmus,provacalórica.

Resultados: Foramavaliados21pacientescomidademédiade42,75±14,38anos.Apenas28% daamostraapresentoutodosostestesnormais.Apresenc¸adeinformac¸ãovestibularassimétrica foidocumentadapelaprovacalóricaem32%daamostraeonistagmoespontâneomostrou-se pistaimportanteparaseudiagnóstico.Aarreflexiavestibularbilateralfoidiagnosticadaem qua-trosujeitos;arreflexiaunilateralemtrêsehiporreflexiabilateralemdois.OHeadImpulseTest

mostrou-seindicadorsignificante(p=0,0001)paradiagnosticararreflexiadaorelhatestada.O testedeRombergsensibilizadoemalmofadafoicapazdediagnosticaroscomprometimentos severosdafunc¸ãovestibular(p=0,003).

Conclusão:Osseistestesclínicosforamcapazesdeidentificarapresenc¸aounãodefunc¸ão vestibulareassimetriadafunc¸ãoentreasorelhasdeummesmoindivíduo.

© 2016 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

Cochlearimplants(CI)arehighlyeffectivedevicesfor recov-eryofhearingfunctioninindividualswithhearinglossand have facilitated integration into social life. The success ofpost-implantrehabilitationhasraisednewchallengesin boththeselectionandtheplanningofthehearing progno-sis of subjects undergoing surgery. Although the cochlear system is distinct from the vestibular system, both have identical neural transmission.The benefits of the electri-calstimulationoftheCIgobeyondtheauditorypathways andalsobenefitthevestibularsystemandposturalcontrol.1

Nonetheless, the CI is not without risk to the semicircu-lar canaland otolithfunction andmayimpairor suppress vestibular function, especially if there is pre-existing pathology.

The prevalenceofpostoperativedizzinessvarieswidely intheliteratureandis around20% inourcases.Itusually resolvesinapproximately30 days.Someof thesepatients developbilateralvestibularareflexia(BVA),whichseverely reducespatientqualityoflife.2Knowledgeofvestibular

sys-temfunction beforeand after CIsurgery is importantfor thesatisfactory managementofeach case.Therefore,we have added vestibular assessment to our outpatient rou-tine prior to CI surgery. Our main goal is to document the existence of vestibular function and possible asym-metriesbetweentheearsbeforesurgery.Thisinformation canhelp intheselection ofwhich eartoimplantand can assistin the management of any postoperative vestibular symptoms.

In adults, preoperative vestibular assessment was designedtobebriefandeasy toperform,usingresources

availableatanyotorhinolaryngologyoutpatientclinic.The testsusedareable toidentifyboth vestibularasymmetry fromunilaterallesionsaswellasbilateralinvolvement.The protocolwasdesignedtobeaccessibletoservicesthat per-formCI surgery but do not always have a neurotological departmentandresearchequipment.

It is not our intention to speak at length about each vestibular test used, but to provide the reader a quick andconvenientmethodtoidentifyvestibularimpairment. Knowledgeofvestibularfunctioncanindicatetheadequate managementandpreventundesirablesideeffects.3,4

Ourgoalistodescribethepreoperativevestibular assess-mentofadultpatientswhoarecochlearimplantcandidates inourinstitution,demonstrateitseffectivenessanddiscuss itsimportanceinthepostoperativeoutcome.

Methods

Thisisadescriptiveandanalyticalcross-sectionalstudythat followed the ethical standards approved by the CAEPesq number0983.07. All participants arefrom the Institution OtorhinolaryngologyClinic.

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Table1 Listofassessedpatientsregardinggender,ageand etiologyofhearingloss.

Gender Age Etiologyofhearingloss

SLNSJ M 20 Meningitis ADPDJ M 21 Meningitis

FDCDSCF M 27 Traumaticbraininjury(TBI)

KPG F 28 Unknown

ROR F 29 Unknown

LTF M 32 MeningitisandTBI

GFR M 35 TBI

AMPDS M 38 Meningitis LJAC F 42 Unknown LALM F 45 Unknown DAA M 45 Meningitis

GBP F 45 Measles

SM F 45 ChronicotitismediaandTBI RDCCDS F 45 Toxoplasmosis

MSC F 46 Genetichearingloss EBDS F 48 Meningitis

ACDS F 49 Unknown

MCB F 51 Unknown

JONDC M 63 Otosclerosis FFT M 66 Chronicotitismedia PLDS M 77 Otosclerosis

completeabsenceofvestibularfunction.Thestudysample includingtheiragesandetiologiesareshowninTable1.

VORandvestibularasymmetryassessment5

Spontaneousnystagmus6

Spontaneousnystagmus(SN)is ocularmovement observed withthepatientinthesittingpositionwiththeeyesfixed straight ahead. The presence of SN indicates vestibular asymmetryandis theresults of asymmetryin oculomotor tonethatoriginatedfromthevestibularsystem.Itconsistsin aslowgazedeviation,followedbyaquickmovementofthe eyeballtothecenterposition(correctivesaccades).When ithasaperipheralorigin,spontaneousnystagmusdecreases witheyefixation and intensifieswhen theeye is diverted 30◦ toward the fast component (Alexander’s Law).6 The

directionof the nystagmusis the direction ofthe correc-tivesaccadewhichiseasiertovisualize.Butitistheslow gazedeviationthatdeterminesthesidewith hypofunction-inglabyrinth.

HeadImpulseTest(HIT)7

TheHeadImpulseTestisasimpleclinicalmaneuverto iden-tifyanimpairedvestibulo-ocularreflexinthetestedearby observingtheocularresponsethatoccursafteraquickhead movement.Whilefacingtheexaminer,thepatientfocuses onatargetontheexaminer’sface.Theexaminerholdsthe patient’sfaceinhis/herhandsandsuddenlyturnshis/her head,andobservestheocularresponse.Anormalindividual willkeephis/hereyesonthetarget,butwhenthe vestibulo-ocular reflex (VOR) is impaired, the eyes will follow the movementoftheheadandthen performasaccadeinthe

oppositedirectiontothecorrectiveheadmovementto re-fixateonthevisualtarget.

HeadShakingNystagmus8,9

TheHeadShakingNystagmus(HSN)examinationinvestigates asymmetryofmuscletoneathighfrequenciesofhead rota-tion.The patientsitsface-to-face withtheexaminer and looksatatargetontheexaminer’sface.Thenthepatient performs20lateralheadturnsathighspeed.Attheendof thetest,thepatientinterruptstherotations,stabilizesthe headandremainsfacingthefrontdirection.The presence ofnystagmusindicatesasymmetryofvestibularinformation. Inperipherallabyrinthinedisorders,theslowgazedeviation indicatesahypofunctioninglabyrinth.

Calorictesting5

Calorictestingisperformedinthesupinepositionwiththe headflexed30◦.Waterat 30and44isthestimulusused

for thetest.Irrigations areperformed inboth earswitha five-minute interval between them. The resulting nystag-musis recordedusingnystagmography equipment.Normal angular velocities of nystagmus are between 7◦ and 52.

Whentheangularvelocityofthemovementsexceedsthese limits,it is called hyperreflexia andwhen it is below the minimum,hyporeflexia. The equipmentusedin this study wasthevector-electronystagmographySCEContronic®.

Labyrinthine predominance (LP) designates asymmetry betweenthevestibularresponses.Avalueof18%waschosen for LP.The presenceofLP meansasymmetryofvestibular informationofperipheralorcentraloriginandalways indi-catesthesidewithbetterfunction.

Posturaltestassessment

Alterations of the Romberg’s and Fukuda’s tests are not pathognomonicofvestibularpathology,althoughtheyhelp with the diagnosis. The tests can be influenced by pro-prioceptive or neurological lesions and should be used in conjunctionwithothervestibulartests.

Romberg’stest10

The patientis instructedtostandwithheelstogetherand toesapartatapproximately30◦

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Figure1 Testusingafoampad.

Fukuda’stest12

Fukuda’stestisusedtoidentifytoneasymmetriesinthe dis-tallower-limbmuscles.Witharmsoutstretched,thepatient isaskedtomarch60stepswiththeeyesclosedandwithout moving.The subject’sanglesof deviationandshiftingare evaluated.Attheendofthetest,anangulardeviationofup to30◦

andthelineardisplacementofupto50cmare consid-erednormal.Theposteriordisplacementinrelationtothe startingpointisnotcommon.Rotationshigherthan45◦are

consideredabnormal.Asymmetricallesionsofthevestibular

Table 2 Significance of the incidence of falls at the Rombergtestusingafoampadinrelationtotheabsenceof vestibular functioninoneearinsubjectswithasymmetric post-caloricfunction(Fisher’sexacttest).

Falls Nofalls Total

Asymmetricwithoutareflexia 0 7 7 Unilateralvestibularareflexia 3 0 3

Total 3 7 10

Fisher’stest,p=0.008.

systemresultin bodyrotationinthedirectionof theslow nystagmuscomponent---thehypofunctioninglabyrinth.

Testresults werequantifiedaspercentagesand associ-atedusingFisher’sexacttestandp-values≤0.05fora95% confidenceintervalwereconsideredstatisticallysignificant.

Results

Themeantimetakentoperformallthetestswas approx-imately 1h. Of the 21 patients, only 6 (28%) had normal resultsin all tests. Therefore,72% of the sample showed sometypeofalterationduringvestibularassessment.

Regardinginformationasymmetry,weidentified10(32%) subjectswiththepresenceofpost-calorictestasymmetry. Ofthese,2(20%)hadspontaneousnystagmus---onecasewas associatedwiththepresenceoflabyrinthinepredominance, whilethe other wasnot.Three subjectswithpost-caloric asymmetryshowed complete lack of response in oneear. Amongtheselastthree,twofellandshowedgreatinstability attheRombergtestusingafoampadandwitheyesclosed (p=0.008)(Table2).

Still considering the caloric test, 1 subject(4.5%) had bilateral hyporeflexia and 4 (18%) bilateral areflexia. All patients(100%)fell duringthe Romberg testusinga foam padwithclosedeyes.Fisher’sexacttest shows an associ-ationbetween the fallat Romberg test usinga foam pad withclosedeyesandareflexiaorseverevestibularfunction impairment(p=0.003)(Table3).

When individuallyanalyzing vestibularfunctionin each ear,thefoursubjectswhohadbilateralareflexia(8ears)and threewithunilateral arreflexia(three ears)at the caloric test,hadapositiveHITresultin6(54%)ears.HITwas consid-eredhighlysignificanttoidentifyareflexicears(p=0.0001) (Table4).

The HSNtest didnotshowanyabnormalresults inthe assessedpatients.

Table 3 Significance of the incidence of falls at the Rombergtestusingafoampadinrelationtothepresenceor absenceofresidualvestibularfunction(Fisher’sexacttest).

Falls Nofalls Total

Presentvestibularfunction 3 13 16 Absentvestibularfunction 5 0 5

Total 8 13 21

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Table4 SignificanceofapositiveHeadImpulseTest(HIT) and absence of function (areflexia) of the assessed ears (Fisher’sexacttest).

PositiveHIT NegativeHIT Total

Areflexicears 8 3 11

Functionalears 0 31 31

Total 8 34 42

Fisher’stest,p=0.0001.

Discussion

Balance is a vital condition for the preservation of our species.Toadequatelyperceivetheenvironmentaroundus andtoreacttoposturalchallengesarenecessaryforbody safety.The structuraland functional integrityof the ves-tibular system is necessary for maintenanceof the entire complexpostural system, adaptationto theenvironment, andthefight-or-flightresponse.The absenceof vestibular functionisaccompaniedbypoorprognosisandsevere lim-itations in the activities of daily life, suchas ambulating inlow-lightenvironmentsoronunevenground,swimming, drivingfast,etc.Afrequentcomplaintisoscillopsiaduring headmovements,especiallyin thedark.13 The benefitsof

theCIareprovenanditspositiveimpactondeafpatients’ auditoryperceptionandqualityarenolongerdebated. How-ever,thesurgicalimplantprocedurerequirestheopeningof thelabyrinthandthereareriskswhenthevestibular func-tionispresent.Priorknowledgeofthevestibularcondition increasesthediagnosticindexandhelpsthemanagementof possiblepostoperativevestibularcomplications. Thereare twoquestionsthatshouldberaised whenweconsiderthe vestibularfunctionofapatientwhowillbesubmittedtoCI: (1)Isvestibularfunction present? (2)Isthe function sym-metric?To answer thesequestionswe developed asimple preoperativeassessmentthatdoesnotrequiresophisticated equipment.

The importanceof thepreoperative assessmentcanbe understoodwhen weobserveour results,whichidentified 72%ofthesamplewithsometypeofvestibularalteration. Incase of normalfunction,when oneearis implanted,it ispossibletoreversethedizzinesssymptom,evenifthere is complete loss of vestibular function on the operated side.Theadequateuseof neuroplasticitymechanismscan restorebodybalancethroughvestibularrehabilitation tech-niques.Thecasesthatoffergreaterriskofpermanentlesion arethosewithvestibularfunctionasymmetrybetweenthe ears.Adequatevestibularassessmentpreventsbilateral ves-tibular areflexia, as it provides data on the presence or absenceofvestibularfunctionandallowschoosingtheear thatofferslowersurgicalrisk.

We identified 10 (32%) subjects with post-caloric test asymmetry. In these cases, spontaneous nystagmus was presentin20%,indicatingthepresenceofvestibular func-tionasymmetryatthecalorictest.

Anotherimportanttesttodetectvestibulartone asym-metry is the HSN test. However, there is difficulty in observingthe head-shakingnystagmus, especiallybecause patientsfixtheirgazeontheexaminer’sfaceattheendof theprocedure.Itisaknownfactthatocularfixationinhibits

nystagmus of peripheral origin. None of our patients had apositive HSNtest, butwhetherthe nystagmusinhibition causedbyocularfixationwouldnothavepreventedthe visu-alizationofthefinalnystagmusisyettobeclarified.Theuse ofFrenzelglasses decreasesthebiasby preventingocular fixation.

Thepatientsevaluatedinthissamplewerenotsubmitted toFukudatest, subsequentlyaddedtothediagnostic rou-tine.Thetestisusefultoassessdeviationssecondarytotone asymmetry and it is routinely usedtoevaluate vestibular compensation during treatment. We decidedtoinclude it subsequentlytoobservetheassociationbetweenvestibular tone asymmetrydiagnosed byspontaneousnystagmusand post-caloricasymmetries--- importantforchoosingtheear tobeimplanted.Insuchcases,boththespontaneous nystag-musandtheFukudatestcontributeimportantinformation whensearchingforunilaterallesions.

Theworstpost-operativesituationisbilateralvestibular areflexia(BVA),asvestibularrehabilitationislimited,only improvingbalanceby50%inthesecases.2BVAcanbe

pre-vented when there is prior knowledge of the vestibular function of the earto be implanted. Classically, BVA can beeasilydiagnosedbyfallincondition5ofthe computer-izeddynamic posturography,whichsubjectstheindividual tooscillationoffootsupportwithclosedeyes.Condition5 canbeperfectlymimickedbytheRombergtestusingafoam pad.Inthissituation,withoutthevisionandwithconflicting proprioceptive information, the only determinant of pos-tureisthevestibularfunctionand,initsabsence,thefall occurs.14,15

Patientswithpost-caloricasymmetryduetoabsenceof vestibular responses on one side also showed a low per-formanceonthe Romberg testusinga foam pad:66% fell and33%showedsevereinstability.Statisticalanalysisofthe sampleshowsthattheRombergtestusingafoam padwas sensitivetodiagnoseseverevestibularfunctionimpairment (p=0.003).Ourdataareconsistentwiththeliteraturethat attributes79%ofsensitivityand80%ofspecificitytothetest whendetectingunilateralorbilateralarreflexia.16

Inthosepatientswhohadnovestibularresponsetothe caloric test, the HIT wasvaluable (p=0.0001). A positive test resultis highlysuggestive of failureof the vestibulo-ocular reflex,withtheadditionaladvantageofidentifying theaffectedside.7 Thediagnosis ofvestibularareflexiain

theeartobeimplantedmakesthesurgeonmoreconfident, asthereisnofunctiontobecompromised.Inbilateralcases, thereisnoriskofpostoperativedizziness.

Finally,itisimportanttorememberthattheknowledge of the vestibular function prior tothe surgery allows the physicianto assesswhat occurred duringsurgery.17 It will

bepossibletosaywhethertherewasalesioninthe oper-ated side or if a pre-existingsituation wasaggravated. A simple,six-stepevaluationbeforesurgeryoffersthe possi-bilityof identifyinglesionsand beingpreparedtomanage anyvestibularimpairments.

Conclusion

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severeimpairmentofthevestibularfunction,confirmedby thecalorictest.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

References

1.Ito J. Influence of the multichannel cochlear implant on vestibular function. Otolaryngol Head Neck Surg. 1998;118: 900---2.

2.Bittar RSM, Bottino MA, Pedalini MEB, Ramalho JRO, CarneiroCG.Arreflexia pós calórica bilateral:aplicabilidade clínica da reabilitac¸ão vestibular. Rev Bras Otorrinolaringol. 2004;70:188---93.

3.Vankatova L, Cao Van H, Perez Fornos A, Guinarnd N. Cochlearimplantation---bettersafethansorry.RevMedSuisse. 2014;10:1820---3.

4.JacotE,AbbeeleTVD,DebreHR,Wiener-VacherR.Vestibular impairmentspreand post-cochlearimplantinchildren.IntJ PedOtorhinolaryngol.2009;73:209---17.

5.MezzaliraR,BittarRSM,AlbertinoS.OtoneurologiaClínica.Rio deJaneiro:Revinter;2014.

6.BalohRW,HonrubiaV.Neurophysiologyofthevestibularsystem. NewYork:Oxford;2011.

7.HalmagyiGM,CurthoisIS.Aclinicalsignalofcanalparesis.Arch Neurol.1988;45:737---9.

8.GuidettiG,MonzaniD,CivieroN.Headshakingnystagmusinthe follow-upofpatientswithvestibulardiseases.ClinOtolaryngol. 2002;27:124---8.

9.KimMB,HuhSH,BanJH.Diversityofheadshakingnystagmus inperipheralvestibulardisease.OtolNeurotol.2012;33:634---9. 10.Rogers JH. Rombergand his test. JLaryngol Otol. 1980;94:

1401---4.

11.HongSK,ParkJH,KnonSY,KimJS,KooJW.Clinicalefficacyof theRombergtestusingafoampadtoidentifybalanceproblems: acomparativestudywiththesensoryorganizationtest.EurArch Otorhinolaryngol.2015;272:2741---7.

12.Fukuda T. Thestepping test: two phasesofthelabyrinthine reflex.ActaOtolaryngol.1959;50:95---108.

13.VibertD,LiardP,HäuslerR.Bilateralidiopathiclossof periph-eralvestibularfunctionwithnormalhearing.ActaOtolaryngol (Stockh).1995;115:611---5.

14.LanskaD,GoetzC.Romberg’ssign:development,adoption,and adaptationinthe19thcentury.Neurology.2000;55:1201---6. 15.Shumway-CookA, HorakF.Assessingtheinfluenceofsensory

interactionof balance.Suggestionfrom thefield.Phys Ther. 1986;66:1548---50.

16.FujimotoC,MurofushiT,ChiharaY,UshioM,SugasawaK, Yam-aguchi T, et al. Assessment of diagnostic accuracy of foam posturography forperipheral vestibulardisorders:analysisof parametersrelatedtovisual andsomatosensorydependence. ClinNeurophysiol.2009;120:1408---14.

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Table 1 List of assessed patients regarding gender, age and etiology of hearing loss.
Figure 1 Test using a foam pad.
Table 4 Significance of a positive Head Impulse Test (HIT) and absence of function (areflexia) of the assessed ears (Fisher’s exact test).

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