Effects of diabetes mellitus and systemic arterial hypertension on elderly patients' hearing,

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www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Effects

of

diabetes

mellitus

and

systemic

arterial

hypertension

on

elderly

patients’

hearing

夽,夽夽

Laurie

Penha

Rolim

a_,_∗

_,

_Alessandra

_Giannella

_Samelli

a

_,

_Renata

_Rodrigues

_Moreira

b

_,

Carla

Gentile

Matas

a

_,

_Itamar

_de

_Souza

_Santos

b

_,

_Isabela

_Martins

_Bensenor

b

_,

Paulo

Andrade

Lotufo

b

a_Universidade_de_São_Paulo_(USP),_Faculdade_de_Medicina_(FM),_Departamento_de_{Fisioterapia,}_{Fonoaudiologia}_e_Terapia Ocupacional,SãoPaulo,SP,Brazil

b_Universidade_de_São_Paulo_(USP),_Hospital_{Universitário}_(HU),_São_Paulo,_SP,_Brazil

Received4May2017;accepted30August2017 Availableonline21September2017

KEYWORDS Hearing; Diabetesmellitus; Systemicarterial hypertension; Hearingloss; Elderly Abstract

Introduction:Chronicdiseasescanactasanacceleratingfactorintheauditorysystem degen-eration.Studiesontheassociationbetween presbycusisanddiabetes mellitusandsystemic arterialhypertensionhaveshowncontroversialconclusions.

Objective:To compare theinitial audiometry (A1) with asubsequent audiometry(A2) per-formedaftera3to4-yearintervalinapopulationofelderlypatientswithdiabetesmellitus and/orsystemicarterialhypertension,toverifywhetherhearinglossinthesegroupsismore acceleratedwhencomparedtocontrolswithouttheseclinicalconditions.

Methods:100elderlyindividualsparticipatedinthisstudy.Fortheauditorythreshold assess-ment,apreviouscompleteaudiologicalevaluation(A1)andanewaudiologicalevaluation(A2) performed3---4yearsaftertheﬁrstonewasutilized.Theparticipantsweredividedintofour groups:20 individualsinthediabetes mellitusgroup,20 individualsinthesystemicarterial hypertensiongroup,20individualsinthediabetesmellitus/systemicarterialhypertensiongroup and40individualsinthecontrolgroup,matchingthemwitheachstudygroup,accordingtoage andgender.ANOVAandKruskal---Wallisstatisticaltestswereused,withasigniﬁcancelevelset at0.05.

夽 _Please_cite_this_article_as:_Rolim_LP,_Samelli_AG,_Moreira_RR,_Matas_CG,_Santos_IS,_Bensenor_IM,_et_al._Effects_of_diabetes_mellitus_and

systemicarterialhypertensiononelderlypatients’hearing.BrazJOtorhinolaryngol.2018;84:754---63.

夽夽_Study_carried_out_at_the_Curso_de_{Fonoaudiologia,}_Departamento_de_{Fisioterapia,}_{Fonoaudiologia}_e_Terapia_Ocupacional,_Faculdade_de

Medicina,UniversidadedeSãoPaulo(USP),SãoPaulo,SP,Brazil.

∗_{Corresponding}_author.

E-mail:[email protected](L.P.Rolim).

PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial. https://doi.org/10.1016/j.bjorl.2017.08.014

1808-8694/©2017AssociaçãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).

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Results:WhencomparingthemeanannualincreaseintheauditorythresholdsoftheA1withthe A2assessment,consideringeachstudygroupanditsrespectivecontrol,itcanbeobservedthat therewasnostatisticallysignificantdifferenceforanyofthefrequenciesforthediabetes mel-litusgroup;forthesystemicarterialhypertensiongroup,significantdifferenceswereobserved after 4kHz. For thediabetes mellitus andsystemic arterialhypertension group,significant differenceswereobservedatthefrequenciesof500,2kHz,3kHzand8kHz.

Conclusion: Itwasobservedthatthesystemicarterialhypertensiongroupshowedthegreatest decreaseinauditorythresholdsinthestudiedsegmentwhencomparedtotheothergroups, suggestingthatamongthethreestudiedconditions,hypertensionseemstohavethegreatest inﬂuenceonhearing.

© 2017 Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico-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 Audição; Diabetesmellitus; Hipertensãoarterial sistêmica; Perdaauditiva; Idoso

Efeitosdadiabetesmellitusehipertensãoarterialsistêmicasobreaaudic¸ãodeidosos

Resumo

Introdução: Doençascrônicaspodem atuarcomo fatordeaceleraçãonadegeneraçãodo sis-temaauditivo.Osestudossobreaassociaçãodapresbiacusiacomodiabetesmellitusecoma hipertensãoarterialsistêmicamostraramconclusõescontroversas.

Objetivo: Compararaaudiometriainicial(A1)comumaaudiometriasequencial(A2)feitacom umintervalodetrêsaquatroanosemumapopulaçãodeidososportadoresdediabetesmellitus e/ouhipertensãoarterialsistêmica,afimdesaberse aperdadeacuidadeauditivanesses gruposémaisaceleradacomparadacomcontrolessemessascondiçõesclínicas.

Método: Participaramdesteestudo 100idosos. Paraaanálisedos limiaresauditivos, foram usadas: umaavaliaçãoaudiológicacompleta feitaanteriormente(A1) eumanovaavaliação audiológica(A2)feitaapóstrêsaquatroanosdaprimeira.Osparticipantesforamdistribuídos em quatro grupos: 20 indivíduos no grupo comdiabetes mellitus, 20 nogrupo hipertensão arterialsistêmica,20nogrupodiabetesmellitus/hipertensãoarterialsistêmicae40indivíduos nogrupocontrole,forampareadoscomcadagrupodeestudo,deacordocomascaracterísticas referentesaidadeesexo.ForamusadosostestesestatísticosAnovaeKruskal-Wallis,comnível designificânciade0,05.

Resultados: Nacomparaçãodamédiadeaumentoanualdoslimiares auditivosdaavaliação A1 comaavaliaçãoA2,considerandocadagrupo estudoeseurespectivocontrole, pode-se observarqueparaogrupodiabetesmellitusnãohouvediferençaestatisticamentesignificante paraqualquerdasfrequências;paraogrupohipertensãoarterialsistêmicaforamobservadas diferençassignificantesapartirde4kHz.Jáparaogrupodiabetesmellitus/hipertensãoarterial sistêmicaforamobservadasdiferençassignificantesnasfrequênciasde500,2k,3ke8kHz. Conclusão:Verificou-sequeogrupohipertensãoarterialsistêmicafoioqueapresentoumaior quedados limiaresauditivos nosegmentoestudado, quandocomparadocomosoutros gru-pos,sugeriuqueentreastrêscondiçõesestudadasahipertensãopareceseraquetevemaior influênciasobreaaudição.

© 2017 Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico-Facial. Publicado por Elsevier Editora Ltda. Este é um artigo Open Access sob uma licença CC BY (http:// creativecommons.org/licenses/by/4.0/).

Introduction

Theagingoftheworld’spopulationiscurrentlyaworldwide phenomenon.Agingisrelatedtotheprocessofprogressive degenerationandcelldeath, whichleadstoadecreasein thebody’sfunctionalcapacity.1,2

The hearing lossresulting fromthedegenerative aging processesisknownaspresbycusis.3_It_is_currently_the_most

frequentsensoryimpairmentobservedintheelderly,with aprevalencerangingfrom25%inthe70---74agegroup,50%

intheelderlyagedupto85years,andgreaterthan80%in peopleover85yearsofage.4,5

Presbycusiscancauseareductioninspeechperception, psychologicalchanges(suchasdepression),socialisolation, problemsrelatedtoalertness anddefense(ability tohear automotive horns,telephone rings, alarms,etc.), as well ascognitivefunctions.5,6 _All_these_factors_have _a_negative

reﬂectontheelderly’squalityoflife.5---7

Despitethehighprevalenceofpresbycusis,someauthors haveshownthatthechronicdiseasesthatmostfrequently

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affect the elderly, such assystemic arterial hypertension (SAH)8---12_and_diabetes_mellitus_(DM)13---19_may_be_related_with

hearingimpairment.

DM is a metabolic disease that causes vascular complicationsandneurologicalimpairment.Thenumberof adults with diabetes worldwide increased from 108 mil-lionin1980to422 millionin2014.20 _ELSA-Brazil,_a_cohort

studyof15,105civilemployeesaged35---74years,founda prevalenceof 19.7%of diabetes.21 _Hearing _loss_in

individ-ualswithDMmayberelatedtodiabeticangiopathy,which interferes withthe supply of nutrientsandoxygen tothe cochlea,leadingtocellandtissuedeath.13,22---24_In_addition

tocochlearalterations,itisbelievedthatDMcancause sec-ondarydegenerationofeighthcranialnerveﬁbers,resulting inneuralhearingloss.13,23,25

Systemic arterial hypertension (SAH) is a multifacto-rial condition characterized by the presence of elevated blood pressure, associated with metabolic and hormonal changes and trophic phenomena (cardiac and vascular hypertrophy).26 _According _to_a _World _Health _Organization

studycarriedoutin2013,theprevalenceofSAHin adults olderthan25yearsofageisaround35%intheAmericas.27

TheaforementionedELSA-Brazilstudy,carriedoutin2015, identiﬁedaprevalenceof35.8%amongthe15,103assessed individuals.28_The_impairment_of_oxygen_and_nutrient

trans-port to the cells due to decreased capillary blood ﬂow areamongthepathogenicmechanismsofSAHthatmaybe involvedinhearingloss.29,30_High_blood_pressure_in_the

vas-cularsystemmayresultinbleedingintheinnerear,which mayleadtopermanenthearingloss.31 _SAH_can _also_cause

hearinglossduetoionicmodiﬁcationsincellpotentials.9

Therefore,despiteseveralstudiesonthistopic concern-ingbothDMandhypertension,thereisstillnoconsensusin theliterature about theassociation between these alter-ations and hearing loss, especially in elderly individuals.

The hypothesis of this study is that elderly hypertensive and/ordiabeticpatientsshowamorepronounced progres-sivehearingloss(duringa3-to-4-yearfollow-up)compared toindividualswithouttheseclinicalconditions.

Methods

The projectwasapprovedbytheEthicsCommitteeofthe institutionundernumber458.284.

Sample

TheELSA-Brazil(LongitudinalAdultHealthStudy)wasa mul-ticenter cohortstudyof 15,000employeesfromsixpublic institutionsofhighereducationandresearchinthe North-east, Southand Southeast regionsof Brazil. The research aimed to investigate the incidence and risk factors for chronic diseases, speciﬁcally cardiovascular diseases and diabetes. All active and retired staff and teachers aged 35---74wereeligibleforthestudy.32,33

Thisisanexcerptfromthelongitudinalhearingfollow-up study of the ELSA-Brazil participants34 ₍_Fig. ₁_). _One

hun-dredindividualsparticipatedinthisstudy.Fortheauditory threshold assessments, a previous complete audiological evaluation(A1)andanewaudiologicalevaluation(A2) per-formedafter3---4yearsaftertheﬁrstonewereutilized.The completeaudiologicalevaluationsconsistedof:anamnesis, meatoscopy,immittancemeasurements,puretone audiom-etryandspeechaudiometry.

The study inclusion criteria comprised the following: being60yearsofageorolder;absenceofexternal acous-tic meatus (EAC) obstruction in both ears; absence of alterationsinthemiddleeardemonstratedbyimmittance measurements;nohistoryofoccupationalexposuretonoise;

ELSA Brazil (N = 15,105) Investigation Center of the São Paulo (N = 5,000)

ELSA São Paulo - Hearing assessment (N = 901) Group AH (N = 20) Group DM (N = 20) Group DMAH (N = 20) Control Group (N = 40)

Figure1 Flowchartoftheselectionsteps.ELSA,LongitudinalAdultHealthStudy(EstudoLongitudinaldeSaúdedoAdulto);AH, arterialhypertension;DM,diabetesmellitus;DMAH,diabetesmellitusandarterialhypertension.a_Among_the₄₀_individuals_without

SAHorDM,foreachpairing(withtheAHgrouporwiththeDMgrouportheDMAHgroup),20‘‘healthy’’participantswerechosen, asdescribedintheDataAnalysisitem.

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havingacompleteinitialaudiologicalevaluation(A1), hav-ingdiabetesmellitusforinclusionintheDMgroup;having systemicarterialhypertensionforinclusionintheAHgroup; and DM associated with SAH for inclusion in the DM+AH group.

For inclusion in each of the groups, we relied on previous medical examinations performed in the same hospital. Diabetes was deﬁned as use of medication to treat diabetes; fasting glycemia≥126mg/dL, glycated hemoglobin(HbA1c)≥6.5%and/or2-houroral glucose tol-erancetest≥200mg/dL.Hypertension wasdeﬁned asuse of medication to treat hypertension; systolic blood pres-sure≥140mmHgordiastolicbloodpressure≥90mmHg.

Thus,accordingtothesecriteria,theparticipants com-prisedfour groups:20 individuals withDM(DMgroup), 20 individualswithSAH(AHgroup),20individualswithDMand SAH (DMAH group) and 40 individuals with no DM or SAH (controlgroup---CG).

Materialsandprocedures

After thesigning of the freeand informed consentform, thefollowing A2audiological assessment procedureswere performed: audiological anamnesis, meatoscopy, tympa-nometry with ipsilateral acoustic reﬂex assessment (the latter wasperformed only toverifythe presence of mid-dleearalteration)andtonalaudiometryatthefrequencies of 250---8000Hz and, if necessary, at the frequencies of 500---4000Hz(when airconduction hearing thresholdwere worse than 20dBHL).It is noteworthy that the A2 audio-logical assessment wasperformed 3---4 years after the A1 audiologicalassessment, followingthewaveperiodicityof theELSA-Brazilstudy.32,33

Dataanalysis

Tostudytheinﬂuenceofdiabetes,hypertensionordiabetes associated withhypertension in the evolution of auditory thresholds during the follow-up (3---4 years), participants withtheseclinicalconditionswerepairedina1:1ratiowith participantsofthesamegenderandage,inwhichthese clin-icalconditionswereabsent.Ateachpairing,20‘‘healthy’’ participantswereselectedfromamongthe40subjects with-out SAH or DM, previously described as‘‘control group’’, usingtheMatchfunctionofthestatisticalsoftwareR Match-ingpackage.Itwasestablishedthatgenderpairingshouldbe exactforeachparticipant,andthattheagepairingwould bechosenbythebestapproximationpossibleforthegroup. Asaresult,weobtainedaperfectpairingforthe distribu-tionbygender andquitesimilarmeans forage ineachof thegroupscomparedtotheircontrol(maximumdifference −0.25years),thusallowinganadequatepairing.

Tocomparetheauditorythresholds,sincenostatistically signiﬁcantdifferenceswereobservedbetweentheearsfor any of the studied groups, these were grouped. To com-paretheauditorythresholdsoftheﬁrstA1assessmentwith the second A2 assessment between the study groups and theirrespectivecontrol,weconsideredthemeanincrease inauditorythresholdsperyear(consideringthe3or4-year interval, depending onthe date of reassessment of each individual).

Table 1 Descriptive statistics and age comparison (in years)betweenthegroups.

Groups n Gender Meanage(SD) p-Value DM 20 12F/8M 64.05(6.08) 1.00 CGDM 20 12F/8M 64.15(5.89) AH 20 7F/13M 65.02(4.33) 0.88 CGAH 20 7F/13M 65(4.21) DMAH 20 11F/9M 64.25(6.35) 0.88 CGDMAH 20 11F/9M 64.5(6.37)

F,female;M,male;SD,standarddeviation;DM,diabetes melli-tus;AH,arterialhypertension;CG,controlgroup.

In the statistical analysis, in addition to the descrip-tivemeasures,weusedANOVAandKruskal---Wallisstatistical tests,withasigniﬁcancelevelof0.05.

Results

Table1showsthemeanageofparticipantsineachgroup. Itcanbeobservedthattherewasnostatisticallysigniﬁcant difference.Thedifferenceinmeanageforeachgroupand theirrespectivecontrolwasverylow(0.25yearsintheworst case).Thegroupswerealsopreciselypairedforgender.

RegardingtheageatdiagnosisofhypertensionandDM, intheDMgroup,themeanagewas61.75years.IntheAH group,themeanagewas52.65yearsandintheDMAHgroup, themeanageatDMdiagnosiswas58yearsandfortheSAH, itwas53.15years.Regardingthetimeofthepathology diag-nosis,intheDMgroupthemeannumberofyearswas6.1. IntheAHgroup,themeanwas16.6yearsandintheDMAH group,themeantimeofdiagnosis forDMwas10.05years andforSAH,14.09years.

Whencomparingthemeanauditorythresholdsatthefirst A1assessmentwiththesecondA2assessmentbetweenthe groups,consideringthemeanincreaseinauditorythresholds peryear,itcanbeobservedthattherewasnostatistically significant difference at any frequency for the DM group comparedtoitscontrolgroup(Fig.2);fortheAHgroup, sig-nificantdifferenceswereobservedat4kHz(p=0.016);6kHz (p=0.013),and8kHz(p=0.037)comparedtoitsCG,aswell asanon-significantdifferenceat3kHz(p=0.060)(Fig.3); fortheDMHAgroup,significantdifferenceswereobserved atthefrequenciesof500Hz(p=0.017),2kHz(p=0.021)and 3kHz(p<0.001)betweenthestudygroupanditscontrol,as wellasnon-significantdifferences at4kHz(p=0.058)and 6kHz(p=0.066)(Fig.4).

Discussion

Thestudyofconditionsthatmaypotentiallyinﬂuencethe evolutionofauditoryfunctionisimportant,sincetheearlier suchchangesaredetected,thegreaterthechancesof ben-eﬁcialhearingrehabilitation.Thus,theaimofthepresent study was to compare the initial audiometry (A1) with a subsequentaudiometry(A2)performedwithina3to4-year intervalinapopulationofelderlyindividualswithDMand/or SAH,toassesswhetherthelossofauditoryacuityinthese groups is more accelerated comparedto controls without theseclinicalconditions.Participants werepaired for age

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10 10 10 10 10 10 10 10 8 8 8 8 8 8 8 8 6 6 6 6 6 6 6 6 4 4 4 4 4 4 4 4 2 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 -2 -2 -2 -2 -2 -2 -2 -2 p=0.870 p=0.290 p=0.570 p=0.892 p=0.744 p=0.107 p=0.570 p=0.924

Mean db increase per y

ear (250Hz)

ear (1000Hz)

ear (3000Hz)

ear (6000Hz)

ear (8000Hz)

ear (4000Hz)

ear (2000Hz)

ear (500Hz) Control group Control group Control group Control group Control group Control group Control group Control group DM group DM group DM group DM group DM group DM group DM group DM group

Figure2 Comparisonofthemeanannualincreaseinauditorythresholds(indBHL)atfrequenciesfrom250Hzto8000Hzbetween A1andA2assessmentsfortheDMgroupanditsrespectivecontrol.

andgendertominimizetheeffectofthesevariablesonthis association.OurﬁndingsindicatedthattheAHgroupshowed thehighestdecreaseinthresholdsinthe3to4-year follow-up,followed by theDMAHgroup when comparedtotheir controlgroups.The DMgroupdidnotshowanysigniﬁcant differencesinrelationtoitscontrolgroup.

Some previous studies on the subject,11,16 _similar _to

the present study, sought to minimize the inﬂuence of thevariables ageand gender ontheresults of the audio-logical assessment, since it is known that thesevariables (mainlyage)canaffectauditorythresholds.35 _A_study

car-riedoutinIranevaluatedthehearingof50diabeticpatients and 50 healthy subjects, paired by gender and age, and

reportedthathearinglosswasmorepronouncedinthe dia-betesgroup,andspeechdiscriminationwasbetterinnormal individuals.Esparzaetal.11_compared_the_hearing_of

hyper-tensive andnon-hypertensiveindividualspaired bygender andage,withagesrangingfrom30to62years,and subdi-videdthesubjectsintotwogroups,thosewithandwithout SAH.Theauthorsobservedgreatercochleardysfunctionsin individuals withSAHand suggestedit might berelatedto vasculardiseasefromSAH.

When we compared the auditory thresholds from the ﬁrst A1assessment to thoseof the second A2assessment betweenthe studygroups andtheirrespectiveCGs,there was no statistically signiﬁcant difference in the mean

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ear (1000Hz)

ear (250Hz)

ear (2000Hz)

ear (4000Hz)

ear (3000Hz)

ear (6000Hz)

ear (8000Hz)

ear (500Hz) 15 15 15 15 15 15 15 15 10 10 10 10 10 10 10 10 5 5 5 5 5 5 5 5 0 0 0 0 0 0 0 0 -5 -5 -5 -5 -5 -5 -5 -5 -10 -10 -10 -10 -10 -10 -10 -10 p=0.903 p=0.586 p=0.597 p=0.060 p=0.013 p=0.037 p=0.016 p=0.797 Control group Control group Control group Control group Control group Control group Control group Control group Hyp group Hyp group Hyp group Hyp group Hyp group Hyp group Hyp group Hyp group

Figure3 Comparisonofthemeanannualincreaseinauditorythresholds(indBHL)atfrequenciesfrom250Hzto8000Hzbetween A1andA2assessments,fortheAHgroupanditsrespectivecontrol.

auditory threshold increase per year for any evaluated frequency inthe DMgroupcomparedtoitsrespectiveCG pairedforgenderandage.

Several authors have found a positive associa-tion between the presence of diabetes and auditory impairment,13,16,36 _while _others _have _not _veriﬁed _this

association.37,38 _Some _authors _have _suggested _that _this

controversy may be related to the presence of many confounding variables, as well as the complexity of the auditorysystem.34,39,40

We observed that some studies that investigated the effect of diabetes on hearing did not exclude some of

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ear (250Hz)

ear (1000Hz)

ear (3000Hz)

ear (6000Hz)

ear (8000Hz)

ear (4000Hz)

ear (2000Hz)

ear (500Hz) p=0.234 p=0.437 p<0.001 p=0.066 p=0.130 p=0.058 p=0.021 p=0.017 10 10 10 10 10 10 10 10 8 8 8 8 8 8 8 8 6 6 6 6 6 6 6 6 4 4 4 4 4 4 4 4 2 2 2 2 2 2 2 2 0 0 0 0 0 0 0 0 -2 -2 -2 -2 -2 -2 -2 -2 -4 -4 -4 -4 -4 -4 -4 -4 Control group Control group Control group Control group Control group Control group Control group Control group DM+Hyp group DM+Hyp group DM+Hyp group DM+Hyp group DM+Hyp group DM+Hyp group DM+Hyp group DM+Hyp group

Figure4 Comparisonofthemeanannualincrease inauditorythresholds(indBHL)atthefrequenciesfrom250Hzto8000Hz betweentheA1andA2assessments,fortheDMAHgroupanditsrespectivecontrol.

the confounding factors, such as: gender,40---42 _age,41 _and

presenceofarterialhypertension,35,39_which_may_have

inﬂu-encedtheobservedresults.Samellietal.34_assessed_hearing

in191diabeticand710non-diabeticindividuals,adultsand elderlyfromELSA-Brazilstudy(SãoPaulo);theauthorsdid

notﬁndanystatisticallysigniﬁcantdifferencesbetweenthe auditory thresholds ofthe twogroups, afteradjustingfor age,genderandpresenceofhypertension,suggestingthat thesefactorsshouldbeconsideredinstudiesofthiskind.It is noteworthy that this study assessed cross-sectional

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data, while the present study used longitudinal data.

RegardingtheAHgroup,considering themeanincrease inauditorythresholdsperyear,significantdifferenceswere observedafter4kHz,whenthisgroupwascomparedtoits CG, aswell asa trendtoa statistically significant differ-enceat 3kHz. Therefore,we observedthat theAH group hadsignificantlyworseauditorythresholdscomparedto non-hypertensiveindividualspairedbygenderandage.

These ﬁndings agreewith previous studies, which also veriﬁed more impaired auditory thresholds in individ-uals with SAH when compared to controls without this disease8,9,12_and_disagree_with_the_studies_of_Rey_et_al.43_and

Baraldietal.,44_which_did_not_observe_such_association.

RegardingtheDMAHgroup,significantdifferenceswere observedat thefrequencies of500,2kHzand3kHz when compared toits control, as well as a trend to a statisti-cally significant difference at 4kHz and 6kHz, indicating a significantly higher annual increase in auditory thresh-oldsat thesefrequenciesintheDMAHgroup.Studies that evaluated hearing in diabetic and hypertensive individ-uals obtained controversial results: Jorgensen and Buch22

didnot observeany inﬂuence of these variableson hear-ing, whereas Duck et al.45 _found _such _association. _Oron

et al.46 _also _observed _that _{cardiovascular} _risk _factors

(including diabetes and hypertension) seem to have an effectonhearing,althoughtherewasnodirectandcausal correlation.

Ifweanalyzetheincreaseinauditorythresholdsduring thestudyperiodinthethreegroups, wecanobservethat theDMgroup,whencomparedtoitscontrol,didnotshow thresholdworsening;theAHGroup,whencomparedtoits control,showed higherthresholdsat the highfrequencies andtheDMAHGroup,comparedtoitscontrol,showedworse thresholdsforlow,mediumandhighfrequencies. Addition-ally,whencomparingtheevolutionofthethreestudygroups (DM,AHandDMAH),itwasobservedthatthemeanannual increase ishigherin theAHgroup, followedby theDMAH and,ﬁnally,theDMgroup.

Oneofthehypothesesforthisﬁndingcouldberelatedto thelongerdurationofthediseaseintheAHgroup.However, itisimportanttonotethatDMandSAHarediseasesthatmay beasymptomaticand,therefore,thetimeofdiseaseonset maybelongerthanthatreported.47

Somestudieshaveinvestigatedtheinﬂuenceofdisease duration on hearing threshold worsening. Regarding arte-rial hypertension,Esparza et al.11 _studied _a_group _with _a

meandiseasediagnosisof4yearsand,evenwiththatshort time since the onset of disease, when compared to the present study they observed cochlear dysfunction in the individuals with SAH. Agarwal et al.48 _evaluated _distinct

groups, divided into three different degreesof hyperten-sion(bypressurelevel);themeandurationof thedisease was 3.7 years for Grade 1 Group; 5.4 years for Grade 2 Group and 9.0 years for Grade 3 Group, with the latter groupshowing theworst auditory thresholds.It shouldbe emphasized that the difference in time of hypertension durationobserved in thedifferentstudies couldinﬂuence the audiological results if we consider this pathology can cause microcirculatory insufﬁciency, which may result in greater or lesser deterioration of the peripheral auditory system.49,50

InrelationtoDM,SunkumandPingile19 _and_Özel_et_al.41

foundapositiveassociationbetweendiabetesdurationand hearing loss, while Akinpelu et al.35 _did _not _ﬁnd _a

sta-tisticallysignificant associationbetweendiabetesduration anddiseaseprogression. However,thestudiedpopulation, themethodsemployedanddiseasedurationvariedwidely between the different studies, which may influence the observed results and explain these contrasting findings. Thus, this association between hearing loss and diabetes durationremainscontroversial.41

As previously mentioned, the groups studied in the present investigation differed with respect to the time sincediagnosis(AH,DMandDMAH).However,ourobjective wasnot to correlate disease duration with auditory acu-ityworsening, butrathertoverify,in thestudy follow-up period,whichpathologywouldhavethegreatestinﬂuence onauditory thresholds. It should be emphasized that, to establishacorrelationbetweentimeofdiagnosisand hear-ing threshold worsening, another study design would be necessary,forinstance, bycomparingtheauditory thresh-oldsofgroupswithdifferentdiseasedurationandanalyzing whether the auditory threshold worsening occurred non-linearly.

However,wecannotignorethepossibleinﬂuenceof dis-easeduration,since,inthepresentstudy,weobservedthat in the study group with a longer disease duration, wors-eningof theauditory thresholds wasmoreevident during thefollow-upandthatthehearingthresholdsincreasedin hypertensiveindividualsatahigherratethaninthecontrol group,even16yearsafterdiagnosis.

Studylimitationsandpotentials

Itisimportanttonote thatthesample sizeofeach study group was small and, perhaps, if comparisons were per-formed with larger groups, the differences between the auditorythresholdscouldbemoreevident.However,inthe assessedagerangeitisdifﬁculttoﬁndindividualsthathave onlytheassessedclinicalconditions(DMand/orSAH).

Additionally,itisimportanttoobservethatthe progres-sion of auditory thresholds was measured linearly over a givenperiodoftime,withoutcorrelatinghearinglosswith diseaseduration,whichwouldalsorequirealargersample. Itisnoteworthythatthepresentstudyperformeda com-pleteauditoryevaluation,aswellasclinicalandbloodtests, whichgives theﬁndings a greater precision regardingthe inclusionofindividualswithAHand/orDM.

Conclusion

Itwasobservedthat,whencomparingtheinitialandfinal audiologicalassessments,themeanannualincreasein audi-torythresholdswashigherintheAHgroup,followedbythe DMAHand,finally,bytheDMgroup,suggestingthatamong thestudiedconditions,arterialhypertensionseemsbethe onethathadthegreatestinfluenceonhearing.Regarding themostaffectedfrequencies,itwasobservedthat,forthe AHgroup,thehighestfrequenciesweremostoftenaffected, whilefortheDMAHgroupmediumandhighfrequencieswere themostaffectedones.

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Funding

Fundac¸ãodeAmparoà PesquisadoEstadodeSãoPaulo ---FAPESP,processnumber2013/05589-2.

Conﬂicts

of

interest

Theauthorsdeclarenoconﬂictsofinterest.

References

1.Paskulin LMG, Valer DB, Vianna LAC. Utilização eacesso de idososaserviçosdeatençãobásicaemPortoAlegre(RS,Brasil). CienSaudeColet.2011;16:2935---44.

2.FontaineR.Psicologiadoenvelhecimento,vol.1.Climepsi Edi-tores;2000.p.1---200.

3.GacekMR,SchuknechtHF.Pathologyofpresbycusis.IntJAudiol. 1969;8:199---209.

4.KoopmannCF.Problemasotolaringológicosnoidoso.MedClinN Am.1991;6:1411---27.

5.ZhangM,GomaaN,HoA.Presbycusis:acriticalissueinour com-munity.IntJOtorhinolaryngolHeadNeckSurg.2013;2:111---20. 6.KricosPB,LesnerAS.Hearingcare forolderadultaudiologic rehabilitation,vol.1.Butterworth-Heinemann;1995.p.1---282. 7.ViudeA.Fatoresassociadosapresbiacusiaemidosos[tese].São Paulo:UniversidadedeSãoPaulo,FaculdadedeSaúdePública; 2002.

8.Marková M. Thecocheovestibular syndrome in hypertension. CeskOtolaryngol.1990;39:89---97.

9.Brohen VM,Caovilla HH, Gananc¸a MM. Dossintomase acha-dosaudiológicosevestibularesemindivíduoscomhipertensão arterial.ActaAwho.1996;15:4---10.

10.Marchiori LLM, Rego EA, Matsuo T. Hipertensão como fator associado à perda auditiva. Braz J Otorhinolaryngol. 2006;72:533---40.

11.Esparza CM, Jáuregui-Renaud K, Morelos CMC, Muhl GEA, MendezMN,CarilloNS,etal.Systemichighbloodpressureand innerear dysfunction: a preliminary study. ClinOtolaryngol. 2007;32:173---8.

12.RolimLP,RabeloCM,LoboIFN,MoreiraRR,SamelliAG. Inter-actionbetweendiabetesmellitusandhypertensiononhearing ofelderly.Codas.2015;27:428---32.

13.MaiaCAS,CamposCAH.DiabetesMellituscomocausadeperda auditiva.BrazJOtorhinolaryngol.2005;71:208---14.

14.BainbridgeKE,HoffmanHJ,Cowie CC.Diabetes andhearing impairmentin theUnitedStates: audiometric evidencefrom theNationalHealthandNutritionExaminationSurveys,1999to 2004.AnnInternMed.2008;149:1---10.

15.DinizTH,GuidaHL.Perdasauditivasempacientesportadores dediabetesmelito.BrazJOtorhinolaryngol.2009;75:573---8. 16.AgarwalA,BalakrishnanR, PujaryK, GanapathyK,Nayak D,

HasanF.Pure toneaudiometryandotoacousticemissionsfor theassessment ofhearinglossin diabeticpatients.Indian J Otolaryngol.2013;19:13---7.

17.KiakojouriK,MonadiM,SheikhzadehM,TaghinejadOmran P, BayaniMA,KhafriS.Investigationofauditorythresholdsintype 2diabeticpatientscomparedtonon-diabeticcases.CaspianJ InternMed.2014;5:99---102.

18.OhI-H,LeeJH,ParkDC,KimM,ChungJH,KimSH,etal. Hear-inglossasafunction ofaginganddiabetesmellitus:a cross sectionalstudy.PLOSONE.2014;9:e116161.

19.Sunkum JK, Pingile S. A clinical study of audiological pro-ﬁle indiabetesmellituspatients. EurArchOtorhinolaryngol. 2013;270:875---9.

20.NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in diabetes since 1980: a pooled analysis of 751

population-basedstudieswith4.4millionparticipants.Lancet. 2016;387:1513---30.

21.Schmidt MI, Hoffmann JF, Diniz MFS, Lotufo PA, Griep RH, BensenorIM,etal.Highprevalenceofdiabetesand interme-diatehyperglycemia---theBrazilianLongitudinalStudyofAdult Health(ELSA-Brasil).DiabetolMetabSyndr.2014;6:1---9. 22.JorgensenMB,BuchNH.Studiesoninner-earandcranialnerves

indiabetes.ActaOtolaryngol.1961;107:179---82.

23.Makishima K, Tanaka AK. Pathological changes of the inner earandcentralauditorypathwayindiabetes.AnnOtolRhinol Laryngol.1971;80:218---28.

24.FukushimaH,CureogluS,SchachernPA,KusunokiT,OktayMF, FukushimaN,etal.Cochlearchangesinpatientswithtype1 dia-betesmellitus.OtolaryngolHeadNeckSurg.2005;133:100---6. 25.FriedmanSA,SchulmanRH,WeissS.Hearinganddiabetic

neu-ropathy.ArchInternMed.1975;135:573---6.

26.Andrade JP, Nobre F, Tavares A, Brandão AA, Sanjuliani AF, Nogueira AR, et al. Sociedade Brasileira de Cardiolo-gia/SociedadeBrasileira de Hipertensão/SociedadeBrasileira deNefrologia.VIDiretrizesBrasileirasdeHipertensão.ArqBras Cardiol.2010;95Suppl.1:1---51.

27.World Health Organization. A global brief on hypertension. Silentkiller,globalpublichealthcrisis:WorldHealthDay,vol. 1;2013.p.1---40.

28.ChorD,RibeiroAL,CarvalhoMS,DuncanBB,LotufoPA,Nobre AA,etal.Prevalence,awareness,treatmentandinﬂuenceof socioeconomic variables on control of high blood pressure: resultsoftheELSA-Brasilstudy.PLOSONE.2015;10:e0127382. 29.ChenYL,DingYP.Relationshipbetweenhypertensionand

hear-ingdisordersintheelderly.EastAfrMedJ.1999;76:344---7. 30.KearneyPM,WheltonM,ReynoldsK,MuntnerP,WheltonPK,He

J.Globalburdenofhypertension:analysisofworldwidedata. Lancet.2005;365:217---23.

31.BachorE,SeligYK,JahnkeK,RettingerG,KaemodyCS.Vascular variationsofinnerear.ActaOtolaryngol.2001;121:35---41. 32.Aquino EML, Barreto SM, Bensenor IM, Carvalho MS, Chor

D, Duncan BB, et al. Brazilian Longitudinal Study of Adult health(ELSA-Brasil): objectivesand design. AmJEpidemiol. 2012;175:315---24.

33.SchmidtMI,DuncanBB,MillJG,LotufoPA,ChorD,BarretoSM, etal.Cohortproﬁle:LongitudinalStudyofAdultHealth (ELSA-Brasil).IntJEpidemiol.2015;44:68---75.

34.Samelli AG, Santos IS, Moreira RR, Rabelo CM, Rolim LP, BensenõrIJ,etal.Diabetesmellitusandsensorineuralhearing loss: is there an association? Baseline of the Brazilian Lon-gitudinal Study of Adult Health (ELSA-Brasil). Clinics. 2017; 72:5---10.

35.AkinpeluOV,Mujica-MotaM,DanielSJ.Istype2diabetes melli-tusassociatedwithalterationsinhearing?Asystematicreview andmetaanalysis.Laryngoscope.2014;124:767---76.

36.Espa˜naAR,BirrunO,Lorente J,TrasseraJ.Hearing and dia-betes.ORLJOtorhinolaryngolRelatSpec.1995;57:325---7. 37.DaltonDS,CruickshanksKJ,KleinR,KleinBE,WileyTL.

Asso-ciation of NIDDM and hearing loss. Diabetes Care. 1998;21: 1540---4.

38.AsmaA, AzmiMN,MazitaA,MarinaMB,SalinaH,NorlailaM. A Single blinded randomized controlled study of the effect of conventional oral hypoglycemic agents versus intensive short-terminsulintherapyonpuretoneaudiometryintypeII diabetesmellitus.IndianJOtolaryngolHeadNeckSurg.2011; 63:114---8.

39.HorikawaC,KodamaS,TanakaS,FujiharaK,HirasawaR,Yachi Y,etal.Diabetesandriskofhearingimpairmentinadults:a meta-analysis.JClinEndocrinolMetab.2013;98:51---8. 40.VigneshSS,JayaV,MosesA,MuraleedharanA.Identifyingearly

onsetofhearinglossinyoungadultswithdiabetesmellitustype 2usinghighfrequencyaudiometry.IndianJOtolaryngolHead NeckSurg.2015;67:234---7.

(10)

41.Özel HE, Özkiri M, Gencer ZK, Saydam L. Audiovestibu-larfunctionsinnoninsulin-dependentdiabetesmellitus. Acta Otolaryngol.2014;134:51---7.

42.KakarlapudiV,SawyerR,StaeckerH.Theeffectofdiabeteson sensorineuralhearingloss.OtolNeurotol.2003;24:382---6. 43.Rey JF, Morello-Castro G, Curto JLB. Factores de riesco

involucrados em la presbiacusia. Acta Otorrinolaringol Esp. 2002;53:572---7.

44.BaraldiGS,AlmeidaLC,BorgesACLC.Perdaauditivae hiperten-são:achadosemumgrupodeidosos.BrazJOtorhinolaryngol. 2004;70:640---4.

45.Duck SW, Prazma J, Bennett PS, Pillsbury HC. Interac-tion between hypertension and diabetes mellitus in the pathogenesis of sensorineural hearing loss. Laryngoscope. 1997;107:1596---605.

46.Oron Y, Elgart K, Marom T, Roth Y. Cardiovascular risk fac-tors as causes for hearing impairment. Audiol Neurootol. 2014;19:256---60.

47.SchmidtMI,DuncanBB,HoffmannIJF,MouraL,MaltaDC, Car-valhoRMAV.PrevalênciadediabetesehipertensãonoBrasil. RevSaudePublica.2009;43:74---82.

48.AgarwarlS,MishraA,JagadeM,KasbekarV,NagleSK.Effectsof hypertensiononhearing.IndianJOtolaryngolHeadNeckSurg. 2013;65:614---8.

49.Carrasco VN, Prazma J, Faber JE. Cochlear microcircula-tioneffectofadrenergicagonistsonarteriolediameter.Arch OtolaryngolHeadNeckSurg.1990;116:411---7.

50.SoaresMA.Perﬁlaudiológicodeadultoscomesemhipertensão arterial[dissertac¸ão].SãoPaulo: Universidade deSão Paulo, FaculdadedeMedicina;2014.