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w w w . e l s e v ie r . c o m / l o c a t e / b j i d

The

Brazilian

Journal

of

INFECTIOUS

DISEASES

Original

article

HIV

testing

and

HIV

knowledge

among

men

who

have

sex

with

men

in

Natal,

Northeast

Brazil

Monica

Baumgardt

Bay

a,∗

,

Marise

Reis

de

Freitas

a

,

Marcia

Cavalcante

Vinhas

Lucas

b

,

Elizabeth

Cristina

Fagundes

de

Souza

b

,

Angelo

Giuseppe

Roncalli

b

aUniversidadeFederaldoRioGrandedoNorte,DepartamentodeDoenc¸asInfecciosas,Natal,RN,Brazil

bUniversidadeFederaldoRioGrandedoNorte,Natal,RN,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received15August2018 Accepted13January2019 Availableonline10February2019

Keywords:

HIVtesting

Menwhohavesexwithmen(MSM) HIVknowledge

a

b

s

t

r

a

c

t

Background:Menwhohavesexwithmen(MSM)accountforthehighestprevalenceofHIV

inBrazil.HIVtestingallowstoimplementpreventivemeasures,reducestransmission, mor-bidity,andmortality.

Methods:Weconductedacross-sectionalstudytoevaluateHIVtestingduringlifetime,

fac-torsassociatedwiththedecisiontotest,knowledgeaboutHIVtransmission,anduseof condomsbetweenMSMfromthecityofNatal,northeastBrazil.

Results:Outof99participants,62.6%hadbeentestedforHIVduringlifetime,46.2%inthelast

year.ThemostfrequentreportedreasontobetestedforHIVinfectionwascuriosity(35.5%). CorrectknowledgeaboutHIVwasobservedinonly9.2%ofparticipants.Inmultivariate analysis,age(PR0.95;95%CI,0.91–0.99;p=0.041)andprevioussyphilistest(PR4.21;95%CI, 1.52–11.70;p=0.006)wereassociatedwithHIVtesting.

Conclusions:ThefrequencyofHIVtestingamongMSMfromNatalisratherlow,especially

inyoungerMSM,andknowledgeaboutHIVtransmissionisinappropriate.

©2019SociedadeBrasileiradeInfectologia.PublishedbyElsevierEspa ˜na,S.L.U.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/ licenses/by-nc-nd/4.0/).

Introduction

TheoverallprevalenceofHIVinfectioninBrazilisestimated at0.4%,butthe epidemicishighlyconcentratedin vulner-ablepopulations, with5.3%prevalenceamongsexworkers and19.8%inmenwhohavesexwithmen(MSM)accordingto thelastreports.1ThehigherriskofHIVinfectionamongMSM

Correspondingauthor.

E-mailaddress:monibay@gmail.com(M.B.Bay).

maybepartlyexplainedbythepracticesandbehaviors associ-atedwithanalsexandtheguttropismofHIV.2,3Besidesthat,

behavioralvulnerabilitiesacttogetherincreasingthechances ofHIVinfectionbetweenMSM,suchasnocondomuse, prac-ticeoftransactionalsex,useofdrugsduringsex,andsexwith casualpartners.4

In 2015, the Joint United Nations Program on HIV/AIDS (UNAIDS) proposedthat by2020,90% ofpeoplelivingwith HIVshouldbeawareoftheirHIVstatus,asthefirstpartof 90-90-90strategytoendAIDSepidemic.5 Earlydetectionof

HIVallowsinitiatingcareforpropertreatment,whichimpacts inmorbidity,mortality,andreducesfurthertransmission.2In

https://doi.org/10.1016/j.bjid.2019.01.003

1413-8670/©2019SociedadeBrasileiradeInfectologia.PublishedbyElsevierEspa ˜na,S.L.U.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

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Brazil,HIVtestingisrecommendedforallpregnantwomen andpatientswithdiagnosisoftuberculosis,visceral leishma-niasis,orsexuallytransmittedinfections.6Studiesestimated

thatthedelaybetweeninfectionandfirstCD4countinBrazil was4.3years,showingthatalargeproportionofindividuals stillstartedtreatmentlateinthecountry.7InNortheastBrazil

8800newcasesofAIDSaredetectedperyearandinNatalthe meanCD4countatdiagnosisis269cells/mm3,pointingtolate

diagnosisofHIV.1

Although the group of MSM accounts for the highest prevalenceofHIVinthecountry,thereisnospecific recom-mendationforHIVtestinginthispopulationinBrazil.6Data availablefromdevelopedcountriesshowthattheproportion ofMSMnevertestingforHIVisgenerallybelow30%.8,9Since

fewstudiesevaluatedHIVtestingamongMSMinBrazil, espe-ciallyinNortheastregion,ourstudyaimedtoaccesstherate and factors associated withHIV testing among MSM from Natalcity,NortheastBrazil.

Materials

and

methods

Studydesign

Thisisacross-sectionalstudy,conductedinthecityofNatal, betweenAugust2011andDecember2012.Theprimary objec-tivewastoevaluatepreviousHIVtestingamongMSMfrom Natalduringlifetime.Basedonpreviousstudiesweanticipate thatyoungerage andlower educationwould beassociated withlackoftesting,10,11

Studysample

Participantswere MSMaged18 yearsold ormore,residing orworkinginNatal.Theywererecruitedusing respondent-driven sampling (RDS) approach initially.12 Six MSM were

selected asinitial seeds, chosenthrough focus group. The focusgroupwasconductedwith15MSMrepresentativesof artisticscene,student activismand socialmovement from Natal,theinitialseedswereselectedconsideringdemographic characteristics,likeageandsocioeconomicstatus,and net-worksize.Eachseedwasallowedtorecruitthreeparticipants, usingstudycouponspre-printedwiththestudycenterphone numberandlocation.Staffscreenedsubjectsinthestudysite forthefollowingeligibilitycriteria:ageover18years,livingor workinginthecityofNatal,andhavingengagedinanal inter-coursewithanothermaninthepreviousyear.Eachincluded participantreceivedthreecouponstoinvitemorepeoplefor thestudy.

Procedures

Thestudywasconductedatahealthcarefacilityinsidethe university. The study questionnaire consisted of objective questionstobeself-administeredandbasedonabehavioral instrumentusedpreviouslywiththispopulationinBrazil.13

Participantsrespondedto thequestions ina privateoffice. Questions included socioeconomic and demographic char-acteristics,historyofHIVtesting,reasonstodothetest,use ofcondominthelast sexualrelation,HIVstatus ofsexual

partners,transactionalsex,previoussyphilistest,knowledge ofplaceswere HIVtesting isfree,andadequateknowledge about HIVprevention,according toUnitedNations General AssemblySpecial Sessionon HIV/AIDS(UNGASS)indicator, defined as the percentage of respondents giving correct answerstoallthefollowingfivequestions14:

Canhavingsexwithonlyonefaithful,uninfectedpartner reducetheriskofHIVtransmission?(yes);

Can usingcondoms reducethe riskof HIVtransmission? (yes);

Canahealthy-lookingpersonhaveHIV?(yes) CanapersongetHIVbyusingpublictoilets?(no)

CanapersongetHIVbysharingamealwithsomeonewho isinfected?(no)

A rapid test for HIV using hole blood was offered for the participantsat study site (Rapid Check HIV-1/2 and/or Bio-ManguinhosHIV-1/2),withpre-andpost-testcounseling andtheresultwasgivenimmediately,accordingtoBrazilian guidelines.15

Statisticalanalysis

Sample size was calculated tobe 95 subjects, assuming a prevalenceof60% forprevious HIVtesting duringlifetime, 95%confidenceanda10%error,basedonpreviousdatafrom Adam et al. for 10 countries in Latin America.16

Descrip-tiveanalysisincludedcentraltendencymeasurescalculated forcontinuousvariablesandproportionswerecalculatedfor categoricalvariables.TheassociationbetweenpreviousHIV testingandexplanatoryvariableswasassessedbyunivariate analysisusingPearson’sChi-squareorFischerexacttestwhen appropriate.Forcontinuousvariables,Student’s“t”testwas performed. Associationswithap-valueless than0.05were consideredsignificant.Inordertoverifytheadjustedeffect, PoissonRegressionModelingwithrobustvariancewere per-formed,includingthosevariableswithp-valueslessthan0.2. DatawereanalyzedusingSPSS(StatisticalPackageSoftware forSocialScience)version20.0.

Ethics

ThestudywasapprovedbytheEthicResearchCommitteeof FederalUniversityofRioGrandedoNorte(number136/11).All participantssignedawritteninformedconsent.

Results

By November 2012, 70 subjects were included using RDS, despitemany effortsofthestudy teamtoimprove recruit-ment, including increase in the hours of operation of the studysiteandaddingsixmoreseeds.Asourplanedsample was95MSM,wedecidedtoincludeavenue-basedsampleof additional31subjectsrecruitedduringthegayprideeventin NatalcityinDecember2012.From101participants,twowere excludedbecausetheyansweredlessthan70%ofthe ques-tionnaire,totalingasampleof99subjects.Sociodemographic characteristicsofparticipantsareshowninTable1.Themean

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Table1–Sociodemographiccharacteristicsof99MSM fromNatal.

Variables Mean/n SD/%

Age(years) 29.1 9.7

Yearsofstudy 11.5 2.2

Monthincome(USdollars) 494 465

Race White 25 27.5 Mulatto/black 66 72.5 Occupation Employed 62 62.6 Unemployed 37 37.4

Useofcondominlastanalsex

Yes 68 71.9

No 27 28.1

PreviousHIVtest

Yes 62 62.6

No 37 37.4

Previoussyphilistest

Yes 34 35.4

No 62 64.6

HIVtestinthestudy

Positive 6 9.2

Negative 59 90.8

KnowwheretotestforHIVforfree

Yes 72 73.5

No 26 26.5

Table2–ReasonforhavingdoneHIVtestamongMSM.

Reason n %

Curiosity 22 35.5

SelfperceptiontobeatriskforHIVinfection 11 17.7

Medicalrecommendation 10 16.2

Blooddonation 7 11.3

Requestedatwork 6 9.7

Partnerwish 3 4.8

Total 62 100

agewas29.1years(SD9.7years),73.3%identifiedthemselves asmulattoorblack,meanmonthlyincomewas494USdollars (SD465dollars),and61.5%wereemployed.Participantshada meanof11.5yearsofschooling(SD2.2years).

Outof99participants,62.6%(CI95%52.5–71.7%)hadbeen testedforHIV,46.2%(CI35.5–57%)inthelastyear.Themost

frequent reason to be tested was curiosity (35.5%), 17.7%

because they perceived themselves to be at risk for HIV

infection,and16.2%wereaskedtobetestedbyahealth pro-fessional(Table2).Themostfrequentplacefortestingwas publicservicesmentionedby52.4%(Table3).Only9.2%of par-ticipantshad adequate knowledgeaboutHIVtransmission. Thequestionswiththehighestpercentagesofwronganswers were“CanapersongetHIVbysharingamealwithsomeone whoisinfected?”(66.7%marked‘yes’)and“Canapersonget HIVbyusingpublictoilets?”(22.9%marked‘yes’)[Table4].

Transactionalsexwas frequent,as42% reported having received money in exchange for sex in the previous six months. Use of condom in the last anal intercourse was

Table3–PlacesofHIVtestingreportedbyMSM.

Places n % Publicservice 32 51.6 Bloodbank 6 9.7 Privateservice 11 17.7 Workplace 5 8.1 Other 8 12.9 Total 62 100

mentionedby71.9%.Only13.1%wereawareoftheHIVstatus ofsexualpartners.Ofthe63MSMwhoagreedtoperforman HIVtest,sixturnedoutpositive(9.5%)[Table1].

In univariate analysis, age (PR 0.93; 95% CI, 0.88–0.97;

p<0.001)andprevioussyphilistest(PR1.85;95%CI,1.41–2.44;

p<0.001)wereassociatedwithHIVtesting.Knowingaplace wheretheHIVtestcouldbedonefree-of-chargewasalso asso-ciatedwithHIVtesting(PR1.69;95%CI,1.05–2.71;p=0.017),as mostMSMdidthetestinpublicservices(Table5).Inadjusted analysis,resultedfromPoissonmodeling,thevariables“age”, “previous syphilistest”,and “knowing whereHIVtest was free”whereincludedinastepwiselogisticregressionanalysis. Inthefinalpredictivemodelonly“age”and“previoussyphilis test” remainedindependentlyassociatedwithpreviousHIV testing(Table5).

Discussion

Ourstudyfoundthat62.6%ofMSMfromNatalhadbeentested forHIVbefore.Thisratewashigherthanthenational aver-age of 37% estimatedfor the generalpopulation in 201113

andthe51.6%foundbyBritoetal.inMSMfrom10Brazilian citiesin2009.10TheseratesareratherdisappointingasMSM

isagroupwithahighprevalenceofHIVinfection.TheWorld HealthorganizationandtheCentersforDiseaseControland Prevention(CDC)inUnitedStates,recommendthatpersons athighriskforHIVinfectionshouldbescreenedforHIVat leastannually.17,18Itshouldbepointedoutthattestingatany

timewasaccountedfor,ratherthanbeingrestrictedtothelast year.Ifonlytestinginthepreviousyearwereconsideredthe ratewouldbeevenlower(46.2%).Previousstudiesconducted inArgentina,Peru,andChinashowedHIVtestingrates vary-ingbetween48%and58%,9,11,19butstudiesfromUnitedStates

andPuertoRicohadamuchbetterresult(82–90%).20,21

LackofknowledgeaboutHIVtransmissionisoneofthe rea-sonsthatleadtolowperceivedriskofbeinginfected.Halletal. foundthat testingwas higheramonghigh schoolstudents iftheyweretaughtatschoolaboutAIDSorHIV.22Although

adequateknowledgeaboutHIVtransmissionwasnot signif-icantlyassociatedwithHIVtesting,itisnoteworthythelow levelofknowledge,despitethehigheducationallevel.The per-centageofadequateknowledgeinastudywiththeBrazilian generalpopulationwas muchhigher,reaching57.1%,13 but

Guimarãesetal.indicateadecreaseintheproportionofMSM withadequate HIVknowledgefrom 35.2%in2009to23.7% in2016.23 Campaignscarried outbythe MinistryofHealth

inBrazilhavefocusedprimarilyoncondomuseasawayto avoidHIVinfection,leavingasideclarificationonsituations thathavenoriskoftransmission,suchassharingamealor

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Table4–KnowledgeaboutHIVbyMSMfromNatalcity,Brazil,2012.

Question n %

CanapersongetHIVbyusingpublictoilets?

Yes 22 22.9

No 57 59.4

Don’tknow 17 17.7

Total 96 100

Canhavingsexwithonlyonefaithful,uninfectedpartnerreducetheriskofHIVtransmission?

Yes 78 78.8

No 16 16.2

Don’tknow 5 5.1

Total 99 100

Canahealthy-lookingpersonhaveHIV?

Yes 94 94.9

No 2 2.0

Don’tknow 3 3.0

Total 99 100

CanusingcondomsreducetheriskofHIVtransmission?

Yes 96 97.0

No 2 2.0

Don’tknow 1 1.0

Total 99 100

CanapersongetHIVbysharingamealwithsomeonewhoisinfected?

Yes 66 66.7

No 17 17.2

Don’tknow 16 16.2

Total 99 100

useofpublictoilets.Inourcountry,AIDSisstillatopicrarely addressedinschools,andevenwhenthisapproachiscarried out,itisusuallynotsystematic.Theschoolisoftentheonly placewhereyoungpeoplecanreceive reliableinformation. However,mostoftenschoolteachersareNOTwellprepared, andmayendupdeliveringincompleteinformation. Alterna-tiveinterventionslikepeereducationandinternetandsocial mediastrategiestoaccessMSMhaveproventobeusefulin studiesfromPeruandUnitedStates.19,24 In2015,ateamof

governmental,research,andnon-governmentalorganizations inthecityCuritibainSouthBrazillaunchedandevaluateda multi-componentimplementationscienceprojecttoimprove HIVoutcomesforMSM.Thisproject,called“AHoraéAgora” (“TheTimeisNow”)implementedaweb-basedplatformand associatedmobile applicationdesignedtoprovideHIV pre-ventioninformation,allowingforself-assessmentofriskand deliveringHIVself-testkits.Theprojectexceededall expecta-tionswith7352HIVself-testrequestsover24months,asthe initialgoalwastodistribute1000testkitsperyear,andwas abletoreachalargepercentage(31%)ofMSMwhohadnever beentestedbefore,withthosebetween18and28yearsold reportingahigherpercentageoffirst-timetesters(36%)than those29yearsorolder(18%).25Thesameprojectisnowbeing

implementedinthecityofSãoPaulo.26

YoungeragewasassociatedwithnevertestingforHIVin this study,which isworrisomesince thelast national epi-demiological report datashowed that the HIV epidemic is increasinginthisgroup.1Astudyevaluatingsexualrisk behav-ioramongMSMfrom10Braziliancitiesshowedthattobeaged

25 years or less wasindependently associatedwith higher scoresofriskybehavior.27ArecentstudyfromGermanyalso

showedthatyoungerage(<25years)wasassociatedwithlower ratesofHIVtesting.28Theveryabsenceoftestingcouldbea

contributingfactortotheincreasednumberofinfectionsin thispopulation,sincepeoplewithHIVonantiretroviralsare lesslikelytotransmitthevirus thanthosewhodonotuse them,acategorywhichincludeHIVcarriersthathavenotbeen diagnosed.29,30Theproposaloftreatmentaspreventionrelies

onamodelofuniversal testing,reinforcing thatbarriersto HIVtestingwillbecomemorerelevanttothefullspectrumof HIVcare.Maximizingtestingopportunitiesandreducing bar-rierstoregulartestingshouldbeacentralcomponentofHIV preventionprograms.31

Thisstudyhassomelimitations.TheRDStechniquewas noteffectiveforthepopulationofMSMfromNatal,asithas notreachedthesamplesizeinitiallycalculated.Fewseedshad enoughwavestodispersethesampleandmakeitclosertoa probabilisticsample,evenwithalleffortsfromtheresearch teamtoimproverecruitment.Similardifficultieshavebeen reported with the use of RDS technique by researches in Singapore.32 We ended up analyzingour entiregroup asa

non-probabilisticsampleasaconsequenceofthese difficul-ties. Therefore, these resultsmay notbe representative of the entireNatalMSM population. Someofthe resultsthat did not show statistical significance may have been influ-encedbythesamplesizethatmayhavenotbeensufficient toshowassociations.However,thereisrelevancetothestudy becauseitrepresentsapopulationthatisdifficulttoaccessin

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Table5–UnivariateanalysisofselectedcharacteristicsofMSMandpriorHIVtestinginNatalcity,Brazil,2012.

Variables PreviousHIVtest Total Unadjusted Adjustedb

Yes No n % pa PR p PR

n % n % Mean SD (CI95%) (CI95%)

Mean SD Mean SD Occupation Employed 39 66.1 20 33.9 59 61.5 0.48 1.23 Unemployed 21 56.8 16 43.2 37 38.5 (0.76–2.13) Total 60 62.5 36 37.5 96 100 Age 31.8 10.0 24.4 6.9 29.1 9.7 <0.001 0.93 0.041 0.95 (0.88–0.97) (0.91–0.99) Race White 15 62.5 9 37.5 24 26.7 0.97 1.01 Non-White 41 62.1 25 37.9 66 73.3 (0.55–1.84) Total 56 62.2 34 37.8 90 100 Yearsofschooling 11.5 2.1 11.4 2.4 11.5 2.2 0.714

Monthlyincome(USdollars) 528 511 434 370 494 465 0.359

KnowledgeaboutHIV

Correct 6 66.7 3 33.3 9 9.2 0.82 1.11 Incorrect 56 62.9 33 37.1 89 90.8 (0.42–2.91) Total 62 63.3 36 36.7 98 100 Transactionalsex No 38 69.1 17 30.9 55 57.9 0.34 1.37 Yes 23 57.5 17 42.5 40 42.1 (0.80–2.34) Total 61 64.2 34 35.8 95 100

Previoussyphilistest

Yes 31 91.2 3 8.8 34 35.8 <0.001 5.76 0.006 4.21

No 30 49.2 31 50.8 61 64.2 (1.90–17.45) (1.52–11.70)

Total 61 64.2 34 35.8 95 100

KnowwhereHIVtestisfree

Yes 50 71.4 20 28.6 70 72.9 0.017 1.69

No 11 42.3 15 57.7 26 27.1 (1.05–2.71

Total 61 63.5 35 36.5 96 100

Useofcondominlastanalsex

Yes 46 67.6 22 32.4 68 71.9 0.27 1.37

No 15 55.6 12 44.4 27 28.1 (0.79–2.37)

Total 61 64.2 34 35.8 95 100

a Forcategoricalvariables,Chi-SquareorFisherExacttest;forcontinuousvariables,Student’s“t”test.

b PoissonRegressionModeling

alocationwherenosimilarstudyhadbeenperformed previ-ously.

Conclusion

Thestudy showsthatHIVtesting ratesarelowamongthis sampleofMSM,andyoungerageandprevioussyphilistest wereassociatedwithnevertestinginmultivariateanalysis. KnowingaplacewheretheHIVtestcanbedonefree-of-charge wasassociatedwithHIVtestinginunivariateanalysisbutlost significanceinthemultivariatemodel.Actionsthatprioritize thedisseminationofplaceswhereHIVtesting canbedone forfreeandtargetedatyoungpeopleseemtobemost suit-ableforscalingupHIVtestingamongMSMinourreality.Also importantisthefactthatknowledgeaboutHIVtransmission waslow,despitethehigheducationalleveloftheparticipants, emphasizingtheneedforinnovativeapproachesto dissemi-natepreventioninformationforMSM.

Sources

of

support

NationalFundofHealth,MinistryofHealth,Brazil.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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