Prevalence of Chlamydia trachomatis and Neisseria gonorrhea and associated factors among women living with Human Immunodeficiency Virus in Brazil: a multicenter study

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

Prevalence

of

Chlamydia

trachomatis

and

Neisseria

gonorrhea

and

associated

factors

among

women

living

with

Human

Immunodeficiency

Virus

in

Brazil:

a

multicenter

study

Angelica

E.

Miranda

_,

_Mariangela

_F.

_Silveira

_,

_Ana

_Gabriela

_Travassos

_,

Teresinha

Tenório

_,

_Isabel

_Cristina

_Chulvis

_do

_Val

_,

_Leonor

_de

_Lannoy

_,

Hortensio

Simões

de

Mattos

Junior

_,

_Newton

_Sergio

_de

_Carvalho

a_{UniversidadeFederaldoEspíritoSanto,Vitória,ES,Brazil} b_{UniversidadeFederaldePelotas,Pelotas,RS,Brazil} c_{UniversidadeEstadualdaBahia,Salvador,BA,Brazil} d_{UniversidadeFederaldePernambuco,Recife,PE,Brazil} e_{UniversidadeFederalFluminense,Niterói,RJ,Brazil} f_{UnidadedeSaúdeMistadaAsaSul,Brasília,DF,Brazil} g_{LaboratórioSãoMarcos,VilaVelha,ES,Brazil} h_{UniversidadeFederaldoParaná,Curitiba,PR,Brazil}

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Articlehistory:

Received17October2016 Accepted17March2017 Availableonline18May2017

Keywords: Chlamydiatrachomatis Neisseriagonorrhoeae HIV Women Brazil

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Background:Chlamydiatrachomatis(CT)andNeisseriagonorrhoeae(GC)causeinfectionsinthe femalegenitaltract,increasingsusceptibilitytoandinfectiousnessofHIV.Theobjectives ofthepresentstudyweretodeterminetheprevalenceandassociatedfactorsofCTandGC infectionamongHIV-infectedwomeninBrazil.

Methods:Cross-sectionalstudyconductedfromMarchtoDecember2015,including HIV-infected women attending referral centers in nine states of Brazil, aged 18–49 years, nonpregnant.Aninterviewwasconductedincludingsocio-demographic,epidemiological andclinicalcharacteristics.Aftertheinterview,gynecologicalexaminationwasconducted tocollectcervicalcytologyandvaginalsecretiontoC.trachomatisandN.gonorrhoeaetests throughmolecularbiology.

Results:Atotalof802(89.1%)womenparticipated.TheprevalenceofCTwas2.1%(17/802) andCGwas0.9%(7/802).TheprevalenceofapositivetestforbothCTand/orGCwas2.7%.The factorsassociatedwithpositiveCT/GCtestinthemultivariatelogisticregressionanalysis wereabnormalPapanicolausmear(OR4.1;95%CI:1.54–11.09)andthepresenceofabnormal

∗ _{Correspondingauthor.}

E-mailaddress:amiranda.ufes@gmail.com(A.E.Miranda).

http://dx.doi.org/10.1016/j.bjid.2017.03.014

1413-8670/©2017SociedadeBrasileiradeInfectologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

cervicaldischarge(OR2.6;95%CI:1.02–6.71).Among377womenwhoreportedprevious STI245(65.0%)reportedusingcondommorefrequentlyafterbeingdiagnosed.62(16.4%) discoveredtheSTIafterthepartnertoldhewasinfected;157(41.6%)hadSTIsymptoms andlookedforcare,and158(41.9%)discovereditinaroutineconsultationforanother reason.

Conclusions: ThecontrolofSTIrepresentsauniqueopportunitytoimprovereproductive healthofwomenlivingwithHIV.STIdiagnosiscanchangetheirbehaviorandreducethe sexualtransmissionofHIVandbacterialSTI.

©2017SociedadeBrasileiradeInfectologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/

licenses/by-nc-nd/4.0/).

Introduction

Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (GC) screeningcanpreventhealthcomplications.Infectioninthe lower genital tract can result in upper genital tract com-plications, such as pelvic inflammatory diseases, ectopic pregnancy, chronic pelvic pain, and infertility in asymp-tomatic women, and transmission of infection during pregnancyandlabor.1,2_{Theyalsoincreasesusceptibilityand}

infectiousnessofHIVinfection.3

In HIV-infected women, infection with CT or GC is an importantbiologicmarkerofbehaviorthatmayexpose oth-ers to HIV. Furthermore, CT and GC are associated with increased cervico-vaginal HIV shedding that may increase HIV transmissibility.4 _{Identification ofHIV-infected women}

withCTorGCcanhelptargetpreventiveinterventionssuch aspromoting safersexual practices. Treatment ofsexually transmittedinfections(STI)alsomayimpactheterosexualHIV transmission.5

PreviousstudiesfromBrazilreportedprevalenceratesof 3.0%ofCTand0.9%ofGCamongHIV-infectedwomeninRio deJaneiro6_{andinManausarateofCTof4.3%.}7_Theseresults

werenotdifferentfromdatareportedinZambiathatfound aprevalencerateof1%ofCTand1.4%ofGCinHIV-infected women.8,9

The aim of the current study was to determine the prevalenceofandassociatedfactorsforCTandGCamong HIV-infectedwomenattendingreferralcarecentersforHIV/AIDS inBrazil.

Methods

Across-sectional study was conductedamong women liv-ing with HIV/AIDS who attended referral care centers for HIV/AIDS in nine different Brazilian states: Amazonas, Pernambuco, Bahia, FederalDistrict, Espirito Santo,Rio de Janeiro,SãoPaulo,Paraná,andRioGrandedoSul,distributed inthefivegeographicalregionsofBrazil,fromMarchthrough December2015.

Nonpregnant women aged 18–49 years, with a positive resultfor HIV infection,being cared foratthe gynecology servicelinkedtoreferencehospitals,whoacceptedto partici-patewereinvitedtotakepartinthestudy.

A 20-min face-to-faceinterview was conductedusing a standardizedquestionnaire(validatedinapilotstudy) that included socio-demographiccharacteristics (age,education, maritalstatus,familyincome,placeofresidence); epidemi-ological (smoking, use of alcohol and illicit drugs, use of condoms, numberofsexualpartners,sexualpractices) and clinical(vaginaldischarge,previousSTI,stageofinfectionwith HIV,CD4cellcountandHIVviralload).Apilotstudywas con-ductedinasmallnumberofwomenlivingwithHIV/AIDSto evaluatethereliabilityandvalidityofthequestionnaire.

Aftertheinterview,gynecologicalexaminationwascarried outtocollectcervicalcytologyandvaginal/cervicalsecretion to test forCT and GC through molecular biology. Samples were analyzed in an automated system forreal time PCR (COBAS4800CT/NG–RocheMolecularSystems,Branchburg, NJ) for detection ofCT and GC, as per the manufacturer’s instructionsattheMolecularBiologyLaboratoryofthe Infec-tiousDiseasesUnitoftheFederalUniversityofEspíritoSanto andSãoMarcosLaboratory,aISO9001:2000(INMETRO)and UKAS(England)certifiedprivatelaboratoryinVilaVelha(ES). Endocervicalsampleswerecollectedusingswabs,PreservCyt transportmediumandstoredat10◦Cuntiltheir transporta-tionatlowtemperaturetothereferencelaboratory,inaperiod ofsevento10days.

Selectionofthestudysampletookintoaccountthe propor-tionofAIDScasesfromthefivegeographicalregionsreported totheAIDSNationalInformationSurveillanceSystemin2010 (consolidatedwiththe InformationSurveillanceSystemfor Mortality,laboratorytests–CD4countsandHIVviralload,and antiretroviraltherapy).Atotalof12,845HIV-infectedwomen were reported:9.7%fromtheNorth;20.1%fromthe North-east;38.6%fromtheSoutheast;25.2%fromtheSouth,and6.4% fromtheMidwestregion.Basedonthesecriterianineclinics wereincluded:oneinNorthernregion,twointheNortheast, threeintheSoutheast,twointheSouthernregion,andonein theMidwestregion.

The sample size was calculated to estimate the preva-lence ofCT and GC inwomen living with HIV/AIDS, with a 95%confidence interval (CI)bilateral sizeof0.5%. Itwas assumedasthelowestexpectedfrequency0.9%ofN. gonor-rhoeaeinwomenlivingwithHIV/AIDS6_{;acceptingavariation}

of±0.3%anumberof773womenwerenecessary.Allowing foraloss of10%,a finalsampleof850womendistributed proportionallyineachclinic95womenperclinicweretobe included.

Table1–DemographicandbehaviorcharacteristicsbyCT/GCpositivityamongwomenlivingwithHIVinBrazil,2015 (N=802).

Variable Total CT/GC+ CT/GC− OR(95%CI)

N(%) N(%) N(%) pvalue Age(years) ≤24 43(5.4) 03(7.0) 40(93.0) 2.9(0.83–10.28) >24 759(94.6) 19(2.5) 740(97.5) 1 Education(years) ≤8 398(49.6) 08(2.1) 390(97.9) 0.6(0.24–1.38) >8 404(50.4) 14(3.5) 390(96.5) 1 Maritalstatus Single/Divorced/Widow 396(49.4) 12(3.0) 384(97.0) 1.2(0.53–2.90) Married/livingtogether 406(50.6) 10(2.5) 396(97.5) 1

Firstsexintercourse

≤15years 299(37.3) 11(3.7) 288(96.3) 1.7(0.73–3.99)

≥16years 503(62.7) 11(2.2) 492(97.8) 1

Numberofpartners(life)

Onlyone 67(8.4) 01(1.5) 66(98.5) 1 2–5 490(61.1) 15(3.1) 475(96.9) 1.0(0.56–1.89) 6–9 79(9.9) 02(2.5) 77(97.5) 1.2(0.85–1.83) ≥10 166(20.7) 04(2.4) 162(97.6) 1.4(0.76–2.53) Tobaccouse Yes 157(19.6) 06(3.8) 151(96.2) 1.6(0.60–4.06) No 645(80.4) 16(2.5) 629(97.5) 1

Illicitdrugabuse

Yes 150(18.7) 6(4.0) 144(96.0) 1.7(0.64–4.31)

No 652(81.3) 16(2.5) 636(97.5) 1

Injectingdruguse

Yes 19(2.4) 01(5.3) 18(94.7) 2.0(0.26–15.81)

No 783(97.3) 21(2.7) 762(97.3) 1

ConsistentCondomuse

No 227(28.3) 06(2.6) 221(97.4) 0.9(0.36–2.45)

Yes 575(71.7) 16(2.8) 559(97.2) 1

Analsex

Yes 350(43.6) 13(3.7) 337(96.3) 1.9(0.80–4.50)

No 452(56.4) 09(2.0) 443(98.0) 1

DatawereanalyzedusingtheSPSS–dataentrystatistical program(StatisticalPackagefortheSocialSciences)version 17.0.Apreliminaryanalysiswasperformedusingexploratory techniques on the data, tocheck the distribution patterns andtrendsofthevariables.Univariateanalysiswasthen per-formedtocheckforthepresenceofassociationbetweenthe variables.Chi-squaretestswereusedtocompareproportions and Student’s t tests and variance analysis were used for testingdifferencesbetweenmeanvalues.Univariateand mul-tivariateoddsratios(ORs)(adjustedforpotentialconfounders) and95%CIswerereported.Variablesthatweresignificantat

p<0.15inunivariateanalysisand knownconfounders(e.g., ageandeducation)wereconsideredinthemultivariate anal-ysisusingastepwisemultiplelogisticregressionmodel.

This project was submitted to and approved by the Research Ethics Committee (#131107/2012) of Center for HealthSciences oftheFederalUniversity ofEspíritoSanto. Allselectedwomenwereinvitedtotakepartvoluntarilyin thestudyandthosewhoacceptedsignedawrittenconsent form.ThosewhowerediagnosedasbeinginfectedbyCTorGC receivedtreatmentasrecommendedbytheBrazilianMinistry ofHealthguidelines.

Results

Outof850eligiblewomen802(94.4%)acceptedtoparticipate inthestudy,fromMarchtoDecember2015.Medianagewas39 (IQR34–46)yearsandmedianyearsofeducationwas9 (IQR6-11).TheprevalenceofCTwas2.1%(17/802)and ofCG0.9% (7/802).TheprevalenceofapositivetestforCTand/orGCwas 2.7%(22cases).

Theprevalenceratesbygeographicalregionwere:North 2.6%; Northeast 2.6%; Midwest 1.2%; Southeast 3.5%, and South2.4%.Therewasnostatisticallysignificantdifference betweenthegeographicalregions.

Table1showsdemographicandbehavior characteristics

ofwomenlivingwithHIVinBrazil.Noneofthevariableswas associatedtoCT/GCpositivetest.Atotalof43(5.4%)women wasyoungerthan25yearsold,299(37.3%)hadthefirst inter-coursebefore16 years,and 575(71.7%)reportedconsistent condomuse.

ClinicalcharacteristicsaredescribedinTable2.Atotalof 137(17.1%)reportedpelvicpain.Abnormalcervicaldischarge (5.7%vs.1.7%,p=0.002);abnormalPapanicolausmear(9.9%

Table2–ClinicalcharacteristicsbyCT/GCpositivityamongwomenlivingwithHIVinBrazil,2015(N=802).

Variable Total CT/GC+ CT/GC− OR(95%CI)

N(%) N(%) N(%) pvalue PreviousSTI Yes 377(47.0) 10(2.7) 367(97.3) 0.9(0.40–2.20) No 425(53.0) 12(2.8) 413(97.2) 1 Previousmiscarriage Yes 171(21.3) 5(2.9) 166(97.1) 1.1(0.40–2.99) No 631(78.7) 17(2.7) 614(97.3) 1 Pelvicpain Yes 137(17.1) 6(4.4) 131(95.6) 1.9(0.71–4.83) No 665(82.9) 16(2.4) 649(97.6) 1 Cervicaldischarge Yes 212(26.4) 12(5.7) 200(94.3) 3.5(1.48–8.20) No 590(73.6) 10(1.7) 580(98.3) 1 Cystitis Yes 116(14.5) 4(3.4) 112(96.6) 1.3(0.44–3.98) No 686(85.5) 18(2.6) 668(97.4) 1 Genitalulcer Yes 52(6.5) 1(1.9) 51(98.1) 1.5(0.19–11/14) No 750(93.5) 21(2.8) 729(97.2) 1 GenitalLymphadenopathy Yes 26(3.2) 2(7.7) 24(92.3) 3.2(0.70–14.29) No 776(96.8) 20(2.6) 756(97.4) 1 GenitalItching Yes 142(17.7) 7(4.9) 135(95.1) 2.2(0.89–5.59) No 660(82.3) 15(2.3) 645(97.7) 1 TARVuse Yes 718(89.5) 20(2.8) 698(97.2) 0.9(0.20–3.70) No 84(10.5) 2(2.4) 82(97.6) 1 CD4Count ≥500 508(63.3) 15(3.0) 493(97.0) 0.8(0.32–1.99) ≤499 294(36.7) 7(2.4) 287(97.6) 1 Papanicolausmear Abnormal 71(8.9) 7(9.9) 64(90.1) 5.2(2.05–13.27) Normal 731(91.1) 15(2.1) 716(97.9) 1 Viralload Detectable 212(26.4) 10(4.7) 202(95.3) 2.3(1.01–5.60) Undetectable 590(73.6) 12(2.0) 578(98.0) 1

Table3–MultivariateanalysisoffactorsassociatedwithCT/GCpositivityamongwomenlivingwithHIVinBrazil,2015.

Variables OR (95%CI) p-value

Ageinyears(Upto24vs.≥25) 2.6 (0.71–9.63) 0.148

Analsex(Yesvs.No) 1.5 (0.62–3.70) 0.361

Papanicolausmear(Abnormalvs.normal) 4.1 (1.54–11.09) 0.005

Pelvicpain(Yesvs.No) 1.3 (0.28–2.24) 0.656

Cervicaldischarge(Yesvs.No) 2.6 (1.02–6.71) 0.046

GenitalItching(Yesvs.No) 1.1 (0.40–3.20) 0.820

GenitalLymphadenopathy(Yesvs.No) 1.5 (0.27–7.94) 0.662

Viralload(Detectablevs.Undetectable) 1.7 (0.67–4.06) 0.274

HosmerandLemeshowtest:X2_{=6.367,df:7,p=0.498.}

Thevariablesinboldwerestatisticallysignificant.Theypresentedapvalue<0.05.

vs.2.1%,p<0.001),anddetectableHIVviralload(4.7%vs.2.0%,

p=0.040)wereassociatedwithapositiveCT/GCtestresult. The factors associated with a positive CT/GC test in themultivariate logisticregression analysiswere abnormal Papanicolau smear (OR 4.1; 95% CI: 1.54–11.09) and the

presence of abnormal cervical discharge (OR=2.6; 95% CI: 1.02–6.71)(Table3).

Table4showssubanalysesperformedin377womenwho

reportedprevious STI.Atotalof245(65.0%)reportedusing condommorefrequentlyafterreceivingthediagnosisofSTI.

Table4–HealthbehaviorofwomenlivingwithHIVinBrazilafterreceivinganSTIdiagnosis,bycondomuse,2015 (N=377).

Variables Condomuse Nocondomuse p-value

N(%) N(%)

HowdidyoudiscovertheSTI 0.043

PartnertoldyouhewasinfectedbyanSTI 38(61.3) 24(38.7)

YouhadSTIsymptomsandlookedforcare 116(73.9) 41(26.1)

Youdiscovereditinaroutineconsultationforanotherreason 123(77.8) 35(22.2)

WhenyouwerediagnosedwithanSTI,wheredidyoutreatit? 0.713

Ididnottreat 5(62.5) 3(37.5)

PrimaryHealthUnit 165(72.1) 64(27.9)

Pharmacy 7(77.8) 2(22.2)

STIclinic 100(73.5) 31(23.7)

DidyoutellyourpartnerabouttheSTIdiagnosis? 0.155

Yes 201(75.6) 65(24.4)

No 76(68.5) 35(31.5)

Afterreceivingthediagnosisdidyouusecondomsmoreoften? 0.001

Yes 207(84.5) 38(15.5)

No 70(53.0) 62(47.0)

Afterreceivingthediagnosisyoudidyoudecreaseyoursexualactivity? 0.331

Yes 132(75.9) 42(24.1)

No 145(71.4) 58(28.6)

Sixty-two(16.4%)discoveredtheSTIafterthepartnertoldhe wasinfectedbyanSTI; 157(41.6%)hadSTIsymptomsand lookedforcare,and158(41.9%)discoveredtheSTIinaroutine consultationforanotherreason.

Discussion

TheprevalenceofCTandGCinHIV-infectedwomeninBrazil waslowerthantheratesreportedamongadolescentsoryoung pregnant women.10,11 _{These resultsare inagreement with}

previousstudiesconductedinRiode Janeiro6 _andManaus7

and a little higher compared to HIV-infectedwomen from Zambia.8Theobservedlowerratescouldbeattributedtothe olderageofthesewomencomparedtopregnantwomenor adolescents.2,10,11 _{DuetotheirHIVstatus,itispossiblethat}

theseparticipantswere morelikelytobereceivingongoing medicalcareandantibioticsprescriptions.Theseresultscan suggestthatengaginginHIVcaremayplayarolefor control-lingSTIinthispopulation.

The factors associated with positive CT/GC test in the finalmultivariatemodelwere abnormalPapanicolausmear andpresenceofabnormalcervicaldischarge,whichdoesnot includeinflammatory results,according with the Bethesda system.12_{SomestudieshavelinkedthepresenceofChlamydia}

inwomenwithHPVinfectionandabnormalPapsmearsinthe generalpopulation.13_{In2011Lehtinenetal.publishedacohort}

studyshowingthatwomenwithCTatbaselinewere1.78times morelikelytodevelopcervicalintraepithelialneoplasiagrade 2dueanyHPVtype,thanthosewithoutCT.14_Screeningfor

cer-vicalasymptomaticCTandGCcanidentifywomenwhoneed follow-upforHPVinfectionandmorecarefulinvestigationof precursorlesionsofcervicalcancer.Theassociationbetween vaginaldischargeandCTandGCinfection,describedinour study,wasnotcommonly reportedinprevious studies.15,16

Thesyndromicmanagementofgenitalinfectionshasnotbeen

consideredeffective,withthissymptombeingapoorpredictor ofcervicitis byCTand GC. Therefore, screeningof asymp-tomaticwomenremainsthebestsuitedrecommendationfor thistargetpopulation.15

WomenwhohavereportedapreviousSTIdiagnosiswere questionedabouthowtheyfoundouttheSTI.Almosthalfof themreceivedtreatmentbecausetheyhadSTIsymptomsand lookedforcareordiscoveredtheSTIinaroutine consulta-tionforanotherreason.ThecontrolofSTIrepresentsaunique opportunitytoimprovereproductivehealthofwomenliving withHIV.5_{Bothulcerativeandnon-ulcerativeSTIincreasethe}

riskofHIVtransmissionbythreeto10times,dependingon the typeand etiology ofthe STI.5 _{HIV-infected individuals}

affected byanSTI haveincreasedHIVviral loadin genital secretions,4,17_{therebyincreasingconsiderablytheirpotential}

ofinfectiousnessandtransmission.

TheriskofHIVsexualtransmissionisdifferentaccording tothesexualrelationship.Female-to-maletransmissionhave ariskof0.04–0.38%persexualact,increasingto5.3%incase ofprevioushistoryorpresenceofSTIandgenitalulcer.18

Sex-ual behaviorhasbeen modifiedworldwide,withmorenew sexualpractices,lowuseofcondom,andlowconcernabout theriskofSTItransmission.19_{Inourstudy,weidentifiedthat}

only41.6%ofthewomenhadthe diagnosisofSTIbecause theylookedforcareduetopresenceofrelatedsymptoms.The knowledgeofthisdiagnosisledtoincreaseduseofcondoms during sexualrelations.The accesstoSTI diagnosisbrings effectivepreventionandcanchangesexualbehavior.

Althoughacross-sectionalstudyisnotidealfor determin-ing riskfactors,itsapplicationisjustified.KnowingCTand GCprevalenceratesanditsassociatedfactorsinHIV-infected women is importantto demonstratetheir susceptibility to complicationscausedbytheseinfections.Giventhelow preva-lenceofsomeriskfactorsinthissample,itispossiblethatthe numberofstudiedwomenwasnotsufficienttofindstatistical associationbetweensomeindependentvariablesandCT/GC

positivity.Thepossibilityofbiasedanswerscannotberuled outbecauseofthegeneraltendencytogivesociallyacceptable repliesinface-to-faceinterviews.

Despitethelimitations,thisstudysuggeststhatscreening programsmustbecost-effectiveandmustbemade accept-abletopatients byusing non-invasiveprocedures.Itcould alsobeconsideredapreventivemeasureaimedtodetermine riskfactors,ordetectandtreatabnormalsignaland symp-tomsthatcould latercausecomplications. Afterthe“Treat asPrevention”strategy,adoptedinBrazilsince2013,20

peo-pleusedcondomlessfrequently,becauseassumedHIVcould notbetransmittedinthepresenceofviralsuppression.21At thesametime,worldwide,bacterialSTI,suchassyphilis,CT, andNGareahighburden,mainlyinpeoplelivingwithHIV.22

ControllingSTIandidentifyingfactorsassociatedwithsuch diseasescontinuestobeanimportantelementinthedesign ofinterventionstargetingSTIandasaresult,HIVprevention inBrazil.

Financial

support

Technicalcooperationagreement–BrazilianDepartmentof STI,AIDSand viralhepatitis,MinistryofHealthandUnited Nationsofficefordrugsandcrime.ProjectBRA/K57,process #01/2013.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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