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
Brief
communication
High
prevalence
of
Chlamydia
trachomatis
and
Neisseria
gonorrhoeae
in
Western
French
Guiana
Maria-Francesca
Manca
a,
Laurence
Rochat-Stettler
b,
Jean-Franc¸ois
Carod
c,
Camille
Agostini
a,
Anne
Jolivet
a,d,∗aWesternFrenchGuianaHospitalCenterFranck-Joly,DepartmentofPublicHealth,Saint-LaurentduMaroni,FrenchGuiana bWesternFrenchGuianaHospitalCenterFranck-Joly,DepartmentofMedicine,Saint-LaurentduMaroni,FrenchGuiana cWesternFrenchGuianaHospitalCenterFranck-Joly,DepartmentofMedicalBiology,Saint-LaurentduMaroni,FrenchGuiana dINSERM,SorbonneUniversité,InstitutPierreLouisd’EpidémiologieetSantéPublique(IPLESP),EquipedeRechercheenEpidémiologie Sociale(ERES),Paris,France
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Articlehistory:
Received4March2020 Accepted23April2020 Availableonline19May2020
Keywords: Chlamydiatrachomatis Neisseriagonorrhoeae FrenchGuiana Prevalence
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ThepurposeofthisstudywastoestimatetheprevalenceofChlamydiatrachomatis(CT)and
Neisseriagonorrhoeae(NG)infectionsinwesternFrenchGuianaandtoanalyzeassociated factorswithbothinfections.Aretrospectivestudywasconductedinasexuallytransmitted infectionsclinicin2017.Women(n=338)weretestedbyreal-timepolymerasechainreaction forvaginal,analandthroatCTandNGinfections.Men(n=192)wereevaluatedusingurine specimens.Socio-demographicandsexualbehaviourdatawerecollectedbynurseswith astructuredquestionnaire.TheprevalenceofCTandNGinfectionsamongwomenwere 24.3%and13.3%,respectively,and12.0%and7.3%amongmen.Womenagedunder25years hadahigherriskofCTandNGinfectionsthanwomenaged35yearsormore.Another riskfactorforCTinfectionwasloweducationallevel,andoccasionalunprotectedsexfor NGinfection.CTandNGinfectionswereassociatedwithreportingsymptomsamongmen. VeryhighprevalencesofCTandNGinfectionsamongwomenandmenwerefound,which suggestthatalarge-scalescreeningstrategyshouldbeimplementedinFrenchGuiana.
©2020SociedadeBrasileiradeInfectologia.PublishedbyElsevierEspa ˜na,S.L.U.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/ licenses/by-nc-nd/4.0/).
Anestimated376millionnewinfectionswithoneofthesefour sexuallytransmittedinfections(STIs)areacquiredeachyear worldwideandnumbersarestillincreasingeachyear: chlamy-dia(127million),gonorrhoea(87million),syphilis(6.3million), andtrichomoniasis(156million).1Chlamydiatrachomatis(CT)
∗ Correspondingauthorat:SorbonneUniversité,INSERM,InstitutPierreLouisd’EpidémiologieetdeSantéPublique(IPLESP),Equipede
RechercheenEpidémiologieSociale(ERES),F75012,Paris,France.Tel:(+33)635258755 E-mailaddress:annejolivet@yahoo.fr(A.Jolivet).
andNeisseriagonorrhoeae(NG)infectionsusuallydisplaya non-specificpatternofsignsandsymptomsamongwomen,and areassociatedwithimportantcomplicationswhen misdiag-nosed or mistreated, suchas pelvic inflammatory disease, infertility, and ectopic pregnancy.2 Maternal CT infections
https://doi.org/10.1016/j.bjid.2020.04.014
1413-8670/©2020SociedadeBrasileiradeInfectologia.PublishedbyElsevierEspa ˜na,S.L.U.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
havealsobeenassociatedwithincreasedperinatal morbid-ity and mortality.3 CT and NG infections are more often
symptomaticamongmeninwhomtheyareresponsiblefor epididymitisandmaycausemaleinfertility.4Theseinfections
alsoplayanimportantroleinenhancingHIVtransmissionin bothsexes.5
FrenchGuiana isa Frenchoverseas department located betweenSurinameandBrazil.IthasthehighestHIV preva-lence in France (1 to 1.5% in pregnant women).6 French
Guianese population may be exposed to a high risk of STIs because of social and economic factors, risky sexual behaviourssuchasunprotectedsexwithmultiplesexual part-ners,andlimitedaccesstopreventionandcare.7TheFrench
NationalHIV/AIDS Councilrecommendedin2018a coordi-natedpolicyonsexual healthinresponsetothis worrying situation.7However,thereisnoclearstrategyforCTandNG
screening in French Guiana. One of the reasons that may explainthissituationisthelimitedepidemiological informa-tionregardingtheseinfections.
Themainobjectiveofthisstudywastoestimatethe preva-lenceofCTandNGinfectionsataSTIclinicinFrenchGuiana. Secondaryobjective wastoanalyzeassociatedfactors with bothinfections.
Aretrospectivestudywasconductedin2017atthe sexu-allytransmittedinfections(STI)clinic(CeGIDD)oftheWestern FrenchGuianaHospitalCentreinSt-LaurentduMaroniwhich isthe secondlargest cityinFrenchGuiana,bordering Suri-name.Thishospital,whichis250kmawayfromthemaincity Cayenne,servesapopulationofaround100,000inhabitants. InhabitantslivinginSt-LaurentduMaroniareyoung(halfare lessthan20yearsold),withloweducationallevel(twothirdsof thepopulationhavenodiploma,vs.20%inmainlandFrance) andlowemploymentrate(42% ofmenand56% ofwomen aged15–24yearswereunemployedin2015).Thecityandthe territoryofwesternFrenchGuianaalsofaceproblemssuch aslimitedaccesstodrinkingwater,spontaneoussettlements, unsanitaryconditions,illegalwork,andviolence.8
CeGIDDisinchargeofapublicservicemissionwithinthe generalpopulationandat-riskcommunities.Itreceivesand takeschargeofeveryuser,regardlessofage,sex,healthstatus, nationality,sexualorientationorgenderidentity.Itensures voluntary,anonymousandfreescreeningofHIV,viral hep-atitisandSTIsuchassyphilis,HTLV,CT,andNGinfections, aswell astheirtreatmentsor referralto aninfectious dis-easespecialistwhenneeded(includingforPrePconsultation). Therefore,usersmayaccesstheSTIclinicafterahigh-risk sex-ualintercourse,iftheyaresymptomatic,orjustforaroutine screening.TheSTIclinicalsoprovidestheuserswithfree pre-ventionmaterial:documentation,condoms,andgels,always accompaniedbyspecificadvice forprimaryand secondary preventionpurposes.
CT/NGscreeningwasintroducedinFebruary2017attheSTI clinic.Allwomenweretestedforvaginal,analandthroatNG andCTinfections.FromFebruarytoAugust2017(firstperiod), women self-collected the three samples in three different tubes(standardofcaretriple-sitetesting).FromSeptemberto December2017(secondperiod)thethreeself-collectedswabs werepooledinto thesametube(pooledsample).Menwere tested forNG and CT infections using urine samples, and thosewhoadmittedtohavesexwithmen(MSM)also
self-collectedpharyngealandrectalsamples.Thesampleswere senttoCerba® Laboratory(SaintOuenl’Aumône,France)and weretestedbyPCRusingtheAbbottm2000Real-TimeSystem. Patientsalsoreceivedastructuredinterviewperformedbya trainednurse,assessingsocio-demographicdata(age, coun-tryofbirth,healthinsurance),useofcontraception(women), relationshipstatus,sexualorientation,numberofsexual part-nersinthelast12months,useofcondoms,historyofforced sexual intercourses, and current symptoms. All data were documentedandcapturedinanelectronicdatabase.The elec-tronicpatientdatabaseoftheSTIclinicwasmergedwiththe laboratorydatabaseandanonymizedthedata.Ifpatientshad cometotheclinicseveraltimes,onlythefirstvisitwas consid-ered.ForwomenandMSM,CTorNGinfectionsweredefined byhavingatleastonepositivesample.CTandNGprevalences withconfidenceinterval(95%CI)werecalculatedseparately forwomenandmen.Forwomen,wecomparedtheestimated prevalencebetweenthetwoperiodswithchisquaretest. Uni-variate logistic regression analyses tested forpredictors of infections for bothwomenand men. Thevariables associ-atedwithinfectionsdefinedbyatwo-sidedp-value≤0.2were furtherexplored ina multivariatemodel and progressively eliminatedusinganautomatedstepwiseproceduretoobtain afinaladjustedmodelwithsignificantvariables(p<0.05)and borderlinessignificantvariables(0.05≤p≤0.1).Theanalyses wereperformedusingSTATA® v13.1software.
From FebruarytoDecember 2017,atotalnumberof530 patientswereincluded,192(36%)menand338(64%)women. Meanagewas31.5yearsamongmenand27.1amongwomen; 35.4%ofmenand45.9%ofwomenwerelessthan25yearsold, 47.1%ofmenand42.9%ofwomenwerenotborninFrance (norinFrenchGuiana).Inaddition,29.5%ofmenand24.5% ofwomenhadnohealthinsuranceand38.8%ofwomenand 74.6%ofmendeclaredtwoormorepartnersduringthelast12 months.Amongwomen,theprevalenceofCTandNG infec-tionswere24.3%(95%CI19.8–29.2)and13.3%(95%CI9.9–17.4), respectively(Table1).Theco-infectionratewas5.9%(95%CI 3.7–9.0). Two hundred and twelvewomen underwent stan-dardofcaretriple-sitetestingduringthefirstperiodand126 weretestedusingapooledsampleinthesecondperiod.The prevalenceofCTinfectionwassimilarinthetwoperiodsof testing.TheprevalenceofNGinfection wasslightly higher duringthe firstperiod,but notstatisticallydifferent(15.6% vs.9.5%,p=0.11).Inthefirstperiod,3.8%ofthewomenhad isolatedextragenitalCTand4.7%(95%CI2.3–8.5)hadisolated extragenitalNG.ExtragenitalCTaccountedfor15.1%(95%CI 5.5–25.3)oftotalCT infectionsand30.3% (95%CI15.6–48.7) oftotalNGinfections.Amongmen,theprevalenceofCTand NGinfection were12.0%(95%CI7.7–17.4)and7.3%(95%CI 4.0–11.9),respectively.Fivemenreportedhavingsexwithmen andnoneofthemtestedpositiveforneitherinfection.
Inmultivariateanalysis(Table2),significantriskfactorsfor CTamongwomenwereyoungageandloweducationallevel. Womenagedunder25yearsoldhadahigherriskofCT(OR adjusted=10.2,95%CI2.2–47.0),followedbythoseaged25–34 (ORa=7.3,95%CI 1.6–34.5),comparedwithwomenaged35 yearsorolder.Womenwhoattended middleschoolorhigh schoolhadhigherriskofCTthanthosewhoattended univer-sity(ORa=4.6,95%CI1.0–2.8).Forcedsexualintercoursewas atthelimitofstatisticalsignificance(ORa=2.0,95%CI0.7–5.5).
Table1–Chlamydiatrachomatis(CT)andNeisseriagonorrhoeae(NG)prevalence,bysex.
Amongwomen Amongmen
Participants, N CTpositive,N (%) NGpositive, N(%)
Participants,N CTpositive,N(%) NGpositive,N(%)
338 82(24.3) 45(13.3) 192 23(12.0) 14(7.3%) Standardofcare triple-sitetesting (Firstperiod) Vaginal +Throat+Rectal 212 53(25.0) 33(15.6) Vaginal 212 45(21.2) 23(10.9) Isolated Extragenital 212 8(3.8) 10(4.7) Pooledsample (Secondperiod) Vaginal+ Throat+Rectal 126 29(23.0) 12(9.5)
Table2–AssociatedfactorsforCTandNGinfection,bysex.
AmongWomen(n=338) Amongmen(n=192)
N(%) CTpositive NGpositive N(%) CTpositive NGpositive
ORa(95%CI) ORa(95%CI) ORa(95%CI) ORa(95%CI)
Age ≥35yearsold 74(21.9) 1 1 64(33.3) 25–34yearsold 109(32.3) 7.3(1.6–34.5) 1.0(0.3–3.3) 60(31.3) <25 155(45.9) 10.2(2.2–47.0) 2.7(1.0–7.8) 68(35.4) Sexforced No 195(89.0) 1 120(95.2) Yes 24(11.0) 2.0(0.7–5.5) 6(4.8) Educationallevel University 33(14.2) 1 25(19.1)
Middleorhighschool 181(78.0) 4.6(1.0–20.8) 96(73.3)
Noneorprimaryschool 18(7.8) 5.1(0.7–37.4) 10(7.6)
HealthInsurance With 247(75.5) 1 129(70.5) Without 80(24.5) 1.7(0.8–3.6) 54(29.5) Useofcondoms Always 85(28.2) 1 70(40.7) Never 94(31.2) 2.6(0.9–7.3) 32(18.6) Sometimes 122(40.5) 2.6(1.0–7.0) 70(40.7) Clinicalsymptoms No 304(89.9) 165(85.9) 1 1 Yes 34(10.1) 27(14.1) 4.2(1.6–11.2) 17.4(5.1–59.8) Relationshipstatus Inarelationship 129(40.6) 81(46.8) 1 Single 189(59.4) 92(53.2) 2.4(0.6–8.9)
ORa,adjustedOddsRatioobtainedbymultiplelogisticregressionanalyses;95%CI,95%ConfidentInterval.
RisksfactorsforNGamongwomenwereageunder25years old(ORa=3.3,95%CI1.2–8.7)andoccasionalunprotectedsex, (ORa=2.6,95%CI1.0–7.0).RatesofCTandNGinfectionswere significantlyhigherinmenwhoreportedtheirsymptomsto themedicalteam(respectively,ORa=4.2,95%CI1.6–11.2and ORa=17.4,95%CI5.1–59.8).
TherewasahighprevalenceofbothCTandNGinfections inwomen(24.3%and13.3%,respectively)andinmen(12.0% and7.3%,respectively).Prevalenceratesvarywidelyaround theworld.Nevertheless,prevalencesfoundinthisstudyare muchhigherthanthosefoundinFranceandEuropean coun-tries,and seemmorecomparabletothose foundinFrench Guiana’sneighbouringcountries.InFrance,CTprevalencein
peopleaged18–44(n=4957)wasestimatedat1.4%formenand 1.6%forwomenin2006.9AstudyconductedinaFrenchSTI
clinicin2009founda7.6%prevalenceforCTand0.36%forNG (n=1381,bothwomenandmen).10Areviewoftheliteraturein
pregnantwomeninmiddle-andlow-incomecountriesfound anadjustedmeanprevalenceof11.2%forCTinsevenstudies and0.3%forNGinthreestudiesinLatinAmerica.11
Datafromtheneighbouringcountriesarescarce.In Suri-name,wedidnotfindanyprevalencestudyintheliterature, andRT-PCRisnotavailableinthatcountry.Manystudieswere conductedinBrazilandfoundawiderangeofratesofCTor NGinfections.AlargestudyconductedamongmeninsixSTIs clinicsinBrazilfoundaprevalenceof13.1%forCTand18.4%
forNG.12OtherstudiesconductedamongwomeninFrench
Guiana’sneighbouringstates(Para,Amazonas)reportedhigh ratesofCTinfections,rangingfrom 4%to18%,particularly amongyoungand poorwomenlivingintheinterior ofthe BrazilianAmazon.13–15
Thehighrateobservedinthisstudymaybeexplainedbyat leastthreefactors.First,wemeasuredgenitaland extragen-italinfections amongwomen,whileotherstudiesgenerally measuredonlygenitalinfections.Nevertheless,ifweconsider onlypositivevaginalsamplesinthefirstperiodoftesting,CT andNGprevalencesremainhighamongwomen(21.2%and 10.9%,respectively).Asecondfactormaybethe characteris-ticsofourstudysample:youngpeople(almosthalfofwomen and morethan onethird ofmen, were less than 25 years old),withlimitedaccesstobasichealthservices(aboutone fourthofwomenormenhadnohealthinsurance),andhigh levelofriskysexualbehaviour(threefourthsofmendeclared twoormorepartnersduringthelast12months).Many stud-ieshaveshownthatCTandNGarefoundpredominantlyin youngwomenormenbecausetheyareathigherriskof acquir-ingthoseinfections.11,15,16Asystematicliteraturereviewalso
foundthatsocialconditions,lackofeconomicopportunities andriskysexualbehaviourareallcloselyassociatedwiththe incidenceofSTIsinyoungpeople.16Athirdfactormightbe
thelimitedscreeningandtreatmentopportunitiesinwestern FrenchGuiana.Indeed,CTandNGscreeninginSTIclinicsonly startedin2017.Moreover,nationalguidelinesdonot recom-mendNGandCTscreeningforpregnantwomen(nevertheless, somedoctorsandmidwivesofferitintheirinitialassessment inFrenchGuiana).Thesefactorscombinedmayleadtohigh numberofunrecognizedinfectedmenorwomenwhich pro-videsareservoirforspreadingtheinfectiontotheirpartners viasexualcontacts.Ononehand,thesefindingsindicatethe needfordisseminatinginformationabouttheriskfactorsfor CTorNG,andmorebroadlyforSTIs.Ontheotherhand,there isaneedtoincreaseopportunitiestoscreenandtreatthese infections.
InFrance,screeningforCTorNGinextragenitalsitesis recommendedforMSMandinbothsexesdependingon sex-ual practicessuch asanal sex. However, literaturereviews reported that anorectal and pharyngeal infections do not appeartoberelatedtoreportedanalintercourse.17Moreover,
accordingtoTrebachetal.1810–25%ofallCTand20–40%of
allGNcasesinwomenaremissedwithstandard cervicovagi-nalorurinescreening.Wefoundsimilarresultsinourstudy with15.1%and30.3%ofCTand NGextragenital infections, respectively.Pharyngealandanalscreeningsseemimportant inordertodetectall infections.However,theclinicalharm ofextragenitalinfections,theirroleinsustainedtransmission andthecost-effectivenessandpublichealthimpactofsuch screeningareareasthathaveyettoberesearched.19
Inordertoreducecostsfromscreeningallsites,wepooled thesamplesfromthethreesites,althoughthisstrategydoes notallowdifferentiationbetweentheinfectedsites.However, thetreatmentisthesameregardlessofthesiteofinfection. Sultanetal.studiedthepoolingofself-takensamplesina pop-ulationofMSMpatients.20Theyfoundnostatisticaldifference
inthesensitivityofpooled-sitetesting(92%)vs.non-pooled testing(96%)fordetectingCTinfections.Conversely,the sen-sitivityofpooled-sitetestingforNGinfectionsdidnotperform
as well (90%vs. 99%). The lower performanceindetecting CTandNGmaybeduetosamplingerrorsorlowerbacterial loadinpharyngealinfections.Inourstudy,theprevalencesof CTinfectionweresimilarbetweenpooledornon-pooled test-ing.Theprevalenceswere slightlyhigherusingnon-pooled samplesforNGinfections,butthedifferencewasstatistically significant(15.6%vs.9.5%,p-value=0.11).
Themainlimitationofthisstudy may berelated tothe relativelyreducedsamplesize,togetherwithpossiblesocial biases in theresponses tothe questionnaire.Furthermore, thenumberofindividualsinsomesubgroupsmayhavebeen insufficient toidentifyfactors significantly associatedwith infections.Furtherlarge-scalestudiesinothercontextsand inthegeneralpopulationshouldbedesigned.
Thehighprevalencefoundinourstudyhelpstoincrease thevisibilityoftheproblemoftheseSTIsinFrenchGuiana and reinforcesthe importance ofdevelopingSTI screening opportunitiesforpopulationsingeneraland,especially,for themostvulnerable.Werecommendalarge-scalescreening strategyforthepopulationinFrenchGuiana,regardlessofage orsexualpractices.Consideringthehighrateofpregnancyin thisFrenchdepartment,antenatalscreeningwouldbe bene-ficialtodecreasemorbidityamongstwomenthemselvesbut alsotopreventvertical(infant)andhorizontal(partner) trans-mission.Morebroadly,sexeducationneedstobeofferedfor youngpeople.Consideringthemultiplevulnerabilitiesinour population, actionstofightSTIs mustbesupported bythe engagementandstrategicvisionattheregionalandnational levels.
Funding
TheARS-Guyane(FrenchGuianaRegionalAgencyofHealth) whofinancetheclinic,didnotparticipateinthewritingofthe article.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
The authors would like to thankthe team working in the STIclinic:DominiqueBeloeil,KellyNesmon,FannyLaurent, Gaic Briolet,LauriettaFowell,Marie-ClaudeBiswana, Pascal Sélé, and theARS-Guyane (FrenchGuianaRegional Agency of Health), who finance the clinic.The authors alsothank MichaelMillerforhiskindhelpintranslatingthearticle.
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