Characteristics of gonorrhea and syphilis cases among the Roma ethnic group in Belgrade, Serbia

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

The

Brazilian

Journal

of

INFECTIOUS

DISEASES

Original

article

Characteristics

of

gonorrhea

and

syphilis

cases

among

the

Roma

ethnic

group

in

Belgrade,

Serbia

Milan

Bjeki´c

a

_,

_Hristina

_Vlajinac

b,∗

,

Sandra ˇSipeti´c-Grujiˇci´c

b

a_City_Institute_for_Skin_and_Venereal_Diseases,_Belgrade,_Serbia

b_University_of_Belgrade,_Faculty_of_Medicine,_Institute_of_{Epidemiology,}_Belgrade,_Serbia

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o

Articlehistory:

Received12November2015 Accepted3May2016 Availableonline6June2016

Keywords: Romapopulation Syphilis Gonorrhea Serbia

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b

s

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Background:TheRomaethnicgroupisthelargestandmostmarginalizedminorityinEurope, believedtobevulnerabletosexuallytransmittedinfections.

Aim: Thepurposeofthestudywastoinvestigatefrequencyandcharacteristicsofgonorrhea andsyphilisamongtheRomapopulationinBelgrade.

Methods:DatafromtheCityInstituteforSkinandVenerealDiseasestowhichallgonorrhea andsyphiliscasesarereferredwereanalyzed.

Results:Duringtheperiodof2010–2014sexuallytransmittedinfectionsweremorefrequent amongRomathaninrestofBelgradepopulation.AveragepercentagesofRomaamongall reportedsubjectswithsyphilisandthosewithgonorrheawere9.6%and13.5%,respectively, whilethepercentageofRomainthetotalBelgradepopulationwasabout1.6%.Romawith syphilisandgonorrheaweremorefrequentlymen(75%),mostfrequentlyaged20–29years (43.4%),nevermarried(64.5%),withelementaryschoolorless(59.2%),unemployed(80.3%), andheterosexual(89.5%).AmongRoma10.5%weresexworkersand68.4%didnotknow thesourceoftheirinfection.SignificantdifferencesbetweenRomacasesandothercasesin BelgradeinallcharacteristicsobservedwereinagreementwithdifferencesbetweenRoma populationandthetotalpopulationofSerbia.

Conclusion: ThepresentstudyconfirmedthevulnerabilityoftheRomapopulationtosexually transmittedinfections.

Introduction

TheRomaareEurope’slargestandmostvulnerableminority. Intotal,about7–9millionRomaliveinEuropeand approxi-mately70%ofthemliveincountriesofCentralandEastern EuropeandthoseoftheformerSovietUnion.1

∗ _{Corresponding}_author_.

E-mailaddress:kristiv@eunet.rs(H.Vlajinac).

Accordingtothepopulationcensusin2011thetotal num-berofdeclaredRomainSerbiawas147,604whichaccountsfor 2.05%ofthepopulationinSerbia.Thehighestconcentration ofdeclaredRomainSerbiaisinBelgrade,thecapitalandthe largestcity,wherethereare27,325or18.5%oftheirtotal num-ber,and1.6%ofthetotalpopulationofBelgrade.2_The_Roma

minorityisthemostvulnerableandmarginalizedinthefield

http://dx.doi.org/10.1016/j.bjid.2016.05.004

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ofhealthbecauseofextremepoverty,improperhygiene,bad nutrition,undignifiedlivingconditions,highunemployment rate and lack of education.2,3 _{Discrimination} _in _accessing

healthcareserviceshaveanadditionalnegativeimpacton theirhealth.

Romamaybeathighriskforsexuallytransmitted infec-tions(STIs)becauseoftheirriskysexualbehavior.According toaninvestigationconductedamongRomayouth(aged15–24 years)inSerbiaduringtheyear2010,riskysexualbehaviors were highlyprevalent,especiallyamongmale subjects.4 _In

Belgrade,outofmaleRomayouth, 36.2%had sexualdebut beforetheageof15years,53.9%hadmorethanonesexual partnerinthe pastyear,11.5%hadengagedincommercial sex,and4.0%reportedhavinganalsexwithothermen.4

STIs are a major global cause of acute illness, infertil-ity,long-termdisabilityanddeathwithseriousmedicaland psychologicalconsequences amongpeople. Gonorrhea and syphilisare common bacterial venereal diseases and their reportingiscompulsoryinSerbia.Duringtheperiod2010–2014 inBelgradesyphilisincidenceincreased182.2%from2.25per 100,000in2010to4.4per100,000in2014,andgonorrhea inci-denceincreased226.2%from2.56per100,000in2010to5.79 per100,000in2014.5

Thepurposeofthisstudywastopresentgonorrheaand syphiliscasesamongRomawhosoughttreatmentattheCity InstituteforSkinandVenerealDiseasesinBelgradeduringthe periodof2010–2014,andtodescribetheirdemographic char-acteristics.Reportingongonorrheaandsyphilisiscompulsory inSerbia,andinBelgradeallreportedcasesweretreatedin theaforementionedInstitutewhichisanexclusivetreatment center.Thereispossibilitythatsomepatientsarereferredto privatephysicians,butthesecasesareusuallynotreported.

Wealsocomparedgonorrheaandsyphiliscasesinorderto identifyanydistinctneedforprevention,diagnosis,screening, orforotherpublichealthmeasuresforthesediseasesofthe Romapopulation.

Methods

Patients withsymptoms ofsexually transmittedinfections were referred to the City Institute for Skin and Venereal DiseasesinBelgrade,bytheirprimarycareprovidersbetween January2010andDecember2014.Theirdiagnoses(gonorrhea andearlysyphilis)attheinitialvisitwerenoted.Alldiagnoses werebasedonpatienthistoryandphysicalexaminationand were confirmed bylaboratory analyses. Casedefinitions of gonorrhea and syphiliswere inline withSTD Surveillance casedefinitions,6_and_updated_definitions_for_gonorrhea_and

syphilis.7 _For _gonorrhea _it _was _required_isolation_of

Gram-negative intracellular diplococci by culture from a clinical specimen(aurethralsmearobtainedfromamaleoran endo-cervical smear obtained from a female). Requirements for syphiliswereasfollows:forprimarysyphilis(PS),ulcersand reactive treponemal (Treponema pallidum hemagglutination assay–TPHA)andnontreponemal(VenerealDiseaseResearch Laboratory–VDRL)serologictests;forsecondarysyphilis(SS), clinicalmanifestationsofthis stagewithbothreactive tre-ponemaltestandanontreponemaltiter≥4;forearlylatent syphilisbothreactive treponemalandnontreponemal tests

andanyofthefollowingcriteriawithinthepast12months: documented seroconversionor fourfold or greater increase intiterofnontreponemaltest, documentedseroconversion onatreponemaltest,ahistoryofsymptomsconsistentwith adiagnosisofPSorSS,sexualexposuretoapersonwithPS, SSorearlylatentsyphilis,andsexualdebutwithinthelast 12months.

The dataon basicdemographic characteristics ofRoma patients(age,sex,maritalstatus,education,workingstatus) wereretrospectivelyabstractedfromtheircharts.Dataabout possible source of infection as well as sexual orientation, providedontheofficialformfornotificationofsyphilisand gonorrhea,werealsoanalyzed.

Intheanalysisofdata,proportionswerecomparedusing 2testandFisher’sexacttest.Allp-valueswerebasedon two-tailedtests,andp<0.05wasconsideredassignificant.

Themanuscriptwasreviewedandapprovedbythe respon-sibleauthoritiesofCityInstituteforSkinandVenerealdisease inBelgrade.

Results

Thefrequencyofsyphilisand gonorrheaamongRomaand otherethnicgroupsofBelgradepopulationtakentogetherare presentedinTable1.Duringtheperiodof2010–2014theRoma accounted for3.4%to17.1%(anaverageof9.6%) out ofall subjectsregistered withsyphilisandfor11.7%to18.8%(an average of13.5%)out ofall registeredpatients with gonor-rhea.Consideringthat thepercentageofRomainthetotal Belgradepopulationwasabout1.6%,bothsyphilisand gon-orrheaweremorefrequentamongRomacomparingwiththe restofBelgradepopulation.

Romawithsyphilisandgonorrheaweremorefrequently men (75%), the majority aged 20–29 years (43.4%), never married(64.5%),withelementaryschoolorless(59.2%), unem-ployed(80.3%),andheterosexual(89.5%).Amongthem10.5% weresexworkersand68.4%didnotknowthesourceoftheir

Table1–Numberofsyphilisandgonorrheacasesin

RomaandallotherethnicgroupsofBelgradepopulation

registeredatCityInstituteforSkinandVenereal Diseases,Belgrade,2010–2014. Year Roma Number(%) Otherethnic groups Number(%) Total Number Syphiliscases 2010 3(9.7) 28(90.3) 31 2011 1(3.4) 28(96.6) 29 2012 6(17.1) 29(82.9) 35 2013 3(10.3) 26(89.7) 29 2014 4(7.4) 50(92.6) 54 Total 17(9.6) 161(90.4) 178 Gonorrheacases 2010 5(12.5) 35(87.5) 40 2011 9(18.8) 39(81.2) 48 2012 14(14.9) 89(85.1) 94 2013 16(11.7) 121(88.3) 137 2014 15(12.6) 104(87.4) 119 Total 59(13.5) 379(86.5) 438

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Table2–Characteristicsofsyphilisandgonorrheacases inRomaandallotherethnicgroupsofBelgrade

populationregisteredatCityInstituteforSkinand VenerealDiseases,Belgrade,2010–2014.

Characteristics Syphilisandgonorrhea cases,number(%)

pvaluea

Roma Otherethnic groups Sex 0.030 Male 57(75.0) 458(84.8) Female 19(25.0) 82(15.2) Age,years <0.001 ≤15 5(6.6) 1(0.2) 16–19 14(18.4) 16(3.0) 20–29 33(43.4) 168(31.1) 30–39 14(18.4) 249(46.1) 40–49 10(13.2) 60(11.1) 50–59 0(0.0) 29(5.4) 60+ 0(0.0) 17(3.1) Maritalstatus <0.001 Nevermarried 49(64.5) 444(82.2) Married 27(35.5) 81(15.0) Divorced 0(0.0) 15(2.8) Education <0.001 ≤Elementary 45(59.2) 44(8.1) Secondary 31(40.8) 432(80.0) High 0(0.0) 64(11.8) Workingstatus <0.001 Employed 15(19.7) 279(51.7) Unemployed 61(80.3) 149(27.6) Pupil/student 0(0.0) 94(17.4) Retired 0(0.0) 18(3.3) Sexualorientation <0.001 Heterosexual 68(89.5) 344(63.7) Homosexual 8(10.5) 196(36.3) Beingsexworker <0.001 Yesb ₈_(10.5) ₁_(0.2) No 68(89.5) 539(99.8) Sourceofinfection <0.001 Known 24(21.6) 314(58.1) Unknown 52(68.4) 226(41.9)

a _According_to_chi_square_test_or_Fisher’s_exact_test. b _All_patients_who_declared_to_be_sex_workers_were_women.

infection(Table2).Thereweresignificantdifferencesbetween Romacasesand other casesinall characteristics observed (Table 2). Roma cases were younger, less educated, more frequently married, and unemployed. Among Roma cases thereweremoresexworkersandgreaterpercentagedidnot knowthesourceofinfection.Althoughwomenwereminority amongallcases,amongRomathereweresignificantlymore womenincomparisonwithothercases.Romalessfrequently declaredthemselvesashomosexual.

Some characteristics of syphilis and gonorrhea cases amongtheRomapopulationarepresentedinTable3.In com-parison with gonorrhea patients, those with syphilis were significantlymorelikelyto behomosexual(23.5% vs.6.4%,

p<0.05)andsexworkers(35.3%vs.3.4%,p<0.001),andmore

Table3–Characteristicsofsyphilisandgonorrheacases

amongRomaofBelgradepopulationregisteredatCity

InstituteforSkinandVenerealDiseases,Belgrade, 2010–2014.

Characteristics Syphiliscases (n=17) Gonorrhea cases(n=59) pvaluea Number(%) Number(%) Sex 0.080 Male 10(58.8) 47(79.7) Female 7(41.2) 12(20.3) Age,years 0.054 ≤15 0(0.0) 5(8.5) 16–19 5(29.4) 9(15.2) 20–29 4(23.5) 29(49.2) 30–39 3(17.7) 11(18.6) 40–49 5(29.4) 5(8.5) Maritalstatus 0.550 Nevermarried 12(70.6) 37(62.7) Married 5(29.4) 22(37.3) Education 0.601 ≤Elementary 11(64.7) 34(57.6) Secondary 6(35.3) 25(42.4) Workingstatus 0.348 Employed 2(11.8) 13(22.0) Unemployed 15(88.2) 46(78.0) Sexualorientation 0.047 Heterosexual 13(76.5) 55(93.2) Homosexual 4(23.5) 4(6.4) Beingsexworker <0.001 Yes 6(35.3) 2(3.4) No 11(64.7) 57(96.6) Sourceofinfection 0.046 Known 2(11.8) 22(37.3) Unknown 15(88.2) 37(62.7)

a _According_to_chi_square_test_or_Fisher’s_exact_test.

frequentlydidnotknowthesourceoftheirinfection(88.2% vs.62.7%,p<0.05).Patientswithsyphiliswerealsoolderthan patientswithgonorrhea,butthisdifferencewasatborderline ofsignificance(p=0.054)–Table3.Primarysyphiliswas diag-nosedinfourcases,secondarysyphilisinother fourcases, andninecaseswereclassifiedasearlylatentsyphilis.

Discussion

TheWorldHealthOrganizationestimatedthatin2008there were10.6millioncasesofsyphilisand106.1millioncasesof gonorrheaamongadultsglobally.8_Syphilis_and_gonorrhea_are

commonlytransmittedthrough sexualcontact(i.e. genital-genital, genital-anorectal, oro-genital or oro-anal contact). Moreover,syphilishasahighertransmissionratethan gonor-rheaandcanbealsotransmittedbybloodorthroughvertical transmissionfromaninfectedmothertoherbaby.9_Both

dis-eases can be followed byserious complications. Untreated cervical gonorrhea inwomencan leadtopelvic inflamma-torydisease,ectopic pregnancyand infertility.10 _Syphilis_is

asystemicinfectionandmayleadtodevastating cardiovas-cularandneurologicalcomplications.Ifleftuntreatedduring

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pregnancy, syphilis may contribute tostillbirth or preterm laborandcausecongenitalchildinfection.11_Syphilis_may_also

increasetheriskofHIVtransmissionandacquisitionby caus-inggenitalulcers.12

Asalreadymentionedtheincidenceofsyphilisand gon-orrhea increasedin Belgrade during the period 2010–2014. BothsyphilisandgonorrheaweremorefrequentamongRoma comparedtotherestofBelgradepopulation.Thereisno pre-viousdataaboutthefrequencyofgonorrheaamongtheRoma populationinBelgrade,butinastudyconductedinthiscity in2012among207Romayouthaged15–24yearsthe preva-lenceofsyphiliswas1%.13_According_to_Gyarmathy_et_al._the

prevalenceofsyphilisamongRomainBudapest was 2%.14

Among286Romatestedforsexuallytransmitteddiseasesin Sofia,21.7%hadatleastonedisease;4.5%hadgonorrheaand 3.5%hadsyphilis.15_Other_study_in_Bulgaria_revealed_that_3.7%

oftheRomahadgonorrheaandnosyphiliswasdetected.16

Accordingtotheresultsofaretrospectivecohortstudyina Romagroupperformedin Campde laBota, Barcelona,the incidenceofAIDSwas104casesper100,000person-yearsof follow-up.17

InthepresentstudytheRomaweresignificantlydifferent from other cases registered in Belgrade in all characteris-ticsobserved. Theywere younger, lesseducated and more frequentlyunemployed,which isinagreementwith differ-encesbetweentheRomapopulationandthetotalpopulation ofSerbia.Accordingtodatafromthe2011census,the aver-ageageoftheSerbianpopulationwas42.2yearsandthatof theRomapopulationwas27.8years.2_The_Roma_who_lived

intownswereevenyoungerbecauseofmigrationofyoung Romatourbansettlement.Accordingtosamedata,15.1%of theRomawere illiterate and about80% had incompleteor completeelementaryschoolvs. 2.0%and 32%,respectively, ofthewholeSerbianpopulation.Unemploymentamongthe Romawasthree-foldhigherthanthetotalpopulationof Ser-bia.IneasternEuropeancountriestheRomawerefoundto beamongthepoorest,withverylowlevelofeducationand withhighrateofunemployment.15_Knezevic_stated_that_the

RomainBelgradearetheethnicgroupthatis“most vulnera-ble,segregated,livingmostlyinslams,showingnointerestin improvingtheirsocialposition”.18_In_such_a_situation_it_is_not

surprisingthat10.5%oftheRomacases,andonly0.2%ofother cases,declaredthemselvesassexworkers,whichcanpartly explainwhyasignificantlygreaterpercentageofRomacases didnotknowthesourceofinfection.Romacaseswere sig-nificantlymorelikelytobesexworkerswhichcanexplainthe higherpresenceofwomenamongRomacases(25%)compared toothercases(15.2%).Accordingto ˇSipeti´cetal.Romasexual workersinSerbiahadthefirstsexualintercoursesignificantly moreoftenbeforetheageof14,38.5%ofthemneverornot alwaysusedcondomwiththeircommercialsexpartnersand almost20%hadsomeSTIinthepastsixmonths.19_They_had

averypoorknowledgeaboutthemeansofHIVtransmission, too.

AsitcouldbeexpectedbothRomaandallothersyphilis andgonorrheacasesweremorefrequentlymen.Gender deter-minesSTIrisksexualbehaviorpatterns,withmenbeingthe mostfrequentlyaffected,but notonlyamongRomacases, atleastnotinSerbia.Traditionally,menhave,moreorless, greatersexualfreedomcomparedtowomen.Inthepresent

studywehavenodataaboutriskysexualbehavior,suchas age of the first sexualintercourse, number ofsexual part-ners,frequencyofcondomuse,andsoon,whichcouldhave helpedtobetterunderstandthedifferences.Asalreadystated, astudyconductedinSerbiaamongtheRomayouthhasshown thatriskysexualbehaviors,suchasearlysexualdebut, mul-tiple sexpartnersand lackofconsistentcondomuse were veryfrequentandtheyweremuchhigheramongyoungRoma in Serbiathan in the generalSerbian youth.4 _In_the _same

studyHIV-relatedknowledgewasloweramongRomayouth. StudiesconductedinBulgariaalsoreportedhigh-risksexual behaviorsamongRomamen.16,20 _According_to_their_results

59%ofRomamenhadmultiplesexpartners,andover52% ofthemreportedunprotectedintercoursewithcasualorwith multiplepartnersduringthelastthreemonths.Inthestudy conductedinBudapest82%oftheRomadidnotuseacondom withtheirmainpartner.14_Our_findings_that_{significantly}_lower

percentageoftheRomacasesthantheothercasesdeclared themselves as homosexual are in line with other studies. AlthoughveryfewRomamenidentifiedtheirsexual orienta-tionashomosexual51.9%and59%ofthemreportedlifetime same-sex activities.16,20 _Nearly_two-thirds _of_men_who _had

unprotectedanalsexwithothermenreceivedmoneyor valu-ablesinexchangeforsexandthe majorityofthem(94.1%) reportedbeingtheinsertivepartner.16

Inthepresentstudy,incomparisonwithRomacaseswith gonorrhea, Roma patients with syphilis were significantly more likelyto behomosexual, sex workers,and more fre-quentlydidnotknowthesourceoftheirinfection,whichisin linewithfactthatsyphilisismorefrequentlyreportedamong menwhohavesexwithmenandsexualworkers,worldwide.8

Routinetestingforsyphilisshouldbeencouragedandoffered toRomasexworkersandMSM.

Thecriticalfeatureofouranalysisistheaccuracyofdata. Itisreasonabletoassume thatthe incidencesofboth dis-eases are underestimated, since there is a possibility that someofthepatientsdonotvisitphysiciansandsome physi-ciansdonotreportallofthecases.Thefactthatsomepatients couldgotoprivatephysicians,whichforbeingexpensivemay bemoreaffordable bynon-Romapatientsand thusatleast partlyexplainthe overrepresentationofRomacasesatthe Institute.

Insummary,thepresentstudyconfirmedthe vulnerabil-ity ofthe RomapopulationtoSTIs.Syphilisand gonorrhea weremuchmorefrequentamongtheRomathantherestof the population inBelgrade duringtheperiod of2010–2014. Theconsequencesofthegovernment’seffortstoimprovethe economicstatusoftheRomapopulationandtohastentheir socialintegrationcannotbeexpectedsoon.Itseemsthatonly the implementation ofvarious modelsofhealth education couldgivegoodresultsinSTIspreventionrelativelyquickly. RiskreductionmessagestargetingtheRomapopulationare more important than ever. In addition, condom distribu-tion and promotion should be an important part of their counseling.

Conflicts

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