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High prevalence of HTLV-I infection in Mashhad, Northeast Iran: A population-based seroepidemiology survey

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High prevalence of HTLV-I infection in Mashhad, Northeast Iran: A population-based seroepidemiology survey
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   JournalofClinicalVirology 52 (2011) 172–176 ContentslistsavailableatScienceDirect  Journal   of    Clinical   Virology  journalhomepage:www.elsevier.com/locate/jcv High   prevalence   of    HTLV-I   infection   in   Mashhad,   Northeast   Iran:A   population-based   seroepidemiology   survey Houshang   Rafatpanah a , b ,   Mohammad   Reza   Hedayati-Moghaddam a , ∗ ,   Farhad   Fathimoghadam a ,Hamid   Reza   Bidkhori a ,   Seyed   Khosro   Shamsian c ,   Sanaz   Ahmadi c ,   Leila   Sohgandi c ,Mahmoud   Reza   Azarpazhooh a , d ,   Seyed   Abdolrahim   Rezaee a , b ,   Reza   Farid a , e ,   Ali   Bazarbachi f  a ResearchCenterforHIV/AIDS,HTLVandViralHepatitis,IranianAcademicCenterforEducation,Culture&Research(ACECR),MashhadBranch,Mashhad,Iran b InflammationandInflammatoryDiseasesResearchCentre,SchoolofMedicine,MashhadUniversityofMedicalSciences,Mashhad,Iran c CenterofPathologicalandMedicalDiagnosticServices,IranianAcademicCenterforEducation,Culture&Research(ACECR),MashhadBranch,Mashhad,Iran d DepartmentofNeurology,GhaemHospital,FacultyofMedicine,MashhadUniversityofMedicalSciences,Mashhad,Iran e  AllergyResearchCenter,SchoolofMedicine,MashhadUniversityofMedicalSciences,Mashhad,Iran f  DepartmentofInternalMedicine,AmericanUniversityofBeirut,Beirut,10Lebanon a   r   t   i   c   l   e   i   n   f   o  Articlehistory: Received30March2011Receivedinrevisedform3July2011Accepted5July2011 Keywords: HTLV-IinfectionSeroepidemiologyRiskfactorsGeneralpopulationMashhadIran a   b   s   t   r   a   c   t Background:   Mashhad,   in   the   northeast   of    Iran   has   been   suggested   as   an   endemic   area   for   human   Tcelllymphotropic   virus   type   I   (HTLV-I)   infection   since   1996. Objectives:   We   performed   acommunity-based   seroepidemiology   study   to   examine   the   prevalence   andriskfactors   for   HTLV-I   infection   in   the   city   of    Mashhad. Studydesign:   Between   May   and   September   2009,   overall   1678   subjects   from   all   the   12geographicalarea   of    Mashhad   were   selected   randomly   by   multistage   cluster   sampling   for   HTLV   antibody.   The   studypopulation   included   763   males   and   915   females,   with   the   mean   age   of    29.1   ±   18.5   years.   1654   serumsamples   were   assessed   for   HTLV   antibody   using   ELISA   and   reactive   samples   were   confirmed   byWesternblot   and   PCR. Results:   The   overall   prevalence   of    HTLV-I   infection   in   whole   population   was   2.12%   (95%   CI,   1.48–2.93)with   no   significant   difference   between   males   and   females   (  p =0.093)   and   the   prevalence   of    HTLV-IIseropositivity   was   0.12%   (95%   CI,   0.02–0.44).TheHTLV-I   Infection   was   associated   with   age   (  p   <0.001),   marital   status   (  p   <   0.001),   education(  p   =   0.047),   and   history   of    blood   transfusion   (  p   =   0.009),   surgery   (  p   <0.001),   traditional   cupping   (  p =   0.002),andhospitalization   (  p =   0.004).   Inlogistic   regression   analysis,   age   was   the   only   variable   that   had   a   signif-icant   relation   with   the   infection   (  p =0.006,   OR    =   4.33). Conclusions:   Our   results   demonstrated   that   Mashhad   still   remains   an   endemic   area   for   HTLV-I   infec-tion   despite   routine   blood   screening.   Thus,   further   strategies   are   needed   for   prevention   of    the   virustransmission   in   whole   population. © 2011 Elsevier B.V. All rights reserved. 1.Background HumanTcelllymphotropicvirustypeI(HTLV-I)isamemberofRetroviridaefamilywhichhasbeenassociatedwithtwo   maindiseases;HTLV-I-associatedmyelopathy/tropicalspasticparapare-sis(HAM/TSP)andadultTcellleukemia(ATL). 1,2 Theprevalenceof HTLV-Iinfectionworldwideisestimatedtobe15–20millions. 3 The ∗ Correspondingauthorat:ResearchcenterforHIV/AIDS,HTLVandViralHepati-tis,ACECR-MashhadBranch,UniversityCampus,AzadiSq.,P.O.Box91775-1376,Mashhad,Iran.Tel.:+985118821533;fax:+985118810177. E-mailaddresses: drhedayati@acecr.ac.ir,drhedayati@yahoo.com(M.R.Hedayati-Moghaddam). mainendemicregionsofHTLV-IaresouthwesternJapan,partsof Africa,SouthAmericaandtheCaribbeanbasin. 4 MorerecentlythenortheastofIran,Mashhad,hasbeensug-gestedasanewendemicregionofHTLV-I.In1996,TheprevalenceofHTLV-IinfectioninMashhadwasestimatedtobe ∼ 2%inblooddonors. 5 Similarly,Safaietal.,reportedtheprevalenceof3%inhealthyindividualswhoreferredtogeneralmedicallaboratoriesorbloodbanks. 6 Mashhad,thecapitalofRazaviKhorasanprovince,isthesecondlargestcityinIranwith ∼ 2.5millionpopulationinthelastcensusin2006. 7 Moreover,itisthoughtthatmorethan20millionpersonsayearmakethepilgrimagetoMashhad,asoneof theholiestcitiesintheworld.HTLV-Iseroprevalenceratesaresexandagedependent,increasingwithageandhigherinfemalesthanmales. 8–10 Discrepanciesinsexualbehaviorandbreast-feeding 1386-6532/$–seefrontmatter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jcv.2011.07.004  H.Rafatpanahetal./JournalofClinicalVirology 52 (2011) 172–176 173 practicescouldcontributetotheheterogeneityinprevalenceratesindifferentcountries.Studieshaveshownadifferenceintheabso-luteprevalenceratesinJapan,JamaicaandtheUSA;however,thesecountriesdemonstratethesamepatternofageandsex-specificprevalence. 9–11 LowersocioeconomicstatussuchaseducationisshowntobeassociatedwithHTLV-Iinfectioninbothendemicandnon-endemicareas. 9,12–15 Furthermore,ithasbeensuggestedthatsocialandenvironmentalfactorsmay   influencetheHTLV-Itransmissionnotonlyinendemiccountriesbutalsoacrosstheworld. 16,17 Inthepreviousstudy,wedemonstratedthedeclinetendencyintheseropositivityofHTLV-IamongblooddonorsinMashhadto0.45%intheyearsof2004–2006. 18 However,thereisnoinformativedataregardingwhethertheprevalenceratesofHTLV-Iinfectioninthepopulationhaschangedsince1996.Furthermore,theinfluenceoffactorssuchasage,sexandsocioeconomicstatus,whichcouldcontributetoHTLV-Iinfection,hasnotbeenstudiedinthisendemiccitysofar. 2.Objectives Inthepresentcross-sectionalstudyweinvestigatedthepreva-lenceratesofHTLV-IinfectionandsomerelatedfactorsinthegeneralpopulationofMashhad. 3.Studydesign  3.1.Studypopulation Fromall12municipalityareasofthecitywithanestimated2.5millionresidents,1678individualswereselectedbymultistageclustersamplingbetweenMay   andSeptember2009.Thesamplingmethodwasdescribedindetailselsewhere. 19 Briefly,eachareaincludedsomedistrictsandmanysubdivisions.Someblockswerechosenfromonesubdivisionineverydistrict.About20householdsineachblockandonlyonepersonineachhouseholdwereselectedrandomly.ThepilgrimsandtravelerstoMashhadwerenotincludedinthissurvey.Informationregardingdemographiccharacteristicssuchassex,age,socioeconomicstatusanddataonmedicalhistoryincludingbloodtransfusion,dentistryprocedure,surgery,hospital-ization,andtraditionalcupping( Hijamat  )werecollected.Historyofbehavioralriskfactorssuchasunsafesexandintravenousdruginjectionwasnotinvestigatedduetoculturallimitations.ThestudywasapprovedbyResearchDeputyshipofIranianAca-demicCenterforEducation,Culture&Research(ACECR)regardingscientificandethicalissues.Informedconsentwas   obtainedfromallparticipantsandincaseofchildrenthewrittenconsentwassignedbytheirparents.  3.2.Serologicalassayandconfirmationtests Fiveml   ofbloodsampleswereobtainedfromeachindividual.Serumwasseparatedthroughcentrifugation,DNAwasextractedfromwholebloodcells,andbothsampleswerestoredat − 20 ◦ C.Serumsampleswerescreenedforthepresenceofanti-HTLV-IantibodieswiththeMP   DiagnosticsHTLVI/IIenzymelinkedimmunosorbentassay(ELISA)4.0(MP   BiomedicalsAsiaPacificPteLtd,Singapore)accordingtothemanufacturer’sinstructions.AllreactivesamplesonserologicscreeningweretestedfurtherbyWesternblot(WB)analysisaccordingtothemanufacturer’sinstructions(MP   DiagnosticsHTLVBlot2.4,MP   BiomedicalsAsiaPacificPteLtd,Singapore).Polymerasechainreaction(PCR)wasalsocarriedoutonallpositiveELISAsamplesforfurtherconfirma-tionofHTLV-Iinfection.Briefly,GenomicDNAwasextractedfromperipheralbloodmononuclearcells(PBMC)usinganavailablecommercialkit(Bloodminikit,Qiagen,Germany)andPCR amplificationwasperformedusingspecificprimersfor tax (5  -AGGGTTTGGACAGAGTCTT-3  and5  -AAGGACCTTGAGGGTCTTA-3  )and LTR regions(5  -CATAAGCTCAGACCTCCGGG-3  and5  -GGATGGCGGCCTCAGGTAGG-3  ).  3.3.Statisticalanalysis Descriptivedataweresummarizedasmean,standarddeviationand/orpercentsandwereanalyzedbySPSS16.0using Chisquare and t  tests.Binarylogisticregressionanalysiswas   usedtoestimatethepotentialriskfactorsforHTLV-Iinfection.Variablesintheequa-tionincluded:age(35andabovevs.<35),maritalstatus(widowedvs.others),Literacy(illiteratevs.literate),andhistoryoftransfu-sion,surgery,traditionalcupping,andhospitalization(yesvs.no).A  p value<0.05was   consideredstatisticallysignificant. 4.Results Thestudypopulationconsistedof1678individualsrangedfrom1to90years.Sevenhundredsixtythreeofthemweremales(45.5%)and915(54.5%)werefemales.Themeanageofmaleswas27.9 ± 19.0andforfemaleswas30.0 ± 18.0andthemaletofemaleratiowas   1.19.Twenty-fourpersonsrefusedbloodwithdrawalandwereexcludedfromsubsequentanalyses.Onethousandsixhun-dredandfifty-fourserumsampleswereanalyzedforanti-HTLVantibodies.IntheprimaryscreeningofthesamplesbyELISA,56(3.39%)werepositiveforHTLVantibodies.TheWB   resultsdemonstratedthat35(62.5%)outof56ELISApositivespecimenswereHTLV-Ipositive(includingtworeactivesamplesforbothHTLV-IandHTLV-II),foursamples(7.1%)wereindeterminateandHTLVpositivitywasnotconfirmedin17cases(30.4%).AccordingtotheWB   results,theoverallprevalenceoftheHTLV-Iinfectioninthepopulationstudywas   2.12%(35/1654)(95%CI,1.48–2.93),whileHTLV-IIpositivitywas   0.12%(2/1654)(95%CI,0.02–0.44).Inordertoconfirmtheinfectionfurther,allthe56positiveELISAsampleswerereexaminedbyPCRusingspecificprimersforHTLV-I.AlloftheWB   positivesamples,includingtwoHTLV-I/IIdualinfec-tionserumswereconfirmedtobeHTLV-I,whilethepresenceof viruswas   notconfirmedinnegativeandindeterminatesamples.TheHTLV-Iinfectionrateforfemaleswas   2.66%(24/903)andformaleswas1.46%(11/751).Nosignificantdifferencesinthesero-prevalencewereobservedbetweenmalesandfemales,althoughtheinfectionrateswere10timeshigherinfemalesolderthan65yearscomparedtomalesofthesameagegroup(23.08%vs.2.38%,  p =0.005)(Fig.1AandB).Bothtwo   caseswithHTLV-I/IIdualinfec-tionwerefemales;onewas29andother58yearsold.Seroprevalencewasassociatedwithage,maritalstatusandliteracy,increasingsignificantlyamongthoseolderthan35years(  p <0.001),illiterates(  p <0.001)andwidowedindividuals(  p <0.001)(Table1).Ontheotherhand,income,ethnicback- ground,employmentstatus,andplaceofbirthhadnosignificantimpactonHTLV-Iinfection.InadditionHTLV-Iinfectionwasasso-ciatedwiththehistoryofbloodtransfusion(  p =0.009),surgery(  p <0.001),traditionalcupping(  p =0.002),andhospitalization(  p =0.004)(Table2).Inlogisticregressionanalysis,age(  p =0.006,OR=4.33;95%CI,1.52–12.29)wastheonlyfactorthatcouldpredictsignificantlytheriskofinfection. 5.Discussion ThepreliminaryseroepidemiologyofHTLV-IinfectioninMash-had,Iranwas   reportedin1996. 5,6 However,theriskfactorsassociatedwithHTLV-Iinfectionhavenotbeenassessedsofar.  174  H.Rafatpanahetal./JournalofClinicalVirology 52 (2011) 172–176 Fig.1. SeroprevalenceofHTLV-IinfectionamonggeneralpopulationinMashhad,Iran,2009:(A)seroprevalencein903females;(B)seroprevalencein751males. Inthepresentstudy,wereporttheseroepidemiologyofHTLV-IinfectioninarepresentativesampleofindividualsofallagesselectedfromtheentiredistrictsinthecityofMashhad.Theover-allprevalenceofHTLV-Iinfectionobservedinourstudywaslowerthantheonereportedbythepreviousstudy.Threepercentof694bloodsamplesobtainedfromreferralstomedicallaboratoriesorbloodbankswereHTLV-Ipositive. 6 However,sexandagedistribu-tionofstudypopulationintheearliersurveywasnotdescribed,anditmightbeactuallydissimilartoourpopulation.Areduc-tionintheHTLV-Iprevalenceamongbloodbankdonorshasbeenshown.AnationwidesurveybyIranianBloodTransfusionOrgani-zation(IBTO)in1996showedthatMashhadhasthehighestHTLV-IinfectionratesinIran. 5 Followingtheseroepidemiologystudiesof HTLV-IinMashhad,theBloodBankscentersinKhorasanprovincesestablishedsystematicscreeningforHTLV-Iantibodiesinordertopreventthespreadofinfectioninthecountry.ThispracticeledtoasharpdropinHTLV-Iinfectioninblooddonationvolun-teerswhichhasbeenremarkablyillustratedinarecentstudyinMashhad. 18 Moreover,araiseinpublicknowledgeoninfectionssuchasHIV/AIDSoccurredintherecentyearscouldhavepartici-patedtothisdecliningtendencyofHTLV-Iinfection.We   demonstratedthatHTLV-Iinfectionincreaseswithageparticularlyamongthoseolderthan35years.Previousstudies  Table1 Socio-demographicfactorsrelatedtoHTLV-IInfectioninthegeneralpopulationof Mashhad,Iran.VariableNo.Positive(%)  p -ValueSexMale 7511.46Female9032.660.093Age   (years)<510305–142840.7015–244190.4825–34311 0.9635–441903.1645–541613.1155–641056.67 ≥ 658112.35<0.001Maritalstatus(peopleolderthan14)Single 4160.96Married 7742.84Widowed160Divorced 41 14.63<0.001Literacy(peopleolderthan5)Illiterate 1109.09Primary-secondaryschool(1–8yrs)6282.55Highschool(9–12yrs)4951.21Academic2650.38<0.001Employment(peopleolderthan14)Employed 489 2.25Unemployed6772.810.553Familyincome(millionRials a permonth)<38012.623–55441.84>5 224 1.340.410EthnicbackgroundFars 1424 2.25Turk1001.00Afghani 610Others b 543.700.446PlaceofbirthRazaviKhorasanProvince 1386 2.16OtherprovincesinIran2150.47Othercountries(Afghanistan,Iraq) 2700.182 a Approximately100U.S.$atthetimeofsurvey. b IncludingKord,Lor,Balooch,Turkman,Arab,etc. reportedthatHTLV-Iseroprevalenceincreaseswithage, 9,20–22 andishigherespeciallyamongsubjectsmorethan40years. 23 Fur-thermore,specificprevalenceofHTLV-IinfectioninthegeneralpopulationofSalvador,Brazil,anendemicareaofHTLV-Iinfec-tion,demonstratedanincreasinglineartrendwithage. 24 TheincreaseinHTLV-Iinfectionwithageandthelowseroprevalence  Table2 Non-sociodemographicriskfactorsrelatedtoHTLV-IInfectioninthegeneralpopu-lationofMashhad,Iran.VariableNo.Positive(%)  p -Value*TransfusionhistoryYes637.94No15451.880.009SurgeryhistoryYes5513.81No 10911.19<0.001DentistryprocedurehistoryYes3482.87No12801.800.206TattooinghistoryYes 53 1.89No15752.100.917TraditionalcuppinghistoryYes2334.72No14001.640.002HospitalizationhistoryYes6263.35No10151.280.004  176  H.Rafatpanahetal./JournalofClinicalVirology 52 (2011) 172–176 ethnicandsociodemographiccharacteristics.  JAcquirImmuneDeficSyndr  2003; 34 :527–31.25.   ArmahHB,Narter-OlagaEG,AdjeiAA,AsomaningK,GyasiRK,TetteyY.Sero-prevalenceofhumanT-celllymphotropicvirustypeIamongpregnantwomenin   Accra,Ghana.  JMed   Microbiol 2006; 55 :765–70.26.   KazanjiM,   GessainA.HumanT-cellLymphotropicVirustypesIandII(HTLV-I/II)inFrenchGuiana:clinicalandmolecularepidemiology. CadSaudePublica 2003; 19 :1227–40.27.   RouetF,FoucherC,RabierM,   GawronskiI,TaverneD,ChancerelB,etal.HumanT-lymphotropicvirustypeIamongblooddonorsfromGuadeloupe:donation,demographic,andbiologiccharacteristics. Transfusion 1999; 39 :639–44.28. PlancoulaineS,BuiguesRP,MurphyEL,vanBeverenM,   PouliquenJF,JoubertM,   etal.DemographicandfamilialcharacteristicsofHTLV-1infectionamonganisolated,highlyendemicpopulationofAfricansrcininFrenchGuiana. IntJ Cancer  1998; 76 :331–6.29.MaloneyEM,   RamirezH,LevinA,BlattnerWA.   AsurveyofthehumanT-celllymphotropicvirustypeI(HTLV-I)insouth-westernColombia. IntJCancer  1989; 44 :419–23.30.   EdlichRF,ArnetteJA,WilliamsFM.   GlobalepidemicofhumanT-celllymphotropicvirustype-I(HTLV-I).  JEmergMed   2000; 18 :109–19.31.   RouetF,Herrmann-StorckC,CouroubleG,DeloumeauxJ,MadaniD,StrobelM.   Acase-controlstudyofriskfactorsassociatedwithhumanT-celllym-photrophicvirustype-IseropositivityinblooddonorsfromGuadeloupe,FrenchWestIndies. VoxSang  2002; 82 :61–6.
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