Risk factors for incomplete vaccination in children less than 18 months of age attending the nurseries of day-care centres in São Paulo, Brazil

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attending

the

nurseries

of

day-care

centres

in

Sao

Paulo,

Brazil

Tulio

Konstantyner

a,∗

_,

_José

_Augusto

_de

_Aguiar

_Carrazedo

_Taddei

a

_,

_Laura

_Cunha

_Rodrigues

b

a_Universidade_Federal_de_São_Paulo,_R._Loefgreen_1647,_04040-032_São_Paulo,_Brazil

b_London_School_of_Hygiene_and_Tropical_Medicine,_Keppel_Street,_WC1E_7HT_London,_United_Kingdom

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received14April2011

Receivedinrevisedform1October2011 Accepted6October2011

Available online 18 October 2011

Keywords:

Riskfactors Day-carecentres Vaccination Vaccinecoverage Healthservicesaccessibility Infant

a

b

s

t

r

a

c

t

Toestimatetheproportionofchildreninday-carecentreswithincompletevaccinationandtoidentify associatedriskfactors,weconductedacross-sectionalstudyamong258childrenlessthan18months ofageattendingpublicandphilanthropicday-carecentresinthecityofSaoPaulo,Brazil.Interviews, bloodcollectionandanthropometrywereperformed.Unconditionallogisticregressionwasadjustedfor incompletevaccinationriskfactors.10.9%ofchildrenhadincompletevaccination.Childrenwhowere bornprematurely(OR=4.27;p=0.004),orweremalnourished(OR=4.99;p=0.049),orlivedin inade-quatehousing(OR=2.88;p=0.039),orwhosemothershadhadpoorprenatalcare(OR=4.98;p=0.040) weremorelikelytohaveincompletevaccination.Opportunitiesarebeingmissedtoidentifychildren withincompletevaccination;strategiestoenhancevaccinationcoverageshouldpayspecialattention totheneedsoffamilieslivingininadequatehousing;andhealthpromotionactionsinprimaryhealth facilitiesandday-carecentresshouldbeperformedasconcomitantactivities.

1. Introduction

Vaccinationisoneofthemostcost-effectivehealth interven-tions. It is estimated that over 2.5 million deaths are averted throughvaccinationeveryyear[1,2].

However, vaccine coverage rates are different according to health services accessibility and socio-economic and cultural characteristics [3]. Although immunization services have been strengthenedworldwide,thereiscontinuingconcernatthefailure toachievehighimmunizationcoverage[3–5].

BrazilhasperformedverywellwiththeProgramaNacionalde Imunizac¸õesasanintegratedprogrammeoftheglobal immuniza-tionstrategiesoftheWorldHealthOrganization(WHO),putting intopracticeroutines,campaignsandmassvaccinationwithfree vaccines[6].Despiteofitssuccess,therearestillongoingchallenges

[7].

One would expect vaccine coverage rates among children attendingnurseriesofday-carecentres(DCCs)inBraziltobehigh, becauseadequate vaccinationis a criterion for enrollment and nurseriesemployahealthprofessionalresponsibleforthehealth careofthechildren.

∗_{Corresponding}_author._Tel.:₊₅₅₁₁₅₅₃₉_1783;_fax:₊₅₅₁₁₅₅₃₉_1783.

E-mailaddresses:[email protected](T.Konstantyner),[email protected]

(J.A.d.A.C.Taddei),[email protected](L.C.Rodrigues).

Inordertogaininsightintotheseissuesweconductedastudy toestimatetheproportionofchildrenwithincompletevaccination andtoidentifyriskfactors.

2. Methods

Weuseddatafromtwosurveys(2004and2007)oftheProjeto CrechEficientewithchildrenlessthan18monthsofageattending public(directadministrationbythecity)andphilanthropic (indi-rectadministrationperformedbyphilanthropicinstitutions)DCCs ofSaoPaulocitywhichhavesimilaroperatingcharacteristicsand abidebyadmissionrulesguaranteeingcareforlow-income fami-lies.Actually,theyarescatteredthroughoutthecityandconstitute singleunpaideducationsystemavailableforearlychildhoodinall city.

Fig.1presentsthemethodologyfortheselectionofDCCs.Survey 1(2004)wasundertakeninthe54DCCsofthecentralregionand survey2(2007)inthe36DCCsofthesub-districtofSantoAmaro. ThemanagersoftheDCCswerecontactedbytelephonetoidentify whichwereeligible.Ofthese,47DCCswereexcludedfornot pos-sessinganursery,fourfornotshowinginterestinparticipatingand eightforhavebeeninvolvedinaprevioushealthresearch,resulting in13and18DCCsinsurveys1and2,respectively.

Those31DCCswerevisited bytheproject’sfield staffanda questionnairewasfilledoutwithinformationabouttheschool’s operating.Afterwards,theseDCCswererankedaccordingtothe existenceofthecharacteristicsofinterestforthedevelopmentof

Open access under the Elsevier OA license.

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Fig.1. Methodologyfortheselectionofpublicandphilanthropicday-carecentresofthemunicipalityofSaoPaulo,2surveys(2004and2007).

theproject[8].Thefollowingcriteriawereprioritisedinorderof decreasingvalue:numberofchildreninthenursery,numberof nurseryteachers,safetyoftheareafortheresearchersandease oftransportandaccesstothepremises.FiveandeightDCCswere selectedatsurveys1and2,respectively.

Theinitialpopulationof these13 selectedDCCs consistedof 274childrenlessthan18monthsofageattendingthenurseries. Thefollowingchildrenwereexcluded:fourwhowerenotpresent duringthefieldactivities;fivewhohadacutediseasesatthetimeof thesurveys;fivewithchronicconditions;andtwowhoseguardians didnotsigntheinformedconsentform.

Threeotherchildrenwereexcludedfromthemultivariate anal-ysis due to missing data. Therefore, 258 were studied in the univariateanalysisand255inthemultivariateanalysis,with sam-plelossesof5.8%and6.9%,respectively.

Interviewswiththemothers,anthropometryandbloodsamples drawnfromthechildrenbydigitalpuncturewereperformedinthe DCCs.

ForthemeasurementofHblevels,aportableHbphotometer (HemoCueHaemoglobinPhotometer®₎_was_used_[9]_._The_children

wereweighedonadigitalpaediatricscale,BPBabymodel,Filizola®

brandandtheheightwasmeasuredusingananthropometricruler, both with an internationalcertification of quality. The anthro-pometricproceduresadoptedarerecommendedinternationally. Z-scoreswereusedtoquantifynutritionaldisorders.The bench-marksadoptedwerethoseoftheWHO[10].

Theoutcomewasincompletevaccinationwhichwasdefined asachildwhodidnotreceivetheexpectedvaccinedosesforthe child’sageaccordingtotheBrazilianbasicvaccinationcalendar. Thatinformationwasascertainedandobtainedfromtheofficial vaccinationdocumentofeachchildduringthemother’sinterview. Toinvestigateassociationsachi-square(2₎_test_was_used._To

adjust for the confounding variables, multivariate analysiswas performedusing“stepwiseforward”technique.Theselection cri-teriaforinclusioninthefinallogisticmodelwereassociationwith

incompletevaccinationwithp<0.20.Alevelofp<0.05waschosen toindicatestatisticallysignificantassociation.

Populationattributablerate(PAR%)wascalculatedtoidentify theproportionofincompletevaccinationattributabletoeachrisk factor(p<0.100).

Childrenwithnutritionaldisordersorincompletevaccination werereferredtooutpatientcareintheDepartmentofPaediatrics oftheUniversidadeFederaldeSãoPaulo.Thestudywasapproved bytheethicsandresearchcommitteeofthesameUniversity.

3. Results

Wefoundthat10.9%(CI95%:7.3–15.3%)ofthechildren had incompletevaccination.

Table1presentstheprevalenceofincompletevaccinationin childrenaccordingtoriskfactorsandthePAR%.Childrenborn pre-maturelywere4timesmorelikelytohaveincompletevaccination (p=0.004)andtheattributableproportionwas20.2%.Childrenhad malnutrition,had siblingslessthan fiveyears ofageand living atinadequatehousingalsopresentedhigherriskstoincomplete vaccination,showingattributableproportionbetween8.1and29.4.

Fig.2presentsthemultiplelogisticmodelforriskfactorsfor incompletevaccination(p=0.0028)andPAR%ofthefourvariables thatexhibitedstatisticallysignificantassociationscontrolledfor sexandage.

Amongthesocioeconomicvariables,livingat“inadequate hous-ing”(unsuitableseweragesystemorwallsmadeofwood,indicating being part of a shanty town) was the first identified to com-posethelogisticmodel.Ofthevariablesindicatingindividualchild processes,“malnutrition”,“prematurity”and“poorprenatalcare” (motherhadnotattendedtheminimallyrecommendedfour ante-natalvisits)werealsoselectedtocomposethefinalmodel.

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Inadequatehousingb

Yes 258 21.2 (7/33) 2.62(1.01;6.75) 0.048 13.8

No 9.3 (21/225) 1.00

Avoidablehospitalization

Yes 258 16.7 (12/72) 2.12(0.95;4.75) 0.053 21.1

No 8.6 (16/186) 1.00

Weightatbirth(kg)

<2.5 256 22.2 (6/27) 2.69(0.98;7.37) 0.057 11.9

≥2.5 9.6 (22/229) 1.00

Prenatalcare(visits)

<4 256 33.3 (3/9) 4.44(1.05;18.86) 0.063 7.3

≥4 10.1 (25/247) 1.00

Exclusivebreastfeeding

<120 250 12.4 (22/178) 2.40(0.80;7.22) 0.081 44.0

≥120 5.6 (4/72) 1.00

Percapita<½MW

Yes 255 15.5 (13/84) 1.90(0.86;4.21) 0.083 20.2

No 8.8 (15/171) 1.00

Childage(months)

<13 258 8.2 (9/110) 0.60(0.026;1.39) 0.161 –

≥13 12.8 (19/148) 1.00

Maternaleducation(years)

<4 256 19.0 (4/21) 2.07(0.64;6.65) 0.184 –

≥4 10.2 (24/235) 1.00

Day-carecentres

Philanthropic 258 9.6 (16/166) 0.71(0.32;1.58) 0.260 –

Public 13.0 (12/92) 1.00

Oralironsupplements

Yes 258 12.5 (11/88) 1.29(0.57;2.88) 0.339 –

No 10.0 (17/170) 1.00

Haemoglobin(g/dL)

<11 258 11.8 (17/144) 1.25(0.56;2.79) 0.365 –

≥11 9.6 (11/114) 1.00

Motherunemployed

Yes 255 12.9 (4/31) 1.36(0.44;4.25) 0.391 –

No 9.8 (22/224) 1.00

Sex

Male 258 10.4 (14/135) 0.90(0.41;1.97) 0.475 –

Female 11.4 (14/123) 1.00

Maternalage(years)

<18 256 14.3 (1/7) 1.37(0.16;11.82) 0.560 –

≥18 10.8 (27/249) 1.00

CI=confidenceintervals;MW=minimumwage;PAR%=populationattributablerate. a_Fisher’s_exact_test.

b_Unsuitable_sewerage_system_or_walls_made_of_wood.

than 120 days, avoidable hospitalization and low birth weight (lessthan2.5kg)attendedtheselectioncriteriatocompoundthe logistic model (p<0.20); however, these werenot remained in becausetheylosttheirstatisticalsignificancewhenincludedinthe model.

4. Discussion

Only4factorswereindependentlyandsignificantlyassociated with incompletevaccination: prematurity, malnutrition, inade-quatehousingandpoorprenatalcare.ThesehavePAR%varying from7to20%.

The rate of incomplete vaccination have been shown to dependent on characteristics of the studied children [11,12].

Studies have shown there are many risk factors associated withsuboptimalcompliancetovaccinations whichare substan-tiallyrelatedtoparental–childhoodcharacteristicsandhealthcare structure–professionaldeterminants[13].

ItisworthnotingthatourstudyincludedDCCsselectedunder operationalease/conveniencecriteriawithalargenumberof chil-drenandlocatedinpoorbutinmoresafeareasofSaoPaulocity. Consequently,theresultsmaynotbegeneralizedtoDCCswitha smallstaffandlocatedinlesssafeareas,andthegroupofchildren isnotprobabilisticallyrepresentativeofthepopulationofchildren whoattendBrazilianDCCs.Therefore,theexternalvaliditymustbe consideredwithcaution.

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Fig.2.Multiplelogisticregressionwithoddsratiosandtheirrespectiveconfidence intervals(95%CI)forriskfactorsforincompletevaccinationamongchildrenlessthan 18monthsofageinpublicandphilanthropicday-carecentresofthemunicipality ofSaoPaulo,2surveys(2004and2007).

systemstoachievethegoaltokeepchildrenperfectlyprotected againstvaccine-preventableinfectiousdiseases.

Prematurityhadthelargestimpact,evenaftercontrollingfor low number of prenatal visits which was an associated factor alsoevidencedinthisresearchconsistentwithotherstudies[2]. Moreover,malnutritionalsowasidentifiedasassociatedfactorfor incompletevaccinationashasbeenshownbyliterature[13].These arelikelytoreflectcommondeterminantsofaccessibilitytochild healthcareservices[14].

Inadequatehousing(anindicatorofsocialdeprivation)hasalso beenpreviouslyreportedasassociatedwithincomplete vaccina-tion [11,15]. This is likely toindicate parental difficult to care theirchildrenappropriately,providingbasicvaccineswithlimited socioeconomicresource,eveninBrazil.

Thisstudydidnotinvestigatetheroleofmaternalanxietyshown tobeassociated withvaccinecoverage indeveloping countries

[16,17]anddidnotidentifyassociationbetweenincomplete vac-cinationandpercapitaincomeormaternalemployment,age,or education,incontrasttootherinvestigations[2,5,15].

Furthermore,thecalculationofthePAR%showedprematurity explainingthehighesteffectonincompletevaccination.However, itisunlikelythatthisconditionisitsdirectdeterminant,because guidelinesdonotrecommendpostponingvaccination(otherthan BCG)eveninprematureorlowweightbabies.

Indeed,prematurity,infantmalnutrition,inadequatehousing, poorprenatalassistanceandsuboptimalcomplianceto vaccina-tionsarefullyassociatedwithpovertyanddifficultofaccessto healthservicesingeneral[13].Thus,itislikelythatthesefour fac-torsarenotbiologicalcausesofincompletevaccination,butare associatedwithparental–childhoodcharacteristicsandhealthcare structure–professional determinants ofthe incomplete vaccina-tion.

Thesefindingsreinforcetheimportanceofhealth promotion strategiesoverallsuchasvisitstovulnerablehouseholdsand inte-grated care across health and education services as means to increaseimmunizationcoverage[2,17].Surely,DCCsare consid-eredprivilegedspacesfortheexecutionofprogrammestocontrol andpreventtheinfantsocio-biologicalvulnerability byparents, managersandhealthprofessionals[18].

We conclude that opportunities are being missed to iden-tifychildrenwithincompletevaccination;andthatstrategiesto enhancevaccinationcoverageshouldpayspecialattentiontothe needsoffamilieslivingininadequatehousing;andthat surveil-lanceandhealthpromotionactionsinprimaryhealthfacilitiesand DCCsshouldbeimprovedperformedasconcomitantactivities[19].

Finally,given therelevance ofparental–childhood character-istics, we recommend that qualitative studies approaching the parentalperceptionoftheneedandsecuritytohavetheirchildren inoculated withvaccine and culturaldimension aspectsshould beperformedtoevidencebehavioralcharacteristicssusceptibleto healthinterventions[20].

Acknowledgements

The present study is integral part of Projeto CrechEficiente, financedbytheFundacãodeAmparoàPesquisadoEstadodeSão Paulo(FAPESP),processno.2006/02597-0.Theauthorsthankthe principalsoftheday-carecentresfortheirassistanceinthe pro-cessofobtainingtheinformedconsentandindatacollection.The authorsalsoexpresstheirappreciationtoFundac¸ãodeAmparoà PesquisadoEstadodeSãoPaulo(FAPESP)forfundingtheresearch project.

Contributors:T.K.wrotethearticle,selectedthestudydesign, and performedthe dataanalysis and interpretation.L.C.R. con-tributedtothedataanalysisandinterpretation,andcollaborated writing thearticle. T.K. and J.A.A.C.T. collaborated in thestudy conception, participated in the process of selecting the survey instrumentand samplingstrategy, andcollaborated inthedata collection.Allauthorsapprovedthecontentsofthemanuscript. Conflictofintereststatement:Theauthorshavenoconflictof inter-est.

References

[1]World Health Organization. Expanded Programme on Immunization (EPI). Immunization service delivery and accelerated disease con-trol. http://www.who.int/immunizationdelivery/en/ [accessed February 2011].

[2]Bondy JN, Thind A, Koval JJ, Speechley KN. Identifying the determi-nants ofchildhoodimmunization inthePhilippines. Vaccine2009;27(1): 169–75.

[3]WorldHealthOrganization,UNICEF,WorldBank.Stateoftheworld’svaccines andimmunization.3rded.Geneva:WorldHealthOrganization;2009. [4]Akmatov MK, Kretzschmar M, Krämer A, Mikolajczyk RT. Timeliness of

vaccination andits effects onfractionof vaccinated population. Vaccine 2008;26(31):3805–11.

[5]JaniJV,DeSchachtC,JaniIV,BjuneG.Riskfactorsforincompletevaccination andmissedopportunityforimmunizationinruralMozambique.BMCPublic Health2008;8:161.

[6]Ministério daSaúde(Brasil).SecretariadeVigilânciaemSaúde.Programa NacionaldeImunizac¸ões30anosSérieC.ProjetoseProgramaseRelatórios. Brasília(DF):MinistériodaSaúde;2003.

[7]FeijóRB,SáfadiMAP.Immunizations:threecenturiesofsuccessandongoing challenges.JPediatr2006;82(Suppl.3):1–3.

[8]BeghinI,CapM,DujardinB.Aguidetonutritionalassessment.Geneva:WHO; 1988.

[9]RosenblitJ,AbreuCR,SzterlingLN,KutnerJM,HamerschlakN,FrutuosoP,etal. Evaluationofthreemethodsforhemoglobinmeasurementinablooddonor setting.SaoPauloMedJ1999;117:108–12.

[10]World Health Organization, Multicentre Growth Reference Study Group. WHOchildgrowthstandards:length/height-for-age,weight-for-age, weight-for-length, weight-for-heightand bodymassindex-for-age: methodsand development.Geneva:WHO;2006.

[11]TopuzogluA,OzaydınGAN,CaliS,CebeciD,KalacaS,HarmanciH.Assessment ofsociodemographicfactorsandsocio-economicstatusaffectingthecoverage ofcompulsoryandprivateimmunizationservicesinIstanbul,Turkey.Public Health2005;119:862–9.

[12]SunM,MaR,ZengY,LuoF,ZhangJ,HouW.Immunizationstatusandrisk factorsofmigrantchildrenindenselypopulatedareasofBeijing,China.Vaccine 2010;28(5):1264–74.

[13] FalagasME,ZarkadouliaE.Factorsassociatedwithsuboptimalcomplianceto vaccinationsinchildrenindevelopedcountries:asystematicreview.CurrMed ResOpin2008;24(6):1719–41.

[14]MonteiroCA,BenicioMH,KonnoSC,SilvaAC,LimaAL,CondeWL.Causesfor thedeclineinchildunder-nutritioninBrazil,1996–2007.RevSaudePublica 2009;43(1):35–43.

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