REVISTA
PAULISTA
DE
PEDIATRIA
www.rpped.com.br
ORIGINAL
ARTICLE
Maternal
breastfeeding,
early
introduction
of
non-breast
milk,
and
excess
weight
in
preschoolers
Viviane
Gabriela
Nascimento
a,∗,
Janaína
Paula
Costa
da
Silva
b,
Patrícia
Calesco
Ferreira
c,
Ciro
João
Bertoli
d,
Claudio
Leone
aaFaculdadedeSaúdePública,UniversidadedeSãoPaulo(USP),SãoPaulo,SP,Brazil
bFaculdadedeCiênciasdaSaúdedoTrairi,UniversidadeFederaldoRioGrandedoNorte(UFRN),Trairi,RN,Brazil cFaculdadedeMedicinadoABC,SantoAndré,SP,Brazil
dUniversidadedeTaubaté,Taubaté,SP,Brazil
Received7December2015;accepted29May2016 Availableonline7September2016
KEYWORDS
Breastfeeding; Complementary feeding; Excessweight; Preschooler; Obesity
Abstract
Objective: Investigateassociationsbetweenexcessweightinpreschoolchildren,breastfeeding durationandageofnon-breastmilkintroduction.
Methods: Cross-sectionalstudyofarepresentativesampleof817preschoolchildren,aged2---4 years,attendingmunicipaldaycarecentersinthecityofTaubaté.Theweightandheightof childrenweremeasuredinthedaycarecentersin2009,2010and2011.Thebodymassindex
z-score(BMIz)wascalculatedandchildrenwereclassifiedasriskofoverweight(BMIz≥1to<2)or excessweight(BMIz≥2).Dataanalysiswascarriedoutbycomparisonofproportions,coefficient ofcorrelationandmultivariatelinearregression.
Results: Theprevalenceofriskofoverweightwas18.9%andofexcessweight(overweightor obesity)was9.3%.Themediandurationofbreastfeedingandageofintroductionofnon-breast milk was 6months. The child’sBMIz showed directcorrelationwith birthweight (r=0.154;
p<0.001)andmaternalbodymassindex(BMI)(r=0.113;p=0.002).Thecorrelationwasinverse withthetotaldurationofbreastfeeding(r=−0.099;p=0.006)andageatnon-breastmilk intro-duction(r=−0.112;p=0.002). Therewas nocorrelationbetween thechild’sBMIzwithbirth length,durationofexclusivebreastfeedingandmother’sage.
Conclusions: Theearliertheintroductionofnon-breastmilk,thehigherthecorrelationwith excessweightatpreschoolage.
©2016PublishedbyElsevierEditoraLtda.onbehalfofSociedadedePediatriadeS˜aoPaulo. ThisisanopenaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/ by/4.0/).
∗Correspondingauthor.
E-mail:[email protected](V.G.Nascimento).
http://dx.doi.org/10.1016/j.rppede.2016.05.002
PALAVRAS-CHAVE
Aleitamentomaterno; Alimentac¸ão
complementar; Sobrepeso; Pré-escolar; Obesidade
Aleitamentomaterno,introduc¸ãoprecocedeleitenãomaternoeexcessodepeso
naidadepré-escolar
Resumo
Objetivo: Investigarrelac¸õesexistentesentreexcessodepesoempré-escolares,durac¸ãodo aleitamentomaternoeaidadedeintroduc¸ãodeleitenãomaterno.
Métodos: Estudotransversaldeamostrarepresentativade817pré-escolares,2-4anosdeidade, decrechesmunicipaisdeTaubaté.Opesoeaalturadascrianc¸asforammensuradosnascreches em 2009,2010e2011.CalculadooescorezdeÍndice deMassaCorporal(zIMC),ascrianc¸as foramclassificadascomoriscodesobrepeso(zIMC≥1a<2)oucomoexcessodepeso(zIMC≥2).A análisedosdadosfoifeitaporcomparac¸ãodeproporc¸ões,coeficientedecorrelac¸ãoeregressão linearmultivariada.
Resultados: Aprevalênciaderiscodesobrepesofoi18,9%edeexcessodepeso(sobrepesoou obesidade)de9,3%.Amedianadedurac¸ãodoaleitamentomaternoeaidadedeintroduc¸ãodo leitenãomaternofoide6meses.OzIMCdacrianc¸aevidencioucorrelac¸ãodiretacomopesoao nascer(r=0,154;p<0,001)ecomoÍndicedeMassaCorporal(IMC)materno(r=0,113;p=0,002). Acorrelac¸ãofoiinversacomadurac¸ãototaldoaleitamentomaterno(r=−0,099;p=0,006)ea idadedeintroduc¸ãodeleitenãomaterno(r=−0,112;p=0,002).Nãohouvecorrelac¸ãoentreo zIMCdacrianc¸acomocomprimentoaonascer,durac¸ãodoaleitamentoexclusivoeidadeda mãe.
Conclusões: Quantomaisprecoceaintroduc¸ãodeleitenãomaterno,maioracorrelac¸ãocom excessodepesonaidadepré-escolar.
©2016PublicadoporElsevierEditoraLtda.emnomedeSociedadedePediatriadeS˜aoPaulo. Este ´eumartigoOpenAccesssobumalicenc¸aCCBY(http://creativecommons.org/licenses/ by/4.0/).
Introduction
Maternalbreastfeedingisanaturalandappropriatewayto feedachildinthefirstmonthsoflife,promotingadequate growthanddevelopment.1 Inthissense,theWorldHealth
Organization recommends that exclusive breastfeeding is maintaineduptosixmonthsandthatitscomplementation withotherfoodsisrequiredonlyafterthatage.2
Severalstudieshave shownthatbreastfeedingisa pro-tective factor for both malnutrition and obesity.3---5 The
momentwhen other foods areintroduced, including solid foods,duringchildhoodhasalsobeenconsideredan impor-tantaspect of childcare, evenduetoitspossible effects onhealththroughoutlife.6Themomentofintroductionand
theamountofsolidfoods7,8introducedintochildren’sdiet
in early life can lead to an increased risk of developing obesityearly inlifeandthecomorbiditiesassociatedwith it.9,10
Obesityiscurrentlyoneofthemajorpublichealth prob-lems, including in the Pediatric population, from infancy toadolescence. In thiscontext, it is knownthat the first monthsoflifeareidentifiedascrucialforthedevelopment ofobesity.11,12Earlyintroductionofsolidfoods,particularly
before4monthsoflife,isassociatedwithincreasedweight gainandevenofbodyfatduringchildhood,13,14 withthese
factorsbeing considered aspredisposingtoobesity in the future.15
There is also a controversy regarding the protective effectofbreastmilkinthedevelopmentofobesity.While some studies suggest that breastfeeding can protect chil-dren against the development of overweight or obesity, otherssuggestthatthefactofstartingtheintroductionof
complementary foods as close as possible to the rec-ommended age is the protective factor against excess weight.3,5
In this context, the aim of this study is to investigate thepossibleassociationbetweenexcessweightatpreschool age and duration of breastfeeding and age of non-breast milk introduction, with birth weight and length control, inadditiontosomematernal riskcharacteristics for early developmentofexcessweight.
Method
This was a cross-sectional study carried out in municipal day care centersin themunicipality of Taubaté, state of SãoPaulo,Brazil,withchildrenofpreschoolage,originally plannedtoevaluatethegrowthandnutritionalstatusof chil-drenstartingdaycareduringtheschoolyearsof2009,2010 and2011.
To calculate the sample, a difference of 1/3 of the standarddeviationinthez-scoreforbodymassindex(BMIz) wasconsidered, withanassumptionofstandard deviation of1.2BMIz, fora 90%test power andan alphaof5%. The minimumnumberestimatedasnecessarywas248children, plus10%toreplacepossiblelossesorrefusals,resultinginan initialsampleof273preschoolersrequiredforeachschool yearevaluation.
Table1 Characteristicsofpreschoolersperyearofdaycarecenterenrollment,2009,2010and2011.
Variables 2009 2010 2011
Mean SD Mean SD Mean SD
Age(months) 38.8 3.7 38.9 3.7 38.8 3.7
Weight(kg) 15.3 2.6 15.4 2.3 15.4 2.4
Height(cm) 97.1 4.7 96.9 4.3 97.1 4.9
BMI 16.2 1.8 16.3 1.6 16.3 1.6
Weight/agez-score 0.269 1.223 0.305 1.038 0.320 1.012
Height/agez-score −0.077 1.088 −0.143 0.913 −0.071 1.140
BMIz 0.460 1.236 0.571 1.061 0.539 1.142
BMI,bodymassindex;BMIz,bodymassindexz-score.
preschoolchildrenaged2tounder4yearsoldwasobtained, whichwereevaluatedin2009,2010and2011,respectively. Aftercollecting thedatafromthe lastschoolyear, we comparedthethreeyearsaimingtoverifypossiblesample similarities.As thethreesampledschool yearsshowedno differencesregardingtheanthropometriccharacteristicsof thepreschoolchildren(Table1),itwasdecidedtocontinue theanalysisofthegroupasawhole,irrespectiveoftheyear whenthechildrenwereassessed.
Therefore, this study included all preschool children enrolled at and attending day care centers in the first semesterofthose3schoolyears,whichresultedinafinal sampleof817children.
Basedonthissample,informationregardingbirthweight andlength,durationofexclusivebreastfeeding,total dura-tionofbreastfeedingandageatintroductionofnon-breast milk was analyzed, as well as maternal age, weight and height.These data werereportedand recorded by moth-ersand/or guardiansofpreschoolchildreninstandardized formsthatweresentbythedaycarecenters.
Children’s anthropometric data regarding weight and heightwereobtainedatthedaycare,ondulyscheduleddays inApril 2009,2010 and 2011. The children wereweighed withoutshoesandwearingaslittleclothingaspossible,on aportable electronic scale (803,Seca®, Portugal),witha
capacityofupto150kgandscaleintervalof100g.
Heightwasmeasuredusingaportablestadiometer(E210, WISO®,SãoPaulo,Brazil)fixedtothewall,withsubdivisions
incentimeters and millimeters.The children touchedthe wallwithheels,calves,glutesandshoulders,withthehead positionedintheFrankfurthorizontalplane.All anthropo-metricmeasurementswere obtainedusingthe techniques describedbyLohmanetal.16 induplicate,recorded
imme-diatelyaftertheyweretaken,withthemeanbeingusedas thefinalvaluefortheanalysis.
Thez-scorevaluesofweight(Wz),height(Hz)andbody mass index (BMIz) of each child were calculated based on the World Health Organization (WHO) reference from 2006.17 The criteriaproposed bythe Ministryof Healthin
200918 wereusedtoclassify thechildren’snutritional
sta-tus.PreschoolchildrenwithBMIz≥1to<2wereconsideredat riskofexcessweight,andasexcessweight,i.e.,overweight orobese,thosewithBMIz≥2.
The data analysis of the three-sample group was con-sidered as a whole through calculations of frequencies, comparisonsandproportions,aswellasPearson’s correla-tioncoefficientcalculation.Furthermore,amultiplelinear
regressionanalysiswasalsoperformedintheend,whichhad thepreschoolchildren’sBMIzasthedependentvariable.For theseanalyses,informationonexclusivebreastfeedingand totalbreastfeedingduration,aswellasageatintroduction ofnon-breastmilk,wascomputedinfullmonths.Asforthe linearregressionanalysismodelofmultiplevariables,nine independent variables were included, namely, the child’s ageandgender, durationofexclusive breastfeeding,total durationofbreastfeeding,ageatnon-breastmilk introduc-tion,birthweightandlength,in additiontomaternal age andBMI.
The project was approved by the Institutional Review Board of Faculdade de Saúde Pública daUniversidade de SãoPaulo(Protocoln.1877,April2009).TheInformed Con-sentformwassenttothechildren’smothersorguardiansby thedaycareandwerereturnedappropriatelyfilledoutand signedbeforethestartofdatacollection,accordingtothe NationalHealthCouncilResolutionn.196/1996,effectiveat thetimeofthestudy.
Results
Table1shows themeanageof thechildrenin2009, 2010 and2011,of38.8,38.9and38.8months,respectively,witha standarddeviation(SD)of3.7monthsatthethreemoments (p=0.465). In relation to the body mass index and their
z-scores, no statistically significant difference was found (p=0.689 and p=0.515, respectively). Regarding the other anthropometric parameters, no statistical difference was observed,either.
Inthetotalsample,51.3%ofchildrenweremales,withno differenceinthisproportionbetween2009,2010and2011, ofwhichvalueswere51.7%,50.4%and52.3%,respectively (chi-square;p=0.907).
Regardingtherisk ofexcessweight(BMIz≥1to<2),the totalsample showedaprevalenceof18.9% andasfor the presenceofexcessweight(BMIz≥2),itwas9.3%.The com-parisonofexcessweightprevalencefor2009,2010and2011 showednodifference, being9.4%,8.5%and9.9%, respec-tively(chi-square;p=0.864).
0 5 10 15 20 25 –4
–2 0 2 4 6
Total breastfeeding duration (months) 1000 2000 3000 4000 5000
–4 –2 0 2 4 6
Birth weight (g) Z-score of body mass index
Z-score of body mass index
Z-score of body mass index
Z-score of body mass index
0 6 12 18 24 –4
–2 0 2 4 6
Age (months) at the introduction of non-breast milk
15 20 25 30 35 40 45 –4
–2 0 2 4 6
Maternal body mass index
Figure1 Correlation/regressiontrendsbetween thez-scoreofbodymassindexofpreschoolchildren andbirthweight,total breastfeedingduration,ageatnon-breastmilkintroductionandmaternalbodymassindex.Taubaté,SãoPaulo,2009---2011.
Table2 Linearregressionofmultiplevariablesassociatedwiththebodymassindexz-scoreofpreschoolchildren.
Variables Coeff. Standarderror SC t p-value
EBFduration(months) 0.001 0.025 0.002 0.055 0.956
Maternalage(years) −0.002 0.006 −0.009 −0.255 0.799
Child’sage(months) 0.003 0.011 0.009 0.245 0.807
Birthlength(cm) −0.012 0.015 −0.031 −0.761 0.447
TotalBFduration(months) −0.007 0.006 −0.049 −1.083 0.279
Malegender −0.189 0.082 −0.082 −2.298 0.022
MaternalBMI(kg/m2) 0.025 0.009 0.099 2.805 0.005
AgeatintroductionofNBM(months) −0.025 0.007 −0.120 −3.397 0.001
Birthweight(r) 0.000 0.000 0.162 4.533 <0.001
Constant −0.942 0.315 --- −2.996 0.003
Coeff.,coefficient;SC,standardizedcoefficient;BMI,bodymassindex;EBF,exclusivebreastfeeding;BF,breastfeeding;NBM,non-breast milk.
Ofthetotalsample,10%ofchildrenreceivedbreastmilkfor 24months.
Asforthematernalcharacteristics,itwasobservedthat 43.7%ofthemotherswereoverweight(BMI≥25)and11.7% wereobese(BMI≥30).
Thebivariateanalysisshowedacorrelationbetweenthe child’s BMIz and birth weight (r=0.154; p<0.001), mater-nal BMI (r=0.113; p=0.002), total breastfeeding duration (r=−0.099;p=0.006)andageatintroductionofnon-breast milk(r=−0.112;p=0.002).Theselasttwovariablesshowed aninversecorrelation(Fig.1).
Themultivariateanalysis(Table2)showedthatonlyfour of the nine variables in the initial model remained sig-nificantlyassociated withthe preschoolers’BMIz, namely, inascendingorderofstatistical significance:malegender, maternalBMI,ageatnon-breastmilkintroductionandbirth
weight.Ofthese,onlythecoefficientsofbirthweightand maternalBMIwerepositive,whiletheywerenegativeforthe othertwovariables,indicatingan inversecorrelation. The child’sage,birthlength,exclusivebreastfeedingduration, totalbreastfeedingdurationandthemother’sagewerenot significantinthemodel.
Discussion
Inthepresentstudytheprevalenceofexcessweightamong preschoolchildrenwas9.3%,whichcanbeconsideredhigh inourcountry.5,19Thehighermaternalbodymassindex,
As for gender, although themalegender showedtobe aprotectivefactorforexcessweight,theimpactwasvery small(standardizedcoefficient=−0.082).Thatexplainsthe absenceofsignificantdifferencesinprevalenceinrelation togender (p=0.907) in thesample, which,incidentally, is in line with other studies that also found no differences in the prevalence of excess weight related tothe child’s gender.20,21
AsforthematernalBMI,itwasfoundthat43.7%ofthe mothershadexcessweight(overweightorobese)andthat therewasa directcorrelation between maternal BMIand thechild’s,afact thathasbeen documentedinthe liter-aturefor sometime,eveninBrazil.22,23 Thisevidenceofa
directassociationbetweenthenutritionalstatusofmothers and children in Brazil and excess weight have been pub-lishedsincethe1980s,whentheNationalSurveyonNutrition and Health (PNSN), while studying children younger than 10 years, found that the risk for a child to have excess weightwas3.2-foldhigherwhenthemotheralsohadexcess weight.24 Moreiraetal.25 alsoshowedahighprevalenceof
excessweightinchildrenassociatedwithmaternalcentral obesityandnon-exclusivebreastfeedingforaperiodshorter than6months.
Whilesomeresearchersconsiderasinconclusivethe evi-dence that breastfeeding is a protective factor against childhood obesity,26 in the last decade others have
con-cludedthatexclusivebreastfeedingprotectsagainstexcess weight in preschool and school-age children.5,21 Hediger
etal.,27intheUnitedStates,concludedthatthe
preschool-ersthathadbeenbreastfedhadalowerriskofbeingobese, butnot of beingoverweight. A longitudinal study of Ger-manchildrendemonstratedtheprotectiveroleofprolonged breastfeedingalsoforoverweight.22 InBrazil,astudy
car-riedoutinPelotaswithchildrenunder4yearsofageshowed thattheprevalenceofoverweightinchildrenbreastfedfor morethan11monthswaslowerthanthatobservedinthose breastfedforlessthan3months.28
In spite of the protective effect of breastfeeding described by several authors, the age of non-breast milk introductionseemstobeamoreimportant riskfactor for thedevelopmentofexcessweightinpreschoolchildren.In ourstudy,totalbreastfeedingdurationshowedacorrelation withBMIz of preschool children in the bivariate analysis, butthissignificancewasnotmaintainedinthemultivariate regression, possiblyindicating that the early introduction of non-breastmilk, evenduring mixedfeeding, with pro-longedmaintenanceofmaternalbreastfeeding,mayresult intheattenuationof theprotectiveeffectof breastmilk. The early introduction of non-breast milkand the conse-quentproteinoversupplymaybeinducingthedevelopment ofexcessweightinchildrenasearlyasatpreschoolage,29
evenwhenassociatedwithbreastmilk,thusreducingthis protectiverole againstthe riskof overweight andobesity development.
Promotingmaternalbreastfeedingasapossiblestrategy forthepreventionofchildhoodobesity makes breastfeed-ingencouragementanindispensabletoolinthefightagainst nutritionalalterations.Ontheotherhand,non-breastmilk shouldbeincludedafterthesixthmonthoflife,asbreast milkasthesoleandexclusivefoodsourcenolongermeets the child’s needs. The correct practice of complemen-tary feeding is considered essential against deviations in
nutritional status,asit occursbetween6 and24 months, aparticularlycriticalperiodforgrowth,caninterferewith thegrowthrate,which inthemediumandlong termmay haveconsequencesforchildren’sdevelopmentandhealth. Inthiscontext,alimitationofthestudywasnottoverify theintroductionofotherfoodsinthechild’sdiet.
Therefore,weconcludethatforchildrenwhosemothers areabletomaintainbreastfeedingforanextendedperiod oftime,evenifnotexclusively,delayingtheintroductionof non-breastmilkuntilabout6monthsofagecancontribute tomaintaintheprotectiveeffectofbreastmilkagainstthe risk ofearly developmentof excessweight,which canbe observedasearlyasinpreschool.
Funding
Thisstudydidnotreceivefunding.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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