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TheHigherTemperatureintheAreolaSupportstheNaturalProgressionoftheBirthtoBreastfeedingContinuumVincenzoZanardo*andGianlucaStraface2015年4月讀書報(bào)告會(huì)PUBMEDAbstract
Numerousfunctionalfeaturesthatpromotethenaturalprogressionofthebirthtobreastfeedingcontinuumareconcentratedinthehumanfemale'sareolarregion.Theaimofthisstudywastolookmorecloselyintothethermalcharacteristicsofareola,whicharesaidtoregulatethelocalevaporationrateofodorsandchemicalsignalsthatareuniquelyimportantfortheneonate's'breastcrawl'.Adermatologicalstudyoftheareolaeandcorrespondinginternbreastquadrantswasundertakenonthemothersof70consecutive,healthy,full-termbreastfedinfants.ThestudytookplacejustafterthebirthsatthePoliclinicoAbanoTerme,inItalyfromJanuarytoFebruary2014.Temperature,pHandelasticitywereassessedonedaypostpartumusingtheSoftPlus5.5(CallegariS.P.A.,Parma,Italy).Themeanareolartemperaturewasfoundtobesignificantlyhigherthanthecorrespondingbreastquadrant(34.60±1.40°Cvs.34.04±2.00°C,p<0.001)andthepHwasalsosignificantlyhigher(4.60±0.59vs.4.17±0.59,p<0.001).Incontrast,theelasticityoftheareolarwassignificantlylower(23.52±7.83vs.29.02±8.44%,p<0.003).Ourfindingsshow,forthefirsttime,thattheareolarregionhasahighertemperaturethanthesurroundingbreastskin,togetherwithhigherpHvaluesandlowerelasticity.Webelievethatthehighertemperatureoftheareolarregionmayactasathermalsignaltoguidetheinfantdirectlytothenippleandtothenaturalprogressionofthebirthtobreastfeedingcontinuum.IntroductionWithinmomentsofanaturalvaginalbirth,withoutinvasivebirthingpractices,newbornsdemonstrateinnatefeedingbehaviorsandinstinctivelyseekoutand‘crawl’towardthemother’sbreasttoattachthemselves[1,2]theirhandsexploringandmassagingthebreast[3].Thefunctionalstepsthatleadmammalianinfantstoseekoutthenippleandattachthemselvestoitbeforepropersuckingsetsinarenotfullyunderstood[2],butitisknownthatearlysuckingbehavioriseasilyupsetbyunfavorableconditions[4].Thehumanfemale’sareolarregionisofspecialinterestinthisjourney,becausenumerousfeatureslinkedtothenaturalprogressionofthebirthtobreastfeedingcontinuumareconcentratedinit[5]Apartfromprovidingtheinfantwithaccesstocolostrumandmilk,thenippleregionprovideschemicalsignalsthatappeartobeparticularlyimportanttotheneonate[6].Theattractivenessofmaternalbreastodorsinthebiologicalcontextofbreastfeedinghasasimilarfunctiontotheroleof‘nipplesearchpheromone’inguidingnewbornmammalianstothenipple.Althoughmaternalodorsmaynotbeascriticalfornipplelocalizationinthehumanspecies,theymayneverthelessfacilitateearlybreastfeedingattempts[7].Inadditiontohelpingtoguidetheinfantdirectlytothenipple,maternalbreastodorsaffectotheraspectsofneonatalbehaviorthatincreasetheprobabilityofsuccessfulnipplegraspingandfeeding[8].Atthesametime,theymayhelptheinfanttorecognizeitsmotherand,therefore,playaroleininfant-motherbonding[9,10].Theareolaregioncontainsadenseaccumulationofapocrineandsebaceousskinglands,whichcouldcontributetoproducingattractivechemicalsignalsorserveasodorfixativesthatprolongtheeffectivenessoftheodor[5].Inaddition,thediffusionofodorousmoleculesmaybeenhancedbytherelativelyhighsurfacetemperatureoftheareola,duetotherichsupplyofbloodvesselsinthisregion[11,12].Thereissomescientificevidencethatdescribeshowtheinfantbehavesandrespondstotheodorsthatarenaturallyreleasedbybreastsoflactatingwomen[13].Thisstudyaimedtoexamineingreaterdetailhowtheinfantlocatesthemother’sbreastandtoassessanumberofpreviouslyoverlookeddermatologicfeatures.Theprimaryobjectiveofthisstudywastomeasurethetemperatureoftheareolaandthecorrespondinginsidesuperiorquadrantearlyafterbirth.BreastpHandelasticitywerealsoassessed.ParticipantsandSettingEverywomanwhogavebirthtoahealthyfull-terminfantintheDepartmentofObstetricsandGynaecologyofthePoliclinicoAbanoTerme,AbanoTerme,Italy,betweenJanuaryandFebruary2014waseligibletotakepartinthedermatologicalstudyoftheareolaeandcorrespondinginternbreastquadrants.Thestudysampleof70mother-infantdyadsconsistedofhealthybreastfeedingwomen,withoutanomaliesinthebreastand,or,nippleanatomyornippledermatitis,whowereatleast18-years-of-age,spokeItalian,hadalow-riskpregnancy,anddeliveredasinglehealthychildofmorethan37weeksofgestation.Thestudywasperformedinaccordancewiththe1997DeclarationofHelsinkiandthelocalinstitutionalreviewboard,theEthicsCommissionofPoliclinicoAbanoTerme,approvedthestudy(ProtocolN.274/2013).Iftheinclusioncriteriawerefulfilled—thepregnancyanddeliverywerenormal,theneonatewashealthyandthemotherintendedtobreastfeed—themotherswereaskedtosignaninformedconsentformsayingthattheyagreedtoparticipateinthestudy.ThestandardpracticeinourDepartmentafteranuneventfuldeliveryistoplacetheinfantonthemother’schestimmediatelyafterbirthandleavethemtherefor15minuteswhilethemidwifehelpsthemothertoachievethefirstsucklingepisode.Theinfantsarethendried,receiveumbilicalcare,andareweighedbeforetheirfirstbath.Duringthenexttwodays,thenewbornsstayonthewardinthesameroomastheirmothers,whoareencouragedtofeedthemondemandwithnomorethanafour-hourintervalbetweenfeeds.Theinfantsreceivecomplementaryformulaifthemidwifedoesnotthinktheyarereceivingsufficientbreastmilk.Aftereachfeed,themothersaresimplyadvisedtowipetheirareolasandnippleswithascentless,humidgauzepad.Theparticipatingmother-infantdyadswerestudiedduringthefirst24hoursafterdelivery.Themotherswereinformedaboutourstudymethods,butwereblindtothespecifichypothesesbeingtested.BreastfeedingpatternsweredefinedaccordingtotheWorldHealthOrganization’sclassifications:exclusivebreastfeedingwasdefinedastheinfantonlyreceivingmaternalmilk,complementarybreastfeedingwasdefinedasofferingbreastmilkandinfantformulasandexclusiveformulafeedingwasdefinedasonlyofferingbottle-fedformula[14].DatacollectionInformationaboutthepregnancy,labor,delivery,Apgarscore,neonatalbirthweightandfirstbreastfeedingattemptswerecollectedfromthemotherandfromhermedicalrecords.AreolardermatologicalfeaturesThemothers’breastswereinspectedbyamidwifeandamemberofthestudygrouponthefirstdaypostpartumbetweenfeedings,beforeassessingtheareolaeandinsidesuperiorquadrantsusingtheSoftPlus5.5device(CallegariS.P.A.,Parma,Italy)[15].Thefollowingareolaandquadrantsurfacevariableswerecollected:Temperature.Measurementprinciple:infraredmeasurementofexternaltemperature.Field:20°-40°C.Resolution:0.1cu(conventionalunits).Precision:±3%.Description:ABSplasticpen-typeprobewithasensoronthetip.Operatingconditions:temperature15÷35°Candmaximumrelativeuncondensedhumidity80%.Measurementmethod:thetworedlightsofthepenprobewerefocuseduntilonlyonewasclearlyvisibleontheareaofskintobemeasured.pH.Measurementprinciple:doublecelledelectrode.Field:2–12.Resolution:0.1.Precision:±1%.Description:rechargeableelectrode.Operatingconditions:temperature15÷35°Candmaximumrelativeuncondensedhumidity80%.Measurementmethod:theelectrodewasplaceddelicatelyontheskinwithoutpressing.Elasticity.Measurementprinciple:stress/deformation.Field:0–50cu.Resolution:1cu.Precision:±10%.Description:ABSplasticpen-typeprobewithasensoronthetip.Operatingconditions:temperature15÷35°C.Measurementmethod:theprobewasplacedatrightanglestotheskin.StatisticalanalysisAdescriptiveanalysiswasusedtoconstructaqualitativeevaluationoftheclinicaldata.Continuousdatawereexpressedasmeansandstandarddeviations(SD).CategoricaldatawerecomparedusingFisher'sexacttest,whilecontinuousdatawerecomparedusingtheStudent’st-test.Ap-valuelessthan0.05wasconsideredsignificant.StatisticalanalysiswasperformedusingR2.12software.ResultsThematernalandneonatalanthropometricalandclinicalcharacteristicsareoutlinedinTable1.ResultsTable2showsthedermatologicfeaturesoftheareolaandcorrespondinginsidebreastquadrantDisscussionThisstudyprovidesnewinformationaboutsomeofthedermatologicpropertiesoftheareolarregioninlactatingmothersandsomeaspectsofthe‘breastcrawl’phenomenon.Ourfindingsshow,forthefirsttime,thattheareolarregionhasahighertemperaturethanthesurroundingbreastskin,togetherwithhigherpHvaluesandlowerelasticity.Tothebestofourknowledge,thesedermatologicalfeatureshaveneverbeenexaminedusingascientificmethodduringtheperiodthatbreastfeedingisbeingestablished,norhavetheybeencomparedquantitativelywiththesurroundingquadrantskin.Higherareolartemperature,aloneorcombinedwithmultiplesourcesofodorantsandlipidfixatives,mayserveasaheat-basedcommunicativefunctionandactasathermalsignaltoguidetheinfantdirectlytothenipple.Newbornscanperceivethedifferenceintemperaturebetweentheareolaandtherestofthebreastskin[16–18],justastheyseemtobesensitiveto,andexhibitapreferencefor,theirmother’sscent[19].Inaseriesofstudies,neonateswerefoundtoconsistentlyprefer,andtomovetowards,thesmelloftheirmothers’breasts[20].Thiscouldbeduetoadoubleaction,bothonthemouthsensitivityreceptorsandontheolfactoryreceptorneurons.Infact,lipsandfingertipsareoftenconsideredtobetheareaswiththehighestconcentrationsofreceptorcells[18].Moreover,theareasofthebrainthatreceivemessagesfromtouchreceptorsinthelipsandhandsaremuchlargerthanthosereceivingmessagesfromlesssensitiveplacesandmorebrainpowerisspentinterpretingtouchsensationsfromthelipsandfingersthanfromotherareas[18].Thisthermalcharacteristicmayalsoplayaroleinregulatingthelocalevaporationrateofodorants,therebyenhancingtheireffectiveroleinstimulation.Thisislinkedtoolfactorylearning,whichisessentialforneonatalbehavioraladaptationinmanymammals,includinghumans[19–21].Birthandthefirsthoursoflifearecrucialforolfactorylearning.Duringthisperiodthesmellsemanatingfromthemotherandnewborninteractwithoneotherandanimalstudieshaveshownthatthereisaninteractioninprocessingolfactorysignalsonbothsides[21,22].Thermalandolfactorysignalsmayhelpthenewborntolocatethenippleandattachtoit,leadingtothefirstsuckingexperience.Althoughitisonlysmall,thenipple-areolarregionisdenselysuppliedwithvariedexocrineandenlargedsebaceousskinglands,withsmallprominencesthatMorgagnicalled‘‘tubercles”[2],coalescingsebaceousglandsandminiaturemammaryacini[2,23].Colostrumandmilkarereleasedfromthenipplethroughthemainlactiferousductsandtheirintrinsicolfactoryqualitiesandodorantsreflectthemother’sdiet,metabolismandgeneticconstitution[24].Thesevariedsourcesofsubstratescombinetocreateacomposite,highlycomplexodorcocktail.ThehigherpHfoundintheareolarskinoriginatesfromthismixtureandmayindeedfavor,oractasanodorfixative,toimprovethestabilityoftheolfactorycomplexthatisformedonthesurfaceoftheareolar[25].Inaddition,Haller’ssubareolarvascularplexusprovidestheareolarwithahighersurfacetemperaturethanthenippleandtherestofthebreast[11].Aswehypothesizedearlierinthispaper,thisthermalcharacteristicmayregulatethelocalevaporationrateofodorants,therebyenhancingtheirstimulatingeffectiveness.Avaginaldeliverysetsoffasurgeofcatecholamine,whichfacilitatesthenewborn’sadaptationtoextrauterinelifeandextensivecrying[26].Itisinterestingtonotethattheareola’sthermalfeatureistriggeredbythecryinginfant[27],resultinginoptimalconditionsforodorreleaseinanticipationofwhentheinfantisofferedthemother’sbreast.Wepresumethatthecharacteristicsoftheareolarregionthatwereportherehaveabiologicalsignificance.Firstly,thehigherpHduringearlylactationmaybelinkedtolocalepidermalandductalprotectionfrompathogens[28].Secondly,lowerareolarelasticityandgreasysecretionsmayhelptopreservetheskinfromthecorrosiveactionoftheinfant’ssalivaandfromsucking-relatedstress[29].Thirdly,skinglandsecretions,infantsalivaandlowerelasticitymayallbeneededtocreatethehermeticsealthatmakessuckingeffective[30].ConclusionsUsingbioengineeringmethodstoassessnippleandbreastskinfeaturesduringthenaturalprogressionfrombirthtobreastfeedinghasnoteliminatedseveralstudylimitations.Inparticular,itwasimpossibletocalculatethestatisticalpowerasthereisnodataintheliteratureregardingareolarpH,temperatureorelasticity.Moreinformationaboutthe‘breastcrawl’phenomenonwouldbenecessarytoclarifyothervariables(i.e.maternalage,parity,iflaborwasinduced,ifandwhattypeofanalgesicswereused,andthedeliveryroute)thatcouldinfluencemothers’hormonalandneuroendocrinalresponse[31]andconfoundthefinaloutcome.Wedidnotobservethemothers’attitudenordidwemonitortheirpsycho-emotionalandhormonalchangesduringthe‘breastcrawl’andearlybreastfeedingwhichcouldinfluencebreastskinpH,temperature,andelasticity.Theseandthefactthattherewasnocontrolgroup,canbeconsideredotherstudylimits.FundingstatementTheauthorshavenosupportorfundingtoreport.ReferenceKlausMMotherandinfant:earlyemotionalties.Pediatrics.1998;102:1244–12469794962[PubMed]2.SchaalB,DoucetS,SagotP,HertlingE,SoussignanRHumanbreastareolaeasscentorgans:morphologicaldataandpossibleinvolvementinmaternal-neonatalcoadaptation.DevPsychobiol.2006;248:100–110.[PubMed]3.MatthiesenAS,Ransjo-ArvidsonAB,NissenE,Uvnas-MobergKPostpartummaternaloxytocinreleasebynewborns:effectsofinfanthandmassageandsucking.Birth.2001;28:13–1911264623[PubMed]4.RighardL,AladeMOEffectofdeliveryroomroutinesonsuccessoffirstbreast-feed.Lancet.1990;336:1105–11071977988[PubMed]5.PorterRH,WinbergJUniquesalienceofmaternalbreastodorsfornewborninfants.NeurosciBiobehavRev.1999;23:439–4499989430[PubMed]6.VarendiH,PorterRHBreastodourastheonlymaternalstimuluselicitscrawlingtowardstheodoursource.ActaPaediatrica.2001;90:372–37511332925[PubMed]7.Widstr?mAM,Ransjo-ArvidsonAB,ChristenssonK,MatthiesenAS,WinbergJ,Uvnas-MobergKGastricsuctioninhealthynewborninfants.ActaPaediatrScand.1987;76:566–5723630673[PubMed]8.RussellMJHumanolfactorycommunication.Nature.1976;260:520–5221264204[PubMed]9.VarendiH,PorterRH,WinbergJDoesthenewbornbabyfindthenipplebysmell?Lancet.1994;344:989–9907934434[PubMed]10.Delaunay-ElAllamM,MarlierL,SchaalBLearningatthebreast:preferenceformationforanartificialscentanditsattractionagainsttheodorofmaternalmilk.InfantBehavDev.2006;29:308–32117138287[PubMed]11.MitzV,LalardrieJPAproposdelavascularisationetdel'innervationsensitivedusein.Senologia.1997;2:33–39.12.BartocciM,WinbergJ,RuggieroC,LBbergqvistLL,SerraG,LagercrantzHInfantsafterodorstimulation:afunctionalNear-InfraredSpectroscopystudy.PediatrRes.2000;48:18–2310879795[PubMed]13.Widstr?mAM,WahlburgW,MatthiesenASShort-termeffectsofearlysucklingandtouchofthenippleonmaternalbehavior.EarlyHumanDev.1990;21:153–1632311552[PubMed]14.WHO/UNICEF.Protecting,PromotingandSupportingBreastfeeding:TheSpecialRoleofMaternityServices.Geneva,Switzerland:WorldHealthOrganization;1989.Available:/programme/nutrition/infantfe/tensteps.htm197208015.SoftPlus5.5Callegari,S.P.A.,Parma,Italy.Available:.16.JacobsR,WuCH,GoossensK,VanLovenK,VanHeesJ,VanSteenbergheDOralmucosalversuscutaneoussensorytesting:areviewoftheliterature.JOralRehabil.2002;29:923–95012421324[PubMed]17.CruzA,GreenBGThermalstimulationoftaste.Nature.2000;403:889–89210706285[PubMed]18.IggoACutaneousthermoreceptorsinprimatesandsub-primates.JPhysiol.1969;200:403–4304974402[PMCfreearticle][PubMed]19.MacfarlaneAOlfactioninthedevelopmentofsocialpreferencesinthehumanneonateIn:PorterR,O'ConnorM,editors.Parent-infantinteractions.NewYork:CibaFound.Symp.33;1975.pp.103–113.20.AlexanderG,StevensDOdorcuestomaternalre
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