www.jped.com.br
ORIGINAL
ARTICLE
Influence
of
the
informal
primary
caretaker
on
glycemic
control
among
prepubertal
pediatric
patients
with
type
1
diabetes
mellitus
夽
Jessie
Nallely
Zurita-Cruz
a,∗,
Elisa
Nishimura-Meguro
b,
Miguel
Angel
Villasís-Keever
a,
Maria
Elena
Hernández-Méndez
b,
Eulalia
Garrido-Maga˜
na
b,
Aleida
De
Jesús
Rivera-Hernández
baInstitutoMexicanodelSeguroSocial,CentroMédicoNacionalSigloXXI,UnidaddeInvestigaciónMédicaenEpidemiología
Clínica,MexicoCity,Mexico
bInstitutoMexicanodelSeguroSocial,CentroMédicoNacionalSigloXXI,UnidaddeEndocrinologíaPediátrica,MexicoCity,Mexico
Received14February2016;accepted15June2016 Availableonline4October2016
KEYWORDS
Type1diabetes; Caregiver; Pediatrics
Abstract
Objectives: Inprepubertaltype1diabeticpatients(DM1),theavailabilityofaninformal
pri-marycaregiver(ICP)iscriticaltomakingmanagementdecisions;inthisstudy,theICP-related riskfactorsassociatedwithglycemiccontrolwereidentified.
Patients,materials,andmethods: Acomparativecross-sectionalstudywasperformed.
Fifty-fivepatientswithDM1undertheageof11yearswereincluded.Thepatient-relatedfactors associatedwithglycemiccontrolevaluatedwerephysicalactivity,DM1timeofevolution,and adherencetomedicalindications.TheICP-relatedfactorsevaluatedwereeducation, employ-ment aspects, depressive traits (Beck questionnaire), family functionality (family APGAR), support ofanother personinpatient care, stress (Perceived Stress Scale), and socioecono-micstatus(Bronfmanquestionnaire).Multivariatelogisticandlinearregressionanalyseswere performed.
Results: Thepatients’medianagewas8years;29patientshadgoodglycemiccontrol,and26
wereuncontrolled.Themainriskfactorassociatedwithglycemicdyscontrolwasstressinthe ICP(OR24.8;95%CI4.06---151.9,p=0.001).While,accordingtothelinearregressionanalysis itwasfoundthatlowerlevelofeducation(ˇ0.991,95%CI0.238---1.743,p=0.011)andstress (ˇ1.918,95%CI1.10---2.736,p=0.001)intheICP,aswellasfamilydysfunction(ˇ1.256,95% CI0.336---2.177,p=0.008)wereassociatedwithhigherlevelsofglycatedhemoglobin.
夽
Pleasecitethisarticleas:Zurita-CruzJN,Nishimura-MeguroE,Villasís-KeeverMA,Hernández-MéndezME,Garrido-Maga˜naE, Rivera-HernándezAD.Influenceoftheinformalprimarycaretakeronglycemiccontrolamongprepubertalpediatricpatientswithtype1diabetes mellitus.JPediatr(RioJ).2017;93:136---41.
∗Correspondingauthor.
E-mail:[email protected](J.N.Zurita-Cruz).
http://dx.doi.org/10.1016/j.jped.2016.06.008
0021-7557/©2016SociedadeBrasileiradePediatria.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-ND
Conclusions: LevelofeducationandstressintheICP,aswellasfamilydysfunction,arefactors thatinfluencethelackofcontrolledbloodglucoselevelsamongprepubertalDM1patients. ©2016SociedadeBrasileiradePediatria.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/ 4.0/).
PALAVRAS-CHAVE
Diabetestipo1; Cuidador; Pediatria
Influênciadocuidadorfamiliarprincipalsobreocontroleglicêmicoentrepacientes pediátricospré-púberescomdiabetesmellitustipo1
Resumo
Objetivos: Em pacientes pré-púberes com diabetes tipo 1(DM1), a disponibilidade de um
cuidadorfamiliarprincipal(CFP)éfundamentalparatomardecisõesdeadministrac¸ão;neste estudo, foramidentificados os fatores de risco relacionadosa CFPs associados ao controle glicêmico.
Pacientes,materiaisemétodos: Foi realizado um estudo transversal comparativo. Foram
incluídos 55 pacientescomDM1 menores de 11anosde idade. Osfatores relacionadosaos pacientesassociadosaocontroleglicêmicoavaliadosforamatividadefísica,tempodeevoluc¸ão daDM1eadesãoàsindicac¸õesmédicas.OsfatoresrelacionadosaCFPsavaliadosforam esco-laridade, aspectos profissionais,trac¸os de depressão(questionáriode Beck),funcionalidade familiar(APGARfamiliar),ajudadeoutrapessoanocuidadodopaciente,estresse(Escalade EstressePercebido)esituac¸ãosocioeconômica(questionáriodeBronfman).Foramrealizadas análisesderegressãologísticamultivariadaederegressãolinear.
Resultados: Aidademédiadospacienteserade8anos;29pacientesapresentavambom
con-troleglicêmicoe26nãotinhamcontrole.Oprincipalfatorderiscoassociadoaodescontrole glicêmicofoioestressenoCFP(RC24,8;ICde95%4,06---151,9,p=0,001).Aopassoque,de acordocomaanálisederegressãolinear,constatamosque:omenorníveldeescolaridade( 0,991,ICde95%0,238---1,743,p=0,011)eestresse(1,918,ICde95%1,10---2,736,p=0,001)do CFP,bemcomoadisfunc¸ãofamiliar(1,256,ICde95%0,336-2,177,p=0,008),foramassociados aníveismaioresdehemoglobinaglicosilada.
Conclusões: OníveldeescolaridadeeoestressedoCFPeadisfunc¸ãofamiliarsãofatoresque
influenciamafaltadeníveisglicêmicoscontroladosentrepacientespré-púberescomDM1. ©2016SociedadeBrasileiradePediatria.PublicadoporElsevierEditoraLtda.Este ´eumartigo OpenAccesssobumalicenc¸aCCBY-NC-ND(http://creativecommons.org/licenses/by-nc-nd/4. 0/).
Introduction
Type1diabetesmellitus(DM1)isoneofthemostcommon chronicdiseasesofchildhoodandadolescence.Itis charac-terizedbychronichyperglycemiaandimpairedmetabolism of carbohydrates, proteins, and lipids. The physiopathol-ogy of this type of diabetes is autoimmune destruction ofpancreatic cellsaccompanied bydeficiencyof insulin production.1
Maintaining the best glycemic control possible, avoid-ingcomplicationsintheshort,mediumandlongterm,and allowing adequate psychological and emotional develop-ment are the main objectives of treatment of DM1.2 To reach these objectives, DM1 patients require the use of insulin,controloftheirdiet,andexercise.3Usually, these patientsareactivelyinvolvedintheirtreatmentonadaily basis, which includes performing various procedures and analyzinginformationtomakedecisionsforinsulin admin-istration, diet, and physical activity. However, glycemic controlmaybecomplicatedandchallenging,evenforthose patients with a good understanding of their illness and complications. Inpediatric patients withDM1,the partic-ipation of an informal primary caregiver (IPC) is needed in the decision-making process because their mental and
physical capacity is not optimal, particularly in younger children.4
AnIPCisapersonintheenvironmentofapatientwhois voluntarilyresponsible for the patient without any remu-neration. Interventions that IPC must provide when they arecaring for children withDM1 include:application and adjustmentof the dose of insulin, properlyproviding the typeandamountoffood,exercisesupervision,monitoring capillary blood glucose, and managing hypoglycemia and hyperglycemia.5 IPC activities are often very demanding; the more timespent in the care of a diabetic child, the more she/he sacrifices her/hisown resources, which can alterher/hishealthandwelfare.6Thecaregivermay expe-rienceanger,fear,emotionalambivalence,socialisolation, pathologicalgrief,anxiety,orstress.7---9
childrenwithDM1.12IthasalsobeenobservedthatIPCswith reasonablereadingandmathematicalskillshaveapositive influenceonglycemiccontrol,13whichalsooccurswhenthe wholefamilyparticipatesin thetreatment or when there aremorepeoplewhosupporttheIPC’sactivities.14
In pediatric patients withDM1, informationabout the impact of the IPC is scarce. Therefore, the aim of this studywastodeterminewhetherIPCcharacteristicsmaybe relatedtoglycemiccontrol.
Patients,
materials,
and
methods
Across-sectionalstudywasperformed.DM1patientstreated in the Pediatric Endocrinology service of the Children’s Hospital,XXICenturyNationalMedicalCenter,Mexican Insti-tute of Social Security (IMSS) were included. All patients wereprepubertal andpredominantly managed by an IPC. Patientswithintheperiodof DM1remission(‘‘honeymoon period’’),thosewithconcomitantuncontrolled chronic ill-ness(suchashypothyroidism,depression,orepilepsy),using steroids, with anemia, or those with a history of hospi-talization or more than three infectious events over the past three months were excluded.3 The following selec-tioncriteriawereconsideredfortheIPC:adultswhocould readandwrite,andwhoundertookspecificactivities(food preparation,applicationofinsulin,andbloodglucose mon-itoring)forthecareofDM1patients.Glycemiccontrolwas assessedbyglycosylatedhemoglobin(HbA1C);patientswere consideredcontrolledoruncontrolledaccordingtothe rec-ommendationsoftheAmericanDiabetesAssociation(ADA). Childrenunder6yearsofagewerecontrolledwithHbA1C <8.5%, and patients between 6 and 12 years of age with levels<8%.1,3 IPCswerescheduledforan interviewandto complete questionnaires within the first two weeks after takingthebloodsampleforHbA1CfromtheDM1patient.
The followingIPC variablesrelatedtoglycemiccontrol were studied: age, sex, patient relationship, occupation, lengthofworkinghours,education,supportofanother per-sonforpatientcare,andthepresenceofanxietyorstress. Socioeconomicstatus(Bronfmanquestionnaire)15andfamily functionalitywerealsoassessed.
Depression in the IPC was identified through the Beck questionnaire,aself-administeredinstrumentvalidatedfor Spanish-speaking adults.Depressed patients weredefined as having a score ≥10.16 The Perceived Stress Scale was
usedtoassess self-perceived stress; thisscale consistsof 14questionswithfiveoptions.Scoresrangefrom0(noneor minimalperceivedstress)to56(maximumperceivedstress); values<30characterizedsubjectswithoutstress.Thisscale hasalsobeenvalidatedintheMexicanpopulation.17,18The FamilyAPGARquestionnairewasusedtodetermine family functionality. It consistsof five components: adaptability, cooperation,development,affection,andresolution capac-ity.Ascore≥7definedgoodfamilyfunctionality.19,20
ThestudywasapprovedbythehospitalHealthResearch Committee;parentssignedaninformedconsentform,and childrenolderthan8yearssignedaletterofassent.
Statisticalanalysis
Quantitativevariablesarepresentedasmedians,minimum values (min.), and maximum values (max.); qualitative
variablesarepresented asabsolute numbersand percent-ages. The chi-squared test, Fisher’s exact test, and the Mann---WhitneyUtest wereusedforcomparisons between the groupwithadequate glycemiccontroland the uncon-trolled group. The association of factors associated with uncontrolledbloodglucosewasdeterminedusingoddsratios (OR)and95%confidenceintervals(95%CI).Amultivariate logisticandalinearregressionmodelwerebuilttocontrol forconfoundingvariables.Allanalyseswereperformedusing SPSS(SPSSforWindows,version15.0,USA).
Results
Sixty-threeeligiblepatientswereidentifiedinthePediatric EndocrinologyService.Eightwereexcluded,threebecause theIPCdeclinedtoparticipate,fourpatientswerein remis-sion,andonepatientwasonsteroidtherapyforeosinophilic colitis. Thus, a total of 55 patients were included with agesrangingfrom2to11years.Thereweremorefemale patients,witha2:1ratio.ThetimeevolutionofDM1ranged from eight months to 11 years nine months. Only eight patientshadconcomitantdiseases(threeprimary hypothy-roidism, threeepilepsy, and twodepression), which were undercontrol.Allof theIPCswerewomen;53(95%)were thepatients’mothers.Theiragerangedfrom21to54years, andmost(42%)hadstudiedthroughhigh-schoolora tech-nical school.Withrespect tothecomposition offamilies, mostwerenuclear(n=43,78%)and20%weresingleparent. The insulinregimenfor allpatientswasbasedonmultiple injectionsduringtheday.Nopatientusedaninsulininfusion pump. In addition,theusual frequency of self-monitoring bloodglucosewasbeforeandtwohoursaftereachmeal.
Comparisonofthecharacteristicsaccordingto glycemiccontrol
Patientsweredividedintwogroupsaccordingtoglycemic controlbasedonthelevelsofHbA1C.Twenty-ninepatients (53%) comprised thecontrolled group, and26 (47%) were in the uncontrolled group. Table 1 compares the charac-teristics of both the patients andthe IPC associatedwith glycemicdyscontrol.Asnoted,therewerestatistically sig-nificantdifferencesinsomepatient-relatedfactors:longer durationofDM1,non-adherencetomedicalindications,and dietetic transgression. Itwas alsodetermined the follow-ingICPfactorswereassociatedwithuncontrolledglycemia: lowereducationallevel,presenceofdepression,stress,and familydysfunction.
Table1 Comparisonoffactorsrelatedtoglycemiccontrolofpediatricpatientswithtype1diabetesmellitus.
Characteristic Controlledn=29 Uncontrolledn=26 p
n(%) n(%)
Glycosylatedhemoglobin(%) 7.6(6.5---8.5)a 9.2(8.6---13)a <0.01
Gender
Male 19(65.5) 17(65.4)
0.67
Female 10(34.5) 9(34)
Patientage(years) 7.6(2---10)a 8.7(4---11)a 0.37
DMtimeofevolution(years) 1.7(0.6---9.1) 3.1(0.7---9.7) 0.008
ICPage(years) 35(24---47)a 34(21---54)a 0.71
ICPeducationallevel
Primary 3(10.4) 2(8)
0.09
Highschoolortechnicalcareer 8(27.6) 15(58)
Undergraduate 5(17.2) 3(11)
Universityeducationorhigher 13(44.8) 6(23)
ICPgroupededucationallevel
Highschool/technicalschoolorprimary 11(38) 17(66) 0.045
ICPemployment
Housewife 18(62.1) 13(50)
0.74
Officeemployee 4(13.8) 9(34.6)
Seller 1(3.4) 0
Manager 4(13.8) 4(15.4)
Teacher 2(6.9) 0
DepressivetraitsinICP 9(31) 17(65) 0.013
StressinICP 2(7) 17(65) <0.001
Socioeconomicstatus
Good 28(89.1) 23(88.5)
0.24
Fair 1(3.4) 3(11.5)
Familyfunctionality
Normal 26(89.6) 16(61.5)
0.049
Mildfamilydysfunction 2(7) 6(23.1)
Severefamilydysfunction 1(3.4) 4(15.4)
Supportofanotherpersoninpatientcare 25(86.2) 16(61.5) 0.036
Inadequatephysicalactivity 8(27.5) 5(19.2) 0.46
Non-adherencetomedicalindications 3(10) 9(35) 0.03
Dietarytransgression 6(21) 22(85) <0.001
ICP,informalprimarycare.
a Median(minimumandmaximumvalues).
years.However,thistrend wasnotstatisticallysignificant (p>0.05).
Thisstudyalsoassessedwhetherthepresenceofanother persontosupportthecare of DM1patientsmayinfluence glycemic control. The proportion of ICPs with stress or depressionwaslowerwhentherewassupportfromanother person compared withthose without such support (21.4% vs. 53.1%). Furthermore, the presence of another person involved in patientcare wasmore prevalentamong func-tionalfamilies(81.0%vs.19.0%)thandysfunctionalfamilies (53.8% vs.46.2%). This differencewasstatistically signifi-cant(p=0.05).
Table 2 shows that presence of stress in the ICP (OR 24.85, 95% CI 4.064---151.96) was the main factor associ-atedtouncontrolledbloodglucose,accordingtothelogistic regressionanalysis,inwhichthefactorsrelatedtothe pri-marycaregiver wereincluded. However,itmust benoted
thattheICPeducationallevel(primaryor highschool)did notreach statistical significance eventhough the OR was 4.34(95%CI0.929---20.267).
Interestingly, in the linear regression model (Table 3), taking into account the quantitative value of glycated hemoglobinas outcome measure, it wasdetermined that lower level of education (ˇ 0.991, 95% CI 0.238---1.743, p=0.011)andstress(ˇ1.918,95%CI1.10---2.736,p=0.001) inthe ICP, aswell asfamily dysfunction(ˇ 1.256,95% CI 0.336---2.177,p=0.008)wereassociatedwithhigherlevels ofglycatedhemoglobin.
Discussion
Table2 Multivariatelogisticregressionanalysisoffactorsassociatedtouncontrolledglycemiclevelsinprepubertalpatients withtype1diabetesmellitus.
Factor OR 95%CI p
Education:primaryorhigh-school 4.34 0.929---20.267 0.062 Lackofsupportfromanotherpersoninpatientcare 0.623 0.0936---4.149 0.625
Familydysfunction 4.86 0.716---33.10 0.106
Depressivetraits 0.762 0.716---2.472 0.651
Stress 24.854 4.064---151.96 0.001
complications. In pediatric patients, the comprehensive managementofthis diseaserequires theactive participa-tionof thepatientand his/herfamily.21 The physical and emotional health of the ICP and his/her ability to make decisionsmayinfluencethecareofchildrenwithdiabetes. Totheauthors’knowledge, thisisthefirststudy reported intheLatin-Americanpopulationontheroleof theICPin DM1pediatricpatients;similarstudieshavebeen reported inpopulationsfromtheUnitedStatesorEurope.22---24
The results of this study shouldbe considered reliable becausedifferentfactorswerecontrolled.Onlyprepubertal patientswereincluded becausetheICP hasavery impor-tantrole inthat age group,aswell astoavoid confusion relatedtohormonalchangesinthevariouspubertalstages. Glycemiccontrol(accordingtoHbA1clevels)wasthemain outcomemeasurebecauseveryfewofthepatientshad addi-tional metabolic alterations, as expected in this type of diabetesinprepubertalpatients.Todeterminetheeffects ofthevariablesdirectlylinkedtotheICP,thisstudyincluded variablesknowntoalterglycemiccontrol.25
Eachpatientincludedinthisstudyisgrantedfree medi-caltreatmentandconsultationondietandexercise,aspart oftheservicesofferedbytheInstitution(IMSS).These fam-ilies, in general,have asocioeconomic status that allows them to follow medical advice. The mothers of patients weretheICPin95%of thecasesstudied;itisnoteworthy that42%workedoutsideofthehome,butthisconditiondid notinfluencethepatients’glycemiccontrol.Indeveloped countries,approximately15%oftheICPsofDM1patientsare thefather,notthemother.24,26UnlikeAmericanorEuropean populations,10,12,23,26 inthepresentstudy,mothersnotonly statedthattheirspouses’employmentstatusdidnotallow themto participatein the care of children withdiabetes but alsothat they believed that care had tobe provided exclusivelybythemothers.
DM1 is a chronic and currently incurable disease that leadstocomplicationsinthemediumandlongterm, requir-ingtheactiveparticipationofpatientsandtheirfamiliesin
treatment.Alloftheseaspectsaffectfamilies,particularly theICP.Usually,afterthefirstyearofdiagnosis,most fam-ilies acceptthediseaseandincorporateit intotheirdaily lives. When this does nothappen or familydysfunction is present, the risk of uncontrolled blood glucose is high.27 Familydysfunction(oftenaccompaniedbyinequitable dis-tributionof responsibilitiesamongmembers),the needto make daily decisionsfor the patient, andlack of adapta-tiontothediseasecan causetheICPtodevelop stressor depression.28,29Asdemonstratedinthepresentstudy,these two conditions are factors associated with uncontrolled patientbloodglucoselevels.Thisfindingisconsistentwith previous studiesinother populations.22,23 This observation supportstheutilityofpsychologicalandeducational inter-ventionswithpatientsandtheirfamilies,inwhichskillsto solveproblems--- notonlythoserelatedtothediseaseitself --- andthosethatcanencourageteamworkarepromoted.28
Additionally,physiciansshouldemphasizethatwhenboth parentsareinvolvedandtrainedinDM1treatment, decision-making that results in the best treatment is increased.30 Physiciansmustalsoinvestigatethepresenceofcertain psy-chologicalfactorsinthepatientorhis/herenvironmentthat requireevaluationbyamentalhealthexpert.
ItmightbeexpectedthatICPswithmoreyearsof school-ing would have a better understanding of the disease, itscomplications,andthedecision-makingprocess.Inthis study ICPschooling influencedthelevelsof HbA1C. Other authorsreportedthatICPswithloweducationallevelscan achievegoodglycemiccontrolinDM1pediatricpatients.22It ispossiblethatnumericalandreadingskillsratherthan edu-cationitselfpositivelyinfluencetheglycemiccontrolofthe patient.13Inaddition,thediseaseevolutiontimemayfavor glycemic control for two main reasons: the ICPs improve theirskills,andpatientslearnandparticipatemoreintheir owntreatment. However,inthelattersituation,the pedi-atric patientis less supervised, whichcan leadto lack of adherencetoallmedicalrecommendations,includingdiet andphysicalactivities.Dietarytransgressionof21---95%has
Table3 Linearregressionanalysisoffactorsassociatedtoglycated hemoglobinlevelsinprepubertal patients withtype1 diabetesmellitus.
Factor ˇ 95%CI p
Education:primaryorhigh-school 0.991 0.238to1.743 0.011 Lackofsupportfromanotherpersoninpatientcare −0.403 −1.331to0.524 0.386
Familydysfunction 1.256 0.336to2.177 0.008
Depressivetraits −0.078 −0.552to0.365 0.725
beenreportedforchildrenunder8yearsold.31These trans-gressionsmayoccurbecausemostchildrenmakedecisions independently.
Toputtheobtainedresultsintoperspective,the limita-tionsofthis studymustbetakenintoaccount.Oneis the design;thiswasacross-sectionalstudy,soHbA1Cwas mea-suredonlyonce, whichdoes notnecessarilyreflectactual glycemiccontrol,atleastinthelastyear.This,inaddition tosmallsample size,couldpreventconclusive determina-tionregardingwhetherdepressioninICPsisassociatedwith glycemicdyscontrol.
In conclusion, this study found that uncontrolled glycemiainprepubertalchildrenwithDM1isassociatedwith factorsdirectlyrelatedtotheICP,suchasstressandfamily dysfunction.Therefore,toimprovetheclinicalconditionof thesepatients,itwillbenecessarytostrengthentheroleof theICPineachoftheaspectsofcomprehensivecare.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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