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Primary Care Diabetes
j o ur na l ho me p ag e:h tt p://ww w . e l s e v i e r . c o m / l o c a t e / p c d
Original research
Impact of diabetes mellitus on COVID-19 clinical symptoms and mortality: Jakarta’s COVID-19 epidemiological registry
Dante S. Harbuwono
a,b,∗,1, Dwi O.T.L. Handayani
c,1, Endang S. Wahyuningsih
c, Novita Supraptowati
c, Ananda
c, Farid Kurniawan
a,b, Syahidatul Wafa
a,b,
Melly Kristanti
b,d, Nico I. Pantoro
b, Robert Sinto
e, Heri Kurniawan
f, Rebekka
c,2, Dicky L. Tahapary
a,b,2aDivisionofEndocrinology,Metabolism,andDiabetes,DepartmentofInternalMedicine,Dr.CiptoMangunkusumoNationalReferralHospital,Facultyof Medicine,UniversitasIndonesia,Jakarta,Indonesia
bMetabolic,Cardiovascular,andAgingCluster,TheIndonesianMedicalEducationandResearchInstitute,FacultyofMedicine,UniversitasIndonesia, Jakarta,Indonesia
cJakartaProvincialHealthDepartment,Indonesia
dDepartmentofPublicHealth,FacultyofMedicineUniversityPembangunanNasional“Veteran”Jakarta,Indonesia
eDivisionofInfectionandTropicalDisease,DepartmentofInternalMedicine,Dr.CiptoMangunkusumoNationalReferralHospital,FacultyofMedicine, UniversitasIndonesia,Jakarta,Indonesia
fDivisionofPulmonologyandCriticalCare,DepartmentofInternalMedicine,Dr.CiptoMangunkusumoNationalReferralHospital,FacultyofMedicine, UniversitasIndonesia,Jakarta,Indonesia
a rt i c l e i nf o
Articlehistory:
Received19October2021 Accepted7November2021 Availableonline12November2021
Keywords:
Clinicalsymptoms COVID-19 Diabetesmellitus Indonesia Mortality
a b s t ra c t
Backgroundandaims:Whilethehigherprevalenceofdiabetesmellitus(DM)atyoungerageinIndonesia mightcontributetotherelativelyhigherCOVID-19mortalityrateinIndonesia,therewerecurrently noavailableevidencenorspecificpolicyintermsofCOVID-19preventionandmanagementamongDM patients.Weaimedtofindouttheassociationbetweendiagnoseddiabetesmellitus(DM)withCOVID-19 mortalityinIndonesia.
Methods:WeperformedaretrospectivecohortstudyusingJakartaProvince’sCOVID-19epidemiological registrywithinthefirst6monthsofthepandemic.AllCOVID-19confirmedpatients,aged>15years withknownDMstatuswereincluded.Patientswereassessedfortheirclinicalsymptomsandmortality outcomebasedontheirDMstatus.AmultivariateCox-regressiontestwasperformedtoobtaintherelative risk(RR)ofCOVID-19mortalityinthediagnosedDMgroup.
Results:Of20,481patientswithCOVID-19,705(3.4%)hadDM.COVID-19mortalityrateinDMgroupwas 21.28%,significantlyhighercomparedto2.77%mortalityinthenon-DMgroup[adjustedRR1.98(CI95%
1.57–2.51),p<0.001].Inaddition,COVID-19patientswithDMgenerallydevelopedmoresymptoms.
Conclusions:DMisassociatednotonlywithdevelopmentofmoreCOVID-19clinicalsymptoms,butalso withahigherriskofCOVID-19mortality.Thisfindingmayprovideabasisforfuturepolicyregarding COVID-19preventionandmanagementamongdiabetespatientsinIndonesia.
©2021PrimaryCareDiabetesEurope.PublishedbyElsevierLtd.Allrightsreserved.
∗ Correspondingauthorat:DivisionofEndocrinology,Metabolism,andDiabetes, DepartmentofInternalMedicine,Dr.CiptoMangunkusumoNationalReferralHos- pital,FacultyofMedicine,UniversitasIndonesia,Jakarta,Indonesia.
E-mailaddress:dante.saksono@ui.ac.id(D.S.Harbuwono).
1 Theseauthorshavecontributedequally.
2 Theseauthorsalsocontributedequallytothiswork.
1. Introduction
Indonesia,asthefourthmostpopulouscountryintheworld,has struggledwithahugenumberofCOVID-19casesduringthemore- than-one-yearpandemic.Thetotalcaseshavesofarreachedmore than1.5millionasofApril2021[1],placingIndonesiaasoneofthe AsiancountrieswiththehighestnumberofCOVID-19cases[1–3].
ThemortalityrateofCOVID-19inIndonesiahasbeenreportedto beslightlyhigher thantheworldwide estimate[1], despitethe relativelyyounger population structure. This,in part,might be contributedbytherelativelyhigherprevalenceofcardiometabolic https://doi.org/10.1016/j.pcd.2021.11.002
1751-9918/©2021PrimaryCareDiabetesEurope.PublishedbyElsevierLtd.Allrightsreserved.
D.S.Harbuwonoetal. PrimaryCareDiabetes16(2022)65–68
diseases,includingdiabetesmellitus(DM),atyoungeragegroup [4–8].
Previous studieshighlightedthatthose withcardiometabolic risk factors such as diabetes mellitus (DM) have been associ- atedwiththeworseclinicalmanifestation andhighermortality inCOVID-19[9–11].Thechroniclow-gradeinflammationstatein peoplewithDMsetthestageforfurtherelevationsofinflamma- torycytokinesinCOVID-19.Furthermore,immunedysregulation inDMimpairsthehost’sabilitytocombatthedisease,providing thesepopulationswithpoorerinfectionoutcomes[12,13].How- ever,despiteoverwhelmingevidenceontheassociationbetween DMandworseCOVID-19outcomes,evidencefromAsiancountries outsideChina,especiallyIndonesiaislacking[14,15].
Thislackofevidenceitselfmightaswellcontributetothelack ofinitiativestoprovideprioritizationofCOVID-19preventionand careamongthosewithDMinIndonesia.Therefore,ourstudyaims todescribetheassociationbetweendiagnosedDMwithCOVID- 19 mortalityfromtheJakartaarea,thecapitalcityofIndonesia, duringthefirst6monthsoftheCOVID-19pandemic.Inaddition, wealsocomparetheclinicalsymptomsbetweenthosewithand withoutDM.Evidencereportedinourstudywillnotonlyenrich theavailableevidenceontheassociationbetweenDMandCOVID- 19mortalityinAsianandlowtomiddleincomecountries,butmay alsosetareasonablebasisforfuturepolicyinthetermsofCOVID-19 preventionstrategies,includingvaccination,whilealsoproviding insightsonthedifferenceonclinicalsymptomsforCOVID-19early detectionandcareamongDMpatient.
2. Methods
Ourstudywasaretrospectivecohortstudywhichincludedall confirmedcaseofCOVID-19fromtheJakartaprovinceareafrom 2ndMarch2020,thefirstCOVID-19caseinIndonesia,until31st August2020.Subjectsaged15yearsoldormoreandwithoutany missing dataonpreviousDMdiagnosisstatus wereincludedin thestudy.EthicalapprovalwasobtainedfromtheResearchEthics CommitteeoftheFacultyofMedicine,UniversitasIndonesiawith approvalnumberKET-821/UN.2.F1/ETIK/PPM.00.02/2020.
2.1. Datacollection
WereviewedtheEpidemiologicalSurveillance(ES)formofall COVID-19patientsintheJakartaprovinceareacollectedbythe JakartaProvincialHealthDepartment.ESformwasfilledbythe attendingdoctorsoftheCOVID-19patientsfromallhealthfacilities, includingallprimaryhealthcare,publicandprivatehospitals.The ESformconsistsofquestionsrelatedtothepatient’sdemographic andclinicalcharacteristics,includingsignsandsymptoms,comor- bidities,andmortalityoutcomes.DiagnosisofCOVID-19caseswas confirmedbyreversetranscriptase-polymerasechainreaction(RT- PCR)oftheoro-and/ornaso-pharyngealswabspecimen.Patients wereclassifiedashavingDMwhenDMwaspresentinthehistory profileand/orreceivedantidiabeticmedicine(s)beforeCOVID-19 diagnosis.Allpatientsnotmeetingthesecriteriawereincludedin thenon-DMgroup.Othercomorbiditiessuchashypertension,heart disease,chronickidneydisease,andchronicliverdiseasewerediag- nosedbasedonthehistoryprofileand/oranytreatmentforeach respectivediseasegivenbeforeCOVID-19diagnosis.
2.2. Studyoutcome
Theprimaryendpointwasall-causemortality.Alldeaththat occurredafterthediagnosisofCOVID-19wasconsideredthecon- sequenceoftheCOVID-19infection.
Fig.1. Consortdiagramofstudysubjectsinclusion.
2.3. Statisticalanalysis
Comparison between two groups was analyzed using Chi- SquaretestforcategoricaldataandunpairedT-testfornumerical data.Asage,sex,andothercomorbiditieswerereportedtoaffect COVID-19mortalityinmanypreviousstudies,theywereconsid- eredasconfoundingvariablesinthisstudy.Thus,amultivariate Cox-regressiontestwasperformedtoobtaintherelativerisk(RR) ofdiagnosedDMwithCOVID-19mortalityandwasadjustedfor age,sex,andothercomorbidities.Alldataanalysiswasperformed usingSPSSversion25.
3. Results
Atotalof27,863COVID-19patientswereregisteredduringthe studyperiod.Afterexclusionofsubjects<15yearsoldandmiss- ingdiabetesdiagnosisstatus, 20,481subjectswereincludedfor analysis(Fig.1).
Thebaselinecharacteristicsofourstudysubjectsaresumma- rizedinTable1.Diabetesdiagnosiswasobservedin705(3.44%) patients.Theyweregenerallyolderandwithmorecomorbidities thanthenon-DMgroup.Moreover,COVID-DMpatientswerealso morelikelytohavesymptomsthanthenon-DMgroup,notably fever,cough,dyspnea,nausea/vomitus,andpneumonia.
WhilethemortalityrateforCOVID-19intheoverallpopulation ofthisstudywas3.41%,forthosewithDMitwas21.28%.Thepres- enceofDMwassignificantlyassociatedwithincreasedmortality inCOVID-19patients[unadjustedRRand95%confidenceinterval (CI):7.67(6.51–9.04)](Table2).Inaddition,afteradjustmentfor age,sex,andothercomorbidities,DMwasassociatedwithalmost twicetimeshighermortalityinCOVID-19patientscomparedto non-DM(Table3).
66
Table1
BaselinecharacteristicsofCOVID-19patientinJakarta.
Characteristics Total(n=20,481) DM(n=705) Non-DM(n=19,776) p-Value
Age(mean,years) 41.8(16.8) 57(14.5) 41(16.6) <0.001
Women(n,%) 9817(47.94) 328(46.52) 9489(47.99) 0.23
Hypertension(n,%) 1189(5.82) 356(50.5) 833(4.2) <0.001
Heartdisease(n,%) 515(2.5) 168(23.9) 347(1.8) <0.001
Chronickidneydisease(n,%) 152(0.74) 89(12.6) 63(0.3) <0.001
Chronicliverdisease(n,%) 54(0.26) 37(5.3) 17(0.1) <0.001
Historyoffever(n,%) 2417(11.80) 349(50.07) 2068(10.48) <0.001
Cough(n,%) 3181(15.53) 459(65.38) 2722(13.78) <0.001
Runnynose(n,%) 1234(6.02) 144(20.51) 1090(5.52) <0.001
Sorethroat(n,%) 1187(5.79) 170(24.22) 1017(5.15) <0.001
Dyspnea(n,%) 1516(7.40) 335(47.65) 1181(5.98) <0.001
Shivering(n,%) 575(2.80) 120(17.39) 455(2.31) <0.001
Headache(n,%) 1369(6.68) 225(32.42) 1144(5.80) <0.001
Musclepain(n,%) 938(4.58) 158(22.80) 780(3.95) <0.001
Nauseaandvomitus(n,%) 1263(6.20) 277(40.38) 986(5.01) <0.001
Abdominalpain(n,%) 594(2.90) 137(19.74) 457(2.32) <0.001
Diarrhea(n,%) 436(2.13) 106(15.30) 330(1.67) <0.001
Pneumonia(n,%) 1670(8.2) 379(54.45) 1291(6.55) <0.001
ComparisonbetweentwogroupswasanalyzedusingChiSquaretestforcategoricaldataandunpairedT-testfornumericaldata.
Table2
TheeffectofDMonCOVID-19patient’smortality.
Variable Mortality Total p-Value RR(95%CI)
Death Survive
DM 150(21.28) 555(78.72) 705(3.44)
<0.001* 7.67(6.51–9.04)
Non-DM 548(2.77) 19,228(97.23) 19,776(96.56)
Total 698(3.41) 19,783(96.59) 20,481(100)
*pValue<0.05,Chi-Squaretest.
Table3
TheeffectofDMonCOVID-19patient’smortalityadjustedandcomparedtoother comorbidities.
Variable SE p-Value AdjustedRR(95%CI)
DM 0.120 <0.001* 1.98(157–2.51)
Hypertension 0.109 <0.001* 2.32(1.87–2.87) Heartdisease 0.131 <0.001* 1.61(1.24–2.08) Chronickidneydisease 0.187 <0.001* 2.02(1.40–2.91) Chronicliverdisease 0.412 0.602 0.81(0.36–1.81)
*pValue<0.05,multivariateCoxregressiontest,dataisadjustedbysexandage.
4. Discussion
Our studyconfirmedpreviousreportsthatDMwasindepen- dentlyassociatedwithasignificantlyhigherCOVID-19mortality.
Inaddition,clinicalsymptomsofCOVID-19wereconsistentlymore observedinthosewithDM.
TheincreasedmortalityriskinCOVID-DMpatientsbytwofold observed inourstudywassimilartothedatashown byprevi- ous meta-analysis [11]. Thereare several mechanisms onhow DMcouldincrease mortalityrisk inCOVID-19 patients. Asitis showninthisstudy,themajorityofDMpatientsinIndonesiahas chronicdiabeticcomplicationsandcardiometaboliccomorbidities, whichinpartisduetothehigherproportionofDMpatientsdiag- nosedatalatestage[6–8].However,despitethestrongattenuation after the adjustmentfor important cardiometabolic comorbidi- ties,theassociationbetweenDMandCOVID-19mortalitywasstill significant,suggestingotherpathwaysmightplayarole.Several pathwayshavebeenreportedtoplayarole:increasedexpression ofangiotensin-convertingenzyme-2(ACE-2)receptor,agingcells, ahigherpro-inflammatorycondition,andimpairedT-cellfunction andantibodyproduction[11].
Itisimportanttonotethatourstudyalsoobservedthatpatients withDMweremorelikelytopresentwithclinicalsymptomscom- paredtonon-DMpatients.Thesefindingswereinlinewithprevious
studywhichshownthatDMincreasestheriskforsevereCOVID-19 infection[9,11,16,17].However,ourfindingswereincontrastwith previousstudyreportedsimilarsymptomsofCOVID-19withpneu- moniaforbothDMandnon-DMgroup[18].Thisdifferencemight berelatedwiththedifferenceinthestudypopulation.Ourstudy analyzedthedatafromacentralizedCOVID-19registry,integrat- ingdatafromcontacttracingatcommunity,primaryhealthcare facilities,andhospital.Italsoincludedasymptomaticindividuals andmaythusbetterrepresenttheCOVID-19casesasawhole.
OurstudycouldnotprovideadirectanswerwhetherDMwas associatedwithahigherrisktocontractCOVID-19infection.Ifany- thing,theprevalenceofDMdiagnosisamongCOVID-19patients (3.4%)observedinourstudywasslightlyhighercomparedtothe DMprevalenceingeneralpopulationoftheJakartaprovincearea (2.6%)[5].OtherregistrybasedstudiesfromChinaandUnitedStates (US)showedaDMprevalenceinCOVID-19patientsof5.3%and 10.9%,respectively[19].ThisprevalenceinChinaislowerthanthe generalpopulation,meanwhileintheUS,theprevalenceissimilar tothegeneralpopulation.However,therelativelylowerorsimilar proportionofDMamongCOVID-19infectedsubjectsincomparison tothoseobservedingeneralpopulationmightalsobecontributed bythewidelyavailablehealthinformationontheriskofCOVID-19 onDMpatientsandthatallDMpatientsshouldprotectthemselves more.
Despitehavingarelativelyyoungerageofpopulation,themor- talityratefor COVID-19inourstudywashigherin comparison toworldwidemortalityrate.Inourstudy,themortalityrateof COVID-19patientsinJakartawas3.41%.Thisnumberiscompa- rablewithIndia,anotherhighly-populatedlow-tomiddle-income country(LMIC),which reporteda casefatalityrateofCOVID-19 as3.17–3.88%inJune2020[20,21].However,otherLMICinSouth EastAsia,suchasMyanmar,showasignificantlylowermortality ratewithonly0.6%thankstoanoverallbettermanagementstrat- egyforCOVID-19preventionandmanagement[22].Nitetal.[23]
D.S.Harbuwonoetal. PrimaryCareDiabetes16(2022)65–68
statedonly302confirmedcasesofCOVID-19withnodeathinCam- bodia,anotherLMICcountryinSouthEastAsiawithlimitedhealth resources.Inpart,thepresenceofDMandothercardiometabolic riskfactorsatayoungeragemightplayarole[7,8].Inaddition,a significantportionofsubjectswithcardiometabolicriskfactorsin Indonesiawereundiagnosedcases,includingthecasewithDMof whichmorethan70%ofDMcaseswereundiagnosed[8].More- over, majorityof DMpatientsin Indonesiafailed toreachtheir glycemictarget[6].Thesefindingsmightfurthercontributetothe increasemortalityrateduetoCOVID-19[24–26]bytheirinfluence onimmunedysfunction[27]andthromboembolicrisks[28].Itis alsoimportanttomentionthatotherfactors,suchasthelimited experienceduringearlypandemicandlimitedhealthcareresources mightalsocontributetotheincreasedmortality[4].Thesefindings mayalsosuggestthatthemanagementofCOVID-19inIndonesia stillhasroomforimprovement.
OurstudyisthefirststudythatshowedtheimpactofDMon COVID-19mortalityinIndonesia,afourthmostpopulouscountry intheworld.Thelargenumberofsubjectsanddataofothercomor- biditieswerestrongpointsforthisstudy.Nonetheless,thereare somelimitations.TheCOVID-19epidemiologicalregistrycollected fromtheESformistheonlydatacurrentlyavailabletobeana- lyzed.However,asthemajorityofresourceshadbeenallocated for thecareofCOVID-19patients,thecompletenessofthedata waslacking.Insuch,wehavenodataonwhetherDMwaswellor poorlycontrolled,andnoinformationonthelaboratoryparameter suchasbloodglucose,ordataondiabetesmedication.Important datarelatedwithmetabolicdisorderssuchasbodymassindexor obesitywasalsolacking.
5. Conclusions
In conclusion, ourstudynot only confirmedpreviousreport thatDMisindependentlyassociatedwithahigherriskofCOVID- 19mortality,butalsoevidencethatCOVID-DMpatientswerealso morelikelytohaveclinicalsymptoms.Thisresultmaybeusedas abasisforsettingapolicyregardingCOVID-19preventionamong DMpatient,includingthepriorityofCOVID-19vaccines.Inaddi- tion,developmentofacuteinfectionsymptomsamongDMpatients might warrant early and priorityaccess to COVID-19 test and care. Furtherstudyiswarranted tounderstandmoretheinter- relationshipbetweenthesetwodoublepandemics,especiallyits shortandlong-termhealthandeconomicimpact.
Conflictofinterest
Theauthorsdeclarethattheyhavenocompetinginterests.
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