The impact of implementing the WHO-2013 criteria for gestational diabetes mellitus on its prevalence and pregnancy outcomes: A comparison of the WHO-1999 and WHO-2013 diagnostic thresholds

Full

length

article

The

impact

of

implementing

the

WHO-2013

criteria

for

gestational

diabetes

mellitus

on

its

prevalence

and

pregnancy

outcomes:

A

comparison

of

the

WHO-1999

and

WHO-2013

diagnostic

thresholds

Madena

Shareef

_,

_Langeza

_Saleh

_*

_,

_Anton

_H.

_van

_den

_Meiracker

_,

_Willy

_Visser

a

DepartmentofObstetricsandGynecology,ErasmusMedicalCenter,Rotterdam,theNetherlands

b

DivisionofVascularMedicineandPharmacology,DepartmentofInternalMedicine,ErasmusMedicalCenter,Rotterdam,theNetherlands

ARTICLE INFO Articlehistory: Received10November2019 Accepted22December2019 Availableonlinexxx Keywords:

Gestationaldiabetesmellitus WorldHealthOrganization Pregnancyoutcomes

75goralglucosetolerancetest(OGTT)

ABSTRACT

Aims/hypothesis:TodeterminetheimpactofimplementingthenewWHO-2013criteriaonprevalenceof

gestationaldiabetesmellitus(GDM)andpregnancyoutcomescomparedtotheWHO-1999criteria.

Methods:AretrospectivestudyconductedinpregnantwomenwhowerereferredtotheErasmusMCfor

anoralglucosetolerancetest(OGTT)between2010and2015.

Results:Of3089women,11.5%(n=354)werediagnosedwithGDMbasedontheWHO-1999criteriaand

17.0%(n=524)basedonthe2013–criteria,with97(3.1%)reclassifiedasnon-GDMand267(8.6%)

reclassifiedasGDMwhenshiftingfromthe1999to2013-criteria.Incontrastto60%ofpatientsinthe

WHO-2013group,only2%oftheWHO-1999groupwasdiagnosedwithGDMbecauseofanelevated

fastingglucoseonly.PatientsreclassifiedasGDMbyWHO-2013criteriahadahigherbodymassindex

(p<0.001)anddeliveredbabieswithahigherbirthweight(p=0.01).Maternalandneonataladverse

outcomeswerecomparablebetweenpatientswithGDMbasedonWHO-1999criteriaandpatientsnewly

includedbyWHO-2013criteria.

Conclusions:Implementingthenewdiagnosticcriterialeadstoaconsiderableincreaseofprevalenceof

GDM.Thenewlyincludedpatientsweremorefrequentlyoverweighedanddeliveredbabieswithahigher

birthweight.TheaddeddiagnosticvalueofthefastingglucosethresholdoftheWHO-1999criteriaisvery

lowcomparedtothe2-hpost-OGTTthreshold,supportingtheuseofalowerfastingglucosethreshold

valueasadvocatedbytheWHO-2013criteria.

Tweet:ThenewWHO-2013criterialeadstoaconsiderableincreaseofprevalenceofGDM.

©2019PublishedbyElsevierB.V.

Introduction

Gestationaldiabetesmellitus(GDM)isdefinedasnewonsetor firstrecognitionofabnormalglucosetoleranceduringpregnancy [1].TheestimatedprevalenceofGDMintheNetherlandsvaries between2–5 % [2]. Due to the rising epidemic of overweight, obesityandincreaseinmeanmaternalagetheprevalenceofGDM

isrisingandconstitutesthemostcommonmetaboliccomplication duringpregnancy[3–5].

AmongthemainconsequencesofGDMareincreasedrisksof preeclampsia (PE),macrosomia and cesareandeliveryand their associatedmorbidities[6].Inaddition,higherplacentalpassageof glucosecanresultinpostnatalhyperinsulinemiaand hypoglyce-miainnewborninfantspotentiallycompromising neurodevelop-mental outcomes [6]. Identifying pregnant women with GDM followedbyfrequentglucosemonitoring andappropriate treat-ment, including dietary advices and/or insulin therapy and/or otherglucoseloweringmedication,hasreportedtobeassociated withadecreaseinmacrosomia,shoulderdystocia,andPE[6].

Since GDM is mostly asymptomatic, laboratory screening is required for its detection. The DutchSociety of Obstetricsand Gynecology (NVOG) recommends screening at 24–28weeks of gestationinpregnantwomenwithriskfactorsfordevelopingGDM andafirstscreeningat16weeksgestationinwomenwithahistory ofGDM[7,8].

Abbreviations: BMI,bodymass index;CS,caesareansection; DM,diabetes mellitus;GDM,gestationaldiabetesmellitus;HAPO,HyperglycemiaandAdverse PregnancyOutcomesstudy;IADPSG,TheInternationalAssociationoftheDiabetes andPregnancy Study Groups;LGA, largefor gestational age; NICU,neonatal intensivecareunit; OGTT,oral glucose tolerancetest;PE,preeclampsia;PIH, pregnancyinducedhypertension;SGA,smallforgestational age;WHO,World HealthOrganization.

*Corresponding authorat:Department ofInternal Medicine,Room Ee1418, ErasmusMedicalCentre,P.O.Box2040,3000CA,Rotterdam,theNetherlands.

E-mailaddress:l.saleh@erasmusmc.nl(L.Saleh).

1

Theseauthorscontributedequally. https://doi.org/10.1016/j.ejogrb.2019.12.013 0301-2115/©2019PublishedbyElsevierB.V.

ContentslistsavailableatScienceDirect

European

Journal

of

Obstetrics

&

Gynecology

and

Reproductive

Biology

Theoralglucosetolerance test(OGTT) ismostoftenusedto diagnose GDM. TheNVOG recommendsa 75g OGTT using the cut-offvaluesoftheWorldHealthOrganization(WHO)published in1999:afastingplasmaglucoselevel(FG)7.0mmol/Lora2-h plasmaglucoselevel(2hG) of7.8mmol/L[7,8].Following the HAPOstudy(HyperglycemiaandAdversePregnancyOutcomes), the International Association of the Diabetes and Pregnancy Study Groups (IADPSG) proposed new diagnostic criteria for GDM: FG5.1mmol/L, 1-hr level of  10mmol/l or a 2hG level8.5mmol/L[9].Subsequently,theWHOadoptedthesenew diagnostic criteria for GDM in 2013 [10]. Compared to the WHO-1999 criteria, the WHO-2013 criteria are based on a considerablylowerthresholdfor fastingbut a higherthreshold forthe2-hpostloadingglucoselevel.

The WHO-2013 criteria have not been implemented in the Netherlands yet. In a retrospective study, we investigated the consequencesofapplyingWHO-2013criteriaontheprevalenceof GDM and the incidence of adverse maternal and neonatal outcomes.

Methods Studyparticipants

Aretrospectivestudywasconductedofpatientswho under-went a 75-g OGTT from June 2010 to September 2015 at the ErasmusMC.Patientswerereferredbytheirmidwifeorbytheir gynecologistfora75-gOGTTiftheyhadoneormoreriskfactorsfor GDM according to the Dutch national guideline [7]. Pregnant women with an abnormal OGTT according to the WHO-1999 criteria or the WHO-2013 criteria were eligible for analysis. Importantly,becauseGDMaccordingtoWHO-2013wasdiagnosed retrospectivelyonlywomenwithadisturbedOGTTaccordingto theWHO-1999criteriaweretreatedforGDM.Womenwith pre-existingdiabetes,twinpregnancyand a deliveryoutside of the ErasmusMCwereexcluded.

Measurements

Plasmaglucosemeasurementswereperformedattheclinical laboratoryoftheErasmusMC.Plasmaglucosewasmeasuredbyan enzymatic hexokinase method(Roche/Hitachi cobas c systems, Manheim,Germany).

Outcomesanddefinitions

Dataonmaternalcharacteristics,pregnancyandfetaloutcomes wereretrospectivelycollectedfromthepatients’records.Alldata wereincorporatedinananonymizeddatabase.

Maternalcharacteristicswereage,parity,pre-gestationalbody mass index (BMI), positive family history of diabetes mellitus (DM),historyofGDM,HbA1clevelsandgestationalageatOGTT. Thematernaloutcomeswerethefollowing:HbA1clevelsofthe mother at time of diagnosis and delivery, treatment of GDM (dietary advices, insulin, oral medication or a combination), pregnancy induced hypertension (PIH) (systolic blood pressure 140mmHgand/oradiastolicbloodpressure90mmHgafter20 weeks of gestation in a previously normotensive woman), preeclampsia(PE)(gestationalorpre-existinghypertensionwith de novo proteinuria (>300mg/24h), mode of delivery (vaginal delivery,instrumentaldelivery,primarycaesareansection(CS)or secondaryCS).

Thefetaloutcomeswerethefollowing:birthweight(grams), small for gestational age (SGA; birth weight <10th percentile correctedforgestationalage,sexandparity),largeforgestational age(LGA;birthweight>90thpercentilecorrectedforgestational

age,sexandparity),prematurity(delivery<37weeksofgestation), shoulder dystocia, hyperbilirubinemia requiring phototherapy, neonatalhypoglycemia(bloodglucoselevel<2.6mmol/Latleast 3hpostpartum), admission to theneonatal intensive careunit (NICU),birthdefects,needforrespiratorysupportandmortality (intra-uterineorpostpartum).

Statisticalanalysis

IBMSPSSStatistics24wasusedforthestatisticalanalysis.The normalityofcontinuousvariableswasassessedusingthe Shapiro-WilkW-test.Continuousdatabetween_>2groupswerecompared usingANOVAincaseofnormaldistribution,theKruskalWallisin caseofskeweddistribution,withtheBonferronicorrectionincase ofmultiplecomparisons.Thechi-squaretestwasusedtocompare categoricaldataamongthegroups.Apvaluelessthan0.05was considered statistically significant. Continuous variables are presentedasmedian(range) andcategoricaldataarepresented asnumbers(percentage).

Results

PrevalenceofGDM

Atotalof3165OGTT’swerecarriedoutin3089subjectsfrom June2010toSeptember2015.Thirteenpatientswithanabnormal OGTT according to the WHO-1999 criteria or the WHO-2013 criteria (respectively five and eight) had to be excluded from analysisduetolosttofollow-up.

TheprevalenceofGDMwas11.5%(n=354)accordingtothe WHO-1999criteria,increasingto17.0%(n=524)whenthe WHO-2013criteriawereused.Whenshiftingfromoldtonewcriteria,97 womenwerereclassifiedasnon-GDM(WHO-2013excluded)and 267womenwerereclassifiedasGDM(WHO-2013included).

According to the WHO-1999 criteria 98 % of patients were diagnosed withGDMbecause ofanelevated 2-h and only2%because ofbothanelevatedfastingand2-hpostOGTTplasmaglucoselevel. Consequently,allwomendiagnosedwithGDMhadanelevated2-h postOGTTplasmaglucoselevel.IntheWHO2013group,58%was diagnosedwithGDMbecauseofanelevatedfastingplasmaglucose, 21%becauseofanelevated2-hplasmaglucoseand21%becauseof bothanelevatedfastingglucose and2-hglucose(Fig.1). Conse-quently79%couldbediagnosedwithGDMusingafastingplasma glucoselevelonlywhenusingtheWHO-2013criteria.

Characteristics

Ageamongthethreegroupswassimilaraswasthehistoryof GDM(Table1).Womenreclassifiedasnon-GDMaccordingtothe WHO-2013 criteria were more often nulliparous than women reclassi_fiedasGDM(p=0.02).ThepregestationalBMIofwomen whowerereclassifiedasGDMwashigher(p<0.001)thanthatofthe twoothergroups(Table1).HbA1clevelswerelower(p<0.001)in theWHO-2013excludedgroupthanintheWHO-1999group.

ThemajorityoftheWHO-2013includedgroupwerenottreated forGDM,buttreatmentmodalitiesforGDMbetweenthe WHO-1999andWHO-2013groupdidnotdiffer(Table2).Gestationalage atdeliveryamongthethreegroupswassimilaraswasthemodeof deliveryandoccurrenceofPE(Table2).Cesareansectionswereless oftenbasedonamaternalindicationintheWHO-2013excluded group. The birth weight in the newly included group was moderately higher than in thetwo othergroups (Table 3), but theproportionsofLGAneonatesamongthethreegroupsdidnot differ. There were no differences between the groups in the prevalenceofprematurity,shoulderdystocia,hyperbilirubinemia requiringphototherapy,admissiontoNICU,birthdefectsandneed

Table1 Maternalcharacteristics. WHO-1999 WHO-2013 excluded WHO-2013 included Column1 versus2 Column1 versus3 Column2 versus3 N 354 97 267 – – – Age,years 34(20–47) 32(20–45) 33(18–46) 0.177 0.999 0.731 Nulliparous 116(32.8) 39(40.2) 72(27.0) 0.185 0.134 0.020* PregestationalBMI,kg/m2 26.8(17–69) 25.6(17–45) 29.8(14–61) 0.223 <0.001* <0.001* PositivefamilyhistoryofDM,n(%) 161(45.9) 37(38.1) 108(41.1) 0.204 0.250 0.630 HistoryofGDM,n(%) 39(11.1) 8(8.3) 36(13.5%) 0.463 0.386 0.207 GestationalageatOGTT,weeks 28(8–40) 27(10–39) 25(10–38) 1.000 <0.001* 0.002* HbA1c,mmol/mol

Atdiagnosis 36(19–73) 33(19–43) – <0.001*

Atdelivery 36(21–56) 34(21–41) – 0.003*

BMI:Bodymassindex,DM:diabetesmellitus,GDM:gestationaldiabetesmellitus,OGTT:oralglucosetolerancetest,*:statisticallysignificant. Fig.1.PrevalenceofGDMinthecohortaccordingtobothcriteria.

PanelA:WHO-1999criteria(n=354)PanelB:WHO-2013criteria(n=524).

Table2 Maternaloutcomes. WHO-1999 WHO-2013 excluded WHO-2013 included Column1 versus2 Column1 versus3 Column2 versus3 N 354 97 267 – – – Treatment,n(%) Notreatment 9(2.5) 5(5.2) 228(85.4) 0.320 <0.001* <0.001* Dietandlifestyleadvice 224(63.3) 69(71.1) 25(9.4) 0.186 <0.001* <0.001* Oralmedication 11(3.1) 1(1.0) 2(0.7) 0.322 0.049* 0.793 Insulintreatment 110(31.1) 22(22.7) 12(4.5) 0.130 <0.001* <0.001* Weeksofinsulintreatment 8(1–25) 7(1–23) 3(1–19) 0.428 0.111 1.000

PIH,n(%) 31(8.8) 5(5.2) 19(7.1) 0.296 0.552 0.636

PE,n(%) 17(4.8) 3(3.1) 8(3.0) 0.587 0.306 1.000

GAatdelivery,weeks 38.7(25.6-41-3) 38.9(25.6–41.3) 39.0(19.0–41.7) 1.000 0.965 1.000 Modeofdelivery,n(%)

Vaginaldelivery 238(67.2) 69(71.1) 180(67.4) 0.539 1.000 0.526 Primarycesareandelivery 76(21.5) 18(18.6) 55(20.6) 0.575 0.843 0.768 Secondarycesareandelivery 41(11.6) 10(10.3) 33(12.4) 0.602 0.904 0.714 Instrumentaldelivery 53(15.0) 11(11.3) 34(12.7) 0.415 0.484 0.857 Indicationforcesareansection,n(%)

Prolongedfirststageoflabor 28(24.1) 5(17.9) 16(18.2) 0.619 0.390 1.000

Elective 49(42.2) 12(42.9) 35(39.8) 1.000 0.775 0.827

Maternalindication 13(11.2) 0(0.0) 15(17.0) 0.073 0.304 0.020* Fetalindication 26(22.4) 11(39.3) 22(25.0) 0.059 0.740 0.156 PIH:pregnancyinducedhypertension,PE:pre-eclampsia,GA:gestationalage,*:statisticallysignificant.

forrespiratory support,norwas therea differencein mortality (Table3).

Of the newly included group, 76 women with an initially negativeOGTTaccordingtoWHO-1999underwentasecondOGTT, as recommended for symptomatic women and women with a history of GDM [7]. Of these women, 30 had a positive OGTT accordingtotheWHO-1999criteriaandweretreatedforGDM.The secondOGTTwasdoneatamedianofsevenweekslaterthanthe firstOGTTandarelativelylargeproportionofthesewomen(37%) deliveredaLGAneonate.

Discussion

This retrospective cohort study shows the impact on the prevalenceandpregnancyoutcomesofGDMwhenshiftingfrom theWHO-1999totheWHO-2013criteria.Implementingthenew criteriaresultsinamajorincreaseinGDMprevalence,whichisin accordance to previous reports [11–14]. The newly included womenweremoreoverweighedand deliveredneonateswitha higherbirthweight.Inaddition,theproportionofLGAneonates tendedtobehigherinthenewlyincludedgroup.Previousstudies alsohaveshownthatwomendiagnosedwiththerevisedcriteria aremorelikelytobeoverweighed[14,16].

Inagreementwithpreviousobservations(15)ourfindingshows thattheaddedvalueofthefastingglucoseoftheWHO-1999criteria todiagnoseGDMisdisappointinglylowasonly2%ofourpatients withGDMhadafastingplasmaglucoselevelabovethethreshold of7.0mmol/L.Thisfindingisastrongargumentforloweringthe fasting glucose threshold as recommended by the WHO-2013 criteriaandresultsinamarkedreductioninthenumberofOGTTsto beperformed,whichnotonlyisbeneficialforthepatientbutalso savescosts.Indeedwithapplicationofthenewdiagnosticcriteriaan OGTTcouldhavebeenavoidedinalmost80%ofourpatients[15]. WomenexcludedbytheWHO-2013criteriahadlowerHbA1clevels than womenintheWHO-1999group,indirectlysupportingtheview thatexclusionofthesewomenwasappropriate.

Thereasonforacesareansectionwaslessoftenbecauseofa maternalindicationintheWHO-2013excludedgroup.Thismay suggestthatmaternalcomorbiditiesarelessoftenprevalentinthis group,whichisreasonablebecauseofthelowerBMIinthisgroup ofexcludedwomen.

Therateofneonatalhypoglycemiawashardlycomparablesince themajorityof thebabiesdelivered intheWHO-2013included groupdidnothaveroutinelyglucosemonitoring.

Thirty-nine women with an initially undisturbed OGTT accordingtoWHO-1999criteriaweretreatedforGDM(Table2). In 30 of these women, treatment was started because of a disturbed OGTT at a second occasion. The indication for the treatment intheotherninewomenwasa highrandomglucose level.Ontheotherhand,ninewomen,whilehavingadisturbed OGTTaccordingtoWHO-1999criteria,werenottreatedforGDM because they were diagnosed after 37 weeks gestation and thereforedeliverywaschoseninsteadofstartingtreatment.

Neonates deliveredby womenwitha delayeddiagnosis and henceadelayintreatmentweremoreoftenlargeforgestational age.Thesewomenweretreatedforashorteramountoftime.One maywonderiftheproportionofLGAandmacrosomiawouldhave beenlowerifnodelayindiagnosishadoccurred,sinceappropriate managementofGDMisassociatedwithalowerbirthweight[6]. Indeed,Koningetal.,havereportedthattreatingwomenequally forGDMbasedeitheronWHO-2013orWHO-1999criteriaresults inasimilarproportionofLGAneonates[17].Sincepatientswith GDMaccordingtotheWHO-2013criteriamakeup22%ofallLGA pregnancies,thismightbeanadequateendpointfordefiningOGTT thresholdvalues[12].

IntheWHO-1999group2.5%ofpatientsandintheWHO-2013 included group 85.4 % of patients were not treated for GDM. Despitethislargedifferenceintreatment,almostnodifferencein maternalorfetal/neonataloutcomesbetweenthesetwo groups was observed. This absent difference in outcomes is likely explainedbythefactthatwiththeOGGTscreeningthemajority of patients has a mild form of GDM as also reflected by the relativelylowHbA1cvalue.

Limitations

Notalldataofallwomencouldbecollectedfromthepatients’ records,relatedtotheretrospectivedesignofthestudy. Further-more,theOGTT’swerecarriedoutinwomenwithoneormorerisk factors for GDM. Theprevalence of GDM found in ourstudy is thereforenotareflectionofthatinthegeneralobstetricpopulation. Finally, women of the WHO-2013 included group were not diagnosedwithGDMandthemajorityofthereforenottreatedfor this condition, thereby limiting the comparison of outcomes betweenthisgroupandtheWHO-1999group.Ofnote,maternal andfetal/neonataloutcomesbetweentheWHO-1999andthe WHO-2013 excluded group were comparable, probably for earlier mentionedreasons.Neonatalglucoselevelshavebeenmeasured Table3 Fetaloutcomes. WHO-1999 WHO-2013 excluded WHO-2013 included Column1 versus2 Column1 versus3 Column2 versus3 N 354 97 267 – – – Birthweight,g 3338(800–4950) 3315(800–4950) 3520(138–5080) 1.000 0.014 0.010 SGA 32(9.0) 10(10.3) 22(8.2) 0.844 0.775 0.676 LGA 48(13.6) 11(11.3) 49(18.4) 0.615 0.118 0.150 Prematurity(<37weeks),n(%) 40(11.3) 8(8.2) 30(11.2) 0.461 1.000 0.447 Shoulderdystocia,n(%) 8(2.3) 1(1.0) 9(3.4) 0.691 0.461 0.301 Hyperbilirubinemiarequiring phototherapy,n(%) 19(5.4) 3(3.1) 24(9.0) 0.437 0.082 0.070 Neonatalhypoglycemia,n(%) 78(22.0) 19(19.6) – 0.677 – -* AdmissiontoNICU,n(%) 61(17.2) 16(16.5) 51(19.1) 0.881 0.598 0.648 Birthdefects,n(%) 39(11.0) 11(11.3) 22(8.2) 1.000 0.278 0.409 Respiratorysupport,n(%) 16(4.5) 7(7.2) 15(5.6) 0.299 0.579 0.620 Mortality,n(%) Intrauterine 1(0.3) 0(0.0) 2(0.7) 1.000 0.580 0.608 Neonatal 5(1.4) 3(3.1) 3(1.1) 0.377 1.000 0.348

SGA:Smallforgestationalage,LGA:Largeforgestationalage,NICU:Neonatalintensivecareunit,*:statisticallysignificant.Neonatalglucoselevelshavebeenmeasuredin48 %ofthecasesintheWHO-2013includedgroup.

in48%ofthecasesintheWHO-2013includedgroupbecauseGDM wasnotdiagnosedortreatedinmostpatientsofthisgroup. Conclusion

Implementingthenewdiagnosticcriterialeadstoa consider-ableincreaseintheprevalenceofGDM,withthenewlyincluded womenbeingmorefrequentlyoverweigheddeliveringbabieswith ahigherbirthweight.Therelativelyhighfastingglucosethreshold ofthe1999-WHOcriteriahasaverylowaddedvaluetodiagnose GDM,favoringtheuseofalowerfastingplasmaglucosethreshold as advocated by the WHO-2013 criteria, thereby reducing the numberofOGTTs.

Prospective, randomized studies are needed to determine whether the newly included women equally benefit from treatment and whether women that will be excluded by the newcriteriacouldbesafelyleftuntreated.

DeclarationofCompetingInterest Theauthorshavenoconflictofinterest. References

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