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RESEARCHARTICLEOpenAccessCardiovasculardiseaseriskprofilesininflammatoryjointdiseaseentitiesGrundeWibetoe1,10*,EirikIkdahl1,SilviaRollefstad1,IngeC.
Olsen2,KjetilBergsmark2,ToreK.
Kvien2,AnneSalberg3,DagMagnarSoldal4,GunnsteinBakland5,seLexberg6,Bjrg-TildeFevang7,HansChristianGulseth8,GlennHaugeberg4,9andAnneGreteSemb1AbstractBackground:Patientswithinflammatoryjointdiseases(IJD)haveincreasedriskofcardiovasculardisease(CVD).
OuraimwastocompareCVDriskprofilesinpatientswithIJD,includingrheumatoidarthritis(RA),axialspondyloarthritis(axSpA)andpsoriaticarthritis(PsA)andevaluatethefutureriskofCVD.
Methods:TheprevalenceandnumbersofmajorCVDriskfactors(CVD-RFs)(hypertension,elevatedcholesterol,obesity,smoking,anddiabetesmellitus)wereestimatedinpatientswithRA,axSpAandPsA.
RelativeandabsoluteriskofCVDaccordingtoSystematicCoronaryRiskEvaluation(SCORE)wascalculated.
Results:Intotal,3791patientswereincluded.
CVDwaspresentin274patients(7.
2%).
OfthosewithoutestablishedCVD;hypertensionandelevatedcholesterolwerethemostfrequentCVD-RFs,occurringin49.
8%and32.
8%ofpatients.
PatientswithPsAweremoreoftenhypertensiveandobese.
Overall,73.
6%ofpatientshadaminimumofoneCVD-RF,whichincreasedfrom53.
2%amongpatientsaged30to140/90mmHg),healthpersonnelareinstructedtoconductthreeconsecutivemeasurementsandrecordtheaverageofthetwolastmeasurements.
Fur-thermore,riskoffatalCVDeventsinthecoming10yearsisestimatedbytheSCOREalgorithm.
Intheseanalyses,weincludedpatientswithRA,axialspondyloarthritis(axSpA)(e.
g.
nonradiographicaxSpAandAS)orPsA,whoatminimumhadrecordingsofBPand/orlipidlevels.
Currently,NOCARdatahavebeenrecordedinsevenclinicslocatedacrossNorway(Oslo(DiakonhjemmetHospital),Lillehammer(HospitalforRheumaticDiseases),Kristiansand(HospitalofSouthernNorway),Skien(Beta-nienHospital),Bergen(HaukelandUniversityHospital),Drammen(VestreVikenHospital)andTroms(UniversityHospitalofNortherNorway)).
CVD-relatedvariableswereincluded,inadditiontodemographic,socioeconomic,andrheumatic-disease-relatedvariablesandantirheumaticmedication(Table1).
Inthecurrentproject,axSpAincludedbothradiographic(AS)andnonradiographicaxSpA.
EstablishedatheroscleroticCVDwasdefinedbyself-reportedMI,percutaneouscoronaryintervention(PCI)and/orcoronaryarterybypassgraft(CABG)surgery,peripheralarterialdisease(PAD),strokeand/ortransientischemicattack(TIA).
IntheabsenceofCVDand/ornoreportedCVD,patientswereclassifiedasbeingwithoutestablishedCVD.
TheprevalenceofconventionalCVD-RFswasassessedinallindividualswithoutdocumentedCVD.
HTwasdefinedaspresenceofself-reportedHT,currentuseofantihypertensivetreatment(AntiHT)orsystolicBP(sBP)/diastolicBP(dBP)≥140/90mmHg[16].
InlinewiththeacknowledgedNationalHealthandNutritionExaminationSurvey(NHANES),elevatedTCwasdefinedasTC≥6.
2mmol/l(240mg/dl)[17]and/oruseoflipid-loweringtherapy(LLT)[8].
Bodymassindex(BMI)≥30kg/m2wasclassifiedasobesity.
Currentsmokinganddiabetesmellitusweredefinedbyself-reportedpresenceoftheseCVD-RFs.
TheCVDrisk(10-yearriskofafatalCVDevent)wasestimatedaccordingtotheelectronicupdatedSCOREalgorithmforcountrieswithlowriskofCVD,availableonlineatHeartScore(www.
HeartScore.
org),whichin-cludesHDL-c.
PatientswereeligibleforCVDriskas-sessmentbySCOREintheabsenceofdiabetesmellitus,establishedCVDanduseofLLTand/orAntiHT.
Inthecaseofincompletereportingofdiabetesmellitusand/orstatusofLLT/AntiHTuse,patientswereanalyzedasnon-diabeticand/ornon-usersofLLT/AntiHTtreat-ment,respectively.
InRA,theSCOREcalculationswereperformedwithandwithoutapplyingtheEULAR1.
5multiplicationfactor[5].
RelativeriskwascalculatedinallpatientseligibleforassessmentofCVDriskusingtheSCOREalgorithm,byfindingthenearestsBPvaluefrom120to180mmHgwith20mmHgincrementsandthenearestTCintegerfrom4to8mmol/lforsmokersandWibetoeetal.
ArthritisResearch&Therapy(2017)19:153Page2of10Table1PatientcharacteristicsVariablesIJD(n=3517)RA(n=1961)axSpA(n=835)PsA(n=721)pFemale,n(%)2046(58.
2)1389(70.
8)293(35.
1)364(50.
5)5.
1),n(%)-63(3.
8)-20(3.
6)-ASDAS(CRP),median(IQR)--1.
59(1.
04,2.
53)1.
54(0.
99,2.
31)-Inactive(3.
5),n(%)--40(6.
4)28(6.
2)-BASDAI,median(IQR)--1.
29(0.
25,4.
13)1.
09(0.
26,3.
73)-Antirheumaticmedication,currentuseGlucocorticoids,n(%)641(18.
2)575(29.
3)17(2.
0)49(6.
8)140/90.
ElevatedTCwasdefinedasTC>6.
2and/oruseoflipid-loweringtherapy.
Bodymassindex>30kg/m2wasclassifiedasobesity,whereascurrentsmokinganddiabetesmellituswasdefinedbytheself-reportedpresenceoftheseCVDriskfactorsWibetoeetal.
ArthritisResearch&Therapy(2017)19:153Page5of10InthosepatientsinwhomtheabsoluteriskofCVDwascalculated,therelativeriskoffutureCVDwasalsoestimatedshowingthat35.
2%ofpatientswithIJDhadarelativeriskof2(RR=2),while24.
7%hadariskoffutureCVDthreetimesorhigher(RR=3–12)comparedtopatientswithoptimalCVD-RFlevels(seeFig.
4.
andAdditionalfile1:TableS5).
DiscussionUsingalargecohortofpatientsfromanationwidepro-ject,wefoundahighprevalenceofCVD-RFsacrossallthemajorIJDentities.
CVD-RFswerealsoprevalentamongtheyoungerpatientswithIJDandtherewerealsosomeinterestingdifferencesacrossIJDentities.
Des-pitethehighfrequencyofCVD-RFs,estimatedCVDriskaccordingtoSCOREwaslow/moderateandhigh,andindividualsatveryhigh-riskwereonlyidentifiedamongtheoldestagestratum.
SeveralstudieshavereportedthefrequencyofcertainCVD-RFsandcomparedpatientswithoneparticularIJDtonon-IJDcontrols,butlargelythereisalackofstudiescomparingtheCVDriskprofileacrossIJDentities.
TodateonlyonestudyhascomparedtheprevalenceofthesefivemajorCVD-RFsacrossallthreeIJDentities[13],whileanotherstudypublishedadecennialagocomparedtheprevalenceofthreeCVD-RFs(HT,lipidabnormalitiesanddiabetesmellitus)amongpatientswithRA,ASandPsA[14].
Moreover,thesestudiesdidnotstratifypatientswithIJDbyin-creasingage,whichisanimportantdeterminantofCVD-RFprevalence.
Withtheexceptionofonestudy,reportscomparingestimatedCVDriskbySCOREacrossIJDentitiesarealsolacking.
Inthisstudy,patientswithdocumentedCVDwereexcludedfromanalysisusingSCORE,butitwasnotstatedwhetherpatientswithFig.
3RiskofcardiovasculardiseaseaccordingtotheSystematicCoronaryRiskEvaluation(SCORE)algorithmforcountrieswithlowriskofCVD,inpatientswithvariousinflammatoryjointdiseases,stratifiedbyage(30to<45years,45to<60yearsand60to≤80years).
RArheumatoidarthritis,mRAmodifiedSCOREbyapplicationoftheEuropeanLeagueAgainstRheumatism1.
5multiplicationfactorinpatientswithRA,axSpAaxialspondyloarthritis,PsApsoriaticarthritis.
Lowtomoderaterisk(SCORE<5%);highrisk(SCORE5<10%);veryhighrisk(SCORE≥10%)Fig.
4Relativeriskandpercentageofpatientswithrheumatoidarthritis,axialspondyloarthritisandpsoriaticarthritiswhohadarelativeriskcorrespondingtonoincreasedrisk(RR=1),atwo-foldrisk(RR=2)orariskthreetimesorhigher(RR=3–12)comparedtoindividualswithoutcardio-vascularriskfactors(nosmoking,systolicbloodpressure≤120mmHgortotalcholesterol≤4mmol/L)Wibetoeetal.
ArthritisResearch&Therapy(2017)19:153Page6of10diabetesmellitusand/orcurrentuseofLLT/AntiHTwereexcluded[13].
PreviousstudiesindicatethatHTismorefrequentinPsA[13,19,20]andAS[13]thaninnon-IJDcontrols.
WhilestudiescomparingHTfrequencyinpatientswithRAversusnon-RAcontrolsreportinconsistenttrends[13,21,22],twostudiescomparingIJDentitiesdescribesimilarHTfrequencyinRA,ASandPsApatients[13,14].
WeobservedthatHTwasthemostprevalentCVD-RF,occurringinabouthalfofallpatientswithIJDwithoutestablishedCVD.
Thisisparticularlyinterestingaspa-tientswithRAappeartobelesslikelytoreceiveadiagno-sisofHTthanindividualswithoutRA[23],anditappearsthatHThasthehighestimpactonCVDmorbidityamongtheconventionalCVD-RFs[9].
Furthermore,ourstudyshowedthatpatientswithPsAweresignificantlymorehypertensivethantheircounterpartswithRAandaxSpAwithinsimilaragestrata.
Twostudiesreportthatthefrequencyofhyperlipid-emiaandhypercholesterolemiadiagnoses,respectively,wascomparableacrossIJDentities[13,14].
Likewise,wedidnotobserveanysignificantdifferencesacrossIJDen-titiesintheprevalenceofelevatedTClevels.
However,asignificantageeffectwaspresent.
ThehighfrequencyofelevatedTClevelsisofparticularinterestaspreviousstudiesindicatethatpatientswithRAarerarelyscreenedforlipidabnormalities[24],andthatpatientswithRA[6,25],andwithaxSpAorPsA[6],areundertreatedintermsoflipid-associatedCVDrisk.
InadditiontobeinganimportantCVD-RF,obesityisariskfactorfordevelopingIJD,especiallyPsA[26].
InlinewithfindingsinSpanishpatientswithIJD[13],wealsoobservedthatobesitywasmorefrequentinPsAcomparedtotheotherIJDentitieswithinthetwoyoun-gestagestrata.
ThesefindingsareinlinewithobesitybeingaparticularlystrongriskfactorforPsA.
However,theprevalenceofobesityamongpatientswithIJD(17.
4%)didnotdifferfromestimationsinthegeneralpopulation(17–20%)bytheNorwegianInstituteofPub-licHealth[27].
Theclinicalrelevanceoftheattentionfo-cusedonobesityisevident,sincemanagingobesitymaynotonlyimproveCVDriskbutalsorheumaticdiseaseactivityandresponsetoantirheumatictreatment[28].
SmokingisanestablishedriskfactorfordevelopingRA[29],PsA[30]andAS[31]andpossiblyinducesautoimmunitybytriggeringcitrullinationofpeptides[32].
AlthoughsmokingwasnotasfrequentinthisstudyaspreviouslyreportedinSpanishpatientswithIJDandDanishpatientswithRA[13,33],weidentifiedapreva-lenceof20.
1%ofdailysmokersamongourpatientswithIJD,whichishigherthanthe13%ofreportedsmokersamongthegeneralNorwegianpopulation[34].
Fortu-nately,dailysmokingappearslessfrequentinyoungerpatientswithIJD.
TheprevalenceofdiabetesmellitushasbeenreportedtobesignificantlyhigherinpatientswithPsAcomparedtothosewithRA[35].
However,wefoundnostatisticallysignificantdifferencesinthefrequencyofdiabetesmelli-tusacrossIJDentitiesexceptaborderlinesignificantlyhigherfrequencyofdiabetesmellitusamongyoungerpatientswithRA.
Furthermore,theoverallprevalenceofdiabetesmellitusamongourpatientswasmuchlowerthaninthepatientsstudiedbyLabitiganetal.
[35].
AlthoughtheprevalenceofdiabetesmellitusamongNorwegianpatientswithIJD(4.
8–6.
0%)wasclosetothatestimatedintheNorwegiangeneralpopulation(4.
3%)[27],thereareindicationsthatdiabetesmellitusisunder-reportedinIJD(e.
g.
inRA)[36].
Moreover,weshowedthatmodifiableCVD-RFswerecommonacrossallIJDentitiesandevenamongpatientsasyoungas30to<45years.
AlthoughCVD-RFpreva-lenceandCVD-RFquantitywerehighlyage-dependent,therewerealsosomesignificantdifferencesbetweenIJDentities.
PatientswithPsAappearedtohavehighernum-bersofCVD-RFsduetofrequentHTand/orobesity.
ThesefindingsareinlinewithobesitybeingaparticularlystrongriskfactorfordevelopmentofPsA[26],andfur-thermore,theassociationbetweenobesityandHT[37].
DespiteahighfrequencyofCVD-RFsinpatientswithIJD,wefoundthatoverallthepatientswithIJDincludedintheanalysishadalowestimatedCVDriskaccordingtoSCORE.
AhighorveryhighCVDriskaccordingtoSCOREwasalmostexclusivelyfoundintheoldestpa-tientswithIJD.
Interestingly,accordingtorelativeriskestimations,therewasahighfrequencyofpatientswithRA,axSpAorPsAwhohadtwofoldorevenhigherriskcomparedtoindividualswithnoCVD-RFs.
Thisillus-tratesthatpatientswithIJDhaveahighrelativeriskofCVDdespitealowabsoluterisk.
PreviousstudiesindicatethattheSCOREalgorithmgenerallyunderestimatesCVDriskinpatientswithRA[11],andagreatnumberofpatientswithRAwithmoderateCVDriskaccordingtoSCOREhavecarotidatherosclerosisonultrasound[38].
InthelatestESCguidelines,atheroscleroticplaque(s)identifiedbycarotidultrasoundareconsideredanequivalentrisktoadiag-nosisofCVD[4].
ApplicationoftheEULAR1.
5multi-plicationfactorinpatientswithRAdidnotresultinasignificantclinicalreclassificationintoahigherCVDriskcategoryexceptforafewoftheoldestpatients(seeFig.
3andAdditionalfile1:TableS4).
Toourknowledge,onlyonepreviousstudyhasre-portedontheprevalenceofthesefiveCVD-RFsacrossIJDentities.
However,thisisthefirstprojectalsoreport-ingonthedistributionofCVD-RFsinrelationtoagestrata.
Furthermore,incontrasttoapreviouspublication[13],weexplicitlyexcludedpatientswithdiabetesmelli-tusand/oruseofLLTandAntiHT,whenestimatingWibetoeetal.
ArthritisResearch&Therapy(2017)19:153Page7of10CVDriskaccordingtotheSCOREalgorithm.
Oneofthestrengthsofourstudyisthatrelativelylargenum-bersofpatientswereincludedinthisnationwideproject,whichsupportsthegeneralizabilityofourfindings.
OurinvestigationofCVD-RFprevalencehashighclinicalrelevanceastheCVD-RFsincludedintheanalysisac-countforhalfofallCVDmorbidityandmortality[8,9].
Furthermore,wehaveclearlydefinedtheCVD-RFsin-vestigated.
Lasty,sinceageisstronglyassociatedwithCVDriskandCVD-RFprevalence,wehaveestimatedtheirdistributionindifferentagestrata.
Severalstudylimitationsshouldbeconsideredwheninterpretingtheseresults.
First,selectionbiasisindi-catedbythehighrateofuseofbDMARDs(especiallyinaxSpA)andtheinclusionrateinNOCARof41%amongalleligiblepatients[6].
PatientsincludedinNOCARap-peartohavehadlowerdiseaseactivityatthetimeofin-clusionand,overall,olderagecomparedtoeligiblebutnon-includedpatients[6].
SincehighdiseaseactivityisassociatedwithincreasedriskofCVD[39],ourresultsmaythusunderestimatetheactualCVDriskinpatientswithIJDwithhighdiseaseactivity.
Second,missingandincompletedataareanotherlimitation.
Unfortunately,duetopoorreporting,nonsteroidalanti-inflammatorydrug(NSAID)usewasexcludedfromtheanalysis.
TherewasalsoincompletereportingonLLTuse(seeAdditionalfile1:TableS6).
SincepatientswithincompletereportingonatheroscleroticCVDcomorbidities(MI,PCI,CABG,strokeand/orTIA),wereclassifiedaspatientswithoutCVD,theprevalenceofestablishedCVDmayhavebeenunderestimated.
Althoughself-reportedriskfactorsmaybepronetosystematicreporterrors,self-reportedtobaccousehaspreviouslybeenshowntobeavalidmarkerforto-baccoexposure[40],andself-reportedinformationonsta-tinsandantihypertensivemedicationshasbeenshowntohavehighagreementwithpharmacyrecords[41].
Further-more,anyrecordeddataaresubjecttoerrorsofcodingormisclassification.
However,wedonotbelievethatanybiaswoulddisproportionatelyaffectoneIJDentitymorethantheothers.
Duetotheabsenceofacontrolgroup,wecouldnotcomparetheCVDriskprofileinindividualswithandwithoutIJD.
Last,aswereportfindingsfromanationwidecohortfromacountrywithlowriskofCVDconsistingofapredominantlyCaucasianpopulation,theexternalvalidityoutsideNorway/Nordiccountriesissomewhatuncertain.
ConclusionsInconclusionwehaveshownforthefirsttimethatthefrequencyofconventionalCVD-RFsisjustashighinpa-tientswithaxSpAandPsAasinRA.
PatientswithPsAevenappeartohavemorefrequenthypertensionandobesity,whichisnotassessedbytheSCORECVDriskalgorithm.
DespitemostpatientswithIJDhavingalow/moderateabsoluteriskofCVD,therelativeriskwasfre-quentlyincreased.
OurfindingsunderscoretheneedforCVDriskassessmentinallpatientswithIJD.
AdditionalfileAdditionalfile1:TableS1Sensitivityanalysesofprevalenceofcardiovasculardiseaseriskfactorsacrossagestratainpatientswithrheumatoidarthritis,axialspondylitisandpsoriaticarthritis.
TableS2Quantityofconventionalcardiovascularriskfactors.
TableS3Tenyearriskoffatalcardiovasculardiseaseevents.
TableS4Cardiovascularriskcategories.
TableS5Relativeriskinpatientswithinflammatoryjointdiseases.
TableS6Dataavailabilityforcardiovascularriskfactors.
TableS7Patientcharacteristicsandcardiovascularriskfactorsaccordingtorheumaticdiseaseactivity.
TableS8Characteristicsofrheumatoidarthritispatientsaccordingtorheumatoidfactorandanti-citrullinatedproteinantibodypositivity.
TableS9Patientcharacteristicsandcardiovascularriskfactorsaccordingtocurrentuseofbiologicagents.
(DOCX58kb)AbbreviationsACPA:Anti-citrullinatedproteinantibody;ANOVA:Analysisofvariance;AntiHT:Antihypertensivetherapy;axSpA:Axialspondyloarthritis;BMI:Bodymassindex;BP:Bloodpressure;CABG:Coronaryarterybypassgraft;CVD:Cardiovasculardisease;CVD-RF:Cardiovasculardiseaseriskfactor;dBP:Diastolicbloodpressure;ESC:EuropeanSocietyofCardiology;EULAR:EuropeanLeagueAgainstRheumatism;HDL-c:Highdensitylipoprotein-cholesterol;HT:Hypertension;IJD:Inflammatoryjointdiseases;LDL-c:Lowdensitylipoprotein-cholesterol;LLT:Lipid-loweringtherapy;MI:Myocardialinfarction;NHANES:NationalHealthandNutritionExaminationSurvey;NOCAR:NorwegianCollaborationonAtheroscleroticdiseaseinpatientswithRheumaticjointdiseases;PAD:Peripheralarterydisease;PCI:Percutaneouscoronaryintervention;PsA:Psoriaticarthritis;RA:Rheumatoidarthritis;RF:Rheumatoidfactor;RR:Relativerisk;sBP:Systolicbloodpressure;SCORE:Systematiccoronaryriskevaluation;sDMARDs:Syntheticdisease-modifyingantirheumaticdrugs;TC:Totalcholesterol;TG:Triglycerides;TIA:TransientischemicattackAcknowledgementsWearethankfultoallstudynurses,medicaldoctorsandhealthpersonnelforparticipatinginandfacilitatingtheNOCARproject.
FundingTheSouthEasternNorwegianRegionalHealthAuthorityprovidedfundingfortwoPhDstudentsintheNOCARproject.
InadditionfundingwasprovidedbyGretheHarbitzlegacyandOlavRaagholtandGerdMeidelRaagholtsfoundation.
Fundingsourceshadnoroleinthedesignofthestudy,collection,analysisorinterpretationofdataorinwritingofthemanuscript.
AvailabilityofdataandmaterialsThedatasetsusedand/oranalyzedduringthecurrentstudyareavailablefromthecorrespondingauthoruponreasonablerequestAuthors'contributionsGWparticipatedinthestudydesign,obtaineddata,conductedstatisticalanalysisanddraftedandwrotethemanuscript.
ICOparticipatedinstatisticalanalysisandrevisedthemanuscript.
EI,SRandAGSparticipatedinthestudydesign,obtaineddata,analyzedthedataandrevisedthemanuscript.
KB,TK,AS,DMS,GB,L,BTF,HCGandGHparticipatedinthestudydesign,obtaineddataandrevisedthemanuscript.
Allauthorsreadandapprovedthefinalmanuscript.
CompetinginterestsTheauthorsdeclarethattheyhavenocompetinginterests.
ConsentforpublicationNotapplicable.
Wibetoeetal.
ArthritisResearch&Therapy(2017)19:153Page8of10EthicsapprovalandconsenttoparticipateBeingaqualityassuranceproject,informedconsentandethicsboardapprovalwasnotrequired.
However,theprojecthasbeenapprovedbyDataProtectionOfficers(reference2014/11741).
Publisher'sNoteSpringerNatureremainsneutralwithregardtojurisdictionalclaimsinpublishedmapsandinstitutionalaffiliations.
Authordetails1PreventiveCardio-RheumaClinic,DepartmentofRheumatology,DiakonhjemmetHospital,POBox23,Vinderen,N-0319,Oslo,Norway.
2DepartmentofRheumatology,DiakonhjemmetHospital,Oslo,Norway.
3LillehammerHospitalforRheumaticDiseases,Lillehammer,Norway.
4DepartmentofRheumatology,HospitalofSouthernNorway,Kristiansand,Norway.
5DepartmentofRheumatology,UniversityHospitalofNorthernNorway,Troms,Norway.
6DepartmentofRheumatology,VestreVikenHospital,Drammen,Norway.
7DepartmentofRheumatology,HaukelandUniversityHospital,Bergen,Norway.
8DepartmentofRheumatology,BetanienHospital,Skien,Norway.
9DepartmentofRheumatology,MartinaHansensHospital,Brum,Norway.
10FacultyofMedicine,UniversityofOslo,Oslo,Norway.
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