Rev. Bras. Reumatol. vol.55 número1

REVISTA

BRASILEIRA

DE

REUMATOLOGIA

www . r e u m a t o l o g i a . c o m . b r

Original

article

Evaluation

of

performance

of

BASDAI

(Bath

Ankylosing

Spondylitis

Disease

Activity

Index)

in

a

Brazilian

cohort

of

1492

patients

with

spondyloarthritis:

data

from

the

Brazilian

Registry

of

Spondyloarthritides

(RBE)

Izaias

Pereira

da

Costa

,

Adriana

B.

Bortoluzzo

,

Célio

R.

Gonc¸alves

,

José

Antonio

Braga

da

Silva

_,

_Antonio

_Carlos

_Ximenes

_,

_Manoel

_B.

_Bértolo

_,

Sandra

L.E.

Ribeiro

_,

_Mauro

_Keiserman

_,

_Rita

_Menin

_,

_Thelma

_L.

_Skare

_,

Sueli

Carneiro

_,

_Valderílio

_F.

_Azevedo

_,

_Walber

_P.

_Vieira

_,

_Elisa

_N.

_Albuquerque

_,

Washington

A.

Bianchi

_,

_Rubens

_Bonfiglioli

_,

_Cristiano

_Campanholo

_,

Hellen

M.S.

Carvalho

_,

_Angela

_L.B.

_Pinto

_Duarte

_,

_Charles

_L.

_Kohem

_,

_Nocy

_H.

_Leite

_,

Sonia

A.L.

Lima

_,

_Eduardo

_S.

_Meirelles

_,

_Ivânio

_A.

_Pereira

_,

_Marcelo

_M.

_Pinheiro

_,

Elizandra

Polito

_,

_Gustavo

_G.

_Resende

_,

_Francisco

_Airton

_C.

_Rocha

_,

Mittermayer

B.

Santiago

_,

_Maria

_de

_Fátima

_L.C.

_Sauma

_,

_Valéria

_Valim

_,

Percival

D.

Sampaio-Barros

a_{UniversidadeFederaldoMatoGrossodoSul,CampoGrande,MS,Brazil}

b_{InstitutoInsperdeEducac¸ãoePesquisa,SãoPaulo,SP,Brazil}

c_{RheumatologyDiscipline,UniversidadedeSãoPaulo,SãoPaulo,SP,Brazil}

d_{UniversidadedeBrasília,Brasília,DF,Brazil}

e_{HospitalGeraldeGoiânia,Goiânia,GO,Brazil}

f_{UniversidadedeCampinas,Campinas,SP,Brazil}

g_{UniversidadeFederaldoAmazonas,Manaus,AM,Brazil}

h_{PontifíciaUniversidadeCatólica,PortoAlegre,RS,Brazil}

i_{FaculdadedeMedicinadeSãoJosédoRioPreto,SãoJosédoRioPreto,SP,Brazil}

j_{HospitalEvangélicodeCuritiba,Curitiba,PR,Brazil}

k_{UniversidadeFederaldoRiodeJaneiro,RiodeJaneiro,RJ,Brazil}

l_{UniversidadeFederaldoParaná,Curitiba,PR,Brazil}

m_{HospitalGeraldeFortaleza,Fortaleza,CE,Brazil}

n_{UniversidadeEstadualdoRiodeJaneiro,RiodeJaneiro,RJ,Brazil}

∗ _{Correspondingauthor.}

E-mail:izapec@hotmail.com(I.P.d.Costa). http://dx.doi.org/10.1016/j.rbre.2014.05.005

o_{SantaCasadoRiodeJaneiro,RiodeJaneiro,RJ,Brazil}

p_{PontifíciaUniversidadeCatólica,Campinas,SP,Brazil}

q_{SantaCasadeSãoPaulo,SãoPaulo,SP,Brazil}

r_{HospitaldeBase,Brasília,DF,Brazil}

s_{UniversidadeFederaldePernambuco,Recife,PE,Brazil}

t_{UniversidadeFederaldoRioGrandedoSul,PortoAlegre,RS,Brazil}

u_{FaculdadedeMedicinaSouzaMarques,RiodeJaneiro,RJ,Brazil}

v_{HospitaldoServidorPúblicoEstadual,SãoPaulo,SP,Brazil}

w_{InstituteofOrthopedyandTraumatology,UniversidadedeSãoPaulo,SãoPaulo,SP,Brazil}

x_{UniversidadeFederaldeSantaCatarina,Florianópolis,SC,Brazil}

y_{UniversidadeFederaldeSãoPaulo,SãoPaulo,SP,Brazil}

z_{SantaCasadeBeloHorizonte,BeloHorizonte,MG,Brazil}

aa_{UniversidadeFederaldeMinasGerais,BeloHorizonte,MG,Brazil}

bb_{UniversidadeFederaldoCeará,Fortaleza,CE,Brazil}

cc_{EscoladeMedicinaeSaúdePública,Salvador,BA,Brazil}

dd_{UniversidadeFederaldoPará,Belém,PA,Brazil}

ee_{UniversidadeFederaldoEspíritoSanto,Vitória,ES,Brazil}

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Articlehistory:

Received13February2013 Accepted19May2014

Availableonline20December2014

Keywords:

Spondyloarthritis Diseaseactivity BASDAI Epidemiology

a

b

s

t

r

a

c

t

Objective:ToanalyzetheresultsoftheapplicationoftheBathAnkylosingSpondylitis

Dis-easeActivityIndex(BASDAI)inalargeseriesofBrazilianpatientswiththediagnosisofSpA andestablishitscorrelationswithspecificvariablesintothegroup.

Methods:Acommonprotocolofinvestigationwasprospectivelyappliedto1492Brazilian

patientsclassifiedasSpAaccordingtotheEuropeanSpondyoarthropathiesStudyGroup (ESSG),attendedat29referralcentersofRheumatologyinBrazil.Clinicalanddemographic variables,anddiseaseindices(BASDAI,Basfi,Basri,Mases,ASQol)wereapplied.Thetotal valuesofBASDAIwerecomparedtothepresenceofthedifferentvariables.

Results:ThemeanscoreofBASDAIwas4.20±2.38.ThemeanscoresofBASDAIwerehigher

inpatientswiththecombined(axial+peripheral+entheseal)(4.54±2.38)clinical presen-tation, compared to the pure axial(3.78±2.27) or pure peripheral (4.00±2.38) clinical presentations(P<0.001).BASDAIalsopresentedhigherscoresassociatedwiththefemale gender(P<0.001)andpatientswhodidnotpracticeexercises(P<0.001).Regardingtheaxial component,highervaluesofBASDAIweresignificantlyassociatedwithinflammatorylow back pain(P<0.049),alternatingbuttockpain(P<0.001),cervicalpain(P<0.001)andhip involvement(P<0.001).TherewasalsostatisticalassociationbetweenBASDAIscoresand theperipheralinvolvement,relatedtothelower(P=0.004)andupperlimbs(P=0.025).The presenceofenthesitiswasalsoassociatedtohigherscoresofBASDAI(P=0.040).Positive HLA-B27andthepresenceofcutaneouspsoriasis,inflammatoryboweldisease,uveitisand urethritiswerenotcorrelatedwiththemeanscoresofBASDAI.LowerscoresofBASDAIwere associatedwiththeuseofbiologicagents(P<0.001).

Conclusion: In thisheterogeneous Brazilian seriesof SpA patients, BASDAIwas ableto

demonstrate“diseaseactivity”inpatientswithaxialaswellasperipheraldisease. ©2014ElsevierEditoraLtda.Allrightsreserved.

Avaliac¸ão

do

desempenho

do

BASDAI

(Bath

Ankylosing

Spondylitis

Disease

Activity

Index)

numa

coorte

brasileira

de

1.492

pacientes

com

espondiloartrites:

dados

do

Registro

Brasileiro

de

Espondiloartrites

(RBE)

Palavras-chave:

Espondiloartrites Atividadededoenc¸a

a

b

s

t

r

a

c

t

Objetivo:Avaliarosresultadosdaaplicac¸ãodoÍndicedeAtividadedeDoenc¸adaEspondilite

BASDAI Epidemiologia

Métodos: Umprotocolocomumdeinvestigac¸ãofoiprospectivamenteaplicadoem1.492

pacientesbrasileirosclassificadoscomoEpApeloscritériosdoGrupoEuropeudeEstudodas Espondiloartropatias(ESSG),acompanhadosem29centrosdereferênciaemreumatologia noBrasil.Variáveisclínicas,demográficaseíndicesdedoenc¸aforamcolhidos.Osvalores totaisdoBASDAIforamcomparadoscomapresenc¸adasdiferentesvariáveis.

Resultados: OvalormédiodoBASDAIfoide4,20±2,38.OsescoresmédiosdoBASDAIforam

maiselevadosnospacientescomformaclínicacombinada,comparadoàsformasaxiais eperiféricasisoladas,nospacientesdosexofemininoenossedentários.Comrelac¸ãoao componenteaxial,valoresmaisaltosdoBASDAIestiveramsignificativamenteassociados àlombalgiainflamatória,àdoralternanteemnádegas,àdorcervicaleaoacometimento decoxofemorais.Houveassociac¸ãoestatísticaentreosvaloresdoBASDAIeo comprome-timentoperiférico,relacionadoaonúmerodearticulac¸õesinflamadas,tantodosmembros inferioresquantodosmembrossuperiores,eàsentesites.ApositividadedoHLA-B27ea presenc¸ademanifestac¸õesextra-articularesnãoestiveramcorrelacionadascomosvalores médiosdoBASDAI.ValoresmaisbaixosdoBASDAIestiveramassociadosaousodeagentes biológicos(p<0,001).

Conclusão: NestasérieheterogêneadepacientesbrasileiroscomEpA,oBASDAIconseguiu

demonstrar“atividadededoenc¸a”tantonospacientescomacometimentoaxialquanto naquelescomenvolvimentoperiférico.

©2014ElsevierEditoraLtda.Todososdireitosreservados.

Introduction

Thedenominationspondyloarthritis(SpA)definesa hetero-geneous group of diseases that share genetic and clinical characteristics,aswellasstructuralchangesinimaging stud-ies.ThepositivityofHLA-B27andtheabsenceofrheumatoid factorare common tothis groupofdiseases,and thehigh frequencyofinflammatoryprocessesofthespine,sacroiliac jointsandenthesisisconsideredthemainclinicalcriteriafor thediagnosisofSpA.1_{Otherclinicalmanifestationsoccurin}

varyingdegrees ofinvolvementin thegroup ofSpA; more often, skin, ocular, intestinal and urogenital injuries and, less frequently, pulmonary, cardiac, renal and neurological involvement.1

Thisgroupofdiseasesconsistsofankylosingspondylitis (AS),psoriatic arthritis (PA),reactive arthritis(ReA), arthri-tisassociatedwithinflammatoryboweldiseases(alsoknown asenterophaticarthritis–EA)andundifferentiated spondy-loarthritis(USpA).1

With the advent of new therapeutic modalities for the groupofSpA,theelaborationofmeasuresofdisease activ-itythatcouldbeusedinlong-termfollow-upwasnecessary.2

Currently,toevaluateandmonitorclinicaldiseaseactivityin SpA,theBathAnkylosingSpondylitisDiseaseActivityIndex (BASDAI)hasbeenused.Thisindexisobtainedbysumming thevaluesofavisualanalog scale(VAS) thatevaluatessix items,namely:fatigue,axialpain, peripheralpain, enthesi-tis,durationandintensityofmorningstiffness.3_BASDAIdoes

notuseany markerofinflammatoryactivity inits calcula-tion,sincethesetestswerenotstandardizedatthetimeof itsproposition.3_{BASDAIvaluesareinternationallyused}

(BAS-DAI≥4isdeemedas“highdiseaseactivity”)fortheindication ofbiologicalagentsinthetreatmentofSpA,whentherewas noresponsetoconventionaltreatmentwithnonsteroidal anti-inflammatorydrugsorwithconventionalremissivedrugs.4,5

When the patient reaches BASDAI 50(improvement in the BASDAI scoreof ≥50%)in the first 12 weeksof treatment, thiscanbeconsideredasaverygoodclinicalresponse.6_Due

toitsimportance,BASDAIhasbeentranslatedandvalidated inseverallanguages,includingFrench,7_Swedish,8_German,9

Spanish,10_Turkish,11_Arabic12_{andPortuguese.}13_Recently,the

Ankylosing SpondylitisDisease Activity Score(ASDAS) was created14_{;thisindexassociatesthepresenceofamarkerof}

inflammatory activity,erythrocytesedimentation rate (ESR) or C-reactive protein (CRP); nowadays, ASDAS has its cut-offscorestodifferentiate“moderate”,“high”and“veryhigh” activity.15

ThispaperanalyzestheapplicationofBASDAIina hetero-geneousBraziliancohortof1492patientswithSpA.

Methods

This is a prospective, observational, multicenter study, conductedwith 1492patientsfrom 29 referral centers par-ticipating in the Brazilian Registry of Spondyloarthritides

(Registro Brasileiro de Espondiloartrites – RBE). All patients

fulfilled the criteria of the European Spondyloarthropathy StudyGroup(ESSG).16_{DatawerecollectedfromJune2006to}

December 2009. RBE participates in the RESPONDIA group

(RegistroIberoamericanodeEspondiloartrites),consistingofnine

LatinAmericancountries(Argentina,Brazil,CostaRica,Chile, Ecuador,Mexico,Peru,UruguayandVenezuela)andthetwo countriesoftheIberianpeninsula(SpainandPortugal).

C-reactive protein – CRP), as well as the treatment (nons-teroidanti-inflammatorydrugs–NSAIDs,corticosteroidsand conventionalandbiologicalremissivedrugs).

ForthediagnosisofAS,theNewYorkcriteriawereused17_;

forpsoriaticarthritis,theparticipantshadtomeetthe crite-riaofMollandWright.18 _{Thediagnosis ofreactive arthritis}

wasconsideredifasymmetricoligoarthritisofthelowerlimbs were present,with enthesopathy and/or inflammatorylow backpainarousingafteranentericorurogenitalinfection,19

andspondyloarthritis/arthritisassociatedwithinflammatory boweldisease,ifthepatienthadaninflammatoryaxial dis-order and/or peripheraljoint involvement, associated with confirmedCrohn’sdiseaseorulcerativecolitis.

BASDAI is a tool for evaluation of disease activity that contains six questions.3 _{The responses were marked on a}

horizontallinemeasuring10cm(from0to10cm),wherethe patientevaluateshowhefeelsinrelationtoeachiteminthe lastweek,markingonthescale:ifthepatientisfine(“very well”),he/shemarkszerocm,graduallyincreasinguntil“very poor”,correspondingtoa10-cmmark.Thesixquestions com-prisingBASDAIareasfollows:(1)Howwouldyoudescribethe degreeoffatigueortirednessyouhavehad?;(2)Howwould youdescribetheoveralllevelofneck,backandhippainrelated toyourillness?;(3)Howwouldyoudescribetheoveralllevel ofpainandedema(swelling)inotherjoints,apartfromneck, backandhip?;(4)Howwouldyoudescribetheoveralllevelof discomfortyoufelttothetouchorcompressioninthepainful regionsofyourbody?;(5)Howwouldyoudescribethe inten-sityofmorningstiffnessyouhavehad,fromthetimeyouwake up?;(6)Howlongdoesyourmorningstiffnesstake,fromthe timeyouwakeup?

Statisticalanalysis

Thevariable categories were comparedusing2 _{and Fisher’s}

exacttests, andcontinuousvariables werecomparedusing ANOVA.Avalue ofP<0.05was considered significant;and 0.05>P>0.10wasconsideredasastatisticaltrend.

Results

ThemeanscoreoftotalBASDAIwas4.20±2.38.Amongthe sixitemsthatmakeupthefinalvalueofBASDAI,theitem2 (relatedtoaxialpain;5.05±3.20)hadthehighestmean,and theitem3(relatedtoperipheralcomponent;3.28±3.18)was thatwiththelowestvalue.ThemeanvaluesofBASDAItoall thequestionsthatmakeuptheindexaredescribedinTable1.

Table1–ResultsofBASDAIperitem.

BASDAI Mean Standard

deviation

Total 4.20 2.38

Question1 4.21 2.99

Question2 5.05 3.20

Question3 3.28 3.18

Question4 4.28 3.34

Question5 4.59 3.29

Question6 3.85 3.36

Table2–ResultsofBASDAIaccordingtospecificSpA.

% Mean SD P

PrimaryAS 67.6 4.21 2.36 PsoriaticAS 4.6 4.38 2.32 EnteropathicAS 2.6 4.70 2.41

PsoriaticArthritis 14.2 4.13 2.47 0.305

USpA 6.8 4.35 2.28

ReactiveArthritis 3.4 4.12 2.57 EnteropathicArthritis 0.8 4.37 3.05

Therewasnosignificantdifferencebetweenthemean val-uesofBASDAIandanyspecificdiseasewithintheSpAgroup. ThemeanvaluesofBASDAIforeachdiseasewithinthegroup are shown in Table 2. As to the clinical presentation, the meanvaluesofBASDAIweresignificantlyhigherinenthesitic (4.96±2.22)and combined(axialand peripheral;4.50±2.38) forms,comparedtopureforms,bothaxial(3.78±2.28) and peripheral(3.87±2.23)(Table3).

Withregardtodemographicvariables,BASDAIwas signifi-cantlyhigherinfemales(P<0.001)andinthosepatientswho didnotexerciseregularly(P<0.001).Ethnicity,HLA-B27 and familyhistoryofSpAdidnotinfluencetheresultsofBASDAI (Table4).

Numerous clinical variables influenced BASDAI scores. Inflammatorylowbackpain(P=0.039),buttockpain(P<0.001), neck pain (P<0.001), hip pain (P<0.001), arthritis oflower (P=0.004)andupper(P=0.025)limbs,andenthesitis(P=0.040) weresignificantlyassociatedwithhighermeanvaluesof BAS-DAI.Extra-articularmanifestationssuchasuveitis,psoriasis,

Table3–ResultsofBASDAIaccordingtoclinicalform.

% Mean SD P

Mixed 48.5 4.50 2.38

Axial 34.5 3.78 2.28 <0.001 Peripheral 11.0 3.87 2.23

Enthesitic 6.0 4.96 2.22

Table4–ResultsofBASDAIaccordingtoepidemiological data.

% Mean SD P

Gender

Male 72.3 3.97 2.95 <0.001 Female 27.7 4.84 3.05

Race

White 67.4 4.03 2.38 0.057 Non-white 32.6 4.30 2.40

Exercise

Yes 40.8 3.89 2.35 <0.001

No 59.2 4.42 2.38

Familyhistory

Yes 18.0 4.32 2.49 0.413

No 82.0 4.18 2.36

HLA-B27

Positive 69.0 4.16 2.33 0.391

Table5–ResultsofBASDAIaccordingtoclinicaldata.

% Mean SD P

Inflammatorylowbackpain 0.049

Yes 67.6 4.29 2.31

No 32.4 4.02 2.53

Buttockpain <0.001

Yes 33.1 4.59 2.39

No 66.9 4.01 2.36

Neckpain <0.001

Yes 30.8 4.64 2.32

No 69.2 4.01 2.39

Hippain <0.001

Yes 25.1 4.63 2.35

No 74.9 4.06 2.38

Arthritis,lowerlimb 0.004

Yes 48.9 4.38 2.35

No 51.1 4.03 2.30

Arthritis,upperlimb

Yes 22.1 4.46 2.40 0.025

No 77.9 4.13 2.37

Enthesitis 0.040

Yes 27.1 4.41 2.41

No 72.9 4.13 2.37

Dactylitis 0.423

Yes 9.1 4.04 2.48

No 90.9 4.22 2.37

Uveitis 0.926

Yes 19.1 4.22 2.53

No 80.9 4.20 2.35

Skinpsoriasis 0.849

Yes 17.8 4.23 2.42

No 82.2 4.20 2.38

Inflammatoryboweldisease 0.106

Yes 4.7 4.67 2.46

No 95.3 4.18 2.38

Urethritis

Yes 4.4 4.51 2.57 0.326

No 95.6 4.19 2.37

inflammatoryboweldiseaseandurethritisdidnotinfluence BASDAIscores(Table5).

Withregardtotreatment,onlytheuseofanti-TNF biolog-icalagentswassignificantlyassociatedwithlowerscoresof BASDAI(P<0.001),whiletheuseofNSAIDs,corticosteroids, methotrexateandsulfasalazinedidnotinfluencethevalues ofBASDAI(Table6).

Discussion

ThisstudyaimedtoevaluatetheactivityofSpAusing BAS-DAI as a clinical activity index; this is a tool traditionally usedinpatientswithSpA.TheresultsshowedthatBASDAI coulddemonstrate “diseaseactivity”,bothinpatients with anaxialcomponentasinthosewithperipheralinvolvement, eveninpatients withSpA but withno diagnosis ofAS.In view of the fact that BASDAI evaluate “axial” (question 2) and“peripheral”(questions3and4)components,an impor-tant finding in this study was represented by the highest meanscoresinpatientswhohadaninvolvementdescribedas “combined”(wherethe“axial”and“peripheral”components areobservedinthesamepatient)–acommon characteris-ticofBrazilianpatients.20_{Similarly,anEuropeanmulticenter}

Table6–ResultsofBASDAIaccordingtotreatment.

% Mean SD P

NSAID 0.888

Yes 67.6 4.21 2.35

No 32.4 4.19 2.45

NSAIDon-demand 0.713

Yes 24.9 4.16 2.40

No 75.1 4.22 2.38

Corticosteroid 0.297

Yes 35.3 4.29 2.37

No 64.7 4.16 2.39

Methotrexate 0.866

Yes 51.7 4.21 2.32

No 48.3 4.19 2.45

Sulfasalazine 0.934

Yes 44.7 4.21 2.44

No 55.3 4.19 2.34

Biologicals <0.001

Yes 20.4 3.73 2.47

No 79.6 4.32 2.35

Infliximab <0.001

Yes 15.3 3.58 2.50

No 84.7 4.32 2.35

Etanercept 0.104

Yes 2.8 4.78 2.30

No 97.2 4.19 2.38

Adalimumab

Yes 2.3 3.70 2.06 0.164

No 97.7 4.22 2.39

studyevaluating214patientswithSpAfoundhighervalues ofBASDAIinthoseparticipantswithaperipheralcomponent (4.4±2.3)comparedtopatientswithanisolatedaxial compo-nent(3.1±1.9)(P<0.001).21_{Alsoimportantwasthefactthat}

themeanvaluesofBASDAIweresignificantlyelevated,bothin presenceofaxial(inflammatorylowbackpain,buttockpain, neckpainandhippain)andperipheral(lowerandupperjoints) clinicalvariables,inadditiontoenthesitis.

InthespectrumofSpA,psoriaticarthritisisthatdisease wheretheperipheralcomponentismoststriking.Ourstudy showedthatBASDAIcanalsobeeffectiveintheevaluationof patientswithPA,asshowninrecentstudies,22,23_evenwhen

comparedtoASDAS.24

With the proposition of ASDAS as a valid method of assessingdiseaseactivityincasesofAS,14,15_itwillbe

impor-tanttoapplythistooltopatientswithSpAinthesecondphase ofRBE,tocompareitseffectivenessversusBASDAI.Thereis noestablishedconsensusaboutwhatisthebestmethodfor assessmentofdiseaseactivityinpatientswithAS(ifASDAS isbetterthanBASDAI).Meanwhile,BASDAIhasbeenshown asanefficientindexinthetherapeuticfollow-upofpatients withAS.6,25,26_{ThecombinationofBASDAIwiththefunctional}

index BASFI (Bath Ankylosing Spondylitis Disease Activity Index)27_{madeitpossibletoobtainimportantcharacteristics}

ofpatientsintheBrazilianRegistryofSpondyloarthritides.28

Althoughrepresentingonly27.7%ofthepatients,women had higher mean BASDAI scores, when compared tomen. These results certainly may vary with the population evaluated.29

differenceinBASDAIscoresinrelationtoHLA-B27,family his-toryandextra-articularmanifestationswasfound.

In short, BASDAI showed to be an efficient method of assessingdiseaseactivityinaheterogeneouspopulationof BrazilianpatientswithSpA.

Conflicts

of

interest

Theelectronicversion ofthe Brazilian Registry of Spondy-loarthritidesissupportedbyagrantfromWyeth/PfizerBrazil, whichhasnoinfluenceonthecaptureandanalysisofdata, aswellasinthewritingandpublicationofarticles.Dr. Per-civalSampaio-BarrosreceivedaresearchgrantfromFederico Foundation.

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