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Low-field magnetic resonance imaging study on carpal arthritis in systemic sclerosis - low-grade erosive arthritis of carpal bones is an unexpected and frequent disease manifestation. PDF

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Preview Low-field magnetic resonance imaging study on carpal arthritis in systemic sclerosis - low-grade erosive arthritis of carpal bones is an unexpected and frequent disease manifestation.

Akbayraketal.ArthritisResearch&Therapy2013,15:R2 http://arthritis-research.com/content/15/1/R2 RESEARCH ARTICLE Open Access Low-field magnetic resonance imaging study on carpal arthritis in systemic sclerosis - low-grade erosive arthritis of carpal bones is an unexpected and frequent disease manifestation Elif Akbayrak, Robert Dinser, Ulf Müller-Ladner and Ingo H Tarner* Abstract Introduction: The aim of the present study was to assess the prevalence and characteristics of subclinical arthritis of carpal and metacarpophalangeal joints in patients with systemic sclerosis (SSc). Methods: Low-field (0.2 T) magnetic resonance imaging (MRI) was performed in consecutive patients with SSc attending our center between January 2010 and March 2011. Results were assessed in a standardized manner using the Rheumatoid Arthritis Magnetic Resonance Imaging Score (RAMRIS) and standardized assessments of all hand joints. Patients with arthritis due to overlap syndromes were excluded. Results: Of 38 inpatients and eight outpatients who were screened for inclusion, 30 patients participated in the study and 26 patients could be evaluated. Erosions, bone marrow edema, synovitis, and joint effusions were found in 87%, 37%, 68%, and 58%, respectively, and 24% of patients had additional tenovaginitis. Arthritis affected only a low number of joints per analyzed hand. All bones and joints could be affected, but synovitis and bone marrow edema occurred predominantly in the proximal row of carpal bones, most frequently affecting the lunate bone. The extent of inflammatory changes measured with the RAMRIS correlated significantly with the functional status assessed with the validated German functional score questionnaire Funktionsfragebogen Hannover. Conclusion: Low-grade arthritic changes on low-field MRI are frequent in patients with pure SSc. The features of arthritis in SSc differ from rheumatoid arthritis. The distribution, the MRI pattern and the predilection for the lunate bone raise the hypothesis that arthritis in SSc may be caused not only by immunological inflammation but also by ischemic mechanisms. Introduction Registerstudies [5,6] and retrospective clinical studies In the clinical evaluation of systemic sclerosis (SSc), including a meta-analysis of existing data [7] have attention is predominantly given to changes of the skin, recentlysuggestedthatinflammatoryarthritismay bean Raynaud’sphenomenonanditscomplications,andinter- underestimatedprobleminSSc.Thissuggestioncouldbe nalorganinvolvement.Whilearthritishasbeenobserved of therapeutic importance because disease-modifying inSSc[1],itisfrequentlyconsideredtoindicateanover- antirheumatic drugs available for inflammatory arthritis lap between rheumatoid arthritis (RA) and SSc [2,3], mightalsobeusefultodelayorpreventjointdamageand whereasjointpaininpatientswithsoleSSciscommonly lossoffunctioninSScpatients. regarded as non-inflammatory arthralgia caused by skin We therefore performed a prospective magnetic reso- tightnessandflexioncontractures[4]. nance imaging (MRI)study of the handsinpatientswith SSc, excluding patients with clinical or immunological signs suggesting an overlap with other forms ofarthritis. *Correspondence:[email protected] We aimed to determine the prevalence of MRI signs of DepartmentofInternalMedicineandRheumatology,Justus-Liebig-University arthritisincludingsynovitis,bonemarrowedema,effusions, Giessen,DepartmentofRheumatologyandClinicalImmunology,Kerckhoff- Klinik,Benekestraße2-8,D-61231BadNauheim,Germany ©2013Akbayraketal.;licenseeBioMedCentralLtd.ThisisanopenaccessarticledistributedunderthetermsoftheCreative CommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,and reproductioninanymedium,providedtheoriginalworkisproperlycited. Akbayraketal.ArthritisResearch&Therapy2013,15:R2 Page2of8 http://arthritis-research.com/content/15/1/R2 and erosionsaswellasto characterizethedistribution of Images were assessed systematically using two joint involvement. MRIwas chosen because it is an ima- approaches.InthefirstapproachtheRheumatoidArthri- gingtoolwithhighsensitivityforthedetectionofinflam- tisMagneticResonanceImagingScore(RAMRIS)[16,17] matoryjointchanges,ashasbeendemonstratedverywell developedforRAandhigh-fieldMRIwasappliedbytwo inRA[8]andalsoinSSc[9,10]. independent investigators, and scores were calculated using the average score of both investigators for each Materials and methods item. Owing to the technical lack of fat suppression for Consecutive patients with SSc treated as inpatients or T1-weighted images in low-field MRI, synovitis was outpatientsinourdepartmentbetweenJanuary2010and assessedbycomparingsignalintensitiesofthesynovium March2011were consideredforthisstudy.Patientshad before and after the application of Gadodiamide side by to fulfill the LeRoy criteria for limited cutaneous SSc or side.Thickeningofthesynoviumwithenhancementafter diffuse cutaneous SSc [11]. We excluded patients with applicationofthecontrastagentwasjudgedassynovitis, the clinical picture of an overlap syndrome (such as which was assessed only if contrast agent could be Sharp’s syndrome) or a clinical association with other applied. Erosions were defined to be present if the con- rheumaticdiseasessuchasankylosingspondylitisorRA. tour of the cortical bone was interrupted in at least two We also excluded patients in whom antibodies against anatomicalplanesandifenhancementofthedefectwith U1-ribonucleoproteinsoranti-citrullinatedpeptideanti- Gadodiamidewasdetected.Inserieswithoutapplication bodies(ACPA) hadbeendetected eitherwithinthe pre- of contrast agent, the first criterion was deemed suffi- viousyear or when screened for enrolment. Outpatients cient.Thepresenceofbonemarrowedemawasscoredas had to live within a radius of 50 km to be able to return definite ifa hyperintense signal couldbe detected in the for the study assessments. To address the problem of short-tau inversion recovery sequence image and a subclinicalarthritis,thepresenceorabsenceofjointpain hypointensesignal couldbedetectedintheT1-weighted orswellingwasnotconsideredforinclusion. image. Afterobtainingwritteninformedconsent,thefollowing AstheRAMRISdoesnotjudgeeffusionsandpreselects assessments were performed: tender and swollen hand joints involved in RA, a second descriptive systematic andfingerjointcounts;fullskinstatususingthemodified analysis for the presence of synovitis, bone marrow Rodnan skin score; and functional assessment using the edema,erosions,jointeffusion,andtenovaginitiswasper- German-language questionnaire Funktionsfragebogen formed for the following areas: radiocarpal, ulnocarpal, Hannover(FFbH)withvaluesrangingfrom0to100,the radioulnar,intercarpalandfirstcarpometacarpaljointsas latterreflecting completely normalfunction[12]. Use of wellasmetacarpophalangealjoints1to5.Forbonemar- theFFbHisstandardatour centerandFFbHvaluescan row edema and erosions, bones ofthe carpusand meta- be converted into health assessment questionnaire carpuswereanalyzedseparately(distalulna,distalradius, (HAQ)valuesusingtheformula: scaphoid, lunate, triquetral, pisiform, trapezium, trape- zoid,capitate, hamate,basesofmetacarpal bones1to5, HAQ = 3.16 − (0.028×FFbH). heads of metacarpal bones1to 5,andbasesofproximal phalanges1to5).Flexorandextensortendonswereana- The calculated HAQ is therefore also presented [13]. lyzedfortenovaginitis. Theerythrocytesedimentationrateand,ifnotdocumen- EachMRIfeaturewasclassifiedasabsentorquestion- ted previously, ACPA were measured. Morbidity and able, clearly present, or severe. If the increase in signal SSc-relatedtreatmentswerealsorecorded. intensityafter contrastinjectionwasobviouseveninthe Patientsunderwentlow-fieldMRI(0.2T,EsaoteC-scan; absenceofacomparisonwiththebaselineimage,synovi- Esaote,Cologne,Germany)ofthecarpusandthemetacar- tiswas classified assevere. Severe erosionswere defined pophalangealjointsineither themorepainfulhandor,if asdefectsoccupyingmorethan50%ofthebonysurface. notapplicable,thedominanthand[14,15].Athree-dimen- Effusionswereanalyzedintheshort-tauinversionrecov- sional, gradient-echo T1-weighted sequence, a fat-satu- ery sequence, with a convex contour of the fluid signal ratedshort-tauinversionrecoveryT2-weightedsequence, withinthejointcapsuleconsidereddefinite,andadisten- and a second three-dimensional, gradient-echo T1- tion of the overlying skin contour considered severe. weighted sequence were acquired after application of a Bone marrow edema of more than 50% of the existing gadolinium-based contrast agent (Gadodiamide, Omnis- bone area was considered severe. Examples for typical can™;GEHealthcare,Munich, Germany). Inconsenting findings for each assessment are shown in Figure S1 in patients,theotherhandwasmeasuredafteratimeinterval Additionalfile1. ofatleast1daytoallowforcompletewashoutofthecon- Forstatisticalanalysis, theWilcoxonranktestorFish- trastagent. er’sexacttestwereusedwhereappropriate.Correlations Akbayraketal.ArthritisResearch&Therapy2013,15:R2 Page3of8 http://arthritis-research.com/content/15/1/R2 wereanalyzedusingKendall’stauranktest[18],whichis exhibitanyclinicalpainorswellinginthejointsassessed similartoSpearman’sRhorankcorrelationtest butdoes byMRI.Only21%ofallhandsdidnotshowanysignsof notimplyalinearcorrelationbetweenvalues. current arthritis on MRI (synovitis, effusion, bone mar- The study was approved by the ethics committee of rowedema). the University of Giessen. Whileeffusionsand erosionswerefrequent,theywere rarelysevere(Table3;forreference,seealsoFigureS1in Results Additionalfile1).Strongsynovialenhancementwaspre- Atotalof52inpatientswerescreenedforenrolment.Four sent in 13% of analyzed patients. Severe bone marrow patients were excluded due to overlap with other rheu- edema occurred in 15% of patients, suggesting a strong maticdiseases,andthreepatientswereexcluded because association of this feature of arthritis with SSc. In the theirclinicalconditiondidnotpermitMRImeasurements. majority of patients, arthritis affected only a few joints Sevenpatientswereunabletoparticipateduetoorganiza- withinonehand. tional difficulties. Of the 38 inpatients enrolled in the When analyzing the localization of affected joints and study,27agreedtoundergoMRImeasurementsinoneor bones, synovitis was found more frequently in the inter- bothhands.Eightoutpatientswerealsofoundtobeeligi- carpal joints than in the metacarpophalangeal joints ble,threeofwhomagreedtoparticipate. (Table 3), with severe synovitis occurring in up to 6% of Three patients had to be excluded from the analysis carpal joint areas. While bone marrow edema could after acquisitionofMRImeasurements,becausepositive affect most bones of the carpus and metacarpus, it most results for ACPA became available in two of them and frequently and most severely affected the lunate, with a the diagnosis had to be revised to Sharp’s syndrome in definite edema occurring in 18% of lunate bones and thethirdpatient.ThesignalqualityoftheMRImeasure- severe edema in 11%. The scaphoid and triquetrum mentswasinadequateforinterpretationinonepatient. were also prone to bone marrow edema. The predilec- A total of 26 patients could therefore be analyzed, of tion of the proximal row of carpal bones for bone mar- whom12agreedtomeasurementsinbothhandsandthe row edema was also reflected in the frequency of other14onlytomeasurementsinonehand.Atotalof38 erosions in these bones (Table 3). No synovitis could be hands could thus be examined. Owing to difficulties in found in 27% of joint areas with bone marrow edema. obtaining venous access, contrast agent could not be None of the patients has had previous severe trauma or applied in seven of the 38 MRI examinations. None of fractures of the distal forearm, carpal bones, metacarpal thepatientsfulfilledeither thecurrentAmericancollege bones, or fingers, and only one patient had a history of ofRheumatology/EuropeanLeagueAgainstRheumatism occupational exposure to vibratory tools or machinery ortheformerAmericanCollegeofRheumatologyclassi- (a construction worker who frequently drilled concrete). ficationcriteriaforRA[19,20]. In the latter patient, however, only the lunate and tri- The characteristics of our group of patients and a quetrum of the left hand each showed a small erosion summary of the results, including the RAMRIS and the without bone marrow edema whereas the other carpal functional FFbH and HAQ scores, are shown in Table 1. bones of both hands showed no abnormality. The detailed RAMRI scores for each patient are pre- The RAMRIS validated for RA correlated moderately sented in Table S1 in Additional file 2. with the overall functional joint status assessed by the At the time of MRI examination, 10 patients received FFbH(correlationcoefficient=-0.48,P=0.002;Figure1) immunomodulatory drug treatments: five patients were as well asthe calculated HAQ scores (correlation coeffi- being treated with methotrexate, one each with lefluno- cient=0.48,P=0.002).Asummaryscorecalculatedfrom mide, mycophenolate, and etanercept, respectively, and the secondary systematic assessment correlated strongly twopatientswere beingtreatedwithcyclophosphamide. with the RAMRIS (correlation coefficient = 0.80, P < All patients on prednisolone took ≤ 5 mg/day. Iloprost 0.0001).Clinicaltenderorswollenjointcountresults did (Ilomedin™; Bayer Vital GmbH, Leverkusen, Germany) not match with MRI findings. The arthritis score was wasappliedto46%ofpatientsatthetimeofMRIexami- more severe in patients with more widespread disease nationbecauseofaclinicalworseningoftheirRaynaud’s involvement, reflected by the number of affected organ syndrome. Nineteen patients were onlong-termvasodi- systems(correlationcoefficient=0.43,P<0.01),butthere latingdrugs(calciumchannelblockers,bosentanandsil- wasnoassociationwiththedegreeofskininvolvementas denafil), and three patients had concomitant measured by the modified Rodnan skin score, systemic arteriosclerotic disease (two coronary heart disease, one inflammation as assessed by erythrocyte sedimentation peripheralarterialdisease). rate,diseaseduration,orage.TheRAMRISdidnotdiffer Whenanalyzingallmeasuredhands,everyMRIfeature betweenpatientswithshortdiseaseduration≤3yearsand ofarthritiswasobservedinahighproportionofpatients patients with longer-standing disease (mean ± standard (Table2)even though64% ofallhandsanalyzeddidnot deviation RAMRIS, 6.3 ± 4.3 vs. 6.6 ± 5.0, P = 0.918). Akbayraketal.ArthritisResearch&Therapy2013,15:R2 Page4of8 http://arthritis-research.com/content/15/1/R2 Table 1Patient characteristics Parameter AllSSc(n=26) DiffusecutaneousSSc(n=6) LimitedcutaneousSSc(n=20) Age(years) 56±13(32to75) 50±9(40to66) 46±14(32to75) Sex(%female) 77 67 80 Diseaseduration(years) 7.9±5.3(1to19) 7.7±6.0(3to19) 8.0±5.2(1to18) ModifiedRodnanskinscore 8.3±6.1(2to19) 16.3±3.3(12to19) 5.8±4.3†(2to18) Organandtissueinvolvement Pulmonaryfibrosis 11(42) 6(100) 5(25)** Pulmonaryhypertension 5(19) 3(50) 2(10) Cardiacinvolvement 6(23) 1(17) 5(25) Gastrointestinalinvolvement 2(8) 1(17) 1(5) Activedigitalulcer 7(27) 0(0) 7(30) Historyofdigitalulcer 16(62) 4(83) 12(55) Arterioscleroticdisease 3(12) 0(0) 3(15) ESR(mm/hour) 19±14 28±20 16±11 Antinuclearantibodypositivity 23(89) 5(83) 18(90) Anti-centromereantibody 11(42) 0(0) 11(55)* Anti-Scl70antibody 9(35) 2(33) 7(35) Medication Immunomodulatorydruga 10(38) 2(33) 8(40) Steroids 6(23) 1(17) 5(25) Iloprost 12(46) 3(50) 9(45) Calcium-channelblockers 9(35) 2(33) 7(35) Betablockers 1(4) 0(0) 1(5) Bosentan 7(27) 3(50) 4(20) Sildenafil 3(12) 0(0) 3(15) Low-doseaspirin 5(19) 0(0) 5(25) RAMRIS 6.5±4.7(0to14) 5.4±4.1(1to12) 7.0±5.0(0to14) Radiographsofthehands 21(81) 4(67) 17(85) Signsofarthritis 2(10) 0(0) 2(12) Acroosteolysis 9(43) 2(50) 7(41) Soft-tissuecalcifications 11(52) 1(25) 10(59) FFbH(%functionalcapacity) 68.7±22.8(33to100) 58.2±25.2(39to100) 71.9±21.7(33to100) HealthAssessmentQuestionnaireb 1.24±0.64(0.36to2.25) 1.54±0.7(0.36to2.08) 1.15±0.61(0.36to2.25) Datapresentedasmean±standarddeviation(range)orn(%).OnlytheRheumatoidArthritisMagneticResonanceImagingScore(RAMRIS)fortheclinically dominantlyaffectedhandwasanalyzed.Percentageswererounded.ESR,erythrocytesedimentationrate(Westergren’smethod);FFbH,Funktionsfragebogen Hannover(German-languagestandardizedassessmentquestionnaireonphysicalfunction);SSc,systemicsclerosis.Significantdifferences:*P<0.05and**P<0.01 betweenthegroupswithlimitedanddiffuseskindiseaseasassessedbyFisher’sexacttest;†P<0.01asassessedbytheMann-WhitneyUtest.Allother comparisonswerenonsignificant.aIncludingmethotrexate,leflunomide,mycophenolate,etanercept,andcyclophosphamide.bValuescalculatedfromtheFFbH usingtheformula:HAQ=3.16-(0.028×FFbH)). Table 2Proportion ofhands showing different featuresofarthritis onmagnetic resonance imaging Erosion Bonemarrowedema Synovitis Jointeffusion Tenovaginitis Signsofarthritis Notpresent/indeterminate 13 63 32 42 76 Present 87 37 68 58 24 Severe 3 16 13 0 0 Affectedjointsinaffectedhands 2.2±1.6(1to6) 1.6±1(1to4) 4.1±2.6(1to9) 4.2±2.6(1to10) N/A Datapresentedaspercentageormeannumber±standarddeviation(range).FordefinitionofdefiniteorseverepleaserefertoMaterialsandmethods.N/A,not applicable. Akbayraketal.ArthritisResearch&Therapy2013,15:R2 Page5of8 http://arthritis-research.com/content/15/1/R2 Table 3Distribution ofmagnetic resonance imaging lunatebonesbutnodefinitiveerosionsonX-ray,whereas findings in individual joints and bonesofthe hand low-fieldMRIclearlyshowedbilaterallunateerosions.In Synovitis Jointeffusion all other patients with lunate erosions on MRI, no Definitive Severe Definitive Severe abnormalitiesweredetectedbyX-rayscan.Ofnote,none of the patients with bone marrow edema of the lunate Joint bonehadradiographicabnormalities.Acroosteolysisand Radiocarpal 19 3 8 - extraarticular soft-tissue calcifications were observed in Radioulnar 23 - - - 43% and 52% of the radiographs, respectively (Table 1). Ulnocarpal 48 6 - - The presence and severity of MRI features of arthritis, Intercarpal 52 3 47 - however, were not correlated with the finding of either Carpometacarpaljoint1 6 - 3 - acroosteolysisorcalcifications. Metacarpophalangeal 13 - 11 - joint1 Metacarpophalangeal 6 - 3 - Discussion joint2 This prospective systematic low-field MRI study shows Metacarpophalangeal 23 - - - thatsubclinicalarthritisofthecarpusand metacarpusis joint3 a frequent manifestation in patients with SSc, which is Metacarpophalangeal 16 - 5 - underestimated by clinical examination as well as plain joint4 radiographs. The relevance of this observation isunder- Metacarpophalangeal 16 - 5 - joint5 lined by the correlation of a quantitative assessment of Bonemarrow Erosion arthriticchanges,theRAMRIS,withvalidatedfunctional edema assessments, the FFbH and HAQ. The arthritis score is Definitive Severe Definitive Severe also associated with severity of disease estimated by the Bone numberofaffectedorgansystems. Ulna/radius - - 3 - The presence of arthritis in SSc has been suggested in Scaphoid 3 - 13 - largeregisterstudies[5,6].Aretrospectivecohortanalysis Lunate 18 11 45 3 with supplementary meta-analysis from our group also Triquetral 8 - 50 - supportsahighprevalenceofclinicalanderosivearthritis Pisiform - - - - as agenuinefeature of SSc[7].Registercohorts havethe Trapezium 5 3 13 - drawbackthat data are frequently collected by nonrheu- Trapezoid - - 5 - matologists,resultinginahighheterogeneityinclassifica- Capitate 3 - 24 - tion of joint findings [5]. Furthermore, a definite Hamate - - 3 - differentiationbetweenoverlapsyndromesandpureSScis Metacarpalbase1to5 2 1 2 - difficult withinregister studies, retrospective approaches Metacarpalhead1to5 1 - 8 - ormeta-analyses[7]. Phalangealbase1to5 - - 2 - MRI is considered a very sensitive method for the detection of arthritis. High-field MRI has thus far been Foreachmagneticresonanceimagingfeature,frequenciesofdefiniteand severemanifestationareindicatedasapercentage.-,notpresent.Joint used to examine hand joints in SSc patients in two effusion,bonemarrowedemaanderosionscouldbedeterminedin38hands smaller studies. One retrospective study on 17 patients fromour26patients.Synovitiscouldonlybeassessedin31hands,dueto lackofvenousaccessfortheapplicationofcontrastagent. with joint pain and SSc observed inflammatory changes in 59% of patients [9]. In this study, bone marrow There was also no correlationbetween immunosuppres- edema was even more prominent (53%) than in our sivedrugtreatment,iloprosttreatment,long-termvasodi- cohort (37%), whereas the proportion of patients with latingdrugtreatment,b-blockeruse,low-doseaspirinuse, erosions was much lower (41%) compared with our or concomitant arteriosclerotic disease and the presence study (87%). Unfortunately, no details are provided on of MRI features of arthritis. Neither was affection of the the localization of bone marrow edema in the different lunate bone correlatedwitharteriosclerosisorthe use of patients [9]. Another prospective study analyzed 17 vasodilatingdrugs,b-blockersorlow-doseaspirin. patients with arthralgias and SSc by ultrasound, eight of Radiographs of the hands were obtained as part of the whom also underwent MRI [10]. Joint synovitis was diagnostic work-up in 21 of the 26 patients (81%; Table found by ultrasound in one of 17 patients initially, in 1). Two patients had radiographic changes of the lunate. three of 13 patients after 6 months, and in eight of eight One of these patients had a small erosion that corre- patients analyzed by MRI. Of these eight patients, five sponded to the erosion seen on low-field MRI. The also exhibited bone marrow edema and six patients had other patient exhibited small cystic changes of both erosions [10]. Ultrasound thus appears to underestimate Akbayraketal.ArthritisResearch&Therapy2013,15:R2 Page6of8 http://arthritis-research.com/content/15/1/R2 Figure1Correlationofthearthritisscorewithglobalfunction.CorrelationoftheRheumatoidArthritisMagneticResonanceImagingScore (RAMRIS)withglobalfunctionassessedbytheGermanFunktionsfragebogenHannover(FFbH)questionnaire. arthritis manifestations in SSc even in patients with clin- MRI. The overall disease severity of SScinthese patients ical arthralgias. wascomparable,butthisdysbalancemaybiasourfindings. ThehighsensitivityoftheMRItechnique,therelatively The prevalence and severity oferosions,bone marrow largenumberofpatientsforasinglecenterandtheinclu- edema,andsynovitisinourcohortwithlongstandingSSc sionofpatientsindependent ofclinicalarthralgiaorjoint are comparable with studies on patients with early RA swellingaswellasthestringentexclusionofknownarthri- [22]. In longstanding RA, the severity of inflammatory tis-associated diseases are specific strengths of our study and destructive changes usually increases and affects forthedeterminationofapointprevalenceofarthritisin more joints, thus leading to more severe MRI findings SSc in comparison withtheother studies.Adrawbackof than those observed in our study [8]. Owing to the fact ourstudyistheabsenceofahealthy controlgroup, since thatthepatientsinourstudydidnotfulfillanyclassifica- erosionscanalsobeobservedinhealthysubjects[21].Even tioncriteriaofRAandthatthedetectedarthriticchanges thoughweusedaverystringentdefinitionoferosion,the wererelativelymilddespitelong-standingdiseasewithout prevalenceoferosionsmaythusbeoverestimated.Onthe disease-modifying anti-rheumatic drug treatment in the contrary,thelow-fieldtechniqueunderestimatesbonemar- majority of cases, we conclude that arthritis in SSc does rowedemacomparedwithhigh-fieldMRI[14],whichmay notreflectanoverlapsyndromewithRA[2,3],butrepre- explain the difference in comparison with the results of sentsagenuinediseasemanifestation. Low and colleagues [9]. The failure to inject intravenous The high prevalence of bone marrow edema in our contrastagentin18.5%ofthe38MRIexaminationsleads cohortisofspecificinterestsincebonemarrowedemain tounderestimationofsynovitisintheRAMRIS.Themulti- RAusuallyheraldserosions[15,22]. Thesameindication tude of arthritis-associated MRI findings and the asso- appearstobetrueforarthritisinSScsincethefindingof ciation of quantitative arthritis assessments with the bone marrow edema was frequently associated with ero- functional score are arguments for the overall validity of sions in our study. The predilection of bone marrow our findings. Another drawback is that 35% of eligible edemaanderosionsforthelunateandotherbonesofthe patientsdeclinedparticipation,eventhoughthepositioning proximalrowofcarpalsisnoteworthyandreminiscentof in the low-field MRI is more tolerable than in high-field earlyosteonecrosis. Akbayraketal.ArthritisResearch&Therapy2013,15:R2 Page7of8 http://arthritis-research.com/content/15/1/R2 This finding raises the hypothesis that not only an Additionalfile2:TableS1presentingasummaryoftheRAMRIS. autoimmune process but also ischemia on the basis of ThistableprovidesanoverviewoftheRAMRISperpatient.N/A,not the characteristic microangiopathy of SSc and the fre- applicableduetolackofvenousaccessfortheinjectionofcontrast agent. quent stenosis of arterial vessels of the wrist in patients with SSc [23,24] may play a role in SSc arthritis and its predilection for the lunate bone. Along this line, four cases have been published [25,26] that illustrate an asso- Abbreviations ciation between osteonecrosis of the lunate bone and ACPA:anti-citrullinatedpeptideantibodies;FFbH:Funktionsfragebogen Hannover;HAQ:HealthAssessmentQuestionnaire;MRI:magneticresonance SSc with severe Raynaud’s phenomenon, the clinical imaging;RA:rheumatoidarthritis;RAMRIS:RheumatoidArthritisMagnetic hallmark of ischemia in SSc. In addition, the severity of ResonanceImagingScore;SSc:systemicsclerosis. Raynaud’s phenomenon has been associated previously Authors’contributions with the development of erosive arthritis in SSc [27]. EA,RD,andIHTdesignedthestudy.EAandIHTperformedtheexamination The prominent affection of the lunate bone and the ofpatientsandthelow-fieldMRImeasurements.EA,RD,andIHTanalyzed high severity of Raynaud’s phenomenon in the majority theMRIimages,RDandIHTperformedtheRAMRIS.EA,RD,UM-L,andIHT discussedandinterpretedalldata.EAdraftedthemanuscript,andRD,UM-L, of our patients - as indicated by the high proportion of andIHTcriticallyreviewedandrevisedthemanuscript.Allauthorsreadand patients complaining of clinical deterioration (62%), the approvedthesubmittedmanuscript.EA,UM-L,andIHTreadandapproved need for intravenous iloprost despite long-term use of thefinalmanuscriptafterRDdeceased. oral vasodilators, and the high proportion of current or Competinginterests previous digital ulcers - thus fit very well with the Theauthorsdeclarethattheyhavenocompetinginterests. hypothesis that SSc arthritis is triggered by reactions to Acknowledgements ischemia in the context of severe Raynaud’s phenom- Theauthorswishtoacknowledgewiththismanuscriptthelifeandworkof enon [28] in addition to immunological mechanisms. Prof.RobertDinser,MD,whodiedinatragicaccidentshortlyafter completionofthisworkandthefirstsubmissionofthismanuscriptto ArthritisResearch&Therapy.Prof.Dinserdevelopedtheideaofthestudyand Conclusion wasthecorrespondingauthorfortheinitialsubmission. Insummary,arthritischaracterizedbymildsynovitis,bone marrow edema with a predilection for the lunate bone, Received:28March2012 Revised:25November2012 Accepted:2January2013 Published:4January2013 mild effusions, and low-grade erosions is a clinically underestimatedbutfrequent,genuinefeatureofSSc.The References patternofarthritisdoesnotresembleRA.Wehypothesize 1. RodnanGP:Thenatureofjointinvolvementinprogressivesystemic thatanischemiccomponentreflectedbysevereRaynaud’s sclerosis(diffusescleroderma).AnnIntMed1962,56:422-439. 2. MisraR,DartonK,JewkesRF,BlackCM,MainiRN:Arthritisinscleroderma. phenomenon may be a key trigger for this type of joint BrJRheumatol1995,34:831-837. manifestation. Further studies on a larger number of 3. 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HunzelmannN,GenthE,KriegT,LehmacherW,MelchersI,MeurerM, MoinzadehP,Müller-LadnerU,PfeifferC,RiemekastenG,Schulze-LohoffE, Additional material SunderkoetterC,WeberM,WormM,KlausP,RubbertA,SteinbrinkK, GrundtB,HeinR,Scharffetter-KochanekK,HinrichsR,WalkerK, SzeimiesRM,KarrerS,MüllerA,SeitzC,SchmidtE,LehmannP,FoeldváriI, Additionalfile1:FigureS1showingtypicalexamplesofarthritis ReichenbergerF,etal:TheregistryoftheGermanNetworkforSystemic featuresonlow-fieldMRI.Thisfigureprovidestypicalexamplesof Scleroderma:frequencyofdiseasesubsetsandpatternsoforgan synovitis,bonemarrowedema,erosions,jointeffusion,andtenovaginitis involvement.Rheumatology2008,47:1185-1192. onlow-fieldMRI.(A)Synovitis:T1-weightedgradient-echosequence 6. 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