new asas criteria for the diagnosis of spondyloarthritis: diagnosing

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Radiología. 2014;56(1):7---15

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UPDATE IN RADIOLOGY

New ASAS criteria for the diagnosis of spondyloarthritis:Diagnosing sacroiliitis by magnetic resonance imaging�

M.E. Banegas Illescas ∗, C. López Menéndez, M.L. Rozas Rodríguez,R.M. Fernández Quintero

Servicio de Radiodiagnóstico, Hospital General Universitario de Ciudad Real, Ciudad Real, Spain

Received 17 January 2013; accepted 10 May 2013Available online 11 March 2014

KEYWORDSSacroiliitis;Diagnosis;Magnetic resonanceimaging;Axial spondy-loarthropathies

Abstract Radiographic sacroiliitis has been included in the diagnostic criteria for spondy-loarthropathies since the Rome criteria were defined in 1961. However, in the last ten years,magnetic resonance imaging (MRI) has proven more sensitive in the evaluation of the sacroiliacjoints in patients with suspected spondyloarthritis and symptoms of sacroiliitis; MRI has provenits usefulness not only for diagnosis of this disease, but also for the follow-up of the disease andresponse to treatment in these patients. In 2009, The Assessment of SpondyloArthritis inter-national Society (ASAS) developed a new set of criteria for classifying and diagnosing patientswith spondyloarthritis; one important development with respect to previous classifications isthe inclusion of MRI positive for sacroiliitis as a major diagnostic criterion.

This article focuses on the radiologic part of the new classification. We describe and illustratethe different alterations that can be seen on MRI in patients with sacroiliitis, pointing out thelimitations of the technique and diagnostic pitfalls.© 2013 SERAM. Published by Elsevier España, S.L. All rights reserved.

PALABRAS CLAVESacroileítis;Diagnóstico;Imagen porresonanciamagnética;

Nuevos criterios ASAS para el diagnóstico de espondiloartritis. Diagnósticode sacroileítis por resonancia magnética

Resumen La sacroileítis radiográfica ha formado parte del diagnóstico de lasespondiloartropatías desde su inclusión en los criterios de Roma en 1961. Sin embargo,en la última década, la resonancia magnética (RM) ha demostrado ser más sensible para

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Espondiloartropatías valorar las articulaciones sacroilíacas en los pacientes con sospecha de espondiloartritis y
síntomas de sacroileítis, no solo para diagnosticarla, sino también para seguir la evolución axialesde la enfermedad y el tratamiento de estos pacientes. El grupo The Assessment of Spondy-loArthritis international Society (ASAS) desarrolló en el ano 2009 unos criterios para clasificary diagnosticar a los pacientes con espondiloartritis, entre los que destacaba la inclusión de unestudio de RM positivo para sacroileítis como criterio diagnóstico mayor.
� Please cite this article as: Banegas Illescas ME, López Menéndez C, Rozas Rodríguez ML, Fernández Quintero RM. Nuevos criterios ASASpara el diagnóstico de espondiloartritis. Diagnóstico de sacroileítis por resonancia magnética. Radiología. 2014;56:7---15.

∗ Corresponding author.E-mail address: marux [email protected] (M.E. Banegas Illescas).

2173-5107/$ – see front matter © 2013 SERAM. Published by Elsevier España, S.L. All rights reserved.

dx.doi.org/10.1016/j.rxeng.2014.02.004

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mailto:[email protected]

8 M.E. Banegas Illescas et al.

Este artículo incide en la parte radiológica de esta clasificación. Se describen e ilustran lasdiferentes alteraciones que podemos encontrarnos en los estudios de RM en pacientes consacroileítis, resaltando las limitaciones y potenciales errores diagnósticos.© 2013 SERAM. Publicado por Elsevier España, S.L. Todos los derechos reservados.

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Table 1 ASAS Categorization Criteria for spondyloarthritisin patients under 45 years old of age with lower back pain of3 months duration.

Radiological diagnosis ofsacroiliitis + 1 or morefeatures ofspondyloarthritis

HLA B27 + 2 or more featuresof spondyloarthritis

Features ofspondyloarthritis--- Low inflammatorypain--- Arthritis--- Enthesitis--- Uveítis--- Dactilitis--- Psoriasis--- Crohn/colitis--- Goof responseto NSAID--- Family history ofspondyloarthropathy--- HLA B27

Radiological diagnosisof sacroiliitis--- Active (acute) inflammationin the MRI highly suggestiveof scaroiliitis due to SpA--- Radiological sacroiliitisdefined according to the NewYork criteria (grade >2 bilateralor grade 3---4 unilateral)

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ntroduction

nder the term spondyloarthritis (SpA) we include a hetero-eneous group of chronic rheumatic inflammatory diseaseshat can affect the axial skeleton predominantly. We canistinguish five (5) different groups: ankylosing spondyli-is (AS), arthritis and reactive SpA (formerly known aseiter’ Syndrome), arthritis associated with inflammatoryowel syndrome, psoriatic arthritis and non-radiologicalxial SpA.1 They all share clinical manifestations (the mostmportant, the inflammatory lower back pain), and radio-ogical manifestations (sacroiliitis) accompanied by familialggregation and a strong association with the antigen HLA27.1 Overall prevalence of these entities is estimatedetween 0.23 and 1.8%.2

Traditionally and given the high frequency of jointffectation---over 90%,1 X-raying the sacroiliac joints (SJ) haseen essential to diagnose, categorize and monitor SpA.3

hus the radiographic sacroiliitis is part of the diagnosticriteria of AS since they were established in Rome in 1961,4

nd part of the diagnostic criteria of SpA since they wereublished by Amor et al. in 1990.5 The signs that can beeen in an X-ray translate into structural changes only vis-ble too late which in turn can delay the diagnosis of theisease between 6 and 8 years since symptom onset.1,6

Nevertheless there have been important innovations dur-ng the last ten years for the early management of SpAue to the development of new biological therapies withnti-tumour necrosis factor (anti-TNF) antagonists and therowing relevance of magnetic resonance (MR) as electiveodality for an early diagnosis of the disease, to evaluate

he therapeutic effects and establish prognosis.3,7---12 Nev-rtheless none of the diagnostic categorizations---not evenhe Roman criteria or the European Spondyloarthropathytudy Group (ESSG) classification included MR as a diagnos-ic criteria.13 Back in 2009 the international panel of expertsnown as the Assessment in SpondyloArthritis internationalociety (ASAS) developed a series of criteria for the catego-ization and early diagnosis of axial SpA (the MR-establishedacroiliitis was among these criteria14).

The purpose of this study is to introduce this catego-ization with special attention to radiological issues andescribe through images the different lesions we can see inn MRI in patients with sacroiliitis. We will also talk about theimitations of this categorization as well as about mistakesade during diagnosis.

he ASAS Categorization: findings in magnetic
esonance and definition of sacroiliitis
SAS criteria to diagnose axial SpAs were published back in009 (Table 1).14 These criteria will be applied to patients

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--- High CRP levels

45 years old with lower back pain of 3 or more monthsuration. Criteria comprise 2 sections: one ‘‘radiologicalection’’ and one ‘‘clinical section’’. To qualify for theadiological section a sacroiliitis on a simple radiographyr MRI and at least one of the characteristic traits of SpAetailed in Table 1 needs to be confirmed. To qualify for thelinical section the patient needs to have a positive HLA B27nd at least two of the characteristic traits of SpA withoutadiologic sacroiliitis being mandatory.

ASAS criteria were validated in an international cohortrial with a sensibility and specificity close to 82.9 and 84.4%,espectively as opposed to Amor et al. criteria (sensibility2.9% and specificity 77.5%) and ESSG (sensibility 85.1% andpecificity 65.1%), both adjusted for MRI.15 It is important toighlight that diagnosis in the radiological section showed a6.2 sensibility and 9733% specificity.15

In an effort to establish common criteria to diagnoseacroiliitis through MRI the ASAS/Outcome Measures inheumatology Network (OMERACT) group made up of 8heumatologists and 2 radiologists collected the signs of SpAeported on MRI studies and established which would beecessary to diagnose sacroiliitis associated with SpA.14 The
esions found in sacroiliac joints (SJ) on the MRI were cat-gorized into 2 big groups: active (or acute) inflammatoryesions and structural lesions.

New ASAS criteria for the diagnosis of spondyloarthritis: Diagnosing sacroiliitis by magnetic resonance imaging 9

Figure 1 (a) T1-weighted coronal oblique image where we can see one periarticular hypointensity with greater affectation of theIR se

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iliac margin of the right sacroiliac joint (arrow). (b) On the SToedema.

Active inflammatory lesions

Four types of inflammatory lesions in sacroiliitis associatedwith SpA could be identified: bone oedema and osteitis, syn-ovitis, enthesitis and capsulitis. Bone oedema and osteitisare indispensable to diagnose active sacroiliitis only.

Bone oedema and osteitisThey are highly suggestive of active sacroiliitis. Boneoedema can be found in up to 90% of patients with SpA16

if found in other conditions and between 2.6% and 20% inhealthy patients.15,17

Oedema was defined as a STIR-weighted signal hyper-intensity and it is usually hypointense in T1-weighted

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Figure 2 Images a and b correspond to the oblique T1-weighted axthe sacroiliac (arrow in a) and iliac (arrow in b) margins of the left

uptake of the described areas compatible with osteitis (arrows).

quence we have one hyperintense zone compatible with bone

equences (Fig. 1). The intraforaminal sacral bone consti-utes the intensity of the reference bone signal. T1-weightedequence enhancement with fat suppression after the IVnjection of paramagnetic contrast (gadolinium) (T1-SG-d) shows an increase of vascularization and the perfusion

eactive to inflammation and it was categorized as osteitisFig. 2).

To diagnose sacroiliitis it was established by consensushat one area of bone oedema/osteitis should be present int least two consecutive cuts but if there was more than oneocus one cut would be enough regardless of its size in both
ases (Table 2). Even though bone affectation is typicallyeriarticular (subchondral bone marrow), ASAS criteria doot establish requirements or stipulations when it comes tohe distribution of lesions.
ial images where we can see a lower periarticular sign of bothsacroiliac joint. On the T1-SG-Gd sequence (c) we can see the

10

Table 2 Diagnostic criteria of sacroiliitis through MRI.

Findings required to diagnose sacroiliitis--- The presence of active lesions at the sacroiliac joints

(reflecting active sacroiliitis) to meet the criterion of‘‘positive MRI for sacroiliitis’’ so the ASAS diagnosticcategorization can be applied is required.

--- EMO (STIR) or osteitis (T1-SG-Gd) are suggestive ofspondyloarthritis as long as they affect the subchondraland periarticular areas of the bone marrow*.

--- The isolated existence of other active inflammatorylesions (synovitis, enthesitis or capsulitis) without boneoedema or osteitis associated is NOT enough accordingto the definition of sacroiliitis through MRI.

--- Structural lesions (fat deposits, erosions, sclerosisor ankylosis) probably reflect prior inflammation;however its presence without bone oedema or osteitisis NOT enough to diagnose sacroiliitis.

The disturbance of signal is mandatory--- If there is one active lesion only (bone

oedema/osteitis) the disturbance of signal needs to bepresent in at least two (2) consecutive cuts.

--- If there is more than just one disturbance of signal(oedema/osteitis) in one cut then only one (1) cut will

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ynovitis was defined as an increase of signal intensity inhe synovial margin of SI joint space similar to vessels in T1-G-Gd sequences (Fig. 3). STIR-weighted sequences cannotistinguish synovitis from joint liquid.

nthesitist was defined as hyperintensity on STIR-or-T1-SG-Gd-eighted sequences at the intersectional areas of tendons
nd ligaments (Fig. 4) including the retroarticular spaceinterbone ligaments). Signal disturbance can spread to bonearrow and adjacent soft tissues.
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igure 3 (a and b) White arrow suggests osteitis at the right periarosion of the joint. Intra-articular uptake of the right sacroiliac jblack arrow). At the left sacroiliac joint there are signs of sclerosis

M.E. Banegas Illescas et al.

apsulitisigns of capsulitis are similar to those of sinovitis thoughn this case the abnormal signal intensity it affects thenterior and posterior capsules (Fig. 5). It can spread bothedially and laterally towards the periosteum.

tructural lesions

here are four (4) types of lesions showing structural dam-ge, prior inflammatory affectation of SI joints: subchondralclerosis, erosion, periarticular fat deposits in the bone mar-ow and bone/ankylosis bridges.

ubchondral sclerosisubchondral sclerosis was defined as foci or areas with lowntensity signal or signal void in all sequences without uptaken the gadolinium-enhanced sequences (Fig. 6). The sclerosisttributable to SpA needs to spread at least 5 mm from theoint space since in healthy individuals small foci of sclerosisan be seen.

rosionsrosions appear as bone defects of the joint surface,ypointense on T1 and hyperintense on STIR when activeFig. 7). Initially they debut as isolated lesions and whenonverge they can cause joint ‘‘pseudo-widening’’.

eriarticular fat bone marrow deposithe fat bone marrow deposit is considered a chronical

esion of SpA because it can be spotted characteristicallyn areas where active inflammatory lesions are located. Itsnatomopathological base is not very well known.16 It isharacterized by an increase of the intensity signal on T1-eighted sequences (Fig. 8). It is an inespecific finding that

s present in 27% of healthy individuals.17

one bridges and ankylosis
hey are hypointense lesions in all sequences and some-imes they are surrounded by fat bone marrow deposits.nitially there are ‘‘bone episodes’’ one against the othernd eventually they converge creating bridges that go
rticular iliac margin while the point of the arrow shows a mildoint on the T1-SG-Gd sequence (b) compatible with synovitis

at the iliac side >5 mm suggestive of sacroiliitis (asterisk).


Figure 4 Disturbance of signal intensity in one of the posterior sacroiliac ligaments (arrows) with hypointensity at the T1-weightedcoronal oblique image (a), and hyperintensity at the STIR coronal oblique image (b). It is accompanied by signal hypointensity atthe osteoligamentous insertion sites at T1-weighted coronal oblique image and signal hyperintensity at STIR compatible with boneoedema (asterisks).

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through the joint and in serious cases they erase the jointspace (ankylosis) (Fig. 9).

With these signs in mind there was consensus that to diag-nose sacroiliitis due to SpA the MRI needs to show foci of
bone oedema on STIR or osteitis on T1 Gd+/− −SG regard-less of the occurrence of other inflammatory or structurallesions.
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Figure 5 Superior capsular enhancement of the left sacroiliac joinot correspond to joint liquid or other signal disturbances at the

periarticular bone margins at the left side and the sacral margin of

tudy protocol and technical issues

he document written by the ASAS/OMERACT panel also
ncludes technical recommendations for the MRI studyf SI joints based on ASAS diagnostic criteria.14 Thetudy protocol needs to include: one STIR sequenceTR/TE/TI 4000/60/150 ms), one T1-weighted sequence
nt at the T1-SG-Gd sequence (point of arrow in b) which doesT2-weighted sequence (a). We can see enhancement of boththe right side as well fully compatible with osteitis (arrows).

12 M.E. Banegas Illescas et al.

Figure 6 Significant extent hypointensity of both margins of left sacroiliac joint (white circle) at the T2-weighted coronal obliques bliqup rinte

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equence (a) without enhancement at the T1-SG-Gd coronal oointing at a marginal enhancement area of sclerosis with hype

TR/TE 500/10 ms), one T2-weighted turbo spin echoequence (TR/TE 4000/60 ms) or one T2-weighted echo-radient (TR/TE 180/7.15 ms).10,14 Later one T1-SG-Gdequence (TR/TE 660/16 ms) can be added to detect activenflammatory lesions and clear suspicious signs in the studyithout the help of contrast agents. The image matrix needs

o have at least 512 pixels and each sequence consists oft least 10---12 cuts (0.4 mm cut separation), and each cute 3---4 mm thick. It is recommended that basic sequencesSTIR and T1 TSE) are obtained through the oblique coro-al plane running parallel to the line that goes through theuperior and dorsal margins of S1 and S1 whereas additionalequences can be obtained through the oblique transversallace---parallel to S1 superior vertebral plateau.

In patients allergic to gadolinium or those with impairedenal function, the T1-SG-Gd sequence can be suppressedince it has been proven that STIR and T1-SG-Gd sequencesre comparable when it comes to detecting periarticular

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igure 7 Marginal irregularities compatible with erosions in bothequence (a), and in the iliac margin of the right sacroiliac joint (ar

e sequence (b) compatible with sclerosis. The arrow in (b) isnsity in (a) fully compatible with osteitis.

nflammation18 and as we have already seen because estab-ishing other active lesions except for osteitis is not decisivehen it comes to diagnosing sacroiliitis. When it comes to

tructural lesions (sclerosis, fat bone marrow deposit, andnkylosis) the T1-weighted sequence is usually enough toetect these even though T1 SG and T2 TSE or EG allow uso see cartilage better and can therefore be useful to findrosions.14,19

In our institution the standard protocol to study SI jointsonsists of STIR and T1-weighted sequences both in theblique coronal plane to detect inflammatory lesions andlso consists of oblique transversal T1 and T2 TSE sequenceso establish structural lesions. The T1-SG-Gd sequence isot routine and is usually reserved to find coexistent active
nflammatory lesions in the presence of bone oedema as wells to characterize lesions and other abnormalities of signalntensity seen at the basic sequences related or not to theacroiliac affectation.
sacroiliac joints (arrows) at the T1-weighted coronal obliquerow) at the T2 TSE coronal oblique image (b).


Figure 8 Areas of periarticular bone signal enhancement at the T1-weighted coronal oblique sequence (arrows in a) whose signalosits.

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is suppressed at the STIR sequence (b), suggestive of fat depperiarticular fat deposit (arrow head).

Differential diagnosis

Some diseases can simulate the aforementioned inflam-matory conditions. It is important to highlight that theinflammation of SI joints attributable to SpA is usuallylimited to the bone or joint. On the contrary the inflamma-tion and infection associated with septic sacroiliitis usuallyspreads to soft tissues.20

Arthrosis is more common in the elderly. It can causeunilateral or bilateral, symmetrical or asymmetrical jointinflammation.21 SpA-induced sacroiliitis and arthrosis canshow common structural changes when the sacroiliac jointhas suffered prior inflammatory changes like subchondralsclerosis, slipped joint (suggestive of SpA when the jointis <2 mm in patients under 40 years old) and ankylosis.Osteophytes, neumocysts and joint void are common ofarthrosis.22 Arthrosis can be associated with small areasof bone oedema too.14

Osteitis condensans ilii has a typical location and configu-ration of both on the MRI and other image modalities (simpleradiography and CT). Characteristically joint affectation isbilateral, symmetrical and consists of a triangular area of

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Figure 9 Ankylosis: the right sacroiliac joint space is erased (asequences (a) and T1-SG-Gd (b), with significant sclerosis of articula

In (b) we can also see bone oedema next to the left sacral

ubchondral sclerosis at the anterior inferior iliac margin---ider at its inferior region.21 This lesion is typical of middle-ged women and is attributed to stress during pregnancy andelivery.23

Insufficiency fractures typical of the sacrum can causelterations of signal that might be compatible with boneedema and osteitis at presentation. Infiltrating the primaryr metastasic tumour should be considered in some casesuring differential diagnosis.14

SAS criteria: pros and cons

SAS criteria show indisputable pros: for the first time theynclude MRI to diagnose axial SpA, describe the agreed find-ngs we can see in this group of conditions and establish aet of stipulations for the diagnosis of sacroiliitis throughRI which can easily be reproduced. Also the introductionf MRI as a diagnostic tool to find acute SpA lesions allows us
o diagnose and manage this condition way before radiologi-al sacroiliitis shows up whose diagnostic delay worsens dueo the great inter-observer variability (0---35%), especially inrades 1 and 2.24
rrows) at the echo-gradient T2-weighted transversal obliquer margins in (a).

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Nevertheless after reviewing the most recent literaturen this regard and based on our own experience we can seehat these criteria have limitations affecting the diagnos-ic and prognostic utility of MRI in these patients. Firstly inbsence of bone oedema or osteitis the MRI-identified struc-ural lesions are not diagnostic of sacroiliits. This exclusion isomehow contradictory due to the fact that the other radio-ogical marker of sacroiliitis is based on structural changeseen on the simple X-ray according to New York new mod-fied criteria despite the great inter-observer variability.25

lso several trials have shown that MRI is not only capa-le of finding structural lesions before they can be seen onhe X-ray without active inflammatory lesions,17,26 but it islso capable of increasing its diagnostic sensibility from 67%o 81% when erosions are analyzed besides bone oedemaithout changes in specificity (88%).27

Secondly even though the ASAS-OMERACT criteria estab-ish the minimum amount of foci of bone oedema or osteitisecessary to consider an MRI a positive MR the number ofoci found is not counted. Healthy controls can have iso-ated foci of hyperintensity on STIR (bone pseudo-oedema)ith a frequency close to 27%.26,27 Aydin et al. followed7 patients with MRIs for 8 years, 28 with inflammatory lowerack and positive ASAS criteria of SpA and 19 healthy individ-als. Results indicate that the proportion of positive MRI wasigher in patients with a clinical diagnosis of SpA (79%) thann controls (22.2%) but they also indicate that if the cut-offoint was raised to 2 or more foci of bone oedema the pro-ortion of false positives (healthy controls with a positiveRI) was halved.28

Thirdly these criteria do not reflect the prognostictility of MR; one agreed universal system capable ofuantifying active inflammatory lesions and evaluating thectivity of the condition and the therapeutic response hasot been developed either. Several authors have high-ighted the importance of evaluating the magnitude andeverity of periarticular bone oedema to predict theppearance of radiographic sacroiliitis due to the impor-ance of its prognostic utility and assess the response toherapy---very more important considering the high cost ofiological therapies.29,30 In the same way different systemso quantify active inflammatory lesions through MR haveeen developed---Spondyloarthritis Research Consortium ofanada [SPARCC], Berlín, Leeds, etc.11 which based on boneedema and its magnitude allow us to monitor the activ-ty and damage of the condition as well as the response toherapy. In this sense ASAS-OMERACT criteria do not resolveoday’s existing heterogeneity and disparity for the assess-ent of these parameters.Taking all this into consideration some authors believe

t is necessary to reassess and update the SpA-positive MRriteria including structural findings and quantifying theagnitude, extension and number of areas of hyperinten-

ity in the para-articular bone marrow by developing onenternational standard method of reading.28,31

A systematic review of literature showed that most arti-les published had series of very few patients and that thereere very few articles of high methodological quality with
n adequate sample size and case-control or longitudinalesigns. Also in most of these works the gold standard usedo assess the diagnostic accuracy of MR was clinical diag-osis which was not independent of the information given
M.E. Banegas Illescas et al.

y the MRI and whose reproducibility was not evaluated.32

o to validate MR as the diagnostic reference standard ofacroiliitis we need longitudinal studies with large cohortsspecially with groups of patients with early SpA and inespe-ific lower back pain.

onclusion

SAS criteria to diagnose axial SpA are the first ones todd MRI to diagnose sacroiliitis which is a turning pointn the clinical-radiological management of this condition.hey describe the different types of lesions we may findactive inflammatory lesions and chronic structural lesions)nd establish the diagnostic criteria to be able to diagnoseacroiliitis through MR based on active inflammatory lesionsnly (bone oedema and osetitis). As radiologists we need toiagnose as sacroiliits various cases which just do not qualifyor ASAS criteria: cases with overt structural damage (ero-ions, sclerosis and even ankylosis) but without presence ofone oedema. Anyway we need to conduct future researcho update these criteria, determine its prognostic value,nd see if we are able to come to terms with a universaluantitative method.

thical responsibilities

rotection of human and animal subjects. Authors confirmhat no experiments have been done with humans or animalsuring this research.

onfidentiality of data. Authors confirm that in this reporthere are no personal data from patients.

ight to privacy and informed consent. Authors confirmhat in this report there are no personal data from patients.

uthors contributions

1 Manager of the integrity of the study: MEBI.2 Original Idea of the Study: MEBI.3 Study Design: MEBI and CLM.4 Data Mining: MEBI and CLM.5 Data Analysis and Interpretation: MEBI, CLM, MLRR and

RMFQ.6 Statistical Analysis: Not available.7 Reference Search: MEBI, CLM, MLRR and RMFQ.8 Writing: MEBI, CLM, MLRR and RMFQ.9 Manuscript critical review with intellectually relevant

contributions: MEBI, CLM, MLRR and RMFQ.0 Final Version Approval: MEBI, CLM, MLRR and RMFQ.

onflict of interest

uthors reported no conflict of interest.

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new asas criteria for the diagnosis of spondyloarthritis: diagnosing

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