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Radiología. 2014;56(1):7---15

www.elsevier.es/rx

UPDATE IN

New ASAS criteria for the diagnosis of spondyloarthritis:

Diagnosing 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 2013

Available online 11 March 2014

KEYWORDS Abstract Radiographic sacroiliitis has been included in the diagnostic criteria for spondy-

Sacroiliitis; loarthropathies since the Rome criteria were defined in 1961. However, in the last ten years,

Diagnosis; magnetic resonance imaging (MRI) has proven more sensitive in the evaluation of the sacroiliac

Magnetic resonance joints in patients with suspected spondyloarthritis and symptoms of sacroiliitis; MRI has proven

imaging; its usefulness not only for diagnosis of this disease, but also for the follow-up of the disease and

Axial spondy- response to treatment in these patients. In 2009, The Assessment of SpondyloArthritis inter-

loarthropathies national Society (ASAS) developed a new set of criteria for classifying and diagnosing patients

with spondyloarthritis; one important development with respect to previous classifications is

the 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 illustrate

the different alterations that can be seen on MRI in patients with sacroiliitis, pointing out the

limitations of the technique and diagnostic pitfalls.

© 2013 SERAM. Published by Elsevier España, S.L. All rights reserved.

PALABRAS CLAVE Nuevos criterios ASAS para el diagnóstico de espondiloartritis. Diagnóstico

Sacroileítis; de sacroileítis por resonancia magnética

Diagnóstico;

Resumen La sacroileítis radiográfica ha formado parte del diagnóstico de las

Imagen por

resonancia espondiloartropatías desde su inclusión en los criterios de Roma en 1961. Sin embargo,

magnética; en la última década, la resonancia magnética (RM) ha demostrado ser más sensible para

Espondiloartropatías valorar las articulaciones sacroilíacas en los pacientes con sospecha de espondiloartritis y

axiales síntomas de sacroileítis, no solo para diagnosticarla, sino también para seguir la evolución

de 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 clasificar

y diagnosticar a los pacientes con espondiloartritis, entre los que destacaba la inclusión de un

estudio 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 ASAS

para 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.

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8 M.E. Banegas Illescas et al.

Este artículo incide en la parte radiológica de esta clasificación. Se describen e ilustran las

diferentes alteraciones que podemos encontrarnos en los estudios de RM en pacientes con

sacroileítis, resaltando las limitaciones y potenciales errores diagnósticos.

© 2013 SERAM. Publicado por Elsevier España, S.L. Todos los derechos reservados.

Introduction

Table 1 ASAS Categorization Criteria for spondyloarthritis

in patients under 45 years old of age with lower of

Under the term spondyloarthritis (SpA) we include a hetero-

3 months duration.

geneous group of chronic rheumatic inflammatory diseases

that can affect the axial skeleton predominantly. We can Radiological diagnosis of HLA B27 + 2 or more features

distinguish five (5) different groups: ankylosing spondyli- sacroiliitis + 1 or more of spondyloarthritis

tis (AS), and reactive SpA (formerly known as features of

Reiter’ Syndrome), arthritis associated with inflammatory spondyloarthritis

bowel syndrome, and non-radiological

Features of Radiological diagnosis

1

axial SpA. They all share clinical manifestations (the most

spondyloarthritis of sacroiliitis

important, the inflammatory lower back pain), and radio-

--- Low inflammatory --- Active (acute) inflammation

logical manifestations (sacroiliitis) accompanied by familial

pain in the MRI highly suggestive

aggregation and a strong association with the antigen HLA

--- Arthritis of scaroiliitis due to SpA

1

B27. Overall prevalence of these entities is estimated

--- Enthesitis --- Radiological sacroiliitis

2

between 0.23 and 1.8%.

--- Uveítis defined according to the New

Traditionally and given the high frequency of joint

--- Dactilitis York criteria (grade >2 bilateral

1

affectation---over 90%, X-raying the sacroiliac joints (SJ) has

--- or grade 3 --- 4 unilateral)

3

been essential to diagnose, categorize and monitor SpA. ---Crohn/colitis

Thus the radiographic sacroiliitis is part of the diagnostic

---Goof response

4

criteria of AS since they were established in Rome in 1961,

to NSAID

and part of the diagnostic criteria of SpA since they were

---Family history of

5

published by Amor et al. in 1990. The signs that can be

seen in an X-ray translate into structural changes only vis-

--- H L A B27

ible too late which in turn can delay the diagnosis of the

---High CRP levels

1,6

disease between 6 and 8 years since symptom onset.

Nevertheless there have been important innovations dur-

ing the last ten years for the early management of SpA

due to the development of new biological with

<45 years old with lower back pain of 3 or more months

anti-tumour necrosis factor (anti-TNF) antagonists and the

duration. Criteria comprise 2 sections: one ‘‘radiological

growing relevance of magnetic resonance (MR) as elective

section’’ and one ‘‘clinical section’’. To qualify for the

modality for an early diagnosis of the disease, to evaluate

radiological section a sacroiliitis on a simple

3,7---12

the therapeutic effects and establish prognosis. Nev-

or MRI and at least one of the characteristic traits of SpA

ertheless none of the diagnostic categorizations---not even

detailed in Table 1 needs to be confirmed. To qualify for the

the Roman criteria or the European Spondyloarthropathy

clinical section the patient needs to have a positive HLA B27

Study Group (ESSG) classification included MR as a diagnos-

and at least two of the characteristic traits of SpA without

13

tic criteria. Back in 2009 the international panel of experts

radiologic sacroiliitis being mandatory.

known as the Assessment in SpondyloArthritis international

ASAS criteria were validated in an international cohort

Society (ASAS) developed a series of criteria for the catego-

trial with a sensibility and specificity close to 82.9 and 84.4%,

rization and early diagnosis of axial SpA (the MR-established

respectively as opposed to Amor et al. criteria (sensibility

14

sacroiliitis was among these criteria ).

82.9% and specificity 77.5%) and ESSG (sensibility 85.1% and

The purpose of this study is to introduce this catego- 15

specificity 65.1%), both adjusted for MRI. It is important to

rization with special attention to radiological issues and

highlight that diagnosis in the radiological section showed a

describe through images the different lesions we can see in 15

66.2 sensibility and 9733% specificity.

an MRI in patients with sacroiliitis. We will also talk about the

In an effort to establish common criteria to diagnose

limitations of this categorization as well as about mistakes

sacroiliitis through MRI the ASAS/Outcome Measures in

made during diagnosis.

Rheumatology Network (OMERACT) group made up of 8

rheumatologists and 2 radiologists collected the signs of SpA

The ASAS Categorization: findings in magnetic reported on MRI studies and established which would be

14

resonance and definition of sacroiliitis necessary to diagnose sacroiliitis associated with SpA. The

lesions found in sacroiliac joints (SJ) on the MRI were cat-

ASAS criteria to diagnose axial SpAs were published back in egorized into 2 big groups: active (or acute) inflammatory

14

2009 (Table 1). These criteria will be applied to patients lesions and structural lesions.

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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 the

iliac margin of the right (arrow). (b) On the STIR sequence we have one hyperintense zone compatible with bone

oedema.

Active inflammatory lesions sequences (Fig. 1). The intraforaminal sacral bone consti-

tutes the intensity of the reference bone signal. T1-weighted

Four types of inflammatory lesions in sacroiliitis associated sequence enhancement with fat suppression after the IV

with SpA could be identified: bone oedema and osteitis, syn- injection of paramagnetic contrast (gadolinium) (T1-SG-

ovitis, enthesitis and capsulitis. Bone oedema and osteitis Gd) shows an increase of vascularization and the perfusion

are indispensable to diagnose active sacroiliitis only. reactive to inflammation and it was categorized as osteitis

(Fig. 2).

To diagnose sacroiliitis it was established by consensus

Bone oedema and osteitis that one area of bone oedema/osteitis should be present in

They are highly suggestive of active sacroiliitis. Bone at least two consecutive cuts but if there was more than one

16

oedema can be found in up to 90% of patients with SpA focus one cut would be enough regardless of its size in both

if found in other conditions and between 2.6% and 20% in cases (Table 2). Even though bone affectation is typically

15,17

healthy patients. periarticular (subchondral bone marrow), ASAS criteria do

Oedema was defined as a STIR-weighted signal hyper- not establish requirements or stipulations when it comes to

intensity and it is usually hypointense in T1-weighted the distribution of lesions.

Figure 2 Images a and b correspond to the oblique T1-weighted axial images where we can see a lower periarticular sign of both

the sacroiliac (arrow in a) and iliac (arrow in b) margins of the left sacroiliac joint. On the T1-SG-Gd sequence (c) we can see the

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

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10 M.E. Banegas Illescas et al.

Capsulitis

Table 2 Diagnostic criteria of sacroiliitis through MRI.

Signs of capsulitis are similar to those of sinovitis though

Findings required to diagnose sacroiliitis in this case the abnormal signal intensity it affects the

--- The presence of active lesions at the sacroiliac joints anterior and posterior capsules (Fig. 5). It can spread both

(reflecting active sacroiliitis) to meet the criterion of medially and laterally towards the periosteum.

‘‘positive MRI for sacroiliitis’’ so the ASAS diagnostic

categorization can be applied is required.

Structural lesions

--- EMO (STIR) or osteitis (T1-SG-Gd) are suggestive of

spondyloarthritis as long as they affect the subchondral

There are four (4) types of lesions showing structural dam-

and periarticular areas of the bone marrow*.

age, prior inflammatory affectation of SI joints: subchondral

--- The isolated existence of other active inflammatory

sclerosis, erosion, periarticular fat deposits in the bone mar-

lesions (synovitis, enthesitis or capsulitis) without bone

row and bone/ankylosis bridges.

oedema or osteitis associated is NOT enough according

to the definition of sacroiliitis through MRI.

Subchondral sclerosis

--- Structural lesions (fat deposits, erosions, sclerosis

Subchondral sclerosis was defined as foci or areas with low

or ankylosis) probably reflect prior inflammation;

intensity signal or signal void in all sequences without uptake

however its presence without bone oedema or osteitis

in the gadolinium-enhanced sequences (Fig. 6). The sclerosis

is NOT enough to diagnose sacroiliitis.

attributable to SpA needs to spread at least 5 mm from the

joint space since in healthy individuals small foci of sclerosis

The disturbance of signal is mandatory

can be seen.

--- I f there is one active lesion only (bone

oedema/osteitis) the disturbance of signal needs to be

Erosions

present in at least two (2) consecutive cuts.

Erosions appear as bone defects of the joint surface,

--- If there is more than just one disturbance of signal

hypointense on T1 and hyperintense on STIR when active

(oedema/osteitis) in one cut then only one (1) cut will

(Fig. 7). Initially they debut as isolated lesions and when

be necessary.

converge they can cause joint ‘‘pseudo-widening’’.

Synovitis Periarticular fat bone marrow deposit

The fat bone marrow deposit is considered a chronical

lesion of SpA because it can be spotted characteristically

Synovitis was defined as an increase of signal intensity in

in areas where active inflammatory lesions are located. Its

the synovial margin of SI joint space similar to vessels in T1- 16

anatomopathological base is not very well known. It is

SG-Gd sequences (Fig. 3). STIR-weighted sequences cannot

characterized by an increase of the intensity signal on T1-

distinguish synovitis from joint liquid.

weighted sequences (Fig. 8). It is an inespecific finding that

17

is present in 27% of healthy individuals.

Enthesitis

It was defined as hyperintensity on STIR-or-T1-SG-Gd-

Bone bridges and ankylosis

weighted sequences at the intersectional areas of tendons

They are hypointense lesions in all sequences and some-

and ligaments (Fig. 4) including the retroarticular space

times they are surrounded by fat bone marrow deposits.

(interbone ligaments). Signal disturbance can spread to bone

Initially there are ‘‘bone episodes’’ one against the other

marrow and adjacent soft tissues.

and eventually they converge creating bridges that go

Figure 3 (a and b) White arrow suggests osteitis at the right periarticular iliac margin while the point of the arrow shows a mild

erosion of the joint. Intra-articular uptake of the right sacroiliac joint on the T1-SG-Gd sequence (b) compatible with synovitis

(black arrow). At the left sacroiliac joint there are signs of sclerosis at the iliac side >5 mm suggestive of sacroiliitis (asterisk).

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New ASAS criteria for the diagnosis of spondyloarthritis: Diagnosing sacroiliitis by magnetic resonance imaging 11

Figure 4 Disturbance of signal intensity in one of the posterior sacroiliac ligaments (arrows) with hypointensity at the T1-weighted

coronal oblique image (a), and hyperintensity at the STIR coronal oblique image (b). It is accompanied by signal hypointensity at

the osteoligamentous insertion sites at T1-weighted coronal oblique image and signal hyperintensity at STIR compatible with bone

oedema (asterisks).

through the joint and in serious cases they erase the joint Study protocol and technical issues

space (ankylosis) (Fig. 9).

With these signs in mind there was consensus that to diag-

The document written by the ASAS/OMERACT panel also

nose sacroiliitis due to SpA the MRI needs to show foci of

includes technical recommendations for the MRI study

bone oedema on STIR or osteitis on T1 Gd+/− −SG regard- 14

of SI joints based on ASAS diagnostic criteria. The

less of the occurrence of other inflammatory or structural

study protocol needs to include: one STIR sequence

lesions.

(TR/TE/TI 4000/60/150 ms), one T1-weighted sequence

Figure 5 Superior capsular enhancement of the left sacroiliac joint at the T1-SG-Gd sequence (point of arrow in b) which does

not correspond to joint liquid or other signal disturbances at the T2-weighted sequence (a). We can see enhancement of both

periarticular bone margins at the left side and the sacral margin of the right side as well fully compatible with osteitis (arrows).

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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 oblique

sequence (a) without enhancement at the T1-SG-Gd coronal oblique sequence (b) compatible with sclerosis. The arrow in (b) is

pointing at a marginal enhancement area of sclerosis with hyperintensity in (a) fully compatible with osteitis.

18

(TR/TE 500/10 ms), one T2-weighted turbo spin echo inflammation and as we have already seen because estab-

sequence (TR/TE 4000/60 ms) or one T2-weighted echo- lishing other active lesions except for osteitis is not decisive

10,14

gradient (TR/TE 180/7.15 ms). Later one T1-SG-Gd when it comes to diagnosing sacroiliitis. When it comes to

sequence (TR/TE 660/16 ms) can be added to detect active structural lesions (sclerosis, fat bone marrow deposit, and

inflammatory lesions and clear suspicious signs in the study ankylosis) the T1-weighted sequence is usually enough to

without the help of contrast agents. The image matrix needs detect these even though T1 SG and T2 TSE or EG allow us

to have at least 512 pixels and each sequence consists of to see cartilage better and can therefore be useful to find

14,19

at least 10---12 cuts (0.4 mm cut separation), and each cut erosions.

be 3 --- 4 mm thick. It is recommended that basic sequences In our institution the standard protocol to study SI joints

(STIR and T1 TSE) are obtained through the oblique coro- consists of STIR and T1-weighted sequences both in the

nal plane running parallel to the line that goes through the oblique coronal plane to detect inflammatory lesions and

superior and dorsal margins of S1 and S1 whereas additional also consists of oblique transversal T1 and T2 TSE sequences

sequences can be obtained through the oblique transversal to establish structural lesions. The T1-SG-Gd sequence is

place---parallel to S1 superior vertebral plateau. not routine and is usually reserved to find coexistent active

In patients allergic to gadolinium or those with impaired inflammatory lesions in the presence of bone oedema as well

renal function, the T1-SG-Gd sequence can be suppressed as to characterize lesions and other abnormalities of signal

since it has been proven that STIR and T1-SG-Gd sequences intensity seen at the basic sequences related or not to the

are comparable when it comes to detecting periarticular sacroiliac affectation.

Figure 7 Marginal irregularities compatible with erosions in both sacroiliac joints (arrows) at the T1-weighted coronal oblique

sequence (a), and in the iliac margin of the right sacroiliac joint (arrow) at the T2 TSE coronal oblique image (b).

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New ASAS criteria for the diagnosis of spondyloarthritis: Diagnosing sacroiliitis by magnetic resonance imaging 13

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

is suppressed at the STIR sequence (b), suggestive of fat deposits. In (b) we can also see bone oedema next to the left sacral

periarticular fat deposit (arrow head).

Differential diagnosis subchondral sclerosis at the anterior inferior iliac margin---

21

wider at its inferior region. This lesion is typical of middle-

aged women and is attributed to stress during and

Some diseases can simulate the aforementioned inflam-

delivery.23

matory conditions. It is important to highlight that the

Insufficiency fractures typical of the can cause

inflammation of SI joints attributable to SpA is usually

alterations of signal that might be compatible with bone

limited to the bone or joint. On the contrary the inflamma-

oedema and osteitis at presentation. Infiltrating the primary

tion and infection associated with septic sacroiliitis usually

20 or metastasic tumour should be considered in some cases

spreads to soft tissues.

14

during differential diagnosis.

Arthrosis is more common in the elderly. It can cause

unilateral or bilateral, symmetrical or asymmetrical joint

21

inflammation. SpA-induced sacroiliitis and arthrosis can ASAS criteria: pros and cons

show common structural changes when the sacroiliac joint

has suffered prior inflammatory changes like subchondral ASAS criteria show indisputable pros: for the first time they

sclerosis, slipped joint (suggestive of SpA when the joint include MRI to diagnose axial SpA, describe the agreed find-

is <2 mm in patients under 40 years old) and ankylosis. ings we can see in this group of conditions and establish a

Osteophytes, neumocysts and joint void are common of set of stipulations for the diagnosis of sacroiliitis through

22

arthrosis. Arthrosis can be associated with small areas MRI which can easily be reproduced. Also the introduction

14

of bone oedema too. of MRI as a diagnostic tool to find acute SpA lesions allows us

Osteitis condensans ilii has a typical location and configu- to diagnose and manage this condition way before radiologi-

ration of both on the MRI and other image modalities (simple cal sacroiliitis shows up whose diagnostic delay worsens due

radiography and CT). Characteristically joint affectation is to the great inter-observer variability (0---35%), especially in

24

bilateral, symmetrical and consists of a triangular area of grades 1 and 2.

Figure 9 Ankylosis: the right sacroiliac joint space is erased (arrows) at the echo-gradient T2-weighted transversal oblique

sequences (a) and T1-SG-Gd (b), with significant sclerosis of articular margins in (a).

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14 M.E. Banegas Illescas et al.

32

Nevertheless after reviewing the most recent literature by the MRI and whose reproducibility was not evaluated.

on this regard and based on our own experience we can see So to validate MR as the diagnostic reference standard of

that these criteria have limitations affecting the diagnos- sacroiliitis we need longitudinal studies with large cohorts

tic and prognostic utility of MRI in these patients. Firstly in especially with groups of patients with early SpA and inespe-

absence of bone oedema or osteitis the MRI-identified struc- cific lower back pain.

tural lesions are not diagnostic of sacroiliits. This exclusion is

somehow contradictory due to the fact that the other radio- Conclusion

logical marker of sacroiliitis is based on structural changes

seen on the simple X-ray according to New York new mod-

25 ASAS criteria to diagnose axial SpA are the first ones to

ified criteria despite the great inter-observer variability.

add MRI to diagnose sacroiliitis which is a turning point

Also several trials have shown that MRI is not only capa-

in the clinical-radiological management of this condition.

ble of finding structural lesions before they can be seen on

17,26 They describe the different types of lesions we may find

the X-ray without active inflammatory lesions, but it is

(active inflammatory lesions and chronic structural lesions)

also capable of increasing its diagnostic sensibility from 67%

and establish the diagnostic criteria to be able to diagnose

to 81% when erosions are analyzed besides bone oedema

27 sacroiliitis through MR based on active inflammatory lesions

without changes in specificity (88%).

only (bone oedema and osetitis). As radiologists we need to

Secondly even though the ASAS-OMERACT criteria estab-

diagnose as sacroiliits various cases which just do not qualify

lish the minimum amount of foci of bone oedema or osteitis

for ASAS criteria: cases with overt structural damage (ero-

necessary to consider an MRI a positive MR the number of

sions, sclerosis and even ankylosis) but without presence of

foci found is not counted. Healthy controls can have iso-

bone oedema. Anyway we need to conduct future research

lated foci of hyperintensity on STIR (bone pseudo-oedema)

26,27 to update these criteria, determine its prognostic value,

with a frequency close to 27%. Aydin et al. followed

and see if we are able to come to terms with a universal

57 patients with MRIs for 8 years, 28 with inflammatory lower

quantitative method.

back and positive ASAS criteria of SpA and 19 healthy individ-

uals. Results indicate that the proportion of positive MRI was

Ethical responsibilities

higher in patients with a clinical diagnosis of SpA (79%) than

in controls (22.2%) but they also indicate that if the cut-off

Protection of human and animal subjects. Authors confirm

point was raised to 2 or more foci of bone oedema the pro-

that no experiments have been done with humans or animals

portion of false positives (healthy controls with a positive

28 during this research.

MRI) was halved.

Thirdly these criteria do not reflect the prognostic

utility of MR; one agreed universal system capable of Confidentiality of data. Authors confirm that in this report

quantifying active inflammatory lesions and evaluating the there are no personal data from patients.

activity of the condition and the therapeutic response has

not been developed either. Several authors have high- Right to privacy and informed consent. Authors confirm

lighted the importance of evaluating the magnitude and that in this report there are no personal data from patients.

severity of periarticular bone oedema to predict the

appearance of radiographic sacroiliitis due to the impor-

Authors contributions

tance of its prognostic utility and assess the response to

---very more important considering the high cost of

1 Manager of the integrity of the study: MEBI.

29,30

biological therapies. In the same way different systems

2 Original Idea of the Study: MEBI.

to quantify active inflammatory lesions through MR have

3 Study Design: MEBI and CLM.

been developed---Spondyloarthritis Research Consortium of

4 Data Mining: MEBI and CLM.

11

Canada [SPARCC], Berlín, Leeds, etc. which based on bone

5 Data Analysis and Interpretation: MEBI, CLM, MLRR and

oedema and its magnitude allow us to monitor the activ- RMFQ.

ity and damage of the condition as well as the response to

6 Statistical Analysis: Not available.

therapy. In this sense ASAS-OMERACT criteria do not resolve

7 Reference Search: MEBI, CLM, MLRR and RMFQ.

today’s existing heterogeneity and disparity for the assess-

8 Writing: MEBI, CLM, MLRR and RMFQ.

ment of these parameters.

9 Manuscript critical review with intellectually relevant

Taking all this into consideration some authors believe

contributions: MEBI, CLM, MLRR and RMFQ.

it is necessary to reassess and update the SpA-positive MR

10 Final Version Approval: MEBI, CLM, MLRR and RMFQ.

criteria including structural findings and quantifying the

magnitude, extension and number of areas of hyperinten-

Conflict of interest

sity in the para-articular bone marrow by developing one

28,31

international standard method of reading.

Authors reported no conflict of interest.

A systematic review of literature showed that most arti-

cles published had series of very few patients and that there

were very few articles of high methodological quality with References

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