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Clinical and epidemiological research
Extended report
Evaluation of the validity of the different arms of the ASAS set of criteria for axial spondyloarthritis and description of the different imaging abnormalities suggestive of spondyloarthritis: data from the DESIR cohort
  1. Anna Moltó1,2,
  2. Simon Paternotte1,
  3. Désirée van der Heijde3,
  4. Pascal Claudepierre4,5,
  5. Martin Rudwaleit6,
  6. Maxime Dougados1
  1. 1Paris Descartes University, Department of Rheumatology, Hôpital Cochin – Assistance Publique- Hôpitaux de Paris, INSERM (U1153): Clinical epidemiology and biostatistics, PRES Sorbonne Paris-Cité, France
  2. 2Departament de Medicina, Universitat Autònoma de Barcelona, Barcelona, Spain
  3. 3Leiden University Medical Center, Leiden, The Netherlands
  4. 4Laboratoire d'Investigation Clinique (LIC) EA4393, Université Paris Est Créteil, Créteil, France
  5. 5Service de Rhumatologie, AP-HP, Hôpital Henri-Mondor, Créteil, France
  6. 6Endokrinologikum Berlin, Berlin, Germany
  1. Correspondence to Dr Anna Moltó, Rheumatology B Department, Hopital Cochin, 27 rue du Faubourg Saint Jacques, Paris 75014, France; anna.molto{at}cch.aphp.fr

Abstract

Background The Assessment of Spondyloarthritis International Society (ASAS) criteria for axial spondyloarthritis (SpA) allows classification of patients with (‘imaging’ arm) and without (‘clinical’ arm) imaging abnormalities of the sacroiliac joints.

Objective To compare the phenotype of early axial SpA with regard to the two arms of the ASAS axial SpA criteria.

Methods Demographics, clinical and biological features of SpA, disease activity, severity parameters, and imaging abnormalities at the sacroiliac and spine levels were compared, in the two arms of the ASAS axial SpA criteria, in the patients of the French cohort of early SpA.

Results Of the 615 patients analysed, 435 (70.7%) met the ASAS criteria (262 (60.2%) and 173 (39.8%) in the imaging and clinical arms, respectively). There were no major differences in the characteristics of the two groups except that those in the imaging arm were more likely to be younger, male and have higher concentrations of C-reactive protein. Imaging abnormalities other than those meeting the ASAS criteria for the imaging arm (ie, x-ray-determined structural damage or MRI-revealed inflammatory changes in the sacroiliac joint (SIJ)) were observed (MRI–SIJ structural damage (55.0% vs 3.5%), MRI–spine inflammatory changes (35.1% vs 12.9%), MRI–spine structural damage (10.3% vs 5.3%) and x-ray–syndesmophytes (11.8% vs 5.3%)) in the imaging versus clinical arm, respectively.

Conclusions Our study confirms the external validity of the clinical arm of the ASAS criteria. It is notable that many patients in the clinical arm showed other imaging changes in SIJs and spine.

  • Ankylosing Spondylitis
  • Magnetic Resonance Imaging
  • Radiography

https://doi.org/10.1136/annrheumdis-2013-204262

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    The Assessment of Spondyloarthritis International Society (ASAS) has proposed a set of criteria1 for recognising patients with early axial spondyloarthritis (SpA). These criteria can be summarised in two main arms, which can both be applied to patients with chronic back pain starting before the age of 45 years:

    • The ‘imaging’ arm, in which a patient meets the criteria if an objective sign of inflammation (MRI)2 or structural damage (conventional pelvic x-ray analysis) is demonstrated in the sacroiliac joints (SIJs), together with a history or current symptoms of at least one feature suggestive of SpA (eg, inflammatory back pain (IBP), psoriasis, enthesitis, etc.)

    • The ‘clinical’ arm, in which a patient meets the criteria despite the lack of demonstration of an objective sign of inflammation on MRI or structural damage in the SIJs. In this case, the patient has to be HLAB27 positive and have a history or current symptoms of at least two features suggestive of SpA (eg, IBP, psoriasis, enthesitis, etc.)

    The validity of these criteria is still under debate both in terms of validity of the clinical arm and with regard to the imaging abnormalities that allow classification of a patient as meeting the criteria of the imaging arm.

    The ASAS criteria for axial SpA (ax-SpA), especially the clinical arm, have been externally validated in different SpA populations and clinical trials3–6 (eg, by evaluating the clinical presentation, the level of activity and/or severity of the disease, the treatment effect of drugs usually effective in radiographic spondyloarthritis), and also in terms of face validity (eg, by evaluating the percentage of patients with histological features suggestive of sacroiliitis despite the lack of imaging (either x-ray analysis or MRI) evidence of such sacroiliitis).7 However, the clinical arm is not well recognised by the different national and international healthcare systems; for example, in many countries, patients with active, severe ax-SpA that is refractory to non-steroidal anti-inflammatory drugs are not eligible for treatment with tumour necrosis factor (TNF) blockers if imaging investigations do not show any sign of sacroiliitis. Moreover, increased C-reactive protein (CRP) is sometimes required.

    Another aspect of the ASAS criteria that is currently under debate is the definition of imaging abnormalities. According to the published criteria, and in order to meet the criteria of the imaging arm, patients must have either obvious structural SIJ damage on pelvic x-ray analysis (eg, bilateral grade 2–4 or unilateral grade 3–4 of the modified New York criteria8) or active (acute) inflammatory lesions of the SIJs observed on pelvic MRI according to the ASAS/OMERACT definition.9

    However, there is increasing evidence that other imaging abnormalities might also be of clinical relevance for classifying a patient as having SpA. For example, structural SIJ damage might be more easily detected by either CT scan10 or MRI,11 ,12 but, because of the potential long-term risk of radiation exposure,13 MRI is the preferred technique. Another example is that, when these changes (eg, acute inflammation or structural damage) are observed at the spinal level, they might also be of relevance in the classification of a patient with symptoms suggestive of SpA, in particular when using MRI technology.14 ,15

    These preliminary observations prompted us to conduct an analysis of the data collected in patients with early IBP suggestive of SpA and participating in the ongoing French multicentre DESIR (acronym which stands in French for outcome of early undifferentiated spondyloarthritis) study with the following two main objectives: (a) to compare patient characteristics with regard to the arm (imaging vs clinical) of the ASAS criteria they meet; (b) to describe the prevalence of the different imaging abnormalities in the two arms of the ASAS criteria.

    Patients and methods

    Study design

    DESIR is a French prospective, multicentre, longitudinal study of patients with early IBP suggestive of SpA (clinicaltrials.gov NCT01648907).16

    This study followed the current Good Clinical Practice guidelines and was approved by the appropriate ethics committees. Participants gave their written informed consent. The website contains the detailed description of the centres, organisation of the cohort, and the full detailed protocol and case report form.17

    A total of 708 patients with early IBP were included (inclusion period October 2007–April 2010). Consecutive patients aged >18 years and <50 years with IBP involving the thoracic or lumbar spine or buttock area for >3 months but <3 years and symptoms suggestive of a diagnosis of SpA (score ≥5 on a numerical rating scale of 0–10 where 0=not suggestive and 10=very suggestive of SpA) were included in the DESIR cohort. Patients had to meet the IBP criteria of Calin et al18 or the Berlin criteria.19 Patients with a definite diagnosis of non-SpA back pain, conditions that might interfere with the validity of informed consent and/or prevent optimal compliance (eg, alcoholism, psychiatric disorders), or a history of treatment with TNF blockers were excluded. For this study, analysis included the whole of the DESIR cohort, and used the dataset locked on 12 December 2011.

    Data collected

    The data collected comprised both patient demographics and clinical presentation of the disease. Demographics included age, gender and body mass index. All items required to adequately classify a patient according to the ASAS criteria were collected. The activity of the disease was evaluated using BASDAI (Bath Ankylosing Spondylitis Disease Activity Index)20 and ASDAS-CRP (Ankylosing Spondylitis Disease Activity Score–CRP).21 The severity of the disease was assessed using BASFI (Bath Ankylosing Spondylitis Functional Index)22 and BASMI (Back Ankylosing Spondylitis Metrology Index).23 Finally, quality of life was evaluated according to the Short Form 36 Health Survey Questionnaire (SF36).24

    To ensure the quality and standardisation of the images collected, a specific written procedure was given to each participating centre. Conventional x-ray analysis of the cervical spine, lumbar spine and pelvis was performed. Radiologists or rheumatologists at each study centre scored each SIJ as follows: 0=normal; 1=doubtful; 2=obviously abnormal; 3=fused. For the present analysis, SIJs were considered abnormal if at least one was scored 2 or 3. This scoring method, used by local investigators in DESIR, is derived from the modified New York criteria for radiographic sacroiliitis changes8 with one modification: grades 2 and 3 of the New York criteria were pooled to make one combined grade.

    The modified Stoke Ankylosing Spondylitis Spine Score (mSASSS)25 was calculated from conventional x-rays of the cervical and lumbar spine. Definite radiographic damage was defined as an mSASSS score of ≥2 at at least one vertebral edge of each patient, representing the appearance of at least one syndesmophyte in that patient.

    MRI scans of the SIJs, upper spine (C2 to T10) and lower spine (T8 to S1) were performed using short-tau inversion recovery and T1 fast spin echo acquisitions. A contrast product was not used.

    The presence of inflammatory and structural damage at the SIJs and spine was assessed by radiologists or rheumatologists at each study centre. Inflammatory changes in the SIJs were defined as the presence of bone oedema. Structural SIJ damage was defined as the presence of clear characteristic lesions such as sclerosis, erosions, bone bridges or ankylosis. The spine was evaluated at three different levels (cervical/thoracic/lumbar), and the presence of either inflammatory (defined as the presence of bone oedema/with contrast enhancement at the entheseal site at vertebral corners or the whole vertebrae, with/without disc involvement) or structural (defined as the presence of sclerosis, erosions or vertebral syndesmophytes) damage was separately assessed at each of these three levels. For each MRI evaluation, radiologists or rheumatologists at each study centre recorded scores as follows: 0=normal; 1=doubtful; 2=abnormal. For this analysis, the MRI finding was considered abnormal only if scored as ‘abnormal’ by a rheumatologist or radiologist.

    DESIR definitions for MRI involvement are similar to, but not identical to, the ASAS/OMERACT definitions for MRI sacroiliitis/MRI spinal involvement in SpA,9 ,26 because the DESIR study was designed before the publication of the ASAS/OMERACT definitions.

    Statistical analysis

    The first step consisted of classifying each patient according to the ASAS criteria for ax-SpA, resulting in the following three categories: patients meeting, or not, the ASAS criteria, and, for those who did not meet the criteria, whether the abnormal image findings permitted classification of the patient in the imaging arm. If they did not, patients were classified in the clinical arm if HLAB27 was positive and two features suggestive of SpA were present.1 For this purpose, we excluded patients who had data missing, preventing us from adequately categorising them into a specific arm of the ASAS criteria for ax-SpA.

    The second step consisted of comparing the patient characteristics according to the arm of the criteria that they met (eg, imaging vs clinical). Categorical variables were compared using the χ2 test (or Fisher exact test as applicable), while continuous variables were compared using the Student T test (the non-parametric Wilcoxon test as applicable).

    Because different scenarios can be observed according to the imaging modalities in the imaging arm and according to the CRP status in the clinical arm, we performed a descriptive analysis in five different subgroups: (1) x-ray-determined definite SIJ damage and MRI inflammatory changes in the SIJ; (2) x-ray-determined definite SIJ damage and normal SIJ on MRI; (3) SIJ normal on x-ray analysis and MRI inflammatory changes in the SIJ; (4) SIJ normal on x-ray analysis and MRI, and CRP abnormal; (5) SIJ normal on x-ray analysis and MRI, and CRP normal (where abnormal CRP was defined as >6 mg/L).

    The third step consisted of evaluating other (not included in the ASAS criteria for ax-SpA) imaging findings suggestive of SpA (eg, MRI-determined structural damage of the SIJ, MRI-determined inflammatory and structural damage at the spine level, and the presence of at least one syndesmophyte at the cervical or lumbar level) observed in the different arms of the ASAS ax-SpA criteria. We then estimated the concordance of the abnormal imaging findings observed with the x-ray and MRI modalities using a κ coefficient of concordance (eg, at the SIJ level between the pelvic x-ray grades 0–1 (normal or doubtful)/2–3 (abnormal or partially fused) vs MRI grades 0–1 (normal or doubtful)/2 (abnormal) of structural damage; at the spine level between spine x-ray (mSASSS ≥2 at at least one vertebral edge, yes/no (cervical or lumbar)) vs spine MRI grades 0–1 (normal or doubtful)/2 (abnormal) of structural damage at at least one of the three levels (cervical/thoracic/lumbar)).

    Results

    Classification of patients according to the ASAS criteria and relating to the two arms of the ASAS criteria

    Figure 1 summarises the flowchart of the recruited patients. Because of missing data, the fulfilment (or not) of the ASAS criteria was assessed in 615 of the 708 patients in the DESIR cohort. Of these 615 patients, 435 met the ASAS criteria: 262 and 173 met the criteria for the imaging and clinical arms, respectively. Within the imaging arm, 126, 47 and 89 patients belonged to the ‘x-ray definite SIJ damage/MRI inflammatory changes in the SIJ’, ‘x-ray definite SIJ damage/MRI SIJ normal’ and ‘x-ray SIJ normal/MRI inflammatory changes in the SIJ’ subgroups, respectively. Thus, of the patients in the imaging arm, 66.0% could be classified as having radiographic ax-SpA, and 34.0% as having non-radiographic ax-SpA. In the clinical arm (eg, ‘x-ray SIJ normal/MRI SIJ normal’), 32 (18.5%) had abnormal CRP levels, and 138 (79.8%) had normal CRP levels. For three patients, the available data allowed them to be classified in the clinical arm despite the absence of CRP data; however, because of the missing data, they were excluded from the subgroup analysis.

    Figure 1
    Figure 1

    Distribution of the 708 patients recruited in the DESIR cohort according to the axial Assessment of Spondyloarthritis International Society (ASAS) criteria.

    Imaging versus clinical arm

    Table 1 summarises the comparison of the patient (age, gender, B27 positivity) and disease (clinical presentation, disease activity and severity) characteristics fulfilling the two arms of the ASAS criteria for ax-SpA. No differences were found between the groups except that those in the imaging arm were younger, more likely to be male and had higher CRP concentrations.

    View this table:
    Table 1

    Comparison of patient and disease characteristics of early axial spondyloarthritis according to the arm (imaging vs clinical) of the ASAS criteria they met

    Comparison of the five subgroups according to imaging and/or CRP abnormalities

    A descriptive analysis was performed (summarised in table 2) in the five different subgroups according to imaging and/or CRP abnormality. Patients in the ‘x-ray definite SIJ damage/MRI inflammatory changes in the SIJ’ subgroup were younger (mean±SD 29.3±6.7 years) than those in the other subgroups. Interestingly, BASDAI was strikingly higher in the ‘abnormal CRP’ subgroup of the clinical arm (57.3±17.2) than in any of the other subgroups. CRP levels were higher in the ‘abnormal CRP’ subgroup than in any of the subgroups of the imaging arm.

    View this table:
    Table 2

    Comparison of patient and disease characteristics of early axial spondyloarthritis according to the ASAS criteria arms (imaging vs clinical) and subarms (x-rays vs CRP) they were fulfilling

    Concerning the structural damage (presence of structural damage, yes/no) of the SIJs and spine, the concordance between MRI and x-ray findings was very low at both the SIJ (κ 0.55 (0.49–0.61)) and spine (0.18 (0.06–0.31)) level (tables 3 and 4).

    View this table:
    Table 3

    Concordance between MRI and x-ray findings on the structural damage of sacroiliac joints (SIJs)

    View this table:
    Table 4

    Concordance between MRI and x-ray findings on the structural damage of the spine

    Other imaging abnormalities

    Table 5 summarises the other imaging findings observed in the five subgroups as previously described. MRI structural damage of the SIJs was, as expected, more common in the subgroup of patients with x-ray-determined damage (65.3%), but, more interestingly, also in 3.5% patients of the clinical arm. MRI-determined inflammatory changes in the spine were more common in the presence of other markers of inflammation (eg, local MRI inflammatory changes in the SIJs (38.6%) or abnormal CRP (21.9%)). Furthermore, in the subgroups without x-ray-determined damage of the SIJs, there was evidence of x-ray-determined damage of the spine in 6.7% of the subgroup ‘x-ray SIJ normal/MRI inflammatory changes in the SIJ’ and 9.4% of the subgroup ‘x-ray SIJ normal/MRI SIJ normal/CRP abnormal’.

    View this table:
    Table 5

    MRI and x-ray findings on spine and sacroiliac joints (apart from those included in the ASAS criteria) in patients with early axial spondyloarthritis

    Discussion

    This analysis of the DESIR cohort allowed us to evaluate potential differences in the clinical presentation of SpA with regard to the different arms of the ASAS criteria they met, in a population of patients with IBP suggestive of SpA. Patients in the DESIR cohort did not have to meet any particular set of criteria, other than to present with IBP for >3 months and <3 years, before the age of 50, and to have a confident physician diagnosis of SpA (above 50%, ie >5 on a 0–10 scale, where 0=no SpA and 10=definite diagnosis of SpA). Only after inclusion in the study were the different sets of criteria applied on the basis of data collected during the first visit.

    Comparison of the patients in the imaging and clinical arms showed that the clinical features (eg, peripheral arthritis, dactylitis, uveitis, psoriasis) and most parameters evaluating the activity (eg, BASDAI), severity (eg, BASFI, BASMI) and impact of the disease in terms of quality of life (eg, SF36) were identical in the two groups.

    Furthermore, this study confirms the presence of structural damage both at the spine and SIJ level and inflammatory lesions of the spine in a small proportion of patients in the clinical arm of the ASAS criteria.

    This study has some weaknesses but also some strengths. First, because of missing data, we were unable to evaluate whether ASAS criteria were met in 26 patients (eg, 3.7%). This raises the question of how to handle the missing items of the ASAS criteria, in particular concerning the B27 antigen and the imaging modalities. In some epidemiological studies, such missing items have been considered as negatives in the evaluation of the ASAS criteria.4 ,27 Because of the main objective of our study, we excluded patients with missing items that would not allow us to classify the patient according to the different arms of the ASAS criteria.

    Second, the technique for evaluating the imaging modalities (eg, by each local participating investigator and not by a central reader) might be seen as a weakness, but this methodology could also be seen as a strength because it reflects daily practice. In any case, in the DESIR study, imaging modalities were standardised in terms of both image collection (eg, standardised written protocols) and evaluation (a specific case report form with a reminder of the definition of the abnormalities suggestive of SpA was provided), since the readers (either a rheumatologist or radiologist) had to complete a case report form as described in the Methods section.

    Another limitation is that the specificity of either arm of the ASAS criteria cannot be evaluated because of the lack of a control group; even though a group of patients in the DESIR cohort did not fulfil the ASAS criteria, they could not be used as a control population, as all patients in the DESIR cohort had to have a confident physician diagnosis of SpA as described above. Another limitation is the cross-sectional design of our study, with no gold standard for the diagnosis of SpA.

    However, our multicentre study also has some strengths. First, our analyses were performed on a large number of patients with IBP suggestive of SpA (N=682), ensuring a good representation of early SpA from a western European country.

    As previously reported, the similarity of the clinical disease manifestations between the patients with regard to the arm of the ASAS criteria they met is a strong argument in favour of the validity of such criteria. Yet, there were also differences between the two arms with respect to age, gender and elevated CRP, which may be have relevance for disease progression, for example.

    Our findings on the prevalence of other imaging abnormalities in the clinical arm of the ASAS criteria raises the question of the potential need to revisit these criteria when conducting clinical epidemiological studies/trials, and also the question of MRI and radiographic investigation of patients presenting with symptoms suggestive of SpA in daily practice. However, these results have to be carefully interpreted, and will need further validation, as the prevalence of these abnormalities in patients without SpA or in a normal population has not been reported so far. Long-term longitudinal evaluation of the patients enrolled in the DESIR study and/or other ongoing studies should permit us to confirm, or not, our findings.

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    Footnotes

    • Handling editor Tore K Kvien

    • Contributors All authors collaborated in the conception and design of the study, or analysis and interpretation of data, revising the manuscript critically for important intellectual content, and gave final approval of the version to be published. AM drafted the article.

    • Funding DESIR is financially supported by unrestricted grants from both the French Society of Rheumatology and Pfizer Ltd France. This study financially supported by a Pfizer grant. The funders had no role in the study design, data collection, analysis, decision to publish or preparation of the manuscript.

    • Competing interests None.

    • Ethics approval Local ethics committee.

    • Patient consent Obtained.

    • Provenance and peer review Not commissioned; externally peer reviewed.