Inflammatory and chronic structural changes are objective signs of axial spondyloarthritis. In the sacroiliac joints (SIJs), inflammation (sacroiliitis) can be visualized as bone marrow edema, whereas chronic structural changes are visualized as fat metaplasia, erosions, sclerosis, or ankylosis in the area of the SIJ. In the spine, bone marrow edema in the vertebral bodies represents spondylitis but can also affect the facet and the costovertebral and costotransverse joints (arthritis), whereas structural changes are visualized as fat metaplasia, sclerosis or syndesmophytes and ankylosis at the vertebral edges.
Key points
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For visualization of inflammatory activity in the sacroiliac joints and the spine in axial spondyloarthritis, MRI is considered the best available imaging technique. MRI, together with conventional radiographs and computed tomography, is able to visualize chronic structural changes.
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Inflammatory changes represent bone marrow edema and are identified as sacroiliitis, whereas chronic structural changes may be seen as erosion, fat metaplasia, sclerosis, or new bone formation in both the sacroiliac joints and the spine.
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Several validated scoring methods exist for quantification of both inflammatory and chronic structural changes when using MRI and conventional radiographs.
Inflammatory and chronic structural changes are objective signs of axial spondyloarthritis (axSpA). In the sacroiliac joints (SIJs), inflammation (sacroiliitis) can be visualized as bone marrow edema, whereas chronic structural changes are visualized as fat metaplasia, erosions, sclerosis, or ankylosis in the areas around the SIJ. In the spine, bone marrow edema in the vertebral bodies represents spondylitis but can also affect the facet and the costovertebral and costotransverse joints (arthritis), whereas structural changes are visualized as fat metaplasia, sclerosis, or ankylosis of the vertebral edges.
MRI is the best imaging method for visualization of active inflammatory changes and for fat metaplasia, whereas structural changes such as erosions and sclerosis are seen better on computed tomography (CT) or on MRI but less well on conventional radiographs. However, radiographs are still considered the gold standard for visualization of new bone formation and ankylosis. CT is even better for the detection of erosions and bone formation, but both techniques are unable to visualized inflammation.
In daily practice, recognition of imaging findings is used for diagnosing patients with axSpA, but a quantification of these lesions is not necessary. Furthermore, measurement of the magnitude of pathologic changes in the axial skeleton of patients with spondyloarthritis is used in clinical trials for studying the natural course of the disease or for the efficacy of antiinflammatory drugs or biologics on the possible inhibition or deceleration of new bone formation. For this purpose, different scoring systems have been developed and proposed for the quantification of lesions in both the SIJ and the spine in patients with axSpA. In addition to clinical parameters, the objective assessment of imaging outcomes provides important information on the efficacy of treatment in patients with axSpA.
Scoring of the sacroiliac joints
Conventional Radiographs
The quantification of structural changes in conventional SIJ radiographs has been used for the classification of patients with ankylosing spondylitis (AS); modified New York criteria were published in 1984. The semiquantitative method of quantification used in these criteria had already been proposed in 1966 ( Table 1 ). According to the modified New York criteria, a patient could be classified as having AS if the structural lesions on conventional radiographs were graded as at least 2 bilaterally or with a grade 3 ( Fig. 1 ) or grade 4 unilaterally, in addition to clinical symptoms such as inflammatory back pain and limitation of mobility in the spine and/or the thorax. The obvious limitation of these criteria is that clinicians have to wait for structural changes to occur; this has been considered unacceptable because of the long delay of up to 7 to 10 years for a diagnosis of AS. Therefore, new criteria and a new nomenclature have been developed and proposed by the Assessment in SpondyloArthritis international Society (ASAS).
| Grade | Definition of Radiographic Changes |
|---|---|
| 0 | Normal |
| 1 | Suspicious changes |
| 2 | Minimal abnormalities: small localized areas with erosion or sclerosis, without alteration in the joint width |
| 3 | Unequivocal abnormality: moderate or advanced sacroiliitis with 1 or more signs of erosions, sclerosis, widening, joint space narrowing, or partial ankylosis |
| 4 | Severe changes: total ankylosis |
MRI
The standard MRI orientation that has been used in most studies so far for quantification of SIJ changes is the semicoronal orientation (parallel to the axis of the sacral bone), although in some scoring systems the semiaxial orientation has also been proposed ( Table 2 ). For the assessment of inflammatory lesions, the use of short-tau inversion recovery (STIR) MRI sequences has been recommended ( Fig. 2 ), and contrast-enhanced fat-suppressed T1-weighted images can also be used for this purpose. For assessment of chronic/structural changes, the T1-weighted MRI sequences are better for this purpose ( Fig. 3 ). The slice thickness used for performance of the MRIs is usually 3 to 4 mm.
| Imaging Specifications | Leeds, | Puhakka et al, 2003 | Hermann et al, 2004 | SPARCC | Madsen & Jurik, 2010 | Berlin, |
|---|---|---|---|---|---|---|
| Imaging orientation and sequence | Semicoronal | Semicoronal and semiaxial | Semicoronal | Semicoronal | Semicoronal and semiaxial | Semicoronal |
| Pathologic lesions | BME only | BME, bone marrow enhancement, and joint space enhancement | BME and joint space edema | BME only | BME and bone marrow enhancement | BME |
| Assessment of SIJ by division in: | Quadrants | 4 areas: iliac and sacral side of cartilaginous and ligamentous joint portion | Quadrants | Quadrant in 6 most severely affected consecutive slices | 4 areas: iliac and sacral side of cartilaginous and ligamentous joint portion | Quadrants |
| Grading | Status: present/absent Change: −3 for improvement to +3 for deterioration or semiquantitatively (resolution, improvement, no change, new lesions) | BME: 0–3 in 4 areas per joint Bone marrow enhancement: 0–3 in 4 areas per joint 0–3: joint space enhancement per half joint | Edema in joint space: grade 1, BME: grade 2–4 | Present/absent: 0–1 High/low intensity: 0–1 Depth <1 cm/≥1 cm: 0–1 | BME: 0–3 BME intensity: +1 point BME enhancement: 0–3 BME intensity: +1 point Depth ≥1 cm and extension ≥1 cm 2 : +1 point | BME: 0–3 |
| Total score (range) | 0–24 | 0–60 | 0–32 | 0–72 | 0–40 (as a mean score of edema and enhancement) | 0–24 |
Assessment of inflammatory sacroiliac joint lesions by MRI
The currently available scoring systems for the assessment of inflammatory activity in the SIJ-MRIs are shown in Table 2 . These scoring systems divide the SIJ into quadrants that are first scored individually and are then summed up to a global SIJ score. Sacroiliac inflammation is quantified and scored based on the extension and intensity of the periarticular bone marrow edema detected. Of note, the periarticular soft tissues (ligamentous joint portion) and the area of the joint space are not included in any of the scoring systems. The most widely used scoring systems for quantification of both the inflammatory activity and also structural changes of the SIJ are the Berlin score and the Spondyloarthritis Research Consortium of Canada (SPARCC) score.
For assessment of bone marrow edema, the Berlin score considers all available MRI slices and evaluates the SIJ by addition of the scores that are derived by dividing the joints in quadrants. Inflammatory activity is considered when increased signal in the STIR (or T1-weighted, contrast-enhanced) sequence is visible. The score ranges from 0 to 4. In comparison, the SPARCC method focuses on only those 6 consecutive slices that show the highest activity. This method scores inflammation in a dichotomous way, considering the presence or absence as well as the signal intensity and extension of bone marrow edema.
A direct comparison of the available scoring methods has been performed. In a multireader experiment organized by ASAS/OMERACT (Outcome Measures in Rheumatology Clinical Trials) working group for MRI in AS, no significant differences between the two approaches was found. In addition, a simplified approach that evaluated the SIJs per joint in a score from 0 to 3 performed similarly well.
Assessment of structural sacroiliac joint lesions by MRI
The available scoring systems for assessment of structural lesions in the SIJ-MRIs are shown in Table 3 . For quantification of structural lesions, the Berlin score has been proposed to quantify fat metaplasia by a dichotomous approach (presence or absence of hyperintense signal on T1-weighted MRI), whereas the amount of erosion per SIJ was also assessed in a semiquantitative way. In another proposal, both the cartilaginous and the ligamentous joint portions are used for scoring of structural changes by grading both the area affected by fat metaplasia and also the severity of erosive changes based on the extent of the affected subcortical bone. Both scoring systems take the entire extent of the SIJ into account. In a more recently published scoring system by SPARCC, structural changes were scored on 5 consecutive slices through the SIJ starting from the transitional slice and assessing pathologic lesions in a dichotomous approach (present or absent).
| Imaging Specifications | Puhakka et al, 2003 | Hermann et al, 2004 | Madsen & Jurik, 2010 | Berlin, | SPARCC MRI SIJ Structural Score |
|---|---|---|---|---|---|
| Imaging orientation | Semicoronal and semiaxial | Semicoronal | Semicoronal and semiaxial | Semicoronal | Semicoronal |
| Pathologic lesions | Erosion, sclerosis, joint space width | Erosions, sclerosis, joint space width, bone bridging/ankylosis | Fat metaplasia, erosion | Fat metaplasia, erosion, sclerosis, ankylosis | Fat metaplasia, erosion, backfill, ankylosis |
| Assessment of SIJ by division in: | Quadrant | Joint | 4 areas: iliac and sacral side of cartilaginous and ligamentous joint portion | Quadrant | Fat metaplasia and erosion: quadrants Backfill and ankylosis: SIJ halves in 5 consecutive slices starting from the transitional slice and scrolling anteriorly |
| Grading | 0–3 for erosion, sclerosis, and joint space width separately | 0–4 per joint (global score) | Fat deposition: 0–3 + 1 point for depth (extension ≥1 cm) Erosion (only in cartilaginous part): 0–3 + point for partial or + 2 points for complete ankylosis | Fat metaplasia and erosions: 0–3 Sclerosis and ankylosis: 0–1 | All lesions: present/absent (0–1) |
| Total score (range) | 0–60 | 0–8 | 0–48 | 0–64 | 0–120 |
In contrast with the quantification of inflammatory activity, so far there has not been any attempt to compare the different scoring systems for structural lesions directly. Furthermore, these scoring systems have not been extensively used for study purposes. The main reasons for this are the still low reliability in scoring chronic changes of the SIJ in MRI examinations and also that most of the treatment compounds used in the respective studies have targeted the inflammatory and not the structural outcomes of the patients.
Scoring of the sacroiliac joints
Conventional Radiographs
The quantification of structural changes in conventional SIJ radiographs has been used for the classification of patients with ankylosing spondylitis (AS); modified New York criteria were published in 1984. The semiquantitative method of quantification used in these criteria had already been proposed in 1966 ( Table 1 ). According to the modified New York criteria, a patient could be classified as having AS if the structural lesions on conventional radiographs were graded as at least 2 bilaterally or with a grade 3 ( Fig. 1 ) or grade 4 unilaterally, in addition to clinical symptoms such as inflammatory back pain and limitation of mobility in the spine and/or the thorax. The obvious limitation of these criteria is that clinicians have to wait for structural changes to occur; this has been considered unacceptable because of the long delay of up to 7 to 10 years for a diagnosis of AS. Therefore, new criteria and a new nomenclature have been developed and proposed by the Assessment in SpondyloArthritis international Society (ASAS).
| Grade | Definition of Radiographic Changes |
|---|---|
| 0 | Normal |
| 1 | Suspicious changes |
| 2 | Minimal abnormalities: small localized areas with erosion or sclerosis, without alteration in the joint width |
| 3 | Unequivocal abnormality: moderate or advanced sacroiliitis with 1 or more signs of erosions, sclerosis, widening, joint space narrowing, or partial ankylosis |
| 4 | Severe changes: total ankylosis |
MRI
The standard MRI orientation that has been used in most studies so far for quantification of SIJ changes is the semicoronal orientation (parallel to the axis of the sacral bone), although in some scoring systems the semiaxial orientation has also been proposed ( Table 2 ). For the assessment of inflammatory lesions, the use of short-tau inversion recovery (STIR) MRI sequences has been recommended ( Fig. 2 ), and contrast-enhanced fat-suppressed T1-weighted images can also be used for this purpose. For assessment of chronic/structural changes, the T1-weighted MRI sequences are better for this purpose ( Fig. 3 ). The slice thickness used for performance of the MRIs is usually 3 to 4 mm.
| Imaging Specifications | Leeds, | Puhakka et al, 2003 | Hermann et al, 2004 | SPARCC | Madsen & Jurik, 2010 | Berlin, |
|---|---|---|---|---|---|---|
| Imaging orientation and sequence | Semicoronal | Semicoronal and semiaxial | Semicoronal | Semicoronal | Semicoronal and semiaxial | Semicoronal |
| Pathologic lesions | BME only | BME, bone marrow enhancement, and joint space enhancement | BME and joint space edema | BME only | BME and bone marrow enhancement | BME |
| Assessment of SIJ by division in: | Quadrants | 4 areas: iliac and sacral side of cartilaginous and ligamentous joint portion | Quadrants | Quadrant in 6 most severely affected consecutive slices | 4 areas: iliac and sacral side of cartilaginous and ligamentous joint portion | Quadrants |
| Grading | Status: present/absent Change: −3 for improvement to +3 for deterioration or semiquantitatively (resolution, improvement, no change, new lesions) | BME: 0–3 in 4 areas per joint Bone marrow enhancement: 0–3 in 4 areas per joint 0–3: joint space enhancement per half joint | Edema in joint space: grade 1, BME: grade 2–4 | Present/absent: 0–1 High/low intensity: 0–1 Depth <1 cm/≥1 cm: 0–1 | BME: 0–3 BME intensity: +1 point BME enhancement: 0–3 BME intensity: +1 point Depth ≥1 cm and extension ≥1 cm 2 : +1 point | BME: 0–3 |
| Total score (range) | 0–24 | 0–60 | 0–32 | 0–72 | 0–40 (as a mean score of edema and enhancement) | 0–24 |
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