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Imaging in Ankylosing Spondylitis: Mikkel Østergaard and Robert G.W. Lambert
Imaging in Ankylosing Spondylitis: Mikkel Østergaard and Robert G.W. Lambert
2012
TAB441759720X11436240M Østergaard and RGW LambertTherapeutic Advances in Musculoskeletal Disease
DOI: 10.1177/
1759720X11436240
Mikkel Østergaard and Robert G.W. Lambert
© The Author(s), 2012.
Reprints and permissions:
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Abstract: Imaging is an integral part of the management of patients with ankylosing spondylitis journalsPermissions.nav
and axial spondyloarthritis. Characteristic radiographic and/or magnetic resonance imaging
(MRI) findings are key in the diagnosis. Radiography and MRI are also useful in monitoring
the disease. Radiography is the conventional, albeit quite insensitive, gold standard method
for assessment of structural damage in spine and sacroiliac joints, whereas MRI has gained
a decisive role in monitoring disease activity in clinical trials and practice. MRI may also, if
ongoing research demonstrates a sufficient reliability and sensitivity to change, become a new
standard method for assessment of structural damage. Ultrasonography allows visualization
of peripheral arthritis and enthesitis, but has no role in the assessment of axial manifestations.
Computed tomography is a sensitive method for assessment of structural changes in the spine
and sacroiliac joints, but its clinical utility is limited due to its use of ionizing radiation and lack
of ability to assess the soft tissues. It is exciting that with continued dedicated research and the
rapid technical development it is likely that even larger improvements in the use of imaging may
occur in the decade to come, for the benefit of our patients.
Introduction This paper describes the virtues of CR and its Correspondence to:
Mikkel Østergaard, MD,
Imaging in ankylosing spondylitis (AS) has current major importance in diagnosis and fol- PhD, DMSc
been synonymous for decades with conventional low-up of AS, but also, by putting emphasis on Department of
Rheumatology, Copenhagen
radiography (CR). However, developments in MRI, stresses that AS management has entered a University Hospital at
computed tomography (CT), ultrasonography time of exciting and expanding therapeutic as well Glostrup, Nordre Ringvej
57, DK-2600 Glostrup,
(US) and particularly magnetic resonance imag- as imaging possibilities. Denmark
ing (MRI) have dramatically increased the amount mo@dadlnet.dk
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Therapeutic Advances in Musculoskeletal Disease 4 (4)
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M Østergaard and RGW Lambert
vertebral margins. This observation is much eas- Enthesitis at the interspinous and supraspinous
ier to make in the lumbar spine where normal ver- ligamentous attachments is very common with
tebrae are always concave anteriorly in comparison bone formation causing whiskering and inters-
to the thoracic and cervical spine where the nor- pinous ankylosis.
mal contour is much more variable and may be
square or occasionally convex.
Use in diagnosis, monitoring and prognostication
The hallmark of spinal disease in AS is the devel- Diagnosis. While the modified New York Crite-
opment of characteristic bony spurs: syndesmo- ria are actually classification criteria, these criteria
phytes (Figure 1). These start as thin vertically are the most commonly used criteria for the diag-
oriented projections of bone that develop due to nosis of AS and are based on clinical features and
ossification within the outer fibres of the annulus radiographic sacroiliitis [van der Linden et al.
fibrosus of the intervertebral disc. Syndesmophytes 1984]. According to these criteria AS may be
are radiographically visible on the anterior and diagnosed if, in addition to one clinical criterion
lateral aspects of the spine starting from the cor- being present, grade 2 sacroiliitis (minimal sacroi-
ner of the vertebra. liitis: loss of definition of the joint margins, mini-
mal sclerosis, joint space narrowing and erosions)
Traditional literature indicates that all of the early or higher occurs bilaterally, or grade 3 (moderate
signs of spinal involvement are most often visual- sacroiliitis: definite sclerosis on both sides of the
ized first near the thoracolumbar junction. While joint, erosions, and loss of joint space) or grade 4
this may be true for radiography, MRI studies (complete bony ankylosis) occurs unilaterally [van
show a predilection for early involvement of the der Linden et al. 1984]. Owing to the requirement
midthoracic spine. Both modalities would agree for these radiographic structural changes, the
that the cervical spine is rarely affected first and duration of disease before diagnosis has been a
spinal disease rarely occurs in the absence of sig- median of 7–10 years [Feldtkeller et al. 2003]. The
nificant SI joint involvement. definitions of radiographic changes according to
the New York Criteria are included in the Assess-
Progressive growth of syndesmophytes will bridge ment of Spondyloarthritis International Society
the intervertebral disc causing ankylosis (Figure 1) (ASAS) classification criteria for SpA [Rudwaleit
and extensive bone formation produces a smooth, et al. 2009b], the European Spondyloarthritis
undulating spinal contour: the ‘bamboo spine’. Study Group (ESSG) criteria for spondyloarthri-
The syndesmophytes that characterize AS must be tis [Dougados et al. 1991] and in the modified
differentiated from other spinal and paraspinal New York Criteria [van der Linden et al. 1984].
bone formation. Degenerative bony spurring in
spondylosis deformans arises several millimetres Monitoring. Radiography of the spine is not
from the discovertebral junction, is typically trian- included in the classification criteria but may be
gular in shape and has a horizontally oriented useful to follow structural disease progression in
segment of variable length at the point of origin. patients with spinal involvement. The bone
In diffuse idiopathic skeletal hyperostosis (DISH), changes seen in patients with axial SpA develop
bone formation in the anterior longitudinal liga- slowly and are often not present in patients with
ment results in a flowing pattern of ossification early disease, and generally only minor changes
that is usually thick and the sacroiliac joints are can be observed in 1–2 years. Different scoring
not involved. methods, all based on assessment of lateral views,
have been developed to quantify changes in the
Erosion of the vertebral endplate is common in spine of patients with AS: the Stoke AS Spine
later stages of AS and may be focal or diffuse. It Score (SASSS), Bath AS Radiology Index
is also seen when pseudarthrosis develops follow- (BASRI) and the modified Stoke AS Spine Score
ing a fracture in a previously ankylosed spine. (mSASSS). A comparative study of the three
Changes in the apophyseal joints are common methods concluded that all measures were reli-
and start with of ill-defined erosion and sclerosis able but mSASSS was more sensitive to change
but may be hard to see. Capsular ossification or [Wanders et al. 2004]. These spine scores are pri-
intra-articular bony ankylosis frequently occurs marily used in clinical research.
in late disease. The ankylosed spine is very sus-
ceptible to fractures, which should always be sus- Prognostication. The amount of data document-
pected in case of unexplained pain exacerbations. ing a prognostic value of CR findings is limited.
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Therapeutic Advances in Musculoskeletal Disease 4 (4)
However, low-grade (grade 1) sacroiliitis has been free from superimposition of overlying
shown to have predictive value for the development structures.
of AS [Huerta-Sil et al. 2006], and the severity of
radiographic damage has been documented to be In AS, the pathological processes start in bone
related to subsequent radiographic damage pro- marrow and at sites of entheses. However, CT has
gression [Maksymowych et al. 2010a; Poddubnyy poor ability to detect soft-tissue change and is
et al. 2011]. usually normal until structural damage is present.
CT can detect osteoporosis or osteosclerosis quite
well but these changes are very nonspecific. New
Computed tomography bone formation is also well visualized in the form
of syndesmophytes, ligamentous ossification and
Technical aspects periarticular and intra-articular ankylosis, but the
Developments in computing and engineering use for CT in this regard is limited. The primary
have resulted in remarkable changes in the CT value of CT in AS is its ability to detect and clearly
technology in the last decade. CT offers fast and define erosion of bone at any joint or enthesis,
reliable acquisition, high resolution and multipla- and for documenting fractures.
nar capabilities that have enhanced its use in
recent years, although the soft-tissue contrast is
still limited. Use in diagnosis, monitoring and
prognostication
Although CT image acquisition is restricted to Diagnosis. The diagnosis of AS is primarily
the axial plane of imaging, the ability to acquire based on the radiographic observation of bilateral
isotropic voxels has resulted in reliable and versa- moderate or unilateral severe sacroiliitis. When
tile multiplanar capabilities so that many CT good quality radiographs of the sacroiliac joints
scans of the body are now interpreted primarily are normal or radiographic changes meet diag-
from coronal or sagittal images in the same way nostic criteria, there is no role for CT. Early detec-
as MRI. The data acquisition is so fast that patient tion of AS is better investigated by MRI and if
motion is rarely a problem as CT scans are now clearly defined structural damage is present on
routinely acquired in few seconds. In fact CT is CR, then there is no additional diagnostic utility
often faster than taking multiple radiographs. for CT. However, CT of the sacroiliac joints is
Complex requirements for patient positioning in much easier to interpret than radiography which
musculoskeletal CT are now substantially less is notoriously subject to poor observer reliability.
important as the majority of studies can be recon- When the radiographic findings are unclear, CT
structed in orthogonal planes. Patient tolerance is will usually resolve this uncertainty. Since CT
excellent and, unlike MRI, there are no absolute shows bone erosion in exquisite detail, CT may
contraindications to CT. Spatial resolution is also have a role to play in the further investigation
high, usually higher than MRI, and contrast reso- of MRI equivocal findings. It should be noted
lution between soft tissue and bone is unsur- that classification criteria for AS depend on radio-
passed by any other modality. However, despite graphic findings and more recently MRI, but not
all of the advantages listed above, the application CT specifically. In the spine, CT is useful in the
of CT will remain somewhat limited, because the diagnosis of complications of late disease such as
soft-tissue contrast is inferior to MRI and US spondylodiscitis or spinal fracture when patients
and ionizing radiation is used. Radiation dose may be unable to tolerate MRI due to pain or spi-
increases with the requirements for spatial detail nal deformity.
and the depth of the body part, which is consider-
able for the sacroiliac joint and spine. Monitoring disease activity and damage. CT has
no useful role in monitoring disease activity or
damage. CT cannot show active inflammation
Ankylosing spondylitis/axial and the relatively high radiation dose of CT pre-
spondyloarthritis cludes its routine use for assessment of damage
CT allows visualization of the same pathologi- progression.
cal processes as CR (erosion, osteoporosis /
sclerosis, and new bone formation/ankylosis) Prognostication. The prognostic value of CT
with the added benefit of multiplanar imaging findings of sacroiliitis require further investigation.
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Figure 4. Bone marrow oedema in the transverse processes, costovertebral joints and manubriosternal joint.
MRI of the cervical and upper thoracic spine of a 29-year-old male patient scans were performed before (A–B and
D–E) and 3 months after (C and F) initiation of anti-TNF therapy. Sagittal slices lateral to the spinal canal are shown.
(A)–(C) Sagittal slice through the pedicle and the lateral parts of the vertebrae, shows moderate bone oedema
on the baseline STIR image (B) in the posterolateral aspects of all of the thoracic vertebral bodies, most
pronounced at T4 and T5. The distribution is typical for inflammation on the vertebral side of the costovertebral
joints. Also note inflammation in the manubriosternal joint anteriorly (arrow). Most foci of inflammation are
still faintly visible after anti-TNF therapy (C), but are clearly less intense.
(D)–(F) Far lateral slice through the transverse processes and ribs. Intense bone marrow oedema is seen in
the transverse processes of the upper thoracic spine (E; arrows), which resolves completely with treatment.
This pattern of bone marrow oedema in the transverse processes, costovertebral joints and manubriosternal
joint are pathognomonic of spondyloarthritis.
criteria, would improve the diagnostic utility of be assessed in a sensitive manner by biochemical
MRI [Weber et al. 2010a, 2010b]. However, (mainly C-reactive protein [CRP]) or physical
ASAS in January 2011 decided to await further evaluation.
data before considering revision of the definition
of a positive MRI in the axial SpA criteria. Several systems for assessment of disease activity
in the sacroiliac joints and in the spine have been
Monitoring disease activity and damage. MRI proposed (see a recent review by Østergaard et al.
can provide objective evidence of currently active [2010] for details). Reproducible and responsive
inflammation in patients with SpA (Figure 4) methods are available [Lukas et al. 2007].
[Hermann and Bollow, 2004; Maksymowych and The sensitivity to change and discriminatory
Landewe, 2006]. Until the introduction of MRI, ability of the three most used spine scoring sys-
disease activity assessment was restricted to tems (The Ankylosing Spondylitis spine Magnetic
patient-reported outcomes, such as the Bath Anky- Resonance Imaging-activity [ASspiMRI-a] score,
losing Spondylitis Disease Activity Index (BAS- the Berlin modification of the ASspiMRI-a score
DAI) and Bath Ankylosing Spondylitis Functional and the Spondyloarthritis Research Consortium
Index (BASFI), because disease activity could not of Canada [SPARCC] scoring system) [Braun
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Therapeutic Advances in Musculoskeletal Disease 4 (4)
Figure 5. Progression of structural damage in the spine in ankylosing spondylitis, visualized by MRI.
T1-weighted MRIs of the thoracolumbar spine with a 3-year interval in a baseline (A) 23-year-old male with
established ankylosing spondylitis. The follow-up MRI (B) demonstrates new anterior ankylosis at T9/10 with
bridging anterior syndesmophytosis containing marrow fat signal. Note also several other findings indicating the
progression of structural damage: the intervertebral disc at T10/11 is completely fused on the second scan; a
new endplate defect has appeared at the inferior endplate of T9 with new fat infiltration; and the signal within the
T8/9 disc has increased suggesting progression of disc ossification.
Table 1. Magnetic resonance imaging definitions of inflammatory and structural lesions in axial
spondyloarthritis (by Canada-Denmark MRI Working Group and MORPHO group [Lambert et al. 2009;
Østergaard et al. 2009; Weber et al. 2010a, 2010b]).
A. Inflammatory lesions
Bone marrow oedema: Increase in bone marrow signal* on STIR images.
B. Structural lesions
Bone erosion: Full-thickness loss of dark appearance of the cortical bone and change in normal bright
appearance of adjacent bone marrow on T1-weighted images**
Fat infiltration: Focal increased signal in bone marrow on T1-weighted images**.
Bone spur: Bright signal on T1-weighted images extending from the vertebral endplate towards the
adjacent vertebra (spine)
Ankylosis: Bright signal on T1-weighted images extending across the sacroiliac joints or extending from
one vertebra being continuous with the adjacent vertebra (spine)
*Reference point for bone marrow signal on STIR images: sacroiliac joints, the centre of the sacrum at the same craniocaudal
level; spine, the centre of the vertebra, if normal; if not normal, the signal in the centre of the closest available normal vertebra.
**Reference point for bone marrow signal on T1-weighted images: sacral bone, the centre of the sacrum at the same
craniocaudal level; iliac bone, normal iliac marrow at the same craniocaudal level; spine, the centre of the vertebra, if normal;
if not normal, the signal in the centre of the closest available normal vertebra.
et al. 2003; Haibel et al. 2006; Maksymowych MRI is much less established for assessment of
et al. 2005] have been demonstrated in clinical structural changes (often referred to as chronic
trials, and they have been tested against each changes) than inflammatory changes. Since MRI
other by the ASAS/OMERACT MRI in AS undoubtedly provides otherwise inaccessible
group [Lukas et al. 2007]. All methods were fea- information on inflammatory activity, just ‘equal-
sible, reliable, sensitive to change and discrimi- ity’ of MRI with radiography concerning struc-
native. The SPARCC method had the highest tural damage assessment is a step forward, because
sensitivity to change, as judged by Guyatt’s effect radiography, and the ensuing need for two exami-
size, and the highest reliability as judged by the nations and exposure to ionizing radiation, could
inter-reader intraclass correlation coefficient then be avoided. Scoring methods assess erosions,
(ICC) [Lukas et al. 2007]. sclerosis, fat deposition and/or bone bridges
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M Østergaard and RGW Lambert
Table 2. Practical use of imaging of axial joints in AS and axial SpA.
separately or as global score [Braun et al. 2003; strong predictor of future AS, whereas mild or no
Madsen and Jurik, 2010b; Østergaard et al. 2009]. sacroiliitis, irrespective of HLA-B27 status, was a
The validation of the methods for damage assess- predictor of not developing AS [Bennett et al.
ment is limited and their value is not yet clarified. 2008]. Data on the value of MRI for predicting
therapeutic response in SpA are very limited.
Prognostication. Several published spine studies A high spine MRI inflammation score and short
have documented an association between the disease duration have been reported as statisti-
presence of bone marrow oedema at the anterior cally significant predictors of clinical response
corners of the vertebrae on MRI and subsequent (BASDAI improvement >50%) to anti-TNF ther-
development of syndesmophytes on radiography apy [Rudwaleit et al. 2008]. Further and larger
after 2 years of follow up. Presence as opposed to studies are needed to clarify the role of MRI in
absence of MRI anterior inflammation provides the prediction of disease course and therapeutic
relative risks of 3–5 for a new anterior radio- response.
graphic syndesmophyte at that level [Baraliakos
et al. 2008; Maksymowych et al. 2009; Pedersen
et al. 2011]. In two studies, the association was Conclusion
even more pronounced in those vertebral corners Imaging is an integral part of the management of
in which the inflammation had resolved following patients with AS and axial SpA (Table 2).
institution of anti-TNF therapy, possibly explained Characteristic radiographic and/or MRI findings
by tumour necrosis factor (TNF) in an active are key in the diagnosis, and these modalities are
inflammatory lesion restricting new bone forma- also useful in monitoring the disease. CR is the
tion, whereas reduction of TNF by applying a conventional, albeit quite insensitive, gold stand-
TNF-antagonist allows tissue repair to manifest ard method for assessment of structural damage
as new bone formation [Maksymowych et al. in spine and sacroiliac joints, whereas MRI has
2009; Pedersen et al. 2011]. A very recent study developed a decisive role in monitoring disease
has demonstrated that fat infiltrations in vertebral activity in clinical trials and practice. MRI may
corners increase the risk of subsequent radio- also, if ongoing research demonstrates a sufficient
graphic syndesmophyte formation [Chiowchan- reliability and sensitivity to change, become a new
wisawakit et al. 2011], bearing very interesting standard method for assessment of structural
implications for fat infiltration (which can be damage. It is exciting that with continued dedi-
easily recognized and reliably scored by MRI cated research and the rapid technical develop-
[Chiowchanwisawakit et al. 2009, 2011]), as a ment it is likely that even larger improvements in
potentially valuable surrogate marker for new the use of imaging may occur in the decade to
bone formation in AS. This, however, needs to be come, for the benefit of our patients.
investigated in further longitudinal studies.
Funding
One study suggests that in early inflammatory This research received no specific grant from any
back pain, severe sacroiliac MRI bone marrow funding agency in the public, commercial, or
oedema together with HLA-B27 positivity is a not-for-profit sectors.
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Therapeutic Advances in Musculoskeletal Disease 4 (4)
Conflict of interest statement Gandjbakhch, F., Terslev, L., Joshua, F., Wakefield,
The authors declare no conflicts of interest in R.J., Naredo, E., d'Agostino, M.A. et al. (2011)
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Haibel, H., Rudwaleit, M., Brandt, H.C.,
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