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Imaging and scoring in ankylosing spondylitis

J. Braun1, W. Golder2, M. Bollow3, J. Sieper3, D. van der Heijde4

1
Rheumazentrum Ruhrgebiet, Herne, ABSTRACT ges visible in the spinal structures are
Germany; 2Department of Radiology and Ankylosing spondylitis (AS), the proto - relevant for outcome (X-rays, MRI)
3
Department of Gastroenterology and type of the spondyloarthritides (SpA), is and relevant for the assessment of dis-
Rheumatology, Klinikum Benjamin a disease subset but also a possible ease activity (MRI).
Franklin, Free University, Berlin, outcome of the SpA. Early diagnosis of
Germany; 4Department of Internal
sacroiliitis, the most frequent clinical Scoring of radiographs as an out-
Medicine, Division of Rheumatology,
University Hospital Maastricht, Maas- symptom often accompanied by inflam - come measure in AS
tricht, The Netherlands. matory back pain, and other inflamma - Radiographic evidence of sacroiliitis is
Please address correspondence to: tory lesions of the spine such as spon - a prerequisite for the classification cri-
Prof.Dr. Jrgen Braun, Rheumazentrum dylitis and spondylodiscitis, can be teria for AS according to almost all pro-
Ruhrgebiet, St. Josefs-Krankenhaus, visualized early by magnetic resonance posals and criteria published over the
44652 Herne, Germany. imaging (MRI). Chronic changes such last decades (1-5), with the exception
Clin Exp Rheumatol 2002; 20 (Suppl. 28): as syndesmophytes are well detected by of the ESSG criteria which concentrate
S178-S184. conventional x-rays of the spine, mostly on the characteristic clinical symptoms
Copyright CLINICAL AND EXPERIMEN- lateral, in the lumbar spine also a.p. and history of SpA (6). In contrast,
TAL R HEUMATOLOGY 2002. Active spinal inflammation can be changes on radiographs have not been
demonstrated by MRI by using either established as an important endpoint
Key words: Spondyloarthritides, the fat saturating STIR technique or by measure in AS to date. However, radio-
ankylosing spondylitis, spinal radio- application of the contrast agent gado - graphic changes in the spine, hips and
graphy, magnetic resonance imaging linium-DTPA. This is especially useful SI joints were selected as part of the
of the spine, methodology, AS out- in early and active disease, in young core set for endpoints in clinical trials
come parameter. women and in children, and for the dif - of DCART therapy (7).
ferential diagnosis of septic sacroiliitis. Radiographs in AS are a result of a
Because of the efficacy of the novel bio - cumulative process of destruction over
logic agents directed against TNF time and, thus, reflect the history of a
such as infliximab and etanercept in pathology. The radiographs in AS
SpA there is a need for spinal imaging change over time and, can be used to
techniques that are more sensitive than assess the serial evaluation of AS.
conventional x-rays. The available scor- Many different spinal structures are
ing tools are limited in their sensitivity involved in this process (Table I).
to change. Novel approaches using If the disease modification of drugs
MRI have been recently proposed. need to be assessed - and this is now
indeed needed for the obviously very
Introduction effective anti-TNF a gents (8) - demon-
Assessment of structural changes in stration of reduction or stopping of
ankylosing spondylitis (AS) is essential
for diagnosis, management (disease
activity) and outcome. The most impor- Table I. Ankylosing spondylitis related
tant locations in AS are the sacroiliac (radiographic) pathology in the spine and
joints and the spine. joints.
The magnitude of the structural chan-
Erosions
ges visible in the sacroiliac joints is rel- Sclerosis
evant for the diagnosis of AS according Joint space narrowing
to accepted criteria (conventional radi- Blurring of joint margins
ography), the measurement of disease Spurs
activity (sequential x-rays, magnetic (Pseudo)widening
resonance imaging (MRI)) and the dif- Complete and incomplete bony fusion
ferentiation towards undifferentiated Bony bridging
spondyloarthritis, septic sacroiliitis, Squaring
osteoarthritis and other mechanic caus- Calcification
Syndesmophytes
es of back pain (computed tomography
Spondylophytes
(CT), MRI).
Spondylo(discitis)
The magnitude of the structural chan-

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Imaging and scoring in ankylosing spondylitis / J. Braun et al.

radiographic progression is as essential full so far include the lumbar spine, Table II. Bath Ankylosing Spondylitis
as in RA (9). However, the situation in none the thoracic spine and one the cer- Scores.
AS is more complex than in RA. Chan- vical spine (10-12).
BASRI-s:
ges in RA such as joint space narrow- However, many sites of the spine can 1. Scoring of
ing and erosions are consequences of be scored: Sacroiliac joints (2-4)
disease activity. In AS, it is possible the vertebra (fractures, squaring) Lumbar spine (0-4)
that not all changes seen on radio- the intervertebral spaces (discitis), Cervical spine (0-4)
graphs are a result of disease activity the vertebral margins and ligaments 2. on a simple scale between 0-4
but could rather reflect healing process- (erosions, syndesmophytes, bony 0 = normal
es (e.g. new bone formation). For prag- bridging) 1 = suspicious
matic reasons, as it stands now, all the zygapophyseal joints 2 = mild
3 = moderate
changes on AS radiographs should be Again, these can be scored on the ante- 4= severe
regarded as result of an inflammatory rior and dorsal site (on a lateral view),
process. Radiographs provide an as- or on the right and left site (on an AP 3. Addition of these 3 scores to the
sessment of cartilage and bone struc- view, or three-quarter view). BASRI-s (spine) score (2-12).
ture, but may not quantify inflamma- For the assessment of the hips and BASRI-h:
tion. To be able to study the relation be- sacroiliac joints an AP pelvis can be 4. Scoring of
tween changes on radiographs and the used. For the assessment of the spine Hip joints (0-4) = BASRI-h (hip)
inflammatory process in more detail, both AP, lateral and threequarter views
5. on a simple scale between 0-4
reliable scoring methods are needed. can be used. The latter are important 0 = normal
These scoring methods can be useful to for assessment of the zygapophyseal 1 = suspicious
study natural history of disease, rela- joints (13). The AP view of the cervical 2 = mild
tion with disease activity and physical spine is hard to interpret and is not use- 3 = moderate
4= severe
function, prognosis and efficacy of ful for scoring purposes. Both AP and
therapy. The choices to be made regar- lateral view of the lumbar spine can 6. Addition of these 4 scores to the
ding the methodological issues depend give additive information. These are BASRI-t (total) score (2-16).
on the purpose for which imaging is both included in the Bath Ankylosing
done (to classify, prognosticate, mea- Spondylitis Radiology Index (BASRI,
sure change over time) and might be 10) (Table II), whereas the Stoke Anky- 470 AS patients were scored using the
different for each purpose. losing Spondylitis Spinal Score New York criteria for the sacroiliac
Quite a large variety of changes can be (SASSS) uses the lateral lumbar view joints (Table III) and, similarly, grading
seen on radiographs in AS patients, only (11,12). It is not clear how much the lumbar and cervical spine on a scale
some in both the spine, and SI and peri- information is lost if one of the two of 0-4 (for normal, suspicious, mild,
pheral joints, others at one site only. views is omitted. moderate, and severe). These 3 scores
AS is predominantly an axial disease were added together to produce the
affecting the whole spine and sacroiliac Available radiographic scoring BASRI-s score (scored 2-12). Radio-
joints, but also axial and root joints in- methods graphs of 188 patients were used to test
cluding hips and shoulders and periph- Up to now, two scoring methods have reproducibility. Blinded radiographs of
eral joints. Based on the relative fre- been published in full papers: the 89 non-AS patients were included, ran-
quency of involvement, scoring chan- SASSS (11) and the BASRI (10). One domly, to assess disease specificity.
ges in the spine, sacroiliac and axial (es- other method was published in a thesis Sensitivity to change was assessed us-
pecially hip) joints are more important. (14) and one in abstract form only (15). ing 177 radiographs from 58 AS pa-
In a recent data set on a group of 470 The SASSS was published first, and tients. Intra- and interobserver varia-
patients with a mean disease duration includes the lateral view of the lumbar tion showed 75-86% and 73-79% com-
of 21 years (9) over 80% of the patients spine, and separately the sacroiliac plete agreement at all sites, respective-
showed involvement of the cervical and/ joints. This is a detailed scoring system ly. Specificities of 0.83 0.89 suggest-
or lumbar spine, the majority (43%) in for the anterior and posterior site of the ed that the lumbar and cervical spine
both parts. These data indicate the lumbar spine with a range from 0-72.
necessity to include both, the cervical The method described by Creemers is a Table III. Radiographic grading of sacroil-
and the lumbar spine, in the score. modification of the SASSS. Only the iac changes in ankylosing spondylitis.
However, only 8% of the patients had anterior site of the spine is scored.
Grade 0 Normal
changes only in the cervical and not in However, now the anterior site of the
Grade 1 Suspicious
the lumbar spine. There are no data on cervical spine is also included. This
Grade 2 Sclerosis, some erosions
involvement of the thoracic spine. This results in the same range as the original
Grade 3 Severe erosions,widening of the joint
will most probably change by the use SASSS.
space, some ankylosis
of MRI. The other method is the BASRI (10).
Grade 4 Complete ankylosis
The two scoring methods published in To validate the BASRI, radiographs of

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Imaging and scoring in ankylosing spondylitis / J. Braun et al.

BASRI scores were disease-specific. scores (18) proved unreliable: moder- Even with a scoring interval of two
Sensitivity to change became apparent ate intraobserver kappa of 0.47-0.58 years the interobserver reliability re-
at 2 years (P < 0.001). Using a lateral and low interobserver kappa of 0.29. mained very good. The reliability of the
view and an AP view of the lumbar After retraining, interobserver kappa relatively new scoring method for the
spine was more sensitive than using a did not improve (0.45 and 0.17). In ret- hips (BASRI-h) proved to be more dis-
lateral view alone. Grading a set of rospect, a one-year period was too ease specific (16) than the Larsen grad-
radiographs (sacroiliac joints, lumbar short to measure sensitivity to change. ing for RA (18) that is also often
spine, and cervical spine) took 30 sec- Observers agreed that no change oc- applied to score the hips in AS. For all
onds. The BASRI has been used first curred in up to 89% of cases. A mea- scoring methods the complete concor-
with and later without the inclusion of surable change of deterioration or im- dance rates for the observers were
the hips. Depending upon the inclusion provement occurred rarely. rather low. The developers of the BAS-
or exclusion of the hips the range is In a second study with two years of fol- RI method found good to excellent
(2-12) or (2-16), respectively. Recently, low-up, the SI New York and SASSS complete concordance rates (21) for the
a modification has been proposed showed intraobserver ks between 0.56 hips between 78 and 95%. They found
changing the features of grades 3 and 4. and 0.84 and interobserver ks between good concordance rates (73-81%) for
This is called BASRI-s for the spine 0.37 and 0.47 (19). The reliability of BASRI applied on lumbar and cervical
only, BASRI-h for the hips only, and BASRI-hip proved to be moderate to spine and they reached comparable
BASRI-t for the summation of both good: intraobserver ks of 0.66 and concordance rates for the SI New York
(16). 0.67 and interobserver k of 0.40. method (78-86%). Concordance rates
In a recent collaborative approach (17), SASSS scores of cervical and lumbar for the SASSS method have not been
two trained observers scored 217 sets spine proved to be most reliable, with reported by the developers.
of AS radiographs from baseline and both high intra- and interobserver intra- Only BASRI-s and BASRI-t were able
one year follow-up, blinded for se- class coefficients (ICC) between 0.90 to detect change in a considerable num-
quence, of an unselected cross section- and 0.96. For BASRI-spine and BAS- ber of patients over a two-year period.
al cohort of AS patients, followed lon- RI-total the ICCs were comparable This change could not be identified by
gitudinally. The SI joints were scored with the SASSS scores, ranging be- the other graded and detailed scoring
in 5 grades by the New York method tween 0.85-0.95. methods. In case of BASRI-s and BAS-
and the SASSS (Stoke Ankylosing Over a 2 year period no difference was RI-t observers agreed in about 50% that
Spondylitis Spine Score). Hips, cervi- found in mean, median and SD for SI no change occurred. Unfortunately, it
cal and lumbar spine were graded 0-4 New York, SI SASSS and BASRI-hip still needs to be concluded that relevant
according to the BASRI-spine (2-12). score (20). For these three methods 0.3- change occurred rarely because obser-
BASRI- spine and BASRI-hip (16) 1.2% of the patients deteriorated 1 vers a greed in only 7.5% of cases that
were combined to form BASRI-total grade according to both observers and real change of at least 1 grade occurred.
(2-16). The anterior and dorsal site of they agreed in up to 89 % of patients This indicates that it is difficult to score
the lumbar spine were also scored in that no change occurred. BASRI-spine AS radiographs and that we might need
detail with a total scoring range from 0- and BASRI-total also showed limited another scoring system which is more
72 (SASSS). A similar scoring was change in mean, median and SD at sensitive to change. At the other hand,
applied to the anterior site of the cervi- baseline and 2 years. Of all patients these data are from an unselected group
cal spine and this was combined with 7.5% and 7.4% deteriorated 1 grade of patients. It is not clear what the pro-
the anterior site of the lumbar spine to in BASRI-spine and BASRI-total and gression will be in a group of patients
form the modified SASSS (range 0- both observers agreed in only up to with active disease selected for e.g.
72). To assess change on an individual 48% that no change occurred. In case TNF-blocking agents. It also needs to
patient level, a smallest detectable dif- of SASSS (spine) the SDD was lowest be stressed that there is a subgroup of
ference (SDD) was estimated for data (7.5) for the modified SASSS. There patients with rapid progression of dis-
on a quasi interval scale (SASSS spine) was little difference in mean and medi- ease which we might just have to detect
and for the grading scales a change of an on baseline and after two years: earlier.
at least 1 grade was defined as the min- 13.8, 6.7 and 15.0, 7.6 resp., but only The developers of the BASRI-h found
imum assessable difference. very few patients (0.8%) deteriorated significant change after 1 year using
In the first study with one year follow- more than the SDD in modified Wilcoxon signed rank test for nonpara-
up (17) BASRI was only moderately SASSS score. Observers agreed up to metric data in 60 patients. For BASRI-s
reliable, with Cohens kappa ranging 92% that no change occured. they found significant change after 2
between 0.50 and 0.82 for intra, and Taken together, in AS, radiological years (n = 31) and after 1 year 30% of
0.38-0.64 for interobserver reliability. scoring methods are moderately to ex- 20 cases showed change of at least 1
Similarly, SI joint scores showed intra- cellently reliable. The combined BAS - grade but this was not significant. In
observer kappa between 0.56 and 0.84, RI scoring methods (BASRI-s and 1999 they reported the magnitude of
and interobserver reliability with kappa BASRI-t) and especially the SASSS change for the BASRI-s was from 7.0
between 0.37 and 0.47. Larsen hip showed good or excellent reliability. to 7.9 in 2 years and 42% of 31 patients

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Imaging and scoring in ankylosing spondylitis / J. Braun et al.

(a) (b)
Fig. 1. Severe acute sacroiliitis in the left sacroiliac joint of a young male patient with undifferentiated spondyloarthritis (normal sacroiliac x-rays) as detect-
ed by the STIR technique (a) and after application of gadolinium-DTPA (b). Note that some edema/enhancement is also seen in the dorsal part of the right
sacroiliac joint.

showed change in BASRI-s score (21). ic method for the hips available and to Detection of inflammatory spinal
In these studies sensitivity to change score the spine we recommend the lesions in AS by MRI
was not specified for BASRI-t. These BASRI. The BASRI-s and BASRI-t There is increasing evidence that not
data were obtained in selected patients can be distinguished from the SASSS only sacroiliac (Fig. 1), but also spinal
that were not followed according to a methods for the spine by its feasibility, inflammatory lesions (Fig. 2) can be
fixed protocol but radiographs were it also takes into account the AP view nicely detected by MRI using the STIR
taken dependent on the clinical situa- of the lumbar spine and it was the only
tion. method which showed change in a con-
The developers of the SASSS methods siderable number of patients over a two
found significant change over a group year period. Further study is needed
of 28 patients in 1 year using Mann- with sets of radiographs in which pro-
Whitney U test with a mean change of gression of damage is likely, e.g. sets
4.1 points (range 0-72) in SASSS-total with a 5 year interval or in a AS popu-
and a mean change of 1 grade in lation with a short disease duration be-
SASSS for the sacroiliac joints (22). In cause these patients tend to show more
this study the order in which the radio- radiological change. Additional studies
graphs were scored was known in con- where AS radiographs are scored in
trast with our study. This is known to both random and chronological order
markedly influence the results. Calcu- are warranted to assess the difference
lation of 95% limits of agreement using in methodology. Importantly, the smal-
the Bland and Altman method can only lest detectable differences of the meth-
be applied reliably in scores with inter- ods (23) need to be especially assessed
val scales with large ranges such as the in the patient subgroups with very
SASSS scores. active and early disease.
Most methods were unable to detect There are two different concepts on the
change over this two year period be- mode of radiographic and functional
cause only few individuals show real progression of AS during the first 10
radiological change over a two year years after disease onset. While two
period in an average AS population. groups reported that the most rapid
Comparing all radiological AS studies progression occurred in this period (24,
available at the moment we recom- 25), another group recently reported
mend to use the New York method for (26) that in their patient population Fig. 2. Acute spondylitis posterior with cos-
the SI joints because it is most widely radiographic progression was linear tovertebral arthritis of the 6th vertebra of the tho-
used. The BASRI-hip should be used with no significant changes between racic spine in a 35-year old female AS patients
(normal x-ray of the thoracic spine).
because it is the only AS disease specif- the decades.

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Imaging and scoring in ankylosing spondylitis / J. Braun et al.

used MRI to document improvement of


inflammatory spinal disease (29-31).
Importantly, the detection of spinal le-
sions by MRI allows to localize the
main inflammatory spot with some pre-
cision, also in areas which used to be
difficult for imaging techniques. This
might facilitate side directed therapy in
the future.

Scoring spinal lesions detected by


MRI
Based on our experience with spinal
MRI in recent years we propose a gra-
ding system (Table IV and Fig. 3) that
has recently been evaluated in 20 AS
patients who took part in the RCT on
Fig. 3. Ankylosing spondylitis MRI activity score. infliximab in AS (32). The preliminary
analysis suggests that especially the
and the dynamic technique with gado- agents, objective evidence of improve- activity score is reliable with good
linium (27, 28). Since more effective ment by modern imaging technology intra- and interobserver correlations
therapies have now become available becomes increasingly important. Of and sensitivity to change over a short
for the SpA in form of anti-TNF interest, three recent pilot studies have period of 3 months. One example of a

Fig. 4. Sacroiliac (a, b) and spinal (c, d) MRIs (STIR technique) of a patient with ankylosing spondylitis treated with infliximab before (a, c) and after ther-
apy (b, d). Sacroiliitis is located in the ventral part of the left sacroiliac joint and spondylitis at the anterior rim of vertebrae 3-5 in the lumbar spine.
(Photos provided courtesy of Dr. M. Bollow, Bochum, Germany).

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Imaging and scoring in ankylosing spondylitis / J. Braun et al.

Table IV. A preliminary score of MR grading of spondylitis: MRI spine score. 1984; 27: 361-8.
6. DOUGADOSM, VAN DER LINDEN S, JUHLIN R
Differential assessment of inflammation and ankylosis et al.: The European Spondylarthropathy
Study Group preliminary criteria for the clas-
Semiquantitative analysis of at least two images/lesion sification of spondylarthropathy. Arthritis
Scoring of all accessible vertebrae from CS 2 S 1 (n = 23) Rheum 1991; 34: 1218-27.
Including the intervertebral space and the discs 7. VAN DER HEIJDE D, BELLAMY N, CALIN A,
DOUGADOS M, KHAN MA, VAN DER LINDEN
One vertebral unit =
SJ : On behalf of the Assessment in Ankylos-
Lower half of vertebra above plus
ing Spondylitis Working Group. Preliminary
Upper half of vertebra below
core sets for endpoints in ankylosing spondy-
litis. J Rheumatol 1997; 24: 2225-9.
Proposed scoring system:
8. BRAUN J, BRANDT J, LISTING J et al.: Treat-
a. activity score: 0-6 for every vertebral unit assessed (n=138): ment of active ankylosing spondylitis with
bone marrow edema by STIR and/or enhancement after contrast infliximab - A double-blind placebo control-
bone marrow edema by STIR and/or enhancement after contrast plus erosions led multicenter trial. Lancet 2002; 359:1187-
b. chronicity score: 0-6 for every vertebral unit assessed (n=138): 93.
sclerosis, erosions, syndesmophytes, partial fusion, ankylosis 9. LIPSKY PE, VAN DER HEIJDE DM, ST CLAIR
EW et al.: Infliximab and methotrexate in the
treatment of rheumatoid arthritis. Anti-Tumor
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score needs to be further evaluated in rays remain the basis for a diagnosis of 10. MACKAY K, MACK C, BROPHY S, CALIN A:
the upcoming clinical trials on inflix- AS. The Bath Ankylosing Spondylitis Radiology
Index (BASRI). A new validated approach to
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