DOI:10.2214/AJR.05.1423
AJR 2006; 187:1420-1426
© American Roentgen Ray Society
MRI of the Sacroiliac Joints in Patients with Moderate to Severe Ankylosing Spondylitis
Miriam A. Bredella1,2,
Lynne S. Steinbach1,
Stephanie Morgan3,
Michael Ward4 and
John C. Davis3
1 Department of Radiology, University of California, San Francisco, San
Francisco, CA.
2 Present address: Department of Radiology, Massachusetts General Hospital, 55
Fruit St., Yawkey Bldg., 6400 (6E), Boston, MA 02114.
3 Department of Internal Medicine, Division of Rheumatology, University of
California, San Francisco, San Francisco, CA.
4 National Institute of Arthritis and Musculoskeletal Skin Diseases, National
Institutes of Health, Bethesda, MD.
Received August 15, 2005;
accepted after revision October 21, 2005.
Address correspondence to M. A. Bredella
(mbredella{at}partners.org).
Abstract
OBJECTIVE. The objectives of our study were to evaluate whether MRI
findings of the sacroiliac joints are able to distinguish between active and
inactive disease in patients with established ankylosing spondylitis and to
determine whether these findings correlate with markers of clinical activity,
disease duration, severity, and degree of radiographic damage.
MATERIALS AND METHODS. Eighteen patients with symptomatic moderate
to severe ankylosing spondylitis were evaluated. MRI of the sacroiliac joint
(1.5 T) was performed using fat-saturated T2-weighted, T1-weighted, STIR, and
fat-saturated contrast-enhanced T1-weighted sequences. The sacroiliac joints
were evaluated by two radiologists for enhancement, subchondral bone marrow
edema, erosions, and subchondral fatty marrow infiltration. Findings on MRI
were analyzed for correlation with multiple clinical characteristics and
measures of disease activity, including radiographic scoring.
RESULTS. In 17 patients, MRI showed abnormal findings of the
sacroiliac joint. Ten patients showed active disease on MRI as measured by
abnormal enhancement and subchondral bone marrow edema. Disease activity
detected using MRI correlated in a positive fashion with only C-reactive
protein (CRP) level. There was no correlation with the other measures of
disease activity or with disease duration. In 14 patients, fatty subchondral
bone marrow was detected on MRI. These changes were seen in patients with
active and chronic disease and correlated with higher radiographic scores but
not with disease duration or markers of disease activity.
CONCLUSION. Contrast-enhanced MRI of the sacroiliac joint is
sensitive in depicting sacroiliitis in patients with established ankylosing
spondylitis. Subchondral edema and enhancement correlate with high CRP levels.
Subchondral fatty bone marrow changes were seen in both active and chronic
sacroiliitis and are correlated with higher radiographic scores; these changes
may be a marker of more advanced disease.
Keywords: ankylosing spondylitis bone joint MRI musculoskeletal imaging sacroiliac joints sacroiliitis
Introduction
Involvement of the sacroiliac joints is a hallmark of ankylosing
spondylitis
[1-4].
The definite diagnosis of ankylosing spondylitis requires radiographic
evidence of sacroiliitis, which is defined as erosions, subchondral sclerosis,
and irregular joint spaces, and clinical features, including inflammatory back
pain [1]. Conventional
radiographs remain the most widely accepted and available screening method for
ankylosing spondylitis; however, radiographs often show normal findings during
the early stages of the disease, and several years may be required for
sacroiliitis to become apparent on radiography
[3-6].
MRI of the sacroiliac joints has been shown to be superior to radiography
in depicting sacroiliitis, and gadolinium-enhanced MRI has been shown to be
useful in the early detection of active sacroiliitis
[7,
8]. New treatment options for
patients with ankylosing spondylitis require sensitive imaging techniques to
not only help diagnose ankylosing spondylitis early, but also determine
disease activity and the degree of damage present at diagnosis
[9-11].
The purposes of our study were to evaluate MRI of the sacroiliac joint in
patients with moderate to severe ankylosing spondylitis and to determine
whether MRI findings of enhancement, edema, and fatty marrow changes were
correlated with clinical features and measures of disease activity.
Materials and Methods
Over a 1-year period, MR images and radiographs of the sacroiliac joints of
18 patients with ankylosing spondylitis who had been recruited for two
clinical trials were evaluated. Patients had moderate to severe disease
activity as defined by the Bath Ankylosing Spondylitis Disease Activity Index
(BASDAI) score of > 40 (range, 0-100) and physician visual analog scale
(VAS) global score of > 40 (range, 0-100). Another criterion for inclusion
in our study was that patients had symptomatic inflammatory lower back pain.
Definite ankylosing spondylitis was diagnosed using the modified New York
criteria [1].
Radiography
Oblique and anteroposterior radiographs of both sacroiliac joints were
available for all patients. Radiographs were graded according to the Bath
Ankylosing Spondylitis Radiology Index (BASRI). Each sacroiliac joint was
evaluated retrospectively by two radiologists in consensus who were blinded to
laboratory results and clinical status. The sacroiliac joints were evaluated
for blurring of joint margins, sclerosis, erosions, and total ankylosis. A
BASRI score was then assigned for each patient.
MRI
All patients underwent MRI of the sacroiliac joints with and without
administration of IV gadolinium. MRI (1.5 T; Signa, GE Healthcare) was
performed using oblique coronal (parallel to the long axis of the sacrum) and
axial fast spin-echo (FSE) T1-weighted sequences (TR/TE, 600/minimum); and
STIR (4,000/60), fat-saturated FSE T2-weighted (4,000/50), and fat-saturated
contrast-enhanced FSE T1-weighted (600/minimum) sequences. The fat-saturated
contrast-enhanced T1-weighted images were obtained after IV administration of
0.1 mmol/kg of body weight of gadopentetate dimeglumine. The field of view was
20 cm; slice thickness, 4 mm; and number of excitations, 2. The imaging times
were 7 minutes for the STIR sequences, 4 minutes for the fat-saturated FSE
T2-weighted sequences, 6 minutes for the FSE T1-weighted sequences, and 6
minutes for the fat-saturated contrast-enhanced FSE T1-weighted sequences.
The sacroiliac joints were retrospectively analyzed by the same two
radiologists in consensus who were blinded to laboratory results and clinical
status. MR images were evaluated at a different time point than the
radiographs, and the results of the radiographs were not available at the time
of MR interpretation. The sacroiliac joints were evaluated for signal
characteristics involving the joint space, surrounding bone, and bone marrow
adjacent to the joint on each imaging sequence. Enhancement, subchondral bone
marrow edema, cartilage abnormalities, periarticular erosions, subchondral
fatty marrow infiltration, and ankylosis were recorded. Chronic disease was
defined as changes that were low signal on T1- and T2-weighted images,
subchondral sclerosis, narrowing of the joint spaces, bone bridging, and
ankylosis. Erosions that were high signal on STIR or T2-weighted images,
subchondral edema, and enhancement within or adjacent to the sacroiliac joint
were considered markers for active inflammatory disease. Findings on MRI of
the sacroiliac joint were graded as 1 (mild), 2 (moderate), or 3 (severe). An
MRI score was obtained for each patient. MRI was performed within 12 weeks of
radiography.
Analysis
Findings on MRI and radiography were analyzed for correlation with clinical
inflammatory markers: C-reactive protein (CRP), erythrocyte sedimentation rate
(ESR), BASDAI, Bath Ankylosing Spondylitis Functional Index (BASFI), back pain
scores (total back pain, nocturnal back pain, inflammatory back pain, and
physician and patient global scores), disease duration, and BASRI scores.
Laboratory markers were obtained within 1 week of MRI. The ESR (Westergren
sedimentation rate test) and CRP level were measured using conventional
laboratory technology, with normal values being < 10 mm/h and < 6 mg/L,
respectively.
The Wilcoxon's rank sum test and Jonckheere-Terpstra test were used to
compare associations between different radiographic measures. The
Jonckheere-Terpstra test is a nonparametric test that accounts for the ordered
nature of the radiographic grading categories. Large values of Z on
the Jonckheere-Terpstra test indicate an important association between
measures.

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Fig. 1A 28-year-old man with ankylosing spondylitis for 10 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
7.3 mg/L; erythrocyte sedimentation rate, 5 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 80.0; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 60.2; inflammatory back pain score, 94; nocturnal back pain
score, 83; total back pain score, 82. Radiographs show indistinct sacroiliac
joint with erosions.
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Fig. 1B 28-year-old man with ankylosing spondylitis for 10 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
7.3 mg/L; erythrocyte sedimentation rate, 5 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 80.0; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 60.2; inflammatory back pain score, 94; nocturnal back pain
score, 83; total back pain score, 82. Coronal T1-weighted MR image shows
subchondral fatty marrow changes (arrows). There is irregularity of
sacroiliac joint.
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Fig. 1C 28-year-old man with ankylosing spondylitis for 10 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
7.3 mg/L; erythrocyte sedimentation rate, 5 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 80.0; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 60.2; inflammatory back pain score, 94; nocturnal back pain
score, 83; total back pain score, 82. Coronal fat-saturated contrast-enhanced
T1-weighted image shows small foci of enhancement at inferior sacroiliac joint
(arrows).
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Results
Multiple demographic and disease activity measures are listed in
Table 1. The patient population
included 14 men and four women with a mean age of 37 years. The mean disease
duration was 14 years (range, 2-39 years). Findings for human leukocyte
antigen (HLA) B-27 were positive in 94.4% of the patients. As expected by the
inclusion criterion of definite ankylosing spondylitis by the modified New
York criteria, conventional radiographs showed involvement of the sacroiliac
joint in all 18 patients. Unilateral involvement was seen in one patient and
bilateral involvement was detected in 17 patients. Seven patients were shown
to have complete ankylosis of the sacroiliac joint. Moderate findings,
corresponding to a BASRI score of 3, were seen in eight patients. One patient
had minimal changes of the sacroiliac joint (BASRI score of 2).
All 18 patients except one had abnormal MRI findings of the sacroiliac
joint: 16 patients had bilateral involvement and one patient had unilateral
involvement. Ten patients showed abnormal enhancement and subchondral bone
marrow edema, suggestive of active disease (Figs.
1A,
1B,
1C,
1D,
1E,
2A,
2B,
2C, and
2D). These findings were
bilateral in all patients. Seven patients were shown to have ankylosis and
subchondral sclerosis of the sacroiliac joint. Two of these patients with
ankylosis showed edema and enhancement on MRI, indicating active disease
(Figs. 3A,
3B,
3C,
3D, and
3E). In 16 patients, fatty
subchondral bone marrow was seen. These changes were seen in patients with MRI
findings suggestive of active disease and in those with MRI findings
suggestive of chronic disease.

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Fig. 1D 28-year-old man with ankylosing spondylitis for 10 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
7.3 mg/L; erythrocyte sedimentation rate, 5 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 80.0; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 60.2; inflammatory back pain score, 94; nocturnal back pain
score, 83; total back pain score, 82. Coronal STIR image shows focal T2
prolongation at inferior sacroiliac joint (arrows).
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Fig. 1E 28-year-old man with ankylosing spondylitis for 10 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
7.3 mg/L; erythrocyte sedimentation rate, 5 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 80.0; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 60.2; inflammatory back pain score, 94; nocturnal back pain
score, 83; total back pain score, 82. Edema (arrows) is not well
visualized on coronal fat-saturated T2-weighted image.
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Fig. 2A 34-year-old woman with ankylosing spondylitis for 21 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
6 mg/L; erythrocyte sedimentation rate, 7 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 77.3; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 75.2; inflammatory back pain score, 100; nocturnal back pain
score, 24; total back pain score, 47. Radiograph shows suspicious changes of
sacroiliac joint.
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Fig. 2B 34-year-old woman with ankylosing spondylitis for 21 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
6 mg/L; erythrocyte sedimentation rate, 7 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 77.3; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 75.2; inflammatory back pain score, 100; nocturnal back pain
score, 24; total back pain score, 47. Coronal T1-weighted MR image shows
normal findings.
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Fig. 2C 34-year-old woman with ankylosing spondylitis for 21 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
6 mg/L; erythrocyte sedimentation rate, 7 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 77.3; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 75.2; inflammatory back pain score, 100; nocturnal back pain
score, 24; total back pain score, 47. Coronal fat-saturated contrast-enhanced
T1-weighted image shows moderate enhancement (arrows).
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Fig. 2D 34-year-old woman with ankylosing spondylitis for 21 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
6 mg/L; erythrocyte sedimentation rate, 7 mm/h; Bath Ankylosing Spondylitis
Functional Index (BASFI), 77.3; Bath Ankylosing Spondylitis Disease Activity
Index (BASDAI), 75.2; inflammatory back pain score, 100; nocturnal back pain
score, 24; total back pain score, 47. Coronal STIR image shows mild bilateral
inferior edema of sacroiliac joint (arrows).
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Fig. 3A 43-year-old man with ankylosing spondylitis for 20 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
17.5 mg/L; erythrocyte sedimentation rate, 34 mm/h; Bath Ankylosing
Spondylitis Functional Index (BASFI), 42.8; Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI), 41.8; inflammatory back pain score, 41.5;
nocturnal back pain score, 62; total back pain score, 63. Radiograph shows
fusion of sacroiliac joint.
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Fig. 3B 43-year-old man with ankylosing spondylitis for 20 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
17.5 mg/L; erythrocyte sedimentation rate, 34 mm/h; Bath Ankylosing
Spondylitis Functional Index (BASFI), 42.8; Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI), 41.8; inflammatory back pain score, 41.5;
nocturnal back pain score, 62; total back pain score, 63. Axial T1-weighted MR
image shows sclerosis and fusion of sacroiliac joint (arrows).
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Fig. 3C 43-year-old man with ankylosing spondylitis for 20 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
17.5 mg/L; erythrocyte sedimentation rate, 34 mm/h; Bath Ankylosing
Spondylitis Functional Index (BASFI), 42.8; Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI), 41.8; inflammatory back pain score, 41.5;
nocturnal back pain score, 62; total back pain score, 63. Coronal T1-weighted
MR image shows sclerosis and fusion of sacroiliac joint (arrows).
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Fig. 3D 43-year-old man with ankylosing spondylitis for 20 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
17.5 mg/L; erythrocyte sedimentation rate, 34 mm/h; Bath Ankylosing
Spondylitis Functional Index (BASFI), 42.8; Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI), 41.8; inflammatory back pain score, 41.5;
nocturnal back pain score, 62; total back pain score, 63. Coronal
fat-saturated contrast-enhanced T1-weighted image shows bilateral enhancement
of sacroiliac joint (arrows).
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Fig. 3E 43-year-old man with ankylosing spondylitis for 20 years.
Laboratory results and clinical findings were as follows: C-reactive protein,
17.5 mg/L; erythrocyte sedimentation rate, 34 mm/h; Bath Ankylosing
Spondylitis Functional Index (BASFI), 42.8; Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI), 41.8; inflammatory back pain score, 41.5;
nocturnal back pain score, 62; total back pain score, 63. Coronal STIR image
shows mild subchondral edema (arrows).
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In all patients with MRI findings of enhancement, bone marrow edema was
seen on STIR and fat-saturated FSE T2-weighted images. No difference in the
severity of edema was detected on STIR images and fat-saturated FSE
T2-weighted images; however, edema was slightly better seen on the STIR images
than the fat-saturated FSE T2-weighted images (Figs.
1A,
1B,
1C,
1D, and
1E). Four of 10 patients with
active disease on MRI showed more extensive enhancement on fat-saturated
T1-weighted images compared with the edematous changes seen on STIR or
fat-saturated FSE T2-weighted images (Figs.
2A,
2B,
2C,
2D,
3A,
3B,
3C,
3D, and
3E). MRI findings of disease
activity correlated only with CRP value
(Table 2). There was no
correlation between MRI findings and ESR, BASRI, BASDAI, BASFI, back pain
scores, or disease duration.
Subchondral fatty changes on MRI correlated with BASRI score but were
inversely related to enhancement (Table
3). MRI findings of fatty subchondral bone marrow did not
correlate with disease duration or clinical inflammatory markers.
Radiographic findings did not correlate with clinical or laboratory markers
of disease activity or of disease duration.
Discussion
Given the development of new promising treatment options for ankylosing
spondylitis, such as tumor necrosis factor alpha, it is important to diagnose
ankylosing spondylitis early, detect active sacroiliitis and differentiate it
from chronic changes, and monitor for potential changes after therapy
[10,
12]. In addition, studies have
shown a lack of correlation between clinical signs of disease activity and
conventional laboratory markers of disease activity such as CRP levels and ESR
[13]. Imaging findings play an
important role in the diagnosis of sacroiliitis in patients with ankylosing
spondylitis, and MRI of the sacroiliac joint has been shown to be able to
reveal the anatomy and degree of inflammation without the use of ionizing
radiation [6]. Also, MRI has
been found to be more sensitive than radiography for detecting sacroiliitis in
patients with ankylosing spondylitis, especially in the evaluation of early
disease [7,
8,
14-16].
The purpose of our study was to focus on the use of MRI in evaluating
disease activity in patients with moderate to severe ankylosing spondylitis
and whether it is possible to show active disease in patients with established
ankylosing spondylitis. In this select group of patients with moderate to
severe ankylosing spondylitis recruited for clinical trials, MRI of the
sacroiliac joint was sensitive in depicting sacroiliitis. MRI allowed lesions
with higher water content due to inflammatory edema to be differentiated from
lesions with reduced water content due to fibrotic tissue or sclerosis. MRI
was also able to show inflammatory changes in advanced stages of ankylosing
spondylitis, even in patients with ankylosis of the sacroiliac joint. This
finding suggests that fusion does not necessarily signal the absence of
associated inflammatory activity at the sacroiliac joint and that patients
with sacroiliitis need to be treated in the later disease stages. When
evaluating the effects of disease-modifying drugs, it may be valuable to
follow these different lesions because they may be, in part, reversible.
Fat-saturated T2-weighted and STIR sequences were slightly less sensitive
than contrast-enhanced T1-weighted sequences for detecting the extent of acute
inflammatory changes. Although all patients with edematous changes on STIR and
fat-saturated FSE T2-weighted images also showed abnormal enhancement, we saw
more enhancing lesions on the fat-saturated contrast-enhanced T1-weighted
images, supporting the use of IV contrast material. The oblique coronal plane
was the most useful plane for detecting changes associated with ankylosing
spondylitis.
MRI findings of disease activity correlated only with CRP value. There was
no correlation between MRI findings and ESR, BASRI, BASDAI, BASFI, back pain
scores, or disease duration. These findings are in contrast to the results of
a study performed by Jee et al.
[2] who found significant
correlation with synovial enhancement and ESR value and with the sum of ESR
and CRP values but not with the CRP value alone.
The observation that some patients had periarticular fat accumulation in
the bone marrow has no apparent pathophysiologic explanation. However, this
finding seems to reflect a later stage of disease because it was associated
with more severe involvement of the sacroiliac joints (ankylosis), as
determined using the BASRI score, and was inversely related to enhancement.
This suggests a temporal change from enhancement to fat as sacroiliac fusion
progresses. The observed fat accumulation supports the concept that the
disease process in sacroiliitis involves subchondral areas and may be due to
an ongoing effect of inflammatory products on local fat metabolism
[17,
18].
Our study had several limitations. First is the relatively small number of
patients and the retrospective nature of the study. Second is the absence of
pathologic tissue confirmation of disease activity. Also, reviewers evaluated
the MR examinations and radiographs without knowledge of the laboratory data;
however, the reviewers were aware that the patients had been diagnosed with
ankylosing spondylitis.
In conclusion, contrast-enhanced MRI of the sacroiliac joint is able to
depict sacroiliitis in patients with moderate to severe ankylosing
spondylitis. MRI findings suggestive of active disease, such as subchondral
edema and enhancement, and MRI findings of fatty bone marrow changes show no
correlation with clinical parameters except CRP level. This suggests that MRI
can reveal changes at a cellular level that are not depicted by clinical
parameters.
Acknowledgments
We thank the Rosalind Russell Medical Center for Arthritis Research for its
support.
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Z. Bozgeyik, S. Ozgocmen, and E. Kocakoc
Role of Diffusion-Weighted MRI in the Detection of Early Active Sacroiliitis
Am. J. Roentgenol.,
October 1, 2008;
191(4):
980 - 986.
[Abstract]
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A. Lacout, B. Rousselin, and J.-P. Pelage
CT and MRI of Spine and Sacroiliac Involvement in Spondyloarthropathy
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M Rudwaleit, S Schwarzlose, E S Hilgert, J Listing, J Braun, and J Sieper
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[Abstract]
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