DOI:10.2214/AJR.07.3865
AJR 2008; 191:980-986
© American Roentgen Ray Society
Role of Diffusion-Weighted MRI in the Detection of Early Active Sacroiliitis
Zulkif Bozgeyik1,
Salih Ozgocmen2 and
Ercan Kocakoc1
1 Department of Radiology, Faculty of Medicine, Firat University, 23119, Elazig,
Turkey.
2 Division of Rheumatology, Department of Physical Medicine and Rehabilitation,
Faculty of Medicine, Firat University, Elazig, Turkey.
Received February 18, 2008;
accepted after revision May 6, 2008.
Address correspondence to Z. Bozgeyik
(bozgeyik4{at}hotmail.com).
Abstract
OBJECTIVE. This study proposed to evaluate the value of
diffusion-weighted MRI (DWI) to detect active inflammatory changes in the
sacroiliac joints of patients with early axial spondyloarthritis (also spelled
spondylarthritis).
SUBJECTS AND METHODS. Forty-two patients with chronic low back pain
underwent clinical and MRI evaluation for axial spondyloarthritis or early
ankylosing spondylitis. STIR, contrast-enhanced T1-weighted, fat-saturated
T2-weighted, and diffusion-weighted (b values: 100, 600, 1,000
s/mm2) images were obtained. The presence of subchondral bone
marrow edema, subchondral fatty marrow infiltration, or contrast enhancement
in the sacroiliac joints or adjacent enthesitis sites was considered a marker
for active inflammatory changes. All MRI sequences were evaluated for the
presence of acute inflammatory changes and inter- and intrarater reliability
of the sequences. Mean apparent diffusion coefficient (ADC) values of
diffusion-weighted images were calculated from normal and involved iliac and
sacral bones of sacroiliac joints.
RESULTS. ADC values measured from the lesions at b values of 1,000
and 600 s/mm2 in patients with sacroiliitis (n = 13) were
significantly higher than values measured from iliac and sacral bones in
patients with low back pain of mechanical origin (n = 29). DWI showed
sensitivity for detecting acute lesions in early sacroiliitis similar to that
of T1-weighted gadolinium images (area under the curve, 0.843–0.971).
Intra- and interrater reliability of DWI was acceptable.
CONCLUSION. DWI is a sensitive, fast sequence and does not require a
contrast agent, which makes it a good and cost-effective alternative for
imaging sacroiliac joints. DWI also offers the possibility of quantifying
diffusion coefficients of the lesions, which helps to discriminate between
normal and involved subchondral bone.
Keywords: ankylosing spondylitis • diffusion-weighted imaging • MRI • sacroiliitis • spondylarthritis • spondyloarthritis
Introduction
Diffusion-weighted MRI (DWI) is based on the tissue-dependent signal
attenuation caused by incoherent thermal motion of water molecules, which is
the brownian water motion of the spins in biologic tissue
[1]. The apparent diffusion
coefficient (ADC), a quantitative parameter calculated from diffusion-weighted
images, combines the effects of capillary perfusion and water diffusion in the
extracellular extravascular space
[2]. DWI has been successfully
used in neuroradiologic settings
[3] and widely used in
intracranial tumors, demyelination diseases, and abscesses of the brain
[4,
5].
Muscle, cartilage, and soft-tissue abnormalities have been also examined
with diffusion-weighted images
[6–8],
as well as traumatic bone marrow edema
[9] and several spinal
abnormalities [1]. DWI may be
helpful in detecting skull metastasis and bone marrow changes of the cranium
[10,
11] and has been shown to be a
useful tool to differentiate pyogenic spondylitis and erosive osteochondritis
or spinal infection from malignancy
[12,
13].
Ankylosing spondylitis is a chronic inflammatory disease of unknown cause
that affects mainly young adults. Inflammatory back pain and alternating
gluteal pain related to sacroiliitis are the leading symptoms in adults with
early ankylosing spondylitis and undifferentiated spondyloarthritis
[14–16].
Pain arising from an inflamed sacroiliac joint is typical in ankylosing
spondylitis and is always considered a diagnostic criterion
[15]. Although sacroiliitis is
the most important element of the classification criteria, it requires
2–5 years to become evident on conventional radiographs, resulting in a
delay in the diagnosis of the ankylosing spondylitis
[14,
15]. Therefore, advanced MRI
techniques such as dynamic contrast-enhanced MRI (DCE-MRI) or DWI may provide
opportunities for the early detection of sacroiliitis. A recent study has
shown that DWI and DCE-MRI might be effective in quantifying inflammatory
changes at involved skeletal sites and useful for assessing treatment efficacy
in ankylosing spondylitis
[17].
The aim of this study was to assess whether DWI can detect bone marrow and
subchondral bone changes in early active sacroiliitis and to compare the
reliability of DWI with other validated methods such as contrast-enhanced and
STIR images. To our knowledge, ours is the first study validating DWI in early
active sacroiliitis.
Subjects and Methods
Patients with chronic low back pain (symptoms for > 3 months) were
recruited from the outpatient clinic of our department. Inclusion criteria for
the study required the presence of chronic low back pain without a confirmed
diagnosis and an age of 18–45 years. Exclusion criteria were current
infections (including brucellosis) of the bone and joints, pregnancy, metallic
implants, and claustrophobia. We followed the diagnostic algorithm suggested
by the Berlin group for the early diagnosis of axial spondyloarthritis
[16]. The Berlin algorithm is
based on the probability of early axial spondyloarthritis in patients with
chronic back pain according to the absence or presence of certain clinical
features, laboratory tests, and skeletal imaging. The entry criteria were
inflammatory back pain and the presence of at least three of seven
spondyloarthritis features: family history of spondyloarthritis, heel pain,
uveitis, synovitis, dactylitis, good response to nonsteroidal antiinflammatory
drugs, and HLA (human leukocyte antigen)-B27 positivity. This algorithm is
also followed when using MRI to evaluate the sacroiliac joints. The result of
the algorithm is express ed as a percentage of probability of axial spondylo
arthritis. The rate above which axial spondylo arthritis is considered a
definite diagnosis is 90%
[16]. All patients were
informed of the study pro cedure and gave their written informed consent.
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Fig. 1A —26-year-old man with early active sacroiliitis. STIR
(A) and fat-saturated fast spin-echo T2-weighted (B) images show
hyperintense lesions consistent with bone marrow edema in sacral and iliac
aspects of sacroiliac joints.
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Fig. 1B —26-year-old man with early active sacroiliitis. STIR
(A) and fat-saturated fast spin-echo T2-weighted (B) images show
hyperintense lesions consistent with bone marrow edema in sacral and iliac
aspects of sacroiliac joints.
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MRI
All patients underwent MRI of the sacroiliac joints with and without IV
administration of gadolinium. MRI was performed using a 1.5-T whole-body
superconducting MR scanner (Signa Excite, GE Healthcare) equipped with
high-speed gradients. All sequences were obtained in the oblique coronal
(parallel to the long axis of the sacroiliac joint) and axial planes using a
4-channel surface coil. The following sequences were ob tained from the
sacroiliac joints: fast spin-echo T1-weighted (TR/TE, 625/minimum), STIR
(4,975/35), fat-saturated fast spin-echo T2-weighted (4,650/120), and
fat-saturated contrast-enhanced fast spin-echo T1-weighted (625/minimum) se
quences. The fat-saturated contrast-enhanced T1-weighted images were obtained
after the admin istration of 0.1 mmol/kg of body weight of gadopentetate
dimeglumine. The field of view was 20 x 20 cm; slice thickness, 5 mm;
number of excitations, 2; and intersection gap, none. The lumbar spine was
also shown using the afore mentioned MRI parameters for visualiza tion of
spinal abnormalities. In addition to the mentioned sequences, T2-weighted
sagittal and axial im ages were obtained for the lumbar spine. On lumbar spine
images, disk lesions, paravert ebral soft-tissue structures, and bone
structures were evaluated.
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Fig. 2A —34-year-old woman with chronic low back pain of mechanical
origin. Sacroiliac joints and subarticular areas were normal. Black-and-white
apparent diffusion coefficient (ADC) map shows 12 regions of interest (ROIs)
placed in subarticular surface of sacroiliac joints.
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Fig. 2B —34-year-old woman with chronic low back pain of mechanical
origin. Sacroiliac joints and subarticular areas were normal. Color ADC map
shows ADC values of ROIs in normal-appearing areas.
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DWI was performed using single-shot spin-echo echo-planar imaging sequences
with diffusion gradient b values of 100, 600, and 1,000 s/mm2. The
following DWI parameters were used: 8,000/minimum; field of view, 20 x
20 cm; number of excitations, 2; matrix size, 128 x 128; slice
thickness, 5 mm; intersection gap, none. The DWI sequences required a total of
96 seconds.
Image Interpretation
The sacroiliac joints were evaluated for signal intensity characteristics
involving the joint space, surrounding bone, and bone marrow adjacent to the
joint on each imaging sequence. The presence of subchondral bone marrow edema
or contrast enhancement in the sacroiliac joints or adjacent enthesitis sites
was considered a marker for active inflammatory changes. Chronic
changes—defined as changes that were low signal on T1- and T2-weighted
sequences—subchondral sclerosis, narrowing of the joint spaces, bone
bridging, and ankylosis, were noted if present.
Patients' identities were removed from STIR images, contrast-enhanced
T1-weighted images, fat-saturated T2-weighted images, and diffusion-weighted
images at b values of 100, 600, and 1,000 s/mm2. Two radiologists
with 6 and 10 years of experience in musculoskeletal diseases assessed these
images for the presence of active inflammatory lesions (at either the iliac or
the sacral bone) on the right and left sacroiliac joints in separate sessions.
Each radiologist assessed only one MRI sequence (i.e., one radiologist
assessed STIR sequences and the other assessed contrast-enhanced T1-weighted
sequences in one session) each day; an interim of at least 2 days was required
before another session. Radiologists assessed images in random order. One of
the radiologists reassessed these images using the same protocol 2 months
after the first assessment.
After completing the inter- and intraobserver procedure, the presence of
acute or active sacroiliitis was decided by consensus between a radiologist
and a rheumatologist after the examination of the STIR, contrast-enhanced
T1-weighted, and fat-saturated T2-weighted images as well as the
diffusion-weighted images at b values of 100, 600, and 1,000 s/mm2
(Fig. 1A,
1B,
1C,
1D,
1E,
1F). The diffusion-weighted
image data were transferred to a work station (Advantage Windows, software
version 2.0, GE Healthcare). A circular region of interest (ROI) having an
area of 73–88 mm2 was placed in the subarticular surface of
the sacroiliac joint. Six ADC measurements were taken from sacroi liac joints
(superior, middle, and inferior por tions of the sacral and iliac bones) of
all the patients (Fig. 2A,
2B). In patients with bone
marrow or subchondral bone changes, ADC measurements were taken from all
apparent lesions as well (Figs.
3A,
3B and
4A,
4B,
4C,
4D). All measurements were
repeated for the three b values (100, 600, 1,000 s/mm2). ADC maps
were calculated automatically by the MR system; ADC values are expressed in
square millimeters per second.
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Fig. 4A —20-year-old man with early active sacroiliitis. STIR
(A) and fat-saturated fast spin-echo T2-weighted (B) images show
hyperintense lesions in sacral and iliac bones of right sacroiliac joint.
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Fig. 4B —20-year-old man with early active sacroiliitis. STIR
(A) and fat-saturated fast spin-echo T2-weighted (B) images show
hyperintense lesions in sacral and iliac bones of right sacroiliac joint.
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Statistical Methods
Statistical calculations were performed on a PC using Statistical Package
for the Social Sciences (SPSS) software. Differences between groups were
assessed using the Mann-Whitney U test. For right and left scans, the
percentage of agreement between the two assessors and the kappa coefficients
were calculated with 95% CIs.
Two-by-two contingency tables were formed, and specificity, sensitivity,
positive and negative predictive values, and likelihood ratios were calculated
for independent diffusion-weighted MR sequences in 95% CIs. The reference
standard for the presence of acute changes was the contrast-enhanced
T1-weighted images. For all separate MR sequences, receiver operator
characteristic (ROC) curves were formed and areas under the curve were
obtained. Values for the area under the curve that are near 1.0 represent
better results; values less than or equal to 0.5 are equivalent or worse
results than expected by random chance. A value greater than 0.7 can be
interpreted as reasonable or fair, and values greater than 0.8, as good,
meaning the test has the capacity to discriminate.
Results
Forty-two patients were included in the study. Patients' characteristics
are given in Table 1. Thirteen
patients with chronic low back pain were diagnosed with inflammatory low back
pain and sacroiliitis suggesting axial spondyloarthritis, and 29 patients were
diagnosed with chronic low back pain of mechanical origin. Thirteen of these
42 patients had acute inflammatory changes on MR images of the sacroiliac
joints. Of these 13 patients, two had erosions on right sacral and iliac bone
surfaces, six had sclerosis either on the right or the left sacral or iliac
subchondral bone or both, and seven had no chronic change on the sacroiliac
joints. Two patients with chronic low back pain of mechanical origin had
sclerosis on the right subchondral surfaces (one on the right iliac bone, one
right iliac and sacral subchondral bones). None of the patients with either
sacroiliitis or low back pain of mechanical origin had ankylosis.
ADC Values Between Groups
Table 2 shows ADC values
measured from the iliac and sacral bones on the right and left sides in
patients with sacroiliitis and mechanical low back pain. Patients with acute
early sacroiliitis had significantly different b values only in the right
iliac and sacral bones at a b value of 1,000 s/mm2 and only on the
right iliac bone at a b value of 100 s/mm2 compared with patients
with mechanical low back pain. ADC values measured at a b value of 600
s/mm2 did not have a significant difference between groups.
However, ADC values measured from the lesions at b values of 1,000 and 600
s/mm2 in patients with sacroiliitis were significantly higher than
values measured from the iliac and sacral bones in patients with mechanical
low back pain (Table 2).
Comparison of T1-Weighted Gadolinium-Enhanced and DWI Sequences
The presence or absence of the lesions on T1-weighted gadolinium images was
compared with the diffusion-weighted images obtained at b factors of 100, 600,
and 1,000 s/mm2. Using the T1-weighted gadolinium images as the
reference standard, ROC curves were formed and values for area under the curve
were obtained. For b values of 1,000 s/mm2, values for area under
the curve on the right iliac and sacral and left iliac and sacral bones were
0.899, 0.908, 0.929, and 0.843, respectively; for b of 600 s/mm2,
0.971, 0.908, 0.929, and 0.914; and for b of 100 s/mm2, 0.971,
0.908, 0.929, and 0.914. These good values mean DWI in all three b gradients
can discriminate acute lesions in sacroiliitis as well as T1-weighted
gadolinium images can.
Inter- and Intrarater Reliability
Interrater reliability for T1-weighted gadolinium-enhanced images and
diffusion-weighted images is shown in Table
3. Intrarater reliability on the right and left sides was good to
excellent for both T1-weighted gadolinium images and diffusion-weighted images
at b values of 1,000, 600, and 100 s/mm2 (
=
0.62–0.93).
Discussion
Ankylosing spondylitis is a common form of spondyloarthritis. MRI of the
sacroiliac joint was sensitive in depicting sacroiliitis. STIR, fat-saturated
T2-weighted images, and contrast-enhanced T1-weighted images have been used to
detect inflammation. Many studies have evaluated the capabilities of these
sequences. Most of those studies showed that contrast-enhanced T1-weighted
images were more sensitive for detecting the presence and extent of acute
inflammatory changes than STIR and fat-saturated T2-weighted images
[18–20].
DWI has become widely available in recent years. This technique has proven
to be a valuable method for tracing the microscopic structure of tissue
[21]. Molecular diffusion is a
physical process that is used to describe the brownian motion of water
molecules [22]. The ADC is
used as a measure of diffusion in biologic systems because the measured
diffusion coefficient may depend on factors other than brownian water motion,
such as perfusion [23]. When
only high b values are applied, the ADC value approximates the true diffusion.
Low b values are influenced by both perfusion and diffusion
[24].
More recently, DWI has been increasingly used in musculoskeletal structures
and diseases. Ward et al. [9]
analyzed the diffusion characteristics of normal and posttraumatic bone marrow
and concluded that increased ADC values in traumatized bone marrow compared
with ADC values of normal bone.
Some DWI studies in the literature relate to spine abnormalities. Baur et
al. [25] evaluated the
usefulness of DWI of the bone marrow for differentiating benign and abnormal
vertebral compression fractures. Signal intensity characteristics of bone
marrow were analyzed for DWI, STIR, and T1-weighted spin-echo images. On DWI,
benign vertebral compression fractures were hypo- to isointense with respect
to adjacent normal vertebral bodies. Pathologic compression fractures were
hyperintense in comparison with normal-appearing vertebral bodies. Those
authors concluded that DWI provided excellent distinction between abnormal and
benign vertebral compression fractures
[25].
Chan et al. [26] showed
that normal vertebral bone marrow had a mean ADC value of 0.23 x
10–3 mm2/s (only diffusion-weighted images with a
b value of 1,000 s/mm2 were used). They also reported the mean ADC
value of benign vertebral fracture to be 1.94 x 10–3
mm2/s, whereas the mean ADC value for vertebral fracture caused by
neoplasm was 0.82 x 10–3 s/mm2
[26]. Dietrich et al.
[27] reported a similar result
of normal vertebral bone marrow having an ADC value of 0.3 x
10–3 mm2/s (four b values between 50 and 500
s/mm2 were used). Our mean ADC values of sacroiliac bone marrow
obtained from the subarticular surface of the sacroiliac joint at different b
values are shown in Table
2.
DWI is also useful in infectious disease of the bone marrow. Buyn
[12] evaluated 10 patients
with pyogenic spondylitis and 50 patients with erosive osteochondritis. All 10
patients with spondylitis showed a hyperintense signal as compared with normal
surrounding bone marrow on DWI. The mean combined ADC value in two patients
with tuberculous spondylitis was 0.98 x 10–3
mm2/s [12]. Pui et
al. [13] investigated the
value of DWI in differentiating spinal infection from malignancy. Cutoff ADC
values of tuberculosis-related vertebral marrow lesions were 1.2 x
10–3 mm2/s; those of pyogenic lesions were 1.3
x 10–3 mm2/s. Normal bone marrow showed an
ADC of 0.38 x 10–3 mm2/s
[13]. The ADC value of an area
with a spinal infection was higher than a normal area of bone marrow. We found
higher ADC values in the affected areas (lesions) in patients with axial
spondyloarthritis compared with iliac and sacral areas in patients with
mechanical low back pain. Bone marrow edema causes a local increase in water
movement, resulting in increased local diffusion that is expressed by high ADC
values of the lesions.
In a recently published report, Gaspersic et al.
[17] evaluated the effects of
different therapies on enthesitis and osteitis in active ankylosing
spondylitis using DWI and DCE-MRI. They concluded that quantitative MRI
parameters diminished significantly with regression of the inflammatory
activity. DWI and DCE-MRI were shown to be effective in quantifying changes in
inflammation during the treatment of ankylosing spondylitis and may be
convenient for assessing treatment efficacy
[17].
In conclusion, DWI is a sensitive, fast sequence and does not require a
contrast agent, which makes it a good and cost-effective alternative for
imaging sacroiliac joints. DWI also offers the possibility of quantifying
diffusion coefficients of the lesions, which can discriminate between normal
and involved subchondral bone, and it offers a new alternative for follow-up.
DWI may be useful in the early diagnosis and follow-up of the acute
inflammatory lesions that occur in early axial spondyloarthritis.
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Abstract
Introduction
