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The diagnostic utility of magnetic resonance imaging in spondylarthritisAn international multicenter evaluation of one hundred eighty-seven subjects.

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ARTHRITIS & RHEUMATISM
Vol. 62, No. 10, October 2010, pp 3048–3058
DOI 10.1002/art.27571
© 2010, American College of Rheumatology
The Diagnostic Utility of Magnetic Resonance Imaging
in Spondylarthritis
An International Multicenter Evaluation of One Hundred Eighty-Seven Subjects
Ulrich Weber,1 Robert G. W. Lambert,2 Mikkel Østergaard,3 Juerg Hodler,1
Susanne J. Pedersen,4 and Walter P. Maksymowych2
sensitivity, specificity, and positive and negative likelihood ratios (LRs) for the diagnosis of SpA based on
global assessment of the MRI scans.
Results. Diagnostic utility was high for all 5
readers, both for patients with AS (sensitivity 0.90,
specificity 0.97, positive LR 44.6) and for patients with
preradiographic IBP (sensitivity 0.51, specificity 0.97,
positive LR 26.0). Diagnostic utility based solely on
detection of bone marrow edema enhanced sensitivity
(67%) for patients with IBP but reduced specificity
(88%); detection of erosions in addition to bone marrow
edema further enhanced sensitivity (81%) without
changing specificity. A single lesion of the sacroiliac
joint on MRI was observed in up to 27% of control
subjects.
Conclusion. This systematic and standardized
evaluation of sacroiliac joints in patients with SpA
showed that MRI has much greater diagnostic utility
than has been documented previously. We present for
the first time a data-driven definition of MRI-visualized
positivity for SpA.
Objective. To systematically assess the diagnostic
utility of magnetic resonance imaging (MRI) to differentiate patients with spondylarthritis (SpA) from patients with nonspecific back pain and healthy volunteers, using a standardized evaluation of MR images of
the sacroiliac joints.
Methods. Five readers blinded to the patients and
diagnoses independently assessed MRI scans (T1weighted and STIR sequences) of the sacroiliac joints
obtained from 187 subjects: 75 patients with ankylosing
spondylitis (AS; symptom duration <10 years), 27 patients with preradiographic inflammatory back pain
(IBP; mean symptom duration 29 months), 26 patients
with nonspecific back pain, and 59 healthy control
subjects; all participants were age 45 years or younger.
Bone marrow edema, fat infiltration, erosion, and ankylosis were recorded according to standardized definitions using an online data entry system. We calculated
Supported by the Canadian Arthritis Society National Research Initiative Award, the Alberta Heritage Foundation for Medical
Research, the Walter L. and Johanna Wolf Foundation, and the
Foundation for Scientific Research at the University of Zurich. Dr.
Maksymowych is a Scientist of the Alberta Heritage Foundation for
Medical Research.
1
Ulrich Weber, MD, Juerg Hodler, MD, MBA: Balgrist
University Hospital, Zurich, Switzerland; 2Robert G. W. Lambert,
MB, FRCPC, Walter P. Maksymowych, MB, FRCPC: University of
Alberta, Edmonton, Alberta, Canada; 3Mikkel Østergaard, MD, PhD,
DMSc: Copenhagen University Hospitals at Hvidovre, Glostrup, and
Gentofte, Copenhagen, Denmark; 4Susanne J. Pedersen, MD: Copenhagen University Hospital at Gentofte, Copenhagen, Denmark.
Dr. Hodler had received consulting fees from the Siemens
MSK Advisory Board (less than $10,000).
Address correspondence and reprint requests to Ulrich Weber, MD, Department of Rheumatology, Balgrist University Hospital,
Forchstrasse 340, 8008 Zurich, Switzerland. E-mail: ulrich.weber@
balgrist.ch.
Submitted for publication January 5, 2010; accepted in revised form May 13, 2010.
Diagnosing early spondylarthritis (SpA) in young
patients presenting with symptoms of inflammatory back
pain (IBP) and normal findings on plain radiographs of
the sacroiliac (SI) joints remains a challenge in routine
practice. Radiography detects postinflammatory structural changes in the subchondral bone of the SI joints,
but changes may become evident only after a symptom
duration of several years (1,2). Magnetic resonance
imaging (MRI) is capable of detecting inflammatory
changes in bone marrow and soft tissue and is now
widely accepted as the most sensitive imaging modality
for detecting sacroiliitis, the hallmark of SpA. Therefore, MRI may be able to detect abnormalities in the SI
3048
DATA-DRIVEN DEFINITION OF MRI POSITIVITY FOR SpA
joints prior to detection using radiography. A systematic
literature review in 2004 (3) addressed those studies that
focused on the diagnostic utility of MRI in patients with
either established ankylosing spondylitis (AS) or IBP
and concluded that the overall sensitivity and specificity
of MRI for SpA was 0.90, with a positive likelihood ratio
(LR) of 9.0. This estimate of diagnostic utility has since
been incorporated into diagnostic algorithms for diagnosing SpA in clinical practice, which rely on estimates
of the degree to which positive findings by MRI increase
the pretest probability of SpA.
There are several reasons, however, why this
estimate of diagnostic utility requires reappraisal. Most
studies included in the systematic review lacked age- and
sex-matched controls and used dynamic (not standard)
contrast-enhanced MRI, which is costly, unreliable, and
not routinely used in clinical practice (4–8). Moreover,
there is increasing acceptance of the necessity for including certain methodologic aspects of study design such as
standardization of technique for acquiring and reading
MR images, consensus definitions of abnormalities visible on MR images, and standardized calibration/
training of readers at different sites. These requirements are aimed at ensuring external validity of study
conclusions.
The recently published Assessment of SpondyloArthritis international Society (ASAS) classification criteria for axial spondylarthritis (9) include, for the first
time, an MR image demonstrating sacroiliitis as an
acceptable imaging criterion indicative of SpA but additionally require the presence of at least 1 clinical feature
of SpA. An ASAS working group has also proposed a
definition of an MR image positive for sacroiliitis according to consensus opinion that is based entirely on
the presence of bone marrow edema on the STIR
sequence or osteitis on gadolinium-enhanced T1weighted images (10). Structural abnormalities that may
be observed on T1-weighted sequences are not included
in this definition.
In this report, we describe a multicenter evaluation of the diagnostic utility of MRI in patients with SpA
that includes age- and sex-matched control subjects, uses
MRI sequences that are widely used in clinical practice,
and is based on a standardized methodology for the
diagnostic evaluation of the SI joint by MRI, as follows:
implementation of standardized definitions of active
inflammatory and structural lesions of the SI joint on
MRI as defined by the Canada–Denmark MRI Working
Group (11,12); development of a reference MR image
set of an SI joint by consensus among study investigators
based on these definitions (www.arthritisdoctor.ca); cal-
3049
ibration of readers using an online training module
developed by the Spondyloarthritis Research Consortium of Canada (SPARCC) (ref. 13 and www.arthritis
doctor.ca) followed by videoteleconferences; and development of a customized online data entry module based
on a standardized approach to recording abnormalities
in the SI joint (www.arthritisimaging.ca).
The study was called MORPHO, because the
morphologic appearance of bright bone marrow edema
on STIR images involving both sides of each sacroiliac
joint resembles the pattern of light reflection on opened
wings of Morpho butterflies (Morpho sp.) that are found
in South American rainforests.
PATIENTS AND METHODS
Subjects. Patients with SpA. One hundred two patients
with SpA, ages ⱕ45 years, were recruited at the rheumatology
outpatient clinics of 2 university hospitals in Edmonton and
Zurich. Of these patients, 75 met the modified New York
classification criteria for AS (14) and had a disease duration of
ⱕ10 years. Nineteen patients with IBP (all recruited from
Balgrist University Hospital, Zurich) not fulfilling the modified New York criteria for radiographic AS did meet the Berlin
criteria for IBP (15) and additionally showed ⱖ1 clinical or
laboratory feature of SpA. In 8 patients with IBP (all from the
University of Alberta) not meeting the modified New York
criteria, disease was defined according to the criteria described
by Calin and colleagues (16) and by expert opinion. Among the
27 patients with IBP, the mean symptom duration was 29
months. Patients with SpA who had received ongoing or
previous treatment with tumor necrosis factor ␣ inhibitors
were not eligible for this study. Plain pelvic radiographs
obtained from patients in both SpA groups were independently
assessed and categorized according to the modified New York
criteria (14), by 2 readers at each site.
Control groups. The first control group comprised 26
patients ages ⱕ45 years, all of whom had nonspecific back
pain. Nonspecific back pain was defined based on clinical
grounds and according to plain radiographs of the SI joint. A
second control group comprised 59 healthy volunteers (ages
ⱕ45 years) from the staffs of both university hospitals that
were involved in the recruitment of patients with SpA. The
eligibility of these volunteers was defined using the Nordic
questionnaire (17); volunteers with symptoms compatible with
IBP or clinical features suggestive of SpA (e.g., psoriasis of the
skin or chronic inflammatory bowel disease) were excluded.
The study protocol was approved by the local ethics
committees; the patients and the healthy participants all gave
written informed consent.
MRI protocol. Scans from both centers included coronal T1-weighted turbo spin-echo and STIR sequences angled
parallel to the SI joint. The scan parameters for all sequences
were as follows: 15–19 slices, 4-mm slice thickness, 0.4-mm
interslice gap, and field of view 280–300 mm. Parameters for
the T1-weighted sequence were as follows: repetition time
(TR) 423–450 msec, echo time (TE) 12–13 msec, echo train
3050
WEBER ET AL
Figure 1. Four types of acute and structural lesions of the sacroiliac (SI) joint as demonstrated by magnetic resonance imaging. A,
Bone marrow edema (arrows) in all quadrants of both SI joints of a 28-year-old HLA–B27–positive female patient with inflammatory
back pain and a symptom duration of 15 months, on STIR sequences. Bone marrow edema is defined as an increase in bone marrow
signal in the SI joint on STIR images; the center of the sacrum at the same craniocaudal level is used as the primary reference for
normal bone marrow signal. B, Erosion at the sacral side of the right SI joint (arrow) of a 25-year-old HLA–B27–positive male patient
with ankylosing spondylitis (AS) with a symptom duration of 24 months, on T1-weighted spin-echo (T1SE) sequences. An erosion is
defined as the full-thickness loss of dark appearance of either iliac or sacral cortical bone of the SI joint and change in normal bright
appearance of adjacent bone marrow on T1-weighted images; adjacent bone marrow demonstrates altered signal intensity on
T1-weighted images as compared with normal iliac or sacral marrow on the same slice at the same craniocaudal level. The lower iliac
portion of the right SI joint shows an erosion at the threshold of definition (broken arrow), while sclerosis (dotted arrow) is seen in
the upper iliac half of the right SI joint (open arrowheads point to the marrow signal medial to the dark area that is similar to adjacent
iliac marrow). The left SI joint displays sclerosis and definite erosion in the left iliac bone (solid arrowheads) and, as a consequence,
pseudo-widening of joint space; loss of adjacent marrow signal is visible compared with normal iliac marrow. C, Fat infiltration
predominantly on the sacral side of both SI joints (arrows) in a 28-year-old HLA–B27–positive male patient with AS with a symptom
duration of 7 years, on T1-weighted spin-echo sequences. Fat infiltration is defined as a focal increased signal in bone marrow on
T1-weighted images. D, Ankylosis (arrows) in the distal part of both SI joints of a 42-year-old HLA–B27–negative male patient with
AS with a symptom duration of 8 years, by T1-weighted spin-echo sequences. Ankylosis is defined as bright signal on T1-weighted
images extending across the SI joint.
length (ETL) 3, and matrix 512 ⫻ 256 pixels. For the STIR
sequence, the parameters were TR 3,700–4,930 msec, inversion time 145–150 msec, TE 50–69 msec, ETL 7–9, and matrix
256–384 ⫻ 256 pixels. These are the usual sequences and scan
parameters for routine MRI evaluation of patients with SpA in
the involved institutions.
Standardized assessment of MR images. STIR and
T1-weighted sequences of semicoronal MR scans of the SI
joint were read and scored independently by 5 readers (2
radiologists [JH and RGL] and 3 rheumatologists [MØ, UW,
and WPM]) who were blinded to patient demographics and
diagnosis. The films were evaluated in random order on
electronic work stations in the institution of each reader. The
following steps were performed in chronological order.
Standardized definitions of lesions on MRI scans. We
adopted standardized definitions of active inflammatory and
structural lesions of the SI joint on MRI, which were developed by the Canada–Denmark MRI Working Group (11,12).
We focused on 4 types of lesions identified by MRI: bone
marrow edema on STIR images, and joint erosion, marrow fat
infiltration, and ankylosis on T1-weighted images (Figures
1A–D). Bone sclerosis and abnormalities of the synovial cavity
were not addressed because of poor reproducibility in prereadout exercises.
DATA-DRIVEN DEFINITION OF MRI POSITIVITY FOR SpA
Reference set of SI joint MR images. We developed a
reference SI joint MR image set by consensus among study
investigators, based on the definitions for these 4 types of
lesion (ref. 13 and www.arthritisdoctor.ca). Four videoteleconference sessions involving the 3 university centers focused on
the application of the standardized definitions of SI joint
lesions on MRI and served to calibrate the reader team by
conducting 2 test-reading exercises on SI joint scans displaying
acute and structural inflammatory lesions. The reference image set served as a benchmark at the time of reading the study
MR images and included lesions considered to be at the
threshold of detection, to facilitate calibration and the assignment of questionable lesions.
Standardized assessment of MRI-visualized lesions of the
SI joint. We standardized the approach to assessing MR
images of the SI joint by adopting the methodology outlined in
the SPARCC online training module (13,18). This training
module has been validated by demonstrating that inexperienced rheumatology fellows can achieve reliability of detection
of bone marrow edema comparable with that recorded by
experienced SPARCC readers after reviewing the training
module (13). Principal features of the module include systematic assessment of the SI joint from anterior to posterior. At
least 1 SI joint must be a minimum of 1 cm in vertical height in
order to score that image; once an SI joint is at least 3 cm in
vertical height, it is divided at the midpoint into 4 equal upper
and lower sacral and iliac quadrants. At the posterior aspect of
the SI joint, there is a natural division of the joint into upper
and lower quadrants by intervening fat and fibrous tissue.
Online data entry module. We developed a customized
online data entry module for recording MRI findings based on
a standardized approach to recording abnormalities in the SI
joint. The module has 2 sections, the first of which contains 3
questions that address global assessment of each scan, as
follows: 1) “This MRI scan confirms the presence of SpA
(agree/disagree)”; 2) “Your conclusion is based on which MRI
sequence (STIR, T1-weighted turbo spin-echo, both sequences)”; and 3) “What is the primary MRI feature on which
your diagnosis of SpA is based (bone marrow edema, fat
infiltration, bone erosion, ankylosis, not applicable because
SpA is not present).” The second section of the Web-based
data entry module consists of a detailed recording section in
which the SI joint is represented as a schematic with 4
quadrants (upper and lower ilium, upper and lower sacrum).
Each lesion, except ankylosis, is recorded as being present/
absent on a dichotomous basis in each quadrant. Ankylosis is
recorded in each half of the joint (upper and/or lower) (Figure 1).
Statistical analysis. The distribution of the 4 MRI
lesions in patients and control subjects was analyzed descriptively according to single readers, mean (range) values for all 5
readers, and concordant data recorded by at least 2 readers.
The ASAS-proposed definition of a positive MRI result based
on consensus opinion stipulates the requirement for 2 bone
marrow edema lesions on the same slice or, if only a single
bone marrow edema lesion is evident, it must be present on 2
consecutive slices (10). We considered this definition as being
met in our data entry module in 2 circumstances. The first
would be when a score of at least 2 for bone marrow edema
was recorded on the same slice, indicating 2 bone marrow
edema lesions in 2 distinct SI joint quadrants or a single lesion
extending across 2 SI joint quadrants. The second circum-
3051
stance would also be a score of at least 2 for bone marrow
edema, but this would be attributable to a score of 1 indicating
a single bone marrow edema lesion being recorded on 2
consecutive slices in the same SI joint quadrant. We adopted a
similar approach to descriptive data for erosions and fat
infiltration.
The diagnostic utility of MRI for SpA according to
global evaluation of both T1-weighted and STIR MRI scans
was determined by calculating the sensitivity, specificity, positive and negative LRs for individual reader data, concordant
data according to at least 2 readers, and for data recorded
concordantly by all 3 rheumatologists and both radiologists.
These analyses were repeated for the proposed ASAS definition of a positive result of MRI. We also formulated a
data-driven proposal for a positive MRI result after recording
a high frequency and specificity of erosions in patients with
preradiographic SpA and after noting that the diagnostic
utility of MRI according to the ASAS definition was less than
that recorded by global assessment. We postulated that global
assessment captured additional diagnostic information beyond
that provided by assessment of bone marrow edema, and that
this information would largely be attributable to the presence
of erosions. We therefore proposed an alternate definition of
a positive MRI result, termed the MORPHO proposal, which
defines SpA as being present on MRI if any of the following 3
criteria are met: 1) bone marrow edema in at least 2 SI joint
quadrants in the same slice or a single SI joint quadrant in 2
consecutive slices (according to the ASAS definition); 2)
erosion in at least 2 SI joint quadrants in the same slice or a
single SI joint quadrant in 2 consecutive slices; and 3) bone
marrow edema and erosion in any SI joint quadrant though not
necessarily in the same quadrant. The diagnostic utility of this
definition was tested by calculating sensitivity, specificity,
positive and negative LRs for individual reader data, concordant data according to at least 2 readers, and data recorded by
all rheumatologists and both radiologists.
RESULTS
Descriptive analysis. Demographics of patients
with SpA and control groups. Among the 75 patients
meeting the modified New York criteria, the mean ⫾ SD
age was 31.1 ⫾ 6.2 years, the mean ⫾ SD disease
duration was 6.1 ⫾ 2.8 years, and 72% of the patients
were male. The mean ⫾ SD Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI) (19) score was 4.4 ⫾
1.9, and the mean ⫾ SD Bath Ankylosing Spondylitis
Functional Index (BASFI) (20) score was 2.9 ⫾ 2.5; both
of these scoring systems are based on a scale of 0–10.
The mean ⫾ SD C-reactive protein (CRP) level was
10.5 ⫾ 18.4 mg/liter. Fifty-nine (83%) of 71 patients with
AS who underwent HLA–B27 testing had positive results. The 27 patients with IBP (67% of whom were
male) had a mean ⫾ SD age of 29 ⫾ 6.8 years and a
mean ⫾ SD symptom duration of 29 ⫾ 26 months; their
mean ⫾ SD BASDAI and BASFI scores were 4.2 ⫾ 2.1
and 2.6 ⫾ 2.2, respectively, and their mean ⫾ SD CRP
3052
WEBER ET AL
Table 1. Frequency of specific MRI abnormalities in SpA patients and controls, as recorded concordantly by ⱖ2 readers and according to the mean
for all 5 readers*
Group
AS patients (n ⫽ 75)
ⱖ1 SIJ quadrant
ⱖ2 SIJ quadrants
ASAS proposal
ⱖ3 SIJ quadrants
IBP patients (n ⫽ 27)
ⱖ1 SIJ quadrant
ⱖ2 SIJ quadrants
ASAS proposal
ⱖ3 SIJ quadrants
NSBP patients (n ⫽ 26)
ⱖ1 SIJ quadrant
ⱖ2 SIJ quadrants
ASAS proposal
ⱖ3 SIJ quadrants
Healthy controls (n ⫽ 59)
ⱖ1 SIJ quadrant
ⱖ2 SIJ quadrants
ASAS proposal
ⱖ3 SIJ quadrants
Bone marrow edema
Erosion
Fat infiltration
68 (90.7)/62.8 (83.7 [59–68])
65 (86.7)/60.4 (80.5 [57–67])
64 (85.3)/59.8 (79.7 [57–66])†
62 (82.7)/58.0 (77.3 [54–66])
70 (93.3)/59.4 (79.2 [42–71])
68 (90.7)/56.6 (75.5 [37–68])
68 (90.7)/56 (74.7 [37–68])‡
63 (84.0)/52.2 (69.6 [32–68])
21 (77.8)/18.6 (68.9 [16–21])
18 (66.7)/16.4 (60.7 [14–19])
18 (66.7)/16.2 (60.0 [14–18])†
16 (59.3)/15.4 (57.0 [14–17])
16 (59.3)/13.0 (48.1 [8–20]) 12 (44.4)/9.6 (35.6 [7–12])
16 (59.3)/11.6 (43.0 [6–19]) 10 (37.0)/8.6 (31.9 [6–11])
13 (48.1)/10.4 (38.5 [5–18])‡ 10 (37.0)/8.4 (31.1 [6–11])‡
11 (40.7)/8.2 (30.4 [4–14])
9 (33.3)/7.2 (26.7 [5–9])
Ankylosis
70 (93.3)/65.2 (86.9 [64–67]) 20 (26.7)/18.4 (24.5 [11–27])
68 (90.7)/62.2 (82.9 [61–66]) 14 (18.7)/14.2 (18.9 [10–19])
68 (90.7)/62 (82.7 [60–66])‡
NA
66 (88.0)/58.8 (78.4 [55–64]) 13 (17.3)/12.6 (16.8 [9–18])
7(26.9)/6.2 (23.8 [3–12])
6 (23.1)/4.4 (16.9 [2–9])
6 (23.1)/4.2 (16.2 [2–8])†
5 (19.2)/3.4 (13.1 [2–5])
2 (7.7)/2.8 (10.8 [0–6])
2 (7.7)/1.6 (6.2 [0–3])
1 (3.8)/1.2 (4.6 [0–2])‡
1 (3.8)/0.8 (3.1 [0–2])
5 (19.2)/4.6 (17.7 [2–7])
5 (19.2)/3.8 (14.6 [2–6])
4 (15.4)/3.6 (13.8 [2–6])‡
2 (7.7)/2.4 (9.2 [2–3])
13 (22.0)/11 (18.6 [4–19])
7 (11.9)/5.6 (9.5 [3–12])
4 (6.8)/4.6 (7.8 [2–9])†
5 (8.5)/3.6 (6.1 [1–8])
5 (8.5)/5.8 (9.8 [1–13])
2 (3.4)/3 (5.1 [1–10])
1 (1.7)/2 (3.4 [0–7])‡
1 (1.7)/1 (1.7 [0–3])
14 (23.7)/10.2 (17.3 [6–19])
9 (15.3)/7.2 (12.2 [4–14])
8 (13.6)/7.2 (12.2 [4–14])‡
8 (13.6)/5.4 (9.2 [3–11])
0 (0)/0.2 (0.007 [0–1])
0 (0)/0 (0 [0])
NA
0 (0)/0 (0 [0])
0 (0)/0.4 (0.02 [0–1])
0 (0)/0.2 (0.008 [0–1])
NA
0 (0)/0.2 (0.008 [0–1])
0 (0)/0 (0 [0])
0 (0)/0 (0 [0])
NA
0 (0)/0 (0 [0])
* Values are the number (%) of abnormalities recorded concordantly by ⱖ2 readers/mean number of abnormalities (% [range]) recorded by all 5
readers. SpA ⫽ spondylarthritis; AS ⫽ ankylosing spondylitis; NA ⫽ not applicable (ankylosis was recorded in each half of the joint, not per
quadrant); IBP ⫽ inflammatory back pain; NSBP ⫽ nonspecific back pain.
† Assessment of SpondyloArthritis international Society (ASAS) proposal for magnetic resonance imaging (MRI) positive for abnormalities (10):
ⱖ2 bone marrow edema (BME) lesions in 2 distinct sacroiliac joint (SIJ) quadrants on the same slice or ⱖ1 BME lesion extending across 2 SIJ
quadrants or ⱖ1 BME lesion recorded on 2 consecutive slices in the same SIJ quadrant.
‡ ASAS operational definition adapted to erosions and fat infiltration (presence of MRI lesions in at least 2 SIJ quadrants in the same slice or in
a single SIJ quadrant on 2 consecutive slices).
levels were 13.8 ⫾ 30.8 mg/liter. Twenty-three (92%) of
25 patients with IBP who underwent testing for HLA–
B27 had positive results. Among the 59 healthy control
subjects, the mean ⫾ SD age was 31.0 ⫾ 6.2 years, and
63% were male. The mean ⫾ SD age of the 26 patients
with nonspecific back pain was 33.8 ⫾ 7.9 years, and
58% were male.
Frequency of specific MRI abnormalities. The
number and percent of patients with SpA and control
subjects with MRI lesions that were recorded concordantly by any 2 readers and the mean number (range and
percent) recorded by all 5 readers for the 4 categories of
MRI lesions are shown in Table 1. Bone marrow edema,
erosion, and fat infiltration were recorded in both
patients and control subjects, while ankylosis was recorded only in patients with SpA and those with nonspecific back pain. Bone marrow edema was the most
common inflammatory lesion in the group with IBP,
followed by erosion and fat infiltration. In contrast,
erosion and fat infiltration were recorded more frequently than bone marrow edema in the group with AS.
Bone marrow edema meeting the proposed ASAS criteria for a positive MRI result was recorded concordantly in 66.7% (18 of 27) and 85.3% (64 of 75) of
patients with IBP and patients with AS, respectively, but
it was also recorded concordantly in 23.1% of patients
with nonspecific back pain and in 6.8% of healthy
control subjects. A single bone marrow edema lesion was
observed in 26.9% of the nonspecific back pain patients
and in 22% of the healthy control subjects. When the
ASAS operational definition was applied to fat infiltration, fat infiltration was recorded concordantly as being
present in at least 2 SI joint quadrants on the same
slice or in 1 SI joint quadrant on 2 consecutive slices
in 90.7%, 37%, 15.4%, and 13.6% of the patients with
AS, those with IBP, patients with nonspecific back pain,
and healthy control subjects, respectively. Applying the
ASAS operational definition to erosions, this was recorded concordantly in 90.7% and 48.1% of patients
with AS and those with IBP, respectively, but in only
3.8% of patients with nonspecific back pain and 1.7% of
healthy control subjects.
Frequency of a diagnosis of SpA in the 4 groups
based on results of the global assessment of SI joint MRI.
The number (percent) of patients in whom SpA was
diagnosed concordantly by ⱖ2 readers according to the
global evaluation of both MRI sequences was 74 (99%)
of 75 in the AS group and 14 (52%) of 27 in the IBP
DATA-DRIVEN DEFINITION OF MRI POSITIVITY FOR SpA
3053
Table 2. Concordance for the diagnosis of SpA according to global assessment by MRI*
Agreement for SpA
Group, readers
AS patients (n ⫽ 75)
All 5 readers
All 3 rheumatologists
Both radiologists
IBP patients (n ⫽ 27)
All 5 readers
All 3 rheumatologists
Both radiologists
NSBP patients (n ⫽ 26)
All 5 readers
All 3 rheumatologists
Both radiologists
Healthy controls (n ⫽ 59)
All 5 readers
All 3 rheumatologists
Both radiologists
Agreement for no SpA
Concordant
Discordant
Concordant
Discordant
51 (68)
56 (75)
65 (87)
19 (25)
13 (17)
10 (13)
0 (0)
2 (3)
0 (0)
5 (7)
4 (5)
NA
12 (44)
13 (48)
13 (48)
2 (7)
0 (0)
1 (4)
11 (41)
11 (41)
13 (48)
2 (7)
3 (11)
NA
0 (0)
0 (0)
0 (0)
0 (0)
1 (4)
NA
24 (92)
24 (92)
25 (96)
2 (8)†
1 (4)
1 (4)
0 (0)
1 (2)
0 (0)
1 (2)
1 (2)
NA
55 (93)
56 (95)
57 (97)
3 (5)‡
1 (2)
2 (3)
* Values are the number (%). Concordance was achieved when all readers of a reader group reported that the magnetic resonance image (MRI)
indicated spondylarthritis or no spondylarthritis. Discordance was reported when the reports of the readers were discordant for either
spondylarthritis or no spondylarthritis. AS ⫽ ankylosing spondylitis; NA ⫽ not applicable (the definition for discordance could not be applied to the
diagnoses reported because there were only 2 radiologists); IBP ⫽ inflammatory back pain.
† In 2 patients with nonspecific back pain (NSPB), NSPB was diagnosed as spondylarthritis (SpA) by 2 of 5 readers each.
‡ In 1 healthy control subject, SpA was diagnosed by 3 of 5 readers; in 2 control subjects, SpA was diagnosed by 2 of 5 readers each.
group. The 13 patients with IBP in whom SpA was not
diagnosed demonstrated few SI joint quadrants with
bone marrow edema, erosion, and fat infiltration (11
patients) or no lesions on MRI at all (2 patients). One
patient with AS in whom SpA was not diagnosed was
reported as having no bone marrow edema by any
reader, although erosions were recorded in up to 5 SI
joint quadrants, and fat infiltration was recorded in up to
7 SI joint quadrants. In 2 (8%) of 26 patients with
nonspecific back pain, SpA was diagnosed by 2 readers
each, primarily on the basis of bone marrow edema in 1
patient and both bone marrow edema and erosions in
the second patient. SpA was diagnosed in 3 (5%) of 59
healthy volunteers (in 1 control subject by 3 readers and
in 2 control subjects by 2 readers, respectively). The
allocation of the 3 healthy volunteers to the SpA group
was mainly based on the presence of bone marrow
edema.
Concordance and discordance for the diagnosis of
SpA according to global assessment by MRI. The concordance for the overall assessment between all 5 readers,
the 3 rheumatologists and both radiologists responding
to the question “This MRI scan confirms the presence of
SpA” is shown in Table 2. Concordance was defined as
all readers in a group being in agreement that the MRI
scan indicated a diagnosis of SpA or no SpA. Readers
were defined as being discordant for either SpA or no
SpA depending on whether the majority considered the
MR image as indicating SpA or no SpA, respectively.
Because there were only 2 radiologists, this definition for
discordance could not be applied to the diagnoses
reported by them. Concordance for the diagnosis of SpA
by MRI in the IBP group was 85% for all 5 readers, 89%
for the 3 rheumatologists, and 96% for both radiologists.
Concordance for the absence of SpA in the 2 control
groups was high, with 92–96% concordance for the
nonspecific back pain control subjects and 93–97%
concordance for the healthy volunteers.
Diagnostic utility of MRI for SpA. Diagnostic
utility of MRI based on global assessment. Table 3 displays
the mean (range) sensitivity, specificity, and positive and
negative LRs for all 5 readers for the diagnosis of SpA
following global assessment by MRI as well as diagnostic
assignments recorded concordantly by all 3 rheumatologists, by both radiologists, and by ⱖ2 of the 5 readers.
Diagnostic utility was, as expected, very high in patients
with established AS (the mean positive LR and mean
negative LR for all 5 readers were 44.6 and 0.10,
respectively). Specificity was consistently high among all
readers (range 94–99%), while sensitivity was somewhat
lower for rheumatologist readers. The diagnostic utility
of MRI for IBP was also high (the mean positive LR and
negative LR for all 5 readers were 26.0 and 0.50,
respectively), with few differences between rheumatologists and radiologists.
3054
WEBER ET AL
Table 3. Diagnostic utility of MRI for SpA as determined by global assessment of MR images by individual readers and according to diagnostic
assignments recorded concordantly*
Group, readers
AS versus NSBP and HC combined
Mean (range) of 5 readers
Concordant assignments
3 rheumatologists
2 radiologists
ⱖ any 2 readers
AS versus NSBP
Mean (range) of 5 readers
Concordant assignments
3 rheumatologists
2 radiologists
ⱖ any 2 readers
AS versus HC
Mean (range) of 5 readers
Concordant assignments
3 rheumatologists
2 radiologists
ⱖ any 2 readers
IBP versus NSBP and HC
combined
Mean (range) of 5 readers
Concordant assignments
3 rheumatologists
2 radiologists
ⱖ any 2 readers
IBP versus NSBP
Mean (range) of 5 readers
Concordant assignments
3 rheumatologists
2 radiologists
ⱖ any 2 readers
IBP versus HC
Mean (range) of 5 readers
Concordant assignments
3 rheumatologists
2 radiologists
ⱖ any 2 readers
Sensitivity
Specificity
Positive LR
Negative LR
0.90 (0.83–0.97)
0.97 (0.94–0.99)
44.6 (16.3–72.5)
0.10 (0.01–0.18)
0.75
0.87
0.99
0.99
1.0
0.95
67.9
NC
18.6
0.26
0.13
0.01
0.90 (0.83–0.99)
0.97 (0.92–1.0)
NC (12.5–NC)
0.10 (0.01–0.17)
0.75
0.87
0.99
1.0
1.0
0.92
NC
NC
12.8
0.25
0.13
0.01
0.90 (0.83–0.99)
0.97 (0.95–0.98)
40.3 (18.8–58.0)
0.10 (0.01–0.17)
0.75
0.87
0.99
0.99
1.0
0.96
53.4
NC
23.0
0.26
0.13
0.01
0.51 (0.48–0.52)
0.97 (0.94–0.99)
26.0 (8.8–43.3)
0.50 (0.49–0.53)
0.48
0.48
0.52
0.99
1.0
0.95
43.6
NC
9.8
0.53
0.52
0.51
0.51 (0.48–0.52)
0.97 (0.92–1.0)
NC (6.7–NC)
0.50 (0.48–0.54)
0.48
0.48
0.52
1.0
1.0
0.92
NC
NC
6.7
0.52
0.52
0.52
0.51 (0.48–0.52)
0.97 (0.95–0.98)
23.0 (10.2–30.5)
0.50 (0.49–0.53)
0.48
0.48
0.52
0.99
1.0
0.96
34.3
NC
12.1
0.53
0.52
0.50
* Except where indicated otherwise, values are the diagnostic assignments recorded concordantly by all 3 rheumatologists, by both radiologists, and
by at least 2 of the 5 readers. MRI ⫽ magnetic resonance imaging; SpA ⫽ spondylarthritis; LR ⫽ likelihood ratio; AS ⫽ ankylosing spondylitis;
NSBP ⫽ nonspecific back pain; HC ⫽ healthy control; NC ⫽ not calculable (specificity ⫽ 1.0); IBP ⫽ inflammatory back pain.
Diagnostic utility of MRI based on the ASAS
definition of a positive MRI. Table 4 compares the
diagnostic utility of MRI as determined by global evaluation of all scans versus the ASAS definition of a
positive MRI result. While sensitivity increased for all 5
readers when using the ASAS definition, there was a
decrease in specificity when compared with global evaluation of MRI. The diagnostic utility of the ASAS
definition was therefore less than that determined by
global assessment for all 5 readers.
Diagnostic utility of MRI based on the MORPHO
definition of a positive MRI. The inclusion of erosions
improved sensitivity (81%) as compared with the ASAS
definition (67%) for all 5 readers, with minimal change
in specificity, so that overall diagnostic utility was better
(Table 4). Although the positive LR (6.9) was still not
quite as good as global assessment of MRI (positive
LR ⫽ 9.8), the negative LR was better (0.2 versus 0.5).
DISCUSSION
This international multireader MRI standardization, calibration, and reading exercise involving 187
patients with SpA and age- and sex-matched control
subjects demonstrated several findings that carry major
clinical implications for the use of MRI in SpA. First, the
adoption of a systematic and standardized approach to
assessment of the SI joint shows that MRI has much
greater diagnostic utility than has been documented
previously. Second, structural changes occur early in the
DATA-DRIVEN DEFINITION OF MRI POSITIVITY FOR SpA
3055
Table 4. Diagnostic utility of MRI by global assessment of all scans compared with the ASAS and MORPHO definitions of a positive MRI in
patients with IBP*
Diagnosis by overall assessment
Sensitivity
Specificity
Positive LR
Negative LR
Diagnosis by ASAS proposal
Sensitivity
Specificity
Positive LR
Negative LR
Diagnosis by MORPHO proposal
Sensitivity
Specificity
Positive LR
Negative LR
Reader 1
Reader 2
Reader 3
Reader 4
Reader 5
Any 2
readers
0.48
0.98
20.0
0.5
0.52
0.97
14.8
0.5
0.52
0.94
8.8
0.5
0.52
0.99
43.4
0.5
0.52
0.99
43.3
0.5
0.52
0.95
9.8
0.5
0.52
0.93
7.3
0.5
0.59
0.92
7.3
0.4
0.67
0.85
4.5
0.4
0.56
0.94
8.8
0.5
0.67
0.89
6.0
0.4
0.67
0.88
5.7
0.4
0.74
0.86
5.3
0.3
0.63
0.91
7.0
0.3
0.78
0.85
5.2
0.3
0.70
0.92
8.8
0.3
0.74
0.89
6.7
0.3
0.81
0.88
6.9
0.2
* The Assessment of SpondyloArthritis international Society (ASAS) proposal for a positive magnetic resonance image (MRI) is ⱖ2 bone marrow
edema (BME) lesions in 2 distinct sacroiliac joint (SIJ) quadrants on the same slice or ⱖ1 BME lesion extending across 2 SIJ quadrants or ⱖ1 BME
lesion recorded on 2 consecutive slices in the same SIJ quadrant. The MORPHO proposal for a positive MRI is fulfillment of any of the following
3 criteria: BME according to the ASAS definition, erosion in ⱖ2 SIJ quadrants in the same slice or a single SIJ quadrant in 2 consecutive slices, or
BME and erosion in any SIJ quadrant though not necessarily in the same quadrant. IBP ⫽ inflammatory back pain; LR ⫽ likelihood ratio.
disease course and are evident in the SI joint even in
patients with a symptom duration of ⬍24 months. Third,
bone marrow edema and the presence of fat infiltration
in ⬎1 SI joint quadrant or extending into consecutive
slices is relatively nonspecific and may occur even in
healthy, asymptomatic individuals. Fourth, erosions are
relatively specific for SpA. Fifth, limiting assessment to
bone marrow edema may fail to capture significant
diagnostic information available from MR sequences
obtained during routine screening.
Our study protocol incorporated several issues
relevant to rheumatology practice. The inclusion criteria
focused on a young population representing the demographic in which SpA develops and also on patients with
recent-onset SpA who may represent a challenge for
early diagnosis. Young persons with nonspecific back
pain and healthy individuals constitute essential control
participants for studies of diagnostic utility in patients
with early SpA in whom unequivocal radiographic sacroiliitis has yet to develop and therefore reflect a frequent diagnostic challenge in daily practice. MRI protocols using T1-weighted and STIR sequences to evaluate
the SI joints of patients with clinically suspected SpA are
widely used in clinical practice; 2 recent studies showed
that additional expensive and time-consuming contrastenhanced MRI sequences do not improve the diagnostic
utility in this clinical setting compared with that of
T1-weighted and STIR sequences alone for evaluation
of the SI joint (21) and the spine (22). The importance
of calibrating readers from different institutions prior to
MRI reading exercises has been demonstrated in previous studies evaluating the SI joint and the spine in
patients with SpA (23,24).
Concordance among all 5 readers for the diagnosis of SpA by global assessment of the SI joint by MRI
was 85% in the IBP group and 68% in the AS group.
Similar concordance values for the 3 rheumatologists
(89% and 78% for the 2 patient groups) compared with
both radiologists (96% versus 87%) support the external
validity of our study results. A study evaluating active
and structural MRI changes in the SI joints of 68
patients with recent-onset IBP showed concordance
rates between 2 readers of 78–85% for acute inflammation and 81–88% for structural changes (25).
In the AS group, erosion and fat infiltration in
the SI joint as recorded by ⱖ2 readers were as frequent
as bone marrow edema, while bone marrow edema was
observed more frequently than structural lesions in the
IBP group. However, erosions were detected in half of
the IBP group with a mean symptom duration of 29
months; this finding indicates that structural damage of
the SI joint starts early in the disease course, long before
it can be captured by plain radiography. Also, fat
infiltration was recorded in up to ⬃44% of the IBP
population; its specificity for SpA has been a matter of
debate since the early reports on the use of MRI in the
diagnostic evaluation of patients with SpA (26–29). Fat
infiltration is not necessarily inflammation driven. Fur-
3056
ther work is needed to assess the diagnostic utility of fat
infiltration per se or in combination with other MRIvisualized lesions suggestive for SpA.
Bone marrow edema and erosions as well as fat
infiltration were recorded concordantly by ⱖ2 readers in
up to 27% of control subjects with nonspecific back pain
and 24% of healthy volunteers. This observation is
consistent with a previous report describing the occurrence of bone marrow edema in the SI joints of 27% of
patients with mechanical back pain and healthy control
subjects (30) and 26% of healthy volunteers in a recent
study assessing acute spinal lesions by MRI in early SpA
(24). The pathophysiologic basis of these acute and
structural MR changes remains speculative; the most
likely explanations may be mechanically induced signal
alterations or degenerative changes. In 2 persons with
nonspecific back pain and 3 healthy control subjects,
SpA was diagnosed by some readers according to the
global assessment of the MRI scans. Ethical reasons
prevented further examination of these 5 individuals, for
instance, by testing for HLA–B27. The clinical implication from these observations is that low-grade acute
lesions of the SI joint visible on MRI should be interpreted with caution to avoid misclassification of young
persons with back pain as having SpA. Compared with
bone marrow edema–like lesions and fat infiltration,
erosions were observed much less frequently in both
control groups, and they may contribute most to improved specificity.
A clinically relevant finding of our study was that
the specificity obtained by global assessment of MRI of
the SI joint, which reflects daily practice, was greater in
the IBP group than that observed with the more detailed
assessment of both the ASAS (10) and MORPHO study
proposals. This may be partly explained by a possible
reader bias when starting the detailed scoring after
global assessment of the MRI: once the scan is regarded
as negative for SpA, the reader may be less likely to
record inflammatory lesions. However, both detailed
evaluations showed a higher sensitivity, which is desirable in clinical practice to diagnose SpA in individual
patients early in the disease course. The lower negative
LR of the MORPHO study proposal compared with the
other 2 approaches may prove useful in daily practice,
where ruling out a diagnosis of SpA is often as important
as confirming the disorder. Incorporating structural lesions in the detailed assessment defined by the MORPHO study proposal as opposed to the ASAS approach
based only on bone marrow edema resulted in higher
sensitivity while maintaining specificity. To our knowledge, the MORPHO study proposal represents the first
WEBER ET AL
data-driven definition of an MR image positive for SpA.
Whether this evaluation system, encompassing both
active and structural SI joint lesions, is able to enhance
diagnostic utility must be confirmed in larger populations of patients with SpA, particularly in the group with
preradiographic IBP.
Limitations of our study are the cross-sectional
design and the relatively low number of patients with
IBP, who represent the most challenging group of
patients with SpA in daily practice, with the need to
confirm the suspected diagnosis on clinical grounds.
Long-term followup of patients with IBP will allow an
estimation of the sensitivity and specificity of MRI
according to the gold standard of radiographically defined sacroiliitis. The greater sensitivity and hence better
diagnostic utility achieved by the radiologists in this
study was mainly attributable to the more frequent
recognition of structural lesions, suggesting that rheumatologists may require greater awareness and more
intensive training to recognize structural lesions if they
are to improve their ability to diagnose SpA on MRI.
In conclusion, this cross-sectional study, adopting
a systematic and standardized evaluation of acute and
structural lesions of the SI joint, showed that MRI has
much greater diagnostic utility in SpA than has been
documented previously. This study also showed that
low-grade acute and structural SI joint lesions may be
present in patients with nonspecific back pain and
healthy volunteers, with a frequency of up to 27%.
Future studies focusing on standardized evaluation of SI
joint lesions should address the contribution of structural SI joint damage to diagnosis in early SpA. There is
a need for greater awareness and training of rheumatologists in recognizing structural lesions on SI joint
MRI.
ACKNOWLEDGMENTS
We thank the patients and the healthy volunteers for
their participation, and we thank the following Swiss rheumatologists, internists, and primary care physicians for referring
their patients: A. Achermann (Luzern), M. Altermatt (Basel),
C. Boetschi (Romanshorn), E. Bona (Chur), P. Bruehlmann
(Zurich), C. Brunner (Zurich), A. Chamot (Morges), B. Elmiger (Bern), D. Galovic (Pfaeffikon), T. Gerber (Zurich), M.
Giger (Menzingen), D. Glenz (Visp), F. Haefelin (Schlieren),
G. Hajnos (Zurich), C. Harder (Luzern), U. Heusser (Winterthur), U. Hintermann (Brugg), M. Hoppler (Zug), P. Imbach
(Zurich), J. Imholz (Zurich), C. Jeanneret (Schwerzenbach),
D. Kaufmann (Zurich), B. Kleinert (Zurich), R. Kloeti
(Brugg), I. Kramers (Zurich), R. Maager (Aarau), N. Masina
(Lugano), C. Merlin (Baden), A. Rapp (Zurich), J. Ryser
(Zurich), N. Satz (Zurich), A. Schmidt (Basel), H. Schwarz
DATA-DRIVEN DEFINITION OF MRI POSITIVITY FOR SpA
(Basel), S. Studer (Zurich), P. Sutter (Zurich), F. Tapernoux
(Rueti), H. Trost (Zurich), B. Weiss (Basel).
We thank Tracey Clare, Clinical Research Manager,
and Paul Filipow, Data Manager, Department of Radiology,
University of Alberta, Edmonton, Canada for coordinating the
Web-based SPARCC scoring index; Christian Streng, Balgrist
University Hospital, Zurich, Switzerland for his technical
assistance with Figure 1, and Rudolf O. Kissling, MD, Department of Rheumatology, Balgrist University Hospital, Zurich,
Switzerland for scoring the sacroiliac joints (Balgrist patients)
on plain radiographs.
3057
10.
11.
12.
AUTHOR CONTRIBUTIONS
All authors were involved in drafting the article or revising it
critically for important intellectual content, and all authors approved
the final version to be published. Dr. Weber had full access to all of the
data in the study and takes responsibility for the integrity of the data
and the accuracy of the data analysis.
Study conception and design. Weber, Lambert, Hodler, Maksymowych.
Acquisition of data. Weber, Lambert, Østergaard, Hodler, Pedersen,
Maksymowych.
Analysis and interpretation of data. Weber, Lambert, Østergaard,
Hodler, Pedersen, Maksymowych.
13.
14.
15.
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