Académique Documents
Professionnel Documents
Culture Documents
RHEUMATOLOGY doi:10.1093/rheumatology/keu439
Advance Access publication 26 November 2014
Original article
Head-to-toe whole-body MRI in psoriatic
arthritis, axial spondyloarthritis and healthy
subjects: first steps towards global
inflammation and damage scores of
Abstract
Objectives. By whole-body MRI (WBMRI), we aimed to examine the frequency and distribution of inflam-
matory and structural lesions in PsA patients, SpA patients and healthy subjects (HSs), to introduce global
WBMRI inflammation/damage scores, and to assess WBMRI’s reproducibility and correlation with con-
ventional MRI (convMRI).
Methods. WBMRI (3.0-T) of patients with peripheral PsA (n = 18) or axial SpA (n = 18) and of HS (n = 12)
was examined for proportion of evaluable features (readability) and the presence and pattern of lesions in
axial and peripheral joints. Furthermore, global WBMRI scores of inflammation and structural damage
were constructed, and WBMRI findings were compared with clinical measures and convMRI (SpA/HS:
spine and SI joints; PsA/HS: hand).
Results. The readability (92100%) and reproducibility (intrareader intraclass correlation coefficient:
0.621.0) were high in spine/SI joint, but lower in the distal peripheral joints. Wrists, shoulders, knees,
CLINICAL
SCIENCE
ankles and MTP joints were most commonly involved, with frequency of synovitis > bone marrow oedema
(BMO) > erosion. WBMRI global BMO scores of peripheral and axial joints were higher in PsA {median 7
[interquartile range (IQR) 315]} and SpA [8 (IQR 214)] than in HSs [2.5 (IQR 14.5)], both P < 0.05.
WBMRI global structural damage scores (erosion, fat infiltration and ankylosis) were higher in SpA
[7 (IQR 312)] than HSs [1.5 (IQR 04.5)], P = 0.012. Correlations between WBMRI and convMRI spine
and SI joint scores were r = 0.200.78.
Conclusion. WBMRI allows simultaneous assessment of peripheral and axial joints in PsA and SpA, and
the distribution of inflammatory and structural lesions and global scores can be determined. The study
strongly encourages further development and longitudinal testing of WBMRI techniques and assessment
methods in PsA and SpA.
Key words: psoriatic arthritis, spondyloarthritis, MRI, clinical examination, healthy subject.
1
Copenhagen Center for Arthritis Research, Copenhagen Center for
Rheumatology and Spinal Diseases, University Hospital Copenhagen
Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of
Submitted 12 March 2014; revised version accepted
Health and Medical Sciences, University of Copenhagen, 3Department
17 September 2014
of Rheumatology and Medicine, University Hospital Copenhagen
Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Correspondence to: René Panduro Poggenborg, Copenhagen Center
Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and for Rheumatology and Spinal Diseases (VRR), Glostrup Hospital,
5
Department of Radiology, University Hospital Copenhagen Herlev, Nordre Ringvej 57, DK-2600 Glostrup, Denmark.
Copenhagen, Denmark E-mail: poggenborg@dadlnet.dk
! The Author 2014. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oup.com
René Panduro Poggenborg et al.
1040 www.rheumatology.oxfordjournals.org
www.rheumatology.oxfordjournals.org
TABLE 1 Whole-body MRI and conventional MRI imaging protocol for examination of patients with PsA and SpA and healthy subjects
Subjects Sequence Stations Orientation TR, ms TE, ms TI, ms FOV, mm Matrix Thk, mm Gap, mm Time, min:s
WBMRI (3T)
All T1 Cervical, thoracic, lumbar, knee, Coronal 733 7.6 — 470 253259 312 171 5 0.5 2:15
Hips/hands, feet 1099 428 228 3 0.3 3:37
Feet Axial 2:15
Neck Sagittal 916 312 168 4 0.4 3:37
STIR Cervical, thoracic, lumbar, hips/ Coronal 6572 70 200 470 279287 256 104 5 0.5 1:03
hands, knee, feet
Feet Axial
Cervical Sagittal 5258
Hips Coronal 13 905 83 380 213 3 0.3 4:38
Conventional
MRI (1.5T)
PsA + HS T1 Hand Coronal 40 12 — 120 120 150 150 0.8 0 5:01
STIR 4548 30 150 120 120 148 149 2 4:24
SpA + HS T1 Cervical, thoracic, lumbar Sagittal 400 7.4 — 270 270 300 216 4 0.4 2:59
SI joints Oblique coronal 550 14 300 270 320 171 2:55
STIR Cervical, thoracic, lumbar Sagittal 5000 80 120 270 270 272 216 0.8 4:10
SI joints Oblique coronal 2500 60 160 300 239 256 163 2:05
T1: T1-weighted sequences acquired before and after administration of gadoteric acid (Dotarem, Guerbet, 0.5 mmol/ml, 0.2 ml/kg). Conventional MRIs of the spine and SI joints are
without contrast. WBMRI: whole-body MRI; FOV: field of view; Gap: gap between slices; HS: healthy subjects; STIR: short tau inversion recovery; TE: echo time; TI: inversion time;
Thk: slice thickness; TR: repetition time.
Whole-body MRI in PsA and SpA
1041
Downloaded from https://academic.oup.com/rheumatology/article-abstract/54/6/1039/1799654 by guest on 15 March 2019
René Panduro Poggenborg et al.
which were not visualized by WBMRI) were evaluated. coefficient (rho) was used to assess correlations, and
Furthermore, each discovertebral unit (DVU) in the spine values >0.20 but 40.50 and >0.50 but 40.80 and
was evaluated separately in the ventral part (vertebral >0.80 were considered to represent small, moderate
body) and posterior part (including pedicles, facet and high correlation, respectively. Reliability analyses
joints and spinous processes), whereas the SI joints included intrareader intraclass correlation coefficients
were evaluated on quadrant level, that is, by dividing (ICCs; two-way mixed model, absolute agreement defin-
each SI joint into upper and lower iliac parts and ition). The statistical analyses were performed in SAS (ver-
upper and lower sacral parts. The readability of WBMRI sion 9. SAS Inc., Cary, NC, USA), except for ICCs, which
was assessed for all inflammatory and structural lesions in were performed in SPSS version 19 (SPSS Inc., Chicago,
all scanned joint regions. Each joint region was classified IL, USA). P < 0.05 was considered statistically significant.
into one of three groups: (i) in the field of view (FOV) and
1042 www.rheumatology.oxfordjournals.org
Whole-body MRI in PsA and SpA
Values are median (IQR) or frequency (%). Disease duration is years since diagnosis. NA: not applicable; SJC: swollen joint
count; TJC: tender joint count.
TABLE 3 Whole-body MRI readability and frequency of lesions in PsA and SpA
76 peripheral joints
Shoulders and AC joints (4) 93/0 90/0 92/0 32 (48) 27 (42) 19 (31) 15 (23) 0 (0) 5 (8)
Elbows (2) 8/0 6/0 5/0 3 (75) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
Wrists and first CMC joints (4) 84/0 83/1 86/0 33 (55) 29 (52) 14 (23) 10 (19) 6 (10) 5 (8)
MCP joints (10) 83/1 79/6 84/16 40 (28) 18 (13) 13 (10) 4 (3) 2 (1) 3 (2)
PIP joints (10) 65/9 59/14 69/8 20 (17) 8 (7) 10 (9) 6 (7) 4 (3) 0 (0)
DIP joints (8) 40/17 28/28 48/11 3 (5) 0 (0) 3 (6) 1 (4) 0 (0) 0 (0)
First sternocostal joints (2) 71/0 66/0 77/0 3 (15) 2 (7) 1 (6) 2 (7) 1 (5) 0 (0)
Hips (2) 99/0 97/0 100/0 6 (17) 6 (17) 1 (3) 1 (3) 0 (0) 2 (6)
Knees (2) 100/0 94/0 100/0 15 (42) 6 (17) 4 (11) 3 (10) 2 (6) 0 (0)
Ankles and TMT joints (4) 95/1 91/1 95/1 28 (42) 22 (32) 11 (17) 7 (11) 0 (0) 2 (3)
Feet MTP joints (10) 83/3 73/6 88/1 41 (28) 52 (34) 19 (16) 16 (12) 13 (8) 5 (3)
Feet PIP joints (10) 61/10 32/37 78/3 15 (14) 10 (8) 13 (25) 14 (22) 5 (4) 2 (1)
Feet DIP joints (8) 45/16 10/53 61/10 0 (0) 4 (6) 1 (6) 0 (0) 0 (0) 0 (0)
Cervical vertebral bodies (6) 96/0 93/0 96/0 10 (10) 18 (17) 20 (20) 17 (17) 1 (1) 0 (0)
Cervical posterior parts (6) 96/0 94/0 97/0 1 (1) 0 (0) 5 (5) 0 (0) 0 (0) 0 (0)
Thoracic vertebral bodies (12) 100/0 100/0 100/0 13 (6) 21 (10) 9 (4) 17 (8) 0 (0) 0 (0)
Thoracic posterior parts (12) 100/0 100/0 100/0 0 (0) 1 (0) 3 (1) 2 (1) 0 (0) 0 (0)
Lumbar vertebral bodies (5) 100/0 95/0 100/0 5 (6) 11 (12) 3 (4) 7 (8) 0 (0) 0 (0)
Lumbar posterior parts (5) 100/0 97/0 100/0 0 (0) 0 (0) 1 (1) 0 (0) 0 (0) 0 (0)
SI joint quadrants (8) 94/0 92/1 94/0 17 (12) 44 (31) 5 (4) 30 (21) 14 (10) 30 (21)
a
Concerning readability: areas are divided into readable (left value), in FOV, but not readable (right value), and not in FOV
(value not shown). For example: 79% of MCP joints could be evaluated for BMO, 6% of MCP joints were in FOV but could not
be evaluated for BMO and 15% of MCP joints were not in FOV. bFrequency of lesions is shown as number of detected
lesions, with the frequency (%) per readable area in brackets. A total of 76 peripheral and axial joints were assessed for
synovitis, BMO and bone erosions, and the spine and SI joint were assessed for fat infiltration, BMO and bone erosions.
Spinal DVUs were assessed separately for vertebral bodies and posterior elements. Parentheses in the left column contain
numbers of joints, DVUs or SI joint quadrants assessed. PIP joints include the interphalangeal joints. AC: acromioclavicular;
BMO: bone marrow oedema; DVU: discovertebral unit; FOV: field of view; TMT: tarsometatarsal.
www.rheumatology.oxfordjournals.org 1043
René Panduro Poggenborg et al.
(AF) A 34-year-old male SpA patient with back and knee pain; (GK) a 32-year-old female with recent onset PsA with
swelling of finger joints. (A) Whole-body MRI (WBMRI) T1-weighted (T1w) fat-saturated (FS) coronal image. (B) WBMRI
post-contrast T1w FS coronal image of right knee, with synovitis at arrow. (C) WBMRI post-contrast T1w FS coronal
image of left knee with synovitis at arrow (zoomed view of left knee shown in (A). (D and E) WBMRI pre- (D) and post- (E)
contrast T1w coronal images of right acromioclavicular (AC) joint (black arrow in D shows AC joint; white arrow in E shows
synovitis). (F) WBMRI T1w coronal image of the SI joints; arrow shows ankylosis. (G) WBMRI T1w coronal image of SI
joints (normal). (H and I) conventional MRI pre- (H) and post- (I) contrast coronal images of second (right) and third (left)
MCP (lower) and PIP (upper) joints, with synovitis at arrows; (J and K) WBMRI pre- (J) and post- (K) contrast coronal
images of the second and third MCP joints shown in (H) and (I), with synovitis at arrows (PIP joints not in field of view).
1044 www.rheumatology.oxfordjournals.org
Whole-body MRI in PsA and SpA
FIG. 2 Distribution of whole-body MRI inflammatory and structural lesions in PsA (upper row) and SpA (lower row)
in upper quadrants (89 vs 67 lesions), whereas no differ- patients, and higher spinal and SI joint structural lesion
ence was found between sacral and iliac sides (76 vs 80 scores in SpA patients than in HSs (Table 4).
lesions). WBMRI BMO scores for 76 peripheral joints correlated
In the SI joints, WBMRI detected BMO in two HSs significantly with WBMRI synovitis (r = 0.48; P = 0.0006)
(Supplementary Fig. S1, available at Rheumatology and erosion (0.51; P = 0.0002). In the spine, WBMRI
Online). convMRI of the SI joint in these two HSs revealed BMO scores correlated with fat infiltration (0.45;
BMO in one (Berlin score 2 in one quadrant), but no BMO P = 0.001). For the WBMRI scores of the SI joints, BMO
in the other. Furthermore, convMRI registered BMO (SI correlated with fat infiltration (0.40; P = 0.005) and erosion
joint Berlin score 1 in two quadrants) in one HS without (0.51; P = 0.0002), and fat infiltration correlated with ero-
BMO by WBMRI. In three HSs, convMRI as well as sion (0.41; P = 0.004) and ankylosis (0.33; P = 0.02). The
WBMRI detected BMO in the cervical vertebrae. They WBMRI global BMO score correlated significantly with
were a 49-year-old man with a family history of psoriasis, the WBMRI global structural damage score (r = 0.52;
a 55-year-old woman who had previously had knee arth- P = 0.0002).
roscopy due to knee pain, and a 61-year-old woman with WBMRI BMO scores for 76 peripheral joints and
a history of surgery for cervical disc herniation. WBMRI global BMO correlated with convMRI PsAMRIS
synovitis scores (r = 0.470.52; P < 0.05), but not with
BMO scores.
WBMRI and convMRI scores
WBMRI and convMRI scores of SI joint BMO, fat infil-
WBMRI and convMRI scores, including global scores, for tration and erosion correlated significantly (r = 0.78/0.71/
PsA, SpA and HSs are shown in Table 4. In PsA, WBMRI 0.72, all P < 0.0005). WBMRI and convMRI SI joint anky-
showed higher BMO scores than in HSs, while there were losis scores did not correlate significantly (0.24; P = 0.22).
no overall significant differences in other parameters. In Spine scores of activity and damage by convMRI (Berlin
SpA, the global BMO and global structural damage scores activity score and ASspiMRI-c scores) and corresponding
were higher than in HSs. Corresponding convMRI re- WBMRI scores showed lower correlations (r = 0.200.55;
vealed higher synovitis scores in the hands in PsA 0.005 < P < 0.20). Correlation between WBMRI and
www.rheumatology.oxfordjournals.org 1045
René Panduro Poggenborg et al.
TABLE 4 Median (IQR) scores of whole-body MRI and conventional MRI findings in joints, discovertebral units and SI
joint quadrants
Whole-body MRI
Conventional MRI
*P < 0.05, MannWhitney test vs healthy subjects. Possible ranges of scores are shown in parentheses after each feature.
Global inflammation score is the sum of synovitis and global BMO score. Global structural damage score is the sum of bone
erosions, fat infiltration and ankylosis. WBMRIs with very low readability (<33%) for assessed features were excluded. 76-
joints: joints included in the 78-tender joint count except for the TM joints; ASspiMRI-c: AS spine MRI scoring system
chronicity score; BMO: bone marrow oedema; DVU: discovertebral unit; PsAMRIS: PsA MRI scoring system.
convMRI scores of synovitis in hands did not reach stat- By convMRI, the PsAMRIS synovitis score correlated
istical significance (0.32; P = 0.15). statistically significantly with 76-SJC (r = 0.45; P = 0.04).
The ASspiMRI-c score assessed by convMRI of the
Association between MRI and clinical examination spine correlated with BASDAI, BASMI and BASFI
(r = 0.42; P = 0.023/r = 0.50; P = 0.0086/r = 0.57;
WBMRI and convMRI findings were compared with clin- P = 0.0016). No further correlations were found between
ical examination. The 28-SJC correlated significantly with convMRI scores in the spine and SI joint and clinical
BMO assessed by WBMRI in the same 28 joints (all par- outcomes.
ticipants: r = 0.31; P = 0.04; PsA-only: r = 0.54; P = 0.03).
In PsA, the SJC and scores of BMO in 76 peripheral joints WBMRI reliability analysis
correlated significantly (r = 0.66; P = 0.006). WBMRI syno- The intrareader reproducibility of WBMRI assessments
vitis was not significantly correlated with SJC or TJC. was assessed, comparing original scores with re-
Apart from weak correlations between WBMRI BMO and anonymized re-scorings of 10 study participants 12
erosion scores for 76 peripheral joints with age (both 0.30, months later. Intrareader ICCs were 0.310.85 for syno-
P < 0.05), no significant correlations between peripheral vitis, BMO and erosion in the 76 peripheral joints,
WBMRI scores and patient characteristics or clinical 0.620.68 for BMO and fat infiltration in the spine, and
measures of disease activity were found. The WBMRI 0.811.0 for BMO, fat infiltration, erosion and ankylosis
scores of spinal fat infiltration correlated with BASMI in the SI joints.
(0.35, P = 0.02), and the SI joint damage score with
BASFI (0.29, P = 0.049), whereas no other significant cor- Discussion
relations were observed.
The WBMRI global structural damage correlated with This prospective pilot study of HSs and patients with PsA
BASMI (0.37, P = 0.016), whereas no other significant cor- or axial SpA demonstrated the ability of head-to-toe
relations were observed with patient characteristics, WBMRI to assess overall disease activity and structural
including clinical measures of disease activity. damage. The readability was good in axial and proximal
1046 www.rheumatology.oxfordjournals.org
Whole-body MRI in PsA and SpA
peripheral joints, while it decreased in more distally techniques, are needed to confirm the pattern of joint
located peripheral joints. The pattern of inflammatory involvement.
and structural changes in SpA and PsA was described. In the present study, BMO was registered by WBMRI in
SI joint involvement was most frequent in SpA, while per- some HSs. This indicates the need to define appropriate
ipheral joint involvement, particularly in knees and hand definitions and cut-offs of pathology on WBMRI in future
MCP and PIP joints, was most frequent in PsA. WBMRI studies before the method is used in clinical practice.
findings correlated moderately with clinical findings. The Nevertheless, BMO was markedly more frequent in PsA
reproducibility of the measurements was dependent on and SpA. Of particular importance are the findings of BMO
the measured parameter and site, with the best result in SI joints, as such changes are part of the definition of
for axial joints. axial SpA in the ASAS criteria for axial SpA [23, 24]. Both
A detailed evaluation of the ability of WBMRI to visualize convMRI and WBMRI detected BMO in two SI joints of
www.rheumatology.oxfordjournals.org 1047
René Panduro Poggenborg et al.
1048 www.rheumatology.oxfordjournals.org
Whole-body MRI in PsA and SpA
16 Boyesen P, McQueen FM, Gandjbakhch F et al. The international Society classification criteria for axial spon-
OMERACT Psoriatic Arthritis Magnetic Resonance dyloarthritis (part II): validation and final selection. Ann
Imaging Score (PsAMRIS) is reliable and sensitive to Rheum Dis 2009;68:77783.
change: results from an OMERACT workshop. 24 Rudwaleit M, Jurik AG, Hermann KG et al. Defining active
J Rheumatol 2011;38:20348. sacroiliitis on magnetic resonance imaging (MRI) for clas-
17 Ostergaard M, McQueen F, Wiell C et al. The OMERACT sification of axial spondyloarthritis: a consensual approach
psoriatic arthritis magnetic resonance imaging scoring by the ASAS/OMERACT MRI group. Ann Rheum Dis 2009;
system (PsAMRIS): definitions of key pathologies, sug- 68:15207.
gested MRI sequences, and preliminary scoring system 25 Weber U, Maksymowych WP. Sensitivity and specificity of
for PsA Hands. J Rheumatol 2009;36:181624. magnetic resonance imaging for axial spondyloarthritis.
18 Haibel H, Rudwaleit M, Brandt HC et al. Adalimumab re- Am J Med Sci 2011;341:2727.
duces spinal symptoms in active ankylosing spondylitis:
www.rheumatology.oxfordjournals.org 1049