Head-to-toe whole-body MRI in psoriatic arthritis, axial spondyloarthritis and healthy subjects: first steps towards global inflammation and damage scores of peripheral and axial joints (original) (raw)

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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1Copenhagen Center for Arthritis Research, Copenhagen Center for Rheumatology and Spinal Diseases, University Hospital Copenhagen Glostrup, Copenhagen, 2Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 3Department of Rheumatology and Medicine, University Hospital Copenhagen Gentofte, Copenhagen, Denmark, 4Department of Diagnostic Imaging, Sheba Medical Center, Tel Giborim, Tel Aviv University Israel and 5Department of Radiology, University Hospital Copenhagen Herlev, Copenhagen, Denmark

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Revision received:

17 September 2014

Published:

26 November 2014

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René Panduro Poggenborg, Susanne Juhl Pedersen, Iris Eshed, Inge Juul Sørensen, Jakob M. Møller, Ole Rintek Madsen, Henrik S. Thomsen, Mikkel Østergaard, Head-to-toe whole-body MRI in psoriatic arthritis, axial spondyloarthritis and healthy subjects: first steps towards global inflammation and damage scores of peripheral and axial joints, Rheumatology, Volume 54, Issue 6, June 2015, Pages 1039–1049, https://doi.org/10.1093/rheumatology/keu439
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Abstract

Objectives. By whole-body MRI (WBMRI), we aimed to examine the frequency and distribution of inflammatory 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 conventional 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 (92–100%) and reproducibility (intrareader intraclass correlation coefficient: 0.62–1.0) were high in spine/SI joint, but lower in the distal peripheral joints. Wrists, shoulders, knees, 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) 3–15]} and SpA [8 (IQR 2–14)] than in HSs [2.5 (IQR 1–4.5)], both P < 0.05. WBMRI global structural damage scores (erosion, fat infiltration and ankylosis) were higher in SpA [7 (IQR 3–12)] than HSs [1.5 (IQR 0–4.5)], P = 0.012. Correlations between WBMRI and convMRI spine and SI joint scores were ρ = 0.20–0.78.

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.

Introduction

In the management of PsA and axial SpA, it is important to accurately monitor current disease activity and the amount of structural damage [1]. MRI enables more sensitive assessment of both inflammatory and structural lesions than conventional clinical and radiographic measures [2, 3]. However, both PsA and SpA are characterized by diverse and anatomically widespread disease manifestations, whereas conventional MRI (convMRI) only allows visualization of a small anatomical area at one examination, which limits its ability to provide an overall assessment of disease status in these diseases. Recently, head-to-toe whole-body MRI (WBMRI) has been introduced. This method allows assessment of all peripheral and axial joints, including spine and SI joints, in only one examination [4, 5]. We have previously reported findings of enthesitis using WBMRI and clinical examination in PsA, SpA and healthy subjects (HSs) [6]. Only a few studies have investigated the ability of head-to-toe WBMRI to assess inflammation and/or structural joint damage in patients with PsA [7] or axial SpA [8–10]. None of these studies have compared WBMRI findings of both peripheral and axial arthritis with convMRI or have included healthy subjects (HSs). Furthermore, none of the studies have assessed the possibility of developing WBMRI global inflammation and structural damage scores including both peripheral and axial joints. Thus, further development and validation, including identification of findings in HSs is needed. The perspective is the development of tools for assessment of patient global inflammation and patient global structural damage, capturing both peripheral and axial features.

In this pilot study, we aimed to (i) examine the ability of WBMRI to visualize inflammatory and structural lesions in axial and peripheral joints, (ii) determine the distribution of peripheral and axial involvement in PsA and SpA, (iii) validate findings by comparison with clinical examination, convMRI and by assessing the reproducibility, and (iv) develop WBMRI global inflammation and global structural damage scores.

Methods

Study participants

Patients were eligible for this prospective study if they had PsA according to Moll and Wright’s criteria [11], or SpA according to the European Spondylarthropathy Study Group criteria [12]. PsA patients were included if they had active disease, defined as a tender joint count (TJC) or swollen joint count (SJC) of ≥3 and ≥1 swollen finger joint or dactylitic finger. SpA patients were included if they had a BASDAI [13, 14] score of ≥30 mm (0–100 mm scale) and active spinal disease according to the treating rheumatologist. Treatment with glucocorticoids or initiation of TNFα inhibitor therapy was not allowed within the 4 weeks before study investigations. The study also included a group of HSs, who could not be included if they had pain from peripheral joints or spine, a family history of PsA, SpA or RA, a medical history of psoriasis, anterior uveitis, IBD, or heel pain.

The study was performed in accordance with the Declaration of Helsinki and approved by the Ethical Committee of The Capital Region of Denmark and the Danish Data Protection Agency. Written informed consent was obtained from all study participants before inclusion into the study.

Clinical examinations

The clinical examination included the 76-SJC and 78-TJC [15] and was performed by experienced rheumatologists. BASDAI, BASFI and BASMI were acquired, as were serum CRP, DAS28(CRP) (four variables).

MRI acquisition

All study participants had a head-to-toe WBMRI performed. Patients with PsA also had convMRI of the fingers, including second–fifth MCP, PIP and DIP joints. Patients with axial SpA had convMRI of the SI joints and total spine. The HSs had convMRI performed for the fingers (n = 2) or spine (n = 8), or fingers and spine (n = 2). WBMRI was performed on a 3T high-field MRI unit (Philips Achieva, Best, The Netherlands) using the integrated quadrature body coil. Pre-contrast short tau inversion recovery and pre- and post-contrast T1-weighted turbo spin echo sequences were performed in six stations with coronal slice orientation (cervical, thoracic, lumbar, hips/hands, knees and feet), one station with sagittal (cervical) and one station with axial orientation (feet). convMRI was performed on a 1.5T high-field MRI unit (Philips Achieva, Best, The Netherlands). Details on WBMRI and convMRI acquisition can be found in Table 1. Scan time for WBMRI was ∼ 60 min; scan time for convMRI 20 min for the hands (PsA and HSs) and 40 min for the spine and SI joints (SpA and HSs).

Table 1

Whole-body MRI and conventional MRI imaging protocol for examination of patients with PsA and SpA and healthy subjects

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.

Table 1

Whole-body MRI and conventional MRI imaging protocol for examination of patients with PsA and SpA and healthy subjects

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.

MRI evaluation

WBMRI and convMRI were evaluated separately by an experienced musculoskeletal radiologist (I.E.), who was blinded to all clinical, biochemical and other imaging information and evaluated the images in random order.

By WBMRI, the 76 joints (hereafter named the 76 peripheral joints) included in the 78-TJC minus the TM joints, which were not visualized by WBMRI) were evaluated. Furthermore, each discovertebral unit (DVU) in the spine was evaluated separately in the ventral part (vertebral body) and posterior part (including pedicles, facet joints and spinous processes), whereas the SI joints were evaluated on quadrant level, that is, by dividing each SI joint into upper and lower iliac parts and upper and lower sacral parts. The readability of WBMRI was assessed for all inflammatory and structural lesions in all scanned joint regions. Each joint region was classified into one of three groups: (i) in the field of view (FOV) and possible to evaluate (i.e. readable); (ii) in FOV, but not possible to evaluate; and (iii) not in the FOV (i.e. not scanned).

In readable areas, WBMRI was scored dichotomously (presence/absence) for bone marrow oedema (BMO) and bone erosions (in 76 peripheral joints, spine and SI joints), synovitis (in 76 peripheral joints), fat infiltration (in spine and SI joints) and ankylosis (in SI joints).

convMRI of the hands was scored for synovitis (0–3 per joint), BMO (0–3 per bone) and bone erosion (0–10 per bone), according to the Outcome Measure in the Rheumatology PsA MRI scoring system PsAMRIS [16, 17]. convMRI of the spine was scored for activity (evaluating BMO; 0–3 per DVU) using the Berlin modification of the AS spine MRI activity score [18], and for structural lesions (global score of sclerosis, squaring, erosion, syndesmophytes and bridging/fusion; 0–6 per DVU) using the AS spine MRI-chronicity (ASspiMRI-c) score [19]. convMRI of the SI joint was scored for activity (evaluating bone oedema; 0–4 per quadrant) and structural lesions (global score of bone erosions, sclerosis, joint space width, bone bridging/ankylosis; 0–1 per quadrant) using the Berlin method [1, 20].

Construction of WBMRI scores including WBMRI global scores

After assessment of all MRIs, different WBMRI peripheral joint scores were calculated for synovitis, BMO and erosion in the 76 peripheral joints. WBMRI spine scores were calculated separately for BMO, fat infiltration and erosion by adding scores for vertebral bodies and posterior elements. For WBMRI, SI joint scores were calculated separately for BMO, fat infiltration, erosion and ankylosis by adding the scores from the quadrants. Furthermore, different WBMRI global scores were calculated for BMO, inflammation and structural damage, respectively. The WBMRI global inflammation score was calculated as the sum of synovitis and BMO in the 76 peripheral joints, and BMO in the spine and SI joints. The WBMRI global structural damage score was calculated as the sum of erosions in 76 peripheral joints, spine and SI joints, fat infiltrations in the spine and SI joints and ankylosis in the SI joints.

Statistics

Results are given as median and interquartile range (IQR). The Mann–Whitney test and Fisher’s exact test were used to compare groups. Spearman’s rank correlation coefficient (rho) was used to assess correlations, and values >0.20 but ≤0.50 and >0.50 but ≤0.80 and >0.80 were considered to represent small, moderate and high correlation, respectively. Reliability analyses included intrareader intraclass correlation coefficients (ICCs; two-way mixed model, absolute agreement definition). The statistical analyses were performed in SAS (version 9. SAS Inc., Cary, NC, USA), except for ICCs, which were performed in SPSS version 19 (SPSS Inc., Chicago, IL, USA). P < 0.05 was considered statistically significant.

Results

Clinical findings

The study included 18 patients with PsA, 18 patients with axial SpA, and 12 HSs. The characteristics of the study participants are provided in Table 2. Compared with HSs, patients with PsA and SpA had higher TJCs and SJCs, DAS28(CRP), BASDAI and BASFI (0.0005 < P < 0.05).

Table 2

Baseline characteristics of the study participants

Values are median (IQR) or frequency (%). Disease duration is years since diagnosis. NA: not applicable; SJC: swollen joint count; TJC: tender joint count.

Table 2

Baseline characteristics of the study participants

Values are median (IQR) or frequency (%). Disease duration is years since diagnosis. NA: not applicable; SJC: swollen joint count; TJC: tender joint count.

Readability of WBMRI

Readability was examined in 76 peripheral joints, 23 spinal DVUs and 8 SI joint quadrants (Table 3). Among the 76 peripheral joints evaluated, we found the highest readability for synovitis, BMO and erosions in the knees (94–100%) and hips (97–100%). Distal peripheral joints generally showed lower readability than more proximal joints; for example, BMO could only be evaluated in 10% of feet DIP joints, due to not being in the FOV (37%), or due to insufficient image quality (53%). The elbows could be evaluated in only 5–8%. In the spine and SI joints, all areas showed high readability (≥92%).

Table 3

Whole-body MRI readability and frequency of lesions in PsA and SpA

aConcerning 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.

Table 3

Whole-body MRI readability and frequency of lesions in PsA and SpA

aConcerning 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.

WBMRI findings

Fig. 1 shows examples of inflammatory lesions detected by WBMRI. The distribution of inflammatory and structural changes in the 76 peripheral joints, spine and SI joints examined are shown in Fig. 2.

Fig. 1

Examples of whole-body and conventional MRI in SpA and PsA

(A–F) A 34-year-old male SpA patient with back and knee pain; (G–K) 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).

Fig. 2

Distribution of whole-body MRI inflammatory and structural lesions in PsA (upper row) and SpA (lower row)

For peripheral and axial joints, the frequencies of the findings (in percentage of readable areas) are provided. Results are summarized for left and right side, with colours indicating frequencies.

In peripheral joints, synovitis was overall more frequent than BMO and much more common than erosion. Hand synovitis (particularly in PIP and DIP joints) was more frequent in PsA than in SpA and HSs. In PsA, the frequency of inflammatory involvement (synovitis and BMO) was similar in hands and feet, whereas SpA patients had more inflammatory lesions in feet than in hands. Large joint involvement was frequent in both PsA and SpA, particularly in shoulders (synovitis in 48% and 42%, respectively), wrists (48% and 50%), knees (42% and 17%) and ankles (44% and 31%) (Table 3).

In the spine, BMO (SpA: 10% and PsA: 8% of vertebral bodies) and fat infiltration (SpA: 12%; PsA: 7%) were the most common findings, and both were more common in SpA than in PsA, whereas erosions were rarely observed (Table 3). BMO in the posterior parts of the spine was observed occasionally in PsA (2% of sites) and SpA (0.4%). In SI joints, BMO (SpA: 21% of quadrants; PsA: 4%) and fat infiltration (SpA: 31%; PsA 12%) were most commonly observed, and BMO, fat infiltration, ankylosis and erosions were more frequent in lower quadrants than in upper quadrants (89 v s 67 lesions), whereas no difference was found between sacral and iliac sides (76 v s 80 lesions).

In the SI joints, WBMRI detected BMO in two HSs (Supplementary Fig. S1, available at Rheumatology Online). convMRI of the SI joint in these two HSs revealed BMO in one (Berlin score 2 in one quadrant), but no BMO in the other. Furthermore, convMRI registered BMO (SI joint Berlin score 1 in two quadrants) in one HS without BMO by WBMRI. In three HSs, convMRI as well as WBMRI detected BMO in the cervical vertebrae. They were a 49-year-old man with a family history of psoriasis, a 55-year-old woman who had previously had knee arthroscopy due to knee pain, and a 61-year-old woman with a history of surgery for cervical disc herniation.

WBMRI and convMRI scores

WBMRI and convMRI scores, including global scores, for PsA, SpA and HSs are shown in Table 4. In PsA, WBMRI showed higher BMO scores than in HSs, while there were no overall significant differences in other parameters. In SpA, the global BMO and global structural damage scores were higher than in HSs. Corresponding convMRI revealed higher synovitis scores in the hands in PsA patients, and higher spinal and SI joint structural lesion scores in SpA patients than in HSs (Table 4).

Table 4

Median (IQR) scores of whole-body MRI and conventional MRI findings in joints, discovertebral units and SI joint quadrants

*P < 0.05, Mann–Whitney 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.

Table 4

Median (IQR) scores of whole-body MRI and conventional MRI findings in joints, discovertebral units and SI joint quadrants

*P < 0.05, Mann–Whitney 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.

WBMRI BMO scores for 76 peripheral joints correlated significantly with WBMRI synovitis (ρ = 0.48; P = 0.0006) and erosion (0.51; P = 0.0002). In the spine, WBMRI BMO scores correlated with fat infiltration (0.45; P = 0.001). For the WBMRI scores of the SI joints, BMO correlated with fat infiltration (0.40; P = 0.005) and erosion (0.51; P = 0.0002), and fat infiltration correlated with erosion (0.41; P = 0.004) and ankylosis (0.33; P = 0.02). The WBMRI global BMO score correlated significantly with the WBMRI global structural damage score (ρ = 0.52; P = 0.0002).

WBMRI BMO scores for 76 peripheral joints and WBMRI global BMO correlated with convMRI PsAMRIS synovitis scores (ρ = 0.47–0.52; P < 0.05), but not with BMO scores.

WBMRI and convMRI scores of SI joint BMO, fat infiltration and erosion correlated significantly (ρ = 0.78/0.71/0.72, all P < 0.0005). WBMRI and convMRI SI joint ankylosis scores did not correlate significantly (0.24; P = 0.22). Spine scores of activity and damage by convMRI (Berlin activity score and ASspiMRI-c scores) and corresponding WBMRI scores showed lower correlations (ρ = 0.20–0.55; 0.005 < P < 0.20). Correlation between WBMRI and convMRI scores of synovitis in hands did not reach statistical significance (0.32; P = 0.15).

Association between MRI and clinical examination

WBMRI and convMRI findings were compared with clinical examination. The 28-SJC correlated significantly with BMO assessed by WBMRI in the same 28 joints (all participants: ρ = 0.31; P = 0.04; PsA-only: ρ = 0.54; P = 0.03). In PsA, the SJC and scores of BMO in 76 peripheral joints correlated significantly (ρ = 0.66; P = 0.006). WBMRI synovitis was not significantly correlated with SJC or TJC. Apart from weak correlations between WBMRI BMO and erosion scores for 76 peripheral joints with age (both 0.30, P < 0.05), no significant correlations between peripheral WBMRI scores and patient characteristics or clinical measures of disease activity were found. The WBMRI scores of spinal fat infiltration correlated with BASMI (0.35, P = 0.02), and the SI joint damage score with BASFI (0.29, P = 0.049), whereas no other significant correlations were observed.

The WBMRI global structural damage correlated with BASMI (0.37, P = 0.016), whereas no other significant correlations were observed with patient characteristics, including clinical measures of disease activity.

By convMRI, the PsAMRIS synovitis score correlated statistically significantly with 76-SJC (ρ = 0.45; P = 0.04). The ASspiMRI-c score assessed by convMRI of the spine correlated with BASDAI, BASMI and BASFI (ρ = 0.42; P = 0.023/ρ = 0.50; P = 0.0086/ρ = 0.57; P = 0.0016). No further correlations were found between convMRI scores in the spine and SI joint and clinical outcomes.

WBMRI reliability analysis

The intrareader reproducibility of WBMRI assessments was assessed, comparing original scores with re-anonymized re-scorings of 10 study participants 12 months later. Intrareader ICCs were 0.31–0.85 for synovitis, BMO and erosion in the 76 peripheral joints, 0.62–0.68 for BMO and fat infiltration in the spine, and 0.81–1.0 for BMO, fat infiltration, erosion and ankylosis in the SI joints.

Discussion

This prospective pilot study of HSs and patients with PsA or axial SpA demonstrated the ability of head-to-toe WBMRI to assess overall disease activity and structural damage. The readability was good in axial and proximal peripheral joints, while it decreased in more distally located peripheral joints. The pattern of inflammatory and structural changes in SpA and PsA was described. SI joint involvement was most frequent in SpA, while peripheral joint involvement, particularly in knees and hand MCP and PIP joints, was most frequent in PsA. WBMRI findings correlated moderately with clinical findings. The reproducibility of the measurements was dependent on the measured parameter and site, with the best result for axial joints.

A detailed evaluation of the ability of WBMRI to visualize inflammatory and structural changes in different parts of the body was undertaken. Some areas, such as hips, knees, spine and SI joints, were almost always successfully visualized, whereas other areas were more difficult—including the elbows and distal joints of the hands and feet. Poorer readability had several causes, including movement artefacts, longer distance from the centre of the MRI unit decreasing field homogeneity (off-centre artefact) and consequently image quality, and smaller size of the joint causing insufficient spatial resolution. Areas like the spine, SI joint and knee were favoured by being positioned close to the coil and the centre of the magnetic field, providing very good readability. Although image acquisition was not consistently of sufficient quality for robust and reliable assessment of all joints of interest, the study demonstrated important aspects of joint involvement in PsA and SpA and illustrated the large future potential of WBMRI to assess these anatomically widespread diseases. Improved hardware becoming available currently and in the future will undoubtedly increase the clinical utility of WBMRI, as will further refined techniques of image acquisition and evaluation. Furthermore, more optimal positioning of the patient in the scanner may facilitate reliable assessment of peripheral joints.

We described the pattern of WBMRI joint involvement in PsA and SpA (Fig. 2). Only a few studies have investigated head-to-toe WBMRI in prospective studies of patients with PsA [7] or SpA [8–10]. In agreement with these, we found widespread inflammation. Inflammatory lesions outside the axial joints were frequent, in both SpA and PsA, which is in agreement with a previous WBMRI pilot study of SpA patients [21]. In PsA, the joints most frequently involved were wrists, shoulders, ankles, knees, MCP and MTP joints. The same pattern was seen in SpA, except that MCP joints were replaced with hip joints. Spine and SI joint involvement were seen in both diseases, but most frequently in SpA, as expected when the PsA population was selected based on peripheral involvement. The DIP joints are often clinically affected in PsA [22], but we rarely detected DIP synovitis or BMO. The fact that some joints were involved to a different extent than expected, for example, that MCP involvement was frequent while DIP joint involvement was rare, may be related both to WBMRI revealing subclinical disease and to the fact that very small joints are more difficult to assess by WBMRI, and therefore may be falsely negative. Future studies, with larger sample sizes and improved techniques, are needed to confirm the pattern of joint involvement.

In the present study, BMO was registered by WBMRI in some HSs. This indicates the need to define appropriate definitions and cut-offs of pathology on WBMRI in future studies before the method is used in clinical practice. Nevertheless, BMO was markedly more frequent in PsA and SpA. Of particular importance are the findings of BMO in SI joints, as such changes are part of the definition of axial SpA in the ASAS criteria for axial SpA [23, 24]. Both convMRI and WBMRI detected BMO in two SI joints of HSs. The extent was, however, limited to 1–2 quadrants. These findings are in agreement with previous convMRI studies in HSs, which report that BMO can be seen in up to one-quarter of healthy controls [25].

The correlation between findings by MRI and by clinical examination was investigated. BMO scores correlated significantly with SJC in PsA, supporting the construct validity of WBMRI BMO scores. In contrast, no association was found between WBMRI synovitis and clinical joint counts. Furthermore, the intrareader reproducibility of peripheral synovitis was low. This indicates that WBMRI assessment of synovitis was difficult in several joints, even though the results probably also partly reflect detection of subclinical inflammation. convMRI is an established method for assessing joint inflammation, and the WBMRI technique differs from convMRI mainly in the much larger area visualized, at the cost of lower image resolution. Probably, higher image resolution and quality than available in the present study will markedly improve the WBMRI assessment of synovitis.

We found a correlation between the SI joint structural damage score and BASFI. We also found that WBMRI spinal BMO and spinal fat infiltration correlated with the metrology index BASMI. This finding adds to an earlier investigation by Althoff et al. [26], who found a correlation between WBMRI inflammation and clinical symptoms. In contrast, Weber et al. [27] found no association between WBMRI assessments and clinical outcomes. In a recent study of WBMRI during anti-TNF treatment, it was reported that change in BASDAI and BASFI correlated with changes in MRI SI joint scores, whereas no correlation was found between MRI spine scores and clinical parameters [9].

We found a moderate agreement between WBMRI and convMRI scores. In SpA, investigation of inflammatory SI joint lesions by WBMRI has previously been compared with convMRI, finding a strong correlation and comparable reliability between the two methods, but no correlation with clinical measures [28]. This study, however, did not examine head-to-toe, but only the SI joints and spine, providing an overall higher imaging quality. Furthermore, it should be noted that the true gold standard for WBMRI is not convMRI, but rather biopsies for inflammatory features, and CT for structural lesions [29]. Future studies including such standard reference methods would be highly relevant.

In the present study, structural lesion scores by convMRI (ASspiMRI-c score and Berlin structural lesion SI joint score) were significantly higher in SpA than in HSs (as were the WBMRI global structural damage scores), and they were also correlated with BASMI, BASFI and BASDAI. Overall, the present and earlier studies have found a low to moderate correlation with clinical findings, indicating that WBMRI does more than provide information already available.

The reliability of WBMRI assessments ranged from poor to excellent for different features. The limited reproducibility in some areas is a consequence of acquiring images at the limits of what is possible technically, and perfect visualization of all features by WBMRI was not expected prior to study initiation. Re-reading of the WBMRIs was performed 1 year after the original readings, and as WBMRI assessment is not routine work, the internal calibration of the reader may have declined between readings. Only a few studies have reported ICCs for WBMRI [9, 10, 30]. However, although high ICCs (>0.85) were reported therein, the reliability in those studies was tested using different techniques. In particular, dedicated coils were applied, positioned close to the various imaged parts of the patients, while such coils were not available in our scanner (in which images were acquired using the integrated quadrature body coil of the unit). Furthermore, the reliabilities reported did not reflect assessment of the entire body but only of the spine, SI joints and, in one case [10], pelvic entheses. To optimize reliability, improved imaging acquisition, revised precise definitions of the scored features, and more extensive reader training and calibration are needed.

In conclusion, this study showed that WBMRI allows assessment of peripheral and axial joints in patients with PsA and SpA. Readability was high for spine, SI joints and proximal peripheral joints, but lower for more distally located joints. Patterns of joint involvement were identified. WBMRI is a very promising tool for global assessment of disease activity and damage in PsA and SpA, and the present study encourages further research aiming at optimization of image acquisition, and assessment and validation in longitudinal studies.

Rheumatology key messages

• Whole-body MRI can visualize inflammatory and structural changes in PsA and SpA patients.
• Bone marrow oedema is more frequent in PsA and SpA patients than in healthy subjects.
• With further optimization, whole-body MRI could be a future tool for global disease assessment.

Acknowledgements

The authors acknowledge the assistance of study participants, radiographers, study nurses and laboratory staff who participated in the study. The study was conducted without any financial support. René Panduro Poggenborg has during his Ph.D. study received grants from The Danish Rheumatism Association, the Scandinavian Journal of Rheumatology and The Danish Psoriasis Research Foundation, and was furthermore supported by The Capital Region of Denmark.

Disclosure statement: The authors have declared no conflicts of interest.

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© 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

Topic:

• magnetic resonance imaging
• idiopathic hypertrophic subaortic stenosis
• inflammation
• henoch-schoenlein purpura
• ankle
• arthritis, psoriatic
• hallermann's syndrome
• knee region
• metatarsophalangeal joint
• prostate-specific antigen
• sacroiliac joint
• spondylarthritis
• synovitis
• toes
• wrist
• ankylosis
• shoulder region
• spine
• erosion
• bone marrow edema
• readability
• nuclear magnetic resonance imaging whole body

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