Abstract
Psoriatic arthritis (PsA) is an inflammatory joint disease characterised by the presence of arthritis and often enthesitis and/or spondylitis in patients with psoriasis. However, it presents a wide range of disease manifestations in various patterns. Imaging is an important part of management of PsA, and is used for multiple reasons including establishing/confirming a diagnosis of inflammatory joint disease, determining the extent of disease, monitoring activity and damage, assessing therapeutic efficacy, and identifying complications of disease or treatment, in the setting of clinical practice or clinical studies. Magnetic resonance imaging (MRI) allows detailed assessment of all peripheral and axial joints involved in PsA, and can visualise both inflammation and structural changes. Ultrasonography (US) can visualise many of the peripheral heterogeneous tissue compartments affected by PsA. In contrast to MRI, US is not useful for assessing axial involvement in the spine and sacroiliac joints. In this paper, we will provide an overview of the status, strengths and limitations of MRI and US in peripheral PsA in routine clinical practice and clinical trials.
Introduction
Psoriatic arthritis (PsA) is a chronic inflammatory joint disease associated with the skin disease psoriasis . It is characterised by arthritis, enthesitis, spondylitis and/or dactylitis. PsA was first described as a distinct rheumatic disease in the 1950s and subsequently in the 1970s as part of spondyloarthropathy (SpA) . Differential diagnoses include rheumatoid arthritis (RA), SpA including ankylosing spondylitis (AS), osteoarthritis (OA), gout and fibromyalgia.
Different imaging procedures, primarily conventional radiography, ultrasonography (US) and magnetic resonance imaging (MRI), all having different strengths and limitations, can be used in suspected or established PsA and provide important information on the disease process. Conventional MRI allows high-resolution visualisation of all structures involved in arthritis, and is sensitive for peripheral and axial disease manifestations. US can visualise the peripheral joints and entheses involved in PsA with high resolution and can guide invasive procedures. However, MRI and US in PsA have received less attention than in RA . However, new studies and developments are constantly emerging, and improved techniques and novel imaging methods such as whole-body MRI, dynamic contrast-enhanced MRI and very high-resolution US are exciting future options. Here, we review MRI and US in terms of technique and findings, diagnosing and management of peripheral PsA in clinical practice, monitoring PsA in clinical trials, and new methodological developments and research agenda. A description of the importance of MRI in axial joints, and the utility of other imaging modalities, such as conventional radiography and computed tomography, is beyond the scope of the present paper.
Ultrasonography
US technique and findings
Musculoskeletal US uses non-ionising sound waves to visualise soft tissues in high detail. It can visualise tendons, entheses, ligaments, synovial recesses, skin and nails ( Fig. 1 ). Of note, ultrasound cannot visualise intraosseous structures but can discern cortical defects on the osteal surface and osteoproliferation. Vascularity within the soft tissues can also be detected without the use of contrast using power Doppler or colour flow Doppler. Sonography has the added advantage of being used at the bedside and on multiple areas, with the optional use of dynamic scanning as well as directed according to patient’s symptoms. In contrast to RA, PsA can affect multiple soft tissue compartments and a variable presentation of synovitis from polyarticular patterns to asymmetric oligoarthritis. In the following section, key sonopathoanatomical findings found in PsA are briefly discussed.
Enthesitis
The importance of enthesitis is denoted by its inclusion in the ClASsification of Psoriatic ARthritis (CASPAR) criteria . Several sonographic entheseal schemes have been published . On the whole, these have reasonable reliability, sensitivity and responsiveness . However, these have not been the designed specifically for PsA but for SpA in general. The majority of these are heavily weighted to include lower extremities entheses. This is problematic since mechanical changes at the lower extremity entheses can have similar appearances to inflammatory enthesitis and can occur in individuals with obesity and with diabetes . A significant proportion of patients with PsA or psoriasis have higher body mass indices. A recent study by Eder et al. revealed that the Madrid Sonographic Enthesitis Index (MASEI) was unable to distinguish patients with PsA, psoriasis and controls when the BMI was greater than 30 . In addition to selecting entheses, there needs to be agreement over what types of elementary changes to examine. Consensus agreement for including tendon hypoechogenicity, tendon thickening, calcification, enthesophytes, erosions and the Doppler activity was recently published . However, bursitis did not reach consensus agreement to be included. Furthermore, areas such as the posterior tibial tendon, extensor tendons of the hand at the metacarpophalangeal (MCP) or proximal interphalangeal (PIP), and ligaments and palmar/plantar plate structures were not considered. There is therefore a need to include structures that are more relevant to PsA and that may be less prone to mechanical factors.
Synovitis
Patients with PsA can have a heterogeneous pattern of joint involvement in addition to significant extra-articular tissue involvement. This may be manifested by soft tissue oedema, joint peri-enthesitis or tendinitis and osteoproliferation. The presence of synovitis, tenosynovitis vascularity, synovial fluid and bony changes including erosions and osteoproliferation can be demonstrated with US . Erosions may not have the same morphology as that in RA and may appear shallow. Although similar numbers of erosions may occur in PsA and RA, the erosions have less preponderance for radial aspects of the MCP joints and on micro-CT, and the morphology was mostly omega shaped and tubule shaped . In contrast to this study, most RA erosions were U shaped.
Dactylitis
Dactylitis is a characteristic feature of PsA. It is associated with increased incidence of erosive disease. Although soft tissue thickening, synovitis, extensor tendon thickening and flexor tenosynovitis have been identified by US, a wider involvement of the digital tissues has been demonstrated by MRI . These have included collateral ligament as well as palmar or plantar plate involvement. Of note, the nail or the nail matrix has not been systematically studied in relationship to dactylitis. The OMERACT group is currently developing a sonographic outcome measure for dactylitis.
Onychopathy
Nail dystrophy may be associated with a threefold increased chance of having PsA in patients with psoriasis . In addition, it may be associated with a higher incidence of subclinical enthesopathy at the upper and lower extremities . The nail matrix can be involved resulting in pitting. When the nail bed is affected, thickening of the nail bed, oil spots and onycholysis may be seen. The extensor slip or tendon has an intimate insertion about the nail matrix area giving rise to the suggestion of the nail-extensor tendon entheseal complex . The nail can be demonstrated as an apparent bilayer on US with obliteration of the bilayer with onychopathy of psoriasis. Thickening of the nail bed as well as central slip or extensor tendon thickening can also be demonstrated . The importance of the nail entheseal complex is underlined by the association of distal interphalangeal (DIP) joint disease even when the nail changes may be subclinical .
Dermopathy
Psoriasis is a common skin condition characterised by scaly plaques. Its histopathology is marked by epidermal hyperproliferation, inflammation and neoangiogenesis . Increased skin thickness and vascularity can be demonstrated by high-resolution US and Doppler techniques . In a small prospective study, Gutierrez et al. demonstrated positive correlation between reduction in power Doppler scoring and improvement in clinical and histological vascularity scores after treatment with etanercept . In a subsequent prospective open label study, De Augustin et al. described reduction of psoriatic plaque Doppler signal as well as psoriatic plaque without any Doppler signals with treatment with infliximab . A later studied by Micali et al. demonstrated reduction of skin thickness as measured by US after treatment with 3 different biological agents. Skin vascularity was followed by videodermatomicroscopy . It has been proposed that the US findings soft skin and nails should be included in the composite sonographic measure of PsA . However, this approach has to be further validated. In summary, the role of US in the examination of psoriatic plaque is still evolving.
Ultrasonography
US technique and findings
Musculoskeletal US uses non-ionising sound waves to visualise soft tissues in high detail. It can visualise tendons, entheses, ligaments, synovial recesses, skin and nails ( Fig. 1 ). Of note, ultrasound cannot visualise intraosseous structures but can discern cortical defects on the osteal surface and osteoproliferation. Vascularity within the soft tissues can also be detected without the use of contrast using power Doppler or colour flow Doppler. Sonography has the added advantage of being used at the bedside and on multiple areas, with the optional use of dynamic scanning as well as directed according to patient’s symptoms. In contrast to RA, PsA can affect multiple soft tissue compartments and a variable presentation of synovitis from polyarticular patterns to asymmetric oligoarthritis. In the following section, key sonopathoanatomical findings found in PsA are briefly discussed.
Enthesitis
The importance of enthesitis is denoted by its inclusion in the ClASsification of Psoriatic ARthritis (CASPAR) criteria . Several sonographic entheseal schemes have been published . On the whole, these have reasonable reliability, sensitivity and responsiveness . However, these have not been the designed specifically for PsA but for SpA in general. The majority of these are heavily weighted to include lower extremities entheses. This is problematic since mechanical changes at the lower extremity entheses can have similar appearances to inflammatory enthesitis and can occur in individuals with obesity and with diabetes . A significant proportion of patients with PsA or psoriasis have higher body mass indices. A recent study by Eder et al. revealed that the Madrid Sonographic Enthesitis Index (MASEI) was unable to distinguish patients with PsA, psoriasis and controls when the BMI was greater than 30 . In addition to selecting entheses, there needs to be agreement over what types of elementary changes to examine. Consensus agreement for including tendon hypoechogenicity, tendon thickening, calcification, enthesophytes, erosions and the Doppler activity was recently published . However, bursitis did not reach consensus agreement to be included. Furthermore, areas such as the posterior tibial tendon, extensor tendons of the hand at the metacarpophalangeal (MCP) or proximal interphalangeal (PIP), and ligaments and palmar/plantar plate structures were not considered. There is therefore a need to include structures that are more relevant to PsA and that may be less prone to mechanical factors.
Synovitis
Patients with PsA can have a heterogeneous pattern of joint involvement in addition to significant extra-articular tissue involvement. This may be manifested by soft tissue oedema, joint peri-enthesitis or tendinitis and osteoproliferation. The presence of synovitis, tenosynovitis vascularity, synovial fluid and bony changes including erosions and osteoproliferation can be demonstrated with US . Erosions may not have the same morphology as that in RA and may appear shallow. Although similar numbers of erosions may occur in PsA and RA, the erosions have less preponderance for radial aspects of the MCP joints and on micro-CT, and the morphology was mostly omega shaped and tubule shaped . In contrast to this study, most RA erosions were U shaped.
Dactylitis
Dactylitis is a characteristic feature of PsA. It is associated with increased incidence of erosive disease. Although soft tissue thickening, synovitis, extensor tendon thickening and flexor tenosynovitis have been identified by US, a wider involvement of the digital tissues has been demonstrated by MRI . These have included collateral ligament as well as palmar or plantar plate involvement. Of note, the nail or the nail matrix has not been systematically studied in relationship to dactylitis. The OMERACT group is currently developing a sonographic outcome measure for dactylitis.
Onychopathy
Nail dystrophy may be associated with a threefold increased chance of having PsA in patients with psoriasis . In addition, it may be associated with a higher incidence of subclinical enthesopathy at the upper and lower extremities . The nail matrix can be involved resulting in pitting. When the nail bed is affected, thickening of the nail bed, oil spots and onycholysis may be seen. The extensor slip or tendon has an intimate insertion about the nail matrix area giving rise to the suggestion of the nail-extensor tendon entheseal complex . The nail can be demonstrated as an apparent bilayer on US with obliteration of the bilayer with onychopathy of psoriasis. Thickening of the nail bed as well as central slip or extensor tendon thickening can also be demonstrated . The importance of the nail entheseal complex is underlined by the association of distal interphalangeal (DIP) joint disease even when the nail changes may be subclinical .
Dermopathy
Psoriasis is a common skin condition characterised by scaly plaques. Its histopathology is marked by epidermal hyperproliferation, inflammation and neoangiogenesis . Increased skin thickness and vascularity can be demonstrated by high-resolution US and Doppler techniques . In a small prospective study, Gutierrez et al. demonstrated positive correlation between reduction in power Doppler scoring and improvement in clinical and histological vascularity scores after treatment with etanercept . In a subsequent prospective open label study, De Augustin et al. described reduction of psoriatic plaque Doppler signal as well as psoriatic plaque without any Doppler signals with treatment with infliximab . A later studied by Micali et al. demonstrated reduction of skin thickness as measured by US after treatment with 3 different biological agents. Skin vascularity was followed by videodermatomicroscopy . It has been proposed that the US findings soft skin and nails should be included in the composite sonographic measure of PsA . However, this approach has to be further validated. In summary, the role of US in the examination of psoriatic plaque is still evolving.
US for diagnosis, monitoring and prognostication of PsA in clinical practice
US in the diagnosis of PsA
There are 2 main areas where US aids in the diagnosis of PsA. The first is to identify patients with psoriasis who have subclinical PsA and second to establish a diagnosis in early inflammatory arthritis. Gisondi et al. prospectively examined patients with psoriasis without known PsA . US detected a higher incidence of entheseal abnormalities in patients with psoriasis than with controls despite the lack of symptoms. The GUESS score without Doppler was used to examine these patients. In a retrospective analysis of this cohort, a more severe dermatologic outcome was noted in patients with enthesitis . However, it could equally be said that patients with higher skin scores are more likely to have underlying enthesitis. In a follow-up study of 28 of these 30 patients, Tinazzi et al. reported new onset of PsA by CASPAR criteria in 7 of the patients . None of the patients had been treated with systemic agents. The GUESS system was again used and revealed similar scores over time. Baseline scores were higher in patients who developed PsA or OA than in those with asymptomatic patients. Gutierrez et al. reported subclinical findings of enthesopathy in 30% of the patients with psoriasis compared with 8% of the healthy controls. Although Doppler was added to the GUESS protocol for examining entheses, active PD was only detected in less than 1% of the entheses. Naredo et al. examined 162 biological-naive psoriasis patients not receiving systemic therapy compared with 60 age-matched controls in a cross-sectional multicentre study. In addition to lower extremity entheses, multiple joints were also examined for synovitis. Three per cent of patients with psoriasis compared with 1.3% controls had synovitis. Enthesopathy was found in 11.6% and 5.4% of psoriasis and control subjects, respectively . In contrast to Gutierrez et al., power Doppler signal was seen in 7.4% of the patients and none in controls. Logistic regression could only identify the presence of psoriasis as predictive of synovitis or enthesopathy. Eder et al. used the MASEI scoring system to examine patients with PsA, psoriasis and healthy controls. They reported that the damage component of the score was higher in patients with PsA than in those with psoriasis and healthy controls. No difference was observed between psoriasis controls and healthy controls. One other major finding of this study was that no significant differences in the scores were seen in the 3 groups when the body mass index was above 30 .
Using entheseal sites that are less mechanically prone to alteration may improve specificity. Zabotti et al. reported a study of 34 patients with early RA and 26 with early PsA. Synovitis was more frequently found in patients with early RA. Periarticular soft tissue oedema was exclusively seen in patients with PsA. In MCP and PIP joints of patients with PsA, extensor tendon or central slip inflammation was observed almost exclusively compared with the RA group . Others have also suggested that extensor paratenonitis at the MCP joints may be exclusive for PsA . However, paratenonitis can also be observed in patients with RA with long-standing disease .
US for prognosticating PsA
In the above section, the discussion outlined possible use of entheseal scores to predict if a patient with psoriasis may develop PsA and that mechanical factors may confound this. US may also reclassify patients with recent onset PsA oligoarticular disease as having polyarticular disease that may affect their prognostic outlook . In contrast to RA, there is sparse evidence for the relationship of ongoing Doppler activity and joint damage. Miedany et al. examined 126 patients with PsA fulfilling CASPAR criteria as well as 112 psoriasis controls . None of the patients had received systemic therapy for psoriasis/PsA. They were followed for 1 year prospectively without any stated treatment with baseline and follow-up radiographs. US was performed at the baseline, 6 months and 12 months for all the joints of the fingers of the hands and toes, first and seventh costosternal joints, anterior superior iliac spine, iliac crest, posterior-superior iliac spine, fifth lumbar spinous process, rotator cuff insertion, Achilles tendon, nails, nail beds and extensor apparatus insertion. Progression of erosion or joint space narrowing was seen in 47% of the joints of the PsA group. Logistic regression identified baseline US gray-scale and power Doppler synovitis, and the presence of baseline enthesopathy/enthesitis as risk factors for progression of joint damage. The highest odds ratio of 6.62 reported was for persistent synovitis or enthesitis at 6 months. This study is somewhat atypical in that it followed patients identified with PsA without any treatment, some of which could have progressed in any case. Further studies are needed to identify factors associated with progression with biological or non-biological treatment. Predicting success of medication tapering in patients in low disease activity is another area where US may be helpful. Araujo et al. investigated the predictors of relapse in patients with minimal PsA activity who were taking methotrexate or tumour necrosis factor (TNF) inhibitors . A substantial portion of their patients relapsed rapidly. Baseline US examination of 30 joints and 20 entheseal areas in each patient revealed surprisingly negligible Doppler activity. No details of the equipment or settings were provided. In addition to long disease duration and severity of skin involvement, baseline US level of synovial hypertrophy was associated with disease relapse. There is therefore limited data on US predictors of worse outcome for joint disease and for predicting relapse in patients with minimal disease activity.
US for monitoring PsA
The approach to monitoring PsA with US has been heterogeneous, ranging from following enthesitis to multiple tissue targets. Gutierrez et al. reported a novel composite targeted power Doppler scoring system involving joint, tendon, enthesis, skin and nail . In this pilot study of 16 patients with PsA receiving anti-TNF therapy, US was done at the baseline and at 8 weeks at areas that had the highest Doppler signal at the baseline. All areas showed improvement in the mean overall score from baseline to 8 weeks. De Agustin et al. used a similar protocol in a multicentre prospective study of 24 patients with PsA treated with infliximab . They also chose to follow skin plaque thickness prospectively. Plaque thickness, joint synovial hypertrophy and power Doppler and plaque Doppler decreased rapidly after initiation of infliximab. In contrast, Litinsky et al. compared the response of 19 patients with PsA receiving methotrexate and 24 patients receiving adalimumab using US measurements of thickness of the second and third finger extensor and flexor tendons, plantar fascia and Achilles tendon bilaterally . Although both groups improved clinically, only the adalimumab group had reduction in thickness in some tendons and enthesis. One shortfall of the study was that no power Doppler was done in these areas. In a smaller study by Acquacalda et al., lower extremity and triceps entheses were examined bilaterally by B-mode and Doppler US . Although a high prevalence of enthesitis was found in both groups, heterogeneous results were reported in patients with psoriasis and PsA undergoing methotrexate or anti-TNF therapy. The authors also reported that no power Doppler signal was seen in any entheseal area.
US and remission status of PsA
Two recent studies examined US in patients with low or minimal disease activity in PsA to examine the performance of clinical composite measures (Disease Activity Index for Psoriatic Arthritis (DAPSA) and Composite Psoriatic Disease Activity Index (CPDAI)) and to assess whether residual activity is present. Husic et al. examined 68 joints and 14 entheses in each of the 70 consecutive patients with PsA . Clinical measures overestimated remission when compared with US measures. DAPSA and Boolean remission were the best predictors of US remission. However, clinical composite measures did not correlate with US signs of enthesitis, dactylitis, tenosynovitis and periarticular inflammation. In a later cross-sectional study of an extensive number of joints, tendons and entheses of 141 patients with PsA, Michelsen et al. found that DAPSA and DAS28 also correlated better with US findings than CPDAI and PASDAS. DAPSA and Boolean definitions of remission better predicted US remission . However, approximately 50% patients had US remission. There was no correlation between patients in US remission and clinical measures.
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