Curr Rheumatol Rep (2014) 16:399 DOI 10.1007/s11926-013-0399-y

IMAGING (P CONAGHAN, SECTION EDITOR)

Role of Modern Imaging Techniques in Hand Osteoarthritis Research and Clinical Practice Ida Kristin Haugen & Hilde Berner Hammer

Published online: 20 December 2013 # Springer Science+Business Media New York 2013

Abstract Hand osteoarthritis (OA) is a frequent disease, which may lead to considerable pain and physical limitations. However, limited research has been performed in hand OA. Lately, modern imaging techniques, such as ultrasonography (US) and magnetic resonance imaging (MRI), have gained increasing attention in hand OA clinical research. Both modalities may provide important knowledge about the natural history and pathogenesis of the disease, in addition to serving as potential outcome measures in clinical trials. In clinical practice, the diagnosis of hand OA should be based on clinical examination and conventional radiography, if necessary. However, US and MRI can provide information about the degree of inflammation and exclude potential differential diagnoses. Keywords Hand . Osteoarthritis . Magnetic resonance imaging . MRI . Ultrasonography . Ultrasound . Imaging . Pain

Introduction Osteoarthritis (OA) is the most common musculoskeletal disease in developed countries, and the finger joints are frequently affected. Symptomatic hand OA occurs in 16 % of women and 8 % of men between 40–84 years of age [1]. In rheumatology clinics, hand OA patients are commonly seen due to pain and limited hand function. In fact, patients with hand OA This article is part of the Topical Collection on Imaging I. K. Haugen (*) : H. B. Hammer Department of Rheumatology, Diakonhjemmet Hospital, Oslo, Norway e-mail: [email protected] H. B. Hammer e-mail: [email protected]

may have similar amounts of complaints as patients with rheumatoid arthritis [2]. There are currently no diseasemodifying treatments licensed for people with hand OA (or OA in other joints) and such people are therefore usually treated with analgesics or anti-inflammatory agents in addition to physical therapy [3], which have at best weak to moderate analgesic effects. Despite the high frequency of the disease and the high levels of symptoms, people with hand OA have been given limited attention by both clinicians and researchers. In the research field of OA, most studies are performed on OA in the lower limb, whereas the investigation of hand OA has been much more limited. Imaging in rheumatology has gained increasing attention in recent years, especially magnetic resonance imaging (MRI). For inflammatory joints diseases, MRI is frequently used both in clinical practice for diagnostic and prognostic purposes as well as in multiple clinical trials and observational studies [4-6]. The use of MRI in OA research has also had a steep increase the recent years, with many observational studies focusing on OA pathological features as demonstrated by MRI [7••, 8••, 9•, 10•, 11]. Furthermore, MRI findings have been the outcome of interest in several clinical trials [12-14], although these imaging outcomes are not yet accepted by regulatory authorities for demonstrating disease-modifying effects [2, 15]. According to guidelines, hand OA should be diagnosed based on medical history and clinical examination, possibly in combination with conventional radiography [16]. However, both ultrasonography (US) and MRI may have a role in clinical care of these people. The current article will describe what we have learned from modern imaging research, and the role of modern imaging in hand OA clinical practice. The focus will be on US and MRI, which represent the most commonly used imaging methods in addition to conventional radiography.

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Ultrasonography (US) What Have we Learned from OA Studies Using US? During the last few years, US has gained acceptance as a useful tool for assessment of inflammation in the finger joints in people with inflammatory joint diseases [17, 18]. Lately, researchers have also looked into the prevalence, validity, and reliability of US features in people with hand OA. Scoring Systems and Reliability of the Scoring In order to facilitate a reliable scoring of US features in the finger joints (including the first carpometacarpal, metacarpophalangeal, proximal, and distal interphalangeal joints), a preliminary scoring system was developed within the Outcome Measures in Rheumatology (OMERACT). A group of experts in the fields of OA, US, and outcome measures agreed upon domains and suggested scaling of the items. In total, three features were included (gray-scale synovial hypertrophy/effusion, power Doppler activity, and osteophytes), representing activity and damage domains. All features were scored as absent/present as well as on semiquantitative scales (grade 0–3) [19]. Operator-dependency represents one of the greatest limitations of US assessment. Several studies have reported interreader reliability based on stored images, which limits the variability related to the actual performance and technique of the procedure. A large reliability exercise was arranged in order to test the reliability of the proposed scoring system, and seven international experts participated [19]. The reliability exercise was based on examination of seven patients, of whom the first patient was examined twice by each ultrasonographer. Despite divergent results between ultrasonographers and for the various features (in general lowest reliability for power Doppler activity and highest for osteophytes), the authors concluded that the results were satisfactory and that the scoring system could be a good basis for further development of US as an outcome tool. Recently, Mathiessen et al. developed an atlas showing examples images of different grades of osteophyte severity in the interphalangeal joints (grades 0–3) [20••]. Using the atlas for scoring of stored US images, the authors found excellent inter-reader reliability. These findings emphasize the importance of standardization. No atlas have so far been developed for gray-scale synovitis and power Doppler activity in hand OA. However, the synovitis found in OA can be scored according to the published comprehensive US atlas for gray-scale synovitis and power Doppler activity in rheumatoid arthritis [21]. The first scoring system by Keen et al. did not include assessment of erosions and cartilage (joint space narrowing) due to concerns about reliable definitions, contemporary US

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technology and feasibility related to the duration of the scanning [19]. Recently, nine expert ultrasonographers achieved consensus on definitions of cartilage pathology in the metacarpophalangeal joints: (1) global cartilage abnormalities (absent/present), (2) loss of anechoic structure and/or cartilage thinning, and (3) irregularities and/or loss of sharpness of ≥1 cartilage margin [22•]. A limitation of this system is the focus on metacarpophalangeal joints only, which are less frequently affected by OA than the interphalangeal and thumb base joints. The reliability exercise was based on the examination of the metacarpophalangeal joints in eight patients, who were examined twice by nine sonographers. Inter-reader reliability varied from fair (irregularities and/or loss of sharpness of) to very good (global assessment). However, the reliability can probably be further improved by modifying definitions and further standardization of the technique [22•].

Prevalence of US Features Most US studies in hand OA have shown high prevalence of gray-scale synovitis, whereas power Doppler activity is less common [23, 24, 25•, 25, 26]. Kortekaas et al. showed that both gray-scale synovitis and power Doppler activity were present in one or more joints in the majority of patients [26], but the number of joints with gray-scale synovitis was considerably higher than the number of joints with power Doppler activity. On the other hand, other studies have demonstrated more similar prevalence of gray-scale synovitis and power Doppler activity [23, 27]. Differences between studies may be due to different study populations, US technology (modern machines allow more sensitive power Doppler detection), and interpretation of findings. US is a valuable tool to evaluate “erosive hand OA”, which is sometimes referred to as “inflammatory OA”. Inflammatory (e.g., effusion/synovitis) and structural changes (erosions) are frequently detected by US (and MRI) in people with both radiographic erosive and non-erosive disease [10•]. This may indicate that erosive hand OA is not a separate entity, but rather represents the severe end of a spectrum of hand OA pathology [10•]. However, it should be noted that the number of joints with inflammation is often higher in those with radiographic erosive hand OA [27]. Kortekaas et al. showed that people with erosive hand OA demonstrated more inflammation in their non-erosive joints compared to what is generally found in people with non-erosive disease [28•]. Previous studies have also indicated that inflammation is more common in joints with radiographic “active” erosions compared to joints that are remodeled (that means new irregular sclerotic subchondral plates are formed, and in between these a new joint space becomes visible) [28•, 29]. These findings may indicate that inflammation is less pronounced in later stages, which needs to be confirmed in longitudinal studies.

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Validity of US Features Against Other Imaging Modalities Several studies have compared US against other imaging modalities. The first report, comparing US and conventional radiography, found that radiography was more sensitive than US to detect erosions [30], which could have been due to interposition of osteophytes disturbing the acoustic window. Subsequent studies have reported that US is more sensitive than radiographs in detecting erosions [9•, 10•, 23] as well as osteophytes and joint space narrowing [9•, 23, 31]. The higher sensitivity of US is likely due to its multiplanar assessment of the joint compared to the projectional nature of radiograph acquisition. Erosions are typically seen in the central part of the joint on radiographs, often with a typical gull-wing configuration. However, US studies have shown that erosions can also be found in the peripheral parts of the joint [23]. Further, lesions misinterpreted as cysts based on conventional radiographs may appear as erosions when looking on the joint from different angles with US [23]. It should be noted that the US evaluation may be problematic in severely affected joints, and various results across studies may be related to difficulties in interpretation of findings in joints with excessive bone formation and deformities. Assessment of joint space narrowing may be difficult since the peripheral parts of the joints can be documented only. Overlying osteophytes may further limit the acoustic window. Despite these limitations, studies have shown that USdetected cartilage thickness is significantly correlated to radiographic severity, joint space narrowing, and width [27, 32]. To date, few studies have compared US and MRI. Good agreement between US and MRI has been shown for both structural features and inflammation [9•, 10•, 20••]. Using US and MRI fusion imaging, Iagnocco et al. found that hyperechoic prominences on US corresponded to MRIdetected osteophytes [33]. The optimum application of fusion imaging has not yet been determined, and the extra time and cost limit its use. Associations to Pain and Physical Function The associations between US OA features and pain have been analyzed at both individual joint level and patient level. In general, studies examining the amount of OA pathology across patients are less likely to show associations to measures of pain and function than analyses performed at the individual joint level (that is, association between OA pathology and pain in the same joint). Analyses at patient level may be confounded by psychosocial factors affecting the self-report of symptoms [34]. Several studies have shown that US-defined gray-scale synovitis, power Doppler activity and osteophytes are associated with pain in the same joint [24, 26, 35•]. Kortekaas et al. found significant associations between gray-scale synovitis

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and pain [26]. However, it should be noted that the analyses were not adjusted for structural features, and the associations could therefore potentially be confounded by co-occurring OA features [26]. Further, there were significant associations between gray-scale synovitis and hand pain, stiffness, and physical disability in analyses performed at the patient level [26]. However, other studies have not been able to confirm these associations [24, 36]. Mallinson et al. found no association between US features in the thumb carpometacarpal joint and self-reported disability [37]. Interestingly, Koutrompas et al. detected significant associations between clinically inflamed joints and physical limitations, whereas no associations were found for US-detected inflammation [36]. These findings may indicate that US detects low-grade inflammation, which may not always be related to physical complaints. The associations between US features and pain and physical limitations need to be confirmed in longitudinal studies. To date, there are few longitudinal observational US studies in hand OA. Keen et al. found a significant decrease of symptoms in people treated with intra-muscular methylprednisolone, whereas the reduction of US-detected inflammation was not statistically significant [25]. Interestingly, there was no association between reduced US-detected inflammation and reduced symptoms [25]. Due to the open-label study design, we cannot rule out that the clinical response represented a placebo effect. Two studies of 4 and 24 weeks duration, respectively, have examined the effect of hyaluronic acid injections in hand OA, of which both demonstrated an effect on US-detected inflammation [38, 39]. Klauser et al. also found significant association between US-detected capsular distension and power Doppler activity and decrease of pain [39]. To date, no placebo-controlled studies using US in hand OA patients have been performed. Should US be Used in Clinical Practice of Hand OA Patients? The benefit of US is the ability to give a multiplanar demonstration of joint pathology without radiation and contraindications. Rheumatologists can readily perform the procedure in the examination room without any inconvenience for the patients. Optimal visualization is achieved by longitudinal and transverse scanning of the dorsal aspects with the finger joint in full flexion and of the volar aspects with the finger joints in neutral position [40]. US allows visualization of a wide spectrum of hand OA features, such as osteophytes, marginal erosions, cartilage, and inflammation. Inflammation can be evaluated as gray-scale synovitis (synovial thickening/effusion) and power Doppler activity, of which the latter represents vascularization and therefore active inflammation of synovium. US may therefore confirm the clinical diagnosis of hand OA and provide information about the amount of inflammation, which may be relevant for the choice of treatment. US cannot differentiate

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OA from, for example, early rheumatoid arthritis based on the examination of synovitis. However, the presence of osteophytes indicates OA (Fig. 1). One disadvantage of US is the inability of the beam to penetrate bony cortex. Hence, due to the joint anatomy, demonstration of cartilage and bone damage is mostly restricted to the peripheral parts [40]. Overlying osteophytes disturbing the acoustic window may further complicate the joint evaluation. The live demonstration also has disadvantages related to the detection of progression. Storing of US images is less feasible than for other imaging modalities, making it more difficult to compare the current joint status with previous examinations. Future Role of US The reliability, validity, and sensitivity of change of US needs to be further improved and validated before US can be approved as an appropriate outcome in clinical trials. So far, no randomized controlled trials have been performed in hand OA using US as outcome measure. With low cost and good availability, US may be important in clinical trials, especially if inflammation is the outcome of interest.

MRI What Have we Learned from OA Studies Using MRI? MRI is an established outcome measure in inflammatory joint diseases and knee OA, and has increased our understanding of the underlying disease mechanisms. With the use of MRI, OA is now recognized as a disease that is not only affecting the cartilage but all joint components [41]. However, in contrast to the large amount of MRI studies performed on knee OA, only limited research has been performed on the prevalence, reliability, and validity of MRI-defined pathology in hand OA. Scoring Systems and Reliability of the Scoring Haugen et al. proposed a comprehensive MRI scoring system and atlas, which included assessment of osteophytes, joint space narrowing, erosions/attrition, cysts, malalignment, synovitis, flexor tenosynovitis, bone marrow lesions (BMLs), and collateral ligament abnormalities [42••]. Most features were scored on 0–3 scales (in the proximal and distal part of the joint separately, if applicable), except cysts, malalignment and collateral ligament abnormalities, which were scored as absent/present [42••]. The scoring system was developed for the interphalangeal joints, and future studies should examine whether the scoring system can be similarly applied to the metacarpophalangeal and thumb base joints. The MRI scans (i.e., dynamic image analyses) from 10 patients were scored twice by three readers, and intra- and

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Fig. 1 Osteophyte demonstrated by US examination of the 2nd proximal interphalangeal joint

inter-reader reliability were good for the majority of features in the scoring system [42••]. Good reliability was also confirmed in another cohort using the same scoring system [43], suggesting that MRI can reliably assess OA pathology in the small finger joints. The proposed scoring system was comprehensive in order to include all potentially relevant features. However, Haugen et al. found that certain features, such as collateral ligament pathology and flexor tenosynovitis, were infrequently present, did not correlate with OA severity, and/or were not associated with pain [7••]. Based on the experience from the Oslo hand OA cohort, the scoring system was further optimized by the “MRI in inflammatory joint diseases” group in the OMERACT [44••]. The changes included exclusion of collateral ligament pathology and flexor tenosynovitis, scoring of the joint as a whole (i.e. not the distal and proximal part separately) and half scores (0.5 increments) for BMLs, synovitis, and erosions in order to better capture changes.

Prevalence of MRI Features Tan et al. confirmed that virtually all structures were affected in interphalangeal joints with early and late OA using highresolution MRI [45]. In addition to a high prevalence of BMLs, erosions and synovitis, they found that collateral ligament abnormalities were universal in both early and late disease. Further, they found a close anatomic relationship between collateral ligament pathology and erosions, BMLs, and bone formation [45]. Nevertheless, it should be noted that collateral ligament abnormalities were also common in elderly controls without OA, and it is therefore unknown whether the current changes are age-related or involved in OA pathogenesis. Secondly, collagenous structures, such as collateral ligaments, may demonstrate increased signal intensity due to an artifact called “magic angle” phenomenon, which may lead to an overestimation of ligament pathology [46]. The frequency of different MRI features has been examined in several hand OA cohorts, of which the Oslo hand OA cohort represents the largest [7••]. One of the interesting

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findings by Haugen et al. was the high frequency of synovitis on contrast-enhanced MR images [7••] (Fig. 2). Synovitis was also commonly present in joints without radiographic hand OA, which is in line with previous observations in knee OA [47]. High prevalence of synovitis has also been confirmed in other smaller cohorts [9•, 43]. It has been shown that minimal MRI enhancement of the synovium may be present in OA-free individuals [48], and synovitis should therefore probably not be scored as present unless there is an accompanying increased thickness of the synovium. BMLs were found in few joints in the Oslo hand OA cohort [7••], in contrast to the high prevalence shown in other smaller cohorts [9•, 43]. The low prevalence may be due to a lower field strength and poorer resolution. However, for assessment of BMLs, it is important to be aware of partial volume artifacts, which may mimic BMLs [49]. Studies suggest that erosive disease represents the severe spectrum of hand OA [50]. Wittoek et al. confirmed that MRIdefined erosions, synovitis, and BMLs were present in both radiographic erosive and non-erosive disease, although the features were more frequent in the former group [9•]. Validity of MRI Features Against Histology and Other Imaging Modalities The validity of MRI features in hand OA has been tested against histology and other imaging modalities, of which the former is often considered as the “gold standard” [7••, 9•, 43, 51-53]. In a cadaver study, Lewis et al. compared MRI features and corresponding histological section in three fingers [51]. Osteophytes and cartilage loss were found on the histological sections, but only the larger structures were identified by MRI [51]. Tan et al. compared the findings at highresolution MRI and cadaveric histological sections in order to better understand the role of collateral ligaments in finger joint OA, and suggested that the MRI-defined ligament abnormalities were caused by degenerative changes [52]. However, the study was limited by the fact that the histological sections and MRIs that were compared were not from the same patients. Several studies have compared MRI against conventional radiography. In general, MRI seems to be more sensitive than conventional radiography in the detection of both erosions [7••, 9•, 10•, 43, 53] and osteophytes [7••, 43]. Higher sensitivity of MRI is most likely due to the multiplanar joint demonstration by MRI, whereas the radiographs are typically in a single plane only (commonly a posteroanterior view]. In addition to the traditional central erosions (typically seen on conventional radiographs], MRI was able to demonstrate marginal erosions [7••]. As described in the section about US, three previous studies have compared OA findings by US and MRI [9•, 10•, 20••]. Vlychou et al. compared OA findings in 25 patients

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Fig. 2 Pre- and post-Gadolinium (Gd) images showing contrast enhancement (synovitis) in distal interphalangeal joint two and three (joints to the right)

using US and 3.0 T MRI. The overall concordance between MRI and ultrasonography was substantial for osteophytes, and excellent for cysts, erosions, synovitis, and tenosynovitis. Associations to Pain and Physical Function Previous studies have shown weak associations between radiographic OA features and pain [54]. In their MRI study, Haugen et al. found that synovitis, BMLs and erosions were associated with pain in the same joint independent of each other [8••]. These findings are in line with several studies on knee OA, supporting the validity of these findings [55, 56]. The findings were also confirmed by Kwok et al. [43], although the authors did not adjust for the co-occurrence of several OA features. Since OA affects the whole joint, several OA pathologies often co-occur, making it difficult to conclude which features have direct associations with pain. Therefore, the associations between MRI features and pain need to be confirmed in longitudinal studies to see whether changes, i.e. both increase and decrease, of MRI features lead to more or less pain, respectively. Structural features, such as bone damage, seemed to be associated with reduced physical function, but the associations were weak and inconsistent [8••]. In the current study, the MRI coil did not cover the metacarpophalangeal and thumb base joints, which may have contributed to the lack of associations. Should MRI be Used in Clinical Practice of Hand OA Patients? One of the main benefits of MRI is the multiplanar imaging of all joint components, including structural features (e.g., osteophytes, cartilage, erosions/cysts, malalignment), soft tissue structures (e.g., ligaments), and inflammatory features (e.g., synovitis, flexor tenosynovitis). MRI is the only imaging modality that is able to demonstrate BMLs, which can be seen

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as high signal intensity on T2-weighted fat-suppressed images or Short TI Inversion Recovery (STIR) images. In knee OA, BMLs have been proven as an important predictor for structural progression and a source of pain [55]. BMLs are seen in OA as well as inflammatory joint diseases, but their location and extent may differ. In OA, the BMLs are typically located in the subchondral bone, and histologically represent areas with bone remodeling [57-59]. However, BMLs in inflammatory joint disease reflect inflammatory processes in the bone [57]. The presence of osteophytes, central versus marginal erosions and the inflammatory pattern (based on dynamic MR imaging) may also be different in OA compared to inflammatory joint diseases [16, 60]. Despite the benefits of MRI in terms of the wide demonstration of joint pathology, there are several limitations. First of all, MRI is not as readily available as US and conventional radiography and involves much higher costs. In order to have a direct assessment of synovitis, contrast agents are necessary [61]. Gadolinium contrast may be contraindicated in elderly people due to comorbidities, and should not be given to people with severely reduced kidney function due to the risk of nephrogenic systemic fibrosis [62]. In rheumatoid arthritis, contrast-enhanced MRI has been shown to be more sensitive that non-contrast-enhanced MRI [63]. Likely, the same it is true for hand OA, although no studies to date have compared MRI with and without contrast in hand OA. Despite the high sensitivity of MRI in the detection of OA features and the demonstration of BMLs, the clinical value is so far limited when the extra costs and the contraindications are taken into account. Since we do not have any diseasemodifying treatment to offer people with OA, the clinical value of early OA diagnosis and demonstration of BMLs is limited. Hence, MRI is not recommended for clinical diagnosis of hand OA, unless there are doubts about differential diagnoses such as rheumatoid arthritis and psoriatic arthritis. Further, MRI should always be used in combination with clinical examination. Characterization of inflammatory diseases of small joints using MRI only remains challenging especially in the differentiation between OA and psoriatic arthritis [64].

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reliability and validity as well as a high sensitivity to change. Hence, there is a need for more validation studies, in which preferably histology and/or computer tomography should be used as the “gold standard”. When or if disease-modifying drugs are available in OA, MRI may also have a role in clinical practice. In this case, MRI may be a valuable tool for demonstrating OA features that can be targeted by specific drugs, as well as demonstrating potential treatment effects.

Conclusions OA is recognized to involve the whole joint, which can be visualized by modern imaging techniques. To date, we rely on mainly cross-sectional US and MRI studies of people with hand OA. Hence, longitudinal studies are very much needed to provide us with important knowledge about the natural history and pathogenesis of hand OA. Further, US and MRI will be important outcome measures in clinical trials, especially if inflammation and BMLs are targeted. In clinical practice, US is readily available and provide information about structural changes and inflammation, and may be a supplement to the clinical examination. MRI has the advantage of a whole-joint demonstration, but involves higher costs and certain contraindications. Although MRI is probably able to detect OA earlier than clinical examination and other imaging modalities, the clinical value is limited, as we do not have any disease-modifying treatment. Therefore, MRI should mostly be used for research and possibly for clinical differential diagnosis. Compliance with Ethics Guidelines Conflict of Interest Ida Kristin Haugen and Hilde Berner Hammer declare that they have no conflict of interest. Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.

Future Role of MRI Using MRI, we may learn more about the association between OA features and pain as well as the natural history of disease and predictors for poor outcome. Longitudinal MRI studies are therefore warranted to provide us knowledge that is needed for the development of disease-modifying drugs in OA. So far, only one clinical trial has used MRI [65]. Due to the advantage of whole-joint evaluation, we assume that several future studies will include MRI as their primary outcome. However, before MRI is an accepted outcome in clinical trials, the proposed scoring systems need to demonstrate good

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Role of modern imaging techniques in hand osteoarthritis research and clinical practice.

Hand osteoarthritis (OA) is a frequent disease, which may lead to considerable pain and physical limitations. However, limited research has been perfo...
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