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Musculoskeletal ultrasound in the evaluation of Polymyalgia Rheumatica

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Review

DOI: 10.11152/mu.2013.2066.173.aig

Abstract

Polymyalgia rheumatica (PMR) is a relatively frequent disease affecting individuals older than 50 years and is character- ized by inflammatory involvement of the shoulder and hip girdles and the neck. Clinical manifestations are represented by pain and morning stiffness in this regions. An extensive and comprehensive assessment of the inflammatory status is crucial in PMR patients, including imaging evaluation. This narrative review reports the current available data in the literature about the role of musculoskeletal ultrasound in PMR.

Keywords: polymyalgia rheumatica, ultrasound, bursitis, tenosynovitis

Musculoskeletal ultrasound in the evaluation of Polymyalgia Rheumatica

Iolanda Maria Rutigliano, Chiara Scirocco, Fulvia Ceccarelli, Annacarla Finucci, Annamaria Iagnocco

Rheumatology Unit, Sapienza Università di Roma, Rome, Italy

Received 30.06.2015 Accepted 08.07.2015 Med Ultrason

2015, Vol. 17, No 3, 361-366

Corresponding author: Annamaria Iagnocco, Sapienza Università di Roma,

V.le del Policlinico 155, Rome – 00161, Italy.

Tel: +39 06 49974634, Fax: +39 06 49974642 E-mail: [email protected]

Introduction

Polymyalgia rheumatica (PMR) is an inflammatory rheumatic condition that typically affects individuals old- er than 50 years, with incidence increasing with age. An Italian epidemiologic study reported an annual incidence rate of PMR over the period 1980–1988 of 12.7/100,000 [1-2]. The etiology of PMR remains unknown, although currently the role of both genetic and environmental fac- tors, such as infections, has been hypothesized. Familiar aggregation has been described and genetic polymor- phisms in human leukocyte antigen (HLA) genes and other genes in the field of immune regulation have been associated with PMR [3-6]. However, to date, no etio- logic theory has been confirmed.

PMR is more frequent in caucasian population and is considered the second most common inflammatory rheu- matic condition in the United States. The prevalence of the disease shows a North-South gradient, with a higher incidence in Northern than in Southern countries, includ- ing Italy [2]. Focusing on the clinical manifestations,

PMR is characterized by pain and morning stiffness, longer than 45 min, involving the neck and the shoulder and hip girdles. Stiffness and pain are usually bilateral, worsen in the morning and improve with activity. Fa- tigue, malaise, anorexia, weight loss and fever are also common and are considered “constitutional symptoms”.

An association between PMR and giant-cell arteritis (GCA) has been described and PMR has been identified in 40-60% of patients affected by GCA; on the contra- ry, GCA has been registered in 16-21% of patients with PMR [7].

An extensive and comprehensive assessment of the inflammatory status is crucial in PMR patients, including imaging evaluation. Musculoskeletal ultrasonography (MSUS) has acquired an increasing role over the recent years in the assessment and monitoring of rheumatic diseases. In fact, thanks to the progressive technological advances and the application of standardized scanning techniques and definitions of US pathology, its diagnos- tic capability has progressively increased [8]. MSUS is a multiplanar and dynamic imaging modality with several advantages: it is safe, feasible, relatively inexpensive and highly accepted by patients. The use of conventional B- mode US provides a wide set of information about the status of different musculoskeletal tissues. In addition, the development of power Doppler (PD) and color Dop- pler (CD) techniques has enhanced the abilities of US to detect and evaluate inflammatory joint activity [9].

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Fig 1. Distribution of the frequency of SAD bursitis (A) and LBT tenosynovitis (B) in the studies analyzed.

This narrative review focuses on the analysis of currently available data in the literature about the role of MSUS in the assessment of patients affected by PMR.

Ultrasonography and PMR

In order to perform a comprehensive sonographic assessment of girdles in PMR patients, US examina- tion should be focused on the evaluation of both intra- articular and extra-articular abnormalities, according to a standardized scanning method and published reference values [10-11].

At shoulder level, the most relevant inflammatory findings that should be investigated by US are repre- sented by gleno-humeral synovitis, subacromial/subdel- toid (SAD) bursitis, and long-head-biceps tenosynovitis.

Similarly to the shoulder, MSUS has a key role also in the assessment of the hip joint where the presence of syn- ovitis can be demonstrated as well as the inflammatory involvement of local synovial structures (trochanteric, iliopsoas, and ischiogluteal bursae).

Ultrasonographic findings in PMR patients In the last years, a number of studies have been per- formed to test the value of MSUS in detecting inflamma- tory lesions in PMR. As shown in table I, most of them were cross-sectional studies, were performed in Southern European countries (above all Italy) and described the main inflammatory US lesions at disease onset or during relapse. Except for the study of Zaccaria et al, they were conducted in small groups of PMR patients [12-28]. In terms of clinical assessment, when patients were inves- tigated for the presence of symptoms, shoulder pain was the most frequent complain. In some cases, clinimetric tests (such as Visual Analogue Scale for pain, patient and medical global assessment, Health Assessment Question- naire, and Leeb’s Disease Activity Score) were also ap- plied [18-20].

In terms of US assessment, all studies were conducted by using B-mode US and in two cases PD was addition- ally applied [19-21] . The shoulder was studied almost in all reports while the hip was assessed in few cases. An extensive polyarticular US examination was performed in two studies which were focused on the comparison be- tween PMR and Rheumatoid arthritis (RA) [21-22]. Con- cerning the scoring system used for grading the severity of inflammatory lesions, in the majority of studies exclu- sively a binary assessment was applied [12,13,19,22-24];

in a few of them a semiquantitative 0 to 3 score was used [18, 25,26], and finally, in two cases both scoring meth- ods were applied [21-27].

The most frequent US abnormalities were detected at shoulder level and were represented by SAD bursitis and

LTB tenosynovitis that have been reported in percent- ages ranging from 6.2%-100% (fig 1) [12-13]. However, the prevalence of SAD bursitis resulted higher compared to LBT tenosynovitis in the majority of the studies, sug- gesting this lesion as the inflammatory hallmark in PMR [13,18-20,22,25,26]. Moreover, as reported in Table I, a frequent US finding was the identification of bilateral in- volvement both at shoulder and hip level [19,21,25-27].

In terms of structures involved, the presence of SAD bursitis and LTB tenosynovitis was described as the most common finding in PMR patients, with a significant higher prevalence compared with RA subjects [13].

As shown in table I, few reports were conducted ex- clusively at hip level and, similarly to the shoulder as- sessments, extra-articular involvement was the most rel- evant finding with the evidence of trochanteric bursitis that was present in a significantly higher number of cases with PMR than in controls [27].

In terms of sensitivity two studies from the same re- search group comparing US to Magnetic Resonance Imag- ing (MRI) demonstrated that, at shoulder level, US-detect- ed SAD bursitis was present in 96% of patients and that finding was confirmed in 100% of those individuals who underwent also MRI assessment [25].At hip level, a sensi- tivity and specificity of 100% for US in detecting trochan- teric bursitis, compared to MRI has been reported [27].

Concerning sensitivity to change, table II summarizes data obtained from the only three longitudinal studies re- ported in the literature, in which PMR patients underwent an US assessment at baseline and after starting treatment

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Table I. Cross-sectional studies performed to test the value of MSUS in detecting inflammatory lesions in PMR Study Country N. of patients US

scoring system Power

Doppler Joints

evaluated US results Lange

et al, 1998

Germany 13 Dichotomic score * No Shoulders GH synovitis: 61.5%

Coari et al, 1999

Italy 16 Dichotomic score * No Shoulders GH effusion: 65.6%

SAD bursitis: 6.2%

LBT tenosynovitis 6.2%

Lange et al, 2000

Germany 22 Dichotomic score * No Shoulders GH synovitis: 40.9 %

Cantini et al, 2001

Italy 57 Semiquantitative score

(0-3) No Shoulders GH synovitis: 77% (bilateral 45%)

SAD bursitis: 96% (bilateral 96%) LBT tenosynovitis: 80% (bilateral 72%) Frediani

et al, 2002

Italy 50 Dichotomic score * No Shoulders, hips, ankles, wrists, elbows, knees, hands, feet

GH effusion: 66%

SAD bursitis: 70%

LBT tenosynovitis: 68%

Cantini et al, 2005

Italy 20 Dichotomic score * Bursitis: Semiquantita- tive-score (0-3)

No Hips CF synovitis: 45%

trochanteric bursitis: 100% (bilateral 90%) Catanoso

et al, 2007

Italy 6 Semiquantitative-score

(0-3) No Shoulders GH synovitis: 33.3%

SAD bursitis: 100%

LBT tenosynovitis: 100%

Zaccaria et al, 2009

Italy 111 Semiquantitative score

(0-3) No Shoulders GH synovitis: 52%

SAD bursitis: 92% (bilateral)

LBT tenosynovitis: 45% (bilateral 34%) Macchioni

et al, 2009

Italy 57 Dichotomic score * Yes° Shoulders GH synovitis: 15.8 % (bilateral) SAD bursitis: 61.4 % (bilateral) PD in SAD bursitis: 33%

LBT tenosynovitis: 71.9 % (bilateral) Jimenez-

Palop et al, 2009

Spain 53 Dichotomic score * No Shoulders, hips GH synovitis: 18%

SAD bursitis:65%

LBT tenosynovitis: 45%

CF synovitis: 30%

Falsetti et

al, 2011 Italy 29 All structures: dichoto- mic score *

PDUS: semiquantita- tive score (0-4)

Yes Hips, shoulders, elbows, wrists, MCPs, knees, MTPs

GH synovitis: 65.5% (bilateral 73.6%) SAD bursitis: 79.3% (bilateral 86.9%) LBT tenosynovitis: 79.3% (bilateral 78.2%) shoulder PDUS score > 0: 6.8%

CF synovitis: 24.1% (bilateral 100%) Ruta

et al, 2012

Argentina 30 Dichotomic score * No Shoulders GH synovitis 11.7%

SAD bursitis: 55%

LBT tenosynovitis: 46.6%

VAS = visual analog scale; MS = morning stiffness; HAQ = health assessment questionnaire; ESR = erythrocyte sedimentation rate; CRP = C-reactive protein; SAD = subacromial-deltoidea; LBT = long biceps tendon; GH = gleno-humeral; CF = coxo-femoral; PD = power Dop- pler; °in 24 patients; *presence/absence

Table II. Prospective studies performed to test the value of MSUS in detecting inflammatory lesions in PMR.

Study Country N Joints evaluated Treatment Follow-up Us results at follow-up Catanoso et al.

2007 Italy 6 Shoulders Etanercept 50 mg/week 24 weeks 50% decrease of inflam-

matory lesions Macchioni et al.

2009 Italy 57 Shoulders Prednisone (starting dose

range 12.5-17.5 mg/day) 24 +/- 3 weeks More than 50% decrease of inflammatory lesions Jimenez-Palop et al.

2009 Spain 53 Shoulders hips Prednisone (starting dose

range 10-20 mg/day) 12 weeks Normal in 50% of patients with lesions at baseline GH = gleno-humeral SAD = subacromial-deltoidea; LBT = long biceps tendon; GH = gleno-humeral; CF = coxo-femoral; PD = power Doppler

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for the disease [18-20]. Two studies, published in 2009, evaluated the modification of US features in more than 50 PMR patients, after 12 weeks [20] and 24 weeks [19]

of treatement with glucocorticoids (prednisone). In both studies the therapy with steroids determined a significant decrease of the prevalence of inflammatory US features.

Interestingly, the study published by Jimenez-Palop et al identified a significant improvement in US inflammatory lesions since week 4.

Previously, Catanoso et al in 2007 evaluated the re- sponse to Etanercept treatment in 6 PMR patients re- fractory to steroid therapy by using US assessment [18].

After 12 weeks of treatment, a 50% decrease in the prevalence of US features was registered in the enrolled patients, suggesting the possible positive effects of anti- Tumor Necrosis Factor drugs to treat PMR patients. This result underlined also the relevant role of US to demon- strate the efficacy of non-conventional treatment in PMR patients.

Concerning reproducibility, only one study assessed the intraobserver and interobserver reliability of US as- sessment in PMR patients, and demonstrated excellent results (k values 0.96 and 0.99, respectively) for both as- sessments [20]. However, the assessment was performed only on stored images and not on real-time US scanning thus limiting the reliability assessment to the interpreta- tion of findings.

Three studies analyzed the correlations between US inflammatory findings and laboratory data [19,20,26].

No significant correlations between disease activity bio- markers and US findings were identified by Macchioni et al: in particular, at the evaluation performed at 24 weeks follow-up, 59.1% of patients in clinical remission or with low disease activity (Leeb’s DAS < 7) showed persistent inflammatory lesions at the US evaluation [19]. Moreo- ver, the studies conducted by Zaccaria et al and Jimenez et al in 2009 identified the absence of significant differ- ences in the US pattern in patients with normal or high erythrocyte sedimentation rate (ESR). In addition, even in the presence of a parallel decrease in the findings, the authors did not find significant correlation between changes of clinical, laboratory and US parameters during the follow-up period [20,26].

In terms of predictive role of US in PMR patients, sonographic findings seem not able to predict the occur- rence of disease relapses [19].

Currently available data suggest a relevant role of US as a diagnostic tool for PMR especially in the dif- ferential diagnosis with other rheumatic conditions with a possible polymyalgic onset and in the patients with- out typical laboratory abnormalities, such as increase of ESR. It is well known that PMR can mimic many other

conditions, resulting in a difficult diagnosis and in the under-evaluation of serious diseases, such as tumors, in- fections, erosive arthritis. According with data from the literature, a shift in the diagnosis has been registered in 5-23% of patients complaining polymyalgic symptoms after a follow-up period of 12 months [14,15,28].

Falsetti et al in 2011 demonstrated an improvement of diagnostic sensitivity for PMR when US assessment was used, especially with the application of PD func- tion. Sixty-one consecutive patients with clinical typical features of PMR underwent multi-district US evaluation at baseline and every three months. After a 12-months follow-up, a different diagnosis was made in half of pa- tients (52%): specifically, they met classification crite- ria for elderly-onset rheumatoid arthritis, elderly onset spondyloarthritis, and calcium pyrophosphate deposition disease. The authors suggested a predictive model of US evaluation to classify PMR patients, including the pres- ence of SAD bursitis, low frequency of wrist, metacar- pophalangeal and metatarsophalangeal effusion/synovi- tis, low frequency of Achilles enthesitis, low frequency of knee menisci chondrocalcinosis, and tendinous cal- caneal calcifications, and low hypervascularization at PDUS analysis in the wrist [19].

Morever, a percentage of PMR patients, ranging from 10 to 15% is reported as having a normal ESR.

The study conducted by Zaccaria in 2009 analyzed this specific subset of patients, comparing them to typical PMR. No significant differences were described in the two groups of patients, concluding that US findings may help in the diagnosis of PMR more than laboratory fea- tures [26].

The primary role of US in the diagnosis of PMR pa- tients determined the inclusion of this imaging tool in the new classification criteria, proposed by American College of Rheumatology (ACR) and European League Against Rheumatism (EULAR) in 2012 [16]. According to those criteria, US findings of bilateral shoulder abnor- malities (SAD bursitis/LTB tenosynovitis/GH effusion) or abnormalities in one shoulder and hip (hip effusion, trochanteric bursitis) may significantly improve the spec- ificity of the clinical criteria. Preliminary to the defini- tion of the last classification criteria, some of the experts participating in the study assessed the inter-observer reli- ability in evaluating shoulders and hips abnormalities in PMR patients [16].

Conclusions

This narrative review confirms that MSUS is able to identify an extensive inflammatory involvement of extra- articular synovial structures in PMR patients. According

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to data described in the literature, the presence of a typi- cal MSUS pattern in PMR can be identified: the shoulder seems to be the most affected site, showing US lesions in a higher percentage compared with others rheumatic conditions and with healthy controls; SAD bursitis, espe- cially when bilaterally, appeared to be the US lesion with the best diagnostic accuracy, followed by the presence of LTB tenosynovitis. Pelvic girdle is less frequently in- volved, with hip synovitis and trocanteric bursitis being the most relevant US lesions reported.

Generally, the depiction of bilateral abnormalities in both girdles achieves high specificity, but has low sensi- tivity. The presence of positive PD has been frequently reported, although this aspect has been investigated only in a few studies.

In order to improve the diagnostic accuracy, as re- ported in the recent classification criteria, US evaluation of shoulder and pelvic girdles is recommended in all pa- tients with suspected PMR [27].

Conflict of interest: none References

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