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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 16  |  Issue : 2  |  Page : 160-167

The role of ultrasonography in the diagnosis of painful shoulder syndrome in rheumatoid arthritis


1 Department of Physical Medicine, Rheumatology and Rehabilitation, Faculty of Medicine for Girls, Al Azhar University, Al Zahraa University Hospital, Cairo, Egypt
2 Department of Radiology, Faculty of Medicine for Girls, Al Azhar University, Al Zahraa University Hospital, Cairo, Egypt

Date of Submission17-Apr-2018
Date of Acceptance27-Nov-2018
Date of Web Publication27-Feb-2019

Correspondence Address:
Samia Abd El Hamid Abd El Megid
Rheumatology and Rehabilitation. Faculty of Medicine for Girls, 54 El Khalifa El Rady Street, Seventh District, Al Azhar University, Nasr City, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AZMJ.AZMJ_29_18

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  Abstract 

Aim of the work To identify the role of ultrasonography in diagnosis of painful shoulder syndrome in rheumatoid arthritis (RA).
Patients and methods A total of 45 patients with RA who fulfilled the ACR/EULAR 2010 criteria for RA were included, involving 65 shoulders. There were seven male and 38 female patients, and their mean age was 48.02±15.41 years. Their mean disease duration was 15.5±11.25 years. They were subjected to full history taking, thorough clinical examination, laboratory investigations, plain radiography, and shoulder ultrasonography.
Results The 65 RA shoulders were divided according to the disease activity score 28 (DAS28) into group A (with high DAS28), which included 15 (23%) shoulder joints, and group B (with moderate DAS28), which included 50 (77%) shoulder joints. Ultrasound findings of groups A and B revealed bicipital tenosynovitis in 47 and 22%, rotator cuff (RC) tendinopathy in 66.7 and 24%, humeral head erosions in 80 and 48%, effusion in 66.7 and 18%, subacromial/subdeltoid (SA/SD) bursitis in 66.7 and 28%, and positive power Doppler signals (PDS) in 60 and 14%, respectively. There was a highly significant difference in effusion and a significant difference in RC tendinopathy and SA/SD bursitis between both groups. There was a significant to highly significant difference in SA/SD bursitis, RC tendinopathy, and bicipital tenosynovitis between patients with positive and negative PDS.
Conclusion Ultrasonography is a useful tool in the diagnosis of shoulder pain in RA that can distinguish between various causes, helping in proper decision making regarding the treatment strategy. Bicipital tenosynovitis, SA/SD bursitis, glenohumeral joint effusion, humeral head erosions, and positive PDS were significant predictors of inflammatory nature of the painful shoulder syndrome.

Keywords: diagnosis, painful shoulder, rheumatoid arthritis, ultrasonography


How to cite this article:
El Megid SA, Abdel-Hak MT, Abd El Rahim MM, Abdel-Whab Hassan IH. The role of ultrasonography in the diagnosis of painful shoulder syndrome in rheumatoid arthritis. Al-Azhar Assiut Med J 2018;16:160-7

How to cite this URL:
El Megid SA, Abdel-Hak MT, Abd El Rahim MM, Abdel-Whab Hassan IH. The role of ultrasonography in the diagnosis of painful shoulder syndrome in rheumatoid arthritis. Al-Azhar Assiut Med J [serial online] 2018 [cited 2019 Mar 19];16:160-7. Available from: http://www.azmj.eg.net/text.asp?2018/16/2/160/253085


  Introduction Top


Shoulder involvement in rheumatoid arthritis (RA) is common. It can be subclinical and compromise the function of the upper limb [1]. Shoulder pain may be caused by different intra-articular, periarticular, and/or extra-articular mechanisms, which can be present in a broad range of inflammatory diseases, such as RA [2].

RA is a chronic inflammatory disease characterized by synovial inflammation, synovial hypertrophy, pannus formation, causing joint destruction, and associated deformities. Pannus formation leads to bony erosions that are specific to RA [3]. Moreover, the pathogenesis of rheumatoid synovitis has been strongly associated with synovial vascularity [4].

Synovitis may present with an anterior effusion resembling a mass. Subdeltoid/subacromial and scapulothoracic bursitis can occur. With chronic, untreated subacromial bursitis, inflammation can progress to destruction of the rotator cuff (RC) tendons, superior subluxation of the humeral head, and extension of the pannus into the glenohumeral joint [5],[6].

Ultrasound (US) has become an effective, noninvasive, reproducible, low-cost, irradiation-lacking, dynamic approach, and readily available tool to assess joints and surrounding areas in patients with different rheumatic conditions [7],[8],[9].


  Aim of the work Top


The aim of the work was to identify the role of ultrasonography in the diagnosis of painful shoulder syndrome in RA.


  Patients and methods Top


This study was conducted on 45 patients with RA who were diagnosed according to the ACR/EULAR 2010 classification criteria for RA. The procedures followed were in accordance with the ethical standards of Al Azhar committee on human experimentation and with the Helsinki Declaration of 1975, as revised in 2000, and all patients gave their written informed consent.

Patients were excluded from this study if they had a history of fracture or severe trauma of the shoulder, patients with any other inflammatory diseases that can affect the shoulder joint such as ankylosing spondylitis and crystal induced arthropathy, and patients who had comorbidity that might influence shoulder pain such as chest tumor, cardiac pain, and gall bladder diseases.

The patients were subjected to full history taking, thorough clinical examination (general examination, detailed articular examination, and shoulder examination), and assessment of disease activity in patients with RA by using 28 tender and swollen joint count [disease activity score (DAS28)]. Plain radiography of the shoulder was done as a routine for detection of soft tissue swelling, juxta-articular osteopenia, erosions, marginal sclerosis, superior migration of humeral head, narrow joint space, osteophytes, and cystic changes. Laboratory investigations were carried out: complete blood count, erythrocyte sedimentation rate, C-reactive protein, and rheumatoid factor. Shoulder ultrasonography was done; all patients were examined with commercially available ultrasound equipment using a 7–11 MHz linear phased array transducer (Xario200, Toshiba ultrasound machine; Toshiba, Toshiba medical systems corporation, Tochigi, Japan).

Shoulder ultrasonographic findings were evaluated according to Sanja and Mirjana [10]. The pathological findings were subdivided to the following:
  1. For long head of biceps (LHB) tendon: tendinopathy (transverse diameter above 3 mm in women and 3.3 mm in men), tenosynovitis (presence of fluid in tendon’s sheath), or subluxation from groove and tendon rupture.
  2. For supraspinatus (SSP) and infraspinatus (ISP) tendons: focal tendinopathy (focal hypertrophy above 5-mm longitudinal scan and focal hypoechogenicity), global tendinopathy (global hypertrophy above 5-mm longitudinal scan and uniform hypoechogenicity with/without small anechogenic areas as a sign of threatening partial rupture), and complete tendon rupture (nonvisualization of tendon).
  3. For subscapularis tendon (SSC): tendinopathy (hypertrophy and hypoechogenicity) and nonvisualization of tendon (established as complete tendon rupture).
  4. Subacromial/subdeltoid bursitis (SA/SD-B): distension of SA/SD-B above 2 mm with anechogenic or hypoechogenic fluid.
  5. Cartilage thickness (CT): normal CT was considered to be 2 mm; the humeral articular cartilage was seen between the SSP and ISP tendons and the humeral head.
  6. For the visualization of the joint effusion: the distance between joint capsule and inferior margin of ISP tendon above 2 mm was considered as a positive sign.
  7. Humeral head erosions (HE): the visualized humeral head and greater tuberosity were evaluated for bone erosions.


Statistical analysis

Data were analyzed using statistical program for the social science, version 20.0 (IBM Inc., NY city, NY, USA). Quantitative data were expressed as mean±SD. Qualitative data were expressed as frequency and percentage.

The following tests were done: χ2 test of significance was used to compare proportions between two qualitative parameters. P value was obtained. P value less than 0.05 was considered significant, P value less than 0.001 was considered as highly significant, and P value more than 0.05 was considered insignificant.


  Results Top


This study was conducted on 45 patients with RA who were diagnosed according to the ACR/EULAR 2010 classification criteria for RA. There were seven (15.56%) male and 38 (84.44%) female patients. Their ages ranged between 28 and 68 years, with a mean age of 48.0 years. Their disease duration ranged between 1 and 30 years, with a mean of 15.5 years. Their shoulder pain duration ranged between 1 and 48 months, with a mean of 24.5 months.

A total of 20 (44.5%) patients with RA had bilateral shoulder pain, 15 (33.3%) patients had right shoulder pain, and 10 (22.2%) patients had left shoulder pain, with a total number of 65 shoulders.

Ultrasonographic findings of LHB tendon in patients with RA revealed that 53 (81.5%) of 65 shoulders were affected, in the form of tenosynovitis (39.6%), tendinopathy (54.7%), and subluxation or rupture (5.6%) ([Figure 1] and [Figure 2]); supraspinatus tendon (SSP) was affected in 63 (∼97%) of 65 RA shoulders, in the form of tendinopathy (55.5%), focal tendinopathy (11.1%), partial tear (19%), and complete tear (14.3%) ([Figure 3]); infraspinatus tendon (ISP) was involved in 37 (∼57%) of 65 shoulders, in the form of tendinopathy in 70.27%, focal tendinopathy in 5.4%, partial tear in 13.5%, and complete tear in 10.8% ([Figure 4]); subscapularis tendon (SSC) was affected in 44 (67.7%) of 65 RA shoulders in the form of tendinopathy (77.3%), focal tendinopathy (13.6%), and partial or complete tear (9.1%); SA/SD-B was detected in 24 (∼37%) of 65 RA shoulders; glenohumeral joint effusion was present in 19 (∼29.3%) of 65 RA shoulders; CT reduction was found in 63 (∼97%) of 65 RA shoulders; and humeral HE was found in 36 (∼55.4%) of 65 RA shoulders ([Table 1] and [Table 2]).
Figure 1 Tenosynovitis of LHB with power Doppler signals (short axis). LHB, long head of biceps.

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Figure 2 Tenosynovitis of LHB with power Doppler signals (long axis). LHB, long head of biceps.

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Figure 3 Supraspinatus (SSP) tendinopathy (long axis).

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Figure 4 Infraspinatus (ISP) tendinopathy and cartilage thickness (long axis).

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{Table 1}{Table 2}

The 65 rheumatoid shoulders were divided according to the disease activity by DAS28 and power Doppler signals (PDS) on ultrasound joint examination into:
  1. Group A (high DAS28): it included 15 (23%) shoulder joints, where nine (60%) of them showed positive PDS on ultrasound joint examination, and six (40%) shoulders showed negative PDS.
  2. Group B (moderate DAS28): it included 50 (77%) shoulder joints, where seven (14%) of them showed positive PDS on ultrasound joint examination, and 43 (86%) shoulders showed negative PDS.


Regarding ultrasound findings of groups A and B, bicipital tenosynovitis was detected in 47 and 22%), RC tendinopathy in 66.7 and 24%, erosions in 80 and 48%, effusion in 66.7 and 18%, and SA/SD-B in 66.7 and 28%, respectively ([Figure 5]).
Figure 5 Comparative study between ultrasonographic findings in patients with high and moderate DAS28. DAS, disease activity score.

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Comparing between the ultrasonographic findings in patients with high DAS28 (group A) and moderate DAS28 (group B), there was a highly significant difference in effusion, significant difference in RC tendinopathy and SA/SD-B, and insignificant difference in bicipital tenosynovitis and erosion ([Figure 5]).

Comparing between the ultrasonographic findings of patients with high DAS28 (group A) with positive or negative PDS, a highly significant difference was found in SA/SD bursitis, RC tendinopathy, and bicipital tenosynovitis, and a significant difference in effusion and erosion ([Figure 6]).
Figure 6 Comparative study between ultrasonographic findings of patients with RA with high DAS28 with positive and negative power Doppler signals. DAS, disease activity score; RA, rheumatoid arthritis.

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[Figure 7] demonstrates a comparative study between the ultrasonographic findings of patients with moderate DAS28 (group B) with positive and negative PDS, a highly significant difference was found in bicipital tenosynovitis and effusion, and a significant difference in SA/SD-B, RC tendinopathy, and erosions.
Figure 7 Comparative study between ultrasonographic findings of patients with RA with moderate DAS28 with positive and negative power Doppler signals. DAS, disease activity score; RA, rheumatoid arthritis.

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  Discussion Top


The shoulder joint is frequently involved in patients with RA. In contrast to younger patients with RA, in late onset of RA, shoulder pain is frequently the first symptom of the disease [11]. The pain in the shoulder may be caused by various intra-articular and extra-articular pathological mechanisms. The painful shoulder in patients with RA may be caused not only by inflammation but also by noninflammatory diseases, such as degenerative disorders [11],[12].

US of the RA shoulders in this study generally revealed in LHB, tenosynovitis in 39.6%, tendinopathy in 54.7%, and subluxation or rupture in 5.6%; supraspinatus tendon (SSP) involvement in ∼97%; infraspinatus tendon (ISP) in ∼57%; subscapularis tendon (SSC) affection in ∼67.7%; SA/SD-B in ∼37%; glenohumeral joint effusion in ∼29.3%; CT reduction in ∼97%; and humeral HE in ∼55.4%.

These results are in agreement with a previous study [13], which detected by US examination tenosynovitis of the LHB tendon in 40% of the examined shoulders, erosions in 82% of the glenohumeral joints, synovitis of the glenohumeral joint in 30%, and bursitis in 36%.

Another study reported that bicipital tendinitis was detected in 63% of patients with RA, RC lesion in 65%, erosion in 12%, effusion in 28.6%, and SA/SD-B in 45.5% [10]. Moreover, these results are in agreement with a study done by Stegbauer et al. [11], who used ultrasonography to investigate causes of new onset of shoulder pain and sites of shoulder inflammation. US detected tenosynovitis of biceps tendon in 35%, effusion and/or synovitis in 58.6%, and subdeltoid bursitis in 35.7%.

This can be interpreted as the biceps tendon sheath and the SA/SD-B may become affected by synovitis that irritates RC tendons and biceps tendon. In addition, inflammation of the acromioclavicular joint or subacromial bursa leads to impingement of the RC tendons between the humeral head and the coracoacromial arch that contributes to progressive RC damage.

Overuse activity coupled with coracoacromial arch changes have a significant effect on RC injury. Significant relationships have been demonstrated between acromion morphology, the patient’s self-reported shoulder function, and the severity of the RC pathology [14],[15].

Others reported a lower incidence of SA/SD-B in patients with RA (29%) [16] or higher incidence (45.5%) [10], and higher incidence of glenohumeral joint effusion (58.6%) [11]. These variations in findings could be interpreted as glenohumeral joint effusion or synovitis is affected by the inflammatory process of the RA in the shoulder and thus influenced by if there is good RA disease control or not.

A previous study reported that humeral HEs in patients with RA were from 50% upon 80% [17]. Other reported studies described bone erosions in patients with RA in lower percentage versus ours, such as 20% [16] and 12% [10], or in higher percentage versus ours (82%) [13], which could be owing to different sample size, good RA disease control, or variable disease duration.

When dividing the RA shoulders into group A with high DAS and group B with moderate DAS, bicipital tenosynovitis was detected in 47 and 22%, RC tendinopathy in 66.7 and 24%, erosions in 80 and 48%, effusion in 66.7 and 18%, and SA/SD-B in 66.7 and 28%, respectively.

In the present study, we found that PDS demonstrates vascularity in the long bicipital tendon sheath in 74% of the patients with RA. These results were in agreement with Strunk et al. [18] who concluded that PDS demonstrates vascularity in the long bicipital tendon sheath in 91.7% of patients with RA, but not in those with degenerative shoulder disorders. Another study stated that US and power doppler ultrasound (PDUS) are mandatory to elucidate the origin of inflammatory and noninflammatory shoulder pain. PDUS showed increased microvascular blood flow in 75% of investigated shoulders [11]. Bursitis and/or tenosynovitis were accompanied by glenohumeral synovitis in 75% of the examined shoulders. Patients with active synovitis had higher DAS28 compared with patients without active synovitis. One of the most conspicuous signs of synovitis is the increase in synovial vascularization owing to angiogenesis, which is crucial for synovial growth and invasiveness [19].

Our study revealed that PDUS showed increased microvascular blood flow in 60% of the RA shoulders with high DAS and in 14% of the shoulders with moderate DAS.

These results are in agreement with a previous study that found a correlation between PD and disease activity in patients with RA with active disease [20]. Other authors concluded that patients with inflammatory involvement of the shoulders had significantly higher DAS28 compared with patient with no inflammatory signs [21]. Another study documented that there is a good correlation between the change in DAS28 with the change in PDUS score [22]. It is suggested that the ongoing inflammation is driven by similar mechanisms in the tenosynovium and joint synovium and that RA is probably a tissue-specific disease that targets systemic synovial tissues [23].

RA requires both improvement of overall disease activity and the disappearance of local synovial vascularity for remission. The evaluation of synovial vascularity provides various information and contributes to the clinical treatment of RA [3].


  Conclusion Top


This study had proved that ultrasonography is useful in the diagnosis of shoulder pain in RA by differentiating between various causes which allows the rheumatologist to properly decide the clinical algorithm of treatment. Bicipital tenosynovitis, SA/SD-B, glenohumeral joint effusion, humeral HEs, and positive PDS were significant predictors of inflammatory nature of the painful shoulder syndrome.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]
 
 
    Tables

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