Doppler sonographic findings in the long bicipital tendon sheath in patients with rheumatoid arthritis as compared with patients with degenerative diseases of the shoulder

Authors


Abstract

Objective

To compare power Doppler sonography (PDS) findings inside the bicipital tendon sheath in patients with rheumatoid arthritis (RA) and degenerative disorders of the shoulder, in order to evaluate the diagnostic value of PDS in distinguishing between inflammatory and noninflammatory shoulder pain.

Methods

The glenohumeral joints of 41 consecutive patients with shoulder pain were examined by ultrasound. Using ventral transverse and longitudinal scanning, the vascularity near and/or inside the bicipital tendon sheath was visualized by PDS. One fully trained and experienced examiner performed the sonography. Representative images were digitally stored and were read, under blinded conditions, by 2 independent investigators, who categorized the Doppler signals as being either inside or outside the tendon sheath.

Results

Biceps tendon sheath effusion, represented by the typical hypoechoic rim, was found in 95.8% of the RA patients (23 of 24) and in 58.8% of the patients with degenerative disorders (10 of 17). PDS signals were localized to inside the tendon sheath in 22 of the RA patients (91.7%) and in none of the patients with degenerative disorders. Although no PDS signal was found inside the tendon sheath in patients with degenerative disorders, in 9 of these patients (52.9%), signals could be localized to the environment of the tendon sheath.

Conclusion

PDS demonstrates vascularity in the long bicipital tendon sheath of patients with RA, but not in those with degenerative shoulder disorders.

Shoulder pain is among the most common symptoms reported by patients of rheumatologists. It is caused by a broad range of inflammatory and noninflammatory diseases, such as rheumatoid arthritis (RA) or degenerative disorders including, among others, impingement syndrome, lesions of the rotator cuff, and shoulder instability (1). For many years joint sonography has been an established imaging technique for the diagnosis and evaluation of a painful shoulder. As well as visualization of soft tissue and detection of fluid collection, ultrasound allows dynamic examination of joint and tendon movements (2).

Technologic improvements such as power Doppler sonography (PDS) enable the assessment of vascular tissues along with the detection of low-velocity blood flow at the microvascular level. There have been several studies on the visualization of vascularized synovium by PDS in joints and tendon sheaths of patients with RA (3, 4). Bicipital tenosynovitis is a common finding both in RA and in degenerative disorders. On gray-scale sonography it is represented by a peritendineous hypoechoic rim, which is described by Sattler (5) as a nonspecific finding in a great variety of the above-mentioned disorders. The demonstration of peritendineous blood flow by PDS suggests that the hypoechoic rim represents vascularized synovium in some cases, rather than complex fluid (6). In the present study we compared PDS findings inside the bicipital tendon sheath in patients with RA and patients with shoulder degenerative disorders, to assess the diagnostic value of PDS in distinguishing between inflammatory and noninflammatory shoulder pain.

PATIENTS AND METHODS

The glenohumeral joints of 41 consecutive patients with shoulder pain were examined by ultrasound (Table 1). The group consisted of 26 women and 15 men (age range 43–78 years). Twenty-four of the patients had RA, with widely ranging disease duration (2 months–50 years). Most of the patients, except for those whose RA was newly diagnosed, had been treated long-term with glucocorticoids and/or disease-modifying antirheumatic drugs. Shoulder pain was evaluated by clinical examination in which the patient moved his or her hand behind the neck and the back as high as possible; external rotation and internal rotation were determined.

Table 1. Clinical characteristics, treatment, and sonographic and power Doppler sonographic findings in the bicipital tendon sheath of the study patients*
Patient/age/sexShoulder studiedClinical diagnosisDisease durationEffusionPDS signal outside tendon sheathPDS signal inside tendon sheathCRP, mg/dlTreatment
  • *

    PDS = power Doppler sonography; CRP = C-reactive protein; R = right; RA = rheumatoid arthritis; Pred. = prednisone; DD = degenerative disorder; L = left; NSAID = nonsteroidal antiinflammatory drug; MTX = methotrexate; LEF = leflunomide.

1/63/MRRA6 months+++2.8Pred.
2/70/FRDD 0.4 
3/50/FRDD +1.0 
4/64/MRDD ++  
5/66/FLRA50 years+++3.9Pred., NSAID
6/62/FRRA10 years+++5.2NSAID
7/66/FRRA1 year+++2.0MTX, NSAID
8/69/FRRA1 year+++0.4Pred., MTX
9/78/FRRA10 years+++2.7Pred.
10/70/MRRA35 years+++7Pred., MTX, NSAID
11/56/FRRA3 years+++1.4MTX, NSAID
12/49/FRDD +0 
13/47/FLDD +1.0 
14/65/FLRA6 years+++7.1Pred., MTX
15/77/FLRA19 years+++3.6Pred., NSAID
16/74/FRRA4 months++1.8Pred., MTX
17/75/FRRA3 months+++0.8NSAID
18/45/FLDD +0 
19/53/FLDD +0.1 
20/66/FLRA17 years+++2.9Pred., NSAID
21/67/MLRA5 years++2.6Pred.
22/72/MRRA2 months+++14NSAID
23/43/FRDD ++0 
24/55/FRDD 0.2 
25/55/FRDD ++0.2 
26/51/FRDD ++1.6 
27/72/FRRA2 months+++5.8NSAID
28/59/FRDD 0.4 
29/64/MRRA6 months+++4.6Pred.
30/50/FRDD ++0.4 
31/57/MLRA8 years+++2.5NSAID
32/74/MRRA4 months+++5.9Pred., MTX
33/59/MLRA2 months+++2.2Pred., NSAID
34/58/MLDD ++0.7 
35/65/MRRA15 years++10.4Pred., MTX
36/72/MRRA5 months++0.4NSAID
37/71/MLRA1 year++2.9Pred., LEF
38/51/MRDD ++0.2 
39/71/MRRA6 months+++2.4Pred., LEF
40/62/FRDD 0.6 
41/60/FRDD 0.2 

Ultrasonography was carried out using a 7.5-MHz transducer (Image Point; Hewlett-Packard, Bad Homburg, Germany). Standardized scans were performed according to previously described guidelines for investigation of the shoulder joint (7), to detect tendon sheath effusion in the bicipital groove, represented by the typical hypoechoic rim. Since there is a large degree of variability in the amount of fluid in the tendon sheath, a comparison with the healthy shoulder was needed in order to determine whether the amount of effusion was pathologic. Although precise quantification of effusion is not possible, the width of the “hypoechoic rim” ranged from 2 mm to 5 mm.

Using ventral transverse and longitudinal scanning at the bicipital groove with the shoulder in neutral position, the vascularity near and/or inside the bicipital tendon sheath was visualized by PDS (Figure 1). Power Doppler settings were standardized with a pulse repetition frequency of 800–1,000 Hz, and the gain was set as suggested by Rubin et al (8). This requires manual elevation of the PDS gain level until the color box is almost uniformly filled with the first indicated color, and with only the minimum amount of the next-highest signal just starting to appear. Only minimal pressure was exerted with the probe on the patient's skin, to avoid compression and collapse of blood vessels.

Figure 1.

a–d, Ventral transverse and e and f, longitudinal ultrasonographic scans of the shoulder, demonstrating the long bicipital tendon with its tendon sheath. a, Tendon sheath without effusion or power Doppler signal (PDS). b, Tendon sheath with marked effusion, without PDS. c and e, Effusion inside the tendon sheath, and PDS outside. d and f, Effusion and PDS inside the tendon sheath.

One fully trained and experienced examiner (JS) performed the sonography. Representative images were digitally stored and were read by 2 independent investigators who were blinded to the patients' clinical and laboratory findings. They localized the Doppler signals as being either inside or outside the tendon sheath.

RESULTS

Biceps tendon sheath effusion, represented by the typical hypoechoic rim, was observed in 23 of the 24 RA patients (95.8%) and in 10 of the 17 patients (58.8%) with degenerative disorders of the shoulder. PDS signal was localized as being inside the tendon sheath in 22 RA patients (91.7%) and in none of the patients with degenerative disorders. In all of these cases the examiner and the 2 investigators were in agreement, except in 1 RA patient, in whom the signal was localized to outside of the tendon sheath (interobserver agreement κ = 0.95). Although no PDS signal was found inside the tendon sheath in patients with degenerative disorders, signal could be localized to the environment of the tendon sheath in 9 of them (52.9%). Occasionally, the blood vessels reached the edge of the sheath in patients with shoulder degenerative disorders, but in no case could these be visualized coursing directly into the tendon sheath itself (Figure 2). Moreover, ultrasound investigation of the shoulder revealed lesions of the rotator cuff in some patients with RA or degenerative disorders, and effusion in the shoulder joint and/or in the subdeltoid bursa in most of the RA patients.

Figure 2.

Number of patients with shoulder degenerative disorders (Deg. Disord.) or rheumatoid arthritis (RA) in whom power Doppler signal (PDS) was found, and location of signal. PDS was found inside the bicipital tendon sheath in 91.7% of RA patients and in none of the patients with degenerative disorders. Biceps tendon sheath effusion and PDS outside the tendon sheath were found in both groups.

DISCUSSION

Musculoskeletal ultrasound has become an established imaging technique in the diagnosis of rheumatic diseases. It is commonly used in the detection of fluid collection in joints and tendon sheaths, as well as in the assessment of soft tissue, cartilage, tendons, and bone surface (9). Technologic advances in recent years have resulted in higher resolution and have made possible the assessment of synovial proliferation (10). In particular, ultrasonographic examination of the shoulder has become an established diagnostic tool. Nevertheless, most sonographic findings are nonspecific. For example, fluid collection may be caused by trauma, inflammation, or degenerative disorders, and synovial thickening can represent tissue debris, blood clots, fibrin, or an inflammatory proliferation.

While conventional color Doppler sonography encodes the mean Doppler frequency shift, power Doppler encodes the amplitude of the spectral density of the Doppler signal, so it is well-suited for detecting low-velocity blood flow at the microvascular level. Several studies have demonstrated the reliability of PDS for visualization of the vascularity of synovial tissue (11). Walther et al showed a correlation between qualitative estimates of blood flow by PDS and vascularity in a histologic section (3). Because magnetic resonance imaging (MRI) is the predominant technique used for visualization of synovial tissue and its vascularity, some studies have correlated MRI findings with power Doppler sonographic detection of blood flow in synovial tissue (12). Investigation of tendons in patients with RA reveals the common appearance of Doppler signals inside the tendon sheaths. Breidahl et al (6) suggested that PDS enables one to distinguish between hypoechoic fluid and synovium inside the tendon sheath, through visualization of small blood vessels.

The tendon of the long head of the biceps brachia is a stabilizer of the humeral head in the glenoid, especially during abduction of the shoulder, as well as of the anterior joint capsule itself. Moreover, it is able to compensate for inadequate rotator cuff function, which results in extreme stress on the tendon, causing it to become a site of predilection for degenerative lesions. The signs of biceps tendon disease on ultrasound include alterations in shape, changes in signal intensity, thickening of the tendon sheath, and the typical hypoechoic rim, which represents effusion (13). Similarly, in RA and especially in so-called “elderly-onset RA,” biceps tendon sheath effusion is often found (14); however, there is a great difference in the pathogenesis of effusion in RA and that in degenerative disorders. The deterioration of the bicipital gliding mechanism is the reason for fluid in the tendon sheath in degenerative disorders, while in RA it is exudative and proliferative synovitis. It is possible that scar tissue formed inside and in the vicinity of the tendon sheath in certain degenerative disorders also exhibits hypervascularity; however, we did not observe this in the limited number of patients with degenerative disorders we studied.

Jain et al demonstrated that tenosynovium in RA produces not only inflammatory enzymes and proteolytic enzymes, but also vascular endothelial growth factor, which suggests that angiogenesis has a role in tenosynovial proliferation and invasion of tendons (15). In the present study, which included patients with RA representing a wide range of forms and stages, Doppler sonographic demonstration of blood flow inside the bicipital tendon sheath indicated that with this method visualization of angiogenesis, an important pathogenic factor in inflammatory rheumatic diseases, can be used to distinguish RA from degenerative disorders of the shoulder. It would be of interest to use PDS to investigate other hyperemic shoulder disorders, such as psoriatic arthritis, gout, septic arthritis, or arthritis in spondylarthropathy, and to compare the findings with those in RA patients and healthy controls.

Acknowledgements

We are grateful to Dr. Mi Strunk for interpretation of the sonographic images.

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