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Br J Radiol. 2012 November; 85(1019): 1482–1487.
PMCID: PMC3500791

Contrast-enhanced MRI of the subdeltoid, subacromial bursa in painful and painless rotator cuff tears

R J Hodgson, PhD, FRCR,1,3 P J O'Connor, FRCR, MRCP,1,2 E M A Hensor, PhD,1,3 D Barron, FRCR,2 and P Robinson, FRCR, MRCP1,2

Abstract

Objective

Although shoulder pain is often associated with rotator cuff tears, many tears are asymptomatic and are not the cause of the patient's pain. This may explain the persistence of symptoms in some patients despite technically successful rotator cuff repair. It has been proposed that rotator cuff tears cause pain through subdeltoid/subacromial bursal inflammation. The aim of this study was to determine whether bursal inflammation seen on MRI is associated with pain in patients with rotator cuff tears of the shoulder.

Methods

The shoulders of 255 patients were screened with ultrasound. 33 full-thickness rotator cuff tears (18 with shoulder pain and 15 without pain) were identified and subsequently studied using contrast-enhanced MRI of the shoulder. Enhancement of the subacromial bursa was scored independently by two musculoskeletal radiologists. Logistic regression was used to determine whether bursal enhancement was independently associated with pain.

Results

There was a significant association between pain and age, with greater likelihood of pain in younger patients. Bursal enhancement was common in both painful and painless tears. No statistically significant link between pain and bursal enhancement was seen, even after accounting for age.

Conclusion

Although enhancement of the subdeltoid/subacromial bursa was common, no evidence was found to support the hypothesis that bursal enhancement is associated with pain in rotator cuff tears. It is therefore unlikely to determine reliably which patients would benefit from rotator cuff repair.

Advances in knowledge

Bursal enhancement and thickening does not reliably correlate with symptoms or presence of rotator cuff tear.

Rotator cuff tears are a common cause of pain in the shoulder. Surgical repair is an effective treatment, but a significant proportion of patients (5–12.5%) fail to achieve a satisfactory outcome [1-4]. Long-term outcome of surgery correlates poorly with the integrity of the cuff repair [5-7] and persistence of pain is a major factor [1]. In some cases, this may be because the shoulder pain is not due to rotator cuff damage at all [8]. Other painful shoulder pathologies are common, particularly in the elderly, including glenohumeral and acromioclavicular arthritis [9], and bone marrow oedema [10]. Asymptomatic rotator cuff tears are common, with increasing incidence with age and a reported prevalence of up to 80% in subjects aged over 80 years [11]. A significant proportion of these are full-thickness tears with one study reporting full-thickness tears in 28% of people over the age of 60 [12]. Rotator cuff tears may remain asymptomatic despite their large size [13] and, although the size of tears often increases, symptoms may develop or resolve with conservative treatment [14-16]. As yet there is no clear consensus regarding the indications for rotator cuff surgery [17,18]. A technique to determine whether a known rotator cuff tear is responsible for an individual patient's pain would therefore be of great clinical value in developing patient management plans. While MRI has been shown to be accurate for detecting rotator cuff tears [19,20], there is no convincing evidence to date that it can be used to determine whether a full-thickness tear is symptomatic [12,21].

The mechanism by which rotator cuff tears cause pain is poorly understood. Tears are associated with histological inflammation of the subdeltoid/subacromial bursa and this has recently been proposed as a cause of pain [22]. Synovial inflammation in the bursa in symptomatic rotator cuff tears could potentially be detected by the associated enhancement in the inflamed bursa seen on MRI after the administration of intravenous contrast agent, in the same way that synovial volume in joints in inflammatory arthritis has been shown to correlate with histological measures of inflammation [23]. The aim of this study was to use contrast-enhanced MRI to assess subacromial bursitis in patients with painful and painless rotator cuff tears in order to test the hypothesis that synovial enhancement at the subacromial bursa is greater in patients with shoulder pain.

Methods and materials

Patients

A group of patients with rotator cuff tears and shoulder pain was recruited from consecutive primary care clinical referrals to the shoulder ultrasound service for shoulder pain with sonographic evidence of a full-thickness rotator cuff tear.

A group of patients with a rotator cuff tear without shoulder symptoms was recruited from consecutive referrals for ultrasound of other regions. Ultrasound of the shoulder was performed and those patients with an incidental full-thickness rotator cuff tear were included in the study. Participants were questioned about the presence of any shoulder symptoms and excluded if they reported any symptoms within the preceding year, there was a history of trauma to the shoulder or the patient had a clinical diagnosis of arthritis involving the shoulder or any other joint.

The study was approved by the local research ethics committee and informed consent was obtained from all participants.

Patient symptoms

Participants completed a shoulder rating questionnaire to assess shoulder pain and its limitation of activity, recreation and work [24]. The global domain score is measured on a 10 cm visual analogue score line ranging from 0 (very poorly) to 10 (very well). The remaining domain scores are calculated from the responses to various questions measured on rating scales; each has a minimum of two (indicating the most severe symptoms) and a maximum of 10 (indicating no symptoms).

Ultrasound

Ultrasound was performed by an experienced consultant musculoskeletal radiologist using an Antares ultrasound machine with a 13.5 MHz linear array transducer (Siemens Healthcare, Erlangen, Germany). The presence or absence of a full-thickness rotator cuff tear was determined using the local standardised ultrasound scanning protocol [25].

MRI

MRI images of the shoulder were acquired using a 1.5 T Gyroscan AXS-NT Scanner (Philips, Best, Netherlands) and a dedicated shoulder coil with the arm by the side in the neutral position. The following images were acquired:

  • proton density-weighted coronal-oblique: repetition time (TR), 2628 ms; echo time (TE), 15 ms; slice thickness, 3 mm; field of view, 16 cm; 256×177 matrix
  • T2 weighted coronal-oblique fat-suppressed: TR, 5332 ms; TE, 100 ms; slice thickness, 3 mm; field of view, 16×13 cm; 256×201 matrix)
  • STIR sagittal-oblique: TR, 1200 ms; TE, 15 ms; slice thickness, 4 mm; field of view, 16×13 cm; 256×204 matrix.

T1 weighted images were acquired before and after the administration of 0.1 mmol kg−1 gadopentetate dimeglumine (Magnevist, Bayer Schering, Leverkusen, Germany) in the coronal-oblique (TR, 500 ms; TE, 15 ms; slice thickness, 3 mm; field of view, 16×13 cm; 256×154 matrix) and sagittal (TR, 375 ms; TE, 14 ms, slice thickness, 3 mm; field of view, 16×13 cm; 256×154 matrix) planes. Contrast-enhanced images were acquired with fat suppression.

MRI scoring

MRI images were assessed independently by two experienced consultant musculoskeletal radiologists blinded to symptoms. Enhancement of the subacromial bursa was assessed using T1 weighted fat-suppressed sagittal-oblique and coronal-oblique contrast-enhanced images. Images were scored on a scale of 0–2 depending on the maximum thickness of enhancing tissue: 0, no abnormal enhancement; 1, up to 3 mm thickness of enhancing tissue; 2, 3 mm or more enhancing tissue (Figures 1 and and22).

Figure 1
Grade 2 subacromial bursitis. There is enhancing tissue >3 mm in thickness in the subacromial bursa.
Figure 2
Grade 1 subacromial bursitis. There is enhancing tissue <3 mm in thickness in the subacromial bursa.

Statistics

To compare agreement between the two observers, the kappa statistic was calculated for the subacromial bursal enhancement scores, in addition to prevalence-adjusted, bias-adjusted kappa (PABAK) [26] and the proportion of scores over which the raters were in exact agreement (PEA). Category-specific proportions of agreement, representing the probability that the second scorer would place a subject in that specific category given that the first scorer placed them in that category, were also calculated.

To determine whether subacromial bursal enhancement was linked to shoulder pain, exact binary logistic regression was performed with age, sex and bursal enhancement as independent variables; adjusted odds ratios (ORs) and 95% confidence intervals (CIs) were calculated for each. Analyses were conducted in SPSS® v. 18.0.3 (SPSS Inc., Chicago, IL) and LogXact® v. 8.0 (Cytel Inc., Cambridge, MA).

Results

18 rotator cuff tears were found out of a total of 53 patients undergoing ultrasonography for shoulder pain. 31 rotator cuff tears were found out of a total of 202 patients undergoing ultrasonography of other regions; 11 met exclusion criteria and 5 patients were unable to tolerate MRI, leaving 15 patients with painless tears.

Symptomatic patients were younger on average (mean symptomatic=55.4, 95% CI=52.2–58.7; asymptomatic=65.2, 95% CI=61.1–69.3) and a much larger proportion were female (proportion symptomatic=72% (13/18), 95% CI=49–88%; asymptomatic=13% (2/15), 95% CI=3–38%).

MRI confirmed the presence of a full-thickness tear of the rotator cuff in all patients diagnosed on ultrasound (e.g. Figure 3). The mean size of the rotator cuff tear was 2.4×2.3 cm in the asymptomatic group and 2.1×2.0 cm in the symptomatic group.

Figure 3
Example of an asymptomatic patient with a large rotator cuff tear and marked changes, including reduction of the distance between the acromion and the humeral head, supraspinatus atrophy, subacromial, glenohumeral and acromioclavicular enhancement, and ...

The results of the shoulder symptoms questionnaire are shown in Table 1. Two subjects did not complete the questionnaire. One subject in the asymptomatic group subsequently reported mild symptoms on the questionnaire. As expected, scores were considerably lower in the subjects with pain.

Table 1
Shoulder rating questionnaire results

The kappa statistic for interobserver agreement of the subdeltoid/subacromial bursal enhancement score was 0.61 (95% CI=0.22–1.00). The prevalence index (the imbalance in the distribution of scores) was 72.7%; when this was accounted for the adjusted kappa was higher (PABAK=0.82). The raters exactly agreed over the majority of scores (PEA=90.9%); however, the agreement was poorer for Grade 2 (66.7%) than for Grade 1 (94.7%).

Subdeltoid/subacromial enhancement (≥Grade 1) was seen in all patients in both the symptomatic and asymptomatic group. Grade 2 enhancement was seen in most shoulders (29/33; 88% overall), including 12/15 (80%) of asymptomatic and 17/18 (94%) of symptomatic patients.

Exact binary logistic regression indicated that the odds of a tear being symptomatic reduced with age (OR=0.84, 95% CI=0.69–0.98, p=0.021) and may be increased in females (OR=8.91, 95% CI=0.83–460.48, p=0.082), but having controlled for these factors there was no clear association between pain and subacromial enhancement (OR=20.44, 95% CI=0.03–22347.73, p=1.00).

Discussion

The aim of the current study was to determine whether shoulder pain was associated with contrast enhancement at the subacromial bursa in patients with rotator cuff tears. There was no significant evidence for a link between pain and enhancement, with only slightly greater enhancement in the group with shoulder pain. No significant association was found between pain and enhancement despite taking into account the age and sex differences between the symptomatic and asymptomatic patient groups, although increased age was associated with painless rotator cuff tears. Were more subjects to be included in a future study, a statistically significant association with subacromial enhancement might emerge, but assuming the same large proportion of patients had Grade 2 subacromial enhancement its predictive utility would nevertheless be limited. The high level of enhancement in asymptomatic patients (80% showed Grade 2 enhancement) means subdeltoid/subacromial enhancement is unlikely to be useful for discriminating between painful and painless rotator cuff tears.

These results have implications for understanding the mechanisms for pain in rotator cuff tears. Since bursitis was common in the asymptomatic group, it seems unlikely that the presence of subacromial bursitis (as determined by MRI) is the sole determinant of pain in patients with rotator cuff pathology. This is consistent with a previous study that looked at the volume of fluid in the subdeltoid/subacromial bursa using indirect magnetic resonance arthrography [27], finding no relationship to shoulder symptoms. Other studies have looked at other factors that may be related to rotator cuff pain and have shown mixed results for tear size, with a link between symptoms and tear size demonstrated in larger studies compensating for age [28,29].

Our study showed an incidence of full-thickness rotator cuff tears on shoulder ultrasound of 15% without shoulder symptoms referred for ultrasound for other reasons. The mean age of these patients was 66 years. This is consistent with a large previously reported study of full-thickness tears in asymptomatic volunteers over 50 years of age, which showed an overall incidence of 8%, with a strong dependence on age [30].

Logistic regression was used in the current study to allow the relationship between bursal enhancement and pain to be studied independently of patient age. In this study population, the age of patients in the group with shoulder pain was lower than that of patients without pain. A similar age difference was seen in a recent publication comparing symptomatic and asymptomatic tears [29], although this has not been present in all studies [31], possibly reflecting differences in underlying study populations. In particular, it seems likely that younger patients with symptoms may be referred more commonly for ultrasound assessment at our institution.

Interobserver reproducibility for subacromial bursal enhancement assessed using the three-point scoring system presented was fair to good (κ=0.61) [32]. The high levels of bursitis identified in both symptomatic and asymptomatic patients (>85% patients scoring the maximum in both groups) might suggest a grading system with more points (subdividing Group 2) could be used, but the authors felt this would reduce interobserver agreement. Direct volume measurement of enhancing bursitis might be an alternative, as for joint synovitis [33], and has the advantage of providing a continuous measure with the potential to discriminate better between groups; however, the high surface area of the subdeltoid/subacromial bursa would be likely to impact on the reproducibility of such measurements.

A limitation of this study is the small size of the groups, and particularly the asymptomatic group, which consisted of only 15 subjects, despite screening over 200 participants. This study would allow the formal powering of a larger study to detect statistically significant differences between symptomatic and asymptomatic groups. Such a study would also benefit from age-matching of the symptomatic and asymptomatic groups. Nevertheless, given the high levels of synovitis demonstrated in patients without shoulder pain in the current study and the inability to detect a significant difference between groups of 15–18 subjects, it is clear that the presence of enhancing synovitis is extremely unlikely to be clinically useful for determining whether pain in a particular patient is the result of an underlying rotator cuff tear. Another limitation of the study to be considered is the underlying assumption that bursal inflammation correlates with MRI enhancement. Although the link between MRI enhancement and histological markers of inflammation has been demonstrated in the knee in rheumatoid arthritis, this has not been proven for subacromial bursitis [23], and dynamic contrast-enhanced MRI may be a better measurement of inflammatory activity [34-37].

In conclusion, this study showed enhancement in the subdeltoid/subacromial bursa is common in the presence of a rotator cuff tear both in patients with shoulder pain and in patients without pain. No evidence was found to support the hypothesis that pain is closely related to synovial enhancement due to subacromial bursal inflammation. Bursal enhancement is unlikely to be helpful in determining whether shoulder pain is arising from a rotator cuff tear.

Acknowledgment

The authors would like to acknowledge the assistance of Dr R Sinha, consultant radiologist, Newcastle upon Tyne.

Footnotes

This project was funded by the Royal College of Radiologists, UK, the British Society of Skeletal Radiologists and the National Institute for Health Research, UK.

References

1. Tashjian RZ, Bradley MP, Tocci S, Rey J, Henn RF, Green A. Factors influencing patient satisfaction after rotator cuff repair. J Shoulder Elbow Surg 2007;16:752–8. [PubMed]
2. Romeo AA, Hang DW, Bach BR, Jr, Shott S. Repair of full thickness rotator cuff tears. Gender, age, and other factors affecting outcome. Clin Orthop Relat Res 1999;367:243–55. [PubMed]
3. Watson EM, Sonnabend DH. Outcome of rotator cuff repair. J Shoulder Elbow Surg 2002;11:201–11. [PubMed]
4. Cofield RH, Parvizi J, Hoffmeyer PJ, Lanzer WL, Ilstrup DM, Rowland CM. Surgical repair of chronic rotator cuff tears. A prospective long-term study. J Bone Joint Surg Am 2001;83A:71–7. [PubMed]
5. Gazielly DF, Gleyze P, Montagnon C. Functional and anatomical results after rotator cuff repair. Clin Orthop Relat Res 1994;304:43–53. [PubMed]
6. Jost B, Pfirrmann CW, Gerber C, Switzerland Z. Clinical outcome after structural failure of rotator cuff repairs. J Bone Joint Surg Am 2000;82:304–14. [PubMed]
7. Knudsen HB, Gelineck J, Sojbjerg JO, Olsen BS, Johannsen HV, Sneppen O. Functional and magnetic resonance imaging evaluation after single-tendon rotator cuff reconstruction. J Shoulder Elbow Surg 1999;8:242–6. [PubMed]
8. Iannotti JP. Full-thickness rotator cuff tears: factors affecting surgical outcome. J Am Acad Orthop Surg 1994;2:87–95. [PubMed]
9. Zingg PO, Jost B, Sukthankar A, Buhler M, Pfirrmann CW, Gerber C. Clinical and structural outcomes of nonoperative management of massive rotator cuff tears. J Bone Joint Surg Am 2007;89:1928–34. [PubMed]
10. McCauley TR, Disler DG, Tam MK. Bone marrow edema in the greater tuberosity of the humerus at MR imaging: association with rotator cuff tears and traumatic injury. Magn Reson Imaging 2000;18:979–84. [PubMed]
11. Milgrom C, Schaffler M, Gilbert S, van Holsbeeck M. Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender. J Bone Joint Surg Br 1995;77:296–8. [PubMed]
12. Sher JS, Uribe JW, Posada A, Murphy BJ, Zlatkin MB. Abnormal findings on magnetic resonance images of asymptomatic shoulders. J Bone Joint Surg Am 1995;77:10–15. [PubMed]
13. Tempelhof S, Rupp S, Seil R. Age-related prevalence of rotator cuff tears in asymptomatic shoulders. J Shoulder Elbow Surg 1999;8:296–9. [PubMed]
14. Yamaguchi K, Tetro AM, Blam O, Evanoff BA, Teefey SA, Middleton WD. Natural history of asymptomatic rotator cuff tears: a longitudinal analysis of asymptomatic tears detected sonographically. J Shoulder Elbow Surg 2001;10:199–203. [PubMed]
15. Baydar M, Akalin E, El O, Gulbahar S, Bircan C, Akgul O, et al. The efficacy of conservative treatment in patients with full-thickness rotator cuff tears. Rheumatol Int 2009;29:623–8. [PubMed]
16. Beaudreuil J, Bardin T, Orcel P, Goutallier D. Natural history or outcome with conservative treatment of degenerative rotator cuff tears. Joint Bone Spine 2007;74:527–9. [PubMed]
17. Dunn WR, Schackman BR, Walsh C, Lyman S, Jones EC, Warren RF, et al. Variation in orthopaedic surgeons' perceptions about the indications for rotator cuff surgery. J Bone Joint Surg Am 2005;87:1978–84. [PubMed]
18. Marx RG, Koulouvaris P, Chu SK, Levy BA. Indications for surgery in clinical outcome studies of rotator cuff repair. Clin Orthop Relat Res 2009;467:450–6. [PMC free article] [PubMed]
19. Farley TE, Neumann CH, Steinbach LS, Jahnke AJ, Petersen SS. Full-thickness tears of the rotator cuff of the shoulder: diagnosis with MR imaging. AJR Am J Roentgenol 1992;158:347–51. [PubMed]
20. Evancho AM, Stiles RG, Fajman WA, Flower SP, Macha T, Brunner MC, et al. MR imaging diagnosis of rotator cuff tears. AJR Am J Roentgenol 1988;151:751–4. [PubMed]
21. Williams GR, Jr, Rockwood CA, Jr, Bigliani LU, Iannotti JP, Stanwood W. Rotator cuff tears: why do we repair them? J Bone Joint Surg Am 2004;86A:2764–76. [PubMed]
22. Voloshin I, Gelinas J, Maloney MD, O'Keefe RJ, Bigliani LU, Blaine TA. Proinflammatory cytokines and metalloproteases are expressed in the subacromial bursa in patients with rotator cuff disease. Arthroscopy 2005;21:1076. [PubMed]
23. Ostergaard M, Stoltenberg M, Lovgreen-Nielsen P, Volck B, Jensen CH, Lorenzen I. Magnetic resonance imaging-determined synovial membrane and joint effusion volumes in rheumatoid arthritis and osteoarthritis: comparison with the macroscopic and microscopic appearance of the synovium. Arthritis Rheum 1997;40:1856–67. [PubMed]
24. L'Insalata JC, Warren RF, Cohen SB, Altchek DW, Peterson MG. A self-administered questionnaire for assessment of symptoms and function of the shoulder. J Bone Joint Surg Am 1997;79:738–48. [PubMed]
25. Allen GM, Wilson DJ. Ultrasound of the shoulder. Eur J Ultrasound 2001;14:3–9. [PubMed]
26. Byrt T, Bishop J, Carlin JB. Bias, prevalence and kappa. J Clin Epidemiol 1993;46:423–9. [PubMed]
27. Hirano Y, Sashi R, Izumi J, Itoi E, Watarai J. Comparison of the MR findings on indirect MR arthrography in patients with rotator cuff tears with and without symptoms. Radiat Med 2006;24:23–7. [PubMed]
28. Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am 2006;88:1699–704. [PubMed]
29. Moosmayer S, Tariq R, Stiris MG, Smith HJ. MRI of symptomatic and asymptomatic full-thickness rotator cuff tears. Acta Orthop 2010;81:361–6. [PMC free article] [PubMed]
30. Moosmayer S, Smith HJ, Tariq R, Larmo A. Prevalence and characteristics of asymptomatic tears of the rotator cuff: an ultrasonographic and clinical study. J Bone Joint Surg Br 2009;91:196–200. [PubMed]
31. Reilly P, Macleod I, Macfarlane R, Windley J, Emery RJ. Dead men and radiologists don't lie: a review of cadaveric and radiological studies of rotator cuff tear prevalence. Ann R Coll Surg Engl 2006;88:116–21. [PMC free article] [PubMed]
32. Fleiss J. The design and analysis of clinical experiments. Toronto, ON: Wiley; 1986. pp 1–32.
33. Savnik A, Malmskov H, Thomsen HS, Graff LB, Nielsen H, Danneskiold-Samsoe B, et al. Magnetic resonance imaging of the wrist and finger joints in patients with inflammatory joint diseases. J Rheumatol 2001;28:2193–200. [PubMed]
34. Gaffney K, Cookson J, Blades S, Coumbe A, Blake D. Quantitative assessment of the rheumatoid synovial microvascular bed by gadolinium-DTPA enhanced magnetic resonance imaging. Ann Rheum Dis 1998;57:152–7. [PMC free article] [PubMed]
35. Ostergaard M, Stoltenberg M, Lovgreen-Nielsen P, Volck B, Sonne-Holm S, Lorenzen I. Quantification of synovitis by MRI: correlation between dynamic and static gadolinium-enhanced magnetic resonance imaging and microscopic and macroscopic signs of synovial inflammation. Magn Reson Imaging 1998;16:743–54. [PubMed]
36. Konig H, Sieper J, Wolf KJ. Rheumatoid arthritis: evaluation of hypervascular and fibrous pannus with dynamic MR imaging enhanced with Gd-DTPA. Radiology 1990;176:473–7. [PubMed]
37. Tamai K, Yamato M, Yamaguchi T, Ohno W. Dynamic magnetic resonance imaging for the evaluation of synovitis in patients with rheumatoid arthritis. Arthritis Rheum 1994;37:1151–7. [PubMed]

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