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Shoulder Appearances at MR Imaging in Long-term Dialysis Recipients¹

¹ From the Department of Medical Imaging, Flinders Medical Centre, Bedford Park, South Australia 5042, Australia (J.P.S., M.R.S.); the Renal Unit, Queen Elizabeth Hospital, Woodville, South Australia (P.T.H.C., A.P.S.D.); and the Menzies School of Health Research, Royal Darwin Hospital, Casuarina, Northern Territory, Australia (S.P.M.). Received May 28, 1999; revision requested July 19; final revision received February 25, 2000; accepted March 7. Address correspondence to J.P.S. (e-mail: rajps@flinders.edu.au).

	ABSTRACT

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PURPOSE: To examine shoulder appearances at magnetic resonance (MR) imaging in long-term dialysis recipients.

MATERIALS AND METHODS: Twenty-two chronic dialysis recipients underwent 1.0-T MR imaging with a combination of T1-, T2-, and T2*-weighted sequences. Rotator cuff tendon thickening was graded as present or absent by a musculoskeletal radiologist, who also measured the supraspinatus and subscapularis tendon thicknesses with electronic calipers. The long-axis dimension and location of focal osseous lesions, in addition to their T1, T2, and T2* signal intensities, were noted.

RESULTS: Supraspinatus (n = 9) and subscapularis (n = 10) tendon thickening was frequently observed. Six (27%) of the 22 patients had combined thickening of the supraspinatus and subscapularis tendons without substantial involvement of the infraspinatus or teres minor tendons. These patients had undergone dialysis longer (median, 19.2 years; range, 16.3–22.8 years) than had the other patients (median, 11.7 years; range, 5.8–19.3 years; P = .004). The 29 intraosseous lesions had high, intermediate, and low T2 signal intensity in six (21%), nine (31%), and 14 (48%) instances, respectively.

CONCLUSION: Supraspinatus and/or subscapularis tendon thickening is common in chronic dialysis recipients. Bone lesions in such patients are of variable T2 signal intensity and usually subchondral or adjacent to the greater tuberosity.

Index terms: Amyloidosis, 41.68 • Dialysis • Shoulder, abnormalities, 41.68 • Shoulder, MR, 41.121411, 41.121412, 41.121416 • Tendons, 41.68 • Tendons, MR, 41.121411, 41.121412, 41.121416

	INTRODUCTION

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Dialysis-related arthropathy is a serious complication arising in the context of long-term hemodialysis or continuous ambulatory peritoneal dialysis (1–3). It occurs owing to deposition of ß₂-microglobulin as an amyloid protein. The main clinical manifestations include chronic polyarthropathy associated with pain and stiffness. Large joints such as the shoulders, wrists, hips, and knees and the spine are typical sites of involvement. In such patients, shoulder pain constitutes a common clinical problem (4) and may be exacerbated during or after hemodialysis (2).

Magnetic resonance (MR) appearances of intraosseous amyloid deposits in patients with dialysis-related amyloid arthropathy have been described in studies involving small numbers of patients (5–7). In an early report (8), intraosseous lesions were noted to have low T2 signal intensity, but the results of other studies (5,9) have revealed mixed intraosseous T2 signal intensity. In the shoulder, thickening of the supraspinatus tendon has been observed (5,10,11), but to our knowledge, other components of the rotator cuff have not been explicitly assessed with MR imaging.

This prospective study was undertaken to define the prevalences and signal intensity patterns of intraosseous lesions in 22 long-term dialysis recipients. The components of the rotator cuff also were examined for tendon thickening. Relationships between shoulder pain, rotator cuff tendon thickening, intraosseous lesions, and duration of dialysis were assessed.

	MATERIALS AND METHODS

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Patients
The study population consisted of 22 long-term dialysis recipients (14 men, eight women; median age, 53 years; age range, 28–80 years) who gave informed consent before undergoing imaging. Approval was obtained from the committee on clinical investigation before the onset of the study. The ages of the patients, durations of dialysis, and modes of dialysis treatment are listed in Table 1. The median duration of dialysis was 16.3 years (range, 5.8–22.8 years). All patients were treated predominantly with hemodialysis, and some had had intervening periods of adequate kidney function because of renal transplantation (median duration, 0.17 years; range, 0–5.25 years). Four patients underwent biopsy.

Thickening of each rotator cuff tendon was subjectively graded (J.P.S.) as present or absent. Electronic calipers were used to measure the supraspinatus and subscapularis tendon thicknesses on T1-weighted oblique-coronal images and T2*-weighted transverse images, respectively. The measurements were obtained 1 cm from the point of tendon insertion and perpendicularly to the course of the tendon, with care taken to exclude humeral cartilage. A measurement was not obtained when a full-thickness supraspinatus tear was present, and a measurement of greater than 6 mm was considered to be abnormal (12,13). Motion artifact was present with at least one sequence in six of 22 patients, but it did not substantially affect the sequences (T1-weighted oblique-coronal and T2*-weighted transverse) with which the measurements were obtained.

Statistical Analyses
Statistical analyses were performed by using SPSS, version 9.0 (SPSS, Chicago, Ill) and STATA, version 6 (STATA, College Station, Tex) software. The number of patients in this study was relatively small, and, accordingly, statistical analysis was used largely to determine patterns of association. The Mann-Whitney U test (exact) for nonpaired comparisons was used to assess relationships between the subjective assessment of tendon thickening and (a) duration of dialysis and (b) patient age. The Fisher exact test was used to investigate the association between shoulder pain and subjective tendon thickening. Relationships between measurements of tendon thickness and dialysis duration were assessed by using quantile (median) regression analysis. Logistic regression analysis was used to determine the relationship between supraspinatus tendon thickening (>6 mm) and dialysis duration and patient age. The Kruskal-Wallis test was used to examine the association between dialysis duration and number of intraosseous lesions.

A P value of .05 was considered to indicate statistical significance; however, owing to the large number of statistical tests performed, the levels of statistical significance should be regarded with caution.

	RESULTS

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The 22 MR studies showed appearances ranging from normal—in three patients— to various combinations of tendon thickening and intraosseous lesions. Biopsy of tendon in three patients and of bone in one patient confirmed the presence of amyloid protein. Muscle signal intensity was normal on T1- and T2-weighted images.

Tendon Thickening
The distribution of tendon thickening among the components of the rotator cuff are listed in Table 2. Tendon thickening was absent in all four rotator cuff tendons in seven of 22 patients. The tendon thicknesses measured with calipers are summarized in Table 3.

Subscapularis.—The MR measurements of subscapularis tendon thickness ranged from 3.1 to 10.8 mm, with a median of 6.2 mm. The results of quantile (median) regression analysis suggested an association between measurements of subscapularis tendon thickness and dialysis duration (r² = 0.3; P = .005). Ten (45%) of the 22 patients had subjective thickening of the subscapularis tendon. These 10 patients had undergone dialysis longer (median, 18.5 years; range, 9.0–22.8 years) than had the rest of the study population (median, 11.7 years; range, 5.8–18.7 years; Mann-Whitney U test, P = .013). No difference in patient age between the two groups was detected (Mann-Whitney U test, P = .18). Subscapularis tendon thickening was not found to be more common in the patients with shoulder pain (Fisher exact test, P = .38).

Combined tendon thickening.—Combined thickening of the supraspinatus and subscapularis tendons was noted in six (27%) of 22 patients. In such cases, the tendon signal intensity was predominantly low to intermediate on T1-weighted images and low on T2- and T2*-weighted images (Fig 1). These six patients had undergone dialysis longer (median, 19.2 years; range, 16.3–22.8 years) than had the other patients (median, 11.7 years; range, 5.8–19.3 years; Mann-Whitney U test, P = .004). The age of these patients was not different from that of the other patients in this study (Mann-Whitney U test, P = .39). These patients had no thickening of the teres minor tendon, and infraspinatus tendon thickening was present in only two cases. This unusual pattern was one of enlargement of the supraspinatus and subscapularis tendons, with sparing of the infraspinatus and teres minor tendons.

View larger version (156K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. MR images of the shoulder in a 46-year-old man with biopsy-proved amyloid protein deposition and chronic shoulder pain. T2*-weighted MR images (not shown) revealed subscapularis tendon thickening. (a) Oblique-coronal T1-weighted turbo spin-echo image (900/12) shows thickening of the supraspinatus tendon (curved arrows) and of the adjacent subdeltoid bursa (arrowheads). There is also a lobulated subchondral bone lesion (straight arrow) exhibiting slight T1 hyperintensity. (b) Corresponding oblique-coronal T2-weighted turbo spin-echo image (3,000/119) shows that the bone lesion (arrowhead) has heterogeneous but predominantly high signal intensity. Thickening of the supraspinatus tendon (arrows) also is seen.

View larger version (176K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. MR images of the shoulder in a 46-year-old man with biopsy-proved amyloid protein deposition and chronic shoulder pain. T2*-weighted MR images (not shown) revealed subscapularis tendon thickening. (a) Oblique-coronal T1-weighted turbo spin-echo image (900/12) shows thickening of the supraspinatus tendon (curved arrows) and of the adjacent subdeltoid bursa (arrowheads). There is also a lobulated subchondral bone lesion (straight arrow) exhibiting slight T1 hyperintensity. (b) Corresponding oblique-coronal T2-weighted turbo spin-echo image (3,000/119) shows that the bone lesion (arrowhead) has heterogeneous but predominantly high signal intensity. Thickening of the supraspinatus tendon (arrows) also is seen.

View larger version (171K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Oblique-coronal T2-weighted turbo spin-echo image (3,000/119) obtained in a 46-year-old man, a chronic dialysis recipient with chronic shoulder pain and biopsy-proved amyloid protein deposition, shows nodular debris (black arrowheads) within a large subdeltoid bursal effusion (E). The anterior humeral bone lesion (white arrowhead) is of low signal intensity.

Bursal Effusions
Subacromial-subdeltoid bursal effusions were present in three instances; two of these effusions contained nodular debris (Fig 2). Subacromial-subdeltoid bursal thickening was present in six patients. Focal hyperintensity within the distal supraspinatus tendon, consistent with a partial tear, was present in six patients, and a full-thickness tear was noted in two. MR imaging depicted joint effusions in eight patients. The MR appearances of subcutaneous fat were normal.

	DISCUSSION

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Although supraspinatus tendon thickening has been documented in studies with chronic hemodialysis recipients (5,10,11), to our knowledge, the other rotator cuff tendons have not been assessed. In the study of Bernageau et al (11), 20 of the 22 patients examined with MR imaging had abnormally thickened supraspinatus tendons, as defined by a measurement of 6 mm taken at the thickest portion of the supraspinatus tendon (mean, 8.1 mm). The median value of 5.8 mm and mean value of 6.0 mm obtained in this study probably reflect our measurement at a different point—1 cm from the supraspinatus tendon insertion. The rotator cuff has also been assessed with ultrasonography (US) in chronic hemodialysis recipients (10), and supraspinatus tendon thickening was similar (mean, 7 mm; range, 3–10 mm). There is, therefore, reasonable agreement between the results of previous studies and those of the current study with regard to supraspinatus tendon thickening in chronic hemodialysis recipients.

Reference is made to the literature to define a criterion for the presence of supraspinatus tendon thickening during statistical analysis. Mirowitz (12) used MR imaging to examine 15 volunteers with no history of shoulder injury or pain. The measurements at the supraspinatus tendon insertion ranged from 2.0 to 4.0 mm (mean, 3.2 mm). Bretzke et al (13) obtained measurements 2 cm from the supraspinatus tendon insertion with a 10-MHz US transducer in a mixed population (ie, 15 asymptomatic subjects and 48 patients) and found a mean thickness (± SD) of 6.0 mm (± 1.1). The measurements in our study were taken at an intermediate point 1 cm from the tendon insertion, and 6-mm thickness was the criterion used to determine the presence of supraspinatus tendon thickening.

In previous studies, little if any attention has been directed toward other components of the rotator cuff, and relative sparing of the infraspinatus and teres minor tendons has not been reported. Subscapularis tendon thickening was noted in 45% (10 of 22 patients) of our study patients, but transverse T2*-weighted images were used for assessment and susceptibility effects may have resulted in generous tendon thickness measurements. When thickening was present, the subscapularis tendon, adjacent joint capsule, and subscapularis bursa were difficult to distinguish. Thus, the subscapularis tendon thickening described and measured in this article may have included a small component of capsular or bursal thickening, but capsular thickening was not apparent elsewhere.

Subjective grading and measurement of tendon thickness revealed an association between increased dialysis duration and supraspinatus and/or subscapularis tendon thickening. Although there are other causes of tendon thickening, it seems likely that tendon thickening, in the context of long-term dialysis, represents infiltration with AA amyloid protein. This contention is supported by the correlation between dialysis duration and tendon thickening and the demonstration of tendon thickening in other studies (5,10,11) with hemodialysis recipients. Although in the current study, the infiltration was confirmed to represent ß₂-related amyloid deposition in three patients who underwent tendon biopsy and in one additional patient who underwent bone biopsy, an important limitation of this study was the lack of pathologic confirmation in the majority of cases.

The reason for the predilection of ß₂-microglobulin for the supraspinatus and subscapularis tendons cannot be readily explained. Because the supraspinatus and subscapularis tendons are potential sites of low-grade trauma due to contact with components of the coracoacromial arch, it is possible that impingement in this region induces inflammation and a subsequent increase in deposition of amyloid proteins. The fact that the infraspinatus and teres minor tendons usually are not subject to impingement may explain the infrequency of tendon thickening in these regions in our study. This concept, however, was not supported by the findings in an experimental model of dialysis arthropathy in which human ß₂-microglobulin was deposited equally in normal and diseased joints (14). The alternative—and in our opinion less favored—argument is that tendon thickening due to amyloid protein deposition induces impingement and thus much of the pain observed in these patients. At present, it remains uncertain whether amyloid infiltration represents a primary phenomenon or is potentiated by impingement.

Escobedo et al (5) examined the shoulders and hips of nine dialysis recipients who underwent MR imaging and found that 10 of 28 osseous lesions had high T2 signal intensity, similar to joint fluid. Others (6,8) have reported focal hyperintensity within intraosseous lesions, but in these studies, the emphasis was on the predominantly low to intermediate T2 signal intensity of such amyloid deposits. The T2 signal intensity of intraosseous bone lesions was variable in this study: High and low T2 signal intensity was noted in six (21%) and 14 (48%) of 29 lesions, respectively. These findings support previous suggestions (5) regarding the variable composition of such intraosseous lesions. The MR appearances of these osseous lesions are nonspecific, but given that the three patients with glenohumeral degenerative change in the current study accounted for a total of three intraosseous lesions (two with high T2 signal intensity), it seems unlikely that more than a small proportion of lesions represent degenerative subchondral cysts.

Cardinal et al (10) performed 19 shoulder US studies in 11 chronic hemodialysis recipients and found periarticular nodules within the subacromial-subdeltoid bursa in four patients. In two cases, we observed an equivalent MR appearance. At US and MR imaging, these nodules are consistent with periarticular amyloid deposits, a well-recognized phenomenon in chronic hemodialysis recipients.

With increasing entry of patients into long-term dialysis programs and constant renal transplantation rates (15), many patients on dialysis are surviving for long periods and thus susceptible to the long-term complications of dialysis treatment. It has been suggested that the use of cuprophan dialysis membranes increases the risk of dialysis-related arthropathy (16,17), but it remains to be seen whether strategies directed toward improved removal of advanced glycation end products will reduce the prevalence of dialysis-related arthropathy in long-term dialysis recipients. In the meantime, it seems likely that shoulder pain and the consequences of dialysis-related arthropathy will remain a clinical problem for patients and their physicians.

In summary, we examined the shoulder appearances at MR imaging in 22 long-term dialysis recipients. Thickening of the supraspinatus and subscapularis tendons was common, and the signal intensities of osseous lesions were variable, with the majority being low or intermediate T2 signal intensity. In addition, an unusual pattern of tendon thickening was detected in a subgroup of six (27%) patients. In this subgroup, both the supraspinatus and subscapularis tendons were predominantly involved, with relative sparing of the teres minor and infraspinatus tendons.

	ACKNOWLEDGMENTS

 
The authors thank Gerald Fon, MBBS, FRACR, for manuscript review and Adrian Esterman for advice and assistance with statistical analysis.

	FOOTNOTES

 
Author contributions: Guarantors of integrity of entire study, J.P.S., P.T.H.C.; study concepts and design, J.P.S., P.T.H.C., A.P.S.D.; definition of intellectual content, J.P.S., P.T.H.C., A.P.S.D.; literature research, J.P.S., P.T.H.C., S.P.M.; clinical studies, P.T.H.C., S.P.M.; data acquisition, J.P.S., P.T.H.C., S.P.M.; data analysis, J.P.S., P.T.H.C.; statistical analysis, J.P.S., P.T.H.C., S.P.M.; manuscript preparation and editing, J.P.S.; manuscript review, all authors.

	REFERENCES

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