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Fatty Atrophy of Supraspinatus and Infraspinatus Muscles: Accuracy of US¹

¹ From the Departments of Radiology (K.S., J.H., C.W.A.P., M.Z.) and Orthopedic Surgery (D.C.M., C.P.), Orthopedic University Hospital, Balgrist, Zurich, Switzerland. Received October 11, 2004; revision requested December 21; revision received January 24, 2005; accepted February 23. Address correspondence to K.S., Department of Nuclear Medicine, University Hospital Zurich, Rämistrasse 100, CH-8091 Zurich, Switzerland (e-mail: klaus.strobel{at}usz.ch).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To prospectively evaluate the accuracy of ultrasonography (US) in depicting fatty atrophy of the supraspinatus (SSP) and infraspinatus (ISP) muscles, with magnetic resonance (MR) imaging as the reference standard.

MATERIALS AND METHODS: Institutional review board approval and informed consent were obtained. SSP and ISP muscles of 65 consecutive patients (27 women, 38 men; mean age, 53.1 years; range, 28–83 years) with possible rotator cuff tears were evaluated with US in two planes. Visibility of muscle contour, pennate pattern, the central tendon, and muscle echogenicity was assessed by two radiologists. On the basis of these findings, diagnosis of substantial fatty atrophy was made at US. Accuracy, sensitivity, specificity, proportion of over- and underestimations, and interobserver agreement in diagnosis of substantial (grade 2 or greater) muscle atrophy were determined. Fatty atrophy was graded at MR imaging as follows: score of 0 = no intramuscular fat, score of 1 = some fatty streaks, score of 2 = fat evident but less extensive than muscle, score of 3 = fat equal to muscle, and score of 4 = fat more extensive than muscle.

RESULTS: For readers 1 and 2, the accuracy of US in depicting fatty atrophy of SSP muscle was 75% (49 of 65) and 72% (47 of 65), sensitivity was 89% (eight of nine) and 100% (nine of nine), and specificity was 73% (41 of 56) and 68% (38 of 56), respectively. For readers 1 and 2, the accuracy of US in depicting fatty atrophy of ISP muscle was 85% (55 of 65) and 80% (52 of 65), sensitivity was 58% (11 of 19) and 63% (12 of 19), and specificity was 96% (44 of 46) and 87% (40 of 46), respectively. Overestimation of SSP muscle atrophy was more common (23% [15 of 65] for reader 1 and 28% [18 of 65] for reader 2) than underestimation (2% [one of 65] for reader 1 and 0% [0 of 65] for reader 2). For readers 1 and 2, overestimation of ISP muscle atrophy was 3% (two of 65) and 9% (six of 65) and underestimation was 12% (eight of 65) and 9% (seven of 65), respectively. Interobserver agreement was moderate for SSP ( = 0.55) and substantial for ISP ( = 0.71) muscles.

CONCLUSION: US is moderately accurate in the diagnosis of substantial fatty atrophy of the SSP or ISP muscle.

© RSNA, 2005

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Fatty atrophy of the rotator cuff muscles associated with tendon tears is an important prognostic factor for the anatomic and functional results after surgical repair of the cuff (1,2). Rotator cuff repair should be performed before substantial fatty atrophy of the muscle appears, because cuff repair does not result in reversal of fatty atrophy, and function of the shoulder joint remains impaired (3,4). Classification of fatty muscle atrophy is commonly performed at computed tomography (CT) (5). Magnetic resonance (MR) imaging, especially with the use of oblique sagittal sequences, is also appropriate for the assessment of the grade of fatty atrophy (6,7).

Although MR imaging is considered by many authors as the standard of reference in the evaluation of shoulder joint derangements, ultrasonography (US) is also accurate in the diagnosis of rotator cuff tears in the hands of experienced investigators (8,9). To our knowledge, the favorable results of US in rotator cuff abnormalities have only related to tendon abnormalities. Studies in which muscle quality was addressed are rare (10).

The purpose of the study was to prospectively evaluate the accuracy of US in depicting fatty atrophy of the supraspinatus and infraspinatus muscles, with MR imaging as the reference standard.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
Sixty-five consecutive patients (mean age, 53.1 years; range, 28–83 years) clinically suspected of having rotator cuff tendon lesions referred to our institution for MR arthrography of the shoulder were included in this prospective study. There were 27 women (mean age, 51.4 years; range, 28–73 years) and 38 men (mean age, 54.5 years; range, 29–83 years). Age distribution was not significantly different between women and men (P > .05, Student t test). The study was approved by the institutional review board, and informed consent was obtained from all patients.

US Examination
US examinations were performed immediately before or after MR arthrography by one of two musculoskeletal (K.S., M.Z.) radiologists with 2 and 10 years of experience in shoulder US. A multifrequency linear probe (7.5–9.0 MHz, Elegra; Siemens Medical Solutions, Erlangen, Germany) was used. The patient sat on a chair, with the examiner standing behind the patient. The US examination was standardized according to a previously published technique (11). Tissue harmonic imaging was used for all patients. The muscle belly of the supraspinatus and infraspinatus muscles was evaluated while the patient was asked to place his or her hand on the anterior ipsilateral thigh for the examination. Each muscle belly was evaluated in two planes. The first plane was perpendicular to the long axis of the muscle belly. The images were acquired at the thickest part of the belly (Fig 1a). The second plane was parallel to the central tendon of the muscle, perpendicular to the first imaging plane (Fig 1b). The images were saved on a picture archiving and communication system (Image Devices, Idstein, Germany) for further review.

View larger version (123K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Investigation of the supraspinatus muscle belly. (a) The transducer is perpendicular to the long axis of the muscle belly and is positioned at the thickest part of the belly. This plane corresponds to the oblique coronal MR image plane. (b) Second plane obtained parallel to the central tendon of the muscle belly, perpendicular to the first plane. This plane corresponds to the oblique sagittal MR image plane.

View larger version (127K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Investigation of the supraspinatus muscle belly. (a) The transducer is perpendicular to the long axis of the muscle belly and is positioned at the thickest part of the belly. This plane corresponds to the oblique coronal MR image plane. (b) Second plane obtained parallel to the central tendon of the muscle belly, perpendicular to the first plane. This plane corresponds to the oblique sagittal MR image plane.

The imaging protocol for the 1.0-T imager included oblique coronal intermediate- and T2-weighted turbo spin-echo images (3500/16–98, 3-mm section thickness, 16-cm field of view, and 256 x 256 matrix), oblique coronal T1-weighted fat-saturated turbo spin-echo images (800/20, 4-mm section thickness, 16-cm field of view, and 256 x 256 matrix), oblique sagittal T1-weighted turbo spin-echo images (700/12, 5-mm section thickness, 16-cm field of view, and 256 x 256 matrix), and transverse T1-weighted spin-echo images (580/20, 4-mm section thickness, 16-cm field of view, and 512 x 512 matrix). The images were saved on the picture archiving and communication system for further review.

Analysis of MR Images
The MR images were evaluated in consensus by two radiologists (C.W.A.P., J.H.) with 6 and 14 years of experience in musculoskeletal radiology. The MR images were not evaluated by the same radiologist who had performed the US examination. The supraspinatus and infraspinatus tendons were classified as normal, partial tear, or complete tear by using established criteria (12,13). The size of the tear was measured in two planes. The grade of fatty atrophy of the supraspinatus and infraspinatus muscle belly was assessed according to the Goutallier et al (5) classification as follows: score of 0 = no intramuscular fat, score of 1 = some fatty streaks, score of 2 = fat less extensive than muscle, score of 3 = fat equal to muscle, and score of 4 = fat more extensive than muscle. The original description of grading was based on findings on CT images; however, it can also be used with MR images (6,7). Oblique sagittal images were used for the assessment of fatty atrophy. On the basis of Goutallier et al results, grade 2 or higher atrophy was defined as substantial (1). The results were used as the standard of reference for the evaluation of US images.

Review of US Images
After data acquisition, all US images were independently reviewed by two musculoskeletal radiologists (K.S., M.Z.). A picture archiving and communication system workstation (Report 5.2; Image Devices) was used for this purpose. To blind the reviewers, patient data and imaging parameters were masked. In addition, there was an interval of 2–12 weeks between data acquisition and the evaluation of images. The readers knew that a rotator cuff tear was suspected in the study patients but were otherwise blinded to clinical data. For the evaluation of fatty atrophy, the visibility of muscle contours, pennate pattern (architecture of the muscle fibers in relationship to the central tendon), and central tendon was graded by using a three-point scale (grade 0 = clearly visible muscle contours, fibers, and central tendon; grade 1 = partially visible structures; and grade 2 = structures no longer visible). Furthermore, echogenicity was graded in comparison to the echogenicity of the deltoid muscle (grade 0 = iso- or hypoechoic in comparison to the deltoid muscle, grade 1 = slightly more echoic than the deltoid muscle, and grade 2 = markedly more echoic than the deltoid muscle). The diagnosis of substantial fatty atrophy was made when the most severe abnormality (grade 2) was found on the basis of at least one of the evaluated US criteria.

Statistical Analysis
MR grades 2–4 were defined as substantial muscle atrophy. Sensitivity, specificity, and accuracy for the US diagnosis of fatty atrophy were calculated for both readers. The proportions of overestimated and underestimated diagnoses were calculated. The Mann-Whitney U test was used to analyze differences between US grades in normal and atrophied muscles. P < .05 was considered to indicate a significant difference. Interobserver agreement was described by using statistics. StatView (version, 4.0; SAS Institute, Cary, NC) and SPSS (version, 10.0.7; SPSS, Chicago, Ill) software were used for statistical analysis.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
MR Imaging
Of 65 patients, 12 had a normal supraspinatus tendon, 12 had partial-thickness tears, and 41 had full-thickness tears. Forty-one patients had normal infraspinatus tendons, 14 had partial-thickness tears, and 10 a full-thickness tear. The mean transverse diameter of the full-thickness cuff tears was 34 mm (range, 6–64 mm), and the mean anteroposterior diameter was 39 mm (range, 6–80 mm).

Twenty-five supraspinatus muscles were classified as grade 0 (Fig 2 ); 31, as grade 1; three, as grade 2 (Fig 3); five, as grade 3; and 1, as grade 4. Twenty-six infraspinatus muscles were classified as grade 0; 20, as grade 1; 10, as grade 2; five, as grade 3; and four, as grade 4 (Fig 4).

View larger version (156K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Oblique (a) sagittal and (b) coronal US images of normal supraspinatus muscle belly. Outer contours (arrowheads) of the muscle are clearly visible. Central tendon (long arrows) and pennate pattern (short arrows) are clearly visible. There is normal echogenicity. (c) Corresponding oblique sagittal T1-weighted MR image (600/12). There are no fatty streaks in the muscle substance. Arrowheads = outer contour, arrow = hypointense central tendon.

View larger version (156K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Oblique (a) sagittal and (b) coronal US images of normal supraspinatus muscle belly. Outer contours (arrowheads) of the muscle are clearly visible. Central tendon (long arrows) and pennate pattern (short arrows) are clearly visible. There is normal echogenicity. (c) Corresponding oblique sagittal T1-weighted MR image (600/12). There are no fatty streaks in the muscle substance. Arrowheads = outer contour, arrow = hypointense central tendon.

View larger version (109K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Oblique (a) sagittal and (b) coronal US images of normal supraspinatus muscle belly. Outer contours (arrowheads) of the muscle are clearly visible. Central tendon (long arrows) and pennate pattern (short arrows) are clearly visible. There is normal echogenicity. (c) Corresponding oblique sagittal T1-weighted MR image (600/12). There are no fatty streaks in the muscle substance. Arrowheads = outer contour, arrow = hypointense central tendon.

View larger version (179K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Oblique (a) sagittal and (b) coronal US images of atrophic supraspinatus muscle (grade 2) show increased echogenicity of the muscle substance (long arrows in a). Contours of the muscle belly are only partially visible (arrowheads). Central tendon (long arrows in b) is not visible on a. Pennate pattern (short arrows) is partially visible. (c) Corresponding oblique sagittal T1-weighted MR image (600/12) shows a decreased bulk of supraspinatus muscle belly. There are many areas of fatty tissue (arrowheads) between muscle fibers and a hypointense central tendon (arrows).

View larger version (182K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Oblique (a) sagittal and (b) coronal US images of atrophic supraspinatus muscle (grade 2) show increased echogenicity of the muscle substance (long arrows in a). Contours of the muscle belly are only partially visible (arrowheads). Central tendon (long arrows in b) is not visible on a. Pennate pattern (short arrows) is partially visible. (c) Corresponding oblique sagittal T1-weighted MR image (600/12) shows a decreased bulk of supraspinatus muscle belly. There are many areas of fatty tissue (arrowheads) between muscle fibers and a hypointense central tendon (arrows).

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 3c. Oblique (a) sagittal and (b) coronal US images of atrophic supraspinatus muscle (grade 2) show increased echogenicity of the muscle substance (long arrows in a). Contours of the muscle belly are only partially visible (arrowheads). Central tendon (long arrows in b) is not visible on a. Pennate pattern (short arrows) is partially visible. (c) Corresponding oblique sagittal T1-weighted MR image (600/12) shows a decreased bulk of supraspinatus muscle belly. There are many areas of fatty tissue (arrowheads) between muscle fibers and a hypointense central tendon (arrows).

View larger version (153K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. (a) Oblique sagittal US image of the infraspinatus muscle belly (image has been rotated to be in the same plane as b) shows normal echogenicity of the cranial one-third of the muscle (arrowheads). There is increased echogenicity of the caudal two-thirds of the muscle (short arrows). Muscle contour is partially visible (long arrows). (b) Corresponding oblique sagittal MR image (600/12) shows normal signal intensity (arrowheads) of the cranial part of the infraspinatus muscle. Caudal part (arrows) is completely replaced by fatty tissue (grade 4). Image quality is decreased because of motion artifacts.

View larger version (120K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. (a) Oblique sagittal US image of the infraspinatus muscle belly (image has been rotated to be in the same plane as b) shows normal echogenicity of the cranial one-third of the muscle (arrowheads). There is increased echogenicity of the caudal two-thirds of the muscle (short arrows). Muscle contour is partially visible (long arrows). (b) Corresponding oblique sagittal MR image (600/12) shows normal signal intensity (arrowheads) of the cranial part of the infraspinatus muscle. Caudal part (arrows) is completely replaced by fatty tissue (grade 4). Image quality is decreased because of motion artifacts.

US Examination
The visibility of the outer contour of the supraspinatus and infraspinatus muscles was significantly inferior in muscles with fatty atrophy (for readers 1 and 2, mean grades of supraspinatus were 1.2 and 1.1 and those of infraspinatus were 0.6 and 0.7, respectively) than in normal muscles (for readers 1 and 2, mean grades of supraspinatus were 0.4 and 0.6 and those of infraspinatus were 0.1 and 0.2, respectively) (Table 1). Fatty muscle atrophy was associated with significant loss of visibility of the central tendon (for readers 1 and 2 mean grades of supraspinatus muscle atrophy were 1.6 and 1.8, those of infraspinatus muscle atrophy were 0.4 and 0.8, those of normal supraspinatus muscle were 0.5 and 0.4, and those of normal infraspinatus muscle were 0.1 and 0.2, respectively). Visibility of the pennate pattern was also associated with muscle fatty atrophy (mean grades of supraspinatus, 1.7 [reader 1] and 1.4 [reader 2]; mean grades of infraspinatus, 0.6 [reader 1] and 0.8 [reader 2]; mean grades of normal supraspinatus muscle, 0.5 [reader 1] and 0.6 [reader 2]; and mean grades of normal infraspinatus muscle, 0.1 [reader 1] and 0.3 [reader 2]). Echogenicity of the muscle tissue was markedly higher in muscles with fatty atrophy (supraspinatus, 1.8 [reader 1] and 1.7 [reader 2]; infraspinatus, 0.6 [reader 1] and 1.1 [reader 2]) than in normal muscles (supraspinatus, 0.5 [reader 1] and 0.6 [reader 2]; infraspinatus, 0.1 [reader 1] and 0.3 [reader 2]).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

To our knowledge, authors of only one recently published retrospective study (10) have assessed US with regard to muscle quality by reviewing a large number of US images for the presence of fatty atrophy of the rotator cuff and by relating fatty atrophy to the presence of US-diagnosed tears.

Our study demonstrates that US is able to depict substantial fatty atrophy of the rotator cuff muscles. This diagnosis is not as straightforward as that with use of MR and CT images. However, with the use of the findings described in this article, including the loss of visibility of the central tendon and the typical muscle pennate pattern, a reliable diagnosis of muscle atrophy is possible.

Sofka et al (10) used increased muscle echogenicity and decreased muscle bulk as indicators for the presence of muscle atrophy. A limitation of their study was the lack of a standard of reference, such as CT or MR imaging.

Generally, increased echogenicity of muscle tissue is an unspecific finding with many possible causes, such as trauma, subacute denervation, or myositis. Previously published study findings have shown that fat replacement is the main cause of increased echogenicity of skeletal muscles (18). Muscle lipomatosis has a much greater influence on muscular echogenicity than does muscle fibrosis (19). Skeletal muscles show a typical pennate pattern. We have investigated the visibility of the pennate pattern in normal and fatty atrophied muscles. The visibility of the pennate pattern is markedly decreased in muscles with fatty atrophy.

US can be used to measure the angles of the pennate pattern (20). Recent experimental studies show that the angle of the pennate pattern increases with increasing fatty atrophy (21). In our experience, US measurement of the angles of the pennate pattern in the rotator cuff muscles is difficult because the pennate pattern is hardly visible in atrophic muscles.

The patients in Sofka et al study (10) and those in our study more commonly had atrophic infraspinatus muscles (25 of 193 in the Sofka et al study; 19 of 65 in our study) than supraspinatus muscles (13 of 193 in the Sofka et al study; nine of 65 in our study). Why atrophy of the infraspinatus muscle can occur with anterior cuff tears while the infraspinatus tendon is intact remains unclear. One explanation may be a compromise of the suprascapular nerve due to the altered biomechanics of the joint (22). Because the subscapularis muscle belly is in part hidden between the thoracic wall and the scapula, this structure is difficult to completely assess with US. Sofka et al diagnosed subscapularis muscle atrophy with US in two patients, but they did not describe their examination technique. There are other new imaging methods to measure the degree of fatty atrophy quantitatively, including MR spectroscopy (23,24). Kostler et al (24) used two-dimensional spectroscopic fast low-angle shot sequences to determine the fat-to-water ratio in a phantom study.

There were some limitations in our study. The accuracy of US evaluations that are based on a selection of static images may be inferior compared with the accuracy in clinical routine, where US examinations are performed dynamically. Further, the relatively small proportion of patients with severe fatty atrophy may have reduced the diagnostic accuracy of US.

In conclusion, US is moderately accurate in the diagnosis of substantial fatty atrophy of the supraspinatus or infraspinatus muscle. Although MR imaging remains the standard of reference for assessment of fatty atrophy of the rotator cuff muscles, the evaluation of supraspinatus and infraspinatus muscle belly should be included when shoulder US is performed in patients suspected of having rotator cuff tears.

	FOOTNOTES

 
Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, K.S., M.Z.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, K.S., J.H., D.C.M., C.W.A.P., M.Z.; clinical studies, K.S., J.H., M.Z.; statistical analysis, K.S., J.H.; and manuscript editing, all authors

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2372041612v1 237/2/584    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Strobel, K. Articles by Zanetti, M. Search for Related Content PubMed PubMed Citation Articles by Strobel, K. Articles by Zanetti, M.