Orthopedics

Feature Article Free

Fatty Degeneration of the Rotator Cuff Reflects Shoulder Strength Deficits in Patients With Rotator Cuff Tears

Jong Pil Yoon, MD; Jae Wook Jung, MD; Chang Hwa Lee, MD; Young Gun Kim, MD; Seok Won Chung, MD; Joon Yub Kim, MD; Hyun Joo Lee, MD; Jee Wook Yoon, MD; Hoseok Lee, MD

Abstract

Fatty degeneration is an important clinical factor in patients with rotator cuff tears. Goutallier grade, occupation ratio, and tangent sign help identify fatty degeneration; however, little is known about how closely these measurement techniques correlate with actual muscle strength deficits. The authors evaluated each method's ability to determine the correlation between fatty degeneration and muscle strength deficits. The authors included 203 patients who underwent full-thickness rotator cuff repair (mean age, 61.29±7.92 years). All patients were evaluated with preoperative magnetic resonance imaging to identify fatty degeneration and with an isokinetic test to determine actual shoulder strength. Fatty degeneration was evaluated using Goutallier grade, occupation ratio, and tangent sign. The actual shoulder strength deficit was evaluated by abduction, whereas external and internal rotation were tested using the isokinetic test. More severe fatty degeneration was correlated with lower degrees of abduction, external rotation, and internal rotation. The occupation ratio was more closely correlated with actual muscle strength deficits. However, in patients with massive tears, the correlation between fatty degeneration and muscle strength was less pronounced. Tangent sign (+) findings had a significantly lower strength of external rotation and abduction. The fatty degeneration of the rotator cuff muscle measured by each method was correlated with actual shoulder strength deficits in patients with rotator cuff tears. However, the correlations were less clear in patients with massive rotator cuff tears. Therefore, in cases of massive rotator cuff tears, fatty degeneration was correlated with muscle strength deficits but was not directly proportional to their extent. [Orthopedics. 201x; xx(x):xx–xx.]

Abstract

Fatty degeneration is an important clinical factor in patients with rotator cuff tears. Goutallier grade, occupation ratio, and tangent sign help identify fatty degeneration; however, little is known about how closely these measurement techniques correlate with actual muscle strength deficits. The authors evaluated each method's ability to determine the correlation between fatty degeneration and muscle strength deficits. The authors included 203 patients who underwent full-thickness rotator cuff repair (mean age, 61.29±7.92 years). All patients were evaluated with preoperative magnetic resonance imaging to identify fatty degeneration and with an isokinetic test to determine actual shoulder strength. Fatty degeneration was evaluated using Goutallier grade, occupation ratio, and tangent sign. The actual shoulder strength deficit was evaluated by abduction, whereas external and internal rotation were tested using the isokinetic test. More severe fatty degeneration was correlated with lower degrees of abduction, external rotation, and internal rotation. The occupation ratio was more closely correlated with actual muscle strength deficits. However, in patients with massive tears, the correlation between fatty degeneration and muscle strength was less pronounced. Tangent sign (+) findings had a significantly lower strength of external rotation and abduction. The fatty degeneration of the rotator cuff muscle measured by each method was correlated with actual shoulder strength deficits in patients with rotator cuff tears. However, the correlations were less clear in patients with massive rotator cuff tears. Therefore, in cases of massive rotator cuff tears, fatty degeneration was correlated with muscle strength deficits but was not directly proportional to their extent. [Orthopedics. 201x; xx(x):xx–xx.]

After a rotator cuff tear develops, muscle fiber atrophy, fibrosis, and fat accumulation within the muscle usually occur.1,2 This change, often termed fatty degeneration, is frequently exacerbated in elderly patients with rotator cuff tears.3

Muscle atrophy and fatty degeneration have great influence on several clinical parameters, such as overall outcome and strength, and can predict rotator cuff repair results.4 The amount of initial atrophy and severity of fatty degeneration in the rotator cuff muscles are among the most important factors determining clinical results and anatomic cuff integrity.4,5 Therefore, evaluating the degree of fatty degeneration in the rotator cuff muscles is important in planning treatment strategies and may be useful for predicting postoperative outcomes.

Several authors have proposed various methods for measuring muscle atrophy and fatty degeneration of the rotator cuff muscles based on imaging techniques such as computed tomography (CT) and magnetic resonance imaging (MRI).6–9 The first such method, the semiquantitative grading system for muscle atrophy and fatty degeneration developed by Goutallier et al,2 is widely used. Fatty degeneration measurements were originally estimated on axial CT images, but MRI eventually became the gold standard for evaluating rotator cuff diseases.9,10 The second method, the occupational ratio, involves calculating areas by using medical image software; for example, occupational ratio of the supraspinatus (SSP) muscle=area of the SSP muscle/(area of SSP fatty degeneration+area of SSP muscle).11,12 The third method, the tangent sign, evaluates the degree of muscular atrophy of the SSP tendon by detecting whether it fails to cross a line from the superior border of the coracoid process to the superior border of the scapular spine.13

Some studies have demonstrated that the findings of these systems were correlated with rotator cuff tear severity.13–15 However, few studies have examined whether fatty degeneration detected by these techniques reflects actual shoulder muscle strength. Therefore, this study aimed to evaluate whether fatty degeneration severity detected by Goutallier grade, occupational ratio, and tangent sign on MRI is correlated with actual shoulder strength measured by an isokinetic instrument. The hypotheses of this study are as follows: (1) each grading system of fatty degeneration is specifically correlated with shoulder strength deficits, and (2) the correlation between fatty degeneration and shoulder strength deficit degree varies according to tear severity.

Materials and Methods

Patient Enrollment

Institutional review board approval was obtained for the study protocol, and informed consent was obtained from all participants. Between April 2011 and September 2015, four hundred three consecutive patients with full-thickness rotator cuff tears were surgically treated at the authors' institutions. The presence of a rotator cuff tear was confirmed by preoperative MRIs and arthroscopic findings. Patients were considered surgical candidates if they had persistent shoulder pain unresponsive to at least 6 months of adequate nonoperative treatment, such as anti-inflammatory medication, physical therapy, subacromial cortisone injection, and activity modification. All patients were evaluated with preoperative MRIs for fatty degeneration and an isokinetic test for actual shoulder strength.

The authors excluded patients with (1) shoulder stiffness for forward elevation at less than 120° passively, external rotation with the arm at the side at less than 30° passively, and internal rotation at the back lower than L3 passively as described in a previous study16 (n=108); (2) difficulty due to pain during the isokinetic test (n=31); (3) symptomatic lesions in the contralateral shoulder (n=48); (4) cuff tear arthropathy (n=9); or (5) a history of previous shoulder surgery (n=4). Finally, 203 patients (104 men, 158 women; mean age, 61.29±7.92 years) were enrolled. Each tear was measured intraoperatively in the anteroposterior direction at the lateral edge of the footprint using a calibrated probe after debridement of the degenerated tendon edges and categorized as follows: small (<1 cm) (n=8), medium (>1 to <3 cm) (n=82), large (>3 to <5 cm) (n=67), and massive (>5 cm) (n=46).

Clinical Variables

All of the clinical data were prospectively collected in the authors' database and were retrospectively reviewed. All data were collected by a clinical researcher who was blinded to the study design. Patients' demographic and other characteristics, including age, sex, hand dominance, symptom duration and aggravation, smoking, underlying disease (diabetes mellitus, hypertension, hypercholesterolemia, and hyperthyroidism), smoking history, number of past steroid injections, and traumatic events, were recorded. Sports activity level was defined as high (extreme or contact sports), medium (static sports), or low (mild or no sports activities).17 Work level was defined as high, medium, or low if the work involved heavy manual labor, manual labor with less physical activity, or sedentary physical activity, respectively.17

Radiologic Findings

All MRIs were acquired digitally using a 3-T Signa HDxt MRI scanner/Discovery MR750w system (General Electric, Milwaukee, Wisconsin). Fat-suppressed T1-weighted turbo spin-echo sequences were collected in the axial and coronal oblique planes parallel to the long axis of the SSP tendon and in the sagittal oblique plane. In addition, T1-weighted, T1-weighted contrast-enhanced, T2-weighted coronal, and T1-weighted sagittal images were obtained. The slice thickness was 3 mm in all of the images.

Fatty degeneration was evaluated using Goutallier grade, occupation ratio, and tangent sign. First, Goutallier grade was modified to a simple grading system with T1-weighted oblique sagittal MRI rather than axial CT images as used by Fuchs et al.10 Second, occupational ratio consists of areas calculated using PACS software. For example, the occupational ratio of the SSP muscle=area of the SSP muscle/(area of SSP fatty degeneration+area of the SSP muscle). This value calculated using Photoshop (Adobe, San Jose, California) on MRI oblique sagittal image. Then, the magic selection tool was used and clicked once on the inner part of the SSP muscle. The program expressed the cross-sectional area of SSP muscle as pixel and calculated the occupation ratio.11 Third, tangent sign is a technique for evaluating the amount of muscular atrophy of SSP tendon. It is the failure of the SSP to cross a line from the superior border of the coracoid process to the superior border of the scapular spine.9

Isokinetic Strength

Actual shoulder strength was evaluated by abduction, external rotation, and internal rotation using an isokinetic test, which was performed up to several days preoperatively using Biodex System 3 (Biodex Corp, Shirley, New York). Abduction was tested with the patient's trunk supported in a reclined position 40° from vertical in the scapular plane between 0° and 110° of abduction, whereas external and internal rotation were tested with the shoulder in a neutral position and the elbow flexed at 90°.2,18 The authors measured the isokinetic strength (peak torque [PT] and total work [TW]) deficit in abduction, external rotation, and internal rotation using a 60° per second load. Assuming the contralateral side was normal, the authors then computed the percentage of these values compared with the contralateral shoulder for each subject. For PT (Nm), the authors used the highest torque value during 5 repetitive isokinetic efforts. Total work (J) indicated the work performed by the subject in the repetition that produced the greatest value during the 5 repetitive isokinetic efforts.19

Statistical Analysis

Mean values were compared using Student's t test or the Mann–Whitney U test for continuous variables and the chi-square or Fisher's exact test for categorical variables to statistically evaluate the intergroup differences. For the correlation analyses, the authors calculated the correlation coefficients of the continuous and categorical variables (strength deficit, fatty degeneration, occupation ratio) using Pearson and Spearman's correlation coefficients. For correlation between tangent sign and strength deficit, receiver operating characteristic (ROC) curves were plotted for test results vs internal rotation strength deficit. Areas under the ROC curve range from 0.50 (indicating that the index performs no better than chance in discriminating between groups) to 1.0 (indicating perfect discrimination).18,20 All statistical analyses were performed using SPSS version 17.0 software (SPSS Inc, Chicago, Illinois), and statistical significance was accepted for P<.05.

Results

No significant differences were found in the baseline data or demographic factors, such as underlying disease (diabetes mellitus, hypertension, thyroid disease, or heart disease), sports activity level, work level, height, weight, body mass index, or bone mineral density between the nonmassive tear group and the massive tear group (all P>.05, Table 1).

Demographic Factors and Clinical Variables

Table 1:

Demographic Factors and Clinical Variables

In all patients, the correlation between fatty degeneration and actual shoulder strength deficit was weak. The occupation ratio was more closely correlated with actual muscle strength than the Goutallier grading system for SSP and abduction (Spearman correlation coefficients: 0.285, P<.001 vs 0.138, P=.08), infraspinatus (ISP) muscle and external rotation (0.180, P=.02 vs 0.041, P=.60), and subscapularis (SSC) muscle and internal rotation (0.166, P=.03 vs 0.116, P=.14) (Figure 1).

The overall correlation between fatty degeneration and shoulder strength was weak. The occupation ratio was more closely correlated with actual muscle strength than the Goutallier grading system for supraspinatus muscle (SSP) and abduction (0.285, P<.001 vs 0.138, P=.08), infraspinatus muscle (ISP) and external rotation (0.180, P=.02 vs 0.041, P=.60), and subscapularis muscle (SSC) and internal rotation (0.166, P=.03 vs 0.116, P=.14).

Figure 1:

The overall correlation between fatty degeneration and shoulder strength was weak. The occupation ratio was more closely correlated with actual muscle strength than the Goutallier grading system for supraspinatus muscle (SSP) and abduction (0.285, P<.001 vs 0.138, P=.08), infraspinatus muscle (ISP) and external rotation (0.180, P=.02 vs 0.041, P=.60), and subscapularis muscle (SSC) and internal rotation (0.166, P=.03 vs 0.116, P=.14).

According to tear size, in the non-massive tear group, the occupation ratio was more closely correlated with actual muscle strength than with the Goutallier grading system for SSP and abduction (0.312, P<.005 vs 0.211, P=.002), ISP and external rotation (0.218, P=.002 vs 0.108, P=.12), and SSC and internal rotation (0.215, P=.002 vs 0.169, P=.016) (Figure 2). However, in the massive tear group, a weaker correlation was observed for SSP and abduction (0.110, P=.46 vs 0.114, P=.45), ISP and external rotation (0.170, P=.26 vs 0.072, P=.63), and SSC and internal rotation (0.127, P=.40 vs 0.074, P=.62) (Figure 3). Data for patients with massive tears demonstrated a significantly inferior correlation between fatty degeneration and shoulder strength than those of patients with nonmassive tears.

In the nonmassive rotator tear group, occupation ratio was more closely correlated with actual muscle strength than the Goutallier grading system for supraspinatus muscle (SSP) and abduction (0.312, P<.005 vs 0.211, P=.002), infraspinatus muscle (ISP) and external rotation (0.218, P=.002 vs 0.108, P=.12), and subscapularis muscle (SSC) and internal rotation (0.215, P=.002 vs 0.169, P=.016).

Figure 2:

In the nonmassive rotator tear group, occupation ratio was more closely correlated with actual muscle strength than the Goutallier grading system for supraspinatus muscle (SSP) and abduction (0.312, P<.005 vs 0.211, P=.002), infraspinatus muscle (ISP) and external rotation (0.218, P=.002 vs 0.108, P=.12), and subscapularis muscle (SSC) and internal rotation (0.215, P=.002 vs 0.169, P=.016).

In the massive tear group, a weaker correlation was observed for supraspinatus muscle (SSP) and abduction (0.110, P=.46 vs 0.114, P=.45), infraspinatus muscle (ISP) and external rotation (0.170, P=.26 vs 0.072, P=.63), and subscapularis muscle (SSC) and internal rotation (0.127, P=.40 vs 0.074, P=.62).

Figure 3:

In the massive tear group, a weaker correlation was observed for supraspinatus muscle (SSP) and abduction (0.110, P=.46 vs 0.114, P=.45), infraspinatus muscle (ISP) and external rotation (0.170, P=.26 vs 0.072, P=.63), and subscapularis muscle (SSC) and internal rotation (0.127, P=.40 vs 0.074, P=.62).

Tangent sign findings indicated significant lower strength of external rotation and abduction. The tangent sign (+) group had significantly more severe deficits in external rotation (62.46±22.06, 95% confidence interval [CI], 55.71–69.91 vs 49.00±22.81, 95% CI, 15.60–52.23, P<.001) and abduction strength (74.86±27.30, 95% CI, 64.61–83.24 vs 64.42±29.66, 95% CI, 60.12–68.66, P=.04) (Table 2). Receiver operating characteristic curves were constructed to compare the relationships between the strength deficits in external rotation and abduction. The areas under the ROC curve for the abduction was 0.613 (P=.03), whereas that for the external rotation was 0.667 (P=.001). Tangent sign cutoff values were 67.23% for abduction and 48.84% for external rotation (Figure 4).

Correlation With Tangent Sign

Table 2:

Correlation With Tangent Sign

Receiver operating characteristic curves were constructed to compare the relationships between the strength deficits in external rotation and abduction. The tangent sign cutoff values were 67.23% for abduction and 48.84% for external rotation.

Figure 4:

Receiver operating characteristic curves were constructed to compare the relationships between the strength deficits in external rotation and abduction. The tangent sign cutoff values were 67.23% for abduction and 48.84% for external rotation.

Discussion

The authors aimed to determine the correlation between fatty degeneration and muscle strength. Fatty degeneration and rotator cuff muscle atrophy have been shown to predict post-repair clinical outcomes and can provide insight into tear severity to act as a guide for potential treatment options.2,4,21 These atrophy and fatty degeneration components greatly influence several clinical parameters, such as overall outcome and strength, and predict rotator cuff repair results.2,4,22,23 Therefore, evaluating the degree of fatty degeneration of the rotator cuff muscles is important in planning treatment strategies and may be useful in the prediction of postoperative outcomes. Several authors have proposed methods such as the Goutallier grading system, occupation ratio, and tangent sign to measure muscle atrophy and fatty degeneration of the rotator cuff muscles using CT and MRI.7–9 However, until now, no studies demonstrated whether fatty degeneration degree is correlated with actual shoulder strength deficits.

The current results showed that fatty degeneration severity was correlated with more severe muscle strength deficits. Therefore, clinicians may consider using fatty degeneration radiological findings to assess and establish actual shoulder strength deficits in the clinical setting. In cases of nonmassive rotator cuff tears in particular, fatty degeneration severity was more closely correlated with shoulder muscle strength deficits. In addition, occupational ratio was more closely correlated with actual shoulder muscle strength deficits than the Goutallier classification. In fact, a previous study reported relatively poorer inter-and intraobserver reliability due to the subjective nature of the Goutallier classification.15

Interestingly, fatty degeneration and shoulder strength demonstrated weaker associations in the massive rotator cuff tear group. The authors believe there are 2 possible explanations for this finding. First, in cases of massive tears, the transverse plane force couple is an essential factor in reestablishing a normal glenohumeral fulcrum.24 This force couple consists of the SSC muscle anteriorly balanced against the posterior rotator cuff (the ISP and teres minor muscles). Substantially balancing the force couple of the cuff and restoring stable fulcrum kinematics of the glenohumeral joint are important factors in rotator cuff tear repairs.25 Therefore, there will be a different correlation between fatty degeneration and actual muscle strength depending on whether the mechanism of force couple is highly functional (ie, the tear is balanced in the massive rotator cuff tear group).

Second, some patients with highly functional compensatory mechanisms in which alternative muscles such as the deltoid are used have a relatively good shoulder function despite a massive rotator cuff tear. A previous study reported that some patients may maintain relatively good strength despite high degrees of fatty degeneration after massive irreparable rotator cuff tears.26

The tangent sign of the SSP muscle is a significant method for identifying rotator cuff status and fatty degeneration.14,27 A previous study reported that a positive tangent sign has key decision-making value for evaluating reparability with good intra- and interobserver reliability.13 However, the correlation between tangent sign and actual shoulder muscle strength deficits is unknown.

The current results showed that a patient with a positive tangent sign had shoulder strength deficits of 62.46% in external rotation and 74.86% in abduction. Because the patient with a positive tangent sign had at least a 50% strength deficit in external rotation and abduction strength, this information may be useful for determining reparability and estimating fatty degeneration degree.

Several limitations should be noted when interpreting the current findings. First, in a previous study, the contralateral healthy shoulder was observed to have an asymptomatic cuff tear, particularly in older patients.28 It could have influenced the strength deficit potentially leading to misestimates. The lack of radiologic screening, such as sonography, of the contralateral shoulder owing to the retrospective study is a limitation, although patients with symptoms of the contralateral shoulder were specifically excluded by clinical test and manual muscle test.

Second, the fatty degeneration grading system may be flawed. The grades were measured at one cross-sectional image rather than the entire muscle belly, which may falsely represent the degree of fatty degeneration.

Third, pain and range of shoulder motion might have interfered with the isokinetic test, potentially underestimating the study's true strength. Although it is difficult to identify the degree to which pain affected the isokinetic results or exclude any effect, the authors excluded patients who were unable to initiate and endure the test because of pain-related pseudoparalysis. They also repeated each isokinetic test 5 times to overcome errors in single isokinetic measurements.

Fourth, each muscle (SSP, ISP, and SSC) was not fully matched by each direction of strength (abduction, external rotation, internal rotation). For example, external rotation strength is the whole sum of 3 muscles: the ISP, posterior part of the SSP, and teres minor.29,30 However, as previously reported, the fatty degeneration of each muscle was highly correlated with each strength direction,31 suggesting that it may useful information for orthopedic surgeons in the outpatient clinical setting. In addition, with standard posture based on the previous articles,31,32 isokinetic strength test was able to reflect the function of each individual rotator cuff muscle to some extent accurately, and therefore it was thought that there was a certain correlation with fatty degeneration.

Further studies including more detailed analyses may be needed to establish the correlation between fatty degeneration of rotator cuff tears and actual shoulder strength muscle deficits.

Conclusion

The fatty degeneration of the rotator cuff muscles measured by each method described here was correlated with actual shoulder strength deficits in patients with rotator cuff tears. However, the correlations were much weaker in patients with massive rotator cuff tears. Therefore, in such cases, fatty degeneration should be considered a factor affecting muscle strength that is not proportional to the muscle strength deficit extent.

References

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Demographic Factors and Clinical Variables

VariableTotalNonmassive Rotator Cuff Tear GroupMassive Rotator Cuff Tear GroupP
Patients, No.20315746
Age, mean, y61.2960.5963.70.34
Sex, male/female, No.88/11564/9324/22.17
Dominant side, No.16012139.62
Symptoms onset, mean, mo3.863.833.98.30
Smoking, No.45405.02a
Trauma history, No.786315.35
Diabetes mellitus, No.28208.42
Hypertension, No.554312.86
Hypercholesterolemia, No.431.91
Hyperthyroidism, No.081.39
Preoperative steroid injection, No.954.11
Sports level, low/moderate/high, No.143/57/3112/43/231/14/1.28
Overhead sports, No.725220.19
Shoulder activity during work, low/moderate/high, No.72/101/3054/79/2418/22/6.98
Tear size, mean, cm3.222.655.15NA
  Small/medium/large/massive, No.8/82/67/46
Combined pathology, No.
  SLAP795920.49
  AC arthritis17116.19
  Biceps tear786216.53
  SSP FD, 0/1/2/3/4, No.0/3/134/29/3795/44/18/0/00/1/16/8/21<.01a
  ISP FD, 0/1/2/3/4, No.107/64/25/1/695/47/14/0/112/17/11/1/5<.01a
  SSC FD, 0/1/2/3/4, No.72/44/60/3/2463/34/51/1/89/10/9/2/16<.01a
  TM FD, 0/1/2/3/4, No.160/39/3/0/1131/22/3/0/129/17/0/0/0.05a
  Tangent sign, No.361820<.01a
  SSP occupation ratio0.440.480.34<.01a
  ISP occupation ratio0.830.850.78.01a
  SSC occupation ratio0.770.810.66.01a

Correlation With Tangent Sign

Tangent SignNo.External Rotation Deficiency (SD)PAbduction Deficiency (SD)P
(+)16562.46 (22.06)<.00174.86 (27.30).04
(−)3849.00 (22.81)64.42 (29.66)
Authors

The authors are from the Department of Orthopaedic Surgery (JPY, JWJ, CHL, YGK, HJL, JWY) and the Department of Radiology (HL), Kyungpook National University Hospital, Daegu; the Department of Orthopaedic Surgery (SWC), Konkuk University Medical Center, Seoul; and the Department of Orthopaedic Surgery (JYK), Myongji Hospital, Gyeonggi-Do, Korea.

The authors have no relevant financial relationships to disclose.

This study was supported in part by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Science, ICT and Future Planning (grant 2015R1C1A1A02036478).

Correspondence should be addressed to: Jae Wook Jung, MD, Department of Orthopaedic Surgery, Kyungpook National University Hospital, 130 Dongdukro, Junggu, Daegu 700-721, Korea ( knuhos_sh@naver.com).

Received: June 15, 2017
Accepted: September 19, 2017

10.3928/01477447-20171106-02

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