The teres minor muscle in rotator cuff tendon tears

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1 Skeletal Radiol (2011) 40: DOI /s SCIENTIFIC ARTICLE The teres minor muscle in rotator cuff tendon tears Barbara Melis & Michael J. DeFranco & Alexandre Lädermann & Renaud Barthelemy & Gilles Walch Received: 13 September 2010 /Revised: 28 February 2011 /Accepted: 10 April 2011 /Published online: 24 May 2011 # ISS 2011 Abstract Objectives Although the teres minor has received little attention in the literature compared to the other musculotendinous units of the rotator cuff, it is an important component of shoulder function. Our purpose was to study the appearance of the teres minor muscle on CT and MRI images in various patterns of rotator cuff tears. Materials and methods We analyzed the appearance of the teres minor according to the Walch classification (normal, hypertrophic, atrophic, or absent) in 1,332 CT and in 240 MRI images of rotator cuff tears and we correlated it with the type of rotator cuff tears, time period between initial onset of symptoms and diagnostic imaging, age of the patient at the time of imaging, and degree of fatty infiltration of other rotator cuff muscles. Results The teres minor was classified as normal in 90.8% of cases, hypertrophic in 5.8%, atrophic in 3.2%, and B. Melis : G. Walch (*) Centre Orthopédique Santy, 24, Avenue Paul Santy, 69008, Lyon, France walch.gilles@wanadoo.fr G. Walch socoly@free.fr M. J. DeFranco Lenox Hill Hospital, New York, NY, USA A. Lädermann Department of Orthopaedic Surgery and Traumatology, University Hospitals of Geneva, Geneva, Switzerland R. Barthelemy Department of Radiology, Clinique du Mail, Grenoble, France absent in 0.2%. Significant variability existed in the appearance of the teres minor muscle among different patterns of rotator cuff tears in the CT (P<0.0001) and MRI groups (P<0.0001). The teres minor appeared most frequently hypertrophic in anterior tears and atrophic in posterior-superior tears. Conclusions The teres minor was normal in most rotator cuff tears. A morphologic classification system allowed the appearance of the teres minor to be defined in isolated and multiple rotator cuff tears in CT and MRI images. Keywords Shoulder. Rotator cuff. Tendon tear. Teres minor. Muscle appearance Introduction Despite numerous reports in the orthopaedic literature on rotator cuff tears, the teres minor infrequently receives attention. Indeed, most reports of the teres minor are described as traumatic injuries to the musculotendinous unit [1, 2] or as neurologic lesions of the posterior branch of the axillary nerve [3, 4]. Damage to the teres minor can also be degenerative, similar to the process that occurs in other musculotendinous units of the rotator cuff. Isolated tears of the teres minor tendon are rare. They occur more commonly in combination with supraspinatus and infraspinatus tendon tears or in massive rotator cuff tears [5]. The teres minor functions primarily to externally rotate the arm and secondarily to depress the humeral head [6 12]. More specifically, the teres minor provides 20 45% of external rotation power to the glenohumeral joint [12 14]. Its function may become even more important when there are large tears of the rotator cuff, especially those involving the infraspinatus.

2 1336 Skeletal Radiol (2011) 40: The atrophy of the teres minor in the presence of a severe fatty infiltration (FI) of the infraspinatus negatively influences the clinical outcome in patients with massive rotator cuff tears and in patients undergoing reverse shoulder arthroplasty [6, 15 17]. In the clinical evaluation and in the diagnosis of rotator cuff lesions, the teres minor has often been considered together with the infraspinatus. In these cases, if the infraspinatus is normal, no test isolates the teres minor for an independent assessment of its function. However, if the infraspinatus is pathologic (e.g., complete tear, paralysis, severe FI), then testing of the teres minor is possible in external rotation at 90 of abduction [7]. The function of the teres minor is proportional to its strength in external rotation at 90 of abduction in the presence of a severe fatty infiltration of the infraspinatus [7]. In cases of significant arthritis, clinical examination of external rotation is not always possible because of the restriction in motion caused by degenerative changes in the glenohumeral joint. In general, and especially in cases where external rotation cannot be assessed on physical examination, understanding the appearance of the teres minor on imaging studies becomes crucial to defining its influence on surgical procedures and clinical outcome. In the classification system for fatty infiltration of rotator cuff muscles, Goutallier and Bernageau [18] did not address the teres minor. Walch et al. [5, 6] introduced a morphologic classification system where four terms are used to describe the status of the teres minor muscle using the sagittal and axial views from CT or MRI images. The goal of this study was to analyze the appearance of the teres minor muscle in rotator cuff tears using the Walch classification and to correlate that appearance with the type of rotator cuff tear, delay elapsed between symptom onset and imaging, age of the patient at imaging, and degree of fatty infiltration of other rotator cuff muscles. Materials and methods This investigation was performed at the Department of Shoulder Surgery, Centre Orthopédique Santy, Lyon, France. The Institutional Review Board and ethics committee have approved this research project. This study is a retrospective review of preoperative CT or MRI of 2,500 patients with rotator cuff tears, who underwent either a tendon repair, an arthroscopic subacromial debridement, or a reverse shoulder arthroplasty at our institution between 1988 and 2005 by the senior author. Patients with previous surgical treatment on the affected shoulder, absence of tendon tears, detected neurologic lesions, or incomplete imaging studies were excluded. After the exclusion criteria were applied, there were 1,572 cases where the quality of imaging was sufficient to study correctly the teres minor muscle on axial and sagittal plane images. Eighty-five percent (1,332/1,572) had a preoperative CT (1,309 CT arthrogram, 23 CT) and 15% (240/1,572) had a preoperative MRI (13 MRI arthrogram, 227 MRI). Soft-tissue windows on CT images and T1 MRI sequences were used. The appearance of the teres minor on the imaging studies was described according to the Walch [5, 6] classification (Fig. 1) as follows: normal: the thickness of the muscle is half of the anterior-posterior width of the glenoid; hypertrophic: the thickness of the muscle is larger than the anterior-posterior width of the glenoid; atrophic: the muscle is thinned in the anterior-posterior width, and there are tracks of fatty infiltration; and absent: the muscle is not identifiable. The appearance of the teres minor was analyzed using images in both planes by one independent observer, an orthopaedic surgeon with fellowship training in shoulder surgery. Images were prepared independently and presented to the interpreter for review. When the appearance of the teres minor was different in each plane, then the axial images were used for the final description of the muscle. The stage of fatty infiltration of the other rotator cuff muscles on the CT mages (soft-tissue windows) was described using the classification system of Goutallier et al. [18] or on T1 MRI sequences using the classification system adapted from Fuchs et al. [19]. In order to increase reliability [19] and to facilitate statistical evaluation, the Goutallier classification, which was used to define fatty infiltration in rotator cuff muscles other than the teres minor, was simplified by using the terms minimal for Goutallier stages 0 and 1, moderate for stage 2, and severe for stages 3 and 4 [19]. For each patient we collected data from the charts including type of cuff tear, etiology of the tear (traumatic, degenerative, uncertain), patient gender, dominant hand, time period between initial onset of symptoms and diagnostic imaging, and age of the patient at imaging. The types of rotator cuff tears in the CT and MRI groups are shown in Table 1. The type of cuff tear, defined by clinical examination and imaging studies, was confirmed in the operative note. Statistical analysis We used the chi-squared likelihood ratio test to test categorical variables and the Fisher exact test to test the qualitative variables. For the quantitative variables, we performed a one-way analysis of variance (ANOVA). Since the values were sometimes quite widely scattered (mean

3 Skeletal Radiol (2011) 40: Fig. 1 Appearance of the teres minor in rotator cuff tears on the axial plane in the CT group (a) and in the MRI group (b). Appearance of the teres minor in rotator cuff tears on the sagittal plane (c)

4 1338 Skeletal Radiol (2011) 40: Fig. 1 (continued) different from the median, nonhomogenous variances), we used the Kruskal-Wallis nonparametric test. Results The supraspinatus tendon was involved in 93% of cases (1,462/1,572), the subscapularis in 38.6% of cases (607/ 1,572), and the infraspinatus in 25% of cases (393/ 1,572). Isolated infraspinatus tendon tears were not seen in this series. All infraspinatus tears occurred in conjunction with a supraspinatus tear, a supraspinatus and teres minor tear, or a supraspinatus and subscapularis tear. A tear of the teres minor was found in 0.9% of all cases, and it was always associated with supraspinatus and infraspinatus tear (Table 1). The average patient age at the time of imaging was 57.3 years (range years). Males represented 59.7% of the patients (938/1,572). The dominant side was involved in 70% of the patients (1,100/1,572). The etiology of the rotator cuff tear was defined as traumatic in 40% (629/1,572), degenerative in 53% (834/1,572), and uncertain in 7% of cases (109/1,572). Appearance of the teres minor on rotator cuff tears Overall, the teres minor was classified as normal in 90.8% of cases (1,428/1,572), hypertrophic in 5.8% (91/1,572), atrophic in 3.2% (50/1,572), and absent in 0.2% of cases (3/ 1,572). As shown in Fig. 2a and b, a significant correlation was found between the type of rotator cuff tear and the appearance of the teres minor muscle in the CT (P<0.0001) and MRI groups (P<0.0001). In the CT group, less variability in the appearance of the teres minor was observed in isolated tears of the supraspinatus compared to that seen in massive rotator cuff tears involving the supraspinatus, infraspinatus, and subscapularis. In the MRI group, less variability in the appearance of the teres minor was observed in isolated tears of the supraspinatus and in supraspinatus+subscapularis tears compared to that seen in massive rotator cuff tears involving the supraspinatus, infraspinatus, and subscapularis.

5 Skeletal Radiol (2011) 40: Table 1 Types of rotator cuff tear in CT and MRI groups SS Supraspinatus, SScap Subscapularis, IS infraspinatus, TM teres minor Type of rotator cuff tear CT group (n) MRI group (n) Total series (n) Full thickness SS Partial thickness SS Isolated SScap SS + SScap SS + IS SS + IS + TM SS + IS + SScap Total 1, ,572 Each group in the teres minor classification (normal, hypertrophic, atrophic, absent) was analyzed collectively with respect to associated rotator cuff tears (Tables 2 and 3). A significant difference was found in the frequency of each type of rotator cuff tear for each type of appearance of the teres minor in the CT (P<0.0001) and MRI groups (P<0.0001). In the CT group (Table 2), the highest percentage of a normal appearing teres minor occurred in the group of isolated supraspinatus tears. The highest percentage of a hypertrophic appearing teres minor occurred in the group with anteriorsuperior tears (supraspinatus + subscapularis). The highest percentage of an atrophic teres minor muscle occurred in posterior-superior tears (supraspinatus, infra- Fig. 2 Frequency of the different appearances of the teres minor for each group of rotator cuff tears in the CT (a) and MRI (b) groups (P< ). SS Supraspinatus, Sscap subscapularis, IS infraspinatus, TM teres minor, thick thickness

6 1340 Skeletal Radiol (2011) 40: Table 2 Frequency of type of rotator cuff tear for each appearance of teres minor in the CT group (P<0.0001) SS Supraspinatus, SScap subscapularis, IS infraspinatus, TM teres minor TM normal TM hypertrophic TM atrophic TM absent n=1,202 n=84 n=43 n=3 Full thickness SS tears 35.4% 6.0% 16.3% 0.0% Partial thickness SS tears 12.0% 1.2% 0.0% 0.0% SS + IS ± TM tears 14.4% 7.1% 44.2% 0.0% SS + SScap tears 21.4% 46.4% 11.6% 33.3% SS + IS + SScap tears 9.9% 17.9% 27.9% 66.7% Isolated SScap tears 6.9% 21.4% 0.0% 0.0% Total 100% 100% 100% 100% spinatus ± teres minor). The highest percentage of an absent teres minor muscle occurred in tears involving the supraspinatus, infrapsinatus + subscapularis. In the MRI group (Table 3), the highest percentage of a normal appearing teres minor occurred in the group of isolated supraspinatus tears. In contrast to the CT group, a hypertrophic appearing teres minor did not occur in the group with anterior-superior tears (supraspinatus + subscapularis). The highest percentage of an atrophic teres minor muscle occurred in posterior-superior tears (supraspinatus, infraspinatus ± teres minor). No absent teres minor muscle was observed. If the appearance of the teres minor in the group with supraspinatus and infraspinatus tears was compared to the group with supraspinatus, infraspinatus, and teres minor tears, the occurrence of teres minor atrophy was different. The appearance of the muscle was atrophic in 6.5% and in 11.1% of patients with tears involving the supraspinatus and infraspinatus, respectively, in the CT and MRI groups. However, these percentages increased to 53.8% in the CT group (P<0.0001) and to 100% in the MRI group (P=0.2) when this tear pattern involves the teres minor. Correlation between the appearance of the teres minor and age As shown in Table 4, the appearance of the teres minor muscle in the CT (P=0.0009) and MRI groups (P=0.1) differed with the age of the patients. The average age of the patients increased with normal, hypertrophic, atrophic, and absent appearance of the teres minor. Correlation between the appearance of the teres minor and the time between the onset of symptoms and diagnosis The appearance of the teres minor was not correlated with time that elapsed between the onset of symptoms and diagnostic imaging in the different patterns of rotator cuff tears in the CT (P=0.05) and MRI groups (P=0.9). Correlation between the appearance of the teres minor and concomitant rotator cuff fatty infiltration CT group There was a correlation between the stage of infraspinatus fatty infiltration and the appearance of the teres minor in the group with supraspinatus and infraspinatus tears (P=0.001) and in the group with a tear involving the supraspinatus, infraspinatus, and subscapularis (P=0.06). In cases of severe fatty infiltration of the infraspinatus, the frequency of teres minor atrophy and hypertrophy increased (Table 5). Also, there was a correlation between the stage of subscapularis fatty infiltration and the appearance of the teres minor in the group with a tear involving the supra- Table 3 Frequency of type of rotator cuff tear for each appearance of teres minor in MRI group (p<0.0001) SS Supraspinatus, SScap subscapularis, IS infraspinatus, TM teres minor TM normal TM hypertrophic TM atrophic TM absent n=226 n=7 n=7 n=0 Full thickness SS tears 43.4% 28.6% 14.3% 0.0% Partial thickness SS tears 20.3% 0.0% 0.0% 0.0% SS + IS ± TM tears 13.3% 28.6% 71.4% 0.0% SS + SScap tears 16.4% 0.0% 0.0% 0.0% SS + IS + SScap tears 3.5% 14.3% 14.3% 0.0% Isolated SScap tears 3.1% 28.5% 0.0% 0.0% Total 100% 100% 100% 100%

7 Skeletal Radiol (2011) 40: Table 4 Average age±standard deviation according with teres minor appearance in the CT (P=0.0009) and MRI groups (P=0.1) spinatus, infraspinatus, and subscapularis (P=0.1) and in the group with isolated subscapularis or supraspinatus and subscapularis tears (P<0.0001). In the presence of severe subscapularis fatty infiltration, the teres minor appears largely hypertrophic (Table 6). MRI group There was no significant correlation between the stage of infraspinatus fatty infiltration and the appearance of the teres minor in the group with supraspinatus and infraspinatus tears (P=0.1) and in the group with a tear involving the supraspinatus, infraspinatus, and subscapularis (P=0.3) (Table 7). Also, no significant correlation was found between the stage of subscapularis fatty infiltration and the appearance of the teres minor in the group with a tear involving the supraspinatus, infraspinatus, and subscapularis (P= 0.2); in the group with isolated subscapularis tears; and in the group with a tear involving the supraspinatus and subscapularis tear (P=1.0) (Table 8). Discussion CT group (years) MRI group (years) Normal 56.8± ±9.2 Hypertrophic 59.4± ±15.3 Atrophic 61.8± ±10.1 Absent 63.7±5.1 - Few studies have examined the appearance of the teres minor in relation to concomitant rotator cuff tears [3, 16, 20]. The results of this study help to characterize the pathology of the teres minor in the presence of various rotator cuff tear patterns. Understanding the pathologic appearance of the teres minor is essential to predicting the potential for successful clinical outcome in rotator cuff repairs, tendon transfers, and reverse shoulder arthroplasty. Worse clinical outcomes have been reported in patients with massive rotator cuff tears and in patients undergoing reverse shoulder arthroplasty in the presence of teres minor atrophy and severe fatty infiltration of the infraspinatus [6, 15, 16]. In our study, the teres minor was classified as normal in 90.8%, hypertrophic in 5.8%, atrophic in 3.2%, and absent in 0.2% of cases. More specifically in the CT and MRI groups, in isolated supraspinatus tears, the most frequent appearance (>97%) of the teres minor was normal. However, in isolated tears of the subscapularis, there was a more hypertrophic appearance. In cases of multiple tendon tears, the most common appearance (>80%) of the teres minor was normal. However, in these cases there was an increasing amount of teres minor atrophy in posterior superior tears. Multiple tendon tears involving the subscapularis consistently revealed a hypertrophic teres minor compared to cases where the subscapularis was intact (Fig. 2a, b). A compensatory hypertrophy of the teres minor has been described in the case of an infraspinatus tendon tear [7, 12]. However, a hypertrophic appearance in the case of anterior rotator cuff tears has not been described before. Latissimus dorsi transfer has been proposed for irreparable postero-superior cuff tears [21] and to restore external rotation in reverse shoulder arthroplasty [16, 17, 22, 23]. In our series, the teres minor was atrophic or absent in only 3.4% of rotator cuff tears, showing that the indications for a latissimus dorsi tendon transfer are not frequent [22, 24]. In addition to the 1,572 cases of rotator cuff tears analyzed in this study, 354 cases were defined as rotator cuff tendonitis without a definitive tear and were not included in this series. In these cases the appearance of the teres minor was normal. Additionally, two cases revealed Table 5 Correlation between the stage of infraspinatus fatty infiltration and appearance of the teres minor in SS+IS tears (P=0.001) and in SS+ IS+SScap tears (P=0.06) in CT group SS+IS tears SS+IS+SScap tears IS FI minimal IS FI moderate IS FI severe IS FI minimal IS FI moderate IS FI severe n=68 n=65 n=52 n=32 n=67 n=48 TM normal 98.5% 93.9% 75.0% 87.5% 85.1% 68.7% TM hypertrophic 1.5% 1.5% 7.7% 12.5 % 6.0% 14.6% TM atrophic 0.0% 4.6% 17.3% 0.0% 8.9% 12.5% TM absent 0.0% 0.0% 0.0% 0.0% 0.0% 4.2% SS Supraspinatus, IS infraspinatus, SScap subscapularis, FI fatty infiltration, TM teres minor

8 1342 Skeletal Radiol (2011) 40: Table 6 Correlation between the stage of subscapularis fatty infiltration and appearance of the teres minor in SS+IS+SScap tears (P=0.1) and in isolated SScap tears or in SS+SScap tears (P<0.0001) in the CT group SS+IS+SScap tears Isolated SScap or SS+SScap tears SScap FI minimal SScap FI moderate SScap FI severe SScap FI minimal SScap FI moderate SScap FI severe n=109 n=29 n=9 n=349 n=38 n=13 TM normal 83.5% 72.4% 66.7% 87.7% 60.5% 61.5% TM hypertrophic 7.3% 13.8% 33.3% 10.6% 39.5% 38.5% TM atrophic 8.3% 10.3% 0.0% 1.4% 0.0% 0.0% TM absent 0.9% 3.5% 0.0% 0.3% 0.0% 0.0% SS Supraspinatus, IS infraspinatus, SScap subscapularis, FI fatty infiltration, TM teres minor isolated fatty infiltration in the teres minor (Fig. 3) and two cases revealed an absent teres minor in an otherwise normal rotator cuff. In the two latter cases, the absence of the teres minor may be a congenital absence or a muscle agenesis that has not been previously described in the literature. There was a trend toward older age being associated with a more atrophic or absent teres minor. No significant relationship was observed between the time to diagnosis (from onset of symptoms to diagnostic imaging) and the appearance of the teres minor. Although this time period most likely contributes to the development of pathology seen in the teres minor, a relationship could not be defined by the data in this study. Although various imaging techniques (ultrasound, CT scan, MRI) allow the distinction to be made between the teres minor and the infraspinatus muscle, identifying a true tendon tear in the teres minor is difficult due to its extensive muscular nature. For this reason and because the status of the muscle belly provides more prognostic information than the tendon, the macroscopic appearance of the teres minor muscle was analyzed in this study using a morphologic classification system instead of a quantitative one. Although the Goutallier classification may be used for describing fatty infiltration, neither the original study presenting this classification nor subsequent ones that applied it [16, 17] discussed its use specifically for the teres minor. The use of descriptive terms for the teres minor allows for a more immediate method for communicating the status of the teres minor muscle. The advantage of a morphologic classification, being qualitative not quantitative, is that it can be applied both to CT and to MRI. In this study we assessed the teres minor according to that principle using both CT and MRI images. We also attempted to analyze the CT and MRI images separately, but the number of patients and RCT patterns did not allow for a meaningful evaluation. Clinically, the most useful classification is the one that can be applied to either CT scan or MR images. Future studies are needed to further evaluate the reliability of the Walch classification specifically with regard to each type of imaging study. This study did not assess whether the changes in the teres minor were reversible or irreversible. In general, with regards to rotator cuff muscles, fatty infiltration is an irreversible phenomenon. The presence of fatty infiltration and atrophy is prognostic and instructive for understanding the potential for healing and satisfactory clinical outcome. A correlation was found between the appearance of the teres minor and fatty infiltration of other rotator cuff muscles. More severe fatty infiltration meant that the teres Table 7 Correlation between the stage of infraspinatus fatty infiltration and appearance of the teres minor in SS+IS tears (P=0.1) and in SS+IS+ SScap tears (P=0.3) in the MRI group SS+IS tears SS+IS+SScap tears IS FI minimal IS FI moderate IS FI severe IS FI minimal IS FI moderate IS FI severe n=13 n=7 n=16 n=2 n=4 n=3 TM normal 100.0% 57.1% 81.3% 100.0% 100.0% 33.4% TM hypertrophic 0.0% 14.3% 6.2% 0.0 % 0.0% 33.3% TM atrophic 0.0% 28.6% 12.5% 0.0% 0.0% 33.3% TM absent 0.0% 0.0% 0.0% 0.0% 0.0% 0.0% SS Supraspinatus, IS infraspinatus, SScap subscapularis, FI fatty infiltration, TM teres minor

9 Skeletal Radiol (2011) 40: Table 8 Correlation between the stage of subscapularis fatty infiltration and appearance of the teres minor in SS+IS+SScap tears (P=0.2) and in isolated SScap tears or in SS+SScap tears (P=1.0) in MRI group SS+IS+SScap tears Isolated SScap or SS+SScap tears SScap FI minimal SScap FI moderate SScap FI severe SScap FI minimal SScap FI moderate SScap FI severe n=6 n=1 n=1 n=37 n=6 n=2 TM normal 100.0% 100.0% 0.0% 94.6% 100.0% 100.0% TM hypertrophic 0.0% 0.0% 0.0% 5.4% 0.0% 0.0% TM atrophic 0.0% 0.0% 100.0% 0.0% 0.0% 0.0% TM absent 0.0% 0.0% 0.0% 0.0% 0.0% 0.0% SS Supraspinatus, IS infraspinatus, SScap subscapularis, FI fatty infiltration, TM teres minor minor was not normal and, in most cases, became atrophic or hypertrophic. Future studies will correlate the findings in this study with patient function and satisfaction to better understand the impact of teres minor pathology on clinical outcome. The appearance of the teres minor in isolated and multiple rotator cuff tendon tears is defined in this study using a morphologic classification system. The teres minor was atrophic or absent in 3.4% of cases and normal or hypertrophic in the remaining part of the series. Understanding the preoperative appearance of the teres minor provides prognostic information about the ability to achieve a successful clinical result. Future studies are necessary to define the postoperative appearance and function of the teres minor muscle and to make comparisons with the preoperative assessment. Fig. 3 Isolated fatty infiltration of the teres minor in the absence of rotator cuff tears: appearance on the axial (a) and on the sagittal (b) planes

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