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Sonography of the Teres Minor: A Study of Cadavers

¹ Department of Orthopaedic Surgery, Washington University School of Medicine, Barnes-Jewish Hospital, St. Louis, MO 63110.
² Abdominal Imaging Section, Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S Kingshighway Blvd., St. Louis, MO 63110.

Received July 31, 2007; accepted after revision October 3, 2007.

 
Address correspondence to S. A. Teefey (teefeys{at}mir.wustl.edu).

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. The purpose of our study was to evaluate in cadavers the ability of highresolution sonography to identify both the normal tendinous insertion and tears of the teres minor.

MATERIALS AND METHODS. The teres minor insertion in five cadaveric shoulders was imaged, and methylene blue dye was injected into both the superior and inferior margins of the teres minor insertion by experienced musculoskeletal radiologists using a 10-5–MHz linear array transducer. Afterward, posterior shoulder dissection was performed. In another group of 11 cadaveric shoulders, an artificial tear was created at the teres minor insertion in six shoulders, and a sham procedure was performed in the remaining five shoulders arthroscopically. After arthroscopy, the teres minor insertion of each shoulder was imaged, and the accuracy of sonography for detecting a tear was evaluated.

RESULTS. The dye was injected correctly into both the superior and inferior margins of the teres minor insertion in all five cadaveric shoulders. All six artificial tears were successfully detected on sonography. Four of the five specimens with the sham procedure were identified as having a normal teres minor insertion. One was misinterpreted as a tear.

CONCLUSION. Sonography can reliably be used to identify the teres minor insertion and to detect tears of the teres minor muscle–tendon unit.

Keywords: artificial tear • cadaver • sonography • teres minor

Introduction

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Although the supraspinatus and infraspinatus tendons are most commonly involved in rotator cuff tears, tears of the subscapularis or teres minor tendons or both may have more severe consequences to shoulder function. Tears in these tendons may jeopardize glenohumeral joint stability by disrupting the rotator cuff force couple, leading to limited ability to elevate above the horizontal. An intact teres minor makes an important contribution to shoulder function in patients with large or massive tears of the rotator cuff [1, 2]; it contributes enough power to externally rotate the abducted arm, helps to maintain the ability to perform important activities of daily living, and reduces symptoms of rotator cuff tears [2].

In the setting of reverse shoulder arthroplasty, where the rotator cuff is not required as a primary stabilizer or mover, the integrity of the teres minor is essential for the recovery of external rotation and significantly influences postoperative shoulder function [3, 4]. Despite its clinical importance, the evaluation of the integrity of the teres minor has largely relied on physical examination. Although the status of the teres minor muscle can be assessed with various radiologic imaging tests such as MRI, CT, and sonography, to our knowledge, no radiologic studies have been published that have sonographically evaluated the anatomy of the humeral insertion of the teres minor. The purpose of this study was to determine whether sonography could identify the normal teres minor insertion and detect tears of the teres minor insertion in cadaveric shoulders.

Materials and Methods

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Cadaveric Study of the Normal Teres Minor Insertion
All the cadavers used for this study were obtained from the department of anatomy at our institution. The cadavers were unembalmed, freshly frozen, and skeletally mature. All were disarticulated from the thorax at the scapulothoracic plane. The specimens were thawed for at least 24 hours before the experiment. Posterior shoulder anatomic dissection was performed on two cadaveric shoulders by an orthopedic surgeon to allow two radiologists with at least 8 years of experience with musculoskeletal sonography to become conversant with the regional anatomy of the posterior shoulder. Topographic relationships between the teres minor and adjacent structures were emphasized.

Next, six cadaveric shoulders were obtained to evaluate the teres minor insertion using sonography. Each cadaveric shoulder was mounted on a holding fixture, simulating the routine position for shoulder sonography; the scapula was in the anatomic position, and the humerus hung free in a vertical orientation in neutral rotation. The teres minor was imaged by two radiologists concurrently. All sonograms were obtained in real time with the use of a Zonare scanner (Z. ONE version 1.6, Zonare Medical Systems) and a highresolution linear array transducer (10-5–MHz). The longitudinal view of the teres minor insertion was obtained with the transducer placed parallel to the direction of the teres minor muscle fibers at the level of the posterior glenohumeral joint line (Fig. 1). Because the teres minor originates from the middle portion of the lateral border of the scapula and inserts onto the inferior aspect of the posterior greater tuberosity, the direction of the teres minor muscle fibers is slightly oblique from inferomedial to superolateral. Therefore, the transducer was oriented in an oblique plane of approximately 30° to the scapular spine. The transverse view of the teres minor was obtained with the transducer placed perpendicular to the direction of the teres minor muscle fibers at the level of the posterior humeral head (Fig. 2). One shoulder was found to have a massive tear of the supraspinatus and infraspinatus that extended into the teres minor on both sonography and dissection. This shoulder was excluded from the study. In the remaining shoulders, images were obtained of the regions presumed to represent the teres minor insertion on the humeral head. To determine correct locali zation of the teres minor insertion, an attempt was made to inject 0.1 mL of methylene blue dye into the regions thought to represent the superior and inferior margins of the teres minor insertion under sonographic guidance using a 25-gauge needle. Immediately after injection, the orthopedic surgeon dissected the posterior shoulder to ident ify the teres minor insertion and to determine the location of the dye.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1 —Longitudinal view of teres minor was obtained with transducer placed parallel to direction of teres minor muscle fibers over posterior glenohumeral joint line. Because of oblique course of teres minor, transducer was at a 30° angle to scapular spine. AC = acromion, SP = scapular spine.

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2 —Transverse view of teres minor was obtained with transducer placed perpendicular to direction of teres minor muscle fibers over posterior humeral head. AC = acromion, SP = scapular spine.

For each procedure, a posterolateral portal was created at a location 2-cm lateral and 1-cm anterior to the posterolateral corner of the acromion and used as a viewing portal. A posterior portal was created at a location 2.5 cm inferior and 1 cm medial to the posterolateral corner of the acromion and used as a working portal. While viewing through the posterolateral portal with an arthroscope, the subacromial and subdeltoid bursae were removed with an arthroscopic shaver through the posterior portal. A limited bursectomy was performed to allow visualization of the teres minor. To create an artificial full-thickness tear, a vertical incision was made through the teres minor approximately 0.5 cm medial to its insertion with a number 11 blade through the posterior portal. The incision was trimmed slightly with the shaver to reproduce a retracted tear. In those shoulders that underwent the sham procedure, only the bursal tissue was removed arthroscopically, leaving the teres minor intact. Before withdrawing the arthroscope and shaver, as much water as possible was removed from the soft tissues with suction and manual compression. The skin incisions were closed with 2–0 nylon sutures. The two radiologists, blinded to the surgical procedures, together scanned the shoulders to determine whether the teres minor insertion was intact or torn. As part of the assessment, the arm was internally and externally rotated. A tear was suspected when there was either an anechoic or hypoechoic disruption of the continuity of the teres minor musculotendinous unit. When the musculotendinous unit did not move with the humerus on repeated internal and external rotation of the arm, a full-thickness tear was suspected. A final decision regarding the absence or presence of a tear was made by consensus. Immediately after sonography, the orthopedic surgeon dissected the posterior shoulder to confirm the sonographic findings.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A —Longitudinal sonograms of infraspinatus and teres minor at insertions on humeral head. GL = glenoid, HH = humeral head, IST = infraspinatus tendon, TM = teres minor tendon, DT = deltoid. Sonogram shows infraspinatus has long, wedge-shaped insertion.

View larger version (84K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B —Longitudinal sonograms of infraspinatus and teres minor at insertions on humeral head. GL = glenoid, HH = humeral head, IST = infraspinatus tendon, TM = teres minor tendon, DT = deltoid. Sonogram shows teres minor has rather quadrangular-shaped insertion.

Top Abstract Introduction Materials and Methods Results Discussion References

The distinction between the two muscle–tendon units was better seen on the transverse view, where the teres minor muscle–tendon unit assumed a narrow, oblong shape as it inserted onto the inferior-most aspect of the greater tuberosity and humeral surgical neck. The average width of the five teres minor muscle–tendon units was 2.53 ± 0.25 cm (mean ± SD) on sonography (Fig. 4). During gross dissection, the teres minor muscle–tendon unit could be easily distinguished from the infraspinatus muscle–tendon unit by observing the two adjacent, but clearly separate, muscle masses and a fatty streak intervening between the two. In all specimens, the injected dye was found at this junction between the two muscle–tendon units (Fig. 5A, 5B). The width of the teres minor muscle–tendon units measured at the time of dissection was almost identical to the measurements on sonography in all specimens (Fig. 6). In one of the five specimens, the injected dye spread into the joint space, staining part of the humeral head articular surface.

View larger version (104K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4 —Transverse sonogram of teres minor muscle–tendon unit shows characteristic oblong contour. HH = humeral head, SN = surgical neck of the humerus, TM = teres minor muscle–tendon unit, DT = deltoid.

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A —Teres minor shown during dissection after sonographically guided dye injection. HH = humeral head, IST = infraspinatus, TM = teres minor. Photograph shows superior margin has narrow fatty streak (white arrow), which facilitates distinction between infraspinatus and teres minor insertions. Methylene blue (black arrows) was injected directly into superior and inferior margins of teres minor insertion.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B —Teres minor shown during dissection after sonographically guided dye injection. HH = humeral head, IST = infraspinatus, TM = teres minor. Photograph after removal of infraspinatus and joint capsule shows teres minor insertion is now well visualized. Arrows indicate methylene blue dye injected into superior and inferior margins of teres minor insertion.

View larger version (137K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6 —Photograph shows width of teres minor insertion measured during dissection was almost identical to measurements on sonography in all specimens. TM = teres minor.

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A —Full-thickness artificial tear created with arthroscopy. HH = humeral head, SN = surgical neck, IST = infraspinatus, TM = remaining part of teres minor. On longitudinal (A) and transverse (B) sonograms, tear (arrow) appears as hypoechoic defect near teres minor insertion.

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B —Full-thickness artificial tear created with arthroscopy. HH = humeral head, SN = surgical neck, IST = infraspinatus, TM = remaining part of teres minor. On longitudinal (A) and transverse (B) sonograms, tear (arrow) appears as hypoechoic defect near teres minor insertion.

View larger version (145K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7C —Full-thickness artificial tear created with arthroscopy. HH = humeral head, SN = surgical neck, IST = infraspinatus, TM = remaining part of teres minor. Photograph shows corresponding tear (arrow) after dissection. Tear was created approximately 0.5-cm medial to insertion.

Discussion

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Along with the infraspinatus, the teres minor primarily acts as an external rotator of the humerus [5, 6]. At greater than 60° of abduction, the infraspinatus no longer has a significant external rotational moment arm, and the teres minor becomes the predominant external rotator [7]. The absence of a functional teres minor imposes a significant functional deficit on the already compromised shoulder. Patients who have a massive rotator cuff tear complicated by a lack of a functional teres minor are unable to bring the hand to the mouth without abducting the affected arm, resulting in positive "hornblower's sign" [2, 8]. Patients with a positive hornblower's sign experience significant difficulties with various activities of daily living because they are not able to clear the affected arm from the body. On the other hand, patients with a massive rotator cuff tear, but with an intact or even hypertrophied teres minor, often have relatively preserved shoulder function for eating, drinking, or washing their face because the intact teres minor contributes enough power for external rotation to allow these activities of daily living.

The integrity of the teres minor is also essential after various reconstructive procedures in cuff-deficient shoulders. Gartsman [1] reported that the integrity of the teres minor and subscapularis was one of the important factors in obtaining a satisfactory range of motion and overhead function after operative débridement and subacromial decompression of massive, irreparable rotator cuff tears. Reverse total shoulder arthroplasty has recently become popular because of its potential to restore function in patients with glenohumeral arthropathy as a result of massive cuff deficiency. Even though reverse arthroplasty does not require the rotator cuff as a primary stabilizer or mover, the integrity of the teres minor is critical for the recovery of external rotation and significantly influences postoperative function [3, 4]. Despite its importance as a major determinant of shoulder function, the integrity of the teres minor insertion has often been overlooked during clinical and radiologic examination. Most of the published radiologic studies focus on only the muscular portion of the teres minor [9–12].

Our study shows that sonography can be used to accurately identify the insertion of the teres minor. At gross dissection, we found that the teres minor insertion was largely muscular apart from a narrow tendinous slip in the superior-most aspect. The muscle fibers ran parallel to the tendinous slip instead of toward it and splayed out creating a broad insertion that began immediately inferior in relation to the equator of the humeral head and extended onto the surgical neck, thus contributing to the overall quadrangular appearance of the muscle–tendon unit. The deep surface of the teres minor insertion was loosely connected with the posterior and inferior joint capsule that covered the humeral head. The lateral-most aspect of the insertion was quite thinned. A fatty streak between the infraspinatus and teres minor muscle–tendon units facilitated the distinction between the two in most specimens.

On sonography, the teres minor insertion was easy to identify on longitudinal views. Once we identified the characteristic shape of the infraspinatus muscle–tendon unit on the longitudinal view by its central tendon and triangular shape, we slid the probe inferiorly, maintaining the same orientation to find the teres minor muscle–tendon unit. We then followed the muscle–tendon unit laterally to its broad insertion on the humerus and turned the probe 90° to obtain the transverse view. On the transverse view, the insertion of the teres minor had a characteristic oblong shape. The superior margin was located immediately inferior in relation to the equator of the humeral head, and the inferior edge tapered in thickness to splay onto the surgical neck. This view allowed us to accurately identify the margins before methylene blue injection. We did not measure the thickness of the tendon at its insertion because in previous cadaver studies we found that the loss of tissue elasticity and difficulty in placing the transducer so as not to compress the muscle resulted in inaccurate measurements.

Our study also showed that sonography is accurate for diagnosing a teres minor tear. We correctly interpreted the integrity of the teres minor insertion in all but one of the 11 specimens. In that one specimen, an apparent anechoic defect with echogenic foci thought to represent a tear, in actuality represented artifactual acoustic shadowing secondary to the ice crystals within the incompletely thawed muscle. This artifactual shadowing combined with fluid around the muscle secondary to the sham arthroscopic procedure led to a misdiagnosis of a tear. The artifact was correctly identified, when present, in all the subsequent specimens. The tears were readily identified in the longitudinal view along the muscle fibers. In the transverse plane, it was more difficult to identify a tear because the transducer was oriented parallel to the plane of the tear. We also found that repeated manual external and internal rotation of the arm assisted with visualization of the tear because it increased the gap between the torn tendon ends.

Our study has several limitations. First, the artificially created tears were easier to identify than naturally occurring tears because the torn tendon ends were often surrounded by water, making the tendon ends readily visible. The tears were also larger than naturally seen in the setting of a chronic degenerated teres minor. In addition, rather than evaluating all 11 rotator cuffs simultaneously with sonography before gross dissection, groups of two or three were imaged sequentially. Individual cuffs were then dissected after each arthroscopic procedure to confirm the sonography findings. This may have hastened the learning curve of the observers. Finally, the use of cadaveric specimens to study the sonographic appearance of the rotator cuff tears has not been validated. However, one experimental study [13] has shown that sonographic evaluation of cadaveric rotator cuffs was as accurate as MRI in detecting tears using the dissected anatomic specimens as the gold standard. There are also a number of studies in the literature that now show the reliability and utility of using cadaveric specimens to study sonographic appearance of tendons and ligaments [14–22]. Our results also validate the use of cadaveric specimens to study the rotator cuff with sonography.

In summary, we think that sonography is a rapid, noninvasive, and inexpensive adjunct to physical and standard radiographic examination of the teres minor. Our study confirms that radiologists can use sonography to accurately identify the normal and abnormal teres minor insertion. This verifies our clinical experience in which examination of the teres minor has been an integral part of our protocol for evaluating the rotator cuff for several years. There is increasing awareness about the importance of the teres minor for predicting outcome after shoulder reconstruction procedures. Our results show that sonography can be a valuable imaging technique for providing prognostic information before these procedures.

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited 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 Google Scholar Google Scholar Articles by Kim, H.-M. Articles by Yamaguchi, K. Search for Related Content PubMed PubMed Citation Articles by Kim, H.-M. Articles by Yamaguchi, K. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?