J Shoulder Elbow Surg (2012) 21, 867-872
www.elsevier.com/locate/ymse
The superior capsule of the shoulder joint complements the insertion of the rotator cuff Akimoto Nimura, MD, PhDa, Atsuo Kato, MDa, Kumiko Yamaguchi, MD, PhDa, Tomoyuki Mochizuki, MD, PhDb, Atsushi Okawa, MD, PhDc, Hiroyuki Sugaya, MD, PhDd, Keiichi Akita, MD, PhDa,* a
Unit of Clinical Anatomy, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan Department of Orthopedics, Kawaguchi Kogyo Hospital, Japan c Department of Orthopedic Surgery, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan d Shoulder and Elbow Service, Funabashi Orthopaedic Sports Medicine Center, Funabashi, Japan b
Background: To date, there are no studies about the attachment of the articular capsule of the superior shoulder joint. The aim of this study was to measure the width of the attachment of the articular capsule on the humerus, and to clarify the anatomy and the relationship to the footprint of the rotator cuff. Methods: The attachment of the articular capsule on the greater tuberosity was exposed. The width of the attachment of the capsule and the footprint of the rotator cuff were measured. Results: The maximum capsular width was located at the border between the infraspinatus and the teres minor, and measured 9.1 mm. The minimum capsular width was 3.5 mm, and it was located at 10.9 mm posterior to the anterior margin of the greater tuberosity and 1.5 mm anterior to the posterior margin of the supraspinatus. Conclusion: Prior studies have overestimated the rotator cuff footprint width due to the lack of discrimination between the actual cuff insertion and capsule. The attachment of the articular capsule of the shoulder joint occupied a substantial area of the greater tuberosity. In particular, at the border between the infraspinatus and the teres minor, the very thick attachment of the articular capsule compensated for the lack of attachment of muscular components. The thinnest point of the articular capsule was 11 mm posterior to the anterior margin of the greater tuberosity and very close to the posterior edge of the tapered insertion of the supraspinatus, which could contribute to the etiology of degenerative rotator cuff tears. Level of evidence: Basic Science Study, Anatomic Study. Ó 2012 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Shoulder joint; supraspinatus; infraspinatus; teres minor; articular capsule
IRB: Not applicable, Basic Science Study. This study was partly supported by Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports (C) (No. 20590168) and also supported by a grant from Nokyo Kyosai Research Institute (Agricultural Cooporative Insurance Research Institute). *Reprint requests: Keiichi Akita, MD, PhD, Unit of Clinical Anatomy, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. E-mail address:
[email protected] (K. Akita).
Tears of the rotator cuff, which frequently occur in elderly patients due to age-related degenerative changes and/or injury, can lead to dysfunction of the shoulder.3 Therefore, identification of the precise location and extent of the tear may be important to facilitate proper surgical treatment to restore function. Most anatomy textbooks and several anatomical studies have stated that the supraspinatus is inserted into the
1058-2746/$ - see front matter Ó 2012 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2011.04.034
868 highest impression of the greater tuberosity, and that the infraspinatus is inserted into the middle impression of the greater tuberosity.2,4-6,8,11 Recently, we re-evaluated the humeral insertions and tendinous structures of the supraspinatus and infraspinatus macroscopically using cadaver shoulders, and revealed that the footprint of the supraspinatus on the greater tuberosity is much smaller than previously described, and the footprint is actually occupied by a substantial amount of the infraspinatus.9,10 In the shoulder joint, the deepest layer of the rotator cuff is a thin continuous sheet of interwoven collagen fibrils, which is the capsule it extends from the glenoid labrum medially to the humerus laterally.1 Though the structure of the articular capsule of the shoulder joint is very sturdy and it is assumed to have functional significance, there has been no study that precisely refers to the function of the articular capsule. Previously, we reported that the width of the attachment of the articular capsule is 4.5 mm at the posterior edge of the footprint of the supraspinatus, which was impressive as it was wider attachment than previously thought.9 Given the fact described above, we hypothesized that the superior capsule had a substantial attachment area which might contribute to the etiology of the degenerative rotator cuff tears. The aim of this study was to measure the width of the attachment of the articular capsule on the humerus, and to clarify the detailed anatomy and the relationship to the footprint of the supraspinatus and the infraspinatus.
Materials and methods Twelve shoulders from 6 Japanese cadavers (2 males and 4 females; average age, 77.3 years old) were used in this study. All cadavers were fixed in 8% formalin and preserved in 30% ethanol. The entire scapula and the proximal third of the humerus and clavicle with soft tissues were obtained by cutting the humerus and clavicle. The skin, subcutaneous tissues, and deltoid muscle were removed from the shoulder. After resection of the acromion, the coracohumeral ligament and the connective tissues overlying the supraspinatus and infraspinatus were removed. After macroscopic observations of the muscular and tendinous fibers of the myotendinous cuff, the supraspinatus, infraspinatus, and teres minor were peeled away from their origin on the scapula toward their insertion on the tuberosity of the humerus, and reflected. The articular capsule was detached posteriorly from the anterior edge of the supraspinatus muscle, which is the same site as the lateral margin of the intertubercular groove, toward the teres minor. The articular capsule was removed and the attachment of the articular capsule on the greater tuberosity was exposed. We examined and measured the size of the footprint of the articular capsule, supraspinatus, and infraspinatus.
Results Humeral insertions of the supraspinatus, infraspinatus, and teres minor The supraspinatus and infraspinatus were inserted into the greater tuberosity (Fig. 1). The anteriormost region of the
A. Nimura et al. insertion of the infraspinatus nearly reached to the anterior margin of the greater tuberosity lateral to the insertion area of the supraspinatus muscle. The teres minor was inserted into the greater tuberosity inferior to the insertion of the infraspinatus. After reflections of the supraspinatus, infraspinatus, and teres minor, the articular capsule was observed. The teres minor was identified as a muscle with superior and inferior portions (Fig. 2). Though the supraspinatus, infraspinatus, and superior portion of the teres minor covered and attached to the articular capsule, the inferior portion of the teres minor was inserted into the humerus without covering the articular capsule (Fig. 2, B). The muscles were removed from the humerus, and footprints of the muscles were observed. The footprint of the supraspinatus was limited to the anteromedial area and that of the infraspinatus occupied the area lateroposterior to that of the supraspinatus (Fig. 3). The superior portion of the teres minor had a round-shaped attachment inferior to the attachments of the infraspinatus. In addition, the inferior portion of the teres minor had a line-shaped attachment (Fig. 3, B).
Humeral attachment of the superior capsule of the shoulder joint The articular capsule was reflected posteriorly and the attachment of the articular capsule on the greater tuberosity was exposed. The attachment of the articular capsule occupied a substantial area of the greater tuberosity (Fig. 4). Near the anterior edge of the supraspinatus and posterior edge of the infraspinatus, the articular capsule had a relatively thick footprint. In particular, at the border between the infraspinatus and teres minor, the very thick attachment of the articular capsule compensated for the lack of tendinous insertion.
Measurement of the footprints of the supraspinatus and infraspinatus tendons and the attachment of the articular capsule We measured the width (medial to lateral) of the attachment of the articular capsule and the footprint of both the supraspinatus and infraspinatus at various sites (Fig. 5; Table). At the anterior margin of the greater tuberosity, the average width of the attachment of the capsule (C1 in Fig. 5) was 5.6 mm (standard deviation [SD], 1.6 mm) and that of the footprint of the rotator cuff tendon (R1 in Fig. 5) was 3.5 mm (SD, 2.3 mm). At the posterior margin of the supraspinatus, the average width of the attachment of the articular capsule (C3 in Fig. 5) was 4.4 mm (SD, 1.2 mm) and that of the footprint of the rotator cuff tendon (R3 in Fig. 5) was 7.6 mm (SD, 1.9 mm). At the point of the maximum width of the infraspinatus, the average width of the attachment of the articular capsule (C4 in Fig. 5) was 5.4 mm (SD, 1.4 mm) and that of the footprint of the rotator cuff tendon (R4 in Fig. 5) was 9.7 mm (SD, 1.7 mm). At the posterior margin of the infraspinatus,
The superior capsule complements the insertion of rotator cuff
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Figure 1 Muscular and tendinous structures of the supraspinatus, infraspinatus, and teres minor near their insertions into the greater tuberosity (right shoulder, the acromion has been removed). After removal of the overlying connective tissues, the superior margin of the infraspinatus (white arrowheads) is clearly observed. (A) Superior aspect of the shoulder. (B) Lateral aspect of the shoulder. CP, coracoid process; ISP, infraspinatus; SS, scapular spine; SSP, supraspinatus; TMi, teres minor; Ant, anterior; Med, medial; Sup, superior; Post, posterior.
Figure 2 The articular capsule after detachment of the supraspinatus, infraspinatus, and teres minor and reflection from the humerus. (A) Superior aspect of the shoulder. (B), Posterior aspect of the shoulder. CAP, articular capsule; CP, coracoid process; ISP, infraspinatus; SS, scapular spine; SSP, supraspinatus; TMi-T, tendinous portion of the teres minor; TMi-M, muscular portion of the teres minor; Ant, anterior; Lat, lateral; Sup, superior.
the average width of the attachment of the articular capsule (C5 in Fig. 5) was 9.1 mm (SD, 1.4 mm). At the point of the minimum width of the articular capsule, the average width of the attachment of the articular capsule (C2 in Fig. 5) was 3.5 mm (SD, 0.8 mm) and that of the footprint of the rotator cuff tendon (R2 in Fig. 5) was 8.1 mm (SD, 2.0 mm). The distance from anterior margin of the greater tuberosity to the point of minimum width of the articular capsule along the lateral border of the articular cartilage (D1 in Fig. 5) was 10.9 mm (SD, 3.1 mm). The distance from the point of minimum width of the articular capsule to the posterior margin of the supraspinatus along the lateral border of the articular cartilage (D2 in Fig. 5) was 1.5 mm (SD, 2.7 mm).
Discussion The articular capsule of the shoulder joint had been recognized as merely a thin membranous structure between the rotator cuff and the joint space. To our knowledge, there
has been no study referring to the details of the attachment of the articular capsule of the superior shoulder joint. We previously measured only the width of the articular capsule as 4.5 mm at the posterior edge of the supraspinatus footprint.9 In the present study, we found that the attachment of the articular capsule occupied a substantial area of the greater tuberosity. Near the anterior edge of the supraspinatus and the posterior edge of the infraspinatus, the articular capsule attached with a relatively thick footprint. In particular, at the posterior margin of the infraspinatus, the width of the capsule attachment was >9 mm. On the other hand, in the middle area of the rotator cuff footprint near the posterior margin of the supraspinatus, the articular capsule had a relatively thin attachment. Some anatomical papers have referred to footprints of the supraspinatus and infraspinatus. Minagawa et al described only the maximum anterior-posterior width of the footprint of the supraspinatus and infraspinatus at the medial margin of the greater tuberosity of the humerus, but they did not include data on the medial-lateral width.8
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Figure 3 The insertion area of the supraspinatus, infraspinatus, and teres minor. These tendons were removed from the humerus. The area outlined by black dotted lines indicates the insertion area of the supraspinatus (star), infraspinatus (circle), tendinous portion (square), and muscular portion of the teres minor (arrowheads). (A) Superior aspect of the shoulder. (B) Posterior aspect of the shoulder. CAP, articular capsule; CP, coracoid process; SS, scapular spine; Ant, anterior; Lat, lateral; Sup, superior.
Figure 4 The attachment area of the articular capsule. The articular capsule has been removed from the humerus. The area outlined by white dotted lines indicates the attachment area of the articular capsule. The area outlined by black dotted lines indicates the insertion area of the supraspinatus (star), infraspinatus (circle), tendinous portion (square), and muscular portion of the teres minor (arrowheads). (A) Superior aspect of the humerus. (B) Posterior aspect of the humerus. HH, humeral head; Ant, anterior; Lat, lateral; Sup, superior.
Dugas et al reported that the mean medial-lateral width of the supraspinatus insertion was 1.27 cm and that of the infraspinatus was 1.34 cm.5 Ruotolo et al stated that the mean medial-lateral width of the supraspinatus at the rotator interval was 11.6 mm, 12.1 mm at mid-tendon, and 12 mm at the posterior edge.11 Curtis et al reported that average maximum width of the insertion of the supraspinatus was (medial to lateral) 16 mm and that of the infraspinatus was 19 mm.4 However, they had not dissected the rotator cuff tendon from the articular capsule, and thus might have measured the mixed construct of the tendon and capsule as the footprint of the rotator cuff. These previous data on the medial-lateral width of the insertion of the rotator cuff tendon are nearly compatible with our data regarding the sum of the articular capsule attachment and rotator cuff tendon insertion. This compatibility can be explained by the fact that the articular capsule had been thought to be a thin and minor structure, and therefore, the presence of the capsule attachment on the greater tuberosity had been neglected. Based on the present study, the articular capsule was shown to attach to the greater tuberosity with a thicker footprint than previously thought.
Based on the present study, the thinnest point of the capsule attachment was located 11 mm posterior to the anterior margin of the greater tuberosity along the articular cartilage border. At this point, the posterior edge of the supraspinatus insertion was very close and the infraspinatus inserted with a relatively thick attachment. In ultrasonogram assessment of 360 shoulders with a rotator cuff tear, Kim et al7 previously showed that degenerative rotator cuff tears most commonly involve a region 13-17 mm posterior to the biceps tendon. This region was near the thinnest point of the articular capsule and the tapered insertion of the supraspinatus in the present study. If the thinnest point of the articular capsule attachment and supraspinatus insertion are hypothesized as mechanically being the most fragile area, it follows that it may be related to the initiation of degenerative rotator cuff tears. On the other hand, based on the present results, at the inferior margin of the infraspinatus where no muscular components are attached, the articular capsule had the thickest attachment. Given the fact that the articular capsule might functionally complement the insertion of the rotator cuff tendon and facilitate maintenance for the endurance of
The superior capsule complements the insertion of rotator cuff
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Figure 5 Illustrations indicating the measurement of the footprints of the supraspinatus and infraspinatus tendons and the attachment of the articular capsule of the right shoulder. (A) Superior aspect of the humerus. (B) Posterior aspect of the humerus. Red double-headed arrows indicate the width of the attachment of the articular capsule. Blue double-headed arrows indicate the width of the footprint of the rotator cuff tendon. GT, greater tuberosity; LT, lesser tuberosity; HH, humeral head; C1, width of the attachment of the articular capsule at the anterior margin of the greater tuberosity; C2, minimum width of the attachment of the articular capsule; C3, width of the attachment of the articular capsule at the posterior margin of the supraspinatus; C4, width of the attachment of the articular capsule at the point of the maximum width of the infraspinatus; C5, width of the attachment of the articular capsule at the posterior margin of the infraspinatus; T1, width of the footprint of the supraspinatus at the anterior margin of the greater tuberosity; T2, width of the footprint of the supraspinatus and infraspinatus at the point of the minimum width of the articular capsule; T3, width of the footprint of the infraspinatus at the posterior margin of the supraspinatus; T4, maximum width of the footprint of the infraspinatus; D, distance from anterior margin of the greater tuberosity to the point of minimum width of the articular capsule. Table
Measurement of the attachment of the articular capsule and the footprint of the rotator cuff
The location of the measurement Supraspinatus Anterior margin of the greater tuberosity Posterior margin of the supraspinatus Infraspinatus Maximum width of the infraspinatus Posterior margin of the infraspinatus Minimum width of the articular capsule Distance from anterior margin of the greater tuberosity to the point of minimum width of the articular capsule Distance from the point of minimum width of the articular capsule to posterior margin of the supraspinatus
Average width and standard deviation (mm) Articular capsule
Rotator cuff tendon
C1: 5.6 1.6 C3: 4.4 1.2
R1: 3.5 2.3 R3: 7.6 1.9
C4: 5.4 1.4 C5: 9.1 1.7 C2: 3.5 0.8
R4: 9.7 1.7 D1: 10.9 3.1
R2: 8.1 2.0
D2: 1.5 2.7
Locations of measurements are demonstrated in Figure 5.
the rotator cuff footprint, knowledge on the attachment of the superior capsule of the shoulder joint contributes as a basis for the development of new concepts for the treatment of rotator cuff tears.
Conclusion Prior studies overestimated the rotator cuff footprint width, as they did not discriminate between the actual
cuff insertion and the capsule. The attachment of the articular capsule of the shoulder joint occupied a substantial area of the greater tuberosity. In particular, at the border between the infraspinatus and teres minor, the very thick attachment of the articular capsule compensated for the lack of the tendinous insertion. The thinnest point of the articular capsule was 11 mm posterior to the anterior margin of the greater tuberosity and very close to the posterior edge of the tapered insertion of the supraspinatus, which could contribute to
872 the etiology of the initiation of degenerative rotator cuff tears.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
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