Fig. 1
Directions of vector line of deltoid, supraspinatus, subscapularis
Activity
To define the activity or contraction of a muscle, it is necessary to consider the motion and position of the shoulder joint. Muscles permitting shoulder motion were defined by Duchenne by means of electric stimuli [16]. Recently, electromyography (EMG) has redefined the activity of all scapular muscles [17–21]. Ackland and Pandy [22] have shown that internal rotation is caused by contraction of the lower portion of the subscapularis; on the contrary, the lower part of the infraspinatus and teres minor are the most important external rotators. The supraspinatus acts as external rotator during abduction and as internal rotator during flexion of the arm. These same authors suggest that it is possible to understand the effect of a cuff tear if the lever arm of the submuscular regions is defined [22]. In addition, in another study, the authors have concluded that a further subdivision of rotator cuff muscles in multifeathered bundles may provide evidence of differences in activity that depend on the position of the shoulder joint [23].
Rotator Cuff Tendon Function in Gleno-Humeral Motion
Supraspinatus
This muscle originates from the supraspinatus fossa of the scapula and ends on the greater tuberosity of the humerus, with a footprint much smaller than that believed in the past [24]. In fact, its footprint occupies a very restricted area of the greater tuberosity, while the infraspinatus and subscapularis fibers are interested in the remaining area. On the basis of this new information, it is possible to understand why the supraspinatus tendon during external rotation is much less important than it was believed to be in the past, with much more relevant flexion/abduction functions [11]. Nevertheless, the function of the whole muscle-tendon unit is still a matter of discussion [25–33]. The supraspinatus, cooperating with the deltoid and other cuff muscles, performs an important function in the flexion of the arm [25]. These observations are confirmed by Liu et al. [25], who proposed to strengthen the rotator cuff and other peri-scapular muscle in case of rotator cuff tear. In addition, literature evidences that a cuff tear causes scapular dyskinesis [34]. Several rehabilitation programs have been proposed, all of them focusing on strengthening and stretching the scapular muscles availing of exercises aimed at improving scapular protraction, retraction, depression, elevation, and rotation [34–36]. Even these exercises should be considered during rehabilitation after repair of rotator cuff and other shoulder pathologies related to scapular malposition and dyskinesis [37].
The functional relation between deltoid and supraspinatus has been described by Sharkey [31]. When the deltoid function is not working properly, there is a uniform reduction of strength during flexion and abduction, whatever position the joint may assume. On the other hand, when the cuff function is not working, strength in the first few degrees of flexion/abduction remains normal, while there is an important deficit beyond 30° of flexion/abduction (Fig. 2).
Fig. 2
Relative contribution of deltoid and supraspinatus to flexion and abduction of the arm
Later, the relation between deltoid and supraspinatus was reviewed. Thompson et al. [27] showed that in cases of paralysis of the supraspinatus, the strength of the lateral deltoid necessary needs to increase to 101 %; furthermore, it is necessary to obtain an increase of 12 % to achieve complete abduction, showing that the supraspinatus is an important abduction trigger. Howell et al. [14] have studied dynamometric data concerning abduction in subjects presenting a lidocaine block of the axillary or supraspinatus nerve. They experienced an equivalent decrease in flexion/abduction strength if the supraspinatus or deltoid were inactivated. These data were confirmed by the clinical experiences of Markhede et al. [28], who observed that patients devoid of deltoids enjoyed good overall functionality of the shoulder. On the contrary, Oh et al. [29] argued that when the supraspinatus is completely detached from its footprint, shoulder flexion/abduction is very limited; when the tendon tear involves the infraspinatus too, the global kinematic of the shoulder changes. In addition, in the presence of a larger tear, the pectoralis major and the latissimus dorsi improve the function which permits them to stabilize the humeral head in the glenoid fossa. Wuelker et al. [30] observed that when the supraspinatus is completely torn, the deltoid improves its function and it is able to guarantee the strength of the shoulder even if it is much weaker than the supraspinatus, availing of only one-third of its strength. These authors also affirm that the supraspinatus has a less effective flexile function than the deltoid. Itoi et al. [33] studied the isokinetic strength of shoulders with an isolated tear of the supraspinatus and observed that the overall strength of the shoulder is reduced to two-thirds of the initial value. The latter data reflect the effective contribution made by the supraspinatus to shoulder strength. Harris and colleagues studied a cohort of patients treated conservatively for rotator cuff tear and concluded that it is possible to obtain a functional and asymptomatic shoulder if scapular dyskinesis is treated with specific exercises to strengthen flexion and abduction [38].
The Infraspinatus and Teres Minor
In literature, the infraspinatus and teres minor are often considered together, especially as far as biomechanics is concerned [12, 30, 32, 39]. These studies, except for the review by Longo and colleagues “Biomechanics of the rotator cuff” [32], precede new anatomic concepts by Mochizuchi et al. [24], who have observed that the footprint of the infraspinatus is much wider than it was believed in the past and that this tendon is always torn considerably in the presence of postero-superior cuff tears. With the arm at rest, the supra- and infraspinatus act as external rotator and flexor/abductor [39]; the functions are also the same with the arm in other positions. In particular, the infraspinatus and teres minor flexor function was shown by Sharkey et al. [39]. The authors highlighted the fact that when the supraspinatus is functioning, the deltoid strength necessary to permit forward elevation of the arm decreases to 72 %, to 64 % when the infraspinatus and teres minor are functioning, and to 41 % when all rotator cuff muscles are functioning. Otis et al. [15] showed that the infraspinatus acts more as an abductor when the arm rotates internally, while during external rotation the subscapularis assumes this function. Furthermore, the infraspinatus and teres minor are of crucial importance as depressors of the humeral head [30–32]. In fact, tears extending to the postero-superior cuff are associated with a greater upward migration of the humeral head and bear a direct relationship with the size of the tear [31]. This depressor function has been confirmed by Su et al. [40], who have studied the lower part of the infraspinatus as the most important depressor. The role of the long head of the biceps tendon as depressor has to be revised, as Gumina and colleagues [41] pointed out in a study including a 30-year follow-up.
The Subscapularis
The subscapularis muscle originates from the anterior aspect of the scapula and ends mostly in the lesser tuberosity of the humerus, while a small portion ends in the greater tuberosity [24]. Besides other cuff tendons, the classical interpretation of the subscapularis as internal rotator needs to be revised/re-evaluated/re-examined. Internal rotation remains its main function, of course, while its secondary roles change depending on the position of the humeral head with respect to the scapula. Consequently, this tendon is an abductor, a flexor, an extensor, and a depressor [42]. Because of the shared insertion of the supraspinatus and subscapularis, it is possible that in certain positions of the arm, the subscapularis may work as external rotator [12, 15, 24].
Because of its broad medial insertion, the muscle-tendon unit was studied in different areas with different functions. In 1989, Kato studied the subscapularis of 40 cadavers and identified three different branches: the upper, midway, and lower [43]. Kadaba et al. [44], on the contrary, found two parts: the upper and lower, with separate innervations. The authors examined the electromyographic activity of the two portions during isometric contraction during internal rotation with the arm at 0° and 90° of abduction [44]. The main result of the study is that abduction influences the activity of the two parts of the deltoid [44]. Otis et al. [15] subdivided the subscapularis into three portions (Fig. 3) and found that the upper part acts prevalently as flexor. Recently, the subscapularis was found to enhance its function and muscle thickness in cases of postero-superior cuff tear in order to rebalance the biomechanics of the shoulder [45]. The function of the subscapularis as flexor/abductor is still a matter of discussion. In the past, Poppen and Walker [13] pointed out that the main function of the subscapularis was not to flex the arm. Gerber et al. [46], studying a cohort of 16 patients with a tear in the upper subscapularis, experienced a flexion strength deficit. In a recent paper, Itoi and colleagues studied the metabolism of the subscapularis after flexion exercises of the arm and found it had increased; it was not clarified whether this muscle is a simple flexor of the arm or if it stabilizes the gleno-humeral joint in cooperation with other muscles [47]. Recently, it emerged that during flexion electromyographic activity increases much more for the subscapularis than for other cuff muscles [48]. Furthermore, Kuechle et al. [11] have shown that the subscapularis is a more important flexor than the supra- and infraspinatus.
Fig. 3
The three different portions of the subscapularis muscle (SSC-S; SSC-M; SSC-I)
Because of its forward position, a subscapularis tear cannot be balanced by the remaining tendons. In 2009, Su et al. [49] pointed out that a superior cuff tear including the upper third of the subscapularis alters the biomechanics of the shoulder significantly and causes antero-superior subluxation of the humeral head. Rotator cuff cable integrity, as described by Burkart et al. [50], is essential to the biomechanics of the shoulder. If preserved, the lower part of the subscapularis suffices to guarantee normal biomechanics of the shoulder. Rupture of the entire tendon alters the biomechanics of any situation. Upper fibers enhance abduction, lower ones adduction [51]. Anteriorly, the subscapularis muscle stabilizes the shoulder joint actively and passively during external and internal rotation. On the axial plane, the muscle-tendon unit balances the activity of the infraspinatus, while on the coronal plane it opposes the upward migration caused by deltoid activity.
Rotator Cuff Function in Gleno-Humeral Stability
The contact area between the glenoid and humeral head articular surface is relatively limited. The capsule, gleno-humeral ligaments, and the labrum make the congruity and the contact area more efficient (static stability). Most of the stabilizing effect of the gleno-humeral joint is due to muscles surrounding the shoulder (dynamic stability). Rotator cuff tendons and muscles, in particular, acting as dynamic stabilizers, favor shoulder stability, thanks to their position and orientation with respect to the joint [52] (Fig. 4).
Fig. 4
Compression of the humeral head in the glenoid fossa
The rotator cuff, together to other shoulder girdle muscles, makes the joint stable during its entire range of movement. Muscles and ligaments have to balance out low articular surface congruity, providing a more important function compared to other joints endowed with greater congruity efficiency. The dynamic stability of the joint is also the result of neuromuscular synchronism between scapula-thoracic and rotator cuff muscles. The scapula-thoracic muscles favor neural feedback from rotator cuff muscles and gleno-humeral ligaments while helping to prevent pathological subluxation of the joint [52]. This neural feedback causes a rapid and efficient proprioceptive response of the shoulder muscles, thus improving shoulder stability [53].