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The etiology of rotator cuff tendinopathy is multi-factorial, and has been attributed to both extrinsic and intrinsic mechanisms. Extrinsic factors that encroach upon the subacromial space and contribute to bursal side compression of the rotator cuff tendons include anatomical variants of the acromion, alterations in scapular or humeral kinematics, postural abnormalities, rotator cuff and scapular muscle performance deficits, and decreased extensibility of pectoralis minor or posterior shoulder. A unique extrinsic mechanism, internal impingement, is attributed to compression of the posterior articular surface of the tendons between the humeral head and glenoid and is not related to subacromial space narrowing. Intrinsic factors that contribute to rotator cuff tendon degradation with tensile/shear overload include alterations in biology, mechanical properties, morphology, and vascularity. The varied nature of these mechanisms indicates that rotator cuff tendinopathy is not a homogenous entity, and thus may require different treatment interventions. Treatment aimed at addressing mechanistic factors appears to be beneficial for patients with rotator cuff tendinopathy, however, not for all patients. Classification of rotator cuff tendinopathy into subgroups based on underlying mechanism may improve treatment outcomes.
). Randomized trials suggest that the short and long-term outcomes of patients with RC tendinopathy treated with surgery are comparable to conservative treatment that includes exercise or exercise combined with a multimodal rehabilitation program (
Arthroscopic surgery versus supervised exercises in patients with rotator cuff disease (stage II impingement syndrome): a prospective, randomized, controlled study in 125 patients with a 2 1/2-year follow-up.
Arthroscopic surgery versus supervised exercises in patients with rotator cuff disease (stage II impingement syndrome): a prospective, randomized, controlled study in 125 patients with a 2 1/2-year follow-up.
). Given the high prevalence and continued pain despite treatment in patients with RC disease, research to better understand the mechanisms to improve effectiveness of treatment, guide specific treatment choices, and better prognosticate treatment outcomes is necessary.
RC disease has been classically described as a progressive disorder of the RC tendons which begins with an acute tendinitis, progresses to tendinosis with degeneration and partial thickness tears, and results in full thickness rupture (
). The diagnostic terms of RC tendinitis and tendinosis represent tendon pathology subsets of RC tendinopathy. RC tendinitis is often used to define both acute and chronic pain associated with, by definition, inflammation. However, histological studies of patients with RC disease have found minimal to no inflammatory cells in the RC tendons (
). Tendinosis is the diagnostic label for tendon pathology that is degenerative with or without inflammation. In contrast, RC tendinopathy is used to signify a combination of pain and impaired performance associated with RC tendons (
). The focus of this review is RC tendinopathy which includes external or internal impingement, tendinitis, tendinosis with degeneration and partial thickness tendon tears. Full thickness tendon tears are unique and beyond the scope of this review.
Mechanisms of RC tendinopathy have been classically described as extrinsic, intrinsic or a combination of both. Extrinsic factors are defined as those causing compression of the RC tendons, while intrinsic mechanisms are those associated with degeneration of the RC tendon. Neer proposed an extrinsic mechanism to the etiology RC tendinopathy with compression of the RC tendons and associated tissues within the subacromial space under the anterior aspect of the acromion or surrounding structures (
). The diagnosis of “subacromial impingement” inherently implies an extrinsic compression mechanism due to narrowing of the subacromial space, which may not accurately represent all RC tendon pathology. A unique extrinsic mechanism, internal impingement, has been described particularly in overhead athletes (
). Internal impingement occurs due to compression of the articular side rather than the bursal side of the RC tendons, between the posterior superior glenoid rim and humerus when the arm is in full external rotation, abduction, and extension (
). Although internal impingement can be considered an extrinsic mechanism, narrowing of the subacromial space is not a hallmark finding. In contrast to extrinsic mechanisms of RC tendinopathy, Codman postulated an intrinsic mechanism due to degeneration within the tendon (
). Fig. 1 illustrates the mechanisms and the relationships of the varied mechanisms of RC tendinopathy. Despite the debate over the pathogenesis, evidence indicates that the etiology of RC tendinopathy is multi-factorial and likely both intrinsic and extrinsic mechanisms play a role (Table 1).
Table 1Rotator cuff pathological mechanisms.
Degeneration of the tendon where tensile loading exceeds the tendon's intrinsic healing and adaptive responses
Compression of the tendon within the subacromial space from anatomical or biomechanical abnormalities
Compression of the tendon posteriorly between the humerus and glenoid rim
Intratendinous and articular-sided tendon pathology without coracoacromial abnormalities
Bursal-sided tendon pathology with coracoacromial abnormalities more common
Articular-sided pathology without coracoacromial abnormalities. May be related to glenohumeral joint instability.
1. Extrinsic mechanisms of rotator cuff tendinopathy
Extrinsic mechanisms of RC tendinopathy that result in bursal-sided RC tendon compression due to narrowing of the subacromial space include anatomical factors, biomechanical factors, or a combination. The subacromial space is the interval between the coracoacromial arch, anterior acromion and the humeral head (
). The acromiohumeral distance (AHD), a linear measure between the acromion and the humeral head used to quantify the subacromial space, has been studied in patients with RC disease using magnetic resonance imaging (MRI) (
). Further research that examines changes in subacromial space with active arm elevation in patients with RC tendinopathy is advocated and may be useful to identify the presence of an extrinsic mechanism influencing the articular side of the RC tendons.
1.1 Anatomical factors
Anatomical factors that may excessively narrow the subacromial space and outlet to the RC tendons include variations in shape of the acromion (
). Bigliani et al. described the role of the shape of the acromion as an extrinsic mechanism of RC tendinopathy by describing the morphologic condition of the acromion as a Type I (flat), Type II (curved), or Type III (hooked) (
). Similarly, other anatomical factors like large subacromial spurs, thickening or ossification of the attachment of the coracoacromial ligament (CAL) are associated with RC pathology with bursal-sided partial thickness tears (
There is substantial evidence that anatomical variants such as subacromial spurs, AC joint spurs, and acromial shape may contribute biomechanically to an extrinsic mechanism of RC tendinopathy and progressive RC disease; however, the presence of these alone may be insufficient to result in RC tendinopathy.
) found that external mechanical compression of RC tendons in rats exposed to normal cage activity did not cause pathological changes, but when combined with overuse activity had a significant effect on tendon injury. Therefore, bony anatomy such as a hooked acromion may not necessarily cause, but predispose an individual to RC tendinopathy. Supporting this theory of a requisite overuse exposure, symptomatic RC disease is more often present in dominant than non-dominant shoulders (
Biomechanical factors that can lead to extrinsic mechanical RC tendon compression include abnormal scapular and humeral kinematics, postural abnormalities, rotator cuff and scapular muscle performance deficits, and decreased extensibility of pectoralis minor or posterior shoulder tissues. Scapular and humeral kinematic abnormalities can cause dynamic narrowing of the subacromial space leading to RC tendon compression secondary to superior translation of the humeral head (
) compared to healthy subjects. As a result, the anterior aspect of the acromion may fail to move away from the humeral head during arm elevation and in theory contribute to a reduction of subacromial space and external RC compression (
). In contrast, increased scapular posterior tilting, upward rotation, and superior translation of the scapula have also been identified in patients with RC tendinopathy compared to asymptomatic subjects (
). While variable patterns of abnormal scapular kinematics in patients with RC tendinopathy have emerged, the differences between groups are small in magnitude which casts doubt upon the significance of these findings related to changes in subacromial space and role of abnormal scapular kinematics as an extrinsic mechanism for all patients with RC tendinopathy.
Interestingly, Graichen et al. suggest that not all patients with RC tendinopathy have altered scapular kinematics, but a subset exists with significant alterations that are greater than 2 standard deviations from the mean of healthy individuals (
) compared to less obvious, or subtle, alternations may have meaningful abnormal scapular kinematics that impacts the subacromial space and contribute to an extrinsic mechanism of RC tendinopathy. Silva et al. found a greater reduction in subacromial space in elite tennis players with scapular dyskinesis compared to players without dyskinesis (
); however, the clinical method used to identify scapular dyskinesis and associated reliability was not reported.
While there is evidence of abnormal scapular kinematics in a subset of patients with RC tendinopathy, the influence of these specific biomechanical alterations on subacromial space remains speculative. Alternatively, passive alterations in scapular position may influence subacromial space (
). In a study by Atalar et al., limiting scapular motion by externally binding the scapular down to the thorax while the arm is positioned at 90° compared to unrestricted scapula caused a reduction in subacromial space in healthy individuals (
). Further research is necessary to determine which scapular kinematic alterations are most related to changes in subacromial space and the magnitude of change in scapular kinematics needed to affect the subacromial space.
The mechanisms responsible for scapular alterations found in subjects with RC tendinopathy have not been clearly defined, but have been theorized to include adaptive shortening of the pectoralis minor muscle (
). Subjects with a relatively shorter pectoralis minor muscle length at rest demonstrate increased scapular internal rotation during arm elevation and decreased scapular posterior tilting at higher arm elevation angles (90° and 120°) when compared with subjects with a relatively longer pectoralis minor muscle length at rest (
). Similarly, overhead athletes with a loss of glenohumeral internal rotation of 20% or more as compared to their opposite shoulder demonstrate increased scapular anterior tilt at end range glenohumeral internal rotation with the arm abducted or flexed to 90° (
). Of particular interest are the relative contributions of the upper and lower serratus anterior muscles and trapezius muscles, found to stabilize the scapula and induce scapular upward rotation, external rotation, and/or posterior tilt (
). Relatively small changes in the muscle performance of the scapulothoracic muscles can alter the position of the scapula at a fixed angle of humeral elevation and, in theory, affect the length–tension relationship (point on the length–tension curve) of the RC muscles and the subacromial space.
Thoracic spine kyphosis posture has been directly linked to alterations in subacromial space (
1.2.2 Humeral kinematics and influence of posture muscle deficits, and soft tissue tightness
Excessive humeral head migration proximally on the glenoid is theorized to reduce subacromial space and contribute to RC tendon compression. Proximal, or superior, humeral migration and reduction of subacromial space have been used synonymously at times; however, the amount of superior displacement of the humeral head has not been correlated with linear measures or the 3D volume of the subacromial space and may not occur at a 1:1 ratio (refer to Fig. 2). This distinction may be futile in patients with a large RC tendon tears who present dramatic excessive proximal humeral migration with the arm at rest (
). The extent of subacromial space narrowing that occurs with superior humeral head translation on the glenoid may be counteracted with scapular rotation that moves the acromion superiorly or posterior which may increase the subacromial space. Furthermore, a combination of aberrant humeral and scapular kinematics could cause a clinically meaningful reduction of the subacromial space. This relationship requires further study.
Proximal migration of the humerus on the glenoid while the arm is at rest is regarded as a sign of advanced RC disease (
). Similar to subacromial space, patients with RC tendinopathy do not exhibit proximal humeral migration on the glenoid with the arm at rest; but rather demonstrate excessive superior–anterior translations of the humeral head with active arm elevation (
) with active arm elevation compared to asymptomatic subjects. Biomechanical mechanisms for excessive proximal humeral migration in patients with RC tendinopathy include shortening of the posterior–inferior glenohumeral joint capsule and decreased RC muscle performance.
Decreased posterior capsule length has been directly linked to excessive anterior–superior humeral translation in cadaveric study (
) that potentially assess posterior capsule length. Content validity for IR ROM has been demonstrated in cadaveric study with a reduction of motion after the posterior–inferior capsule was artificially shortened (
). Clinical measures of glenohumeral internal rotation and horizontal adduction range of motion may also be influenced by potential adaptations of the infraspinatus, teres minor, and/or posterior deltoid musculature (
). Although more recently, the concept that decreased RC muscle performance alone can result in proximal humeral migration has been challenged with an in vivo study. Artificially induced paralysis of the supraspinatus and infraspinatus muscles in 10 healthy individuals resulted in no immediate effects on proximal humeral head translation (
). Results of this study suggest that time, or duration of the muscle impairment may also be a factor. Significant decreases in RC muscle peak isometric, concentric, and eccentric torque have been demonstrated in patients with RC tendinopathy compared to asymptomatic subjects (
). Reddy et al. found a decrease in electromyographic (EMG) activity of the infraspinatus, and subscapularis from 30° to 60° of active elevation and in the infraspinatus muscle alone from 60° to 90° of active elevation in subjects with tendinopathy compared to healthy subjects (
). However, alterations in muscle activity were also found in the asymptomatic side leading the authors to propose alterations in muscle activity are a factor in the pathogenesis not a result of RC tendinopathy. Lastly, Myers et al. found a decrease in co-activation ratios of the subscapularis–infraspinatus and supraspinatus–infraspinatus muscles with arm elevation from 0 to 30°, and an increase at elevation above 90°in patients with impingement compared to control participants (
). Biomechanical consequences of altered RC muscle activity may be an extrinsic mechanism of RC tendinopathy as superior migration may narrow the subacromial space or result in altered stress and intrinsic tendon degradation. Diminished RC muscle performance correlates with patient-rated function and health-related quality of life in patients with RC tendinopathy (
No study has concurrently examined the influence of scapular position on RC muscle activity in patients with RC tendinopathy; however, there is evidence to suggest that a change in scapular position can alter muscle performance (
). Kebaetse et al. found a decrease in isometric abduction muscle force with the arm at 90° concurrent with an increase in scapular anterior tilt in healthy subjects actively assuming a slouched trunk posture compared to an erect posture (
), with an increase noted with reposition and conflicting results with scapular retraction. Changes in muscle force may be due to improved proximal stability or alterations in RC muscle length at the same humeral elevation angle.
2. Extrinsic mechanisms for the subgroup of internal impingement
A unique subset of RC tendinopathy with an extrinsic mechanism is internal impingement. Patients with internal impingement tend to present with pain located in the posterior and superior aspects of the shoulder typically while the arm is in abduction and external rotation of the late cocking phase of throwing (
). In this position, the articular aspect of the RC tendons becomes mechanically impinged between the posterior superior glenoid rim and the humeral head. This is accentuated with further hyperangulation of the humerus to the glenoid with anterior glenohumeral joint instability (
). Alterations in scapular kinematics were found in a cohort of baseball players with internal impingement, confirmed with arthroscopy, of greater scapular posterior tilt compared to age matched healthy baseball players (
), but may be a result of differences in underlying mechanism. Further study should examine potential differences in mechanisms of this unique subgroup of RC tendinopathy.
3. Intrinsic mechanisms of rotator cuff tendinopathy
There is a growing body of evidence to support an intrinsic mechanism. Intrinsic mechanisms of RC tendinopathy influence tendon morphology and performance. Intrinsic factors of RC tendinopathy result in tendon degradation due to the natural process of aging (
). Furthermore, RC tendinopathy with an intrinsic mechanism may lead to a reduction in subacromial space creating an interaction of intrinsic and extrinsic mechanisms.
The morphology of the RC tendons has been studied in detail. The RC tendon near their insertions have been shown to interdigitate; specifically, the supraspinatus tendon consists of five axial plane layers from the bursal to articular side (
). RC tendinopathy can include symptomatic tendon pathology with degeneration and partial thickness tears that extend through several, but not all layers. It is commonly described as occurring in 3 regions: bursal sided, mid-substance, and articular sided. Furthermore, pathology that occurs within the mid-substance and articular-sided layers without bursal-side involvement is further support for the intrinsic mechanisms of RC tendinopathy (
described RC disease as a continuum of pathology with 3 stages characterized by age: less than 25 years for stage I, between 25 and 40 years for stage II, and greater than 40 years of age for stage III respectively. Although Neer's theory is biased by an extrinsic mechanism, age was included as an important factor for RC disease. The prevalence of tendon degeneration including partial and full thickness tears increases as a function of age starting at 40 years (
Age has been shown to have a negative impact on tendon properties. Evidence from biomechanical studies suggest that there is a reduced toe region of a stress–strain curve, decreased elasticity, and decreased overall tensile strength of tendons with age (
). Histological study of RC tendons have shown calcification and fibrovascular proliferation degenerative changes in elderly subjects without history of shoulder ailments that were not present in younger subjects, both without a history of shoulder ailments (
). There is no consensus whether changes in the tendon are primarily due to aging or a secondary consequence of reduced mechanical properties that make the tendon more susceptible to injury with repetitive motion. Regardless, age related changes to the tendon appear to be a significant factor in the intrinsic pathoetiology of RC tendinopathy.
A deficient vascular supply of the human RC tendons has been implicated in the pathogenesis and mechanism of RC tendinopathy. Codman first described the ‘critical zone’, an area within the supraspinatus tendon approximately 1 cm from the insertion on the greater tubercle with decreased vascularity and the most common site for RC tendon injury (
). It is unclear whether this avascular condition is a cause of progressive tendinopathy or a consequence of a complete tear. In subjects with RC tendinopathy, imaging with laser or ultrasound color Doppler has been used to detect the presence of neovascularization in vivo (
). Levy et al. found subjects with acute RC tendinopathy (impingement without tear) had hypovascularity in the supraspinatus tendon compared to subjects without RC disease, while those with chronic RC tears had hypervascularity near the degenerative changes (
). The role of vascularity in the intrinsic mechanism of symptomatic RC tendinopathy has not been fully elucidated, however it does appear to be a factor that is influenced by and/or influences the extent and duration of tendon pathology.
3.3 Impact of alterations in tendon matrix on mechanical properties
The composition and organization of the tendon matrix dictate the morphology and mechanical properties of tendons. Tendons are composed of proteins, collagen, and cells referred to as tenocytes. Collagen fibers in tendons are composed predominately of type I molecules in tight and parallel fiber bundles and a small proportion (<5%) of type III collagen fibers that are thinner, weaker, and more irregularly arranged (
). Within the RC tendons of elderly samples, the distribution of collagen types has been shown to vary with greater proportion of type II and III collagen near the insertional fibrocartilagenous region compared to more proximal tendon (
). Since type III collagen fibrils are considered more extensible than type I fibers and tend to be more irregularly arranged, authors theorized that the insertional region of the supraspinatus may be subjected to greater non-linear stresses than other RC tendons. In agreement with this theory, Lake et al. quantified the degree of collagen fiber alignment in different longitudinal sections of the supraspinatus tendon and demonstrated a highly inhomogeneous tissue with a relatively low degree of fiber alignment in the region near the tendon to bone insertion (
). These changes correlated with diminished mechanical properties in this region. Furthermore, histological evidence of inferior tissue organization, greater disorganization in the mid-substance and/or the articular side compared to more regularly arranged collagen on the bursal-side layers of the RC tendons has been proposed to weaken the tendon and precede complete tendon tear (
) in patients with chronic RC tendinopathy compared to cadaveric samples of normal tendon. Additionally, greater tenocyte apoptosis (cell death) has been found in tendons of patients with chronic RC tendinopathy as compared to normal tendons (
The effects of scapular taping on the surface electromyographic signal amplitude of shoulder girdle muscles during upper extremity elevation in individuals with suspected shoulder impingement syndrome.
). Cholewinski et al. found thinning of the RC tendons in patients with chronic unilateral (>6 months) subacromial impingement compared to an asymptomatic individuals without a history of shoulder injury (
In contrast, an accumulation of GAGs and disorganization of the collagen fibers, which is theorized to cause tendon thickening in RC tendinopathy, has been demonstrated within 12 weeks of the onset of injury (
) found that increased RC tendon thickness of greater than or equal to 0.80 mm compared to the asymptomatic shoulder was associated with RC tendinopathy. The conflicting findings of tendon thickness in this study compared to those of tendon thinning by
) were greater than 1 month with 30% of the subjects having pain less than 3 months in duration compared to an inclusion criteria of pain greater than 6 months in duration in the study by Cholewinski et al. (mean duration was 7 months, range 6–48 months). Overall, tendon morphology has been suggested to vary based on the duration of tendon injury. An acute injury exhibits increased diffuse tendon thickness associated with matrix changes of a healing response (