Shoulder Disorder: From Dysfunction to the Lesion

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CHAPTER 2 Shoulder Disorder: From Dysfunction to the Lesion

Giovanni DiGiacomo, Alberto Costantini, Andrea DeVita

“From dysfunction to lesion” is a very complex concept that involves knowledge and interpretation of different parameters that could alter a function and bring about a short-term and more often a long-term anatomic lesion. Initially, an ultrastructural lesion may evolve with distinctive peculiarities, and can be clinical or subclinical. It can show up with subjective and objective symptoms only under certain circumstances and according to intrinsic and extrinsic factors combined.1

Subacromial impingement syndrome is the most common shoulder disorder. It is present in 44% to 65% of all patients with a painful shoulder. This disorder can present in many forms, ranging from inflammation to degeneration of the bursa and rotator cuff tendons. It may lead to a full-thickness tear of the rotator cuff tendons and degenerative disease of the joints of the shoulder girdle. Impingement arises from mechanical compression of the rotator cuff, centered primarily on the supraspinatus tendinous insertion onto the greater tuberosity against the undersurface of the anterior third of the acromion.

Over the past few decades, this syndrome has been increasingly diagnosed. It was first described in the early 20th century. In 1931, Meyer2 proposed that rotator cuff tears occurred secondary to friction against the undersurface of the acromion and described corresponding lesions on the undersurface of the acromion and greater tuberosity. However, he did not implicate the acromion directly. Codman,3 in 1934, defined the critical zone where most degenerative changes occur as the portion of the rotator cuff located 1 cm medial to the insertion of the supraspinatus on the greater tuberosity. Armstrong4 introduced the term supraspinatus syndrome.

Neer and Welsh5 have described subacromial impingement syndrome as a distinct clinical entity and hypothesized that the rotator cuff is impinged on by the anterior third of the acromion, coracoacromial ligament, and acromioclavicular joint, rather than merely by the lateral aspect of the acromion. The clinical diagnosis of impingement syndrome is commonly based on findings defined by the impingement sign and test. The patient’s history typically includes pain at night and positional discomfort referred as a painful arc. The clinical presentation may be confusing, and it is important to differentiate subacromial impingement syndrome from other conditions that may cause symptoms in the shoulder. Especially in young patients and in overhead athletes, the diagnosis of impingement should be made carefully.

Partial or complete resection of the acromion has been reported to be a promising method in the treatment of rotator cuff syndrome. On the other hand, the disappointing results of complete and lateral acromionectomy prompted Neer6 to focus on the undersurface of the acromion as the offending area. He developed the technique of anterior acromioplasty, which includes acromioclavicular resection arthroplasty, when indicated, to correct impingement by decompressing the subacromial space. This procedure has been the gold standard for the treatment of impingement and still represents the main procedure for many surgeons.

The fact that acromioplasty relieves the impingement pain suggests the importance of the acromion in the cause of this disease. The shape of the acromion and angles of the spine of the scapula are associated with the pathogenesis of impingement syndrome. On the other hand, the mechanical cause of impingement might be related to several other factors. These numerous aspects are attributed to the extrinsic theory of the cause of impingement, according to which the lesion appears purely mechanical. The alternative to this mechanical theory is called the intrinsic theory. Its central idea is that the impingement syndrome occurs because of inherent degeneration of the rotator cuff tendons and associated shoulder muscle dysfunction.

CAUSATIVE FACTORS OF IMPINGEMENT SYNDROME

Many causes have been proposed for subacromial impingement syndrome. These factors can be broadly classified as intrinsic or intratendinous factors, which are related to the intrinsic theory on the origin of impingement, and extrinsic or extratendinous factors, which are related to the mechanical theory. They can be further characterized as primary or secondary. A primary cause, either intrinsic or extrinsic, results in the impingement process by decreasing the subacromial space or by causing a degenerative process of the rotator cuff tendons. A secondary cause is the result of another process, such as instability, neurologic injury, tight posterior capsule of the glenohumeral joint, or muscle dysfunction.

Intrinsic Theory

Degenerative Tendinopathy

Ozaki and colleagues7 have studied the pathologic changes on the undersurface of the acromion as associated with tears of the rotator cuff in 200 cadaveric shoulder. They suggested that rotator cuff tears or injuries are the result of intrinsic rather than extrinsic causes associated with impingement, as advocated by Neer.8 They found that although a lesion in the anterior third of the undersurface of the acromion was always associated with a rotator cuff tear, the reverse was not true, and they concluded that the pathogenesis of most cuff tears was probably an intrinsic process.

According to the extrinsic theory of the pathogenesis of impingement, the lesion in the rotator cuff tendon is caused by mechanical compression by the coracoacromial arch. Consequently, the disease process should come to a halt after decompressive acromioplasty, and the surgical outcome should be permanent. On the other hand, if the symptoms recur and the disease progresses to the tear stage despite acromioplasty, intrinsic factors, a degenerative process in the rotator cuff tendons, might be significant.

They concluded that the pathogenesis of most tears is probably a degenerative process. Ogata and Uhthoff9 have suggested that tendon degeneration is the primary cause of partial tears of the rotator cuff, and that they might allow proximal migration of the humeral head, which could result in impingement and lead to complete tears of the rotator cuff.

Muscle Dysfunction

It has been observed that an intrinsic contractile tension overload on the muscle rather than primary impingement is the major factor in the cause of rotator cuff tendinitis. When the arm is in the overhead position, eccentric contraction of the supraspinatus decelerates internal rotation and adduction of the arm, causing an overload. This phenomenon is most dramatic in those involved in overhead sports, and it may also occur in manual workers who use overhead motions in their work. The proximal migration of the humeral head has also been associated with muscle fatigue, injury, and degenerative changes in the rotator cuff tendons. Bigliani and Levine10 have noted that resection of the coracoacromial ligament should be avoided in this situation because it may not relieve the impingement, but could allow for additional proximal migration of the humeral head. Decrease in proprioceptive sense with muscle fatigue might play a role in decreasing athletic performance and in fatigue-related shoulder dysfunction.

Imbalance of the rotator cuff muscles in athletes, who have developed this as a result of training or sport activities, has generally been found to be a predisposing factor or a consequence of the impingement syndrome. Brox and coworkers11 have reported that surgery and supervised exercise improve rotator cuff disease equally and significantly compared with placebo, suggesting the importance of considering this factor.

Extrinsic (Mechanical) Theory

Shape of the Acromion

Acromial morphology and differences in the shape and slope of the acromion as a potential source of symptoms in the shoulder have often been observed. Neer6 focused on the cause and effect relationship between acromial morphology and subacromial impingement. He proposed that variations in the shape and slope of the anterior aspect of the acromion were responsible for subacromial impingement and associated tears of the rotator cuff. A spur protruding into the subacromial space10 apparently was thought to be caused by tensile forces on the coracoacromial ligament. In another study, Morrison and Bigliani12 evaluated supraspinatus outlet radiographs and found that 80% of 82 patients who had a tear of the rotator cuff visible on an arthrogram had a type III acromion (hook acromion).

The classification system described by Bigliani and colleagues13 has been cited widely in the literature, but investigators have questioned its reliability. Zuckerman and associates14 reported low interobserver reliability during the evaluation of 110 anatomic specimens to determine acromial shape according to this classification.13 Jacobson and coworkers15 also reported low interobserver reliability when the system was used to evaluate acromial morphology as seen on a supraspinatus outlet view. They also questioned the correlation between acromial morphology and tears of the rotator cuff. The classification of acromial morphology on the basis of a subacromial outlet projection has reportedly been difficult because of individual differences in the supraspinatus outlet angle. Some investigators have stated that fluoroscopic control is necessary for a proper supraspinatus outlet view.

Wuh and Snyder16 have modified their classification system13 by addressing the thickness as well as the shape of the acromion. Three types of acromion were identified: type A (<8 mm), type B (8 to 12 mm) and type C (>12 mm).

Toivonen and colleagues17 measured the acromial angle, which is in accordance with the hypothesis proposed by Morrison and Bigliani12 of an association between acromion type III and rotator cuff tears. Aoki and associates18 studied 130 cadaveric shoulders and found that acromions with spur formation had a flatter slope and were associated with increased pitting on the surface of the greater tuberosity. They also showed that the prevalence of spurs in the subacromial space increased with age and noted a decreased alpha angle (also called acromial tilt) in the patients with impingement.

Degeneration of the Acromioclavicular Joint

Neer6,8 proposed that degeneration of the acromioclavicular joint may contribute to subacromial impingement. This hypothesis is supported by several other authors. Osteophytes protruding inferiorly from the undersurface of a degenerative acromioclavicular joint can contribute to impingement narrowing the supraspinatus outlet. Kessel and Watson19 found that one third of the patients in their study had lesions of the supraspinatus tendon, usually associated with degeneration of the acromioclavicular joint. Penny and Welsh20 subsequently found that osteoarthritis of the acromioclavicular joint may lead to failure of operative treatment of subacromial impingement. However, resection of the acromioclavicular joint should be performed only if the patient has symptoms in the joint region and if osteophytes contribute to the impingement.10

Coracoid Impingement

Coracoid impingement along the more medial aspect of the coracoacromial arch is less common, but has been reported.21 In patients with coracoid impingement, the pain is usually located on the anteromedial aspect of the shoulder and is felt in the arm and forearm. Forward elevation and internal rotation may elicit pain.10 In a recent study, cine magnetic resonance imaging was used to measure the interval between the coracoid process and the lesser tuberosity. In the asymptomatic control group, the average interval between the coracoid process and the lesser tuberosity was 11 mm, whereas in symptomatic patients the interval was found to be 6 mm. Gerber and coworkers22 have reported that coracoid impingement can be idiopathic, iatrogenic, or traumatic. As a choice for operative treatment, Dines and colleagues23 have recommended coracohumeral decompression.

Impingement by the Coracoacromial Ligament

A number of investigators6,8,24 have also implied the coracoacromial ligament as a source of impingement. McLaughlin25 observed the condition termed snapping shoulder and concluded that the coracoacromial ligament is an offending structure in painful shoulders.

Soslowsky and colleagues26 found statistically significant changes in the geometric dimensions of the lateral band of the coracoacromial ligament, which is the region most likely to impinge on the rotator cuff. In another study, they found significant changes in the material properties of the ligament. Sarkar and associates27 and Uhthoff and coworkers24 reported that histologic studies of specimens of the coracoacromial ligament from patients who had impingement syndrome revealed only degenerative changes without thickening.

Os Acromiale

Os acromiale is an unfused distal acromial epiphysis first described in 1863 by Gruber.28 Folliasson29 classified the lesion into four distinct types according to the anatomic location, with mesoacromion being the most common type. The prevalence of os acromiale, as reported in both radiographic and anatomic studies, has varied a great deal, with a range from 1% to 15%. It is difficult to detect an os acromiale on routine anteroposterior plain x-rays and an axillary view may thus be needed.10 An association between os acromiale, impingement syndrome, and rotator cuff tears has been reported. Impingement may occur because the unfused epiphysis on the anterior aspect of the acromion may be hypermobile and may tilt anteriorly as a result of its attachment to the coracoacromial ligament. Hertel and colleagues30 have recommended stable fusion of a sizeable and hypermobile os acromiale.

Tight Posterior Capsule

There is a subset of patients who may have an initial diagnosis of impingement syndrome, but remain refractory to nonoperative and traditional operative treatment. Posterior capsule tightness may be forcing the humeral head forward, causing mechanical impingement and a loss of range of motion as a result of the avoidance of painful movements. Although the factors contributing to secondary shoulder impingement are multiple, the posterior capsule tightness is thought to alter arthrokinematics, with superior translation of the humeral head during flexion such that the rotator cuff is compromised by the overlying coracoacromial arch.

Harryman and associates31 have stated that oblique glenohumeral translations are not the result of ligament insufficiency or laxity. Instead, translation results when the capsule is asymmetrically tight. Asymmetrical tightness is thought to cause anterior and superior migration of the humeral head during forward elevation of the shoulder, possibly contributing to impingement.

Glenohumeral joint inflexibility can also create abnormal biomechanics of the scapula. Posterior shoulder inflexibility caused by capsular or muscular tightness affects the smooth motion of the glenohumeral joint31 and creates a wind-up effect so that the glenoid and scapula actually get pulled in a forward and inferior direction by the moving and rotating arm. This can create an excessive amount of protraction of the scapula on the thorax as the arm continues into the horizontally adducted position in follow-through. Because of the geometry of the upper aspect of the thorax, the more the scapula is protracted in follow-through, the farther it and its acromion move anteriorly and inferiorly around the thorax.

It is unclear why the posterior capsule becomes scarred and contracted, although some would postulate that in case of injury associated with a traction mechanism, trauma to the posterior capsule results in localized and excessive scarring. In patients who underwent a posterior capsular shift procedure, the repair might too tight or there might be an excessive scarring in this region following the repair.

Reeves32 has proposed that the stiff shoulder be classified as a frozen shoulder or post-traumatic stiff shoulder. The term frozen shoulder, introduced by Codman33 in 1934, refers to no traumatic stiffness of the glenohumeral joint capsule.

Idiopathic adhesive capsulitis is a condition of uncertain cause characterized by limited active and passive shoulder motion. Primary adhesive capsulitis develops insidiously, following minimal or no trauma, with a gradual loss of function caused by pain and restriction of motion. Adhesive capsulitis may also occur secondary to intrinsic shoulder pathology, such as subacromial impingement syndrome, extrinsic disorders such as pulmonary disease, or systemic conditions such as diabetes. Despite these associations, the underlying cause and pathophysiology of this disorder remain unknown.

Although many different causes have been proposed for frozen shoulder, the common thread in most causal theories is the presence of inflammation. On the other hand, a post-traumatic stiff shoulder may originate from a traumatic extracapsular process; however, subsequent capsular contracture may soon develop. Each of these diagnoses may exhibit a different underlying pathology, history, and treatment.

Clinically, much attention has been paid to how a tight posterior capsule might affect normal glenohumeral arthrokinematics. In all cases of suspected impingement, a careful examination of passive and active motion in all planes is needed. In patients with limited internal rotation and flexion, a therapy program should be directed at improving these motion planes.

Scapulothoracic Dyskinesia

Scapulothoracic dyskinesia is abnormal scapular motion characterized by medial border prominence or inferior angle prominence, early scapular elevation or shrugging, rapid downward rotation during lowering, or a combination of these. It is noteworthy that in the causative pathogenetic classification of the most common shoulder disorder (impingement syndrome), an anatomostructural alteration (e.g., acromion III, os acromiale, posterior capsule tightening) is often seen as the trigger element, without considering the shoulder as part of a kinetic chain.

Our research, based on a number of studies, leads us to consider more comprehensively the causative pathogenetic mechanisms of this joint’s pathologies. Always bearing in mind possible local anatomic lesions, we try to interpret those distant musculoskeletal dysfunctions as trigger points that through neurophysiologic and biomechanical mechanisms, can lead to ligament and shoulder tendon lesions. In this case, the shoulder joint becomes the victim and not the culprit of a dysfunction, eventually resulting in an anatomic injury, with clinical findings affecting the shoulder girdle.

This type of approach might explain the failure of some surgical ligament and tendon repair techniques, often attributed to failed materials (e.g., anchors, suture, biologic and not reabsorbable) or local biologic factors (e.g., vascularization, fatty infiltration), forgetting that these anatomic lesions are often the end point of a failure in the kinetic chain, which if not corrected could inevitably reproduce the lesion over time, even after surgery.

The dynamic scapulothoracic stability and importance of the core stability strongly indicate that those mechanisms, when altered, can lead to shoulder dysfunction. The shoulder is a complex mechanical structure containing several joints connecting the humerus, scapula, clavicle, and sternum. The scapula slides over the dorsal part of the thorax; it can glide over the so-called scapulothoracic gliding plane. It is a closed-chain mechanism. The relationship between the rotations of the humerus and scapula is commonly referred to as the scapulohumeral rhythm. The scapular motion strongly affects the mechanical energy delivered by muscles and the metabolic cost required to obtain the desired force. At the same time, the scapula has different roles; it is a functional part of the glenohumeral joint, retracting and protracting along the thoracic wall and elevating the acromion. It is a site for muscle attachment and a link in the proximal to distal sequencing of velocity, energy, and force that allows the most appropriate shoulder function.34

The core is where the center of gravity is located and where movement begins. An efficient core allows for maintenance of the physiologic length-tension relationship of functional agonists and antagonists, and for a normal force couple in the lumbar pelvic hip complex. The musculoskeletal core of the body includes the spine, hips, pelvis, proximal lower limb, and abdominal structures. Muscles of the trunk and pelvis are responsible for the maintenance of stability of the spine and are critical for the transfer of energy from large to small body parts during many work and sports activities. The roof of the core muscle structures is the diaphragm; the opposite end of the trunk component of the core muscles is the pelvic floor muscles. Core muscles have large cross-sectional areas and generate a great amount of force and power for athletic activities. The thoracolumbar fascia is an important structure that connects the lower limbs (via the gluteus maximus) to the upper limbs (via the latissimus dorsi).

Function, the end result of the kinetic chain, can be defined as optimal anatomy acted on by physiologic muscle activations to produce optimal biomechanical forces and motions. Core stability is essential for the maximum efficiency of shoulder function. A functional definition of core stability is the ability to control the trunk over the pelvis to allow the coordinated sequenced activation of body part to produce, transfer, and control force and motion to the terminal segments in integrated body activities to obtain the desired work or athletic task.35 This definition implies patterned sequences for force generation and transfer, proximal stability for distal mobility, and control in three dimensions.

Muscle activation in kinetic chain function is based on preprogrammed patterns that are task-oriented, specific for different activities, and improved by repetition. Core muscle activation is used to generate rotational torques around the spine and provides stiffness to the entire central mass, making a rigid cylinder that confers a long lever arm around which rotation can occur and against which muscles can be stabilized as they contract.36

One of the most important abnormalities in scapular biomechanics is actually the loss of the link function in the kinetic chain. If the scapula becomes deficient in motion or position, transmission of the large generated forces from the lower to the upper extremity is impaired. This creates a deficiency in resultant maximum force, which can be delivered to the hand or creates a situation of catch-up, in which the more distal links have to work more actively to compensate for the loss of the proximally generated force. This can impair the function of the distal links because they do not have the size, muscle cross-sectional area, or time to develop these larger forces efficiently. Kibler’s34 calculations have shown that a 20% decrease in kinetic energy delivered from the hip and trunk to the arm necessitates an 80% increase in mass or a 34% increase in rotational velocity at the shoulder to deliver the same amount of resultant force to the hand. This required adaptation can cause overload problems with repeated use.

In condition of work-related or sports-related stress, regulatory imbalance might result in typical reaction patterns and individual response specificity. This can explain the anatomic and pathologic differences of the several lesions (e.g., extension, site, degrees of retraction), and justifies those clinical pictures that even if triggered by similar lesions, appear at different times and with different clinical features.

Adaptation Mechanisms: Allostasis.

The adaptation mechanism in this case is first neuromuscular, aimed at temporarily maintaining a work- or sports-related function. In addition to overloading some muscle groups, they stress joints, ligaments, and tendons to work outside the save zones, placing these structures at risk. All this can lead to the concept of allostasis introduced by Sterling and Eyer.37

To adapt to or ultimately survive a stressful situation, animals and humans must be able to change their behavior and physiology. Allostasis is the coordinated process that promotes such adaptation and increases the chance of survival. For example, in response to an intensive emotional stressor, the sympathetic branch of the autonomic nervous system is activated and the adrenal medulla secretes epinephrine (adrenaline). This prepares the individual for intense and vigorous physical activity by mobilizing energy resources. The blood flow is redirected to the skeletal muscles, heart, and brain. The heart and respiratory rates, as well as arousal and vigilance, increase. The behavior is changed toward, for example, an appropriate level of aggressiveness—the fight-or-flight response described by Cannon.38 When the adaptation to a stressor is successful, the allostatic responses protect the body and help the individual to cope effectively.

This example initially can seem excessive for the shoulder, but a careful evaluation can help in understanding how every body system survives, thanks to function-dependent replacement mechanisms that have to meet different versatility characteristics. However, so as not to impose unnecessary wear and tear on the organism, the physiologic responses should return to baseline (resting values) quickly after the challenge or threat has terminated, and a period of rest and recovery should follow before a new challenge is encountered. The evolutionary basis for this defense reaction is very old, but in modern society mental and social stressors probably elicit it more often than physical threats requiring a vigorous effort and thus using the energy mobilized. Furthermore, important to the concept of allostasis is the primary role of the brain in regulating physiologic processes, thereby emphasizing the potential role of psychological and social processes in health and disease.37

Allostasis focuses on variability (from the Greek allo, meaning variable), in contrast to the older concept of homeostasis, which focuses on the importance of maintaining a constant internal environment. Accordingly, allostasis can be translated as stability through change.37 This refers to the principle that an organism, to achieve (homeostatic) stability, must have the ability to vary its physiology to match different challenges or demands of varying severity. These two principles can be seen as representing different ways of functioning for different physiologic systems. According to the concept of allostasis, a balance between activity and rest is important for sustaining health. In physiologic terms, this can be described as a necessary balance between catabolism (when energy is used) and anabolism (when energy is stored and tissues are repaired).37 When this balance is disrupted (e.g., because of chronic physical overload or psychosocial stress), the excessive and sustained activation of the allostatic systems results in what has been termed allostatic load, a term coined by McEwen and Stellar.39 Allostatic responses are beneficial over the short term because they promote adaptation. With time, however, they may lead to allostatic load, which can be described as the cumulative wear and tear on the organism, sometimes referred to as the price of adaptation. According to McEwen and Seeman,40 at least four situations can lead to allostatic load:

1. Frequent activation of allostatic systems, without enough time for rest and recovery
2. Failure to adapt or get used to repeated exposure to the same stressor
3. Failure to shut off the allostatic responses, leading to a prolonged exposure to mediators of allostasis, such as glucocorticoids and cathecholamines
4. Failure to activate an adequate allostatic response in one allostatic system; may cause other systems to increase their activity in a compensatory way

Thus, too much use of allostatic systems or their dysfunction (overactivity or underactivity) results in a cumulative wear and tear on the organism, which over long periods promotes pathophysiologic changes and may lead to various pathologic conditions and diseases. Examples in the literature are atherosclerosis, hypertension, insulin resistance, abdominal obesity, type 2 diabetes, autoimmune and inflammatory disorders, cuff tears, labral tears, and SICK syndrome (scapular malposition, inferior medial border prominence, coracoid pain and malposition, dyskinesis of scapular movement).39,40 The processes leading to allostatic load are complex and are influenced not only by the impact of stressful events and daily hassles from work or sports that accumulate over long periods (chronic stress), but also from genetic factors, early life experiences, personality characteristics,and lifestyle factors, such as exercise, diet, smoking, and alcohol.40 A typical example is the functional overload of some shoulder ligament and/or tendon structures (allostatic response) in the presence of scapulothoracic and core dysfunctions.

Scapular roles can be affected by many factors to create abnormal biomechanics and physiology. The factors may be local around the scapula or distant in other links of the kinetic chain (e.g., core instability such as weakness and/or tightness at the hip, alteration of knee flexion). They may be directly related to an injury or more often may be related to overuse, fatigue, or neuromuscular alteration.

Nerve injury to the long thoracic nerve or spinal accessory nerve can alter muscular function of the serratus anterior or trapezius muscle, respectively, causing abnormal stabilization and control. This occurs in less than 5% of muscle function problems. The bony anatomy and positioning of the scapula can be altered by body posture or bony injury. A resting posture of cervical lordosis or thoracic kyphosis can result in expressive scapular protraction and acromial depression in all phases of work or athletic activity, increasing the incidence of impingement.

More commonly, the scapular stabilizers are injured by the following: (1) direct blow trauma; (2) microtrauma-induced strain in the muscles, leading to muscle weakness and force couple imbalance; (3) becoming fatigued from repetitive tensile use (also true for catch-up); (4) or inhibition by painful conditions around the shoulder (it is assumed that muscle pain has the potential to change the coordination between agonist and antagonist by reflex mediation). These causes are responsible for the causative pathogenetic mechanisms of work and sports-related shoulder dysfunctions that can become potentially symptomatic in case of a supposed allostatic load on the compensatory structures.

High-Frequency and Low- Frequency Fatigue

The type of repetitive work frequently associated with shoulder and upper extremity disorders usually involves prolonged sustained or repetitive muscle activation, with low external force demands, often combined with high demands on precision—for example, computerized data entry or assembly operations. The required contraction patterns of distal muscles differ from those of proximal muscles, with short repetitive contractions for the former and more prolonged static stabilizing cocontractions for the latter. Static work postures, especially with muscles in shortened positions, may also result in asymmetrical shortening of muscles, compression, and tension on nerves.

Stereotyped low-intensity repetitive work has some important characteristics, significant for their possible causal relation to shoulder dysfunction. A constrained movement pattern during the work task not only leads to a restricted load distribution among muscles but could also have deleterious effects on specific subsets of muscle fibers. Because muscle fibers belonging to low-threshold motor units are the first to be recruited and the last to be derecruited, according to the ordered recruitment principle, they are most susceptible to long-lasting fatiguing overload. For this reason, these fibers have been called Cinderella fibers. A protective mechanism against the Cinderella syndrome could be the rotation of different motor units in which units are activated in turn during prolonged contraction periods. However, this protective mechanism may fail, especially during prolonged work exposure with biomechanically constrained work tasks involving stereotypic movement patterns. The reason for this failure is probably complex and not yet well understood. One possible reason may be that the central nervous system (CNS) freedom to choose motor units may be reduced in repetitive work tasks with biomechanical restraints. Also, low-intensity work is likely to cause only a moderate metabolic effect, which may be too weak to trigger any protective mechanism (allostatic response) for motor unit rotation. Thus, in some work tasks, the Cinderella mechanism may affect muscle performance. If so, muscle fibers connected with low-threshold motor units will be overloaded and eventually fatigued.

The type of fatigue brought about by prolonged low-intensity work is called low-frequency fatigue (LFF). In contrast to high-frequency fatigue (HFF), LFF has a very slow recovery and its effects last in the absence of larger metabolic or electrical disturbances in the muscle. Because of its slow recovery, this type of fatigue may accumulate over time and increases the risk of the intramuscular accumulation of substances involved in developing pain and altering neuromuscular control (muscle inhibition).

In the shoulder, muscle inhibition is seen as decreased ability for muscles to exert torque and stabilize the scapula and as disorganization of the normal muscle firing patterns around the shoulder girdle.41 This is common in glenohumeral and subacromial pathologies, whether resulting from cuff tears, instability, labral pathology, arthrosis, muscular fatigue, or postural disorders. Muscle inhibition and the resulting scapular dyskinesia appear to be a nonspecific response to a painful condition in the shoulder rather than a specific response to a specific glenohumeral pathologic situation. The exact nature of this inhibition is not clear. The nonspecific response and disorganization of motor patterns suggest a proprioceptively based mechanism. Pain from direct muscle injury or indirect sources, such as fatigue or uncontrolled muscle strain, have been shown to alter proprioceptive input from Golgi tendon organs and muscles spindles.

Proprioception And Muscular Fatigue

Normal shoulder function relies on correct scapular biomechanics and balance within the kinetic chain. The kinetic chain is coordinated by the sensorimotor system, which is defined as all the sensory, motor, and central integration and processing components involved in maintaining joint stability and coordination. It consists of the visual, vestibular, and somatosensory systems.

The somatosensory system is the collection of peripheral sensory receptors responsible for giving rise to afferent information for the perceptions of mechanoreceptive (tactile and proprioceptive), thermoreceptive, and pain sensations. Because proprioception is a component of neuromuscular control, the two terms are often used interchangeably and incorrectly. Proprioception is defined as the specialized variation of the sensory modality of touch that encompasses the sensation of joint movement (kinesthesia) and joint position,42 whereas neuromuscular control is the unconscious motor efferent response to afferent sensory (proprioceptive) information. A mechanoreceptor is a specialized neuroepithelial structure found in the skin, ligamentous, muscular, and tendinous tissue that relays information about a joint.43 It transduces functional and mechanical deformation into frequency-modulated neural signals. An increase in deformation causes an increase in afferent discharge of neural signals back to the CNS.

Proprioceptive feedback regarding joint position results from mechanical stimulation of the mechanoreceptors located in the periarticular tendons, muscles, ligaments, and possibly skin.43,44 Ruffini-type mechanoreceptors are predominant in all articular structures of the shoulder except for the glenohumeral ligaments, where pacinian corpuscle-type receptors are most abundant.44 Muscle spindles and Golgi tendon organs are present in the muscles.

The capsuloligamentous and myotendinous receptors gather information that is modulated by the central nervous system through afferent pathways. Various muscle groups are activated and coordinated via the efferent pathways. The interplay between capsuloligamentous restraints and muscles is crucial; its role in maintaining scapular-thoracic coordination and stability at the glenohumeral joint is not fully appreciated, but it is influenced by mechanical and sensorimotor factors.1 Moreover, the existence of a reflex arc from mechanoreceptors within the glenohumeral capsule to muscles crossing the joint confirms and extends the concept of synergism between the passive and active restraints of the glenohumeral joint.31 Receptors are divided into rapidly and slowly adapting types, which work in an integrated fashion and with different excitement thresholds.

This combination of muscle and joint receptors forms an integral component of a complex sensorimotor system that plays a role in the proprioceptive mechanism and is part of a feedback–feed-forward system initiated by an activation of mechanoreceptors. The sensory input (afferent) from the mechanoreceptors is relayed by the peripheral nervous system (PNS) to the CNS. The CNS responds to the afferent stimulus by discharging a motor signal (efferent), which modulates effector muscle function by controlling joint motion and/or position.

The afferent and efferent pathways involved with this complex system mediate proprioception at three distinct levels in the CNS. At the spinal level, proprioception operates unconsciously with reflexes subserving movement patterns received from higher levels of the nervous system. This provides reflex splinting under abnormal stress about the joint and has significant implications for rehabilitation. The muscle spindles play a major role in the control of muscular movement by adjusting activity in the lower motor neurons. The second level of motor control is at the brainstem (basal ganglia and cerebellum), where joint afference is relayed to maintain the body’s posture and balance. The final aspect of motor control includes the highest level of CNS function, the motor cortex, and is mediated by cognitive awareness of body position and motion. Proprioception at this level functions consciously and is crucial for proper muscle and joint functioning in daily activities, sports, and occupational tasks. These higher centers initiate and program motor commands for voluntary movements.

Because mechanoreceptors, which are responsible for proprioceptive feedback causing neuromuscular responses, are present in the muscular structure surrounding the joint,43 it is highly likely that as a muscle fatigues, proprioceptive feedback is delayed, and consequently neuromuscular control and shoulder function are impaired. Fatigue affects sensation of joint movement, decreases work and athletic performance, and increases fatigue-related shoulder dysfunction. Voight and colleagues45 have noted that that the decrease in ability after fatigue is caused by dysfunctional mechanoreceptors.

Deafferentation refers to damage to mechanoreceptors, cutting off neural supply and reducing or eliminating the afferent supply arising from the damaged structure. Some of the most frequent causes of deafferentation (dysfunctional mechanoreceptors) are muscle fatigue, pain, hyperlaxity, and repetitive microtrauma, which can alter receptor functions so that the CNS receives incorrect information. This modulates the efferent pathways, thus creating a potential dysfunction.

Both central and peripheral fatigue may also influence proprioception and neuromuscular control. Central fatigue results from CNS influence, whereas peripheral fatigue occurs at the level of the sarcomere and involves failure at the neuromuscular junction, sarcolemma, and transverse tubules. Because central fatigue appears so commonly in human performance, one might expect that its development confers some evolutionary advantages. Perhaps drive is limited because continued stimuli to the muscle would put the neuromuscular junction, or more likely the intracellular events accompanying excitation-contraction coupling and actin-myosin interactions, into a catastrophic state, from which recovery would be delayed or impossible. More relevant to the aim of this chapter is Winter’s definition,46 which refers to muscle fatigue as occurring when the muscle tissue cannot support metabolism at the contractile element because of ischemia (insufficient oxygen) or local depletion of any of the metabolic substrates.

In addition to being a manifestation of overuse (overtraining in work and sports) and of the catch-up mechanism described earlier, muscle fatigue can be influenced by the patient’s genetic profile, manifesting with widely different phenotypical characteristics such as incorrect posture, poor tissue quality, and neuroendocrine imbalance regulating repair processes. All this translates into a functional overload of the muscle tissue.

In inflamed, ischemic, or fatigued muscle, certain chemicals are produced, including lactic acid, bradykinins, prostaglandins, serotonins, and potassium. The effect of these substances is to sensitize the free nerve endings. Under these circumstances, a much larger proportion of muscular free nerve endings has a resting discharge and a larger proportion responds to physiologic joint movements.

The small-diameter group III and IV afferents from these hyperactive free nerve endings, may stimulate the α afferents through the posterior horn, leading in turn to abnormal afferent output from the muscle spindles. The end result may be a disturbed joint position and direction of movements (dysfunction), which this may lead to an anatomic lesion over time.

Because local blood flow and metabolic changes are more pronounced in muscles than in articular structures, muscle mechanoreceptors may be more affected than articular mechanoreceptors. The serratus anterior and lower trapezius are the most susceptible muscles of the shoulder girdle to the effects of the inhibition, and are more frequently involved in early phases of shoulder injury.

The failure of interplay in the kinetic chain—for example, caused by fatigability of the latissimus dorsi and serratus anterior—can lead to scapulothoracic dyskinesia. These two muscles form a crucial part of the force couple responsible for elevating the acromion. They can be inhibited, as stated earlier (allostatic load), by an unstable core or altered proximal rings of the kinetic chain. An alteration of the scapulothoracic rhythm sets off a series of events; a minor scapular retraction that reduces the subacromial space. Lack of acromial elevation and consequent secondary impingement can be seen very early in many shoulder problems, such as rotator cuff tendinitis and glenohumeral instability, and can play a major role in defining the clinical problems that are associated with these diagnostic entities. Therefore, the abnormal scapular biomechanics, occurring as a result of dysfunction, create an abnormal scapular position that decreases normal shoulder function and exposes the shoulder to injury (impingement, instability).

Overuse Dysfunction

The shoulder at risk may be considered the typical example of how a dysfunction can evolve into a lesion, and how both (a dysfunction and lesion) can be subclinical and show up clinically not only after time, but also on the basis of the type of athletic move, the intensity of the athletic efforts, and external events, such as more or less severe traumas. Throwing athletes are therefore likely to develop the dead arm syndrome. Generally, a shoulder at risk is subjectively asymptomatic, but exhibits small to moderate amounts of a throwing-acquired glenohumeral internal rotation deficit (GIRD), a malpositioned SICK scapula, or both. If the athlete with a shoulder at risk keeps throwing, the magnitude of the shoulder dysfunction will lead to intra-articular structural damage and the patient becomes symptomatic.

Under healthy conditions, a glenohumeral distraction force generated during the acceleration phase, from 1 to 1.5 times body weight, is present at ball release. This distraction force is normally compensated by a concomitant violent contracture of the posterior shoulder musculature (cuff, scapular stabilizers, and quadrangular space muscles) at ball release, lasting through the first third of follow-through. With repetitive overuse, deconditioned (weak) posterior shoulder musculature, usually involving the scapular stabilizers and rotator cuff, results in the distraction force not being fully compensated. This allows the posterior inferior capsule to receive abnormal tensile load, because at ball release with the shoulder flexed 90 degrees forward and adducted to neutral or more the posterior band of the inferior glenohumeral ligament (IGHL) is directly in line to receive most or all of any glenohumeral distractive force. This focal repetitive distractive load applied to the posterior inferior capsule is thought to stimulate a fibroblastic response, which initiates and propagates the throwing acquired posterior inferior capsular contracture (Wolff’s law of collagen).

Painless loss of velocity and command occur initially subtly but overtly over time. This is caused by the early loss of GIRD secondary to throwing acquired focal posterior inferior capsular contracture. Posterior or posterior superior shoulder stiffness and trouble loosening up occur. This is caused by a worsened posterior inferior capsular contracture. Posterior or posterior superior shoulder pain is felt without mechanical symptoms, usually described as occurring during the late cocking and early acceleration phases of the throwing cycle. This is to the result of posterior superior glenohumeral instability directed by the posterior inferior capsular contracture as the shoulder abduces and rotates. The posterior superior shift of the glenohumeral contact and rotational point creates strain on the posterior superior labral glenoid interface. It also allows for increased external humeral rotation, which brings the undersurface of the posterior superior rotator cuff in contact with the posterior superior glenoid margin, resulting in the early symptoms of internal impingement.

The slap event occurs when the posterior superior labrum and biceps anchor fail in tension from their glenoid attachments secondary to the capsular contracture mediated by posterior superior glenohumeral instability. Once the slap event has occurred, the thrower promptly develops mechanical symptoms in the late cocking and early acceleration phases. Once mechanical symptoms appear, the problem becomes surgical and will not be improved or solved conservatively. Conversely, prior to the slap event, the symptomatic throwing shoulder can usually be successfully treated by a series of focused posterior inferior capsular stretches to eliminate the contracture and strength exercises. these can rehabilitate any concomitant rotator cuff– and scapular stabilizer–deconditioned musculature.

After the mechanical symptoms of the slap event, if the thrower continues to throw, subacromial and rotator cuff symptoms ensue because of contracture-mediated increasing posterior superior glenohumeral instability, with secondary subacromial space restriction and increasing internal impingement. If throwing continues, the anterior inferior labrum and/or capsule can begin to fail as result of a tertiary event caused primarily by the contracture and secondarily by the posterior superior glenohumeral instability. This produces anterior capsular pseudolaxity and allows for pathologic excessive humeral external rotation, which in turn causes the capsule to fail, resulting in tertiary anterior glenohumeral instability.

Static or dynamic dyskinesis is a manifestation of deconditioning of some or all of the 18 muscles attached to the scapula that control scapular position and motion. In the setting of the overhead or throwing athlete without a history of single-event trauma, scapular asymmetry is the result of repetitive overuse muscular fatigue weakness. This muscular fatigue weakness is also the major cause of the throwing acquired posterior inferior capsular contracture.

CONCLUSIONS

Shoulder injuries can occur in two main modes, acute and chronic. The acute mode is the result of an acute macrotrauma. The chronic mode is the result of a microtrauma with a gradual onset of symptoms. Injury may lead to mild subclinical tensile overload in specific tissues.

It is noteworthy how a seemingly localized shoulder microtrauma (e.g., peel back in the slap lesion during the cocking phase of throwing, or posterior capsular overload in follow-through) generally does not result only from a local cause. For example, a scapulothoracic dyskinesia causes a more protracted scapula and therefore a higher bicipital anchor stress during late cocking or early acceleration phase of the throwing sequence; this reduces the eccentric posterior cuff contraction, causing a posterior capsular overload during the follow-through (localized posteroinferior capsular contracture).

The functional shoulder overload, often resulting from a compensation mechanism caused by the lack of force and energy delivered through the more proximal links on the kinetic chain, tends to appear in certain structures (e.g., rotator cuff tendons, subacromial bursa, capsular labral system) susceptible to microtraumas (overload). This catch-up phenomenon is dangerous and inefficient for the shoulder structures that have to absorb more stress and load.

Anatomic-biomechanical deficits thus ensue in these tissues, with a corresponding increased lesion risk and decreased performance. The mildest anatomic deficits are accompanied by functional, often subclinical, biomechanical ones and become biomechanically abnormal only when the shoulder is under stress in specific work or sports activity. These biomechanical impairments alter joint stability, range of motion, instant center of rotation, muscle strength, force balance, force application across joints, muscle flexibility, proprioception, and neuromuscular control.

Pain in a chronic injury may be fairly widespread because of the functional adaptation of the musculoskeletal system (allostasis). It is actually biomechanical maladaptation (asymptomatic strength deficit, inflexibility, and biomechanical changes out of the save zone) that could predispose the patient to future injury. This slight subclinical balance, characterized by minimal anatomic lesions and biomechanical alterations supported by a dysfunction resulting from an altered kinetic chain, is concealed by compensation mechanisms susceptible to frequency, intensity, duration, and rest from the functional effort, in addition to typical reaction patterns and individual response specificity.

Over time, these are the same elements that dictate the developing anatomic characteristics of these lesions; however, they can also result from an external event such as trauma, a functional overload period, or activity resumption after prolonged inactivity. Reducing the effect of the compensatory mechanisms, these can produce a clinical picture that is the end result of dysfunction and the anatomic lesion.

To demonstrate how these criteria can be applied to different shoulder pathologies, let us consider the subset of patients suffering from capsular laxity, with cuff disorders or more frequent small lesions of the capsulolabral complex. Because the athlete has had good posture and good neuromuscular control over the years, such anatomic lesions created by repeated overuse will remain asymptomatic because of a variety of adaptive neurophysiologic and biomechanical mechanisms (see earlier). If overhead activity demands on the athlete increase, (muscle fatigue), or if the athlete restarts training after a long period of inactivity, he or she loses the appropriate neuromuscular control and the chances of compensation decrease. If this situation persists without correct training or rehabilitative treatment, the clinical picture worsens and the anatomic lesions previously asymptomatic become symptomatic (emerging lesion). The anatomic lesions and biomechanical deficits may also influence deafferentation, thus generating a vicious circle in which the factors triggering the deafferentation worsen the lesion, and vice versa.

This strengthens the concept of the evolving lesion, which develop over time, so that the pain threshold is slowly exceeded and the lesion becomes clinically evident. A correct balance of functional requirement, rest, use of painkillers and anti-inflammatory drugs, compensation mechanisms, or constitutional and rehabilitative adaptation will determine the evolution of the anatomic changes and the clinical evidence of the lesion.

The treatment of such gradually developing lesions depends on how early the patient is examined and whether the tissue is inflamed or reversibly damaged, assessed by clinical and imaging investigations. Generally, we would opt for rehabilitative treatment, bearing in mind certain variables that in our experience may affect the case or the type of treatment (e.g., mechanical symptoms, posture, condition of the damaged tissue, patient’s gender, age, work, sport, goals). A well-designed comprehensive diagnostic process and good patient selection can provide the best treatment. Other factors such as working environment, quality of rehabilitation, and genetic profile may also influence the decision.

In most cases of more pronounced anatomic lesions, the injury repair is suggested and then rehabilitation is recommended, which aims at treating the real cause (dysfunction) leading to the anatomic lesion. Rehabilitation that ignores these aspects can result in surgical failures—for example, of rotator cuff repair. A high incidence of relapses of surgically repaired cuff lesions has been noted in recent studies; these have been identified with ultrasound and MRI tests, and such retears are often asymptomatic, with he most evident effect being a loss of strength.47

Failure to eliminate the postural defect and mechanical weakness through rehabilitation may justify the unsuccessful anatomic repair and therefore the loss of strength. Pain remission might be caused by deafferentation of the pain receptors that inevitably follows bursectomy, release, débridement, and repair of unstable redundant margins. Rehabilitative postsurgical treatment nevertheless improves subacromial compliance and the kinetic chain.

Without consideration of high-impact traumas, shoulder pathologies generally result from anatomic lesions of varying degree and location. These are the slow and progressive result of dysfunctions of the kinetic chain often caused by reduced neuromuscular efficiency.

The concepts and implications discussed are to be remembered—the evolving lesion that evolves slowly over time, and the emerging lesion, which often requires an external event to emerge clinically. Lesions that evolve through deafferentation, which might be the manifestation of different factors (e.g., muscle fatigue, trauma, laxity) may gradually turn into emerging lesions and therefore become symptomatic. It is possible, therefore, to be faced with tissue damage that only recently has become symptomatic but may have long-standing morphofunctional causes, which can seriously affect the outcome of rehabilitation and/or surgery.

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