Anterior shoulder instability identifying neuromotor control patterns during overhead arm motions

Anterior Shoulder Instability – Rajaratnam B S 2007 Shoulder stabilization surgeries such as re-tensioning of the lax capsule prevented recurrent dislocations and facilitated transmissio

Anterior Shoulder Instability – Rajaratnam B S (2007)

CHAPTER ONE: INTRODUCTION

“Neuromotor control is a function about which we may know a great deal but,

in reality, we understand very little.” Garrett Jr & Kirkendall (2000) page 53

During dynamic arm elevation, the passive and active restraint systems

at the glenohumeral joint ensured the proper alignment of the humerus within the glenoid fossa throughout the range of shoulder movements (Calliet 1981; Lephart et al 2000) Forceful and traumatic dislocation at the glenohumeral joint (GH) disrupted the structural congruency of the passive restraints and altered the force equilibriums generated primarily by the active systems Anterior dislocation of the humeral head is common after trauma to the shoulder and occurs in ninety eight percent of patients with shoulder instability (Hayes et al 2002) Eighty three percent of patients were less than twenty years old while 20% were aged 60 and more (Rowe 1956; Gumina & Postaccini 1997; Robinson et al 2002) After a first shoulder dislocation, as much as 60% of patients sustained a re-dislocation over a 10-year period, usually when performing non-traumatic activities such as putting on their t-shirt or during quick trivial overhead arm movements (Hovelius et al 1996; Robinson et al 2002; Deitch et al 2003) A high prevalence of nerve palsy was present after the first dislocation (Robinson et al 2002) Twenty-two percent of recurrent shoulder dislocations occurred among elderly patients who are less likely to be involved in overhead arm associated sports (Gumina & Postacchini 1997)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Shoulder stabilization surgeries such as re-tensioning of the lax capsule prevented recurrent dislocations and facilitated transmission of kinesthesia and joint position signals to the brain for neuromotor control processing (Hovelius et al 1996) However, a recent Cochrane review stated that there was limited evidence to support primary surgery to prevent recurrent dislocations for patients with anterior shoulder instability (Handoll et

al 2005) Despite having undergone a stabilization procedure and correction

of structural deficits, 5 of 16 adolescents patients (31%) experienced operative shoulder dislocation (Deitch et al 2003) while arthroscopic stabilization decreased recurrence to 5% to 22% (Lawton et al 2002) Saha (1983) was of the opinion that when there was no history of shoulder injury and when no Bankart lesion was demonstrable, recurrent shoulder dislocation occurred due to a lack of the stabilizing factors Superimposed trauma may cause the GH joint to undergo spontaneous dislocation with or without minimal stress Furthermore, two factors that contributed to negative outcomes after surgery other than damages to osseous restraints were the presence of multidirectional instability features and injuries to the rotator cuff muscles (Robinson et al 2002; Meehan & Petersen 2005) Poor functional return may be anticipated even after surgery if uncorrected mixed pathologies

post-of muscle imbalances and altered muscle activation patterns are present (McAuliffe et al 1988; Sharkey & Marder 1995; McMahon & Lee 2002; Lewis

et al 2004; Myers et al 2004; Morris et al 2004; Barden et al 2005)

Albeit, no study has quantified neuromotor control strategies at the unstable shoulder during overhead arm motion even though studies have

Anterior Shoulder Instability – Rajaratnam B S (2007)

quantified defective activation patterns among patients with chronic low back and neck pain (Panjabi 1992; Hodges & Richardson 1999; Sahrmann 2002; Krishnamoorthy et al 2003; Ko et al 2003; Falla et al 2004a; Silfes et al 2005) The findings among patients with spinal disorders led to better rehabilitation programs and functional outcomes for them

Current rehabilitation strategies for patients with anterior shoulder instability (ASI) are focused mainly on strengthening of the rotator cuff and scapula-thoracic muscles after shoulder injury and surgical correction of shoulder instability (Gibson et al 2004) Understanding how quickly minimal practice of inappropriate muscle activation patterns alters the cortical maps and synaptic connections is important (Hayashi et al 2002; Falla et al 2004a & b; On et al 2004) Quantifying temporal-spatial characteristics of the muscle activation patterns at the shoulder among patients with ASI also provides an insight to how the central nervous system activates feed forward and feedback neuromotor controls to regulate GH joint stability throughout the range of arm elevation Understanding these quantifiable evidences of altered neuromotor control strategies can lead to more effective musculoskeletal rehabilitation for better management of the unstable shoulder (van Vliet & Heneghan 2006)

Rehabilitation programmes for the unstable shoulder also advocated correction of deficits in proprioception However, neurophysiological studies highlighted that proprioceptive signal from mechanoreceptors within the labral-ligamentous junctions of the unstable shoulder were undamaged and

Anterior Shoulder Instability – Rajaratnam B S (2007)

maintained direct afferent neurological pathways to the cerebral cortex (Lephart et al 1994; Tibone et al 1997) The mechanoreceptor arrangement of muscle spindles and Golgi Tendon Organs (GTO) senses changes in length and force respectively during arm elevation (Nichols 2002) The central nervous system utilized signals from mechanoreceptors to co-ordinate the actions of the rotator cuff muscles and generated compressive forces in excess of 0.92 times body weight for maximal concavity compression between the humeral head and the glenoid fossa (Poppen & Walker 1976; Howell & Kraft 1991; Inman et al 1944; Itoi et al 1996; Apreleva et al 2000) Anecdotal evidence suggests that the central nervous system priority is to maximize concavity compression and restrain abnormal humeral head translation at all cost (Latash & Anson 1996; Apreleva et al 2000; Magarey & Jones 2003) However, cadaver studies do not evaluate the regulatory role of the neuromotor control system during motion even though placing the unstable arm in overhead arm positions has been reported to stimulate muscle imbalances that contribute to GH joint instability (Lee et al 2000; An 2002; McMahon & Lee 2002; Labriola et al 2004 and 2005)

A conceptual model of stability in the spine described by Panjabi (1992) that involved the dynamic interactions between the passive, active and neuromotor control systems can be adopted to study central nervous system

of shoulder stability (Figure 1.1)

Anterior Shoulder Instability – Rajaratnam B S (2007)

PASSIVE SYSTEM

(anatomical structures)

(bone, glenoid labrum

and caps ule, glenohumeral ligaments,

interarticular pressure)

ACTIVE SYSTEM(muscles)

(rotator cuff and periscapular muscl es including long head of biceps, pectoralis, latissmus, deltoids, trapezius , serratus anterior, rhomboids)

NEUROMOTOR CONTROL SYSTEM

(spinal cord and central ner vous s ystem)

Figure 1.1: Conceptual model of dynamic shoulder stability at the glenohumeral joint (model adopted from Panjabi M.M The stabilizing system of the spine 1 Function, dysfunction, adaptation and enhancement Journal of Spinal Disorders 1992; 5/4: 383-389)

Panjabi (1992) proposed that 80% of cervical spine stability was attributed to the muscular system (active system) while the ligaments, capsules and other passive structures accounted for the remaining 20% Patients with chronic recurrent low back pain had altered anticipatory neuromotor control of their proximal spine and this adversely affected lumbar spinal stability (Hodges & Richardson 1999) Patients with chronic neck pain delayed the activation of their deep cervical flexors, contralateral sternocleidomastoid and anterior scalene muscles during neck flexion (Falla

et al 2004a) The neuromotor control system subconsciously can compensate for structural deficits or local dysfunctions by activating atypical muscle patterns, synergistic muscle alliances and substitution muscle actions that create new subsets of temporary neuromotor maps (Latash & Anson 1996; Lieber & Friden 2000; Schmidt & Wrisberg 2000; O’Sullivan 2000)

Anterior Shoulder Instability – Rajaratnam B S (2007)

The minimally constrained ball and socket GH joint requires significant intra-socket negative pressure and GH ligament-muscle alliances to keep the humeral head centered within the glenoid fossa for stability (Howell & Kraft 1991; Bigliani et al 1996) Unlike the ligaments in the knee, the glenohumeral ligaments do not have the strength characteristics to stabilize the GH joint alone They function in concert with the dynamic shoulder stabilizers and align themselves with numerous scapulo-thoracic and rotator cuff muscles (Bigliani

et al 1996) Also structurally, at least half of the glenohumeral ligaments intermingle with the rotator cuff muscles to contribute to GH joint stability (Clark et al 1990; Lippitt et al 1993; Thompson et al 1996)

Atypical neuromotor control among patients with ASI during elevation was observed as altered muscle recruitment patterns included suppression of the activities of the pectoralis major, supraspinatus and subscapularis, increased peak activation of other rotator cuff muscles and delayed reflex latency of the biceps brachii (Myers et al 2004) Patients with shoulder laxity increased the magnitudes of their biceps and supraspinatus and decreased the recruitment of their pectoralis major, subscapularis, latissimus dorsi and serratus anterior during performance of throwing (Glousman et al 1988) Patients with multidirectional instability also altered the activation patterns of their deltoids and pectoralis major during arm elevation (Morris et al 2004; Barden et al 2004 & 2005) The hallmark of an intact cortical neuromotor maps is it ability to precisely inhibit and excite the agonist and antagonist

Anterior Shoulder Instability – Rajaratnam B S (2007)

shoulder and rotator cuff muscles throughout the range of arm movement for maximal concavity compression (Voigt et al 1998; Diederichen et al 2004)

Re-establishing the appropriate actions of the dynamic shoulder stabilizers before and during shoulder motion are essential neuromotor control strategies that influence articular stability (Ide et al 1996; Hogervorst & Brand 1998; Hodges & Richardson 1999; David et al 2000) Atypical muscle activation patterns also hint towards disrupted feed forward and feedback central nervous system control mechanisms Cadaver studies reported that failure to correct atypical muscles patterns in the unstable shoulder led to further instability (Figure 1.2) However, the identification of atypical shoulder muscle patterns among patients with ASI as they perform overhead elevation tasks has eluded us, probably due to the failure by researchers to quantify the various neuromotor control strategies the central nervous system activates in various planes and ranges of arm elevation during motion

Anterior Shoulder Instability – Rajaratnam B S (2007)

INSTABILITY

Trauma

POOR STABILITY

GOOD STABILITY

Mechanoreceptor damage+Increase sensitivity of nociceptors+Atypical Neuromotor Control

neuromotor retraining

Surgical CorrectionRehabilitation

At ypical neuromotorcontrol strategies

Figure 1.2: Paradigm of shoulder instability Even though surgical correction and rehabilitation aims to re-establish stability at the glenohumeral joint, failure to address atypical neuromotor control strategies due to altered cortical neuromotor maps will lead to further shoulder instability

When the shoulder was placed in the elevated and apprehension arm position and selected shoulder muscles mechanically stimulated, cadaver studies reported reduced infraspinatus activity and increased pectoralis major activity that together increased the anterior shear forces at the GH joint by 143% and pulled the humeral head into an unstable anterior-inferior position (McMahon & Lee 2002; Labriola et al 2005) To compensate for weakened infraspinatus in the late cocking phase of throwing, pitchers with chronic ASI increased their supraspinatus activity (Glousman et al 1988), while patients

Anterior Shoulder Instability – Rajaratnam B S (2007)

with generalized shoulder laxity activated peak supraspinatus activity earlier (Kronberg et al 1991) However, cadaver models indicated that increased supraspinatus activity during overhead elevation generated significant anterior directed translational or shear forces on the head of the humerus that have the potential to destabilize the GH joint (Lee et al 2000) The contradictory findings between cadaver and EMG studies reflect the importance of studying shoulder neuromotor control in vivo Cadaver studies are unable to replicate real-world setting and do not permit the study of how the central nervous system maintains GH joint stability in the presence of shoulder dysfunction

Morphological changes to muscle fibers with increased age affected shoulder muscle strength and movement speed even among the most active older person (Hughes et al 1999) The elderly above 60 years of age experienced a high recurrent shoulder dislocation rate of 22% that was not associated with participation in overhead arm sports or further damages to peripheral structures at the shoulder (Gumina & Postacchini 1997) Hence, age-related peripheral muscle skeletal changes may contribute to altered neuromotor control strategies among the elderly

The association between changes within the active and passive systems and neuromotor control is not well established even thought it is important for the development of better clinical outcomes for patients with ASI Identifying shoulder muscle activation patterns in the different planes of arm elevation provides critical information to understand how the central nervous system establishes cortical neuromotor maps from neural signals recorded by

Anterior Shoulder Instability – Rajaratnam B S (2007)

mechanoreceptors located at the passive and active systems The results could lead to better shoulder rehabilitation programs and thus, better functional outcomes after acute ASI and after surgical correction of the unstable shoulder A thorough quantification of neuromotor control strategies adopted by patients with ASI during the performance of everyday functional reaching tasks is currently lacking

The aim of this thesis was to identify the muscle activation patterns at the shoulder when patients with ASI perform everyday overhead tasks in two planes of arm elevation Their results were compared with healthy young and elderly subjects to evaluate confounding factors that may influence GH joint stability during overhead arm motions

Anterior Shoulder Instability – Rajaratnam B S (2007)

CHAPTER TWO: REVIEW OF THE LITERATURE

The following chapter is a detailed yet concise description of the biomechanics of the shoulder during arm elevation, the muscle alliances at the shoulder joint, and the effects of increased age and changes after stroke

on muscle morphology

2.1 Biomechanics of shoulder elevation

More than 30 muscles coordinate the synchronized actions of the sternoclavicular, acromioclavicular, GH and scapulothoracic (ST) joints to produce smooth and efficient shoulder motions in various planes of arm elevation Although the sternoclavicular and acromioclavicular joints are important joints, the GH and ST joints are the focus of concern and controversy associated with shoulder instability Studying the excursion of the

ST and GH joints during unrestricted arm motions provides insight to how the central nervous system maintains shoulder joint stability by:

a Altering scapulo-humeral rhythm to generate a safe and effective concavity compression zone between the glenoid and the humerus;

b Coordinating the activity of shoulder musculature to perform explosive and injury free shoulder elevation motions

Anterior Shoulder Instability – Rajaratnam B S (2007)

The following discussions are limited to the kinematics of the scapula and, the translation and rotation actions of the humeral head within the glenoid fossa during arm elevation

2.1.1 Scapula kinematics

During elevation, the scapula rotates and tilts about its orthogonal axes with respect to the trunk for maximal GH joint stability (Figure 2.1.1) The initial 60º of elevation or the “setting phase” involves 60 of internal rotation, 20º

of posterior tilting and upward rotation of the scapula (Laumann 1987; Wu & Cavangah 1995) Above 90º of elevation, the scapula rotates at least 16º externally and tilts posteriorly to avoid shoulder impingement of the rotator cuff muscles (Laumann 1987; Lukasiewicz et al 1999; McClure et al 2001) The alignment of the scapula with the trunk also influences the pain-free range of shoulder motion Trunk flexed posture reduced shoulder abduction

by 23.60 compared with an erect trunk posture as humeral translation was more superior and there was more shoulder internal rotation (Kebaetse et al 1999) The rotation and rolling of the humerus within the glenoid fossa minimizes the mechanical energy required to stabilize the GH joint during arm elevation (Saha 1983, Cheng 2005) Hence, any change to scapula excursion during arm elevation would require more humeral axial rotation for joint stability through range (Saha 1983, Karduna et al 2000)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Figure 2.1.1: Schematic representation of the Euler angles at the scapula (From Karduna AR, McClure PW, Michener LA Scapular kinematics: effects of altering the Euler angle sequence

of rotation Journal of Biomechanics 2000;33:1064)

The axis of rotation of the scapula continuously changes during arm elevation From zero to 30º of elevation, the axis of rotation is at the spine of the scapula; thereafter from 30º to 100º of scapula rotation, the axis changes

to an imaginary point between the sternoclavicular joint and the spine of the scapula From 100º onwards, the axis of rotation of the scapula is at the acromioclavicular joint (Peat 1986; Culham & Peat 1993) By changing the axis of rotation of the scapula, shoulder muscles are more efficient (Inman et

al 1944; Doody et al 1970; Paine & Voight 1993) For instance, the initial scapula rotation better positions the deltoids for shoulder elevation

The trapezius, serratus anterior and rhomboids are the most active scapulothoracic muscles in the “setting phase”, and function to position the firm, yet mobile glenoid socket underneath the humerus for maximal concavity compression throughout range (Pronk 1989; Halder et al 2000) Overactivity

of the trapezius and muscle imbalances between the serratus anterior and rhomboids were identified as common compensatory strategies associated

Anterior Shoulder Instability – Rajaratnam B S (2007)

with abnormal scapula movements (Kamkar et al 1993; Paine & Voight 1993; Jobe 1996; Weiser et al 1999) As further evidence, patients with shoulder impingement excessively activated the pectoralis major, rhomboids and levator scapulae for arm elevation above 80º (Ludewig et al 1996; Borstad & Ludewig 2002)

An optimal length-tension relationship between the deltoids and rotator cuff muscles generated sufficient concavity compression and minimal translation of the humeral head within the glenoid fossa (Jobe et al 1984; Pronk 1989; Ludewig et al 1996) However, when temporal and magnitude profiles of the scapulothoracic and rotator cuff muscles were altered during elevation, more anterior glenohumeral translation occurred (Arsenault et al 1991; Paletta et al 1997; Kibler 1998; Weiser et al 1999; Lukasiewicz et al 1999; Endo et al 2001; Baeyens et al 2001) Patients with shoulder impingement syndrome rotated and anteriorly tilted their scapula more in the mid and end ranges of arm elevation to establish an efficient length-tension relationship between the deltoids and rotator cuff muscles (Lukasiewicz et al 1999; Ludewig & Cook 2002) Sixty-four percent of patients with ASI also demonstrated scapula winging and asymmetry during repetitive forward flexion (Warner et al 1992) Thus, the optimal and appropriate sequencing of scapulohumeral rhythm during elevation is an important feature to minimize the translational stress forces at the GH joint (Johnson 1937; McClure et al 2001)

Anterior Shoulder Instability – Rajaratnam B S (2007)

2.1.2 Scapulohumeral rhythm

The classical 2:1 Codman’s ratio between the GH and ST joints during arm elevation actually varied from 1.7:1 to 7.5:1 (Inman et al 1944; Bagg & Forrest 1998; McQuade & Smith 1998; McClure et al 2001) The ratio was not constant through range After 30º of abduction, it was 5:4, 1.5:1 at 60º and 2.4:1 at 120º abduction (Poppen & Walker 1976; Graichen et al 2000) Carrying a light load altered the ratio to 4.3:1 and with a heavier load to 4.5:1, with large inter-individual variability (McQuade & Smith 1998; Pascoal et al 2000) Unfortunately, most studies that quantified scapulohumeral rhythm used techniques such as roentgenographic and goniometric that required subjects to halt the movement periodically through range and thus did not measure dynamic arm motion (Freedman et al 1966; Doody et al 1970; Ludewig et al 1996; McQuade et al 1998) The invasive electromagnetic tracking devices with pins inserted into the scapula were more accurate for dynamic motion studies as the technique does not halt arm movement (McClure et al 2001) Due to the invasive nature of this technique, it is not suitable for clinical application and likely to be confounded by the pain due to the insertion of pins No known non-invasive instrumentation can evaluate scapulohumeral rhythm continuously during motion and through the rull range

of arm elevation in the clinical setting

The GH:ST relationship also varied when there were deficits to the passive and active systems of the shoulder When suprascapular nerve blocks paralyzed the supraspinatus and infraspinatus, the scapula rotated more than normal (McCully et al 2006) Patients with shoulder instability also

Anterior Shoulder Instability – Rajaratnam B S (2007)

demonstrated greater GH joint motion in the first 45º of motion compared to asymptomatic subjects (Glousman et al 1988; Kronberg et al 1991a; McMahon et al 1996; Paletta et al 1997) Cailliet (1981) described the coupling between GH and ST joints as being “programmed for daily activity” Thus, knowing the actual ratio is less important than understanding the appropriate neuromuscular control mechanisms that regulate GH joint stability during the execution of an extensive repertoire of precise functional actions in

an effortless and pain free manner (Michiels & Grevenstein 1995)

Compensatory strategies such as altered shoulder muscle firing patterns facilitated the re-establishment of normal scapulohumeral rhythm especially in the upper quadrants of arm elevation (Basmajian & Bazant 1959; Paine & Voight 1993; Kronberg et al 1991; Scovazzo et al 1991) At the exact time when the serratus anterior exhibited low muscle activity among swimmers with painful shoulders, the scapula rotated and protracted for more upper trapezius and rhomboids motor units to be recruited (Scovazzo et al 1991) Patients with hemiparesis of the upper limb and weak serratus anterior recruited the infraspinatus, teres minor, deltoids and supraspinatus earlier to stabilize the GH joint and sometimes even before movement commenced (Peat & Grahame 1977; Rajaratnam et al 1999a & b; Rajaratnam et al 2006b)

Over time, abnormal muscle recruitment patterns established new sets

of cortical neuromotor maps that become ingrained within the movement repetoire (Babyar 1996) When abnormal muscle activation patterns persisted

Anterior Shoulder Instability – Rajaratnam B S (2007)

after surgical correction of structural deficits associated with ASI, they contributed to further GH joint instability (Paletta et al 1997)

2.1.3 Dynamic glenohumeral stability

A Bankart lesion altered the integrity of the glenoid labrum, the capsule, the rotator interval, glenohumeral and coracohumeral ligaments, and weakened the strength of the rotator cuff and biceps muscles (Warner et al 1995; Bigliani et al 1996) The radii of the humeral head and glenoid fossa are almost equal with no more than 2-3% deviation even though the surface area

of the glenoid fossa does not enclose the entire humeral head (Soslowsky et

al 1992a) The intact inter-socket pressure and ligament compressive forces kept the humeral head centered within the glenoid fossa in the rest position (Howell & Kraft 1991)

Shoulder muscles were actively involved as joint movers to initiate arm elevation, and as joint stabilizers to maintain GH joint stability throughout range of movement (Iannotti et al 1992; Gielo-Perczak et al 2006) The moments generated by the rotator cuff, deltoids and biceps will raise the arm and their contraction generate compressive forces in excess of 0.92 times body weight between 60º to 90º of arm elevation to maintain GH joint stability (Inman et al 1994; Poppen et al 1976; Kronberg et al 1990; Howell & Kraft 1991; Kronberg et al 1991b; Karlsson & Peterson 1992; Malicky et al 1996; Sakurai et al 1998; Gaichen et al 2000; Lee et al 2000) Maximum GH joint contact occurred at 120º of arm elevation (Soslowsky et al 1992b) Obligatory

Anterior Shoulder Instability – Rajaratnam B S (2007)

external rotation during arm elevation above 90º further facilitated greater GH joint stability by shifting the humeral head into a posterior and more centered location within the glenoid fossa (Soslowsky et al 1992; Jobe et al 1995) However, when patients with lesions to the superior portion of the labrum raised their arm overhead into an external rotated position, their humeral head translated more in an anterior direction (Howell et al 1988; Pagnai et al 1995)

In addition, osteoarthritis and old age narrowed the GH joint space (Prescher 2000) Thus, changes in the anatomical structures of the shoulder would increase the magnitude of muscles that generate translational and compressive forces

Saha (1983) postulated that three main factors contributed to dynamic

GH stability during the various stages of arm elevation:

1 normal retrotilt of the glenoid articular surface in relation to the axis

by radiogram could be corrected by rotating the upper shaft of the humerus

Anterior Shoulder Instability – Rajaratnam B S (2007)

and transferring the tendon of the latissimus dorsi to the lowest posterior limit

of the greater tuberosity and the lower insertion of the infraspinatus tendon Theoretically, this reinforced the subscapularis and short posterior steering muscles by holding the humeral head back and lessening its anterior advance

to dislocation

Saha (1983) also developed multiple muscle transfer techniques that also permitted typical accessory movement of the clavicle, scapula and the For instance, during elevation to 60O in flexion or 30O in abduction, the following accessory movements occur:

1 12-15 O of elevation of the outer end of the clavicle;

2 scapular rotation through an antero-posterior axis;

3 counter-clockwise rotation of the scapula round a vertical axis through the acromio-clavicular joint that increases the angle between the scapular spine and the clavicle by about 10O

The muscles around the shoulder are classified into three cone groups:

1 the short cone consist of the supraspinatus, infraspinatus, teres minor and subscapularis,

2 the intermediate cone consist of the teres major, pectoralis major, latissmus dorsi and the deep fibers of deltoid, and

3 the large cone consist of the triceps, long head of the biceps, coracobrachialis and superficial fibers of the deltoid (Saha 1983)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Electromyography studies reveal that in the early phase of abduction, the intermediate cone deltoid muscle precedes the short cone supraspinatus muscle to facilitate mobility However, during flexion the supraspinatus demonstrate an earlier rise to ensure stability before the deltoids facilitates elevation (Saha 1983) The tension of the short cone infraspinatus, teres minor and subscapularis muscles increases again after about 90O of elevation

to facilitate stability (Inman et al 1944) Their actions externally rotate and depress the humeral head for the greater tuberosity to slide underneath the acromium process However, when they are paralysed, the large cone biceps and triceps muscles harness their power to remain stability in the overhead elevation Unbalanced forces at the GH joint will facilitate gliding and development of shear forces between the joint surfaces (Saha 1983)

Moreover, lack of accessory movement and external rotation during elevation will result in the shoulder muscles twisting on themselves and not be able to generate power for mobility and stability (Saha 1983) But when the arm is placed in the overhead position, the three cone groups of muscles are aligned coaxially and, thus loose their rotatory properties

Saha (1983) also pleaded for recognition of the “zero-position” of the GH joint which was defined as that position where the humero-scapular aligned axis coincides with the common axis of the cone muscle groups This position

is when the glenohumeral joint looses all active rotation and estimated to be

at about 165O overhead and 45 O in front of the coronal plane The short cone muscles will provide axial pull to reduce a dislocation arm towards complete

Anterior Shoulder Instability – Rajaratnam B S (2007)

alignment when placed in the zero position and with the application of firm traction,

Although surgical tightening of lax anterior capsules shifted the humeral head into a posterior position within the glenoid fossa, the procedure imposed

an increased joint contact pressure in the opposite direction that resulted in further GH joint instability (Dempster 1965; Blasier et al 1992; Bigliani et al 1996; Abboud & Soslowsky 2002) Contraction of the rotator cuff muscles increased the tension of the GH ligaments and heightened the capsules restraining properties (Halder et al 2000; Kuhn et al 2005)

Results of cadaver studies suggest that the risk of GH joint instability increased when the humeral translational forces exceeded 18º±2º from the centre of the glenoid to the end of the effective glenoid arc; the area of the articular surface available for maximal concavity compression (Labriola et al 2005) This concept called balanced stability angle implies that typically shoulder muscles regulate safe humeral translation during arm elevation (Figure 2.1.4) However, strong contraction of a muscle such as pectoralis major when the arm in placed in the apprehension position would generate a large anterior humeral translation outside the balance stability angle (McMahon & Lee 2002)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Figure 2.1.4: Axial views of GH joint (A) The effective glenoid arc (shaded) is defined as the areas of the glenoid’s articular surface available for humeral head compression (B) The balance stability angle (shaded) is defined as the angle between the center of the glenoid and the end of the effective glenoid arc (From Labriola JE, Lee TQ, Debski RE, McMahon PJ Stability and instability of the glenohumeral joint: The role of the shoulder muscles J Shoulder Elbow Surg 2005; 14:32S-38S)

Ultrasound findings among patients with ASI with their arm placed in the apprehension position indicated that the humeral head translated anteriorly on average 4.9 mm compared with 1.9 mm among asymptomatic subjects The intact passive stabilizers of the GH joint were unable to restrain the large humeral head translation, and had to increase the magnitude of shoulder muscle activations to re-establish maximal concavity compression between the humeral head and the glenoid fossa (Morrey et al 1998; Krarup

et al 1999) Thus, neural signals from joint and muscle mechanoreceptors in the unstable shoulder activate different neuromotor control strategies that present as abnormal muscle activation patterns (Lewis et al 2004)

Joint mechanoreceptors within the capsule, ligaments, labrum, bursa and muscle-tendon junctions transmit neural inputs about position, motion and acceleration of a limb or proprioception to the central nervous system 45% of

Anterior Shoulder Instability – Rajaratnam B S (2007)

the superior glenohumeral ligament, 42% of the middle glenohumeral ligament and 48% of the inferior glenohumeral ligament have mechanoreceptors (Guache et al 1999) The properties of the different types

of shoulder joint mechanoreceptors have been extensively studied (Table 2.1.1)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Table 2.1.1: Classification of human joint mechanoreceptors*

in average size Located where joint capsule links to rotator cuff

a Very slow adapting, high threshold and dynamic mechanoreceptor which detect direction of movement and exact joint position sense

b Together with muscle spindle and Ruffini, sense tension of ligaments in extreme joint positions

c May also influence muscle tone Type 4

(free nerve

endings)

Non-encapsulated unmyelinated close-meshed network of nerve fibers (between 0.5-1.5 µm in diameter)

a Function as fast non-adapting high threshold mechanoreceptors when present in intramuscular connective tissue

b Also located within joint capsule layer

as nociceptors

*Modified from the system introduced by Freeman & Wyke, 1967

Mechanoreceptors are broadly classified as fast adapting Pacinian mechanoreceptors (Pacinian FAMs) and slow adapting Ruffinian mechanoreceptors (Ruffinian SAMs) Their exact locations at the shoulder have not been fully established (Table 2.1.2) Ruffinian SAMs are generally most abundant in the capsuloligamentous structures of the shoulder while Pacinian FAMs outnumber Ruffinian SAMs within the glenohumeral ligaments (Vangsness et al 1995)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Table 2.1.2: Locations of mechanoreceptors in the glenohumeral ligamentous and capsular structures

Pacinian in the subsynovial layers

Ruffinian and GTO

Type 1-4

Guanche et al 1999; Vangsnees et al 1995 Middle

glenohumeral

ligament

Pacinian in the subsynovial layers

Pacinian and Ruffinian

Type 1-4

Jerosch et al 1993;

Vangsnees et al 1995 Inferior

Capsule Pacinian located on lateral aspect of the anterior

and inferior capsule Also Ruffinian

Pacinian and Free nerve endings

Free nerve endings

Ruffinian and GTO at capsulolabral junction

Rare distribution of Pacinian and Free nerve endings in glenoid labrum

(GTO: Golgi tendon organ)

FAMs are sensitive to compression and tension forces during the initiation and termination of movement SAMs respond to continuous tension, and monitor changes in movement and position (Malinovsky 1987a & b; Schuttle et al 1987; Myer & Lephart 2002) Quick stretches stimulate FAMs while sustained low intensity forces heighten the proprioceptive activity of SAMs (Hunt 1990; Jami 1992; Refshauge & Fitzpatrick 1995; Proske et al 2000)

Anterior Shoulder Instability – Rajaratnam B S (2007)

The central nervous system receives neural signals from the mechanoreceptors at the shoulder and regulates shoulder muscles to maintain the humeral head within 1 mm of the glenoid centre throughout elevation in an intact joint (Gauche et al 1999; Steinbeck et al 2003) The central nervous system also utilizes signals from pre-programed (or pre-set) cortical neuromotor maps to increase muscle stiffness and protect the joint from injury even before movement commenced (Jerosch et al 1993; David et

al 2000; Zhang et al 2000) Stretching of the capsuloligamentous complex at the end of range of movement enhances the acuity of the shoulder’s position sense (Janwantanakul et al 2001) However, capsular laxity initiates abnormal muscle activation patterns that resulted in excessive humeral translation during forceful throwing actions in the vulnerable overhead position (Myer & Lephart 2002) The administration of lidocaine to paralyze the shoulder muscles elicited inappropriate muscle activation patterns that led to signs of shoulder instability (Jerosch et al 1993; Vangsness et al 1995; Carpenter et al 1998; Minaki et al 1999)

A dynamic partnership between mechanoreceptors and nociceptors was observed when pitchers with a recent history of shoulder pain due to rotator cuff tendonitis demonstrated significant deficits in proprioception in their affected upper limbs but not their other shoulder (Safran et al 2001) Repeated microtrauma released chemical mediators such as human alpha calcitonin gene-related peptide (CGRP) and the coexisting substance P that further increased nociceptor sensitivity (Konttinen et al 1994; Ide et al 1996;

Anterior Shoulder Instability – Rajaratnam B S (2007)

Yamashita et al 1999) The raised sensitivity of nociceptors signaled Type 3 Golgi Tendon Organ (GTO) mechanoreceptors to recruit muscles in an uncoordinated manner, altered muscle tone and induced willful painful movement (Ide et al 1996; Johnson 1997) In chronic situations, nociceptors maintained their heightened sensitivity state despite the absence of on-going tissue damage or mechanical stress and thus further aggravated GH joint

instability (Konttinen et al 1994; Johnson 1997)

2.1.4 Summary

1 The passive and active systems at the GH joint permits shoulder stability

to co-exist at both rest and during movement Scapula rotation initiated by the active system is an important and dynamic component of arm elevation that generates a safe concavity compression zone between the glenoid fossa and the humeral head

2 Maximal compressive forces at the GH joint occurred between 60º to 90º

of arm elevation Obligatory external rotation during elevation maximized

GH joint contact by shifting the humeral head into a superior-central and posterior location within the glenoid fossa in a stable shoulder joint

3 However, patients with ASI translated the humeral head further forward during arm elevation resulting in less humeral contact with the glenoid fossa compared to asymptomatic subjects In the overhead apprehension

Anterior Shoulder Instability – Rajaratnam B S (2007)

position, their humeral head translated as much as 4.9mm within the glenoid fossa compared to 1.9 mm among asymptomatic subjects

4 Mechanoreceptors located on the capsuloligamentous-muscle structures sense excessive translation of the humeral head and signal from the central nervous system re-program the shoulder muscles to protect the

GH joint from further injury However, repetitive overhead activities by the unstable shoulder elicit inappropriate neuromotor control strategies that alter shoulder muscle activation patterns that further destabilized the shoulder joint

Anterior Shoulder Instability – Rajaratnam B S (2007)

2.2 Muscle alliances at the shoulder joint

The central nervous system regulates the neuromotor control system to create synergisms and substitutions between the GH capsuloligamentous structures and shoulder muscles

2.2.1 Capsuloligamentous-muscle alliances

The capsuloligamentous structures at the GH joint minimize excessive translation of the humeral head within the glenoid fossa at rest and at the end ranges of shoulder motion Unlike the ligaments in the knee, at least half of the glenohumeral ligaments are histologically aligned with the shoulder muscles (Table 2.2.1) For instance, the long head of the biceps tendon has a fibrous sling that intermingles laterally with the superior glenohumeral and coracohumeral ligaments, and together with the rotator interval integrates the fibers of supraspinatus and subscapularis (Jost et al 2000)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Table 2.2.1: Main capsuloligamentous-muscle alliances at the glenohumeral joint

CHL with subscapularis Ferrari 1990; Terry et al 1991; Harryman et al 1992; Neer et al

1992; Blasier et al 199; Werner et al 2000; Kuhn et al 2000 SGHL with long head of

biceps & subscapularis

Turkel et al 1981; O’Brien et al 1990; Ferrari 1990; O’Connell et al 1990; Clark et al 1990; Harryman et al 1992; Clark & Harryman 1992; Warner et al 1992; Itoi et al 1993; Rodosky et al 1994; Pagnani et al 1995; Blasier et al 1997; Werner et al 2000; Jost et

MGHL with subscapularis Turkel et al 1981; Ferrari 1990; O’Brien et al 1990; O’Connell et al

1990; Warner et al 1992; William et al 1994; Werner et al 2004 IGHL complex with

serratus anterior

O’Brien et al1990; O’Brien et al 1995; O’Connell et al 1990; Warner et al 1992; Bigliani et al 1992; Bigliani et al 1996; Soslowsky et al 1997; McMahon et al 1998; McMahon et al 1999; Weiser et al 1999; Kuhn et al 2000; Burkart & Debski 2003; Jost

& Debski 2003; Kuhn et al 2005

IGHL complex with

middle & posterior

deltoids

O’Brien et al 1990; O’Brien et al 1995; O’Connell et al 1990; Warner et al 1992; Bigliani et al 1992; Bigliani et al 1996; Soslowsky et al 1997; McMahon et al 1998; McMahon et al 1999; Kuhn et al 2000; Halder et al 2001a; Burkart & Debski 2003; Jost

et al 2000; Kuhn et al 2005

RI with supraspinatus &

subscapularis, CHL,

SGHL & joint capsule

Harryman et al 1992; Jost et al 2000; Cole et al 2001

RI with long head of

biceps & SGHL

Harryman et al 1992; Werner et al 2000

(CHL coracohumeral ligament, CAL coracoacromial ligament , SGHL superior glenohumeral ligament, MGHL middle glenohumeral ligament, IGHL inferior glenohumeral ligament, RI rotator interval, IR internal rotation, ER external rotation, Abd abduction, Flex flexion, Ext extension)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Neural signals from the mechanoreceptors of capsuloligamentous structures were found to be directly connected to the shoulder muscles in feline studies Subscapular and suprascapular articular nerve spinal reflex networks transmitted signals from capsuloligamentous mechanoreceptors to the long head of biceps, supraspinatus and infraspinatus (Solomonow et al 1996) The reflex networks were hypothesized to be activated automatically without higher central nervous system involvement as their response time was fast (Gauche et al 1995; Solomonow et al 1996) Stretching the inferior capsule and the inferior glenohumeral ligaments during throwing almost instantaneously activated the infraspinatus and teres minor to stabilize the GH joint (Cain et al 1987)

However, Jerosh and colleague (1997) found a long latency period between the time of stimulating the anterior-superior joint capsule and the responses of eight shoulder muscles in anaesthetized humans They suggested that signals from mechanoreceptors were first sent to the central nervous system for processing before delivering efferent information to regulate muscle length and tension For instance, stimulation of the capsule and coracoacromial ligament induced an initial inhibition follow by a pronounce facilitation of the rotator cuff muscles

2.2.2 Muscle alliances

The neuromotor control system delicately balances the actions of the agonist and antagonist muscles for both mobility and stability to coexist at the

Anterior Shoulder Instability – Rajaratnam B S (2007)

GH joint as it moves through space (Voigt et al 1998; Diederichsen et al 2004) Before movement commenced, the neuromotor control system initiated feed-forward signals to activate appropriate muscles to stabilize the GH joint (David et al 2000; Falla et al 2004b) On-going feedback from mechanoreceptors of limbs moving through range signaled the central nervous system to regulate muscle activities that minimize excessive humeral translation at the GH joint (Nichols 2002) However, even a small amount of repetitive activation of muscle imbalances generated a new cortical neuromotor map that further threatened GH joint stability during arm elevation (Hayashi et al 2002)

In the lumbar spine, stability in the neutral zone involves the dynamic interaction between local and global muscle systems (Bergmark 1989; Hodge

& Richardson 1996; Allison et al 1997) The local muscle system consisting of intrinsic muscles increase muscle stiffness for segmental stability (O’Sullivan

et al 1997a) while the global muscle system involving the large muscles facilitate mobility Injury to the spine altered the timings and magnitudes of both groups of muscle systems and elicited inappropriate balance reflexes and poor righting responses (O’Sullivan et al 1997b; O’Sullivan 2000) Patients with chronic neck pain delayed their recruitment of the deep cervical flexors, contralateral sternocleidomastoid and anterior scalene muscles when they flexed their neck (Falla et al 2004a) Delayed activation of the transverse abdominus also occurred among patients with chronic low back pain (Hodges

& Richardson 1999) The altered recruitment of both local and global muscles was ineffective to maintain joint stability and resulted in tissue failure (Figure

Anterior Shoulder Instability – Rajaratnam B S (2007)

2.2.1) Thus, high loads that induce structural instability would lead to altered and low muscle activities that would overload and irritate the soft tissues and result in further increase risk of instability and injuries (Cholewicki & McGill 1996)

Figure 2.2.1: Hypothetical model for injury risk to the spine due to tissue failure and spine instability While high loads can cause injury by tissue disruption, instability at low loads may allow sufficient local joint movement to overload or irritate soft tissue (from Cholewicki J & McGill SM Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain Clinical Biomechanics 1996; 11/1:1-15)

Patients with ASI who had their supraspinatus and infraspinatus paralyzed rotated their scapula further upwards to re-establish the normal kinematics between the humeral head and the glenoid fossa (Howell et al 1991; McCully et al 2006) Patients also altered the activities of the latissmus dorsi, teres major and subscapularis at extreme shoulder positions (Halder et

Anterior Shoulder Instability – Rajaratnam B S (2007)

al 2001a; Steinbeck et al 2003; McCully et al 2005) These results suggested that the purpose of compensatory or substitution muscle alliances in the unstable GH joint was to facilitate GH joint stability However, the exact temporal-spatial pattern of shoulder muscle activations at the unstable shoulder are relatively unknown even though substitution muscle alliances or synergisms among lower limb musculatures are well established (Sirin & Patla 1987; McLean & Goudy 2004)

Synergistic muscles are not the antagonistic muscle of the primary muscle but the additive contributors that facilitate joint stability by acting either

in a trade-off or co-activation manner with the primary muscle (Basmajian & DeLuca 1985) Trade-off muscle synergism allows the primary muscle to decrease its force magnitude when influenced by pain or fatigue while the synergistic muscle increases its contribution to compensate and facilitate joint stability Co-activating synergistic muscles facilitates and works collaboratively with the primary muscles to maximize voluntary contraction and delay the onset of fatigue (Nieminen et al 1995; McLean & Goudy 2004) Besides regulating the magnitude of muscles, altering the timing of muscle activations facilitated joint stability For instance, besides synergistically recruiting the serratus anterior and rotator cuff muscles when performing skillful throwing sports, early activation of the upper trapezius in the setting phase of arm elevation prevented shoulder dislocation and reduced the risk of shoulder impingement (Myer et al 2005; Tripp et al 2006)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Some researchers reported that substitution muscle alliances can also contribute to joint dislocation (McMahon & Lee 2002; Labriola et al 2005) For example, stimulation of the tight pectoralis major muscle in the unstable shoulder resulted in less compressive forces at the glenoid fossa and more anterior translation of the humeral head during horizontal abduction (Blasier et

al 1997; McMahon & Lee 2002) Recruitment of the anterior deltoid also increased the anterior translation of the humeral head when arms of cadavers were placed in extension and at 600 of abduction (Lee & An 2002; Labriola et

al 2005) The presence of altered shoulder muscle activations in the apprehension position among patients with atraumatic shoulder instability may explain why they commonly experience shoulder dislocation in this position (Eisenhart-Rothe et al 2002) In the same study, patients who experienced shoulder instability due to trauma recruited the dynamic stabilizers to re-center their humeral head in the overhead arm position The different cortical neuromotor maps adopted by patients who experience either trauma or atraumatic shoulder instability have not been explored Hence, understanding how the neuromotor control system coordinates the muscle activation patterns

at the unstable shoulder can facilitate the design of more effective programmes in the acute and post-surgical phase of rehabilitation

To understand the local muscle actions better, the synergistic properties of the trapezius muscle will be reviewed first The muscle has a number of fascicles that are orientated from 110 to 800 direction from the horizontal to draw the clavicle backwards and medially (Johnson et al 1994) The upper and lower fibers of the trapezius together with the serratus anterior

Anterior Shoulder Instability – Rajaratnam B S (2007)

work in concert to rotate the scapula upward with zero net force at the GH joint (Johnson et al 1994) However, excessive recruitment of the upper trapezius negatively increases the compression forces at the sternoclavicular joint (Basmajian & Deluca 1985; Johnson et al 1994) The average physiological cross-sectional area (PCSA) of the upper trapezius is 2.34 to 4.01cm2, and consists of 51%-57% of slow twitch fibers (Karlsson & Peterson 1992; Nieminen et al 1995) The muscle generates in excess of 350 Newtons that is second only to the force generating capacity of the infraspinatus (Nieminen et al 1995) The muscle’s lines of action and it’s sacromere force-length relationship below 1500 of elevation favors shoulder flexion and abduction rather than extension or adduction (Laursen et al 1998; Klein et al 1999)

Table 2.2.2 lists the biomechanical properties of the shoulder muscles including the supraspinatus, infraspinatus, subscapularis, teres minor and major and deltoids Data from cadavers indicates that there is a correlation between PCSA of a muscle and its force generation capability Moreover, the subscapularis and teres major generate substantial greater forces than the shoulder external rotators The infraspinatus and subscapularis have large force generating capacity and greater potential moments as joint movers than the supraspinatus (Kuechle et al 2000; An 2002)

Anterior Shoulder Instability – Rajaratnam B S (2007)

Table 2.2.2: Physiological properties of shoulder muscles {from: 1) Howell et al: Clarification

of the role of the supraspinatus muscle in shoulder function The Journal of Bone and Joint Surgery 1986, 68: 398-404; 2) Bassett et al: Glenohumeral muscle force and moment mechanics in a position of shoulder instability Journal of Biomechanics 1990; 23:405-415; 3) Veeger et al Inertia and muscle contraction parameters for musculoskeletal modeling of the shoulder mechanism Journal of Biomechanics 1991; 24 (7), 615-629}

length (cm)

Muscle belly length (cm)

PCSA in cm2 (%

contribution

of MCSh*)

Volume

in cm3(% mean)

Moment arm about COH* (cm)

Potential moments in

N cm-1 (SD)

(5.6%)

47.6 (3.48)

(23.0) Infraspinatus

(+ teres minor)

(13.4%)

123.0 (8.96)

Biceps

(1.9%)

59.05 (4.24)

Anterior Shoulder Instability – Rajaratnam B S (2007)

head and to reduce capsuloligamentous strains (Sharkey & Marder 1995; Labriola et al 2004) The infraspinatus-teres minor alliance also pulls the humeral head posterior by 4mm to centre the humeral head within the glenoid fossa and limits excessive external rotation of the humerus (Cain et al 1987; Kronberg et al 1989; Sharkey & Marder 1995; Arwert et al 1997; Wuekler et al 1998; Lee et al 2000) During the initiation of abduction, the direction of the lines of action of the supraspinatus was upward but changed with increased elevation and external rotation to a horizontal plane (Sharkey & Marder 1995; Labriola et al 2004) At 60º of elevation, contraction of the supraspinatus contributed to 10.6% of GH joint stability, decreased to 4.4% at 90º of elevation and remained unchanged at 2.6% at 120º of arm elevation (Poppen

& Walker 1978; Graichen et al 2001) Below 30º of arm elevation, the direction

of its lines of action was anterior but shifted to a posterior direction with increased elevation (Labriola et al 2004) When the arms of cadaver models were positioned in the apprehension position, the direction of the lines of action of the supraspinatus changed to an anterior position and this action potentially could destabilize the GH joint

Anterior Shoulder Instability – Rajaratnam B S (2007)

Table 2.2.3 Lines of action (in degrees) from medial direction to a superior-inferior (SI) and anterior-posterior (AP) directions in various ranges of arm elevation and rotation* (from Labriola et al Active stability of the glenohumeral joint decreases in the apprehension position Clinical Biomechanics 2004; 19: 801-809)

position

300 ext rot

SI (A0)

AP (B0)

SI (A0)

AP (B0)

SI (A0)

AP (B0)

SI (A0)

AP (B0)

*{-ve value for (A) is inferiorly directed; -ve value for (B) is posteriorly directed}

The directions of the lines of action of the subscapularis and teres major were anterior throughout arm elevation They are primary shoulder movers as their lines of actions generate large degrees of deviation from the centre of the glenoid fossa (potential moments) The direction of the lines of action of the deltoids suggests that they are GH joint movers during the initiation of abduction The middle deltoid is an abductor from 0º to 60º of arm elevation while the anterior deltoid contributes only after 15º of elevation The

Anterior Shoulder Instability – Rajaratnam B S (2007)

anterior deltoid also contributes as an internal rotator whereas the middle and posterior fibers contributes mainly as external rotators

The dynamic interaction between the internal and external shoulder rotators centralized the head of the humerus within the glenoid fossa throughout the ranges of arm elevation Moreover, arm elevation requires an

“obligatory” external rotation of 35º to achieve full range of shoulder motion (Johnson 1937; Browne et al 1990; Kuechle et al 2000) External rotation shortens the tendon of the teres minor and infraspinatus to generate large potential moments in both the sagittal and coronal planes of elevation (Table 2.2.4) The subscapularis generates the largest internal rotation potential moments in all planes of elevation and this counteracted the external rotation moments generated by infraspinatus and teres minor The supraspinatus and the anterior deltoid generated internal rotation potential moments in the sagittal plane but external rotation potential moments in the coronal plane of arm elevation (Ihashi et al 1998; Kuechle et al 2000)