Princeton, New Jersey, USA
Monday 24th March 2014

Whilst there was a rather lengthy gap between the posts regarding the range of movement components of shoulder impingement rehabilitation & those aiming to address the first element of the lack of muscle performance, I am making sure I waste no time continuing on to the final part of the equation.

As I discussed in the last post, the second stage of the muscle performance rehabilitation procedure that Cools et al (2013) describe involves developing the muscle control & strength necessary for executing daily activities.

This is where the algorithm points in the direction of concentrating on “muscle control & co-contraction” to improve control during simple activities, or “muscle strengthening” according to what has come to light in the objective assessment. 

The key here is to identify any imbalances of the scapular muscles & ensure you choose exercises that enable the patient to selectively activate weaker muscles (or muscle portions), whilst minimally activating more hyperactive muscles.

Cools et al (2008) recommend that because excessive activation of the upper trapezius is often combined with a lack of activation of the serratus anterior, lower and middle trapezius muscles, it is particularly important to be aware of the upper traps:lower traps, upper traps:middle traps and upper traps:serratus anterior balance ratios throughout.

Cools et al (2007) compared muscle activation ratios during 12 commonly used scapular exercises using surface electromyography (EMG).  Each exercise was conducted through three distinct phases over three seconds (concentric, isometric & eccentric), following a familiarisation with no resistance. The authors identified four exercises with low upper traps:lower traps or upper traps:middle traps ratios deemed suitable for addressing intramuscular balance:  

  1. Side-lying forward flexion (UT:LT)
  2. Side-lying external rotation (UT:LT)
  3. Prone horizontal abduction with external rotation (UT:MT)
  4. Prone extension in neutral position (UT:MT)

The authors were unable to find an exercise that strengthened the serratus anterior, whilst sufficiently inhibiting upper trapezius muscle activation, thus promoting inter-muscular balance.  Ludewig et al (2004) reported relatively low upper traps:serratus anterior activation during most of the push-up modalities they tested but Cools et al (2007) were not able to replicate these exercises with such low levels of upper trapezius activation.  

The issue that Cools et al (2007) identified with all four of these exercises is that they are all conducted in either side or prone lying positions, which prevents their integration into a global functional kinetic chain pattern by employing diagonal patterns combined with trunk & lower limb stabilisation.  

As a result, Cools et al (2008) suggest that these exercises should be used in the early stages of the muscle control & strength phase, as a pre-cursor to more functional exercises.

Barreto et al (2012) investigated the percentage activation of the serratus anterior & lower trapezius muscles during a different variety of five exercises.  

Whilst Cools et al (2007) relied on the testers to apply resistance, Barreto et al (2012) used a load of 2kg to achieve a desired activation of between 20% & 40% of maximum voluntary contraction.  This was to ensure that the outcome had a positive influence on the motor control, as opposed to developing muscle strength or encouraging adaptive movements with recruitment of other muscle fibres.

Barreto et al suggest that the results achieved by Cools et al (2007) would have had more of an effect on developing muscle strength, given the maximum voluntary contraction nature of the exercises.  The fatiguing nature of the protocol stipulated in the earlier study is also discussed, with the authors voicing the opinion that the reliability of the results may have been subsequently compromised.  

It must be remembered,however, that Cools et al (2007) were trying to address comparative co-contraction ratios by recruiting under-active muscle groups, whilst inhibiting the over-active ones to attain a change in the motor pattern.  

That said, when De Mey et al (2012) incorporated the four exercises recommended by Cools et al (2007), they reported that whilst the exercise programme was able to elicit changes in the activation level of the scapular muscles, they could not alter the timing of the muscle activation during arm elevation in the scapular plane.  

So it would be interesting to repeat that study but modifying the recruitment levels to those advocated by Barreto et al (2012) & subsequently reevaluating the timing of muscle activation.

Barreto et al (2012) chose the modified military press, pull over, low row, modified crucifix & escalation exercises because they were predominantly conducted in an open kinetic chain, requiring minimal scapular control, whilst avoiding scapular or trunk compensation.  Subjects conducted one set of five reps, with an interval of at least one minute between exercises.

The results of the study demonstrated that the highest percentage of maximum voluntary contraction in the serratus anterior muscle was achieved during the scapation exercise, where the subject stood whilst performing 130º elevation in the scapular plane, with the forearm in neutral.  

Adequate activation to promote neuromuscular reeducation of the serratus anterior was also reported during a modified military press, with the subject seated, upper limbs abducted to 90º in the plane of the scapula, 90º elbow flexion and shoulder forearm pronation.

The highest percentage of maximum voluntary contraction in the lower trapezius muscles was recorded during the scapation & low row exercises, with both intensities being adequate for neuromuscular reeducation.

Given the importance of limiting the percentage of maximum voluntary contraction when conducting these exercises, I have found that athletes, in particular need close supervision & constant reminding not to exceed the effort of contraction advised.  Athletes tend to subscribe to the “if it’s not hard work, it’s not doing me much good” mantra & so a clear, simple explanation as to the reasons behind the protocol is imperative.

De Mey et al (2013) report that in open kinetic chain low row exercises, a unilateral stance on the contralateral leg increases scapular muscle activity, whilst also improving the upper trapezius:lower trapezius ratio.  They further suggest that conducting the exercises in sitting or whilst adopting a bilateral stance does not favour optimal scapular muscle balance.

Whilst the open kinetic chain exercises require minimal scapular control & avoid scapular or trunk compensations, it is important to also address closed kinetic chain exercises in this second phase of the programme.  Closed kinetic chain exercises improve the dynamic stability of the glenohumeral joint through stimulation of the intra-articular & peri-articular proprioceptors, which enhance the co-contraction of the rotator cuff muscles.

Hardwick et al (2006) investigated the ability of the wall slide exercise to activate the serratus anterior muscle at & above 90º of humeral elevation.  

The wall slide exercise requires subjects to stand facing a wall, with their dominant foot against the foot of the wall & the opposite foot, shoulder width apart & behind the front foot.  Elbows & shoulders start at 90º flexion, with the ulnar border of the forearms against the wall.  Shoulders are elevated in a plane approximating the scapular plane.  Subjects then slide their forearms up the wall, leaning into it by transferring weight from the back foot to the front foot, before finishing with their forearms in maximum shoulder elevation.  The investigator provides the verbal cue “bring your shoulder blades out & around as you slide up the wall”.

They compared the 3D position of the thorax, scapula & humerus along with the muscle activity of the serratus anterior, the upper & lower trapezius and the latissimus dorsi muscles during the wall slide, a wall push-up plus & scapation.

The results of the study led the authors to conclude that the wall slide was an effective exercise to recruit the serratus anterior muscle at & above 90º of shoulder elevation but that it was not significantly different from activation levels achieved during the push-up plus or scapation exercises.

The push-up plus exercise is favoured by many of the studies I have reviewed here (De Mey et al, 2013; Cools et al, 2007; Cools et al, 2013).  In comparison to the push-up plus exercise, Hardwick et al (2006) suggested that the wall slide exercise does activate the serratus anterior muscle above 90º elevation, which may be important in overhead sports, where the altered scapular kinematics often give rise to painful symptoms & impingement.  

The wall slide is also less likely to put the glenohumeral joint in a position that decreases the subacromial space in the presence of scapular dyskinesis (Cools et al, 2013).

Whereas Hardwick et al (2006) suggested the dominant leg was always in front of the non-dominant leg during testing of the wall slide exercise, they do not stipulate whether this should vary when working with a pathological subject related to the arm affected.  

Maenhout et al (2010) investigated the activation of the serratus anterior & lower trapezius muscles & how they were influenced by integrating kinetic chain components into the exercise.  They reported that increased serratus anterior activity was obtained if the ipsilateral leg was extended during the push-up plus exercise, whereas lower trapezius activity improved if the contralateral leg was extended.

The third stage of the muscle performance rehabilitation procedure that Cools et al (2013) describe involves general scapular strengthening exercises, which should be introduced once muscle balance is restored, with the aim of increasing muscle strength.

It is during this stage that advanced scapular muscle control components must be addressed, along with integrating strength into sport-specific movements, which incorporate the kinetic chain in addition to introducing eccentric & plyometric exercises.

If I consider former athletes I have worked with, it is at this stage where the rehabilitation programmes of my throwers would look dramatically different to those of my swimmers, basketball players, tennis players, rugby hookers, American football quarterbacks or kayakers.  Not only would the positions that I conducted the exercises in be different, the nature of the resistances applied would vary considerably to address the specific demands of the ranges, speeds & consistency of force application which are unique to each athlete.

Ellenbecker & Cools (2010) discuss various techniques that can be utilised throughout the various stages of rehabilitation.  As the challenges progress, they recommend introducing oscillatory & rhythmic stabilisation techniques, before then introducing more sporadic external demands through the use of perturbations delivered by the clinician.  Exercise duration should reflect the stamina of the muscle group being worked at any one time.

Isokinetic machines can be integrated into the programmes to focus on developing faster, more functional contractile velocities in order to build up to overhead tasks such as those required by tennis players, basketball players or quarterbacks, for example.

Medicine balls can be used to incorporate plyometrics into the repertoire, which will help develop both concentric & eccentric rotator cuff strength.

In addition to improving the strength & control at greater speeds, local muscle endurance must also be addressed.  As such, reps & sets must be modified to address the physiological demands the clinician is trying to address at each specific stage.  Ellenbecker & Cools (2010) advise prescribing 3 sets of 15-20 reps for developing local muscular endurance, however, there are several options you can use to achieve the desired result.

Holmgren et al (2012) investigated the use of eccentric exercises to strengthen the rotator cuff, whilst using concentric/eccentric exercises to focus on strengthening the scapular stabilisers in patients with scapular impingement.  They reported successful outcomes in reducing pain & improving the overall prognosis after a twelve week exercise period, which incorporated six or seven physiotherapy sessions consisting of manual mobilisation & exercise review.

Maenhout et al (2013) added heavy load eccentric training to the experimental group of a population of patients with subacromial impingement to compare the effects to those assigned to a more traditional rotator cuff training group.  

The authors measured isometric strength at 0º, 45º & 90º of scapular abduction as well as in internal & external rotation.  After a 12 week period, which also included 9 physiotherapy sessions, both groups had demonstrated significant isometric strength gains in all directions, along with significant decreases in pain.  However, the heavy load eccentric training group showed a 15% higher gain in abduction strength at 90º of scapular abduction compared to the traditional exercise group.

Return to play criteria have not been extensively reported in the literature that I have read.  McCarty et al (2004) suggest returning to play once little or no pain is reported, in addition to subjective satisfaction of treatment by the patient, near normal range of movement & strength along with normal functional ability & sport-specific skills.  However, it really is an area that requires more research to provide more stringent guidelines for clinicians but there are some groups doing some great work out there so it’s definitely an evolving field.

I hope that my run through the literature has been food for thought, although I do recommend taking time to read through the references below to compare the methodologies & being aware of the limitations of each.

I’d be interested to hear from any of you that have developed your own assessment & management algorithms, to see which schools of thought have significantly influenced your practice. 

Barreto, R.P.G. et al (2012).  Lower trapezius & serratus anterior activation: which exercise to use for scapular neuromuscular reeducation?  ConS Saúde; 11(4): pp660-667

Cools, A.M. et al (2007).  Rehabilitation of scapular muscle balance: which exercises to prescribe?   Am J Sports Med; 35: pp1744-1751

Cools, al (2008).  Internal impingement in the tennis player: rehabilitation guidelines.  Br J Sports Med; 42: pp165-171

Cools, A.M. et al (2013).  Rehabilitation of scapular dyskinesis: from the office worker to the overhead athlete.  Br J Sports Med; 48(8): pp 675-676

De Mey, K. et al (2012).  Kinetic chain influences on upper & lower trapezius muscle activation during eight variations of a scapular retraction exercise in overhead athletes.  J Sci Med Sport; 16: pp65-70

Hardwick, D.H. et al (2006).  A comparison of serratus anterior muscle activation during a wall slide exercise & other traditional exercises.  J Orthop Sports Phys Ther; 36: pp 903-910

Kibler, W.B. & Sciascia, A. (2010).  Current concepts: scapular dyskinesis.  Br J Sports Med; 44: pp300-305

Lewis, J.S. et al (2005).  Subacromial impingement syndrome: the effect of changing posture on shoulder range of movement.  J Orthop Sports Phys Ther; 35: pp72-87

Ludewig, P. et al (2004).  Relative balance of serratus anterior and upper trapezius muscle activity during push-up exercises.  Am J Sports Med; 32: pp484-493

Lunden, J.B. et al (2010).  Shoulder kinematics during the wall push-up plus exercise.  J Shoulder Elbow Surg; 19: pp216-223

Maenhout, A.G. et al (2010).  Electromyographic analysis of knee push-up plus variations: what is the influence of the kinetic chain on scapular muscle activity?  Br J Sports Med; 44: pp1010-1015

Maenhout, A.G. et al (2013).  Does adding heavy load eccentric training to rehabilitation of patients with unilateral subacromial impingement result in better outcome?  A randomised clinical trial.  Knee Surg Sports Traumatol Arthrosc; 21(5): pp1158-1167

McCarty, E.C. et al (2004).  Shoulder instability: return to play.  Clin Sports Med; 23: pp335-351

Mottram, S.L. et al (2009).  Motion analysis study of a scapular orientation exercise & subjects’ ability to learn the exercise.  Man Ther; 14: pp13-18

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