Scapular dyskinesis: Patterns, functional disability and associated factors in people with shoulder disorders

Accepted Manuscript Scapular Dyskinesis: Patterns, Functional Disability and Associated Factors in People with Shoulder Disorders Tsun-Shun Huang, Chien-ying Huang, Hsiang-Ling Ou, Jiu-Jenq Lin PII:

S1356-689X(16)30709-3

DOI:

10.1016/j.math.2016.09.002

Reference:

YMATH 1903

To appear in:

Manual Therapy

Received Date: 11 May 2016 Revised Date:

12 August 2016

Accepted Date: 3 September 2016

Please cite this article as: Huang T-S, Huang C-y, Ou H-L, Lin J-J, Scapular Dyskinesis: Patterns, Functional Disability and Associated Factors in People with Shoulder Disorders, Manual Therapy (2016), doi: 10.1016/j.math.2016.09.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Scapular Dyskinesis: Patterns, Functional Disability and Associated Factors in People with Shoulder Disorders Tsun-Shun Huang1, Chien-ying Huang1, Hsiang-Ling Ou1, Jiu-Jenq Lin1, * 1

School and Graduate Institute of Physical Therapy, College of Medicine, National

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Taiwan University, Taipei, Taiwan

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* Corresponding author. E-mail: [email protected]

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Abstract Background: Patterns of scapular dyskinesis have unique scapular kinematics and

be associated with functional disability.

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associated muscular activation. The characteristics of unique dyskinesis patterns may

Objectives: To investigate whether the shoulder function level and primary

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dysfunction items were different in unique dyskinesis pattern. The factors associated

Design: Cross-sectional study

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with shoulder dysfunction in different dyskinesis patterns were identified.

Methods: Fifty-one participants with unilateral shoulder pain were classified as having a single dyskinesis pattern (inferior angle prominence, pattern I; medial border

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prominence, pattern II) or a mixed dyskinesis pattern (patterns I+II). Clinical measurements with the Flexilevel Scale of Shoulder Function (FLEX-SF), shoulder

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range of motion and pectoralis minor index were recorded. These clinical

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measurements, 3-D scapular kinematics (electromagnetic-based motion analysis), and associated muscular activation (electromyography on the upper/middle/lower trapezius and serratus anterior muscles) during arm elevation were analyzed for associations with functional disability. Results: We found FLEX-SF scores and primary dysfunction items were similar among the patterns of dyskinesis. In inferior angle prominence, increased shoulder

ACCEPTED MANUSCRIPT function was associated with decreased upper trapezius activity (R2=0.155, p=0.035), which accounted for approximately 16% of the variance of FLEX-SF scores. In medial border prominence, increased shoulder function was associated with increased

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lower trapezius activity (R2=0.131, p=0.017), which accounted for approximately 13% of the variance of FLEX-SF scores.

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Conclusion: Upper and lower trapezius activities are important to consider in the

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evaluation of patients with pattern I and II, respectively. No other factors were related to shoulder dysfunction due to insufficient challenge of arm elevation tasks.

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Keywords: scapular dyskinesis, function, predictive factor

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Introduction Scapular dyskinesis is defined as abnormal scapular position and motion.(Kibler et al., 2013) Common signs of scapular dyskinesis are medial border prominence or inferior angle

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prominence, early scapula elevation or shrugging during arm elevation, and abnormal

scapulohumeral rhythm during arm elevation/lowering.(Kibler et al., 2002, McClure et al.,

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2009) Previous studies demonstrated that 33 to 100 percent of patients with various shoulder

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disorders, including glenohumeral instability, rotator cuff disorders, and labral tears, have scapular dyskinesis.(Kawasaki et al., 2012, Myers et al., 2013, Paletta et al., 1997, Warner et al., 1992) Recent study showed that the prevalence of scapular dyskinesis was 61 percent in overhead athletes, which was significantly higher than nonoverhead athletes (33%).(Burn et

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al., 2016) As a result, evaluation of scapulothoracic joint is an essential part for restoring

population.

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shoulder dysfunction in patients with shoulder disorders, especially in an overhead athletic

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Alterations of muscular activation or coordination and tightness of soft tissues have been reported to be associated with scapular dyskinesis.(Kibler et al., 2013) First, scapular muscles (the upper trapezius, UT; lower trapezius, LT; serratus anterior, SA) are coordinated as force couples in task-specific movements to control the position and motion of the scapula.(Magarey and Jones, 2003) Abnormal scapular kinematics can result from uncoordinated force coupling. Excessive activity of the UT muscle combined with reduced 1

ACCEPTED MANUSCRIPT activity of the LT and SA muscles have been observed in patients with shoulder impingement.(Cools et al., 2003, Ludewig and Cook, 2000) Second, tightness of the muscles or ligaments may change scapular kinematics. Shortening of the pectoralis minor or the short

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head of the biceps can result in excessive scapular anterior tilt and downward

rotation.(Borstad and Ludewig, 2005, Ellenbecker and Cools, 2010) Third, posterior shoulder

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muscles or capsules can create excessive scapular internal rotation and anterior tilt.(Laudner

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et al., 2010)

Kibler et al. classified scapular dyskinesis into 4 movement patterns: inferior scapular border prominence, medial scapular border prominence, superior scapular border prominence, and the symmetric pattern.(Kibler et al., 2002) A modified method for comprehensive testing

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of scapular dyskinesis involves classifying scapular dyskinesis into a single pattern or mixed patterns according to visual observation combined with palpation in the raising and lowering

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phases, respectively, and provides higher reliability than does the method of Kibler et

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al.(Huang et al., 2015a) In addition, specific alterations of scapular muscular activation and kinematics have been found in different patterns of scapular dyskinesis.(Huang et al., 2015b) Given that shoulder dysfunction is associated with alteration of scapular movement and muscular activation, and with soft tissue shortening, in unique patterns of scapular dyskinesis, we believed that finding different patterns of abnormalities could provide further information on how to treat specific problems associated with scapular dyskinesis. Flexilevel Scale of 2

ACCEPTED MANUSCRIPT Shoulder Function (FLEX-SF) with 15 shoulder functional movement in daily activities was used to represent shoulder functional level and chose several important biomechanical/clinical factors such as scapular kinematics and muscular activation, shoulder range of motion,

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anterior/posterior shoulder tightness and pectoralis minor index to find the association between these factors and shoulder dysfunction level in different patterns of scapular

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dyskinesis. The purposes of this study were (1) to investigate whether shoulder dysfunction

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items were related to unique patterns of scapular dyskinesis, and (2) to investigate the related

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factors associated with shoulder dysfunction in unique patterns of scapular dyskinesis.

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Methods In this cross-sectional study, function-related factors in patients with different patterns of scapular dyskinesis were investigated. Fifty-one participants (40 males; age= 22.5±2.4 years;

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height=171.4 ± 8.0 cm; weight= 64.9 ± 10.5 kg) were recruited from an outpatient clinic of a university hospital and through local Internet media. Participants were included if they (1)

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were from 18 to 50 years old, (2) had unilateral shoulder pain around the glenohumeral joint

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while performing shoulder movement and (3) had scapular dyskinesis. Participants were excluded if they had a history of shoulder dislocation, fracture, or shoulder surgery within the past 1 year, or a history of direct contact injury to the neck or upper extremities within the past 1 month, or neurological disorders from cervical region, or inability to perform full angle

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of arm elevation in scapular plane. All eligible volunteers gave written and informed consent prior to participation. The study was approved by the Institutional Review Board of the

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Instrumentations

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National Taiwan University Hospital.

The surface EMG (sEMG) assemblies included pairs of silver chloride circular (recording diameter of 10 mm) surface electrodes (The Ludlow Company LP, Chocopee, MA) with an interelectrode (center-to-center) distance of 20 mm, and a Grass AC/DC amplifier (Model 15A12, Astro-Med Inc. RI, USA) with a gain of 1,000, a common mode rejection ratio of 86dB at 60 Hz, and a bandwidth (-3dB) of 10 to 500 Hz. The sEMG data were collected at 4

ACCEPTED MANUSCRIPT 1,000Hz/channel using a 16-bit analog to digital converter (Model MP 150, Biopac systems Inc., CA, USA). An impedance meter (Model F-EZM5, Astro- Med Inc., Ri, USA) was used to measure the impedance between the electrodes over the muscle with the value less than 10

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kΩ. The electrodes were placed over the upper/middle/lower trapezius (UT/MT/LT) and

serratus anterior (SA) muscles using previously established methods.(Huang et al., 2013,

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Perotto and Delagi, 1994)

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The Polhemus 3Space FASTRAK system (Polhemus Inc., Colchester, VT, USA) was used for collecting 3-dimensional kinematic data of the scapula. According to the manufacturer, the accuracy of the FASTRAK system is 0.8 mm and 0.15 degrees. Karduna et al.(Karduna et al., 2001) confirmed that the skin-based method is valid when arm elevation is below 120 degrees.

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The details of the methodology can be found in a previous paper.(Lin et al., 2005) The sensors were placed at the sternum and the flat surface of the acromion with adhesive tape. The third

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sensor was attached to the distal humerus with Velcro straps. Anatomic landmarks used in a

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previous study were palpated and marked with a stylus by a physical therapist.(Huang et al., 2015b) These marks were used for subsequent receiver mounting and landmark digitization. The transmitter served as a global reference frame and was fixed to a rigid plastic base and oriented such that it was level and its coordinate axes were aligned with the cardinal planes of the human body. Procedures 5

ACCEPTED MANUSCRIPT Male participants were asked to remove their shirts, and females were asked to wear halter tops. Participants were instructed to practice arm elevation in the scapular plane and become familiar with the tempo of a metronome. Participants were asked to elevate their arms, using

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the thumb-up position, to the end range over a 3-second count and then to lower them. The dumbbells in each hand weighed 2.3 kg (5 lb) or 1.4 kg (3 lb), depending on each participant’s

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ability to elevate the arm (Fig 1). Participants performed 6 trials of bilateral, active, weighted

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arm elevation in the scapular plane and a therapist classified the scapular motion into specific patterns of scapular dyskinesis. (Huang et al., 2015a) The therapist had 4 years of specific clinical/research experience related to glenohumeral and /or scapulothoracic joint. Next, the kinematics and sEMG data were collected during 5 trials of weighted arm elevation in

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scapular plane. Then maximal voluntary isometric contraction (MVIC) was tested and used to normalize the sEMG data.(Huang et al., 2015b, Kendall F and McCreary E, 2010) The

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MVICs were collected for 5 seconds and 3 trials with 1 minute of rest between 2 trials.

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Visual combined palpation was used for the classification of the scapular dyskinesis pattern (single pattern or mixed patterns) in both the raising/lowering phases. The four single patterns were inferior angle prominence (pattern I), medial border prominence (pattern II), abnormal scapular upward rotation/elevation (pattern III), and normal movement (pattern IV) (Fig 2). A previous study showed the inter-rater reliability of this comprehensive classification

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ACCEPTED MANUSCRIPT test was moderate (κ=0.49) and moderate to substantial (κ/κw=0.57/0.64) in the raising and lowering phases, respectively.(Huang et al., 2015a) In self-reported flexilevel scale of shoulder function (FLEX-SF), participants answer a

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single question that grossly classifies their function level as low, medium, or high. Then they respond to 15 items that target only their levels of function. Scores range from 1 to 50, and

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higher scores indicate less limitation of shoulder function.(Cook et al., 2003)

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The length of the pectoralis minor from the medial-inferior angle of the coracoid process to the sternocostal junction of the inferior aspect of the fourth rib was measured with a digitizing sensor of an 3-D motion system.(Borstad, 2008) This method is normalized to patient height to determine the relative length as the pectoralis minor index, which is

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calculated by dividing pectoralis minor length by participant height and multiplying by 100.(Borstad and Ludewig, 2005)

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For the assessment of posterior and anterior shoulder tightness, horizontal adduction

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ROM and horizontal abduction ROM were measured, respectively, in supine position with an inclinometer.(Lin and Yang, 2006) A greater ROM indicates more flexibility of posterior/anterior shoulder soft tissues. Passive ROM of shoulder internal and external rotation were also assessed. The passive internal and external rotation was measured with the humerus placed at the starting position of 90 degrees of shoulder abduction in supine position

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ACCEPTED MANUSCRIPT and the scapula stabilized. The angle measured by the inclinometer was recorded by the second tester. Data reduction

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Raw kinematic data were low-pass filtered at a 6-Hz cutoff frequency and converted into anatomically defined rotations. Shoulder joint coordinate system was constructed following

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the ISB guidelines.(Wu et al., 2005) The absolute axes defined by the sensors of the

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FASTRAK device were converted to anatomically defined axes. Scapular orientation relative to the thorax was described using a Euler angle sequence of rotation about Zs (protraction/retraction), rotation about Y's (downward /upward rotation), and rotation about X"s (posterior/anterior tipping). Full bandwidth sEMG data, captured by data acquisition

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software (AcqKnowledge, Biopac systems Inc., CA, USA), were reduced using a root mean square (RMS) algorithm to produce sEMG envelopes with an effective sampling rate of 50

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samples per second and normalized to the MVIC. The EMG data for each muscle were

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averaged for each phase of the middle 3 trials. A phase was defined by a trigger marked and synchronized on the sEMG data and scapular kinematics data. The kinematic data at 30, 60, 90, and 120 degrees and EMG data for the ranges of 0-30 degrees, 30-60 degrees, 60-90 degrees, 90-120 degrees, and above 120 degrees in the raising and lowering phases were used as dependent variables. Statistical Analysis 8

ACCEPTED MANUSCRIPT The Statistical Package for the Social Sciences (SPSS) 17.0 was used for data analysis. The Shapiro-Wilk test was performed to confirm normal distribution of outcomes. First, one-way ANOVA was used to investigate the FLEX-SF scores of different patterns of

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scapular dyskinesis. Descriptive statistics were calculated to demonstrate three primary

dysfunction tasks (most complaint among participants) in each pattern of scapular dyskinesis.

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Bonferroni correction was used to adjust for multiple pair-wise comparisons. The significance

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value was set at p<0.05. Second, stepwise multiple linear regressions were used to determine the relationships between shoulder function scores and all related factors if the assumptions of normality and linearity were met. Data of participants with pattern I+II dyskinesis were included in both the pattern I and the pattern II groups for final analysis. Pairwise associations

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between continuous variables were checked if any related factors were strongly correlated (r > 0.8) to avoid problems of multicollinearity. Related factors were entered into the model if they

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were associated with the FLEX-SF score (p<0.2). Those predictive factors were included in

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the final regression model if they were associated with FLEX-SF score with a p value of less than 0.05.

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Results Primary shoulder dysfunction items There were no differences in FLEX-SF scores among these patterns. For the questions on

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the FLEX-SF, 3 participants completed the medium function subscale, and 48 participants, the high function subscale. Of the 15 items, 2 items were scored “no difficulty” by the 48

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participants. The three primary dysfunction items (most complaint among participants) for

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each dyskinesis pattern were found in the following 4 tasks: (1) weighted overhead, (2) pull weight back to front, (3) reach back, and (4) overhead 2 min (Table 1). Predictive factors of shoulder dysfunction

Tests for normality and linearity revealed that the data were normally distributed and

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pairwise associations appeared linear. Furthermore, the predictive factors of shoulder dysfunction were analyzed by separating the data for inferior angle prominence from that of

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medial border prominence. Twenty-nine and 43 participants were included in pattern I and

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pattern II, respectively (Table 2). Pattern III dyskinesis was not included in final analysis due to insufficient numbers of participants. For inferior angle prominence, the variables associated with the FLEX-SF scores were entered into the stepwise regression model (p<0.2; Table 3). These were posterior tipping at 60 degrees of arm lowering (PTL60), internal rotation at 60 degrees of arm lowering (IRL60) and upper trapezius activity during 90 to 60 degrees of arm lowering (UTL9060). Only one 10

ACCEPTED MANUSCRIPT variable, UTL9060, was related to the FLEX-SF score (standardized β=-0.394, R2=0.155, p=0.035). This model indicated that higher FLEX-SF scores can be predicted by lower UTL9060. This predictor accounted for approximately 16% of the variance of FLEX-SF scores.

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For medial border prominence, the variables associated with FLEX-SF scores were

entered into the stepwise regression model (p<0.2; Table 3). These variables were external

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rotation ROM, posterior shoulder tightness and lower trapezius activity during 60 to 30

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degrees of arm lowering (LTL6030). Only one variable, LTL6030, was correlated with FLEX-SF scores (standardized β=0.362, R2=0.131, p=0.017). This model indicated that higher FLEX-SF scores are associated with higher LTL6030. This predictor accounted for approximately 13% of the variance of FLEX-SF scores. Detailed information of correlations

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between FLEX-SF score and all predictive factors were shown in Appendix 1.

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Discussion Scapular dyskinesis has been reported to be associated with functional disability.(Lopes et al., 2015) We wanted to further investigate (1) the relationship between dyskinesis patterns

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and shoulder dysfunction and (2) to determine whether the characteristics of shoulder

dysfunction varied according to dyskinesis patterns. Regarding our first purpose, the findings

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demonstrated that dysfunction levels and the major limited items of the FLEX-SF scale were

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similar among pattern I, pattern II, and pattern I+II dyskinesis. For our second purpose, different predictive factors were associated with functional disability in patients with inferior angle and medial border prominence. Previously, specific alterations of scapular kinematics and muscular activation in unique patterns of scapular dyskinesis have been reported.(Huang

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et al., 2015b) As a result, we believed that classification of dyskinesis patterns is an essential part of evaluation for the patients. In present study, despite similarities in the level of

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dysfunction among dyskinesis patterns were found, effective rehabilitation strategies may be

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specific to unique impairments for each pattern. Specific impairments in each unique dyskinesis pattern may not be directly related to functional disability. Presumably, inferior angle prominence is related to the angle of scapular posterior tipping, the flexibility of the pectoralis minor, and lower trapezius/serratus anterior activity.(Borstad and Ludewig, 2005, Neumann, 2010) Medial border prominence is also thought to be associated with the angle of scapular internal rotation, posterior shoulder 12

ACCEPTED MANUSCRIPT tightness, and middle trapezius/serratus anterior activity.(Laudner et al., 2010, Neumann, 2010) Interestingly, we found that upper trapezius activity was the only factor associated with functional disability in patients with inferior angle prominence. Additionally, the lower

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trapezius activity was the only factor associated with functional disability in patients with medial border prominence. Indeed, when our expected factors were entered into the

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regression model, low R square values were found (R2=0.268 and 0.106 for dyskinesis

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patterns I and II, respectively).

Decreased upper trapezius activity and increased lower trapezius activity were related to higher levels of shoulder function. Our findings are consistent with previous findings that a combination of excessive activity of the upper trapezius and reduced activity of the lower

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trapezius muscle has been observed in patients with shoulder impingement.(Cools et al., 2003, Ludewig and Cook, 2000) The upper trapezius functions as a scapular elevator and secondary

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upward rotator and controls the scapular movement as force couples with the lower trapezius

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and serratus anterior.(Neumann, 2010) Patients with inferior angle prominence may exhibit insufficient lower trapezius and serratus anterior recruitment to control anterior tipping of the scapula. As a result, while the upper trapezius plays a greater role in scapular upward rotation and simultaneous excessive scapular elevation, imbalances in the recruitment of the upper and lower trapezius and serratus anterior may increase the risk of subacromial impingement and influence shoulder function. On the other hand, the lower trapezius generates scapular upward 13

ACCEPTED MANUSCRIPT rotation and posterior tipping and stabilizes the glenoid for constant axis of rotation of the humerus for arm elevation.(Neumann, 2010) The serratus anterior and middle trapezius control the medial border of the scapula to avoid winging. Patients with medial border

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prominence may have insufficient serratus anterior and middle trapezius activity to control the internal rotation of the scapula. As part of a force couple to control scapular movement, the

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lower trapezius needs to assist scapular external rotation and upward rotation to effect

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shoulder movement. As a result, therapists need to provide treatment to restore scapular muscle balance by inhibiting upper trapezius activity and facilitating lower trapezius activity. Some predictive factors that were not significantly correlated with shoulder function are worthy of mention. First, it was surprising to find no significant correlation between shoulder

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function and each pattern of scapular kinematics or serratus anterior muscle activation. Previous studies had reported that altered scapular movement, including decreased upward

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rotation, posterior ripping, and external rotation, were found in patients with shoulder

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disorders (Ludewig and Cook, 2000; Timmons et al., 2012). Additionally, serratus anterior muscle activation has been proposed to be associated with altered scapular kinematics (Ludewig and Cook, 2000; Cools et al., 2004). In the present study, performing a few arm elevations in the scapular plane with 3 or 5 pound loads may not have been as challenging to the subjects as functional activities. Thus, no significant correlation was found. On the other hand, decreased upper trapezius and increased lower trapezius activity appeared to be related 14

ACCEPTED MANUSCRIPT to higher shoulder function in these elevation tasks. The recruitment of inhibiting upper trapezius and facilitating lower trapezius muscle is important to consider in rehabilitation programs for subjects with symptomatic dyskinesis. Second, pectoralis minor length was not

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related to shoulder function. Shortening of the pectoralis minor muscle length lower than 7.65 has been shown to produce more scapular internal rotation (Borstad and Ludewig, 2005). All

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participants in the present study had a length higher than 7.65, which may explain why no

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significant correlation was found between length and shoulder function. Future studies will need to investigate the kinematics and muscular activity in other challenging functional tasks and include patients with shortening of the pectoralis minor muscle length. The predictive factors accounted for only about 13-16% of the variance of the FLEX-SF

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scores in patients with inferior angle or medial border prominence. Several possible reasons should be provided for this finding. First, the participants were included if they were able to

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complete the entire experiment with only slight discomfort in order to avoid the pain effect on

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EMG collection. Scapular plane elevation with 3 or 5 pounds may not have been sufficiently challenging to cause shoulder dysfunction, which was mentioned in previous paragraph. Second, several functional daily activities in the FLEX-SF score, including reaching behind and forward, touching the middle or lower back, and so on, were reported to be difficult by the participants. Despite reporting difficulties in several functional activities, subjects may not have had dysfunction in our selected arm elevation movement. As a result, the presented 15

ACCEPTED MANUSCRIPT impairments of scapular kinematics and muscular activation during arm elevation may underestimate their functional disability as only 13-15% of the variance of the FLEX-SF scores. Third, the small sample size may have had insufficient power to provide a stable

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regression model. Future studies will need to investigate the kinematics and muscular activity in other challenging functional tasks with a larger sample in order to fully understanding the

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factors related to shoulder dysfunction in patients with scapular dyskinesis.

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Other limitations of this study were as follows. First, the use of surface electrodes during dynamic movements cannot exclude the influence of movement artifacts and crosstalk. However, a 6-Hz filter and the less than 10 kΩ skin resistance of the EMG data reduced the potential influence.(Cools et al., 2003) Additionally, adjacent electrodes pairs were placed

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more than 2 cm apart to minimize the effects of crosstalk from the other muscles.(Huang et al., 2013) Second, our study focused only on 4 superficial scapulothoracic muscles, including 3

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parts of the trapezius and the serratus anterior, which have been shown to play primary roles

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in scapulothoracic motion. Third, in the current study, the participants’ male to female ratio was 4:1. Since no studies to date have investigated the factors related to functional activity between genders, the effects of gender on such factors is unknown. Therefore, the current results should be generalized to a specific gender with caution. Fourth, subjective qualification of difficulty was used in the FLEX-SF scale to measure shoulder function in the current study. However, this type of qualification ("little", "some") may have confounded the 16

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should be conducted to validate the current findings.

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Conclusion Similar levels of dysfunction and the primary dysfunction items of the FLEX-SF scale were identified among 3 dyskinesis patterns. During arm elevation, upper and lower trapezius

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activities were associated with functional disability in patients with inferior angle and medial border prominence, respectively. However, these factors accounted for only a low percentage

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of the variance of the FLEX-SF scores. Although altered scapular kinematics and serratus

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anterior activity have been reported in patients with shoulder disorders, no relation of these factors to shoulder dysfunction was found in the current study. In addition to the arm elevation task, complex functional tasks should be investigated to validate the relations

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between these factors and functional tasks.

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References Borstad JD. Measurement of pectoralis minor muscle length: validation and clinical application. J Orthop Sports Phys Ther. 2008;38:169-74. Borstad JD, Ludewig PM. The effect of long versus short pectoralis minor resting length on scapular kinematics in healthy individuals. J Orthop Sports Phys Ther. 2005;35:227-38.

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Burn MB, McCulloch PC, Lintner DM, Liberman SR, Harris JD. Prevalence of Scapular Dyskinesis in Overhead and Nonoverhead Athletes: A Systematic Review. Orthop J Sports Med. 2016;4:2325967115627608.

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Cook KF, Roddey TS, Gartsman GM, Olson SL. Development and psychometric evaluation of the Flexilevel Scale of Shoulder Function. Med Care. 2003;41:823-35. Cools AM, Witvrouw EE, Declercq GA, Danneels LA, Cambier DC. Scapular muscle recruitment patterns: trapezius muscle latency with and without impingement symptoms. Am

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J Sports Med. 2003;31:542-9. Cools AM, Witvrouw EE, Declercq GA, Vanderstraeten GG, Cambier DC. Evaluation of isokinetic force production and associated muscle activity in the scapular rotators during a protraction-retraction movement in overhead athletes with impingement symptoms. Br J Sports Med. 2004;38:64-8. Ellenbecker TS, Cools A. Rehabilitation of shoulder impingement syndrome and rotator cuff injuries: an evidence-based review. Br J Sports Med. 2010;44:319-27.

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Huang HY, Lin JJ, Guo YL, Wang WT, Chen YJ. EMG biofeedback effectiveness to alter muscle activity pattern and scapular kinematics in subjects with and without shoulder impingement. J Electromyogr Kinesiol. 2013;23:267-74. Huang TS, Huang HY, Wang TG, Tsai YS, Lin JJ. Comprehensive classification test of scapular dyskinesis: A reliability study. Man Ther. 2015a;20:427-32. Huang TS, Ou HL, Huang CY, Lin JJ. Specific kinematics and associated muscle activation in

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individuals with scapular dyskinesis. J Shoulder Elbow Surg. 2015b;24:1227-34. Karduna AR, McClure PW, Michener LA, Sennett B. Dynamic measurements of three-dimensional scapular kinematics: a validation study. J Biomech Eng. 2001;123:184-90. Kawasaki T, Yamakawa J, Kaketa T, Kobayashi H, Kaneko K. Does scapular dyskinesis affect top rugby players during a game season? J Shoulder Elbow Surg. 2012;21:709-14. Kendall F, McCreary E. Muscle Testing and Function. 5th ed. Baltimore, Md: Williams & Wilkins; 2010. Kibler WB, Ludewig PM, McClure PW, Michener LA, Bak K, Sciascia AD. Clinical implications of scapular dyskinesis in shoulder injury: the 2013 consensus statement from the 'Scapular Summit'. Br J Sports Med. 2013;47:877-85. Kibler WB, Uhl TL, Maddux JW, Brooks PV, Zeller B, McMullen J. Qualitative clinical evaluation of scapular dysfunction: a reliability study. J Shoulder Elbow Surg. 2002;11:550-6. 19

ACCEPTED MANUSCRIPT Laudner KG, Moline MT, Meister K. The relationship between forward scapular posture and posterior shoulder tightness among baseball players. Am J Sports Med. 2010;38:2106-12. Lin JJ, Hanten WP, Olson SL, Roddey TS, Soto-Quijano DA, Lim HK, et al. Functional activities characteristics of shoulder complex movements: Exploration with a 3-D electromagnetic measurement system. J Rehabil Res Dev. 2005;42:199-210. Lin JJ, Yang JL. Reliability and validity of shoulder tightness measurement in patients with

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stiff shoulders. Man Ther. 2006;11:146-52. Lopes AD, Timmons MK, Grover M, Ciconelli RM, Michener LA. Visual scapular dyskinesis: kinematics and muscle activity alterations in patients with subacromial impingement

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syndrome. Arch Phys Med Rehabil. 2015;96:298-306. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80:276-91. Magarey ME, Jones MA. Dynamic evaluation and early management of altered motor control

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around the shoulder complex. Man Ther. 2003;8:195-206. McClure P, Tate AR, Kareha S, Irwin D, Zlupko E. A clinical method for identifying scapular dyskinesis, part 1: reliability. J Athl Train. 2009;44:160-4. Myers JB, Oyama S, Hibberd EE. Scapular dysfunction in high school baseball players sustaining throwing-related upper extremity injury: a prospective study. J Shoulder Elbow Surg. 2013;22:1154-9. Neumann DA. Kinesiology of the Musculoskeletal System: Foundations for Physical

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Rehabilitation. 2nd ed. Philadelphia: Mosby; 2010. Paletta GA, Jr., Warner JJ, Warren RF, Deutsch A, Altchek DW. Shoulder kinematics with two-plane x-ray evaluation in patients with anterior instability or rotator cuff tearing. J Shoulder Elbow Surg. 1997;6:516-27. Perotto A, Delagi EF. Anatomical guide for the electromyographer : the limbs and trunk. 3rd ed. Springfield, Ill., USA: Charles C. Thomas; 1994.2013;32:1288-98.

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Timmons MK, Thigpen CA, Seitz AL, Karduna AR, Arnold BL, Michener LA. Scapular kinematics and subacromial-impingement syndrome: a meta-analysis. J Sport Rehabil 2012;21:354-70. Warner JJ, Micheli LJ, Arslanian LE, Kennedy J, Kennedy R. Scapulothoracic motion in normal shoulders and shoulders with glenohumeral instability and impingement syndrome. A study using Moire topographic analysis. Clin Orthop Relat Res. 1992:191-9. Wu G, van der Helm FC, Veeger HE, Makhsous M, Van Roy P, Anglin C, et al. ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion--Part II: shoulder, elbow, wrist and hand. J Biomech. 2005;38:981-92.

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ACCEPTED MANUSCRIPT Table 1: Descriptive data of primary shoulder dysfunction tasks in unique pattern of scapular dyskinesis Pattern I

II

I+II

Place an object (4 kg) on a shelf overhead (Weighted overhead)

RI PT

Difficulty

Little

2 (29%)

8 (38%)

8 (40%)

Some

2 (29%)

1 (5%)

2 (10%)

(Pull weight back to front) Little

4 (57%)

8 (38%)

Some

1 (14%)

1 (5%)

Little

4 (57%)

Some

0 (0)

11 (55%) 0 (0)

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Reach the middle of your back (Reach back)

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Pull a medium weight object (2-5 kg) from the back seat to the front seat of the car

6 (29%)

4 (20%)

0 (0)

2 (10%)

Work overhead for more than 2 minutes (Overhead 2min) Little

3 (43%)

Some

0 (0)

6 (29%)

8 (40%)

1 (5%)

1 (5%)

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Inferior angle of scapula prominence (pattern I), medial border of scapula prominence (pattern II), inferior angle combined medial border of scapula prominence (pattern I+II)

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ACCEPTED MANUSCRIPT Table 2: Participants demographic data (8 participants in pattern I, 22 participants in pattern II, 21 participants in pattern I+II) Pattern II included

Pattern I

Pattern I+II Total

Pattern II

Pattern I+II Total

Mean± SD

Mean± SD

Mean± SD

Mean± SD

Mean± SD

Mean± SD

Number

8

21

29

22

21

43

Sex

M= 5

M= 15

M= 20

M= 20

M= 15

M= 35

Age (yrs)

21.6 ± 3.0

22.0 ± 2.1

21.9 ± 2.3

23.2 ± 2.3

22.0 ± 2.1

22.6 ± 2.2

Height (cm)

169.4 ± 8.4

170.4 ± 8.6

170.2 ± 8.4

173.1 ± 7.3

170.4 ± 8.6

171.8 ± 8.0

Weight (kg)

61.3 ± 7.3

63.2 ± 8.3

62.7 ± 8.0

67.8 ± 12.7

63.2 ± 8.3

65.6 ± 10.9

Duration of symptoms (month)

12.7 ± 16.8

17.9 ± 22.1

16.4 ± 20.6

18.6 ± 17.8

17.9 ± 22.1

18.2 ± 19.8

Dominant side

R: 8

R: 20

R: 28

R: 19

R: 20

R: 39

Involved side

R: 8

R: 18

R: 26

R: 16

R: 18

R: 34

FLEX-SF score

40.8 ± 5.0

42.6 ± 5.0

43.4 ± 4.7

42.6 ± 5.0

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RI PT

Pattern I included

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Abbreviations: M: male, R: right Inferior angle of scapula prominence (pattern I), medial border of scapula prominence (pattern II), inferior angle combined medial border of scapula prominence (pattern I+II)

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ACCEPTED MANUSCRIPT Figure Legends Figure 1: Scapular plane elevation task. (A) Active, weighted, bilateral arm elevation in scapular plane with (B) kinematics sensors placed on sternum, flat surface of acromion, and

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distal humerus and EMG electrodes placed on upper/middle/lower trapezius and serratus anterior muscle.

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Figure 2: Scapular dyskinesis patterns with specific alteration of scapular kinematics. Pattern I (inferior angle of scapular prominence), pattern II (medial border of scapular prominence),

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pattern III (excessive/inadequate scapular upward rotation or elevation), combination of above

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patterns, and pattern IV (normal scapular movement).

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Figure 1.

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RI PT

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Figure 2.

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ACCEPTED MANUSCRIPT Appendix 1: Correlations between FLEX-SF score and all predictive factors. Predictive factors

Correlation to FLEX-SF score (r) Pattern II included

GIR ROM, GER ROM

-0.062, 0.181

-0.147, 0.282*

PST, AST

0.044, -0.089

-0.282*, 0.112

PMI

0.065

0.176

PTL120, PTL90, PTL60, PTL30

-0.076, -0.217, -0.319*, -0.211

-0.077, -0.119, -0.064, 0.005

IRL120, IRL90, IRL60, IRL30

-0.082, 0.063, 0.284*, 0.213

-0.082, -0.104, -0.060, -0.026

URL120, URL90, URL60, URL30

0.146, 0.079, -0.053, -0.179

0.210, 0.156, 0.100, -0.017

UTLup120, UTL12090, UTL9060,

-0.159, -0.321*, -0.394*,

-0.148, -0.176, -0.147,

UTL6030, UTL300

-0.393*, -0.197

-0.077, 0.116

MTLup120, MTL12090,

0.094, 0.122, 0.083,

-0.028, -0.027, -0.041,

MTL9060, MTL6030, MTL300

0.093, -0.100

-0.012, 0.053

LTLup120, LTL12090, LTL9060, LTL6030, LTL300

-0.158, -0.158, -0.116, -0.025, -0.086

0.034, 0.147, 0.277*, 0.362*, 0.247*

SALup120, SAL12090, SAL9060, SAL6030, SAL300

-0.006, 0.045, -0.099, -0.213, -0.199

0.018, -0.003, -0.083, -0.126, -0.013

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RI PT

Pattern I included

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Abbreviations: GIR/GER: internal/external rotation of glenohumeral joint; ROM:

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range of motion; PST/AST: posterior/anterior shoulder tightness; PMI: pectoralis minor index; PT: posterior tipping; IR: internal rotation of scapula; UR: upward rotation of scapila; UT: upper trapezius activity; MT: middle trapezius activity; LT: lower trapezius activity; SA: serratus anterior activity; Lup120: arm elevation angle interval from highest degree to 120 in lowering phase; L120~90: arm elevation angle interval from 120 to 90 degree in lowering phase

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*: correlation between FLEX-SF score and predictive factors (p<0.2)

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Lower upper trapezius activity is related to higher shoulder function in pattern I More lower trapezius firing is related to higher shoulder function in pattern II Low R square value for predicting shoulder function during light weight elevation

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Highlights Similar dysfunction level and limited tasks are found among dyskinesis patterns