Biomechanical measures in participants with shoulder pain: Intra-rater reliability

Manual Therapy xxx (2015) 1e8

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Original article

Biomechanical measures in participants with shoulder pain: Intra-rater reliability Lori A. Michener a, *, Kevin A. Elmore b, Benjamin J. Darter b, Mark K. Timmons c a

Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA 90089, USA Department of Physical Therapy, Virginia Commonwealth University, Richmond, VA 23298, USA c School of Kinesiology, Marshall University, Huntington, WV 25755, USA b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 April 2015 Received in revised form 23 October 2015 Accepted 24 October 2015

Biomechanical measures are used to characterize the mechanisms of treatment for shoulder pain. The objective was to characterize test-retest reliability and measurement error of shoulder surface electromyographic(sEMG) and kinematic measures. Individuals(n ¼ 12) with subacromial pain syndrome were tested at 2 visits. Five repetitions of shoulder scapular plane elevation were performed while collecting sEMG of the upper trapezius(UT), middle trapezius(MT), lower trapezius(LT), serratus anterior(SA) middle-deltoid, and infraspinatus muscles during ascending and descending phases. Simultaneously, electromagnetic sensors measured 3-dimensional kinematics of scapular internal/external rotation, upward/downward rotation, posterior/anterior tilt, and clavicular elevation/depression and clavicular protraction/retraction. Kinematic and sEMG variables were reduced for the total phase of ascending and descending elevation (30 e120 , 120 e30 ), at 30 intervals for sEMG, and at every 30 discrete kinematic angle. The intraclass correlation coefficients(ICC) ranged from 0.08 to 0.99 for sEMG and 0.23e0.95 for kinematics. Correspondingly, the standard error of the measurement(SEM) and minimal detectable change(MDC) for sEMG measures varied from 2.3% to 103.8% of a reference contraction(REF-contraction). For kinematics, the SEM and MDC varied from 1.4 to 5.9 . Between-day reliability was good to very good, except for scapular internal/external rotation kinematics, and sEMG for the LT, UT, and SA. sEMG error values were highest (>25%REF-contraction) for most of the LT, UT, and SA variables. Kinematic error values indicate changes or differences of 2 e3 are meaningful, except for upward/downward rotation and internal/external rotation with MDCs of 4 e6 . Generally, data from the total phase of movement had better reliability and lower error than the data from sEMG interval or kinematic discrete angles. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Scapula Rotator cuff Impingement syndrome Kinematics Electromyography

1. Introduction The shoulder is a common site for musculoskeletal injury. Subacromial pain syndrome which includes rotator cuff disease is a shoulder disorder with multi-faceted biomechanical mechanisms. Manual therapy interventions are often used to address the biomechanical shoulder impairments and restore shoulder function. Evidence indicates that manual therapy can be effective for some patients, but it is not clear why manual therapy is not helpful for all patients with shoulder pain (Ho et al., 2009; Kromer et al., 2009; Gebremariam et al., 2014). To enable treatment decision-

* Corresponding author. Division of Biokinesiology and Physical Therapy, University of Southern California, 1540 E. Alcazar Street, CHP 155, Los Angeles, CA 90089, USA. Tel.: þ1 323 442 0247; fax: þ1 323 442 1515. E-mail address: [email protected] (L.A. Michener).

making, a better understanding of how manual therapy works is needed (Bialosky et al., 2008). Specifically, identification of those impairments that improve with manual therapy and are associated with improved functional outcomes. Biomechanical impairments can be studied by using kinematics and surface electromyography (sEMG) techniques to elucidate the mechanisms of the effects of the manual therapy. Biomechanical mechanisms of the effects of manual therapy can be studied with kinematic analysis and surface electromyography (sEMG), to characterize shoulder motion and muscle activity. A meta-analysis (Timmons et al., 2012) reported altered kinematics of decreased scapular upward rotation, external rotation and posterior tilt, and decreased clavicular elevation and retraction during active arm elevation in the scapular plane in those with subacromial pain syndrome. These altered scapular motions may be caused by or lead to dysfunctional scapular and rotator cuff muscle

http://dx.doi.org/10.1016/j.math.2015.10.011 1356-689X/© 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Michener LA, et al., Biomechanical measures in participants with shoulder pain: Intra-rater reliability, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.10.011

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L.A. Michener et al. / Manual Therapy xxx (2015) 1e8

activity. A systematic review (Chester et al., 2010) described abnormal scapular muscle activity of increased upper trapezius, along with decreased middle trapezius, serratus anterior, deltoid and infraspinatus activity in individuals with subacromial pain syndrome. Improvements in shoulder muscle activity and kinematics have been demonstrated after exercise (DeMey et al., 2012) and spinal manipulation in patients with shoulder pain (Muth et al., 2012; Haik et al., 2014b). Kinematic and sEMG methods used to measure the mechanistic effects of manual therapy should demonstrate acceptable measurement properties which include reliability and error metrics. Reliability studies are needed of shoulder kinematic and sEMG techniques used to assess the biomechanical impairments targeted with manual therapy. Prior reliability studies of dynamic shoulder kinematics have largely used healthy individuals or in participants with cerebral palsy, (Thigpen et al., 2005; Myers et al., 2006; Roren et al., 2013; Scibek and Carcia, 2013; Lempereur et al., 2014) thus limiting the application of these findings to patients with shoulder pain. One study has reported reliability for shoulder kinematics in patients with shoulder pain, however reliability was limited to 3 of the 5 scapular kinematic variables (Haik et al., 2014a). The reliability of sEMG shoulder muscle activity has only been studied in healthy individuals (Seitz and Uhl, 2012). Because reliability estimates can vary between healthy and impaired individuals (Harris et al., 2005; Wagner et al., 2008), studies are needed to characterize the measurement properties for sEMG and to extend the understanding for kinematics in individuals with shoulder pain. Estimates of inter-session reliability can extend our understanding of the reliability and error when measures are taken longitudinally over time in patients with shoulder pain. The purpose of this study was to characterize the test-retest inter-session reliability and measurement error of shoulder kinematics and sEMG in individuals with subacromial pain syndrome related shoulder pain. 2. Methods 2.1. Participants Participants (n ¼ 12) seeking treatment for shoulder pain were recruited from local clinics (Table 1). Inclusion criteria for subacromial pain syndrome was 3 or more positive tests of painful arc, pain or weakness with resisted external rotation, Neer, HawkinseKennedy and Jobe/Empty Can tests (Michener et al., 2009; Hegedus et al., 2012). Exclusion criteria included adhesive capsulitis (50% loss of passive shoulder external rotation and 25% loss of shoulder elevation), history of upper arm fracture, systemic musculoskeletal disease, shoulder surgery, cervical motion reproducing shoulder pain, or a full thickness rotator cuff tear (positive ultrasound or MRI imaging). The study was approved by Virginia Commonwealth University Internal Review Board, and all participants provided written informed consent. An a priori power analysis indicated a sample size of 10 participants was adequate; hypothesizing a relationship of 0.80 (95%CI ¼ 0.55, 0,92), power >0.80 and significance level of 0.05, a sample size of 10 would be adequate (Weir, 2005; Hertzog, 2008). 2.2. Procedures Participants completed 2 test sessions, separated by a mean of 5.2 (3e6) days based on participant availability to return for testing. The Pennsylvania Shoulder Scale(Penn) (Leggin et al., 2006) measured shoulder pain, satisfaction, and function with daily activities (0e100; 100 ¼ full use). Scapular 3-dimensional kinematics and sEMG of shoulder muscle activity of the participants' symptomatic shoulder were assessed during arm elevation and lowering

Table 1 Participant demographics and characteristics (n ¼ 12). Variable

Distribution

Age (years); mean (sd) Weight (kg); mean (sd) Height (cm); mean (sd) Body mass index (kg/m2); mean (sd) Male gender; n (%) Dominant arm; n (%) Initial visit Penn Shoulder Score (0e100; 100 ¼ no disability) Pain (0e30, 30 ¼ no pain) Satisfaction subscale (0e10, 10 ¼ fully satisfied) Function subscale (0e60, 60 ¼ full function) Re-test visit Penn Shoulder Score (0e100; 100 ¼ no disability) Pain (0e30, 30 ¼ no pain) Satisfaction subscale (0e10, 10 ¼ fully satisfied) Function subscale (0e60, 60 ¼ full function)

49.2 90.3 178.0 28.3 8 10

(14.7) (22.2) (7.2) (5.7) (66.7) (83.3)

78.9 22.9 6.1 49.9

(8.8) (4.3) (2.4) (8.8)

77.8 24.9 6.0 46.9

(8.2) (3.4) (2.1) (8.1)

in the scapular plane defined as 40 anterior to the frontal plane (Karduna et al., 2001). Starting with the arm at the side of the body, the participant raised their arm with their thumb pointing towards the ceiling, to maintain a position of mid-range humeral rotation. Elevation was standardized to a 3-s count during the ascending and descending phases to control for effects of velocity (Roy et al., 2008). Arm elevation in the scapular plane was monitored visually to ensure that the plane of elevation was maintained. Participants held weights during testing; 1.4 kg (3-lb) for those under 68.1 kg and a 2.3 kg (5-lb) weight for those over 68.1 kg (Tate et al., 2009). Five consecutive repetitions were completed with the middle 3 repetitions used for kinematic and EMG analysis. The same investigator performed all test sessions, while data analysis was performed by a second investigator blinded to test session. On the re-test visit, the Penn Shoulder Score was completed to ensure no change in pain, satisfaction, and shoulder function between test days (Table 1). Procedures were performed by a biomechanist with 8 years of experience collecting shoulder kinematics and sEMG data. 2.3. Measurements Kinematics. The scapula, humerus, and thorax were instrumented with sensors and tracked using the Polhemus 3SPACE FASTRACK (Polhemus Inc, Colchester, VT) electromagnetic motiontracking system (Fig. 1). The sensors received an electromagnetic signal emitted from a transmitter secured on a support platform 115 cm above the floor. One sensor was affixed with adhesive tape on the third thoracic vertebrae to capture upper trunk movement. A second was affixed with adhesive tape on the flat surface of the posterior-lateral acromion for tracking scapular motion. The third sensor was fixed with a rubber strap to the posterior aspect of the distal humerus midway between the medial and lateral epicondyles. Scapular motion was expressed relative to the thorax by humeral elevation angles, with humeral motion expressed with respect to thorax. A digitizing wand connected to a 4th sensor was used to digitize bony landmarks to create local coordinate systems. The trunk was defined by digitizing the seventh cervical spinous process, seventh thoracic spinous process, suprasternal notch, and the most caudal point of the xyphoid process. The scapula was defined by the root of the spine of the scapula, the inferior angle of the scapula, and the posterior-lateral acromion angle. The humerus was defined by the medial and lateral epicondyles, and the center of the humeral head; the center was approximated by the coincident point of the vectors using the least squares method recorded during multiple humeral positions.

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Fig. 1. EMG Electrode (named by the muscle) and electromagnetic motion capture sensor (rounded boxes) placements.

Kinematics were collected at 30 Hz per sensors and recorded by The Motion Monitor software package (Innovative Sports, Chicago, Illinois). Sensor orientations were rotated mathematically for alignment with anatomically based and clinically meaningful axis systems. Rotations of the clavicle, scapula, and humerus were computed following guidelines by the International Society of Biomechanics (ISB) (Wu et al., 2005). The thorax coordinate system was defined relative to the global coordinate system by rotating around the global axes in the Z-X-Y order. Scapular rotations were calculated from the thorax rotations by pivoting the axes in the Y-XZ order. Internal/external rotation of the scapula was computed as a rotation around the thorax Y axis. Upward/downward rotation of the scapula was measured as a difference of rotation around the X axis of the thorax. Scapular anterior/posterior tilt was defined as a rotation around the Z axis of the thorax. Scapular position was described by the motion of the clavicle which was tracked by the scapular and thoracic sensors. Negligible translation at the acromioclavicular joint was assumed, and the scapula was limited to two degrees of freedom for translations. Clavicular elevation/ depression and protraction/retraction were derived from the digitized locations at the sternal notch and the acromioclavicular joint, which were tracked with the thoracic and scapular receivers respectively. Humeral elevation was defined in the Y-X-Y order, with the first rotation as the plane of elevation, the second rotation of X was the angle of humeral elevation, and the third defined the humeral internal/external rotation. The positive directions of the five kinematic variables were: scapular internal rotation, scapular upward rotation, scapular posterior tilt, clavicular elevation, and clavicular protraction. Kinematics were calculated during both ascending and descending total phase from 30 to 120 and at discrete arm elevation angles of 30 , 60 , 90 , 120 in the scapular plane. Surface Electromyography (sEMG). Muscle activity was recorded using dual silver bar pre-amplified sEMG electrodes (Bagnoli-8; Delsys Inc, Boston, MA) with a 10 mm inter-electrode distance, amplification factor of 10,000, and a common mode rejection ratio >92 dB at 60 Hz. Raw sEMG data were collected at 960 Hz using a 16-bit analog to digital converter and synced with kinematic data by the Motion Monitor software. First, the skin was shaved as

needed and vigorously cleaned with alcohol. Electrode placement: Electrodes were placed over the middle deltoid, upper trapezius(UT), infraspinatus, serratus anterior(SA), middle trapezius(MT), and lower trapezius(LT) in parallel with the muscle fibers (Fig. 1) and affixed with adhesive tape (Perotto, 1994; Ludewig et al., 1996; Ekstrom et al., 2004). The middle deltoid electrode was placed immediately distal to a point midway between the acromion process and the insertion of the deltoid muscle, along a line contacting the posterior acromion process and insertion of the deltoid. The infraspinatus electrode was placed 1 inch inferior to the spine of the scapula at a point midway between the root of the spine of the scapula and posterior acromion process. The UT electrode was placed lateral to a point midway between the spinous process of 1st thoracic vertebra and the acromion process, along a line connecting 1st thoracic vertebra and the acromion process. The MT electrode was placed immediately lateral to a point midway between the spinous process of the third thoracic vertebra and the root of the spine of the scapula, along a line connecting third thoracic vertebra and the root of the spine of the scapula. The LT electrode was placed immediately lateral to the midway point between the spinous process of seventh thoracic vertebra and the inferior angle of the scapula, along a line contacting the posterior acromion process and seventh thoracic vertebra. The SA electrode was placed along the mid-axillary line over rib six for the lower portion of the SA, with the participants arm at 90 of elevation in the scapular plane. Confirmation was made that the SA electrode was not placed over the latissimus dorsi with a muscle test for the latissimus dorsi. A reference electrode was affixed with adhesive tape on the contralateral olecranon process. Processing the sEMG was conducted by Motion Monitor and MatLab software (The MathWorks, Inc; Natick, MA). The EMG signal was sampled at 960 Hz and bandpass filtered from 20 Hz to 400 Hz in Motion Monitor. Further EMG signal processing was performed using custom written MatLab programming. A 0.5 Hz notch filter centered on 60 Hz was applied to remove ambient electrical noise. The EMG signal was visually inspected for cardiac artifact, and if the artifact was greater than 10% of the reference contraction, then the data was excluded. Custom-written MatLab code performed full wave rectification followed by a trapezoidal

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integration algorithm to calculate the average rectified EMG value during arm elevation (Kamen and Gabriel, 2010). The average rectified value parameter was chosen to capture the magnitude of the sEMG signal throughout the time period of the ascending and descending phases of scapular plane motion. The average rectified values were calculated for the both the total ascending phase and descending phase of 30 e120 elevation, and for 3 interval phases (30 e60 ; 60 e90 ; 90 e120 ). The left hand limit of integration was determined as the time when the arm passed the lower threshold (30 ) of the arm elevation interval and the right hand limit of integration was set as the time when the arm passed the upper threshold of the interval (120 ). The EMG values calculated were then normalized a REF-contraction (Burden, 2010). A REF-contraction was performed at 90 of scapular plane elevation, as it was the mid-point of the arc of the test motion (Cram and Kasman, 1998). During pilot testing, participants complained of fatigue and shoulder pain when 6 separate muscle tests were used for a reference contraction, therefore we used this single REF-contraction. Practice for the REF-contraction was provided prior to data collection by having participants perform 3 submaximal contractions and 1 maximal contraction. Next, 2 trials were performed and averaged for the REF-contraction. The REFcontraction procedure was a maximal isometric contraction effort for 5 s at 90 of scapular plane elevation, with the participant pushing upward against an immovable stabilized resistance applied at the participant's wrist. Verbal encouragement was given during the trials. The REF-contraction was collected before the dynamic arm elevation task. Data reduction of the REFcontraction EMG was calculated using 3 thousand points (3.125 s) during the mid-portion of each of the 2 REF-contraction trials. For the REF-contraction, the limits of integration were determined by first visually indicating the approximate start and end of the contraction, and then the MatLab code calculated the mid-point of the contraction. From the mid-point of the contraction, the left hand limit of integration was set 1500 ms prior to the mid-point and the right hand limit of integration was 1500 ms after the mid-point of the contraction (3s analysis window). EMG during the elevation task was normalized to the REF-contraction for each muscle (EMG-elevation task/EMG-REF-contraction). Pain during the REF-contractions was verbally rated on a numeric pain rating scale (0e10, 10 ¼ worst pain imaginable). Participants were asked to rate their pain on a numeric pain rating scale (0e10) during the REF-contraction on both test days of data collection, to assess if pain was different between test days as pain during the REF-contraction may impact the effort of the participant during the REF-contraction. 3. Data analysis Means and standard deviations for kinematic and sEMG variables were calculated for each test session. Pain ratings during the REF-contraction were averaged across trials for each day, and then the average pain was compared between test days using a t-test. Intraclass correlation coefficients [ICC(2-way random)] were used to determine the inter-session reliability of the sEMG and kinematic variables. ICC values are considered very good for values 0.81e1.00, good for 0.61e0.80, moderate for 0.41e0.60, fair for 0.21e0.40, and poor for values below 0.20 (Altman et al., 2001). Measurement error was calculated with the standard error of measure SEM ¼ standard deviation x [√(1eICC)], which estimates the error about a single measure of a variable. The minimal detectable change (MDC) represents the error when a measure is taken twice (change over time), and was calculated by multiplying the SEM by the √2 (Stratford, 2004; Weir, 2005). SPSS 19 statistical software (SPSS Inc., Chicago, Ill) was used for data analysis.

4. Results The Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were followed for reporting the results of this study (Kottner et al., 2011). All participants (n ¼ 12) had complete data from 2 test sessions. No participant had a change in shoulder function between sessions greater than the MDC of 12.1 points for the Penn (Leggin et al., 2006). Scapular Kinematics during scapular plane elevation. Participants elevated from 11.5 (5.2 ) to 135.5 (9.1 ) on day 1, and 12.1 (3.5 ) to 136.7 (9.5 ) on the re-test day. For the ascending and descending total phases 30 e120 for the 5 kinematic variables, the ICC(2-way, random) ranged from 0.62 to 0.95, the SEM ranged from 1.5 to 3.5 and the MDC from 2.1 to 5.0 (Table 2). For the discrete arm angles of 30 , 60 , 90 , and 120 , the ICC ranged from 0.23 to 0.95, the SEM from 1.4 to 4.2 and the MDC from 2.0 to 5.9 (Table 3). Normalized sEMG during scapular plane elevation. The REFcontraction sEMG muscle activity had good to very good reliability [ICC(2-way random) ¼ 0.75e0.95]; Table 4. Pain during the REF-contraction was not different (p ¼ 0.34) between test days, and the mean difference of 0.4/10 between sessions was less than the MDC of 2 points for pain (Mintken et al., 2009; Michener et al., 2011). For the sEMG during the ascending and descending total phase of 30 e120 , the ICC ranged from 0.53 to 0.97, the SEM from 2.5% to 25.0%REF-contraction, and the MDC was 3.6%e35.4%REFcontraction (Table 5). For the 3 interval phases for sEMG (Table 6), the ICC ranged from 0.08 to 0.99, the SEM from 2.3% to 73.7% and the MDC from 3.3%to 103.8%REF-contraction. 5. Discussion Shoulder kinematics and muscle activity sEMG measures can characterize changes in shoulder movement patterns that occur with manual therapy treatment for shoulder pain. This study provides inter-session reliability and measurement error values for

Table 2 Kinematic variables for the ascending and descending total phase of arm elevation in the scapular plane: mean (standard deviation) for the initial and re-test visits, error values of standard error of the measure (SEM) and the minimal detectable change (MDC) expressed in degrees; test-retest reliability coefficients [(ICC, 2-way random] and 95% confidence interval (CI). Motiona

Initial visit mean(SD)

Ascending phase (30 e120 ) Upward/Downward 54.8 (7.4) rotation Posterior/Anterior tilt 5.8 (7.2)

Retest visit ICC (95% CI) SEM MDC mean (SD)

52.5 (9.4) 0.83 (0.34e0.94) 6.4 (6.3) 0.95 (0.82e0.99) External/Internal rotation 5.6 (7.9) 4.5 (5.4) 0.86 (0.53e0.96) Clavicular 21.0 (3.8) 18.9 (4.9) 0.82 elevation/Depression (0.32e0.95) Clavicular 16.2 (3.3) 15.7 (3.5) 0.70 protraction/Retraction (0.08e0.91) Descending phase (30 e120 ) Upward/Downward 54.9 (5.7) 53.1 (5.4) 0.80 Rotation (0.20e0.93) Posterior/Anterior tilt 6.2 (8.6) 7.6 (7.1) 0.94 (0.80e0.98) External/Internal rotation 2.9 (9.5) 0.4 (6.1) 0.84 (0.44e0.96) Clavicular 20.1 (3.3) 18.5 (3.3) 0.62 elevation/Depression (0.20e0.88) Clavicular 16.8 (2.7) 18.2 (2.3) 0.65 protraction/Retraction (0.37e0.87)

3.5

5.0

1.5

2.1

2.5

3.5

1.9

2.6

1.9

2.7

2.5

3.5

1.9

2.7

3.2

4.5

2.1

2.9

1.5

2.1

a Positive values are upward rotation, posterior tilt, external rotation, clavicular elevation, clavicular protraction.

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30

Ascending phase Upward/Down ward rotation Posterior/anterior tilt External/Internal rotation Clavicular elevation/ Depression Clavicular protraction/ Retraction Descending phase Upward/Down ward rotation Posterior/Anterior tilt External/Internal rotation Clavicular elevation/ Depression Clavicular protraction/ Retraction

60

90

120

Initial mean (SD)

Re-test mean (SD)

ICC (95%CI)

SEM

MDC

Initial mean (SD)

Re-test mean (SD

ICC (95%CI)

SEM

MDC

Initial mean (SD)

Re-test mean (SD)

ICC (95%CI)

SEM

MDC

Initial mean (SD)

Re-test mean (SD)

ICC (95%CI)

SEM

MDC

6.1 (12.1) 13.0 (4.7) 24.0 (4.6) 9.4 (5.9) 19.5 (6.0)

5.7 (11.6) 11.5 (5.1) 24.3 (4.6) 10.9 (6.2) 20.7 (6.2)

0.91 (0.68, 0.97) 0.84 (0.57, 0.90) 0.23 (0.10, 0.65) 0.83 (0.54, 0.93) 0.80 (0.59, 0.88)

3.6

5.1

24.3 (14.7) 11.3 (5.0) 22.7 (5.0) 15.6 (6.1) 23.0 (6.1)

22.5 (11.6) 10.0 (6.0) 21.9 (4.7) 16.5 (6.2) 25.3 (7.3)

0.92 (0.68, 0.96) 0.85 (0.44, 0.91) 0.41 (0.05, 0.73) 0.85 (0.68, 0.98) 0.76 (0.57, 0.90)

3.7

5.3

43.5 (13.0) 9.8 (7.7) 23.7 (6.0) 22.5 (6.2) 27.5 (6.6)

41.7 (13.4) 8.1 (8.0) 22.7 (5.4) 23.0 (5.9) 29.9 (6.4)

0.91 (0.75, 0.94 (0.54, 0.66 (0.29, 0.91 (0.58, 0.73 (0.41,

4.0

5.6

59.6 (11.8) 7.9 (9.5) 26.7 (8.2) 29.0 (5.6) 33.2 (6.1)

57.9 (10.5) 4.7 (9.3) 24.1 (7.5) 29.1 (6.0) 35.5 (5.3)

0.90 (0.71, 0.95 (0.56, 0.88 (0.49, 0.94 (0.76, 0.74 (0.46,

3.5

5.0

2.1

3.0

2.7

3.8

1.4

2.0

2.9

4.1

6.5 (13.4) 14.1 (3.7) 23.1 (5.2) 9.1 (6.1) 20.0 (6.5)

5.8 (11.8) 12.0 (5.7) 22.3 (5.7) 10.5 (5.6) 22.1 (7.8)

0.91 (0.69, 0.79 (0.54, 0.41 (0.17, 0.71 (0.53, 0.80 (0.61,

22.1 (12.2) 11.9 (4.5) 23.95 (5.8) 14.7 (5.9) 24.6 (7.3)

22.2 (13.8) 9.5 (4.6) 21.8 (5.6) 16.3 (6.7) 26.9 (7.7)

0.91 (0.71, 0.81 (0.59, 0.63 (0.52, 0.82 (0.64, 0.82 (0.62,

43.2 (14.2) 7.9 (6.4) 22.9 (7.0) 22.8 (5.9) 28.8 (6.8)

41.1 (10.5) 5.3 (6.0) 20.2 (6.3) 23.1 (5.9) 31.5 (7.0)

0.91 (0.69, 0.90 (0.61, 0.74 (0.52, 0.90 (0.66, 0.75 (0.51,

61.2 (10.8) 5.8 (9.7) 27.8 (9.5) 30.1 (5.6) 33.8 (5.6)

57.2 (10.1) 2.8 (9.6) 24.8 (8.7) 29.1 (6.0) 22.1 (6.2)

0.88 (0.73, 0.93 (0.71, 0.89 (0.68, 0.94 (0.59, 0.69 (0.38,

3.6

5.1

2.6

3.7

3.1

4.3

1.4

2.0

3.3

4.6

2.0 4.0 2.5 2.7

3.8

2.8 5.6 3.5 3.8

5.4

0.99) 2.2

3.1

0.91) 4.2

5.9

0.76) 3.2

4.4

0.89) 3.2 0.97)

4.5

2.1 3.7 2.4 3.3

3.9

3.0 5.3 3.4 4.6

5.5

0.94) 2.0

2.9

0.93) 3.5

4.9

0.90) 2.7

3.8

0.93) 3.2 0.94)

4.5

0.95) 1.9

2.7

0.96) 3.3

4.7

0.84) 1.8

2.6

0.99) 3.4

4.8

0.89) 3.7

5.2

0.97) 2.0

2.8

0.99) 3.4

4.8

0.91) 1.9

2.7

0.96) 3.5 0.89)

4.9

0.94) 0.99) 0.90) 0.98) 0.85)

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Table 3 Kinematic variables at discrete humeral angles during ascending and descending arm elevation in the scapular plane: mean (SD), test-retest reliability coefficients ICC (2-way random); error values expressed in degrees. Positive values: upward rotation, posterior tilt, external rotation, clavicular elevation, clavicular protraction.

0.93) 0.99) 0.93) 0.96) 0.85)

5

6

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Table 4 Reference contraction: mean (standard deviation) at initial and re-test visits and SEM and MDC in milliVolts, test re-test reliability coefficients [(ICC, 2-way random]. Numeric Pain Rating (0e10, 10 ¼ worst pain) of pain reported during the reference contraction. Muscle

Initial visit mean (SD)

Retest visit mean (SD)

Visits comparison p-value

ICC (95% CI)

SEM

MDC

Middle deltoid Infraspinatus Upper trapezius Middle trapezius Lower trapezius Serratus anterior Numeric pain rating (0e10) with reference contraction

0.110 0.046 0.096 0.083 0.070 0.068 2.9

0.161 0.052 0.132 0.095 0.071 0.047 2.5

0.22 0.16 0.11 0.17 0.96 0.48 0.34

0.80 0.92 0.75 0.95 0.81 0.82

0.068 0.007 0.041 0.015 0.033 0.049

0.096 0.010 0.059 0.021 0.048 0.070

(0.088) (0.020) (0.062) (0.057) (0.061) (0.164) (1.1)

shoulder kinematics and sEMG muscle activity, which can be used to interpret changes in these data. Specifically, estimates were reported for kinematics at discrete arm angles, sEMG for 3 interval phases, and for both kinematics and sEMG for the total ascending and descending phases (30 e120 ) of arm elevation and lowering. The large majority of kinematic and muscle activity measures demonstrated good to very good inter-session reliability. Those variables with moderate or lower reliability (ICC  0.60) at 1 or more discrete arm angles or interval phases of motion were scapular internal/external rotation, and sEMG for the SA, UT, and LT. Correspondingly, these same variables had large measurement errors, which may limit the ability to detect changes in these variables with manual therapy treatment. The error needs to be considered when selecting the variable(s), in relation to the hypothesized differences expected with treatment. Generally, data from the total phase of motion had better reliability and lower error than the data from sEMG interval or kinematic discrete angles. Error values can aid the interpretation of data of a single measurement (SEM), and error estimates of a change in a measure between sessions or change over time (MDC), and used to determine effect sizes in planning future studies using the same methods. The 5 kinematics variables in this study can be measured consistently using 3-dimensional electromagnetic tracking in individuals with shoulder pain. However, the level of inter-session reliability is dependent on the method of data reduction and the specific kinematic variable. The only variable with less than very good reliability was scapular internal/external rotation at the discrete angles of 30 and 60 (ICC ¼ 0.23e0.41), thus warranting caution when interpreting data collected at these lower discrete arm angles. Our reliability estimates are very similar to those

Table 5 Normalized sEMG during ascending and descending total phases of scapular plane elevation: mean and standard deviation, standard error of the measure (SEM), and minimal detectable change (MDC) values expressed as %REF-contraction; Test-retest reliability coefficients: ICC (2-way random) with 95% CI. Muscle

Initial visit mean (SD)

Ascending phase (30 e120 ) Middle deltoid 49.9 (21.2) Infraspinatus 61.2 (23.6) Upper trapezius 100.2 (38.8) Middle trapezius 49.6 (31.9) Lower trapezius 57.0 (27.6) Serratus anterior 88.2 (23.2) Descending phase (120 e30 ) Middle deltoid 40.8 (18.5) Infraspinatus 37.9 (13.4) Upper trapezius 48.2 (21.7) Middle trapezius 17.0 (6.6) Lower trapezius 25.8 (10.9) serratus anterior 45.9 (26.3)

Retest visit mean (SD)

ICC (95% CI)

SEM

MDC

49.6 68.6 103.8 47.2 62.0 108.5

(21.6) (26.5) (23.8) (19.8) (29.5) (56.0)

0.97 0.95 0.53 0.82 0.76 0.60

(0.90e0.99) (0.70e0.99) (0.09e0.88) (0.35e0.95) (0.09e0.94) (0.42e0.90)

3.6 5.7 21.4 10.9 14.1 25.0

5.2 8.2 30.3 15.5 19.9 35.4

42.7 38.6 46.0 19.5 26.8 42.4

(18.8) (13.4) (10.8) (8.0) (10.4) (20.6)

0.92 0.95 0.81 0.88 0.84 0.89

(0.71e0.98) (0.82e0.99) (0.34e0.95) (0.49e0.97) (0.31e0.96) (0.58e0.97)

5.4 3.1 7.0 2.5 4.2 7.9

7.6 4.4 10.3 3.6 6.0 11.2

(0.216) (0.027) (0.102) (0.077) (0.094) (0.068) (0.8)

(0.67e0.90) (0.78e0.97) (0.53e0.96) (0.73e0.99) (0.76e0.90) (0.74e0.92)

reported by Haik et al. (2014a), who assessed inter-session reliability for 3 scapular kinematics variables during sagittal plan elevation in individuals with shoulder pain. Estimates of measurement error allows for direct interpretation of data. For the kinematic variables, the amount of change needed to be considered greater than error (MDC) ranged from 2 to 3 at discrete arm elevation angles and the total phase of elevation for all variables except upward/downward and internal/external rotation which had MDCs of 4 e6 . Putting these error values in context, prior literature, (Timmons et al., 2012) has reported differences between those with and without shoulder pain of 2 e5 of upward rotation across the entire phase and at discrete arm angles. Given the error values we reported for upward rotation, only those differences for total phase of motion (30 e120 ) during the descending phase are likely meaningful differences because they are greater than measurement error. Haik et al. (2014a) reported the lowest error values consistently at the lower arm angles, and the highest errors at the highest arm angles (120 ). In the current study, there was no pattern of error values for higher versus lower arm angles, phase of elevation, or discrete versus total phase of elevation. Other prior reliability studies of dynamic scapular kinematics described in a recent systematic review (Lempereur et al., 2014) or a more recent study performed in healthy individuals, (Roren et al., 2013) and thus are not directly comparable to our study. For the sEMG variables, reliability estimates were good or higher for all interval and total phases of motion for the MT, deltoid, and infraspinatus, The SA, UT, and LT had moderate or lower reliability estimates during the ascending total phase (30 e120 ) for the SA and UT, and during the 30 e60 interval phase for the SA, UT, and LT. In a prior study of healthy individuals (Seitz and Uhl, 2012) reported the reliability estimates were good for the SA, UT, and MT, and moderate for the LT and deltoid during arm elevation and descent. This study provides reliability and error estimates for those with shoulder pain. Generally, the sEMG error values were lower in the total phase of elevation than for the interval phases. The deltoid, infraspinatus, and MT had the lowest error values for both the total phase of elevation and the 3 interval phases. For the sEMG interval phases, the MDC was >25%REF-contraction for the SA, UT, and LT error during all 3 ascent phases and for the SA during the descending interval of 120 e90 . Interestingly, the errors were generally higher during the ascending than the descending interval and total phases. The relatively higher error during ascent may be due to the variability in the motor control patterns during elevation of the arm in patients with subacromial pain syndrome (Chester et al., 2010). The confidence bounds for the ICCs reliability estimates were wide for the majority of the variables. This may be due to the small sample size used. We performed a priori power analysis, based on the pearson's correlation value of 0.80. This may not have adequately assessed the sample size, given that we used subsequently used ICC's to assess test-retest reliability.

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0.99) 3.7 5.3 0.99) 2.7 3.8 0.78) 9.8 13.9 0.97) 6.7 9.4 0.84) 11.1 15.6 0.92) 20.0 28.2 (0.85, (0.86, (0.40, (0.55, (0.33, (0.55, 0.98 0.95 0.61 0.79 0.63 0.74 (26.0) (12.3) (12.7) (14.1) (16.3) (36.1)

0.99) 6.9 9.7 0.97) 7.1 10.0 0.79) 22.7 32.0 0.96) 9.3 13.1 0.87) 36.6 51.6 0.92) 15.6 22.1 (0.81, (0.81, (0.23, (0.41, (0.34, (0.71, 0.99 0.92 0.67 0.89 0.51 0.81 (67.4) (23.9) (34.8) (24.3) (47.2) (35.1)

0.99) 2.4 3.4 0.98) 3.9 5.5 0.91) 5.9 8.3 0.77) 10.0 14.1 0.98) 8.5 12.0 0.99) 8.3 11.8 (0.76, (0.76, (0.61, (0.38, (0.69, (0.74, 0.98 0.93 0.85 0.61 0.82 0.83

9.1 13.5 27.4 18.5 17.0 29.0 6.5 9.5 19.4 13.1 12.0 20.5 0.99) 0.97) 0.92) 0.89) 0.94) 0.94) (0.68, (0.71, (0.59, (0.31, (0.52, (0.58, 0.96 0.90 0.71 0.78 0.86 0.78

(0.80, 0.99) 2.3 (0.78, 0.97) 5.3 (0.63, 0.95) 5.5 (0.59, 0.94) 6.9 (0.13, 0.64) 16.8 (0.61, 0.98) 10.7 0.95 0.90 0.86 0.82 0.18 0.77

3.2 7.5 7.8 9.8 23.7 15.1

(0.80, 0.98) 5.3 7.5 (0.75, 0.96) 8.8 12.4 (0.27, 0.54) 24.9 35.0 (0.68, 0.97) 7.4 10.5 (0.01, 0.62) 28.5 40.1 (0.10, 0.51) 73.7 103.8 0.92 0.91 0.08 0.82 0.35 0.35

SEM MDC SEM MDC Initial mean (SD) Retest mean (SD) ICC (95%CI)

90 e120 Interval 98.7 (69.2) 96.0 61.6 (25.9) 63.7 116.6 (44.1) 101.3 53.15 (31.7) 47.8 52.2 (57.4) 77.7 104.9 (36.7) 92.4 120 e90 Interval 49.3 (26.3) 48.1 37.2 (11.5) 37.1 62.1 (18.8) 53.3 21.9 (15.2) 19.7 25.1 (20.3) 34.9 66.1 (42.4) 46.7 60 e90 Interval 62.6 (31.2) 67.5 (33.5) 66.9 (26.9) 78.5 (33.3) 105.2 (30.5) 105.6 (41.6) 47.5 (28.6) 48.1 (27.1) 62.7 (30.6) 73.8 (33.4) 104.1 (38.1) 121.7 (49.2) 90 e60 Interval 32.0 (15.9) 34.8 (18.7) 0.40.2 (14.2) 42.3 (15.5) 49.2 (17.1) 50.6 (13.3) 18.7 (19.1) 22.2 (13.0) 32.6 (19.7) 30.9 (20.2) 45.3 (24.0) 43.4 (16.2)

SEM MDC Initial mean (SD) Retest mean (SD) ICC (95%CI) Initial mean (SD) Retest mean (SD) ICC (95%CI)

30 e60 Interval 38.2 (17.1) 38.9 (20.3) 48.9 (30.7) 58.6 (27.8) 87.6 (26.7) 93.2 (25.2) 36.1 (18.5) 40.3 (16.2) 65.5 (50.1) 47.5 (20.5) 77.9 (90.7) 109.5 (91.9) 60 e30 Interval 20.3 (10.0) 23.0 (10.2) 35.5 (17.4) 38.7 (16.3) 32.5 (16.8) 37.6 (12.7) 24.1 (16.5) 25.1 (16.4) 20.5 (18.2) 21.0 (19.0) 28.1 (24.8) 35.9 (19.8) Ascending phase Deltoid Infraspinatus Upper trapezius Middle trapezius Lower trapezius Serratus anterior Descending phase Deltoid Infraspinatus Upper trapezius Middle trapezius Lower trapezius Serratus anterior

Table 6 Normalized sEMG for 3 interval phases of ascending and descending of scapular plane elevation: mean and standard deviation, standard error of the measure (SEM), and minimal detectable change (MDC) values expressed as % REF-contraction; test-retest reliability coefficients: ICC (2-way random).

L.A. Michener et al. / Manual Therapy xxx (2015) 1e8

7

Our sEMG results are not directly comparable in magnitude to others that used different normalization procedures. In this study, a reference contraction was used, which may not have produced the maximum muscle activity for each muscle tested. The REFcontraction demonstrated good to very good reliability. Pain may be a contributor to the variance in EMG values between days. However, there was no difference in pain ratings (mean difference ¼ 2/30 points Penn Pain subscale), or between numeric pain ratings during the reference contraction (mean difference ¼ 0.4/10 points) between test days. The electrical signals of the kinematics can create noise in the sEMG data (Clancy et al., 2002). Visual inspection of the sEMG data was performed, and notch filters were used to remove artificial noise. Even with these steps, it is possible that noise was present. Every attempt was made to ensure reduced impedance and confirmation of sEMG electrode placement over the intended muscle, but we cannot confirm that cross-talk was eliminated from other muscles. We used a single reference contraction for normalization, which may not have elicited the maximum contraction for each muscle. An individual muscle test for each muscle under study can be used for normalization, however there is not a single “best” muscle test for each shoulder muscle (Ekstrom et al., 2005). It is important to note that the measurement properties of the sEMG variables are generalizable to those studies that use the same reference contraction for normalization used in this study. The validity of SA surface electromyography has been challenged, with a report of consistently lower magnitude in SA activity from surface electrodes as compared to indwelling electrodes (Hackett et al., 2014). We placed the SA electrode with the arm at the mid-range of arm elevation, however we cannot be assured the SA muscle remained under the surface electrode at lower or higher arm elevation angles. Other speeds of motion or planes of motion, different loads used during elevation, and other discrete points of humeral elevation could result in different estimates. In between test days it is unknown if factors may have differed that affected measurements, such as motivation, clothing, daily use of their shoulder. Finally, error estimates were calculated at the baseline CI level of 68%, and to allow for readers to calculate other CI such as 90% or 95%. This study has expanded the understanding of the measures of shoulder kinematics and muscle activity by providing intra-rater test-retest reliability and error metrics. Very good to good reliability can be achieved for the large majority of measures, and with error metrics that can be used to assess the relative meaning of experimental results using these measurement techniques. Further refinement of the measures may be needed for future studies using these methods, depending on the angle of elevation and type of reduction (total phase versus discrete angles or intervals of motion) used in the study.

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Please cite this article in press as: Michener LA, et al., Biomechanical measures in participants with shoulder pain: Intra-rater reliability, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.10.011