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Reliability and minimal detectable change in scapulothoracic neuromuscular activity
Journal of Electromyography and Kinesiology 22 (2012) 968–974
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Reliability and minimal detectable change in scapulothoracic neuromuscular activity Amee L. Seitz a,⇑, Timothy L. Uhl b a b
Department of Physical Therapy, Bouvé College of Health Sciences, Northeastern University, Boston, MA, USA Department of Rehabilitation Sciences, College of Health Sciences, University of Kentucky, Lexington, KY, USA
a r t i c l e
i n f o
Article history: Received 27 December 2011 Received in revised form 13 May 2012 Accepted 13 May 2012
Keywords: Shoulder EMG Lower trapezius Serratus anterior Impingement Scapula
a b s t r a c t Alterations in scapular muscle activity, including excess activation of the upper trapezius (UT) and onset latencies of the lower trapezius (LT) and serratus anterior (SA) muscles, are associated with abnormal scapular motion and shoulder impingement. Limited information exists on the reliability of neuromuscular activity to demonstrate the efficacy of interventions. The purpose of this study was to characterize the reproducibility of scapular muscle activity (mean activity, relative onset timing) over time and establish the minimal detectable change (MDC). Surface electromyography (sEMG) of the UT, LT, SA and anterior deltoid (AD) muscles in 16 adults were captured during an overhead lifting task in two sessions, oneweek apart. sEMG data were also normalized to maximum isometric contraction and the relative onset and mean muscle activity during concentric and eccentric phases of the scapular muscles were calculated. Additionally, reliability of the absolute sEMG data during the lifting task and MVIC was evaluated. Both intrasession and intersession reliability of normalized and absolute mean scapular muscle activity, assessed with intraclass correlation coefficients (ICC), ranged from 0.62 to 0.99; MDC values were between 1.3% and 11.7% MVIC and 24 to 135 mV absolute sEMG. Reliability of sEMG during MVIC was ICC = 0.82–0.99, with the exception of intersession upper trapezius reliability (ICC = 0.36). Within session reliability of muscle onset times was ICC = 0.88–0.97, but between session reliability was lower with ICC = 0.43–0.73; MDC were between 39 and 237 ms. Small changes in scapular neuromuscular mean activity (>11.7% MVIC) can be interpreted as meaningful change, while change in muscle onset timing in light of specific processing parameters used in this study is more variable. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Abnormal scapular motion has been implicated in the pathogenesis of shoulder pain and impingement (Kibler, 1998; Kibler and Mcmullen, 2003; Kibler and Sciascia, 2010) and has been characterized by changes in scapular muscle electromyographic (EMG) activity (Ludewig and Cook, 2000). Of particular interest are the relative contributions of the serratus anterior and trapezius muscles that stabilize the scapula and induce scapular motion necessary for humeral elevation (Bagg and Forrest, 1988; Johnson and Pandyan, 2005; Kronberg et al., 1990). Abnormal scapular neuromuscular control, demonstrated by excess EMG mean activity of the upper trapezius, decreased mean activity of the serratus anterior (Ludewig and Cook, 2000), and altered EMG onset timing in the lower trapezius and serratus anterior muscles, has been found in individuals with shoulder pain associated with impingement ⇑ Corresponding author. Address: Department of Physical Therapy, Northeastern University, 360 Huntington Ave., Robinson 6, Boston, MA 02115, USA. Tel.: +1 617 373 7626; fax: +1 617 373 7630. E-mail address: [email protected] (A.L. Seitz). 1050-6411/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jelekin.2012.05.003
(Cools et al., 2007, 2003, 2005; Roy et al., 2009b; Wadsworth and Bullock-Saxton, 1997). Given these findings, therapeutic interventions that address an imbalance in scapular muscle neuromuscular activity and control rather than purely muscle strength have been advocated in evidence-based shoulder rehabilitation and injury prevention programs (Kuhn, 2009; Ludewig and Borstad, 2003; Reinold et al., 2009; Roy et al., 2009a; Tate et al., 2010). A recent systematic review suggests that muscle onset timing as measured with EMG can be changed with therapeutic exercise (Crow et al., 2011). However, there is a lack of evidence that the scapular muscle balance and control as measured with EMG can be altered with exercise, despite the widespread use of therapeutic exercise to address such impairments in injury prevention and rehabilitation programs. To determine whether programs are effective at normalizing scapular muscle balance, reliable measures of neuromuscular function such as mean muscle activity and onset timing are needed. To date, limited information exists on the reliability of scapular muscle EMG. Cools et al. (2002) established good reliability of between day scapular muscle EMG onset relative to the deltoid during a sudden arm perturbation with intraclass correlation
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coefficients (ICC) = 0.73–0.78. However, the reliability of onset timing during a purposeful movement was not studied. Minning et al. reported good within day (0.75–0.83) but poor between day reliability (ICC = 0.03–0.29) of mean scapular muscle activity during an isometric fatiguing contraction (Minning et al., 2007). Ludewig and Cook reported within-day between trial reliability of mean normalized scapular EMG amplitude data to be between ICC = 0.73 and 0.89 with an overhead lifting task with and without hand weights (Ludewig and Cook, 2000). Ebaugh and Spinelli compared eccentric and concentric surface EMG of absolute scapular muscle activity during an overhead reaching task without weight and found very good between within session relative reliability (ICC = 0.87–0.94) for root mean square amplitude data (Ebaugh and Spinelli, 2010). Authors also reported absolute reliability with the standard error of the measure, in millivolts because the EMG data were not normalized. Furthermore, this study consisted of a single testing session as such the intersession reliability was not studied. Crow et al. (2011) reported the absolute intersession reliability of select scapular muscles, specifically the serratus anterior and upper trapezius, with co-efficients of variation for between day normalized mean amplitude EMG data from 4.2% to 10.3% a maximum voluntary contraction during concentric and eccentric phases of a repetitive lifting task. However, relative reliability with intraclass correlation coefficients, the mean activity of the lower trapezius muscle, and muscle onset timing were not factors examined in this study. The absolute and relative intersession reliability of scapular muscle EMG amplitude and onset timing during purposeful movements such as an overhead lifting task is necessary to determine whether change in measures of scapular neuromuscular control with therapeutic intervention over time is beyond measurement error. Therefore, the purpose of this study is to characterize the reproducibility of scapular muscle activity (mean activity, relative onset timing) during a resisted bilateral overhead lifting task, determine the stability of these measures over time, and establish the absolute error with the standard error of the measure (SEM) and minimal detectable change (MDC). 2. Methods 2.1. Subjects Sixteen volunteers (8 males; 8 females; mean age = 28.0 ± 6.9 years; BMI = 23.3 ± 2.8) free from shoulder pain were recruited by a sample of convenience from the community and met eligibility criteria. All subjects were between the ages of 18 and 65 years, free of shoulder and neck pain within the last 6 months, and had no known shoulder or neck pathology, neurological disorders, adhesive allergies, or history of shoulder fracture or surgery. Eligible subjects were screened for normal shoulder range of motion and pain free shoulder strength. All eligible volunteers gave written and informed consent prior to participation. The study was approved by the University of Kentucky Institutional Review Board. All subjects completed two testing sessions that were between 4 and 10 days apart (mean 6.4 days, SD 1.8). No subject reported participating in an unusually strenuous activity 48 h prior to the first testing session and reported adherence to the request to avoid unusually strenuous activity between testing sessions. 2.2. Electromyography During each session, a 16-channel EMG system (Run Technologies, Mission Viejo, CA) was used to record muscle activity at a bandwidth of 10–2000 Hz. All raw EMG data was transmitted at 2000 Hz via a fiber optic cable through a Myopac transmitter unit
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(Run Technologies, Mission Viejo, CA) to its receiver unit with impedance of 1 MX and common mode rejection ratio of 90 dB min at 60 Hz. The sEMG were differentially amplified at 2000 times. All signals EMG were transferred to an analog to digital converter (12 bit resolution) before being imported into a desktop computer for processing and analysis. Surface EMG (sEMG) electrodes were placed over the upper and lower portion of the trapezius, serratus anterior, and anterior deltoid muscles in specific anatomical locations using previously established standardized methods (Ekstrom et al., 2004; Mclean et al., 2003; Nieminen et al., 1993; Zipp, 1982) described in Table 1. These specific scapular muscles were chosen given their function to control normal scapular motion during arm elevation (Bagg and Forrest, 1988; Johnson and Pandyan, 2005; Kronberg et al., 1990). The deltoid was examined as a prime mover for humeral elevation. To apply the surface electrodes, the skin was shaved, lightly abrading with fine sandpaper, and cleaned with alcohol to minimize skin impedance (De Luca, 1997). Bipolar Ag/AgCl circular pre-gelled surface electrodes (Blue Sensor; Ambu Inc., Glen Burnie, MD) were placed parallel to each muscle with a 2-cm center to center interelectrode distance. A reference electrode was placed over the contralateral acromion. The surface electrodes were connected to a belt amplifier which was secured posteriorly to the subject’s waist. Correct electrode placement was confirmed by visual inspection of the raw sEMG signals on an oscilloscope. Measurement (cm) of distances from the specific anatomical landmarks for exact electrode placement were recorded and referenced in the second testing session. The same examiner performed data collection on all subjects and was blinded to the first session EMG data during the second session testing. 2.3. Electrogoniometer An electrogoniometer, used to define the concentric and eccentric phases of the lifting task, was placed on the shoulder fixed to the spine of the scapula and middle deltoid. The electrogoniometer and sEMG signals were collected synchronous during data collection through the Myopac acquisition hardware and displayed synchronously in Datapac signal processing software (Version 5.0, Run Technologies, Mission Viejo, CA). The electrogoniometer signal was differentially amplified 1000 times and transferred to an analog to digital converter (12 bit resolution) before being imported into a desktop computer for recording and analysis. 2.4. Lifting task During each session, simultaneous sEMG and electrogoniometer data were collected continuously while the subjects performed 10 repetitions of bilateral humeral elevation holding either 1.4 kg (3 lb) or 2.3 kg (5 lb) weights. The heavier (2.3 kg) weights were used by individuals over 68.1 kg of body weight. Subjects started with the arms resting at his or her side. Then subjects were asked to raise both arms with thumbs facing upwards (medially to maximum elevation) with elbows extended (Mcclure et al., 2009). The plane of humeral elevation was standardized to 40° anterior to the coronal plane with two free standing poles to serve as a visual guide. A metronome set at 60 beats per minute was used to standardize the rate of humeral elevation and lowering (Melton et al., 2011). Subjects practiced the rate of movement from rest to maximal elevation in 2 s and lowering to start position in 2 s (Fig. 1a–c.). Subjects were instructed to relax for 2 s between trials. 2.5. Maximum voluntary isometric contractions Maximum voluntary isometric contractions (MVIC) were used to verify sEMG signal integrity with each muscle and normalize
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Table 1 Surface electrode placement and positions used to establish the maximum voluntary isometric contraction. Electrode placement and maximum voluntary isometric contraction test positions of each muscle Muscle
Electrode placement
Position
Anterior deltoid
A measure 1/5th length of the clavicle from the anterior lateral aspect was made and marked. The electrodes were placed with 1/ 5th distance between this point and the lateral epicondyle (elbow bent, neutral shoulder rotation) Zipp (1982) A mark was made on the skin at the midpoint on a line joining the C7 spinous process and tip of the acromion. The electrodes were placed over a point 1/2 the distance between this point and the posterior lateral angle of the acromion Mclean et al. (2003) With the arm elevated in the scapular plane to 125°, the electrodes were placed at the midpoint from the T7 spinous process to the inferior angle of the scapula Nieminen et al. (1993) With the arm elevated in the scapular plane to 125°, the electrodes were placed over the 7th intercostal space, just anterior to the fibers of the latissimus dorsi Ekstrom et al. (2004)
While seated, resistance was applied to the distal arm as the subject performed humeral elevation at 125° of flexion
Upper trapezius
Lower trapezius
Serratus Anterior
the sEMG data during the lifting task. The standardized MVIC test positions are summarized in Table 1. For each muscle, two MVIC 5s maximal contractions were captured with a 1-min rest between contractions. In each session, a resting sEMG level of each muscle was also recorded with the subject standing. 2.6. Data reduction All raw sEMG data were processed with Datapac Version 5.0 software (Run Technologies, Mission Viejo, CA). Raw sEMG signals were digitally filtered to correct for any DC offset with a passive demeaning filter, followed by a high pass 4th order finite impulse response filter with a 10 Hz cut-off frequency, then full wave rectified. A low pass 4th order Butterworth filter with 6 Hz cut off frequency was used to smooth the data. The MVIC was determined by averaging the highest 500 ms window of mean sEMG activity during two separate 5 s trials for each muscle. Mean normalized and absolute sEMG amplitude was also calculated for both the concentric and eccentric phases of the lifting task by first subtracting the background resting sEMG data from the mean activity during each phase. The phases of elevation were defined by positive and negative signals of the first derivative of the electro-goniometer signal. Mean sEMG amplitude was expressed as absolute values (in millivolts) and normalized as the percentage of MVIC (Burden, 2010). Five middle trials (repetitions 4–8) of the elevation task in each muscle in each session were used for statistical analysis. A threshold of >10% MVIC beyond resting activity was used to determine muscle onset timing during the concentric phase elevation. The 10% threshold was used in previous research to enhance consistency and minimize interference with resting muscle activity (Cools et al., 2002) and has been consistently used to identify scapular muscle timing disorders in individuals with impingement (Cools et al., 2002, 2003; De Mey et al., 2009). Early activation of the stabilizing muscles at the proximal scapulothoracic joint in relation to prime-mover activation (deltoid) at the glenohumeral joint is necessary for proper scapulothoracic stability (Magarey and Jones, 2003). Additionally, temporal sequence of the scapular muscles to actual arm movements are important factors in coordinating scapular motion with humeral elevation (Kibler, 1998). Thus, scapular muscle onset timing in this study was expressed in milliseconds both relative to the onset of the humeral prime mover the deltoid and humeral elevation defined using goniometer. Negative timing values reflect earlier onset of the upper trapezius, lower trapezius, or serratus anterior muscle in relation to the anterior deltoid or goniometer. Positive onset timing values reflect onset of muscle activity after either the anterior deltoid activity or humeral movement. The mean scapular muscle onset timing of the
While seated, resistance was applied to the distal humerus as the subject performed shoulder abduction at 90° of abduction
While in a prone position with the arm abducted to 120°, resistance is applied to the radial aspect of the distal forearm as the subject performed horizontal abduction While seated, resistance was applied to the distal arm as the subject performed humeral elevation at 125° of flexion
five middle trials (repetitions 4–8) for each muscle were used for statistical analysis. 3. Statistical analysis The relative reliability of absolute (in millivolts) and normalized (%MVIC) mean sEMG activity during each phase (concentric, eccentric) and scapular muscle onset relative to anterior deltoid and humeral elevation was determined by calculating the Intraclass Correlation Coefficient (ICC) for criterion measures both within and across sessions (Shrout and Fleiss, 1979). The within session reliability were calculated comparing five trials (repetitions 4 through 8) and the between session reliability were calculated by comparing the mean of the five trials between sessions. To improve the generalizability of the normalized sEMG results, we calculated the reliability of the MVIC sEMG amplitude in each muscle. The within session MVIC sEMG reliability were calculated comparing two trials of the MVIC, and the between session reliability were calculated by comparing the mean of two trials between sessions. For all analyses, the ICC values were considered: poor when below 0.20; fair from 0.21 to 0.40; moderate from 0.41 to 0.60; good from 0.61 to 0.80; and very good from 0.81 to 1.00 (Altman et al., 2001). The absolute reliability was defined as the SEM and the MDC. The SEM was defined as the standard deviation multiplied by the square root of the ICC subtracted from 1 (Stratford et al., 1996a). The MDC was calculated by multiplying the SEM by the square root of 2 (Stratford et al., 1996b). All statistical analyses were conducted with the IBM SPSS Statistics software (Version 19; IBM Corp, Armonk, NY). 4. Results Results of the within and between session reliability of sEMG with the ICC, SEM, and MDC are shown in Tables 2–5. 4.1. Intra-session and inter-session absolute mean sEMG Intra-session relative reliability of absolute mean scapular and anterior deltoid muscle activity during both phases of elevation was very good (ICC = 0.95–0.99). Intra-session MDC values were between 42 and 219 mV in all muscles during both phases of elevation. Inter-session reliability of absolute mean sEMG activity during both phases of the lifting task in the serratus anterior were very good (ICC = 0.89–0.90), good for the upper trapezius (ICC = 0.70) and lower trapezius (0.62–0.74), and good to very good for the anterior deltoid (ICC = 0.78–0.85). In all muscles, the intersession MDC of absolute mean muscle activity was between 90 and
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Fig. 1. (a) Start, (b) middle, and (c) end position of the overhead lifting task.
Table 2 Intra and inter-session reliability results for absolute mean scapular muscle sEMG activity (in millivolts) during the overhead lifting task. Variable
Scapular muscle
Intra-session
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
Concentric mean absolute activity (mV)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.99 0.96 0.97 0.98
202 216 219 77
13 23 33 6
18 32 46 8
0.85 0.90 0.70 0.62
202 320 216 90
36 95 70 33
51 135 99 47
Eccentric mean absolute activity (mV)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.99 0.95 0.97 0.97
68 46 100 42
5 8 16 4
7 11 23 6
0.78 0.89 0.70 0.74
69 55 97 49
14 16 27 17
19 23 39 24
mV, millivolts; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
320 mV during the concentric phase of elevation and between 49 and 97 mV during the eccentric phase. 4.2. Intra and inter-session MVIC sEMG Absolute sEMG maximum values (in mV) during the MVICs and reliability results are provided in Table 3. Intra-session reliability of absolute mean values during the two MVIC trials were very good (ICC = 0.97–0.99) for both the deltoid and scapular muscles with MDC values between 46 and 82 mV. The inter-session reliability of the mean MVIC sEMG values were very good for the anterior deltoid, serratus anterior, and lower trapezius muscles (ICC = 0.82– 0.89) with MDC absolute values between 121 and 204 mV, but fair for the upper trapezius muscle (ICC = 0.36). The inter-session MDC for mean MVIC EMG values of the upper trapezius was 316 mV. 4.3. Intra-session and inter-session normalized EMG Results of the within and between session normalized EMG reliability of the elevation task is shown in Table 4. Intra-session relative reliability of normalized scapular and anterior deltoid muscle activity during both phases of elevation was very good (ICC = 0.96–0.99). Intra-session MDC values were less than 3% MVIC for the normalized data during both phases of elevation. Inter-session reliability of normalized mean EMG activity during both phases of the lifting task in the lower trapezius and serratus anterior were very good (ICC = 0.82–0.86), good for the upper trapezius (ICC = 0.66–0.79), and moderate for the anterior deltoid (ICC = 0.59). The intersession MDC for lower trapezius normalized
mean muscle activity during both phases of elevation was between 3.2% and 3.9% MVIC. The intersession MDC for normalized mean muscle activity of the serratus anterior and upper trapezius during the concentric phase was 10.3% and 11.4%, respectively. Corresponding with smaller mean normalized sEMG activity, the MDC values were lower in all muscles during the eccentric phases ranging from 3% to 8% MVIC. The intersession MDC for mean muscle activity of the deltoid during the concentric phase was 11.7% and 5.8% during the eccentric phase. 4.4. Intra-session and inter-session relative muscle onset timing Results of the within and between session relative muscle onset timing reliability of the elevation task is shown in Table 5. Reliability of scapular muscle onset times relative to the prime mover of the deltoid was very good (ICC = 0.88–0.97) within session, but poor to moderate (ICC = 0.43–0.73) between sessions. Similarly the relative onset of the scapular muscles to the goniometer was very good (ICC = 0.93–0.96) within session, but poor to moderate (ICC = 0.08–0.49) between sessions. Reliability was higher and MDC values were smaller for the scapular muscle onset timing relative to the deltoid (MDC between 39 and 237 ms) compared to the goniometer (MDC between 62 and 250 ms). 5. Discussion To determine the efficacy of injury prevention and rehabilitation programs prescribed to normalize scapular muscle function, measures of neuromuscular activity must be reliable. The results of this
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Table 3 Intra and inter-session reliability results for absolute mean scapular muscle sEMG activity (in millivolts) with two trials of maximum isometric voluntary contraction in each session. Variable
Scapular muscle
Reliability MVIC maximum amplitude (mV)
Intra-session
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
0.98 0.99 0.97 0.98
392 364 468 445
33 33 58 46
47 46 82 65
0.89 0.83 0.36 0.82
433 398 490 502
85 144 223 144
121 204 316 204
MVIC, percent of maximal voluntary isometric contraction; mV, millivolts; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
Table 4 Intra and inter-session reliability results for normalized mean scapular muscle sEMG activity during the overhead lifting task. Variable
Scapular muscle
Intra-session
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
Concentric mean activity (%MVIC)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.98 0.99 0.98 0.97
53.4 44.4 45.6 19.7
2.0 1.5 1.7 1.2
2.9 2.1 2.5 1.7
0.59 0.86 0.66 0.85
51.6 44.8 45.0 19.2
8.3 7.3 8.0 2.7
11.7 10.3 11.4 3.9
Eccentric mean activity (%MVIC)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.97 0.99 0.96 0.97
18.4 18.4 20.3 11.1
1.0 1.7 1.3 1.0
1.5 2.4 1.9 1.3
0.59 0.85 0.79 0.82
18.3 18.1 20.9 11.1
4.1 5.4 3.5 2.3
5.8 7.6 4.9 3.2
%MVIC, percent of maximal voluntary isometric contraction; msec, millisecond; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
Table 5 Intra and inter-session reliability results for onset timing relative to the anterior deltoid and goniometer during the overhead lifting task. Variable
Scapular muscle
Intra-session
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
Relative onset to anterior deltoid (msec)
Serratus anterior Upper trapezius Lower trapezius
0.93 0.97 0.88
67.0 8.9 147.4
38.7 28.0 57.3
54.8 39.6 81.0
0.67 0.73 0.43
85.0 12.0 201.8
89.8 84.5 167.9
127.0 119.6 237.5
Relative onset to goniometer (msec)
Serratus anterior Upper trapezius Lower trapezius
0.95 0.96 0.93
13.9 89.8 66.4
52.1 43.9 65.6
73.7 62.1 92.8
0.49 0.35 0.08
31.1 41.9 147.9
120.5 133.4 176.9
170.4 188.6 250.1
msec, millisecond; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
study suggest normalized and absolute mean activity of the serratus anterior, lower trapezius, upper trapezius and deltoid as measured with sEMG during a functional bilateral overhead lifting task is reproducible. Reproducible normalized sEMG data is also dependent upon reliable MVIC data (Table 2). The relatively small SEM and the MDC values for within-session mean normalized and absolute scapular muscle activity suggest that small changes (exceeding 3% or 46 mV) in mean scapular muscle sEMG activity in a single testing session are likely to represent true changes. Additionally, the inter-session normalized and absolute mean sEMG reliability established in this study support the use of either sEMG to detect changes in scapulothoracic neuromuscular activity over time. The changes in sEMG exceeding 11.7% MVIC or 135 mV between sessions are likely true changes that exceed measurement error. Scapular muscle activity has been examined in single testing session during various tasks such as wheelchair transfers (Finley et al., 2005), swimming (Ruwe et al., 1994), and contractions against resistance (Cools et al., 2007). We investigated scapular muscle EMG reliability during a bilateral overhead lifting task for two reasons. First, it is a functional movement common to many activities of daily living (Lin et al., 2005). Second, this task is used frequently to clinically evaluate shoulder motion and function (Mcclure et al., 2009; Uhl et al., 2009). Only a few have studies have
examined scapular muscle EMG activity during an overhead lifting or elevation task and reported reliability of these measures. Ludewig and Cook (2000) found scapular muscle alterations between 4% and 18% MVIC during a similar purposeful lifting task in individuals with shoulder impingement compared to asymptomatic controls in single session. Authors reported inter-trial (withinsession) relative reliability in the lower trapezius, upper trapezius, and serratus anterior with ICCs between 0.78 and 0.89 during three separate phases of a concentric overhead lifting task (2.3 kg), but did not relate the EMG findings to absolute error (SEM) or report the reliability of the MVIC data used to normalize the EMG data. Our reliability results for within session normalized activity during the concentric elevation phase are comparable (ICC = 0.97–0.99). In a second study, Lin et al. (2011) also identified alterations between 14% and 25% in mean normalized serratus anterior and upper trapezius muscle activity in amateur and student athletes with shoulder impingement compared to asymptomatic controls during a purposeful arm elevation task. However, in this study reliability was not reported and findings were not related to SEM. Lastly, a study by Ebaugh and Spinelli examined mean absolute scapular EMG during an overhead lifting task in a single session (Ebaugh and Spinelli, 2010). In healthy individuals, authors found significantly reduced mean muscle activity of the lower trapezius
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(42%), serratus anterior (39%), and upper trapezius (61%) during the eccentric compared to the concentric phase of elevation in healthy individuals. In our study, muscle activity of scapular muscles during the eccentric phase was also lower by 54% in the lower trapezius, 21% in the serratus anterior, and 45% in upper trapezius. Ebaugh and Spinelli reported absolute scapular muscle mean activity (range 5– 250 mV) and SEM (range 18–21 mV) during an overhead lifting task without normalizing the data to reference task or contraction. Our results are comparable (Table 2) with absolute mean EMG activity during the lifting task (range 77–219 mV) in the concentric phase and (range 42–100 mV) in the eccentric phase and SEM with a range of 4–33 mV. However, we caution against a comparison of absolute values between studies without normalization because it does not take into account numerous technical, anatomical and physiological factors that can influence EMG magnitude (Burden, 2010; Deluca, 1997). Normalization processing attempts to avoid threats to misinterpretation of the signal across studies (Lehman and Mcgill, 1999). The absolute error in mean EMG activity during an overhead lifting task established in this study provides a magnitude of error that may be used to interpret scapular mean activity data between healthy cohorts and in individuals over time. However, these results are generalizable to the sEMG data processing parameters and methods applied including the ability to obtain reliable MVIC to report normalized data (Table 3). The within session MVIC sEMG data in our study was very good (ICC > 0.96). We also averaged two trials of maximum sEMG data generated with MVIC to improve reliability of our normalization data. While a few studies have reported SEM of mean scapular sEMG data during an elevation task (Ebaugh and Spinelli, 2010; Ludewig and Cook, 2000), to our knowledge this is the first study to establish the intra- or inter-session absolute error of scapular muscle mean activity in terms of the MDC and inter-session reliability. In the current study, the reliability of scapular muscle onset timing was established with the feed forward activity using a 10% threshold for onset determination to facilitate comparison with prior studies (Cools et al., 2002, 2003; De Mey et al., 2009) and to minimize issues using lower threshold values with interference during rest phase between trials. Mean muscle onset timing is likely influenced by the type of task, feed forward versus feedback, which complicates comparison of our results to prior studies. Feed forward activities consist of planned intentional movements such as bilateral overhead lifting. In contrast, feedback activities are those that require a muscle respond to an external stimulus and are likely sensitive to reaction time. Good inter-session reliability (ICC) and SEM for mean relative scapular muscle onset timing relative to movement of the arm has been previously reported during a feedback type of activity, such as a reaction to an external perturbation of the arm (Cools et al., 2002). However the MDC was not presented. Other studies have examined muscle onset timing with a feedforward tasks relative to the movement of the arm (Wadsworth and Bullock-Saxton, 1997) or relative to the deltoid (De Mey et al., 2009), but did not report reliability. This is the first study to provide evidence of between day reliability for scapular muscle onset timing with a feed forward task both relative to movement of the arm (goniometer) and relative to onset of the prime mover of the deltoid. Our results suggest that reliability of muscle onset is slightly better when calculated relative to the activation of prime mover than to the onset of arm movement; however both methods were challenged by lower ICC values.
6. Limitations There are some limitations that we recognize. Collecting EMG data with surface sensors provides data on only a small region of
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the muscle, just beneath the sensor. Although careful placement of the electrodes and visual confirmation of the raw sEMG signal was performed, we are unable to completely the eliminate the potential of cross talk from surrounding muscles. This study evaluated the sEMG reliability in healthy subjects with a specific intentional overhead lifting task. Therefore, the results are generalizable to asymptomatic individuals who may be at risk of shoulder pain but without symptoms. Additionally we recognize these results are generalizable to specific testing and processing parameters including the use of the average of two MVICs to normalize the data and selection of a 10% threshold for onset determination. Onset determination using other methods or with a different task may yield more reliable results. We selected these parameters based on procedures established in prior studies and methods used to clinically to evaluate shoulder motion so that the findings may be more generalizable to pre-participation or employment injury prevention screenings. 7. Conclusion Mean activity and relative onset timing of the serratus anterior, lower trapezius, and upper trapezius as determined by EMG is reliable in individuals during an overhead lifting task within a session. Mean activity of the scapular muscles are also reliable between sessions, but measures of relative onset timing during a feed forward activity are more variable using these specific processing (10% onset threshold) parameters. The MDC necessary to infer a meaningful change that is beyond error of the measure was established. Relatively small changes over time in normalized mean scapular activity during both concentric and eccentric phases of elevation can be interpreted as true change. Future studies are necessary to determine the effects of exercise on scapular neuromuscular performance in laborers, overhead athletes, and the general population susceptible to shoulder injuries. References Altman DG, Schulz KF, Moher D, Egger M, Davidoff F, Elbourne D, et al. The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Ann Intern Med 2001;134:663–94. Bagg SD, Forrest WJ. A biomechanical analysis of scapular rotation during arm abduction in the scapular plane. Am J Phys Med Rehabil 1988;67:238–45. Burden A. How should we normalize electromyograms obtained from healthy participants? What we have learned from over 25 years of research. J Electromyogr Kinesiol 2010;20:1023–35. Cools AM, Declercq GA, Cambier DC, Mahieu NN, Witvrouw EE. Trapezius activity and intramuscular balance during isokinetic exercise in overhead athletes with impingement symptoms. Scand J Med Sci Sports 2007;17:25–33. Cools AM, Witvrouw EE, De Clercq GA, Danneels LA, Willems TM, Cambier DC, et al. Scapular muscle recruitment pattern: electromyographic response of the trapezius muscle to sudden shoulder movement before and after a fatiguing exercise. J Orthop Sports Phys Ther 2002;32:221–9. Cools AM, Witvrouw EE, Declercq GA, Danneels LA, Cambier DC. Scapular muscle recruitment patterns: trapezius muscle latency with and without impingement symptoms. Am J Sports Med 2003;31:542–9. Cools AM, Witvrouw EE, Mahieu NN, Danneels LA. Isokinetic scapular muscle performance in overhead athletes with and without impingement symptoms. J Athl Train 2005;40:104–10. Crow J, Pizzari T, Buttifant D. Muscle onset can be improved by therapeutic exercise: a systematic review. Phys Ther Sport 2011;12:199–209. De Luca CJ. The use of surface electromyography in biomechanics. /Utilisation de l’ electromyographie de surface en biomecanique. J Appl Biomech 1997;13:135–63. De Mey K, Cagnie B, Danneels LA, Cools AM, Van De Velde A. Trapezius muscle timing during selected shoulder rehabilitation exercises. J Orthop Sports Phys Ther 2009;39:743–52. Deluca C. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–6. Ebaugh DD, Spinelli BA. Scapulothoracic motion and muscle activity during the raising and lowering phases of an overhead reaching task. J Electromyogr Kinesiol 2010;20:199–205. Ekstrom RA, Bifulco KM, Lopau CJ, Andersen CF, Gough JR. Comparing the function of the upper and lower parts of the serratus anterior muscle using surface electromyography. J Orthop Sports Phys Ther 2004;34:235–43.
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Finley MA, Mcquade KJ, Rodgers MM. Scapular kinematics during transfers in manual wheelchair users with and without shoulder impingement. Clin Biomech 2005;20:32–40. Johnson GR, Pandyan AD. The activity in the three regions of the trapezius under controlled loading conditions–an experimental and modelling study. Clin Biomech (Bristol, Avon) 2005;20:155–61. Kibler WB. The role of the scapula in athletic shoulder function. Am J Sports Med 1998;26:325–37. Kibler WB, Mcmullen J. Scapular dyskinesis and its relation to shoulder pain. J Am Acad Orthop Surg 2003;11:142–51. Kibler WB, Sciascia A. Current concepts: scapular dyskinesis. Br J Sports Med 2010;44:300–5. Kronberg M, Nemeth G, Brostrom LA. Muscle activity and coordination in the normal shoulder An electromyographic study. Clin Orthop 1990;257:76–85. Kuhn JE. Exercise in the treatment of rotator cuff impingement: a systematic review and a synthesized evidence-based rehabilitation protocol. J Shoulder Elbow Surg 2009;18:138–60. Lehman GJ, Mcgill SM. The importance of normalization in the interpretation of surface electromyography: a proof of principle. J Manipulative Physiol Ther 1999;22:444–6. 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 3D electromagnetic measurement system. J Rehabil Res Dev 2005;42:199–210. Lin JJ, Hsieh SC, Cheng WC, Chen WC, Lai Y. Adaptive patterns of movement during arm elevation test in patients with shoulder impingement syndrome. J Orthopaedic Res 2011;29:653–7. Ludewig PM, Borstad JD. Effects of a home exercise programme on shoulder pain and functional status in construction workers. Occup Environ Med 2003;60:841–9. 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. Specific evaluation of the function of force couples relevant for stabilization of the genohumeral joint. Man Ther 2003;8:247–53. 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. Mclean L, Chislett M, Keith M, Murphy M, Walton P. The effect of head position, electrode site, movement and smoothing window in the determination of a reliable maximum voluntary activation of the upper trapezius muscle. J Electromyogr Kinesiol 2003;13:169–80. Melton C, Mullineaux DR, Mattacola CG, Mair SD, Uhl TL. Reliability of video motion-analysis systems to measure amplitude and velocity of shoulder elevation. J Sport Rehab 2011;20:393–405. Minning S, Eliot CA, Uhl TL, Malone TR. EMG analysis of shoulder muscle fatigue during resisted isometric shoulder elevation. J Electromyogr Kinesiol 2007;17:153–9. Nieminen H, Takala EP, Viikari-Juntura E. Normalization of electromyogram in the neck-shoulder region. Eur J Appl Physiol Occup Physiol 1993;67:199–207. Reinold MM, Escamilla RF, Wilk KE. Current concepts in the scientific and clinical rationale behind exercises for glenohumeral and scapulothoracic musculature. J Orthop Sports Phys Ther 2009;39:105–17. Roy JS, Moffet H, Hebert LJ, Lirette R. Effect of motor control and strengthening exercises on shoulder function in persons with impingement syndrome: a single-subject study design. Man Ther 2009a;14:180–8. Roy JS, Moffet H, Mcfadyen BJ, Lirette R. Impact of movement training on upper limb motor strategies in persons with shoulder impingement syndrome. Sports Med Arthrosc Rehabil Ther Technol 2009b;1:8. Ruwe PA, Pink M, Jobe FW, Perry J, Scovazzo ML. The normal and the painful shoulders during the breaststroke. Electromyographic and cinematographic analysis of twelve muscles. Am J Sports Med 1994;22:789–96.
Shrout P, Fleiss J. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 1979;86:420–8. Stratford PW, Binkley FM, Riddle DL. Health status measures: strategies and analytic methods for assessing change scores. Phys Ther 1996a;76:1109–23. Stratford PW, Binkley J, Solomon P, Finch E, Gill C, Moreland J. Defining the minimum level of detectable change for the Roland–Morris questionnaire. Phys Ther 1996b;76:359–65. Tate AR, Mcclure PW, Young IA, Salvatori R, Michener LA. Comprehensive impairment-based exercise and manual therapy intervention for patients with subacromial impingement syndrome: a case series. J Orthop Sports Phys Ther 2010;40:474–93. Uhl TL, Kibler WB, Gecewich B, Tripp BL. Evaluation of clinical assessment methods for scapular dyskinesis. Arthroscopy 2009;25:1240–8. Wadsworth DJ, Bullock-Saxton JE. Recruitment patterns of the scapular rotator muscles in freestyle swimmers with subacromial impingement. Int J Sports Med 1997;18:618–24. Zipp P. Recommendations for the standardization of lead positions in surface electromyography. Eur J Appl Physiol 1982;50:41–54.
Amee L. Seitz, PhD, DPT, OCS is currently an Assistant Professor in the Department of Physical Therapy and Director of the Biomotion Research Laboratory at Northeastern University. She completed a Bachelor of Science in Physical Therapy at Ohio University, and an advanced Masters of Science in Orthopaedic Physical Therapy and a transitional Clinical Doctorate from the MGH Institute of Health Professions. She earned a PhD in Rehabilitation & Movement Science from Virginia Commonwealth University and completed post-doctoral work as a visiting scholar at the University of Kentucky. She is a Board-Certified Orthopaedic Clinical Specialist from the American Board of Physical Therapy Specialties and serves as an Editorial Board Member for the Journal of Sport Rehabilitation. Amee’s clinical expertise is in the rehabilitation of patients with shoulder disorders. Her research focus is on the neuromuscular and biomechanical mechanisms of upper extremity musculoskeletal disorders and associated rehabilitation outcomes.
Timothy L. Uhl, PhD, PT, ATC, FNATA is an associate professor and co-director of the Musculoskeletal Laboratory in the Department of Rehabilitation Sciences at the University of Kentucky, Lexington, KY, USA. He received his PT degree in 1985 from the University of Kentucky, his masters’ in kinesiology from the University of Michigan in 1992 and his doctorate from the University of Virginia in 1998. His research focuses on shoulder rehabilitation outcomes and exercise progressions.
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Reliability and minimal detectable change in scapulothoracic neuromuscular activity Amee L. Seitz a,⇑, Timothy L. Uhl b a b
Department of Physical Therapy, Bouvé College of Health Sciences, Northeastern University, Boston, MA, USA Department of Rehabilitation Sciences, College of Health Sciences, University of Kentucky, Lexington, KY, USA
a r t i c l e
i n f o
Article history: Received 27 December 2011 Received in revised form 13 May 2012 Accepted 13 May 2012
Keywords: Shoulder EMG Lower trapezius Serratus anterior Impingement Scapula
a b s t r a c t Alterations in scapular muscle activity, including excess activation of the upper trapezius (UT) and onset latencies of the lower trapezius (LT) and serratus anterior (SA) muscles, are associated with abnormal scapular motion and shoulder impingement. Limited information exists on the reliability of neuromuscular activity to demonstrate the efficacy of interventions. The purpose of this study was to characterize the reproducibility of scapular muscle activity (mean activity, relative onset timing) over time and establish the minimal detectable change (MDC). Surface electromyography (sEMG) of the UT, LT, SA and anterior deltoid (AD) muscles in 16 adults were captured during an overhead lifting task in two sessions, oneweek apart. sEMG data were also normalized to maximum isometric contraction and the relative onset and mean muscle activity during concentric and eccentric phases of the scapular muscles were calculated. Additionally, reliability of the absolute sEMG data during the lifting task and MVIC was evaluated. Both intrasession and intersession reliability of normalized and absolute mean scapular muscle activity, assessed with intraclass correlation coefficients (ICC), ranged from 0.62 to 0.99; MDC values were between 1.3% and 11.7% MVIC and 24 to 135 mV absolute sEMG. Reliability of sEMG during MVIC was ICC = 0.82–0.99, with the exception of intersession upper trapezius reliability (ICC = 0.36). Within session reliability of muscle onset times was ICC = 0.88–0.97, but between session reliability was lower with ICC = 0.43–0.73; MDC were between 39 and 237 ms. Small changes in scapular neuromuscular mean activity (>11.7% MVIC) can be interpreted as meaningful change, while change in muscle onset timing in light of specific processing parameters used in this study is more variable. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Abnormal scapular motion has been implicated in the pathogenesis of shoulder pain and impingement (Kibler, 1998; Kibler and Mcmullen, 2003; Kibler and Sciascia, 2010) and has been characterized by changes in scapular muscle electromyographic (EMG) activity (Ludewig and Cook, 2000). Of particular interest are the relative contributions of the serratus anterior and trapezius muscles that stabilize the scapula and induce scapular motion necessary for humeral elevation (Bagg and Forrest, 1988; Johnson and Pandyan, 2005; Kronberg et al., 1990). Abnormal scapular neuromuscular control, demonstrated by excess EMG mean activity of the upper trapezius, decreased mean activity of the serratus anterior (Ludewig and Cook, 2000), and altered EMG onset timing in the lower trapezius and serratus anterior muscles, has been found in individuals with shoulder pain associated with impingement ⇑ Corresponding author. Address: Department of Physical Therapy, Northeastern University, 360 Huntington Ave., Robinson 6, Boston, MA 02115, USA. Tel.: +1 617 373 7626; fax: +1 617 373 7630. E-mail address: [email protected] (A.L. Seitz). 1050-6411/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jelekin.2012.05.003
(Cools et al., 2007, 2003, 2005; Roy et al., 2009b; Wadsworth and Bullock-Saxton, 1997). Given these findings, therapeutic interventions that address an imbalance in scapular muscle neuromuscular activity and control rather than purely muscle strength have been advocated in evidence-based shoulder rehabilitation and injury prevention programs (Kuhn, 2009; Ludewig and Borstad, 2003; Reinold et al., 2009; Roy et al., 2009a; Tate et al., 2010). A recent systematic review suggests that muscle onset timing as measured with EMG can be changed with therapeutic exercise (Crow et al., 2011). However, there is a lack of evidence that the scapular muscle balance and control as measured with EMG can be altered with exercise, despite the widespread use of therapeutic exercise to address such impairments in injury prevention and rehabilitation programs. To determine whether programs are effective at normalizing scapular muscle balance, reliable measures of neuromuscular function such as mean muscle activity and onset timing are needed. To date, limited information exists on the reliability of scapular muscle EMG. Cools et al. (2002) established good reliability of between day scapular muscle EMG onset relative to the deltoid during a sudden arm perturbation with intraclass correlation
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coefficients (ICC) = 0.73–0.78. However, the reliability of onset timing during a purposeful movement was not studied. Minning et al. reported good within day (0.75–0.83) but poor between day reliability (ICC = 0.03–0.29) of mean scapular muscle activity during an isometric fatiguing contraction (Minning et al., 2007). Ludewig and Cook reported within-day between trial reliability of mean normalized scapular EMG amplitude data to be between ICC = 0.73 and 0.89 with an overhead lifting task with and without hand weights (Ludewig and Cook, 2000). Ebaugh and Spinelli compared eccentric and concentric surface EMG of absolute scapular muscle activity during an overhead reaching task without weight and found very good between within session relative reliability (ICC = 0.87–0.94) for root mean square amplitude data (Ebaugh and Spinelli, 2010). Authors also reported absolute reliability with the standard error of the measure, in millivolts because the EMG data were not normalized. Furthermore, this study consisted of a single testing session as such the intersession reliability was not studied. Crow et al. (2011) reported the absolute intersession reliability of select scapular muscles, specifically the serratus anterior and upper trapezius, with co-efficients of variation for between day normalized mean amplitude EMG data from 4.2% to 10.3% a maximum voluntary contraction during concentric and eccentric phases of a repetitive lifting task. However, relative reliability with intraclass correlation coefficients, the mean activity of the lower trapezius muscle, and muscle onset timing were not factors examined in this study. The absolute and relative intersession reliability of scapular muscle EMG amplitude and onset timing during purposeful movements such as an overhead lifting task is necessary to determine whether change in measures of scapular neuromuscular control with therapeutic intervention over time is beyond measurement error. Therefore, the purpose of this study is to characterize the reproducibility of scapular muscle activity (mean activity, relative onset timing) during a resisted bilateral overhead lifting task, determine the stability of these measures over time, and establish the absolute error with the standard error of the measure (SEM) and minimal detectable change (MDC). 2. Methods 2.1. Subjects Sixteen volunteers (8 males; 8 females; mean age = 28.0 ± 6.9 years; BMI = 23.3 ± 2.8) free from shoulder pain were recruited by a sample of convenience from the community and met eligibility criteria. All subjects were between the ages of 18 and 65 years, free of shoulder and neck pain within the last 6 months, and had no known shoulder or neck pathology, neurological disorders, adhesive allergies, or history of shoulder fracture or surgery. Eligible subjects were screened for normal shoulder range of motion and pain free shoulder strength. All eligible volunteers gave written and informed consent prior to participation. The study was approved by the University of Kentucky Institutional Review Board. All subjects completed two testing sessions that were between 4 and 10 days apart (mean 6.4 days, SD 1.8). No subject reported participating in an unusually strenuous activity 48 h prior to the first testing session and reported adherence to the request to avoid unusually strenuous activity between testing sessions. 2.2. Electromyography During each session, a 16-channel EMG system (Run Technologies, Mission Viejo, CA) was used to record muscle activity at a bandwidth of 10–2000 Hz. All raw EMG data was transmitted at 2000 Hz via a fiber optic cable through a Myopac transmitter unit
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(Run Technologies, Mission Viejo, CA) to its receiver unit with impedance of 1 MX and common mode rejection ratio of 90 dB min at 60 Hz. The sEMG were differentially amplified at 2000 times. All signals EMG were transferred to an analog to digital converter (12 bit resolution) before being imported into a desktop computer for processing and analysis. Surface EMG (sEMG) electrodes were placed over the upper and lower portion of the trapezius, serratus anterior, and anterior deltoid muscles in specific anatomical locations using previously established standardized methods (Ekstrom et al., 2004; Mclean et al., 2003; Nieminen et al., 1993; Zipp, 1982) described in Table 1. These specific scapular muscles were chosen given their function to control normal scapular motion during arm elevation (Bagg and Forrest, 1988; Johnson and Pandyan, 2005; Kronberg et al., 1990). The deltoid was examined as a prime mover for humeral elevation. To apply the surface electrodes, the skin was shaved, lightly abrading with fine sandpaper, and cleaned with alcohol to minimize skin impedance (De Luca, 1997). Bipolar Ag/AgCl circular pre-gelled surface electrodes (Blue Sensor; Ambu Inc., Glen Burnie, MD) were placed parallel to each muscle with a 2-cm center to center interelectrode distance. A reference electrode was placed over the contralateral acromion. The surface electrodes were connected to a belt amplifier which was secured posteriorly to the subject’s waist. Correct electrode placement was confirmed by visual inspection of the raw sEMG signals on an oscilloscope. Measurement (cm) of distances from the specific anatomical landmarks for exact electrode placement were recorded and referenced in the second testing session. The same examiner performed data collection on all subjects and was blinded to the first session EMG data during the second session testing. 2.3. Electrogoniometer An electrogoniometer, used to define the concentric and eccentric phases of the lifting task, was placed on the shoulder fixed to the spine of the scapula and middle deltoid. The electrogoniometer and sEMG signals were collected synchronous during data collection through the Myopac acquisition hardware and displayed synchronously in Datapac signal processing software (Version 5.0, Run Technologies, Mission Viejo, CA). The electrogoniometer signal was differentially amplified 1000 times and transferred to an analog to digital converter (12 bit resolution) before being imported into a desktop computer for recording and analysis. 2.4. Lifting task During each session, simultaneous sEMG and electrogoniometer data were collected continuously while the subjects performed 10 repetitions of bilateral humeral elevation holding either 1.4 kg (3 lb) or 2.3 kg (5 lb) weights. The heavier (2.3 kg) weights were used by individuals over 68.1 kg of body weight. Subjects started with the arms resting at his or her side. Then subjects were asked to raise both arms with thumbs facing upwards (medially to maximum elevation) with elbows extended (Mcclure et al., 2009). The plane of humeral elevation was standardized to 40° anterior to the coronal plane with two free standing poles to serve as a visual guide. A metronome set at 60 beats per minute was used to standardize the rate of humeral elevation and lowering (Melton et al., 2011). Subjects practiced the rate of movement from rest to maximal elevation in 2 s and lowering to start position in 2 s (Fig. 1a–c.). Subjects were instructed to relax for 2 s between trials. 2.5. Maximum voluntary isometric contractions Maximum voluntary isometric contractions (MVIC) were used to verify sEMG signal integrity with each muscle and normalize
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Table 1 Surface electrode placement and positions used to establish the maximum voluntary isometric contraction. Electrode placement and maximum voluntary isometric contraction test positions of each muscle Muscle
Electrode placement
Position
Anterior deltoid
A measure 1/5th length of the clavicle from the anterior lateral aspect was made and marked. The electrodes were placed with 1/ 5th distance between this point and the lateral epicondyle (elbow bent, neutral shoulder rotation) Zipp (1982) A mark was made on the skin at the midpoint on a line joining the C7 spinous process and tip of the acromion. The electrodes were placed over a point 1/2 the distance between this point and the posterior lateral angle of the acromion Mclean et al. (2003) With the arm elevated in the scapular plane to 125°, the electrodes were placed at the midpoint from the T7 spinous process to the inferior angle of the scapula Nieminen et al. (1993) With the arm elevated in the scapular plane to 125°, the electrodes were placed over the 7th intercostal space, just anterior to the fibers of the latissimus dorsi Ekstrom et al. (2004)
While seated, resistance was applied to the distal arm as the subject performed humeral elevation at 125° of flexion
Upper trapezius
Lower trapezius
Serratus Anterior
the sEMG data during the lifting task. The standardized MVIC test positions are summarized in Table 1. For each muscle, two MVIC 5s maximal contractions were captured with a 1-min rest between contractions. In each session, a resting sEMG level of each muscle was also recorded with the subject standing. 2.6. Data reduction All raw sEMG data were processed with Datapac Version 5.0 software (Run Technologies, Mission Viejo, CA). Raw sEMG signals were digitally filtered to correct for any DC offset with a passive demeaning filter, followed by a high pass 4th order finite impulse response filter with a 10 Hz cut-off frequency, then full wave rectified. A low pass 4th order Butterworth filter with 6 Hz cut off frequency was used to smooth the data. The MVIC was determined by averaging the highest 500 ms window of mean sEMG activity during two separate 5 s trials for each muscle. Mean normalized and absolute sEMG amplitude was also calculated for both the concentric and eccentric phases of the lifting task by first subtracting the background resting sEMG data from the mean activity during each phase. The phases of elevation were defined by positive and negative signals of the first derivative of the electro-goniometer signal. Mean sEMG amplitude was expressed as absolute values (in millivolts) and normalized as the percentage of MVIC (Burden, 2010). Five middle trials (repetitions 4–8) of the elevation task in each muscle in each session were used for statistical analysis. A threshold of >10% MVIC beyond resting activity was used to determine muscle onset timing during the concentric phase elevation. The 10% threshold was used in previous research to enhance consistency and minimize interference with resting muscle activity (Cools et al., 2002) and has been consistently used to identify scapular muscle timing disorders in individuals with impingement (Cools et al., 2002, 2003; De Mey et al., 2009). Early activation of the stabilizing muscles at the proximal scapulothoracic joint in relation to prime-mover activation (deltoid) at the glenohumeral joint is necessary for proper scapulothoracic stability (Magarey and Jones, 2003). Additionally, temporal sequence of the scapular muscles to actual arm movements are important factors in coordinating scapular motion with humeral elevation (Kibler, 1998). Thus, scapular muscle onset timing in this study was expressed in milliseconds both relative to the onset of the humeral prime mover the deltoid and humeral elevation defined using goniometer. Negative timing values reflect earlier onset of the upper trapezius, lower trapezius, or serratus anterior muscle in relation to the anterior deltoid or goniometer. Positive onset timing values reflect onset of muscle activity after either the anterior deltoid activity or humeral movement. The mean scapular muscle onset timing of the
While seated, resistance was applied to the distal humerus as the subject performed shoulder abduction at 90° of abduction
While in a prone position with the arm abducted to 120°, resistance is applied to the radial aspect of the distal forearm as the subject performed horizontal abduction While seated, resistance was applied to the distal arm as the subject performed humeral elevation at 125° of flexion
five middle trials (repetitions 4–8) for each muscle were used for statistical analysis. 3. Statistical analysis The relative reliability of absolute (in millivolts) and normalized (%MVIC) mean sEMG activity during each phase (concentric, eccentric) and scapular muscle onset relative to anterior deltoid and humeral elevation was determined by calculating the Intraclass Correlation Coefficient (ICC) for criterion measures both within and across sessions (Shrout and Fleiss, 1979). The within session reliability were calculated comparing five trials (repetitions 4 through 8) and the between session reliability were calculated by comparing the mean of the five trials between sessions. To improve the generalizability of the normalized sEMG results, we calculated the reliability of the MVIC sEMG amplitude in each muscle. The within session MVIC sEMG reliability were calculated comparing two trials of the MVIC, and the between session reliability were calculated by comparing the mean of two trials between sessions. For all analyses, the ICC values were considered: poor when below 0.20; fair from 0.21 to 0.40; moderate from 0.41 to 0.60; good from 0.61 to 0.80; and very good from 0.81 to 1.00 (Altman et al., 2001). The absolute reliability was defined as the SEM and the MDC. The SEM was defined as the standard deviation multiplied by the square root of the ICC subtracted from 1 (Stratford et al., 1996a). The MDC was calculated by multiplying the SEM by the square root of 2 (Stratford et al., 1996b). All statistical analyses were conducted with the IBM SPSS Statistics software (Version 19; IBM Corp, Armonk, NY). 4. Results Results of the within and between session reliability of sEMG with the ICC, SEM, and MDC are shown in Tables 2–5. 4.1. Intra-session and inter-session absolute mean sEMG Intra-session relative reliability of absolute mean scapular and anterior deltoid muscle activity during both phases of elevation was very good (ICC = 0.95–0.99). Intra-session MDC values were between 42 and 219 mV in all muscles during both phases of elevation. Inter-session reliability of absolute mean sEMG activity during both phases of the lifting task in the serratus anterior were very good (ICC = 0.89–0.90), good for the upper trapezius (ICC = 0.70) and lower trapezius (0.62–0.74), and good to very good for the anterior deltoid (ICC = 0.78–0.85). In all muscles, the intersession MDC of absolute mean muscle activity was between 90 and
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Fig. 1. (a) Start, (b) middle, and (c) end position of the overhead lifting task.
Table 2 Intra and inter-session reliability results for absolute mean scapular muscle sEMG activity (in millivolts) during the overhead lifting task. Variable
Scapular muscle
Intra-session
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
Concentric mean absolute activity (mV)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.99 0.96 0.97 0.98
202 216 219 77
13 23 33 6
18 32 46 8
0.85 0.90 0.70 0.62
202 320 216 90
36 95 70 33
51 135 99 47
Eccentric mean absolute activity (mV)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.99 0.95 0.97 0.97
68 46 100 42
5 8 16 4
7 11 23 6
0.78 0.89 0.70 0.74
69 55 97 49
14 16 27 17
19 23 39 24
mV, millivolts; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
320 mV during the concentric phase of elevation and between 49 and 97 mV during the eccentric phase. 4.2. Intra and inter-session MVIC sEMG Absolute sEMG maximum values (in mV) during the MVICs and reliability results are provided in Table 3. Intra-session reliability of absolute mean values during the two MVIC trials were very good (ICC = 0.97–0.99) for both the deltoid and scapular muscles with MDC values between 46 and 82 mV. The inter-session reliability of the mean MVIC sEMG values were very good for the anterior deltoid, serratus anterior, and lower trapezius muscles (ICC = 0.82– 0.89) with MDC absolute values between 121 and 204 mV, but fair for the upper trapezius muscle (ICC = 0.36). The inter-session MDC for mean MVIC EMG values of the upper trapezius was 316 mV. 4.3. Intra-session and inter-session normalized EMG Results of the within and between session normalized EMG reliability of the elevation task is shown in Table 4. Intra-session relative reliability of normalized scapular and anterior deltoid muscle activity during both phases of elevation was very good (ICC = 0.96–0.99). Intra-session MDC values were less than 3% MVIC for the normalized data during both phases of elevation. Inter-session reliability of normalized mean EMG activity during both phases of the lifting task in the lower trapezius and serratus anterior were very good (ICC = 0.82–0.86), good for the upper trapezius (ICC = 0.66–0.79), and moderate for the anterior deltoid (ICC = 0.59). The intersession MDC for lower trapezius normalized
mean muscle activity during both phases of elevation was between 3.2% and 3.9% MVIC. The intersession MDC for normalized mean muscle activity of the serratus anterior and upper trapezius during the concentric phase was 10.3% and 11.4%, respectively. Corresponding with smaller mean normalized sEMG activity, the MDC values were lower in all muscles during the eccentric phases ranging from 3% to 8% MVIC. The intersession MDC for mean muscle activity of the deltoid during the concentric phase was 11.7% and 5.8% during the eccentric phase. 4.4. Intra-session and inter-session relative muscle onset timing Results of the within and between session relative muscle onset timing reliability of the elevation task is shown in Table 5. Reliability of scapular muscle onset times relative to the prime mover of the deltoid was very good (ICC = 0.88–0.97) within session, but poor to moderate (ICC = 0.43–0.73) between sessions. Similarly the relative onset of the scapular muscles to the goniometer was very good (ICC = 0.93–0.96) within session, but poor to moderate (ICC = 0.08–0.49) between sessions. Reliability was higher and MDC values were smaller for the scapular muscle onset timing relative to the deltoid (MDC between 39 and 237 ms) compared to the goniometer (MDC between 62 and 250 ms). 5. Discussion To determine the efficacy of injury prevention and rehabilitation programs prescribed to normalize scapular muscle function, measures of neuromuscular activity must be reliable. The results of this
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Table 3 Intra and inter-session reliability results for absolute mean scapular muscle sEMG activity (in millivolts) with two trials of maximum isometric voluntary contraction in each session. Variable
Scapular muscle
Reliability MVIC maximum amplitude (mV)
Intra-session
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
0.98 0.99 0.97 0.98
392 364 468 445
33 33 58 46
47 46 82 65
0.89 0.83 0.36 0.82
433 398 490 502
85 144 223 144
121 204 316 204
MVIC, percent of maximal voluntary isometric contraction; mV, millivolts; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
Table 4 Intra and inter-session reliability results for normalized mean scapular muscle sEMG activity during the overhead lifting task. Variable
Scapular muscle
Intra-session
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
Concentric mean activity (%MVIC)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.98 0.99 0.98 0.97
53.4 44.4 45.6 19.7
2.0 1.5 1.7 1.2
2.9 2.1 2.5 1.7
0.59 0.86 0.66 0.85
51.6 44.8 45.0 19.2
8.3 7.3 8.0 2.7
11.7 10.3 11.4 3.9
Eccentric mean activity (%MVIC)
Anterior deltoid Serratus anterior Upper trapezius Lower trapezius
0.97 0.99 0.96 0.97
18.4 18.4 20.3 11.1
1.0 1.7 1.3 1.0
1.5 2.4 1.9 1.3
0.59 0.85 0.79 0.82
18.3 18.1 20.9 11.1
4.1 5.4 3.5 2.3
5.8 7.6 4.9 3.2
%MVIC, percent of maximal voluntary isometric contraction; msec, millisecond; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
Table 5 Intra and inter-session reliability results for onset timing relative to the anterior deltoid and goniometer during the overhead lifting task. Variable
Scapular muscle
Intra-session
Inter-session
ICC
Mean
SEM
MDC
ICC
Mean
SEM
MDC
Relative onset to anterior deltoid (msec)
Serratus anterior Upper trapezius Lower trapezius
0.93 0.97 0.88
67.0 8.9 147.4
38.7 28.0 57.3
54.8 39.6 81.0
0.67 0.73 0.43
85.0 12.0 201.8
89.8 84.5 167.9
127.0 119.6 237.5
Relative onset to goniometer (msec)
Serratus anterior Upper trapezius Lower trapezius
0.95 0.96 0.93
13.9 89.8 66.4
52.1 43.9 65.6
73.7 62.1 92.8
0.49 0.35 0.08
31.1 41.9 147.9
120.5 133.4 176.9
170.4 188.6 250.1
msec, millisecond; ICC, intraclass correlation coefficient; SEM, standard error of the measure; MDC, minimal detectable change.
study suggest normalized and absolute mean activity of the serratus anterior, lower trapezius, upper trapezius and deltoid as measured with sEMG during a functional bilateral overhead lifting task is reproducible. Reproducible normalized sEMG data is also dependent upon reliable MVIC data (Table 2). The relatively small SEM and the MDC values for within-session mean normalized and absolute scapular muscle activity suggest that small changes (exceeding 3% or 46 mV) in mean scapular muscle sEMG activity in a single testing session are likely to represent true changes. Additionally, the inter-session normalized and absolute mean sEMG reliability established in this study support the use of either sEMG to detect changes in scapulothoracic neuromuscular activity over time. The changes in sEMG exceeding 11.7% MVIC or 135 mV between sessions are likely true changes that exceed measurement error. Scapular muscle activity has been examined in single testing session during various tasks such as wheelchair transfers (Finley et al., 2005), swimming (Ruwe et al., 1994), and contractions against resistance (Cools et al., 2007). We investigated scapular muscle EMG reliability during a bilateral overhead lifting task for two reasons. First, it is a functional movement common to many activities of daily living (Lin et al., 2005). Second, this task is used frequently to clinically evaluate shoulder motion and function (Mcclure et al., 2009; Uhl et al., 2009). Only a few have studies have
examined scapular muscle EMG activity during an overhead lifting or elevation task and reported reliability of these measures. Ludewig and Cook (2000) found scapular muscle alterations between 4% and 18% MVIC during a similar purposeful lifting task in individuals with shoulder impingement compared to asymptomatic controls in single session. Authors reported inter-trial (withinsession) relative reliability in the lower trapezius, upper trapezius, and serratus anterior with ICCs between 0.78 and 0.89 during three separate phases of a concentric overhead lifting task (2.3 kg), but did not relate the EMG findings to absolute error (SEM) or report the reliability of the MVIC data used to normalize the EMG data. Our reliability results for within session normalized activity during the concentric elevation phase are comparable (ICC = 0.97–0.99). In a second study, Lin et al. (2011) also identified alterations between 14% and 25% in mean normalized serratus anterior and upper trapezius muscle activity in amateur and student athletes with shoulder impingement compared to asymptomatic controls during a purposeful arm elevation task. However, in this study reliability was not reported and findings were not related to SEM. Lastly, a study by Ebaugh and Spinelli examined mean absolute scapular EMG during an overhead lifting task in a single session (Ebaugh and Spinelli, 2010). In healthy individuals, authors found significantly reduced mean muscle activity of the lower trapezius
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(42%), serratus anterior (39%), and upper trapezius (61%) during the eccentric compared to the concentric phase of elevation in healthy individuals. In our study, muscle activity of scapular muscles during the eccentric phase was also lower by 54% in the lower trapezius, 21% in the serratus anterior, and 45% in upper trapezius. Ebaugh and Spinelli reported absolute scapular muscle mean activity (range 5– 250 mV) and SEM (range 18–21 mV) during an overhead lifting task without normalizing the data to reference task or contraction. Our results are comparable (Table 2) with absolute mean EMG activity during the lifting task (range 77–219 mV) in the concentric phase and (range 42–100 mV) in the eccentric phase and SEM with a range of 4–33 mV. However, we caution against a comparison of absolute values between studies without normalization because it does not take into account numerous technical, anatomical and physiological factors that can influence EMG magnitude (Burden, 2010; Deluca, 1997). Normalization processing attempts to avoid threats to misinterpretation of the signal across studies (Lehman and Mcgill, 1999). The absolute error in mean EMG activity during an overhead lifting task established in this study provides a magnitude of error that may be used to interpret scapular mean activity data between healthy cohorts and in individuals over time. However, these results are generalizable to the sEMG data processing parameters and methods applied including the ability to obtain reliable MVIC to report normalized data (Table 3). The within session MVIC sEMG data in our study was very good (ICC > 0.96). We also averaged two trials of maximum sEMG data generated with MVIC to improve reliability of our normalization data. While a few studies have reported SEM of mean scapular sEMG data during an elevation task (Ebaugh and Spinelli, 2010; Ludewig and Cook, 2000), to our knowledge this is the first study to establish the intra- or inter-session absolute error of scapular muscle mean activity in terms of the MDC and inter-session reliability. In the current study, the reliability of scapular muscle onset timing was established with the feed forward activity using a 10% threshold for onset determination to facilitate comparison with prior studies (Cools et al., 2002, 2003; De Mey et al., 2009) and to minimize issues using lower threshold values with interference during rest phase between trials. Mean muscle onset timing is likely influenced by the type of task, feed forward versus feedback, which complicates comparison of our results to prior studies. Feed forward activities consist of planned intentional movements such as bilateral overhead lifting. In contrast, feedback activities are those that require a muscle respond to an external stimulus and are likely sensitive to reaction time. Good inter-session reliability (ICC) and SEM for mean relative scapular muscle onset timing relative to movement of the arm has been previously reported during a feedback type of activity, such as a reaction to an external perturbation of the arm (Cools et al., 2002). However the MDC was not presented. Other studies have examined muscle onset timing with a feedforward tasks relative to the movement of the arm (Wadsworth and Bullock-Saxton, 1997) or relative to the deltoid (De Mey et al., 2009), but did not report reliability. This is the first study to provide evidence of between day reliability for scapular muscle onset timing with a feed forward task both relative to movement of the arm (goniometer) and relative to onset of the prime mover of the deltoid. Our results suggest that reliability of muscle onset is slightly better when calculated relative to the activation of prime mover than to the onset of arm movement; however both methods were challenged by lower ICC values.
6. Limitations There are some limitations that we recognize. Collecting EMG data with surface sensors provides data on only a small region of
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the muscle, just beneath the sensor. Although careful placement of the electrodes and visual confirmation of the raw sEMG signal was performed, we are unable to completely the eliminate the potential of cross talk from surrounding muscles. This study evaluated the sEMG reliability in healthy subjects with a specific intentional overhead lifting task. Therefore, the results are generalizable to asymptomatic individuals who may be at risk of shoulder pain but without symptoms. Additionally we recognize these results are generalizable to specific testing and processing parameters including the use of the average of two MVICs to normalize the data and selection of a 10% threshold for onset determination. Onset determination using other methods or with a different task may yield more reliable results. We selected these parameters based on procedures established in prior studies and methods used to clinically to evaluate shoulder motion so that the findings may be more generalizable to pre-participation or employment injury prevention screenings. 7. Conclusion Mean activity and relative onset timing of the serratus anterior, lower trapezius, and upper trapezius as determined by EMG is reliable in individuals during an overhead lifting task within a session. Mean activity of the scapular muscles are also reliable between sessions, but measures of relative onset timing during a feed forward activity are more variable using these specific processing (10% onset threshold) parameters. The MDC necessary to infer a meaningful change that is beyond error of the measure was established. Relatively small changes over time in normalized mean scapular activity during both concentric and eccentric phases of elevation can be interpreted as true change. Future studies are necessary to determine the effects of exercise on scapular neuromuscular performance in laborers, overhead athletes, and the general population susceptible to shoulder injuries. References Altman DG, Schulz KF, Moher D, Egger M, Davidoff F, Elbourne D, et al. The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Ann Intern Med 2001;134:663–94. Bagg SD, Forrest WJ. A biomechanical analysis of scapular rotation during arm abduction in the scapular plane. Am J Phys Med Rehabil 1988;67:238–45. Burden A. How should we normalize electromyograms obtained from healthy participants? What we have learned from over 25 years of research. J Electromyogr Kinesiol 2010;20:1023–35. Cools AM, Declercq GA, Cambier DC, Mahieu NN, Witvrouw EE. Trapezius activity and intramuscular balance during isokinetic exercise in overhead athletes with impingement symptoms. Scand J Med Sci Sports 2007;17:25–33. Cools AM, Witvrouw EE, De Clercq GA, Danneels LA, Willems TM, Cambier DC, et al. Scapular muscle recruitment pattern: electromyographic response of the trapezius muscle to sudden shoulder movement before and after a fatiguing exercise. J Orthop Sports Phys Ther 2002;32:221–9. Cools AM, Witvrouw EE, Declercq GA, Danneels LA, Cambier DC. Scapular muscle recruitment patterns: trapezius muscle latency with and without impingement symptoms. Am J Sports Med 2003;31:542–9. Cools AM, Witvrouw EE, Mahieu NN, Danneels LA. Isokinetic scapular muscle performance in overhead athletes with and without impingement symptoms. J Athl Train 2005;40:104–10. Crow J, Pizzari T, Buttifant D. Muscle onset can be improved by therapeutic exercise: a systematic review. Phys Ther Sport 2011;12:199–209. De Luca CJ. The use of surface electromyography in biomechanics. /Utilisation de l’ electromyographie de surface en biomecanique. J Appl Biomech 1997;13:135–63. De Mey K, Cagnie B, Danneels LA, Cools AM, Van De Velde A. Trapezius muscle timing during selected shoulder rehabilitation exercises. J Orthop Sports Phys Ther 2009;39:743–52. Deluca C. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–6. Ebaugh DD, Spinelli BA. Scapulothoracic motion and muscle activity during the raising and lowering phases of an overhead reaching task. J Electromyogr Kinesiol 2010;20:199–205. Ekstrom RA, Bifulco KM, Lopau CJ, Andersen CF, Gough JR. Comparing the function of the upper and lower parts of the serratus anterior muscle using surface electromyography. J Orthop Sports Phys Ther 2004;34:235–43.
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Amee L. Seitz, PhD, DPT, OCS is currently an Assistant Professor in the Department of Physical Therapy and Director of the Biomotion Research Laboratory at Northeastern University. She completed a Bachelor of Science in Physical Therapy at Ohio University, and an advanced Masters of Science in Orthopaedic Physical Therapy and a transitional Clinical Doctorate from the MGH Institute of Health Professions. She earned a PhD in Rehabilitation & Movement Science from Virginia Commonwealth University and completed post-doctoral work as a visiting scholar at the University of Kentucky. She is a Board-Certified Orthopaedic Clinical Specialist from the American Board of Physical Therapy Specialties and serves as an Editorial Board Member for the Journal of Sport Rehabilitation. Amee’s clinical expertise is in the rehabilitation of patients with shoulder disorders. Her research focus is on the neuromuscular and biomechanical mechanisms of upper extremity musculoskeletal disorders and associated rehabilitation outcomes.
Timothy L. Uhl, PhD, PT, ATC, FNATA is an associate professor and co-director of the Musculoskeletal Laboratory in the Department of Rehabilitation Sciences at the University of Kentucky, Lexington, KY, USA. He received his PT degree in 1985 from the University of Kentucky, his masters’ in kinesiology from the University of Michigan in 1992 and his doctorate from the University of Virginia in 1998. His research focuses on shoulder rehabilitation outcomes and exercise progressions.