G Model JSAMS-1239; No. of Pages 6 ARTICLE IN PRESS Journal of Science and Medicine in Sport xxx (2015) xxx–xxx Contents lists available at ScienceDirect Journal of Science and Medicine in Sport journal homepage: www.elsevier.com/locate/jsams Original research Does load influence shoulder muscle recruitment patterns during scapular plane abduction? Darren Reed a,∗ , Ian Cathers a , Mark Halaki b , Karen A. Ginn a a b Discipline of Biomedical Science, School of Medical Sciences, Sydney Medical School, The University of Sydney, Australia Discipline of Exercise and Sport Science, Faculty of Health Sciences, The University of Sydney, Australia a r t i c l e i n f o Article history: Received 27 July 2015 Received in revised form 12 October 2015 Accepted 29 October 2015 Available online xxx Keywords: Shoulder Abduction Muscle activation Electromyography a b s t r a c t Objectives: Load is used to increasingly challenge muscle function and has been shown to increase muscle activity levels with no change in activation patterns during shoulder flexion, extension, adduction and rotation. However, the effect of load during shoulder abduction, a movement commonly used in assessment of shoulder dysfunction and to improve shoulder function, has not been comprehensively examined. Therefore, the purpose of this study was to determine if load influences shoulder muscle activation patterns and levels during scapular plane abduction in normal subjects. Design: Experimental study. Methods: Fourteen volunteers performed shoulder abduction in the scapular plane at 25%, 50% and 75% of maximum load. Eight shoulder muscles were investigated using a combination of indwelling and surface electromyographic recordings: middle deltoid, infraspinatus, subscapularis, supraspinatus, serratus anterior, upper and lower trapezius and rhomboid major. Results: All muscles tested showed increasing average muscle activation levels with increasing load and strong correlations in the activation patterns between loads. Conclusions: Increasing shoulder abduction load not only increases activity in middle deltoid but also in the rotator cuff (infraspinatus, subscapularis, supraspinatus) and axioscapular (serratus anterior, upper and lower trapezius, rhomboid major) muscles. The functional stabilising role of both the rotator cuff and axioscapular muscles is considered an important contribution to the increased activation levels in these muscle groups as they function to counterbalance potential translation forces produced by other muscles during shoulder abduction. The activation patterns of all shoulder muscle groups during abduction can be trained at low load and progressively challenged with increasing load. © 2015 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved. 1. Introduction Increasing load is commonly used in shoulder rehabilitation or gym based exercise programs to progressively challenge muscles with the aim of improving strength and muscle function.1,2 Electromyography (EMG) has been used to confirm muscle activation levels and patterns during rehabilitation exercises and it has been suggested that exercises producing low muscle activation levels be used early in rehabilitation programs3 while higher activation levels are described as more demanding and better suited to later in rehabilitation programs.4,5 Previous EMG studies have shown that normal shoulder muscle activation levels increase not only in the torque producing muscles but also in the rotator cuff and axioscapular muscles with increased load during dynamic shoulder ∗ Corresponding author. E-mail address: darren.reed@sydney.edu.au (D. Reed). flexion,6 extension,6 rotation7,8 and isometric adduction.9 Furthermore, in these studies shoulder muscle activation patterns did not change with increasing load with the same shoulder muscles recruited at low load also recruited at medium and high load. This implies that the normal recruitment pattern of muscles involved in moving and stabilising the humerus and scapula during shoulder movements can be established at low load and as load increases, all increase their activity. Scapular plane abduction has been described as the most functional plane of shoulder abduction2,10 and is a commonly recommended exercise used in rehabilitation and exercise programs to improve function at the shoulder.4,5 Although shoulder muscle recruitment patterns and levels have been investigated in previous studies during scapular plane abduction at low load1,4,11 and high load12 significant methodological considerations such as differences in the EMG normalisation process, makes comparison between these studies at different loads invalid. Two previous EMG studies have concurrently investigated the effects of increasing http://dx.doi.org/10.1016/j.jsams.2015.10.007 1440-2440/© 2015 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved. Please cite this article in press as: Reed D, et al. Does load influence shoulder muscle recruitment patterns during scapular plane abduction? J Sci Med Sport (2015), http://dx.doi.org/10.1016/j.jsams.2015.10.007 G Model JSAMS-1239; No. of Pages 6 ARTICLE IN PRESS D. Reed et al. / Journal of Science and Medicine in Sport xxx (2015) xxx–xxx 2 load during scapular plane abduction; however, direct comparison between muscle activation at different loads is still problematic.2,13 One of these studies only investigated inner range abduction (0◦ to 90◦ )13 and neither study included load as a factor in the statistical analysis so that significant differences between muscle activation levels at different loads cannot be confirmed.2,13 Additionally while middle deltoid and rotator cuff muscles were investigated in both studies, the only axioscapular muscle investigated was upper trapezius and only in the 0–90◦ abduction range.13 As no single EMG study has comprehensively investigated the effect of load on normal shoulder muscle activation levels and patterns during scapular plane abduction, it is still not known if increasing load during abduction systematically increases activation levels with no change in activation patterns in all shoulder muscle groups. Therefore, the aim of this experiment was to quantify and compare activation levels and recruitment patterns of middle deltoid (abduction torque producing muscle), supraspinatus, infraspinatus and subscapularis (rotator cuff muscles) and serratus anterior, upper and lower trapezius and rhomboid major (axioscapular muscles) in normal subjects through full range scapular plane abduction at low, medium and high loads. 2. Material and methods The shoulder of the arm used for writing of fourteen asymptomatic subjects (5 female and 9 male) aged between 18 and 49 years (mean age 22.5 years) was investigated in this study. Participants had no history of shoulder pain, no pain on maximally resisted rotation tests and demonstrated full normal range of shoulder abduction (180◦ ) with normal scapulohumeral rhythm (assessed visually by an experienced physiotherapist). The study was approved by the Human Research Ethics Committee of the University of Sydney and all subjects gave written informed consent before participating. A power analysis using G power software14 was performed to calculate the required sample size. Mean activity levels recorded from middle deltoid (38 ± 11%MVC) and supraspinatus (39 ± 11%MVC) in a previous EMG study investigating shoulder abduction11 were chosen for this analysis as the muscles most responsible for producing shoulder abduction torque. With power set at 0.80, significance level ˛ = 0.05, a mean detectable difference of 6%MVC and a correlation value of 0.80, a sample size of 13 (middle deltoid data) and 14 (supraspinatus data) subjects was required. Consequently a sample size of 14 subjects was chosen for this current study. Following subject familiarisation with the exercise protocol, pairs of silver/silver chloride surface electrodes (Red Dot, 2258, 3M) were placed over middle deltoid and upper trapezius15 at an inter electrode distance of 20 mm and impedance <5 k. Bipolar intramuscular electrodes16 were used to record activity from the remaining muscles i.e. deep muscles inaccessible to surface electrodes (supraspinatus, subscapularis, rhomboid major), muscles where crosstalk (infraspinatus17 ) and geometric displacement (serratus anterior18 ) have been shown to significantly affect surface electrode recordings and thin muscles (lower trapezius) where underlying muscles could produce crosstalk. The intramuscular electrode insertion sites were prepared with an anaesthetic gel (Xylocaine 2% jelly, AstraZeneca Pty Ltd, NSW, Australia), an antiseptic solution (Betadine, Faulding Healthcare Pty Ltd, Virginia, Australia) and cleaned with alcohol. A sterile insertion technique using a 23 ga hypodermic needle as a cannula was used to place indwelling electrodes. The placement of electrodes in all muscles, except for subscapularis, were according to the recommendations of Geiringer.19 A single bipolar electrode was placed in the midsection of subscapularis using the method described by Kadaba et al.20 Due to the thin nature of lower trapezius and close proximity of the underlying rhomboid major, insertion of the electrodes into these muscles was guided and confirmed by a digital ultrasonic diagnostic imaging system (Mindray, DP-9900). Correct placement of the other intramuscular electrodes was confirmed by visual inspection of the raw EMG signals during submaximal contractions expected to produce moderate activity in the target muscle with low activity in adjacent muscles.15 A surface ground electrode (Universal Electrosurgical Pad, 9160F, 3M) was placed over the spine of the scapula on the contralateral shoulder. The EMG signals were amplified and filtered (Iso-DAM 8 amplifiers, World Precision Instruments, gain = 100 or 1000 depending on the signal voltage as to not saturate the amplifier and provide good digital resolution, bandpass between 10 Hz and 1 kHz, Common Mode Rejection Ratio:100 dB at 50 Hz) before transferring to a personal computer with a 16 bit analog to digital converter (1401, Cambridge Electronics Design) at a sampling rate of 2564 Hz using Spike2 software (version 4.00, Cambridge Electronics Design). Before application/insertion of the electrodes subjects were trained to abduct the arm from the side through full range of abduction in the scapular plane leading with the thumb. Feet were comfortably spaced apart and the opposite hand rested on the adjacent hip to limit compensatory trunk movements. Speed was standardised to a count of 3 s in the concentric phase, a second at full range abduction and 3 s in the eccentric phase of motion. Tape markings on the floor were a guide to indicate the scapular plane of movement and an examiner standing on this line provided an additional visual target for the subject. Using dumbbell weights, the maximum load (100% load) able to be lifted in one repetition with normal scapulohumeral rhythm and no compensatory trunk movement was determined for each subject. A minimum rest interval of 30 s was given between attempts and a maximum of five attempts were required to determine the 100% load in this cohort. Following electrode placement and signal verification, resting EMG activity was recorded for each muscle. Five standardised maximum isometric shoulder normalisation tests15,21 were performed in sitting, three times each in random order with a 30 s break between repetitions and 2 min between tests. These included: resisted abduction at 90◦ abduction with humerus externally rotated; resisted extension in 30◦ abduction; resisted horizontal adduction at 90◦ flexion; resisted flexion in 125◦ flexion; resisted internal rotation at 90◦ abduction. These tests have a high likelihood of generating maximum activity in the shoulder muscles tested.15,21 Abduction was performed in the scapular plane while holding a dumbbell weight corresponding to 25%, 50% and 75% of maximum abduction load. Two full repetitions of shoulder abduction were completed at each load. Different load conditions were performed in random order with a 30 s break between each load condition. Synchronisation of the EMG signal with movement was achieved by a draw-wire sensor (Micro-Epsilon, WPS-1000-MK46P10, Germany), attached to the wrist of the arm being tested.6 If compensatory trunk or scapular movements occurred, or timing varied, the test was repeated. EMG signals were high pass filtered (10 Hz, zero lag 8th order Butterworth), rectified then low pass filtered (5 Hz, zero lag 8th order Butterworth) using Matlab 7.1 (The Mathworks). The maximum value obtained during the normalisation tests for each muscle was used to normalise EMG recordings during shoulder abduction. The signals were time normalised over the period of the combined concentric and eccentric phases of movement (0–100% representing the duration of movement). Group mean data (±SD) for each muscle was generated from the averages of the two trials at each load. Three out of 672 signals (14 subjects × 3 loads × 8 muscles × 2 trials) or less than 1% of data was eliminated due to electrode Please cite this article in press as: Reed D, et al. Does load influence shoulder muscle recruitment patterns during scapular plane abduction? J Sci Med Sport (2015), http://dx.doi.org/10.1016/j.jsams.2015.10.007 G Model ARTICLE IN PRESS JSAMS-1239; No. of Pages 6 D. Reed et al. / Journal of Science and Medicine in Sport xxx (2015) xxx–xxx 80 25% load 50% load 75% load ‡ ‡ ‡ EMG (% MVC) 70 ‡ ‡ ‡ 60 50 3 * * * * * ‡ ‡ 40 30 20 10 0 middle deltoid supraspinatus infraspinatus subscapularis upper trapezius serr atus anterior lower trapezius rhomboid major MUSCLES Fig. 1. Average (±SD) normalised EMG activation levels (%MVC) of the eight muscles tested during scapular plane shoulder abduction at 25%, 50% and 75% loads. ‡ Indicates significantly greater activation levels at 75% load than 25% load. * Indicates significantly greater activation levels at 50% load than 25% load. failure in subscapularis in one subject, serratus anterior in another and rhomboid major in another. A two factor repeated measures ANOVA (Statistica, version 7.1, Statsoft) was performed to compare the activation levels of the eight muscles examined across the three loads (25%, 50% and 75% of maximum load). Tukey post hoc analysis was used to identify specific differences when significant ANOVA results were obtained. Statistical significance was set at p < 0.05. Pearson’s correlation analysis was conducted between the time normalised group mean EMG signals from each muscle at different loads to determine the consistency of muscle activation patterns between 25/50%, 50/75% and 25/75% loads and between muscles. Correlation strengths were defined as “weak” for 0.1 < r < 0.3, “medium” 0.3 < r < 0.5 and “strong” 0.5 < r < 1.0.22 3. Results The average normalised muscle activation levels of the eight shoulder muscles examined during abduction performed in the scapular plane at 25%, 50% and 75% maximum load are shown in Fig. 1. Time normalised and averaged EMG muscle activation patterns during the concentric and eccentric phases of full range shoulder abduction in the scapular plane at 25%, 50% and 75% maximum load are illustrated in Fig. 2. The lowest correlation coefficient value between 25% and 50%, 50% and 75%, and 25% and 75% loads for each muscle is reported, with a strong correlation (r ≥ 0.65, p < 0.05) indicating a similar pattern of activation between loads for all muscles tested. There were significant ANOVA main effects for load (F2,26 = 87.4, p < 0.01), muscles (F7,91 = 4.2, p < 0.01) and significant interaction between load and muscles (F14,182 = 3.6, p < 0.01). Tukey post hoc testing revealed that significantly greater muscle activity occurred at 50% than at 25% load and at 75% than at 50% load (p < 0.01) and that there was a significant increase in activity levels with increasing load for all muscles (p < 0.01). To illustrate the interaction effects, comparison of average activation levels between muscles at the low, medium and high loads are shown in Fig. 3. Muscles are ordered by decreasing level of activity during shoulder abduction and grouped by boxes indicating no significant differences in activity between muscles within a box and with associated p-values from Tukey post hoc tests. There were significantly different activity levels between muscles in different boxes (p < 0.05). Correlation analysis between muscle activation patterns indicated: • the pattern of activation of middle deltoid was similar to infraspinatus and subscapularis across all loads with a strong correlation (r ≥ 0.67, p < 0.05) and to supraspinatus with a medium correlation (0.47 ≥ r ≥ 0.42, p < 0.05). Middle deltoid activity pattern had a strong correlation to the pattern of all axioscapular muscles investigated (r ≥ 0.59, p < 0.05). • the pattern of activation of all rotator cuff muscles was similar with a strong correlation (r ≥ 0.75, p < 0.05). Infraspinatus and subscapularis activity patterns had a strong correlation with the pattern of all axioscapular muscles investigated (r ≥ 0.57, p < 0.05) and supraspinatus had a medium or strong correlation with the axioscapular muscles (r ≥ 0.45, p < 0.05). • the pattern of activation of all axioscapular muscles investigated was similar with a strong correlation (r ≥ 0.67, p < 0.05). 4. Discussion The results of this study examining shoulder abduction in the scapular plane indicate that as load increases, average activation levels also increase systematically in all muscles tested. This includes the torque producing muscle (middle deltoid), rotator cuff muscles (supraspinatus, infraspinatus and subscapularis) and axioscapular muscles (upper trapezius, lower trapezius, serratus anterior and rhomboid major). The systematic increase in all muscles through full range abduction found in this current study would suggest that shoulder muscle recruitment during abduction, does not follow the ‘law of minimal activation’ which states that ‘the muscles with least synergistic activity will be recruited first and then as load increases other muscles are recruited’.23 Rather these results suggest a ‘law of proportional activation’, where the complex coordinated muscle activation pattern required to produce shoulder abduction in the scapular plane is established at low load and maintained as load increases. This would imply that normal muscle activation patterns during abduction can be trained at low load and then progressively challenged by adding resistance to the exercise through part or full range abduction. This is consistent with previous shoulder EMG research investigating normal muscle activation during shoulder adduction,9 flexion,6 extension,6 and Please cite this article in press as: Reed D, et al. Does load influence shoulder muscle recruitment patterns during scapular plane abduction? J Sci Med Sport (2015), http://dx.doi.org/10.1016/j.jsams.2015.10.007 G Model JSAMS-1239; No. of Pages 6 4 ARTICLE IN PRESS D. Reed et al. / Journal of Science and Medicine in Sport xxx (2015) xxx–xxx Fig. 2. Time normalised and averaged EMG muscle activation patterns of the eight muscles tested during shoulder abduction in the scapular plane at 25%, 50% and 75% loads. Time of 0% cycle represents start of movement and 100% cycle represents return to the starting position. Draw wire sensor trace, time normalised to maximum voltage is included as a final graph. r = lowest correlation value between 25/50%, 50/75% and 25/75% loads for each muscle. rotation7,8 which has shown systematic increases in middle deltoid, rotator cuff and axioscapular muscle activity with increasing load. These results also support the conclusions of previous research which have reported increasing muscle activity trends in the rotator cuff and middle deltoid with increasing load during scapular plane abduction from 0 to 90◦ .2,13 However, in the range greater than 90◦ abduction, the systematic increases in activation levels in the current study do not concur with the only previous study investigating the effect of load during abduction in this range, where inconsistent results were reported.2 The results of the current study demonstrate that as load increases during shoulder abduction the main abduction torque producing muscle (middle deltoid) increases its activation levels to produce movement of the arm. As middle deltoid activity increases during abduction, the superior translatory forces on the humerus24,25 would also increase, resulting in greater potential for impingement of subacromial structures between the humeral head and the coracoacromial arch. A subsequent increase in activity in parts of the rotator cuff able to prevent this superior translation (e.g. mid to lower sections of infraspinatus and subscapularis) would be expected.24,26 The results from this current study provide strong evidence to support this interaction between middle deltoid and both infraspinatus and subscapularis. Activation levels in infraspinatus and subscapularis increased systematically with increasing middle deltoid activity. In addition, there was a strong correlation between middle deltoid and both infraspinatus and subscapularis at all loads, indicating a similar pattern of activation between these muscles. Activation patterns in infraspinatus and subscapularis were also strongly correlated with that recorded in supraspinatus supporting the belief that, as part of the rotator cuff, supraspinatus is contributing to dynamic stability at the shoulder by providing a medial stabilising force on the humeral head during abduction.24,26 Although activity in infraspinatus and subscapularis was strongly correlated and highly likely to be activating with a common stabilising function, infraspinatus was activated at higher levels than subscapularis during abduction at all loads tested (Fig. 3). This may reflect the additional role of infraspinatus to externally rotate the humerus to prevent the greater tubercle from impacting on the acromion during the abduction movement. Similarly the greater activation levels in supraspinatus, compared with that recorded from subscapularis, in this study may reflect its additional role of producing abduction torque (Fig. 3). Biomechanical studies have suggested that supraspinatus has a more favourable abduction moment arm than middle deltoid in the early stages of shoulder abduction24 and therefore, is a more effective abductor than middle deltoid in this range of movement.27 The results of the current study support the above hypothesis, Please cite this article in press as: Reed D, et al. Does load influence shoulder muscle recruitment patterns during scapular plane abduction? J Sci Med Sport (2015), http://dx.doi.org/10.1016/j.jsams.2015.10.007 G Model JSAMS-1239; No. of Pages 6 ARTICLE IN PRESS D. Reed et al. / Journal of Science and Medicine in Sport xxx (2015) xxx–xxx 5 Fig. 3. Muscles ordered by level of activity during scapular plane abduction at 25%, 50% and 75% load and grouped by boxes indicating no significant differences between muscles within a box and with associated p-values from Tukey post hoc tests. Significant differences are indicated for muscles in different boxes (p < 0.05). although it has been clearly shown that supraspinatus does not initiate abduction.28 Supraspinatus activation levels were twice that of middle deltoid at the start of the abduction movement (Fig. 2), peak activation levels in supraspinatus occurred earlier in range than that of middle deltoid (Fig. 2) and there was only a moderate correlation between the activity patterns in these two muscles. Full range abduction at the shoulder depends not only on humeral elevation but also on the synchronised upward rotation of the scapula,25 with the axioscapular muscles (serratus anterior, upper trapezius and lower trapezius) acting as the torque producing muscles for this rotation.10,25 However, as increased load on the arm does not directly increase load on the scapula, the torque producing role of the axioscapular muscles does not fully explain their increase in activation levels during abduction with load. The axioscapular muscles must also stabilise the scapula to provide a fixed attachment site for the scapulohumeral muscles (middle deltoid and the rotator cuff) to enable them to produce glenohumeral joint torque and stability, rather than their origin and insertion being reversed and potentially producing lateral movement of the scapula.6,27,29 A strong correlation between the activation patterns of the axioscapular and scapulohumeral muscles suggests that as middle deltoid, infraspinatus and subscapularis increase their activation levels with increased load, they exert an increased lateral pull on the scapula necessitating a corresponding increase in activation of axioscapular muscles to counterbalance this pull. This argument is further strengthened by the finding that, similar to other axioscapular muscles, rhomboid major was activated at moderate, increasing average levels as abduction load increased (20–44%MVC). As rhomboid major is a downward rotator of the scapula30 it cannot be functioning to upwardly rotate the scapula during the shoulder abduction task under investigation. The strong correlation between the pattern of activation in rhomboid major and all other axioscapular muscles and scapulohumeral muscles tested in this current study indicates that it is providing a stabilising force to prevent lateral movement of the scapula. 5. Conclusion The results of this study show that in asymptomatic subjects, increasing load during scapular plane abduction increases activation levels in the main abduction torque producing muscle (middle deltoid) and consequently in the rotator cuff muscles (infraspinatus, subscapularis, supraspinatus) and axioscapular muscles (serratus anterior, upper and lower trapezius and rhomboid major). This increase in activation levels is systematic and indicates that the pattern of individual muscle activation does not change as load increases. The shoulder muscle recruitment pattern at low loads is similar to that at high loads. Practical implications • Training with increasing abduction load will result in strength increases in rotator cuff and axioscapular muscles as well as deltoid with potential fatigue implications in any of these muscles at higher loads. • The strength increases in the rotator cuff and axioscapular muscles which occur with increasing abduction load are predominantly as result of their role as dynamic stabilisers: o increased deltoid activity with greater abduction load will result in increased translational forces on the humeral head requiring greater rotator cuff activity as they function to counterbalance these destabilising forces, o increased deltoid and rotator cuff activity will result in increased translation forces on the scapula requiring increased Please cite this article in press as: Reed D, et al. Does load influence shoulder muscle recruitment patterns during scapular plane abduction? J Sci Med Sport (2015), http://dx.doi.org/10.1016/j.jsams.2015.10.007 G Model JSAMS-1239; No. of Pages 6 ARTICLE IN PRESS D. Reed et al. / Journal of Science and Medicine in Sport xxx (2015) xxx–xxx 6 axioscapular muscle activity to counterbalance these destabilising forces. • The activation patterns of all shoulder muscle groups during abduction can be trained at low load and progressively challenged with increasing load. Institutional review board Ethics approval was granted by The University of Sydney Human Ethics Committee with approval number 07-2007/10/10122. Acknowledgement No external funding was received for this study. References 1. McCann PD, Wootten ME, Kadaba MP et al. A kinematic and electromyographic study of shoulder rehabilitation exercises. Clin Orthop 1993;(288):179–188. 2. Alpert SW, Pink MM, Jobe FW et al. Electromyographic analysis of deltoid and rotator cuff function under varying loads and speeds. J Shoulder Elbow Surg 2000; 9(1):47–58. 3. 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