Introduction
Healthy shoulder function is a compromise between mobility and stability. Given the shoulder joint's mobility, stability is based mainly on active muscle control, which requires a finely tuned activation balance between the serratus anterior and the upper and lower trapezius (24). Musculoskeletal pain in the neck and shoulder, which is associated with restricted range of motion and loss of strength (11), is one of the most common conditions treated by physical therapists. Similarly shoulder impingement is common in people who participate in overhead sports (4,8). The role of the scapula in the pathogenesis of these types of shoulder disorders has received much attention. Excess activation of the upper trapezius, combined with decreased control of the lower trapezius and the serratus anterior, is proposed as contributing to shoulder pain (17). Supporting this, patients with shoulder disorders show an altered muscle activation balance toward increased upper trapezius activation and reduced serratus anterior activation (13). Thus, specific training of the lower trapezius and serratus anterior although minimizing activation of the overloaded upper trapezius requires detailed knowledge of exercise-specific activation of the scapular muscles.
A high level of muscle activation—that is, at high training intensity—is essential to induce gains in muscle strength, and high-intensity strength training of the scapular muscles has previously proven effective in rehabilitation of trapezius myalgia (3). Training intensities of 60% of maximal voluntary force and higher generally are recommended to obtain increased strength (22). Although Cools et al. showed that certain exercises at low intensities predominantly activate the lower trapezius and serratus anterior over the upper trapezius (7), it is unknown whether this finding holds true for high-intensity exercises necessary to build strength. Thus, more knowledge is needed about the specificity of muscle activity of scapular muscles during exercises both at low and high intensities.
This study determines if the activation pattern in scapular muscle changes during selected shoulder exercises when they are performed at low and high intensity. We compare surface electromyographic (EMG) responses at low and high intensities (Borg 3 and 8) and determine activation difference and ratio between the respective muscles.
Methods
Experimental Approach to the Problem
The study was conducted over 2 separate days. On the first day, (practice) the subjects were familiarized with the exercises, and loadings for each exercise corresponding to an effort of level 3 and level 8 on the Borg CR10 scale for each exercise were found. Borg level 3 is characterized by the exertion from the exercise being “Very weak” and Borg level 8 by the exertion being “Very strong” (6). An increase in perceived exertion, as a function of relative load, is found to show a strong linear trend (1,21). The loadings found on the practice day were used on the second day for testing (Table 1). On the second day, 3 repetitions of each exercise were performed in a fixed order separated by 2-minute rest intervals to avoid fatigue. First all the exercises were performed at the predetermined Borg 3 load in the order described below, and then the subjects performed the exercises at the predetermined Borg 8 load. Immediately after each set of exercise, the Borg CR10 scale was used to rate the actual perceived loading during the exercise on the day of testing. Before both practice and testing, the meaning of the scale was carefully explained to each individual.
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Table 1: Values are expressed as mean (95% confidence interval).*†
Subjects
A group of 17 healthy women (age 29 ± 7.2 years, height 168 ± 6.3 cm, weight 62.7 ± 11.1 kg) were recruited on a voluntary basis. Exclusion criteria were a known history of disc prolapse, rheumatoid arthritis, or other serious musculoskeletal disorders. None of the recruited subjects met these exclusion criteria. All the subjects were informed about the purpose and content of the project and gave written informed consent to participate in the study, which conformed to The Declaration of Helsinki and was approved by the Local Ethical Committee (HC-2008-103).
Muscle Activation (Electromyography)
The EMG signal sampling and analysis EMG signals were recorded from the upper, middle and lower trapezius, and the serratus anterior. A bipolar surface EMG configuration (Neuroline 720-01-K, Medicotest A/S, Ølstykke, Denmark) and an interelectrode distance of 2 cm were used. The skin of the respective area was prepared by scrubbing gel (Acqua gel, Meditec, Parma, Italy). Before affixing the electrodes, it was checked whether the impedance was <10 kΩ. The procedure followed the SENIAM recommendations, which are available at www.seniam.org. The EMG electrodes were connected directly to small preamplifiers located near the recording site. The raw EMG signals were led through shielded wires to instrumental differentiation amplifiers, with a bandwidth of 10–500 Hz and a common mode rejection ratio better than 100 dB, sampled at 1,000 Hz using a 16 bit A/D converter (DAQ Card Al 16XE 50, National Instruments, Austin, TX, USA) and recorded on computer via a laboratory interface (CED 1401, Spike2 software, Cambridge Electronic Devices, Cambridge, United Kingdom). In the following analysis, all raw EMG signals obtained during maximal voluntary isometric contraction (MVCs) and during exercises were digitally filtered, consisting of (a) high pass filtering at 10 Hz and (b) a moving root mean square (RMS) filter of 500 milliseconds. For each individual muscle, peak RMS EMG of the 3 repetitions performed at each level was determined, and the average value of these 3 repetitions was then normalized to the maximum RMS EMG (1).
Maximal Voluntary Isometric Contraction
Before the exercises described below, isometric MVCs were performed according to standardized procedures (2) during shoulder abduction, prone shoulder flexion, prone shoulder abduction, and scapula protraction to induce a maximal EMG response of the respective muscles. Two isometric MVCs were performed for each muscle, and the trial with the overall highest EMG was used for the normalization of the peak EMGs in the training exercises. The subjects were instructed to gradually increase muscle contraction force toward maximum over a period of 2 seconds, sustain the MVC for 3 seconds, and then slowly release the force again. Strong verbal encouragement was given during all the trials.
Exercise Description
Choice of exercises is based on biomechanical principles and empirical experience for contribution of the upper trapezius contra lower trapezius and serratus anterior. (a) Shoulder press: The subject sits upright on the bench holding the dumbbells in front of the shoulders, and she then pushes the dumbbells straight up until the arms are straight (Figure 1A). Progression: Using heavier dumbbells. (b) One-arm row: The subject bends her torso forward to approximately 30° from horizontal with one knee on the bench and the other foot on the floor. The subject now pulls the dumbbell toward the ipsilateral lower rib, while the contralateral arm is maintained extended and supports the body on the bench (Figure 1B). Progression: Using heavier dumbbells. (c) Press-up: The subject sits erect on a training bench, feet on the floor with straight arms and the palms on the edge of the bench fingers pointing forward. She now lifts herself off the bench and then dips down just in front of the seat just moving the shoulder girdle (Figure 1C). Progression: placing weight plates on the thigh. (d) Prone abduction with external rotation: The subject lies on the chest with the arms pointing toward the floor, arms externally rotated. The shoulders are abducted with the thumbs pointing toward the ceiling until the upper arm is horizontal, while the elbows are in a static slightly flexed position (∼5°) during the entire range of motion (Figure 1D). Progression: Using heavier dumbbells. (e) Prone flexion: The subject lies on the chest with the arms pointing toward the floor, arms in neutral rotation. The shoulders are flexed with the thumbs pointing toward the ceiling until the upper arm is horizontal, while the elbows are in a static slightly flexed position (∼5°) during the entire range of motion (Figure 1E). Progression: Using heavier dumbbells. (f) Ring fallouts: The subject is placed on the knees with the hands in the gymnastic rings, which are suspended just above the ground level. She then lowers herself and pushes the rings forward allowing movement only to happen in the shoulder (Figure 1F). Progression: moving the knees backward in the setup phase. (g) Push-up plus: The subject starts from a push-up position on the hands and feet or knees, bracing the abdominals to keep the torso rigid. The subject now pushes the body as high as possible off the floor by protracting the scapulas (Figure 1G). Progression: moving from the knees to the feet and from there adding resistance by positioning plates of iron on the upper back.
Figure 1: The 7 training exercises used in this study. A) Shoulder press, B) one-arm row, C) press-up, D) prone abduction with external rotation, E) prone flexion, F) ring fallouts, and G) push-up plus.
Statistical Analyses
Using SAS statistical software (version 9.2) analysis of variance with repeated measures determined whether differences during the 7 exercises existed in the activation difference between the upper and lower trapezius, between the serratus anterior and the upper trapezius, between the upper and middle trapezius, and between the serratus anterior and the lower trapezius. Only preplanned analyses were performed.
A difference of ≥10% in the normalized EMG between the muscles was considered a clinically relevant difference. A priori power analysis showed that 16 participants in this paired design were sufficient to obtain a statistical power of 80% at a minimal relevant difference of 10% and a type 1 error probability of 5%, assuming an SD of 10% based on previous research in our laboratory (2). An alpha of <5% was considered statistically significant. Values are reported as means (SE) in the figures and means (95% confidence intervals) in the tables.
Results
Table 1 shows the level of muscle activation (normalized EMG) and loadings used during the different exercises. As shown by the first column of Table 1, the target exertion level was met to an acceptable extent on the day of testing. Table 1 further shows that shoulder press, prone abduction, and prone flexion at Borg level 8 induced high levels of muscle activation (>60% of max EMG) in the upper trapezius. One-arm row and prone flexion at Borg level 8 and prone abduction at Borg levels 3 and 8 induced high levels of muscle activation in the middle trapezius. Prone abduction at Borg 8 and prone flexion at Borg levels 3 and 8 induced high levels of muscle activation in the lower trapezius. Further, shoulder press at Borg levels 3 and 8 and push-up plus at Borg level 8 induced high levels of muscle activation in the serratus anterior.
Table 2 and Figures 2–5 show the muscle activation difference between the serratus anterior and the upper, middle and lower compartments of the trapezius. Table 2 also shows muscle activation ratios. Several of the exercises—push-up plus, shoulder press, and press-up at Borg levels 3 and 8—predominantly activated the serratus anterior over the upper trapezius (activation difference [Δ] 18–45%) (Figure 2). Likewise, several of the investigated exercises—press-up, prone flexion, one-arm row, and prone abduction at Borg level 3 and press-up, push-up plus and one-arm row at Borg 8—predominantly activated the lower trapezius over the upper trapezius (Δ13–30%) (Figure 3). The middle trapezius was activated over the upper trapezius by one-arm row and prone abduction (Δ21–30%) (Figure 4). Several exercises predominantly activated either the serratus anterior or the lower trapezius. Although shoulder press and push-up plus activated the serratus anterior over the lower trapezius (Δ22–33%), the opposite was true for prone flexion, one-arm row and prone abduction (Δ16–54%) (Figure 5). Only the press-up and push-up plus activated both the lower trapezius and the serratus anterior over the upper trapezius.
Table 2: Activation difference and activation ratios for upper trapezius—middle trapezius, upper trapezius—lower trapezius, upper trapezius—serratus anterior and lower trapezius—serratus anterior.*†
Figure 2: Difference in normalized electromyography (EMG) between serratus anterior and upper trapezius during the different exercises and intensities. *Indicates 10% significantly different activation between muscles.
Figure 3: Difference in normalized electromyography (EMG) between lower trapezius and upper trapezius during the different exercises and intensities. *Indicates 10% significantly different activation between muscles.
Figure 4: Difference in normalized electromyography (EMG) between middle trapezius and upper trapezius during the different exercises and intensities. *Indicates 10% significantly different activation between muscles.
Figure 5: Difference in normalized electromyography (EMG) between serratus anterior and lower trapezius during the different exercises and intensities. *Indicates 10% significantly different activation between muscles.
Discussion
Our study is the first to demonstrate predominant activation of specific parts of the scapular musculature at both low and high intensities. This has implications for rehabilitation, injury prevention, and performance training. Whether the aim is strengthening specific tissues or improving neural activation, higher training intensities, for example, Borg 8—provide a stronger stimulus for the body to adapt. Five of the selected exercises produced activation of at least 60% for one of the targeted muscles and can formally be classified as strengthening exercises (22,23). Furthermore, our study shows that specific scapular muscle activation difference between exercises can be determined based on EMG analysis. Several of the investigated exercises predominantly activate the serratus anterior or the lower trapezius, respectively, over the upper trapezius and may considered isolation exercises. Both prone flexion and prone abduction activated all 3 compartments of the trapezius >60% of max at Borg 8 and general compound exercises for the trapezius. The relevance of these findings is discussed below.
Proper serratus anterior function is important for normal shoulder function because it contributes to all components of normal 3-D scapular movements during humeral elevation, including upward rotation, posterior tilt and external rotation. There is general consensus that the middle and lower serratus anterior is the prime mover of the scapula on the thorax (20). Because the upper trapezius is often overactivated relative to the lower part and serratus anterior (13,14,19), physical therapists recommend unloading the upper trapezius (7,14,19). Thus, improvement in the function of the serratus anterior, middle-, or lower trapezius through rehabilitation may help alleviate pain and dysfunction.
Previous studies have investigated serratus anterior activation during different exercises (9,10,12,16,18). Although these studies recommend exercises inducing high serratus anterior activation, they do not consider the simultaneous impact of these exercises on the upper trapezius. In other words, these studies did not account for the activation difference between the serratus anterior and the upper trapezius. Only few previous studies have investigated the activation difference between the serratus anterior and the upper trapezius during exercises (5,7,16), and none of these investigated activation difference during high-intensity exercise. Because strengthening specific muscles requires a high level of muscle activation, their proposed exercises may not effectively strengthen the serratus anterior.
Our study is the first to evaluate activation difference of the scapular muscles during both low- and high-intensity exercises. Importantly, we show that the push-up plus exercise performed at high intensity strongly activates the serratus anterior while maintaining a low level of upper trapezius activity. Also, the muscle activation ratio between upper trapezius and serratus anterior is lower during high-intensity push-up plus (0.34) than when performed at a low intensity (0.44). An earlier study found that when performing the standard push-up, push-up on knees, and wall push-up, serratus activity is greater when full scapular protraction occurs after the elbows fully extend, that is, push-up plus (16). Moreover, in their study, serratus anterior activity was lowest in the wall push-up plus, exhibited moderate activity during the push-up plus on knees and high to very high activity during the standard push-up plus and push-up plus with the feet elevated (9,16). However, we showed that although the shoulder press and press-up also had a serratus dominant activation, it also activates the upper trapezius to a high extent. Further, the shoulder press is often clinically problematic because of impingement. Although, the press-up at both low and high intensities has a serratus anterior dominant activation difference over the upper trapezius, the level of serratus anterior activation is only moderate and may not induce effective strength gains. Based on our findings, the push-up plus superiorly activates the serratus anterior over the upper trapezius at intensities sufficient to strengthen the serratus anterior.
The lower trapezius contributes to posterior tilt and external rotation of the scapula during humeral elevation (15), which decreases subacromial impingement risk (14). Overall, the trapezius is more active during abduction as compared with during flexion, consistent with less scapular internal rotation present in scapular plane abduction as compared with flexion (20). We show that the press-up most efficiently activated the lower trapezius over the upper trapezius, as also shown by the low upper trapezius/lower trapezius ratio. However, the levels of lower trapezius activation are only moderate, indicating that despite the selective activation, this exercise may not induce strength gains. In the prone flexion, the activation difference is dependent on exercise intensity; only at Borg 3, is the activation difference shifted toward dominance of the lower trapezius. Performing this exercise at Borg 8 activates all 3 parts of the trapezius to a high extent. Although one-arm row and prone abduction at Borg level 3 and push-up plus and one-arm row at Borg 8 also predominantly activated the lower trapezius over the upper trapezius, performing these exercises at the given intensity levels may not induce strength gains because levels of muscle activation were only moderate.
For selective activation of the lower trapezius, the press-up superiorly activates this muscle over the upper trapezius although intensity might not be sufficient to induce strength gains. Our findings also show that for prone abduction at Borg level 3, the lower trapezius is highly activated with moderate activity in the upper trapezius.
The middle part of the trapezius—together with the rhomboids—primarily adducts the scapula and is only to a lesser extent involved in external rotation. Although the middle trapezius in a traditional sense is neither agonist nor antagonist to the upper trapezius, a proper level of activation of this muscle is important (7,14,25).
Our analysis of activation differences between the middle and upper trapezius shows that one-arm row and prone abduction predominantly activate the middle trapezius over the upper trapezius at both Borg 3 and Borg 8. Because the activation difference between the 2 intensities in the 1-arm row are not significantly different, based on the upper trapezius/middle trapezius ratio, low intensity is preferable for the selective strengthening of the middle trapezius.
A strong synergism between the serratus anterior and lower trapezius is commonly thought to exist. Although both the serratus anterior and the lower trapezius perform upward rotation of the scapula, based on our data, a total synergism between the lower trapezius and serratus anterior is not evident, because these muscles showed significantly different levels of activation during specific exercises. Although shoulder press and push-up plus activate the serratus anterior over the lower trapezius, the opposite is true for prone flexion, one-arm row, and prone abduction. The prone abduction with external rotation exercise frequently is promoted for optimal shoulder rehabilitation (7,18). Moseley et al. included this exercise in their selection for glenohumeral and scapulothoracic muscle strengthening programs. Various authors have suggested that shoulder abnormalities and abnormal scapular motions may be linked to either global weakness of the scapulothoracic muscles or to scapular muscular imbalance rather than absolute strength deficits (7,8). Our results show that when the prone abduction is performed at high intensity, all parts of the trapezius may be strengthened, and therefore, this exercise performed at high intensity cannot be used for the selective strengthening of any specific trapezius compartment.
Our findings show that the shoulder press and push-up plus superiorly activate the serratus anterior over the lower trapezius at intensities efficient to strengthen the serratus anterior with only moderate lower trapezius activation. On the other hand, the prone flexion and prone abduction superiorly activate the lower trapezius over the serratus anterior at intensities efficient to strengthen the lower trapezius with only moderate serratus anterior activation.
Practical Applications
Several of the investigated exercises both at low and high intensities predominantly activate the serratus anterior and lower and middle trapezius, respectively, over the upper trapezius. Of the examined exercises, only the press-up and push-up plus activated both the lower trapezius and the serratus anterior over the upper trapezius. From a practical point of view, these exercises can be performed with body weight or by adding an external resistance, for example, an elastic resistance band or added resistance at the shoulder by a training partner. The Borg CR10 scale is easy to use and understand and thereby allows for a rough determination of exercise intensity during exercises where the exact repetition maximum is difficult to determine.
Study Limitations
Extrapolation of our results to patients with shoulder injury should be done with caution. We cannot conclude if patients suffering from shoulder pain or local muscle imbalances will show a similar muscle activation difference performing the exercises we propose. We consider this study as a first step in the investigation of rehabilitation exercises for the restoration of trapezius muscle balance, where the use of subjects without serious shoulder disorders must be recognized as a clinical limitation.
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