Musculoskeletal factors of scapular dysfunction include continuous abnormal posture (30), repetitive movements deviating from normal scapulohumeral rhythm (22) or glenohumeral, and scapulothoracic muscle imbalance (3,9). In particular, scapular winging, which is a subtype of scapular dysfunction has 2 common causes: (a) denervation of the long thoracic nerve causing difficulty in active shoulder flexion above 120° or (b) weakness of the serratus anterior (SA) muscle in theory.
The SA, which maintains components of normal 3-dimensional scapular movements (18,24), is one of the most important factors for preventing winging and anterior tilt of the scapula (7,26). Serratus anterior abnormal muscle firing patterns caused by muscle weakness or fatigue are associated with painful shoulder conditions such as subacromial impingement and scapular winging (17,20). Therefore, many therapeutic exercise protocols for the SA activity have been investigated for prevention and rehabilitation of scapular dysfunction.
Standard push-up plus (SPP) shows the highest average SA activation as compared with other SA activation exercises and has been recommended to effectively elicit SA muscles (2,5,10,23). In addition, modifications to the SPP are commonly recommended, including the knee push-up plus (KPP), elbow push-up plus, and wall push-up plus (WPP). This is because these alternatives are believed to limit the amount of weight bearing during the exercise and are especially suggested in the earlier stage of rehabilitation programs, when patients might be unable to repetitively perform the SPP (19).
Previous researches have reported that pectoralis major (PM) activates with SA during active scapular exercises (6,11,12,14,28,34). People with scapular winging showed higher PM activation than those in the control group during push-up plus exercises (14). In addition, imbalanced PM and SA ratio can be disadvantageous for people with scapular winging because this high PM/SA ratio can be associated with shoulder joint pathology (28). Thus, it is important to investigate the PM/SA ratio during SA activation exercises.
The purposes of this study were to compare the PM/SA electromyographic (EMG) activity ratio, as well as the PM and SA EMG amplitudes between men with and without scapular winging during 3 push-up plus exercises (SPP, KPP, and WPP) and to determine which exercise induced the lowest PM/SA ratio in each group. Our first hypothesis was that subjects with scapular winging would demonstrate a greater PM activity and lower SA activity and higher PM/SA ratio during 3 push-up plus exercises compared with those without scapular winging. Second hypothesis was that the PM/SA ratio would be different among 3 push-up plus exercises.
Experimental Approach to the Problem
This study was designed to examine the differences between subjects with and without scapular winging in the PM/SA EMG activity ratio and the PM and SA EMG amplitudes during 3 push-up plus exercises and to determine which exercise induced the lowest PM/SA ratio in each group. To investigate this, we recruited a scapular winging group of 13 participants and a control group of 15 participants. This study used mixed-model analyses of variance (ANOVAs) with a between-subject factor (groups: scapular winging and control) and a within-subject factor (push-up plus type: SPP, KPP, and WPP).
A total of 30 male volunteers between the ages of 20 and 26 were recruited from university student population through phone calls or in person. Two subjects were excluded based on previous medical conditions identified by an exclusion questionnaire, resulting in a sample size of 28. Thirteen subjects had scapular winging, and 15 subjects were without scapular winging. Scapular winging was confirmed by measuring the distance between the thoracic wall and the inferior angle of the scapula using a scapulometer (interclass correlation coefficient: 0.97, 95% confidence interval: 0.87–0.99, standard error of the measurement: 0.1 cm). The distance equal to or greater than 2 cm was defined as scapular winging (34). The exclusion criteria were a history of shoulder pain or injury that considerably limited shoulder motion or led to gross instability of the shoulder during daily activities, signs and symptoms of long thoracic nerve damage, cervical pain, or a current complaint of numbness or tingling in the upper extremity. Additional exclusion criteria were a history of participation in overhead sports at a competitive level and upper-limb strength training for more than 5 h·wk−1 (11). Clinical orthopedic examination was conducted by an examiner, who has 2 years of clinical experience in the field of orthopedic physical therapy, after a 5-hour training session. Table 1 shows the demographic data of the subjects. The investigation was approved by the Institutional Review Board of Yonsei University Wonju, and written informed consent was obtained from each subject before participation.
Sample Size Estimation
To the best of our knowledge, there are no previous studies that have investigated this issue. Pilot testing was performed on 6 volunteers (3 with scapular winging, 3 without scapular winging) to determine the number of subjects required in this study. A power analysis based on the results of the pilot study was completed to achieve a significant α level (0.05), power (0.8), and effect size (0.9). The results of the power analysis showed that this study would require 6 subjects in each group.
Electromyographic Recording and Data Processing
Self-adhesive Ag/AgCl snap electrodes for surface EMG were placed over the PM and SA muscles. The electrodes for PM (sternal fiber) were attached on the chest wall horizontal from the arising muscle mass (∼2 cm out from the axillary fold) (4). The electrodes for SA were located just below the axillary area, at the level of the inferior tip of the scapula, and medial of the latissimus dorsi (4). Two electrodes were placed approximately 20 mm apart in the direction of the muscle fibers, and a ground electrode was placed over the ipsilateral clavicle. The skin was prepared before attaching the electrodes by shaving the site and cleaning with alcohol to reduce the skin impedance. Data were collected from the scapular winging side (scapular winging group) and the dominant side (control group). Surface EMG data were collected using a Noraxon TeleMyo 2400 system and analyzed using Noraxon MyoResearch 1.06 XP software (Noraxon USA Inc, Scottsdale, AZ, USA). The EMG signals were amplified and band-pass filtered (10 and 450 Hz) and notch-filtered (60, 120 Hz) before being digitally recorded at 1,000 Hz, and processed to the root mean square. To calculate the PM/SA ratio, the normalized PM amplitude was divided by the normalized SA amplitude.
Reference voluntary contractions (RVCs) were collected for normalizing the EMG data. Subjects raised their tested arm in the scapular plane with a 6.5-kg sandbag on their forearm until the shoulder was flexed at 90° (29). Subjects held this posture for 5 seconds without moving their center of mass to the nontested side. We collected the middle 3 seconds of the 5-second contraction for data analysis. A 1-minute rest was given to all participants between trials. The mean value of 3 trials for each muscle activity was taken as the RVCs. The EMG signals collected during push-up plus exercises were expressed as a percentage of the calculated root mean square of RVCs (%RVC).
Subjects were uniformly instructed by a single instructor on how to perform each exercise and were allowed to practice for approximately 20 minutes until the proper motion and timing were achieved. Three push-up plus exercises used in this study were modifications of exercises used by Ludewig et al. (19). The SPP is a standard push-up with the addition of full scapular protraction (the “plus”) after obtaining full elbow extension at the end of the usual push-up with feet together. The KPP was performed in the same way as the SPP, except that the knees shoulder-width apart was the distal point of contact with the ground rather than the feet. The WPP was performed in a standing position with the hands in contact with the wall and feet shoulder-width apart (Figure 1). The order of 3 push-up plus exercises was randomized using the random number generator in Microsoft Excel (Microsoft Corp., Redmond, WA, USA) to avoid systematic influences of fatigue and learning effects. All trials were completed in the standardized position with the hands shoulder-width apart, elbows fully extended, and 90° of shoulder flexion during the exercises. A bar was placed at the T4 level where the scapula was fully protracted. The neck, trunk, pelvis, and lower extremities were aligned in a straight line. The period of push-up plus exercises was divided as follows: (a) starting phase: protracting the scapula by translating the thorax posteriorly until the spinous process of the thoracic vertebra touched a target bar for 2 seconds, (b) holding phase: holding the position for 5 seconds, and (c) ending phase: returning to the starting position for 2 seconds. First, the author observed and determined whether the subject performed push-up plus exercises correctly. Trials during which the subject failed to maintain the standardized position and holding period were excluded in the data analysis. The duration of each exercise was controlled by a sound signal generated by a metronome. Participants performed 3 trials of each push-up plus exercise with 1-minute resting period between trials. The EMG signals were collected during the middle 3 seconds of the holding phase. The mean value of 3 trials of each push-up plus exercise was used for data analysis.
Mixed-model ANOVAs were used to determine the interaction effects for the ratio of PM and SA EMG activity and PM/SA EMG activity. The level of significance was set at p = 0.05. If a significant interaction was not revealed from a mixed-model ANOVA, the main effect for the group and push-up plus type was determined. Bonferroni's correction was used for post hoc tests if a significant main effect for push-up plus was observed (with α = 0.05/3 = 0.016). If a significant interaction was found, a pair-wise comparison with Bonferroni's correction (with α= 0.05/3 = 0.016) was used to determine the simple effect. All statistical analyses were performed using PASW Statistics 18 (SPSS Inc, Chicago, IL, USA).
For the normalized PM EMG activity, no significant group × push-up plus type interaction was found (p > 0.05). A significant main effect of the group was observed (p ≤ 0.05), but no significant main effect of the push-up plus type (p > 0.05) was found. The normalized PM EMG activity for subjects in the scapular winging group was significantly greater than for those in the control group (Figure 2). In the normalized SA EMG activity, no significant group × push-up plus type interaction was observed (p > 0.05). Significant main effects of the group (p ≤ 0.05) and push-up plus type (p ≤ 0.05) were found. The normalized SA EMG activity was significantly lower for subjects in the scapular winging group than for those in the control group (Figure 3). In addition, a post hoc comparison test revealed that the normalized SA EMG activity was significantly decreased in the order of SPP > KPP > WPP (p < 0.016) (Figure 4). For the PM/SA EMG activity ratio, a significant group × push-up plus type interaction was found (F [2.25] = 6.975, p ≤ 0.05), with the PM/SA EMG ratio significantly greater in the scapular winging group compared with the control group across all push-up plus exercises (p < 0.016) (Figure 5). In addition, the PM/SA EMG activity ratio for SPP was significantly lower compared with that in the KPP and WPP exercises.
Our results demonstrated that subjects with scapular winging showed significantly greater PM activity compared with those without scapular winging. This result is consistent with the finding of Kim et al. (14) who reported that PM activities are greater in a scapular winging group than that in a control group during push-up plus, although different normalization methods make direct comparison between the results of this study and previous studies difficult. This increased PM activity in the subjects with scapular winging during push-up plus exercises can be explained by characteristics of PM as a synergist and the reduced activation of the SA. Scapular protraction is occurring through clavicular protraction during the plus phase of the push-up plus exercise (21). In addition, anterior translation of the humeral head increases during initial to mid-phase of push-up plus exercise (19). Pectoralis major may help clavicular protraction and the anterior translation of the humerus during the scapular protraction, originating from the medial third of the clavicle, the lateral side of the sternum, the cartilages of the first 6 ribs, and the external abdominal oblique fascia, and inserting into the lateral lip of the bicipital groove of the humerus (13). Synergistic muscles that work together can influence each other through movement (1,27). Specifically, when push-up plus exercises are performed in the standardized position, less scapular protraction caused by reduced SA activity can give rise to increased PM activity for achieving the same range of motion by additional clavicular protraction and humeral translation. However, the excessive PM activation might cause several disadvantages such as a decreased volume of the subacromial space (32), increased compressive forces on the glenoid (16), and subacromial impingement (15,25).
Subjects with scapular winging showed significantly lower SA activation than those without scapular winging. Although direct comparison between the results of this study and previous study is difficult because of different normalizing methods, our findings are consistent with previous studies reporting reduced SA EMG activity in subjects with various scapular dysfunction, including throwers with glenohumeral instability (8), construction workers with shoulder impingement (17), and swimmers with shoulder pain (31). Because the scapula provides a stable base for glenohumeral movements, it seems reasonable to expect that normal pattern of glenohumeral rhythm may be affected if the position of the scapula is altered or muscles become weak or fatigued. Shoulder pathology may be linked to abnormal scapular motion and imbalanced muscle activity rather than global weakness of scapulothoracic muscles (17).
The PM/SA activity ratio for subjects in the scapular winging group was significantly higher than that for subjects in the control group. The PM/SA activity ratio in the control group was equal to or lesser than 1, whereas the PM/SA activity ratio in the scapular winging group was greater than 1. A high PM/SA indicated that the PM was highly activated, proportionately to the SA being minimally activated. Therefore, the results of this study confirm the presence of greater PM activity and lower SA activity in subjects with scapular winging compared with those without scapular winging. Selective SA activation without high PM activation is required to reduce possible glenohumeral and scapulothoracic joint dyskinesia. Thus, exercises demonstrating low PM activity would be an important factor for rehabilitation to facilitate selective SA activation and reduction of the risk of the glenohumeral joint pathology.
The findings in this study indicated that SPP had a significantly lower PM/SA ratio than that of the KPP and WPP exercises in both subjects with and without scapular winging. Lower PM/SA ratio in SPP can be explained by the greater demands for shoulder muscle activity when subjects performing the SPP. Uhl et al. (33) reported that loads greater than 35% of the body weight were exerted on a single upper extremity during the SPP. Therefore, increased levels of upper extremity weight produce and induce more SA activity for stability of the shoulder complex. In addition, we found that the PM/SA ratios in the subjects with scapular winging during KPP and WPP exercises were higher than 3. Furthermore, Lunden et al. (21) reported that there were significant internal rotation and downward rotation of the scapula during the WPP exercise. These altered scapulothoracic and glenohumeral motion patterns observed during the WPP tend to cause a position that resulted in a decreased volume of the subacromial space or internal impingement of the rotator cuff. In light of these scapular kinematics results, our study suggests that the WPP may not be a beneficial exercise in shoulder rehabilitation patients with shoulder dysfunction related with weak SA (21).
Our findings are limited to a young male student population without shoulder pain, and the results cannot be generalized to other populations, including symptomatic women or older populations. Second, a method for identifying scapular winging is reliable but lacks validity. Third, we included the normalizing procedure for EMG activity as a percentage of RVCs. Although it was impossible to compare the results of this study with those of previous studies using maximal voluntary contraction, the RVC normalization method could prevent the risk of injury or pain in the shoulder and provide a more stable method than manual resistance. Fourth, we investigated the EMG activities of only SA and PM (sternal fiber). Further study should consider examining other muscles that contribute to scapular winging.
Subjects with scapular winging demonstrated higher PM activity, lower SA activity, and higher PM/SA ratios during 3 push-up plus exercises compared with the control group. In addition, the PM/SA ratio during the SPP was the lowest among the 3 push-up plus exercises. Our findings indicate that greater PM activity was found in subjects with scapular winging, and that the SPP can be an optimal exercise in the clinical setting for subjects with scapular winging, where maximum activation of the SA with minimal activation of the PM is desired.
All authors contributed to the concept, design, and data collection and analysis of this study. The authors appreciate all participants in this study. The authors certify that no party having a direct interest in the results of the research supporting this article has or will confer a benefit on us or on any organization with which we are associated.
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Keywords:Copyright © 2014 by the National Strength & Conditioning Association.
decreased serratus anterior activity; increased pectoralis major activity; modified push-up plus exercises; scapular dysfunction