Editorial Type:
Article Category: Research Article
 | 
Online Publication Date: 01 Nov 2019

Serratus Anterior and Upper Trapezius Electromyographic Analysis of the Push-Up Plus Exercise: A Systematic Review and Meta-Analysis

MS,
MS,
PT, BS, and
PhD
Page Range: 1156 – 1164
DOI: 10.4085/1062-6050-237-18
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Context

Whereas the serratus anterior (SA) and the upper trapezius (UT) work as a force couple for scapular motion, weakness of the SA and overactivation of the UT are often present in overhead athletes with shoulder dysfunction. Therefore, researchers addressing an intramuscular imbalance between the SA and UT have focused on finding exercises that target the weak SA and minimally activate the UT.

Objective

To compare the effectiveness of push-up plus (PUP) exercise variants based on the electromyographic (EMG) activity of the SA and UT.

Data Sources

A systematic search of PubMed and Scopus between January 1, 2000, and March 31, 2008.

Study Selection

Studies of PUP exercises that involved EMG analysis.

Data Extraction

We assessed study quality using the Critical Appraisal Skills Program. For the systematic analysis, the following data were extracted: (1) author, year, and study design; (2) participant characteristics; (3) type of PUP intervention; (4) EMG outcome measures; and (5) main results. For the meta-analysis, the EMG data of the SA and UT were calculated using the mean difference of EMG activity with a 95% confidence interval.

Data Synthesis

Based on 19 studies with 356 participants, different hand positions (the distance between the hands, shoulder-flexion angle, and elbow-flexion angle) and different lower extremity positions variably affected the activation of the SA and UT during the PUP exercise. Also, when participants performed the PUP on an unstable surface compared with a stable surface, UT activity increased 2.74% (95% confidence interval = 0.07%, 5.41%).

Conclusions

The standard PUP exercise elicited high EMG activity of the SA. Participants generated higher SA and lower UT EMG activity when they performed the PUP exercise on a stable surface in full elbow extension, with the hands placed shoulder-width apart, shoulder-flexion angles of 110° or 120°, and the ipsilateral lower extremity lifted.

Keywords: healthy participants; stable and unstable surfaces; scapular motion

The transfer of kinetic energy through the shoulder at rapid speeds with large ranges of motion and high precision is evident in the increased prevalence of shoulder injuries among overhead athletes.1,2 Scapular dyskinesis, defined as altered position and motion of the scapula, has been associated with shoulder impingement syndrome, rotator cuff tendinopathy, and multidirectional impairments.1,3,4 Reviewing 5 studies of 419 athletes, Hickey et al4 indicated that scapular dyskinesis increased the risk of future shoulder pain by 43% in asymptomatic athletes. Therefore, to regain a stable base for the optimal throwing motion, scapular-muscle training is an important part of injury prevention in and rehabilitation of overhead athletes.5–7

The serratus anterior (SA) and trapezius play important roles in moving and stabilizing the scapula during upper extremity motion.8,9 Whereas the SA protracts and upwardly rotates the scapula as the mover, it also stabilizes the middle border and inferior angle of the scapula to prevent winging and anterior tilt during upper extremity movements.10 Serratus anterior weakness is often present in overhead athletes and can result in shoulder dysfunction due to altered scapular kinematics, such as winging and tipping.8,11 Researchers11 who addressed an intramuscular imbalance between the SA and upper trapezius (UT) focused on finding exercises to target the weak SA and minimally activate the UT. The lower activation level of the SA with compensation via hyperactivity of the UT during upper extremity motion could result in a shoulder-shrugging motion with excessive superior translation, less efficient upward rotation, and posterior tipping of the scapula, which can lead to shoulder impingement.8,11

Practically, the push-up plus (PUP) exercise is often prescribed for strengthening the SA.8,12–14 During the PUP exercise, full scapular protraction (the plus) is added after full elbow extension at the end of the usual exercise.8 The plus phase during the PUP exercise elicits the highest average SA electromyographic (EMG) activity compared with other SA-activating and closed kinetic chain exercises.12–14 After finding that the standard PUP (SPP) and knee PUP exercises induced the highest SA and lowest UT : SA EMG measures, Ludewig et al8 recommended these exercises for selective SA strengthening. Researchers5,9,15–26 have investigated whether the PUP exercise performed on different unstable bases stimulated mechanoreceptors and increased SA EMG activity, thereby enhancing shoulder-joint stabilization. The use of unstable or stable surfaces during the PUP exercise is under debate. Some authors9,19 have suggested that performing the PUP exercise on an unstable base can lead to greater recruitment of related muscles, whereas others14,18 have indicated that performing the exercise on an unstable surface did not increase SA activity. Moreover, the PUP exercise performed on an unstable surface could generate higher UT activity.27 However, no difference in UT activation has been reported.28 To our knowledge, no investigators have published systematic reviews with meta-analyses in which they examined how PUP exercises performed on stable and unstable surfaces affected SA and UT EMG activity.

Other PUP modifications have been examined. One modification that may increase SA activity is performing the exercise on 1 hand.29,30 The influence of lower extremity extension on scapular-muscle activity during the PUP exercise has also been studied.29 Maenhout et al29 proposed that tightening the thoracolumbar fascia using a gluteus maximus muscle contraction during extension of the lower extremity in the PUP exercise may alter scapular-muscle activity. The functional length of the SA can change the contraction distance of the muscle, which affects muscle activity. Researchers16,31–34 have examined muscle activity using different hand orientations and at shoulder-flexion angles of 110°, 90°, and 70° during the PUP exercise. Lee et al16 reported larger SA EMG activity during the PUP exercise with the shoulder externally rotated than with it in neutral or internally rotated. Kim et al17 found that SA activity during the PUP exercise was higher when the ipsilateral lower extremity was raised than when the base of support (stable or unstable surface) was changed. Furthermore, performing the PUP exercise on an unstable surface would only challenge the external oblique and internal oblique muscles, which could facilitate lumbar stabilization. Lehman et al18 suggested that push-ups with the feet on an exercise bench and the hands on the floor had a greater influence on SA muscle activity. However, despite these influential factors, no standard exists for how the PUP exercise should be performed.

Considering the closed kinetic chain of the whole body during PUP exercise performance, we analyzed the effects of different factors acting concurrently on SA and UT muscle activity in this review. Therefore, the purpose of our study was to (1) analyze the effectiveness of varied PUP exercises on SA and UT muscle activity and (2) conduct a meta-analysis to verify the effects on SA and UT muscle activity of performing the PUP exercise on different surfaces (eg, a Swiss ball, wobble ball, or suspension sling).

METHODS

Search Strategy

This review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.35 Using PROSPERO, we confirmed that our research did not duplicate a review being conducted by another team and had not been registered. A systematic search was conducted on 2 databases, PubMed and Scopus, using 2 search strategies, with 1 related to each purpose. For the first purpose, published articles related to PUP variation exercises were included. Key words were push-up plus and electromyography. For the second purpose, studies comparing SA and UT activity during the PUP exercise performed on stable and unstable surfaces were selected. Key words were healthy subject, push-up plus, electromyography, and stable/unstable surface. Full search syntaxes can be found in the Supplemental Table (available online at http://dx.doi.org/10.4085/1062-6050-237-18.S1). Secondary searches were performed by (1) scanning the reference list of each full text that was evaluated and (2) performing citation tracking of the included studies. This search was limited to articles published between January 1, 2000, and March 31, 2018.

Inclusion Criteria and Outcome Measurement

To be included in our study, articles had to be written in English. Studies were included in the systematic review if the authors examined different PUP exercises by analyzing SA and UT EMG activity. For the meta-analysis, we included studies that were conducted of SA and UT EMG activity during the PUP exercise on stable and unstable surfaces and excluded those that did not provide means and standard deviations.

To reduce selection bias, 2 authors (F.J.K., H.L.O.) independently conducted the search processes. Studies were excluded based on the title, abstract, or full text. Disagreements were resolved by discussion and consensus with a third author (J.J.L.).

Data Extraction and Assessment of Risk of Bias

Two investigators (F.J.K., H.L.O.) separately extracted data from each trial. The data extracted from the selected studies were participant characteristics, information on exercise protocols, and details of the outcome measurements. When conflicts occurred in study qualifications between the data extractions, they were resolved by a third author (J.J.L.).

All included studies were assessed by 2 reviewers using the Critical Appraisal Skills Program, an evaluation tool for observational studies.36 The 6 criteria for evaluation were matching of participants and controls, a power calculation justifying the sample size, reproducibility of the electrode positions, reliability of the EMG equipment, the tester being blinded to group allocation, and sufficient results in the text or supplied by the authors. If information about any of the 6 criteria was not found in the article, a score of 0 was given. A third author (J.J.L.) settled any conflicts in study assessments.

Statistical Analysis

For the systematic analysis, the following data were extracted from the included articles: (1) author, year, and study design; (2) participant characteristics; (3) type of PUP intervention; (4) EMG outcome measures; and (5) main results. If data were missing, 2 researchers (F.J.K., H.L.O.) attempted to contact the authors to request the required information. A meta-analysis was deemed unfeasible for this part because of the small number of studies.

For the meta-analysis, the EMG data of the SA and UT were calculated using the mean difference (MD) with a 95% confidence interval (CI). During the PUP exercise, a positive effect size implied favorable outcomes on an unstable surface. All data were pooled using a random model of meta-analysis. Statistical heterogeneity across studies was quantified using I2 statistics: likely not important (0%–30%), moderate heterogeneity (31%–50%), substantial heterogeneity (51%–75%), and considerable heterogeneity (76%–100%), as recommended by Higgins and Green.37 Publication bias was examined using funnel plots. The α level was set at .05. We used Review Manager (version 5.3; The Cochrane Collaboration, Copenhagen, Denmark) to analyze the statistics.

RESULTS

Study Selection

The full search strategy and selection process are outlined in Figure 1. The initial database search was completed on March 31, 2018. We identified 30 study titles that potentially met the inclusion criteria. Of the 11 excluded studies, 3 examined different exercise types,12,38 and 8 used outcome measures other than EMG activity.39–46 Nineteen articles were included in the final analysis. Seven articles examined the effects of PUP variations (eg, performing the exercise in a standing or lying position8 or using different upper or lower extremity positions29,31,47–50) on SA and UT muscle activity. Twelve articles focused on the effects of the base of support during PUP exercises.9,15–23,51,52 After further checking for the meta-analysis, 1 article was excluded due to insufficient data for the means and standard deviations.51 Therefore, 11 articles were included in this meta-analysis for analyzing the differences in SA and UT muscle activity during the PUP performed on stable and unstable surfaces.9,15–23,52

Figure 1. Flow chart showing article selection.Figure 1. Flow chart showing article selection.Figure 1. Flow chart showing article selection.
Figure 1 Flow chart showing article selection.

Citation: Journal of Athletic Training 54, 11; 10.4085/1062-6050-237-18

Quality Assessment

The assessment of study quality is presented in Table 1. We did not include studies in which the testers were blinded to group allocation. Also, only data from healthy participants were included. All studies provided data from the electrode positions.

Table 1 Study Design and Methodologic Evaluation
Table 1

Synthesis of Results and Meta-Analysis

For the systematic review, we included the 7 articles in which the authors examined the effects of PUP variations on SA and UT muscle activity. The characteristics of the participants, interventions, outcome measures, and main results of the included studies are presented in Table 2. The sample sizes of the included studies ranged from 9 to 47 participants.

Table 2 Study Characteristics of Selected Articles Continued on Next Page
Table 2

For the meta-analysis, 11 articles were included.9,15–23,52 These articles involved a total of 213 participants, and all addressed PUP exercise programs on stable and unstable surfaces (Table 3). For the EMG outcome measures, we extracted data for the SA and UT (Table 2). The forest plot of the mean difference in SA EMG activity revealed no difference (0.01% maximal voluntary isometric contraction; 95% CI = −4.90, 4.92) between stable and unstable surfaces (Figure 2A). However, the forest plot of the mean difference in UT EMG activity (−2.85% maximal voluntary isometric contraction; 95% CI = −5.51, −0.19) revealed a difference between stable and unstable surfaces, with more UT activity elicited by unstable than stable surfaces (Figure 2B).

Table 3 Differences in Upper Trapezius and Serratus Anterior Electromyographic Muscle Activity During Push-Up Plus Exercise on Stable and Unstable Surfaces, Mean ± SD
Table 3
Figure 2. Forest plots demonstrating the individual point estimates and overall effect sizes for the questions, A, ‘‘Does the push-up plus exercise on an unstable surface elicit higher serratus anterior electromyographic muscle activity?'' and, B, ‘‘Does the push-up plus exercise on an unstable surface elicit higher upper trapezius electromyographic muscle activity?'' Abbreviation: CI, confidence interval.Figure 2. Forest plots demonstrating the individual point estimates and overall effect sizes for the questions, A, ‘‘Does the push-up plus exercise on an unstable surface elicit higher serratus anterior electromyographic muscle activity?'' and, B, ‘‘Does the push-up plus exercise on an unstable surface elicit higher upper trapezius electromyographic muscle activity?'' Abbreviation: CI, confidence interval.Figure 2. Forest plots demonstrating the individual point estimates and overall effect sizes for the questions, A, ‘‘Does the push-up plus exercise on an unstable surface elicit higher serratus anterior electromyographic muscle activity?'' and, B, ‘‘Does the push-up plus exercise on an unstable surface elicit higher upper trapezius electromyographic muscle activity?'' Abbreviation: CI, confidence interval.
Figure 2 Forest plots demonstrating the individual point estimates and overall effect sizes for the questions, A, ‘‘Does the push-up plus exercise on an unstable surface elicit higher serratus anterior electromyographic muscle activity?'' and, B, ‘‘Does the push-up plus exercise on an unstable surface elicit higher upper trapezius electromyographic muscle activity?'' Abbreviation: CI, confidence interval.

Citation: Journal of Athletic Training 54, 11; 10.4085/1062-6050-237-18

Despite using different methods to evaluate SA and UT EMG activity, we observed no heterogeneity among the analyzed studies (SA: P = .10, I2 = 37%; UT: P = .80, I2 = 0%). As determined by the Begg test, all P values were more than .05 without obvious funnel-plot asymmetry, revealing no publication bias for the effect sizes of SA and UT EMG activity (Figure 3).

Figure 3. Funnel plots demonstrating that publication bias was unlikely for electromyographic muscle activity during the push-up plus exercise on stable and unstable surfaces for the, A, serratus anterior and, B, upper trapezius.Figure 3. Funnel plots demonstrating that publication bias was unlikely for electromyographic muscle activity during the push-up plus exercise on stable and unstable surfaces for the, A, serratus anterior and, B, upper trapezius.Figure 3. Funnel plots demonstrating that publication bias was unlikely for electromyographic muscle activity during the push-up plus exercise on stable and unstable surfaces for the, A, serratus anterior and, B, upper trapezius.
Figure 3 Funnel plots demonstrating that publication bias was unlikely for electromyographic muscle activity during the push-up plus exercise on stable and unstable surfaces for the, A, serratus anterior and, B, upper trapezius.

Citation: Journal of Athletic Training 54, 11; 10.4085/1062-6050-237-18

DISCUSSION

Based on the database search, we included 18 articles in this review. Seven articles discussed the effects of PUP variations (eg, different upper extremity,31,47,48,50 lower extremity,29,49 and PUP8 positions) on training the SA and UT. Eleven articles9,15–23,52 focused on the effects of the base of support for PUP exercises. From our systematic review, we determined a suitable exercise prescription for training the SA and UT using PUP variations. During the PUP exercise, participants generated higher SA EMG activity and lower UT EMG activity with full elbow extension at normal shoulder width (hand placement equal to the participant's shoulder width) and shoulder-flexion angles of 110° or 120° while lifting the ipsilateral lower extremity. Moreover, according to the 11 articles, no difference in SA activity between stable and unstable surfaces was found during the PUP exercises. Yet more UT activity was generated on an unstable than a stable surface while performing. Activation of the UT likely increased during the PUP exercise when participants used an unstable surface because the hands were off the ground; if the feet maintained the same normalized position, raising the hands off the ground moved the glenohumeral joint into increased flexion, causing scapular elevation.

Whereas the SPP is an optimal exercise prescription for scapular-muscle training, the hand position, elbow flexion, shoulder flexion, and lower extremity extension all affect SA activation. Researchers8,47 have found that the SPP elicited higher SA EMG activity and a lower UT : SA ratio than the knee or elbow PUP. Batbayar et al48 reported that different hand positions induced differences in SA EMG activity. During the SPP, hand placement at normal shoulder width resulted in better SA EMG activity and a better UT : lower trapezius ratio than hand placement at a narrower or wider shoulder width.48 Lee et al31 noted that during the PUP exercise, the greatest SA muscle activity occurred at 110° of shoulder flexion. Hwang et al50 also observed that 120° of shoulder flexion should be used during the PUP exercise because it produces greater SA activation than 60° or 90° of shoulder flexion. Investigators29,49 have also demonstrated that lower extremity extension also influences SA EMG activity during the PUP exercise. When the ipsilateral lower extremity is extended, the contralateral extremity bears more weight, resulting in greater hip stabilization. This activates the contralateral internal oblique muscle, which in turn stimulates the ipsilateral external oblique muscle, possibly resulting in greater SA muscle recruitment.

Interestingly, we found no difference in SA EMG activity when the PUP exercise was performed on stable and unstable surfaces. As a closed kinetic chain exercise, the PUP would presumably stimulate the mechanoreceptors and enhance shoulder-joint and scapular stabilization. This stimulus is suggested to increase on an unstable base, possibly challenging neuromuscular control.53 However, from our review, it appears that using different kinds of base support was not the major factor affecting SA EMG activity during the PUP exercise. Other factors, such as hand position,15,16 neuromuscular control,53 or upper extremity weight-bearing status,18,30 may overcome the effects of the base of support. Gioftsos et al15 determined that the SA and UT activations during the PUP exercise were not affected by the support surface but were affected by the phase of the exercise and the hand position. Lee et al16 also reported that positioning the hands at 90° of external rotation during the PUP exercise elicited more SA EMG activity than positioning the hands at neutral or 90° of internal rotation. Moreover, a high correlation (r = 0.97, P < .01) existed between increasing weight-bearing posture and muscular activity during the PUP.30

The various parts of the SA muscle are activated differently during the PUP exercise. Park and Yoo9 studied the upper and lower portions of the SA using surface EMG. In healthy participants, the lower fibers of the SA showed increased activation on an unstable surface, which required more joint stability than a stable base; however, the upper fibers showed no difference between the stable and unstable surfaces. Inman et al54 indicated that the lower portions of the SA and trapezius were crucially important in stabilizing the inferior angle of the scapula during upper extremity movement. Taking this point of view, the lower part of the SA would seem to demonstrate greater activity in stabilizing the scapula on an unstable surface; however, many researchers who used surface EMG to detect muscle activity focused only on the lower part of the SA. Therefore, in the future, investigators should focus on other parts of the SA during the PUP exercise.

To our knowledge, this review is the first to systematically summarize the activity of the SA and UT during the PUP variation exercise and our meta-analysis is the first to summarize the activity of the SA and UT during the PUP on a stable or unstable surface. However, our study had some methodologic limitations. Few authors of the included studies justified their sample sizes or performed reliability tests.

Motor control during the different PUP exercises is unclear. More research is needed to address motor control of variables such as muscle timing or recruitment patterns during the PUP exercise and to investigate other shoulder and scapular muscles, such as the lower trapezius, middle trapezius, and rotator cuff. Moreover, it would be worthwhile to study kinematic motion during the PUP to understand the relationships between muscle activity and the movements of humeral internal and external rotation and scapular upward and downward rotation.

CONCLUSIONS

Participants can generate higher SA and lower UT EMG activity if they perform the PUP exercise in full elbow extension, at normal shoulder width, at shoulder-flexion angles of 110° or 120°, and while lifting the ipsilateral lower extremity. Performing the PUP exercise on an unstable surface may induce higher levels of UT activation but will not increase SA activation. If the goal of the exercise program is to strengthen the SA muscle with less UT activity, the PUP exercise should be performed on a stable surface.

ACKNOWLEDGMENTS

This review was supported by award 104-2314-B-002-026-MY13 from the Ministry of Science and Technology, Taiwan.

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SUPPLEMENTAL MATERIAL

Supplemental Table. Searching strategy using Scopus and PubMed.

Found at DOI: http://dx.doi.org/10.4085/1062-6050-237-18.S1

Copyright: © by the National Athletic Trainers' Association, Inc
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Figure 1
Figure 1

Flow chart showing article selection.

Figure 2
Figure 2

Forest plots demonstrating the individual point estimates and overall effect sizes for the questions, A, ‘‘Does the push-up plus exercise on an unstable surface elicit higher serratus anterior electromyographic muscle activity?'' and, B, ‘‘Does the push-up plus exercise on an unstable surface elicit higher upper trapezius electromyographic muscle activity?'' Abbreviation: CI, confidence interval.

Figure 3
Figure 3

Funnel plots demonstrating that publication bias was unlikely for electromyographic muscle activity during the push-up plus exercise on stable and unstable surfaces for the, A, serratus anterior and, B, upper trapezius.

Contributor Notes

Address correspondence to Jiu-Jenq Lin, PhD, Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, No. 1 Changde Street, Zhongzheng District, Taipei, Taiwan, 100. Address e-mail to jiujlin@ntu.edu.tw.
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