Physical Therapy Korea

Scapular winging (SW) is a specific condition in which the medial border of the scapular lifts off the thoracic wall in the scapulothoracic joint [1,2]. It is a painful condition, and affected individuals find it hard to lift, pull, and push objects, as well as perform activities of daily living such as brushing hair and teeth or carrying bags [2]. Commonly, weakness of the serratus anterior (SA) muscle leads to SW [3]. The SA is the primary muscle that prevents SW and anterior tilting of the scapula during arm movement [3,4]. During arm movement, altered scapular kinematics due to weakness of the SA are associated with an imbalance in the activity of the other scapular muscles, such as the upper trapezius (UT), thus causing scapular dysfunction and impingement [5,6].

Previous studies have studied the activity of the scapular muscles during shoulder flexion in individuals with shoulder impingement to identify scapular dysfunction [5,7,8]. Shoulder flexion is accompanied by upward rotation of the scapula, which occurs as a force couple of the SA, UT, and lower trapezius (LT) muscles [3,9]. The weakness of the SA may contribute to the overuse of the synergistic muscles, such as the UT [10]. The overuse of UT during shoulder flexion causes excessive scapular elevation, resulting in kinematic movement dysfunction or shoulder impingement [5,11].

Previous studies reported that the SA activity was significantly lesser in individuals with SW than in those without SW during push-up or shoulder protraction movements [12-15]. Additionally, the UT/SA ratio of muscle activity was greater in individuals with SW than in those without SW during shoulder protraction [12].

The study by Namdari et al. [16] showed that 121 ± 6.7° of shoulder flexion is needed for daily activities. Understanding the difference in the activity of the scapular muscles between individuals with and without SW during 120° shoulder flexion is important for the evaluation and management of SW. However, previous studies investigated the difference in the activity of the scapular muscles between individuals with and without SW only during shoulder protraction [12-15]. Therefore, this study aimed to compare the activity of the scapular muscles between individuals with and without SW during 120° shoulder flexion with a load.

1. Participants

This study enrolled 27 individuals with SW (n = 14) and without SW (n = 13). A scapulometer was used to determine SW [17]. Participants with limited range of motion of the shoulder, neurological dysfunction, shoulder pain, or history of shoulder surgery were excluded [18]. The general characteristics of the participants are shown in Table 1. This study was approved by the Institutional Review Board (1041849-201709-BM-094-03) of Yonsei University, and all volunteered participants provided written informed consent.

Table 1 . General characteristics of the participants.

Characteristic	Group without SW (n = 13)	Group with SW (n = 14)	p-value
Age (y)	23.69 ± 4.36	21.92 ± 1.77	0.176
Height (cm)	175.46 ± 4.33	174.42 ± 4.01	0.526
Weight (kg)	75.11 ± 9.39	72.20 ± 9.30	0.426
SW (cm)	1.37 ± 0.31	2.44 ± 0.52	0.000*

Values are presented as mean ± standard deviation. SW, scapular winging. *p < 0.05..

2. Instruments

Noraxon TeleMyo 2400 system (Noraxon Inc., Scottsdale, AZ, USA) and Noraxon MyoResearch 1.08 XP software (Noraxon Inc.) were used to collect and analyze the electromyography (EMG) data. In this study, three bipolar Ag/AgCl disposable electrodes were used. The EMG data signals were amplified and band-pass filtered (10–500 Hz) before being recorded at 1,000 Hz and then processed as the root mean square values.

The EMG activity of the UT, LT, and SA muscles was measured during shoulder flexion. The electrodes were attached to UT, LT, and SA muscles parallel to the muscle fibers. The UT electrode was attached at the midpoint between the acromion and the seventh cervical vertebra. The LT electrode was attached from the inferior medial border of the scapula to the spine at an oblique angle, approximately 5 cm. The SA electrode was attached to the anterior aspect of the scapula [19]. The skin of the participants was shaved and wiped with alcohol before attaching the electrodes.

The EMG data of the UT, LT, and SA muscles were normalized by maximal voluntary isometric contraction (MVIC). The EMG activity was recorded in a manual muscle testing position to calculate the MVIC as per previous research [9]. The EMG data were collected three times for five seconds. The data of the middle 3-second period were used for calculating the MVIC. A rest period of one minute was given to prevent fatigue between the trials.

Smart KEMA tension sensor (KOREATECH Co., Ltd., Seoul, Korea) was used to determine the load during shoulder flexion. Participants were made to sit on a chair in an upright position and flex their shoulder at 90° (Figure 1). A strap was attached just above the wrist of the testing arm, and the participants flexed their arm upward as much as possible. The maximal force was recorded by Smart KEMA tension sensor, and 25% of this maximal shoulder flexion force was used as the testing load for 120° shoulder flexion in each participant [20].

Figure 1. Measurement of maximal shoulder flexion force.

A scapulometer was used to measure the degree of SW [1]. In the standing position, the participant flexed the elbow at 90° and placed the forearm and wrist in a neutral position. Following this, weight corresponding to 5% of the body weight was applied to the wrist, and the scapulometer was placed on the thoracic wall of the participant. SW was defined if the distance between the thoracic wall and the scapular inferior angle was more than 2 cm. The interrater and intrarater reliability of this instrument are 0.955 and 0.921, respectively [17].

3. Procedures

Each participant sat in the chair with their feet on the ground and back straight [21]. With an extended elbow and neutral position of the forearm, 120° shoulder flexion was performed (Figure 2). The range of shoulder flexion was controlled by a horizontal target bar adjusted by a smartphone inclinometer. The participants performed the test with dumbbell of load equivalent to 25% of the maximum shoulder flexion force measured using Smart KEMA tension sensor [20]. They practiced the task using a smartphone metronome (60 beats/min) for five minutes to achieve the required movement velocity [18]. After a 5-minute rest, the participants flexed their shoulder to the target bar for five seconds [22]. The 5-second data were used for analysis, and 30-second resting time was given to minimize muscle fatigue. Shoulder flexion was performed three times in this manner to collect the EMG data.

Figure 2. Shoulder flexion with load.

4. Statistical Analysis

All statistical analyses were performed using SPSS version 21.0 (IBM Co., Armonk, NY, USA). The Shapiro–Wilk test was used to assess the normal distribution of the data. Independent t-test was used to identify significant differences in the SA, UT, and LT muscle activities and SA/UT activity ratio between the groups with and without SW during shoulder flexion. The level of statistical significance was set at α of 0.05.

The results of the activities of the scapular muscles are shown in Table 2. The results showed that the SA activity under 25% load of the maximal shoulder flexion force was significantly lesser in the group with SW than in the group without SW. There were no significant differences in the UT and LT activity and SA/UT ratio.

Table 2 . Comparison of the muscle activities and activity ratio between the groups with and without scapular winging.

	Group without SW (n = 13)	Group with SW (n = 14)	t	p-value
SA	39.00 ± 12.12	28.53 ± 7.97	−2.66	0.013*
UT	20.38 ± 6.92	21.86 ± 11.10	0.41	0.683
LT	23.88 ± 9.20	21.80 ± 5.51	−0.71	0.481
SA/UT	2.07 ± 0.80	1.61 ± 0.85	−1.44	0.161

Values are presented as %MVIC ± standard deviation. SW, scapular winging; SA, serratus anterior; UT, upper trapezius; LT, lower trapezius; %MVIC, %maximal voluntary isometric contraction. *p < 0.05..

This study investigated the difference in the activity of the scapular muscles between the groups with and without SW during shoulder flexion with 25% load of the maximal shoulder flexion force. This study hypothesized that SA activity is lesser in the group with SW than in the group without SW, and the results proved the hypothesis right by showing a significant difference in the SA activity between the two groups. This corroborated with the findings of previous studies [12-15]. The second hypothesis was that the compensatory muscle activity of UT or LT would be greater in the group with SW than in the group without SW. However, the results showed no significant differences in the UT and LT activity with 25% load of the maximal shoulder flexion force between the two groups.

In the study by Kim et al. [12], the SA activity and SA/UT ratio were significantly lesser in individuals with SW than in those without SW during shoulder protraction, which was similar to our findings. Since SW accompanies SA weakness, the UT muscle might show increased activity to compensate for the upward rotation of the scapula. Lawrence et al. [23] reported that shoulder flexion requires humeral angular movement as well as scapular upward rotation. Furthermore, the humeral angular movement was more than the scapular upward rotation during shoulder flexion in the sagittal plane than in the other planes such as scapular and coronal planes. In our study, the UT and LT activity and SA/UT ratio did not show significant differences between the groups. Although there were no compensatory activations in the UT and LT in our study, it is possible that movements occur in the humeral angular joint to compensate for the SA weakness.

Ludewig and Cook [5] reported that there was no significant difference in the UT activity between individuals with and without shoulder dysfunction, when no load or a low load (2.6 kg) was applied. On the other hand, the UT activity was significantly greater in individuals with shoulder dysfunction than in those without shoulder dysfunction, when a load of 4.6 kg was applied. In our study, the UT activity did not show a significant difference between the two groups with a load. The load used was 25% of the maximum shoulder flexion force (group with SW: 2.17 ± 0.52 kg; group without SW: 2.14 ± 0.4 kg). It is possible that the compensatory activations of the UT and LT muscles were not observed due to the low load in our study. Therefore, it is necessary to study the difference in the UT activity when a greater load is applied during shoulder flexion.

Compensatory scapular retraction could occur in the group with SW to reduce the load. Scapular retraction relieves the load during shoulder flexion, because this movement can shorten the lever arm [3]. In our study, it is possible that there were compensatory movements, such as scapular retraction and depression, in the group with SW. Therefore, further studies measuring scapular movements and the activities of scapular muscles simultaneously are warranted.

Shoulder flexion involves scapular upward rotation in coordination with humeral angular motion [23]. The deltoid muscle is the prime mover of the humeral angular motion during arm elevation. Moreover, the rotator cuff muscles play an important role in stabilizing the glenohumeral joint by restricting the excessive translation of the humeral head superiorly during arm elevation [24]. Myers et al. [25] reported that individuals with shoulder dysfunction exhibited greater activation of the deltoid muscle and lesser activation of the rotator cuff muscles than those without shoulder dysfunction did. Therefore, studies on the deltoid and rotator cuff muscles are needed to confirm compensatory humeral movement.

This study has some limitations. First, we only used 25% load of the maximal shoulder flexion force; hence, it is necessary to investigate the activity of the scapular muscles with greater loads. Second, our study enrolled only healthy and relatively young men. Thus, our findings cannot be generalized to individuals with shoulder dysfunction and to women or an older population. Further studies are needed to investigate the scapular and humeral joint movements simultaneously with shoulder muscles, such as the deltoid, rotator cuff, and pectoralis major muscles.

This study investigated the difference in the EMG activity of the scapular muscles during shoulder flexion with 25% load of the maximal shoulder flexion force between individuals with and without SW. The results showed that the SA activity was lesser in the group with SW than in the group without SW. However, there was no compensatory activity in the UT and LT muscles. Thus, further studies are warranted to clarify the compensatory movement strategy of the scapular muscles during shoulder flexion in individuals with SW.

None.

None to declare.

No potential conflict of interest relevant to this article was reported.

Conceptualization: OK. Data curation: JJ. Formal analysis: SJ. Investigation: JJ, SK. Methodology: JJ, SJ. Project administration: JJ, SJ. Resources: JJ, SK. Supervision: OK. Validation: JJ, SJ. Writing - original draft: JJ. Writing- review & editing: SJ, OK.