Physical Therapy Korea

Rotator cuff (RC) repair is an operation performed to recover muscle weakness and functional limitations caused by RC tendon injury, and most patients expect to recover muscle strength after surgery [1]. The RC plays a multiple and pivotal role in performing efficient shoulder functions, so this muscle recovery is considered important to restore shoulder function after shoulder injury [2,3].

Scapular dyskinesis is found in most patients with shoulder injuries [4,5]. Scapular dyskinesis refers to the appearance of incorrect position or movement of the scapula during scapulohumeral movement. Clinically observable findings in scapular dyskinesia are the prominence of the medial scapular border and inferior angle, which are related to the scapular position during internal rotation and anterior tilting [4]. Studies using magnetic resonance imaging (MRI) suggest that changes in scapular kinematics during shoulder movement may be related to changes in subacromial space [6], and such abnormal scapular movement control may be a risk factor for increasing the risk of subacromial compression of RC tendons [7,8]. The scapula functions to provide stability for optimal activation of scapular muscles, but positional changes such as internal rotation or protection of the scapular cause muscle weakness [9,10]. Excessive scapular protraction was frequently observed in patients with scapular dyskinesis and decreased maximal RC strength by 23% [9]. By taking a passive stabilization position and a scapula-retracted posture, the strength of the RC may be improved [11].

The biceps brachii is the flexor muscle of the elbow and the supinator muscle, and also plays a role in shoulder flexion [12,13]. The short head of the biceps attaches at the coracoid process to the anterior part of the scapula. The position of an altered scapula affects the length-tension relationship of the biceps and can lead to an instability of the scapula, resulting in muscle weakness [14]. Therefore, the scapular position can affect not only the muscle strength of the RC, but also the strength of the biceps muscle. However, as far as we are concerned, there is still a lack of evidence that upper extremity muscle strength changes according to the scapula position.

Many previous studies have demonstrated an association between scapular dyskinesis and shoulder pain, as well as the decreased muscle strength in patients with a RC tear. Although scapular kinematics problems may cause RC injury, studies of scapular dyskinesis after RC repair have not been evaluated. Furthermore, the scapular dyskinesis may be a cause of upper extremity muscle weakness in patients with RC tears, but abnormal movements of scapular after surgery is not considered.

The purpose of this study is to investigate the presence of scapular dyskinesis in arthroscopic RC repair patients and the effects of scapular position on upper extremity muscle strength in patients with RC repair. We hypothesized that patients with RC repair have scapular dyskinesis and that upper extremity muscle strength would significantly increase in the passive scapular stabilization position.

1. Participants

A total of 30 patients after RC repair (14 males and 16 females) participated in this study. All participants were at least 12 weeks after arthroscopic RC repair due to a tear of the supraspinatus tendon. For a precise comparative study under homogeneous conditions, only patients with medium- or large-sized tears were included in the study [15,16]. Exclusion criteria were patients with multi-tendon tears, superior labrum from anterior to posterior (SLAP) lesions, glenohumeral arthritis, acromioclavicular arthritis, or subjects who underwent tenotomy or tendon fixation of the long head of the biceps brachii [17]. The demographic data of the participants is shown in Table 1. Prior to the experimental procedures, all participants were provided with information about the study and all subjects signed an informed consent form approved by the Institutional Ethics Committee of Inje University (IRB no. INJE 2018-10-014-001).

Table 1 . Demographic data for patients.

Variable	Total (N = 30)
Age (y)	51.81 ± 9.10
Sex
Male	14 (62.5)
Female	16 (71.4)
Height (cm)	167.10 ± 8.38
Weight (kg)	73.09 ± 13.67
VAS for shoulder pain	5.40 ± 1.00
Repaired side
Dominant	18 (60.0)
Non-dominant	12 (40.0)
Arthroscopic finding
Size of rotator cuff rear
Small	9 (30.0)
Medium	21 (70.0)

Values are presented as mean ± standard deviation or number (%). VAS, visual analog scale..

The sample size was determined using the free statistical package, G*power software (ver. 3.0; Franz Faul, Kiel University, Kiel, Germany), based on our own pilot test, because no prior research has examined differences in scapular dyskinesis between with and without the arthroscopic RC repair. The pilot test consisted of five postoperative shoulder and five contralateral shoulder, and it showed that at least 27 subjects would be required to detect a significant difference in scapular dyskinesis between the two groups using a 1-tailed test with a power of 0.95% at a significance level of 0.05 and an effect size of 0.8. Given our decision to use scapular dyskinesis as the primary end point, only the scapular dyskinesis, and no other winged scapular and muscle strength (abduction, flexion, and external rotation [ER]), was used in the sample size. Owing to the possibility of withdrawals and loss to follow-up, we recruited 30 subjects.

2. Measurement of the Winged Scapula

The winged scapula (WS) was measured with each subject standing in a neutral rotation position of the shoulder, the elbow flexion at 90°, and the forearm in a neutral position. Static induced WS was measured to test the subject’s ability to stably maintain the scapular position from an external load by placing a weight cuff of 5% of the subject’s body weight on the wrist. In this position, a scapulometer was used to measure the distance between the thorax and the inferior angle of the scapula (Figure 1). The WS extent was confirmed based on the average distance of three measurements [18].

Figure 1. Measurement of winged scapula using a scapulometer.

3. Observational Clinical Assessment of Scapular Dyskinesis

Two blinded clinicians conducted an independent assessment process for each subject’s scapular motion. Each clinician observed the medial and superior scapular border during the patient performed 3–5 trials of arm elevation tasks in the sagittal and scapular planes. Clinicians classified the scapular motion into one of four categories (4-type methods) according to the “predominant pattern of scapular asymmetry observed,” among the asymmetric motion of scapula [19]. This category of Kibler et al. [7] is considered the golden standard. This clinical assessment method was based on an altered scapular motion or resting position occurring in a single scapular kinematic [20,21].

Type 1 dyskinesis pattern is characterized by the prominence of an inferior medial scapular angle and is associated with an excessive anterior tilting of the scapula. Type 2 abnormal dyskinesis patterns are characterized by excessive internal rotation of the scapula and prominent of the entire medial border. In the pattern of Type 3 dyskinesis pattern, prominence of the superior border and excessive upward translation of the scapula appears. Type 4 pattern is classified as “normal” and indicates that no asymmetry in bilateral scapular motion was observed and no medial or superior border prominence was observed. Normal scapular motion is described by posterior tilt, ER, and slightly superior translation during arm elevation [18]. When clinicians observed the movement of the scapula in multiple planes of motion, one dominant pattern was determined among a various asymmetric patterns.

4. Measurement of Isometric Upper Extremity Muscle Strength and Procedures

The measurement of isometric shoulder abduction, elbow flexion, forearm supination, and strength was using fixed-based instrumentation that was customized for measuring the strength of upper extremity muscles. The load cell (RSBA-50L; Radian, Seoul, Korea) is connected to a fixed based, which is a device designed as a digital indicator that displays the peak force value, with a force detection range of 0 to 490 N, a resolution of 0.01 N, and a precision of ± 0.03 N. The sampling rate was 100 Hz. This measuring instrument has demonstrated excellent intra- and inter-rater correlation (ICC) for strength measurement of isometric shoulder protraction in a previous study [22].

5. Experimental Procedures

This study was divided into abnormal movement of the scapula and measurement of upper extremity muscle strength when the scapula was passively stabilized. To assess abnormal movement of the scapula, the WS was measured and the type of scapula dyskinesis was classified. Before measuring upper extremity muscle strength, each participant practiced this process in a seated position for 5 minutes to familiarize themselves with isometric forward flexion, elbow flexion, and forearm supination. Three isometric upper extremity strength tests were performed at random: 1) shoulder abduction, 2) elbow flexion, and 3) forearm supination. Each muscle test was performed as follows (Figure 2). The test for isometric shoulder abduction strength was evaluated in a sitting position with the shoulder in 90° of abduction in the scapular plane (a plane angled 30° anterior to the coronal plane) and 90° of ER of the humerus (the “full can” position) [17]. Isometric elbow flexion strength was evaluated in a sitting position with the shoulder in a neutral position, the forearm in supination, and the elbow flexed to 90° [23]. Isometric forearm supination strength was evaluated in a sitting position with the shoulder in a neutral position, the forearm at 75% supination, and the elbow flexed to 90° [24]. During the test, participants were asked to keep their elbows at their sides in a stable position with their elbows against their waist. Data were collected while each subject was uniformly instructed to exert the sub-maximal isometric forward flexion, elbow flexion, and forearm supination for 5 seconds with 1 minute rest periods between the trials. Three repetitions and a mean value of the peak force data were used for data analysis. The same examination procedure was performed after a separate examiner stabilized the shoulder in a posterior tilting position, the scapula was put into an ER in relation to the thorax, and the patient’s back rested against the wall to apply force along the medial border of the scapula. This procedure was classified as the scapular reposition test [4].

Figure 2. Three upper extremity strength in sitting position. (A) Shoulder abduction, (B) elbow flexion, and (C) elbow supination.

6. Statistical Analysis

The statistical analyses were performed using PASW Statistics ver. 18.0 for Windows (IBM Co., Armonk, NY, USA). A chi-square test was used to determine that statistical difference between two different variables for comparison of scapula type. An independent t-test was used to compare the average distance between the thorax and the scapula inferior angle for the RC repair shoulder and contralateral shoulder. A 2-way mixed measures analysis of variance (ANOVA) was used to determine differences in muscle strength (shoulder abduction, elbow flexion, and forearm supination) during scapular position (natural and stabilization) between RC repair shoulder and contralateral shoulder. In analyses, p < 0.05 was deemed to be statistically significant. If a significant group and condition interaction was not revealed form the 2-mixed way ANOVA, the main effects of group and condition were determined. If a significant main effect were observed, the Bonferroni correction was used and if a significant group and conditions interaction was found, a pair-wise comparison with Bonferroni correction was used. The blinded evaluator collected the data.

Table 1 presents the demographic characteristics of the 30 subjects in this study. This study collected all variables in a prospective manner, and there was no missing data on quantitative variables. The 30 participants were assessed and found to have scapular dyskinesis in each RC repair shoulder and the contralateral (non-RC repair) shoulder. The type of scapular dyskinesis is shown in Table 2 and Figure 3. Regarding the type of RC repair in the scapular plane, Type 1 was found in nine participants, Type 2 in 14 participants, and Type 3 in five participants, while the normal type was found in two participants. For the contralateral shoulder, Type 1 was found in five participants, Type 2 in eight participants, and Type 3 in four participants, while the normal type was found in 13 participants (Table 2, Figure 3). The results of the paired t-test showed that the distance between the thorax and the inferior angle of the scapula is significantly increased in the RC repair shoulder compared to the distance in the contralateral shoulder (F = 0.052, p < 0.01) (Table 3, Figure 4).

Table 2 . Statistical difference between two different variables for comparison of scapula type (N = 30).

Group	Type 1	Type 2	Type 3	Type 4	X2
RC repair	9 (30.0)	14 (46.0)	5 (17.0)	2 (7.0)	10.957
Non-RC repair	5 (17.0)	8 (27.0)	4 (13.0)	13 (43.0)	0.012*

Values are presented as number (%). Type 1: Abnormal dyskinesis patterns with the prominence of an inferior medial scapular angle, excessive anterior tilting of the scapula. Type 2: Abnormal dyskinesis patterns with the excessive internal rotation of the scapula and prominent of the entire medial border. Type 3: Abnormal dyskinesis patterns with the prominence of the superior border and excessive upward translation of the scapula. Type 4: A pattern classified as “normal” and no asymmetry in bilateral scapular motion. RC, rotator cuff. *p < 0.05..

Table 3 . Comparison of rotator cuff repair shoulder and contralateral shoulder in the winged scapula.

Variable	Subject shoulder		p-value
	RC repair	non-RC repair
Scapular winging (cm)	1.98 ± 0.53	1.11 ± 0.54	< 0.01**

Values are presented as mean ± standard deviation. RC, rotator cuff. **p < 0.01..

Figure 3. The graph shows significant difference the type of scapular dyskinesis between RC repair and non-RC repair. Type 1: Abnormal dyskinesis patterns with the prominence of an inferior medial scapular angle, excessive anterior tilting of the scapula. Type 2: Abnormal dyskinesis patterns with the excessive internal rotation of the scapula and prominent of the entire medial border. Type 3: Abnormal dyskinesis patterns with the prominence of the superior border and excessive upward translation of the scapula. Type 4: A pattern classified as “normal” and no asymmetry in bilateral scapular motion. RC, rotator cuff.

Figure 4. The graph shows significant difference for the winged scapula between RC repair and non-RC repair. RC, rotator cuff. **p < 0.01.

Three muscle strength measurements (shoulder abduction, elbow flexion, and forearm supination) taken during two scapular positions (scapular natural position and scapular stabilization position) in each RC repair and non-RC repair shoulder are shown Table 4. For shoulder abduction, there were significant main effects for RC Repair (F = 72.935, p < 0.01), a main effect for the scapular position condition (F = 4.362, p < 0.05), and a significant interaction (F = 25.593, p < 0.01) (Figure 5). A significant main effect was found for RC repair (F = 32.814, p < 0.01) and the scapular position condition (F = 47.149, p < 0.01) in the elbow flexion strength and a significant interaction was revealed (F = 14.204, p < 0.01) (Figure 6). In the forearm supination strength, the main effect for RC repair (F = 49.635, p < 0.01) and the scapular position condition (F = 17.917, p < 0.01) were significant, but the interaction was not significant (F = 0.374, p = 0.546) (Figure 7). At the RC repair, muscle strength in the shoulder abduction (p < 0.01), elbow flexion (p < 0.01) and forearm supination (p < 0.05) were significantly higher in the scapular stabilization position than in the scapular natural position. In contrast, muscle strength in elbow flexion (p = 0.189), forearm supination (p = 0.23) was significantly different but forward flexion (p = 0.464) showed no significant difference in the non-RC repair shoulder.

Table 4 . Comparison of muscle strength with and without scapular stabilization in RC repair and non-RC repair shoulder.

Variable	Group	SNP	SSP	Within-group change	Between-group change
Shoulder abduction	RC repair	2.78 ± 1.56	3.45 ± 1.69	0.66 (–0.85 to –0.47)**	3.90 (–4.86 to –2.94)**
	Non-RC repair	7.10 ± 3.40	6.94 ± 3.08	0.16 (–0.21 to 0.54)*
Elbow flexion	RC repair	5.66 ± 2.53	7.17 ± 3.50	1.51 (–1.97 to –1.04)**	4.13 (–5.55 to 2.70)**
	Non-RC repair	9.66 ± 4.20	10.86 ± 5.57	0.61 (–0.94 to –0.28)**
Forearm supination	RC repair	2.43 ± 1.26	2.80 ± 1.51	0.37 (–0.56 to –0.18)**	0.73 (–2.23 to –1.23)
	Non-RC repair	4.20 ± 0.99	4.56 ± 1.04	0.30 (–0.51 to –0.91)**

Values are presented as mean ± standard deviation or mean difference (95% CI). RC, rotator cuff; SNP, scapular natural position; SSP, scapular stabilization position. *p < 0.05, **p < 0.01..

Figure 5. Comparison of shoulder abduction strength during SNP and SSP between RC repair and non-RC repair. SNP, scapular natural position; SSP, scapular stabilization position; RC, rotator cuff. **p < 0.01.

Figure 6. Comparison of elbow flexion strength during SNP and SSP between RC repair and non-RC repair. SNP, scapular natural position; SSP, scapular stabilization position; RC, rotator cuff. **p < 0.01.

Figure 7. Comparison of forearm supination strength during SNP and SSP between RC repair and non-RC repair. SNP, scapular natural position; SSP, scapular stabilization position; RC, rotator cuff. **p < 0.01.

The purpose of this study was to compare the scapular position and motion of the RC repair shoulder with the contralateral shoulder of a patients who operated arthroscopic RC repair and suggest the effect of passive scapular stabilization to increase upper extremity muscle strength. The results of the present study showed that the affected shoulder had a significantly greater WS than the contralateral shoulder, with scapular dyskinesia, and showed differences in upper extremity muscle strength. Our results demonstrate that passive scapular stabilization had the effect of increasing upper extremity strength in the affected shoulder.

In the present study, after arthroscopic RC repair, it is confirmed that most patients (93.3%) scapula remains in an anterior tilting and internally rotated position. Although the causal relationship between scapular dyskinesis and shoulder pathology is uncertain [25,26], this scapular position affects the subacromial space, which may increase the risk of external impingement. Such impingement may cause the risk of RC tear and reduced RC muscle strength. In previous studies, it was expected that recovery of the RC and normal muscle activity pattern of the scapular muscle would lead to normalization of scapular movement after surgery [27]. However, our study result is different. Because, it was measured 12 weeks after surgery, there was a possibility that the results differed from previous studies. As a result of this study, patients feel pain in the surgical site after initial RC repair, so compensation for scapular motion can continue as if it was adapted to protect the shoulder from preoperative pain. Therefore, it is possible that scapular kinematics are not corrected during initial rehabilitation and strength training is performed, the RC may be damaged again at any time.

In this study, upper extremity muscle strength was significantly different in the RC repair shoulder and contralateral shoulders. A decrease in muscle strength was observed in individuals with RC tears. Especially, because the supraspinatus is the shoulder abductor muscle that contributes to ER, symptomatic patients with RC tears showed weakness in abduction and flexion strength compared to those without a tear [28]. Our study showed a weakness in the shoulder abduction of the affected shoulder, as well as in elbow flexion and forearm supination. This biceps muscle is a supinator and elbow flexor muscle and, it also acts as a shoulder flexor anatomically [12,14]. Proximal biceps disorder usually results in anterior shoulder pain with radiation into the arm along the muscle belly in some cases [29,30]. However, this study excluded patients with biceps tendinitis. Therefore, the causes of weaknesses other than RC tear or biceps disorders may be found elsewhere. Altered scapular motion could shorten the biceps muscles and reduce the ability of these muscles to generate tension during isometric elbow flexion and forearm supination. The short head of the biceps brachii was attached from the coracoid process of the scapula to the radial tuberosity, and thus the scapula positional change was associated with the biceps brachii function.

In this study, the upper extremity muscle strength of the affected shoulder significantly increased in the passive scapular stabilization position. The increase in supraspinatus strength we identified is similar to the findings of Kibler et al. [11]. They reported a statistically significant increase in supraspinatus strength in both non-injured and injured patients when the scapula was in the retraction position. In our study, on the other hand, this effect was present in affected shoulders, but there was no significant difference in contralateral shoulders. This finding is probably due to the different test position during shoulder flexion in each studies. While previous studies were examined with empty can position, this study was tested with full can position. Empty can position was in greater scapular upward rotation, internal rotation, and clavicular elevation and in less scapular posterior tilt than full can position. Therefore, in our study, the effect of scapular of stabilization would have been smaller because the change of the scapular in healthy subjects is less than that in empty can position. Our study also shows that biceps muscle strength significantly increased in the scapular stabilization position. This means that the position of the scapular can affect the muscle strength of the RC muscle as well as other upper extremity. Scapular dyskinsis have a possibiliy to negative effect on muscle strength recovery after RC repair. Scapular dyskinesis is a common in patients with shoulder injury. Our study showed that patients who underwent arthroscopy RC repair have a significant association with scapular dyskinesis. The scapula may not be appropriate to provide an optimal basis for muscle strength. This means that decreased upper extremity strength could not only be caused by RC tear, as well as the exact cause of the could be a change in the kinematic chain. The passive scapular stabilization position in the posterior tilting and the ER of the scapula minimizes the kinetic chain influences and allows the upper extremity muscles to maximize stable origin to produce maximum possible force. Upper extremity strength is improved by a passive scapular stabilization position. Therefore, it is necessary to increase the stability of the scapula to improve kinematic chain function at the start of rehabilitation.

Our study has some limitations. First, this study, the patient’s contralateral shoulder was considered healthy. Therefore, imaging modalities such as ultrasonography and MRIs were not performed to find occult damage in the non-RC repair shoulder. Although physical examination was performed to confirm RC tear, there may have been some subjects whose careful physical examination was not sufficient to determine the presence of RC tears. Second, in order to eliminate pain that may occur during maximal muscle strength, the muscle strength test was performed with less than the maximum effort, but bias due to pain during movement cannot be completely excluded, especially in the strength test 12 weeks after surgery. Thus, when measuring muscle strength in a clinical setting, care should be taken to the occurrence of patient pain.

Third, in this study, the dominant hand was not considered in the muscle strength test, and we did not evaluate the effect of arm dominance. However, the muscle strength test tried to similarly match the subject proportions of the dominant and non-dominant arms. Finally, since there was no preoperative measurement, it is difficult to determine whether the abnormal scapula pattern was caused by surgery or already deformed before surgery. However, since the purpose of this study was to investigate the effect on postoperative deformed scapula on the upper extremity muscle strength, there were no difficulties in interpreting the results.

Scapular dyskinesis is common in patients with shoulder injuries. Our study showed that patients with RC repair had a significant association with scapular dyskinesis. We also found that, if the scapula remained in an anterior tilting and internally rotated position after RC repair, secondary damage may occur to the RC unless the scapular kinematics was corrected. Decreased upper extremity strength is thought to be responsible for the supraspinatus tear, but the alteration in the kinematic chain may be the exact cause. The passive scapular stabilization position in the posterior tilting and the ER of the scapula minimizes the kinetic chain influences and allows the upper extremity muscles to maximize stable origin to produce maximum possible force. Upper extremity strength is improved by a passive scapular stabilization position; therefore, the first step in the rehabilitation is to provide a treatment that improves the stability of scapula.

None.

None to declare.

No potential conflicts of interest relevant to this article are reported.

Conceptualization: JO. Data curation: WJ. Formal analysis: JO. Investigation: WJ. Methodology: WJ. Project administration: DA, JO. Resources: WJ. Supervision: DA, JO. Validation: WJ. Visualization: WJ. Writing - original draft: WJ. Writing - review & editing: JO.