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Sci Rep
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Scientific Reports
2045-2322
Nature Publishing Group UK London

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10.1038/s41598-024-71331-4
Article
Innovative boxing training program outperforms the traditional scapular stabilization training program in post-stroke patients
http://orcid.org/0000-0001-8407-2287
Ersoy Ceren ceren.ersoy@outlook.com.tr

1
http://orcid.org/0000-0001-8346-9952
Iyigun Gozde 2
1 grid.510436.5 Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Final International University, North Cyprus Via Mersin 10, 99320 Kyrenia, Turkey
2 grid.461270.6 0000 0004 0595 6570 Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Eastern Mediterranean University, North Cyprus Via Mersin 10, Famagusta, Turkey
9 9 2024
9 9 2024
2024
14 2100110 3 2024
27 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Facilitating the restoration of upper limb functionality is a key objective of stroke rehabilitation. This study aimed to compare the effects of boxing and scapular stabilization training on scapular mobility, balance angle, muscle strength, motor function, and satisfaction in hemiparetic patients. A total of sixty patients were randomly assigned to one of three groups: the boxing group (BG; n = 20), the scapular stabilization group (SSG; n = 20), or the control group (CG; n = 20) which received no treatment at all. Each treatment group participated in three sessions per week for a total of eight weeks. The scapular mobility, balance angle (SBA), muscle strength, upper extremity motor functions (Manual Function Test-MFT), and treatment satisfaction were evaluated. The BG group showed greater improvements in the SBA (F = 59,951; p = 0.000; η2 = 0.682), mobility-frontal plane (F = 7998; p = 0.000; η2 = 0.222), mobility-sagittal plane (F = 91,632; p = 0.000; η2 = 0.766), and mobility-transverse plane (F = 48,713; p = 0.000; η2 = 0.635) than did the CG group. BG strengthened the serratus anterior (F = 42,227; p = 0.000; η2 = 0.601), while SSG strengthened the infraspinatus (F = 31,772; p = 0.000; η2 = 0.532) more than did CG. Compared with those in the SSG, supraspinatus (F = 52,589; p = 0.000; η2 = 0.653), upper trapezius (F = 42,890; p = 0.000; η2 = 0.605), anterior deltoideus (F = 30,844; p = 0.000; η2 = 0.524), latissimus dorsi (F = 84,345; p = 0.000; η2 = 0.751), MFTs (F = 52,363; p = 0.000; η2 = 0.652) and satisfaction (p = 0.008) were greater in the BG. Both approaches had a beneficial impact on the recovery process. However, boxing training was more effective than scapular stabilization training for several parameters. Clinical Trial Number: NCT05568173 date 5/10/2022.

Keywords

Boxing
Scapular mobility
Scapular stabilization exercise
Stroke
Upper extremity functions
Subject terms

Health occupations
Medical research
Neurology
issue-copyright-statement© Springer Nature Limited 2024
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pmcIntroduction

The prevalence of upper extremity impairment in hemiplegic individuals ranges from approximately 37–63%1. The initial stage observed in individuals experiencing a stroke is the flaccid phase, during which voluntary muscle control is absent. During the flaccid phase, significant modifications occur in the orientation of the glenoid fossa due to decreased muscular tone in the trapezius, serratus anterior, and rhomboid muscles. These changes lead to an augmented downward rotation of the scapula, leading to scapular depression and protraction2. During the following stage, the development of flexor spasticity in the upper extremity leads to scapular retraction, internal rotation, and adduction of the shoulder, as well as retraction and depression of the scapula3. The muscles exhibiting greater tone include the subscapularis and pectoral muscles4. In addition, the rhomboid, serratus anterior, deltoid, and middle and lower portions of the trapezius muscles are particularly prone to weakening5. The serratus anterior and lower trapezius muscles are crucial for stabilizing the scapulothoracic area6. The deltoid and rotator cuff muscles synergistically function as force couples to accomplish this task. Proper coupling involves the scapula’s upward rotation and posterior tilting, together with the external rotation of the humerus7. Decreased voluntary neural drive due to stroke may interfere with the timing and activation of the scapulothoracic and rotator cuff muscles8.

Scapular dyskinesia, which refers to alterations in the positioning and motion of the scapula, has a direct effect on the performance of the upper extremities7. While the distal portion of the upper extremity is in motion, the scapular muscles serve as proximal stabilizers. Several studies have investigated the effects of scapular stabilization exercises on various aspects of hemiplegia patient recovery after stroke. These studies have explored the impact of such exercises on paretic hand function and gait ability9, scapular position9,10, upper extremity function11,12, and dynamic standing position13.

In our previous study, we compared the impact of virtual and real boxing training on upper extremity function, balance, and cognitive skills in stroke patients. The findings revealed significant improvements in all measured parameters for both groups14. To the best of our knowledge, there is a dearth of research comparing the effects of scapular stabilization and boxing training on various parameters related to scapular, shoulder, and upper extremity functions among individuals with stroke. Therefore, this study aimed to compare the effects of boxing and scapular stabilization training on scapular mobility, balance angle, muscle strength, upper extremity motor function, and treatment satisfaction in hemiparetic individuals with stroke. The underlying hypothesis of this study was that stroke patients who participated in scapular stabilization training and boxing training would experience greater improvements in scapular mobility, scapular balance angle, scapular muscle strength, upper extremity motor functions, and treatment satisfaction compared to control group participants.

Methods

Ethical procedures

The research received ethical approval by Eastern Mediterrean University. The Board of Scientific Research and Publications of Eastern Mediterranean University approved the study by the decision number ETK00-2022-0181-date 30.06.22 and administered. All studies were conducted in accordance with relevant guidelines/regulations. Written informed consent was obtained from the volunteers prior to participation. The research was conducted in accordance with the Declaration of Helsinki.Clinical trial registration approval was obtained prior to the first patient enrollment. This study was registered at ClinicalTrials.gov (NCT05568173)-date 5.10.2022.

Participants

The study was designed as a prospective randomized controlled trial. Patients were recruited from Eastern Mediterrean University's Health Center Neurology Unit and those who were suitable based on the following inclusion and exclusion criteria were directed to the Eastern Mediterrean University Faculty of Physical Therapy and Rehabilitation. Patients diagnosed with stroke obtained from the hospital records and local community were screened for eligibility between October 2022 and September 2023. Randomization was done by an experienced researcher and physiotherapist (G.İ.). Clinical assessments and one-on-one treatment sessions were done by an experienced physiotherapist and researcher (C.E.). The inclusion criteria for this study were as follows: Patients with hemiparesis who have been diagnosed with their first stroke and have had at least 6 months after the diagnosis, between the ages of 40 and 70, with a Mini-Mental Test score ≥ 23, a functional level of < 4 on the Modified Rankin Scale, and upper extremity spasticity of < 2 on the Modified Ashworth Scale, as well as shoulder flexion of 120 degrees. Individuals were excluded from the study if they had any of the following criteria: uncontrolled hypertension, heart disease, subluxation and fracture in the shoulder, visual and hearing impairment, unilateral neglect, prior boxing experience, and botulinum toxin administration or surgical operation in the last six months14.

Interventions

The participants were randomly assigned to one of three groups: boxing training, scapular stabilization training, or a control group. The exercises were conducted three times per week for 8 weeks, with each session lasting 50 min. The boxing and scapular stabilization training group was provided with a 30-min session of boxing or scapular stabilization training a 10-min warm-up and a 10-min cool-down routine. The scapular stabilization and boxing training groups received training for 30 min three times per week over a period of 8 weeks.

Boxing training

Boxing training requires trunk stabilization, rotation, postural adjustments (i.e., dynamic weight transfer), bilateral upper extremity movement, and coordinated multidirectional lower extremity movement. The ability to recall the sequence of boxing motions requires a rapid selection of complex motor programs for movement, which entails integrating cognitive processes such as executive functions and attention skills14.

The physiotherapist, certified in boxing training, supervised modified boxing that progressively increased complexity. There were four distinct levels of difficulty. The protocol details for boxing training are presented in Table 1 and this link: https://m.youtube.com/watch?v=bn3Zn3nVAy8.Table 1 Boxing training protocol.

Level 1	0–2 weeks	30-s of right and left punches (high jab) with 1 min of rest were given unilaterally on a fixed boxing mat hanging on the wall

30-s of right and left punches (low jab) with 1-min rest were given unilaterally on a fixed boxing mat hanging on the wall

30-s of right and left punches (hook) with 1-min rest were given unilaterally on a fixed boxing mat hanging on the wall

	
Level 2	2–4 weeks	30-s right and left punches (high jab) with a 1-min rest were given unilaterally to the hand target glove held by the physiotherapist

30-s right and left uppercut were given with a 1-min rest

30-s right and left punches (hook) with a 1-min rest were given unilaterally to the target glove held by the physiotherapist

1 kg sandbag was tied to the wrist and 2 right and 2 left side jabs were repeated for 30-s and then a 1 min rest were given

1 kg sandbag was tied to the ankle, and trunk rotation and maximum hip flexion movements were repeated to the right and left sides for 30-s, and then a 1-min rest was given

	
Level 3	4–6 weeks	30-s of right and left punches (high jab) with 1 min of rest were given unilaterally on the boxing stand

30-s of right and left uppercuts with 1 min of rest were given unilaterally on the boxing stand

30-s of right and left punches (hook) with 1 min of rest were given unilaterally on the boxing stand

2 kg sandbag were tied to the wrist and 2 right and 2 left side jabs were repeated for 30-s and then a 1 min rest were given

2 kg sandbag were tied to the ankle, and trunk rotation and maximum hip flexion movements were repeated to the right and left sides for 30-s, and then a 1-min rest was given

	
Level 4	6–8 weeks	30-s of mixed bilateral punches (low jab), 1 right, 2 left, 2 right, 1 left were given to be thrown into the physiotherapist's glove, and trunk rotation, and then a 1-min rest were given

30-s of mixed bilateral punches (low jab), 1 right, 2 left, 2 right, 1 left were given to be thrown into the physiotherapist's body cushion and then a 1-min rest was given

30-s of 4 right side punches (hooks), 4 left side punches (hooks) were given to be thrown on the physiotherapist's body cushion, and then a 1-min rest was given

30-s of a left uppercut to be thrown to the physiotherapist's trunk cushion and then to his left glove, followed by a right uppercut to be thrown to the trunk cushion and right glove, and then a 1-min rest was given

2 kg sandbag were tied to the wrist and 2-kg sandbag were tied to the ankle, and 2 right and 2 left side punches, as well as trunk rotation and maximum hip flexion movement, were repeated on the right and left side for 30-s, and then a 1-min rest were given

	

Scapular stabilization training

Shoulder stabilization exercises are intended to restore a balanced control ability between shoulder stabilizers. In stroke patients, progressive exercises focusing on scapular stabilization, consisting of closed and open kinetic chain exercises to prevent strength imbalance in the muscles surrounding the scapula, can improve upper extremity functions and trunk balance9,15.

There were four distinct levels of difficulty. The protocol details for scapular stabilization training are presented in Table 2 and this link: https://www.youtube.com/watch?v=aZzf7noIjEg.Table 2 Scapular stabilization training protocol.

Level 1	0–2 weeks	Rolling a small soft ball with palms in different directions on the wall in elbow extension shoulder 90 degree flexion position for 30 s and scapular clock exercise, and then a 1 min rest was given

Obstacle crossing exercise from a 4 cm single obstacle in the sitting position with elbow extension for 30 s, and then a 1 min rest was given

Wall sliding exercise with yellow theraband on the wall for 30 s with forearms in pronation shoulder 90° flexion position and bilateral scapular retraction with elbow flexion to extension, and then a 1-min rest was given

Push-up exercise on the wall at the level of 120° shoulder flexion for 30 s, and then a 1-min rest was given

Trunk rotation and maximum hip flexion movement were repeated for 30 s, one to the right and one to the left, and then a 1-min rest was given

	
Level 2	2–4 weeks	Rolling a small hard ball with palms in different directions in elbow extension position, shoulder 90° flexion position on the wall for 30 s and scapular clock exercise, and then a 1-min rest was given

Obstacle crossing exercise from two 4 cm obstacles in the sitting position with elbow extension for 30 s, and then a 1-min rest was given

Wall sliding exercise with red theraband on the wall for 30 s with the forearms in pronation shoulder 90° flexion position and bilateral scapular retraction with elbow flexion to extension, and then a 1-min rest was given

Push-up exercise on the wall at the level of 90° shoulder flexion for 30 s, and then a 1-min rest was given

1 kg sandbag was tied to the wrist and 2 right and 2 left side jabs were repeated for 30-s and then a 1-min rest were given

1 kg sandbag was tied to the ankle, and trunk rotation and maximum hip flexion movements were repeated to the right and left sides for 30-s, and then a 1-min rest was given

	
Level 3	4–6 weeks	Rolling a small soft ball weighing 0.5 kg with palms in different directions in elbow extension, shoulder 90° flexion position on the wall for 30 s and scapular clock exercise, and then a 1-min rest was given

Obstacle crossing exercise from a 7 cm single obstacle in the prone position with elbow extension for 30 s, and then a 1-min rest was given

Wall sliding exercise with green theraband on the wall for 30 s, with forearms in pronation shoulder 90° flexion position, bilateral scapular retraction and elbow flexion to extension, and then a 1-min rest was given

Push-up exercise on the table for 30 s with the body in 60° flexion, and then a 1-min rest was given

2 kg sandbag were tied to the wrist and 2 right and 2 left side jabs were repeated for 30-s and then a 1-min rest was given

2 kg sandbag were tied to the ankle, and trunk rotation and maximum hip flexion movements were repeated to the right and left sides for 30-s, and then a 1-min rest was given

	
Level 4	6–8 weeks	Rolling a small hard ball weighing 0.5 kg with palms in different directions in elbow extension, shoulder 90° flexion position on the wall for 30 s and scapular clock exercise, and then a 1-min rest were given

Obstacle crossing exercise from a 7 cm single obstacle in the prone position with elbow extension for 30 s, and then a 1-min rest was given

Wall sliding exercise with blue theraband on the wall for 30 s with forearms in pronation, shoulder 90° flexion position and bilateral scapular retraction with elbow flexion to extension, and then a 1-min rest was given

Push-up exercise on the table for 30 s on the floor and then a 1-min rest were given

2 kg sandbag were tied to the wrist and 2-kg sandbag were tied to the ankle, and

2 right and 2 left side punches, as well as trunk rotation and maximum hip flexion movement were repeated on the right and left side for 30-s, and then a 1-min rest was given

	

Control group

The control group participants were not administered any form of intervention or therapy. Assessments were conducted at baseline and after 8 weeks. The control group was informed that a treatment program could be administered at the conclusion of the evaluation period upon their request.

Outcome measures

The sociodemographic data [age, sex, body mass index, and dominant side], disease-related data [time since stroke and side of hemiparesis] and the presence of scapular dyskinesia were recorded. The primary outcome measure of this research was scapular mobility, and the secondary outcome measures were the scapular balance angle, scapular muscle strength, upper extremity motor function and treatment satisfaction. The outcome measures were assessed at baseline (0 weeks) and after treatment completion (8 weeks). Assessments were conducted over two separate days to mitigate fatigue.

Primary outcome measures

Scapular mobility: Upwards and downwards rotation in the scapular plane, anterior and posterior tilt in the sagittal plane, and internal and external rotation in the transverse plane were measured by using a digital goniometer (Meloq EasyAngle®). Clinical measurements using an electric goniometer were recorded during upper extremity elevation in the frontal, transverse and sagittal planes. For each anatomical plane, the calibration technique and specific position of the electric goniometer based on various scapular landmarks followed the standard procedure of a validity and reliability study previously conducted with the easy angle goniometer16. The examiner recorded the clinical measurements made with the electric goniometer during the elevation of the upper extremity in the frontal, transverse, and sagittal planes. The calibration technique and specific location for the electric goniometer in each anatomical plane were determined by a standard procedure that was based on multiple scapular landmarks. The electric goniometer was calibrated to the floor directly beneath participants to represent 0° in order to measure scapular motion in the frontal plane. The electric goniometer was positioned on the scapular spine at a distance of one-third of the distance between the root of the scapular spine and the posterior acromial angle, as measured and marked using a cloth tape measure and oriented posteriorly. The electric goniometer was calibrated by placing a perpendicular edge of a floor tile beneath participants to represent 0° in order to measure scapular motion in the transverse plane. The electric goniometer was positioned at the same location on the scapular spine as described for frontal-plane motion, but it was oriented superiorly. The electric goniometer was calibrated to the vertical I-beam square level to represent 0° in order to record scapular motion in the sagittal plane. The goniometer was positioned on the most prominent portion of the medial scapular border and oriented laterally(Fig. 1).Fig. 1 (A) Identification of one-third of the distance between the root of the scapular spine and the posterior acromial angle. Orientation of the electric goniometer (EasyAngle; Meloq AB) for measuring scapular motion in the (B) frontal plane; (C) transverse plane; and (D) sagittal plane, with inset illustrating calibration in the sagittal plane.

All participants began each trial by sitting on a 35 cm high stool in an upright position with their feet flat on the floor. Upper extremity elevation movement was explained and demonstrated. They were able to practice the movement several times and ask questions before collecting data. To begin each trial, the researcher applied the electric goniometer to the designated scapula point and instructed the participant to assume an upright and comfortable sitting position. The scapular rest position was recorded and the participant was then asked to perform the desired condition. After completing the active movement, the subject maintained the final position for several seconds, during which the examiner measured the scapular tip position. Total excursion values ​​were calculated by subtracting the initial scapular position (rest) from the final scapular position (end) after the movement was completed (Fig. 2). While measuring the scapular positions, the arm lifting range was controlled with the electronic goniometer. Three trials of active upper extremity elevation were recorded for each scapular condition, for a total of 9 trials for data collection purposes. Constant pressure and contact with the scapular landmark were maintained during each movement. The order of the anatomical planes was randomly selected before testing.Fig. 2 Measurement of scapular motion in the frontal plane during upper extremity elevation to 120° in the scapular plane.

Clinical measurements of scapular motion were interpreted following the guidelines of the International Society of Biomechanics: positive scapular motion in the frontal, transverse, and sagittal planes was defined as downward rotation, internal rotation, and posterior tilt, respectively17. Intersession evaluator reliability was found to be moderate to good (Intraclass Correlation Coefficient I—ICC2,3 range = 0.628–0.874), and in-session interpreter reliability was determined to be moderate to excellent (ICC2,3 range = 0.545–0.912)18.

Secondary outcome measures

Scapular balance angle measurement: Bilateral markings were made to show the scapula’s lower angle, and a line was drawn connecting these markings. In addition, the SBA was recorded by measuring the angles formed by the vertical line between the spinous processes of C7 and T9–T10 and the line connecting the lower angles of the scapula to the vertical line passing through the spine using a goniometer. In healthy subjects, the scapular balance angle was 2.505 ± 2.340°, while in abnormal patients, the angle was greater than 7.185°. The intraobserver and interobserver ICCs reported were 0.87 and 0.84, respectively19.

Shoulder and scapular muscle strength: The isometric muscular strength of the supraspinatus, upper trapezius, infraspinatus, serratus anterior, latissimus dorsi, and anterior deltoid muscles was measured using a hand-held dynamometer (HHD). For upper trapezius muscle strength measurement, the patient sat down and resistance was applied with the dynamometer over the upper scapula and the patient was asked to lift his shoulder against the resistance. Supraspinatus, anterior deltoid, and latissimus dorsi muscle strengths were evaluated in the sitting position. The subject lifted the arm halfway between flexion and abduction (30° anterior to the coronal plane) for the supraspinatus and 90° flexion for the anterior deltoid. Resistance was applied over the elbow. The serratus anterior muscle strength test was evaluated in the supine position with 90° flexion. Resistance was applied to the ulna along the humeral axis. To measure latissimus dorsi muscle strength, the elbow was placed in 90° flexion and the shoulder in 30° extension. Resistance was applied from the back of the upper arm, above the elbow. Three attempts were made for each muscle, separated by 30 s of a rest period20,21

Upper-extremity motor function: The Manual Function Test (MFT) consists of 8 sections and 32 items that measure arm movements and manipulative activities. A validity and reliability study of the scale in stroke patients was conducted22. The test–retest reliability coefficient and interrater reliability of the MFT were consistently found to be above 0.95. The Cronbach’s α coefficient for the internal consistency of the eight items was 0.9523

Treatment satisfaction: Treatment satisfaction was measured after boxing and scapular stabilization training with a visual analog scale (VAS). The VAS for satisfaction is a horizontal line 100 mm long. At the beginning and the end, two descriptors represent extremes of satisfaction (i.e., no satisfaction and extreme satisfaction). The exact question was “How satisfied were you with the treatment you received?”24,25.

Sample size calculation and randomization

The sample size was calculated by using the G*Power 3.1.9.2 program. The mean and standard deviation data were obtained from the study conducted by Kim et al.9. There was a statistically significant difference in the manual function test results between the groups, with an effect size of d = 1.687. In this study, high variation was expected in the manual function test between groups, and the effect size of the F value was taken as d = 0.59. Accordingly, the sample size required for 95% (1 − β = 0.95) power at the α = 0.05 level was 51 individuals. Nevertheless, considering that the number of dropouts increased by 20%, 60 individuals were planned to be included. Therefore, 20 subjects were enrolled in each group based on the power calculation. A total of 88 patients were screened, among whom 60 met the inclusion criteria and underwent randomization, as shown in the CONSORT flow diagram (Fig. 3). This study was a randomized controlled trial. Participants were randomly assigned to one of three groups using the block randomization method: 20 individuals in the boxing training group, 20 individuals in the scapular stabilization training group, and 20 individuals in the control group.Fig. 3 Study protocol (CONSORT diagram).

Statistical analysis

The statistical analysis was carried out using the statistical package SPSS version 26.0. The variables are reported as percentages (%) and means ± standard deviations (x ± sd). The chi-square test was used to compare the demographic characteristics and posttreatment pain conditions of the participants according to their groups. Analysis of covariance (ANCOVA) was performed to examine the effect of treatment according to the groups. A pretest–posttest design was used where the dependent variable was the posttest, and the pretest was used as a covariate, not an outcome. p < 0.05 was accepted as the statistically significant level. The arithmetic means are presented with a 95% confidence interval (95% CI) with lower and upper limit values. Both “p” values and 95% CI values were considered while interpreting the differences between the groups. Eta-squared (η2) calculations were used to calculate the effect sizes, and the guidelines proposed by Cohen were used to interpret the results26. The effect sizes are interpreted as follows: small (η2 = 0.01), medium (η2 = 0.06), and large (η2 = 0.14) effects26

Results

The numbers of subjects screened, enrolled, randomized, and completing thetrial are shown in Fig. 1. A total of 88 patients were screened, among whom 60 met the inclusion criteria and underwent randomization, as shown in the CONSORT flow diagram (Fig. 1). Table 3 shows the distribution of participants according to their sociodemographic and clinical characteristics. There was no difference between the BG, SSG, and CG in terms of sociodemographic or clinical features before treatment (p > 0.05). The posttreatment pain intensity scores of participants who received boxing training were lower than those of patients who received scapular stabilization training (p < 0.05).Table 3 Sociodemographic and clinical characteristics of the participants.

	BG (n = 20)	SSG (n = 20)	CG (n = 20)	X2	p-value	
n	%	n	%	n	%		
Age (years)	
 55 years ≥ 	10	50	8	40	9	45			
 56–65 years	5	25	7	35	6	30		
 66 years ≤ 	5	25	5	25	5	25		
Mean ± SD	57.50 ± 8.92	57.85 ± 9.02	57.75 ± 9.50	0.014	0.993	
Sex	
 Female	6	30.0	7	35.0	7	35.0	0.150	0.928	
 Male	14	70.0	13	65.0	13	65.0	
Time since stroke (months)	
 Mean ± SD	27.90 ± 9.72	28.40 ± 10.41	26.70 ± 9.50	0.156	0.856	
Paretic side extremity	
 Right	10	50.0	9	45.0	10	50.0	0.133	0.935	
 Left	10	50.0	11	55.0	10	50.0	
Dominant extremity	
 Right	15	75.0	16	80.0	17	85.0	a	a	
 Left	5	25.0	4	20.0	3	15.0	
Shoulder pain after treatment	
 Exist	10	50.0	6	30.0		1.667	0.197	
 Does not exist	10	50.0	14	70.0		
Posttreatment pain characteristics	
 Stable	4	40.0	7	50		a	a	
 Progressive	1	10.0	1	7.1		
 Improvement	5	50.0	6	42.9		
Post treatment type	
 Sharp	2	20.0	9	64.3		b	0.047	
 Vague	8	80.0	5	35.7		
Shoulder pain severity after treatment	
 Mild	8	80.0	5	35.7		b	0.047	
 Moderate	2	20.0	9	64.3		
Posttreatment shoulder pain increased with movement?	
 Yes	9	90.0	13	92.9		b	1.000	
 No	1	10.0	1	7.1		
Posttreatment pain VAS	
 Mean ± SD	2.80 ± 2.04	4.71 ± 1.07		− 2.265	0.024	
BG Boxing group, SSG scapular stabilization group, CG control group, a: Pearson chi-square test assumptions could not be met; b: Fisher’s exact chi-square test.

Results of the primary outcome

There was a statistically significant difference with a large effect size between the pretest and posttest measurements for scapular mobility in the frontal plane (F = 7,998, p = 0,001), sagittal plane (F = 91,632, p = 0,000), and transverse plane (F = 48,713, p = 0,000). According to these results, there was a difference in shoulder mobility between the BG and CG (p < 0.05), while there was no difference between the BG and SSG or between the SSG and CG. The BG had the greatest difference in scapular mobility, with a decrease of 7.45% in the frontal plane, 7.85% in the sagittal plane, and an increase of 9.20% in the transverse plane.

The results of secondary outcomes

Table 4 shows comparisons of scapular mobility, balance angle, and manual function test results within and between the three groups (BG, SSG and CG). A statistically significant difference existed between the pretest and posttest measures for the SBA tests, with a large effect size (F = 59,951, p = 0.000). A significant difference in SBA was observed between the BG and CG (p < 0.05), whereas no such difference was observed between the BG and SSG or between the SSG and CG. Moreover, BG experienced the greatest decline in SBA (− 2.12%).Table 4 Comparisons of scapular mobility, balance angle, and manual function test results within and between the three groups (BG, SSG and CG).

		Before treatment
x¯±sd
(95% CI)	After treatment
x¯±sd
(95% CI)	∆ (%)	F	p-valuea	η2	Differences	
Scapular mobility

Frontal planea

	BG	− 17.95 ± 4.97

(20.13 to − 15.77)

	− 25.40 ± 11.59

(− 30.48 to − 20.32)

	− 7.45	7.998	0.001†	0.222	BG vs CG	
SSG	− 18.45 ± 4.59

(5.86 to 7.54)

	− 25.35 ± 4.86

(4.75 to 5.84)

	− 6.90					
CG	− 19.70 ± 3.64

(6.63 ± 2.07)

	− 19.60 ± 3.25

(5.76 to 7.6)

	− 6.15					
Scapular mobility

Sagittal planeb

	BG	− 3.65 ± 2.87

(− 20.13 to − 15.77)

	− 11.50 ± 1.57

(− 30.48 to − 20.32)

	− 7.85	91.632	0.000†	0.766	BG vs CG	
SSG	− 4.05 ± 4.22

(− 20.46 to − 16.44)

	− 10.05 ± 3.03

(− 27.48 to − 23.22)

	− 6.00					
CG	− 4.45 ± 4.52

(− 21.3 to − 18.1)

	− 5.10 ± 4.33

(− 21.03 to − 18.18)

	− 5.65					
Scapular mobility

Transverse planec

	BG	12.70 ± 4.81

(− 4.91 to − 2.39)

	21.90 ± 3.60

(− 12.19 to − 10.81)

	9.20	48.713	0.000†	0.635	BG vs CG	
SSG	12.25 ± 4.35

(− 5..9 to − 2.2)

	20.15 ± 3.62

(− 11.38 to − 8.72)

	7.90					
CG	14.2 ± 5.18

(− 6.43 to − 2.47)

	14.80 ± 4.98

(− 7 to − 3.2)

	6.80					
SBA	BG	6.00 ± 1.70

(5.25 to 6.74)

	3.88 ± 0.94

(3.46 to 4.29)

	− 2.12	59.951	0.000†	0.682	BG vs CG	
SSG	6.70 ± 1.92

(5.86 to 7.54)

	5.29 ± 1.25

(4.75 to 5.84)

	− 1.41					
CG	6.63 ± 2.07

(5.72 to 7.54)

	6.68 ± 2.10

(5.76 to 7.6)

	− 1.15					
MFT (score)	BG	26.2 ± 3.02

(24.88 to 27.52)

	28.55 ± 2.70

(27.37 to 29.74)

	2.35	52.363	0.000†	0.652	BG vs SSG

BG vs CG

SSG vs CG

	
SSG	24.7 ± 2.45

(23.63 to 25.77)

	25.80 ± 2.84

(24.56 to 27.04)

	1.10					
CG	26.65 ± 2.60

(25.51 to 27.79)

	26.55 ± 2.58

(25.42 to 27.68)

	− 0.1					
Treatment satisfaction	BG		8.25 ± 1.16			0.008†			
SSG		7.00 ± 1.62						
aPositive values indicate downwards rotation; bPositive values indicate internal rotation; cPositive values indicate posterior tilt; BG Boxing Group, SSG Scapular Stabilization Group, CT Control Group, η2 Eta Coefficient test; Values are means (SD); †P < 0.05: Significant difference between groups; SBA Scapular Balance Angle, MFT Manual function test.

Table 5 shows comparison of scapular muscle strength within and between the three groups (BG, SSG and CG).Table 5 Comparison of scapular muscle strength within and between the three groups (BG, SSG and CG).

		Before Treatment
x¯±sd
(95% CI)	After Treatment
x¯±sd
(95% CI)	∆ (%)	F	p-valuea	η2	Differences	
Supraspinatus	BG	8.60 ± 3.76

(6.95–10.24)

	13.51 ± 4.39

(11.58–15.43)

	4.91	52.589	0.000†	0.653	BG vs SSG

SSG vs CG

BG vs CG

	
SSG	6.84 ± 2.57

(5.72–7.97)

	9.24 ± 2.81

(8.01–10.47)

	2.40					
CG	6.12 ± 3.03

(4.79–7.44)

	6.76 ± 2.89

(5.49–8.02)

	0.64					
Upper Trapezius	BG	7.80 ± 2.72

(6.61–8.99)

	13.16 ± 3.40

(11.67–14.65)

	5.36	42.890	0.000†	0.605	BG vs SSG

SSG vs CG

BG vs CG

	
SSG	6.34 ± 2.70

(5.16–7.52)

	9.36 ± 3.45

(7.84–10.87)

	3.02					
CG	5.36 ± 2.99

(4.04–6.67)

	6.65 ± 3.31

(5.2–8.1)

	1.29					
Anterior Deltoideus	BG	9.08 ± 3.80

(7.42–10.75)

	13.92 ± 4,77

(11.83–16.01)

	4.84	30.844	0.000†	0.524	BG vs SSG

SSG vs CG

BG vs CG

	
SSG	7.55 ± 3.38

(6.07–9.03)

	10.64 ± 4.08

(8.85–12.43)

	3.10					
CG	5.76 ± 2.60

(4.62–6.9)

	6.69 ± 2.41

(5.63–7.74)

	0.92					
Serratus

Anterior

	BG	7.54 ± 2.82

(6.3–8.77)

	12.89 ± 3.31

(11.44–14.33)

	5.35	42.227	0.000†	0.601	BG vs CG	
SSG	7.74 ± 2.96

(6.44–9.04)

	10.63 ± 3,36

(9.15–12.1)

	2.89					
CG	6.25 ± 2.49

(5.15–7.34)

	7.63 ± 2.67

(6.45–8.8)

	1.38					
Infraspinatus	BG	6.30 ± 2.20

(5.33–7.26)

	8.99 ± 2.36

(7.95–10.02)

	2.69	31.772	0.000†	0.532	SSG vs CG	
SSG	6.49 ± 1.60

(5.78–7.19)

	9.79 ± 1.60

(9.09–10.49)

	3.30					
CG	6.22 ± 1.25

(5.67–6.77)

	7.45 ± 1.43

(6.82–8.07)

	1.23					
Latissimus

Dorsi

	BG	8.08 ± 2.13

(7.15–9.01)

	12.26 ± 2.08

(11.35–13.17)

	4.18	84.345	0.000†	0.751	BG vs SSG

SSG vs CG

BG vs CG

	
SSG	8.64 ± 1.94

(7.79–9.48)

	10.95 ± 1.98

(10.08–11.82)

	2.32					
CG	8.46 ± 2.13

(7.52–9.39)

	9.37 ± 2.24

(8.39–10.35)

	0.915					
BG Boxing Group, SSG Scapular Stabilization Group, CT Control Group, η2 Eta coefficient test, Values are means (SD); †P < 0.05: Significant difference between groups.

In the muscle strength test, there was a statistically significant difference with a large effect size between the pre- and posttest measurement times for the following paretic side muscles: supraspinatus (F = 52,589, p = 0.000), upper trapezius (F = 42,890, p = 0.000), anterior deltoideus (F = 30,844, p = 0.000), serratus anterior (F = 42,227, p = 0.000), infraspinatus (F = 31,772, p = 0.000), and latissimus dorsi (F = 84,345, p = 0.000). According to these results, there was a difference in the strength of the supraspinatus, upper trapezius, and anterior deltoideus muscles between the BG and the SSG, with greater gains in the strength of the hemiparetic side supraspinatus (4.91%), upper trapezius (5.36%), anterior deltoideus (4.84%) and latissimus dorsi (4.18%) muscles in the BG. Furthermore, differences in serratus anterior muscle strength were detected between the BG and CG (BG: 4.91% increase), and differences in infraspinatus muscle strength were detected between the SSG and CG (SSG: 3.30% increase).

The difference between the pretest and posttest measurement times for the MFTs of the participants was statistically significant, with a large effect size (F = 52,363, p = 0.000). A statistically significant difference was observed in the MFTs between the BG and SSG groups (p < 0.05); the BG group exhibited the greatest increase in MFTs (2.35%).

The difference between the treatment satisfaction (VAS) scores of the participants in the BG and SSG was statistically significant (p < 0.05). The satisfaction (VAS) scores in the BG were greater than those in the SSG.

Discussion

This study aimed to compare the effects of boxing and scapular stabilization training on scapular mobility, the balance angle, shoulder and scapular muscle strength, upper extremity motor functions and treatment satisfaction in hemiparetic individuals with stroke. The study showed that boxing and scapular stabilization training improved all these parameters. Compared to scapular stabilization training, boxing training was more effective in increasing motor functions of the upper extremities and strengthening the supraspinatus, upper trapezius, anterior deltoideus, and latissimus dorsi muscles. Furthermore, boxing training was more effective for improving scapular mobility and balance angle than receiving no treatment at all. Boxing training was more effective in improving the strength of the serratus anterior muscle, whereas scapular stabilization training was shown to be more effective in increasing the strength of the infraspinatus muscle compared to receiving no treatment. The study findings supported our hypothesis that both treatment groups would achieve superior outcomes compared to the control group for many parameters. Additionally, the results suggested that boxing training was more effective than scapular stability training in improving several parameters, including upper extremity motor functions and muscle strengthening.

Poststroke, muscle weakness, and motor coordination deficits can disrupt the typical positioning and motions of the scapula. During arm elevation, scapular internal rotation, upwards rotation, and posterior tilting are all observed in healthy individuals27. The angle of scapular upwards rotation reflects the strength of the trapezius, serratus anterior, and supraspinatus. Poststroke individuals have been shown to have increased scapular upwards rotation with elevation of the paretic arm compared to healthy controls28. In contrast, Lixandrao et al. demonstrated that individuals with chronic stroke showed increased bilateral scapular internal rotation and anterior tilt and increased and decreased arm elevation in comparison to healthy individuals29. Furthermore, scapular internal rotation and anterior tilt may be exacerbated by increased muscle tone in the muscles involved in the anterior tilt of the scapula (i.e., rhomboid, levator scapulae, and pectoralis minor)30 and reduced muscle strength in the muscles involved in upwards rotation, posterior tilt, and external rotation of the scapula (i.e., the serratus anterior, middle trapezius, and lower trapezius)31

Although several studies10,32,33 have examined the effects of scapular stabilization exercises on the scapula in stroke patients, none of these studies have investigated scapular mobility. While some studies conducted on nonstroke populations have suggested that scapular stabilization exercises do not affect scapular mobility, others have shown that these exercises do lead to improvements in scapular kinematics, specifically in terms of external rotation, posterior tilt, and upwards rotation34,35. No prior research in the literature has investigated the efficacy of boxing training in improving scapular mobility in stroke patients. In the present study, improvements were observed in the upwards rotation, external rotation, and posterior tilt of the scapula with shoulder elevation in both training groups. The relationship between the trapezius–serratus force couple and scapulothoracic stability in the two training groups might influence this outcome. The BG had the greatest difference in scapular mobility, with improvements in upwards rotation (7.45%), external rotation (7.85%), and posterior tilt (9.20%). However, there was a significant difference in shoulder mobility between the BG and CG. The enhanced muscular strength in the serratus anterior and trapezius muscles may account for the more pronounced enhancement in scapular mobility observed in the BG than in the CG.

This scapular imbalance can be attributed to a weakening of the serratus anterior and lower trapezius36, as well as increased muscular tone in the rhomboids, levator scapula, pectoralis minor, and latissimus dorsi37, which causes scapular downwards rotation. A number of studies examining the impact of different scapular strengthening programs on the scapular position in stroke patients have concluded that the exercise program contributed to an improvement in scapular position32,33,38,39. Awad et al. reported that the incorporation of scapular strengthening exercises in shoulder strengthening programs for stroke patients resulted in a significant increase in the angle of scapular upwards rotation and a significant decrease in the angle of spinal lateral deviation. The study also demonstrated that the peak force of the trapezius, serratus anterior, and supraspinatus muscles is related to the upwards scapular rotation angle and is negatively correlated with the spinal lateral deviation angle15.

In this study, the scapular imbalance was effectively reduced with both boxing training and scapular stabilization training, as evidenced by the decrease in the SBA observed in both groups. The BG (− 2.12%) had a greater decline in SBA than did the SSG (− 1.41). However, there was a significant difference in the SBA only between the BG and CG. All three groups were initially not suspected of having scapular dyskinesia based on the specified cut-off values19; however, after treatment, only the patients in the BG had a reduction in their SBA angle to below 5°. The observed greater enhancement in preposttreatment SBA values in the BG group may be attributed to the fact that boxing training specifically improves the upwards rotator muscles, as demonstrated in the study conducted by Awad et al. In the aforementioned study, it was found that incorporating scapular strengthening exercises into shoulder strengthening programs for stroke patients resulted in significant improvements in muscular strength for the trapezius, serratus anterior, and supraspinatus muscles. However, the group that performed scapular strengthening exercises showed a particularly significant increase in peak forces for all three muscles15. The scapular balance angle and scapular mobility improved consistently in both the scapular stabilization and boxing training groups. The enhancement reported in both measures may have occurred simultaneously with the improvement in scapular muscular strength.

There has been no previous research examining the effectiveness of boxing training on scapular muscle strength in stroke patients. However, it is known that the serratus anterior, together with external and internal oblique rhomboids, shows a “serape effect” to produce rotational force while punching. Additionally, the serratus anterior muscle has myofascial connections with the latissimus dorsi and indirect connections with the gluteus maximus muscles via the thoracolumbar fascia40. As a result, engaging in boxing activities may activate all of the aforementioned muscles.

The results of the present research showed that compared with the CG, the BG significantly improved the strength of the supraspinatus, upper trapezius, anterior deltoideus, and latissimus dorsi muscles. In contrast, the infraspinatus muscle strength in the SSG was significantly greater than that in the CG. Boxing training requires rotational movements of the trunk, which leads to the activation of additional muscles, particularly the serratus anterior and latissimus dorsi, resulting in the serape effect. While the exercises provided in the SSG did not specifically focus on the rotator cuff muscles, the significant improvement in infraspinatus muscular strength in this group can be attributed to the closed kinetic chain nature of the scapular stabilization exercises.

Proper scapula alignment is essential for generating powerful arm movement5,41. Changes in the scapular orientation of paretic arms may result from a force imbalance in the scapular muscles, exacerbated by the weakness of the scapular stabilizers8. Numerous studies have shown that scapular stabilization of the extremities improves upper extremity functions in stroke patients9,10,12,42. In a systematic review by Sánchez-Lastra et al., in which they investigated the effects of adapted boxing training on people with different health problems, it was determined that adapted boxing training led to improvements in upper extremity motor function43. Park et al. found that a sitting boxing program was effective in the recovery of upper extremity functions in stroke patients43. In our previous research, we compared the impact of virtual and real boxing training on the upper extremities of stroke patients. The results indicated that both virtual and real boxing training were successful in enhancing upper extremity functions14. The present study revealed a statistically significant difference between the BG and the SSG on the upper extremity function test, with the BG demonstrating a more significant increase in MFTs (2.35%) than the SSG (1.10%).

The results of this study demonstrated a notable improvement in dynamic stabilizer muscle strength after boxing training compared to scapular stability training. It was found that boxing training resulted in greater strength improvement in several muscles, including the supraspinatus, upper trapezius, anterior deltoideus, latissimus dorsi, and serratus anterior muscles, but not in the infraspinatus muscle. At the nervous system level, large amounts of repetition can strengthen connections between neurons and trigger restructuring in areas of the cerebral cortex corresponding to the affected limb, thus improving motor function44. This may be a contributing factor to the greater improvement in upper extremity functions observed in the boxing training group. An alternative explanation for our results is that boxing training facilitates the development of anticipatory postural adjustments (APAs). APAs allow for distal motion while providing proximal stability45. Research has demonstrated that anticipatory postural control may be enhanced by boxing training46,47. Therefore, boxing training will likely lead to greater enhancements in upper extremity functional skills and more significant alterations in neural plasticity than basic and repeated upper extremity exercise training, such as scapular stabilization training.

The treatment satisfaction scores of those receiving boxing training were greater than those of participants receiving scapular stabilization training. The unique, playful nature of boxing training may be useful in increasing individuals' motivation to perform therapeutic tasks48,49. Again, having different levels of difficulty during therapy and providing appropriate levels of difficulty to meet the needs of different patients can help them avoid boredom or frustration during therapy. Linking positive feedback from the physical therapist to improved or successful therapeutic task performance may also motivate and satisfy individuals to participate in rehabilitation50.

This study had some limitations that should be considered. There are several factors that contribute to the limitations that may be inferred from the results of this study. Upon analyzing the results about post-treatment pain, it becomes evident that a greater number of individuals in the SSG experience pain. Additionally, the participants reported that the pain in the SSG was more severe and increased with movement. Based on these information, the major limitation of this study is the absence of pain assessment before the treatment. Hence, the likelihood of a greater number of individuals in the SSG experiencing pain prior to therapy may result in the interpretations being ambiguous. If we assume that the levels of pain were the same in both groups before to therapy, we may explain it as follows: As a result of the stroke, certain muscles experience weakening while others may become hypertonic. Consequently, the implementation of scapular stabilization exercises may have led to the strengthening of the weak muscles while simultaneously increasing the tone of the hypertonic muscles. The dysfunction in force couples may have caused an increase in post-treatment pain. Further studies may incorporate muscle tone measurement into the outcome measures, considering its influence on the kinematics and functions of the scapula. Moreover, incorrect alignment might potentially alter the traction angle of the muscles, thereby exacerbating pain after the treatment in the SSG. Another potential limitation of this study is that the study specifically excludes individuals with acute and subacute stroke, as well as those with severely impaired upper extremity functions and inability to stand (Brunnstrom level 1–5). Therefore, care should be taken when generalizing the results of this study to all stroke patients. A single physiotherapist (CE) conducted all assessments and treatments. One of the other limitations of this study is that the investigator responsible for administering the assessment and intervention program was unable to maintain blinding to allocation due to the inherent characteristics of the interventions. Another limitation of the study is the lack of long-term follow-up and the inability to monitor the duration of the improvements. Validity and reliability studies of all measurements used in the study have been conducted in previous studies, and test–retest reliability coefficient and inter-rater reliability values ​​are presented in the text. The validity and reliability of all outcome measures used in this study have been established in previous research. We included all psychometric data for our outcome measures accordingly. We did not collect inter-rater or inter-rater reliability data. We believe this is a limitation of our study. Nevertheless, the sole physiotherapist (CE) responsible for conducting all the measurements is an experienced practitioner who has consistently applied the evaluation criteria on stroke patients over an extended period of time. Hence, we believe that the discrepancy between measurements is minimal.

Conclusion

The study showed that boxing and scapular stabilization training improved all these parameters. Compared to scapular stabilization training, boxing training was more effective in increasing motor functions of the upper extremities and muscle strengthening (i.e., supraspinatus, upper trapezius, anterior deltoideus, and latissimus dorsi). Furthermore, boxing training was more effective for improving scapular mobility and the scapular balance angle than receiving no treatment at all. Compared with no treatment, boxing training was more effective at improving the strength of the serratus anterior muscle, whereas scapular stabilization training was more effective at increasing the strength of the infraspinatus muscle. The results showed that boxing training outperformed scapular stabilization exercises in terms of various parameters, suggesting that it could be a new alternative rehabilitation method that better suits the unique needs of people with chronic stroke. Nevertheless, both methods contributed positively to the rehabilitation process.

Author contributions

Conceptualization: C.E. and G.İ.; methodology: C.E. and G.İ.; writing—original draft preparation: C.E.; writing—review and editing: G.İ.; supervision: G.İ. Consent will be obtained from the participants.

Funding

This research did not receive funding from public, commercial, or not-for-profit agencies.

Data availability

The datasets generated and/or analysed during the current study are not publicly available due the data are confidential since the participants of this study were informed upon admission to the hospital that the data would remain confidential and would not be shared with third parties but are available from the corresponding author on reasonable request.

Competing interests

The authors declare no competing interests.

Consent to participate

Both written and verbal consent will be obtained from the participants before the study.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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References

1. Hunter SM Crome P Hand function and stroke Rev. Clin. Gerontol. 2002 12 1 68 81 10.1017/S0959259802012194
Hunter, S. M. & Crome, P. Hand function and stroke. Rev. Clin. Gerontol. 12(1), 68–81. 10.1017/S0959259802012194 (2002).10.1017/S0959259802012194
2. Murie-Fernández M Carmona Iragui M Gnanakumar V Meyer M Foley N Teasell R Painful hemiplegic shoulder in stroke patients: Causes and management Neurología (English Edition) 2012 10.1016/j.nrleng.2012.05.002
Murie-Fernández, M. et al. Painful hemiplegic shoulder in stroke patients: Causes and management. Neurología (English Edition)10.1016/j.nrleng.2012.05.002 (2012).10.1016/j.nrleng.2012.05.002
3. Jain NB Predictors of pain and functional outcomes after the nonoperative treatment of rotator cuff tears Orthop. J. Sports Med. 2018 10.1177/2325967118788531 30480014
Jain, N. B. et al. Predictors of pain and functional outcomes after the nonoperative treatment of rotator cuff tears. Orthop. J. Sports Med.10.1177/2325967118788531 (2018).30480014 10.1177/2325967118788531
4. Benjamin Kibler W Sciascia A Wilkes T Scapular dyskinesis and its relation to shoulder injury J. Am. Acad. Orthop. Surg. 2012 10.5435/JAAOS-20-06-364 22661566
Benjamin Kibler, W., Sciascia, A. & Wilkes, T. Scapular dyskinesis and its relation to shoulder injury. J. Am. Acad. Orthop. Surg.10.5435/JAAOS-20-06-364 (2012).22661566 10.5435/JAAOS-20-06-364
5. De Baets L Jaspers E Janssens L Van Deun S Characteristics of neuromuscular control of the scapula after stroke: A first exploration Front. Hum. Neurosci. 2014 10.3389/fnhum.2014.00933 25477805
De Baets, L., Jaspers, E., Janssens, L. & Van Deun, S. Characteristics of neuromuscular control of the scapula after stroke: A first exploration. Front. Hum. Neurosci.10.3389/fnhum.2014.00933 (2014).25477805 10.3389/fnhum.2014.00933
6. Ludewig PM Cook TM Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement Phys. Ther. 2000 10.1093/ptj/80.3.276 10696154
Ludewig, P. M. & Cook, T. M. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys. Ther.10.1093/ptj/80.3.276 (2000).10696154 10.1093/ptj/80.3.276
7. McClure PW Michener LA Sennett BJ Karduna AR Direct 3-dimensional measurement of scapular kinematics during dynamic movements in vivo J. Should. Elb. Surg. 2001 10.1067/mse.2001.112954
McClure, P. W., Michener, L. A., Sennett, B. J. & Karduna, A. R. Direct 3-dimensional measurement of scapular kinematics during dynamic movements in vivo. J. Should. Elb. Surg.10.1067/mse.2001.112954 (2001).10.1067/mse.2001.112954
8. Hardwick DD Lang CE Scapular and humeral movement patterns of people with stroke during range-of-motion exercises J. Neurol. Phys. Ther. 2011 10.1097/NPT.0b013e318208efa1 21475080
Hardwick, D. D. & Lang, C. E. Scapular and humeral movement patterns of people with stroke during range-of-motion exercises. J. Neurol. Phys. Ther.10.1097/NPT.0b013e318208efa1 (2011).21475080 10.1097/NPT.0b013e318208efa1
9. Kim J Lee J Lee B Effect of scapular stabilization exercise during standing on upper limb function and gait ability of stroke patients J. Neurosci. Rural Pract. 2017 8 4 540 10.4103/JNRP.JNRP_464_16 29204011
Kim, J., Lee, J. & Lee, B. Effect of scapular stabilization exercise during standing on upper limb function and gait ability of stroke patients. J. Neurosci. Rural Pract. 8(4), 540. 10.4103/JNRP.JNRP_464_16 (2017).29204011 10.4103/JNRP.JNRP_464_16
10. Park SE Kim YR Kim YY Immediate effects of scapular stabilizing exercise in chronic stroke patient with winging and elevated scapula: A case study J. Phys. Ther. Sci. 2018 10.1589/jpts.30.190 30568338
Park, S. E., Kim, Y. R. & Kim, Y. Y. Immediate effects of scapular stabilizing exercise in chronic stroke patient with winging and elevated scapula: A case study. J. Phys. Ther. Sci.10.1589/jpts.30.190 (2018).30568338 10.1589/jpts.30.190
11. Kim HJ Lee Y Sohng KY Effects of bilateral passive range of motion exercise on the function of upper extremities and activities of daily living in patients with acute stroke J. Phys. Ther. Sci. 2014 10.1589/jpts.26.149 25540519
Kim, H. J., Lee, Y. & Sohng, K. Y. Effects of bilateral passive range of motion exercise on the function of upper extremities and activities of daily living in patients with acute stroke. J. Phys. Ther. Sci.10.1589/jpts.26.149 (2014).25540519 10.1589/jpts.26.149
12. Song CS Effects of scapular stabilization exercise on function of paretic upper extremity of chronic stroke patients J. Phys. Ther. Sci. 2013 10.1589/jpts.25.403 24259839
Song, C. S. Effects of scapular stabilization exercise on function of paretic upper extremity of chronic stroke patients. J. Phys. Ther. Sci.10.1589/jpts.25.403 (2013).24259839 10.1589/jpts.25.403
13. Lee JH Min DK Choe HS Lee JH Shin SH The effects of upper and lower limb position on symmetry of vertical ground reaction force during sit-to-stand in chronic stroke subjects J. Phys. Ther. Sci. 2018 30 2 242 10.1589/JPTS.30.242 29545686
Lee, J. H., Min, D. K., Choe, H. S., Lee, J. H. & Shin, S. H. The effects of upper and lower limb position on symmetry of vertical ground reaction force during sit-to-stand in chronic stroke subjects. J. Phys. Ther. Sci. 30(2), 242. 10.1589/JPTS.30.242 (2018).29545686 10.1589/JPTS.30.242
14. Ersoy C Iyigun G Boxing training in patients with stroke causes improvement of upper extremity, balance, and cognitive functions but should it be applied as virtual or real? Top. Stroke Rehabil. 2021 10.1080/10749357.2020.1783918 32574096
Ersoy, C. & Iyigun, G. Boxing training in patients with stroke causes improvement of upper extremity, balance, and cognitive functions but should it be applied as virtual or real?. Top. Stroke Rehabil.10.1080/10749357.2020.1783918 (2021).32574096 10.1080/10749357.2020.1783918
15. Awad A Shaker H Shendy W Fahmy M Effect of shoulder girdle strengthening on trunk alignment in patients with stroke J. Phys. Ther. Sci. 2015 10.1589/jpts.27.2195 26311953
Awad, A., Shaker, H., Shendy, W. & Fahmy, M. Effect of shoulder girdle strengthening on trunk alignment in patients with stroke. J. Phys. Ther. Sci.10.1589/jpts.27.2195 (2015).26311953 10.1589/jpts.27.2195
16. Silverson OA Lemaster NG Hettrich CM Heebner NR Uhl TL Reliability and validity of a clinical assessment tool for measuring scapular motion in all 3 anatomical planes J. Athl. Train. 2021 56 6 586 593 10.4085/276-20 33150418
Silverson, O. A., Lemaster, N. G., Hettrich, C. M., Heebner, N. R. & Uhl, T. L. Reliability and validity of a clinical assessment tool for measuring scapular motion in all 3 anatomical planes. J. Athl. Train. 56(6), 586–593. 10.4085/276-20 (2021).33150418 10.4085/276-20
17. Wu G ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion—Part II: Shoulder, elbow, wrist and hand J. Biomech. 2005 38 5 981 992 10.1016/J.JBIOMECH.2004.05.042 15844264
Wu, G. et al. ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion—Part II: Shoulder, elbow, wrist and hand. J. Biomech. 38(5), 981–992. 10.1016/J.JBIOMECH.2004.05.042 (2005).15844264 10.1016/J.JBIOMECH.2004.05.042
18. Silverson OA Lemaster NG Hettrich CM Heebner NR Uhl TL Reliability and validity of a clinical assessment tool for measuring scapular motion in all 3 anatomical planes J. Athl. Train. 2021 10.4085/276-20 33150418
Silverson, O. A., Lemaster, N. G., Hettrich, C. M., Heebner, N. R. & Uhl, T. L. Reliability and validity of a clinical assessment tool for measuring scapular motion in all 3 anatomical planes. J. Athl. Train.10.4085/276-20 (2021).33150418 10.4085/276-20
19. Contreras J Scapular balance angle reference values in a healthy population Revista Española de Cirugía Ortopédica y Traumatología (English Edition) 2014 10.1016/j.recote.2013.12.004
Contreras, J. et al. Scapular balance angle reference values in a healthy population. Revista Española de Cirugía Ortopédica y Traumatología (English Edition)10.1016/j.recote.2013.12.004 (2014).10.1016/j.recote.2013.12.004
20. Celik D Dirican A Baltaci G Intrarater reliability of assessing strength of the shoulder and scapular muscles J. Sport Rehabil. 2012 21 1 1 5 10.1123/JSR.2012.TR3 22495260
Celik, D., Dirican, A. & Baltaci, G. Intrarater reliability of assessing strength of the shoulder and scapular muscles. J. Sport Rehabil. 21(1), 1–5. 10.1123/JSR.2012.TR3 (2012).22495260 10.1123/JSR.2012.TR3
21. Niessen M Janssen T Meskers C Koppe P Konijnenbelt M Veeger DJ Kinematics of the contralateral and ipsilateral shoulder: A possible relationship with post-stroke shoulder pain J. Rehabil. Med. 2008 10.2340/16501977-0201 18509565
Niessen, M. et al. Kinematics of the contralateral and ipsilateral shoulder: A possible relationship with post-stroke shoulder pain. J. Rehabil. Med.10.2340/16501977-0201 (2008).18509565 10.2340/16501977-0201
22. Miyamoto S Hondo T Suzukamo Y Michimata A Izumi SI Reliability and validity of the manual function test in patients with stroke Am. J. Phys. Med. Rehabil. 2009 10.1097/PHM.0b013e3181951133 19661779
Miyamoto, S., Hondo, T., Suzukamo, Y., Michimata, A. & Izumi, S. I. Reliability and validity of the manual function test in patients with stroke. Am. J. Phys. Med. Rehabil.10.1097/PHM.0b013e3181951133 (2009).19661779 10.1097/PHM.0b013e3181951133
23. Kim HJ Clinical applicability and psychometric properties of manual function test for patients with stroke Tohoku J. Exp. Med. 2017 10.1620/tjem.243.85 29238001
Kim, H. J. et al. Clinical applicability and psychometric properties of manual function test for patients with stroke. Tohoku J. Exp. Med.10.1620/tjem.243.85 (2017).29238001 10.1620/tjem.243.85
24. Brokelman RBG Haverkamp D van Loon C Hol A van Kampen A Veth R The validation of the visual analogue scale for patient satisfaction after total hip arthroplasty Eur. Orthop. Traumatol. 2012 10.1007/s12570-012-0100-3 22798966
Brokelman, R. B. G. et al. The validation of the visual analogue scale for patient satisfaction after total hip arthroplasty. Eur. Orthop. Traumatol.10.1007/s12570-012-0100-3 (2012).22798966 10.1007/s12570-012-0100-3
25. Voutilainen A Pitkäaho T Kvist T Vehviläinen-Julkunen K How to ask about patient satisfaction? The visual analogue scale is less vulnerable to confounding factors and ceiling effect than a symmetric Likert scale J. Adv. Nurs. 2016 10.1111/jan.12875 26689434
Voutilainen, A., Pitkäaho, T., Kvist, T. & Vehviläinen-Julkunen, K. How to ask about patient satisfaction? The visual analogue scale is less vulnerable to confounding factors and ceiling effect than a symmetric Likert scale. J. Adv. Nurs.10.1111/jan.12875 (2016).26689434 10.1111/jan.12875
26. Cohen, J. Statistical Power Analysis for the Behavioral Sciences, 2nd ed. (Lawrence Earlbaum Associates, 1988).
27. Ludewig PM Reynolds JF The association of scapular kinematics and glenohumeral joint pathologies J. Orthop. Sports Phys. Ther. 2009 39 2 90 104 10.2519/JOSPT.2009.2808 19194022
Ludewig, P. M. & Reynolds, J. F. The association of scapular kinematics and glenohumeral joint pathologies. J. Orthop. Sports Phys. Ther. 39(2), 90–104. 10.2519/JOSPT.2009.2808 (2009).19194022 10.2519/JOSPT.2009.2808
28. Rundquist PJ Dumit M Hartley J Schultz K Finley MA Three-dimensional shoulder complex kinematics in individuals with upper extremity impairment from chronic stroke Disabil. Rehabil. 2012 10.3109/09638288.2011.607214 22351959
Rundquist, P. J., Dumit, M., Hartley, J., Schultz, K. & Finley, M. A. Three-dimensional shoulder complex kinematics in individuals with upper extremity impairment from chronic stroke. Disabil. Rehabil.10.3109/09638288.2011.607214 (2012).22351959 10.3109/09638288.2011.607214
29. Lixandrão MC Camargo PR Scarpa CEN Prado-Medeiros CL Salvini TF Bilateral changes in 3-D scapular kinematics in individuals with chronic stroke Clin. Biomech. 2017 10.1016/j.clinbiomech.2017.06.002
Lixandrão, M. C., Camargo, P. R., Scarpa, C. E. N., Prado-Medeiros, C. L. & Salvini, T. F. Bilateral changes in 3-D scapular kinematics in individuals with chronic stroke. Clin. Biomech.10.1016/j.clinbiomech.2017.06.002 (2017).10.1016/j.clinbiomech.2017.06.002
30. Culham EG Noce RR Bagg SD Shoulder complex position and glenohumeral subluxation in hemiplegia Arch. Phys. Med. Rehabil. 1995 10.1016/S0003-9993(95)80552-4 7668958
Culham, E. G., Noce, R. R. & Bagg, S. D. Shoulder complex position and glenohumeral subluxation in hemiplegia. Arch. Phys. Med. Rehabil.10.1016/S0003-9993(95)80552-4 (1995).7668958 10.1016/S0003-9993(95)80552-4
31. Neumann DA Camargo PR Kinesiologic considerations for targeting activation of scapulothoracic muscles—Part 1: Serratus anterior Braz. J. Phys. Ther. 2019 10.1016/j.bjpt.2019.01.008 30797676
Neumann, D. A. & Camargo, P. R. Kinesiologic considerations for targeting activation of scapulothoracic muscles—Part 1: Serratus anterior. Braz. J. Phys. Ther.10.1016/j.bjpt.2019.01.008 (2019).30797676 10.1016/j.bjpt.2019.01.008
32. Jadhav R Pazare S Effect of scapular kinesiotaping as an adjunct to dynamic neuromuscular stabilization exercises on upper extremity functions in stroke patients Int. J. Health Sci. Res. 2022 10.52403/ijhsr.20220103
Jadhav, R. & Pazare, S. Effect of scapular kinesiotaping as an adjunct to dynamic neuromuscular stabilization exercises on upper extremity functions in stroke patients. Int. J. Health Sci. Res.10.52403/ijhsr.20220103 (2022).10.52403/ijhsr.20220103
33. Oz R Duray M Korkmaz NC Effects of isometric scapular exercises on the scapular stability in patients with stroke J. Neurol. Sci. 2021 10.1016/j.jns.2021.118571
Oz, R., Duray, M. & Korkmaz, N. C. Effects of isometric scapular exercises on the scapular stability in patients with stroke. J. Neurol. Sci.10.1016/j.jns.2021.118571 (2021).10.1016/j.jns.2021.118571
34. Worsley P Motor control retraining exercises for shoulder impingement: Effects on function, muscle activation, and biomechanics in young adults J. Should. Elb. Surg. 2013 10.1016/J.JSE.2012.06.010
Worsley, P. et al. Motor control retraining exercises for shoulder impingement: Effects on function, muscle activation, and biomechanics in young adults. J. Should. Elb. Surg.10.1016/J.JSE.2012.06.010 (2013).10.1016/J.JSE.2012.06.010
35. Turgut E Duzgun I Baltaci G Effects of scapular stabilization exercise training on scapular kinematics, disability, and pain in subacromial impingement: A randomized controlled trial Arch. Phys. Med. Rehabil. 2017 10.1016/j.apmr.2017.05.023 28652066
Turgut, E., Duzgun, I. & Baltaci, G. Effects of scapular stabilization exercise training on scapular kinematics, disability, and pain in subacromial impingement: A randomized controlled trial. Arch. Phys. Med. Rehabil.10.1016/j.apmr.2017.05.023 (2017).28652066 10.1016/j.apmr.2017.05.023
36. Jeong J-R Lee W-H The study of asymmetrical of the serratus anterior and lower trapezius muscles in chronic stroke patients J. Korean Soc. Phys. Med. 2015 10.13066/kspm.2015.10.4.81
Jeong, J.-R. & Lee, W.-H. The study of asymmetrical of the serratus anterior and lower trapezius muscles in chronic stroke patients. J. Korean Soc. Phys. Med.10.13066/kspm.2015.10.4.81 (2015).10.13066/kspm.2015.10.4.81
37. Dabholkar A Mehta D Yardi S Dabholkar T Assessment of scapular behavior in stroke patients Int. J. Health Rehabil. Sci. IJHRS. 2015 10.5455/ijhrs.000000079
Dabholkar, A., Mehta, D., Yardi, S. & Dabholkar, T. Assessment of scapular behavior in stroke patients. Int. J. Health Rehabil. Sci. IJHRS.10.5455/ijhrs.000000079 (2015).10.5455/ijhrs.000000079
38. Alizadeh, M. H., Daneshmandi, H., Shademan, B., Ahmadizad, S. The effects of exercise training on scapula position of muscle activity measured by EMG. World J. Sport Sci. 2(1) (2009).
39. Bhagat, P., Harishchandre, M., Ganvir, S. Comparative study of immediate and short term effect of 4 days of scapular stabilizing exercises and scapular proprioceptive neuromuscular facilitation on scapular alignment and functional task in patients with stroke—An experimental study. Int. J. Clin. Biomed. Res. 1–8 (2023). https://ijcbr.com/index.php/ijcbr/article/view/414 (accessed 08 Jan 2024).
40. Kaur, N., Bhanot, K., Brody, L. T., Bridges, J., Berry, D. C., Ode, J. J. Effects of lower extremity and trunk muscles recruitment on serratus anterior muscle activation in healthy male adults. Int. J. Sports Phys. Ther. 9(7) (2014).
41. Barnes CJ Van Steyn SJ Fischer RA The effects of age, sex, and shoulder dominance on range of motion of the shoulder J. Should. Elb. Surg. 2001 10.1067/mse.2001.115270
Barnes, C. J., Van Steyn, S. J. & Fischer, R. A. The effects of age, sex, and shoulder dominance on range of motion of the shoulder. J. Should. Elb. Surg.10.1067/mse.2001.115270 (2001).10.1067/mse.2001.115270
42. You YY Her JG Woo JH Ko T Chung SH The effects of stretching and stabilization exercise on the improvement of spastic shoulder function in hemiplegic patients J. Phys. Ther. Sci. 2014 10.1589/jpts.26.491 24764618
You, Y. Y., Her, J. G., Woo, J. H., Ko, T. & Chung, S. H. The effects of stretching and stabilization exercise on the improvement of spastic shoulder function in hemiplegic patients. J. Phys. Ther. Sci.10.1589/jpts.26.491 (2014).24764618 10.1589/jpts.26.491
43. Sánchez-Lastra MA Ayán C Sener M Cancela JM The use of adapted boxing as a rehabilitation strategy in people with diverse health conditions: A systematic review Eur. J. Adapt. Phys. Act. 2020 10.5507/euj.2020.004
Sánchez-Lastra, M. A., Ayán, C., Sener, M. & Cancela, J. M. The use of adapted boxing as a rehabilitation strategy in people with diverse health conditions: A systematic review. Eur. J. Adapt. Phys. Act.10.5507/euj.2020.004 (2020).10.5507/euj.2020.004
44. Levac, D. E., Sveistrup, H. Motor Learning and Virtual Reality 25–46 (2014). 10.1007/978-1-4939-0968-1_3.
45. Sciascia A Thigpen C Namdari S Baldwin K Kinetic chain abnormalities in the athletic shoulder Sports Med. Arthrosc. Rev. 2012 20 1 16 21 10.1097/JSA.0B013E31823A021F 22311288
Sciascia, A., Thigpen, C., Namdari, S. & Baldwin, K. Kinetic chain abnormalities in the athletic shoulder. Sports Med. Arthrosc. Rev. 20(1), 16–21. 10.1097/JSA.0B013E31823A021F (2012).22311288 10.1097/JSA.0B013E31823A021F
46. King LA Horak FB Delaying mobility disability in people with Parkinson disease using a sensorimotor agility exercise program Phys. Ther. 2009 89 4 384 393 10.2522/PTJ.20080214 19228832
King, L. A. & Horak, F. B. Delaying mobility disability in people with Parkinson disease using a sensorimotor agility exercise program. Phys. Ther. 89(4), 384–393. 10.2522/PTJ.20080214 (2009).19228832 10.2522/PTJ.20080214
47. Shin BW Berg WP Stutz MM Hughes MR Effect of non-contact boxing training on the frequency and timing of anticipatory postural adjustments in healthy adults J. Sports Med. Phys. Fitness 2022 62 12 1646 1653 10.23736/S0022-4707.22.13495-X 35112818
Shin, B. W., Berg, W. P., Stutz, M. M. & Hughes, M. R. Effect of non-contact boxing training on the frequency and timing of anticipatory postural adjustments in healthy adults. J. Sports Med. Phys. Fitness 62(12), 1646–1653. 10.23736/S0022-4707.22.13495-X (2022).35112818 10.23736/S0022-4707.22.13495-X
48. Cheung, K. L., Tunik, E., Adamovich, S. V., Boyd, L. A. Neuroplasticity and Virtual Reality (2014). 10.1007/978-1-4939-0968-1_2.
49. Wong RSM Development and pilot evaluation of a mobile app on parent-child exercises to improve physical activity and psychosocial outcomes of Hong Kong Chinese children BMC Public Health 2020 10.1186/s12889-020-09655-9 33238941
Wong, R. S. M. et al. Development and pilot evaluation of a mobile app on parent-child exercises to improve physical activity and psychosocial outcomes of Hong Kong Chinese children. BMC Public Health10.1186/s12889-020-09655-9 (2020).33238941 10.1186/s12889-020-09655-9
50. Holden MK Virtual environments for motor rehabilitation: Review Cyberpsychol. Behav. 2005 10.1089/cpb.2005.8.187 15971970
Holden, M. K. Virtual environments for motor rehabilitation: Review. Cyberpsychol. Behav.10.1089/cpb.2005.8.187 (2005).15971970 10.1089/cpb.2005.8.187
