
==== Front
J Phys Ther Sci
J Phys Ther Sci
JPTS
Journal of Physical Therapy Science
0915-5287
2187-5626
The Society of Physical Therapy Science

2024-059
10.1589/jpts.36.513
Original Article
Short-term intervention effect analysis of neuromuscular joint facilitation in patients who experienced stroke with shoulder subluxation: a clinical randomized controlled trial
Xie Hualong 1 a
Liu Shan 2 a
Zhan Jiawen 1 a
Chen Lei 3
Yu Suli 3
Chen Jing 4
Onoda Ko 5
Maruyama Hitoshi 5
Zhu Liguo 1
Zhang Qing 1 *
Huo Ming 2 3 *
1) Wangjing Hospital of China Academy of Chinese Medical Sciences: Beijing, Chaoyang District, China
2) University of Health and Rehabilitation Sciences, China
3) Jilin Province Power Hospital, China
4) The Affiliated Hospital of Inner Mongolia Medical University, China
5) International University of Health and Welfare, Japan
a These authors have contributed equally to this work.
* Corresponding authors. Qing Zhang (E-mail: zhangqinggys@163.com); Ming Huo (E-mail: huoming8@gmail.com)
5 9 2024
9 2024
36 9 513517
14 5 2024
02 6 2024
2024©by the Society of Physical Therapy Science. Published by IPEC Inc.
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License. (CC-BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/)
[Purpose] Shoulder subluxation is a common complication of acute stroke that affects clinical rehabilitation training and hinders the recovery of upper limb motor function. This study explored the short-term interventional effects of neuromuscular joint facilitation in patients who experienced stroke with shoulder subluxation. [Participants and Methods] We recruited 36 patients who experienced stroke with shoulder subluxation. All patients were randomly divided into two groups: the neuromuscular joint facilitation group (n=18) and the control group (n=18). The control group underwent routine rehabilitation treatment. The intervention in the neuromuscular joint facilitation group involved neuromuscular joint facilitation of the shoulder joint in four modes based on conventional rehabilitation treatment. Four different interventions were administered. The thickness of the supraspinatus muscle and the acromion-greater tuberosity distance were measured using ultrasound to observe the curative effect. [Results] In neuromuscular joint facilitation group, the thickness of supraspinatus muscle, acromion-greater tuberosity distance and acromion-greater tuberosity distance difference were significantly different before and after intervention. In the control group, there were no significant difference before and after intervention. [Conclusion] Neuromuscular joint facilitation intervention improved the thickness of the supraspinatus muscle, shortened the distance between the acromion and the greater tubercle, and improved shoulder subluxation in patients who experienced stroke.

Stroke
Shoulder subluxation
Neuromuscular joint facilitation
==== Body
pmcINTRODUCTION

Shoulder subluxation is one of the common complications experienced during the acute phase of stroke, with a reported prevalence range of 17–81%1, 2). Sixty-seven percent of patients who were followed up for 10 experienced limited functional recovery owing to the presence of shoulder subluxation3). Stroke hemiplegia with shoulder subluxation affects clinical rehabilitation and hinders the recovery of upper limb motor function4).

Shoulder subluxation at the early stage of stroke makes it difficult to maintain the weight of the upper limb owing to paralysis of the muscles around the shoulder joint centered on the supraspinatus muscle5, 6). Therefore, the development of treatment strategies for restoring the function of the supraspinatus muscle is important. Previous studies have shown that through neuromuscular joint facilitation (NJF) intervention in the shoulder joint of healthy people, the thickness of the supraspinatus muscle increases, and the stability of the shoulder joint improves. It is reported that the EMG response time of shoulder joint pronation is shortened by7,8,9,10,11).

Neuromuscular joint facilitation is a new type of exercise therapy that merges the benefit of proprioceptive neuromuscular facilitation (PNF) and joint mobilization. It directly stimulates the movement in the joint capsule while promoting the nerves, muscles, and joint functions. This further improves the movement in the joint capsule by improving the alignment of the joint capsule12). The effect of NJF on shoulder subluxation in patients with hemiplegia has not been extensively studied, and its mechanism of action remains unclear. The purpose of this study is to explore the short-term intervention effect of neuromuscular joint facilitation on stroke patients with shoulder subluxation.

PARTICIPANTS AND METHODS

We conducted a clinical randomized controlled trial. A total of 36 stroke patients with shoulder subluxation participated in this study conducted at the rehabilitation department of a hospital. The attributes of the participants are highlighted in Table 1Table 1. Characteristics of the participants

	NJF group	Control group	Total	
N=18	N=18	n=36	
Age (years)	55.1 ± 13.1	53.6 ± 8.8	54.3 ± 11.0	
Height (cm)	166.6 ± 6.8	168.5 ± 8.3	167.9 ± 7.5	
Weight (kg)	67.2 ± 14.3	66.9 ± 15.3	67.1 ± 14.6	
Mean ± standard deviation. NJF: neuromuscular joint facilitation.

(23 males, 13 females, 11 right-sided hemiplegias, and 25 left-sided hemiplegias, for patients within 6 months of initial onset, Brunstrom stage I: 14, II: 11, III: 9, IV: 2). We calculated the minimum total sample size required using G*Power software for analysis of variance (ANOVA) with repeated measures and within-between interaction methods, setting α at 0.05 and test efficacy (1-β) at 0.8, resulting in a determination of 24 participants13). This study included 36 patients with stroke and shoulder subluxation. A simple random sampling method was used in this study. All eligible participants were randomly assigned to two groups using a random number sequence generated by a computer software. The number assignments were stored in sealed opaque envelopes, which could only be opened when qualified participants agreed to participate in the test; then the participants accepted the corresponding intervention methods. All patients were randomly divided into two groups: experimental group (n=18) and control group (n=18).

Inclusion criteria: Meet the diagnostic criteria for stroke patients; Stroke hemiplegia patients with the first onset and within 6 months of onset; The manual palpation method is more than 1/2 of the transverse finger14) and the acromion-greater tuberosity distance (AGTD) difference between the two sides is ≥0.2 cm or more15); Ability of the patient to sit independently; Aged 18–65; No serious cognitive impairment and the patient can cooperate with researchers; Those who know the research process and significance, and sign the informed consent form. Exclusion criteria: Patients with unstable general state and neurological symptoms, orthopedic diseases, cognitive disorders, and mental diseases; Patients with cognitive impairment and inability to understand instructions; Patients with brain stem disease or bilateral paralysis; Patients with exercise-restrictive respiratory diseases and circulatory diseases. This study was approved by the Ethics Review Committee of the International University of Health and Welfare (NO.19-Io-45). The purpose and content of the study were explained to the participants in advance, and informed consent was obtained from all participants before the start of the study.

The control group received the conventional rehabilitation treatment. (1) Extension: The rehabilitator helps the patient to lie in the supine or lateral positions, and helps the patient to move the shoulder joint when the shoulder joint is moved in the normal clockwise or counterclockwise range; the patient keeps the elbow extended, and the rehabilitator pushes the shoulder blade of the patient to drive the arm upward and downward; (2) Upper Extension: The rehabilitator adjusts the shoulder blade of the patient by pushing the upper extremity of the patient forward and straightening the elbow; (3) Up and Down Movement: The rehabilitator assists the patient with arm flexion and extension, keeping the shoulder joint in the normal position. Four interventions were conducted.

The NJF group received a modification of the conventional rehabilitation treatment. Four NJF shoulder patterns were used16) (shoulder flexion-adduction-external rotation, shoulder extension-abduction-internal rotation, shoulder flexion-abduction-external rotation, and shoulder extension-adduction-internal rotation). Each pattern involved five passive and resistance movements. The physical therapist who participated in the NJF technology operation in this study had more than five years’ experience in using NJF and completed the intermediate certification course.

This study used an ultrasound scanner (SonoSite Ultrasound System 180 plus, SonoSite, Inc., Bothell, WA, USA) equipped with a 7.5 MHz linear transducer for measuring both the supraspinatus muscle thickness and AGTD. Measurement position and method: The patients were seated with feet flat on the ground, bilateral upper limbs naturally hanging down on the side of the body, elbow flexion 90° flexion, forearms on pillows (pillows placed on the thigh of the patient), and the elbows were unsupported.

The acromion-greater tuberosity distance (AGTD) was measured as follows. During measurement, the examiner stood on the side of the patient’s hemiplegic limb. First, the acromion and the greater tuberosity were palpated and marked. The ultrasonic probe was placed on the outer edge of the acromion along the longitudinal axis of the humerus, rotated, and the image was frozen when the outer edge of the acromion and the greater tuberosity were simultaneously visible on the screen. Finally, the distance between the acromion and the greater tuberosity was measured17). The examiner measures the AGTD on both sides twice and takes the average value as the representative value.

The AGTD difference: The AGTD difference is the AGTD on the hemiplegic side minus the AGTD on the non-hemiplegic side.

The supraspinatus muscle thickness was measured as follows: The examiner stood on the dorsal side of the patient, placing the ultrasound probe vertically against the midpoint of the scapular ridge to measure the supraspinatus thickness. They then moved the ultrasound probe in parallel until identifying the thickest cross-section of the supraspinatus muscle, froze the image, and measured the distance of the thickest portion of the supraspinatus muscle18). The thickness of the supraspinatus muscle was measured twice on each side, and the average of the two measurements was taken as the representative value.

The data measured in the experiment were recorded using Microsoft Excel and statistically analyzed using SPSS 23.0 statistical software. The measurement data are expressed in mean ± standard deviation, while the counted data are expressed in absolute and relative numbers. Normally distributed measurement data are subject to repeated measurement two-factor analysis of variance and t-tests, and the measurement data that are not normally distributed and classified counting data are subject to the rank sum test. Inspection level α=0.05, p<0.05, the difference was statistically significant.

RESULTS

Based on the results of bivariate analysis of variance, there was an interaction between the time of AGTD (before and after intervention) and the group, so the lower test was used. The AGTD on the hemiplegic side was statistically significant only in the NJF intervention group (p<0.01). The AGTD decreased after NJF intervention. The difference in the AGTD was statistically significant only in the NJF intervention group (p<0.05), and the AGTD decreased after the NJF intervention. The thickness of the supraspinatus muscle on the hemiplegic side was statistically significant only in the NJF intervention group (p<0.01). The thickness of the supraspinatus muscle increased after NJF intervention (Table 2Table 2. Results for each measurement item before and after the intervention (unit: cm)

	NJF group (n=18)	Control group (n=18)	
		
Pre-intervention	Post-intervention	Pre-intervention	Post-intervention	
AGTD-hemiplegia side	2.87 ± 0.54	2.52 ± 0.47**	2.73 ± 0.37	2.73 ± 0.42	
Supraspinatus thickness-hemiplegia side	0.97 ± 0.27	1.11 ± 0.25**	0.91 ± 0.29	0.92 ± 0.33	
AGTD difference	1.00 ± 0.57	0.66 ± 0.41*	0.93 ± 0.46	0.94 ± 0.51	
Mean ± standard deviation; before and after the intervention: *p<0.05; **p<0.01.

NJF: neuromuscular joint facilitation; AGTD: acromion-greater tuberosity distance.

).

DISCUSSION

This intervention effect of NJF on stroke patients with shoulder subluxation was investigated in this study. We found that, compared with conventional rehabilitation therapy alone, the addition of the NJF intervention significantly improved the thickness of the supraspinatus muscle and the distance from the acromion to the humeral head in patients with hemiplegia. The intervention also improved the degree of shoulder joint subluxation and improved the motor function of the upper limb.

The supraspinatus and deltoid muscles are important muscles that help maintain the stability of the shoulder joint19). The supraspinatus muscle is considered to be the most important muscle group that helps prevent shoulder subluxation in stroke patients with hemiplegia. The function of the supraspinatus muscle is to abduct the upper limb. Because the attachment point of the supraspinatus muscle is mostly in front of the major tubercle, it is speculated that the abduction function of the shoulder joint in the external rotation position is stronger than that in the internal rotation position. The contraction of the supraspinatus muscle enhances the horizontal tension of the shoulder joint capsule and keeps the humeral head in contact with the shoulder socket. In addition, the supraspinatus muscle responds to the load of the joint. Shoulder joint subluxation is more common in stroke patients with hemiplegia owing to the paralysis of the supraspinatus muscle5, 6, 20). In addition, in patients with stroke, there is a significant difference between the hemiplegic and the non-hemiplegic sides of the supraspinatus muscle. The thickness of the supraspinatus muscle on the hemiplegic side decreases significantly in patients with stroke6). In this study, we found that the thickness of the supraspinatus muscle in hemiplegic patients increased after NJF intervention. In previous studies, during chemotherapy, they observed that the NJF shoulder joint model has a positive clinical intervention effect in patients with breast cancer patients. After NJF intervention, the thickness and grip strength of the supraspinatus muscle increase, improving the shoulder joint movement disorder, pain, grip strength, and external rotation function16). Therefore, the NJF shoulder joint movement mode has a positive effect on improving the function of supraspinatus muscles.

Neuromuscular joint facilitation technology adopts appropriate resistance training, applies muscle stretch, and diagonal spiral movements. By implementing auxiliary or resistance movements at the proximal end of the joint, it promotes movement within the joint capsule, enhancing joint range of motion and strengthening small muscles in the deep layers around the joint. This approach yields dual benefits of improving joint stability and mobility. NJF utilizes the spiral diagonal motion of the PNF, focusing on multi-axis and multidirectional joint movements. This movement reflects natural motions used in everyday activities and sports, and synchronously promotes nerves, muscles, and joint functions21, 22). In addition, the difference in the AGTD can be used to evaluate important indexes of shoulder subluxation in patients with stroke15). The distance from the greater tubercle to the acromion can be observed intuitively by ultrasonic measurement. We found that after NJF intervention, the distance between the acromion and the greater tubercle reduced, the difference in the AGTD between the hemiplegic and non-hemiplegic sides reduced, and the degree of subluxation improved. Therefore, we conclude that NJF increases supraspinatus muscle thickness and muscle tension, prevents the humeral head from falling downward, and improves shoulder subluxation.

Our study had some limitations. First, the study lacked an untreated control group, because it was immoral for the patients not to receive treatment during rehabilitation. Therefore, the natural recovery process could not be observed. Second, this was a short-term observational study; however, long-term intervention and regular follow-up are necessary to confirm these findings.

Funding

This work was supported by the National Natural Science Foundation of China (grant number 82372585).

Conflict of interest

None.
==== Refs
REFERENCES

1 Turner-Stokes L Jackson D : Shoulder pain after stroke: a review of the evidence base to inform the development of an integrated care pathway. Clin Rehabil, 2002, 16 : 276–298. 12017515
2 Huang SW Liu SY Tang HW et al. : Relationship between severity of shoulder subluxation and soft-tissue injury in hemiplegic stroke patients. J Rehabil Med, 2012, 44 : 733–739. 22854896
3 Smith RG Cruikshank JG Dunbar S et al. : Malalignment of the shoulder after stroke. Br Med J (Clin Res Ed), 1982, 284 : 1224–1226.
4 Kumar P Cruziah R Bradley M et al. : Intra-rater and inter-rater reliability of ultrasonographic measurements of acromion-greater tuberosity distance in patients with post-stroke hemiplegia. Top Stroke Rehabil, 2016, 23 : 147–153. 26653884
5 Chaco J Wolf E : Subluxation of the glenohumeral joint in hemiplegia. Am J Phys Med, 1971, 50 : 139–143. 5579071
6 Liu S Cao C Xie H et al. : Evaluation of supraspinatus muscle changes in the shoulder joint of stroke patients with hemiplegic and shoulder subluxation using ultrasonography: comparison between affected and unaffected sides. J Phys Ther Sci, 2022, 34 : 44–48. 35035079
7 Huo M Desheng LI Meng GE et al. : Effects of neuromuscular joint facilitation on electromechanical reaction time of human teres major. J Phys Ther Sci, 2012, 24 : 93–95.
8 Huo M Ge M Li D et al. : Effects of neuromuscular joint facilitation on electromechanical reaction time of rectus femoris. J Phys Ther Sci, 2012, 24 : 55–57.
9 Huo M Wang H Ge M et al. : The immediate effect of neuromuscular joint facilitation (NJF) treatment on electromechanical reaction times of hip flexion. J Phys Ther Sci, 2013, 25 : 1463–1465. 24396211
10 Huo M Li D Ge M et al. : Effects of neuromuscular joint facilitation on electromechanical reaction times of the teres major. J Phys Ther Sci, 2012, 24 : 93–95.
11 Wu P Huo M Maruyama H : Effects of neuromuscular joint facilitation on baseball pitching velocity and electromechanical reaction times of the teres major of young amateur baseball players. J Phys Ther Sci, 2013, 25 : 1459–1461. 24396210
12 Huo M : Neuromuscular joint facilitation method. Tokyo: IPEC, 2010, pp 3–16.
13 Kang H : Sample size determination and power analysis using the G*Power software. J Educ Eval Health Prof, 2021, 18 : 17. 34325496
14 Hall J Dudgeon B Guthrie M : Validity of clinical measures of shoulder subluxation in adults with poststroke hemiplegia. Am J Occup Ther, 1995, 49 : 526–533. 7645665
15 Kumar P Mardon M Bradley M et al. : Assessment of glenohumeral subluxation in poststroke hemiplegia: comparison between ultrasound and fingerbreadth palpation methods. Phys Ther, 2014, 94 : 1622–1631. 25060958
16 Huo M Zhang X Fan J et al. : Short-term effects of a new resistance exercise approach on physical function during chemotherapy after radical breast cancer surgery: a randomized controlled trial. BMC Womens Health, 2024, 24 : 160. 38443932
17 Yang C Chen P Du W et al. : Musculoskeletal ultrasonography assessment of functional magnetic stimulation on the effect of glenohumeral subluxation in acute poststroke hemiplegic patients. BioMed Res Int, 2018, 2018 : 6085961. 30065941
18 Xie H Lu K Lyu G et al. : Reliability of ultrasonographic measurement of the supraspinatus thickness at different angles of shoulder abduction in patients with stroke. J Phys Ther Sci, 2020, 32 : 257–259. 32184543
19 Faghri PD Rodgers MM Glaser RM et al. : The effects of functional electrical stimulation on shoulder subluxation, arm function recovery, and shoulder pain in hemiplegic stroke patients. Arch Phys Med Rehabil, 1994, 75 : 73–79. 8291967
20 Yoshihiro K : Shoulder joint—physical therapy management, 1st ed. Tokyo: Medical View, 2019, pp 11–18.
21 Chen L Sun J Liu S et al. : Immediate effects of neuromuscular joint-facilitation bridging exercises on walking ability and balance function in stroke patients. J Phys Ther Sci, 2022, 34 : 172–176. 35291474
22 Xie H Huo M Huang Q et al. : Immediate effects of lumbar spine patterns after neuromuscular joint facilitation on balance in stroke patients. J Phys Ther Sci, 2019, 31 : 979–982. 32038068
