Physical Therapy Korea

After stroke, spasticity appears during passive stretching, and flexion synergies occur during active motion [1]. Although flexion synergies may occur first, prior to the appearance of spasticity, these two factors act as a complex form of spastic motor disorder owing to their close interaction. Once spasticity occurs, distinguishing it from flexion synergies becomes difficult. The pathophysiological phenomenon of motor disorders resulting from spasticity depends on various factors, including abnormal regulation at the upper spinal cord level, abnormal reflex control, and changes in the biomechanical properties of muscles [2]. Consequently, the accompanying joint contracture will interfere with rehabilitation outcomes, including range of motion limitation, pain, and gait disability [3].

Spastic motor disorders have been identified using scientific method in various aspects of patients with upper-motor neuron syndrome, including changes in synergy structures and recruitment patterns of the upper-extremity [4-6], changes in the muscle activation patterns of the lower extremity [7,8], muscle co-activation during voluntary behaviors [9,10], the perception of force by spasticity, and involuntary synergy activation [11]. Furthermore, the spasticity of the elbow flexor during a stretch reflex has been quantified [12,13].

Various methods have been recommended for reducing spasticity and flexion synergies, including electrical stimulation therapy [14-17], surgical methods [18], neurophysiological approaches such as the Bobath technique [19], and medical treatments [20,21]. The efficacy and safety of other methods, such as drug administration, chemical nerve block, or neurosurgical treatments are controversial, because they may reduce spasticity but could also induce muscle weakness or paralysis [16]. In neurophysiological approaches, various conventional approaches have been employed to reduce spasticity and flexion synergies. However, only a few studies have shown scientific evidence that these techniques are effective in reducing spasticity flexion synergies [22-24].

Another technique to reduce spasticity and flexion synergies is the Ueda method, which was introduced by Ueda Tadashi in 1988 in Japan. This method was developed with a concept different from that of conventional brain-oriented approach, indicating that the resolution of spasticity caused by impairment to the upper-motor neurons are essential for motor function improvement. Moreover, its application is the opposite of conventional rehabilitation principles. Instead of stretching the spastic muscles, the Ueda method reduces spasticity by further enhances the abnormal synergic postures and positions that are accompanied by muscle hypertension. Therefore, the Ueda method has a therapeutic principle that reduction in spasticity can be achieved by regulating excitement of the spinal cord circuit and driving the reciprocal inhibition circuit. Despite the unique characteristics and originality of this technique, relatively few empirical studies on the scientific mechanism and therapeutic effects of the Ueda method have been conducted [25,26].

Therefore, in this study, we aimed to investigate the immediate effects of the application of the Ueda method on patients with spastic motor dysfunctions after stroke via an electrophysiological study.

1. Study Design

This study was a randomized double-blind pilot study. Patients were randomly allocated to the convention (n = 15) and Ueda (n = 15) groups using a computer-generated block random number table (Microsoft Excel 2016; Microsoft, Redmond, WA, USA). Conventional therapy or the Ueda method was applied for 15 minutes after pre-test. After five minutes of rest, a re-test was performed. The two physical therapists who supervised the interventions were not involved in the evaluation of participants; three evaluators performed all experimental procedures.

2. Participants

A total of 30 stroke patients were recruited in this study. The inclusion criteria were as follows: (1) stroke diagnosis (cerebral infarction, cerebral hemorrhage) provided by a neurosurgeon, (2) Korean Mini-Mental State Examination score of ≥ 24 points, (3) elbow joint passive range of ≥ 120°, (4) spasticity score of 1–2 according to the modified Ashworth scale (MAS), and (5) above-normal level of independence in performing activities of daily living (modified Barthel index of ≥ 50 points). The exclusion criteria were as follows: (1) sensory deficit, (2) intake of medications for reducing muscle tonicity, (3) visual impairment such as unilateral neglect, and (4) musculoskeletal disorders of the upper extremities. All patients and their guardians provided informed consent in accordance with the Declaration of Helsinki. And, the study was approved by Institutional Review Board of the Busan Veterans Hospital, Busan (IRB no. 2018-1).

3. Intervention

The Ueda method basically includes neck, shoulder girdle, upper-extremity, lower extremity, and shoulder pelvis techniques. The shoulder girdle and upper-extremity techniques were applied to the Ueda group. The shoulder girdle technique is performed to reduce the muscle tone of the upper arm and shoulder girdle. The patients held the following positions for three minutes: slight shoulder abduction with maximum internal rotation, slight elbow flexion with maximum forearm pronation, wrist flexion, finger flexion, and thumb abduction (Figure 1). The upper-extremity technique was applied to reduce the hypertonus of the upper-extremity muscles and consists of the following three steps: (1) maintaining flexion for three minutes, (2) performing reciprocal movements of flexion and extension 30 times, and (3) maintaining flexion for three minutes again (Figure 2). For the upper-extremity technique, the following flexion positions of the upper extremities were employed: mid-position of the shoulder joint, elbow flexion, forearm pronation, wrist flexion, finger flexion, and thumb adduction. The extension positions performed as reciprocal movements of the upper extremities were as follows: shoulder abduction and external rotation, elbow extension, and wrist extension. All techniques were performed for 15 minutes in total.

Figure 1. Shoulder girdle technique.

Figure 2. Upper-extremity technique. [A] Flexion position. [B] Extension position.

The rehabilitation therapy applied to the convention group for 15 minutes included upper-extremity training (e.g., inhibition techniques and active/passive exercises) that involved the techniques of the Ueda method: flexion, extension, abduction, and adduction motion of the shoulder, flexion and extension motion of the elbow, pronation and supination motion of the forearm, flexion and extension motion of the wrist, and flexion and extension motion of the fingers.

4. Materials

We used wireless surface electromyography (EMG) (Noraxon TeleMyo Clinical DTS; Noraxon Inc., Scottsdale, AZ, USA) to compare the changes in stretch reflexes and activation ratios of the upper-extremity muscles. The EMG activities were collected at 1,000 Hz from six upper-extremity muscles. The Ag/AgCl surface electrodes were placed along the direction of the muscle fibers with a distance of 2 cm between electrodes. To reduce the skin resistance, the skin was wiped with a cotton pad soaked in alcohol to remove the foreign substances. The recorded muscles included the deltoid (anterior, lateral, posterior), biceps brachii, triceps brachii, and trapezius.

5. Measurements

To investigate the changes in stretch reflexes, all participants were seated on a comfortable chair. They were asked to refrain from moving their extremities and trunk; subsequently two surface electrodes were placed on the biceps brachii and triceps brachii, respectively. The experimenter supported the elbow joint (90° of shoulder flexion) and then performed passive extension and flexion movements of the elbow joint by holding the patient’s wrist. The passive range of elbow motion was 0°–120°, and the flexion and extension movements were repeated three times at an angular velocity of approximately 60° per second. The resting time was approximately eight seconds. The experimenter evaluated the spasticity grade during the passive range of elbow motion.

To evaluate changes in the activation ratios of the upper-extremity muscles, all participants were seated on a chair in front of a table. They were asked to place one hand on the table for measurement (90° elbow flexion, 0° shoulder flexion, and 40 abductions) and to place the other hand on their knee. Another experimenter fixed their trunk to minimize compensatory movements, which appear during voluntary arm reaching. The arm reaching protocol included the following four directions based on previous studies [27,28]: reaching forward from the anticardium height (Reach 1), 45-degree medial reach (Reach 2), 45-degree lateral reach (Reach 3), and reaching shoulder height (Reach 4). All targets were positioned at 90% of the maximum arm length of the participants. The cones for the occupational therapy were fixed at the position of each target. During the start of the reaching task, all participants were instructed to place their hands at the positions marked with a colored tape. After the start signal, they were seated in a comfortable starting position for five seconds; thereafter, they reached their arms out in the four directions as directed verbally by the experimenter. All participants performed the reaching tasks three times repeatedly toward the four targets and were given an inter-target interval of three seconds.

6. Data Processing

The EMG signals were bandpass-filtered (80–250 Hz) and notch-filtered (60 Hz) to remove noise using the Noraxon MR3.10 software (Noraxon Inc., Scottsdale, AZ, USA). Moreover, the root mean square (RMS) of the collected signals was computed, and the smoothed values were subsequently used for data analysis. Based on the study by Wang et al. [14], the A-ApA index, which is calculated using the RMS of agonist muscle activity by the mean between the RMS of agonistic and antagonistic muscle activations, was used to compare the stretch reflexes. This method can be employed to quantitatively evaluate the tension of elbow flexors and extensors based on the collected surface EMG signals, compare changes within participants, and identify differences between participants through normalization. The equation used was as follows:

where aRMS is the RMS of the agonist and antRMS is the RMS of the antagonist.

Changes in the activation ratios of the upper-extremity muscles were compared by conversion to the percentage of each muscle’s activity out of the sum of the total activity of the six upper-extremity muscles based on the percentage of reference voluntary contraction.

7. Statistical Analysis

The Consolidated Standards of Reporting Trials (CONSORT) flow diagram of the participants is shown in Figure 3. Among the 30 stroke patients analyzed in this study, two patients were excluded from the analysis: (1) one patient who did not complete the reaching task and (2) one patient with missing EMG data. Statistical analysis was performed using SPSS ver. 18.0 for Windows (IBM Co., Armonk, NY, USA). A paired t-test was used to confirm the changes in the A-ApA index and activation ratios of the upper-extremity muscles after the intervention. Repeated-measures analysis of variance (ANOVA) was used to confirm the therapeutic effect (2 × 2) as a function of group (Ueda vs. convention) and time (before/after the intervention) on all outcome measures. Statistical significance was set at p < 0.05 for all analyses. Cohen’s d effect size was obtained as an indicator of the effect size for the paired t-test, and partial eta squared was obtained for the repeated-measures ANOVA.

Figure 3. Consolidated Standards of Reporting Trials flow diagram. EMG, electromyography.

The demographic and clinical characteristics of both groups as well as their spasticity clinical measurements are summarized in Table 1.

Table 1 . Characteristics of the study sample (N = 28).

	Ueda group (n = 14)	Convention group (n = 14)
Demographic characteristic
Age (y)	49 ± 8.31	54 ± 9.95
Sex
Female	2 (14%)	5 (36%)
Male	12 (86%)	9 (64%)
Medical characteristic
Time after onset (mo)	21 ± 10.30	22 ± 18.13
Side of injury
Right	8 (57%)	9 (64%)
Left	6 (43%)	5 (36%)
MBI	68 ± 8.04	65 ± 7.81
Pre_MAS	1.93 ± 0.73	1.92 ± 0.86
Post_MAS	1.57 ± 0.94	2.08 ± 1.04

Values are presented as mean ± standard deviation or number (%). A score of 0 indicates MAS grade 0; score of 1, MAS grade 1; score of 2, MAS grade 1+; score of 3, MAS grade 2; score of 4, MAS grade 3; and score of 5, MAS grade 4. MBI, modified Barthel index; MAS, modified Ashworth scale..

In the Ueda group, the means of the A-ApA index before and after the intervention showed a significant decrease (p = 0.041), showing a weak evidence level; however, its effect size was medium (d = 0.503). Conversely, in the convention group, the means of the A-ApA index before (95% confidence interval, 0.62–0.74) and after (95% confidence interval, 0.63–0.81) the intervention did not show a sgnificant difference (p = 0.175); nonetheless, its effect size was small (d = 0.272; Table 2).

Table 2 . Mean changes in the A-ApA index after the intervention in both groups.

Group	Before (n = 14)			After (n = 14)		t	p-value
	Mean ± SD	95% CI		Mean ± SD	95% CI
Convention	0.68 ± 0.12	0.62–0.74		0.72 ± 0.17	0.63–0.81	–1.433	0.175
Ueda	0.77 ± 0.12	0.71–0.83		0.69 ± 0.19	0.59–0.79	2.286	0.041

Mean ± SD, mean ± standard deviation; CI, confidence interval..

The main effects of the A-ApA index before and after the intervention was not significant (p = 0.448). However, the interaction effects of the A-ApA index between the two methods (Ueda vs. convention) and between pre-intervention and post-intervention were significant (p = 0.012; Table 3), indicating that the improvement between the two methods after the intervention was significantly different. The evidence level for the interaction effects of the A-ApA index between the two methods and between pre-intervention and post-intervention was weak, but its effect size was large ($n_p^2$ = 0.220).

Table 3 . The A-ApA index before and after the intervention between the Ueda method and conventional method.

Parameter	SS	df	Mean square	F	p-value
Before-after	0.003	1	0.003	0.593	0.448
Methods before-after	0.041	1	0.041	7.314	0.012
Error	0.145	26	0.006

SS, sum of square; df, degree of freedom..

In the Ueda group, the activation ratio of the anterior deltoid fiber significantly decreased after the intervention in all reaching tasks. Effect sizes were medium for the Reach 1 task (d = 0.509), Reach 2 task (d = 0.686), and Reach 4 task (d = 0.651). The largest effect size was found for the Reach 3 task (d = 0.927). Nevertheless, no significant differences in the activation ratios of all other muscles during all reaching tasks were found (Table 4).

Table 4 . Changes in the activation ratios of the upper-extremity muscles in the Ueda group.

	Before (n = 14)			After (n = 14)		t	p-value	d
	Mean ± SD	95% CI		Mean ± SD	95% CI
Reach 1
Ant.Del	0.36 ± 0.12	0.30–0.42		0.31 ± 0.07	0.27–0.35	2.301	0.040	–0.509
Reach 2
Ant.Del	0.38 ± 0.12	0.32–0.44		0.31 ± 0.08	0.27–0.35	2.818	0.016	–0.686
Reach 3
Ant.Del	0.31 ± 0.10	0.26–0.36		0.23 ± 0.07	0.19–0.27	3.098	0.009	–0.927
Reach 4
Ant.Del	0.35 ± 0.11	0.29–0.41		0.29 ± 0.07	0.25–0.33	2.267	0.043	–0.651

Mean ± SD, mean ± standard deviation; CI, confidence interval; Ant.Del, anterior deltoid..

In the convention group, the activation ratios of all upper-extremity muscles after applying the intervention were not significantly different in all reaching tasks, and the effect sizes were weak or had no effect (Table 5).

Table 5 . Changes in the activation ratios of the upper-extremity muscles in the convention group.

	Before (n = 14)			After (n = 14)		t	p-value	d
	Mean ± SD	95% CI		Mean ± SD	95% CI
Reach 1
Ant.Del	0.27 ± 0.08	0.23–0.31		0.25 ± 0.06	0.22–0.28	1.264	0.230	–0.283
Reach 2
Ant.Del	0.27 ± 0.09	0.22–0.32		0.26 ± 0.08	0.22–0.30	0.683	0.508	–0.117
Reach 3
Ant.Del	0.24 ± 0.07	0.20–0.28		0.22 ± 0.06	0.19–0.25	0.964	0.354	–0.307
Reach 4
Ant.Del	0.23 ± 0.08	0.19–0.27		0.25 ± 0.06	0.22–0.28	0.676	0.512	0.283

Mean ± SD, mean ± standard deviation; CI, confidence interval; Ant.Del, anterior deltoid..

The typical characteristic of spasticity is the hyperexcitability of the tonic stretch reflex [29]. Therefore, we attempted to investigate the effects of the Ueda method on upper-extremity flexor spasticity by measuring the changes in stretch reflexes. Our results indicated that the stretch reflex was significantly more reduced in the Ueda group than in the convention group.

Various methods using specific equipment have been attempted to reduce spasticity. Málly and Dinya [30] applied transcranial magnetic stimulation to stroke patients and reported that this improved patients’ functional behaviors, movements, and upper-extremity spasticity. In the study by Chang et al. [31], passive therapy with robotic-assist therapeutic devices were applied to 14 patients with a completely injured spinal cord for four weeks. The study showed that the MAS scores were improved and recovered from post-activation depression after the intervention. In our study applying the Ueda method, MAS scores were slightly different but not statistically significant (Table 1). This results suggest that clinical measurement such as MAS, when compared to electrophysical measurement may not be sufficient to detect the changes in subtle muscle tone from spastic stroke patients.

In clinical practice, it is important to note that these methods may not be applicable to the number of stroke patients, since it requires costly equipment and creates a great amount of noise in an enclosed space. In contrast, the Ueda method has the advantage of convenience without any special equipment, and neither requires excessive force nor causes pain to patients. According to the above studies, the common therapeutic principle that author suggest is that control of excitability of the spinal cord circuitry should reduce spasticity. Given these interpretations, the Ueda method should have attributed to reducing spasticity by regulating the excitement of the spinal cord circuit and driving the reciprocal inhibition circuit.

The abnormal synergies of a limb after stroke reflect co-contraction due to the interferences on the reciprocal inhibition circuit of the agonist and antagonist [8,10]. In particular, the activity of the middle deltoid fiber increases along with that of the anterior deltoid fiber during arm reaching [32]. Therefore, we compared the changes in the activity ratio of the upper-extremity muscles to verify the effectiveness of the Ueda method on the upper-extremity flexion synergies. We found that the activation ratio of the anterior deltoid fiber after the intervention significantly decreased during all reaching tasks. This result implies that the techniques used in this study can change the upper-extremity flexion synergies. Interestingly, the most significant effective changes occurred in the anterior deltoid fiber among the measured upper-extremity muscles. We assume that this is because the target muscles of the shoulder girdle and the upper-extremity technique are the flexors of the upper extremities.

In the case study performed by Tojo [25], the Ueda method was applied for six weeks to children with severe motor injuries and intellectual disabilities due to drowning accident. In a subsequent study performed by Tojo [26], which involved two children with cerebral palsy, reported that spasticity was significantly reduced, and the children were able to relax their posture easily. However, these studies have only been descriptive reports of a few cases without scientific analysis. Thus far, because the Ueda method has not been systemically validated in stroke patients, the benefits of this method are not well understood. This study was the first to use an electrophysiological technique in the upper-extremity muscles to identify the possibility of applying the Ueda method in adult stroke patients. In this study, we demonstrated the effects of the Ueda method in reducing the exaggerated stretch reflex of the biceps brachii and found the effective changes in the flexor synergies of the upper extremities during arm reaching. Our results showed the possibility of restoring the altered circuit at the brainstem and spinal levels by the Ueda method. Moreover, given that the Ueda method was applied only once in this study, the change in the upper-extremity synergies during the active behavior that is immediately present, as well as the change in the reflex during a passive stretch, is a positive result.

There are, however, some problems that remain to be solved in this study. Firstly, it remains unclear whether all results lead to the improvement in motor function. Secondly, the long-term effects after the application of the Ueda method were not investigated. Thirdly, the sample size was small. Finally, the effects of the two techniques used in this study (i.e., shoulder girdle and upper-extremity techniques) were not distinguished.

We confirmed that the application of the Ueda method effectively should change upper-extremity flexor spasticity and upper-extremity flexion synergies in stroke patients. Hence, we suggest that the Ueda method should be considered as a rehabilitation therapy for stroke patients with spasticity. This study is clinically significant, as it introduced a new concept of rehabilitation therapy that should address the limitations of conventional therapy, which should be difficult to perform in patients with spasticity. Further studies with larger samples are required to confirm the correlation between electrophysiological changes and improved motor function after applying the Ueda method. Moreover, we will need to design a study with longer follow-up periods to verify the effectiveness of the method according to its specific techniques and steps.

None.

This study was supported by a Veterans Health Service Medical Center Research Grant, Republic of Korea, grant number VHSMC18025.

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

Conceptualization: YHR. Data curation: YHR, JBS, KHP, BSK, JCH. Formal analysis: YHR, JBS. Funding acquisition: YHR. Investigation: YHR, KHL, JBS, KHP, BSK, JCH. Methodology: YHR, KHL, JBS, KHP. Project administration: YHR, KHL, BSK, JCH. Resources: YHR, KHL, KHP, BSK, JCH. Supervision: YHR, KHL, JBS. Validation: YHR. Visualization: JBS. Writing - original draft: YHR, JBS. Writing- review & editing: YHR.