Combining Afferent Stimulation and Mirror Therapy for Rehabilitating Motor Function,Motor Control,Ambulation,and Daily Functions After Stroke

Abstract

Background. Mirror therapy (MT) and mesh glove (MG) afferent stimulation may be effective in reducing motor impairment after stroke. A hybrid intervention of MT combined with MG (MT + MG) may broaden aspects of treatment benefits. Objective. To demonstrate the comparative effects of MG + MT, MT, and a control treatment (CT) on the outcomes of motor impairments, manual dexterity, ambulation function, motor control, and daily function. Methods. Forty-three chronic stroke patients with mild to moderate upper extremity impairment were randomly assigned to receive MT + MG, MT, or CT for 1.5 hours/day, 5 days/week for 4 weeks. Outcome measures were the Fugl-Meyer Assessment (FMA) and muscle tone measured by Myoton-3 for motor impairment and the Box and Block Test (BBT) and 10-Meter Walk Test (10 MWT) for motor function. Secondary outcomes included kinematic parameters for motor control and the Motor Activity Log and ABILHAND Questionnaire for daily function. Results. FMA total scores were significantly higher and synergistic shoulder abduction during reach was less in the MT + MG and MT groups compared with the CT group. Performance on the BBT and the 10 MWT (velocity and stride length in self-paced task and velocity in as-quickly-as-possible task) were improved after MT + MG compared with MT. Conclusions. MT + MG improved manual dexterity and ambulation. MT + MG and MT reduced motor impairment and synergistic shoulder abduction more than CT. Future studies may integrate functional task practice into treatments to enhance functional outcomes in patients with various levels of motor severity. The long-term effects of MG + MT remain to be evaluated.

Keywords

stroke rehabilitation mirror therapy electrical stimulation kinematics activities of daily living

Introduction

Stroke has become the most frequent cause of adult-onset disability and costs a tremendous amount of related care expense.¹ About 65% of people after stroke experience difficulty in incorporating the affected hand into activities.¹ Several novel and theory-based rehabilitation interventions have been developed to improve motor recovery of the upper extremity (UE).² Among novel interventions, mirror therapy (MT) was beneficial and comparatively low cost.²

Substantial evidence showed that MT reduced UE motor impairment, as measured by the Fugl-Meyer Assessment (FMA). Reduced impairments might result from recruiting the premotor cortex or balancing neural activation within the primary motor cortex toward the affected hemisphere.^2-4 The benefits in certain aspects of outcomes are inconclusive, however; for instance, Cacchio et al⁵ found MT improved hand function, but others² reported no significant effect. Results of research on the effects of MT on spasticity, ambulation function, and daily function have been inconsistent.^5-10

Another compelling approach is afferent sensory stimulation applied to the UE, which was beneficial for motor recovery, as demonstrated by the FMA.¹¹ One type of afferent stimulation is provided by the mesh glove (MG; Prizm-Medical Inc, Oakwood, GA). The MG uses a 2-channel electrical stimulator to provide synchronous or reciprocal sensory stimulation with variant amplitudes and can provide stimulation of the entire hand. The MG can be used to reduce muscle hypertonia and facilitate residual movement, which may ameliorate motor impairment and increase volitional activity of the hand and arm in stroke patients.^12,13 A study by Zehr et al¹⁴ also suggests that stimulation of the superficial radial nerve at the wrist may increase dorsiflexion bilaterally in the stance-swing transition of ambulation. Providing MG stimulation might also result in plastic changes in the primary motor cortex¹⁵ and induce a long-lasting effect on motor cortical excitability.^16-18

Combining 2 treatment protocols has been advocated as a way to improve treatment efficacy.^19-21 MG stimulation could be used to supplement other treatment,²² such as MT, to normalize muscle tone and enhance hand or ambulation function. Besides, the possible mechanism of brain plasticity underlying MG is similar to the mechanism behind MT, in that the primary motor cortex might be activated. Adding MG to MT might further augment cortical reorganization.^19,20 MG stimulation added to MT improved manual dexterity and ability to transfer skill during daily activities.²³ However, this pilot study did not recruit a control group and therefore could not estimate a possible gained value, if any, in providing this new approach. The present study included a larger sample of stroke patients, a control group that received task-oriented therapy, and further explored the possible benefits of MT coupled with MG.

This study used the Myoton-3 myometer to objectively assess the treatment effects on muscle tone in the UE instead of a subjective measure such as the Modified Ashworth Scale (MAS).²⁴ This study also included kinematic analyses to obtain objective information on spatial and temporal characteristics (eg, movement time, displacement, and joint recruitment) of UE movements. Kinematic analysis helps us understand whether a true change in the end point control and joint motion/synergy patterns has occurred^21,25,26 and infer possible reorganization of the brain after treatment.^27,28 No previous research, to our knowledge, has addressed change in the motor control mechanism after MT.

The present study combined MG stimulation with MT (MT + MG) and compared the efficacy of MT + MG, MT, and a control therapy (CT) on motor impairment, as measured by the FMA and Myoton-3, and on motor function, as measured by the Box and Block Test (BBT) and 10-Meter Walk Test (10-MWT). Also investigated were strategies of motor control indicated by kinematic parameters and function in daily life situations measured by the Motor Activity Log (MAL) and ABILHAND questionnaire. Possible adverse effects, including pain and fatigue, were monitored.

Methods

Participants

The study recruited 43 patients (11 women) with stroke from 4 medical centers who had met the following criteria: (a) onset of an ischemic or hemorrhagic stroke of at least 6 months duration; (b) the ability to reach Brunnstrom stage III or above in the proximal and distal part of the arm; (c) no severe spasticity in any joints of the affected arm (Modified Ashworth Scale ≤ 2)²⁹; (d) no serious cognitive deficits (Mini-Mental State Examination score > 24)³⁰; (e) no serious vision or visual perception deficits (score of 0 on the best gaze and visual subtest of the National Institutes of Health Stroke Scale)³¹; (f) no history of other neurologic, neuromuscular, or orthopedic disease; and (g) no participation in other studies concurrent with this study. Participants signed informed consent forms approved by the institutional review boards of the participating facilities.

Design

The study was a single-blind, randomized, pretest and posttest control group design (Figure 1). Participants were stratified into 4 strata according to the side of lesion and the level of motor impairment (the cutoff point was 40 in total scores of the FMA UE subtest³²). A set of numbered envelopes containing cards indicating the allocated group was prepared for each stratum. When a new eligible participant was registered, an envelope was randomly extracted, and the relevant therapist was informed of the group allocation.

Figure 1.

Flow diagram shows enrollment of patients and completion of study according to the CONSORT statement.

Four certified occupational therapists were trained in the administration of these 3 protocols by 2 primary investigators to conduct consistent intervention. Outcome measurements were administered at baseline and immediately after the intervention by 2 trained occupational therapists. The evaluators were unaware of group allocation, and the participants were blinded to the study hypotheses.

Interventions

All participants received a 1.5-hour training session per day, 5 days/week for 4 weeks. The treatments were provided during the daily occupational therapy sessions. All other routine interdisciplinary stroke rehabilitation was continued as usual.

MT Protocol

The MT protocol included 10 minutes of warm-up, 1 hour of mirror box training, and 20 minutes of functional task practice. The warm-up activities included stretching and passive range of motion exercises. During the mirror box training, a mirror box that reflected the image of the unaffected arm was placed in the participant’s midsagittal plane. Participants were required to symmetrically move both hands as simultaneously as possible while watching the reflection of the unaffected arm in the mirror as if it were the affected one. To ensure that the participants focused on the reflection, the unaffected arm was placed in the mirror box, and vision of the affected arm was occluded by a vertical board placed beside the mirror box. The activities consisted of transitive (eg, gross motor tasks, such as reaching out to put a cup on a shelf, or fine motor tasks, such as picking up marbles) and intransitive movements (eg, gross motor movements, such as pronation and supination, or fine motor movements, such as finger opposition). After the mirror box training, functional task practice was provided according to task-oriented treatment principles.

MG Stimulation Combined With MT

The protocols of the MT + MG group were similar to the MT group (ie, 10 minutes of warm-up, 1 hour of mirror box training, and 20 minutes of functional task practice). The MT + MG group also wore the MG during mirror box training (Figure 2). For safety reasons, the conscious sensory threshold, with a feeling of tingling on palmar and dorsal sides, was set on the unaffected hand. Then, the MG was applied on the affected hand.

Figure 2.

The intervention setup of mesh-glove stimulation combined with mirror therapy.

The MG protocol depended on the muscle tone of the participants. Participants with a MAS score of 2 points in any joint of the affected hand received 2-step electrical stimulation. The first step was 80% of the conscious sensory threshold that was a subthreshold, and the second step was at the conscious sensory threshold. Each step lasted about 30 minutes. Participants with a MAS score lower than 2 points received 3-step electrical stimulation. The first 2 steps were the same as that mentioned above, and step 3 was stimulation above the threshold, defined by 120% of the conscious sensory threshold. Each step took 20 minutes.¹⁶ The subthreshold stimulation could decrease spasticity, and stimulation at the threshold or higher could improve awareness of the hand and enhance volitional activity.^16,18,33

CT Group

The CT group received 1.5 hours of therapeutic activities equivalent in duration and intensity to the MT + MG and MT groups, based on task-oriented treatment principles. Tasks used for practice were selected in accord with the abilities of the participants. In addition to functional task practice, this group also received warm-up similar to the other 2 groups.

Outcome Measures

This study included clinical measures for motor impairment, motor function, daily function, and adverse effects, and kinematic data for motor control. All measures have been reported to be adequately reliable and valid.^24,34-38

Primary Outcomes

Motor impairment

The UE subscale of FMA total score was used to evaluate several dimensions of motor impairments. The FMA measures the movements and reflexes of the UEs and coordination/speed on a 3-point ordinal scale (0 = cannot perform; 1 = can perform partially; 2 = can perform fully).³⁴

We used myotonometric measurements obtained with the Myoton-3 device (Muomeetria AS, Tallinn, Estonia) to assess the tone of skeletal muscles. The Myotone-3, which is placed perpendicular to the skin surface above the muscle to be tested, produces a short impulse on the muscle. An acceleration transducer records the damped oscillations of the muscle response. The muscle tone values of the biceps, flexor carpi radialis, and flexor carpi ulnaris were recorded.²⁴

Motor function

The BBT was used to assess manual dexterity. A box is separated into 2 equal sides. Subjects used the affected hand to move as many blocks as possible, one at a time, from one side to the other in 60 seconds. The number of blocks is calculated at the end of the test.³⁵

The 10-MWT was used to assess the mobility function, measuring the time and the numbers of strides required to walk 10 meters under 2 conditions: (a) each participant’s self-pace (self-pace) and (b) the quickest speed that each participant could walk (as quickly as possible [AQAP]).³⁶ The velocity and stride length of the participant were calculated.

Secondary Outcomes

Daily function

The MAL is a semistructured interview that assesses subjective report of 30 common daily tasks evaluating the frequency of affected UE use. It consists of subscales assessing the amount of use (AOU) and quality of movement (QOM). The MAL uses a 6-point ordinal scale, with higher scores indicating better performance.³⁷

The ABILHAND questionnaire is a self-report assessment of UE function that consists of 23 bilateral activities in daily life. Patients were asked to estimate their difficulty in performing each activity using a 3-point ordinal scale. The higher the scores, the more difficulty the patients feel.³⁸ The Rasch model was used to estimate a linear ability for each patient and linear difficulty for each item.³⁸

Motor control

The experimental task required participants to press a desk bell with their affected hand as quickly as possible. Participants sat on a height-adjustable, straight-backed chair with the seat height set to 100% of the lower leg length. The tested arm was pronated, and the hand rested on the edge of the table in a neutral position with 90° flexion at the elbow joint. The desk bell was placed in the midline of the table. The bell distance, measuring from the medial border of the axilla to the bell, was standardized to 125% of the participant’s functional arm length (defined as from the medial border of the axilla to the distal wrist crease³⁹). If the maximum distance the participant could reach was less than 125% of the functional arm length, the bell distance was adjusted to the maximum reachable distance. The instruction to the participants was, “When you hear the start signal ring, please use the index finger of the affected hand to reach and press the bell as fast as possible.” After a practice trial, 3 trials were performed.

A 7-camera motion capture system (VICON MX, Oxford Metrics Inc, Oxford, UK) at a sampling frequency of 120 Hz was used with a personal computer to record kinematic data. Three channels of analog signals were collected simultaneously: one for instruction of movement start and the others for target bells. Markers were placed on the acromion, middle of humerus, lateral epicondyle, styloid process of ulna and radius, and index nail of the affected side. Movement onset was defined as a rise of tangential wrist velocity above 5% of its peak value. Movement offset was defined as a fall of tangential wrist velocity below 5% of its peak value. Movement was digitally low-pass filtered at 5 Hz using a second-order Butterworth filter with forward and backward pass.

Kinematic data were processed with an analysis program coded by LabVIEW language (National Instruments, Inc, Austin, TX). Kinematic variables included normalized movement time and normalized movement units to represent end point control, and joint recruitment, including normalized shoulder flexion, normalized elbow extension, and maximum shoulder abduction, to describe movement patterns. Movement time, which refers to the execution time of the reaching movement and is the interval between movement onset and offset, was a variable to represent temporal efficiency.^40,41 Movement unit was defined as 1 acceleration and 1 deceleration, which refers to motor smoothness.^40,41 Joint recruitment was defined as the difference of shoulder flexion or elbow extension from movement onset and movement offset, and maximum shoulder abduction during each reaching motion. Maximum shoulder abduction and elbow flexion are 2 critical components of the flexor synergy pattern often exhibited by patients with stroke.^42,43 Reduced maximum shoulder abduction with enhanced elbow extension indicates a diminished synergy pattern.⁴² Because bell distance varied, depending on the individual’s arm length, and therefore influenced reaching distance (defined as the distance between the initial index marker position at resting and the target desk bell), all variables, except for maximum shoulder abduction, were normalized to reaching distance.

Possible adverse effects

Self-reported assessments on pain and fatigue severity were administered immediately after the first and last treatment sessions to evaluate adverse effects. The evaluator presented the question, “What did you feel in terms of pain/fatigue severity during the treatment today?” The participant responded on an 11-point ordinal scale (0 = no pain/fatigue; 10 = the most severe pain/fatigue).

Data Analysis

Data were analyzed with SPSS 19.0 software (SPSS Inc, Chicago, IL). We calculated that a sample size of 42 was needed for an 80% likelihood in detecting a group difference with a type I error of .05, based on the previous pilot study showing that MT combined with afferent stimulation resulted in improvements with effect sizes of approximately .50.²³ Baseline differences among groups were analyzed by analysis of variance for continuous data and by χ² for categorical data. To control the variance among groups in the pretest scores, analysis of covariance was used to compare the treatment effects among groups on different end points at posttest. The pretest performance was the covariate, group was the independent variable, and posttest performance was the dependent variable. No multiple testing corrections were made to restrain the type II error considering the early stage of intervention development.

Post hoc analysis using highly significant differences was used to evaluate the difference of each group. The η² was calculated for each outcome variable to index the magnitude of group differences. The η² value represents the variability in the dependent variable (posttest performance) that can be explained by the independent variable (group). A large effect is represented by an η² of at least 0.14, a moderate effect by an η² of 0.06, and a small effect by an η² of 0.01. The level of statistical significance (α) was set at .05 for all comparisons.⁴⁴

Results

The study recruited 43 participants (mean age = 55.0 years). The MT + MG and the MT group consisted of 14 participants each, and the CT group consisted of 15 participants. After the treatment programs, the Myoton and kinematic data were missing for 2 participants. There were no significant differences in demographic characteristics among groups (Table 1). Group differences were not significant for pain (F_2,39 = 1.65, P = .06) and fatigue (F_2,39 = 3.05, P = .21).

Table 1.

Characteristics of Study Participants (N = 43).

Variable	MT + MG (n = 14)	MT (n = 14)	CT (n = 15)	Statistic^a	P Value
Gender, n				0.02	.90
Male	11	10	11
Female	3	4	4
Age (years), $\bar{X}$ (SD)	55.79 (14.59)	56.01 (12.53)	53.34 (10.12)	0.21	.82
Side of brain lesion, n				0.62	.74
Right	8	6	8
Left	6	8	7
Months after stroke onset, $\bar{X}$ (SD)	22.71 (13.62)	18.50 (11.61)	17.80 (10.56)	0.70	.50
Years of education, $\bar{X}$ (SD)	10.54 (5.01)	11.07 (4.75)	11.17 (3.71)	0.08	.93
Brunnstroms stage, $\bar{X}$ (SD)
Proximal	4.25 (0.64)	4.25 (0.64)	4.17 (0.62)	0.33	.85
Distal	4.11 (0.86)	4.00 (0.83)	4.10 (0.83)	0.12	.94
MMSE, $\bar{X}$ (SD)	27.62 (2.47)	27.91 (1.76)	28.21 (2.15)	0.26	.77

Abbreviations: MT + MG, mirror therapy combined with mesh glove; MT, mirror therapy; CT, control treatment; MMSE, Mini-Mental State Examination.

Statistic associated with χ² test or the Fisher exact test for categorical variables, 1-way analysis of variance for continuous variables, and nonparametric test for ordinal variables.

Primary Outcomes

Table 2 reports the descriptive and inferential results, except the kinematic performance. Total FMA scores were significantly different, with a large effect among the 3 groups (F_2,40 = 3.35, P = .045, η² = .147). Post hoc analyses revealed that the MT + MG and the MT groups were significantly higher than the CT group for the FMA total score (P = .0032 and .0031, respectively). Group differences in the muscle tone were not significant.

Table 2.

Descriptive and Inferential Statistics for Clinical Outcome Measures.

Variable	Pretest ( $\bar{X}$ ± SD)			Posttest ( $\bar{X}$ ± SD)			ANCOVA
Variable	MT + MG	MT	CT	MT + MG	MT	CT	F	P	η²
FMA	(n = 14)	(n = 14)	(n = 15)	(n = 14)	(n = 14)	(n = 15)	F _2,40
Proximal	31.86 (4.77)	30.50 (4.00)	31.13 (4.36)	34.43 (4.91)	33.57 (3.99)	32.73 (3.83)	2.004	.15	.09
Distal	13.57 (6.90)	13.71 (7.37)	12.67 (7.66)	16.50 (6.67)	16.29 (5.62)	14.40 (7.53)	1.614	.21	.08
Total	45.43 (9.23)	44.21 (10.69)	43.80 (10.68)	50.93 (9.41)	49.86 (8.97)	47.13 (10.12)	3.350	.045^a	.15
Myoton	(n = 14)	(n = 13)	(n = 14)	(n = 14)	(n = 13)	(n = 14)	F _2,38
Biceps	14.41 (1.86)	13.39 (2.23)	13.87 (3.45)	14.16 (1.67)	12.90 (1.98)	12.56 (1.64)	2.200	.13	.11
Flexor carpi radialis	15.85 (2.19)	14.13 (2.38)	15.41 (2.61)	15.45 (3.20)	15.17 (1.59)	15.20 (2.46)	0.129	.88	.007
Flexor carpi ulnaris	14.15 (2.47)	13.57 (2.56)	13.15 (7.13)	14.34 (2.49)	13.75 (2.16)	12.28 (6.15)	1.68	.20	.083
BBT affected hand	12.00 (11.11)	16.43 (14.41)	15.73 (14.38)	17.29 (12.38)	16.93 (16.46)	19.93 (15.23)	4.392	.02^a	.18
10 MWT	(n = 14)	(n = 14)	(n = 15)	(n = 14)	(n = 14)	(n = 15)	F _2,40
Self-paced velocity (m/s)	0.557 (0.234)	0.707 (0.317)	0.580 (0.268)	0.658 (0.284)	0.697 (0.314)	0.649 (0.251)	5.020	.01^a	.21
Self-paced stride length (m)	0.377 (0.120)	0.444 (0.144)	0.415 (0.118)	0.430 (0.130)	0.431 (0.145)	0.443 (0.098)	7.129	.002^a	.27
AQAP velocity (m/s)	0.772 (0.293)	0.916 (0.418)	0.796 (0.383)	0.878 (0.355)	0.914 (0.441)	0.873 (0.378)	4.061	.03^a	.18
AQAP stride length (m)	0.453 (0.151)	0.496 (0.163)	0.522 (0.235)	0.523 (0.206)	0.491 (0.178)	0.522 (0.119)	0.787	.46	.04
MAL	(n = 14)	(n = 14)	(n = 15)	(n = 14)	(n = 14)	(n = 15)	F _2,40
AOU	1.00 (1.05)	1.35 (1.07)	0.86 (0.97)	1.23 (0.89)	1.43 (1.09)	1.14 (1.25)	0.796	.46	.04
QOM	1.09 (1.18)	1.31 (1.02)	0.97 (1.02)	1.22 (1.02)	1.61 (1.19)	1.18 (1.10)	0.617	.55	.03
ABILHAND total score	29.14 (8.74)	38.43 (12.91)	28.00 (14.27)	33.07 (11.27)	40.64 (13.25)	34.13 (14.18)	0.215	.81	.01

Abbreviations: ANCOVA, analysis of covariance; MT + MG, mirror therapy combined with mesh glove; MT, mirror therapy; CT, control treatment; FMA, Fugl-Meyer Assessment; BBT, Box and Block Test; 10 MWT, 10-Meter Walk Test; AQAP, as quickly as possible; MAL, Motor Activity Log; AOU, amount of use; QOM, quality of movement.

P < .05.

Significant and large effects on motor function were measured by the BBT (F_2,40 = 4.39, P = .019, η² = .184) and the 10-MWT (velocity of self-pace: F_2,40 = 5.02, P = .011, η² = .205; stride of self-pace: F_2,40 = 7.13, P = .002, η² = .268; velocity of AQAP: F_2,40 = 4.06, P = .025, η² = .176). No significant difference was found in stride length of the AQAP subscores in the10-MWT. Post hoc analyses revealed that the MT + MG and the CT group improved more than the MT group in the BBT (P = .007 and P = .036, respectively). The MG + MT group showed larger improvements than the MT group on the velocity of self-paced ambulation (P = .004), the stride of self-paced ambulation (P = .016), and the velocity of AQAP (P = .014). The CT group showed larger improvements than the MT group on the velocity of self-paced ambulation (P = .031), the stride of self-paced ambulation (P = .016), and the velocity of AQAP (P = .023).

Secondary Outcomes

For daily function, no significant group effects were found on the ABILHAND or on the AOU and QOM of the MAL. Table 3 reports the descriptive and inferential results for the kinematic performance. The results revealed significant and large effects on normalized shoulder flexion (F_2,38 = 3.43, P = .043, η² = .157) and reduction of maximum shoulder abduction during reach (F_2,38 = 4.55, P = .017, η² = .198) among the 3 groups. Post hoc analyses revealed that the MG + MT (P = .008) and the MT groups (P = .023) showed significantly greater reduction of maximum shoulder abduction than the CT group. The CT group showed larger improvements than the MT group on normalized shoulder flexion (P = .0013). Small and nonsignificant effects were found on normalized movement time, normalized movement unit, and the normalized elbow extension.

Table 3.

Descriptive and Inferential Statistics for Analysis of Kinematics Performance.

	Pretest			Posttest			ANCOVA
Variable	MT + MG (n = 14)	MT (n = 13)	CT (n = 14)	MT + MG (n = 14)	MT (n = 13)	CT (n = 14)	F _2,38	P	η²
Wrist Nmt (s/mm)	0.0050 (0.0056)	0.0032 (0.0015)	0.0039 (0.0023)	0.0033 (0.0013)	0.0033 (0.0017)	0.0030 (0.0014)	0.713	.50	.04
Wrist nMU (unit/mm)	0.0270 (0.0391)	0.0153 (0.0113)	0.0202 (0.0160)	0.0137 (0.0082)	0.0154 (0.0108)	0.0131 (0.0079)	1.006	.38	.05
nShoulder flex (°/mm)	0.1490 (0.0287)	0.1470 (0.0412)	0.1450 (0.0263)	0.1469 (0.0265)	0.1313 (0.0247)	0.1582 (0.0336)	3.432	.04^a	.16
nElbow ext (°/mm)	0.0624 (0.0505)	0.0691 (0.0391)	0.0802 (0.0195)	0.0720 (0.0375)	0.0708 (0.0351)	0.0821 (0.0211)	0.279	.76	.02
Max shoulder abd (°/mm)	0.1526 (0.0415)	0.1432 (0.0253)	0.1316 (0.0250)	0.1333 (0.0258)	0.1328 (0.0229)	0.1474 (0.0303)	4.554	.02^a	.20

Abbreviations: ANCOVA, analysis of covariance; MT + MG, mirror therapy combined with mesh glove; MT, mirror therapy; CT, control treatment; nMT, normalized movement time; nMU, normalized motor unit; nShoulder flex, normalized angle recruitment of shoulder flexion; nElbow ext, normalized angle recruitment of elbow extension; Max shoulder abd, maximum angle recruitment of shoulder abduction.

P < .05.

Discussion

The present study demonstrated that patients in the MT + MG and MT groups performed better compared with those in the CT group in the reduction of motor impairment. Combining MT with MG stimulation showed additional effects on manual dexterity of the affected hand, self-paced ambulation, and velocity of quickly paced ambulation compared with MT alone. Relative to CT, MT + MG and MT reduced maximum shoulder abduction during forward reach, which is regarded as reducing a critical component of the flexor synergy pattern. However, CT increased shoulder flexion more than the other groups. For daily function, we found no group differences immediately after the 4-week interventions. There was no adverse effect as measured by self-reported pain and fatigue.

Compared with the CT group, the MT + MG and MT groups showed improved motor impairment as indicated by the FMA total scores, in line with previous research on MT.^2,6,10 As an explanation for the treatment effects, the visual input during MT could substitute for absent or reduced proprioceptive input from the affected body side⁴⁵ and, consequently, helped recruit the premotor cortex or balance the neural activation within the primary motor cortex toward the affected hemisphere to facilitate motor improvements.^3,4,46

We found MT combined with MG stimulation provided additional benefits on manual dexterity compared with MT alone, consistent with the findings of a pilot study on MT combined with somatosensory stimulation²³ and studies related to electrical stimulation.^47,48 The extra benefit on manual dexterity is very encouraging, considering its importance for activities of daily living⁴⁹ and that previous studies of MT showed unclear results on manual dexterity.^2,6 MG stimulation might induce rapid plastic change in sensorimotor regions of the cortex^16,17,50 related to the hand to which the stimulation was applied and modulate the intracortical γ-aminobutyric acid pathways that reduce intracortical inhibition in the motor cortex of the ipsilesional hemisphere.⁴⁸ Combining MT with MG could provide cross-modal inputs (ie, sensation from electric stimulation and visual image input from the mirror) during training that may modulate activation of the somatosensory cortex and facilitate dexterity recovery.^21,51

Another important finding is that combining MT with MG demonstrated significant improvements on ambulation function measured by the 10-MWT compared with MT alone. This finding is consistent with a pilot study²³ and some studies of electrical stimulation on the UE.^12,52 Stimulation of cutaneous nerves of the hand could elicit an interlimb reflex response in muscles across the body that is believed to be related to motor coordination between arms and legs during walking.^14,53 In addition, arm integration during reciprocal activities, which were part of the training, could alter leg movement via propriospinal neural pathways.⁵⁴ Improvement in UE motor control may contribute to arm swing and help generate forward propulsion at the foot.⁵⁵

Our kinematic results revealed that MT + MG or MT might reduce shoulder synergy movements, as indicated by less maximum shoulder abduction⁴² during elbow extension, compared with the CT group. According to the assumption of motor learning, the neural structures controlling movement are required to adapt to constraints imposed by, at least, physical demands.⁵⁶ MT restrained arm movement in a size-limited box, which might not allow for a great range of shoulder abduction during task performance. Consequently, the synergy pattern of shoulder abduction might be inhibited. This result can also be cross-validated by our findings of improved total FMA scores, because the FMA involves the ability to perform out-of-synergy movements,³⁴ the scores of the FMA indicated a reduction in shoulder synergy movement.⁵⁷ In contrast, the CT patients gained a greater amount of shoulder flexion than the MT + MG and MT patients. The CT involved a variety of therapeutic activities requiring shoulder forward flexion and elevation. Accordingly, the CT patients exhibited better improvement in shoulder flexion than patients receiving the other 2 treatments. Task-specific training has been shown to be effective in recovery of movement poststroke.⁵⁸

No group differences were noted in the muscle tone of the biceps, flexor carpi radialis, and flexor carpi ulnaris. One possibility is that our participants had mild to moderate spasticity (MAS ≤ 2) at pretest. Most participants in the MT + MG group received the 3-step MG stimulation protocol to increase awareness of the affected hand and enhance volitional activity rather than the protocol to reduce spasticity,^15,17,32 resulting in nonsignificant effects on spasticity.

We found no group differences in daily function, which is in accord with previous research.²³ However, a scrutiny of the descriptive data showed all groups improved in some activities of daily living outcomes, and additional statistical analysis showed significant differences between pre- and posttreatment for each group (P = .014-.047), indicating that all treatments were beneficial to daily function. Future research might include follow-up assessments to study possible changes in activities of daily living or incorporate more functional task practice into MT + MG or MT to improve function in daily-life situations.

As a limitation, our study included only people with mild to moderate motor impairments. Some studies have reported that patients with severe motor deficits achieved more improvements after interventions.⁵⁹ The evidence for optimal intensity of afferent stimulation (eg, electric current intensity) for stroke rehabilitation is limited.⁵⁹ Because we found no adverse effects using stimulation at the threshold level, it might be possible to increase the intensity of the electrical stimulation.⁵⁹

Conclusions

This study is unique in demonstrating the comparative effects of MT + MG, MT alone, and task-oriented therapy on a variety of motor and functional outcomes. MT + MG and MT alone improved motor impairment and reduced the critical component of synergy patterns (ie, shoulder abduction) more than CT. MT + MG yields broader aspects of motor recovery. Our study showed the benefits of combining MT and MG stimulation for improving manual dexterity and ambulation function. In addition, all treatments here showed benefits in daily function. Future research may address the dosing issue by studying the effects of stimulation intensity and integrating functional task practice in the MT + MG protocol in an attempt to optimize the effects on daily function.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This project was supported in part by the National Health Research Institutes (NHRI-EX101-9920PI and NHRI-EX101-10010PI), the National Science Council (NSC-100-2314-B-002-008-MY3 and NSC99-2314-B-182-014-MY3), and the Healthy Ageing Research Center at Chang Gung University (EMRPD1B0371) in Taiwan.

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