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508468

research-article2013
NNRXXX10.1177/1545968313508468Neurorehabilitation and Neural RepairLin et al

Clinical Reasearch Article


Neurorehabilitation and

Combining Afferent Stimulation and Mirror


Neural Repair
2014, Vol. 28(2) 153­–162
© The Author(s) 2013
Therapy for Rehabilitating Motor Function, Reprints and permissions:
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Motor Control, Ambulation, and Daily DOI: 10.1177/1545968313508468


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Functions After Stroke

Keh-chung Lin, ScD1,2, Pai-chuan Huang, ScD3, Yu-ting Chen, MS3,


Ching-yi Wu, ScD3, and Wen-ling Huang, MS4

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 spasticity, ambulation function, and daily function have


been inconsistent.5-10
Stroke has become the most frequent cause of adult-onset Another compelling approach is afferent sensory stimu-
disability and costs a tremendous amount of related care lation applied to the UE, which was beneficial for motor
expense.1 About 65% of people after stroke experience dif- recovery, as demonstrated by the FMA.11 One type of affer-
ficulty in incorporating the affected hand into activities.1 ent stimulation is provided by the mesh glove (MG; Prizm-
Several novel and theory-based rehabilitation interventions Medical Inc, Oakwood, GA). The MG uses a 2-channel
have been developed to improve motor recovery of the electrical stimulator to provide synchronous or reciprocal
upper extremity (UE).2 Among novel interventions, mirror sensory stimulation with variant amplitudes and can
therapy (MT) was beneficial and comparatively low cost.2
Substantial evidence showed that MT reduced UE motor
1
impairment, as measured by the Fugl-Meyer Assessment National Taiwan University, Taipei, Taiwan
2
National Taiwan University Hospital, Taipei, Taiwan
(FMA). Reduced impairments might result from recruiting 3
Chang Gung University, Taoyuan, Taiwan
the premotor cortex or balancing neural activation within 4
Chang Gung Medical Foundation, Taoyuan, Taiwan
the primary motor cortex toward the affected hemisphere.2-4
Corresponding Author:
The benefits in certain aspects of outcomes are inconclu-
Ching-yi Wu, Department of Occupational Therapy and Graduate
sive, however; for instance, Cacchio et al5 found MT Institute of Behavioral Sciences, College of Medicine, Chang Gung
improved hand function, but others2 reported no significant University, 259 Wenhua 1st Rd, Taoyuan 333, Taiwan.
effect. Results of research on the effects of MT on Email: cywu@mail.cgu.edu.tw

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154 Neurorehabilitation and Neural Repair 28(2)

and joint motion/synergy patterns has occurred21,25,26 and


Potentially eligible participants (n = 168)
infer possible reorganization of the brain after treatment.27,28
Enrollment

Excluded (n = 83) No previous research, to our knowledge, has addressed


Not meeting inclusion change in the motor control mechanism after MT.
criteria (n = 42) The present study combined MG stimulation with MT
Randomized (n = 43) (MT + MG) and compared the efficacy of MT + MG, MT,
and a control therapy (CT) on motor impairment, as mea-
Allocation

sured by the FMA and Myoton-3, and on motor function, as


MG+MT MT CT measured by the Box and Block Test (BBT) and 10-Meter
(n = 14) (n = 14) (n = 15) Walk Test (10-MWT). Also investigated were strategies of
motor control indicated by kinematic parameters and func-
Analysis

Analyzed Analyzed Analyzed tion in daily life situations measured by the Motor Activity
(n = 14) (n = 14) (n = 14) Log (MAL) and ABILHAND questionnaire. Possible
adverse effects, including pain and fatigue, were monitored.
Figure 1.  Flow diagram shows enrollment of patients and
completion of study according to the CONSORT statement. Methods
Abbreviations: CT, control therapy; MG, mesh glove; MT, mirror
therapy. Participants
The study recruited 43 patients (11 women) with stroke
provide stimulation of the entire hand. The MG can be used from 4 medical centers who had met the following criteria:
to reduce muscle hypertonia and facilitate residual move- (a) onset of an ischemic or hemorrhagic stroke of at least 6
ment, which may ameliorate motor impairment and increase months duration; (b) the ability to reach Brunnstrom stage
volitional activity of the hand and arm in stroke patients.12,13 III or above in the proximal and distal part of the arm; (c) no
A study by Zehr et al14 also suggests that stimulation of the severe spasticity in any joints of the affected arm (Modified
superficial radial nerve at the wrist may increase dorsiflex- Ashworth Scale ≤ 2)29; (d) no serious cognitive deficits
ion bilaterally in the stance-swing transition of ambulation. (Mini-Mental State Examination score > 24)30; (e) no seri-
Providing MG stimulation might also result in plastic ous vision or visual perception deficits (score of 0 on the
changes in the primary motor cortex15 and induce a long- best gaze and visual subtest of the National Institutes of
lasting effect on motor cortical excitability.16-18 Health Stroke Scale)31; (f) no history of other neurologic,
Combining 2 treatment protocols has been advocated as neuromuscular, or orthopedic disease; and (g) no participa-
a way to improve treatment efficacy.19-21 MG stimulation tion in other studies concurrent with this study. Participants
could be used to supplement other treatment,22 such as MT, signed informed consent forms approved by the institu-
to normalize muscle tone and enhance hand or ambulation tional review boards of the participating facilities.
function. Besides, the possible mechanism of brain plastic-
ity underlying MG is similar to the mechanism behind MT,
Design
in that the primary motor cortex might be activated. Adding
MG to MT might further augment cortical reorganiza- The study was a single-blind, randomized, pretest and
tion.19,20 MG stimulation added to MT improved manual posttest control group design (Figure 1). Participants were
dexterity and ability to transfer skill during daily activi- stratified into 4 strata according to the side of lesion and
ties.23 However, this pilot study did not recruit a control the level of motor impairment (the cutoff point was 40 in
group and therefore could not estimate a possible gained total scores of the FMA UE subtest32). A set of numbered
value, if any, in providing this new approach. The present envelopes containing cards indicating the allocated group
study included a larger sample of stroke patients, a control was prepared for each stratum. When a new eligible par-
group that received task-oriented therapy, and further ticipant was registered, an envelope was randomly
explored the possible benefits of MT coupled with MG. extracted, and the relevant therapist was informed of the
This study used the Myoton-3 myometer to objectively group allocation.
assess the treatment effects on muscle tone in the UE instead Four certified occupational therapists were trained in the
of a subjective measure such as the Modified Ashworth administration of these 3 protocols by 2 primary investiga-
Scale (MAS).24 This study also included kinematic analyses tors to conduct consistent intervention. Outcome measure-
to obtain objective information on spatial and temporal ments were administered at baseline and immediately after
characteristics (eg, movement time, displacement, and joint the intervention by 2 trained occupational therapists. The
recruitment) of UE movements. Kinematic analysis helps evaluators were unaware of group allocation, and the par-
us understand whether a true change in the end point control ticipants were blinded to the study hypotheses.

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Lin et al 155

unaffected hand. Then, the MG was applied on the affected


hand.
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 sen-
sory 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
Figure 2.  The intervention setup of mesh-glove stimulation
combined with mirror therapy. activity.16,18,33

CT Group.  The CT group received 1.5 hours of therapeutic


Interventions activities equivalent in duration and intensity to the MT +
All participants received a 1.5-hour training session per day, MG and MT groups, based on task-oriented treatment prin-
5 days/week for 4 weeks. The treatments were provided ciples. Tasks used for practice were selected in accord with
during the daily occupational therapy sessions. All other the abilities of the participants. In addition to functional
routine interdisciplinary stroke rehabilitation was continued task practice, this group also received warm-up similar to
as usual. the other 2 groups.

MT Protocol. The MT protocol included 10 minutes of


Outcome Measures
warm-up, 1 hour of mirror box training, and 20 minutes of
functional task practice. The warm-up activities included This study included clinical measures for motor impair-
stretching and passive range of motion exercises. During ment, motor function, daily function, and adverse effects,
the mirror box training, a mirror box that reflected the and kinematic data for motor control. All measures have
image of the unaffected arm was placed in the participant’s been reported to be adequately reliable and valid.24,34-38
midsagittal plane. Participants were required to symmetri-
cally move both hands as simultaneously as possible while Primary Outcomes
watching the reflection of the unaffected arm in the mirror Motor impairment.  The UE subscale of FMA total score
as if it were the affected one. To ensure that the participants was used to evaluate several dimensions of motor impair-
focused on the reflection, the unaffected arm was placed in ments. The FMA measures the movements and reflexes of
the mirror box, and vision of the affected arm was occluded the UEs and coordination/speed on a 3-point ordinal scale
by a vertical board placed beside the mirror box. The activi- (0 = cannot perform; 1 = can perform partially; 2 = can per-
ties consisted of transitive (eg, gross motor tasks, such as form fully).34
reaching out to put a cup on a shelf, or fine motor tasks, We used myotonometric measurements obtained with
such as picking up marbles) and intransitive movements the Myoton-3 device (Muomeetria AS, Tallinn, Estonia) to
(eg, gross motor movements, such as pronation and supina- assess the tone of skeletal muscles. The Myotone-3, which
tion, or fine motor movements, such as finger opposition). is placed perpendicular to the skin surface above the muscle
After the mirror box training, functional task practice was to be tested, produces a short impulse on the muscle. An
provided according to task-oriented treatment principles. acceleration transducer records the damped oscillations of
the muscle response. The muscle tone values of the biceps,
MG Stimulation Combined With MT.  The protocols of the MT flexor carpi radialis, and flexor carpi ulnaris were recorded.24
+ MG group were similar to the MT group (ie, 10 minutes
of warm-up, 1 hour of mirror box training, and 20 minutes Motor function.  The BBT was used to assess manual dex-
of functional task practice). The MT + MG group also wore terity. A box is separated into 2 equal sides. Subjects used
the MG during mirror box training (Figure 2). For safety the affected hand to move as many blocks as possible, one
reasons, the conscious sensory threshold, with a feeling of at a time, from one side to the other in 60 seconds. The num-
tingling on palmar and dorsal sides, was set on the ber of blocks is calculated at the end of the test.35

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156 Neurorehabilitation and Neural Repair 28(2)

The 10-MWT was used to assess the mobility function, Hz using a second-order Butterworth filter with forward
measuring the time and the numbers of strides required to and backward pass.
walk 10 meters under 2 conditions: (a) each participant’s Kinematic data were processed with an analysis program
self-pace (self-pace) and (b) the quickest speed that each coded by LabVIEW language (National Instruments, Inc,
participant could walk (as quickly as possible [AQAP]).36 Austin, TX). Kinematic variables included normalized
The velocity and stride length of the participant were movement time and normalized movement units to repre-
calculated. sent end point control, and joint recruitment, including nor-
malized shoulder flexion, normalized elbow extension, and
Secondary Outcomes maximum shoulder abduction, to describe movement pat-
Daily function. The MAL is a semistructured interview terns. Movement time, which refers to the execution time of
that assesses subjective report of 30 common daily tasks the reaching movement and is the interval between move-
evaluating the frequency of affected UE use. It consists of ment onset and offset, was a variable to represent temporal
subscales assessing the amount of use (AOU) and quality of efficiency.40,41 Movement unit was defined as 1 acceleration
movement (QOM). The MAL uses a 6-point ordinal scale, and 1 deceleration, which refers to motor smoothness.40,41
with higher scores indicating better performance.37 Joint recruitment was defined as the difference of shoulder
The ABILHAND questionnaire is a self-report assess- flexion or elbow extension from movement onset and
ment of UE function that consists of 23 bilateral activities in movement offset, and maximum shoulder abduction during
daily life. Patients were asked to estimate their difficulty in each reaching motion. Maximum shoulder abduction and
performing each activity using a 3-point ordinal scale. The elbow flexion are 2 critical components of the flexor syn-
higher the scores, the more difficulty the patients feel.38 The ergy pattern often exhibited by patients with stroke.42,43
Rasch model was used to estimate a linear ability for each Reduced maximum shoulder abduction with enhanced
patient and linear difficulty for each item.38 elbow extension indicates a diminished synergy pattern.42
Because bell distance varied, depending on the individual’s
Motor control. The experimental task required par- arm length, and therefore influenced reaching distance
ticipants to press a desk bell with their affected hand as (defined as the distance between the initial index marker
quickly as possible. Participants sat on a height-adjustable, position at resting and the target desk bell), all variables,
straight-backed chair with the seat height set to 100% of except for maximum shoulder abduction, were normalized
the lower leg length. The tested arm was pronated, and to reaching distance.
the hand rested on the edge of the table in a neutral posi-
tion with 90° flexion at the elbow joint. The desk bell was Possible adverse effects. Self-reported assessments on
placed in the midline of the table. The bell distance, mea- pain and fatigue severity were administered immediately
suring from the medial border of the axilla to the bell, was after the first and last treatment sessions to evaluate adverse
standardized to 125% of the participant’s functional arm effects. The evaluator presented the question, “What did
length (defined as from the medial border of the axilla to you feel in terms of pain/fatigue severity during the treat-
the distal wrist crease39). If the maximum distance the par- ment today?” The participant responded on an 11-point
ticipant could reach was less than 125% of the functional ordinal scale (0 = no pain/fatigue; 10 = the most severe
arm length, the bell distance was adjusted to the maximum pain/fatigue).
reachable distance. The instruction to the participants was,
“When you hear the start signal ring, please use the index
Data Analysis
finger of the affected hand to reach and press the bell as
fast as possible.” After a practice trial, 3 trials were per- Data were analyzed with SPSS 19.0 software (SPSS Inc,
formed. Chicago, IL). We calculated that a sample size of 42 was
A 7-camera motion capture system (VICON MX, Oxford needed for an 80% likelihood in detecting a group differ-
Metrics Inc, Oxford, UK) at a sampling frequency of 120 ence with a type I error of .05, based on the previous pilot
Hz was used with a personal computer to record kinematic study showing that MT combined with afferent stimulation
data. Three channels of analog signals were collected simul- resulted in improvements with effect sizes of approximately
taneously: one for instruction of movement start and the .50.23 Baseline differences among groups were analyzed by
others for target bells. Markers were placed on the acro- analysis of variance for continuous data and by χ2 for cate-
mion, middle of humerus, lateral epicondyle, styloid pro- gorical data. To control the variance among groups in the
cess of ulna and radius, and index nail of the affected side. pretest scores, analysis of covariance was used to compare
Movement onset was defined as a rise of tangential wrist the treatment effects among groups on different end points
velocity above 5% of its peak value. Movement offset was at posttest. The pretest performance was the covariate,
defined as a fall of tangential wrist velocity below 5% of its group was the independent variable, and posttest perfor-
peak value. Movement was digitally low-pass filtered at 5 mance was the dependent variable. No multiple testing

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Lin et al 157

Table 1.  Characteristics of Study Participants (N = 43).

Variable MT + MG (n = 14) MT (n = 14) CT (n = 15) Statistica P Value


Gender, n 0.02 .90
 Male 11 10 11  
 Female 3 4 4  
Age (years), 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, X (SD) 22.71 (13.62) 18.50 (11.61) 17.80 (10.56) 0.70 .50
Years of education, X (SD) 10.54 (5.01) 11.07 (4.75) 11.17 (3.71) 0.08 .93
Brunnstroms stage, 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, 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.
a
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.

corrections were made to restrain the type II error consider- Significant and large effects on motor function were
ing the early stage of intervention development. measured by the BBT (F2,40 = 4.39, P = .019, η2 = .184)
Post hoc analysis using highly significant differences and the 10-MWT (velocity of self-pace: F2,40 = 5.02, P =
was used to evaluate the difference of each group. The η2 .011, η2 = .205; stride of self-pace: F2,40 = 7.13, P = .002,
was calculated for each outcome variable to index the mag- η2 = .268; velocity of AQAP: F2,40 = 4.06, P = .025, η2 =
nitude of group differences. The η2 value represents the .176). No significant difference was found in stride length
variability in the dependent variable (posttest performance) of the AQAP subscores in the10-MWT. Post hoc analyses
that can be explained by the independent variable (group). revealed that the MT + MG and the CT group improved
A large effect is represented by an η2 of at least 0.14, a mod- more than the MT group in the BBT (P = .007 and P =
erate effect by an η2 of 0.06, and a small effect by an η2 of .036, respectively). The MG + MT group showed larger
0.01. The level of statistical significance (α) was set at .05 improvements than the MT group on the velocity of self-
for all comparisons.44 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
Results MT group on the velocity of self-paced ambulation (P =
The study recruited 43 participants (mean age = 55.0 .031), the stride of self-paced ambulation (P = .016), and
years). The MT + MG and the MT group consisted of 14 the velocity of AQAP (P = .023).
participants each, and the CT group consisted of 15 partici-
pants. After the treatment programs, the Myoton and kine- Secondary Outcomes. For daily function, no significant
matic data were missing for 2 participants. There were no group effects were found on the ABILHAND or on the AOU
significant differences in demographic characteristics and QOM of the MAL. Table 3 reports the descriptive and
among groups (Table 1). Group differences were not sig- inferential results for the kinematic performance. The results
nificant for pain (F2,39 = 1.65, P = .06) and fatigue (F2,39 = revealed significant and large effects on normalized shoul-
3.05, P = .21). der flexion (F2,38 = 3.43, P = .043, η2 = .157) and reduction
Primary Outcomes. Table 2 reports the descriptive and of maximum shoulder abduction during reach (F2,38 = 4.55,
inferential results, except the kinematic performance. P = .017, η2 = .198) among the 3 groups. Post hoc analyses
Total FMA scores were significantly different, with a revealed that the MG + MT (P = .008) and the MT groups (P
large effect among the 3 groups (F2,40 = 3.35, P = .045, η2 = .023) showed significantly greater reduction of maximum
= .147). Post hoc analyses revealed that the MT + MG and shoulder abduction than the CT group. The CT group showed
the MT groups were significantly higher than the CT larger improvements than the MT group on normalized
group for the FMA total score (P = .0032 and .0031, shoulder flexion (P = .0013). Small and nonsignificant
respectively). Group differences in the muscle tone were effects were found on normalized movement time, normal-
not significant. ized movement unit, and the normalized elbow extension.

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158
Table 2.  Descriptive and Inferential Statistics for Clinical Outcome Measures.

Pretest ( X ± SD) Posttest ( 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) F2,40  
 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 .045a .15
Myoton (n = 14) (n = 13) (n = 14) (n = 14) (n = 13) (n = 14) F2,38  
 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 .02a .18
10 MWT (n = 14) (n = 14) (n = 15) (n = 14) (n = 14) (n = 15) F2,40  
  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 .01a .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 .002a .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 .03a .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) F2,40  

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 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.
a
P < .05.
Lin et al 159

Discussion could alter leg movement via propriospinal neural path-


ways.54 Improvement in UE motor control may contribute
The present study demonstrated that patients in the MT + to arm swing and help generate forward propulsion at the
MG and MT groups performed better compared with those foot.55
in the CT group in the reduction of motor impairment. Our kinematic results revealed that MT + MG or MT
Combining MT with MG stimulation showed additional might reduce shoulder synergy movements, as indicated by
effects on manual dexterity of the affected hand, self-paced less maximum shoulder abduction42 during elbow exten-
ambulation, and velocity of quickly paced ambulation com- sion, compared with the CT group. According to the
pared with MT alone. Relative to CT, MT + MG and MT assumption of motor learning, the neural structures control-
reduced maximum shoulder abduction during forward ling movement are required to adapt to constraints imposed
reach, which is regarded as reducing a critical component of by, at least, physical demands.56 MT restrained arm move-
the flexor synergy pattern. However, CT increased shoulder ment in a size-limited box, which might not allow for a
flexion more than the other groups. For daily function, we great range of shoulder abduction during task performance.
found no group differences immediately after the 4-week Consequently, the synergy pattern of shoulder abduction
interventions. There was no adverse effect as measured by might be inhibited. This result can also be cross-validated
self-reported pain and fatigue. by our findings of improved total FMA scores, because the
Compared with the CT group, the MT + MG and MT FMA involves the ability to perform out-of-synergy move-
groups showed improved motor impairment as indicated by ments,34 the scores of the FMA indicated a reduction in
the FMA total scores, in line with previous research on shoulder synergy movement.57 In contrast, the CT patients
MT.2,6,10 As an explanation for the treatment effects, the gained a greater amount of shoulder flexion than the MT +
visual input during MT could substitute for absent or MG and MT patients. The CT involved a variety of thera-
reduced proprioceptive input from the affected body side45 peutic activities requiring shoulder forward flexion and
and, consequently, helped recruit the premotor cortex or elevation. Accordingly, the CT patients exhibited better
balance the neural activation within the primary motor cor- improvement in shoulder flexion than patients receiving the
tex toward the affected hemisphere to facilitate motor other 2 treatments. Task-specific training has been shown to
improvements.3,4,46 be effective in recovery of movement poststroke.58
We found MT combined with MG stimulation provided No group differences were noted in the muscle tone of
additional benefits on manual dexterity compared with MT the biceps, flexor carpi radialis, and flexor carpi ulnaris.
alone, consistent with the findings of a pilot study on MT One possibility is that our participants had mild to moderate
combined with somatosensory stimulation23 and studies spasticity (MAS ≤ 2) at pretest. Most participants in the MT
related to electrical stimulation.47,48 The extra benefit on + MG group received the 3-step MG stimulation protocol to
manual dexterity is very encouraging, considering its increase awareness of the affected hand and enhance voli-
importance for activities of daily living49 and that previous tional activity rather than the protocol to reduce spastic-
studies of MT showed unclear results on manual dexter- ity,15,17,32 resulting in nonsignificant effects on spasticity.
ity.2,6 MG stimulation might induce rapid plastic change in We found no group differences in daily function, which
sensorimotor regions of the cortex16,17,50 related to the hand is in accord with previous research.23 However, a scrutiny
to which the stimulation was applied and modulate the of the descriptive data showed all groups improved in some
intracortical γ-aminobutyric acid pathways that reduce activities of daily living outcomes, and additional statistical
intracortical inhibition in the motor cortex of the ipsile- analysis showed significant differences between pre- and
sional hemisphere.48 Combining MT with MG could pro- posttreatment for each group (P = .014-.047), indicating
vide cross-modal inputs (ie, sensation from electric that all treatments were beneficial to daily function. Future
stimulation and visual image input from the mirror) during research might include follow-up assessments to study pos-
training that may modulate activation of the somatosensory sible changes in activities of daily living or incorporate
cortex and facilitate dexterity recovery.21,51 more functional task practice into MT + MG or MT to
Another important finding is that combining MT with improve function in daily-life situations.
MG demonstrated significant improvements on ambulation As a limitation, our study included only people with mild
function measured by the 10-MWT compared with MT to moderate motor impairments. Some studies have reported
alone. This finding is consistent with a pilot study23 and that patients with severe motor deficits achieved more
some studies of electrical stimulation on the UE.12,52 improvements after interventions.59 The evidence for opti-
Stimulation of cutaneous nerves of the hand could elicit an mal intensity of afferent stimulation (eg, electric current
interlimb reflex response in muscles across the body that is intensity) for stroke rehabilitation is limited.59 Because we
believed to be related to motor coordination between arms found no adverse effects using stimulation at the threshold
and legs during walking.14,53 In addition, arm integration level, it might be possible to increase the intensity of the
during reciprocal activities, which were part of the training, electrical stimulation.59

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160
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) F2,38 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 .04a .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 .02a .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, normal-
ized 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

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shoulder abduction.
a
P < .05.
Lin et al 161

Conclusions 8. Ezendam D, Bongers RM, Jannink MJ. Systematic review of


the effectiveness of mirror therapy in upper extremity func-
This study is unique in demonstrating the comparative tion. Disabil Rehabil. 2009;31:2135-2149.
effects of MT + MG, MT alone, and task-oriented therapy 9. Rothgangel AS, Braun SM, Beurskens AJ, Seitz RJ, Wade
on a variety of motor and functional outcomes. MT + MG DT. The clinical aspects of mirror therapy in rehabilita-
and MT alone improved motor impairment and reduced the tion: a systematic review of the literature. Int J Rehabil Res.
critical component of synergy patterns (ie, shoulder abduc- 2011;34:1-13.
tion) more than CT. MT + MG yields broader aspects of 10. Lee MM, Cho HY, Song CH. The mirror therapy program
motor recovery. Our study showed the benefits of combin- enhances upper-limb motor recovery and motor function in acute
stroke patients. Am J Phys Med Rehabil. 2012;91:689-696.
ing MT and MG stimulation for improving manual dexter-
11. Hankey GJ, Pomeroy VM, King LM, Pollock A, Baily-Hallam
ity and ambulation function. In addition, all treatments A, Langhorne P. Electrostimulation for promoting recovery
here showed benefits in daily function. Future research of movement or functional ability after stroke: systematic
may address the dosing issue by studying the effects of review and meta-analysis. Stroke. 2006;37:2441-2442.
stimulation intensity and integrating functional task prac- 12. Peurala SH, Pitkanen K, Sivenius J, Tarkka IM. Cutaneous
tice in the MT + MG protocol in an attempt to optimize the electrical stimulation may enhance sensorimotor recovery in
effects on daily function. chronic stroke. Clin Rehabil. 2002;16:709-716.
13. Dimitrijevic MM, Stokic DS, Wawro AW, Wun CCC.

Declaration of Conflicting Interests Modification of motor control of wrist extension by mesh-
glove electrical afferent stimulation in stroke patients. Arch
The author(s) declared no potential conflicts of interest with respect
Phys Med Rehabil. 1996;77:252-258.
to the research, authorship, and/or publication of this article.
14. Zehr EP, Klimstra M, Dragert K, et al. Enhancement of arm
and leg locomotor coupling with augmented cutaneous feed-
Funding back from the hand. J Neurophysiol. 2007;98:1810-1814.
The author(s) disclosed receipt of the following financial support 15. Christova M, Rafolt D, Golaszewski S, Gallasch E.

for the research, authorship, and/or publication of this article: This Outlasting corticomotor excitability changes induced by 25
project was supported in part by the National Health Research Hz whole-hand mechanical stimulation. Eur J Appl Physiol.
Institutes (NHRI-EX101-9920PI and NHRI-EX101-10010PI), 2011;111:3051-3059.
the National Science Council (NSC-100-2314-B-002-008-MY3 16. Golaszewski SM, Bergmann J, Christova M, et al. Increased
and NSC99-2314-B-182-014-MY3), and the Healthy Ageing motor cortical excitability after whole-hand electrical stimu-
Research Center at Chang Gung University (EMRPD1B0371) in lation: a TMS study. Clin Neurophysiol. 2010;121:248-254.
Taiwan. 17. Golaszewski SM, Bergmann J, Christova M, et al. Modulation
of motor cortex excitability by different levels of whole-
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