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research-article2014
NNRXXX10.1177/1545968314562111Neurorehabilitation and Neural RepairLiao et al

Clinical Research Article


Neurorehabilitation and

Virtual Reality–Based Training to


Neural Repair
2015, Vol. 29(7) 658­–667
© The Author(s) 2014
Improve Obstacle-Crossing Performance Reprints and permissions:
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and Dynamic Balance in Patients With DOI: 10.1177/1545968314562111


nnr.sagepub.com

Parkinson’s Disease

Ying-Yi Liao, PhD1,2, Yea-Ru Yang, PhD2, Shih-Jung Cheng, MD3,


Yih-Ru Wu, MD4,5, Jong-Ling Fuh, MD2,6, and Ray-Yau Wang, PhD2

Abstract
Background. Obstacle crossing is a balance-challenging task and can cause falls in people with Parkinson’s disease (PD).
However, programs for people with PD that effectively target obstacle crossing and dynamic balance have not been
established. Objective. To examine the effects of virtual reality–based exercise on obstacle crossing performance and
dynamic balance in participants with PD. Methods. Thirty-six participants with a diagnosis of PD (Hoehn and Yahr score
ranging 1 to 3) were randomly assigned to one of three groups. In the exercise groups, participants received virtual
reality–based Wii Fit exercise (VRWii group) or traditional exercise (TE group) for 45 minutes, followed by 15 minutes
of treadmill training in each session for a total of 12 sessions over 6 weeks. Participants in the control group received no
structured exercise program. Primary outcomes included obstacle crossing performance (crossing velocity, stride length,
and vertical toe obstacle clearance) and dynamic balance (maximal excursion, movement velocity, and directional control
measured by the limits-of-stability test). Secondary outcomes included sensory organization test (SOT), Parkinson’s
Disease Questionnaire (PDQ39), fall efficacy scale (FES-I), and timed up and go test (TUG). All outcomes were assessed
at baseline, after training, and at 1-month follow-up. Results. The VRWii group showed greater improvement in obstacle
crossing velocity, crossing stride length, dynamic balance, SOT, TUG, FES-I, and PDQ39 than the control group. VRWii
training also resulted in greater improvement in movement velocity of limits-of-stability test than TE training. Conclusions.
VRWii training significantly improved obstacle crossing performance and dynamic balance, supporting implementation of
VRWii training in participants with PD.

Keywords
obstacle crossing, balance, virtual reality, exercise training, Parkinson’s disease

Introduction the obstacle crossing task compared with normal older


adults.8 Therefore, strategies to improve balance and
Parkinson’s disease (PD) is a progressive neurodegenera-
tive disease. With progression of the disease, patients may
demonstrate postural instability, gait dysfunction, difficulty 1
managing functional tasks, such as obstacle crossing, and Jen-Teh Junior College of Medicine, Nursing and Management, Miaoli,
Taiwan
frequent falls.1-4 More than two thirds of community-dwell- 2
National Yang-Ming University, Taipei, Taiwan
ing individuals with PD experience falls once per year, and 3
Department of Neurology, Mackay Memorial Hospital, Taipei, Taiwan
tripping over obstacles is the major cause of these falls.5 4
Department of Neurology, Chang-Gung Memorial Hospital, Linkou,
During obstacle crossing, participants with PD usually step Taiwan
5
their leading foot closer to the obstacle than age-matched Chang-Gung University College of Medicine, Linkou, Taiwan
6
Department of Neurology, Neurological Institute, Taipei Veterans
controls because of their smaller steps, which may result in General Hospital, Taipei, Taiwan
hitting the obstacle and subsequent falls.6 These individuals
also adopt a conservative strategy during obstacle crossing Corresponding Author:
Ray-Yau Wang, Department of Physical Therapy and Assistive
and maintain their center of mass (COM) more medially to Technology, National Yang-Ming University, 155, Sec 2, Li-Nong Street,
their stance leg.7 This alteration reduces the distance Shih-Pai, Taipei, Taiwan.
between the center of pressure (COP) and COM throughout Email: rywang@ym.edu.tw
Liao et al 659

obstacle crossing ability may help improve functional abil- The diagnostic criteria were at least 2 of the 4 features (rest-
ity and to reduce the incidence of falls. ing tremor, bradykinesia, rigidity, and asymmetric onset) in
Some patients with PD may lack satisfactory to drug which the resting tremor or bradykinesia must be present.31
regimens or surgical options, and they still have consider- All participants met the following inclusion criteria: (a)
able symptoms while on medications. The lack of satisfac- Hoehn and Yahr stages I to III, (b) ability to walk indepen-
tory treatment options provides motivation to investigate dently without any walking aids, (c) stable medication
the effects of exercise on functional improvement. usage, (d) with or without deep brain stimulation, and (e) a
Stretching, strengthening, balance exercise, and gait train- score of ≥24 on the Mini-Mental State Examination
ing improve motor function, balance, and gait performance (MMSE). The exclusion criteria were as follows: (a) unsta-
in participants with PD.9-13 Treadmill training has also been ble medical condition; (b) history of other neurological, car-
used widely in participants with PD to improve gait perfor- diopulmonary, or orthopedic diseases known to interfere
mance and walking economy.14-16 However, the effects of with participation in the study; (c) past history of seizure;
such training on obstacle-crossing performance has not yet (d) use of cardiac pacemaker; and (e) vision deficits. In
been investigated. Combining resistance, aerobic, balance, total, 43 individuals were identified as potential participants
stretching, and treadmill training are likely to be optimal for for this study. Of these, 36 participants provided informed
improving gait speed in participants with PD.17 Whether the consent, which was approved by the Institutional Human
combination of training can carry-over to obstacle crossing Research Ethics Committee of Chang Gung Medical
performance need further investigation. Foundation (Figure 1).
Virtual reality (VR) systems are novel and potentially
useful technologies that allow users to interact with a com-
puter-generated scenario.18 Augmented visual, sensory, and
Experimental Design
auditory feedback are provided when subjects performing This study was a single-blinded, stratified, randomized con-
tasks in virtual environment.19 VR training has been used in trolled trial. The stratification was achieved based on the
older adults and stroke patients to improve postural control, Hoehn and Yahr stage as follows: stage 1 to 1.5, stage 2 to
increase mobility, and reduce fall risk.20-24 In PD partici- 2.5, and stage 3. An individual who was not involved with
pants, VR training has been demonstrated to improve sen- the study selected sealed envelopes to assign participants to
sory organization.25 VR combining treadmill training was 1 of the 3 groups. Participants received VR-based Wii Fit
also reported to improve gait performance during usual and exercise (VRWii group) or traditional exercise (TE group)
complex challenging condition (dual task and obstacle for 45 minutes with additional treadmill training for 15 min-
crossing) in PD participants.26 However, VR combining dif- utes. The exercise was administered for a total of 12 sessions
ferent types of exercise on obstacle-crossing and balance (2 sessions per week) over a 6-week period by the same
performance has not yet been explored. Recently, the gam- physical therapist. Individuals in the control group received
ing industry has developed a variety of affordable and only fall-prevention education, such as minding the environ-
accessible VR systems, such as Wii Fit, that have been mental factors (slippery surface, obstacles, stairs, uneven
reported to improve functional ability in PD participants, ground) after the baseline assessment and were encouraged
such as timed up and go (TUG), sit to stand, unipedal stance, to carry out their regular exercise. All outcomes were mea-
balance, walking speed, and overall quality of life.27-30 sured the day before intervention (pre), the day after com-
These effects, however, have yet to be validated in a ran- pleting the intervention (post), and the 30th day after
domized controlled trial. Furthermore, whether this completing the intervention (follow-up) by the same rater
VR-based Wii Fit exercise is more effective than traditional blinded to group assignment. The measurement and inter-
exercise, especially regarding its effects on advanced gait vention were conducted with patients in the “on” state.
function such as obstacle crossing, warrants investigation.
Therefore, the purpose of this study was to elucidate the
Interventions
effects of VR-based Wii Fit exercise on obstacle crossing
and dynamic balance ability in participants with PD by Traditional Exercise (TE).  This program included 10 minutes
comparing the results of Wii Fit training, traditional exer- of stretching exercises, 15 minutes of strengthening exer-
cise, and a no-exercise control. cises, and 20 minutes of balance exercises in each session as
described below.

Methods 1. Stretching exercises: The stretching exercises


focused on upper body and upper and lower extrem-
Participants ities with gentle joint extension and flexion and
Participants were recruited from a medical center in Taiwan trunk rotation in a standing position. Deep breathing
and were diagnosed with idiopathic PD by a neurologist. was emphasized during the exercise.
660 Neurorehabilitation and Neural Repair 29(7)

Figure 1.  Flowchart of participants recruited in this study.

2. Strengthening exercise: The strengthening exercises increasing the number of repetitions, and increasing difficulty
focused on the lower extremity muscles that are of exercise, such as increasing the height of the blocks during
important for posture, balance, and gait. Participants the stepping-up exercise, increasing the forward/sideward
performed the following exercises in standing posi- stepping distance during the stepping exercise, holding the
tion: (a) one leg forward/sideward swing, (b) stepping squatting position for longer duration during the squatting
up and down, (c) multidirectional leg raising, (d) heel exercise. The criteria for progression were determined by the
and toe raising, and (e) squatting. Participants per- ability of the participant to perform the activities without dif-
formed 3 sets of 10 to 15 repetitions for each activity. ficulty and by the perceived exertion (Borg rate of perceived
Participants used ankle weights that started at 1 kg and exertion <13, somewhat hard).
were gradually increased to 2 kg for each leg. Natural
breathing was emphasized during the exercise. Virtual Reality–Based Wii Fit Exercise.  The Wii Fit Plus gam-
3. Balance exercises: The balance exercises were com- ing system and Wii Fit balance board (Nintendo Phuten Co,
binations of dynamic balance training and sensory Ltd, Taiwan) were used for VRWii exercise. The Wii Fit
integration training. The dynamic balance training balance board is a novel system that tracks changes in the
exercises were symmetric weight shifting with slow COP during exercise. A virtual environment was displayed
and fast speed, catching and throwing balls, and on a screen with a 230 cm width and height in front of the
multidirectional stepping in a standing position. The participant. Through avatar technology, images were pro-
sensory integration training exercises included sin- jected on the screen through a projector. The virtual charac-
gle leg stance with eyes open and closed and stand- ter provides instantaneous visual and auditory feedback.
ing on foam with eyes open and closed. Participants can imitate the virtual character and adjust their
own movements according to feedback (knowledge of the
The progressions in both TE and VRWii group included performance) in real time (<20 ms lag between player and
adding more weights during strengthening exercise, avatar movement). At the end of the game, the Wii Fit system
Liao et al 661

also provides the total score on the screen (knowledge of stepped over the obstacle, and continued to walk to the end
the results). In each Wii Fit exercise session, participants of the walkway at a comfortable speed without any con-
underwent 10 minutes of yoga exercises, 15 minutes of strain. Three obstacle-crossing variables were analyzed as
strengthening exercises, and 20 minutes of balance games follows:
as described below.
1. Crossing stride length: The distance from the heel-
1. Yoga exercises: The yoga exercises were empha- strike of the leg before the obstacle to the heel-strike
sized more on muscle stretching. This program of the same leg after crossing the obstacle.
included sun-salutation modified lunges, chair pose, 2. Crossing stride velocity: The velocity from the heel-
tree pose with arms straight above the head and strike of the leg before the obstacle to the heel-strike
palms together, and table top in standing position. of the same leg after crossing the obstacle.
2. Strengthening exercises: The exercise program, 3. Vertical toe-obstacle clearance: The vertical dis-
intensity, and principle of adding ankle weights tance between the toe sensor of the leg and the
were similar to the strengthening exercise program obstacle when the toe of the leg was directly above
emphasized in the TE group, but in this case, the the obstacle.
strengthening exercises were performed in a
VR-based environment. Dynamic Balance Performance. Dynamic balance was
3. Balance games: The balance games included the assessed by the Balance Master system (NeuroCom Inter-
soccer heading, marble balance, ski slalom, and bal- national, Inc, Clackamas, OR). Limits of stability (LOS)
ance bubble. When performing these games, partici- testing was used to document dynamic balance perfor-
pants needed to shift their COM as quickly and mance. 33,34 To assess the LOS, the subject stood on the for-
accurately as possible to hit the soccer, put the roll- ceplate and shifted his or her center of gravity (COG) to
ing marble in the hole, ski without hitting the obsta- reach a maximal distance in the target direction as quickly
cles, and navigate the bubble through the maze and accurately as possible without moving the feet. The
without popping it. directions assessed included forward, right, and left.
Because of insignificant difference between right and left
Treadmill Training. Participants in both exercise groups direction, data from the right and left directions were aver-
received treadmill training (Biodex, Shirley, NY) after the aged to indicate sideward control. Movement velocity
above exercise training sessions to enhance the effects of (MV), maximum excursion (ME), and directional control
exercise training. Each treadmill session lasted 15 minutes. (DC) were collected during the LOS test in this study. MV
The treadmill speed was set at 80% of the individual’s over- is defined as the average speed in degrees/second in a spe-
ground comfortable walking speed and was increased by an cific direction. ME is defined as the farthest distance trav-
increment of 0.2 km/h per 5 minutes as tolerated. A safety eled by the COG during the trial. DC is defined as the
harness without body weight support was provided during amount of movement in the intended direction minus the
treadmill training to prevent falls. amount of extraneous movement. A DC score of 100% indi-
cates that the participant does not deviate from a straight
path during the test.
Primary Outcomes
Obstacle-Crossing Performance.  The Liberty system (Polhte-
Secondary Outcomes
mus, Inc, Colchester, VT) was used to measure spatial tem-
poral variables during obstacle crossing. This system is an Sensory Integration Ability. The sensory organization test
electromagnetic motion capture device for tracking (SOT) was assessed using the Balance Master system to
3-dimensional movement at a speed of 240 updates per sec- evaluate sensory integration ability. The equilibrium score
ond. Two sensors were attached to the top of the second toe was obtained under each of 6 visual and support surface
of each foot. These sensors recorded the 3-dimensional conditions (SOT1-SOT6). Through sway of the visual sur-
positioning of the foot. The validity and reliability of the round and support surfaces, inaccurate information was
Liberty system have been previously established.32 Obsta- delivered to the somatosensory, visual, and vestibular sys-
cle crossing required participants to walk on a 10-meter tems. The SOT scores used in this study are the weighted
walkway with an obstacle positioned in the middle of the averages from all equilibrium scores to indicate sensory
walkway. The obstacle was a plastic crossbar (60 cm long integration ability.35
and 1.5 cm in diameter) supported by 2 vertical posts. The
height of the obstacle was 20% of the subject’s leg length The 39-Question Parkinson’s Disease Questionnaire. This
(14-20 cm) to emulate the height of a curb or stair. During questionnaire was developed to assess the quality of life of
obstacle crossing trials, participants initiated walking, patients with PD.36 This questionnaire contains 8
662 Neurorehabilitation and Neural Repair 29(7)

dimensions with 39 items and assesses mobility, activities Table 1.  Demographic Characteristics of Included Participants.
of daily living, emotions, stigmas, social issues, cognition,
Control TE VRWii
communication, and body pain. Subjects filled out the ques- (n = 12) (n = 12) (n = 12)
tionnaire according to the presence of problems during the
previous month. The validity of the 39-question Parkinson’s Age (years) 64.6 ± 8.6 65.1 ± 6.7 67.3 ± 7.1
Disease Questionnaire (PDQ39) was reported previously.37 Gender (male/ 5/7 6/6 6/6
A higher score represents a poor quality of life. The Chinese female)
Disease duration   6.4 ± 3.0   6.9 ± 2.8   7.9 ± 2.7
version of the PDQ39 was used in this study.38
(years)
Hoehr and Yahr   1.9 ± 0.8   2.0 ± 0.8   2.0 ± 0.7
Falls Efficacy Scale–International.  The Falls Efficacy Scale– stage
International (FES-I) is widely used in elderly persons to  1-1.5 5 6 5
indicate concerns about falling. There are 16 items assess-  2-2.5 4 5 4
ing functional tasks and social-related activities, and scor-  3 3 3 3
ing ranges from 1 to 4. Subjects rated the items according to MMSE 29.7±0.6 29.8±0.3 29.5±0.7
their concerns about falling. A higher score indicates a
greater concern about falling. The validity of the FES-I has Abbreviations: MMSE, Mini-Mental State Examination; TE, traditional
exercise; VRWii, virtual reality–based Wii Fit exercise.
been reported for older adults.39,40

Timed Up and Go Test.  For the Timed Up and Go (TUG) test, Obstacle-Crossing Performance
participants were asked to stand up from a chair, walk 3 m,
turn around, return to the chair, and sit down. The time The results of the obstacle crossing performance evaluation
taken to complete this task was measured with a stopwatch. are shown in Table 2 and Figure 2. The VRWii group
This test has been demonstrated to have high reliability in showed significant improvements in crossing stride length
people with PD.41 and velocity compared with the control group after training
and at the 1-month follow-up (stride length, VRWii vs con-
trol, P = .003 at posttraining, P = .001 at follow-up; stride
Statistical Analysis velocity, VRWii vs control, P = .011 at posttraining, P =
Descriptive statistics were generated for all variables, and .001 at follow-up); however, no significant difference
distributions of variables were expressed as mean ± stan- between the VRWii and the TE groups was found. The par-
dard deviation. Intergroup differences among baseline char- ticipants contacted the obstacle in 2% of the trials (15 fail-
acteristics were evaluated using the 1-way analysis of ure trials out of total 642 trials with 6 leading foot toe
variance (ANOVA) or χ2 analysis with significant level at contact and 9 trailing foot toe contact).
P < .05. Change values were calculated by subtracting the
baseline data from the post-training data or by subtracting Dynamic Balance and Sensory Organization
the baseline data from the follow-up data. To analyze inter-
Test
group improvement, the changes values were analyzed
using a 1-way ANOVA with group as a factor, followed by The results of dynamic balance assessment are shown in
Tukey post hoc test. As change values (between post and Table 3. Both the VRWii and the TE groups exhibited sig-
pre, and between follow-up and pre) in 1-way ANOVA nificant improvements in MV and SOT compared with the
were examined twice, the significance level was corrected control group after training and at the 1-month follow-up
with a Bonferroni correction (P = .025) to reduce the pos- (forward MV, VRWii vs control, P < .001 at posttraining,
sibility of statistical error. P < .001 at follow-up, TE vs control, P = .015 at posttrain-
ing, P = .012 at follow-up; sideward MV, VRWii vs control,
Results P < .001 at posttraining, P < .001 at follow-up, TE vs con-
trol, P = .004 at posttraining; SOT, VRWii vs control, P <
Thirty-six participants were randomly assigned to the con- .001 at posttraining, P < .001 at follow-up, TE vs control,
trol, TE, or VRWii groups (n = 12 for each group). None of P = .015 at posttraining, P = .001 at follow-up). Moreover,
the participants reported any adverse events. One partici- the VRWii group exhibited greater improvement than the
pant in the control group withdrew at the time of follow-up TE group on MV (forward MV, VRWii vs TE, P < .001 at
because of low motivation (Figure 1). No significant group posttraining, P < .001 at follow-up; sideward MV, VRWii
differences in baseline demographic characteristics were vs TE, P < .001 at posttraining, P < .001 at follow-up). The
found (Table 1). Similarly, no significant group differences VRWii group also showed significant improvements in ME
were noted in the outcome measures at preintervention and DC compared with the control group after training and
assessment (Tables 2-4). at follow-up (forward ME, VRWii vs control, P = .023 at
Liao et al 663

Table 2.  Comparisons of Obstacle Crossing Performance.


Control (n = 12) TE (n = 12) VRWii (n = 12)
a
  Pre Post Follow-up Pre Post Follow-up Pre Post Follow-up

Velocity (cm/s) 80.4 ± 16.1 78.5 ± 17.0 78.2 ± 17.3 77.5 ± 21.8 85.8 ± 18.0 84.7 ± 21.4 75.2 ± 11.4 87.0 ± 16.5 91.1 ± 20.0
  Change valuesb –1.9 ± 3.9 –0.9 ± 3.9 8.3 ± 9.0 7.4 ± 7.0 11.9 ± 16.2* 16.0 ± 15.5**
Stride length (cm) 109.8 ± 17.5 108.3 ± 19.0 107.0 ± 19.3 110.3 ± 19.12 118.6 ± 18.7 115.7 ± 18.6 108.9 ± 8.4 123.0 ± 14.2 125.2 ± 13.7
  Change valuesb –1.5 ± 11.9 –1.9 ± 9.2 7.3 ± 7.3 5.4 ± 9.4 14.4 ± 12.3** 16.9 ± 12.3**
Toe-obstacle 14.1 ± 4.0 14.0 ± 3.7 14.9 ± 3.6 14.9 ± 4.2 14.7 ± 3.5 15.7 ± 1.6 12.9 ± 4.0 12.5 ± 3.4 13.2 ± 3.7
clearance (cm)
  Change valuesb 0.3 ± 2.7 0.8 ± 2.6 0.1 ± 2.7 –0.9 ± 1.1 –0.5 ± 2.9 –0.5 ± 2.5

Abbreviations: TE, traditional exercise; VRWii, virtual reality–based Wii Fit exercise.
a
n = 11.
b
Change values were calculated by subtracting the baseline data from the posttraining data (post) or by subtracting the baseline data from the follow-up data (follow-up).
*Significance level <.025 for intergroup comparisons (TE vs Control; VRWii vs Control).
**Significance level <.01 for intergroup comparisons (TE vs Control; VRWii vs Control).

Table 3.  Comparisons of Dynamic Balance and SOT Score.


Control (n = 12) TE (n = 12) VRWii (n = 12)
a
  Pre Post Follow-up Pre Post Follow-up Pre Post Follow-up

Forward ME (%) 58.9 ± 14.0 59.5 ± 15.0 58.8 ± 15.4 57.8 ± 12.2 65.3 ± 12.8 64.9 ± 16.4 55.8 ± 16.7 68.9 ± 16.8 68.5 ± 17.8
  Change valuesb 0.6 ± 13.6 –0.0 ± 10.1 7.5 ± 8.3 7.1 ± 10.7 13.1 ± 11.5* 12.6 ± 10.4*
Sideward ME 77.2 ± 14.5 74.0 ± 15.0 75.3 ± 14.3 75.8 ± 12.9 79.9 ± 10.8 79.0 ± 9.6 74.5 ± 11.7 81.0 ± 11.0 82.5 ± 13.8
  Change valuesb –3.0 ± 10.1 –1.9 ± 10.6 4.1 ± 8.9 3.2 ± 5.7 6.6 ± 8.3 8.0 ± 6.2*
Forward MV (%) 2.4 ± 0.7 2.4 ± 0.8 2.3 ± 1.1 2.2 ± 0.9 3.0 ± 1.1 3.0 ± 1.3 2.0 ± 0.6 3.6 ± 0.8 3.6 ± 1.3
  Change valuesb 0.1 ± 0.1 –0.1 ± 0.7 0.8 ± 0.9* 0.8 ± 0.7* 1.6 ± 0.4**† 1.6 ± 0.9**†
Sideward MV 2.9 ± 0.9 2.7 ± 1.0 2.9 ± 1.2 2.9 ± 1.2 3.8 ± 1.6 3.7 ± 1.3 2.7 ± 0.6 4.3 ± 0.9 4.3 ± 1.1
  Change valuesb –0.2 ± 0.5 –0.0 ± 0.5 0.8 ± 0.8* 0.8 ± 0.7 1.7 ± 0.9**† 1.7 ± 1.1**†
Forward DC (%) 76.6 ± 10.4 76.1 ± 11.0 76.5 ± 11.0 74.5 ± 9.7 81.3 ± 6.4 80.5 ± 3.8 73.5 ± 14.8 84.0 ± 10.0 83.2 ± 10.7
  Change valuesb –0.5 ± 2.6 –0.1 ± 1.9 6.1 ± 7.6 5.6 ± 6.8 10.4 ± 6.6** 9.7 ± 7.0**
Sideward DC (%) 76.7 ± 6.6 74.2 ± 9.2 73.6 ± 11.0 77.3 ± 5.8 80.1 ± 5.8 78.2 ± 6.9 74.9 ± 9.3 79.7 ± 6.3 81.6 ± 4.2
  Change valuesb –2.5 ± 5.7 –3.1 ± 7.1 2.8 ± 4.7 0.8 ± 9.2 4.8 ± 5.6** 6.7 ± 6.9*
SOT score (%) 68.2 ± 8.1 67.2 ± 11.0 65.7 ± 9.3 67.9 ± 10.5 74.3 ± 8.2 74.7 ± 6.7 65.4 ± 8.5 75.9 ± 5.0 75.8 ± 6.2
  Change valuesb –1.0 ± 5.2 –2.5 ± 4.0 5.0 ± 4.6* 5.3 ± 5.4** 10.5 ± 5.9** 10.4 ± 4.9**

Abbreviations: DC, directional control; ME, maximal excursion; MV, movement velocity (scores range from 0% to 100%, and higher percentages indicate better balance
control); SOT, sensory organization test (scores range from 0% to 100%, and higher percentages indicate better sensory integration ability); TE, traditional exercise; VRWii,
virtual reality–based Wii Fit exercise.
a
n = 11.
b
Change values were calculated by subtracting the baseline data from the posttraining data (post) or by subtracting the baseline data from the follow-up data (follow-up).
*Significance level <.025 for intergroup comparisons (TE vs Control; VRWii vs Control).
**Significance level <.01 for intergroup comparisons (TE vs Control; VRWii vs Control).

Significance level <.025 for intergroup comparisons (VRWii vs TE).

posttraining, P = .014 at follow-up; sideward ME, VRWii posttraining, P < .001 at follow-up; TE vs control, P = .025
vs control, P = .011 at follow-up; forward DC, P = .001 at at posttraining, P = .008 at follow-up).
posttraining, P = .002 at follow-up; sideward DC, P = .006
at posttraining, P = .012 at follow-up).
PDQ39 and FES-I
Both the VRWii and TE groups showed significant improve-
Timed Up and Go ments in PDQ39 and FES-I scores compared with the con-
The results of TUG analysis are shown in Table 4. Both the trol group at follow-up (PDQ39, VRWii vs control, P = .004
VRWii and the TE groups showed significant improvement at posttraining, P = .001at follow-up, TE vs control, P = .022
in TUG results compared with the control group after train- at follow-up; FES-I, VRWii vs control, P < .001 at posttrain-
ing and at follow-up (VRWii vs control, P < .001 at ing, P = .001 at follow-up, TE vs control, P = .019 at
664 Neurorehabilitation and Neural Repair 29(7)

Table 4.  Comparisons of TUG, PDQ39, and FES-I.


Control (n = 12) TE (n = 12) VRWii (n = 12)
a
  Pre Post Follow-up Pre Post Follow-up Pre Post Follow-up

TUG (seconds) 11.9 ± 2.7 12.6 ± 3.6 12.9 ± 3.8 12.1 ± 2.1 11.0 ± 1.8 10.7 ± 1.5 12.6 ± 4.1 9.7 ± 2.1 9.7 ± 2.3
  Change valuesb 0.7 ± 1.7 1.0 ± 1.9 –1.1 ± 0.1* –1.3 ± 0.9** –2.9 ± 2.2** –2.9 ± 2.2**
PDQ39 78.2 ± 23.3 79.0 ± 24.3 80.2 ± 24.5 82.2 ± 27.3 70.8 ± 27.1 70.0 ± 26.5 84.5 ± 26.0 68.8 ± 20.0 65.8 ± 18.3
  Change valuesb 0.7 ± 3.5 2.0 ± 3.6 –11.4 ± 8.2 –12.2 ± 8.5* –15.7 ± 18.2** –18.7 ± 19.4**
FES-I 34.4 ± 11.0 34.9 ± 12.0 35.2 ± 13.0 38.7 ± 12.4 31.5 ± 9.0 31.5 ± 10.8 39.0 ± 14.0 27.8 ± 9.4 28.0 ± 11.4
  Change valuesb 0.5 ± 3.6 0.8 ± 6.6 –7.1 ± 8.0* –7.2 ± 7.5* –11.2 ± 7.0** –11.0 ± 6.7**

Abbreviations: FES-I, Falls Efficacy Scale–International; PDQ39, 39-question Parkinson’s Disease Questionnaire; TUG, timed up and go; TE, traditional exercise; VRWii,
virtual reality–based Wii Fit exercise.
a
n = 11.
b
Change values were calculated by subtracting the baseline data from the posttraining data (post) or by subtracting the baseline data from the follow-up data (follow-up).
*Significance level <.025 for intergroup comparisons (TE vs Control; VRWii vs Control).
**Significance level <.01 for intergroup comparisons (TE vs Control; VRWii vs Control).

Significance level <.025 for intergroup comparisons (VRWii vs TE).

Figure 2.  Change values of crossing velocity (A) and change values of crossing stride length (B) at post and follow-up. VRWii group
showed significant improvements in crossing velocity (P = .011) and stride length (P = .003) compared with the control group after
training. The improvements at posttraining were retained at follow-up (crossing velocity, P = .001; crossing stride length, P = .001).
* Indicates significant difference between groups.

posttraining, P = .021 at follow-up); however, there was no assessment of falls risk in PD patients.43,44 Therefore, the
significant difference between the VRWii and TE groups in VRWii as part of a multifaceted training intervention can
the PDQ39 and FES-I results (Table 4). exert better results than traditional intervention with both
statistical and clinical meaningfulness.
The relationship between obstacle-crossing perfor-
Discussion mance and dynamic balance has been demonstrated in our
In this study, we demonstrated that 12 sessions of VRWii as previous study, in which crossing stride length and velocity
part of a multifaceted training intervention is effective in correlated with ME, MV, DC in the LOS test, and SOT.45 In
improving obstacle-crossing performance in participants the present study, we designed the treatment program
with PD compared with control group. Such improvement according to these influencing factors and noted that
is accompanied by concurrent increases in dynamic balance improved dynamic balance and SOT after 12 sessions of
control and sensory integration ability, and these improve- VRWii training coincides with improved crossing perfor-
ments persisted for at least one month. We further demon- mance. Obstacle crossing is a balance demanding task that
strated that the VR-based Wii Fit exercise is more effective requires control of single leg support and COM forward
than traditional exercise in improving MV in LOS test. The shifting46 which are core programs of our balance exercise.
LOS test can indicate balance control in participants with With improved balance, the individuals may move their
PD.42 In addition, the LOS is useful in the prospective COM further, faster and more correctly.47 Meanwhile, with
Liao et al 665

improved SOT, the individuals may process sensory infor- Taken together, these possibilities may help participants
mation (vision, vestibular, and somatosensory) more accu- with PD improve their mobility and balance control, as
rately in order to control their trunk and limbs in response to demonstrated in the LOS test. It should also be noted that
sensory challenges.48 Therefore, participants in the VRWii treadmill training was part of our training program. The
group demonstrated increased stride length and velocity effect of treadmill training is known to improve gait perfor-
strategies during obstacle crossing. Previous studies mance and balance, thus we included the treadmill training
reported that individuals with PD place their leading foot after VR-based Wii Fit exercise (VRWii group) and tradi-
closer to the obstacle and more often hit the obstacle.6 tional exercise (TE group) for 15 minutes to enhance the
Therefore, a longer stride length may reduce the risk of the effects of exercise training. Therefore, the improvements in
leading foot hitting the obstacle.49 Also, a faster crossing both exercise groups could also partly be attributed to the
velocity may represent an effective motor coordination treadmill training.
strategy. However, this safe and efficient crossing strategy A previous study indicated that an increase in the weigh-
was not achieved with the traditional exercise training. ing of sensory inputs is required to prepare for an ensuing
Previous studies indicated that participants with PD can change in direction.52 During TE and VRWii training, the
adjust the vertical toe-obstacle clearance in response to dif- participants were required to adjust their joint angles to
ferent obstacle heights, although the short stride length shift their body weight and to move the head and trunk.
remains. Therefore, PD participants have greater difficulty These changes in joint angles and head positions stimu-
in lengthening their step over the obstacle than increasing lated somatosensory and vestibular receptors to enhance
the foot height during the obstacle crossing.6,50 Our results the central integration ability, as demonstrated by the
suggest that VRWii training is especially effective in results of SOT.
increasing the horizontal crossing length and velocity as Improvement in dynamic balance (ME, MV, and DC)
opposed to improving vertical toe clearance in participants and SOT may also increase functional ability in daily life,
with PD. including transitioning between sitting and standing posi-
Previous studies on exercise intervention found that PD tion, turning, and walking. These functional tasks are key
participants improved their dynamic balance after 20 ses- components of TUG. In addition, the training effect also
sions over 10 weeks of training.13 In the present study, par- extended to patients’ concerns about falling as indicated by
ticipants in both exercise groups showed significant the improvement in FES-I. The questions identified in
improvements in MV of LOS test as compared with the FES-I are not just limited to basic daily activities at home
control. However, VRWii exercise resulted in additional but also contain social activities outside the home. After
improvements in ME and DC, which are key factors of training, patients may become more confident in balance-
crossing performance.45 Furthermore, the MV was improved demanding tasks, such as walking on a slippery or uneven
more in the VRWii group than the TE group, suggesting that surface, walking up or down a slope, and walking in a place
incorporating VRWii training into the exercise program is with crowds. The significant improvement in PDQ39 scores
effective for patients with PD for improving balance and for both the TE and VRWii groups further supported the
obstacle crossing ability. notion that exercise not only increases physical function but
Virtual reality–based Wii Fit exercise was more effective also increases emotional well-being, social support, cogni-
than traditional exercise on improving dynamic balance tion, and communication, and decreases bodily discomfort.
which may be due to the following factors. First, VR is a The significant improvements observed in TUG, fall effi-
form of external feedback. In this study, knowledge of per- cacy, and quality of life in patients with PD in the present
formance and knowledge of results were provided during study support the benefits of both traditional and VRWii
training in the form of auditory and visual feedback. training.
Participants were then able to make corrections according to The small sample size of our study is one of the limita-
the feedback to enhance their motor performance. Previous tions. A larger randomized controlled clinical trial is needed
studies reported that PD participants rely more on external to validate the reported benefits of the VR intervention.
cues or feedback to execute movement as a result of an inter- Despite the small sample size, the statistical power is rela-
nal trigger deficit.36 Second, some of our VRWii gaming tively strong for our outcomes (crossing velocity, 0.96;
programs require either attention or problem-solving ability. crossing stride length, 0.94). In addition, the therapist was
Active participation in cognition-demanding programs may not blinded to the exercise group and, although unavoidable,
activate cognitive pathway networks and consolidate the this limitation may introduce bias. Also, the FES-I does not
learning effect.18 Third, observation of the virtual perfor- represent the real incidence of falls, and therefore the reduc-
mance on the screen may also facilitate the participation of tion of fall incidence after training warrants further follow-
mirror neurons. Activation of mirror neurons located in up, especially for PD patients with a history of falls.
cerebral cortices may help to make connections in the neu- Furthermore, it should be noted that both interventions
ral network that enhance learning and motor performance.51 included treadmill training to enhance the effects of exercise
666 Neurorehabilitation and Neural Repair 29(7)

training. However, this may dilute the distinction between persons with idiopathic Parkinson’s disease. Arch Phys Med
the VR Wii and TE groups. In summary, VRWii as part of a Rehabil. 2003;84:1109-1117.
multifaceted training intervention is effective in improving 11. Schenkman M, Cutson TM, Kuchibhatla M, et al. Exercise
obstacle-crossing performance, dynamic balance, functional to improve spinal flexibility and function for people with
Parkinson’s disease: a randomized, controlled trial. J Am
ability, and quality of life in PD patients. These improve-
Geriatr Soc. 1998;46:1207-1216.
ments can persist for at least 1 month. These findings sup-
12. Toole T, Hirsch MA, Forkink A, Lehman DA, Maitland

port the inclusion of VRWii training in the exercise program CG. The effects of a balance and strength training pro-
for participants with PD. gram on equilibrium in parkinsonism: a preliminary study.
NeuroRehabilitation. 2000;14:165-174.
Declaration of Conflicting Interests 13. Hackney ME, Earhart GM. Tai chi improves balance and
The author(s) declared no potential conflicts of interest with mobility in people with Parkinson disease. Gait Posture.
respect to the research, authorship, and/or publication of this 2008;28:456-460.
article. 14. Pohl M, Rockstroh G, Ruckriem S, Mrass G, Mehrholz J.
Immediate effects of speed-dependent treadmill training on
Funding gait parameters in early parkinson’s disease. Arch Phys Med
Rehabil. 2003;84:1760-1766.
The author(s) disclosed receipt of the following financial support
15. Herman T, Giladi N, Hausdorff JM. Treadmill training for
for the research, authorship, and/or publication of this article:
the treatment of gait disturbances in people with parkinson’s
Support was provided by the National Science Council (NSC
disease: a mini-review. J Neural Transm. 2009;116:307-
100-2314-B-010-022-MY2) and Aim for the Top University Plan
318.
(101AC-P508) of the Ministry of Education of the Republic of
16. Schenkman M, Hall DA, Baron AE, Schwartz RS, Mettler
China.
P, Kohrt WM. Exercise for people in early- or mid-stage
Parkinson disease: a 16-month randomized controlled trial.
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