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DOI: 10.1177/0031512518769204
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Parkinson’s Disease

Melissa L. M. Alves1 , Beatriz S. Mesquita2,


Wenderson S. Morais3, Josevan C. Leal3,
Corina E. Satler3, and
Felipe A. dos Santos Mendes3

Abstract
This study investigated changes in motor and cognitive skills, anxiety levels, and
quality of life perception among patients with Parkinson’s Disease (PD) following
training with different commercial gaming devices—Nintendo WiiTM and Xbox
KinectTM. We used a quasi-experimental, simple blinded clinical trial, dividing 27
patients with PD into three equal groups of nine members: (a) Nintendo WiiTM,
(b) Xbox KinectTM, and (c) control group. After pretests, experimental group par-
ticipants spent 10 sessions playing four games of the selected gaming device, while
control group participants received no intervention. Only those engaged with the
Nintendo WiiTM significantly improved their performance on single and dual task gait
tests, decreased anxiety levels, and improved memory, attention, and reversibility.
The control group showed no changes on any measures.

Keywords
Parkinson’s disease, virtual reality, video game, Xbox Kinect, Nintendo Wii,
cognitive, motor

1
Faculty of Physical Education, University of Brasilia, Brazil
2
Faculty of Ceilandia, University of Brasilia, Brazil
3
Federal District Secretary of Health, Brasilia, Brazil
Corresponding Author:
Melissa L. M. Alves, Faculty of Physical Education, University of Brazilia, Darcy Ribeiro University
Campus, Brasilia 70910-900, Brazil.
Email: melissa.lorraynne@gmail.com
2 Perceptual and Motor Skills 0(0)

Introduction
Parkinson’s disease (PD) is a chronic, degenerative, and progressive condition of
the central nervous system that causes motor and cognitive impairments such
as rigidity, tremor, bradykinesia, postural instability, and changes in memory,
language, visuospatial capacity, and executive functions (Souza et al., 2011).
The cognitive symptoms may lead to increased disability and poor quality of
life, and make it difficult to treat motor symptoms (Kummer, 2009). Besides the
motor and cognitive symptoms of PD, anxiety has a high prevalence in this
population and can make a great impact on activities of daily living and quality
of life for patients with PD. It is estimated that 40–50% of patients with PD have
relevant anxiety symptoms (Rutten et al., 2015).
PD treatment involves three modalities: medical, surgical, and rehabilitation.
As drugs and surgery do not prevent disease progression or significantly assist
cognitive functions, rehabilitation has been important (David et al., 2015;
Goodwin, Richards, Taylor, Taylor, & Campbell, 2008), and continuous treat-
ment, like physical therapy, is often needed (Pompeu et al., 2014).
Among various treatment modalities, virtual reality (VR) training has become
an emergent rehabilitation resource. VR allows the person to interact with an
artificial reality via computer simulation (Arias, Robles-Garcı́a, Sanmartı́n,
Flores, & Cudeiro, 2012; Mirelman et al., 2011), and it provides real-time game
performance feedback, offering possible control over exercise duration and inten-
sity and furnishing patients with enriched auditory and visual environmental
stimulation (Arias et al., 2012; Deutsch, Borberly, Filler, Huhn, & Guarrera-
Bowlby, 2008; Mirelman et al., 2011). Over the last decade, commercial gaming
devices have become a rehabilitation intervention tool. Their main advantages are
their low cost, compared with other treatment methods, their positive effect on
motivation and engagement, and their potential for home use (Bonnechère,
Jansen, Omelina, Sholukha, & Jan, 2016; Lohse, Shirzad, Verster, Hodges, &
Van Der Loos, 2013). Previous studies have shown gaming devices to be benefi-
cial, economic, and safe for patients with PD (Bonnechère et al., 2016; Herz et al.,
2013; Zimmermann et al., 2014), and they have been found to require skills such
as logic, memory, problem solving, programming, visuospatial functions, motor
sequencing, and motor control (Herz et al., 2013; Mirelman et al., 2013).
Nintendo WiiTM and Xbox KinectTM exemplify commercial gaming
devices that have been studied for rehabilitation use. These systems differ
mainly in how they require and measure participant motion. The Nintendo
WiiTM works with a handheld controller and a force platform named Wii
Balance BoardTM (WBB), while the Xbox KinectTM requires no controller to
capture movements and works with infrared sensors (Beaulieu-Boire et al.,
2015). We found 13 prior intervention studies among patients with PD using
Nintendo WiiTM (Dos Santos Mendes et al., 2012; Esculier, Vaudrin, Bériault,
Gagnon, & Tremblay, 2012; Esculier, Vaudrin, & Tremblay, 2014; Gonçalves,
2013; Gonçalves, Leite, Orsini, & Pereira, 2014; Herz et al., 2013; Liao et al.,
Alves et al. 3

2015; Mhatre et al., 2013; Negrini et al., 2016; Pompeu et al., 2012; Zalecki et al.,
2013; Zimmermann et al., 2014), while we located only two using Xbox KinectTM
commercial games (Dos Santos Mendes et al., 2015; Pompeu et al., 2014). To our
knowledge, no empirical research papers to date have compared the effects of
these different VR systems in their use with patients with PD. Therefore, the
purpose of this study was to compare the relative effects of these two commercially
available gaming devices—the Nintendo WiiTM and Xbox KinectTM—with regard
to motor and cognitive performance, anxiety levels, and perceived quality of life
changes in patients with PD.

Method
This study used a quasi-experimental clinical trial, assessor blinded. We received
advance approval for this protocol from the Ethics and Research Committee
of the Faculty of Ceilândia of the University of Brası́lia (Ref. No.
68491017.4.0000.8093).

Participants
Of 110 patients first recruited, only 27 satisfied all inclusion/exclusion eligibility.
Thus, research participants were 27 patients (25 men; mean age: 61 years,
SD ¼ 10.7) with PD, diagnosed by a neurologist and screened by a physical
therapist for study eligibility. Participants were recruited through flyers and
advertising banners in the local community associations and hospitals for
patients with PD in Brası́lia, Brazil. We conducted all procedures in the physical
therapy laboratories at the Faculty of Ceilândia of the University of Brası́lia
(UnB), Brazil, between January and June 2017. After undergoing screening to
confirm eligibility, individuals who agreed to participate in the study provided
informed written consent.
Patients were included if they (a) were on stable treatment with Levodopa, (b)
were classified as stage one to three according to the Hoehn and Yahr scale, (c)
presented a Mini Mental State Examination score 24, (d) had at least four
years of formal education, and (e) had good visual and auditory acuity.
Exclusion criteria were those who had (a) other neurological disorders or
organic pathological conditions that would prevent participation in the training,
(b) previous experience with the selected games from Nintendo WiiTM and Xbox
KinectTM gaming devices, (c) another specialized rehabilitation program, and
(d) a Geriatric Depression Scale score > 6.

Dependent Measures
The same examiner who was blinded as to which group patients were allocated
performed all evaluations. The examiner was one of the physical therapists of
4 Perceptual and Motor Skills 0(0)

the research team who received adequate training to apply the clinical tests (W.
S. M.). Evaluations occurred at the same time of day and with uniform proced-
ures at baseline (pretesting), seven days postintervention (posttesting), and at 1-
month postintervention (follow-up testing) in phase with the administration of
anti-Parkinsonian medication.

Gait Performance. Three trials of each gait performance test were performed and
recorded at each evaluation session, and we entered the mean performance of
these three trials into data analysis. The participants were instructed to walk as
quickly and safely as possible without running, following the examiner’s dem-
onstration of the task. The gait measures were: (a) Timed Up and Go (TUG;
Morris, Morris, & Iansek, 2001); (b) 10-Meter Walk Test (10MWT; Paker et al.,
2015); and (c) 30-Seconds Walk Test in simple and dual task conditions
(Knutson, Schimmel, & Ruff, 1999). TUG has been widely used to evaluate
functional mobility and has been shown to be reliable for people with PD,
with intraclass correlation coefficients 0.87 (Almeida, Valenca, Negreiros,
Pinto, & Oliveira-Filho, 2016; Fernandes, Mendes, Rocha, & Tavares, 2016;
Morris et al., 2001; Paker et al., 2015). It measures how long it takes to get
up from a chair, walk three meters, return to the same chair, and sit again. The
10MWT is an easy, fast, reliable, and valid test for gait speed measurement in
people with PD (intraclass correlation coefficients ¼ .96; Lang, Kassan,
Devaney, Colon-Semenza, & Joseph, 2016). Participants performed this task
in a 14-meter corridor, with the two additional meters at the beginning and
end to permit acceleration and deceleration (Salbach et al., 2001), and we rec-
orded the time required to cover the 10 meters. The 30-Seconds Walk Test was
used to assess the gait performance in simple and complex conditions. The
participants walked during 30 seconds in a simple task condition (just walk)
and in a dual task condition (walk and speak words with a predetermined initial
letter), while we recorded the distance walked and the number of steps and
words evoked. The 30-Seconds Walk Test is a general measure for child mobility
(Knutson et al., 1999). Although the test was developed for children, it has been
chosen because it was considered appropriate to ensure that patients had ade-
quate time to perform the cognitive task simultaneously, unlike the 10MWT.

Cognitive Performance, Anxiety, and Quality of Life Measures. Two cognitive measures
were employed: (a) Digit Span forward and backward (Wechsler, 1997) and (b)
Verbal Fluency Test (VFT; Henry & Crawford, 2004). In addition, we evaluated
participant’s anxiety levels with the Beck Anxiety Inventory (BAI; Cunha, 2001)
and World Health Organization Quality of Life for Older Persons (WHOQOL-
OLD) module (Fleck, Chachamovich, & Trentini, 2006).
The Digit Span test we used was a sub-test of the Wechsler Adult Intelligence
Scale (WAIS-III; Ryan & Schnakenberg-Ott, 2003). The WAIS-III is a 60- to 90-
minute intelligence test with many separate subtests and several summary indices
Alves et al. 5

that represent an examinee’s score in relation to a normative group of same aged


persons as standard scores with a mean of 100 and standard deviation of 15.
The WAIS-III was adapted, validated, and standardized for Brazilian samples
by Nascimento (2000). Among different cognitive subskills measured by this
instrument is executive functioning (Macuglia et al., 2015). The Digit Span
subtest of the WAIS-III evaluates attention, working memory, and sequential
processing, all of which are frequently altered functions in patients with PD
(David et al., 2015; Fernandes et al., 2016; Kudlicka, Clare, & Hindle, 2011;
Macuglia et al., 2015).
The VFT is easy to apply, not time consuming, and sensitive to cognitive
difficulties commonly seen among persons with PD (Koerts et al., 2013).
Through speed and efficiency of verbal fluency, this test directly and indirectly
measures associated organization skills, executive functioning, psychomotor
speed, operational memory, and inhibition of inappropriate responses (Da Silva
et al., 2011; Henry & Crawford, 2004; Koerts et al., 2013). Within this test, par-
ticipants are required to verbalize as many words as possible belonging to an
assigned semantic category (e.g., animals or fruits) within one minute.
The BAI is a self-report scale of anxiety. The instrument has been shown to be
appropriate for use not only in psychiatric patients but also to the medical clinic
and for the nonclinical population as elderly people. It takes about five minutes
to complete, and it measures self-reported anxiety severity. It has been found to
be internally consistent (Cronbach’s alpha coefficient between .83 and .92) for an
elderly population (Baptista & Carneiro, 2011). Internal consistency of the BAI
for use in PD was satisfactory (Cronbach’s a ¼ 0.88), as was the test–retest reli-
ability (r ¼ 0.77; Dissanayaka, Torbey, & Pachana, 2015).
The WHOQOL_OLD is an instrument intended for assessing self-perceived
quality of life. It comprises 24 items rated on a 5-point Likert scale; it evaluates
sensory abilities, autonomy, self-perception of some physical activities, the indi-
vidual’s perception about death, and the person’s self-perceived satisfaction with
intimacy issues (Margis, Donis, Schönwald, & Rieder, 2010). The WHOQOL-
OLD module is a useful alternative with good psychometric performance in
the investigation of quality of life in older adults. The WHOQOL-OLD was
validated for use in Brazil by Fleck et al. (2006) and has adequate internal
consistency (Cronbach’s alpha coefficients ranging from 0.71 to 0.88), discrim-
inant validity (p < .01), concurrent validity (correlation coefficients ranging from
0.61 to 0.50) and test–retest reliability (correlation coefficients ranging from
0.58 to 0.82).

Interventions
After their initial evaluations with the tools described earlier, participants were
distributed nonrandomly into three different equal-sized groups of nine partici-
pants each—the two experimental groups: Xbox KinectTM group and Nintendo
6 Perceptual and Motor Skills 0(0)

WiiTM group—and a control group. The two experimental groups each received
10 individual training sessions (specific to each group) overseen by a physical
therapist, occurring two times per week, during the ‘‘on’’ phase of dopaminergic
medication. One physical therapist (F. A. S. M.) and a neuropsychologist (C. S.)
with more than 10 years of clinical experience selected in advance four games
from each gaming device so that participants receiving either Xbox KinectTM or
Nintendo WiiTM game exposure engaged in games that had similar motor and
cognitive demands. The game selection procedure was initiated by analyzing the
motor demands of the entire repertoire of games offered by the Wii Fit Plus and
Kinect (Adventures and Your Shape: Fitness Evolved) packages, by a physical
therapist. The game selection procedure, with regard to motor demands, was
established by the identification of games that had potential for gait training,
based on the description of the movements to be performed by the player that is
provided by each gaming device. With this procedure, 16 games were selected.
Then, the neuropsychologist who established four pairs of games based on their
cognitive demands (four games from each gaming device), analyzed the main
tasks of the games. Therefore, the games selected for training had similar motor
and cognitive demands (Table 1).
From Nintendo WiiTM, games were Rhythm Parade, Obstacle Course,
Tightrope Walk, and Basic Step; from Xbox KinectTM, games were Hurdles,
River Rush, Reflex Ridge, and Light Race. The gaming devices were connected
to an interact projector that projected the game image onto a screen positioned
two meters away and in front of the participant. Participants played the games
selected for their specific group three or five times per game in each session,
depending on the game’s duration. Before the start of the first virtual training
session, the physical therapist explained the objectives and allowed each partici-
pant a trial attempt per game to familiarize themselves with the tasks and equip-
ment. During these first attempts, the physical therapist gave manual and verbal
cues to the patient to promote a correct posture and perform movements
required to interact with the game and achieve its goals. Each virtual training
session lasted 45–60 minutes. In the last attempt, the participants played without
any help, except for verbal motivation. Rest periods were observed between
games as needed. For clinical safety, we monitored participants’ heart rates
and blood pressure in all training sessions. The control group performed all
pre-, post-, and follow-up testing evaluations over the 5-week period but
received no training of any type during the 5-week game training period.

Data Analysis
All analyses were performed using the SPSS 21.0 statistical package (SPSS Inc.,
Chicago, IL, USA). Group data were summarized with means and standard
deviations. Univariate Analysis of Variance (ANOVA) was performed to test
between-group comparisons. The Shapiro–Wilk test confirmed the normality of
Table 1. Main Games Tasks and Demands.

Nintendo Xbox Main cognitive


Wii games Tasks Kinect games Tasks Main motor demands demands

Obstacle Walk as fast as possible on Hurdles Run avoiding obstacles Fast stationary walk Response inhibition
Course a course, avoiding avoiding obstacles and planning to
obstacles avoid obstacles
Basic Step Alternate steps according Light Race Alternate steps Alternate steps Sustained attention
to the game’s music according to the according to rhythm and visuospatial
rhythm and visual game’s rhythmic determined by game capacity to follow
stimuli visual stimuli visual and auditory
cues which direct
foot movements
Rhythm Parade Marching in place to the Reflex Ridge Avoid obstacles while Alternate steps while Divided attention
sound of a beat while moving arms to moving arms between alternating
moving arms according collect virtual coins steps and moving
to the visual stimuli both arms
Tightrope Walk Keep balance while walk- River Rush Drive a boat choosing Shift center of gravity Sustained attention
ing on a tightrope and the best way to latero-laterally and decision making
avoid obstacles avoid obstacles and on shifting direction
collect virtual coins

7
8 Perceptual and Motor Skills 0(0)

Table 2. Participant Characteristics and Between-Group Comparisons.

Groups

Nintendo Xbox Control


Characteristics Wii Kinect Group Total p ES

Age (years) 58.89 (11.16) 62.67 (13.81) 61.67 (10.74) 61.07 (10.74) .75 .23
Education (years) 10.56 (4.64) 12 (4.89) 11.78 (4.94) 11.44 (4.68 .79 .01
MME (score) 27.11 (2.8) 27.44 (2.35) 25.44 (2.29) 26.67 (2.55) .21 .12
GDS-15 (score) 3.67 (1.9) 2.67 (2.91) 5.00 (0.86) 3.78 (2.22) .07 .19
H&Y 1.89 (0.92) 1.56 (0.72) 1.78 (0.83) 1.74 (0.81) .69 .03
Male gender (n, %) 9 (100) 8 (88.8) 8 (88.8) 25 (92.6)
Note. n ¼ 9 for all groups. Statistics presented as M (SD). ES ¼ effect size; MME ¼ mini mental examination;
H&Y ¼ Hoehn and Yahr scale; GDS-15 ¼ Geriatric Depression Scale—15 items.

the data distribution, and a repeated measures ANOVA (RM-ANOVA) with


time (pre, post, and follow-up) as the within-subjects factor and groups
(Nintendo WiiTM, Xbox KinectTM and Control group) as the between subjects
factor was used to evaluate clinical outcomes. The Tukey test was used for post
hoc analysis of specific two-way comparisons between variables.

Results
Participant Characteristics
The demographic and clinical characteristics of the participants are presented in
Table 2. Baseline features of both groups were similar for all variables.

Clinical Outcomes
Table 3 shows clinical outcomes on gait performance for each group. In the
30-second gait test under the simple task condition, we observed a decrease in
the number of steps in relation to the distance walked in the Nintendo WiiTM
group, relative to other groups, F(2, 19) ¼ 3.37, p ¼ .007, suggesting an increase
in the length of the step. In the dual condition walking task, participants in the
Nintendo WiiTM group also showed an increase in the distance walked and a
decrease in the number of steps per meter, F(2, 19) ¼ 4.57, p ¼ .049, and F(2,
19) ¼ 4.98, p ¼ .035, respectively. The Xbox KinectTM and control groups dem-
onstrated no significant improvements in either condition of the walking task or
on other measures. Table 4 describes the results of individuals’ cognitive per-
formance, anxiety, and quality of life measures. Participants in the Nintendo
WiiTM group showed improved scores on Digit Span backward, F(2, 19) ¼ 3.44,
Table 3. Patients’ Performance in Gait Assessments Pre and Post Training and 30 Days After the End of Training for Experimental and
Control Groups.
Alves et al.

Mean difference (SD) Mean difference (SD)


Follow-up between pre training between pre training
Pretesting Posttesting testing and post training and follow-up
Mean (SD) Mean (SD) Mean (SD) [95% CI of difference] [95% CI of difference]

Timed Up and Go Test (RM-ANOVA; p  .05; observed power ¼ 0.511)


Nintendo Wii group 10.44 (2.16) 9.77 (1.5) 9.86 (1.48) 0.66 (0.70) [0.80 a 2.13] 0.58 (0.82) [1.13 a 2.29]
Xbox Kinect group 11.68 (5.22) 9.82 (3.41) 9.86 (1.48) 1.86 (0.70) [0.39 a 3.33] 1.37 (0.82) [3.34 a 3.08]
Control group 13.13 (5.80) 12.46 (4.67) 11.33 (5.28) 0.33 (0.75) [1.24 a 1.91] 2.12 (0.8) [0.43 a 3.8]
Total 11.51 (4.34) 10.37 (3.21) 10.36 (3.06)
10Meter Walk Test: Time (s) (RM-ANOVA; p  .05; observed power ¼ 0.292)
Nintendo Wii group 7.03 (1.52) 6.89 (1.05) 7.95 (1.54) 0.13 (0.32) [0.54 a 0.81] 0.91 (0.36) [1.67 a 0.16]
Xbox Kinect group 7.07 (1.40) 6.96 (1.46) 6.81 (1.43) 0.10 (0.32) [0.57 a 0.78] 0.25 (0.36) [0.50 a 1.01]
Control group 9.31 (3.80) 8.63 (3.06) 7.68 (3.00) 0.68 (0.43) [0.22 a 1.59] 1.62 (0.48) [0.60 a 2.64]
Total 7.54 (2.26) 7.30 (1.84) 7.45 (1.88)
10-Meter Walk Test: Velocity (m/s) (RM-ANOVA; p  .05; observed power ¼ 0.112)
Nintendo Wii group 1.47 (0.31) 1.47 (0.23) 1.29 (0.24) 0.003 (0.05) [0.11 a 0.11] 0.18 (0.07) [0.03 a 0.33]
Xbox Kinect group 1.44 (0.21) 1.48 (0.27) 1.51 (0.26) 0.03 (0.05) [0.15 a 0.07] 0.06 (0.07) [0.21 a 0.08]
Control group 1.24 (0.56) 1.29 (0.52) 1.45 (0.54) 0.05 (0.07) [0.20 a 0.10) 0.21 (0.09) [0.41 a 0.23)
Total 1.41 (0.34) 1.43 (0.32) 1.41 (0.33)
30-Seconds Walk Test in simple task: Distance (m) (RM-ANOVA; p.05; observed power ¼ 0.665)
Nintendo Wii group 36.27 (6.40) 36.91 (6.53) 36.71 (3.67) 0.64 (1.62) [4.03 a 2.74] 0.44 (1.76) [4.12 a 3.23]
Xbox Kinect group 43.64 (7.91) 42.07 (3.52) 45.09 (8.08) 1.57 (1.62) [1.81 a 4.96] 1.44 (1.76) [5.12 a 2.23]
Control group 30.82 (6.80) 31.19 (5.99) 37.07 (9.90) 0.37 (2.18) [4.91 a 4.17] 6.24 (2.36) [11.18 a 1.3]
Total 37.97 (8.49) 37.68 (6.65) 40.07 (7.96)

9
9

(continued)
10
Table 3. Continued

Mean difference (SD) Mean difference (SD)


Follow-up between pre training between pre training
Pretesting Posttesting testing and post training and follow-up
Mean (SD) Mean (SD) Mean (SD) [95% CI of difference] [95% CI of difference]

30-Seconds Walk Test in simple task: Steps/distance (steps/m) (RM-ANOVA; p  .05; observed power ¼ 0.664)
Nintendo Wii group 1.64 (0.31) 1.52 (0.28) 1.44 (0.25)a 0.12 (0.06) [0.008 a 0.25] 0.20 (0.06) [0.06 a 0.33]
Xbox Kinect group 1.41 (0.16) 1.52 (0.08) 1.43 (0.24) 0.10 (0.06) [0.23 a 0.02] 0.17(0.06) [0.15 a 0.12]
Control group 1.78 (0.4) 1.78 (0.38) 1.62 (0.44) 0.004 (0.08) [0.17 a 0.17] 0.15 (0.08) [0.28 a 0.34]
Total 1.58 (0.31) 1.58 (0.26) 1.48 (0.29)
30-Seconds Walk Test in dual task: Distance (m) (RM-ANOVA; p  .05; observed power ¼ 0.573)
Nintendo Wii group 31.18 (5.8) 32.70 (5.33) 34.79 (5.14)b 1.5 (2.08) [5.86 a 2.84] 3.6 (1.71) [7.18 a 0.01]
Xbox Kinect group 40.76 (4.14) 39.73 (10.79) 40.09 (8.55) 1.03 (2.08) [3.32 a 5.38] 0.66 (1.71) [2.91 a 4.25]
Control group 28.39 (11.16) 26.54 (8.7) 32.34 (9.13) 1.85 (2.8) [3.98 a 7.69) 3.9 (2.3) [8.7 a 0.85)
Total 34.32 (8.37 34.11 (9.65) 36.33 (7.85)
30-Seconds Walk Test in dual task: Steps/distance (steps/m) (RM-ANOVA; p  .05; observed power ¼ 0.735)
Nintendo Wii group 1.72 (0.34) 1.68 (0.36) 1.53 (0.22)c 0.04 (0.10) [0.16 a 0.25] 0.19 (0.08) [0.16 a 0.37]
Xbox Kinect group 1.49 (0.14) 1.57 (0.27) 1.52 (0.21) 0.07 (0.10) [0.28 a 0.12] 0.03 (0.08) [0.21 a 0.14]
Control group 2.21 (0.68) 2.21 (0.68) 1.91 (0.42) 0.004 (0.13) [0.27 a 0.28) 0.29 (0.11) [0.05 a 0.53)
Total 1.74 (0.46) 1.75 (0.46) 1.61 (0.30)
RM-ANOVA ¼ repeated measures analysis of variance; SD ¼ standard deviation; CI ¼ confidence interval.
a
Post hoc Tukey tests: pre testing  follow-up testing comparison: p ¼ .007.
b
Post hoc Tukey tests: pre testing  follow-up testing comparison: p ¼ .049.
c
Post-hoc Tukey tests: pre testing  follow-up testing comparison: p ¼ .035.
Table 4. Patients’ Performance in Cognitive Performance, Anxiety, and Quality of Life Measure Pre- and Posttraining and 30 Days After
the End of Training for Experimental and Control Groups.

Mean difference (SD) Mean difference (SD)


between pre training between pre training
Pre testing Post testing Follow-up testing and post training and follow-up
Mean (SD) Mean (SD) Mean (SD) [95% CI of difference] [95% CI of difference]

Digit Span Forward


(RM-ANOVA; p  .05; observed power ¼ 0.115)
Nintendo Wii group 10.56 (2.16) 11.0 (1.58) 10.89 (1.48) 0.44 (0.51) [1.51 a 0.62] 0.33 (0.52) [1.42 a 0.75]
Xbox Kinect group 8.78 (2.58) 8.89 (2.14) 8.22 (2.43) 0.11 (0.51) [1.17 a 0.95] 0.55 (0.52) [0.53 a 1.64]
Control group 7.40 (1.14) 7.40 (2.30) 7.20 (1.92) 0.00 (0.68) [1.43 a 1.43] 0.20 (0.70) [1.26 a 1.66]
Total 9.17 (2.46) 9.39 (2.36) 9.04 (2.82)
Digit Span Backward
(RM-ANOVA; p  .05; observed power ¼ 0.512)
Nintendo Wii group 4.44 (2.24) 4.43 (1.29) 6.00 (2.12)a 0.013 (0.55) [1.13 a 1.16] 1.55 (0.44) [2.49 a 0.62]
Xbox Kinect group 4.71 (1.43) 4.69 (1.23) 5.21 (1.29) 0.024 (0.55) [1.12 a 1.17] 0.49 (0.44) [1.43 a 0.44]
Control group 4.00 (1.22) 4.20 (1.64) 4.00 (2.0) 0.20 (0.74) [1.74 a 1.34] 1.0 (0.60) [1.25 a 1.25]
Total 4.45 (1.71) 4.48 (1.3) 5.25 (1.88)
Verbal Fluency Test
(RM-ANOVA; p  .05; observed power ¼ 0.086)
Nintendo Wii group 14.00 (4.18) 15.22 (4.41) 15.33 (3.31) 1.22 (2.45) [6.35 a 3.90] 1.33 (1.29) [4.02 a 1.36]
Xbox Kinect group 19.33 (5.91) 17.00 (7.93) 16.89 (4.54) 2.33 (2.45) [2.79 a 7.46] 2.44 (1.29) [0.25 a 5.13]
Control group 14.20 (8.04) 12.60 (4.39) 13.20 (8.40) 1.60 (3.30) [5.28 a 8.48) 1.00 (1.73) [2.61 a 4.61)
Total 16.13 (6.14) 15.35 (6.02) 15.48 (5.13)
(continued)

11
12
Table 4. Continued

Mean difference (SD) Mean difference (SD)


between pre training between pre training
Pre testing Post testing Follow-up testing and post training and follow-up
Mean (SD) Mean (SD) Mean (SD) [95% CI of difference] [95% CI of difference]

Beck Anxiety Inventory


(RM-ANOVA; p  .05; observed power ¼ 0.112)
Nintendo Wii group 11.33 (9.92) 7.19 (4.73)b 6.24 (3.97)c 4.13 (1.93) [0.09 a 8.17] 5.08 (2.19) [0.51 a 9.65]
Xbox Kinect group 7.61 (4.73) 4.91 (2.43) 4.69 (2.13) 2.70 (1.93) [1.33 a 6.74) 2.92 (2.19) [1.64 a 7.49]
Control group 21.80 (9.09) 18.0 (7.51) 19.60 (10.08) 3.80 (2.6) [1.62 a 9.22] 2.20 (2.94) [3.93 a 8.33]
Total 12.15 (9.24) 8.65 (6.85) 8.54 (7.86)
Quality of Life Questionnaire (WHOQOL_OLD) (RM-ANOVA; p  .05; observed power ¼ 0.102)
Nintendo Wii group 90.56 (14.32) 93.78 (14.95) 88.44 (16.94) 3.22 (2.63) [8.71 a 2.27] 2.11 (2.65) [3.43 a 7.65]
Xbox Kinect group 74.33 (8.97) 74.33 (11.12) 75.22 (9.96) 1.14 (2.63) [5.49 a 5.49] 0.88 (2.65) [6.43 a 4.65]
Control group 73.80 (11.45) 74.00 (7.58) 74.00 (11.24) 0.20 (3.53) [7.57 a 7.17) 0.20 (3.56) [7.63 a 7.23]
Total 80.57 (13.96) 81.87 (15.23) 80.13 (14.49)
RM-ANOVA ¼ repeated measures analysis of variance; SD ¼ standard deviation; CI ¼ confidence interval.
a
Post hoc Tukey tests: pre testing  follow-up testing comparison: p ¼ .002.
b
Post hoc Tukey tests: pre testing  post testing comparison: p ¼ .045.
c
Post hoc Tukey tests: pre testing  follow-up testing comparison: p ¼ .031.
Alves et al. 13

p ¼ .002, and BAI scores pre- and posttesting, F(2, 19) ¼ 3.76, p ¼ .045, and
p ¼ .031, respectively, meaning improved working memory and reduced anxiety,
respectively.

Discussion
To the authors’ knowledge, this is the first comparative study of commercial video
game-based rehabilitation training for patients with PD. Our main finding was of
greater patient improvement with the Nintendo WiiTM console, compared with
Xbox KinectTM or a control group condition of no rehabilitation training.
Training gains after 10 sessions of 45–60 minutes each with the Nintendo WiiTM
were evident with respect to gait improvements, better working memory on Digit
Span Backward from the WAIS-III, and reduced anxiety on the BAI. Participants
who trained with the Xbox KinectTM and those in the control group failed to
improve. This finding is in contrast to our hypothesis that those trained with the
Xbox KinectTM would also show gains in relation to those in the control group.
Given that all the groups were closely matched and that games of both devices had
similar motor and cognitive demands, the differences we found in participants’
clinical improvements across these groups may be attributed to differences in the
features of these devices. Nintendo WiiTM is a commercial gaming device that uses a
manual wireless controller and a force platform called WBB, allowing the user to
simulate a variety of cognitive-motor activities in an easy-to-use, inexpensive
format that offers good reliability (Holmes, Jenkins, Johnson, Hunt, & Clark,
2012). Previous studies also investigated the motor and cognitive effects of training
with Nintendo WiiTM in patients with PD, though they did not directly compare
these game effects with the game effects of the Xbox KinectTM. Pompeu et al. (2012)
compared Nintendo WiiTM games with conventional training through balance
exercises and found that both training methods promoted improved performance
of activities of daily living, balance, and cognition. Zimmermann et al. (2014)
compared two types of computer training for improving cognitive functions in 39
persons with PD over 12 sessions, using four games in CogniPlusTM (a specific game
system for cognitive training) and four games in the Nintendo WiiTM (a nonspecific
game system for cognitive training). The Nintendo WiiTM produced slightly super-
ior improvement in attention, relative to the CogniPlusTM.
In our study, participants’ improvements in gait performance when trained on
the Nintendo WiiTM were evident on the 30-Second Walk Test in both single task
and dual task conditions through both an increase in distance covered and a
decrease in the number of steps taken, suggesting longer participant step
length. This finding is consistent with findings of Gonçalves et al. (2014), who
identified increased step length in patients with PD after 14 training sessions with
Wii Fit Plus games. Gonçalves et al. also demonstrated an increase in walking
speed in these individuals. The average velocity for participants in this study,
however, was 0.48 meters/second in the initial evaluation, different from
14 Perceptual and Motor Skills 0(0)

participants in our study whose velocity was faster, 1.41 meters/second. In previ-
ous studies of patients with PD, reported gait velocity was between 0.18 and
1.21 metrs/second (Brusse, Zimdars, Zalewski, & Steffen, 2005; Combs, Diehl,
& Filip, 2014; Paker et al., 2015; Steffen & Seney, 2008). Thus, our participants’
faster initial walking speed may have left less room for further improvement from
proposed interventions.
Patients with PD have both motor and cognitive dysfunction, making
them more vulnerable to performance problems in dual task conditions
when they are more apt to walk slowly and increase their fall risk (Hausdorff,
2009; Yogev-Seligmann, Giladi, Borzgol, & Hausdorff, 2012). In the
present study, both distance walked and step length increased significantly
even in the dual task 30-Second Walk Test after training with the Nintendo
WiiTM gaming device. Similarly, Yogev-Seligmann et al. (2012) also demon-
strated a reduction in gait variability of patients with PD after 12 specific train-
ing sessions to reduce the negative effects of dual task conditions on walking.
This training consisted of five walking blocks of five minutes each with simul-
taneous cognitive tasks.
The TUG is a test designed to evaluate elderly mobility, and it is also a useful
tool for evaluating patients with PD (Morris et al., 2001). Previous studies have
shown a mean score of over 13.7 seconds in participants with PD on the TUG
(Martinez-Martin, 1997; Paker et al., 2015), and Nocera et al. (2013) proposed a
cutoff value of 11.5 seconds to discriminate fall risk for people with PD. In our
study, participants in both the experimental groups, Nintendo WiiTM and Xbox
KinectTM, presented scores lower than this cutoff, with mean values at 10.44 and
11.13, respectively, with no significant reduction after performing the virtual
training. Thus, here too our participants appeared to be higher functioning
than those in some prior studies.
We also found that BAI anxiety scores of our participants with PD decreased
significantly after training with the Nintendo WiiTM Decreased anxiety level
facilitates the treatment of motor symptoms since anxiety is associated with
an increase in motor symptoms, more severe gait changes, and dyskinesia.
These participants’ reduced anxiety level may be related to the offer of graphics,
sounds, images, and friendly tasks provided by the Nintendo WiiTM that con-
tributed to the participants’ ability to perform larger movements that were pre-
viously avoided by a fear of falling. However, as noted, the Xbox KinectTM did
not facilitate these improvements.
The treatment of cognitive dysfunction in patients with PD is a challenge, as
it frequently does not respond to dopaminergic therapy. Research investigating
the effect of exercise on cognitive changes in patients with PD has demonstrated
promising results (David et al., 2015). David et al. (2015) showed, through a
randomized clinical trial of 46 patients with PD, that 24 months of exercises,
performed twice a week, improved attention and working memory, identified by
improved performance on the Digit Span and Stroop Tests. Similarly, the
Alves et al. 15

present study showed that 10 VR training sessions with the Nintendo WiiTM
gaming device improved Digit Span Backward scores of persons with PD. A
low score on this test may indicate inability to expend the attention needed to
solve more difficult mental activities (Lopes et al., 2012). Fernandes et al. (2016)
investigated the relationship between balance and executive functioning and
showed that Digit Span was sufficiently associated with balance skills in this
population that scores on this test were able to predict balance skills in individ-
uals with PD. Even with training through the Nintendo WiiTM, patients did not
improve their performance on the Digit Span Forward or VFT, probably
because these tests were less sensitive to game-related improvements, perhaps
specifically including reverse sequential processing and the ability to retain
immediate and long-term memory (Lopes et al., 2012).
Few studies have investigated the therapeutic effects of Xbox KinectTM. In con-
trast to the Nintendo WiiTM, the Xbox KinectTM tracks body movements with an
infrared camera that recognizes real-time three-dimensional gestures, allowing the
user to interact with the game without controllers. This is considered an equipment
and efficiency advantage in comparison with the Nintendo WiiTM (Dos Santos
Mendes et al., 2015; Pompeu et al., 2014), as both the Xbox KinectTM and the
Nintendo WiiTM games were developed only for recreation and not for rehabilita-
tion needs of people with neurological disabilities. However, the net effect, when
these devices are used with persons who have PD is that the Kinect sensor is less
sensitive than the WBB to tracking the center of pressure displacement, making it
less useful for providing tactile feedback to the user. WBB can also be considered a
visual reference and a cue to facilitate patient movement in patients with PD who
have well documented difficulties initiating movement. Xbox KinectTM does not
have visual references that delimit the sensor capable space. Thus, when users reach
areas beyond the space recognized by the sensor, their movements are not trans-
ferred to the games, and the game adapts by projecting on the screen an image
directing the users to the correct location. This information can be considered a
further distractor for people with PD. As people with PD have difficulty with divided
attention, achievement of dual tasks, inhibition of response, and sustained attention,
Xbox KinectTM games may be more difficult and less effective rehabilitative tools for
persons with PD. Wii hardware can be integrated into physical rehabilitation pro-
grams more easily (Bonnechère et al., 2016). Also complicating rehabilitation
through the Xbox KinectTM, the graphics of these games have more details and
may present more interference through distractors for patients with PD whose cog-
nitive alterations may include visuospatial disorders, slow decision processes, and
difficulty in selective attention. For these reasons, people with PD seem to experience
greater benefits in the simpler and less distracting interface of the Nintendo WiiTM.
Among the most important limitations of the present study is our small par-
ticipant sample size, perhaps rendering insufficient statistical power for the
detection of statistically significant differences of small effect size and limiting
wide generalizability of these findings to other persons with PD, particularly
16 Perceptual and Motor Skills 0(0)

given our inclusion/exclusion criteria for entry into this study. A second import-
ant concern is that we were not able to randomly allocate participants to the
experimental and control groups but, instead, assigned participants by recruit-
ment order, where the experimental groups, Nintendo WiiTM and Xbox
KinectTM, respectively, were first arranged and thereafter, the control group.
Given these limitations, there is a clear need for replication of these results in a
larger participant sample, randomly assigned to research groups and, for future
studies, to address the extent to which these findings may or may not apply more
broadly to a more impaired subgroup of people with PD.

Declaration of Conflicting Interests


The author(s) declared no potential conflict 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, author-
ship, and/or publication of this article: The research was supported by the ‘‘Fundação de
Apoio à Pesquisa do Distrito Federal (FAPDF)’’ (Grant Number: 193.000655/2015).

ORCID iD
Melissa L. M. Alves http://orcid.org/0000-0003-0250-5160

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Author Biographies
Melissa L. M. Alves, Msc, is a physiotherapist graduated by the Faculty of Ceilǎndia at the University
of Brasilia. She received her Master’s Degree in Physical Education from the University of Brasilia in
2017. Her research interests are the use of virtual reality in Parkinson’s Disease.

Beatriz S. Mesquita, Msc, is a physiotherapist graduated by the Faculty of Ceilǎndia at the


University of Brasilia. She received her Master’s Degree in Physical Education from the
University of Brasilia in 2016.

Wenderson S. Morais is a physiotherapist graduated by the Faculty of Ceilǎndia at the University of


Brasilia. Currently, Wenderson is a Master’s Degree student in the Rehabilitation Program of the
Faculty of Ceilǎndia at the University of Brasilia, investigating the use of Virtual Reality in
Parkinson’s Disease.

Josevan C. Leal, PhD, is an assistant professor in the Faculty of Ceilǎndia at the University of
Brası́lia. He received his PhD Degree in Medical Sciences from the University of Brasilia in 2010.
His research interests are the use of virtual reality in rehabilitation of cognitive and motor impair-
ments in neurological patients and aquatic rehabilitation.

Corina E. Satler, PhD, is an assistant professor in the Faculty of Ceilǎndia at the University of
Brasilia. She received her PhD degree in Neuroscience and Behavior from the University of Brasilia
in 2012. His research interests are in the area of neuropsychology and cognitive neuroscience.

Felipe A. dos Santos Mendes, PhD, is an assistant professor in the Faculty of Ceilǎndia at the
University of Brasilia. He received his PhD degree in Neuroscience and Behavior from the
University of Sao Paulo in 2012. His research interests are the use of virtual reality in rehabilitation
of cognitive and motor impairments in neurological patients.

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