578295

research-article2015

CRE0010.1177/0269215515578295Clinical RehabilitationWang et al.

CLINICAL
REHABILITATION

Article

Cognitive motor intervention for

gait and balance in Parkinsons
disease: systematic review and
meta-analysis

Clinical Rehabilitation
2016, Vol. 30(2) 134144
The Author(s) 2015
Reprints and permissions:
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DOI: 10.1177/0269215515578295
cre.sagepub.com

Xue-Qiang Wang1*, Yan-Ling Pi2*, Bing-Lin Chen1,

Ru Wang1, Xin Li1 and Pei-Jie Chen1

Abstract
Objective: We performed a systematic review and meta-analysis to assess the effect of cognitive motor
intervention (CMI) on gait and balance in Parkinsons disease.
Data sources: PubMed, Embase, Cochrane Library, CINAHL, Web of Science, PEDro, and China Biology
Medicine disc.
Methods: We included randomized controlled trials (RCTs) and non RCTs. Two reviewers independently
evaluated articles for eligibility and quality and serially abstracted data. A standardized mean difference
standard error and 95% confidence interval (CI) was calculated for each study using Hedges g to quantify
the treatment effect.
Results: Nine trials with 181 subjects, four randomized controlled trials, and five single group intervention
studies were included. The pooling revealed that cognitive motor intervention can improve gait speed
(Hedges g = 0.643 0.191; 95% CI: 0.269 to 1.017, P = 0.001), stride time (Hedges g = -0.536 0.167;
95% CI: -0.862 to -0.209, P = 0.001), Berg Balance Scale (Hedges g = 0.783 0.289; 95% CI: 0.218 to
1.349, P = 0.007), Unipedal Stance Test (Hedges g = 0.440 0.189; 95% CI: 0.07 to 0.81, P =0.02).
Conclusions: The systematic review demonstrates that cognitive motor intervention is effective for
gait and balance in Parkinsons disease. However, the paper is limited by the quality of the included trials.
Keywords
Cognitive motor intervention, Parkinsons disease, gait, balance, systematic review
Received: 11 October 2014; accepted: 14 February 2015

Introduction
Cognitive motor intervention is becoming an
increasingly popular means of enhancing gait and
balance ability.1 Cognitive motor intervention is
where a cognitive exercise and a motor exercise are
conducted simultaneously, such as performing balance exercise while doing cognitive exercise.2 In
fact, most daily activities require the ability to
maintain balance while performing various tasks.

1Sport

Medicine & Rehabilitation Center, Shanghai University

of Sport, Shanghai, China
2Department of Rehabilitation Medicine, Shanghai Punan
Hospital, Shanghai, China
*These authors contributed equally to this study.
Corresponding author:
Pei-Jie Chen, Sport Medicine & Rehabilitation Center, Shanghai
University of Sport, Changhai Rd 399, Shanghai 200438, China.
Email: chenpeijie@sus.edu.cn

Wang et al.
Therefore, falling could be prevented by training to
perform cognitive motor tasks simultaneously.
Parkinsons disease is a neurodegenerative disease that often leads to movement impairments,
particularly gait and balance dysfunction.3 de
Bruin showed that cognitive motor intervention,
conversing whilst the music accompanied walks,
can improve the gait and motor function of
patients with Parkinsons disease.4 And a recent
systematic review with 15 randomized controlled
trials demonstrated that cognitive motor intervention could be effective for improving gait speed,
stride length, cadence and balance function for
patients with stroke.5 Many studies found exercise was an effective strategy for improving gait
and balance function.68 However, the effect of
cognitive motor intervention on the gait and balance of Parkinsons disease patients remains
unclear.
A published systematic review,9 which included
28 articles, reported that limited evidence is available on the ability of cognitive motor intervention to
promote physical function in patients with neurological impairments. And another systematic review,
which covered 30 randomized controlled trials with
1,206 subjects, showed that cognitive motor intervention was more effective than no intervention or
single-task exercise for improving gait and balance
function in older people.10 However, this review did
not focus on Parkinsons disease.
To date, no systematic review or meta-analysis
has been conducted on cognitive motor intervention in relation to the gait and balance function of
patients with Parkinsons disease. Moreover, the
extent of cognitive motor interventions effectiveness to improve the gait and balance in Parkinsons
disease remains unclear. Thus, the aim of this systematic review and meta-analysis is to assess the
effect of cognitive motor intervention for gait and
balance functionin Parkinsons disease.

Methods
Relevant articles dated June 1980 to January 2015
were identified from the following databases:
PubMed, Embase, Cochrane Library, Ebsco
(CINAHL), Web of Science, PEDro, and China

135
Biology Medicine disc. The electronic search
strategies for all of the databases are provided in
supplementary material Appendix 1. Manual
searching was also performed. The protocol was
registered on the international prospective register
of systematic reviews (PROSPERO registration
number: CRD42012002606).
Inclusion criteria were as follows: types of studies were randomized controlled trials (RCTs) and
non-RCTs; we included studies on patients with
Parkinsons disease; types of outcome measures
were gait variables, such as gait speed and stride
length, and balance function, such as Berg Balance
Scale, center of pressure sway. Inclusion criteria
interventions: (1) subjects who performed cognitive motor intervention were compared with those
who underwent other therapies or no intervention;
(2) subjects who performed cognitive motor intervention and were assessed before and after treatment. In cognitive motor intervention, subjects
perform a motor task (e.g., balance exercise) while
accomplishing a cognitive task exercise (e.g., addition/subtraction questions, 8 + 5 = 13).2 Other
forms of feedback and attention strategies can also
be included in cognitive motor exercise, such as
the use of virtual reality techniques and electronic
gaming (e.g., Wii).9
Two authors independently used the same selection criteria to screen titles, abstracts, and full papers
of the relevant articles. Studies that failed to meet
the inclusion criteria were removed. Any disagreement is resolved through discussion. A third author
was consulted if any disagreement persisted.
A standardized form was used to extract the data
from the included studies. The following data were
extracted: study characteristics (e.g., author and
year), participant characteristics (e.g., age and
number of subjects), description of interventions,
duration of trial period, and types of outcomes
assessed. The data extraction was performed by the
same two authors who selected the studies.
The Physiotherapy Evidence Database scale11
(with scores from 1 to 10) was used to assess the
quality of the RCTs and non-RCTs with a control
arm. We used modified Downs and Black tool12 to
evaluate the quality of the single-group interventional studies. The modified Downs and Black

136
tool comprised 27 questions about study description, external validity, internal validity, and statistical power.
Two review authors independently used a standardized assessment form to assess the methodological quality of each study. A third author was
consulted if any disagreement occurred.
A standardized mean difference (SMD) standard error and 95% confidence interval (CI) were
calculated for each study by using Hedges g to
quantify the treatment effect. The means and standard deviations could be estimated if the data are
reported in a graph rather than a table. Authors
were contacted if their standard deviations were
not provided. Only the data from the cognitive
motor intervention group were used in the pooled
analyses if the trials estimated the treatment contrast of cognitive motor intervention versus an
alternative intervention.
We used the Comprehensive Meta-analysis software (version 2.0, Biostat, Englewood, NJ, USA)13
to analyze effect sizes, forest plots, and heterogeneity. Cohen14 suggested that an effect size greater
than 0.5 is large, that ranging from 0.2 to 0.5 is
moderate, and that lower than 0.2 is small. Q statistic and I2 statistic were used to assess heterogeneity
among the studies. We used the random effects
model. We considered P < 0.05 to be statistically
significant. If a meta-analysis was not possible, the
results from the clinical trials were described
qualitatively.

Results
Figure 1 shows the process of identifying eligible
trials. Basing on their titles and abstracts, we
included 43 potentially eligible studies (n = 181
patients) from 1048 identified records. After the
full papers were reviewed, nine articles 9, 1522 satisfied the inclusion criteria. The remaining 34 trials
were excluded, because the participants considered
had other neurological illness (e.g., cognitive
impairment and stroke), no intervention or other
interventions. Protocol articles were also excluded.
Four RCTs conducted a comparison between an
intervention group (cognitive motor intervention)
and a control group (no treatment or other

Clinical Rehabilitation 30(2)

interventions). Five articles were single-group
intervention trials, in which all of the subjects were
subjected to cognitive motor intervention. Table 1
presents the characteristics of each included study.
We used the Physiotherapy Evidence Database
scale (with scores from 1 to 10) to assess the methodological quality of RCTs. The PEDro score
(mean SD) for the RCTs was 5.51. Three articles9,15,16 attempted to blind the assessors to the
allocated treatment; one article17 reported allocation concealment; one article15 performed intention-to-treat analysis; and no article blinded the
subjects and the therapist. The modified Downs
and Black tool was used to evaluate the quality of
the single-group interventional studies. The D
owns and Black score (mean SD) for the singlegroup interventional studies was 15.51.30.
Gait variables: three studies9,18,19 with six comparisons were included to assess the effect of cognitive motor intervention on gait speed. The results
showed that cognitive motor intervention improves
the gait speed of patients with Parkinsons disease
(Hedges g = 0.643 0.191; 95% CI: 0.269 to
1.017, P = 0.001) (Figure 1A). Two studies 9,18 with
four comparisons were included to assess the effect
of cognitive motor intervention on stride length.
We found that stride length presented no significant difference between pre- and post-intervention
in Parkinsons disease (Hedges g = 0.245 0.181;
95% CI: 0.110 to 0.600, P = 0.176) (Figure 2B).
Three studies9,18,19 with six comparisons were
included to assess the effect of cognitive motor
intervention on stride time. The results showed that
cognitive motor intervention improves stride time
(Hedges g = 0.536 0.167; 95% CI: 0.862 to
0.209, P = 0.001) (Figure 2C). One study9 with
two comparisons was included to estimate the
effect of cognitive motor intervention on cadence.
The results showed that cadence exhibited no significant difference between pre- and post-intervention (Hedges g = 0.484 0.308; 95% CI: 0.118 to
1.087, P = 0.115) (Figure 2D).
Balance function: three studies9,16,18 were
included to assess the effect of cognitive motor
intervention on the Unified Parkinsons Disease
Rating Scale. We found that cognitive motor intervention improves Unified Parkinsons Disease

Wang et al.

Figure 1. Flow chart of the study selection procedure.

137

Yogev 201219
Single group
intervention trail

Mirelman
201118
Single group
intervention trail

Ma 201117
RCT

Pompeu 201216
RCT

Three times a
week for 4 weeks

Gait (gait speed,

stride time)

Gait (gait speed,

stride length, stride
time),balance (FSST)
and UPDRS score

Three times a
week for 6 weeks

Cognitive motor exercise

Movement time

1 hour per trail

for 60 trails

G1: cognitive motor

exercise
G2: conventional balance
training
Cognitive motor exercise

Balance (BBS, UST)

and UPDRS score

Gait (gait speed,

stride length, stride
time, cadence),
UPDRS score

Balance performance
(COP sway)

Outcome

Twice a week for

7 weeks

Three times
a week for 13
weeks

Twice a week for

6 weeks

Duration of trial
period

G1: cognitive motor

exercise
G2: balance training

G1: cognitive motor

exercise
G2: conventional balance
training
G3: No intervention
G1: cognitive motor
exercise
G2: regular activities

Source: hospital 42 patients

(G1=14, G2=14, G3=14).
Mean age (SD): G1=70.4 y (6.5),
G2=70.1 y (6.9), G3=71.6 y (5.8)
Hoehn and Yahr stages: 2 to 3
Source: not specified 22 patients
(G1=11, G2=11).
Mean age (SD): G1=64.1 y (4.2),
G2=67.0 y (8.1)
Hoehn and Yahr stages: 2 to 3
Source: not specified 22 patients
(G1=11, G2=11).
Age range: 60 to 85 y
Hoehn and Yahr stages: 1 to 2
Source: hospital 31 patients
(G1=17, G2=16).
Age range: 50 to 75
Hoehn and Yahr stages: 2 to 3
Source: not specified 20 patients.
Age range: 55 to 79
Hoehn and Yahr stages: 2 to 3
UPDRS motor score mean (SD) =
26.5 (7.6)
Source: hospital 7 patients.
Age range: 50 to 90
Hoehn and Yahr stages: 2 to 3

Yen 201115
RCT

de Bruin
20109
RCT

Intervention

Patients characteristic

Study, study type

Table 1. Characteristics of included studies.

(Continued)

Downs and
Black: 16

Downs and
Black: 15

PEDro: 5

PEDro: 5

PEDro: 5

PEDro: 7

Quality
assessment

138
Clinical Rehabilitation 30(2)

Three times a
week for 6 weeks
Two times a
week for 7 weeks

Cognitive motor exercise

Cognitive motor exercise

Source: not specified 11 patients.

Age range: 48 to 80 y
UPDRS motor score mean (SD) =
18.4 (7.6)
Source: hospital 16 patients.
Mean age (SD): 68.6 y (8.0)
Hoehn and Yahr stages: 1 to 2

Balance (STST,
TUGT, POMA, CBM,
ABC, UST, 10m walk
test)
Balance (FRT)

Balance (BBS,
DGI,SRT, ABC, COP
sway)

Outcome

Downs and
Black: 14

Downs and
Black: 14

Downs and
Black: 17

Quality
assessment

ABC: Activities-Specific Balance Confidence scale, BBS: Berg Balance Scale, CBM: Community Balance and Mobility assessment, COP: Center of pressure, DGI: Dynamic Gait
Index, FRT: Functional Reach test, FSST: Four Square Step Test, PEDro: Physiotherapy Evidence Database, POMA: Tinetti Performance Oriented Mobility Assessment, RCT:
randomized controlled trial, SRT: Sharpened Romberg Test, STST: Sit-to-Stand test, TUGT: Timed Up and Go test, UPDRS: Unified Parkinsons Disease Rating Scale, UST:
Unipedal Stance Test.

Three times a
week for 8 weeks

Cognitive motor exercise

Source: hospital 10 patients.

Mean age: 67.1 y
Hoehn and Yahr stages: 2.5 to 3

Duration of trial
period

Mhatre
201320
Single group
intervention trail
Esculier
201221
Single group
intervention trail
dos Santos
201222
Single group
intervention trail

Intervention

Patients characteristic

Study, study type

Table 1. (Continued)

Wang et al.
139

140

Clinical Rehabilitation 30(2)

Figure 2. Meta-analyses of cognitive motor intervention on gait function. A: gait speed, B: stride length, C: stride
time and D: cadence. 95% CI=95% confidence intervals. CMI: cognitive motor intervention.
*represents the performance under dual task test condition.

Wang et al.
Rating Scale (Hedges g = 0.492 0.21; 95% CI:
0.903 to 0.081, P = 0.019) (Figure 3A). Two studies15,20 with four comparisons were included to
assess the effect of cognitive motor intervention on
center of pressure sway. We found that center of
pressure sway significantly improved between preand post-intervention (Hedges g = 0.438 0.071;
95% CI: 0.576 to 0.299, P < 0.001) (Figure 3B).
Two studies16,20 were included to assess the effect of
cognitive motor intervention on Berg Balance Scale.
The results showed that cognitive motor intervention improved Berg Balance Scale after intervention
(Hedges g = 0.783 0.289; 95% CI: 0.218 to 1.349,
P = 0.007) (Figure 3C). Two studies 16,21 with four
comparisons were included to assess the effect of
cognitive motor intervention on Unipedal Stance
Test. We found that Unipedal Stance Test significantly improved between pre- and post-intervention
(Hedges g = 0.440 0.189; 95% CI: 0.07 to 0.81, P
=0.02) (Figure 3D).
These studies assessed the effect of cognitive
motor intervention on different outcomes, demonstrating that cognitive motor intervention could
improve the Four Square Step Test,18 the Dynamic
Gait Index,20 the Sit-to-Stand test,21 the Timed Up
and Go test,21 the Tinetti Performance Oriented
Mobility Assessment,21 the 10 m walk test,21 and
the Community Balance and Mobility assessment.21 However, no significant difference was
found for Sharpened Romberg Test20 between preand post-intervention.

Discussion
This systematic review and meta-analysis of articles from four RCTs and five single-group interventional studies, which included 181 subjects,
verified the effect of cognitive motor intervention
in Parkinsons disease. Cognitive motor intervention was found to significantly benefit the following outcomes: gait speed, stride time, Unified
Parkinsons Disease Rating Scale, center of pressure sway, Berg Balance Scale, Unipedal Stance
Test, Four Square Step Test, Dynamic Gait Index,
Sit-to-Stand test, Timed Up and Go test, Tinetti
Performance Oriented Mobility Assessment, 10 m
walk test, and Community Balance and Mobility

141
assessment. The sizes of the majority of the
observed effects between pre- and post-intervention were predominantly not large. However, the
levels of improvements for gait speed, Unified
Parkinsons Disease Rating Scale, center of pressure sway area, Berg Balance Scale, Dynamic Gait
Index, Sit-to-Stand test, Timed Up and Go test, 10
m walk test, and Tinetti Performance Oriented
Mobility Assessment may signify clinical importance in Parkinsons disease. Moreover, no adverse
events for cognitive motor intervention were found
in nine studies.
Various exercise interventions are used to
improve the gait and balance function of patients
with Parkinsons disease. Previous most systematic reviews and meta-analyses2326 have focused
on motor exercise (e.g., resistance exercise and
balance exercise). And previous5, 8, 9, 10, 27, 28 systematic reviews of cognitive motor intervention
have either focused on qualitative synthesis or
have not selected subjects with Parkinsons disease. However, this work is the first systematic
review and meta-analysis that estimates the effects
of cognitive motor intervention on gait and balance function in Parkinsons disease. Compared
with previous reviews, the present systematic
review and meta-analysis only included subjects
with Parkinsons disease for all articles. Most of
the included studies were newly published.
Moreover, we performed a meta-analysis of the
effects of cognitive motor intervention between
pre- and post-intervention of patients with
Parkinsons disease. We conducted a wide range of
electronic search for the systematic review.29. No
restrictions were placed on language or publication date. Study selection, data extraction, and
quality evaluation were independently performed
by two authors to minimize transcription errors
and bias. In view of the abovementioned points,
the results of our meta-analysis are considered
extremely robust.
However, several limitations were found in our
review. First, high-quality studies remained inadequate despite our efforts to cover most of the studies
within the last three years in our review. Four RCTs
and five single-group interventional studies were
found. According to their PEDro score, all of the

142

Clinical Rehabilitation 30(2)

Figure 3. Meta-analyses of cognitive motor intervention on balance function. A: Unified Parkinsons Disease Rating
Scale (UPDRS), B: Center of pressure (COP) sway, C: Berg balance scale (BBS) and D: Unipedal Stance Test (UST).
95% CI=95% confidence intervals. CMI: cognitive motor intervention.
*represents the performance under dual task test condition. # represents the performance under eye close.

143

Wang et al.
RCTs were of moderate quality. Only one study conducted concealed allocation and intention-to-treat
analyses. All studies failed to blind the subjects and
therapists. Three studies attempted to blind assessors. Second, only a limited number of comparisons
(one to three) were made in the systematic review
with regard to the effect of cognitive motor intervention on the following outcomes: cadence, Unified
Parkinsons Disease Rating Scale, Berg Balance
Scale, Four Square Step Test, Dynamic Gait Index,
Sit-to-Stand test, Timed Up and Go test, Tinetti
Performance Oriented Mobility Assessment, 10 m
walk test, and Community Balance and Mobility
assessment. In fact, the number of articles may be
too small to discover the differences between preand post-intervention on these outcomes.
Furthermore, the total number of subjects was small
for the systematic review. Slight differences between
pre and post-intervention were also difficult to estimate. Third, we intended to perform the meta-analysis on long-term gait and balance. However, most of
the articles reported short follow-up periods and
involved short intervention durations.
Overall, our systematic review lacked highquality articles. The methodological standards
must be improved in future studies to reduce possible biases. We should improve the following
standards: conduct random allocation and concealed allocation; attempt to blind assessors,
therapists, and subjects; perform intention-totreat analysis; and employ adequate follow-up
period. Moreover, studies should be registered to
reduce bias and should be conducted in accordance with the standards of clinical trials (e.g.,
the Consolidated Standards of Reporting Trials
statement).30
As previously mentioned, most of the studies in
this systematic review had small sample size. Thus,
additional large-scale RCTs should be performed
to evaluate the effect of cognitive motor intervention. To estimate the duration for any improvement
outcome to be sustained for cognitive motor intervention, future studies should have follow-up sessions with longer durations. In addition, different
training programs for cognitive motor intervention
can be used, which may lead to different results.
Therefore, a systematic review and meta-analysis

of different cognitive motor interventions should

be conducted to determine the optimal intervention
program for patients with Parkinsons disease.
The results of our systematic review and metaanalysis show that cognitive motor intervention can
significantly improve the following outcomes: gait
speed, stride time, Unified Parkinsons Disease Rating
Scale, center of pressure sway, Berg Balance Scale,
Unipedal Stance Test, Four Square Step Test, Dynamic
Gait Index, Sit-to-Stand test, Timed Up and Go test,
Tinetti Performance Oriented Mobility Assessment,
10 m walk test, and Community Balance and Mobility
assessment. Therefore, our review results should be
useful for patients with Parkinsons disease, healthcare decision makers, and medical staff.
Clinical messages
Cognitive motor intervention is effective
for gait and balance function in Parkinsons
disease.
In the future, it is necessary to have more
high quality RCTs to confirm these
results.
Acknowledgements
We would like to thank Prof Chetwyn Chan for his
advice.

Conflict of interest
The authors declare that there is no conflict of interest.

Funding
This study was supported by the Key Laboratory of
Exercise and Health Sciences (Shanghai University
of Sport), Ministry of Education, Shanghai University of
Sport; Ministry of Education, the First-class Disciplines
of Shanghai Colleges and Universities (Psychology);
Shanghai Committee of Science and Technology
(14490503800); Shanghai Youth Science and Technology
Sail Project (15YF1411400).

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