HUMAN MOVEMENT
2018; 19(1): 57– 63
DUAL-TASK EXERCISE AS A THERAPY FOR EXECUTIVE
MOTOR FUNCTION IN PARKINSON’S DISEASE
original paper
DoI: https://doi.org/10.5114/hm.2018.73613
© University school of Physical Education in Wrocław
GILMARA GOMES DE ASSIS1, TATIANE ALVES DA SILVA2,
PAULO MOREIRA SILVA DANTAS2
1
2
Physiology Department, Federal University of Rio Grande do Norte, Natal, Brazil
Physical Education Department, Federal University of Rio Grande do Norte, Natal, Brazil
ABstRAct
Purpose. to evaluate the effects of aerobic exercise with dual-task on the motor function in patients with Parkinson’s
disease.
Methods. clinically evaluated by the Unified Parkinson’s Disease Rating scale – III and the senior Fitness test battery,
20 patients with Parkinson’s disease were randomly divided into a control and an experimental group, with the latter
performing a 4-week program of water-walking in a deep pool while executing dual-tasks. Evaluations were made before
and after 4 weeks in both groups.
Results. Patients with Parkinson’s disease revealed significant improvements in pre-/post-exercise motor function, with
a moderate effect (p < 0.001; d = 0.44). Bradykinesia (p < 0.001) and agility (p < 0.001) exhibited significant changes individually.
Conclusions. Regular exercise combined with executive challenge such as dual-task may counteract the advanced motor
symptoms of Parkinson’s disease neurodegeneration.
Key words: dual-task exercise, aerobic exercise, executive function, motor control, Parkinson’s disease
Introduction
Parkinson’s disease (PD) is a neurodegenerative disorder that affects 10–14 new individuals per 100,000
people a year in the world, according to WHo. Usually manifested after the 5th decade of a life, PD is
primarily expressed by the motor symptoms of hypokinesia (partial loss of muscle movements), bradykinesia (slowness of movements), rigidity, and resting
tremor [1]. such movement disorders rise as a consequence of a progressive neuronal loss in sub-thalamic nuclei, importantly involved in the central control
of voluntary movement [2]. the disease’s severity is
described in stages of advance that represent the degree of motor impairment, with special attention to
patient’s balance, speed of movements and gait [1]. clinically, the patients can be assessed within 5 stages of
motor impairment, as recommended by the Movement
Figure 1. Hoehn and Yahr recommended scale for
Parkinson’s disease staging [16]
Disorders society – Hoehn and Yahr stating scale
(Figure 1).
PD slowly evolves in time, with the lesions in the central nervous system initiating quite before the first symptoms, which makes it possible to take decades for the
disease to be fully visible and reveal the whole symp-
Correspondence address: Gilmara Gomes De Assis, Federal University of Rio Grande do Norte, center of Health science,
Physiology Department, Avenida senador salgado Filho, 3000 – Lagoa Nova, Natal – RN, 59064-741, Brazil,
e-mail: garotagomes@gmail.com
Received: september 20, 2017
Acepted for publication: November 24, 2017
Citation: De Assis GG, Da silva tA, Dantas PMA. Dual-task exercise as a therapy for executive motor function in Parkinson’s disease. Hum Mov. 2018;19(1):57–63; doi: https://doi.org/10.5114/hm.2018.73613.
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tomatic picture. the disease course starts from intraneuronal lesions, continually progressing in severity
throughout the encephalon, in predictable patterns
[3, 4]. Patients with PD may live long periods with the
disease and supposedly have had it in a ‘blind’ phase
for even more time than after diagnosis [5].
currently, PD treatment focuses on the recovery
of the dopaminergic transmission depletion caused
by the loss of dopamine-deliver neuronal tissue, but
the drug efficacy is not fully satisfying and may lead the
patient to accumulation of new motor disturbances
as a side effect [6]. therefore, the search for new opportunities to improve the patients’ status or to reduce their
symptoms is an actual challenge.
Voluntary movements require a more advanced
strategy of executive control than externally generated
stimuli, involving integrated cognitive functions [7].
therefore, cognitive-motor interference based therapies, referred to as dual-task (Dt) ones – when two tasks
are performed and simultaneously interact within primary motor cortex – have been well required for patients
with motor impairment. such methodology has shown
to provoke significant adaptive changes in the executive processing of patients with PD [8]. For instance,
great costs of cognition have been evidenced in individuals with PD while performing Dt whereas their
inefficiency to walk during a Dt was associated with
losses in specific domains of executive functions [9].
Exercising, instead, physiologically impacts on the
metabolic profile of individuals with and without disease, thus improving the trophic support necessary for
neuroplasticity [10], as it has been observed in brain
areas specifically related to the executive function
[11, 12]. Moreover, a symptomatic relief pronounced
by exercise in individuals with PD is attributed to an
enhance of dopaminergic transmission in the same
circuitry as those assessed by medication [13]. Additionally, Dt strategies have also been successfully approached in people with PD in order to recover functional capacities [14].
As current pharmacological and surgical approaches
are poorly effective in the control of motor symptoms
in PD [15], the appropriate exercise would potentially
suit as a complementary therapy for the recovery and
preservation of the patients’ motor functions, even for
those in advanced stages of the disease. In this study,
patients with PD were submitted to a water-walking
Dt exercise program in order to check the effect of
a 4-week program on their executive motor function.
58
Material and methods
Participants
the total of 20 patients with PD (stages 2–3 on the
Hoehn and Yahr scale), aged 59–73 years, with a medical permission to exercise were recruited from the
Neurology Department of University Hospital onofre
Lopes at the Rio Grande do Norte state, Brazil. the
subjects were randomly divided into equal groups
(10 individuals each). the experimental group (EG)
was enrolled in a 4-week aerobic exercise program with
30-min sessions of water-walking with Dt, while the
control group (cG) remained in a sedentary routine
during the same period. the exclusion criteria involved
inability to walk independently, as well as lack of completion of at least 85% of the exercise program.
Assessment procedures
the subjects were briefed on the procedures and
objectives of the exercise program, and completed demographic and psychometric questionnaires referring
to executive function and fitness evaluations. All tests
were conducted in phase oN of medication, that is between 20 and 40 min after the latest dose of levodopa.
the executive function and fitness evaluations comprised the Unified Parkinson’s Disease Rating scale
(UPDRs), part III, which incorporates elements from
the existing motor control scales compiled into one [16];
and the senior Fitness test (sFt), referring to a nonlaboratory battery of tasks used to assess the physical
valences of strength and agility [17]. All the physical
tests were applied 4 days both before and after the
exercising period.
Water-walking program
the EG underwent a 2-week adaptation phase in
a 120-cm deep pool, 25/12.5 m sidelong, with the
water controlled for pH and chlorine, and of natural
temperature (28–32°). the subjects had to wear a colet
Power EVA floater for safety. Heart rate (HR) and blood
pressure (BP) were recorded before and after all sessions.
the adaptive phase consisted of 3 goals: (1) to walk
along the entire width (12 m) of the pool without any
help; (2) to walk all the length (25 m) of the pool without help; (3) to walk along the four corners of the pool
without help. these stages could require more than
1 session. During this phase, Borg scale of perceived exertion was introduced for subjective control of intensity.
In the exercising phase, the subjects had a 10-min
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warm-up (free water-walking), then they were positioned at the longitudinal side of the pool (12.5 m) and,
at the evaluator’s signal, they started walking along
the length of the pool (25 m) as fast as possible, from one
side to another, during 30 min. to stimulate speed during the walk, they were given the mission of carrying
the biggest number of ‘flags’ from one side of the pool
to the other. In addition to this walking, one motor
task – meaning new movements to be executed either
with the arms or legs, or the whole body – was requested
from the subjects at the frequency of 1/min, summing
up to 15 different motor tasks plus 15 min of free water-walking each session. Data from Borg scale were
collected every 10 min per session. All the sessions
were terminated with 10 min of cooling down and
stretching exercises. the motor tasks added to the water-walking were previously tested and recorded, and
then executed in a systematic sequence.
statistical analysis
Normality and homogeneity of variances were verified by the shapiro-Wilk and Levene’s tests, respectively.
Parametric variable data are presented as mean and
standard deviation, and nonparametric data as median and interquartile range. Data from the sFt were
normalized by logarithmic transformation. the independent t-test was used to compare parametric variables, and the Mann-Whitney U-test for non-parametric
analysis. ANoVA split-plot (2 × 2) with Bonferroni’s
post hoc were applied for inter- and intragroup comparison of all dependent variables. size effect was calculated by partial eta squared ( 2p) to indicate the
proportion of variance in the dependent variable explained by the independent variable, and cohen’s d.
the statistical procedures were carried out with the
sPss 22.0 software (statistical Package for social sciences, chicago, UsA). the significance level was set
at p < 0.05 for all tests.
Ethical approval
the research related to human use has been complied with all the relevant national regulations and
institutional policies, has followed the tenets of the
Declaration of Helsinki, and has been approved by
the authors’ institutional review board or an equivalent committee.
this study, registered as U1111-1191-0247, has been
approved by the Institutional Human Research Ethics
committee in accordance with Resolution No. 466/2012
of the Brazilian National Health council and the code
of Ethics of the World Medical Association’s Declaration of Helsinki – N.°46205815.1.0000.5537.
Informed consent
Informed consent has been obtained from all individuals included in this study.
Results
After excluding the patients who did not accomplish at least 85% of the program, the final number of
subjects in the EG was 7. the general data for both
groups are shown in table 1. No significant difference
was observed for the perceived effort between sessions (Borg scale).
Repeated measures ANoVA presented a significant time effect for systolic (p = 0.04) and diastolic (p =
0.02) BP with an effect revealed for the EG (d = 0.36).
A significant time × group interaction (F(1, 10) = 33.75,
p < 0.001, 2p = 0.771) was shown with a significant
time effect (F(1, 10) = 61.12, p < 0.001, 2p = 0.859)
for UPDRs III. the post hoc Bonferroni test revealed
a significant difference in executive motor functions
between the pre- and post-intervention only for the EG
(p < 0.001, d = 0.44) (Figure 2). the most relevant differences observed among items of UPDRs III observed
at the pre- and post-exercise assessment occurred for
bradykinesia (p < 0.001), lower limb agility (p < 0.001),
and postural stability (p < 0.05).
For the stF (Figure 3), repeated measures ANoVA showed no significant time × group interaction
(F(1, 10) = 1.81, p = 0.209, 2p = 0.153), as well as no
effect of time (F(1, 10) = 1.81, p = 0.209, 2p = 0.153)
for the lower limbs strength (Figure 3A). For the upper
limbs strength, there was no time × group interaction
(F(1, 10) = 3.51, p = 0.090, 2p = 0.260) but there was
table 1. characteristics of the control group
and experimental group. Data are presented as means
and SD for parametric, and median and interquartile
range for non-parametric analyses
control
group
(n = 10)
sex (male/female)
Age (years)
stature (m)
Body mass (kg)
BMI (kg/m2)
tD (years)
Hoehn and Yarh (score)*
MocA (score)
8/2
66.4 ± 6.1
1.67 ± 0.06
64.5 ± 5.4
23.0 ± 1.0
10.8 ± 5.9
3.0 ± 0.8
20.4 ± 1.7
Experimental
group
p value
(n = 7)
5/2
65.0 ± 5.4
1.62 ± 0.10
65.6 ± 13.1
25.0 ± 3.1
12.3 ± 6.2
3.0 ± 1.0
21.1 ± 5.3
0.684
0.287
0.861
0.202
0.685
0.558
0.770
BMI – body mass index, tD – time since diagnosis,
Hoehn and Yarh – disease severity scale of Hoehn
and Yarh, MocA – Montreal cognitive assessment
* non-parametric variable
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CG – control group, EG – experimental group,
UPDRS III – Unified Parkinson’s Disease Rating Scale, part II
Figure 2. the effects of 4 weeks of aerobic exercise
with cognitive interference on the motor function
of patients with PD. control group: n = 5, experimental
group: n = 7, UPDRs III: clinician-scored monitored
motor evaluation scale
a significant effect of time (F(1, 10) = 6.27, p = 0.031,
2
p = 0.385). the post hoc Bonferroni test revealed
a significant difference between the pre- and post-intervention status only for EG (p = 0.007, d = –1.17)
(Figure 3B). similar to the lower limbs, the variable of
agility / dynamic balance did not show time × group
interaction (F(1, 10) = 0.01, p = 0.928, 2p = 0.001) or an
effect of time (F(1, 10) = 0.41, p = 0.535, 2p = 0.040)
(Figure 3c).
Discussion
Regular exercise evokes changes in many levels of
a human organism that ultimately display in the individuals profile; so it was observed in individuals’
BP after exercising. the positive change found in the
resting levels of BP of the patients submitted to exercise is attributed to an improvement in their fitness
conditions as an adaptive exercise response required
for the production of energy with a smaller load of heart
function [18]. the water-walking showed to be as effective as a solo walking when it refers to the motor
function and balance gains. the aerobic exercise combined with a cognitive stimulation effectively evoked
positive changes in the clinical parameters of motor
function in the subjects with advanced symptoms of PD.
Furthermore, although the self-selected speed and the
water resistance featured by this model of exercise may
have represented a limitation in the gains of strength,
they did show to be of a great advantage for the activation of the processes of central control of the motor
action provided by the incremental tasks [19].
60
CG – control group, EG – experimental group, RF MMII – lower limb strength, RF
MMSS – upper limb strength, Agil/ED – agility/dynamics
Figure 3. Effect of 4 weeks of aerobic exercise
with cognitive interference on lower (A) and upper (B)
limb strength, and agility / dynamic balance (c)
of patients with moderate Parkinson’s disease.
control group: n = 5, experimental group: n = 7
the usage of Dt approaches to improve the motor
function of patients with PD has been explored for a few
decades. A motor-cognitive interference that occurs
in the brain owing to an overlap of tasks generated by
such a technique is revealed to yield a positive impact
on the specific spatiotemporal domains of velocity
and step planning, as well as on domains of balance
and cognition. therefore, Dt challenges may evoke important changes in patients with PD at executive levels
[20]. For instance, the participants’ gait has been no-
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ticed to improve in balance, with the risk of fall decreasing in number [21].
Water-based aerobic exercise has already shown to
be effective for the improvement of functional mobility in patients with PD in the earliest stages [22]. In
the present study, it has been demonstrated that patients at a more advanced stage of disability can execute an exercise training program, thus being able to
yield gains in the executive motor function and the
strength levels. the aquatic environment designed for
the exercise provided an indispensable scope for the
accomplishment of the aerobic training combined with
cognitive stimulation, in a way that is suitable for the
effective practice in individuals at elevated levels of
motor disability. After the exercise, a positive change
was detected in the clinical profile of the patients’ motor function, as expressed by a battery of motor tasks
evaluated by a neurologist (UPDRs III), and also in the
parameters of fitness conditions as strength and BP.
our results indicate that the exercise benefits related to the executive control of the patients must have
been potentiated by the increment of Dt. Further,
gains of strength can indeed be pronounced by patients in severe stages of PD, although a limited number
of studies have addressed exercise to this population,
to whom alternative therapies are of a greater importance.
considered as the major contributor for the motor
disability faced by patients with PD, bradykinesia was
the most responsive symptom affected by the exercise
program. this likely occurred owing to an exerciseinduced increase in muscle activity that triggers a series
of cellular and molecular processes which ultimately
elevate the oxidative and excitatory neuromuscular
capability. these changes may counteract the compensatory mechanisms of cortical developed hyperconnectivity in patients with PD in stages of sub-thalamic
nuclei degeneration that impedes proper movement
[23]. Additionally, the exercise-related increases in
epinephrine and norepinephrine raise these neurotransmitters supply and uptake by the central nervous
system, positively impacting on the sub-thalamic circuits of neurotransmission and so the effectiveness
of rapid movement [24].
Aerobic exercise has been shown to play an important role in neuroplasticity. Interestingly, the exercise
can induce adaptive neurophysiological responses as
much as the coordination stimulus can induce changes
in the information processing with respect of energy
expenditure and cognitive demands, where the latter
is more crucial for potentiation of molecular and cel-
lular processes involved in neuroplasticity [25]. the
water-walking with Dt proposed in this study is thus
suggested to improve motor performance in PD by
the incorporation of goal-based motor skills learning
to an automatic exercise, enhancing the cognitive engagement. combining goal-based tasks with aerobic
training may have increased the exercise effect, thus
becoming possible to reach the executive motor control improvement not only to the walking skill itself, but
also in a wider spectrum of motor functions as measured by UPDRs III [26].
Whereas exercise effects on executive function in
PD has previously been associated with the exercise
frequency and volume [2], in our study, the increment
of Dt during aerobic stimulation is believed to be the
crucial factor for the achievement of such executive
gains in a relatively shorter period comparing with
programs supplying only exercise, even to less compromised individuals [27, 28].
the water-walking with Dt enabled the participants with a strong motor disadvantage to restore
a range of movements hitherto compromised by the
severity of the disease. the amplified repertory of movement provided by the Dt and made especially possible by the aquatic environment was essential for the
motor gains, with the advantage of the exercise adaptations, as blood perfusion in central areas, oxygen
delivery, and neurotrophic transport, which are necessary for the support of neuronal circuits.
Conclusions
Aerobic exercise with Dt is effective to improve general motor function and fitness conditions in patients
with PD even on severe stages of disease in a short
period of time.
Limitations
the access to individuals with movement disorders
makes administration of long-term exercise protocols
a challenge. side effects of supplementary medication may occur during the process as a confusing bias.
Disclosure statement
No author has any financial interest or received any
financial benefit from this research.
Conflict of interest
the authors state no conflict of interest.
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