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Official Title of Study: -
INFLUENCE OF AEROBIC EXERCISE ON
INHIBITORY CONTROL OF EXCUTIVE
FUNCTION IN SPASTIC HEMIPLEGIC
CEREBRAL PALSY: A Randomized
Controlled Trail
Document Date: - 01/08/2019.
Human Subjects protection review board
approval date: - 31/03/2019
INFLUENCE OF AEROBIC EXERCISE ON INHIBITORY CONTROL
OF EXCUTIVE FUNCTION IN SPASTIC HEMIPLEGIC CEREBRAL
PALSY: A Randomized Controlled Trail
Abstract
Background: Inhibitory control of executive functions (EF) is one of the main specific
cognitive impairments that affect children with cerebral palsy, cognitive skills begin
to develop in infancy and continuing through the pre-school years, childhood and into
adolescence it changes across the lifespan of an individual and has great effect on
their participation and quality of life. Aim: The aim of study was to assess the
influence of aerobic exercise on inhibitory control of executive functions in spastic
hemiplegic cerebral palsy. Methods: Sixty children with spastic hemiplegic cerebral
palsywere enrolled in this studyand were assessed for eligibility. Their aged ranged
fromseven and eleven years. They were assignedrandomly into twoequal
groups.Group (A) the study group received aerobic exercise in addition to selected
physical therapy program. And group (B) the control group received the same
selected physical therapy program only. The treatment was conducted for one hour,
three times / weak for three successful months. Eriksen flanker test and StroopColor-
Word test were used to assess inhibitory control of EF pre and post treatment.
Results:Post treatment there was significant increase in accuracy inEriksen flanker
test and StroopColor-Word test and decrease in reaction time ( congurant and
incongurant)only in study group, P< 0.05. Conclusion:Aerobic exercise has
significant effect on inhibitory control of executive functions in spastic hemiplegic
cerebral palsy. Key words: Hemiplegic cerebral palsy,inhibitory control of executive
functions and aerobic exercise.
Introduction:
Cerebral palsy (CP) isa group of permanent disorders of the development
of movement and posturecausing activity limitation. It is the most
common cause of physical disability that attributed to non-progressive
neurological condition that occur in the developing fetal or infant brain.[1]
Motor impairment has frequently been associated with secondary
disturbances as communication,sensation, perception, behavior and
cognition, as well as the presence of epilepsy, disequilibrium[2], and
secondary musculoskeletalproblems[3].Hemiplegic CP is a subtype in
which one side of the body is involved. It affects about 1 in 1,300 live
births[4].It is characterized by a clinical pattern of unilateral motor
impairment[5]. The severity of motor impairment varies widely,
dependingon the site and severity of brain lesion[6, 7].Early brain injury
impacts concomitantly on motor, function and cognitive
development[8].Cognitive ability is a mental process of acquiring
knowledge and understanding through acquired knowledge and
experience[9].
Executive function (EF) constitutes a set of cognitive processes
that comprise distinct yet highly interrelated components such as
cognitive flexibility, inhibitory control, and working memory [10].Because
EF is involved in the regulation of both thought and action, the behavioral
manifestations of EF can be assessed [11], including difficulty switching
between tasks, difficulty initiating new nonroutine actions, and a lack of
impulse control [12].EF have received considerable interest and are strong
predictors of children`s early school success and it includes intentional
shifting/flexibility, working memory, and inhibitory control[13].
Inhibitory control referred to as response inhibition, is one of the
separable cognitive processes thought to comprise the construct of
executive function. In the past, inhibitory control was thought to emerge
only in middle to late childhood, corresponding with improvements in the
child’s ability to execute complex, higher-order integrative tasks [14].
Aerobic exercise refers to exercise that involves or improves
oxygen consumption by the body. It is the type of activity that uses large
muscle groups. Its performance is in a continuous and rhythmic way with
a main goal to make the heart and lungs work harder than they do when
the person at rest [15].Aerobic exercise produces vascular changes,
including an increase in oxygen saturation, promotes angiogenesis, and
increases cerebral blood flow (CBF) in areas related to cognitive function
[16]. Aerobic exercise training improves cerebral perfusion[17]and
metabolism [18], resulting in the reduction in Aβ load [19], up-regulation of
neurotrophins[18], and hippocampal neurogenesis and volume [20].
Exercise increases serum calcium levels, which can then be transported to
the brain to activate the rate limiting enzyme for catecholamine
(dopamine and norepinephrine) synthesis. Both norepinephrine and
dopamine are neurotransmitters [21].Aerobic exercise is an efficient
strategy to positively influence executive control during [22].and after
exercise [23].
Subjects and methods:
A pretest-posttest randomized controlled study was conducted in
outpatient clinic in faculty of physical therapy, Cairo university. Informed
consent was provided for each child from their parents. The procedures
followed were in accordance with the Institutional Ethical Committee
Clearance No:P.T.REC/012/002278
Subjects:Sixty children with spastic hemiplegic cerebral palsy were
enrolled in this study and were assessed for eligibility. Their aged ranged
from seven and eleven years, they were from both sexes, they have left
side hemiplegic cerebral palsy and they were able to walk independently.
We excluded children with visual or auditory problems,children with
history of drug intake that may affect the cognitive function, medically
unstable children especially with cardiovascular disorders and
uncooperative children.
They were assigned randomly into two equal groups. Group (A) the study
group received aerobic exercise in addition to selected physical therapy
program. And group (B) the control group received the same selected
physical therapy program only. The treatment was conducted one hour,
three times / weak for three successful months.
Materials for evaluation:
Eriksen Flanker test and Stroop Color-Word test were used to assess
inhibitory control of EF pre and after treatment.
1) Eriksen Flanker Test: Modified Eriksen Flanker task that has
been widely employed to examine the inhibitory aspect of
executive function [24]. The Flanker task consisted of 20 trials
consisted of two trial types, with either congruent reaction time
(CRT) or incongruent reaction time (iCRT) to certain visual
stimuli. The congruent trial was a horizontally arranged array of
arrows presented in the same direction. The incongruent trial had a
similar array of arrows, but the middle arrow, the target, was
displayed in the opposite direction. Participants were asked to
respond to the direction of the target arrow within the array of
arrows by pressing the corresponding right or left finger button as
quickly and accurately as possible. The accuracy percentage and
reaction times of correct responses on both congruent and
incongruent trials were identified as metrics of behavioral
cognitive performance.
2) Stroop Color-Word Test:One measure of executive function is
the color word Stroop Test, originally developed in 1935 by Stroop
to measure selective attention and cognitive flexibility. It is most
often described as measuring the individual’s ability to shift
cognitive set [25]; it is believed to provide a measure of cognitive
inhibition[26], or the ability to inhibit an over learned (i.e., dominant
response) in favor of an unusual one [25]. The Color–Word task on
which the individual is shown the names of colors printed in
conflicting ink colors(e.g., the word “blue” in red ink) and the
participants were asked to respond to is asked to name the color of
the ink rather than the word by pressing the corresponding first
letter of the color if red press(r) button if yellow press (y)button if
orang press (o) button if purple press (p)button if green press
(g)button if blue press (b) button as quickly and accurately as
possible [27].The Strooptest consisted of 20 trials consisted of two
trial types,with either normal congruent reaction time (CRT) or
incongruent reaction time (iCRT) to certain visual. The normal
trial was when color of the ink is the same color of the word and
The interfere trial the color of the ink not the same as the color of
word . The accuracy percentage and reaction times of correct
responses on both congruent and incongruent trials were identified
as metrics of behavioral cognitive performance.
Flow chart
Fig 1, flow chart
Assessed for
eligibility (n= 66)
Randomized
(n=60)
Allocation
Allocated to intervention (n=30)
reasons) (n= 0 )
Allocated to intervention (n=30)
Did not receive allocated intervention (give reasons) (n=0 )
Excluded (n=6)
(n=3)
Analysis
Analysis
Analysed (n=30)
Excluded from analysis
(n=0)
Analysed (n=30)
Excluded from analysis
(n=0)
Methods of Treatment Group (A) which is the study group received 20 min. selectedphysical
therapy program which contain strengthening exercises for upper limb
and lower limb muscles, stretching exercises for elbow extensors, hand
supinator, wrist extensors, knee extensors and ankle dorsiflexors,
balancing exercises, coordination exercises and gait training exercises in
open environment. In addition toaerobic exercise on a bicycleergometer
for 40 min. Bicycle ergometer (Monark Rehab trainer model 88E) was
used to train children in study group. It is a stationary bicycle with an
ergometer (electronically braked) to measure the work done by the
exerciser. It is equipped with an electronic meter showing pedal
revolutions per minute, total pedal revolutions and time function. It
provides low-impact, safe, and effective cardiovascular exercise. This
low-impact movement does not put much stress on joints.
Before starting the training procedure each child was instructed to wear
comfortable training suit and shoes and to sit vertically on the bicycle
ergometer seat with erect back. Extra strap was placed on child's feet to
provide complete fixation on ergometer pedal. The exercise on bicycle
was done under supervision of researcher to ensure correct and accurate
application.
In the first week, children bicycled to tolerance at 40% to 50% max HR,
and then progressed to the 70% max HR in the second week. Intensity of
aerobic exercise was systematically progressed for each child by
increasing resistance to maintain conditioning at 70% of max HR.
maximum HR calculated from the following equation: max HR=220-age
[28].The first five minutes of each session were dedicated to warmingup
exercise on the bicycle in the form of slow progression exercise (to
decrease the risk of musculoskeletal injury and cardiovascular
complications), followed by the active phase of exercise for 30 min., and
finally cooling down phase for five min. with intensity and speed
decreased gradually until reaching the resting heart rate (RHR) [29].
Group (B): which is the control group received the same selected physical
therapy program only for one hour.The treatment was conducted one
hour, three times / weak for three successful months.
Statistical analysis
For analysis of data in the present study, SPSS software version 21 was
used for data analysis. Descriptive statistics was used to identify the mean
and standard deviation for each variable. Paired t-test was used to test pre
and post changes in each group of the study.
Results:
The mean values of age and grade in study group (A) were 9.77±1.135
and 4.77±1.135 respectively and in control group (B) were9.2±1.243 and
4.2±1.243respectively.There was no significant difference between the
two groups in theirmean values of ages and grades (P > 0.05).
In the study group (A) the number of boys was 21 (70%) and the number
of girls was 9 (30%), while in the control group (B) the number of boys
was 17 (56.7%)and the number of girls was 13 (43.3%)there was no
significant difference between the two groupsingender distribution.
There was no significant difference in pre treatment values Flanker test
accuracy,CRT and iCRTand stroop test accuracy,CRT and iCRTbetween
two groups P > 0.05. While there was significant difference in post
treatment values Flanker test accuracy,CRT and iCRT and stroop test
accuracy,CRT and iCRTbetween two groups P<0.05in favor of the study
group(A).
The mean values of the Flanker test accuracy,CRT and iCRT post
treatment in study group (A) were 90± 10.91, 1161± 291.7and 1417±
588.1respectively, andin control group (B) were 82± 10.88, 1489±
509and 1792± 755.7 respectively. Comparison of the mean value of each
test in study group (A) with the corresponding mean value in control
group (B) revealed significant difference of all variables (p< 0.05) in
favor of study group (A).
The mean values of the Stroop test accuracy,CRT and iCRT post
treatment in study group (A) were 83.5± 11.15, 2240± 947.7and 2647±
729.9respectively, and in control group (B) were 75.67± 12.37, 2752±
911.1and 2990± 558.4 respectively. Comparison of the mean value of
each test in study group(A)with the corresponding mean value in control
group revealed significant difference of all variables (p< 0.05) in favor of
study group (A).
There was a significant increasein post treatment valuesof Flanker test
accuracy 16.17 and stroop test accuracy 13.33 while P-value was 0.0001
and the percentage of improvement was 21.9% and 18.9% respectively.
While there was a significant decrease in post treatment values of
Flanker test CRT 406, iCRT410and the percentage of improvement was
25.91% and 22.44% respectivelyand also there was a significant decrease
in post treatment values of stroop test CRT 741 iCRT 360 and the
percentage of improvement was 24.88% and 11.97% respectively while
P-value was 0.0001.
Variable
Study Group (A) Control Group (B)
Pre
treatme
nt
Post
treatm
ent
Difference
(% change)
t-value
P-value
Pre
treatme
nt
Post
treatm
ent
Difference
(% change)
t-value
P-value
Mean±S
D Mean±S
D Mean±S
D Mean±S
D
Flanker
test
accuracy
73.83±
10.4
90±
10.91
16.17
(21%)
12.8
2
0.0001
**
78.5±
11.9
82±
10.88
3.5
(4.46%)
1.966 0.0589
Flanker
test
CRT
1567±
369.2
1161±
291.7
406
(25.91%) 6.13
8
0.0001
***
1588±
438.6
1489±
509
99
(6.23%) 1.741 0.0923
Flanker
test
iCRT
1827±
779.6
1417±
588.1
410
(22.44%) 2.74
0.0104
*
1847±
787.6
1792±
755.7
55
(2.98%)
0.506
4 0.6164
Stroop
test
accuracy
70.17±
8.758
83.5±
11.15 13.33
(18.9%)
7.10
2
0.0001
**
73.17±
9.048
75.67±
12.37 2.5
(3.42%)
1.525 0.1380
Stroop
test
CRT
2982±
992
2240±
947.7
741
(24.88%) 4.96
9
0.0001
***
2923±
895.5
2752±
911.1
171
(5.85%) 1.36 0.1842
Strooptes
t Icrt 3007±
885.1
2647±
729.9
360
(11.97%)
2.74
9
0.0102
*
3118±
746.3
2990±
558.4
128
(4.1%)
1.257 0.2187
Non-significant: p< 0.05*Significant: p>0.05
Discussion:
This study was conducted to assess the influence of aerobic exercise on
inhibitory control of EFin spastic hemiplegic cerebral palsy. The children
that was selected in this study have left side hemiplegic cerebral palsy
that agreed withGodefroy&Bogousslausky 2007[30]who concluded that
damage in right hemisphere, hemi-spatial neglect is the most frequent
deficit where there is impaired or lost ability to react to or to process
sensory stimuli in the hemispace opposite to the lesion side. This
visuospatial perceptual deficits can affect different cognitive activities
which show up as difficulty copying designs, making constructions,
discriminating pattern of faces , selecting the correct sleeve and self-
monitoring left side or covering the paretic shoulder.
In the current study, selection of hemiplegic cerebral palsied
children comes in agreement withBodimeade et al.[31]who concluded that
although disruptions in motor functioning are often the most recognizable
feature of CP, executive function impairment is also a central feature of
CP when compared EF in children with CP (mean age 11 y/o) to typically
developing controls.
The choice of using a bicycle ergometer for aerobic exercise
training instead of a treadmill was because safety was our foremost
concern for the participants. The bicycles were powered by participants
and easy for them to get on and off, which reduced fall risk, a prevalent
problem in the study population
The present study was revealed significant improvement of all
measured variables of inhibitory control of EF after three successful
months that agreed withRenaud, et al. 2010[32] who observed that only 3
months of well-structured and supervised exercise is associated with a
significant improvement in attention and executive functions.
The results of the present study revealed significant improvement
of all measured variables in study group (A)as there wassignificant
increase in accuracy and decrease reaction time congurant and
incongurantthat mean improvement of inhibitory control of EFthis was
attributed to aerobic exercise.
The results of the present study proved that there was no significant
improvement in all measured variables of Flanker test accuracy,CRT and
iCRTin the control group (B), while there was significant improvement in
all measured variables of Flanker test accuracy,CRT and iCRTin the
control group (A). This improvement may be attributed to the
physiological effect of aerobic exercise on brain as it increases the
cerebral tissue oxygenation, blood flow velocity and cerebral metabolism
and homeostasis which in turn improve the speed of information
processing, motor learning, implicit memory and executive function. This
result agreed with McAuley et al., 2004[33], Kluding et al., 2011[34],
Barbara et al., 2009[35] and Rand et al., 2010[36]. Improvement in
cognitive flexibility was proportional to the degree of exercise Masley et
al., 2009[37].
The improvement of EF afteraerobic exercises may be due to
increases activity in cortical areas associated with cognition, including the
right medial frontal gyrus (BA 46), superior frontal gyrus (BA 8), and
superior parietal lobe (BA 40). It increases the number of
interconnections (synapses) in frontal and parietal gray matter, allowing
for greater systematic recruitment of these areas under higher cognitive
load and also increases prefrontal and anterior cingulate plasticity in the
aging brain to a level more consistent with neurologically intact young
adults This results agreed with(Colcombe and Kramer, 2004).[38].
The results of this study showed that there was significant changes
in all measured variables Stroop test accuracy, CRT and iCRTwhen
comparing pre and post treatment variables between two groups in favor
of the study group (A) this improvement comes in agreement with Pottet
al., (1996) [39], and Ainslie et al., (2008)[40] who reported that aerobic
exercise increases oxygen consumption, reduces blood pressure and
resting heart rate, strengths and enlarges the heart muscle which reflects
on its pumping efficiency leading to increase in global ®ional cerebral
blood flow. Plus aerobic exercise was proved to promote angiogenesis
and increase in capillary density.
Gapin et al., 2011[41]also supports the beneficial effects of
physical activity on EF and suggests that effects might be particularly
large for children.
Most studies supported greater improvements of EFafter
moderateto vigorous aerobic exercise in typically developing (TD)
children (Crova et al., 2014[42]; Diamondand Lee, 2011[43]; Verburgh
et al., 2014)[44].
The improvements of EF after sustainedaerobic exercises is (over
months) is required for cognitive improvement this comes in agreement
with Masley2009.[37].
Previous studies have reported improved performance on a variety
of cognitive task categories, including attention, information processing,
memory, and executive function, after a single bout of aerobic exercise
(Audiffren, Tomporowski, &Zagrodnik, 2008[45]; Coles
&Tomporowski,2008[46]; Hillman et al.,2009[47].
The significant improvementin post treatment Stroop test accuracy,
reaction timecongurant andreaction timeincongurantis supported by
EtnierandChang 2009[48]that found a significant improvement in the
Stroop Test after an acute moderate-intensity strength exercise (10 sets of
10 repetitions for six exercises) session in healthy middle-aged (49 ± 9
years) adults. Altogether, these findings reveal the potential of both
aerobic and strength exercise alone in improving executive function.
The potential benefits of physical exercise in promoting increased
EF in our study are consistent with the findings reported in recent
empirical studies on regular aerobic activity and open-skill exercise in
children with and without disabilities(Chang et al., 2014[49]; Guiney and
Machado, 2013[50]; Hilton et al., 2014[51]; Pan et al., 2015[52]; Tsai et
al., 2012[53]).
The results of the present study contradicted with the finding of
Ploughman et al.,(2008)[54] who reported that treadmill exercise did not
cause improvement in cognitive function (including the Trail Making
Test A and B, Symbol Digit Substitution Test, and Paced Auditory
Serial). The discrepancy between the present and Ploughman et
al.[54]study may be attributed to the small sample size and the short
duration of the physical therapy intervention of Ploughman et
al.[54]study. It was assumed thatsustained aerobic exercise (over months)
is required for cognitive improvement(Masley, 2009).[37].
The results of the present study also contradicted with the finding
of Correia et al., (2010)[55]who demonstrated that acute strengthening
exercises do not induce significant alterations in the levels of brain-
derived neurotrophic factor plasma concentrations in healthy individuals.
The discrepancy of results between two studies may be attributed to the
type of exercise program that may be a decisive factor in altering
peripheral brain-derived neurotrophic factor level.
Conclusion: It can be concluded that aerobic exercise has
significant effect on inhibitory control of executive functions in spastic
hemiplegic cerebral palsy children.
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