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Children with Attention Deficit Hyperactivity Disorder Have Impaired

Balance Function: Involvement of Somatosensory, Visual, and Vestibular


Systems
Selina B. M. Shum, MSc and Marco Y. C. Pang, PhD

Objectives To compare standing balance performance and sensory organization of balance control in children
with attention deficit hyperactivity disorder (combined type) (ADHD-C) and typically developing children.
Study design School-aged children (n = 43) with ADHD-C and 50 age- and sex-matched typically developing
children participated in the study. Sensory organization of standing balance was evaluated using the Sensory Or-
ganization Test (SOT). In addition to the composite equilibrium score, somatosensory, vestibular, and visual ratios,
which were indicators of the ability of the child to use information from the respective sensory systems to maintain
balance, were computed. Multivariate analysis of covariance (MANCOVA) was used to compare the outcome vari-
ables between the 2 groups while controlling for physical activity level.
Results MANCOVA revealed that children with ADHD-C had significantly lower composite equilibrium scores (P <
.001) and somatosensory (P = .029), vestibular (P = .037), and visual ratios (P = .001) than control children, by 10.3%,
2.1%, 15.6%, and 16.0%, respectively.
Conclusions Children with ADHD-C had significant deficits in standing balance performance in all conditions that
included a disruption of sensory signals. The visual system tends to be more involved in contributing to the balance
deficits in children with ADHD-C than the somatosensory and vestibular systems. (J Pediatr 2009;155:245-9).

A
ttention deficit hyperactivity disorder (ADHD) is one of the most common behavioral disorders in childhood,
affecting approximately 3% to 9% of typically-developing children.1 Apart from the classic symptoms of inatten-
tion, impulsivity, and hyperactivity, mounting evidence from behavioral and electrophysiological studies has
shown that many children with ADHD sustain deficiencies in sensory processing.2-4 In addition, neuroimaging studies
in children with ADHD have also revealed abnormalities not only in brain regions important for executive function
such as the prefrontal cortex5-7 but also in areas that are integral to sensorimotor control, particularly the cerebellum
and basal ganglia.8-11 These factors may underlie the suboptimal motor performance previously reported in some children
with ADHD.8,12-16
Balance control is an important sensorimotor function that may be compromised in the ADHD population because it
requires the ability to integrate inputs from various sensory systems (ie, somatosensory, visual, vestibular) and to utilize the
integrated sensory signals in generating coordinated motor actions to maintain body equilibrium.17 Studying balance perfor-
mance in children with ADHD is important, as impairments in balance ability may interfere with activity and partcipation18
and may increase the risk of injuries.19
To date, only 2 studies have examined sensory contributions to balance function in children with ADHD.20,21 Although
both studies found that the sway velocity of the center of pressure (COP) was significantly higher in the ADHD group
than in the control group in various testing conditions (eg, standing with the eyes closed, standing on a foam pad),
the extent to which different sensory systems contribute to the balance deficits in these children remains elusive. More-
over, no information on the ADHD subtypes (ie, predominantly hyperactive-impulsive, predominantly inattentive, com-
bined) and comorbidities [eg, developmental coordination disorder (DCD)] was provided. Because these factors may
influence the nature and severity of sensorimotor deficits,12,13,22 it would be important to use a homogeneous sample
of children with ADHD.

ADHD Attention deficit hyperactivity disorder


ADHD-C Attention deficit hyperactivity disorder (combined type)
COP Center of pressure
DCD Developmental coordination disorder From the Department of Rehabilitation Sciences, Hong
ICF International Classification of Functioning, Disability and Health Kong Polytechnic University, Hong Kong, China

MANCOVA Multivariate analysis of covariance The authors declare no conflicts of interest.

SOT Sensory Organization Test 0022-3476/$ - see front matter. Copyright Ó 2009 Mosby Inc.
All rights reserved. 10.1016/j.jpeds.2009.02.032

245
THE JOURNAL OF PEDIATRICS  www.jpeds.com Vol. 155, No. 2

The objectives of this cross-sectional case-control study with ADHD-C did not fulfill the eligibility criteria and were
were to compare standing balance ability and sensory organi- thus excluded. As a result, a total of 43 children with
zation of standing balance control between school-aged chil- ADHD-C and 50 typically developing children participated
dren with ADHD (combined type; ADHD-C) and age- and in the study. Subject characteristics are described in Table I.
sex-matched typically developing children and to identify The 2 groups of children did not differ significantly on phys-
which sensory system(s) may contribute to balance deficits ical activity level and other demographic variables.
in children with ADHD-C. All data collection was performed by an experienced pedi-
atric physiotherapist between February 2007 and July 2008.
Children who were taking prescribed medications for
Methods ADHD (ie, methylphenidate, atomoxetine) were instructed
not to take the medication on the day of testing. All proce-
Children with ADHD were recruited from the Central Kow- dures were conducted in accordance with the Declaration
loon Child Assessment Centre, which is a major institution of Helsinki. Relevant information such as medical history
that provides assessment service for children in Hong and medications was obtained by interviewing the parent.
Kong. Children who had recently been diagnosed with During the same interview, the physical activity level of
ADHD after a formal multidisciplinary evaluation at the each child was estimated by asking the parent the type of
Child Assessment Centre were screened by the research extracurricular physical activity that his or her child was
team to determine whether the following eligibility criteria most actively engaged in during a typical week within the
were fulfilled. The inclusion criteria were (1) a formal diag- past year. The physical activity level [in metabolic equivalent
nosis of ADHD-C made by a pediatrician, child psychologist, (MET) hours per week] was calculated, based on the intensity
or child psychiatrist, according to the ADHD criteria of (light, moderate, hard), duration (hours) and frequency
Diagnostic and Statistical Manual of Mental Disorders (times per week) of the activity as provided by the parent,
(DSM-IV-TR),23 (2) age between 6 and 12 years, and (3) as well as the assigned MET value of the activity according
studying in a regular education framework. Individuals to the Compendium of Energy Expenditures for Youth devel-
were excluded from the study if they had any of the following: oped by Ridley et al.26 This compendium was modeled after
(1) a history of neurological conditions (eg, cerebral palsy) the Adult Compendium of Physical Activities27 and contains
and other movement disorders (eg, tic disorders, athetosis, a list of more than 200 activities commonly performed by
chorea, dystonia), (2) mental retardation, (3) autistic disor- children and their associated MET values.26
der, and (4) significant musculoskeletal or cardiopulmonary Body height (m) and weight (kg) of each child were mea-
conditions that may influence balance performance (eg, sured by a mechanical scale equipped with a height rod
amputations, bone fractures, heart disease). Additionally, (420KL Physician Scale, Health-O-Meter, Bridgeview, Illi-
children were excluded if they had a diagnosis of DCD nois). The Sensory Organization Test (SOT) was used to
because they also demonstrate deficits in sensory organiza- evaluate the contributions of different sensory systems to
tion of balance control24 and may thus confound our results. standing balance control.28 The test is a common research
The screening of DCD during the multidisciplinary assess- tool in the evaluation of sensory organization of balance con-
ment was based on the diagnostic criteria described in trol and has been previously used by other researchers in
DSM-IV-TR.23 To warrant a diagnosis of DCD, the child studying balance performance in children.29 The system
had to demonstrate motor coordination substantially below used (SMART BalanceMaster, NeuroCom International,
that expected of the child’s age (ie, gross motor composite Inc, Clackamas, Oregon) consists of a dynamic 18  18
score <42 as measured by the Bruininks-Oseretsky Test of inch dual forceplate that provides data on the movement of
Motor Proficiency)25 which interfered with activities of daily the COP and a visual surround. The forceplate and visual sur-
living and academic performance. Each child also underwent round could tilt in response to the child’s anteroposterior
a neurological screening performed by a pediatrician to rule body sway in certain testing conditions (ie, sway-referenced),
out other causes of motor deficits before a diagnosis of thereby disrupting the information delivered from the
DCD was made. In addition, typically developing children, somatosensory and visual systems so that the vestibular sys-
matched to the ADHD group by age and sex, were recruited tem could be isolated.28 During the SOT, each child was
from the community. They had to fulfill the same inclusion asked to stand upright at the appointed position on the plat-
and exclusion criteria set above, except that they did not form for 20 seconds and try to keep his or her body as stable
have any history of ADHD. Ethics approval was obtained as possible under 6 different test conditions. The details of
from the Hong Kong Polytechnic University. The study was each condition are described in Table II. A practice trial
explained in detail to each child and his or her parent. Written for each condition was given before the actual recording. A
informed consent was obtained from the parent if he or she total of 3 trials were conducted for each condition. In each
agreed to participate in the study. As stipulated by the ethics trial, the system compared the child’s sway with the theoret-
committee, any child aged 7 years or more was also required ical limits of stability and generate an equilibrium score, with
to sign on the consent form before participating in the study. a higher equilibrium score indicating better standing stabil-
Forty-nine children with ADHD-C and 50 typically develop- ity. If the child had a fall, a score of 0 was given for that trial.
ing children volunteered for the study. However, 6 children A composite equilibrium score is also generated by the
246 Shum and Pang
August 2009 ORIGINAL ARTICLES

Table I. Subject characteristics Table II. The six test conditions of the Sensory
Control group Organization Test
ADHD group (n = 43) (n = 50) P value Sensory
Age, y 8.8  1.1 8.8  1.5 .984 signals Useful sensory
Sex (boys/girls), n 28/15 31/19 .756 Condition Description disrupted signals available
Height, m 1.31  0.07 1.30  0.10 .576 1 Eyes open, None Somatosensory,
Weight, kg 30.8  5.9 28.2  6.9 .060 fixed platform visual, vestibular
On medications for treating 8 — — 2 Eyes closed, Visual signals Somatosensory,
ADHD fixed platform removed vestibular
Methylphenidate, n 7 — — 3 Eyes open, Conflicting visual Somatosensory,
Atomoxetine, n 1 — — fixed platform, signals vestibular
Type of extracurricular sway-referenced
physical activities surround
Badminton, n 0 3 — 4 Eyes open, Conflicting somato- Visual, vestibular
Basketball, n 3 6 — sway-referenced sensory signals
Camping, n 3 3 — platform
Dancing, n 3 4 — 5 Eyes closed, Visual signals Vestibular
Drawing, n 3 0 — sway-referenced removed and
Ice skating, n 0 1 — platform conflicting
Kickboxing/martial arts, n 6 7 — somatosensory
Piano playing, n 2 5 — signals
Soccer, n 2 7 — 6 Eyes open, Conflicting visual Vestibular
Swimming, n 10 5 — sway-referenced and
Table tennis, n 1 0 — platform somatosensory
Violin playing, n 5 5 — and surround signals
No extracurricular 9 8 —
physical activity
Physical activity level 6.2  5.6 6.5  4.8 0.799
(MET hours per week)

Results
system, after taking into account the equilibrium scores at- MANCOVA revealed an overall significant difference in bal-
tained in all 6 different test conditions.28 The SMART Balan- ance performance between the two groups (Wilk’s l = 3.156,
ceMaster system also performed sensory ratio analysis, which P = .001). When each individual primary outcome was con-
yielded 4 different ratios, namely, the somatosensory, vestib- sidered, the between-group difference remained significant
ular, visual and preference ratios (Table III). for all the test conditions, except condition 1 (Table IV).
Descriptive statistics were used to describe all relevant vari- The composite equilibrium score was also significantly lower
ables. Normality of data was checked using the Kolmogorov- in the ADHD-C group than the control group by 10.3%
Smirnov test. Independent t tests and c2 tests were used to (P < .001). In addition, the somatosensory, vestibular, and
compare the continuous (ie, age, height, weight, physical visual ratios were all significantly lower in the ADHD-C
activity level) and categorical demographic variables (ie, group than the control group by 2.1% (P = .029), 15.6%
sex), respectively, between the ADHD-C group and the con- (P = .037), and 16.0% (P = .001), respectively. The preference
trol children. To compare balance performance between the ratio, on the other hand, showed no significant between-
2 groups while accounting for the possible confounding ef- group difference (P = .857). For those primary outcomes
fect of physical activity, a single multivariate analysis of co- that showed significant between-group differences, the par-
variance (MANCOVA) incorporating all primary outcomes tial h2 values ranged from 0.048 to 0.148, indicating medium
(ie, SOT-derived equilibrium scores and sensory ratios) to large effect sizes (Table IV).
was performed, with group (ie, ADHD-C versus control chil-
dren) as the fixed factor and physical activity level as the co-
variate. The results from this analysis showed the effects of Discussion
group on all primary outcomes simultaneously as well as
the corresponding Bonferroni-adjusted P values, thus avoid- Children with ADHD-C have significantly poorer balance
ing the increased probability of type I errors associated with performance than control children, after adjusting for physi-
multiple comparisons. Partial eta-squared (partial h2), which cal activity level. It is noteworthy that children with ADHD-C
is the standardized measure of effect size within the context of do not have particular problems in simple static standing bal-
MANCOVA,30 was also presented for each primary outcome. ance when information from all 3 sensory systems is available
By convention, partial h2 values of 0.01, 0.06, and 0.14 are (ie, condition 1 of SOT). However, when sensory information
considered to be small, medium, and large, respectively.30 from one of the systems is removed or distorted, balance def-
A significance level of .05 was set for all statistical tests icits would emerge in these more challenging conditions.
(2-tailed). All statistical analyses were performed using the Typically developing children should be able to utilize
Statistical Package for Social Sciences 16.0 software (SPSS somatosensory information effectively for maintaining bal-
Inc, Chicago, Illinois). ance well before school age, at around 3 to 4 years.29 In this
Children with Attention Deficit Hyperactivity Disorder Have Impaired Balance Function: Involvement of Somatosensory, 247
Visual, and Vestibular Systems
THE JOURNAL OF PEDIATRICS  www.jpeds.com Vol. 155, No. 2

Table III. Sensory ratio analysis Table IV. Results from the Sensory Organization Test
Sensory ratio* Description Computation ADHD group Control group Effect
(n = 43) (n = 50) P value size†
Somatosensory The ability of the child Condition 2
to use somatosensory Condition 1 Equilibrium score
information for maintaining for each test
balance. Condition 1 90.3  3.1 90.6  4.0 .704 .002
Visual The ability of the child Condition 4 Condition 2 86.1  3.6 88.1  4.3 .022* .057
to use visual information for Condition 1 Condition 3 85.4  5.0 87.6  4.5 .032* .050
maintaining balance. Condition 4 57.1  16.5 68.3  15.0 .001* .116
Vestibular The ability of the child Condition 5 Condition 5 34.5  16.2 40.9  13.2 .036* .048
to use vestibular Condition 1 Condition 6 34.0  15.2 43.0  17.2 .010* .071
information for maintaining Composite equilibrium 57.2  8.8 63.8  7.3 <.001* .148
balance. score
Preference The extent to which the child Condition 3 + 6 Sensory ratio analysis
relies on visual information Condition 2 + 5 Somatosensory ratio 0.95  0.04 0.97  0.04 .029* .052
to maintain balance, even Visual ratio 0.63  0.18 0.75  0.16 .001* .115
though the visual Vestibular ratio 0.38  0.18 0.45  0.14 .037* .048
information is incorrect. Preference ratio 1.02  0.17 1.02  0.16 .857 <.001
*The sensory ratios were generated automatically by the SMART BalanceMaster system; *Significant between-group difference (P < .05).
computational formulas are shown. †Effect sizes were calculated in partial eta-squared values (partial h2).

study, we showed that the somatosensory system may con-


tribute to the observed balance impairment in children ADHD-C had substantial difficulty with maintaining balance
with ADHD-C, as indicated by the significantly lower when they were forced to rely more on the visual information
somatosensory ratio in the ADHD-C group. However, the when somatosensory signals are disrupted (ie, condition 4).
deficit is relatively minor, as reflected by the modest Indeed, the visual system may be the most involved system
between-group difference in somatosensory ratio (2.1%). in contributing to the balance deficits among children with
The possible involvement of the somatosensory system in ADHD-C, as the visual ratio showed the greatest between-
balance dysfunction in children with ADHD is not entirely group difference (16.0%, large effect size of 0.115) when
surprising, as evidence from behavioral and electrophysio- compared with the somatosensory and vestibular ratios
logical studies has suggested that children with ADHD may (Table IV). This finding may also reveal that children with
have altered somatosensory function, including reduced tac- ADHD-C could not successfully compensate by utilizing
tile discrimination, and impaired modulation of kinesthetic visual information for maintaining balance. Had they been
information.2-4 able to compensate by using the visual inputs, the visual ratio
The vestibular system not only senses head position and would have sustained less deficit than the somatosensory and
movement but also plays an important role in gaze stabiliza- vestibular ratios. The lack of excessive reliance on visual infor-
tion.17 A properly functioning vestibular system is thus crit- mation for balance control is also reflected by the insignificant
ical in balance control. In the current study, we found that between-group difference in the preference ratio (Table IV).
children with ADHD-C have decreased ability to use vestib- Although we have identified significant balance deficits in
ular information to maintain balance, as reflected by the sig- children with ADHD-C, some important questions arise.
nificantly lower vestibular ratio. Wang et al21 also found that How are the balance deficits related to the behavioral symp-
in children with ADHD, a significant correlation exists be- toms of ADHD (ie, impulsivity, hyperactivity, inattention)?
tween sway velocity during standing on a foam pad with What are the possible neural substrates for the observed bal-
the eyes closed (similar to condition 5 in our study) and ves- ance dysfunctions? Neuroimaging studies have provided
tibular dysfunction as measured by the sensory integration some insights into these areas.5-11
check scale, again highlighting the possible involvement of Unusual activity in the prefrontal cortex, an area impor-
the vestibular system in balance dysfunctions. Interestingly, tant for executive functions such as moderating socially
Yochman et al4 did not find any significant deficits in vestib- acceptable behaviors and decision-making, has been reported
ular processing and modulation in preschool children with in some individuals with ADHD.5-8 Interestingly, abnormal-
ADHD. However, balance performance was not examined ities (eg, reduced size, decreased blood flow) in the cerebel-
in their study. The link between the vestibular and visual sys- lum and caudate nucleus have also been found in some
tems (ie, gaze stabilization) was also not explored. Moreover, children with ADHD.8-10 Both of these brain structures
it is possible that deficits in vestibular processing in children have extensive interconnections with the prefrontal cor-
with ADHD may not be as apparent in preschool age, as the tex.8,17 Thus, dysfunction in one component of this neural
vestibular system is the last to reach full functional matura- circuitry may affect functioning of other parts of the system.8
tion in balance control (around 15 years of age).29 Although the prefrontal cortex has been thought to con-
Deficits in visual information processing and visual-motor tribute to the behavioral symptoms observed in ADHD,8,9
integration in children with ADHD have been previously its intimate connections with the cerebellum and the caudate
reported.3,4 In this study, we found that children with nucleus may partly explain the coexistence of sensorimotor
248 Shum and Pang
August 2009 ORIGINAL ARTICLES

deficits and behavioral symptoms in children with ADHD.8,9 computed tomorgraphy (SPECT), electro-encephalogram (EEG), be-
The cerebellum, in particular, receives extensive inputs from havior symptoms, cognition and neurological soft signs in children
with attention-deficit hyperactivity disorder (ADHD). Acta Paediatr
the somatosensory, vestibular, and visual systems and plays
2000;89:830-5.
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When coupled with ADHD-related symptoms (inattention, attention deficit hyperactivity disorder: subtype differences and the effect
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21:919-45.
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school children with attention deficit hyperactivity disorder. Percept
There are several limitations in this study. First, a conve-
Mot Skills 2006;102:175-86.
nience sample was used, and self-selection bias may be 15. Raggio DJ. Visuomotor perception in children with ADHD-combined
involved. For example, parents who were more concerned type. Percept Mot Skills 1999;88:448-50.
about the children’s balance ability might be more willing 16. Raberger T, Wimmer H. On the automaticity/cerebellar deficit hypoth-
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dren were receiving medications for ADHD. The sample
17. Kandel ER, Schwartz JH, Jessell TM. Principles of neural science. 4th ed.
might reflect a group of children with a milder expression New York: McGraw-Hill; 2000.
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Submitted for publication Sep 19, 2008; last revision received Dec 30, 2008; dysfunction in attention deficit hyperactivity disorder children. Chin J
accepted Feb 13, 2009. Clin Med 2002;6:1372-4.
Reprint requests: Dr Marco Y.C. Pang, Department of Rehabilitation Sciences, 21. Wang J, Wang Y, Ren Y. A case control study on balance function of at-
Hong Kong Polytechnic University, Kowloon, Hong Kong. E-mail: rsmpang@ tention deficit hyperactivity disorder (ADHD) children. J Peking Univ
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Children with Attention Deficit Hyperactivity Disorder Have Impaired Balance Function: Involvement of Somatosensory, 249
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