METHODS
Subjects
From 107 children 9 to 14 years of age, admitted
consecutively to National Jewish Center for
Im-munology and Respiratory Medicine, 67 asthmatic
children were selected for neuromotor evaluation.
Children were selected for evaluation who were
suspected of being at increased risk of neuromotor
impairment because of reduced academic skills or
observed motor awkwardness.
Instruments
Neuromotor Testing. The Bruininks-Oseretsky
Psychomotor
Adaptation
in Children
With
Severe
Chronic
Asthma
Bruce G. Bender,
PhD, Louise
Belleau,
BS, Jolene
T. Fukuhara,
BA,
David A. Mrazek,
MD, MRCPsych,
and Robert
C. Strunk,
MD
From the Departments of Pediatrics and Rehabilitation Services, National Jewish Center for Immunology and Respiratory Medicine, Denver, and the Departments of Psychiatry and Pediatrics, University of Colorado School of Medicine, Denver
ABSTRACT.
Acute effects of steroid medications orhy-poxic-induced brain damage have been hypothesized to
cause neuropsychologic impairment in children with
se-vere asthma. The present investigation included
neuro-motor, cognitive, psychosocial, and medical evaluations
of 67 hospitalized asthmatic children from 9 to 14 years
of age, at risk for motor dysfunction. Mean scores from
the Bruininks-Oseretsky Test of Motor Proficiency
(BOTMP) were similar to test norm means and were not
indicative of neuromotor impairment. Scores of the
BOTMP correlated significantly (P < .01) with measures
of child and family psychosocial adaptation but not with measures of cognitive ability, steroid dose at admission, or severity of asthma. Thirteen children had battery
composite scores more than 1 SD below age means but
did not demonstrate decreased IQ or increased steroid use, respiratory failure, seizures, or abnormal neurologic signs compared with the other 55 children. These results
indicate that most severely asthmatic children, including
many with histories of hypoxia and high-dose steroid use, do not demonstrate psychomotor impairments indicative of brain damage. It is concluded that neuromotor
devel-opment in asthmatic children is associated with psycho-logic characteristics that influence adaptation to illness and activity level. Pediatrics 1987;79:723-727; psycho-motor adaptation, asthma, IQ, neuromotor impairment, steroids.
Children with asthma are at increased risk for
learning problems,”2 psychosocial dysfunction,36
and impaired physical conditioning.7 Specific
infor-mation about the psychomotor development of
asthmatic children is limited. Dunleavy and
colleagues’#{176} examined a group of 20 severely
asth-matic children with the Halstead
Neuropsycholog-ical Battery and found them to have deficits in
spatial, visual-motor, and motor skills. The absence
of a relationship between neuropsychologic findings
and severity of illness, use of medications, and
school histories was briefly discussed, and histories of cyanotic respiratory arrests in four affected
chil-then were cited as evidence of hypoxia-induced
brain damage.
This investigation examines neuromotor
func-tions in children with severe asthma and the
rela-tionship between neuromotor dysfunction and
cog-nitive ability, psychosocial adaptation, and severity
of physical illness. To help determine whether the
presence of neuromotor dysfunction is associated
with events that might underlie neurologic
impair-ment, histories of respiratory arrest, seizure
disor-ABBREVIATIONS. BOTMP, Bruininks-Oseretsky Test of Motor Proficiency; CBCL, Children’s Behavior Checklist; CGAS, Chil-then’s Global Assessment Scale; FGAS, Family Global Assess-ment Scale.
Asthma, a chronic respiratory illness, imposes
far-reaching effects on individual development.
Received for publication April 28, 1986; accepted June 17, 1986. Reprint requests to (B.G.B.) Department of Pediatrics, National Jewish Center for Immunology and Respiratory Medicine, 1400
Jackson St. Denver, CO 80206.
PEDIATRICS (ISSN 0031 4005). Copyright © 1987 by the
American Academy of Pediatrics.
-FINE MOTOR COMPOSITE _______________________
BATTERY COMPOSITE
O,-Z U))4
,. iW +
Figure. Neuromotor Scores of 67 Hospitalized Asth-matic Children
Test of Motor Proficiency (BOTMP)” is a
stand-ardized test instrument which has been used to
assess neuromotor functioning in a variety of
spe-cial populations, including children with learning
disabilities,’2 hearing impairment,’3 visual
impair-ment,’4 and hypothyroidism.’5 The battery consists
of eight subtests of motor proficiency (running
speed and agility, balance, bilateral coordination,
strength, upper-limb coordination, response speed,
visual-motor coordination, upper limb speed and
dexterity) and three composite scores (gross motor
composite, fine motor composite, battery
compos-ite), which have been described in detail
else-where.1’
All patients were also examined for the following
signs
of neurologic abnormality: (1) abnormalmus-cle tone and deep tendon reflexes, (2) abnormal eye
movements (tracking, nystagmus), (3) diadokinesis,
(4) disequilibrium, (5) proprioceptic dysfunction,
(6) choreoathetosis, (7) dyspraxia, (8) tactile
defen-siveness, (9) hyperactivity, (10) involuntary
move-ments, (1 1) abnormal sequential finger opposition,
(12) incompletely established lateral hand domi-nance, and (13) visual-motor dysfunction.
Cognitive and Academic Testing. The Slosson
In-telligence Scale’6 yielded a measure of general
in-tellectual ability. The reading, written language,
and math subsection scores from the
Woodcock-Johnson Psychoeducational Battery’7 provided an
assessment of academic skills.
Psychosocial Testing. The Children’s Behavior
Checklist (CBCL),18”9 a 118-item parental report
questionnaire used to assess behavioral problems,
was completed by mothers of 59 of the 67 children.
The total scores for behavior problem,
internaliz-ing, and externalizing are reported.
The Children’s Global Assessment Scale
(CGAS)2#{176}provided a single-index assessment of
severity of disturbance. In contrast to the CBCL
parental report questionnaire, this scale was
com-pleted by concensus of the clinical psychosocial
staff (psychiatry, psychology, social work) following initial evaluation and observation.
The Family Global Assessment Scale (FGAS)2’
was designed recently by National Jewish Center
researchers as a continuous-scale index of each
family’s general adaptation. The FGAS, which is
based upon the format and structure of the CGAS,
was also completed by the staffing team.
Medical History and Pulmonary Functions.
Infor-mation was included to reflect history of asthma
and medical intervention, presence of events or
treatments that increase likelihood of
neuropsycho-logic impairment, and status of pulmonary
func-tions at admission. Information included was as
follows: (1) pulmonary function test results from
the first 24 to 48 hours of hospitalization, including
forced expiratory volume, forced expiratory flow,
thoracic gas volume, and specific airways
conductance22; (2) age of asthma onset; (3) number
of asthma-related hospitalizations in year prior to
admission to the National Jewish Center (data
confirmed by calling the medical records
depart-ments of all previous hospitals in which the child
stayed; (4) steroid dose at admission; (5) history,
taken from parents on admission, of steroid use in
the year prior to admission, dichotomized into
cat-egories (no use or occasional use v long-term use,
ranging from continuous every-other-day use to
daily ingestion); (6) history of respiratory failure
requiring ventilation; and (7) history of seizures
associated with asthma attacks (hypoxic).
RESULTS
The BOTMP performance profile indicated that,
on average, the 67 asthmatic children had normal
ability for all neuromotor skills (Figure).
Correla-tions between BOTMP scores and other variables
are reported in Table 1. Because ofthe large number
of correlations, a conservative .01 a level was
Se-lected.
Severity of illness, as assessed by degree of
air-ways obstruction on pulmonary function tests, age
of asthma onset, number of hospitalizations for
treatment of asthma, and steroid dose at admission,
was not associated with the level of neuromotor
function (Table 1). In addition, none of the
neuro-motor scores was correlated significantly with IQ,
reading, math, or written language scores.
Signifi-cant correlations were found only between
meas-ures of psychosocial adaptation (Table 1). Lower
RUNNING SPEED S AGILITY
J
BALANCE
BILATERAL COORDINATION STRENGTH UPPER-LIMB COORDINATION
RESPONSE SPEED
VISUAL-MOTOR CONTROL UPPER.LIMB SPEED S DEXTERITY
0 2 4 6 8 10 12 14 16 18 20
gross motor and battery composite scores were
moderately associated (r = .38 to .43), with
de-creased psychosocial adaptation of both individual
children (CGAS) and families (FGAS). In contrast
to the significant correlations for CGAS and FGAS,
neuromotor function did not correlate with CBCL.
To more clearly establish whether the children
with neuromotor deficits present histories and
functional characteristics suggestive of
neuropsy-chologic impairment related to high-risk events, the
children with BOTMP battery composite scores
more than 1 SD below age means were evaluated as
a separate group. Thirteen children had scores
plac-ing them below the cutoff selected to define
neu-romotor impariment, two more than would be
pre-dicted on the basis of normal distribution in any
unselected group of 67 individuals. For the 13
im-paired and 54 unimpaired children, means and
standard deviations are reported in Table 2 on
measures that may correlate with neuromotor skill,
including CGAS, FGAS, IQ, steroid use, respiratory
failure, seizures, and abnormal neurologic signs. As
expected, measures of individual and family
psy-chosocial adaptation were significantly lower in the
impaired group. However, IQ scores and histories
of steroid use were similar in the two groups.
Inci-dences of respiratory failure, seizures, and
abnor-ma! neurologic signs were low in both groups.
Al-though results suggested that these occurred more
frequently in the impaired group, no significant differences were found.
Respiratory failure, identified elsewhere as a
po-tential cause of neurologic injury in many asthmatic
children, did not emerge as a strong predictor of
neuromotor scores. After the correlations between
CGAS and FGAS and BOTMP composite scores,
were determined, respiratory failure accounted for
only 1 % of the variance in neuromotor functions.
TABLE 1. Pearson Correlations Between Bruininks-Oseretsky Test of Motor Proficiency Composite Scores and 16
Potentially Related Variables
Gross Motor Fine Motor Composite Composite
Battery Composite
Medical
Forced expiratory volume in 1 s -.11 -.07 -.07
Forced expiratory flow from 25%-75% of -.17 -.18 -.11
vital capacity
Thoracic gas volume .03 -.09 .07
Specific airways conductance .04 -.11 .01
Age of asthma onset .16 .14 .15
Hospitalization in previous yr -.07 .14 -.14
Steroid dose at admission -.01 .06 -.06
Cognitive/academic
IQ .26 .17 .24
Reading .06 -.02 .02
Math .19 .19 .22
Written language .09 .00 .05
Psychologic
Children’s global assessment scale .42t .17 .38*
Family global assessment scale .43t .30 #{149}43*
Children’s behavior checklist-internal -.26 -.19 -.24
Children’s behavior checklist-external -.14 -.04 -.13
Children’s behavior checklist-total -.18 -.10 -.15
* P .01, significant at a level.
t
P .001, nonsignificant at a level.:1:
P .05, nonsignificant at a level.TABLE 2. Characteristics of Neuromotor Impaired and Unimpaired Asthmatic Children
Characteristic Impaired Unimpaired Student’s x2 P Value
(n=13) (n=54) tValue
Children’s global assessment scale 50.4 ± 8.0 58.6 ± 10.7 -3.07 .005
(mean ± SD)
Family global assessment scale 52.5 ± 10.6 59.8 ± 10.9 -2.19 .032
(mean ± SD)
IQ (mean ± SD) 100.7 ± 14.2 108.9 ± 13.7 -1.83 .087
High-dose steroid use (%) 58 52 .017 .897
Respiratory failure (%) 23 13 .844 .380
Seizures (%) 31 19 .951 .329
Finally, examination of individual cases did not
reveal an association between respiratory failure
and other clinical evidence of neurologic
impair-ment. No child demonstrated a pattern of history
of respiratory failure combined with reduced
neu-romotor performance, low IQ, and indicators of
neurologic abnormalities. Only four children had
abnormal neurologic signs, including hypotonia,
dyspraxia, dysequilibrium, and hyperactivity. One
of the two children in the neuromotor-impaired
group showing these signs had a history of
respi-ratory failure and seizures; the same child had an
IQ of 128. The only other child with history of
respiratory failure had an IQ of 95 and no abnormal
neurologic signs.
DISCUSSION
Decreased neuromotor scores were not associated
with severity of illness or medical histories in
chil-then with severe asthma. Within this group,
psy-chosocial functioning alone was correlated with
neuromotor skills. It is possible that children with
poor psychologic function, as reflected by a low
CGAS score, may be physically inactive, withdrawn
from peers, and frequently absent from school
be-cause of chronic illness, making decreased motor
skills more likely. The lower family scores may be
associated with the lower BOTMP scores because
of problems in support and availability from within
a poorly functioning family system. Without
posi-tive parental action in caring for their child’s
asthma, opportunities to increase activity levels and
foster motor development may be underused.
It is also possible that decreased psychosocial
functioning may be the result, rather than the
cause, of decreased neuromotor functioning.
How-ever, even in the group of 13 impaired children, the
degree of neuromotor deficit was not severe and
unlikely to represent a significant stress to
psycho-logic adaptation. The well-recognized presence of
psychologic dysfunction in asthmatic children3
remains a primary characteristic of the children in
this study, with neuromotor dysfunction a likely secondary result.
Unlike the assessments made by clinicians
(CGAS and FGAS), the mother’s assessments of
behavior (CBCL) did not correlate with neuromotor
skills. This finding may reflect the desire by some
parents to deny behavioral difficulty associated
with their child’s illness or the parents relatively
limited knowledge of the child’s internal state. The
internalizing score from the CBCL approached a
significant correlation with the gross motor
corn-posite score, suggesting that an increase in
depres-sive or anxiety-related symptoms may be associated
with impeded neuromotor development.
Psycho-logic dysfunction, which occurs with increased
fre-quency in asthmatic children,3 is a powerful factor
that must be addressed if their illness is to be
effectively treated.
Our results differ from those of Dunleavy and
Baade,8 who found perceptual and motor deficits in
a group of severely asthmatic children and
con-cluded that seven (37%) had significant
neuropsy-chologic impairment. They hypothesized that brain
damage may have been sustained during severe
hypoxic attacks. Increased incidence of
psychomo-tor impairment suggestive of pronounced
neuropsy-chologic impairment or brain damage was not found
in this study, even though all subjects had severe
asthma and were selected for increased risk of
academic and motor dysfunction. As a group, the
67 asthmatic children in this study possess average
neuromotor skills across measures of speed, agility,
strength, dexterity, and coordination. Decreased
neuromotor skill occurred only slightly more
fre-quently than expected by chance and was not
ac-companied by decreased general intelligence. In
addition, none of the neuromotor scores were
cor-related with reading, math, or written language
scores, although correlation between IQ and the
gross motor composite score on BOTMP
ap-proached significance. Furthermore, no clear
rela-tionship was found among the variables of reduced
motor scores, severity of illness, or medical events
hypothesized to place these children at increased
risk for brain damage, including histories of seizures
and respiratory arrest and steroid use. Finally, even
in the 19% of children in this sample with deficient
motor skills, the deficits were not associated with
high-risk histories or with atypical intellectual or
neurologic findings.
For the majority of asthmatic children, the term
brain damage, with its implications of dramatic and
irreversible changes in functional skills, cannot be
appropriately assigned. An occasional asthmatic
child may suffer severe enough hypoxia to result in
brain damage, especially because instances of
oxy-gen deprivation are known to result in subtle
changes in cognition.23’24 It is also possible that
temporary and subtle changes in cognitive
func-tions may result from steroid use without
perma-nent alteration of brain functions. Suess et al24a
found reduced verbal memory in asthmatic children
eight hours, but not 24 hours, after ingestion of
corticosteroids. Suppression of ACTH has been
hypothesized as the primary mechanism by which
steroids exert their temporary influence on
mem-ory.25’26 Other medications used by asthmatic
chil-dren, in particular theophylline, may also cause
acute behavioral side effects, including reduced
ability to concentrate.27
severe asthma and its treatments on children’s
development promises to yield important
theoreti-cal and clinical information. Emphasis on the study
of psychosocial correlates of childhood asthma,
alone found to be associated with neuromotor skills
in this sample of asthmatic children, is underscored
by recent proof that psychologic risk factors were
present among children who died of asthma?
Asth-matic children with psychologic difficulties,
there-fore, represent a particularly problematic group
whose dysfunction may include deficient
neuro-motor development. This information indicates
again the central role of psychologic intervention
in a comprehensive treatment program. Combined
medical, rehabilitative, educational, and
psycho-logic treatment has been shown to improve
cardio-vascular conditioning in asthmatic children,7 an
important step toward stabilization and integration
into age-appropriate social, academic, and physical
activities.
ACKNOWLEDGMENTS
This work was supported, in part, by a grant from
National Jewish Center for Immunology and Respiratory
Medicine. Dr Mrazek was the recipient of National
In-stitute of Mental Health research scientist development
award I-K01-MH00430-O1A1. Dr Strunk was the
recipi-ent of allergic diseases academic award I-K07-A100543
from the National Institute of Allergies and Infectious
Diseases.
We thank Georgia Wheeler for typing the manuscript.
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