Journal of Pediatric Psychology, Vol. 28, No. 1, 2003, pp. 59-65
© 2003 Society of Pediatric Psychology
A Prospective Study of the Relationship Over Time of Behavior Problems, Intellectual Functioning, and Family Functioning in Children With Sickle Cell Disease: A Report From the Cooperative Study of Sickle Cell Disease
1 Duke University, 2 University of Miami School of Medicine, 3 New England Research Institute, 4 Cedar Sinai Hospital, Los Angeles, 5 St. Jude Children's Research Hospital
All correspondence should be sent to Robert J. Thompson, Jr., Duke University, 114 Allen Building, Box 90042, Durham, North Carolina 27708-0042. E-mail: bobt{at}asdean.duke.edu.
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Abstract |
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Objective To longitudinally assess the relationship of behavioral problems, intellectual functioning, and family functioning in children with sickle cell disease (SCD). Method The study sample included 222 children enrolled in the Cooperative Study of Sickle Cell Disease (CSSCD). The study protocol included intellectual evaluation and brain magnetic resonance imaging (MRI) of the children, and mothers completed the Child Behavior Checklist and Family Environment Scale. At least two complete sets of measures were obtained across four assessment points over the study period of 9 years. Results Intellectual functioning declined, but family functioning and behavior problem scores did not change significantly. Consistent behavior problems were reported by mothers for 9% of the children. The risk of consistent behavior problems was not related to MRI classification, gender, education level of mother, or age of the child but significantly increased with higher baseline levels of family conflict and decreased with higher baseline full-scale IQ. An increase in behavior problems was associated with an increase in family conflict. Conclusions Maternal appraisal of family conflict is a risk factor for the small subgroup of children with SCD with consistent mother-reported behavior problems and a salient intervention target for fostering adaptation.
Key words: family functioning; intellectual functioning; behavior problems; sickle cell disease.
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Introduction |
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There is increasing evidence that children with sickle cell disease (SCD) are at risk for behavior problems and neurocognitive impairment. The evidence regarding the behavioral adjustment of children with SCD is similar to that for children with chronic illness in general: There is an increased risk for adjustment problems, but good adjustment is typical (Thompson & Gustafson, 1996
). Research is now focused on identification of
socio-ecological and neurocognitive processes associated with behavioral
adjustment. Adjustment problems have been associated with family functioning
characterized by high levels of conflict and low levels of support or cohesion
(Wallander & Thompson,
1995). Furthermore, there is an increased risk of adjustment
problems with conditions involving the brain
(Wallander & Thompson,
1995), and intellectual functioning has been found to have a
compensatory relationship with self-, parent-, and teacher-reported adjustment
(Perrin, Ayoub, & Willett,
1993).
The Cooperative Study of Sickle Cell Disease (CSSCD), a national natural
history study with patients from 15 clinical sites
(Farber, Koshy, & Kinney,
1985; Gaston & Rosse,
1982), provided radiological evidence of a brain infarct in
children, 6-12 years of age, with HbSS (sickle cell anemia): 6.6% had a
clinical cerebrovascular accident and 15.6% had a silent infarct
(Armstrong et al., 1996).
Neurocognitive functioning was linked with magnetic resonance imaging (MRI)
status. Children with MRI abnormalities performed more poorly on an array of
neuropsychological measures than children with no evidence of neurologic
impairment (Armstrong et al.,
1996). This association of neurological impairment and deficits in
intellectual and academic functioning has been found in other studies of
children with SCD. For example, frontal lobe impairment has been associated
with deficits in sustained attention (Brown et al.,
1993,
2000). Furthermore, a recent
prospective study from the CSSCD found a decrease in verbal IQ and math scores
with increasing age in children with sickle cell anemia and normal MRI
findings (Wang et al.,
2001).
The CSSCD also provided an opportunity to examine the independent and
combined contributions of family functioning and neurocognitive functioning to
the adjustment of children with SCD. In an initial cross-sectional study of
289 children, 6-15 years of age, 30% had a mother-reported behavior problem
(Thompson, Armstrong, et al.,
1999). The subgroup with behavior problems had significantly lower
verbal IQ, reading, and math scores and lower levels of family support and
higher levels of family conflict than the subgroup without behavior problems.
However, there was no significant difference in the rate of behavior problems
across the three subgroups formed on the basis of MRI status (normal,
clinically apparent cerebral infarction, silent infarction). Demographic
parameters of child age and gender and mother age and education accounted for
only 2% of the variance in behavior problems, and the biomedical parameters of
type of SCD and hematocrit level accounted for another 2%. Family functioning
characterized as conflicted, reflecting high levels of conflict and a lack of
both organization and support, accounted for a 19% increment in variance in
behavior problems beyond the 4% accounted for by the demographic and
biomedical parameters. Contrary to expectations, the neuropsychological
parameters of verbal, performance, and full-scale IQ scores; reading and math
cluster scores; and MRI status did not account for a significant portion of
variance in behavior problem scores.
Given the progressive course of SCD, one objective of the CSSCD was to
longitudinally assess functioning. This study addresses behavior problems,
neurocognitive functioning, and family functioning over time. Based on the
findings of the cross-sectional study
(Thompson, Armstrong, et al.,
1999), we tested four specific hypotheses. First, neurocognitive
functioning, as reflected in full-scale IQ scores and MRI status, would
decline over time. Second, there would be no significant change in mean
behavioral problem scores or family functioning factor scores. Third,
consistent behavior problems would be associated with higher baseline levels
of family conflict and lower levels of intellectual functioning. Fourth,
changes in behavior problem scores would be positively related to changes in
ratings of family conflict but not related to changes in intellectual
scores.
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Method |
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Participants
The study sample was a subset of the 431 children with HbSS or HbSC disease who were enrolled in the CSSCD and were born between October 1978 and August 1988. Informed consent was obtained from parents (or legal guardians) in accordance with institution review board requirements at participating centers. The study protocol was prospective and longitudinal and included serial assessment every 2 years with MRI, intellectual, and academic assessment of each child, and mother-completed measures of child behavior problems and family functioning. The study sample included 222 children (111 girls and 111 boys) who met the following inclusion criteria: at least two complete sets of measures were obtained across four assessment points over the study period of 9 years; the maximum interval between the MRI and other measures obtained at each assessment phase did not exceed 180 days; and family and child behavior questionnaires were completed by mothers who were living with their child. Of the study sample of 222, 104 (47%) completed two assessments, 87 (39%) completed three assessments, and 31 (14%) completed four assessments. Details related to patient recruitment and enrollment procedures, as well as psychometric testing methods, have been previously descibed (Armstrong et al., 1996
;
Farber et al., 1985;
Gaston & Rosse, 1982). At the time the maternal caregivers were first interviewed, the children ranged in age from 5 to 15 years with a mean of 8.2 (SD = 2.0). At the time of the last evaluation, the children were 7 to 17 years of age with a mean of 12.5 (SD = 2.3). Maternal age at the time of the first interview ranged from 21 to 59 years with a mean of 33.6 (SD = 6.5). Eighty-four (37.8%) mothers had less than a high school education, 65 (29.3%) were high school graduates or obtained the general equivalency degree (GED), 17 (7.7%) had some technical training after high school, 41 (18.5%) had some college education, 10 (4.5%) were college graduates, and 5 (2.2%) completed an advanced degree after college. Seventy-six (34.2%) mothers were married living with their spouse, 34 (15.3%) were divorced or separated, and 112 (50.4%) were never married.
The study sample (N = 222) did not differ significantly
(chi-square or t test) from those not in the study (i.e., did not
meet inclusion criteria; n = 209) in the proportion of phenotype
(HbSS vs. HbSC), gender, mean percentage hematocrit, maternal education, total
behavior problem score, family functioning factor scores, or full-scale,
performance, or verbal IQ scores at the time of the first neuropsychological
evaluation. The study sample had slightly lower mean child age (8.2 yrs vs.
8.7 yrs, t = 2.14, p = .03), and the mothers were more
likely to have never married (48% vs. 34%, 
2 = 6.71, 2 df,
p = .04) than those not in the study.
Within the study sample, there were no significant differences between the subgroups completing two or three or four assessments in the proportion of child phenotype (HbSS vs. HbSC), gender, or mean percentage hematocrit, marital status, maternal education, family functioning factor scores, total behavior problem score, child age, or full-scale, performance scale, or verbal scale IQ scores at the time of the first assessment. There was no significant difference in mean child age at the time of the initial assessment between those subgroups with two (8.4 yrs), three (8.3 yrs) or four (7.8 yrs) asessments.
Medical Parameters
Phenotype was confirmed by the Centers for Disease Control and Prevention:
150 children (68%) had HbSS and 72 children (32%) had HbSC. The percentage
hematocrit, obtained closest to the time of the first neuropsychological
evaluation, ranged from 15.7% to 39.3%, with a mean of 26.3% and a standard
deviation of 5.2% (HbSS M = 23.7%; HbSC M = 31.3%).
Behavioral Problems. Mothers completed the Child Behavior
Checklist (CBCL; Achenbach & Edelbrock,
1983), which assesses the frequency of 112 problem behaviors on a
3-point scale (not true, somewhat or sometimes true, very true or often true).
A total behavior problem score above the 90th percentile (T > 63; 1983
norms) was considered to be indicative of a clinically significant behavior
problem.
Intellectual Evaluation. The standardized test battery,
individually administered by trained examiners under the supervision of a
licensed psychologist, included measures of intellectual functioning. The
Wechsler Intelligence Scale for Children-Revised (WISC-R;
Wechsler, 1974) was used until
April 1994 and the Wechsler Intelligence Scale, Third Edition (WISC-III;
Wechsler, 1991) was used
thereafter. Both measures yielded full-scale, verbal scale, and performance
scale intelligence quotients (IQ). Comparison studies have found the WISC-III
scores to be lower than WISC-R scores
(Edelman, 1996;
Vance, Maddux, Fuller, & Awadh,
1996), and a recent CSSCD report found that WISC-III scores were
lower than WISC-R scores by 5, 2, and 7 points, respectively, for full-,
verbal, and performance scale IQ scores
(Wang et al., 2001).
Across the four assessments of the study sample of 222, 28 children completed only the WISC-R, 28 children completed only the WISC-III, and 166 completed both measures. Of the 104 children who completed two assessments, 28 completed only the WISC-R, 24 completed only the WISC-III, and 52 completed both. Of the 87 children who completed three assessments, none completed only the WISC-R, 4 completed only the WISC-III, and 47 and 36 completed one or two WISC-IIIs, respectively. Of the 31 children who completed four assessments, all completed both measures with 1, 27, and 3 children completing one, two, and three WISC-IIIs, respectively.
Magnetic Resonance Imaging. MRIs of the brain without contrast
were performed in accordance with the standard study protocol that was
implemented at each institution (see Moser
et al., 1996). Each patient's MRI was reviewed independently by
two neuroradiologists without knowledge of the patient's diagnosis or clinical
history. If there was no consensus interpretation, a third neuroradiologist
reviewed the film, and consensus was reached by discussion among the three
neuroradiologists (Moser et al.,
1996).
Location and extent of gray and white matter abnormalities were noted on a
standardized form. Atrophy was defined as a lesser than expected volume of
brain substance, and infarction/ischemia was defined as an area of abnormally
increased signal on the intermediate and T2-weighted pulse
sequences (Moser et al.,
1996). Patients with infarction were further classified as having
had a clinically apparent cerebrovascular accident (CVA) based on
documentation in their CSSCD database. Patients with infarction/ischemia
identified by MRI but without documented CVA were classified as having silent
infarcts (Moser et al.,
1996).
MRIs were obtained on all 222 children within 180 days of the
neuropsychological evaluation and were classified into one of three subgroups:
normal, clinically apparent cerebral infarction, and silent cerebral
infarction (see Armstrong et al.,
1996, for a more detailed description of MRI classification
procedures and criteria).
Family Functioning. Mothers completed the Family Environment Scale
(FES; Moos & Moos, 1981),
a 90-item, true-false, measure of the social environments of families. The FES
is composed of 10 subscales, which cluster into three empirically derived
higher-order components: supportive, conflicted, and controlling
(Kronenberger & Thompson,
1990). The component structure of the FES has been replicated with
both adolescent and adult samples drawn from the normative FES data
(Kronenberger & Thompson,
1990) and with the families of children with sickle cell disease
who were included in the CSSCD baseline neuropsychological functioning study
(Thompson, Gustafson, Gil, Kinney, &
Spock, 1999).
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Results |
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Hypotheses 1 and 2, regarding changes over time in behavior problems, neurocognitive functioning, and family functioning, were assessed using a mixed model (Little, Miliken, Stroup, & Wolfinger, 1996
), which is a repeated measure analysis of
variance (MANOVA) that reflects change in variables (e.g., age, MRI status, IQ
scores) over time. The intercept was allowed to vary between children
accounting for the correlation of results due to repeated testing of the same
child. The mixed model ignores cases with missing data for the variables
involved. The means and standard deviations for total behavior problem score;
verbal, performance, and full-scale IQ scores; and the supportive, conflicted,
and controlling factors of family functioning are presented by MRI (normal,
silent infarct, and stroke) subgroups in
Table I for children with HbSS
and Table II for children with
HbSC. As hypothesized, there were no significant changes in behavior problem
or family functioning scores over time, as measured by both the order of the
assessment and the child's age overall, or within the normal or abnormal MRI
subgroups, or HbSS or HbSC subgroups. However, there were differences in
intellectual functioning over time that varied with both age and order of the
assessment. A model was fit with HbSS and HbSC subgroups combined that
included age, order, MRI classification, and an indicator of WISC-III or
WISCR. Table III shows the
effects of each factor in the model. There was an increase in scores with
subsequent assessments (adjusted for age) and a decrease in scores with age
(adjusted for subsequent assessments). There was a decrease in scores due to
the change in tests. The silent infarct and stroke subgroups had lower scores
than those in the normal subgroup. On average, full-scale IQ decreases 1.2
points per year with age. Compared with a child with normal MRI, full-scale IQ
was 3.8 points lower for a child with a silent infarct and 14.4 points lower
for a child with stroke.
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There also was change in MRI status over time. At the time of the first assessment, there were 174 children in the normal group, 10 with clinically apparent cerebral infarction, and 38 with silent cerebral infarction. By the time of the last evaluation, five children had changed from the normal group to the silent infarct group and three children changed from silent infarct to confirmed stroke.
Hypothesis 3, that consistently poor adjustment would be related to baseline levels of family functioning and neurocognitive functioning, was assessed by comparing the consistently good and consistently poor behavior problem (total behavior problem score: T > 63) subgroups using logistic regression. Of the 118 children with at least three CBCL measures across the four assessment points, there were 11 children (9%) with consistent behavior problems and 60 children (51%) with consistently good adjustment. Of the 47 children (40%) who changed classification over time, 15 (13%) changed from good to poor adjustment, 17 (14%) changed from poor to good adjustment, 10 (8%) changed from good to poor to good adjustment, and 5 (4%) changed from poor to good to poor adjustment. The risk of consistent behavior problems (with 95% confidence interval in brackets) was significantly increased with a higher baseline level of family conflict (odds ratio [OR] = 1.05 [1.01, 1.08]) and significantly decreased with a higher baseline full-scale IQ (OR = 0.92 [0.87, 0.98]). To evaluate the possibility that baseline full-scale IQ moderated the effect of family conflict on risk for behavior problems, the interaction term was added to the logistic regression but was not significant (p > .05). The risk of behavior problems was not significantly related to MRI classification, gender, education level of the mother, or age of the child.
Hypothesis 4, that changes in behavior problems would be related to changes in family functioning but not neurocognitive functioning, was assessed overall and for MRI and phenotype subgroups using the mixed model approach previously described for hypotheses 1 and 2. Change in total behavior problem score was not significantly related with change in IQ but was related with change in family functioning such that total behavior problem score increased .14 (95% confidence interval; .12, .16) units for every unit increase of conflicted factor score.
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Discussion |
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TopAbstractIntroductionMethodResultsDiscussionReferences |
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The major hypotheses, formulated on the basis of the previous cross-sectional study (Thompson et al., 1999
,Thompson et al.,
1999), were supported in this longitudinal study of children with
SCD. More specifically, intellectual functioning declined overall, and more
substantially in subgroups with silent infarct and stroke, but there were no
significant changes over time in mother-reported behavior problems or family
functioning. The rate of classification of behavior problems, based on
mother-report, remained consistent across at least three assessment points for
60% of the children. These findings of moderate consistency in mother-reported
behavior problems are comparable to the findings in other studies of children
with SCD and other chronic childhood illnesses
(Thompson & Gustafson,
1996; Thompson, Gustafson, et
al., 1999). Of particular importance is the finding that only 9%
of the children had consistently reported behavior problems, compared to 51%
with consistently good adjustment. It has been argued previously that the
subgroup of children with consistent behavioral and adjustment problems in
particular needs to be identified for intervention
(Thompson & Gustafson,
1996).
Consistently poor adjustment was related to higher baseline levels of
family functioning, and more specifically family conflict. Moreover, changes
in mother-reported behavior problems were directly related to changes in
maternal appraisals of family conflict. These findings suggest that family
conflict serves as a risk factor for behavior problems. Thus, further support
is provided for the suggestion, stemming from the initial cross-sectional
study (Thompson, Armstrong, et al.,
1999), that family functioning is a salient target for fostering
the adaptation of children to SCD. However, given the possible
bidirectionality of the association of family conflict and maternal report of
child behavior problems, the next step is to undertake experimental research
to confirm the role of family functioning in adaptation to SCD through
intervention studies that seek to reduce family conflict and increase
organization and support. Contrary to the hypotheses, based on the findings of
the initial cross-sectional study
(Thompson, Armstrong, et al.,
1999), that consistently poor adjustment would be unrelated to
neurocognitive functioning, the findings of this longitudinal study indicate
that the risk of behavior problems significantly decreased with higher initial
level of intellectual functioning. This finding is consistent with the
findings in a study of children with cerebral palsy, orthopedic problems, and
seizure disorders and healthy controls that parents and teachers rated those
with higher intelligence quotients as better adjusted
(Perrin et al., 1993).
The strengths of this study relate to the multisite, prospective,
longitudinal design with concurrent medical, MRI, neurocognitive, and
behavioral assessment. The major contributions of this study are the
association of family functioning and intellectual functioning with
mother-reported adjustment of children with SCD and the linkage of changes in
mother-reported behavior problems with changes in family conflict. There are,
however, several important limitations of the study. These include the
well-recognized problems of reliance on maternal report as the sole measure of
children's behavior problems (Thompson
& Gustafson, 1996), whereas multiple reports are desirable,
and shared method variance in mother-report of behavior problems and family
functioning. Also, given the sample size, the logistic regression model may be
overfitting the data. The necessity of changing from the WISC-R to the
WISC-III midway through the study was a complication, but not a substantive
one, because the differences that occurred as a function of different measures
were accounted for in the data analysis. In addition, this study did not
examine the relationship of behavior problems with other symptoms of SCD
unrelated to brain impairment or with other socioecological dimensions such as
coping skills. For example, the importance of pain coping strategies to
adjustment is well established (Gil, Williams, Thompson, & Kinney, 1991).
Inclusion of additional biomedical and socioecological parameters in future
studies would enable the identification of resiliency, as well as risk
factors, which, in turn, would provide a more comprehensive basis for the
formulation of interventions to promote adaptive child and family functioning
in the face of the stresses associated with SCD.
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Acknowledgments |
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This work was supported by the Division of Blood Diseases and Resources of the National Heart, Lung, and Blood Institute of the National Institutes of Health. Senior Investigators from the Cooperative Study of Sickle Cell Disease: K. Frempong, J. Radcliffe, Children's Hospital (Philadelphia); G. Bray, M. McCabe, Children's Hospital National Medical Center (Washington, DC); E. Vichinsky, C. Johnson, Children's Hospital (Oakland, CA); T. Kinney, R. Thompson, Duke University (Durham, NC); J. Smith, Y. Khakoo, T. Schile, Harlem Hospital (New York); O. Castro, C. Uy-Lee, S. Wilson, Howard University (Washington, DC); L. Guarini, J. Sambursky, W. Lebowitz, Interfaith Medical Center (Brooklyn, NY); W. Wang, J. Wilimas, R. Mulhurn, B. Smith, St. Jude's Children's Research Hospital (Memphis, TN); S. Miller, M. Browman, State University of New York Health Science Center at Brooklyn (Brooklyn, NY); D. Wethers, R. Grover, L. Susan Branche, St. Luke's-Roosevelt Medical Center (New York); M. Koshy, N. Talishy, A. Hurtig, University of Illinois (Chicago); C. Pegelow, F. D. Armstrong, University of Miami (Miami, FL): M. DeBaun, J. Marnett, C. Tershak, Washington University (St. Louis, MO); U. Subramanian, F. Zelco, Wyler Children's Hospital (Chicago); H. Pearson, D. Scott, Yale University (New Haven, CT). Statistical Coordinating Center: S. McKinlay, O. Platt, D. Gallagher, L. Sleeper, New England Research Institutes (Watertown, MA). Program Administration: C. Reid, D. Bonds, M. Waclawiw, National Heart, Lung, and Blood Institute (Bethesda, MD). We thank George Reed, PhD, for initial statistical analyses of these data.
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Notes |
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This paper was reviewed and accepted during the term of the previous editor, Anne E. Kazak, PhD, ABPP
Received May 25, 2001; revision received October 24, 2001; revision received March 1, 2002; accepted March 27, 2002
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