DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY
ORIGINAL ARTICLE
Everyday psychological functioning in children with unilateral cerebral palsy: does executive functioning play a role? KOA WHITTINGHAM 1,2
| HARRIET L BODIMEADE 1,2 | OWEN LLOYD 3 | ROSLYN N BOYD 1
1 Queensland Cerebral Palsy and Rehabilitation Research Centre, Discipline of Paediatrics and Child Health, School of Medicine, The University of Queensland, Brisbane, Qld; 2 School of Psychology, Faculty of Social and Behavioural Sciences, The University of Queensland, Brisbane, Qld; 3 Queensland Paediatric Rehabilitation Service, Royal Children’s Hospital, Herston, Brisbane, Qld, Australia. Correspondence to Koa Whittingham, Queensland Cerebral Palsy and Rehabilitation Research Centre Level 7, Block 6, Royal Brisbane & Women’s Hospital, Herston, Brisbane, Qld 4029, Australia. E-mail: [email protected]
PUBLICATION DATA
Accepted for publication 10th November 2013. Published online 7th January 2014. ABBREVIATIONS
BRIEF SDQ CTD
Behavior Rating Inventory of Executive Function Strengths and Difficulties Questionnaire Children with typical development
AIM To identify whether executive functioning mediates the effect of having unilateral cerebral palsy (CP) on executive functioning in everyday life, psychological functioning, and social functioning. METHOD A cross-sectional cohort of 46 children with unilateral CP (25 males, 21 females; mean age 11y 1mo, SD 2y 5mo; 24 right-sided, 22 left-sided) and 20 children with typical development (nine males, 11 females; mean age 10y 10mo, SD 2y 4mo). Cognitive executive functioning was tested using a neuropsychological battery. Executive functioning in everyday life was measured with the Behavior Rating Inventory of Executive Function (BRIEF; teacher and parent reports) and psychological and social functioning by the Strengths and Difficulties Questionnaire (SDQ). Analysis included analysis of covariance and bootstrapping. RESULTS Children with unilateral CP were found to have significantly decreased functioning, compared with children with typical development, on the BRIEF Behavioral Regulation Index, the BRIEF Metacognition Index, and on the SDQ emotion, conduct, hyperactivity, and peer problems subscales. Group differences were mediated by cognitive executive functioning for the BRIEF Metacognition Index (teacher and parent report), the BRIEF Behavioral Regulation Index (parent report only), the SDQ conduct subscale, and the SDQ hyperactivity subscale. INTERPRETATION This study suggests that the increased risk of children with unilateral CP experiencing executive functioning difficulties in everyday life, conduct problems, and hyperactivity can be partly explained by decreased cognitive executive functioning abilities relative to children with typical development.
Unilateral cerebral palsy (CP) is the most common type of CP among children born at term and the second most common type in children born preterm, with an incidence of one in 1300 live births.1,2 Researchers and clinicians are becoming increasingly aware that, in addition to the hallmark motor impairments, CP often involves cognitive deficits,3 emotional and behavioural difficulties,4 and social difficulties.4,5 In fact, a recent meta-analysis showed that one in four children with CP have a behavioural disorder6,7 compared with one in 10 children with typical development (CTD).8 Children with CP are also at an increased risk of impaired social development, with as many as seven in 10 preschool children with CP showing significant delay in social milestones relative to community norms and evidence of continued social difficulties at school age.4,5 Improved understanding of why children with CP are vulnerable to behavioural and social difficulties may lead to effective interventions. General cognitive functioning (IQ), was found to be the strongest predictor of psychiatric problems in a 572 DOI: 10.1111/dmcn.12374
cross-sectional study of 428 children with unilateral CP.7 One possible explanation is that the behavioural and social functioning of children with CP is affected by cognitive deficits in executive functioning, because among children with an early brain injury (as is the case in unilateral CP) IQ and executive functioning are highly correlated.9–11 ‘Executive functioning’ is a broad term that encompasses the skills necessary for novel, goal-directed, and complex activity including the following: abstract thinking; problem solving; initiating, monitoring, sustaining and shifting behaviour; organization; planning; mental flexibility; goal selection; self-control and regulation; and use of feedback; and metacognition.12 Everyday functioning relies on executive functioning. Executive functioning underpins an individual’s ability to acquire new skills, apply newly learnt information and skills to the world, and develop functional independence. Impairments in executive functioning have been found in a range of neurodevelopmental disorders, including Asperger syndrome and non-verbal learning disorder,13,14 attention-deficit disorder,14,15 myelomeningocele © 2014 Mac Keith Press
and hydrocephalus,16 fetal alcohol syndrome disorders,17 and traumatic brain injury.18 Children with unilateral CP show global executive functioning deficits across all domains of executive functioning.9,10 Deficits in cognitive executive functioning, as identified by structured neuropsychological assessments, may also be apparent in everyday life, manifesting as disorganization and poor planning, inability to focus and attend to tasks, disinhibition, perseveration, or a careless response style to tasks, impulsivity, increased errors without subsequent selfcorrection, taking longer to complete tasks, and inflexible thinking and behavioural patterns.12 As well as being important for cognitive functioning, executive skills are involved in emotional responses, behavioural actions, and social skills.12,19,20 Yet, there is a paucity of research investigating the impact of cognitive executive functioning deficits on children with unilateral CP on everyday executive functioning. The increased risk of children with CP for behavioural disorders and social difficulties may be partly explained by cognitive executive functioning deficits. However, we could find no research investigating if this is, in fact, the case. The aim of the present study was to identify whether cognitive executive functioning, as measured by neuropsychological assessment, mediates the effect of having unilateral CP on the behavioural manifestations of executive functioning in everyday life, psychological functioning, and social functioning. We hypothesized that the increased risk of children with unilateral CP having behavioural and social difficulties, and impairments in everyday executive functioning skills, is partly explained by cognitive executive functioning deficits.
METHOD Participants Methods for this study are reported in depth in the study protocol.21 The study forms part of a larger study examining executive functioning in children with unilateral CP, with a previous paper identifying a global executive functioning deficit.10 Institutional ethics approval was obtained from the School of Psychology Ethics Committee at the University of Queensland, Brisbane, (10-PSYCH-DCP-32-JM) and from the Queensland Children’s Health Services Human Research Ethics Committee, Brisbane, Australia (HREC/ 10/QRCH/31). Participants were a prospective group of children aged 8 to 16 years divided across two clinical groups: (1) children with unilateral CP (both left- and rightsided) and (2) a group consisting of CTD. A sample size of 21 in each of the three groups (i.e. left unilateral CP, right unilateral CP, and CTD) was calculated to have at least 80% power of detecting a large effect size using an analysis of covariance (ANCOVA) with three comparison groups.22 Group with unilateral CP Children were included if they had a diagnosis of unilateral CP, could follow instructions, and had English as their first language. Children were ineligible if they had an
• • •
What this paper adds Executive functioning predicts psychological and social functioning in children with unilateral CP. Children with unilateral CP are at increased risk of everyday executive functioning difficulties, conduct problems, and hyperactivity. This increased risk is partly explained by a cognitive executive functioning deficit.
uncontrolled seizure disorder. They were identified from a research database of children born in Queensland attending state-wide CP health services as described in the Australian CP Child Study protocol23 and in the protocol for this study.21 Identification of children for inclusion in the research database followed the guidelines of the Surveillance of Cerebral Palsy in Europe24 and used a working definition of CP as a motor impairment stemming from an early, non-progressive brain lesion.25
Group with typical development Children were either typically developing siblings or friends of children from the unilateral CP group. Children were ineligible if English was not their first language or if they had a history of developmental, neurological, physical, or psychiatric conditions. CTD (age and sex matched) were recruited as a reference sample. Siblings and friends of children with unilateral CP were invited to take part in the study, as well as recruitment through staff newsletters and from other studies within the centre. A trainee psychologist conducted a brief telephone screen-interview to ensure the children met the criteria for study selection. Design and procedure A cross-sectional design with three groups was used: (1) children with right unilateral CP; (2) children with left unilateral CP; and (3) CTD who were matched for age and sex. Background measures All parents completed a demographic questionnaire. Children’s motor functioning was classified using the Gross Motor Function Classification System (GMFCS)26 and manual ability using the Manual Ability Classification System (MACS).27 Cognitive executive functioning measures A neuropsychological battery was developed that included the Rey Complex Figure Test28 and subtests from the Delis–Kaplan Executive Function System,29 Test of Everyday Attention for Children,30 and the Wechsler Intelligence Scale for Children (4th edition).31 A full description of the battery has been published in the study protocol,21 and detailed comparisons between children with unilateral CP and CTD on each component of executive functioning have been published.10 In this paper, a composite executive functioning measure was used, created by standardizing and averaging all measures. The use of a global executive functioning composite is appropriate in this sample
Cognitive Executive Functioning and Everyday Functioning Koa Whittingham et al.
573
because children with unilateral CP demonstrated a global executive functioning deficit compared with CTD.10 Further, all measures of executive functioning were highly intercorrelated in this sample and the composite executive functioning measure had excellent internal consistency (a=0.93). Analysing every component of executive functioning as a potential mediator was impractical and would have required a much larger sample size. All children completed the assessments using their unimpaired hand.
Psychological and everyday functioning measures Psychological and social functioning was measured by parent report on the Strengths and Difficulties Questionnaire (SDQ).32 Executive functioning performance in everyday life was measured by parent and teacher report on the Behaviour Rating Inventory of Executive Function (BRIEF).19 A full description of each measure for this study, including psychometrics, has previously been published.21 For this paper, the BRIEF index scores and the SDQ subscales were used. The BRIEF produces two index scores: the Behavioral Regulation Index (including initiate, working memory, plan/organize, organization of materials, and monitor) and the Metacognition Index (including inhibit, shift, and emotional control). The SDQ produces five subscales (emotional symptoms, conduct problems, inattention/hyperactivity, peer problems, and prosocial behaviour), with higher scores indicating poorer functioning on all except the prosocial subscale. Statistical analyses Between-group differences, in terms of executive functioning in everyday life and psychological and social functioning, were examined by a series of ANCOVAs controlling for age. Significant between-groups differences were followed up with a priori linear contrasts, comparing the CTD with all children with unilateral CP and comparing participants with left and right unilateral CP. Bootstrapping (with 5000 re-samples) was used to determine whether cognitive executive functioning (as measured by the executive functioning composite) mediated the effects
of group (CTD, left unilateral CP, right unilateral CP) on behavioural manifestations of executive functioning in everyday life and psychological and social functioning. Bootstrapping is a nonparametric statistical technique that can be applied to mediation analysis to test and quantify the effect of the independent variable on the dependent variable as mediated by the tested mediator. This is referred to as the indirect effect; the total effect of the independent variable on the dependent variable is referred to as the total effect.33 The latest techniques allow for the use of bootstrapping when the independent variable is a multicategorical grouping, such as in this analysis, through indicator or dummy coding.34 Within this analysis, dummy coding was performed such that the CTD group functioned as the reference category.
RESULTS A total of 188 children and adolescents diagnosed with unilateral CP were assessed for eligibility from the Queensland Cerebral Palsy and Rehabilitation Research Centre database, with 46 children and adolescents (25 males, 21 females; mean age 11y 1mo SD 2y 5mo) 24 with right handed and 22 with left handed unilateral CP selected to take part along with 20 CTD (nine males, 11 females; mean age 10y 10mo SD 2y 4mo; Fig 1). Demographic information Overall, 12 of children with unilateral CP had some form of learning disorder compared with none of the CTD (v2[2]=7.1, p=0.029). Children with unilateral CP were more likely to have visual difficulties (33%) than CTD (0%) (v2[2]=9.17, p=0.01) and were more likely to be living in single-parent families or with a step-parent than CTD (v2[6]=16.76, p=0.033; Table I). The children with unilateral CP were predominantly in GMFCS level I, walking independently without a gait aid and not requiring a handrail with stairs, and were predominantly in MACS level II for manual ability, indicating they were able to handle most objects but with somewhat reduced quality and/or speed of achievement.
CTD Participants
Unilateral CP Participants Assessed for eligibility (n=188)
Did not meet criteria (n=112)
Assessed for eligibility (n=21)
Attended screening assessment (n=76)
Declined (n=36) Did not want to miss school (n=28) Too far to travel (n=8)
Attended screening assessment (n=21)
Enrolled in study (n=46)
Analyses (n=46)
Declined (n=1) ADHD diagnosis
Enrolled in study (n=20)
Analyses (n=20)
Figure 1: Study flow chart. CP, cerebral palsy; CTD, children with typical development; ADHD, attention-deficit–hyperactivity disorder. 574 Developmental Medicine & Child Neurology 2014, 56: 572–579
Table I: Participant characteristics
Characteristics
Right unilateral CP (n=22)
Left unilateral CP (n=24)
Age, mean, (SD) y 11.09 (2.54) 11.08 Sex, n (%) Male 12 (55) 13 Female 10 (45) 11 GMFCS, n (%) Level I 14 (64) 21 Level II 8 (36) 3 MACS, n (%) Level I 1 (5) 5 Level II 21 (95) 19 Handedness, n (%) Right 0 (0) 24 Left 21 (95) 0 Ambidextrous 1 (5) 0 Intellectual functioning, mean (SD) Full-scale IQ 84.95 (14.65) 86.75 Verbal IQ 87.23 (16.14) 91.12 Performance IQ 85.18 (13.45) 84.96 Ethnicity, n (%) Caucasian 21 (95) 22 Australian New Zealand 0 (0) 1 Maori Lebanese 0 (0) 1 Australian Chinese Australian 1 (5) 0 Other diagnoses, n (%) Seizure disorder 3 (14) 4 (controlled) Learning disorder 6 (27) 7 Hearing impairment 1 (5) 3 (corrected) Vision impairment 6 (27) 9 (corrected) 3 (14) 3 Attention-deficit– hyperactivity disorder Autistic spectrum 2 (19) 3 disorder Anxiety disorder 1 (5) 0 Perthes disease 1 (5) 0 Medication use, n (%) Yes 7 (32) 4 No 15 (68) 20 Gross household income, n (%) Under $25 000 1 (5) 2 $25 000–50 000 3 (14) 3 $50 000–75 000 4 (19) 4 $75 000–100 000 5 (24) 8 Over $100 000 8 (38) 6 Family type in which child living, n (%) Original 13 (59) 15 Step-family 7 (32) 2 Sole parent 1 (5) 6 Joint custody 0 (0) 0 Parental marital status, n (%) Married 17 (77) 17 Single 1 (5) 4 De facto 4 (18) 0 Divorced/separated 0 (0) 3
(2.38) (54) (46)
CTD (n=20) 10.8 (2.29) 9 (45) 11 (55)
(88) (13)
n/a n/a
(21) (79)
n/a n/a
(100) (0) (0) (17.96) (20.83) (15.03)
17 (85) 3 (15) 0 (0) 116.5 (10.7) 118.25 (15.41) 111.25 (11.29)
(92)
20 (100)
(4)
0 (0)
(4)
0 (0)
(0)
0 (0)
(17)
0 (0)
(29) (13)
0 (0) 0 (0)
(38)
0 (0)
(13)
0 (0)
(13)
0 (0)
(0) (0)
0 (0) 0 (0)
(17) (83)
0 (0) 20 (100)
(9) (13) (17) (35) (26)
0 2 2 3 11
(0) (11) (11) (16) (63)
(63) (8) (25) (0)
18 1 1 0
(90) (5) (5) (0)
(77) (17) (0) (13)
19 0 0 1
(95) (0) (0) (5)
CP, cerebral palsy; CTD, children with typical development; GMFCS, Gross Motor Function Classification System; MACS, Manual Ability Classification System.
Preliminary analyses Small proportions of randomly missing data due to colour blindness and non-compliance were managed with pairwise
analyses. Analysis with outliers removed and cases Winsorized at the 95th centile did not change interpretation; thus the cases were retained for the main analysis. Several measures showed significant skew within groups. Again, results did not differ because of the transformation so untransformed data are presented.
Main analyses Between-group differences in everyday life, psychological functioning, and social functioning Analyses revealed that children with unilateral CP differed from CTD: they had significantly higher scores, indicative of greater levels of executive dysfunction in everyday life, on the parent-rated (F1,59=19.18, p
ORIGINAL ARTICLE
Everyday psychological functioning in children with unilateral cerebral palsy: does executive functioning play a role? KOA WHITTINGHAM 1,2
| HARRIET L BODIMEADE 1,2 | OWEN LLOYD 3 | ROSLYN N BOYD 1
1 Queensland Cerebral Palsy and Rehabilitation Research Centre, Discipline of Paediatrics and Child Health, School of Medicine, The University of Queensland, Brisbane, Qld; 2 School of Psychology, Faculty of Social and Behavioural Sciences, The University of Queensland, Brisbane, Qld; 3 Queensland Paediatric Rehabilitation Service, Royal Children’s Hospital, Herston, Brisbane, Qld, Australia. Correspondence to Koa Whittingham, Queensland Cerebral Palsy and Rehabilitation Research Centre Level 7, Block 6, Royal Brisbane & Women’s Hospital, Herston, Brisbane, Qld 4029, Australia. E-mail: [email protected]
PUBLICATION DATA
Accepted for publication 10th November 2013. Published online 7th January 2014. ABBREVIATIONS
BRIEF SDQ CTD
Behavior Rating Inventory of Executive Function Strengths and Difficulties Questionnaire Children with typical development
AIM To identify whether executive functioning mediates the effect of having unilateral cerebral palsy (CP) on executive functioning in everyday life, psychological functioning, and social functioning. METHOD A cross-sectional cohort of 46 children with unilateral CP (25 males, 21 females; mean age 11y 1mo, SD 2y 5mo; 24 right-sided, 22 left-sided) and 20 children with typical development (nine males, 11 females; mean age 10y 10mo, SD 2y 4mo). Cognitive executive functioning was tested using a neuropsychological battery. Executive functioning in everyday life was measured with the Behavior Rating Inventory of Executive Function (BRIEF; teacher and parent reports) and psychological and social functioning by the Strengths and Difficulties Questionnaire (SDQ). Analysis included analysis of covariance and bootstrapping. RESULTS Children with unilateral CP were found to have significantly decreased functioning, compared with children with typical development, on the BRIEF Behavioral Regulation Index, the BRIEF Metacognition Index, and on the SDQ emotion, conduct, hyperactivity, and peer problems subscales. Group differences were mediated by cognitive executive functioning for the BRIEF Metacognition Index (teacher and parent report), the BRIEF Behavioral Regulation Index (parent report only), the SDQ conduct subscale, and the SDQ hyperactivity subscale. INTERPRETATION This study suggests that the increased risk of children with unilateral CP experiencing executive functioning difficulties in everyday life, conduct problems, and hyperactivity can be partly explained by decreased cognitive executive functioning abilities relative to children with typical development.
Unilateral cerebral palsy (CP) is the most common type of CP among children born at term and the second most common type in children born preterm, with an incidence of one in 1300 live births.1,2 Researchers and clinicians are becoming increasingly aware that, in addition to the hallmark motor impairments, CP often involves cognitive deficits,3 emotional and behavioural difficulties,4 and social difficulties.4,5 In fact, a recent meta-analysis showed that one in four children with CP have a behavioural disorder6,7 compared with one in 10 children with typical development (CTD).8 Children with CP are also at an increased risk of impaired social development, with as many as seven in 10 preschool children with CP showing significant delay in social milestones relative to community norms and evidence of continued social difficulties at school age.4,5 Improved understanding of why children with CP are vulnerable to behavioural and social difficulties may lead to effective interventions. General cognitive functioning (IQ), was found to be the strongest predictor of psychiatric problems in a 572 DOI: 10.1111/dmcn.12374
cross-sectional study of 428 children with unilateral CP.7 One possible explanation is that the behavioural and social functioning of children with CP is affected by cognitive deficits in executive functioning, because among children with an early brain injury (as is the case in unilateral CP) IQ and executive functioning are highly correlated.9–11 ‘Executive functioning’ is a broad term that encompasses the skills necessary for novel, goal-directed, and complex activity including the following: abstract thinking; problem solving; initiating, monitoring, sustaining and shifting behaviour; organization; planning; mental flexibility; goal selection; self-control and regulation; and use of feedback; and metacognition.12 Everyday functioning relies on executive functioning. Executive functioning underpins an individual’s ability to acquire new skills, apply newly learnt information and skills to the world, and develop functional independence. Impairments in executive functioning have been found in a range of neurodevelopmental disorders, including Asperger syndrome and non-verbal learning disorder,13,14 attention-deficit disorder,14,15 myelomeningocele © 2014 Mac Keith Press
and hydrocephalus,16 fetal alcohol syndrome disorders,17 and traumatic brain injury.18 Children with unilateral CP show global executive functioning deficits across all domains of executive functioning.9,10 Deficits in cognitive executive functioning, as identified by structured neuropsychological assessments, may also be apparent in everyday life, manifesting as disorganization and poor planning, inability to focus and attend to tasks, disinhibition, perseveration, or a careless response style to tasks, impulsivity, increased errors without subsequent selfcorrection, taking longer to complete tasks, and inflexible thinking and behavioural patterns.12 As well as being important for cognitive functioning, executive skills are involved in emotional responses, behavioural actions, and social skills.12,19,20 Yet, there is a paucity of research investigating the impact of cognitive executive functioning deficits on children with unilateral CP on everyday executive functioning. The increased risk of children with CP for behavioural disorders and social difficulties may be partly explained by cognitive executive functioning deficits. However, we could find no research investigating if this is, in fact, the case. The aim of the present study was to identify whether cognitive executive functioning, as measured by neuropsychological assessment, mediates the effect of having unilateral CP on the behavioural manifestations of executive functioning in everyday life, psychological functioning, and social functioning. We hypothesized that the increased risk of children with unilateral CP having behavioural and social difficulties, and impairments in everyday executive functioning skills, is partly explained by cognitive executive functioning deficits.
METHOD Participants Methods for this study are reported in depth in the study protocol.21 The study forms part of a larger study examining executive functioning in children with unilateral CP, with a previous paper identifying a global executive functioning deficit.10 Institutional ethics approval was obtained from the School of Psychology Ethics Committee at the University of Queensland, Brisbane, (10-PSYCH-DCP-32-JM) and from the Queensland Children’s Health Services Human Research Ethics Committee, Brisbane, Australia (HREC/ 10/QRCH/31). Participants were a prospective group of children aged 8 to 16 years divided across two clinical groups: (1) children with unilateral CP (both left- and rightsided) and (2) a group consisting of CTD. A sample size of 21 in each of the three groups (i.e. left unilateral CP, right unilateral CP, and CTD) was calculated to have at least 80% power of detecting a large effect size using an analysis of covariance (ANCOVA) with three comparison groups.22 Group with unilateral CP Children were included if they had a diagnosis of unilateral CP, could follow instructions, and had English as their first language. Children were ineligible if they had an
• • •
What this paper adds Executive functioning predicts psychological and social functioning in children with unilateral CP. Children with unilateral CP are at increased risk of everyday executive functioning difficulties, conduct problems, and hyperactivity. This increased risk is partly explained by a cognitive executive functioning deficit.
uncontrolled seizure disorder. They were identified from a research database of children born in Queensland attending state-wide CP health services as described in the Australian CP Child Study protocol23 and in the protocol for this study.21 Identification of children for inclusion in the research database followed the guidelines of the Surveillance of Cerebral Palsy in Europe24 and used a working definition of CP as a motor impairment stemming from an early, non-progressive brain lesion.25
Group with typical development Children were either typically developing siblings or friends of children from the unilateral CP group. Children were ineligible if English was not their first language or if they had a history of developmental, neurological, physical, or psychiatric conditions. CTD (age and sex matched) were recruited as a reference sample. Siblings and friends of children with unilateral CP were invited to take part in the study, as well as recruitment through staff newsletters and from other studies within the centre. A trainee psychologist conducted a brief telephone screen-interview to ensure the children met the criteria for study selection. Design and procedure A cross-sectional design with three groups was used: (1) children with right unilateral CP; (2) children with left unilateral CP; and (3) CTD who were matched for age and sex. Background measures All parents completed a demographic questionnaire. Children’s motor functioning was classified using the Gross Motor Function Classification System (GMFCS)26 and manual ability using the Manual Ability Classification System (MACS).27 Cognitive executive functioning measures A neuropsychological battery was developed that included the Rey Complex Figure Test28 and subtests from the Delis–Kaplan Executive Function System,29 Test of Everyday Attention for Children,30 and the Wechsler Intelligence Scale for Children (4th edition).31 A full description of the battery has been published in the study protocol,21 and detailed comparisons between children with unilateral CP and CTD on each component of executive functioning have been published.10 In this paper, a composite executive functioning measure was used, created by standardizing and averaging all measures. The use of a global executive functioning composite is appropriate in this sample
Cognitive Executive Functioning and Everyday Functioning Koa Whittingham et al.
573
because children with unilateral CP demonstrated a global executive functioning deficit compared with CTD.10 Further, all measures of executive functioning were highly intercorrelated in this sample and the composite executive functioning measure had excellent internal consistency (a=0.93). Analysing every component of executive functioning as a potential mediator was impractical and would have required a much larger sample size. All children completed the assessments using their unimpaired hand.
Psychological and everyday functioning measures Psychological and social functioning was measured by parent report on the Strengths and Difficulties Questionnaire (SDQ).32 Executive functioning performance in everyday life was measured by parent and teacher report on the Behaviour Rating Inventory of Executive Function (BRIEF).19 A full description of each measure for this study, including psychometrics, has previously been published.21 For this paper, the BRIEF index scores and the SDQ subscales were used. The BRIEF produces two index scores: the Behavioral Regulation Index (including initiate, working memory, plan/organize, organization of materials, and monitor) and the Metacognition Index (including inhibit, shift, and emotional control). The SDQ produces five subscales (emotional symptoms, conduct problems, inattention/hyperactivity, peer problems, and prosocial behaviour), with higher scores indicating poorer functioning on all except the prosocial subscale. Statistical analyses Between-group differences, in terms of executive functioning in everyday life and psychological and social functioning, were examined by a series of ANCOVAs controlling for age. Significant between-groups differences were followed up with a priori linear contrasts, comparing the CTD with all children with unilateral CP and comparing participants with left and right unilateral CP. Bootstrapping (with 5000 re-samples) was used to determine whether cognitive executive functioning (as measured by the executive functioning composite) mediated the effects
of group (CTD, left unilateral CP, right unilateral CP) on behavioural manifestations of executive functioning in everyday life and psychological and social functioning. Bootstrapping is a nonparametric statistical technique that can be applied to mediation analysis to test and quantify the effect of the independent variable on the dependent variable as mediated by the tested mediator. This is referred to as the indirect effect; the total effect of the independent variable on the dependent variable is referred to as the total effect.33 The latest techniques allow for the use of bootstrapping when the independent variable is a multicategorical grouping, such as in this analysis, through indicator or dummy coding.34 Within this analysis, dummy coding was performed such that the CTD group functioned as the reference category.
RESULTS A total of 188 children and adolescents diagnosed with unilateral CP were assessed for eligibility from the Queensland Cerebral Palsy and Rehabilitation Research Centre database, with 46 children and adolescents (25 males, 21 females; mean age 11y 1mo SD 2y 5mo) 24 with right handed and 22 with left handed unilateral CP selected to take part along with 20 CTD (nine males, 11 females; mean age 10y 10mo SD 2y 4mo; Fig 1). Demographic information Overall, 12 of children with unilateral CP had some form of learning disorder compared with none of the CTD (v2[2]=7.1, p=0.029). Children with unilateral CP were more likely to have visual difficulties (33%) than CTD (0%) (v2[2]=9.17, p=0.01) and were more likely to be living in single-parent families or with a step-parent than CTD (v2[6]=16.76, p=0.033; Table I). The children with unilateral CP were predominantly in GMFCS level I, walking independently without a gait aid and not requiring a handrail with stairs, and were predominantly in MACS level II for manual ability, indicating they were able to handle most objects but with somewhat reduced quality and/or speed of achievement.
CTD Participants
Unilateral CP Participants Assessed for eligibility (n=188)
Did not meet criteria (n=112)
Assessed for eligibility (n=21)
Attended screening assessment (n=76)
Declined (n=36) Did not want to miss school (n=28) Too far to travel (n=8)
Attended screening assessment (n=21)
Enrolled in study (n=46)
Analyses (n=46)
Declined (n=1) ADHD diagnosis
Enrolled in study (n=20)
Analyses (n=20)
Figure 1: Study flow chart. CP, cerebral palsy; CTD, children with typical development; ADHD, attention-deficit–hyperactivity disorder. 574 Developmental Medicine & Child Neurology 2014, 56: 572–579
Table I: Participant characteristics
Characteristics
Right unilateral CP (n=22)
Left unilateral CP (n=24)
Age, mean, (SD) y 11.09 (2.54) 11.08 Sex, n (%) Male 12 (55) 13 Female 10 (45) 11 GMFCS, n (%) Level I 14 (64) 21 Level II 8 (36) 3 MACS, n (%) Level I 1 (5) 5 Level II 21 (95) 19 Handedness, n (%) Right 0 (0) 24 Left 21 (95) 0 Ambidextrous 1 (5) 0 Intellectual functioning, mean (SD) Full-scale IQ 84.95 (14.65) 86.75 Verbal IQ 87.23 (16.14) 91.12 Performance IQ 85.18 (13.45) 84.96 Ethnicity, n (%) Caucasian 21 (95) 22 Australian New Zealand 0 (0) 1 Maori Lebanese 0 (0) 1 Australian Chinese Australian 1 (5) 0 Other diagnoses, n (%) Seizure disorder 3 (14) 4 (controlled) Learning disorder 6 (27) 7 Hearing impairment 1 (5) 3 (corrected) Vision impairment 6 (27) 9 (corrected) 3 (14) 3 Attention-deficit– hyperactivity disorder Autistic spectrum 2 (19) 3 disorder Anxiety disorder 1 (5) 0 Perthes disease 1 (5) 0 Medication use, n (%) Yes 7 (32) 4 No 15 (68) 20 Gross household income, n (%) Under $25 000 1 (5) 2 $25 000–50 000 3 (14) 3 $50 000–75 000 4 (19) 4 $75 000–100 000 5 (24) 8 Over $100 000 8 (38) 6 Family type in which child living, n (%) Original 13 (59) 15 Step-family 7 (32) 2 Sole parent 1 (5) 6 Joint custody 0 (0) 0 Parental marital status, n (%) Married 17 (77) 17 Single 1 (5) 4 De facto 4 (18) 0 Divorced/separated 0 (0) 3
(2.38) (54) (46)
CTD (n=20) 10.8 (2.29) 9 (45) 11 (55)
(88) (13)
n/a n/a
(21) (79)
n/a n/a
(100) (0) (0) (17.96) (20.83) (15.03)
17 (85) 3 (15) 0 (0) 116.5 (10.7) 118.25 (15.41) 111.25 (11.29)
(92)
20 (100)
(4)
0 (0)
(4)
0 (0)
(0)
0 (0)
(17)
0 (0)
(29) (13)
0 (0) 0 (0)
(38)
0 (0)
(13)
0 (0)
(13)
0 (0)
(0) (0)
0 (0) 0 (0)
(17) (83)
0 (0) 20 (100)
(9) (13) (17) (35) (26)
0 2 2 3 11
(0) (11) (11) (16) (63)
(63) (8) (25) (0)
18 1 1 0
(90) (5) (5) (0)
(77) (17) (0) (13)
19 0 0 1
(95) (0) (0) (5)
CP, cerebral palsy; CTD, children with typical development; GMFCS, Gross Motor Function Classification System; MACS, Manual Ability Classification System.
Preliminary analyses Small proportions of randomly missing data due to colour blindness and non-compliance were managed with pairwise
analyses. Analysis with outliers removed and cases Winsorized at the 95th centile did not change interpretation; thus the cases were retained for the main analysis. Several measures showed significant skew within groups. Again, results did not differ because of the transformation so untransformed data are presented.
Main analyses Between-group differences in everyday life, psychological functioning, and social functioning Analyses revealed that children with unilateral CP differed from CTD: they had significantly higher scores, indicative of greater levels of executive dysfunction in everyday life, on the parent-rated (F1,59=19.18, p
