ISSN: 1751-8423 (print), 1751-8431 (electronic) Dev Neurorehabil, Early Online: 1–6 ! 2014 Informa UK Ltd. DOI: 10.3109/17518423.2014.916761


Executive functions in preschool children with cerebral palsy – Assessment and early intervention – A pilot study Kristian Sørensen1, Janne Risholm Liverød2, Bjørn Lerdal1, Ida E. Vestrheim1, & Jon Skranes1,3 Child Habilitation Unit, Department of Pediatrics, Sørlandet Hospital HF, Kristiansand, Norway, 2Adult Habilitation Unit, Department of Rehabilitation, Sørlandet Hospital HF, Kristiansand, Norway, and 3Department of Laboratory Medicine, Children’s and Women’s Health, Medical Faculty, Norwegian University of Science and Technology (NTNU), Trondheim, Norway

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Objective: To assess the level of executive functioning among preschool children with cerebral palsy (CP) and evaluate effects of the Program Intensified habilitation (PIH). Methods: In this non-randomized, prospective study, 15 preschool children with CP, and their parents attended the PIH for a 1-year period. Executive functions were evaluated using the Behavior Rating Inventory of Executive functions – Preschool version (BRIEF-P), filled out by parents and preschool teachers. Results: Before PIH, scores of executive function difficulties were close to the general population mean. After PIH, fathers and preschool teachers reported reduced levels of executive difficulties on, respectively, the Emergent Metacognition Index and the Flexibility Index on the BRIEF-P. Mothers reported no changes. Conclusion: The children in our sample showed age-appropriate levels of executive functions before attending PIH. Some aspects of executive skills difficulties were reduced after PIH. Using BRIEF-P contributed to the differentiation of cognitive strengths and weaknesses among the children.

Cerebral palsy, executive functions, intervention, intensive habilitation, preschool children

Introduction Executive functions are the cognitive functions that enable us to plan, solve problems, self-regulate, and flexibly fit into social systems. These functions are located mainly in the prefrontal areas of the brain, and have a developmental trajectory of 20–25 years. At preschool age these brain functions are at an early stage of development [1]. Executive functions in typically developing children evolve through brain maturation and learning experiences during adaptation to rules of behavior in the social world [2]. Preschool children mainly experience this through participation in everyday activities and play. Children with cerebral palsy (CP) are diagnosed on the basis of having a motor problem. In addition, many of these children experience cognitive difficulties including executive function deficits. Communication and language dysfunctions are also common [3]. Visual perception and visual–spatial abilities, attention, and memory are frequently affected and it is estimated that learning problems occur in about half of the children with CP [4, 5]. Pirila et al. [6] found mean IQ scores at the lower end of the normal distribution in a group of children with bilateral spastic CP. White and Christ [7] found disruptions in prefrontally mediated executive aspects of learning and memory among children with bilateral spastic Correspondence: Kristian Sørensen, Child Habilitation Unit, Department of Pediatrics, Sørlandet Hospital HF, Kristiansand, Service Box 416, 4604 Kristiansand, Norway. Tel: +47 38073978. Fax: +47 98404962. E-mail: [email protected]

History Received 2 January 2014 Revised 14 April 2014 Accepted 16 April 2014 Published online 19 May 2014

CP. Related to this, Jenks et al. [8] conclude that children with CP are at risk for deficits in executive functioning and working memory. As executive functions are at an early stage of development in preschool ages, the possibility of strengthening them through structured intervention seems natural to investigate. The Norwegian Knowledge Centre for the Health Services (NOKC) has published a report summarizing and evaluating the effectiveness of both Norwegian and international intensive training programmes for children with congenital or early acquired brain injuries [9]. In conclusion, the report shows that structured intensive intervention programmes carried out by professionals working together, with specific amounts of motor, language, or cognitive stimulation over a period of time and clearly defined goals have a somewhat better effect than ordinary habilitation services, where the child typically would be examined in a hospital setting once a year and the daily stimulation is carried out by different local professionals in different locations. However, few of the reviewed programmes had strengthening of cognitive functions as a defined aim. Cognitive training programmes do, however, exist for other patient groups. Van’t Hooft et al. [10] studied a group of children with traumatic brain injury, attending a broad based cognitive training programme and found encouraging long-term effects on complex tasks of attention and memory. Løhaugen [11] reports improved working memory among adolescents born preterm with extremely low birth weight, after completing a computer-based working memory training programme for 5 weeks. The effect of the

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K. Sørensen et al.

training was maintained at retesting after 6 months. Grunewaldt et al. [12] found that a preschool version of the same computer-based working memory training programme seemed effective in preterm born very low birth weight children at age 5–6 years, not only on working memory tasks but also by having a generalizing effect regarding memory and learning. Both these groups of preterm children included some children with CP. When interpreting research and neuropsychological assessments of preschool children with CP, it is critical to consider the developmental aspect. Bottcher [13] points out the dynamic and reciprocal relationship among neural processes, cognition and child participation, and that brain damage acts as a neurobiological constraint on this entire system. As many brain functions are relatively immature in preschool age, there is also the question of what is really being assessed, and to which degree, the functions are really affected or delayed at a specific point in the child’s brain development. Assessment of executive functions at an early age by traditional neuropsychological testing is also a challenge, as tests are relatively few, norms are uncertain and confounding variables as motivation and confidence in the testing situation might influence the results. Using the Behavior Rating Inventory of Executive Function – Preschool Version (BRIEF-P) [14] is a way of assessing executive functions that reduces the influence of confounding variables. BRIEF-P is a questionnaire for parents and teachers designed to tap information about executive functions in preschool children and its major advantage is the possibility of assessing functionality in everyday life. In Program Intensified Habilitation (PIH) for children with CP at Sørlandet Hospital in Norway, the intervention areas concerning the child are motor functions, communication, and executive functions. PIH is based on the clinical experience in working with groups of children with CP, elements from other training programmes [2, 15–17], central principles of learning [18], and the CanChild family centered concept [19]. Keeping the neurodevelopmental perspective in mind, it is natural to assume that early assessment of executive functions and intervention may prevent some of the cognitive problems children with CP experience [4, 5]. In addition, it should enable parents and professionals to create developmental possibilities that strengthen executive functions. Aims of the present study were to investigate the general level of executive functions in preschool children with spastic cerebral palsy both unilateral (hemiplegic) and bilateral (diplegic) type, when assessed with the BRIEF-P, and to explore whether participation in the PIH programme would enhance the development of executive functions. Our hypothesis is that participation in PIH will strengthen early executive functions in these children.

Methods Design Children with CP were assessed before and after participation in the one year PIH programme, using the BRIEF-P [14]. One or both parents, and one preschool teacher, filled out the BRIEF-P questionnaires. Each child was therefore assessed by two or three persons at two different time points.

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Data collection was carried out during a 5-year period, in a total of four groups of children with CP attending the PIH programme. Participants The inclusion criteria in PIH and the current study are age (2–4 years), CP diagnosis and a referral from the child’s local habilitation service. Fifteen children with CP participated in the study. One child did not complete the training programme and was excluded from the analysis. Of the 14 children that completed the programme, there were seven girls and seven boys (ages from 2 years 2 months to 4 years 9 months at first evaluation, mean age 3 years 3 months). Seven children were diagnosed with unilateral spastic CP (hemiplegic); and seven with bilateral spastic CP (diplegic). Gross Motor Function Classification System level (GMFCS) [20] varied from I to III for the participating children. Children with genetic syndromes, autism spectrum disorder, extensive visual and hearing impairments, or receptive language disorders are excluded from the PIH and the current study. The PIH – Program of Intensified Habilitation The Program of Intensified Habilitation [21] is offered to families with preschool children with CP. The PIH is a multidimensional programme, focusing on family centered cooperation, improving knowledge about the child, goal setting and goal directed working, training and stimulation. Figure 1 shows the annual structure of the PIH programme. During each group session in the habilitation unit in the hospital, the children are given an individual training programme aimed at strengthening motor, communication, and executive functions, based on developmentally appropriate play oriented interventions. The children and their parents live at the hospital for 1 or 2 weeks during the group sessions and local professionals also participate for one or more days. During the periods in between, while children are in their home settings, parents, and local professionals arrange the training based on the interventions agreed upon in the group sessions. Executive functions are stimulated through social dramatic play (role play), activities of daily life and structured activities both in the child’s preschool and at home. Participation in the PIH is covered through the general welfare system in Norway, so the child and both parents can participate free of charge for all 6 weeks and the parents can also have their income refunded. Outcome measure BRIEF-P is a rating form that consists of 63 items and measures the range of executive function in everyday activities in preschool-aged children (age range 2–5 years). It is filled out by parents, teachers, or day-care providers. Results are divided into five clinical scales: inhibit, shift, emotional control, working memory and plan/organize. The clinical scales are then divided into three broad indices: inhibitory self-control (combining scores from the Inhibit and Emotional control scales), flexibility (combining scores from the Shift and Emotional control scales), and emergent metacognition (combining scores from the Working memory and Plan/organize scales). The total score is summarized into

Executive functions in preschool children with cerebral palsy

DOI: 10.3109/17518423.2014.916761


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Figure 1. Overview of the Program Intensified Habilitation (PIH). Table I. T-score mean values (SD) on the BRIEF-P main indices before participation, reported by parents and preschool teachers.

Mothers (n ¼ 14) Fathers (n ¼ 12) Preschool teachers (n ¼ 14)

Inhibitory Self-Control Index

Flexibility Index

Emergent Metacog. Index

Global Executive Composite

48.4 (9.1) 48.7 (9.8) 53.3 (8.7)

49.8 (7.0) 48.8 (9.8) 51.8 (8.6)

50.6 (10.3) 51.0 (12.7) 54.7 (9.5)

49.9 (9.7) 50.0 (11.5) 55.4 (10.6)

Metacog., metacognition.

a Global Executive Composite (GEC). All scores on the clinical scales and the GEC are converted into standardized Tscore (mean ¼ 50, standard deviation ¼ 10). BRIEF-P is the first standardized rating scale designed to specifically measure the range of behavioral manifestations of executive functioning in preschool-aged children [14]. Scores above T-score ¼ 65 (+1.5 SD) on the clinical scales and the GEC of the BRIEF-P are defined as above normal levels of executive functions difficulties. Norwegian age referenced norms do not exist, so the original US age referenced norms are used in this study. The US norms are based on a representative sample of children and their parents and preschool teachers. Clinical samples include children with language disorders, autism spectrum disorders, ADHD, and children born prematurely. Internal consistency reliability is reported to be 0.80–0.95 for the parent sample and 0.90–0.97 for the teacher sample. Test– retest reliability is reported to be 0.78–0.90 for the parent sample and 0.64–0.94 for the teacher sample. Studies show convergent and discriminant validity with measurers of hyperactivity/impulsivity, somatic complaints, inattention, depression, and anxiety [14]. Statistics IBM SPSS Statistics version 16.0 (SPSS Inc, Chicago, IL) for Windows was used for data analysis. Differences in mean values between respondents before the intervention were analyzed using the Mann–Whitney U test. Wilcoxon’s signed rank test was used for evaluating paired data and changes in scores before and after participating in PIH. The significance level chosen was 0.05.

study protocol. The study is registered in Clinical (NCT00202761). Written informed consent was obtained from the participating parents and preschool teachers.

Results The assessment of executive functions before participation in the PIH programme showed a level similar to that reported for the general population of age-matched children [14]. There were no significant differences in index scores among mothers’, fathers’ and teachers’ reports at baseline, i.e., before participation in PIH (Table I). Before participation in the PIH programme, mothers reported more executive function difficulties among children with bilateral spastic type CP than among those with the unilateral type, on the Flexibility Index (FI) and the GEC (Table II). Fathers and preschool teachers’ results did not show any differences between the two CP groups. No gender differences in scores were seen in our study population. Neither did we find any significant correlation between age at assessment or GMFCS level and reported executive function difficulties. The effect analysis in our study was based on the reduction in T-score levels after participating in the PIH programme and the results are shown in Table III. Fathers reported a significant reduction in mean T-score levels on the Emergent Metacognition Index (EMI), while the preschool teachers reported a reduction on the FI of the BRIEF-P. Mothers’ scores did not change significantly from before to after participation in PIH (Table III).

Discussion Ethics The Regional Committee of Medical Ethics and the Data Inspectorate in Southern Norway approved the

The level of reported executive function difficulties seems relatively low in our group of preschool children with CP, as mean scores before participation in the PIH programme were


K. Sørensen et al.

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Table II. Mean (SD) T-score values before participation, based on type of CP. Unilat. spastic CP (n ¼ 7)

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Mothers ISCI FI EMI GEC Fathers ISCI FI EMI GEC Preschool teachers ISCI FI EMI GEC

Bilat. spastic CP (n ¼ 7)


43.1 44.3 45.4 43.7

(6.5) (6.0) (5.8) (5.9)

52.6 54.3 53.7 54.6

(9.6) (3.3) (11.8) (9.6)

9.5 4* 13 8*

46.1 46.1 46.0 45.7

(9.8) (11.8) (12.3) (12.1)

54.3 53.8 59.8 58.0

(3.7) (4.9) (11.6) (7.9)

7 7 6 6

51.1 50.6 52.1 51.1

(9.3) (8.5) (10.5) (9.9)

54.9 52.3 57.1 59.1

(8.9) (9.6) (9.3) (11.1)

16 22 16.5 14.5

ISCI, Inhibitory self-control; FI, Flexibility Index; EMI, Emergent Metacognition Index; GEC, Global Executive Composite. *p50.05 (unilateral versus bilateral CP). Mann–Whitney U test. Table III. Reduction in T-scores on the main indices of the BRIEF-P after participation in the PIH programme. Parents’ and preschool teachers’ evaluations of the CP children are shown.

Mothers ISCI FI EMI GEC Fathers ISCI FI EMI GEC Preschool teachers ISCI FI EMI GEC



0.441 1.040 0.385 0.094

0.659 0.298 0.700 0.925

1.009 1.262 2.253 1.423

0.313 0.207 0.024* 0.155

1.214 2.032 1.265 1.367

0.225 0.042* 0.206 0.172

ISCI: Inhibitory Self-Control; FI: Flexibility Index; EMI: Emergent Metacognition Index; GEC: Global Executive Composite. *p50.05 (before and after participation). Wilcoxon signed ranks test.

similar to the mean scores of what is reported in the general population. This finding was somewhat unexpected, as others have pointed to elevated levels of executive function deficits in children with CP, when measured by neuropsychological tests [5]. One possible explanation is that the cognitive functions of the children in our sample are affected to a very low degree. Another possible explanation is that the children are still very young, and parents and preschool teachers might not be so attentive to executive function difficulties yet. Behavior that could reflect executive function difficulties at this age often resembles other age appropriate behaviors such as rigidity, self-regulation difficulties, or poor organizing skills. The children in our sample could also be a selected group already receiving close optimized follow-up that aids their development and prevents difficulties. Participation in

the PIH is optional and perhaps parents with the most energy, understanding of their child’s needs and commitment to strengthening their child’s development in the first place, are the ones that choose to participate. However, families that participate are recruited and referred from their own local habilitation service, and their experience is that most families that are offered a referral choose to participate. There is also a question as to whether BRIEF-P is sufficiently accurate in assessing these functions in preschool age. Studies have argued that both questionnaires and neuropsychological tests should be applied when assessing executive functions in preschool children. Nevertheless, these studies also suggest that questionnaires are probably better suited for measuring executive functioning in everyday life situations than standardized tests [22, 23]. The comparison between groups of children with unilateral and bilateral spastic type CP shows more executive function difficulties among the latter group of children, when rated by mothers before the PIH programme. The bilateral type of CP is generally caused by more extensive brain injury than seen for the unilateral type, with areas of both brain hemispheres affected. This increases the possibility of impairment in the cognitive networks and the total integrity of the brain. Recent studies on the plasticity of the brain show that the impact of early brain damage relies heavily on the type of injury. Anderson et al. [24] demonstrated that early focal injuries have a favorable developmental outcome compared with diffuse injuries. This difference might reflect the negative effects of a diffuse injury on the fiber networks in the brain, since normal early brain development depends on intact connectivity between brain regions [25]. No correlation was found between executive function difficulties and GMFCS levels. This may indicate that the topographical distribution of the brain damage is a more powerful predictor of executive function difficulties than the degree of motor impairment. It also accentuates the importance of focusing on cognitive functions regardless of the child’s motor functions. From clinical experience, it seems that the cognitive challenges of children with CP are sometimes underestimated, especially if the child’s motor functions are relatively strong. Research also shows that premature children with relatively mild forms of CP, in forms of spastic diplegia, still can have extensive cognitive impairments [26]. In our study, some indices in the BRIEF-P improved after participation in PIH. One can question whether this positive change in behavior/executive functions is due to the intensive habilitation programme, or simply a result of other factors, as general cognitive development and maturation. Natural maturation is an important factor as brain development is rapid in the early years of life. Nevertheless, of importance to our study, the BRIEF-P is based on age-referenced norms, enabling us to measure age appropriate change with time. Also, other programmes focusing on strengthening executive skills through daily activities and play in the general population of preschool children have been evaluated [27]. Barnett et al. [28] reported that a developmentally appropriate preschool programme with a strong emphasis on play [2], strengthened early executive skills in 3–4 year olds. Blair and Razza [29] found that self-regulation and inhibitory control aspects of executive function were prominent correlates of

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DOI: 10.3109/17518423.2014.916761

early math and reading ability, independent of general intelligence, and stressed the importance of play as the main intervention in preschool programmes improving executive skills. Fathers reported improved executive functioning in the area of emergent metacognitive skills after participation in PIH. This index is based on scores from items assessing working memory and planning/organizing skills. The working memory component seems especially important in the development and utilization of executive functions [11, 30]. Considering this, the possibility of stimulating development of working memory among children with CP seems both fascinating and necessary to employ. Preschool teachers’ assessment in the study is valuable as it provides comparative information about the children. Preschool teachers reported better functioning in the area of flexibility after the intervention. The FI is based on scores from items assessing the ability to shift between activities, and the ability to self-regulate emotions. The everyday activities and play situations in preschool often require the child to adapt to new situational demands. The finding that increased flexibility was found only in preschool teachers’ report and not by the parents could be explained by the fact that these functions are not challenged to similar degrees in the home setting, and the behavioral manifestations of eventual improvement at home are therefore also less salient. The mothers in our study did not report reduced levels of executive function difficulties after participation in the PIH programme. From experience, and based on the literature [31], mothers of children receiving habilitation services are usually very well informed about their child’s skills, functions, and difficulties. Hence, it might seem strange that mothers have not seen and reported the same positive tendency as fathers and preschool teachers. One possible explanation is that there might be a difference in demands regarding executive functioning based on which parent who is interacting with the child. There could also be a gender difference among the parents concerning whose activities the parents do with their children and the distribution of care giving and other daily life activities between the parents. However, these possible explanations are merely suggestions, as our data material does not contain information enabling us to explore them further. In this study, BRIEF-P was used as the assessment tool. The children were not tested with a full neuropsychological battery and a question is whether neuropsychological tests could have supplemented the evaluation of executive functions of the preschool children in this programme. As Anderson et al. [22] suggest executive skills can be difficult to measure with traditional assessment tools before the age of 6 years. One of the subtests from the NEPSY-II neuropsychological battery (Statue) could potentially be used [32], providing normative data from 3 years of age. However, concerning the motor impairments of the participants in this study, this test would not necessarily be valid. Given the age of preschool children, measuring daily life functions by parents and preschool teacher, proxy-reports seem more appropriate than using traditional assessment tools in a testing situation. As preschool children are too young to give selfreport, one has to rely on caretakers’ evaluation. Rater bias

Executive functions in preschool children with cerebral palsy


could therefore have affected the results [23], but since interrater reliability is reported to be high [14] and the same rater fills out the questionnaire on both occasions this is assumed to be of less importance in our study, at least concerning the assessment of change. Whether BRIEF-P is sufficiently sensitive to change is another issue. Studies using the BRIEFP as a tool for measuring change in executive functions in response to intervention are few. The fact that mothers’ scores in our study did not indicate reduced levels of executive function difficulties after participation in the PIH programme might suggest that this is a concern regarding the responsiveness to change of the BRIEF-P. Another aspect regarding the validity of the BRIEF-P in this study is whether it is a valid tool to evaluate executive functions in children with CP. The clinical samples included in the development of the BRIEF-P were children with language disorders, autism spectrum disorders, ADHD, and children born prematurely. Even though children with CP were not a specific clinical sample, the executive functions that are found to be affected in the clinical samples seem to resemble what can be found when working with children with CP [7, 8]. This supports the use of the BRIEF-P, as a way of collecting valuable information that is difficult to assess otherwise.

Limitations and future directions A weakness of the study is the lack of a control group, especially of age-matched children with CP who did not participate in the programme. This most likely would have improved the validity of this study. However, ethical considerations have been important in our decision of not to include such a group in this study. PIH was initiated to give families an intensified local programme of habilitation that they had not had before. It was therefore not an issue to exclude patients at enrollment, or let them serve as a comparison group in the research study, without getting the full PIH. The findings concerning effect of the intervention on executive functioning are modest in this study. There is also some inconsistency among mothers, fathers and preschool teachers’ scores. Rater bias, different contexts, and number of participants might account for some of these limitations. The number of participants has been as high as possible, based on the actual participating families in the PIH. Later studies with more participants would obviously be a valuable supplement in future research for evaluating generalization and general validity of this pilot study. Follow-up studies using BRIEF-P at later time points would give important information about factors like reliability or potential consistency of improved executive functioning after participation in the intensified programme.

Implications and conclusion Few studies exist that focus on executive functioning of preschool children with CP and on effects of intervention. Accordingly, our results should be of interest to others working with neurodevelopmental disorders, and especially children with CP in this age group. Fathers and preschool teachers reported reduction in executive function difficulties after the intervention


K. Sørensen et al.

programme. Therefore, it seems appropriate to suggest that intensified habilitation focusing on executive functions through appropriate play oriented interventions, probably is suitable for supporting the development of early executive functions in children with CP. Using the BRIEF-P also contributed to the process of differentiating cognitive strengths and weaknesses among the participating children in PIH. The results were, therefore, also helpful in the development of appropriate training and stimulation strategies for the individual child.

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14. 15.

16. 17.

Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this paper.

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Executive functions in preschool children with cerebral palsy--Assessment and early intervention--A pilot study.

To assess the level of executive functioning among preschool children with cerebral palsy (CP) and evaluate effects of the Program Intensified habilit...
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