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Developmental Neurorehabilitation

ISSN: 1751-8423 (Print) 1751-8431 (Online) Journal homepage: https://www.tandfonline.com/loi/ipdr20

An Exploratory Study of Executive Function


Development in Children with Autism, after
Receiving Early Intensive Behavioral Training

Erik Winther Skogli, Per Normann Andersen & Jørn Isaksen

To cite this article: Erik Winther Skogli, Per Normann Andersen & Jørn Isaksen (2020):
An Exploratory Study of Executive Function Development in Children with Autism, after
Receiving Early Intensive Behavioral Training, Developmental Neurorehabilitation, DOI:
10.1080/17518423.2020.1756499

To link to this article: https://doi.org/10.1080/17518423.2020.1756499

Published online: 13 May 2020.

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https://www.tandfonline.com/action/journalInformation?journalCode=ipdr20
DEVELOPMENTAL NEUROREHABILITATION
https://doi.org/10.1080/17518423.2020.1756499

An Exploratory Study of Executive Function Development in Children with Autism,


after Receiving Early Intensive Behavioral Training
Erik Winther Skoglia, Per Normann Andersenb, and Jørn Isaksenc
a
Innlandet Hospital Trust, Division Mental Health Care, Child and Adolescent Psychiatric Clinic, Lillehammer, Norway; bDepartment of Psychology,
Inland Norway University of Applied Sciences, Lillehammer, Norway; cInnlandet Hospital Trust, Lillehammer, Norway

ABSTRACT ARTICLE HISTORY


Objective: To examine the development of executive functions, in preschool children with autism Received October 28, 2019
spectrum disorders (ASD), receiving early intensive behavioral training (EIBI). Revised April 10, 2020
Method: Executive functions (EF) were assessed with The Behavior Rating Inventory of Executive Accepted April 12, 2020
Function – Preschool Version (BRIEF-P), by parents and preschool teachers at the time of diagnostic KEYWORDS
assessment and after 15 months of EIBI intervention. Ten children with ASD (M = 2.9 years, nine males) Autism; children; early
participated in the study. Reliable Change Index scores were computed for each of the participants in intensive behavioral
order to investigate any significant change in BRIEF-P T-scores. training; executive functions;
Results: Three children showed a significant improvement in EF, based on parent ratings. Four children brief; reliable change index
showed a significant improvement in EF based on preschool teacher ratings.
Conclusion: Findings indicating a reliable improvement in one third of preschool children with ASD
receiving EIBI are encouraging but need to be replicated in larger scale controlled studies.

Introduction ASD and Executive Dysfunction


Autism spectrum disorders (ASD) constitute a group of neuro- Executive functions (EF) are commonly referred to as a set of
developmental disorders, emerging in childhood, characterized higher order cognitive abilities necessary for goal-directed beha-
by pervasive deficits in social behavior and interaction.1 The key vior, including response inhibition, cognitive flexibility and the
manifestations of ASD are impaired social interaction, commu- maintenance of information in working memory.9 There is an
nication deficits and restricted and repetitive patterns of beha- ongoing debate as to whether single- or multifactor models of EF
viors, interests and activities. In the last revision of the best encapsulate the construct. There is, however, ample evi-
Diagnostic and Statistical Manual of Mental Disorders dence of a multifactorial model of EF, where a unitary or single-
(DSM-5), ASD subtypes were eliminated and the social interac- factor model seem to be more appropriate in preschool
tion and social communication domains were collapsed into populations.10,11 Preschool years and childhood are character-
a single combined domain.2,3 ASD is genetically and phenotypi- ized by rapid changes in EF, 12 and a developmental delay in EF
cally heterogeneous with variable degrees of severity, sympto- is considered a central source of the disability associated with
matology and different outcomes. However, the common ASD.13–17 Impaired EF, have been associated with poor beha-
denominator is that ASD is a life-long persistent neurodevelop- vioral, social, educational and occupational outcomes in neuro-
mental disorder that may cause detrimental functional impair- developmental populations, and meta-analyses have found
ment in school, work and family life, as well as increased levels of robust associations between EF impairment and ASD.18,19
co-morbidity across the lifespan.3,4 With reported worldwide Furthermore, EF have been associated with Theory of Mind
prevalence estimates ranging between 0.7% and 1.2%, ASD (ToM) in children with ASD.20–22 Although EF have been
represent a major public health challenge.5,6 Furthermore, high found to predict changes in ToM abilities in ASD, ToM seems
levels of heterogeneity with regard to symptom manifestation, to have little impact on changes in EF abilities. Impaired EF as
co-morbidity, cognitive function and impairment level, often such, may be one putative factor limiting the development of
cloud the diagnostic picture and may hamper treatment ToM, causing difficulties in the social functioning of children
planning.7 Knowing that behavioral symptoms associated with with ASD.22–24 Furthermore, EF seem to be a better predictor of
ASD are not always stable over time, concerns have been raised social-communication problems in ASD than ToM.25 Given the
that approaches focusing on behavioral symptoms only, may not robust associations between EF and functional outcome in ASD,
18,19
address the range of clinically relevant symptoms in children it is interesting to note that EF impairments unfolding
with this disorder. Despite high levels of heterogeneity, cognitive throughout childhood, seem to persist in neurodevelopmental
deficits linked to prefrontal and temporal brain regions, which pediatric populations, despite a reduction in symptom
are crucial for executive functions, have been proposed as one manifestation.26–28 Clearly, the persistence of executive dysfunc-
common hallmark for children and adults with ASD.8 tions across time, may cause detrimental functional impairment

CONTACT Erik Winther Skogli erik.winther.skogli@sykehuset-innlandet.no Innlandet Hospital Trust, Division Mental Health Care, Child and Adolescent
Psychiatric Clinic, Anders Sandvigsgate 17, 2629 Lillehammer, Norway
© 2020 Taylor & Francis Group, LLC
2 E. W. SKOGLI ET AL.

in school, work and family life. This elucidates the centrality of regulation.45,46 Thus, given the strong associations between EF
targeting these EF deficits to plan intervention and improve and IQ,35,36 one hypothesis could thus be, that improved results
social functioning in children and adolescents with ASD. in IQ-tests, reported by,30 are mainly driven by improved EF in
children with ASD receiving EIBI. From this perspective, it could
be possible that improved EF in children with ASD who receive
Early Intensive Behavioral Intervention EIBI, simply make these children more able to use their intellec-
Thorough reviews of research29 and meta-analyses,30,31 have tual capabilities and hence improve their scores on intelligence
reported early intensive behavioral intervention (EIBI) to be an tests. The aim of this pilot study was, therefore, to examine the
effective and well documented approach in improving current development of EF, in a group of children with ASD, receiving
and future functioning in preschool children with ASD. There is EIBI. Based on current knowledge we hypothesized that children
a growing body of evidence that EIBI may result in significant with ASD receiving EIBI, will show a greater improvement over-
improvements in adaptive behavior, language as well as intellec- all in everyday EF, than would be expected, based on the
tual functioning in preschool children with ASD.29 Using parti- Behavior Rating Inventory of Executive Functions – Preschool
cipant data,30 reported a reliable positive change in intellectual version (BRIEF-P) T-scores at baseline (T1).
functioning (IQ), based on IQ test-scores for 29% of children
with ASD receiving EIBI. With regard to adaptive behavior,30
reported a reliable positive change in adaptive behavior compo-
Method
site scores, based on Vineland Adaptive Behavior Scales32 in 20% Procedure and Participants
of children with ASD receiving EIBI. Other controlled studies
This study included children from three to six years referred in
have reported that approximately 50% of children with ASD
an ordinary manner to the Division of Habilitation and
manage school without support, and 40% of children with
Rehabilitation, Innlandet Hospital Trust for an assessment of
ASD show age appropriate language skills after receiving EIBI
ASD. The subjects were recruited as consecutive referrals to the
in preschool years.30,33 Around 10% show little or no benefit
Habilitation Clinic at Lillehammer, Norway. Ten children parti-
from EIBI treatment.30,34 Given the strong associations between
cipated in the study (Table 1). All the children received training
EF and IQ,35,36 previous reports are promising findings regard-
based on EIBI, and had more than 25 hours a week of intensive
ing the potential effects of EIBI on improved EF in children with
behavioral treatment. The treatment met the criterion for quality
ASD. Although there has been a growing interest in behavioral
treatment described in.47 All children were enrolled in full-time
intervention aiming to improve EF in children with ASD,37 few
kindergartens for neurotypical children. They received on aver-
studies have investigated EF outcome in children with ASD
age 15.3 months of intervention between the pre- (T1) – and
receiving EIBI or other behavioral intervention programmes.
posttest (T2) assessment (range 10–19 months).
In one single-subject design study, addressing working
memory,38 reported improved performance on a counting
span task, using positive reinforcement in three children with
Measures
ASD. Further, Cognitive-Functional intervention is reported to
show moderate to large improvements in EF for young children All participants underwent a comprehensive assessment according
with Attention Deficit Hyperactivity Disorder (ADHD) after to common clinical practice. The assessment comprised
12 weeks of intervention.39 Parental training programmes aim- a structured diagnostic interview with the parents (Autism
ing to support EF in preschool children with ADHD, have also Diagnostic Interview – Revised),48 a diagnostic observation sche-
reported promising results regarding improved executive func- dule (Autism diagnostic observation schedule–2nd edition),49
tioning in everyday situations.40 Intervention programmes aim- a cognitive assessment, an assessment of language functioning
ing to amend EF in neurotypical children have also reported and a medical examination. The diagnostic evaluation with
improved EF.41–44 One randomized controlled study reported Autism Diagnostic Interview – Revised (ADI-R) and the Autism
significantly greater EF improvement in a group of children after diagnostic observation schedule–2nd edition (ADOS-2) were sup-
12 weeks of school curricula intervention, relative to the control plemented with information from the Social Communication
group.41 There is also some evidence for improved EF in pre- Questionnaire – Current (SCQ-C),50 which covers the DSM-
school programmes, aimed at improving behavior and emotion IV51 and ICD-1052 symptoms for ASD. The SCQ-C was filled

Table 1. Overview of diagnosis, gender, age at assessment, mental age at assessment and duration of treatment for each of the ten participants.
Diagnosis Diagnosis Age in months diagnostic Mental age in Age in months expressive Age in months impressive
Child ICD-10 DSM-IV Gender assessment months language language
1 84.9 299.80 boy 39 *27 *22 *26
2 84.0 299.00 boy 45 *27 *25 *25
3 84.0 299.00 boy 41 *26 - *17
4 84.0 299.00 boy 38 *12 - *9
5 84.0 299.00 boy 33 * 42 *42 *42
6 84.9 299.80 boy 48 ** 25 **13 **14
7 84.1 299.80 boy 33 *39 *37 *36
8 84.0 299.00 boy 24 - - -
9 84.0 299.00 girl 28 - - -
10 84.0 299.00 boy 29 *19 *16 *15
*Bayley Scales of Infant Development-III, cognitive scale, **Psychoeducational Profile-third edition (PEP-3), -Not assessed.
DEVELOPMENTAL NEUROREHABILITATION 3

out by parents and preschool teachers. ADI-R interviews with the clinics. In this guideline, procedures are described with regard
parents and ADOS-2 observations with the children, were per- to the supervision of municipal employees and parents in the
formed by experienced psychologists, special education teachers implementation of highly specialized treatment techniques,
and social educators at the Division of Habilitation and based on the principles of applied behavior analysis. The inter-
Rehabilitation, Innlandet Hospital Trust. The ADI-R, ADOS-2 vention was supervised and conducted by highly specialized
and SCQ-C have shown robust psychometric properties with behavioral analysts, mainly social educators, with considerable
regard to the classification of ASD.53–56 Additional information knowledge of EIBI for preschool children with ASD. The
from preschool teachers with regard to kindergarten functioning intervention is complex because it is executed in collaboration
(language development, social and motor function), which is with and by means of interaction between the specialist health
mandatory on referral, was also incorporated into the diagnostic services, municipal services, patients and guardians. The EIBI
evaluation. Diagnoses were considered positive, if, based on intervention method involves behavioral training from 20 to
a comprehensive evaluation of the ADI-R, ADOS-2, teacher infor- 30 hours per week. Children received intervention in multiple
mation and rating scales, DSM-IV51 and ICD-1052 criteria were settings including the home, kindergarten and the community.
met. Cognitive functioning was assessed by experienced psychol- Each child’s training was delivered by a team of three to four,
ogists with the Bayley Scales of Infant Development, Third trained preschool teachers, teaching assistants and parents.
Edition,57 cognitive scale, or Psychoeducational Profile-third EIBI treatment goals include all aspects of a child’s functioning,
edition.58 Language development was assessed by experienced targeting areas such as compliance skills, joint attention skills,
special education teachers with the Bayley Scales of Infant language and communication skills, play and social skills, self-
Development, Third Edition (Bayley-III), impressive and expres- help skills and preschool skills. Within these areas, more spe-
sive scales. Bayley-III is an individually administered norm- cific training programmes are individually tailored to teach the
referenced scale assessing cognitive development, language func- children skills such as planning, sequencing, initiating, flexibil-
tion (receptive and expressive communication) and motor func- ity in doing and thinking, adaptability, self-evaluation, organiz-
tion (gross and fine) in children age 1–42 months.57 Bayley-III is ing and self-regulation. The basis of the intervention comprises
widely used in both clinical practice and research, and has demon- behavior analytic techniques, including numerous reinforce-
strated robust psychometric properties.57 Psychoeducational ments, instructional, shaping and prompt/prompt fading pro-
Profile-third edition (PEP-3) is another individually- cedures. The behavioral programming is inspired by different
administered, norm-referenced scale assessing cognitive develop- treatment manuals.47,62,63 Instruction occurred both during
ment, language function (receptive and expressive communica- formal, structured sessions as well as in less structured situa-
tion) and motor function (gross and fine) in children from six tions such as play sessions, both in kindergarten and at a child’s
months to seven years.58 PEP-3 has demonstrated good internal home including with other children. The preschool teachers are
consistency and test-retest reliability, with correlations ranging trained and supervised closely by specialists in behavior analy-
from .78 to .99.58 Preschool children with ASD were assessed sis and early intervention at the Division of Habilitation and
with The Behavior Rating Inventory of Executive Function – Rehabilitation, Innlandet Hospital Trust. Initially the preschool
Preschool Version (BRIEF-P)59 at the time of diagnostic assess- teachers receive supervision on a weekly basis. After two to
ment (T1) and after 15 months of EIBI intervention (T2). In the three months, when behavioral training has been well estab-
current study, parents and preschool teachers were asked to com- lished, the specialists at the Division of Habilitation and
plete the written form of the Norwegian version of BRIEF-P60 at Rehabilitation supervise the preschool teachers every
each time point. Exclusion criteria for all participants included fourteenth day. The procedural integrity requirements were
severe head injury (with loss of consciousness) and any disease set for the implementation of the individual training pro-
affecting the central nervous system. grammes. All preschool teachers were tested for training skills
and had to meet quality requirements, outlined in the
Norwegian regional guideline for EIBI.61
Attrition
In this study, we initially included 18 children with diagnoses
Outcome Measure
within the autism spectrum disorders. Eight children were
excluded from the study, due to failure to meet EIBI require- The Behavior Rating Inventory of Executive Function – Preschool
ments, according to the number of intervention hours or quality Version (BRIEF-P)59 has been developed to assess EF behavior in
of intervention or incomplete data sets. Only those children children aged two to five years. The BRIEF-P includes 63 items,
whose treatment met the EIBI requirements and whose test – each of which is rated on a three-point scale with the values:
retest data were complete, are included in the study. 1 = Never, 2 = Sometimes and 3 = Often. These 63 items are
composed into five clinical scales (Inhibition, Working Memory,
Shift, Emotional Control, Plan/Organize). These five clinical scales
Intervention
form three broad classifications of executive functioning –
Clinical experience with EIBI together with extensive Inhibitory Self Control Index (ISCI), Flexibility Index (FI),
research30,31 has led to the preparation of a Norwegian regional Emergent Metacognition Index (EMI), as well as an overall
guideline for EIBI. The guideline61 was made available in the Global Executive Composite (GEC) score.59 The GEC score is
National Health Library in February 2017. This procedure reported in this article. BRIEF-P scores are converted into stan-
addresses specialist health services, such as Child Habilitation dardized T-scores (M = 50, SD = 10). T-scores ≥ 65 (+1.5 SD) are
Services and Child and Adolescent Psychiatric outpatient defined as EF problems in the clinical range.59 BRIEF-P
4 E. W. SKOGLI ET AL.

demonstrated high internal consistency (Cronbach’s α = .80 − .97) Table 3. Teacher rated BRIEF-P Global Executive Composite (GEC) T-scores at
baseline (T1) and 15 months follow up (T2). Change status and RCIs for each of
and good test-retest reliability (r = 0.78–0.90).64 These values are the ten participants.T-scores are based on the original norms. Elevated BRIEF-P
at the same level as Cronbach’s α, reported in the original BRIEF T-scores indicate a higher degree of impairment.
manual (.80 − .98).65 In the current study, parents and preschool Child T1 T2 Change RCI
teachers are asked to complete the written form of the Norwegian 1 65 57 −8 −1.63
translation of BRIEF-P.60 T-scores are based on the original 2 78 60 −18 −3.67*
3 76 43 −33 −6.74*
norms and elevated BRIEF-P T-scores indicate a higher degree 4 84 81 −3 −0.61
of impairment. 5 87 75 −12 −2.45*
6 88 65 −23 −4.70*
7 80 81 1 0.20
8 81 83 2 0.41
Data Analyses 9 56 71 15 3.06*
10 82 77 −5 −1.02
BRIEF-P data are presented in Tables 2 and 3 as composite
BRIEF-P; Behavior Rating Inventory of Executive Function-Preschool version. *RCI
T-scores at the baseline (T1) and at the 15 months follow up values ≥ ±1.96 indicate a reliable change at a 95% confidence level (p-value ≤
(T2) for each of the ten participants. Parent ratings are reported 0.05). Positive change scores indicate increasing EF problems. Negative change
in Table 2. Preschool teacher ratings are reported in Table 3. In scores indicate decreasing EF problems.
order to investigate any significant change in BRIEF-P T-scores
across time, a Reliable Change Index (RCI)66 was computed for
each of the participants. The RCI is a statistical technique, a chance of above 95% of detecting a genuine effect should
designed to test whether any observed difference between two one exist and not explained by a measurement error.
or more time points have occurred by chance, or not. The
advantage of this approach is that RCI can provide an evi- x2  x1
RCI ¼ rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
dence-based analysis of change within individuals, across time
or conditions.67 In line with the original publication by,66 we 2ðSD 1  rxx Þ2
computed an RCI for each of the participants, by dividing
BRIEF-P change scores (T2 – T1) by the standard error of Hence, we used this approach to test and reject the hypothesis that
the difference (Sdiff) for each of the participants. observed differences within each participant in EF from T1 to T2
x2  x1 have occurred by chance. Furthermore, by applying age adjusted
RCI ¼ T-scores instead of raw scores, T-scores allow us to detect sig-
Sdiff
nificant changes in each individual that are not due to maturation.
Decreasing T-scores indicate a lower degree of impairment from
In order to estimate the standard error of the difference T1 to T2, while increasing T-scores indicate a higher degree of
(Sdiff), we calculated the standard error (Se), using impairment from T1 to T2. Unchanged T-scores from T1 to T2
a standard deviation of ten (SD), a test-retest reliability of indicate an unchanged level of impairment from T1 to T2, in
0.90 (parent rating) and 0.88 (teacher rating) from the nor- which the children display a maturation of EF-skills as expected,
mative sample of BRIEF-P.59 relative to neurotypical children. RCI-scores based on the original
qffiffiffiffiffiffiffiffiffiffiffiffi proposals by,66 may also be calculated using the RCI-calculator,
Sdiff ¼ 2ðSe Þ2 developed by,68 http://daniel-zahra.webs.com/publications.htm

pffiffiffiffiffiffiffiffiffiffiffiffiffiffi
Se ¼ SD 1  rxx Ethics
RCI values ≥ ±1.96 are considered to indicate a reliable The study was approved by the Norwegian Center for
change at a 95% confidence level [p-value ≤ 0.05), i.e., Research Data (project number: 51533) and conducted in
accordance with the Helsinki Declaration of the World
Table 2. Parent rated BRIEF-P Global Executive Composite (GEC) T-scores at Medical Association Assembly. According to the Regional
baseline (T1) and 15 months follow up (T2). Change status and RCIs for each Committee for Medical Research Ethics in Eastern Norway
of the ten participants.T-scores are based on the original norms. Elevated BRIEF-
P T-scores indicate a higher degree of impairment. (REK), this study did not require REK-approval (REK ref.
Child T1 T2 Change RCI
2017/72). The study is also registered in the www.isrctn.com
1 53 56 3 0.67
clinical trial register (ISRCTN registry – 33010). The parents
2 66 57 −9 −2.01* of all the children were informed about the research project
3 84 73 −11 −2.46* both in person and in writing, and they were asked if they
4 72 72 0 0.00
5 66 68 2 0.45 agreed to allow the data from the EIBI intervention to be used
6 80 70 −10 −2.24* for research purposes. Participants were also asked whether
7 96 94 −2 −0.45
8 63 64 −1 0.22 they could be contacted again 12 months after intervention
9 39 75 36 8.05* had been terminated, for a follow-up evaluation with the
10 78 73 −5 −1.12 BRIEF-P. Subjects who did not wish to participate in the
BRIEF-P; Behavior Rating Inventory of Executive Function-Preschool version. *RCI research project were provided the same clinical assessment
values ≥ ±1.96 indicate a reliable change at a 95% confidence level (p-value ≤
0.05). Positive change scores indicate increasing EF problems. Negative change and offered the same intervention method as those participat-
scores indicate decreasing EF problems. ing in the study.
DEVELOPMENTAL NEUROREHABILITATION 5

Results children with ASD showed no increase in EF-problems from


T1 to T2. Interestingly, no reliable change in EF-problems for
Parent Report
six of the children may thus indicate an age adequate matura-
Ten children with ASD (M = 2.9 years, nine males) were rated tion of EF in more than half of the children with ASD
with BRIEF-P at the time of diagnostic assessment and after receiving EIBI.59 Our findings showing a reliable EF improve-
15.3 months of EIBI intervention. The results are presented in ment in three out of ten children, are somewhat correspond-
Table 2. Based on computed Reliable Change Indexes (RCI) ing to previous studies reporting a reliable change in IQ for
for each of the participants and comparing GEC T-scores at 29% of children with ASD receiving EIBI, and a reliable
T1 and T2, three children showed a reliable decrease in GEC change in adaptive behavior for 20% of the children with
T-scores from T1 to T2 (child two T1: 66, T2: 57, RCI: −2.01; ASD receiving EIBI.30,34 Unfortunately, parents of one child
child three T1: 84, T2: 73, RCI: −2.46; child six T1: 80, T2: 70, reported elevated levels of EF-problems at T2 compared to
RCI: −2.24). Six children showed no significant change in T1. Although empirical evidence has found EIBI to be an
GEC T-scores from T1 to T2 (child one T1: 53, T2: 56, RCI: effective treatment for children with ASD, a minority of
0.67; child four T1: 72, T2: 72, RCI: 0.0; child five T1: 66, T2: children with ASD (10%) are reported to show little or no
68, RCI: 0.45; child seven T1: 96, T2: 94, RCI: −0.45; child benefit from the treatment with regard to adaptive behavior,
eight T1: 63, T2: 64, RCI: 0.22, child ten T1: 78, T2: 73, RCI: language or intellectual functioning.30,34 Clearly, it is possible
−1.12). One child displayed increased GEC T-scores from T1 that EF-problems will persist in some children with ASD
to T2 (child nine T1: 39, T2: 75, RCI: 8.05.) receiving EIBI. One explanation may be that parents receive
information regarding their children’s difficulties at the time
of their diagnostic assessment and later in EIBI treatment
Preschool Teacher Report meetings. Improved knowledge regarding the children’s diffi-
The results are presented in Table 3. Based on computed culties, may thus make some parents more sensitive to EF
Reliable Change Indexes (RCI) for each of the participants problems, leading to elevated scores on BRIEF-P question-
and comparing GEC T-scores at T1 and T2, four children naires at T2.
showed a reliable decrease in GEC T-scores from T1 to T2
(child two T-score T1: 78, T2: 60, RCI: −3.67; child three T1: Preschool Teacher Report
76, T2: 43, RCI: −6.74; child five T1: 87, T2: 75, RCI: −2.45;
child six T1: 88, T2: 65, RCI: −4.70). Five children showed no With regard to preschool teacher reports, four out of ten
significant change in GEC T-scores from T1 to T2 (child one children displayed a significant improvement in EF skills
T1: 65, T2: 57, RCI: −1.63; child four T1: 84, T2: 81, RCI: from T1 to T2. Five out of ten children showed no significant
−0.61; child seven T1: 80, T2: 81, RCI: 0.20; child eight T1: 81, change in EF, while one child showed a significant increase in
T2: 83, RCI: 0.41, child ten T1: 82, T2: 77, RCI: −1.02). One EF problems from T1 to T2. Intra-class correlations show
child showed increased GEC T-scores from T1 to T2 (child a good to moderate inter-rater reliability between parent and
nine T1: 56, T2: 71, RCI: 3.06) preschool teacher reports at T1 (ICC: 0.71) and T2 (ICC: 0.56)
indicating the same tendency in parent and preschool teacher
reports at T1 and T2. Preschool teachers, however, seem to
Discussion report a reliable improvement in more cases than the parents.
Furthermore, preschool teachers seem to report larger RCI
Parent Report
effects for those children showing a reliable improvement in
We found that three out of ten children with ASD receiving BRIEF-P ratings, compared to parent reports (see Tables 2
EIBI, showed a significant improvement in EF (GEC and 3). When inspecting T-scores at T1 and T2, preschool
T-scores) from T1 to T2, based on parent ratings. Six of the teachers, in general, report greater EF impairment at T1
children displayed no significant change in EF from T1 to T2. compared to parent ratings (T1: parent mean 69.7, teacher
The parents of one child reported a significant increase in EF mean 77.7; T2: parent mean 70.2, teacher mean 70.3). Larger
problems from T1 to T2. Age adjusted T-scores allowed us to RCIs in preschool teacher ratings compared to parent ratings,
detect an improvement in EF beyond that which could be may thus be driven by higher ratings of EF-problems at T1 by
expected due to maturation. A significant decrease in BRIEF- preschool teachers. Challenges in everyday EF may be more
P T-scores might thus reflect a development in EF skills and demanding in a kindergarten setting than at home. Preschool
beyond age expected maturation from T1 to T2 for three of teachers may thus be more susceptible to detecting subtle
the ten participants.59 When inspecting BRIEF-P T-scores for differences in children’s EF over time. By comparison, pre-
the three children showing a reliable improvement from T1 to vious research on the parent-teacher agreement reveals that
T2, one child no longer displayed EF problems in the clinical parents of neurotypical children rate their children as having
range, i.e., T-score < 65 at T2. The other two children still more EF difficulties than preschool teachers.64 However, the
struggled with EF problems in the clinical range at T2, but at children in our study were all diagnosed with ASD and this
a significantly lower level compared to age-referenced norms may represent a greater challenge in kindergarten than at
at T1.59 Furthermore, results showing no reliable change in home. This is in line with the findings of,69 with regard to
six of the children, indicated no improvement in EF-problems children with ADHD. The participants in our study were very
relative to age-referenced norms from T1 to T2. Nonetheless, young (age range 24 to 48 months) and problems with emo-
no reliable change in EF-problems indicated that six of the tional self-regulation, impulse-control and attention, will
6 E. W. SKOGLI ET AL.

often be interpreted as age appropriate behavior at this stage (n = 37). Other intervention programmes aiming to enhance
of development. Often preschool teachers will have a better EF and learning in preschool and school age children, have
opportunity than parents to compare the developmental levels reported similar findings with a reduction in problem behavior,
of children of the same age. This could make preschool improved emotion-regulation and better social problem-solving
teachers more sensitive to EF-problems when behavior man- skills, after being enrolled in different kindergarten and school
ifestations are difficult to understand in young children. curricula programmes.46,74,75 Previous research with neurotypi-
Nevertheless, direct observations could be more sensitive to cal children elucidates the centrality of improved emotional and
subtle behavior changes than indirect observations like behavioral regulation when aiming to improve EF through dif-
BRIEF-P ratings.70 Consequently, inferior sensitivity in indir- ferent intervention programmes. Furthermore, as previous
ect observations compared to direct observations, may be one research has reported behavior regulation to be closely linked
possible explanation of our results, indicating a reliable to social function in children with ASD,76 these findings may
improvement in only a minority of the participants. The indicate that the key advantage of such intervention pro-
child reported to show more EF-problems at T2 according grammes are related to children’s social function, rather than
to parent ratings, was also reported to show elevated levels of academic outcome.41 Improved social function may boost test
EF problem behavior at T2 by preschool teachers. performance in intelligence tests and academic outcome, as
Interestingly, parents report this aggravation in EF problems better social competencies enhance the co-operation needed
as being on a much larger scale than preschool teachers for solving many of the tasks given in school settings.41
(parent report RCI 8.05, preschool teacher report RCI 3.06). Our results, which indicate a reliable improvement in
As previously discussed, parents’ increased knowledge regard- a minority of the participants, raises the question whether
ing the children’s functioning at T2 may be one potential BRIEF-P is sufficiently sensitive to change in preschool chil-
explanation of larger RCI effects in parent reports, by com- dren with ASD. Previous studies have reported that neurop-
parison with preschool teacher reports for the same child. sychological EF test results are only tenuously linked to the
symptom severity in neurodevelopmental disorders, with up
to 50% of children and adolescents with ADHD or ASD
Development of EF in Children with ASD Who Receive EIBI
performing normally on EF tests.26,77–79 These findings have
In this exploratory study we wanted to investigate the develop- raised a concern regarding the ecological validity of EF test
ment of EF in children with ASD who receive EIBI. Based on results.80 Where traditional neuropsychological EF tests seem
parent ratings before intervention (T1), seven out of ten children to capture “best estimates” in an ideal setting,81 the Behavior
with ASD displayed EF problems in the clinical range (T-scores Rating Inventory of Executive Function (BRIEF) was designed
≥ 65) on the Global Executive Composite. Based on preschool to assess EF performance in ecologically valid situations.65 In
teacher ratings, nine out of ten children displayed EF problems clinical practice, the BRIEF has proven to be a valuable addi-
in the clinical range on the Global Executive Composite at T1. tional assessment tool for the identification of impaired EF in
Thus, the majority of children with ASD participating in this school-aged children, demonstrating better sensitivity in the
study, displayed clinical levels of EF problems. These findings assessment of EF problems than neuropsychological EF tests.-
80,82–84
corresponded to previous studies reporting impaired EF in As such, BRIEF-P may seem more suited to detecting
pediatric populations with ASD,18 as well as in other neurode- EF-change in preschool children with ASD, than neuropsy-
velopmental populations.71,72 In this exploratory study, we chological tests. Furthermore, other intervention studies with
wanted to test the hypothesis that children with ASD who pediatric populations have reported inconsistent results, using
receive EIBI will show a greater overall improvement in everyday BRIEF as an outcome measure,85 reported lesser treatment
EF, than would be expected based on BRIEF-P T-scores at T1. effects based on BRIEF-P as an outcome measure in preschool
Our findings indicated a significant decrease in EF problems in children with cerebral palsy, compared to the BRIEF-P
three to four of the children with ASD after 15 months of EIBI T-score changes in our study. Results from one study by,39
treatment. Five to six children showed no reliable decrease or supports the effectiveness of cognitive-functional (Cog-Fun)
increase in EF problems after 15 months of EIBI treatment. One intervention on improved BRIEF and BRIEF-P scores in chil-
child displayed more severe EF problems after 15 months of EIBI dren with ADHD. Promising results have also been reported
treatment. In summary, our findings revealed that a minority of from parental training programmes, aiming to support EF in
children with ASD receiving EIBI, showed increasing levels of EF preschool children with ADHD when assessed with BRIEF
problems in everyday situations. These are potentially interest- and BRIEF-P.40 Thus, in spite of inconsistent findings, the
ing findings regarding the centrality of EF problems in children results of our study indicating a reliable change in approxi-
with ASD18,19 and the detrimental effects EF deficits may have mately one third of the participants, as well as findings
on social-, educational- and occupational function across the reported by,39,40 and may support the use of BRIEF-P when
lifespan.13–17 By comparison, intervention programmes aiming assessing EF change in preschool children with ASD.
to improve EF through learning and behavioral interventions in
neurotypical children have reported improved EF.41–44,73 In an
Limitations and Future Directions
RCT-intervention study with school age children,41 reported
a significantly greater improvement in global EF and improved The lack of a control group represents a major limitation in this
behavior regulation skills after 12 weeks of school curricula, exploratory study. Consequently, we investigated EF change
aiming to enhance EF (Art of Learning) in those children receiv- within individuals across time, and applied RCI analyses in
ing intervention (n = 66) compared to the control group order to investigate any reliable change from T1 to T2. A small
DEVELOPMENTAL NEUROREHABILITATION 7

sample size is another limitation. A larger sample size could have Disclosure statement
allowed for more replications of the results in this study, which The authors declare no conflict of interest with respect to the authorship
could have strengthened the findings. However, a well-powered or publication of this article.
RCT would strengthen the quality of the findings in future
studies, investigating the effect of EIBI on EF outcomes in
children with ASD. Another potential limitation is that the Funding
sample was drawn from a clinical population and represents
those parents who are willing to seek help for their children. Skogli’s authorship was supported financially by the Innlandet Hospital
Trust (grant number 150610). Andersen’s efforts were supported by the
Although the participants were recruited as consecutive referrals
Inland Norway University of Applied Sciences.Isaksen’s efforts were
to the Habilitation Clinic at Lillehammer, Norway, only ten of supported by the Innlandet Hospital Trust and Inland Norway,
the initial 18 children were included in the study. This relatively University of Applied Sciences.
high attrition rate might hamper our findings in this study.
Furthermore, the lack of neuropsychological assessment of EF
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