Research in Developmental Disabilities 33 (2012) 858865

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Research in Developmental Disabilities

Executive dysfunctions among boys with Attention Decit Hyperactivity Disorder (ADHD): Performance-based test and parents report
Maayan Shimoni a,*, Batya Engel-Yeger a, Emanuel Tirosh b,c
a

Department of Occupational Therapy, Faculty of Welfare and Health Sciences, University of Haifa, Israel The Hannah Khoushy Child Development Center, Bnai Zion Medical Center. Faculty of Medicine, Technion, Israel c Institute of Technology, Israel
b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 16 October 2011 Received in revised form 20 November 2011 Accepted 15 December 2011 Available online Keywords: ADHD BRIEF BADS-C Performance-based test Parent questionnaire

Difculty in executive functions (EF) is a core symptom of ADHD. Yet, the EF assessments are still in controversy. It is still unclear whether the everyday implementation of EF can be assessed under laboratory conditions. Therefore, the purposes of the present study are: (a) to examine EF among boys with ADHD both in everyday behavior (as reported by parents) and in a performance-based test. (b) To examine correlations between the two tests. Both the Behavior Assessment of Dysexecutive Functions for Children (BADS-C) and the Behavior Rating Inventory of Executive Functions (BRIEF) were independently applied to 25 boys aged 811 years with ADHD and 25 age-matched typical boys. Results of the two assessments were compared between the two groups to indicate differences in EF. Correlations between the two assessments for all participants were evaluated. Overall, signicant differences in EF were found between the two groups on both assessments. Signicant correlations were found between BADS-C and BRIEF, specically in metacognition but not in behavioral regulation. Findings indicate that poor EF manifests itself in everyday behavior. These difculties are found in metacognitive and behavioral regulation components. Nevertheless, applying a valid ecological assessment of behavior regulation merits future research. 2012 Published by Elsevier Ltd.

1. Introduction Executive functions (EF) refers to the mental skills required to proceed towards future goals in terms of self-awareness, metacognition and attention skills (Welsh & Pennington, 1988; Welsh, Pennington, & Grossier, 1991). Difculties in EF are related to various frontal and prefrontal lobe disorders (Alverez & Emory, 2006; Fuster, 2002; Stuss, 1992; Stuss & Alexander, 2000). Therefore, one would expect to nd high rates of EF difculties among children with ADHD (Barkley, 2006; Barkley & Murphy, 2010; Nigg, Stavro, et al., 2005; Willcutt, Doyle, Nigg, Faraone, & Pennington, 2005). ADHD is a neural developmental disorder characterized by non-adaptive levels of sustained attention, impulsiveness and hyperactivity (DSMIV, 2001). Inherent in this description are difculties in EF, particularly self-regulation difculties and uninhibited behavior. Since Barkley (1997) rst published the model of inhibitory control as the basis of executive dysfunction (EDF) in ADHD, this issue has been extensively investigated. Some have argued that inefcient regulatory control or delay aversion explain attention disorders and EF difculties (Sonuga-Barke, 2005; Sonuga-Barke, Sergeant, Nigg, & Willcutt, 2008; Thorell, 2007),

* Corresponding author. E-mail address: mayyan74@walla.com (M. Shimoni). 0891-4222/$ see front matter 2012 Published by Elsevier Ltd. doi:10.1016/j.ridd.2011.12.014

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whereas others claimed that EDF are caused by energetic factors (Sergeant, 2000). Studies further examined whether EDF are a co-morbidity or a core symptom in ADHD (Barkley, Murphy, & Fischer, 2008; Beiderman et al., 2006; Nigg, Willcutt, Doyle, & Sonuga-Barke, 2005). Either way, most studies found EDF to be a main component of ADHD (Barkley, 2006; Castellanos & Tannock, 2002; Pennington & Ozonoff, 1996; Willcutt, Doyle, et al., 2005; Willcutt, Pennington, Olson, Chhabildas, & Huslander, 2005). Difculties in EF have far-reaching everyday implications and inuence academic achievement, social competence and professional occupation (Barkley & Murphy, 2010; Canu, Newman, Morrow, & Pope, 2008; Graaf, Kessler, Fayyad, Have, Alonso, Angermayer, Borges et al., 2008; Hale et al., 2011; Massetti et al., 2008; Rogers, Hwang, Toplak, Weiss, & Tannock, 2011). Given that children with ADHD often show poor skills in these areas, assessing EF is most relevant for clinicians and for research purposes. Moreover, assessments should have a wide perspective and include everyday behavior contexts along with specic skill measurements. To address this issue, two types of EF assessments are in use: performance-based assessments (PBT) and everyday function assessments. PBT include tests that are administered under laboratory conditions and relate to specic EF skills. Among these tests are the commonly used Continuous Performance Tests (CPT) (Conners, 1997), Wisconsin Card Sorting Test (WCST) (Kimberg, DEsposito, & Farah, 1997), Tower of Hanoi (Borys, Spitz, & Dorans, 1982), Walk Dont Walk (Manly, Robertson, Anderson, & Nimmo-Smith, 1999), Trail-Making tests (Dellis, Kaplan, & Kramer, 2001) and others. These PBTs are benecial for identifying specic executive difculties and are used in various studies that compare EF between typical children and children with ADHD (Frazier, Demareem, & Youngstrom, 2004; Hervey, Epstein, & Curry, 2004). However, they lack ecological validity and do not express everyday EF. Designed to be administered under laboratory conditions, they lack different attributes that are inherent to the routine use of EF, such as motivation, emotion control and sustained attention in natural distractions. On the other hand, everyday function assessments evaluate everyday demands of EF in the natural setting. Parents, teachers, caregivers, or the person with the disorder are asked to describe the behavior related to EF. These assessments are rooted in the client/family-centered approach, according to which the perception of abilities and disabilities should be understood from the individuals point of view (Law, Baptiste, & Mills, 1998; Woodside, Rosenbaum, King, & King, 2001). Among these assessments, especially those referring to childrens assessments are parent and teacher questionnaires and check-lists. Referring to the way EF decits are expressed in daily life scenarios is of supreme importance and ts the ICF framework (WHO, 2000). Accordingly, disabilities should be related to the everyday context rather than to the specic skill decits. Anchored in this updated framework, the Behavioral Rating Inventory of Executive Functions (BRIEF) (Gioia, Isquick, Guy, & Kenworthy, 2000) was designed to test EF in everyday life situations as perceived by parents and teachers. Using various questionnaire assessments, EF were found to discriminate between children with ADHD and typical children (Jarratt, Riccio, Siekierski, 2005; McCandless & Olaughlin, 2007). Nevertheless, family and parent perceptions of the childs disabilities are essential for diagnostic and intervention purposes, and cannot rely solely on potentially biased parent or teacher reports. Although various studies found poor EF among people with ADHD (Berlin, Bohlin, Nyberg & Janols, 2004; Nigg, Stavro, et al., 2005; Sergeant, Geurtz, & Oosterlaan, 2002; Shallice et al., 2002; Willcutt, Pennington, et al., 2005), to the best of our knowledge, only few studies have compared executive skills and their everyday expression. The existing studies show low correlations between PBT meant to test executive skills and questionnaires that examine everyday functions (Bodnar, Prahme, Cutting, Dencla, & Mahone, 2007; Mahone et al., 2002). Yet, the assessments in these studies include a diversity of EF tests, each directed to specic executive skills. The present study is designed to overcome the limitations of previously used EF assessments by using an ecologically valid, comprehensive test together with a validated standardized parent report. In particular, this study aimed to: (a) compare EF of children with ADHD and typical children; and (b) examine the relationships between executive skills (as performed by the children) and executive everyday functions (as reported by the parents). Our hypotheses were that using the Behavioral Assessment of Dysexecutive Functions for Children (BADS-C) and the BRIEF would reveal signicant low executive skills and functions among the boys with ADHD compared to typical boys and that the BADS-C and BRIEF scores of all study participants would be signicantly correlated in some aspects and complementary in others. 2. Method 2.1. Participants A total of 50 Israeli boys aged 811 years (age range in months 96130; mean 110.0; SD 10.09) participated in the study. The study group comprised 25 boys with ADHD with either: hyperactive-impulsive, inattentive or combined type. Participants were recruited from several clinics in the north of Israel through convenience sampling. Diagnosis of ADHD subtype was made by neurologists according to the DSM-IV criteria, and severity was assessed using other clinical assessments such as the Conners Rating Scales-Revised CPRS-R (Conners, 1997). The group included 25 typically developing boys who were recruited as a convenience sample. All participants attended mainstream elementary schools, were Hebrew speaking, and came from diverse socioeconomic backgrounds. The study group and the control group were matched by age, socioeconomic background, place of residence and religion. Boys with known chronic health conditions (except for ADHD) or with another associated formally diagnosed

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disorder such as depression or anxiety (DSM-TR) were excluded from the study. As ADHD symptoms may differ between boys and girls (Biederman et al., 2002; Gaub & Carlson, 1997), the study focused on boys only. 2.2. Measurements 2.2.1. Demographic questionnaire Demographic questionnaire pertaining to participants personal data such as age, school grade, socioeconomic level, learning difculties and health status. This questionnaire was administered to the childrens parents. 2.2.2. Behavior Assessment of Dysexecutive Syndrome for Children (BADS-C) Behavior Assessment of Dysexecutive Syndrome for Children (BADS-C) (Emslie, Wilson, Burden, Nimmo-Smith, & Wilson, 2003), designed to assess EF among children and adolescents from 8 to 16 years old. The BADS-C includes multitasks comprising six subtests. The six subtests examine several aspects of EF: planning, sequence behavior, sustained attention, resistance to interference, feedback utilization, changing sets and dealing with new situations. Standardized scores on each subtest range from 1 to 19. Total score is obtained by summing the six subtest scores (BADS-C manual). Description of the six subtests is as follows: 1. Playing cards test: This assesses the childs ability to change an established pattern of responding. The test uses 21 spiralbound non-picture playing cards that are turned over one at a time. In the rst part of the test, children are instructed to say yes to red cards and no to black cards, and to respond as quickly as possible. In the second part of the task, the rule is changed: The children are asked to say yes if the card is the same color as the one before it and to say no if the card is of a different color from the one before it. This test measures cognitive exibility as the child shifts from one rule to another and also assesses the childs ability to keep track of the color of the previous card and the current rule (BADS-C manual page 7). 2. Water test: The children are asked to extract a cork from a tube full of water using a set of tools. Reaching the solution requires a ve-step plan of action. This test measures mainly the ability to plan a set of actions. 3. Key search: The children are presented with a drawing of a 100 mm square that represents a eld in which they have lost their key. Underneath the square is a dot showing where they are standing. The children are asked to draw a pathway through which it would be reasonable to search for the lost key. This test examines the childrens ability to plan an efcient, systematic plan of action without monitoring. 4. Zoo map 1: The children are asked to plan a pathway on a given zoo map in which they could pass through a list of drawn animals according to a set of rules. This subtest is an open-ended task with little structure that examines the childrens ability to plan. 5. Zoo map 2: Similar to the zoo map 1 subtest, the children are asked to plan a pathway according to the order on the animal list. Planning skills in this test are examined in a rule governed task. 6. Six-part test: Children are given three different color-coded tasks to perform: a green test (simple arithmetic), blue test (picture naming) and red task (sorting). Each of these tasks has two parts. Children have to schedule their time to attempt something from all six parts over a 5-min period with restrictions on the order in which the parts can be attempted. This test examines planning, task scheduling and performance monitoring. Reliability: inter-rater reliability ranging from r = .91 to 1.00 on most tests (except water test r = .53) (BADS-C manual page 9). Discriminative validity was constructed comparing typical children and children with various learning and behavioral disabilities (Baron, 2007). BADS-C discriminate validity was also conrmed in studies which compared EF of persons with intellectual disability to typical controls. For example, Willner, Bailey, Parry, and Dymond (2010) found that participants with IQ impairments scored far below the bottom published scale (page 371) indicating impaired EF. 2.2.3. Behavior Rating Inventory of Executive Functions (BRIEF)-parents The BRIEF is a behavioral rating measure for children of 518 years old, designed to elicit everyday EF, as observed by the parents in natural, everyday environments (Gioia et al., 2000). The BRIEF composes two major index scales: behavioral regulation index (BRI) and metacognition index (MC), in addition to a global executive composite (GEC). Each index is further divided into executive component scales: BRI is composed of inhibition, shift and emotional control scales, whereas MC is composed of initiation, working memory, planning, organization of materials, and monitoring scales. A total of 86 statements describe various behaviors in which the parent rates the behavior frequency on a Likert Scale ranging from 1 (rare) to 3 (often). Total scores are revised into standardized scores: scores above 60 reect executive impairments. Testretest reliability r = .86 for GEC, r = .88 for BRI, r = .84 for MC (Gioia et al., 2000). 2.3. Procedure The study was approved by the Helsinki ethics committee of the Bnai Zion Medical Center. Parents signed an informed consent form and the childs informed consent was obtained. The control group was recruited through an advertisement published in several neighborhoods in the north of Israel calling for participating in a study about EF among boys

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in elementary school. Each participant completed the BADS-C while parents lled in the BRIEF questionnaire in a nearby room. 2.4. Data analysis t-Tests were applied on BRIEF and BADS-C total scores, and on BADS-C subtests. Given the signicant correlations between the BRIEF scales and subscales, MANOVA was applied on these variables. Pearson test was applied to compute correlations between BADS-C and BRIEF total scores and subtests/scales for all participants. 3. Results 3.1. EF comparison between ADHD and typical boys 3.1.1. Executive functions assessed by BADS-C performance-based test Analysis indicated that compared to the typical group, the ADHD group scored signicantly lower on the total score and on four subtests: Water, Key, Zoo 1 and Zoo 2. On two subtests, however, Cards and Six-part, no signicant differences were found between the groups (Table 1). 3.1.2. Executive functions assessed by BRIEF parent questionnaire Analyses indicated lower EF among boys with ADHD compared to typical boys on the BRIEF total score (GEC) and on both MC and BRI. Lower EF was also found among ADHD boys on all subscales, with the exception of Attention shift and Organization (see Table 2). 3.2. Correlations between PBT and parent report Signicant correlations were found between BRIEF and BADS-C total scores and between BADS-C total score and BRIEF MC Scale and emotion control, working memory, planning, monitoring and inhibition subscales. No
Table 1 Statistical comparison for the two groups on BADS-C total score and on each BADS-C subscale separately. BADS-C scores Boys with ADHD Mean Total scorea Cards Water Key Zoo 1 Zoo 2 Six-part
*

Boys without ADHD SD 11.24 4.23 3.27 3.28 3.70 5.12 1.52 Mean 66.88 8.80 13.27 9.84 12.08 11.68 6.32 SD 8.21 3.34 2.05 2.32 3.52 2.61 3.67

t-Test

48.36 7.00 10.96 7.32 8.84 8.96 5.92

5.21*** 1.67 2.80** 3.14*** 3.17*** 2.37* .50

p 0.05. p 0.01. *** p 0.001. a Total score range 3585.

**

Table 2 Statistical comparison for the two groups on BRIEF total score and on each index separately. BRIEF scores Boys with ADHD Mean BRIEF total score MC BRI Inhibition Attention shift Emotional control Initiation Working memory Planning Organization Monitoring
* **

Boys without ADHD SD 9.10 9.66 12.33 7.93 15.89 10.00 10.47 10.62 11.59 12.59 10.06 Mean 46.56 45.28 50.64 41.60 63.92 50.16 46.56 46.32 47.32 41.12 39.88 SD 7.06 8.50 7.80 6.18 12.23 8.90 8.19 7.16 7.70 5.32 11.19

F values

59.16 58.88 61.04 50.80 70.52 61.52 56.20 61.16 58.84 41.20 55.28

5.47*** 27.96*** 12.7*** 20.95*** 2.71 18.00*** 13.14*** 33.55*** 17.14*** .001 26.19***

***

p 0.05. p 0.01. p 0.001.

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Table 3 Correlations between BADS-C and BRIEF. BRIEF BADS-C

a

Total score .36

*

MCa .37
**

BRIb .25

ECc .32
*

Working memory .47

**

Plan .46
**

Monitor .41
**

Inhibition .27
**

Organize .25

Initiation .20

Attention shift .06

MC metacognition. b BRI behavioral regulation index. c EC emotion control. * p 0.05. ** p 0.01. *** p 0.001.

signicant correlations were found between BADS-C total score and organization of materials, initiation and attention shift (see Table 3).

4. Discussion The present study examined EF among boys with ADHD and typical peers by comparing executive functions as measured by PBT and as expressed in their parents reports regarding everyday behavior. As hypothesized, in general, boys with ADHD had lower EF according to both measures. 4.1. EF comparison between ADHD and typical boys 4.1.1. Executive functions assessed by BADS-C performance-based test As measured by the BADS-C, compared to typical controls, poor EF were found among boys with ADHD. This supports the ability of BADS-C to reveal EF difculties in this population. Results of the present study are consistent with recent research using other EF assessments (Castellanos, Edmund, Sonuga-Barke, Milham, & Tannock, 2006; Martinussen, Hayden, HoggJhonson, & Tannock, 2005; Nigg, 2001; Pennington & Ozonoff, 1996; Willcutt, Doyle, et al., 2005). However, as opposed to other assessments, the advantages of BADS-C are its ability to test a variety rather than a limited number of EF with the same instrument and its ecological validity. The tests innovation lies in the similarity of its tasks to those required of children and adolescents in everyday life as opposed to the tasks required in many other, more widely used, EF tests (Baron, 2007). Whereas many EF tests evaluate separate EF components in closed-ended tasks, BADS-C subtests include open-ended tasks and enable the children to integrate their various abilities into a purposeful goal-oriented activity (Engel-Yeger, Josman, & Rosenblum, 2009). Although the differences between the performances of the two groups were signicant for the Water, Key search, Zoo 1, and the Zoo 2 BADS-C subtests, on the Card and Six-part subtests, both study groups had similar averages. On the Card subtest, both groups excelled with high scores. This result is probably due to a ceiling effect, whereas the Six-part test seemed to be difcult for the two study groups. The Six-part test involves shift of attention, planning and organization. As shift of attention did not differ in either the Card test, the Six-part test or the BRIEF subscale, it is possible that these attributes are unique to a subgroup of children with ADHD or alternatively, that the present test is not sensitive enough to detect these differences. This issue merits further research. 4.1.2. Executive functions assessed by BRIEF parent questionnaire In line with recent research (Isquick & Gioia, 2000; Jarratt, Riccio, & Siekierski, 2005; McCandless & Olaughlin, 2007; Pratt, 2000), using the BRIEF, parents of children with ADHD reported lower EF as expressed in their childrens everyday behavior. This enables the understanding of further EF implications and removes the assessment from the laboratory to real life. However, as for specic executive skills, results were equivocal: on most metacognition indices and behavior regulation indices, boys with ADHD had signicantly lower executive skills than typical boys. Nonetheless, on the attention shift and organization indices (similar to the BADS-C results), the differences between the two groups were not signicant. Regarding attention shift scores, the similarity between the groups might have resulted from the childrens stage of development. According to Brocki and Bohilin (2004), there are two stages of attention shift maturation: one between the ages 7.6 and 9.5 years and the other between the ages 9.6 and 11.5 years. Similar results were also found by Engel-Yeger et al. (2009). In the present study, childrens age ranged from 8 to 11.5 years and results from both groups indicated difculties in this domain. Thus, differentiating between the children according to their chronological age and subsequent stage of EF maturation might show different results. Referring to the Organization of materials, the similar scores of the two groups can possibly be explained by parents subjectivity. On the BRIEF Organization of materials index, statements include: organizing the closet, etc. It is possible that organizing materials does not depend on executive abilities but on familial habits or parents attitude. This explanation is indirectly supported by previous studies (Isquick & Gioia, 2000; Jarratt, Riccio, & Siekierski, 2005), showing disagreements between parent and teacher rating in this subscale. As Organization of materials relies on external support, this might be the

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underlying factor explaining both the parents rating in the present study and the lack of agreement between the two measures in recent studies. In the past decade, an increasing number of intervention programs emerge from the family-centered approach. According to this approach, attitudes, beliefs and routines differ from family to family and should be considered in the evaluation process and in constructing therapy (Law et al., 1998; Woodside, Rosenbaum, King & King, 2001). Hence, using the BRIEF may enhance parents awareness, involvement in therapy and interactions with their child. All of this may lead to optimal therapeutic results expressed in the childs better performance in daily living. 4.2. Correlations between PBT and parent report The second goal of the present study was to examine the executive skills as assessed by the laboratory test and their relationships to everyday executive functions. This goal was based on the World Health Organization new ICF (WHO, 2001), dening the relationships between skill acquisition and everyday functions as the basis of health and sickness. As was hypothesized, BADS-C and BRIEF scores were signicantly correlated indicating that EF (low as well as normal scores) have everyday expressions that are observed by parents. These results are only partially in line with previous research. Toplak et al. (2009) tested the associations between PBT and BRIEF in adolescents, using the Stop task-SSRT, trail making, verbal and memory composite, and Stockings of Cambridge standard scores. Every one of these tests was independently applied. Their results showed that although overall correlations were found, each measure was not correlated with its respective BRIEF subscale. Likewise, Barkley and Murphy (2010) tested self-reports of EF and EF tests as predictors of occupation functions among adults with ADHD. Although several EF tests were signicant predictors of function impairments, EF self-ratings had substantially more contribution. However, as opposed to the specic skill PBT used in these previous studies, BADS-C uniqueness is expressed in its integration of simultaneous executive functions in each subtest. Although total scores were related between BRIEF and BADS-C, BADS-C was signicantly correlated only with BRIEF metacognition but not with BRI index. Two explanations are possible: rst, the nature of the BADS-C subtests; second, the connection between EF decits and ADHD subtypes. In natural settings, behavior regulation includes affective characteristics and processes such as maintenance of motivation, goal-oriented behavior or response to distractions. BADS-C tasks are administered in short sessions, over a limited time, with a constructed goal and therefore do not involve behavior regulation as it is expressed in everyday functions. Alternatively, the BADS-C tasks do require problem-solving processes that rely on metacognition. Moreover, factors such as familiarity with the task and the consequent degree of automatic performance, as are required in the BRIEF, may have been the cause of the differences. The second explanation refers to the relationship between ADHD subtypes and EF decits. Whereas the ADHD-inattentive subtype is associated with metacognition difculties, BRI difculties are related to the ADHD-combined subtype (Isquick & Gioia, 2000; McCandless & Olauplin, 2007). Due to the small sample of participants, we could not conrm this hypothesis. To conclude this issue, in general, both assessments indicated difculties in EF in children with ADHD; these difculties were present in test performance and in parents reports regarding childrens everyday behavior. The fact that each assessment emphasizes different aspects of EF supports the need to combine the two assessments in the evaluation procedure. Evaluating how specic difculties are expressed in daily living, referring to parents reports together with evaluating the childrens performance can assist in dening therapeutic goals related to the childrens and familys real life situations, applying the childrens abilities to actual daily activities. 4.3. Research limitations The study had limitations and further research is needed. First, a larger sample would facilitate demonstration of possible differences between ADHD subtypes, age and other related variables (August & Garnkel, 1989; Lockwood, Marcotte, & Stern, 2001; Marshall, Schafer, ODonnell, Elliot, & Handwerk, 1999; Nolan, Volpe, Gadow, & Sprafkin, 1999). Furthermore, the use of a teachers report in addition to the parents report may shed more light on the value of EF assessment as related to school performance, thereby increasing the signicance of this assessment. An additional intriguing challenge is to nd a clinical performance-based measure that assesses the behavioral regulation (such as motivation and initiation) to accompany the assessment of metacognition and everyday EF. 5. Conclusion In conclusion, boys with ADHD show lower EF abilities than typical peers according to both PBT and parent report BADSC and BRIEF. The combination of an ecological assessment such as the BADS-C, together with parents reports about childrens real-life performance may facilitate an integrative and ecologically more valid delineation of the childrens weaknesses and strengths and consequently a more effective intervention. Thus, it is recommended to use both childs evaluations and parents reports in the evaluation process. This may also enhance childrens and parents awareness of difculties that arise from limited EF abilities, assist in providing them with strategies to deal with these difculties in daily living, and strengthen the involvement of both children and parents in the therapeutic process.

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