University of Groningen ADHD and its relationship to comorbidity … · 2016-03-09 · (e) is often “on the go” or often acts as if “driven by a motor” (f) often talks excessively

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ADHD and its relationship to comorbidity and genderJónsdóttir, Sólveig

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ADHD and its relationship to comorbidity and gender

Sólveig Jónsdóttir

The studies presented in this dissertation were funded in part by:

1) Vísindasjóður Landspítala-háskólasjúkrahúss2) Sjóður Odds Ólafssonar, Öryrkjabandalagi Íslands3) Minningarsjóður um Ólafíu Jónsdóttur, Geðverndarfélagi Íslands

ADHD and its relationship to comorbidity and gender/Sólveig Jónsdóttir Thesis Rijksuniversiteit Groningen, Groningen, The Netherlands, with summary in Dutch and Icelandic

ISBN 9979-70-166-8ISBN 978-9979-70-166-8

Copyright 2006, Sólveig Jónsdóttir. All rights reserved

Printed in Iceland by Íslandsprent

Cover illustration is Anne Marie Trechslin’s rendering of the rose “Josephine Bruce”

RIJKSUNIVERSITEIT GRONINGEN

ADHD and its relationship to comorbidity and gender

PROEFSCHRIFT

ter verkrijging van het doctoraat in de

Medische Wetenschappen

aan de Rijksuniversiteit Groningen

op gezag van de

Rector Magnificus, dr. F. Zwarts,

in het openbaar te verdedigen op

woensdag 27 september 2006

om 14:45 uur

door

Sólveig Jónsdóttir

geboren op 24 mei 1949

te Reykjavik, IJsland

�

Promotores:

Beoordelingscommissie:

Prof.dr. E.J.A. Scherder

Prof.dr. J.M. Bouma

Prof.dr. J.A. Sergeant

Prof.dr. H. Swaab

Prof.dr. P. van Geert

Prof.dr. R. Minderaa

�

To my husband and children:

Gestur

Erla Sigríður

Ása Fanney

Þorgeir

Jón Gunnlaugur

�

CONTENTS

1. Introduction ......................................................................................................................... 7

2. Gender differences in symptoms of ADHD and associated factors as rated by parents and teachers in an Icelandic normal population ............................................................................................................. 17

Submitted

3. The impact of specific language impairment on working memory in children with ADHD combined subtype ...................................................... 41ArchivesofClinicalNeuropsychology,2005,20,443-456

4. Relationships between neuropsychological measures of executive function and behavioural measures of ADHD symptoms and comorbid behaviour ................................................................................ 59ArchivesofClinicalNeuropsychology,inpress,availableonline28July,2006

5. Effects of transcutaneous electrical nerve stimulation (TENS) on cognition, behaviour, and the rest-activity rhythm in children with attention deficit hyperactivity disorder, combined type .................................................................................................... 81

NeurorehabilitationandNeuralRepair,2004,18,212-221

6. Summary and general discussion..................................................................................... 99 Nederlandse samenvatting (Summary in Dutch) ......................................................... 109

Samantekt á íslensku (Summary in Icelandic) ............................................................. 119

Words of thanks ............................................................................................................... 129

Curriculum vitae ............................................................................................................. 133

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CHAPTER ONE 1Introduction

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INTRODUCTION

Attention deficit hyperactivity disorder (ADHD) is the most common neuropsychiatric disorder of childhood and constitutes approximately 50% of referrals to child and adolescent mental health clinics. The disorder is associated with negative impact on families and both academic and vocational outcomes. Estimated prevalence is approximately 3%-7% in school-age children according to the DiagnosticandStatisticalManualofMentalDisorders, Fourth Edition, Text Revision (DSM-IV-TR), published by the American Psychiatric Association in 2000, but rates of ADHD vary depending on race and ethnicity, gender, and age. Diagnostic rates are on the increase with accompanying financial burden to health care services.

Diagnostic features

The main diagnostic features of ADHD are age inappropriate symptoms of inattention, motor restlessness and impulsivity. According to the DSM-IV the diagnostic criteria for ADHD are the following:A. Either (1) or (2):

(1) Symptoms of inattention (six or more of the following symptoms must have persisted for at least 6 months to a degree that is maladaptive and inconsistent with developmental level)

(a) often fails to give close attention to details or makes careless mistakes in schoolwork, work, or other activities

(b) often has difficulty sustaining attention in tasks or play activities(c) often does not seem to listen when spoken to directly(d) often does not follow through on instructions and fails to finish schoolwork,

chores, or duties in the workplace (not due to oppositional behaviour or failure to understand instructions)

(e) often has difficulty organizing tasks and activities(f) often avoids, dislikes, or is reluctant to engage in tasks that require sustained

mental effort (such as schoolwork or homework)(g) often loses things necessary for tasks or activities (e.g., toys, school assignments,

pencils, books, or tools(h) is often easily distracted by extraneous stimuli(i) is often forgetful in daily activities

(2) Symptoms of hyperactivity (six or more of the following symptoms must have persisted for at least 6 months to a degree that is maladaptive and inconsistent with developmental level)

(a) often fidgets with hands or feet or squirms in seat(b) often leaves seat in classroom or in other situations in which remaining seated is

expected

Introduction

Chapter one

10

(c) often runs about or climbs excessively in situations in which it is inappropriate (in adolescents or adults, may be limited to subjective feelings of restlessness)

(d) often has difficulty playing or engaging in leisure activities quietly(e) is often “on the go” or often acts as if “driven by a motor”(f) often talks excessively

Symptoms of impulsivity(g) often blurts out answers before questions have been completed(h) often has difficulty awaiting turn(i) often interrupts or intrudes on others (e.g., butts into conversations or games)

B. Some symptoms of hyperactivity/impulsivity or inattention that caused impairment were present before age 7 years.C. Some impairment from the symptoms is present in two or more settings (e.g., at school [or work] and at home).D. There must be clear evidence of clinically significant impairment in social, academic or occupational functioning.E. The symptoms do not occur exclusively during the course of a Pervasive Developmental Disorder, Schizophrenia, or other Psychotic Disorder and are not better accounted for by another mental disorder (e.g., Mood Disorder, Anxiety Disorder, Dissociative Disorder, or a Personality Disorder).

The DSM-IV delineates three subtypes of the disorder according to the level of presenting symptoms; ADHDCombinedType if 6 or more symptoms of both inattention and hyperactivity/impulsivity symptoms have been present for the past 6 months, ADHDPredominantly Inattentive Type if only 6 or more symptoms of inattention have been present for the last 6 months,ADHDPredominantlyHyperactive-ImpulsiveTypeif only 6 or more symptoms of hyperactivity/impulsivity have been present for the last 6 months.

Gender differences

Epidemiological studies have shown that ADHD is more prevalent in males than in females. The male-to-female ratio is greater in clinic based samples (9:1) than in community based (2:1). Most studies in the past have relied on male subjects and identification of girls with ADHD has been hampered by parental and teacher bias, and confusion. Studies have shown that there are some cultural variations in how ADHD symptoms and associated problems are assessed with respect to gender. Girls are more likely to be inattentive without being hyperactive or impulsive, compared to boys (Staller & Faraone, 2006). There may be less gender differences in the PredominantlyInattentiveTypethan in the other two subtypes. Chapter 2 of this thesis examines gender differences in ADHD symptoms and associated problems in a normal Icelandic school sample. This is the first study to assess these disorders in an Icelandic normal sample using the Behavior Assessment System for Children (BASC).

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Comorbidity

ADHD is often associated with other disorders. Approximately half of clinic-referred children with ADHD also have problems associated with aggression (oppositional defiant disorder (ODD) or conduct disorder (CD)). Internalizing problems are also common, with approximately 25% or more of ADHD children suffering from mood and anxiety disorders, and at least 20% to 25% meet criteria for a learning disorder (Barkley, 1998; Biederman, 2005; Pliszka, 1998).

All three subtypes of ADHD are associated with significant impairment but in differing degrees. Academic deficits and school-related problems are mostly associated with the types with inattention problems (the PredominantlyInattentiveType and the CombinedType). Peer rejection and accident proneness are more associated with hyperactive/impulsive symptoms (Hyperactive-Impulsive and Combined Types). Children with the Predominantly Inattentive Type tend to be socially passive and seem to be neglected rather than rejected by peers. Research during the last three decades has tended to rely on the CombinedType of ADHD. As a result more studies of the InattentiveType have been called for, especially since it might include a higher proportion of girls, than the subtypes with hyperactivity/impulsivity (National Institutes of Health, 1998).

Sleeping disorders are a frequent comorbidity in children with ADHD and used to be a diagnostic criterion in previous versions of the DSM (American Psychiatric Association, 1980). It has been estimated that as many as 25% to 50% of children and adolescents with ADHD have sleep problems compared to 7% of normal controls. ADHD children have been shown to have more movements during sleep and to have a more unstable sleep-wake system than normal children. They have also been shown to spend less time in rapid eye movement (REM) sleep than other children. Many studies have shown that sleep fragmentation has a negative effect on neurobehavioral functioning. Recent studies have indicated that the system that is the most sensitive to sleep deprivation, sleep disorders, or reduced alertness, is executive control, which is mainly located in the prefrontal cortex. Of note is, that methylphenidate treatment has been found to increase sleep disturbances in children with ADHD (Schwartz, 2004).

It has been argued that the most parsimonious approach to diagnosing comorbidities in ADHD is by using rating scales that have broad coverage of symptoms (Pelham et al., 2005).

The role of executive functions in ADHD

In spite of decades of research, the causes of ADHD are still unknown. Twin, adoption, and molecular genetic studies have shown it to be highly heritable, and evidence from animal and human studies implicates the dysregulation of frontal-subcortical-cerebellar catecholaminergic circuits in the pathophysiology of ADHD. Several neuropsychological theories of ADHD have been proposed. One of the most prominent suggests that its symptoms arise from a primary deficit in executive functions (EFs), defined as

Introduction

Chapter one

12

“neurocognitive processes that maintain an appropriate problem-solving set to attain a later goal”. Russell Barkley (1997) has argued that the various deficits observed in ADHD, including apparent attention problems, are caused by one main feature: Impairment in the development of delayed responding, or response inhibition. He has put forth a theory that specifies that behavioural inhibition facilitates the effective performance of four EFs: Working memory, internalization of speech, self-regulation of affect-motivation-arousal, and reconstitution (behavioural analysis and synthesis). These four EFs influence the motor system in the service of goal-directed behaviour and originate within the brain’s motor system (prefrontal and frontal cortex). The prefrontal cortex and its connections with the striatum play an important role in EFs. One of the EFs purported to be deficient in ADHD according to Barkley’s model, i.e. working memory, is also deficient in other common childhood disorders, including specific language impairment (SLI). Since ADHD is highly comorbid with SLI and the core problem in SLI is considered to be deficient verbal working memory, the main goal of Chapter 3 is to examine what impact comorbid SLI has on both verbal and spatial working memory in children with DSM-IV CombinedType ADHD.

Diagnostic procedures

The American Academy of Pediatrics (AAP) has developed clinical practice guidelines for the diagnosis of ADHD in children aged 6-12 years old (AAP, 2000). These guidelines emphasize: 1) the use of explicit criteria for the diagnosis using DSM-IV criteria; 2) the importance of obtaining information regarding the child’s symptoms in more than one setting and especially from schools; and 3) the search for coexisting conditions that may make the diagnosis more difficult or complicate treatment planning. Procedures conventionally used in the diagnostic process of ADHD include 1) parent and teacher ratings of ADHD symptoms, 2) an in-depth diagnostic interview with parents and 3) a clinical assessment of the child involving an interview and/or psychological evaluation. A recent article (Pelham et al., 2005), examining evidence-based practices for ADHD, concluded that the most efficient assessment method is obtaining information through parent and teacher rating scales. It was also concluded that no incremental validity or utility was conferred by structured interviews when parent and teacher ratings are utilized. It was argued that DSM diagnoses per se have not been shown to have treatment utility, so minimal time and expense should be spent on the diagnostic phase of assessment, but more resources focused on other aspects of assessment, especially treatment planning.

To date there is no consensus on which rating scales and which psychological tests should be used in the evaluation of ADHD symptoms. Studies have furthermore shown that generally there is little agreement between the various measures used to assess the main constructs in ADHD that is inattention, hyperactivity and impulsivity. In Chapter 4 the relationships between parent and teacher ratings of ADHD symptoms and associated problems and performance on tests of EF, intelligence and language development, were examined.

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Treatment

Stimulant drug therapy is the most frequently used and the most effective therapy known today for ADHD. The limitations of stimulant drug therapy are that although it helps 65% to 75% of ADHD children, there are many nonresponders, there are some side effects, there is an abuse potential, there are wear-off or rebound effects, it may increase sleep disturbances, and many parents are reluctant to give their children drugs. While short-term trials of stimulants have shown beneficial effects on the defining symptoms of ADHD and associated aggressiveness, findings consistently show that in spite of improvement in the core symptoms, there is little improvement in academic achievement or social skills (National Institutes of Health, 1998). In view of these limitations, it is of utmost importance to seek and develop safe alternative nonpharmacological types of stimulations for ADHD. One way of stimulating the central nervous system externally is by using peripheral electrical nerve stimulation applied to the skin. In the past decades, the effects of peripheral electrical stimulation in Alzheimer’s disease (AD) have been studied in a series of placebo-controlled experiments. Improvements were found in certain aspects of cognition, behaviour, and the rest-activity rhythm. In Chapter 5 the results of a study on the effects of peripheral electrical stimulation on symptoms of ADHD are presented.

Summary and aims of this thesis

ADHD is the most commonly diagnosed neuropsychiatric disorder of childhood, constituting about half of all referrals to child and adolescent mental health clinics. It impairs educational and vocational endeavours and has lasting effects into adulthood. Diagnostic rates are on the increase with accompanying increase in medical prescriptions causing enormous financial burden to health care services. Etiology is not known at this time in spite of vigorous research during previous decades. Studies have shown that there are important differences in symptomatology as a function of comorbidity and gender. The most common comorbidities are related to aggression and language based learning problems. Subtypes differ with respect to comorbidity. Hyperactive/impulsive symptoms are mostly associated with aggression while inattentive symptoms are mostly related to learning problems. There are gender differences that vary according to culture, community or clinical settings. Boys are much more numerous than girls in clinical samples, but to a lesser degree in community samples. Boys have generally been shown to have higher rates of hyperactivity/impulsivity and aggressive symptoms while there is less gender difference in inattentive symptoms and learning problems. There is to date no consensus on which instruments to use in the diagnostic process of the disorder and there is little agreement between the various measures used to assess ADHD symptoms. The most common and effective therapy is stimulant medication, which does not help everyone, has some side effects, and is not an option for many parents. In view of this status of affairs it is of great importance that diagnostic criteria, methods of diagnosis and

Introduction

Chapter one

1�

diagnostic measures used are refined and specific and that additional therapeutic methods are sought.

In summary, this thesis tried to expand on previous knowledge of the subject by examining:

1) To what extent normal Icelandic girls and boys differ with respect to ADHD symptomatology and associated features as rated by parents and teachers (Chapter 2).

2) The impact that comorbid specific language impairment (SLI) has on working memory in ADHD (Chapter 3).

3) To what extent neuropsychological and behavioural measures of ADHD symptoms agree (Chapter 4).

4) The effects of transcutaneous electrical nerve stimulation (TENS) on cognition, behaviour and the rest-activity rhythm in children with

ADHD (Chapter 5).

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REFERENCES

American Academy of Pediatrics (2000). Clinical practice guideline: Diagnosis and evaluation of the child with attention-deficit/hyperactivity disorder. Pediatrics,105, 1158-1170.

American Psychiatric Association (1980).DiagnosticandStatisticalManualofMental Disorders,3rd ed. Washington, DC: Author. American Psychiatric Association (2000). DiagnosticandStatisticalManualofMental

Disorders,4th ed. Text Revision. Washington, DC: Author.Barkley, R.A. (1997). Behavioral inhibition, sustained attention, and executive functions:

Constructing a unifying theory of ADHD. PsychologicalBulletin,121, 65-94.Barkley, R.A. (1998). Attention-deficithyperactivitydisorder:Ahandbookfordiagnosis

andtreatment,2nd ed. New York: Guilford Press.Biederman, J. (2005). Attention-deficit/hyperactivity disorder: A selective overview.

BiologicalPsychiatry,57, 1215-1220.National Institutes of Health (1998). Diagnosis and treatment of attention deficit

hyperactivity disorder (ADHD). NIH Consensus Statement,16, 1-37.Pelham, W.E. Jr., Fabiano, G.A., & Massetti, G.M. (2005). Evidence-based assessment

of attention deficit hyperactivity disorder in children and adolescents. JournalofClinicalChildandAdolescentPsychology,34, 449-476.

Pliszka, S.R. (1998). Comorbidity of attention-deficit/hyperactivity disorder with psychiatric disorder: An overview. TheJournalofClinicalPsychiatry,59, 50-58.

Schwartz, G., Amor, L.B., Grizenko, N., Lageix, P., Baron, C., Boivin, D.B., & Joober, R. (2004). Actigraphic monitoring during sleep of children with ADHD on methylphenidate and placebo. Journalof theAmericanAcademyof ChildandAdolescentPsychiatry,43, 1276-1282.

Staller, J. & Faraone, S.V. (2006). Attention-deficit hyperactivity disorder in girls:Epidemiology and management. CNSDrugs,20, 107-123.

Introduction

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CHAPTER TWO 2Gender differences in symptoms of ADHD and associated factors in normal Icelandic children as rated by parents and teachers

Solveig Jonsdottir, Anke Bouma, Sigurlin H. Kjartansdottir, Pieter-Jelle Vuijck, Joseph A. Sergeant, Erik J.A. Scherder

Submitted

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ABSTRACT

Objective: To examine gender differences in symptoms of attention deficit hyperactivity disorder (ADHD) and associated factors as rated by parents and teachers in a sample of normal Icelandic children.

Method: A school-based sample of 115 children (68 boys and 47 girls), aged 6 to 11 years old, was evaluated by their parents and teachers with the Behavior Assessment System for Children (BASC).

Results: Parents and teachers rated boys significantly higher than girls on hyperactivity/impulsivity and aggression symptoms. Teachers rated boys higher than girls on inattention symptoms but parents did not. Externalizing problems best predicted hyperactivity/impulsivity symptoms and internalizing problems and learning problems best predicted inattention symptoms in both boys and girls. There was a significant correlation between parents’ and teachers’ ratings of ADHD symptoms in boys but not in girls.

Conclusion: More externalizing behaviours of boys than girls may be inflating their ratings of ADHD symptoms, especially among teachers. The clinical relevance of the observed poor concordance between parents and teachers in their reports of ADHD symptoms in girls is discussed.

Chapter Two

Gender differences in symptoms of ADHD

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INTRODUCTION

Attention deficit hyperactivity disorder (ADHD) is the most commonly diagnosed neuropsychiatric disorder of childhood, and is associated with serious academic and behavioural problems, that in many cases impair the quality of life throughout, for the inflicted individuals (Barkley, 2002: Klassen et al., 2004). The main characteristics of the disorder are inattention, hyperactivity and impulsivity. The DSM-IV-TR(American Psychiatric Association, 2000), differentiates three subtypes of the disorder according to levels of presenting symptoms: The predominantly inattentive subtype (ADHD-I), the predominantly hyperactive-impulsive subtype (ADHD-HI), and the combined subtype (ADHD-C).

Prevalence rates of ADHD range between 1% to 12% of school-aged children depending on the stringency of criteria used and the settings and cultures examined (American Academy of Pediatrics, 2000; American Psychiatric Association, 2000; Brewis & Schmidt, 2003; Hudziak et al., 1998; Leung et al., 1996; Swanson et al., 1998). The ratio of boys versus girls with symptoms of ADHD ranges from 2-3:1 in community samples to 9:1 in clinical samples (American Psychiatric Association, 2000), while equal gender distribution has been found in studies of adult ADHD (Biederman et al., 1994; Hartung & Widiger, 1998). Because of the much higher rates of boys in clinical samples, research on ADHD has tended to rely on male subjects (Arnold, 1996).

ADHD is highly comorbid with other externalizing disorders (oppositional defiant disorder (ODD) and conduct disorder (CD)), internalizing disorders (depression and anxiety disorders), and cognitive disorders (language impairment and learning disorders) (American Psychiatric Association, 2000; Barkley, 1998; Cohen, 2000). This high rate of comorbidity has led some researchers to question the validity of the ADHD diagnosis (Hudziak, 1998). The three subtypes of ADHD have shown differing degrees of associated behavioural and learning variables (e.g. Chhabildas et al., 2001; Decker et al., 2001; Gaub & Carlson, 1997a; Lockwood et al., 2001; Marshall et al., 1999; Schmitz et al., 2002; Todd et al., 2002; Warner-Rogers et al. 2000; Weiss et al., 2003; Willcutt et al., 1999; Wolraich et al. 1996; Wolraich et al. 2003). Generally the ADHD-I subtype has been found to have more internalizing problems, learning disorders and speech and language problems and to have less serious behavioural impairment than the ADHD-HI and the ADHD-C subtypes. The ADHD-HI type is characterized by behavioural problems and minimal cognitive impairment. The ADHD-C type has been found to have problems with both learning and behaviour and represents the most serious form of the disorder with the worst prognosis (e.g., Faraone et al., 1998; Todd et al., 2002; Willcutt, 1999; Wolraich et al. 1996). It has been suggested that symptoms of inattention, rather than symptoms of hyperactivity/impulsivity, are associated with neuropsychological impairment in children with ADHD (Chhabildas et al., 2001). The most common subtype in community samples, for both sexes, is the ADHD-I, while the most frequent subtype in clinical samples, for both girls and boys, is the ADHD-C subtype (Biederman, 2004; Crystal et al., 2001; Gaub

Chapter two

20

& Carlson, 1997a; Hudziak, 1998; Wolraich et al., 1996). In clinical samples, girls with ADHD have been found to be 2.2 times more likely to be diagnosed as ADHD-I, than boys with ADHD (Biederman, 2004).

According to DSM-IV, symptoms of ADHD have to be present in multiple settings to fulfil diagnostic criteria. This requirement is customarily met by obtaining information about the child’s behaviour from both parents and teachers. Concordance between parents’ and teachers’ ratings of children’s behaviour have generally been found to be modest (e.g. Achenbach et al., 1987; McNamara et al., 1994; Mitsis et al., 2000; Montiel Nava & Pena, 2001; Sherman, 1997). Achenbach et al. (1987) found for example only a mean correlation of .28 between ratings of parents and teachers in a meta-analytic study. In most, if not all studies on agreement between parents’ and teachers’ assessments of children’s behaviour problems, boys and girls are treated as onegroup. To the authors’ best knowledge, no studies have been conducted so far that examine if agreement between parents and teachers vary as a function of gender.

Studies of sex differences in ADHD symptoms have most commonly been examined with various behavioural rating scales. These studies have typically found that boys in general have higher elevations of hyperactive/impulsive and inattentive symptoms than girls, both according to parents and teachers (Abicoff et al., 2002; Jackson & King, 2004; Magnusson et al., 1999). Other studies have shown different results indicating that ADHD symptoms can be assessed differently depending on both culture and rater (e.g. Brewis, 2002; Brewis & Schmidt 2003; Esparo et al., 2004; Gomez et al., 1999). Esparo et al. (2004) found for example that 6-year-old Spanish girls had significantly more borderline problems than boys and also tended to have more externalizing problems. In a study on Mexican children Brewis et al. (2003) found that while teachers ascribed more inattention symptoms to boys than girls, parents did not report any differences between boys and girls in symptoms of ADHD.

It has been suggested that because of more overtly aggressive and disruptive behaviour, boys are being referred for ADHD treatment more often than girls. (Abikoff, 2002; Gaub & Carlson, 1997b; Jackson & King, 2004). It has also been suggested that girls with ADHD tend to be inattentive rather than aggressive and disruptive and therefore they may be overlooked by teachers and healthcare providers (Quinn & Wigal, 2004). Aggressive and disruptive behaviour has been found to inflate teachers’ ratings of ADHD (Jackson & King, 2004).

The aim of the current study was to investigate sex differences in symptoms of hyperactivity/impulsivity and inattention, and associated factors in a school-based sample of Icelandic boys and girls between the ages of 6 and 11, as rated by parents and teachers. The ratings scales used were parent and teacher authorized Icelandic-language versions of the Behavior Assessment System for Children (BASC: Reynolds & Kamphaus, 1992). This is the first study that has examined sex differences in ADHD symptoms and associated factors in Icelandic children using the BASC. In view of the current literature it was hypothesized that boys would score higher than girls on hyperactivity/impulsivity and inattention according to both parents and teachers. It was also hypothesized that


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externalizing factors would best predict hyperactive/impulsive symptoms and that learning problems and internalizing factors would best predict inattention symptoms. It was also hypothesized that male-to-female ratio of severe ADHD symptoms would be higher among teachers than parents. Moreover, we were especially interested in possible differences in concordance rates between parents and teachers with respect to gender. It should be emphasized that in the current study we are investigating normal variation in child behaviour but not children affected with ADHD.

METHOD

Participants

A randomized sample of 232 children, aged 6 to 11-year-old was selected from the pupils of an elementary school in Reykjavik, Iceland. The parents of 137 children consented to participate and gave their permission for the children’s teachers to rate their behaviour. Eighteen out of nineteen teachers agreed to rate the children. This procedure provided 115 children (68 boys and 47 girls), aged 6 to 11, who were rated by both their parents and their teachers.

Procedures

The parents of the 115 children participating in the study filled out the Parent Rating Scales (PRS) of the BASC and the teachers of the children filled out the Teacher Rating Scales (TRS). The BASC Enhanced ASSIST computer program (American Guidance Service, 1999) was used to score the forms in order to obtain scales’ raw scores. The raw scores of each scale were subsequently entered into the SPSS program and analyzed.

Instruments

BehaviorAssessmentSystemforChildren(BASC)The BASC is a multimethod, multidimensional measure designed to evaluate numerous

aspects of behaviour, emotions and self-perceptions of children and adolescents aged 2½ to 18 years. It measures both adaptive and problematic dimensions, as well as behaviour linked to ADHD. One of the advantages of the BASC is that, unlike some other commonly used rating scales for children e.g. the Child Behavior Checklist (CBCL), Achenbach, 1991), it measures hyperactivity/impulsivity symptoms and inattention symptoms on two separate scales. Research has shown that the BASC is better suited than the CBCL for predicting ADHD subtypes, especially the predominantly inattentive subtype (Vaughn, Riccio, Hynd, & Hall, 1997). Crystal et al. (2001) using the BASC, performed logistic regression equations to predict membership in control versus ADHD groups, and to discriminate between ADHD subtypes. Results showed that the AttentionProblems scale

Chapter two

22

of the BASC was the most powerful predictor of membership in the ADHD group versus the control group. Contrary to expectations, however, the Aggression scale rather than the Hyperactivity scale emerged as the second most predictive variable of an ADHD diagnosis. The authors did not however do a separate analysis on gender.

The Parent Rating Scales (PRS) of the BASC have nine clinical scales. Three scales called Hyperactivity (including both hyperactivity and impulsivity items), Aggression, and Conduct Problems measure externalizing problems. Three scales called Anxiety,Depression,and Somatization,measure internalizing problems.Three additional scales are calledAttentionProblems, Atypicalityand Withdrawal.

The Teacher Rating Scales (TRS) have in addition to the aforementioned nine scales, a clinical scale called LearningProblems. In this study an additional scale called ADHDsymptomswas formed by combining scores on the Hyperactivityscale and the AttentionProblems scale.

The child form of the BASC (ages 6-11) was used in this study. The scales used in multiple regression analysis were the scales measuring externalizing problems, internalizing problems and learning disorders. On the child form of the BASC, parents and teachers rate 138 and 148 symptoms respectively. Symptoms are rated on a 4-point scale of frequency (never = 0, sometimes= 1, often= 2, and almostalways= 3).

Internal consistency coefficients (Kjartansdottir, 2002) for the BASC Icelandic-language version of the PRS child form range from .52 (Atypicality) to .90 (Depression). The TRS child form correspondingly has coefficients that range from .69 (Withdrawal) to .93 (Aggression).

Statistical analyses

Results were analyzed using the Statistical Package for the Social Science-Windows version 11. Univariate analyses of variance (ANOVA) were used to examine group differences. Pearson correlation coefficients were calculated to test the strength of the linear relationships between the ratings of parents and teachers with respect to boys and girls. Exploratory stepwise regression analyses were performed, using scales measuring externalizing problems, internalizing problems and learning disorders, to establish which variables accounted for the most variability in hyperactive/impulsive and inattentive symptoms. The ratio of boys versus girls with ADHD symptoms ratings exceeding 1½ SD from the combined groups’ mean, according to both parents and teachers, was calculated.


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RESULTS

Difference between boys and girls on the BASC subscales as rated by parents and teachers

One-way analysis of variance (ANOVA) was performed to measure possible differences in subscales’ scores between boys and girls. With respect to the PRS, a significant difference was observed on the subscales Hyperactivity and Aggression, and a trend for the subscale ConductProblems. The difference between both groups on these three subscales was due to higher mean scores for the boys compared to the girls. For means, standard deviations, F and pvalues and effect sizes, see Table 1. Analyses of the scores on the TRS also showed significantly higher scores for boys on the subscales Hyperactivity and Aggression, in comparison with girls. In addition, compared to girls, boys scored significantly higher on the subscale AttentionProblems. For means, standard deviations, F and pvalues and effect sizes, see Table 2.

TABLE 1

Difference between boys and girls on the clinical scales of the BASC Parent Rating Scales. F and pvalues and effect sizes

Boys Girls (n=68) (n=47)

BASC subscales Mean (SD) Mean (SD) F ratio(df=114)

P value Effect Size

Hyperactivity 6.37 (4.01) 4.74 (3.40) 5.135 .025 .21

Aggression 8.40 (3.78) 6.96 (3.89) 3.935 .050 .18

ConductProblems 2.49 (2.16) 1.81 (2.09) 2.797 .097 .16

Anxiety 7.32 (3.99) 8.17 (5.16) .983 .324 .09

Depression 4.87 (4.36) 5.45 (5.63) .385 .536 .06

Somatization 4.38 (3.12) 4.13 (2.92) .195 .659 .04

Atypicality 2.49 (2.48) 2.17 (1.87) .544 .463 .07

Withdrawal 5.25 (3.29) 5.51 (2.94) .190 .664 .04

AttentionProblems 6.15 (3.75) 5.09 (3.41) 2.399 .124 .15

ADHDsymptoms¹ 12.50 (6.93) 9.83 (5.72) 4.741 .032 .21

¹ ADHDsymptoms = Hyperactivity and AttentionProblems scales combined

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TABLE 2

Difference between boys and girls on the clinical scales of the BASC Teacher Rating Scales.

F and pvalues and effect sizes

Boys Girls (n=68) (n=47)

BASC subscales Mean (SD) Mean (SD) F ratio(df=114)

P value Effect Size

Hyperactivity 8.85 (7.40) 4.38 (5.50) 12.402 .001 .32

Aggression 8.69 (8.53) 4.91 (6.27) 6.700 .011 .24

ConductProblems 1.90 (2.46) 1.36 (2.16) 1.449 .231 .12

Anxiety 2.37 (2.91) 3.38 (4.10) 2.414 .123 .14

Depression 3.15 (3.51) 3.06 (4.41) .013 .911 .01

Somatization 1.51 (2.37) 2.28 (3.40) 2.007 .159 .13

Atypicality 1.47 (2.62) 1.00 (1.97) 1.088 .299 .10

Withdrawal 3.46 (3.29) 3.53 (3.51) .014 .906 .01

AttentionProblems 7.26 (4.84) 4.23 (4.61) 11.331 .001 .31

LearningProblems 5.69 (5.15) 5.51 (5.07) .035 .853 .02

ADHDsymptoms¹ 16.12 (11.16) 8.64 (8.93) 14.628 .000 .35

¹ ADHDsymptoms = Hyperactivity and AttentionProblems scales combined

Prediction of Hyperactivity and Attention Problems in boys and girls

We conducted a series of multiple regressions with Hyperactivity and AttentionProblems completed by the parents and teachers as criterion measures and Aggression,Conduct Problems,Anxiety,Depression,Somatization,andLearningProblems(only included in the TRS)as predictors. The scale AttentionProblems was also used as predictor when the Hyperactivity scale was the criterion measure and the scale Hyperactivity was added as predictor when the AttentionProblems scale was the criterion measure. Regressions were conducted with respect to separate outcomes of (1) AttentionProblems in boys and girls, obtained from the PRS, (2) AttentionProblems in boys and girls, obtained from the TRS (see Table 3), (3) Hyperactivity in boys and girls, obtained from the PRS, and (4) Hyperactivity in boys and girls obtained from the TRS (see Table 4).


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TABLE 3

Standard regression analyses for variables predicting AttentionProblems in boys and girls

VariableUnstandardisedCoefficient (B)

t-value p-value F-value p-value

Attention Problems in boys, obtained from the PRS 25.31 .000

Aggression .24 1.92 .059

Anxiety .34 3.66 .001

Hyperactivity .28 2.56 .013

Attention Problems in girls, obtained from the PRS 14.94 .000

Somatization .42 2.48 .017

Anxiety .23 2.46 .018

Attention Problems in boys, obtained from the TRS 43.97 .000

LearningProblems .40 5.00 .000

Depression .49 4.16 .000


Attention Problems in girls, obtained from the TRS 29.55 .000



Depression .27 2.42 .020

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TABLE 4

Standard regression analyses for variables predicting Hyperactivity in boys and girls



Hyperactivity in boys, obtained from the PRS 26.16 .000


Somatization .26 2.37 .021

ConductProblems .45 2.13 .037

Hyperactivity in girls, obtained from the PRS 35.55 .000



Hyperactivity in boys, obtained from the TRS 62.61 .000



AttentionProblems .31 2.47 .016

Hyperactivity in girls, obtained from the TRS 56.46 .000



Anxiety -.26 -.2.18 .035

Prediction of inattentive symptoms in boys and girls

Attention Problems in boys, obtained from the Parent Rating Scales (PRS). The combination of the predictors Aggression,Anxiety, and Hyperactivity was significantly related to AttentionProblems(see Table 3). The sample multiple correlation coefficient was .74, indicating that approximately 54% of the variance of the score on the AttentionProblems subscale could be accounted for by the combination of Aggression,Anxiety, and Hyperactivity.

The unstandardized coefficients indicate that Anxiety is the strongest predictor for AttentionProblems in boys as rated by parents.

Attention Problems in girls, obtained from the Parent Rating Scales (PRS). The combination of the predictors Somatization and Anxiety was significantly related to Attention Problems (see Table 3). The sample multiple correlation coefficient was .64, indicating that approximately 40% of the variance of the score on the AttentionProblems subscale could be accounted for by the combination of Somatization and Anxiety.

The unstandardized coefficients indicate that Somatizationand Anxietyare the strongest predictors of AttentionProblemsin girls as rated by parents.


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Attention Problems in boys, obtained from the Teacher Rating Scales. The combination of the predictors Learning Problems, Depression, and Hyperactivity was significantly related to AttentionProblems (see Table 3). The sample multiple correlation coefficient was .82, indicating that approximately 67% of the variance of the score on the Attention Problems scale could be accounted for by the combination of LearningProblems,Depression, and Hyperactivity.

According to the unstandardized coefficients LearningProblems and Depression were the strongest predictors for AttentionProblems.

Attention Problems in girls, obtained from the Teacher Rating Scales (TRS). The combination of the predictors Learning Problems, Hyperactivity and Depression was significantly related to AttentionProblems (see Table 3). The sample multiple correlation coefficient was .81, indicating that approximately 67% of the variance of the score on AttentionProblemscould be accounted for by the combination of LearningProblems,Hyperactivityand Depression.

The unstandardized coefficients indicated that the scale LearningProblems was the strongest predictor of AttentionProblems in girls as rated by teachers.

When LearningProblems was taken out as a predictor for AttentionProblems the scale Depression was the best predictor for AttentionProblems in both boys and girls as rated by teachers.

Prediction of hyperactive/impulsive symptoms in boys and girls

Hyperactivity in boys, obtained from the Parent Rating Scales (PRS). The combination of the predictors Aggression, Somatization and Conduct Problems was significantly related toHyperactivity (see Table 4). The sample multiple correlation coefficient was .74, indicating that approximately 55% of the variance of the score on the Hyperactivity subscale can be accounted for by the combination of Aggression, Somatization and ConductProblems.

The unstandardized coefficients show that the Aggression scale is the strongest predictor of Hyperactivity in boys as rated by parents.

Hyperactivity in girls, obtained from the Parent Rating Scales (PRS). The combination of the predictors Conduct Problems and Aggression was significantly related to Hyperactivity (see Table 4). The sample multiple correlation coefficient was .79, indicating that approximately 62% of the variance of the score on the Hyperactivity scale can be accounted for by the combination of ConductProblems and Aggression.

The unstandardized coefficients indicate that the scale Conduct Problems is the strongest predictor for Hyperactivity in girls as rated by parents.

Hyperactivity in boys, obtained from the Teacher Rating Scales (TRS). The combination of the predictors Aggression,ConductProblems, and AttentionProblems was significantly related to Hyperactivity (see Table 4). The sample multiple correlation coefficient was .86, indicating that approximately 75% of the variance of the score on Hyperactivity could be accounted for by the combination of Aggression, Conduct

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Problems, and AttentionProblems.The unstandardized coefficients indicate the scale ConductProblemsas the strongest

predictor of Hyperactivity in boys as rated by teachers.Hyperactivity in girls, obtained from the Teacher Rating Scales (TRS). The combination

of the predictors Aggression,LearningProblemsand Anxiety, was significantly related to Hyperactivity (see Table 4). The sample multiple correlation coefficient was .89, indicating that approximately 80% of the variance of the score on the Hyperactivity scale could be accounted for by the combination of Aggression,LearningProblems,and Anxiety.

The unstandardized coefficients indicate Aggression as the strongest predictor of Hyperactivity in girls as rated by teachers.

Correlations between ratings of parents and teachers on the BASC

The correlation matrices of the parents’ and teachers’ ratings are shown in Table 5. The results indicate that there is a great difference in the significance of the correlations depending on gender rated. Thus there is a significant correlation between the ratings of parents and teachers with respect to boys on all 10 measures, but with respect to girls there is only significant correlation on 3 out of 10 measures. With respect to ADHD symptoms, the correlation between parents’ and teachers’ ratings of boys is significant at the 0.01 level, but with respect to girls the correlation is not significant.

TABLE 5

Correlations between parent and teacher ratings on the BASC, child level form

US normsboys and girls

(n = 745)

Icelandic sampleboys and girls

(n= 115)

Icelandic sampleboys only(n= 68)

Icelandic samplegirls only(n= 47)

Aggression 0.38 0.25** 0.30* 0.08

Conduct Problems 0.49 0.28** 0.32** 0.17

Hyperactivity 0.42 0.30** 0.30* 0.14

Anxiety 0.12 0.33** 0.41** 0.25

Depression 0.37 0.49** 0.54** 0.46**

Somatization 0.19 0.20* 0.26* 0.15

Attention Problems 0.62 0.49** 0.58** 0.31*

Atypicality 0.31 0.31** 0.32** 0.26

Withdrawal 0.24 0.48** 0.52** 0.42**

ADHD symptoms¹ 0.42** 0.47** 0.21

**. Correlation is significant at the 0.01 level (2-tailed) *. Correlation is significant at the 0.05 level (2-tailed) ¹ADHDsymptoms = Hyperactivity and AttentionProblems scales combined


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The ratio of boys versus girls with ADHD symptoms

The ratio of boys versus girls with ADHDsymptoms ratings exceeding 1½ SDs from the group’s mean was calculated. According to parents the ratio is 3 boys versus 1 girl, and according to teachers the ratio is 9 boys versus 1 girl.

DISCUSSION

Differences between genders according to parents

As had been expected, parents rated boys significantly higher than girls on the externalizing scales Hyperactivityand Aggression and somewhat higher (a trend) for the scale ConductProblems. This is in agreement with the findings of Crijnen et al. (1997) who found that parents rated boys higher than girls on externalizing problems in 12 different cultures. These results are also in line with those of Bongers et al. (2003, 2004), who performed a large longitudinal multiple birth-cohort study of children aged 4 – 18 years old, based on parental reports of problem behaviours. They found that, overall, males showed higher levels of externalizing behaviour than did females. Our findings are in contrast to those of Esparo et al. (2004) who found in a non-clinical group of 6-year-old Spanish children, no differences between sexes in the prevalence of total psychological problems, while girls tended to have more externalizing problems than boys.

Contrary to our expectation, there was not a significant difference between boys and girls on the AttentionProblemsscale according to parents. This is not in agreement with those studies that have generally found higher levels of inattention in boys on parent rating scales (Bohlin & Janols, 2004; Gomez, 1999; Magnusson, 1999). Our findings also contrast with those of Brewis & Schmidt (2003) who did not find significant gender differences in identification of children’s ADHD symptoms in parents’ ratings of 206 middle-class Mexican children, aged 6-12 years. Possibly these differences can be explained by cultural differences in expected and socially acceptable behaviour of boys and girls.

Differences between genders according to teachers

Teachers rated boys higher than girls on the subscales Hyperactivity, Aggressionand also on AttentionProblems in contrast to parents. Our findings partly agree with those of Brewis & Schmidt (2003) who found that teachers ascribe more inattention problems to boys than girls. The reason why teachers find boys to have more inattention symptoms than girls while parents do not might be that relatively higher teacher scores of boys on hyperactivity and aggression are inflating their ratings of attention problems. Our findings are in line with most previous findings in other cultures (e.g. Abikoff et al. 2002; Bohlin & Janols, 2004; Jackson & King, 2004) but in contrast to the findings of Esparo et al. (2004). These results emphasize that there may be cultural variations in how hyperactive/

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impulsive and inattentive symptoms are rated by parents and teachers with respect to gender.

Prediction of inattentive symptoms in boys and girls

According to parents’ ratings the scale Anxietybest predicted AttentionProblems in boys and the scales Somatization and Anxietybest predicted AttentionProblems in girls. These findings were expected and are in accordance with most of the previous literature that has found high associations between inattention and internalizing problems in boys and girls.

According to the teachers, the best predictor of inattentive symptoms was the LearningProblems scale for both boys and girls. These findings are in line with numerous other studies that have found high associations between inattentive symptoms and learning problems (e.g. Chhabildas, Pennington, & Willcutt, 2001; Gomez et al., 2003; Levy et al., 2005; Willcutt, & Pennington, 2000; Wolraich et al., 2003). Interestingly, Gomez et al., (2003) found a moderate to strong correlation (.60) between inattention and academic problems trait factors, while the correlation between hyperactivity/impulsivity and academic problems trait factors was almost zero (.02). Most learning problems like reading disorders, spelling disorders and mathematical disorders are language based and are related to deficits in verbal working memory (e.g. Rucklidge & Tannock, 2002; Wilson & Swanson, 2001). Specific language impairment which is also highly comorbid with ADHD is also associated with deficient verbal working memory (Jonsdottir, 2005; Montgomery, 2003). The question remains to what extent inattention problems in children are in fact caused by deficits in verbal working memory (e.g. Martinussen et al., 2005).

When LearningProblems was taken out as a predictor for AttentionProblems the scale Depression was the best predictor for AttentionProblems in both boys and girls as rated by teachers. Our findings agree with those of Willcutt et al. (1999) who found that symptoms of inattention were associated with lower full scale intelligence and higher levels of depression, whereas symptoms of hyperactivity/impulsivity were more associated with oppositional defiant disorder and conduct disorder. The causal relationship between learning problems, inattention and depression needs further examination.

According to teachers there is no gender difference in ratings of LearningProblems and Depression (see Table 2) which are the two best predictors of inattention in both boys and girls. Therefore it is suggested that higher ratings of boys on the Hyperactivitysubscale, which is the third best predictor of inattention in the regression analysis, may be elevating their scores on the AttentionProblems subscale as rated by teachers (see Table 2).

Prediction of hyperactive/impulsive symptoms in boys and girls

According to parents, externalizing problems (Aggression and ConductProblems) best predicted Hyperactivity in both boys and girls. These findings are consistent with those of Levy et al. (2005) who examined gender differences in ADHD symptom comorbidity


31

in a large sample of twins and siblings in Australia. They found no significant gender differences in comorbidity for externalizing disorders. In a similar vain, Gabel et al. (1996) did not find any sex differences in comorbid externalizing problems on parental behaviour ratings of hyperactive boys and girls aged 6-11 years.

According to teachers Conduct Problems associated with Aggression and AttentionProblems best predicted hyperactivity symptoms in boys while Aggression associated withLearningProblems and Anxiety best predicted hyperactivity symptoms in girls. Thus it seems that externalizing problems are predicting hyperactivity symptoms in boys to a greater extent than in girls and that internalizing problems and learning disorders are predicting hyperactivity symptoms to a greater extent in girls than in boys. Our results also show that more observable behaviour is predicting hyperactivity to a greater extent in boys than in girls.

Correlations between ratings of parents and teachers on the BASC

Correlational analysis showed that agreement between parent and teacher ratings in the sample as a whole were generally in the low to moderate range (see Table 5). When the sample was divided according to gender, interesting and unexpected differences became apparent. While the correlations between parent and teacher ratings of boys were significant on all 10 measures they were only significant on 3 measures of girls (AttentionProblems, Depression and Withdrawal). On the scale with ADHD symptoms combined, the correlation was .47 (significant at the .01 level) with respect to boys, but only .21 (nonsignificant) with respect to girls (see Table 5). These results are difficult to explain but may reflect the finding of Quinn & Wigal (2004) who found that 4 out of 10 teachers reported more difficulty in recognizing ADHD symptoms in girls than in boys. They also found that the majority of parents and teachers think that girls with ADHD are more likely to remain undiagnosed. Possible explanation for the better agreement between parents and teachers with respect to boys might be that because they have more externalizing problems than girls their behaviour is more easily observable.

The ratio of boys versus girls with ADHD symptoms

According to parents, the ratio between boys and girls with the highest ratings of AttentionProblems and Hyperactivitycombined was 3 boys to 1 girl. This is similar to findings generally reported in the literature of ratios between girls and boys with ADHD in community samples. According to teachers the comparable ratio was 9 boys to 1 girl which is similar to the ratio between boys and girls with ADHD in clinic-referred samples. This large difference of boys and girls with severe ADHD symptoms in a normal sample as assessed by teachers is unexpected, although most of the literature suggests that teachers tend to report higher rates of ADHD in children than parents do (e.g. Sherman et al.,

Chapter two

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1997). It has been proposed that this may be because teachers ascribe ADHD symptoms in children who have a variety of other behavioural problems. It has also been suggested that parents underreport ADHD in children because they do not have the benefit of a large reference group like teachers do (Gaub and Carlson 1997b).

Abikoff et al. (1993) found in their study that oppositional tendencies in a male model tended to inflate teachers’ ratings of ADHD. Jackson and King (2004) did a similar study using both male and female models and found that oppositional behaviour was associated with higher teacher ratings of hyperactivity and inattentiveness. They also found gender differences in the effects of oppositional behaviour on teacher ratings of ADHD symptoms suggesting that teacher rating tendencies could contribute to higher diagnostic rates of ADHD among boys and conduct disorders among girls. Interestingly, in our study teachers did not find a significant difference in ConductProblems between boys and girls although they found very significant differences in Hyperactivity. In contrast, parents found less differences between sexes in Hyperactivity ratings than teachers and more differences between genders in ConductProblems. Our findings suggest that teachers may, to a greater extent than parents, rate conduct disorders as Hyperactivity in boys and as ConductProblems in girls, agreeing with the findings of Jackson and King (2004).

SUMMARY AND CONCLUSION

The main findings of the study are that in a normal Icelandic school-based sample, boys score higher than girls on ratings of hyperactivity/impulsivity and aggression according to both parents and teachers and also on ratings of inattention according to teachers. The results of the present study also show that inattentive symptoms in boys and girls are mainly related to learning problems and internalizing variables like anxiety and depression, while hyperactive/impulsive symptoms are mainly associated with externalizing problems like aggression and conduct problems, supporting the two symptom clusters model of ADHD. With respect to internalizing problems, inattention problems associated more with anxiety according to parents and with depression according to teachers.

The differences in levels of inattention, hyperactivity and aggression between boys and girls found in this study are similar to those that have been found between boys and girls with ADHD in nonreferred populations (Gaub & Carlson, 1997b), supporting the view that sex differences that have been observed in studies of ADHD might be a reflection of normal sex variation and not a specific attribute of ADHD.

The fact that boys are rated more aggressive than girls both according to parents and teachers might be explained by the effect of sex hormones on behaviour. A study has shown that there is a positive relationship between levels of testosterone and serious aggression in preschool boys (Sánchez-Martín et al., 2000). Another study found significantly higher levels of androgen in male but not in female adolescents with elevated scores of externalizing behaviour. The study also showed that boys with persistent externalizing behaviour had the highest levels of androgens (Maras et al., 2003).


33

It is suggested that more aggressive behaviour in boys than girls may be inflating their ADHD ratings especially among teachers. It seems that more aggressive behaviour is a normal attribute of being a boy (e.g. Hudziak et al., 2003) and the question remains if there might be other ways to tackle boys’ aggressive behaviour problems than with medication. Parent management training has been shown to be an effective means of treating aggression in children (e.g. Kazdin, 2000) and social cognitive intervention programs have shown promising results (Van Manen et al., 2004). In view of the difference between the genders in temperament and personality traits, such as aggression, it might be possible that different teaching methods are needed for boys and girls. Teaching the genders in separate classes might be interesting to try.

The poor concordance between parents and teachers in their ratings of ADHD symptoms in girls in this study is an unexpected and new finding that may be of clinical importance. According to DSM-IV diagnostic criteria for ADHD, symptoms have to be present in multiple settings e.g. both at home and at school. Poor interrater agreement has been found to decrease diagnostic rates for ADHD in a clinical sample (Wolraich et al., 2004). The poor concordance between parents’ and teachers’ ratings of ADHD symptoms with respect to girls may result in their underdiagnosis and can potentially partly explain the much higher diagnostic rates of boys with ADHD.

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Chapter two

3�

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3�

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�0

�1

CHAPTER THREE 3The impact of specific language impairment on working memory in children with ADHD combined subtype

Solveig Jonsdottir, Anke Bouma, Joseph A. Sergeant, Erik J.A. Scherder

Archives of Clinical Neuropsychology, Volume 20, Issue 4, 1 June 2005, Pages 443-456

Chapter three

�2

ABSTRACT

The objective of this study was to examine the impact of comorbid specific language impairment (SLI) on verbal and spatial working memory in children with DSM-IV combined subtype Attention Deficit Hyperactivity Disorder (ADHD-C). Participants were a clinical sample of 8½ -to12½ - year- old children diagnosed with ADHD-C. A group of ADHD-C with SLI was compared to a group of ADHD-C without SLI, and a group of normal children, matched on age and nonverbal intelligence. The results show that ADHD-C children with SLI scored significantly lower than those without SLI and normal children, on verbal working memory measures only. Both ADHD groups performed normally on spatial working memory measures. It is concluded that working memory deficits are not a specific characteristic of ADHD but are associated with language impairments. The importance of screening for language disorders in studies of neuropsychological functioning in children with ADHD is emphasized.

The impact of specific language impairment on working memory

�3

INTRODUCTION

Attention deficit hyperactivity disorder (ADHD) is the most common neuropsychiatric disorder of childhood, affecting approximately 1-7% of school-aged children, depending on the stringency of criteria used (American Psychiatric Association, 1994; Swanson, Sergeant, Taylor, Sonuga-Barke, Jensen & Cantwell, 1998). The main characteristics of the disorder are inattention, hyperactivity and impulsivity. DSM-IVdifferentiates three subtypes of the disorder according to levels of presenting symptoms: the combined subtype (ADHD-C), the predominantly inattentive subtype (ADHD-I), and the predominantly hyperactive-impulsive subtype (ADHD-HI). Denckla (2003) has proposed that many of the externally observable diagnostic characteristics of ADHD, particularly of the ADHD-I subtype, can really be caused by language processing difficulties.

Language impairment (LI) is a highly prevalent comorbidity in children with psychiatric disorders and behavioural problems (Beitchman et al., 1986a, 1986b, 1996a, 1996b, 2001; Cantwell & Baker, 1987; Cohen, et al., 1993, 1998; Young et al., 2002). The most common psychiatric diagnosis among children with LI is ADHD (Cohen et al., 1998), and conversely, LI is a frequent comorbidity found in children with ADHD (Cantwell, 1996; Kovac et al., 2001; Purvis & Tannock, 1997). One study found that approximately two thirds of a consecutively referred ADHD sample reached criteria for LI (Cohen et al., 1998). Despite the frequent co-occurrence of these two common disorders, there have been relatively few studies that specifically investigate language abilities of children with ADHD (Cohen, 2000; McInnes et al., 2003), and it is seldom screened for in studies on neuropsychological deficits in children with ADHD (Sergeant et al., 2002).

The term specific language impairment (SLI) has been used by many researchers to refer to children with normal nonverbal intelligence and a deficit in expressive and/or receptive language that does not appear to be a secondary manifestation of an associated medical disorder (Bartlett et al., 2002; Bishop et al., 1992; Williams et al., 2000). SLI is believed to affect approximately 7% of children (Leonard, 1998; Tomblin et al., 1997). Neuropsychological studies of SLI have revealed deficits in verbal working memory (Hulme and Roodenrys, 1995; Kamhi et al., 1988) which is believed by many researchers to be at the root of the language difficulties (e.g. Baddeley & Wilson, 1993; Gathercole & Baddeley, 1989; Swank, 1999). According to Montgomery (2003), some researchers have proposed, that deficient verbal working memory might serve as “a reliable, culture-free marker of SLI”.

Decreased working memory, both verbal and spatial, are among the cognitive deficits purported to be characteristic of ADHD (Barkley 1997; 2003; Karatekin & Asarnow, 1998; Tannock, 1998). Working memory is one of four executive functions considered to be impaired in ADHD as a result of a lack in behavioural inhibition (Oosterlaan, Logan & Sergeant, 1998), which in turn has been proposed by Barkley (1997) to be the fundamental impairment in children with ADHD. Studies on working memory in ADHD have shown conflicting results (e.g. Bedard et al., 2004; Cohen et al., 2000; Geurts et al., 2004;

Chapter three

��

Karatekin & Asarnow, 1998; McInnes et al., 2003; Muir-Broaddus et al., 2002; Scheres et al., 2004; Siklos & Kerns, 2004; Van Goozen et al., 2004). Verbal working memory has been studied more extensively in ADHD children than spatial working memory, but language impaired children have not been screened for in many of these studies and results have been mixed. Findings of studies of spatial working memory in ADHD have also been equivocal. Cohen et. al. (2000) found, that verbal and spatial working memory measures, used to tap the core cognitive deficit of ADHD in executive functions, were more closely associated with language disorders than with ADHD. The authors concluded that caution must be exercised in attributing to children with ADHD what might be a reflection of problems for children with language disorders generally. The results of Cohen’s study do not agree with those of McInnes et. al. (2003) who found that working memory, both verbal and spatial, was impaired in ADHD children irrespective of language impairment.

Baddeley and Hitch (1974) have proposed a three component model of working memory comprised of a control system, thecentralexecutive, which is assisted by two subsidiary systems for maintaining information: a verbal storage system called the phonologicalloop, and a visual storage system called the visuospatial sketchpad. In this model, working memory is considered to be a limited-capacity system, which stores information for brief periods of time, and is believed to underlie human thought processes (Baddeley, 2003). Neuroimaging studies have indicated that spatial working memory is primarily localized in the right hemisphere, while the phonologicalloop has been associated with the left temporoparietal region. The centralexecutive is believed to be mainly located in the frontal lobes (Baddeley, 2003). A recent meta-analytic study of the neural bases of working memory has shown that Brodmann’s areas in the superior frontal cortex, respond most when working memory must be continuously updated and when temporal order must be maintained (Wager & Smith, 2003).

The purpose of the present study was to examine the impact that comorbid SLI has on verbal and spatial working memory in children diagnosed with ADHD-C. Children with ADHD-C, with and without SLI, and a normal control group were compared on measures of verbal and spatial working memory. The first hypothesis was that ADHD-C children with SLI would show deficits in verbal working memory, but not in spatial working memory. The second hypothesis was that ADHD-C children without SLI would not differ from normal children on verbal or spatial working memory measures.

METHODS

Participants

The clinical sample included 127 children aged 6-13 years old who had been consecutively referred for neuropsychological assessment at the Department of Child and Adolescent Psychiatry, Landspitali-University Hospital in Reykjavík, Iceland. The department is a tertiary referral facility serving the whole population of Iceland with


��

approximately 290.000 inhabitants. Out of this group, children who fulfilled the following criteria were selected: (1) age

between 8½ and 12½ years; (2) psychiatric diagnosis of ADHD combined subtype; (3) native Icelandic speaker; (4) no neurological or other medical disorders. A paediatrician or a child/adolescent psychiatrist assessed the children with the aid of a diagnostic interview based on DSM-IV (American Psychiatric Association 1994) criteria, the Icelandic version of the Achenbach parent/teacher rating scales (Hannesdottir, 2002) and the Icelandic version of the ADHD Rating Scale (Magnusson et al, 1999). The ADHD-I subtype was excluded and no child had the diagnosis of ADHD-HI subtype. The number of children who fulfilled the aforementioned criteria were 47 in total, 76.6% were male and 23.4% female.

Criteriaforspecificlanguageimpairment(SLI). Selection for SLI versus non-SLI ADHD groups, was made on the basis of performance

on the Nonverbal Scale of the Kaufman Assessment Battery for Children (K-ABC) (Kaufman & Kaufman 1983) (see later) and the Icelandic version of the Test of Language Development-2 Intermediate (TOLD-2I; Hamill & Newcomer, 1988; Símonardóttir & Guðmundsson, 1996). The TOLD-2I is comprised of six subtests which are combined to make composite scores of spoken language quotient (SLQ), receptive language, expressive language, semantics and syntax.

Although some researchers use the cutoff score of 85 on language measures when assessing LI children, we have chosen for somewhat stricter criteria, so that only children who received SLQ standard score of less than or equal to 80 on the TOLD-2I, were considered having LI. The score of 80 is approximately 1½ SD below the standardized mean of 100 and falls at the ninth percentile rank. There were 20 children (43% of the sample), that fulfilled this stricter criterion. Children who received SLQ standard score of 90 (the 25th percentile) or above, were considered without LI and 15 children (31.9% of the sample), fulfilled that criterion.

In order to fulfill criteria for SLI, children are required to have nonverbal intelligence within the normal range (e.g., > 85 standard score), in addition to impaired language ability. In the present study only children with nonverbal intelligence > 85 on the K-ABC were included; one child was dropped from the LI group of 20 children because of this requirement. The above procedure provided two comparable groups: 19 (14 boys, 5 girls) ADHD children with SLI (ADHD+SLI) and 15 (11 boys, 4 girls) ADHD children without SLI (ADHD non-SLI). Also a control group of 15 (9 boys, 6 girls) normal children (NC) was included. The NC were screened for ADHD with the help of parent/teacher rating scales and a clinical interview.

The three groups of children did not show a significant difference with respect to age (F(2,46) = 0.486, ns), gender (X2= 0.890, df = 2, ns), or nonverbal IQ (F(2,46) = 1.83, ns) (for means and standard deviations, see Table 1).

Chapter three

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TABLE 1

Neuropsychological measures

Neuropsychological differences between groups were assessed with the K-ABC (Kaufman & Kaufman, 1983; Kaufman et al., 1987). The K-ABC is an individually administered measure of intelligence and achievement intended for children aged 2½ through 12½ years. It is based on research and theory in cognition and neuropsychology and is designed to measure ability (intelligence) on the basis of the processing style required to solve tasks. Problem solving abilities are measured on two mental processing scales: Sequentialand Simultaneous. The SequentialProcessingScale is composed of the subtests HandMovements,NumberRecall, and WordOrder. The SimultaneousProcessingScale is composed of the subtests GestaltClosure, Triangles, MatrixAnalogies, SpatialMemory and PhotoSeries. Sequential processing ability is believed to rely more on the functioning of the left cerebral hemisphere and simultaneous processing more on the right cerebral hemisphere.

The K-ABC also includes a NonverbalScale, which according to the authors, serves as a good estimate of intellectual potential of children who have problems in the areas of receptive or expressive language, who have language disorders, or use English as a second language. The NonverbalScale is composed of the subtests: HandMovements, Triangles, MatrixAnalogies, SpatialMemory and PhotoSeries.

S. Jonsdottir et al. / Archives of Clinical Neuropsychology 20 (2005) 443–456 ��

Table 1Age, nonverbal intelligence, and performance of groups on the TOLD-2I

Whole ADHDgroup (n = ��)

ADHD + SLI(n = 1�)

ADHD non-SLI(n = 1�)

Normal controls(n = 1�)

Mean S.D. Mean S.D. Mean S.D. Mean S.D.

Age (years) 10.�� 1.2� 10.�� 1.1� 10.�� 1.2� 10.33 1.2�Nonverbal IQa 103.�2 12.�2 10�.�3 12.�� 10�.0� 10.�� 113.2� 11.��

TOLD-2I CompositesSLQb �3.�� 1�.3� ��.2� �.�� 101.20 10.�1 10�.�0 12.�0Receptive language 86.�� 1�.�0 �1.1� 10.�� 10�.�0 �.�2 10�.00 12.3�Expressive language 82.�� 1�.33 �1.32 10.0� ��.�� 12.�� 102.33 11.��Semantics ��.�� 1�.0� �2.�� 10.�3 ��.�3 10.0� 10�.13 10.��Syntax �3.�1 1�.�1 ��.�3 11.�0 103.33 12.�� 103.�� 13.��

SubtestsSentence combining 6.�� 2.�� .00 1.�� .�3 1.�� .20 2.11Vocabulary 8.2� 2.�� .3� 2.�� 11.00 1.�1 11.�0 2.�1Word ordering 8.23 2.�� .21 1.�3 10.�� 2.03 10.�0 2.��Generals 8.�0 2.00 �.21 1.�1 �.2� 2.2� 11.0� 1.�1Grammatic Compr.c �.�� 3.01 �.�� 2.�� 11.�0 1.�� 11.�� 2.�2Malapropism 8.1� 2.�0 �.21 2.�2 10.20 1.�� 11.33 1.��

a Nonverbal IQ = nonverbal intelligence.b SLQ = spoken language quotient.c Grammatic Compr.: grammatic comprehension.

to solve tasks. Problem solving abilities are measured on two mental processing scales: Se-quential and Simultaneous. The Sequential Processing Scale is composed of the subtestsHand Movements, Number Recall, and Word Order. The Simultaneous Processing Scaleis composed of the subtests Gestalt Closure, Triangles, Matrix Analogies, Spatial Memoryand Photo Series. Sequential processing ability is believed to rely more on the function-ing of the left cerebral hemisphere and simultaneous processing more on the right cerebralhemisphere.

The K-ABC also includes a Nonverbal Scale, which according to the authors, serves as agood estimate of intellectual potential of children who have problems in the areas of receptiveor expressive language, who have language disorders, or use English as a second language. TheNonverbal Scale is composed of the subtests Hand Movements, Triangles, Matrix Analogies,Spatial Memory and Photo Series.

1.3. Assessment of verbal and spatial working memory

According to Barkley (1997), verbal and spatial working memory has often been assessedin neuropsychological research with the following tasks: “retention and oral repetition of digitspans (especially in reverse order); mental arithmetic, such as serial addition; locating stimuliwithin spatial arrays of information that must be held in memory; and holding sequences ofinformation in memory to properly execute a task, as in self-ordered pointing tasks”. In thecurrent study, the K-ABC subtests Number Recall and Word Order were considered measures


��

Assessment of verbal and spatial working memory

According to Barkley (1997), verbal and spatial working memory has often been assessed in neuropsychological research with the following tasks: “retention and oral repetition of digit spans (especially in reverse order); mental arithmetic, such as serial addition; locating stimuli within spatial arrays of information that must be held in memory; and holding sequences of information in memory to properly execute a task, as in self-ordered pointing tasks”. In the current study, the K-ABC subtests NumberRecall and WordOrder were considered measures of verbal working memory and the subtests HandMovements and SpatialMemory were considered measures of spatial working memory.


Within the whole group of ADHD-C children (n = 47), paired t-tests were used to analyse the difference between the two mental processing scales of the K-ABC (Sequentialand Simultaneous) and between spatial and verbal working memory.

In addition, analyses of variance (ANOVA) were performed with Group (ADHD+SLI, ADHD non-SLI, NC) as an independent variable and with K-ABC measures (Composite scores; Subtest scores, Spatial and Verbal Working Memory) as a dependent variable. In case of a main effect of Group, analyses were performed to determine three contrasts: (1) ADHD+SLI versus ADHD non-SLI, (2) ADHD+SLI versus NC, and (3) ADHD non-SLI versus NC. Effect sizes (eta squared: 2) were calculated, that is, small < .01, medium < .06, and large ≥ .14.

Furthermore, correlational analyses were employed to investigate the relationship between the K-ABC measures (Composite scores; Subtest scores, Spatial and Verbal Working Memory) and spoken language quotient (SLQ) on the TOLD-21 and to examine the relationship between working memory measures.

The SPSS-PC program was used to analyse the data.

RESULTS

K-ABC composites and subtests

Table 2 shows the results (means, standard deviations, ANOVAs, and contrasts) of the different ADHD groups and the control group. Within the entire ADHD group, paired t-tests showed that ADHD children performed significantly better on theSimultaneousProcessingScalethan on the SequentialProcessingScale (t(46) = 6.73, P=.000). The difference in performance was highly significant in the ADHD+SLI group (t(18) = 6.72, P= .000), but also, although smaller, significant in the ADHD non-SLI group (t(14) = 2.29, P=.04), and the control group (t(14) = 4.47, P = .001).

Chapter three

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S. Jonsdottir et al. / Archives of Clinical Neuropsychology 20 (2005) 443–456 ��

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Subsequently, main effects of Group were calculated for K-ABC composites, and K-ABC subtests, by means of ANOVA. A significant main effect of Group was observed for MPC, SequentialProcessing Scale, NumberRecall, and WordOrder (for means, standard deviations and ANOVAs, see Table 2). With respect to MPC, ADHD+SLI group scored significantly lower only in comparison with the control group (F(1,32)= 7.75, P = .009). On the Sequential Processing Scale, the ADHD+SLI group performed significantly worse than the other two groups (control group and ADHD non-SLI) (F(1,32) = 13.86, P = .001, and (F(1,32) = 8.33, P = .007), respectively. The ADHD+SLI group performed also significantly worse than these two groups (control group and ADHD non-SLI) on the subtests NumberRecall (F(1,32) = 11.76, P= .002) and (F(1,32) = 7.82, P = .009), respectively, and WordOrder of the SequentialProcessingScale (F(1,32) = 11.87, P= .002), and (F(1,32) = 9.92, P = .004), respectively.

Working memory

The entire ADHD group performed significantly worse on verbal working memory (Verbal WM) than on spatial working memory (Spatial WM) (t(46) = 2.74, P= .009) (see Table 2). Interestingly, this effect appeared to be only significant in the ADHD+SLI group (t(18) = 3.29, P=.004), but not in the ADHD non-SLI group (t(14) = .06, ns). There was no significant difference between Verbal WM and Spatial WM in the control group (t(16) = 1.44, P= .168).

Data analysis further indicated a main effect of Group only with respect to Verbal WM (see Table 2). ANOVAs of the contrasts showed that the ADHD+SLI group performed significantly worse than the ADHD non-SLI group (F(1,32) = 12.28, P = .001) and the control group (F(1,32) = 16.64, P = .000).

Relationship between K-ABC measures and spoken language quotient (SLQ)

Pearson’s correlations were calculated within the whole group of 47 ADHD children in order to investigate the relationship between the K-ABC measures (composite scores, subtest scores, Spatial WM and Verbal WM) and SLQ on the TOLD-2I. The results showed that the SLQ is significantly correlated with the SequentialProcessingScale (r=.48, n = 47, P= .001), but not with the SimultaneousProcessingScale(r=.09, n = 47, ns). Moreover, SLQ was significantly related to Verbal WM (r= .51, n = 47, P = .000). No significant relation between SLQ and Spatial WM was observed (r= .15, n = 47, ns).In addition, SLQ appeared to be significantly related to WordOrder (r=.37, n = 47, P = .01) and NumberRecall (r=.52, n = 47, P = .000), but not with HandMovements (r=.21, n = 47, ns).

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Relationship between working memory measures

Pearson’s correlations were calculated for the entire group of 47 ADHD children in order to investigate the relationship between the four working memory measures. The two verbal working memory measures NumberRecall and WordOrder were significantly correlated (r = .55, n = 47, P = .000). The two spatial working memory measures SpatialMemoryand HandMovements were also significantly correlated (r= .39, n = 47, P = .007). HandMovementscorrelated significantly with both NumberRecall (r = .309, n = 47, p = .03) and WordOrder (r = .41, n = 47, p = .004). No other correlations were found to be significant.

DISCUSSION

K-ABC composites and subtests

When examining the outcome of the ADHD-C group as a whole on the K-ABC, several things stand out (see Table 2). The group deviates from the standardized mean on the Sequential Processing Scale, consisting of the three sequential subtests, HandMovements, NumberRecalland WordOrder. All these tasks may be considered to rely on working memory ability (e.g. Alloway et al., 2004; Baddeley, 2003; Frencham et al., 2003; Helland & Asbjornsen, 2004; Montgomery, 2004). At first glance, this might indicate that children with ADHD-C in general are deficient in working memory, both verbal and spatial. When the ADHD-C group on the other hand has been divided according to language ability, interesting differences become apparent. The ADHD+SLI children score significantly lower than ADHD non-SLI children and normal controls on the K-ABC Sequential Processing Scale and on the sequential subtests, Number Recall and WordOrder, which both rely on verbal working memory. The performance of the ADHD+SLI children did not differ significantly from the ADHD non-SLI group and the control group on the subtest HandMovements, which relies on nonverbal sequential processing. The three groups did not differ significantly from one another on the SimultaneousProcessing Scale or any of its subtests. According to Kaufman and Kaufman (1983), the SimultaneousProcessingScale may be considered to depend on the functioning of the right cerebral hemisphere. These findings do not agree with those of researchers who have found right brain deficiency in ADHD children (e.g. Aman et al., 1998).

The results of our study are comparable with studies on SLI in children. Preis et al. (1997) used the K-ABC to describe the typical pattern of processing in 25 children with normal nonverbal intelligence and developmental language disorder (DLD) of the phonologic-syntactic subtype, a mixed receptive-expressive DLD with grammatical and phonologic deficits. The results of the K-ABC showed a significant deficit in sequential processing, whereas simultaneous processing was in the normal range. The children scored significantly below the norms on only two subtests, Number Recall and Word


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Order similarly to our ADHD+SLI sample.The poor performance of the ADHD+SLI group on the NumberRecall test in this study,

is in agreement with studies on SLI children using the DigitSpan test of the Wechsler Scales (Wechsler, 1991). As reported by Williams et al. (2000) most studies on the Wechsler Scales have also shown significant effects of ADHD on the DigitSpan test and several studies have shown this subtest to be the most sensitive to attentional deficit. The DigitSpanForwards test of the Wechsler Scales has in the neuropsychological literature customarily been assumed to measure attention (Lezak, 1995; Spreen & Strauss, 1998). Our results indicate that repeating digits forward might be related to language ability rather than to attentional capacity, at least in ADHD children.

These findings suggest that ADHD children with language disorders are characterized by verbal sequential deficits, rather than by nonverbal sequential deficits.

Working memory

The findings of the present study show that the ADHD+SLI group performed significantly worse than the ADHD non-SLI group and the control group on Verbal WM (NumberRecall + WordOrder), but there were no significant differences between the three groups on Spatial WM (HandMovements + SpatialMemory) which is within the normal range in all three groups (see Table 2). This is in agreement with previous studies that have not found spatial working memory deficits in ADHD (e.g., Scheres et al., 2004). Our findings agree with those of Cohen et al. (2000) who found that working memory deficits in children with ADHD were primarily related to their language abilities. Our results do not agree with their findings that ADHD children with LI perform poorer than ADHD children without LI on spatial measures as well as verbal. The results of the present study are also not in line with those of McInnes et al. (2003) who found that working memory – both verbal and spatial – was impaired in ADHD children, irrespective of language impairment. The reason for the difference in findings might be due to differences in groups examined, differences in diagnostic criteria or differences in diagnostic measures used. In this study, for example, the normal controls were matched with the ADHD groups on nonverbal intelligence, which was not the case in the McInnes study. We also examined only the ADHD-C subtype, while other subtypes were also included in the previously mentioned studies. In addition, our sample was a clinical ADHD sample with serious educational and/or behavioural problems and might not have the same characteristics as a community sample of ADHD children.

The finding that ADHD non-SLI do not have deficits in working memory, does not support Barkley’s (1997) theoretical model of ADHD, which predicts that the executive function of working memory is a general deficit in ADHD.

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Relationship between K-ABC measures and spoken language quotient (SLQ)

The present results indicate that SLQ is significantly correlated with the SequentialProcessingScale but not with the SimultaneousProcessingScale.More specifically, SLQ appeared to be significantly related to the sequential subtests WordOrder and NumberRecall but not with HandMovements.

In addition, SLQ was also found to be significantly related to Verbal WM but not to Spatial WM. This finding is in agreement with numerous previous neuropsychological studies on SLI, that have shown a deficit in verbal working memory (e.g., Gillam et al., 1998; Montgomery, 2004). Taken together, our findings show that ADHD children with comorbid language disorders are characterized by verbal working memory deficits similarly to children with SLI (see review by Montgomery, 2003).

Relationship between working memory measures

The correlational analysis showed that the two verbal working memory measures, Number Recall and Word Order are significantly correlated and that the two spatial working memory measures SpatialMemoryand HandMovements are also significantly correlated. In addition, the HandMovements test is significantly related to both verbal subtests, indicating that it is not a “pure” measure of spatial working memory. The HandMovements test is an adaptation of Luria´s fist-edge-palm test of motor function, which has been widely used as a neuropsychological assessment tool. In addition to the K-ABC, a similar test has also been included in another neuropsychological battery for children, the NEPSY (Korkman et al., 1998). According to Frencham et al. (2003), there is some uncertainty as to which cognitive processes are involved in performing the HandMovementstest. Although Kaufman and Kaufman (1983) presented the HandMovementstest as a nonverbal task, they also commented that performance would benefit from using verbal labelling as a mediating strategy. Frencham et al. (2003) studied the HandMovements test within a working memory theoretical framework and did indeed find that performance of the task relied on verbal recoding strategies. The findings of our study showed no significant differences between the ADHD+SLI, ADHD non-SLI and normal control groups on the HandMovementstest emphasizing the nonverbal nature of this task rather than the verbal one.

CONCLUSIONS

In sum, the results of our study show, that children with ADHD-C do not have a general working memory deficit. Only ADHD-C children with comorbid language disorders showed deficits in verbal working memory - but not in spatial working memory. ADHD-C children with normal language development, did not perform differently from normal


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children on verbal and spatial working memory measures. These results emphasize the importance of screening for language disorders when examining neuropsychological deficits in ADHD.

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CHAPTER FOUR 4Relationships between neuropsychological measures of executive function and behavioural measures of ADHD symptoms and comorbid behaviour


Archives of Clinical Neuropsychology, in press, available online 28 July 2006

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ABSTRACT

Objective: The aim of this study was to examine the relationships between executive functions (EFs), as measured by neuropsychological tests, and symptoms of attention deficit hyperactivity disorder (ADHD) and comorbid behaviour, as rated by parents and teachers. As intelligence and language ability are important covariates they were also assessed.

Method: The sample consisted of 43 children aged 7-11 years who were referred for neuropsychological assessment at a tertiary clinical facility. Most of the children had the diagnosis of ADHD combined or inattentive type. Different aspects of EFs were assessed.

Results: EFs were not significantly related to symptoms of ADHD, but only to comorbid symptoms of depression and autistic symptomatology. Language ability rather than EFs best predicted teacher ratings of inattention.

Conclusions: The results of the study do not support the EF theory of ADHD. The importance of screening for comorbid language disorders in children referred for ADHD is emphasized.

Executive functions and ADHD symptoms

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INTRODUCTION

Attention deficit hyperactivity disorder (ADHD) is the most prevalent neurobehavioural condition of childhood, affecting a substantial proportion of the population around the world (Faraone et al., 2003). The disorder is characterized by age inappropriate symptoms of inattention, motor restlessness and impulsive behaviour (DSM-IV-TR; American Psychiatric Association, 2000). The DSM-IV delineates three subtypes of the disorder: The predominantly inattentive (ADHD-IA), the predominantly hyperactive-impulsive (ADHD-HI), and the combined (ADHD-C). Children with ADHD place a heavy financial burden on educational, social and clinical services and some are impaired for lifetime. In view of the prevalence and financial cost of ADHD and its possible overdiagnosis, it is imperative that measures be used in the diagnostic process that are refined and specific (Sergeant et al., 2002).

While the etiology of ADHD remains unknown at this time, most recent neuropsychological theories have targeted deficient executive function (EF) as being the main characteristic of the disorder (Barkley, 1997, 2003; Pennington & Ozonoff, 1996; Willcutt et al. 2005). Executive functions (EFs) have been defined as “neurocognitive processes that maintain an appropriate problem solving set to attain a future goal” (Welsh and Pennington, 1988). A recent meta-analysis (Willcutt et al., 2005) showed that, while EF deficits are prevalent in ADHD populations, they are “neither necessary nor sufficient to cause all cases of ADHD”. A recent review of studies in the area of EF deficits in children with neurodevelopmental disorders has shown that they are not specific to ADHD (Sergeant et al., 2002). The strongest and most consistent EF deficits in ADHD have been found to be on measures of response inhibition, vigilance, working memory (WM), and planning (Willcutt et al., 2005). It has been suggested that EFs rely on structures in the frontal cortex (e.g. Max et al., 2005), and structural brain imaging studies have shown that children with ADHD tend to have smaller volumes in various areas of the brain including the dorsolateral prefrontal cortex (Seidman et al., 2005). A dysfunctional frontostriatal system has also been implicated in other neurodevelopmental disorders such as autism, depression, obsessive compulsive disorder, schizophrenia, and Tourette’s syndrome (Bradshaw & Sheppard, 2000).

ADHD is highly comorbid with other disorders, mainly externalizing disorders like oppositional defiant disorder (ODD) and conduct disorder (CD), internalizing disorders like anxiety and depression and language related disorders like dyslexia and language impairment (LI). Research has shown that the three subtypes of ADHD have differing types and degrees of comorbidity. Cognitive and language related disorders and internalizing problems have mainly been associated with inattention symptoms rather than hyperactivity/impulsivity symptoms (e.g. Chhabildas et al., 2001; Harrier & DeOrnellas, 2005; Willcutt et al., 1999). There has been relatively little research on the relationship between ADHD and its comorbid disorders with the executive function system (e.g. Oosterlaan et al., 2005; Sarkis et al. 2005), and research has shown that there is often considerable lack of agreement between the various behavioural and cognitive

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measures conventionally used in the diagnostic process of children with ADHD. Naglieri et al. (2005) examined the relationships between the Wechsler Intelligence Scale for Children Third Edition (WISC-III) and the Cognitive Assessment System (CAS), with Conners’ Behavior Rating Scale and Conners’ Continuous Performance Test (CPT) in a sample of children with attention, emotional and behavioural problems. The results showed that there were generally low and non-significant correlations between parent and teacher behavioural ratings and performance on measures purported to be sensitive to ADHD symptoms. The authors concluded “practitioners should expect to find a lack of consistency between the scores provided by the measures examined and should be conservative of their use in clinical settings”. One reason for Naglieri and colleagues’ findings might possibly be that the measures used in their study are not specific enough for ADHD problems. The Conners’ behavioural rating scale used in their study, does not, for example, differentiate between inattention symptoms and hyperactivity/impulsivity symptoms and research has shown that neuropsychological impairment is mainly related to inattention but not to hyperactivity/impulsivity in children with ADHD (Chhabildas et al., 2001; Harrier & DeOrnellas, 2005).

One of the behavioural instruments often used, when diagnosing children with ADHD, is the Behavior Assessment System for Children (BASC; Reynolds & Kamphaus, 1992). The BASC is a multi-method, multidimensional instrument designed to evaluate the behaviour and emotions of children, including symptoms of ADHD. One advantage of the BASC, compared to other similar broadband behavioural instruments, is that it measures inattention symptoms and hyperactivity/impulsivity symptoms on two separate scales. Research has demonstrated the usefulness of the BASC in the diagnostic process of ADHD and shown that it is especially well suited in differentiating between subtypes of ADHD (e.g. Jarratt et al., 2005; Ostrander et al., 1998; Vaughn et al., 1997). In addition to ADHD symptoms, the BASC also evaluates symptoms of aggression, conduct problems, anxiety, depression, somatization, learning problems, atypical behaviour (autistic symptomatology) and withdrawal. To our knowledge, parent and teacher ratings on the BASC have not thus far been examined in relation to performance on EF tasks.

A recently developed neuropsychological battery for children, the NEPSY (Korkman et al. 1998), examines five domains of neuropsychological functioning in children. One of these is called Attention/Executive Functions,which is purported to be sensitive to ADHD symptoms. There have not been many validation studies comparing the NEPSY with behavioural measures (e.g. Schmitt & Wodrich, 2004). The NEPSY manual (Korkman et al., 1998) reports one study using the Devereux Scales of Mental Disorders (DSMD; Naglieri, LeBuffe, & Pfeiffer, 1994). The sample used was a mixed one of 10 non-clinical children and 13 children diagnosed with either ADHD or LD. The results of that study showed that DSMD ratings of attention and conduct problems were negatively correlated with Attention/Executive Functions Core Domain Scores on the NEPSY. The study also showed that internalizing problems were generally not related to neuropsychological functioning. Korkman et al. (2004) examined the validity of a newly developed parental rating scale, Five to Fifteen (FTF), in detecting developmental disorders in five-year-


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old children using the NEPSY as the external criterion measure. The FTF was designed to assess ADHD and comorbid conditions in 5 to 15 year old children (Kadesjö et al., 2004). The results of this study showed that the Attention/Executive Functions Domain of the NEPSY and the Attention and Impulsivity Domain of the FTF were only almost significantly related.

This study examined the association between parent and teacher ratings of ADHD symptoms and comorbid behaviour and performance on EF tasks. This is the first study on this relationship using broadband behavioural ratings that separate inattention and hyperactivity/impulsivity symptoms. The different aspects of EF examined were planning, vigilance and WM. The neuropsychological instruments used to assess EF, were the Towerand the Visual Attention subtests from the NEPSY and the Number Recall and WordOrder subtests from the Kaufman Assessment Battery for Children (K-ABC; Kaufman & Kaufman, 1983). The behavioural measures used were the parent rating scale (PRS) and the teacher rating scale (TRS) of the BASC. Based on the existing literature it was expected that EF measures would correlate with parent and teacher ratings of inattention and hyperactivity/impulsivity.

It has been demonstrated previously that measures of EF tend to correlate with IQ (e.g. Arffa et al., 1998; Harrier & DeOrnellas, 2005; Mahone et al., 2002), and it has been debated if IQ should be controlled for in studies on EF. It has been argued that it is a stronger case when EF differences exist after taking IQ into account (Sergeant et al., 2002). In view of the known relationship between EF and IQ, we assessed intellectual ability with the K-ABC. As language disorders have been found to be a highly prevalent comorbidity in ADHD (e.g. Cohen et al., 2000; Jonsdottir et al., 2005), language ability was assessed with the Test of Language Development (TOLD; Hammill & Newcomer, 1988).

METHOD

Participants

The sample consisted of 43 children (30 boys and 13 girls), aged 7-11 years (mean age was 9.27 years SD=1.34). Full Scale IQ was 99.88 (SD = 11.90). All the children had been referred for neuropsychological assessment because of serious behavioural and/or learning problems at the Department of Child and Adolescent Psychiatry of the Landspitali-University Hospital in Reykjavik, which is a tertiary facility serving the whole population of Iceland. Most of the children had the diagnosis of either ADHD combined or inattentive subtype. The diagnostic procedures used were an in-depth interview with the parents based on DSM-IV criteria, and parent/teacher ratings on the Icelandic versions of the Child Behavior Checklist (CBCL; Achenbach, 1991; Hannesdottir, 2002) and the ADHD rating scale (Magnusson et al., 1999).

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Instruments

TheNEPSY:ADevelopmentalNeuropsychologicalAssessmentThe NEPSY: A Developmental Neuropsychological Assessment (NEPSY; Korkman

et al., 1998) is a comprehensive measure of neuropsychological functioning in children aged 3-12 years. It has been validated for use with children diagnosed with learning disabilities, ADHD, autistic disorders, and speech and language impairment and is designed for use in a variety of cultural and ethnic groups. The NEPSY is divided into five functional domains. The tests used in this study are two subtests from the Attention/Executive Functions Domain: The Tower test and theVisualAttention test. The Tower test is designed to assess the EFs of nonverbal planning, monitoring, self-regulation, and problem solving. The child moves three colored balls to target positions on three pegs in a prescribed number of moves. The Tower test is based on the TowerofLondon test (ToL; Shallice, 1982) that has been extensively used in the neuropsychological literature to assess EFs. Studies have suggested that performance on the ToL relies to a large extent on the functioning of the frontostriatal system (Beauchamp, 2003; Owen, 1997). The VisualAttention test is designed to measure selective and sustained attention and assesses the speed and accuracy with which a child is able to focus selectively on and maintain attention to visual targets within an array. The child is penalized for both omission and commission errors, thus, in addition to vigilance, the test is also sensitive to inhibition. Standard scores with a mean of 10 and S.D. of 3 are used for the NEPSY subtests.

KaufmanAssessmentBatteryforChildren(K-ABC)The Kaufman Assessment Battery for Children (K-ABC; Kaufman & Kaufman, 1983)

is an individually administered measure of intelligence and achievement intended for children aged 2½ through 12½ years. It is based on research and theory in cognition and neuropsychology and is designed to measure ability (intelligence) on the basis of the processing style (sequential or simultaneous), required to solve tasks. The K-ABC has been widely used in the literature to assess cognitive function in children. Two subtests from the Sequential Processing scale: NumberRecall and WordOrder were combined to assess the EF of verbal WM (see Jonsdottir et al., 2005). The K-ABC uses standard scores with a mean of 100 and SD of 15 for its composites and a mean of 10 and SD of 3 for its subtests.

TestofLanguageDevelopment(TOLD)The Test of Language Development (TOLD; Hammill & Newcomer, 1988) is a

comprehensive measure of structural language designed to assess verbal ability in children. The TOLD is comprised of several subtests that are combined to make composite scores of a spoken language quotient (SLQ), receptive language, expressive language, semantics and syntax. The Icelandic version of the TOLD (Símonardóttir & Guðmundsson, 1996) was used here. The TOLD uses standard scores with a mean of 100 and SD of 15 for its composites and a mean of 10 and SD of 3 for its subtests.


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TheBehaviorAssessmentSystemforChildren(BASC)The Behavior Assessment System for Children (BASC: Reynolds, & Kamphaus, 1992)

is a well-validated comprehensive multidimensional measure designed to evaluate various externalizing, internalizing and school problems in children and adolescents aged 2½ to 18 years. It measures both adaptive and problematic dimensions, as well as behaviour linked to ADHD. The Parent Rating Scale (PRS) of the BASC has nine clinical scales. Three scales called Hyperactivity (including both hyperactivity and impulsivity items), Aggression, and ConductProblemsmeasure externalizing problems.Three scales calledAnxiety,Depression,and Somatization,assess internalizing problems.Three additional scales are calledAttentionProblems, Atypicalityand Withdrawal.The Teacher Rating Scale (TRS) has, in addition to the aforementioned nine scales, a clinical scale called LearningProblems. The child version of the BASC (ages 6-11) was used in this study. Parents and teachers rated 138 and 148 symptoms respectively. Symptoms are rated on a 4-point scale of frequency (never = 0, sometimes= 1, often= 2, and almostalways= 3).

Internal consistency coefficients (Kjartansdottir, 2002) for the BASC Icelandic-language version of the PRS child form range from .52 (Atypicality) to .90 (Depression). The TRS child form correspondingly has coefficients that range from .69 (Withdrawal) to .93 (Aggression).

Procedure

The NEPSY subtests, the K-ABC, and the TOLD were all administered to the participants by a licensed clinical child neuropsychologist according to the standard testing procedures. In addition, the children’s parents/teachers filled out the BASC versions for ages 6 to 11.


To analyse the group’s deviation from the standardized mean on tests of EF, the K-ABC and on the TOLD, t-tests were employed.

To compare parent/teacher ratings of the clinical group on the BASC with those of a normal school sample, t-tests were used. Effect sizes (eta squared: 2) were calculated, that is small .01, medium .06, and large .14. (Cohen, 1988).

In addition, correlational analyses were performed to investigate the relationships between EFs, intelligence and language measures. Furthermore, correlational analyses were performed to examine the relationships between parent/teacher ratings on the BASC and performance on EF tasks, intelligence and language ability, both with and without intelligence controlled.

Finally stepwise regression analyses were executed to analyse which cognitive variables best predicted parent/teacher ratings on the BASC.

Results were analysed utilizing SPSS version 11.0 for Windows.

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RESULTS

Means and standard deviations for age and the BASC TRS and PRS scores are presented in Table 1. As the BASC has not been standardized in the Icelandic population, the means and standard deviations for a normal Icelandic school sample of 115 children are provided for comparison (Jonsdottir et al, 2005, submitted). The results show that the clinical group examined in this study was rated significantly higher than the normal comparison group on the AttentionProblems and Hyperactivity subscales of the PRS and TRS of the BASC. In addition, the clinical group also scored significantly higher than the comparison group on most other clinical scales. The greatest difference between the groups, according to both parents and teachers, is on the AttentionProblems subscale, with large effects sizes ( 2 = .38 and .34, respectively).

TABLE 1

Comparison of Means and S.D.s for BASC Teacher Rating Scale (TRS) and Parent Rating Scale (PRS)

Clinical Group (n=43) Normal Controls (n=115)

Mean S.D. Mean S.D. F df p Eta

Age 9.27 1.34 9.05 1.65 .65 1,156 .42 .00BASC-TRSHyperactivity 14.23 11.14 7.03 7.02 22.24 1,152 .000 .13Aggression 11.87 10.19 7.15 7.88 8.96 1,152 .003 .06ConductProblems 3.36 3.59 1.68 2.35 11.16 1,152 .001 .07Anxiety 6.15 3.81 2.78 3.47 26.20 1,152 .000 .15Depression 8.56 6.27 3.11 3.88 40.99 1,152 .000 .21Somatization 4.38 4.34 1.83 2.85 17.67 1,152 .000 .10AttentionProblems 14.28 5.29 6.03 4.96 78.07 1,152 .000 .34LearningProblems 13.33 5.76 5.62 5.10 62.43 1,152 .000 .29Atypicality 5.56 4.19 1.28 2.38 62.04 1,152 .000 .29 Withdrawal 7.00 4.36 3.49 3.37 27.14 1,152 .000 .15

BASC-PRSHyperactivity 10.00 5.44 5.70 3.84 30.79 1,156 .000 .17Aggression 11.49 4.66 7.81 3.88 25.21 1,156 .000 .14ConductProblems 4.65 3.13 2.21 2.15 31.03 1,156 .000 .17Anxiety 12.09 6.13 7.67 4.50 24.57 1,156 .000 .14Depression 12.26 7.71 5.10 4.91 47.66 1,156 .000 .23Somatization 7.33 5.00 4.28 3.03 21.63 1,156 .000 .12Atypicality 5.51 3.86 2.36 2.25 40.40 1,156 .000 .21Withdrawal 5.42 2.68 5.36 3.14 .01 1,156 .91 .00AttentionProblems 12.12 3.61 5.71 3.64 97.37 1,156 .000 .38

Note:BASC, Behavior Assessment System for Children; TRS, teacher rating scale; PRS, parent rating scale.

BASC values are raw scores. Normal comparison group is an Icelandic school sample of 115 children


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Table 2 shows the means and standard deviations for the NEPSY Tower and VisualAttention subtests, the verbal WM composite, the K-ABC full-scale IQ (Mental Processing Composite, MPC), Sequential Processing, Simultaneous Processing and the full-scale language ability score (spoken language quotient, SLQ) of the TOLD. The results showed that the clinical group scored lower than expected on the Tower test, the VisualAttention test, and on verbal WM. The results also showed that the clinical group has an average full-scale IQ. However, the Sequential Processing score of the clinical group is lower than the expected group’s mean, but the Simultaneous Processing score of this group is higher than expected. Moreover, the group’s total language ability score was lower than would be expected.

TABLE 2

Means, S.D.s and deviations from expected group means for tests of executive function, Kaufman

Assessment Battery for Children and Test of Language Development

Mean S.D. t df p

Tests of executive function

Tower 7.90 2.61 -5.20 41 .000

VisualAttention 8.90 2.77 -2.51 39 .016

VerbalWorkingMemory 8.66 2.37 -3.69 42 .001

Kaufman Assessment Battery for Children (K-ABC)

MentalProcessingComposite(MPC) 99.88 11.90 -.06 42 ns

SequentialProcessing 93.26 12.56 -3.52 42 .001

SimultaneousProcessing 104.51 11.10 2.67 42 .011

Test of Language Development (TOLD)

SpokenLanguageQuotient(SLQ) 92.05 18.71 -2.69 40 .011

Note: K-ABC and TOLD values are standard scores (mean of 100, S.D. of 15),

Executive function values are standard scores (mean of 10, S.D. of 3).

Table 3 shows the Pearson correlations between the three executive measures (the Towertest, the VisualAttention test and verbalWM), and the relationship between the EF tasks and the K-ABC MPC, Sequential Processing and Simultaneous Processing scales, and the TOLD SLQ scale. Of the three EF tasks, only verbalWM appeared to be significantly related to Tower. Moreover, the different EF functions were significantly related to all IQ measures, except the VisualAttention test was not related to the Sequential Processing scale. Only verbal WM was significantly related to the language test, the TOLD. The results further showed that language ability as measured with the TOLD is significantly related to intelligence, as measured with the K-ABC (r = .51, p = .001).

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TABLE 3

Pearson Correlations between tests of executive function, intelligence and language development

EF tests K-ABC Tower Vis.Att. V.WM MPC Seq.Pr. Sim.Pr. SLQ

Tower 1 .04 .42** .43** .41** .36* .13

VisualAttention 1 .24 .44** .24 .51** .31

VerbalWM 1 .83** .95** .58** .48**

Note: EF, executive function; K-ABC, Kaufman Assessment Battery for Children; TOLD, Test of Language Development; Vis. Att., Visual Attention; V. WM, verbal working memory; MPC, Mental Processing Composite; Seq. Pr., Sequential Processing; Sim. Pr., Simultaneous Processing; SLQ, Spoken Language Quotient.

**. Correlation is significant at the 0.01 level (2-tailed).

*. Correlation is significant at the 0.05 level (2-tailed).

Table 4 shows the Pearson correlations between the BASC TRS and PRS and performance on the Tower test, the VisualAttention test, verbalWM, K-ABC and TOLD. The major finding is that there were no significant relationships between teacher rated hyperactivity symptoms and EFs, IQ and language. There were no significant correlations between parent rated symptoms of ADHD (Hyperactivity,AttentionProblems) and the cognitive measures. In contrast, teacher rated symptoms of inattention were significantly related to the Tower test (r = -.38, p = .02), the K-ABC full-scale IQ (r = -.33, p = .04), simultaneous processing (r = -.36, p = .03), and language (r = -.38, p = .02).

Another major finding is that there were significant correlations between teacher rated LearningProblems and all three EF measures: Tower (r = -.33, p = .04), VisualAttention (r = -.46, p = .004), and verbal WM (r = -.49, p = .002). Teacher rated LearningProblems were significantly and negatively related to intelligence (r = -.62, p = .000), and language ability (r = -.67, p = .000).

Interestingly, teacher rated Atypicality and Depression was significantly and negatively related to the Tower test (r = -.43, p = .007 and r = -.38, p = .02 respectively) and teacher rated Anxiety was significantly and negatively related to the VisualAttentiontest (r = -.37, p = .03).

The only significant relationship on the PRS was between ConductProblemsand the VisualAttention test (r = -.32, p = .05).

TOLD


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TABLE 4

Pearson correlations between BASC TRS and PRS and performance on tests of attention/executive

function, intelligence and language development

Tower Vis. Att. V. WM MPC Seq. Pr. Sim. Pr. SLQ

BASC-TRS

Hyperactivity -.29 -.03 .14 .01 .15 -.10 .11

Aggression -.09 -.02 .05 -.00 .09 -.07 .17

ConductProblems -.14 -.07 -.07 -.14 -.07 -.17 .06

Anxiety -.26 -.37* -.07 -.16 -.08 -.19 -.29

Depression -.38* -.19 -.17 -.09 -.09 -.06 .01

Somatization -.31 -.16 -.10 -.09 -.08 -.09 -.16

AttentionProblems -.38* -.21 -.19 -.33* -.19 -.36* -.38*

LearningProblems -.33* -.46** -.49** -.62** -.57** -.54** -.67**

Atypicality -.43** -.32 -.04 -.09 -.05 -.11 .04

Withdrawal -.16 -.16 -.29 -.11 -.21 -.01 -.26

BASC-PRS

Hyperactivity -.27 -.24 -.15 -.23 -.08 -.30 .09

Aggression -.18 -.17 -.16 -.15 -.07 -.18 .21

ConductProblems -.15 -.32* -.06 -.12 -.01 -.19 .16

Anxiety -.16 .02 -.11 -.07 -.10 -.04 -.08

Depression -.29 .05 -.11 -.09 -.04 -.11 .09

Somatization -.16 -.08 -.07 -.11 -.06 -.13 .02

Atypicality -.06 -.03 -.23 -.03 -.16 .07 -.01

Withdrawal -.06 .11 -.05 -.02 -.06 .02 .26

AttentionProblems -.10 .07 -.25 -.16 -.21 -.11 -.22Note: Vis. Att., Visual Attention; MPC, Mental Processing Composite (full scale intelligence), Seq. Pr., Sequential Processing; Sim. Pr., Simultaneous Processing; V. WM, verbal working memory; SLQ, Spoken Language Quotient; BASC, Behavior Assessment System for Children; TRS, Teacher Rating Scale, PRS, Parent Rating Scale

Bold fonts for significant correlations (*p <0.05; **p <0.01).

In order to examine to what extent EFs and behavioural variables were due to IQ, partial correlations were run with IQ as a covariate (see Table 5). When the influence of IQ on EFs was controlled, only associated ADHD behaviour was related to executive functioning. Teacher rated Atypicalityand Depression related significantly and negatively with the Tower test (r = -.43, p = .008, and r = -.37, p = .02, respectively). Teacher rated Anxiety and Atypicality was significantly and negatively related to VisualAttention (r = -.34, p = .05 and r = -.34, p = .04), and teacher rated Withdrawal was significantly and negatively related to verbal WM (r = -.37, p = .02).

On the PRS ConductProblems were significantly and negatively related to VisualAttention(r = -.38, p = .02), and Atypicality was significantly and negatively related to verbalWM (r = -.35, p = .03).

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TABLE 5

Pearson correlations between BASC TRS and PRS and tests of executive function controlling for

intelligence

Tower VisualAttention VerbalWM¹BASC-TRS

Hyperactivity -.32 -.08 .25

Aggression -.09 -.05 .11

ConductProblems -.09 -.04 .06

Anxiety -.22 -.34* .10

Depression -.37* -.19 -.21

Somatization -.32 -.17 -.04

AttentionProblems -.28 -.10 .07

LearningProblems -.09 -.25 -.15

Atypicality -.43** -.34* .04

Withdrawal -.13 -.15 -.37*

BASC-PRS

Hyperactivity -.20 -.19 -.05

Aggression -.13 -.15 -.13

ConductProblems -.11 -.32* -.03

Anxiety -.14 .05 -.10

Depression -.27 .06 -.09

Somatization -.14 -.09 .01

Atypicality -.04 -.09 -.35*

Withdrawal -.04 .11 -.10

AttentionProblems -.04 .15 -.26

Note: BASC, Behavior Assessment System for Children; TRS, Teacher Rating Scale, PRS, Parent Rating Scale¹K-ABC Nonverbal Intelligence Scale was used to control for intelligence

Bold fonts for significant correlations (*p<0.05; **p<0.01).

In order to examine which cognitive variables best predicted behaviour on the BASC TRS and PRS, stepwise regression analyses were performed (see Table 6). Table 6 shows that the TRS Atypicality and Depression subscales were best predicted by performance on the Tower test. Teacher ratings of AttentionProblems were best predicted by performance on the language test (TOLD). Low scores on both the language test and the intelligence test best predicted teacher ratings of LearningProblems. No parent ratings were significantly predicted by performance on EF tasks.


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TABLE 6

Stepwise regression analyses for cognitive variables predicting ratings on BASC TRS and PRS



TRS Depression 4.29 .05

Tower -.89 -2.07 .05

TRS Attention Problems 6.34 .02

SLQ -.12 -2.52 .02

TRS Learning Problems 18.62 .000

SLQ -.13 -2.99 .005

MPC -.20 -2.97 .006

TRS Atypicality 7.45 .01

Tower -.72 -2.73 .01

Note: BASC, Behavior Assessment System for Children; TRS, Teacher Rating Scale; PRS, Parent Rating Scale; SLQ, Spoken Language Quotient; MPC, Mental Processing Composite.

Predictors in the model: Tower,VisualAttention,VerbalWorkingMemory,MPC,andSLQ.

DISCUSSION

The aim of the present study was to examine the relationship between neuropsychological measures of attention/executive functions and behavioural symptoms of ADHD and associated behaviour as rated by parents and teachers. Previous studies have shown a lack of consistency between these measures, although they are all meant to assess similar constructs (e.g. Naglieri et al., 2005).

One of the main findings of our study is that, when intelligence was controlled for, there were no significant relationships between parent and teacher ratings of ADHD symptoms and performance on EF tasks. These findings are in agreement with those of Marks et al. (2005), who studied the neuropsychological status of 22 preschoolers at risk for ADHD. They found no relations between performance on executive measures and objective indices of activity level or ratings of ADHD symptoms. The authors concluded that their findings cast doubt on whether EF deficits and/or frontostriatal networks contribute etiologically to early behavioural manifestations of ADHD. Sonuga-Barke et al. (2002) did not find any association between the EFs of planning and WM and symptoms of ADHD in a heterogeneous sample of preschool children. Our findings contrast with those of Oosterlaan et al. (2005), who found relationships between teacher rated ADHD and performance on EF tests. The authors concluded that EF deficits were unique to ADHD and not caused by associated conduct problems. The reason for the conflicting results might be that Oosterlaan et al. used different rating scales to assess ADHD symptoms and

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different tasks to assess EFs than we did. Another main finding of our study is that we found significant relationships between

EF tasks and behavioural constructs commonly co-occurring with ADHD and between non-EF tasks and ADHD symptoms, but only for teacher rating of behaviour. Our findings partly agree with those of Sarkis et al. (2005), who studied the impact that comorbidity in children with ADHD has on EF. In their study a computerized version of the Tower of London (ToL) test was used to assess EF and a semi-structured interview with the parents was used to assess behaviour. Sarkis et al. found that comorbid disorders did not have a significant effect on performance of EF. Similarly in our study, we did not find a significant association of parent ratings with EF. In contrast, teacher ratings of comorbid ADHD symptoms were significantly related to performance on EF tasks.

Interestingly, among the three different aspects of EF examined in our study, only the Towertest and verbal WM were significantly related (Table 3). A recent study by Joseph et al. (2005) showed, that the NEPSY Tower test was significantly related to language ability in normal children but not in children with autism. The authors interpreted this finding as suggesting that children with autism are less able than normal children to verbally encode and manipulate goal-related information in WM, when performing the Tower task. Lewis et al. (2003) showed a positive relationship between verbal WM and performance on the Tower of London (ToL) test in patients with Parkinson’s disease. They found that patients with impaired performance on the ToL were specifically impaired at manipulating information within verbal WM, compared to both controls and patients who were not impaired on the ToL. These findings are somewhat surprising considering that the towers tests are considered to be visuospatial and non-verbal measures of EF.

All three measures of EF were significantly related to IQ, except the VisualAttention test, which was not significantly related to the Sequential Processing scale of the K-ABC. These findings are in line with previous research that has shown a strong relationship between IQ and EF (Arffa et al., 1998; Harrier & DeOrnellas, 2005; Mahone et al., 2002). On the other hand, only verbal WM was significantly related to language development, supporting the contention that the core problem in language disorders is deficient verbal WM (e.g. Baddeley & Wilson, 1993; Gathercole & Baddeley, 1989; Montgomery, 2003; Swank, 1999).

Interestingly, the Tower test was the only EF measure that related to ratings of behaviour, i.e. teacher ratings of depressive and autistic symptomatology (Table 6). Previous studies have found impairment in performance on towers tests in groups suffering from depression. Purcell et al. (1997) studied neuropsychological function in young patients with unipolar major depression. Among their findings was that, compared to controls, the depressive group displayed impaired subsequent movement latencies on the ToL task. The authors interpreted this finding as suggesting deficits in the ability to sustain motor responses in depression. Sarkis et al. (2005) found that, although the presence of mood disorders did not predict total move score in a sample of ADHD children, those children with comorbid mood disorders took more moves to solve a ToL problem than other children. The authors speculated that this might be caused by depression symptoms of psychomotor


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retardation, fatigue, or reduced ability to concentrate. Similarly, Goethals et al. (2005) studied planning times and accuracy in depressed patients and found that, compared to controls, they spent more time thinking, although they were just as accurate. In view of the current and previous reseach, it might be speculated that ineffective performance on towers tests might in part be caused by depression.

The strong relationships between performance on the Tower test and ratings of Atypicality on the TRS of the BASC, is a somewhat unexpected finding.According to Reynolds & Kamphaus (1992), clinical groups with childhood autism and depression have been found to score high on the Atypicality scale. These two clinical groups have also been found to score high on the Hyperactivity and AttentionProblems scales of the BASC showing the great overlap between these childhood disorders (e.g. Bradshaw & Sheppard, 2000; Blackman et al., 2005; Clark et al., 1999; Towbin et al., 2005). Studies have shown that ADHD and autism often co-occur (Geurts et al., 2004; Sturm et al., 2004) and that it may prove to be difficult to differentiate between these two disorders on behavioural scales commonly used to screen for attentional and behavioural disorders (Jensen et al., 1997). Children with high functioning autism (HFA) have been shown to have more general and severe EF deficits (Geurts et al., 2004; Pennington & Ozonoff, 1996), and to score lower on towers tests, than children with ADHD (Sergeant et al., 2002). Childhood autism, depression and ADHD are all neurodevelopmental disorders that often co-occur and have all been associated with dysfunction of the frontostriatal system (Bradshaw & Sheppard, 2000) which in turn has been shown to be involved in the performance of the towers tests (e.g. Dagher et al., 2001; van den Heuvel et al., 2003).

The finding that the VisualAttention test was not significantly related to parent/teacher ratings of inattention supports previous findings indicating that ADHD is not characterized by deficient visual attention (e.g. Booth et al., 2005; Huang-Pollock & Nigg, 2003; van der Meere et al., 1991). The finding that a test of language development best predicted teachers’ ratings of inattention in children is intriguing. Language impairment (LI) is highly prevalent in children with psychiatric disorders and behavioural problems. The most common psychiatric diagnosis of children with LI is ADHD (Cohen et al., 1998, 2000), and conversely, LI is a frequent comorbidity in children with ADHD (Cantwell, 1996; Kovac et al., 2001; Purvis & Tannock, 1997). In children referred for psychiatric services, those with LI have been shown to be the most impaired regardless of the psychiatric diagnosis (Cohen et al., 2000). Additional studies have shown that the EF construct of WM, which has been considered to be a core problem in ADHD, is more closely related to LI than to ADHD (Cohen et al., 2000; Jonsdottir et al., 2005). Denckla (2003) has suggested that many of the externally observable diagnostic characteristics of ADHD, particularly of the inattentive subtype, might be caused by language processing difficulties. Our results here seem to support that contention. It is somewhat surprising that in spite of the fact that language disorders are so frequently associated with ADHD, they are not generally screened for in its diagnostic process.

Regression analyses (see Table 6) showed only relationships between the various cognitive constructs and teacher as opposed to parent ratings of behaviour. These results

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are similar to those of previous studies (e.g. Oosterlaan et al., 2005) emphasizing that teachers may be better informants of neuropsychological problems in children than parents. The reason for that might be that teachers see children in more structured situations than parents do, and that they focus on cognitive functions. Teachers also have the benefit of being able to compare children with a large number of other children.

Taken together, our findings suggest that EF deficits in ADHD may be indicative of possible autistic and/or depressive symptomatology. The results of the study do not support the EF theory of ADHD. Our results further imply that inattention symptoms in ADHD may in some cases be caused by language disorders and highlight the importance of screening for language ability when assessing ADHD in children.


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CHAPTER FIVE 5Effects of transcutaneous electrical nerve stimulation (TENS) on cognition, behaviour, and the rest-activity rhythm in children with attention-deficit hyperactivity disorder combined type


Neurorehabilitation and Neural Repair, Volume 18, Number 4, December 2004, Pages 212-221

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ABSTRACT

Objective:The aim of this study was to examine the effects of transcutaneous electrical nerve stimulation (TENS) on cognition, behaviour and the rest-activity rhythm in children with attention deficit-hyperactivity disorder, combined type (ADHD-CT).

Methods: Twenty-two children diagnosed with ADHD-CT received TENS treatment during 6 weeks, 2 times 30 minutes a day. Neuropsychological tests were administered to assess cognition, parent/teacher behavioural rating scales were used to measure behaviour and actigraphy was used to assess the rest-activity rhythm.

Results:TENS appeared to have a moderate beneficial influence on cognitive functions that load particularly on executive function (EF). There was also improvement in behaviour as measured by parent/teacher behavioural rating scales. Moreover, motor restlessness during sleep and motor activity during the day decreased by TENS.

Conclusions:The effects of TENS in children with ADHD are modest but encouraging and warrant further research.

TENS therapy in ADHD

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INTRODUCTION

Attention deficit hyperactivity disorder (ADHD) is the most common neuropsychiatric disorder of childhood, affecting between 1% and 7% of children depending on the stringency of criteria used (American Psychiatric Association, 1994, 2000; Swanson et al., 1998). The condition is manifested by excessive motor activity, impulsivity, and inattention and is associated with impairments in academic and social functioning. The etiology of the disorder is not known at this time, but several theories have been proposed to explain it. Barkley (1997) has argued that the various deficits observed in ADHD, including apparent attentional problems, are caused by one main feature: an impairment in the development of delayed responding or response inhibition. He has put forth a theory that specifies that behavioural inhibition facilitates the effective performance of four executive neuropsychological functions: working memory, internalization of speech, self-regulation of affect-motivation-arousal, and reconstitution (behavioural analysis and synthesis). These four executive functions influence the motor system in the service of goal-directed behaviour and originate within the brain’s motor system (prefrontal and frontal cortex). The prefrontal cortex and its connections with the striatum play an important role in executive functions (Mercugliano, 1999). A relation has been observed between the volumetric properties of the frontostriatal system and the performance on inhibition tasks (Casey et al., 1997). Abnormalities in the function and structure of the frontostriatal system have been observed in children with ADHD (Mercugliano, 1999; Shelley-Tremblay & Rosen, 1996), and a decrease in inhibition is a main hallmark of ADHD (Oosterlaan & Sergeant, 1998; Rubia et al., 1998). Sergeant, Oosterlaan and van der Meere (1999) have argued that it is an oversimplification to conclude that ADHD children uniquely suffer from an inhibition deficit that accounts for all of the experimental findings of impaired performance on a myriad of tasks. They have used information-processing theory and its associated energetic model (arousal, activation, and effort) for isolating the central deficits in ADHD within that paradigm. They emphasize the inadequate allocation of cognitive-energetic resources during the motor output stage of information processing. Douglas (1999) on the other hand, has viewed attentional and inhibitory deficits as different manifestations of an underlying regulatory control problem and believes this to be a more inclusive conceptual framework within which attentional, inhibitory and motor- processing problems can be integrated.

Research has shown that ADHD is associated with various neuropsychological deficits, such as difficulties with planning and forethought, delay of gratification, resistance to temptation, and sustained goal-directed behaviour (Barkley, 1997). They also include deficiencies in problem solving, flexibility of responding, working memory, and self-directed private speech, which is believed to comprise the phonological loop in verbal working memory (Barkley, 1997). These deficits have in common their association with the concept of executive functioning (Denckla, 1996).

Sleeping disorders have been frequently reported in ADHD children and used to be a diagnostic criterion for ADHD (American Psychiatric Association, 1980; Barkley,

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1998; Marcotte et al., 1998; Ring et al., 1998). ADHD children have been shown to be more motor active in their sleep (Porrino et al., 1983) and to have a more unstable sleep-wake system (Gruber et al., 2000) than normal children. Thunström (2002) found that approximately one in four children with severe sleep problems in infancy would later qualify for the diagnosis of ADHD. A recent study by O’Brien and colleagues (2003) found that both stimulant-medicated and nonmedicated ADHD children had more sleep disturbances than controls. They also found that children with ADHD spend less time in rapid eye movement (REM) sleep than controls. During REM sleep, most muscles of the body are relatively paralyzed, so there is no motor activity during that time. The fact that ADHD children spend less time in REM sleep than other children might be one explanation for more motoric activity during sleep. Studies have indicated that REM sleep may be associated with the secretion of brain-derived neurotrophic factor (BDNF), which in turn is believed to be involved in sleep regulation (Sei et al., 2000, 2003).

Stimulant drug therapy is the most frequently used and the most effective therapy known today for ADHD (Barkley, 1998; Shaywitz et al., 2001). The limitations of stimulant drug therapy are that although it helps 65% to 75% of ADHD children (Santosh & Taylor, 2000), there are many nonresponders, there are some side effects, there is a need for frequent dosing, there is an abuse potential, there are wear-off or rebound effects (Findling & Dogin, 1998; Garland, 1998), and many parents are reluctant to give their children drugs. In view of these limitations, it is of utmost importance to seek and develop safe alternative nonpharmacological types of stimulation for ADHD. One type of nonpharmacological neuronal stimulation is transcutaneous electrical nerve stimulation (TENS).

In a series of studies, the effects of TENS on memory, (affective) behaviour, and the rest-activity rhythm were examined in patients with probable Alzheimer’s disease (AD) (Scherder et al., 1992, 1995, 1998, 1999, 2000; Van Someren et al., 1998). The results showed that visual short-term memory, visual and verbal long-term (recognition) memory and verbal fluency improved with TENS. In addition, patients who were stimulated participated more independently in activities of daily life and showed an improvement in their mood and in their rest-activity rhythm. The improvement in the rest-activity rhythm of the AD patients implied that the nightly restlessness decreased.

One explanation for the observed treatment effects might be that TENS activates the hippocampus, the hypothalamus, and the hypothalamic suprachiasmatic nucleus (SCN), the “biological clock” of the brain, through direct spinoseptal and spinohypothalamic pathways (Burstein & Giesler, 1989; Burstein et al., 1990; Cliffer et al., 1991; Giesler et al., 1994). These areas are involved in memory processes (Carpenter & Grossberg, 1993), affective behaviour, and the rest-activity rhythm (Swaab, 1997; Swaab et al., 1998), respectively, and are affected in AD (Braak & Braak, 1991; Scheltens et al., 1992; Swaab, 1997). Alternatively one could also argue that TENS stimulates the ascending reticular activating system (ARAS) through, for example, the locus coeruleus and the nucleus raphe dorsalis (Scherder et al., 2003). These brain stem areas, which are the origin of the noradrenergic and serotonergic system, respectively (Rossor, 1988), are part of the


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ARAS (Kayama & Koyama, 1998). One of the end fields of the ARAS is the prefrontal cortex (Robbins & Everitt, 1995), which plays a crucial role in executive functions, such as inhibition (Casey et al., 1997; Jonides et al., 1998; Rosenberg et al., 1997; Strik et al., 1998) and working memory.

Based on the positive effects of TENS on cognition, behaviour and the rest-activity rhythm in AD patients and the rationale underlying those effects, that is, TENS might stimulate cortical activity through the ARAS, it was hypothesized in the present study that TENS could have a beneficial influence on cognition, behaviour and the rest-activity rhythm in children with ADHD.

METHODS

Subjects

The sample consisted of 22 children (21 boys and 1 girl), drawn from schools, from an ADHD advisory centre, and from an ADHD patients’ association. The children had been diagnosed with ADHD combined type (DSM-IV) by a paediatrician or a child psychiatrist on the basis of a clinical interview. To further support the diagnosis, the Disruptive Behavior Disorders Rating Scale (Pelham et al., 1992), Dutch version (Oosterlaan et al., 2000) was administered to the parents and the teacher. They filled in the questionnaire independent from each other. The items belong to one of four DSM-IV disorders: attention deficit (9 items), hyperactivity/impulsivity (9 items), oppositional defiant disorder (16 items), and conduct disorder (16 items). Raw scores were transformed into percentile scores. The cut-off score for inclusion in the present study was set at a percentile score of 90 for attention deficit and hyperactivity/impulsivity on questionnaires from both parents and teachers.

The patients ranged in age from 8 to 14 years, with a mean age of 10.59. Children were included if they had normal intelligence and when they were prepared to be medication free during the study period of 12 weeks. Individuals were excluded from participation in this study if they had a history of epilepsy, dyslexia, pervasive developmental disorder, schizophrenia, Gilles de la Tourette, or a personality disturbance.

The parents and the children were extensively informed about the goal and the procedure of the study and gave their informed consent. It was emphasized that a beneficial influence of TENS on cognition, behaviour, and the rest-activity rhythm could not be guaranteed. Next, the patients were familiarized with the electrostimulation method by applying a trial treatment during which they could experience the electrical stimulus. The parents and the children subsequently gave their informed consent.

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Materials and procedure

To evaluate possible treatment effects on cognition, behaviour, and the rest-activity rhythm, several neuropsychological tests, a behavioural rating scale, and actigraphy were applied, respectively, before the onset of the treatment period (pre), directly after the 6-week treatment period (post), and again after 6 weeks without treatment (delayed). The administration of the tests took place by an investigator who was not blind with respect to treatment. Similarly, the parents and the teachers who filled in the behavioural rating scales knew that the child received TENS treatment.

Neuropsychological tests

The subtests Arithmetic,DigitSpan and Codingfrom the Wechsler Intelligence Scale for Children-Revised (WISC-R) (Wechsler, 1974) can be combined into one separate IQ factor, called FreedomfromDistractibility (Kaufman, 1975), also sometimes called the “ThirdFactor” (F3IQ).The subtest Arithmetic implies that the children have to solve sums, for which fundamental arithmetical skills are required (e.g. subtracting) (M= 10). On the subtest Coding, the child is asked to associate a specific number with a specific symbol (M= 10). On the subtest DigitSpan, the child has to repeat a number of digits in the same and in a reversed sequence. Besides a variety of cognitive functions, all three subtests may be considered to tap the executive function of working memory (Barkley, 1997; Denckla, 1996).

The Bourdon-Vos(Bourdon & Wiersma, 1962) is a task that requires sustained visual attention and visuomotor speed. The test consists of a sheet of paper with groups of dots printed on it. Each group has a varying number of dots, that is, 3, 4, or 5 dots, and moreover, the dots are differently situated in each group. The child is asked to cross out as quickly and accurately as possible the groups with 4 dots. Administration of the Bourdon-Vos results in two scores: 1) the mean time in seconds per line (M= 10) and 2) the total number of omissions (M= 15) (Zeeuw, 1995). Test-retest reliability for the mean time per line appeared to be 0.87, and interrater-reliability was 0.91 (Zeeuw, 1995).

The StroopColourandWordTest, Dutch version (Hammes, 1971), is meant to measure executive (cognitive) processing. The test consists of three cards with 100 items each. All items relate to the colours red, yellow, blue, and green. On card 1, the names of these four colours are printed in black ink and the child is asked to read aloud the printed names as quickly as possible. Subsequently, card 2 is presented to the child. On card 2, the colours themselves are shown, and the subject is required to name the colours as quickly as possible. On card 3, the colour of the ink does not match the name of the colour. For example, the word redis printed in yellow ink. The child is asked to read aloud the colour of the ink (e.g., yellow), instead of the name of the colour (e.g., the word red), as quickly as possible. For an adequate performance, the child has to suppress the impulse to read the words themselves. The difference in time between card 2 and card 3 results in an interference score. A high interference score may point to a deficit in executive function.


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Children with ADHD have been shown to be slower than controls on the Stroop tasks (Nigg et al., 2002).

Behavioural measures

The Revised Conners Parent and Teacher Rating Scales (Goyette et al., 1978) was used to rate the various behavioural symptoms. The scale includes 7 subscales, that is, conduct problems I (max. score: 30), learning problems (max. score: 12), psychosomatic problems (max. score: 15), impulsive-hyperactive (max. score: 12), conduct problems II (max. score: 9), anxiety (max. score: 12), and other items (max. score: 54). A lowering of the score implies an improvement in behaviour.

Actigraphy

The rest-activity rhythm was assessed using actigraphy (Van Someren et al., 1998), for three periods: five days before treatment (pre) during which the children were medication free, five days immediately following a 6-week treatment period (post), and again five days after a treatment-free period of six weeks (delayed). On each occasion, the child wore an actigraph around the right wrist. The actigraph registers arm movements. From the resulting rest-activity rhythms, five variables were calculated: 1) The interdaily stability (IS) quantifies the strength of coupling between the rest-activity rhythm and supposedly stable zeitgebers. In normal cases, the activity patterns of individual days resemble each other very much, whereas days may differ considerably with rhythm disturbances. 2) The intradaily variability (IV) quantifies the fragmentation of the rhythm, that is, the frequency and extent of transitions between rest and activity. In normal cases, one has a major activity period during the day and a major inactivity period during the night, whereas brief alternating bouts of rest and activity are characteristic of rhythm disturbances. 3) The relative amplitude (RA) quantifies the difference between the main activity (day) and rest (night) periods. 4) M10 reflects 10 hours of the child’s maximum activity within 24 hours. 5) L5 represents the 5 least active hours within 24 hours. In normal cases, the daytime activity is high and the nighttime activity is low, resulting in high amplitude. With circadian rhythm disturbances, nighttime activity may increase, whereas daytime activity may decrease resulting in a low amplitude.

TENS treatment

Frequency and intensity. The children were treated with an electrostimulator, type Premier 10s. This stimulator generates transcutaneous electrostimulation that consists of asymmetric biphasic square impulses, applied in bursts of trains, nine pulses per train, with an internal frequency of 160 Hz, a repetition rate of 2 Hz, and a pulse width of 100 μseconds. This type of TENS is known as BURST-TENS (Eriksson et al., 1979). The intensity of the stimulation triggered visible muscular twitches, which were painless. A

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flickering green light placed on the electrostimulator indicated stimulation. Location. Two 2 x 3 cm (h x w) self-adhesive carbon rubber electrodes were fixed on

the patient’s back between Th1 and Th5, each on one side of the spinal column.

Duration. The children were offered a stimulation time of 30 minutes, twice a day, that is, early in the morning between 0700 and 0800 before going to school and after school, in the afternoon between 1600 and 2000. TENS was applied at home, by one of the parents, 7 days a week during a 6-week period.

Trialtreatment. The children were familiarized with the electrostimulation method by applying a trial treatment during which they could experience the electrical stimulus. During the trial period, no negative reactions to TENS were observed.

Data analyses

For each of the neuropsychological tests, the (subscales of the) observation scale, and the actigraphy variables (IS, IV, RA, L5 and M10), one-tailed nonparametric Wilcoxon signed rank tests were used at a 0.05 significance level on two contrasts: pre versus post and post versus delayed. In addition, effect sizes were calculated, d’ = .20 is small, d’ = .50 is moderate, and d’ = .80 is large (Cohen, 1988).

RESULTS

Cognition

The third factor (Freedom from Distractibility). Data-analyses by means of the nonparametric Wilcoxon signed rank test showed that after a treatment period of 6 weeks, the children showed a significant improvement in the total score of F3IQ. The effect size d appeared to be small: .19. Analyses of the posttreatment scores on the three subtests revealed only a significant higher score on the subtest Coding, with a small to moderate effect size d of .31 (see Table 1 for means, standard deviations, and the Wilcoxon signed ranks test). After a treatment-free period of 6 weeks, the observed higher scores on F3IQ and Coding had disappeared (see Table 1).

Bourdon-Vos. Data-analyses revealed that the time during which the Bourdon-Vos was performed was significantly shorter after the treatment period, compared to the performance before the treatment-period. The effect size d was small to moderate: .28. Not only did the duration of the performance of the test decrease, but also the number of omissions decreased significantly, with a moderate effect size d of .49. After the period without treatment, data-analyses showed no further significant decline in the duration of task performance and the number of omissions.


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with a moderate effect size d of .49. After the periodwithout treatment, data analyses showed no further sig-nificant decline in thedurationof taskperformanceandthe number of omissions.

Stroop. TheWilcoxon Signed Ranks Test showed thatthe interference score (card 3 minus card 2) decreasedsignificantlyafter the treatment period. Theeffect sizedwasmoderate: .48.No further significant decreasein theinterference score was observed during the treatment-free period (see Table 1 for means, standard deviations,and the Wilcoxon Signed Ranks Test).

Behavior

TheRevisedConners Parent andTeacherRatingScales, Par-ent version. Data-analyses by means of the WilcoxonRanked Signs Test showed that, according to the par-ents, the child’s overall behavior significantly improvedafter the treatment period. The effect size d was large:.81 (see Table 2 for means, standard deviations, and theWilcoxonSignedRanks Test). Morespecifically, accord-ingto theparents, thechildren improvedsignificantlyonall subscales, with moderate to large effect sizes d rang-ing from .25 (subscaleAnxiety) to 1.14 (subscale Impul-sive/Hyperactive). After the treatment-free period of 6weeks, the observed improvements remained level. Formeans, standard deviations, and the Wilcoxon SignedRanks Test, see Table 2.

The Revised Conners Parent and Teacher Rating Scales,Teacher version. Similar to the parents’ version, the teach-ers also found that the overall behavior of the childrenimproved significantly after the treatment period. How-ever, theeffect sizedwas moderate: .37. It is noteworthy

that after the stimulation was ended the children’s over-all behavior further improved during the treatment-freeperiod, with even a somewhat larger effect size dof .51.With respect to the various subscales, significant im-provements were observed for the subscales LearningProblems, Impulsive/Hyperactive, and Conduct Prob-lems II, with small to moderate effect sizes dof .23, .52,and .28, respectively. Thescores on these3 subscales didnot change significantly after the treatment-free period(for means, standard deviations, and the WilcoxonSigned Ranks Test, see Table 2).

Rest-Activity Rhythm

As Table 3 shows, the scores on the actigraphy vari-able L5 significantly declined after the treatment periodof 6 weeks. Although the M10 variable also declined, itdid not reach statistical significance. The effect sizes dwere .92 (large) and .66 (moderate), respectively (formeans, standard deviations, and the Wilcoxon SignedRanks Test, see Table 3). No treatment effects wereobserved with respect to IS, IV, and RA. Of note is thatthescoreonL5 showedasignificant increaseafter the6-week period without treatment (moderate effect size dof .60). The increase in scores on M10 after the treat-ment-free period was not significant (for means, stan-dard deviations, and the Wilcoxon Signed Ranks Test,see Table 3).

DISCUSSION

The goal of the present pilot study was to examinewhether TENS, a nonpharmacological central nervoussystem stimulant, could have a beneficial influenceon cognition, behavior, and the rest-activity rhythm ofchildren with ADHD. The results will be discussed

Neurorehabilitation and Neural Repair XX(X); 2004 5

Effects of TENS on ADHD

Table 1. Means, StandardDeviations, and theWilcoxonSignedRanks Tests (Z Scores, P Values)withRespect to theScores on theVarious Neuropsychological Tests, Administeredbeforeandafter aTreatment Periodof 6 Weeks andafter aTreatment-FreePeriodof 6 Weeks

Wilcoxon WilcoxonPre Post Delay Pre-Post Post-Delayed

Neuropsychological Tests M SD M SD M SD Z P Z P

Third factor total score 85.73 13.20 88.59 13.33 90.53 9.74 1.83 0.03 1.22 0.22Arithmetic 7.23 2.43 7.19 2.08 7.16 2.46 0.16 0.44 0.35 0.73Digit Span 8.41 3.12 8.59 2.17 9.00 2.56 0.65 0.26 1.29 0.20Coding 7.77 3.53 8.68 3.40 9.58 2.36 1.98 0.02 1.15 0.25Bourdon-Vos Time (seconds) 17.92 4.15 16.76 4.83 14.72 3.37 2.69 0.004 1.89 0.06Bourdon-Vos Omissions 21.67 30.66 9.24 7.01 7.84 7.76 2.37 0.009 0.88 0.38Stroop Card 3 – Card 2 96.41 44.60 73.72 30.87 60.44 29.38 1.82 0.03 1.60 0.11

Stroop. The Wilcoxon signed rank test showed that the interference score (Card 3 minus Card 2) decreased significantly after the treatment period. The effect size d was moderate: .48. No further significant decrease in the interference score was observed during the treatment-free period (see Table 1 for means, standard deviations, and the Wilcoxon signed rank test).

TABLE 1

Means, standard deviations, and the Wilcoxon Signed Rank Tests (Z-scores, p-values) with

respect to the scores on the various neuropsychological tests, administered before and after a

treatment period of 6 weeks and after a treatment-free period of 6 weeks.

Behaviour

TheRevisedConnersParentandTeacherRatingScales,Parentversion. Data-analyses by means of the Wilcoxon signed rank test showed that, according to the parents, the children’s overall behaviour significantly improved after the treatment-period. The effect size d was large: .81 (see Table 2 for means, standard deviations, and the Wilcoxon signed rank test). More specifically, according to the parents the children improved significantly on all subscales, with moderate to large effect sizes d ranging from .25 (subscale Anxiety) to 1.14 (subscale Impulsive/Hyperactive). After the treatment-free period of 6 weeks, the observed improvements remained level. For means, standard deviations, and the Wilcoxon signed rank test, see Table 2.

TheRevisedConnersParentandTeacherRatingScales,Teacherversion. Similar to the parents’ version, the teachers also found that the overall behaviour of the children improved significantly after the treatment period. However, the effect size d was moderate: .37. It is noteworthy that after the stimulation was ended the children’s overall behaviour further improved during the treatment free period, with a somewhat larger effect size d of .51. With respect to the various subscales, significant improvements were observed for the subscales Learning Problems, Impulsive/Hyperactive, and Conduct Problems II, with

Chapter five

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small to moderate effect sizes d of .23, .52, and .28, respectively. The scores on these three subscales did not change significantly after the treatment-free period (for means, standard deviations, and the Wilcoxon signed rank test, see Table 2).

Rest-activity rhythm

As Table 3 shows, the scores on the actigraphy variable L5 significantly declined after the treatment period of 6 weeks. Although the M10 variable also declined, it did not reach statistical significance. The effect sizes d were .92 (large) and .66 (moderate), respectively (for means, standard deviations, and the Wilcoxon signed rank test, see Table 3). No treatment effects were observed with respect to IS, IV, and RA. Of note is that the score on L5 showed a significant increase after the 6 weeks period without treatment

per domain: cognition, behavior, and the rest-activityrhythm.

Cognition

The preliminary results indicate a positive effect ofTENS on cognitive functioning, though the strength ofthe effect varies from small to moderate (d .19 to d .61).By comparison, a recent study61 found minimal im-provement inneuropsychological functioning followingmethylphenidate treatment in children with ADHD.Thefinding that theperformanceon themajorityof thetests did not continue to improve significantly duringthe treatment-free period indicates a real treatmenteffect rather than a test-retest effect. Thepositiveeffectof TENS on the Stroop interference performance sup-ports its effect on executive control functions and more

specifically on the prefrontal cortex and the anteriorcingulate cortex.62

One explanation for these findings might be as fol-lows. Han63 showed that high-frequency bursts of elec-trical nerve stimulation as was applied in the presentstudy facilitate the secretion of BDNF. BDNF is crucialfor normal development and plasticity of the brain.64

Behavior

According to the parents who filled in the RevisedConners Parent and Teacher Rating Scales, the childrenshoweda strong improvement in all aspects of behaviorafter TENS treatment. The greatest improvement wasobserved in impulsivity and hyperactivity (subscaleImpulsive/Hyperactive), whereas anxiety decreased theleast. The child’s behavior did not change remarkably

6 Neurorehabilitation and Neural Repair XX(X); 2004

S. Jonsdottir et al.

Table2. Means, StandardDeviations, and theWilcoxonSignedRanks Tests (Z Scores, PValues)withRespect to theScores on theRevised Conners Parents & Teacher Rating Scale (Conners), Administered to the Parents and the Teachers, before and after theTreatment Period of 6 Weeks and after a Treatment-Free Period of 6 Weeks


Conners M SD M SD M SD Z P Z P

Parents’ versionTotal score 52.52 18.44 39.10 17.63 38.74 16.25 3.22 0.0005 0.15 0.88Conduct problems I 11.76 4.89 9.20 4.69 8.79 5.13 2.46 0.007 0.06 0.95Learning problems 7.38 1.80 6.05 2.24 6.37 2.50 2.14 0.02 0.09 0.93Psychosomatic problems 1.71 1.59 1.05 1.32 0.84 1.07 2.16 0.02 0.70 0.48Impulsive/hyperactive 7.33 2.01 4.90 2.49 4.84 1.83 3.07 0.001 0.11 0.91Conduct problems II 2.52 1.94 1.90 1.68 1.79 1.47 2.28 0.01 0.32 0.75Anxiety 3.10 2.57 2.50 2.24 2.47 1.95 1.82 0.03 0.66 0.51Other items 19.19 8.95 13.60 8.36 13.11 7.28 3.30 0.0005 0.04 0.97

Teachers’ versionTotal score 42.40 18.84 35.75 14.83 26.62 7.90 1.92 0.03 2.29 0.01Conduct problems I 11.15 5.50 9.00 4.49 6.85 3.69 1.54 0.06 1.96 0.03Learning problems 6.40 2.78 5.94 2.68 4.62 1.80 1.38 0.08 1.63 0.10Psychosomatic problems 0.88 1.36 0.47 0.64 0.46 1.21 0.94 0.18 0.58 0.56Impulsive/hyperactive 6.50 3.15 5.18 2.74 4.08 1.44 1.32 0.09 0.53 0.59Conduct problems II 1.85 1.35 1.35 1.50 1.46 1.27 1.78 0.04 0.81 0.42Anxiety 2.20 1.85 2.76 2.80 1.38 1.66 0.24 0.41 0.11 0.92Other items 13.50 7.49 12.35 7.32 7.85 3.87 1.08 0.28 2.19 0.01

Table 3. Means, Standard Deviations, and theWilcoxon Signed Ranks Tests (Z Scores, P Values)with Respect to theActigraphy-Variables, Obtained before and after the Treatment Period of 6 Weeks and after a Treatment-Free Period of 6 Weeks


Actigraphy M SD M SD M SD Z P Z P

Interdaily stability 0.69 0.09 0.62 0.13 0.61 0.15 1.29 0.20 0.47 0.64Intradaily variability 0.62 0.16 0.70 0.25 0.64 0.14 1.29 0.47 0.91 0.36Relative amplitude 0.96 0.01 0.97 0.01 0.95 0.04 0.40 0.35 1.41 0.08L5 801 277 595 303 1354 1751 2.07 0.02 1.66 0.05M10 45810 15473 37967 21187 44478 20639 1.45 0.07 0.73 0.47

L5 = 5 least active hours; M10 = 10 most active hours.

per domain: cognition, behavior, and the rest-activityrhythm.

Cognition

The preliminary results indicate a positive effect ofTENS on cognitive functioning, though the strength ofthe effect varies from small to moderate (d .19 to d .61).By comparison, a recent study61 found minimal im-provement inneuropsychological functioning followingmethylphenidate treatment in children with ADHD.Thefinding that theperformanceon themajorityof thetests did not continue to improve significantly duringthe treatment-free period indicates a real treatmenteffect rather than a test-retest effect. Thepositiveeffectof TENS on the Stroop interference performance sup-ports its effect on executive control functions and more

specifically on the prefrontal cortex and the anteriorcingulate cortex.62

One explanation for these findings might be as fol-lows. Han63 showed that high-frequency bursts of elec-trical nerve stimulation as was applied in the presentstudy facilitate the secretion of BDNF. BDNF is crucialfor normal development and plasticity of the brain.64

Behavior

According to the parents who filled in the RevisedConners Parent and Teacher Rating Scales, the childrenshoweda strong improvement in all aspects of behaviorafter TENS treatment. The greatest improvement wasobserved in impulsivity and hyperactivity (subscaleImpulsive/Hyperactive), whereas anxiety decreased theleast. The child’s behavior did not change remarkably

6 Neurorehabilitation and Neural Repair XX(X); 2004

S. Jonsdottir et al.

Table2. Means, StandardDeviations, and theWilcoxonSignedRanks Tests (Z Scores, PValues)withRespect to theScores on theRevised Conners Parents & Teacher Rating Scale (Conners), Administered to the Parents and the Teachers, before and after theTreatment Period of 6 Weeks and after a Treatment-Free Period of 6 Weeks


Conners M SD M SD M SD Z P Z P

Parents’ versionTotal score 52.52 18.44 39.10 17.63 38.74 16.25 3.22 0.0005 0.15 0.88Conduct problems I 11.76 4.89 9.20 4.69 8.79 5.13 2.46 0.007 0.06 0.95Learning problems 7.38 1.80 6.05 2.24 6.37 2.50 2.14 0.02 0.09 0.93Psychosomatic problems 1.71 1.59 1.05 1.32 0.84 1.07 2.16 0.02 0.70 0.48Impulsive/hyperactive 7.33 2.01 4.90 2.49 4.84 1.83 3.07 0.001 0.11 0.91Conduct problems II 2.52 1.94 1.90 1.68 1.79 1.47 2.28 0.01 0.32 0.75Anxiety 3.10 2.57 2.50 2.24 2.47 1.95 1.82 0.03 0.66 0.51Other items 19.19 8.95 13.60 8.36 13.11 7.28 3.30 0.0005 0.04 0.97

Teachers’ versionTotal score 42.40 18.84 35.75 14.83 26.62 7.90 1.92 0.03 2.29 0.01Conduct problems I 11.15 5.50 9.00 4.49 6.85 3.69 1.54 0.06 1.96 0.03Learning problems 6.40 2.78 5.94 2.68 4.62 1.80 1.38 0.08 1.63 0.10Psychosomatic problems 0.88 1.36 0.47 0.64 0.46 1.21 0.94 0.18 0.58 0.56Impulsive/hyperactive 6.50 3.15 5.18 2.74 4.08 1.44 1.32 0.09 0.53 0.59Conduct problems II 1.85 1.35 1.35 1.50 1.46 1.27 1.78 0.04 0.81 0.42Anxiety 2.20 1.85 2.76 2.80 1.38 1.66 0.24 0.41 0.11 0.92Other items 13.50 7.49 12.35 7.32 7.85 3.87 1.08 0.28 2.19 0.01

Table 3. Means, Standard Deviations, and theWilcoxon Signed Ranks Tests (Z Scores, P Values)with Respect to theActigraphy-Variables, Obtained before and after the Treatment Period of 6 Weeks and after a Treatment-Free Period of 6 Weeks


Actigraphy M SD M SD M SD Z P Z P

Interdaily stability 0.69 0.09 0.62 0.13 0.61 0.15 1.29 0.20 0.47 0.64Intradaily variability 0.62 0.16 0.70 0.25 0.64 0.14 1.29 0.47 0.91 0.36Relative amplitude 0.96 0.01 0.97 0.01 0.95 0.04 0.40 0.35 1.41 0.08L5 801 277 595 303 1354 1751 2.07 0.02 1.66 0.05M10 45810 15473 37967 21187 44478 20639 1.45 0.07 0.73 0.47

L5 = 5 least active hours; M10 = 10 most active hours.


�1

(moderate effect size d of .60). The increase in scores on M10 after the treatment-free period was not significant (for means, standard deviations, and the Wilcoxon signed rank test, see Table 3).

DISCUSSION

The goal of the present pilot study was to examine whether TENS, a nonpharmacological central nervous system stimulant, could have a beneficial influence on cognition, behaviour, and the rest-activity rhythm of children with ADHD. The results will be discussed per domain: cognition, behaviour, and the rest-activity rhythm.

Cognition

The preliminary results indicate a positive effect of TENS on cognitive functioning, though the strength of the effect varies from small to moderate (d= .19 to d= .61). By comparison, a recent study (Yang et al., 2004) found minimal improvement in neuropsychological functioning following methylphenidate treatment in children with ADHD. The finding that the performance on the majority of the tests did not continue to improve significantly during the treatment-free period indicates a real treatment effect rather than a test-retest effect. The positive effect of TENS on the Stroop interference performance supports its effect on executive control functions and more specifically on the prefrontal cortex and the anterior cingulate cortex (Markela-Lerenc et al., 2004).

One explanation for these findings might be as follows. Han (2003) showed that high-frequency bursts of electrical nerve stimulation as was applied in the present study, facilitate the secretion of BDNF. BDNF is crucial for normal development and plasticity of the brain (Webster et al., 2002).

Behaviour

According to the parents who filled in the Revised Conners Parent and Teacher Rating Scales, the children showed a strong improvement in all aspects of behaviour after TENS-treatment. The greatest improvement was observed in impulsivity and hyperactivity (subscale Impulsive/Hyperactive), whereas anxiety decreased the least. The children’s behaviour did not change remarkably after cessation of treatment. Although significant, the opinion of the teachers on the overall children’s behaviour was less pronounced in comparison with the parents’. It is remarkable that the strongest effect was again observed with respect to hyperactivity and impulsivity (subscale Impulsive/Hyperactive), suggesting that TENS, similar to stimulant medication (Levy & Swanson, 2001), might restore the children’s inhibitory capacity by stimulating the prefrontal cortex. Another interesting finding is that overall behaviour, as evaluated by the teachers, further improved significantly during the treatment-free period, with a moderate effect-size d of .51. One possible explanation might be that a positive development in behaviour may

Chapter five

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further increase or be more easily noticed only in a highly structured environment such as school.

Rest-activity rhythm

Although no significant changes were observed with respect to the rest-activity variables IS, IV, and RA after the treatment period of 6 weeks, both L5 and M10 showed decreases, effects with a large and moderate effect size, respectively. The finding that after the treatment-free period L5 significantly increased and M10 increased to a somewhat lesser extent, supports a real treatment effect of TENS. L5 represents the 5 least active hours, which most probably represent the hours at nighttime. In contrast, M10 implies the 10 most active hours, which will probably take place during the day. Similar to the effects of TENS on cognition and behaviour, the finding that both L5 and M10 decreased by TENS supports the rationale that TENS enhances inhibition mediated by the prefrontal cortex. One explanation might be that TENS has a modulatory effect on the SCN. It has been proposed that dysfunction of the SCN may be contributing to many of the symptoms seen in ADHD (Sylvester et al., 2002). The neurotrophin BDNF, which is an important rhythmic output from the SCN circadian clock (Allen et al., 2004), has been found to be involved in sleep regulation (Kushikata et al., 1999; Sei et al., 2000; Sei et al., 2003; Taishi, et al., 2001). It might be speculated that the effect of TENS treatment on sleeping patterns both in AD and ADHD might possibly be the result of increased BDNF, which in turn has a beneficial effect on sleep.

The positive effect of TENS on L5 and M10 in ADHD could be of particular clinical relevance in that ADHD is characterized by nightly restlessness and hyperactivity during the day. Although stimulant medication therapy has been shown to decrease awake activity rates in children with ADHD (Butte et al., 1999), a recent study found that stimulant medication did not seem to affect sleeping patterns in ADHD children (Ring et al., 1998).

Limitations

A first limitation of the present study was that the investigator who administered the neuropsychological tests and the parents/teachers who filled in the Revised Conners Parents and Teacher Rating Scales were not blind with respect to the study design. On the other hand, both the parents’ and teachers’ ratings would probably have been very critical because the extent of the parents’ and teachers’ burden is directly related to the effectiveness of the treatment. In other words, both parents and teachers have nothing to gain by reporting positive results that are not realistic. The only real objective measurement in the present study concerned the assessment of the rest-activity rhythm by actigraphy. A second limitation of the present study is the lack of a control group. For ethical reasons, that is, the children who participate have to stop their medication, we first wanted to do a pilot study to examine whether TENS could have a positive effect in


�3

children with ADHD. A third limitation is that we did not apply a Bonferroni correction to the significance level of 0.05 to control for multiple tests.

Considering the encouraging effects of TENS on cognition, behaviour, and the rest-activity rhythm in children with ADHD in the present study, it is justified to do a next study with a more rigorous design, including a control group.

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CHAPTER SIX 6Summary and concluding remarks

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Summary and concluding remarks

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SUMMARY AND CONCLUDING REMARKS

Attention deficit hyperactivity disorder (ADHD) is a neurodevelopmental disorder affecting a large number of children and adolescents in all parts of the world (Faraone et al., 2003). Approximately half of those referred to child and adolescent psychiatric clinics are diagnosed with ADHD. There are still many questions unresolved with respect to comorbidity with other disorders, gender differences, neuropsychological deficits, methods of assessment, and treatment of the disorder.

The main aim of the present thesis was to expand on existing knowledge by examining the following:

a) Gender differences in ADHD symptoms in a normal Icelandic population.b) The impact of associated specific language impairment (SLI) on working memory

in children with combined subtype of ADHD.c) The relationships between behavioural and neuropsychological assessments of

ADHD symptoms.d) The effects of peripheral electrical nerve stimulation on cognition, behaviour

and the rest-activity rhythm in children with ADHD combined subtype.

Chapter 2. Most previous studies in western cultures have shown that boys are more likely than girls to develop ADHD, but gender differences have been shown to differ with respect to cultures examined (Brewis & Schmidt, 2003; Pineda et al., 1999). Our study examined the gender differences in ADHD symptoms in a sample of normal Icelandic children. The results show that Icelandic parents and teachers rate boys significantly higher than girls on hyperactivity/impulsivity symptoms and on aggression symptoms. Teachers also rate boys higher than girls on inattention symptoms but parents do not. Furthermore, externalizing problems best predicted hyperactivity/impulsivity symptoms and internalizing problems and learning problems best predicted inattention symptoms in both boys and girls. Interestingly there was a significant correlation between parents’ and teachers’ ratings of ADHD symptoms in boys, but not in girls. It is argued that more externalizing behaviours of boys in general, may be inflating their ratings of ADHD symptoms, especially among teachers. The indication of poor concordance rate between parents and teachers in their reports of ADHD symptoms in girls may be of clinical relevance since it may cause under-identification of girls with ADHD.

Chapter 3. Some researchers have theorized that deficient working memory is a specific feature of ADHD. The core problem in another developmental disorder, named specific language impairment (SLI), has been shown to be deficient verbal working memory. SLI is a common comorbidity in ADHD and conversely, ADHD occurs frequently in SLI. This study examined to what extent comorbid SLI in children with ADHD combined subtype (ADHD-C), affects their working memory. The results show that children with ADHD-C and comorbid SLI scored significantly lower than those without SLI and normal children, on verbal working memory measures. Children with ADHD were found to score normally

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on spatial working memory measures. It is concluded that working memory deficits are not a specific characteristic of ADHD but are associated with language impairments. The results of the study show the importance of screening for language disorders in studies on neuropsychological deficits in ADHD.

Chapter 4. Most recent neuropsychological theories of ADHD have stated that deficient executive functions (EFs) are the main characteristic of the disorder. Previous studies, however, have shown a poor relationship between EFs tests believed to be sensitive to ADHD symptoms and behavioural ratings of the same symptoms. This relationship was examined in a clinical group of 7-11 year old children, most of whom had been diagnosed with ADHD. Different aspects of EFs were studied. In addition IQ and language ability were assessed. The results show that the relationships between tests of EFs and ratings of ADHD symptoms were generally low and non-significant. When controlling for intelligence, EF tasks were significantly related to ratings of autistic symptomatology and depression, rather than to symptoms of inattention and hyperactivity. It is noteworthy, that the measure that best predicted teacher ratings of inattention was a test of language ability, but not tests of EF. It is concluded that the results of the study do not support the EF theory of ADHD and that they emphasize the importance of screening for language impairment in the diagnostic process of ADHD.

Chapter 5. In this chapter, data on the effects of TENS treatment on cognition, behaviour and the rest-activity rhythm in children with ADHD are presented. The results show that TENS treatment appeared to have a moderate beneficial influence on cognitive functions that load especially on EF. There was also improvement in behaviour as measured by parent/teacher rating scales. Interestingly also motor activity, as measured with actigraphy, decreased with TENS, both during the day and the night.

Taken together, the main diagnostic symptoms of ADHD are inattention and hyperactivity/impulsivity. However, this thesis has shown important effects of comorbidity and gender in ADHD on cognition (Chapters 3, 4, and 5) and on behaviour (Chapter 2). That is, in Chapter 2 we show that normal Icelandic boys are rated higher than normal girls on hyperactivity and aggression symptoms both according to parents and teachers. The implication of this finding might be that boys are normally more aggressive and externalizing in their behaviour than girls, and therefore are being referred more often for diagnosis. Alternatively, there may possibly be a rater bias. The study also showed that teachers rate boys higher than girls on inattention symptoms, but parents do not. The explanation for this might be that inattention symptoms are highly related to learning problems for which teachers are more sensitive to than parents. The more externalizing behaviour of boys than girls might explain why teachers are more observant of their inattention (learning) problems and therefore rate them to a higher degree. More observable behaviour of boys might also explain why there is more agreement between parents and teachers on ratings of ADHD symptoms with respect to them than to girls.


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Recent studies have shown that teachers may be over-identifying children with ADHD and that environmental factors like class size and culture may influence teachers’ perceptions about which students have the disorder (Havey et al., 2005). In our study it was generally the mothers that rated the children’s behaviour and all the teachers rating behaviour were female. Studies have shown that ADHD children show greater obedience to their fathers and to male teachers than to their mothers and female teachers (Barkley, 1998). It would be of great interest in future studies to examine if gender differences in ADHD symptoms would be different if behaviour was rated by fathers and male teachers.

The role of language impairment, which is not generally screened for, is highly underestimated in assessment of ADHD. It has been theorized that the EF of working memory is one of the core problems in ADHD. The study in Chapter 3 shows that working memory deficits are caused by comorbid language impairment. The results of the study in Chapter 4 show that language problems best predicted teacher ratings of inattention. Possibly, several diagnostic criteria for ADHD according to DSM-IV, especially for inattention symptoms, might in fact be explained by language comprehension problems. Examples of these diagnostic criteria are: “Often does not seem to listen when spoken to directly; often does not follow through on instructions and fails to finish schoolwork, chores, or duties in the workplace”. Conversational skills, like taking turns and maintaining a topic, can be impaired both in ADHD and SLI. Impairments in language comprehension can be subtle and often do not appear except on formal assessment. Comorbid language impairment in ADHD may explain why stimulant treatment, the most frequently used therapy for ADHD, does not improve academic achievement or social skills (Bennett et al., 1999; Chronis et al., 2006). It has been suggested that the inattentive type of ADHD and the combined type are actually separate and unique childhood psychiatric disorders (Barkley, 1998; Bauermeister et al., 2005). Children with the inattentive type have been shown to have a later onset of inattention symptoms, have more sluggish cognitive tempo, appear to be less prone to initiate social interactions and are less likely to have externalizing behaviours than children with the combined type (Bauermeister et al., 2005). The results of the studies in this thesis raise the question if the inattention symptoms in ADHD are in fact caused by structural language problems. Further research is needed to confirm this hypothesis. In Chapter 5 it is shown that TENS treatment had a beneficial effect on neurobehavioral functioning in children with ADHD. The significantly less nocturnal restlessness is an especially intriguing finding considering the frequent reports of sleep disturbances in ADHD (e.g. Barkley, 1998). Children with ADHD have been shown to have higher levels of nocturnal activity, have increased rapid eye movement (REM) sleep latency and decreased REM sleep percentages than control children (Bullock & Schall, 2005; Konofal et al., 2001; Sangal et al., 2005). Studies have suggested that REM sleep may have a beneficial effect on consolidation of cognitive skills and that it is associated with increased BDNF (brain derived neurotrophic factor) level in the dorsal hippocampus (Ulloor & Datta, 2005). It has been hypothesized that BDNF is involved in the pathogenesis of ADHD (Kent et al. 2005; Tsai, 2003). Studies have shown that disrupted sleep can affect daytime learning and attention in childhood and lead to ADHD

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symptoms. It has been suggested that disrupted sleep architecture can cause executive dysfunction, impaired vigilance, depression, anxiety and hyperactivity (El-Ad & Lavie, 2005; O’Brien et al., 2004; Sadeh et al., 2002). Our findings of decreased nocturnal movement with TENS therapy might indicate that the children are spending more time in REM sleep, during which there is no muscle movement. Previous studies have shown that REM sleep is associated with the secretion of neurotrophic factors and may thus for example contribute to memory functions. The results of our study possibly indicate that TENS treatment may have an effect on sleep efficiency in children with ADHD with beneficial effects on neurobehavioral functioning. This finding may also be of clinical importance considering reports of increased sleep disturbance in ADHD children treated with methylphenidate (Schwartz et al., 2004).

In sum, the studies reported in this thesis provide evidence that gender differences, EF deficits and symptoms of inattention in ADHD are mainly related to comorbid factors. Gender differences in diagnostic rates of ADHD may be explained by boys being normally more aggressive and externalizing in their behaviour than girls and therefore being referred in greater number than girls for ADHD. Poorer interrater agreement between parents and teachers with respect to ADHD symptoms in girls than in boys might also be a factor. According to DSM-IV diagnostic criteria, some impairment from ADHD symptoms have to be present in two or more settings. If there is less agreement between parents and teachers in their assessment of girls’ behaviour, it may be less likely that they reach diagnostic criteria than boys do. Deficits in the EF of working memory were shown to be more related to language impairment than to ADHD. Deficits in the EF of planning were shown to be more associated with symptoms of autism and depression than with symptoms of ADHD. Language impairment was shown to be the best predictor of teacher ratings of inattention. Some ADHD symptoms may be caused by comorbid sleep disturbance and may improve with TENS treatment.

It is the main conclusion of this thesis, that it is essential for the assessment of ADHD to screen for comorbidity, so that functional deficits in both academic achievement and social skills can be treated more appropriately.

The following recommendations with respect to future studies can be made as a conclusion of this thesis:

1. Examine the concordance between parent and teacher ratings of ADHD symptoms in girls by using larger samples.

2. Compare ADHD ratings of fathers and male teachers to ratings of mothers and female teachers.

3. Study the association between language impairment and symptoms of inattention in children with ADHD.


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4. Study further the association between executive dysfunction and symptoms of autism and depression in children with ADHD.

5. Study further the effects of TENS treatment on children with ADHD by using larger samples and control groups.

6. Compare the sleep architecture in children with ADHD treated with stimulant drugs as opposed to TENS.

7. Study the influence of sleep disturbances on ADHD symptoms and associated disorders.

8. Study the relationship between the sleep-wake rhythm and executive function in children.

9. Study the effects of TENS therapy on children with sleep disturbances.10. Study the effects of TENS on the executive function of planning in children.11. Study the effects of TENS therapy on REM sleep in children and adults.12. Study the effects of TENS therapy on restless legs syndrome/periodic leg movement

disorder.13. Study the effects of TENS therapy on the noradrenergic, serotonergic, dopaminergic,

and other neurotransmitter systems using neuroimaging tools such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) scans.

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REFERENCES



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Havey, J.M., Olson, J.M., McCormick, C., & Cates, G.L. (2005). Teachers’ perceptions of the incidence and management of attention-deficit hyperactivity disorder. AppliedNeuropsychology,12, 120-127.

Kent, L., Green, E., Hawi, Z., Kirley, A., Dudbridge, F., Lowe, N., Raybould, R., Langley, K., Bray, N., Fitzgerald, M., Owen, M.J., O’Donovan, M.C., Gill, M., Thapar, A., & Craddock, N. (2005). Association of the paternally transmitted copy of common Valine allele of the Val66Met polymorphism of the brain-derived neurotrophic factor (BDNF) gene with susceptibility to ADHD.MolecularPsychiatry,10,939-943.

Konofal, E., Lecendreux, M., Bouvard, M.P., & Mouren-Simeoni, M.C. (2001). High levels of nocturnal activity in children with attention-deficit hyperactivity disorder: A video analysis. PsychiatryandClinicalNeurosciences,55, 97-103.

Montgomery, J.W. (2003). Working memory and comprehension in children with specific language impairment: What we know so far. JournalofCommunicationDisorders,36,221-231.

O’Brien, L.M., Mervis, C.B., Holbrook, C.R., Bruner, J.L., Smith, N.H., McNally, N., McClimment, M.C., & Gozal, D. (2004). Neurobehavioral correlates of sleep-disordered breathing in children. JournalofSleepResearch,13, 165-172.

Pelham, W.E.Jr., Fabiano, G.A., & Massetti, G.M. (2005). Evidence-based assessment of attention deficit hyperactivity disorder in children and adolescents. JournalofClinicalChildandAdolescentPsychology,34, 449-476.


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Pineda, D., Ardila, A., Rosselli, M., Arias, B.E., Henao, G.C., Gomez, L.F., Mejia, S.E., & Miranda, M.L. (1999). Prevalence of attention-deficit/hyperactivity disorder symptoms in 4- to 17-year-old children in the general population. Journal ofAbnormalPsychology,27,455-462.

Sangal, R.B., Owens, J.A., Sangal, J. (2005). Patients with attention-deficit/hyperactivity disorder without observed apneic episodes in sleep or daytime sleepiness have normal sleep on polysomnography. Sleep,28, 1143-1148.

Schwartz, G., Amor, L.B., Grizenko, N., Lageix, P., Baron, C., Boivin, D.B., & Joober, R. (2004). Actigraphic monitoring during sleep of children with ADHD on methylphenidate and placebo. Journal of the American Academy of Child andAdolescentPsychiatry,43,1276-1282.

Tsai, S.J. (2003). Attention-deficit hyperactivity disorder and brain-derived neurotrophic factor: A speculative hypothesis. MedicalHypotheses,60, 849-851.

Ulloor, J., & Datta, S. (2005). Spatio-temporal activation of cyclic AMP response element-binding protein, activity-regulated cytoskeletal-associated protein and brain-derived nerve growth factor: A mechanism for pontine-wave generator activation-dependent two-way active-avoidance memory processing in the rat. Journal ofNeurochemistry,95, 418-428.

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Samenvatting

Dutch translation by Erik J.A. Scherder

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SAMENVATTING EN CONCLUSIES

Attention deficit hyperactivity disorder (ADHD) is een ontwikkelingsstoornis die voorkomt bij een groot aantal kinderen en volwassenen over de gehele wereld (Faraone et al., 2003). Bij ongeveer de helft van de mensen die worden verwezen naar psychiatrische klinieken voor kinderen en volwassenen wordt de diagnose ADHD vastgesteld. Vele vragen met betrekking tot comorbiditeit met andere stoornissen, geslachtsverschillen, neuropsychologische stoornissen, en de methoden van diagnostiek en behandeling van ADHD zijn echter nog onbeantwoord.

Het hoofddoel van het huidige proefschrift was om een bijdrage te leveren aan de bestaande kennis door het volgende te onderzoeken:

a) Geslachtsverschillen in ADHD symptomen binnen een normale IJslandse populatie.

b) De invloed van gerelateerde specifieke taalstoornissen op het werkgeheugen van kinderen met ADHD Combined Type.

c) De relaties tussen gedrags- en neuropsychologische diagnostiek van ADHD symptomen.

d) De effecten van perifere elektrische zenuwstimulatie op cognitie, gedrag en het rust-activiteitsritme van kinderen met ADHD Combined type.

Hoofdstuk 2. De meeste studies in de Westerse cultuur hebben tot nu toe aangetoond dat jongens een grotere kans hebben ADHD te ontwikkelen dan meisjes maar geslachtsverschillen lijken samen te hangen met de verschillen tussen de diverse culturen (Brewis & Schmidt, 2003; Pineda et al., 1999). Onze studie onderzocht de geslachtsverschillen in ADHD symptomen in een steekproef van normale kinderen in IJsland. De resultaten tonen aan dat volgens de ouders en leerkrachten in IJsland bij jongens meer symptomen van hyperactiviteit/impulsiviteit en agressie voorkomen dan bij meisjes. In tegenstelling tot de ouders, stellen leerkrachten ook meer aandachtsstoornissen vast bij jongens dan bij meisjes. Vervolgens, blijken ‘externalizing’ problemen het beste hyperactiviteit/impulsiviteit te voorspellen en ‘internalizing’ problemen en leerproblemen het beste aandachtsstoornissen te voorspellen bij zowel jongens als meisjes. Interessant is dat alleen bij de jongens de beoordeling van de ADHD symptomen door de ouders en de leerkrachten een significante correlatie vertoonde. Verondersteld wordt dat het ‘externalizing’ gedrag van de jongens de beoordeling van de ADHD symptomen beïnvloed, vooral bij leerkrachten. De bevinding dat de beoordelingen van de ouders en de leerkrachten wat betreft ADHD symptomen bij meisjes minder goed overeenkomen kan klinisch relevant zijn; het kan de oorzaak zijn van het feit dat minder meisjes dan jongens de diagnose ADHD krijgen.

Hoofdstuk 3. Sommige onderzoekers beweren dat een verminderd functioneren van het werkgeheugen een specifiek kenmerk is van ADHD. Het kernprobleem van een andere ontwikkelingsstoornis, genaamd ‘specific language impairment (SLI)’,

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blijkt een verminderd verbaal werkgeheugen te zijn. SLI is een comorbiditeit die veel voorkomt bij ADHD en, omgekeerd, ADHD komt frequent voor bij SLI. Deze studie onderzocht in welke mate SLI bij kinderen met ADHD Combined type (ADHD-C) het werkgeheugen beïnvloedt. De resultaten tonen aan dat kinderen mét ADHD-C en SLI significant lager scoren op verbale werkgeheugen taken dan kinderen zonder SLI en normale kinderen. Kinderen met ADHD scoorden normaal op taken die een beroep doen op het spatiëel werkgeheugen. Geconcludeerd wordt dat het verminderd functioneren van het werkgeheugen niet een specifiek kenmerk is van ADHD maar gerelateerd is aan taalstoornissen. De resultaten van deze studie onderstrepen het belang van het beoordelen van de taalvaardigheden in studies die gericht zijn op neuropsychologische stoornissen in ADHD.

Hoofdstuk 4. De meest recente neuropsychologische theorieën betreffende ADHD stellen dat een vermindering in executieve functies (EF) het meest kenmerkend is voor deze aandoening. Eerdere studies, echter, hebben een zwakke relatie aangetoond tussen testen voor EF en gedrag die verondersteld worden gevoelig te zijn voor dezelfde ADHD symptomen. Deze relatie werd onderzocht in een klinische groep kinderen in de leeftijd van 7 tot 11 jaar, van wie de meeste de diagnose ADHD hadden. Er werden verschillende aspecten van EF onderzocht. Bovendien werden IQ en taalvaardigheid in de studie betrokken. De resultaten tonen aan dat de relatie tussen testen voor EF en ADHD symptomen in het algemeen laag was en niet significant. Indien er gecontroleerd werd voor IQ, bleken de scores op EF taken significant gecorreleerd te zijn met autistische en depressieve symptomen en niet met symptomen van verminderde aandacht en hyperactiviteit. Een opmerkelijke bevinding was dat de test die het beste de beoordeling door de leerkracht van verminderde aandacht voorspelde, een test voor taalvaardigheid was en niet de tests voor EF. Geconcludeerd wordt dat de resultaten van deze studie niet de ‘EF-theorie van ADHD’ ondersteunen.

Hoofdstuk 5. In dit hoofdstuk, worden de resultaten gepresenteerd van een studie naar de effecten van TENS op cognitie, gedrag, en het rust-activiteitsritme van kinderen met ADHD. De resultaten tonen aan dat een behandeling met TENS een matig gunstig effect heeft op cognitieve functies die vooral een beroep doen op EF. Aan de hand van ouders/leerkrachten vragenlijsten werd ook een verbetering in gedrag vastgesteld. Een opvallende bevinding is dat ook motorische activiteit overdag en ‘s nachts, gemeten met behulp van actigrafie, afnam door TENS.

Samengevat, de hoofdsymptomen van ADHD zijn verminderde aandacht en hyperactiviteit/impulsiviteit. Dit proefschrift heeft echter belangrijke effecten van comorbiditeit en geslacht op het cognitief functioneren (Hoofdstukken 3, 4, en 5) en op het gedrag (Hoofdstuk 2) van kinderen met ADHD aangetoond. Dat wil zeggen dat we in Hoofdstuk 2 aangetoond hebben dat volgens ouders en leerkrachten normale IJslandse jongens hoger scoren op hyperactiviteit en agressie dan normale IJslandse meisjes. De

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implicatie van deze bevinding is dat jongens normaal gesproken meer agressief en ‘externalizing’ zijn in hun gedrag dan meisjes en om die reden vaker worden verwezen voor nadere diagnostiek. Een alternatieve verklaring is dat er sprake kan zijn van een ‘beoordelaar’s bias’. De studie toonde namelijk aan dat, in tegenstelling tot de ouders, de leerkrachten symptomen van verminderde aandacht vooral toedichten aan jongens. De verklaring hiervoor kan zijn dat symptomen van verminderde aandacht sterk gerelateerd zijn aan leerproblemen waarvoor leerkrachten meer gevoelig zijn dan ouders. Door het meer ‘externalizing’ gedrag van jongens, in vergelijking met meisjes, vallen de problemen in aandacht (en leren) van de jongens eerder op bij de leerkrachten. Juist bij jongens is het gedrag meer observeerbaar wat een verklaring kan zijn voor de grotere overeenkomst tussen ouders en leerkrachten als het gaat om de beoordeling van ADHD symptomen bij jongens dan bij meisjes.

Recente studies hebben aangetoond dat leerkrachten kinderen met ADHD bovenidentificeren, onder invloed van omgevingsfactoren zoals de grootte van de klas en de cultuur (Havey et al., 2005). In onze studie, waren het vooral de moeders die het gedrag van de kinderen beoordeelden en de leerkrachten waren vrouwen. Studies hebben aangetoond dat ADHD kinderen zijn meer gehoorzaam aan hun vaders en aan mannelijke leerkrachten (Barkley, 1998). Het zou zeer interessant zijn om in toekomstige studies te onderzoeken of geslachtsverschillen in ADHD symptomen afhankelijk zijn van het geslacht van de beoordelaars.

De rol van een taalstoornis, waarvoor in het algemeen niet gecontroleerd wordt, wordt sterk onderschat in de diagnostiek van ADHD. Verondersteld wordt dat een vermindering in werkgeheugen een van de kernproblemen van ADHD is. De studie in Hoofdstuk 3 toont aan dat een vermindering in werkgeheugen veroorzaakt wordt door een stoornis in taalvaardigheid. De resultaten in de studie van Hoofdstuk 4 tonen aan dat taalproblemen de beste voorspeller zijn voor de beoordeling van verminderde aandacht door de leerkracht. Mogelijk worden enkele DSM-IV diagnostische criteria voor ADHD, in ’t bijzonder voor verminderde aandacht, verklaard door problemen met taalbegrip. Voorbeelden van deze diagnostische criteria zijn: “Luistert dikwijls niet als men direct wordt aangesproken”; “Volgt dikwijls geen instructies op, kan het huiswerk niet afmaken, of verplichtingen op de werkvloer niet nakomen”. Gespreksvaardigheden zoals het initiatief nemen in een gesprek of bij het onderwerp van het gesprek blijven, kunnen verminderd zijn bij ADHD en SLI. Een achteruitgang in taalbegrip kan subtiel zijn en pas naar voren komen bij formele diagnostiek. Een taalstoornis bij ADHD kan verklaren waarom een behandeling met een stimulant, de meest toegepaste vorm van behandeling bij ADHD, geen gunstig effect heeft op academische vorming en sociale vaardigheden (Bennett et al., 1999; Chronis et al., 2006). Er wordt verondersteld dat het ‘Inattentive type’ en het ‘Combined type’ van ADHD in werkelijkheid twee afzonderlijke en unieke psychiatrische stoornissen zijn die voorkomen in de kinderjaren (Barkley, 1998; Bauermeister et al., 2005). Kinderen met het ‘Inattentive type’ tonen pas op latere leeftijd een vermindering in aandacht, hebben een traag cognitief tempo, zijn minder geneigd tot het maken van sociale contacten en hebben minder kans op ‘externalizing’ gedrag dan kinderen met het ‘Combined type’

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(Bauermeister et al., 2005). De resultaten van de studies in dit proefschrift roepen de vraag op of stoornissen in aandacht in ADHD niet veroorzaakt worden door structurele taalproblemen. Nader onderzoek is noodzakelijk om deze hypothese te bevestigen. In Hoofdstuk 5 is aangetoond dat een behandeling met TENS een gunstig effect heeft op de cognitie en het gedrag van kinderen met ADHD. De significante afname in nachtelijke onrust is intrigerend gezien het veelvuldige voorkomen van slaapproblemen bij ADHD (e.g. Barkley, 1998). Kinderen met ADHD vertonen hogere niveaus van nachtelijke activiteit, vertonen een toename in rapid eye movement (REM) en slaap latentie en een afname in het percentage REM slaap dan kinderen zonder ADHD (Bullock & Schall, 2005; Konofal et al., 2001; Sangal et al., 2005). Sommige studies suggereren dat REM slaap een gunstig effect heeft op de consolidatie van cognitieve vaardigheden en dat het geassocieerd is met een toename in het niveau van brain derived neurotrophic factor (BDNF) in de dorsale hippocampus (Ulloor & Datta, 2005). Verondersteld wordt dat BDNF betrokken is bij de pathogenese van ADHD (Kent et al. 2005; Tsai, 2003). Studies hebben aangetoond dat verstoorde slaap een negatief effect kan hebben op leren en aandacht van kinderen en kan leiden tot ADHD symptomen. Ook wordt aangenomen dat verstoorde slaap de oorzaak kan zijn van executieve disfuncties, verminderde waakzaamheid, depressie, angst en hyperactiviteit (El-Ad & Lavie, 2005; O’Brien et al., 2004; Sadeh et al., 2002). Een afname in nachtelijke onrust door TENS kan inhouden dat de kinderen langer in een REM slaap zijn; tijdens de REM slaap is er geen spieractiviteit. Eerdere studies hebben aangetoond dat REM slaap gerelateerd is aan de secretie van neurotrophe factoren en op die manier een bijdrage levert aan geheugenfuncties. De resultaten van onze studie doen veronderstellen dat TENS een effect heft op de slaap efficiëntie van kinderen met ADHD, met gunstige effecten op cognitie en gedrag. Deze bevinding kan ook klinisch relevant zijn aangezien het bekend is dat kinderen met ADHD die behandeld worden met methylfenidaat in toenemende mate slaapstoornissen vertonen (Schwartz et al., 2004).

Samenvattend, de studies die in dit proefschrift worden beschreven doen veronderstellen dat geslachtsverschillen, achteruitgang in EF en aandachtsstoornissen in ADHD vooral gerelateerd zijn aan comorbiditeit. Geslachtsverschillen in de mate waarin ADHD gediagnosticeerd wordt kunnen worden verklaard door het feit dat jongens meer dan meisjes meer agressief en ‘externalizing’ zijn en daardoor vaker dan meisjes worden doorverwezen voor het vaststellen van ADHD. De slechtere overeenkomst tussen ouders en leerkrachten in de beoordeling van ADHD symptomen bij meisjes dan bij jongens kan ook een factor zijn.

Volgens de DSM-IV criteria, moet er op basis van ADHD symptomen sprake zijn van enige achteruitgang in twee of meer settings. Indien er minder overeenkomst is tussen ouders en leerkrachten wat betreft hun beoordeling van meisjes, is het ook minder waarschijnlijk dat zij voldoen aan de diagnostische criteria. Een afname van het werkgeheugen lijkt meer gerelateerd te zijn aan een taalstoornis dan aan ADHD. Een afname in een EF functie als planning bleek meer verbonden te zijn met tekenen van autisme en depressie dan met symptomen van ADHD. Een taalstoornis bleek de beste voorspeller te zijn van de beoordeling van aandachtscapaciteit van het kind door de leerkracht. Sommige ADHD

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symptomen kunnen veroorzaakt worden door slaapstoornissen en kunnen mogelijk verbeterd worden door TENS.

De belangrijkste conclusie van dit proefschrift is dat het voor de diagnostiek van ADHD essentieel is de kinderen te testen op comorbiditeit zodat functionele tekortkomingen in academische vorming en sociale vaardigheden zo adequaat mogelijk behandeld kunnen worden.

Concluderend kunnen de volgende aanbevelingen voor toekomstig onderzoek gemaakt worden:

1. Onderzoek naar de overeenkomst tussen de beoordelingen van de ouders en de leerkrachten van ADHD symptomen bij meisjes in een veel grotere steekproef.

2. Vergelijking van de beoordeling van ADHD door vaders en mannelijke leerkrachten met de beoordeling van ADHD door moeders en vrouwelijke leerkrachten.

3. Onderzoek naar de relatie tussen taalstoornissen en aandachtsstoornissen bij kinderen met ADHD.

4. Verder onderzoek naar de relatie tussen executieve disfuncties en symptomen van autisme en depressie bij kinderen met ADHD.

5. Verder onderzoek naar de effecten van TENS bij kinderen met ADHD met een grotere steekproef en een controle groep.

6. Onderzoek naar het slaappatroon van kinderen met ADHD die worden behandeld met een stimulant of met TENS.

7. Onderzoek naar de invloed van slaapstoornissen op ADHD symptomen en aanverwante stoornissen.

8. Onderzoek naar de relatie tussen het slaap-waakritme en executieve functies bij kinderen.

9. Onderzoek naar de effecten van TENS bij kinderen met slaapstoornissen.10. Onderzoek naar de effecten van TENS op de executieve functie ‘planning’ van

kinderen.11. Onderzoek naar de effecten van TENS op de REM slaap van kinderen en

volwassenen.12. Onderzoek naar de effecten van TENS op het ‘restless legs syndrome/periodic

leg movement disorder’.13. Onderzoek naar de effecten van TENS op het noradrenerge, serotonerge,

dopaminerge, en andere neurotransmitter systemen door middel van beeldvormende technieken zoals functional magnetic resonance imaging (fMRI) en positron emission tomography (PET) scans.

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REFERENCES















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Athyglisbrestur með ofvirkni (attention-deficit/hyperactivity disorder, ADHD) er algengasta taugageðröskun barna og unglinga og greinist hjá um helmingi þeirra sem leita á barna- og unglingageðdeildir. Röskun þessi hefur neikvæð áhrif á fjölskyldulíf barna, námsárangur þeirra, starfshæfni og samskiptahæfileika. Einkenna gætir í mörgum tilfellum fram á fullorðinsár. Helstu einkenni röskunarinnar hjá börnum eru skert athygli, hreyfiofvirkni og hvatvísi. Orsakir eru enn óþekktar, en taugasálfræðilegar kenningar hafa verið settar fram um að ADHD einkennist helst af skertri stjórnunarfærni (executive function, EF). Greining á ADHD byggist yfirleitt á lýsingu foreldra og kennara á hegðun barnsins. Einnig er oftast stuðst við greindarpróf og/eða taugasálfræðileg próf. Mörgum spurningum er enn ósvarað hvað varðar fylgni ADHD við aðrar geð- og þroskaraskanir, kynjamun, taugasálfræðilega veikleika, greiningaraðferðir og meðferð.

Meginmarkmið þessarar doktorsrannsóknar er að auka við núverandi þekkingu með því að athuga eftirfarandi þætti:

a) Kynjamun á ADHD einkennum í heilbrigðu íslensku þýði.b) Áhrif sértækrar málþroskaröskunar (specific language impairment, SLI) á

vinnsluminni barna, sem eru með samsetta gerð af ADHD.c) Sambandið á milli hegðunarmats og taugasálfræðilegs mats á ADHD

einkennum.d) Áhrif taugaraförvunar gegnum húð (transcutaneous electrical nerve stimulation,

TENS) á vitsmunastarfsemi, hegðun og sveifluna á milli hvíldar og virkni í börnum með samsetta gerð af ADHD.

Kafli 2. Megin tilgangur rannsóknarinnar var að athuga kynjamun á einkennum um ADHD og fylgikvillum þess í þýði heilbrigðra íslenskra barna. Annar tilgangur var að athuga hvaða tengdir hegðunarþættir spáðu best fyrir einkennum um ADHD. Flestar rannsóknir í hinum vestræna heimi hafa sýnt að drengir eru líklegri en stúlkur til að greinast með ADHD, en kynjamunur hefur sýnt sig að vera breytilegur eftir menningarkimum og eftir því hvaða aðili metur hegðun barnsins (Brewis & Schmidt, 2003; Pineda et al., 1999). Meirihluti þeirra rannsókna, sem framkvæmdar hafa verið fram til þessa á ADHD, hefur stuðst við úrtök drengja, sem greinst hafa með röskunina og því er tiltölulega lítið vitað um einkenni röskunarinnar hjá stúlkum. Niðurstöður þessarar rannsóknar sýndu, að íslenskir foreldrar og kennarar meta drengi með marktækt meiri ofvirknis- og hvatvísiseinkenni og marktækt meiri einkenni um árásargirni (aggression), heldur en stúlkur. Kennarar meta líka drengi með fleiri einkenni um athyglisbrest heldur en stúlkur, en að mati foreldra er ekki kynjamunur á þeim einkennum. Úthverf vandamál (externalizing problems) eins og árásargirni og hegðunarvandamál spáðu best fyrir einkennum um ofvirkni og hvatvísi og innhverf vandamál (internalizing problems) eins og kvíði og þunglyndi ásamt með námsvandamálum, spáðu best fyrir athyglisbrestseinkennum hjá bæði drengjum og stúlkum. Áhugavert er, að marktæk fylgni var á milli mats foreldra og kennara á ADHD

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einkennum hvað drengi varðaði, en ekki þegar stúlkur áttu í hlut. Sú tilgáta er sett fram að úthverf hegðun, sem er drengjum eiginlegri en stúlkum, kunni að hafa hvetjandi áhrif til hækkunar mats á ADHD einkennum þeirra, einkum meðal kennara. Vísbendingar, sem komu fram um lélegri samsvörun milli hegðunarmats foreldra og kennara á ADHD einkennum með tilliti til stúlkna, gæti haft klínískt mikilvægi, því það gæti valdið því að færri stúlkur en drengir nái greiningarskilmerkjum um ADHD og fái þá síður viðeigandi meðferð við vandamálum sínum.

Kafli 3. Tilgangur rannsóknar þessarar var að athuga hvaða áhrif sértæk málþroskaröskun hefur á yrt og óyrt vinnsluminni barna, sem eru með samsetta gerð af ADHD. Nokkrir vísindamenn hafa sett fram þá kenningu að skert vinnsluminni sé einkennandi fyrir ADHD. Rannsóknir hafa sýnt að skert yrt vinnsluminni er grunnvandamál í annarri þroskaröskun, sem nefnd hefur verið sértæk málþroskaröskun (specific language impairment, SLI). SLI er algengur fylgikvilli með ADHD. Niðurstöður rannsóknarinnar sýna að börn, sem eru bæði með ADHD og SLI, standa sig mun verr á prófum, sem mæla yrt vinnsluminni, heldur en bæði börn sem eru með ADHD án SLI og þau sem eru heilbrigð. Börn með ADHD bæði með og án málþroskaröskunar stóðu sig jafnvel og heilbrigð börn á prófum, sem mæla óyrt vinnsluminni. Það er ályktað að skert vinnsluminni sé ekki einkennandi fyrir ADHD og að skert yrt vinnsluminni tengist meðfylgjandi málþroskaröskun. Niðurstöður rannsóknarinnar benda á mikilvægi þess að skimað sé fyrir málþroskaröskun í rannsóknum á taugasálfræðilegum veikleikum barna með ADHD.

Kafli 4. Inntak flestra nýlegra taugasálfræðilegra kenninga, sem settar hafa verið fram um ADHD, hefur verið, að helstu einkenni röskunarinnar sé skert stjórnunarfærni (executive function, EF). Tiltölulega fáar rannsóknir hafa hins vegar verið gerðar á sambandinu á milli mats foreldra og kennara á ADHD einkennum barna og frammistöðu þeirra á taugasálfræðilegum prófum, sem talin eru næm á stjórnunarfærni. Markmið þessarar rannsóknar var að athuga sambandið á milli stjórnunarfærni eins og hún er mæld með taugasálfræðilegum prófum annars vegar og ADHD einkenna og tengdri hegðun eins og hún er metin af foreldrum og kennurum hins vegar. Samband þetta var athugað í hópi 7-11 ára barna, sem flest höfðu áður verið greind með ADHD. Nokkrar mismunandi gerðir stjórnunarfærni voru athugaðar. Auk þess var gerð athugun á greind og málþroska barnanna. Niðurstöður sýna, að sambandið á milli einkenna um ADHD og frammistöðu á prófum, sem meta stjórnunarfærni, er yfirleitt lítið og ómarktækt. Þegar tekið var tillit til greindar voru próf, sem meta stjórnunarfærni, marktækt tengd einkennum um einhverfu og einkennum um þunglyndi, en tengdust ekki einkennum um athyglisbrest eða ofvirkni/hvatvísi. Athyglisvert er að það próf, sem spáði best fyrir mati kennara á athyglisbrestseinkennum, var málþroskapróf, en ekki próf, sem meta stjórnunarfærni. Það er ályktað að niðurstöður rannsóknarinnar styðji ekki kenningar um að skert stjórnunarfærni sé einkennandi fyrir ADHD. Vísbendingar komu fram um að einkenni um athyglisbrest kunni í sumum tilfellum að stafa af skertum málskilningi. Mikilvægt er að skima fyrir málþroskaröskun hjá börnum, sem grunuð eru um að vera með ADHD bæði til að auka líkur á réttri greiningu og enn frekar til að þau hljóti viðeigandi meðferð.

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Kafli 5. Í þessum kafla er fjallað um áhrif TENS meðferðar á vitsmunastarfsemi, hegðun og sveifluna á milli hvíldar og virkni í börnum með samsetta gerð af ADHD. Niðurstöður rannsóknarinnar sýna, að TENS meðferð hafði jákvæð áhrif á vitsmunastarf, sérstaklega það sem reynir á stjórnunarfærni. Hegðun eins og hún var metin af foreldrum og kennurum batnaði einnig. Athyglisvert er að TENS meðferð dró úr hreyfivirkni eins og hún var mæld með virknimæli (actigraphy) bæði að nóttu sem degi. Sú tilgáta er sett fram að áhrif TENS meðferðar, sem fram koma í þessari rannsókn, séu vegna örvunar heilasvæða, sem stjórna svefni og vöku, í gegnum dreifina.

Megin greiningarskilmerki ADHD eru athyglisbrestur, ofvirkni og hvatvísi. Hins vegar hefur verið sýnt fram á í þessari ritgerð, að fylgikvillar og kynferði í ADHD hafa mikilvæg áhrif á vitsmunastarfsemi (Kaflar 3,4 og 5) og á hegðun (Kafli 2). Þannig er í Kafla 2 sýnt fram á að heilbrigðir íslenskir drengir eru metnir með meiri einkenni um ofvirkni/hvatvísi og árásargirni, en heilbrigðar íslenskar stúlkur bæði af foreldrum og kennurum. Þessar niðurstöður gefa vísbendingu um að drengir, sem eru frá náttúrunnar hendi almennt árásargjarnari og með meiri hreyfióróleika en stúlkur, séu vegna þeirra eiginleika líklegri en stúlkur til að verða greindir með ADHD. Einnig er hugsanlegt að til staðar sé kerfisbundin skekkja (rater bias) hjá þeim er leggja mat á hegðun barnanna. Rannsóknin sýndi einnig, að kennarar meta drengi með meiri einkenni um athyglisbrest en stúlkur, en að þessi kynjamunur kemur ekki fram hjá foreldrum. Skýringin á þessu gæti verið sú, að einkenni um athyglisbrest eru mjög tengd námserfiðleikum og kennarar eru næmari fyrir þeim, en foreldrar. Meira áberandi hegðun drengja en stúlkna gæti skýrt hversvegna kennarar taka betur eftir athyglisbrestseinkennum (námserfiðleikum) og meta þau þess vegna meiri. Sjáanlegri hegðunareinkenni drengja gætu líka útskýrt hvers vegna meiri samsvörun er á milli hegðunarmats foreldra og kennara hvað drengi varðar heldur en stúlkur. Nýlegar rannsóknir hafa sýnt að kennarar geti í sumum tilfellum verið að ofgreina einkenni um ADHD og að þættir eins og bekkjarstærð og menningarsvæði geti haft áhrif á skoðanir kennara á því, hverjir nemenda þeirra séu með einkenni um röskunina (Havey et al., 2005). Í rannsókn okkar voru það yfirleitt mæður barnanna, sem lögðu mat á hegðunina og allir kennararnir, sem mátu hegðun barnanna, voru kvenkyns. Rannsóknir hafa sýnt að börn með ADHD eru mun líklegri til að hlýða feðrum sínum og karlkennurum heldur en mæðrum sínum og kvenkennurum (Barkley, 1998). Það væri mjög áhugavert að gera rannsókn á því, hvort munur sé á mati karla og kvenna á hegðun barna.

Þáttur málþroskaröskunar, sem yfirleitt er ekki skimað fyrir, er stórlega vanmetinn í greiningu á ADHD. Sett hefur verið fram sú kenning að stjórnunarfærniþátturinn vinnsluminni, sé eitt af grundvallarvandamálunum í ADHD. Rannsóknin í Kafla 3 sýnir, að skert vinnsluminni stafar af málþroskaröskun, sem er samfara ADHD einkennum. Niðurstöður rannsóknarinnar í Kafla 4 sýna að málþroskavandamál spá best fyrir mati kennara á athyglisbresti. Það er hugsanlegt, að sum greiningarskilmerkin fyrir ADHD samkvæmt DSM-IV, sérstaklega hvað einkenni um athyglisbrest snertir, gætu í raun skýrst af skertum málskilningi. Dæmi um þessi greiningarskilmerki eru: “Virðist oft ekki

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hlusta þegar talað er beint til hans/hennar; virðist oft ekki fylgja fyrirmælum og lætur oft hjá líða að ljúka skólaverkefnum, viðvikum eða vinnuskyldum”. Samræðuhæfileikar eins og að skiptast á að tala og halda sér við umræðuefnið eru skertir bæði í ADHD og í málþroskaröskun. Lélegur málskilningur getur farið mjög leynt og kemur oft ekki í ljós fyrr en barnið er prófað formlega. Máþroskaröskun samhliða ADHD gæti hugsanlega skýrt hvers vegna meðferð með örvandi lyfjum, sem er algengasta meðferðarform við ADHD, virðist ekki bæta námsárangur eða félagslega færni (Bennett et al., 1999; Chronis et al., 2006). Sú tilgáta hefur verið sett fram, að ADHD án ofvirkni/hvatvísi og ADHD með ofvirkni/hvatvísi séu sitt hvor röskunin (Barkley, 1998; Bauermeister et al., 2005). Börn með þá gerð ADHD, þar sem eingöngu er um athyglisbrestseinkenni að ræða, fá einkennin seinna, virðast vera lengur að átta sig, virðast síðri til að hefja mannleg samskipti og eru ólíklegri til að vera með hegðunarvandamál heldur en börn með þá gerð ADHD, þar sem bæði einkenni um athyglisbrest og ofvirkni/hvatvísi eru til staðar (Bauermeister et al., 2005). Niðurstöður rannsókna í þessari ritgerð vekja þá spurningu, hvort athyglisbrestseinkennin í ADHD stafi í raun af skertum málskilningi. Þörf er á frekari rannsóknum til að athuga hvort svo geti verið. Í Kafla 5 kemur fram, að meðferð með TENS (taugaraförvun gegnum húð) hafði jákvæð áhrif á hegðun barna með ADHD. Þær niðurstöður, sem sýndu að marktækt dró úr hreyfivirkni barnanna í svefni, eru sérstaklega áhugaverðar í ljósi þess, að svefntruflanir eru algengt vandamál barna, sem eru með ADHD (e.g. Barkley, 1998). Rannsóknir hafa sýnt, að börn með ADHD hreyfa sig meira í svefni, eru lengur að komast á REM (rapid eye movement) svefnstigið og eyða minni tíma í REM svefni heldur en önnur börn (Bullock & Schall, 2005; Konofal et al., 2001; Sangal et al., 2005). Rannsóknir hafa sýnt að REM svefn kunni að hafa jákvæð áhrif á vitsmunastarfsemi og að honum tengist aukin framleiðsla á BDNF (brain derived neurotrophic factor) í ákveðnum svæðum sæhestsins (dorsal hippocampus) (Ulloor & Datta, 2005). Sú tilgáta hefur verið sett fram að BDNF sé hugsanlega tengt orsökum ADHD (Kent et al., 2005; Tsai, 2003). Rannsóknir hafa sýnt að truflun á svefni geti haft neikvæð áhrif á nám og athygli barna og jafnvel leitt til einkenna um ADHD. Því hefur verið haldið fram að truflun á svefnmynstri geti valdið skertri stjórnunarfærni, slakri athygli, þunglyndi, kvíða og ofvirkni (El-Ad & Lavie, 2005; O’Brien et al., 2004; Sadeh et al., 2002). Niðurstöður okkar, sem sýna að TENS meðferð dregur úr hreyfivirkni í svefni, gætu bent til þess að börnin séu að eyða meiri tíma í REM svefni, en meðan á því svefnstigi stendur, eru engar vöðvahreyfingar til staðar og líkaminn er sem lamaður. Fyrri rannsóknir hafa sýnt að REM svefn tengist framleiðslu á taugaverjandi þáttum (neurotrophic factors) og kunni þannig til dæmis að hafa jákvæð áhrif á minnisstarfsemi. Niðurstöður okkar kunna hugsanlega að vera vísbending um að TENS meðferð geti haft jákvæð áhrif á svefn barna með ADHD og um leið haft jákvæð áhrif á hegðunarmynstur þeirra. Þessar niðurstöður gætu einnig verið klínískt mikilvægar í ljósi rannsókna sem sýnt hafa fram á auknar svefntruflanir hjá börnum með ADHD, sem eru á meðferð örvandi lyfja (Schwartz et al., 2004).

Rannsóknirnar, sem greint er frá í ritgerð þessari, gefa til kynna að þættir eins og kynjamunur, skert stjórnunarfærni og einkenni um skerta athygli í ADHD tengist einkum fylgikvillum röskunarinnar. Ein ástæðan fyrir því, að svo miklu fleiri drengir en stúlkur greinast með ADHD, gæti verið sú, að drengir eru frá náttúrunnar hendi árásargjarnari og

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fyrirferðarmeiri en stúlkur og að þeim sé af þeim sökum frekar vísað í greiningu. Minni samsvörun á mati foreldra og kennara á hegðun stúlkna en drengja gæti líka skýrt það að einhverju leyti. Til að uppfylla greiningarskilmerki samkvæmt DSM-IV þurfa einkenni um ADHD að vera til staðar við fleiri en einar aðstæður, t.d. bæði á heimili og í skóla. Ef foreldrar og kennarar eru síður sammála um hegðunarmat sitt á stúlkum en drengjum gæti verið erfiðara fyrir stúlkur að ná tilskyldum greiningarskilmerkjum og að þær fái því hugsanlega síður viðeigandi meðferð við sínum vandamálum. Skert vinnsluminni barna, sem sumir vísindamenn hafa talið vera einkennandi fyrir ADHD, reyndist samkvæmt rannsókn þessari vera tengdara málþroskaröskun, heldur en ADHD einkennum. Skert skipulagsfærni reyndist vera tengdari einkennum um einhverfu og þunglyndi, heldur en einkennum um ADHD. Í ljós kom að málþroskaröskun spáir best fyrir mati kennara á athyglisbrestseinkennum. Hugsanlegt er, að sum einkenni um ADHD geti stafað af svefntruflunum, sem ef til vill má bæta með TENS meðferð.

Það er megin niðurstaða þessarar doktorsrannsóknar, að þegar greining á ADHD fer fram, sé það grundvallaratriði, að skimað sé fyrir öðrum hugsanlegum röskunum, sem valdið geti einkennum eins og t.d. málþroskaröskun og svefntruflunum, svo tryggt sé að börnin fái viðeigandi meðferð.

Í ljósi niðurstaðna þeirra rannsókna, sem greint er frá í ritgerð þessari, mætti benda á eftirfarandi framtíðarrannsóknarefni:

1. Rannsókn á samsvöruninni á milli mats foreldra og kennara á ADHD einkennum stúlkna með því að nota stærri úrtök.

2. Samanburður á mati feðra og karlkyns kennara á einkennum um ADHD og mati mæðra og kvenkyns kennara.

3. Athugun á sambandinu á milli málþroskaröskunar og einkenna um athyglisbrest hjá börnum með ADHD.

4. Nánari rannsókn á sambandinu á milli stjórnunarfærni (EF) og einkenna um einhverfu og þunglyndi meðal barna með ADHD.

5. Rannsókn á áhrifum TENS meðferðar á börn með ADHD, í stærra úrtaki og með því að nota samanburðarhópa.

6. Bera saman svefnmynstur barna, sem eru á lyfjameðferð við ADHD og þeirra sem fá TENS meðferð.

7. Athugun á áhrifum svefntruflana á ADHD einkenni og tengdar raskanir.8. Rannsókn á sambandinu á milli svefnmynsturs og stjórnunarfærni í börnum.9. Athugun á áhrifum TENS meðferðar á börn, sem eiga við svefnvandamál að

stríða.10. Könnun á áhrifum TENS meðferðar á skipulagsfærni barna.11. Rannsókn á áhrifum TENS meðferðar á REM svefn í börnum og fullorðnum.12. Athugun á áhrifum TENS meðferðar á fótaóeirð (restless leg syndrome/periodic

leg movement disorder).13. Rannsókn á áhrifum TENS meðferðar á noradrenalin, serotonin, dopamine og

önnur taugaboðefni, með því að nota taugamyndgreiningu svo sem starfræna segulómun (fMRI) og PET (positron emission tomography) skönnun.

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Words of thanks

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WORDS OF THANKS

This thesis would not have been made without the help and support of many. I would like to extend my sincere gratitude to all those who made it possible.

I thank Erik, my first promoter. Without him this project would never have been realized. It was through a series of coincidences that I came to hear of his studies with TENS. The talk he gave at the European Graduate School of Child Neuropsychology in the spring of 1998 was the seed that started the sprouting of this thesis. I thank you Erik for all your help and unrelenting support through these last several years. I thank you for always believing in me and assuring me that this would be possible, in spite of me living and working in another country. I thank you for your invaluable expert scientific guidance. I thank you for your endless patience and good humour. I thank you and your wife, Sylvia, for all your assistance on my trips to Amsterdam and Groningen. I thank you for inviting me to your home and making me feel like one of the family. Special thanks to Sylvia for introducing me to the exciting world of antique auctions.

I thank Anke, my second promotor. Thank you Anke for all your assistance and support in the making of this thesis. It has been invaluable to have a scientist of your exceptional standard to guide me. Thank you for solving problems with your superb analytical thinking and skill. Thank you for your positive attitude and enthusiasm. Thank you and your husband, Louis, for all the enjoyable discussions we have had in your home, both in Amsterdam and Groningen.

I thank Joe, my third promoter, for all the help he has given me with this project. It has been a great privilege to have had access to his expert knowledge of the field of ADHD. Thank you Joe for lending your great critical scientific eye to my work and for all your excellent advice throughout the years.

My sincere thanks to all the children, parents and teachers who have participated in this research.

I thank the psychology students who participated in the data collection for parts of this research.

I extend my gratitude to the people that have contributed to the funding of this thesis.I thank my co-workers at the Landspitali-University Hospital who have given me

support and friendship.I thank all my friends who have always stood by me and given their moral support, no

matter what.I thank my dear mother, Sigríður Soffía Jónsdóttir and my late father, Jón Gunnlaugur

Halldórsson, for all the love and support they have given me throughout the years.I thank my mother-in-law, Ása Guðmundsdóttir and my late father-in-law, Þorgeir

Gestsson for all their love and support in years past.I thank my children and their spouses for their patience, understanding and love and

my four beautiful grandchildren, Sólveig, Gestur, Sævar and Eyjólfur, for lighting up my life.

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And last, but not least, I would like to thank my husband, my best friend and soulmate, for his input. Dear Gestur. Of course this would never have been possible without your constant support, patience and love. Thank you for always being there, through both the highs and the lows connected to this enterprise.

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Curriculum vitae

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CURRICULUM VITAE Sólveig Jónsdóttir was born in Reykjavík, the capital of Iceland, in 1949. She obtained

her B.A. degree in psychology from the University of Iceland in 1975. In 1978, after working for a few years as an English teacher in a junior high school in Reykjavík, she moved with her husband and children to Cleveland, Ohio in the USA. She received her master’s degree in Educational Psychology from John Carroll University in Ohio, in 1982. In 1984, after two years of postgraduate study, she received her certification in the speciality of School Psychology from John Carroll University. In 1997, after working as a psychologist in schools and for the social services in Reykjavík for 12 years, she went to Amsterdam in The Netherlands, where she attended The European Graduate School of Child Neuropsychology. She received her diploma in child neuropsychology in 1998. Her final thesis named “Neuropsychological Deficits in Children Prenatally Exposed to Alcohol”, was published in Læknablaðið, The Icelandic Medical Journal, in February 1999. She started working at the Department of Child and Adolescent Psychiatry at the Landspitali-University Hospital in Reykjavík in 1998. In 2000 she started her PhD studies in clinical neuropsychology with professor dr. Erik J.A. Scherder and professor dr. Anke Bouma at the Rijksuniversiteit Groningen in Groningen and with professor dr. Joseph A. Sergeant at Vrije Universiteit in Amsterdam. She received certification in the speciality of Clinical Child Psychology in 2000 and in the subspeciality of Clinical Child Neuropsychology in 2002. She is currently working in the Department of Neurology and the Department of Rehabilitation at the Landspitali-University Hospital in Reykjavik.

Curriculum vitae

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University of Groningen ADHD and its relationship to comorbidity … · 2016-03-09 · (e) is often “on the go” or often acts as if “driven by a motor” (f) often talks excessively