ADHD and its relationship to comorbidity and gender
Sólveig Jónsdóttir
The studies presented in this dissertation were funded in part by:
1) Vísindasjóður Landspítala-háskólasjúkrahúss
2) Sjóður Odds Ólafssonar, Öryrkjabandalagi Íslands
3) 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 9979-70-166-8
ISBN 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:
Prof.dr. E.J.A. Scherder
Prof.dr. J.M. Bouma
Prof.dr. J.A. Sergeant
Beoordelingscommissie:
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 ...................................................... 41
Archives of Clinical Neuropsychology, 2005, 20, 443-456
4. Relationships between neuropsychological measures of
executive function and behavioural measures of ADHD
symptoms and comorbid behaviour ................................................................................ 59
Archives of Clinical Neuropsychology, in press, available online 28 July, 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
Neurorehabilitation and Neural Repair, 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
CHAPTER ONE
1
Introduction
Introduction
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 Diagnostic and Statistical Manual of Mental
Disorders, 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
Chapter one
(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; ADHD Combined Type if 6 or more symptoms of both inattention
and hyperactivity/impulsivity symptoms have been present for the past 6 months, ADHD
Predominantly Inattentive Type if only 6 or more symptoms of inattention have been
present for the last 6 months, ADHD Predominantly Hyperactive-Impulsive Type if 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 Predominantly Inattentive
Type than 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).
10
Introduction
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 Predominantly Inattentive Type and the Combined
Type). 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 Combined Type of ADHD. As a result more studies of the Inattentive Type 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 sleepwake 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
11
Chapter one
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
Combined Type 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.
12
Introduction
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
13
Chapter one
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).
1
Introduction
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). Diagnostic and statistical manual of mental
Disorders, 3rd ed. Washington, DC: Author..
American Psychiatric Association (2000). Diagnostic and Statistical Manual ofMental
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. Psychological Bulletin,121,
65-94.
Barkley, R.A. (1998). Attention-deficit hyperactivity disorder: A handbook for diagnosis
and treatment, 2nd ed. New York: Guilford Press.
Biederman, J. (2005). Attention-deficit/hyperactivity disorder: A selective overview.
Biological Psychiatry, 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. Journal of
Clinical Child and Adolescent Psychology, 34, 449-476.
Pliszka, S.R. (1998). Comorbidity of attention-deficit/hyperactivity disorder with
psychiatric disorder: An overview. The Journal of Clinical Psychiatry, 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. Journal of the American Academy of Child and
Adolescent Psychiatry, 43, 1276-1282.
Staller, J. & Faraone, S.V. (2006). Attention-deficit hyperactivity disorder in girls:
Epidemiology and management. CNS Drugs, 20, 107-123.
1
1
CHAPTER TWO
2
Gender 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
1
Chapter Two
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.
1
Gender differences in symptoms of ADHD
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
1
Chapter two
& 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 one group. 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
20
Gender differences in symptoms of ADHD
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
Behavior Assessment System for Children (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 Attention Problems scale
21
Chapter two
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 called Attention Problems, Atypicality and Withdrawal.
The Teacher Rating Scales (TRS) have in addition to the aforementioned nine scales,
a clinical scale called Learning Problems. In this study an additional scale called ADHD
symptoms was formed by combining scores on the Hyperactivity scale and the Attention
Problems 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 almost always = 3).
Internal consistency coefficients (Kjartansdottir, 2002) for the BASC Icelandiclanguage 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.
22
Gender differences in symptoms of ADHD
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 Conduct Problems. 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 p values 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 Attention Problems. For means, standard deviations,
F and p values 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 p values and effect sizes
Boys
(n=68)
BASC subscales
Mean
Girls
(n=47)
(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
Conduct Problems
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
Attention Problems
6.15
(3.75)
5.09
(3.41)
2.399
.124
.15
ADHD symptoms¹
12.50
(6.93)
9.83
(5.72)
4.741
.032
.21
¹ ADHD symptoms = Hyperactivity and Attention Problems scales combined
23
Chapter two
TABLE 2
Difference between boys and girls on the clinical scales of the BASC Teacher Rating Scales
F and p values and effect sizes
Boys
(n=68)
BASC subscales
Girls
(n=47)
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
.12
Conduct Problems
1.90
(2.46)
1.36
(2.16)
1.449
.231
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
Attention Problems
7.26
(4.84)
4.23
(4.61)
11.331
.001
.31
Learning Problems
5.69
(5.15)
5.51
(5.07)
.035
.853
.02
ADHD symptoms¹
16.12
(11.16)
8.64
(8.93)
14.628
.000
.35
¹ ADHD symptoms = Hyperactivity and Attention Problems scales combined
Prediction of Hyperactivity and Attention Problems in boys and girls
We conducted a series of multiple regressions with Hyperactivity and Attention Problems
completed by the parents and teachers as criterion measures and Aggression, Conduct
Problems, Anxiety, Depression, Somatization, and Learning Problems (only included in
the TRS) as predictors. The scale Attention Problems was also used as predictor when
the Hyperactivity scale was the criterion measure and the scale Hyperactivity was added
as predictor when the Attention Problems scale was the criterion measure. Regressions
were conducted with respect to separate outcomes of (1) Attention Problems in boys and
girls, obtained from the PRS, (2) Attention Problems 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).
2
Gender differences in symptoms of ADHD
TABLE 3
Standard regression analyses for variables predicting Attention Problems in boys and girls
Variable
Unstandardised
Coefficient (B)
t-value
p-value
Attention Problems in boys, obtained from the PRS
Aggression
.24
1.92
.059
Anxiety
.34
3.66
.001
Hyperactivity
.28
2.56
.013
Attention Problems in girls, obtained from the PRS
Somatization
.42
2.48
.017
Anxiety
.23
2.46
.018
Attention Problems in boys, obtained from the TRS
Learning Problems
.40
5.00
.000
Depression
.49
4.16
.000
Hyperactivity
.16
2.59
.012
Attention Problems in girls, obtained from the TRS
Learning Problems
.44
4.48
.000
Hyperactivity
.22
2.68
.010
Depression
.27
2.42
.020
F-value
p-value
25.31
.000
14.94
.000
43.97
.000
29.55
.000
2
Chapter two
TABLE 4
Standard regression analyses for variables predicting Hyperactivity in boys and girls
Variable
Unstandardised
Coefficient (B)
t-value
p-value
Hyperactivity in boys, obtained from the PRS
Aggression
.50
4.13
.000
Somatization
.26
2.37
.021
Conduct Problems
.45
2.13
.037
Hyperactivity in girls, obtained from the PRS
Conduct Problems
.75
3.22
.002
Aggression
.33
2.62
.012
Hyperactivity in boys, obtained from the TRS
Aggression
.44
5.46
.000
Conduct Problems
.82
2.81
.007
Attention Problems
.31
2.47
.016
11.57
.000
Hyperactivity in girls, obtained from the TRS
Aggression
Learning Problems
Anxiety
.73
.47
4.97
.000
-.26
-.2.18
.035
F-value
p-value
26.16
.000
35.55
.000
62.61
.000
56.46
.000
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 Attention Problems (see Table 3). The sample multiple correlation coefficient
was .74, indicating that approximately 54% of the variance of the score on the Attention
Problems subscale could be accounted for by the combination of Aggression, Anxiety,
and Hyperactivity.
The unstandardized coefficients indicate that Anxiety is the strongest predictor for
Attention Problems 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 Attention Problems
subscale could be accounted for by the combination of Somatization and Anxiety.
The unstandardized coefficients indicate that Somatization and Anxiety are the strongest
predictors of Attention Problems in girls as rated by parents.
2
Gender differences in symptoms of ADHD
Attention Problems in boys, obtained from the Teacher Rating Scales. The
combination of the predictors Learning Problems, Depression, and Hyperactivity was
significantly related to Attention Problems (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 Learning
Problems, Depression, and Hyperactivity.
According to the unstandardized coefficients Learning Problems and Depression were
the strongest predictors for Attention Problems.
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 Attention Problems (see Table 3). The sample multiple correlation
coefficient was .81, indicating that approximately 67% of the variance of the score on
Attention Problems could be accounted for by the combination of Learning Problems,
Hyperactivity and Depression.
The unstandardized coefficients indicated that the scale Learning Problems was the
strongest predictor of Attention Problems in girls as rated by teachers.
When Learning Problems was taken out as a predictor for Attention Problems the scale
Depression was the best predictor for Attention Problems 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 to Hyperactivity (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 Conduct Problems.
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 Conduct Problems 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, Conduct Problems, and Attention Problems
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
2
Chapter two
Problems, and Attention Problems.
The unstandardized coefficients indicate the scale Conduct Problems as 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, Learning Problems and 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, Learning Problems, 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 norms
boys and girls
(n = 745)
Icelandic sample
boys and girls
(n = 115)
Icelandic sample
boys only
(n = 68)
Icelandic sample
girls only
(n = 47)
Aggression
Conduct Problems
0.38
0.49
0.25**
0.28**
0.30*
0.32**
0.08
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
ADHD symptoms¹
0.24
0.48**
0.42**
0.52**
0.47**
0.42**
0.21
**. Correlation is significant at the 0.01 level (2-tailed)
*. Correlation is significant at the 0.05 level (2-tailed)
¹ADHD symptoms = Hyperactivity and Attention Problems scales combined
2
Gender differences in symptoms of ADHD
The ratio of boys versus girls with ADHD symptoms
The ratio of boys versus girls with ADHD symptoms 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 Hyperactivity and Aggression and somewhat higher (a trend) for the
scale Conduct Problems. 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 Attention Problems scale 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, Aggression and
also on Attention Problems 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/
2
Chapter two
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 Anxiety best predicted Attention Problems in
boys and the scales Somatization and Anxiety best predicted Attention Problems 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 Learning
Problems 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 Learning Problems was taken out as a predictor for Attention Problems the scale
Depression was the best predictor for Attention Problems 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 Learning Problems 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 Hyperactivity subscale,
which is the third best predictor of inattention in the regression analysis, may be elevating
their scores on the Attention Problems subscale as rated by teachers (see Table 2).
Prediction of hyperactive/impulsive symptoms in boys and girls
According to parents, externalizing problems (Aggression and Conduct Problems) 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
30
Gender differences in symptoms of ADHD
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 Attention
Problems best predicted hyperactivity symptoms in boys while Aggression associated
with Learning Problems 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 (Attention
Problems, 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
Attention Problems and Hyperactivity combined 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.,
31
Chapter two
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 Conduct Problems 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 Conduct Problems. Our findings suggest that teachers
may, to a greater extent than parents, rate conduct disorders as Hyperactivity in boys and
as Conduct Problems 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).
32
Gender differences in symptoms of ADHD
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.
33
Chapter two
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3
0
CHAPTER THREE
3
The 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
1
Chapter three
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.
2
The impact of specific language impairment on working memory
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-IV differentiates 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;
3
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, the central executive, which is assisted by two subsidiary
systems for maintaining information: a verbal storage system called the phonological
loop, 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 phonological loop has been associated with
the left temporoparietal region. The central executive 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 ADHDC 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
The impact of specific language impairment on working memory
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.
Criteria for specific language impairment (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
TABLE 1
Table 1
Age, nonverbal intelligence, and performance of groups on the TOLD-2I
Whole ADHD
group (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.
10.
103.2
1.2
12.2
10.
10.3
1.1
12.
10.
10.0
1.2
10.
10.33
113.2
1.2
11.
TOLD-2I Composites
SLQb
Receptive language
Expressive language
Semantics
Syntax
3.
86.
82.
.
3.1
1.3
1.0
1.33
1.0
1.1
.2
1.1
1.32
2.
.3
.
10.
10.0
10.3
11.0
101.20
10.0
.
.3
103.33
10.1
.2
12.
10.0
12.
10.0
10.00
102.33
10.13
103.
12.0
12.3
11.
10.
13.
Subtests
Sentence combining
Vocabulary
Word ordering
Generals
Grammatic Compr.c
Malapropism
6.
8.2
8.23
8.0
.
8.1
2.
2.
2.
2.00
3.01
2.0
.00
.3
.21
.21
.
.21
1.
2.
1.3
1.1
2.
2.2
.3
11.00
10.
.2
11.0
10.20
1.
1.1
2.03
2.2
1.
1.
.20
11.0
10.0
11.0
11.
11.33
2.11
2.1
2.
1.1
2.2
1.
Age (years)
Nonverbal IQa
a
b
c
Nonverbal IQ = nonverbal intelligence.
SLQ = spoken language quotient.
Grammatic Compr.: grammatic comprehension.
to solve tasks. Problem solving abilities are measured on two mental processing scales:
Neuropsychological measures
Neuropsychological differences between groups were assessed with the K-ABC
(Kaufman & Kaufman,
1983; processing
Kaufman etability
al., 1987).
The K-ABC
an individually
Sequential
is believed
to relyismore
on the functioning
of the leftmeasure
cerebralofhemisphere
more
on theaged
right2½
cerebral
administered
intelligenceand
andsimultaneous
achievementprocessing
intended for
children
through 12½ years. It is based on research and theory in cognition and neuropsychology
K-ABC also
includes ability
a
, which
to the
authors, serves
andThe
is designed
to measure
(intelligence)
on theaccording
basis of the
processing
style as a
good
estimate
of
intellectual
potential
of
children
who
have
problems
in
the
areas
of
receptive
required to solve tasks. Problem solving abilities are measured on two mental processing
or
expressive
language,
who
have
language
disorders,
or
use
English
as
a
second
language.
scales: Sequential and Simultaneous. The Sequential Processing Scale is composed of the The
subtests Hand Movements, Number Recall, and Word Order. The Simultaneous Processing
Scale is composed of the subtests Gestalt Closure, Triangles, Matrix Analogies, Spatial
Memory and Photo Series. 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.
According
to Barkley (1997), verbal and spatial working memory has often been assessed
The
K-ABC
also includes
a Nonverbal
Scale, which
theoral
authors,
servesof digit
in neuropsychological
research
with the following
tasks:according
“retentiontoand
repetition
as a good
estimateinof
intellectual
of childrensuch
whoashave
problems
inlocating
the areasstimuli
spans
(especially
reverse
order);potential
mental arithmetic,
serial
addition;
of
receptive
or
expressive
language,
who
have
language
disorders,
or
use
English
as a
within spatial arrays of information that must be held in memory; and holding sequences
of
second
language.
The
Nonverbal
Scale
is
composed
of
the
subtests:
Hand
Movements,
information in memory to properly execute a task, as in self-ordered pointing tasks”. In the
Triangles,
Matrix
Analogies,
Spatial Memory and Photo Series.
current
study,
the K-ABC
subtests
The impact of specific language impairment on working memory
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 selfordered pointing tasks”. In the current study, the K-ABC subtests Number Recall and
Word Order were considered measures of verbal working memory and the subtests Hand
Movements and Spatial Memory were considered measures of spatial working memory.
Statistical analyses
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 (Sequential
and 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 the Simultaneous
Processing Scale than on the Sequential Processing Scale (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).
ADHD group
(n = )
Group 1,
ADHD + SLI
(n = 1)
Group 2,
ADHD non-SLI
(n = 1)
Group 3,
normal controls
(n = 1)
Main effect of
group ANOVA
Measures
Mean
S.D.
Mean
S.D.
Mean
S.D.
Mean
S.D.
F
K-ABC Composites
MPC
Sequential Prc.
Simultaneous Prc.
100.
91.21
107.02
11.
13.3
12.1
100.0
.3
10.1
10.1
12.2
11.0
10.3
.0
10.0
10.2
11.
12.
110.33
101.3
11.0
10.
.1
11.3
Subsets
Hand Movements
Gestalt Closure
Number Recall
Triangles
Word Order
Matrix Analogies
Spatial Memory
Photo Series
8.1
11.13
8.
11.1
8.
11.3
10.3
10.
2.2
3.00
3.02
2.
2.
2.
2.1
2.3
.
10.
.2
11.
.
12.00
10.
11.
3.21
2.1
3.0
2.3
1.
2.1
2.
2.
.0
11.
.3
12.0
10.20
11.3
10.
10.0
2.10
2.2
2.2
2.
2.
3.11
2.23
2.
10.2
10.
10.33
13.3
10.2
12.2
11.33
12.20
.
.
2.22
2.
.
.0
2.2
2.0
10.03
10.0
1.
2.1
10.0
10.30
Working Memory
Spatial WMa
Verbal WMb
Chapter three
Table 2
Means, standard deviations, ANOVAs, and contrasts of the different ADHD groups and the control group
df
P
Groups 1–3
contrasts
3.98
.99
1.05
2,46
2,46
2,46
.026
.001
ns
1<3
1 < 2,3
1.3
2.1
1.
2.10
2.0
2.
2.1
2.3
1.34
.37
.75
2.23
.81
.31
.56
1.85
2,46
2,46
2,46
2.
2,46
2,46
2,46
2,46
ns
ns
.001
ns
.003
ns
ns
ns
1.
1.
1.20
10.07
2,46
2,46
ns
.000
1 < 2, 3
1 < 2, 3
1 < 2, 3
Means, standard deviations, and analyses of variance (ANOVA) and contrasts of the scores of the K-ABC Composites and Subtests, and the Spatial and Verbal
Working Memory (WM) of the ADHD + specific language impairment (SLI), the ADHD non-specific language impairment (SLI) and the normal control
groups. K-ABC: Kaufman Assessment Battery for Children; MPC: Mental Processing Composite; Sequential Prc.: Sequential Processing; Simultaneous Prc.:
Simultaneous Processing.
a
Spatial working memory (WM) is composed of Hand Movements and Spatial Memory.
b
Verbal Working Memory (WM) is composed of Number Recall and Word Order.
The impact of specific language impairment on working memory
Subsequently, main effects of Group were calculated for K-ABC composites, and KABC subtests, by means of ANOVA. A significant main effect of Group was observed for
MPC, Sequential Processing Scale, Number Recall, and Word Order (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 Number Recall (F(1,32) = 11.76, P = .002) and (F(1,32) = 7.82, P = .009),
respectively, and Word Order of the Sequential Processing Scale (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 Sequential Processing Scale (r
= .48, n = 47, P = .001), but not with the Simultaneous Processing Scale (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 Word Order (r = .37, n = 47, P =
.01) and Number Recall (r = .52, n = 47, P = .000), but not with Hand Movements (r =
.21, n = 47, ns).
Chapter three
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 Number Recall and Word Order were significantly
correlated (r = .55, n = 47, P = .000). The two spatial working memory measures Spatial
Memory and Hand Movements were also significantly correlated (r = .39, n = 47, P =
.007). Hand Movements correlated significantly with both Number Recall (r = .309, n =
47, p = .03) and Word Order (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, Hand
Movements, Number Recall and Word Order. 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 Word
Order, 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 Hand Movements, which relies on nonverbal sequential processing. The
three groups did not differ significantly from one another on the Simultaneous Processing
Scale or any of its subtests. According to Kaufman and Kaufman (1983), the Simultaneous
Processing Scale 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
0
The impact of specific language impairment on working memory
Order similarly to our ADHD+SLI sample.
The poor performance of the ADHD+SLI group on the Number Recall test in this study,
is in agreement with studies on SLI children using the Digit Span 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 Digit Span test and
several studies have shown this subtest to be the most sensitive to attentional deficit. The
Digit Span Forwards 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
(Number Recall + Word Order), but there were no significant differences between the three
groups on Spatial WM (Hand Movements + Spatial Memory) 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.
1
Chapter three
Relationship between K-ABC measures and spoken language quotient
(SLQ)
The present results indicate that SLQ is significantly correlated with the Sequential
Processing Scale but not with the Simultaneous Processing Scale. More specifically, SLQ
appeared to be significantly related to the sequential subtests Word Order and Number
Recall but not with Hand Movements.
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 Spatial Memory and Hand Movements are also significantly
correlated. In addition, the Hand Movements test is significantly related to both verbal
subtests, indicating that it is not a “pure” measure of spatial working memory. The Hand
Movements 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 KABC, 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 Hand
Movements test. Although Kaufman and Kaufman (1983) presented the Hand Movements
test 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 Hand
Movements 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 Hand Movements test 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. ADHDC children with normal language development, did not perform differently from normal
2
The impact of specific language impairment on working memory
children on verbal and spatial working memory measures. These results emphasize the
importance of screening for language disorders when examining neuropsychological
deficts in ADHD.
3
Chapter three
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CHAPTER FOUR
4
Relationships between
neuropsychological measures of
executive function and behavioural
measures of ADHD symptoms and
comorbid behaviour
Solveig Jonsdottir, Anke Bouma, Joseph A. Sergeant, Erik J.A. Scherder
Archives of Clinical Neuropsychology, in press, available online 28 July 2006
Chapter four
ABSTRACT
Objective: The aim of this study was to examine the relationship 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.
0
Executive functions and ADHD symptoms
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
1
Chapter four
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-year2
Executive functions and ADHD symptoms
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 Tower
and the Visual Attention subtests from the NEPSY and the Number Recall and Word
Order 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).
3
Chapter four
Instruments
The NEPSY: A Developmental Neuropsychological Assessment
The 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 the Visual Attention 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 Tower of London 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
Visual Attention 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.
Kaufman Assessment Battery for Children (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: Number Recall and Word Order 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.
Test of Language Development (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.
Executive functions and ADHD symptoms
The Behavior Assessment System for Children (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 Conduct Problems measure externalizing problems. Three scales called
Anxiety, Depression, and Somatization, assess internalizing problems. Three additional
scales are called Attention Problems, Atypicality and Withdrawal. The Teacher Rating
Scale (TRS) has, in addition to the aforementioned nine scales, a clinical scale called
Learning Problems. 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 almost always = 3).
Internal consistency coefficients (Kjartansdottir, 2002) for the BASC Icelandiclanguage 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.
Statistical analyses
To analyse the group’s deviation from the standardized mean on tests of EF, the KABC 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.
Chapter four
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 Attention Problems 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 Attention Problems 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)
Mean
S.D.
Normal Controls (n=115)
Mean
S.D.
F
df
p
Eta
Age
BASC-TRS
Hyperactivity
Aggression
Conduct Problems
Anxiety
Depression
Somatization
Attention Problems
Learning Problems
Atypicality
Withdrawal
9.27
1.34
9.05
1.65
.65
1,156
.42
.00
14.23
11.87
3.36
6.15
8.56
4.38
14.28
13.33
5.56
7.00
11.14
10.19
3.59
3.81
6.27
4.34
5.29
5.76
4.19
4.36
7.03
7.15
1.68
2.78
3.11
1.83
6.03
5.62
1.28
3.49
7.02
7.88
2.35
3.47
3.88
2.85
4.96
5.10
2.38
3.37
22.24
8.96
11.16
26.20
40.99
17.67
78.07
62.43
62.04
27.14
1,152
1,152
1,152
1,152
1,152
1,152
1,152
1,152
1,152
1,152
.000
.003
.001
.000
.000
.000
.000
.000
.000
.000
.13
.06
.07
.15
.21
.10
.34
.29
.29
.15
BASC-PRS
Hyperactivity
Aggression
Conduct Problems
Anxiety
Depression
Somatization
Atypicality
Withdrawal
Attention Problems
10.00
11.49
4.65
12.09
12.26
7.33
5.51
5.42
12.12
5.44
4.66
3.13
6.13
7.71
5.00
3.86
2.68
3.61
5.70
7.81
2.21
7.67
5.10
4.28
2.36
5.36
5.71
3.84
3.88
2.15
4.50
4.91
3.03
2.25
3.14
3.64
30.79
25.21
31.03
24.57
47.66
21.63
40.40
.01
97.37
1,156
1,156
1,156
1,156
1,156
1,156
1,156
1,156
1,156
.000
.000
.000
.000
.000
.000
.000
.91
.000
.17
.14
.17
.14
.23
.12
.21
.00
.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
Executive functions and ADHD symptoms
Table 2 shows the means and standard deviations for the NEPSY Tower and Visual
Attention 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 Visual Attention
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
Tests of executive function
Tower
Mean
S.D.
t
df
p
7.90
2.61
-5.20
41
.000
Visual Attention
8.90
2.77
-2.51
39
.016
Verbal Working Memory
8.66
2.37
-3.69
42
.001
Kaufman Assessment Battery for Children (K-ABC)
Mental Processing Composite (MPC)
99.88
11.90
-.06
42
ns
Sequential Processing
93.26
12.56
-3.52
42
.001
104.51
11.10
2.67
42
.011
92.05
18.71
-2.69
40
.011
Simultaneous Processing
Test of Language Development (TOLD)
Spoken Language Quotient (SLQ)
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 Tower
test, the Visual Attention test and verbal WM), 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 verbal WM appeared to be significantly
related to Tower. Moreover, the different EF functions were significantly related to all IQ
measures, except the Visual Attention 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).
Chapter four
TABLE 3
Pearson Correlations between tests of executive function, intelligence and language development
EF tests
Tower
Tower
Visual Attention
Verbal WM
1
TOLD
K-ABC
Vis.Att.
V.WM
MPC
Seq.Pr.
Sim.Pr.
SLQ
.04
.42**
.43**
.41**
.36*
.13
.24
.44**
.24
.51**
.31
1
.83**
.95**
.58**
.48**
1
Note: NEPSY, A Developmental Neuropsychological Assessment; 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 Visual Attention test, verbal WM, 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, Attention Problems) 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
Learning Problems and all three EF measures: Tower (r = -.33, p = .04), Visual Attention
(r = -.46, p = .004), and verbal WM (r = -.49, p = .002). Teacher rated Learning Problems
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 Visual Attention test (r = -.37,
p = .03).
The only significant relationship on the PRS was between Conduct Problems and the
Visual Attention test (r = -.32, p = .05).
Executive functions and ADHD symptoms
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
-.29
-.09
-.03
-.02
.14
.05
.01
-.00
.15
.09
-.10
-.07
.11
.17
-.14
-.07
-.37*
-.07
-.14
-.07
-.17
.06
-.07
-.16
-.08
-.19
-.29
-.19
-.17
-.09
-.09
-.06
.01
-.16
-.10
-.09
-.33*
-.08
-.19
-.49**
-.09
-.36*
-.16
-.38*
-.54**
-.67**
BASC-TRS
Hyperactivity
Aggression
Conduct Problems
Anxiety
Depression
Somatization
-.26
-.38*
-.31
-.38*
Learning Problems
-.33*
-.21
-.46**
-.62**
-.19
-.57**
Atypicality
-.43**
-.32
-.04
-.09
-.05
-.11
.04
Withdrawal
-.16
-.16
-.29
-.11
-.21
-.01
-.26
Aggression
-.27
-.18
-.15
-.16
-.23
-.15
-.08
-.07
-.30
-.18
.09
.21
Attention Problems
BASC-PRS
Hyperactivity
Conduct Problems
-.15
-.24
-.17
-.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
Attention Problems
-.06
-.10
.11
.07
-.05
-.25
-.02
-.16
-.06
-.21
.02
-.11
.26
-.22
Note: 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 Atypicality and 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 Visual Attention (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 Conduct Problems were significantly and negatively related to Visual
Chapter four
Attention (r = -.38, p = .02), and Atypicality was significantly and negatively related to
verbal WM (r = -.35, p = .03).
TABLE 5
Pearson correlations between BASC TRS and PRS and tests of executive function controlling for
intelligence
Tower
Visual Attention
Verbal WM¹
Aggression
-.09
-.05
.11
Conduct Problems
-.09
Anxiety
-.04
-.34*
.10
Depression
-.22
-.37*
-.19
-.21
Somatization
-.32
-.17
-.04
Attention Problems
-.28
-.10
.07
Learning Problems
-.09
-.43**
-.25
-.34*
-.15
Atypicality
Withdrawal
-.13
-.15
BASC-TRS
Hyperactivity
.06
.04
-.37*
BASC-PRS
Hyperactivity
Aggression
-.13
-.11
-.15
-.32*
-.13
Conduct Problems
Anxiety
-.14
.05
-.10
Depression
-.27
.06
-.09
Somatization
-.14
-.09
Atypicality
-.04
-.09
.01
-.35*
Withdrawal
Attention Problems
-.04
-.04
.11
.15
-.10
-.26
-.03
Note: NEPSY, A Developmental Neuropsychological Battery; BASC, Behavior Assessment
System for Children; TRS, Teacher Rating Scale, PRS, Parent Rating Scale
¹K-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 Attention Problems 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 Learning Problems. No parent ratings were significantly
predicted by performance on EF tasks.
0
Executive functions and ADHD symptoms
TABLE 6
Stepwise regression analyses for cognitive variables predicting ratings on BASC TRS and PRS
Variable
Unstandardised
Coefficient (B)
t-value
p-value
TRS Depression
Tower
-.89
-2.07
.05
-.12
-2.52
.02
TRS Attention Problems
SLQ
TRS Learning Problems
SLQ
-.13
-2.99
.005
MPC
-.20
-2.97
.006
-.72
-2.73
.01
TRS Atypicality
Tower
F-value
p-value
4.29
.05
6.34
.02
18.62
.000
7.45
.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, Visual Attention, Verbal Working Memory, MPC, and SLQ.
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
1
Chapter four
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
Tower test 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
All three measures of EF were significantly related to IQ, except the Visual Attention
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
retardation, fatigue, or reduced ability to concentrate. Similarly, Goethals et al. (2005)
2
Executive functions and ADHD symptoms
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 Attention Problems 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 Visual Attention 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
are similar to those of previous studies (e.g. Oosterlaan et al., 2005) emphasizing that
3
Chapter four
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.
Executive functions and ADHD symptoms
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0
CHAPTER FIVE
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
Solveig Jonsdottir, Anke Bouma, Joseph A. Sergeant, Erik J.A. Scherder
Neurorehabilitation and Neural Repair, Volume 18, Number 4, December 2004,
Pages 212-221
1
Chapter five
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.
2
TENS therapy in ADHD
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 informationprocessing 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 selfdirected 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,
3
Chapter five
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 sleepwake 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
TENS therapy in ADHD
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.
Chapter five
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 6week 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, Digit Span and Coding from the Wechsler Intelligence Scale
for Children-Revised (WISC-R) (Wechsler, 1974) can be combined into one separate IQ
factor, called Freedom from Distractibility (Kaufman, 1975), also sometimes called the
“Third Factor” (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 Digit Span, 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 BourdonVos 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 Stroop Colour and Word Test, 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 red is 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.
TENS therapy in ADHD
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
Chapter five
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.
Trial treatment. 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.
TENS therapy in ADHD
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, administered before and after a treatment
period of 6 weeks and after a treatment-free period of 6 weeks.
Pre
Neuropsychological Tests
Third factor total score
Arithmetic
Digit Span
Coding
Bourdon-Vos Time (seconds)
Bourdon-Vos Omissions
Stroop Card 3 – Card 2
Post
Delay
M
SD
M
SD
M
SD
85.73
7.23
8.41
7.77
17.92
21.67
96.41
13.20
2.43
3.12
3.53
4.15
30.66
44.60
88.59
7.19
8.59
8.68
16.76
9.24
73.72
13.33
2.08
2.17
3.40
4.83
7.01
30.87
90.53
7.16
9.00
9.58
14.72
7.84
60.44
9.74
2.46
2.56
2.36
3.37
7.76
29.38
Wilcoxon
Pre-Post
Z
P
1.83
0.16
0.65
1.98
2.69
2.37
1.82
0.03
0.44
0.26
0.02
0.004
0.009
0.03
Wilcoxon
Post-Delayed
Z
P
1.22
0.35
1.29
1.15
1.89
0.88
1.60
Behaviour
The Revised Conners Parent and Teacher Rating Scales, Parent version. 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.
The Revised Conners Parent and Teacher Rating Scales, Teacher version. 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
0.22
0.73
0.20
0.25
0.06
0.38
0.11
Chapter five
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).
Table 2. Means, Standard Deviations, and the Wilcoxon Signed Ranks Tests (Z Scores, P Values) with Respect to the Scores on the
Revised Conners Parents & Teacher Rating Scale (Conners), Administered to the Parents and the Teachers, before and after the
Treatment Period of 6 Weeks and after a Treatment-Free Period of 6 Weeks
Pre
Conners
Parents’ version
Total score
Conduct problems I
L earning problems
Psychosomatic problems
Impulsive/ hyperactive
Conduct problems II
Anxiety
Other items
Teachers’ version
Total score
Conduct problems I
L earning problems
Psychosomatic problems
Impulsive/ hyperactive
Conduct problems II
Anxiety
Other items
Post
Delay
Wilcoxon
Pre-Post
Z
P
Wilcoxon
Post-Delayed
Z
P
M
SD
M
SD
M
SD
52.52
11.76
7.38
1.71
7.33
2.52
3.10
19.19
18.44
4.89
1.80
1.59
2.01
1.94
2.57
8.95
39.10
9.20
6.05
1.05
4.90
1.90
2.50
13.60
17.63
4.69
2.24
1.32
2.49
1.68
2.24
8.36
38.74
8.79
6.37
0.84
4.84
1.79
2.47
13.11
16.25
5.13
2.50
1.07
1.83
1.47
1.95
7.28
3.22
2.46
2.14
2.16
3.07
2.28
1.82
3.30
0.0005
0.007
0.02
0.02
0.001
0.01
0.03
0.0005
0.15
0.06
0.09
0.70
0.11
0.32
0.66
0.04
0.88
0.95
0.93
0.48
0.91
0.75
0.51
0.97
42.40
11.15
6.40
0.88
6.50
1.85
2.20
13.50
18.84
5.50
2.78
1.36
3.15
1.35
1.85
7.49
35.75
9.00
5.94
0.47
5.18
1.35
2.76
12.35
14.83
4.49
2.68
0.64
2.74
1.50
2.80
7.32
26.62
6.85
4.62
0.46
4.08
1.46
1.38
7.85
7.90
3.69
1.80
1.21
1.44
1.27
1.66
3.87
1.92
1.54
1.38
0.94
1.32
1.78
0.24
1.08
0.03
0.06
0.08
0.18
0.09
0.04
0.41
0.28
2.29
1.96
1.63
0.58
0.53
0.81
0.11
2.19
0.01
0.03
0.10
0.56
0.59
0.42
0.92
0.01
Table 3. Means, Standard Deviations, and the Wilcoxon Signed Ranks Tests (Z Scores, P Values) with Respect to the ActigraphyVariables, Obtained before and after the Treatment Period of 6 Weeks and after a Treatment-Free Period of 6 Weeks
Pre
Actigraphy
Interdaily stability
Intradaily variability
Relative amplitude
L5
M10
M
Post
SD
M
Delay
SD
M
SD
0.69
0.09
0.62
0.13
0.61
0.15
0.62
0.16
0.70
0.25
0.64
0.14
0.96
0.01
0.97
0.01
0.95
0.04
801
277
595
303
1354
1751
45810 15473
37967
21187
44478
20639
Wilcoxon
Pre-Post
Z
P
1.29
1.29
0.40
2.07
1.45
0.20
0.47
0.35
0.02
0.07
Wilcoxon
Post-Delayed
Z
P
0.47
0.91
1.41
1.66
0.73
L 5 = 5 least active hours; M10 = 10 most active hours.
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
0
0.64
0.36
0.08
0.05
0.47
TENS therapy in ADHD
(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 highfrequency 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 TENStreatment. 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
1
Chapter five
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
2
TENS therapy in ADHD
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 restactivity 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.
3
Chapter five
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CHAPTER SIX
6
Summary and concluding remarks
100
Summary and concluding remarks
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
101
Chapter six
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.
102
Summary and concluding remarks
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
103
Chapter six
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 activity. 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 also may 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.
10
Summary and concluding remarks
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.
10
Chapter six
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10
10
Samenvatting
Dutch translation by Erik J.A. Scherder
10
110
Samenvatting
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:
e) Geslachtsverschillen in ADHD symptomen binnen een normale IJslandse
populatie.
f) De invloed van gerelateerde specifieke taalstoornissen op het werkgeheugen van
kinderen met ADHD Combined Type.
g) De relaties tussen gedrags- en neuropsychologische diagnostiek van ADHD
symptomen.
h) 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
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Samenvatting
jongens hoger scoren op hyperactiviteit en agressie dan normale IJslandse meisjes. De
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
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Samenvatting
hebben minder kans op ‘externalizing’ gedrag dan kinderen met het ‘Combined type’
(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
11
Samenvatting
de beoordeling van aandachtscapaciteit van het kind door de leerkracht. Sommige ADHD
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.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
Onderzoek naar de overeenkomst tussen de beoordelingen van de ouders en de
leerkrachten van ADHD symptomen bij meisjes in een veel grotere steekproef.
Vergelijking van de beoordeling van ADHD door vaders en mannelijke
leerkrachten met de beoordeling van ADHD door moeders en vrouwelijke
leerkrachten.
Onderzoek naar de relatie tussen taalstoornissen en aandachtsstoornissen bij
kinderen met ADHD.
Verder onderzoek naar de relatie tussen executieve disfuncties en symptomen
van autisme en depressie bij kinderen met ADHD.
Verder onderzoek naar de effecten van TENS bij kinderen met ADHD met een
grotere steekproef en een controle groep.
Onderzoek naar het slaappatroon van kinderen met ADHD die worden behandeld
met een stimulant of met TENS.
Onderzoek naar de invloed van slaapstoornissen op ADHD symptomen en
aanverwante stoornissen.
Onderzoek naar de relatie tussen het slaap-waakritme en executieve functies bij
kinderen.
Onderzoek naar de effecten van TENS bij kinderen met slaapstoornissen.
Onderzoek naar de effecten van TENS op de executieve functie ‘planning’ van
kinderen.
Onderzoek naar de effecten van TENS op de REM slaap van kinderen en
volwassenen.
Onderzoek naar de effecten van TENS op het ‘restless legs syndrome/periodic
leg movement disorder’.
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.
11
Samenvatting
REFERENCES
Barkley, R.A. (1998). Attention-deficit hyperactivity disorder: A handbook for diagnosis
and treatment, 2nd ed. New York: Guilford Press.
Brewis, A., & Schmidt, K.L. (2003). Gender variation in the identification of Mexican
children’s psychiatric symptoms. Medical Anthropology Quarterly, 17, 376-393.
Bennett, F.C., Brown, R.T., Craver, J., & Anderson, D. (1999). Stimulant medication for
the child with attention-deficit/hyperactivity disorder. Pediatric Clinics of North
America, 46, 929-944.
Bullock, G.L., & Schall, U. (2005). Dyssomnia in children diagnosed with attention
deficit hyperactivity disorder: A critical review. Australian and New Zealand
Journal of Psychiatry, 39, 373-377.
Chronis, A.M., Jones, H.A., & Raggi, V.L. (2006). Evidence-based psychosocial
treatments for children and adolescents with attention-deficit/hyperactivity
disorder. Clinical Psychology Review (in press).
Dahl R.E. (1996). The impact of inadequate sleep on children’s daytime cognitive
function. Seminars in Pediatric Neurology, 3, 44-50.
El-Ad, B., & Lavie, P. (2005). Effect of sleep apnea on cognition and mood. International
Review of Psychiatry, 17, 277-282.
Faraone, S.V., Sergeant, J., Gillberg, C., & Biederman, J. (2003). The worldwide
prevalence of ADHD: Is it an American condition? World Psychiatry, 2, 104-113.
Havey, J.M., Olson, J.M., McCormick, C., & Cates, G.L. (2005). Teachers’ perceptions of
the incidence and management of attention-deficithyperactivity disorder. Applied
Neuropsychology, 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. Molecular Psychiatry, 10, 939943.
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. Psychiatry and Clinical Neurosciences, 55, 97-103.
Montgomery, J.W. (2003). Working memory and comprehension in children with specific
language impairment: What we know so far. Journal of Communication Disorders,
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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 sleepdisordered breathing in children. Journal of Sleep Research, 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. Journal of
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Clinical Child and Adolescent Psychology, 34, 449-476.
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 of
Abnormal Psychology, 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 and
Adolescent Psychiatry, 43, 1276-1282.
Tsai, S.J. (2003). Attention-deficit hyperactivity disorder and brain-derived neurotrophic
factor: A speculative hypothesis. Medical Hypotheses, 60, 849-851.
Ulloor, J., & Datta, S. (2005). Spatio-temporal activation of cyclic AMP response elementbinding protein, activity-regulated cytoskeletal-associated protein and brainderived nerve growth factor: A mechanism for pontine-wave generator activationdependent two-way active-avoidance memory processing in the rat. Journal of
Neurochemistry, 95, 418-428.
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Samantekt
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Samantekt
SAMANTEKT
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)
b)
c)
d)
kynjamun á ADHD einkennum í heilbrigðu íslensku þýði.
áhrif sértækrar málþroskaröskunar (specific language impairment, SLI) á
vinnsluminni barna, sem eru með samsetta gerð af ADHD.
sambandið á milli hegðunarmats og taugasálfræðilegs mats á ADHD
einkennum.
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 þróa
með sér 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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Samantekt
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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Samantekt
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 séu fordómar 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
hlusta þegar talað er beint til hans/hennar; virðist oft ekki fylgja fyrirmælum og lætur
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Samantekt
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
fyrirferðarmeiri en stúlkur og að þeim sé af þeim sökum frekar vísað í greiningu. Minni
12
Samantekt
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 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 málþroskarökun, 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.
12
Samantekt
REFERENCES
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and treatment, 2nd ed. New York: Guilford Press.
Brewis, A., & Schmidt, K.L. (2003). Gender variation in the identification of Mexican
children’s psychiatric symptoms. Medical Anthropology Quarterly, 17, 376-393.
Bennett, F.C., Brown, R.T., Craver, J., & Anderson, D. (1999). Stimulant medication for
the child with attention-deficit/hyperactivity disorder. Pediatric Clinics of North
America, 46, 929-944.
Bullock, G.L., & Schall, U. (2005). Dyssomnia in children diagnosed with attention
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Chronis, A.M., Jones, H.A., & Raggi, V.L. (2006). Evidence-based psychosocial
treatments for children and adolescents with attention-deficit/hyperactivity
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Dahl R.E. (1996). The impact of inadequate sleep on children’s daytime cognitive
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El-Ad, B., & Lavie, P. (2005). Effect of sleep apnea on cognition and mood. International
Review of Psychiatry, 17, 277-282.
Faraone, S.V., Sergeant, J., Gillberg, C., & Biederman, J. (2003). The worldwide
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Havey, J.M., Olson, J.M., McCormick, C., & Cates, G.L. (2005). Teachers’ perceptions of
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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
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factor (BDNF) gene with susceptibility to ADHD. Molecular Psychiatry, 10, 939943.
Konofal, E., Lecendreux, M., Bouvard, M.P.,& Mouren-Simeoni, M.C. (2001). High
levels of nocturnal activity in children with attention-deficit hyperactivity disorder:
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Montgomery, J.W. (2003). Working memory and comprehension in children with specific
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McClimment, M.C., & Gozal, D. (2004). Neurobehavioral correlates of sleepdisordered breathing in children. Journal of Sleep Research, 13, 165-172.
Pelham, W.E.Jr., Fabiano, G.A., & Massetti, G.M. (2005). Evidence-based assessment
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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
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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 and
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Tsai, S.J. (2003). Attention-deficit hyperactivity disorder and brain-derived neurotrophic
factor: A speculative hypothesis. Medical Hypotheses, 60, 849-851.
Ulloor, J., & Datta, S. (2005). Spatio-temporal activation of cyclic AMP response elementbinding protein, activity-regulated cytoskeletal-associated protein and brainderived nerve growth factor: A mechanism for pontine-wave generator activationdependent two-way active-avoidance memory processing in the rat. Journal of
Neurochemistry, 95, 418-428.
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Words of thanks
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130
Words of thanks
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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Words of thanks
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
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 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 LandspitaliUniversity 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 has worked on her research for the last 6 years,
alongside her work as a clinical neuropsychologist at the Landspitali-University Hospital,
where she is currently working mainly in the Department of Neurology.
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