Attention-Deficit Hyperactivity Disorder, Attention Problems, and Epilepsy



Attention-Deficit Hyperactivity Disorder, Attention Problems, and Epilepsy


David W. Dunn

William G. Kronenberger



Behavior problems and learning disabilities are common problems in children with epilepsy. The more common behavioral problems in children with epilepsy are the disruptive behavioral disorders, depression, and anxiety. In addition, seizures occur frequently in children with autistic disorder. Mental retardation is associated with the symptomatic generalized epilepsies, and learning disabilities are found in as many as half of children with normal intelligence and epilepsy (1). Problems with attention and attention-deficit hyperactivity disorder (ADHD) are particularly important both as a major behavioral problem and as a contributor to the learning difficulties of children with epilepsy. In a meta-analysis of studies of behavioral problems in children with epilepsy, Rodenburg et al. (2) found that attention problems were more specifically related to epilepsy, whereas depression and anxiety were seen almost as often in children with other chronic disorders. In a study of learning disability associated with childhood epilepsy, Williams et al. (3) found that, after controlling for intelligence, academic problems were more often associated with attention problems than with memory disturbance, self-esteem, or socioeconomic status.

In this chapter, we review studies of attention and ADHD in children with epilepsy and discuss risk factors for attention problems in such children. For the ongoing care of children with seizures, we review methods of assessment for attention and benefits and risk of the available treatments for ADHD in children with epilepsy.

The current accepted definition of ADHD is found in the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) (4). The diagnosis of ADHD requires an onset of symptoms before age 7 and evidence of impairment in two or more settings. The DSM-IV lists nine items in the inattentive cluster and nine in the hyperactivity-impulsivity cluster, with six hyperactivity criteria and three impulsivity criteria. Examples of inattentive criteria are distractibility, poor concentration, forgetfulness, poor organization, and difficulty in completing tasks. Hyperactivity is defined
by constant movement, inability to stay seated, excessive talking, and an inability to play quietly. The criteria for impulsivity are interrupting, answering questions before they are finished, and trouble waiting for one’s turn. At least six of the nine criteria for either subtype must be present for at least 6 months in order to make the diagnosis. A diagnosis of ADHD combined type can be made if criteria for both inattention and hyperactivity-impulsivity are met, ADHD predominantly inattentive type if only criteria for inattention are fulfilled, and ADHD predominantly hyperactive-impulsive type if only criteria for hyperactivity-impulsivity are met.

Current theory has begun to consider a deficit in inhibition as the primary problem for children with ADHD combined type. Barkley contends that these children have a defect in behavioral inhibition, limiting their ability to delay a response, interrupt an ongoing behavior, or screen competing stimuli (5). This adversely affects the executive functions of working memory, self-regulation, and analysis and planning, resulting in the behaviors characteristic of ADHD. This theory seems consistent with recent neuroimaging studies showing a difference in prefrontal and striatal regions when comparing individuals with and without ADHD.

Children may have attention problems without meeting criteria for a diagnosis of ADHD. Multiple pathways in the central nervous system are important in attention. Disruptions may lead to impairment in the ability to perceive and select a stimulus for attention, maintain or switch attention, inhibit response to extraneous stimuli, and hold information in mind while proceeding to a goal (6). These types of attention problems may be particularly important in children with epilepsy. Sánchez-Carpintero and Neville (7) recently reviewed studies of attention in children with epilepsy and concluded that these children most consistently have difficulty with sustained attention.


Frequency of Attention-Deficit Hyperactivity Disorder and Attention Problems in Children with Epilepsy

Are attention problems more common in children with epilepsy than in children from the general population? A major difficulty in determining the prevalence of the attention problems or ADHD in epilepsy is the paucity of epidemiological studies, the changing definitions of these disorders, and the variability of measures used to diagnose attention problems. Rutter, Graham, and Yule documented behavioral disorders in 28.6% of children with uncomplicated seizures, and 58.3% of children with both seizures and additional central nervous system dysfunction (8). The hyperkinetic syndrome was more frequent than expected in the children with epilepsy but the numbers (4 of 34 children) were too small to be reliable. McDermott, Mani, and Krishnaswami (9), using a population-based analysis, compared children with seizures and/or cardiac disorders with controls. The children with epilepsy experienced more difficulties than the children with heart disease or the normal controls. Hyperactive behavior was found in 28.1% of the children with epilepsy (cardiac 12.6%; controls 4.9%). Compared with controls, the adjusted odds ratio in children with epilepsy was 7.4 for hyperactivity. Carlton-Ford et al. (10) reviewed the survey data from 11,160 children of ages 6 through 17. Within this sample, there were 32 children with active epilepsy and 86 children with a history of seizures but no episodes in the past year. They found that 11% of the children with no history of seizures and 39% of the children with current or past epilepsy were highly impulsive. Though impulsivity was more common in the group with active epilepsy, there was no statistically significant difference between the active and inactive epilepsy samples. Davies et al. (11) reported results from a
nationwide epidemiological study conducted in England. In their survey of 10,316 children, they found 67 children with epilepsy, of which 42 had uncomplicated epilepsy and 25 had complicated epilepsy. They noted behavioral problems in 56% of the children with complicated epilepsy, 26% of the children with uncomplicated epilepsy, 10.6% of children with diabetes, and 9.3% of controls. They described ADHD in 12% of the children with complicated epilepsy but in none of the children with uncomplicated epilepsy.

The more prominent occurrence of ADHD symptoms in the studies of McDermott et al. (9) and Carlton-Ford et al. (10) as compared with the studies of Rutter et al. (8) and Davies et al. (11) probably reflects the more stringent criteria used in England for the diagnosis of hyperkinetic syndrome or ADHD. The higher prevalence rates reported by McDermott et al. (9) and Carlton-Ford et al. (10) are also likely due to the use of a combination of children with true ADHD and children with symptoms of attention problems and hyperactivity but without ADHD in their study.

Additional information on the prevalence of ADHD and attention problems in children with epilepsy comes from assessments of behavior problems in epilepsy clinic populations. One problem with these studies is a potential referral bias. There is probably a tendency for children with more complicated seizures and children with comorbid behavior disorders to be seen in university-based tertiary clinics. A second problem with many of these studies is the failure to use exact diagnostic criteria or varying measures of the disruptive behavior disorders. Often, symptoms of disruptive behaviors are reported without complete criteria as outlined in the DSM-IV, the broad category of ADHD is not separated into the subtypes of predominantly inattentive, predominantly hyperactive-impulsive, or combined types, and a clear delineation of coexisting conditions is lacking.

We were able to find only five studies that utilized DSM criteria for the diagnosis of ADHD in children with epilepsy. Hempel et al. (12) described ADHD in 40 of 109 (37%) children with epilepsy. They found that the children with intractable generalized seizures had a higher incidence of ADHD. Williams et al. (13) did neuropsychological testing in 79 children with epilepsy. They noted that 11 of the 79 children (14%) had a diagnosis of ADHD. In addition, the children with seizures had significantly lower attention scores on formal testing as compared with controls even when the children with ADHD were excluded from the analysis. Similarly, Semrud-Clikeman and Wical (14) evaluated 33 children with complex partial seizures (CPS) and found that 12 (36%) had ADHD. The diagnosis of ADHD was based on DSM-III-R criteria with additional information from structured interviews with both the parent and the child’s teacher. Semrud-Clikeman and Wical also used a computerized continuous performance test to assess attention and found inattention in children with epilepsy regardless of the prior diagnosis of ADHD. Dunn et al. (15) assessed behavioral problems in children with epilepsy using the Child Behavior Checklist (CBCL) and the Child or Adolescent Symptom Inventory. This latter measure uses DSM-IV criteria for classification, and includes a division of ADHD into combined, inattentive, and hyperactive-impulsive subtypes. They found that 42 of 175 children with epilepsy had symptoms consistent with ADHD predominantly inattentive type, 20 had ADHD combined type, and 4 had ADHD hyperactive-impulsive type. Thome-Souza et al. (16) assessed 55 children with epilepsy. They found evidence of ADHD, from either an interview by a child psychiatrist or a structured interview, in 29.1% of the children.

Several studies have reported symptoms of ADHD in children with epilepsy without reference to DSM criteria. In these clinically derived series, the prevalence of ADHD symptoms has ranged from 8% to 77%, reflecting differences in the sample and in the diagnostic classification of behavioral symptoms. The highest figure comes from the study of Ferrie et al. (17), who noted that at least one symptom of ADHD
was reported by either parent or teacher in 17 of 22 (77%) of children with epileptic encephalopathies, including intractable myoclonic or myoclonic-astatic seizures and the Lennox-Gastaut syndrome. Most had significant cognitive handicaps and therefore would probably be more likely to have major problems with attention. The lower prevalence figure of 8% comes from the early report of Ounsted (18), who described severe overactivity, distractibility, inattention, aggression, mood lability, a lack of shyness, fearlessness, an absence of spontaneous affection, and wide scatter on formal psychological testing in 70 of 830 children with epilepsy. These children had more difficulties than would be currently considered consistent with pure ADHD and probably would be classified as having ADHD with comorbid oppositional defiant disorder (ODD), conduct disorder, or possibly childhood-onset bipolar disorder.

In other studies, the prevalence of ADHD symptoms in children with epilepsy was in the range of 20% to 60%, depending again on the sample and the type of measure used to determine the presence of ADHD. Holdsworth and Whitmore, in a sample of 85 children with epilepsy, found that teachers reported problems with attention in 36 of the 85 (42%) children (19). When Holdsworth and Whitmore divided the children into groups based on school achievement, they noted that inattention was seen in 20% of the children with average to above average school performance and 59% of the children with below average or severely delayed achievement. Hoare and Kerley used the Rutter parent and teacher’s scales to evaluate 108 children with epilepsy (20). The three items of the hyperactive subscale were endorsed as probably abnormal by parents of 21% to 31% of the children with epilepsy and by teachers of 9% to 45% of the children. The teachers reported more inattention and the parents reported more restlessness. Hoare and Mann compared children with epilepsy and children with diabetes mellitus using the CBCL (21). They found that 30% of the children with epilepsy scored in the “at risk” range for attention problems compared with 10% of the children with diabetes. Sturniolo and Galletti gathered the teacher’s impressions of the behavior of 41 children with idiopathic epilepsy (22). The teachers mentioned inattention or hyperactivity in 58% of the children. In the sample described by Harvey et al., parents reported hyperactivity in 14 of 63 (22%) children with new-onset temporal lobe epilepsy (23). None of these studies used DSM criteria, and only Hoare and Kerley and Hoare and Mann used standardized measures of behavior (20,21).

Three additional studies used structured psychiatric interviews to assess the behavior in children with CPS or primary generalized epilepsy (PGE), predominantly childhood absence epilepsy, compared with controls. The authors reported the prevalence of disruptive behavior disorders (ADHD, ODD, conduct disorder) but did not list the rate of ADHD separately. In the first study, Caplan et al. (24) found disruptive behavior disorder, including disruptive behavior disorder with comorbid affective or anxiety disorders, in 39% of the children with CPS and 42% of the children with PGE. Ott et al. (25) reported disruptive behavior disorder in 21% of the children with CPS and 23% of those with PGE and found an additional 19% of the CPS children and 15% of the children with PGE to have comorbid disruptive behavior disorder and affective or anxiety disorder. In a subsequent study, Caplan et al. (26) noted disruptive behavior disorder in 17% and comorbid disorders in 23% of children with CPS compared with disruptive behavior disorder in 6% and comorbid disorder in 3% of controls.

Are ADHD and attention problems more prevalent in children with epilepsy? Comparative prevalence figures for the general population indicate that 3% to 5% of school-age children have ADHD (4). From the studies reviewed, we conclude that children with epilepsy do have an increased risk of ADHD and attention problems. Although the prevalence figures vary by population and definition of ADHD, we estimate that one third of children with epilepsy are at risk for ADHD. They may be at particular risk for the inattentive form of ADHD.



Risk Factors and Etiologies

Assuming the child with epilepsy is at risk for ADHD and may have higher attention difficulties, how does one determine which child is at increased risk? Because of limited resources, it may be difficult to screen all children with epilepsy for behavioral disturbances. Ideally, the subgroup of children with epilepsy more likely to have attention problems should receive a screening assessment or, at least, closer monitoring of academic progress.

A number of risk factors have been determined for behavioral disorders in children with epilepsy. Risk factors may include demographic variables, central nervous system function, seizure type and syndrome, antiepileptic drugs (AEDs), and psychosocial effects of seizures on the child and family (1). Current research in ADHD suggests a combination of genetic and neurophysiological factors in the causation of ADHD. Central nervous system damage, toxins such as lead, and medications less frequently contribute to the etiology of ADHD. Theories of social causation of ADHD have mostly been discredited (27).

Gender is a potential risk factor, as studies of children from the general population have consistently shown that ADHD is more common in boys (4,27). In children with epilepsy, the data is inconsistent. Stores et al. have shown that boys, but not girls, with epilepsy fare worse than controls in measures of attention (28). Ounsted noted that boys with seizures were more likely to have hyperkinetic syndrome (18). Dunn et al. found no statistically significant difference by gender in ADHD in children with epilepsy (15).

The combination of seizures and central nervous system damage appears to be associated with an increased risk of behavioral problems (8,26,29). Two studies reported a low prevalence of ADHD in children with both seizures and brain damage. Steffenburg et al. found ADHD in 7% of children with epilepsy and mental retardation (30). Riikonen and Amnell noted hyperkinetic behavior in 29 of 192 (15%) children who had experienced infantile spasms. All the children in this sample were mentally handicapped (31). The relatively low number of children with disruptive disorders in these two studies may be explained by the high prevalence of autistic disorder, which usually precludes a diagnosis of ADHD. Ferrie et al. did not exclude children with mental retardation and impaired adaptive behavior and found symptoms of ADHD in 77% of children with an epileptic encephalopathy (17).

Seizure type or seizure syndrome is often considered a potential risk factor for behavioral problems in children with epilepsy. However, there has not been a consistent association between these potential risk factors and attention problems or ADHD. In five reports, there was no effect of seizure type on ADHD or inattention (10,13,15,32,33). Hempel et al. (12) found that children with generalized seizures had an increased prevalence of ADHD compared with those with focal seizures. Piccirilli et al. found that children with benign focal epilepsy of childhood had impairment of attention if there was a right-sided epileptic focus, but had normal attention if the focus was left sided (34).

The degree of seizure control may be a factor in behavioral problems. Hermann, Whitman, and Dell found that poor control of seizures was associated with hyperactivity in girls with epilepsy, and poor control was associated with aggression and delinquency in both boys and girls (35). Inattention was a prominent factor in children with epileptic encephalopathy, a seizure type that is usually intractable (17).

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Aug 28, 2016 | Posted by in PSYCHIATRY | Comments Off on Attention-Deficit Hyperactivity Disorder, Attention Problems, and Epilepsy

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