J Dev Phys Disabil (2008) 20:11–20 DOI 10.1007/s10882-007-9075-3 O R I G I N A L A RT I C L E

The Neuropsychological and Neurobehavioral Consequences of ADHD Comorbid with LD and Otitis Media Ilean Padolsky

Published online: 9 June 2007 # Springer Science + Business Media, LLC 2007

Abstract The purpose of this study was to identify a possible subtype of attention deficit hyperactivity disorder (ADHD) comorbid with learning disabilities (LD) and otitis media (OM). Data collected from children with ADHD, LD and otitis media included: Wechsler Intelligence Scale for Children—III, Intermediate Visual and Auditory continuous performance test, neurobehavioral rating, neuropsychological testing, neurophysiological function, and school grades. Findings included deficits in: auditory processing, interpersonal relations, increased social stress, external locus of control, and academic impairment. Parents rated ADHD as mild despite high theta to beta ratios along with neuropsychological dysfunction. Increased severity of ADHD and LD was associated with OM. There may be a unique ADHD subtype with phonological processing deficits. Implications for auditory vs. visual information transmission are discussed. Keywords Attention deficit hyperactivity disorder . Learning disabilities . Otitis media . Neuropsychological . Neurobehavioral Attention deficit hyperactivity disorder (ADHD) is characterized by pervasive inattention, developmentally inappropriate levels of hyperactivity and impulsivity with onset prior to age seven. ADHD is associated with deficits in social, academic, and/or occupational functioning (APA 2000; Center for Disease Control; CDC 2003). Learning disabilities (LD) can be defined as achievement below expected levels in reading, mathematics, or written expression (APA 2000). Research reported The data collected was obtained from the author’s dissertation completed at The Union Institute & University. I. Padolsky The Union Institute & University, Cincinnati, OH, USA I. Padolsky (*) 3901 Nostrand Avenue, Brooklyn, NY 11235, USA e-mail: [email protected]

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by Pliska (2000), describing the patterns of psychiatric comorbidity with ADHD, indicated that there are approximately 20 to 25% of children with ADHD who meet the criteria for LD. Dyslexia or specific reading disability is a disorder within the language system which impairs phonological processing. Functional magnetic resonance imaging (fMRI) studies have provided evidence of disruption in the parieto-temporal and occipito-temporal posterior brain systems associated with reading disability (Shaywitz and Shaywitz 2005). Lazar and Frank (1998) found that frontal system dysfunction was evident in children with ADHD and LD. The findings indicated a strong connection between information processing and executive function systems. Willcutt et al. (2001) conducted research comparing the cognitive deficits in reading disability (RD) and ADHD. The results indicated that ADHD was associated with inhibition deficits and RD was linked to significant impairment in phonemic awareness and verbal working memory. Children with ADHD comorbid with RD were impaired on all three measures. Processing speed (PS) deficits have also been observed in ADHD and reading disability. PS deficit is a shared cognitive risk factor which may be linked to the comorbidity of these two conditions (Shanahan et al. 2006). Mayes et al. (2000) reported that LD co-occurred in 70% of children with ADHD in a diagnostic clinic. The children with LD comorbid with ADHD had more severe learning problems than the group with LD alone. There appears to be a continuum of learning and attention disorders in which these conditions are interrelated and frequently comorbid. In 2003, the findings of a national health survey indicated that the prevalence of ADHD or LD among US children (aged 5–17 years) was approximately 16% in boys and 8% in girls (Center for Disease Control 2003). Other researchers have also linked otitis media or middle ear infection to ADHD and LD (Adesman et al. 1990; Golz et al. 2005, 2006; Winskel 2006). Acute otitis media is defined as the abrupt onset of middle-ear inflammation and effusion (American Academy of Family Physicians 2004). Otitis media (OM) is common during the first three years of life when speech and language categories are formed. In research assessing children with and without OM, children with OM had lower scores on measures of phonological awareness, rhyme and non-word reading, semantic skills of expressive vocabulary, word definitions, and reading. An early history of middle ear infection can be associated with deficits in language and literacy development (Winskel 2006). In a study of children with ADHD or LD, children with ADHD had significantly more middle ear infections. The findings indicated that OM can co-occur with ADHD (Adesman et al. 1990). The current research will explore a subtype of ADHD co-occurring with otitis media. The association between ADHD, otitis media, and LD has not been widely recognized. Therefore, OM may be overlooked by clinicians as a factor linked to auditory processing deficits exacerbating ADHD comorbid with LD. This research points to the need for early diagnosis and treatment of OM to reduce or alleviate auditory processing deficits associated with ADHD and LD. The intent of this preliminary initial research was to identify a possible subtype of ADHD in terms of a neuropsychological, neurophysiological, and neurobehavioral profile within school-aged children as reflected by multiple assessments across functional domains.

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Materials and Methods Participants Three subjects (two males/one female; all Caucasian) ranging in age from 8 to 12 years participated in this study. Each child was referred by his/her pediatrician or neurologist to the Behavioral Medicine & Biofeedback Clinic for evaluation of attention deficit hyperactivity disorder and learning disabilities. All children had a history of recurrent middle ear infection or otitis media. Procedures were explained and informed consent was obtained from parents prior to their children’s participation in the study. Data were collected including: the Wechsler Intelligence Scale for Children—III IQ (WISC-III) and subtest scores, Intermediate Visual and Auditory (IVA) continuous performance test, parent rating of behavior, child report of personality, neuropsychological testing, theta, beta, SMR (sensorimotor), and EMG (electromyographic) amplitudes, and school grades. Materials All neuropsychological and neurobehavioral assessments were converted to z-scores to provide a common metric for comparison of test scores across subjects. A z-score distribution table was utilized for conversion of standard scores, scaled scores and t scores. Therefore, z-scores above zero were interpreted as elevated, while those below zero represented below age norms. The Wechsler Intelligence Scale for Children—Third Edition (WISC-III; Wechsler 1991) was developed for assessment of children aged 6 years through 16 years–11 months. The three indices include: verbal, performance, and full scale IQ. Each index has a mean of 100 and a standard deviation of 15. The average reliability coefficient of WISC-III subtests range from 0.69 to 0.87 (Wechsler 1991; Spreen and Strauss 1998). The Intermediate Visual and Auditory continuous performance test (IVA; Sandford and Turner 1995) is designed to assess response control, visual as well as auditory sustained attention in individuals age 5 years though adult. Computer scoring of the IVA includes: errors of commission, errors of omission, consistency of response times, variability of response time, and mean correct response time. Seckler et al. (1995) reported test–retest correlations ranging from 0.37 to 0.75. Subscale scores had significant positive relationships and correlations ranging from 0.46 to 0.88. A Developmental Neuropsychological Assessment (NEPSY; Korkman et al. 1998) evaluates neuropsychological function in children aged 3–12 years in five domains: attention/executive, language/communication, sensorimotor/visuospatial, and learning/memory. Reliabilities ranged from 0.59 to 0.83 for core domain scores in children aged 5–12 years. Correlations with the Wechsler Intelligence Scale for Children—III ranged from 0.33 to 0.70 for the NEPSY administered to an ADHD sample (Korkman et al. 1998). Neurophysiological measurement was obtained utilizing CapScan equipment (CapScan Corporation 1994). Five isolation amplifiers performed isolation, amplification, low frequency bandlimiting, and antialias high frequency bandlimiting of signals to permit multi-channel data acquisition and processing. Amplifier noise

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level and input impedance were appropriate for handling low level EEG and EMG signals. Electrode placement was at Cz or the central vertex site. Silver cup electrodes were utilized to ensure that the most accurate recording may be obtained. S. Othmer (personal communication, July 2000) explained that the crucial areas impacted at the Cz sensor site were “attention, arousal, and affect.” The Attention-Deficit/Hyperactivity Disorder Test (ADHDT; Gilliam 1995) is a rating scale administered to parents to obtain levels of inattention, hyperactivity, and impulsivity in individuals aged 3 to 23 years. Coefficient alphas for all subtests are above 0.90. Correlations with the Attention Deficit Disorders Evaluation Scale— School Version were 0.57 to 0.88. The Self Report of Personality (SRP) of the Behavior Assessment System for Children (BASC; Reynolds and Kamphaus 1992) is a behavioral inventory designed to assess children aged 8–18 years. The SRP screens for the presence of anxiety, depression, locus of control, sense of inadequacy and atypicality; attitude toward teachers and school; relations with parents, interpersonal relations, self-esteem, and self-reliance. Test–retest reliabilities average 0.76 at each age level. Validity was studied in terms of factor analyses yielding a three factor solution including: (1) social maladjustment; (2) clinical maladjustment; and (3) personal adjustment. Academic grades were obtained from records released by the school with the consent of parents.

Results The findings are divided into tables representing four key domains for subjects 1–3: (1) neuropsychological measures of auditory information processing; (2) brainwave and electromyographic activity in microvolts; (3) academic assessment; and (4) neurobehavioral measures. As shown in Fig. 1 in the Appendix, there is a pattern of below age level auditory processing across all three subjects in the following domains: phonemic analysis (NEPSY phonological processing), ability to understand and follow directions of increasing complexity (NEPSY comprehension of directions), auditory recall of sentences of increasing length (NEPSY sentence repetition), and speed of auditory information processing (IVA auditory speed). Gaps in information acquisition (WISC-III Information) were observed in subjects 2 and 3, however not in subject 1. Subjects 2 and 3 both had recurrent otitis media throughout childhood until the present. However, subject 1 had recurrent otitis media only between 3 and 5 years of age. In Fig. 2 in the Appendix, theta to beta ratios ranged from 4.93:1 to 5.90:1 for subject 1 and 2 while theta to SMR ratios were 4.57:1 for subject 3. EMG (electromyographic) activity, reflecting physical effort utilized in shifting production of slow to fast wave activity, was equivalent to the amplitudes of beta and SMR. In Fig. 3 in the Appendix, the range of academic subjects passed was three out of six for all participants indicating impairment in this domain. Figure 4 in the Appendix illustrates the mild levels of hyperactivity, impulsivity, and inattention attributed to children by their parents (ADHDT) which do not coincide

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with the neuropsychological and neurophysiological findings indicating below age level auditory information processing skills and attentional deficits accompanied by excessive theta levels. In the child self report ratings (SRP) a pattern of deficits in interpersonal relations, increased external locus of control, and social stress emerged.

Discussion The results of the current research suggest that there may be a unique subtype of ADHD comorbid with otitis media and LD. The findings indicated a pattern of deficits in auditory information processing and auditory recall, impaired interpersonal relations, increased social stress, external locus of control, as well as academic deficits associated with ADHD comorbid with LD and otitis media. Parents had a tendency to rate levels of inattention, hyperactivity, and impulsivity as mild despite high theta to beta ratios along with neuropsychological dysfunction. The dichotomy in the actual function across domains and parent rating of the severity of symptomatology suggests a tendency to underestimate the impact of the disorder. Distinct neurophysiological subtypes of ADHD and LD have been reported by other researchers (Chabot et al. 2001). Subtypes may include: frontal theta hypercoherence; deficits in theta, alpha, and beta absolute power; frontal alpha incoherence; central alpha incoherence; and frontal, central, and temporal power asymmetry. In 80% of children with attention disorders, QEEG anomalies may be present (Chabot et al. 2001). A neurophysiological signature has been proposed (Chabot et al. 2001; Monastra et al. 2005; White et al. 2005) which focuses on theta/ beta ratios as reflected by an excessive level of theta and low levels of beta or SMR. Although researchers have investigated neurophysiological subtypes of ADHD, previous research has not identified a subtype of ADHD comorbid with LD and otitis media characterized by deficits in phonological processing. Shanahan et al. (2006) provided evidence that processing speed deficits are evident in both ADHD as well as reading disabilities (RD). Processing speed deficits may be a cognitive risk factor explaining the comorbidity of these two disorders. In another study, phonological processing impairment was found to differentiate ADHD and reading disability. Both groups had deficits on measures of inhibitory control (Purvis and Tannock 2000). Mayes et al. (2000) found that learning and attention problems frequently co-occur, are interrelated, and exist on a continuum. Willcutt et al. (2001) reported that ADHD was associated with inhibition deficits and RD was linked to significant impairment in phonemic awareness and verbal working memory. Children with ADHD comorbid with RD were impaired on all three measures. These findings provide further support for the neuropsychological and neuropshysiological patterns of disregulation and academic impairment as reported in the current initial research. Deficits in phonological processing, acquisition of verbal information, and speed of auditory information processing may also be linked to otitis media (OM). The findings of a national survey indicated an increased prevalence of early onset OM and repeated OM between 1988 and 1994 among US preschool children. During this

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period, rates of early onset OM and repeated OM corresponded to increases of 561,000 and 720,000, respectively (Auinger et al. 2003). In a study comparing the history of OM in children with LD and children with ADHD, children with ADHD had significantly more middle ear infections. The findings indicated that OM can cooccur with ADHD (Adesman et al. 1990). As shown in the current research, early onset and recurrent OM can exacerbate the severity of ADHD in terms of auditory information processing speed. Recurrent OM may be a factor in the etiology of language-based learning disability and dyslexia. OM may also contribute to increased severity of LD symptomatology. In the current research, children had patterns of deficits in phonological processing, verbal auditory recall, and following verbal directions. There is a need for early diagnosis and treatment of OM to prevent or alleviate these deficits. Corbeel (2007) noted that the high recurrence rate of OM is associated with eustachian tube dysfunction and immaturity of the immune system in early childhood. When OM is untreated, it can be associated with hearing loss and deafness. Therefore, early identification and treatment of OM is essential. Kataria et al. (1992) reported that children with ADHD comorbid with LD had deficits in auditory ordered recall. The findings indicated that the most information was lost during auditory conditions in contrast to visual presentation. These results have implications for learning styles in ADHD comorbid with LD and otitis media in terms of auditory vs. visual presentation of information. Winskel (2006) described otitis media as a middle ear infection common in the first 3 years of childhood when speech and language categories are developed. Early history of middle ear infection can have an impact on children’s language and literacy development (Winskel 2006). Golz et al. (2005) reported that children with recurrent or prolonged middle ear infections in the first five years of life were at greater risk for delayed reading than age matched controls. In a follow-up study, the findings indicated that reading continued to be impaired among children who had otitis media in later school years (Golz et al. 2006). Balbani and Montovani (2003) found that the consequences of otitis media include phonetic and articulation problems in addition to impaired reading comprehension. In a study of 8 year-old children with a history of repetitive ear infections, a significant decrease was noted on tasks of phonological processing in contrast to controls (Majerus et al. 2005). The aforementioned findings are in accord with the current research including: impaired speed of auditory information processing, deficits in phonemic analysis, and impaired ability to follow directions of increasing syntactic complexity. The gaps in information acquisition occurring in subjects 2 and 3 with recurrent middle ear infections were also observed in other research. In a dichotic listening study, Asbjornsen et al. (2000) found that children with persistent middle ear infections had lasting auditory attention impairment. In the current study, the gaps in information acquisition during intermittent periods of hearing loss were associated with recurrent ear infection. When otitis media is not addressed as a chronic problem rather than a series of acute episodes, ear infection can be an exacerbating factor in LD. Early diagnosis and intervention could alleviate the severity of LD.

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Crawford et al. (2006) reported that children with ADHD in addition to two or more comorbid disorders had increased prevalence of behavior and cognitive deficits as well as impairment in daily functioning. Sprouse et al. 1998 reported that children with ADHD comorbid with LD were rated as less socially perceptive than controls. These findings confirm the results of the current study indicating that children with ADHD comorbid with LD and otitis media had increased social stress and deficits in interpersonal relations as well as academic impairment. As a result, they had an external locus of control associated with a tendency to attribute successes and failures to forces beyond their control. In addition, there was a tendency to project problems onto peers, parents, and teachers. Parents who underestimate the severity of ADHD symptomatology may also have unrealistic expectations for their children’s cognitive, academic, and psychosocial function. In the current study, the findings suggest a unique subtype of ADHD comorbid with LD and otitis media. Future research is suggested with increased sample sizes to confirm these findings. In addition, the learning styles of ADHD children with cooccurring OM and LD can be assessed contrasting visual and auditory presentation of information. It is also suggested that future research utilizing larger sample sizes evaluate the relationship between parental ratings of the severity of ADHD symptomatology, psychosocial function, and the locus of control in childhood ADHD with comorbid disorders. The apparent prevalence of OM in children with ADHD highlights the need for clinicians to recognize a possible subtype of ADHD. ADHD comorbid with otitis media can exacerbate LD. Deficits in auditory processing have an impact on the transmission and acquisition of information. Gaps in acquired information may be the result of impaired auditory processing. Therefore, information transmitted primarily in an auditory modality may place children with this subtype of ADHD at a disadvantage.

Appendix

Fig. 1 Measures of auditory processing (z-scores)

3 2

Phonological Processing

1

Comprehen. of Instruction

0

Sentence Repetition

-1

IVA Auditory Speed

-2 -3 1

2

3

WISC-III Information

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Fig. 2 Theta, beta/SMR, and EMG amplitudes in microvolts

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24.00 22.00 20.00 18.00 16.00 14.00 12.00 10.00 8.00 6.00 4.00 2.00 0.00

Theta Amplitude Beta/SMR Amplitude EMG Amplitude

1

Fig. 3 Number of academic subjects passed

2

3

6.00 5.00 4.00

Academic Subjects Passed

3.00 2.00 1.00 0.00 1

Fig. 4 ADHDT parent ratings of inattention and child self report of personality ratings (z-scores). Hyp=hyperactivity; Imp.=impulsivity; Inat.=inattention; Interp.=interpersonal relations; LC=locus of control; S.Stress=social stress

2

3

3.00 2.00

ADHDT Hyp.

1.00

ADHDT Imp. ADHDT Inat.

0.00

SRP Interp.

-1.00

SRP LC.

-2.00

SRP S.Stress

-3.00 1

2

3

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