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ORIGINAL ARTICLE 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 ChildrenIII, 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 informa- tion 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 J Dev Phys Disabil (2008) 20:1120 DOI 10.1007/s10882-007-9075-3 The data collected was obtained from the authors 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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ORIGINAL ARTICLE

The Neuropsychological and NeurobehavioralConsequences of ADHD Comorbid with LDand 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 attentiondeficit hyperactivity disorder (ADHD) comorbid with learning disabilities (LD) andotitis media (OM). Data collected from children with ADHD, LD and otitis mediaincluded: Wechsler Intelligence Scale for Children—III, Intermediate Visual andAuditory continuous performance test, neurobehavioral rating, neuropsychologicaltesting, neurophysiological function, and school grades. Findings included deficitsin: auditory processing, interpersonal relations, increased social stress, external locusof control, and academic impairment. Parents rated ADHD as mild despite high thetato beta ratios along with neuropsychological dysfunction. Increased severity ofADHD and LD was associated with OM. There may be a unique ADHD subtypewith phonological processing deficits. Implications for auditory vs. visual informa-tion transmission are discussed.

Keywords Attention deficit hyperactivity disorder . Learning disabilities .

Otitis media . Neuropsychological . Neurobehavioral

Attention deficit hyperactivity disorder (ADHD) is characterized by pervasiveinattention, developmentally inappropriate levels of hyperactivity and impulsivitywith onset prior to age seven. ADHD is associated with deficits in social, academic,and/or occupational functioning (APA 2000; Center for Disease Control; CDC2003). Learning disabilities (LD) can be defined as achievement below expectedlevels in reading, mathematics, or written expression (APA 2000). Research reported

J Dev Phys Disabil (2008) 20:11–20DOI 10.1007/s10882-007-9075-3

The data collected was obtained from the author’s dissertation completed at The Union Institute &University.

I. PadolskyThe Union Institute & University,Cincinnati, OH, USA

I. Padolsky (*)3901 Nostrand Avenue, Brooklyn, NY 11235, USAe-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 meetthe criteria for LD.

Dyslexia or specific reading disability is a disorder within the language systemwhich impairs phonological processing. Functional magnetic resonance imaging(fMRI) studies have provided evidence of disruption in the parieto-temporal andoccipito-temporal posterior brain systems associated with reading disability(Shaywitz and Shaywitz 2005). Lazar and Frank (1998) found that frontal systemdysfunction was evident in children with ADHD and LD. The findings indicated astrong connection between information processing and executive function systems.

Willcutt et al. (2001) conducted research comparing the cognitive deficits in readingdisability (RD) and ADHD. The results indicated that ADHD was associated withinhibition deficits and RD was linked to significant impairment in phonemic awarenessand verbal working memory. Children with ADHD comorbid with RD were impairedon all three measures. Processing speed (PS) deficits have also been observed in ADHDand reading disability. PS deficit is a shared cognitive risk factor which may be linked tothe comorbidity of these two conditions (Shanahan et al. 2006).

Mayes et al. (2000) reported that LD co-occurred in 70% of children with ADHDin a diagnostic clinic. The children with LD comorbid with ADHD had more severelearning problems than the group with LD alone. There appears to be a continuum oflearning and attention disorders in which these conditions are interrelated andfrequently comorbid.

In 2003, the findings of a national health survey indicated that the prevalence ofADHD or LD among US children (aged 5–17 years) was approximately 16% inboys and 8% in girls (Center for Disease Control 2003). Other researchers have alsolinked 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 abruptonset of middle-ear inflammation and effusion (American Academy of FamilyPhysicians 2004).

Otitis media (OM) is common during the first three years of life when speech andlanguage categories are formed. In research assessing children with and without OM,children with OM had lower scores on measures of phonological awareness, rhymeand non-word reading, semantic skills of expressive vocabulary, word definitions,and reading. An early history of middle ear infection can be associated with deficitsin language and literacy development (Winskel 2006).

In a study of children with ADHD or LD, children with ADHD had significantlymore middle ear infections. The findings indicated that OM can co-occur withADHD (Adesman et al. 1990). The current research will explore a subtype ofADHD co-occurring with otitis media. The association between ADHD, otitismedia, and LD has not been widely recognized. Therefore, OMmay be overlooked byclinicians as a factor linked to auditory processing deficits exacerbating ADHDcomorbid with LD. This research points to the need for early diagnosis and treatment ofOM 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 ofADHD in terms of a neuropsychological, neurophysiological, and neurobehavioralprofile within school-aged children as reflected by multiple assessments acrossfunctional domains.

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Materials and Methods

Participants

Three subjects (two males/one female; all Caucasian) ranging in age from 8 to 12years participated in this study. Each child was referred by his/her pediatrician orneurologist to the Behavioral Medicine & Biofeedback Clinic for evaluation ofattention deficit hyperactivity disorder and learning disabilities. All children had ahistory of recurrent middle ear infection or otitis media. Procedures were explainedand informed consent was obtained from parents prior to their children’sparticipation in the study. Data were collected including: the Wechsler IntelligenceScale for Children—III IQ (WISC-III) and subtest scores, Intermediate Visual andAuditory (IVA) continuous performance test, parent rating of behavior, child reportof personality, neuropsychological testing, theta, beta, SMR (sensorimotor), andEMG (electromyographic) amplitudes, and school grades.

Materials

All neuropsychological and neurobehavioral assessments were converted to z-scoresto provide a common metric for comparison of test scores across subjects. A z-scoredistribution table was utilized for conversion of standard scores, scaled scores and tscores. Therefore, z-scores above zero were interpreted as elevated, while thosebelow 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 16years–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 reliabilitycoefficient of WISC-III subtests range from 0.69 to 0.87 (Wechsler 1991; Spreen andStrauss 1998).

The Intermediate Visual and Auditory continuous performance test (IVA;Sandford and Turner 1995) is designed to assess response control, visual as wellas auditory sustained attention in individuals age 5 years though adult. Computerscoring of the IVA includes: errors of commission, errors of omission, consistency ofresponse times, variability of response time, and mean correct response time. Seckleret al. (1995) reported test–retest correlations ranging from 0.37 to 0.75. Subscalescores 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 fivedomains: attention/executive, language/communication, sensorimotor/visuospatial,and learning/memory. Reliabilities ranged from 0.59 to 0.83 for core domain scoresin children aged 5–12 years. Correlations with the Wechsler Intelligence Scale forChildren—III ranged from 0.33 to 0.70 for the NEPSY administered to an ADHDsample (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 bandlimitingof 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 EMGsignals. Electrode placement was at Cz or the central vertex site. Silver cupelectrodes were utilized to ensure that the most accurate recording may be obtained.S. Othmer (personal communication, July 2000) explained that the crucial areasimpacted at the Cz sensor site were “attention, arousal, and affect.”

The Attention-Deficit/Hyperactivity Disorder Test (ADHDT; Gilliam 1995) is arating scale administered to parents to obtain levels of inattention, hyperactivity, andimpulsivity in individuals aged 3 to 23 years. Coefficient alphas for all subtests areabove 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 forChildren (BASC; Reynolds and Kamphaus 1992) is a behavioral inventory designedto assess children aged 8–18 years. The SRP screens for the presence of anxiety,depression, locus of control, sense of inadequacy and atypicality; attitude towardteachers and school; relations with parents, interpersonal relations, self-esteem, andself-reliance. Test–retest reliabilities average 0.76 at each age level. Validity wasstudied 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 theconsent 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) brainwaveand 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 auditoryprocessing across all three subjects in the following domains: phonemic analysis(NEPSY phonological processing), ability to understand and follow directions ofincreasing complexity (NEPSY comprehension of directions), auditory recall ofsentences of increasing length (NEPSY sentence repetition), and speed of auditoryinformation 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 thepresent. However, subject 1 had recurrent otitis media only between 3 and 5 years ofage.

In Fig. 2 in the Appendix, theta to beta ratios ranged from 4.93:1 to 5.90:1 forsubject 1 and 2 while theta to SMR ratios were 4.57:1 for subject 3. EMG(electromyographic) activity, reflecting physical effort utilized in shifting productionof 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 ofsix for all participants indicating impairment in this domain.

Figure 4 in the Appendix illustrates the mild levels of hyperactivity, impulsivity, andinattention attributed to children by their parents (ADHDT) which do not coincide

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with the neuropsychological and neurophysiological findings indicating below agelevel auditory information processing skills and attentional deficits accompanied byexcessive theta levels. In the child self report ratings (SRP) a pattern of deficits ininterpersonal 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 ofADHD comorbid with otitis media and LD. The findings indicated a pattern ofdeficits in auditory information processing and auditory recall, impaired interper-sonal relations, increased social stress, external locus of control, as well as academicdeficits associated with ADHD comorbid with LD and otitis media. Parents had atendency to rate levels of inattention, hyperactivity, and impulsivity as mild despitehigh theta to beta ratios along with neuropsychological dysfunction.

The dichotomy in the actual function across domains and parent rating of theseverity of symptomatology suggests a tendency to underestimate the impact of thedisorder.

Distinct neurophysiological subtypes of ADHD and LD have been reported byother researchers (Chabot et al. 2001). Subtypes may include: frontal thetahypercoherence; deficits in theta, alpha, and beta absolute power; frontal alphaincoherence; central alpha incoherence; and frontal, central, and temporal powerasymmetry. In 80% of children with attention disorders, QEEG anomalies may bepresent (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 andotitis media characterized by deficits in phonological processing.

Shanahan et al. (2006) provided evidence that processing speed deficits areevident in both ADHD as well as reading disabilities (RD). Processing speed deficitsmay be a cognitive risk factor explaining the comorbidity of these two disorders. Inanother study, phonological processing impairment was found to differentiateADHD and reading disability. Both groups had deficits on measures of inhibitorycontrol (Purvis and Tannock 2000). Mayes et al. (2000) found that learning andattention problems frequently co-occur, are interrelated, and exist on a continuum.Willcutt et al. (2001) reported that ADHD was associated with inhibition deficits andRD was linked to significant impairment in phonemic awareness and verbal workingmemory. Children with ADHD comorbid with RD were impaired on all threemeasures. These findings provide further support for the neuropsychological andneuropshysiological patterns of disregulation and academic impairment as reportedin the current initial research.

Deficits in phonological processing, acquisition of verbal information, and speedof auditory information processing may also be linked to otitis media (OM). Thefindings of a national survey indicated an increased prevalence of early onset OMand 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 of561,000 and 720,000, respectively (Auinger et al. 2003). In a study comparing thehistory of OM in children with LD and children with ADHD, children with ADHDhad significantly more middle ear infections. The findings indicated that OM can co-occur with ADHD (Adesman et al. 1990).

As shown in the current research, early onset and recurrent OM can exacerbatethe severity of ADHD in terms of auditory information processing speed. RecurrentOM may be a factor in the etiology of language-based learning disability anddyslexia. OM may also contribute to increased severity of LD symptomatology. Inthe current research, children had patterns of deficits in phonological processing,verbal auditory recall, and following verbal directions. There is a need for earlydiagnosis and treatment of OM to prevent or alleviate these deficits.

Corbeel (2007) noted that the high recurrence rate of OM is associated witheustachian 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 thatchildren with ADHD comorbid with LD had deficits in auditory ordered recall. Thefindings indicated that the most information was lost during auditory conditions incontrast to visual presentation. These results have implications for learning styles inADHD comorbid with LD and otitis media in terms of auditory vs. visual presentationof information.

Winskel (2006) described otitis media as a middle ear infection common in thefirst 3 years of childhood when speech and language categories are developed. Earlyhistory of middle ear infection can have an impact on children’s language andliteracy development (Winskel 2006). Golz et al. (2005) reported that children withrecurrent or prolonged middle ear infections in the first five years of life were atgreater risk for delayed reading than age matched controls. In a follow-up study, thefindings indicated that reading continued to be impaired among children who hadotitis media in later school years (Golz et al. 2006).

Balbani and Montovani (2003) found that the consequences of otitis mediainclude phonetic and articulation problems in addition to impaired readingcomprehension. In a study of 8 year-old children with a history of repetitive earinfections, a significant decrease was noted on tasks of phonological processing incontrast to controls (Majerus et al. 2005). The aforementioned findings are in accordwith the current research including: impaired speed of auditory informationprocessing, deficits in phonemic analysis, and impaired ability to follow directionsof increasing syntactic complexity. The gaps in information acquisition occurring insubjects 2 and 3 with recurrent middle ear infections were also observed in otherresearch. In a dichotic listening study, Asbjornsen et al. (2000) found that childrenwith persistent middle ear infections had lasting auditory attention impairment. Inthe current study, the gaps in information acquisition during intermittent periods ofhearing loss were associated with recurrent ear infection. When otitis media is notaddressed as a chronic problem rather than a series of acute episodes, ear infectioncan be an exacerbating factor in LD. Early diagnosis and intervention could alleviatethe severity of LD.

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Crawford et al. (2006) reported that children with ADHD in addition to two ormore comorbid disorders had increased prevalence of behavior and cognitive deficitsas well as impairment in daily functioning. Sprouse et al. 1998 reported that childrenwith ADHD comorbid with LD were rated as less socially perceptive than controls.These findings confirm the results of the current study indicating that children withADHD comorbid with LD and otitis media had increased social stress and deficits ininterpersonal relations as well as academic impairment. As a result, they had anexternal locus of control associated with a tendency to attribute successes andfailures to forces beyond their control. In addition, there was a tendency to projectproblems onto peers, parents, and teachers. Parents who underestimate the severityof ADHD symptomatology may also have unrealistic expectations for theirchildren’s cognitive, academic, and psychosocial function.

In the current study, the findings suggest a unique subtype of ADHD comorbidwith LD and otitis media. Future research is suggested with increased sample sizesto confirm these findings. In addition, the learning styles of ADHD children with co-occurring OM and LD can be assessed contrasting visual and auditory presentationof information. It is also suggested that future research utilizing larger sample sizesevaluate the relationship between parental ratings of the severity of ADHDsymptomatology, psychosocial function, and the locus of control in childhoodADHD with comorbid disorders.

The apparent prevalence of OM in children with ADHD highlights the need forclinicians to recognize a possible subtype of ADHD. ADHD comorbid with otitismedia can exacerbate LD. Deficits in auditory processing have an impact on thetransmission and acquisition of information. Gaps in acquired information may bethe result of impaired auditory processing. Therefore, information transmittedprimarily in an auditory modality may place children with this subtype of ADHDat a disadvantage.

Appendix

-3

-2

-1

0

1

2

3

1 2 3

PhonologicalProcessing

Comprehen. ofInstruction

SentenceRepetition

IVA AuditorySpeed

WISC-IIIInformation

Fig. 1 Measures of auditoryprocessing (z-scores)

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0.002.004.006.008.00

10.0012.0014.0016.0018.0020.0022.0024.00

1 2 3

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Beta/SMRAmplitude

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Fig. 2 Theta, beta/SMR,and EMG amplitudes inmicrovolts

0.00

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