Speech-Sound Disorders and Attention-Deficit/Hyperactivity

LWW/TLD TLD200113 July 27, 2012 1:55

Top Lang Disorders Vol. 32, No. 3, pp. 247–263 Copyright c 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins Speech-Sound Disorders and Attention-Deﬁcit/Hyperactivity Disorder Symptoms

Barbara A. Lewis, Elizabeth J. Short, Sudha K. Iyengar, H. Gerry Taylor, Lisa Freebairn, Jessica Tag, Allison A. Avrich, and Catherine M. Stein

Purpose: The purpose of this study was to examine the association of speech-sound disorders (SSD) with symptoms of attention-deﬁcit/hyperactivity disorder (ADHD) by the severity of the SSD and the mode of transmission of SSD within the pedigrees of children with SSD. Participants and Methods: The participants were 412 children who were enrolled in a longitudinal family study of SSD. Children were grouped on the basis of the severity of their SSD as determined by their scores on the Goldman–Fristoe Test of Articulation and history of an SSD. Five severity groups were compared: no SSD, resolved SSD, mild SSD, mild–moderate SSD, and moderate–severe SSD. Participants were also coded for comorbid language impairment (LI), based on scores on a standardized language test. Pedigrees of children were considered to represent bilineal inheritance of disorders if there was a history for SSD on both the maternal and paternal sides of the family. Parents completed the ADHD rating scale and a developmental questionnaire for each of their children. Results and Conclusions: Children with moderate–severe SSD had higher ratings on the inattention and hyperactive/impulsivity scales than children with no SSD. Children whose family pedigrees demonstrated bilineal inheritance had higher ratings of inattention than children without bilineal inheritance. To determine the best predictors of ADHD ratings, multiple linear regression analyses were conducted. LI was more predictive of ADHD symptoms than SSD severity, bilineal inheritance of SSD, age, or gender. Findings support that LI rather than SSD is associated with ADHD. Key words ADHD, attention, genetics, language impairment, reading disorder, speech sound disorder

PEECH SOUND DISORDERS (SSD), lan- S guage impairment (LI), and attention- deficit/hyperactivity disorder (ADHD) are common developmental disorders that can Author Affiliations: Departments of Psychological significantly impact academic success. The Sciences (Drs Lewis and Short and Mss Freebairn comorbidity of these disorders may substan- and Tag), Epidemiology and Biostatistics (Drs Iyengar and Stein and Ms Avrich), and Pediatrics tially add to the difficulties experienced by the (Dr Taylor), Case Western Reserve University, child and require a combined treatment ap- Cleveland, Ohio. proach. SSD and LI are often comorbid, with This research was supported by the National Institutes approximately 40%–60% of children with SSD of Health, National Institute on Deafness and Other at preschool (Shriberg & Kwiatkowski, 1994) Communication Disorders, Grant DC00528, awarded to Barbara A. Lewis. and 11%–15% of 6-year-old children with SSD presenting with LI (Shriberg, Tomblin, & Mc- The authors have no relevant financial or nonfinancial relationships to disclose. Sweeny, 1999). LI and ADHD are often comorbid as well, with rates of comorbidity re- Corresponding Author: Barbara A. Lewis, PhD, De- partment of Psychological Sciences, Case Western Re- ported to be 30%–50% in children seen at serve University, 11635 Euclid Ave., Room 330, Cleve- ADHD clinics (Tannock & Schachar, 1996). land, OH 44106 ([email protected]). Although there are only a few reports on DOI: 10.1097/TLD.0b013e318261f086 the comorbidity of SSD and ADHD, these 247

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studies have suggested that LI, rather than of SSD) has on the presence of comorbid SSD, is associated with ADHD (McGrath, ADHD. Hutaff-Lee, Scott, Boada, Shriberg, & Penning- ton, 2007; Short, Freebairn, Hansen, & Lewis, 2008). THERELATIONSHIPOFADHDTOSSD Children with SSD have varied academic AND LI outcomes depending on the constellation of deficits that they exhibit. In our previous stud- The onset and prevalence of developmen- ies, we found that children with SSD in isola- tal disorders vary widely. SSD is highly preva- tion had better school-age outcomes on liter- lent in young children, with rates as high as acy measures than children with comorbid LI 15.6% of 3-year-old children (Campbell et al., (Lewis, Freebairn, & Taylor, 2002). We also 2003) declining to 3.8% of 6-year-old children demonstrated that children with SSD and co- (Shriberg et al., 1999). LI has reported preva- morbid conditions of LI or reading disorder lence estimates of 7.4% in kindergarten (males (RD) or both perform more poorly than chil- = 8%, females = 6%; Tomblin et al., 1997). dren with isolated SSD on measures of en- Prevalence estimates of ADHD vary from 1.9% dophenotypes, including phonological mem- to 17.8% of school-age children, with esti- ory, phonological awareness, and speeded mates differing depending on the nature of naming (Lewis, Avrich, Freebairn, Taylor, the sample recruited (Greenhill, Benton, & Iyengar, & Stein, 2011). Furthermore, we have Tirmizi, 2003). reported that children with SSD and comor- Children with combined SSD and LI com- bid LI are rated more poorly by their parents prise approximately 7% of the general popu- on an ADHD rating scale (ARS) than children lation (Johnson et al., 1999) and appear to be with isolated SSD (Short et al., 2008). In that at increased risk for ADHD. Reilly, Cunning- study, we examined three groups of partici- ham, Richards, Elbard, and Mahoney (1999) pants: children with SSD alone (n = 71), chil- reported that more than 30% of children diag- dren with SSD and comorbid LI (n = 77), and nosed with SSD + LI met criteria for ADHD. typical children (n = 72). Children with SSD Estimates of comorbid ADHD may vary de- + LI were more likely to have been diagnosed pending on whether the sample is clinically as- with ADHD by a health care provider, and certained or population based. Rates of ADHD to have reading problems and spelling prob- were 5 times higher in the language-disabled lems, than children with SSD alone or typi- population obtained from a speech and lan- cal children. Although the ARS was the best guage clinic than in a sample of children from predictor of ADHD, the combination of the the general population without a diagnosis ADHD rating score and a score on the Clin- of LI. Similarly, rates were quite high in a ical Evaluation of Language Fundamentals 3 prospective sample of Canadian kindergarten (CELF-3) improved the prediction of ADHD. children (Beitchman, Nair, Clegg, Ferguson, This suggests that language abilities are pre- & Patel, 1986), with 16% of children diag- dictive of ADHD over and above the ARS. nosed with both SSD and LI simultaneously However, in these studies the severity of SSD diagnosed with ADHD, as compared with and the family history for disorders were not only 6% of typical kindergarten children diag- considered. This article extends these findings nosed with ADHD. In a later study, Beitchman by examining differences in ADHD ratings in et al. (1989) reported that 59% of children children with resolved, mild, mild–moderate, with both SSD and LI had comorbid attention or moderate–severe SSD with and without deficits, whereas only 5% of children with SSD comorbid LI. Furthermore, we consider the alone demonstrated these attentional prob- impact that family history for SSD reported lems. Many children diagnosed with ADHD for both parents (i.e., bilineal transmission have both articulation and language problems

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(Baker & Cantwell, 1992), with expressive One method of subgrouping children with language difficulties noted more frequently in SSD has been to group children on the ba- children with ADHD than receptive language sis of the severity of SSD (Lewis et al., 2011). difficulties (Barkeley, DuPaul, & McMurray, Traditionally, clinical severity ratings of SSD 1990). can be identified as mild, moderate, or se- In addition, a study by McGrath et al. (2007) vere depending upon the speech–language examined ADHD symptoms as rated by par- pathologist’s (SLP’s) judgment of the child’s ents and teachers in 108 children aged 4– intelligibility of conversational speech or the 7 years with SSD who were also diagnosed number of speech sound errors that the child with or without LI. Children with combined exhibits on a standardized articulation test. SSD and LI had higher rates of inattention Another measure of severity, which is more than children with SSD alone. It should be objective, is the Percentage of Consonants noted, however, that no differences were Correct (PCC) developed by Shriberg and found in the children with and without LI Kwiatkowski (1982). The PCC includes the on the hyperactivity/impulsivity ratings. An number of consonants produced correctly in unexpected finding was that children with a continuous speech sample divided by the SSD and LI whose speech disorder had nor- total number of consonants in the sample. malized tended to have higher rates of inat- Severity of SSD is classified as mild (85%–100% tention than children with persistent SSD. correct), mild–moderate (65%–85% correct), This suggests heterogeneity within the SSD moderate–severe (50%–65% correct), or se- population. One hypothesis proposed by Mc- vere (<50% correct). Despite the widespread Grath et al. to account for their findings usage of severity ratings to make treatment is that children with comorbid SSD and LI decisions, however, clinicians do not al- whose SSD resolves may exhibit more gen- ways agree in their perceptual ratings of a eral language learning disabilities that are ac- child’s speech (Flipsen, Hammer, & Yost, companied by inattention disorders, whereas 2005). children with persistent SSD may demon- An issue that is not yet resolved is whether strate a more circumscribed phonological children with more severe forms of SSD deficit. are qualitatively different than children with Comorbidity rates of SSD, LI, and ADHD are milder forms of SSD, and as such, present with also high when the sample is ascertained pri- different etiologies, speech sound character- marily by an ADHD diagnosis. In ADHD clin- istics, and developmental trajectories. Most ics, rates of language problems range from clinicians and researchers assume that chil- 30% to 50% (Tannock & Schachar, 1996). dren with severe language disorders are more Levy, Hay, McLaughlin, Wood, and Wald- biologically compromised than those with man (1996) surveyed a nonselected sample milder disorders. Geneticists have long used a of 1,938 families for both ADHD and speech variety of severity measures in their selection and language disorders, and found a strong as- of families and populations (e.g., recurrent sociation of ADHD with speech and reading clustering in families, earlier age at onset, and problems. the number of manifest conditions) hoping that severity might be a useful tool for isolat- SUBGROUPING CHILDREN WITH SSD BY ing genes specifically tied to the condition or SEVERITY disease. As severity is currently defined, children with the most severe forms of the dis- Despite the high prevalence rates of ADHD order require the most extensive treatments and LI, few researchers have considered SSD and present with lifelong problems that even- separately from LI, and they have not con- tually manifest as lost productivity and poorer sidered subtypes within the SSD population. perceived quality of life (Ruben, 2000).

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GENETIC LOAD AND COMORBIDITY OF members demonstrated orofacial apraxia and SSD AND ADHD associated speech–language disorders. The FOXP2 gene is located on chromosome 7. A substantial number of researchers have Individuals who carried the mutant FOXP2 argued that susceptibility to SSD is genetic allele evidenced a variety of deficits, includ- (Hurst, Baraitser, Auger, Graham, & Norell, ing SSD, as well as impairments in IQ, LI, 1990; Spitz, Tallal, Flax, & Benasich, 1997; and RD (Lai, Fisher, Hurst, Vargha-Khadem, Whitehurst et al., 1991). Family studies have & Monaco, 2001). Findings from neuroimag- demonstrated familial aggregation for SSD, ing studies of the KE family suggested that with 20%–40% of first-degree relatives af- the FOXP2 gene has pleiotropic (i.e., multi- fected (Felsenfeld, McGue, & Broen, 1995; ple) effects on many aspects of brain devel- Lewis, Cox, & Byard, 1993; Lewis, Ekelman, & opment, accounting for the co-occurrence of Aram, 1989; Tallal, Ross, & Curtiss, 1989). Seg- SSD and LI (Liegeois,´ Morgan, Connelly, & regation analyses also have confirmed familial Vargha-Khadem, 2011). Although the FOXP2 aggregation of SSD and have supported both a mutation has been found in only a few families major gene and polygenic modes of transmis- and does not account for the majority of SSD, sion of the disorder (Lewis et al., 1993). Twin these findings confirm the existence of genes studies (Bishop, North, & Donlan, 1995) also that influence SSD (Shriberg et al., 2006). This have supported a genetic basis for SSD. Bishop gene remains of interest because mouse pups and Haiyou-Thomas ( 2008) found that LI was with a knockout (i.e., deactivation) for FOXP2 more heritable when comorbid with SSD than showed disruptions in ultrasonic vocalization when occurring in isolation. Rates of heritabil- that interfered with the communication be- ity for SSD have been estimated as high as .97 tween pup and mother (Shu et al., 2005). whereas the heritability of LI has been esti- Thus, it is feasible that unidentified variants mated to range from 0.38 to 0.76, depending in this molecule cause some forms of SSD. on the severity of the disorder (Viding et al., The genetics of ADHD are also complex 2004). Several studies have estimated the her- (Pauls, 2005; Poelmans, Pauls, Buitelaar, & itability of component skills of SSD (Bishop, Franke, 2011). Genetic studies of ADHD in- Adams, & Norbury, 2006). Reported heritabili- cluding family, adoption, and twin studies ties for these skills are as follows: 0.37 for artic- (Faraone & Doyle, 2000; Smalley, 1997; Tan- ulation, 0.37 for oral motor skills, 0.43 for lan- nock, 1998) and molecular genetic studies guage, 0.60 for phonological awareness, 0.52 (Fisher & DeFries, 2002) have suggested a ge- for semantics, 0.30 for syntax, 0.63 for phono- netic component to ADHD, with estimates of logical memory, and 0.64 for rapid naming. heritability exceeding 0.70. A recent review A study by Bishop et al., (2006) reported the of five genome-wide association studies of heritability of phonological memory, based on ADHD revealed 85 candidate genes, with 45 of nonword repetition, to be 0.61, a sentence im- these influencing a neurodevelopmental net- itation task to be 0.36, and a syntax task to be work (Poelmans et al., 2011). Candidate genes 0.82. for ADHD influence processes such as neu- Only a few molecular genetic studies of ronal migration, cell adhesion, and cell divi- SSD have been conducted. Two genes specific sion (Banaschewski, Becker, Scherag, Franke, to speech and voice disorders (i.e., FOXP2 & Coghill, 2010). Endophenotypes examined and TOSPEAK) have been isolated, whereas in genetic studies of ADHD include those re- other genes appear to primarily be associated lating to executive function, motor deficits, re- with RD and LI (i.e., KIAA0319, DCDC2, CNT- action time, speed of processing, set shifting, NAP2, DYX1C1,andROBO1). and cognitive impulsiveness (Kebir & Joober, Discovery of the FOXP2 gene resulted from 2011; Rommelse et al., 2009). studies of a large three-generation family with Given the comorbidity of disorders that of- an SSD, designated as the KE family, whose ten occur in SSD, LI, and ADHD, researchers

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have been assuming common underlying ge- with SSD are a heterogeneous group, and fac- netic bases for these disorders. Pennington tors such as severity of impairment and family and Bishop (2009) have contended that the history for SSD may influence the develop- comorbidity observed in these diagnostic mental trajectory of the disorder. In addition, groups may result from shared deficits in en- high genetic load, which is defined as bilin- dophenotypes or cognitive skills, including eal inheritance in families that report affected memory, processing speed, or attention (Mc- individuals for SSD in both maternal and pater- Grath et al., 2007; Pennington & Bishop, 2009; nal pedigrees, may be associated with higher Peterson, Pennington, Shriberg, & Boada, rates of comorbidities. This study addressed 2009). Quite likely, these endophenotypes two research questions: may be influenced by genes that have broad 1. Is there an association between sever- effects on neural development and processing ity of early SSD (none, resolved, mild, (Lewis et al., 2011). For example, Castellanos mild–moderate or moderate–severe) and and Tannock (2002) have suggested that en- later ADHD symptoms; and, if so, which dophenotypes, such as a delay in temporal variables (i.e., severity of SSD, comorbid processing or working memory deficits, ap- LI,gender,orage)bestpredictADHD pear to underlie ADHD, with the same en- ratings? dophenotypes contributing to SSD and LI. A 2. Is there an association between early SSD child with ADHD may not attend to features and later ADHD symptoms if the family of speech and language necessary for mastery. demonstrates bilineal inheritance of SSD; Similarly, the multiple deficit model suggests and, if so, which variables (i.e., bilineal that shared deficits in processing speed may inheritance of SSD, comorbid LI, gender, account for the comorbidities of these disor- or age) best predict ADHD ratings? ders (Pennington, 2006). Not surprisingly, genetic overlap between METHOD these disorders has been observed. Genetic linkage studies have demonstrated that SSD Participants and ADHD share a common locus on chro- All participants were part of an ongoing mosome 6p22 (Smith, Pennington, Boada, & family study of speech and language disorders Shriberg, 2005; Wilcutt et al., 2002). How- (Lewis et al., 2002; Lewis, Freebairn, & Tay- ever, studies of children with SLI have not lor, 2000a, 2000b). Families were recruited found linkage to this locus (Bartlett et al., from the clinical caseloads of SLPs working 2002; The SLI Consortium, 2002, 2004). Al- in the greater Cleveland area. All children in though SSD, LI, RD, and ADHD often may be each family were tested regardless of whether comorbid, there is evidence of both shared they were enrolled in speech–language ther- and independent genetic effects for these dis- apy. Proband children with SSD (n = 163) met orders that is consistent with the pleiotropic the following criteria at the time of their ini- effects of some genes, that is, with one tial assessment: (a) scored below the 10th per- gene influencing multiple traits or pheno- centile on the Goldman–Fristoe Test of Articu- types (Gayan et al., 2005; Hart et al., 2010). lation (GFTA)–Sounds in Words Subtest (Gold- To date, only a few studies have specifically man & Fristoe, 1986); (b) exhibited at least examined the comorbidity of SSD and ADHD. three phonological process error types on the Although these studies have considered co- Khan–Lewis Phonological Analysis (Khan & morbid LI, they have not examined the sever- Lewis, 1986); (c) passed a pure tone hearing ity of SSD, nor have they considered family screening bilaterally suggesting normal hear- history for SSD. The purpose of this study was ing and had less than six episodes of otitis me- to examine rates of comorbid ADHD in a clin- dia prior to the age of 3 years; (d) exhibited ical sample of children diagnosed with early a normal oral peripheral speech mechanism SSD with and without comorbid LI. Children as determined by a licensed SLP; (e) showed

252 TOPICS IN LANGUAGE DISORDERS/JULY–SEPTEMBER 2012

no signs of other neurological or developmen- ered affected if the parents reported that they tal delays per parent report; (f) demonstrated had a history of SSD. Families were coded as normal cognitive skills on the performance demonstrating bilineal inheritance if both the subscale of the Wechsler Preschool and Pri- paternal and maternal family pedigree had at mary Scale of Intelligence Revised (WPPSI-R) least one member other than the proband and (performance IQ [PIQ] > 80; Wechsler, 1989) his or her siblings with an SSD. or Wechsler Intelligence Scale for Children- 3rd Edition (WISC-III) (PIQ > 80; Wechsler, Measures and procedures 1991). Siblings of the proband children (n = Speech–sound development 248) also were enrolled in the study. Siblings The GFTA was administered to determine were classified as having SSD if they met the the presence of speech–sound errors. It uses aforementioned criteria or if they had a history 35 picture plates and 44 target words to elicit of SSD that required speech–language ther- consonants in the initial, medial, and final apy. Siblings who had never had SSD served position of words, as well as 12 consonant as the typical control group (no SSD group). clusters (blends) in the initial position. Re- The severity of SSD in the participants was sponses were audio taped, phonetically tran- defined by scores, based on the GFTA (Gold- scribed, and plotted on the consonant error man & Fristoe, 1986). A mean GFTA per- matrix. Age-adjusted percentile scores were centile score of 75 (SD = 31) was obtained employed in the severity classification. for children who had never received speech– language therapy and had not reported a his- Language tory of speech or language disorders. On the basis of this mean score, five groups were cre- The Clinical Evaluation of Language ated: moderate–severe SSD (<−2 SD from the Fundamentals–Preschool (CELF-P; Wiig, Sec- mean; n = 109), mild–moderate SSD (≥−2 SD ord, & Semel, 1992), CELF-3, or TOLD-P:3 but <−1 SD, n = 119), mild SSD (≥−1 SD but was administered to assess expressive and below the mean; n = 54), resolved SSD (at or receptive language skills. Age-adjusted stan- above the mean but a reported history of ther- dard scores were employed to classify chil- apy for SSD; n = 39), and no history of SSD dren with LI. (at or above the mean with no history of SSD; Performance IQ n = 91). Children were further diagnosed as SSD Participants were required to demonstrate with comorbid LI, if they earned a scaled score normal intelligence as defined by a prorated of 8 or less on two or more subtests of CELF- PIQ of at least 80 on the WPPSI-R or WISC-III. 3 (Semel, Wiig, & Secord, 1995) or the Test of Language Development–Primary 3rd Edi- Semistructured interview tion (TOLD-P:3; Newcomer & Hammill, 1997) All comorbidity data were obtained by par- prior to their initiation of therapy. This defini- ent report in a semistructured interview. Par- tion was based on the criteria for LI of Tomblin ents were asked to indicate whether their et al. (1997), which defined LI as a scaled child was ever diagnosed with the follow- score of less than 8 on two or more subtests of ing disorders: learning disabilities, LI, ADHD, the Test of Language Development–Primary or RD. Family pedigree data were collected 2nd Edition. The normal speech and language for both the paternal and maternal families group (n = 91) did not meet criteria for either through the Family History Interview (Lewis SSD or LI. & Freebairn, 1993), a pedigree was drawn, Affection status of parents and extended and families were coded as demonstrating bi- family members was determined by a lineal inheritance if both the maternal and semistructured interview, described in the fol- paternal sides of the family reported affected lowing text. Family members were consid- members for SSD.

Speech-Sound Disorders and ADHD 253

ADHD rating scale language pathologist administered all of the In this study, comorbid ADHD was docu- measures. Testing was carried out in a speech mented either by parent report of a previous research laboratory at Case Western Reserve diagnosis of ADHD by a health care provider University or, at the parent’s request, in a or by ratings within the clinical range on quiet and adequately lit room in the fam- the ADHD Rating Scale (ARS) (Diagnostic ily’s home. The speech productions from the and Statistical Manual of Mental Disorders GFTA were recorded using a Sony Profes- [Third Edition Revised] and Diagnostic and sional Tape Recorder (WM-DC6; Walkman Statistical Manual of Mental Disorders Professional, Sony Corporation, New York, [Fourth Edition] versions; DuPaul, 1991; NY) and an Audio-Technica Omnidirectional DuPaul et al., 1996). Symptoms of ADHD (but Microphone (AT-804; Audio-Technica U.S., not necessarily a clinical diagnosis of ADHD) lnc., Stow, Ohio). Responses were recorded were documented through the ARS. The ARS initially online using phonetic transcription. assesses the commonly noted symptoms of In addition, children were administered the ADHD, including hyperactivity, impulsivity, standardized language tests according to the and inattention. The home report version instruction manuals. A semistructured inter- of the ARS was employed in the present view, the Family History Interview, and the investigation. The parent is asked to evaluate ADHD questionnaire were completed by the the child’s behavior over the last 6 months by examiner with parents. This study was ap- rating 18 different home behaviors on severity proved by the Human Subjects Committee of rating scale of “0” (never or rarely) to “3” (very University Hospitals Case Medical Center of often). Three global percentile scores were Cleveland, OH. Informed consent and assent obtained from the ARS: an inattention index, were obtained from participants before test- a hyperactivity/impulsivity index, and a total ing. ADHD index. The ARS has been shown to discriminate children diagnosed with ADHD Design and analysis from those children who have learning dis- Chi-square analyses and one-way analysis of abilities, to differentiate children with hyper- variance (ANOVA) were conducted to com- activity from children without hyperactivity, pare severity groups on demographic vari- and to be sensitive to stimulant drug effects ables, articulation and language measures, and (Barkeley et al., 1990). Behavior ratings scales the ARS scores. ANOVAs were employed to are widely used to assess ADHD because they compare bilineal inheritance and lack of bilin- are norm based and reliable (Merrell, 1999, eal inheritance groups on the proband’s ARS Mueller & Tomblin, 2012). Although the use scores. Significant differences were followed of parent rating scales may result in the overi- by Tukey post hoc analyses. dentification of behavior problems in children To examine the influence of predictor vari- with speech and language impairments (Red- ables of SSD severity group, bilineal inheri- mond, 2002), to our knowledge there are tance, gender and age on the ARS ratings of no data to suggest that the ratings of parents inattention, hyperactivity/impulsivity, and to- of children with both SSD and LI would be tal rating score, we conducted linear regres- more inflated than the ratings of parents of sion analyses. Regressions were conducted children with SSD alone. Children meeting in a backward-stepwise fashion, such that all rating scale criteria for ADHD, based on the variables were in the starting model, and vari- ARS, were those with percentiles greater ables were taken out one at a time starting than 85 on any of the three global scores. with the highest p values. At each iteration, we checked how closely the model fit the data Procedures by evaluating R2 values to make sure the high- The participants were tested individually in est possible R2 value was used with the lowest two sessions. A licensed and certified speech– p values for each variable in the model. The

254 TOPICS IN LANGUAGE DISORDERS/JULY–SEPTEMBER 2012 p a,b,c,d,e,f a,d,f a,b,c,d,e,f,g,h,i d,g d,f,g,i,j .0001 .0001 .0001 .0001 .0001 < < < < < ) .0048 2 χ ) df ( F speech-sound disorders. = 2 η performance IQ; SSD = SSD Total Severe Moderate– SSD Mild– Moderate Goldman–Fristoe Test of Articulation; PIQ = 91 39 54 119 109 412 No SSD Resolved SSD Mild SSD 8.54 (2.26) 8.58 (1.66) 6.26 (2.29) 7.93 (5.41) 5.69 (2.34) 7.31 (3.65) 10.80 12.32 (4,411) 10.15 (4.04) 9.50 (3.26) 8.26 (5.76) 9.12 (6.00) 6.74 (4.05) 8.69 (5.01) 6.36 6.91 (4,411) 97.05 (5.93) 95.85 (7.83) 59.87 (8.70) 25.61 (8.84) 5.03 (4.18) 46.99 (37.98) 96.62 2,906.09 (4,411) 109.18 (15.34) 102.46 (16.76) 102.85 (18.05) 102.13 (16.07) 95.99106.37 (14.49) (16.59) 102.31 (16.46) 94.56 (20.16) 8.10 100.48 (17.68) 98.90 (17.04) 89.93 (15.18) 8.33 (4,332) 97.96 (17.83) 11.35 12.55 (4,396) Comparison of SSD severity groups on demographics speech, language, and PIQ measures ) ) ADHD, attention-deﬁcit/hyperactivity disorder; GFTA SD SD testing, mean years ( percentile score standard score siﬁcation, mean years ( Recovered SSD differs from mild–moderate SSD. No SSD differs from mild SSD. No SSD differs from moderate SSD. No SSD differs from mild–moderate SSD. Male/female 42/49 22/17 33/21 63/56 78/31 238/174 14.94 (4,411) ( n Age at ADHD GFTA PIQ standard Language Age at SSD clas- Mild SSD differs from mild–moderate SSD. Recovered SSD differs from mild SSD. Recovered SSD differs from moderate SSD. Mild–moderate SSD differs from moderate SSD. Mild SSD differs from moderate SSD. No SSD differs from recovered SSD. Table 1. Note. a b c d e f g h i j

Speech-Sound Disorders and ADHD 255

final models included only significant vari- 65). With the exception of RD, the moderate– ables (p < 0.05). severe group had the highest rates of comorbid disorders (LI = 74%; RD = 21%; ADHD = RESULTS 21%). Although the resolved group had higher rates of RD (46%), this observation is consis- As can be seen in Table 1, the groups (no tent with the older age of this group and the SSD, resolved SSD, mild SSD, mild–moderate fact that RD is typically diagnosed at an older SSD, and moderate–severe SSD) differed sig- age. nificantly in gender, χ 2(4, 411) = 14.9, p = The severity groups were also compared .005, and age, F(4, 411) = 12.32, p < .0001. on the ARS scores of inattention, hyperactiv- There were proportionally more males than ity/impulsivity, and total score. As shown in females. The mean age at the time of the Table 3, significant differences across groups initial assessment with the moderate–severe were observed for the inattention scale, F(4, = = SSD group (M = 5.69; SD = 2.34 years) was 411) 3.22, p .013. In addition, significant less than that for the other groups and the differences across groups were observed on no SSD (M = 8.54; SD = 2.26) and the re- the hyperactivity/impulsivity score, F(4, 411) = = solved SSD (M = 8.58; SD = 1.66) were the 3.20, p .013. Finally, significant differ- oldest groups. The groups also differed on the ences across groups were observed on the to- = = composite language scores of the TOLD-P:3, tal scores, F(4, 411) 3.86; p .004. Post hoc CELF-P, or CELF-3, with the moderate–severe testing revealed significant group differences group performing more poorly (M = 89.93; between the no SSD and the moderate–severe < SD = 15.18) than the no SSD, mild SSD, and SSD groups for all three scores at the p .05 mild–moderate SSD groups. The no SSD group level. Effect sizes were small for these com- η2 = η2 also scored higher than the resolved and mild– parisons ( 3.06 for inattention score; = moderate SSD groups. In addition, the no SSD 3.05 for the hyperactivity/impulsivity score; η2 = group scored higher on the PIQ measure (M = and 3.66 for total score; Cohen, 1973). 109.18; SD = 15.34) than the mild–moderate This indicated that severity of SSD made a (M = 102.13; SD = 16.07) and moderate– small contribution to the differences in inat- severe (M = 95.99; SD = 14.49) SSD groups. tention, hyperactivity/impulsivity, and total Comorbid conditions reported by the par- score ratings among the groups. ents for participants in each group are shown Comparisons of the bilineal and nonbilineal in Table 2. Language impairment (n = 166) inheritance groups were made for probands was the most frequently reported comorbid only, because siblings and probands share condition; the next most commonly reported identical pedigree information. As shown in conditions were RD (n = 92) and ADHD (n = Table 4, probands with bilineal inheritance

Table 2. Number of participants with comorbid conditions by severity group

Mild– Moderate- Moderate Severe No SSD Resolved SSD Mild SSD SSD SSD

Language impairment 11 (12%) 19 (49%) 16 (30%) 39 (33%) 81 (74%) (n = 166) Reading disorder 21 (23%) 18 (46%) 13 (24%) 17 (14%) 23 (21%) (n = 92) ADHD (n = 65) 9 (10%) 12 (31%) 9 (17%) 12 (10%) 23 (21%)

Note.ADHD= attention-deﬁcit/hyperactivity disorder; SSD = speech-sound disorders.

256 TOPICS IN LANGUAGE DISORDERS/JULY–SEPTEMBER 2012

demonstrated higher ratings of inattention a a a

p than probands whose pedigrees were not bilineal, F(1, 162) = 5.08, p = .026. No signiﬁcant differences were observed for the

) hyperactivity/impulsivity scale or total score.

df The effect size was small for this compari- ( 2 F son (η = 3.06), indicating that bilineal inheritance made a small contribution to variations in ratings of inattention on the ARS. As shown 2

η in Table 5, chi-square analyses revealed no sig- niﬁcant differences between the bilineal and not bilineal groups in severity of SSD or comorbidity of LI; hence, these factors fail to account for the effects of bilineal inheritance on symptoms of ADHD. Regression analyses were conducted to determine whether severity of SSD was a predic- ) Total tor of ADHD ratings. Predictors in the regres- SD

( sion model included severity of SSD, gender,

M age at ADHD assessment, and comorbid LI. Moderate– Severe SSD, As seen in Table 6, comorbid LI predicted all three scores-–inattention (R2 = .13), hyperactivity/impulsivity (R2 = .06), and total (R2 ) = .11). SD ( A second series of regressions were em- Mild– M

Moderate, ployed to determine whether bilineal inheritance was a predictor of ADHD ratings. Again, only the probands were included in this anal- ) ysis so as not to include each family pedi- SD ( gree more than once. Predictors in the re- M

Mild SSD, gression models were the presence/absence speech-sound disorders.

= of bilineal inheritance, gender, age at ADHD assessment, and comorbid LI. Bilineal inher- M

) itance, age, and comorbid LI predicted the 2 =

SD inattention score (R .24). The only predic- (

SSD, tor for the hyperactivity/impulsivity score was Resolved LI (R2 = .07). Predictors for the ADHD total scoreweregender,age,andLI(R2 = .18; see

) Table 7). SD (

M DISCUSSION No SSD, 38.65 (32.41) 54.08 (35.85)31.63 (30.32) 45.22 (32.90) 45.13 (37.93) 43.96 (34.24) 46.36 (34.50) 53.83 (33.61) 43.61 (34.18) 46.5 (34.02) 47.20 (32.99) 3.06 42.4 (33.83) 3.22 (4,411) 3.05 .0129 3.20 (4,411) .0132 This study examined ADHD symptoms in a clinical population of children recruited for

attention-deﬁcit/hyperactivity disorder; SSD SSD. Previous research suggested that chil- = Comparison of SSD severity groups’ performance on ADHD rating scale mean (SD) dren with SSD and comorbid LI were more at risk for ADHD than children with isolated ADHD

scale ity/impulsivity scale SSD (McGrath et al., 2007; Short et al., 2008). ADHD inattention ADHD hyperactiv- ADHD total score 34.81 (29.41) 51.10 (35.62) 44.09(32.51) 45.42 (33.06) 51.84 (32.23) 45.1 (32.69) 3.66 3.86 (4,411) .0043 No SSD differs from moderate–severe SSD.

Table 3. Note. a However, these studies did not consider the

Speech-Sound Disorders and ADHD 257

Table 4. Comparison of probands with bilineal and not bilineal inheritance of SSD on ADHD rating scale

Not Bilineal, Bilineal, M (SD) M (SD) Total η2 F (df) p

ADHD inattention 47.54 (34.69) 60.35 (33.08) 51.40 (34.54) 3.06 5.08 (1,162) .0256a scale ADHD hyperactiv- 43.86 (33.58) 51.69 (34.83) 45.89 (34.13) 1.17 1.91 (1,162) .1687 ity/impulsivity scale ADHD total score 47.36 (33.30) 55.76 (32.77) 49.61 (33.23) 1.42 2.32 (1,162) .1294

Note. ADHD = attention-deﬁcit/hyperactivity disorder. aNot bilineal inheritance differs from bilineal inheritance.

Table 5. Comparison of probands with bilineal and not bilineal inheritance on SSD severity and comorbidity of language impairment

Bilineal Not Bilineal χ 2 (df) p

Resolved SSD 5 4 3.79 (1,162) .2846 Mild SSD 4 11 Mild–moderate SSD 13 37 Moderate–severe SSD 32 57 SSD alone 18 39 0.0950 (1,162) .7579 SSD + LI 36 70

Note. SSD = speech-sound disorders.

phenotypic or genetic heterogeneity within a function of the severity of SSD and bilineal their SSD cohorts. Findings by McGrath et al. inheritance for disorders. (2007) suggested that heterogeneity of SSD may account for the difference in ADHD rates for children with resolved SSD as compared Severity of SSD and ADHD symptoms with children with persistent SSD. This study Children with more severe forms of SSD extended ﬁndings of previous research by ex- had poorer language scores, as measured by amining differences in symptoms of ADHD as the CELF-P, CELF-3, or TOLD-P:3, and more

Table 6. Predictors of ADHD ratings of inattention, hyperactivity/impulsivity, and total ADHD scores

Variable Predictor β b (SE) pR2

ADHD inattention scale Language impairment 25.16 3.19 <.0001 .13 ADHD hyperactivity/ impulsivity scale Language impairment 16.72 3.30 <.0001 .06 ADHD total score Language impairment 22.40 3.10 <.0001 .11

Note. ADHD, attention-deﬁcit/hyperactivity disorder.

258 TOPICS IN LANGUAGE DISORDERS/JULY–SEPTEMBER 2012

Table 7. Predictors of ADHD ratings of inattention, Hyperactivity /Impulsivity and Total ADHD scores by bilineal inheritance (probands only)

Variable Predictor β b (SE) pR2

ADHD inattention scale Bilineal 11.60 5.06 .0231 .24 Age 4.39 1.61 .0071 Language impairment 29.55 5.00 <.0001 ADHD hyperactivity/impulsivity scale Language impairment 19.26 5.35 .0004 .07 ADHD total score Gender 10.26 5.08 .0450 .18 Age 3.03 1.46 .0398 Language impairment 25.48 4.99 <.0001

Note. ADHD, attention-deﬁcit/hyperactivity disorder.

frequent comorbid LI. The moderate–severe higher rates of ADHD than their persistent SSD group demonstrated more symptoms of SSD group. McGrath and colleagues suggested inattention and hyperactivity/impulsivity than that SSD in the resolved group may have pre- the children without SSD. These findings are sented early in life due to neurodevelopmen- in partial agreement with those of McGrath tal immaturity, with their speech sound errors et al. (2007) who found that speech and lan- resolving with development or intervention guage disorders were associated with inat- or both. Further evidence for this hypothe- tention disorders. However, McGrath et al. sis of neurodevelopmental immaturity can be (2007) did not find differences in the hyper- seen in the work of Raitano, Pennington, Tu- activity ratings as we did, perhaps, in part, nick, Boada, and Shriberg (2004), who found because of the older age of their participants. the resolved SSD group with LI was poorer on However, as the moderate–severe group had rapid serial naming, a processing speed mea- the highest rate of comorbid LI at 74%, it may sure, and had lower nonverbal IQs than the be that LI rather than SSD is related to inat- resolved SSD group without LI. In our sample, tention and hyperactivity/impulsivity symp- all our SSD groups (resolved, mild–moderate, toms. This was supported by the regression and moderate–severe) had lower PIQs than analyses that found that LI rather than sever- the no SSD group. ity of SSD was the most predictive of inattention and hyperactivity/impulsivity ratings. Bilineal inheritance of SSD and ADHD Our findings lend further support to a recent To examine the influence of family history meta-analysis by Ebert and Kohnert (2011), for disorders on the comorbidity of ADHD in which they reported that children with LI with SSD, pedigrees were sorted according demonstrate subclinical deficits in sustained to the presence/absence of bilineal mode of attention when compared with typically de- inheritance of SSD. The bilineal and nonbi- veloping peers. lineal groups did not differ in the severity of Our resolved SSD group, children who had SSD or the rates of comorbidity of LI. How- a history of SSD but no longer presented with ever, proband children from bilineal fami- speech sound errors, had the highest rates lies had higher ratings of inattention symp- of RD (46%) and a rate of previous diagno- toms than children whose pedigrees did not sis of ADHD by a health provider (31%) that demonstrate bilineal inheritance. These find- was higher than that of the moderate–severe ings support the association between inatten- SSD group (21%). These findings are con- tion symptoms and SSD but not hyperactiv- sistent with those of McGrath et al. (2007) ity/impulsivity symptoms. Results also suggest who reported that their resolved group had that a higher genetic load for disorders is

Speech-Sound Disorders and ADHD 259

associated with inattention symptoms. Al- Second, SSDs are heterogeneous and sub- though the groups did not differ in rates of types may differ in their association with co- LI, regression analyses revealed that comorbid morbid conditions. In this study, we subtyped LI was predictive of all three scores on the SSD by severity and found that more severe ARS (inattention, hyperactivity/impulsivity, disorders were associated with attention diffi- and total). However, comorbid LI was more culties. The presence of comorbid attentional closely associated with the inattentive rating impairments complicates the treatment regi- than with bilineal inheritance. men for children with SSD. Although atten- There may be several explanations for tional impairments may be treated effectively these findings. First, children whose fami- by psychopharmacological agents, SSD and lies demonstrate bilineal inheritance may rep- LI are not. Failure to distinguish attentional resent a subtype of SSD with a polygenic problems from language processing difficul- mode of transmission of disorders, with many ties may result in inappropriate treatment of genes making small contributions to the phe- the problem. That is, children may be seen notype. These genes may have biological func- as inattentive when in fact their surface pre- tions that influence cognitive processes or sentation of inattention stems, not from dys- endophenotypes affecting multiple develop- regulation, but rather, from a failure to un- mental disorders. For example, genes related derstand language (Short et al., 2008). Un- to slow speed of processing may contribute fortunately, we were unable to separate out to SSD, LI, and ADHD. A second explanation the effects of comorbid LI in our SSD sample. is that a major gene or multiple genes may be Clinicians should be aware that SSD subtypes responsible for the developmental problems may differ in their response to treatment, in of children without a bilineal pattern of inher- part, due to variations in their comorbid con- itance of SSD. These genes may be unique to ditions. Differential diagnoses, particularly as SSD, LI, or ADHD, but do not influence cogni- they pertain to teasing out the presence of LI tive processes that are shared across multiple and attentional problems, are needed to in- disorders. For example, a gene that influenced sure that comorbid conditions are identified oral motor skills may be unique to SSD but may and treated appropriately. not contribute to LI or ADHD. Finally, family history is important for iden- tifying children who are at risk for comorbid attention deficits. Children with bilineal in- Clinical implications heritance should be monitored for attention The findings from this study have several problems. Although the shared genetic bases clinical implications. First, as reported previ- for these disorders have not been identified, it ously, children with combined SSD and LI are is likely that both polygenic and major genes at risk for attention deficits. Longitudinal stud- influence SSD and its comorbid conditions. ies have reported that children with isolated SSD have better academic prognoses than chil- Limitations and future directions dren with comorbid LI (Baker & Cantwell, Several limitations of this study should be 1992; Beitchman et al., 1986; King, Jones noted. First, the ADHD ratings were limited & Lasky, 1985). Children with SSD and LI to parent reports, and teacher ratings were are at risk for literacy difficulties (Aram & not obtained. Teacher ratings of ADHD would Hall, 1989; Hall & Tomblin, 1978; Lewis et likely differ from parent ratings, as teachers al., 2000a; Nathan, Stackhouse, Goulandris, & observe the child in a more structured setting Snowling, 2004). Additional attention difficul- that requires more linguistic proficiency than ties will most likely impede academic success the home setting (Redmond, 2002). Redmond even more. Clinicians should be aware of the and Rice (1998) reported differences between comorbidity of these disorders and coordinate teacher and parent ratings for children with remediation strategies for each. LI, with teachers more stringent in their

260 TOPICS IN LANGUAGE DISORDERS/JULY–SEPTEMBER 2012

ratings than parents. Second, the study did not surface speech sound errors, also may be im- include a group of children with LI only, and, portant to consider. Dodd proposed subtypes as such, we cannot determine the influences of articulation disorder, phonological delay, of LI alone on ADHD ratings. Future studies consistent phonological disorder, and incon- should include this group so that associations sistent phonological disorder. Finally, genetic of LI and ADHD may be teased out from the heterogeneity may exist within the bilineal or influences of SSD. Also, neuropsychological nonbilineal groups, and, therefore, different assessments of attention or executive func- phenotypes may be represented within a sin- tion were not administered. Such measures gle group. may help to quantify the deficits in attention The findings from this study highlight the and self-regulation and aid in designing reme- genetic and phenotypic complexity of these diation programs. Finally, other subgrouping developmental disorders. Unique combina- schema besides severity of SSD should be ex- tions of comorbid conditions may require dif- amined, as they might yield different results. ferent treatment strategies, result in diverse One possibility is subgrouping SSD by specific outcomes, and represent differing genetic cognitive skill deficits or endophenotypes, in- bases. Molecular genetic studies are needed cluding oral motor skills, phonological mem- to identify genetic subgroups of SSD with var- ory, vocabulary, speeded naming, and phono- ious comorbidities. Ultimately, the identifica- logical awareness skills (Lewis et al., 2011). tion of pleiotropic and unique genes may re- Another subtyping schema, such as the one sult in uncovering neural networks that un- proposed by Dodd (2005), which is based on derlie these comorbidities.

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