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Specific Neurological Phenotypes in Autism Spectrum Disorders Are Associated with Sex Representation RESEARCH ARTICLE

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Specific Neurological Phenotypes in Autism Spectrum Disorders Are Associated with Sex Representation RESEARCH ARTICLE RESEARCH ARTICLE Specific Neurological Phenotypes in Autism Spectrum Disorders Are Associated with Sex Representation Esther Ben-Itzchak, Shay Ben-Shachar, and Ditza A. Zachor Autism spectrum disorder (ASD) is a heritable disorder occurring predominantly in males. The aim of this study was to compare sex differences in the prevalence of specific neurological phenotypes commonly described in ASD. The study included 663 participants, aged 18 months to 15 years, diagnosed with ASD. Neurological and behavioral assessments were performed using standardized tests, and obtaining medical, developmental, and familial histories from the parents. Phenotypes under investigation were macro- and microcephaly, developmental regression, minor neurological and musculoskeletal deficits (MNMD), and seizures. Male : female ratio in the ASD group was 6.7:1. No sex differences in autism severity, cognitive ability, and adaptive functioning were noted. Mean head circumference percentile for males (50.1 ± 25.6) was significantly larger than females (43.4 ± 30.2). Micro- and macrocephaly were more frequent in ASD than expected (5.9%; 18.1%, respectively). Microcephaly in females (15.1%) was significantly more prevalent than in males (4.5%). The prevalence of macrocephaly in both sexes did not differ significantly. Regression was noted in 30.2% of the females with ASD, significantly higher than in males (18.9%). MNMD was documented in 73.8% of the females, significantly higher than in males (57.1%). M:F ratio decreased in a group with two or more phenotypes (3.6:1), while male predominance was more significant in the group without phenotypes (13.6:1). Neurological phenotypes associated with ASD are more prevalent in females than in males, resulting in more complex clinical and neurological manifesta- tions in females. Therefore, involvement of different etiologies is suggested in ASD in females. Autism Res 2013, ••: ••–••. © 2013 International Society for Autism Research, Wiley Periodicals, Inc. Keywords: autism spectrum disorder; male:female ratio; microcephaly; macrocephaly; developmental regression, minor neurological and musculoskeletal deficits, seizures. Introduction Minderaa, & Hadders-Algra, 2011; Ming, Brimacombe, & Wagner, 2007]. The most commonly reported neurologi- Autism spectrum disorders (ASD) are a group of neuro- cal deficits were hypotonia, abnormal reflexes, and behavioral disorders characterized by a classic triad of cranial nerves dysfunction [De Jong et al., 2011]. Abnor- symptoms, including impaired social and communication mal neurological signs might indicate involvement of skills, and stereotyped behaviors. It is well accepted now multiple brain networks associated with ASD that may that ASD represents a heterogeneous group of conditions. affect neurological outcome. Epilepsy has been docu- It is not surprising, therefore, that some individuals show mented in about 5–46% of individuals with ASD in other phenotypes in addition to the core symptoms. ASD different studies, suggesting that autism and epilepsy is a highly heritable disorder, with heritability indices share a common neurobiological basis [Kagan-Kushnir, estimated at 60–92%, suggesting a major role for genetic Roberts, & Snead, 2005; Tuchman & Rapin, 2002]. factors in the etiology of ASD [Schaaf & Zoghbi, 2011]. Male predominance in ASD has been noted in all epi- Accelerated head growth and relative increased head demiological studies and is a well-established fact in the circumference have been documented in ASD in numer- field of ASD. The male : female (M:F) ratio has been ous studies [Courchesne & Pierce, 2005; Fombonne, Roge, reported in many studies in the range of 4–5:1 Claverie, Courty, & Fremolle, 1999; Minshew & Williams, [Fombonne, 2003; Holtmann, Bolte, & Poustka, 2007; 2007]. Developmental regression has been estimated at Newschaffer et al., 2007]. 15–30% in individuals with ASD [Baird et al., 2008; Parr In general, sex differences in autism severity and cog- et al., 2011]. Children with ASD are often described with nitive abilities have been examined in previous research. clumsiness and motor skills delay [Zachor, Ilanit, & Ben Studies looking at sex differences in autism severity Itzchak, 2010]. In addition, soft neurological signs were found conflicting results even when controlling for IQ. frequently documented in ASD [De Jong, Punt, De Groot, Several studies reported more severe symptoms in girls From the Department of Communication Disorders, Ariel University Center of Samaria, Ariel, Israel (E.B-I.); The Autism Center, Department of Pediatrics, Assaf Harofeh Medical Center, Zerifin, Israel (E.B-I., D.A.Z.); The Genetic Institute, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel (S.B-S.);TelAviv University, Tel-Aviv, Israel (D.A.Z.) Received July 31, 2012; accepted for publication June 17, 2013 Address for correspondence and reprints: Esther Ben-Itzchak, The Autism Center, Assaf Harofeh Medical Center, Zerifin 70300, Israel. E-mail: [email protected] Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1319 © 2013 International Society for Autism Research, Wiley Periodicals, Inc. INSAR Autism Research ••: ••–••, 2013 1 comparing to boys especially in the communication The study included 690 participants who underwent a domain [Carter et al., 2007; Hartley & Sikora, 2009], full diagnosis for ASD during the years 2002–2011. Par- while others reported that boys had more severe symp- ticipants younger than 18 months (n = 11) or with diag- toms especially in repetitive stereotyped behaviors noses of specific syndromes (n = 16) were excluded from [Lord, Schopler, & Revicki, 1982; Mandy et al., 2012; the study. The final cohort included 663 participants (577 McLennan, Lord, & Schopler, 1993; Szatmari et al., 2012]. males, 86 females) within the age range of 18 months to Others found no sex differences in autism symptom 15 years. (M = 44.1 m. ± 28.7) diagnosed with ASD. Of severity [Holtmann et al., 2007; Pilowsky, Yirmiya, the cohort, 536 participants (80.8%) were 18 months to 5 Shulman, & Dover, 1998; Zwaigenbaum et al., 2012]. years old, 106 (15.9%) were between 5 and 10 years old, Earlier studies, especially those conducted prior to the use and 21 (3.3%) were older than 10 years. This research was of DSM-IV, found that females had higher rates of intel- approved by the institutional review board of the medical lectual disability compared with boys [Lord & Schopler, center as required. 1985; Volkmar, Szatmari, & Sparrow, 1993]. However several later studies did not find significant sex differ- Procedure ences [Mandy et al., 2012; Zwaigenbaum et al., 2012]. Dworzynski, Ronald, Bolton, and Happé [2012] reported Participants were referred to the autism center for a com- that girls, but not boys, meeting criteria for ASD showed prehensive assessment of a possible diagnosis of ASD. The more additional problems, such as low intellectual level evaluation included a neurological assessment, and and behavioral difficulties. Researchers suggested sex bias behavioral, cognitive, and functional evaluations. Assess- in the diagnosis of ASD. In the absence of additional ments were conducted by a skilled interdisciplinary team. intellectual or behavioral problems, girls are less likely Pediatric neurologists obtained medical, developmental, than boys to meet diagnostic criteria for ASD at equiva- and familial histories from the parents, and conducted a lently high levels of autistic-like traits. comprehensive neurological examination of all the Only a few studies have examined the association participants. between M:F ratio and specific neurological phenotypes The diagnosis of autism/ASD was obtained by using in ASD. For example, Miles, Hadden, Takahashi, and two standardized tests: the Autism Diagnosis Interview- Hillman [2000] tested 137 individuals with autism, and Revised (ADI-R) [Rutter, Le Couteur, & Lord, 2003] and found no significant difference in sex ratio between the Autism Diagnosis Observation Schedule (ADOS) normocephalic (M:F 6.9:1) and macrocephalic (M:F 4.3:1) [Lord, Rutter, DiLavore, & Risi, 1999], and by meeting individuals. However, they did find that sex ratio was criteria for autism/ASD based on DSM-IV [American closer to normal (M:F 1.5:1) in individuals with micro- Psychiatric Association, 1994]. All the professionals cephaly. Epilepsy in ASD was associated with sex (female) involved in the diagnostic process established reliability [Amiet et al., 2008; Steffenburg & Gillberg, 1986; as required. Cognitive and developmental abilities (IQ/ Tuchman, Rapin, & Shinnar, 1991] and with intellectual DQ) were assessed using the Mullen Scales of Early Learn- disability [Amiet et al., 2008; Bolton et al., 2011]. ing (Mullen, 1995) , Bayley Scales of Infant Development However, the M:F ratio has not been specifically exam- (Bayley, 1993), Wechsler Preschool and Primary Scale of ined in the subpopulation of ASD and epilepsy. Further- Intelligence (Wechsler, 1989), Stanford–Binet Intelligence more, previous studies have not described M:F ratio Scales (Thorndike, Hagen, & Sattler, 1986), Kaufman differences in ASD with developmental regression [Parr Assessment Battery for Children-II (Kaufman, 1983), or et al., 2011; Shumway et al., 2011]. Wechsler Intelligence Scale for Children III and IV As ASD occurs more frequently in males, we hypoth- (Wechsler, 2003), according to the child’s age and lan- esized that the relatively small group of females with ASD guage level. Since 2006, developmental and cognitive may have a different clinical expression
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