What About the Girls? Sex-Based Differences in Autistic Traits and Adaptive Skills
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There is growing evidence of a camouflaging effect among females with autism spectrum disorder (ASD), particularly among those without intellectual disability, which may affect performance on gold-standard diagnostic measures. This study utilized an age- and IQ-matched sample of school-aged youth (n = 228) diagnosed with ASD to assess sex differences on the ADOS and ADI-R, parent-reported autistic traits, and adaptive skills. Although females and males were rated similarly on gold-standard diagnostic measures overall, females with higher IQs were less likely to meet criteria on the ADI-R. Females were also found to be significantly more impaired on parent reported autistic traits and adaptive skills. Overall, the findings suggest that some autistic females may be missed by current diagnostic procedures.
KeywordsAutism spectrum disorder Sex differences Diagnosis Adaptive skills
Funding for this project was provided by grants and financial support through several institutions, including: The Isadore and Bertha Gudelsky Family Foundation, Children’s National Health Institute IDDRC P30 HD040677, Pennsylvania State Department of Health, The Philadelphia Foundation, Pfizer, Robert Wood Johnson Foundation, Virginia Tech Center for Autism Research, and the National Institute of Child Health and Human Development (R03HD081070). We are grateful to the children and families who participated in this study.
ABR collected the data, ran the analyses, and wrote the paper. LK served as co-principal investigator for one site of the project, collected the data, helped design the analyses, and wrote the paper. BEY served as co-principal investigator for one site of the project, collected the data, provided feedback on analyses, and wrote the paper. JB provided insight and feedback on the interpretation of analyses and edited the paper. ATW collected the data and edited the paper. SWW served as co-principal investigator for one site of the project, collected the data, provided feedback on analyses, and edited the paper. GLW collected the data, helped design the analyses, and edited the paper. CP collected the data, provided feedback on analyses, and wrote the paper. RTS collected the data, provided feedback on analyses, and edited the paper. THO collected the data, provided feedback on analyses, and edited the paper. AS collected the data, provided feedback on analyses, and edited the paper. SS collected the data, managed the database, and edited the paper. KR-B provided feedback on analyses and edited the paper. AM served as co-principal investigator for one site of the project, collected the data, provided feedback on analyses, and edited the paper. LGA served as co-principal investigator for one site of the project, collected the data, helped design the analyses, and edited the paper.
Compliance with Ethical Standards
Conflict of interest
All authors declare no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.
- American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text revision). Washington, DC: American Psychiatric Association.Google Scholar
- Banach, R., Thompson, A., Szatmari, P., Goldberg, J., Tuff, L., Zwaigenbaum, L., & Mahoney, W. (2009). Brief report: Relationship between non-verbal IQ and Gender in Autism. Journal of Autism and Developmental Disorders, 39(1), 188–193. https://doi.org/10.1007/s10803-008-0612-4.CrossRefPubMedGoogle Scholar
- Bargiela, S., Steward, R., & Mandy, W. (2016). The experiences of late-diagnosed women with autism spectrum conditions: An investigation of the female autism phenotype. Journal of Autism and Developmental Disorders, 46(10), 3281–3294. https://doi.org/10.1007/s10803-016-2872-8.CrossRefPubMedPubMedCentralGoogle Scholar
- Begeer, S., Mandell, D., Wijnker-Holmes, B., Venderbosch, S., Rem, D., Stekelenburg, F., & Koot, H. M. (2013). Sex differences in the timing of identification among children and adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 43(5), 1151–1156. https://doi.org/10.1007/s10803-012-1656-z.CrossRefPubMedGoogle Scholar
- Bejerot, S., Eriksson, J. M., Bonde, S., Carlström, K., Humble, M. B., & Eriksson, E. (2012). The extreme male brain revisited: Gender coherence in adults with autism spectrum disorder. The British Journal of Psychiatry: The Journal of Mental Science, 201, 116–123. https://doi.org/10.1192/bjp.bp.111.097899.CrossRefGoogle Scholar
- Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, 57(1), 289–300. Retrieved from http://www.jstor.org/stable/2346101.
- Boat, T. F., & Wu, J. T. (Eds.). (2015). Prevalence of autism spectrum disorder. In Mental disorders and disabilities among low-income children (pp. 241–266). Washington, DC: The National Academies Press.Google Scholar
- Brown, L. (2011). Identity-first language/autistic self advocacy network. Retrieved May 26, 2017, from http://autisticadvocacy.org/about-asan/identity-first-language/.
- Chawarska, K., Paul, R., Klin, A., Hannigen, S., Dichtel, L. E., & Volkmar, F. (2007). Parental recognition of developmental problems in toddlers with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(1), 62–72. https://doi.org/10.1007/s10803-006-0330-8.CrossRefPubMedGoogle Scholar
- Cohen, J. (1988). Statistical power and analysis for the behavioral sciences (2nd ed.). Hillsdale: Lawrence Erlbaum Associates, Inc.Google Scholar
- Constantino, J. N., & Gruber, C. (2012). The Social Responsiveness Scale Manual, Second Edition (SRS-2). Los Angeles: Western Psychological Services.Google Scholar
- Constantino, J. N., & Gruber, C. P. (2005). Social responsiveness scale (SRS). Los Angeles: Western Psychological Services.Google Scholar
- Cridland, E. K., Jones, S. C., Caputi, P., & Magee, C. A. (2014). Being a girl in a boys’ world: Investigating the experiences of girls with autism spectrum disorders during adolescence. Journal of Autism and Developmental Disorders, 44(6), 1261–1274. https://doi.org/10.1007/s10803-013-1985-6.CrossRefPubMedGoogle Scholar
- Elliot, C. D. (2007). Differential Ability Scales–Second Edition (DAS-II). San Antonio, TX: Harcourt Assessment.Google Scholar
- Frazier, T. W., Georgiades, S., Bishop, S. L., & Hardan, A. Y. (2014a). Behavioral and cognitive characteristics of females and males with autism in the simons simplex collection. Journal of the American Academy of Child & Adolescent Psychiatry, 53(3), 329–340. https://doi.org/10.1016/j.jaac.2013.12.004.CrossRefGoogle Scholar
- Frazier, T. W., Ratliff, K. R., Gruber, C., Zhang, Y., Law, P. A., & Constantino, J. N. (2014b). Confirmatory factor analytic structure and measurement invariance of quantitative autistic traits measured by the social responsiveness scale-2. Autism: The International Journal of Research and Practice, 18(1), 31–44. https://doi.org/10.1177/1362361313500382.CrossRefGoogle Scholar
- Giarelli, E., Wiggins, L. D., Rice, C. E., Levy, S. E., Kirby, R. S., Pinto-Martin, J., & Mandell, D. (2010). Sex differences in the evaluation and diagnosis of autism spectrum disorders among children. Disability and Health Journal, 3(2), 107–116. https://doi.org/10.1016/j.dhjo.2009.07.001.CrossRefPubMedGoogle Scholar
- Gilman, S. R., Iossifov, I., Levy, D., Ronemus, M., Wigler, M., & Vitkup, D. (2011). Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron, 70(5), 898–907. https://doi.org/10.1016/j.neuron.2011.05.021.CrossRefPubMedPubMedCentralGoogle Scholar
- Halladay, A. K., Bishop, S., Constantino, J. N., Daniels, A. M., Koenig, K., Palmer, K., … Szatmari, P. (2015). Sex and gender differences in autism spectrum disorder: Summarizing evidence gaps and identifying emerging areas of priority. Molecular Autism, 6(1), 36. https://doi.org/10.1186/s13229-015-0019-y.CrossRefPubMedPubMedCentralGoogle Scholar
- Hartley, S. L., & Sikora, D. M. (2009). Sex differences in autism spectrum disorder: An examination of developmental functioning, autistic symptoms, and coexisting behavior problems in toddlers. Journal of Autism and Developmental Disorders, 39(12), 1715–1722. https://doi.org/10.1007/s10803-009-0810-8.CrossRefPubMedPubMedCentralGoogle Scholar
- Howe, Y. J., O’Rourke, J. A., Yatchmink, Y., Viscidi, E. W., Jones, R. N., & Morrow, E. M. (2015). Female autism phenotypes investigated at different levels of language and developmental abilities. Journal of Autism and Developmental Disorders, 45(11), 3537–3549. https://doi.org/10.1007/s10803-015-2501-y.CrossRefPubMedPubMedCentralGoogle Scholar
- Jacquemont, S., Coe, B. P., Hersch, M., Duyzend, M. H., Krumm, N., Bergmann, S., … Eichler, E. E. (2014). A higher mutational burden in females supports a “female protective model” in neurodevelopmental disorders. American Journal of Human Genetics, 94(3), 415–425. https://doi.org/10.1016/j.ajhg.2014.02.001.CrossRefPubMedPubMedCentralGoogle Scholar
- Kanne, S. M., Gerber, A. J., Quirmbach, L. M., Sparrow, S. S., Cicchetti, D. V., & Saulnier, C. A. (2011). The role of adaptive behavior in autism spectrum disorders: Implications for functional outcome. Journal of Autism and Developmental Disorders, 41(8), 1007–1018. https://doi.org/10.1007/s10803-010-1126-4.CrossRefPubMedGoogle Scholar
- Kataoka, S., Takuma, K., Hara, Y., Maeda, Y., Ago, Y., & Matsuda, T. (2013). Autism-like behaviours with transient histone hyperacetylation in mice treated prenatally with valproic acid. The International Journal of Neuropsychopharmacology, 16(1), 91–103. https://doi.org/10.1017/S1461145711001714.CrossRefPubMedGoogle Scholar
- Klin, A., Saulnier, C. A., Sparrow, S. S., Cicchetti, D. V., Volkmar, F. R., & Lord, C. (2007). Social and communication abilities and disabilities in higher functioning individuals with autism spectrum disorders: The Vineland and the ADOS. Journal of Autism and Developmental Disorders, 37(4), 748–759. https://doi.org/10.1007/s10803-006-0229-4.CrossRefPubMedGoogle Scholar
- Kreiser, N., & White, S. (2014). ASD in females: Are we overstating the gender difference in diagnosis? Clinical Child and Family Psychology Review. Retrieved from http://link.springer.com/article/https://doi.org/10.1007/s10567-013-0148-9.
- Lai, M.-C., Baron-Cohen, S., & Buxbaum, J. D. (2015). Understanding autism in the light of sex/gender. Molecular Autism, 6(1). https://doi.org/10.1186/s13229-015-0021-4.
- Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism Diagnostic Observation Schedule–2nd Edition (ADOS-2). Los Angeles: Western Psychological Corporation.Google Scholar
- Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. S. (2001). Autism Diagnostic Observation Schedule: Manual. Los Angeles: Western Psychological Services.Google Scholar
- Mandic-Maravic, V., Pejovic-Milovancevic, M., Mitkovic-Voncina, M., Kostic, M., Aleksic-Hil, O., Radosavljev-Kircanski, J., … Lecic-Tosevski, D. (2015). Sex differences in autism spectrum disorders: Does sex moderate the pathway from clinical symptoms to adaptive behavior? Scientific Reports, 5, 10418. https://doi.org/10.1038/srep10418.CrossRefPubMedPubMedCentralGoogle Scholar
- Mandy, W., Chilvers, R., Chowdhury, U., Salter, G., Seigal, A., & Skuse, D. (2012). Sex differences in autism spectrum disorder: Evidence from a large sample of children and adolescents. Journal of Autism and Developmental Disorders, 42(7), 1304–1313. https://doi.org/10.1007/s10803-011-1356-0.CrossRefPubMedGoogle Scholar
- Messinger, D. S., Young, G. S., Webb, S. J., Ozonoff, S., Bryson, S. E., Carter, A., … Zwaigenbaum, L. (2015). Early sex differences are not autism-specific: A Baby Siblings Research Consortium (BSRC) study. Molecular Autism, 6(1). https://doi.org/10.1186/s13229-015-0027-y.
- Øien, R. A., Hart, L., Schjølberg, S., Wall, C. A., Kim, E. S., Nordahl-Hansen, A., … Shic, F. (2017). Parent-endorsed sex differences in toddlers with and without ASD: Utilizing the M-CHAT. Journal of Autism and Developmental Disorders, 47(1), 126–134. https://doi.org/10.1007/s10803-016-2945-8.CrossRefPubMedGoogle Scholar
- Pilowsky, T., Yirmiya, N., Shulman, C., & Dover, R. (1998). The autism diagnostic interview-revised and the childhood autism rating scale: Differences Between diagnostic systems and comparison between genders. Journal of Autism and Developmental Disorders, 28(2), 143–151. https://doi.org/10.1023/A:1026092632466.CrossRefPubMedGoogle Scholar
- Pine, D. S., Guyer, A. E., Goldwin, M., Towbin, K. A., & Leibenluft, E. (2008). Autism spectrum disorder scale scores in pediatric mood and anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 47(6), 652–661. https://doi.org/10.1097/CHI.0b013e31816bffa5.CrossRefPubMedPubMedCentralGoogle Scholar
- Pugliese, C. E., Anthony, L., Strang, J. F., Dudley, K., Wallace, G. L., & Kenworthy, L. (2015). Increasing adaptive behavior skill deficits from childhood to adolescence in autism spectrum disorder: Role of executive function. Journal of Autism and Developmental Disorders, 45, 1579–1587. https://doi.org/10.1007/s10803-014-2309-1.CrossRefPubMedPubMedCentralGoogle Scholar
- Reinhardt, V. P., Wetherby, A. M., Schatschneider, C., & Lord, C. (2015). Examination of sex differences in a large sample of young children with autism spectrum disorder and typical development. Journal of Autism and Developmental Disorders, 45(3), 697–706. https://doi.org/10.1007/s10803-014-2223-6.CrossRefPubMedPubMedCentralGoogle Scholar
- Rutter, M., Le Couteur, A., & Lord, C. (2003). Autism diagnostic interview-revised (Vol. 29, p. 30). Los Angeles: Western Psychological Services.Google Scholar
- Schoch, H., Kreibich, A. S., Ferri, S. L., White, R. S., Bohorquez, D., Banerjee, A., … Brodkin, E. S. (2017). Sociability deficits and altered amygdala circuits in mice lacking Pcdh10, an autism associated gene. Biological Psychiatry, 81(3), 193–202. https://doi.org/10.1016/j.biopsych.2016.06.008.CrossRefPubMedGoogle Scholar
- Shattuck, P. T., Durkin, M., Maenner, M., Newschaffer, C., Mandell, D. S., Wiggins, L., … Cuniff, C. (2009). Timing of identification among children with an autism spectrum disorder: Findings from a population-based surveillance study. Journal of the American Academy of Child & Adolescent Psychiatry, 48(5), 474–483. https://doi.org/10.1097/CHI.0b013e31819b3848.CrossRefGoogle Scholar
- Sparrow, S. S., Balla, D. A., & Cicchetti, D. V. (2005). Vineland-II adaptive behavior scales. Circle Pines: AGS Publishing.Google Scholar
- Strang, J. F., Kenworthy, L., Dominska, A., Sokoloff, J., Kenealy, L. E., Berl, M., … Wallace, G. L. (2014). Increased gender variance in autism spectrum disorders and attention deficit hyperactivity disorder. Archives of Sexual Behavior, 43(8), 1525–1533. https://doi.org/10.1007/s10508-014-0285-3.CrossRefPubMedGoogle Scholar
- Trubanova, A., Donlon, K., Kreiser, N. L., Ollendick, T. H., & White, S. W. (2014). Under-identification of ASD in females: A case series illustrating the unique presentation of ASD in young adult females. Scandinavian Journal of Child and Adolescent Psychiatry and Psychology, 2(2), 66–76.CrossRefGoogle Scholar
- Van Wijngaarden-Cremers, P. J. M., van Eeten, E., Groen, W. B., Van Deurzen, P. A., Oosterling, I. J., & Van der Gaag, R. J. (2014). Gender and age differences in the core triad of impairments in autism spectrum disorders: A systematic review and meta-analysis. Journal of Autism and Developmental Disorders, 44(3), 627–635. https://doi.org/10.1007/s10803-013-1913-9.CrossRefPubMedGoogle Scholar
- Volkmar, F., Sparrow, S. S., Goudreau, D., Cicchetti, D. V., Paul, R., & Cohen, D. J. (1987). Social deficits in autism: An operational approach using the Vineland Adaptive Behavior Scales. Journal of the American Academy of Child & Adolescent Psychiatry, 26(2), 156–161. https://doi.org/10.1097/00004583-198703000-00005.CrossRefGoogle Scholar
- Wechsler, D. (2003). Wechsler Intelligence Scale for Children–Fourth Edition (WISC-IV). San Antonio, TX: The Psychological Corporation.Google Scholar
- Wechsler, D. (2008). Wechsler Adult Intelligence Scale-Fourth Edition (WAIS-IV). San Antonio, TX: The Psychological Corporation-Pearson.Google Scholar
- Wechsler, D. (2011). Wechsler abbreviated scale of intelligence–Second edition (WASI-II). San Antonio, TX: NCS Pearson.Google Scholar
- Wechsler, D. (2014). WPPSI-IV: Wechsler Preschool and Primary Scale of Intelligence-Fourth Edition technical and interpretive manual. San Antonio, TX: Pearson.Google Scholar
- Wechsler, D. (2014). Wechsler Intelligence Scale for Children–Fifth Edition (WISC-V). Bloomington, MN: The Psychological Corporation.Google Scholar
- Wechsler, D., & Hsiao-pin, C. (2011). WASI-II: Wechsler abbreviated scale of intelligence. Bloomington: Pearson.Google Scholar
- Yerys, B. E., Wallace, G. L., Sokoloff, J. L., Shook, D. A., James, J. D., & Kenworthy, L. (2009). Attention deficit/hyperactivity disorder symptoms moderate cognition and behavior in children with autism spectrum disorders. Autism Research: Official Journal of the International Society for Autism Research, 2(6), 322–333. https://doi.org/10.1002/aur.103.Google Scholar