Abstract
Discernment of possible sex-based variations in presentations of autism spectrum disorder (ASD) symptoms is limited by smaller female samples with ASD and confounds with ASD ascertainment. A large national cohort of individuals with autism, SPARK, allowed parent report data to be leveraged to examine whether intrinsic child characteristics and extrinsic factors differentially impact males and females with ASD. Small but consistent sex differences in individuals with ASD emerged related to both intrinsic and extrinsic factors, with different markers for males and females. Language concerns in males may make discernment of ASD more straightforward, while early motor concerns in females may hamper diagnosis as such delays are not identified within traditional ASD diagnostic criteria.
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References
Alexander, G. M., & Wilcox, T. (2012). Sex differences in early infancy. Child Development Perspectives, 6(4), 400–406. https://doi.org/10.1111/j.1750-8606.2012.00247.x
American Psychiatric Association. (2013). DSM-5 diagnostic classification. Diagnostic and Statistical Manual of Mental Disorders. https://doi.org/10.1176/appi.books.9780890425596.x00diagnosticclassification
Angell, A. M., Deavenport-Saman, A., Yin, L., Zou, B., Bai, C., Varma, D., & Solomon, O. (2021). Sex differences in co-occurring conditions among autistic children and youth in Florida: A retrospective cohort study (2012–2019). Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-020-04841-5
Backer van Ommeren, T., Koot, H. M., Scheeren, A. M., & Begeer, S. (2017). Sex differences in the reciprocal behaviour of children with autism. Autism, 21(6), 795–803. https://doi.org/10.1177/1362361316669622
Baio, J. (2012). Prevalence of autism spectrum disorders: Autism and developmental disabilities monitoring network, 14 sites, United States, 2008. Autism Spectrum Disorders: Guidance, Research and Federal Activity, 61(3), 1–19.
Bakeman, R. (2005). Reccomended effect size statistics for repeated measures design. Behavioral Research Methods, 37(3), 379–384. https://doi.org/10.3758/BF03192707
Becerra-Culqui, T. A., Lynch, F. L., Owen-Smith, A. A., Spitzer, J., & Croen, L. A. (2018). Parental first concerns and timing of autism spectrum disorder diagnosis. Journal of Autism and Developmental Disorders, 48(10), 3367–3376. https://doi.org/10.1007/s10803-018-3598-6
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, 1151–1156. https://doi.org/10.1007/s10803-012-1656-z
Beggiato, A., Peyre, H., Maruani, A., Scheid, I., Rastam, M., Amsellem, F., Gillberg, C. I., Leboyer, M., Bourgeron, T., Gillberg, C., & Delorme, R. (2017). Gender differences in autism spectrum disorders Divergence among specific core symptoms. Autism Research, 1014, 680–689. https://doi.org/10.1002/aur.1715
Bishop-Fitzpatrick, L., & Kind, A. J. (2017). A scoping review of health disparities in autism spectrum disorder. Journal of Autism and Developmental Disorders, 47(11), 3380–3391. https://doi.org/10.1007/s10803-017-3251-9
Chandler, S., Charman, T., Baird, G., Simonoff, E., Loucas, T., Meldrum, D., Scott, M., & Pickles, A. (2007). Validation of the Social Communication Questionnaire in a population cohort of children with autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 46(10), 1324–1332. https://doi.org/10.1097/chi.0b013e31812f7d8d
Cohen, J. (1988). Statistical Power of Analysis for the Behavioral Sciences (2nd Edition). Erlbaum.
Crane, L., Chester, J. W., Goddard, L., Henry, L. A., & Hill, E. (2016). Experiences of autism diagnosis: A survey of over 1000 parents in the United Kingdom. Autism, 20(2), 153–162. https://doi.org/10.1177/1362361315573636
Daniels, A. M., Rosenberg, R. E., Anderson, C., Law, J. K., Marvin, A. R., & Law, P. A. (2012). Verification of parent-report of child autism spectrum disorder diagnosis to a web-based autism registry. Journal of Autism and Developmental Disorders, 42, 257–265. https://doi.org/10.1007/s10803-011-1236-7
Dean, M., Harwood, R., & Kasari, C. (2017). The art of camouflage: Gender differences in the social behaviors of girls and boys with autism spectrum disorder. Autism, 21(6), 678–689. https://doi.org/10.1177/1362361316671845
Durkin, M. S., Maenner, M. J., Meaney, F. J., Levy, S. E., DiGuiseppi, C., Nicholas, J. S., Kirby, R. S., Pinto-Martin, J. A., & Schieve, L. A. (2010). Socioeconomic inequality in the prevalence of autism spectrum disorder: evidence from a US cross-sectional study. PLoS ONE, 5(7), e11551.
Dworzynski, K., Ronald, A., Bolton, P., & Happé, F. (2012). How different are girls and boys above and below the diagnostic threshold for autism spectrum disorders? Journal of the American Academy of Child and Adolescent Psychiatry, 51(8), 788–797. https://doi.org/10.1016/j.jaac.2012.05.018
Estrin, G. L., Milner, V., Spain, D., Happé, F., & Colvert, E. (2020). Barriers to autism spectrum disorder diagnosis for young women and girls: A systematic review. Review Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s40489-020-00225-8
Feliciano, P., Daniels, A. M., Green Snyder, L. A., Beaumont, A., Camba, A., Esler, A., Gulsrud, A. G., Mason, A., Gutierrez, A., Nicholson, A., Paolicelli, A. M., McKenzie, A. P., Rachubinski, A. L., Stephens, A. N., Simon, A. R., Stedman, A., Shocklee, A. D., Swanson, A., Finucane, B., & Chung, W. K. (2018). SPARK: A US Cohort of 50,000 families to accelerate autism research. Neuron, 89(3), 488–493. https://doi.org/10.1016/j.neuron.2018.01.015
Ferri, S. L., Abel, T., & Brodkin, E. S. (2018). Sex differences in autism spectrum disorder: a review. Current Psychiatry Reports. https://doi.org/10.1007/s11920-018-0874-2
Frazier, T. W., & Hardan, A. Y. (2017). Equivalence of symptom dimensions in females and males with autism. Autism, 21(6), 749–759. https://doi.org/10.1177/1362361316660066
Gabis, L. V., Attia, O. L., Roth-Hanania, R., & Foss-Feig, J. (2020). Motor delay- An Early and more common “red flag” in girls rather than boys with autism spectrum disorder. Research in Developmental Disabilities. https://doi.org/10.1016/j.ridd.2020.103702
Halladay, A. K., Bishop, S., Constantino, J. N., Daniels, A. M., Koenig, K., Palmer, K., Messinger, D., Pelphrey, K., Sanders, S. J., Singer, A. T., Taylor, J. L., & Szatmari, P. (2015). Sex and gender differences in autism spectrum disorder: Summarizing evidence gaps and identifying emerging areas of priority. Molecular Autism. https://doi.org/10.1186/s13229-015-0019-y
Harrop, C., Libsack, E., Bernier, R., Dapretto, M., Jack, A., McPartland, J. C., Van Horn, J.D., Webb, S.J., Pelphrey, K., & GENDAAR Consortium. (2021). Do Biological Sex and Early Developmental Milestones Predict the Age of First Concerns and Eventual Diagnosis in Autism Spectrum Disorder? Autism Research, 14(1), 156–168.
Ingram, D. D., & Franco, S. J. (2014). 2013 NCHS urban-rural classification scheme for counties. Vital and Health Statistics, Series 2: Data Evaluation and Methods Research.
Jensen, C. M., Steinhausen, H. C., & Lauritsen, M. B. (2014). Time trends over 16 years in incidence-rates of autism spectrum disorders across the lifespan based on nationwide Danish register data. Journal of Autism and Developmental Disorders, 44, 1808–1818. https://doi.org/10.1007/s10803-014-2053-6
Kaat, A. J., Shui, A. M., Ghods, S. S., Farmer, C. A., Esler, A. N., Thurm, A., & Georgiades, S. (2021). Sex differences in scores on standardized measaures of autism symptoms: A Multisite integrative data analysis. The Journal of Child Psychology and Psychiatry, 62(1), 97–106. https://doi.org/10.1111/jcpp.13242
Kreiser, N. L., & White, S. W. (2014). ASD in females: are we overstating the gender difference in diagnosis? Clinical Child and Family Psychology Review, 17, 67–84. 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. https://doi.org/10.1186/s13229-015-0021-4
Lai, M. C., Lombardo, M. V., Auyeung, B., Chakrabarti, B., & Baron-Cohen, S. (2015). Sex/gender differences and autism: setting the scene for future research. Journal of the American Academy of Child and Adolescent Psychiatry, 54(1), 11–24. https://doi.org/10.1016/j.jaac.2014.10.003
Lai, M. C., Lombardo, M. V., Ruigrok, A. N. V., Chakrabarti, B., Auyeung, B., Szatmari, P., Happé, F., & Baron-Cohen, S. (2017). Quantifying and exploring camouflaging in men and women with autism. Autism, 21(6), 690–702. https://doi.org/10.1177/1362361316671012
Lee, L. C., David, A. B., Rusyniak, J., Landa, R., & Newschaffer, C. J. (2007). Performance of the social communication questionnaire in children receiving preschool special education services. Research in Autism Spectrum Disorders, 1(2), 126–138. https://doi.org/10.1016/j.rasd.2006.08.004
Lee, H., Marvin, A. R., Watson, T., Piggot, J., Law, J. K., Law, P. A., Constantino, J. N., & Nelson, S. F. (2010). Accuracy of phenotyping of autistic children based on internet implemented parent report. American Journal of Medical Genetics, Part b: Neuropsychiatric Genetics, 153B(6), 1119–1126. https://doi.org/10.1002/ajmg.b.31103
Lehnhardt, F.-G., Gawronski, A., Pfeiffer, K., Kockler, H., Schilbach, L., & Vogeley, K. (2013). The investigation and differential diagnosis of asperger syndrome in adults. Deutsches Aerzteblatt Online., 110(45), 755–763. https://doi.org/10.3238/arztebl.2013.0755
Levine, T. R., & Hullett, C. R. (2002). Eta squared, partial eta squared, and misreporting of effect size in communication research. Human Communication Research, 28(4), 612–625.
Licari, M. K., Alvares, G. A., Varcin, K., Evans, K. L., Cleary, D., Reid, S. L., & Whitehouse, A. J. (2020). Prevalence of motor difficulties in autism spectrum disorder: Analysis of a population-based cohort. Autism Research, 13(2), 298–306. https://doi.org/10.1002/aur.2230
Little, L. M., Wallisch, A., Salley, B., & Jamison, R. (2017). Do early caregiver concerns differ for girls with autism spectrum disorders? Autism, 21(6), 728–732. https://doi.org/10.1177/1362361316664188
Loomes, R., Hull, L., & Mandy, W. P. L. (2017). What is the male-to-female ratio in autism spectrum disorder? A systematic review and Meta-analysis. Journal of the American Academy of Child and Adolescent Psychiatry, 56(6), 466–474. https://doi.org/10.1016/j.jaac.2017.03.013
Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659–685. https://doi.org/10.1007/BF02172145
Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., Dilavore, P. C., Pickles, A., & Rutter, M. (2000). The Autism Diagnostic Observation Schedule-Generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205–223. https://doi.org/10.1023/A:1005592401947
Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism Diagnostic Observation Schedule, (ADOS-2) Modules 1–4. Western Psychology Publishing.
Mandy, W., & Lai, M. C. (2017). Towards sex- and gender-informed autism research. Autism, 21(6), 643–645. https://doi.org/10.1177/1362361317706904
Monz, B. U., Houghton, R., Law, K., & Loss, G. (2019). Treatment patterns in children with autism in the United States. Autism Research, 12(3), 517–526. https://doi.org/10.1002/aur.2070
Nguyen, C. T., Krakowiak, P., Hansen, R., Hertz-Picciotto, I., & Angkustsiri, K. (2016). Sociodemographic disparities in intervention service utilization in families of children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 46(12), 3729–3738.
Ozonoff, S., Young, G. S., Landa, R. J., Brian, J., Bryson, S., Charman, T., Chawarska, K., Macari, S. L., Messinger, D., Stone, W. L., Zwaigenbaum, L., & Iosif, A. M. (2015). Diagnostic stability in young children at risk for autism spectrum disorder: A baby siblings research consortium study. Journal of Child Psychology and Psychiatry, 56(9), 988–998. https://doi.org/10.1111/jcpp.12421
Ozonoff, S., Li, D., Deprey, L., Hanzel, E. P., & Iosif, A. M. (2018). Reliability of parent recall of symptom onset and timing in autism spectrum disorder. Autism, 22(7), 891–896. https://doi.org/10.1177/1362361317710798
Pisula, E., Pudło, M., Słowińska, M., Kawa, R., Strząska, M., Banasiak, A., & Wolańczyk, T. (2017). Behavioral and emotional problems in high-functioning girls and boys with autism spectrum disorders: Parents’ reports and adolescents’ self-reports. Autism, 21(6), 738–748. https://doi.org/10.1177/1362361316675119
Ratto, A. B., Kenworthy, L., Yerys, B. E., Bascom, J., Wieckowski, A. T., White, S. W., & Anthony, L. G. (2018). What about the girls? Sex-based differences in autistic traits and adaptive skills. Journal of Autism and Developmental Disorders, 48(5), 1698–1711. https://doi.org/10.1007/s10803-017-3413-9
Roman-Urrestarazu, A., van Kessel, R., Allison, C., Matthews, F. E., Brayne, C., & Baron-Cohen, S. (2021). Association of race/ethnicity and social disadvantage with autism prevalence in 7 million school children in England. JAMA Pediatrics, 175, 210–2100.
Rutherford, M., McKenzie, K., Johnson, T., Catchpole, C., O’Hare, A., McClure, I., Forsyth, K., McCartney, D., & Murray, A. (2016). Gender ratio in a clinical population sample, age of diagnosis and duration of assessment in children and adults with autism spectrum disorder. Autism, 20(5), 628–634. https://doi.org/10.1177/1362361315617879
Rutter, M., Le Couteur, A., & Lord, C. (2003a). Autism Diagnostic Interview-Revised (ADI-R). Los Angeles: Western Psychological Services.
Rutter Bailey, A., Lord, C., & M. (2003b). Manual of the Social Communication Questionnaire. Western Psychology Publishing.
Rynkiewicz, A., Schuller, B., Marchi, E., Piana, S., Camurri, A., Lassalle, A., & Baron-Cohen, S. (2016). An investigation of the “female camouflage effect” in autism using a computerized ADOS-2 and a test of sex/gender differences. Molecular Autism. https://doi.org/10.1186/s13229-016-0073-0
Scharf, R. J., Scharf, G. J., & Stroustrup, A. (2016). Developmental milestones. Pediatrics in Review. https://doi.org/10.1542/pir.2014-0103
Tierney, S., Burns, J., & Kilbey, E. (2016). Looking behind the mask: Social coping strategies of girls on the autistic spectrum. Research in Autism Spectrum Disorders, 23, 73–83. https://doi.org/10.1016/j.rasd.2015.11.013
Uljarević, M., Hedley, D., Alvares, G. A., Varcin, K. J., & Whitehouse, A. J. (2017). Relationship between early motor milestones and severity of restricted and repetitive behaviors in children and adolescents with autism spectrum disorder. Autism Research, 10(6), 1163–1168. https://doi.org/10.1002/aur.1763
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, 627–635. https://doi.org/10.1007/s10803-013-1913-9
Wodka, E. L., Parish-Morris, J., Annett, R. D., Carpenter, L., Dillon, E., Michaelson, J., Kim, S.H., Landa, R.J., the Spark Consortium & Kanne, S. (2021). Co-occurring attention-deficit/hyperactivity disorder and anxiety disorders differentially affect males and females with autism. The Clinical Neuropsychologist. https://doi.org/10.1080/13854046.2021.1942554
Acknowledgements
We gratefully acknowledge the families who participated in SPARK and the aid and support of the Simon’s Foundation. We have no other contributors to mention here, nor any funding to report.
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Funding for the Senior Author: SPARK: Simons Foundation Powering Autism Research for Knowledge, Simons Foundation (SPARK #534041, ELW).
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All authors contributed to the study conception and design. Material preparation and secondary data analysis were performed by EW and ED. The first draft of the manuscript was written by ED and EW; SK and RL provided input into data analyses and editing initial drafts. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Dillon, E.F., Kanne, S., Landa, R.J. et al. Sex Differences in Autism: Examining Intrinsic and Extrinsic Factors in Children and Adolescents Enrolled in a National ASD Cohort. J Autism Dev Disord 53, 1305–1318 (2023). https://doi.org/10.1007/s10803-021-05385-y
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DOI: https://doi.org/10.1007/s10803-021-05385-y