Abstract
Purpose
The Social Responsiveness Scale (SRS) is frequently used in research settings to measure characteristics associated with autism spectrum disorders (ASD). A short version has been developed but not yet tested for certain properties of the full SRS, such as familiality. The purpose of this study was to determine if prior familiality findings for the full SRS can be replicated using the short form by measuring the associations of the parental Social Responsiveness Scale-Short Form (SRS-SF) scores with child ASD diagnoses and child SRS-SF scores.
Methods
We used a nested case–control study within a longitudinal cohort study design. Participants were selected from the Nurses’ Health Study II (NHS II). Cases were children of study participants who had been diagnosed with ASD, while controls had not been diagnosed with ASD and were frequency matched by year of birth to cases. 2144 out of 3161 eligible participants returned SRS forms for a child and at least one parent. Participants in NHS II completed SRS forms for their spouses and spouses completed SRS forms for NHS II participants. Parental SRS-SF scores were based on a subset of 16 questions from the SRS. ASD diagnosis among children was reported by the mothers and validated in a subset using the Autism Diagnostic Interview–Revised, as well as child SRS-SF scores.
Results
Children whose parents both had elevated SRS-SF scores (those in the top 20% of the study distribution) had a higher odds of ASD diagnosis than those who did not have elevated parental scores (OR 2.25; 95% CI 1.41, 3.58). Additionally, children whose fathers had elevated SRS-SF scores had a higher odds of ASD diagnosis (OR 2.18; 95% CI 1.60, 2.97) than those whose fathers scores were not elevated. In sex-stratified analyses, male children with elevated parental SRS-SF scores had a higher odds of ASD diagnosis than those who did not have elevated parental scores. These associations were not as evident among female children. Parental SRS-SF scores also predicted child SRS-SF scores among controls.
Conclusion
These findings are similar to prior findings for the full SRS and support the ability of the SRS-SF to capture familiality of ASD-related traits.
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References
Alemany, S., Blok, E., Jansen, P. R., Muetzel, R. L., & White, T. (2021). Brain morphology, autistic traits, and polygenic risk for autism: A population-based neuroimaging study. Autism Research, 14(10), 2085–2099. https://doi.org/10.1002/aur.2576
Ames, J. L., Burjak, M., Avalos, L. A., et al. (2023). Prenatal Exposure to Per- and Polyfluoroalkyl Substances and Childhood Autism-related Outcomes. Epidemiology, 34(3), 450–459. https://doi.org/10.1097/EDE.0000000000001587
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. Published online May 22, 2013. doi:https://doi.org/10.1176/APPI.BOOKS.9780890425596
Blanken, L. M. E., Mous, S. E., Ghassabian, A., Muetzel, R. L., Schoemaker, N. K., El Marroun, H., van der Lugt, A., Jaddoe, V. W. V., Hofman, A., Verhulst, F. C., Tiemeier, H., & White, T. (2015). Cortical morphology in 6- to 10-year old children with autistic traits: a population-based neuroimaging study. American Journal of Psychiatry, 172(5), 479–486. https://doi.org/10.1176/APPI.AJP.2014.14040482
Bölte, S. (2012). Brief report: the social responsiveness scale for adults (SRS-A): initial results in a German cohort. Journal of Autism and Developmental Disorders, 42(9), 1998–1999. https://doi.org/10.1007/s10803-011-1424-5
Bölte, S., Westerwald, E., Holtmann, M., Freitag, C., & Poustka, F. (2011). Autistic traits and autism spectrum disorders: the clinical validity of two measures presuming a continuum of social communication skills. Journal of Autism and Developmental Disorders, 41(1), 66. https://doi.org/10.1007/S10803-010-1024-9
Brandler WM, Antaki D, Gujral M, et al. 2018 Paternally inherited cis-regulatory structural variants are associated with autism. Science 360(6386): 327–331. Doi: https://doi.org/10.1126/SCIENCE.AAN2261/SUPPL_FILE/AAN2261_TABLES9.XLSX
Constantino JN, Gruber C. Social Responsiveness Scale. Second Edition. Western Psychological Services; 2012.
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., Metzger, L. M., Shoushtari, C. S., Splinter, R., & Reich, W. (2003). Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433. https://doi.org/10.1023/A:1025014929212
Constantino, J. N., Lajonchere, C., Lutz, M., et al. (2006). Autistic social impairment in the siblings of children with pervasive developmental disorders. American Journal of Psychiatry, 163(2), 294–296. https://doi.org/10.1176/appi.ajp.163.2.294
Constantino, J. N., & Todd, R. D. (2005). Intergenerational transmission of subthreshold autistic traits in the general population. Published Online. https://doi.org/10.1016/j.biopsych.2004.12.014
Constantino, J. N., Zhang, Y., Frazier, T., Abbacchi, A. M., & Law, P. (2010). Sibling recurrence and the genetic epidemiology of autism. American Journal of Psychiatry, 167(11), 1349–1356. https://doi.org/10.1176/APPI.AJP.2010.09101470
de La Marche, W., Noens, I., Luts, J., Scholte, E., van Huffel, S., & Steyaert, J. (2012). Quantitative autism traits in first degree relatives: Evidence for the broader autism phenotype in fathers, but not in mothers and siblings. Autism, 16(3), 247–260. https://doi.org/10.1177/1362361311421776
Donovan, A. P. A., & Basson, M. A. (2017). The neuroanatomy of autism - a developmental perspective. Journal of Anatomy, 230(1), 4–15. https://doi.org/10.1111/joa.12542
Duku, E., Vaillancourt, T., Szatmari, P., Georgiades, S., Zwaigenbaum, L., Smith, I. M., Bryson, S., Fombonne, E., Mirenda, P., Roberts, W., Volden, J., Waddell, C., Thompson, A., & Bennett, T. (2013). Investigating the measurement properties of the social responsiveness scale in preschool children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 43(4), 860–868. https://doi.org/10.1007/S10803-012-1627-4
Duvekot, J., van der Ende, J., Verhulst, F. C., & Greaves-Lord, K. (2015). The screening accuracy of the parent and teacher-reported social responsiveness scale (SRS): comparison with the 3Di and ADOS. Journal of Autism and Developmental Disorders, 45(6), 1658–1672. https://doi.org/10.1007/s10803-014-2323-3
Girault, J. B., Swanson, M. R., Meera, S. S., et al. (2020). Quantitative trait variation in ASD probands and toddler sibling outcomes at 24 months. Journal of Neurodevelopmental Disorders, 12(1), 5. https://doi.org/10.1186/s11689-020-9308-7
Hallmayer, J., Cleveland, S., Torres, A., et al. (2011). Genetic heritability and shared environmental factors among twin pairs with autism. Archives of General Psychiatry, 68(11), 1095–1102. https://doi.org/10.1001/archgenpsychiatry.2011.76
Ho, A., Todd, R. D., & Constantino, J. N. (2005). Brief report: autistic traits in twins vs. non-twins–a preliminary study. Journal of Autism and Developmental Disorders, 35(1), 129–133. https://doi.org/10.1007/s10803-004-1040-8
Hyseni, F., Blanken, L. M. E., Muetzel, R., Verhulst, F. C., Tiemeier, H., & White, T. (2019). Autistic traits and neuropsychological performance in 6- to-10-year-old children: A population-based study. Child Neuropsychology, 25(3), 352–369. https://doi.org/10.1080/09297049.2018.1465543
Katz, J., Reichenberg, A., & Kolevzon, A. (2021). Prenatal and perinatal metabolic risk factors for autism: A review and integration of findings from population-based studies. Current Opinion in Psychiatry, 34(2), 94–104. https://doi.org/10.1097/YCO.0000000000000673
Knapp, E. A., Kress, A. M., Parker, C. B., Page, G. P., McArthur, K., Gachigi, K. K., Alshawabkeh, A. N., Aschner, J. L., Bastain, T. M., Breton, C. V., Bendixsen, C. G., Brennan, P. A., Bush, N. R., Buss, C., Camargo, C. A., Catellier, D., Cordero, J. F., Croen, L., Dabelea, D., … on behalf of program collaborators for Environmental Influences on Child Health Outcomes. (2023). The Environmental Influences on Child Health Outcomes (ECHO)-Wide Cohort. American Journal of Epidemiology. https://doi.org/10.1093/aje/kwad071
Landa, R. J., Holman, K. C., & Garrett-Mayer, E. (2007). Social and communication development in toddlers with early and later diagnosis of autism spectrum disorders. Archives of General Psychiatry, 64(7), 853–864. https://doi.org/10.1001/archpsyc.64.7.853
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(5), 659–685. https://doi.org/10.1007/BF02172145
Lyall, K. (2023). What are quantitative traits and how can they be used in autism research? Autism Research. https://doi.org/10.1002/aur.2937
Lyall, K., Constantino, J. N., Weisskopf, M. G., Roberts, A. L., Ascherio, A., & Santangelo, S. L. (2014). Parental social responsiveness and risk of autism spectrum disorder in offspring. JAMA Psychiatry., 71(8), 936. https://doi.org/10.1001/JAMAPSYCHIATRY.2014.476
Lyall, K., Hosseini, M., Ladd-Acosta, C., et al. (2021). Distributional properties and criterion validity of a shortened version of the social responsiveness scale: results from the ECHO program and implications for social communication research. Journal of Autism and Developmental Disorders, 51(7), 2241–2253. https://doi.org/10.1007/s10803-020-04667-1
Lyall, K., Ning, X., Aschner, J. L., et al. (2022). Cardiometabolic Pregnancy Complications in Association With Autism-Related Traits as Measured by the Social Responsiveness Scale in ECHO. American Journal of Epidemiology, 191(8), 1407–1419. https://doi.org/10.1093/aje/kwac061
Lyall, K., Rando, J., Toroni, B., et al. (2022). Examining shortened versions of the Social Responsiveness Scale for use in autism spectrum disorder prediction and as a quantitative trait measure: Results from a validation study of 3–5 year old children. JCPP Advances. https://doi.org/10.1002/jcv2.12106
Marrus, N., Hall, L. P., Paterson, S. J., Elison, J. T., Wolff, J. J., Swanson, M. R., Parish-Morris, J., Eggebrecht, A. T., Pruett, J. R., Hazlett, H. C., Zwaigenbaum, L., Dager, S., Estes, A. M., Schultz, R. T., Botteron, K. N., Piven, J., & Constantino, J. N. (2018). Language delay aggregates in toddler siblings of children with autism spectrum disorder. Journal of Neurodevelopmental Disorders, 10(1), 29. https://doi.org/10.1186/s11689-018-9247-8
Messinger, D., Young, G. S., Ozonoff, S., Dobkins, K., Carter, A., Zwaigenbaum, L., Landa, R. J., Charman, T., Stone, W. L., Constantino, J. N., Hutman, T., Carver, L. J., Bryson, S., Iverson, J. M., Strauss, M. S., Rogers, S. J., & Sigman, M. (2013). Beyond autism: a baby siblings research consortium study of high-risk children at three years of age. Journal of the American Academy of Child & Adolescent Psychiatry, 52(3), 300–308. https://doi.org/10.1016/j.jaac.2012.12.011
Nayar, K., Sealock, J. M., Maltman, N., et al. (2021). Elevated Polygenic burden for autism spectrum disorder is associated with the broad autism phenotype in mothers of individuals with autism spectrum disorder. Biological Psychiatry, 89(5), 476–485. https://doi.org/10.1016/J.BIOPSYCH.2020.08.029/ATTACHMENT/6A8BB438-8F31-477A-B36B-982094936CFB/MMC2.XLSX
Page, J., Constantino, J. N., Zambrana, K., Martin, E., Tunc, I., Zhang, Y., Abbacchi, A., & Messinge, D. (2016). Quantitative autistic trait measurements index background genetic risk for ASD in Hispanic families. Molecular Autism. https://doi.org/10.1186/S13229-016-0100-1
Piven, J., Palmer, P., Jacobi, D., Childress, D., & Arndt, S. (1997). Broader autism phenotype: Evidence from a family history study of multiple-incidence autism families. American Journal of Psychiatry, 154(2), 185–190. https://doi.org/10.1176/ajp.154.2.185
Robinson, E. B., Pourcain, B. S., Anttila, V., et al. (2016). Genetic risk for autism spectrum disorders and neuropsychiatric variation in the general population HHS Public Access Author manuscript. Nature Genetics, 48(5), 552–555. https://doi.org/10.1038/ng.3529
Román, G. C., Ghassabian, A., Bongers-Schokking, J. J., et al. (2013). Association of gestational maternal hypothyroxinemia and increased autism risk. Annals of Neurology, 74(5), 733–742. https://doi.org/10.1002/ANA.23976
Ruzich, E., Allison, C., Smith, P., Ring, H., Auyeung, B., & Baron-Cohen, S. (2017). The Autism-Spectrum Quotient in Siblings of People With Autism. Autism Research, 10(2), 289–297. https://doi.org/10.1002/aur.1651
Sandin, S., Lichtenstein, P., Kuja-Halkola, R., Larsson, H., Hultman, C. M., & Reichenberg, A. (2014). The familial risk of autism. JAMA, 311(17), 1770–1777. https://doi.org/10.1001/jama.2014.4144
Schwichtenberg, A. J., Young, G. S., Sigman, M., Hutman, T., & Ozonoff, S. (2010). Can family affectedness inform infant sibling outcomes of autism spectrum disorders? Journal of Child Psychology and Psychiatry, 51(9), 1021–1030. https://doi.org/10.1111/J.1469-7610.2010.02267.X
Sharp, T. H., Elsabbagh, M., Pickles, A., & Bedford, R. (2023). The subcortical correlates of autistic traits in school-age children: A population-based neuroimaging study. Mol Autism., 14(1), 6. https://doi.org/10.1186/s13229-023-00538-5
Skogheim TS, Weyde KVF, Aase H, et al. 2021 Prenatal exposure to per- and polyfluoroalkyl substances (PFAS) and associations with attention-deficit/hyperactivity disorder and autism spectrum disorder in children. Environment Research 202: 111692. doi:https://doi.org/10.1016/j.envres.2021.111692
Skuse, D. H., & Gallagher, L. (2011). Genetic influences on social cognition. Pediatric Research, 69(5 Pt 2), 85R-91R. https://doi.org/10.1203/PDR.0b013e318212f562
Sturm, A., Kuhfeld, M., Kasari, C., & McCracken, J. T. (2017). Development and validation of an item response theory-based Social Responsiveness Scale short form. Journal of Child Psychology and Psychiatry., 58(9), 1053–1061. https://doi.org/10.1111/JCPP.12731
Virkud, Y. V., Todd, R. D., Abbacchi, A. M., Zhang, Y., & Constantino, J. N. (2009). Familial aggregation of quantitative autistic traits in multiplex versus simplex autism. American Journal of Medical Genetics. Part b, Neuropsychiatric Genetics, 150B(3), 328–334. https://doi.org/10.1002/ajmg.b.30810
Virkud, Y. V., Todd, R. D., Abbacchi, A. M., Zhang, Y., & Constantino, J. N. (2009). Familial aggregation of quantitative autistic traits in multiplex versus simplex autism. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 150B(3), 328–334. https://doi.org/10.1002/AJMG.B.30810
Wang, J., Lee, L. C., Chen, Y. S., & Hsu, J. W. (2012). Assessing autistic traits in a Taiwan preschool population: Cross-cultural validation of the Social Responsiveness Scale (SRS). Journal of Autism and Developmental Disorders, 42(11), 2450–2459. https://doi.org/10.1007/s10803-012-1499-7
Warrier, V., Zhang, X., Reed, P., et al. (2022). Genetic correlates of phenotypic heterogeneity in autism. Nature Genetics, 54(9), 1293–1304. https://doi.org/10.1038/s41588-022-01072-5
Werling, D. M., & Geschwind, D. H. (2013). Sex differences in autism spectrum disorders. Current Opinion in Neurology, 26(2), 146–153. https://doi.org/10.1097/WCO.0b013e32835ee548
Yang, D. Y. J., Beam, D., Pelphrey, K. A., Abdullahi, S., & Jou, R. J. (2016). Cortical morphological markers in children with autism: A structural magnetic resonance imaging study of thickness, area, volume, and gyrification. Mol Autism., 7, 11. https://doi.org/10.1186/s13229-016-0076-x
Acknowledgements
We would like to acknowledge the Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital as the home of the Nurses’ Health Study II.
Funding
This research was funded by the following grants: National Institutes of Health Grant Numbers U01 CA176726, N1U2COD023375-02, and CA50385; Autism Speaks Foundation Grant Number 1788; and United States Army Medical Research and Materiel Command Grant Number A-14917. Additionally, Dr. Anna V. Oppenheimer received salary support from National Institute of Environmental Health Sciences/National Institute of Health NIEHS/NIH, Grant Number T32ES007069.
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Oppenheimer, A.V., Weisskopf, M.G. & Lyall, K. An Examination of Family Transmission of Traits Measured by the Social Responsiveness Scale—Short Form. J Autism Dev Disord (2023). https://doi.org/10.1007/s10803-023-06115-2
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DOI: https://doi.org/10.1007/s10803-023-06115-2