Relationship Between Early Social-Emotional Behavior and Autism Spectrum Disorder: A High-Risk Sibling Study

Abstract

Social-emotional behavior in autism spectrum disorder (ASD) was examined among high-risk (HR; siblings of children diagnosed with ASD) and low-risk (LR; no family history of ASD) toddlers. Caregivers completed the Infant-Toddler Social Emotional Assessment (ITSEA) at 18 months, and blind diagnostic assessment for ASD was conducted at 36 months. Results indicated impairment in social-emotional functioning among HR toddlers subsequently diagnosed with ASD compared to other HR and LR toddlers, such that ITSEA domains (Internalizing, Dysregulation, Competence) and subdomains predicted later ASD symptoms and diagnosis. Receiver operating curves of optimal ITSEA cutoffs ranged from 0.23 to 0.44 for sensitivity, and 0.74 to 0.89 for specificity. Although classification accuracy for ASD was limited, group differences highlight the importance of considering social-emotional development when assessing ASD risk.

This is a preview of subscription content, log in to check access.

References

  1. Achenbach, T. M. (1966). The classification of children’s psychiatric symptoms: A factor-analytic study. Psychological Monographs, 80, 615.

    Google Scholar 

  2. Akobeng, A. K. (2007). Understanding diagnostic tests 3: Receiver operating characteristic curves. Acta Paediatrica, 96, 644–647.

    PubMed  Google Scholar 

  3. Allison, C., Baron-Cohen, S., Wheelwright, S., Charman, T., Richler, J., Pasco, G., & Brayne, C. (2008). The Q-CHAT (quantitative checklist for autism in toddlers): A normally distributed quantitative measure of autistic traits at 18–24 month of age: Preliminary report. Journal of Autism and Developmental Disorders, 38, 1414–1425.

    PubMed  Google Scholar 

  4. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental of mental disorders (fourth edition, text revision). Washington, DC: American Psychiatric Publishing.

    Google Scholar 

  5. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.

    Google Scholar 

  6. Baranek, G. T., Watson, L. R., Crais, E. R., & Reznick, J. S. (2003). First Year Inventory (FYI) (version 2.0). Chapel Hill, NC: The University of North Carolina at Chapel Hill.

    Google Scholar 

  7. Bauminger, N., Solomon, M., & Rogers, S. J. (2010). Externalizing and internalizing behaviors in ASD. Autism Research: Official Journal of the International Society for Autism Research, 3, 101–112.

    Google Scholar 

  8. 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 (Methodological), 57, 289–300.

    Google Scholar 

  9. Ben-Sasson, A., Amit-Ben-Simhon, H., & Meyer, S. (2015). Cross-parent reliability in rating ASD markers in infants. Developmental Neurorehabilitation, 18, 155–161.

    PubMed  Google Scholar 

  10. Ben-Sasson, A., Cermak, S. A., Orsmond, G. I., Tager-Flusberg, H., Carter, A. S., Kadlec, M. B., & Dunn, W. (2007). Extreme sensory modulation behaviors in toddlers with autism spectrum disorders. American Journal of Occupational Therapy, 61, 584–592.

    PubMed  Google Scholar 

  11. Ben-Sasson, A., Cermak, S. A., Orsmond, G. I., Tager-Flusberg, H., Kadlec, M. B., & Carter, A. S. (2008). Sensory clusters of toddlers with autism spectrum disorders: Differences in affective symptoms. Journal of Child Psychology and Psychiatry, 49, 817–825.

    PubMed  Google Scholar 

  12. Ben-Sasson, A., Soto, T. W., Martinez-Pedraza, F., & Carter, A. S. (2013). Early sensory over-responsivity in toddlers with autism spectrum disorders as a predictor of family impairment and parenting stress. Journal of Child Psychology and Psychiatry, 54, 846–853.

    PubMed  Google Scholar 

  13. Bolton, P. F., Golding, J., Emond, A., & Steer, C. D. (2012). Autism spectrum disorder and autistic traits in the Avon Longitudinal Study of Parents and Children: Precursors and early signs. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 249–260.

    PubMed  Google Scholar 

  14. Brereton, A., Tonge, B., & Einfeld, S. (2006). Psychopathology in children and adolescents with autism compared to young people with intellectual disability. Journal of Autism Developmental Disorders, 36, 863–870.

    PubMed  Google Scholar 

  15. Briggs-Gowan, M. J., & Carter, A. S. (1998). Preliminary acceptability and psychometrics of the infant–toddler social and emotional assessment (ITSEA): A new adult-report questionnaire. Infant Mental Health Journal, 19, 422–445.

    Google Scholar 

  16. Briggs-Gowan, M. J., & Carter, A. S. (2002). Brief Infant-Toddler Social and Emotional Assessment (BITSEA) manual (version 2.0). New Haven: Yale University.

    Google Scholar 

  17. Briggs-Gowan, M. J., Carter, A. S., Irwin, J. R., Wachtel, K., & Cicchetti, D. V. (2004). The brief infant-toddler social and emotional assessment: Screening for social-emotional problems and delays in competence. Journal of Pediatric Psychology, 29, 143–155.

    PubMed  Google Scholar 

  18. Bryson, S., Zwaigenbaum, L., Brian, J., Roberts, W., Szatmari, P., Rombough, V., & McDermott, C. (2007). A prospective case series of high-risk infants who developed autism. Journal of Autism and Developmental Disorders, 37, 12–24.

    PubMed  Google Scholar 

  19. Bryson, S. E., Zwaigenbaum, L., McDermott, C., Rombough, V., & Brian, J. (2008). The autism observation scale for infants: Scale development and reliability data. Journal of Autism and Developmental Disorders, 38, 731–738.

    PubMed  Google Scholar 

  20. Carpenter, M., & Tomasello, M. (2000). Joint attention, cultural learning, and language acquisition: Implications for children with autism. In A. M. Wetherby & B. M. Prizant (Eds.), Autism spectrum disorders: A transactional developmental perspective, Communication and language intervention series (pp. 21–54). Baltimore: Brookes Publishing.

    Google Scholar 

  21. Carter, A. S., & Briggs-Gowan, M. J. (2006). The infant–toddler social and emotional assessment (ITSEA) manual. San Antonio, TX: Harcourt Assessment.

    Google Scholar 

  22. Carter, A. S., Briggs-Gowan, M. J., Jones, S. M., & Little, T. D. (2003). The infant-toddler social and emotional assessment (ITSEA): Factor structure, reliability, and validity. Journal of Abnormal Child Psychology, 31, 495–514.

    PubMed  Google Scholar 

  23. Charman, T., Young, G., Brian, J., Carver, A., Carver, L., Chawarska, K., Curtin, S., Dobkins, K., Elsabbagh, M., Georgiades, S., Hertz-Picciotto, I., Hutman, T., Iverson, J., Jones, E., Landa, R., Macari, S., Messinger, D., Nelson, C., Ozonoff, S., Saulnier, C., Stone, W., Tager-Flusberg, H., Webb, S., Yirmiya, N., & Zwaigenbaum, L. (2017). Non-ASD outcomes at 36 months in siblings at familial risk for autism spectrum disorder (ASD): A baby siblings research consortium (BSRC) study. Autism Research, 10(1), 169–178.

    PubMed  Google Scholar 

  24. Clifford, S., Young, R., & Williamson, P. (2007). Assessing the early characteristics of autistic disorder using video analysis. Journal of Autism and Developmental Disorders, 37, 301–313.

    PubMed  Google Scholar 

  25. Clifford, S. M., Hudry, K., Elsabbagh, M., Charman, T., & Johnson, M. H. (2013). Temperament in the first 2 years of life in infants at high-risk for autism spectrum disorders. Journal of Autism and Developmental Disorders, 43, 673–686.

    PubMed  Google Scholar 

  26. Cornew, L., Dobkins, K. R., Akshoomoff, N., McCleery, J. P., & Carver, L. J. (2012). Atypical social referencing in infant siblings of children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 42, 2611–2621.

    PubMed  PubMed Central  Google Scholar 

  27. Dunn, W. (2002). Infant/toddler sensory profile manual. New York: The Psychological Corporation.

    Google Scholar 

  28. Filliter, J. H., Longard, J., Lawrence, M. A., Zwaigenbaum, L., Brian, J., Garon, N., … Bryson, S. E. (2015). Positive affect in infant siblings of children diagnosed with autism spectrum disorder. Journal of Abnormal Child Psychology, 43, 567–575.

    PubMed  Google Scholar 

  29. Fischer, J. E., Bachmann, L. M., & Jaeschke, R. (2003). A readers’ guide to the interpretation of diagnostic test properties: Clinical example of sepsis. Intensive Care Medicine, 29, 1043–1051.

    PubMed  Google Scholar 

  30. Gadow, K., DeVincent, C., Pomeroy, J., & Azizian, A. (2004). Psychiatric symptoms in preschool children with PDD and clinic and comparison samples. Journal of Autism and Developmental Disorders, 34, 379–393.

    PubMed  Google Scholar 

  31. Garon, N., Bryson, S., Zwaigenbaum, L., Smith, I. M., Brian, J., Roberts, W., & Szatmari, P. (2009). Temperament and its relationship to autistic symptoms in a high-risk infant sib cohort. Journal of Abnormal Child Psychology, 37, 59–78.

    PubMed  Google Scholar 

  32. Garon, N., Zwaigenbaum, L., Bryson, S., Smith, I. M., Brian, J., Roncadin, C., Valliancourt, T., Armstrong, V., Sacrey, L. R., & Roberts, W. (2016). Temperament and its association with autism symptoms in a high-risk population. Journal of Abnormal Child Psychology, 44, 757–769.

    PubMed  Google Scholar 

  33. Georgiades, S., Szatmari, P., Duku, E., Zwaigenbaum, L., Bryson, S., Roberts, W., Fombonne, E., Mirenda, P., Smith, I., Vaillancourt, T., Volden, J., Waddell, C., Thompson, A. & Pathways in ASD Study Team. (2011). Phenotypic overlap between core diagnostic features and emotional/behavioral problems in preschool children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 41, 1321–1329.

    PubMed  Google Scholar 

  34. Georgiades, S., Szatmari, P., Zwaigenbaum, L., Bryson, S., Brian, J., Roberts, W., Smith, I., Vaillancourt, T., Roncadin, C., & Garon, N. (2013). A prospective study of autistic-like traits in unaffected siblings of probands with autism spectrum disorder. JAMA Psychiatry, 70, 42–48.

    PubMed  Google Scholar 

  35. Gomez, C., & Baird, S. (2005). Identifying early indicators for autism in self-regulation difficulties. Focus on Autism and Other Developmental Disabilities, 20, 106–116.

    Google Scholar 

  36. Gotham, K., Pickles, A., & Lord, C. (2009). Standardizing ADOS scores for a measure of severity in autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 693–705.

    PubMed  Google Scholar 

  37. Gotham, K., Risi, S., Pickles, A., & Lord, C. (2007). The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders, 37, 613–627.

    PubMed  Google Scholar 

  38. Ingersoll, B., & Wainer, A. (2014). The broader autism phenotype. In F. Volkmar, A. Klin, R. Paul, & D. Cohen (Eds.), Handbook of autism and pervasive developmental disorders (4th ed., pp. 28–56). New York: Wiley.

    Google Scholar 

  39. Kim, J. A., Szatmari, P., Bryson, S. E., Streiner, D. L., & Wilson, F. J. (2000). The prevalence of anxiety and mood problems among children with autism and Asperger syndrome. Autism, 4, 117–133.

    Google Scholar 

  40. Kiss, I. G., Feldman, M. S., Sheldrick, R. C., & Carter, A. S. (2017). Developing autism screening criteria for the brief infant toddler social emotional assessment (BITSEA). Journal of Autism and Developmental Disorders, 47, 1269–1277.

    PubMed Central  Google Scholar 

  41. Kruizinga, I., Visser, J. C., Van Batenburg-Eddes, T., Carter, A. S., Jansen, W., & Raat, H. (2014). Screening for autism spectrum disorders with the brief infant-toddler social and emotional assessment. PLoS ONE, 9(5), e97630.

    PubMed  PubMed Central  Google Scholar 

  42. Lord, C., Luyster, R. J., Gotham, K., & Guthrie, W. (2012a). Autism diagnostic observation schedule, second edition (ADOS-2) manual (Part II): Toddler module. Torrance: Western Psychological Services.

    Google Scholar 

  43. Lord, C., Risi, S., Lambrecht, L., Cook, E., Leventhal, B., DiLavore, P., 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.

    PubMed  Google Scholar 

  44. Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. L. (2012b). Autism diagnostic observation schedule, second edition (ADOS-2) manual (Part I): Modules 1–4. Torrance: Western Psychological Services.

    Google Scholar 

  45. Lord, C., Rutter, M., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., & Schopler, E. (1989). Autism diagnostic observation schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185–212.

    PubMed  Google Scholar 

  46. Lord, C., Rutter, M., & LeCouteur, A. (1994). Autism Diagnostic Interview-Revised: A revised version of the diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659–685.

    PubMed  Google Scholar 

  47. Luyster, R., Gotham, K., Guthrie, W., Coffing, M., Petrak, R., Pierce, K., & Lord, C. (2009). The autism diagnostic observation schedule-toddler module: A new module of a standardized diagnostic measure for autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 1305–1320.

    PubMed  PubMed Central  Google Scholar 

  48. Mundy, P., & Sigman, M. (2006). Joint attention social competence and developmental psychopathology. In D. Cicchetti & D. J. Cohen (Eds.), Developmental psychopathology: Theory and method (pp. 293–332). Hoboken: Wiley.

    Google Scholar 

  49. Ozonoff, S., Young, G. S., Belding, A., Hill, M., Hill, A., Hutman, T., Johnson, S., Miller, M., Rogers, S. J., Schwichtenberg, A. J., Steinfeld, M., & Iosif, A. M. (2014). The broader autism phenotype in infancy: When does it emerge? Journal of the American Academy of Child and Adolescent Psychiatry, 53, 398–407.e2.

    PubMed  PubMed Central  Google Scholar 

  50. Pisula, E., & Ziegart-Sadowska, K. (2015). Broader autism phenotype in siblings of children with ASD—A review. International Journal of Molecular Sciences, 16(6), 13217–13258.

    PubMed  PubMed Central  Google Scholar 

  51. Reynolds, S., & Lane, S. J. (2008). Diagnostic validity of sensory over-responsivity: A review of the literature and case reports. Journal of Autism and Developmental Disorders, 38, 516–529.

    PubMed  Google Scholar 

  52. Reznick, J. S., Baranek, G. T., Reavis, S., Watson, L. R., & Crais, E. R. (2007). A parent-report instrument for identifying one-year-olds at risk for an eventual diagnosis of autism: The first year inventory. Journal of Autism and Developmental Disorders, 37, 1691–1710.

    PubMed  Google Scholar 

  53. Robins, D. L., Casagrande, K., Barton, M., Chen, C. A., Dumont-Mathieu, T., & Fein, D. (2014). Validation of the modified checklist for autism in toddlers, revised with follow-up (M-CHAT-R/F). Pediatrics, 133, 37–45.

    PubMed  PubMed Central  Google Scholar 

  54. Sullivan, M., Finelli, J., Marvin, A., Garrett-Mayer, E., Bauman, M., & Landa, R. (2007). Response to joint attention in toddlers at risk for autism spectrum disorder: A prospective study. Journal of Autism and Developmental Disorders, 37, 37–48.

    PubMed  Google Scholar 

  55. Toth, K., Dawson, G., Meltzoff, A. N., Greenson, J., & Fein, D. (2007). Early social, imitation, play, and language abilities of young non-autistic siblings of children with autism. Journal of Autism and Developmental Disorders, 37, 145–157.

    PubMed  PubMed Central  Google Scholar 

  56. Visser, J. C., Smeekens, S., Rommelse, N., Verkes, R. J., van der Gaag, R. J., & Buitelaar, J. K. (2010). Assessment of psychopathology in 2- to 5-year-olds: Applying the infant-toddler social emotional assessment. Infant Mental Health Journal, 31, 611–629.

    PubMed  Google Scholar 

  57. Watson, L. R., Baranek, G. T., Crais, E. R., Reznick, S., Dystra, J., & Perryman, T. (2007). The first year inventory: Retrospective parent responses to a questionnaire designed to identify one-year olds at risk for autism. Journal of Autism and Developmental Disorders, 37, 49–61.

    PubMed  Google Scholar 

  58. Witwer, A. N., & Lecavalier, L. (2008). Examining the validity of autism spectrum disorder subtypes. Journal of Autism and Developmental Disorders, 38, 1611–1624.

    PubMed  Google Scholar 

  59. Woods, J. J., & Wetherby, A. M. (2003). Early identification of and intervention for infants and toddlers who are at risk for autism spectrum disorder. Language, Speech and Hearing Services in Schools, 34, 180–193.

    Google Scholar 

  60. Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience, 23, 143–152.

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank all the families who participated in the research, as well as the research coordinators at each site. This study was supported by Women & Children’s Health Research Institute (WCHRI), Alberta Innovates-Health Solutions, Brain Canada, Kids Brain Health Network (formerly NeuroDevNet), Canadian Institutes of Health Research (CIHR), Azrieli Foundation, and Stollery Children’s Hospital Foundation Chair in Autism.

Funding

This study was funded by Women & Children’s Health Research Institute (WCHRI), Alberta Innovates-Health Solutions, Brain Canada, Kids Brain Health Network (formerly NeuroDevNet), Canadian Institutes of Health Research (CIHR), Azrieli Foundation, and Stollery Children’s Hospital Foundation Chair in Autism.

Author information

Affiliations

Authors

Contributions

SR made substantial contributions to the conception and design of the paper, analyzed data, and prepared all drafts of the paper. LRS, LZ, SB, JB, IMS, WR, PS, TV, CR, and NG contributed to the conception of the project, provided critical review of the manuscript, and approved the final draft.

Corresponding author

Correspondence to Sarah Raza.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Raza, S., Sacrey, L.R., Zwaigenbaum, L. et al. Relationship Between Early Social-Emotional Behavior and Autism Spectrum Disorder: A High-Risk Sibling Study. J Autism Dev Disord 50, 2527–2539 (2020). https://doi.org/10.1007/s10803-019-03977-3

Download citation

Keywords

  • Autism
  • Autism spectrum disorder
  • Early detection
  • Social-emotional behavior
  • High-risk infant siblings