Abstract
To investigate temperament as an early risk marker for autism spectrum disorder (ASD), we examined parent-reported temperament for high-risk (HR, n = 170) and low-risk (LR, n = 77) siblings at 8, 14, and 24 months. Diagnostic assessment was performed at 36 months. Group-based analyses showed linear risk gradients, with more atypical temperament for HR-ASD, followed by HR-Atypical, HR-Typical, and LR siblings. Temperament differed significantly between outcome groups (0.03 ≤ ηp2 ≤ 0.34). Machine learning analyses showed that, at an individual level, HR-ASD siblings could not be identified accurately, whereas HR infants without ASD could. Our results emphasize the discrepancy between group-based and individual-based predictions and suggest that while temperament does not facilitate early identification of ASD individually, it may help identify HR infants who do not develop ASD.
Similar content being viewed by others
References
Bates, D., Machler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using {lme4}. Journal of Statistical Software, 67, 1–48.
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(1), 289–300.
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(3), 249–260. https://doi.org/10.1016/j.jaac.2011.12.009.
Bussu, G., Jones, E. J. H., Charman, T., Johnson, M. H., Buitelaar, J. K., & Team, B. (2018). Prediction of autism at 3 years from behavioural and developmental measures in high-risk infants: A longitudinal cross-domain classifier analysis. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-018-3509-x.
Casalin, S., Luyten, P., Vliegen, N., & Meurs, P. (2012). The structure and stability of temperament from infancy to toddlerhood: A one-year prospective study. Infant Behavior and Development, 35(1), 94–108. https://doi.org/10.1016/j.infbeh.2011.08.004.
Clifford, S. M., Hudry, K., Elsabbagh, M., Charman, T., Johnson, M. H., & Team, B. (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(3), 673–686. https://doi.org/10.1007/s10803-012-1612-y.
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Erlbaum Associates.
Del Rosario, M., Gillespie-Lynch, K., Johnson, S., Sigman, M., & Hutman, T. (2014). Parent-reported temperament trajectories among infant siblings of children with autism. Journal of Autism and Developmental Disorders, 44(2), 381–393. https://doi.org/10.1007/s10803-013-1876-x.
Fox, N. A. (2004). Temperament and early experience form social behavior. Annals of the New York Academy of Sciences, 1038, 171–178. https://doi.org/10.1196/annals.1315.025.
Gagne, J. R., Van Hulle, C. A., Aksan, N., Essex, M. J., & Goldsmith, H. H. (2011). Deriving childhood temperament measures from emotion-eliciting behavioral episodes: Scale construction and initial validation. Psychological Assessment, 23(2), 337–353. https://doi.org/10.1037/a0021746.
Garon, N., Bryson, S. E., Zwaigenbaum, L., Smith, I. M., Brian, J., Roberts, W., et al. (2009). Temperament and its relationship to autistic symptoms in a high-risk infant sib cohort. Journal of Abnormal Child Psychology, 37(1), 59–78. https://doi.org/10.1007/s10802-008-9258-0.
Garon, N., Zwaigenbaum, L., Bryson, S., Smith, I. M., Brian, J., Roncadin, C., et al. (2016). Temperament and its association with autism symptoms in a high-risk population. Journal of Abnormal Child Psychology. https://doi.org/10.1007/s10802-015-0064-1.
Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the revised Infant Behavior Questionnaire. Infant Behavior & Development, 26(1), 64–86. https://doi.org/10.1016/S0163-6383(02)00169-8.
Georgiades, S., Szatmari, P., Zwaigenbaum, L., Bryson, S., Brian, J., Roberts, W., et al. (2013). A prospective study of autistic-like traits in unaffected siblings of probands with autism spectrum disorder. JAMA Psychiatry, 70(1), 42–48. https://doi.org/10.1001/2013.jamapsychiatry.1.
Gomez, C. R., & Baird, S. (2005). Identifying early indicators for autism in self-regulation difficulties. Focus on Autism and Other Developmental Disabilities. https://doi.org/10.1177/10883576050200020101.
Goodman, R., Ford, T., Richards, H., Gatward, R., & Meltzer, H. (2000). The development and well-being assessment: Description and initial validation of an integrated assessment of child and adolescent psychopathology. Journal of Child Psychology and Psychiatry, 41(5), 645–655.
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(5), 693–705. https://doi.org/10.1007/s10803-008-0674-3.
Johnson, M. H. (2012). Executive function and developmental disorders: The flip side of the coin. Trends in Cognitive Sciences, 16(9), 454–457. https://doi.org/10.1016/j.tics.2012.07.001.
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.
Loth, E., Charman, T., Mason, L., Tillmann, J., Jones, E. J. H., Wooldridge, C., et al. (2017). The EU-AIMS Longitudinal European Autism Project (LEAP): Design and methodologies to identify and validate stratification biomarkers for autism spectrum disorders. Molecular Autism. https://doi.org/10.1186/s13229-017-0146-8.
Macari, S. L., Koller, J., Campbell, D. J., & Chawarska, K. (2017). Temperamental markers in toddlers with autism spectrum disorder. Journal of Child Psychology and Psychiatry. https://doi.org/10.1111/jcpp.12710.
Mullen, E. (1995). Mullen scales of early learning (AGS ed.). Circle Pines: American Guidance Service.
Nigg, J. T. (2006). Temperament and developmental psychopathology. Journal of Child Psychology and Psychiatry, 47(3–4), 395–422. https://doi.org/10.1111/j.1469-7610.2006.01612.x.
Ozonoff, S., Iosif, A. M., Baguio, F., Cook, I. C., Hill, M. M., Hutman, T., et al. (2010). A prospective study of the emergence of early behavioral signs of autism. Journal of the American Academy of Child and Adolescent Psychiatry, 49(3), 256–266. https://doi.org/10.1016/j.jaac.2009.11.009.
Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., et al. (2011). Recurrence risk for autism spectrum disorders: A Baby Siblings Research Consortium study. Pediatrics, 128(3), e488–e495. https://doi.org/10.1542/peds.2010-2825.
Perez-Edgar, K., & Fox, N. A. (2005). Temperament and anxiety disorders. Child and Adolescent Psychiatric Clinics of North America, 14(4), 681–706. https://doi.org/10.1016/j.chc.2005.05.008.
Picardi, A., Fagnani, C., Medda, E., Toccaceli, V., Brambilla, P., & Stazi, M. A. (2015). Genetic and environmental influences underlying the relationship between autistic traits and temperament and character dimensions in adulthood. Comprehensive Psychiatry. https://doi.org/10.1016/j.comppsych.2014.12.018.
Putnam, S. P., Ellis, L. K., & Rothbart, M. K. (2001). The structure of temperament from infancy through adolescence. In A. E. A. Angleitner (Ed.), Advances/proceedings in research on temperament (pp. 165–182). Lengerich: Pabst Scientist Publisher.
Putnam, S. P., Gartstein, M. A., & Rothbart, M. K. (2006). Measurement of fine-grained aspects of toddler temperament: The Early Childhood Behavior Questionnaire. Infant Behavior and Development, 29(3), 386–401. https://doi.org/10.1016/j.infbeh.2006.01.004.
Rothbart, M. K. (1986). Longitudinal observation of infant temperament. Development and Psychopathology, 22(3), 356–365. https://doi.org/10.1037/0012-1649.22.3.356.
Rutter, M., Bailey, A., & Lord, C. (2003a). SCQ. The Social Communication Questionnaire. Los Angeles: Western Psychological Services.
Rutter, M., Le Couteur, A., & Lord, C. (2003b). ADI-R: Autism diagnostic interview—Revised. Los Angeles: Western Psychological Services.
Sheese, B. E., Voelker, P. M., Rothbart, M. K., & Posner, M. I. (2007). Parenting quality interacts with genetic variation in dopamine receptor D4 to influence temperament in early childhood. Development and Psychopathology, 19(4), 1039–1046. https://doi.org/10.1017/S0954579407000521.
Shiner, R. L., Buss, K. A., McClowry, S. G., Putnam, S. P., Saudino, K. J., & Zentner, M. (2012). What is temperament now? Assessing progress in temperament research on the twenty-fifth anniversary of Goldsmith et al. (1987). Child Development Perspectives, 6(4), 436–444.
Sparrow, S. S., Balla., D. A., Cicchetti, D. V., & Doll, E. A. (2005). Vineland adaptive behavior scales (Vineland-II) (2nd ed.). Mineapolis: Pearson.
Tabachnik, B. G., & Fidell, L. S. (2001). Using multivariate statistics. Needham Heights: Allyn and Bacon.
Tackett, J. L. (2006). Evaluating models of the personality-psychopathology relationship in children and adolescents. Clinical Psychology Review, 26(5), 584–599. https://doi.org/10.1016/j.cpr.2006.04.003.
Voelker, P., Sheese, B. E., Rothbart, M. K., & Posner, M. I. (2009). Variations in catechol-O-methyltransferase gene interact with parenting to influence attention in early development. Neuroscience, 164(1), 121–130. https://doi.org/10.1016/j.neuroscience.2009.05.059.
Wan, M. W., Green, J., Elsabbagh, M., Johnson, M., Charman, T., Plummer, F., et al. (2013). Quality of interaction between at-risk infants and caregiver at 12–15 months is associated with 3-year autism outcome. Journal of Child Psychology and Psychiatry, 54(7), 763–771. https://doi.org/10.1111/jcpp.12032.
White, L. K., Lamm, C., Helfinstein, S. M., & Fox, N. A. (2012). Neurobiology and neurochemistry of temperament in children. In M. Zentner, & R. L. Shiner (Eds.), Handbook of temperament. New York: Guilford.
Whittle, S., Allen, N. B., Lubman, D. I., & Yucel, M. (2006). The neurobiological basis of temperament: Towards a better understanding of psychopathology. Neuroscience & Biobehavioral Reviews, 30(4), 511–525. https://doi.org/10.1016/j.neubiorev.2005.09.003.
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(2–3), 143–152. https://doi.org/10.1016/j.ijdevneu.2004.05.001.
Acknowledgments
The data included in this study were collected by the British Autism Study of Infant Siblings (BASIS, http://www.basisnetwork.org) project as part of a larger study. We gratefully thank all parents and children who participated in this study. The research leading to these results received support from MRC Programme grants (G0701484 and MR/K021389/1) to MHJ, and the BASIS funding consortium led by Autistica. This research has also received funding from the Innovative Medicines Initiative Joint Undertaking under grant agreement number 115300 (EU-AIMS), resources of which are composed of financial contribution from the European Union’s Seventh Framework Programme (FP7/2007–2013) and the European Federation of Pharmaceutical Industries and Associations (EFPIA) companies’ in kind contribution. The research was further supported by the Marie Sklodowska Curie Actions of the European Community’s Horizon 2020 Program under grant agreement n°642996 (Brainview). The BASIS Team in alphabetical order: Phase 1: Baron-Cohen, S., Bedford, R., Bolton, P., Chandler, S., Elsabbagh, M., Fernandes, J., Garwood, H., Gliga, T., Hudry, K., Pickles, A., Tucker, L., Volein, A.; Phase 2: Baron-Cohen, S., Bedford, R., Bolton, P., Blasi, A., Cheung, C., Davies, K., Elsabbagh, M., Fernandes, J., Gammer, I., Gliga, T., Guiraud, J., Liew, M., Lloyd-Fox, S., M.H., Maris, H., O’Hara, L., Pickles, A., Ribeiro, H., Salomone, E., Tucker, L.
Author information
Authors and Affiliations
Consortia
Contributions
TC, MHJ, and EJHJ designed the study leading to the data included in the current work, and developed acquisition protocols. Data were collected from the BASIS team. GP was involved in data collection and processing. MKJP performed statistical analysis, interpreted data, and drafted the first and final version of the manuscript. GB performed statistical analysis and interpretation for individual prediction. JKB, NNJR, and IJO helped data interpretation. All authors read and approved the final version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical Approval
All procedures performed in this study 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.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The members of The BASIS Team are listed in Acknowledgments.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pijl, M.K.J., Bussu, G., Charman, T. et al. Temperament as an Early Risk Marker for Autism Spectrum Disorders? A Longitudinal Study of High-Risk and Low-Risk Infants. J Autism Dev Disord 49, 1825–1836 (2019). https://doi.org/10.1007/s10803-018-3855-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-018-3855-8