Abstract
Early communication impairment is among the most-reported first concerns in parents of young children with autism spectrum disorder (ASD). Using a parent-report questionnaire, we derived trajectory groups for early language and gesture acquisition in siblings at high risk for ASD and in children at low risk, during their first 2 years of life. Developmental skills at 6 months were associated with trajectory group membership representing growth in receptive language and gestures. Behavioral symptoms also predicted gesture development. All communication measures were strongly related to clinical and developmental outcomes. Trajectory groups further indicated slowest language/gesture acquisition in infants with later ASD diagnoses, in particular when associated with language delay. Overall, our results confirm considerable variability in communication development in high-risk infants.
Similar content being viewed by others
References
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th edn. text rev; DSM-IV-TR). Washington, DC: American Psychiatric Association.
American Psychiatric Association. (2013). Cautionary statement for forensic use of DSM-5. In Diagnostic and statistical manual of mental disorders (5th edn.). https://doi.org/10.1176/appi.books.9780890425596.744053.
Bhat, A. N., Galloway, J. C., & Landa, R. J. (2012). Relation between early motor delay and later communication delay in infants at risk for autism. Infant Behavior and Development, 35(4), 838–846. https://doi.org/10.1016/j.infbeh.2012.07.019.
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.
Bradshaw, J., Steiner, A. M., Gengoux, G., & Koegel, L. K. (2015). Feasibility and effectiveness of very early intervention for infants at-risk for autism spectrum disorder: A systematic review. Journal of Autism and Developmental Disorders, 45(3), 778–794. https://doi.org/10.1007/s10803-014-2235-2.
Brady, N. C., Marquis, J., Fleming, K., & McLean, L. (2004). Prelinguistic predictors of language growth in children with developmental disabilities. Journal of Speech, Language, and Hearing Research, 47(3), 663–677. https://doi.org/10.1044/1092-4388(2004/051).
Brian, A. J., Roncadin, C., Duku, E., Bryson, S. E., Smith, I. M., Roberts, W., et al. (2014). Emerging cognitive profiles in high-risk infants with and without autism spectrum disorder. Research in Autism Spectrum Disorders, 8(11), 1557–1566. https://doi.org/10.1016/j.rasd.2014.07.021.
Brian, J. A., Smith, I. M., Zwaigenbaum, L., & Bryson, S. E. (2017). Cross-site randomized control trial of the Social ABCs caregiver-mediated intervention for toddlers with autism spectrum disorder. Autism Research: Official Journal of the International Society for Autism Research, 10(10), 1700–1711. https://doi.org/10.1002/aur.1818.
Brian, J. A., Smith, I. M., Zwaigenbaum, L., Roberts, W., & Bryson, S. E. (2016). The Social ABCs caregiver-mediated intervention for toddlers with autism spectrum disorder: Feasibility, acceptability, and evidence of promise from a multisite study. Autism Research: Official Journal of the International Society for Autism Research, 9(8), 899–912. https://doi.org/10.1002/aur.1582.
Bryson, S. E., Zwaigenbaum, L., Brian, J., Roberts, W., Szatmari, P., Rombough, V., et al. (2007). A prospective case series of high-risk infants who developed autism. Journal of Autism and Developmental Disorders, 37(1), 12–24. https://doi.org/10.1007/s10803-006-0328-2.
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(4), 731–738. https://doi.org/10.1007/s10803-007-0440-y.
Charman, T. (2003a). Why is joint attention a pivotal skill in autism? Philosophical Transactions of the Royal Society of London: Biological Sciences, 358(1430), 315–324. https://doi.org/10.1098/rstb.2002.1199.
Charman, T., Baron-Cohen, S., Swettenham, J., Baird, G., Drew, A., & Cox, A. (2003b). Predicting language outcome in infants with autism and pervasive developmental disorder. International Journal of Language & Communication Disorders, 38(3), 265–285. https://doi.org/10.1080/136820310000104830.
Charman, T., Drew, A., Baird, C., & Baird, G. (2003c). Measuring early language development in preschool children with autism spectrum disorder using the MacArthur communicative development inventory (Infant Form). Journal of Child Language, 30(1), 213–236.
Charman, T., Taylor, E., Drew, A., Cockerill, H., Brown, J.-A., & Baird, G. (2005). Outcome at 7 years of children diagnosed with autism at age 2: Predictive validity of assessments conducted at 2 and 3 years of age and pattern of symptom change over time. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 46(5), 500–513. https://doi.org/10.1111/j.1469-7610.2004.00377.x.
Chawarska, K., Macari, S., & Shic, F. (2013). Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biological Psychiatry, 74(3), 195–203. https://doi.org/10.1016/j.biopsych.2012.11.022.
DeGiacomo, A., & Fombonne, E. (1998). Parental recognition of developmental abnormalities in autism. European Child & Adolescent Psychiatry, 7(3), 131–136.
Drew, A., Baird, G., Baron-Cohen, S., Cox, A., Slonims, V., Wheelwright, S., et al. (2002). A pilot randomised control trial of a parent training intervention for pre-school children with autism. European Child & Adolescent Psychiatry, 11(6), 266–272. https://doi.org/10.1007/s00787-002-0299-6.
Ellis Weismer, S., Lord, C., & Esler, A. (2010). Early language patterns of toddlers on the autism spectrum compared to toddlers with developmental delay. Journal of Autism and Developmental Disorders, 40(10), 1259–1273. https://doi.org/10.1007/s10803-010-0983-1.
Estes, A., Zwaigenbaum, L., Gu, H., John, T. S., Paterson, S., Elison, J. T., et al. (2015). Behavioral, cognitive, and adaptive development in infants with autism spectrum disorder in the first 2 years of life. Journal of Neurodevelopmental Disorders, 7(1), e1–e10. https://doi.org/10.1186/s11689-015-9117-6.
Fenson, L., Dale, J., Reznick, S., Thal, D., Bates, E., Hartung, J. P., et al. (1993). MacArthur communicative development inventories: User’s guide and manual. San Diego, CA: Singular Publishing Group.
Flanagan, J. E., Landa, R., Bhat, A., & Bauman, M. (2012). Head lag in infants at risk for autism: A preliminary study. The American Journal of Occupational Therapy, 66(5), 577–585. https://doi.org/10.5014/ajot.2012.004192.
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.
Ibanez, L. V., Grantz, C. J., & Messinger, D. S. (2013). The development of referential communication and autism symptomatology in high-risk infants. Infancy, 18(5), 687–707. https://doi.org/10.1111/j.1532-7078.2012.00142.x.
Ingersoll, B., & Dvortcsak, A. (2010). Teaching social communication to children with autism. New York: The Guilford Press.
Iverson, J. M. (2010). Developing language in a developing body: The relationship between motor development and language development. Journal of Child Language, 37(2), 229–261. https://doi.org/10.1017/S0305000909990432.
Iverson, J. M., Northrup, J. B., Leezenbaum, N. B., Parlade, M. V., Koterba, E. A., & West, K. L. (2017). Early gesture and vocabulary development in infant siblings of children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 115(3), 517–527. https://doi.org/10.1007/s10803-017-3297-8.
Jones, B. L., Nagin, D., & Roeder, K. (2001). A SAS procedure based on mixture models for estimating developmental trajectories. Sociological Methods & Research, 29, 374–393.
Jones, B. L., & Nagin, D. S. (2007). Advances in group-based trajectory modeling and an SAS procedure for estimating them. Sociological & Research, 35(4), 542–571. https://doi.org/10.1177/0049124106292364.
Jones, E. A., Carr, E. G., & Feeley, K. M. (2006). Multiple effects of joint attention intervention for children with autism. Behavior Modification, 30(6), 782–834. https://doi.org/10.1177/0145445506289392.
Jones, E. J. H., Gliga, T., Bedford, R., Charman, T., & Johnson, M. H. (2014). Developmental pathways to autism: A review of prospective studies of infants at risk. Neuroscience & Biobehavioral Reviews, 39, 1–33. https://doi.org/10.1016/j.neubiorev.2013.12.001.
Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2–6-month-old infants later diagnosed with autism. Nature, 504(7480), 427–431. https://doi.org/10.1038/nature12715.
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.
LeBarton, E. S., & Iverson, J. M. (2013). Fine motor skill predicts expressive language in infant siblings of children with autism. Developmental Science, 16(6), 815–827. https://doi.org/10.1111/desc.12069.
Leonard, H. C., Bedford, R., Pickles, A., Hill, E. L., & BASIS Team. (2015). Predicting the rate of language development from early motor skills in at-risk infants who develop autism spectrum disorder. Research in Autism Spectrum Disorders, 13–14, 15–24. https://doi.org/10.1016/j.rasd.2014.12.012.
Longard, J., Brian, J., Zwaigenbaum, L., Duku, E., Moore, C., Smith, I. M., et al. (2017). Early expressive and receptive language trajectories in high-risk infant siblings of children with autism spectrum disorder. Autism & Developmental Language Impairments, 2(3), 239694151773741. https://doi.org/10.1177/2396941517737418.
Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule–generic: A standard measure of social and communicative deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205–223.
Manwaring, S. S., Mead, D. L., Swineford, L., & Thurm, A. (2017). Modelling gesture use and early language development in autism spectrum disorder. International Journal of Language & Communication Disorders, 52(5), 637–651. https://doi.org/10.1111/1460-6984.12308.
Messinger, D., Young, G. S., Ozonoff, S., Dobkins, K., Carter, A., Zwaigenbaum, L., et al. (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 and Adolescent Psychiatry, 52(3), 300–308. https://doi.org/10.1016/j.jaac.2012.12.011.
Mitchell, S. M., Brian, J., Zwaigenbaum, L., Roberts, W., Szatmari, P., Smith, I., et al. (2006). Early language and communication development of infants later diagnosed with autism spectrum disorder. Journal of Developmental and Behavioral Pediatrics, 27(2), 68–78.
Mullen, E. M. (1995). Mullen scales of early learning. Circle Pines, MN: American Guidance.
Murray, D. S., Creaghead, N. A., Manning-Courtney, P., Shear, P. K., Bean, J., & Prendeville, J.-A. (2008). The relationship between joint attention and language in children with autism spectrum disorders. Focus on Autism and Other Developmental Disabilities, 23(1), 5–14. https://doi.org/10.1177/1088357607311443.
Nagin, D. S. (1999). Analyzing developmental trajectories: A semi-parametric, group based approach. Psychological Methods, 4, 139–177.
Nagin, D. S. (2005). Group-based modeling of development. Cambridge, MA: Harvard University Press.
Ozonoff, S., Heung, K., Byrd, R., Hansen, R., & Hertz-Picciotto, I. (2008). The onset of autism: Patterns of symptom emergence in the first years of life. Autism Research, 1(6), 320–328. https://doi.org/10.1002/aur.53.
Ozonoff, S., Young, G. S., Belding, A., Hill, M., Hill, A., Hutman, T., et al. (2014). The broader autism phenotype in infancy: When does it emerge? Journal of the American Academy of Child and Adolescent Psychiatry, 53(4), 398–407. https://doi.org/10.1016/j.jaac.2013.12.020.
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.
Parlade, M. V., & Iverson, J. M. (2015). The development of coordinated communication in infants at heightened risk for autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(7), 2218–2234. https://doi.org/10.1007/s10803-015-2391-z.
Paul, R., Chawarska, K., Cicchetti, D., & Volkmar, F. (2008). Language outcomes of toddlers with autism spectrum disorders: A two year follow-up. Autism Research, 1(2), 97–107. https://doi.org/10.1002/aur.12.
Paul, R., Fuerst, Y., Ramsay, G., Chawarska, K., & Klin, A. (2011). Out of the mouths of babes: Vocal production in infant siblings of children with ASD. Journal of Child Psychology and Psychiatry, 52(5), 588–598. https://doi.org/10.1111/j.1469-7610.2010.02332.x.
Piven, J., Elison, J. T., & Zylka, M. J. (2017). Toward a conceptual framework for early brain and behavior development in autism. Molecular Psychiatry, 22(10), 1385–1394. https://doi.org/10.1038/mp.2017.131.
Ray-Subramanian, C. E., & Ellis Weismer, S. (2012). Receptive and expressive language as predictors of restricted and repetitive behaviors in young children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 42(10), 2113–2120. https://doi.org/10.1007/s10803-012-1463-6.
Richards, M., Mossey, J., & Robins, D. L. (2016). Parentsʼ concerns as they relate to their childʼs development and later diagnosis of autism spectrum disorder. Journal of Developmental & Behavioral Pediatrics, 37(7), 532–540. https://doi.org/10.1097/DBP.0000000000000339.
Rogers, S. J. (2009). What are infant siblings teaching us about autism in infancy? Autism research. Official Journal of the International Society for Autism Research, 2(3), 125–137. https://doi.org/10.1002/aur.81.
Rogers, S. J., Estes, A., Lord, C., Vismara, L., Winter, J., Fitzpatrick, A., et al. (2012). Effects of a brief early start Denver model (ESDM)-based parent intervention on toddlers at risk for autism spectrum disorders: A randomized controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry, 51(10), 1052–1065. https://doi.org/10.1016/j.jaac.2012.08.003.
Rogers, S. J., Vismara, L., Wagner, A. L., McCormick, C., Young, G., & Ozonoff, S. (2014). Autism treatment in the first year of life: A pilot study of infant start, a parent-implemented intervention for symptomatic infants. Journal of Autism and Developmental Disorders, 44(12), 2981–2995. https://doi.org/10.1007/s10803-014-2202-y.
Rowe, M. L., & Goldin-Meadow, S. (2009). Early gesture selectively predicts later language learning. Developmental Science, 12(1), 182–187. https://doi.org/10.1111/j.1467-7687.2008.00764.x.
Rutter, M., Le Couteur, A., & Lord, C. (2003). ADI-R: Autism diagnostic Interview revised manual. Los Angeles: Western Psychological Services.
Sacrey, L.-A. R., Zwaigenbaum, L., Bryson, S., Brian, J., Smith, I. M., Roberts, W., et al. (2015). Can parents’ concerns predict autism spectrum disorder? A prospective study of high-risk siblings from 6 to 36 months of age. Journal of the American Academy of Child and Adolescent Psychiatry, 54(6), 470–478. https://doi.org/10.1016/j.jaac.2015.03.014.
Schertz, H. H., & Odom, S. L. (2007). Promoting joint attention in toddlers with autism: A parent-mediated developmental model. Journal of Autism and Developmental Disorders, 37(8), 1562–1575. https://doi.org/10.1007/s10803-006-0290-z.
Stone, W. L., McMahon, C. R., Yoder, P. J., & Walden, T. A. (2007). Early social-communicative and cognitive development of younger siblings of children with autism spectrum disorders. Archives of Pediatrics & Adolescent Medicine, 161(4), 384–390. https://doi.org/10.1001/archpedi.161.4.384.
Stone, W. L., & Yoder, P. J. (2001). Predicting spoken language level in children with autism spectrum disorders. Autism, 5(4), 341–361. https://doi.org/10.1177/1362361301005004002.
Szatmari, P., Bryson, S. E., Boyle, M. H., Streiner, D. L., & Duku, E. (2003). Predictors of outcome among high functioning children with autism and Asperger syndrome. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 44(4), 520–528.
Szatmari, P., Chawarska, K., Dawson, G., Georgiades, S., Landa, R., Lord, C., et al. (2016). Prospective longitudinal studies of infant siblings of children with autism: Lessons learned and future directions. Journal of the American Academy of Child and Adolescent Psychiatry, 55(3), 179–187. https://doi.org/10.1016/j.jaac.2015.12.014.
Thurm, A., Lord, C., Lee, L.-C., & Newschaffer, C. (2007). Predictors of language acquisition in preschool children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(9), 1721–1734. https://doi.org/10.1007/s10803-006-0300-1.
Toth, K., Munson, J., Meltzoff, A. N., & Dawson, G. (2006). Early predictors of communication development in young children with autism spectrum disorder: Joint attention, imitation, and toy play. Journal of Autism and Developmental Disorders, 36(8), 993–1005. https://doi.org/10.1007/s10803-006-0137-7.
Volden, J., Smith, I. M., Szatmari, P., Bryson, S., Fombonne, E., Mirenda, P., et al. (2011). Using the preschool language scale, fourth edition to characterize language in preschoolers with autism spectrum disorders. American Journal of Speech-Language Pathology, 20(3), 200–210. https://doi.org/10.1044/1058-0360(2011/10-0035).
West, K. L., Leezenbaum, N. B., Northrup, J. B., & Iverson, J. M. (2017). The relation between walking and language in infant siblings of children with autism spectrum disorder. Child Development, 17(1), 213. https://doi.org/10.1111/cdev.12980.
Winder, B. M., Wozniak, R. H., Parlade, M. V., & Iverson, J. M. (2013). Spontaneous initiation of communication in infants at low and heightened risk for autism spectrum disorders. Developmental Psychology, 49(10), 1931–1942. https://doi.org/10.1037/a0031061.
Yirmiya, N., Gamliel, I., Pilowsky, T., Feldman, R., Baron-Cohen, S., & Sigman, M. (2006). The development of siblings of children with autism at 4 and 14 months: Social engagement, communication, and cognition. Journal of Child Psychology and Psychiatry, 47(5), 511–523. https://doi.org/10.1111/j.1469-7610.2005.01528.x.
Young, G. S., Merin, N., Rogers, S. J., & Ozonoff, S. (2009). Gaze behavior and affect at 6 months: Predicting clinical outcomes and language development in typically developing infants and infants at risk for autism. Developmental Science, 12(5), 798–814. https://doi.org/10.1111/j.1467-7687.2009.00833.x.
Zwaigenbaum, L., Bryson, S., Lord, C., Rogers, S., Carter, A., Carver, L., et al. (2009). Clinical assessment and management of toddlers with suspected autism spectrum disorder: Insights from studies of high-risk infants. Pediatrics, 123(5), 1383–1391. https://doi.org/10.1542/peds.2008-1606.
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.
Zwaigenbaum, L., Bryson, S. E., Szatmari, P., Brian, J., Smith, I. M., Roberts, W., et al. (2012). Sex differences in children with autism spectrum disorder identified within a high-risk infant cohort. Journal of Autism and Developmental Disorders, 42(12), 2585–2596. https://doi.org/10.1007/s10803-012-1515-y.
Acknowledgments
The authors would like to thank all the families who kindly volunteered to participate as well as all the person involved in data collection. This work was supported by the Canadian Institutes of Health Research [Grant Number MOP102655] and Autism Speaks Canada [Grant Number ASCanada-2010-01]. MF was further supported by an individual grant from the Swiss National Science Foundation (Grant Number P2GEP1_171686).
Author information
Authors and Affiliations
Contributions
SEB, LZ, and JB designed and planned the cohort study. MF and IMS conceived the current study. JB, SEB, LZ, IMS, WR, and CR participated in data collection. MF performed the analyses. ED provided support in the statistical analyses. ED, IMS, VA, and MF contributed to the interpretation of the results. MF took the lead in writing the manuscript, and IMS supervised the writing. All authors provided critical feedback and helped shape the research, analysis, and manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Franchini, M., Duku, E., Armstrong, V. et al. Variability in Verbal and Nonverbal Communication in Infants at Risk for Autism Spectrum Disorder: Predictors and Outcomes. J Autism Dev Disord 48, 3417–3431 (2018). https://doi.org/10.1007/s10803-018-3607-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-018-3607-9