Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T14:51:23.277Z Has data issue: false hasContentIssue false
  • English
  • Français

Rethinking the idea of late autism spectrum disorder onset

Published online by Cambridge University Press:  14 August 2017

Elizabeth C. Bacon ,
Eric Courchesne ,
Cynthia Carter Barnes ,
Debra Cha ,
Sunny Pence ,
Laura Schreibman ,
Aubyn C. Stahmer  and
Karen Pierce
Elizabeth C. Bacon*
Affiliation:
University of California, San Diego
Eric Courchesne
Affiliation:
University of California, San Diego
Cynthia Carter Barnes
Affiliation:
University of California, San Diego
Debra Cha
Affiliation:
University of California, San Diego
Sunny Pence
Affiliation:
University of California, San Diego
Laura Schreibman
Affiliation:
University of California, San Diego
Aubyn C. Stahmer
Affiliation:
University of California, Davis
Karen Pierce
Affiliation:
University of California, San Diego
*
Address correspondence and reprint requests to: Elizabeth Bacon, Department of Neurosciences, Autism Center of Excellence, University of California, San Diego, 8110 La Jolla Shores Drive, La Jolla, CA, 92037; E-mail: ebacon@ucsd.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

A common theory of autism spectrum disorder (ASD) symptom onset includes toddlers who do not display symptoms until well after age 2, which are termed late-onset ASD cases. Objectives were to analyze differences in clinical phenotype between toddlers identified as ASD at initial evaluations (early diagnosed) versus those initially considered nonspectrum, then later identified as ASD (late diagnosed). Two hundred seventy-three toddlers recruited from the general population based on a failed developmental screening form or parent or physician concerns were followed longitudinally from 12 months and identified as early- and late-diagnosed cases of ASD, language delayed, or typically developing. Toddlers completed common standardized assessments and experimental eye-tracking and observational measures every 9–12 months until age 3. Longitudinal performance on standardized assessments and experimental tests from initial evaluations were compared. Delay in social communication skills was seen in both ASD groups at early-age initial assessment, including increased preference for nonsocial stimuli, increased stereotypic play, reduced exploration, and use of gestures. On standardized psychometric assessments, early-diagnosed toddlers showed more impairment initially while late-diagnosed toddlers showed a slowing in language acquisition. Similar social communication impairments were present at very early ages in both early-detected ASD and so-called late-onset ASD. Data indicate ASD is present whether detected or not by current methods, and development of more sensitive tools is needed.

Type
Regular Articles
Information
Development and Psychopathology , Volume 30 , Issue 2 , May 2018 , pp. 553 - 569
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

This work was supported by NIH Grants ACE P50-MH081755 and R01-MH080134. We sincerely thank the toddlers and families who participated in this research. The Geometric Preference Test is licensed by the University of California, San Diego, and Karen Pierce receives royalties. The other authors have no conflicts of interest or financial disclosures relevant to this article. The funding agency had no role in the conception or writing of this manuscript.

References

Avino, T. A., & Hutsler, J. J. (2010). Abnormal cell patterning at the cortical gray-white matter boundary in autism spectrum disorders. Brain Research, 1360, 138–146. doi:10.1016/j.brainres.2010.08.091Google Scholar
Bedford, R., Elsabbagh, M., Gliga, T., Pickles, A., Senju, A., Charman, T., … BASIS Team. (2012). Precursors to social and communication difficulties in infants at-risk for autism: Gaze following and attentional engagement. Journal of Autism and Developmental Disorders, 42, 2208–2218. doi:10.1007/s10803-012-1450-yGoogle Scholar
Boyd, B. A., Odom, S. L., Humphreys, B. P., & Sam, A. M. (2010). Infants and toddlers with autism spectrum disorder: Early identification and early intervention. Journal of Early Intervention, 32, 75–98.Google Scholar
Bryson, S. E., 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. doi:10.1007/s10803-006-0328-2Google Scholar
Chawarska, K., Shic, F., Macari, S., Campbell, D. J., Brian, J., Landa, R., … Bryson, S. (2014). 18-month predictors of later outcomes in younger siblings of children with autism spectrum disorder: A baby siblings research consortium study. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 1317–1327. doi:10.1016/j.jaac.2014.09.015Google Scholar
Christensen, L., Hutman, T., Rozga, A., Young, G. S., Ozonoff, S., Rogers, S. J., … Sigman, M. (2010). Play and developmental outcomes in infant siblings of children with autism. Journal of Autism and Developmental Disorders, 40, 946–957. doi:10.1007/s10803-010-0941-yGoogle Scholar
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. doi:10.1007/s10803-012-1518-8Google Scholar
Corsello, C. M. (2005). Early intervention in autism. Infants & Young Children, 18, 74–85.Google Scholar
Courchesne, E., Mouton, P. R., Calhoun, M. E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M. J., … Pierce, K. (2011). Neuron number and size in prefrontal cortex of children with autism. Journal of the American Medical Association, 306, 2001–2010. doi:10.1001/jama.2011.1638Google Scholar
Curran, P. J., Obeidat, K., & Losardo, D. (2010). Twelve frequently asked questions about growth curve modeling. Journal of Cognitive Development, 11, 121–136. doi:10.1080/15248371003699969Google Scholar
Davidovitch, M., Levit-Binnun, N., Golan, D., & Manning-Courtney, P. (2015). Late diagnosis of autism spectrum disorder after initial negative assessment by a multidisciplinary team. Journal of Developmental and Behavioral Pediatrics, 36, 227–234. doi:10.1097/DBP.0000000000000133Google Scholar
Dawson, G. (2008). Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder. Development and Psychopathology, 20, 775–803. doi:10.1017/S0954579408000370Google Scholar
Eldevik, S., Hastings, R. P., Hughes, J. C., Jahr, E., Eikeseth, S., & Cross, S. (2009). Meta-analysis of Early Intensive Behavioral Intervention for children with autism. Journal of Clinical Child and Adolescent Psychology, 38, 439–450. doi:10.1080/15374410902851739Google Scholar
Elison, J. T., Wolff, J. J., Reznick, J. S., Botteron, K. N., Estes, A. M., Gu, H., … Infant Brain Imaging Study Network. (2014). Repetitive behavior in 12-month-olds later classified with autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 1216–1224. doi:10.1016/j.jaac.2014.08.004Google Scholar
Fountain, C., Winter, A. S., & Bearman, P. S. (2012). Six developmental trajectories characterize children with autism. Pediatrics, 129, e1112–e1120. doi:10.1542/peds.2011-1601Google Scholar
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. doi:10.1007/s10803-008-0674-3Google Scholar
Gotham, K., Pickles, A., & Lord, C. (2012). Trajectories of autism severity in children using standardized ADOS scores. Pediatrics, 130, e1278–e1284. doi:10.1542/peds.2011-3668Google Scholar
Ibanez, L. V., Grantz, C. J., & Messinger, D. S. (2013). The development of referential communication and autism symptomatology in high-risk infants. Infancy, 18. doi:10.1111/j.1532-7078.2012.00142.xGoogle Scholar
Itzchak, E. B., & Zachor, D. A. (2011). Who benefits from early intervention in autism spectrum disorders? Research in Autism Spectrum Disorders, 5, 345–350.Google Scholar
Jónsdóttir, S. L., Saemundsen, E., Antonsdóttir, I. S., Sigurdardóttir, S., & Ólason, D. (2011). Children diagnosed with autism spectrum disorder before or after the age of 6 years. Research in Autism Spectrum Disorders, 5, 175–184.Google Scholar
Landa, R. J., & Garrett-Mayer, E. (2006). Development in infants with autism spectrum disorders: A prospective study. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 47, 629–638. doi:10.1111/j.1469-7610.2006.01531.xGoogle Scholar
Landa, R. J., Gross, A. L., Stuart, E. A., & Bauman, M. (2012). Latent class analysis of early developmental trajectory in baby siblings of children with autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 53, 986–996. doi:10.1111/j.1469-7610.2012.02558.xGoogle Scholar
Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2002). Autism Diagnostic Observation Schedule. Los Angeles: Western Psychological Services.Google Scholar
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 Services.Google Scholar
Macari, S. L., Campbell, D., Gengoux, G. W., Saulnier, C. A., Klin, A. J., & Chawarska, K. (2012). Predicting developmental status from 12 to 24 months in infants at risk for autism spectrum disorder: A preliminary report. Journal of Autism and Developmental Disorders, 42, 2636–2647. doi:10.1007/s10803-012-1521-0Google Scholar
Mullen, E. M. (1995). Mullen Scales of Early Learning. Circle Pines, MN: American Guidance Service.Google Scholar
Nadig, A. S., Ozonoff, S., Young, G. S., Rozga, A., Sigman, M., & Rogers, S. J. (2007). A prospective study of response to name in infants at risk for autism. Archives of Pediatrics and Adolescent Medicine, 161, 378–383. doi:10.1001/archpedi.161.4.378Google Scholar
Ozonoff, S., Iosif, A. M., Baguio, F., Cook, I. C., Hill, M. M., Hutman, T., … Young, G. S. (2010). A prospective study of the emergence of early behavioral signs of autism. Journal of the American Academy of Child & Adolescent Psychiatry, 49, 256–266.Google Scholar
Ozonoff, S., Young, G. S., Landa, R. J., Brian, J., Bryson, S., Charman, T., … 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, and Allied Disciplines, 56, 988–998. doi:10.1111/jcpp.12421Google Scholar
Parikshak, N. N., Luo, R., Zhang, A., Won, H., Lowe, J. K., Chandran, V., … Geschwind, D. H. (2013). Integrative functional genomic analyses implicate specific molecular pathways and circuits in autism. Cell, 155, 1008–1021. doi:10.1016/j.cell.2013.10.031Google Scholar
Perry, A., Condillac, R. A., & Freeman, N. L. (2002). Best practices and practical strategies for assessment and diagnosis of autism. Journal on Developmental Disabilities, 9, 61–75.Google Scholar
Pierce, K., Carter, C., Weinfeld, M., Desmond, J., Hazin, R., Bjork, R., & Gallagher, N. (2011). Detecting, studying, and treating autism early: The 1-Year Well-Baby Check-Up Approach. Journal of Pediatrics, 159, 458–465. doi:10.1016/j.jpeds.2011.02.036Google Scholar
Pierce, K., Conant, D., Hazin, R., Stoner, R., & Desmond, J. (2011). Preference for geometric patterns early in life as a risk factor for autism. Archives of General Psychiatry, 68, 101–109. doi:10.1001/archgenpsychiatry.2010.113Google Scholar
Pierce, K., & Courchesne, E. (2001). Evidence for a cerebellar role in reduced exploration and stereotyped behavior in autism. Biological Psychiatry, 49, 655–664.Google Scholar
Pierce, K., Marinero, S., Hazin, R., McKenna, B., Barnes, C. C., & Malige, A. (2016). Eye tracking reveals abnormal visual preference for geometric images as an early biomarker of an autism spectrum disorder subtype associated with increased symptom severity. Biological Psychiatry, 79, 657–666. doi:10.1016/j.biopsych.2015.03.032Google Scholar
Pramparo, T., Pierce, K., Lombardo, M. V., Carter Barnes, C., Marinero, S., Ahrens-Barbeau, C., … Courchesne, E. (2015). Prediction of autism by translation and immune/inflammation coexpressed genes in toddlers from pediatric community practices. JAMA Psychiatry, 72, 386–394. doi:10.1001/jamapsychiatry.2014.3008Google Scholar
Rozga, A., Hutman, T., Young, G. S., Rogers, S. J., Ozonoff, S., Dapretto, M., & Sigman, M. (2011). Behavioral profiles of affected and unaffected siblings of children with autism: Contribution of measures of mother-infant interaction and nonverbal communication. Journal of Autism and Developmental Disorders, 41, 287–301. doi:10.1007/s10803-010-1051-6Google Scholar
Sacrey, L. A., Bryson, S. E., & Zwaigenbaum, L. (2013). Prospective examination of visual attention during play in infants at high-risk for autism spectrum disorder: A longitudinal study from 6 to 36 months of age. Behavioral Brain Research, 256, 441–450. doi:10.1016/j.bbr.2013.08.028Google Scholar
Shumway, S., Thurm, A., Swedo, S. E., Deprey, L., Barnett, L. A., Amaral, D. G., … Ozonoff, S. (2011). Brief report: Symptom onset patterns and functional outcomes in young children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 41, 1727–1732. doi:10.1007/s10803-011-1203-3Google Scholar
Sparrow, S. S., Balla, D. A., Cicchetti, D. V., Harrison, P. L., & Doll, E. A. (1984). Vineland Adaptive Behavior Scales. Circle Pines, MN: American Guidance Service.Google Scholar
Sparrow, S. S., Cicchetti, D. V., & Balla, D. A. (2005). Vineland Adaptive Behavior Scales (2nd ed.). Bloomington, IN: Pearson.Google Scholar
Stoner, R., Chow, M. L., Boyle, M. P., Sunkin, S. M., Mouton, P. R., Roy, S., … Courchesne, E. (2014). Patches of disorganization in the neocortex of children with autism. New England Journal of Medicine, 370, 1209–1219. doi:10.1056/NEJMoa1307491Google Scholar
Wan, M. W., Green, J., Elsabbagh, M., Johnson, M., Charman, T., Plummer, F., & BASIS Team. (2012). Parent-infant interaction in infant siblings at risk of autism. Research in Developmental Disabilities, 33, 924–932. doi:10.1016/j.ridd.2011.12.011Google Scholar
Wetherby, A. M., Brosnan-Maddox, S., Peace, V., & Newton, L. (2008). Validation of the Infant–Toddler Checklist as a broadband screener for autism spectrum disorders from 9 to 24 months of age. Autism, 12, 487–511. doi:10.1177/1362361308094501Google Scholar
Wiggins, L. D., Baio, J., & Rice, C. (2006). Examination of the time between first evaluation and first autism spectrum diagnosis in a population-based sample. Journal of Developmental and Behavioral Pediatrics, 27(2 Suppl), S79–S87.Google Scholar
Willsey, A. J., Sanders, S. J., Li, M., Dong, S., Tebbenkamp, A. T., Muhle, R. A., … State, M. W. (2013). Coexpression networks implicate human midfetal deep cortical projection neurons in the pathogenesis of autism. Cell, 155, 997–1007. doi:10.1016/j.cell.2013.10.020Google Scholar
Young, G. S., Rogers, S. J., Hutman, T., Rozga, A., Sigman, M., & Ozonoff, S. (2011). Imitation from 12 to 24 months in autism and typical development: A longitudinal Rasch analysis. Developmental Psychology, 47, 1565–1578. doi:10.1037/a0025418Google Scholar
Zwaigenbaum, L., Bauman, M. L., Choueiri, R., Fein, D., Kasari, C., Pierce, K., … Wetherby, A. (2015). Early identification and interventions for autisms spectrum disorder: Executive summary. Pediatrics, 136(Suppl 1), S1–S9. doi:10.1542/peds.2014-3667BGoogle Scholar
Zwaigenbaum, L., Bauman, M. L., Stone, W. L., Yirmiya, N., Estes, A., Hansen, R. L., … Wetherby, A. (2015). Early identification of autism spectrum disorder: Recommendations for practice and research. Pediatrics, 136(Suppl. 1), S10–S40. doi:10.1542/peds.2014-3667CGoogle Scholar
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. doi:10.1016/j.ijdevneu.2004.05.001Google Scholar