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Shared and distinct developmental pathways to ASD and ADHD phenotypes among infants at familial risk

Published online by Cambridge University Press:  16 September 2020

Meghan Miller*
Affiliation:
Department of Psychiatry & Behavioral Sciences and MIND Institute, University of California, Davis, CA, USA
Shane Austin
Affiliation:
Graduate Group in Biostatistics, University of California, Davis, CA, USA
Ana-Maria Iosif
Affiliation:
Department of Public Health Sciences, University of California, Davis, CA, USA
Leiana de la Paz
Affiliation:
Department of Psychiatry & Behavioral Sciences and MIND Institute, University of California, Davis, CA, USA
Annie Chuang
Affiliation:
Department of Psychiatry & Behavioral Sciences and MIND Institute, University of California, Davis, CA, USA
Burt Hatch
Affiliation:
Department of Psychiatry & Behavioral Sciences and MIND Institute, University of California, Davis, CA, USA
Sally Ozonoff
Affiliation:
Department of Psychiatry & Behavioral Sciences and MIND Institute, University of California, Davis, CA, USA
*
Author for Correspondence: Meghan Miller, PhD, MIND Institute, University of California Davis Health System, 2825 50th Street, Sacramento, CA95817, USA; E-mail: mrhmiller@ucdavis.edu.

Abstract

Autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD) are believed to share partially overlapping causal mechanisms suggesting that early risk markers may also overlap. Using latent profile analysis (LPA) in a sample of infants enriched for ASD and ADHD, we first examined the number of distinct groups of 3-year-old children, based on ADHD and ASD symptomatology. To investigate early predictors of ASD and ADHD symptom profiles, we next examined differences in trajectories of infant behaviors among the LPA classes spanning general development, negative affect, attention, activity level, impulsivity, and social behavior. Participants included 166 infants at familial risk for ASD (n = 89), ADHD (n = 38), or low-risk for both (n = 39) evaluated at 12, 18, 24, and 36 months of age. A three-class solution was selected reflecting a Typically Developing (TD) class (low symptoms; n = 108), an ADHD class (high ADHD/low ASD symptoms; n = 39), and an ASD class (high ASD/ADHD symptoms; n = 19). Trajectories of infant behaviors were generally suggestive of a gradient pattern of differences, with the greatest impairment within the ASD class followed by the ADHD class. These findings indicate a mixture of overlapping and distinct early markers of preschool ASD- and ADHD-like profiles that can be difficult to disentangle early in life.

Type
Special Section Articles
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press.

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References

Ames, C. S., & White, S. J. (2011). Brief report: Are ADHD traits dissociable from the autistic profile? Links between cognition and behaviour. Journal of Autism and Developmental Disorders, 41, 357363. doi:10.1007/s10803-010-1049-0CrossRefGoogle Scholar
Antshel, K. M., Zhang-James, Y., Wagner, K. E., Ledesma, A., & Faraone, S. V. (2016). An update on the comorbidity of ADHD and ASD: A focus on clinical management. Expert Review of Neurotherapeutics, 16, 279293. doi:10.1586/14737175.2016.1146591CrossRefGoogle ScholarPubMed
Auerbach, J. G., Berger, A., Atzaba-Poria, N., Arbelle, S., Cypin, N., Friedman, A., & Landau, R. (2008). Temperament at 7, 12, and 25 months in children at familial risk for ADHD. Infant and Child Development, 17, 321338. doi:10.1002/icd.579CrossRefGoogle Scholar
Bandeen-roche, K., Miglioretti, D. L., Zeger, S. L., & Rathouz, P. J. (1997). Latent variable regression for multiple discrete outcomes. Journal of the American Statistical Association, 92, 13751386. doi:10.1080/01621459.1997.10473658CrossRefGoogle Scholar
Cicchetti, D. (1994). Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychological Assessment, 6, 284290. doi:10.1037/1040-3590.6.4.284CrossRefGoogle Scholar
Conners, K. C., Erhardt, D., & Sparrow, E. (1998). The Conners Adult ADHD Rating Scale (CAARS). Toronto: Multi-Health Systems Inc.Google Scholar
Corsello, C., Hus, V., Pickles, A., Risi, S., Cook, E. H., Leventhal, B. L., & Lord, C. (2007). Between a ROC and a hard place: Decision making and making decisions about using the SCQ. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 48, 932940. doi:10.1111/j.1469-7610.2007.01762.xCrossRefGoogle Scholar
Cuthbert, B. N. (2014). The RDoC framework: Facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology. World Psychiatry, 13, 2835. doi:10.1002/wps.20087CrossRefGoogle ScholarPubMed
Dalsgaard, S., Østergaard, S. D., Leckman, J. F., Mortensen, P. B., & Pedersen, M. G. (2015). Mortality in children, adolescents, and adults with attention deficit hyperactivity disorder: A nationwide cohort study. The Lancet, 385, 21902196. doi:10.1016/S0140-6736(14)61684-6CrossRefGoogle ScholarPubMed
DeWolfe, N. A., Byrne, J. M., & Bawden, H. N. (2000). Preschool inattention and impulsivity-hyperactivity: Development of a clinic-based assessment protocol. Journal of Attention Disorders, 4, 8090. doi:10.1177/108705470000400202CrossRefGoogle Scholar
Freitag, C. M. (2007). The genetics of autistic disorders and its clinical relevance: a review of the literature. Molecular Psychiatry, 12, 222. doi:10.1038/sj.mp.4001896CrossRefGoogle ScholarPubMed
Freitag, C. M., Rohde, L. A., Lempp, T., & Romanos, M. (2010). Phenotypic and measurement influences on heritability estimates in childhood ADHD. European Child and Adolescent Psychiatry, 19, 311323. doi:10.1007/s00787-010-0097-5CrossRefGoogle ScholarPubMed
Friard, O., & Gamba, M. (2016). BORIS: A free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology & Evolution, 7, 13251330. doi:10.1111/2041-210X.12584CrossRefGoogle Scholar
Fusar-Poli, P., Solmi, M., Brondino, N., Davies, C., Chae, C., Politi, P., … McGuire, P. (2019). Transdiagnostic psychiatry: A systematic review. World Psychiatry, 18, 192207. doi:10.1002/wps.20631CrossRefGoogle ScholarPubMed
Gimpel, G. A., & Kuhn, B. R. (2000). Maternal report of attention deficit hyperactivity disorder symptoms in preschool children. Child: Care, Health and Development, 26, 163176. discussion 176-179. doi:10.1046/j.1365-2214.2000.00126.xGoogle ScholarPubMed
Goodwin, A., Salomone, S., Bolton, P., Charman, T., Jones, E. J. H., Pickles, A., … Johnson, M. H. (2016). Attention training for infants at familial risk of ADHD (INTERSTAARS): Study protocol for a randomised controlled trial. Trials, 17, 608. doi:10.1186/s13063-016-1727-0CrossRefGoogle ScholarPubMed
Gopin, C., Healey, D., Castelli, K., Marks, D., & Halperin, J. M. (2010). Usefulness of a clinician rating scale in identifying preschool children with ADHD. Journal of Attention Disorders, 13, 479488. doi:10.1177/1087054709332476CrossRefGoogle ScholarPubMed
Hinshaw, S. P. (2015). Introduction: Developmental psychopathology, ontogenic process models, gene-environment interplay, and brain development: An emerging synthesis. Journal of Abnormal Psychology, 124, 771775. doi:10.1037/abn0000110CrossRefGoogle Scholar
Howlin, P., Moss, P., Savage, S., & Rutter, M. (2013). Social outcomes in mid- to later adulthood among individuals diagnosed with autism and average nonverbal IQ as children. Journal of the American Academy of Child and Adolescent Psychiatry, 52, 572581. doi:10.1016/j.jaac.2013.02.017CrossRefGoogle ScholarPubMed
Howse, R. B., Calkins, S. D., Anastopoulos, A. D., Keane, S. P., & Shelton, T. L. (2003). Regulatory contributors to children's kindergarten achievement. Early Education & Development, 14, 101120. doi:10.1207/s15566935eed1401_7CrossRefGoogle Scholar
Johnson, M. H., Gliga, T., Jones, E., & Charman, T. (2015). Annual research review: Infant development, autism, and ADHD – Early pathways to emerging disorders. Journal of Child Psychology and Psychiatry, 56, 228247. doi:10.1111/jcpp.12328CrossRefGoogle ScholarPubMed
Konst, M. J., Matson, J. L., Goldin, R., & Rieske, R. (2014). How does ASD symptomology correlate with ADHD presentations? Research in Developmental Disabilities, 35, 22522259. doi:10.1016/j.ridd.2014.05.017CrossRefGoogle ScholarPubMed
Kuriyan, A. B., Pelham, W. E., Molina, B. S. G., Waschbusch, D. A., Gnagy, E. M., Sibley, M. H., … Kent, K. M. (2013). Young adult educational and vocational outcomes of children diagnosed with ADHD. Journal of Abnormal Child Psychology, 41, 2741. doi:10.1007/s10802-012-9658-zCrossRefGoogle ScholarPubMed
Lavelle, T. A., Weinstein, M. C., Newhouse, J. P., Munir, K., Kuhlthau, K. A., Prosser, L. A., … Newschaffer, C. (2014). Economic burden of childhood autism spectrum disorders. Pediatrics, 133, e520–9. doi:10.1542/peds.2013-0763CrossRefGoogle ScholarPubMed
Lo, Y., Mendell, N., & Rubin, D. (2001). Testing the number of components in a normal mixture. Biometrika, 88, 767778. doi:10.1093/biomet/88.3.767CrossRefGoogle Scholar
Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism Diagnostic Observation Schedule, (ADOS-2) Modules 1-4. Los Angeles, CA: Western Psychological Corporation.Google Scholar
Maenner, M. J., Shaw, K. A., Baio, J., Washington, A., Patrick, M., DiRienzo, M., … Dietz, P. M. (2020). Prevalence of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network, 11 sites, United States, 2016. MMWR Surveillance Summaries, 69, 112.CrossRefGoogle Scholar
Matza, L. S., Paramore, C., & Prasad, M. (2005). A review of the economic burden of ADHD. Cost Effectiveness and Resource Allocation, 3, 5. doi:10.1186/1478-7547-3-5CrossRefGoogle ScholarPubMed
Mayes, S. D., Calhoun, S. L., Mayes, R. D., & Molitoris, S. (2012). Autism and ADHD: Overlapping and discriminating symptoms. Research in Autism Spectrum Disorders, 6, 277285. doi:10.1016/j.rasd.2011.05.009CrossRefGoogle Scholar
McCulloch, C., Searle, S., & Neuhaus, J. (2008). Generalized, linear, and mixed models. Hoboken, NJ: Wiley.Google Scholar
McGoey, K. E., DuPaul, G. J., Haley, E., & Shelton, T. L. (2007). Parent and teacher ratings of attention-deficit/hyperactivity disorder in preschool: The ADHD rating scale-IV preschool version. Journal of Psychopathology and Behavioral Assessment, 29, 269276. doi:10.1007/s10862-007-9048-yCrossRefGoogle Scholar
Miller, M., Iosif, A. M., Young, G. S., Bell, L. J., Schwichtenberg, A. J., Hutman, T., & Ozonoff, S. (2019a). The dysregulation profile in preschoolers with and without a family history of autism spectrum disorder. Journal of Child Psychology and Psychiatry, 60, 516523. doi:10.1111/jcpp.13003CrossRefGoogle Scholar
Miller, M., Iosif, A., Young, G., Hill, M., Phelps Hanzel, E., Hutman, T., … Ozonoff, S. (2016). School-age outcomes of infants at risk for autism spectrum disorder. Autism Research, 9, 632642. doi:10.1002/aur.1572CrossRefGoogle ScholarPubMed
Miller, M., Musser, E., Young, G., Olson, B., Steiner, R., & Nigg, J. (2019m). Sibling recurrence risk and cross-aggregation of attention-deficit/hyperactivity disorder and autism spectrum disorder. JAMA Pediatrics, 173, 147152. doi:10.1001/jamapediatrics.2018.4076CrossRefGoogle Scholar
Mitchell, S. K. (1979). Interobserver agreement, reliability, and generalizability of data collected in observational studies. Psychological Bulletin, 86, 376390. doi:10.1037/0033-2909.86.2.376CrossRefGoogle Scholar
Moffitt, T. E., Arseneault, L., Belsky, D., Dickson, N., Hancox, R. J., Harrington, H., … Caspi, A. (2011). A gradient of childhood self-control predicts health, wealth, and public safety. Proceedings of the National Academy of Sciences of the United States of America, 108, 26932698. doi:10.1073/pnas.1010076108CrossRefGoogle ScholarPubMed
Mullen, E. M. (1995). Mullen Scales of Early Learning, AGS Edition: Manual and item administrative books. American Guidance Services, Inc., 192.Google Scholar
Musser, E. D., Hawkey, E., Kachan-Liu, S. S., Lees, P., Roullet, J. B., Goddard, K., … Nigg, J. T. (2014). Shared familial transmission of autism spectrum and attention-deficit/ hyperactivity disorders. Journal of Child Psychology and Psychiatry, 55, 819827. doi:10.1111/jcpp.12201CrossRefGoogle ScholarPubMed
Muthén, L. K., & Muthén, B. O. (2017). Mplus user's guide (Eighth Edition). Los Angeles, CA.Google Scholar
Nylund, K. L., Asparouhov, T., & Muthén, B. O. (2007). Deciding on the number of classes in latent class analysis and growth mixture modeling: A Monte Carlo simulation study. Structural Equation Modeling, 14, 535569. doi:10.1080/10705510701575396CrossRefGoogle 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, 256266e2. doi:10.1097/00004583-201003000-00009Google ScholarPubMed
Ozonoff, S., Young, G. S., Belding, A., Hill, M., Hill, A., Hutman, T., … 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, 398407.e2. doi:10.1016/j.jaac.2013.12.020CrossRefGoogle ScholarPubMed
Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., … Stone, W. L. (2011). Recurrence risk for autism spectrum disorders: A Baby Siblings Research Consortium study. Pediatrics, 128, e488–95. doi:10.1542/peds.2010-2825Google ScholarPubMed
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, 56, 988998. doi:10.1111/jcpp.12421CrossRefGoogle ScholarPubMed
Rommelse, N. N. J., Franke, B., Geurts, H. M., Hartman, C. A., & Buitelaar, J. K. (2010). Shared heritability of attention-deficit/hyperactivity disorder and autism spectrum disorder. European Child and Adolescent Psychiatry, 19, 281295. doi:10.1007/s00787-010-0092-xCrossRefGoogle ScholarPubMed
Rommelse, N. N. J., Geurts, H. M., Franke, B., Buitelaar, J. K., & Hartman, C. A. (2011). A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes. Neuroscience and Biobehavioral Reviews, 35, 13631396. doi:10.1016/j.neubiorev.2011.02.015CrossRefGoogle ScholarPubMed
Ronald, A., Larsson, H., Anckarsäter, H., & Lichtenstein, P. (2014). Symptoms of autism and ADHD: A Swedish twin study examining their overlap. Journal of Abnormal Psychology, 49, 535542. doi:10.1037/a0036088Google Scholar
Ronald, A., Simonoff, E., Kuntsi, J., Asherson, P., & Plomin, R. (2008). Evidence for overlapping genetic influences on autistic and ADHD behaviours in a community twin sample. Journal of Child Psychology and Psychiatry, 49, 535542. doi:10.1111/j.1469-7610.2007.01857.xCrossRefGoogle Scholar
Rubin, D. (1987). Multiple imputation for nonresponse in surveys. New York, NY: John Wiley & Sons, Inc.CrossRefGoogle Scholar
Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire. Los Angeles, CA: Western Psychological Services.Google Scholar
Shephard, E., Bedford, R., Milosavljevic, B., Gliga, T., Jones, E. J. H., Pickles, A., … Charman, T. (2019). Early developmental pathways to childhood symptoms of attention-deficit hyperactivity disorder, anxiety and autism spectrum disorder. Journal of Child Psychology and Psychiatry, 60, 963974. doi:10.1111/jcpp.12947CrossRefGoogle ScholarPubMed
Stergiakouli, E., Davey Smith, G., Martin, J., Skuse, D. H., Viechtbauer, W., Ring, S. M., … St Pourcain, B. (2017). Shared genetic influences between dimensional ASD and ADHD symptoms during child and adolescent development. Molecular Autism, 8, 18. doi:10.1186/s13229-017-0131-2CrossRefGoogle ScholarPubMed
Sullivan, E. L., Holton, K. F., Nousen, E. K., Barling, A. N., Sullivan, C. A., Propper, C. B., & Nigg, J. T. (2015). Early identification of ADHD risk via infant temperament and emotion regulation: A pilot study. Journal of Child Psychology and Psychiatry, 56, 949957. doi:10.1111/jcpp.12426CrossRefGoogle ScholarPubMed
Taylor, M. J., Charman, T., & Ronald, A. (2015). Where are the strongest associations between autistic traits and traits of ADHD? Evidence from a community-based twin study. European Child and Adolescent Psychiatry, 24, 11291138. doi:10.1007/s00787-014-0666-0CrossRefGoogle ScholarPubMed
Uebel, H., Albrecht, B., Asherson, P., Börger, N. A., Butler, L., Chen, W., … Banaschewski, T. (2010). Performance variability, impulsivity errors and the impact of incentives as gender-independent endophenotypes for ADHD. Journal of Child Psychology and Psychiatry, 51, 210218. doi:10.1111/j.1469-7610.2009.02139.xCrossRefGoogle ScholarPubMed
Van Der Meer, J. M. J., Oerlemans, A. M., Van Steijn, D. J., Lappenschaar, M. G. A., De Sonneville, L. M. J., Buitelaar, J. K., & Rommelse, N. N. J. (2012). Are autism spectrum disorder and attention-deficit/hyperactivity disorder different manifestations of one overarching disorder? Cognitive and symptom evidence from a clinical and population-based sample. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 11601172. doi:10.1016/j.jaac.2012.08.024CrossRefGoogle ScholarPubMed
Visser, S. N., Danielson, M. L., Bitsko, R. H., Holbrook, J. R., Kogan, M. D., Ghandour, R. M., … Blumberg, S. J. (2014). Trends in the parent-report of health care provider-diagnosed and medicated attention-deficit/hyperactivity disorder: United States, 2003–2011. Journal of the American Academy of Child and Adolescent Psychiatry, 53. doi:10.1016/j.jaac.2013.09.001Google ScholarPubMed
Willcutt, E. G., Pennington, B. F., Duncan, L., Smith, S. D., Keenan, J. M., Wadsworth, S., … Olson, R. K. (2010). Understanding the complex etiologies of developmental disorders: behavioral and molecular genetic approaches. Journal of Developmental & Behavioral Pediatrics, 31, 533544. doi:10.1097/DBP.0b013e3181ef42a1CrossRefGoogle ScholarPubMed
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