Abstract
Objectives
Differences in the development of autistic children have been observed within the first year of life. Infant siblings of autistic children who are later diagnosed with autism themselves have differences in temperament, social communication, attention, and sensory and motor behaviors by 12 months of age. However, less is known about the early development of other increased-likelihood groups. Some studies have identified that children born to mothers with asthma have a slightly elevated likelihood of autism. However, no studies have examined other aspects of their early development.
Methods
Using a case series design, we profiled the temperament (Carey Temperament Scales), sensory (Sensory Profile 2), and global developmental features (Bayley-III) of seven Australian infants born to mothers with asthma who were screened to have an elevated likelihood of autism (First Year Inventory).
Results
We found differences from the norms in temperament across the three timepoints (6 weeks, 6 months, and 12 months), in the domains of rhythmicity, mood, persistence, and distractibility. Infants had typical sensory features at 6 weeks and 6 months; however, a sensory-sensitivity subtype was observed at 12 months. Lastly, at 12 months, cognitive skills were mostly typical, language skills were underdeveloped, and motor skills varied between infants.
Conclusions
Results suggest that there may be a developmental profile indicative of an elevated likelihood of autism in infants born to mothers with asthma. However, due to the small sample size, these findings need to be considered with caution. Further research is needed to confirm diagnoses of autism in our sample.
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References
Albers, C. A., & Grieve, A. J. (2006). Test review: Bayley scales of infant and toddler development–third edition. Journal of Psychoeducational Assessment, 25(2), 180–190. https://doi.org/10.1177/0734282906297199
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). American Psychiatric Association. https://doi.org/10.1176/appi.books.9780890425596
Baranek, G. T. (1999). Autism during infancy: A retrospective video analysis of sensory-motor and social behaviors at 9–12 months of age. Journal of Autism and Developmental Disorders, 29(3), 213–224. https://doi.org/10.1023/A:1023080005650
Baranek, G. T., David, F. J., Poe, M. D., Stone, W. L., & Watson, L. R. (2006). Sensory experiences questionnaire: Discriminating sensory features in young children with autism, developmental delays, and typical development. Journal of Child Psychology and Psychiatry, 47(6), 591–601. https://doi.org/10.1111/j.1469-7610.2005.01546.x
Barbaro, J., & Dissanayake, C. (2010). Prospective identification of autism spectrum disorders in infancy and toddlerhood using developmental surveillance: The social attention and communication study. Journal of Developmental & Behavioral Pediatrics, 31(5), 376–385. https://doi.org/10.1097/dbp.0b013e3181df7f3c
Bayley, N. (2006). Bayley scales of infant and toddler development (3rd ed.). Harcourt.
Betancur, C. (2011). Etiological heterogeneity in autism spectrum disorders: More than 100 genetic and genomic disorders and still counting. Brain Research, 1380, 42–77. https://doi.org/10.1016/j.brainres.2010.11.078
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(1), 12–24. https://doi.org/10.1007/s10803-006-0328-2
Carey, W. B., & McDevitt, S. C. (1978). Revision of the infant temperament questionnaire. Pediatrics, 61(5), 735–739. https://doi.org/10.1037/t05932-000
Chuang, I. C., Tseng, M.-H., Lu, L., & Shieh, J.-Y. (2012). Sensory correlates of difficult temperament characteristics in preschool children with autism. Research in Autism Spectrum Disorders, 6(3), 988 995. https://doi.org/10.1016/j.rasd.2012.01.002
Clifton, V. L., Engel, P., Smith, R., Gibson, P., Brinsmead, M., & Giles, W. B. (2009). Maternal and neonatal outcomes of pregnancies complicated by asthma in an Australian population. The Australian and New Zealand Journal of Obstetrics & Gynaecology, 49(6), 619–626. https://doi.org/10.1111/j.1479-828X.2009.01077.x
Coleman, M. T., & Rund, D. A. (1997). Nonobstetric conditions causing hypoxia during pregnancy: Asthma and epilepsy. American Journal of Obstetrics and Gynecology, 177(1), 1–7. https://doi.org/10.1016/S0002-9378(97)70429-0
Croen, L. A., Grether, J. K., Yoshida, C. K., Odouli, R., & Van de Water, J. (2005). Maternal autoimmune diseases, asthma and allergies, and childhood autism spectrum disorders: A case-control study. Archives of Pediatrics & Adolescent Medicine, 159(2), 151–157. https://doi.org/10.1001/archpedi.159.2.151
Croen, L. A., Qian, Y., Ashwood, P., Daniels, J. L., Fallin, D., Schendel, D., Schieve, L. A., Singer, A. B., & Zerbo, O. (2019). Family history of immune conditions and autism spectrum and developmental disorders: Findings from the study to explore early development. Autism Research, 12(1), 123–135. https://doi.org/10.1002/aur.1979
Dellapiazza, F., Michelon, C., Oreve, M. J., Robel, L., Schoenberger, M., Chatel, C., Vesperini, S., Maffre, T., Schmidt, R., Blanc, N., Vernhet, C., Picot, M. C., Baghdadli, A., & ELENA study group. . (2020). The impact of atypical sensory processing on adaptive functioning and maladaptive behaviors in autism spectrum disorder during childhood: Results from the ELENA cohort. Journal of Autism and Developmental Disorders, 50(6), 2142–2152. https://doi.org/10.1007/s10803-019-03970-w
Delobel-Ayoub, M., Arnaud, C., White-Koning, M., Casper, C., Pierrat, V., Garel, M., Burguet, A., Roze, J.-C., Matis, J., & Picaud, J.-C. (2009). Behavioral problems and cognitive performance at 5 years of age after very preterm birth: The EPIPAGE Study. Pediatrics, 123(6), 1485–1492. https://doi.org/10.1542/peds.2008-1216
Dunn, W. (2014). Sensory Profile 2 manual. PsychCorp.
Dunn, W., & Daniels, D. B. (2002). Initial development of the infant/toddler sensory profile. Journal of Early Intervention, 25(1), 27–41. https://doi.org/10.1177/105381510202500104
Eigsti, I.-M., de Marchena, A. B., Schuh, J. M., & Kelley, E. (2011). Language acquisition in autism spectrum disorders: A developmental review. Research in Autism Spectrum Disorders, 5(2), 681–691. https://doi.org/10.1016/j.rasd.2010.09.001
Einspieler, C., Sigafoos, J., Bartl-Pokorny, K. D., Landa, R., Marschik, P. B., & Bölte, S. (2014). Highlighting the first 5 months of life: General movements in infants later diagnosed with autism spectrum disorder or Rett syndrome. Research in Autism Spectrum Disorders, 8(3), 286–291. https://doi.org/10.1016/j.rasd.2013.12.013
Fernell, E., Eriksson, & Gillberg, C. (2013). Early diagnosis of autism and impact on prognosis: A narrative review. Clinical Epidemiology, 5, 33-44. https://doi.org/10.2147/clep.s41714.
Garon, N., Zwaigenbaum, L., Bryson, S., Smith, I. M., Brian, J., Roncadin, C., Vaillancourt, T., Armstrong, V., Sacrey, L.-A.R., & Roberts, W. (2016). Temperament and its association with autism symptoms in a high-risk population. Journal of Abnormal Child Psychology, 44(4), 757–769. https://doi.org/10.1007/s10802-015-0064-1
Georgiades, S., Szatmari, P., & Boyle, M. (2013). Importance of studying heterogeneity in autism. Neuropsychiatry, 3(2), 123–125. https://doi.org/10.2217/npy.13.8
Global Initiative for Asthma. (2017). Global strategy for asthma management and prevention. http://www.ginasthma.org/
Gong, T., Lundholm, C., Rejnö, G., Bölte, S., Larsson, H., D’Onofrio, B. M., Lichtenstein, P., & Almqvist, C. (2019). Parental asthma and risk of autism spectrum disorder in offspring: A population and family-based case-control study. Clinical & Experimental Allergy, 49, 883–891. https://doi.org/10.1111/cea.13353
Green, E., Stroud, L., Bloomfield, S., Cronje, J., Foxcroft, C., Hurter, K., Lane, H., Marais, R., Marx, C., McAlinden, P., Paradice, R., & Venter, D. (2016). Griffiths scales of child development (3rd ed.). Hogrefe.
Grzeskowiak, L. E., Smith, B., Roy, A., Dekker, G. A., & Clifton, V. L. (2016). Patterns, predictors and outcomes of asthma control and exacerbations during pregnancy: A prospective cohort study. ERJ Open Research, 2(1), e00054-02015. https://doi.org/10.1183/23120541.00054-2015
Guerra, C. C., Moraes Barros, M. C., Goulart, A. L., Fernandes, L. V., Kopelman, B. I., & dos Santos, A. (2014). Premature infants with birth weights of 1500–1999g exhibit considerable delays in several developmental areas. Acta Pædiatrica, 103(1), e1–e6. https://doi.org/10.1111/apa.12430
Hepburn, S. L., & Stone, W. L. (2006). Using carey temperament scales to assess behavioral style in children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(5), 637–642. https://doi.org/10.1007/s10803-006-0110-5
IBM Corporation. (2017). IBM SPSS Statistics (Version 25) [computer software]. IBM Corporation.
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
Landry, O., & Al-Taie, S. (2016). A meta-analysis of the wisconsin card sort task in autism. Journal of Autism and Developmental Disorders, 46(4), 1220–1235. https://doi.org/10.1007/s10803-015-2659-3
Lane, A. E., Molloy, C. A., & Bishop, S. L. (2014). Classification of children with autism spectrum disorder by sensory subtype: A case for sensory-based phenotypes. Autism Research, 7(3), 322–333. https://doi.org/10.1002/aur.1368
Maestro, S., Muratori, F., Cavallaro, M. C., Pei, F., Stern, D., Golse, B., & Palacio-Espasa, F. (2002). Attentional skills during the first 6 months of age in autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 41(10), 1239–1245. https://doi.org/10.1097/00004583-200210000-00014
Maestro, S., Muratori, F., Cesari, A., Cavallaro, M., Paziente, A., Pecini, C., Grassi, C., Manfredi, A., & Sommario, C. (2005). Course of autism signs in the first year of life. Psychopathology, 38(1), 26–31. https://doi.org/10.1159/000083967
Mallise, C. A., Lane, A. E., Woolard, A. J., Whalen, O. M., Murphy, V. E., Karayanidis, F., & Campbell, L. E. (2020). The temperament features associated with autism spectrum disorder in childhood: A systematic review. Research in Developmental Disabilities, 104, 103711. https://doi.org/10.1016/j.ridd.2020.103711
Masi, A., Demayo, M. M., Glozier, N., & Guastella, A. J. (2017). An overview of autism spectrum disorder, heterogeneity and treatment options. Neuroscience Bulletin, 33(2), 183–193. https://doi.org/10.1007/s12264-017-0100-y
Micai, M., Fulceri, F., Caruso, A., Guzzetta, A., Gila, L., & Scattoni, M. L. (2020). Early behavioral markers for neurodevelopmental disorders in the first 3 years of life: An overview of systematic reviews. Neuroscience & Biobehavioral Reviews, 116, 183–201. https://doi.org/10.1016/j.neubiorev.2020.06.027
Miller, H. L., Ragozzino, M. E., Cook, E. H., Sweeney, J. A., & Mosconi, M. W. (2015). Cognitive set shifting deficits and their relationship to repetitive behaviors in autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(3), 805–815. https://doi.org/10.1007/s10803-014-2244-1
Mozolic-Staunton, B., Donelly, M., Yoxall, J., & Barbaro, J. (2020). Early detection for better outcomes: Universal developmental surveillance for autism across health and early childhood education settings. Research in Autism Spectrum Disorders, 71, 101496. https://doi.org/10.1016/j.rasd.2019.101496
Murphy, V. E., & Gibson, P. G. (2009). Asthma in pregnancy. In K. Rosene-Montella & G. Bourjeily (Eds.), Pulmonary problems in pregnancy: Clinical and research aspects (pp. 143–162). Humana Press. https://doi.org/10.1007/978-1-59745-445-2_11
Murphy, V. E., Jensen, M. E., Mattes, J., Hensley, M. J., Giles, W. B., Peek, M. J., Bisits, A., Callaway, L. K., McCaffery, K., Barrett, H. L., Colditz, P. B., Seeho, S. K., Attia, J., Searles, A., Doran, C., Powell, H., & Gibson, P. G. (2016). The breathing for life trial: A randomised controlled trial of fractional exhaled nitric oxide (FENO)-based management of asthma during pregnancy and its impact on perinatal outcomes and infant and childhood respiratory health. BMC Pregnancy and Childbirth, 16(1), 111–120. https://doi.org/10.1186/s12884-016-0890-3
Murphy, V. E., Namazy, J., Powell, H., Schatz, M., Chambers, C., Attia, J., & Gibson, P. (2011). A meta-analysis of adverse perinatal outcomes in women with asthma. BJOG: An International Journal of Obstetrics and Gynaecology, 118(11), 1314–1323. https://doi.org/10.1111/j.1471-0528.2011.03055.x
Niedźwiecka, A., Domasiewicz, Z., Kawa, R., Tomalski, P., & Pisula, E. (2019). Sensory processing in toddlers with autism spectrum disorders. European Journal of Developmental Psychology, 17(4), 527–555. https://doi.org/10.1080/17405629.2019.1676715
Ozonoff, S., Iosif, A. M., Baguio, F., Cook, I. C., Hill, M. M., Hutman, T., Rogers, S. J., Rozga, A., Sangha, S., Sigman, M., Steinfeld, M. B., & 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(3), 256–266. https://doi.org/10.1016/j.jaac.2009.11.009
Patel, S., Cooper, M. N., Jones, H., Whitehouse, A. J. O., Dale, R. C., & Guastella, A. J. (2020a). Maternal immune-related conditions during pregnancy may be a risk factor for neuropsychiatric problems in offspring throughout childhood and adolescence. Psychological Medicine, 1–11. https://doi.org/10.1017/S0033291720001580
Patel, S., Dale, R. C., Rose, D., Heath, B., Nordahl, C. W., Rogers, S., Guastella, A. J., & Ashwood, P. (2020b). Maternal immune conditions are increased in males with autism spectrum disorders and are associated with behavioural and emotional but not cognitive co-morbidity. Translational Psychiatry, 10(1), 286. https://doi.org/10.1038/s41398-020-00976-2
Philpott-Robinson, K., Lane, A. E., & Harpster, K. (2016). Sensory features of toddlers at risk for autism spectrum disorder. The American Journal of Occupational Therapy, 70(4), e7004220010. https://doi.org/10.5014/ajot.2016.019497
Poljac, E., Hoofs, V., Princen, M. M., & Poljac, E. (2017). Understanding behavioural rigidity in autism spectrum conditions: The role of intentional control. Journal of Autism and Developmental Disorders, 47(3), 714–727. https://doi.org/10.1007/s10803-016-3010-3
Psimas, L. (2014, October 23–25). Assessing sensory strengths and challenges [short course]. Illinois Occupational Therapy Association Annual Conference, Naperville, IL, Unites States.
Raudeliūnaitė, R., & Steponėnienė, E. (2020). Challenges for primary school teachers in ensuring inclusive education for children with Autism Spectrum Disorders. Pedagogika, 138(2), 209–225. https://doi.org/10.15823/p.2020.138.12
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(9), 1691–1710. https://doi.org/10.1007/s10803-006-0303-y
Sacrey, L. A. R., Zwaigenbaum, L., Bryson, S., Brian, J., Smith, I. M., Roberts, W., Szatmari, P., Roncadin, C., Garon, N., & Novak, C. (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 & Adolescent Psychiatry, 54(6), 470–478. https://doi.org/10.1016/j.jaac.2015.03.014
Schieve, L. A., Tian, L. H., Rankin, K., Kogan, M. D., Yeargin-Allsopp, M., Visser, S., & Rosenberg, D. (2016). Population impact of preterm birth and low birth weight on developmental disabilities in US children. Annals of Epidemiology, 26(4), 267–274. https://doi.org/10.1016/j.annepidem.2016.02.012
Simpson, K., Adams, D., Alston-Knox, C., Heussler, H. S., & Keen, D. (2019). Exploring the sensory profiles of children on the autism spectrum using the Short Sensory Profile-2 (SSP-2). Journal of Autism and Developmental Disorders, 49(5), 2069–2079. https://doi.org/10.1007/s10803-019-03889-2
Stroustrup, A., Hsu, H.-H., Svensson, K., Schnaas, L., Cantoral, A., González, M. S., Torres-Calapiz, M., Amarasiriwardena, C., Bellinger, D. C., & Coull, B. A. (2016). Toddler temperament and prenatal exposure to lead and maternal depression. Environmental Health, 15(1), e71. https://doi.org/10.1186/s12940-016-0147-7
Takeuchi, A., Yorifuji, T., Takahashi, K., Nakamura, M., Kageyama, M., Kubo, T., Ogino, T., & Doi, H. (2016). Neurodevelopment in full-term small for gestational age infants: A nationwide Japanese population-based study. Brain & Development, 38(6), 529–537. https://doi.org/10.1016/j.braindev.2015.12.013
Tees, M. T., Harville, E. W., Xiong, X., Buekens, P., Pridjian, G., & Elkind-Hirsch, K. (2010). Hurricane Katrina-related maternal stress, maternal mental health, and early infant temperament. Maternal and Child Health Journal, 14(4), 511–518. https://doi.org/10.1007/s10995-009-0486-x
Tomchek, S. D., & Dunn, W. (2007). Sensory processing in children with and without autism: A comparative study using the short sensory profile. The American Journal of Occupational Therapy, 61(2), 190–200. https://doi.org/10.5014/ajot.61.2.190
Turner-Brown, L. M., Baranek, G. T., Reznick, J. S., Watson, L. R., & Crais, E. R. (2013). The First Year Inventory: A longitudinal follow-up of 12-month-olds to 3 years of age. Autism, 17(5), 527–540. https://doi.org/10.1177/1362361312439633
Veness, C., Prior, M., Bavin, E., Eadie, P., Cini, E., & Reilly, S. (2012). Early indicators of autism spectrum disorders at 12 and 24 months of age: A prospective, longitudinal comparative study. Autism, 16(2), 163–177. https://doi.org/10.1177/1362361311399936
Volkmar, F. R. (2014). Editorial: The importance of early intervention. Journal of Autism and Developmental Disorders, 44(12), 2979–2980. https://doi.org/10.1007/s10803-014-2265-9
Weitlauf, A. S., Gotham, K. O., Vehorn, A. C., & Warren, Z. E. (2014). Brief report: DSM-5 “levels of support:” A comment on discrepant conceptualizations of severity in ASD. Journal of Autism and Developmental Disorders, 44(2), 471–476. https://doi.org/10.1007/s10803-013-1882-z
Whalen, O. M., Karayanidis, F., Murphy, V. E., Lane, A. E., Mallise, C. A., & Campbell, L. E. (2019, 2019/02/01). The effects of maternal asthma during pregnancy on child cognitive and behavioral development: A systematic review. Journal of Asthma, 56(2), 130–141. https://doi.org/10.1080/02770903.2018.1437174
Yin, R. K. (2018). Case study research and applications: Design and methods (6th ed.). SAGE Publications.
Zwaigenbaum, L., Bauman, M. L., Stone, W. L., Yirmiya, N., Estes, A., Hansen, R. L., McPartland, J. C., Natowicz, M. R., Choueiri, R., Fein, D., Kasari, C., Pierce, K., Buie, T., Carter, A., Davis, P. A., Granpeesheh, D., Mailloux, Z., Newschaffer, C., Robins, D., … Wetherby, A. (2015). Early identification of autism spectrum disorder: Recommendations for practice and research. Pediatrics, 136(Supplement), S10-S40. https://doi.org/10.1542/peds.2014-3667c
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
Acknowledgements
This manuscript was prepared from part of the first author’s doctoral dissertation. The authors would like to thank the researchers and staff from the Breathing for Life Trial and Breathing for Life Trial-Infant Development research projects who contributed to participant recruitment and data collection, particularly Kelly Steel. An additional thank you to Annelies Robijn who assisted in the extraction and coding of pregnancy data for the asthma cohort. We would also like to thank the mothers and infants who participated in this research study.
Funding
CAM, AW, and OMW were supported by a Research Training Program Stipend Scholarship provided by the Australian Government. VEM was supported by a Career Development Fellowship from the National Health and Medical Research Council (1084816). The Breathing for Life Trial research project was supported by a National Health and Medical Research Council project grant (1060983). This research was conducted with financial assistance from the Priority Research Centre GrowUpWell® at The University of Newcastle. The funding bodies had no role in the design of the study, data collection, data analysis, interpretation of data nor in writing the manuscript.
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CAM: designed the study, collected, analyzed and interpreted data, wrote and revised the manuscript. AEL: contributed to the study conception, collected and interpreted data, commented on manuscript. VEM: contributed to the study conception, commented on manuscript. AW: collected data and commented on manuscript. OMW: collected data, commented on and edited manuscript. PGG: contributed to the study conception, commented on manuscript. FK: contributed to the study conception, commented on manuscript. LEC: contributed to the study conception and design, collected and interpreted data, revised manuscript.
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All procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and standards, laid down in the 1964 Helsinki Declaration. Ethical approval of the study was granted by the Hunter New England Human Research Ethics Committee (15/05/20/4.05) and the University of Newcastle Human Research Ethics Committee (H-2015-0307).
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Mallise, C.A., Lane, A.E., Murphy, V.E. et al. Developmental Profiles of Infants with an Elevated Likelihood of Autism Who Were Born to Mothers with Asthma: a Case Series. Adv Neurodev Disord 5, 473–487 (2021). https://doi.org/10.1007/s41252-021-00221-x
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DOI: https://doi.org/10.1007/s41252-021-00221-x