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Original Investigation |

Parental Social Responsiveness and Risk of Autism Spectrum Disorder in Offspring

Kristen Lyall, ScD1,2; John N. Constantino, MD3; Marc G. Weisskopf, PhD, ScD4,5; Andrea L. Roberts, PhD6; Alberto Ascherio, MD, DrPH1,4,7; Susan L. Santangelo, ScD4,8
[+] Author Affiliations
1Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts
2Department of Public Health Sciences, University of California, Davis
3Department of Psychiatry, Washington University, St Louis, Missouri
4Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts
5Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts
6Department of Social and Behavioral Sciences, Harvard School of Public Health, Boston, Massachusetts
7Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts
8Department of Psychiatry, Maine Medical Center/Maine Medical Center Research Institute, Portland
JAMA Psychiatry. 2014;71(8):936-942. doi:10.1001/jamapsychiatry.2014.476.
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Importance  Although autism spectrum disorder (ASD) is known to be heritable, patterns of inheritance of subclinical autistic traits in nonclinical samples are poorly understood.

Objective  To examine the familiality of Social Responsiveness Scale (SRS) scores of individuals with and without ASD.

Design, Setting, and Participants  We performed a nested case-control study (pilot study: July 1, 2007, through June 30, 2009; full-scale study: September 15, 2008, through September 14, 2012) within a population-based longitudinal cohort. Participants were drawn from the Nurses’ Health Study II, a cohort of 116 430 female nurses recruited in 1989. Case participants were index children with reported ASD; control participants were frequency matched by year of birth of case participants among those not reporting ASD. Of 3161 eligible participants, 2144 nurses (67.8%) returned SRS forms for a child and at least 1 parent and were included in these analyses.

Exposure  The SRS scores, as reported by nurse mothers and their spouses, were examined in association with risk of ASD using crude and adjusted logistic regression analyses. The SRS scores of the children were examined in association with SRS scores of the parents using crude and adjusted linear regression analyses stratified by case status.

Main Outcomes and Measures  Autism spectrum disorder, assessed by maternal report, validated in a subgroup with the Autism Diagnostic Interview–Revised.

Results  A total of 1649 individuals were included in these analyses, including 256 ASD case participants, 1393 control participants, 1233 mothers, and 1614 fathers. Risk of ASD was increased by 85.0% among children whose parents had concordantly elevated SRS scores (odds ratio [OR], 1.85; 95% CI, 1.08-3.16) and by 52.0% when the score of either parent was elevated (OR, 1.52; 95% CI, 1.11-2.06). Elevated scores of the father significantly increased the risk of ASD in the child (OR, 1.94; 95% CI, 1.38-2.71), but no association was seen with elevated scores of the mother. Elevated parent scores significantly increased child scores in controls, corresponding to an increase in 23 points (P < .001).

Conclusions and Relevance  These findings support the role of additive genetic influences in concentrating inherited ASD susceptibility in successive generations and the potential role of preferential mating, and suggest that typical variation in parental social functioning can produce clinically significant differences in offspring social traits.

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Figures

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Figure 1.
Density Plot of Raw Social Responsiveness Scale (SRS-A) Scores

Values below 0 are due to the plotting of the smoothed density distribution of the SRS-A score.

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Figure 2.
Density Plot of Raw Social Responsiveness Scale (SRS) Scores of Children According to Parent Elevated Scores

Values below 0 are due to the plotting of the smoothed density distribution of the SRS score.

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Figure 3.
Association Between Raw Social Responsiveness Scale (SRS) Scores of Children and Quintiles of Raw SRS-A Scores of Parents in Control Participants

Results of multivariate linear regression, using the lowest quintile (quintile 1) of the parent score as the referent for respective mother and father models. Results were adjusted for child year of birth, child sex, maternal age, household income, reported maternal depression, and reported attention-deficit/hyperactivity disorder in the child. Error bars indicate SEs. Models for mothers and fathers were run separately; adjustment of the scores of the mother for scores of the father slightly attenuated results, whereas adjustment of the scores of the father for scores of the mother did not materially alter quintile estimates. Tests of trend were significant for the mother and father models (P < .001).

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