Prenatal paternal anxiety symptoms predict child DHEA levels and internalizing symptoms during adrenarche

Sherri Lee Jones; Victoria De Braga; Christina Caccese; Jimin Lew; Guillaume Elgbeili; Natalie Castellanos-Ryan; Sophie Parent; Gina Muckle; Catherine M Herba; William D Fraser; Simon Ducharme; Julia Barnwell; Jacquetta Trasler; Jean R Séguin; Tuong-Vi Nguyen; Tina C Montreuil

doi:10.3389/fnbeh.2023.1217846

Prenatal paternal anxiety symptoms predict child DHEA levels and internalizing symptoms during adrenarche

Front Behav Neurosci. 2024 Jan 4:17:1217846. doi: 10.3389/fnbeh.2023.1217846. eCollection 2023.

Authors

Sherri Lee Jones^{1

2

3}, Victoria De Braga^{1

2

4}, Christina Caccese^{1

2}, Jimin Lew^{2

5}, Guillaume Elgbeili^{2

3}, Natalie Castellanos-Ryan⁶, Sophie Parent⁶, Gina Muckle⁷, Catherine M Herba^{8

9}, William D Fraser^{8

10}, Simon Ducharme^{1

3}, Julia Barnwell^{2

11

12}, Jacquetta Trasler^{2

11

12}, Jean R Séguin^{8

13}, Tuong-Vi Nguyen^{1

2

14}, Tina C Montreuil^{1

2

8

11

15}

Affiliations

¹ Department of Psychiatry, Faculty of Medicine and Health Sciences, McGill University, Montreal, QC, Canada.
² Department of Psychiatry, Research Institute of the McGill University Health Center, Montreal, QC, Canada.
³ Department of Psychiatry, Douglas Research Center, Douglas Mental Health University Institute, Montreal, QC, Canada.
⁴ School of Medicine, McGill University, Montreal, QC, Canada.
⁵ Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada.
⁶ School of Psychoeducation, Université de Montréal, Montreal, QC, Canada.
⁷ Centre de Recherche du Centre Hospitalier Universitaire (CHU) de Québec, School of Psychology, Laval University, Québec, QC, Canada.
⁸ Centre Hospitalier Universitaire (CHU) Ste-Justine Research Centre, Université de Montréal, Montreal, QC, Canada.
⁹ Department of Psychology, Université du Québec à Montréal (UQAM), Montreal, QC, Canada.
¹⁰ Department of Obstetrics and Gynecology, Centre de Recherche du CHU de Sherbrooke, University of Sherbrooke, Sherbrooke, QC, Canada.
¹¹ Department of Pediatrics, Faculty of Medicine and Health Sciences, McGill University, Montreal, QC, Canada.
¹² Human Genetics and Pharmacology and Therapeutics, Faculty of Medicine and Health Sciences, McGill University, Montreal, QC, Canada.
¹³ Department of Psychiatry and Addiction, Université de Montréal, Montreal, QC, Canada.
¹⁴ Reproductive Psychiatry Program, McGill University Health Centre, Departments of Psychiatry and Obstetrics and Gynecology, Montreal, QC, Canada.
¹⁵ Department of Educational and Counselling Psychology, McGill University, Montreal, QC, Canada.

Abstract

Introduction: This study examined (1) whether measures of paternal anxious and depressive symptoms collected prenatally and during a follow-up assessment when the child was in middle childhood, predict child neuroendocrine outcomes, and (2) whether neuroendocrine outcomes are intermediate factors between paternal mental health and child cognitive/behavioral outcomes. Middle childhood coincides with increased autonomy as the child transitions into grade school, and with adrenarche, as the maturing adrenal gland increases secretion of dehydroepiandrosterone (DHEA) and its sulfated metabolite (DHEA-S), hormones that are implicated in corticolimbic development which regulate emotions and cognition.

Methods: Participants were recruited from a subsample of a large prospective birth cohort study (3D study). We conducted a follow-up study when children were 6-8 years old (N = 61 families, 36 boys, 25 girls). Parental symptoms of anxiety, stress and depression were assessed via validated self-report questionnaires: prenatally using an in-house anxiety questionnaire, the Perceived Stress Scale (PSS) and the Center for Epidemiologic Studies Depression (CES-D), and at the follow up, using the Beck Anxiety and Beck Depression Inventories. Children provided salivary hormone samples, and their pituitary gland volume was measured from structural Magnetic Resonance Imaging (MRI) scans. Child behaviors were measured using the Strengths and Difficulties Questionnaire and cognitive outcomes using the WISC-V. Multiple regression analyses were used to test whether paternal mental health symptoms assessed prenatally and during childhood are associated with child neuroendocrine outcomes, adjusting for maternal mental health and child sex. Indirect-effect models assessed whether neuroendocrine factors are important intermediates that link paternal mental health and cognitive/behavioral outcomes.

Results: (1) Fathers' prenatal anxiety symptoms predicted lower DHEA levels in the children, but not pituitary volume. (2) Higher prenatal paternal anxiety symptoms predicted higher child internalizing symptoms via an indirect pathway of lower child DHEA. No associations were detected between paternal anxiety symptoms measured in childhood, and neuroendocrine outcomes. No child sex differences were detected on any measure.

Conclusion: These results highlight the often-overlooked role of paternal factors during pregnancy on child development, suggesting that paternal prenatal anxiety symptoms are associated with child neuroendocrine function and in turn internalizing symptoms that manifest at least up to middle childhood.

Keywords: DHEA; MRI; child development; internalizing; middle childhood; neuroendocrine; paternal mental health; pituitary.

Grants and funding

Funding for this project was provided by the Research Institute of the McGill University Health Centre (RI-MUHC) and Merck, Sharp and Dohme Corp (T-VN), Canadian Institute for Health Research (T-VN, MY5-155371), Fonds de la Recherche en Santé du Quebec (T-VN, 36776), Montreal General Hospital and MUHC Foundations (T-VN), a Graduate Excellence Fellowship in Mental Health Research (McGill University, Department of Psychiatry) (CC) and a Ferring Fellowship in Reproductive Health (SLJ). The 3D and 3D-transition studies were both supported by the Canadian Institutes of Health Research (CRI 88413 and PJT-148551, respectively). JRS is supported by the Fonds Monique Gaumond pour la Recherche en Maladies Affectives. Open-Access fees were subsidized using research stipends provided by FRQS-Chercheur Boursier Jr. 1 (TCM, 309805). The funding agencies were not involved in the study design, collection, analysis, interpretation of data, the writing of this article or the decision to submit it for publication.