Associations of Maternal Prenatal Stress and Depressive Symptoms With Childhood Neurobehavioral Outcomes in the ECHO Cohort of the NICHD Fetal Growth Studies: Fetal Growth Velocity as a Potential Mediator

Babineau, Vanessa; Fonge, Yaneve N.; Miller, Emily S.; Grobman, William A.; Ferguson, Pamela L.; Hunt, Kelly J.; Vena, John E.; Newman, Roger B.; Guille, Constance; Tita, Alan T.N.; Chandler‐Laney, Paula; Lee, Seonjoo; Feng, Tianshu; Scorza, Pamela; Takács, Lajos; Wapner, Ronald J.; Palomares, Kristy; Skupski, Daniel; Nageotte, Michael P.; Sciscione, Anthony; Gilman, Stephen E.; Monk, Catherine

doi:10.1016/j.jaac.2022.03.021

Cited by 16 publications

(15 citation statements)

References 55 publications

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Section: Discussionmentioning

confidence: 99%

“…Additional environmental factors should also be considered, such as infections during pregnancy, which are common in individuals with PIDs, as well as prenatal maternal stress. 31 Interestingly, the hypothesized causal role of infections during pregnancy on offspring psychiatric outcomes has been questioned by a growing number of observational studies, [32][33][34][35] suggesting that familial confounding is a more plausible explanation. Mothers are generally more likely than fathers to spend time with their offspring after birth, particularly after a separation or divorce, so disruption of the early life environment (eg, impaired parenting due to recurrent health issues, particularly in mothers who also struggle with their own mental health) could also be a contributing environmental factor affecting the reported associations.…”

Section: Discussionmentioning

confidence: 99%

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Association of Primary Immunodeficiencies in Parents With Psychiatric Disorders and Suicidal Behavior in Their Offspring

et al. 2023

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ImportanceMaternal immune activation (MIA) leading to altered neurodevelopment in utero is a hypothesized risk factor for psychiatric outcomes in offspring. Primary antibody immunodeficiencies (PIDs) constitute a unique natural experiment to test the MIA hypothesis of mental disorders.ObjectiveTo assess the association of maternal and paternal PIDs with psychiatric disorders and suicidal behavior in offspring.Design, Setting, and ParticipantsCohort study of 4 294 169 offspring of parents with and without PIDs living in Sweden at any time between 1973 and 2013. Data were extracted from Swedish nationwide health and administrative registers and were analyzed from May 5 to September 30, 2022. All individuals with diagnoses of PIDs identified between 1973 and 2013 from the National Patient Register were included. Offspring were included if born before 2003. Parent-offspring pairs in which both parents had a history of PIDs were excluded.ExposuresLifetime records of parental PIDs according to the International Classification of Diseases, Eighth Revision (ICD-8); International Classification of Diseases, Ninth Revision (ICD-9); and International Statistical Classification of Diseases and Related Health Problems, Tenth Revision (ICD-10) diagnostic codes.Main Outcomes and MeasuresLifetime records of 10 psychiatric disorders and suicidal behavior identified using ICD-8, ICD-9, and ICD-10 diagnostic codes, including suicide attempts and death by suicide, among offspring. Covariates included sex, birth year, parental psychopathology, suicide attempts, and autoimmune diseases. Additional analyses excluded offspring with their own PIDs and autoimmune diseases. Poisson regression models were fitted separately for mothers and fathers to estimate incidence rate ratios (IRRs) and 95% CIs for the risk of psychiatric and suicidal behavior outcomes in the offspring of PID-exposed vs PID-unexposed mothers or fathers.ResultsThe cohort included 4 294 169 offspring (2 207 651 males [51.4%]) and 3 954 937 parents (1 987 972 females [50.3%]). A total of 7270 offspring (0.17%) had parents with PIDs, and 4 286 899 offspring had parents without PIDs. In fully adjusted models, offspring of mothers with PIDs had an increased risk of any psychiatric disorder, while no such risks were observed in offspring of fathers with PIDs (IRR, 1.17; 95% CI, 1.10-1.25 vs IRR, 1.03; 95% CI, 0.94-1.14; P &lt; .001). Likewise, an increased risk of suicidal behavior was observed among offspring of mothers with PIDs but not offspring of fathers with PIDs (IRR, 1.20; 95% CI, 1.06-1.36 vs IRR, 1.10; 95% CI, 0.91-1.34; P = .01). For the offspring of mothers with PIDs, the risk of developing any psychiatric disorder was significantly higher for those with mothers with 6 of 10 individual disorders, with IRRs ranging from 1.15 (95% CI, 1.04-1.26) for anxiety and stress-related disorders and 1.15 (95% CI, 1.03-1.30) for substance use disorders to 1.71 (95% CI, 1.37-2.14) for bipolar disorders. Offspring of mothers with both PIDs and autoimmune diseases had the highest risk for any psychiatric disorder (IRR, 1.24; 95% CI, 1.11-1.38) and suicidal behavior (IRR, 1.44; 95% CI, 1.17-1.78).Conclusions and RelevanceFindings of this cohort study suggest that maternal, but not paternal, PIDs were associated with a statistically significant increased risk of psychiatric disorders and suicidal behavior in the offspring, particularly when PIDs co-occur with autoimmune diseases. These findings align with the MIA hypothesis of mental disorders, but the precise mechanisms remain to be elucidated.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Association of Primary Immunodeficiencies in Parents With Psychiatric Disorders and Suicidal Behavior in Their Offspring

et al. 2023

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“…For example, infants with an initially difficult temperament may be more modestly dysregulated, or have an attuned and sensitive caregiver with whom the interaction can lead to an attenuation of dysregulation over time, whereas others may be too dysregulated or experience less downregulation from the caregiving match (Washington et al, 1986). Screening and identification of dysregulation assessed at this malleable period of development may be Maternal prenatal mood symptoms have consistently been associated with altered child neurodevelopment and increased risk for psychopathology (Babineau et al, 2022;Monk et al, 2019), and uncertainty remains regarding the biological mechanisms that lead to individual differences in children's response to prenatal distress (O'Donnell et al, 2017). Many potential pathways have been identified within and outside of the placenta, including the hypothalamicpituitary-adrenal axis, immune system, and microbiome (Monk et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Additional limitations of this study included our use of maternal report measures for dysregulation and perinatal mood, which could have led to shared method variance (Atella et al., 2003). Nevertheless, the questionnaires allowed for a longer observation period, multiple time points with repeated measures, and a reduction of bias given the recent occurring behaviors reported (Gartstein & Rothbart, 2003).…”

Section: Discussionmentioning

confidence: 99%

Maternal prenatal depression is associated with dysregulation over the first five years of life moderated by child polygenic risk for comorbid psychiatric problems

Babineau

Jolicoeur-Martineau

Székely

et al. 2023

Developmental Psychobiology

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Dysregulation is a combination of emotion, behavior, and attention problems associated with lifelong psychiatric comorbidity. There is evidence for the stability of dysregulation from childhood to adulthood, which would be more fully characterized by determining the likely stability from infancy to childhood. Early origins of dysregulation can further be validated and contextualized in association with environmental and biological factors, such as prenatal stress and polygenic risk scores (PRS) for overlapping child psychiatric problems. We aimed to determine trajectories of dysregulation from 3 months to 5 years (N = 582) in association with maternal prenatal depression moderated by multiple child PRS (N = 232 pairs with available PRS data) in a prenatal cohort. Mothers reported depression symptoms at 24-26 weeks' gestation and child dysregulation at 3, 6, 18, 36, 48, and 60 months. The PRS were for major depressive disorder, attention deficit hyperactivity disorder, cross disorder, and childhood psychiatric problems. Covariates were biological sex, maternal education, and postnatal depression. Analyses included latent classes and regression. Two dysregulation trajectories emerged: persistently low dysregulation (94%), and increasingly high dysregulation (6%). Stable dysregulation emerged at 18 months. High dysregulation was associated with maternal prenatal depression, moderated by PRS for child comorbid psychiatric problems. Males were at greater risk of high dysregulation.

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“…This study by Wu et al incorporates cutting-edge neuroscience into DOHaD neurodevelopmental research by directly assessing fetal brain development and showing that it mediates the association between maternal prenatal stress and child cognition and is relevant to other domains of functioning nearly 2 years later. A key outcome associated with maternal stress, cognitive functioning at 18 months, is observer based, consistent with other recent findings that strengthen the rigor of DOHaD research using maternal prenatal mood as an exposure variable. Finally, with the positive associations between prenatal and postnatal distress, Wu et al control for postnatal parenting stress in their models, elegantly isolating prenatal stress as the active agent in child outcomes.…”

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confidence: 99%

Neuroscience Advances and the Developmental Origins of Health and Disease Research

Monk

Fernández

2022

JAMA Netw Open

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Decades ago, when David Barker 1 introduced the developmental origins of health and disease (DOHaD) conceptual model and later demonstrated that the prenatal period is relevant for future well-being, he could not have envisioned that fetal brain imaging would substantiate his claims or that maternal stress would be a potent prenatal exposure affecting health outcomes. Barker's focus was inadequate maternal nutrition, to which he hypothesized fetuses adapt, resulting in programmed changes in physiology and metabolism that contribute to disease risk in adulthood, including coronary heart disease and the related disorders stroke, diabetes, and hypertension. 1 Briefly, lower birth weight, which was viewed as a proxy for nonoptimal maternal nutrition, was found to be associated with increased risk for coronary heart disease years later. 1 When the DOHaD approach was applied to national health records from the World War II-era Dutch Famine and neurodevelopment was added as a disease outcome-showing, for example, far higher rates of schizophrenia in men who had been in utero during the famine rather than the months before or after it-maternal stress was not considered as an additional exposure factor. 2 In the 21st century, DOHaD researchers pivoted, ultimately establishing stress, depression, and anxiety as maternal experiences affecting child prenatal and future development, although to be sure, much of this research was based on maternal report of child outcomes such that the mother was both the source of the independent variable (mood state in pregnancy, often associated with postpartum mood state) and dependent variable (child temperament and emotional or behavioral symptoms) years

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Associations of Maternal Prenatal Stress and Depressive Symptoms With Childhood Neurobehavioral Outcomes in the ECHO Cohort of the NICHD Fetal Growth Studies: Fetal Growth Velocity as a Potential Mediator

Cited by 16 publications

References 55 publications

Association of Primary Immunodeficiencies in Parents With Psychiatric Disorders and Suicidal Behavior in Their Offspring

Association of Primary Immunodeficiencies in Parents With Psychiatric Disorders and Suicidal Behavior in Their Offspring

Maternal prenatal depression is associated with dysregulation over the first five years of life moderated by child polygenic risk for comorbid psychiatric problems

Neuroscience Advances and the Developmental Origins of Health and Disease Research

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