Associations between biological markers of prenatal stress and infant negative emotionality are specific to sex

Braithwaite, Elizabeth; Murphy, Susannah E.; Ramchandani, Paul; Hill, Jonathan

doi:10.1016/j.psyneuen.2017.09.004

Cited by 44 publications

(44 citation statements)

References 81 publications

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“…Braithwaite et al ( N = 216) found a sex interaction such that 5-week-old girls exposed to maternal cortisol exhibited elevated negative emotionality, whereas cortisol-exposed boys exhibited attenuated negative emotionality [44•]. They then replicated this interaction effect in an independent sample ( N = 88) of 2-month-old infants [50]. However, findings from the Queensland Flood Study ( N = 121) showed an interaction with a contrasting pattern: disaster-related PNMS was associated with increased irritability in boys and was unrelated to irritability in girls [47].…”

Section: Resultsmentioning

confidence: 99%

Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

Sutherland

Brunwasser

2018

Curr Psychiatry Rep

132

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Most articles (k = 35) found evidence of either sex-specific associations (significant in one sex but not the other) or significant PNMSstress interactions for at least one child health outcome. Evidence for sex-dependent effects was strongest in the group of studies evaluating child neural/nervous system development and temperament as outcomes. There is sufficient evidence of sex-dependent associations to recommend that researchers always consider the potential role of child sex in PNMS programming studies and report descriptive statistics for study outcomes stratified by child biological sex.

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Section: Resultsmentioning

confidence: 99%

Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

Sutherland

Brunwasser

2018

Curr Psychiatry Rep

132

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“…Regarding the literature just summarized, we would be remiss if we did not mention that some studies detect sex differences in the effects of prenatal stress on behavioral and physiological dysregulation (e.g., Braithwaite, Murphy, Ramchandani, & Hill, ). While not discussed in depth in this paper, it is likely that offspring sex plays a role in the mechanistic processes of prenatal programming (see Bale & Epperson, for review).…”

Section: Prenatal Stress and Behavioral–physiological Dysregulationmentioning

confidence: 99%

mentioning

confidence: 99%

Prenatal stress enhances postnatal plasticity: The role of microbiota

Hartman

Sayler

Belsky

2018

Developmental Psychobiology

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Separate fields of inquiry indicate (a) that prenatal stress is associated with heightened behavioral and physiological reactivity and (b) that these postnatal phenotypes are themselves associated with increased susceptibility to both positive and negative environmental influences. Collectively, this work supports Pluess and Belsky's (Psychopathology, 2011, 23, 29) claim that prenatal stress fosters, promotes or “programs” postnatal developmental plasticity. Herein, we review animal and human evidence consistent with this hypothesis before advancing the novel idea that infant intestinal microbiota may be one candidate mechanism for instantiating developmental plasticity as a result of prenatal stress. We then review research indicating that prenatal stress predicts differences in infant intestinal microbiota; that infant intestinal microbiota is associated with behavioral and physiological reactivity phenotypes; and, thus, that prenatal stress may influence infant intestinal microbiota in a way that results in heightened physiological and behavioral reactivity and, thereby, postnatal developmental plasticity. Finally, we offer ideas for testing this claim and consider implications for intervention and use of probiotics during early infancy.

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“…The effects of prenatal stress on female offspring depression-like behaviour are eliminated by adrenalectomy (2), consistent with risks mediated by glucocorticoid mechanisms that are specific to females. In the human literature, maternal prenatal cortisol, the main glucocorticoid hormone, has been associated with the following outcomes in females, but not males: reduced fetal growth, an established risk factor for later depression (4); increased infant negative emotionality (5,6); fearful infant temperament (7); affective problems in childhood (8); pre-adolescent anxiety (7), depression and a flattened diurnal cortisol profile in adolescence (9). In combination, these results present convincing evidence that exposure to prenatal cortisol increases risk of later affective symptoms in females.…”

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confidence: 99%

“…Animal models show that in utero exposure to elevated maternal glucocorticoids is associated with increased glucocorticoid receptor expression in the amygdala (12), structural changes in sub regions of amygdaloid nuclei (13) and associated depression-like behaviours in adult offspring (12). Human studies have demonstrated a female-specific association between prenatal stress and negative emotionality (5,6) and fearful temperament (7), which have been linked with amygdala activation. There is also direct evidence that elevated maternal cortisol in early, but not late, pregnancy is associated with a larger right amygdala volume in girls, but not boys (8).…”

mentioning

confidence: 99%

Sex-specific associations between maternal prenatal cortisol and child callous-unemotional traits: Findings from the Wirral Child Health and Development Study

Wright¹,

Pickles²,

Braithwaite³

et al. 2018

Preprint

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Background: Maternal prenatal stress may impact on fetal development in a sex-dependent way.Evidence from the human and animal literature supports a theory of glucocorticoid-mediated risk in females, which results in elevated affective symptoms via increased amygdala connectivity and activity. We sought to investigate whether this mechanism may be protective against psychopathology associated with reduced amygdala activity, specifically callous-unemotional (CU) traits.Methods: Participants (n=225) were members of a stratified subsample of an epidemiological cohort (n=1233). Maternal diurnal cortisol was measured using the log of the area under the curve (LogAUC) from saliva samples collected over two days at 32 weeks gestation (on waking, 30-min post-waking and during the evening). Mothers reported on child CU traits and internalizing symptoms at 2.5, 3.5 and 5 years of age.Results: Higher maternal prenatal cortisol was significantly associated with lower CU traits in girls.This effect remained when controlling for confounders and internalizing symptoms. The effect in boys was consistently different from girls (interaction term p<0.001), but never different from zero, indicating no association. There was a significant interaction term to predict internalizing symptoms, however the effect became non-significant when confounders and CU traits were included in the model. Conclusions:The findings extend existing understanding of the adaptive model of prenatal programming in females, where exposure to prenatal stress increases risk for affective disorders via glucocorticoid mechanisms and altered amygdala functioning. Our findings suggest that exposure to elevated prenatal cortisol in females may confer risk or be a protective mechanism depending on the outcome.

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Associations between biological markers of prenatal stress and infant negative emotionality are specific to sex

Cited by 44 publications

References 81 publications

Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

Prenatal stress enhances postnatal plasticity: The role of microbiota

Sex-specific associations between maternal prenatal cortisol and child callous-unemotional traits: Findings from the Wirral Child Health and Development Study

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