Buss C, Davis EP, Muftuler T, et al. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children

Department of Psychiatry and Human Behavior, University of California, Irvine, Orange, CA 92868, United States.
Psychoneuroendocrinology (Impact Factor: 4.94). 09/2009; 35(1):141-53. DOI: 10.1016/j.psyneuen.2009.07.010
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Because the brain undergoes dramatic changes during fetal development it is vulnerable to environmental insults. There is evidence that maternal stress and anxiety during pregnancy influences birth outcome but there are no studies that have evaluated the influence of stress during human pregnancy on brain morphology. In the current prospective longitudinal study we included 35 women for whom serial data on pregnancy anxiety was available at 19 (+/-0.83), 25 (+/-0.9) and 31 (+/-0.9) weeks gestation. When the offspring from the target pregnancy were between 6 and 9 years of age, their neurodevelopmental stage was assessed by a structural MRI scan. With the application of voxel-based morphometry, we found regional reductions in gray matter density in association with pregnancy anxiety after controlling for total gray matter volume, age, gestational age at birth, handedness and postpartum perceived stress. Specifically, independent of postnatal stress, pregnancy anxiety at 19 weeks gestation was associated with gray matter volume reductions in the prefrontal cortex, the premotor cortex, the medial temporal lobe, the lateral temporal cortex, the postcentral gyrus as well as the cerebellum extending to the middle occipital gyrus and the fusiform gyrus. High pregnancy anxiety at 25 and 31 weeks gestation was not significantly associated with local reductions in gray matter volume.This is the first prospective study to show that a specific temporal pattern of pregnancy anxiety is related to specific changes in brain morphology. Altered gray matter volume in brain regions affected by prenatal maternal anxiety may render the developing individual more vulnerable to neurodevelopmental and psychiatric disorders as well as cognitive and intellectual impairment.

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    • "Our results extend recent literature highlighting the importance of temporal-specificity of effects of prenatal disruptions on integrity of fetal and postnatal development (Mueller and Bale, 2007, 2008), including programming of stress pathways (Bale, 2010). High prenatal anxiety during mid-gestation has been linked to neuroanatomical integrity (e.g., diminished gray matter density) in 6-to 9-year-old children (Buss et al., 2010). Moreover, prenatal disruptions and adverse exposures during early-to mid-pregnancy have been shown to predispose to later development of psychiatric disorders (e.g., Malaspina et al., 2008), although some studies point to mid-to late-prenatal periods (e.g., Kinney et al., 2008b). "
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    ABSTRACT: Research implicates prenatal maternal stress (PNMS) as a risk factor for neurodevelopmental disorders; however few studies report PNMS effects on autism risk in offspring. We examined, prospectively, the degree to which objective and subjective elements of PNMS explained variance in autism-like traits among offspring, and tested moderating effects of sex and PNMS timing in utero. Subjects were 89 (46F/43M) children who were in utero during the 1998 Quebec Ice Storm. Soon after the storm, mothers completed questionnaires on objective exposure and subjective distress, and completed the Autism Spectrum Screening Questionnaire (ASSQ) for their children at age 6½. ASSQ scores were higher among boys than girls. Greater objective and subjective PNMS predicted higher ASSQ independent of potential confounds. An objective-by-subjective interaction suggested that when subjective PNMS was high, objective PNMS had little effect; whereas when subjective PNMS was low, objective PNMS strongly affected ASSQ scores. A timing-by-objective stress interaction suggested objective stress significantly affected ASSQ in first-trimester exposed children, though less so with later exposure. The final regression explained 43% of variance in ASSQ scores; the main effect of sex and the sex-by-PNMS interactions were not significant. Findings may help elucidate neurodevelopmental origins of non-clinical autism-like traits from a dimensional perspective.
    Psychiatry Research 05/2014; 219(2). DOI:10.1016/j.psychres.2014.04.034 · 2.47 Impact Factor
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    • "In particular, compared to controls, animals exposed to prenatal stress exhibited initially reduced, and subsequently increased, amygdala volume (Salm et al. 2004; Kraszpulski et al. 2006). These fi ndings of an altered neurodevelopmental trajectory are supported by human studies, which have also reported an association between increased maternal prenatal cortisol levels and increased amygdala volume in later childhood (Buss et al. 2010; Buss et al. 2012) and reduced volume in prefrontal cortical brain regions, including orbitofrontal cortex (Buss et al. 2010). However, brain regions do not function in isolation – they form networks connected by white matter tracts. "
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    ABSTRACT: Abstract Objectives. Maternal prenatal stress is associated with elevated risk of adverse behavioural outcomes in offspring. This association may involve developmental disruption to limbic-prefrontal white matter circuitry, of which the uncinate fasciculus is the major tract. One potential candidate for modulating brain development is maternal prenatal stress. We provide the first prospective study of prenatal stress and white matter microstructure in children. Methods. A total of 22 healthy children (mean age 7 years) of mothers recruited in pregnancy underwent diffusion tensor magnetic resonance imaging. We examined correlations between prenatal stressful life events and white matter microstructural organisation indices (fractional anisotropy (FA) and perpendicular diffusivity (Dperp)) of the uncinate fasciculus and a "control" tract. Results. Maternal prenatal stressful life events were correlated positively with right uncinate fasciculus FA, and negatively with right uncinate fasciculus Dperp in their child, with a similar trend with left uncinate fasciculus Dperp. Prenatal stress was not associated with control tract properties; sociodemographic/obstetric variables were not associated with FA/Dperp of either tract. Conclusions. Variation in maternal prenatal stress may be associated with differences in the development of white matter within brain networks underlying child social behaviour.
    The World Journal of Biological Psychiatry 05/2014; 15(4):346-52. DOI:10.3109/15622975.2014.903336 · 4.18 Impact Factor
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    • "Although a few prior studies have shown that prenatal distress measures averaged across pregnancy are predictive of gestational length (Lobel, Dunkel Schetter, & Scrimshaw, 1992; Roesch et al., 2004), the majority of studies show that pregnancy anxiety at specific times in gestation or changes over time in pregnancy anxiety are predictive of birth and infant outcomes (e.g., Buitelaar et al., 2003; Buss et al., 2009; Mancuso et al., 2004). There are several potential explanations for why changes in pregnancy anxiety were not predictive of cortisol in the current study. "
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    ABSTRACT: Pregnancy anxiety is a potent predictor of adverse birth and infant outcomes. The goal of the current study was to examine one potential mechanism whereby these effects may occur by testing associations between pregnancy anxiety and maternal salivary cortisol on 4 occasions during pregnancy in a sample of 448 women. Higher mean levels of pregnancy anxiety over the course of pregnancy predicted steeper increases in cortisol trajectories compared to lower pregnancy anxiety. Significant differences between cortisol trajectories emerged between 30 to 31 weeks of gestation. Results remained significant when adjusted for state anxiety and perceived stress. Neither changes in pregnancy anxiety over gestation, nor pregnancy anxiety specific to only a particular time in pregnancy predicted cortisol. These findings provide support for one way in which pregnancy anxiety may influence maternal physiology and contribute to a growing literature on the complex biological pathways linking pregnancy anxiety to birth and infant outcomes.
    Biological psychology 04/2014; 100(1). DOI:10.1016/j.biopsycho.2014.04.003 · 3.40 Impact Factor
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