Exploring the relationship between maternal prenatal stress and brain structure in premature neonates

Lautarescu, Alexandra; Hadaya, Laila; Craig, Michael C.; Makropoulos, Antonis; Batallé, Dafnis; Nosarti, Chiara; Edwards, A. David; Counsell, Serena; Victor, Suresh

doi:10.1371/journal.pone.0250413

Cited by 7 publications

(5 citation statements)

References 71 publications

(22 reference statements)

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“…Structural MRI (s-MRI) log-Jacobian determinant maps were calculated to quantify regional brain volumes (greater log-Jacobian values reflect larger relative structural volumes), using Tensor Based Morphometry, following methods described in our previous work [ 53 , 54 ] and in Supplemental Information .…”

Section: Methodsmentioning

confidence: 99%

Parsing brain-behavior heterogeneity in very preterm born children using integrated similarity networks

et al. 2023

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Very preterm birth (VPT; ≤32 weeks’ gestation) is associated with altered brain development and cognitive and behavioral difficulties across the lifespan. However, heterogeneity in outcomes among individuals born VPT makes it challenging to identify those most vulnerable to neurodevelopmental sequelae. Here, we aimed to stratify VPT children into distinct behavioral subgroups and explore between-subgroup differences in neonatal brain structure and function. 198 VPT children (98 females) previously enrolled in the Evaluation of Preterm Imaging Study (EudraCT 2009-011602-42) underwent Magnetic Resonance Imaging at term-equivalent age and neuropsychological assessments at 4–7 years. Using an integrative clustering approach, we combined neonatal socio-demographic, clinical factors and childhood socio-emotional and executive function outcomes, to identify distinct subgroups of children based on their similarity profiles in a multidimensional space. We characterized resultant subgroups using domain-specific outcomes (temperament, psychopathology, IQ and cognitively stimulating home environment) and explored between-subgroup differences in neonatal brain volumes (voxel-wise Tensor-Based-Morphometry), functional connectivity (voxel-wise degree centrality) and structural connectivity (Tract-Based-Spatial-Statistics). Results showed two- and three-cluster data-driven solutions. The two-cluster solution comprised a ‘resilient’ subgroup (lower psychopathology and higher IQ, executive function and socio-emotional scores) and an ‘at-risk’ subgroup (poorer behavioral and cognitive outcomes). No neuroimaging differences between the resilient and at-risk subgroups were found. The three-cluster solution showed an additional third ‘intermediate’ subgroup, displaying behavioral and cognitive outcomes intermediate between the resilient and at-risk subgroups. The resilient subgroup had the most cognitively stimulating home environment and the at-risk subgroup showed the highest neonatal clinical risk, while the intermediate subgroup showed the lowest clinical, but the highest socio-demographic risk. Compared to the intermediate subgroup, the resilient subgroup displayed larger neonatal insular and orbitofrontal volumes and stronger orbitofrontal functional connectivity, while the at-risk group showed widespread white matter microstructural alterations. These findings suggest that risk stratification following VPT birth is feasible and could be used translationally to guide personalized interventions aimed at promoting children’s resilience.

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Section: Methodsmentioning

confidence: 99%

Parsing brain-behavior heterogeneity in very preterm born children using integrated similarity networks

et al. 2023

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“…The template was generated from a subset of 161 participants using advanced normalization tools software as described in Lautarescu et al . 62 . Data were spatially smoothed with a 4 mm full-width half-maximum Gaussian kernel.…”

Section: Methodsmentioning

confidence: 99%

Neonatal amygdala resting-state functional connectivity and socio-emotional development in very preterm children

Kanel

Vanes

Ball

et al. 2022

Brain Communications

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Very preterm children are more likely to exhibit difficulties in socio-emotional processing than their term-born peers. Emerging socio-emotional problems may be partly due to alterations in limbic system development associated with infants’ early transition to extrauterine life. The amygdala is a key structure in this system and plays a critical role in various aspects of socio-emotional development, including emotion regulation. The current study tested the hypothesis that amygdala resting-state functional connectivity at term-equivalent age is associated with socio-emotional outcomes in childhood. Participants were 129 very preterm infants who underwent resting-state functional magnetic resonance imaging (MRI) at term and received a neurodevelopmental assessment at 4-7 years (median = 4.64). Using the left and right amygdala as seed regions, we investigated associations between whole-brain seed-based functional connectivity and three socio-emotional outcome factors which were derived using exploratory factor analysis (Emotion Moderation, Social Function and Empathy), controlling for sex, neonatal sickness, post-menstrual age at scan, and social risk. Childhood Emotion Moderation scores were significantly associated with neonatal resting-state functional connectivity of the right amygdala with right parahippocampal gyrus and right middle occipital gyrus, as well as with functional connectivity of the left amygdala with the right thalamus. No significant associations were found between amygdala resting-state functional connectivity and either Social Function or Empathy factors. The current findings suggest that amygdalar functional connectivity assessed at term is associated with later socio-emotional outcomes in very preterm children.

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“…The amygdalae reach anatomical “maturity” early in development (Bachevalier et al 1986; Berger et al 1990; Gabard-Durnam et al 2018; Humphrey 1968; Kordower, Piecinski, and Rakic 1992; Machado and Bachevalier 2003). Individual differences in early amygdala volume have been linked to maternal pre- and postnatal psychological distress (Supplementary Table 1), although the results have been inconsistent, ranging from positive (Donnici et al 2021; Groenewold et al 2022; Wen et al 2017) to negative (Acosta, Tuulari, et al 2020; Lehtola et al 2020; Wang et al 2018; Wu et al 2021) with some studies reporting no associations (Hidalgo et al 2022; Lautarescu et al 2021; El Marroun et al 2016; Moog et al 2021) between maternal pre- or postnatal distress and offspring amygdala volume.…”

Section: Introductionmentioning

confidence: 99%

Parental childhood maltreatment associates with offspring left amygdala volume at early infancy

Tuulari

Pulli

Kataja

et al. 2023

Preprint

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Background: Childhood maltreatment exposure (CME) and related trauma could be considered some of psychiatry's greatest public health challenges. CME and early adversity have been associated with increased amygdala volume in exposed individuals. Emerging evidence implies that CME could also affect prenatal development of the offspring. Methods: As part of the FinnBrain Birth Cohort Study, we measured bilateral amygdala volumes from MR images in 76 healthy infants at 2 to 5 weeks of gestation corrected age and obtained the Trauma and Distress Scale (TADS) questionnaire from both parents. The associations between neonatal amygdala volumes and TADS scores were examined in stepwise regression models. Results: We found that maternal CME associated positively with infant left amygdala volume (p = .045) while the positive association for the paternal trauma score was only marginally significant (p = .099). Similar associations were not observed for the right amygdala. In the exploratory analyses, we used age ranges (0 to 6, 7 to 12, and 13 to 18 years) as estimate of the timing of the CME and included all three time points from both parents using left amygdala volume into the stepwise regression models. We found that maternal TADS scores from 13 to 18 years of age associated positively with infant left amygdala volumes (p = .008). Correspondingly, paternal TADS scores from 0 to 6 years of age associated positively with the infant left amygdala volumes (p = .014). Conclusions: Our link the infant offspring amygdala volume with parental CME with some agreement with prior findings, and they also imply links paternal CME to infant amygdala volumes. Amygdala is one of the key brain structures associated with both early life exposures and later psychiatric health, which makes it crucially important to elucidate both the underlying mechanisms and the later relevance of these associations in future studies.

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Exploring the relationship between maternal prenatal stress and brain structure in premature neonates

Cited by 7 publications

References 71 publications

Parsing brain-behavior heterogeneity in very preterm born children using integrated similarity networks

Parsing brain-behavior heterogeneity in very preterm born children using integrated similarity networks

Neonatal amygdala resting-state functional connectivity and socio-emotional development in very preterm children

Parental childhood maltreatment associates with offspring left amygdala volume at early infancy

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