Sex differences in the association between prenatal exposure to maternal obesity and hippocampal volume in children

Luo, Shan; Chow, Ting; Herting, Megan M.; Xiang, Anny H.; Page, Kathleen A.

doi:10.1002/brb3.1522

Cited by 24 publications

(37 citation statements)

References 83 publications

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“…shown that the hippocampus of boys is particularly sensitive to in utero metabolic insults (Alves et al, 2020;Zhu et al, 2018). Importantly, while the interaction with GDM exposure and sex on child hippocampal volume and right CA1 subfield volume was independent of age and intracranial volume, sex stratified results in boys were no longer significant after adjusting for age and intracranial volume.…”

Section: Discussionmentioning

confidence: 96%

“…Additionally, the hippocampus exhibits a high metabolic demand (Jabès, Lavenex, Amaral, & Lavenex, 2011;Kirschen, Kéry, & Ge, 2018), which makes it susceptible to perturbations in vital nutrients, such as glucose, iron and oxygen. Moreover, prior neuroimaging studies have shown that prenatal exposure to alcohol or maternal obesity preferentially impacts hippocampal volume of offspring, most notably in a sex-specific manner (Alves et al, 2020;Treit et al, 2017). Collectively, prior studies provide evidence that the hippocampus may be particularly sensitive to in utero insults.…”

Section: Introductionmentioning

confidence: 91%

“…Further rigorous quality check and segmentation details for the hippocampal subfield analysis can be found in the methods section of Alves et al (2020).…”

Section: Quality Assurance Proceduresmentioning

confidence: 99%

“…Therefore, for the first time in humans, we investigated if children exposed to GDM in utero differ in hippocampal shape and individual hippocampal subfields when compared to unexposed children. Additionally, because of known sex differences in the effects of maternal metabolic disorders during pregnancy on the developing hippocampus (Alves et al, 2020;Zhu et al, 2018), we assessed whether there are sex differences in associations between GDM-exposure and hippocampal morphology in children.…”

Section: Introductionmentioning

confidence: 99%

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Selective morphological and volumetric alterations in the hippocampus of children exposed in utero to gestational diabetes mellitus

Lynch

Chow

Clark

et al. 2021

Human Brain Mapping

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Prior epidemiological studies have found that in utero exposure to gestational diabetes mellitus (GDM) is associated with increased risk for neurodevelopmental disorders. However, brain alterations associated with GDM are not known. The hippocampus is pivotal for cognition and emotional regulation. Therefore, we assessed relationships between in utero exposure to GDM and hippocampal morphology and subfield structure during childhood. One hundred seventeen children aged 7-11 years (57% girls, 57% exposed to GDM), born at Kaiser Permanente Southern California, participated in the BrainChild Study. Maternal GDM status was determined from electronic medical records. Children underwent brain magnetic resonance imaging. Freesurfer 6.0 was used to measure hippocampal and individual hippocampal subfield gray matter volume (mm 3 ). Morphological analyses on the hippocampal surface were carried out using shape analysis. GDMexposed children exhibited reduced radial thickness in a small, spatially-restricted portion of the left inferior body of the hippocampus that corresponds to the CA1 subfield. There was a significant interaction between GDM-exposure and sex on the right hippocampal CA1 subfield. GDM-exposed boys had reduced right CA1 volume compared to unexposed boys, but this association was no longer significant after controlling for age.No significant group differences were observed in girls. Our results suggest that GDMexposure impacts shape of the left hippocampal CA1 subfield in both boys and girls and may reduce volume of right hippocampal CA1 only in boys. These in-depth findings illuminate the unique properties of the hippocampus impacted by prenatal GDM-exposure and could have important implications for hippocampal-related functions.

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 91%

“…Further rigorous quality check and segmentation details for the hippocampal subfield analysis can be found in the methods section of Alves et al (2020).…”

Section: Quality Assurance Proceduresmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Selective morphological and volumetric alterations in the hippocampus of children exposed in utero to gestational diabetes mellitus

Lynch

Chow

Clark

et al. 2021

Human Brain Mapping

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show abstract

“…Studies in rodents and humans link maternal obesity to neurological changes in offspring. A recent human study reported a negative association between maternal BMI and hippocampal volume in male children at 7–11 years of age [ 76 ]. Furthermore, consumption of diets high in polyunsaturated omega-6 fatty acids during pregnancy impairs healthy brain structure and development in the foetus.…”

Section: Underlying Mechanisms By Which Maternal Obesity Programs mentioning

confidence: 99%

Mechanisms Underlying the Cognitive and Behavioural Effects of Maternal Obesity

2021

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The widespread consumption of ‘western’-style diets along with sedentary lifestyles has led to a global epidemic of obesity. Epidemiological, clinical and preclinical evidence suggests that maternal obesity, overnutrition and unhealthy dietary patterns programs have lasting adverse effects on the physical and mental health of offspring. We review currently available preclinical and clinical evidence and summarise possible underlying neurobiological mechanisms by which maternal overnutrition may perturb offspring cognitive function, affective state and psychosocial behaviour, with a focus on (1) neuroinflammation; (2) disrupted neuronal circuities and connectivity; and (3) dysregulated brain hormones. We briefly summarise research implicating the gut microbiota in maternal obesity-induced changes to offspring behaviour. In animal models, maternal obesogenic diet consumption disrupts CNS homeostasis in offspring, which is critical for healthy neurodevelopment, by altering hypothalamic and hippocampal development and recruitment of glial cells, which subsequently dysregulates dopaminergic and serotonergic systems. The adverse effects of maternal obesogenic diets are also conferred through changes to hormones including leptin, insulin and oxytocin which interact with these brain regions and neuronal circuits. Furthermore, accumulating evidence suggests that the gut microbiome may directly and indirectly contribute to these maternal diet effects in both human and animal studies. As the specific pathways shaping abnormal behaviour in offspring in the context of maternal obesogenic diet exposure remain unknown, further investigations are needed to address this knowledge gap. Use of animal models permits investigation of changes in neuroinflammation, neurotransmitter activity and hormones across global brain network and sex differences, which could be directly and indirectly modulated by the gut microbiome.

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A systematic review of MRI studies on the effects of maternal obesity on offspring brain structure and function

Parsaei,

Hashemi,

Moghaddam

et al. 2024

J of Neuroscience Research

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Maternal obesity before or during pregnancy has been associated previously in offspring with a wide range of poor neurodevelopmental outcomes and mental health problems. The effects of maternal obesity on offspring brain structure and function that may be responsible for these poor outcomes are not well understood. We, therefore, undertook a systematic review of magnetic resonance imaging (MRI) studies that have assessed the associations of maternal obesity with brain measures in offspring. A systematic search was conducted in PubMed, Web of Science, Scopus, and PsycINFO on August 20, 2023. Of 15 eligible studies, seven employed functional MRI (fMRI), five diffusion tensor imaging (DTI), and four anatomical MRI (one used both DTI and anatomical MRI) in the offspring. The ages of offspring varied widely: one was a study of fetuses in utero, five of neonates, one of infants, five of school‐aged children, two of both neonates and infants, and one of both children and adults. Collectively, 12 studies reported significant associations of maternal obesity with structural or functional alterations of the offspring's brain, most frequently in the prefrontal cortex and limbic system. In conclusion, maternal obesity appears to have a profound influence on offspring brain development, particularly within the prefrontal and limbic networks that regulate emotion and behavior. Further studies are needed to identify how changes in brain structure and function mediate the effects of maternal obesity on long‐term emotional and behavioral outcomes, as well as the molecular pathways through which maternal obesity alters offspring brain development.

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Sex differences in the association between prenatal exposure to maternal obesity and hippocampal volume in children

Cited by 24 publications

References 83 publications

Selective morphological and volumetric alterations in the hippocampus of children exposed in utero to gestational diabetes mellitus

Selective morphological and volumetric alterations in the hippocampus of children exposed in utero to gestational diabetes mellitus

Mechanisms Underlying the Cognitive and Behavioural Effects of Maternal Obesity

A systematic review of MRI studies on the effects of maternal obesity on offspring brain structure and function

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