Prenatal famine exposure has sex-specific effects on brain size

Rooij, Susanne R. de; Caan, Matthan W.A.; Swaab, Dick F.; Nederveen, Aart J.; Majoie, Charles B; Schwab, Matthias; Painter, Rebecca C.; Roseboom, Tessa J.

doi:10.1093/brain/aww132

Cited by 58 publications

(55 citation statements)

References 26 publications

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“…Our results are also in line with prior studies in humans that have observed sex differences in the effects of prenatal exposures on brain development (de Rooij et al, ; Treit et al, ). Evans and Myatt () showed that male fetuses of obese mothers have higher levels of reactive oxidative species compared to female fetuses (Evans & Myatt, ).…”

Section: Discussionsupporting

confidence: 93%

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

Luo

Chow²,

Herting

et al. 2020

Brain and Behavior

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Introduction Animal studies have shown that male but not female offspring exposed to maternal obesity have abnormal hippocampal development. Similar sex differences were observed in animal models of developmental programming by prenatal stress or maternal diabetes. We aimed to translate this work into humans by examining sex‐specific effects of exposure to maternal obesity on hippocampal volume in children. Methods Eighty‐eight children (37 boys and 51 girls) aged 7–11 years completed the study. Maternal prepregnancy body mass index (BMI) was obtained from electronic medical records. A high‐resolution anatomical scan was performed using a 3‐Tesla magnetic resonance imaging (MRI) scanner. Total hippocampal volume and hippocampal subfield volumes were analyzed using FreeSurfer 6.0. Linear regression was used to investigate sex differences in relationships between maternal prepregnancy BMI and child hippocampal volume. Results Maternal prepregnancy BMI ranged from 19.0 to 50.4 kg/m2. We observed a significant interaction between maternal prepregnancy BMI and sex on total hippocampal volume (p < .001) such that boys (r = −.39, p = .018) but not girls (r = .11, p = .45) had a significant negative relationship between maternal prepregnancy BMI and total hippocampal volume. This relationship in boys remained significant after adjusting for child and maternal covariates (β = −126.98, p = .012). The sex interactions with prepregnancy BMI were consistently observed in hippocampal subfields CA1 (p = .008), CA2/3 (p = .016), CA4 (p = .002), dentate gyrus (p < .001), and subiculum (p < .001). Conclusions Our results support findings in animal models and suggest that boys may be more vulnerable to the adverse effects of exposure to maternal obesity on hippocampal development than girls.

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Section: Discussionsupporting

confidence: 93%

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

Luo

Chow²,

Herting

et al. 2020

Brain and Behavior

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“…The translational power of these studies is shown by a parallel MRI study in the Dutch famine birth cohort, in which decreased total brain volume in late adulthood was already shown in those who had been undernourished prenatally (de Rooij et al, 2016). Further research in the Dutch famine birth cohort will investigate whether exposure to fetal undernutrition during early gestation has an effect on individual brain aging in late-life.…”

Section: Discussionmentioning

confidence: 99%

Premature Brain Aging in Baboons Resulting from Moderate Fetal Undernutrition

Franke

Clarke

Dahnke

et al. 2017

Front. Aging Neurosci.

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Contrary to the known benefits from a moderate dietary reduction during adulthood on life span and health, maternal nutrient reduction during pregnancy is supposed to affect the developing brain, probably resulting in impaired brain structure and function throughout life. Decreased fetal nutrition delivery is widespread in both developing and developed countries, caused by poverty and natural disasters, but also due to maternal dieting, teenage pregnancy, pregnancy in women over 35 years of age, placental insufficiency, or multiples. Compromised development of fetal cerebral structures was already shown in our baboon model of moderate maternal nutrient reduction. The present study was designed to follow-up and evaluate the effects of moderate maternal nutrient reduction on individual brain aging in the baboon during young adulthood (4–7 years; human equivalent 14–24 years), applying a novel, non-invasive neuroimaging aging biomarker. The study reveals premature brain aging of +2.7 years (p < 0.01) in the female baboon exposed to fetal undernutrition. The effects of moderate maternal nutrient reduction on individual brain aging occurred in the absence of fetal growth restriction or marked maternal weight reduction at birth, which stresses the significance of early nutritional conditions in life-long developmental programming. This non-invasive MRI biomarker allows further longitudinal in vivo tracking of individual brain aging trajectories to assess the life-long effects of developmental and environmental influences in programming paradigms, aiding preventive and curative treatments on cerebral atrophy in experimental animal models and humans.

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“…Similarly, cardiovascular mortality (but not morbidity) was increased among women exposed to famine in early gestation (Van Abeelen et al 2012a, Ekamper et al 2014. However, other effects were more pronounced in men: the overall smaller size of the brain after prenatal famine exposure was only found in men and not women (de Rooij et al 2016). Also a number of mental disorders, including addiction and depression, are more common after prenatal exposure to famine in men (Franzek et al 2008, Stein et al 2009.…”

Section: Sex Differencesmentioning

confidence: 97%

“…Prenatal famine exposure has also been associated with affective psychoses and depression, though not all studies replicated this finding (Stein et al 2009, de Rooij et al 2011. Imaging studies of the brains have shown lasting effects of famine exposure on brain size and structure (Hulshoff Pol et al 2000, de Rooij et al 2016. Men who had been exposed to famine in early gestation had smaller intracortical volumes and total brain volumes than unexposed men.…”

Section: Central Nervous Systemmentioning

confidence: 99%

Epidemiological evidence for the developmental origins of health and disease: effects of prenatal undernutrition in humans

Roseboom

2019

Journal of Endocrinology

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This paper describes the findings of studies among men and women who were born around the time of the Dutch famine of 1944–1945, investigating the effects of undernutrition during critical periods of development on later health and disease. The Dutch famine was remarkable in several ways and its unique features have allowed scientists to investigate the long-term consequences of prenatal undernutrition in humans. The effects of undernutrition depended on its timing during gestation, and the organs and tissues undergoing critical periods of development at that time. Early gestation appeared to be the most vulnerable. The effects of famine were widespread and affected the structure and function of many organs and tissues, resulted in altered behaviour and increased risks of chronic degenerative diseases, which in turn led to reduced participation in the labour market and increased mortality. Also, the effects of famine were independent of size at birth, which suggests that programming may occur without altering size at birth. Studies in other settings show that those faced with undernutrition during the critical earliest stages of development have increased rates of chronic generative disease in adult life. This suggests that these findings reflect biologically fundamental processes that describe human plasticity. These findings teach us the fundamental importance of a good start in life. Adequately feeding women before and during pregnancy will allow future generations to reach their full potential and lead healthier and more productive lives, ultimately leading to healthier and more equal future.

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Prenatal famine exposure has sex-specific effects on brain size

Cited by 58 publications

References 26 publications

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

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

Premature Brain Aging in Baboons Resulting from Moderate Fetal Undernutrition

Epidemiological evidence for the developmental origins of health and disease: effects of prenatal undernutrition in humans

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