The link between maternal obesity and offspring neurobehavior: A systematic review of animal experiments

Menting, Malou D.; Beek, C. van de; Mintjens, Stijn; Wever, Kimberley E.; Kőrösi, Anikó; Ozanne, Susan E.; Limpens, Jacqueline; Roseboom, Tessa J.; Hooijmans, Carlijn R.; Painter, Rebecca C.

doi:10.1016/j.neubiorev.2018.12.023

Cited by 33 publications

(21 citation statements)

References 69 publications

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“…1). Rodent models on high fat diet (HFD) or with hyperglycemia have been used in this context supporting a role of the intrauterine environment [20,[60][61][62][63]. Offspring to pregnant dams of these models display altered behaviors such as hyperactivity, reduced sociability and anxious and depressive-like behaviors [20].…”

Section: Brief Overview Of Potential Pathways and Mechanismsmentioning

confidence: 99%

Relationship of prenatal maternal obesity and diabetes to offspring neurodevelopmental and psychiatric disorders: a narrative review

et al. 2020

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Obesity and diabetes is a worldwide public health problem among women of reproductive age. This narrative review highlights recent epidemiological studies regarding associations of maternal obesity and diabetes with neurodevelopmental and psychiatric disorders in offspring, and provides an overview of plausible underlying mechanisms and challenges for future human studies. A comprehensive search strategy selected terms that corresponded to the domains of interest (maternal obesity, different types of diabetes, offspring cognitive functions and neuropsychiatric disorders). The databases searched for articles published between January 2010 and April 2019 were PubMed, Web of Science and CINAHL. Evidence from epidemiological studies strongly suggests that maternal pre-pregnancy obesity is associated with increased risks for autism spectrum disorder, attention-deficit hyperactivity disorder and cognitive dysfunction with modest effect sizes, and that maternal diabetes is associated with the risk of the former two disorders. The influence of maternal obesity on other psychiatric disorders is less well studied, but there are reports of associations with increased risks for offspring depression, anxiety, schizophrenia and eating disorders, at modest effect sizes. It remains unclear whether these associations are due to intrauterine mechanisms or explained by confounding family-based sociodemographic, lifestyle and genetic factors. The plausible underlying mechanisms have been explored primarily in animal models, and are yet to be further investigated in human studies.

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Section: Brief Overview Of Potential Pathways and Mechanismsmentioning

confidence: 99%

Relationship of prenatal maternal obesity and diabetes to offspring neurodevelopmental and psychiatric disorders: a narrative review

et al. 2020

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“…Triacylgycerol is elevated, however, in these males (Tarrade et al, 2013). A systemic review of animal studies further suggests that maternal obesity is associated with offspring neurobehavioral disruptions as evidenced by elevated locomotor activity and anxiogenic behaviors (Menting et al, 2019). Rhesus macaque offspring of mothers with increased baseline adiposity or gestational weight gain display poor adaptability with exaggerated emotional responses and reduced interest in novel stimuli (Walker, VandeVoort, Li, Chaffin, & Capitanio, 2018).…”

Section: Introductionmentioning

confidence: 99%

The placenta‐brain‐axis

Rosenfeld

2020

J of Neuroscience Research

125

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All mammalian species depend on the placenta, a transient organ, for exchange of gases, nutrients, and waste between the mother and conceptus. Besides serving as a conduit for such exchanges, the placenta produces hormones and other factors that influence maternal physiology and fetal development. To meet all of these adaptations, the placenta has evolved to become the most structurally diverse organ within all mammalian taxa. However, commonalities exist as to how placental responses promote survival against in utero threats and can alter the trajectory of fetal development, in particular the brain. Increasing evidence suggests that reactions of the placenta to various in utero stressors may lead to long‐standing health outcomes, otherwise considered developmental origin of health and disease effects. Besides transferring nutrients and gases, the placenta produces neurotransmitters, including serotonin, dopamine, norepinephrine/epinephrine, that may circulate and influence brain development. Neurobehavioral disorders, such as autism spectrum disorders, likely trace their origins back to placental disturbances. This intimate relationship between the placenta and brain has led to coinage of the term, the placenta‐brain‐axis. This axis will be the focus herein, including how conceptus sex might influence it, and technologies employed to parse out the effects of placental‐specific transcript expression changes on later neurobehavioral disorders. Ultimately, the placenta might provide a historical record of in utero threats the fetus confronted and a roadmap to understand how placenta responses to such encounters impacts the placental‐brain‐axis. Improved early diagnostic and preventative approaches may thereby be designed to mitigate such placental disruptions.

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“…Brain areas most frequently implicated by prenatal obesity are important for reward processing, higher order cognitive functioning, and mental health, including the prefrontal cortex (Glendining, Fisher, & Jasoni, 2018; Grissom et al, 2014), nucleus accumbens (Naef et al, 2011; Vucetic et al, 2010), and hippocampus (Niculescu & Lupu, 2009; Tozuka et al, 2010). Many of these neurological findings have been linked to alterations in cognitive (e.g., spatial learning), reward, and social behavior, as well as increased anxious and ADHD‐like traits (Menting et al, 2019; Sullivan, Nousen, & Chamlou, 2014). Taken together, these studies demonstrate that prenatal obesity influences the developing brain before birth, and they provide insight into the specific neurological pathways by which obesity‐related transfer of risk may occur.…”

Section: Introductionmentioning

confidence: 99%

An examination of maternal prenatal BMI and human fetal brain development

Norr

Hect

Lenniger

et al. 2020

Child Psychology Psychiatry

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Background: Prenatal development is a time when the brain is acutely vulnerable to insult and alteration by environmental factors (e.g., toxins, maternal health). One important risk factor is maternal obesity (Body Mass Index > 30). Recent research indicates that high maternal BMI during pregnancy is associated with increased risk for numerous physical health, cognitive, and mental health problems in offspring across the lifespan. It is possible that heightened maternal prenatal BMI influences the developing brain even before birth. Methods: The present study examines this possibility at the level of macrocircuitry in the human fetal brain. Using a data-driven strategy for parcellating the brain into subnetworks, we test whether MRI functional connectivity within or between fetal neural subnetworks varies with maternal prenatal BMI in 109 fetuses between the ages of 26 and 39weeks. Results: We discovered that strength of connectivity between two subnetworks, left anterior insula/inferior frontal gyrus (aIN/ IFG) and bilateral prefrontal cortex (PFC), varied with maternal BMI. At the level of individual aIN/IFG-PFC connections, we observed both increased and decreased between-network connectivity with a tendency for increased within-hemisphere connectivity and reduced cross-hemisphere connectivity in higher BMI pregnancies. Maternal BMI was not associated with global differences in network topography based on network-based statistical analyses. Conclusions: Overall effects were localized in regions that will later support behavioral regulation and integrative processes, regions commonly associated with obesity-related deficits. By establishing onset in neural differences prior to birth, this study supports a model in which maternal BMI-related risk is associated with fetal connectomelevel brain organization with implications for offspring long-term cognitive development and mental health.

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The link between maternal obesity and offspring neurobehavior: A systematic review of animal experiments

Cited by 33 publications

References 69 publications

Relationship of prenatal maternal obesity and diabetes to offspring neurodevelopmental and psychiatric disorders: a narrative review

Relationship of prenatal maternal obesity and diabetes to offspring neurodevelopmental and psychiatric disorders: a narrative review

The placenta‐brain‐axis

An examination of maternal prenatal BMI and human fetal brain development

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