Adverse Prenatal Exposures and Fetal Brain Development: Insights From Advanced Fetal Magnetic Resonance Imaging

doi:10.1016/j.bpsc.2021.11.009

Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

Volume 7, Issue 5, May 2022, Pages 480-490

https://doi.org/10.1016/j.bpsc.2021.11.009 Get rights and content

Abstract

Converging evidence from clinical and preclinical studies suggests that fetal vulnerability to adverse prenatal exposures increases the risk for neuropsychiatric diseases such as autism spectrum disorder, schizophrenia, and depression. Recent advances in fetal magnetic resonance imaging have allowed us to characterize typical fetal brain growth trajectories in vivo and to interrogate structural and functional alterations associated with intrauterine exposures, such as maternal stress, environmental toxins, drugs, and obesity. Here, we review proposed mechanisms for how prenatal influences disrupt neurodevelopment, including the role played by maternal and fetal inflammatory responses. We summarize insights from magnetic resonance imaging research in fetuses, highlight recent discoveries in normative fetal development using quantitative magnetic resonance imaging techniques (i.e., three-dimensional volumetry, proton magnetic resonance spectroscopy, placental diffusion imaging, and functional imaging), and discuss how baseline trajectories are shaped by prenatal exposures.

Section snippets

Fetal Brain Imaging

Quantitative MRI techniques are difficult to implement in the fetus. The main challenges of in vivo fetal MRI include unpredictable and largely unconstrained fetal motion during scans, low tissue contrast, small anatomical structures, and rapidly changing brain morphology. The development of subsecond, ultrafast T2-weighted sequences (i.e., single-shot fast spin echo) in the mid-1990s has greatly enhanced our ability to image the fetal brain (25,26). Rapid acquisition techniques minimized image

Preclinical Findings

In utero exposure to alcohol, nicotine, and drugs can profoundly impact brain development (45). The cellular and molecular mechanisms underpinning adverse long-term neurologic outcomes in exposed fetuses remain unclear, but animal models suggest that increased inflammatory chemokines/cytokines in maternal sera and fetal brain likely disrupt fetal neurodevelopment. For example, increased fetal interleukin (IL) 1β and IL-17 in alcohol-exposed mice have been linked to altered myelination, impaired

Preclinical Findings

Exposure to environmental toxins, such as lead, mercury, and arsenic, may also adversely affect fetal brain development and has been linked to delayed cognitive functioning, developmental disorders (i.e., autism spectrum disorder [ASD]), and neurologic impairments (59,60). Increased glial activation, which induces a pathologic proinflammatory state, has been shown postnatally in brains of rats chronically exposed to lead in utero. Lead-related neuroinflammatory changes were most pronounced in

Preclinical Findings

Infection in pregnancy is a powerful mediator of fever and inflammation (63). Maternal infection, and particularly intrauterine infection, activates the fetal inflammatory response syndrome, a condition associated with adverse neurologic outcomes (4,63). The underlying mechanisms on how inflammation impacts fetal brain development remain unclear, but several mechanisms have been proposed, including direct teratogenicity of hyperthermia and toxins (64,65), medication exposure, activation of

Preclinical Findings

In utero exposure to maternal stress, anxiety, and depression has been associated with lower birth weight, reduced GA at birth (84), poor neonatal behavioral outcomes (85), sociocognitive delays (86, 87, 88), and various neuropsychiatric conditions, such as mood disorders, attention-deficit/hyperactivity disorder, and ASD (89). Several mechanisms have been proposed on how maternal mental state influences fetal development and long-term neurologic outcomes. Maternal stress–induced immune

Preclinical Findings

Maternal obesity and malnutrition can influence long-term health and vulnerability to diseases of offspring. High maternal body mass index (BMI) has been shown to negatively affect cognitive performance in children (100); heighten their risk for developing neuropsychiatric disorders, such as depression, attention-deficit/hyperactivity disorder, and ASD (101); and increase their risk for developing obesity-related disorders (101). Obesity is considered a low-grade local and systemic inflammatory

Preclinical Findings

Evidence suggests that prenatal exposure to chronic hypoxia influences fetal brain development and may increase the risk for later neurologic impairment. Placental insufficiency and other obstetric complications, infection, vascular disorders, and conditions such as CHD may lead to reduced substrate delivery to the fetal brain; this interacts with a range of molecular and epigenetic processes that can shape neurodevelopment. Neurons are especially vulnerable to hypoxia, and this is likely one

Adverse Prenatal Exposures and Epigenetic Programming

While effects of prenatal adverse exposures appear to converge on maternal immune activation and the fetal inflammatory response, neurologic outcomes likely arise from complex interactions between inflammatory pathways, genetics, and epigenetic factors. Interactions with epigenetic factors may be especially relevant, as epigenetics includes mechanisms that modify gene expression mechanisms (i.e., DNA methylation and histone modification) that can link early life events to long-term outcomes.

Conclusions

Advances in fetal MRI are transforming our ability to noninvasively evaluate early neurodevelopment and more accurately study the impact of maternal and environmental factors on fetal wellness. These advances include technical improvements that lessen the effect of fetal motion and improve signal quality as well as innovative applications that allow for the study of dynamic, functional brain development. Early neurodevelopment is especially unique given the specific maturational processes that

Acknowledgments and Disclosures

The authors report no biomedical financial interests or potential conflicts of interest.

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Citation Excerpt :
Future epilepsy genetic panels will screen the fetus and neonate at risk for later epilepsy and comorbidities like ASD based on these genetic biomarkers. Targeted pregnancies with increased risk factors to the MPF triad such as maternal RA will apply trimester-specific imaging studies to the fetal brain and placenta74 to select those triads to screen for ASD and epilepsy. With expression of the great neonatl neurological syndromes these genetic and imaging screening tools can be applied or repeated as neurologic phenotypes are expressed.
Gene-environment (G x E) interactions significantly influence neurologic outcomes. The maternal-placental-fetal (MPF) triad, neonate, or child less than 2 years may first exhibit significant brain disorders. Neuroplasticity during the first 1000 days will more likely result in life-long effects given critical periods of development. Developmental origins and life-course principles help recognize changing neurologic phenotypes across ages. Dual diagnostic approaches are discussed using representative case scenarios to highlight time-dependent G x E interactions that contribute to neurologic sequelae. Horizontal analyses identify clinically relevant phenotypic form and function at different ages. Vertical analyses integrate the approach using systems-biology from genetic through multi-organ system interactions during each developmental age to understand etiopathogenesis. The process of ontogenetic adaptation results in immediate or delayed positive and negative outcomes specific to the developmental niche, expressed either as a healthy child or one with neurologic sequelae. Maternal immune activation, ischemic placental disease, and fetal inflammatory response represent prenatal disease pathways that contribute to fetal brain injuries. These processes involve G x E interactions within the MPF triad, phenotypically expressed as fetal brain malformations or destructive injuries within the MPF triad. A neonatal minority express encephalopathy, seizures, stroke, and encephalopathy of prematurity as a continuum of trimester-specific G x E interactions. This group may later present with childhood sequelae. A healthy neonatal majority present at older ages with sequelae such as developmental disorders, epilepsy, mental health diseases, tumors, and neurodegenerative disease, often during the first 1000 days. Effective preventive, rescue, and reparative neuroprotective strategies require consideration of G x E interactions interplay over time. Addressing maternal and pediatric health disparities will maximize medical equity with positive global outcomes that reduce the burden of neurologic diseases across the lifespan.

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ReviewAdverse Prenatal Exposures and Fetal Brain Development: Insights From Advanced Fetal Magnetic Resonance Imaging

Abstract

Section snippets

Fetal Brain Imaging

Preclinical Findings

Preclinical Findings

Preclinical Findings

Preclinical Findings

Preclinical Findings

Preclinical Findings

Adverse Prenatal Exposures and Epigenetic Programming

Conclusions

Acknowledgments and Disclosures

Am J Obstet Gynecol

Semin Fetal Neonatal Med

Brain Res

Am J Obstet Gynecol

Neuroimage

Int J Dev Neurosci

Neuroimage

Neuroimage

Neuroimage

Neuroimage

Placenta

Brain Behav Immun

Brain Res Dev Brain Res

J Neuroradiol

Neuroimage

Neuroimage

J Trace Elem Med Biol

Environ Res

Neuroimage

J Clin Virol

Brain Behav Immun

Biol Psychiatry

Handb Clin Neurol

Clin Microbiol Infect

J Obstet Gynaecol Can

Clin Perinatol

J Am Acad Child Adolesc Psychiatry

Biol Psychiatry

Inflammation during fetal and neonatal life: Implications for neurologic and neuropsychiatric disease in children and adults

Ann Neurol

Models of fetal brain injury, intrauterine inflammation, and preterm birth

Am J Reprod Immunol

The fetal inflammatory response syndrome

Clin Obstet Gynecol

Placental assessment provides insight into mechanisms and timing of neonatal hypoxic-ischemic encephalopathy

J Neonatal Perinatal Med

Chorioamnionitis in the development of cerebral palsy: A meta-analysis and systematic review

Pediatrics

Placental immune responses to viruses: Molecular and histo-pathologic perspectives

Int J Mol Sci

Role of inflammation in virus pathogenesis during pregnancy

J Virol

Hypoxia and oxidative stress induce sterile placental inflammation in vitro

Sci Rep

Preeclampsia and neurodevelopmental outcomes: Potential pathogenic roles for inflammation and oxidative stress?

Mol Neurobiol

Prenatal environmental metal exposure and preterm birth: A scoping review

Int J Environ Res Public Health

Unique maternal immune and functional microbial profiles during prenatal stress

Sci Rep

Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal antiinflammatory treatment

Endocrinology

Complex trajectories of brain development in the healthy human fetus

Cereb Cortex

Feasibility of QSM in the human placenta

Magn Reson Med

Fetal cerebral oxygenation is impaired in congenital heart disease and shows variable response to maternal hyperoxia

J Am Heart Assoc

Assessment of MRI-based automated fetal cerebral cortical folding measures in prediction of gestational age in the third trimester

AJNR Am J Neuroradiol

Quantitative in vivo MRI measurement of cortical development in the fetus

Brain Struct Funct

Global Network Organization of the Fetal Functional Connectome

Cereb Cortex

Short communication: MR imaging of fetal brain abnormalities using a HASTE sequence

Br J Radiol

MR imaging of the fetus by a HASTE sequence

Review
Adverse Prenatal Exposures and Fetal Brain Development: Insights From Advanced Fetal Magnetic Resonance Imaging