Antenatal depressive symptoms impair offspring neurodevelopment by inducing maternal gut microbiota dysbiosis during pregnancy
COMMENTED ARTICLE - Children’ section
By Prof. Emmanuel Mas
Gastroenterology and Nutrition Department,
Children’s Hospital, Toulouse, France
Comments on the original article by Zhou et al.¹
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About this article
In a cohort of more than 2,000 pregnant women, the authors of this article found that depressive symptoms occurring during any trimester of pregnancy were associated with delayed neurocognitive development in infants. Analysis of the maternal gut microbiota revealed a reduction in butyrate-producing bacteria and disruptions in amino acid metabolism among women experiencing antenatal depression. These alterations were correlated with poorer cognitive outcomes in their children. To investigate causality, the microbiota from women with depressive symptoms was transplanted into germ-free pregnant mice. This transfer led to impaired intestinal barrier function, increased foetal brain inflammation, and metabolic disturbances in the developing brain, ultimately resulting in cognitive deficits in the offspring. Maternal supplementation with butyrate partially reversed these abnormalities. Overall, the findings suggest that antenatal depression may influence foetal brain development through changes in the maternal gut microbiota and its metabolites, highlighting potential preventive and therapeutic targets.
What do we already know about this subject?
Antenatal depression (AND) prevalence is around 20% worldwide and is associated with increased risk of miscarriage, preterm birth and low birth weight. However, the link between AND and neurodevelopmental issues has not been clearly established. Studies show that depression can alter the composition of the gut microbiota (GM). According to some studies, maternal mood disorders during pregnancy can also disrupt both their own GM and that of their offspring. Disruption to maternal GM during pregnancy could therefore alter brain development.
To assess the effect of maternal GM, prior to mating the authors transferred GM taken from AND at-risk mothers (AND-M group) and controls (Control-M group) to germ-free mice. The GM composition of the mice was similar prior to mating while at E18.5 (late foetal stage) it was similar to that of the respective donors. AND-M mice exhibited impaired performance in neurodevelopmental tests (escape time, platform crossing) (figure 2). A foetal brain metabolomic analysis showed reduced activity of polyunsaturated fatty-acid (PUFAs) pathways and amino-acid pathways in AND-M mice. An increase in inflammatory cytokines (TNF-α and IL-1β) was also observed in the AND-M group. Finally, mothers in the AND-M group had increased intestinal permeability, as assessed by immunohistochemistry, which revealed lower expression of tight junction proteins (claudin-1, ZO-1, and ZO-2) (figure 3), as well as higher inflammatory cytokine levels in serum (TNF-α and IL-1β).
Butyrate supplementation given to mice during pregnancy not only improved the neurodevelopment of their offspring but also increased PUFA and amino-acid levels, improved maternal gut barrier function and reduced the levels of inflammatory cytokines in foetal brains and maternal serum.
What are the consequences in practice?
The effects of antenatal depression on the developing foetal brain may be mitigated through butyrate supplementation.
Key points
- Antenatal depression is associated with altered infant neurodevelopment
- Maternal gut microbiota could play a role in this association
- In mice, butyrate mitigated the anomalies observed and improved neurodevelopment
Assessment of neurodevelopment in the offspring of germ-free mice having received faecal matter from control mothers (Control_M), AND mothers (AND_M) and AND mothers treated with butyrate during pregnancy (AND+butyr_M). Tests assessed mobility on a platform and showed that mobility was impaired in the AND_M group and improved after receiving butyrate supplementation during pregnancy.
Measurement of tight junction protein expression (claudin-1, ZO-1, ZO-2) between colonocytes, reflecting gut permeability in germ-free mice having received faecal matter from control mothers (Control_M), AND mothers (AND_M) and AND mothers treated with butyrate during pregnancy (AND+butyr_M). Permeability was impaired in the AND_M group and improved with butyrate supplementation during pregnancy.
Conclusion
Antenatal depression impairs neurodevelopment in children, linked to changes in the maternal GM. Experiments conducted in mice showed that maternal gut dysbiosis increases intestinal permeability, which in turn is associated with foetal brain inflammation and lower activity of metabolic pathways (PUFAs and amino acids). Butyrate supplementation during pregnancy mitigated these effects.