The mediating effect of maternal gut microbiota between prenatal psychological distress and neurodevelopment of infants

J Affect Disord. 2024 Oct 1:362:893-902. doi: 10.1016/j.jad.2024.07.045. Epub 2024 Jul 14.

Abstract

Background: Prenatal psychological distress and maternal inflammation can increase the risk of neurodevelopmental delay in offspring; recently, the gut microbiota has been shown to may be a potential mechanism behind this association and not fully elucidated in population study.

Methods: Seventy-two maternal-infant pairs who completed the assessments of prenatal psychological distress during the third trimester and neurodevelopment of infants at age 6-8 months of age were included in this study. The gut microbiota and its short-chain fatty acids (SCFAs) of maternal-infant were determined by 16S rRNA sequencing and liquid chromatography-mass spectrometry analysis. Inflammatory cytokines in the blood of pregnant women during the third trimester were detected by luminex liquid suspension microarrays.

Results: This study found that infants in the prenatal psychological distress group had poorer fine motor skills (β = -4.396, 95 % confidence interval (CI) = -8.546, -0.246, p = 0.038), problem-solving skills (β = -5.198, 95 % CI = -10.358, -0.038, p = 0.048) and total development (β = -22.303, 95%CI = -41.453, -3.153, p = 0.022) compared to the control group. The study also indicated that the higher level of interleukin-1β (IL-1β) (β = -1.951, 95%CI = -3.321, -0.581, p = 0.005) and interferon-inducible protein-10 (IP-10) (β = -0.019, 95%CI = -0.034, -0.004, p = 0.015) during the third trimester, the poorer fine motor skills in infants. Also, the higher level of IL-10 (β = -0.498, 95%CI = -0.862, -0.133, p = 0.007), IL-12p70 (β = -0.113, 95%CI = -0.178, -0.048, p = 0.001), IL-17 A (β = -0.817, 95%CI = -1.517, -0.118, p = 0.022), interferon-γ (β = -0.863, 95%CI = -1.304, -0.422, p < 0.001), IP-10 (β = -0.020, 95%CI = -0.038, -0.001, p = 0.035), and regulated upon activation normal T cell expressed and secreted (β = -0.002, 95%CI = -0.003, -0.001, p = 0.005) during the third trimester, the poorer problem-solving skills in infants. After controlling for relevant covariates, this study found that maternal gut microbiota Roseburia mediates the relationship between prenatal psychological distress and total neurodevelopment of infants (a = 0.433, 95%CI = 0.079, 0.787, p = 0.017; b = -19.835, 95%CI = -33.877, -5.792, p = 0.006; c = 22.407, 95%CI = -43.207,-1.608, p = 0.035; indirect effect = -8.584, 95%CI = -21.227, -0.587).

Conclusions: This is the first study to emphasize the role of the maternal-infant gut microbiota in prenatal psychological distress and infant neurodevelopment. Further studies are needed to explore the biological mechanisms underlying the relationship between prenatal psychological distress, maternal-infant gut microbiota, and infant neurodevelopment.

Keywords: Gut microbiota; Infant; Inflammation; Neurodevelopment; Prenatal psychological distress; Short-chain fatty acids.

MeSH terms

  • Adult
  • Child Development* / physiology
  • Cytokines / blood
  • Female
  • Gastrointestinal Microbiome* / physiology
  • Humans
  • Infant
  • Male
  • Neurodevelopmental Disorders / microbiology
  • Pregnancy
  • Pregnancy Complications / microbiology
  • Pregnancy Complications / psychology
  • Pregnancy Trimester, Third
  • Prenatal Exposure Delayed Effects* / microbiology
  • Prenatal Exposure Delayed Effects* / psychology
  • Psychological Distress
  • Stress, Psychological / microbiology

Substances

  • Cytokines