Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis

ABSTRACT

Recent evidence has suggested that changes in maternal gut microbiota in early life may generate neurobiological consequences associated with psychiatric-related abnormalities. However, the number of studies on humans investigating this problem is limited, and preclinical findings sometimes conflict. Therefore, we run a meta-analysis to examine whether maternal microbiota disturbance (MMD) during neurodevelopment might affect the offspring during adulthood. We found thirteen studies, from a set of 459 records selected by strategy registered on PROSPERO (#289224), to target preclinical studies that evaluated the behavioral outcomes of the rodents generated by dams submitted to perinatal enteric microbiota perturbation. The analysis revealed a significant effect size (SMD = −0.51, 95% CI = −0.79 to −0.22, p < .001, T2 = 0.54, I2 = 79.85%), indicating that MMD might provoke behavioral impairments in the adult offspring. The MMD also induces a significant effect size for the reduction of the sociability behavior (SMD = −0.63, 95% CI = −1.18 to −0.07, p = 0.011, T2 = 0.30, I2 = 76.11%) and obsessive-compulsive-like behavior (SMD = −0.68, 95% CI = −0.01 to −1.36, p = 0.009, T2 = 0.25, I2 = 62.82%) parameters. The effect size was not significant or inconclusive for memory and anxiety-like behavior, or inconclusive for schizophrenia-like and depressive-like behavior. Therefore, experimental perinatal MMD is vertically transmitted to the offspring, negatively impacting behavioral parameters related to psychiatric disorders.

GRAPHICAL ABSTRACT

KEYWORDS:

• Maternal microbiome disturbance
• neurodevelopment
• gut-brain axis
• psychiatric disorder
• sociability
• autism spectrum disorder

Acknowledgments

The authors are thankful to Andreia Vieira, Carla Saudanha, and André Sales for their kind office and technical support. CLO received funds from the Alexander von Humboldt Foundation to keep the website CAMARADES BR (https://camaradesbrasil.bio.br/).

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2226282

Additional information

Funding

The work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [88887.630534/2021-00]; Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro [E-26/203.383/2021].