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

ABSTRACTRecent 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...

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Main Authors: Lucas Hassib, Cilene Lino de Oliveira, Guilherme Araujo Rouvier, Alexandre Kanashiro, Francisco Silveira Guimarães, Frederico Rogério Ferreira
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2023.2226282
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author Lucas Hassib
Cilene Lino de Oliveira
Guilherme Araujo Rouvier
Alexandre Kanashiro
Francisco Silveira Guimarães
Frederico Rogério Ferreira
author_facet Lucas Hassib
Cilene Lino de Oliveira
Guilherme Araujo Rouvier
Alexandre Kanashiro
Francisco Silveira Guimarães
Frederico Rogério Ferreira
author_sort Lucas Hassib
collection DOAJ
description ABSTRACTRecent 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.
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spelling doaj.art-d8141a2f690645f985e8cf1afcb946e72024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2226282Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysisLucas Hassib0Cilene Lino de Oliveira1Guilherme Araujo Rouvier2Alexandre Kanashiro3Francisco Silveira Guimarães4Frederico Rogério Ferreira5Oswaldo Cruz Institute, Oswaldo Cruz Foundation, Rio de Janeiro, BrazilDepartment of Physiological Sciences, Center of Biological Sciences, Federal University of Santa Catarina, Florianópolis, BrazilOswaldo Cruz Institute, Oswaldo Cruz Foundation, Rio de Janeiro, BrazilDepartment of Dermatology, Medical Sciences Center, University of Wisconsin-Madison, Madison, WI, USADepartment of Pharmacology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilOswaldo Cruz Institute, Oswaldo Cruz Foundation, Rio de Janeiro, BrazilABSTRACTRecent 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.https://www.tandfonline.com/doi/10.1080/19490976.2023.2226282Maternal microbiome disturbanceneurodevelopmentgut-brain axispsychiatric disordersociabilityautism spectrum disorder
spellingShingle Lucas Hassib
Cilene Lino de Oliveira
Guilherme Araujo Rouvier
Alexandre Kanashiro
Francisco Silveira Guimarães
Frederico Rogério Ferreira
Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis
Gut Microbes
Maternal microbiome disturbance
neurodevelopment
gut-brain axis
psychiatric disorder
sociability
autism spectrum disorder
title Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis
title_full Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis
title_fullStr Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis
title_full_unstemmed Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis
title_short Maternal microbiome disturbance induces deficits in the offspring’s behaviors: a systematic review and meta-analysis
title_sort maternal microbiome disturbance induces deficits in the offspring s behaviors a systematic review and meta analysis
topic Maternal microbiome disturbance
neurodevelopment
gut-brain axis
psychiatric disorder
sociability
autism spectrum disorder
url https://www.tandfonline.com/doi/10.1080/19490976.2023.2226282
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