Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study

Abstract Background and aim Maternal overweight and breastfeeding seem to have a significant impact on the gut microbiota colonization process, which co-occurs simultaneously with brain development and the establishment of the “microbiota-gut-brain axis”, which potentially may affect behavior later...

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Main Authors: Ana Nieto-Ruiz, Tomás Cerdó, Belén Jordano, Francisco J. Torres-Espínola, Mireia Escudero-Marín, María García-Ricobaraza, Mercedes G. Bermúdez, José A. García-Santos, Antonio Suárez, Cristina Campoy
Format: Article
Language:English
Published: BMC 2023-03-01
Series:Child and Adolescent Psychiatry and Mental Health
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Online Access:https://doi.org/10.1186/s13034-023-00589-9
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author Ana Nieto-Ruiz
Tomás Cerdó
Belén Jordano
Francisco J. Torres-Espínola
Mireia Escudero-Marín
María García-Ricobaraza
Mercedes G. Bermúdez
José A. García-Santos
Antonio Suárez
Cristina Campoy
author_facet Ana Nieto-Ruiz
Tomás Cerdó
Belén Jordano
Francisco J. Torres-Espínola
Mireia Escudero-Marín
María García-Ricobaraza
Mercedes G. Bermúdez
José A. García-Santos
Antonio Suárez
Cristina Campoy
author_sort Ana Nieto-Ruiz
collection DOAJ
description Abstract Background and aim Maternal overweight and breastfeeding seem to have a significant impact on the gut microbiota colonization process, which co-occurs simultaneously with brain development and the establishment of the “microbiota-gut-brain axis”, which potentially may affect behavior later in life. This study aimed to examine the influence of maternal overweight, obesity and/or gestational diabetes on the offspring behavior at 3.5 years of age and its association with the gut microbiota already established at 18 months of life. Methods 156 children born to overweight (OV, n = 45), obese (OB, n = 40) and normoweight (NW, n = 71) pregnant women participating in the PREOBE study were included in the current analysis. Stool samples were collected at 18 months of life and gut microbiome was obtained by 16S rRNA gene sequencing. Behavioral problems were evaluated at 3.5 years by using the Child Behavior Checklist (CBCL). ANOVA, Chi-Square Test, ANCOVA, Spearman’s correlation, logistic regression model and generalized linear model (GLM) were performed. Results At 3.5 years of age, Children born to OV/OB mothers showed higher scores in behavioral problems than those born to NW mothers. Additionally, offspring born to OB mothers who developed gestational diabetes mellitus (GDM) presented higher scores in attention/deficit hyperactivity and externalizing problems than those born to GDM OV/NW mothers. Fusicatenibacter abundance found at 18 months of age was associated to lower scores in total, internalizing and pervasive developmental problems, while an unidentified genus within Clostridiales and Flavonifractor families abundance showed a positive correlation with anxiety/depression and somatic complaints, respectively. On the other hand, children born to mothers with higher BMI who were breastfed presented elevated anxiety, internalizing problems, externalizing problems and total problems scores; likewise, their gut microbiota composition at 18 months of age showed positive correlation with behavioral problems at 3.5 years: Actinobacteria abundance and somatic complaints and between Fusobacteria abundance and withdrawn behavior and pervasive developmental problems. Conclusions Our findings suggests that OV/OB and/or GDM during pregnancy is associated with higher behavioral problems scores in children at 3.5 years old. Additionally, associations between early life gut microbiota composition and later mental health in children was also found.
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spelling doaj.art-95d15d8b91ee42f1aad7afe71d6346292023-03-22T10:26:17ZengBMCChild and Adolescent Psychiatry and Mental Health1753-20002023-03-0117111810.1186/s13034-023-00589-9Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up studyAna Nieto-Ruiz0Tomás Cerdó1Belén Jordano2Francisco J. Torres-Espínola3Mireia Escudero-Marín4María García-Ricobaraza5Mercedes G. Bermúdez6José A. García-Santos7Antonio Suárez8Cristina Campoy9Department of Paediatrics, Faculty of Medicine, University of GranadaMaimonides Biomedical Research Institute of Córdoba (IMIBIC), Reina Sofia University Hospital, University of CórdobaDepartment of Paediatrics, Faculty of Medicine, University of GranadaBiomedical Research Centre, EURISTIKOS Excellence Centre for Paediatric Research, University of GranadaDepartment of Paediatrics, Faculty of Medicine, University of GranadaDepartment of Paediatrics, Faculty of Medicine, University of GranadaDepartment of Paediatrics, Faculty of Medicine, University of GranadaDepartment of Paediatrics, Faculty of Medicine, University of GranadaDepartment of Biochemistry and Molecular Biology 2, School of Pharmacy, University of GranadaDepartment of Paediatrics, Faculty of Medicine, University of GranadaAbstract Background and aim Maternal overweight and breastfeeding seem to have a significant impact on the gut microbiota colonization process, which co-occurs simultaneously with brain development and the establishment of the “microbiota-gut-brain axis”, which potentially may affect behavior later in life. This study aimed to examine the influence of maternal overweight, obesity and/or gestational diabetes on the offspring behavior at 3.5 years of age and its association with the gut microbiota already established at 18 months of life. Methods 156 children born to overweight (OV, n = 45), obese (OB, n = 40) and normoweight (NW, n = 71) pregnant women participating in the PREOBE study were included in the current analysis. Stool samples were collected at 18 months of life and gut microbiome was obtained by 16S rRNA gene sequencing. Behavioral problems were evaluated at 3.5 years by using the Child Behavior Checklist (CBCL). ANOVA, Chi-Square Test, ANCOVA, Spearman’s correlation, logistic regression model and generalized linear model (GLM) were performed. Results At 3.5 years of age, Children born to OV/OB mothers showed higher scores in behavioral problems than those born to NW mothers. Additionally, offspring born to OB mothers who developed gestational diabetes mellitus (GDM) presented higher scores in attention/deficit hyperactivity and externalizing problems than those born to GDM OV/NW mothers. Fusicatenibacter abundance found at 18 months of age was associated to lower scores in total, internalizing and pervasive developmental problems, while an unidentified genus within Clostridiales and Flavonifractor families abundance showed a positive correlation with anxiety/depression and somatic complaints, respectively. On the other hand, children born to mothers with higher BMI who were breastfed presented elevated anxiety, internalizing problems, externalizing problems and total problems scores; likewise, their gut microbiota composition at 18 months of age showed positive correlation with behavioral problems at 3.5 years: Actinobacteria abundance and somatic complaints and between Fusobacteria abundance and withdrawn behavior and pervasive developmental problems. Conclusions Our findings suggests that OV/OB and/or GDM during pregnancy is associated with higher behavioral problems scores in children at 3.5 years old. Additionally, associations between early life gut microbiota composition and later mental health in children was also found.https://doi.org/10.1186/s13034-023-00589-9ObesityGestational diabetes mellitusPregnancyMicrobiota-gut-brain axisEarly programmingChildren
spellingShingle Ana Nieto-Ruiz
Tomás Cerdó
Belén Jordano
Francisco J. Torres-Espínola
Mireia Escudero-Marín
María García-Ricobaraza
Mercedes G. Bermúdez
José A. García-Santos
Antonio Suárez
Cristina Campoy
Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study
Child and Adolescent Psychiatry and Mental Health
Obesity
Gestational diabetes mellitus
Pregnancy
Microbiota-gut-brain axis
Early programming
Children
title Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study
title_full Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study
title_fullStr Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study
title_full_unstemmed Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study
title_short Maternal weight, gut microbiota, and the association with early childhood behavior: the PREOBE follow-up study
title_sort maternal weight gut microbiota and the association with early childhood behavior the preobe follow up study
topic Obesity
Gestational diabetes mellitus
Pregnancy
Microbiota-gut-brain axis
Early programming
Children
url https://doi.org/10.1186/s13034-023-00589-9
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