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      Michigan cohorts to determine associations of maternal pre-pregnancy body mass index with pregnancy and infant gastrointestinal microbial communities: Late pregnancy and early infancy

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          Abstract

          Background

          About 25% of women in the United States are obese prior to becoming pregnant. Although there is some knowledge about the relationship between the gastrointestinal microbiota and obesity, little is known about the relationship between pre-pregnancy obesity and the gastrointestinal microbiota in pregnancy or its impact on infant gut microbiota. However, the composition of the gut microbiota early in life may influence childhood health. Thus, the objective of this research was to identify associations between maternal pre-pregnancy obesity and the pregnancy (n = 39) or early infancy (n = 39) microbiotas.

          Results

          Fecal bacterial communities from overweight women had lower microbiota diversity (Chao1: p = 0.02; inverse Simpson: p = 0.05; Shannon: p = 0.02) than communities from normal weight or obese women. The within-group microbiota composition of overweight women differed from those of normal and obese women at the genus and phylum levels (p = 0.003 and p = 0.02, respectively). Pre-pregnancy overweight women had higher abundances of Bacteroides and lower Phascolarctobacterium than women who were normal weight or obese prior to becoming pregnant. Normal weight women had lower abundances of Acidaminococcus and Dialister than overweight and obese women. Infant community composition tended to differ in membership (Sorensen index) by maternal pre-pregnancy BMI category, and significantly differed by delivery mode and breastfeeding exclusivity (p = 0.06, p = 0.001, p = 0.008, respectively). Infants from normal weight women had lower abundances of Megasphaera than infants from overweight or obese women. Streptococcus was lowest in infants from overweight women, and Staphylococcus was lowest in infants from obese women.

          Conclusion

          Maternal and infant microbiotas are associated with and might be affected by maternal pre-pregnancy BMI. Future work should determine if there are also functional differences in the infant microbiome, if those functional differences are related to maternal pre-pregnancy BMI, and whether differences in composition or traits persist over time.

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          Most cited references38

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          Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort

          Background The gut is the most extensively studied niche of the human microbiome. The aim of this study was to characterise the initial gut microbiota development of a cohort of breastfed infants (n = 192) from 1 to 24 weeks of age. Methods V4-V5 region 16S rRNA amplicon Illumina sequencing and, in parallel, bacteriological culture. The metabolomic profile of infant urine at 4 weeks of age was also examined by LC-MS. Results Full-term (FT), spontaneous vaginally delivered (SVD) infants’ microbiota remained stable at both phylum and genus levels during the 24-week period examined. FT Caesarean section (CS) infants displayed an increased faecal abundance of Firmicutes (p < 0.01) and lower abundance of Actinobacteria (p < 0.001) after the first week of life compared to FT-SVD infants. FT-CS infants gradually progressed to harbouring a microbiota closely resembling FT-SVD (which remained stable) by week 8 of life, which was maintained at week 24. The gut microbiota of preterm (PT) infants displayed a significantly greater abundance of Proteobacteria compared to FT infants (p < 0.001) at week 1. Metabolomic analysis of urine at week 4 indicated PT-CS infants have a functionally different metabolite profile than FT (both CS and SVD) infants. Co-inertia analysis showed co-variation between the urine metabolome and the faecal microbiota of the infants. Tryptophan and tyrosine metabolic pathways, as well as fatty acid and bile acid metabolism, were found to be affected by delivery mode and gestational age. Conclusions These findings confirm that mode of delivery and gestational age both have significant effects on early neonatal microbiota composition. There is also a significant difference between the metabolite profile of FT and PT infants. Prolonged breastfeeding was shown to have a significant effect on the microbiota composition of FT-CS infants at 24 weeks of age, but interestingly not on that of FT-SVD infants. Twins had more similar microbiota to one another than between two random infants, reflecting the influence of similarities in both host genetics and the environment on the microbiota. Electronic supplementary material The online version of this article (doi:10.1186/s40168-016-0213-y) contains supplementary material, which is available to authorized users.
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            Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: a prospective cohort study.

            Dysbiosis of the infant gut microbiota may have long-term health consequences. This study aimed to determine the impact of maternal intrapartum antibiotic prophylaxis (IAP) on infant gut microbiota, and to explore whether breastfeeding modifies these effects.
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              Interactions between Gut Microbiota, Host Genetics and Diet Modulate the Predisposition to Obesity and Metabolic Syndrome.

              Obesity, diabetes, and metabolic syndrome result from complex interactions between genetic and environmental factors, including the gut microbiota. To dissect these interactions, we utilized three commonly used inbred strains of mice-obesity/diabetes-prone C57Bl/6J mice, obesity/diabetes-resistant 129S1/SvImJ from Jackson Laboratory, and obesity-prone but diabetes-resistant 129S6/SvEvTac from Taconic-plus three derivative lines generated by breeding these strains in a new, common environment. Analysis of metabolic parameters and gut microbiota in all strains and their environmentally normalized derivatives revealed strong interactions between microbiota, diet, breeding site, and metabolic phenotype. Strain-dependent and strain-independent correlations were found between specific microbiota and phenotypes, some of which could be transferred to germ-free recipient animals by fecal transplantation. Environmental reprogramming of microbiota resulted in 129S6/SvEvTac becoming obesity resistant. Thus, development of obesity/metabolic syndrome is the result of interactions between gut microbiota, host genetics, and diet. In permissive genetic backgrounds, environmental reprograming of microbiota can ameliorate development of metabolic syndrome.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 March 2019
                2019
                : 14
                : 3
                : e0213733
                Affiliations
                [1 ] Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI, United States of America
                [2 ] Department of Epidemiology and Biostatistics, College of Human Medicine, Michigan State University, East Lansing, MI, United States of America
                [3 ] Department of Pediatrics and Human Development, College of Human Medicine, Michigan State University, East Lansing, MI, United States of America
                University of Missouri Columbia, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-3107-7652
                Article
                PONE-D-18-22520
                10.1371/journal.pone.0213733
                6422265
                30883572
                72d41b48-b6aa-48e5-9bb2-69d419138633
                © 2019 Sugino et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 30 July 2018
                : 27 February 2019
                Page count
                Figures: 2, Tables: 5, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: UG3 OD023285
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100011138, AgBioResearch, Michigan State University;
                Award Recipient :
                Kameron Sugino was supported by a research assistantship from the Michigan State University Department of Food Science and Human Nutrition. This research was financially supported by funds provided to SSC by Michigan State AgBioResearch and by funds provided to NP by the National Institutes of Health Environmental Influences on Child Health Outcomes (ECHO) Program (Prenatal Exposures and Child Health Outcomes: A Statewide Study (UG3 OD023285)).
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                All relevant data are with the manuscript, its Supporting Information files, and the NCBI SRA, with sequences available under accession number PRJNA506270.

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