Maternal exposures and the infant gut microbiome: a systematic review with meta-analysis

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ABSTRACT

Early life, including the establishment of the intestinal microbiome, represents a critical window of growth and development. Postnatal factors affecting the microbiome, including mode of delivery, feeding type, and antibiotic exposure have been widely investigated, but questions remain regarding the influence of exposures in utero on infant gut microbiome assembly. This systematic review aimed to synthesize evidence on exposures before birth, which affect the early intestinal microbiome. Five databases were searched in August 2019 for studies exploring pre-pregnancy or pregnancy ‘exposure’ data in relation to the infant microbiome. Of 1,441 publications identified, 76 were included. Factors reported influencing microbiome composition and diversity included maternal antibiotic and probiotic uses, dietary intake, pre-pregnancy body mass index (BMI), gestational weight gain (GWG), diabetes, mood, and others. Eleven studies contributed to three meta-analyses quantifying associations between maternal intrapartum antibiotic exposure (IAP), BMI and GWG, and infant microbiome alpha diversity (Shannon Index). IAP, maternal overweight/obesity and excessive GWG were all associated with reduced diversity. Most studies were observational, few included early recruitment or longitudinal follow-up, and the timing, frequency, and methodologies related to stool sampling and analysis were variable. Standardization and collaboration are imperative to enhance understanding in this complex and rapidly evolving area.

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Diet rapidly and reproducibly alters the human gut microbiome

Lawrence A David, Corinne F. Maurice, Rachel Carmody … (2013)

Long-term diet influences the structure and activity of the trillions of microorganisms residing in the human gut 1–5 , but it remains unclear how rapidly and reproducibly the human gut microbiome responds to short-term macronutrient change. Here, we show that the short-term consumption of diets composed entirely of animal or plant products alters microbial community structure and overwhelms inter-individual differences in microbial gene expression. The animal-based diet increased the abundance of bile-tolerant microorganisms (Alistipes, Bilophila, and Bacteroides) and decreased the levels of Firmicutes that metabolize dietary plant polysaccharides (Roseburia, Eubacterium rectale, and Ruminococcus bromii). Microbial activity mirrored differences between herbivorous and carnivorous mammals 2 , reflecting trade-offs between carbohydrate and protein fermentation. Foodborne microbes from both diets transiently colonized the gut, including bacteria, fungi, and even viruses. Finally, increases in the abundance and activity of Bilophila wadsworthia on the animal-based diet support a link between dietary fat, bile acids, and the outgrowth of microorganisms capable of triggering inflammatory bowel disease 6 . In concert, these results demonstrate that the gut microbiome can rapidly respond to altered diet, potentially facilitating the diversity of human dietary lifestyles.

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Human gut microbiome viewed across age and geography

Tanya Yatsunenko, Federico E Rey, Mark Manary … (2012)

Gut microbial communities represent one source of human genetic and metabolic diversity. To examine how gut microbiomes differ between human populations when viewed from the perspective of component microbial lineages, encoded metabolic functions, stage of postnatal development, and environmental exposures, we characterized bacterial species present in fecal samples obtained from 531 individuals representing healthy Amerindians from the Amazonas of Venezuela, residents of rural Malawian communities, and inhabitants of USA metropolitan areas, as well as the gene content of 110 of their microbiomes. This cohort encompassed infants, children, teenagers and adults, parents and offspring, and included mono- and dizygotic twins. Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the representation of genes involved in vitamin biosynthesis and metabolism. Pronounced differences in bacterial species assemblages and functional gene repertoires were noted between individuals residing in the USA compared to the other two countries. These distinctive features are evident in early infancy as well as adulthood. In addition, the similarity of fecal microbiomes among family members extends across cultures. These findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations, and the impact of Westernization.

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Metabolic endotoxemia initiates obesity and insulin resistance.

Patrice Cani, Jacques Amar, Miguel Angel Iglesias … (2007)

Diabetes and obesity are two metabolic diseases characterized by insulin resistance and a low-grade inflammation. Seeking an inflammatory factor causative of the onset of insulin resistance, obesity, and diabetes, we have identified bacterial lipopolysaccharide (LPS) as a triggering factor. We found that normal endotoxemia increased or decreased during the fed or fasted state, respectively, on a nutritional basis and that a 4-week high-fat diet chronically increased plasma LPS concentration two to three times, a threshold that we have defined as metabolic endotoxemia. Importantly, a high-fat diet increased the proportion of an LPS-containing microbiota in the gut. When metabolic endotoxemia was induced for 4 weeks in mice through continuous subcutaneous infusion of LPS, fasted glycemia and insulinemia and whole-body, liver, and adipose tissue weight gain were increased to a similar extent as in high-fat-fed mice. In addition, adipose tissue F4/80-positive cells and markers of inflammation, and liver triglyceride content, were increased. Furthermore, liver, but not whole-body, insulin resistance was detected in LPS-infused mice. CD14 mutant mice resisted most of the LPS and high-fat diet-induced features of metabolic diseases. This new finding demonstrates that metabolic endotoxemia dysregulates the inflammatory tone and triggers body weight gain and diabetes. We conclude that the LPS/CD14 system sets the tone of insulin sensitivity and the onset of diabetes and obesity. Lowering plasma LPS concentration could be a potent strategy for the control of metabolic diseases.

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Journal

Journal ID (nlm-ta): Gut Microbes

Journal ID (iso-abbrev): Gut Microbes

Title: Gut Microbes

Publisher: Taylor & Francis

ISSN (Print): 1949-0976

ISSN (Electronic): 1949-0984

Publication date (Electronic, pub): 12 May 2021

Publication date (Electronic, collection): 2021

Publication date PMC-release: 12 May 2021

Volume: 13

Issue: 1

Electronic Location Identifier: 1897210

Affiliations

[a ]Central Clinical School, Faculty of Medicine and Health, University of Sydney; , Camperdown, New South Wales (NSW), Australia

[b ]Charles Perkins Centre, University of Sydney; , Camperdown, NSW, Australia

[c ]School of Health Sciences, Faculty of Health and Medicine, University of Newcastle; , Callaghan, NSW, Australia

[d ]Priority Research Centre for Physical Activity and Nutrition, University of Newcastle; , Callaghan, NSW, Australia

[e ]School of Life and Environmental Sciences, Faculty of Science, University of Sydney; , Camperdown, NSW, Australia

Author notes

CONTACT Allison Grech agre2034@ 123456uni.sydney.edu.au Charles Perkins Centre, the University of Sydney; , Camperdown, NSW, 2006, Australia.

Article

Publisher ID: 1897210

DOI: 10.1080/19490976.2021.1897210

PMC ID: 8276657

PubMed ID: 33978558

SO-VID: 3be99ff9-45c1-4bd7-ab2f-cd214a1d9c5a

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Maternal exposures and the infant gut microbiome: a systematic review with meta-analysis

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Most cited references 192

Diet rapidly and reproducibly alters the human gut microbiome

Human gut microbiome viewed across age and geography

Metabolic endotoxemia initiates obesity and insulin resistance.

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