Gut-Brain Axis in the Early Postnatal Years of Life: A Developmental Perspective

Jena, Ankita; Montoya, Carlos A.; Mullaney, Jane A.; Dilger, Ryan N.; Young, Wayne; McNabb, Warren C.; Roy, Nicole C.

doi:10.3389/fnint.2020.00044

Cited by 64 publications

(61 citation statements)

References 249 publications

(324 reference statements)

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“…These pathways play pivotal roles in regulating cellular processes of oxidative stress and immune activation, energy metabolism, and biosynthesis, and also involved in degenerative disorders and aging ( Orlandi et al., 2020 ). These differences may relate to the sex differences in the hypothalamic-pituitary-adrenal (HPA) axis’ response to early life stress among preterm infants, mediated by HPA produced glucocorticoids, cortisol, and other hormones ( Cong et al., 2015 ; Jena et al., 2020 ). Limited studies are discovering gut microbiome metabolism in human infants.…”

Section: Discussionmentioning

confidence: 99%

Sex Differences in Gut Microbial Development of Preterm Infant Twins in Early Life: A Longitudinal Analysis

Chen

Hird

et al. 2021

Front. Cell. Infect. Microbiol.

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Infant gut microbiota plays a vital role in immune response, mediates neurobehavioral development and health maintenance. Studies of twins’ gut microbiota found that gut microbiota composition and diversity tend to be mature and stable with increasing postnatal age (PNA). Preterm infant gut microbiome shifts dramatically when they were staying in the neonatal intensive care unit (NICU). Compositions and shifting characteristics of gut microbiota among neonatal preterm twins and triplets during their early life are still unknown, which impedes a better understanding of the mechanism underpinning neurobehavioral development and precise intervention/health of preterm neonates. This longitudinal cohort study used a twins/triplets design to investigate the interaction of genetic (e.g., male vs. female) and environmental factors influencing the development of the gut microbiome in early life. We included 39 preterm infants, 12 were Female twins/triplets (Female T/T) including 3 twins pairs and 2 triplets, 12 were male twins (Male T) including 6 twins pairs, and 15 were mixed-sex twins/triplets (Mix T/T) including 6 twins pairs and 1 triplet (8 females and 7 males) during the first four weeks of NICU stay. Weekly gut microbiota patterns between females and males were compared by linear discriminant analysis (LDA) effect size (LEfSe). Metagenomics function of gut microbiota was predicted by using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt). Weekly function (KEGG pathways) differences between females and males were detected by using Statistical Analysis of Metagenomic Profiles (STAMP). Results found that female pairs and male pairs were significantly different in gut microbiome diversity, compositions, and predicted metabolic profiles, importantly, females and males were also significantly dissimilar within their co-twin/triplet pairs of the mixed-sex group, infants of co-twins/triplets shared more similar features than un-related infants from different twins’ pair. Future research developing personalized interventions for vulnerable high-risk infants should consider sex, and the interaction of sex and environmental factors.

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Section: Discussionmentioning

confidence: 99%

Sex Differences in Gut Microbial Development of Preterm Infant Twins in Early Life: A Longitudinal Analysis

Chen

Hird

et al. 2021

Front. Cell. Infect. Microbiol.

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“…Bacteroidetes species may play a key role in promoting neurodevelopment during a critical time in late infancy when myelination and expanded connectivity of neuronal networks normally occur; when these processes are slowed, pervasive developmental delay can result. 38,39 With successive increases to gut microbial species richness in both young and older infants, greater connectivity in brain areas that support cognitive development and language acquisition has been reported. 40,41 We observed that presence of the Bacteroidetes-cluster (with the highest species richness of Bacteroidetes), as well as higher relative abundance of genus Bacteroides at 1 year, were associated with improved neurodevelopmental outcomes.…”

Section: B Cluster-1mentioning

confidence: 99%

Bacteroides-dominant gut microbiome of late infancy is associated with enhanced neurodevelopment

et al. 2021

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Dysbiosis of gut microbiota has been retrospectively linked to autism spectrum disorders but the temporal association between gut microbiota and early neurodevelopment in healthy infants is largely unknown. We undertook this study to determine associations between gut microbiota at two critical periods during infancy and neurodevelopment in a general population birth cohort.Here, we analyzed data from 405 infants (199 females) from the CHILD (Canadian Healthy Infant Longitudinal Development) Cohort Study. Neurodevelopmental outcomes were objectively assessed using the Bayley Scale of Infant Development (BSID-III) at 1 and 2 years of age. Microbiota profiling with 16S rRNA gene sequencing was conducted on fecal samples obtained at a mean age of 4 and 12 months.Using clustering methods, we identified three groups of infants based on relative abundance of gut microbiota at 12 months: Proteobacteria-dominant cluster (22.4% higher abundance at 12 months), Firmicutes-dominant cluster (46.0% higher abundance at 12 months) and Bacteroidetes-dominant cluster (31.6% higher abundance at 12 months). Relative to the Proteobacteria-dominant cluster, the Bacteroidetes-dominant cluster was associated with higher scores for cognitive (4.8 points; FDRp = .02), language (4.2 points; FDRp≤0.001), and motor (3.1 points; FDRp = .03) development at age 2 in models adjusted for covariates. When stratified by sex, only male infants with a Bacteroidetes-dominant microbiota had more favorable cognitive (5.9 points, FDRp = .06) and language (7.9 points; FDRp≤0.001) development. Genus Bacteroides abundance in gut microbiota was positively correlated with cognitive and language scores at age 2. Fully adjusted linear mixed model analysis revealed a positive association between Bacteroidetesdominant cluster and change in cognitive and language performance from 1 to 2 years, predominantly among males. No associations were evident between 4-month microbiota clusters and BSID-II scores. Noteworthy is that enhanced sphingolipid synthesis and metabolism, and antagonism or competition between Bacteroides and Streptococcus were characteristic of a Bacteroidetes-dominant gut microbiota.This study found strong evidence of positive associations between Bacteroidetes gut microbiota in late infancy and subsequent neurodevelopment, most prominently among males but not females.

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“…More likely, an early modulation of neurodevelopment which could lead to long-term consequences on brain structure and function may be suspected. Whether early microbiota participates in the development of the central nervous system has been proposed in a series of publications and examined through the observation that key events as microglia proliferation, synaptogenesis, and pruning are impacted in germ-free mice, after antibiotics treatment or after specific fecal transplantation and result in behavioral modifications as anxiety-like symptoms, depression, or autism spectrum disorder ( Goyal et al, 2015 ; Jena et al, 2020 ; Morais et al, 2020 ). Food intake regulation is the result of complex interplays between a large number of structures; therefore, to deepen our knowledge on the impact of early microbiota transfer, we need to go further and perform a detailed anatomical, transcriptomic, and functional analysis of the brain structures (VTA, NAc, HT, and NTS) and the different element of the gut–brain communication that can be disturbed according to the existing microbiota.…”

Section: Discussionmentioning

confidence: 99%

Maternal Microbiota Transfer Programs Offspring Eating Behavior

et al. 2021

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Understanding the link between mother’s obesity and regulation of the child’s appetite is a prerequisite for the design of successful preventive strategies. Beyond the possible contributions of genetic heritage, family culture, and hormonal and metabolic environment during pregnancy, we investigate in the present paper the causal role of the transmission of the maternal microbiotas in obesity as microbiotas differ between lean and obese mothers, maternal microbiotas are the main determinants of a baby’s gut colonization, and the intestinal microbiota resulting from the early colonization could impact the feeding behavior of the offspring with short- and long-term consequences on body weight. We thus investigated the potential role of vertical transfers of maternal microbiotas in programming the eating behavior of the offspring. Selectively bred obese-prone (OP)/obese-resistant (OR) Sprague-Dawley dams were used since differences in the cecal microbiota have been evidenced from males of that strain. Microbiota collected from vagina (at the end of gestation), feces, and milk (at postnatal days 1, 5, 10, and 15) of OP/OR dams were orally inoculated to conventional Fischer F344 recipient pups from birth to 15 days of age to create three groups of pups: F-OP, F-OR, and F-Sham group (that received the vehicle). We first checked microbiotal differences between inoculas. We then assessed the impact of transfer (from birth to adulthood) onto the intestinal microbiota of recipients rats, their growth, and their eating behavior by measuring their caloric intake, their anticipatory food reward responses, their preference for sweet and fat tastes in solutions, and the sensations that extend after food ingestion. Finally, we searched for correlation between microbiota composition and food intake parameters. We found that maternal transfer of microbiota differing in composition led to alterations in pups’ gut microbiota composition that did not last until adulthood but were associated with specific eating behavior characteristics that were predisposing F-OP rats to higher risk of over consuming at subsequent periods of their life. These findings support the view that neonatal gut microbiotal transfer can program eating behavior, even without a significant long-lasting impact on adulthood microbiota composition.

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Gut-Brain Axis in the Early Postnatal Years of Life: A Developmental Perspective

Cited by 64 publications

References 249 publications

Sex Differences in Gut Microbial Development of Preterm Infant Twins in Early Life: A Longitudinal Analysis

Sex Differences in Gut Microbial Development of Preterm Infant Twins in Early Life: A Longitudinal Analysis

Bacteroides-dominant gut microbiome of late infancy is associated with enhanced neurodevelopment

Maternal Microbiota Transfer Programs Offspring Eating Behavior

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