Role of the Human Breast Milk-Associated Microbiota on the Newborns’ Immune System: A Mini Review

Toscano, Marco; Grandi, Roberta De; Grossi, Enzo; Drago, Lorenzo

doi:10.3389/fmicb.2017.02100

Cited by 109 publications

(110 citation statements)

References 39 publications

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“…Breast milk also supports the initial intestinal colonization in early life [51]. In the present study, the rat milk microbiota was vastly dominated by Proteobacteria and Firmicutes, similarly to human breast milk [33].…”

Section: Discussionsupporting

confidence: 60%

Associations of Breast Milk Microbiota, Immune Factors, and Fatty Acids in the Rat Mother–Offspring Pair

et al. 2020

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The present study aimed to analyze the rat breast milk profile of fatty acids (FA), immunoglobulins (Ig), microbiota, and their relationship, and to further assess their associations in the mother–offspring pair. Dams were monitored during the three weeks of gestation, allowed to deliver at term, and followed during two weeks of lactation. At the end of the study, milk was obtained from the dams for the analysis of fatty acids, microbiota composition, immunoglobulins, and cytokines. Moreover, the cecal content and plasma were obtained from both the dams and pups to study the cecal microbiota composition and the plasmatic levels of fatty acids, immunoglobulins, and cytokines. Rat breast milk lipid composition was ~65% saturated FA, ~15% monounsaturated FA, and ~20% polyunsaturated FA. Moreover, the proportions of IgM, IgG, and IgA were ~2%, ~88%, and ~10%, respectively. Breast milk was dominated by members of Proteobacteria, Firmicutes, and Bacteroidetes phyla. In addition, forty genera were shared between the milk and cecal content of dams and pups. The correlations performed between variables showed, for example, that all IgGs subtypes correlated between the three compartments, evidencing their association in the mother-milk-pup line. We established the profile of FA, Ig, and the microbiota composition of rat breast milk. Several correlations in these variables evidenced their association through the mother-milk-pup line. Therefore, it would be interesting to perform dietary interventions during pregnancy and/or lactation that influence the quality of breast milk and have an impact on the offspring.

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Section: Discussionsupporting

confidence: 60%

Associations of Breast Milk Microbiota, Immune Factors, and Fatty Acids in the Rat Mother–Offspring Pair

et al. 2020

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“…As we previously reported, C. difficile was associated with lower sIgA concentrations among EBF infants (p = 0.047, Figure 3) (11). Since infant secretion of sIgA has been positively correlated with breastmilk sIgA levels and breastmilk microbiota, maternal factors may contribute to lower concentrations in the infant (35,36). Notably, animal models have shown that offspring nursed by mothers who are sIgA-deficient have a different gut microbiota composition than those receiving sIgA through breastmilk (37,38).…”

Section: Resultsmentioning

confidence: 51%

“…Similar to what we observed in EBF C. difficile positive infants, reduced fecal sIgA was associated with compositional differences that included an increased relative abundance of Lachnospiraceae and pro-inflammatory microbiota. Previous work from the CHILD Cohort Study has shown that sIgA in breastmilk may be depleted due to factors such as depression (21) or an altered maternal milk microbiota (36), which may predispose the infant to colonization by C. difficile and related dysbiosis. Although sIgA can bind enteric pathogens (34), there is a lack of evidence suggesting that C. difficile contributes to the destruction of sIgA or reduce production of this protein.…”

Section: Resultsmentioning

confidence: 99%

Clostridioides difficile Colonization Is Differentially Associated With Gut Microbiome Profiles by Infant Feeding Modality at 3–4 Months of Age

et al. 2019

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Colonization with Clostridioides difficile occurs in up to half of infants under the age of 3 months, is strongly influenced by feeding modality and is largely asymptomatic. In spite of this, C. difficile's presence has been associated with susceptibility to chronic disease later in childhood, perhaps by promoting or benefiting from changes in infant gut microbiome development, including colonization with pathogenic bacteria and disrupted production of microbial bioactive metabolites and proteins. In this study, the microbiomes of 1554 infants from the CHILD Cohort Study were described according to C. difficile colonization status and feeding mode at 3-4 months of age. C. difficile colonization was associated with a different gut microbiome profile in exclusively breastfed (EBF) vs. exclusively formula fed (EFF) infants. EBF infants colonized with C. difficile had an increased relative abundance of Firmicutes and Proteobacteria, decreased relative abundance of Bifidobacteriaceae, greater microbiota alpha-diversity, greater detectable fecal short chain fatty acids (SCFA), and lower detectable fecal secretory Immunoglobulin A (sIgA) than those not colonized. Similar but less pronounced differences were seen among partially breastfed infants (PBF) but EFF infants did not possess these differences in the gut microbiome according to colonization status. Thus, breastfed infants colonized with C. difficile appear to possess a gut microbiome that differs from non-colonized infants and resembles that of EFF infants, but the driving force and direction of this association remains unknown. Understanding these compositional differences as drivers of C. difficile colonization may be important to ensure future childhood health.

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“…Furthermore, breastfed infants showed a longer period of pulmonary health and stability prior to their first pulmonary exacerbation, with 20% of breastfed children having no exacerbation over the first 30 months of life, in contrast to exclusively formula-fed infants, all of whom experienced CF exacerbations by 9 months (8). Given the impact of breastfeeding on intestinal microbiota composition (16)(17)(18), one possible explanation for these findings in CF is an effect of intestinal bacterial communities on airway disease outcomes. Consistent with this idea, a previous analysis of a subset of subjects from our cohort (aged 0 to 34 months) showed that community composition in the intestine, rather than the airway microbiota, was significantly associated with pulmonary exacerbations prior to age 6 months (8).…”

mentioning

confidence: 99%

Altered Stool Microbiota of Infants with Cystic Fibrosis Shows a Reduction in Genera Associated with Immune Programming from Birth

et al. 2019

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Previous work from our group indicated an association between the gastrointestinal microbiota of infants with cystic fibrosis (CF) and airway disease in this population. Here we report that stool microbiota of infants with CF demonstrates an altered but largely unchanging within-individual bacterial diversity (alpha diversity) over the first year of life, in contrast to the infants without CF (control cohort), which showed the expected increase in alpha diversity over the first year. The beta diversity, or between-sample diversity, of these two cohorts was significantly different over the first year of life and was statistically significantly associated with airway exacerbations, confirming our earlier findings. Compared with control infants, infants with CF had reduced levels of Bacteroides, a bacterial genus associated with immune modulation, as early as 6 weeks of life, and this significant reduction of Bacteroides spp. in the cohort with CF persisted over the entire first year of life. Only two other genera were significantly different across the first year of life: Roseburia was significantly reduced and Veillonella was significantly increased. Other genera showed differences between the two cohorts but only at selected time points. In vitro studies demonstrated that exposure of the apical face of polarized intestinal cell lines to Bacteroides species supernatants significantly reduced production of interleukin 8 (IL-8), suggesting a mechanism whereby changes in the intestinal microbiota could impact inflammation in CF. This work further establishes an association between gastrointestinal microbiota, inflammation, and airway disease in infants with CF and presents a potential opportunity for therapeutic interventions beginning in early life. IMPORTANCE There is growing evidence for a link between gastrointestinal bacterial communities and airway disease progression in CF. We demonstrate that infants with CF ≤1 year of age show a distinct stool microbiota versus that of control infants of a comparable age. We detected associations between the gut microbiome and airway exacerbation events in the cohort of infants with CF, and in vitro studies provided one possible mechanism for this observation. These data clarify that current therapeutics do not establish in infants with CF a gastrointestinal microbiota like that in healthy infants, and we suggest that interventions that direct the gastrointestinal microbiota closer to a healthy state may provide systemic benefits to these patients during a critical window of immune programming that might have implications for lifelong health.

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Role of the Human Breast Milk-Associated Microbiota on the Newborns’ Immune System: A Mini Review

Cited by 109 publications

References 39 publications

Associations of Breast Milk Microbiota, Immune Factors, and Fatty Acids in the Rat Mother–Offspring Pair

Associations of Breast Milk Microbiota, Immune Factors, and Fatty Acids in the Rat Mother–Offspring Pair

Clostridioides difficile Colonization Is Differentially Associated With Gut Microbiome Profiles by Infant Feeding Modality at 3–4 Months of Age

Altered Stool Microbiota of Infants with Cystic Fibrosis Shows a Reduction in Genera Associated with Immune Programming from Birth

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