Contributions to human breast milk microbiome and enteromammary transfer of Bifidobacterium breve

Abstract

Increasing evidence supports the importance of the breast milk microbiome in seeding the infant gut. However, the origin of bacteria in milk and the process of milk microbe-mediated seeding of infant intestine need further elucidation. Presumed sources of bacteria in milk include locations of mother-infant and mother-environment interactions. We investigate the role of mother-infant interaction on breast milk microbes. Shotgun metagenomics and 16S rRNA gene sequencing identified milk microbes of mother-infant pairs in breastfed infants and in infants that have never latched. Although breast milk has low overall biomass, milk microbes play an important role in seeding the infant gut. Breast milk bacteria were largely comprised of Staphylococcus, Streptococcus, Acinetobacter, and Enterobacter primarily derived from maternal areolar skin and infant oral sites in breastfeeding pairs. This suggests that the process of breastfeeding is a potentially important mechanism for propagation of breast milk microbes through retrograde flux via infant oral and areolar skin contact. In one infant delivered via Caesarian section, a distinct strain of Bifidobacteria breve was identified in maternal rectum, breast milk and the infant's stool potentially suggesting direct transmission. This may support the existence of microbial translocation of this anaerobic bacteria via the enteromammary pathway in humans, where maternal bacteria translocate across the maternal gut and are transferred to the mammary glands. Modulating sources of human milk microbiome seeding potentially imply opportunities to ultimately influence the development of the infant microbiome and health.

Breast Milk, a Source of Beneficial Microbes and Associated Benefits for Infant Health

“…More recently, Kordy et al used shotgun metagenomics to identify a distinct Bifidobacterium breve strain in the mother's rectum, breast milk, and infant gut. Therefore, this study may support the hypothesis of entero-mammary pathway, allowing for the transport of Bifidobacteriium breve from maternal gut to the mammary gland [232].…”

Antibiotics and the developing intestinal microbiome, metabolome and inflammatory environment: a randomized trial of preterm infants

“…Our results confirm that feeding type also have a significant influence on gut microbiome richness, diversity and bacterial load 31–33 . Exclusive or partial feeding with mother’s own milk tended to associate with high bacterial load, which is supported by evidence that breast milk harbors maternal-originating bacteria, as well as nutritional components (prebiotics) that support bacterial proliferation in the intestinal tract 34,35 . Interestingly, formula-fed infants had comparable levels of richness, diversity and bacterial load as mother’s milk.…”

Analysis of the Human Breast Milk Microbiome and Bacterial Extracellular Vesicles in Healthy Mothers

“…It has been suggested that commensal bacteria from maternal skin (such as Staphylococcus, Corynebacterium, and Cutibacterium) or the infant's mouth (such as Streptococcus) can enter the mammary duct during breastfeeding [32]. Another hypothesis is that the maternal gut bacteria enter the mammary glands through the entero-mammary pathway, which would require the cells to penetrate the intestinal epithelium and reach the mammary glands through the bloodstream [33][34][35]. The observation that anaerobic bacteria such as Bacteroides, Bifidobacterium, Parabacteroides, and Clostridium that are not found on the skin are detected and shared between HBM and infant feces supports this hypothesis.…”

“…We especially highlighted Bifidobacterium, as the gut microbiota of infant feces usually exhibits high abundance of this bacterium, with exclusively breastfeeding infants in particular exhibiting relatively abundant Bifidobacterium in the feces [36,37]. [35,36]. Several lines of evidence suggest that the relative level of Bifidobacterium abundance correlates with the development of disease or immunity.…”