Strong Multivariate Relations Exist Among Milk, Oral, and Fecal Microbiomes in Mother-Infant Dyads During the First Six Months Postpartum

Abstract

Background Neonatal gastrointestinal (GI) bacterial community structure may be related to bacterial communities of the mother, including those of her milk. However, very little is known about the diversity in and relationships among complex bacterial communities in mother-infant dyads. Objective Our primary objective was to assess whether microbiomes of milk are associated with those of oral and fecal samples of healthy lactating women and their infants. Methods Samples were collected 9 times from day 2 to 6 mo postpartum from 21 healthy lactating women and their infants. Milk was collected via complete breast expression, oral samples via swabs, and fecal samples from tissue (mothers) and diapers (infants). Microbiomes were characterized using high-throughput sequencing of the 16S ribosomal RNA (rRNA) gene. Alpha and beta diversity indices were used to compare microbiomes across time and sample types. Membership and composition of microbiomes were analyzed using nonmetric multidimensional scaling and canonical correlation analysis (CCA). The contribution of various bacterial communities of the mother-infant dyad to both milk and infant fecal bacterial communities were estimated using SourceTracker2. Results Bacterial community structures were relatively unique to each sample type. The most abundant genus in milk and maternal and infant oral samples was Streptococcus (47.1% ± 2.3%, 53.9% ± 1.3%, and 69.1% ± 1.8%, respectively), whereas Bacteroides were predominant in maternal and infant fecal microbiomes (22.9% ± 1.3% and 21.4% ± 2.4%, respectively). The milk microbiome was more similar to the infant oral microbiome than the infant fecal microbiome. However, CCA suggested strong associations between the complex microbial communities of milk and those of all other sample types collected. Conclusions These findings suggest complex microbial interactions between breastfeeding mothers and their infants and support the hypothesis that variation in the milk microbiome may influence the infant GI microbiome.

Milk Microbiota: What Are We Exactly Talking About?

“…With milk now being regarded as an inoculum for the infant GIT, the existence of an enteromammary route has been explored. Although milk and maternal feces microbiota are distinct, a strong correlation has been reported between them (Williams et al, 2019). The isolation of a common strain of the obligate anaerobe Bifidobacterium longum from maternal and neonate feces as well as from milk supports the hypothesis of an enteromammary route (Jost et al, 2014).…”

“…Shared genera between mother's milk and infant feces accounted for 70-88% of the relative abundance of fecal microbiota (Murphy et al, 2017). Contribution of milk microbiota to infant gastrointestinal microbiota was also pointed out by Williams et al (2019), who estimated a direct contribution of ∼4.9% and suggested additional contribution through a probable effect on the microbiota present in the stomach, small intestine, and upper large intestine. Likewise, in a metagenomic study, Pärnänen et al (2018) reported that 76% of the species found in milk were present in the infant's GIT.…”

“…Some retrograde flow back into the mammary ducts can occur during suckling or mechanical milking (Ramsay et al, 2004). Williams et al (2019) estimated the infant oral microbiota contributed to milk microbiota to be ∼21% at day 2 and 66% at month 5. Of course, milk can also provide bacteria to the oral cavity of the baby or the offspring.…”

“…The infant gastrointestinal microbiota colonization has long been regarded as the sole result of environmental contributions, resulting from the vaginal passage, the mother-child skin contacts, and newborn's environment. Human milk microbiota is now also considered as a reservoir of microbes for gastrointestinal colonization in newborns (Jost et al, 2014;Williams et al, 2019). This is supported by the significant overlap between infant feces and mother milk bacterial compositions.…”

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

“…Furthermore, bacteria from breast milk could be influenced by the infant oral cavity, where studies have reported, via ultrasound imaging, retrograde back flow of milk due to infant suckling. This back flow of milk into the mammary ducts provides one possible mechanism detailing the transfer of bacteria from infant's mouth into the mother's mammary gland [214][215][216]. Additionally, it was suggested that breast pump expression could influence the microbiome, proposing the pump could play a potential role in retrograde of exogenous bacteria into the milk ducts [217,218].…”