Microbial Community Dynamics in Mother’s Milk and Infant’s Mouth and Gut in Moderately Preterm Infants

Abstract

Mother’s own milk represents the optimal source for preterm infant nutrition, as it promotes immune defenses and gastrointestinal function, protects against necrotizing enterocolitis, improves long-term clinical outcome and is hypothesized to drive gut microbiota assembly. Preterm infants at birth usually do not receive their mother’s milk directly from the breast, because active suckling and coordination between suckling, swallowing and breathing do not develop until 32–34 weeks gestational age, but actual breastfeeding is usually possible as they grow older. Here, we enrolled moderately preterm infants (gestational age 32–34 weeks) to longitudinally characterize mothers’ milk and infants’ gut and oral microbiomes, up to more than 200 days after birth, through 16S rRNA sequencing. This peculiar population offers the chance to disentangle the differential contribution of human milk feeding per se vs. actual breastfeeding in the development of infant microbiomes, that have both been acknowledged as crucial contributors to short and long-term infant health status. In this cohort, the milk microbiome composition seemed to change following the infant’s latching to the mother’s breast, shifting toward a more diverse microbial community dominated by typical oral microbes, i.e., Streptococcus and Rothia. Even if all infants in the present study were fed human milk, features typical of healthy, full term, exclusively breastfed infants, i.e., high percentages of Bifidobacterium and low abundances of Pseudomonas in fecal and oral samples, respectively, were detected in samples taken after actual breastfeeding started. These findings underline the importance of encouraging not only human milk feeding, but also an early start of actual breastfeeding in preterm infants, since the infant’s latching to the mother’s breast might constitute an independent factor helping the health-promoting assembly of the infant gut microbiome.

Microbial Communities in Human Milk Relate to Measures of Maternal Weight

“…While the average abundance of these four microbes are similar across all samples, two clusters each were characterized by higher abundances of Streptococcus and Staphylococcus, or Pseudomonas and Acinetobacter with differences in alpha diversity and the abundances of numerous other taxa further differentiating these clusters. The clusters we identified share both similarities and differences with the breast milk microbiome clusters identified in Chinese (Li et al, 2017), Italian (Biagi et al, 2018), and Canadian (Moossavi et al, 2019b) mothers, suggesting that some patterns of microbial populations in human milk may be similar amongst geographically and racially distinct populations. Bacteria belonging to the genera Acinetobacter and Pseudomonas are often thought of as pathogens contributing to nosocomial infections (Fazeli et al, 2012;Custovic et al, 2014).…”

“…Preliminary small studies using 16S rRNA gene sequencing and metagenomics approaches to assess breast milk microbial composition have reported that Streptococcus, Staphylococcus, Pseudomonas, Bacteroides, Acinetobacter, and others comprise the core breast milk microbiome, whereas Bifidobacterium and Lactobacillus abundances are comparatively low (Hunt et al, 2011;Jost et al, 2013;Ward et al, 2013;Jiménez et al, 2015;Sakwinska et al, 2016;Urbaniak et al, 2016;Murphy et al, 2017). Clusters of breast milk microbiota have been reported, often defined by the abundance of Staphylococcus, Streptococcus, and Pseudomonas, Enterobacteriaceae, and other rarer bacteria (Li et al, 2017;Biagi et al, 2018;Moossavi et al, 2019b).…”

“…Other important factors to the human milk microbiome have been identified, including the method of feeding, likely due to microbes from the infant oral cavity being transferred to the breast during feeding or microbes derived from the breast pump contaminating pumped milk. In a study of preterm infant-mother pairs, the microbial composition of breast milk changed after infants began direct feeding by latching (Biagi et al, 2018). Further, milk samples from mothers who sometimes fed infants indirectly via pumped milk show decreased alpha diversity, reduced prevalence of Bifidobacterium, and increased levels of Enterobacteriaceae and Pseudomonadaceae (Moossavi et al, 2019b).…”

Human Milk’s Hidden Gift: Implications of the Milk Microbiome for Preterm Infants’ Health

“…As for the degree of premature delivery, a progressive increase in total bacterial count appears to be associated with increasing length of gestation [38]. In the two studies by Biagi et al [25,28], examining two distinct cohorts of term-delivering vs. moderately preterm-delivering mothers from the same study site, the differences in HMM were significant, especially when HM samples collected in the first few days after delivery from mothers of preterm infants were compared to those from mothers of term infants. Nonetheless, differences between the two cohorts appeared to decrease when moderately preterm infants started to be fed directly at their mothers' breast, strengthening the hypothesis of a direct influence of breastfeeding on HMM composition.…”

“…These observations document the presence in human colostrum, before delivery, of bacteria which are typical of the infants' mouth; this supports the hypothesis of a direct colonization of the infant's mouth through breastfeeding, as part of a dynamic cycle with a bidirectional flow of bacteria between the mother and the infant during suckling. In a prospective study, Biagi et al recruited a cohort of HM-fed moderately preterm infants (gestational age 32-34 weeks) and examined their mother's milk microbiota before and after the beginning of actual breastfeeding [28]. The infant's latching to the mother's breast produced an increase in HMM diversity and a shift in its composition, characterised by the dominance of typical oral microbes, such as Streptococcus and Rothia.…”