Systematic Review of the Human Milk Microbiota

Abstract

Human milk-associated microbes are among the first to colonize the infant gut and may help to shape both short- and long-term infant health outcomes. We performed a systematic review to characterize the microbiota of human milk. Relevant primary studies were identified through a comprehensive search of PubMed (January 1, 1964, to June 31, 2015). Included studies were conducted among healthy mothers, were written in English, identified bacteria in human milk, used culture-independent methods, and reported primary results at the genus level. Twelve studies satisfied inclusion criteria. All varied in geographic location and human milk collection/storage/analytic methods. Streptococcus was identified in human milk samples in 11 studies (91.6%) and Staphylococcus in 10 (83.3%); both were predominant genera in 6 (50%). Eight of the 12 studies used conventional ribosomal RNA (rRNA) polymerase chain reaction (PCR), of which 7 (87.5%) identified Streptococcus and 6 (80%) identified Staphylococcus as present. Of these 8 studies, 2 (25%) identified Streptococcus and Staphylococcus as predominant genera. Four of the 12 studies used next-generation sequencing (NGS), all of which identified Streptococcus and Staphylococcus as present and predominant genera. Relative to conventional rRNA PCR, NGS is a more sensitive method to identify/quantify bacterial genera in human milk, suggesting the predominance of Streptococcus and Staphylococcus may be underestimated in studies using older methods. These genera, Streptococcus and Staphylococcus, may be universally predominant in human milk, regardless of differences in geographic location or analytic methods. Primary studies designed to evaluate the effect of these 2 genera on short- and long-term infant outcomes are warranted.

The Bacterial Ecosystem of Mother’s Milk and Infant’s Mouth and Gut

“…In other words, the milk ecosystem of the 36 enrolled mothers was richer and more similarly composed among samples (in terms of bacterial species) than the fecal or mouth ecosystem of their children, suggesting that the milk duct might act as an environmental filter allowing for the survival and proliferation of the same bacterial species in most individuals (a “niche-based” community assembly, according to Costello et al (2012). As expected (Fitzstevens et al, 2016), the milk ecosystem phylogenetic structure showed a slight dominance of Streptococcaceae (average rel. ab., 24.5%), with Streptococcus being the dominant genus in 53% of samples, but also a considerable representation of the typically infant fecal family Bifidobacteriaceae (11.2%, with Bifidobacterium being the dominant genus in 19% of samples) and Staphylococcaceae, which is instead a common skin and mouth inhabitant (Belkaid and Segre, 2014) (11.1%, with Staphylococcus being the dominant genus in 11% of samples) ( Figure 2 ).…”

“…Research struggles to give a conclusive demonstration for the origin of the bacteria recovered in human milk: even if a controversial “bacterial entero-mammary pathway” has been proposed (Rodríguez, 2014), contamination by the surrounding skin microbiota and other environmental sources might also occur. Indeed, facultative anaerobic or prevalently aerobic species are the major colonizers of the human milk ecosystem: Streptococcus and Staphylococcus are the most frequently isolated and abundant bacterial groups in milk samples, together with skin-derived or environmental contaminants (i.e., Propionibacterium and genera of the Enterobacteriaceae family) (Fitzstevens et al, 2016). However, well-known intestinal probiotic bacteria (i.e., Bifidobacterium and Lactobacillus ) are often retrieved by both molecular and cultivation-based studies (Fitzstevens et al, 2016).…”

“…Indeed, facultative anaerobic or prevalently aerobic species are the major colonizers of the human milk ecosystem: Streptococcus and Staphylococcus are the most frequently isolated and abundant bacterial groups in milk samples, together with skin-derived or environmental contaminants (i.e., Propionibacterium and genera of the Enterobacteriaceae family) (Fitzstevens et al, 2016). However, well-known intestinal probiotic bacteria (i.e., Bifidobacterium and Lactobacillus ) are often retrieved by both molecular and cultivation-based studies (Fitzstevens et al, 2016). Next generation sequencing also allowed the detection of obligate anaerobic, gut-associated genera, such as Bacteroides , Blautia , Dorea , and Faecalibacterium (Jost et al, 2013); if alive, these bacteria could act as pioneers in the infant gut for the construction of the adult gut microbiota, which will begin to settle down at weaning (Rodríguez, 2014).…”

Bacterial Composition and Diversity in Breast Milk Samples from Mothers Living in Taiwan and Mainland China

“…Fitzstevens et al (2016) suggested that two genera, Streptococcus and Staphylococcus , may be universally predominant in human milk, regardless of differences in geographic location or analytical methods. However, in fact, varied results for the whole microbial composition have been obtained from previous studies performed in different countries by using different subjects and different analytical methods.…”

Safety and risk assessment for the human superorganism

“…Microbial exposures during development are part of our necessary physiological/immunological maturation. For example, human breast milk itself is loaded with mutualistic, commensal, and potentially pathogenic microbes such as Streptococcus and Staphylococcus bacteria in addition to prebiotic oligosaccharides (Barile and Rastall 2013) and immune components (Fitzstevens et al 2016).…”