The Microbiota of the Human Mammary Ecosystem

Abstract

Human milk contains a dynamic and complex site-specific microbiome, which is not assembled in an aleatory way, formed by organized microbial consortia and networks. Presence of some genera, such as Staphylococcus, Streptococcus, Corynebacterium, Cutibacterium (formerly known as Propionibacterium), Lactobacillus, Lactococcus and Bifidobacterium, has been detected by both culture-dependent and culture-independent approaches. DNA from some gut-associated strict anaerobes has also been repeatedly found and some studies have revealed the presence of cells and/or nucleic acids from viruses, archaea, fungi and protozoa in human milk. Colostrum and milk microbes are transmitted to the infant and, therefore, they are among the first colonizers of the human gut. Still, the significance of human milk microbes in infant gut colonization remains an open question. Clinical studies trying to elucidate the question are confounded by the profound impact of non-microbial human milk components to intestinal microecology. Modifications in the microbiota of human milk may have biological consequences for infant colonization, metabolism, immune and neuroendocrine development, and for mammary health. However, the factors driving differences in the composition of the human milk microbiome remain poorly known. In addition to colostrum and milk, breast tissue in lactating and non-lactating women may also contain a microbiota, with implications in the pathogenesis of breast cancer and in some of the adverse outcomes associated with breast implants. This and other open issues, such as the origin of the human milk microbiome, and the current limitations and future prospects are addressed in this review.

Human Milk Virome Analysis: Changing Pattern Regarding Mode of Delivery, Birth Weight, and Lactational Stage

“…This is a detailed metagenomic study of the HM virome in which we first demonstrated the impact of the delivery mode, prematurity, birth weight for gestational age, and lactation period (transient or mature milk) on the composition of HM viruses. We detected viruses (bacteriophages and eukaryotic viruses) in 92.0% of all HM samples, and, as in other HM microbiome studies, the virome composition was distinguished by certain interindividual variability; each mother harbored a morphologically distinct bacteriophage population [ 8 ]. Viromes have been found in the gut, skin, respiratory tract, blood, and cerebrospinal fluid.…”

“…Bacteriophage predominance also varies according to preterm birth, mode of delivery, and birth weight for gestational age. Both pathogenic and non-pathogenic viruses (HIV, cytomegalovirus, Ebola, and Zika) can be transmitted to infants through HM [ 8 , 9 , 17 , 28 ]. Pannaraj et al [ 16 ] analyzed the HM virome and found that bacteriophages ( Myoviridae, Siphoviridae, and Podoviridae families) made up a substantial part (95%) of the viruses present in HM, with only a few eukaryotic viruses.…”

“…The mother’s geographical location might also play a direct or indirect role in the HM microbiota composition. The influence of lifestyle, maternal diet, and environment on the composition of the HM microbiota has been suggested [ 2 , 8 ]. Recently, Maqsood et al [ 30 ] found that cytomegalovirus (found in 98% of human milk samples) dominated the HM virome of HIV-positive mothers in Kenya, with the bacteriophage families Myoviridae , Siphoviridae , and Podoviridae ; virome profiles and diversity were not substantially altered by HIV immunosuppression or associated with infant mortality.…”

“…Changes in the microbial composition during this period can affect health later in life [ 2 ]. The HM microbiota is a significant source of microbes that colonize the infant gut early in life, promote the growth of beneficial microbiota, aid in the maturation of the innate and adaptive immune systems, provide protection against gastrointestinal infections, and may help to form both short- and long-term infant health outcomes through metabolic programming, immunomodulation, and neuromodulation [ 4 , 5 , 6 , 7 , 8 ]. Breastfeeding affects the regulation of intestinal, neurological, and behavioral functions via the gut–brain axis in early life, which may imprint on the central nervous system and immune system throughout the lifespan.…”

The Gut‒Breast Axis: Programming Health for Life

“…In the last 20 years, several studies have shown that human milk harbors a low biomass microbiota under physiological conditions and that milk, maternal feces, and/or infant feces share some bacteria [ 24 , 140 , 141 , 142 , 143 ]. The ultimate origin (skin, oro-nasopharynx, gastrointestinal tract, vagina) of the microbes present in human milk is difficult to elucidate because of the complex and dynamic interactions between different body locations of the mother‒infant dyad.…”