Human Milk Microbiota: Origin and Potential Uses

Summary

The mucosa or epithelial surfaces from diverse human organs that are in direct contact with the host environment (e.g., lungs or mammary glands) had traditionally been considered to be sterile under physiological conditions. At the beginning of the XXI century, microbiological studies on human milk switched from considering it a potential vehicle for pathogens to describing the existence of its own microbiota.

The human milk microbiota in hygienically collected samples from healthy women contains a relatively low bacterial load which is dominated by Staphylococcus (mainly S. epidermidis and other coagulase-negative species), Streptococcus (from S. mitis and salivarius groups), Coryne bacterium, Propionibacterium, and other gram-positive bacteria, including Lactobacillus and Bifidobacterium [1]. It is also possible to detect DNA from strict anaerobic bacteria in human milk, but not viable bacterial cells, as they cannot be grown using conventional culture techniques.

However, when the milk is collected by pumping, a high concentration of
contamination or Stenotrophomonas) and yeasts may arise from the rinsing water and/or poor hygienic manipulation practices. Culture-independent techniques also reveal the presence of contaminant DNA of bacteria typically associated to soil arising from molecular-biological reagents (i.e., Acinetobacter, Methylobacterium, Pseudomonas, Sphingobium Sphingomonas, Stenotro­ phomonas, or Xanthomonas).

Although the human milk microbiome may be influenced by several factors, the exact triggers or drivers of differences in the composition of the human milk microbiota/microbiome need to be elucidated in the future. Colostrum and milk bacteria are among the first colonizers of the infant gut and, therefore, may play a key role in driving the development of its microbiota. A vertical mother-infant transfer of human milk micro-organisms has been proven using both culture-dependent and -independent techniques. However, studies dealing with the potential functions of such microbiota are scarce. In fact, the complex composition of human

milk, including nutrients, bioactive molecules, and cells that may act synergistically, makes it difficult to delimit the specific functions of human milk microbiota. Despite this, several studies, including clinical trials, have shown the ability of bacteria isolated from human milk to inhibit a wide range of pathogenic bacteria by different mechanisms and to reduce the incidence of gastrointestinal and upper respiratory tract infections in infants.

Human milk bacteria may participate in the correct maturation of the infant immune system by modulating both innate and acquired immune responses and enhancing tolerance mechanisms (Fig. 1). Some human milk strains colonize and are metabolically active in the infant intestine.

Although Lactobacillus and Bifidobacterium have attracted much attention from scientists and industries, some staphylococcal and streptococcal strains, which are dominant in human milk, may play important empirical probiotic roles in the breastfed infant.

A well-balanced human milk microbiota is also relevant for maternal breast health. Mastitis, a mammary bacterial dysbiosis, is mostly caused by various bacterial species showing antibiotic resistance and the ability to form biofilms. Probiotic treatment using strains isolated from human milk is a promising alternative or complement to antibiotic therapy in the prevention or treatment of mastitis.

The origin of the bacteria present in human milk still remains largely unknown and is a subject of scientific controversy. The infant’s oral cavity and the maternal skin, particularly the external surfaces closer to the exit point of milk, may provide bacteria to milk. Additionally, selected bacteria of the maternal digestive microbiota may access the mammary glands through oral- and enteromammary pathways [2]. Mononuclear
cells may be involved in the transport of intestinal bacteria to the mammary glands. The existence of such bacterial oral- and enteromammary pathways would provide new opportunities for manipulating maternal- fetal microbiota, reducing the risk of preterm birth or infant diseases [3].

References
1 Fernández L, Langa S, Martín V, et al: The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 2013;69:1–10.
2 Mira A, Rodríguez JM: The origin of human milk bacteria; in McGuire M, McGuire
MA, Bode L (eds): Prebiotics and Probiotics in Human Milk: Origins and Functions of Milk-Borne Oligosaccharides and Bacteria. London, Academic Press, 2016, pp 349–364.
3 Martín R, Langa S, Reviriego C, et al: Human milk is a source of lactic acid bacteria
for the infant gut. J Pediatr 2003;143:754–758.