Human milk microbiome

The human milk microbiota refers to the community of microorganisms residing in the human mammary glands and breastmilk.[1] Human milk has been traditionally assumed to be sterile,[1][2] but more recently both culture and culture-independent techniques have confirmed that human milk contains diverse communities of bacteria which are distinct from other microbial communities inhabiting the human body.[3][4][5]

Taxonomic composition overview

Bacteria commonly isolated in human milk samples include Bifidobacterium, Lactobacillus, Staphylococcus, Streptococcus, Bacteroides, Clostridium, Micrococcus, Enterococcus, and Escherichia.[3][3][5] Metagenome analyses of human milk find it is dominated by Staphylococcus, Pseudomonas, and Edwardsiella.[6][7] The human milk microbiome likely varies by population and between individual women,[8] however, a study based on a group of U.S. women observed the same 9 bacterial taxa in all samples from all of their participants, suggesting a common "core" of the milk microbiome, at least in that population.[9] Bacterial communities of human colostrum have been reported as being more diverse than those found in mature milk.[1][10]

Origins of establishment

While the origins of the human milk microbiome are not exactly known,[1] several hypotheses for its establishment have been proposed. Bacteria present in human milk may be derived from the surrounding breast skin[11][12] or the infant's oral cavity.[9][7][13][14] Retrograde backflow during nursing or suckling may also lead to bacterial establishment in the mammary duct,[15] supported by the observation that a certain degree of flowback has been shown to occur during nursing using infrared photography[16] Alternatively, bacteria may be translocated to the mammary duct from the maternal gastrointestinal tract via an entero-mammary pathway, facilitated by dendritic cells.[2][3][17]

Factors shaping the human milk microbiome

Geographic location

Both the taxonomic composition and diversity of bacteria present in human milk likely vary by maternal geographic location,[1][8][9] however, more large-scale studies are needed to better understand variation between populations.[1]

Lactation stage

The human milk microbiome varies across lactation stage, with higher microbial diversity observed in colostrum than in mature milk.[1][10] Taxonomic composition of human milk also varies across the lactation period, initially dominated by Weisella, Leuconostoc, Staphylococcus, Streptococcus, and Lactococcus species,[10] and later composed primarily of Veillonella, Prevotella, Leptotrichia, Lactobacillus, Streptococcus, Bifidobacterium, and Enterococcus[10][18]

Human milk oligosaccharides

Human milk oligosaccharides, a primary component of human milk, are prebiotics which have been shown to promote growth of beneficial Bifidobacterium and Bacteroides species.[19][20][21]

Delivery mode

Mode of delivery may influence composition of the human milk microbiome, vaginal births being associated with high taxonomic diversity and high prevalence of Bifidobacterium and Lactobacillus, and the opposite trend being seen with Cesarean births,[10][18][22][23][24] however, no relationship between delivery mode and the maternal milk microbiome has also been observed.[25]

Gestational age

Women delivering term and preterm show differences in their milk microbiome composition, with mothers of term-births showing lower abundances of Enterococcus species and higher amounts of Bifidobacterium species in their milk than mothers of pre-term births.[18]

Maternal health

Maternal health status is associated with changes in the bacterial composition of milk. Higher maternal body mass index (BMI) and obesity are associated with changes in the levels of Bifidobacterium and Staphylococcus species and overall lower bacterial diversity.[10][26] Milk of women with celiac disease is observed to have reduced levels of Bacteroides and Bifidobacterium[27] Women who are HIV-positive show higher bacterial diversity and increased abundances of Lactobacillus in their milk than do non-HIV-positive women.[28] Mastitis has been linked to changes in human milk microbiota at the phylum level, lower microbial diversity, and decreased abundance of obligate anaerobic taxa.[29][30][7]

Antibiotic use

Maternal perinatal antibiotic use is associated with changes in the prevalence of Lactobacillus, Bifidobacterium, Staphylococcus, and Eubacterium in milk.[23][31][32]

Maternal diet

Few studies have been conducted examining the influence of maternal diet on the milk microbiome,[1] but diet is known to influence other aspects of milk composition, such as the lipid profile[33][34] which in turn could affect its microbial composition.[1] Variation in the fat and carbohydrate content of the maternal diet may influence the taxonomic composition of the milk microbiome.[35]

Social influences

Social network density of mother-infant dyads was found to be associated with increased bacterial diversity in the milk microbiome of mothers in the Central African Republic.[36]

Influences on infant health and development

Breastfeeding is thought to be an important driver of infant gut microbiome establishment.[37] The gut microbiome of breastfed infants is less diverse, contains higher amounts of Bifidobacterium and Lactobacillus species, and fewer potential pathogenic taxa than the gut microbiome of formula-fed infants.[38][39][40] Human milk bacteria may reduce risk of infection in breastfed infants by competitively excluding harmful bacteria,[41][42] and producing antimicrobial compounds which eliminate pathogenic strains,[43][44][45][41] Certain lactobacilli and bifidobacteria, the growth of which is stimulated by human milk oligosaccharides[46] contribute to healthy metabolic and immune-related functioning in the infant gut.[47][48][2][49]

Evolutionary implications

There is some indication of relationships between milk microbiota and other human milk components, including human milk oligosaccharides (HMOs), maternal cells, and nutrient profiles.[21][50] Specific bacterial genera have been shown to be associated with variation in levels of milk macronutrients such as lactose, proteins, and fats.[50] HMOs selectively facilitate growth of particular beneficial bacteria, notably Bifidobacterium species.[51][52] Furthermore, as bifidobacterial genomes are uniquely equipped to metabolize HMOs,[53] which are otherwise indigestible by enzymes of the infant gut, some have suggested a coevolutionary dynamic between HMOs and certain bacteria common in both the milk and infant gastrointestinal microbiomes.[54][55] Furthermore, relative to other mammalian milks, primate milk, particularly human milk, appears to be unique with respect to the complexity and diversity of its oligosaccharide repertoire. Human milk is typified by greater overall HMO diversity and predominance of oligosaccharides known to promote growth of Bifidobacterium in the infant gut.[56] Milk microbiota are thought to play an essential role in programming the infant immune system, and tend to reduce the risk of adverse infant health outcomes.[49] Differences in milk oligosaccharides between humans and non-human primates could be indicative of variation in pathogen exposure associated with increased sociality and group sizes.[57] Together, these observations may indicate that milk microbial communities have coevolved with their human host,[55] supported by the expectation that microbes which promote host health facilitate their own transmission and proliferation.[58]

Known comparisons to other mammalian milk microbiomes

Both human and macaque milks contains high abundances of Streptococcus and Lactobacillus bacteria, but differ in their respective relative abundances of these taxa.[59] Bacteria observed to be most common in healthy bovine milk include Ralstonia, Pseudomonas, Sphingomonas, Stenotrophomonas, Psychrobacter, Bradyrhizobium, Corynebacterium, Pelomonas, Staphylococcus, Fecalibacterium, Lachnospiraceae, Propionibacterium, Aeribacillus, Bacteroides, Staphyloccus, Streptococcus, Anaerococcus, Lactobacillus, Porphyromonas, Comamonas, Fusobacterium, and Enterococcus.[60][61][62][63]

See also

References

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  2. 1 2 3 Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM (March 2013). "The human milk microbiota: origin and potential roles in health and disease". Pharmacological Research. 69 (1): 1–10. doi:10.1016/j.phrs.2012.09.001. PMID 22974824.
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  4. ↑ Díaz-Ropero MP, Martín R, Sierra S, Lara-Villoslada F, Rodríguez JM, Xaus J, Olivares M (February 2007). "Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response". Journal of Applied Microbiology. 102 (2): 337–43. doi:10.1111/j.1365-2672.2006.03102.x. PMID 17241338.
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  6. ↑ Ward TL, Hosid S, Ioshikhes I, Altosaar I (May 2013). "Human milk metagenome: a functional capacity analysis". BMC Microbiology. 13: 116. doi:10.1186/1471-2180-13-116. PMID 23705844.
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