The Relationship Between Breast Milk Components and the Infant Gut Microbiota

Abstract

The assembly of the newborn's gut microbiota during the first months of life is an orchestrated process resulting in specialized microbial ecosystems in the different gut compartments. This process is highly dependent upon environmental factors, and many evidences suggest that early bacterial gut colonization has long-term consequences on host digestive and immune homeostasis but also metabolism and behavior. The early life period is therefore a "window of opportunity" to program health through microbiota modulation. However, the implementation of this promising strategy requires an in-depth understanding of the mechanisms governing gut microbiota assembly. Breastfeeding has been associated with a healthy microbiota in infants. Human milk is a complex food matrix, with numerous components that potentially influence the infant microbiota composition, either by enhancing specific bacteria growth or by limiting the growth of others. The objective of this review is to describe human milk composition and to discuss the established or purported roles of human milk components upon gut microbiota establishment. Finally, the impact of maternal diet on human milk composition is reviewed to assess how maternal diet could be a simple and efficient approach to shape the infant gut microbiota.

Keywords: gut microbiota; maternal diet; milk bacteria; milk lipids; milk oligosaccharides.

Figure 1

Macronutrient composition of colostrum and mature term human milk.

Figure 2

Human milk concentrations of the top human milk oligosaccharides (HMOs) over the first 4 months of lactation (n = 290 European healthy mothers), adapted from (67) and (64). [1, 2, 3, and/or 4] indicate the highest HMO concentration in milk of secretor [α1-2-fucosyltransferase FUT2 secretor (Se) gene] and Lewis [α1-3/4-fucosyltransferase FUT3; Lewis (Le) gene] groups (1, Se+Le+; 2, Se–Le+; 3, Se+Le–; 4, Se–Le–).

Figure 3

Milk microbiota major taxa and overlap with infant feces and mouth and maternal skin microbiota. Overview of milk microbiota major taxa and their possible origin [based on the reviews by Oikonomou et al. (89) and Jost et al. (90) for milk microbiota and Byrd et al. (119) and Xiao et al. (120) for maternal skin and infant oral microbiota, respectively, and based on comparative studies between microbiota associated with these different sites (–100, 106, 121)]. The taxa in bold correspond to those for which isolates have been obtained (~viable fraction of milk microbiota). ^aTaxa for which shared strains between milk and infant feces have been reported; *generally considered as a contaminant.

Figure 4

Human milk components shaping the infant gut microbiota and influence of maternal diet and nutritional status. The different components of human milk (HM) that have been shown or are suspected to influence the infant gut microbiota establishment are represented. Their size in the milk drop is proportional to their suspected role in shaping the infant gut microbiota. The influence of maternal diet or nutritional status on these HM components concentrations is depicted with arrows.