Goat Milk Oligosaccharides: Their Diversity, Quantity, and Functional Properties in Comparison to Human Milk Oligosaccharides

Abstract

Human milk is considered the golden standard in infant nutrition. Free oligosaccharides in human milk provide important health benefits. These oligosaccharides function as prebiotics, immune modulators, and pathogen inhibitors and were found to improve barrier function in the gut. Infant formulas nowadays often contain prebiotics but lack the specific functions of human milk oligosaccharides (hMOS). Milk from domesticated animals also contains milk oligosaccharides but at much lower levels and with less diversity. Goat milk contains significantly more oligosaccharides (gMOS) than bovine (bMOS) or sheep (sMOS) milk and also has a larger diversity of structures. This review summarizes structural studies, revealing a diversity of up to 77 annotated gMOS structures with almost 40 structures fully characterized. Quantitative studies of goat milk oligosaccharides range from 60 to 350 mg/L in mature milk and from 200 to 650 mg/L in colostrum. These levels are clearly lower than in human milk (5-20 g/L) but higher than in other domesticated dairy animals, e.g., bovine (30-60 mg/L) and sheep (20-40 mg/L). Finally, the review focuses on demonstrated and potential functionalities of gMOS. Some studies have shown anti-inflammatory effects of mixtures enriched in gMOS. Goat MOS also display prebiotic potential, particularly in stimulating growth of bifidobacteria preferentially. Although functional studies of gMOS are still limited, several structures are also found in human milk and have known functions as immune modulators and pathogen inhibitors. In conclusion, goat milk constitutes a promising alternative source for milk oligosaccharides, which can be used in infant formula.

Keywords: goat milk oligosaccharides; health benefits; prebiotics; quantitative analysis; structures.

Figure 1

Major milk components (g/L), fat, lactose, casein, and whey, in human (blue), goat (green), cow (purple) and sheep (red) milk, compiled from available literature sources.^,,−

Scheme 1. Overview of All Neutral gMOS Structures Reported in Goat Colostrum and Milk, with Relative Abundances Reported in Neutral and Acidic Pools, Respectively

The hMOS column (Y/N) indicates whether the structure has been observed in human milk. Hypothetical interactions with galectins are indicated, according to Urashima et al. Possible interaction epitopes are marked green; blocked epitopes are marked red; and gray boxes indicate uncertain interactions where exact structures are not known, with relative peak intensities in the neutral and acidic pool, respectively (on the basis of the study by Albrecht et al.).

Scheme 2. Overview of All Acidic gMOS Structures Reported in Goat Colostrum and Milk, with Relative Abundances Reported in Neutral and Acidic Pools, Respectively

The hMOS column (Y/N) indicates whether the structure has been observed in human milk. Hypothetical interactions with galectins are indicated, according to Urashima et al. Possible interaction epitopes are marked green; blocked epitopes are marked red; and gray boxes indicate uncertain interactions where exact structures are not known, with relative peak intensities in the neutral and acidic pool, respectively (on the basis of the study by Albrecht et al.).

Figure 2

Biosynthesis of neutral and acidic complex (left) human milk oligosaccharides (hMOS) and (right) goat milk oligosaccharides (gMOS). Enzymes probably involved are indicated in the human pathway. Required enzyme activities to achieve known structures are notated in the goat pathway. Iβ6GlcNAcTx refers to a potential separate enzyme as observed in marsupial lactation, capable of adding GlcNAc(β1–6) branching of 3′-GL. Main pathways and structure types are depicted in bold with thicker arrows. The human hypothetical pathway is compiled from Urashima et al., Bode et al., Blank et al., and Van Leeuwen et al. and combined with the Kyoto Encyclopedia of Genes and Genomes (KEGG) glycosphingolipid biosynthesis: lacto and neolacto series.

Figure 3

Average levels (mg/L) of 3′-SL, 6′-SL, and DSL in milk of (A) Garganica, (B) Maltese, and (C) Saanen goats over time and adapted from Claps et al.^,

Figure 4

Comparison of acidic and neutral MOS concentration levels between human (blue), goat (green), cow (purple), and sheep (red) colostrum (Col) and mature milk (Mat). For sheep colostrum, there are no data (n.d.) available. The open part of the bars shows the highest concentration level reported, and the filled part of the bars represents the lowest reported concentration.^,,,,,,,

Figure 5

Overview of relative intensities of gMOS derived from Albrecht et al. compared to hMOS in term and preterm milk derived from Austin et al. Clockwise from the top, first, acidic oligosaccharides are grouped together, presented according to relative abundance, followed by neutral oligosaccharides in order of abundance. Structures similar between human and goat milk are presented in bold, and corresponding segments are offset from the ring chart.