Effects of dietary caprine milk oligosaccharides enriched fraction on maternal large intestine and the consequences for the development of the offspring : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy, Massey University, Palmerston North, New Zealand
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2015
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Massey University
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Abstract
The colonisation of the neonate gastrointestinal tract by health-promoting microbiota is likely
to improve the overall health of the infant and may also have health benefits in later life.
Initial development and maturation of the foetal/neonatal gastrointestinal tract is heavily
influenced by the in utero environment which itself, may be altered by the maternal diet and
gastrointestinal tract microbiota composition. The maternal gastrointestinal tract microbiota
can be altered by supplementation with synthetic oligosaccharides; however, positive effects
on the health and well-being of the offspring have not been adequately established. Human
milk contains natural oligosaccharides known to improve the gastrointestinal tract
colonisation and the development and maturation of the infant gastrointestinal tract. Among
domestic farm animals, caprine milk has oligosaccharides structurally similar to human milk
and potentially similar beneficial effects for the infant. We hypothesised that feeding caprine
milk oligosaccharide enriched product to pregnant and lactating mice would induce changes
in the maternal large intestine microbiota and milk composition, accelerating the
development and maturation of the offspring’s large intestine tissue and altering the
gastrointestinal tract microbiota composition. The aim of this project was to obtain
bifidobacteria from the faeces of breast-fed human infants and determine which were of
capable fermenting caprine milk oligosaccharide enriched product. Subsequently, the effects
of the best strains on the morphology and metabolic pathways of the colonic mucosa of
germ-free and conventionally raised mice, supplemented with dietary caprine milk
oligosaccharide enriched product.
The present study is the first to report New Zealand Saanen caprine colostrum, milk and
whey. An enrichment method previously described was used to produce a caprine milk
oligosaccharide enriched product for in vitro and in vivo assessment of its health effects.
Caprine milk oligosaccharide enriched product was shown to differentially stimulate the
growth of bifidobacteria, commonly found in the gastrointestinal tract of breast-fed infants.
Among the bifidobacterial species tested, Bifidobacterium bifidum utilised caprine milk
oligosaccharide enriched product most efficiently when compared to Bifidobacterium breve
and Bifidobacterium longum subsp. longum. B. bifidum (AGR2166) was shown to ferment
the sialyloligosaccharides, 3’- and 6’-sialyl-lactose present in caprine milk oligosaccharide
enriched product through cell-associated sialidase expression. Augmented microbial
biomass associated with enhanced growth and in vitro fermentation of caprine milk
oligosaccharide enriched product, increased the production of microbial fermentation end
products such as acetate and lactate. These findings indicate that in vivo caprine milk
oligosaccharide enriched product may stimulate the growth and fermentation of
bifidobacteria within the gastrointestinal tract.
Germ-free mice or mice mono-associated with B. bifidum (AGR2166) were used to test the
in vivo effects of maternal caprine milk oligosaccharide enriched product consumption during
pregnancy and the effects on the foetus. Caprine milk oligosaccharide enriched product diet
showed no effects on maternal gastrointestinal tract or foetal growth regardless of microbial
status. Mice inoculated with B. bifidum (AGR2166) and fed caprine milk oligosaccharide
enriched product diet, however, showed an increased bacterial translocation from maternal
gastrointestinal tract to organs and placenta (inferred by the presence of the bifidobacteria
16S rRNA gene in the maternal organs). Increased translocation of commensal bacteria
from maternal gastrointestinal tract to the foetus may have important effects on foetal
immunological programming.
The consumption of caprine milk oligosaccharide enriched product, during gestation and
lactation were also tested in conventional rodents and it had no effects on maternal
gastrointestinal tract microbiota and morphology. Changes on maternal lipid metabolism and
increased maternal milk protein, however, were observed. These modifications may have
positively affected the development of the pups, relative abundance of gastrointestinal tract
bifidobacteria and butyric acid production at weaning. Important changes in the plasma and
urine metabolites involved in bile acid and fatty acid metabolism were also observed in the
pups as a consequence of maternal caprine milk oligosaccharide-enriched diet. The effects
of maternal caprine milk oligosaccharide enriched product diet on pups, were no longer
apparent after 30 days of consuming a control diet post-weaning, however, detrimental
physiological characteristics such as an increased body fat were observed. Further studies,
are needed to understand the physiological effects of caprine milk oligosaccharides on the
maternal/infant pair.
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Keywords
Goat milk, Oligosaccharides, Caprine milk, Goat milk composition, Bifidobacterium bifidum