Acquisition Of The Gut Microbiota

Acquisition of the normal microbiota is a biological succession which commences during or immediately following birth (depending on the mode of delivery). During natural birth, the neonate is exposed to the maternal microbiota, both vaginal and fecal (22-24). However, colonization is delayed in infants born via Caesarian section and the major source of inoculation is thought to be from the environment (including nosocomially from within the maternity ward) (23). Caesarean section delivery has been correlated with an increased clostridial component in the infant microbiota. Indeed, recent studies have demonstrated that higher clostridial counts in children delivered by Caesarean section relative to children delivered vaginally persist even after 7 years of age (25).

During the initial phase of acquisition, facultative anaerobes predominate (enterobacteria and streptococci) and effectively reduce the redox potential of the gut environment enabling colonization by obligate anaerobes (including bacteroides, bifidobacteria, clostridia, and eubacteria). Factors such as diet and host genetics play important roles in the development of the microbiota (with some bacterial populations eliminated and others maintained) (3,24). The classical studies by Tissier almost a century ago first highlighted the significant difference of the fecal microbiota harbored by breastfed and formula-fed infants. Indeed, Tissier described three phases of microbial acquisition in infants: 1, initial hours of life when the fecal bacterial content was nil; 2, beginning between the tenth and twentieth hour of life, comprising a heterogeneous microbiota; 3, after passage of maternal milk through the intestinal tract, the microbiota being predominated by bifidobacteria (an obligately anaerobic Gram-positive bacillus which often exhibits bifurcating morphology, formerly named Bacillus bifidus by Tissier) (3,26,27). A fourth phase, following introduction of solid foods (weaning), was later described and is characterized by modulation of the breast-fed microbiota towards an adult-type microbiota (climax community) harboring a more complex and diverse bacterial community (13,28,29). It is worth noting that Tissier also speculated that subdominant populations (including facultative anaerobes) were harbored during phase three of acquisition and that complete bacteriological examination was necessary to determine this. No doubt some such populations are then re-established as predominant members within the heterogeneous climax community through the introduction of complex carbohydrates into the diet.

Bottle-fed infants did not demonstrate the same succession of micro-organisms as seen in their breast-fed counterparts. Indeed, Tissier observed that formula-fed infants maintained a heterogeneous fecal microbiota beyond day 4. Much work has been compiled over the last 30 years comparing the fecal microbiota of exclusively milk-fed infants. Until recently, such studies were performed using traditional cultivation techniques. A range of data has accumulated and while notable differences may still be observed between breastfed and formula-fed infants, they are not as startling as those shown by Tissier. In general, the bifidobacterial microbiota, both carriage (percentage of infants harboring bifidobacteria) and population level, of exclusively milk-fed infants was not significantly different (30-33). However, levels of other organisms, notably Bacteroides, clostridia and enterobacteria, were significantly higher in formula-fed infants. Thus, breast-fed infants harbored a bifidobacterially predominant fecal microbiota, whereas formula-fed infants harbored a larger bacterial load comprising greater heterogeneity with higher levels of Bacteroides, enterobacteria and clostridia. Studies investigating the fecal microbiota of infants fed different formulae (for example, following fortification with iron and/or oligosaccharides) have shown that the constituents of the infant formulae impact upon the microbial composition (24,34). Recent studies employing molecular biological methods have further clarified the situation, demonstrating an initial diverse microbiota during the first 4-6 days of life (phase 2) followed by establishment of a bifidobacterially predominant microbiota in breast-fed infants (phase 3) which is not as obvious in formula-fed infants. Namely, bifidobacteria formed 60-91% of the bacterial composition of breast-fed infants (n = 6) and between 28 and 75% of the total microbial load of formula-fed infants (n = 6) after day six (35). Inter-individual differences were noted in both feeding groups, with respect to the relative proportions of the bacterial groups studied. Molecular characterization studies of the predominant isolates from concurrent cultivation work further highlighted the distinction between the microbiota harbored by infants [both between feeding groups and inter-individually (35)].

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