Review Article

Review Article: Dietary Fibre in the era of Microbiome Science

John O'Grady; Eibhlís M. O'Connor; Fergus Shanahan

Disclosures

Aliment Pharmacol Ther. 2019;49(5):506-515. 

In This Article

Variability of Response to Dietary Fibre

As fibre is digested by microbes, a beneficial response to dietary fibre intervention may be dependent on the established microbiota. Diet influences which microbes colonise, flourish, retain or disappear in humans throughout life.[10,26] Long-term dietary habits with little dietary fibre intake results in diminished microbial diversity.[26,43,44] The response to increased dietary fibre intake is, therefore, not uniform and varies depending on the composition of an individual's pre-existing microbiota which is influenced by previous dietary habits.[26,43,44,45,46,47,48,49,50,51,52] Dietary and lifestyle habits of rural African children is associated with a microbiome enriched with Bacteroidetes and reduced Firmicutes phyla when compared with microbiota of European children.[53] Of the Bacteroidetes, a Prevotella-enriched microbiome is associated with higher concentrations of SCFAs due to specific enzymes for polysaccharide breakdown.[54] Furthermore, healthy subjects with improved glucose metabolism following fibre supplementation had a higher Prevotella/Bacteroides ratio than those who did not respond to increased fibre.[55]

Low-fibre diet fed to ex-germ-free mice containing a human faecal microbiome leads to progressive loss of microbial diversity, which is only partially reversible on fibre re-introduction. If this reduced microbial diversity with missing taxa is transmitted to subsequent generations, fibre re-introduction is unable to reverse these losses[56] (Figure 4). This may be of particular significance when considering dietary advice for antenatal women and to establish microbial diversity in the neonate. Further murine studies suggest impaired microbial responses to dietary intervention, reflective of previous dietary habits, may necessitate introduction of specific dietary-responsive bacteria from other individuals.[57] In pig microbiome analysis, high fibre/low-fat diet is associated with higher concentration of Bifidobacteria, Lactobacilli and Faecalibacterium prausnitzii, which have a protective role in intestinal inflammation,[58] as well as increased SCFA production.[59] In the same study, high fat/low fibre diet led to increased abundance of Enterobacteriaceae, which in humans has been associated with overweight and type 2 diabetes and includes the pathogenic strains Escherichia coli and Salmonella enterica.[59] Further evidence favouring a fibre-based diet is provided by a murine model of antibiotic-induced Clostridium difficile infection (CDI).[5] In this study, a diet deficient in fibre was linked with prolonged CDI, while addition of either inulin or a fibre mixture reduced the burden of C difficile and supported a microbial diversity favouring exclusion of C difficile.[5]

Figure 4.

Irreversible loss of microbial species with dietary fibre restriction over time and down the generations in experimental animals harbouring a human microbiome. Based on Sonnenburg et al. Nature 201656

The impact of diet also appears to be reflected in various human studies. Fibre supplementation in Canadian children resulted in significant increases in Bifidobacterium genus and a decrease in Bacteroides vulgatus, which correlated with reduced adiposity.[60] The microbiome of children from the West African country of Burkina Faso, with a fibre-rich African diet, has been compared with that of children in Italy. The microbiota of the African children had significantly higher proportions of Prevotella, Xylanibacter, Butyrivibrio and Treponema genera. These are known to contain genes for cellulose and xylan hydrolysis to maximise fermentation of dietary fibre.[53] The Hadza tribe of Tanzania, a hunter-gatherer community, have a more diverse faecal microbiome that is linked to their foraging lifestyle, compared with industrialised countries.[61] The Hadza dietary habits are similar to those of human ancestors and interestingly, their microbiome contains unclassified Bacteroidetes and Clostridiales, broadening their diversity more than their established fibre enrichment of Prevotella, Treponema and Clostridiales.[61] Compared with Italian adult microbiota, the Hadza microbiota has a higher abundance of Bacteroidetes, in particular Prevotella and less Firmicutes, consistent with how high dietary fibre intake influences the composition of the microbiome. A recent systematic review further concluded that, in healthy adults, fibre intervention, particularly with fructans and galacto-oligosaccharide, leads to increased abundance of both Bifidobacterium and Lactobacillus species.[62]

In contrast, elderly western populations have reduced gut microbial diversity which correlates significantly with nutritional status, frailty, co-morbidity, markers of inflammation and faecal water metabolites. Furthermore, a significantly less diverse microbiota is found amongst elderly subjects in long-term care facilities versus those in the community, with a less diverse diet of those in long-term care facilities at least partly implicated in the microbial species collapse.[63] It is evident that a fibre-based diet, in both animal and human studies, has favourable effects on gut microbial diversity which, in turn, influences the fermentation by-products of fibre metabolism. It remains to be determined if fibre alone is sufficient to reverse microbial collapse in humans, though current evidence would suggest that a re-introduction of specific fibre-sensitive taxa may be required in addition to high fibre diet.

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