Detection of changes in regional colonic fermentation in response to supplementing a low FODMAP diet with dietary fibres by hydrogen concentrations, but not by luminal pH

Abstract

Background: Carbohydrate fermentation plays a pivotal role in maintaining colonic health with excessive proximal and deficient distal fermentation being detrimental.

Aims: To utilise telemetric gas- and pH-sensing capsule technologies for defining patterns of regional fermentation following dietary manipulations, alongside conventional techniques of measuring fermentation.

Methods: In a double-blind crossover trial, 20 patients with irritable bowel syndrome were fed low FODMAP diets that included no extra fibre (total fibre content 24 g/day), or additional poorly fermented fibre, alone (33 g/day) or with fermentable fibre (45 g/day) for 2 weeks. Plasma and faecal biochemistry, luminal profiles defined by tandem gas- and pH-sensing capsules, and faecal microbiota were assessed.

Results: Plasma short-chain fatty acid (SCFA) concentrations (μmol/L) were median (IQR) 121 (100-222) with fibre combination compared with 66 (44-120) with poorly fermented fibre alone (p = 0.028) and 74 (55-125) control (p = 0.069), but no differences in faecal content were observed. Luminal hydrogen concentrations (%), but not pH, were higher in distal colon (mean 4.9 [95% CI: 2.2-7.5]) with fibre combination compared with 1.8 (0.8-2.8) with poorly fermented fibre alone (p = 0.003) and 1.9 (0.7-3.1) control (p = 0.003). Relative abundances of saccharolytic fermentative bacteria were generally higher in association with supplementation with the fibre combination.

Conclusions: A modest increase in fermentable plus poorly fermented fibres had minor effects on faecal measures of fermentation, despite increases in plasma SCFA and abundance of fermentative bacteria, but the gas-sensing capsule, not pH-sensing capsule, detected the anticipated propagation of fermentation distally in the colon. The gas-sensing capsule technology provides unique insights into localisation of colonic fermentation.

Trial registration: ACTRN12619000691145.

Keywords: dietary fibre; fermentation; irritable bowel syndrome; microbiota; resistant starch.

FIGURE 1

Metabolite concentrations in plasma and faeces across the dietary interventions. (A) Total plasma short‐chain fatty acid (SCFA) concentration (bar as median). (B) Relative change in total plasma SCFA concentration relative to Control (mean ± SEM). (C) Total faecal SCFA concentration (bar as mean). (D) Relative change in total faecal SCFA concentration relative to Control (mean ± SEM). (E) Total faecal branched‐chain fatty acid (BCFA) concentration (bar as mean). (F) Relative change in faecal SCFA:BCFA relative to Control (mean ± SEM).

FIGURE 2

Luminal pH and hydrogen profiles across the dietary interventions. (A) Overall colonic pH (bar as mean). (B) Regional colonic pH per quartile of relative colonic transit time (bar as mean). (C) Overall colonic hydrogen concentration (% of gas detected within the lumen; bar as mean). (D) Peak hydrogen concentration (bar as mean). (E) Regional colonic hydrogen concentration per quartile of relative colonic transit time (bar as mean). (F) Time to peak hydrogen concentration relative to colonic transit time (bar as mean).

FIGURE 3

(A) Luminal pH and (B) hydrogen profiles per quartile of relative colonic transit time. Mean pH or hydrogen concentration (% of gas detected within the lumen;) per quartile shown.

FIGURE 4

Influence of three interventional diets on faecal microbiota via 16S amplicon sequencing. (A, B) Sample analysis plots for sparse partial least‐squares discriminant analysis (sPLS‐DA) projected into the first three components. (C) Clustered heatmap after sPLSDA modelling for the optimal selected features with the cell colours depicting the centred log ratio (CLR)‐transformed abundance values. (D, E) The loading values (importance) of the top 30 contributing features for the first and second components. (F) Differences in relative abundance (CLR transformed) of amplified sequence variants (ASVs), with selected boxplots on the basis of marked expansion of Ruminococcus when exposed to the sugarcane bagasse and resistant starch, but no differences in other relevant ASVs (Bifidobacterium and Bilophila). Bar lengths correspond to the importance (the multivariate regression coefficient for that particular feature on each component) of the feature in the final sPLS‐DA model (A, B).