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In Vivo Effects of Einkorn Wheat (Triticum Monococcum) Bread on the Intestinal Microbiota, Metabolome, and on the Glycemic and Insulinemic Response in the Pig Model

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In Vivo Effects of Einkorn Wheat (Triticum Monococcum) Bread on the Intestinal Microbiota, Metabolome, and on the Glycemic and Insulinemic Response in the Pig Model

Francesca Barone et al. Nutrients.

Abstract

Einkorn wheat (Triticum monococcum) is characterized by high content of proteins, bioactive compounds, such as polyunsaturated fatty acids, fructans, tocols, carotenoids, alkylresorcinols, and phytosterols, and lower α-, β-amylase and lipoxygenase activities compared to polyploid wheat. These features make einkorn flour a good candidate to provide healthier foods. In the present study, we investigated the effects of einkorn bread (EB) on the intestinal physiology and metabolism of the pig model by characterizing the glycemic and insulinemic response, and the microbiota and metabolome profiles. Sixteen commercial hybrid pigs were enrolled in the study; four pigs were used to characterize postprandial glycemic and insulinemic responses and twelve pigs underwent a 30-day dietary intervention to assess microbiota and metabolome changes after EB or standard wheat bread (WB) consumption. The postprandial insulin rise after an EB meal was characterized by a lower absolute level, and, as also observed for glucose, by a biphasic shape in contrast to that in response to a WB meal. The consumption of EB led to enrichment in short-chain fatty acid producers (e.g., Blautia, Faecalibacterium, and Oscillospira) in the gut microbiota and to higher metabolic diversity with lower content of succinate, probably related to improved absorption and therefore promoting intestinal gluconeogenesis. The observed changes, at both a compositional and metabolic scale, strongly suggest that EB consumption may support a health-promoting configuration of the intestinal ecosystem.

Keywords: einkorn; glycemic response; gut metabolites; gut microbiota; insulinemic response.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Postprandial glucose and insulin responses after einkorn (EB) or wheat (WB) bread consumption in the pig model (n = 4). (A) Glucose and (B) insulin trend waves among diets (fold of increase with respect to time 0). Area under the curve (AUC) for the entire curve (C) and for the first peak (D), in the three groups (EB, 50 g of einkorn bread; WB, 50 g of wheat bread; C (control), 50 g of glucose as a reference food). * for p value < 0.05, Kruskal–Wallis test.
Figure 2
Figure 2
Modulation of the swine fecal microbiota after einkorn vs. wheat bread-based intervention. Principal Coordinate Analysis (PCoA) of unweighted (A) and weighted (B) UniFrac distances between the microbial profiles of pigs before and after 30-day consumption of einkorn (cyan, t0; blue, t30) or wheat bread (orange, t0; red, t30). A significant separation between t0 and t30 samples was found for both groups, according to both metrics (p value ≤ 0.003, permutation test with pseudo-F ratios). (C) Relative abundance of phylum-level taxa in the fecal microbiota of einkorn vs. wheat bread-fed pigs. Bars below the area chart are colored according to the diet group and time point, as in (A). (D) Genus-level signatures of response to nutritional interventions, shown as Log2 fold changes between t30 and t0 samples for the einkorn (light blue) or wheat (yellow) bread group. *, unclassified Operational Taxonomic Units (OTUs) reported at higher taxonomic level. p value < 0.05, Wilcoxon test.
Figure 3
Figure 3
Mucosa-associated microbiota from ileum and colon after einkorn vs. wheat bread-based intervention. (A) Box plots showing the distribution of alpha diversity values, according to the observed OTU metrics. Samples are identified with colored dots within boxes (orange: ileal mucosa from wheat bread (WB)-fed pigs; red, ileal mucosa from einkorn bread (EB)-fed pigs). A significant difference between diet groups was found (p-value = 0.02, Wilcoxon test). (B) Principal Coordinate Analysis (PCoA) of weighted UniFrac distances between the mucosal microbial profiles of pigs after 30-day consumption of EB (ileum, red; colon, blue) or WB (ileum, orange; colon, cyan). Ellipses include 99% confidence area based on the standard error of the weighted average of sample coordinates. Only in the ileum compartment, the mucosa-associated microbiota fractions clustered in distinct groups according to diet (p-value = 0.04, permutation test with pseudo-F ratios). (C) Relative abundance of phylum-level taxa in the ileal or colonic mucosal microbiota of EB- vs. WB-fed pigs. Bars that are below the area chart are colored according to diet and intestinal compartment, as in (B). (D) Box plots showing the distribution of the relative abundance values of discriminant taxa between the EB and WB group, at the ileum or colon level. Same color code as in (B). *, unclassified OTU reported at higher taxonomic level. p value < 0.05, Wilcoxon test.
Figure 4
Figure 4
Concentration of glucose, short-chain fatty acids (SCFAs) (acetate, butyrate, and propionate), succinate and leucine along the pig intestine. Boxplots show, for wheat (black) and einkorn (red) bread-based diets, the concentration (mmol/L) of the metabolites in feces, at t0 and t30, and in ileum and colon contents, at t30. The inserts highlight the trends at t30 significantly affected by the diets, while significance of the differences at t0 or at t30 for feces are reported over the corresponding boxes. ** p value < 0.05.
Figure 5
Figure 5
Metabolomics signatures along the pig intestine, associated with einkorn or wheat bread-based intervention. Robust principal component analysis (RPCA) models were calculated on the concentrations of significantly different molecules between the wheat (WB) and einkorn bread (EB) groups, as outlined in Supplementary Tables S5–S7, centered and scaled to unity variance. Panels (A,C,E) show the corresponding score plots, with samples from the WB group represented by black squares and samples from the EB group by red circles. The samples are connected to their median values by lines. Panels (B,D,F) show the corresponding correlation between molecules concentrations and their importance along PC 1, with dashed lines evidencing correlations lower than −0.5 and higher than 0.5. In panel (A), the samples at t0 are superimposed because their metabolome has been subtracted to the one of each sample from the same subject to consider the paired nature of the data.
Figure 6
Figure 6
Distribution of fecal volatile molecules, analyzed by gas chromatography-mass spectrometry (GC-MS), before (t0) and after (t30) einkorn (EB) vs. wheat (WB) bread-based dietary intervention.
Figure 7
Figure 7
Boxplots showing the concentrations of the main fecal volatile molecules, analyzed by GC-MS, discriminating between t0 (blue) and t30 (orange) in the einkorn (EB; Figure 7A) and wheat (WB; Figure 7B) bread-based diet groups, as determined through Random Forest. *, outliers. p values were determined by Wilcoxon test.
Figure 8
Figure 8
Boxplots showing the concentrations of the main fecal volatile molecules, analyzed by GC-MS, discriminating between the wheat (WB) and einkorn (EB) bread-based diet groups at the end of the intervention (t30), as determined through Random Forest. *, outliers. p values were determined by Wilcoxon test.

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