Substituting whole grains for refined grains in a 6-wk randomized trial has a modest effect on gut microbiota and immune and inflammatory markers of healthy adults

Abstract

Background: Observational studies suggest an inverse association between whole-grain (WG) consumption and inflammation. However, evidence from interventional studies is limited, and few studies have included measurements of cell-mediated immunity.Objective: We assessed the effects of diets rich in WGs compared with refined grains (RGs) on immune and inflammatory responses, gut microbiota, and microbial products in healthy adults while maintaining subject body weights.Design: After a 2-wk provided-food run-in period of consuming a Western-style diet, 49 men and 32 postmenopausal women [age range: 40-65 y, body mass index (in kg/m2) <35] were assigned to consume 1 of 2 provided-food weight-maintenance diets for 6 wk.Results: Compared with the RG group, the WG group had increased plasma total alkyresorcinols (a measure of WG intake) (P < 0.0001), stool weight (P < 0.0001), stool frequency (P = 0.02), and short-chain fatty acid (SCFA) producer Lachnospira [false-discovery rate (FDR)-corrected P = 0.25] but decreased pro-inflammatory Enterobacteriaceae (FDR-corrected P = 0.25). Changes in stool acetate (P = 0.02) and total SCFAs (P = 0.05) were higher in the WG group than in the RG group. A positive association was shown between Lachnospira and acetate (FDR-corrected P = 0.002) or butyrate (FDR-corrected P = 0.005). We also showed that there was a higher percentage of terminal effector memory T cells (P = 0.03) and LPS-stimulated ex vivo production of tumor necrosis factor-α (P = 0.04) in the WG group than in the RG group, which were positively associated with plasma alkylresorcinol concentrations.Conclusion: The short-term consumption of WGs in a weight-maintenance diet increases stool weight and frequency and has modest positive effects on gut microbiota, SCFAs, effector memory T cells, and the acute innate immune response and no effect on other markers of cell-mediated immunity or systemic and gut inflammation. This trial was registered at clinicaltrials.gov as NCT01902394.

Keywords: gut microbiota; healthy adults; immune; inflammation; whole grains.

© 2017 American Society for Nutrition.

Figures

FIGURE 1

Schematic outline of the study protocol. DTH, delayed-type hypersensitivity; RG, refined grain; WG, whole grain.

FIGURE 2

Consolidated Standards of Reporting Trials diagram. 1Other reasons included an unwillingness to eat all study foods, current participation in other studies, and being over the BMI range at the start date but after signing consent. 2Unwilling to eat all study foods. RG, refined grain; WG, whole grain.

FIGURE 3

α-Diversity comparisons of gut microbiota in stool samples that were collected at baseline and at the end of the intervention. Data are presented as box-and-whisker plots that show the distribution of data in quartiles. α Diversity did not significantly change from baseline after the intervention in either diet group as observed with the use of phylogenic diversity–richness metrics. The α diversity in stool samples that were collected at baseline was lower in the WG group (n = 38) than in the RG group (n = 39) (P = 0.01). RG, refined grain; WG, whole grain.

FIGURE 4

β-Diversity comparisons of gut microbiota in stool samples that were collected at baseline and after the intervention. Data are shown from WG participants (n = 38) before the intervention (dark-blue dots) and after the intervention (light-blue dots) as well as from RG participants (n = 39) before the intervention (dark-orange dots) and after the intervention (light-orange dots). A PC analysis of weighted (A) and unweighted (B) UniFrac distances. A permutation-based ANOVA [Adonis function in the vegan package in R software (60); 99 permutations] with weighted UniFrac-distance metrics revealed that the variation in the gut microbiota community structure could not be explained by the intervention group either at baseline (P = 0.39) or after the intervention (P = 0.25). However, a similar analysis with the use of unweighted UniFrac metrics showed differences in the microbiota structure of WG and RG groups at P = 0.05 and P = 0.07 for baseline and after the intervention, respectively. PC, principal coordinate; RG, refined grain; WG, whole grain.