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

Authors: VANEGAS, SALLY - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; MEYDANI, MOHSEN - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; BARNETT, JUNAIDAH - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; GOLDIN, BARRY - Tufts University; KANE, ANNE - Tufts University; RASMUSSEN, HELEN - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; BROWN, CARRIE - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; VANGAY, PAJAU - University Of Minnesota; KNIGHTS, DAN - University Of Minnesota; JONNALAGADDA, SATYA - The Bell Institute; KOECHER, KATIE - The Bell Institute; KARL, J. PHILIP - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; THOMAS, MICHAEL - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; DOLNIKOWSKI, GREGORY - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; LI, LIJUN - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; SALTZMAN, EDWARD - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; WU, DAYONG - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; MEYDANI, SIMIN - Jean Mayer Human Nutrition Research Center On Aging At Tufts University

Submitted to: The American Journal of Clinical Nutrition
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/27/2016
Publication Date: 2/8/2017
Citation: Vanegas, S.M., Meydani, M., Barnett, J.B., Goldin, B., Kane, A., Rasmussen, H., Brown, C., Vangay, P., Knights, D., Jonnalagadda, S., Koecher, K., Karl, J., Thomas, M.J., Dolnikowski, G.G., Li, L., Saltzman, E., Wu, D., Meydani, S.N. 2017. 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. American Journal of Clinical Nutrition. 105:635-650. doi: 10.3945/ajcn.116.146928.

Interpretive Summary: Observational studies suggest an inverse association between whole grains consumption and inflammation, a key risk factor for chronic diseases. However, evidence from interventional studies is limited, most of which did not control total calorie intake and body weight, and few included comprehensive measurements of immune function. In this study, 49 men and 32 post-menopausal women (40-65 years old with body mass index (BMI) less than 35) were provided whole grain or refined grain weight-maintenance diets for 6 weeks. We found that participants had good adherence to the study diets. The main scientific findings are that compared to refined grains group, whole grain group had an increased stool weight and frequency; more importantly, whole grain group also showed some favorable changes in gut short-chain fatty acids, commensal bacteria, and immune function markers. This is the first well-controlled study to determine the effect of increasing whole grain consumption while body weight is maintained on gut health and immune function, and the results show that whole grain without weight loss modestly impacts gut and immune health.

Technical 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 Entero-bacteriaceae (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-alpha (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.