Increases in Colonic Bacterial Diversity after ω-3 Fatty Acid Supplementation Predict Decreased Colonic Prostaglandin E2 Concentrations in Healthy Adults

Author:

Djuric Zora12,Bassis Christine M3,Plegue Melissa A1,Sen Ananda14,Turgeon D Kim5,Herman Kirk5,Young Vincent B3,Brenner Dean E56,Ruffin Mack T7

Affiliation:

1. Departments of Family Medicine

2. Nutritional Sciences

3. Microbiology

4. Biostatistics

5. Internal Medicine

6. Pharmacology, University of Michigan, Ann Arbor, MI

7. Family and Community Medicine, Penn State Health, Milton S Hershey Medical Center, Hershey, PA

Abstract

ABSTRACT Background The intestinal microbiome is an important determinant of inflammatory balance in the colon that may affect response to dietary agents. Objective This is a secondary analysis of a clinical trial, the Fish Oil Study, to determine whether interindividual differences in colonic bacteria are associated with variability in the reduction of colonic prostaglandin E2 (PGE2) concentrations after personalized supplementation with ω-3 (n–3) fatty acids. Methods Forty-seven healthy adults (17 men, 30 women, ages 26–75 y) provided biopsy samples of colonic mucosa and luminal stool brushings before and after personalized ω-3 fatty acid supplementation that was based on blood fatty acid responses. Samples were analyzed using 16S ribosomal RNA sequencing. The data analyses focused on changes in bacterial community diversity. Linear regression was used to evaluate factors that predict a reduction in colonic PGE2. Results At baseline, increased bacterial diversity, as measured by the Shannon and Inverse Simpson indexes in both biopsy and luminal brushing samples, was positively correlated with dietary fiber intakes and negatively correlated with fat intakes. Dietary supplementation with ω-3 fatty acids increased the Yue and Clayton community dis-similarity index between the microbiome in luminal brushings and colon biopsy samples post-supplementation (P = 0.015). In addition, there was a small group of individuals with relatively high Prevotella abundance who were resistant to the anti-inflammatory effects of ω-3 fatty acid supplementation. In linear regression analyses, increases in diversity of the bacteria in the luminal brushing samples, but not in the biopsy samples, were significant predictors of lower colonic PGE2 concentrations post-supplementation in models that included baseline PGE2, baseline body mass index, and changes in colonic eicosapentaenoic acid–to–arachidonic acid ratios. The changes in bacterial diversity contributed to 6–8% of the interindividual variance in change in colonic PGE2 (P = 0.001). Conclusions Dietary supplementation with ω-3 fatty acids had little effect on intestinal bacteria in healthy humans; however, an increase in diversity in the luminal brushings significantly predicted reductions in colonic PGE2. This trial was registered at www.clinicaltrials.gov as NCT 01860352.

Funder

University of Michigan Medical School Host Microbiome Initiative

Cancer Center Support Grant for the University of Michigan Comprehensive Cancer Center

Clinical Translational Science

National Institutes of Health

Michigan Diabetes Research Center

Michigan Nutrition and Obesity Research Center

Publisher

Oxford University Press (OUP)

Subject

Nutrition and Dietetics,Medicine (miscellaneous)

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