Diet Quality, Microbial Lignan Metabolites, and Cardiometabolic Health among US Adults

Author:

Koemel Nicholas A.12ORCID,Senior Alistair M.134,Benmarhnia Tarik5,Holmes Andrew13ORCID,Okada Mirei13,Oulhote Youssef6ORCID,Parker Helen M.12ORCID,Shah Sanam7,Simpson Stephen J.13,Raubenheimer David13,Gill Timothy P.128,Laouali Nasser567ORCID,Skilton Michael R.2ORCID

Affiliation:

1. Charles Perkins Centre, The University of Sydney, Sydney 2006, Australia

2. Sydney Medical School, The University of Sydney, Sydney 2006, Australia

3. School of Life and Environmental Sciences, The University of Sydney, Sydney 2006, Australia

4. Sydney Centre for Precision Data Science, The University of Sydney, Sydney 2006, Australia

5. Scripps Institution of Oceanography, University of California, San Diego, CA 92093, USA

6. Department of Biostatistics and Epidemiology, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA 01003, USA

7. “Exposome and Heredity” Team, CESP, Paris-Saclay University, UVSQ, University Paris-Sud, Inserm, Gustave Roussy, F-94805 Villejuif, France

8. Susan Wakil School of Nursing and Midwifery, The University of Sydney, Sydney 2006, Australia

Abstract

The gut microbiome has been shown to play a role in the relationship between diet and cardiometabolic health. We sought to examine the degree to which key microbial lignan metabolites are involved in the relationship between diet quality and cardiometabolic health using a multidimensional framework. This analysis was undertaken using cross-sectional data from 4685 US adults (age 43.6 ± 16.5 years; 50.4% female) participating in the National Health and Nutrition Examination Survey for 1999–2010. Dietary data were collected from one to two separate 24-hour dietary recalls and diet quality was characterized using the 2015 Healthy Eating Index. Cardiometabolic health markers included blood lipid profile, glycemic control, adiposity, and blood pressure. Microbial lignan metabolites considered were urinary concentrations of enterolignans, including enterolactone and enterodiol, with higher levels indicating a healthier gut microbial environment. Models were visually examined using a multidimensional approach and statistically analyzed using three-dimensional generalized additive models. There was a significant interactive association between diet quality and microbial lignan metabolites for triglycerides, low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, insulin, oral glucose tolerance, adiposity, systolic blood pressure, and diastolic blood pressure (all p < 0.05). Each of these cardiometabolic health markers displayed an association such that optimal cardiometabolic health was only observed in individuals with both high diet quality and elevated urinary enterolignans. When comparing effect sizes on the multidimensional response surfaces and model selection criteria, the strongest support for a potential moderating relationship of the gut microbiome was observed for fasting triglycerides and oral glucose tolerance. In this study, we revealed interactive associations of diet quality and microbial lignan metabolites with cardiometabolic health markers. These findings suggest that the overall association of diet quality on cardiometabolic health may be affected by the gut microbiome.

Funder

University of Sydney Faculty of Medicine and Health Executive Dean Stipend Scholarship

doctoral funding from l’Ecole Doctorale de Santé Publique, Ministère de l’enseignement supérieur, de la recherche et de l’innovation

the Fondation de France

Australian government NHMRC Program

Publisher

MDPI AG

Subject

Food Science,Nutrition and Dietetics

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