Eur J Nutr. , 2020., 59(6): 2411–2425. doi: 10.1007/s00394-019-02088-0

Metabolically and immunologically beneficial impact of extra virgin olive and flaxseed oils on composition of gut microbiota in mice

Millman, J Okamoto, S Kimura, A et al.

Abstract

Purpose: Extra virgin olive oil (EVOO) and flaxseed oil (FO) contain a variety of constituents beneficial for chronic inflammation and cardio-metabolic derangement. However, little is known about the impact of EVOO and FO on dysbiosis of gut microbiota, intestinal immunity, and barrier. We, therefore, aimed to assess the impact of EVOO and FO on gut microbiota, mucosal immunity, barrier integrity, and metabolic health in mice. Methods: C57BL/6 J mice were exposed to a low-fat (LF), lard (HF), high fat-extra virgin olive oil (HF-EVOO), or high fat-flaxseed oil (HF-FO) diet for 10 weeks. Gut microbiota assessment was undertaken using 16S rRNA sequencing. Levels of mRNA for genes involved in intestinal inflammation and barrier maintenance in the intestine and bacterial infiltration in the liver were measured by qPCR.

Results: HF-EVOO or HF-FO mice showed greater diversity in gut microbiota as well as a lower abundance of the Firmicutes phylum in comparison with HF mice (P < 0.05). The qPCR analyses revealed that mRNA level of FoxP3, a transcription factor, and IL-10, an inducer of regulatory T cells, was significantly elevated in the intestines of mice-fed HF-EVOO in comparison with mice-fed HF (P < 0.05). The mRNA level of the antimicrobial peptide, RegӀӀӀγ, was markedly elevated in the intestines of HF-EVOO and HF-FO compared with HF group (P < 0.05). Conclusions: Our data suggest that the consumption of EVOO or FO can beneficially impact gut microbiota, enhance gut immunity, and assist in the preservation of metabolic health in mice.

Link to Full Text

Key Points

To date, little is known about the potential impact of specific plant-derived dietary fats and oils on composition of gut microbiota and host metabolic health. Extra Virgin Olive oil (EVOO) and Flaxseed oil (FO), two major oils marketed as ‘functional foods,’ contain a wide variety of compounds purported to have anti-inflammatory properties and beneficial effects on markers of metabolic health including blood glucose and lipids, body weight, and inflammation.

In this context, the present study aims to characterize the potential impact of EVOO and FO on mouse gut microbiota, with a particular focus on gut barrier integrity, mucosal immunity, and metabolic health—specifically in relation to fuel homeostasis, inflammation, and gut permeability. The hypothesis is that the ingestion of either EVOO or FO will exert superior effects on mouse gut microbiota composition and diversity, intestinal immune function, and metabolic health in comparison with mice-fed HF or even LF diets.

The present study demonstrates that mice-fed HF-EVOO and HF-FO exhibited a variety of beneficial effects on markers of health. Specifically, HF-EVOO- and HF-FO-fed mice exemplified a significantly positive impact on blood glucose compared to HF-fed mice. Noticeably, these beneficial effects on glucose homeostasis were observed despite no significant differences in body weight gain or energy intake among groups. In light of this finding, specific components within EVOO and FO, including the ω9 and ω3 fatty acids from EVOO and FO, respectively, may be partially accountable for such a favorable impact.

The present study demonstrates that plasma concentrations of SCFAs differed significantly among groups. Total SCFA concentration as well as the major SCFA, acetate, was significantly lower in mice-fed LF in comparison with mice-fed HF-EVOO, HF-FO, and HF diets.

A substantial impact on the composition of gut microbiota was observed in mice-fed EVOO and FO. HF-EVOO and HF-FO-fed mice displayed significantly higher diversity in gut microbiota compared to HF-fed mice as well as β-diversity plots revealing clear differences between HF-EVOO and HF-FO groups vs. LF and HF groups.

The data provides novel evidence that the consumption of EVOO and FO can beneficially impact the composition of gut microbiota, increase microbial diversity as well as influence the production of microbial-derived metabolites contributing to the activation of mucosal immune system, enhancement of markers of gut barrier integrity, and ultimately support metabolic health in mice. Further studies are warranted to test this hypothesis in human clinic-based dietary interventions.