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Hunter Adams
Hunter Adams

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The causal relationship between the gut microbiota and overall pathological conditions is still unclear. Indeed, it is still unclear whether a disease-prone microbial composition exists (so-called dysbiosis) or whether the changes in the microbial community occur after the onset of the disease [3]. Conversely, diet undoubtedly influences the composition of gut microbiota, providing nutrients for both the host and the bacteria. This gut community has many degrading enzymes and metabolic capabilities that are able to break down macromolecules into smaller chemical compounds, which can then be uptaken by enterocytes [4]. Moreover, long-term dietary habits have been shown to play a crucial role in creating an inter-individual variation in microbiota composition [5]. However, despite the great number of publications on the effects of carbohydrates, the impacts of dietary fats and protein on the gut microbiota are less well defined. In particular, gut microbiota changes associated with omega-3 fatty acids are poorly understood.

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Among the omega-3 polyunsaturated fatty acids (PUFAs), eicosapentaenoic acid (EPA, C20:5) and docosahexaenoic acid (DHA, C22:6) are the two main bioactive forms in humans. These fatty acids can be synthesized from the dietary precursor and essential fatty acid, α-linolenic acid (ALA, C18:3). However, the synthesis pathway requires several elongation and desaturation chemical reactions, so that the conversion of the two active forms in mammals is less efficient than dietary uptake. For this reason, consumption of EPA- and DHA-rich foods is recommended. However, since foods rich in these fatty acids are not widespread, EPA and DHA are widely used as nutritional supplements, often as nutraceuticals. Several papers have demonstrated the correlation between omega-3 PUFAs and the inflammatory response. Although the literature on this topic is discordant, omega-3 PUFAs are generally associated with anti-inflammatory effects, in comparison with the omega-6 PUFAs that are linked to pro-inflammatory effects, due to the different downstream lipid metabolites [6]. Also, with regards to the link to immunity, studies have shown that the supplementation of omega-3 PUFAs provides multiple health benefits against different chronic degenerative diseases, such as cardiovascular diseases [7], rheumatoid arthritis [8], inflammatory bowel disease (IBD) [9], depression [10], and cancer [11].

Another dietary intervention was the Pilchardus Study, a multicentre randomized trial in patients diagnosed with type 2 diabetes (glycated haemoglobin level between 6.0% and 8.0%) and not subjected to insulin treatment or antidiabetic drugs [18]. In this study, the participants followed a six-month dietary intervention of either a standard diet for diabetes, control (n = 15), or a standard diet supplemented with 100 g of sardines five days a week (n = 17), which provided approximately 3 g of EPA and DHA. The analysis of the abundance of the target bacteria by quantitative real-time polymerase chain reaction (qPCR) revealed a significant decrease in Firmicutes phylum in both experimental groups, with the Firmicutes/Bacteroidetes ratio decreasing in the omega-3 group. Moreover, E. coli concentrations increased in both groups and the proportions of Bacteroides-Prevotella increased in the sardine-fed group [18].

In another case report, Noriega and co-workers analyzed the effect of omega-3 PUFA supplementation on human gut microbiota using NGS technology [19]. In this study, a daily supplementation of 600 mg of omega-3 PUFAs through a fish protein diet was implemented for two weeks in one 45-year-old man. This intervention led to an increase in the Firmicutes phylum, and to a simultaneous decrease in Bacteroidetes and Actinobacteria. Moreover, a reduction in Faecalibacterium genus versus an increase in Blautia, Roseburia, Coprococcus, Ruminococcus, and Subdoligranulum genera was recorded. Some of these recorded genera are still associated with butyrate production. However, after two washout weeks, a reversal trend was observed, indicating that gut microbiota is strongly sensitive to diet changes [19].

The recent study of Menni and co-workers [20] correlated DHA circulating levels with DHA dietary intake, determined by a Food Frequency Questionnaire. The association with major taxa was determined in the largest population studied to date in this topic, with 876 participants, based on a cohort of middle-aged and elderly women (mean age = 64.98 years old). They found that a DHA intake of 350 mg/day resulted in a serum DHA concentration of 0.14 mmol/L, and was significantly associated with 36 Operational Taxonomic Units (OTUs). Of these, 21 OTUs (58%) belonged to Lachnospiraceae, 7 to Ruminococcaceae (19%), and 5 to Bacteroidetes (14%). In this study, a correlation between serum DHA and faecal metabolites was evaluated, and a positive correlation with N-carbamylglutamate was found. Even in this analysis, a positive correlation between omega-3 PUFAs and SCFA-producing bacteria (Lachnospiraceae family) was highlighted. The authors hypothesized that the levels of N-carbamylglutamate present in the gut lumen may mediate the association between the found taxa and serum DHA [20].

Studies have shown that different types of dietary fat, including saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs), and PUFAs, and their abundance in the diet, could change gut microbiota composition [48]. In particular, omega-3 PUFAs share the important immune system activation/inhibition pathway with gut microbes modulating pro-inflammatory profiles [49]. For example, supplementation with an equal mixture of EPA and DHA decreased intestinal barrier dysfunction and decreased PPAR-γ levels caused by ischemia and reperfusion intestinal injury in a Sprague Dawley rat model [50]. Several types of fatty acids have an antimicrobial activity, and this activity occurs after the complete enzymatic hydrolysis of fat by the gut microbiota in the lower gastrointestinal tract [51]. The antimicrobial activity of fatty acids depends on the length of their carbon chain and on the presence, number, position, and orientation of double bonds. Unsaturated fatty acids tend to have greater activity than saturated fatty acids with the same length carbon chain [51]. The antimicrobial activity of PUFAs increases in the direction of the number of double bonds in their carbon chain; the cis-orientation seems to have more activity than the trans-orientation. Some studies have shown that omega-3 PUFAs can modify the intestinal microbiota composition [52] by increasing the number of Bifidobacteria that decrease gut permeability [53], and increase the number of Enterobacteria that increase intestinal permeability [54], allowing increased systemic concentration of LPS and endotoxemia.

Caesar and colleagues [57] showed that the type of dietary fat is a major driver of community structure, affecting both the composition and diversity of the gut microbiota. The authors fed two different groups of rats either a fish-oil diet or a lard diet. The results showed that mice fed fish oil had higher levels of Lactobacillus and Akkermansia muciniphila than mice fed with lard, in which Bilophila was abundant. The increase of Lactobacillus is associated with reduced inflammation in several inflammatory bowel diseases. The increase of Akkermansia muciniphila improves the barrier function and glucose metabolism, and also decreases macrophage infiltration in the white adipose tissue (WAT) [58]. In a study comparing different types of high-fat diets on the profile of gut bacteria in a mouse model, Liu and co-workers [55] observed that consumption of an SFA-rich diet resulted in a significant decrease in the abundance of Bacteroidetes compared to either omega-3 PUFA-rich or omega-6 PUFA-rich diets. A mouse study [59] reported that a diet supplemented with EPA and DHA significantly increased the abundance of Firmicutes and reduced the percentage of Bacteroidetes, compared with a diet supplemented with oleic acid. As for human studies [16,17], the changes in metabolic parameters after DHA intake in mice could be the result of interactions between gut microbiota and DHA metabolites, potentially through the enterohepatic circulation of bile salts [17]. Myles et al. [60] indicated that omega-3 PUFA intake in pregnant mice could influence offspring microbiota and immune response through the anti-inflammatory effects of omega-3 PUFAs. These findings suggest that the administration of omega-3 PUFAs during embryonic development is important for the proper development of the microbiota and immune system.

Studies on mice-transplanted faeces showed that the omega-3 PUFAs can modify the microbiota through the production and secretion of intestinal alkaline phosphatase (IAP), leading to a reduction in the number of LPS-producing bacteria, thus reducing metabolic endotoxemia [52]. Mujico et al. [59] showed that, in diet-induced obese mice, supplementation with a combination of EPA and DHA significantly increased the quantities of Firmicutes, and especially the Lactobacillus taxa. Evidence suggests that some physiological effects of the microbiota could be associated with the interactions between dietary PUFAs. Dietary PUFAs have been suggested to affect the attachment sites for the gastrointestinal microbiota, possibly by modifying the fatty acid composition of the intestinal wall [61]. Data from animal models indicates that fish oil in particular has effects on shaping the microbiome. Ghosh et al. [62] found that mice fed a diet supplemented with fish oil had a reduced abundance of Enterobacteriaceae and Clostridia species compared with mice fed a diet rich in omega-6 fatty acids.

The role of omega-3 on microbiota composition and diversity has not yet been thoroughly explored in human cohorts in comparison to animal models. As described above, increased intestinal permeability is involved in several disorders associated with chronic low-grade inflammation, including obesity, obesity-associated insulin resistance, type 2 diabetes, and IBD. The integrity of the intestinal epithelium is created by the tight junctions. Tight junctions are composed of multiple proteins, including cytosolic zonula occludin. Zonulin, a detectable protein in human serum [63], has been shown to reflect intestinal permeability [64,65]. Serum zonulin has been used as a serum marker for intestinal permeability in several studies [66,67,68]. Increased serum concentrations have been detected in a range of metabolic conditions associated with chronic low-grade inflammation. This marker was used by Mokkala and co-workers [69] to analyze intestinal permeability in pregnant women. Numerous metabolic alterations accompany pregnancy that support foetal growth and development. Initial results suggested that healthy pregnant women exhibited an increase in intestinal permeability compared with non-pregnant women [70]. However, little is known about the effects of pregnancy on intestinal permeability and whether this could lead to subsequent health consequences.


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