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«Nutrients 2014, 6, 4822-4838; doi:10.3390/nu6114822 OPEN ACCESS nutrients ISSN 2072-6643 Review The Health Advantage ...»

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van Faassen et al. [40] were among the first to include a vegan diet as one of their experimental diet conditions. The authors compared subjects on a 20-day vegan diet as compared to 20-day lacto-ovo vegetarian and mixed Western diets. While subjects were on the vegan diet they showed the lowest levels of fecal Lactobacilli and Enterococci, along with lower concentrations of bile acids, coprostanol, and coprostanol plus cholesterol. These results are notable in that the vegan diet produced a significantly different result than the lacto-ovo vegetarian diet, suggesting that the broad distinction between meat and non-meat diets seen in earlier studies was not sufficient and a focus on vegan diets in their own right is warranted.

In the last few years the research community has focused greater attention on vegan diets as a distinct experimental dietary condition. Recent studies have provided more detailed analysis of vegan, vegetarian and omnivore gut microbial profiles. Matijaŝić et al. [34] compared bacterial DNA from fecal samples of 20 vegans, 11 lacto-vegetarians and 29 omnivores who were comparable in gender, age, body mass and height, and found an association between diet type and bacterial community composition. PCR-based DNA profiling methods were used to quantify microbiota by group. Both the vegetarian and vegan subjects were associated with a higher ratio of the Bacteroides-Prevotella group when compared to omnivores. Both vegan and vegetarian subjects also had a lower ratio of Clostridium cluster XIVa when compared to omnivores, a result similarly noted by Kabeerdoss et al. [41], but in Nutrients 2014, 6 4827 contrast to the findings of Kim et al. [33]. Only two distinctions were found between the vegans and the other vegetarians examined. Vegans had a higher ratio of Faecalibacterium prausnitzii, an anti-inflammatory bacterium and abundant butyrate producer in the class Clostridia (phylum Firmicutes), purported to play a protective role for colonocytes. Vegans also displayed a higher ratio of C. clostridioforme within the C. coccoides grouping.

A recent, large-scale study by Zimmer et al. [42] set out to distinguish the fecal microbiota profile of vegans (n = 105), from that of vegetarians (n = 144), and an equal number of controls consuming an omnivorous diet. Vegan and vegetarian subjects had adhered to their proclaimed diet for at least 4 weeks prior to the study. Vegan samples had significantly lower microbial counts than their omnivore counterparts for four bacterial taxa: Bacteroides, Bifidobacterium, E. coli and Enterobacteriaceae. Interestingly, the vegetarian sample also showed significantly reduced Bacteroides and Bifidobacteria, a result found 37 years earlier by Reddy [39]. It is important to note that Zimmer found that vegans and vegetarians were not significantly different from each other in these four taxa, nor did they differ in Enterobacter, Enterococcus, Clostridium, Klebsiella or Lactobacillus, when compared to each other or to the omnivore samples. Vegan diets are higher in carbohydrates and fiber than omnivores, and as such the vegan samples had significantly reduced stool pH than did controls. The lower pH was strongly correlated with reduced counts of E. coli and Enterobacteriacea, species which are not tolerant of the more acidic environment. The authors concluded that the gut microbiota and stool pH of vegetarians fell on a continuum between that of vegans and omnivores. These results suggest that the composition of the human gut is altered by diet along a continuum, with vegan diets being the most distinct from that of omnivores, but not necessarily significantly different from that of other vegetarians.

Interestingly, these findings are opposite those of other studies, although differing methodologies can make direct comparisons difficult. Matijaŝić et al. [34] found a higher ratio of the Bacteroides-Prevotella group associated with the vegetarian diets, while van Faassen et al. [40] found no effect of a vegan or vegetarian diet on Bifidobacteria and Bacteroides. Yet they did find lower counts of aerobic Lactobacilli and Enterococci, a result not found by Zimmer et al. [42]. Despite their often contradictory findings, these studies provide the first indication that there may be some distinction between the gut microbiota of a vegan and a vegetarian, although both diets appear to be responsible for significant shifts away from the omnivore’s gut profile. More large-scale studies are warranted to discern whether a distinction between vegans and vegetarians is legitimate, or whether life-long vegans can be compared with test subjects following a vegan diet for a short-term such as 20 days.

Can a Dietary Shift Modify the Gut Profile?

It is not clear whether adopting a vegan diet as short-term medical nutrition therapy can lead to a gut profile or “enterotype” comparable to that of a long-term vegan. A new avenue of research is examining whether our intestinal microbiota is a stable ecosystem, resistant to change, or whether a novel diet can facilitate a rapid, adaptive shift in the intestinal microbial community [43–46]. There is evidence that the ratio of bacteria species in the intestines may shift in response to a novel diet, though this change in species may not constitute a larger shift from one enterotype to another. For example, Wu et al. [22] found that among 98 subjects, those who identified as vegetarian (including one vegan) Nutrients 2014, 6 4828 showed enrichment in the Prevotella enterotype, while those who consumed meat as part of a Western diet were enriched in Bacteroides. Ten subjects who switched to a high-fat/low-fiber or low-fat/high-fiber diet displayed detectible changes in their microbiome composition within 24 hours, although their enterotype identity remained stable for the duration of the 10-day trial. Similarly, David et al. [43] reported a rapid adaptation of gut microbiota in response to a plant-based or animal-based diet, with adaptations to herbivorous and carnivorous functional profiles evident within five days on the new diet. Their data suggest that an animal-based diet has a greater impact on altering the gut microbiota than does a plant-based diet, as the animal-based diet increased levels of fecal bile acids, which increased the abundance of bile-tolerant organisms and decreased those species that metabolize dietary plant polysaccharides. Notably, the one life-long vegetarian among the 10 subjects showed a reduction in the genus Prevotella during the switch to an animal-based diet.

What is not clear from these short-term trials is whether dietary interventions, such as adopting a vegetarian or vegan diet, could stably switch subjects to a more beneficial enterotype and confer lasting health advantages. The human colonic microbiome is characterized by high resilience, a central concept in ecology whereby communities are able to withstand disturbance [21]. Faith et al. [44] followed 37 adult subjects and found that approximately 60% of their 200 microbial strains remained stable over the course of 5 years. Shared strains from family members suggest that hosts may retain their stable microbiota for decades. Rajilić-Stojanović et al. [46] followed 5 subjects for 8–12 years and concluded that although the relative abundance of intestinal bacteria species changed with diet, travel or antibiotic use, the core community of microbiota specific to each subject was conserved over many years. Similarly, Martínez et al. [45] followed three human subjects for one year and detected a stable core microbiota per individual, consisting of approximately 40 species (80% of the microbiota), which maintained persistent populations. The authors suggest that diet change may induce shifts within core members but the overall bacterial populations show resilience and return to baseline levels after the dietary intervention ceases. These findings call into question the efficacy of treating inflammatory diseases and metabolic disorders with short-term dietary interventions. More studies are warranted to determine if a long-term commitment to a plant-based therapeutic diet could more permanently alter an individual’s microbiota and confer health advantages.

3. Vegan Gut Microbiota May Be Protective against Metabolic Syndrome

Obesity is associated with an altered gut profile such that resident bacteria may be responsible for an increased capacity for energy harvest and a state of chronic, low-grade inflammation. This inflammation, in turn, can interfere with insulin signaling and results in the metabolic dysfunction found in obesity and type 2 diabetes [47,48]. Obesity has been linked to a decreased prevalence of Bacteroidetes (which includes both Prevotella and Bacteroides), and an increase in Firmicutes and Actinobacteria [49,50]. Ley et al. [30] found that a reduced calorie diet was sufficient to increase the relative abundance of Bacteroidetes relative to Firmicutes in obese subjects; the increase in Bacteroidetes and decrease in Firmicutes correlated with the percentage loss of body weight. In contrast, a balanced diet characterized by high consumption of fruits and vegetables and low consumption of meat leads to a highly diverse intestinal flora and a greater abundance of Prevotella over Bacteroides [49].

Nutrients 2014, 6 4829 Interestingly, F. prausnitzii, the most abundant bacterium in the intestines of healthy adults and a member of the Firmicutes, is one of the species Matijaŝić et al. [34] noted was distinctly more prevalent in vegans than in vegetarians. F. prausnitzii appears to play a significant protective role in metabolic disease, with depressed levels associated with intestinal disorders, inflammation and obesity [51], and type 2 diabetes [52,53]. Remely et al. [52] found that the gut profile of diabetics differs from that of lean controls, and noted that F. prausnitzii was most abundant in lean controls but least abundant in type 2 diabetics, a finding that agrees with prior studies. The prevalence of this species in the gut has been linked to diet, specifically ingestion of the plant polysaccharide, inulin [51].

Intestinal microbiota are able to produce short chain fatty acids (SCFA), acetate, propionate, and butyrate, through metabolism of dietary fiber. A strong positive correlation has been found between F. prausnitzii and butyrate production in the gastrointestinal tract, suggesting that this species may be associated with higher fiber intake and reduced risk for cardiovascular disease, colon cancer, diabetes and obesity [54].

It is possible that the disproportionately high prevalence of this beneficial bacterium in the vegan gut is attributable to a high fiber diet. The role of dietary fiber needs to be examined in greater depth, beyond its mechanical effect of increasing stool bulk and speeding transit time. Dietary fiber also influences the intestinal environment by inhibiting pathogen adhesion, altering bacterial fermentation patterns and short chain fatty acid concentrations, modifying microbiota community profiles, and lowering stool pH [32,42]. De Filippo et al. [29] found a greater concentration of SCFA in fecal samples of children in rural Africa as compared to their European counterparts. The authors hypothesized that SCFA-producing bacteria are selected for by a diet high in plant polysaccharides and low in fat and sugar. Further research is warranted to determine if there is a link between a vegan diet, type and quantity of dietary fiber, an increased intestinal prevalence of F. prausnitzii and other SCFA-producing bacteria, and a corresponding reduction in the prevalence of obesity, type 2 diabetes, inflammation and intestinal disorders.

Inflammation may be the critical component linking gut microbiota with obesity as well as metabolic dysfunction and chronic disease [48,55]. Verdam et al. [56] found that among 28 subjects, the microbiota of the obese subjects, unlike that of the non-obese, was characterized by a reduced bacterial diversity, a decreased ratio of Bacteroidetes to Firmicutes, and an increased abundance of potentially inflammatory Proteobacteria. Moreover, the microbiota of obese subjects was associated with markers of local and systemic inflammation (fecal calprotectin and plasma C-reactive protein, respectively).

The role of a vegan diet in influencing obesity and inflammation was explored by Kim et al. [33], in their study of 6 obese subjects with diabetes and/or hypertension. Subjects who followed a vegan diet for one month, were found to have improved blood glucose levels and reduced body weight, as well as a reduction in triglycerides, total cholesterol, LDL-cholesterol and Hemoglobin A1c. The vegan diet therapy induced an altered gut microbiota by reducing the abundance of Firmicutes and increasing the abundance of Bacteroidetes significantly. Despite alterations in the Firmicutes-to-Bacteroidetes ratio, these changes did not result in a switch of the host’s enterotype, as both Prevotella and Bacteroides (responsible for degradation of plant polysaccharides) increased in response to a vegan diet. Notably, the vegan diet was associated with a decrease in pathobionts such as Enterobacteriaceae, a family of bacteria implicated in triggering low-grade inflammation, which Zimmer [42] also found were reduced Nutrients 2014, 6 4830 in vegan subjects. The authors measured decreasing concentrations of the inflammation markers, fecal lipocalin-2 (Lcn-2), as the subjects progressed on their vegan diets, and concluded that the vegan diet directly reduced the population of pathobionts, thereby reducing inflammation and contributing to the improved glucose tolerance and lipid metabolism of their vegan subjects [33]. It has to be considered that the fiber content of vegan diets may play a significant role in regulating the inflammatory response. SCFA generated by gut microbiota can act as signaling molecules, activating G protein-coupled receptors and modulating the host’s inflammatory response [32]. Thus dietary fiber may be a key variable in any evaluation of vegan diets and inflammatory disease.

The most recent evidence that a vegan diet promotes a gut microbiota that directly reduces metabolic disease risk is the research linking diet to L-carnitine metabolism and atherosclerosis risk.

Koeth et al. [57] found that microbial metabolism of dietary L-carnitine, a trimethylamine found in red meat, produces trimethylamine-N-oxide (TMAO), which has been shown to promote atherosclerosis.

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