«Nutrients 2014, 6, 4822-4838; doi:10.3390/nu6114822 OPEN ACCESS nutrients ISSN 2072-6643 Review The Health Advantage ...»
Nutrients 2014, 6, 4822-4838; doi:10.3390/nu6114822
The Health Advantage of a Vegan Diet: Exploring the Gut
Marian Glick-Bauer and Ming-Chin Yeh *
Nutrition Program, CUNY School of Public Health, Hunter College, City University of New York,
2180 Third Avenue, Room 614, New York, NY 10035, USA; E-Mail: email@example.com
* Author to whom correspondence should be addressed; E-Mail: firstname.lastname@example.org;
Tel.: +1-212-396-7776; Fax: +1-212-396-7638.
Received: 12 August 2014; in revised form: 16 October 2014 / Accepted: 27 October 2014 / Published: 31 October 2014 Abstract: This review examines whether there is evidence that a strict vegan diet confers health advantages beyond that of a vegetarian diet or overall healthy eating. Few studies include vegan subjects as a distinct experimental group, yet when vegan diets are directly compared to vegetarian and omnivorous diets, a pattern of protective health benefits emerges. The relatively recent inclusion of vegan diets in studies of gut microbiota and health allows us the opportunity to assess whether the vegan gut microbiota is distinct, and whether the health advantages characteristic of a vegan diet may be partially explained by the associated microbiota profile. The relationship between diet and the intestinal microbial profile appears to follow a continuum, with vegans displaying a gut microbiota most distinct from that of omnivores, but not always significantly different from that of vegetarians. The vegan gut profile appears to be unique in several characteristics, including a reduced abundance of pathobionts and a greater abundance of protective species.
Reduced levels of inflammation may be the key feature linking the vegan gut microbiota with protective health effects. However, it is still unclear whether a therapeutic vegan diet can be prescribed to alter the gut microflora for long-term health benefits.
Keywords: vegan; vegetarian; gut microbiota; microflora; weight; obesity Nutrients 2014, 6 4823
1. Introduction As vegetarian diets have increased in popularity, veganism has gained recognition as a healthy and potentially therapeutic dietary choice . A recent survey utilizing a food frequency questionnaire from 1475 participants, including 104 vegans, found that a vegan diet received the highest diet quality score as measured by the Healthy Eating Index 2010and the Mediterranean Diet Score, while unrestricted omnivores received the lowest . Vegan diets have gained acceptance as a dietary strategy for maintaining good health and managing disease conditions ranging from cardiovascular disease to cancer . Vegan diets may prove useful as medical nutrition therapy in treating the conditions of metabolic syndrome, including obesity, diabetes and cardiovascular risk [3–5], and may confer protection against inflammatory conditions such as rheumatoid arthritis (RA) [6,7]. This review examines whether there is evidence that strict vegan diets confer protective benefits beyond that of vegetarian diets or overall healthy eating. Furthermore, the possibility that a vegan health advantage may be associated with a unique gut microbiota profile will be explored as a mechanism by which a vegan diet might be protective against metabolic and inflammatory disease states.
1.1. Are the Health Benefits of a Vegan Diet Unique?
Very few studies rigorously evaluate and compare omnivorous, vegetarian and vegan subjects as distinct experimental groups. It is thus difficult to discern whether the health advantages attributed to vegans could be generalized to all vegetarians or even to moderate meat eaters following a healthy diet. For example, Goff et al.  compared biochemical profiles of vegans and omnivores matched for gender, age and body mass index. The 21 vegans were found to have lower blood pressure, and lower fasting triacylglycerol and glucose concentrations than 25 omnivorous subjects, as well as a biochemical profile that was cardioprotective and beta-cell protective. Similarly, the health characteristics of 21 sedentary vegans who followed a long-term raw vegan diet were found to be comparable to that of endurance exercisers, with reduced BMI, lipids, lipoproteins, glucose, insulin, C-reactive protein, blood pressure and carotid artery intima-media thickness when compared to 21 sedentary subjects following a Western diet .
However, as these studies only compared vegans to omnivores, it is probable that a similar advantage may have been observed in vegetarian subjects as well. Vegetarian diets in general have been credited with improving insulin resistance , lowering diabetes risk [4,11], and lowering cardiometabolic disease risk . A study of 170 vegetarian Buddhist monks and 126 omnivorous men found that the vegetarians had significantly lower BMI, blood pressure, and triglycerides as well as more favorable lipoprotein and apolipid profiles and lower predicted probability of coronary heart disease . A study of 45 long-term (≥15 years) vegetarians found lower levels of oxidative stress, body fat and cholesterol than in 30 gender- and age-matched omnivores .
Even diets which allow moderate amounts of animal products may be protective against disease. A pooled analysis of five prospective cohort studies, involving 76,000 subjects found that both vegetarians and those who followed a “prudent” diet allowing small amounts of red meat benefited from a reduced risk of coronary heart disease and type 2 diabetes . A retrospective cohort study utilizing a Taiwan longitudinal health checkup database of 93,209 participants (of which 1116 were Nutrients 2014, 6 4824 vegan), found no decrease in metabolic syndrome with a vegan diet when compared to pescovegetarian, lactovegetarian and nonvegetarian diets . These studies suggest that a vegan diet warrants further investigation to distinguish any uniquely protective effects not available from vegetarian or other less restrictive diets.
The Adventist Health Study-2 provides a unique opportunity to compare not only vegetarians to omnivores, but to distinguish between four types of vegetarian diet, designated as vegan, lacto-ovo vegetarian, pescovegetarian, and semi-vegetarian. While vegetarian diets in general were found to be beneficial when compared to omnivore diets, vegan diets appeared to confer a particular advantage in lowering odds ratios for developing type 2 diabetes [4,16], and all-cause mortality . Hazard ratios for developing overall and female-specific cancers was similarly lower for those adhering to a vegan diet. Vegans in this population were found to have the lowest BMI when compared to all other diet types , although researchers noted some inadequate nutrient intake by the subjects following the strictest vegetarian diets. While Le and Sabaté  found that vegetarian diets in the Adventist cohort conferred protection against cardiovascular diseases, cardiometabolic risk factors, some cancers and total mortality, vegan diets in particular provided additional protection against obesity, hypertension, type 2 diabetes and cardiovascular mortality.
Other studies support the findings of the Adventist Health Study-2 population. A 74-week study on type 2 diabetes patients found that a low-fat vegan diet improved glycemia and plasma lipids significantly more than did a conventional diabetes diet [19,20]. A study of 23 overweight hyperlipidemic men and postmenopausal women who followed either a low-carbohydrate vegan diet or a high-carbohydrate lacto-ovo vegetarian diet for 7 months found that the vegan diet resulted in greater weight loss and decreases in LDL-cholesterol and triglycerides, and improved heart disease risk factors . Thus in studies where vegans are compared to not only omnivores but to other vegetarians as well, a pattern of protective health benefits is emerging.
1.2. Link between Diet, Microbiota and Health
Recent gains in our understanding of the human gut microbiome has caused a shift in thinking, away from the concept of the “normal” gut, and toward an understanding of the complexity of our microbial communities and their functional properties in influencing health and disease . The majority of microorganisms in the human intestine belong to the phyla Firmicutes (which includes Clostridium, Enterococcus, Lactobacillus and Ruminococcus) and Bacteroidetes (which includes Bacteroides and Prevotella in proportions determined in part by diet) [22,23] (See Table 1). Within
these, three distinct enterotypes of the human gut microbiome were proposed by Arumugam :
(1) abundant Bacteroides; (2) few Bacteroides but abundant Prevotella; and (3) abundance of Ruminococcus. Each of these genera may be linked to distinct nutrient-metabolism functions and thus long-term dietary influences may play a key role. (See Power et al.  for a table of diet-microbe associations). Wu et al.  found two enterotypes associated with diet; the enterotype dominated by Bacteroides is adapted to diets high in protein and animal fats, while the Prevotella enterotype is associated with carbohydrate metabolism and a vegetarian diet. The National Institutes of Health Human Microbiome Project (HMP) found that bacteria from stool samples fell into four community types represented by a cluster of numerous taxa . Others have concluded that although the HMP Nutrients 2014, 6 4825 cohort is consistent with the two biome types found by Wu et al. , the data supports a gradient of microbial communities rather than distinct enterotypes [26,27].
Diet history is a factor that must be considered in the analysis of gut microbiota of any subjects . Ruengsomwong et al.  found that among 13 Thai adults, non-vegetarians had a significantly higher abundance of Bacteroides while vegetarian subjects were enriched in the Prevotella genera. Microbiota dominated by Firmicutes (which includes Ruminococcus) have been strongly associated with a Western diet , and obesity , although there is debate over the significance of the relative ratios of Bacteroidetes and Firmicutes in lean and obese humans .
A study by De Filippo et al.  comparing European children to children in Burkina Faso, Africa found that the microbiome of European children consuming a Western diet is characterized by a predominance of the Bacteroides enterotype and a greater abundance of Gram-positive bacteria, mainly Firmicutes. The African microbiome, influenced by a high fiber, vegetarian diet is dominated by the Prevotella enterotype, with an overall enrichment in Gram-negative bacteria, mainly Bacteroidetes, and a corresponding depletion in Firmicutes. The African microbiome is also characterized by a higher microbial richness and diversity and a comparatively lower prevalence of pathogenic strains of Enterobacteriaceae. While diet plays a dominant role in shaping the gut microbiota in these disparate geographic communities, many other factors are thought to have an influence, including hygienic and sanitary conditions, prevalence of breast feeding, use of antibiotics and vaccines, ethnicity and geographic conditions .
Comparisons of dietary associations are complicated by the different methodologies used to study gut microbiota . For example, both Bacteroides and Prevotella are characterized by polysaccharide-degrading bacteria . As a group, Bacteroides-Prevotella have been shown to increase in abundance with a vegetarian or vegan diet using PCR-based DNA profiling techniques .
Thus the associations between diet and microbial communities may vary depending on whether researchers are conducting global assessments of gut microbiota or seeking greater taxonomic detail through DNA sequencing .
direct influence on our health . Gut dysbiosis, resulting from continued perturbations to the intestinal ecosystem, is implicated in disease states  as well as obesity . Gut dysbiosis may contribute to a myriad of ailments in the host including allergies, celiac disease, gastric cancer, autism, obesity, anorexia, Irritable Bowel Disease, Crohn’s Disease, and type 2 diabetes (see Clemente et al.  for a table of implicated microbiota). It is likely that our host-gene-microbial interactions underlie complex autoimmune and inflammatory diseases, and that a better understanding of both the diversity and stability of our microbiota is necessary to identify personal disease phenotypes and improve medical treatments . The inclusion of vegan diets in studies of gut microbiota and health allows us the opportunity to assess whether the vegan gut microbiota is distinct from that of vegetarians and omnivores, and whether the health advantages characteristic of a vegan diet may be partially explained by the associated microbiota profile.
2. Is the Vegan Gut Profile Unique?
As early as the 1970s researchers have been examining the role of diet on gut microflora by comparing diets high in meat (“mixed Western diet”) with vaguely defined non-meat diets. For example, Reddy et al.  found evidence that omnivores had an anaerobic microflora enriched in Bacteroides, Bifidobacterium, Peptococcus and Lactobacillus when compared to non-meat eaters. In the 1980’s vegan diets emerged as a defined subset of vegetarians worthy of study. While a few studies were able to take advantage of subjects who have been long-term vegans or lifelong vegetarians (such as the 7th Day Adventist research set), the majority of researchers relied upon experiments in which a short-term Western, vegetarian or vegan diet was imposed on subjects in order to measure the subsequent effect on gut microbiota or the products of microbial metabolism. This research has brought attention to the possibility of utilizing vegan or other therapeutic diets as medical intervention for a host of disease states.