July 2018 Issue

Plant-Based Diets and the Gut Microbiota
By Carrie Dennett, MPH, RDN, CD
Today's Dietitian
Vol. 20, No. 7, P. 36

Learn how healthful dietary patterns can shape the gastrointestinal environment and reduce risk of chronic disease.

There are several reasons to eat plenty of plant foods, one of them being that diets rich in fruits, vegetables, pulses, whole grains, and nuts and seeds are associated with lowered disease risk and overall better health. One major reason likely has nothing to do with the vitamins and minerals—although those are important, too. It may be how they interact with the gut microbiota.

The link between diet and cardiometabolic health is well established, and accumulating research suggests that the gut microbiota may be a mediator of dietary impact on the host's metabolic status.1 Gut dysbiosis—the disturbance of healthy microbial communities—has been implicated in CVD and its risk factors, including atherosclerosis (a chronic inflammatory condition characterized by plaque formation in the arteries) and hypertension.2

High microbial diversity generally is associated with health, while lower diversity is linked with inflammatory bowel disease, type 1 and type 2 diabetes, and other disorders.3

Dietary Patterns and the Microbiota
The gut microbiota is the community of bacteria and other microbes—some 100 trillion of them—that live in the gastrointestinal tract, primarily in the large intestine. (The microbiome is the collective DNA of this community.) The gut microbiota begins developing in utero and continues rapidly for the first two to three years of life,4 forming our individualized "core" microbiota. However, environment, especially long-term dietary patterns, continue to shape the microbiota and its functions throughout the lifespan.3-5

Bacteroidetes and Firmicutes are the dominant bacterial phyla found in the gut, and diet-related shifts in the ratio of these groups have been of much interest,6 as is the idea of a microbial "enterotype" at the genus level (genus is several steps below phylum in bacterial taxonomy). The Bacteroides-dominant enterotype is associated with a Western-type diet high in protein and fat, while the Prevotella-dominant enterotype is associated with a diet higher in fiber, or microbiota-accessible carbohydrates (MACs).7

MACs are resistant to our digestive enzymes but are digestible by enzymes that gut microbes produce. They include resistant starch, nonstarch polysaccharides, and oligosaccharides.8

Research has found major differences in bacteria populations at the phylum level between the microbiota of Africans and South Americans, who have diets high in plant-based polysaccharides, and North Americans, who have lower fiber consumption.6,9 While dietary intervention studies have found that decreasing or increasing MACs alters the microbiota composition,6,10 short-term studies have found that one's "assigned" enterotype doesn't readily change.7 That doesn't mean diet doesn't matter—even if dietary interventions don't change the microbial population, they could change the metabolites they produce.

Speaking at the Nutrition & Health Conference in Boston in May, Emeran Mayer, MD, a professor in the departments of medicine, physiology, and psychiatry at the David Geffen School of Medicine at UCLA and author of The Mind-Gut Connection, used an orchestra analogy to describe the effects of dietary intervention: "The orchestra is hired in the first three years of life, but this orchestra can still play different tunes depending on what you pay the players and what you instruct them to play."

Mayer said food is one of the most important means of instruction. "Any intervention we do in an adult does not change the basic blueprint, but it influences what this orchestra puts out," he said.

Microbes, Plants, and Health
A diet rich in MACs can affect the microbiota directly and indirectly. Bacteria that thrive on fiber will increase in number and robustness on a MAC-rich diet, but so will groups of microbes that thrive on the byproducts of fiber degradation.6 Diverse microbiotas are associated with better health, while low diversity and dysbiosis is associated with chronic diseases like type 2 diabetes, inflammatory bowel diseases, rheumatoid arthritis, and asthma.

Diet is one factor—genetics, aging, stress, and antibiotic use are others—that can lead to dysbiosis.11,12

Gut Wall Integrity and Immune Health
What happens when individuals don't get enough MACs? Bacteria extract carbon from carbohydrates, but they also can get carbon from the glycoprotein-rich mucus that provides a protective barrier between microbes and the epithelial cells lining the intestine.11,13,14

RDs can think of the mucus layer as the gut wall's first line of defense. Lack of MACs leads to a mucus-degrading microbiota, allowing greater access to the epithelial cells by pathogenic bacteria.15 Bacteria that can thrive on both MACs and mucus will shift into mucus-degrading mode, while bacterial species that specialize in degrading mucus, including many pathogenic bacteria, will thrive at the expense of MAC degraders.2,11

On the other hand, a plant-based diet encourages growth of beneficial bifidobacteria, which don't eat mucus and thus help maintain the integrity of the gut wall. They also promote the production of glucagonlike-peptide (GLP-2), which regulates the expression of the proteins that make up the tight junctions between epithelial cells.2

Because the majority of immune cells are located in the gut wall, a diet with adequate MACs—and MAC-degrading microbes—can have significant effects on immune function by preserving the mucosal layer.11 The intestinal immune system navigates a fine line between allowing commensal (normal) microbes and resisting pathogenic microbes.16 One reason is short-chain fatty acids (SCFAs), which appear to play a role in regulating the function of many immune cells.11

SCFAs
SCFAs are byproducts of microbial fermentation of carbohydrates. SCFAs lower the pH of the intestine, helping to inhibit the growth of certain pathogenic microbes. They also act as signaling molecules, affecting gut motility. It's unclear whether positive health effects associated with SCFAs are due to the acids themselves or to their interactions with the other metabolites produced by a diverse, healthy microbiota.16

The primary SFCAs are acetate, butyrate, and propionate. Butyrate, which is the primary energy source for normal, healthy colon cells, guards against colon cancer and inflammation, in part because it helps protect a gene-expression pattern (epigenetic regulation) that discourages development and proliferation of cancer cells.16,17 It also helps protect against atherosclerosis.2

When a diet is low in MACs, microbes may metabolize protein—mostly in the form of peptides and amino acids that have escaped digestion in the small intestine—and dietary fat. This leads to an overall reduction in SCFA formation and an increase in potentially toxic microbial metabolites, such as branched-chain fatty acids, which may contribute to insulin resistance.16

Polyphenols
Several studies have found that dietary polyphenols—found in many plant foods, including fruits, vegetables, grains, tea, coffee, and wine—may positively affect the gut microbial population. Polyphenols generally have low bioavailability compared with vitamins and minerals, so their benefits may be largely due to their prebiotic properties—an estimated 5% to 10% are absorbed in the small intestine, while the rest make it to the colon virtually intact, where gut microbes break them down into more easily absorbed metabolites. These metabolites may be responsible for the health benefits associated with the consumption of polyphenol-rich foods.18

Many studies have linked the metabolism of dietary polyphenols in the gut to reduced cancer risk via various possible mechanisms. Polyphenol metabolites may up- or downregulate key enzymes, inhibit inflammatory cytokines, or reduce cell proliferation and increase apoptosis (programmed cell death).18

The Shifting Microbiota — Edging Toward Extinction?
People in traditional societies have dietary fiber intake between 50 and 120 g per day—compared with 15 g per day for the average American—and have much more diverse microbiotas. The Industrial Revolution ushered in a shift from traditional diets to the modern "Western diet," which is higher in sugar, fat, protein, and heavily processed foods, and lower in micronutrients and dietary fiber.11

Western microbiotas have 15% to 30% fewer species than non-Western microbiotas and lack certain species that consistently show up in non-Western microbiotas, including Xylanibacter, Prevotella, Butyrivibrio, and Treponema, which can ferment indigestible polysaccharides to produce high levels of SCFAs.11,19

Human populations with diets rich in complex carbohydrates have more diverse microbiotas, while populations with long-term high-fat, high-sugar, low-fiber diets may experience not only a decline in diversity, but the actual extinction of entire microbial groups.16,20 Mouse studies have shown that a loss of diversity can worsen over generations to the point where a high-MAC diet can't restore diversity.11

In their 2014 study "Starving the Microbial Self," Stanford microbiologists Erica and Justin Sonnenburg, PhDs, authors of the book The Good Gut, wrote that "it remains to be determined whether the simplified Western microbiota has lost species that cannot be recovered upon increased dietary MACs."21

Authors of an August 2010 study in Proceedings of the National Academy of Sciences of the United States comparing the microbiotas of children from Florence, Italy, with those from a small rural village in Africa found that the latter group consumed about twice as much fiber and had significantly greater microbial richness and diversity.19

However, a January 2016 study in Gut comparing the microbiota of vegans with omnivores in an urban US environment found few differences in microbiota composition, although they did find differences in blood levels of metabolites, including metabolites produced by the gut microbiota.22

Grains and Dietary Fats
Grains—even whole grains—get a bad rap from those following a low-carb or Paleo diet, but science supports their health benefits. At least some of the observed benefits of whole grains are mediated through their effects on the gut microbiota.

One study that looked at the effects of brown rice and whole grain barley found that test meals including those grains caused an increase in microbial diversity, possibly because whole grains contain a variety of carbohydrates and may affect a broader scope of bacterial species. These changes also coincided with reductions in the inflammatory cytokine interleukin 6 (IL-6) and improvements in glucose and lipid metabolism.23

One argument in support of eating more whole grains is that they tend to be more satiating than refined grains. However, the fiber content alone doesn't appear to account for this difference. It may be that SCFAs produced through the intestinal fermentation of the fiber in whole grains affects satiety.24 In particular, acetate, the most abundant SCFA in circulation outside the large intestine, can cross the blood-brain barrier and reduce appetite via a central homeostatic mechanism.16

Many studies on diet and the microbiota emphasize that a high-fat diet is linked to dysbiosis. But what type of fat? Some quality animal studies have found that diets high in saturated fats promote the proliferation of pathobionts, gut microbes that have the potential to perturb the immune system, contributing to chronic inflammatory health conditions. This hasn't been observed with plant-based poly- and monounsaturated fats, such as from avocados, olive oil, and nuts.12,25,26 However, these studies may or may not translate to human health outcomes, says Hannah D. Holscher, PhD, RD, an assistant professor of nutrition at the University of Illinois.

"Unfortunately, there's limited work investigating the impact of different types of fat (eg, saturated, mono- and polyunsaturated) on the human microbiota," says Holscher, who's the lead author of a study published in May in the Journal of Nutrition that found that, among the 18 healthy male and female participants, eating walnuts produced favorable changes in the gut microbiota, including an increase in butyrate-producing microbes.27 It also found significant reductions in the amount of proinflammatory secondary bile acids. Humans can't make secondary bile acids, but microbes can metabolize them from the primary bile acids secreted from the gallbladder.

"There are a number of nutrients in walnuts that may be contributing to changes in the human gastrointestinal microbiota, including fiber, unsaturated fatty acids, and phytonutrients," Holscher says. "We need additional studies that isolate these nutrients to be able to confidently say what nutrient or combination of nutrients in walnuts is causing the changes in the composition of the microbiota."

What About FODMAPs?
While the benefits of a diet rich in fermentable fiber are evident, it's a diet that can be problematic for patients with irritable bowel syndrome (IBS). When an IBS patient is also vegetarian or vegan, it becomes even more complicated.

Boston-based dietitian Kate Scarlata, RDN, LDN, author of The Low-FODMAP Diet Step by Step, says that the gut microbiota of IBS patients appear to be less stable compared with those without IBS, and their fiber intake varies widely.

"Eating a variety of fibers is important for gut health, and registered dietitians should work with their IBS patients to slowly up their fiber intake to their personal tolerance," she says. "IBS patients can consume a high-fiber diet, but I find increasing fiber slowly works best and trying a variety of different fibers to assess tolerance is key."

For example, IBS patients with diarrhea tend to be bothered by insoluble fiber foods, such as those in large salads.

For IBS patients with additional food intolerances or limitations, such as a vegan diet, Scarlata limits the elimination phase of the low-FODMAP diet to two weeks, generally enough time to assess whether they're FODMAP sensitive.

She says a well-designed low-FODMAP diet generally can provide all the nutrients and fiber a patient needs. However, in patients following a vegan diet, the low-FODMAP diet can fall short, particularly in calcium, iron, and protein. A few low-FODMAP vegan plant protein sources include 1/4 cup canned chickpeas, 1/2 cup canned lentils, a handful of suitable nuts and seeds (peanuts, walnuts, macadamia, pecans, chia, hemp, flax), buckwheat, quinoa, tempeh (made with low-FODMAP ingredients), and firm tofu.

(Scarlata says firm tofu has its water-soluble galacto-oligosaccharides drained off, while silken tofu does not.)

Counseling Strategies for RDs
Plant-based diets can take many forms, from vegan and vegetarian to flexitarian and omnivore. The common denominator is that they make plant foods the focal point of the plate.

However, when many patients hear "plant-based," they think "vegan." Telling patients that "plant-based" doesn't mean "plant-only" may help them become more receptive to making gradual changes they can enjoy and sustain. That's important, because long-term dietary patterns matter most for shaping the microbiota. Here are a few places to start:

• Eat vegetarian one day per week (perhaps establishing "Meatless Mondays"), then try adding a few more vegetarian meals during the week.
• Move away from the "meat as the center of the plate" eating style. Choose more veggie-rich dishes, such as entrée salads, whole grain dishes, curries, etc. Use meat as a seasoning, as many cultures do around the world—one portion can flavor a whole family-sized meal in dishes like stews, casseroles, pastas, and stir-fries.
• Base more meals on beans and lentils, such as chili, bean burritos, or lentil soup, and convert favorite dishes like lasagna, spaghetti, and tacos to meatless versions.
• For patients who strongly prefer a higher-protein, higher-fat diet, make sure they're also getting enough dietary fiber.
• Many patients are unfamiliar with how to cook whole grains or dried beans—and are bored with their usual ways of preparing vegetables. Provide handouts or web links with instructions on cooking methods, and perhaps some simple recipes that you've tested and vetted.

— Carrie Dennett, MPH, RDN, CD, is the nutrition columnist for The Seattle Times and speaks frequently on nutrition-related topics. She also provides nutrition counseling via the Menu for Change program in Seattle.

References
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