April 2018 Issue

The Facts About Fermented Foods
By Carrie Dennett, MPH, RDN, CD
Today's Dietitian
Vol. 20, No. 4, P. 24

Looking Beyond the Hype to the True Health Benefits

Food scientist Keith Steinkraus, PhD, once wrote, "The processes required for fermented foods were present on earth when man appeared on the scene. … When we study these foods, we are in fact studying the most intimate relationships between man, microbe, and foods."1

It's an elegant way to describe what might otherwise sound like rot. Fermentation is the slow, controlled decomposition of organic substances by microorganisms or enzymes of plant or animal origin.2 Not only does fermentation convert sugars into acids, alcohols, and carbon dioxide—useful for both health and culinary purposes—but it also provides several other benefits. Most notable are enhancement of nutrients, removal of antinutrients, delivery of probiotic bacteria, and inhibition of foodborne pathogens.2-4

"Humans have been consuming fermented foods and beverages for thousands of years," says Robert Hutkins, PhD, a researcher and professor of food science at the University of Nebraska-Lincoln. "Indeed, during much of human civilization, a major part of the human diet probably consisted of bread, yogurt, olives, sausages, wine, and other fermentation-derived foods. They can be considered perhaps as our first 'processed foods.'"1,4

Fermentation produces many antimicrobial end products, including alcohol and acids, which act as a biological method of food preservation.4 Modern use of chemical preservatives and refrigeration, combined with industrialization of the food supply, has reduced the use of fermented foods in the West, although they remain part of many traditional cuisines. Today, fermented foods and beverages account for about one-third of the global human diet and, as knowledge about the human gut microbiota increases, so has interest in fermented foods.1,3,4 Some experts even recommend that fermented foods be included in national dietary recommendations.2,4

Given the long history of fermented foods, Hutkins says researchers like himself—his lab studies bacteria important in fermented foods and human health—are a bit surprised that fermented foods suddenly have become trendy. "Consumers are now more interested than ever in fermented foods, from ale to yogurt, and all the kimchi and miso in between," he says. "This interest is presumably driven by all the small/local/craft/artisan manufacturing of fermented foods and beverages, but the health properties these foods are thought to deliver are also a major driving force."

Mechanics of Fermentation
The most frequently used microbes in fermentation are bacteria and yeast. Yeast fermentation produces alcohol and carbon dioxide. For example, different strains of Saccharomyces cerevisiae produce carbon dioxide to help bread dough rise or alcohol in beer and wine production. Bacterial fermentation produces acid. For instance, many types of bacteria—including Lactobacillus, Streptococcus, Enterococcus, Lactococcus, and Bifidobacterium—collectively known as lactic acid bacteria (LAB), convert sugar or other carbohydrates to lactic acid.2,4 Wine, "sour" beers, and kombucha fermented tea use a multistep fermentation with both yeast and bacteria.3

There are thousands of food-microbe combinations, which means there are thousands of different fermented foods and beverages, each with unique flavors and textures.4 For example, during yogurt fermentation, lactic acid-producing bacteria feed on the sugars and other nutrients in milk, producing compounds that change the flavor, texture, and nutrients.5

Fermentation may occur naturally and spontaneously or through careful addition of a starter culture.2 With some fermented foods, microbes are still alive when consumed. These include fresh kimchi, sauerkraut, and sour dill pickles as well as yogurt, kefir, kombucha, unpasteurized miso, some cheeses, water- or brine-cured olives, traditional salami, and European-style dry fermented sausages. Microbrewed beer that hasn't been filtered or heated still contains live yeasts and bacteria.6

With other foods, these microbes are destroyed with further processing, such as heating, baking, pasteurization, or filtering. These include tempeh, most soy sauce, most beer and wine, sourdough bread, chocolate, and shelf-stable sauerkraut and kimchi. Fresh cheeses, including cottage cheese, are heated. Aged cheese may not contain many live bacteria, since most die during storage.6

California-based dietitian and cookbook author Jill Nussinow, MS, RDN, aka The Veggie Queen, an adjunct chef instructor at Santa Rosa Junior College, frequently gives talks to consumers about fermented foods. "They often think that foods that might be fermented such as pickles and sauerkraut but are canned, processed, or pasteurized still have beneficial probiotic effects. They also do not understand that food such as yogurt doesn't always have active cultures."

State of the Science
Mary Ellen Sanders, PhD, executive science officer for the International Scientific Association for Probiotics and Prebiotics (ISAPP), says the research on functional health benefits of fermented foods is evolving. "We need more randomized, controlled trials on defined fermented foods so we can better understand the health benefits associated with their consumption," she says. "Mechanistic studies are needed to better understand what aspects of a fermented food—the live microbe, a fermentation-derived metabolite, or nutrition—contribute to conferring the benefit."

Sanders says there's evidence that some fermented foods are associated with healthier blood lipid profiles, improved glucose tolerance, improved digestive function and, in the case of yogurt, improved tolerance to lactose. However, their renewed popularity can oversimplify a complex area of science. "There's little downside to consuming fermented foods as part of a healthful diet, and, in fact, there may be benefits. But it's important not to let the hype get ahead of the science," Sanders says.

Are Fermented Foods Probiotics?
Fermented foods with live cultures may contribute to the health of the gut microbiota, in turn reducing the risk of some acute and chronic diseases.5 But, as mentioned, some fermented foods don't retain live cultures. Those that do don't necessarily have probiotic functions. One common myth about fermented foods is that they're the same thing as probiotics. The World Health Organization defines probiotics as live microorganisms, which, when administered in adequate amounts, confer a health benefit on the host.7 "To be a probiotic food, a fermented food must retain an adequate level of live microbes that have been shown to have a health benefit. Not all fermented foods reach that bar," Sanders says.

"Demonstrating that a microorganism actually confers a health benefit is a key point and requires substantial clinical evidence, including randomized clinical trials," Hutkins says. "Importantly, such studies also require that specific and well-defined microbial strains are used." For example, Lactobacillus rhamnosus GG is a known probiotic, and referred to by genus, species, and strain.

Hutkins says live microorganisms in fermented foods rarely are characterized or defined, let alone tested to determine whether they confer probiotic health benefits. One reason may be logistical; the specific organisms in foods such as kimchi, sauerkraut, and miso vary by batch, manufacturer, and location. The one exception is yogurt. "European health authorities have determined that even the generic yogurt bacteria can help improve digestion of lactose among individuals with lactose maldigestion," Hutkins says.

Science and industry are moving far beyond "artisan," aiming to provide specific health benefits by optimizing starter cultures and producing fermented functional foods.3,8 Hutkins gives the example of probiotic bacteria added to fermented foods such as yogurt, kefir, or kombucha. "These foods are essentially serving as the delivery vehicle for the probiotic," he says. "In this case, adding the probiotic to fermented foods makes sense, since they will be kept cold, and any acid or sourness they might produce would hardly be noticed. Some foods (especially dairy) also may protect the organisms during digestion."

Sanders points to examples of several foods that contain true probiotics: Yakult (L casei Shirota), Activia (Bifidobacterium animalis DN-173 010/CNCM I-2494), Nancy's yogurt (B lactis BB-12), Dahlicious Lassi (B lactis BB-12 and L acidophilus LA-5), Good Belly (L plantarum 299v), Gerber Good Start Infant Formula (B lactis BB-12), and Tropicana Probiotic juice (B lactis HN019).

Link to Gut Health: The Big Picture
Many fermented foods contain 1 million to 1 billion viable microbes per gram or milliliter, and a large portion of those survive passage through the digestive tract, so eating fermented foods could increase the number of microbes in the diet by up to 10,000-fold. While these microbes may play only a transient role in an individual's native microbiota, they still have demonstrated benefits, including benefits for brain and immune function.4 But is this because they're probiotic? This is where Hutkins says it gets interesting.

"Organisms in sauerkraut, kimchi, and other fermented foods are often closely related, even to the species level, to organisms that have been reported to have probiotic functions," Hutkins says. "For example, one of the most abundant organisms in sauerkraut and kimchi is Lactobacillus plantarum. One particular strain called L plantarum 299v, is a very well-studied probiotic that is added to a range of commercial foods and supplements. So do the wild strains of L plantarum share the same traits that make 299v a probiotic?"

This question was addressed at a recent ISAPP meeting. "The researchers suggested that there were health benefits that were indeed strain-specific, whereas others were more general and likely shared by most members of the same species or even genus," Hutkins says.

On one hand, many species of Lactobacillus and Bifidobacterium help crowd out pathogens, maintain gut barrier function, and produce organic acids that nourish colonic cells and enhance gut health. Some immune effects also may be shared broadly among similar species. On the other hand, certain clinical benefits—such as production of a particular vitamin in the gastrointestinal tract or a particular immune effect—may be limited to a specific strain.

Transforming Nutrients and Bioactives
Even though live cultures are one important way fermented foods can benefit consumers, Hutkins says it's not the only way. "Wine is free of organisms at the time of consumption, but the yeasts produce ethanol during fermentation and the ethanol enhances extraction of phenolic compounds from the grapes. These phenolics have antioxidant activity known to have many health benefits, ranging from heart health to systemic anti-inflammatory effects. Likewise, the bacteria and yeast used in the manufacture of sourdough bread are inactivated during the baking process, but during fermentation, sourdough bacteria combined with enzymes may degrade part of the gluten—although not quite enough to be gluten-free." This is why many people with nonceliac gluten sensitivities find they can tolerate breads that have long fermentations.

The enzymatic and microbial activity of fermentation also can enrich the content of protein, fatty acids, and micronutrients.3 Fermented dairy often is more digestible than nonfermented milk because microbes digest lactose and break down proteins into peptides (small protein fragments) and amino acids.2,4 In addition, dairy peptides have antimicrobial and antioxidant properties and may contribute to reduced risk of hypertension and improved immune response.4,9

Fermentation of fiber-rich foods can produce novel bioactive compounds that may have benefits for immunity, glycemic response, and an inflammatory state.1 It can also do the following:

• increase the bioavailability of nutrients, including the B vitamins, magnesium, and zinc1,4;
• resynthesize some of the folate that's destroyed by heat during milk pasteurization2;
• convert unsaturated fatty acids such as linoleic and linolenic acids to conjugated linoleic acid, which has demonstrated anti-inflammatory and antioxidant properties9;
• improve the polyphenol and vitamin content and reduce the amount of caffeine in tea3;
• remove or reduce toxic or antinutrients in raw foods, such as phytic acid, and increase food safety and shelf life4,5;
• produce a form of the neurotransmitter gamma-aminobutyric acid that may help reduce anxiety1,10; and
• create the bioactive isoflavones genistein and daidzein out of their precursors in soyfoods.3

Fermented Foods, Cancer, and Food Safety
There's been some concern about links between fermented vegetables and increased risk of certain cancers, primarily gastric and esophageal. This is largely based on retrospective epidemiological evidence gathered from cancer registries established in China in the 1960s.11 However, other factors also may increase gastric cancer risk—in some areas of China where data were gathered, smoking, high-fat diets, and/or high consumptions of barbecued meat were common. In addition, in some areas, pickled vegetables constituted a large proportion of the daily diet, and fresh vegetables were virtually absent, which itself can increase gastric cancer risk.12

Researchers do know that certain microorganisms associated with pickled foods (including fungi) can convert nitrates and nitrites into N-nitroso compounds (NOCs), which may be carcinogenic.11 The increased risk of gastric cancer may be due to an interaction between infection with Helicobacter pylori bacteria and exposure to NOCs, as H pylori alone doesn't lead to gastric cancer in most cases.13 It's worth noting that pickled foods are higher in salt, and high salt intake may encourage H pylori growth.13

What about other aspects of safety? Nussinow frequently hears concerns that fermented food is "spoiled food" and can be dangerous. However, fermentation, especially with LAB, can improve shelf life and enhance food safety by inhibiting growth of foodborne pathogens and degrading toxins, such as aflatoxin. Fermented foods, whether produced in the home or industrially, have a good safety record, and LAB strains in particular have a long history of safety. However, fermentation doesn't eliminate risk, and new emergent strains of bacteria should have their safety confirmed through research studies.3

Benefits in the Kitchen and on the Plate
Another benefit of fermentation is that it creates desirable tastes and textures. For example, fermentation removes the bitter taste from fresh table olives—making them edible—and turns flour, water, and salt into leavened bread dough.4 "Parmesan, Roquefort, and aged cheddar cheese. A tart cup of yogurt or effervescent kefir. A crusty sourdough rye bread. Miso soup. Kalamata olives. Cabernet sauvignon. They enrich our lives in so many ways," Hutkins says.

In fact, the flavor factor may be a good tool for helping patients incorporate more fermented foods in their diets. Nussinow suggests adding pickle or sauerkraut juice to mixed grain bowls for more umami flavor. The juice—along with miso and plain yogurt—are good choices for patients who can't tolerate fermented vegetables. "Fermented foods have the ability to turn a bowl of brown rice into an 'exotic, gourmet' meal. Nothing like a bowl with brown rice and veggies with some kimchi on top and a drizzle of tahini—at least for me."

— 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

1. Selhub EM, Logan AC, Bested AC. Fermented foods, microbiota, and mental health: ancient practice meets nutritional psychiatry. J Physiol Anthropol. 2014;33:2.

2. Chilton SN, Burton JP, Reid G. Inclusion of fermented foods in food guides around the world. Nutrients. 2015;7(1):390-404.

3. Borresen EC, Henderson AJ, Kumar A, Weir TL, Ryan EP. Fermented foods: patented approaches and formulations for nutritional supplementation and health promotion. Recent Pat Food Nutr Agric. 2012;4(2):134-140.

4. Marco ML, Heeney D, Binda S, et al. Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol. 2017;44:94-102.

5. Hutkins R. Fermented foods. International Scientific Association for Probiotics and Prebiotics website. https://isappscience.org/fermented-foods/. Accessed January 24, 2018.

6. Campbell K. Your guide to the difference between fermented foods and probiotics. Gut Microbiota News Watch website. http://www.gutmicrobiotaforhealth.com/en/guide-difference-fermented-foods-probiotics/. Published July 26, 2017. Accessed January 20, 2018.

7. Morelli L, Capurso L. FAO/WHO guidelines on probiotics: 10 years later. J Clin Gastroenterol. 2012;46 Suppl:S1-S2.

8. Leroy F, De Vuyst L. Fermented food in the context of a healthy diet: how to produce novel functional foods? Curr Opin Clin Nutr Metab Care. 2014;17(6):574-581.

9. Fernández M, Hudson JA, Korpela R, de los Reyes-Gavilán CG. Impact on human health of microorganisms present in fermented dairy products: an overview. Biomed Res Int. 2015;2015:412714.

10. Kim B, Hong VM, Yang J, et al. A review of fermented foods with beneficial effects on brain and cognitive function. Prev Nutr Food Sci. 2016;21(4):297-309.

11. Islami F, Ren JS, Taylor PR, Kamangar F. Pickled vegetables and the risk of oesophageal cancer: a meta-analysis. Br J Cancer. 2009;101(9):1641-1647.

12. Ren JS, Kamangar F, Forman D, Islami F. Pickled food and risk of gastric cancer — a systematic review and meta-analysis of English and Chinese literature. Cancer Epidemiol Biomarkers Prev. 2012;21(6):905-915.

13. Gancz H, Jones KR, Merrell DS. Sodium chloride affects Helicobacter pylori growth and gene expression. J Bacteriol. 2008;190(11):4100-4105.

RESOURCES

• International Scientific Association for Probiotics and Prebiotics: https://isappscience.org
The Art of Fermentation: An In-Depth Exploration of Essential Concepts and Processes From Around the World by Sandor Ellix Katz
• National Center for Home Food Preservation: http://nchfp.uga.edu


TYPES OF MICROBES

While this isn't a comprehensive list, it gives an overview of types of bacteria and fungi frequently used in fermentation, whether as part of a starter culture or as backslopping (inoculation with part of the previous batch).2,4

Bacteria
Acetobacter xylinum (kombucha)
Bacillus subtilis var. natto (natto)
Gluconacetobacter kombuchae (kombucha)
Lactobacillus bulgaricus (yogurt, sausage), L plantarum (olives, kefir, sauerkraut), L reuteri and L sanfranciscensis (sourdough bread), L brevis (beer)
Lactococcus lactis (cheese, sour cream, crème fraîche)
Leuconostoc mesenteroides (cheese, sour cream, sauerkraut, kimchi)
Oenococcus oeni (wine)
Pediococcus acidilactici (sausage)
Saccharomyces cerevisiae (wine, beer, kefir, bread starter)
Staphylococcus carnosus and S xylosus (sausage)
Streptococcus thermophilus (yogurt)
Tetragenococcus halophilus (soy sauce, miso)

Yeasts and Molds
Aspergillus soyae (soy sauce, miso)
Candida humilis (sourdough)
Debaryomyces hansenii (cheese)
Penicillium roqueforti (cheese)
Trichosporon ovoides (cheese)
Yarrowia lipolytica (cheese)
Zygosaccharomyces rouxii (soy sauce, miso), Z kombuchaensis (kombucha)

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