research paper on fermented foods

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• RESEARCH HIGHLIGHT
• 23 August 2021

Health benefits of fermented foods

• Karen O’Leary 0

Karen O’Leary is an Associate Research Analysis Editor with Nature Medicine.

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It is well known that diet influences the gut microbiome, which in turn can affect host health. Microbiome changes caused by ‘westernized’ diets are linked to increases in inflammation, BMI and other markers of poor health, whereas high-fiber and fermented foods are associated with health benefits including reduced risk of certain diseases.

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doi: https://doi.org/10.1038/d41591-021-00053-1

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REVIEW article

Fermented foods as a dietary source of live organisms.

• Department of Food Science and Technology, University of Nebraska—Lincoln, Lincoln, NE, United States

The popularity of fermented foods and beverages is due to their enhanced shelf-life, safety, functionality, sensory, and nutritional properties. The latter includes the presence of bioactive molecules, vitamins, and other constituents with increased availability due to the process of fermentation. Many fermented foods also contain live microorganisms that may improve gastrointestinal health and provide other health benefits, including lowering the risk of type two diabetes and cardiovascular diseases. The number of organisms in fermented foods can vary significantly, depending on how products were manufactured and processed, as well as conditions and duration of storage. In this review, we surveyed published studies in which lactic acid and other relevant bacteria were enumerated from the most commonly consumed fermented foods, including cultured dairy products, cheese, fermented sausage, fermented vegetables, soy-fermented foods, and fermented cereal products. Most of the reported data were based on retail food samples, rather than experimentally produced products made on a laboratory scale. Results indicated that many of these fermented foods contained 10 5−7 lactic acid bacteria per mL or gram, although there was considerable variation based on geographical region and sampling time. In general, cultured dairy products consistently contained higher levels, up to 10 9 /mL or g. Although few specific recommendations and claim legislations for what constitutes a relevant dose exist, the findings from this survey revealed that many fermented foods are a good source of live lactic acid bacteria, including species that reportedly provide human health benefits.

Introduction

Fermentation has long been used to preserve and enhance the shelf-life, flavor, texture, and functional properties of food ( Hutkins, 2018 ). More recently, the consumption of fermented foods containing live microorganisms has emerged as an important dietary strategy for improving human health ( Marco et al., 2017 ). In general, lactic acid bacteria (LAB) from several genera, including Lactobacillus, Streptococcus , and Leuconostoc are predominant in fermented foods, but other bacteria as well as yeast and fungi also contribute to food fermentations. Commercially-produced fermented foods also frequently serve as carriers for probiotic bacteria. Despite this interest and the potential public health benefits of these foods, there is still considerable confusion about which fermented foods actually contain live microorganisms, as well as understanding the role of these microbes on the gut microbiome ( Slashinski et al., 2012 ).

Nonetheless, yogurt and other cultured dairy products are generally perceived by consumers as good sources of live and health-promoting organisms ( Panahi et al., 2016 ). Moreover, in a survey of 335 adults, yogurt was the main food associated with probiotic bacteria ( Stanczak and Heuberger, 2009 ). However, the actual concept of fermentation is evidently not so familiar—a survey of 233 college students attending Brescia University College in London, Ontario revealed that nearly two-thirds were unfamiliar with the term “fermented dairy products,” and about the same percent were unsure that several cultured dairy products were fermented ( Hekmat and Koba, 2006 ).

That a particular food or beverage is produced by fermentation does not necessarily indicate that it contains live microorganisms. Bread, beer, wine, and distilled alcoholic beverages require yeasts for fermentation, but the production organisms are either inactivated by heat (in the case of bread and some beers) or are physically removed by filtration or other means (in the case of wine and beer). Moreover, many fermented foods are heat-treated after fermentation to enhance food safety or to extend shelf-life. Thus, fermented sausages are often cooked after fermentation, and soy sauce and sauerkraut and other fermented vegetables are made shelf-stable by thermal processing. Some products, such as many of the commercial pickles and olives, are not fermented at all, but rather are placed into brines containing salt and organic acids. Even non-thermally processed fermented foods may yet contain low levels of live or viable organisms simply due to inhospitable environmental conditions that reduce microbial populations over time. It is important to note, however, that the absence of live microbes in the final product does not preclude a positive functional role. For example, food fermentation microbes may produce vitamins or other bioactive molecules in situ or inactivate anti-nutritional factors and yet be absent at the time of consumption.

Labeling Live Microbes in Fermented Foods and Beverages

Yogurt, kefir, and other cultured dairy product manufacturers have long promoted the presence of live cultures. Indeed, the “live and active” seal was created by the National Yogurt Association (NYA), for yogurt products in the United States containing at least 100 million cells or cfu per gram at the time of manufacture ( Frye and Kilara, 2016 ). According to the NYA, the “live and active” seal refers only to yogurt cultures, and specifically to the two species that comprise such cultures, Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus . However, frozen yogurt, kefir and other cultured dairy products also claim the presence of live and active cultures, even though the microorganisms may be different than those found in yogurt. In the U.S., there is no regulatory requirement to state microbial levels, thus these label declarations are strictly voluntary.

In contrast, in other regions, the number of live microbes present in yogurt and other cultured dairy products must satisfy regulatory requirements. For example, according to the CODEX standards for fermented milk products, the minimum number of starter culture bacteria in yogurt is 10 7 cfu per g (CODEX STAN 243-2003). If other organisms are indicated on the label, they must be present at 10 6 cfu per g. Nonetheless, in Europe, to make a claim for yogurt containing live cultures for improving lactose digestion, the European Food Safety Agency requires a minimum of 10 8 cfu per g of live bacteria ( EFSA Panel on Dietetic Products, Nutrition and Allergies, 2010 ). In contrast, in Australia and New Zealand, a minimum of only 10 6 cfu per g is required ( Commonwealth of Australia Gazette, 2015 ).

For many years, cultured dairy products were the only fermented foods that included label declarations regarding the presence of live microorganisms. Label declarations on sauerkraut or kimchi or miso, had, until recently, been rare. The popularity of artisan-style fermented foods ( Johnson, 2016 ) and interest in their health properties ( Marco et al., 2017 ) has led more manufacturers to inform consumers, via food labels, that their products contain live microorganisms. In some cases, the species in these types of foods have been identified and then compared to label claims ( Yeung et al., 2002 ; Scourboutakos et al., 2017 ). However, to our knowledge, data on the actual levels of live microorganisms in most fermented retail products has not readily been reported or summarized in an organized form. Therefore, consumers, despite their interest in probiotics and functional fermented foods ( Linares et al., 2017 ), have had little access to this useful information.

Survey Design

The purpose of this study, therefore, was to survey the scientific literature and identify published papers in which the number of live microorganisms in a range of fermented foods was reported. Included were so-called western-fermented foods such as yogurt, cheese, and sausage, as well as soy-based and cereal-based fermented foods that are widely consumed in other regions ( Tamang et al., 2016 ). We then organized and summarized the quantitative data from those reports. Our interest was focused on those reports in which foods were obtained from retail locations or were made under manufacturing conditions. Thus, reports describing results from experimentally-produced fermented foods on a laboratory or pilot scale were excluded, in part because they do not reflect commercial processing, distribution, and storage conditions as do retail products. A large number of the reports in the literature in which levels of microbes in fermented foods were described were of this sort. In addition, many reports have analyzed the importance of microbial food safety and hygienic conditions of fermented food products and have reported the presence of spoilage microorganisms or food pathogens. However, the organisms responsible for fermentation and that are commonly present in the finished products were the focus of this current study.

Search Criteria

Scientific articles were chosen that satisfied specific parameters relevant to our stated goals. Specifically, our database search (Google Scholar, WorldCat, Scopus, and PubMed) focused on those studies that enumerated microorganisms exclusively in fermented food products. Keywords for these searches included, but were not limited to, the type of fermented food analyzed and, “commercially produced,” “commercial product,” “enumerated,” “lactic acid bacteria,” “microbial characterization,” “probiotic,” and “culture.” Food products that served only as vehicles for delivery of probiotic microorganisms were not included. Thus, studies that reported counts for frozen yogurt were included, but studies on ice cream containing probiotic microorganisms were not. In general, results were only included for commercial products, bought at retail locations, or those experimentally-produced under industrial manufacturing conditions. Thus, strictly experimental products (e.g., made in a laboratory or under small experimental-scale conditions) were not considered. The only exceptions were for products for which little or no data from retail or industrially manufactured sources was available. In those cases, lab- or pilot-scale-produced products were included, provided they were made using traditional manufacturing methods. No restrictions for date, location, or language were applied.

Data Reporting

For most products, quantitative data relied on cultural methods using well-established types of differential, selective, and general purpose media, as well as appropriate incubation conditions. LAB were the main group described, although other bacterial groups were occasionally reported. Some studies reported single microbial counts, whereas other reported ranges. Although papers reported counts either as log or as actual values, all of the data described in this review are shown as logs. For some products, values were estimated from graphs or figures. When products were held for shelf-life or aging studies, the counts from multiple times points are shown. Otherwise, single time-point data was reported. The region or origin of product manufacture was also noted.

General Survey Results

Approximately 400 published studies were reviewed in which fermented foods were characterized for the presence of live microorganisms. However, about three-fourths were excluded and not used in our results. Several excluded studies focused on development of selective methods for distinguishing between different species of LAB, determining ratios (e.g., cocci-to-rods in yogurt), or for enumerating only probiotics organisms. Although most studies reported data based on traditional plating methods, many of the more recent studies reported abundance data (i.e., 16S rRNA-based community sequencing). Because the latter 16S-based methods also detect non-viable cells, these studies were excluded unless total counts were also reported. Ultimately, more than 140 studies were included in our survey. Although the literature from which the results were assembled covers a 50 year period and a range of different regions and methodologies, the results are remarkably consistent. As summarized below, nine groups of fermented foods were reviewed in this survey. These included yogurt and other cultured dairy products, cheese, fermented meats, fermented vegetables, traditional fermented Asian products, fermented cereals, beer, and fermented tea (Kombucha).

Yogurt and Other Cultured Dairy Products

Studies were conducted for retail or commercially manufactured yogurts and other cultured dairy products obtained in the U.S., Australia, Spain, France, Norway, Greece, Argentina, and South Africa (Table 1 ). All of the yogurts examined contained the yogurt culture organisms, S. thermophilus and L. delbrueckii subsp. bulgaricus , at levels ranging from < 10 4 to 10 9 cfu/g or ml. In general, counts for S. thermophilus were somewhat higher than for L. delbrueckii subsp. bulgaricus . In several studies, other microorganisms, including Bifidobacterium spp. and Lactobacillus spp., were also enumerated. Levels of the latter ranged from undetectable (< 10 cfu/g) to 10 8 cfu/g. The addition of these probiotic bacteria did not appear to have any effect on levels of the yogurt culture organisms. Although most studies reported counts at only a single time point, other studies reported initial counts as well as at a second time point, usually considered end-of-shelf-life. In such cases, counts were generally similar at both time points (>10 6 cfu/g), provided samples were stored at refrigeration temperatures ( Hamann and Marth, 1984 ).

Table 1 . Organisms in commercial yogurt products by region.

In addition to fresh yogurt, frozen yogurt was also examined for bacteria. Results from several studies indicates that when these products were assessed for the relevant yogurt LAB, levels were generally similar to fresh yogurt, with counts ranging from 10 4 to 10 9 cfu/g. The stability of lactic cultures in frozen yogurt during long-term storage at freezer temperature (-23 C) has also been studied ( Lopez et al., 1998 ). In general, LAB ( S. thermophilus and L. delbrueckii subsp. bulgaricus ) survived beyond the designated shelf-life period (1 year), with less than a 0.5 log reduction for most samples.

The number and type of live microorganisms in other cultured dairy products have also been reported (Table 2 ). These include kefir, cultured buttermilk and simply “fermented milk.” As for other cultured dairy products, populations of LAB were in the 10 5 –10 9 cfu/g range.

Table 2 . Organisms in commercial cultured dairy products separated by product.

Although considerable microbiological data for cheese exists, most of these reports are concerned with microorganisms having public health or cheese quality implications. Still, levels of lactic acid and related bacteria were reported for more than 30 types of cheese from 18 countries including the United States, Italy, France, Germany, Mexico, Ireland, and South Africa (Table 3 ). Many papers reported the microorganisms as mesophilic streptococci, lactococci, and lactobacilli or as thermophilic streptococci and lactobacilli. Others reported total microorganisms and total LAB. For most products, only one time period was recorded (usually the most aged sample). Microbial counts ranged from undetectable (< 10 3 cfu/g) to 10 9 cfu/g, with the highest levels found in Tilsit cheese (typically aged 2–4 months). In contrast, Grana Padano aged 1 year, Parmesan aged greater than 1 year, and Swiss Gruyere aged greater than 1 year all showed no detectable microorganisms (< 10 3 cfu/g). As noted for other products, the methods used by the investigators may have influenced the reported data. Thus, enumeration of selected organisms (e.g., S. thermophilus ) was only possible if the appropriate medium and growth conditions were used.

Table 3 . Organisms in commercial cheese separated by product.

Fermented Meats

Microbial counts for fermented sausages are shown in Table 4 . In general, samples were either obtained from retail, directly from manufacturers, or were produced via industrial conditions. Most samples were from the United States, Spain, Portugal, and Italy and were composed of pork and/or beef. The levels of microorganisms (LAB and total) ranged from undetectable (< 10 2 cfu/g) to 10 10 cfu/g. Data were reported as either within the product shelf life or after ripening or maturation of the sausage. Counts of viable microorganisms in sausages from the United States were generally lower (< 10 7 cfu/g) compared to sausages from other countries. In particular, LAB levels were all < 10 6 cfu/g. In contrast, several of the European sausages contained high levels of LAB (>10 8 cfu/g.). European sausages were more often artisan sausages from smaller manufacturers, although similar microorganisms are used in comparison to sausages from the United States.

Table 4 . Organisms in commercial sausage products by region.

Fermented Vegetables

Microbial counts for fermented vegetables, including sauerkraut, olives, mustard pickles, pickles, and kimchi are summarized in Table 5 . Fermented cucumbers products were also considered (listed as pickles). Laboratory-manufactured products, using industrial or traditional practices, were included due to the lack of literature on fermented vegetables from retail sources.

Table 5 . Organisms in fermented vegetables separated by product.

Microbial counts for sauerkraut were generally reported as LAB with counts ranging from 10 3 to 10 8 cfu/g. Reported samples were for sauerkraut originating from the United States, Finland, and Croatia. Levels of LAB and Lactobacillus were reported for olives produced in Italy, Greece, Portugal, Spain, and the United States. These products contained 10 4 to 10 8 cfu/g and were between 30 and 200 days.

Other products for which quantitative data were reported included mustard pickles and kimchi from Taiwan and pickled cucumbers from China, India, and the United States. Microbial counts ranged from undetectable (< 10 1 ) to 10 8 cfu/g. For several of these products, levels of species (e.g., Lactobacillus plantarum, Lactobacillus brevis , and Pediococcus cerevisiae ) were reported. Species of Leuconostoc, Weissella and Lactobacillus were also reported for Korean kimchi, where they were generally present between 10 7 and 10 8 cfu/g.

Traditional Asian Fermented Products

Another group of fermented foods that contain lactic acid bacteria and other bacteria are those products traditionally manufactured in Asia and that rely on grain or legume substrates. One important difference in the fermentation of these food products compared to other fermented foods is the reliance on fungal enzymes to convert complex carbohydrates to simple sugars. Aerobic conditions are another unique characteristic used in various parts of the fermentation process. Data were collected for several products, including miso, tempeh, fish sauce, and fermented fish (Table 6 ). Similar to the fermented vegetables, there were few reports on products from retail sources. Therefore, laboratory manufactured products made using industrial or traditional practices were included. In general, aerobic bacteria counts of miso ranged from 10 2 to 10 7 cfu/g. Similar bacterial counts were reported for fish sauce. LAB counts for tempeh and fermented fish were between 10 3 to 10 7 cfu/g with fermented fish being at the lower end of the range.

Table 6 . Organisms present in traditional Asian fermented products separated by product.

Fermented Cereals

Fermented porridges and gruels are widely consumed in many African countries. Here, studies were reported from Burkina Faso, Uganda, Ghana, Benin, Tanzania, and Mexico (Table 7 ). These cereals were made using pearl millet, millet, sorghum, and maize as starting grains. In general, the cereals contained LAB and mesophilic aerobic bacteria with a range of 10 5 to 10 9 cfu/g.

Table 7 . Organisms in commercial fermented cereals from Africa and Mexico.

Several sour beer products from Belgium, such as lambic and gueuze, were included in the survey (Table 8 ). LAB counts were reported for these products, ranging from 10 2 to 10 5 cfu/g. The age of the products reported in the table refers to the longest time the beer was left to age. This maximum aging time was found to range from 40 days to 5 years across the different products.

Table 8 . Organisms in commercial sour beer products.

Fermented Tea (Kombucha)

Kombucha is a fermented beverage made from sweetened tea to which a specialized culture is added. The latter is comprised of a s ymbiotic c ulture o f b acteria and y east or SCOBY, normally within a cellulose-type membrane. Bacteria commonly found in kombucha include the acetic acid bacteria belonging to the genera, Acetobacter, Gluconacetobacter , and Gluconobacter , as well as LAB. Most of the yeasts associated with kombucha are species of Saccharomyces , although other yeast genera may also be present ( Teoh et al., 2004 ; Coton et al., 2017 ). While this product is now widely consumed, and manufacturers promote the presence of live microorganisms on product labels, there are few published data on the levels of microbes present in retail products. One recent study reported both bacterial and yeast counts for two kombucha products that were produced under industrial manufacturing conditions ( Coton et al., 2017 ). In general, acetic acid bacteria levels ranged from 10 6 to 10 7 cfu/mL at the end of the fermentation, and similar counts were reported for LAB and total aerobic bacteria. Total yeast counts of about 10 7 cfu/mL were also reported.

Food-Associated Microbes Travel and Interact in the Gut

The human gastrointestinal tract is home to more than 10 12 microbes. This diverse ecosystem provides protection against pathogens, extracts nutrients from dietary components, and modulates the immune system ( Lozupone et al., 2013 ). The gut microbiota is also very stable, although several factors, including exposure to antibiotics, stress, and disease can disrupt this community, leading to dysbiosis ( Sommer et al., 2017 ). The ability of diet and dietary components to modulate the gastrointestinal microbiota, redress dysbiosis, and enhance human health is now well- established ( David et al., 2014 ; Graf et al., 2015 ; Sonnenburg and Bäckhed, 2016 ).

Among the food components known to influence the composition of the microbiota are fermentable fibers and prebiotics that enrich for particular members of the gut microbiota. Another route by which the gastrointestinal microbiota may be modulated is via consumption of probiotics—live microbes consumed at a dose sufficient to provide beneficial effects ( Hill et al., 2014 ). Probiotics, however, are temporary members of the microbiome and rarely persist more than a few days ( Tannock, 2003 ; Derrien and van Hylckama Vlieg, 2015 ; Zhang et al., 2016 ).

Perhaps the easiest and most common way to introduce potentially beneficial microbes to the gastrointestinal tract is via consumption of microbe-containing foods, and fermented foods and beverages, in particular. Like many probiotics, many microbes associated with fermented foods may also have the capacity to survive digestion, reach the gastrointestinal tract, and ultimately provide similar health benefits ( Marco et al., 2017 ). When consumed regularly, these fermentation-associated microbes form what some researchers have called the “transient microbiome” ( Derrien and van Hylckama Vlieg, 2015 ).

In general, the microorganisms present in fermented foods and beverages originate via one of two ways. For so-called natural or spontaneous fermented foods, the microorganisms are autochthonous and are naturally present in the raw material or manufacturing environment. To survive fermentation and processing, the LAB, yeasts, and any other microorganisms present in the finished product must manage a range of selective and competitive pressures, including salt, organic acids, ethanol, anaerobiosis, and low pH. Many of the fermented foods reviewed in this survey, including fermented cereals, sauerkraut, kimchi, and other fermented vegetables, and fermented soy-based products are made by natural fermentation. In addition, many wines and even some fermented sausages and beers are made in this manner.

Other fermented foods rely on the addition of a starter cultures. Cultured dairy products, cheese, and fermented sausages are commonly made using starter cultures. When cultures are used, their selection is based on the performance characteristics specific to the product. In addition, the incubation temperature during fermentation and the nutrient content are usually well-suited to the needs of the microorganisms. In many cases, the culture is added at such high inoculum levels, there would be little competition from other organisms. Collectively, most food fermentation microorganisms are well-adapted to the food environment.

In contrast, once the organisms present in fermented foods are consumed, they become foreign or allochthonous to the gastrointestinal tract. In most cases, they lack the physiological and biochemical resources to compete in this ecological niche. If they survive transit, they do not become stable members of this community ( Zhang et al., 2016 ). Nonetheless, the presence of food fermentation-associated microorganisms in the GI tract, even if they are just “passing through,” is now well-documented ( Lee et al., 1996 ; Walter et al., 2001 ; Dal Bello et al., 2003 ; David et al., 2014 ; Derrien and van Hylckama Vlieg, 2015 ; Zhang et al., 2016 ; Lisko et al., 2017 ).

Evidence of Health Benefits Associated with Fermented Foods

The evidence for the potential health benefits of fermented foods is based on numerous epidemiological as well as clinical reports (reviewed in Marco and Golomb, 2016 ; Kok and Hutkins, in press ). In general, epidemiological studies have shown that consumption of fermented foods is associated with improvements of health status or reductions in disease risk. For example, yogurt-rich diets were associated with a reduced risk of metabolic syndrome in older Mediterranean adults ( Babio et al., 2015 ). A similar finding was reported in another large cohort study that showed cultured milk consumption reduced the risk of bladder cancer ( Larsson et al., 2008 ). Yogurt consumption has also been associated with reduced weight gain ( Mozaffarian et al., 2011 ). Epidemiological data also suggests that consumption of other fermented foods may be correlated to beneficial health outcomes. Consumption of kimchi and other fermented vegetables, for example, correlated with reduced incidence of asthma and atopic dermatitis in Korean adults ( Park and Bae, 2016 ; Kim et al., 2017 ). Reduced risks of type 2 diabetes and high blood pressure among Japanese adults was associated with consumption of fermented soybean foods rich in phytoestrogens and bioactive peptides ( Kwon et al., 2010 ; Nozue et al., 2017 ). In contrast, the large European Prospective Investigation into Cancer and Nutrition cohort study from the Netherlands reported no association between fermented foods consumption and overall mortality ( Praagman et al., 2015 ).

Although many human clinical studies have assessed the effects of probiotic-containing fermented foods on health biomarkers, fewer randomized controlled trials (RCT) have considered fermented foods alone. Nonetheless, several reports provide evidence that fermented foods, such as kimchi, fermented soy products, and yogurt, can improve relevant biomarkers. For example, kimchi consumption improved fasting blood glucose and other metabolic syndrome symptoms in overweight and obese adults ( Kim et al., 2011 ), and similar improvements were observed in healthy adults ( Choi et al., 2013 ). Consumption of a fermented soybean paste also improved plasma triglyceride levels in obese adults ( Lee Y. et al., 2017 ). Perhaps the strongest evidence is for yogurt and improved lactose tolerance, due to in vivo expression and release of β-galactosidase by the yogurt culture microbes, S. thermophilus and L. delbrueckii subsp. bulgaricus ( Kolars et al., 1984 ; Martini et al., 1987 ; Pelletier et al., 2001 ; Savaiano, 2014 ). This is the only approved health claim approved by the European Food Safety Authority ( EFSA Panel on Dietetic Products, Nutrition and Allergies, 2010 ).

As noted previously, some fermented foods could impart health benefits even in the absence of live microorganisms in the finished products. For example, in sour dough bread manufacture, LAB may express phytase enzymes that degrade phytates and therefore enhance mineral absorption ( Nuobariene et al., 2015 ). In the manufacture of red wine, ethanol produced early in the fermentation enhances extraction of polyphenolic compounds from the grape skins. Fermented foods may also contain vitamins and other bioactive molecules produced in situ from microbial metabolism that are not present in the original food. Recently, Saubade et al. (2017) noted that folic acid deficiency is a global health problem and suggested that fermented foods could be a food-based alternative for delivering folic acid to at-risk populations. Although some LAB are able to produce modest levels of folate ( Leblanc et al., 2011 ), amounts produced in foods may be too low to be reach required levels ( Saubade et al., 2017 ). Thus, selection of over-producing strains, as well as combining strains with non-LAB may be necessary to enhance production of this vitamin in foods.

If present, fermentation-derived microorganisms, despite their transient nature, may yet have the potential to influence gut microbiota diversity, structure, and function ( Zhang et al., 2016 ). Notably, they may also affect health due to their ability to out-compete pathogens for resources, produce short chain fatty acids from available carbohydrates, secrete anti-microbial agents, contribute to immune homeostasis, and produce vitamins, in situ ( Derrien and van Hylckama Vlieg, 2015 ).

The Number of Fermentation-Associated Microbes Depends on Region and Product Age

In this survey, we reviewed the literature for studies that included quantitative data on microorganisms present in commercial fermented food products. To our knowledge, this is the first time that there has been a compilation of the hundreds of previous studies that enumerated microbes in fermented foods from retail samples or commercial products. In general, most of the products for which data were available contained at least 10 6 cells/mL or g. However, there was considerable variation depending on product age and region, and several relevant bacterial species or groups were present at less than that amount.

Although regular consumption of yogurt is often included in dietary guidelines ( Smug et al., 2014 ), recommendations for other fermented foods rarely exist ( Chilton et al., 2015 ). Likewise, to our knowledge, there are few guidelines for what constitutes a minimum dose of live microorganisms. The one exception is the yogurt health claim for “improved lactose tolerance” that was approved in 2010 by the European Food Safety Authority ( EFSA Panel on Dietetic Products, Nutrition and Allergies, 2010 ). The claim states that yogurt should contain at least 10 8 cfu live starter microorganisms per gram- the same count the NYA requires for the “live and active” seal, as noted above.

Even in the absence of a seal or stamp, many commercial yogurt products, as well as kefir, fermented vegetables, and miso, also provide numerical information on their labels. Recently, Derrien and van Hylckama Vlieg (2015 ) suggested that consumption of 10 10 cells would be necessary to induce an effect on the microbiota and host health. This could be achieved by consuming 100 g of fermented food containing 10 8 cells/g.

According to the results reported in this survey, many commercial fermented food products would be close to meeting this requirement (Figure 1 ). However, several caveats are relevant. First, there was a wide range of reported microbial counts (over several logs) within the various product groups. Some products also reported total LAB, whereas other reported specific genera or species or as thermophilic or mesophilic. Second, for most products, enumeration relied on standard cultural methods for LAB (including medium and incubation conditions), which may have under-estimated more fastidious species. This can be attributed to the high stress conditions of fermented products that can occasionally lead to injured microorganisms that are viable but not culturable.

Figure 1 . Summary of lactic acid bacteria (LAB) counts in all fermented foods as reported in Tables 1–8 . The bar plots represents a range (minimum to maximum) of counts found across the studies surveyed. The number of studies used here for each fermented food is shown in brackets. Products were excluded if they had no viable counts or when LAB counts were not reported. For yogurt, initial counts were used for products that had counts for more than one timepoint. For cheese, the products were divided by aging time (60 days) and were excluded if aging time was not reported.

Finally, the age or time at which the products were analyzed also varied considerably. In general, “fresher” products had higher numbers. These would include yogurt and cultured dairy products, as well as kimchi, sauerkraut, and other fermented vegetables. The counts from the cheeses also varied widely, with the longer aged cheeses (e.g., Parmesan, Grana) consistently having the lowest counts.

Recommendation of Fermented Foods as Part of Dietary Guidelines

In many cultures, fermented foods containing live microorganisms are consumed on a regular or even daily basis ( Hutkins, 2018 ). Based on the data reported in this survey, consumption of fermented foods would not only provide important macronutrients, they could also deliver large numbers of potentially beneficial microorganisms to the gastrointestinal tract. For example, if Korean kimchi contains 10 8 lactic acid bacteria per g (Table 5 ), and given per capita consumption of kimchi is estimated at 100 g per person per day, then the daily consumption of live microbes from kimchi alone would be 10 10 . Likewise, in the Netherlands, where yogurt consumption is also around 100 g per day, similar levels of microbes (i.e., 10 10 cfu per day) would be ingested. These are the doses noted above that can influence the gut microbiota and provide a potential health benefit ( Derrien and van Hylckama Vlieg, 2015 ).

Recently, the concept of “shared core benefits” was introduced to explain how and why phylogenetically related organisms could deliver similar health benefits ( Sanders et al., 2018 ). Thus, although the microbes in fermented foods cannot, by definition, be considered probiotic, many of them are evolutionarily highly related to probiotic organisms, and they often share the same molecular mechanisms responsible for health-promoting properties in probiotic organisms. The application of various omic approaches to understand functional properties of fermentation-derived microbes will also likely reveal new attributes relevant to the health benefits these microbes may provide ( Macori and Cotter, 2018 ).

In part, this is why several prominent groups have recommended that health care professionals should promote fermented foods containing live microbes as part of public health policy ( Ebner et al., 2014 ; Sanders et al., 2014 ; Chilton et al., 2015 ; Bell et al., 2017 ; Hill et al., 2017 ). In particular, including fermented foods in dietary guidelines for specific populations has also been recommended. For example, Bell et al. (2018) recently suggested fermented foods should be introduced to children early in life and incorporated into their everyday meal plans. In addition, regular consumption of fermented foods could be especially important for low income, resource-challenged communities that are disproportionally susceptible to gastrointestinal infections ( Kort et al., 2015 ).

Author Contributions

SR, CK, and RH each contributed 30% to data collection. MH contributed 10% to data collection. SR, CK, and RH wrote the manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This project was funded by the National Dairy Council and facilitated by the International Scientific Association for Probiotics and Prebiotics. We thank Mary Ellen Sanders for her helpful comments.

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Keywords: fermented foods, live microbes, lactic acid bacteria, health benefits, probiotics

Citation: Rezac S, Kok CR, Heermann M and Hutkins R (2018) Fermented Foods as a Dietary Source of Live Organisms. Front. Microbiol . 9:1785. doi: 10.3389/fmicb.2018.01785

Received: 13 May 2018; Accepted: 17 July 2018; Published: 24 August 2018.

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Copyright © 2018 Rezac, Kok, Heermann and Hutkins. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Robert Hutkins, [email protected]

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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Fermented-food diet increases microbiome diversity, decreases inflammatory proteins, study finds

Stanford researchers discover that a 10-week diet high in fermented foods boosts microbiome diversity and improves immune responses.

July 12, 2021 - By Janelle Weaver

Stanford researchers found that eating a diet high in fermented foods such as kimchi increases the diversity of gut microbes, which is associated with improved health. Nungning20/Shutterstock

A diet rich in fermented foods enhances the diversity of gut microbes and decreases molecular signs of inflammation, according to researchers at the Stanford School of Medicine .

In a clinical trial, 36 healthy adults were randomly assigned to a 10-week diet that included either fermented or high-fiber foods. The two diets resulted in different effects on the gut microbiome and the immune system.

Eating foods such as yogurt, kefir, fermented cottage cheese, kimchi and other fermented vegetables, vegetable brine drinks, and kombucha tea led to an increase in overall microbial diversity, with stronger effects from larger servings. “This is a stunning finding,” said Justin Sonnenburg , PhD, an associate professor of microbiology and immunology. “It provides one of the first examples of how a simple change in diet can reproducibly remodel the microbiota across a cohort of healthy adults.”

In addition, four types of immune cells showed less activation in the fermented-food group. The levels of 19 inflammatory proteins measured in blood samples also decreased. One of these proteins, interleukin 6, has been linked to conditions such as rheumatoid arthritis, Type 2 diabetes and chronic stress.

“Microbiota-targeted diets can change immune status, providing a promising avenue for decreasing inflammation in healthy adults,” said Christopher Gardner , PhD, the Rehnborg Farquhar Professor and director of nutrition studies at the Stanford Prevention Research Center . “This finding was consistent across all participants in the study who were assigned to the higher fermented food group.”

Justin Sonnenburg

Microbe diversity stable in fiber-rich diet

By contrast, none of these 19 inflammatory proteins decreased in participants assigned to a high-fiber diet rich in legumes, seeds, whole grains, nuts, vegetables and fruits. On average, the diversity of their gut microbes also remained stable. “We expected high fiber to have a more universally beneficial effect and increase microbiota diversity,” said Erica Sonnenburg , PhD, a senior research scientist in basic life sciences, microbiology and immunology. “The data suggest that increased fiber intake alone over a short time period is insufficient to increase microbiota diversity.”

The study published online July 12 in Cell. Justin and Erica Sonnenburg and Christopher Gardner are co-senior authors. The lead authors are Hannah Wastyk , a PhD student in bioengineering, and former postdoctoral scholar Gabriela Fragiadakis, PhD, who is now an assistant professor of medicine at UC-San Francisco.

A wide body of evidence has demonstrated that diet shapes the gut microbiome, which can affect the immune system and overall health. According to Gardner, low microbiome diversity has been linked to obesity and diabetes.

“We wanted to conduct a proof-of-concept study that could test whether microbiota-targeted food could be an avenue for combatting the overwhelming rise in chronic inflammatory diseases,” Gardner said.

The researchers focused on fiber and fermented foods due to previous reports of their potential health benefits. While high-fiber diets have been associated with lower rates of mortality, the consumption of fermented foods can help with weight maintenance and may decrease the risk of diabetes, cancer and cardiovascular disease.

Erica Sonnenburg

The researchers analyzed blood and stool samples collected during a three-week pre-trial period, the 10 weeks of the diet, and a four-week period after the diet when the participants ate as they chose.

The findings paint a nuanced picture of the influence of diet on gut microbes and immune status. On one hand, those who increased their consumption of fermented foods showed similar effects on their microbiome diversity and inflammatory markers, consistent with prior research showing that short-term changes in diet can rapidly alter the gut microbiome. On the other hand, the limited change in the microbiome within the high-fiber group dovetails with the researchers’ previous reports of a general resilience of the human microbiome over short time periods.

Designing a suite of dietary and microbial strategies

The results also showed that greater fiber intake led to more carbohydrates in stool samples, pointing to incomplete fiber degradation by gut microbes. These findings are consistent with other research suggesting that the microbiome of people living in the industrialized world is depleted of fiber-degrading microbes.

“It is possible that a longer intervention would have allowed for the microbiota to adequately adapt to the increase in fiber consumption,” Erica Sonnenburg said. “Alternatively, the deliberate introduction of fiber-consuming microbes may be required to increase the microbiota’s capacity to break down the carbohydrates.”

In addition to exploring these possibilities, the researchers plan to conduct studies in mice to investigate the molecular mechanisms by which diets alter the microbiome and reduce inflammatory proteins. They also aim to test whether high-fiber and fermented foods synergize to influence the microbiome and immune system of humans. Another goal is to examine whether the consumption of fermented food decreases inflammation or improves other health markers in patients with immunological and metabolic diseases, and in pregnant women and older individuals.

Christopher Gardner

“There are many more ways to target the microbiome with food and supplements, and we hope to continue to investigate how different diets, probiotics and prebiotics impact the microbiome and health in different groups,” Justin Sonnenburg said.

Other Stanford co-authors are Dalia Perelman, health educator; former graduate students Dylan Dahan, PhD, and Carlos Gonzalez, PhD; graduate student Bryan Merrill; former research assistant Madeline Topf; postdoctoral scholars William Van Treuren, PhD, and Shuo Han, PhD; Jennifer Robinson, PhD, administrative director of the Community Health and Prevention Research Master’s Program and program manager of the Nutrition Studies Group; and Joshua Elias, PhD.

Researchers from Chan-Zuckerberg Biohub also contributed to the study.

The work was supported by donations to the Center for Human Microbiome Research; Paul and Kathy Klingenstein; the Hand Foundation; Heather Buhr and Jon Feiber; Meredith and John Pasquesi; the National Institutes of Health (grant T32 AI 7328-29); a Stanford Dean’s Postdoctoral Fellowship; a National Science Foundation Graduate Student Fellowship; and seed funding from the Institute for Immunity, Transplantation and Infection and from the Sean N. Parker Center for Allergy and Asthma Research.

• Janelle Weaver

About Stanford Medicine

Stanford Medicine is an integrated academic health system comprising the Stanford School of Medicine and adult and pediatric health care delivery systems. Together, they harness the full potential of biomedicine through collaborative research, education and clinical care for patients. For more information, please visit med.stanford.edu .

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Advancing Fermented Food Products: Exploring Bioprocess Technologies and Overcoming Challenges

• Published: 30 December 2023

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• Sudarsini B 1 ,
• Venkateswarulu T. C 1 ,
• Krupanidhi S 1 ,
• Sumalatha B 2 &
• Indira M 1  

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The fermented foods have been a part of the human diet in both traditional and modern cultures. Fermented food products are those produced through the addition of microbes such as yeast and bacteria. Each fermented food has distinct population of microorganisms, acts as probiotics, and produces a variety of metabolites and bioactive compounds. The physical and chemical changes in fermented food are due to the presence of probiotics and prebiotics, resulting in improved quality and long-term stability of the product. The positive health benefits have been investigated intensively, and the consolidated data are presented in this review. Once ingested, the beneficial bacteria colonize in the gut microbiome, produce bioactive compounds, and protect the human body from pathogenic microorganisms in various ways. The purpose of this paper is to present various types of fermented foods and beverages, probiotics, and prebiotics present in the foods, bioprocess technologies used for processing of fermented foods, nutritional quality of the fermented foods, and the influence of fermented foods on gut microbiome and health. Therefore, the benefits of fermented foods and beverages on gut microbiome should be studied and pursued to promote good health.

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An overview of fermentation in the food industry - looking back from a new perspective

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The authors would like to acknowledge the Department of Biotechnology, School of Biotechnology and Pharmaceutical Sciences, Vignan’s Foundation for Science Technology and Research, for providing the platform to carry out the research work.

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B, S., C, V.T., S, K. et al. Advancing Fermented Food Products: Exploring Bioprocess Technologies and Overcoming Challenges. Food Bioprocess Technol (2023). https://doi.org/10.1007/s11947-023-03287-8

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Fiber and fermented foods may aid microbiome, overall health

May 10, 2024 — It’s well-known that eating a diet rich in fiber and fermented foods fosters healthy digestion, but research suggest that these foods may offer additional health benefits.

According to an April 26 Harvard Health Publishing article, high-fiber foods such as vegetables and whole grains can help with weight control and lower levels of LDL, or “bad” cholesterol, and promote a healthy gut microbiome —which ultimately may help reduce inflammation linked to increased risk of developing chronic conditions including heart disease, type 2 diabetes, and some cancers. Fermented foods such as yogurt and kimchi contain probiotics and prebiotics—good bacteria and food for good bacteria—which help promote a healthy gut microbiome.

Individual fiber needs can vary. Eric Rimm , professor in the Departments of Epidemiology and Nutrition , suggested in the article that people focus on adding more fiber-rich foods to their diets rather than trying to track daily amounts. It’s ok to add fiber supplements, he said, but whole foods should be the primary source of dietary fiber.

There are no recommended daily amounts for probiotics or prebiotics. Rimm said that fermented foods are a better source of these nutrients than dietary supplements, which do not require FDA approval and are not guaranteed to contain the ingredients and benefits listed on their labels.

Read the Harvard Health Publishing article: How—and why—to fit more fiber and fermented food into your meals

Photo: iStock / courtneyk

Health benefits of fermented foods

Affiliations.

• 1 a Biruni University, Faculty of Health Sciences , Nutrition and Dietetics Department , İstanbul , Turkey.
• 2 b Gazi University, Faculty of Health Sciences , Nutrition and Dietetics Department , Ankara , Turkey.
• 3 c Gazi University, Faculty of Tourism , Department of Gastronomy and Culinary Art , Gölbaşı/Ankara , Turkey.
• PMID: 28945458
• DOI: 10.1080/10408398.2017.1383355

In the past, the beneficial effects of fermented foods on health were unknown, and so people primarily used fermentation to preserve foods, enhance shelf life, and improve flavour. Fermented foods became an important part of the diet in many cultures, and over time fermentation has been associated with many health benefits. Because of this, the fermentation process and the resulting fermented products have recently attracted scientific interest. In addition, microorganisms contributing to the fermentation process have recently been associated with many health benefits, and so these microorganisms have become another focus of attention. Lactic acid bacteria (LAB) have been some of the most studied microorganisms. During fermentation, these bacteria synthesize vitamins and minerals, produce biologically active peptides with enzymes such as proteinase and peptidase, and remove some non-nutrients. Compounds known as biologically active peptides, which are produced by the bacteria responsible for fermentation, are also well known for their health benefits. Among these peptides, conjugated linoleic acids (CLA) have a blood pressure lowering effect, exopolysaccharides exhibit prebiotic properties, bacteriocins show anti-microbial effects, sphingolipids have anti-carcinogenic and anti-microbial properties, and bioactive peptides exhibit anti-oxidant, anti-microbial, opioid antagonist, anti-allergenic, and blood pressure lowering effects. As a result, fermented foods provide many health benefits such as anti-oxidant, anti-microbial, anti-fungal, anti-inflammatory, anti-diabetic and anti-atherosclerotic activity. However, some studies have shown no relationship between fermented foods and health benefits. Therefore, this paper aims to investigate the health effects of fermented foods.

Keywords: Fermented food; anti-carcinogenic; bioactive peptides; cardiovascular disease; lactic acid bacteria.

Publication types

• Anti-Infective Agents / analysis
• Anti-Inflammatory Agents / analysis
• Antifungal Agents / analysis
• Antioxidants / analysis
• Atherosclerosis / prevention & control
• Cultured Milk Products / analysis
• Fermentation
• Fermented Foods* / analysis
• Health Promotion*
• Hypoglycemic Agents / analysis
• Lactobacillales / metabolism
• Meat Products
• Minerals / metabolism
• Vitamins / biosynthesis
• Anti-Infective Agents
• Anti-Inflammatory Agents
• Antifungal Agents
• Antioxidants
• Hypoglycemic Agents

Showbizz Daily (English)

Fermented foods: The easy and delicious way to boost your health

Posted: January 5, 2024 | Last updated: April 26, 2024

What are fermented foods?

Fermented foods have been a staple of diets worldwide for thousands of years. They're made by letting bacteria, yeast, or fungi work their magic on various foods and drinks, producing delicious tangy, sour, or fizzy results that scientists now say can boost health and even longevity.

What's good for the gut is good for you

The latest scientific research shows that eating fermented food can change the makeup of the ecosystem of trillions of bacteria, viruses and fungi living in your gut, which is collectively known as the gut microbiome.

A landmark study shows fermented foods reduce inflammation

A 2021 Stanford University study looked at how fermented foods affected healthy adults. Half of a group of 36 were told to eat more fiber-rich plant foods like fruit and veggies, while the other half started eating a lot of fermented foods. After ten weeks, the fermented food group saw big reductions in inflammatory proteins associated with diseases like diabetes and arthritis.

Higher levels of gut microbiome diversity

Unspuringly, the guts of the people eating fermented foods also began to host more diverse microbes. The same study found more fermented foods were associated with more biodiversity. However, it wasn't only that the specific probiotics consumed started growing in the intestines. Instead, the fermented foods seemed to recruit a whole array of different microbes to the gut.

Specific food studies

While there are tons of different fermented foods, and it's a fairly new realm of study, a 2022 meta-analysis published in the journal Nutrients highlighted some of the most solid scientific evidence around the specific health effects of fermented foods so far.

Yogurt is associated with a reduced risk of type 2 diabetes

A study that followed nearly 4,000 people for decades found that dairy products didn't impact the chances of developing type 2 diabetes. That's good news in itself for dairy lovers, but yogurt was even linked to a reduced risk of developing the disease.

Fermented dairy products are good for longevity

A study that followed more than 4,500 people for a decade found that fermented dairy products like cheese, kefir or yogurt were inversely associated with overall mortality. In other words, people who consumed them more died less (during the study period).

Fermented dairy could help prevent cardiovascular disease

Population studies from around the world have found that consuming fermented dairy foods like cheese and yogurt is associated with a reduced risk for cardiovascular disease, according to a 2015 paper in the British Journal of Nutrition.

Fermented milk is good for muscle soreness

A 2013 Japanese study found that a fermented milk product alleviated muscle soreness and related biological markers after high-intensity exercise in a group of healthy young men.

Kimchi was linked to anti-diabetic and anti-obesity effects

One study found fermented kimchi to be beneficial in a group of people with pre-diabetes, even compared to those who ate fresh kimchi. Another study found consuming fermented kimchi reduced body weight and boosted the metabolism in overweight and obese people.

Potential effects on your mental health

In recent years, scientists have found strong links between the gut biome and mental health and cognitive performance. While studies are few, a 45-person review found people eating more fiber, prebiotics (like oatmeal) and fermented foods reported feeling less stressed than a control group on a different diet. Another 2015 study found fermented food consumption was linked to less social anxiety.

Miso: Calmness, lower blood pressure and decreased heart rate

A 2020 Japanese study found that miso, a fermented soybean paste often used for soup, can lower blood pressure, decrease heart rate and calm nerve activity even though it has a high salt content. That's interesting because salt is generally known to provoke the opposite effects.

Natto: Linked to reduced blood clots, lower blood pressure and increased nutrient absorption

Natto is another soy-based fermented food rich in protein, vitamins and minerals. But most health benefits are found in the nattokinase enzyme produced during fermentation. Studies link it to reduced blood clots, lower blood pressure, increased bone strength, and increased nutrient absorption.

Tempeh: Another fermented soy product from Japan linked to longevity

After controlling for other diet components, hypertension, diabetes, smoking, alcohol intake and other factors, scientists looking at nearly 100,000 Japanese people for 15 years found that 10% of people who ate the most fermented soy like tempeh, miso and natto compared with those in the lowest one-fifth for fermented soy intake had a 10% lower risk of death.

Photo: Ella Olsson/Unsplash

Kombucha: Fewer studies but a promising fermented drink

Besides evidence to support the power of fermented foods in general, kombucha, a fermented tea, hasn't been deeply studied. According to the Mayo Clinic, some research suggests kombucha tea may support a healthy immune system and prevent constipation, but more evidence is needed.

Pickles and sauerkraut: Check to see if they're pasteurized

These two beloved staples are both packing fiber, but they can either come with the benefits of fermented foods… or not. As a rule, if you buy them un-refrigerated, they are probably pasteurized, a heating process that kills all the probiotics. If unpasteurized pickles and sauerkraut are unavailable at the store, you can make them at home.

Democratized health: DYI fermented food

Pretty much any whole food can be fermented in your home on the cheap. "What I like about fermented foods is that they democratize science. They don't really cost much, and you don't have to get them from some fancy store. You can do it yourself," John Cryan, a professor of anatomy and neuroscience at University College Cork, told BBC.

Olives: Fermented but commonly pasteurized

Olives are one of the oldest fermented foods in the Mediterranean area. While some traditionally cured olives are available, many are often pasteurized too. That means they won't all carry the same probiotic punch as seen with other fermented foods. However, they have still been linked to numerous health benefits.

Fermented breads like sourdough are also promising

Again, studies are really just getting started, but a 2022 experiment in mice showed potential health benefits of sourdough bread, such as cholesterol reduction, inflammation alleviation, and healthy gut microbiota maintenance when compared to non-fermented but similar white bread.

Photo: Vicky Ng/Unsplash

Beer is fermented. Does that mean it's a superfood?

Yes, beer is fermented, but that doesn't mean that guzzling pints is good for your health. Most beers are pasteurized, which kills all bacteria, including the beneficial probiotics. However, some contain live bacteria, and studies have shown moderate consumption could boost gut microbiota. However, that must be balanced with the negative effects of alcohol.

Photo: Timothy Dykes/Unsplash

What about wine?

Wine is also made by fermenting grapes, but sulfites can inhibit the growth of beneficial probiotics. A 2019 study by Kings College London found red wine (not white) was associated with increased gut microbiota diversity, but suggested that the high levels of polyphenols, not probiotics, could be responsible for much of wine's controversial health benefits when used in moderation.

Photo: Nacho Domínguez Argenta/Unsplash

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