Fermented foods: consensus statement and reviewing them

23rd March 2021

Translated from the original article in Catalan

The term “fermented foods” has been widely used but so far has not had a clear definition, there are inconsistencies related to the use of the term “fermented” and is sometimes used including more or less related products, such as probiotics. Although these foods have been consumed for thousands of years, they have recently received increasing attention among biologists, nutritionists, other scientists, and consumers.

In order to develop a definition and describe the role of fermented foods in the human diet, the International Scientific Association for Probiotics and Prebiotics (ISAPP) convened in September 2019 a group of experts to get a consensus on it. ISAPP is a non-profit organization, led by scientists and academics, and although it is funded by companies, its activities are not stipulated by industry. Its mission is to provide objective and scientific information on probiotics, prebiotics and other topics related to nutrition and health.

Figure 1. Website homepage of the International Scientific Association of Probiotics and Prebiotics (ISAPP)

These ISAPP experts have been a total of 13, from the USA, Ireland, Canada, Belgium and South Korea. Most of them are from universities and some companies, and their findings have been published recently (Marco et al 2021).

One of the main conclusions of the consensus they have reached is the definition of fermented foods and beverages: they are those made using the desired microbial growth, which involves enzymatic conversions of food components. In this work, in addition to reviewing what they are, the distinction between fermented and probiotic foods is defined, and the current knowledge about the safety, risks and benefits of these foods is revised. Finally, regulation of fermented foods and the possibility of including them in the dietary guidelines of different countries are reviewed.

What are fermented foods ?

Humans learned a few thousand years ago how to consume and make fermented foods, probably in parallel with the development of agriculture and livestock. See for example my article on fermented cheeses and milks made 7000 years ago.

The consumption of fermented foods spread and promoted from the prehistory to all civilizations especially because it is one of the most effective ways to preserve food, due to the formation of compounds that inhibit other harmful microbes and/or pathogens. These compounds produced by the microorganisms fermenting foods include organic acids (such as lactic or acetic acid), ethanol or bacteriocins. Just remember on the one hand all dairy products that can be stored longer than milk thanks to lactic acid produced by bacteria in cheeses, yogurts, etc. And on the other hand, the consumption of beers or wines as a good hygienic alternative in places and times where uncontaminated running water was not available. The greater sustainability of fermented foods is still very important today in poor regions of the world where there is not enough food security or where there is not access to electricity, refrigeration or clean water.

Other methods of preserving food are decreasing aqueous activity (a_w) by: 1) adding salt or sugar or drying; 2) adding inhibitory compounds (e.g. spices or smoking); 3) vacuuming; and 4) heat treatments (cold or heat), among others.

The other reason for the consumption of fermented foods is the appearance of new organoleptic qualities, such as pleasant and different tastes, smells or textures, due to the biochemical transformations of microorganisms in the composition of the food.

Fermented foods are an important part of the human diet, even in developed regions where food safety and food preservation are well controlled. It has been estimated that more than 5,000 varieties of fermented foods (and beverages) are currently produced and consumed globally (Tamang et al. 2016).

Thus, in the above-mentioned consensus definition of ISAPP, it is very clear that fermented foods are those prepared in a way intended by humans where the activity of microorganisms is required and where they carry out a series of enzymatic reactions of the food components.

Although endogenous or exogenous enzymes, from plants, animals or other sources, may also be present in these foods, this activity is not sufficient to be considered a fermented food, as microbial activity is required.

On the other hand, the main difference with foods spoiled by microorganisms is that these foods are unwanted, and the fermented ones are deliberately made and controlled to generate desirable qualities.

It should also be pointed out that in fermented foods the action of microorganisms is not always through metabolism of fermentation. Indeed, from a biochemical point of view, “fermentation” is a type of metabolism where the energy source and both the electron donor and acceptor are organic compounds (especially carbohydrates), where ATPs are synthesized by phosphorylation of substrate (e.g. in glycolysis) and there is no ATP formation by oxidative phosphorylation with membrane-bound electron transport chains, as would be the case for respiration (Figure 2). Many classic fermented foods are made by fermentative metabolism such as lactic or alcoholic fermentations, but some are also considered fermented foods where microorganisms are doing aerobic respiration, such as acetic vinegar bacteria or molds from some cheeses. Therefore the term “fermented foods” has a broader view, independent of metabolism, where only the active and desired intervention of microorganisms is needed.

Figure 2. Main reactions of the basic mechanisms of ATP synthesis: Oxidative phosphorylation by electron transport chains (top) and Substrate-level phosphorylation (bottom).

Which are the fermented foods and the microorganisms involved ?

We find a good global relationship in the work of Tamang et al (2016), with the microorganisms involved, summarized in Table 1. Of course, this article is not an exhaustive relationship, as for example we miss the traditional Balearic “sobrassada”, although the Sicilian “soppressata” appears in the list, and probably both are related in origin. We see some of the best-known fermented foods in Figure 3.

Table 1. Types of fermented foods and the microorganisms involved (adapted from Tamang et al (2016)

Type	Products	Countries	Microorganisms
Fermented milks and derivatives	Yoghurts, cheeses, buttermilk, kefir, kumis, leben, etc. They are from cows and also from many other mammals, such as sheep, goats, mares, camels, yaks and buffalo	Worldwide	Lactic acid bacteria (LAB) Some bifidobacteria Some yeasts Molds (Penicillium)
Fermented vegetable products (fruits, stems, bulbs, leaves, roots, legumes)	Olives, sauerkraut, kimchi, various pickled vegetables (radishes, aubergines, onions, carrots), fermented cassava, soy products (sauce soy, miso, natto, tempeh). Wines (see below)	Worldwide	LAB Bacillus and other Firmicutes Yeasts Some molds (Rhizopus)
Other fermented vegetable derivatives	Vinegar Fermented tea (i.e. kombucha) and fermented cocoa to make chocolate	Worldwide	Acetic acid bacteria Yeasts
Fermented meat	Sausages such as chorizo, pepper, sausages, sobrassada	Worldwide, especially Europe	LAB Other Firmicutes Some yeasts
Fermented fish and sauces	Very diverse, i.e., nuroc mam, nam plaGarum	East and Southeast Asia Ancient Rome	LAB Other Firmicutes Other bacteria
Alcoholic beverages from cereals, produced with fungal amylolytic cultures	Sake	Japan	Aspergillus oryzae Yeasts
Alcoholic beverages from cereals, produced with human saliva	Chicha	South America	Saliva Yeasts LAB and others
Alcoholic beverages from malt, germinated cereal grain (mainly barley, wheat)	Beer	Worldwide	Yeasts Some lactic acid bacteria
Alcoholic beverages from plant parts	Pulque from agave	Mexico	LAB Zymomonas Yeasts
Alcoholic beverages from fruits	Vine wines	All regions of temperate climate	Yeasts Oenococcus (malolactic fermentation)
Alcoholic beverages from honey	Mead tej	Especially ancient world Ethiopia	Yeasts LAB

As we see in Table 1, the main microorganisms in many fermented foods, from milk to meat and vegetables and others, are lactic acid bacteria (LAB). They are gram-positive bacteria of the phylum Firmicutes (DNA with low G+C), non-spore-forming, aerotolerant anaerobes, and are considered safe. Other bacteria responsible for some fermented foods are Bacillus (sporulated Firmicutes), other Firmicutes such as Staphylococcus, and bacteria of the phylum Actinobacteria (gram-positive with DNA of high G+C) such as Bifidobacterium, Propionibacterium and Brevibacterium. Among the few gram-negative bacteria, the acetic acid bacteria (phylum Alphaproteobacteria) stand out and we must also mention Zymomonas, from the same phylum. You can see the phylogenetic location of all these bacteria in my post “Bacteria: 21 Main phyla, with 147 Important genera”.

In Table 1 we see that besides LAB, the other most important microorganisms in fermented foods are yeasts, especially Saccharomyces, unicellular ascomycete fungus. Other fungi acting in fermented foods are some filamentous ones, such as the ascomycetes Penicillium and Aspergillus, and the zygomycete Rhizopus.

Figure 3. Various fermented foods: sobrassada, cheeses, blue cheese, yogurt, olives, soy sauce, beer and wine.

Living or dead microorganisms in fermented foods ?

Microorganisms that have been actively involved in the processing of fermented foods may be present and viable, that is, alive, in some of these. However, they are absent in other fermented foods because they have been separated from the food or this has had a treatment, usually thermal, removing them (Marco et al 2021).

Among the fermented foods that contain living microorganisms we can mention yogurt, kefir and other fermented milks, most cheeses, miso, natto and tempeh, many of the fermented vegetable products that have not been heat treated such as olives, many of the sausages, kombucha, and some beers.

Fermented foods where microorganisms have been eliminated or removed are for instance bread, heat-treated fermented vegetable products, soy sauce, vinegar, wines, most beers, and coffee and cocoa beans once roasted.

In many uninoculated fermented foods, that is, with their own spontaneous microbiota, there is more than one microorganism responsible for the changes that take place from the original food to the fermented one. There is often a succession of types of microorganisms, depending on the composition of the food and the environmental conditions to which it is subjected: salt, temperature, dryness, etc. For example, in the fermentation of table olives, yeasts and other bacteria first predominate, and finally the LAB end up being imposed.

Differences between fermented foods and probiotics

Although sometimes fermented foods are labelled or named as “probiotics” or “contain probiotics,” it should be made clear that it is not the same in most cases. The term probiotic is only correct to use it when it has been shown to have some beneficial effect on the health of the consumer, and that this effect is due to a living and well-characterized microorganism. This health benefit is beyond the nutritional benefits of the food matrix that contains it. Therefore, the terms “fermented food” and “probiotic” cannot be used by each other.

In the case of fermented foods that may contain some probiotic microorganism, with proven effects on health, it should only be labelled with “contains probiotics” in the event that the probiotic microorganism is well characterized at the strain level and in quantities significant throughout the shelf life of the food.

Fermented foods and food safety

Fermented foods increase the safety of food for the consumer, in the sense that it is more difficult for harmful or pathogenic organisms to grow than with respect to the original foods before fermentation. Indeed, they often contain remarkable amounts of organic acids, such as lactic acid produced by LAB or acetic acid produced by homonymous bacteria. Many of these products at the same time have low water activity, and contain salt and other antimicrobials, making them safe (Adams & Mitchell 2002). Similarly, beverages containing > 4% ethanol or pH < 4.5 are also considered microbiologically safe.

In addition, many LAB, whether native or inoculated, produce bacteriocins that inhibit other undesirable bacteria, such as Listeria or Clostridium.

Some fermented foods also increase safety by removing toxic or antinutrient compounds from raw foods, as is the case with many fermentations of cereals, legumes, and tubers. For example, cassava contains cyanogenic glycosides which are eliminated in fermentation by Lactobacillus plantarum (Lei et al 1999). Also, in the fermentation of the sourdough some LAB facilitate the degradation, by the enzyme phytase (a phosphatase), of phytic acid present in cereals, which is a chelator of divalent cations (Ca, Mg, Fe, Zn) and therefore decreases its adsorption (López et al. 2001).

Furthermore, it can be stated that, with very few exceptions, the microorganisms that are the protagonists of fermented foods, basically LAB, yeasts and filamentous fungi, are not pathogenic nor produce toxic or harmful compounds. In fact, many of them, such as LAB themselves, but also many others (such as some Bacillus, Figure 4) are considered GRAS (generally recognized as safe) by the US FDA or QPS (qualified presumption of safety) by the European EFSA.

Figure 4. One of the last ingredients declared GRAS by the US FDA is precisely a Bacillus subtilis that can also be used in fermented foods. Source: US FDA Gras Notices.

However, as in any type of food, it is always necessary to be very careful, to make sure that the ingredients are fresh and safe, avoid any alteration, and have good controls throughout the production process and in the finished product, checking that there is no contamination of the usual food pathogens.

Some fermented foods contain compounds that can pose food safety risks if consumed in excess. This is the case with alcoholic beverages, which should be taken in moderation due to the effects of ethanol and should be avoided by people at risk. For a different reason and not related to microorganisms, it is also important not to overeat fermented foods that contain salt, such as soy sauce or kimchi.

Some of the few compounds produced by LAB that need to be controlled are biogenic amines, which can be found in small amounts in fermented foods such as cheese, sausages, some vegetables and wine. Biogenic amines can cause various health problems and especially migraines. Their production must be minimized by controlling potential producers species and inoculating non-producing strains.

Mycotoxins such as aflatoxins, ochratoxins and many others, are the main concern of foods fermented with filamentous fungi such as Aspergillus and Penicillium from fermented soybeans, cheeses and others (Sivamaruthi et al 2019). However, in most of these products selected strains are used, either by domestication over centuries or more recently by artificial selection, which do not produce toxins.

Benefits of eating fermented foods on human nutritional health

Beyond food preservation reasons and organoleptic qualities, there is some epidemiological evidence to suggest that diets rich in fermented foods may reduce the risk of disease and increase longevity, health, and quality of life. But these diets, such as the Mediterranean diet, include foods other than fermented ones, and therefore it is not certain that the positive effects are due exclusively to fermented foods. In addition, with the exception of yogurt and other fermented milks, few well-designed and controlled clinical studies have been conducted on the potential health benefits of fermented foods in terms of specific diseases (Marco et al 2021).

However, the indirect health effects of fermented foods are quite apparent when considering the nutritional aspects. Microbial activity leads to the enrichment and / or elimination of various compounds that affect and improve the nutritional composition of the final product.

First, microorganisms reduce the content of high-calorie sugars, id est, monosaccharides and disaccharides, present in milk, meat and vegetables. This reduces the glycemic index and reduces food intolerance, such as lactose in dairy products, wheat fructans, or raffinose and stachyose from legumes. Fermentation hydrolyses polysaccharides, proteins and fats, which facilitates digestion, and as mentioned, it removes various toxic or antinutrient compounds such as phytic acid.

In the case of foods containing polyphenols, lactobacilli have been shown to increase the bioavailability of flavonoids, tannins, and other bioactive compounds. The biosynthesis of vitamins, amino acid derivatives, organic acids such as lactic acid, peptides and cofactors by food-fermenting microbes is well known (Melini et al 2019).

It has been shown that many of the living microorganisms in fermented foods can survive gastric transit and reach the colon, as for example many LAB are tolerant of acidic pH and bile salts and have been shown to be able to maintain transiently in the colon (Elli et al. 2006). Although these microorganisms are unlikely to survive long, it has been shown that they may be metabolically active in the gastrointestinal tract, and that this short-term colonization would be sufficient to produce bioactive compounds, inhibit pathogens, and positively influence the immune system. These effects are increased if there is a daily and repeated consumption of fermented food.

Fermented foods, and the microorganisms they contain, have also been shown to influence the composition of the intestinal microbiota itself (Taylor et al 2020). See also González et al in 2019 and Le Roy et al in 2020. Another additional positive factor in the case of fermented vegetable foods is that many components of these are prebiotics and therefore favour the intestinal microbiota.

In addition, we must take into account the importance of what we eat, including fermented foods, in relation to the immune system. In humans and other mammals 70% of this system is in the gastrointestinal tract, and food is the main source of contact between external antigens and our body. This is particularly important in infants and the initial microbial colonization of the digestive tract. Ingestion of fermented foods during the early years of childhood has been associated with a reduced risk of childhood atopy (genetic predisposition to allergies) (Alm et al. 1999). For any age, it seems that the microorganisms of fermented foods and their components, such as glycopeptide, surface proteins, exopolysaccharides, lipoteichoic acid, or D-phenyl-lactic acid from LAB (Peters et al. 2019) are beneficial for the immune system, especially more demonstrated in fermented milks (Bourrie et al. 2016; Foligne et al. 2016).

In Figure 5 we see a diagram of the basic mechanisms of the possible benefits of fermented foods.

Figure 5. Basic mechanisms of the health benefits of fermented foods, especially from a nutritional point of view, with the transformations of food components into bioactive substances. SCFAs are short-chain fatty acids. Source: Marco et al 2021.

Finally, to conclude, it is necessary to remind that although fermented foods are consumed worldwide and account for approximately 1/3 of the human diet, they are usually absent as recommended foods in diet guidelines (Marco et al 2021). It is also a pity that most of the information that comes out in the media or in popular magazines or on social media about this type of food is exaggerated or wrong, often making them synonymous with probiotics.

Bibliography

Adams M, Mitchell R (2002) Fermentation and pathogen control: a risk assessment approach. Int. J. Food Microbiol. 79, 75–83

Alm J S, Swartz J, Lilja G, Scheynius A, Pershagen, G (1999) Atopy in children of families with an anthroposophic lifestyle. Lancet 353, 1485–1488

Bourrie B C, Willing B P, Cotter P D (2016) The microbiota and health promoting characteristics of the fermented beverage kefir. Front Microbiol 7, 647

Elli M et al (2006) Survival of yogurt bacteria in the human gut. Appl Environ Microbiol 72, 5113–5117

Foligne B et al (2016) Immunomodulation properties of multi-species fermented milks. Food Microbiol 53, 60–69

González S et al (2019) Fermented dairy foods: impact on intestinal microbiota and health-linked biomarkers. Front Microbiol 10, 1046.

Iraporda C. et al (2015) Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology 220, 1161–1169

ISAPP, The International Scientific Association for Probiotics and Prebiotics: https://isappscience.org

Lei V, Amoa-Awua WK, Brimer L (1999) Degradation of cyanogenic glycosides by Lactobacillus plantarum strains from spontaneous cassava fermentation and other microorganisms. Int. J. Food Microbiol. 53, 169–184

Le Roy C I et al (2020) Red wine consumption associated with increased gut microbiota α-diversity in 3 independent cohorts. Gastroenterology 158, 270–272

López HW et al (2001) Prolonged fermentation of whole wheat sourdough reduces phytate level and increases soluble magnesium. J. Agric. Food Chem. 49, 2657–2662

Marco ML, Sanders ME, Gänzle M et al (2021) The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on fermented foods. Nature Rev Gastroenterol Hepatol. https://www.nature.com/articles/s41575-020-00390-5

Melini F, Melini V, Luziatelli F, Ficca AG, Ruzzi M (2019) Health-promoting components in fermented foods: an up-to-date systematic review. Nutrients 11, 1189

Peters A et al. (2019) Metabolites of lactic acid bacteria present in fermented foods are highly potent agonists of human hydroxycarboxylic acid receptor 3. PLoS Genet. 15, e1008145

Sivamaruthi BS, Kesika P, Chaiyasut C (2019) Toxins in fermented foods: prevalence and preventions – A mini review. Toxins 11, 4

Tamang JP, Watanabe K, Holzapfel WH (2016) Review: Diversity of microorganisms in global fermented foods and beverages. Front Microbiol 7, 377

Tarvainen M, Fabritius M, Yang B (2019) Determination of vitamin K composition of fermented food. Food Chem 275, 515–522

Taylor B C et al (2020) Consumption of fermented foods is associated with systematic differences in the gut microbiome and metabolome. mSystems 5, e00901-19