Fermented foods, such as sauerkraut and kombucha, have become popular for health reasons. I have made my own sauerkraut in the past and have recently made the tasty, fermented Korean side dish, kimchi. I did it not only for the taste but also for the hope that the bacteria responsible for the fermentation of the cabbage — lactic acid bacteria (LAB) — would contribute to the diversity of my gut microbiota.
As a research scientist in the field of bacterial pathogenesis, this made sense to me. Now that I have started blogging about health and fitness and have been writing more in depth articles about health related topics, I started wondering what research has been done on the health benefits of fermented foods. Can the bacteria in fermented foods even survive the harsh conditions of the human gastrointestinal (GI) tract, particularly the stomach?
I was amazed to learn that the fermentation of food has been used by humans for thousands of years as a way to preserve foods, and that the health benefits go beyond their microorganisms (don’t worry, citations are provided below). The fermentation process enhances the nutritional quality of food by contributing beneficial compounds such as vitamins, and by increasing the bioavailability of minerals. Probiotics, including those found in kimchi, have a range of positive effects on health, including the improvement of various intestinal inflammatory conditions, positive impacts on the immune system and even weight loss, and can alter the composition of the gut microbiome.
However, these effects mostly depend on whether the bacteria actually make it in sufficient numbers to the colon. And let me tell you, the journey to the colon is one harsh and dangerous ride!
What are fermented foods?
Fermentation is a mostly anaerobic process, meaning without oxygen, carried out by microorganisms or cells. These microorganisms convert sugars, such as glucose, into other compounds, such as alcohol, to produce energy to fuel their metabolism. Bacteria and yeasts — which undergo lactic acid fermentation and ethanol fermentation, respectively — are used in the fermentation of foods. The unique flavours and textures of fermented foods are due to the different species of bacteria and yeast used.
Humans have fermented foods for thousands of years throughout the world, and many dishes are unique to specific ethnic groups.1 Not only does the fermentation of foods add flavour and texture, but fermentation can also improve its shelf-life and may have been initially used to preserve fruits and vegetables during times of scarcity.2 The fermentation of food can occur spontaneously by the natural LAB surface microflora or by the use of a starter culture.3
Types of fermented foods
Lactic acid bacteria are the main bacteria in the production of fermented dairy products, such as yoghurt, cheese and kefir milk. They make lactic acid from lactose, the main sugar in milk. This increases acidity and makes life difficult for other microorganisms. The most common LAB involved in the fermentation of dairy are members of the genera Lactobacillus, Streptococcus, Leuonostoc, Enterococcus, and Lactococcus. Bifidobacteria are also included in fermented milk products.4 Most yoghurt, the fermented dairy product people know best, is produced with a culture of L. delbrueckii subp. bulgaricus and S. thermophiles.5
During the fermentation of dairy, many beneficial compounds are produced or increased by the metabolic activity of LAB, propionibacteria, yeast and mould, such as vitamin B-12, folic acid and biotin.6 Conjugated linoleic acid (CLA), a fatty acid with reported health benefits including fat loss, is also increased in fermented milk7 (I have previously blogged about CLA and found the mechanism by which it causes fat loss somewhat concerning, as it may damage surrounding cells, increase fatty deposits in the liver, and make blood lipids more prone to atherosclerosis aka hardening of the arteries.) Bioactive peptides with reported antihypertensive, antimicrobial, antioxidative, and immune-modulatory activities are also released by the activity of LAB in fermented milk products.8
Another potentially beneficial compound in fermented dairy is the non-digestible carbohydrate galacto-oligosaccharide, which is synthesized by LAB from lactose. Galacto-oligosaccharide has a prebiotic effect on intestinal microbiota, meaning it probably promotes the growth of beneficial bacteria in the gut.9
In addition, yoghurt in particular is a rich source of dietary minerals, including calcium, magnesium, potassium, phosphorus, and zinc.10 The concentration of these minerals is nearly 50% higher in yoghurt than in milk,11 and they are easier to digest and absorb: the acidic environment created by fermentation with LAB can enhance the bioavailability of these minerals.
And there’s more: yoghurt is also an excellent source of essential amino acids. The amount of free amino acids is increased due to the pre-digestion of milk proteins by the activity of bacterial cultures, allowing for better protein digestibility.12
Large cohort studies conducted in the Netherlands, Sweden, and Denmark found that fermented milk products were significantly associated with decreased disease states. These disease states include bladder cancer, cardiovascular disease, and periondontitis.13-15 Based on these findings, I am going to enjoy my Greek yoghurt for breakfast even more now!
Although harmful compounds, including mycotoxins and biogenic amines, can contaminate fermented dairy products, strict regulatory standards are set by international agencies for the monitoring of these substances. Fortunately, reliable methods to detect these compounds have been developed.16-19
The fermentation by LAB is recognized as a simple and valuable method to maintain and enhance the safety, nutritional quality, and the shelf life of vegetables, particularly when access to fresh vegetables is limited. The most commercially significant fermented vegetables are:
- Cabbage, in the form of sauerkraut and kimchi
- Cucumbers, in the form of pickles
Typically the fermentation of vegetables occurs spontaneously just from the bacteria already present on the surface, but starter cultures can also be used. Starter cultures speed up the fermentation process, ensure reliability of the final product, prevent the risk of fermentation failure, and assist with the inhibition of spoilage and pathogenic microorganisms.20
Lactic fermentation has been shown to enhance the nutritional value of vegetables. When used with maize, soybeans, and sorghum (a grain), it reduces phytate content, a well-known inhibitor of iron and zinc absorption.21 It has also been shown that fermentation of maize enhances the bioavailability of iron.22 A 2015 study published in the European Journal of Nutrition found that the reason for the increased bioavailability of iron in lactic-fermented vegetables compared to fresh vegetables is due to an increase in the concentration of hydrated ferric iron (Fe3+) which may be more favourable for iron absorption.23
It is clear to me that the fermentation process boosts the nutritional quality of foods. Now, what about the impact of the actual bacteria carrying out the fermentation?
The impact of fermented foods and probiotics on the microbiome
Understanding of the importance of the human gut microbiota and microbiome to health and disease has expanded rapidly with the advances in DNA sequencing technology. (The gut microbiota is the microorganisms that inhabit the gut, while the gut microbiome is the total genome content of the gut microbiota.) Research in this field has focused on what role this complex bacterial community plays in human health and disease, and how it can be altered.
Diet is one of the main influences on the human gut microbiota.24, 25 Many food-ingested bacteria can temporarily join the gut microbiota, possibly affecting the behaviour of the resident gut microbial community. These food-ingested bacteria can be found in great numbers in fermented foods and as probiotics. Probiotics are defined as live microorganisms in food that confer a health benefit on the host.26 Here on SBM, Scott Gavura concluded, “There’s reasonably good evidence that probiotics, when taken with antibiotics, will reduce the risk of antibiotic-associated diarrhea.” In her review of Martin Blaser’s Missing Microbes, Dr. Harriet Hall wrote, “This is exciting stuff! I wish I could be alive 100 years from now to see how research into the microbiome will change the practice of medicine.”
The bacteria in fermented foods are considered probiotics.
Recent research suggests that the human gut microbiome is made up of a core population of bacteria and a variable commensal community, and it seems that bacteria ingested via food contribute to this “variable microbiome”.27 As I have already mentioned, LAB are the most widely-used strains to ferment foods. While some LAB species are thought to be permanent inhabitants of the gastrointestinal (GI) tract, other species, such as L. plantarum, L. rhamonosus, and L. paracasei appear to be temporary colonizers.28 Some species of bifidobacteria, which are found in fermented dairy, are also typical members of the transient microbiota.29
A recent study in Scientific Reports directly compared the impact of fermented and non-fermented milk products on the gut microbiome of subjects with irritable bowel syndrome (IBS). The fermented milk product altered the species of the gut microbiota more than the non-fermented milk product. Additionally, consumption of the fermented milk product decreased the “pathobionts” Bilophila wadsworthia and Clostridium sp. HGF2.30 Pathobionts is a new term describing members of the resident microbiota that have disease-causing potential.31
Bacteria derived from food appear to be members of the variable human microbiome with the ability to alter the gut microbiome. But do the bacteria we ingest in common fermented foods, such as yoghurt (and my new favourite fermented food, kimchi) actually survive once we eat them? In other words, are common fermented foods a direct source of bacteria that contribute to our microbiome?
Can bacteria from fermented foods survive the human GI tract?
Before ingested bacteria can have a beneficial impact in the human intestinal system, they must first be able to survive within the food matrix, the nutrient and non-nutrient components of food plus their interactions at a molecular level. Many factors can affect probiotic viability in the food matrix, such as the acidity, oxygen availability, concentration of sugars, moisture content, and the storage temperature.32
Immediately after swallowing, these poor little microbes must be able to withstand the hostile environment of the human upper GI tract, which includes the mouth, esophagus, stomach, and duodenum (the first part of the small intestine). After being chewed and mixed with enzymes from saliva in the mouth, the bacteria from fermented foods then pass down the throat and esophagus and into the stomach. The stomach is an extremely acidic environment (pH <3) and contains destructive digestive enzymes, such as pepsin, which break down proteins into smaller amino acid building blocks. Most ingested bacteria will not survive this first part of the journey.
Those bacteria that do survive then enter the remainder of the small intestine, where the pH rises to over 6, but they are exposed to bile and many more digestive enzymes, including amylase (which breaks starches into simple sugars), lipase (which breaks down fats), and protease (which further breaks down proteins). Some bacterial strains can recover, and even grow in the small intestine, and these cells must then continue their journey on to the colon.33 Not only must these ingested bacteria be able to survive the human GI tract, they must also be able to adhere to the gut epithelial cells in order to have any beneficial effects.34, 35
Variation in the ability of probiotic strains to survive the human GI tract has been demonstrated. Studies subjecting various strains to conditions simulating the environment of the human GI tract found that strains of B. animalis, L. casei, L. rhamnosus and L. plantarum have the greatest resilience.33, 36-38
Since many of us are familiar with yoghurt as a fermented food, I wanted to know if the bacteria within commercial yoghurts actually survive this treacherous journey. A study of 15 healthy adult volunteers looked at the effect on the fecal bacterial community of probiotic LAB in commercial yoghurt.39 The subjects were divided into three groups: one group consuming 110 grams of yoghurt A, one group consuming 180ml of yoghurt B, and the third group consuming 90 grams of yoghurt C. Everyone ate one serving per day for 20 days. The labels of yoghurt A and B stated that these products contain a probiotic Lactobacillus strain, while yoghurt C did not state this on the label.
The probiotic strains were detected in the feces of subjects consuming yoghurt A and B for up to 28 days after the first day of consumption. This showed that probiotic strains in yoghurt survive the human GI tract. The study also detected changes in the populations of bacterial groups in the fecal microbiota in all three groups.
Another similar study of 36 subjects looked at the persistence of four probiotic strains from capsules, yoghurts, or cheese at a dose of 1.9–5.0 × 109 colony-forming units (CFUs). They found that all four probiotic strains survived the GI tract and could be detected in fecal samples following consumption in all subjects. Two strains endured better, with the highest quantities recovered in the fecal samples from the yoghurt group,40 so it does seem that probiotics present in yoghurt can survive the human GI tract provided that the bacteria are present in high enough numbers in the yoghurt to begin with.
How about the LAB in kimchi? One study found that L. plantarum KC21 isolated from kimchi showed acid and bile tolerance and the ability to adhere to human intestinal cells.41 Another found that subjects who consumed 300g/day of kimchi had significantly higher counts of fecal Lactobacillus species and Leuconostoc species during the kimchi intake period.42 As with the yoghurt, these results suggest that LAB will survive in your gut if it’s present in sufficient numbers in your kimchi in the first place.
Now let’s look at the clinical studies investigating the health benefits.
Clinical studies on the health benefits of probiotics and fermented foods
Many clinical studies have investigated the effect of probiotics on human health. The reported beneficial effects of probiotic consumption include improvement of constipation, diarrhea, and intestinal inflammatory conditions (such as Crohn’s disease, ulcerative colitis, irritable bowel syndrome, and necrotizing enterocolitis),43 and the prevention of allergic disease in infants.44, 45 Furthermore, supplementation with probiotics has been shown to positively enhance immune system function,46-48 improve the symptoms of lactose intolerance, and can prevent infection with pathogenic or disease causing microorganisms.49 One promising study recently published in The Journal of Allergy and Clinical Immunology showed possible alleviation of peanut allergy in children by coadministering probiotics with a peanut oral immunotherapy. Previous studies found that administration of probiotics or peanut oral immunotherapy alone did not have this effect.80
The mechanisms by which probiotics exert these influences are not yet clear. The cells lining the intestine, the intestinal epithelial cells, are an important part of the innate or non-specific immune system and act as a link to the adaptive or specific immune system. The intestinal epithelial cells are able to recognize many bacterial components and are the first point of contact for ingested microbes.50, 51 The latest research suggests several mechanisms by which probiotic microbiota may produce health effects:
- outcompeting bacterial pathogens
- preventing attachment of pathogens to host cells52-54
- strengthening the mucosal barrier55
- release of immune-cell-stimulating and anti-inflammatory molecules (cytokines)56, 57
- the production of antimicrobial substances, including organic acids, hydrogen peroxide, and bacteriocins (small strings of amino acids that inhibit the growth of other bacteria)58, 59
Probiotics can be in food or supplements, such as pills and capsules. In 2009 the global probiotic supplement market was worth about $1.5 billion USD60 and predicted to rise to $32.6 billion by 2014.61 The probiotic industry holds about a 10% share of the global functional food market.62
How many microorganisms do you have to eat to get a benefit?
Dosages of probiotics are measured in CFUs per serving: the number of cells able to grow from a single serving (food or capsule) in a petri dish. There seems to be agreement in the literature that, for health benefits to be achieved, a dosage of 108–109 CFUs is needed.63-65 That’s one hundred million to one billion per serving. Bacteria are small!
A 2013 study published in the Journal of Applied Microbiology found between 107 and 108 CFU/ml of Lactobacillus delbrueckii subsp. bulgaricus within a commercial brand of yoghurt (Activia® from Danone) — and most people probably eat more than a fifth of a teaspoon of yoghurt at a time.66 Other studies have also found that commercial yoghurts do contain enough Lactobacillus to confer potential health benefits.67
Does kimchi have health benefits too?
Let’s zoom in on kimchi. I am a big fan of this tasty fermented side dish, and have started getting into making it at home. After looking at the studies, I am even more enthusiastic!
Kimchi has been eaten in Korea for about 2,000 years. The most popular kimchi is baechu or Chinese cabbage kimchi, which is generally made by LAB fermentation of baechu cabbage, radish, green onion, red pepper powder, garlic, ginger and fermented seafoods.68 Most kimchi contains 107 – 109 CFUs/gram of LAB. The profile of LAB species in kimchi changes with the pH throughout the fermentation process. Leuconostoc mesenteroides is present during the early stages (pH 5.64–4.27) while Lactobacillus sakei dominates in the later stages of (pH 4.15).69 Other LAB contributing to kimchi fermentation include Leu. citreum, Leu. gasicomitatum, L. brevis, L. curvatus, L. plantarum, Lactococcus lactis, Pediociccus pentosaceus, Weissella confusa and W. koreensis.70, 71
Studies investigating the potential beneficial effects of the bacteria isolated from kimchi have found the following:
- One of the LAB strains isolated from kimchi was found to have potent antioxidative activity in vitro.72
- L. plantarum from kimchi has shown various immune-modulatory activities, such as the activation and stimulation of cytokine production in mouse macrophages,73, 74 and a variety of other immune-modulating activities.75, 76
- LAB from kimchi was found to have antiobesity effects in rats77, 78 and mice.78
- LAB isolated from kimchi has shown antimicrobial activities against a range of pathogenic bacteria.41, 79
So it appears that kimchi is more than just a delicious addition to my bibimbap.
Conclusion: Fermented foods probably deserve their healthful reputation
The bacteria in fermented dairy and vegetables can survive their perilous journey through the digestive tract. Once they are there, it’s clear that they have at least some positive effects on human health, ranging from the enhanced nutritional contents of the foods themselves, to alleviation of inflammatory bowel conditions, to restoring normal gut microbiota after antibiotics, to enhancement of the immune system, and possibly even weight loss. It would be nice to know more about the mechanisms of these effects — and maybe we will know soon, because it is currently a hot area of research. I will continue to enjoy fermented foods not only for their delicious tastes and textures, but also for the health benefits. Have some fun and have a go at making your own kimchi. It is absolutely worth the effort.
Lucy Shewell, PhD, is a research scientist in the field of molecular microbiology. Her current research focuses on bacterial toxins and their interactions with host cells. Her research has been published in leading scientific journals including The Proceedings of the National Academy of Sciences and Nature Communications. In her spare time, Dr. Shewell trains for and competes in multisport and endurance races, fuels her training and racing with practical, easy to prepare, and nutritious whole foods, and researching and writing articles on topics in health, nutrition, fitness and athletic performance using quality, peer-reviewed science. You can find her whole food recipes and articles at her new blog, I Can’t Believe That’s Healthy.
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