How to make kimchi plus everything you always wanted to know about fermented foods

Kimchi daysFermented foods, such as sauerkraut and kombucha, have become increasingly popular in the health space at the moment. I have been making sauerkraut at home for several years in the belief that the bacteria responsible for the fermentation of the cabbage, lactic acid bacteria (LAB), predominantly Lactobacillus plantarum, 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 this blog and have been writing more in depth articles about health related topics, I started thinking about what actual research has been conducted on the health benefits of fermented foods and do the bacteria within fermented foods actually survive the harsh conditions of the gastrointestinal tract, particularly the stomach? Hence I put together this review (supported by peer-reviewed science) about everything I always wanted to know regarding fermented foods.

What are fermented foods?

Fermentation is a predominantly anaerobic process, meaning without oxygen, carried out by microorganisms or cells in which sugars, such as glucose, are converted to other compounds, such as alcohol, for the purpose of energy production. Typically bacteria and yeast, 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 all throughout the world, with particular foods being unique to certain ethnic groups (1). Not only does the fermentation of foods add to the flavour and texture, but fermentation also improves the shelf-life of food. It is believed that fermentation processes were originally developed as a way to preserve fruit 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

Fermented diary

Lactic acid bacteria (LAB) are the main bacteria involved in the production of fermented dairy products, such as yoghurt, cheese and kefir milk, where they convert lactose (the main sugar in milk) to lactic acid. This results in an increased acidity making the growth of other microorganisms unfavourable. The most common LAB involved in the fermentation of dairy include members of the genera Lactobacillus, Streptococcus, Leuonostoc, Enterococcus and Lactococcus. Bifidobacteria are also included in fermented milk products. (4). Yoghurt is typically produced by using a culture of L. delbrueckii subp. bulgaricus and S. thermophiles (5).

During the fermentation of dairy a number of beneficial compounds are produced by the metabolic activity of LAB, propionibacteria, yeast and mould. The content of vitamin B-12, folic acid and biotin are enriched during the fermentation of milk by LAB (6). Conjugated linoleic acid (CLA), which I have previously discussed, is also increased in fermented milk (7). Bioactive peptides with reported antihypertensive, antimicrobial, antioxidative and immune-modulatory activities are released by the activity of LAB in fermented milk products (8). Galactooligosaccharide, which is synthesized by LAB from lactose, has a prebiotic effect on intestinal microbiota, meaning it 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). The acidic environment created by fermentation with LAB can enhance the bioavailability of these minerals. Furthermore, 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).

Harmful compounds, including mycotoxins and biogenic amines can also contaminate fermented dairy products, however, strict regulatory standards are set by international agencies for the monitoring of these substances and reliable methods to detect these compounds have been developed (13-16).

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 includ bladder cancer, cardiovascular disease and periondontitis (17-19).

Kombucha

Kombucha has become a popular fermented beverage. It is a sweetened black tea fermented by a symbiotic colony of bacteria and yeast, meaning that both the bacteria and yeast live in close physical association and have a mutually beneficial relationship. The interaction of these microorganisms results in a floating cellulose layer on the surface of the fermented tea, which becomes thicker the longer it is fermented. The species that constitute the bacterial component of kombucha cultures are the acetic acid bacteria Acetobacter xylinum, A. xylinoides, Bacterium gluconicum, A. suboxydans, Gluconbacter liquefaciens, A. aceti and A. pasteruians and LAB including Lactobacillus bulgaricus (20).

The earliest known use of this beverage was by Dr. Kombu in 220BC who used it to cure the digestive troubles of Japan’s emperor (I did not make this up!) (21). The main metabolites found in kombucha are acetic acid, lactic, gluconic and glucuronic acids (22, 23). Kombucha also contains polyphenols, amino acids, vitamins and a variety of micronutrients (24).

Not a lot of studies have been conducted on the health benefits of kombucha. However, I did discover that kombucha contains the compound D-saccharic acid-1,4-lactone (DSL). DSL is a derivative of D-glucaric or saccharic acid (25) and is known to possess antioxidative properties (26). The chronic hyperglycemia associated with diabetes mellitus results in oxidative stress due to the overproduction of reactive oxygen species causing tissue damage such as renal (kidney) injury (27). Studies investigating the effects of feeding DSL to diabetic rats found that DSL was able to reduce renal injury and oxidative stress in the kidney tissues. The authors of this study speculate that this is due to the ability of DSL to maintain intracellular antioxidant machineries, such as the antioxidant enzymes superoxide dismutase, catalase and glutathione reductase, at normal levels (28, 29).

Fermented vegetables

The fermentation of vegetables by LAB is recognized as a simple and valuable method to maintain and enhance the safety, nutritional quality and the shelf life of vegetables. This method is particularly important 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, and olives. Typically the fermentation of vegetables occurs spontaneously by the surface microbiota, however, starter cultures are also used. Starter cultures can 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 (30).

Lactic fermentation has been shown to enhance the nutritional value of foods, including vegetables. Lactic fermentation of maize, soybeans and sorghum (a grain) reduces the content of phytate, a well-known inhibitor of iron and zinc absorption (31). It has also been shown that fermentation of maize enhances the bioavailability iron (32). A recent 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 (33).

One of the metabolites produced by the LAB responsible for the fermentation of vegetables, known as bacteriocins (antimicrobial compounds which are discussed later), has attracted attention for their potential use as safe and natural food preservatives (34).

The impact of fermented foods and probiotics on the human gut microbiome and health

With our increasing understanding of the importance of the human gut microbiota and microbiome to health and disease, research in this field has focused on how the composition of this complex bacterial community is modulated (to clarify the gut microbiota is the microorganisms that inhabit the gut while the gut microbiome is the total genome content of the gut microbiota). Diet is one of the main factors that influence the human gut microbiota (35, 36). Many food-ingested bacteria are capable of transiently or temporarily integrating into the gut microbiota where they may have an impact on the composition and the activity of the resident gut microbial community. These food-ingested bacteria can be found in fermented foods and as probiotics. Probiotics are defined as the live microorganisms, when supplemented in adequate amounts as part of food, confer a health benefit on the host (37). The bacteria used to ferment foods can be considered probiotics. Recent research suggests that the human gut microbiome is made up of a core AND a variable commensal community and it seems that bacteria ingested via food contribute to this ‘variable microbiome’ (38).

As already discussed, LAB are the most widely used strains to ferment foods. Some LAB species are thought to be permanent inhabitants of the gastrointestinal (GI) tract while other species, such as L. plantarum, L. rhamonosus and L. paracasei appear to be transient colonizers (39). Some species of bifidobacteria, which are the dominant members of the microbiota of breast-fed babies (40) but make up only 1% of the total adult gut bacteria (41), are also typical members of the transient microbiota (42). Some species of bifidobacteria are used as probiotics. The propionibacteria, commonly used to make Swiss-type cheeses, are another common form of ingested microbes (43).

In order for ingested bacteria to have any sort of beneficial impact in the human intestinal system, they must first be able to survive within the food matrix. A number of factors can affect the probiotic viability in the food matrix, such as the acidity, oxygen availability, the concentration of sugars, the moisture content and the storage temperature (44).

Next these microbes must be able to withstand the very hostile environment of the human upper GI tract. After ingestion, the bacteria from fermented foods and probiotics initially passage through the stomach, which is very acidic (pH <3) and contains enzymes, such as pepsin, which break down proteins. Most ingested bacteria will not survive. Those bacteria that do happen to survive then enter the small intestine, where the pH rises to over 6, but they are exposed to bile and more digestive enzymes, such as pancreatin and lipase. Some bacterial strains can recover, and even grow in the small intestine before these cells continue on to the colon (45). Ingested bacteria must also be able to adhere to the gut epithelial cells of the human host in order to have any beneficial effects (46, 47).

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 (45, 48-50).

Numerous clinical studies have been conducted investigating the impact of probiotics on human health. The reported beneficial effects of probiotic consumption include improvement of constipation, diarrhea, intestinal inflammatory conditions such as, Crohn’s disease, ulcerative colitis, irritable bowel syndrome and necrotizing enterocolitis (51), and the prevention of allergic disease in infants (52, 53). Furthermore, supplementation with probiotics has been shown to positively enhance immune system function (54-56), improve the symptoms of lactose intolerance, and can prevent infection with pathogenic or disease causing microorganisms (57). The mechanisms by which probiotics exert these benefits to humans are not yet totally clear. What the research tells us is that the intestinal epithelial cells of the GI tract are a very 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 (58, 59). The latest research suggests that possible mechanisms for the health benefits of probiotics include outcompeting disease causing bacterial pathogens, inhibiting attachment of pathogens to host cells (60-62), strengthening the mucosal barrier (63), stimulation of anti-inflammatory cytokine production (cytokines are cell signalling proteins which are produced by a range of cells, importantly immune cells) (64, 65) and the production of antimicrobial substances, including bacteriocins (66), which are antimicrobials peptides that inhibit the growth of other bacteria, organic acids and hydrogen peroxide (67).

Products containing probiotics can come as either supplements, such as pills and capsules, or as foods. In 2009 it was estimated that the global probiotic supplement market was approximately $1.5 billion USD (68) and was predicted to expand to $32.6 billion by 2014 (69). It is estimated that the probiotic industry holds about a 10% share of the global functional food market (70). There seems to be agreement in the literature that at least 108 – 109 (100 000 000 – 1 000 000 000) viable cells must reach the intestine for health benefits to be achieved. This means that the product or food must contain 108 – 109 CFUs/serving (CFUs stands for colony forming units – when the product/food is plated, this amount of colonies must grow from 1 serving) (71-73). The traditional method of plating used to validate the amount of bacteria present in food is quite time-consuming, however, faster more reliable methods are becoming available. A study in 2013 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). This strain was mentioned on the product’s package (74). Other studies have also found that commercial yoghurts do contain significant numbers of Lactobacillus species to confer potential health benefits (75).

So do the bacteria within commercial yoghurts actually survive the treacherous journey through the human GI tract? A study involving 15 healthy volunteers between the ages of 24 and 46 looked at the effect of commercial yoghurt consumption containing probiotic LAB on the fecal bacterial community. The subjects were divided into 3 groups with one group consuming 110grams of yoghurt A, one group consuming 180ml of yoghurt B and the third group consuming 90 grams of yoghurt C. The subjects consumed one serve 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. The study also detected changes in the populations of bacterial groups of the fecal microbiota in all three groups (76). This study showed that probiotic strains in yoghurt can survive the human GI tract, however, it seems that the consumption of yoghurt, and not just the presence of probiotics in the yoghurt, can influence the composition of bacterial groups in the fecal microbiota. Another study involving 36 subjects looked at the persistence of 4 probiotic strains administered as capsules, yoghurts or cheese at a dose of 1.9 – 5.0 x 109 CFUs. This study found that all four probiotic strains survived the GI tract and could be detected in fecal samples following consumption in all subjects. This study also found that the food matrix had an effect on the survival of 2 of the 4 strains, with the highest quantities recovered in the fecal samples from the yoghurt group (77). These studies suggest 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.

On 24 April 2013, the First Global Summit on the Health Effects of Yoghurt was held. Keep in mind that sponsors of this event included the Dairy Research Institute and the Danone Institute, who may have vested interests. However, The Nutrition Society and The American Society of Nutrition were also sponsors. The conclusions from this summit were that there is accumulating preclinical, clinical and epidemiological evidence to support the health benefits associated with yoghurt consumption. Further research needs to be conducted to firmly establish these findings including investigations across the life span, from the very young to the old, randomized, placebo-controlled studies in healthy and diseased populations, more detailed descriptions of the types and doses of bacteria present in the yoghurt products being used in studies, assessment of the delivery matrix on the efficacy of probiotic bacteria, the effects of live compared to killed bacteria in yoghurt and studies into the mechanisms of yoghurt and/or probiotic bacteria on gut health and the microbiome (5).

So what about the health benefits of other fermented foods, such as vegetables? I will focus on kimchi as, eventually, I will be describing how to make this tasty fermented side dish. Kimchi has been consumed for about 2000 years in Korea. The most popular kimchi is baechu or chinese cabbage kimchi, which is generally made by LAB fermentation of beachu cabbage, radish, green onion, red pepper powder, garlic, ginger and fermented seafoods (78). Usually kimchi contains approximately 107 – 109 CFUs/gram of LAB. The LAB profile of kimchi actually changes during the fermentation process due to the pH. Leuconostoc mesenteroides is present during the early fermentation (pH 5.64 – 4.27) while Lactobacillus sakei dominates in the later stages of fermentation (pH 4.15) (79). 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 (80, 81).

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 (82). L. plantarum from kimchi has shown various immune-modulatory activities, such as the activation and stimulation of cytokine production in macrophages (a type of innate immune cell) from mice (83, 84). Furthermore, L. plantarum enhanced immune function when fed to mice (85, 86). LAB from kimchi was found to have antiobesity effects in rats (87, 88) and in mouse adipocytes (fat cells) (88). LAB isolated from kimchi has shown antimicrobial activities against a range of pathogenic bacteria (89, 90).

Again this raises the question of whether the LAB found in kimchi can survive the human GI tract? One study found that L. plantarum KC21 isolated from kimchi showed acid and bile tolerance and the ability to adhere to human intestinal cells (90). Another study found that human subjects who consumed 300grams/day of kimchi containing 108 CFU/gram of LAB for 2 weeks had significantly higher counts of fecal Lactobacillus species and Leuconostoc species during the kimchi intake period (91). These results suggest that if LAB is present in sufficient numbers in your kimchi then the bacteria will survive the journey through your GI tract and may confer health benefits.

Conclusions

My final thoughts after conducting this thorough analysis of the research are as follows: although further research needs to be conducted on probiotics, including those found in fermented foods, it is clear that these microorganisms have positive effects on human health. It also seems that the consumption of fermented foods can have a can confer these health benefits, if the bacteria are present in high enough numbers to begin with and have survived the storage conditions. Not only do the microbes themselves confer health benefits, but the fermentation process also enhances the nutritional qualities of the food. I will continue to enjoy fermented foods knowing that the microbes are beneficial for my health. However, I do suggest that you are wary of the high sugar content that is present in a lot of commercially available yoghurt and go for unsweetened and add you own stevia or a little bit of honey.

Now that we have established that fermented foods are good for your health, here is how to make kimchi.

As with most of my recipes, I am always looking for short cuts that reduce the preparation time without reducing the quality of the end product. Some methods for making kimchi that I came across online instruct you to soak the cabbage overnight, but in my experience this is not necessary. I soak the cabbage for one hour and the texture is perfect and the fermentation is successful.

Typically kimchi contains a seafood flavour, such as fish sauce or shrimp paste, however, I actually despise both of these ingredients and although I do enjoy traditional kimchi, I decided to have a go at making kimchi without the seafood flavour. I enjoyed the taste, so this version is actually vegan. I find the process of making kimchi enjoyable, it is tasty, there are health benefits associated with eating it, beyond the presence of the probiotics, and the total cost to make a huge jar, which keeps in the fridge, was about $3. Have a go at it this weekend. I will be posting some follow up recipes involving my homemade kimchi soon.

Homemade kimchi

Ingredients

¾ wombok cabbage

Salt

3 tablespoons Korean red pepper powder (purchase this at your local Asian supermarket)

3 tablespoons soy sauce

1 large clove garlic, finely minced

3 cm fresh ginger, finely grated

3 tablespoons water

2 shallots (green part only), chopped

Utensils

Chopping board

Sharp knife

Large mixing bowl

Colander or large strainer

Small mixing bowl

Spoon

Large glass jar with lid for fermenting

Method

  • Chop the wombok cabbage into quarters lengthwise and remove the core. Slice the cabbage into about 2 -3 cm thick strips and place the cabbage into a large bowl. Salt the cabbage and massage it with your hands until it begins to soften. Cover the cabbage with water and allow it to soak for at least one hour.Kimchi soaking cabbage
  • Keep ¼ cup of the salty water that the cabbage is soaking in. Place the cabbage into a colander or large strainer and rinse it well in water and drain it. Rinse the bowl that the cabbage was soaked in and place the cabbage back into the bowl after it has drained.
  • To make the paste combine the red pepper powder, soy sauce, garlic, ginger and water into the small mixing bowl and mix well. Add in the chopped shallots and mix.Kimchi paste
  • Add the kimchi paste to the cabbage and mix it into the cabbage. I found using clean hands is the easiest way to do this.

Kimchi cabbage mixed

  • Using your hands put the cabbage into a large glass jar, pressing the cabbage down firmly with each handful. The idea is to remove as much oxygen as possible to create the correct environment for the fermentation to occur. This process does get a bit messy.
  • Wipe the sides of the jar down and place the kimchi into a warm spot to ferment. I typically ferment my kimchi for 3 days, however, I believe that this would vary depending on the climate. I live on the Gold Coast in Queensland, Australia. Even in the middle of winter the temperature can reach 20°C, so if you live in a colder climate you may need to ferment it for longer. Taste the kimchi and continue fermenting until your desired taste is achieved.Kimchi day 0
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14 thoughts on “How to make kimchi plus everything you always wanted to know about fermented foods

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      • It’s very easy to make and would be a breeze for someone with your background. It’s has a Greek yogurt taste only a little tangier. It’s great for making smoothies and salad dressing. If you follow my be healthy board in Pinterest I have several good articles on how to. Look me up under pinners as Hilda Solares. It would be a great post for you to put up.

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      • That’s awesome! Are they live ones? If so the process is fairly easy and it’s basically means replacing every 24 hours with fresh whole milk. It must not be skim or fat free. You drain or scoop out the grains and pour the kefir that forms into a container and place in the fridge. I keep adding to the container a weeks worth at a time. I also just replace the milk and don’t even bother to wash the container where the grains are forming the kefir. It must be in a mason jar because the pressure will cause it to explode. But your the scientist😜 can’t wait to see what all you learn 😚

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  2. Pingback: Giant kimchi pancake for one | I can't believe that's healthy

  3. I’m half Korean and grew up on this stuff! I feel like most people who have tried kimchi either love it or hate it, there is no in between! I’m glad to see this recipe being shared! When my family makes it, we add a splash of coke for a kick and Saeujeot (Salted Fermented Shrimp) to give it a very slight fish taste. Thanks for sharing your recipe! -Angela

    http://www.hangrywife.com

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  4. Hi Lucy, for the fermentation of the Sauerkraut etc do you use the same kind of jar with a lid? because I just find you blog today and I purchased yesterday some large glass jars ($4 from Woolworths in Melb for the 2 Lt+) with a plan to do some fermentation, during the next few days I will drill a hole in the top to add an airlock to stop outside air going in during the fermentation process, and for storage I will install in the same hole some sort of rubber seal into the hole if you look here (http://goo.gl/DtSGU9) my plans are very similar. But for the airlock I will use the ones with the S shape than you can see in the following link to eBay http://goo.gl/M8KZZO . From Ozfarmers the same jars with hole and airlock cost a lot more. As well when I was reading your writting about milk kefir I remembered the episode 4 of “Superfoods the real story” from the UK than was aired only in the last weeks, here it is the link to episode
    http://www.dailymotion.com/video/x2zgzgm but on the top right you have the other 3 shows. Thanks for the all tech info included in all your posts.

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    • Hi Raul,
      I just use a simple glass jar with a lid. The lid has a rubber seal – it does not even lock on. I have never heard about creating an airlock and have never bothered to do this and my fermenting of sauerkraut and kimchi has been successful so far. I honestly don’t think you need to bother. The liquid creates a fairly anaerobic environment and I believe that the high salt content will prevent the growth of most bacteria except the Lactobacillus species that you are after. Just make sure you give the glass jars a good wash before you start.

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