FERMENTED FOOD FOR HEALTH AND PERFORMANCE

: by Ian Craig; in Articles; on 15 April 2016

FUNCTIONAL SPORTS NUTRITION MAGAZINE - Mar/Apr 2016

The last decade has seen a large amount of supportive evidence towards probiotic utilisation by the sports person. Ian Craig questions whether we might expect the same benefits in health and potentially performance from traditionally made fermented foods.

Early in 2015, I was standing in the queue at the local farmer’s market, waiting to pay for my super-nutritious locally grown, organic vegetables, when I got to witness the traditional making of sauerkraut: fermented cabbage, essentially. I’d eaten sauerkraut before, but this German lady’s produce was somehow different - it had the sour flavour typical of lactic acid fermentation, which complimented the taste experience of my lunchtime salad. When the stall holder then sent me a link to a on-line interview between the infamous Dr Mercola and fermenting expert and author, Sandor Katz, proclaiming a 10 trillion bacteria count in a 4-6 ounce serving (1), I was even more intrigued. Fermented vegetables may do more than simply stimulate an un-touched taste bud in your mouth; they may be a powerful probiotic.

Because it is such an important topic, we have written about gastrointestinal (GI) health and athletic performance in FSN on several occasions (2-8). For the purposes of this article, I’m going to stay very bug-focussed and attempt to bring you up to speed with the latest information on our microbiota and in particular, assess the benefits of traditional methods of fermenting foods.

What is the microbiota?

We used to simply talk about our gut based bacteria, but now we have developed names for these little critters: the microbiota and microbiome. On one hand, the purposeful naming of our gut bacteria make them sound more scientific and more important (which of course they are), but on the other hand, the nomenclature is confusing a lot of people. So, before moving on, I would like to quickly define them:

In the scientific literature, the words microbiome and microbiota are often used interchangeably, but the microbiome refers to the genetic material that bacterial cells harbour (9). The microbiome is particularly significant for human health because it is at least 150 times larger than the genome of the human host, plus the microbes in our bodies collectively make up to 100 trillion cells; ten-fold the number of human cells (10). Since in this article, we are most interested in the bacterial colonies themselves, we will refer to the ‘microbiota’.

Significantly for health, if the microbiota is disturbed via dysbiosis (an imbalance between ‘good’ and ‘bad’ bacteria), it can lead to intestinal permeability and an increase in circulating inflammatory cytokines. Immune tolerance may be threatened, meaning an increase in hypersensitivity reactions such as allergies and autoimmune diseases (11), which have become common place in hard-training athletes. For example, Sir Steve Redgrave was carrying ulcerative colitis with him into his epic 4th and 5th rowing Olympic Gold attempts. In 2011, Venus Williams was diagnosed with Sjögren's Syndrome, causing her to withdraw from the US Open, and Manchester United midfielder Darren Fletcher was diagnosed with ulcerative colitis.

Probiotics, our gut and our immunity

When it comes to an athlete’s immune and GI health, probiotic supplements have received a decent amount of scientific airtime over the past decade - this ties in nicely with the timing of the microbiota research because healthy bacterial supplements should obviously influence the microbiota in some way.

For example, a study of 64 male and 35 female cyclists were randomised to either a probiotic (Lactobacillus fermentum) or placebo treatment for 11 weeks in a double-blind, randomised, controlled trial (12). The men experienced a substantial reduction in the severity of gastrointestinal illness at the mean training load and diminished exercise-induced cytokine expression. The positive changes weren’t so apparent in females.

In relation to upper respiratory tract infections (URTIs), a common point of reference for exercise immunologists, a 2011 meta-analysis involving 3451 sporting and non-sporting subjects concluded that there is a likely benefit for probiotic supplementation in reducing URTI incidence (13). Another randomised, double-blind study investigated the effects of probiotic versus placebo supplementation during a 3-month marathon training programme in 141 runners (14). There were no differences in the number of URTI or GI infections between groups, but the duration of GI symptoms was significantly less in the runners consuming probiotics.

Finally, 14 weeks of probiotic supplementation has been shown to decrease fecal markers of zonulin (a marker of intestinal permeability) and systemic levels of oxidative stress and the inflammatory cytokine TNF-⍺ (15).

These are just a small sampling of probiotic research studies - I simply wanted to create an obvious link between the oral introduction of healthy bacteria and positive gastrointestinal and immune outcomes. View the articles by Dowson, Wakeman and Patounas (6-8) for a more comprehensive view of this topic.

Fermented food

After that fated market day, it has now been a year since I started actively increasing the food-based sources of healthy bacteria into my body and I can antidotally say that my gut has never been so happy. Most days, I consume sauerkraut, kefir and sourdough rye bread. But, were these ancient fermentation practices simply there to preserve food, and was I succumbing to the placebo effect, or are there health consequences associated with them?

If you look at pretty much any traditional culture, you’ll find fermented foods. Here are a few examples:

Sauerkraut - meaning ‘sour cabbage’ in German, is a traditional food preparation in German and Dutch communities, although there are records of the Chinese fermenting cabbage in rice wine hundreds of years ago. Sauerkraut is made by massaging organic cabbage with rough salt until the cabbage releases its liquid, and then fermenting it in a crock pot for a few weeks, depending on taste.
Kimchi - is Korean fermented vegetables, traditionally served with steamed rice at every meal. Kimchi can be made from many vegetables, but common ingredients include cabbage, radish, onions and cucumbers. Additionally it is seasoned with herbs and spices, such as ginger, garlic and chilli peppers. It is made in a similar way to sauerkraut.
Yogurt - is a word that comes from Turkey, but yogurt making can be traditionally found in pretty much any population group that kept animals for milk. Examples of bacterial colonies found in yogurts include; Bifidobacterium lactis, Lactobacillus acidophilus, Lactobacillus delbrueckii sp. bulgaricus and Streptococcus thermophilus, although many other cultures have been used. Yogurt is made by adding a starter culture (or a spoonful of your previous yogurt batch) to milk and leaving overnight at the right temperature.
Kefir - is believed to originate from the Caucasian mountains of eastern Europe. The kefir grains are made up of live bacteria and yeasts that exist in a matrix on a surface of a complex polysaccharide, with a casein core. Kefir contains many species of bacteria and yeasts, which can vary depending on culturing location and conditions (16,17). It is made by adding the grains to a glass container of milk and leaving for one to two days.
Other fermented foods - soya products such as natto, tempeh and miso, sourdough breads, kombucha (fermented teas), cheeses, beer, wine and cider.

According to Sandor Katz (18), the benefits of fermenting foods include: pre-digestion of our foods, increasing nutrient-density (especially B-vitamins and certain minerals), activating certain active compounds (see glucosinolates below), and breaking down toxins such as pesticides found in food and anti-nutrients such as phytates, which can bind and inhibit absorption of minerals into our body.

With the excitement and realisation that my daily ferments were good for me, I took to Pubmed. After all, if what Dr Mercola said about sauerkraut is correct, and I can get over a trillion healthy micro-organisms into my salad compared to several billion from my expensive white pill, then we’re onto something good.

Fermented milk products

To keep my search focussed, I only considered yogurt and kefir, using the search terms ‘yogurt benefits’, ‘yogurt probiotic’, ‘kefir health’ and ‘kefir probiotic’.

In the past decade, it seems that the research on yogurt and kefir has really taken off. Daily consumption of a probiotic food may be useful in improving digestive comfort and symptom experience of adults with good health (19). Other benefits associated with the fermented milk have included the reduction of lactose intolerance symptoms, stimulation of the immune system, lowering of cholesterol, and anti-mutagenic and anti-carcinogenic properties (20,21). In particular, human studies have clearly demonstrated that yogurt containing viable bacteria (Streptococcus thermophilus and Lactobacillus delbrueckii sp. bulgaricus) improves lactose digestion and eliminates symptoms of lactose intolerance (22). Importantly, it appears that probiotics administered to the body through the medium of yogurt or cheese survives the gastrointestinal tract (23) and can adhere to GI epithelial cells (17).

Salva and colleagues (24) additionally demonstrated that a fermented milk product, used during the recovery of immunocompromised malnourished mice, effectively accelerated the recovery of certain clinical parameters associated with malnutrition, and it increased the resistance against intestinal and respiratory infections.

Helicobacter pylori (H. pylori) infection has been noted as the major cause of acute and chronic gastritis, gastro-duodenal ulcers and gastric cancer. Interestingly, Yang and Sheu (25) demonstrated that children infected with H. Pylori had a lower fecal Bifidobacterium spp. count and Bifidobacterium spp. to E. coli ratio when compared with control subjects. Four weeks of yogurt consumption reduced the IL-6 cytokine and H. Pylori counts, while elevating the secretory IgA levels (indicative of improved GI immunity).

And finally a sport-specific kefir study: 67 young males and females were divided into an endurance training or active control group with a kefir or control drink consumed twice per week (26). The structured training programme was over a 15-week period, which resulted in an improvement in 1500m running times. The authors noted that kefir consumption may have been associated with attenuation of the C-reactive protein increases that were seen during the training programme, leading them to conclude that kefir may improve the risk profile with respect to cardiovascular disease. The authors didn’t exactly exude extreme confidence with their conclusions, but it’s a good start - what might have happened to recovery if the subjects had consumed kefir every day?

Fermented vegetables

Again, I kept my search quite focussed and used the terms ‘sauerkraut health, ‘sauerkraut probiotics’, kimchi health’ and ‘kimchi probiotic.’

According to Park et al (27), from their research and that of others, the health functionality of kimchi includes anti-cancer, anti-obesity, anti-constipation, colorectal health promotion, probiotic properties, cholesterol reduction, fibrolytic effects, anti-oxidative and anti-ageing properties, brain health promotion, immune promotion, and skin health promotion. Additionally, Han and colleagues (28) confirmed that a specially prepared kimchi reduced the H. pylori-induced expression of the pro-inflammatory COX-2 enzyme, inducible nitric oxide synthase (iNOS) and tumour necrosis factor alpha (TNF-α), and induced apoptosis specifically to gastric cancer cells.

With respect to sauerkraut, several of the Lactobacillus plantarum strains that were isolated from Chinese sauerkraut were found to possess desirable probiotic properties. This included the ability to survive at a pH of 2.0 for 60 min, tolerate pancreatin and bile salts, and produce anti-microbial activity against E. coli O157 and Shigella flexneri CMCC(B) (29). Additionally, researchers showed that the fermentation of cabbage, even if subsequently heated, increased the initial values of antioxidant activity (30) and vitamin C levels, which would typically drop after a vegetable was picked, showed a good retention percentage in sauerkraut and in sauerkraut juice, ranging from 62 to 100 per cent (31).

Cruciferous vegetables, including cabbage, are known for their detoxification-supporting effects; the fermentation process, via enzymatic conversion of glucosinolates, leads to the formation of ascorbigen, indole-3-carbinol and isothiocyanates, which collectively support Phase I and II detoxification pathways (32,33). Palani et al (32) found that peak levels of these detoxifiers appeared between days five and nice of fermentation, so if this was your sole purpose for making sauerkraut, it may be best to stop the process after about a week. This of course will depend on the season, because fermentation occurs at a more rapid rate in higher temperatures and it’s been shown that fermentation outcomes vary per season and location (34).

Another useful property of sauerkraut is that Lactobacillus plantarum ZS2058, found in the fermented cabbage has been shown to synthesise conjugated linoleic acid (CLA) (35). CLA is a popular weight-loss supplement and its use has also been linked to improved outcomes with several degenerative diseases.

For a comprehensive view of traditional fruit and vegetable fermentation, read the review article by Swain et al (36).

Conclusions

Let’s finish with reference to a systemic review entitled ‘Probiotics and athletic performance’ (37). The author (Nichols) noted that numerous health benefits have been attributed to probiotics from fermented foods, including better GI health and immune function, plus improved control of blood lipids, blood pressure, and allergic conditions. The review failed to elicit any ergogenic benefits from probiotic consumption, but this is not the point of such an enquiry. The point is that if we can improve the health of an athlete via consumption of fermented food, we can improve their potential for athletic performance and recovery from training. Following this thought, Nichols went on to highlight two studies that demonstrated an enhanced immune responses of fatigued athletes who were taking probiotics. Nichols then rightly concluded, as I do, that probiotics (from foods or quality supplements) may provide athletes with secondary health benefits such as improved GI function, immunity, recovery from fatigue, which will positively support performance during training and competition.

If we compare probiotic supplements with fermented foods, the advantage of supplements is that you cannot certify that they contain certain strains of micro-organisms in certain quantities, while the advantage of fermented foods is that if well prepared, they contain a large microbial diversity, just as we find in the human digestive tract.

Footnote

For more information about fermented products, the website www.culturesforhealth.com is useful.

References

Plotner B (2014). Sauerkraut Test Divulges Shocking Probiotic Count. Nourishing Plot. www.nourishingplot.com/2014/06/21/sauerkraut-test-divulges-shocking-probiotic-count/ (accessed Feb 2016)
Craig I (2010). Gut instinct: how to stop digestion being a performance limiter. Functional Sports Nutrition. 1(3): 6-8.
Bailey C (2011). Practical solutions for testing and tackling food allergies. Functional Sports Nutrition. 1(10):6-8.
Walker A (2011). Do you have the guts to train? Functional Sports Nutrition. 1(10):14-15.
Clay L (2011). Does your fitness have holes in it? Functional Sports Nutrition. 1(10):16-18.
Dowson D (2013). Probiotics and sports nutrition. Functional Sports Nutrition. Jan/Feb 2013:30-31.
Wakeman M (2013). Functional probiotics and their role in sports performance. Functional Sports Nutrition. Nov/Dec 2013:24-26.
Patounas H (2015). The gut microbiota and Formula 1 performance. Functional Sports Nutrition. Jul/Aug 2015:8-10.
Ursell L et al (2012). Defining the human microbiome. Nutri Rev. 70(supp 1):S38-S44.
Qin J et al. MetaHIT Consortium (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 464:59–65.
Bischoff S (2011). “Gut health”: a new objective in medicine? BMC Med. 9:24.
West N et al (2011). Lactobacillus fermented (PCC(R)) supplementation and gastrointestinal and respiratory tract illness symptoms: a randomised control trial in athletes. Nutrition Journal. 10:30.
Hao Q et al (2011). Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst Rev. 9:CD006895.
Kekkonen R et al (2007). The effect of probiotics on respiratory 282 infections and gastrointestinal symptoms during training in marathon runners. Int J Sport Nutr Exerc Metab. 7:352-363.
Lamprecht I et al (2012). Probiotic supplementation affects markers of intestinal barrier, oxidation, and inflammation, in trained mean; a randomised, double-blinded, placebo-controlled trial. J Int Soc Sports Nut. 9:45.
Chen H et al (2008). Microbiological study of lactic acid bacteria in kefir grains by culture-dependent and culture-independent methods. Food Microbiology. 25:492–501.
Diosma G et al (2014). Yeasts from kefir grains: isolation, identification, and probiotic characterization. World J Microbiol Biotechnol. 30(1):43-53.
Katz S (2012). The Art of Fermentation. Chelsea Green Publishing.
Guyonnet D et al (2009). Fermented milk containing Bifidobacterium lactis DN-173 010 improved self-reported digestive comfort amongst a general population of adults. A randomized, open-label, controlled, pilot study. J Dig Dis. 10(1):61-70.
Guzel-Seydim Z et al (2011). Review: functional properties of kefir. Crit Rev Food Sci Nutr. 51(3):261-268.
Shiby V & Mishra H (2013). Fermented milks and milk products as functional foods - a review. Crit Rev Food Sci Nutr. 53(5):482-96.
Guarner F et al (2005). Should yoghurt cultures be considered probiotic? Br J Nutr. 93(6):783-786.
Saxelin M et al (2010). Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese. Int J Food Microbiol. 144(2):293-300.
Salva et al (2011). Development of a fermented goats' milk containing Lactobacillus rhamnosus: in vivo study of health benefits. J Sci Food Agric. 91(13):2355-2362.
Yang Y & Sheu B (2012). Probiotics-containing yogurts suppress Helicobacter pylori load and modify immune response and intestinal microbiota in the Helicobacter pylori-infected children. Helicobacter. 17(4):297-304.
O'Brien K et al (2015). The effects of postexercise consumption of a kefir beverage on performance and recovery during intensive endurance training. J Dairy Sci. 98(11):7446-7449.
Park K et al (2014). Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. J Med Food. 17(1):6-20.
Han Y et al (2015). Dietary, non-microbial intervention to prevent Helicobacter pylori- associated gastric diseases. Ann Transl Med. 3(9):122.
Yu Z et al (2013). Evaluation of probiotic properties of Lactobacillus plantarum strains isolated from Chinese sauerkraut. World J Microbiol Biotechnol. 29(3):489-498.
Kusznierewicz B et al (2008). The effect of heating and fermenting on antioxidant properties of white cabbage. Food Chem. 108(3):853-861.
Goldoni J et al (1983). Comparative study of vitamin C of cabbage cultivars (Brassica oleraceae L., var. capitata L.), before and after their processing in sauerkraut. Arch Latinoam Nutr. 33(1):45-56.
Palani K et al (2016). Influence of fermentation on glucosinolates and glucobrassicin degradation products in sauerkraut. Food Chem. 190:755-762.
Tolonen M et al (2002). Plant-derived biomolecules in fermented cabbage. J Agric Food Chem. 50(23):6798-6803.
Martinez-Villaluenga C et al (2009). Influence of fermentation conditions on glucosinolates, ascorbigen, and ascorbic acid content in white cabbage (Brassica oleracea var. capitata cv. Taler) cultivated in different seasons. J Food Sci. 74(1):C62-67.
Yang B et al (2015). Complete genome sequence of Lactobacillus plantarum ZS2058, a probiotic strain with high conjugated linoleic acid production ability. J Biotechnol. 214:212-213.
Swain M et al (2014). Fermented Fruits and Vegetables of Asia: A Potential Source of Probiotics. Biotechnol Res Int. 2014:250424.
Nichols A (2007). Probiotics and athletic performance: a systematic review. Curr Sports Med Rep. 6(4):269-273.