This post will cover more of the science and nerdy aspects of fermentation. I’ll be focusing on the science of sauerkraut in particular however other ferments will pop up.

WARNING, it’s a long post and has extended well beyond what I had initially planned for this post but I could not help myself reviewing the literature.

Probiotic - Greek Pro = for , Biotic = Life — “For Life”

Bacteria involved in fermentation -

There are 4 main species of lactic acid bacteria (LAB) present in sauerkraut fermentation (Plengvidhya et.al. 2007);

1) Leuconostoc mesenteroides

2) Lactobacillus brevis

3) Pediococcus pentosaceus and

4 ) Lactobacillus plantarum

The lactic acid and acetic acid that are produced via fermentation are largely inhibitory to a lot of other microorganisms and pathological bacteria, which is the premise as to why fermented foods are preserved for such a long time and don’t putrefy like a fresh cabbage/vegetable would if just left out exposed to air (Wiander & Ryhanen, 2005). In fact it is actually the acetic acid that has the greatest antimicrobial effect (this was new to me).

Stages of fermentation

Generally speaking there are 3 stages.

Stage 1) Initiation of fermentation of the vegetable via the less acid tolerant heterofermentative LAB Leuconostoc mesenteroides over the first 3 days. This stage essentially kick starts the anaerobic (without oxygen) cycle by producing carbon dioxide and crowding out the oxygen. This is when the largest amounts of antimicrobial acetic acid are produced. During this time pH drops rapidly (Wiander & Ryhanen, 2005). This drop in pH and oxygen level provides an environment that decreases the chances of pathogenic bacteria and yeasts from proliferating. As Viander et.al., (2003) state:

a rapid decrease in pH in the beginning of fermentation is of great importance for the quality of the end product. The rapid increase in acidity minimises the influence of spoilage bacteria

This is one reason why starter cultures have been extensively used. By using a starter culture that is predominately L. mesenteroides there is a more rapid drop in pH and increase in lactic and acetic acid thus reducing the incidence of spoilage.

Stage 2) This stage then takes over and lasts upto 30 days, the two main bacteria (which are more acid tolerant) involved in this time are Lactobacillus plantarum and Lactobacillus cucumeris.

Stage 3) This last stage which lasts less than 7 days is dominated by Lactobacillus brevis, at this point the ferment is then over and you will not see any more bubbles within the ferment. One of the benefits of taste testing your ferment over the course of its fermenting time is you will be exposing yourself to the different varieties of LAB as the ferment undergoes these microbiological changes. This is another reason to support eating your ferment over the first month to 2 months whilst it is fermenting at room temperature, and if you manage to have any left over after that period then transferring it to the refrigerator. Down side is by opening the container you are allowing oxygen in and increasing the risk of cross contamination.

Starter Cultures & Other Variables

Beganovic et.al. (2011) showed that using a starter culture (Lactobacillus plantarum L4 and Leuconostoc mesenteroides LMG 7954) reduced the need for the amount of salt and decreased the fermentation time whilst increasing the overall probiotic content of the final product. Of note the research was done on whole cabbage heads NOT shredded cabbage, in which case there is a higher concentration of salt needed (4%) as opposed to (1-2%) for shredded cabbage. From my perspective I only ferment shredded cabbage anyway so this research doesn’t shed much light on the matter to me. If I do ever go down the path of fermenting whole cabbage heads I will certainly take this research into consideration though!

Viander et. Al. (2003), make the argument that by using a starter culture you can control the ferment better by initiating a more rapid drop in pH and increase the lactic and acetic acid content thereby reducing the incidence of spoilage. They also suggest that natural fermentations are hard to achieve good repeatability. Repeatability does not bother me personally it’s actually one of the things I enjoy about fermenting as each batch is a bit of a surprise and no two batches taste the same. My conclusion on starter cultures after reviewing the literature is as follows… Let me first preface that whilst my background is in the sciences I am the first to admit that research whilst important does have its limitations and quite often has motives (particularly financial oriented). I may be paranoid or overly skeptical but my interpretation on the research of this topic has me questioning whether the studies are really interested in improving fermentation or if they are trying to promote something that can be sold for profit. What we know from the science is fermentation works and works perfectly fine WITHOUT starter cultures. What these studies on starter cultures are portraying to the reader is that starter cultures possibly help improve the ferment by setting up a more “controlled” environment to allow for reproducibility between batches. This may be useful in large scale commercial production, but for small scale homemade krauts and ferments its not essential. My opinion at this point in time is that there are financial motives behind these research articles on starter cultures and I will continue to practice my fermentation without them. I am not alone with these thoughts found on page 135 of Sandor Katz book

I continue to regard the use of commercial starter cultures as unnecessary, even though they can speed fermentation and acidification. The central criticism I have of them is how they are generally marketed, which is exploiting fear and exaggerating the risk associated with spontaneous fermentation. (Katz, 2012).

Martinez-Villaluenga C., et.al. (2009) examined different fermenting conditions such as season of the year, salt concentrations (0.5% and 1.5%) and use of starter cultures (L. plantarum and L. mesenteroides). They looked at these parameters on levels of glucosinolates (GLS), ascorbigen and ascorbic acid. They did however only ferment for a total of 7 days. Summer ferments produced more GLS, whereas winter produced more ascorbigen precursor. Lower salt concentration yielded ferments with higher ascorbigen content.

Health Implications -

Research has shown that there are over 500 different species of bacteria inhabiting the human gastrointestinal tract, which accounts for approximately 95% of the total number of cells within the human body! (Lin, 2003). I find these facts staggering essentially we are more bacteria than we are human!

Parvez et.al. (2006) conducted a review of the literature on the health benefits of probiotic foods and beverages.

Some of the beneficial effect of lactic acid bacteria consumption include: (i) improving intestinal tract health; (ii) enhancing the immune system, synthesizing and enhancing the bioavailability of nutrients; (iii) reducing symptoms of lactose intolerance, decreasing the prevalence of allergy in susceptible individuals; and (iv) reducing risk of certain cancers.

Furthermore a review done by Lin (2003) states “Evidence suggests the following beneficial effects of probiotics: normalization of the intestinal microflora, ability to block the invasion of potential pathogens in the gut, prophylactic or therapeutic treatment for several types of diarrhoea, relief of symptoms of irritable bowel syndrome and inflammatory bowel disease, amelioration of lactose intolerance, prevention of colon cancer, modulation of immune function, inhibition of Helicobacter pylori, and possible enhancement of calcium absorption and reduction of blood cholesterol levels.”

Protein and fat bioavailability is enhanced via fermentation as the bacterial enzymatic hydrolysis yields free form amino acids and short chain fatty acids (Parvez et.al., 2006). Increases in folic acid, niacin and riboflavin have shown to occur during the fermentation process of certain foods (Parvez et.al., 2006). Studies have shown that probiotics are helpful in treating diarrhoea of viral or bacterial origin possibly by increasing secretary IgA, and by competing with pathogenic bacteria and viruses at the binding sites of the epithelium (Parvez et.al., 2006). Alleviation of lactose intolerance by increasing lactase activity in the small intestine (Parvez et.al., 2006). Hepatic encephalopathy is been reported to be treated with probiotics.

Probiotics have been shown to help with inflammation and arthritis, one proposed mechanism is via immune modulation and changes in cytokines and other inflammatory mediators as well as reinforcing the gut mucosal barrier (Parvez et.al., 2006). Probiotics have been shown to down regulate the immune response in people with hypersensitivity reactions such as atopic eczema and food allergies (Parvez et.al., 2006). Pessi et. al. (2000) showed that probiotics caused an up-regulation of interleukin-10, an anti-inflammatory cytokine in atopic children.

Wagner et.al. (1997) found that systemic Candida albicans was decreased in the immunodeficient rat model by Lactobacillus sp., and Bifidobacterium. Parvez et.al., (2006) cited clinical studies that showed probiotics and fermented foods demonstrating anti-hypertensive effects. Research into cancer and probiotics is lacking at the current time however Parvez et.al., (2006) states that “there are hypotheses out there that probiotic cultures might decrease the exposure to chemical carcinogens by: (i) detoxifying ingested carcinogens; (ii) altering the environment of the intestine and thereby decreasing populations or metabolic activities of bacteria that may generate carcinogenic compounds; (iii) producing metabolic products (e.g. butyrate) which improve a cells ability to die when it should die (a process known as apoptosis or programmed cell death); (iv) producing compounds that inhibit the growth of tumour cells; or (v) stimulating the immune system to better defend against cancer cell proliferation.”

Clinical trials have showed probiotics have helped with symptoms of diarrhoea, bloating, flatulence and abdominal pain in people with irritable bowel and functional bowel disorders (Parvez et.al., 2006). In vitro studies have shown that high lactic acid producing Lactobacillus salivarius can inhibit the growth of Helicobacter pylori. Nichols (2007) conducted a systematic review on probiotics and athletic performance. What was found was at the time of the review there were no studies that investigated the direct link between the two. There was however two studies that showed that in fatigued athletes probiotics enhanced the immune response. I suspect this is something that will be studied more the future.

One question that I have always had with probiotics is how well they survive in the human digestive tract. Yu et.al. (2013) conducted research on the specific culture Lactobacillus plantarum (commonly found in sauerkraut) for its viability against acid and bile acid, simulated human GI tract (gastric and pancreatic juices), susceptibility to antibiotics and antimicrobial activity. All the probiotics strains could tolerate acidity of pH 3.0, whereas at pH 2.0 the viability of the strains were strongly affected with a marked reduction. Viability against bile showed that all cultures survived well. The strains survived relatively well against gastric and pancreatic juices. The strains were resistant to antibiotic strains kanamycin, vancomycin, polymyxin B, streptomycin and gentamicin, but were sensitive to erythromycin, chloromycetin, penicillin and rifampicin. So in a nutshell there is good evidence to support that Lactobacillus plantarum can tolerate the simulated human digestive tract.

Fermented Foods & Cancer Research -

It is well established that estrogens have a lot to answer for as promoters and initiatory of breast cancer. Mutations of certain estrogen metabolites have been shown to be initiators of the carcinogenic process (Licznerska et.al., 2013). Aromatase is a cytochrome P450 encoded by CYP19. Aromatase synthesises estrogen by converting C19 androgens into aromatic C18 estrogenic steroids, and it has been shown that human breast cancer tissue has high expression of aromatase (Licznerska et. al., 2013). Thus aromatase inhibitors (AIs) have been studied as strategies for protective and treatment of breast cancer. A 72% reduction in breast cancer was found in a migrant epidemiological study when foods consumed in the Brassica genus which contain natural AIs as well as their fermented forms during adolescence was in high doses (Nelson, 2006).

Research into the effects of raw cabbage and sauerkraut juices and their potential anti-carcinogen effects were studied by Szaefer et.al. (2012). Cytochrome P450 enzymes (CYPs) are hemoproteins and are involved in the metabolising and detoxification of endogenous substrates, toxins and carcinogens (Szaefer et.al. 2012). CYPs and pathways have been a topic of study for the cancer chemoprotective strategies. Epidemiological studies have shown that in cultures where white cabbage and sauerkraut is a large part of their diet there is a lower risk of pancreatic, breast and prostate cancers (Larsson et. al. 2006). In their study Szaefer et al. (2012) specifically analysed CYP1A1/1A2, 1B1, and CYP2B enzymes and the effect of cabbage and sauerkraut juices on them. They found that sauerkraut juice was a more potent initiator of the CYPs than plain raw cabbage juice in rats. The authors suggested that sauerkraut fermentation may yield other products that have not yet been studied, which may explain why the fermented variety of cabbage is more potent initiator of CYPs (Szaefer et.al. 2012). It was concluded

the present study demonstrated that raw cabbage and sauerkraut juices could affect CYPs involved in the activation of +carcinogens/xenobiotics and in this way exert anticarcinogenic/chemopreventive activity.
(Szaefer et.al. 2012).

Let’s dig a little deeper to better understand why cabbage (part of the Brassica family of vegetables) has these effects on the CYPs. Brassica vegetables contain relatively high levels of glucosinolates (GLS). It has been shown that GLS themselves exert rather poor bioavailability, but under thermal degradation and enzymatic hydrolysis other more biological active compounds are formed such as indoles (e.g. indole-3-carbinol, I3C, diindolylmethane (DIM) and isothiocyanates (ITCs) (Szaefer et.al. 2012, Licznerska et. al., 2013). The shredding process actually transforms a specific GLS (glucobrassicin) into Indole-3-carbinol (I3C) via the action of myrosinase activity during fermentation, as the pH decreases, this indole reacts nonenzymatically with L-ascorbic acid to yield [ascorbigen] ABG (Szaefer et.al. 2012). Furthermore ABG is thought to induce antioxidant and detoxification genes via the activation of NF-E2-receptor related transcription factor 2 (Nrf2) and aryl-hydrocarbon receptor (AhR) (Szaefer et.al. 2012). It is also suggested that ABG is responsible for the down-regulation of the CYP19 expression in the MCF10A cell line, thus exerting anticarcinogenic activity (Licznerska et.al., 2013).

I3C and DIM are anti-estrogenic, anti-proliferative and proapoptotic via the stimulation of number of different cellular responses (Licznerska et.al., 2013). In Licznerska et. al., (2013) study they investigated the effects of raw cabbage and sauerkraut juices (from industrial and organic farmed sources) and their major components I3C and DIM on aromatase expression on 2 breast cancer cell lines as well as 1 non-tumorigenic breast cell line. Sauerkraut juice exerted the most potent effects on aromatase expression in the non-tumorigenic breast cells, whilst I3C and DIM were more efficient in decreasing the aromatase expression in the estrogen dependant MCF7 breast cancer cells. When the organic vs non-organic sauerkraut juices were analysed it was found that the organic was a more potent inhibitor of CYP19 expression on both mRNA and protein level in MCF10A (cancerous) cells (Licznerska et.al., 2013).

During the fermentation process of vegetables there is a breakdown of the cell walls promoting microbial hydrolysis reactions and increasing the phenolic compounds and flavonoids which gives rise to the increased antioxidant benefits (Hur et.al. 2014). Antioxidant activity by these compounds can then act as metal detoxification and free-radical terminators (reducing agents). Enzymes that exert antihypertensive effects have also been seen with fermented foods such as gamma-aminobutyric acid angiotensin converting enzyme inhibitory peptides (Hur et.al. 2014). Some of the microbial enzymes that are produced by fermentation and facilitate flavonoid production include; glucosidase, amylase, cellulase, inulinase, phytase, chitinase, xylanase, tannase, esterase, invertase and lipase (Hur et.al. 2014).See image below taken from (Hur et.al. 2014 for a summary of the formation of antioxidants from fermented foods.

Histamines & Fermentation

Monoamines are biogenic amines (BAs) and have been reported to be problematic to sensitive individual and when in large doses. The main monoamines responsible are histamine (HI), tyramine (TY) and tryptamine (TR). They are formed by the microbial decarboxylation of amino acids (Kalac et.al., 2000). Fermented foods are reported to naturally contain these BAs and have been reported to be poorly tolerated in individuals who are sensitive to them. Normally these BAs are metabolised in the intestinal tract efficiently by monoamine oxidase (MAO) and diamine oxidase (DAO), although is individual specific. I can’t go into the specifics as it requires a whole article on its own but HI and TY in particular are reported to cause a vast symptom set when either consumed in large doses or by sensitive individuals due to their psychoactive (affecting the neural transmitters) and vasoactive effects (vasoconstrictive in the case of TY and vasodilation with HI) (Kalac et.al., 2000). Before we can carry on further it’s important to mention the levels that are considered recommended maximum for BAs in foods; 50-100, 100-800, 30 or 100-200 mg kg-1 for HI, TY, 2-phenylethylamine or total, respectively (Kalac et.al., 1999). Specifically it has been reported that TY in doses of 10-80mg may cause swellings and headaches, doses above 100mg may cause migraines. Individuals on MAO inhibitors it is suggested that TY intake should not exceed 6mg in a 4hr period (Diel et.al., 1997; Kalac et.al., 1999).

Kalac et.al., (2000) looked at ways of potentially decreasing BAs through the use of lactic acid bacteria in sauerkraut fermentation. Four amines, HI, TR, SPD [spermadine] and SPM [spermine], were detected mostly in concentrations below 10 mg/kg and in some samples their levels were below detection limits. Thus, their biological effects on man may be considered as limited and they are not taken into further consideration. They further noted sauerkrauts inoculated with L.plantarum or Microsil had significantly (P<0.005) lower concentrations of TY, PUT [putrescine] and CAD [cadaverine] and similarly lower levels of acetic acid, ammonia and alpha-amino groups than other variants. Note the researchers used spontaneously wild fermented sauerkraut as their control. So in summary the above study seemed to show that HI, TR, SPD and SPM in fermented sauerkraut (fermented for 14 days @ 22oC then stored for 6months @ 5-6o C) were at insignificant levels and sometimes not even detected. This leads me to think two things

1) their fermentation time is a very long time (6 months) which is beyond what most people are doing thus may explain the low to no levels of the insulting amines whereas what people are doing at home with shorter ferment times may be producing a product with higher levels of the BAs.

2) Perhaps it’s not actually the HI and TR that is the offense BAs in fermented foods that cause some individuals to be sensitive, perhaps it’s some of the other BAs. In an earlier study conducted by the same authors Kalac et.al. (1999), they reviewed 121 different sauerkraut samples for BA levels. The specific details about the fermentation process wasn’t specified, the only information given was all samples did NOT contain starter cultures; 53 samples were non-pasteurised commercial, 10 samples were commercial and pasteurised, 29 were traditional house-hold prepared and the final 29 were prepared and then sterilised in jars. So let’s see what was found… For TY 5.8% of samples exceeded 500mg Kg-1 , 47.6% exceeded 200 mg Kg-1 , and only 9.9% of samples had levels below 20mg Kg-1. What was interesting was the house-hold prepared sauerkrauts had the lowest levels. The authors report that “surprisingly, histamine levels were usually lower than those reported in the literature”.

They found that 43.8% of samples tested were below the detection limit of 2.1mg Kg-1. Only 6.6% were above 20mg Kg-1. The other three amines SPD, TR and SPM were often below detection levels.

In another study by Kalac et.al.., (2000) they examined the effect of fermentation time on BA concentration in sauerkraut. They examined the kraut (which was fermented as above) at 2, 4,6 and 12 months. They found HI, TR and SP were below detection limits. They found TY was in high levels and its concentration increased with fermentation time. They concluded that

high tyramine levels seem to be the most problematic among the BAs in sauerkraut

In a more recent study by Penas et.al., (2010) they looked at the BA content in sauerkraut over a 3 month fermentation span. They analysed two different salt concentrations (0.5% and 1.5%) as well as 2 different starter cultures (L.plantarum and L.mesenteroides), fermentation was 7 days at room temperature (22-25oC) then stored at 4oC and samples taken at 0,1,2 and 3 months. They found that over the fermentation period the presence of BAs increased 2-3 fold when compared to plain raw cabbage. They found the batch fermented with L.mesenteroides had less BAs than the L.plantarum batch. The batches that were fermented with more salt (1.5%) yielded more BAs than the 0.5%. Specifically it was noted that the histamine levels ranged from 2.1-11.3mg/kg which is considered very low. The fermentation and storage conditions used in the present work led to lower histamine and tyramine levels in sauerkrauts than the upper limits recommended for fermented food products. They also concluded that fermentation with 0.5% Salt and use of L.mesenteroides as a starter culture as the ideal sauerkraut from a quality and safety perspective.

In another recent study by Rabie et.al., (2011), they looked at the effect of three direct lactobacilli strains as cultures on BA levels. They used a control which did not receive any salt or cultures. Their method was as follows: Incubation at 15oC for 10 days followed by storage at 5-6oC for a further 45 days. Worth mentioning they used screw cap lids, not airlock. They found in the control sauerkraut the total BA content almost doubled between days 10-45. The lowest BA content at the end of the 45 day period was found with the kraut cultured with L.curvatus. By day 45 they found that histamine and tyramine in the experimental groups had no detectable levels, whereas the control did contain these BAs. Their conclusion is that

specific lactic acid strains of the Lactobacillus genus can effectively prevent biogenic amines from building-up excessively, with an emphasis on histamine

The fact they used a non-airlock device for fermentation essentially means that they did not provide a totally anaerobic environment for the fermentation process this in my opinion somewhat makes this methodology less than ideal.

Taylor et. al. (1978) conducted research to determine the levels of histamine in 50 different samples of sauerkraut to ascertain if the levels were near that needed to cause food poisoning (100mg/100g of food product). They found that in the 50 samples they took the average amount was 5.06mg/100g with a range from 0.91mg/100g to 13mg/100g. Thus their conclusion was that histamine levels were well below the levels required to produce food poisoning.

Diel et.al. (1997) analysed the National Food Intolerance Databank (NFID) in Europe to see which foods ranked highest in BA concentrations. Of the foods they analysed they found that fresh fish, sausages, sauerkraut and wine had the lowest HI concentrations. Cheese had the highest levels of HI.

Organic (ORG) Vs Conventional (CONV) Beetroots & Beetroot Fermented Juice|

Kazimierczak et.al. (2014) conducted a very interesting study which has been accepted for publication but at the present time not released. They compared vitamin, mineral contents and anti-carcinogen properties with ORG vs CONV beetroots as well as fermented ORG beetroot juice and fermented CONV beetroot juice. They found that fermented ORG beetroot juice had statistically significant higher levels of vitamin C than CONV.

It was found that anticancer activity was stronger in the case of Organic fermented juices when compared with Conventional ones
Kazimierczak et.al. (2014).

The cancer cell line that they used in their research was AGS- Gastric Adenocarcinoma stomach cancer. Their method of fermenting was what I found interesting. All beetroots were thoroughly washed and cut into four wedges; next, two opposite wedges were used to prepare the fermented juice. Beetroot samples were shredded with a food processor Coupe 30 CL. Water, with added salt (3%) and garlic, was then poured over the shredded beetroot, which was then incubated at a temperature of between 20-23 degrees C to obtain pH 3.80. The fermentation process was controlled by measuring and maintaining the pH level. After two weeks the fermented juices were filtered into jars, and pasteurized for 15 min at 80 Degrees C. Next, the juices were analysed for chemical composition and anticancer activity. The fact that these were pasteurised surprises me and sounds counterintuitive to the point of fermentation. The fact that there were still these anti-carcinogenic properties post pasteurisation is interesting to me and I’d love to see what the results would look like if the fermented beverage was not pasteurised and fully raw with all nutrients left intact.

References:

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