What is kimchi

Kimchi is a traditional fermented vegetable, a staple in Korean cuisine and is an indispensable side dish of every meal in Korea ¹⁾. Moreover, the annual tradition Gimjang involves preparing and storing a large quantity of kimchi for the winter season ²⁾. There are about 187 kinds of Kimchi according to the ingredients and processing methods ³⁾. Kimchi is prepared by various ingredients, such as Chinese cabbage (Brassica pekinensis Rupr.), processed with seasoning mixture mainly consisting of red pepper (Capsicum annuum L.) powder, garlic, ginger, edible Allium varieties other than garlic, and radish in the presence of salt. These ingredients may be chopped, sliced and broken into pieces ⁴⁾. Kimchi is then fermented in brine before or after being packaged into appropriate containers to ensure the proper ripening and preservation of the product by lactic acid production at low temperatures. The drained weight of the final product, as a percentage of the indicated weight, should be not less than 80% by weight, calculated on the basis of the weight of distilled water at 20 °C which the sealed container will hold when completely filled. The drained weight of the final product as a percentage by the indicated weight shall not be less than 80% by weight. Kimchi is currently recognized worldwide as a nutritious and healthy food ⁵⁾.

Traditional kimchi that is fermented naturally at low temperatures without any starter is a complex system, with dynamic biological and biochemical changes during fermentation ⁶⁾. Because kimchi fermentation is accomplished by a succession of naturally occurring different lactic acid bacteria, fermentative metabolic features of microbial communities during kimchi fermentation process are different every time, which makes it difficult to consistently produce standardized kimchi with high quality ⁷⁾. Until now, rational and systematic approaches to control kimchi fermentation for the production of kimchi with uniform quality have not been developed because the understanding of kimchi microbial communities during fermentation has not yet been accomplished ⁸⁾. Therefore, comprehensive investigation on the fermentative metabolic features of kimchi lactic acid bacteria during fermentation is indispensable to control kimchi fermentation ⁹⁾. With metatranscriptomic analysis, it is relatively easy to investigate the metabolic features of microbial communities in fermented foods such as kimchi, because these communities are not so complex as those in other natural environments. Therefore, a transcriptomic analysis was performed to examine the metabolic features of Leuconostoc mesenteroides during kimchi fermentation. Relative abundances (%) of mRNA sequencing reads mapped to the genomes of Leuconostoc mesenteroides strains for total lactic acid bacteria mRNA sequencing reads during the kimchi fermentation were calculated. The relative abundances were high at the early kimchi fermentation period and decreased to the lowest value at 18 days as the fermentation progressed, suggesting that members of Leuconostoc mesenteroides are more responsible for kimchi fermentation during the early fermentation period. The metabolic properties of Leuconostoc mesenteroides during kimchi fermentation were investigated by metabolic mapping of the Leuconostoc mesenteroides mRNA sequencing. The transcriptomic analysis showed that genes associated with carbohydrate metabolisms, nucleotide metabolism, fatty acid biosynthesis, oxidative phosphorylation, riboflavin metabolism, and glutamine and glutamate metabolism were highly expressed during kimchi fermentation ¹⁰⁾. Genes associated with fatty acid biosynthesis, nucleotide metabolism, and amino acid metabolism, probably more related to cell growth, were up-regulated in Leuconostoc mesenteroides during the early kimchi fermentation period, which may explain why Leuconostoc mesenteroides is more abundant at that stage. Conversely, genes associated with oxidative phosphorylation, biosynthesis of other secondary metabolisms, and glutamine and glutamate metabolism were up-regulated during the late kimchi fermentation period ¹¹⁾. Genes associated with the biosynthesis of riboflavin were highly expressed during the entire kimchi fermentation, suggesting that Leuconostoc mesenteroides may be an important producer of riboflavin during the kimchi fermentation ¹²⁾.

Leuconostoc mesenteroides (Leu. mesenteroides) comprises Gram-positive, catalase-negative, facultatively anaerobic, non-spore-forming, and spherical heterofermentative and mostly dextran-producing lactic acid bacteria (LAB), with coccus shapes and relatively low G + C contents ¹³⁾. Leuconostoc mesenteroides members are reported to be mainly responsible for the fermentation of various vegetables, such as kimchi and sauerkraut (pickled cabbage), under low temperature and moderate salinity conditions, although some Leuconostoc mesenteroides strains have been isolated from dairy products such as cheese ¹⁴⁾. In particular, Leuconostoc mesenteroides strains were found to be the major lactic acid bacteria, along with Lactobacillus sakei and Weissella koreensis, present during kimchi fermentation, suggesting that they are well adapted to kimchi fermentation conditions ¹⁵⁾. Moreover, because Leuconostoc mesenteroides strains produce mannitol, a compound with antidiabetic and anticarcinogenic properties known for imparting a refreshing taste, and bacteriocins during fermentation and have some health improving effects ¹⁶⁾, they have been considered as starter cultures for kimchi fermentation or potential probiotics in industries ¹⁷⁾.

Although Leuconostoc mesenteroides strains are generally considered to be non-infectious agents in humans, there have been some clinical reports that Leuconostoc mesenteroides might be associated with certain human diseases such as brain abscess, endocarditis, nosocomial outbreaks, and central nervous system tuberculosis ¹⁸⁾. In addition, there is a report that Leuconostoc mesenteroides can cause spoilage in some types of food products ¹⁹⁾. These reports suggest that further studies on the physiological and fermentative properties of Leuconostoc mesenteroides strains are needed to vouch for the safety and quality of kimchi and sauerkraut products fermented with Leuconostoc mesenteroides ²⁰⁾.

Figure 1. Kimchi

Kimchi nutrition

Nutritionally, Kimchi is a low-calorie food (15 kcal/100 g) and an important source of vitamins, minerals, and fiber ²¹⁾. It is also a good source of phytochemicals (e.g., β-sitosterol, glucosinolates, isothiocyanate, indoles, allyl compounds) and probiotic strains (e.g., Lactobacillus plantarum, Lactobacillus brevis, Leuconostoc mesenteroides) ²²⁾. In regard to these nutrition properties, many functional properties of Kimchi have been reported including anti-oxidative activity ²³⁾, anti-mutagenic and anti-tumor activities ²⁴⁾, anti-atherogenic activity ²⁵⁾ and weight-controlling activity ²⁶⁾.

Table 1. Kimchi nutrition facts

Nutrient	Unit	Value per 100 g
Approximates
Water	g	94.3
Energy	kcal	15
Energy	kJ	65
Protein	g	1.1
Total lipid (fat)	g	0.5
Ash	g	1.7
Carbohydrate, by difference	g	2.4
Fiber, total dietary	g	1.6
Sugars, total	g	1.06
Minerals
Calcium, Ca	mg	33
Iron, Fe	mg	2.5
Magnesium, Mg	mg	14
Phosphorus, P	mg	24
Potassium, K	mg	151
Sodium, Na	mg	498
Zinc, Zn	mg	0.22
Copper, Cu	mg	0.024
Selenium, Se	µg	0.5
Vitamins
Vitamin C, total ascorbic acid	mg	0
Thiamin	mg	0.01
Riboflavin	mg	0.21
Niacin	mg	1.1
Vitamin B-6	mg	0.213
Folate, total	µg	52
Folic acid	µg	0
Folate, food	µg	52
Folate, DFE	µg	52
Choline, total	mg	15.5
Vitamin B-12	µg	0
Vitamin B-12, added	µg	0
Vitamin A, RAE	µg	5
Retinol	µg	0
Carotene, beta	µg	55
Carotene, alpha	µg	1
Cryptoxanthin, beta	µg	0
Vitamin A, IU	IU	93
Lycopene	µg	0
Lutein + zeaxanthin	µg	49
Vitamin E (alpha-tocopherol)	mg	0.11
Vitamin E, added	mg	0
Vitamin D (D2 + D3)	µg	0
Vitamin D	IU	0
Vitamin K (phylloquinone)	µg	43.6
Lipids
Fatty acids, total saturated	g	0.067
04:00:00	g	0
06:00:00	g	0
08:00:00	g	0
10:00:00	g	0
12:00:00	g	0.003
14:00:00	g	0.003
16:00:00	g	0.057
18:00:00	g	0.003
Fatty acids, total monounsaturated	g	0.037
16:1 undifferentiated	g	0
18:1 undifferentiated	g	0.037
20:01:00	g	0
22:1 undifferentiated	g	0
Fatty acids, total polyunsaturated	g	0.241
18:2 undifferentiated	g	0.104
18:3 undifferentiated	g	0.137
18:04:00	g	0
20:4 undifferentiated	g	0
20:5 n-3 (EPA)	g	0
22:5 n-3 (DPA)	g	0
22:6 n-3 (DHA)	g	0
Cholesterol	mg	0
Other
Alcohol, ethyl	g	0
Caffeine	mg	0
Theobromine	mg	0

[Source: United States Department of Agriculture Agricultural Research Service ²⁷⁾]

Kimchi health benefits

In Korea, where the aging of population is rapidly increasing and westernized lifestyle is becoming more prevalent, cardiovascular disease and metabolic syndrome–related diseases such as type two diabetes mellitus are becoming important public health issues. In fact, during the last two decades, crude mortality from ischemic heart disease dramatically increased for men (10.3-fold increase), and women (17.5-fold increase), and diabetes-related mortality was also increased four times for men and six times for women ²⁸⁾. These tendencies are shown throughout the world. Therefore, many trials to prevent or decrease the prevalence of these degenerative diseases have been performed with modification of environmental factors such as dietary patterns and screening for biologically effective compounds from foods.

Many studies have reported the beneficial effects of kimchi, including its anti-oxidative activity ²⁹⁾, ³⁰⁾, anti-obesity ³¹⁾, anti-asthma ³²⁾, anti-aging effects ³³⁾, anti-cancer and antimutagenic activities ³⁴⁾, ³⁵⁾, anti-atherosclerotic ³⁶⁾ and cholesterol- lowering effects ³⁷⁾ and antimicrobial activity ³⁸⁾, immune stimulatory activity ³⁹⁾, weight reduction and lipid lowering effects ⁴⁰⁾ and anti-atherogenic activity ⁴¹⁾.

Numerous studies have reported on the lipid-lowering mechanisms of kimchi or its ingredients such as Chinese cabbage, hot red pepper, garlic, green leek, and ginger ⁴²⁾. β-sitosterol in Chinese cabbage, S-methlycysteinsulfoxide and S-allylcysteinsulfoxide in garlic, capsaicin in red pepper are known bioactive compounds present in kimchi ingredients responsible for lowering blood lipids ⁴³⁾. β-Sitosterol, a phyto-cholesterol, competes with dietary cholesterol in the intestine for absorption ⁴⁴⁾. Sulfur compounds in onion and garlic stimulate lipolysis by elevating the hormone secretion such as adrenalin and glucagon, or suppressing enzyme activities responsible for cholesterol synthesis. Acetyl-CoA synthetase and/or 3-hydroxy-3-methyl-glutaryl CoA reductase activity was inhibited by allin or allicine ⁴⁵⁾. Capsaicin stimulates the secretion of plasma cholesterol to extra-circulation as bile via elevating 7α-hydroxylase activity ⁴⁶⁾. It also increases energy expenditure by regulating thyroid hormone secretion ⁴⁷⁾. Additionally, lactic acid bacteria produced during the fermentation of kimchi are believed to contribute to the cholesterol lowering activity. Lactobacillus acidophilus usually detected in kimchi can bind the cholesterol in their cell wall besides decomposing the cholesterol for assimilation and de-conjugates the bile acids ⁴⁸⁾. In previous study, kimchi effectively attenuated plasma cholesterol levels in rats and rabbits fed high cholesterol diets ⁴⁹⁾. In addition, hypercholesterolemic rabbits administered bioactive compound of kimchi, 3-(4′-hydroxyl-3′,5′-dimethoxyphenyl)propionic acid (HDMPPA) showed a drop in plasma cholesterol and LDL “bad” cholesterol within 4 days of treatment ⁵⁰⁾. These results supported the findings that kimchi supplementation to young adults for a short period could alleviate serum cholesterol concentration ⁵¹⁾. In another study ⁵²⁾, kimchi consumption significantly lowered the fasting blood glucose concentration according to amount of kimchi intake. There are several considerations about the lowering effect of kimchi on fasting blood glucose. Compared with energy and carbohydrate intake between pre- and post-test, these two factors showed no difference in the two groups. Furthermore, in a previous questionnaire for physical activity, 36% and 27% subjects in the low and high group answered “no extra exercise”, respectively. These data suggested that a relatively greater reduction of fasting blood glucose or plasma lipids in the high group could be related with intake of kimchi ⁵³⁾.

Focusing on the effect of fermentation, this study ⁵⁴⁾ hypothesized that consumption of fermented kimchi would have more beneficial effects compared with that of fresh kimchi on metabolic parameters that are related to cardiovascular disease and metabolic syndrome risks in overweight and obese subjects. Twenty-two overweight and obese patients with body mass indexes greater than 25 kg/m² were randomly assigned to two 4-week diet phases separated by a 2-week washout period (crossover design). During each diet phase, the subjects consumed either fresh or fermented kimchi. Anthropometric data showed significant decreases in body weight, body mass index, and body fat in both groups, and the fermented kimchi group showed a significant decrease in the waist-hip ratio and fasting blood glucose. Net differences in the systolic blood pressure, diastolic blood pressure, percent body fat, fasting glucose, and total cholesterol in the fermented kimchi group were significantly greater than those in the fresh kimchi group. There was also a tendency for a decrease in fasting insulin after consumption of fermented kimchi. Therefore, the ingestion of fermented kimchi had positive effects on various factors associated with metabolic syndrome, including systolic and diastolic blood pressures, percent body fat, fasting glucose, and total cholesterol, compared with the fresh kimchi. These results suggest that the maturity of kimchi (fresh vs fermented) may affect obesity, lipid metabolism, and inflammatory processes ⁵⁵⁾.

Chinese cabbage, a main ingredient of Kimchi, is rich in minerals, vitamin C, dietary fibers, and especially phytochemicals ⁵⁶⁾. Also, cabbage contains several organic sulfur compounds, such as isothiocyanates and dithiolethiones. In a previous study ⁵⁷⁾, these organic sulfur compounds were shown to exert diverse biological effects including the inhibition of tumor cell proliferation, antimicrobial effects, and free radical scavenging. Another ingredient, garlic, contains various sulfur-contained compounds; S-allyl-l-cysteine, S-allyl-l-cysteine sulfoxides and alliin ⁵⁸⁾. It suppress the production of inflammatory cytokines, such as TNF-a, IL-1, IL-6, and interferon-γ ⁵⁹⁾. Red pepper contains high levels (25-80 mg%) of capsaicin. Capsaicin (8-methyl-N-vanillyl-6-nonenamide) is involved in physiological functions related to immune response ⁶⁰⁾.

In a previous study, 3-(4′-hydroxyl-3′,5′-dimethoxyphenyl)propionic acid (HDMPPA), an active principle in cabbage kimchi ⁶¹⁾, demonstrated anti-atherogenic activity in terms of preventing the fatty streak formation or atherosclerosis in rabbits ⁶²⁾. Among the possible mechanisms, it was suggested that HDMPPA suppressed transcription rate for the enzymes responsible for the production of reactive oxygen species and also inhibited adhesion molecule expression whereas endothelial nitric oxide synthase activity in the aorta was elevated ⁶³⁾. In a human study, kimchi consumption exerted favorable plasma lipid lowering effects and improved metabolic syndrome parameters in obese people ⁶⁴⁾.

Probiotics are living micro-organisms that have a health benefit for their host. Orally ingested probiotic bacteria are able to modulate the immune system; however, differences exist in the immunomodulatory effects of different probiotic strains ⁶⁵⁾. Especially, lactic acid bacteria produced during the fermentation process from Kimchi : Leuconostoc mesenteroides, Leuconostoc citreum, Leuconostoc gasicomitatum, Leuconostoc kimchii, Leuconostoc inhae, Weissella Koreensis, Weissella cibaria, Lactobacillus plantarum, Lactobacillus sakei, Lactobacillus delbrueckii, Lactobacillus buchneri, Lactobacillus brevis, Lactobacillus fermentum, Pediococcus acidilactici and Pediococcus Pentosaceus ⁶⁶⁾.

According to the Lee et al. ⁶⁷⁾, suppressor T lymphocyte cells and Natural killer cells are increased with Lactobacillus casei and Bifidobacterium longumi treatment. However, another study ⁶⁸⁾, T-helper cells and suppressor T cells were not affected by the consumption of Kimchi. T lymphocyte cells play central roles in the immune system, in which their major function assisting B lymphocyte cells in the production of antibodies. Serum Ig (immunoglobulin) levels are routinely measured in clinical practice to examine immune balance. Typical ranges are suggested (Ig A; 1.4-0.4 mg/mL, Ig G; 8-16 mg/mL, and Ig M; 0.5-2.0 ng/mL). Low levels of Ig were observed in humoral immunodeficiency, while high levels of Ig were observed in chronic inflammatory diseases. Until now, many studies showed that Kimchi inhibited Ig E levels in the NC/nga mice atopic animal model [24,25]. Also, lactobacillus plantarum isolated from Kimchi increased the production of Ig A in normal or S180-bearing BALB/C tumor-induced mouse ⁶⁹⁾. On the other hand, 4 weeks of Kimchi supplementation does not changes of Ig A, Ig G or Ig M ⁷⁰⁾.

Gut microbiota dysbiosis plays a key role in the pathogenesis of inflammatory bowel disease (IBD). Much research has focused on the use of gut microbiota for the treatment of inflammatory bowel disease (IBD). Probiotics, live microorganisms that benefit host health, are commonly used to control chronic gastrointestinal inflammation in inflammatory bowel disease (IBD) patients. Lactobacillus and Bifidobacterium species are widely used as probiotics ⁷¹⁾. Administration of Lactobacillus plantarum ameliorates the severity of colitis in IL-10-knockout mice ⁷²⁾. Lactobacillus paracasei isolated from kimchi, reduces colitis disease by decreasing the number of Th1 (IFN-γ or Interferon gamma) cells and macrophages in the lamina propria ⁷³⁾. Treatment with Lactobacillus acidophilus reduces the STAT3 and phosphorylated STAT3 levels in colon tissue from mice with Dextran sulfate sodium (DSS)-induced colitis and increases the number of Treg cells among intestinal intraepithelial and lamina propria lymphocytes in a 2,4,6-trinitrobenzene sulfonic acid-induced colitis model ⁷⁴⁾. Treatment with Bifidobacterium longum ameliorates colorectal colitis in rats by altering the methylation level of the Foxp3 promoter, resulting in an increased number of Treg cells ⁷⁵⁾. Moreover, Streptococcus thermophilus suppresses bacterial translocation, which reduces gastrointestinal bleeding and weight loss ⁷⁶⁾. Treatment with lactobacilli and bifidobacteria promoted recovery of Dextran sulfate sodium (DSS)-induced intestinal injury and inflammation in a mouse model of colitis ⁷⁷⁾. Lactobacillus casei and Bifidobacterium lactis ameliorated injury to the intestinal mucosa and liver in a 2,4,6-trinitrobenzene sulfonic acid-induced colitis model ⁷⁸⁾. Also, treatment with a probiotic combination that included lactobacilli, bifidobacteria, and streptococci reduced the levels of proinflammatory cytokines in colitis ⁷⁹⁾.

Cytokines, protein mediators produced by immune cells, are involved in immune regulation. The levels of pro-inflammatory cytokines are increased in chronic inflammatory diseases while the levels of anti-inflammatory cytokines are decreased. Kim et al. ⁸⁰⁾ showed that the consumption of fermented Kimchi (300 g/day for 4 weeks) had no effects on the levels of Tumor Necrosis Factor-α (TNF-α) and Interleukin 6 (IL-6) in overweight and obese patients (22 subjects, mean age of 38.6 ± 8.5 years). In another study ⁸¹⁾, the levels of TNF-α and IL-6 were significantly decreased in the Kimchi and non-Kimchi groups. It is unclear why the levels of pro-inflammatory cytokines in the non-Kimchi group were decreased. The study author ⁸²⁾ postulated the decreased levels of TNF-α and IL-6 in placebo group may be due to the use of radish. Because of these conflicting results more research are needed before any opinion can be formed regarding the effects of kimchi on the immune system (e.g., immune stimulating activity).