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 ⁶. 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 ⁶. Therefore, comprehensive investigation on the fermentative metabolic features of kimchi lactic acid bacteria during fermentation is indispensable to control kimchi fermentation ⁷. 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 ⁶. 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 ⁶. 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 ⁶.

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 ⁸. 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 ⁸. 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 ⁷. 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 ⁹, they have been considered as starter cultures for kimchi fermentation or potential probiotics in industries ¹⁰.

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 ¹¹. In addition, there is a report that Leuconostoc mesenteroides can cause spoilage in some types of food products ¹². 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 ⁶.

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 ¹³. 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) ¹⁴. In regard to these nutrition properties, many functional properties of Kimchi have been reported including anti-oxidative activity ¹⁵, anti-mutagenic and anti-tumor activities ¹⁶, anti-atherogenic activity ¹⁷ and weight-controlling activity ¹⁸.

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 ¹⁹]

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 ²⁰. 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 ²¹, ²², anti-obesity ²³, anti-asthma ²⁴, anti-aging effects ²⁵, anti-cancer and antimutagenic activities ²⁶, ²⁷, anti-atherosclerotic ²⁸ and cholesterol- lowering effects ²⁹ and antimicrobial activity ³⁰, immune stimulatory activity ³¹, weight reduction and lipid lowering effects ³² and anti-atherogenic activity ³³.

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 ²⁰. 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 ³⁴. β-Sitosterol, a phyto-cholesterol, competes with dietary cholesterol in the intestine for absorption ³⁵. 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 ³⁴. Capsaicin stimulates the secretion of plasma cholesterol to extra-circulation as bile via elevating 7α-hydroxylase activity ³⁶. It also increases energy expenditure by regulating thyroid hormone secretion ³⁷. 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 ³⁸. In previous study, kimchi effectively attenuated plasma cholesterol levels in rats and rabbits fed high cholesterol diets ³⁹. 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 ⁴⁰. These results supported the findings that kimchi supplementation to young adults for a short period could alleviate serum cholesterol concentration ⁴¹. In another study ⁴¹, 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 ⁴¹.

Focusing on the effect of fermentation, this study ⁴² 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 ⁴².

Chinese cabbage, a main ingredient of Kimchi, is rich in minerals, vitamin C, dietary fibers, and especially phytochemicals ⁴³. Also, cabbage contains several organic sulfur compounds, such as isothiocyanates and dithiolethiones. In a previous study ⁴⁴, 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 ⁴⁵. It suppress the production of inflammatory cytokines, such as TNF-a, IL-1, IL-6, and interferon-γ ⁴⁶. 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 ⁴⁷.

In a previous study, 3-(4′-hydroxyl-3′,5′-dimethoxyphenyl)propionic acid (HDMPPA), an active principle in cabbage kimchi ⁴⁸, demonstrated anti-atherogenic activity in terms of preventing the fatty streak formation or atherosclerosis in rabbits ⁴⁹. 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 ⁵⁰. In a human study, kimchi consumption exerted favorable plasma lipid lowering effects and improved metabolic syndrome parameters in obese people ⁵¹.

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 ⁵². 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 ⁵³.

According to the Lee et al. ⁵⁴, suppressor T lymphocyte cells and Natural killer cells are increased with Lactobacillus casei and Bifidobacterium longumi treatment. However, another study ⁵⁵, 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 ⁵⁶. On the other hand, 4 weeks of Kimchi supplementation does not changes of Ig A, Ig G or Ig M ⁵⁵.

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 ⁵⁷. Administration of Lactobacillus plantarum ameliorates the severity of colitis in IL-10-knockout mice ⁵⁸. 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 ⁵⁹. 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 ⁶⁰. 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 ⁶¹. Moreover, Streptococcus thermophilus suppresses bacterial translocation, which reduces gastrointestinal bleeding and weight loss ⁶². Treatment with lactobacilli and bifidobacteria promoted recovery of Dextran sulfate sodium (DSS)-induced intestinal injury and inflammation in a mouse model of colitis ⁶³. Lactobacillus casei and Bifidobacterium lactis ameliorated injury to the intestinal mucosa and liver in a 2,4,6-trinitrobenzene sulfonic acid-induced colitis model ⁶⁴. Also, treatment with a probiotic combination that included lactobacilli, bifidobacteria, and streptococci reduced the levels of proinflammatory cytokines in colitis ⁶⁵.

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. ¹⁸ 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 ⁵⁵, 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 ⁵⁵ 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).

References

1. Chang JY, Chang HC. Growth inhibition of foodborne pathogens by Kimchi prepared with bacteriocin-producing starter culture. J Food Sci. 2011;76:M72–M78 https://www.ncbi.nlm.nih.gov/pubmed/21535696
2. Hwang HS, Han BR, Han BJ, Chung L. Korean Traditional Local Food Written by Three Generation. Paju: Kyomun Publishing Co.; 2010. pp. 1–300.
3. Cheigh HS, Park KY. Biochemical, microbiological, and nutritional aspects of Kimchi (Korean fermented vegetable products) Crit Rev Food Sci Nutr. 1994;34:175–203 https://www.ncbi.nlm.nih.gov/pubmed/8011144
4. Lee GI, Lee HM, Lee CH. Food safety issues in industrialization of traditional Korean foods. Food Control. 2012;24:1–5.
5. Lee H, Kim DY, Lee MA, Jang J-Y, Choue R. Immunomodulatory Effects of Kimchi in Chinese Healthy College Students: A Randomized Controlled Trial. Clinical Nutrition Research. 2014;3(2):98-105. doi:10.7762/cnr.2014.3.2.98. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4135247/
6. Pan-genomic and transcriptomic analyses of Leuconostoc mesenteroides provide insights into its genomic and metabolic features and roles in kimchi fermentation. Scientific Reports 2017, volume 7, Article number: 11504. https://www.nature.com/articles/s41598-017-12016-z
7. Jung, J. Y., Lee, S. H. & Jeon, C. O. Kimchi microflora: history, current status, and perspectives for industrial kimchi production. Appl Microbiol Biotechnol 2014; 98, 2385–2393
8. Jeon, H. H. et al. A proposal of Leuconostoc mesenteroides subsp. jonggajibkimchii subsp. nov. and reclassification of Leuconostoc mesenteroides subsp. suionicum (Gu et al., 2012) as Leuconostoc suionicum sp. nov. based on complete genome sequences. Int J Syst Evol Microbiol in press doi: https://doi.org/10.1099/ijsem.0.001930
9. Beganović, J. et al. Improved sauerkraut production with probiotic strain Lactobacillus plantarum L4 and Leuconostoc mesenteroides LMG 7954. J Food Sci 2011; 76, M124–M129
10. Yi, Y.-J. et al. Potential use of lactic acid bacteria Leuconostoc mesenteroides as a probiotic for the removal of Pb (II) toxicity. J Microbiol 2017; 55, 296–303
11. Barletta, J. et al. Meningitis due to Leuconostoc mesenteroides associated with central nervous system tuberculosis: a case report. Ann Clin Case Rep 2017; 2, 1228
12. de Paula, A. T., Jeronymo-Ceneviva, A. B., Todorov, S. D. & Penna, A. L. B. The two faces of Leuconostoc mesenteroides in food systems. Food Rev Int 2015; 31, 147–171
13. Choi IH, Noh JS, Han JS, Kim HJ, Han ES, Song YO. Kimchi, a fermented vegetable, improves serum lipid profiles in healthy young adults: randomized clinical trial. J Med Food. 2013;16:223–229. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3598433/
14. Park KY, Kil JH, Jung KO, Kong CS, Lee LM. Functional properties of Kimchi (Korean fermented vegetables) Acta Hortic. 2006;706:167–172.
15. Lee YM, Kwon MJ, Kim JK, Suh HS, Choi JS, Song YO. Isolation and identification of active principle in Chinese cabbage Kimchi responsible for antioxidant effect. Korean J Food Sci Technol. 2004;36:129–133.
16. Cho EJ, Rhee SH, Lee SM, Park KY. In vitro antimutagenic and anticancer effects of Kimchi fractions. J Korean Assoc Cancer Prev. 1997;2:113–121.
17. Kwon MJ, Chun JH, Song YS, Song YO. Daily Kimchi consumption and its hypolipidemic effect in middle-aged men. J Korean Soc Food Sci Nutr. 1999;28:1144–1150.
18. Kim EK, An SY, Lee MS, Kim TH, Lee HK, Hwang WS, Choe SJ, Kim TY, Han SJ, Kim HJ, Kim DJ, Lee KW. Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutr Res. 2011;31:436–443. https://www.ncbi.nlm.nih.gov/pubmed/21745625
19. United States Department of Agriculture Agricultural Research Service. National Nutrient Database for Standard Reference Legacy Release. https://ndb.nal.usda.gov/ndb/search/list
20. Choi IH, Noh JS, Han J-S, Kim HJ, Han E-S, Song YO. Kimchi, a Fermented Vegetable, Improves Serum Lipid Profiles in Healthy Young Adults: Randomized Clinical Trial. Journal of Medicinal Food. 2013;16(3):223-229. doi:10.1089/jmf.2012.2563. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3598433/
21. Lee YM, Kwon MJ, Kim JK, Suh HS, Choi JS, Song YO: Isolation and identification of active principle in Chinese cabbage kimchi responsible for antioxidant effect. Korean J Food Sci Technol 2004;36:129–133
22. Kim JH, Ryu JD, Lee HG, et al. The effect of kimchi on production of free radicals and anti-oxidative enzyme activities in the brain of SAM. J Korean Soc Food Sci Nutr. 2002;31:117–123.
23. Park JA, Tirupathi Pichiah PB, Yu JJ, Oh SH, Daily JW, 3rd, Cha YS. Anti-obesity effect of kimchi fermented with Weissella koreensis OK1-6 as starter in high-fat diet-induced obese C57BL/6J mice. J Appl Microbiol. 2012;113:1507–1516 https://www.ncbi.nlm.nih.gov/pubmed/22978326
24. Kim H, Oh SY, Kang MH, Kim KN, Kim Y, Chang N. Association between kimchi intake and asthma in Korean adults: the fourth and fifth Korea National Health and Nutrition Examination Survey (2007-2011) J Med Food. 2014;17:172–178 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3901325/
25. Kim JH, Ryu JD, Lee HG, Park JH: The effect of kimchi on production of free radicals and anti-oxidative enzyme activities in the brain of SAM. J Korean Soc Food Sci Nutr 2002;31:117–123
26. Park KY: The nutritional evaluation and anti-mutagenic and anticancer effects of kimchi. J Korean Soc Food Sci Nutr 1995;24:169–182
27. Wang Y, Li F, Wang Z, Qiu T, Shen Y, Wang M. Fruit and vegetable consumption and risk of lung cancer: a dose-response meta-analysis of prospective cohort studies. Lung Cancer. 2015;88:124–130. https://www.ncbi.nlm.nih.gov/pubmed/25747805
28. Park KY, Jeong JK, Lee YE, Daily JW., 3rd Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. J Med Food. 2014;17:6–20. https://www.ncbi.nlm.nih.gov/pubmed/24456350
29. Choi EA, Chang HC. Cholesterol-lowering effects of a putative probiotic strain Lactobacillus plantarum EM isolated from kimchi. LWT – Food Sci Technol (Campinas) 2015;62:210–217.
30. Sheo HJ, Seo YS: The antibacterial action of Chinese cabbage kimchi juice on Staphylococcus aureus, Salmonella enteritidis, Vibrio parahaemolyticus and Enterobacter cloacae. J Korean Soc Food Sci Nutr 2003;32:1351–1356
31. Kim MJ, Kwon MJ, Song YO, Lee EK, Youn HJ, Song YS: The effects of kimchi on hematological and immunological parameters in vivo and in vitro. J Korean Soc Food Sci Nutr 1997;26:1–7
32. Kwon JY, Cheigh HS, Song YO: Weight reduction and lipid lowering effects of kimchi lactic acid powder in rats fed high fat diets. Korean J Food Sci Technol 2004;36:1014–1019
33. Noh JS, Kim HJ, Kwon MJ, Song YO: Active principle of kimchi, 3-(40-hydroxyl-3050-dimethoxyphenyl)propionic acid, retards fatty streak formation at aortic sinus of apolipoprotein E knockout mice. J Med Food 2009;12:1206–1212 https://www.ncbi.nlm.nih.gov/pubmed/20041773
34. Sheela CG. Augusti KT. Effects of S-allyl cysteine sulfoxide isolated from Allium sativm Linn and gugulipid on some enzymes and fecal excretions of bile and acids and sterols in cholesterol fed rats. Indian J Exp Biol. 1995;33:749–751 https://www.ncbi.nlm.nih.gov/pubmed/8575806
35. Miettinen TA. Vanhanen H. Dietary sitosterol related to absorption, synthesis and serum level of cholesterol in different apolipoprotein E phenotypes. Atherosclerosis. 1994;105:217–226 https://www.ncbi.nlm.nih.gov/pubmed/8003098
36. Kawada T. Hagihara K. Iwai K. Effects of capsaicin on lipid metabolism in rats fed a high fat diet. J Nutr. 1986;116:1272–1278. https://www.ncbi.nlm.nih.gov/pubmed/2875141
37. Yoshioka M. St-Pierre S. Suzuki M. Tremblay A. Effects of red pepper added to high-fat and high-carbohydrate meals on energy metabolism and substrate utilization in Japanese women. Br J Nutr. 1998;80:503–510. https://www.ncbi.nlm.nih.gov/pubmed/10211048
38. Gilliland SE. Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol Rev. 1990;7:175–188. https://www.ncbi.nlm.nih.gov/pubmed/2271223
39. Kwon MJ. Song YO. Song YS. Effects of kimchi on tissue and fecal lipid composition and apolipoprotein and thyroxine levels in rats. J Korean Soc Food Sci Nutr. 1997;26:507–513.
40. Kim HJ. Kwon MJ. Seo JM, et al. The effect of 3-(4′-hydroxyl-3′5′-dimethoxyphenyl)propionic acid in Chinese cabbage kimchi on lowering hypercholesterolemia. J Korean Soc Food Sci Nutr. 2004;33:52–58.
41. Choi IH, Noh JS, Han J-S, Kim HJ, Han E-S, Song YO. Kimchi, a Fermented Vegetable, Improves Serum Lipid Profiles in Healthy Young Adults: Randomized Clinical Trial. Journal of Medicinal Food. 2013;16(3):223-229. doi:10.1089/jmf.2012.2563.
42. Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutrition Research Volume 31, Issue 6, June 2011, Pages 436-443. https://www.sciencedirect.com/science/article/pii/S027153171100114X
43. Chu YF, Sun J, Wu X, Liu RH. Antioxidant and antiproliferative activities of common vegetables. J Agric Food Chem. 2002;50:6910–6916 https://www.ncbi.nlm.nih.gov/pubmed/12405796
44. Moriarty RM, Naithani R, Surve B. Organosulfur compounds in cancer chemoprevention. Mini Rev Med Chem. 2007;7:827–838. https://www.ncbi.nlm.nih.gov/pubmed/17692044
45. Amagase H, Petesch BL, Matsuura H, Kasuga S, Itakura Y. Intake of garlic and its bioactive components. J Nutr. 2001;131:955S–962S. https://www.ncbi.nlm.nih.gov/pubmed/11238796
46. Salman H, Bergman M, Bessler H, Punsky I, Djaldetti M. Effect of a garlic derivative (alliin) on peripheral blood cell immune responses. Int J Immunopharmacol. 1999;21:589–597. https://www.ncbi.nlm.nih.gov/pubmed/10501628
47. Singh S, Natarajan K, Aggarwal BB. Capsaicin (8-methyl-N-vanillyl-6-nonenamide) is a potent inhibitor of nuclear transcription factor-kappa B activation by diverse agents. J Immunol. 1996;157:4412–4420. https://www.ncbi.nlm.nih.gov/pubmed/8906816
48. Lee YM. Kwon MJ. Kim JK. Suh HS. Choi JS. Song YO. Isolation and identification of active principle in Chinese cabbage kimchi responsible for antioxidant effect. Korean J Food Sci Technol. 2004;36:129–133.
49. 3-(4′-hydroxyl-3′,5′-dimethoxyphenyl)propionic acid, an active principle of kimchi, inhibits development of atherosclerosis in rabbits. Kim HJ, Lee JS, Chung HY, Song SH, Suh H, Noh JS, Song YO. J Agric Food Chem. 2007 Dec 12; 55(25):10486-92. https://www.ncbi.nlm.nih.gov/pubmed/18004805/
50. Active principle of kimchi, 3-(4′-hydroxyl-3′,5′-dimethoxyphenyl)propionic acid, retards fatty streak formation at aortic sinus of apolipoprotein E knockout mice. Noh JS, Kim HJ, Kwon MJ, Song YO. J Med Food. 2009 Dec; 12(6):1206-12. https://www.ncbi.nlm.nih.gov/pubmed/20041773/
51. Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Kim EK, An SY, Lee MS, Kim TH, Lee HK, Hwang WS, Choe SJ, Kim TY, Han SJ, Kim HJ, Kim DJ, Lee KW. Nutr Res. 2011 Jun; 31(6):436-43. https://www.ncbi.nlm.nih.gov/pubmed/21745625/
52. Lee H, Lee IS, Choue R. Obesity, inflammation and diet. Pediatr Gastroenterol Hepatol Nutr. 2013;16:143–152. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3819692/
53. Krehbiel CR, Rust SR, Zhang G, Gilliland SE. Bacterial direct-fed microbials in ruminant diets: performance response and mode of action. J Anim Sci. 2003;81:E120–E132.
54. Lee JW, Shin JG, Kim EH, Kang HE, Yim IB, Kim JY, Joo HG, Woo HJ. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J Vet Sci. 2004;5:41–48. https://www.ncbi.nlm.nih.gov/pubmed/15028884
55. Lee H, Kim DY, Lee MA, Jang J-Y, Choue R. Immunomodulatory Effects of Kimchi in Chinese Healthy College Students: A Randomized Controlled Trial. Clinical Nutrition Research. 2014;3(2):98-105. doi:10.7762/cnr.2014.3.2.98 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4135247/
56. Won TJ, Kim B, Lim YT, Song DS, Park SY, Park ES, Lee DI, Hwang KW. Oral administration of Lactobacillus strains from Kimchi inhibits atopic dermatitis in NC/Nga mice. J Appl Microbiol. 2011;110:1195–1202 https://www.ncbi.nlm.nih.gov/pubmed/21338447
57. Stanton C, Gardiner G, Meehan H, Collins K, Fitzgerald G, Lynch PB, Ross RP. Market potential for probiotics. Am J Clin Nutr. 2001;73:476S–483S. doi: 10.1093/ajcn/73.2.476s https://www.ncbi.nlm.nih.gov/pubmed/11157361
58. Xia Y, Chen HQ, Zhang M, Jiang YQ, Hang XM, Qin HL. Effect of Lactobacillus plantarum LP-Onlly on gut flora and colitis in interleukin-10 knockout mice. J Gastroenterol Hepatol. 2011;26:405–411. doi: 10.1111/j.1440-1746.2010.06498.x https://www.ncbi.nlm.nih.gov/pubmed/21261733
59. Park JS, Joe I, Rhee PD, Jeong CS, Jeong G. A lactic acid bacterium isolated from kimchi ameliorates intestinal inflammation in DSS-induced colitis. J Microbiol. 2017;55:304–310. doi: 10.1007/s12275-017-6447-y https://www.ncbi.nlm.nih.gov/pubmed/28124779
60. Roselli M, Finamore A, Nuccitelli S, Carnevali P, Brigidi P, Vitali B, Nobili F, Rami R, Garaguso I, Mengheri E. Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of gammadeltaT and regulatory T cells of intestinal intraepithelial lymphocytes. Inflamm Bowel Dis. 2009;15:1526–1536. doi: 10.1002/ibd.20961 https://www.ncbi.nlm.nih.gov/pubmed/19504616
61. Zhang M, Zhou L, Zhang S, Yang Y, Xu L, Hua Z, Zou X. Bifidobacterium longum affects the methylation level of forkhead box P3 promoter in 2, 4, 6-trinitrobenzenesulphonic acid induced colitis in rats. Microb Pathog. 2017;110:426–430. doi: 10.1016/j.micpath.2017.07.029 https://www.ncbi.nlm.nih.gov/pubmed/28733028
62. Bailey JR, Vince V, Williams NA, Cogan TA. Streptococcus thermophilus NCIMB 41856 ameliorates signs of colitis in an animal model of inflammatory bowel disease. Benef Microbes. 2017;8:605–614. doi: 10.3920/BM2016.0110 https://www.ncbi.nlm.nih.gov/pubmed/28618865
63. Toumi R, Soufli I, Rafa H, Belkhelfa M, Biad A, Touil-Boukoffa C. Probiotic bacteria lactobacillus and bifidobacterium attenuate inflammation in dextran sulfate sodium-induced experimental colitis in mice. Int J Immunopathol Pharmacol. 2014;27:615–627. doi: 10.1177/039463201402700418 https://www.ncbi.nlm.nih.gov/pubmed/25572742
64. Bellavia M, Rappa F, Lo Bello M, Brecchia G, Tomasello G, Leone A, Spatola G, Uzzo ML, Bonaventura G, David S, et al. Lactobacillus casei and bifidobacterium lactis supplementation reduces tissue damage of intestinal mucosa and liver after 2,4,6-trinitrobenzenesulfonic acid treatment in mice. J Biol Regul Homeost Agents. 2014;28:251–261 https://www.ncbi.nlm.nih.gov/pubmed/25001657
65. Kim MS, Byun JS, Yoon YS, Yum DY, Chung MJ, Lee JC. A probiotic combination attenuates experimental colitis through inhibition of innate cytokine production. Benef Microbes. 2017;8:231–241. doi: 10.3920/BM2016.0031 https://www.ncbi.nlm.nih.gov/pubmed/28008786