Kimchi improves irritable bowel syndrome: results of a randomized, double-blind placebo-controlled study

  • Hee-Young Kim Korean Medicine Research Center for Healthy Aging, Pusan National University, Yangsan, Gyeongsangnam-do, Republic of Korea https://orcid.org/0000-0002-2637-8621
  • Eui-Seong Park uhan Care R&D Center, Yongin, Gyeonggi-do, Republic of Korea
  • Young Sik Choi Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea
  • Seun Ja Park Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea
  • Jae Hyun Kim Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea
  • Hee Kyung Chang Department of Pathology, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea
  • Kun-Young Park Department of Food Science and Biotechnology, Cha University, Seongnam, Gyeonggi-do, Republic of Korea; and Chongqing Collaborative Innovation Center for Functional Food, Chongqing University of Education, Chongqing, China
Keywords: kimchi, irritable bowel syndrome, IBS, lactic acid bacteria, LAB, Lactobacillus plantarum nF1, microbiome, gut, clinical study

Abstract

Background: Irritable bowel syndrome (IBS) can be caused by abnormal bowel movements, altered brain-gut axis, gut microbiota change, and low levels of inflammation or immune activation. The intake of food containing much fiber and lactic acid bacteria (LABs) can alleviate IBS.

Objective: This study was undertaken to confirm the alleviative effect of kimchi on symptoms of IBS.

Design: Three types of kimchi (standard kimchi, SK; dead nano-sized Lactobacillus plantarum nF1 (nLp) added to standard kimchi, nLpSK; or functional kimchi, FK) were given to 30 individuals in each of three groups, that is, the SK group (n = 30), the nLpSK group (n = 30), or the FK group (n = 30) at 210 g a day for 12 weeks. Food intake records, serum levels of inflammatory factors, fecal levels of harmful enzymes, and microbiome changes were investigated over the 12-week study period.

Results: After intervention, dietary fiber intake was increased in all groups. Typical IBS symptoms (abdominal pain or inconvenience, desperation, incomplete evacuation, and bloating), defecation time, and stool type were also improved. In serum, all groups showed reductions in tumor necrosis factor (TNF)-α (P < 0.001) levels. In addition, serum IL-4 (P < 0.001), IL-10 (P < 0.001), and IL-12 (P < 0.01) were significantly reduced in the nLpSK and FK groups, and serum monocyte chemotactic protein (MCP)-1 (P < 0.05) was significantly reduced in the nLpSK group. Furthermore, activities of fecal β-glucosidase and β-glucuronidase were significantly decreased in all three groups, and these reductions were greatest in the nLpSK group. Gut microbiome analysis showed that kimchi consumption increased Firmicutes populations at the expense of Bacteroidetes and Tenericutes populations. In addition, the Bifidobacterium adolescentis population increased significantly in the FK group (P = 0.026).

Conclusion: Kimchi intake helps alleviate IBS by increasing dietary fiber intake and reducing serum inflammatory cytokine levels and harmful fecal enzyme activities. Notably, nLp improved the immune system, and several functional ingredients in FK promoted the growth of Bifidobacterium adolescentis in gut.

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Author Biographies

Hee-Young Kim, Korean Medicine Research Center for Healthy Aging, Pusan National University, Yangsan, Gyeongsangnam-do, Republic of Korea

Korean Medicine Research Center for Healthy Aging, Pusan National University

Eui-Seong Park, uhan Care R&D Center, Yongin, Gyeonggi-do, Republic of Korea

Department of Food and Nutrition, Yonsei University

Young Sik Choi, Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea

Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine

Seun Ja Park, Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea

Department of Gastroenterology, Kosin University Gospel Hospital, Kosin University College of Medicine

Jae Hyun Kim, Department of Internal Medicine, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea

Department of Gastroenterology, Kosin University Gospel Hospital, Kosin University College of Medicine

Hee Kyung Chang, Department of Pathology, Kosin University Gospel Hospital, Kosin University College of Medicine, Busan, Republic of Korea

Department of Pathology, Kosin University Gospel Hospital, Kosin University College of Medicine

Kun-Young Park, Department of Food Science and Biotechnology, Cha University, Seongnam, Gyeonggi-do, Republic of Korea; and Chongqing Collaborative Innovation Center for Functional Food, Chongqing University of Education, Chongqing, China

Department of Food Science and Biotechnology

References


  1. Drossman DA. The functional gastrointestinal disorders and the Rome II process. Gut 1999; 45 Suppl 2: Ii1–5. doi: 10.1136/gut.45.2008.ii1

  2. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterol 2006; 130: 1480–91. doi: 10.1053/j.gastro.2005.11.061

  3. Cash B, Sullivan S, Barghout V. Total costs of IBS: employer and managed care perspective. Am J Manag Care 2005; 11: S7–16.

  4. Han SH, Lee OY, Bae SC, Lee SH, Chang YK, Yang SY, et al. Prevalence of irritable bowel syndrome in Korea: population-based survey using the Rome II criteria. J Gastroenterol Hepatol 2006; 21: 1687–92. doi: 10.1111/j.1440-1746.2006.04269.x

  5. Yu J. Update view of irritable bowel syndrome. J Korean Life Insur Med Assoc 2002; 21: 23–31.

  6. Ling WH, Korpela R, Mykkänen H, Salminen S, Hänninen O. Lactobacillus strain GG supplementation decreases colonic hydrolytic and reductive enzyme activities in healthy female adults. J Nutr 1994; 124: 18–23. doi: 10.1093/jn/124.1.18

  7. Clarke G, Quigley EM, Cryan JF, Dinan TG. Irritable bowel syndrome: towards biomarker identification. Trends Mol Med 2009; 15: 478–89. doi: 10.1016/j.molmed.2009.08.001

  8. Chang L, Adeyemo M, Karagiannides I, Videlock EJ, Bowe C, Shih W, et al. Serum and colonic mucosal immune markers in irritable bowel syndrome. Am J Gastroenterol 2012; 107: 262–72. doi: 10.1038/ajg.2011.423

  9. Park KY, Jeong JK, Lee YE, Daily III JW. Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. J Med Food 2014; 17: 6–20. doi: 10.1089/jmf.2013.3083

  10. Jung JY, Lee SH, Jin HM, Hahn Y, Madsen EL, Jeon CO. Metatranscriptomic analysis of lactic acid bacterial gene expression during kimchi fermentation. Int J Food Microbiol 2013; 163: 171–9. doi: 10.1016/j.ijfoodmicro.2013.02.022

  11. 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: 129–33.

  12. Cui M, Kim HY, Lee KH, Jeong JK, Hwang JH, Yeo KY, et al. Antiobesity effects of kimchi in diet-induced obese mice. J Ethn Foods 2015; 2: 137–44. doi: 10.1016/j.jef.2015.08.001

  13. Kim EK, An SY, Lee MS, Kim TH, Lee HK, Hwang WS, et al. Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutr Res 2011; 31: 436–43. doi: 10.1016/j.nutres.2011.05.011

  14. Islam MS, Choi H. Antidiabetic effect of Korean traditional Baechu (Chinese cabbage) kimchi in a type 2 diabetes model of rats. J Med Food 2009; 12: 292–7. doi: 10.1089/jmf.2008.0181

  15. Lee HA, Bong YJ, Kim H, Jeong JK, Kim HY, Lee KW, et al. Effect of nanometric Lactobacillus plantarum in kimchi on dextran sulfate sodium-induced colitis in mice. J Med Food 2015; 18: 1073–80. doi: 10.1089/jmf.2015.3509

  16. Kim HY, Song JL, Chang HK, Kang SA, Park KY. Kimchi protects against azoxymethane/dextran sulfate sodium-induced colorectal carcinogenesis in mice. J Med Food 2014; 17: 833–41. doi: 10.1089/jmf.2013.2986

  17. Kim HY, Park KY. Clinical trials of kimchi intakes on the regulation of metabolic parameters and colon health in healthy Korean young adults. J Funct Foods 2018; 47: 325–33. doi: 10.1016/j.jff.2018.05.052

  18. Lee KH, Song JL, Park ES, Ju J, Kim HY, Park KY. Anti-obesity effects of starter fermented kimchi on 3T3-L1 adipocytes. Prev Nutr Food Sci 2015; 20: 298–302. doi: 10.3746/pnf.2015.20.4.298

  19. Drossman DA, Dumitrascu DL. Rome III: new standard for functional gastrointestinal disorders. J Gastrointestin Liver Dis 2006; 15: 237–41.

  20. Ringel Kulka T, Palsson OS, Maier D, Carroll I, Galanko JA, Leyer G, et al. Probiotic bacteria Lactobacillus acidophilus NCFM and Bifidobacterium lactis Bi-07 versus placebo for the symptoms of bloating in patients with functional bowel disorders: a double-blind study. J Clin Gastroenterol 2011; 45: 518–25. doi: 10.1097/MCG.0b013e31820ca4d6

  21. Riegler G, Esposito I. Bristol scale stool form. A still valid help in medical practice and clinical research. Tech Coloproctol 2001; 5: 163–4. doi: 10.1007/s101510100019

  22. Lee KE, Choi UH, Ji GE. Effect of kimchi intake on the composition of human large intestinal bacteria. Korean J Food Sci Technol 1996; 28: 981–6.

  23. Jung JY, Lee SH, Kim JM, Park MS, Bae JW, Hahn Y, et al. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl Environ Microbiol 2011; 77: 2264–74. doi: 10.1128/aem.02157-10

  24. Chun J, Kim KY, Lee JH, Choi Y. The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol 2010; 10: 1–8. doi: 10.1186/1471-2180-10-101

  25. Huber T, Faulkner G, Hugenholtz P. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinform 2004; 20: 2317–9. doi: 10.1093/bioinformatics/bth226

  26. Kim JN, Kim BS, Kim SJ, Cerniglia CE. Effects of crude oil, dispersant, and oil-dispersant mixtures on human fecal microbiota in an in vitro culture system. MBio 2012; 3: e00376–12. doi: 10.1128/mBio.00376-12

  27. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB, Mattarelli P, et al. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 2020; 70: 2782–858. doi: 10.1099/ijsem.0.004107

  28. Lee HA, Kim H, Lee KW, Park KY. Dead nano-sized Lactobacillus plantarum inhibits azoxymethane/dextran sulfate sodium-induced colon cancer in balb/c mice. J Med Food 2015; 18: 1400–5. doi: 10.1089/jmf.2015.3577

  29. 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: 223–9. doi: 10.1089/jmf.2012.2563

  30. Yu K-H, Chung C-E, Ly S-Y. Analysis of dietary fiber intake in the Korean adult population using 2001 Korean National Health and Nutrition Survey data and newly established dietary fiber database. J Nutr Health 2008; 41: 100–10.

  31. Seyedmirzaee S, Hayatbakhsh MM, Ahmadi B, Baniasadi N, Rafsanjani AMB, Nikpoor AR, et al. Serum immune biomarkers in irritable bowel syndrome. Clin Res Hepatol Gastroenterol 2016; 40: 631–7. doi: 10.1016/j.clinre.2015.12.013

  32. Darkoh C, Comer L, Zewdie G, Harold S, Snyder N, DuPont HL. Chemotactic chemokines are important in the pathogenesis of irritable bowel syndrome. PLoS One 2014; 9: e93144. doi: 10.1371/journal.pone.0093144

  33. Hughes PA, Harrington AM, Castro J, Liebregts T, Adam B, Grasby DJ, et al. Sensory neuro-immune interactions differ between irritable bowel syndrome subtypes. Gut 2013; 62: 1456–65. doi: 10.1136/gutjnl-2011-301856

  34. Hughes PA, Zola H, Penttila IA, Blackshaw LA, Andrews JM, Krumbiegel D. Immune activation in irritable bowel syndrome: can neuroimmune interactions explain symptoms? Am J Gastroenterol 2013; 108: 1066–74. doi: 10.1038/ajg.2013.120

  35. Berg LK, Goll R, Fagerli E, Ludviksen JK, Fure H, Moen OS, et al. Intestinal inflammatory profile shows increase in a diversity of biomarkers in irritable bowel syndrome. Scand J Gastroenterol 2020; 55: 537–42. doi: 10.1080/00365521.2020.1754455

  36. Liebregts T, Adam B, Bredack C, Gururatsakul M, Pilkington KR, Brierley SM, et al. Small bowel homing T cells are associated with symptoms and delayed gastric emptying in functional dyspepsia. Am J Gastroenterol 2011; 106: 1089–98. doi: 10.1038/ajg.2010.512

  37. Swan C, Duroudier NP, Campbell E, Zaitoun A, Hastings M, Dukes GE, et al. Identifying and testing candidate genetic polymorphisms in the irritable bowel syndrome (IBS): association with TNFSF15 and TNFα. Gut 2013; 62: 985–94. doi: 10.1136/gutjnl-2011-301213

  38. Kucharzik T, Stoll R, Lügering N, Domschke W. Circulating antiinflammatory cytokine IL-10 in patients with inflammatory bowel disease (IBD). Clin Exp Immunol 1995; 100: 452–6. doi: 10.1111/j.1365-2249.1995.tb03721.x

  39. Lee HA, Kim H, Lee KW, Park KY. Dead Lactobacillus plantarum stimulates and skews immune responses toward T helper 1 and 17 polarizations in RAW 264.7 cells and mouse splenocytes. J Microbiol Biotechnol 2016; 26: 469–76. doi: 10.4014/jmb.1511.11001

  40. Hasegawa H, Kan T. Immunity for longevity and lactic acid bacteria: the effect of nanometric particles of lactic acid bacteria on Th1 cell induction. New Food Ind 2008; 50: 1–8.

  41. Tabata Y, Inoue Y, Ikada Y. Size effect on systemic and mucosal immune responses induced by oral administration of biodegradable microspheres. Vaccine 1996; 14: 1677–85. doi: 10.1016/S0264-410X(96)00149-1

  42. Lee CH, Kim JK, Kim HY, Park SM, Lee SM. Immunomodulating effects of Korean mistletoe lectin in vitro and in vivo. Int Immunopharmacol 2009; 9: 1555–61. doi: 10.1016/j.intimp.2009.09.011

  43. Oei SL, Thronicke A, Schad F. Mistletoe and immunomodulation: insights and implications for anticancer therapies. Evid Based Complement Alternat Med 2019; 2019: 5893017. doi: 10.1155/2019/5893017

  44. Kim YT, Kim BK, Park KY. Antimutagenic and anticancer effects of leaf mustard and leaf mustard kimchi. Prev Nutr Food Sci 2007; 12: 84–8. doi: 10.3746/jfn.2007.12.2.084

  45. Srinivasan K. Antioxidant potential of spices and their active constituents. Crit Rev Food Sci Nutr 2014; 54: 352–72. doi: 10.1080/10408398.2011.585525

  46. Kajander K, Krogius-Kurikka L, Rinttilä T, Karjalainen H, Palva A, Korpela R. Effects of multispecies probiotic supplementation on intestinal microbiota in irritable bowel syndrome. Aliment Pharmacol Ther 2007; 26: 463–73. doi: 10.1111/j.1365-2036.2007.03391.x

  47. Brenner DM, Chey WD. Bifidobacterium infantis 35624: a novel probiotic for the treatment of irritable bowel syndrome. Rev Gastroenterol Disord 2009; 9: 7–15.

  48. Ortiz Lucas M, Tobias A, Sebastián J, Saz P. Effect of probiotic species on irritable bowel syndrome symptoms: a bring up to date meta-analysis. Rev Esp Enferm Dig 2013; 105: 19–36. doi: 10.4321/S1130-01082013000100005

  49. Higashikawa F, Noda M, Awaya T, Nomura K, Oku H, Sugiyama M. Improvement of constipation and liver function by plant-derived lactic acid bacteria: a double-blind, randomized trial. Nutrition 2010; 26: 367–74. doi: 10.1016/j.nut.2009.05.008

  50. Kim JY, Kim OY, Yoo HJ, Kim TI, Kim WH, Yoon YD, et al. Effects of fiber supplements on functional constipation. J Nutr Health 2006; 39: 35–43.

  51. Lee KH, Bong YJ, Lee HA, Kim HY, Park KY. Probiotic effects of Lactobacillus plantarum and Leuconostoc mesenteroides isolated from kimchi. J Korean Soc Food Sci Nutr 2016; 45: 12–9. doi: 10.3746/jkfn.2016.45.1.012

  52. Choi HS, Shon CI, Cho YK, Kim HJ, Park DI, Chun WK, et al. The effect of red pepper on gastric emptying. Kor J Neurogastroenterol Motil 2005; 11: 33–7.

  53. Kawada T, Suzuki T, Takahashi M, Iwai K. Gastrointestinal absorption and metabolism of capsaicin and dihydrocapsaicin in rats. Toxicol Appl Pharmacol 1984; 72: 449–56. doi: 10.1016/0041-008x(84)90121-2

  54. Suresh D, Srinivasan K. Studies on the in vitro absorption of spice principles–curcumin, capsaicin and piperine in rat intestines. Food Chem Toxicol 2007; 45: 1437–42. doi: 10.1016/j.fct.2007.02.002

  55. Bortolotti M, Coccia G, Grossi G, Miglioli M. The treatment of functional dyspepsia with red pepper. Aliment Pharmacol Ther 2002; 16: 1075–82. doi: 10.1046/j.1365-2036.2002.01280.x

  56. Martineau B, Laflamme D. Effect of diet on markers of intestinal health in dogs. Res Vet Sci 2002; 72: 223–7. doi: 10.1053/rvsc.2002.0548

  57. Goldin BR, Gorbach SL. The relationship between diet and rat fecal bacterial enzymes implicated in colon cancer. J Natl Cancer Inst 1976; 57: 371–5. doi: 10.1093/jnci/57.2.371

  58. Mueller C, Friedel A, Michel P, Oh Y-J. The influence of sauerkraut and kimchi on bacterial enzyme activities and the pH of human faeces. Aktuel Ernahrungsmed 1993; 18: 351.

  59. Krogius Kurikka L, Lyra A, Malinen E, Aarnikunnas J, Tuimala J, Paulin L, et al. Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers. BMC Gastroenterol 2009; 9: 95. doi: 10.1186/1471-230x-9-95

  60. Rajilić Stojanović M, Biagi E, Heilig HG, Kajander K, Kekkonen RA, Tims S, et al. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterol 2011; 141: 1792–801. doi: 10.1053/j.gastro.2011.07.043

  61. Balsari A, Ceccarelli A, Dubini F, Fesce E, Poli G. The fecal microbial population in the irritable bowel syndrome. Microbiologica 1982; 5: 185–94.

  62. Si JM, Yu YC, Fan YJ, Chen SJ. Intestinal microecology and quality of life in irritable bowel syndrome patients. World J Gastroenterol 2004; 10: 1802. doi: 10.3748/wjg.v10.i12.1802

Published
2022-05-23
How to Cite
Kim H.-Y., Park E.-S., Choi Y. S., Park S. J., Kim J. H., Chang H. K., & Park K.-Y. (2022). Kimchi improves irritable bowel syndrome: results of a randomized, double-blind placebo-controlled study. Food & Nutrition Research, 66. https://doi.org/10.29219/fnr.v66.8268
Section
Original Articles