Journal of Digestive Cancer Research

Korean Society of Gastrointestinal Cancer Research (대한소화기암연구학회)
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Interaction between Dietary Factors and Gut Microbiota in Ulcerative Colitis

궤양성 대장염에서 식이 인자와 장 마이크로비오타의 상호작용

  • Mi-Kyung Sung (Department of Food and Nutrition, Sookmyung Women's University)
  • 성미경 (숙명여자대학교 식품영양학과)
  • Received : 2022.05.09
  • Accepted : 2022.05.21
  • Published : 2022.06.01
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Abstract

Ulcerative colitis (UC) exhibits chronic intestinal inflammatory conditions with cycles of relapse and remission. The incidence is rapidly growing in Asian countries including South Korea possibly due to changes in lifestyles. Although the etiology of inflammatory bowel disease is inconclusive, gut microbiota composition is considered a critical factor involved in the pathogenesis of UC. The overgrowth of pathogenic bacteria evokes hyper-immune responses in gut epithelium causing tissue inflammation and damage. Also, failure to regulate gut epithelium integrity due to chronic inflammation and mucus depletion accelerates bacterial translocation aggravating immune dysregulation. Gut microbiota composition responds to the diet in a very rapid manner. Epidemiological studies have indicated that the risk of UC is associated with low plant foods/high animal foods consumption. Several bacterial strains consistently found depleted in UC patients use plant food-originated dietary fiber producing short chain fatty acids to maintain epithelial integrity. These bacteria also use mucus layer mucin to keep gut microbiota diversity. These studies partly explain the association between dietary modification of gut microbiota in UC development. Further human intervention trials are required to allow the use of specific bacterial strains in the management of UC.

Keywords

Acknowledgement

This study was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2022R1A2C1004626).

References

  1. GBD 2017 Inflammatory Bowel Disease Collaborators. The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol 2020;5:17-30. https://doi.org/10.1016/S2468-1253(19)30333-4
  2. Park J, Cheon JH. Incidence and prevalence of inflammatory bowel disease across Asia. Yonsei Med J 2021;62:99-108. https://doi.org/10.3349/ymj.2021.62.2.99
  3. Ng SC, Shi HY, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 2017;390:2769-2778. Erratum in: Lancet 2020;396:e56.
  4. Graham DB, Xavier RJ. Pathway paradigms revealed from the genetics of inflammatory bowel disease. Nature 2020;578:527-539. https://doi.org/10.1038/s41586-020-2025-2
  5. Tysk C, Lindberg E, Jarnerot G, Floderus-Myrhed B. Ulcerative colitis and Crohn's disease in an unselected population of monozygotic and dizygotic twins. A study of heritability and the influence of smoking. Gut 1988;29:990-996. https://doi.org/10.1136/gut.29.7.990
  6. Orholm M, Binder V, Sorensen TI, Rasmussen LP, Kyvik KO. Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scand J Gastroenterol 2000;35:1075-1081. https://doi.org/10.1080/003655200451207
  7. Kahrstrom CT, Pariente N, Weiss U. Intestinal microbiota in health and disease. Nature 2016;535:47.
  8. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med 2016;375:2369-2379. https://doi.org/10.1056/NEJMra1600266
  9. Sonnenburg JL, Backhed F. Diet-microbiota interactions as moderators of human metabolism. Nature 2016;535:56-64. https://doi.org/10.1038/nature18846
  10. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol 2011;106:563-573. https://doi.org/10.1038/ajg.2011.44
  11. Li F, Liu X, Wang W, Zhang D. Consumption of vegetables and fruit and the risk of inflammatory bowel disease: a meta-analysis. Eur J Gastroenterol Hepatol 2015;27:623-630. https://doi.org/10.1097/MEG.0000000000000330
  12. Racine A, Carbonnel F, Chan SS, et al. Dietary patterns and risk of inflammatory bowel disease in Europe: results from the EPIC study. Inflamm Bowel Dis 2016;22:345-354. https://doi.org/10.1097/MIB.0000000000000638
  13. Jantchou P, Morois S, Clavel-Chapelon F, Boutron-Ruault MC, Carbonnel F. Animal protein intake and risk of inflammatory bowel disease: the E3N prospective study. Am J Gastroenterol 2010;105:2195-2201. https://doi.org/10.1038/ajg.2010.192
  14. Siva S, Rubin DT, Gulotta G, Wroblewski K, Pekow J. Zinc deficiency is associated with poor clinical outcomes in patients with inflammatory bowel disease. Inflamm Bowel Dis 2017;23:152-157.
  15. Kanauchi O, Suga T, Tochihara M, et al. Treatment of ulcerative colitis by feeding with germinated barley foodstuff: first report of a multicenter open control trial. J Gastroenterol 2002;37 Suppl 14:67-72.
  16. Casellas F, Borruel N, Torrejon A, et al. Oral oligofructose-enriched inulin supplementation in acute ulcerative colitis is well tolerated and associated with lowered faecal calprotectin. Aliment Pharmacol Ther 2007;25:1061-1067. https://doi.org/10.1111/j.1365-2036.2007.03288.x
  17. Bhattacharyya S, Shumard T, Xie H, et al. A randomized trial of the effects of the no-carrageenan diet on ulcerative colitis disease activity. Nutr Healthy Aging 2017;4:181-192. https://doi.org/10.3233/NHA-170023
  18. Wright R, Truelove SC. A controlled therapeutic trial of various diets in ulcerative colitis. Br Med J 1965;2:138-141. https://doi.org/10.1136/bmj.2.5454.138
  19. Pedersen N, Ankersen DV, Felding M, et al. Low-FODMAP diet reduces irritable bowel symptoms in patients with inflammatory bowel disease. World J Gastroenterol 2017;23:3356-3366.
  20. Pariente N. A field is born. 2019. https://media.nature.com/original/magazine-assets/d42859-019-00006-2/d42859-019-00006-2.pdf (accessed April 23, 2022).
  21. Tang L. Sequence-based identification of human-associated microbiota. 2019. https://media.nature.com/original/magazine-assets/d42859-019-00011-5/d42859-019-00011-5.pdf (accessed April 23, 2022).
  22. Bondar T. Regulation of mucosal immunity by the microbiota. 2019. https://media.nature.com/original/magazineassets/d42859-019-00014-2/d42859-019-00014-2.pdf (accessed April 23, 2022).
  23. Aldars-Garcia L, Chaparro M, Gisbert JP. Systematic review: the gut microbiome and its potential clinical application in inflammatory bowel disease. Microorganisms 2021;9:977.
  24. Ott SJ, Musfeldt M, Wenderoth DF, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004;53:685-693. https://doi.org/10.1136/gut.2003.025403
  25. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010;107:14691-14696. https://doi.org/10.1073/pnas.1005963107
  26. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 2014;146:1564-1572. https://doi.org/10.1053/j.gastro.2014.01.058
  27. Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature 2016;529:212-215. https://doi.org/10.1038/nature16504
  28. Nemoto H, Kataoka K, Ishikawa H, et al. Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis. Dig Dis Sci 2012;57:2955-2964. https://doi.org/10.1007/s10620-012-2236-y
  29. Santoru ML, Piras C, Murgia A, et al. Cross sectional evaluation of the gut-microbiome metabolome axis in an Italian cohort of IBD patients. Sci Rep 2017;7:9523. Erratum in: Sci Rep 2018;8:4993.
  30. Kumari R, Ahuja V, Paul J. Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India. World J Gastroenterol 2013;19:3404-3414. https://doi.org/10.3748/wjg.v19.i22.3404
  31. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012;13:R79.
  32. Guo X, Huang C, Xu J, et al. Gut microbiota is a potential biomarker in inflammatory bowel disease. Front Nutr 2022;8:818902.
  33. Machiels K, Joossens M, Sabino J, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 2014;63:1275-1283. https://doi.org/10.1136/gutjnl-2013-304833
  34. Wang W, Chen L, Zhou R, et al. Increased proportions of Bifidobacterium and the Lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J Clin Microbiol 2014;52:398-406. https://doi.org/10.1128/JCM.01500-13
  35. Pittayanon R, Lau JT, Leontiadis GI, et al. Differences in gut microbiota in patients with vs without inflammatory bowel diseases: a systematic review. Gastroenterology 2020;158:930-946.e1. https://doi.org/10.1053/j.gastro.2019.11.294
  36. Chelakkot C, Ghim J, Ryu SH. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med 2018;50:1-9. https://doi.org/10.1038/s12276-018-0126-x
  37. Marchiando AM, Graham WV, Turner JR. Epithelial barriers in homeostasis and disease. Annu Rev Pathol 2010;5:119-144. https://doi.org/10.1146/annurev.pathol.4.110807.092135
  38. Tailford LE, Crost EH, Kavanaugh D, Juge N. Mucin glycan foraging in the human gut microbiome. Front Genet 2015;6:81.
  39. Nakayama J, Zhang H, Lee YK. Asian gut microbiome. Sci Bull 2017;62:816-817. https://doi.org/10.1016/j.scib.2017.04.001
  40. Pareek S, Kurakawa T, Das B, et al. Comparison of Japanese and Indian intestinal microbiota shows diet-dependent interaction between bacteria and fungi. NPJ Biofilms Microbiomes 2019;5:37.
  41. Derrien M, Belzer C, de Vos WM. Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 2017;106:171-181.
  42. Derrien M, Van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos WM. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol 2011;2:166.
  43. Ottman N, Huuskonen L, Reunanen J, et al. Characterization of outer membrane proteome of Akkermansia muciniphila reveals sets of novel proteins exposed to the human intestine. Front Microbiol 2016;7:1157.
  44. Ottman N, Reunanen J, Meijerink M, et al. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS One 2017;12:e0173004.
  45. Mariadason JM, Corner GA, Augenlicht LH. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res 2000;60:4561-4572.
  46. Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol 2017;19:29-41.
  47. Zhuang X, Li T, Li M, et al. Systematic review and meta-analysis: short-chain fatty acid characterization in patients with inflammatory bowel disease. Inflamm Bowel Dis 2019;25:1751-1763. https://doi.org/10.1093/ibd/izz188
  48. Xu HM, Zhao HL, Guo GJ, et al. Characterization of short-chain fatty acids in patients with ulcerative colitis: a meta-analysis. BMC Gastroenterol 2022;22:117.
  49. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 2009;294:1-8. https://doi.org/10.1111/j.1574-6968.2009.01514.x