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Increasing incidence of inflammatory bowel disease in children and adolescents: significance of environmental factors

  • Park, Sowon (Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Severance Pediatric IBD Research Group, Severance Children's Hospital, Yonsei University College of Medicine) ;
  • Kang, Yunkoo (Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Wonju Severance Christian Hospital, Wonju College of Medicine, Yonsei University) ;
  • Koh, Hong (Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Severance Pediatric IBD Research Group, Severance Children's Hospital, Yonsei University College of Medicine) ;
  • Kim, Seung (Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Severance Pediatric IBD Research Group, Severance Children's Hospital, Yonsei University College of Medicine)
  • Received : 2019.05.15
  • Accepted : 2019.11.22
  • Published : 2020.09.15

Abstract

Inflammatory bowel disease (IBD) is a chronic relapsing immune-mediated disease of the intestinal tract. Although its prevalence is reportedly lower in Asia than in Western countries, the rapid increase in the incidence of IBD has drawn attention to its etiology, including genetic susceptibility and environmental factors. Specifically, recent studies concerning dietary treatments and intestinal microbiota suggest that these factors may interact with the immune system, and the imbalance of this relationship may lead to immune dysregulation in IBD. Changes in diet or alterations in the composition of the intestinal microbiota may be associated with the increasing incidence of IBD in Asia. Here, we aim to review recent studies on the role of diet and intestinal microbiota in IBD pathogenesis and the results of the investigations performed to modulate these factors.

Keywords

References

  1. Benchimol EI, Manuel DG, Guttmann A, Nguyen GC, Mojaverian N, Quach P, et al. Changing age demographics of inflammatory bowel disease in Ontario, Canada: a population-based cohort study of epidemiology trends. Inflamm Bowel Dis 2014;20:1761-9. https://doi.org/10.1097/MIB.0000000000000103
  2. Kappelman MD, Moore KR, Allen JK, Cook SF. Recent trends in the prevalence of Crohn's disease and ulcerative colitis in a commercially insured US population. Dig Dis Sci 2013;58:519-25. https://doi.org/10.1007/s10620-012-2371-5
  3. Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology 2017;152:313-21.e2. https://doi.org/10.1053/j.gastro.2016.10.020
  4. Asakura K, Nishiwaki Y, Inoue N, Hibi T, Watanabe M, Takebayashi T. Prevalence of ulcerative colitis and Crohn's disease in Japan. J Gastroenterol 2009;44:659-65. https://doi.org/10.1007/s00535-009-0057-3
  5. Yang SK, Yun S, Kim JH, Park JY, Kim HY, Kim YH, et al. Epidemiology of inflammatory bowel disease in the Songpa-Kangdong district, Seoul, Korea, 1986-2005: a KASID study. Inflamm Bowel Dis 2008;14:542-9. https://doi.org/10.1002/ibd.20310
  6. Benchimol EI, Mack DR, Nguyen GC, Snapper SB, Li W, Mojaverian N, et al. Incidence, outcomes, and health services burden of very early onset inflammatory bowel disease. Gastroenterology 2014;147:803-13.e7;quiz e14-5. https://doi.org/10.1053/j.gastro.2014.06.023
  7. Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006;3:390-407. https://doi.org/10.1038/ncpgasthep0528
  8. Kaplan GG. The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol 2015;12:720-7. https://doi.org/10.1038/nrgastro.2015.150
  9. Halfvarson J, Bodin L, Tysk C, Lindberg E, Jarnerot G. Inflammatory bowel disease in a Swedish twin cohort: a long-term follow-up of concordance and clinical characteristics. Gastroenterology 2003;124:1767-73. https://doi.org/10.1016/S0016-5085(03)00385-8
  10. Legaki E, Gazouli M. Influence of environmental factors in the development of inflammatory bowel diseases. World J Gastrointest Pharmacol Ther 2016 6;7:112-25. https://doi.org/10.4292/wjgpt.v7.i1.112
  11. Levine A, Wine E, Assa A, Sigall Boneh R, Shaoul R, Kori M, et al. Crohn's disease exclusion diet plus partial enteral nutrition induces sustained remission in a randomized controlled trial. Gastroenterology 2019;157:440-50.e8. https://doi.org/10.1053/j.gastro.2019.04.021
  12. Jeon SR, Chai J, Kim C, Lee CH. Current evidence for the management of inflammatory bowel diseases using fecal microbiota transplantation. Curr Infect Dis Rep 2018;20:21. https://doi.org/10.1007/s11908-018-0627-8
  13. Vermeire S, Joossens M, Verbeke K, Wang J, Machiels K, Sabino J, et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohns Colitis 2016;10:387-94. https://doi.org/10.1093/ecco-jcc/jjv203
  14. Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, et al. Fecal microbiota transplantation through mid-gut for refractory Crohn's disease: safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol 2015;30:51-8. https://doi.org/10.1111/jgh.12727
  15. Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet 2017;389:1218-28. https://doi.org/10.1016/S0140-6736(17)30182-4
  16. Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 2015;149:102-9.e6. https://doi.org/10.1053/j.gastro.2015.04.001
  17. Rossen NG, Fuentes S, van der Spek MJ, Tijssen JG, Hartman JH, Duflou A, et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 2015;149:110-8.e4. https://doi.org/10.1053/j.gastro.2015.03.045
  18. Huang EY, Devkota S, Moscoso D, Chang EB, Leone VA. The role of diet in triggering human inflammatory disorders in the modern age. Microbes Infect 2013;15:765-74. https://doi.org/10.1016/j.micinf.2013.07.004
  19. Agus A, Denizot J, Thevenot J, Martinez-Medina M, Massier S, Sauvanet P, et al. Western diet induces a shift in microbiota composition enhancing susceptibility to Adherent-Invasive E. coli infection and intestinal inflammation. Sci Rep 2016;6:19032. https://doi.org/10.1038/srep19032
  20. Statovci D, Aguilera M, MacSharry J, Melgar S. The impact of western diet and nutrients on the microbiota and immune response at mucosal interfaces. Front Immunol 2017;8:838. https://doi.org/10.3389/fimmu.2017.00838
  21. Zuo T, Ng SC. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front Microbiol 2018;9:2247. https://doi.org/10.3389/fmicb.2018.02247
  22. Sakamoto N, Kono S, Wakai K, Fukuda Y, Satomi M, Shimoyama T, et al. Dietary risk factors for inflammatory bowel disease: a multicenter casecontrol study in Japan. Inflamm Bowel Dis 2005;11:154-63. https://doi.org/10.1097/00054725-200502000-00009
  23. Haskey N, Gibson DL. An Examination of diet for the maintenance of remission in inflammatory bowel disease. Nutrients 2017;9:259. https://doi.org/10.3390/nu9030259
  24. 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;106:563-73. https://doi.org/10.1038/ajg.2011.44
  25. John S, Luben R, Shrestha SS, Welch A, Khaw KT, Hart AR. Dietary n-3 polyunsaturated fatty acids and the aetiology of ulcerative colitis: a UK prospective cohort study. Eur J Gastroenterol Hepatol 2010;22:602-6. https://doi.org/10.1097/MEG.0b013e3283352d05
  26. Soderholm JD, Oman H, Blomquist L, Veen J, Lindmark T, Olaison G. Reversible increase in tight junction permeability to macromolecules in rat ileal mucosa in vitro by sodium caprate, a constituent of milk fat. Dig Dis Sci 1998;43:1547-52. https://doi.org/10.1023/A:1018823100761
  27. Soderholm JD, Olaison G, Peterson KH, Franzen LE, Lindmark T, Wiren M, et al. Augmented increase in tight junction permeability by luminal stimuli in the non-inflamed ileum of Crohn's disease. Gut 2002;50:307-13. https://doi.org/10.1136/gut.50.3.307
  28. Lammers KM, Lu R, Brownley J, Lu B, Gerard C, Thomas K, et al. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology 2008;135:194-204.e3. https://doi.org/10.1053/j.gastro.2008.03.023
  29. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol 2014;14:329-42. https://doi.org/10.1038/nri3661
  30. Swidsinski A, Ung V, Sydora BC, Loening-Baucke V, Doerffel Y, Verstraelen H, et al. Bacterial overgrowth and inflammation of small intestine after carboxymethylcellulose ingestion in genetically susceptible mice. Inflamm Bowel Dis 2009;15:359-64. https://doi.org/10.1002/ibd.20763
  31. Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 2015;519:92-6. https://doi.org/10.1038/nature14232
  32. Roberts CL, Keita AV, Duncan SH, O'Kennedy N, Soderholm JD, Rhodes JM, et al. Translocation of Crohn's disease Escherichia coli across M-cells: contrasting effects of soluble plant fibres and emulsifiers. Gut 2010;59:1331-9. https://doi.org/10.1136/gut.2009.195370
  33. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65. https://doi.org/10.1038/nature08821
  34. Prakash S, Rodes L, Coussa-Charley M, Tomaro-Duchesneau C. Gut microbiota: next frontier in understanding human health and development of biotherapeutics. Biologics 2011;5:71-86. https://doi.org/10.2147/BTT.S19099
  35. Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013;13:321-35. https://doi.org/10.1038/nri3430
  36. De Cruz P, Prideaux L, Wagner J, Ng SC, McSweeney C, Kirkwood C, et al. Characterization of the gastrointestinal microbiota in health and inflammatory bowel disease. Inflamm Bowel Dis 2012;18:372-90. https://doi.org/10.1002/ibd.21751
  37. Halfvarson J, Brislawn CJ, Lamendella R, Vazquez-Baeza Y, Walters WA, Bramer LM, et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol 2017;2:17004. https://doi.org/10.1038/nmicrobiol.2017.4
  38. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 2014;146:1489-99. https://doi.org/10.1053/j.gastro.2014.02.009
  39. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014;15:382-92. https://doi.org/10.1016/j.chom.2014.02.005
  40. Olbjorn C, Cvancarova Smastuen M, Thiis-Evensen E, Nakstad B, Vatn MH, Jahnsen J, et al. Fecal microbiota profiles in treatment-naive pediatric inflammatory bowel disease - associations with disease phenotype, treatment, and outcome. Clin Exp Gastroenterol 2019;12:37-49. https://doi.org/10.2147/ceg.s186235
  41. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. Version 2. PLoS Biol 2007;5:e177. https://doi.org/10.1371/journal.pbio.0050177
  42. Wu GD, Bushmanc FD, Lewis JD. Diet, the human gut microbiota, and IBD. Anaerobe 2013;24:117-20. https://doi.org/10.1016/j.anaerobe.2013.03.011
  43. Lai KP, Chung YT, Li R, Wan HT, Wong CK. Bisphenol A alters gut microbiome: Comparative metagenomics analysis. Environ Pollut 2016;218:923-30. https://doi.org/10.1016/j.envpol.2016.08.039
  44. Islam KB, Fukiya S, Hagio M, Fujii N, Ishizuka S, Ooka T, et al. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 2011;141:1773-81. https://doi.org/10.1053/j.gastro.2011.07.046
  45. Day AS, Lopez RN. Exclusive enteral nutrition in children with Crohn's disease. World J Gastroenterol 2015;21:6809-16. https://doi.org/10.3748/wjg.v21.i22.6809
  46. Swaminath A, Feathers A, Ananthakrishnan AN, Falzon L, Li Ferry S. Systematic review with meta-analysis: enteral nutrition therapy for the induction of remission in paediatric Crohn's disease. Aliment Pharmacol Ther 2017;46:645-56. https://doi.org/10.1111/apt.14253
  47. Ruemmele FM, Veres G, Kolho KL, Griffiths A, Levine A, Escher JC, et al. Consensus guidelines of ECCO/ESPGHAN on the medical management of pediatric Crohn's disease. J Crohns Colitis 2014;8:1179-207. https://doi.org/10.1016/j.crohns.2014.04.005
  48. Ashton JJ, Gavin J, Beattie RM. Exclusive enteral nutrition in Crohn's disease: Evidence and practicalities. Clin Nutr 2019;38:80-9. https://doi.org/10.1016/j.clnu.2018.01.020
  49. de Bie C, Kindermann A, Escher J. Use of exclusive enteral nutrition in paediatric Crohn's disease in The Netherlands. J Crohns Colitis 2013;7:263-70. https://doi.org/10.1016/j.crohns.2012.07.001
  50. Damas OM, Garces L, Abreu MT. Diet as adjunctive treatment for inflammatory bowel disease: review and update of the latest literature. Curr Treat Options Gastroenterol 2019;17:313-25. https://doi.org/10.1007/s11938-019-00231-8
  51. Gunasekeera V, Mendall MA, Chan D, Kumar D. Treatment of Crohn's disease with an IgG4-guided exclusion diet: a randomized controlled trial. Dig Dis Sci 2016;61:1148-57. https://doi.org/10.1007/s10620-015-3987-z
  52. Olendzki BC, Silverstein TD, Persuitte GM, Ma Y, Baldwin KR, Cave D. An anti-inflammatory diet as treatment for inflammatory bowel disease: a case series report. Nutr J 2014;13:5. https://doi.org/10.1186/1475-2891-13-5
  53. Sigall-Boneh R, Pfeffer-Gik T, Segal I, Zangen T, Boaz M, Levine A. Partial enteral nutrition with a Crohn's disease exclusion diet is effective for induction of remission in children and young adults with Crohn's disease. Inflamm Bowel Dis 2014;20:1353-60. https://doi.org/10.1097/MIB.0000000000000110
  54. Svolos V, Hansen R, Nichols B, Quince C, Ijaz UZ, Papadopoulou RT, et al. Treatment of active Crohn's disease with an ordinary food-based diet that replicates exclusive enteral nutrition. Gastroenterology 2019;156:1354-67.e6. https://doi.org/10.1053/j.gastro.2018.12.002
  55. Obih C, Wahbeh G, Lee D, Braly K, Giefer M, Shaffer ML, et al. Specific carbohydrate diet for pediatric inflammatory bowel disease in clinical practice within an academic IBD center. Nutrition 2016;32:418-25. https://doi.org/10.1016/j.nut.2015.08.025
  56. Cohen SA, Gold BD, Oliva S, Lewis J, Stallworth A, Koch B, et al. Clinical and mucosal improvement with specific carbohydrate diet in pediatric Crohn disease. J Pediatr Gastroenterol Nutr 2014;59:516-21. https://doi.org/10.1097/MPG.0000000000000449
  57. Suskind DL, Wahbeh G, Cohen SA, Damman CJ, Klein J, Braly K, et al. Patients perceive clinical benefit with the specific carbohydrate diet for inflammatory bowel disease. Dig Dis Sci 2016;61:3255-60. https://doi.org/10.1007/s10620-016-4307-y
  58. Suskind DL, Wahbeh G, Gregory N, Vendettuoli H, Christie D. Nutritional therapy in pediatric Crohn disease: the specific carbohydrate diet. J Pediatr Gastroenterol Nutr 2014;58:87-91. https://doi.org/10.1097/MPG.0000000000000103
  59. Rajendran N, Kumar D. Food-specific IgG4-guided exclusion diets improve symptoms in Crohn's disease: a pilot study. Colorectal Dis 2011;13:1009-13. https://doi.org/10.1111/j.1463-1318.2010.02373.x
  60. Zhan YL, Zhan YA, Dai SX. Is a low FODMAP diet beneficial for patients with inflammatory bowel disease? A meta-analysis and systematic review. Clin Nutr 2018;37:123-9. https://doi.org/10.1016/j.clnu.2017.05.019
  61. Miele E, Shamir R, Aloi M, Assa A, Braegger C, Bronsky J, et al. Nutrition in pediatric inflammatory bowel disease: a position paper on behalf of the porto inflammatory bowel disease group of the European Society of Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr 2018;66:687-708. https://doi.org/10.1097/MPG.0000000000001896
  62. Petrof EO, Kojima K, Ropeleski MJ, Musch MW, Tao Y, De Simone C, et al. Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 2004;127:1474-87. https://doi.org/10.1053/j.gastro.2004.09.001
  63. McCarthy J, O'Mahony L, O'Callaghan L, Sheil B, Vaughan EE, Fitzsimons N, et al. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 2003;52:975-80. https://doi.org/10.1136/gut.52.7.975
  64. O'Mahony C, Scully P, O'Mahony D, Murphy S, O'Brien F, Lyons A, et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 2008;4:e1000112. https://doi.org/10.1371/journal.ppat.1000112
  65. Vindigni SM, Zisman TL, Suskind DL, Damman CJ. The intestinal microbiome, barrier function, and immune system in inflammatory bowel disease: a tripartite pathophysiological circuit with implications for new therapeutic directions. Therap Adv Gastroenterol 2016;9:606-25. https://doi.org/10.1177/1756283X16644242
  66. Miele E, Pascarella F, Giannetti E, Quaglietta L, Baldassano RN, Staiano A. Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol 2009;104:437-43. https://doi.org/10.1038/ajg.2008.118
  67. Tursi A, Brandimarte G, Papa A, Giglio A, Elisei W, Giorgetti GM, et al. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol 2010;105:2218-27. https://doi.org/10.1038/ajg.2010.218
  68. Wehkamp J, Harder J, Wehkamp K, Wehkamp-von Meissner B, Schlee M, Enders C, et al. NF-kappaB- and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium. Infect Immun 2004;72:5750-8. https://doi.org/10.1128/IAI.72.10.5750-5758.2004
  69. Schultz M. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1012-8. https://doi.org/10.1002/ibd.20377
  70. Malchow HA. Crohn's disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn's disease? J Clin Gastroenterol 1997;25:653-8. https://doi.org/10.1097/00004836-199712000-00021
  71. Derwa Y, Gracie DJ, Hamlin PJ, Ford AC. Systematic review with metaanalysis: the efficacy of probiotics in inflammatory bowel disease. Aliment Pharmacol Ther 2017;46:389-400. https://doi.org/10.1111/apt.14203
  72. Martin R, Miquel S, Chain F, Natividad JM, Jury J, Lu J, et al. Faecalibacterium prausnitzii prevents physiological damages in a chronic low-grade inflammation murine model. BMC Microbiol 2015;15:67. https://doi.org/10.1186/s12866-015-0400-1
  73. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011;332:974-7. https://doi.org/10.1126/science.1206095
  74. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 2008;105:16731-6. https://doi.org/10.1073/pnas.0804812105
  75. Walker AW, Duncan SH, McWilliam Leitch EC, Child MW, Flint HJ. pH and peptide supply can radically alter bacterial populations and shortchain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 2005;71:3692-700. https://doi.org/10.1128/AEM.71.7.3692-3700.2005
  76. Rasmussen HE, Hamaker BR. Prebiotics and Inflammatory Bowel Disease. Gastroenterol Clin North Am 2017;46:783-795. https://doi.org/10.1016/j.gtc.2017.08.004
  77. Videla S, Vilaseca J, Antolin M, Garcia-Lafuente A, Guarner F, Crespo E, et al. Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat. Am J Gastroenterol 2001;96:1486-93. https://doi.org/10.1016/S0002-9270(01)02365-6
  78. Lara-Villoslada F, Debras E, Nieto A, Concha A, Galvez J, Lopez-Huertas E, et al. Oligosaccharides isolated from goat milk reduce intestinal inflammation in a rat model of dextran sodium sulfate-induced colitis. Clin Nutr 2006;25:477-88. https://doi.org/10.1016/j.clnu.2005.11.004
  79. Daddaoua A, Puerta V, Requena P, Martinez-Ferez A, Guadix E, de Medina FS, et al. Goat milk oligosaccharides are anti-inflammatory in rats with hapten-induced colitis. J Nutr 2006;136:672-6. https://doi.org/10.1093/jn/136.3.672
  80. Hoentjen F, Welling GW, Harmsen HJ, Zhang X, Snart J, Tannock GW, et al. Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm Bowel Dis 2005;11:977-85. https://doi.org/10.1097/01.MIB.0000183421.02316.d5
  81. Lindsay JO, Whelan K, Stagg AJ, Gobin P, Al-Hassi HO, Rayment N, et al. Clinical, microbiological, and immunological effects of fructooligosaccharide in patients with Crohn's disease. Gut 2006;55:348-55. https://doi.org/10.1136/gut.2005.074971
  82. Benjamin JL, Hedin CR, Koutsoumpas A, Ng SC, McCarthy NE, Hart AL, et al. Randomised, double-blind, placebo-controlled trial of fructooligosaccharides in active Crohn's disease. Gut 2011;60:923-9. https://doi.org/10.1136/gut.2010.232025
  83. Kanauchi O, Mitsuyama K, Homma T, Takahama K, Fujiyama Y, Andoh A, et al. Treatment of ulcerative colitis patients by long-term administration of germinated barley foodstuff: multi-center open trial. Int J Mol Med 2003;12:701-4.
  84. Hallert C, Kaldma M, Petersson BG. Ispaghula husk may relieve gastrointestinal symptoms in ulcerative colitis in remission. Scand J Gastroenterol 1991;26:747-50. https://doi.org/10.3109/00365529108998594
  85. Furrie E, Macfarlane S, Kennedy A, Cummings JH, Walsh SV, O'neil DA, et al. Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut 2005;54:242-9. https://doi.org/10.1136/gut.2004.044834
  86. Welters CF, Heineman E, Thunnissen FB, van den Bogaard AE, Soeters PB, Baeten CG. Effect of dietary inulin supplementation on inflammation of pouch mucosa in patients with an ileal pouch-anal anastomosis. Dis Colon Rectum 2002;45:621-7. https://doi.org/10.1007/s10350-004-6257-2
  87. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 1958;44:854-9.
  88. Paramsothy S, Paramsothy R, Rubin DT, Kamm MA, Kaakoush NO, Mitchell HM, et al. Faecal microbiota transplantation for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis 2017;11:1180-99. https://doi.org/10.1093/ecco-jcc/jjx063
  89. Singh S, Feuerstein JD, Binion DG, Tremaine WJ. AGA technical review on the management of mild-to-moderate ulcerative colitis. Gastroenterology 2019;156:769-808.e29. https://doi.org/10.1053/j.gastro.2018.12.008
  90. Kunde S, Pham A, Bonczyk S, Crumb T, Duba M, Conrad H Jr, et al. Safety, tolerability, and clinical response after fecal transplantation in children and young adults with ulcerative colitis. J Pediatr Gastroenterol Nutr 2013;56:597-601. https://doi.org/10.1097/MPG.0b013e318292fa0d
  91. Kellermayer R, Nagy-Szakal D, Harris RA, Luna RA, Pitashny M, Schady D, et al. Serial fecal microbiota transplantation alters mucosal gene expression in pediatric ulcerative colitis. Am J Gastroenterol 2015;110:604-6. https://doi.org/10.1038/ajg.2015.19
  92. Vandenplas Y, Veereman G, van der Werff Ten Bosch J, Goossens A, Pierard D, Samsom JN, et al. Fecal microbial transplantation in earlyonset colitis: caution advised. J Pediatr Gastroenterol Nutr 2015;61:e12-4.
  93. Suskind DL, Singh N, Nielson H, Wahbeh G. Fecal microbial transplant via nasogastric tube for active pediatric ulcerative colitis. J Pediatr Gastroenterol Nutr 2015;60:27-9. https://doi.org/10.1097/MPG.0000000000000544
  94. Shimizu H, Arai K, Abe J, Nakabayashi K, Yoshioka T, Hosoi K, et al. Repeated fecal microbiota transplantation in a child with ulcerative colitis. Pediatr Int 2016;58:781-5. https://doi.org/10.1111/ped.12967
  95. Pai N PJ, Lee C. A randomized, placebo-controlled trial of fecal microbial transplantation for pediatric ulcerative colitis [Pedifetch Trial]. J Pediatr Gastroenterol Nutr 2016;63:S79-80.
  96. Kumagai H, Yokoyama K, Imagawa T, Inoue S, Tulyeu J, Tanaka M, et al. Failure of fecal microbiota transplantation in a three-year-old child with severe refractory ulcerative colitis. Pediatr Gastroenterol Hepatol Nutr 2016;19:214-20. https://doi.org/10.5223/pghn.2016.19.3.214
  97. Karolewska-Bochenek K, Grzesiowski P, Banaszkiewicz A, Gawronska A, Kotowska M, Dziekiewicz M, et al. A two-week fecal microbiota transplantation course in pediatric patients with inflammatory bowel disease. Adv Exp Med Biol 2018;1047:81-7.
  98. Goyal A, Yeh A, Bush BR, Firek BA, Siebold LM, Rogers MB, et al. Safety, clinical response, and microbiome findings following fecal microbiota transplant in children with inflammatory bowel disease. Inflamm Bowel Dis 2018;24:410-21. https://doi.org/10.1093/ibd/izx035
  99. Yodoshi T, Hurt TL. Fecal microbiota transplantation to patients with refractory very early onset ulcerative colitis. Pediatr Gastroenterol Hepatol Nutr 2018;21:355-60. https://doi.org/10.5223/pghn.2018.21.4.355
  100. Suskind DL, Brittnacher MJ, Wahbeh G, Shaffer ML, Hayden HS, Qin X, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn's disease. Inflamm Bowel Dis 2015;21:556-63. https://doi.org/10.1097/MIB.0000000000000307
  101. Baxter M, Colville A. Adverse events in faecal microbiota transplant: a review of the literature. J Hosp Infect 2016;92:117-27. https://doi.org/10.1016/j.jhin.2015.10.024
  102. Narula N, Kassam Z, Yuan Y, Colombel JF, Ponsioen C, Reinisch W, et al. Systematic review and meta-analysis: fecal microbiota transplantation for treatment of active ulcerative colitis. Inflamm Bowel Dis 2017;23:1702-9. https://doi.org/10.1097/MIB.0000000000001228

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