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Inflammatory Bowel Disease

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The Microbiome in Rheumatic Diseases and Infection

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Abstract

The inflammatory bowel diseases (IBD) are characterized by chronic intestinal inflammation of unknown etiology. There are two main categories of IBD, ulcerative colitis (UC) and Crohn disease (CD), which are differentiated on the basis of pathologic features. The prevalence in the United States of both forms of IBD appears to be about 200 per 100,000 people (Kappelman et al., Clin Gastroenterol Hepatol 5(12):1424–1429, 2007), and there is geographic variation around the world as well as temporal variation (de Mesquita et al., Dig Liver Dis 40(1):3–11, 2008). Both forms of IBD can result in substantial impairments in quality of life, with complications including but not limited to malabsorption, intestinal adhesions and perforation, infections, and cancer (Kappelman et al., Clin Gastroenterol Hepatol 5(12):1424–1429, 2007). Although the pathogenesis is unclear, factors involving the human intestinal microbiota have long been suspected (Seneca and Henderson, Gastroenterology 15(1 1):34–39, 1950). Indeed, the role of the intestinal microbiota in IBD has been studied in far more depth in this condition than in any other systemic condition. While no solid consensus is observed among the studies, they coincide in the loss of diversity and changes in specific taxa. This chapter will review data on the contents of the microbiota, as well as the relationship between the microbiota and immunity, and the potential for treating IBD through manipulation of the microbiota.

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Abbreviations

Ahr:

Aryl hydrocarbon receptor

ASCA:

Anti-Saccharomyces cerevisiae antibodies

CD:

Crohn disease

DSS:

Dextran sulfate sodium

EEN:

Exclusive enteral nutrition

FMT:

Fecal microbial transplantation

FXR:

Farnesoid X receptor

IBD:

Inflammatory bowel disease

IL:

Interleukin

ILC:

Innate lymphoid cells

IPA:

Indolepropionic acid

MyD88:

Myeloid differentiation primary response 88

PSA:

Polysaccharide A

SCFA:

Short-chain fatty acids

SFB:

Segmented filamentous bacteria

SpA:

Spondyloarthritis

Treg:

Regulatory T cells

TLR:

Toll-like receptor

TNF:

Tumor necrosis factor

UC:

Ulcerative colitis

References

  1. Kappelman MD, Rifas-Shiman SL, Kleinman K, Ollendorf D, Bousvaros A, Grand RJ, et al. The prevalence and geographic distribution of Crohn’s disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol. 2007;5(12):1424–9.

    Article  PubMed  Google Scholar 

  2. de Mesquita MB, Civitelli F, Levine A. Epidemiology, genes and inflammatory bowel diseases in childhood. Dig Liver Dis. 2008;40(1):3–11.

    Article  PubMed  CAS  Google Scholar 

  3. Seneca H, Henderson E. Normal intestinal bacteria in ulcerative colitis. Gastroenterology. 1950;15(1 1):34–9.

    PubMed  CAS  Google Scholar 

  4. Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity. 2014;40(6):833–42.

    Article  PubMed  CAS  Google Scholar 

  5. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491(7422):119–24.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Ubeda C, Lipuma L, Gobourne A, Viale A, Leiner I, Equinda M, et al. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J Exp Med. 2012;209(8):1445–56.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K, Doi Y, et al. Foxp3(+) T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity. 2014;41(1):152–65.

    Article  PubMed  CAS  Google Scholar 

  8. Kawamoto S, Tran TH, Maruya M, Suzuki K, Doi Y, Tsutsui Y, et al. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science. 2012;336(6080):485–9.

    Article  PubMed  CAS  Google Scholar 

  9. Rankin LC, Girard-Madoux MJ, Seillet C, Mielke LA, Kerdiles Y, Fenis A, et al. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat Immunol. 2016;17(2):179–86.

    Article  PubMed  CAS  Google Scholar 

  10. Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature. 2016;535(7610):65–74.

    Article  PubMed  CAS  Google Scholar 

  11. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, et al. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science. 2011;334(6053):255–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Nakahashi-Oda C, Udayanga KG, Nakamura Y, Nakazawa Y, Totsuka N, Miki H, et al. Apoptotic epithelial cells control the abundance of Treg cells at barrier surfaces. Nat Immunol. 2016;17(4):441–50.

    Article  PubMed  CAS  Google Scholar 

  13. Ahern PP, Izcue A, Maloy KJ, Powrie F. The interleukin-23 axis in intestinal inflammation. Immunol Rev. 2008;226:147–59.

    Article  PubMed  Google Scholar 

  14. Abraham C, Cho JH. IL-23 and autoimmunity: new insights into the pathogenesis of inflammatory bowel disease. Annu Rev Med. 2009;60:97–110.

    Article  PubMed  CAS  Google Scholar 

  15. Mukherjee S, Hooper LV. Antimicrobial defense of the intestine. Immunity. 2015;42(1):28–39.

    Article  PubMed  CAS  Google Scholar 

  16. Goodlad RA, Ratcliffe B, Fordham JP, Wright NA. Does dietary fibre stimulate intestinal epithelial cell proliferation in germ free rats? Gut. 1989;30(6):820–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Fukata M, Michelsen KS, Eri R, Thomas LS, Hu B, Lukasek K, et al. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am J Physiol Gastrointest Liver Physiol. 2005;288(5):G1055–65.

    Article  PubMed  CAS  Google Scholar 

  18. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229–41.

    Article  PubMed  CAS  Google Scholar 

  19. Silva MA, Jury J, Porras M, Vergara P, Perdue MH. Intestinal epithelial barrier dysfunction and dendritic cell redistribution during early stages of inflammation in the rat: role for TLR-2 and -4 blockage. Inflamm Bowel Dis. 2008;14(5):632–44.

    Article  PubMed  Google Scholar 

  20. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461(7268):1282–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Hernández-Chirlaque C, Aranda CJ, Ocón B, Capitán-Cañadas F, Ortega-González M, Carrero JJ, et al. Germ-free and antibiotic-treated mice are highly susceptible to epithelial injury in DSS colitis. J Crohn’s Colitis. 2016;10(11):1324–35.

    Article  Google Scholar 

  22. Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Investig. 2013;123(2):700–11.

    PubMed  PubMed Central  CAS  Google Scholar 

  23. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13(9):R79.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, et al. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol. 2004;5(1):104–12.

    Article  PubMed  CAS  Google Scholar 

  25. Hoffmann TW, Pham H-P, Bridonneau C, Aubry C, Lamas B, Martin-Gallausiaux C, et al. Microorganisms linked to inflammatory bowel disease-associated dysbiosis differentially impact host physiology in gnotobiotic mice. ISME J. 2016;10(2):460–77.

    Article  PubMed  CAS  Google Scholar 

  26. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31(4):677–89.

    Article  PubMed  CAS  Google Scholar 

  27. Lecuyer E, Rakotobe S, Lengline-Garnier H, Lebreton C, Picard M, Juste C, et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity. 2014;40(4):608–20.

    Article  PubMed  CAS  Google Scholar 

  28. Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y, Narushima S, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell. 2015;163(2):367–80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Jonsson H. Segmented filamentous bacteria in human ileostomy samples after high-fiber intake. FEMS Microbiol Lett. 2013;342(1):24–9.

    Article  PubMed  CAS  Google Scholar 

  30. Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ, Targan SR, et al. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Investig. 2004;113(9):1296–306.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Targan SR, Landers CJ, Yang H, Lodes MJ, Cong Y, Papadakis KA, et al. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn’s disease. Gastroenterology. 2005;128(7):2020–8.

    Article  PubMed  CAS  Google Scholar 

  32. Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, Datsi A, et al. Circulating and tissue-resident CD4(+) T cells with reactivity to intestinal Microbiota are abundant in healthy individuals and function is altered during inflammation. Gastroenterology. 2017;153(5):1320–37.e16.

    Article  PubMed  CAS  Google Scholar 

  33. Feng T, Qin H, Wang L, Benveniste EN, Elson CO, Cong Y. Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production. J Immunol. 2011;186(11):6313–8.

    Article  PubMed  CAS  Google Scholar 

  34. 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(43):16731–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Smelt MJ, de Haan BJ, Bron PA, van Swam I, Meijerink M, Wells JM, et al. The impact of lactobacillus plantarum WCFS1 teichoic acid D-alanylation on the generation of effector and regulatory T-cells in healthy mice. PLoS One. 2013;8(4):e63099.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Zakostelska Z, Kverka M, Klimesova K, Rossmann P, Mrazek J, Kopecny J, et al. Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS One. 2011;6(11):e27961.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Shen J, Zuo ZX, Mao AP. Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn’s disease, and pouchitis: meta-analysis of randomized controlled trials. Inflamm Bowel Dis. 2014;20(1):21–35.

    Article  PubMed  Google Scholar 

  38. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature. 2013;502(7469):96–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Macia L, Tan J, Vieira AT, Leach K, Stanley D, Luong S, et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat Commun. 2015;6:6734.

    Article  CAS  PubMed  Google Scholar 

  40. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446–50.

    Article  PubMed  CAS  Google Scholar 

  41. Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell. 2012;48(4):612–26.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, de Roos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014;111(6):2247–52.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40(1):128–39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 2013;17(2):225–35.

    Article  PubMed  CAS  Google Scholar 

  46. Joyce SA, MacSharry J, Casey PG, Kinsella M, Murphy EF, Shanahan F, et al. Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. Proc Natl Acad Sci U S A. 2014;111(20):7421–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Vavassori P, Mencarelli A, Renga B, Distrutti E, Fiorucci S. The bile acid receptor FXR is a modulator of intestinal innate immunity. J Immunol. 2009;183(10):6251–61.

    Article  PubMed  CAS  Google Scholar 

  48. Schubert K, Olde Damink SWM, von Bergen M, Schaap FG. Interactions between bile salts, gut microbiota, and hepatic innate immunity. Immunol Rev. 2017;279(1):23–35.

    Article  PubMed  CAS  Google Scholar 

  49. Gadaleta RM, van Erpecum KJ, Oldenburg B, Willemsen EC, Renooij W, Murzilli S, et al. Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease. Gut. 2011;60(4):463–72.

    Article  PubMed  CAS  Google Scholar 

  50. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, et al. Tryptophan Catabolites from Microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via Interleukin-22. Immunity. 2013;39(2):372–85.

    Article  PubMed  CAS  Google Scholar 

  51. Hashimoto T, Perlot T, Rehman A, Trichereau J, Ishiguro H, Paolino M, et al. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature. 2012;487(7408):477–81.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  52. Lanis JM, Alexeev EE, Curtis VF, Kitzenberg DA, Kao DJ, Battista KD, et al. Tryptophan metabolite activation of the aryl hydrocarbon receptor regulates IL-10 receptor expression on intestinal epithelia. Mucosal Immunol. 2017;10(5):1133–44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Lamas B, Richard ML, Leducq V, Pham HP, Michel ML, Da Costa G, et al. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med. 2016;22(6):598–605.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ, Higginbottom SK, et al. A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature. 2017;551(7682):648–52.

    PubMed  PubMed Central  CAS  Google Scholar 

  55. Walker AW, Sanderson JD, Churcher C, Parkes GC, Hudspith BN, Rayment N, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011;11:7.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Hansen R, Russell RK, Reiff C, Louis P, McIntosh F, Berry SH, et al. Microbiota of de-novo pediatric IBD: increased Faecalibacterium prausnitzii and reduced bacterial diversity in Crohn’s but not in ulcerative colitis. Am J Gastroenterol. 2012;107(12):1913–22.

    Article  PubMed  CAS  Google Scholar 

  57. Prideaux L, Kang S, Wagner J, Buckley M, Mahar JE, De Cruz P, et al. Impact of ethnicity, geography, and disease on the microbiota in health and inflammatory bowel disease. Inflamm Bowel Dis. 2013;19(13):2906–18.

    Article  PubMed  Google Scholar 

  58. Tong M, Li X, Wegener Parfrey L, Roth B, Ippoliti A, Wei B, et al. A modular organization of the human intestinal mucosal microbiota and its association with inflammatory bowel disease. PLoS One. 2013;8(11):e80702.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Chen L, Wang W, Zhou R, Ng SC, Li J, Huang M, et al. Characteristics of fecal and mucosa-associated microbiota in Chinese patients with inflammatory bowel disease. Medicine (Baltimore). 2014;93(8):e51.

    Article  CAS  Google Scholar 

  60. Perez-Brocal V, Garcia-Lopez R, Nos P, Beltran B, Moret I, Moya A. Metagenomic analysis of Crohn’s disease patients identifies changes in the Virome and Microbiome related to disease status and therapy, and detects potential interactions and biomarkers. Inflamm Bowel Dis. 2015;21(11):2515–32.

    Article  PubMed  Google Scholar 

  61. Quince C, Ijaz UZ, Loman N, Eren AM, Saulnier D, Russell J, et al. Extensive modulation of the fecal Metagenome in children with Crohn’s disease during exclusive enteral nutrition. Am J Gastroenterol. 2015;110(12):1718–29. quiz 30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Dunn KA, Moore-Connors J, MacIntyre B, Stadnyk AW, Thomas NA, Noble A, et al. Early changes in microbial community structure are associated with sustained remission after nutritional treatment of pediatric Crohn’s disease. Inflamm Bowel Dis. 2016;22(12):2853–62.

    Article  PubMed  Google Scholar 

  63. Hedin C, van der Gast CJ, Rogers GB, Cuthbertson L, McCartney S, Stagg AJ, et al. Siblings of patients with Crohn’s disease exhibit a biologically relevant dysbiosis in mucosal microbial metacommunities. Gut. 2016;65(6):944–53.

    Article  PubMed  CAS  Google Scholar 

  64. Hoarau G, Mukherjee PK, Gower-Rousseau C, Hager C, Chandra J, Retuerto MA, et al. Bacteriome and mycobiome interactions underscore microbial dysbiosis in familial Crohn’s disease. MBio. 2016;7(5):e01250–16.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Liguori G, Lamas B, Richard ML, Brandi G, da Costa G, Hoffmann TW, et al. Fungal dysbiosis in mucosa-associated microbiota of Crohn’s disease patients. J Crohns Colitis. 2016;10(3):296–305.

    Article  PubMed  Google Scholar 

  66. Mar JS, LaMere BJ, Lin DL, Levan S, Nazareth M, Mahadevan U, et al. Disease severity and immune activity relate to distinct interkingdom gut microbiome states in ethnically distinct ulcerative colitis patients. MBio. 2016;7(4):e01072–16.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Shaw KA, Bertha M, Hofmekler T, Chopra P, Vatanen T, Srivatsa A, et al. Dysbiosis, inflammation, and response to treatment: a longitudinal study of pediatric subjects with newly diagnosed inflammatory bowel disease. Genome Med. 2016;8(1):75.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2016;66(6):1039–48.

    Article  PubMed  CAS  Google Scholar 

  69. Ijaz UZ, Quince C, Hanske L, Loman N, Calus ST, Bertz M, et al. The distinct features of microbial “dysbiosis” of Crohn’s disease do not occur to the same extent in their unaffected, genetically-linked kindred. PLoS One. 2017;12(2):e0172605.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Knoll RL, Forslund K, Kultima JR, Meyer CU, Kullmer U, Sunagawa S, et al. Gut microbiota differs between children with Inflammatory Bowel Disease and healthy siblings in taxonomic and functional composition—a metagenomic analysis. Am J Physiol Gastrointest Liver Physiol. 2016;312(4):G327–39. ajpgi 00293 2016.

    Article  PubMed  Google Scholar 

  71. Pascal V, Pozuelo M, Borruel N, Casellas F, Campos D, Santiago A, et al. A microbial signature for Crohn’s disease. Gut. 2017;66(5):813–22.

    Article  PubMed  CAS  Google Scholar 

  72. Michail S, Durbin M, Turner D, Griffiths AM, Mack DR, Hyams J, et al. Alterations in the gut microbiome of children with severe ulcerative colitis. Inflamm Bowel Dis. 2012;18(10):1799–808.

    Article  PubMed  Google Scholar 

  73. Kang S, Denman SE, Morrison M, Yu Z, Dore J, Leclerc M, et al. Dysbiosis of fecal microbiota in Crohn’s disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis. 2010;16(12):2034–42.

    Article  PubMed  Google Scholar 

  74. Erickson AR, Cantarel BL, Lamendella R, Darzi Y, Mongodin EF, Pan C, et al. Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn’s disease. PLoS One. 2012;7(11):e49138.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. De Preter V, Machiels K, Joossens M, Arijs I, Matthys C, Vermeire S, et al. Faecal metabolite profiling identifies medium-chain fatty acids as discriminating compounds in IBD. Gut. 2015;64(3):447–58.

    Article  PubMed  CAS  Google Scholar 

  76. Bradley PH, Pollard KS. Proteobacteria explain significant functional variability in the human gut microbiome. Microbiome. 2017;5(1):36.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Nguyen GC, Kaplan GG, Harris ML, Brant SR. A national survey of the prevalence and impact of Clostridium difficile infection among hospitalized inflammatory bowel disease patients. Am J Gastroenterol. 2008;103(6):1443–50.

    Article  PubMed  Google Scholar 

  78. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010;139(6):1844–54.e1.

    Article  PubMed  Google Scholar 

  79. 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(3):382–92.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Kolho KL, Korpela K, Jaakkola T, Pichai MV, Zoetendal EG, Salonen A, et al. Fecal microbiota in pediatric inflammatory bowel disease and its relation to inflammation. Am J Gastroenterol. 2015;110(6):921–30.

    Article  PubMed  Google Scholar 

  81. Naftali T, Reshef L, Kovacs A, Porat R, Amir I, Konikoff FM, et al. Distinct microbiotas are associated with ileum-restricted and Colon-involving Crohn’s disease. Inflamm Bowel Dis. 2016;22(2):293–302.

    Article  PubMed  Google Scholar 

  82. He Q, Gao Y, Jie Z, Yu X, Laursen JM, Xiao L, et al. Two distinct metacommunities characterize the gut microbiota in Crohn’s disease patients. Gigascience. 2017;6(7):1–11.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Assa A, Butcher J, Li J, Elkadri A, Sherman PM, Muise AM, et al. Mucosa-associated ileal microbiota in new-onset pediatric Crohn’s disease. Inflamm Bowel Dis. 2016;22(7):1533–9.

    Article  PubMed  Google Scholar 

  84. Tedjo DI, Smolinska A, Savelkoul PH, Masclee AA, van Schooten FJ, Pierik MJ, et al. The fecal microbiota as a biomarker for disease activity in Crohn’s disease. Sci Rep. 2016;6:35216.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. De Cruz P, Kang S, Wagner J, Buckley M, Sim WH, Prideaux L, et al. Association between specific mucosa-associated microbiota in Crohn’s disease at the time of resection and subsequent disease recurrence: a pilot study. J Gastroenterol Hepatol. 2015;30(2):268–78.

    Article  PubMed  Google Scholar 

  86. Qiu X, Zhang M, Yang X, Hong N, Yu C. Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J Crohns Colitis. 2013;7(11):e558–68.

    Article  PubMed  Google Scholar 

  87. Rossi O, van Berkel LA, Chain F, Tanweer Khan M, Taverne N, Sokol H, et al. Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci Rep. 2016;6:18507.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Kellermayer R, Mir SA, Nagy-Szakal D, Cox SB, Dowd SE, Kaplan JL, et al. Microbiota separation and C-reactive protein elevation in treatment-naive pediatric granulomatous Crohn disease. J Pediatr Gastroenterol Nutr. 2012;55(3):243–50.

    Article  PubMed  CAS  Google Scholar 

  89. Tyler AD, Knox N, Kabakchiev B, Milgrom R, Kirsch R, Cohen Z, et al. Characterization of the gut-associated microbiome in inflammatory pouch complications following ileal pouch-anal anastomosis. PLoS One. 2013;8(9):e66934.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Shah R, Cope JL, Nagy-Szakal D, Dowd S, Versalovic J, Hollister EB, et al. Composition and function of the pediatric colonic mucosal microbiome in untreated patients with ulcerative colitis. Gut Microbes. 2016;7(5):384–96.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–45.

    Article  PubMed  CAS  Google Scholar 

  92. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.

    Article  CAS  Google Scholar 

  93. Louis P, Young P, Holtrop G, Flint HJ. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol. 2010;12(2):304–14.

    Article  PubMed  CAS  Google Scholar 

  94. Morrison DJ, Mackay WG, Edwards CA, Preston T, Dodson B, Weaver LT. Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Br J Nutr. 2006;96(3):570–7.

    PubMed  CAS  Google Scholar 

  95. Scott KP, Martin JC, Duncan SH, Flint HJ. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol Ecol. 2014;87(1):30–40.

    Article  PubMed  CAS  Google Scholar 

  96. Rios-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilan CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569–73.

    Article  PubMed  CAS  Google Scholar 

  98. Marchesi JR, Holmes E, Khan F, Kochhar S, Scanlan P, Shanahan F, et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res. 2007;6(2):546–51.

    Article  PubMed  CAS  Google Scholar 

  99. Le Gall G, Noor SO, Ridgway K, Scovell L, Jamieson C, Johnson IT, et al. Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome. J Proteome Res. 2011;10(9):4208–18.

    Article  PubMed  CAS  Google Scholar 

  100. Dunn KA, Moore-Connors J, MacIntyre B, Stadnyk A, Thomas NA, Noble A, et al. The gut microbiome of pediatric Crohn’s disease patients differs from healthy controls in genes that can influence the balance between a healthy and dysregulated immune response. Inflamm Bowel Dis. 2016;22(11):2607–18.

    Article  PubMed  Google Scholar 

  101. Lepage P, Hasler R, Spehlmann ME, Rehman A, Zvirbliene A, Begun A, et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology. 2011;141(1):227–36.

    Article  PubMed  Google Scholar 

  102. Takahashi K, Nishida A, Fujimoto T, Fujii M, Shioya M, Imaeda H, et al. Reduced abundance of butyrate-producing bacteria species in the fecal microbial community in Crohn’s disease. Digestion. 2016;93(1):59–65.

    Article  PubMed  CAS  Google Scholar 

  103. Zhou Y, Zhi F. Lower level of bacteroides in the gut microbiota is associated with inflammatory bowel disease: a meta-analysis. Biomed Res Int. 2016;2016:5828959.

    PubMed  PubMed Central  Google Scholar 

  104. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453(7195):620–5.

    Article  PubMed  CAS  Google Scholar 

  105. 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(6032):974–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010;107(27):12204–9.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Telesford KM, Yan W, Ochoa-Reparaz J, Pant A, Kircher C, Christy MA, et al. A commensal symbiotic factor derived from Bacteroides fragilis promotes human CD39(+)Foxp3(+) T cells and Treg function. Gut Microbes. 2015;6(4):234–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Vaahtovuo J, Munukka E, Korkeamaki M, Luukkainen R, Toivanen P. Fecal microbiota in early rheumatoid arthritis. J Rheumatol. 2008;35(8):1500–5.

    PubMed  CAS  Google Scholar 

  110. Tito RY, Cypers H, Joossens M, Varkas G, Van Praet L, Glorieus E, et al. Brief report: dialister as a microbial marker of disease activity in spondyloarthritis. Arthritis Rheumatol. 2017;69(1):114–21.

    Article  PubMed  CAS  Google Scholar 

  111. Nwosu FC, Thorkildsen LT, Avershina E, Ricanek P, Perminow G, Brackmann S, et al. Age-dependent fecal bacterial correlation to inflammatory bowel disease for newly diagnosed untreated children. Gastroenterol Res Pract. 2013;2013:302398.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Stoll ML, Kumar R, Morrow CD, Lefkowitz EJ, Cui X, Genin A, et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res Ther. 2014;16(6):486.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Tejesvi MV, Arvonen M, Kangas SM, Keskitalo PL, Pirttila AM, Karttunen TJ, et al. Faecal microbiome in new-onset juvenile idiopathic arthritis. Eur J Clin Microbiol Infect Dis. 2016;35(3):363–70.

    Article  PubMed  CAS  Google Scholar 

  114. Aggarwal A, Sarangi AN, Gaur P, Shukla A, Aggarwal R. Gut microbiome in children with enthesitis-related arthritis in a developing country and the effect of probiotic administration. Clin Exp Immunol. 2017;187(3):480–9.

    Article  PubMed  CAS  Google Scholar 

  115. Giongo A, Gano KA, Crabb DB, Mukherjee N, Novelo LL, Casella G, et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 2011;5(1):82–91.

    Article  PubMed  CAS  Google Scholar 

  116. Vatanen T, Kostic AD, d’Hennezel E, Siljander H, Franzosa EA, Yassour M, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016;165(4):842–53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Papa E, Docktor M, Smillie C, Weber S, Preheim SP, Gevers D, et al. Non-invasive mapping of the gastrointestinal microbiota identifies children with inflammatory bowel disease. PLoS One. 2012;7(6):e39242.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Lavelle A, Lennon G, O’Sullivan O, Docherty N, Balfe A, Maguire A, et al. Spatial variation of the colonic microbiota in patients with ulcerative colitis and control volunteers. Gut. 2015;64(10):1553–61.

    Article  PubMed  CAS  Google Scholar 

  119. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54(Pt 5):1469–76.

    Article  PubMed  CAS  Google Scholar 

  120. Woting A, Blaut M. The intestinal microbiota in metabolic disease. Forum Nutr. 2016;8(4):202.

    Google Scholar 

  121. Asquith MJ, Stauffer P, Davin S, Mitchell C, Lin P, Rosenbaum JT. Perturbed mucosal immunity and dysbiosis accompany clinical disease in a rat model of spondyloarthritis. Arthritis Rheumatol. 2016;68(9):2151–62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  122. Vaile JH, Meddings JB, Yacyshyn BR, Russell AS, Maksymowych WP. Bowel permeability and CD45RO expression on circulating CD20+ B cells in patients with ankylosing spondylitis and their relatives. J Rheumatol. 1999;26(1):128–35.

    PubMed  CAS  Google Scholar 

  123. Munkholm P, Langholz E, Hollander D, Thornberg K, Orholm M, Katz KD, et al. Intestinal permeability in patients with Crohn’s disease and ulcerative colitis and their first degree relatives. Gut. 1994;35(1):68–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Dorofeyev AE, Vasilenko IV, Rassokhina OA, Kondratiuk RB. Mucosal barrier in ulcerative colitis and Crohn’s disease. Gastroenterol Res Pract. 2013;2013:431231.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. Rey FE, Gonzalez MD, Cheng J, Wu M, Ahern PP, Gordon JI. Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc Natl Acad Sci U S A. 2013;110(33):13582–7.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Pitcher MC, Beatty ER, Harris RM, Waring RH, Cummings JH. Sulfur metabolism in ulcerative colitis: investigation of detoxification enzymes in peripheral blood. Dig Dis Sci. 1998;43(9):2080–5.

    Article  PubMed  CAS  Google Scholar 

  127. Ijssennagger N, Belzer C, Hooiveld GJ, Dekker J, van Mil SW, Muller M, et al. Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon. Proc Natl Acad Sci U S A. 2015;112(32):10038–43.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Wang W, Jovel J, Halloran B, Wine E, Patterson J, Ford G, et al. Metagenomic analysis of microbiome in colon tissue from subjects with inflammatory bowel diseases reveals interplay of viruses and bacteria. Inflamm Bowel Dis. 2015;21(6):1419–27.

    PubMed  Google Scholar 

  129. Chassaing B, Rolhion N, de Vallee A, Salim SY, Prorok-Hamon M, Neut C, et al. Crohn disease—associated adherent-invasive E. coli bacteria target mouse and human Peyer’s patches via long polar fimbriae. J Clin Investig. 2011;121(3):966–75.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. Bucker R, Schulz E, Gunzel D, Bojarski C, Lee IF, John LJ, et al. α-Haemolysin of Escherichia coli in IBD: a potentiator of inflammatory activity in the colon. Gut. 2014;63(12):1893–901.

    Article  PubMed  CAS  Google Scholar 

  131. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2(2):119–29.

    Article  PubMed  CAS  Google Scholar 

  132. He F, Morita H, Ouwehand AC, Hosoda M, Hiramatsu M, Kurisaki J, et al. Stimulation of the secretion of pro-inflammatory cytokines by Bifidobacterium strains. Microbiol Immunol. 2002;46(11):781–5.

    Article  PubMed  CAS  Google Scholar 

  133. Medina M, Izquierdo E, Ennahar S, Sanz Y. Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol. 2007;150(3):531–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  134. Elian SD, Souza EL, Vieira AT, Teixeira MM, Arantes RM, Nicoli JR, et al. Bifidobacterium longum subsp. infantis BB-02 attenuates acute murine experimental model of inflammatory bowel disease. Benefic Microbes. 2015;6(3):277–86.

    Article  CAS  Google Scholar 

  135. Chehoud C, Albenberg LG, Judge C, Hoffmann C, Grunberg S, Bittinger K, et al. Fungal signature in the gut microbiota of pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(8):1948–56.

    Article  PubMed  Google Scholar 

  136. Israeli E, Grotto I, Gilburd B, Balicer RD, Goldin E, Wiik A, et al. Anti-Saccharomyces cerevisiae and antineutrophil cytoplasmic antibodies as predictors of inflammatory bowel disease. Gut. 2005;54(9):1232–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012;336(6086):1314–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Hansen JJ, Sartor RB. Therapeutic manipulation of the microbiome in IBD: current results and future approaches. Curr Treat Options Gastroenterol. 2015;13(1):105–20.

    Article  PubMed  PubMed Central  Google Scholar 

  139. Lewis JD, Abreu MT. Diet as a trigger or therapy for inflammatory bowel diseases. Gastroenterology. 2017;152(2):398–414.e6.

    Article  PubMed  CAS  Google Scholar 

  140. Nitzan O, Elias M, Peretz A, Saliba W. Role of antibiotics for treatment of inflammatory bowel disease. World J Gastroenterol. 2016;22(3):1078–87.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. Reinisch W. Fecal microbiota transplantation in inflammatory bowel disease. Dig Dis. 2017;35(1–2):123–6.

    Article  PubMed  Google Scholar 

  142. MacLellan A, Moore-Connors J, Grant S, Cahill L, Langille MGI, Van Limbergen J. The impact of exclusive enteral nutrition (EEN) on the gut microbiome in Crohn’s disease: a review. Nutrients. 2017;9(5):0447.

    Article  Google Scholar 

  143. Richman E, Rhodes JM. Review article: evidence-based dietary advice for patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2013;38(10):1156–71.

    Article  PubMed  CAS  Google Scholar 

  144. Dziechciarz P, Horvath A, Shamir R, Szajewska H. Meta-analysis: enteral nutrition in active Crohn’s disease in children. Aliment Pharmacol Ther. 2007;26(6):795–806.

    Article  PubMed  CAS  Google Scholar 

  145. 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(10):1179–207.

    Article  PubMed  CAS  Google Scholar 

  146. Gerasimidis K, Bertz M, Hanske L, Junick J, Biskou O, Aguilera M, et al. Decline in presumptively protective gut bacterial species and metabolites are paradoxically associated with disease improvement in pediatric Crohn’s disease during enteral nutrition. Inflamm Bowel Dis. 2014;20(5):861–71.

    Article  PubMed  Google Scholar 

  147. Benjamin JL, Hedin CR, Koutsoumpas A, Ng SC, McCarthy NE, Hart AL, et al. Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn’s disease. Gut. 2011;60(7):923–9.

    Article  PubMed  CAS  Google Scholar 

  148. Kronman MP, Zaoutis TE, Haynes K, Feng R, Coffin SE. Antibiotic exposure and IBD development among children: a population-based cohort study. Pediatrics. 2012;130(4):e794–803.

    Article  PubMed  PubMed Central  Google Scholar 

  149. Cojocariu C, Stanciu C, Stoica O, Singeap AM, Sfarti C, Girleanu I, et al. Clostridium difficile infection and inflammatory bowel disease. Turk J Gastroenterol. 2014;25(6):603–10.

    Article  PubMed  Google Scholar 

  150. Kerman DH, Deshpande AR. Gut microbiota and inflammatory bowel disease: the role of antibiotics in disease management. Postgrad Med. 2014;126(4):7–19.

    Article  PubMed  Google Scholar 

  151. Wang SL, Wang ZR, Yang CQ. Meta-analysis of broad-spectrum antibiotic therapy in patients with active inflammatory bowel disease. Exp Ther Med. 2012;4(6):1051–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Derikx LA, Dieleman LA, Hoentjen F. Probiotics and prebiotics in ulcerative colitis. Best Pract Res Clin Gastroenterol. 2016;30(1):55–71.

    Article  PubMed  Google Scholar 

  153. Durchschein F, Petritsch W, Hammer HF. Diet therapy for inflammatory bowel diseases: the established and the new. World J Gastroenterol. 2016;22(7):2179–94.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  154. Doron S, Snydman DR. Risk and safety of probiotics. Clin Infect Dis. 2015;60(Suppl 2):S129–34.

    Article  PubMed  PubMed Central  Google Scholar 

  155. Wang AY, Popov J, Pai N. Fecal microbial transplant for the treatment of pediatric inflammatory bowel disease. World J Gastroenterol. 2016;22(47):10304–15.

    Article  PubMed  PubMed Central  Google Scholar 

  156. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44(5):854–9.

    PubMed  CAS  Google Scholar 

  157. Fischer M, Kao D, Kelly C, Kuchipudi A, Jafri SM, Blumenkehl M, et al. Fecal microbiota transplantation is safe and efficacious for recurrent or refractory Clostridium difficile infection in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2016;22(10):2402–9.

    Article  PubMed  Google Scholar 

  158. Zhang FM, Wang HG, Wang M, Cui BT, Fan ZN, Ji GZ. Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn’s disease. World J Gastroenterol. 2013;19(41):7213–6.

    Article  PubMed  PubMed Central  Google Scholar 

  159. Borody TJ, Warren EF, Leis S, Surace R, Ashman O. Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol. 2003;37(1):42–7.

    Article  PubMed  Google Scholar 

  160. Keshteli AH, Millan B, Madsen KL. Pretreatment with antibiotics may enhance the efficacy of fecal microbiota transplantation in ulcerative colitis: a meta-analysis. Mucosal Immunol. 2017;10(2):565–6.

    Article  PubMed  CAS  Google Scholar 

  161. Baxter M, Colville A. Adverse events in faecal microbiota transplant: a review of the literature. J Hosp Infect. 2016;92(2):117–27.

    Article  PubMed  CAS  Google Scholar 

  162. Wyllie R, Hyams J. Pediatric gastrointestinal and liver diseases. Philladelphia: Elsevier; 2015.

    Google Scholar 

  163. Davenport M, Poles J, Leung JM, Wolff MJ, Abidi WM, Ullman T, et al. Metabolic alterations to the mucosal microbiota in inflammatory bowel disease. Inflamm Bowel Dis. 2014;20(4):723–31.

    Article  PubMed  Google Scholar 

  164. Reshef L, Kovacs A, Ofer A, Yahav L, Maharshak N, Keren N, et al. Pouch inflammation is associated with a decrease in specific bacterial taxa. Gastroenterology. 2015;149(3):718–27.

    Article  PubMed  Google Scholar 

  165. Forbes JD, Van Domselaar G, Bernstein CN. Microbiome survey of the inflamed and noninflamed gut at different compartments within the gastrointestinal tract of inflammatory bowel disease patients. Inflamm Bowel Dis. 2016;22(4):817–25.

    Article  PubMed  Google Scholar 

  166. Hasler R, Sheibani-Tezerji R, Sinha A, Barann M, Rehman A, Esser D, et al. Uncoupling of mucosal gene regulation, mRNA splicing and adherent microbiota signatures in inflammatory bowel disease. Gut. 2016;66(12):2087–97.

    Article  PubMed  Google Scholar 

  167. Tyler AD, Kirsch R, Milgrom R, Stempak JM, Kabakchiev B, Silverberg MS. Microbiome heterogeneity characterizing intestinal tissue and inflammatory bowel disease phenotype. Inflamm Bowel Dis. 2016;22(4):807–16.

    Article  PubMed  Google Scholar 

  168. Mukhopadhya I, Hansen R, Meharg C, Thomson JM, Russell RK, Berry SH, et al. The fungal microbiota of de-novo paediatric inflammatory bowel disease. Microbes Infect. 2015;17(4):304–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  169. El Mouzan M, Wang F, Al Mofarreh M, Menon R, Al Barrag A, Korolev KS, et al. Fungal Microbiota Profile in Newly Diagnosed Treatment-naïve Children with Crohn’s Disease. J Crohns Colitis. 2017;11(5):586–592.

    Google Scholar 

  170. Greenblum S, Turnbaugh PJ, Borenstein E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A. 2012;109(2):594–9.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Food Nutrition and Health Team, AgResearch, Palmerston North, New Zealand

    Wayne Young

  2. Riddet Institute, Massey University, Palmerston North, New Zealand

    Wayne Young

  3. High-Value Nutrition, National Science Challenge, Auckland, New Zealand

    Wayne Young

  4. Department of Pediatrics, Division of Gastroenterology, University of Alabama at Birmingham, Birmingham, AL, USA

    Traci Jester

  5. Department of Pediatrics, Division of Rheumatology, University of Alabama at Birmingham, Birmingham, AL, USA

    Matthew L. Stoll

  6. Institute of Molecular Medicine, RWTH Aachen University, Aachen, Germany

    Ana Izcue

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  1. Faculty of Medicine, Cairo University, Cairo, Egypt

    Gaafar Ragab

  2. University of Alabama, Birmingham, Alabama, USA

    T. Prescott Atkinson

  3. University of Alabama, Birmingham, Alabama, USA

    Matthew L. Stoll

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Young, W., Jester, T., Stoll, M.L., Izcue, A. (2018). Inflammatory Bowel Disease. In: Ragab, G., Atkinson, T., Stoll, M. (eds) The Microbiome in Rheumatic Diseases and Infection. Springer, Cham. https://doi.org/10.1007/978-3-319-79026-8_19

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