Volume 12 Issue 5
May  2021
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Sheng Liu, Wenjing Zhao, Ping Lan, Xiangyu Mou. The microbiome in inflammatory bowel diseases: from pathogenesis to therapy[J]. Protein&Cell, 2021, 12(5): 331-345. doi: 10.1007/s13238-020-00745-3
Citation: Sheng Liu, Wenjing Zhao, Ping Lan, Xiangyu Mou. The microbiome in inflammatory bowel diseases: from pathogenesis to therapy[J]. Protein&Cell, 2021, 12(5): 331-345. doi: 10.1007/s13238-020-00745-3

The microbiome in inflammatory bowel diseases: from pathogenesis to therapy

doi: 10.1007/s13238-020-00745-3

We thank Drs. Xiaojian Wu, Zhen He and Jia Ke for helpful discussion. We thank Peijie Li for assisting preparation of this manuscript. This work has been supported by National Key Research and Development Program of China (No. 2017YFC1308800), the Fundamental Research Funds for the Central Universities (19ykzd33, Sun Yat-sen University) and the National Natural Science Foundation of China (Grant No. 31900056).

  • Received Date: 2020-02-10
  • Rev Recd Date: 2020-05-30
  • Inflammatory bowel disease (IBD) has become a global disease with accelerating incidence worldwide in the 21st century while its accurate etiology remains unclear. In the past decade, gut microbiota dysbiosis has consistently been associated with IBD. Although many IBDassociated dysbiosis have not been proven to be a cause or an effect of IBD, it is often hypothesized that at least some of alteration in microbiome is protective or causative. In this article, we selectively reviewed the hypothesis supported by both association studies in human and pathogenesis studies in biological models. Specifically, we reviewed the potential protective bacterial pathways and species against IBD, as well as the potential causative bacterial pathways and species of IBD. We also reviewed the potential roles of some members of mycobiome and virome in IBD. Lastly, we covered the current status of therapeutic approaches targeting microbiome, which is a promising strategy to alleviate and cure this inflammatory disease.
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  • [1]
    Abraham BP, Quigley EMM (2017) Probiotics in inflammatory bowel disease. Gastroenterol Clin N Am 46:769-782
    Agus A, Planchais J, Sokol H (2018) Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe 23:716-724
    Akram W, Garud N, Joshi R (2019) Role of inulin as prebiotics on inflammatory bowel disease. Drug Discov Ther 13:1-8
    Alhagamhmad MH, Day AS, Lemberg DA, Leach ST (2016) An overview of the bacterial contribution to Crohn disease pathogenesis. J Med Microbiol 65:1049-1059
    An D, Oh SF, Olszak T, Neves JF, Avci FY, Erturk-Hasdemir D, Lu X, Zeissig S, Blumberg RS, Kasper DL (2014) Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 156:123-133
    Ansaldo E, Slayden LC, Ching KL, Koch MA, Wolf NK, Plichta DR, Brown EM, Graham DB, Xavier RJ, Moon JJ et al (2019) Akkermansia muciniphila induces intestinal adaptive immune responses during homeostasis. Science 364:1179-1184
    Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB et al (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338:120-123
    Atherly T, Mosher C, Wang C, Hostetter J, Proctor A, Brand MW, Phillips GJ, Wannemuehler M, Jergens AE (2016) Helicobacter bilis infection alters mucosal bacteria and modulates colitis development in defined microbiota mice. Inflamm Bowel Dis 22:2571-2581
    Barnett MP, McNabb WC, Cookson AL, Zhu S, Davy M, Knoch B, Nones K, Hodgkinson AJ, Roy NC (2010) Changes in colon gene expression associated with increased colon inflammation in interleukin-10 gene-deficient mice inoculated with Enterococcus species. BMC Immunol 11:39
    Barnich N, Carvalho FA, Glasser AL, Darcha C, Jantscheff P, Allez M, Peeters H, Bommelaer G, Desreumaux P, Colombel JF et al (2007) CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Investig 117:1566-1574
    Bell A, Brunt J, Crost E, Vaux L, Nepravishta R, Owen CD, Latousakis D, Xiao A, Li W, Chen X et al (2019) Elucidation of a sialic acid metabolism pathway in mucus-foraging Ruminococcus gnavus unravels mechanisms of bacterial adaptation to the gut. Nat Microbiol 4:2393-2404
    Bian X, Wu W, Yang L, Lv L, Wang Q, Li Y, Ye J, Fang D, Wu J, Jiang X et al (2019) Administration of Akkermansia muciniphila ameliorates dextran sulfate sodium-induced ulcerative colitis in mice. Front Microbiol 10:2259
    Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100:1539-1546
    Bjarnason I, Sission G, Hayee B (2019) A randomised, double-blind, placebo-controlled trial of a multi-strain probiotic in patients with asymptomatic ulcerative colitis and Crohn's disease. Inflammopharmacology 27:465-473
    Blandford LE, Johnston EL, Sanderson JD, Wade WG, Lax AJ (2019) Promoter orientation of the immunomodulatory Bacteroides fragilis capsular polysaccharide A (PSA) is off in individuals with inflammatory bowel disease (IBD). Gut Microbes 10:569-577
    Breban M, Tap J, Leboime A, Said-Nahal R, Langella P, Chiocchia G, Furet JP, Sokol H (2017) Faecal microbiota study reveals specific dysbiosis in spondyloarthritis. Ann Rheum Dis 76:1614-1622
    Bringer MA, Glasser AL, Tung CH, Meresse S, Darfeuille-Michaud A (2006) The Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 replicates in mature phagolysosomes within J774 macrophages. Cell Microbiol 8:471-484
    Burrello C, Garavaglia F, Cribiu FM, Ercoli G, Lopez G, Troisi J, Colucci A, Guglietta S, Carloni S, Guglielmetti S et al (2018) Therapeutic faecal microbiota transplantation controls intestinal inflammation through IL10 secretion by immune cells. Nat Commun 9:5184
    Cammarota G, Ianiro G, Tilg H, Rajilic-Stojanovic M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A et al (2017) European consensus conference on faecal microbiota transplantation in clinical practice. Gut 66:569-580
    Cammarota G, Ianiro G, Kelly CR, Mullish BH, Allegretti JR, Kassam Z, Putignani L, Fischer M, Keller JJ, Costello SP et al (2019) International consensus conference on stool banking for faecal microbiota transplantation in clinical practice. Gut 68:2111-2121
    Cao X (2017) Intestinal inflammation induced by oral bacteria. Science 358:308-309
    Castano-Rodriguez N, Kaakoush NO, Lee WS, Mitchell HM (2017) Dual role of Helicobacter and Campylobacter species in IBD:a systematic review and meta-analysis. Gut 66:235-249
    Chai JN, Peng Y, Rengarajan S, Solomon BD, Ai TL, Shen Z, Perry JSA, Knoop KA, Tanoue T, Narushima S et al (2017) Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation. Sci Immunol 2(13):eaal5068
    Chehoud C, Albenberg LG, Judge C, Hoffmann C, Grunberg S, Bittinger K, Baldassano RN, Lewis JD, Bushman FD, Wu GD (2015) Fungal signature in the gut microbiota of pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis 21:1948-1956
    Chiaro TR, Soto R, Zac Stephens W, Kubinak JL, Petersen C, Gogokhia L, Bell R, Delgado JC, Cox J, Voth W et al (2017) A member of the gut mycobiota modulates host purine metabolism exacerbating colitis in mice. Sci Transl Med 9(380):eaaf9044
    Chua HH, Chou HC, Tung YL, Chiang BL, Liao CC, Liu HH, Ni YH (2018) Intestinal dysbiosis featuring abundance of Ruminococcus gnavus associates with allergic diseases in infants. Gastroenterology 154:154-167
    Chung L, Thiele Orberg E, Geis AL, Chan JL, Fu K, DeStefano Shields CE, Dejea CM, Fathi P, Chen J, Finard BB et al (2018) Bacteroides fragilis toxin coordinates a pro-carcinogenic inflammatory cascade via targeting of colonic epithelial cells. Cell Host Microbe 23(203-214):e205
    Clooney AG, Sutton TDS, Shkoporov AN, Holohan RK, Daly KM, O'Regan O, Ryan FJ, Draper LA, Plevy SE, Ross RP et al (2019) Whole-virome analysis sheds light on viral dark matter in inflammatory bowel disease. Cell Host Microbe 26:764-778.e765
    Coker OO, Nakatsu G, Dai RZ, Wu WKK, Wong SH, Ng SC, Chan FKL, Sung JJY, Yu J (2019) Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut 68:654-662
    Colombel JF, Shin A, Gibson PR (2019) AGA clinical practice update on functional gastrointestinal symptoms in patients with inflammatory bowel disease:expert review. Clin Gastroenterol Hepatol 17:380-390.e381
    Connors J, Dunn KA, Allott J, Bandsma R, Rashid M, Otley AR, Bielawski JP, Van Limbergen J (2019) The relationship between fecal bile acids and microbiome community structure in pediatric Crohn's disease. ISME J 14:702-713
    Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, Huang G, Liu Z, Wu P, Fan Z et al (2015) Fecal microbiota transplantation through mid-gut for refractory Crohn's disease:safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol 30:51-58
    Darfeuille-Michaud A (2002) Adherent-invasive Escherichia coli:a putative new E. coli pathotype associated with Crohn's disease. Int J Med Microbiol 292:185-193
    Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127:412-421
    De Hertogh G, Aerssens J, Geboes KP, Geboes K (2008) Evidence for the involvement of infectious agents in the pathogenesis of Crohn's disease. World J Gastroenterol 14:845-852
    Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K, Harris K, Gilmour KC, Soothill J, Jacobs-Sera D, Schooley RT et al (2019) Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat Med 25:730-733
    Dejea CM, Fathi P, Craig JM, Boleij A, Taddese R, Geis AL, Wu X, DeStefano Shields CE, Hechenbleikner EM, Huso DL et al (2018) Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science 359:592-597
    Derwa Y, Gracie DJ, Hamlin PJ, Ford AC (2017) Systematic review with meta-analysis:the efficacy of probiotics in inflammatory bowel disease. Aliment Pharmacol Ther 46:389-400
    Dickson I (2018) Gut microbiota:oral bacteria:a cause of IBD? Nat Rev Gastroenterol Hepatol 15:4-5
    Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ, Higginbottom SK, Le A, Cowan TM, Nolan GP, Fischbach MA et al (2017) A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature 551:648-652
    Draper LA, Ryan FJ, Smith MK, Jalanka J, Mattila E, Arkkila PA, Ross RP, Satokari R, Hill C (2018) Long-term colonisation with donor bacteriophages following successful faecal microbial transplantation. Microbiome 6:220
    Duan Y, Llorente C, Lang S, Brandl K, Chu H, Jiang L, White RC, Clarke TH, Nguyen K, Torralba M et al (2019) Bacteriophage targeting of gut bacterium attenuates alcoholic liver disease. Nature 575:505-511
    Duboc H, Rajca S, Rainteau D, Benarous D, Maubert MA, Quervain E, Thomas G, Barbu V, Humbert L, Despras G et al (2013) Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 62:531-539
    Duerkop BA, Kleiner M, Paez-Espino D, Zhu W, Bushnell B, Hassell B, Winter SE, Kyrpides NC, Hooper LV (2018) Murine colitis reveals a disease-associated bacteriophage community. Nat Microbiol 3:1023-1031
    Eaton K, Pirani A, Snitkin ES, Reproducibility Project:Cancer B, Iorns E, Tsui R, Denis A, Perfito N, Errington TM, Iorns E et al (2018). Replication Study:intestinal inflammation targets cancer-inducing activity of the microbiota. Elife 7:e34364.
    el-Omar E, Penman I, Cruikshank G, Dover S, Banerjee S, Williams C, McColl KE (1994) Low prevalence of Helicobacter pylori in inflammatory bowel disease:association with sulphasalazine. Gut 35:1385-1388
    Erickson AR, Cantarel BL, Lamendella R, Darzi Y, Mongodin EF, Pan C, Shah M, Halfvarson J, Tysk C, Henrissat B et al (2012) Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn's disease. PLoS ONE 7:e49138
    Fedorak RN, Feagan BG, Hotte N, Leddin D, Dieleman LA, Petrunia DM, Enns R, Bitton A, Chiba N, Pare P et al (2015) The probiotic VSL#3 has anti-inflammatory effects and could reduce endoscopic recurrence after surgery for Crohn's disease. Clin Gastroenterol Hepatol 13:928-935.e922
    Franzosa EA, Sirota-Madi A, Avila-Pacheco J, Fornelos N, Haiser HJ, Reinker S, Vatanen T, Hall AB, Mallick H, McIver LJ et al (2019) Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat Microbiol 4:293-305
    Freedman SB, Williamson-Urquhart S, Farion KJ, Gouin S, Willan AR, Poonai N, Hurley K, Sherman PM, Finkelstein Y, Lee BE et al (2018) Multicenter trial of a combination probiotic for children with gastroenteritis. N Engl J Med 379:2015-2026
    Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T et al (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446-450
    Galtier M, De Sordi L, Sivignon A, de Vallee A, Maura D, Neut C, Rahmouni O, Wannerberger K, Darfeuille-Michaud A, Desreumaux P et al (2017) Bacteriophages targeting adherent invasive Escherichia coli strains as a promising new treatment for Crohn's disease. J Crohns Colitis 11:840-847
    Garrett WS (2019) The gut microbiota and colon cancer. Science 364:1133-1135
    Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, Punit S, Karlsson M, Bry L, Glickman JN et al (2010) Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8:292-300
    Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD et al (2017) Expert consensus document:The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491-502
    Gogokhia L, Buhrke K, Bell R, Hoffman B, Brown DG, Hanke-Gogokhia C, Ajami NJ, Wong MC, Ghazaryan A, Valentine JF et al (2019) Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe 25:285-299.e288
    Hall AB, Yassour M, Sauk J, Garner A, Jiang X, Arthur T, Lagoudas GK, Vatanen T, Fornelos N, Wilson R et al (2017) A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients. Genome Med 9:103
    Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A (2012) Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol 107:761-767
    Hang S, Paik D, Yao L, Kim E, Trinath J, Lu J, Ha S, Nelson BN, Kelly SP, Wu L et al (2019) Bile acid metabolites control TH17 and Treg cell differentiation. Nature 576:143-148
    Hedin C, van der Gast CJ, Rogers GB, Cuthbertson L, McCartney S, Stagg AJ, Lindsay JO, Whelan K (2016) Siblings of patients with Crohn's disease exhibit a biologically relevant dysbiosis in mucosal microbial metacommunities. Gut 65:944-953
    Henke MT, Kenny DJ, Cassilly CD, Vlamakis H, Xavier RJ, Clardy J (2019) Ruminococcus gnavus, a member of the human gut microbiome associated with Crohn's disease, produces an inflammatory polysaccharide. Proc Natl Acad Sci USA 116:12672-12677
    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S et al (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506-514
    Hvas CL, Dahl Jørgensen SM, Jørgensen SRP, Storgaard M, Lemming L, Hansen MM, Erikstrup C, Dahlerup JF (2019) Fecal microbiota transplantation is superior to fidaxomicin for treatment of recurrent Clostridium difficile infection. Gastroenterology 156:1324-1332.e1323
    Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, Brown J, Becker CA, Fleshner PR, Dubinsky M et al (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336:1314-1317
    Imhann F, Vich Vila A, Bonder MJ, Fu J, Gevers D, Visschedijk MC, Spekhorst LM, Alberts R, Franke L, van Dullemen HM et al (2018) Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut 67:108-119
    Jergens AE, Wilson-Welder JH, Dorn A, Henderson A, Liu Z, Evans RB, Hostetter J, Wannemuehler MJ (2007) Helicobacter bilis triggers persistent immune reactivity to antigens derived from the commensal bacteria in gnotobiotic C3H/HeN mice. Gut 56:934-940
    Joossens M, Huys G, Cnockaert M, De Preter V, Verbeke K, Rutgeerts P, Vandamme P, Vermeire S (2011) Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 60:631-637
    Kalischuk LD, Buret AG (2010) A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Am J Physiol Gastrointest Liver Physiol 298:29
    Khoruts A, Sadowsky MJ (2016) Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol 13:508-516
    Khoruts A, Rank KM, Newman KM, Viskocil K, Vaughn BP, Hamilton MJ, Sadowsky MJ (2016) Inflammatory bowel disease affects the outcome of fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol 14:1433-1438
    Kim MH, Kang SG, Park JH, Yanagisawa M, Kim CH (2013) Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 145(396-406):e391-e310
    Kirk KF, Nielsen HL, Thorlacius-Ussing O, Nielsen H (2016) Optimized cultivation of Campylobacter concisus from gut mucosal biopsies in inflammatory bowel disease. Gut Pathog 8:27
    Kostic AD, Xavier RJ, Gevers D (2014) The microbiome in inflammatory bowel disease:current status and the future ahead. Gastroenterology 146:1489-1499
    Kotlowski R, Bernstein CN, Sepehri S, Krause DO (2007) High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56:669-675
    Kruis W, Fric P, Pokrotnieks J, Lukas M, Fixa B, Kascak M, Kamm MA, Weismueller J, Beglinger C, Stolte M et al (2004) Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53:1617-1623
    Kullberg MC, Rothfuchs AG, Jankovic D, Caspar P, Wynn TA, Gorelick PL, Cheever AW, Sher A (2001) Helicobacter hepaticus-induced colitis in interleukin-10-deficient mice:cytokine requirements for the induction and maintenance of intestinal inflammation. Infect Immun 69:4232-4241
    Kullberg MC, Jankovic D, Feng CG, Hue S, Gorelick PL, McKenzie BS, Cua DJ, Powrie F, Cheever AW, Maloy KJ et al (2006) IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med 203:2485-2494
    Laharie D, Asencio C, Asselineau J, Bulois P, Bourreille A, Moreau J, Bonjean P, Lamarque D, Pariente A, Soule JC et al (2009) Association between entero-hepatic Helicobacter species and Crohn's disease:a prospective cross-sectional study. Aliment Pharmacol Ther 30:283-293
    Lam S, Zuo T, Ho M, Chan FKL, Chan PKS, Ng SC (2019) Review article:fungal alterations in inflammatory bowel diseases. Aliment Pharmacol Ther 50:1159-1171
    Lamb CA, Kennedy NA, Raine T, Hendy PA, Smith PJ, Limdi JK, Hayee B, Lomer MCE, Parkes GC, Selinger C et al (2019) British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults. Gut 68:s1-s106
    LaMont JT (2018) Probiotics for children with gastroenteritis. N Engl J Med 379:2076-2077
    Levy M, Thaiss CA, Zeevi D, Dohnalova L, Zilberman-Schapira G, Mahdi JA, David E, Savidor A, Korem T, Herzig Y et al (2015) Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163:1428-1443
    Li Q, Wang C, Tang C, He Q, Li N, Li J (2014) Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn's disease. J Clin Gastroenterol 48:513-523
    Li XV, Leonardi I, Iliev ID (2019) Gut mycobiota in immunity and inflammatory disease. Immunity 50:1365-1379
    Limon JJ, Tang J, Li D, Wolf AJ, Michelsen KS, Funari V, Gargus M, Nguyen C, Sharma P, Maymi VI et al (2019) Malassezia is associated with Crohn's disease and exacerbates colitis in mouse models. Cell Host Microbe 25:377-388.e376
    Liu Z, Ramer-Tait AE, Henderson AL, Demirkale CY, Nettleton D, Wang C, Hostetter JM, Jergens AE, Wannemuehler MJ (2011) Helicobacter bilis colonization enhances susceptibility to Typhlocolitis following an inflammatory trigger. Dig Dis Sci 56:2838-2848
    Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brislawn CJ et al (2019) Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature 569:655-662
    Lo Presti A, Zorzi F, Del Chierico F, Altomare A, Cocca S, Avola A, De Biasio F, Russo A, Cella E, Reddel S et al (2019) Fecal and mucosal microbiota profiling in irritable bowel syndrome and inflammatory bowel disease. Front Microbiol 10:1655
    Lynch SV, Pedersen O (2016) The human intestinal microbiome in health and disease. N Engl J Med 375:2369-2379
    Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K et al (2014) A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63:1275-1283
    Machiels K, Sabino J, Vandermosten L, Joossens M, Arijs I, de Bruyn M, Eeckhaut V, Van Assche G, Ferrante M, Verhaegen J et al (2017) Specific members of the predominant gut microbiota predict pouchitis following colectomy and IPAA in UC. Gut 66:79-88
    Mahendran V, Riordan SM, Grimm MC, Tran TA, Major J, Kaakoush NO, Mitchell H, Zhang L (2011) Prevalence of Campylobacter species in adult Crohn's disease and the preferential colonization sites of Campylobacter species in the human intestine. PLoS ONE 6:e25417
    Mahendran V, Liu F, Riordan SM, Grimm MC, Tanaka MM, Zhang L (2016) Examination of the effects of Campylobacter concisus zonula occludens toxin on intestinal epithelial cells and macrophages. Gut Pathog 8:18
    Man SM, Kaakoush NO, Leach ST, Nahidi L, Lu HK, Norman J, Day AS, Zhang L, Mitchell HM (2010) Host attachment, invasion, and stimulation of proinflammatory cytokines by Campylobacter concisus and other non-Campylobacter jejuni Campylobacter species. J Infect Dis 202:1855-1865
    Mar JS, LaMere BJ, Lin DL, Levan S, Nazareth M, Mahadevan U, Lynch SV (2016) Disease severity and immune activity relate to distinct interkingdom gut microbiome states in ethnically distinct ulcerative colitis patients. mBio. https://doi.org/10.1128/mBio.01072-16
    Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM (2004) Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 127:80-93
    Martin R, Miquel S, Benevides L, Bridonneau C, Robert V, Hudault S, Chain F, Berteau O, Azevedo V, Chatel JM et al (2017) Functional characterization of novel Faecalibacterium prausnitzii strains isolated from healthy volunteers:a step forward in the use of F. prausnitzii as a next-generation probiotic. Front Microbiol 8:1226
    Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122:107-118
    Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620-625
    McCallin S, Alam Sarker S, Barretto C, Sultana S, Berger B, Huq S, Krause L, Bibiloni R, Schmitt B, Reuteler G et al (2013) Safety analysis of a Russian phage cocktail:from metagenomic analysis to oral application in healthy human subjects. Virology 443:187-196
    Miele E, Pascarella F, Giannetti E, Quaglietta L, Baldassano RN, Staiano A (2009) Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol 104:437-443
    Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch W et al (2015) Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149:102-109.e106
    Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB et al (2012) Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13:R79
    Mukhopadhya I, Thomson JM, Hansen R, Berry SH, El-Omar EM, Hold GL (2011) Detection of Campylobacter concisus and other Campylobacter species in colonic biopsies from adults with ulcerative colitis. PLoS ONE 6:e21490
    Mylonaki M, Rayment NB, Rampton DS, Hudspith BN, Brostoff J (2005) Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis 11:481-487
    Nattramilarasu PK, Bucker R, Lobo de Sa FD, Fromm A, Nagel O, Lee IM, Butkevych E, Mousavi S, Genger C, Klove S et al (2020) Campylobacter concisus impairs sodium absorption in colonic epithelium via ENaC dysfunction and claudin-8 disruption. Int J Mol Sci 21(2):373
    Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, Panaccione R, Ghosh S, Wu JCY, Chan FKL et al (2018) Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century:a systematic review of population-based studies. Lancet 390:2769-2778
    Ni J, Wu GD, Albenberg L, Tomov VT (2017) Gut microbiota and IBD:causation or correlation? Nat Rev Gastroenterol Hepatol 14:573-584
    Nishino K, Nishida A, Inoue R, Kawada Y, Ohno M, Sakai S, Inatomi O, Bamba S, Sugimoto M, Kawahara M et al (2018) Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol 53:95-106
    Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY, Keller BC, Kambal A, Monaco CL, Zhao G, Fleshner P et al (2015) Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447-460
    Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313:848-851
    Ohkusa T, Sato N, Ogihara T, Morita K, Ogawa M, Okayasu I (2002) Fusobacterium varium localized in the colonic mucosa of patients with ulcerative colitis stimulates species-specific antibody. J Gastroenterol Hepatol 17:849-853
    Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N (2003) Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut 52:79-83
    Ohkusa T, Yoshida T, Sato N, Watanabe S, Tajiri H, Okayasu I (2009) Commensal bacteria can enter colonic epithelial cells and induce proinflammatory cytokine secretion:a possible pathogenic mechanism of ulcerative colitis. J Med Microbiol 58:535-545
    Oliva S, Di Nardo G, Ferrari F, Mallardo S, Rossi P, Patrizi G, Cucchiara S, Stronati L (2012) Randomised clinical trial:the effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis. Aliment Pharmacol Ther 35:327-334
    Ossa JC, Ho NK, Wine E, Leung N, Gray-Owen SD, Sherman PM (2013) Adherent-invasive Escherichia coli blocks interferon-gamma-induced signal transducer and activator of transcription (STAT)-1 in human intestinal epithelial cells. Cell Microbiol 15:446-457
    O'Toole PW, Marchesi JR, Hill C (2017) Next-generation probiotics:the spectrum from probiotics to live biotherapeutics. Nat Microbiol 2:17057
    Owen CD, Tailford LE, Monaco S, Suligoj T, Vaux L, Lallement R, Khedri Z, Yu H, Lecointe K, Walshaw J et al (2017) Unravelling the specificity and mechanism of sialic acid recognition by the gut symbiont Ruminococcus gnavus. Nat Commun 8:2196
    Palmela C, Chevarin C, Xu Z, Torres J, Sevrin G, Hirten R, Barnich N, Ng SC, Colombel JF (2018) Adherent-invasive Escherichia coli in inflammatory bowel disease. Gut 67:574-587
    Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, Leong RWL, Connor S, Ng W, Paramsothy R et al (2017a) Multidonor intensive faecal microbiota transplantation for active ulcerative colitis:a randomised placebo-controlled trial. Lancet 389:1218-1228
    Paramsothy S, Paramsothy R, Rubin DT, Kamm MA, Kaakoush NO, Mitchell HM, Castano-Rodriguez N (2017b) Faecal microbiota transplantation for inflammatory bowel disease:a systematic review and meta-analysis. J Crohns Colitis 11:1180-1199
    Paramsothy S, Nielsen S, Kamm MA, Deshpande NP, Faith JJ, Clemente JC, Paramsothy R, Walsh AJ, van den Bogaerde J, Samuel D et al (2019) Specific bacteria and metabolites associated with response to fecal microbiota transplantation in patients with ulcerative colitis. Gastroenterology 156:1440-1454.e1442
    Pittayanon R, Lau JT, Leontiadis GI, Tse F, Yuan Y, Surette M, Moayyedi P (2019) Differences in gut microbiota in patients with vs without inflammatory bowel diseases:a systematic review. Gastroenterology 158(4):930-946.e1
    Plovier H, Everard A, Druart C, Depommier C, Van Hul M, Geurts L, Chilloux J, Ottman N, Duparc T, Lichtenstein L et al (2017) A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med 23:107-113
    Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105:2420-2428
    Postler TS, Ghosh S (2017) Understanding the holobiont:how microbial metabolites affect human health and shape the immune system. Cell Metab 26:110-130
    Praveschotinunt P, Duraj-Thatte AM, Gelfat I, Bahl F, Chou DB, Joshi NS (2019) Engineered E. coli Nissle 1917 for the delivery of matrix-tethered therapeutic domains to the gut. Nat Commun 10:5580
    Prindiville TP, Sheikh RA, Cohen SH, Tang YJ, Cantrell MC, Silva J Jr (2000) Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg Infect Dis 6:171-174
    Prorok-Hamon M, Friswell MK, Alswied A, Roberts CL, Song F, Flanagan PK, Knight P, Codling C, Marchesi JR, Winstanley C et al (2014) Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut 63:761-770
    Quevrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermudez-Humaran LG, Pigneur B et al (2016) Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease. Gut 65:415-425
    Ring C, Klopfleisch R, Dahlke K, Basic M, Bleich A, Blaut M (2019) Akkermansia muciniphila strain ATCC BAA-835 does not promote short-term intestinal inflammation in gnotobiotic interleukin-10-deficient mice. Gut Microbes 10:188-203
    Rokkas T, Gisbert JP, Niv Y, O'Morain C (2015) The association between Helicobacter pylori infection and inflammatory bowel disease based on meta-analysis. United Eur Gastroenterol J 3:539-550
    Rossi O, van Berkel LA, Chain F, Tanweer Khan M, Taverne N, Sokol H, Duncan SH, Flint HJ, Harmsen HJ, Langella P et al (2016) 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 6:18507
    Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, Mazmanian SK (2011) The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974-977
    Sarker SA, Sultana S, Reuteler G, Moine D, Descombes P, Charton F, Bourdin G, McCallin S, Ngom-Bru C, Neville T et al (2016) Oral phage therapy of acute bacterial diarrhea with two coliphage preparations:a randomized trial in children from Bangladesh. EBioMedicine 4:124-137
    Sarker SA, Berger B, Deng Y, Kieser S, Foata F, Moine D, Descombes P, Sultana S, Huq S, Bardhan PK et al (2017) Oral application of Escherichia coli bacteriophage:safety tests in healthy and diarrheal children from Bangladesh. Environ Microbiol 19:237-250
    Sassone-Corsi M, Nuccio SP, Liu H, Hernandez D, Vu CT, Takahashi AA, Edwards RA, Raffatellu M (2016) Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature 540:280-283
    Scaldaferri F, Gerardi V, Mangiola F, Lopetuso LR, Pizzoferrato M, Petito V, Papa A, Stojanovic J, Poscia A, Cammarota G et al (2016) Role and mechanisms of action of Escherichia coli Nissle 1917 in the maintenance of remission in ulcerative colitis patients:an update. World J Gastroenterol 22:5505-5511
    Schirmer M, Garner A, Vlamakis H, Xavier RJ (2019) Microbial genes and pathways in inflammatory bowel disease. Nat Rev Microbiol 17:497-511
    Schnadower D, Tarr PI, Casper TC, Gorelick MH, Dean JM, O'Connell KJ, Mahajan P, Levine AC, Bhatt SR, Roskind CG et al (2018) Lactobacillus rhamnosus GG versus placebo for acute gastroenteritis in children. N Engl J Med 379:2002-2014
    Seishima J, Iida N, Kitamura K, Yutani M, Wang Z, Seki A, Yamashita T, Sakai Y, Honda M, Yamashita T et al (2019) Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host. Genome Biol 20:252
    Sekizuka T, Ogasawara Y, Ohkusa T, Kuroda M (2017) Characterization of Fusobacterium varium Fv113-g1 isolated from a patient with ulcerative colitis based on complete genome sequence and transcriptome analysis. PLoS ONE 12:e0189319
    Sepehri S, Khafipour E, Bernstein CN, Coombes BK, Pilar AV, Karmali M, Ziebell K, Krause DO (2011) Characterization of Escherichia coli isolated from gut biopsies of newly diagnosed patients with inflammatory bowel disease. Inflamm Bowel Dis 17:1451-1463
    Seregin SS, Golovchenko N, Schaf B, Chen J, Pudlo NA, Mitchell J, Baxter NT, Zhao L, Schloss PD, Martens EC et al (2017) NLRP6 protects Il10(-/-) mice from colitis by limiting colonization of Akkermansia muciniphila. Cell Rep 19:733-745
    Sinha SR, Haileselassie Y, Nguyen LP, Tropini C, Wang M, Becker LS, Sim D, Jarr K, Spear ET, Singh G et al (2020) Dysbiosis-induced secondary bile acid deficiency promotes intestinal inflammation. Cell Host Microbe 27(4):659-670.e5
    Sivignon A, de Vallee A, Barnich N, Denizot J, Darcha C, Pignede G, Vandekerckove P, Darfeuille-Michaud A (2015) Saccharomyces cerevisiae CNCM I-3856 prevents colitis induced by AIEC bacteria in the transgenic mouse model mimicking Crohn's disease. Inflamm Bowel Dis 21:276-286
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, Blugeon S, Bridonneau C, Furet J-P, Corthier G et al (2008a) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105:16731-16736
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G et al (2008b) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105:16731-16736
    Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Dore J (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15:1183-1189
    Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, Cohen D, Liguori G, Bourrier A, Nion-Larmurier I et al (2017) Fungal microbiota dysbiosis in IBD. Gut 66:1039-1048
    Song X, Sun X, Oh SF, Wu M, Zhang Y, Zheng W, Geva-Zatorsky N, Jupp R, Mathis D, Benoist C et al (2020) Microbial bile acid metabolites modulate gut RORgamma(+) regulatory T cell homeostasis. Nature 577:410-415
    Sonnenberg A, Genta RM (2012) Low prevalence of Helicobacter pylori infection among patients with inflammatory bowel disease. Aliment Pharmacol Ther 35:469-476
    Sonnenborn U (2016) Escherichia coli strain Nissle 1917-from bench to bedside and back:history of a special Escherichia coli strain with probiotic properties. FEMS Microbiol Lett 363(19):fnw212
    Tailford LE, Owen CD, Walshaw J, Crost EH, Hardy-Goddard J, Le Gall G, de Vos WM, Taylor GL, Juge N (2015) Discovery of intramolecular trans-sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation. Nat Commun 6:7624
    Tang C, Kamiya T, Liu Y, Kadoki M, Kakuta S, Oshima K, Hattori M, Takeshita K, Kanai T, Saijo S et al (2015) Inhibition of Dectin-1 signaling ameliorates colitis by inducing Lactobacillus-mediated regulatory T cell expansion in the intestine. Cell Host Microbe 18:183-197
    Thiele Orberg E, Fan H, Tam AJ, Dejea CM, Destefano Shields CE, Wu S, Chung L, Finard BB, Wu X, Fathi P et al (2017) The myeloid immune signature of enterotoxigenic Bacteroides fragilis-induced murine colon tumorigenesis. Mucosal Immunol 10:421-433
    Tiago FC, Porto BA, Ribeiro NS, Moreira LM, Arantes RM, Vieira AT, Teixeira MM, Generoso SV, Nascimento VN, Martins FS et al (2015) Effect of Saccharomyces cerevisiae strain UFMG A-905 in experimental model of inflammatory bowel disease. Benef Microbes 6:807-815
    Underwood AP, Kaakoush NO, Sodhi N, Merif J, Seah Lee W, Riordan SM, Rawlinson WD, Mitchell HM (2016) Campylobacter concisus pathotypes are present at significant levels in patients with gastroenteritis. J Med Microbiol 65:219-226
    van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG et al (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368:407-415
    Vich Vila A, Imhann F, Collij V, Jankipersadsing SA, Gurry T, Mujagic Z, Kurilshikov A, Bonder MJ, Jiang X, Tigchelaar EF et al (2018) Gut microbiota composition and functional changes in inflammatory bowel disease and irritable bowel syndrome. Sci Transl Med 10(472):eaap8914
    Wagner J, Maksimovic J, Farries G, Sim WH, Bishop RF, Cameron DJ, Catto-Smith AG, Kirkwood CD (2013) Bacteriophages in gut samples from pediatric Crohn's disease patients:metagenomic analysis using 454 pyrosequencing. Inflamm Bowel Dis 19:1598-1608
    Wang L, Tang L, Feng Y, Zhao S, Han M, Zhang C, Yuan G, Zhu J, Cao S, Wu Q et al (2020) A purified membrane protein from Akkermansia muciniphila or the pasteurised bacterium blunts colitis associated tumourigenesis by modulation of CD8(+) T cells in mice. Gut. https://doi.org/10.1136/gutjnl-2019-320105
    Wick EC, Rabizadeh S, Albesiano E, Wu X, Wu S, Chan J, Rhee KJ, Ortega G, Huso DL, Pardoll D et al (2014) Stat3 activation in murine colitis induced by enterotoxigenic Bacteroides fragilis. Inflamm Bowel Dis 20:821-834
    Wildt S, Nordgaard I, Hansen U, Brockmann E, Rumessen JJ (2011) A randomised double-blind placebo-controlled trial with Lactobacillus acidophilus La-5 and Bifidobacterium animalis subsp. lactis BB-12 for maintenance of remission in ulcerative colitis. J Crohns Colitis 5:115-121
    Williams BB, Van Benschoten AH, Cimermancic P, Donia MS, Zimmermann M, Taketani M, Ishihara A, Kashyap PC, Fraser JS, Fischbach MA (2014) Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe 16:495-503
    Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Jarnerot G, Tysk C, Jansson JK, Engstrand L (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139:1844-1854.e1841
    Wlodarska M, Luo C, Kolde R, d'Hennezel E, Annand JW, Heim CE, Krastel P, Schmitt EK, Omar AS, Creasey EA et al (2017) Indoleacrylic acid produced by commensal Peptostreptococcus species suppresses inflammation. Cell Host Microbe 22:25-37.e26
    Xu M, Pokrovskii M, Ding Y, Yi R, Au C, Harrison OJ, Galan C, Belkaid Y, Bonneau R, Littman DR (2018) c-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont. Nature 554:373-377
    Yang I, Eibach D, Kops F, Brenneke B, Woltemate S, Schulze J, Bleich A, Gruber AD, Muthupalani S, Fox JG et al (2013) Intestinal microbiota composition of interleukin-10 deficient C57BL/6J mice and susceptibility to Helicobacter hepaticus-induced colitis. PLoS ONE 8:e70783
    Yilmaz B, Juillerat P, Oyas O, Ramon C, Bravo FD, Franc Y, Fournier N, Michetti P, Mueller C, Geuking M et al (2019) Microbial network disturbances in relapsing refractory Crohn's disease. Nat Med 25:323-336
    Zamani S, Hesam Shariati S, Zali MR, Asadzadeh Aghdaei H, Sarabi Asiabar A, Bokaie S, Nomanpour B, Sechi LA, Feizabadi MM (2017) Detection of enterotoxigenic Bacteroides fragilis in patients with ulcerative colitis. Gut Pathog 9:53
    Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D'Angelo C, Massi-Benedetti C, Fallarino F et al (2013) Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372-385
    Zhang L, Man SM, Day AS, Leach ST, Lemberg DA, Dutt S, Stormon M, Otley A, O'Loughlin EV, Magoffin A et al (2009) Detection and isolation of Campylobacter species other than C. jejuni from children with Crohn's disease. J Clin Microbiol 47:453-455
    Zhang FM, Wang HG, Wang M, Cui BT, Fan ZN, Ji GZ (2013) Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn's disease. World J Gastroenterol 19:7213-7216
    Zhang L, Lee H, Grimm MC, Riordan SM, Day AS, Lemberg DA (2014) Campylobacter concisus and inflammatory bowel disease. World J Gastroenterol 20:1259-1267
    Zhu W, Winter MG, Byndloss MX, Spiga L, Duerkop BA, Hughes ER, Buttner L, de Lima Romao E, Behrendt CL, Lopez CA et al (2018) Precision editing of the gut microbiota ameliorates colitis. Nature 553:208-211
    Zhu W, Miyata N, Winter MG, Arenales A, Hughes ER, Spiga L, Kim J, Sifuentes-Dominguez L, Starokadomskyy P, Gopal P et al (2019) Editing of the gut microbiota reduces carcinogenesis in mouse models of colitis-associated colorectal cancer. J Exp Med 216:2378-2393
    Zuo T, Wong SH, Cheung CP, Lam K, Lui R, Cheung K, Zhang F, Tang W, Ching JYL, Wu JCY et al (2018) Gut fungal dysbiosis correlates with reduced efficacy of fecal microbiota transplantation in Clostridium difficile infection. Nat Commun 9:3663
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