7,427
Views
225
CrossRef citations to date
0
Altmetric
Review

Intestinal microbiota, fecal microbiota transplantation, and inflammatory bowel disease

& ORCID Icon
Pages 238-252 | Received 10 Oct 2016, Accepted 24 Jan 2017, Published online: 23 Feb 2017

References

  • Ventham NT, Kennedy NA, Nimmo ER, Satsangi J. Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology 2013; 145:293-308; PMID:23751777; http://dx.doi.org/10.1053/j.gastro.2013.05.050
  • Miyoshi J, Chang EB. The gut microbiota and inflammatory bowel diseases. Transl Res 2016; 179:38-48; PMID:27371886
  • Loddo I, Romano C. Inflammatory Bowel Disease: Genetics, Epigenetics, and Pathogenesis. Front Immunol 2015; 6:551; PMID:26579126; http://dx.doi.org/10.3389/fimmu.2015.00551
  • Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med 2009; 361:2066-78; PMID:19923578; http://dx.doi.org/10.1056/NEJMra0804647
  • Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A. Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol 2012; 107:761-7; PMID:22290405; http://dx.doi.org/10.1038/ajg.2011.482
  • van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013; 368:407-15; PMID:23323867; http://dx.doi.org/10.1056/NEJMoa1205037
  • Khoruts A, Weingarden AR. Emergence of fecal microbiota transplantation as an approach to repair disrupted microbial gut ecology. Immunol Lett 2014; 162:77-81; PMID:25106113;http://dx.doi.org/10.1016/j.imlet.2014.07.016
  • Damman CJ, Miller SI, Surawicz CM, Zisman TL. The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am J Gastroenterol 2012; 107:1452-9; PMID:23034604; http://dx.doi.org/10.1038/ajg.2012.93
  • Dasgupta S, Kasper DL. Relevance of commensal microbiota in the treatment and prevention of inflammatory bowel disease. Inflamm Bowel Dis 2013; 19:2478-89; PMID:23846489;http://dx.doi.org/10.1097/MIB.0b013e318297d884
  • Kahn SA, Gorawara-Bhat R, Rubin DT. Fecal bacteriotherapy for ulcerative colitis: patients are ready, are we? Inflamm Bowel Dis 2012; 18:676-84; PMID:21618362; http://dx.doi.org/10.1002/ibd.21775
  • Abrams GD, Bauer H, Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest 1963; 12:355-64
  • Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature 2007; 449:804-10; PMID:17943116; http://dx.doi.org/10.1038/nature06244
  • Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9:313-23; PMID:19343057; http://dx.doi.org/10.1038/nri2515
  • Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139:485-98; PMID:19836068;http://dx.doi.org/10.1016/j.cell.2009.09.033
  • Crabbe PA, Nash DR, Bazin H, Eyssen H, Heremans JF. Immunohistochemical observations on lymphoid tissues from conventional and germ-free mice. Lab Invest 1970; 22:448-57; PMID:4911977
  • El Aidy S, Hooiveld G, Tremaroli V, Bäckhed F, Kleerebezem M. The gut microbiota and mucosal homeostasis: colonized at birth or at adulthood, does it matter? Gut Microbes 2013; 4:118-24; PMID:23333858; http://dx.doi.org/10.4161/gmic.23362
  • Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012; 336:489-93; PMID:22442383; http://dx.doi.org/10.1126/science.1219328
  • Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, et al. The maternal microbiota drives early postnatal innate immune development. Science 2016; 351:1296-302; PMID:26989247; http://dx.doi.org/10.1126/science.aad2571
  • Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol 2010; 105:2687-92; PMID:20940708; http://dx.doi.org/10.1038/ajg.2010.398
  • 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:e794-803; PMID:23008454; http://dx.doi.org/10.1542/peds.2011-3886
  • Hviid A, Svanstrom H, Frisch M. Antibiotic use and inflammatory bowel diseases in childhood. Gut 2011; 60:49-54; PMID:20966024; http://dx.doi.org/10.1136/gut.2010.219683
  • Lopez-Serrano P, Perez-Calle JL, Perez-Fernandez MT, Fernández-Font JM, Boixeda de Miguel D, Fernández-Rodríguez CM. Environmental risk factors in inflammatory bowel diseases. Investigating the hygiene hypothesis: a Spanish case-control study. Scand J Gastroenterol 2010; 45:1464-71
  • Hugot JP, Chamaillard M, Zouali H, Lesage S, Cézard JP, Belaiche J, Almer S, Tysk C, O'Morain CA, Gassull M, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001; 411:599-603; PMID:11385576; http://dx.doi.org/10.1038/35079107
  • Strober W, Watanabe T. NOD2, an intracellular innate immune sensor involved in host defense and Crohn's disease. Mucosal Immunol 2011; 4:484-95; PMID:21750585; http://dx.doi.org/10.1038/mi.2011.29
  • Fritz T, Niederreiter L, Adolph T, Blumberg RS, Kaser A. Crohn's disease: NOD2, autophagy and ER stress converge. Gut 2011; 60:1580-8; PMID:21252204; http://dx.doi.org/10.1136/gut.2009.206466
  • Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001; 411:603-6; PMID:11385577; http://dx.doi.org/10.1038/35079114
  • Petnicki-Ocwieja T, Hrncir T, Liu YJ, Biswas A, Hudcovic T, Tlaskalova-Hogenova H, Kobayashi KS. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A 2009; 106:15813-8; PMID:19805227;http://dx.doi.org/10.1073/pnas.0907722106
  • Rehman A, Sina C, Gavrilova O, Häsler R, Ott S, Baines JF, Schreiber S, Rosenstiel P. Nod2 is essential for temporal development of intestinal microbial communities. Gut 2011; 60:1354-62; PMID:21421666; http://dx.doi.org/10.1136/gut.2010.216259
  • Mondot S, Barreau F, Al Nabhani Z, Dussaillant M, Le Roux K, Doré J, Leclerc M, Hugot JP, Lepage P. Altered gut microbiota composition in immune-impaired Nod2(−/−) mice. Gut 2012; 61:634-5; PMID:21868489; http://dx.doi.org/10.1136/gutjnl-2011-300478
  • Smith P, Siddharth J, Pearson R, Holway N, Shaxted M, Butler M, Clark N, Jamontt J, Watson RP, Sanmugalingam D, et al. Host genetics and environmental factors regulate ecological succession of the mouse colon tissue-associated microbiota. PLoS One 2012; 7:e30273; PMID:22272321;http://dx.doi.org/10.1371/journal.pone.0030273
  • Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nuñez G, Flavell RA. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005; 307:731-4; PMID:15692051; http://dx.doi.org/10.1126/science.1104911
  • Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, Huot L, Grandjean T, Bressenot A, Delanoye-Crespin A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 2013; 123:700-11; PMID:23281400
  • Travassos LH, Carneiro LA, Ramjeet M, Hussey S, Kim YG, Magalhães JG, Yuan L, Soares F, Chea E, Le Bourhis L, et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol 2010; 11:55-62; PMID:19898471; http://dx.doi.org/10.1038/ni.1823
  • Cooney R, Baker J, Brain O, Danis B, Pichulik T, Allan P, Ferguson DJ, Campbell BJ, Jewell D, Simmons A. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat Med 2010; 16:90-7; PMID:19966812; http://dx.doi.org/10.1038/nm.2069
  • Elson CO, Cong Y, McCracken VJ, Dimmitt RA, Lorenz RG, Weaver CT. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev 2005; 206:260-76; PMID:16048554; http://dx.doi.org/10.1111/j.0105-2896.2005.00291.x
  • Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 2002; 160:2253-7; PMID:12057927; http://dx.doi.org/10.1016/S0002-9440(10)61172-8
  • Waidmann M, Bechtold O, Frick JS, Lehr HA, Schubert S, Dobrindt U, Loeffler J, Bohn E, Autenrieth IB. Bacteroides vulgatus protects against Escherichia coli-induced colitis in gnotobiotic interleukin-2-deficient mice. Gastroenterology 2003; 125:162-77; PMID:12851881; http://dx.doi.org/10.1016/S0016-5085(03)00672-3
  • Stepankova R, Powrie F, Kofronova O, Kozakova H, Hudcovic T, Hrncir T, Uhlig H, Read S, Rehakova Z, Benada O, et al. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm Bowel Dis 2007; 13:1202-11; PMID:17607724; http://dx.doi.org/10.1002/ibd.20221
  • Eun CS, Mishima Y, Wohlgemuth S, Liu B, Bower M, Carroll IM, Sartor RB. Induction of bacterial antigen-specific colitis by a simplified human microbiota consortium in gnotobiotic interleukin-10−/− mice. Infect Immun 2014; 82:2239-46; PMID:24643531; http://dx.doi.org/10.1128/IAI.01513-13
  • Schaubeck M, Clavel T, Calasan J, Lagkouvardos I, Haange SB, Jehmlich N, Basic M, Dupont A, Hornef M, von Bergen M, et al. Dysbiotic gut microbiota causes transmissible Crohn's disease-like ileitis independent of failure in antimicrobial defence. Gut 2016; 65:225-37; PMID:25887379; http://dx.doi.org/10.1136/gutjnl-2015-309333
  • Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007; 131:33-45; PMID:17923086; http://dx.doi.org/10.1016/j.cell.2007.08.017
  • Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145:745-57; PMID:21565393; http://dx.doi.org/10.1016/j.cell.2011.04.022
  • Brinkman BM, Becker A, Ayiseh RB, Hildebrand F, Raes J, Huys G, Vandenabeele P. Gut microbiota affects sensitivity to acute DSS-induced colitis independently of host genotype. Inflamm Bowel Dis 2013; 19:2560-7; PMID:24105395; http://dx.doi.org/10.1097/MIB.0b013e3182a8759a
  • Singh V, Kumar M, San Yeoh B, Xiao X, Saha P, Kennett MJ, Vijay-Kumar M. Inhibition of Interleukin-10 Signaling Induces Microbiota-dependent Chronic Colitis in Apolipoprotein E Deficient Mice. Inflamm Bowel Dis 2016; 22:841-52; PMID:26891260; http://dx.doi.org/10.1097/MIB.0000000000000699
  • Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, Punit S, Karlsson M, Bry L, Glickman JN, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010; 8:292-300; PMID:20833380; http://dx.doi.org/10.1016/j.chom.2010.08.004
  • Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature 2012; 487:104-8; PMID:22722865
  • Mottawea W, Chiang CK, Muhlbauer M, Starr AE, Butcher J, Abujamel T, Deeke SA, Brandel A, Zhou H, Shokralla S, et al. Altered intestinal microbiota-host mitochondria crosstalk in new onset Crohn's disease. Nat Commun 2016; 7:13419; PMID:27876802; http://dx.doi.org/10.1038/ncomms13419
  • Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N. Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut 2003; 52:79-83; PMID:12477765; http://dx.doi.org/10.1136/gut.52.1.79
  • Eckburg PB, Relman DA. The role of microbes in Crohn's disease. Clin Infect Dis 2007; 44:256-62; PMID:17173227; http://dx.doi.org/10.1086/510385
  • Sibartie V, Kirwan WO, O'Mahony S, Stack W, Shanahan F. Intestinal tuberculosis mimicking Crohn's disease: lessons relearned in a new era. Eur J Gastroenterol Hepatol 2007; 19:347-9; PMID:17353702; http://dx.doi.org/10.1097/MEG.0b013e328012122b
  • Woodman I, Schofield JB, Haboubi N. The histopathological mimics of inflammatory bowel disease: a critical appraisal. Tech Coloproctol 2015; 19:717-27; PMID:26385573; http://dx.doi.org/10.1007/s10151-015-1372-8
  • Nazareth N, Magro F, Machado E, Ribeiro TG, Martinho A, Rodrigues P, Alves R, Macedo GN, Gracio D, Coelho R, et al. Prevalence of Mycobacterium avium subsp. paratuberculosis and Escherichia coli in blood samples from patients with inflammatory bowel disease. Med Microbiol Immunol 2015; 204:681-92; PMID:25994082; http://dx.doi.org/10.1007/s00430-015-0420-3
  • Gui GP, Thomas PR, Tizard ML, Lake J, Sanderson JD, Hermon-Taylor J. Two-year-outcomes analysis of Crohn's disease treated with rifabutin and macrolide antibiotics. J Antimicrob Chemother 1997; 39:393-400; PMID:9096189; http://dx.doi.org/10.1093/jac/39.3.393
  • Borody TJ, Leis S, Warren EF, Surace R. Treatment of severe Crohn's disease using antimycobacterial triple therapy–approaching a cure? Dig Liver Dis 2002; 34:29-38; PMID:11926571; http://dx.doi.org/10.1016/S1590-8658(02)80056-1
  • Shafran I, Kugler L, El-Zaatari FA, Naser SA, Sandoval J. Open clinical trial of rifabutin and clarithromycin therapy in Crohn's disease. Dig Liver Dis 2002; 34:22-8; PMID:11930899; http://dx.doi.org/10.1016/S1590-8658(02)80055-X
  • Selby W, Pavli P, Crotty B, Florin T, Radford-Smith G, Gibson P, Mitchell B, Connell W, Read R, Merrett M, et al. Two-year combination antibiotic therapy with clarithromycin, rifabutin, and clofazimine for Crohn's disease. Gastroenterology 2007; 132:2313-9; PMID:17570206; http://dx.doi.org/10.1053/j.gastro.2007.03.031
  • Elliott DE, Urban JJ, Argo CK, Weinstock JV. Does the failure to acquire helminthic parasites predispose to Crohn's disease? Faseb j 2000; 14:1848-55; PMID:10973934; http://dx.doi.org/10.1096/fj.99-0885hyp
  • Khan WI, Blennerhasset PA, Varghese AK, Chowdhury SK, Omsted P, Deng Y, Collins SM. Intestinal nematode infection ameliorates experimental colitis in mice. Infect Immun 2002; 70:5931-7; PMID:12379667; http://dx.doi.org/10.1128/IAI.70.11.5931-5937.2002
  • Elliott DE, Setiawan T, Metwali A, Blum A, Urban JF Jr, Weinstock JV. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur J Immunol 2004; 34:2690-8; PMID:15368285; http://dx.doi.org/10.1002/eji.200324833
  • Ashour DS, Othman AA, Shareef MM, Gaballah HH, Mayah WW. Interactions between Trichinella spiralis infection and induced colitis in mice. J Helminthol 2014; 88:210-8; PMID:23402295; http://dx.doi.org/10.1017/S0022149X13000059
  • Hasby EA, Hasby Saad MA, Shohieb Z, El Noby K. FoxP3+ T regulatory cells and immunomodulation after Schistosoma mansoni egg antigen immunization in experimental model of inflammatory bowel disease. Cell Immunol 2015; 295:67-76; PMID:25766778; http://dx.doi.org/10.1016/j.cellimm.2015.02.013
  • Glendinning L, Nausch N, Free A, Taylor DW, Mutapi F. The microbiota and helminths: sharing the same niche in the human host. Parasitology 2014; 141:1255-71; PMID:24901211; http://dx.doi.org/10.1017/S0031182014000699
  • Walk ST, Blum AM, Ewing SA, Weinstock JV, Young VB. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm Bowel Dis 2010; 16:1841-9; PMID:20848461; http://dx.doi.org/10.1002/ibd.21299
  • Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thompson R, Weinstock JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 2003; 98:2034-41; PMID:14499784; http://dx.doi.org/10.1111/j.1572-0241.2003.07660.x
  • Sandborn WJ, Elliott DE, Weinstock J, Summers RW, Landry-Wheeler A, Silver N, Harnett MD, Hanauer SB. Randomised clinical trial: the safety and tolerability of Trichuris suis ova in patients with Crohn's disease. Aliment Pharmacol Ther 2013; 38:255-63; PMID:23730956; http://dx.doi.org/10.1111/apt.12366
  • Helmby H. Human helminth therapy to treat inflammatory disorders - where do we stand? BMC Immunol 2015; 16:12; PMID:25884706; http://dx.doi.org/10.1186/s12865-015-0074-3
  • Croese J, O'Neil J, Masson J, Cooke S, Melrose W, Pritchard D, Speare R. A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 2006; 55:136-7; PMID:16344586; http://dx.doi.org/10.1136/gut.2005.079129
  • Lee SC, Tang MS, Lim YA, Choy SH, Kurtz ZD, Cox LM, Gundra UM, Cho I, Bonneau R, Blaser MJ, et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl Trop Dis 2014; 8:e2880; PMID:24851867; http://dx.doi.org/10.1371/journal.pntd.0002880
  • Cantacessi C, Giacomin P, Croese J, Zakrzewski M, Sotillo J, McCann L, Nolan MJ, Mitreva M, Krause L, Loukas A. Impact of experimental hookworm infection on the human gut microbiota. J Infect Dis 2014; 210:1431-4; PMID:24795483; http://dx.doi.org/10.1093/infdis/jiu256
  • Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007; 104:13780-5; PMID:17699621; http://dx.doi.org/10.1073/pnas.0706625104
  • Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012; 13:R79; http://dx.doi.org/10.1186/gb-2012-13-9-r79
  • Gevers D, Kugathasan S, Denson LA, Vázquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014; 15:382-92; http://dx.doi.org/10.1016/j.chom.2014.02.005
  • Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 2005; 43:3380-9; PMID:16000463; http://dx.doi.org/10.1128/JCM.43.7.3380-3389.2005
  • Knights D, Silverberg MS, Weersma RK, Gevers D, Dijkstra G, Huang H, Tyler AD, van Sommeren S, Imhann F, Stempak JM, et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med 2014; 6:107; PMID:25587358; http://dx.doi.org/10.1186/s13073-014-0107-1
  • Rutgeerts P, Goboes K, Peeters M, Hiele M, Penninckx F, Aerts R, Kerremans R, Vantrappen G. Effect of faecal stream diversion on recurrence of Crohn's disease in the neoterminal ileum. Lancet 1991; 338:771-4; PMID:1681159; http://dx.doi.org/10.1016/0140-6736(91)90663-A
  • Dey N, Soergel DA, Repo S, Brenner SE. Association of gut microbiota with post-operative clinical course in Crohn's disease. BMC Gastroenterol 2013; 13:131; PMID:23964800; http://dx.doi.org/10.1186/1471-230X-13-131
  • De Cruz P, Kang S, Wagner J, Buckley M, Sim WH, Prideaux L, Lockett T, McSweeney C, Morrison M, Kirkwood CD, 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; 30:268-78; PMID:25087692; http://dx.doi.org/10.1111/jgh.12694
  • Matijasic M, Mestrovic T, Peric M, Čipčić Paljetak H, Panek M, Vranešić Bender D, Ljubas Kelečić D, Krznarić Ž, Verbanac D. Modulating Composition and Metabolic Activity of the Gut Microbiota in IBD Patients. Int J Mol Sci 2016; 17:pii: E578. PMID:27104515
  • Sokol H. Probiotics and antibiotics in IBD. Dig Dis 2014; 32(Suppl 1):10-7; PMID:25531348; http://dx.doi.org/10.1159/000367820
  • Khan KJ, Ullman TA, Ford AC, et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol 2011; 106:661-73; http://dx.doi.org/10.1038/ajg.2011.72
  • Sutherland L, Singleton J, Sessions J, Hanauer S, Krawitt E, Rankin G, Summers R, Mekhjian H, Greenberger N, Kelly M, et al. Double blind, placebo controlled trial of metronidazole in Crohn's disease. Gut 1991; 32:1071-5; PMID:1916494; http://dx.doi.org/10.1136/gut.32.9.1071
  • Prantera C, Lochs H, Campieri M, Scribano ML, Sturniolo GC, Castiglione F, Cottone M. Antibiotic treatment of Crohn's disease: results of a multicentre, double blind, randomized, placebo-controlled trial with rifaximin. Aliment Pharmacol Ther 2006; 23:1117-25; PMID:16611272; http://dx.doi.org/10.1111/j.1365-2036.2006.02879.x
  • Wu XW, Ji HZ, Wang FY. Meta-analysis of ciprofloxacin in treatment of Crohn's disease. Biomed Rep 2015; 3:70-74
  • Henker J, Muller S, Laass MW, Schreiner A, Schulze J. Probiotic Escherichia coli Nissle 1917 (EcN) for successful remission maintenance of ulcerative colitis in children and adolescents: an open-label pilot study. Z Gastroenterol 2008; 46:874-5; http://dx.doi.org/10.1055/s-2008-1027463
  • Kruis W, Schutz E, Fric P, Fixa B, Judmaier G, Stolte M. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 1997; 11:853-8; PMID:9354192; http://dx.doi.org/10.1046/j.1365-2036.1997.00225.x
  • Kato K, Mizuno S, Umesaki Y, Ishii Y, Sugitani M, Imaoka A, Otsuka M, Hasunuma O, Kurihara R, Iwasaki A, et al. Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Aliment Pharmacol Ther 2004; 20:1133-41; http://dx.doi.org/10.1111/j.1365-2036.2004.02268.x
  • Zocco MA, dal Verme LZ, Cremonini F, Piscaglia AC, Nista EC, Candelli M, Novi M, Rigante D, Cazzato IA, Ojetti V, et al. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 2006; 23:1567-74; PMID:16696804; http://dx.doi.org/10.1111/j.1365-2036.2006.02927.x
  • Guslandi M. Saccharomyces boulardii plus rifaximin in mesalamine-intolerant ulcerative colitis. J Clin Gastroenterol 2010; 44:385. PMID:20104184
  • Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 2005; 100:1539-46; PMID:15984978; http://dx.doi.org/10.1111/j.1572-0241.2005.41794.x
  • Mardini HE, Grigorian AY. Probiotic mix VSL#3 is effective adjunctive therapy for mild to moderately active ulcerative colitis: a meta-analysis. Inflamm Bowel Dis 2014; 20:1562-7; http://dx.doi.org/10.1097/MIB.0000000000000084
  • Chapman TM, Plosker GL, Figgitt DP. VSL#3 probiotic mixture: a review of its use in chronic inflammatory bowel diseases. Drugs 2006; 66:1371-87; PMID:16903771; http://dx.doi.org/10.2165/00003495-200666100-00006
  • Maldonado-Gomez MX, Martinez I, Bottacini F, O'Callaghan A, Ventura M, van Sinderen D, Hillmann B, Vangay P, Knights D, Hutkins RW, et al. Stable Engraftment of Bifidobacterium longum AH1206 in the Human Gut Depends on Individualized Features of the Resident Microbiome. Cell Host Microbe 2016; 20:515-526; http://dx.doi.org/10.1016/j.chom.2016.09.001
  • Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 1958; 44:854-9; PMID:13592638
  • Khoruts A, Dicksved J, Jansson JK, Sadowsky MJ. Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea. J Clin Gastroenterol 2010; 44:354-60; PMID:20048681
  • Hamilton MJ, Weingarden AR, Unno T, Khoruts A, Sadowsky MJ. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes 2013; 4:125-35; PMID:23333862; http://dx.doi.org/10.4161/gmic.23571
  • Weingarden A, Gonzalez A, Vazquez-Baeza Y, Weiss S, Humphry G, Berg-Lyons D, Knights D, Unno T, Bobr A, Kang J, et al. Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection. Microbiome 2015; 3:10; PMID:25825673; http://dx.doi.org/10.1186/s40168-015-0070-0
  • Bojanova DP, Bordenstein SR. Fecal Transplants: What Is Being Transferred? PLoS Biol 2016; 14:e1002503; PMID:27404502; http://dx.doi.org/10.1371/journal.pbio.1002503
  • Bennet JD, Brinkman M. Treatment of ulcerative colitis by implantation of normal colonic flora. Lancet 1989; 1:164; PMID:2563083; http://dx.doi.org/10.1016/S0140-6736(89)91183-5
  • Borody TJ, Campbell J. Fecal microbiota transplantation: techniques, applications, and issues. Gastroenterol Clin North Am 2012; 41:781-803; PMID:23101687; http://dx.doi.org/10.1016/j.gtc.2012.08.008
  • Borody TJ, Warren EF, Leis S, Surace R, Ashman O. Treatment of ulcerative colitis using fecal bacteriotherapy. Journal of Clinical Gastroenterology 2003; 37:42-47; PMID:12811208; http://dx.doi.org/10.1097/00004836-200307000-00012
  • Borody T, Wettstein A, Campbell J, et al. Fecal microbiota transplantation in ulcerative colitis: Review of 24 years experience. Am J Gastronerol Conf 77th Annu Sci Meet Am Coll Gastroenterol 2012 Oct 19 - 24, Las Vegas, NV; 107:S665.
  • Kunde S, Pham A, Bonczyk S, Crumb T, Duba M, Conrad H Jr, Cloney D, Kugathasan S. Safety, tolerability, and clinical response after fecal transplantation in children and young adults with ulcerative colitis. J Pediatr Gastroenterol Nutr 2013; 56:597-601; PMID:23542823; http://dx.doi.org/10.1097/MPG.0b013e318292fa0d
  • 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; http://dx.doi.org/10.1097/MPG.0000000000000544
  • Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, Stollman N, Rohlke F, Surawicz C. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol 2012; 107:1079-87; PMID:22450732; http://dx.doi.org/10.1038/ajg.2012.60
  • Kump PK, Grochenig HP, Lackner S, Trajanoski S, Reicht G, Hoffmann KM, Deutschmann A, Wenzl HH, Petritsch W, Krejs GJ, et al. Alteration of intestinal dysbiosis by fecal microbiota transplantation does not induce remission in patients with chronic active ulcerative colitis. Inflamm Bowel Dis 2013; 19:2155-65; PMID:23899544;http://dx.doi.org/10.1097/MIB.0b013e31829ea325
  • Damman CJ, Brittnacher MJ, Hayden HS, et al. Single colonoscopically administered fecal microbiota transplant for ulcerative colitis-a pilot study to determine therapeutic benefit and graft stability. Paper presented at: Digestive Diseases Week 2014; 2014 May 3-6, Chicago, IL. Gastroenterology 2014:S-460
  • Vermeire S, Joossens M, Verbeke K, Wang J, Machiels K, Sabino J, Ferrante M, Van Assche G, Rutgeerts P, Raes J. Donor Species Richness Determines Faecal Microbiota Transplantation Success in Inflammatory Bowel Disease. J Crohns Colitis 2016; 10:387-94; http://dx.doi.org/10.1093/ecco-jcc/jjv203
  • Wei Y, Zhu W, Gong J, Guo D, Gu L, Li N, Li J. Fecal Microbiota Transplantation Improves the Quality of Life in Patients with Inflammatory Bowel Disease. Gastroenterol Res Pract 2015; 2015:517597; PMID:26146498; http://dx.doi.org/10.1155/2015/517597
  • Libertucci JW, Whelan FJ, Moayyedi P, et al. Investigating the microbiome pre and post fecal microbiota therapy from active ulcerative colitis patients in a randomized placebo controlled trial. Paper presented at: Digestive Diseases Week 2014; 2014 May 3-6, Chicago, IL. Gastroenterology 2014; 146:S-902; http://dx.doi.org/10.1016/S0016-5085(14)63280-7
  • Kahn SA, Rubin DT. When Subjects Violate the Research Covenant: Lessons Learned from a Failed Clinical Trial of Fecal Microbiota Transplantation. Am J Gastroenterol 2016; 111(11):1508-1510; PMID:27166127
  • Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch W, et al. Fecal Microbiota Transplantation Induces Remission in Patients With Active Ulcerative Colitis in a Randomized Controlled Trial. Gastroenterology 2015; 149(1):102-109; http://dx.doi.org/10.1053/j.gastro.2015.04.001
  • Rossen NG, Fuentes S, van der Spek MJ, Tijssen JG, Hartman JH, Duflou A, Löwenberg M, van den Brink GR, Mathus-Vliegen EM, de Vos WM, et al. Findings From a Randomized Controlled Trial of Fecal Transplantation for Patients With Ulcerative Colitis. Gastroenterology 2015; 149(1):110-118; PMID:25836986; http://dx.doi.org/10.1053/j.gastro.2015.03.045
  • Paramsothy S, Kamm MA, Walsh A, et al. 600 Multi Donor Intense Faecal Microbiota Transplantation is an Effective Treatment for Resistant Ulcerative Colitis: A Randomised Placebo-Controlled Trial. Paper presented at: Digestive Diseases Week 2016; 2016 May 21-24; San Diego, CA. Gastroenterology 2016; 150:S122-S123; http://dx.doi.org/10.1016/S0016-5085(16)30517-0
  • Kao D, Hotte N, Gillevet P, Madsen K. Fecal microbiota transplantation inducing remission in Crohn's colitis and the associated changes in fecal microbial profile. J Clin Gastroenterol 2014; 48:625-8; PMID:24667590;http://dx.doi.org/10.1097/MCG.0000000000000131
  • Vermeire S, Joossens M, Verbeke K, et al. Pilot Study on the safety and efficacy of faecal microbiota transplantation in refractory Crohn's disease. Paper presented at: Digestive Diseases Week 2012; 2012 May 19-22; San Diego, CA. Gastroenterology 2012; 142:S360; http://dx.doi.org/10.1016/S0016-5085(12)61356-0
  • Gordon H, Harbord M. A patient with severe Crohn's colitis responds to Faecal Microbiota Transplantation. J Crohns Colitis 2014; 8:256-7; PMID:24239403; http://dx.doi.org/10.1016/j.crohns.2013.10.007
  • Borody TJ, George L, Andrews P, Brandl S, Noonan S, Cole P, Hyland L, Morgan A, Maysey J, Moore-Jones D. Bowel-flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome? Med J Aust 1989; 150:604. PMID:2783214
  • 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; 19:7213-6; http://dx.doi.org/10.3748/wjg.v19.i41.7213
  • Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, Huang G, Liu Z, Wu P, Fan Z, 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; http://dx.doi.org/10.1111/jgh.12727
  • Suskind DL, Brittnacher MJ, Wahbeh G, Shaffer ML, Hayden HS, Qin X, Singh N, Damman CJ, Hager KR, Nielson H, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn's disease. Inflamm Bowel Dis 2015; 21:556-63; http://dx.doi.org/10.1097/MIB.0000000000000307
  • Vaughn BP, Vatanen T, Allegretti JR, Bai A, Xavier RJ, Korzenik J, Gevers D, Ting A, Robson SC, Moss AC. Increased Intestinal Microbial Diversity Following Fecal Microbiota Transplant for Active Crohn's Disease. Inflamm Bowel Dis 2016; 22:2182-90; PMID:27542133; http://dx.doi.org/10.1097/MIB.0000000000000893
  • Zella GC, Hait EJ, Glavan T, Gevers D, Ward DV, Kitts CL, Korzenik JR. Distinct microbiome in pouchitis compared to healthy pouches in ulcerative colitis and familial adenomatous polyposis. Inflamm Bowel Dis 2011; 17:1092-100; PMID:20845425; http://dx.doi.org/10.1002/ibd.21460
  • Young VB, Raffals LH, Huse SM, Vital M, Dai D, Schloss PD, Brulc JM, Antonopoulos DA, Arrieta RL, Kwon JH, et al. Multiphasic analysis of the temporal development of the distal gut microbiota in patients following ileal pouch anal anastomosis. Microbiome 2013; 1:9; http://dx.doi.org/10.1186/2049-2618-1-9
  • Landy J, Walker AW, Li JV, Al-Hassi HO, Ronde E, English NR, Mann ER, Bernardo D, McLaughlin SD, Parkhill J, et al. Variable alterations of the microbiota, without metabolic or immunological change, following faecal microbiota transplantation in patients with chronic pouchitis. Sci Rep 2015; 5:12955; PMID:26264409; http://dx.doi.org/10.1038/srep12955
  • Anderson JL, Edney RJ, Whelan K. Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther 2012; 36:503-16; PMID:22827693; http://dx.doi.org/10.1111/j.1365-2036.2012.05220.x
  • Sha S, Liang J, Chen M, Xu B, Liang C, Wei N, Wu K. Systematic review: faecal microbiota transplantation therapy for digestive and nondigestive disorders in adults and children. Aliment Pharmacol Ther 2014; 39:1003-32; PMID:24641570; http://dx.doi.org/10.1111/apt.12699
  • Colman RJ, Rubin DT. Fecal microbiota transplantation as therapy for inflammatory bowel disease: A systematic review and meta-analysis. J Crohns Colitis 2014; 8(12):1569-81; PMID:25223604
  • De Leon LM, Watson JB, Kelly CR. Transient flare of ulcerative colitis after fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol 2013; 11:1036-8; PMID:23669309; http://dx.doi.org/10.1016/j.cgh.2013.04.045
  • Fischer M, Kao D, Kelly C, Kuchipudi A, Jafri SM, Blumenkehl M, Rex D, Mellow M, Kaur N, Sokol H, 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; 22:2402-9; PMID:27580384; http://dx.doi.org/10.1097/MIB.0000000000000908
  • Khoruts A, Rank KM, Newman KM, Viskocil K, Vaughn BP, Hamilton MJ, Sadowsky MJ. Inflammatory Bowel Disease Affects the Outcome of Fecal Microbiota Transplantation for Recurrent Clostridium difficile Infection. Clin Gastroenterol Hepatol 2016; 14(10):1433-8; PMID:26905904; http://dx.doi.org/10.1016/j.cgh.2016.02.018
  • Ananthakrishnan AN. Epidemiology and risk factors for IBD. Nat Rev Gastroenterol Hepatol 2015; 12:205-17; PMID:25732745;http://dx.doi.org/10.1038/nrgastro.2015.34
  • Hilmi I, Jaya F, Chua A, Heng WC, Singh H, Goh KL. A first study on the incidence and prevalence of IBD in Malaysia–results from the Kinta Valley IBD Epidemiology Study. J Crohns Colitis 2015; 9:404-9; PMID:25744112; http://dx.doi.org/10.1093/ecco-jcc/jjv039
  • Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature 2012; 486:222-7; PMID:22699611
  • Rampelli S, Schnorr SL, Consolandi C, Turroni S, Severgnini M, Peano C, Brigidi P, Crittenden AN, Henry AG, Candela M. Metagenome Sequencing of the Hadza Hunter-Gatherer Gut Microbiota. Curr Biol 2015; 25:1682-93; PMID:25981789; http://dx.doi.org/10.1016/j.cub.2015.04.055
  • Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, Zech Xu Z, Van Treuren W, Knight R, Gaffney PM, et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat Commun 2015; 6:6505; http://dx.doi.org/10.1038/ncomms7505
  • Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature 2016; 529:212-5; PMID:26762459; http://dx.doi.org/10.1038/nature16504
  • Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 2014; 63:1275-83; PMID:24021287; http://dx.doi.org/10.1136/gutjnl-2013-304833
  • Wang W, Chen L, Zhou R, Wang X, Song L, Huang S, Wang G, Xia B. Increased proportions of Bifidobacterium and the Lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J Clin Microbiol 2014; 52:398-406; http://dx.doi.org/10.1128/JCM.01500-13
  • Takahashi K, Nishida A, Fujimoto T, Fujii M, Shioya M, Imaeda H, Inatomi O, Bamba S, Sugimoto M, Andoh A. Reduced Abundance of Butyrate-Producing Bacteria Species in the Fecal Microbial Community in Crohn's Disease. Digestion 2016; 93:59-65; http://dx.doi.org/10.1159/000441768

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.