6,507
Views
36
CrossRef citations to date
0
Altmetric
Review

MICROBIOTA INSIGHTS IN CLOSTRIDIUM DIFFICILE INFECTION AND INFLAMMATORY BOWEL DISEASE

, , , , , , & show all
Article: 1725220 | Received 07 Aug 2019, Accepted 27 Jan 2020, Published online: 04 Mar 2020

References

  • Rodriguez C, Van Broeck J, Taminiau B, Delmée M, Daube G. Clostridium difficile infection: early history, diagnosis and molecular strain typing methods. Microb Pathog. 2017;97:59–25. doi:10.1016/j.micpath.2016.05.018. PMID: 27238460.
  • Matsuoka K, Kobayashi T, Ueno F, Matsui T, Hirai F, Inoue N, Kato J, Kobayashi K, Koganei K, Kunisaki R, et al. Evidence-based clinical practice guidelines for inflammatory bowel disease. J Gastroenterol. 2018;53:305–353. doi:10.1007/s00535-018-1439-1. PMID: 29429045.
  • D´Aoust J, Battat R, Bessissow T. Management of inflammatory bowel disease with clostridium difficile infection. World J Gastroenterol. 2017;23:4986–5003. doi:10.3748/wjg.v23.i27.4986. PMID: 28785153.
  • Hourigan SK, Sears CL, Oliva-Hemker M. Clostridium difficile infection in pediatric inflammatory bowel disease. Inflamm Bowel Dis. 2016;22:1020–1025. doi:10.1097/MIB.0000000000000666. PMID: 26689599.
  • Li Y, Qian J, Queener E, Shen B. Risk factors and outcome of PCR-detected Clostridium difficile infection in ileal pouch patients. Inflamm Bowel Dis. 2013;19:397–403. doi:10.1097/MIB.0b013e318280fcb9. PMID: 23328770.
  • Regnault H, Bourrier A, Lalande V, Nion-Larmurier I, Sokol H, Seksik P, Barbut F, Cosnes J, Beaugerie L. Prevalence and risk factors of Clostridium difficile infection in patients hospitalized for flare of inflammatory bowel disease: a retrospective assessment. Dig Liver Dis. 2014;46:1086–1092. doi:10.1016/j.dld.2014.09.003. PMID: 25294795.
  • Vitikainen K, Haapamäki J, Färkklä M, Anttila VJ, Arkkila P. Clostridium difficile infection in patients with inflammatory bowel disease: a case control study. Scand J Gastroenterol. 2018;53:947–951. doi:10.1080/00365521.2018.1492012. PMID: 30041549.
  • Razik R, Rumman A, Bahreini Z, McGeer A, Nguyen GC. Recurrence of Clostridium difficile infection in patients with inflammatory bowel disease: the RECIDIVISM Study. Am J Gastroenterol. 2016;111:1141–1146. doi:10.1038/ajg.2016.187. PMID: 27215924.
  • Rao K, Higgins P. Epidemiology, diagnosis and management of Clostridium difficile infection in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2016;22:1744–1754. doi:10.1097/MIB.0000000000000793. PMID: 27120571.
  • Hall IC, O´Toole E. Intestinal flora in new-born infants with a description of a new pathogenic anaerobe, Bacillus difficilis. Am J Dis Child. 1935;49:309–402. doi:10.1001/archpedi.1935.01970020105010.
  • George RH, Symonds JM, Dimock F, Brown JD, Arabi Y, Shinagawa N, Keighley MR, Alexander-Willians J, Burdon DW. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J. 1978;1:695. doi:10.1136/bmj.1.6114.695. PMID: 630301.
  • George WL, Sutter VL, Goldstein EJ, Ludwig SL, Finegold SM. Aetiology of antimicrobial-agent-associated colitis. Lancet. 1978;1:802–803. doi:10.1016/s0140-6736(78)93001-5. PMID: 85818.
  • Perlmann P, Hammarström S, Lagercrantz R, Campbell D. Auto-antibodies to colon in rats and human ulcerative colitis: cross-reactivity with E. coli 014 antigen. Proc Soc Exptl Biol Med. 1967;125:975. doi:10.3181/00379727-125-32253. PMID: 15938314.
  • LaMont JT, Trnka YM. Therapeutic implications of Clostridium difficile toxin during relapse of chronic inflammatory bowel disease. Lancet. 1980;1(8165):381–383. doi:10.1016/s0140-6736(80)90939-3. PMID: 6101841.
  • Bolton RP, Sherriff RJ, Read AE. Clostridium difficile associated diarrhoea: a role in inflammatory bowel disease? Lancet. 1980;1(8165):383–384. doi:10.1016/s0140-6736(80)90940-x. PMID: 6101842.
  • Barlett JG. Clostridium difficile and inflammatory bowel disease. Gastroenterology. 1981;80(4):863–865. doi:10.1016/0016-5085(81)90154-2.
  • Keighley MR, Youngs D, Johnson M, Allan RN, Burdon DW. Clostridium difficile toxin in acute diarrhoea complicating inflammatory bowel disease. Gut. 1982;23:410–414. doi:10.1136/gut.23.5.410. PMID: 7076018.
  • Tvede M, Willumsen L. Clostridium difficile in patients with irritable bowel syndrome and ulcerative colitis. Lancet. 1982;1(8281):1124. doi:10.1016/s0140-6736(82)92305-4. PMID: 6122916.
  • Bolton RP, Read AE. Clostridium difficile in toxin megacolon complicating acute inflammatory bowel disease. Br Med J (Clin Res Ed). 1982;285(6340):475–476. doi:10.1136/BMJ.285.6340.475-a. PMID: 6809132.
  • Greenfield C, Aguilar-Ramirez JR, Pounder RE, Williams T, Danvers M, Marper SR. Clostridium difficile and inflammatory bowel disease. Gut. 1983;24(8):713–717. doi:10.1136/gut.24.8.713.
  • Gurian L, Klein K, Ward TT. Role of Clostridium difficile and Campylobacter jejuni in relapses of inflammatory bowel diseases. West J Med. 1983;138(3):359–360. PMID:6858121.
  • Pokorney BH, Nichols TW Jr. Pseudomembranous colitis. A complication of sulfasalazine therapy in a patient with Crohn´s colitis. Am J Gastroenterol. 1981;76(4):374–376. PMID: 6119900.
  • Browman RA, Riley TV. Routine culturing for Clostridium difficile? Pathology. 1984;16:240–242. doi:10.3109/00313028409068530. PMID: 6514390.
  • Hyams JS, McLaughlin JC. Lack of relationship between Clostridium difficile toxin and inflammatory bowel disease in children. J Clin Gastroenterol. 1985;7(5):387–390. doi:10.1097/00004836-198510000-00003. PMID: 4067226.
  • Gryboski JD. Clostridium difficile in inflammatory bowel disease relapse. J Pediatr Gastroenterol Nutr. 1991;13:39–41. doi:10.1097/00005176-199107000-00007. PMID: 1919950.
  • Kochhar R, Ayygari A, Goenka MK, Dhali GK, Aggarwai R, Mehta SK. Role of infectious agents in exacerbations of ulcerative colitis in India. A study of Clostridium difficile. J Clin Gastroenterol. 1993;16:26–30. doi:10.1097/00004836-199301000-00008. PMID: 8421140.
  • Tremaine WJ. Inflammatory bowel disease and Clostridium difficile-associated diarrhoea: a growing problem. Clin Gastroenterol Hepatol. 2007;5:310–311. doi:10.1016/j.cgh.2006.12.030.3. PMID: 17368229.
  • Issa M, Vijayapal A, Graham MB, Beaulieu DB, Otterson MF, Lundeen S, Skaros S, Weber LR, Komorowski RA, Knox JF, et al. Impact of Clostridium difficile on inflammatory bowel disease. Clin Gastroenterol Hepatol. 2007;5(3):345–351. doi:10.1016/j.cgh.2006.12.028. PMID: 17368234.
  • Ananthakrishnan AN, McGinley EL, Bionion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut. 2008;57(2):205–210. doi:10.1136/gut.2007.128231. PMID: 17905821.
  • Zilberbeg MD, Shorr AF, Kollef MH. Increase in Clostridium difficile-related hospitalizations among infants in the United States, 2000-2005. Pediatr Infect Dis J. 2008;27(12):1111–1113. doi:10.1097/inf.0b013e31817eef13. PMID: 19068517.
  • Issa M, Ananthakrishnan AN, Binion DG. Clostridium difficile and inflammatory bowel disease. Inflamm Bowel Dis. 2008;14(10):1432–1442. doi:10.1002/ibd.20500. PMID: 18484669.
  • DuPont HL, Garey K, Caeiro JP, Jiang ZD. New advances on Clostridium difficile infection: changing epidemiology, diagnosis, treatment and control. Curr Opin Infect Dis. 2008;21:500–507. doi:10.1097/qco.0b013e32830f9397. PMID: 18725800.
  • Ali S, Tamboli CP. Advances in epidemiology and diagnosis of inflammatory bowel diseases. Curr Gastr Rep. 2008;10(6):576–584. doi:10.1007/s11894-008-0105-9. PMID: 19006614.
  • Hermens DJ, Miner PB Jr. Exacerbation of ulcerative colitis. Gastroenterology. 1991;101(1):254–262. doi:10.1016/0016-5085(91)90487-6.
  • Torsten T, Gilbert J, Meyer F. Metagenomics -a guide from sampling to data analysis. Microb Inform Exp. 2012;2:3. doi:10.1186/2042-5783-2-3. PMID: 22587947.
  • Bajer L, Kuerka M, Kostovcik M, Macinga P, Dvorak J, Stehlikova Z, Brezina J, Wohl P, Spicak J, Drastich P. Distinct gut microbiota profiles in patients with primary sclerosing cholangitis and ulcerative colitis. World J Gastroenterol. 2017;23(25):4548–4558. doi:10.3748/wjg.v23.i25.4548. PMID: 28740343.
  • Alipour M, Zaidi D, Valcheva R, Jovel J, Martinez I, Sergi C, Walter J, Mason AL, Wong GK, Dieleman LA, et al. Mucosal barrier depletion and loss of bacterial diversity are primary abnormalities in paediatric ulcerative colitis. J Crohns Colitis. 2016;10(4):462–471. doi:10.1093/ecco-jcc/jiv223. PMID: 26660940.
  • 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(9):R79. doi:10.1186/gb-2012-13-9-r79. PMID: 23013615.
  • Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedmann M, McDonough P, Kim SG, et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn´s disease involving the ileum. Isme J. 2007;1(5):403–418. doi:10.1038/ismej.2007.52. PMID: 18043660.
  • 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-naïve microbioma in new-onset Crohn´s disease. Cell Host Microbe. 2014;15(3):382–392. doi:10.1016/j.chom.2014.02.005. PMID: 24629344.
  • Aden K, Rehman A, Waschina S, Pan WH, Walker A, Lucio M, Nunez AM, Bharti R, Zimmerman J, Bethge J, et al. Metabolic functions of gut microbes associate with efficacy of tumor necrosis factor antagonists in patients with inflammatory bowel disease. Gastroenterology. 2019;157(5):1279–1292. doi:10.1053/j.gastro.2019.07.025. PMID: 31326413.
  • Nemoto H, Kataoka K, Ishikawa H, Ikata K, Arimochi H, Iwasaki T, Ohnishi Y, Kuwchara T, Yasutomo K. Reduced diversity and imbalanced fecal microbiota in patients with ulcerative colitis. Dig Dis Sci. 2012;57(11):2955–2964. doi:10.1007/s10620-012-2236-y. PMID:22623042.
  • Kabeerdoss J, Jayakanthan P, Pugazhendhi S, Ramakrishna SB. Alterations of mucosal microbiota in the colon of patients with inflammatory bowel disease revealed by real time polymerase chain reaction amplification of 16S ribosomal ribonucleic acid. Indian J Med Res. 2015;142(1):23–32. doi:10.4103/0971-5916.162091. PMID: 26261163.
  • Danilova NA, Abdulkhakov SR, Grigoryeva TV, Markelova MI, Vailyev IY, Boulygina EA, Ardatskaya MD, Pavlenko AV, Tyakht AV, Odintsova AK, et al. Markers of dysbiosis in patients with ulcerative colitis and Crohn´s disease. Ter Arkh. 2019;91(4):17–24. doi:10.26442/00403660.2019.04.000211. PMID: 31094471.
  • Altomare A, Putignani L, Del Chierico F, Cocca S, Angeletti S, Ciccozzi M, Tripiciano C, Dalla Piccola B, Cicala M, Guarino MPL, et al. Gut mucosal-associated microbiota better discloses inflammatory bowel disease differential patterns than faecal microbiota. Dig Liver Dis. 2019;51(5):648–656. doi:10.1016/j.dld.2018.11.021. PMID: 30573380.
  • Imhann F, Vich Vila A, Bonder MJ, Fu J, Gevers D, Visschedijk MC, Spekhorst LM, Alberts R, Franke L, van Dullemen HM, et al. Interplay of host genetics and gut microbiota underlaying the onset and clinical presentation of inflammatory bowel disease. Gut. 2018;67(1):108–119. doi:10.1136/gutjnl-2016-312135. PMID: 27802154.
  • Shaw KA, Bertha M, Hofmekler T, Chopra P, Vatanen T, Srivatsa A, Prince J, Kumar A, Sauer C, Zwick ME. Dysbiosis, inflammation, and response to treatment: a longitudinal study of pediatric subjects with newly diagnosed inflammatory bowel disease. Genome Med. 2016;8(1):75. doi:10.1186/s13073-016-0331-y. PMID: 27412252.
  • Andoh A, Kuzuoka H, Tsujikawa T, Nakamura S, Hirai F, Suzuki Y, Matsui T, Fujiyama Y, Matsumoto T. Multicenter analysis of fecal microbiota profiles in Japanese patients with Crohn´s disease. J Gastroenterol. 2012;47(12):1298–1307. doi:10.007/s00535-012-0605-0. PMID:22576027.
  • 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. Fecal and mucosa microbiota profiling in irritable bowel syndrome and inflammatory bowel disease. Front Microbiol. 2019;10:1655. doi:10.3389/fmicb.2019.01655. PMID: 31379797.
  • Nishino K, Nishida A, Inoue R, Kawada Y, Ohno M, Skai S, Inatomi O, Bamba S, Sugimoto M, Kawahara M, et al. Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol. 2018;53(1):95–106. doi:10.1007/s00535-017-1384-4. PMID: 28852861.
  • Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier L, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, et al. Reduced diversity of faecal microbiota in Crohn´s disease revealed by a metagenomic approach. Gut. 2006;55(2):205–211. doi:10.1136/gut.2005.073817. PMID: 16188921.
  • Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel disease. Proc Natl Acad Sci USA. 2007;104(34):13780–13785. doi:10.1073/pnas.0706625104. PMID: 17699621.
  • Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett. 2002;217(2):133–139. doi:10.1111/J.1574-6968.2002.tb11467.x. PMID: 12480096.
  • Rajca S, Grondin V, Louis E, Venier-Massoville G, Grimaud JC, Bouhnik Y, Laharie D, Dupas JL, Pillant H, Picon L, et al. Alterations in the intestinal microbiome (dysbiosis) as a predictor of relapse after infliximab withdrawal in Crohn´s disease. Inflamm Bowel Dis. 2014;20(6):978–986. doi:10.1097/MIB.0000000000000036. PMID: 24788220.
  • Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, Timmis KN, Schreiber S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53(5):685–693. doi:10.101136/gut2003.025403. PMID: 15082587.
  • Lewis DJ, Chen EZ, Baldassson RN, Otley AR, Griffiths AN, Lee D, Bithinger K, Bailey A, Friedman ES, Hoffmann C, et al. Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn´s disease. Cell Host Microbe. 2015;18(4):489–500. doi:10.1016/j.chom.2015.09.008. PMID:26468751.
  • Halfvarson J, Brislawn CJ, Lamendella R, Vazquez-Baeza Y, Walters WA, Bramer LM, D´Amato M, Bonfiglio F, McDonald D, Gonzalez A, et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol. 2017;2:17004. doi:10.1038/nmicrobiol.2017.4. PMID: 28191884.
  • Rojas-Feria M, Romero-García T, Fernández Caballero-Rico JA, Pastor Ramírez H, Avilés-Recio M, Castro-Fernández M, Chueca Porcuna N, Romero-Gómez M, García F, Grande L, et al. Modulation of faecal metagenome in Crohn´s disease: role of microRNAs as biomarkers. World J Gastroenterol. 2018;24(46):5223–5233. doi:10.3748/wjg.v24.i46.5223. PMID: 30581271.
  • Andoh A, Imaeda H, Aomatsu T, Inatomi O, Bamba S, Sasaki M, Saito Y, Tsujikama T, Fujiyama Y. Comparison of the fecal microbiota profiles between ulcerative colitis and Crohn´s disease using terminal restriction fragment length polymorphism analysis. J Gastroenterol. 2011;46(4):479–486. doi:10.1007/s00535-010-0368-4. PMID: 21253779.
  • Knoll RL, Forslund K, Kultima JR, Meyer CU, Kullmer U, Sunagawa S, Bork P, Gehring S. 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. 2017;312(4):G327–G339. doi:10.1152/ajpgi.00293.2016. PMID: 28039159.
  • Franzosa EA, Sirota-Madi A, Avila-Pacheco J, Fornelos N, Haiser HJ, Reinker S, Vatanen T, Hall AB, Mallick H, Mclver LJ, et al. Gut microbiome structure and metabolic activity in inflammatory bowel disease. Natural Microbiol. 2019;4(2):293–305. doi:10.1038/s41564-018-0306-5. PMID: 30531976.
  • Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brisawn CJ, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel disease. Nature. 2019;569(7758):655–662. doi:10.1038/s41586-019-1237-9. PMID: 31142855.
  • Fujimoto T, Imaeda H, Takahashi K, Kasumi E, Bamba S, Fujiyama Y, Amdoh A. Decrease abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn´s disease. J Gastroenterol Hepatol. 2013;28(4):613–619. doi:10.1111/jgh.12073. PMID: 23216550.
  • Wright EK, Kamm MA, Wagner J, Teo SM, Cruz P, Hamilton AL, Ritchie KJ, Inouye M, Kirkwood CD. Microbial factors associated with postoperative Crohn´s disease recurrence. J Crohns Colitis. 2017;11(2):191–203. doi:10.1093/ecco-jcc/jjw136. PMID: 27466174.
  • Vaster-Andersen MK, Mirsepasi-Lauridsen HC, Prosberg MV, Mortensen CO, Träger C, Skovsen K, Thorkilgaard T, Nojgaard C, Vind I, Krogfelt KA, et al. Increased abundance of proteobacteria in aggressive Crohn´s disease seven years after diagnosis. Sci Rep. 2019;9(1):13473. doi:10.1038/s41598-019-49833-3. PMID: 31530835.
  • Swidsinski A, Loening-Baucke V, Vaneechoutte M, Doerffel Y. Active Crohn´s disease and ulcerative colitis can be specifically diagnosis and monitored based on the biostructure of fecal flora. Inflamm Bowel Dis. 2008;14(2):147–161. doi:10.101002/ibd.20330. PMID: 18050295.
  • Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. Mucolytic bacteria wit increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105(11):2420–2428. doi:10.1038/ajg.2010.281. PMID: 20648002.
  • Jacobs JP, Goudarzi M, Singh N, Tong M, McHardy IH, Rvegger P, Asadourian M, Moon B, Ayson A, Borneman Y, et al. A disease-associated microbial and metabolomics state in relatives of pediatric inflammatory bowel disease patients. Cell Mol Gastroenterol Hepatol. 2016;2(6):750–766. doi:10.1016/j.jcmgh.2016.06.004. PMID: 281747747.
  • Forbes JD, Van Domselaar G, Bernstein CN. Microbiome survey of the inflamed and non-inflamed gut at different compartments within the gastrointestinal tract of inflammatory bowel disease patients. Inflamm Bowel Dis. 2016;22(4):817–825. doi:10.1097/MIB.0000000000000684. PMID: 26937623.
  • Humbel F, Rieder JH, Franc Y, Juillerat P, Scharl M, Misselwitz B, Schreiner P, Begré S, Rogler G, von Känel R, et al. Association of alterations in intestinal microbiota with impaired psychological function in patients with inflammatory bowel disease in remission. Clin Gastroenterol Hepatol. 2019;20. PMID: 31546058. doi:10.1016/j.cgh.2019.09.022.
  • Lopez-Siles M, Enrich-Capó N, Aldeguer X, Sabat-Mir M, Duncan SH, Garcia-Gil LJ, Martinez-Medina M. Alterations in the abundance and co-occurrence of Akkermansia muciniphila and Faecalibacterium prausnitzii in the colonic mucosa of inflammatory bowel disease subjects. Front Cell Infect Microbiol. 2018;8:281. doi:10.3389/fcimb.2018.00281. PMID: 30245977.
  • Ring C, Klopfleisch R, Dahlke K, Basic M, Bleich A, Blaut M. Akkermansia nuciniphila strain ATCC BAA-835 does not promote short-term intestinal inflammation in gnotobiotic interleukin-10-deficient mice. Gut Microbes. 2019;10(2):180–203. doi:10.1080/19490976.2018.1511663. PMID: 30252588.
  • Geerlings SY, Kostopoulos I, de Vos WM, Belzer C. Akkermansia. muciniphila in the human gastrointestinal tract: when, where, and how? Microorganisms. 2018;6(3):75. doi:10.3390/microorganisms6030075. PMID: 30041463.
  • Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, K V, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63(8):1275–1283. doi:10.1136/gutjnl-2013-304833. PMID: 24021287.
  • Rajilic-Stojanovic M, Shanahan F, Guarner F, de Vos WM. Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis. 2013;19(3):481–488. doi:10.1097/MIB.0b013E31827fec6d. PMID: 23385241.
  • Sokol H, Jegou S, McQuitty C, Straub M, Leducq V, Landman C, Kirchgesner J, Le Gall G, Bourrier A, Nion-Larmurier I, et al. Specificities in the intestinal microbiota in patients with inflammatory bowel disease and Clostridium difficile infection. Gut Microbes. 2018;9(1):55–60. doi:10.1080/19490976.2017.1361092. PMID: 28786749.
  • Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. Short chain fatty acids (SCFAs)- mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277. doi:10.3389/fimmu.2019.00227. PMID: 30915065.
  • Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009;139(9):1619–1625. doi:10.3945/jn.109.104638. PMID:19625695.
  • Antharam VC, Li EC, Ishmael A, Sharma A, Mai V, Rand KH, Wang GP. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbial. 2013;51(9):2884–2892. doi:10.1128/JCM.00845-13. PMID: 23804381.
  • Wilson BC, Vatanen T, Cutfield WS, O´Sullivan JM. The Super-Donor Phenomenon in fecal microbiota transplantation. Front Cell Infect Microbiol. 2019;9:2. doi:10.3389/fcjmb.2019.00002. PMID: 30719428.
  • Kellingray L, Le Gall G, Defernez M, Beales ILP, Franslem-Elumogo N, Narbad A. Microbial taxonomic and metabolic alterations during faecal microbiota transplantation to treat Clostridium difficile infection. J Infect. 2018;77(2):107–118. doi:10.1016/j.jinf.2018.04.012. PMID: 29746938.
  • Collins J, Auchtung JM. Control of Clostridium difficile infection by defined microbial communities. Microbiol Spectr. 2017;5(5). doi:10.1128/microbiolspec.BAD-0009-2016. PMID: 28936948.
  • Hudson LE, Anderson SE, Corbett AH, Lamb TJ. Gleaning insights from fecal microbiota transplantation and probiotic studies for the rational design of combination microbial therapies. Clin Microbiol Rev. 2017;30(1):191–231. doi:10.1128/CMR.00049-16. PMID: 27856521.
  • Shankar V, Hamilton MJ, Khoruts A, Kilburn A, Unno T, Paliy O, Sadowsky MJ. Species and genus level resolution analysis of gut microbiota in Clostridium difficile patients following fecal microbiota transplantation. Microbiome. 2014;2:13. doi:10.1186/2049-2618-2-13. PMID: 24855561.
  • Amrane S, Hocquart M, Afouda P, Kuete E, Pham TPT, Dione N, Ngom II, Valles C, Banchar D, Raoult D, et al. Metagenomic and culturomic analysis of gut microbiota dysbiosis during Clostridium difficile infection. Sci Rep. 2019;9:12807. doi:10.1038/s41598-019-49189-8. PMID 31488869.
  • Mullish BH, JAK M, Pechlivanis A, Allegratti JR, Kao D, Barker GF, Kapila D, Petrof EO, Joyce SA, Gahan CGM, et al. Microbial bile salt hydrolases mediate the efficacy of faecal microbiota transplant in the treatment of recurrent Clostridioides difficile infection. Gut. 2019;11. PMID: 30816855. doi:10.1136/gutjnl-2018-317842.
  • Thoma C. Bile salt involved in the effectiveness of FMT for Clostridium difficile infection. Nat Rev Gastroenterol Hepatol. 2019;16(4):198. doi:10.1038/s41575-019-0128-8. PMID: 30837698.
  • Hatziioanou D, Gherghisan-Filip C, Saalbach G, Horn N, Wegmann U, Ducan SH, Flint HJ, Mayer MJ, Narbad A. Discovery of a novel lantibiotic nisin O from Blautia obeum A2-162, isolated from the human gastrointestinal tract. Microbiology. 2017;163(9):1292–1305. doi:10.1099/mic.0.000515. PMID: 28857034.
  • Tvede M, Rask-Madsen J. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet. 1989;1(8648):1156. doi:10.1016/s0140-6736(89)92749-9. PMID: 2566734.
  • Bäumer AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535(7610):85–93. doi:10.1038/nature18849. PMID: 27383983.
  • Ng SC, Kamm MA, Yeoh YK, Chan PKS, Zuo T, Tang W, Sood A, Andoh A, Ohmiya N, Zhou Y, et al. Scientific frontiers in faecal microbiota transplantation: joint document of Asia-Pacific association of gastroenterology (APAGE) and Asia-Pacific Society for digestive endoscopy (APSDE). Gut. 2019;14. PMID: 31611298. doi:10.1136/gutjnl-2019-319407.
  • Mirpuri J, Raetz M, Sturge CR, Wilhelm CL, Benson A, Savani RC, Hooper LV, Yarovinsky F. Proteobacteria-specific IgA regulates maturation of the intestinal microbiota. Gut Microb. 2014;5(1):28–39. doi:10.4161/gmic.26489. PMID: 24637807.
  • Ross CL, Spinter JK, Savidge TC. Structural and functional changes within the gut microbiota and susceptibility to Clostridium difficile infection. Anaerobe. 2016;41:37–43. doi:10.1016/j.anaerobe.2016.05.006. PMID: 2718006.
  • Ni J, Wu GD, Albenberg L, Tomov VT. Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol. 2017;14(10):573–584. doi:10.1038/nrgastro.2017.88. PMID: 28743984.
  • Pitts AC, Tuck LR, Faulds-Pain A, Lewis RJ, Marles-Wright J. Structural insight into the Clostridium difficile ethanolamine utilisation microcompartment. PLoS One. 2012;7(10):e48360. doi:10.1371/journal.pone.0048360. PMID: 23144756.
  • Stecher B. The roles of inflammation, nutrient availability and the commensal microbiota in enteric pathogen infection. Microbial Spectr. 2015;3(3). doi:10.1128/microbiolspec.MBP-0008-2014. PMID: 26185088.
  • Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature. 2013;502(7469):96–99. doi:10.1038/nature12503. PMID: 23995682.
  • Passmore IJ, Letertre MPM, Preston MD, Bianconi I, Harrison MA, Nasher F, Kaur H, Hong HA, Baines SD, Cutting SM, et al. Paracresol production by Clostridium difficile affects microbial diversity and membrane interplay of Gram-negative bacteria. PLoS One. 2018;14(9):e1007191. doi:10.1371/journal.ppat.1007191. PMID: 30208103.
  • Vidal-Lletjós S, Beaumont M, Torné D, Benamouzig R, Blachier F, Lan A. Dietary protein and amino acid supplementation in inflammatory bowel disease course: what impact on the colonic mucosa? Nutrients. 2017;9(3):310. doi:10.3390/nu9030310. PMID: 28335546.
  • Hellmann J, Andersen H, Fei L, Linn A, Bezold R, Lake K, Jackson K, Meyer D, Dirksing K, Bonkowski E, et al. Microbial shifts and shorter time to bowel resection surgery associated with C. difficile in pediatric Crohn´s disease. Inflamm Bowel Dis. 2019;14. PMID 31725875. doi:10.1093/ibd/izz263.
  • Crost EH, Tailford LE, Le Gall G, Fons M, Henrissat B, Juge N. Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus ls strain-dependent. PLoS One. 2013;8(10):e76341. doi:10.1371/journal.pone.0076341. PMID: 24204617.
  • Milani C, Ticinesi A, Gerritsen J, Nouvenne A, Lugli GA, Mancabelli L, Turroni F, Duranti S, Mangifecta M, Viappiani A, et al. Gut microbiota composition and Clostridium difficile infection in hospitalized elderly individuals: a metagenomic study. Sci Rep. 2016;6:25945. doi:10.1038/srep25945. PMID:27166072.
  • Shin JH, Gao Y, II JH M, Bolick DT, Kolling GL, Wu M, Warren CA. Innate Immune response and outcome of Clostridium difficile infection are dependent on fecal bacterial composition in the aged host. J Infect Dis. 2018;217(2):188–197. doi:10.1093/infdis/jix414. PMID:28968660.
  • 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(2):125–135. doi:10.4161/gmic.23571. PMID: 23333862.
  • Zhang X, Deeke SA, Ning Z, Starr AE, Butcher J, Li J, Mayne J, Cheng K, Liao B, Li L, et al. Metaproteomics reveals associations between microbiome and intestinal extracellular vesicle proteins in pediatric inflammatory bowel disease. Nat Commun. 2018;9:2873. doi:10.1038/s41467-018-05357-4. PMID: 30030445.
  • Cascio V, Gittings D, Merloni K, Hurton M, Laprade D, Austriaco N. S-Adenpsyl-L. Methionine protects the probiotic yeast, Saccharomyces boulardii, from acid-induced cell death. BMC Microbiol. 2013;13:35. doi:10.1186/1471-2180-13-35. PMID: 23402325.
  • Walker LJ, Aldhous MC, Drummond HE, Smith BR, Nimmo ER, Arnott ID, Satsangi J. Anti-Saccharomyces cerevisiae antibodies (ASCA) in Crohn´s disease are associated with disease severity but not NOD2/CARD15 mutations. Clin Exp Immunol. 2004;135(3):490–496. doi:10.1111/j.1365-2249.2003.02392.x. PMID: 15008984.
  • Levy AN, Allegretti JR. Insights into the role of transplantation for the treatment of inflammatory bowel disease. Therap Adv Gastroenterol. 2019;12. doi:10.1177/1756284819836893. PMID: 24241245.
  • Fisher 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 with inflammatory bowel disease. Inflamm Bowel Dis. 2016;22(10):2402–2409. doi:10.1097/MIB0000000000000908. PMID: 27580384.
  • Chin SM, Sauk J, Mahabamunuge J, Kaplan JL, Hohmann EL, Khalili H. Fecal microbiota transplantation for recurrent Clostridium difficile infection in patients with inflammatory bowel disease: a single center experience. Clin Gastroenterol Hepatol. 2017;15(4):597–599. doi:10.1016/j.cgh.2016.11.028. PMID: 27923723.
  • 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):1433–1438. doi:10.1016/j.cgh.2016.02.018. PMID: 26905904.
  • Meighani A, Hart BR, Bourgi K, Miller N, John A, Ramesh M. Outcome of fecal microbiota transplantation for Clostridium difficile infection in patients with IBD. Dig Dis Sci. 2017;62(10):2870–2875. doi:10.1007/s10620-017-4580-4. PMID: 28451916.
  • Kahn S, Kahn S, Kashyap P, Laine L, Rubin D, Atreja A, Moore T, Wu G. Update on FMT 2015: indications, methodologies, mechanisms and outlook. Gastroenterology. 2016;159(1):223–237. doi:10.1053/j.gastro.2015.05.008. PMID: 25982290.
  • Wang B, Zhang L, Zhu SW, Zhang JD, Duan LP. Short chain fatty acids contribute to gut microbiota-induced promotion of colonic melatonin receptor expression. J Biol Regul Homeost Agents. 2019;33(3):763–771. PMID:31204469.
  • Ling Z, Liu X, Jia X, Cheng Y, Luo Y, Yuan L, Wang Y, Zhao C, Guo S, Li L, et al. Impacts of infection with different toxigenic Clostridium difficile strains on feacal microbiota. Sci Rep. 2014;4:7485. doi:10.1038/srep07485. PMID: 25501371.
  • Li N, Tian H. Current research progress and thinking of fecal microbiota transplantation for the treatment of gastrointestinal disorders. Zhunghua Wei Chang Ke Za ZHi. 2017;20(10):1104–1108. PMID:29130220.
  • Qazi T, Amaratunga T, Barnes EL, Fisher M, Kassam Z, Allegretti JR. The risk of inflammatory bowel disease flares after fecal microbiota transplantation: systematic review and meta-analysis. Gut Microbes. 2017;8(6):574–588. doi:10.1080/19490976.2017.1353848. PMID: 28723262.
  • Terveer EM, van Gool T, Ooijevaar RE, Sanders IMJG, Boeije-Koppenol E, Keller JJ, Bart A, Kuijper EJ, Terveer EM, Vendrik K, et al. Human transmission of Blastocystis by fecal microbiota transplantation without development of gastrointestinal symptoms in recipients. Clin Infect Dis. 2019;15. PMID: 31728525. doi:10.1093/cid/ciz1122.
  • Zhang T, Lu G, Zhao Z, Liu Y, Shen Q, Li P, Chen Y, Yin H, Wang H, Marcella C, et al. Washed microbiota transplantation vs. manual fecal microbiota transplantation: clinical findings, animal studies and in vitro screening. Protein Cell. 2020;9. PMID: 31919742. doi:10.1007/s13238-019-00684-8.
  • Bassos PJ, NOS C, Sales-Campos H. Microbial-based therapies in the treatment of inflammatory bowel disease- an overview of human studies. Front Pharmacol. 2019;9:1571. doi:10.3389/fphar.2018.01571. PMID: 30687107.
  • Li Y, Liu M, Zhou J, Hou B, Su X, Liu Z, Yuan J, Li M. Bacillus licheniformis Zhengchangsheng attenuates DSS-induced colitis and modulates the gut microbiota in mice. Benef Microbes. 2019;10(5):543–553. doi:10.3920/BM2018.0122. PMID: 31122042.
  • Bjarnason I, Sission G, Hayee B. A randomised, double-blind, placebo-controlled trial of a multi-strain probiotic in patients with asymptomatic ulcerative colitis and Crohn’s disease. Inflammopharmacology. 2019;27(3):446–473. doi:10.1007/s10787-019-00595-4. PMID: 31054010.
  • Nagamine T, Matsumoto Y, Nakamura M. Combination probiotics may prevent Clostridium difficile infection among elderly patients undergoing an orthopedic surgery. Biosci Microbiota Food Health. 2019;38(1):31–33. doi:10.12938/bmfh.18-009. PMID: 30705800.
  • Mills JP, Rao K, Young VB. Probiotics for prevention of Clostridium difficile infection. Curr Opin Gastroenterol. 2018;34(1):3–10. doi:10.1097/MOG.0000000000000410. PMID: 29189354.
  • Dai D, Wang T, Wu S, Gao NL, Chen WH. Metabolic dependencies underlie interaction patterns of gut microbiota during enteropathogenesis. Front Microbiol. 2019;10:1205. doi:10.3389/fmicb.2019.01205. PMID: 31214144.