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Perspectives

Clostridioides difficile Infection in Patients with Inflammatory Bowel Disease May be Favoured by the Effects of Proinflammatory Cytokines on the Enteroglial Network

ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon
Pages 7443-7453 | Published online: 30 Dec 2021

References

  • Lawson PA, Citron DM, Tyrrell KL, Finegold SM. Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prévot 1938. Anaerobe. 2016;40:95–99. doi:10.1016/j.anaerobe.2016.06.008
  • Cho JM, Pardi DS, Khanna S. Update on treatment of Clostridioides difficile infection. Mayo Clin Proc. 2020;95(4):758–769. doi:10.1016/j.mayocp.2019.08.006
  • Fettucciari K, Marconi P, Marchegiani A, Fruganti A, Spaterna A, Bassotti G. Invisible steps for a global endemy: molecular strategies adopted by Clostridioides difficile. Therap Adv Gastroenterol. 2021;14:175628482110327. doi:10.1177/17562848211032797
  • Czepiel J, Dróżdż M, Pituch H, et al. Clostridium difficile infection: review. Eur J Clin Microbiol Infect Dis. 2019;38(7):1211–1221. doi:10.1007/s10096-019-03539-6
  • Yadav D, Khanna S. Safety of fecal microbiota transplantation for Clostridioides difficile infection focusing on pathobionts and SARS-CoV-2. Therap Adv Gastroenterol. 2021;14:1–11. doi:10.1177/17562848211009694
  • Shafiq M, Alturkmani H, Zafar Y, et al. Effects of co-infection on the clinical outcomes of Clostridium difficile infection. Gut Pathog. 2020;12(1). doi:10.1186/s13099-020-00348-7
  • Goudarzi M, Seyedjavadi SS, Goudarzi H, Mehdizadeh Aghdam E, Nazeri S. Clostridium difficile infection: epidemiology, pathogenesis, risk factors, and therapeutic options. Scientifica (Cairo). 2014;2014:1–9. doi:10.1155/2014/916826
  • Fettucciari K, Fruganti A, Marchegiani A, Brancorsini S, Marconi P, Bassotti G. Proinflammatory cytokines: possible accomplices for the systemic effects of Clostridioides difficile toxin b. J Inflamm Res. 2021;14:57–62. doi:10.2147/JIR.S287096
  • Di Bella S, Ascenzi P, Siarakas S, Petrosillo N, Di Masi A. Clostridium difficile toxins A and B: insights into pathogenic properties and extraintestinal effects. Toxins (Basel). 2016;8(5):134. doi:10.3390/toxins8050134
  • Kochan TJ, Foley MH, Shoshiev MS, Somers MJ, Carlson PE, Hanna PC. Updates to Clostridium difficile spore germination. J Bacteriol. 2018;200(16):1–12. doi:10.1128/JB.00218-18
  • Shen A. Clostridioides difficile spore formation and germination: new insights and opportunities for intervention. Annu Rev Microbiol. 2020;74(1):545–566. doi:10.1146/annurev-micro-011320-011321
  • Castro-Córdova P, Mora-Uribe P, Reyes-Ramírez R, et al. Entry of spores into intestinal epithelial cells contributes to recurrence of Clostridioides difficile infection. Nat Commun. 2021;12. doi:10.1038/s41467-021-21355-5
  • Sun X, Hirota SA. The roles of host and pathogen factors and the innate immune response in the pathogenesis of Clostridium difficile infection. Mol Immunol. 2015;63(2):193–202. doi:10.1016/j.molimm.2014.09.005
  • Oliva A, Aversano L, de Angelis M, et al. Persistent systemic microbial translocation, inflammation, and intestinal damage during Clostridioides difficile infection. Open Forum Infect Dis. 2020;7(1). doi:10.1093/ofid/ofz507
  • Dalal RS, Allegretti JR. Diagnosis and management of Clostridioides difficile infection in patients with inflammatory bowel disease. Curr Opin Gastroenterol. 2021;37(4):336–343. doi:10.1097/MOG.0000000000000739
  • Zhang T, Lin QY, Fei JX, et al. Clostridium difficile infection worsen outcome of hospitalized patients with inflammatory bowel disease. Sci Rep. 2016;6:1–9. doi:10.1038/srep29791
  • Khanna S. Management of Clostridioides difficile infection in patients with inflammatory bowel disease. Intest Res. 2021;19(3):265–274. doi:10.5217/ir.2020.00045
  • Chandrasekaran R, Lacy DB. The role of toxins in Clostridium difficile infection. FEMS Microbiol Rev. 2017;41(6):723–750. doi:10.1093/femsre/fux048
  • Sun X, Savidge T, Feng H. The enterotoxicity of Clostridium difficile toxins. Toxins (Basel). 2010;2(7):1848–1880. doi:10.3390/toxins2071848
  • Aktories K, Schwan C, Jank T. Clostridium difficile toxin biology. Annu Rev Microbiol. 2017;71(1):281–307. doi:10.1146/annurev-micro-090816-093458
  • Pruitt RN, Lacy DB. Toward a structural understanding of Clostridium difficile toxins A and B. Front Cell Infect Microbiol. 2012;2:28. doi:10.3389/fcimb.2012.00028
  • Rodriguez C, Taminiau B, Van Broeck J, Delmée M, Daube G. Clostridium difficile infection and intestinal microbiota interactions. Microb Pathog. 2015;89:201–209. doi:10.1016/j.micpath.2015.10.018
  • Darkoh C, Plants-Paris K, Bishoff D, DuPont HL. Clostridium difficile modulates the gut microbiota by inducing the production of indole, an interkingdom signaling and antimicrobial molecule. mSystems. 2019;4(2). doi:10.1128/msystems.00346-18
  • Rodríguez C, Romero E, Garrido-Sanchez L, et al. Microbiota insights in Clostridium difficile infection and inflammatory bowel disease. Gut Microbes. 2020;12(1):1725220. doi:10.1080/19490976.2020.1725220
  • Fettucciari K, Ponsini P, Gioè D, et al. Enteric glial cells are susceptible to Clostridium difficile toxin B. Cell Mol Life Sci. 2017;74(8):1527–1551. doi:10.1007/s00018-016-2426-4
  • Macchioni L, Davidescu M, Fettucciari K, et al. Enteric glial cells counteract Clostridium difficile toxin B through a NADPH oxidase/ROS/JNK/caspase-3 axis, without involving mitochondrial pathways. Sci Rep. 2017;7. doi:10.1038/srep45569
  • Fettucciari K, Macchioni L, Davidescu M, et al. Clostridium difficile toxin B induces senescence in enteric glial cells: a potential new mechanism of Clostridium difficile pathogenesis. Biochim Biophys Acta. 2018;1865(12):1945–1958. doi:10.1016/j.bbamcr.2018.10.007
  • Bassotti G, Macchioni L, Corazzi L, Marconi P, Fettucciari K. Clostridium difficile-related postinfectious IBS: a case of enteroglial microbiological stalking and/or the solution of a conundrum? Cell Mol Life Sci. 2018;75(7):1145–1149. doi:10.1007/s00018-017-2736-1
  • Bassotti G, Marchegiani A, Marconi P, Fettucciari K. The cytotoxic synergy between Clostridioides difficile toxin B and proinflammatory cytokines: an unholy alliance favoring the onset of Clostridioides difficile infection and relapses. Microbiologyopen. 2020;9(8). doi:10.1002/mbo3.1061
  • Bloomfield LE, Riley TV. Epidemiology and risk factors for community-associated Clostridium difficile infection: a narrative review. Infect Dis Ther. 2016;5(3):231–251. doi:10.1007/s40121-016-0117-y
  • Rahier JF, Magro F, Abreu C, et al. Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohn's Colitis. 2014;8(6):443–468. doi:10.1016/j.crohns.2013.12.013
  • Antonelli E, Baldoni M, Giovenali P, Villanacci V, Essatari M, Bassotti G. Intestinal superinfections in patients with inflammatory bowel diseases. J Crohn's Colitis. 2012;6:154–159. doi:10.1016/j.crohns.2011.07.012
  • Chen XL, Deng J, Chen X, Wan SS, Wang Y, Cao Q. High incidence and morbidity of Clostridium difficile infection among hospitalized patients with inflammatory bowel disease: a prospective observational cohort study. J Dig Dis. 2019;20(9):460–466. doi:10.1111/1751-2980.12798
  • Zhou F, Hamza T, Fleur AS, et al. Mice with inflammatory bowel disease are susceptible to Clostridium difficile infection with severe disease outcomes. Inflamm Bowel Dis. 2018;24(3):573–582. doi:10.1093/ibd/izx059
  • Flegel WA, Muller F, Daubener W, Fischer HG, Hadding U, Northoff H. Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect Immun. 1991;59(10):3659–3666. doi:10.1128/iai.59.10.3659-3666.1991
  • Abt MC, McKenney PT, Pamer EG. Clostridium difficile colitis: pathogenesis and host defence. Nat Rev Microbiol. 2016;14(10):609–620. doi:10.1038/nrmicro.2016.108
  • Wu X, Lai X, Tu H, Zou H, Cao J. Elevated serum CXCL10 in patients with Clostridium difficile infection are associated with disease severity. Int Immunopharmacol. 2019;72:92–97. doi:10.1016/j.intimp.2019.03.033
  • Salas A, Hernandez-Rocha C, Duijvestein M, et al. JAK–STAT pathway targeting for the treatment of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2020;17(6):323–337. doi:10.1038/s41575-020-0273-0
  • Leppkes M, Neurath MF. Cytokines in inflammatory bowel diseases – update 2020. Pharmacol Res. 2020;158:104835. doi:10.1016/j.phrs.2020.104835
  • Villanacci V, Cadei M, Lanzarotto F, et al. Localization of TNF alpha in ileocolonic biopsies of patients with inflammatory bowel disease. Ann Diagn Pathol. 2019;38:20–25. doi:10.1016/j.anndiagpath.2018.10.011
  • Pouillon L, Bossuyt P, Peyrin-Biroulet L. Considerations, challenges and future of anti-TNF therapy in treating inflammatory bowel disease. Expert Opin Biol Ther. 2016;16(10):1277–1290. doi:10.1080/14712598.2016.1203897
  • Gareb B, Otten AT, Frijlink HW, Dijkstra G, Kosterink JGW. Review: local tumor necrosis factor-α inhibition in inflammatory bowel disease. Pharmaceutics. 2020;12(6):1–31. doi:10.3390/pharmaceutics12060539
  • Strober W, Fuss IJ. Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases. Gastroenterology. 2011;140(6):1756–1767.e1. doi:10.1053/j.gastro.2011.02.016
  • Soufli I, Toumi R, Rafa H, Touil-Boukoffa C. Overview of cytokines and nitric oxide involvement in immuno-pathogenesis of inflammatory bowel diseases. World J Gastrointest Pharmacol Ther. 2016;7(3):353. doi:10.4292/wjgpt.v7.i3.353
  • Bassotti G, Villanacci V, Antonelli E, Morelli A, Salerni B. Enteric glial cells: new players in gastrointestinal motility? Lab Investig. 2007;87(7):628–632. doi:10.1038/labinvest.3700564
  • Grubišić V, Gulbransen BD. Enteric glia: the most alimentary of all glia. J Physiol. 2017;595(2):557–570. doi:10.1113/JP271021
  • Cabarrocas J, Savidge TC, Liblau RS. Role of enteric glial cells in inflammatory bowel disease. Glia. 2003;41(1):81–93. doi:10.1002/glia.10169
  • Bassotti G, Villanacci V, Nascimbeni R, et al. Enteric neuroglial apoptosis in inflammatory bowel diseases. J Crohn's Colitis. 2009;3(4):264–270. doi:10.1016/j.crohns.2009.06.004
  • Capoccia E, Cirillo C, Gigli S, et al. Enteric glia: a new player in inflammatory bowel diseases. Int J Immunopathol Pharmacol. 2015;28(4):443–451. doi:10.1177/0394632015599707
  • Villanacci V, Bassotti G, Nascimbeni R, et al. Enteric nervous system abnormalities in inflammatory bowel diseases. Neurogastroenterol Motil. 2008;20(9):1009–1016. doi:10.1111/j.1365-2982.2008.01146.x
  • Kermarrec L, Durand T, Neunlist M, Naveilhan P, Neveu I. Enteric glial cells have specific immunosuppressive properties. J Neuroimmunol. 2016;295–296:79–83. doi:10.1016/j.jneuroim.2016.04.011
  • Pochard C, Coquenlorge S, Freyssinet M, et al. The multiple faces of inflammatory enteric glial cells: is crohn’s disease a gliopathy? Am J Physiol. 2018;315(1):G1–G11. doi:10.1152/ajpgi.00016.2018
  • Fitzgibbon G, Mills KHG. The microbiota and immune-mediated diseases: opportunities for therapeutic intervention. Eur J Immunol. 2020;50(3):326–337. doi:10.1002/eji.201948322
  • Nitzan O, Elias M, Chazan B, Raz R, Saliba W. Clostridium difficile and inflammatory bowel disease: role in pathogenesis and implications in treatment. World J Gastroenterol. 2013;19(43):7577–7585. doi:10.3748/wjg.v19.i43.7577
  • Belkind-Gerson J, Graham HK, Reynolds J, et al. Colitis promotes neuronal differentiation of Sox2+ and PLP1+ enteric cells. Sci Rep. 2017;7(1). doi:10.1038/s41598-017-02890-y
  • Abhyankar MM, Ma JZ, Scully KW, et al. Immune profiling to predict outcome of Clostridioides difficile infection. MBio. 2020;11(3). doi:10.1128/mBio.00905-20
  • Dieterle MG, Putler R, Perry DA, et al. Systemic inflammatory mediators are effective biomarkers for predicting adverse outcomes in Clostridioides difficile infection. MBio. 2020;11(3). doi:10.1128/mBio.00180-20
  • Koon HW, Wang J, Mussatto CC, et al. Fidaxomicin and OP-1118 inhibit Clostridium difficile toxin A- and B-mediated inflammatory responses via inhibition of NF-κB activity. Antimicrob Agents Chemother. 2018;62(1). doi:10.1128/AAC.01513-17
  • Louie TJ, Miller MA, Mullane KM, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011;364:422–431. doi:10.1056/nejmoa0910812
  • Spiceland CM, Khanna S, Pardi DS. Outcomes with fidaxomicin therapy in Clostridium difficile infection. J Clin Gastroenterol. 2018;52(2):151–154. doi:10.1097/MCG.0000000000000769
  • Qiu H, Sun X, Sun M, He C, Li Z, Liu Z. Serum bacterial toxins are related to the progression of inflammatory bowel disease. Scand J Gastroenterol. 2014;49(7):826–833. doi:10.3109/00365521.2014.919018
  • Schneeweiss S, Korzenik J, Solomon DH, Canning C, Lee J, Bressler B. Infliximab and other immunomodulating drugs in patients with inflammatory bowel disease and the risk of serious bacterial infections. Aliment Pharmacol Ther. 2009;30:253–264. doi:10.1111/j.1365-2036.2009.04037.x
  • Ananthakrishnan AN, Oxford EC, Nguyen DD, Sauk J, Yajnik V, Xavier RJ. Genetic risk factors for Clostridium difficile infection in ulcerative colitis. Aliment Pharmacol Ther. 2013;38(5):522–530. doi:10.1111/apt.12425
  • Mazzuoli S, Guglielmi FW, Antonelli E, Salemme M, Bassotti G, Villanacci V. Definition and evaluation of mucosal healing in clinical practice. Dig Liver Dis. 2013;45(12):969–977. doi:10.1016/j.dld.2013.06.010
  • Gholam-Mostafaei FS, Yadegar A, Aghdaei HA, Azimirad M, Daryani NE, Zali MR. Anti-TNF containing regimens may be associated with increased risk of Clostridioides difficile infection in patients with underlying inflammatory bowel disease. Curr Res Transl Med. 2020;68:125–130. doi:10.1016/j.retram.2020.03.002
  • Seicean A, Moldovan-Pop A, Seicean R. Ulcerative colitis worsened after Clostridium difficile infection: efficacy of infliximab. World J Gastroenterol. 2014;20(17):5135–5140. doi:10.3748/wjg.v20.i17.5135