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Clostridioides difficile (formerly Clostridium difficile) infection in the critically ill: an expert statement

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Abstract

Clostridioides difficile (formerly Clostridium difficile) infection (CDI) represents a worrisome condition, often underestimated, with severe clinical presentations, frequently requiring intensive care unit (ICU) admission. The aim of the present expert statement was to give an overview of the management of CDI in critically ill patients, for whom CDI represents a redoubtable problem, in large part related to the use and abuse of antibiotics. The available knowledge about pathophysiology, risk factors, diagnosis and treatment concerning critical care patients affected by CDI has been reviewed, even though most of the existing information come from studies performed outside the ICU and the evidence on several issues in this specific context is scarce. The adoption of potential preventive and therapeutic strategies aimed to stem the phenomenon were discussed, including the faecal microbiota transplantation. This possibility could represent a highly interesting option in critically ill patients, but current evidence is limited and future well designed studies are needed. A special insight on the specific challenges that the ICU physicians may face caring for the critically ill patients with CDI was also proposed.

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Abbreviations

CD:

Clostridioides difficile

PMC:

Pseudomembranous colitis

CDI:

Clostridioides difficile infection

RT:

Ribotype

ECDC:

European Centre for Disease Prevalence and Control

EUCLID:

European, multicenter, prospective, biannual, point-prevalence study of CDI in hospitalized patients with diarrhea

CA-CDI:

Community-acquired Clostridium difficile infection

HA-CDI:

Hospital-acquired Clostridium difficile infection

NSAIDs:

Non steroideal anti-inflammatory drugs

PPIs:

Proton pump inhibitors

OR:

Odds ratio

CI:

Confidence interval

H2RAs:

H2 receptor antagonists

SUP:

Stress ulcer prophylaxis

RCTs:

Randomized controlled trials

ICU:

Intensive Care Unit

NAAT:

Nucleic acid amplification test

ELISA:

Enzyme-linked immunosorbent assay

GDH:

Glutamate dehydrogenase

ESCMID:

European society of clinical microbiology and infectious disease

NPV:

Negative predictive value

PPV:

Positive predictive value

PMs:

Pseudomembranes

CT:

Computed tomography

IDSA:

Infectious Diseases Society of America

NGT:

Nasogastric tube

FCDI:

Fulminant Clostridioides difficile infection

FMT:

Fecal microbiota transplantation

MDR:

Multi-drug resistant

COX:

Cyclooxygenase

References

  1. Curry S (2010) Clostridium difficile. Clin Lab Med 30(1):329–342. https://doi.org/10.1016/j.cll.2010.04.001

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sartelli M, Di Bella S, McFarland LV, Khanna S, Furuya-Kanamori L, Abuzeid N, Abu-Zidan FM, Ansaloni L, Augustin G, Bala M, Ben-Ishay O, Biffl WL, Brecher SM, Camacho-Ortiz A, Cainzos MA, Chan S, Cherry-Bukowiec JR, Clanton J, Coccolini F, Cocuz ME, Coimbra R, Cortese F, Cui Y, Czepiel J, Demetrashvili Z, Di Carlo I, Di Saverio S, Dumitru IM, Eckmann C, Eiland EH, Forrester JD, Fraga GP, Frossard JL, Fry DE, Galeiras R, Ghnnam W, Gomes CA, Griffiths EA, Guirao X, Ahmed MH, Herzog T, Kim JI, Iqbal T, Isik A, Itani KMF, Labricciosa FM, Lee YY, Juang P, Karamarkovic A, Kim PK, Kluger Y, Leppaniemi A, Lohsiriwat V, Machain GM, Marwah S, Mazuski JE, Metan G, Moore EE, Moore FA, Ordonez CA, Pagani L, Petrosillo N, Portela F, Rasa K, Rems M, Sakakushev BE, Segovia-Lohse H, Sganga G, Shelat VG, Spigaglia P, Tattevin P, Trana C, Urbanek L, Ulrych J, Viale P, Baiocchi GL, Catena F (2019) 2019 update of the WSES guidelines for management of Clostridioides (Clostridium) difficile infection in surgical patients. World J Emerg Surg WJES 14:8. https://doi.org/10.1186/s13017-019-0228-3

    Article  PubMed  Google Scholar 

  3. Killgore G, Thompson A, Johnson S, Brazier J, Kuijper E, Pepin J, Frost EH, Savelkoul P, Nicholson B, van den Berg RJ, Kato H, Sambol SP, Zukowski W, Woods C, Limbago B, Gerding DN, McDonald LC (2008) Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein A gene sequence typing. J Clin Microbiol 46(2):431–437. https://doi.org/10.1128/jcm.01484-07

    Article  CAS  PubMed  Google Scholar 

  4. Smith A (2005) Outbreak of Clostridium difficile infection in an English hospital linked to hypertoxin-producing strains in Canada and the US. Euro Surveill Bul Europeen sur les maladies transmissibles Eur Commun Dis Bull 10(E050630):050632. https://doi.org/10.2807/esw.10.26.02735-en

    Article  Google Scholar 

  5. Kuijper EJ, van den Berg RJ, Debast S, Visser CE, Veenendaal D, Troelstra A, van der Kooi T, van den Hof S, Notermans DW (2006) Clostridium difficile ribotype 027, toxinotype III, the Netherlands. Emerg Infect Dis 12(5):827–830. https://doi.org/10.3201/eid1205.051350

    Article  PubMed  PubMed Central  Google Scholar 

  6. Carl Suetens SH, Jana Kolman, Liselotte Diaz Högberg (2013) European Centre for Disease Prevention and Control. Point prevalence survey of healthcare- associated infections and antimicrobial use in European acute care hospitals. http://www.ecdc.europa.eu/en/publications/Publications/healthcare-associated-infections-antimicrobial-use-PPS.pdf

  7. Davies KA, Longshaw CM, Davis GL, Bouza E, Barbut F, Barna Z, Delmee M, Fitzpatrick F, Ivanova K, Kuijper E, Macovei IS, Mentula S, Mastrantonio P, von Muller L, Oleastro M, Petinaki E, Pituch H, Noren T, Novakova E, Nyc O, Rupnik M, Schmid D, Wilcox MH (2014) Underdiagnosis of Clostridium difficile across Europe: the European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea (EUCLID). Lancet Infect Dis 14(12):1208–1219. https://doi.org/10.1016/s1473-3099(14)70991-0

    Article  PubMed  Google Scholar 

  8. Davies KA, Ashwin H, Longshaw CM, Burns DA, Davis GL, Wilcox MH (2016) Diversity of Clostridium difficile PCR ribotypes in Europe: results from the European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea (EUCLID), 2012 and 2013. Euro Surveill Bull Europeen sur les maladies transmissibles Eur Commun Dis Bull. https://doi.org/10.2807/1560-7917.es.2016.21.29.30294

    Article  Google Scholar 

  9. Dubberke ER, Olsen MA (2012) Burden of Clostridium difficile on the healthcare system. Clin Infect Dis 55(Suppl 2):S88–92. https://doi.org/10.1093/cid/cis335

    Article  PubMed  PubMed Central  Google Scholar 

  10. Voth DE, Ballard JD (2005) Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 18(2):247–263. https://doi.org/10.1128/cmr.18.2.247-263.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lange K, Buerger M, Stallmach A, Bruns T (2016) Effects of antibiotics on gut microbiota. Dig Dis (Basel Switz) 34(3):260–268. https://doi.org/10.1159/000443360

    Article  Google Scholar 

  12. Brown KA, Khanafer N, Daneman N, Fisman DN (2013) Meta-analysis of antibiotics and the risk of community-associated Clostridium difficile infection. Antimicrob Agents Chemother 57(5):2326–2332. https://doi.org/10.1128/aac.02176-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Baur D, Gladstone BP, Burkert F, Carrara E, Foschi F, Dobele S, Tacconelli E (2017) Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis. Lancet Infect Dis 17(9):990–1001. https://doi.org/10.1016/s1473-3099(17)30325-0

    Article  PubMed  Google Scholar 

  14. Maseda D, Zackular JP, Trindade B, Kirk L, Roxas JL, Rogers LM, Washington MK, Du L, Koyama T, Viswanathan VK, Vedantam G, Schloss PD, Crofford LJ, Skaar EP, Aronoff DM (2019) Nonsteroidal anti-inflammatory drugs alter the microbiota and exacerbate Clostridium difficile colitis while dysregulating the inflammatory response. mBio. https://doi.org/10.1128/mbio.02282-18

    Article  PubMed  PubMed Central  Google Scholar 

  15. Cao F, Chen CX, Wang M, Liao HR, Wang MX, Hua SZ, Huang B, Xiong Y, Zhang JY, Xu YL (2018) Updated meta-analysis of controlled observational studies: proton-pump inhibitors and risk of Clostridium difficile infection. J Hosp Infect 98(1):4–13. https://doi.org/10.1016/j.jhin.2017.08.017

    Article  CAS  PubMed  Google Scholar 

  16. Azab M, Doo L, Doo DH, Elmofti Y, Ahmed M, Cadavona JJ, Liu XB, Shafi A, Joo MK, Yoo JW (2017) Comparison of the hospital-acquired Clostridium difficile infection risk of using proton pump inhibitors versus histamine-2 receptor antagonists for prophylaxis and treatment of stress ulcers: a systematic review and meta-analysis. Gut Liver 11(6):781–788. https://doi.org/10.5009/gnl16568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ro Y, Eun CS, Kim HS, Kim JY, Byun YJ, Yoo KS, Han DS (2016) Risk of Clostridium difficile infection with the use of a proton pump inhibitor for stress ulcer prophylaxis in critically Ill patients. Gut Liver 10(4):581–586. https://doi.org/10.5009/gnl15324

    Article  PubMed  PubMed Central  Google Scholar 

  18. Krag M, Marker S, Perner A, Wetterslev J, Wise MP, Schefold JC, Keus F, Guttormsen AB, Bendel S, Borthwick M, Lange T, Rasmussen BS, Siegemund M, Bundgaard H, Elkmann T, Jensen JV, Nielsen RD, Liboriussen L, Bestle MH, Elkjaer JM, Palmqvist DF, Backlund M, Laake JH, Badstolokken PM, Gronlund J, Breum O, Walli A, Winding R, Iversen S, Jarnvig IL, White JO, Brand B, Madsen MB, Quist L, Thornberg KJ, Moller A, Wiis J, Granholm A, Anthon CT, Meyhoff TS, Hjortrup PB, Aagaard SR, Andreasen JB, Sorensen CA, Haure P, Hauge J, Hollinger A, Scheuzger J, Tuchscherer D, Vuilliomenet T, Takala J, Jakob SM, Vang ML, Paelestik KB, Andersen KLD, van der Horst ICC, Dieperink W, Fjolner J, Kjer CKW, Solling C, Solling CG, Karttunen J, Morgan MPG, Sjobo B, Engstrom J, Agerholm-Larsen B, Moller MH (2018) Pantoprazole in patients at risk for gastrointestinal bleeding in the ICU. N Engl J Med 379(23):2199–2208. https://doi.org/10.1056/NEJMoa1714919

    Article  CAS  PubMed  Google Scholar 

  19. Selvanderan SP, Summers MJ, Finnis ME, Plummer MP, Ali Abdelhamid Y, Anderson MB, Chapman MJ, Rayner CK, Deane AM (2016) Pantoprazole or placebo for stress ulcer prophylaxis (POP-UP): randomized double-blind exploratory study. Crit Care Med 44(10):1842–1850. https://doi.org/10.1097/ccm.0000000000001819

    Article  CAS  PubMed  Google Scholar 

  20. Alhazzani W, Guyatt G, Alshahrani M, Deane AM, Marshall JC, Hall R, Muscedere J, English SW, Lauzier F, Thabane L, Arabi YM, Karachi T, Rochwerg B, Finfer S, Daneman N, Alshamsi F, Zytaruk N, Heel-Ansdell D, Cook D (2017) Withholding pantoprazole for stress ulcer prophylaxis in critically Ill patients: a pilot randomized clinical trial and meta-analysis. Crit Care Med 45(7):1121–1129. https://doi.org/10.1097/ccm.0000000000002461

    Article  PubMed  Google Scholar 

  21. Reynolds PM, MacLaren R (2019) Re-evaluating the utility of stress ulcer prophylaxis in the critically Ill patient: a clinical scenario-based meta-analysis. Pharmacotherapy 39(3):408–420. https://doi.org/10.1002/phar.2172

    Article  CAS  PubMed  Google Scholar 

  22. Hung YP, Tsai PJ, Hung KH, Liu HC, Lee CI, Lin HJ, Wu YH, Wu JJ, Ko WC (2012) Impact of toxigenic Clostridium difficile colonization and infection among hospitalized adults at a district hospital in southern Taiwan. PLoS One 7(8):e42415. https://doi.org/10.1371/journal.pone.0042415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tschudin-Sutter S, Carroll KC, Tamma PD, Sudekum ML, Frei R, Widmer AF, Ellis BC, Bartlett J, Perl TM (2015) Impact of toxigenic Clostridium difficile colonization on the risk of subsequent C. difficile infection in intensive care unit patients. Infect Control Hosp Epidemiol 36(11):1324–1329. https://doi.org/10.1017/ice.2015.177

    Article  PubMed  Google Scholar 

  24. Crobach MJ, Terveer EM, Kuijper EJ (2016) Effect of detecting and isolating asymptomatic Clostridium difficile carriers. JAMA Intern Med 176(10):1572–1573. https://doi.org/10.1001/jamainternmed.2016.5339

    Article  PubMed  Google Scholar 

  25. Longtin Y, Paquet-Bolduc B, Gilca R, Garenc C, Fortin E, Longtin J, Trottier S, Gervais P, Roussy JF, Levesque S, Ben-David D, Cloutier I, Loo VG (2016) Effect of detecting and isolating Clostridium difficile carriers at hospital admission on the incidence of C difficile infections: a quasi-experimental controlled study. JAMA Intern Med 176(6):796–804. https://doi.org/10.1001/jamainternmed.2016.0177

    Article  PubMed  Google Scholar 

  26. McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, Dubberke ER, Garey KW, Gould CV, Kelly C, Loo V, Shaklee Sammons J, Sandora TJ, Wilcox MH (2018) Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 Update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis 66(7):e1–e48. https://doi.org/10.1093/cid/cix1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chang VT, Nelson K (2000) The role of physical proximity in nosocomial diarrhea. Clin Infect Dis 31(3):717–722. https://doi.org/10.1086/314030

    Article  CAS  PubMed  Google Scholar 

  28. Cohen SH, Tang YJ, Muenzer J, Gumerlock PH, Silva J Jr (1997) Isolation of various genotypes of Clostridium difficile from patients and the environment in an oncology ward. Clin Infect Dis 24(5):889–893. https://doi.org/10.1093/clinids/24.5.889

    Article  CAS  PubMed  Google Scholar 

  29. Lawrence KL, Kollef MH (2009) Antimicrobial stewardship in the intensive care unit: advances and obstacles. Am J Respir Crit Care Med 179(6):434–438. https://doi.org/10.1164/rccm.200809-1394CP

    Article  PubMed  Google Scholar 

  30. Crobach MJ, Planche T, Eckert C, Barbut F, Terveer EM, Dekkers OM, Wilcox MH, Kuijper EJ (2016) European society of clinical microbiology and infectious diseases: update of the diagnostic guidance document for Clostridium difficile infection. Clinical microbiology and infection 22(Suppl 4):S63–81. https://doi.org/10.1016/j.cmi.2016.03.010

    Article  PubMed  Google Scholar 

  31. Gateau C, Couturier J, Coia J, Barbut F (2018) How to: diagnose infection caused by Clostridium difficile. Clin Microbiol Infect 24(5):463–468. https://doi.org/10.1016/j.cmi.2017.12.005

    Article  CAS  PubMed  Google Scholar 

  32. Fang FC, Polage CR, Wilcox MH (2017) Point-counterpoint: what is the optimal approach for detection of Clostridium difficile infection? J Clin Microbiol 55(3):670–680. https://doi.org/10.1128/jcm.02463-16

    Article  PubMed  PubMed Central  Google Scholar 

  33. Guerri S, Danti G, Frezzetti G, Lucarelli E, Pradella S, Miele V (2019) Clostridium difficile colitis: cT findings and differential diagnosis. Radiol Med (Torino). https://doi.org/10.1007/s11547-019-01066-0

    Article  Google Scholar 

  34. Burkart NE, Kwaan MR, Shepela C, Madoff RD, Wang Y, Rothenberger DA, Melton GB (2011) Indications and relative utility of lower endoscopy in the management of Clostridium difficile infection. Gastroenterol Res Pract 2011:626582. https://doi.org/10.1155/2011/626582

    Article  PubMed  PubMed Central  Google Scholar 

  35. Debast SB, Bauer MP, Kuijper EJ (2014) European Society of Clinical Microbiology and Infectious Diseases: update of the treatment guidance document for Clostridium difficile infection. J Clin Microbiol 20(Suppl 2):1–26. https://doi.org/10.1111/1469-0691.12418

    Article  CAS  Google Scholar 

  36. Al Momani LA, Abughanimeh O, Boonpheng B, Gabriel JG, Young M (2018) Fidaxomicin vs vancomycin for the treatment of a first episode of Clostridium difficile infection: a meta-analysis and systematic review. Cureus 10(6):e2778. https://doi.org/10.7759/cureus.2778

    Article  PubMed  PubMed Central  Google Scholar 

  37. Penziner S, Dubrovskaya Y, Press R, Safdar A (2015) Fidaxomicin therapy in critically ill patients with Clostridium difficile infection. Antimicrob Agents Chemother 59(3):1776–1781. https://doi.org/10.1128/aac.04268-14

    Article  PubMed  PubMed Central  Google Scholar 

  38. Rokas KE, Johnson JW, Beardsley JR, Ohl CA, Luther VP, Williamson JC (2015) The addition of intravenous metronidazole to oral vancomycin is associated with improved mortality in critically Ill patients with Clostridium difficile infection. Clin Infect Dis 61(6):934–941. https://doi.org/10.1093/cid/civ409

    Article  CAS  PubMed  Google Scholar 

  39. Gergely Szabo B, Kadar B, Szidonia Lenart K, Dezsenyi B, Kunovszki P, Fried K, Kamotsay K, Nikolova R, Prinz G (2016) Use of intravenous tigecycline in patients with severe Clostridium difficile infection: a retrospective observational cohort study. Clin Microbiol Infect 22(12):990–995. https://doi.org/10.1016/j.cmi.2016.08.017

    Article  CAS  PubMed  Google Scholar 

  40. Marra AR, Edmond MB, Wenzel RP, Bearman GM (2007) Hospital-acquired Clostridium difficile-associated disease in the intensive care unit setting: epidemiology, clinical course and outcome. BMC Infect Dis 7:42. https://doi.org/10.1186/1471-2334-7-42

    Article  PubMed  PubMed Central  Google Scholar 

  41. Karanika S, Paudel S, Zervou FN, Grigoras C, Zacharioudakis IM, Mylonakis E (2016) Prevalence and clinical outcomes of Clostridium difficile infection in the intensive care unit: a systematic review and meta-analysis. Open Forum Infect Dis. https://doi.org/10.1093/ofid/ofv186

    Article  PubMed  Google Scholar 

  42. Zahar JR, Schwebel C, Adrie C, Garrouste-Orgeas M, Francais A, Vesin A, Nguile-Makao M, Tabah A, Laupland K, Le-Monnier A, Timsit JF (2012) Outcome of ICU patients with Clostridium difficile infection. Crit Care (Lond Engl) 16(6):R215. https://doi.org/10.1186/cc11852

    Article  Google Scholar 

  43. Apisarnthanarak A, Razavi B, Mundy LM (2002) Adjunctive intracolonic vancomycin for severe Clostridium difficile colitis: case series and review of the literature. Clin Infect Dis 35(6):690–696. https://doi.org/10.1086/342334

    Article  PubMed  Google Scholar 

  44. Osman KA, Ahmed MH, Hamad MA, Mathur D (2011) Emergency colectomy for fulminant Clostridium difficile colitis: striking the right balance. Scand J Gastroenterol 46(10):1222–1227. https://doi.org/10.3109/00365521.2011.605469

    Article  CAS  PubMed  Google Scholar 

  45. Markelov A, Livert D, Kohli H (2011) Predictors of fatal outcome after colectomy for fulminant Clostridium difficile colitis: a 10-year experience. Am Surg 77(8):977–980

    PubMed  Google Scholar 

  46. Juo YY, Sanaiha Y, Jabaji Z, Benharash P (2019) Trends in diverting loop ileostomy vs total abdominal colectomy as surgical management for Clostridium difficile colitis. JAMA Surg. https://doi.org/10.1001/jamasurg.2019.2141

    Article  PubMed  PubMed Central  Google Scholar 

  47. Grundfest-Broniatowski S, Quader M, Alexander F, Walsh RM, Lavery I, Milsom J (1996) Clostridium difficile colitis in the critically ill. Dis Colon Rectum 39(6):619–623. https://doi.org/10.1007/bf02056938

    Article  CAS  PubMed  Google Scholar 

  48. Quraishi MN, Widlak M, Bhala N, Moore D, Price M, Sharma N, Iqbal TH (2017) Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Ther 46(5):479–493. https://doi.org/10.1111/apt.14201

    Article  CAS  PubMed  Google Scholar 

  49. Ianiro G, Maida M, Burisch J, Simonelli C, Hold G, Ventimiglia M, Gasbarrini A, Cammarota G (2018) Efficacy of different faecal microbiota transplantation protocols for Clostridium difficile infection: a systematic review and meta-analysis. United Eur Gastroenterol J 6(8):1232–1244. https://doi.org/10.1177/2050640618780762

    Article  Google Scholar 

  50. Prechter F, Katzer K, Bauer M, Stallmach A (2017) Sleeping with the enemy: Clostridium difficile infection in the intensive care unit. Crit Care (Lond Engl) 21(1):260. https://doi.org/10.1186/s13054-017-1819-6

    Article  Google Scholar 

  51. Gao T, He B, Pan Y, Deng Q, Sun H, Liu X, Chen J, Wang S, Xia Y (2015) Association of Clostridium difficile infection in hospital mortality: a systematic review and meta-analysis. Am J Infect Control 43(12):1316–1320. https://doi.org/10.1016/j.ajic.2015.04.209

    Article  PubMed  Google Scholar 

  52. Ianiro G, Masucci L, Quaranta G, Simonelli C, Lopetuso LR, Sanguinetti M, Gasbarrini A, Cammarota G (2018) Randomised clinical trial: faecal microbiota transplantation by colonoscopy plus vancomycin for the treatment of severe refractory Clostridium difficile infection-single versus multiple infusions. Aliment Pharmacol Ther 48(2):152–159. https://doi.org/10.1111/apt.14816

    Article  CAS  PubMed  Google Scholar 

  53. Cammarota G, Ianiro G, Magalini S, Gasbarrini A, Gui D (2015) Decrease in surgery for Clostridium difficile infection after starting a program to transplant fecal microbiota. Ann Intern Med 163(6):487–488. https://doi.org/10.7326/l15-5139

    Article  PubMed  Google Scholar 

  54. Fischer M, Sipe B, Cheng YW, Phelps E, Rogers N, Sagi S, Bohm M, Xu H, Kassam Z (2017) Fecal microbiota transplant in severe and severe-complicated Clostridium difficile: a promising treatment approach. Gut Microbes 8(3):289–302. https://doi.org/10.1080/19490976.2016.1273998

    Article  CAS  PubMed  Google Scholar 

  55. Kelly CR, Ihunnah C, Fischer M, Khoruts A, Surawicz C, Afzali A, Aroniadis O, Barto A, Borody T, Giovanelli A, Gordon S, Gluck M, Hohmann EL, Kao D, Kao JY, McQuillen DP, Mellow M, Rank KM, Rao K, Ray A, Schwartz MA, Singh N, Stollman N, Suskind DL, Vindigni SM, Youngster I, Brandt L (2014) Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol 109(7):1065–1071. https://doi.org/10.1038/ajg.2014.133

    Article  PubMed  PubMed Central  Google Scholar 

  56. Bilinski J, Grzesiowski P, Sorensen N, Madry K, Muszynski J, Robak K, Wroblewska M, Dzieciatkowski T, Dulny G, Dwilewicz-Trojaczek J, Wiktor-Jedrzejczak W, Basak GW (2017) Fecal microbiota transplantation in patients with blood disorders inhibits gut colonization with antibiotic-resistant bacteria: results of a prospective, single-center study. Clin Infect Dis 65(3):364–370. https://doi.org/10.1093/cid/cix252

    Article  CAS  PubMed  Google Scholar 

  57. Alagna L, Haak BW, Gori A (2019) Fecal microbiota transplantation in the ICU: perspectives on future implementations. Intensive Care Med 45(7):998–1001. https://doi.org/10.1007/s00134-019-05645-7

    Article  PubMed  Google Scholar 

  58. Cammarota G, Ianiro G, Tilg H, Rajilic-Stojanovic M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A, Segal J, Aloi M, Masucci L, Molinaro A, Scaldaferri F, Gasbarrini G, Lopez-Sanroman A, Link A, de Groot P, de Vos WM, Hogenauer C, Malfertheiner P, Mattila E, Milosavljevic T, Nieuwdorp M, Sanguinetti M, Simren M, Gasbarrini A (2017) European consensus conference on faecal microbiota transplantation in clinical practice. Gut 66(4):569–580. https://doi.org/10.1136/gutjnl-2016-313017

    Article  PubMed  Google Scholar 

  59. Dionne JC, Sullivan K, Mbuagbaw L, Takaoka A, Duan EH, Alhazzani W, Devlin JW, Duprey M, Moayyedi P, Armstrong D, Thabane L, Tsang JLY, Jaeschke R, Hamielec C, Karachi T, Cartin-Ceba R, Muscedere J, Alshahrani MSS, Cook DJ (2019) Diarrhoea: interventions, consequences and epidemiology in the intensive care unit (DICE-ICU): a protocol for a prospective multicentre cohort study. BMJ Open 9(6):e028237. https://doi.org/10.1136/bmjopen-2018-028237

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Anesthesiology, Intensive Care and Emergency Medicine, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy

    Massimo Antonelli & Maria Sole Vallecoccia

  2. Università Cattolica del Sacro Cuore, Rome, Italy

    Massimo Antonelli, Antonio Gasbarrini & Maria Sole Vallecoccia

  3. Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), St. James’s Hospital, St James Street, Dublin 8, Dublin, Ireland

    Ignacio Martin-Loeches

  4. Hospital Clinic, IDIBAPS, Universidad de Barcelona, Ciberes, Barcelona, Spain

    Ignacio Martin-Loeches

  5. Critical Care Department, ATTIKON University Hospital, Medical School, National and Kapodistrian University of Athens, Athens, Greece

    George Dimopoulos

  6. Department of Internal Medicine and Gastroenterology, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy

    Antonio Gasbarrini

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  1. Massimo Antonelli
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  2. Ignacio Martin-Loeches
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  3. George Dimopoulos
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  4. Antonio Gasbarrini
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  5. Maria Sole Vallecoccia
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Contributions

MA conceived the idea for the article. MA, IML, GD, AG and MSV drafted the manuscript. MA and MSV took care of the editing and supervised the work. MA, IML, GD, AG and MSV read and approved the final version.

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Correspondence to Massimo Antonelli.

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Antonelli, M., Martin-Loeches, I., Dimopoulos, G. et al. Clostridioides difficile (formerly Clostridium difficile) infection in the critically ill: an expert statement. Intensive Care Med 46, 215–224 (2020). https://doi.org/10.1007/s00134-019-05873-x

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