Top

Published in:

Open Access 01-12-2019 | Vancomycin | Review

2019 update of the WSES guidelines for management of Clostridioides (Clostridium) difficile infection in surgical patients

Authors: Massimo Sartelli, Stefano Di Bella, Lynne V. McFarland, Sahil Khanna, Luis Furuya-Kanamori, Nadir Abuzeid, Fikri M. Abu-Zidan, Luca Ansaloni, Goran Augustin, Miklosh Bala, Offir Ben-Ishay, Walter L. Biffl, Stephen M. Brecher, Adrián Camacho-Ortiz, Miguel A. Caínzos, Shirley Chan, Jill R. Cherry-Bukowiec, Jesse Clanton, Federico Coccolini, Maria E. Cocuz, Raul Coimbra, Francesco Cortese, Yunfeng Cui, Jacek Czepiel, Zaza Demetrashvili, Isidoro Di Carlo, Salomone Di Saverio, Irina M. Dumitru, Christian Eckmann, Edward H. Eiland, Joseph D. Forrester, Gustavo P. Fraga, Jean L. Frossard, Donald E. Fry, Rita Galeiras, Wagih Ghnnam, Carlos A. Gomes, Ewen A. Griffiths, Xavier Guirao, Mohamed H. Ahmed, Torsten Herzog, Jae Il Kim, Tariq Iqbal, Arda Isik, Kamal M. F. Itani, Francesco M. Labricciosa, Yeong Y. Lee, Paul Juang, Aleksandar Karamarkovic, Peter K. Kim, Yoram Kluger, Ari Leppaniemi, Varut Lohsiriwat, Gustavo M. Machain, Sanjay Marwah, John E. Mazuski, Gokhan Metan, Ernest E. Moore, Frederick A. Moore, Carlos A. Ordoñez, Leonardo Pagani, Nicola Petrosillo, Francisco Portela, Kemal Rasa, Miran Rems, Boris E. Sakakushev, Helmut Segovia-Lohse, Gabriele Sganga, Vishal G. Shelat, Patrizia Spigaglia, Pierre Tattevin, Cristian Tranà, Libor Urbánek, Jan Ulrych, Pierluigi Viale, Gian L. Baiocchi, Fausto Catena

Published in: World Journal of Emergency Surgery | Issue 1/2019

Abstract

In the last three decades, Clostridium difficile infection (CDI) has increased in incidence and severity in many countries worldwide. The increase in CDI incidence has been particularly apparent among surgical patients. Therefore, prevention of CDI and optimization of management in the surgical patient are paramount. An international multidisciplinary panel of experts from the World Society of Emergency Surgery (WSES) updated its guidelines for management of CDI in surgical patients according to the most recent available literature. The update includes recent changes introduced in the management of this infection.

Clements AC, Magalhães RJ, Tatem AJ, Paterson DL, Riley TV. Clostridium difficile PCR ribotype 027: assessing the risks of further worldwide spread. Lancet Infect Dis. 2010;10:395–404.PubMed

Lessa FC, Gould CV, McDonald LC. Current status of Clostridium difficile infection epidemiology. Clin Infect Dis. 2012;55:65–70.

Goudarzi M, Seyedjavadi SS, Goudarzi H, Mehdizadeh Aghdam E, Nazeri S. Clostridium difficile infection: epidemiology, pathogenesis, risk factors, and therapeutic options. Scientifica (Cairo). 2014;2014:916826.

To KB, Napolitano LM. Clostridium difficile infection: update on diagnosis, epidemiology, and treatment strategies. Surg Infect. 2014;15:490–502.

Eckmann C, Wasserman M, Latif F, Roberts G, Beriot-Mathiot A. Increased hospital length of stay attributable to Clostridium difficile infection in patients with four co-morbidities: an analysis of hospital episode statistics in four European countries. Eur J Health Econ. 2013;14:835–46.PubMed

Surawicz CM, Brandt LJ, Binion DG, Ananthakrishnan AN, Curry SR, Gilligan PH, McFarland LV, Mellow M, Zuckerbraun BS. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol. 2013;108:478–98.PubMed

Debast SB, Bauer MP, Kuijper EJ. European Society of Clinical Microbiology and Infectious Diseases. European Society of Clinical Microbiology and Infectious Diseases: update of the treatment guidance document for Clostridium difficile infection. Clin Microbiol Infect. 2014;20(Suppl 2):1–26.PubMed

Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:825–34.PubMed

Annual Epidemiological Report for 2016 Clostridium difficile infections. https://ecdc.europa.eu/sites/portal/files/documents/AER_for_2016-C-difficile.pdf. Accessed 11 Jan 2019.

10.

Honda H, Yamazaki A, Sato Y, Dubberke ER. Incidence and mortality associated with Clostridium difficile infection at a Japanese tertiary care Centre. Anaerobe. 2014;25:5–10.PubMed

11.

Riley TV, Kimura T. The epidemiology of Clostridium difficile infection in Japan: a systematic review. Infect Dis Ther. 2018;7:39–70.PubMedPubMedCentral

12.

Kim YS, Han DS, Kim YH, Kim WH, Kim JS, Kim HS, et al. Incidence and clinical features of Clostridium difficile infection in Korea: a nationwide study. Epidemiol Infect. 2013;141:189–94.PubMed

13.

Wong-McClure RA, Ramírez-Salas E, Mora-Brenes N, Aguero-Sandí L, Morera-Sigler M, Badilla-Vargas X, et al. Long term effect of infection control practices and associated factors during a major Clostridium difficile outbreak in Costa Rica. J Infect Dev Ctries. 2013;7:914–21.PubMed

14.

Legenza L, Barnett S, Rose W, Bianchini M, Safdar N, Coetzee R. Epidemiology and outcomes of Clostridium difficile infection among hospitalised patients: results of a multicentre retrospective study in South Africa. BMJ Glob Health. 2018;3(4):e000889.PubMedPubMedCentral

15.

Zerey M, Paton BL, Lincourt AE, Gersin KS, Kercher KW, Heniford BT. The burden of Clostridium difficile in surgical patients in the United States. Surg Infect. 2007;8:557–66.

16.

Halabi WJ, Nguyen VQ, Carmichael JC, Pigazzi A, Stamos MJ, Mills S. Clostridium difficile colitis in the United States: a decade of trends, outcomes, risk factors for colectomy, and mortality after colectomy. J Am Coll Surg. 2013;217:802–12.PubMed

17.

Herzog T, Deleites C, Belyaev O, Chromik AM, Uhl W. Clostridium difficile in visceral surgery. Chirurg. 2015;86:781–6.PubMed

18.

Abdelsattar ZM, Krapohl G, Alrahmani L, Banerjee M, Krell RW, Wong SL, et al. Postoperative burden of hospital-acquired Clostridium difficile infection. Infect Control Hosp Epidemiol. 2015;36:40–6.PubMedPubMedCentral

19.

Sartelli M, Malangoni MA, Abu-Zidan FM, Griffiths EA, Di Bella S, McFarland LV, et al. WSES guidelines for management of Clostridium difficile infection in surgical patients. World J Emerg Surg. 2015;10:38.PubMedPubMedCentral

20.

Guyatt G, Gutterman D, Baumann MH, Addrizzo-Harris D, Hylek EM, Phillips B, et al. Grading strength of recommendations and quality of evidence in clinical guidelines: report from an American College of Chest Physicians task force. Chest. 2006;129:174–81.PubMed

21.

Brozek JL, Akl EA, Jaeschke R, Lang DM, Bossuyt P, Glasziou P, et al. Grading quality of evidence and strength of recommendations in clinical practice guidelines: part 2 of 3. The GRADE approach to grading quality of evidence about diagnostic tests and strategies. Allergy. 2009;64:1109–16.PubMed

22.

Viscidi R, Willey S, Bartlett JG. Isolation rates and toxigenic potential of Clostridium difficile isolates from various patient populations. Gastroenterology. 1981;81:5–9.PubMed

23.

Samore MH, DeGirolami PC, Tlucko A, Lichtenberg DA, Melvin ZA, Karchmer AW. Clostridium difficile colonization and diarrhea at a tertiary care hospital. Clin Infect Dis. 1994;18:181–7.PubMed

24.

Walker KJ, Gilliland SS, Vance-Bryan K, Moody JA, Larsson AJ, Rotschafer JC, Guay DR. Clostridium difficile colonization in residents of long-term care facilities: prevalence and risk factors. J Am Geriatr Soc. 1993;41:940–6.PubMed

25.

Linsenmeyer K, O'Brien W, Brecher SM, Strymish J, Rochman A, Itani K, Gupta K. Clostridium difficile screening for colonization during an outbreak setting. Clin Infect Dis. 2018;67:1912–4.PubMed

26.

Cheng AC, Ferguson JK, Richards MJ, Robson JM, Gilbert GL, McGregor A, et al. Australasian Society for Infectious Diseases guidelines for the diagnosis and treatment of Clostridium difficile infection. Med J Aust. 2011;194:353–8.PubMed

27.

McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. NEJM. 1989;320:204–10.PubMed

28.

Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, et al. Emerging infections program healthcare-associated infections and antimicrobial use prevalence survey team. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014;370:1198–208.PubMedPubMedCentral

29.

Spigaglia P, Mastrantonio P, Barbanti F. Antibiotic resistances of Clostridium difficile. Adv Exp Med Biol. 2018;1050:137–59.PubMed

30.

Shaughnessy MK, Micielli RL, DePestel DD, Arndt J, Strachan CL, Welch KB, Chenoweth CE. Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect Control Hosp Epidemiol. 2011;32:201–6.PubMed

31.

Pruitt RN, Lacy DB. Toward a structural understanding of Clostridium difficile toxins a and B. Front Cell Infect Microbiol. 2012;2:28.PubMedPubMedCentral

32.

Jank T, Giesemann T, Aktories K. Rho-glucosylating Clostridium difficile toxins A and B: new insights into structure and function. Glycobiology. 2007;17:15R–22R.PubMed

33.

Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, Minton NP. The role of toxin A and toxin B in Clostridium difficile infection. Nature. 2010;467:711–3.PubMed

34.

Carter GP, Rood JI, Lyras D. The role of toxin A and toxin B in the virulence of Clostridium difficile. Trends Microbiol. 2012;20:21–9.PubMed

35.

Kuehne SA, Collery MM, Kelly ML, Cartman ST, Cockayne A, Minton NP. Importance of toxin A, toxin B, and CDT in virulence of an epidemic Clostridium difficile strain. J Infect Dis. 2014;209:83–6.PubMed

36.

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.

37.

Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, et al. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet. 2005;366:1079–84.PubMed

38.

Eckert C, Coignard B, Hebert M, Tarnaud C, Tessier C, Lemire A, et al. Clinical and microbiological features of Clostridium difficile infections in France: the ICD-RAISIN 2009 national survey. Med Mal Infect. 2013;43:67–74.PubMed

39.

Barbut F, Mastrantonio P, Delmée M, Brazier J, Kuijper E. Poxton I; European study group on Clostridium difficile (ESGCD). Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. Clin Microbiol Infect. 2007;13:1048–57.PubMed

40.

Bauer MP, Notermans DW, van Benthem BH, Brazier JS, Wilcox MH, Rupnik M, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet. 2011;377:63–73.PubMed

41.

De Rosa FG, Cavallerio P, Corcione S, Parlato C, Fossati L, Serra R, et al. Molecular characterization of toxigenic Clostridium difficile in a northern Italian hospital. Curr Microbiol. 2015;70:154–5.PubMed

42.

Geric B, Johnson S, Gerding DN, Grabnar M, Rupnik M. Frequency of binary toxin genes among Clostridium difficile strains that do not produce large clostridial toxins. J Clin Microbiol. 2003;41:5227–32.PubMedPubMedCentral

43.

Barth H. Uptake of binary actin ADP-ribosylating toxins. Rev Physiol Biochem Pharmacol. 2004;152:165–82.PubMed

44.

Bacci S, Mølbak K, Kjeldsen MK, Olsen KE. Binary toxin and death after clostridium difficile infection. Emerg Infect Dis. 2011;17:976–82.PubMedPubMedCentral

45.

Sundriyal A, Roberts AK, Ling R, McGlashan J, Shone CC, Acharya KR. Expression, purification and cell cytotoxicity of actin-modifying binary toxin from Clostridium difficile. Protein Expr Purif. 2010;74:42–8.PubMed

46.

Furuya-Kanamori L, Marquess J, Yakob L, Riley TV, Paterson DL, Foster NF, et al. Asymptomatic Clostridium difficile colonization: epidemiology and clinical implications. BMC Infect Dis. 2015;15:516.PubMedPubMedCentral

47.

Crobach MJT, Vernon JJ, Loo VG, Kong LY, Péchiné S, Wilcox MH, Kuijper EJ. Understanding Clostridium difficile colonization. Clin Microbiol Rev. 2018;31(2):e00021.PubMedPubMedCentral

48.

Zacharioudakis IM, Zervou FN, Pliakos EE, Ziakas PD, Mylonakis E. Colonization with toxinogenic C. difficile upon hospital admission, and risk of infection: a systematic review and meta-analysis. Am J Gastroenterol. 2015;110:381–90.PubMed

49.

Riley TV, Collins DA, Karunakaran R, Kahar MA, Adnan A, Hassan SA, et al. High prevalence of toxigenic and nontoxigenic Clostridium difficile strains in Malaysia. J Clin Microbiol. 2018;56(6):e00170.PubMedPubMedCentral

50.

McNamara SE, Abdujamilova N, Somsel P, Gordoncillo MJ, DeDecker JM, Bartlett PC. Carriage of Clostridium difficile and other enteric pathogens among a 4-H avocational cohort. Zoonoses Public Health. 2011;58:192–9.PubMed

51.

Arvand M, Moser V, Schwehn C, Bettge-Weller G, Hensgens MP, Kuijper EJ. High prevalence of Clostridium difficile colonization among nursing home residents in Hesse Germany. PLoS One. 2012;7:e30183.PubMedPubMedCentral

52.

Aronsson B, Mollby R, Nord CE. Antimicrobial agents and Clostridium difficile in acute enteric disease: epidemiological data from Sweden, 1980-1982. J Infect Dis. 1985;151:476–81.PubMed

53.

Kato H, Kita H, Karasawa T, Maegawa T, Koino Y, Takakuwa H, et al. Colonisation and transmission of Clostridium difficile in healthy individuals examined by PCR ribotyping and pulsed-field gel electrophoresis. J Med Microbiol. 2001;50:720–7.PubMed

54.

Galdys AL, Nelson JS, Shutt KA, Schlackman JL, Pakstis DL, Pasculle AW, et al. Prevalence and duration of asymptomatic Clostridium difficile carriage among healthy subjects in Pittsburgh Pennsylvania. J Clin Microbiol. 2014;52:2406–9.PubMedPubMedCentral

55.

Stojanović P, Stojanović N, Kocic B, Stanković-Dordević D, Babić T, Stojanović K. Asymptomatic carriers of Clostridium difficile in serbian population. Cent Eur J Med. 2012;7:769–74.

56.

Loo VG, Bourgault AM, Poirier L, Lamothe F, Michaud S, Turgeon N, et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med. 2011;365:1693–703.PubMed

57.

McFarland LV. Renewed interest in a difficult disease: Clostridium difficile infections—epidemiology and current treatment strategies. Curr Opin Gastroenterol. 2009;25:24–35.PubMed

58.

Vecchio AL, Zacur GM. Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options. Curr Opin Gastroenterol. 2012;28:1–9.PubMed

59.

Hassan SA, Rahman RA, Huda N, Wan Bebakar WM, Lee YY. Hospital-acquired Clostridium difficile infection among patients with type 2 diabetes mellitus in acute medical wards. J R Coll Physicians Edinb. 2013;43:103–7.PubMed

60.

Sanders NL, Bollinger RR, Lee R, Thomas S, Parker W. Appendectomy and Clostridium difficile colitis: relationships revealed by clinical observations and immunology. World J Gastroenterol. 2013;19:5607–14.PubMedPubMedCentral

61.

Seretis C, Seretis F, Goonetilleke K. Appendicectomy and clostridium difficile infection: is there a link? J Clin Med Res. 2014;6:239–41.PubMedPubMedCentral

62.

Clanton J, Subichin M, Drolshagen K, Daley T, Firstenberg MS. Fulminant Clostridium difficile infection: an association with prior appendectomy? World J Gastrointest Surg. 2013;27:233–8.

63.

Yong FA, Alvarado AM, Wang H, Tsai J, Estes NC. Appendectomy: a risk factor for colectomy in patients with Clostridium difficile. Am J Surg. 2015;209:532–5.PubMed

64.

Khanna S, Baddour LM, Dibaise JK, Pardi DS. Appendectomy is not associated with adverse outcomes in clostridium difficile infection: a population-based study. Am J Gastroenterol. 2013;108:626–7.PubMed

65.

Huang H, Wu S, Chen R, Xu S, Fang H, Weintraub A, Nord CE. Risk factors of Clostridium difficile infections among patients in a university hospital in Shanghai, China. Anaerobe. 2014;30:65–9.PubMed

66.

Walker AS, Eyre DW, Wyllie DH, Dingle KE, Harding RM, O'Connor L, et al. Characterisation of Clostridium difficile hospital ward-based transmission using extensive epidemiological data and molecular typing. PLoS Med. 2012;9:e1001172.PubMedPubMedCentral

67.

Theriot CM, Young VB. Microbial and metabolic interactions between the gastrointestinal tract and Clostridium difficile infection. Gut Microbes. 2014;5:86–95.PubMed

68.

Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13:321–35.PubMed

69.

Pérez-Cobas AE, Artacho A, Ott SJ, Moya A, Gosalbes MJ, Latorre A. Structural and functional changes in the gut microbiota associated to Clostridium difficile infection. Front Microbiol. 2014;5:335.PubMedPubMedCentral

70.

Kamada N, Chen GY, Inohara N, Núñez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14:685–90.PubMedPubMedCentral

71.

Tedesco FJ, Barton RW, Alpers DH. Clindamycin-associated colitis: a prospective study. Ann Intern Med. 1974;81:429–33.PubMed

72.

Bartlett JG, Onderdonk AB, Cisneros RL, Kasper DL. Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. In: Bartlett JG, Onderdonk AB, Cisneros RL, Kasper DL, editors. J Infect Dis. 2004;190:202–9. CommentaryPubMed

73.

Hensgens MP, Goorhuis A, Dekkers OM, Kuijper EJ. Time interval of increased risk for Clostridium difficile infection after exposure to antibiotics. J Antimicrob Chemother. 2012;67:742–8.PubMed

74.

Kazakova SV, Ware K, Baughman B, Bilukha O, Paradis A, Sears S, et al. A hospital outbreak of diarrhea due to an emerging epidemic strain of Clostridium difficile. Arch Intern Med. 2006;166:2518–24.PubMed

75.

Muto CA, Pokrywka M, Shutt K, Mendelshon AB, Nouri K, Posey K, et al. A large outbreak of Clostridium difficile–associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol. 2005;26:273–80.PubMed

76.

Loo VG, Poirier L, Miller MA, Oughton M, Libman MB, Michaud S, et al. A predominately clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med. 2005;353:2442–9.PubMed

77.

Pépin J, Saheb N, Coulombe MA, Alary ME, Corriveau MP, Authier S, et al. Emergence of fluoroquinolones as the predominant risk factor for Clostridium difficile-associated diarrhea: a cohort study during an epidemic in Quebec. Clin Infect Dis. 2005;41:1254–60.PubMed

78.

Dubberke ER, Reske KA, Yan Y, Olsen MA, McDonald LC, Fraser VJ. Clostridium difficile-associated disease in a setting of endemicity: identification of novel risk factors. Clin Infect Dis. 2007;45:1543–9.PubMed

79.

Owens RC, Donskey CJ, Gaynes RP, Loo VG, Muto CA. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin Infect Dis. 2008;46:19–31.

80.

McCusker ME, Harris AD, Perencevich E, Roghmann M. Fluoroquinolone use and Clostridium difficile-associated diarrhea. Emerg Infect Dis. 2003;9:730–3.PubMedPubMedCentral

81.

Gerding DN, Olson MM, Peterson LR, Teasley LR, Gebhard RL, Schwartz ML, Lee JT Jr. Clostridium difficile-associated diarrhea and colitis in adults. Arch Intern Med. 1986;146:95–100.PubMed

82.

Brown E, Talbot GH, Axelrod P, Provencher M, Hoegg C. Risk factors for Clostridium difficile toxin-associated diarrhea. Infect Control Hosp Epidemiol. 1990;11:283–90.PubMed

83.

Oldfield EC IV, Oldfield EC III, Johnson DA. Clinical update for the diagnosis and treatment of Clostridium difficile infection. World J Gastrointest Pharmacol Ther. 2014;5:1–26.PubMed

84.

Privitera G, Scarpellini P, Ortisi G, Nicastro G, Nicolin R, De Lalla F. Prospective study of Clostridium difficile intestinal colonization and disease following single-dose antibiotic prophylaxis in surgery. Antimicrob Agents Chemother. 1991;35:208–10.PubMedPubMedCentral

85.

Yee J, Dixon CM, McLean AP, Meakins JL. Clostridium difficile disease in a department of surgery. The significance of prophylactic antibiotics. Arch Surg. 1991;126:241–6.PubMed

86.

Al-Obaydi W, Smith CD, Foguet P. Changing prophylactic antibiotic protocol for reducing Clostridium difficile-associated diarrhoeal infections. J Orthop Surg (Hong Kong). 2010;18:320–3.

87.

Cunningham R, Dale B, Undy B, Gaunt N. Proton pump inhibitors as a risk factor for Clostridium difficile diarrhoea. J Hosp Infect. 2003;54:243–5.PubMed

88.

Dial S, Alrasadi K, Manoukian C, Huang A, Menzies D. Risk of Clostridium difficile diarrhea among hospital inpatients prescribed proton pump inhibitors: cohort and case-control studies. CMAJ. 2004;171:33–8.PubMedPubMedCentral

89.

Kwok CS, Arthur AK, Anibueze CI, Singh S, Cavallazzi R, Loke YK. Risk of Clostridium difficile infection with acid suppressing drugs and antibiotics: meta-analysis. Am J Gastroenterol. 2012;107:1011–9.PubMed

90.

Shah S, Lewis A, Leopold D, Dunstan F, Woodhouse K. Gastric acid suppression does not promote clostridial diarrhoea in the elderly. QJM. 2000;93:175–81.PubMed

91.

Cao F, Chen CX, Wang M, Liao HR, Wang MX, Hua SZ, et al. Updated meta-analysis of controlled observational studies: proton-pump inhibitors and risk of Clostridium difficile infection. J Hosp Infect. 2018;98:4–13.PubMed

92.

Azab M, Doo L, Doo DH, Elmofti Y, Ahmed M, Cadavona JJ, et al. 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. 2017;11:781–8.PubMedPubMedCentral

93.

Wijarnpreecha K, Sornprom S, Thongprayoon C, Phatharacharukul P, Cheungpasitporn W. Nasogastric tube and outcomes of Clostridium difficile infection: a systematic review and meta-analysis. J Evid Based Med. 2018;11:40–5.PubMed

94.

Kent KC, Rubin MS, Wroblewski L, Hanff PA, Silen W. The impact of Clostridium difficile on a surgical service: a prospective study of 374 patients. Ann Surg. 1998;227:296–301.PubMedPubMedCentral

95.

McDonald LC, Killgore GE, Thompson A, Owens RC Jr, Kazakova SV, Sambol SP, et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med. 2005;353:2433–41.PubMed

96.

Rodrigues MA, Brady RR, Rodrigues J, Graham C, Gibb AP. Clostridium difficile infection in general surgery patients; identification of high-risk populations. Int J Surg. 2010;8:368–72.PubMed

97.

Kim MJ, Kim BS, Kwon JW, Ahn SE, Lee SS, Park HC, Lee BH. Risk factors for the development of Clostridium difficile colitis in a surgical ward. J Korean Surg Soc. 2012;83:14–20.PubMedPubMedCentral

98.

Yasunaga H, Horiguchi H, Hashimoto H, Matsuda S, Fushimi K. The burden of Clostridium difficile-associated disease following digestive tract surgery in Japan. J Hosp Infect. 2012;82:175–80.PubMed

99.

Wren SM, Ahmed N, Jamal A, Safadi BY. Preoperative oral antibiotics in colorectal surgery increase the rate of Clostridium difficile colitis. Arch Surg. 2005;140:752–6.PubMed

100.

Yeom CH, Cho MM, Baek SK, Bae OS. Risk factors for the development of Clostridium difficile-associated colitis after colorectal Cancer surgery. J Korean Soc Coloproctol. 2010;26:329–33.PubMedPubMedCentral

101.

Damle RN, Cherng NB, Flahive JM, Davids JS, Maykel JA, Sturrock PR, et al. Clostridium difficile infection after colorectal surgery: a rare but costly complication. J Gastrointest Surg. 2014;18:1804–11.PubMed

102.

Skancke M, Vaziri K, Umapathi B, Amdur R, Radomski M, Obias V. Elective stoma reversal has a higher incidence of postoperative Clostridium difficile infection compared with elective colectomy: an analysis using the American College of Surgeons National Surgical Quality Improvement Program and targeted colectomy databases. Dis Colon Rectum. 2018;61:593–8.PubMed

103.

Lumpkins K, Bochicchio GV, Joshi M, Gens R, Bochicchio K, Conway A, et al. Clostridium difficile infection in critically injured trauma patients. Surg Infect. 2008;9:497–501.

104.

Bishara J, Farah R, Mograbi J, Khalaila W, Abu-Elheja O, Mahamid M, Nseir W. Obesity as a risk factor for Clostridium difficile infection. Clin Infect Dis. 2013;57:489–93.PubMed

105.

Leung J, Burke B, Ford D, Garvin G, Korn C, Sulis C, Bhadelia N. Possible association between obesity and Clostridium difficile infection. Emerg Infect Dis. 2013;19:1791–8.PubMedPubMedCentral

106.

Nathanson BH, Higgins TL. McGee WT the dangers of extreme body mass index values in patients with Clostridium difficile. Infection. 2017;45:787–93.PubMed

107.

Punni E, Pula JL, Asslo F, Baddoura W, DeBari VA. Is obesity a risk factor for Clostridium difficile infection? Obes Res Clin Pract. 2015;9:50–4.PubMed

108.

Mulki R, Baumann AJ, Alnabelsi T, Sandhu N, Alhamshari Y, Wheeler DS. Body mass index greater than 35 is associated with severe Clostridium difficile infection. Aliment Pharmacol Ther. 2017;45:75–81.PubMed

109.

Hussan H, Ugbarugba E, Bailey MT, Porter K, Needleman B, Noria S, et al. The impact of bariatric surgery on short term risk of Clostridium difficile admissions. Obes Surg. 2018;28:2006–13.PubMed

110.

Stallmach A, Anttila VJ, Hell M, Gwynn S, Merino-Amador P, Petrosillo N, et al. Inflammatory bowel disease and Clostridium difficile infection: contrasting views of international clinical professionals. Z Gastroenterol. 2018;56:731.

111.

Navaneethan U, Mukewar S, Venkatesh PG, Lopez R, Shen B, Nitzan O, et al. Clostridium difficile infection is associated with worse long term outcome in patients with ulcerative colitis. J Crohns Colitis. 2012;6:330–6.PubMed

112.

Jodorkovsky D, Young Y, Abreu MT. Clinical outcomes of patients with ulcerative colitis and co-existing Clostridium difficile infection. Dig Dis Sci. 2010;55:415–20.PubMed

113.

Issa M, Vijayapal A, Graham MB, Beaulieu DB, Otterson MF, Lundeen S, et al. Impact of Clostridium difficile on inflammatory bowel disease. Clin Gastroenterol Hepatol. 2007;5:345–51.PubMed

114.

Ananthakrishnan AN, McGinley EL, Binion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut. 2008;57:205–10.PubMed

115.

Chen Y, Furuya-Kanamori L, Doi SA, Ananthakrishnan AN, Kirk M. Clostridium difficile infection and risk of colectomy in patients with inflammatory bowel disease: a bias-adjusted meta-analysis. Inflamm Bowel Dis. 2017;23:200–7.PubMed

116.

Clayton EM, Rea MC, Shanahan F, Quigley EM, Kiely B, Hill C, Ross RP. The vexed relationship between Clostridium difficile and inflammatory bowel disease: an assessment of carriage in an outpatient setting among patients in remission. Am J Gastroenterol. 2009;104:1162–9.PubMed

117.

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;30:253–64.PubMed

118.

Kariv R, Navaneethan U, Venkatesh PG, Lopez R, Shen B. Impact of Clostridium difficile infection in patients with ulcerative colitis. J Crohns Colitis. 2011;5:34–40.PubMed

119.

Rezapour M, Galoosian A, Liu B, Bhuket T, Wong RJ. Clostridium difficile co-infection in inflammatory bowel disease is associated with significantly increased in-hospital mortality. Eur J Gastroenterol Hepatol. 2018;30:1041–6.PubMed

120.

Absah I, Faubion WA. Concomitant therapy with methotrexate and anti-TNF-α in pediatric patients with refractory crohn’s colitis: a case series. Inflamm Bowel Dis. 2012;18:1488–92.PubMed

121.

Rodemann JF, Dubberke ER, Reske KA, da Seo H, Stone CD. Incidence of Clostridium difficile infection in inflammatory bowel disease. Clin Gastroenterol Hepatol. 2007;5:339–44.PubMed

122.

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.PubMed

123.

Tsironi E, Irving PM, Feakins RM, Rampton DS. “Diversion” colitis caused by Clostridium difficile infection: report of a case. Dis Colon Rectum. 2006;49:1074–7.PubMed

124.

Ben-Horin S, Margalit M, Bossuyt P, Maul J, Shapira Y, Bojic D, et al. Prevalence and clinical impact of endoscopic pseudomembranes in patients with inflammatory bowel disease and Clostridium difficile infection. J Crohns Colitis. 2010;4:194–8.PubMed

125.

Yanai H, Nguyen GC, Yun L, Lebwohl O, Navaneethan U, Stone CD, et al. Practice of gastroenterologists in treating flaring inflammatory bowel disease patients with clostridium difficile: antibiotics alone or combined antibiotics/immunomodulators? Inflamm Bowel Dis. 2011;17:1540–6.PubMed

126.

Khanna S, Shin A, Kelly CP. Management of Clostridium difficile infection in inflammatory bowel disease: expert review from the clinical practice updates committee of the AGA Institute. Clin Gastroenterol Hepatol. 2017;15:166–74.PubMed

127.

Honda H, Dubberke ER. Clostridium difficile infection in solid organ transplant recipients. Curr Opin Infect Dis. 2014;27:336–41.PubMed

128.

Albright JB, Bonatti H, Mendez J, Kramer D, Stauffer J, Hinder R, et al. Early and late onset Clostridium difficile-associated colitis following liver transplantation. Transpl Int. 2007;20:856–66.PubMed

129.

Chopra T, Alangaden GJ, Chandrasekar P. Clostridium difficile infection in cancer patients and hematopoietic stem cell transplant recipients. Expert Rev Anti-Infect Ther. 2010;8:1113–9.PubMed

130.

Rodríguez Garzotto A, Mérida García A, Muñoz Unceta N, Galera Lopez MM, Orellana-Miguel MA, Díaz-García CV, et al. Risk factors associated with Clostridium difficile infection in adult oncology patients. Support Care Cancer. 2015;23:1569–77.PubMed

131.

Haines CF, Moore RD, Bartlett JG, Sears CL, Cosgrove SE, Carroll K, Gebo KA. Clostridium difficile in a HIV-infected cohort: incidence, risk factors, and clinical outcomes. AIDS. 2013;27:2799–807.PubMed

132.

Collini PJ, Kuijper E, Dockrell DH. Clostridium difficile infection in patients with HIV/AIDS. Curr HIV/AIDS Rep. 2013;10:273–82.PubMed

133.

Furuya-Kanamori L, Riley TV, Paterson DL, Foster NF, Huber CA, Hong S, et al. Comparison of Clostridium difficile ribotypes circulating in Australian hospitals and communities. J Clin Microbiol. 2016;55:216–25.PubMedPubMedCentral

134.

Lessa FC, Winston LG, McDonald LC. Emerging infections program C. difficile surveillance team. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:825–34.PubMed

135.

Namiki H, Kobayashi T. Long-term, low-dose of clarithromycin as a cause of community-acquired Clostridium difficile infection in a 5-year-old boy. Oxf Med Case Reports. 2018;2018:omx106.PubMedPubMedCentral

136.

Khanna S, Pardi DS, Aronson SL, Kammer PP, Baddour LM. Outcomes in community-acquired Clostridium difficile infection. Aliment Pharmacol Ther. 2012;35:613–8.PubMedPubMedCentral

137.

Gupta A, Khanna S. Community-acquired Clostridium difficile infection: an increasing public health threat. Infect Drug Resist. 2014;7:63–72.PubMedPubMedCentral

138.

Furuya-Kanamori L, Stone JC, Clark J, McKenzie SJ, Yakob L, Paterson DL, et al. Comorbidities, exposure to medications, and the risk of community-acquired Clostridium difficile infection: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2015;36:132–41.PubMed

139.

Zainul NH, Ma ZF, Besari A, Siti Asma H, Rahman RA, Collins DA, et al. Prevalence of Clostridium difficile infection and colonization in a tertiary hospital and elderly community of north-eastern peninsular Malaysia. Epidemiol Infect. 2017;145:3012–9.PubMed

140.

Garey KW, Sethi S, Yadav Y, DuPont HL. Meta-analysis to assess risk factors for recurrent Clostridium difficile infection. J Hosp Infect. 2008;70:298–304.PubMed

141.

Eyre DW, Walker AS, Wyllie D, Dingle KE, Griffiths D, Finney J, et al. Predictors of first recurrence of Clostridium difficile infection: implications for initial management. Clin Infect Dis. 2012;55:77–87.

142.

Zilberberg MD, Reske K, Olsen M, Yan Y, Dubberke ER. Risk factors for recurrent Clostridium difficile infection (CDI) hospitalization among hospitalized patients with an initial CDI episode: a retrospective cohort study. BMC Infect Dis. 2014;14:306.PubMedPubMedCentral

143.

Rotramel A, Poritz LS, Messaris E, Berg A, Stewart DB. PPI therapy and albumin are better predictors of recurrent Clostridium difficile colitis than choice of antibiotics. J Gastrointest Surg. 2012;16:2267–73.PubMed

144.

Petrosillo N. Tackling the recurrence of Clostridium difficile infection. Med Mal Infect. 2018;48:18–22.PubMed

145.

Deshpande A, Pasupuleti V, Thota P, Pant C, Rolston DD, Hernandez AV, et al. Risk factors for recurrent Clostridium difficile infection: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2015;36:452–60.PubMed

146.

Cornely OA, Miller MA, Louie TJ, Crook DW, Gorbach SL. Treatment of first recurrence of Clostridium difficile infection: fidaxomicin versus vancomycin. Clin Infect Dis. 2012;55:154–61.

147.

McFarland LV, Clarridge JE, Beneda HW, Raugi GJ. Fluoroquinolone use and risk factors for Clostridium difficile-associated disease within a veterans administration health care system. Clin Infect Dis. 2007;45:1141–51.PubMed

148.

Jaber MR, Olafsson S, Fung WL, Reeves ME. Clinical review of the management of fulminant clostridium difficile infection. Am J Gastroenterol. 2008;103:3195–203.PubMed

149.

Kazanowski M, Smolarek S, Kinnarney F, Grzebieniak Z. Clostridium difficile: epidemiology, diagnostic and therapeutic possibilities—a systematic review. Tech Coloproctol. 2014;18:223–32.PubMed

150.

Welfare MR, Lalayiannis LC, Martin KE, Corbett S, Marshall B, Sarma JB. Co-morbidities as predictors of mortality in Clostridium difficile infection and derivation of the ARC predictive score. J Hosp Infect. 2011;79:359–63.PubMed

151.

Hu MY, Katchar K, Kyne MS, Tummala S, Dreisbach V, et al. Prospective derivation and validation of a clinical prediction rule for recurrent Clostridium difficile infection. Gastroenterology. 2009;136:1206–14.PubMed

152.

Voelker R. Increased Clostridium difficile virulence demands new treatment approach. JAMA. 2010;26:2017–9.

153.

Bauer MP, Hensgens MPM, Miller MA, Gerding DN, Wilcox MH, Dale AP, et al. Renal failure and leukocytosis are predictors of a complicated course of Clostridium difficile infection if measured on day of diagnosis. Clin Infect Dis. 2012;55:149–53.

154.

Abou Chakra CN, Pepin J, Valiquette L. Prediction tools for unfavourable outcomes in Clostridium difficile infection: a systematic review. PLoS One. 2012;7:e30258.PubMedPubMedCentral

155.

Miller MA, Louie T, Mullane K, Weiss K, Lentnek A, Golan Y, et al. Derivation and validation of a simple clinical bedside score (ATLAS) for Clostridium difficile infection which predicts response to therapy. BMC Infect Dis. 2013;13:148.PubMedPubMedCentral

156.

Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31:431–55.PubMed

157.

Di Masi A, Leboffe L, Polticelli F, Tonon F, Zennaro C, Caterino M, et al. Human serum albumin is an essential component of the host defense mechanism against Clostridium difficile intoxication. J Infect Dis. 2018;22:1424–35.

158.

Flegel W, Muller F, Daubener W, Fisher HG, Hadding U, Northoff H. Cytokine response by human monocytes to Clostridium difficile toxin a and toxin B. Infect Immun. 1991;59:3659–66.PubMedPubMedCentral

159.

Castagliuolo I, Keates AC, Wang CC, Pasha A, Valenick L, Kelly CP, et al. Clostridium difficile toxin a stimulates macrophage- inflammatory protein-2 production in rat intestinal epithelial cells. J Immunol. 1998;160:6039–45.PubMed

160.

Dallal RM, Harbrecht BG, Boujoukas AJ, Sirio CA, Farkas LM, Lee KK, Simmons RL. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg. 2002;235:363–72.PubMedPubMedCentral

161.

Adams SD, Mercer DW. Fulminant Clostridium difficile colitis. Curr Opin Crit Care. 2007;13:450–5.PubMed

162.

Malnick SD, Zimhony O. Treatment of Clostridium difficile-associated diarrhea. Ann Pharmacother. 2002;36:1767–75.PubMed

163.

McFarland LV, Elmer GW, Surawicz CM. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol. 2002;97:1769–75.PubMed

164.

Kelly JP. Can we identify patients at high risk of recurrent Clostridium difficile infection? Clin Microbiol Infect. 2012;18(Suppl 6):21–7.PubMed

165.

Fekety R, McFarland LV, Surawicz CM, Greenberg RN, Elmer GW, Mulligan ME. Recurrent Clostridium difficile diarrhea: characteristics of and the risk factors for patients enrolled in a prospective, randomized, double-blinded trial. Clin Infect Dis. 1997;24:324–33.PubMed

166.

Johnson S. Recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J Inf Secur. 2009;58:403–10.

167.

Samie AA, Traub M, Bachmann K, Kopischke K, Theilmann L. Risk factors for recurrence of Clostridium difficile-associated diarrhea. Hepatogastroenterology. 2013;60:1351–4.PubMed

168.

LaBarbera FD, Nikiforov I, Parvathenani A, Pramil V, Gorrepati S. A prediction model for Clostridium difficile recurrence. J Community Hosp Intern Med Perspect. 2015;5:26033.PubMed

169.

Hookman P, Barkin JS. Clostridium difficile associated infection, diarrhea and colitis. World J Gastroenterol. 2009;15:1554–80.PubMedPubMedCentral

170.

Sheitoyan-Pesant C, Abou Chakra CN, Pépin J, Marcil-Héguy A, Nault V, Valiquette L. Clinical and healthcare burden of multiple recurrences of Clostridium difficile infection. Clin Infect Dis. 2016;62:574–80.PubMed

171.

Tabak YP, Zilberberg MD, Johannes RS, Sun X, McDonald LC. Attributable burden of hospital-onset Clostridium difficile infection: a propensity score matching study. Infect Control Hosp Epidemiol. 2013;34:588–96.PubMed

172.

Campbell R, Dean B, Nathanson B, Haidar T, Strauss M, Thomas S. Length of stay and hospital costs among high-risk patients with hospital-origin Clostridium difficile-associated diarrhea. J Med Econ. 2013;16:440–8.PubMed

173.

Magalini S, Pepe G, Panunzi S, Spada PL, De Gaetano A, Gui D. An economic evaluation of Clostridium difficile infection management in an Italian hospital environment. Eur Rev Med Pharmacol Sci. 2012;16:2136–41.PubMed

174.

Egorova NN, Siracuse JJ, McKinsey JF, Nowygrod R. Trend, risk factors and costs of Clostridium difficile infections in vascular surgery. Ann Vasc Surg. 2015;S0890-5096:00015–1.

175.

Skovrlj B, Guzman JZ, Silvestre J, Al Maaieh M, Qureshi SA. Clostridium difficile colitis in patients undergoing lumbar spine surgery. Spine. 2014;39:1167–73.

176.

Mittal C, Hassan S, Arshad S, Jeepalyam S, Bruni S, Miceli M, et al. Clostridium difficile infection in liver transplant recipients: a retrospective study of rates, risk factors and outcomes. Am J Transplant. 2014;14:1901–7.PubMed

177.

Lee DY, Chung EL, Guend H, Whelan RL, Wedderburn RV, Rose KM. Predictors of mortality after emergency colectomy for Clostridium difficile colitis: an analysis of ACS-NSQIP. Ann Surg. 2014;259:148–56.PubMed

178.

Piacenti FJ, Leuthner KD. Antimicrobial stewardship and Clostridium difficile-associated diarrhea. J Pharm Pract. 2013;26:506–13.PubMed

179.

Feazel LM, Malhotra A, Perencevich EN, Kaboli P, Diekema DJ, Schweizer ML. Effect of antibiotic stewardship programmes on Clostridium difficile incidence: a systematic review and meta-analysis. J Antimicrob Chemother. 2014;69:1748–54.PubMed

180.

Davey P, Marwick CA, Scott CL, Charani E, McNeil K, Brown E, et al. Interventions to improve antibiotic prescribing practices forhospital inpatients. Cochrane Database Syst Rev. 2017;2:CD003543.PubMed

181.

Dingle KE, Didelot X, Quan TP, Eyre DW, Stoesser N, Golubchik T, et al. Modernising medical microbiology informatics group. Effects of control interventions on Clostridium difficile infection in England: an observational study. Lancet Infect Dis. 2017;17:411–21.PubMedPubMedCentral

182.

Marufu O, Desai N, Aldred D, Brown T, Eltringham I. Analysis of interventions to reduce the incidence of Clostridium difficile infection at a London teaching hospital trust, 2003-2011. J Hosp Infect. 2014;89:38–45.PubMed

183.

Barker AK, Ngam C, Musuuza JS, Vaughn VM, Safdar N. Reducing Clostridium difficile in the inpatient setting: a systematic review of the adherence to and effectiveness of C. difficile prevention bundles. Infect Control Hosp Epidemiol. 2017;38:639–50.PubMedPubMedCentral

184.

Owens RC. Clostridium difficile-associated disease: an emerging threat to patient safety: insights from the Society of Infectious Diseases Pharmacists. Pharmacotherapy. 2006;26:299–311.PubMed

185.

Longtin Y, Paquet-Bolduc B, Gilca R, Garenc C, Fortin E, Longtin J, et al. 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. 2016;176:796–804.PubMed

186.

Garner JS. Guideline for isolation precautions in hospitals. The hospital infection control practices advisory committee. Infect Control Hosp Epidemiol. 1996;17:53–80.PubMed

187.

Vonberg RP, Kuijper EJ, Wilcox MH, Barbut F, Tull P, Gastmeier P, et al. Infection control measures to limit the spread of Clostridium difficile. Clin Microbiol Infect. 2008;14:2–20.PubMed

188.

Chang VT, Nelson K. The role of physical proximity in nosocomial diarrhea. Clin Infect Dis. 2000;31:717–22.PubMed

189.

Gerding DN, Meyer T, Lee C, Cohen SH, Murthy UK, Poirier A, et al. Administration of spores of nontoxigenic Clostridium difficile strain M3 for prevention of recurrent C. difficile infection: a randomized clinical trial. JAMA. 2015;313:1719–27.

190.

Brouwer MS, Roberts AP, Hussain H, Williams RJ, Allan E, Mullany P. Horizontal gene transfer converts non-toxigenic Clostridium difficile strains into toxin producers. Nat Commun. 2013;4:2601.PubMedPubMedCentral

191.

Curry SR, Muto CA, Schlackman JL, Pasculle AW, Shutt KA, Marsh JW, Harrison LH. Use of multilocus variable number of tandem repeats analysis genotyping to determine the role of asymptomatic carriers in Clostridium difficile transmission. Clin Infect Dis. 2013;57:1094–102.PubMedPubMedCentral

192.

Biswas JS, Patel A, Otter JA, van Kleef E, Goldenberg SD. Contamination of the hospital environment from potential Clostridium difficile excretors without active infection. Infect Control Hosp Epidemiol. 2015;36:975–7.PubMed

193.

Oughton MT, Loo VG, Dendukuri N, Fenn S, Libman MD. Hand hygiene with soap and ater is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile. Infect Control Hosp Epidemiol. 2009;30:939–44.PubMed

194.

Willt M, Odenhott I, Walder M. Activity of three disinfectants and acidified nitrate against Clostridium difficile spores. Infect Control Hosp Epidemiol. 2003;24:765–8.

195.

Deyneko A, Cordeiro F, Berlin L, Ben-David D, Perna S, Longtin Y. Impact of sink location on hand hygiene compliance after care of patients with Clostridium difficile infection: a cross-sectional study. BMC Infect Dis. 2016;16:203.PubMedPubMedCentral

196.

Louh IK, Greendyke WG, Hermann EA, Davidson KW, Falzon L, Vawdrey DK, et al. Clostridium difficile infection in acute care hospitals: systematic review and best practices for prevention. Infect Control Hosp Epidemiol. 2017;38:476–82.PubMedPubMedCentral

197.

Barbut F. How to eradicate Clostridium difficile from the environment. J Hosp Infect. 2015;89:287–95.PubMed

198.

McCord J, Prewitt M, Dyakova E, Mookerjee S, Otter JA. Reduction in Clostridium difficile infection associated with the introduction of hydrogen peroxide vapour automated room disinfection. J Hosp Infect. 2016;94:185–7.PubMed

199.

Marra AR, Schweizer ML, Edmond MB. No-touch disinfection methods to decrease multidrug-resistant organism infections: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2018;39:20–31.PubMed

200.

Tschudin-Sutter S, Kuijper EJ, Durovic A, Vehreschild MJGT, Barbut F, Eckert C, et al. Guidance document for prevention of Clostridium difficile infection in acute healthcare settings. Clin Microbiol Infect. 2018;24:1051.PubMed

201.

Huber CA, Foster NF, Riley TV, Paterson DL. Challenges for standardization of Clostridium difficile typing methods. J Clin Microbiol. 2013;51:2810–4.PubMedPubMedCentral

202.

McDonald EG, Lee TC. Clostridium difficile infection. N Engl J Med. 2015;373:286–8.PubMed

203.

Barbut F, Surgers L, Eckert C, Visseaux B, Cuingnet M, Mesquita C, et al. Does a rapid diagnosis of Clostridium difficile infection impact on quality of patient management? Clin Microbiol Infect. 2014;20:136–44.PubMed

204.

Kundrapu S, Sunkesula VC, Jury LA, Sethi AK, Donskey CJ. Utility of perirectal swab specimens for diagnosis of Clostridium difficile infection. Clin Infect Dis. 2012;55:1527–30.PubMed

205.

Carroll KC. Tests for the diagnosis of Clostridium difficile infection: the next generation. Anaerobe. 2011;17:170–4.PubMed

206.

Kyne L, Warny M, Qamar A, Kelly CP. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med. 2000;342:390–7.PubMed

207.

Planche T, Aghaizu A, Holliman R, Riley P, Poloniecki J, Breathnach A, Krishna S. Diagnosis of Clostridium difficile infection by toxin detection kits: a systematic review. Lancet Infect Dis. 2008;8:777–84.PubMed

208.

Brecher SM, Novak-Weekley SM, Nagy E. Laboratory diagnosis of Clostridium difficile infections: there is light at the end of the colon. Clin Infect Dis. 2013;57:1175–81.PubMed

209.

Chen S, Gu H, Sun C, Wang H, Wang J. Rapid detection of Clostridium difficile toxins and laboratory diagnosis of Clostridium difficile infections. Infection. 2017;45:255–62.PubMed

210.

Gerding DN, Johnson S, Rupnik M, Aktories K. Clostridium difficile binary toxin CDT: mechanism, epidemiology, and potential clinical importance. Gut Microbes. 2014;5:15–27.PubMed

211.

Gilligan PH. Optimizing the laboratory diagnosis of Clostridium difficile infection. Clin Lab Med. 2015;35:299–312.PubMed

212.

Smits WK, Lyras D, Lacy DB, Wilcox MH, Kuijper EJ. Clostridium difficile infection. Nat Rev Dis Primers. 2016;2:16020.PubMedPubMedCentral

213.

Lyerly DM, Barroso LA, Wilkins TD. Identification of the latex test-reactive protein of Clostridium difficile as glutamate dehydrogenase. J Clin Microbiol. 1991;29:2639–42.PubMedPubMedCentral

214.

Polage CR, et al. Outcomes in patients tested for Clostridium difficile toxins. Diagn Microbiol Infect Dis. 2012;74:369–73.PubMedPubMedCentral

215.

Schmidt ML, Gilligan PH. Clostridium difficile testing algorithms: what is practical and feasible? Anaerobe. 2009;15:270–3.PubMed

216.

Planche TD, Davies KA, Coen PG, Finney JM, Monahan IM, Morris KA, et al. Differences in outcome according to Clostridium difficile testing method: a prospective multicentre diagnostic validation study of C. difficile infection. Lancet Infect Dis. 2013;13:936–45.PubMedPubMedCentral

217.

Martínez-Meléndez A, Camacho-Ortiz A, Morfin-Otero R, Maldonado-Garza HJ, Villarreal-Treviño L, Garza-González E. Current knowledge on the laboratory diagnosis of Clostridium difficile infection. World J Gastroenterol. 2017;23:1552–67.PubMedPubMedCentral

218.

Napolitano LM, Edmiston CE Jr. Clostridium difficile disease: diagnosis, pathogenesis, and treatment update. Surgery. 2017;162:325–48.PubMed

219.

Ros PR, Buetow PC, Pantograg-Brown L, Forsmark CE, Sobin LH. Pseudomembranous colitis. Radiology. 1996;198:1–9.PubMed

220.

Merine DS, Fishman EK, Jones B. Pseudomembranous colitis: CT evaluation. J Comput Assist Tomogr. 1987;2:1017–20.

221.

Fishman EK, Kavuru M, Jones B, Kuhlman JE, Merine DS, Lillimoe KD, Siegelman SS. Pseudomembranous colitis: CT evaluation of 26 cases. Radiology. 1991;180:57–60.PubMed

222.

Boland GW, Lee MJ, Cats AM, Gaa JA, Saini S, Mueller PR. Antibiotic-induced diarrhea: specificity of abdominal CT for the diagnosis of Clostridium difficile disease. Radiology. 1994;191:103–6.PubMed

223.

Wang MF, Ding Z, Zhao J, Jiang CQ, Liu ZS, Qian Q. Current role of surgery for the treatment of fulminant Clostridium difficile colitis. Chin Med J. 2013;126:949–56.PubMed

224.

Kirkpatrick ID, Greenberg HM. Evaluating the CT diagnosis of Clostridium difficile colitis: should CT guide therapy? Am J Roentgenol. 2001;176:635–9.

225.

Abu-Zidan FM. Point-of-care ultrasound in critically ill patients: where do we stand? J Emerg Trauma Shock. 2012;5:70–1.PubMedPubMedCentral

226.

O'Malley ME, Wilson SR. US of gastrointestinal tract abnormalities with CT correlation. Radiographics. 2003;23:59–72.PubMed

227.

Downey DB, Wilson SR. Pseudomembranous colitis: sonographic features. Radiology. 1991;180:61–4.PubMed

228.

Ramachandran I, Sinha R, Rodgers P. Pseudomembranous colitis revisited: spectrum of imaging findings. Clin Radiol. 2006;61:535–44.PubMed

229.

Razzaq R, Sukumar SA. Ultrasound diagnosis of clinically undetected Clostridium difficile toxin colitis. Clin Radiol. 2006;61:446–52.PubMed

230.

Johal SS, Hammond J, Solomon K, James PD, Mahida YR. Clostridium difficile associated diarrhoea in hospitalised patients: onset in the community and hospital and role of flexible sigmoidoscopy. Gut. 2004;53:673–7.PubMedPubMedCentral

231.

Kyne L, Merry C, O’Connell B, Kelly A, Keane C, O’Neill D. Factors associated with prolonged symptoms and severe disease due to Clostridium difficile. Age Ageing. 1999;28:107–13.PubMed

232.

Bagdasarian N, Rao K, Malani PN. Diagnosis and treatment of Clostridium difficile in adults: a systematic review. JAMA. 2015;313:398–408.PubMed

233.

Bartlett JG. The case for vancomycin as the preferred drug for treatment of Clostridium difficile infection. Clin Infect Dis. 2008;46:1489–92.PubMed

234.

Teasley DG, Gerding DN, Olson MM, Peterson LR, Gebhard RL, Schwartz MJ, Lee JT Jr. Prospective randomised trial of metronidazole vs vancomycin for Clostridium difficile-associated diarrhea and colitis. Lancet. 1983;2:1043–6.PubMed

235.

Fekety R, Silva J, Buggy B, Deery HG. Treatment of antibiotic-associated colitis with vancomycin. J Antimicrob Chemother. 1984;14:97–102.PubMed

236.

Bartlett JG, Tedesco FJ, Shull S, Lowe B, Chang T. Symptomatic relapse after oral vancomycin therapy of antibiotic-associated pseudomembranous colitis. Gastroenterology. 1980;78:431–4.PubMed

237.

Louie TJ, Miller MA, Mullane KM, Weiss K, Lentnek A, Golan Y, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011;364:422–31.PubMed

238.

Cornely OA, Crook DW, Esposito R, Poirier A, Somero MS, Weiss K, et al. Fidaxomicin versus vancomycin for infection with Clostridium difficile in Europe, Canada, and the USA: a double-blind, non-inferiority, randomised controlled trial. Lancet Infect Dis. 2012;12:281–9.PubMed

239.

Gerber M, Ackermann G. OPT-80. A macrocyclic antimicrobial agent for the treatment of clostridium difficile infections: a review. Expert Opin Investig Drugs. 2008;17:547–53.PubMed

240.

Nelson RL. Antibiotic treatment for Clostridium difficile-associated diarrhea in adults. Cochrane Database Syst Rev. 2011;11:CD004610.

241.

Goolsby TA, Jakeman B, Gaynes RP. Clinical relevance of metronidazole and peripheral neuropathy: a systematic review of the literature. Int J Antimicrob Agents. 2018;51:319–25.PubMed

242.

McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, et al. 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. 2018;66:e1–e48.PubMedPubMedCentral

243.

Li R, Lu L, Lin Y, Wang M, Liu X. Efficacy and safety of metronidazole monotherapy versus vancomycin monotherapy or combination therapy in patients with Clostridium difficile infection: a systematic review and meta-analysis. PLoS One. 2015;10:e0137252.PubMedPubMedCentral

244.

Nelson RL, Suda KJ, Evans CT. Antibiotic treatment for Clostridium difficile-associated diarrhoea in adults. Cochrane Database Syst Rev. 2017;3:CD004610.PubMed

245.

Zar FA, Bakkanagari SR, Moorthi KM, Davis MB. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis. 2007;45:302–7.PubMed

246.

Al-Nassir WN, Sethi AK, Nerandzic MM, Bobulsky GS, Jump RL, Donskey CJ. Comparison of clinical and microbiological response to treatment of Clostridium difficile -associated disease with metronidazole and vancomycin. Clin Infect Dis. 2008;47:56–62.PubMed

247.

Johnson S, Louie TJ, Gerding DN, Cornely OA, Chasan-Taber S, Fitts D, et al. Vancomycin, metronidazole, or tolevamer for Clostridium difficile infection: results from two multinational, randomized, controlled trials. Clin Infect Dis. 2014;59:345–54.PubMed

248.

Kim PK, Zhao P, Teperman S. Evolving treatment strategies for severe Clostridium difficile colitis: defining the therapeutic window. In: Sartelli M, Bassetti M, Martin-Loeches I, editors. Abdominal Sepsis. A multidisciplinary approach. Hot topics in acute care surgery and trauma. Cham: Springer; 2018. p. 225–39.

249.

Kim PK, Huh HC, Cohen HW, Feinberg EJ, Ahmad S, Coyle C, et al. Intracolonic vancomycin for severe Clostridium difficile colitis. Surg Infect. 2013;14:532–9.

250.

Eiland EH 3rd, Sawyer AJ, Massie NL. Fidaxomicin use and clinical outcomes for Clostridium difficile-associated diarrhea. Infect Dis Clin Pract (Baltim Md). 2015;23:32–5.

251.

Vargo CA, Bauer KA, Mangino JE, Johnston JE, Goff DA. An antimicrobial stewardship program's real-world experience with fidaxomicin for treatment of Clostridium difficile infection: a case series. Pharmacotherapy. 2014;34:901–9.PubMed

252.

Guery B, Menichetti F, Anttila VJ, Adomakoh N, Aguado JM, Bisnauthsing K, et al. Extended-pulsed fidaxomicin versus vancomycin for Clostridium difficile infection in patients 60 years and older (EXTEND): a randomised, controlled, open-label, phase 3b/4 trial. Lancet Infect Dis. 2018;18:296–307.PubMed

253.

Herpers BL, Vlaminckx B, Burkhardt O, Blom H, Biemond-Moeniralam HS, Hornef M, et al. Intravenous tigecycline as adjunctive or alternative therapy for severe refractory Clostridium difficile infection. Clin Infect Dis. 2009;48:1732–5.PubMed

254.

El-Herte RI, Baban TA, Kanj SS. Recurrent refractory Clostridium difficile colitis treated successfully with rifaximin and tigecycline: a case report and review of the literature. Scand J Infect Dis. 2012;44:228–30.PubMed

255.

Musher DM, Logan N, Mehendiratta V, Melgarejo NA, Garud S, Hamill RJ. Clostridium difficile colitis that fails conventional metronidazole therapy: response to nitazoxanide. J Antimicrob Chemother. 2007;59:705–10.PubMed

256.

Girotra M, Kumar V, Khan JM, Damisse P, Abraham RR, Aggarwal V, Dutta SK. Clinical predictors of fulminant colitis in patients with Clostridium difficile infection. Saudi J Gastroenterol. 2012;18:133–9.PubMedPubMedCentral

257.

Kaiser AM, Hogen R, Bordeianou L, Alavi K, Wise PE, Sudan R, CME Committee of the SSAT. Clostridium difficile infection from a surgical perspective. J Gastrointest Surg. 2015;19:1363–77.PubMed

258.

Khanna S, Pardi DS. Clostridium difficile infection: new insights into management. Mayo Clin Proc. 2012;87:1106–17.PubMedPubMedCentral

259.

Clanton J, Fawley R, Haller N, Daley T, Porter J, Paranjape C, Bonilla H. Patience is a virtue: an argument for delayed surgical intervention in fulminant Clostridium difficile colitis. Am Surg. 2014;80:614–9.PubMed

260.

Carchman EH, Peitzman AB, Simmons RL, Zuckerbraun BS. The role of acute care surgery in the treatment of severe, complicated Clostridium difficile-associated disease. J Trauma Acute Care Surg. 2012;73:789–800.PubMed

261.

Stewart DB, Hollenbeak CS, Wilson MZ. Is colectomy for fulminant Clostridium difficile colitis life saving? A systematic review. Color Dis. 2013;15:798–804.

262.

Ali SO, Welch JP, Dring RJ. Early surgical intervention for fulminant pseudomembranous colitis. Am Surg. 2008;74:20–6.PubMed

263.

Chan S, Kelly M, Helme S, Gossage J, Modarai B, Forshaw M. Outcomes following colectomy for Clostridium difficile colitis. Int J Surg. 2009;7:78–81.PubMed

264.

Hall JF, Berger D. Outcome of colectomy for Clostridium difficile colitis: a plea for early surgical management. Am J Surg. 2008;196:384–8.PubMed

265.

Osman KA, Ahmed MH, Hamad MA, Mathur D. Emergency colectomy for fulminant Clostridium difficile colitis: striking the right balance. Scand J Gastroenterol. 2011;46:1222–7.PubMed

266.

Seder CW, Villalba MR Jr, Robbins J, Ivascu FA, Carpenter CF, Dietrich M, Villalba MR Sr. Early colectomy may be associated with improved survival in fulminant Clostridium difficile colitis: an 8-year experience. Am J Surg. 2009;197:302–7.PubMed

267.

Van der Wilden GM, Chang Y, Cropano C, Subramanian M, Schipper IB, Yeh DD, et al. Fulminant Clostridium difficile colitis: prospective development of a risk scoring system. J Trauma Acute Care Surg. 2014;76:424–30.PubMed

268.

Ferrada P, Velopulos CG, Sultan S, Haut ER, Johnson E, Praba-Egge A, et al. Timing and type of surgical treatment of Clostridium difficile-associated disease: a practice management guideline from the Eastern Association for the Surgery of trauma. J Trauma Acute Care Surg. 2014;76:1484–93.PubMed

269.

Sailhamer EA, Carson K, Chang Y, Zacharias N, Spaniolas K, Tabbara M, et al. Fulminant Clostridium difficile colitis: patterns of care and predictors of mortality. Arch Surg. 2009;144:433–9.PubMed

270.

Bhangu A, Nepogodiev D, Gupta A, Torrance A, Singh P; West midlands research collaborative. Systematic review and meta-analysis of outcomes following emergency surgery for Clostridium difficile colitis. Br J Surg 2012;99:1501–1513.

271.

Lamontagne F, Labbé AC, Haeck O, Lesur O, Lalancette M, Patino C, et al. Impact of emergency colectomy on survival of patients with fulminant Clostridium difficile colitis during an epidemic caused by a hypervirulent strain. Ann Surg. 2007;245:267–72.PubMedPubMedCentral

272.

Neal MD, Alverdy JC, Hall DE, Simmons RL, Zuckerbraun BS. Diverting loop ileostomy and colonic lavage: an alternative to total abdominal colectomy for the treatment of severe, complicated Clostridium difficile associated disease. Ann Surg. 2011;254:423–37.PubMed

273.

Olivas AD, Umanskiy K, Zuckerbraun B, Alverdy JC. Avoiding colectomy during surgical management of fulminant Clostridium difficile colitis. Surg Infect. 2010;11:299–305.

274.

Ferrada P, Callcut R, Zielinski MD, Bruns B, Yeh DD, Zakrison TL, et al. Loop ileostomy versus total colectomy as surgical treatment for Clostridium difficile-associated disease: an eastern association for the surgery of trauma multicenter trial. J Trauma Acute Care Surg. 2017;83:36–40.PubMedPubMedCentral

275.

Xu JY, Chen QH, Xie JF, Pan C, Liu SQ, Huang LW, et al. Comparison of the effects of albumin and crystalloid on mortality in adult patients with severe sepsis and septic shock: a meta-analysis of randomized clinical trials. Crit Care. 2014;18:702.PubMedPubMedCentral

276.

O'Horo JC, Jindai K, Kunzer B, Safdar N. Treatment of recurrent Clostridium difficile infection: a systematic review. Infection. 2014;42:43–59.PubMed

277.

McFarland LV, Evans CT, Goldstein EJC. Strain-specificity and disease-specificity of probiotic efficacy: a systematic review and meta-analysis. Front Med (Lausanne). 2018;5:124.

278.

McFarland LV. Primary prevention of Clostridium difficile infections—how difficult can it be? Expert Rev Gastroenterol Hepatol. 2017;11:507–21.PubMed

279.

Avadhani A, Miley H. Probiotics for prevention of antibiotic-associated diarrhea and Clostridium difficile-associated disease in hospitalized adults—a meta-analysis. J Am Acad Nurse Pract. 2011;23:269–74.PubMed

280.

Goldenberg JZ, Ma SS, Saxton JD, Martzen MR, Vandvik PO, Thorlund K, et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database Syst Rev. 2013;5:CD006095.

281.

Johnston BC, Ma SS, Goldenberg JZ, Thorlund K, Vandvik PO, Loeb M, et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea: a systematic review and meta-analysis. Ann Intern Med. 2012;157:878–88.PubMed

282.

McFarland LV. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am J Gastroenterol. 2006;101:812–22.PubMed

283.

Johnson S, Maziade PJ, McFarland LV, Trick W, Donskey C, Currie B, et al. Is primary prevention of Clostridium difficile infection possible with specific probiotics? Int J Infect Dis. 2012;16:e786–92.PubMed

284.

Goldenberg JZ, Yap C, Lytvyn L, Lo CK, Beardsley J, Mertz D, Johnston BC. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database Syst Rev. 2017;12:CD006095.PubMed

285.

McFarland LV, Ship N, Auclair J, Milletteu M. Primary prevention of Clostridium difficile infections with a specific probiotic combining Lactobacillus acidophilus, L. casei and L. rhamnosus strains: assessing the evidence. J Hosp Infect. 2018;99:443–52.PubMed

286.

McFarland LV, Surawicz CM, Greenberg RN, Fekety R, Elmer GW, Moyer KA, et al. A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. JAMA. 1994;271:1913–8.PubMed

287.

Surawicz CM, McFarland LV, Greenberg RN, Rubin M, Fekety R, Mulligan ME, et al. The search for a better treatment for recurrent Clostridium difficile disease: use of high-dose vancomycin combined with Saccharomyces boulardii. Clin Infect Dis. 2000;31:1012–7.PubMed

288.

Bakken JS, Borody T, Brandt LJ, Brill JV, Demarco DC, Franzos MA, et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9:1044–9.PubMedPubMedCentral

289.

Gough E, Shaikh H, Manges AR. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis. 2011;53:994–1002.PubMed

290.

Cammarota G, Ianiro G, Gasbarrini A. Fecal microbiota transplantation for the treatment of Clostridium difficile infection: a systematic review. J Clin Gastroenterol. 2014;48:693–702.PubMed

291.

Quraishi MN, Widlak M, Bhala N, Moore D, Price M, Sharma N, Iqbal TH. Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Ther. 2017;46:479–93.

292.

Orenstein R, Dubberke E, Hardi R, Ray A, Mullane K, Pardi DS, et al. Safety and durability of RBX2660 (microbiota suspension) for recurrent Clostridium difficile infection: results of the PUNCH CD study. Clin Infect Dis. 2016;62:596–602.PubMed

293.

Postigo R, Kim JH. Colonoscopic versus nasogastric fecal transplantation for the treatment of Clostridium difficile infection: a review and pooled analysis. Infection. 2012;40:643–8.PubMed

294.

Furuya-Kanamori L, Doi SA, Paterson DL, Helms SK, Yakob L, McKenzie SJ, et al. Upper versus lower gastrointestinal delivery for transplantation of fecal microbiota in recurrent or refractory Clostridium difficile infection: a collaborative analysis of individual patient data from 14 studies. J Clin Gastroenterol. 2017;51:145–50.PubMed

295.

Hirsch BE, Saraiya N, Poeth K, Schwartz RM, Epstein ME, Honig G. Effectiveness of fecal-derived microbiota transfer using orally administered capsules for recurrent Clostridium difficile infection. BMC Infect Dis. 2015;15:191.PubMedPubMedCentral

296.

Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA. 2014;312:1772–8.PubMed

297.

Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500–8.PubMed

298.

Van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–15.PubMed

299.

Di Bella S, Gouliouris T, Petrosillo N. Fecal microbiota transplantation (FMT) for Clostridium difficile infection: focus on immunocompromised patients. J Infect Chemother. 2015;21:230–7.PubMed

300.

Kelly CR, Ihunnah C, Fischer M, Khoruts A, Surawicz C, Afzali A, et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065–71.PubMedPubMedCentral

301.

Bartlett JG. Bezlotoxumab—a new agent for Clostridium difficile infection. N Engl J Med. 2017;376:381–2.PubMed

302.

Wilcox MH, Gerding DN, Poxton IR, Kelly C, Nathan R, Birch T, et al. Bezlotoxumab for prevention of recurrent Clostridium difficile infection. N Engl J Med. 2017;376:305–17.PubMed

303.

Lübbert C, Nitschmann S. Bezlotoxumab for the secondary prevention of Clostridium difficile infection: MODIFY I and MODIFY II studies. Internist (Berl). 2017;58:639–42.

304.

Gerding DN, Kelly CP, Rahav G, Lee C, Dubberke ER, Kumar PN, et al. Bezlotoxumab for prevention of recurrent Clostridium difficile infection in patients at increased risk for recurrence. Clin Infect Dis. 2018;67:649–56.PubMedPubMedCentral

305.

Abourgergi MS, Kwon JH. Intravenous immunoglobulin for the treatment of Clostridium difficile infection: a review. Dig Dis Sci. 2011;56:19–26.

306.

Shahani L, Koirala J. Use of intravenous immunoglobulin in severe Clostridium difficile-associated diarrhea. Hosp Pract. 2015;43:154–7.

307.

Juang P, Skledar SJ, Zgheib NK, Paterson DL, Vergis EN, Shannon WD, et al. Clinical outcomes of intravenous immune globulin in severe clostridium difficile-associated diarrhea. Am J Infect Control. 2007;35:131–7.PubMed

308.

Sullivan PB. Nutritional management of acute diarrhea. Nutrition. 1998;14:758–62.PubMed

309.

Choi EY, Park DA, Park J. Calorie intake of enteral nutrition and clinical outcomes in acutely critically ill patients: a meta-analysis of randomized controlled trials. JPEN J Parenter Enteral Nutr. 2015;39:291–300.PubMed

310.

Gerding DN. Acquisition of Clostridium difficile and Clostridium difficile-associated diarrhea in hospitalized patients receiving tube feeding. Ann Intern Med. 1998;129:1012–9.PubMed

311.

Bliss DZ, Johnson S, Savik K, et al. Acquisition of C. difficile and C. diff-associated diarrhea in hospitalized patients receiving tube feeding. Ann Intern Med. 1998;129:1012–9.PubMed

312.

O'Keefe SJ. A guide to enteral access procedures and enteral nutrition. Nat Rev Gastroenterol Hepatol. 2009;6:207–15.PubMed

313.

O'Keefe SJ. Tube feeding, the microbiota, and Clostridium difficile infection. World J Gastroenterol. 2010;16:139–42.PubMedPubMedCentral

314.

Puri BK, Hakkarainen-Smith J, Monro JA. The potential use of cholestyramine to reduce the risk of developing Clostridium difficile-associated diarrhoea in patients receiving long-term intravenous ceftriaxone. Med Hypotheses. 2015;84:78–80.PubMed

315.

Koo HL, Koo DC, Musher DM, DuPont HL. Antimotility agents for the treatment of Clostridium difficile diarrhea and colitis. Clin Infect Dis. 2009;48:598–605.PubMed

Title: 2019 update of the WSES guidelines for management of Clostridioides (Clostridium) difficile infection in surgical patients
Authors: Massimo Sartelli
Stefano Di Bella
Lynne V. McFarland
Sahil Khanna
Luis Furuya-Kanamori
Nadir Abuzeid
Fikri M. Abu-Zidan
Luca Ansaloni
Goran Augustin
Miklosh Bala
Offir Ben-Ishay
Walter L. Biffl
Stephen M. Brecher
Adrián Camacho-Ortiz
Miguel A. Caínzos
Shirley Chan
Jill R. Cherry-Bukowiec
Jesse Clanton
Federico Coccolini
Maria E. Cocuz
Raul Coimbra
Francesco Cortese
Yunfeng Cui
Jacek Czepiel
Zaza Demetrashvili
Isidoro Di Carlo
Salomone Di Saverio
Irina M. Dumitru
Christian Eckmann
Edward H. Eiland
Joseph D. Forrester
Gustavo P. Fraga
Jean L. Frossard
Donald E. Fry
Rita Galeiras
Wagih Ghnnam
Carlos A. Gomes
Ewen A. Griffiths
Xavier Guirao
Mohamed H. Ahmed
Torsten Herzog
Jae Il Kim
Tariq Iqbal
Arda Isik
Kamal M. F. Itani
Francesco M. Labricciosa
Yeong Y. Lee
Paul Juang
Aleksandar Karamarkovic
Peter K. Kim
Yoram Kluger
Ari Leppaniemi
Varut Lohsiriwat
Gustavo M. Machain
Sanjay Marwah
John E. Mazuski
Gokhan Metan
Ernest E. Moore
Frederick A. Moore
Carlos A. Ordoñez
Leonardo Pagani
Nicola Petrosillo
Francisco Portela
Kemal Rasa
Miran Rems
Boris E. Sakakushev
Helmut Segovia-Lohse
Gabriele Sganga
Vishal G. Shelat
Patrizia Spigaglia
Pierre Tattevin
Cristian Tranà
Libor Urbánek
Jan Ulrych
Pierluigi Viale
Gian L. Baiocchi
Fausto Catena
Publication date: 01-12-2019
Publisher: BioMed Central
Keywords: Vancomycin
Respiratory Microbiota
Clostridioides Difficile
Published in: World Journal of Emergency Surgery / Issue 1/2019
Electronic ISSN: 1749-7922
DOI: https://doi.org/10.1186/s13017-019-0228-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

2019 update of the WSES guidelines for management of Clostridioides (Clostridium) difficile infection in surgical patients

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

2019 WSES guidelines for the management of severe acute pancreatitis

Does the conventional landmark help to place the tip of REBOA catheter in the optimal position? A non-controlled comparison study

Open conversion for laparoscopically difficult cholecystectomy is still a valid solution with unsolved aspects

Kunafa knife and play dough is an efficient and cheap simulator to teach diagnostic Point-of-Care Ultrasound (POCUS)

The impact of polytrauma on sRAGE levels: evidence and statistical analysis of temporal variations

Optimal management of malignant left-sided large bowel obstruction: do international guidelines agree?