Clostridium difficile infection in solid organ transplant recipients

Current Opinion in Organ Transplantation

Volumn 13, Issue 6, 2008, Pages 592-600

  Riddle, David J ^a   Dubberke, Erik R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibiotic associated diarrhea; Clostridium difficile; Nosocomial infection; Pseudomembranous colitis; Solid organ transplant

Indexed keywords

ANTIINFECTIVE AGENT; IMMUNOGLOBULIN; METRONIDAZOLE; PROTON PUMP INHIBITOR; TACROLIMUS; VANCOMYCIN;

ANTIMICROBIAL THERAPY; CLINICAL FEATURE; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; DIAGNOSTIC VALUE; DISEASE SEVERITY; DRUG DOSE REDUCTION; DRUG DOSE REGIMEN; DRUG EFFICACY; EARLY DIAGNOSIS; ENVIRONMENTAL FACTOR; EPIDEMIC; HUMAN; IMMUNOPATHOLOGY; INFECTION CONTROL; INFECTION PREVENTION; INFECTION RISK; NONHUMAN; ORGAN TRANSPLANTATION; RECURRENT INFECTION; REVIEW; ABDOMINAL SURGERY; ANIMAL; CLOSTRIDIUM DIFFICILE; HOSPITALIZATION; INCIDENCE; MICROBIOLOGY; PATHOGENICITY; PSEUDOMEMBRANOUS COLITIS; RISK FACTOR; TREATMENT OUTCOME; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; CLOSTRIDIUM DIFFICILE; DIGESTIVE SYSTEM SURGICAL PROCEDURES; ENTEROCOLITIS, PSEUDOMEMBRANOUS; HUMANS; INCIDENCE; INFECTION CONTROL; METRONIDAZOLE; ORGAN TRANSPLANTATION; RISK FACTORS; SEVERITY OF ILLNESS INDEX; TREATMENT OUTCOME; VANCOMYCIN; VIRULENCE;

EID: 60849125772     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0b013e3283186b51     Document Type: Review

References (150)

1. Altiparmak MR, Trablus S, Pamuk ON, et al. Diarrhoea following renal transplantation. Clin Transplant 2002; 16:212-216.
2. Bunnapradist S, Neri L, Wong W, et al. Incidence and risk factors for diarrhea following kidney transplantation and association with graft loss and mortality. Am J Kidney Dis 2008; 51:478-486.
3. Wong NA, Bathgate AJ, Bellamy CO. Colorectal disease in liver allograft recipients: a clinicopathological study with follow-up. Eur J Gastroenterol Hepatol 2002; 14:231-236.
4. Fruhwirth M, Fischer H, Simma B, Ellemunter H. Elevated tacrolimus trough levels in association with mycophenolate mofetil-induced diarrhea: a case report. Pediatr Transplant 2001; 5:132-134.
5. Hochleitner BW, Bosmuller C, Nehoda H, et al. Increased tacrolimus levels during diarrhea. Transpl Int 2001; 14:230-233.
6. Stelzmueller I, Goegele H, Biebl M, et al. Clostridium difficile colitis in solid organ transplantation: a single-center experience. Dig Dis Sci 2007; 52:3231-3236.
7. Cao S, Cox K, Esquivel CO, et al. Posttransplant lymphoproliferative disorders and gastrointestinal manifestations of Epstein-Barr virus infection in children following liver transplantation. Transplantation 1998; 66:851-856.
8. Ginsburg PM, Thuluvath PJ. Diarrhea in liver transplant recipients: etiology and management. Liver Transpl 2005; 11:881-890.
9. Heo JS, Park JW, Lee KW, et al. Posttransplantation lymphoproliferative disorder in pediatric liver transplantation. Transplant Proc 2004; 36:2307-2308.
10. Miras M, Carballo F, Egea J, et al. Clinical evolution in the first 3 months of patients after liver transplantation in maintenance phase converted from mycophenolate mofetil to mycophenolate sodium due to gastrointestinal complications. Transplant Proc 2007; 39:2314-2317.
11. Hall IC, OToole E. Intestinal flora in ew-born infants with a description of a new pathogenic anaerobe, Bacillus difficilis. Am J Dis Child 1935; 49:390-402.
12. Bartlett JG, Chang TW, Gurwith M, et al. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 1978; 298:531-534.
13. Larson HE, Price AB, Honour P, Borriello SP. Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1978; 1:1063-1066.
14. Barbut F, Corthier G, Charpak Y, et al. Prevalence and pathogenicity of Clostridium difficile in hospitalized patients. A French multicenter study. Arch Intern Med 1996; 156:1449-1454.
15. Johnson S, Gerding DN. Clostridium difficile-associated diarrhea. Clin Infect Dis 1998; 26 (5):1027-1034; quiz 1035-1036.
16. Riley TV. Clostridium difficile: a pathogen of the nineties. Eur J Clin Microbiol Infect Dis 1998; 17:137-141.
17. Aslam S, Musher DM. An update on diagnosis, treatment, and prevention of Clostridium difficile-associated disease. Gastroenterol Clin North Am 2006; 35:315-335.
18. TriadafilopoulosG, PothoulakisC, O'Brien MJ, LaMont JT. Differential effects of Clostridium difficile toxins A and B on rabbit ileum. Gastroenterology 1987; 93:273-279.
19. Pothoulakis C, Sullivan R, Melnick DA, et al. Clostridium difficile toxin A stimulates intracellular calcium release and chemotactic response in human granulocytes. J Clin Invest 1988; 81:1741-1745.
20. Riegler M, Sedivy R, Pothoulakis C, et al. Clostridium difficile toxin B is more potent than toxin A in damaging human colonic epithelium in vitro. J Clin Invest 1995; 95:2004-2011.
21. Meyer GK, Neetz A, Brandes G, et al. Clostridium difficile toxins A and B directly stimulate human mast cells. Infect Immun 2007; 75:3868-3876.
22. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996-2003. Emerg Infect Dis 2006; 12:409-415.
23. Loo VG, Poirier L, Miller MA, et al. A predominantly clonal multiinstitutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 2005; 353:2442-2449.
24. McDonald LC, Killgore GE, Thompson A, et al. An epidemic, toxin genevariant strain of Clostridium difficile. N Engl J Med 2005; 353:2433-2441.
25. Warny M, Pepin J, Fang A, et al. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 2005; 366:1079-1084.
26. Muto CA, Pokrywka M, Shutt 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; 26:273-280.
27. Pepin J, Valiquette L, Cossette B. Mortality attributable to nosocomial Clostridium difficile-associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 2005; 173:1037-1042.
28. Pepin J, Saheb N, Coulombe MA, 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; 41:1254-1260.
29. Clabots CR, Johnson S, Olson MM, et al. Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis 1992; 166:561-567.
30. McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989; 320:204-210.
31. Barbut F, Petit JC. Epidemiology of Clostridium difficile- associated infections. Clin Microbiol Infect 2001; 7:405-410.
32. Riggs MM, Sethi AK, ZabarskyTF, et al. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin Infect Dis 2007; 45:992-998.
33. Simor AE, Bradley SF, Strausbaugh LJ, et al. Clostridium difficile in longterm-care facilities for the elderly. Infect Control Hosp Epidemiol 2002; 23:696-703.
34. Hyland M, Ofner-Agostini M, Miller M, et al. N-CDAD in Canada: results of the Canadian Nosocomial Infection Surveillance Program 1997 N-CDAD Prevalence Surveillance Project. Can J Infect Dis 2001; 12:81-88.
35. Zerey M, Paton BL, Lincourt AE, et al. The burden of Clostridium difficile in surgical patients in the United States. Surg Infect (Larchmt) 2007; 8:557-566.
36. Samore MH, DeGirolami PC,TluckoA, et al. Clostridium difficile colonization and diarrhea at a tertiary care hospital. Clin Infect Dis 1994; 18:181-187.
37. Albright JB, Bonatti H, Mendez J, et al. Early and late onset Clostridium difficile-associated colitis following liver transplantation. Transpl Int 2007; 20:856-866.
38. Niemczyk M, Leszczyniski P, Wyzgal J, et al. Infections caused by Clostridium difficile in kidney or liver graft recipients. Ann Transplant 2005; 10:70-74.
39. Keven K, Basu A, Re L, et al. Clostridium difficile colitis in patients after kidney and pancreas-kidney transplantation. Transpl Infect Dis 2004; 6:10-14.
40. West M, Pirenne J, Chavers B, et al. Clostridium difficile colitis after kidney and kidney-pancreas transplantation. Clin Transplant 1999; 13:318-323.
41. Ziring D, Tran R, Edelstein S, et al. Infectious enteritis after intestinal transplantation: incidence, timing, and outcome. Transplant Proc 2004; 36:379-380.
42. Munoz P, Giannella M, Alcala L, et al. Clostridium difficile-associated diarrhea in heart transplant recipients: is hypogammaglobulinemia the answer? J Heart Lung Transplant 2007; 26:907-914.
43. Dallal RM, Harbrecht BG, Boujoukas AJ, et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg 2002; 235:363-372.
44. Gunderson CC, Gupta MR, Lopez F, et al. Clostridium difficile colitis in lung transplantation. Transpl Infect Dis 2008; 10:245-251.
45. Crabtree T, Aitchison D, Meyers BF, et al. Clostridium difficile in cardiac surgery: risk factors and impact on postoperative outcome. Ann Thorac Surg 2007; 83:1396-1402.
46. Kent KC, Rubin MS, Wroblewski L, et al. The impact of Clostridium difficile on a surgical service: a prospective study of 374 patients. Ann Surg 1998; 227:296-301.
47. McCarter MD, Abularrage C, Velasco FT, et al. Diarrhea and Clostridium difficile-associated diarrhea on a surgical service. Arch Surg 1996; 131:1333-1337.
48. Clostridium difficile. Am J Transplant 2004; 4:28-30.
49. Arslan H, Inci EK, Azap OK, et al. Etiologic agents of diarrhea in solid organ recipients. Transpl Infect Dis 2007; 9:270-275.
50. Adams SD, Mercer DW. Fulminant Clostridium difficile colitis. Curr Opin Crit Care 2007; 13:450-455.
51. Gellad ZF, Alexander BD, Liu JK, et al. Severity of Clostridium difficileassociated diarrhea in solid organ transplant patients. Transpl Infect Dis 2007; 9:276-280.
52. Kelly CP, Pothoulakis C, LaMont JT. Clostridium difficile colitis. N Engl J Med 1994; 330:257-262.
53. Kyne L, Merry C, O'Connell B, et al. Factors associated with prolonged symptoms and severe disease due to Clostridium difficile. Age Ageing 1999; 28:107-113.
54. Beaulieu M, Williamson D, Pichette G, Lachaine J. Risk of Clostridium difficile-associated disease among patients receiving proton-pump inhibitors in a Quebec medical intensive care unit. Infect Control Hosp Epidemiol 2007; 28:1305-1307.
55. Hurley BW, Nguyen CC. The spectrum of pseudomembranous enterocolitis and antibiotic-associated diarrhea. Arch Intern Med 2002; 162:2177-2184.
56. Mogg GA, Burdon DW, Keighley M. Oral metronidazole in Clostridium difficile colitis. Br Med J 1979; 2:335.
57. Tedesco FJ. Pseudomembranous colitis: pathogenesis and therapy. Med Clin North Am 1982; 66:655-664.
58. Lykavieris P, Fabre M, Pariente D, et al. Clostridium difficile colitis associated with inflammatory pseudotumor in a liver transplant recipient. Pediatr Transplant 2003; 7:76-79.
59. Theunissen C, KnoopC, Nonhoff C, et al. Clostridium difficile colitis in cystic fibrosis patients with and without lung transplantation. Transpl Infect Dis 2008; 10:240-244.
60. Bignardi GE. Risk factors for Clostridium difficile infection. J Hosp Infect 1998; 40:1-15.
61. Gaynes R, Rimland D, Killum E, et al. Outbreak of Clostridium difficile infection in a long-term care facility: association with gatifloxacin use. Clin Infect Dis 2004; 38:640-645.
62. Gurwith MJ, Rabin HR, Love K. Diarrhea associated with clindamycin and ampicillin therapy: preliminary results of a cooperative study. J Infect Dis 1977; 135 (Suppl):S104-S110.
63. Mohr J. Outbreak of Clostridium difficile infection and gatifloxacin use in a long-term care facility. Clin Infect Dis 2004; 39:875-876; author reply 876-877.
64. Owens RC Jr, Ambrose PG. Antimicrobial safety: focus on fluoroquinolones. Clin Infect Dis 2005; 41 (Suppl 2):S144-S157.
65. Poutanen SM, Simor AE. Clostridium difficile-associated diarrhea in adults. CMAJ 2004; 171:51-58.
66. Shim JK, Johnson S, Samore MH, et al. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 1998; 351:633-636.
67. 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; 342:390-397.
68. Goldfarb NS, Avery RK, Goormastic M, et al. Hypogammaglobulinemia in lung transplant recipients. Transplantation 2001; 71:242-246.
69. Yamani MH, Avery R, Mawhorter S, et al. Hypogammaglobulinemia after heart transplantation: impact of preemptive use of immunoglobulin replacement (CytoGam) on infection and rejection outcomes. Transpl Infect Dis 2001; 3 (Suppl 2):40-43.
70. Doron S, Ruthazer R, Werner BG, et al. Hypogammaglobulinemia in liver transplant recipients: incidence, timing, risk factors, and outcomes. Transplantation 2006; 81:697-703.
71. Chen KJ, Chen CH, Cheng CH, et al. Risk factors for peptic ulcer disease in renal transplant patients: 11 years of experience from a single center. Clin Nephrol 2004; 62:14-20.
72. Cunningham R, Dale B, Undy B, Gaunt N. Proton pump inhibitors as a risk factor for Clostridium difficile diarrhoea. J Hosp Infect 2003; 54:243-245.
73. Dial S, Alrasadi K, Manoukian C, et al. Risk of Clostridium difficile diarrhea among hospital inpatients prescribed proton pump inhibitors: cohort and case-control studies. CMAJ 2004; 171:33-38.
74. Dubberke ER, Reske KA, Yan Y, et al. Clostridium difficile: associated disease in a setting of endemicity - identification of novel risk factors. Clin Infect Dis 2007; 45:1543-1549.
75. Jump RL, Pultz MJ, Donskey CJ. Vegetative Clostridium difficile survives in room air on moist surfaces and in gastric contents with reduced acidity: a potential mechanism to explain the association between proton pump inhibitors and C. difficile-associated diarrhea? Antimicrob Agents Chemother 2007; 51:2883-2887.
76. Wilson KH, Sheagren JN, Freter R. Population dynamics of ingested Clostridium difficile in the gastrointestinal tract of the Syrian hamster. J Infect Dis 1985; 151:355-361.
77. Thorens J, Froehlich F, Schwizer W, et al. Bacterial overgrowth during treatment with omeprazole compared with cimetidine: a prospective randomised double blind study. Gut 1996; 39:54-59.
78. Wilkins TD, Lyerly DM. Clostridium difficile testing: after 20 years, still challenging. J Clin Microbiol 2003; 41:531-534.
79. Peterson LR, Kelly PJ. The role of the clinical microbiology laboratory in the management of Clostridium difficile-associated diarrhea. Infect Dis Clin North Am 1993; 7:277-293.
80. Chang TW, Bartlett JG, Gorbach SL, Onderdonk AB. Clindamycin-induced enterocolitis in hamsters as a model of pseudomembranous colitis in patients. Infect Immun 1978; 20:526-529.
81. Nachamkin I, Lotz-Nolan L, Skalina D. Evaluation of a commercial cytotoxicity assay for detection of Clostridium difficile toxin. J Clin Microbiol 1986; 23:954-955.
82. Bartlett JG, Gerding DN. Clinical recognition and diagnosis of Clostridium difficile infection. Clin Infect Dis 2008; 46 (Suppl 1):S12-S18.
83. Gelone SP, Fishman N, Gerding DN, Broom C. Clostridium difficile epidemiology: results of an international web-based survey project. In: Proceedings of SHEA '06; 2006; Chicago: Society for Healthcare Epidemiology of America; 2006.
84. Lyerly DM, Neville LM, Evans DT, et al. Multicenter evaluation of the Clostridium difficile TOX A/B TEST. J Clin Microbiol 1998; 36:184-190.
85. Musher DM, Manhas A, Jain P, et al. Detection of Clostridium difficile toxin: comparison of enzyme immunoassay results with results obtained by cytotoxicity assay. J Clin Microbiol 2007; 45:2737-2739.
86. Reyes RC, John MA,Ayotte DL, et al. Performance of TechLabC, DIFF QUIK CHEK and TechLab C. DIFFICILE TOX A/B II for the detection of Clostridium difficile in stool samples. Diagn Microbiol Infect Dis 2007; 59:33-37.
87. Sunenshine RH, McDonald LC. Clostridium difficile-associated disease: new challenges from an established pathogen. Cleve Clin J Med 2006; 73:187-197.
88. Wanahita A, Goldsmith EA, Marino BJ, Musher DM. Clostridium difficile infection in patients with unexplained leukocytosis. Am J Med 2003; 115:543-546.
89. Cohen SH, Gerding DN, Johnson S, et al. Clostridium difficile infection: clinical practice guidelines by SHEA and IDSA. In: IDSA 45th Annual Meeting; 2007; San Diego, California: Infectious Diseases Society of America; 2007. Updated comprehensive clinical practice guidelines presented at the 45th annual IDSA. The lecture can be reviewed on the IDSA website http://idsociety.org/ Content.aspx?id=7048.
90. 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; 45:302-307.
91. McFarland LV, Beneda HW, Clarridge JE, Raugi GJ. Implications of the changing face of Clostridium difficile disease for healthcare practitioners. Am J Infect Control 2007; 35:237-253.
92. Bartlett JG. Treatment of antibiotic-associated pseudomembranous colitis. Rev Infect Dis 1984; 6 (Suppl 1):S235-S241.
93. Olson MM, Shanholtzer CJ, Lee JT Jr, Gerding DN. Ten years of prospective Clostridium difficile-associated disease surveillance and treatment at the Minneapolis VA Medical Center, 1982-1991. Infect Control Hosp Epidemiol 1994; 15:371-381.
94. Teasley DG, Gerding DN, Olson MM, et al. Prospective randomised trial of metronidazole versus vancomycin for Clostridium-difficile- associated diarrhoea and colitis. Lancet 1983; 2:1043-1046.
95. Bolton RP, Culshaw MA. Faecal metronidazole concentrations during oral and intravenous therapy for antibiotic associated colitis due to Clostridium difficile. Gut 1986; 27:1169-1172.
96. Friedenberg F, Fernandez A, Kaul V, et al. Intravenous metronidazole for the treatment of Clostridium difficile colitis. Dis Colon Rectum 2001; 44:1176-1180.
97. Johnson S, Peterson LR, Gerding DN. Intravenous metronidazole and Clostridium difficile-associated diarrhea or colitis. J Infect Dis 1989; 160:1087-1088.
98. Louie T, Gerson M, Grimard D, et al. Results of a phase III trial comparing tolevamar, vancomycin and metronidazole in patients with Clostridium difficile-associated diarrhea (CDAD) In: Proceedings of the 47th Annual ICAAC; 2007; Chicago: Interscience Conference on Antimicrobial Agents and Chemotherapy; 2007.
99. Wenisch C, Parschalk B, Hasenhundl M, et al. Comparison of vancomycin, teicoplanin, metronidazole, and fusidic acid for the treatment of Clostridium difficile-associated diarrhea. Clin Infect Dis 1996; 22:813-818.
100. Al-Nassir WN, Sethi AK, Li Y, et al. Both oral metronidazole and oral vancomycin promote persistent overgrowth of vancomycin-resistant enterococci during treatment of Clostridium difficile-associated disease. Antimicrob Agents Chemother 2008; 52:2403-2406.
101. Salgado CD, Giannetta ET, Farr BM. Failure to develop vancomycin-resistant Enterococcus with oral vancomycin treatment of Clostridium difficile. Infect Control Hosp Epidemiol 2004; 25:413-417.
102. Page RL 2nd, Klem PM, Rogers C. Potential elevation of tacrolimus trough concentrations with concomitant metronidazole therapy. Ann Pharmacother 2005; 39:1109-1113.
103. Edlund C, Barkholt L, Olsson-Liljequist B, Nord CE. Effect of vancomycin on intestinal flora of patients who previously received antimicrobial therapy. Clin Infect Dis 1997; 25:729-732.
104. Hecht DW, Galang MA, Sambol SP, et al. In vitro activities of 15 antimicrobial agents against 110 toxigenic Clostridium difficile clinical isolates collected from 1983 to 2004. Antimicrob Agents Chemother 2007; 51:2716-2719.
105. ApisarnthanarakA, Razavi B, Mundy LM. Adjunctive intracolonic vancomycin for severe Clostridium difficile colitis: case series and review of the literature. Clin Infect Dis 2002; 35:690-696.
106. Malnick SD, Zimhony O. Treatment of Clostridium difficile- associated diarrhea. Ann Pharmacother 2002; 36:1767-1775.
107. Nathanson DR, Sheahan M, Chao L, Wallack MK. Intracolonic use of vancomycin for treatment of Clostridium difficile colitis in a patient with a diverted colon: report of a case. Dis Colon Rectum 2001; 44:1871-1872.
108. Pasic M, Carrel T, Opravil M, et al. Systemic absorption after local intracolonic vancomycin in pseudomembranous colitis. Lancet 1993; 342:443.
109. Rubin MS, Bodenstein LE, Kent KC. Severe Clostridium difficile colitis. Dis Colon Rectum 1995; 38:350-354.
110. Ali SO, Welch JP, Dring RJ. Early surgical intervention for fulminant pseudomembranous colitis. Am Surg 2008; 74:20-26.
111. Hall JF, Berger D. Outcome of colectomy for Clostridium difficile colitis: a plea for early surgical management. Am J Surg 2008; 196:384-388.
112. Byrn JC, Maun DC, Gingold DS, et al. Predictors of mortality after colectomy for fulminant Clostridium difficile colitis. Arch Surg 2008; 143:150-154; discussion 155.
113. Hassoun A, Ibrahim F. Use of intravenous immunoglobulin for the treatment of severe Clostridium difficile colitis. Am J Geriatr Pharmacother 2007; 5:48-51.
114. McPherson S, Rees CJ, Ellis R, et al. Intravenous immunoglobulin for the treatment of severe, refractory, and recurrent Clostridium difficile diarrhea. Dis Colon Rectum 2006; 49:640-645.
115. Salcedo J, Keates S, Pothoulakis C, et al. Intravenous immunoglobulin therapy for severe Clostridium difficile colitis. Gut 1997; 41:366-370.
116. Warny M, Denie C, Delmee M, LefebvreC. Gammaglobulin administration in relapsing Clostridium difficile-induced pseudomembranous colitis with a defective antibody response to toxin A. Acta Clin Belg 1995; 50:36-39.
117. Juang P, Skledar SJ, Zgheib NK, et al. Clinical outcomes of intravenous immune globulin in severe Clostridium difficile-associated diarrhea. Am J Infect Control 2007; 35:131-137.
118. Barbut F, Richard A, Hamadi K, et al. Epidemiology of recurrences or reinfections of Clostridium difficile-associated diarrhea. J Clin Microbiol 2000; 38:2386-2388.
119. Fekety R, McFarland LV, Surawicz CM, et al. Recurrent Clostridium difficile diarrhea: characteristics of and risk factors for patients enrolled in a prospective, randomized, double-blinded trial. Clin Infect Dis 1997; 24:324-333.
120. McFarland LV, Elmer GW, Surawicz CM. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 2002; 97:1769-1775.
121. Tedesco FJ, Gordon D, Fortson WC. Approach to patients with multiple relapses of antibiotic-associated pseudomembranous colitis. Am J Gastroenterol 1985; 80:867-868.
122. Beales IL. Intravenous immunoglobulin for recurrent Clostridium difficile diarrhoea. Gut 2002; 51:456.
123. Wilcox MH. Descriptive study of intravenous immunoglobulin for the treatment of recurrent Clostridium difficile diarrhoea. J Antimicrob Chemother 2004; 53:882-884.
124. Avery R, Mehta A, Schmitt S, et al. Lactobacillus acidophilus may help to decrease recurrences and ameliorate severity of C. difficile-associated diarrhea in lung transplant recipients. In: International Society for Heart and Lung Transplantation (ISHLT). Boston, MA; 2008.
125. Kimmey MB, Elmer GW, Surawicz CM, McFarland LV. Prevention of further recurrences of Clostridium difficile colitis with Saccharomyces boulardii. Dig Dis Sci 1990; 35:897-901.
126. McFarland LV, Surawicz CM, Greenberg RN, et al. A randomized placebocontrolled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. JAMA 1994; 271:1913-1918.
127. Lawrence SJ, Korzenik JR, Mundy LM. Probiotics for recurrent Clostridium difficile disease. J Med Microbiol 2005; 54 (Pt 9):905-906.
128. Segarra-Newnham M. Probiotics for Clostridium difficile-associated diarrhea: focus on Lactobacillus rhamnosus GG and Saccharomyces boulardii. Ann Pharmacother 2007; 41:1212-1221.
129. Cassone M, Serra P, Mondello F, et al. Outbreak of Saccharomyces cerevisiae subtype boulardii fungemia in patients neighboring those treated with a probiotic preparation of the organism. J Clin Microbiol 2003; 41:5340-5343.
130. De Groote MA, Frank DN, Dowell E, et al. Lactobacillus rhamnosus GG bacteremia associated with probiotic use in a child with short gut syndrome. Pediatr Infect Dis J 2005; 24:278-280.
131. Lherm T, Monet C, Nougiere B, et al. Seven cases of fungemia with Saccharomyces boulardii in critically ill patients. Intensive Care Med 2002; 28:797-801.
132. Vonberg RP, Kuijper EJ, Wilcox MH, et al. Infection control measures to limit the spread of Clostridium difficile. Clin Microbiol Infect 2008; 14 (Suppl 5): 2-20.
133. Bettin K, Clabots C, Mathie P, et al. Effectiveness of liquid soap vs. chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands. Infect Control Hosp Epidemiol 1994; 15:697-702.
134. Boyce JM, Ligi C, Kohan C, et al. Lack of association between the increased incidence of Clostridium difficile-associated disease and the increasing use of alcohol-based hand rubs. Infect Control Hosp Epidemiol 2006; 27:479-483.
135. Gopal RaoG, Jeanes A, Osman M, et al. Marketing hand hygiene in hospitals: a case study. J Hosp Infect 2002; 50:42-47.
136. Gordin FM, Schultz ME, Huber RA, Gill JA. Reduction in nosocomial transmission of drug-resistant bacteria after introduction of an alcohol-based handrub. Infect Control Hosp Epidemiol 2005; 26:650-653.
137. Johnson S, Gerding DN, Olson MM, et al. Prospective, controlled study of vinyl glove use to interrupt Clostridium difficile nosocomial transmission. Am J Med 1990; 88:137-140.
138. Zafar AB, Gaydos LA, Furlong WB, et al. Effectiveness of infection control program in controlling nosocomial Clostridium difficile. Am J Infect Control 1998; 26:588-593.
139. Muto CA, Blank MK, Marsh JW, et al. Control of an outbreak of infection with the hypervirulent Clostridium difficile BI strain in a university hospital using a comprehensive 'bundle'approach. Clin Infect Dis 2007; 45:1266-1273.
140. Dubberke ER, Reske KA, Noble-Wang J, et al. Prevalence of Clostridium difficile environmental contamination and strain variability in multiple healthcare facilities. Am J Infect Control 2007; 35:315-318.
141. Perez J, Springthorpe VS, Sattar SA. Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control. Am J Infect Control 2005; 33:320-325.
142. McMullen KM, ZackJ, Coopersmith CM, et al. Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea. Infect Control Hosp Epidemiol 2007; 28:205-207.
143. Valiquette L, Cossette B, Garant MP, et al. Impact of a reduction in the use of high-risk antibiotics on the course of an epidemic of Clostridium difficile-associated disease caused by the hypervirulent NAP1/027 strain. Clin Infect Dis 2007; 45 (Suppl 2):S112-S121.
144. Fowler S, Webber A, Cooper BS, et al. Successful use of feedback to improve antibiotic prescribing and reduce Clostridium difficile infection: a controlled interrupted time series. J Antimicrob Chemother 2007; 59:990-995.
145. Climo MW, Israel DS, Wong ES, et al. Hospital-wide restriction of clindamycin: effect on the incidence of Clostridium difficile-associated diarrhea and cost. Ann Intern Med 1998; 128 (12 Pt 1):989-995.
146. Davey P, Brown E, Fenelon L, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2005:CD003543.
147. Khan R, Cheesbrough J. Impact of changes in antibiotic policy on Clostridium difficile-associated diarrhoea (CDAD) over a five-year period in a district general hospital. J Hosp Infect 2003; 54:104-108.
148. O'Connor KA, Kingston M, O'Donovan M, et al. Antibiotic prescribing policy and Clostridium difficile diarrhoea. QJM 2004; 97:423-429.
149. Gerding DN, Muto CA, Owens RC Jr. Measures to control and prevent Clostridium difficile infection. Clin Infect Dis 2008; 46 (Suppl 1):S43-S49.
150. Johnson S, Homann SR, Bettin KM, et al. Treatment of asymptomatic Clostridium difficile carriers (fecal excretors) with vancomycin or metronidazole. A randomized, placebo-controlled trial. Ann Intern Med 1992; 117:297-302.