Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-20T05:37:11.991Z Has data issue: false hasContentIssue false

Clostridium difficile in Long-Term–Care Facilities for the Elderly

Published online by Cambridge University Press:  02 January 2015

Andrew E. Simor*
Affiliation:
Department of Microbiology, Sunnybrook and Women's College Health Sciences Centre, Toronto, Ontario, Canada
Suzanne F. Bradley
Affiliation:
Department of Internal Medicine, Veterans' Affairs Health Systems, and theUniversity of Michigan Medical School, Ann Arbor, Michigan
Larry J. Strausbaugh
Affiliation:
VA Medical Center and Oregon Health and, Sciences University School of Medicine, Portland, Oregon
Kent Crossley
Affiliation:
Departments of Education and Internal Medicine, Minneapolis VA Medical Center, and theUniversity of Minnesota Medical School, Minneapolis, Minnesota
Lindsay E. Nicolle
Affiliation:
Department of Medicine, Health Sciences Centre, Winnipeg, Manitoba, Canada.
*
Department of Microbiology, Sunnybrook and Women's College Health Sciences Centre, B121-2075 Bayview Avenue, North York, Ontario M4N 3M5, Canada

Abstract

Antimicrobial agents are among the most frequently prescribed medications in long-term–care facilities (LTCFs). Therefore, it is not surprising that Clostridium difficile colonization and C. difficile-associated diarrhea (CDAD) occur commonly in elderly LTCF residents. C. difficile has been identified as the most common cause of non-epidemic acute diarrheal illness in nursing homes, and outbreaks of CDAD in LTCFs have also been recognized. This position paper reviews the epidemiology and clinical features of CDAD in elderly residents of LTCFs and, using available evidence, provides recommendations for the management of C. difficile in this setting.

Type
SHEA Position Paper
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2002

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.McFarland, LV, Mulligan, ME, Kwok, RY, Stamm, WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204210.Google Scholar
2.Ho, M, Yang, D, Wyle, FA, Mulligan, ME. Increased incidence of Clostridium difficile-associated diarrhea following decreased restriction of antibiotic use. Clin Infect Dis 1996;23(suppl 1):S102S106.CrossRefGoogle ScholarPubMed
3.Karlström, O, Frykland, B, Tullus, K, Burman, LG. A prospective nationwide study of Clostridium difficile-associated diarrhea in Sweden. Clin Infect Dis 1998;26:141145.Google Scholar
4.Alfa, MJ, Du, T, Beda, G. Survey of incidence of Clostridium difficile infection in Canadian hospitals and diagnostic approaches. J Clin Microbiol 1998;36:20762080.CrossRefGoogle ScholarPubMed
5.Nash, JQ, Chattopadhyay, B, Honeycombe, J, Tabaqchali, S. Clostridium difficile and cytotoxin in routine faecal specimens. J Clin Pathol 1982;35:561565.CrossRefGoogle ScholarPubMed
6.Bartlett, JG. Antibiotic-associated pseudomembranous colitis. Rev Infect Dis 1979;1:530539.Google Scholar
7.Aronsson, B, Möllby, R, Nord, CE. Antimicrobial agents and Clostridium difficile in acute enteric disease: epidemiologic data from Sweden, 1980-1982. J Infect Dis 1985;151:476481.CrossRefGoogle ScholarPubMed
8.McFarland, LV, Surawicz, CM, Stamm, WE. Risk factors for Clostridium difficile carriage and C. difficile-associated diarrhea in a cohort of hospitalized patients. J Infect Dis 1990;162:678684.CrossRefGoogle Scholar
9.Brown, E, Talbot, GH, Axelrod, P, Provencher, M, Hoegg, C. Risk factors for Clostridium difficile toxin-associated diarrhea. Infect Control Hosp Epidemiol 1990;11:283290.CrossRefGoogle ScholarPubMed
10.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;28:107113.Google Scholar
11.Hirschorn, LR, Trnka, Y, Onderdonk, A, Lee, ML, Platt, R. Epidemiology of community-acquired Clostridium difficile-associated diarrhea. J Infect Dis 1994;169:127133.Google Scholar
12.Brazier, JS, Fitzgerald, TC, Hosein, I, et al. Screening for carriage and nosocomial acquisition of Clostridium difficile by culture: a study of 284 admissions of elderly patients to six general hospitals in Wales. J Hosp Infect 1999;43:317319.CrossRefGoogle ScholarPubMed
13.Gerding, DN, Johnson, S, Peterson, LR, Mulligan, ME, Silva, J Jr. Clostridium difficile-associated diarrhea and colitis. Infect Control Hosp Epidemiol 1995;16:459477.CrossRefGoogle ScholarPubMed
14.Thomas, DR, Bennett, RG, Laughon, BE, Greenough, WB 3rd, Bartlett, JG. Postantibiotic colonization with Clostridium difficile in nursing home patients. J Am Geriatr Sac 1990;38:415420.CrossRefGoogle ScholarPubMed
15.Simor, AE, Yake, SL, Tsimidis, K. Infection due to Clostridium difficile among elderly residents of a long-term-care facility. Clin Inject Dis 1993;17:672678.CrossRefGoogle ScholarPubMed
16.Sims, RV, Hauser, RJ, Adewale, AO, et al. Acute gastroenteritis in three community-based nursing homes. J Gerontol 1995;50A:M252M256.CrossRefGoogle Scholar
17.Fulton, JD, Fallon, RJ. Is Clostridium difficile endemic in chronic-care facilities? Lancet 1987;2:393394.CrossRefGoogle ScholarPubMed
18.Campbell, RR, Beere, D, Wilcock, GK, Brown, EM. Clostridium difficile in acute and long-stay elderly patients. Age Ageing 1988;17:333336.CrossRefGoogle ScholarPubMed
19.Cefai, C, Elliott, TS, Woodhouse, KW. Gastrointestinal carriage rate of Clostridium difficile in elderly, chronic care hospital patients. J Hosp Infect 1988;21:335339.Google Scholar
20.Corrado, OJ, Mascie-Taylor, BH, Hall, MJ, Bolton, RP. Prevalence of Clostridium difficile on a mixed-function ward for the elderly. J Hosp Infect 1990;21:287292.Google Scholar
21.Bentley, DW. Clostridium difficile-associated disease in long-term care facilities. Infect Control Hosp Epidemiol 1990;11:434438.CrossRefGoogle ScholarPubMed
22.Larson, E, Bobo, L, Bennett, R, et al. Lack of care giver hand contamination with endemic bacterial pathogens in a nursing home. Am J Infect Control 1992;20:1115.CrossRefGoogle ScholarPubMed
23.Walker, KJ, Gilliland, SS, Vance-Bryan, K, et al. Clostridium difficile colonization in residents of long-term care facilities: prevalence and risk factors. J Am Geriatr Soc 1993;41:940946.CrossRefGoogle ScholarPubMed
24.Bender, BS, Bennett, R, Laughon, BE, et al. Is Clostridium difficile endemic in chronic-care facilities? ancet 1986;2:1113.Google ScholarPubMed
25.Monsieur, I, Mets, T, Lauwers, S, De Bock, V, Delmée, M. Clostridium difficile infection in a geriatric ward. Arch Gerontol Geriatr 1991;13:255262.Google Scholar
26.Bennett, GCJ, Allen, E, Millard, PH. Clostridium difficile diarrhoea: a highly infectious organism. Age Ageing 1984;13:363366.Google Scholar
27.Kerr, RB, McLaughlin, DI, Sonnenberg, LW. Control of Clostridium difficile colitis outbreak by treating asymptomatic carriers with metronidazole. Am J Infect Control 1990;18:332335.Google Scholar
28.Cartmill, TDI, Shrimpton, SB, Panigrahi, H, Khanna, V, Brown, R, Poxton, IR. Nosocomial diarrhoea due to a single strain of Clostridium difficile: a prolonged outbreak in elderly patients. Age Ageing 1992;21:245249.CrossRefGoogle ScholarPubMed
29.McNulty, C, Logan, M, Donald, IP, et al. Successful control of Clostridium difficile infection in an elderly care unit through use of a restrictive antibiotic policy. J Antimicrob Chemother 1997;40:707711.CrossRefGoogle Scholar
30.Impallomeni, M, Galletly, NP, Wort, SJ, Starr, JM, Rogers, TR. Increased risk of diarrhoea caused by Clostridium difficile in elderly patients receiving cefotaxime. BMJ 1995;311:13451346.CrossRefGoogle ScholarPubMed
31.Talon, D, Bailly, P, Delmée, M, et al. Use of pulsed-field gel electrophoresis for investigation of an outbreak of Clostridium difficile infection among geriatric patients. Eur J Clin Microbiol Infect Dis 1995;14:987993.Google Scholar
32.Brooks, SE, Veal, RO, Kramer, M, Dore, L, Schupf, N, Adachi, M. Reduction in the incidence of Clostridium dijficile-assodated diarrhea in an acute care hospital and a skilled nursing facility following replacement of electronic thermometers with single-use disposables. Infect Control Hosp Epidemiol 1992;13:98103.CrossRefGoogle Scholar
33.Fawley, WN, Wilcox, MH. Molecular epidemiology of endemic Clostridium difficile infection. Epidemiol Infect 2001;126:343350.Google Scholar
34.Fekety, R, Kim, KH, Brown, D, Batts, DH, Cudmore, M, Silva, J Jr. Epidemiology of antibiotic-associated colitis: isolation of Clostridium diffidle from the hospital environment. Am J Med 1981;70:906908.Google Scholar
35.Samore, MH, Venkataraman, L, DeGirolami, PC, Arbeit, RD, Karchmer, AW. Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea. Am J Med 1996;100:3240.Google Scholar
36.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;88:137140.CrossRefGoogle ScholarPubMed
37.Savage, AM, Alford, RH. Nosocomial spread of Clostridium difficile. Infect Control 1983;4:3133.Google Scholar
38.Bartlett, JG. Clostridium difficile: history of its role as an enteric pathogen and the current state of knowledge about the organism. Clin Infect Dis 1994;18(suppl 4):S265S272.CrossRefGoogle ScholarPubMed
39.Johnson, S, Gerding, DN. Clostridium difficile-associated diarrhea. Clin Infect Dis 1998;26:10271036.Google Scholar
40.Johnson, S, Clabots, CR, Linn, FV, Olson, MM, Peterson, LR, Gerding, DN. Nosocomial Clostridium difficile colonisation and disease. Lancet 1990;336:97100.Google Scholar
41.Shim, JK, Johnson, S, Samore, MH, Bliss, DZ, Gerding, DN. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 1998;351:633636.Google Scholar
42.Bassaris, HP, Lianou, PE, Legakis, NJ, Papavassiliou, JT. Interaction between Clostridium difficile and polymorphonuclear leucocytes from the elderly and post-operative cancer patients: phagocytosis and bactericidal function. Med Microbiol Immunol 1984;173:4955.CrossRefGoogle ScholarPubMed
43.Nakamura, S, Mikawa, M, Nakashio, S, et al. Isolation of Clostridium difficile from the feces and the antibody in sera of young and elderly adults. Microbiol Immunol 1981;25:345351.Google Scholar
44.Bacon, AE 3rd, Fekety, R. Immunoglobulin G directed against toxins A and B of Clostridium difficile in the general population and patients with antibiotic-associated diarrhea. Diagn Microbiol Infect Dis 1994;18:205209.Google Scholar
45.Kyne, L, Warny, M, Qamar, A, Kelly, CP. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet 2001;357:189193.Google Scholar
46.Wilcox, M, Minton, J. Role of antibody response in outcome of antibiotic-associated diarrhoea. Lancet 2001;357:158159.CrossRefGoogle ScholarPubMed
47.Viscidi, R, Laughon, BE, Yolken, R, et al. Serum antibody response to toxins A and B of Clostridium difficile. J Infect Dis 1983;148:93100.CrossRefGoogle Scholar
48.Kyne, L, Warny, M, Qamar, A, Kelly, CP. Asymptomatic carriage of Clostridium diffidle and serum levels of IgG antibody against toxin A. N Engl J Med 2000;342:390397.CrossRefGoogle ScholarPubMed
49.Gerding, DN, Brazier, JS. Optimal methods for identifying Clostridium difficile infections. Clin Infect Dis 1993;16(suppl 4) :S439S442.Google Scholar
50.Rybolt, AH, Bennett, RG, Laughon, BE, Thomas, DR, Greenough, WB 3rd, Bartlett, JG. Protein-losing enteropathy associated with Clostridium diffidle infection. Lancet 1989;1:13531355.Google Scholar
51.Bennett, RG, Greenough, WB 3rd. C. difficile diarrhea: a common—and overlooked—nursing home infection. Geriatrics 1990;45:7787.Google Scholar
52.Brandt, LJ, Rosche, KA, Greenwald, DA, Berkman, D. Clostridium difficile-associated diarrhea in the elderly. Am J Gastroenterol 1999;94:32633266.Google Scholar
53.Young, GP, Bayley, N, Ward, P, St.John, DJB, McDonald, MI. Antibiotic-associated colitis caused by Clostridium difficile: relapse and risk factors. Med J Aust 1986;144:303306.Google Scholar
54.Ramaswamy, R, Grover, H, Corpuz, M, Daniels, P, Pitchumoni, CS. Prognostic criteria in Clostridium difficile colitis. Am J Gastroenterol 1996;91:460464.Google ScholarPubMed
55.Fekety, R, McFarland, LV, Surawicz, CM, Greenberg, RN, Elmer, GW, Mulligan, ME. Recurrent Clostridium difficile diarrhea: characteristics of and risk factors for patients enrolled in a prospective, randomized, double-blinded trial. Clin Infect Dis 1997;24:324333.Google Scholar
56.Nair, S, Yadav, D, Corpuz, M, Pitchumoni, CS. Clostridium difficile colitis: factors influencing treatment failure and relapse, a prospective evaluation. Am J Gastroenterol 1998;93:18731876.Google Scholar
57.Do, AN, Fridkin, SK, Yechouron, A, et al. Risk factors for early recurrent Clostridium difficile-associated diarrhea. Clin Infed Dis 1998;26:954959.Google Scholar
58.Aronsson, B, Möllby, R, Nord, CE. Diagnosis and epidemiology of Clostridium diffidle enterocolitis in Sweden. J Antimicrob Chemother 1984;14(suppl D):8595.Google Scholar
59.Cohen, SH, Tang, YJ, Hansen, B, Silva, J Jr. Isolation of a toxin B-deficient mutant strain of Clostridium difficile in a case of recurrent C. difficile-associated diarrhea. Clin Infect Dis 1998;26:410412.CrossRefGoogle Scholar
60.Al-Barrack, A, Embil, J, Dyck, B, et al. An outbreak of toxin A negative, toxin B positive Clostridium difficile-associated diarrhea in a Canadian tertiary-care hospital. Can Commun Dis Rep 1999;25:6569.Google Scholar
61.Limaye, AP, Turgeon, DK, Cookson, BT, Fritsche, TR. Pseudomembranous colitis caused by a toxin A(-)B(+) strain of Clostridium difficile. J Clin Microbiol 2000;38:16961697.Google Scholar
62.Doern, GV, Coughlin, RT, Wu, L. Laboratory diagnosis of Clostridium difficile-associated gastrointestinal disease: comparison of a monoclonal antibody enzyme immunoassay for toxins A and B with a monoclonal antibody enzyme immunoassay for toxin A only and two cytotoxin assays. J Clin Microbiol 1992;30:20422046.Google Scholar
63.Riederer, KM, Lawson, P, Held, MS, Petrylka, K, Briski, LE, Khatib, R. Diagnosis of Clostridium difficile associated diarrhea: comparison of three rapid methods employing different markers for detection. Can J Microbiol 1995;41:8891.Google Scholar
64.Aldeen, WE, Bingham, M, Alderzada, A, Kucera, J, Jense, S, Carroll, KC. Comparison of the TOX A/B test to a cell culture cytotoxidty assay for the detection of Clostridium difficile in stools. Diagn Microbiol Infect Dis 2000;36:211213.Google Scholar
65.Kristiánsson, M, Samore, MH, Gerding, DN, et al. Comparison of restriction endonuclease analysis, ribotyping, and pulsed-field gel electrophoresis for molecular differentiation of Clostridium difficile strains. J Clin Microbiol 1994;32:19631969.Google Scholar
66.Samore, MH, Kristiánsson, M, Venkataraman, L, DeGirolami, PC, Arbeit, RD. Comparison of arbitrarily-primed polymerase chain reaction, restriction enzyme analysis and pulsed-field gel electrophoresis for typing Clostridium difficile. J Microbiol Methods 1996;25:215224.CrossRefGoogle Scholar
67.Samore, M, Killgore, G, Johnson, S, et al. Multicenter typing comparison of sporadic and outbreak Clostridium difficile isolates from geographically diverse hospitals. J Infect Dis 1997;176:12331238.Google Scholar
68.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;15:371381.Google Scholar
69.Fekety, R. Guidelines for the diagnosis and management of Clostridium difficile-associated diarrhea and colitis. American College of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol 1997; 92:739750.Google ScholarPubMed
70.Teasley, DG, Gerding, DN, Olson, MM, et al. Prospective randomised trial of metronidazole versus vancomycin for Clostridium difficile-associated diarrhoea and colitis. Lancet 1983;2:10431046.Google Scholar
71.Wenisch, C, Parschalk, B, Hasenhündl, M, Hirschl, AM, Graninger, W. Comparison of vancomycin, teicoplanin, metronidazole, and fusidic acid for the treatment of Clostridium difficile-associated diarrhea. Clin Infed Dis 1996;22:813818.CrossRefGoogle ScholarPubMed
72.Kelly, CP, Pothoulakis, C, LaMont, JT. Clostridium difficile colitis. N Engl J Med 1994;330:257262.Google Scholar
73.Hospital Infection Control Practices Advisory Committee (HICPAC). Recommendations for preventing the spread of vancomycin resistance. Infect Control Hosp Epidemiol 1995;16:105113.CrossRefGoogle Scholar
74.Cohen, H, Brocavich, JM. Managing Clostridium difficile colitis in patients who lack oral access. Infections in Medicine 1996;13:101109.Google Scholar
75.Young, GP, Ward, PB, Bayley, N, et al. Antibiotic-associated colitis due to Clostridium difficile: double-blind comparison of vancomycin with bacitracin. Gastroenterology 1985;89:10381045.Google Scholar
76.Dudley, MN, McLaughlin, JC, Carrington, G, Frick, J, Nightingale, CH, Quintiliani, R. Oral bacitracin vs vancomycin therapy for Clostridium difficile-induced diarrhea: a randomized double-blind trial. Arch Intern Med 1986;146:11011104.CrossRefGoogle ScholarPubMed
77.Cronberg, S, Castor, B, Thorén, A. Fusidic add for the treatment of antibiotic-associated colitis induced by Clostridium difficile. Infection 1984;12:276279.Google Scholar
78.de Lalla, F, Nicolin, R, Rinaldi, E, et al. Prospective study of oral teicoplanin versus oral vancomycin for therapy of pseudomembranous colitis and Clostridium difficile-associated diarrhea. Antimicrob Agents Chemother 1992;36:21922196.CrossRefGoogle ScholarPubMed
79.Kurtz, CB, Cannon, EP, Brezzani, A, et al. GT160-246, a toxin binding polymer for treatment of Clostridium difficile colitis. Antimicrob Agents Chemother 2001;45:23402347.Google Scholar
80.Gerding, DN. Treatment of Clostridium difficile-associated diarrhea and colitis. Current Topics in Clinical Microbiology and Immunology 2000;250:127139.Google Scholar
81.Barbut, F, Richard A Hamadi, K, Chomette, V, Burghoffer, B, Petit, J-C. Epidemiology of recurrences or reinfections of Clostridium difficile-associated diarrhea. J Clin Microbiol 2000;38:23862388.CrossRefGoogle ScholarPubMed
82.Buggy, BP, Fekety, R, Silva, J Jr. Therapy of relapsing Clostridium difficile-associated diarrhea and colitis with the combination of vancomycin and rifampin. J Clin Gastroenterol 1987;9:155159.CrossRefGoogle ScholarPubMed
83.McFarland, LV, Surawicz, CM, Greenberg, RN, et al. A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. JAMA 1994;271:19131918.Google Scholar
84.Surawicz, CM, McFarland, LV, Greenberg, RN, et al. The search for a better treatment for recurrent Clostridium diffidle disease: use of high-dose vancomycin combined with Saccharomyces boulardii. Clin Infect Dis 2000;31:10121017.Google Scholar
85.Gorbach, SL, Chang, T-W, Goldin, B. Successful treatment of relapsing Clostridium difficile colitis with Ladobacillus GG. Lancet 1987;2:1519.Google Scholar
86.Bennett, RG, Gorbach, SL, Goldin, BR, et al. Treatment of relapsing Clostridium difficile diarrhea with Ladobacillus GG. Nutrition Today Supplement 1996;31:35S38S.Google Scholar
87.Kelly, CP, LaMont, JT. Clostridium difficile infection. Annual Reviews of Medicine 1998;49:375390.Google Scholar
88.Lipsett, PA, Samantaray, DK, Tam, ML, Bartlett, JG, Lillemoe, KD. Pseudomembranous colitis: a surgical disease? Surgery 1994;116:491496.Google Scholar
89.Bettin, K, Clabots, C, Mathie, P, Willard, K, Gerding, DN. Effectiveness of a liquid soap vs chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands. Infect Control Hosp Epidemiol 1994;15:697702.Google Scholar
90.Boyce, JM. Using alcohol for hand antisepsis: dispelling old myths. Infect Control Hosp Epidemiol 2000;21:438441.Google Scholar
91.Larson, EL. APIC guideline for handwashing and hand antisepsis in health care settings. Am J Infect Control 1995;23:251269.Google Scholar
92.Struelens, MJ, Maas, A, Nonhoff, C, et al. Control of nosocomial transmission of Clostridium difficile based on sporadic case surveillance. Am J Med 1991;91(suppl 3B):138S144S.Google Scholar
93.Zafar, AB, Gaydos, IA, Furlong, WB, Nguyen, MH, Mennonna, PA. Effectiveness of infection control program in controlling nosocomial Clostridium difficile. Am J Infect Control 1998;26:588593.Google Scholar
94.Wilcox, MH, Fawley, WN. Hospital disinfectants and spore formation by Clostridium difficile. Lancet 2000;356:1324.Google Scholar
95.Delmée, M, Vandercam, B, Avesani, V, Michaux, JL. Epidemiology and prevention of Clostridium difficile infections in a leukemia unit. Eur J Clin Microbiol 1987;6:623627.CrossRefGoogle Scholar
96.Kaatz, GW, Gitlin, SD, Schaberg, DR, et al. Acquisition of Clostridium difficile from the hospital environment. Am J Epidemiol 1988;127:12891294.Google Scholar
97.Mayfield, JL, Leet, T, Miller, J, Mundy, LM. Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis 2000;31:9951000.Google Scholar
98.Verity, P, Wilcox, MH, Fawley, W, Parnell, P. Prospective evaluation of environmental contamination by Clostridium difficile in isolation side rooms. J Hosp Infect 2001;49:204209.CrossRefGoogle ScholarPubMed
99.Perry, C, Marshall, R, Jones, E. Bacterial contamination of uniforms. J Hosp Infect 2001;48:238241.Google Scholar
100.Samore, MH. Epidemiology of nosocomial Clostridium difficile diarrhoea. J Hosp Infect 1999;43(suppl):S183S190.Google Scholar
101.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;117:297302.Google Scholar
102.Pear, SM, Williamson, TH, Bettin, KM, Gerding, DN, Galgiani, JN. Decrease in nosocomial Clostridium difficile-associated diarrhea by restricting clindamycin use. Ann Intern Med 1994;120:272277.Google Scholar
103.Climo, MW, Israel, DS, Wong, ES, Williams, D, Coudron, P, Markowitz, SM. Hospital-wide restriction of clindamycin: effect on the incidence of Clostridium difficile-associated diarrhea and cost. Ann Intern Med 1998;128:989995.Google Scholar
104.Nicolle, LE, Bentley, DW, Garibaldi, R, Neuhaus, EG, Smith, PW. Antimicrobial use in long-term-care facilities. Infect Control Hosp Epidemiol 2000;21:537545.Google Scholar
105.Surawicz, CM, Elmer, GW, Speelman, P, McFarland, LV, Chinn, J, van Belle, G. Prevention of antibiotic-associated diarrhea by Saccharomyces boulardii: a prospective study. Gastroenterology 1989;96:981988.Google Scholar
106.Lewis, SJ, Potts, LF, Barry, RE. The lack of therapeutic effect of Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea in elderly patients. J Infect 1998;36:171174.CrossRefGoogle Scholar
107.Gotz, V, Romankiewicz, JA, Moss, J, Murray, HW. Prophylaxis against ampicillin-associated diarrhea with a lactobacillus preparation. American Journal of Hospital Pharmacy 1979;36:754757.Google Scholar
108.Thomas, MR, Litin, SC, Osmon, DR, Corr, AP, Weaver, AL, Lohse, CM. Lack of effect of Ladobacillus GG on antibiotic-associated diarrhea: a randomized, placebc-controlled trial. Mayo Clin Proc 2001;76:883889.Google Scholar
109.Gross, PA, Barrett, TI, Dellinger, EP, et al. Consensus development of quality standards. Infect Control Hosp Epidemiol 1994;151:180181.Google Scholar