Risk factors for acquisition and loss of Clostridium difficile colonization in hospitalized patients

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 8, 2015, Pages 4533-4543

  Dubberke, Erik R ^a   Reske, Kimberly A ^a   Seiler, Sondra ^a   Hink, Tiffany ^a   Kwon, Jennie H ^a   Burnham, Carey Ann D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE; BETA LACTAMASE INHIBITOR; CARBAPENEM; CEPHALOSPORIN; CLINDAMYCIN; CLOSTRIDIUM TOXIN; DAPTOMYCIN; DOXYCYCLINE; HISTAMINE H2 RECEPTOR ANTAGONIST; LAXATIVE; LINEZOLID; MACROLIDE; METRONIDAZOLE; NARCOTIC AGENT; PENICILLIN DERIVATIVE; PROTON PUMP INHIBITOR; VANCOMYCIN; ANTIINFECTIVE AGENT; CEPHALOSPORIN DERIVATIVE;

ADULT; AGE; AGED; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATE; CHRONIC KIDNEY DISEASE; CHRONIC LIVER DISEASE; CHRONIC LUNG DISEASE; CLINICAL LABORATORY; CLOSTRIDIUM INFECTION; COHORT ANALYSIS; COMORBIDITY; CONGESTIVE HEART FAILURE; DIABETES MELLITUS; DISEASE EXACERBATION; DRUG USE; FECES ANALYSIS; FEMALE; FEVER; GASTROINTESTINAL ENDOSCOPY; GENDER; HEALTH CARE FACILITY; HEALTH CARE PERSONNEL; HEMATOLOGIC MALIGNANCY; HOME; HOSPITAL ADMISSION; HOSPITAL DISCHARGE; HOSPITAL PATIENT; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOCOMPROMISED PATIENT; INFLAMMATORY BOWEL DISEASE; INTERVIEW; LABORATORY TEST; LENGTH OF STAY; MAJOR CLINICAL STUDY; MALE; MEDICAL HISTORY; MEDICAL RECORD REVIEW; NONHUMAN; NURSING HOME; ORGAN TRANSPLANTATION; OUTPATIENT DEPARTMENT; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; PROSPECTIVE STUDY; RACE; RETROSPECTIVE STUDY; RIBOTYPING; RISK FACTOR; SOLID TUMOR; STEM CELL TRANSPLANTATION; STOMA; SURGICAL WARD; TERTIARY CARE CENTER; CLOSTRIDIUM INFECTIONS; CROSS INFECTION; DRUG EFFECTS; FECES; HOSPITAL; HOSPITALIZATION; ISOLATION AND PURIFICATION; MICROBIOLOGY; PROCEDURES; STATISTICAL MODEL;

ANTI-BACTERIAL AGENTS; BETA-LACTAMASE INHIBITORS; CEPHALOSPORINS; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; CROSS INFECTION; FECES; FEMALE; HOSPITALIZATION; HOSPITALS; HUMANS; LOGISTIC MODELS; MALE; PROSPECTIVE STUDIES; RIBOTYPING; RISK FACTORS;

EID: 84939824536     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00642-15     Document Type: Article

References (54)

1. Dubberke ER, Butler AM, Reske KA, Agniel D, Olsen MA, D'Angelo G, McDonald LC, Fraser VJ. 2008. Attributable outcomes of endemic Clostridium difficile-associated disease in nonsurgical patients. Emerg Infect Dis 14:1031-1038. http://dx.doi.org/10.3201/eid1407.070867.
2. Johnson S. 2009. Recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J Infect 58:403-410. http://dx.doi.org/10.1016/j.jinf.2009.03.010.
3. Karas JA, Enoch DA, Aliyu SH. 2010. A review of mortality due to Clostridium difficile infection. J Infect 61:1-8. http://dx.doi.org/10.1016/j.jinf.2010.03.025.
4. Miller M, Gravel D, Mulvey M, Taylor G, Boyd D, Simor A, Gardam M, McGeer A, Hutchinson J, Moore D, Kelly S. 2010. Health care-associated Clostridium difficile infection in Canada: patient age and infecting strain type are highly predictive of severe outcome and mortality. Clin Infect Dis 50:194-201. http://dx.doi.org/10.1086/649213.
5. Dubberke ER, Olsen MA. 2012. Burden of Clostridium difficile on the healthcare system. Clin Infect Dis 55(Suppl 2):S88-S92. http://dx.doi.org/10.1093/cid/cis335.
6. Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S, Bourgault AM, Nguyen T, Frenette C, Kelly M, Vibien A, Brassard P, Fenn S, Dewar K, Hudson TJ, Horn R, Rene P, Monczak Y, Dascal A. 2005. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 353:2442-2449. http://dx.doi.org/10.1056/NEJMoa051639.
7. Muto CA, Pokrywka M, Shutt K, Mendelsohn AB, Nouri K, Posey K, Roberts T, Croyle K, Krystofiak S, Patel-Brown S, Pasculle AW, Paterson DL, Saul M, Harrison LH. 2005. 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 26:273-280. http://dx.doi.org/10.1086/502539.
8. Pépin J, Valiquette L, Cossette B. 2005. Mortality attributable to nosocomial Clostridium difficile-associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 173:1037-1042. http://dx.doi.org/10.1503/cmaj.050978.
9. Kelly CP, LaMont JT. 2008. Clostridium difficile-more difficult than ever. N Engl J Med 359:1932-1940. http://dx.doi.org/10.1056/NEJMra0707500.
10. McDonald LC, Owings M, Jernigan DB. 2006. Clostridium difficile infection in patients discharged from U.S. short-stay hospitals, 1996-2003. Emerg Infect Dis 12:409-415. http://dx.doi.org/10.3201/eid1203.051064.
11. McFarland LV, Mulligan ME, Kwok RY, Stamm WE. 1989. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320:204-210. http://dx.doi.org/10.1056/NEJM198901263200402.
12. Samore MH, Venkataraman L, DeGirolami PC, Arbeit RD, Karchmer AW. 1996. Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea. Am J Med 100:32-40. http://dx.doi.org/10.1016/S0002-9343(96)90008-X.
13. Sethi AK, Al-Nassir WN, Nerandzic MM, Bobulsky GS, Donskey CJ. 2010. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol 31:21-27. http://dx.doi.org/10.1086/649016.
14. Didelot X, Eyre DW, Cule M, Ip CL, Ansari MA, Griffiths D, Vaughan A, O'Connor L, Golubchik T, Batty EM, Piazza P, Wilson DJ, Bowden R, Donnelly PJ, Dingle KE, Wilcox M, Walker AS, Crook DW, Peto TE, Harding RM. 2012. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol 13:R118. http://dx.doi.org/10.1186/gb-2012-13-12-r118.
15. Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A, O'Connor L, Ip CL, Golubchik T, Batty EM, Finney JM, Wyllie DH, Didelot X, Piazza P, Bowden R, Dingle KE, Harding RM, Crook DW, Wilcox MH, Peto TE, Walker AS. 2013. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 369:1195-1205. http://dx.doi.org/10.1056/NEJMoa1216064.
16. Walker AS, Eyre DW, Wyllie DH, Dingle KE, Harding RM, O'Connor L, Griffiths D, Vaughan A, Finney J, Wilcox MH, Crook DW, Peto TE. 2012. Characterisation of Clostridium difficile hospital ward-based transmission using extensive epidemiological data and molecular typing. PLoS Med 9:e1001172. http://dx.doi.org/10.1371/journal.pmed.1001172.
17. Wullt M, Laurell MH. 1999. Low prevalence of nosocomial Clostridium difficile transmission, as determined by comparison of arbitrarily primed PCR and epidemiological data. J Hosp Infect 43:265-273. http://dx.doi.org/10.1016/S0195-6701(99)90422-X.
18. Clabots CR, Johnson S, Olson MM, Peterson LR, Gerding DN. 1992. Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis 166:561-567. http://dx.doi.org/10.1093/infdis/166.3.561.
19. Lanzas C, Dubberke ER, Lu Z, Reske KA, Grohn YT. 2011. Epidemiological model for Clostridium difficile transmission in healthcare settings. Infect Control Hosp Epidemiol 32:553-561. http://dx.doi.org/10.1086/660013.
20. Curry SR, Muto CA, Schlackman JL, Pasculle AW, Shutt KA, Marsh JW, Harrison LH. 2013. Use of multilocus variable number of tandem repeats analysis genotyping to determine the role of asymptomatic carriers in Clostridium difficile transmission. Clin Infect Dis 57:1094-1102. http://dx.doi.org/10.1093/cid/cit475.
21. McDonald LC. 2013. Editorial commentary: looking to the future: vertical vs horizontal prevention of Clostridium difficile infections. Clin Infect Dis 57:1103-1105. http://dx.doi.org/10.1093/cid/cit477.
22. Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN. 1990. Nosocomial Clostridium difficile colonisation and disease. Lancet 336:97-100. http://dx.doi.org/10.1016/0140-6736(90)91605-A.
23. Alasmari F, Seiler SM, Hink T, Burnham CA, Dubberke ER. 2014. Prevalence and risk factors for asymptomatic Clostridium difficile carriage. Clin Infect Dis 59:216-222. http://dx.doi.org/10.1093/cid/ciu258.
24. Eyre DW, Griffiths D, Vaughan A, Golubchik T, Acharya M, O'Connor L, Crook DW, Walker AS, Peto TE. 2013. Asymptomatic Clostridium difficile colonisation and onward transmission. PLoS One 8:e78445. http://dx.doi.org/10.1371/journal.pone.0078445.
25. Hutin Y, Casin I, Lesprit P, Welker Y, Decazes JM, Lagrange P, ModaïJ, Molina JM. 1997. Prevalence of and risk factors for Clostridium difficile colonization at admission to an infectious diseases ward. Clin Infect Dis 24:920-924. http://dx.doi.org/10.1093/clinids/24.5.920.
26. Leekha S, Aronhalt KC, Sloan LM, Patel R, Orenstein R. 2013. Asymptomatic Clostridium difficile colonization in a tertiary care hospital: admission prevalence and risk factors. Am J Infect Control 41:390-393. http://dx.doi.org/10.1016/j.ajic.2012.09.023.
27. Samore MH, DeGirolami PC, Tlucko A, Lichtenberg DA, Melvin ZA, Karchmer AW. 1994. Clostridium difficile colonization and diarrhea at a tertiary care hospital. Clin Infect Dis 18:181-187. http://dx.doi.org/10.1093/clinids/18.2.181.
28. Loo VG, Bourgault AM, Poirier L, Lamothe F, Michaud S, Turgeon N, Toye B, Beaudoin A, Frost EH, Gilca R, Brassard P, Dendukuri N, Beliveau C, Oughton M, Brukner I, Dascal A. 2011. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med 365:1693-1703. http://dx.doi.org/10.1056/NEJMoa1012413.
29. Hink T, Burnham CA, Dubberke ER. 2013. A systematic evaluation of methods to optimize culture-based recovery of Clostridium difficile from stool specimens. Anaerobe 19:39-43. http://dx.doi.org/10.1016/j.anaerobe.2012.12.001.
30. Westblade LF, Chamberland RR, Maccannell D, Collins R, Dubberke ER, Dunne WM, Jr, Burnham CA. 2013. Development and evaluation of a novel, semiautomated Clostridium difficile typing platform. J Clin Microbiol 51:621-624. http://dx.doi.org/10.1128/JCM.02627-12.
31. Antikainen J, Pasanen T, Mero S, Tarkka E, Kirveskari J, Kotila S, Mentula S, Könönen E, Virolainen-Julkunen AR, Vaara M, Tissari P. 2009. Detection of virulence genes of Clostridium difficile by multiplex PCR. APMIS 117:607-613. http://dx.doi.org/10.1111/j.1600-0463.2009.02509.x.
32. Brazier JS, Fitzgerald TC, Hosein I, Cefai C, Looker N, Walker M, Bushell AC, Rooney P. 1999. 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 43:317-319. http://dx.doi.org/10.1016/S0195-6701(99)90431-0.
33. Heard SR, O'Farrell S, Holland D, Crook S, Barnett MJ, Tabaqchali S. 1986. The epidemiology of Clostridium difficile with use of a typing scheme: nosocomial acquisition and cross-infection among immunocompromised patients. J Infect Dis 153:159-162. http://dx.doi.org/10.1093/infdis/153.1.159.
34. Kyne L, Warny M, Qamar A, Kelly CP. 2000. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med 342:390-397. http://dx.doi.org/10.1056/NEJM200002103420604.
35. Rudensky B, Rosner S, Sonnenblick M, van Dijk Y, Shapira E, Isaacsohn M. 1993. The prevalence and nosocomial acquisition of Clostridium difficile in elderly hospitalized patients. Postgrad Med J 69:45-47. http://dx.doi.org/10.1136/pgmj.69.807.45.
36. Schoevaerdts D, Swine C, Verroken A, Huang TD, Glupczynski Y. 2011. Asymptomatic colonization by Clostridium difficile in older adults admitted to a geriatric unit: a prospective cohort study. J Am Geriatr Soc 59:2179-2181. http://dx.doi.org/10.1111/j.1532-5415.2011.03685.x.
37. Labbé AC, Poirier L, Maccannell D, Louie T, Savoie M, Beliveau C, Laverdiere M, Pépin J. 2008. Clostridium difficile infections in a Canadian tertiary care hospital before and during a regional epidemic associated with the BI/NAP1/027 strain. Antimicrob Agents Chemother 52:3180-3187. http://dx.doi.org/10.1128/AAC.00146-08.
38. See I, Mu Y, Cohen J, Beldavs ZG, Winston LG, Dumyati G, Holzbauer S, Dunn J, Farley MM, Lyons C, Johnston H, Phipps E, Perlmutter R, Anderson L, Gerding DN, Lessa FC. 2014. NAP1 strain type predicts outcomes from Clostridium difficile infection. Clin Infect Dis 58:1394-1400. http://dx.doi.org/10.1093/cid/ciu125.
39. Walker AS, Eyre DW, Wyllie DH, Dingle KE, Griffiths D, Shine B, Oakley S, O'Connor L, Finney J, Vaughan A, Crook DW, Wilcox MH, Peto TE, Infections in Oxfordshire Research Database. 2013. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin Infect Dis 56:1589-1600. http://dx.doi.org/10.1093/cid/cit127.
40. Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, Frost E, McDonald LC. 2005. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 366:1079-1084. http://dx.doi.org/10.1016/S0140-6736(05)67420-X.
41. Slimings C, Riley TV. 2014. Antibiotics and hospital-acquired Clostridium difficile infection: update of systematic review and metaanalysis. J Antimicrob Chemother 69:881-891. http://dx.doi.org/10.1093/jac/dkt477.
42. Dubberke ER, Reske KA, Yan Y, Olsen MA, McDonald LC, Fraser VJ. 2007. Clostridium difficile-associated disease in a setting of endemicity: identification of novel risk factors. Clin Infect Dis 45:1543-1549. http://dx.doi.org/10.1086/523582.
43. Wilcox MH, Freeman J, Fawley W, MacKinlay S, Brown A, Donaldson K, Corrado O. 2004. Long-term surveillance of cefotaxime and piperacillin-tazobactam prescribing and incidence of Clostridium difficile diarrhoea. J Antimicrob Chemother 54:168-172. http://dx.doi.org/10.1093/jac/dkh285.
44. Alston WK, Ahern JW. 2004. Increase in the rate of nosocomial Clostridium difficile-associated diarrhoea during shortages of piperacillintazobactam and piperacillin. J Antimicrob Chemother 53:549-550. http://dx.doi.org/10.1093/jac/dkh127.
45. Settle CD, Wilcox MH, Fawley WN, Corrado OJ, Hawkey PM. 1998. Prospective study of the risk of Clostridium difficile diarrhoea in elderly patients following treatment with cefotaxime or piperacillin-tazobactam. Aliment Pharmacol Ther 12:1217-1223. http://dx.doi.org/10.1046/j.1365-2036.1998.00428.x.
46. Cleary RK, Grossmann R, Fernandez FB, Stull TS, Fowler JJ, Walters MR, Lampman RM. 1998. Metronidazole may inhibit intestinal colonization with Clostridium difficile. Dis Colon Rectum 41:464-467. http://dx.doi.org/10.1007/BF02235760.
47. Rodriguez S, Hernandez MB, Tarchini G, Zaleski M, Vatanchi M, Cardona L, Castro-Pavia F, Schneider A. 2014. Risk of Clostridium difficile infection in hospitalized patients receiving metronidazole for a non-C. difficile infection. Clin Gastroenterol Hepatol 12:1856-1861. http://dx.doi.org/10.1016/j.cgh.2014.02.040.
48. Pultz NJ, Donskey CJ. 2005. Effect of antibiotic treatment on growth of and toxin production by Clostridium difficile in the cecal contents of mice. Antimicrob Agents Chemother 49:3529-3532. http://dx.doi.org/10.1128/AAC.49.8.3529-3532.2005.
49. Baines SD, Freeman J, Wilcox MH. 2005. Effects of piperacillin/tazobactam on Clostridium difficile growth and toxin production in a human gut model. J Antimicrob Chemother 55:974-982. http://dx.doi.org/10.1093/jac/dki120.
50. Johnson S, Homann SR, Bettin KM, Quick JN, Clabots CR, Peterson LR, Gerding DN. 1992. Treatment of asymptomatic Clostridium difficile carriers (fecal excretors) with vancomycin or metronidazole. A randomized, placebo-controlled trial. Ann Intern Med 117:297-302.
51. Baines SD, O'Connor R, Freeman J, Fawley WN, Harmanus C, Mastrantonio P, Kuijper EJ, Wilcox MH. 2008. Emergence of reduced susceptibility to metronidazole in Clostridium difficile. J Antimicrob Chemother 62:1046-1052. http://dx.doi.org/10.1093/jac/dkn313.
52. Shim JK, Johnson S, Samore MH, Bliss DZ, Gerding DN. 1998. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 351:633-636. http://dx.doi.org/10.1016/S0140-6736(97)08062-8.
53. Adams DA, Riggs MM, Donskey CJ. 2007. Effect of fluoroquinolone treatment on growth of and toxin production by epidemic and nonepidemic Clostridium difficile strains in the cecal contents of mice. Antimicrob Agents Chemother 51:2674-2678. http://dx.doi.org/10.1128/AAC.01582-06.
54. Owens RC, Jr, Donskey CJ, Gaynes RP, Loo VG, Muto CA. 2008. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin Infect Dis 46(Suppl 1):S19-S31. http://dx.doi.org/10.1086/521859.