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Open Access 01-12-2015 | Research article

Asymptomatic Clostridium difficile colonization: epidemiology and clinical implications

Authors: Luis Furuya-Kanamori, John Marquess, Laith Yakob, Thomas V. Riley, David L. Paterson, Niki F. Foster, Charlotte A. Huber, Archie C. A. Clements

Published in: BMC Infectious Diseases | Issue 1/2015

Abstract

Background

The epidemiology of Clostridium difficile infection (CDI) has changed over the past decades with the emergence of highly virulent strains. The role of asymptomatic C. difficile colonization as part of the clinical spectrum of CDI is complex because many risk factors are common to both disease and asymptomatic states. In this article, we review the role of asymptomatic C. difficile colonization in the progression to symptomatic CDI, describe the epidemiology of asymptomatic C. difficile colonization, assess the effectiveness of screening and intensive infection control practices for patients at risk of asymptomatic C. difficile colonization, and discuss the implications for clinical practice.

Methods

A narrative review was performed in PubMed for articles published from January 1980 to February 2015 using search terms ‘Clostridium difficile’ and ‘colonization’ or ‘colonisation’ or ‘carriage’.

Results

There is no clear definition for asymptomatic CDI and the terms carriage and colonization are often used interchangeably. The prevalence of asymptomatic C. difficile colonization varies depending on a number of host, pathogen, and environmental factors; current estimates of asymptomatic colonization may be underestimated as stool culture is not practical in a clinical setting.

Conclusions

Asymptomatic C. difficile colonization presents challenging concepts in the overall picture of this disease and its management. Individuals who are colonized by the organism may acquire protection from progression to disease, however they also have the potential to contribute to transmission in healthcare settings.

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Hall I, O’Toole E. Intestinal flora in new-born infants: with a description of a new pathogenic anaerobe, Bacillus difficilis. Am J Dis Child. 1935;49:390–402.

Tattevin P, Buffet-Bataillon S, Donnio PY, Revest M, Michelet C. Clostridium difficile infections: do we know the real dimensions of the problem? Int J Antimicrob Agents. 2013;42:S36–40.PubMed

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

Centers for Disease Control & Prevention. Antibiotic Resistance Threats in the United States, 2013. U.S. Department of Health and Human Services. 2013. http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf. Accessed Jun 2015.

Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol. 2009;7:526–36.PubMed

Voth DE, Ballard JD. Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev. 2005;18:247–63.PubMedCentralPubMed

McFarland LV, Beneda HW, Clarridge JE, Raugi GJ. Implications of the changing face of Clostridium difficile disease for health care practitioners. Am J Infect Control. 2007;35:237–53.PubMed

Shim JK, Johnson S, Samore MH, Bliss DZ, Gerding DN. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet. 1998;351:633–6.PubMed

Riggs MM, Sethi AK, Zabarsky TF, Eckstein EC, Jump RL, Donskey CJ. 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;45:992–8.PubMed

10.

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

11.

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

12.

Johnson S, Gerding DN, Olson MM, Weiler MD, Hughes RA, Clabots CR, et al. Prospective, controlled study of vinyl glove use to interrupt Clostridium difficile nosocomial transmission. Am J Med. 1990;88:137–40.PubMed

13.

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

14.

Clements AC, Magalhaes 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

15.

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

16.

Gerding DN, Johnson S, Peterson LR, Mulligan ME, Silva Jr J. Clostridium difficile-associated diarrhea and colitis. Infect Control Hosp Epidemiol. 1995;16:459–77.PubMed

17.

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.PubMedCentralPubMed

18.

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

19.

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

20.

Polage CR, Solnick JV, Cohen SH. Nosocomial diarrhea: evaluation and treatment of causes other than Clostridium difficile. Clin Infect Dis. 2012;55:982–9.PubMedCentralPubMed

21.

McFarland LV. Epidemiology of infectious and iatrogenic nosocomial diarrhea in a cohort of general medicine patients. Am J Infect Control. 1995;23:295–305.PubMed

22.

Gerding DN, Olson MM, Peterson LR, Teasley DG, Gebhard RL, Schwartz ML, et al. Clostridium difficile-associated diarrhea and colitis in adults. A prospective case-controlled epidemiologic study. Arch Intern Med. 1986;146:95–100.PubMed

23.

Geric B, Carman RJ, Rupnik M, Genheimer CW, Sambol SP, Lyerly DM, et al. Binary Toxin–Producing, Large Clostridial Toxin–Negative Clostridium difficile Strains Are Enterotoxic but Do Not Cause Disease in Hamsters. J Infect Dis. 2006;193:1143–50.PubMed

24.

Natarajan M, Walk ST, Young VB, Aronoff DM. A clinical and epidemiological review of non-toxigenic Clostridium difficile. Anaerobe. 2013;22:1–5.PubMedCentralPubMed

25.

Behroozian AA, Chludzinski JP, Lo ES, Ewing SA, Waslawski S, Newton DW, et al. Detection of mixed populations of Clostridium difficile from symptomatic patients using capillary-based polymerase chain reaction ribotyping. Infect Control Hosp Epidemiol. 2013;34:961–6.PubMedCentralPubMed

26.

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.

27.

Ozaki E, Kato H, Kita H, Karasawa T, Maegawa T, Koino Y, et al. Clostridium difficile colonization in healthy adults: transient colonization and correlation with enterococcal colonization. J Med Microbiol. 2004;53:167–72.PubMed

28.

Miyajima F, Roberts P, Swale A, Price V, Jones M, Horan M, et al. Characterisation and carriage ratio of Clostridium difficile strains isolated from a community-dwelling elderly population in the United Kingdom. PLoS ONE. 2011;6, e22804.PubMedCentralPubMed

29.

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

30.

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.PubMedCentralPubMed

31.

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

32.

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

33.

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.PubMedCentralPubMed

34.

Rousseau C, Levenez F, Fouqueray C, Dore J, Collignon A, Lepage P. Clostridium difficile colonization in early infancy is accompanied by changes in intestinal microbiota composition. J Clin Microbiol. 2011;49:858–65.PubMedCentralPubMed

35.

Belmares J, Johnson S, Parada JP, Olson MM, Clabots CR, Bettin KM, et al. Molecular epidemiology of Clostridium difficile over the course of 10 years in a tertiary care hospital. Clin Infect Dis. 2009;49:1141–7.PubMed

36.

Bender BS, Bennett R, Laughon BE, Greenough 3rd WB, Gaydos C, Sears SD, et al. Is Clostridium difficile endemic in chronic-care facilities? Lancet. 1986;2:11–3.PubMed

37.

Campbell RR, Beere D, Wilcock GK, Brown EM. Clostridium difficile in acute and long-stay elderly patients. Age Ageing. 1988;17:333–6.PubMed

38.

Bauer MP, Farid A, Bakker M, Hoek RA, Kuijper EJ, van Dissel JT. Patients with cystic fibrosis have a high carriage rate of non-toxigenic Clostridium difficile. Clin Microbiol Infect. 2014;20:1469–0691.

39.

Peach SL, Borriello SP, Gaya H, Barclay FE, Welch AR. Asymptomatic carriage of Clostridium difficile in patients with cystic fibrosis. J Clin Pathol. 1986;39:1013–8.PubMedCentralPubMed

40.

Welkon CJ, Long SS, Thompson Jr CM, Gilligan PH. Clostridium difficile in patients with cystic fibrosis. Am J Dis Child. 1985;139:805–8.PubMed

41.

Yahav J, Samra Z, Blau H, Dinari G, Chodick G, Shmuely H. Helicobacter pylori and Clostridium difficile in cystic fibrosis patients. Dig Dis Sci. 2006;51:2274–9.PubMed

42.

Pant C, Sferra TJ, Deshpande A, Olyaee M, Gilroy R, Anderson MP, et al. Clostridium difficile infection in hospitalized patients with cystic fibrosis. Infect Control Hosp Epidemiol. 2014;35:1547–8.PubMed

43.

Dumford 3rd DM, Nerandzic M, Chang S, Richmond MA, Donskey C. Epidemiology of Clostridium difficile and vancomycin-resistant Enterococcus colonization in patients on a spinal cord injury unit. J Spinal Cord Med. 2011;34:22–7.PubMedCentralPubMed

44.

Stevens V, Dumyati G, Fine LS, Fisher SG, van Wijngaarden E. Cumulative Antibiotic Exposures Over Time and the Risk of Clostridium difficile Infection. Clin Infect Dis. 2011;53:42–8.PubMed

45.

Marciniak C, Chen D, Stein AC, Semik PE. Prevalence of Clostridium difficile colonization at admission to rehabilitation. Arch Phys Med Rehabil. 2006;87:1086–90.PubMed

46.

Gerding DN, Muto CA, Owens Jr RC. Measures to control and prevent Clostridium difficile infection. Clin Infect Dis. 2008;46:S43–9.PubMed

47.

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;51:2883–7.PubMedCentralPubMed

48.

Sarker MR, Paredes-Sabja D. Molecular basis of early stages of Clostridium difficile infection: germination and colonization. Future Microbiol. 2012;7:933–43.PubMed

49.

Testore GP, Nardi F, Babudieri S, Giuliano M, Di Rosa R, Panichi G. Isolation of Clostridium difficile from human jejunum: identification of a reservoir for disease? J Clin Pathol. 1986;39:861–2.PubMedCentralPubMed

50.

Spigaglia P, Barketi-Klai A, Collignon A, Mastrantonio P, Barbanti F, Rupnik M, et al. Surface-layer (S-layer) of human and animal Clostridium difficile strains and their behaviour in adherence to epithelial cells and intestinal colonization. J Med Microbiol. 2013;62:1386–93.PubMed

51.

Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature. 2015;517:205–8.PubMedCentralPubMed

52.

Rea MC, O’Sullivan O, Shanahan F, O’Toole PW, Stanton C, Ross RP, et al. Clostridium difficile carriage in elderly subjects and associated changes in the intestinal microbiota. J Clin Microbiol. 2012;50:867–75.PubMedCentralPubMed

53.

Vincent C, Stephens DA, Loo VG, Edens TJ, Behr MA, Dewar K, et al. Reductions in intestinal Clostridiales precede the development of nosocomial Clostridium difficile infection. Microbiome. 2013;1:2049–618.

54.

Britton RA, Young VB. Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol. 2012;20:313–9.PubMedCentralPubMed

55.

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.PubMed

56.

Brouwer MSM, 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;4:42601.

57.

Ishida Y, Maegawa T, Kondo T, Kimura A, Iwakura Y, Nakamura S, et al. Essential involvement of IFN-gamma in Clostridium difficile toxin A-induced enteritis. J Immunol. 2004;172:3018–25.PubMed

58.

Meyer GK, Neetz A, Brandes G, Tsikas D, Butterfield JH, Just I, et al. Clostridium difficile toxins A and B directly stimulate human mast cells. Infect Immun. 2007;75:3868–76.PubMedCentralPubMed

59.

Carroll KC, Bartlett JG. Biology of Clostridium difficile: implications for epidemiology and diagnosis. Annu Rev Microbiol. 2011;65:501–21.PubMed

60.

Lyerly DM, Saum KE, MacDonald DK, Wilkins TD. Effects of Clostridium difficile toxins given intragastrically to animals. Infect Immun. 1985;47:349–52.PubMedCentralPubMed

61.

Komatsu M, Kato H, Aihara M, Shimakawa K, Iwasaki M, Nagasaka Y, et al. High frequency of antibiotic-associated diarrhea due to toxin A-negative, toxin B-positive Clostridium difficile in a hospital in Japan and risk factors for infection. Eur J Clin Microbiol Infect Dis. 2003;22:525–9.PubMed

62.

Drudy D, Fanning S, Kyne L. Toxin A-negative, toxin B-positive Clostridium difficile. Int J Infect Dis. 2007;11:5–10.PubMed

63.

Steele J, Mukherjee J, Parry N, Tzipori S. Antibody Against TcdB, but Not TcdA, Prevents Development of Gastrointestinal and Systemic Clostridium difficile Disease. J Infect Dis. 2013;207:323–30.PubMedCentralPubMed

64.

Lyras D, O’Connor JR, Howarth PM, Sambol SP, Carter GP, Phumoonna T, et al. Toxin B is essential for virulence of Clostridium difficile. Nature. 2009;458:1176–9.PubMedCentralPubMed

65.

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

66.

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

67.

Simor AE, Yake SL, Tsimidis K. Infection due to Clostridium difficile among elderly residents of a long-term-care facility. Clin Infect Dis. 1993;17:672–8.PubMed

68.

Corrado OJ, Mascie-Taylor BH, Hall MJ, Bolton RP. Prevalence of Clostridium difficile on a mixed-function ward for the elderly. J Infect. 1990;21:287–92.PubMed

69.

Cefai C, Elliott TS, Woodhouse KW. Gastrointestinal carriage rate of Clostridium difficile in elderly, chronic care hospital patients. J Hosp Infect. 1988;11:335–9.PubMed

70.

Ryan J, Murphy C, Twomey C, Paul Ross R, Rea MC, MacSharry J, et al. Asymptomatic carriage of Clostridium difficile in an Irish continuing care institution for the elderly: prevalence and characteristics. Ir J Med Sci. 2010;179:245–50.PubMed

71.

Zidaric V, Kevorkijan BK, Oresic N, Janezic S, Rupnik M. Comparison of two commercial molecular tests for the detection of Clostridium difficile in the routine diagnostic laboratory. J Med Microbiol. 2011;60:1131–6.PubMed

72.

Johnson S, Homann SR, Bettin KM, Quick JN, Clabots CR, Peterson LR, 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.PubMed

73.

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

74.

Kim KH, Fekety R, Batts DH, Brown D, Cudmore M, Silva Jr J, et al. Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated colitis. J Infect Dis. 1981;143:42–50.PubMed

75.

Curry SR, Muto CA, Schlackman JL, Pasculle AW, Shutt KA, Marsh JW, et al. 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.PubMedCentralPubMed

76.

Malamou-Ladas H, O’Farrell S, Nash JQ, Tabaqchali S. Isolation of Clostridium difficile from patients and the environment of hospital wards. J Clin Pathol. 1983;36:88–92.PubMedCentralPubMed

77.

Savage AM, Alford RH. Nosocomial spread of Clostridium difficile. Infect Control. 1983;4:31–3.PubMed

78.

Barbut F, Petit JC. Epidemiology of Clostridium difficile-associated infections. Clin Microbiol Infect. 2001;7:405–10.PubMed

79.

Clabots CR, Johnson S, Olson MM, Peterson LR, Gerding DN. Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis. 1992;166:561–7.PubMed

80.

Jinno S, Kundrapu S, Guerrero DM, Jury LA, Nerandzic MM, Donskey CJ. Potential for transmission of Clostridium difficile by asymptomatic acute care patients and long-term care facility residents with prior C. difficile infection. Infect Control Hosp Epidemiol. 2012;33:638–9.PubMed

81.

Sethi AK, Al-Nassir WN, Nerandzic MM, Bobulsky GS, Donskey CJ. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol. 2010;31:21–7.PubMed

82.

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;100:32–40.PubMed

83.

Wilcox MH, Fawley WN, Wigglesworth N, Parnell P, Verity P, Freeman J. Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection. J Hosp Infect. 2003;54:109–14.PubMed

84.

Boyce JM, Havill NL, Otter JA, McDonald LC, Adams NM, Cooper T, et al. Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting. Infect Control Hosp Epidemiol. 2008;29:723–9.PubMed

85.

Nerandzic MM, Cadnum JL, Pultz MJ, Donskey CJ. Evaluation of an automated ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens in hospital rooms. BMC Infect Dis. 2010;10:1471–2334.

86.

Lanzas C, Dubberke ER, Lu Z, Reske KA, Grohn YT. Epidemiological model for Clostridium difficile transmission in healthcare settings. Infect Control Hosp Epidemiol. 2011;32:553–61.PubMedCentralPubMed

87.

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;9:7.

88.

Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A, O’Connor L, et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med. 2013;369:1195–205.PubMed

89.

Yakob L, Riley TV, Paterson DL, Clements AC. Clostridium difficile exposure as an insidious source of infection in healthcare settings: an epidemiological model. BMC Infect Dis. 2013;13:376.PubMedCentralPubMed

90.

Kong LY, Dendukuri N, Schiller I, Bourgault AM, Brassard P, Poirier L, et al. Predictors of asymptomatic Clostridium difficile colonization on hospital admission. Am J Infect Control. 2015;43:248–53.PubMed

91.

Leekha S, Aronhalt KC, Sloan LM, Patel R, Orenstein R. Asymptomatic Clostridium difficile colonization in a tertiary care hospital: Admission prevalence and risk factors. Am J Infect Control. 2013;41:390–3.PubMed

92.

Gerding DN, Olson MM, Johnson S, Peterson LR, Lee Jr JT. Clostridium difficile diarrhea and colonization after treatment with abdominal infection regimens containing clindamycin or metronidazole. Am J Surg. 1990;159:212–7.PubMed

93.

Nakamura S, Mikawa M, Nakashio S, Takabatake M, Okado I, Yamakawa K, et al. Isolation of Clostridium difficile from the feces and the antibody in sera of young and elderly adults. Microbiol Immunol. 1981;25:345–51.PubMed

94.

Morris Jr JG, Jarvis WR, Nunez-Montiel OL, Towns ML, Thompson FS, Dowell VR, et al. Clostridium difficile Colonization and toxin production in a cohort of patients with malignant hematologic disorders. Arch Intern Med. 1984;144:967–9.PubMed

95.

Clayton EM, Rea MC, Shanahan F, Quigley EM, Kiely B, Hill C, et al. 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

96.

Kyne L, Warny M, Qamar A, Kelly CP. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet. 2001;357:189–93.PubMed

97.

Sanchez-Hurtado K, Corretge M, Mutlu E, McIlhagger R, Starr JM, Poxton IR. Systemic antibody response to Clostridium difficile in colonized patients with and without symptoms and matched controls. J Med Microbiol. 2008;57:717–24.PubMed

98.

Kelly CP. Immune response to Clostridium difficile infection. Eur J Gastroenterol Hepatol. 1996;8:1048–53.PubMed

99.

Kelly CP, Kyne L. The host immune response to Clostridium difficile. J Med Microbiol. 2011;60:1070–9.PubMed

100.

Warny M, Vaerman JP, Avesani V, Delmee M. Human antibody response to Clostridium difficile toxin A in relation to clinical course of infection. Infect Immun. 1994;62:384–9.PubMedCentralPubMed

101.

Warren CA, Li Y, Calabrese GM, Freire RS, Zaja-Milatovic S, van Opstal E, et al. Contribution of adenosine A(2B) receptors in Clostridium difficile intoxication and infection. Infect Immun. 2012;80:4463–73.PubMedCentralPubMed

102.

Sambol SP, Merrigan MM, Tang JK, Johnson S, Gerding DN. Colonization for the prevention of Clostridium difficile disease in hamsters. J Infect Dis. 2002;186:1781–9.PubMed

103.

Yakob L, Riley TV, Paterson DL, Marquess J, Magalhaes RJ, Furuya-Kanamori L, et al. Mechanisms of hypervirulent Clostridium difficile ribotype 027 displacement of endemic strains: an epidemiological model. Sci Rep. 2015;5:12666.PubMedCentralPubMed

104.

Burdon DW. Clostridium difficile: the epidemiology and prevention of hospital-acquired infection. Infection. 1982;10:203–4.PubMed

105.

Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN. Nosocomial Clostridium difficile colonisation and disease. Lancet. 1990;336:97–100.PubMed

106.

Guerrero DM, Becker JC, Eckstein EC, Kundrapu S, Deshpande A, Sethi AK, et al. Asymptomatic carriage of toxigenic Clostridium difficile by hospitalized patients. J Hosp Infect. 2013;85:155–8.PubMed

107.

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

108.

Yakob L, Riley TV, Paterson DL, Marquess J, Clements ACA. Assessing control bundles for Clostridium difficile: a review and mathematical model. Emerg Microbes Infect. 2014;3:e43.PubMedCentralPubMed

109.

Hung YP, Tsai PJ, Hung KH, Liu HC, Lee CI, Lin HJ, et al. Impact of Toxigenic Clostridium difficile Colonization and Infection among Hospitalized Adults at a District Hospital in Southern Taiwan. PLoS ONE. 2012;7, e42415.PubMedCentralPubMed

110.

Al-Jumaili IJ, Shibley M, Lishman AH, Record CO. Incidence and origin of Clostridium difficile in neonates. J Clin Microbiol. 1984;19:77–8.PubMedCentralPubMed

111.

Jangi S, Lamont JT. Asymptomatic colonization by Clostridium difficile in infants: implications for disease in later life. J Pediatr Gastroenterol Nutr. 2010;51:2–7.PubMed

112.

Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–21.PubMed

113.

Stark PL, Lee A, Parsonage BD. Colonization of the large bowel by Clostridium difficile in healthy infants: quantitative study. Infect Immun. 1982;35:895–9.PubMedCentralPubMed

114.

Rudensky B, Rosner S, Sonnenblick M, van Dijk Y, Shapira E, Isaacsohn M. The prevalence and nosocomial acquisition of Clostridium difficile in elderly hospitalized patients. Postgrad Med J. 1993;69:45–7.PubMedCentralPubMed

115.

Rivera EV, Woods S. Prevalence of asymptomatic Clostridium difficile colonization in a nursing home population: A cross-sectional study. J Gend Specif Med. 2003;6:27–30.PubMed

116.

Fulton JD, Fallon RJ. Is Clostridium difficile endemic in chronic-care facilities? Lancet. 1987;2:393–4.PubMed

117.

Schoevaerdts D, Swine C, Verroken A, Huang TD, Glupczynski Y. Asymptomatic colonization by Clostridium difficile in older adults admitted to a geriatric unit: a prospective cohort study. J Am Geriatr Soc. 2011;59:2179–81.PubMed

118.

McCoubrey J, Starr J, Martin H, Poxton IR. Clostridium difficile in a geriatric unit: a prospective epidemiological study employing a novel S-layer typing method. J Med Microbiol. 2003;52:573–8.PubMed

119.

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;162:678–84.PubMed

120.

Heard SR, O’Farrell S, Holland D, Crook S, Barnett MJ, Tabaqchali S. The epidemiology of Clostridium difficile with use of a typing scheme: nosocomial acquisition and cross-infection among immunocompromised patients. J Infect Dis. 1986;153:159–62.PubMed

121.

Barbut F, Corthier G, Charpak Y, Cerf M, Monteil H, Fosse T, et al. Prevalence and pathogenicity of Clostridium difficile in hospitalized patients. A French multicenter study. Arch Intern Med. 1996;156:1449–54.PubMed

122.

Mainardi JL, Lacassin F, Guilloy Y, Goldstein FW, Leport C, Acar JF, et al. Low rate of Clostridium difficile colonization in ambulatory and hospitalized HIV-infected patients in a hospital unit: a prospective survey. J Infect. 1998;37:108–11.PubMed

123.

Hell M, Sickau K, Chmelizek G, Kern JM, Maass M, Huhulescu S, et al. Absence of Clostridium difficile in asymptomatic hospital staff. Am J Infect Control. 2012;40(10):1023–4.PubMed

124.

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.PubMedCentralPubMed

125.

Rotimi VO, Jamal WY, Mokaddas EM, Brazier JS, Johny M, Duerden BI. Prevalent PCR ribotypes of clinical and environmental strains of Clostridium difficile isolated from intensive-therapy unit patients in Kuwait. J Med Microbiol. 2003;52:705–9.PubMed

Title: Asymptomatic Clostridium difficile colonization: epidemiology and clinical implications
Authors: Luis Furuya-Kanamori
John Marquess
Laith Yakob
Thomas V. Riley
David L. Paterson
Niki F. Foster
Charlotte A. Huber
Archie C. A. Clements
Publication date: 01-12-2015
Publisher: BioMed Central
Published in: BMC Infectious Diseases / Issue 1/2015
Electronic ISSN: 1471-2334
DOI: https://doi.org/10.1186/s12879-015-1258-4

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