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Risk factors for Clostridioides difficile colonization among hospitalized adults: A meta-analysis and systematic review

Published online by Cambridge University Press:  29 October 2020

Scott Anjewierden
Affiliation:
Cleveland Clinic Lerner College of Medicine at Case Western Reserve University, Cleveland, Ohio
Zheyi Han
Affiliation:
Cleveland Clinic Lerner College of Medicine at Case Western Reserve University, Cleveland, Ohio
Adam M. Brown
Affiliation:
University of Cincinnati College of Medicine, Cincinnati, Ohio
Curtis J. Donskey
Affiliation:
Geriatric Research Education and Clinical Center, Louis Stokes Cleveland Veterans’ Affairs Medical Center, Cleveland, Ohio
Abhishek Deshpande*
Affiliation:
Medicine Institute, Center for Value Based Care Research, Cleveland Clinic, Cleveland, Ohio Department of Infectious Diseases, Cleveland Clinic, Cleveland, Ohio
*
Author for correspondence: Abhishek Deshpande, E-mail: abhishekdp@gmail.com

Abstract

Objective:

To identify risk factors for asymptomatic Clostridioides difficile colonization among hospitalized adults utilizing a meta-analysis, which may enable early identification of colonized patients at risk of spreading C. difficile.

Design:

Meta-analysis and systematic review.

Methods:

We systematically searched MEDLINE, Scopus, Web of Science, and EMBASE from January 1, 1975, to February 15, 2020, for articles related to C. difficile colonization among hospitalized adults. Studies with multivariable analyses evaluating risk factors for asymptomatic colonization were eligible.

Results:

Among 5,506 studies identified in the search, 19 studies met the inclusion criteria. Included studies reported 20,334 adult patients of whom 1,588 were asymptomatically colonized with C. difficile. Factors associated with an increased risk of colonization were hospitalization in the previous 6 months (OR, 2.18; 95% CI, 1.86–2.56; P < .001), use of gastric acid suppression therapy within the previous 8 weeks (OR, 1.42; 95% CI, 1.17–1.73; P < .001), tube feeding (OR, 2.02; 95% CI, 1.06–3.85; P = .03), and corticosteroid use in the previous 8 weeks (OR, 1.58; 95% CI, 1.14–2.17; P = .006). Receipt of antibiotics in the previous 3 months (OR, 1.37; 95% CI, 0.94–2.01; P = .10) was not associated with statistically significant effects on risk of colonization.

Conclusions:

C. difficile colonization was significantly associated with previous hospitalization, gastric acid suppression, tube feeding, and corticosteroid use. Recognition of these risk factors may assist in identifying asymptomatic carriers of C. difficile and taking appropriate measures to reduce transmission.

Type
Original Article
Copyright
© 2020 by The Society for Healthcare Epidemiology of America. All rights reserved.

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Footnotes

a

Authors of equal contribution.

References

McDonald, LC, Gerding, DN, Johnson, S, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis 2018;66(7):e1e48.CrossRefGoogle Scholar
Magill, SS, Edwards, JR, Bamberg, W, et al. Multistate point-prevalence survey of healthcare-associated infections. N Engl J Med 2014;370:11981208.CrossRefGoogle Scholar
Loo, VG, Bourgault, A-M, Poirier, L, et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med 2011;365:16931703.CrossRefGoogle ScholarPubMed
Thomas, C, Stevenson, M, Riley, TV. Antibiotics and hospital-acquired Clostridium difficile–associated diarrhoea: a systematic review. J Antimicrob Chemother 2003;51:13391350.CrossRefGoogle ScholarPubMed
Guh, AY, Mu, Y, Winston, LG, et al. Trends in US burden of Clostridioides difficile infection and outcomes. N Engl J Med 2020;382:13201330.CrossRefGoogle Scholar
Zacharioudakis, IM, Zervou, FN, Pliakos, EE, Ziakas, PD, Mylonakis, E. Colonization with toxinogenic C. difficile upon hospital admission, and risk of infection: a systematic review and meta-analysis. Am J Gastroenterol 2015;110:381390.CrossRefGoogle Scholar
Blixt, T, Gradel, KO, Homann, C, et al. Asymptomatic carriers contribute to nosocomial Clostridium difficile infection: a cohort study of 4,508 patients. Gastroenterology 2017;152:10311041.e2.CrossRefGoogle Scholar
Curry, SR, Muto, CA, Schlackman, JL, 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;57:10941102.CrossRefGoogle ScholarPubMed
Furuya-Kanamori, L, Marquess, J, Yakob, L, et al. Asymptomatic Clostridium difficile colonization: epidemiology and clinical implications. BMC Infect Dis 2015;15:516.CrossRefGoogle ScholarPubMed
Bruns, AHW, Oosterheert, JJ, Kuijper, EJ, et al. Impact of different empirical antibiotic treatment regimens for community-acquired pneumonia on the emergence of Clostridium difficile . J Antimicrob Chemother 2010;65:24642471.CrossRefGoogle ScholarPubMed
Kong, LY, Dendukuri, N, Schiller, I, et al. Predictors of asymptomatic Clostridium difficile colonization on hospital admission. Am J Infect Control 2015;43:248253.CrossRefGoogle ScholarPubMed
Furuya-Kanamori, L, Clements, ACA, Foster, NF, et al. Asymptomatic Clostridium difficile colonization in two Australian tertiary hospitals, 2012–2014: prospective, repeated cross-sectional study. Clin Microbiol Infect 2017;23:48.e148.e7.CrossRefGoogle ScholarPubMed
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 2009;151:264269.CrossRefGoogle ScholarPubMed
Dekkers, OM, Vandenbroucke, JP, Cevallos, M, Renehan, AG, Altman, DG, Egger, M. COSMOS-E: guidance on conducting systematic reviews and meta-analyses of observational studies of etiology. PLoS Med 2019;16(2):e1002742.CrossRefGoogle ScholarPubMed
Sterne, JA, Hernán, MA, Reeves, BC, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 2016;355:i4919.CrossRefGoogle ScholarPubMed
Linsenmeyer, K, O’Brien, W, Brecher, SM, et al. Clostridium difficile screening for colonization during an outbreak setting. Clin Infect Dis 2018;67:19121914.Google ScholarPubMed
Muñoz-Price, LS, Hanson, R, Singh, S, et al. Association between environmental factors and toxigenic Clostridioides difficile carriage at hospital admission. JAMA Netw Open 2020;3(1):e1919132e1919132.CrossRefGoogle ScholarPubMed
DerSimonian, R, Laird, N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177188.CrossRefGoogle ScholarPubMed
Egger, M, Smith, GD, Schneider, M, Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629634.CrossRefGoogle ScholarPubMed
Duval, S, Tweedie, R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000;56:455463.CrossRefGoogle ScholarPubMed
Gilboa, M, Houri-Levi, E, Cohen, C, et al. Environmental shedding of toxigenic Clostridioides difficile by asymptomatic carriers: a prospective observational study. Clin Microbiol Infect 2020;26:10521057.CrossRefGoogle ScholarPubMed
Pépin, J, Saheb, N, Coulombe, M-A, 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;41:12541260.CrossRefGoogle ScholarPubMed
Deshpande, A, Pasupuleti, V, Thota, P, et al. Community-associated Clostridium difficile infection and antibiotics: a meta-analysis. J Antimicrob Chemother 2013;68:19511961.CrossRefGoogle ScholarPubMed
Theriot, CM, Young, VB. Microbial and metabolic interactions between the gastrointestinal tract and Clostridium difficile infection. Gut Microbes 2014;5:8695.CrossRefGoogle ScholarPubMed
Zhang, L, Dong, D, Jiang, C, Li, Z, Wang, X, Peng, Y. Insight into alteration of gut microbiota in Clostridium difficile infection and asymptomatic C. difficile colonization. Anaerobe 2015;34:17.CrossRefGoogle ScholarPubMed
Tariq, R, Cho, J, Kapoor, S, et al. Low risk of primary Clostridium difficile infection with tetracyclines: a systematic review and meta-analysis. Clin Infect Dis 2018;66:514522.CrossRefGoogle Scholar
Crobach, MJT, Planche, T, Eckert, C, et al. European Society of Clinical Microbiology and Infectious Diseases: update of the diagnostic guidance document for Clostridium difficile infection. Clin Microbiol Infect 2016;22 suppl 4:S63S81.CrossRefGoogle Scholar
Behar, L, Chadwick, D, Dunne, A, et al. Toxigenic Clostridium difficile colonization among hospitalised adults; risk factors and impact on survival. J Infect 2017;75:2025.CrossRefGoogle ScholarPubMed
Cui, Y, Dong, D, Zhang, L, et al. Risk factors for Clostridioides difficile infection and colonization among patients admitted to an intensive care unit in Shanghai, China. BMC Infect Dis 2019;19. doi: 10.1186/s12879-019-4603-1.CrossRefGoogle Scholar
Eyre, DW, Griffiths, D, Vaughan, A, et al. Asymptomatic Clostridium difficile colonisation and onward transmission. PLoS ONE 2013;8(11):e78445.CrossRefGoogle ScholarPubMed
Guerrero, DM, Becker, JC, Eckstein, EC, et al. Asymptomatic carriage of toxigenic Clostridium difficile by hospitalized patients. J Hosp Infect 2013;85:155158.CrossRefGoogle ScholarPubMed
Hung, Y-P, Lin, H-J, Wu, T-C, et al. Risk factors of fecal toxigenic or nontoxigenic Clostridium difficile colonization: impact of toll-like receptor polymorphisms and prior antibiotic exposure. PLoS One 2013;8(7):e69577.CrossRefGoogle ScholarPubMed
Kundrapu, S, Sunkesula, VCK, Jury, LA, et al. Do piperacillin/tazobactam and other antibiotics with inhibitory activity against Clostridium difficile reduce the risk for acquisition of C. difficile colonization? BMC Infect Dis 2016;16:159.CrossRefGoogle ScholarPubMed
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;41:390393.CrossRefGoogle Scholar
Mallia, G, Van Toen, J, Rousseau, J, et al. Examining the epidemiology and microbiology of Clostridium difficile carriage in elderly patients and residents of a healthcare facility in southern Ontario, Canada. J Hosp Infect 2018;99:461468.CrossRefGoogle ScholarPubMed
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
Meltzer, E, Smollan, G, Huppert, A, et al. Universal screening for Clostridioides difficile in a tertiary hospital: risk factors for carriage and clinical disease. Clin Microbiol Infect 2019;25:11271132.CrossRefGoogle Scholar
Nissle, K, Kopf, D, Rösler, A. Asymptomatic and yet C. difficile–toxin positive? Prevalence and risk factors of carriers of toxigenic Clostridium difficile among geriatric inpatients. BMC Geriatr 2016;16:185.CrossRefGoogle Scholar
Starr, JM, Martin, H, McCoubrey, J, Gibson, G, Poxton, IR. Risk factors for Clostridium difficile colonisation and toxin production. Age Ageing 2003;32:657660.CrossRefGoogle ScholarPubMed
Zeng, X-L, Zhang, Y-F, Tian, Q, Xue, Y, An, R-F. Effects of metformin on pregnancy outcomes in women with polycystic ovary syndrome. Medicine (Baltimore) 2016;95(36):e4526.CrossRefGoogle ScholarPubMed
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