Antimicrobial‐Associated Risk Factors for Clostridium difficile Infection
Abstract
Antimicrobial therapy plays a central role in the pathogenesis of Clostridium difficile infection (CDI), presumably through disruption of indigenous intestinal microflora, thereby allowing C. difficile to grow and produce toxin. Investigations involving animal models and studies performed in vitro suggest that inhibitory activity against C. difficile and differences in the propensity to stimulate toxin production may also influence the likelihood that particular drugs may cause CDI. Although nearly all antimicrobial classes have been associated with CDI, clindamycin, third-generation cephalosporins, and penicillins have traditionally been considered to harbor the greatest risk. Recent studies have also implicated fluoroquinolones as high-risk agents, a finding that is most likely to be related in part to increasing fluoroquinolone resistance among epidemic strains (i.e., restriction-endonuclease analysis group BI/North American PFGE type 1 strains) and some nonepidemic strains of C. difficile. Restrictions in the use of clindamycin and third-generation cephalosporins have been associated with reductions in CDI. Because use of any antimicrobial has the potential to induce the onset of CDI and disease caused by other health care-associated pathogens, antimicrobial stewardship programs that promote judicious use of antimicrobials are encouraged in concert with environmental and infection control-related efforts.
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Susceptibility to CDI is predominantly driven by antibiotic-induced perturbations to the intestinal microbiota resulting in a loss of colonization resistance.
“Susceptibility to CDI is predominantly driven by antibiotic-induced perturbations to the intestinal microbiota resulting in a loss of colonization resistance”
From Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut (2023) · cites this paper as [23]
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Shaughnessy, M. K., Micielli, R., DePestel, D. D., Arndt, J. L., Strachan, C. L., Welch, K. B., & Chenoweth, C. (2011) · Infection Control and Hospital Epidemiology · doi:10.1086/658669 · Cited by 308 · see citing works
“Prolonged use as well as use of multiple antibiotics conveys increased risk, although infection can occur after a single preoperative dose of antibiotics.(14) Additional medications that have been implicated in increased CDI risk include antimotility agents, chemotherapies, laxatives, proton pump inhibitors, and H2 bl…”
BackgroundInteractions Between the Gastrointestinal Microbiome and Clostridium difficile
Theriot, C. M., & Young, V. B. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104115 · Cited by 301 · see citing works
“Many other antibiotics were subsequently demonstrated to predispose to CDI, with the highest risk associated with clindamycin, cephalosporin, penicillin, and fluoroquinolones (41, 90).”
BackgroundImpact of Reported Beta-Lactam Allergy on Inpatient Outcomes: A Multicenter Prospective Cohort Study
MacFadden, D. R., Delfa, A. L., Leen, J., Gold, W. L., Daneman, N., Weber, E., Al-Busaidi, I. S., Petrescu, D., Saltzman, I., Devlin, M. K., et al. (2016) · Clinical Infectious Diseases · doi:10.1093/cid/ciw462 · Cited by 297 · see citing works
Probiotics for the prevention of pediatric antibiotic-associated diarrhea
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“In particular, antibiotics such as aminopenicillins, cephalosporins and clindamycin that act on anaerobes are most commonly associated with diarrhea (Wistrom 2001; Owens 2008; McFarland 2008).”
BackgroundProbiotics for the prevention of pediatric antibiotic-associated diarrhea
Johnston, B. C., Goldenberg, J. Z., Vandvik, P. O., Sun, X., & Guyatt, G. H. (2011) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004827.pub3 · Cited by 258 · see citing works
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Practical Guidance for Clinical Microbiology Laboratories: Diagnosis of Bacterial Gastroenteritis
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Commensal bacteria mediated defenses against pathogens
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The role of the intestinal microbiota in enteric infection
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Historical Perspectives on Studies ofClostridium difficileandC. difficileInfection
Bartlett, J. G. (2008) · Clinical Infectious Diseases · doi:10.1086/521865 · Cited by 189 · see citing works
Foley, M. H., Walker, M. E., Stewart, A. K., O’Flaherty, S., Gentry, E. C., Patel, S., Beaty, V. V., Allen, G., Pan, M., Simpson, J. B., et al. (2023) · Nature Microbiology · doi:10.1038/s41564-023-01337-7 · Cited by 181 · see citing works
Epidemiology and Risk Factors for Clostridium difficile Infection in Children
Sandora, T. J., Fung, M., Flaherty, K. R., Helsing, L., Scanlon, P., Potter-Bynoe, G., Gidengil, C. A., & Lee, G. M. (2011) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0b013e31820bfb29 · Cited by 169 · see citing works
“difficile to flourish.(31) We found recent antibiotic exposure to be a risk factor for CDI in children.”
BackgroundAntimicrobial resistance in Clostridium difficile
Huang, H., Weintraub, A., Fang, H., & Nord, C. E. (2009) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2009.09.012 · Cited by 166 · see citing works
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Association of Gastric Acid Suppression With Recurrent Clostridium difficile Infection
Tariq, R., Singh, S., Gupta, A., Pardi, D. S., & Khanna, S. (2017) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2017.0212 · Cited by 160 · see citing works
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“of hospitalization days in previous 6 mo 0–30 89 (63) 46 (64) 11 (65) 31–60 36 (26) 20 (28) 6 (36) 61–183 16 (11) 6 (8) 0”
BackgroundClinical and economic outcomes of a prospective antimicrobial stewardship program
Nowak, M. A., Nelson, R. E., Breidenbach, J. L., Thompson, P. A., & Carson, P. J. (2012) · American Journal of Health-System Pharmacy · doi:10.2146/ajhp110603 · Cited by 145 · see citing works
“difficile and MRSA infections with increased use of quinolones.(46,47) In our study, quinolone use was not a particular target of the ASP but did fall substantially in the postimplementation period.”
BackgroundSeekatz, A. M., Theriot, C. M., Molloy, C. T., Wozniak, K. L., Bergin, I. L., & Young, V. B. (2015) · Infection and Immunity · doi:10.1128/iai.00459-15 · Cited by 145 · see citing works
“Although it is clear that antibiotic use is correlated with the majority of CDI cases (9), the standard therapy for CDI is the administration of an antibiotic regimen with activity against C.”
BackgroundA Gram-negative-selective antibiotic that spares the gut microbiome
Muñoz, K. A., Ulrich, R. J., Vasan, A. K., Sinclair, M., Wen, P., Holmes, J. R., Lee, H. Y., Hung, C., Fields, C. J., Tajkhorshid, E., et al. (2024) · Nature · doi:10.1038/s41586-024-07502-0 · Cited by 142 · see citing works
Unnecessary use of fluoroquinolone antibiotics in hospitalized patients
Werner, N. L., Hecker, M. T., Sethi, A. K., & Donskey, C. J. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-187 · Cited by 137 · see citing works
“In addition, fluoroquinolone exposure has been 51 associated with colonization and infection with other healthcare-associated pathogens, including 52 methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), 53 and Clostridium difficile [3-5].”
BackgroundSelf-citationGuo, B., Harstall, C., Louie, T., van Zanten, S. V., & Dieleman, L. A. (2012) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2012.05033.x · Cited by 134 · see citing works
Risk Factors and Outcomes Associated With Severe Clostridium difficile Infection in Children
Kim, J., Shaklee, J., Smathers, S. A., Prasad, P. A., Asti, L., Zoltanski, J., Dul, M. J., Nerandzic, M. M., Coffin, S. E., Toltzis, P., et al. (2011) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0b013e3182352e2c · Cited by 132 · see citing works
“Conclusions: Increasing age and exposure to multiple antibiotic classes were risk factors for severe CDI.”
BackgroundInfluentialPathogenicity and virulence of Clostridioides difficile
Buddle, J. E., & Fagan, R. P. (2022) · Virulence · doi:10.1080/21505594.2022.2150452 · Cited by 133 · see citing works
“itself can also contribute to CDI, by exacerbating dysbiosis and leaving the patient acutely sensitive to reinfection or relapse [8].”
Clostridium difficileInfection: A Comprehensive Review
Kachrimanidou, M., & Malisiovas, N. (2011) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2011.556598 · Cited by 129 · see citing works
“Increased duration of antibiotic use and use of multiple antimicrobial agents are also associated with increased risk of CDI (Owens et al., 2008).”
BackgroundHospital Ward Antibiotic Prescribing and the Risks of Clostridium difficile Infection
Brown, K. A., Valenta, K., Fisman, D. N., Simor, A. E., & Daneman, N. (2015) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2014.8273 · Cited by 129 · see citing works
Expression of recombinant Clostridium difficile toxin A and B in Bacillus megaterium
Yang, G., Zhou, B., Wang, J., He, X., Sun, X., Nie, W., Tzipori, S. R., & Feng, H. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-192 · Cited by 129 · see citing works
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Clostridium difficile Infection in Children
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Safety Profile of the Respiratory Fluoroquinolone Moxifloxacin
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Self-citationAntibiotic Utilization for Acute Respiratory Tract Infections in U.S. Emergency Departments
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“In addition, antibiotic use and the risk of Clostridium difficile infection have become important concerns (5, 6).”
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Antimicrobial Stewardship Programs: How to Start and Steer a Successful Program
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Covering more territory to fight resistance: considering nurses’ role in antimicrobial stewardship
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“Furthermore, HCAIs caused by resistant organisms are associated with increased morbidity and mortality, and a longer hospital stay compared with infections caused by more sensitive organisms ( Cosgrove, 2006 ; Owens et al, 2008 ).”
BackgroundRole of the Pharmacist in Antimicrobial Stewardship
Parente, D. M., & Morton, J. B. (2018) · Medical Clinics of North America · doi:10.1016/j.mcna.2018.05.009 · Cited by 118 · see citing works
Impact of Antibiotics on Necrotizing Enterocolitis and Antibiotic-Associated Diarrhea
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Role of nanomaterials in deactivating multiple drug resistance efflux pumps – A review
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“fluoroquinolones [22].”
Clostridium difficile Infection: Epidemiology, Pathogenesis, Risk Factors, and Therapeutic Options
Goudarzi, M., Seyedjavadi, S. S., Goudarzi, H., Aghdam, E. M., & Nazeri, S. (2014) · Scientifica · doi:10.1155/2014/916826 · Cited by 110 · see citing works
“CDI is one of the most prevalent problems in hospitals and nursing homes where patients frequently receive antibiotics [5].”
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“Clostridium difficile is a spore-forming, toxin-producing Gram-positive bacterial pathogen and is a major cause of antibiotic-associated diarrhea (1, 2).”
BackgroundAntimicrobial stewardship: a call to action for surgeons
Sartelli, M., Duane, T. M., Catena, F., Tessier, J. M., Coccolini, F., Kao, L. S., De Simone, B., Labricciosa, F. M., May, A. K., Ansaloni, L., et al. (2016) · Surgical Infections · doi:10.1089/sur.2016.187 · Cited by 107 · see citing works
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“Receipt of cephalosporins has been reported to be a risk factor for CDI in allogeneic transplants (17).”
BackgroundHumanClostridium difficileinfection: inhibition of NHE3 and microbiota profile
Engevik, M. A., Engevik, K. A., Yacyshyn, M. B., Wang, J., Hassett, D. J., Darien, B. J., Yacyshyn, B., & Worrell, R. T. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00090.2014 · Cited by 104 · see citing works
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Immune responses to Clostridium difficile infection
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“difficile infection [12], and infection with C.”
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“Previously identified risk factors for Clostridium difficile infection (CDI) include admission to hospital or nursing home, old age, chronic comorbidity, longer hospital stay, antibiotic usage and prior chemotherapy [1], use of gastric acid suppressants, and nasogastric tubes.”
BackgroundO’Riordan, W. D., Cardenas, C., Shin, E., Sirbu, A., Garrity-Ryan, L. K., Das, A., Eckburg, P. B., Manley, A. L., Steenbergen, J. N., Tzanis, E. L., et al. (2019) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(19)30275-0 · Cited by 98 · see citing works
Clostridium difficileIsolates Resistant to Fluoroquinolones in Italy: Emergence of PCR Ribotype 018
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WSES guidelines for management of Clostridium difficile infection in surgical patients
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Antimicrobial Susceptibility of Clostridium Difficile Clinical Isolates in Iran
Goudarzi, M., Goudarzi, H., Alebouyeh, M., Rad, M. A., Mehr, F. S. S., Zali, M. R., & Aslani, M. M. (2013) · Iranian Red Crescent Medical Journal · doi:10.5812/ircmj.5189 · Cited by 92 · see citing works
“Therefore Antimicrobial therapy plays a central role in the development of CDI (4, 6).”
BackgroundColonization Versus Carriage of Clostridium difficile
Donskey, C. J., Kundrapu, S., & Deshpande, A. (2015) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2014.11.001 · Cited by 91 · see citing works
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“Prior treatment with antimicrobials is considered the main risk factor for CDAD, and continued antibiotic treatment has been associated with a poor clinical course of this condition (2, 9, 25, 41, 42).”
BackgroundMiller, A. C., Arakkal, A. T., Sewell, D. K., Segre, A. M., Tholany, J., Polgreen, P. M., & CDC MInD-Healthcare Group (2023) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofad413 · Cited by 89 · see citing works
Antimicrobial Stewardship and Antimicrobial Resistance
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Microbiota-based markers predictive of development of Clostridioides difficile infection
Berkell, M., Mysara, M., Xavier, B. B., van Werkhoven, C. H., Monsieurs, P., Lammens, C., Ducher, A., Vehreschild, M. J. G. T., Goossens, H., de Gunzburg, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22302-0 · Cited by 82 · see citing works
Clostridium difficile Infections: A Global Overview of Drug Sensitivity and Resistance Mechanisms
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“difficile, including metronidazole, vancomycin, and fidaxomicin [27, 28].”
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A 76-Year-Old Man With Recurrent Clostridium difficile–Associated Diarrhea
Kelly, C. P. (2009) · JAMA · doi:10.1001/jama.2009.171 · Cited by 79 · see citing works
Critchley, I. A., Green, L. S., Young, C. L., Bullard, J. M., Evans, R. J., Price, M., Jarvis, T. C., Guiles, J. W., Janjić, N., & Ochsner, U. A. (2009) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkp041 · Cited by 77 · see citing works
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“Most antimicrobial agents have been implicated in the induction of CDI, but clindamycin, third-generation cephalosporins, fluoroquinolones, and aminopenicillins are particularly noted for their propensity to induce CDI [3].”
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“Historically, clindamycin, cephalosporins, and amoxicillin were most frequently associated with CDI [5].”
BackgroundAntimicrobial Use, Human Gut Microbiota and Clostridium difficile Colonization and Infection
Vincent, C., & Manges, A. R. (2015) · Antibiotics · doi:10.3390/antibiotics4030230 · Cited by 70 · see citing works
“Although nearly all classes of antibiotics have been associated with CDI, clindamycin, penicillins, cephalosporins, and, more recently, fluoroquinolones seem to pose the greatest risk [6–8].”
BackgroundSlattery, J. M., MacFabe, D. F., & Frye, R. E. (2016) · Clinical Medicine Insights Pediatrics · doi:10.4137/cmped.s38338 · Cited by 72 · see citing works
When not to start antibiotics: avoiding antibiotic overuse in the intensive care unit
Denny, K. J., Wale, J. D., Laupland, K. B., Harris, P. N. A., & Lipman, J. (2019) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2019.07.007 · Cited by 72 · see citing works
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Dingle, T. C., Wee, S., Mulvey, G. L., Greco, A., Kitova, E. N., Sun, J., Lin, S., Klassen, J. S., Palcic, M. M., Ng, K. K.-S., et al. (2008) · Glycobiology · doi:10.1093/glycob/cwn048 · Cited by 70 · see citing works
“…whom correspondence should be addressed: Tel: 1+403-220-6885; Fax: 1-403-270-2772; e-mail: glen.armstrong@ucalgary.ca frequently in hospitalized subjects who are receiving common broad spectrum antibiotic treatment because their capacity to fight infections is diminished (Owens et al. 2008).”
Background
- Authors
- Owens, Jr., Donskey, C. J., Gaynes, R. P., Loo, V. G., & Muto, C. A.
- Affiliations
- Louis Stokes Cleveland VA Medical Center (US)
- Centers for Disease Control and Prevention (US)
- McGill University Health Centre (CA)
- UPMC Presbyterian (US)
- Venue
- Clinical Infectious Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-01-15
- Volume
- 46
- Issue
- s1
- Pages
- S19-S31
- ISSN
- 1058-4838 (ISSN-L)
- 1537-6591
- OpenAlex
- W2111990189
- Cited by
- 603
- References
- 85
- Citations by year
- 2026: 13 · 2025: 19 · 2024: 19 · 2023: 27 · 2022: 20 · 2021: 23 · 2020: 27 · 2019: 38 · 2018: 38 · 2017: 49 · 2016: 45 · 2015: 54 · 2014: 32 · 2013: 48 · 2012: 25
- FWCI
- 4.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Infectious Diseases (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
- Health Sciences › Medicine › Infectious Diseases › Infection Control in Healthcare
- Keywords
- Clostridium difficile infection, clindamycin, third-generation cephalosporins, penicillin, fluoroquinolones, fluoroquinolone resistance, toxin production, antimicrobial stewardship, nosocomial infections, infection control
- MeSH terms
- Adult, Anti-Infective Agents, Drug Therapy, Combination, Enterocolitis, Pseudomembranous, Humans, Intestines, Risk Factors, Time Factors, Clostridioides difficile, Ecosystem, Disease Management, Drug Resistance, Bacterial
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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