Impact of Reduced Fluoroquinolone Use on Clostridioides difficile Infections Resulting From the Fluoroquinolone-Resistant Ribotype 027 Strain in a Veterans Affairs Medical Center

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Sarah N. Redmond
Sandra Y. Silva
Brigid M. Wilson
Jennifer L. Cadnum
Curtis J. Donskey

Abstract

Background: Fluoroquinolone restriction has been proposed as a control measure for Clostridioides difficile infection (CDI) outbreaks associated with fluoroquinolone-resistant ribotype 027 strains. However, relatively few reports of fluoroquinolone restriction interventions have evaluated the impact on C. difficile strain types and fluoroquinolone resistance.

Methods: In a hospital and affiliated long-term care facility (LTCF), antimicrobial stewardship and environmental cleaning interventions were implemented between 2009 and 2018, and C. difficile isolates during this period (~20 per year) were ribotyped and tested for fluoroquinolone resistance by moxifloxacin minimum inhibitory concentrations (MICs). Pearson’s correlation coefficient was used to assess the association between use of fluoroquinolones and the percentage of CDI cases due to the 027 strain over time.

Results: Between 2009 and 2018, prescribing of fluoroquinolones to inpatients decreased by 43%, coinciding with significant reductions in the healthcare-associated CDI rates in the hospital and LTCF and a decline in the percentage of C. difficile isolates that were ribotype 027 from 70% to 10%. Ninety-five percent of ribotype 027 and 6% of non-027 isolates were moxifloxacin resistant. Hospital fluoroquinolone use was strongly correlated with the incidence of hospital-associated CDI (r = 0.79, 95% confidence interval, 0.31-0.95), but LTCF fluoroquinolone use was not correlated with LTCF-associated CDI (r = 0.29, 95% confidence interval, -0.43-0.77). During the study period, there were statistically significant downward trends in the use of penicillins, intravenous vancomycin, carbapenems, and clindamycin.

Conclusion: Our results provide support for fluoroquinolone restriction as a control measure for CDI outbreaks due to fluoroquinolone-resistant 027 strains, but also highlight the need for randomized trials as factors such as reduction in other antibiotic classes and improved cleaning may also impact CDI rates.

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References

1. McDonald LC, Killgore GE, Thompson A, Owens RC, Jr., Kazakova SV, Sambol SP, Johnson S, Gerding DN. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med. 2005;353(23):2433-41. PubMed PMID: 16322603. doi: 10.1056/NEJMoa05159

2. Wieczorkiewicz JT, Lopansri BK, Cheknis A, Osmolski JR, Hecht DW, Gerding DN, Johnson S. Fluoroquinolone and Macrolide Exposure Predict Clostridium difficile Infection with the Highly Fluoroquinolone- and Macrolide-Resistant Epidemic C. difficile Strain BI/NAP1/027. Antimicrob Agents Chemother. 2016;60(1):418-23. PubMed PMID: 26525793. Pubmed Central PMCID: 4704185. doi: 10.1128/AAC.01820-15

3. Donskey CJ. Fluoroquinolone restriction to control fluoroquinolone-resistant Clostridium difficile. Lancet Infect Dis. 2017;17(4):353-4. PubMed PMID: 28130062. doi: 10.1016/S1473-3099(17)30052-X

4. Dingle KE, Didelot X, Quan TP, Eyre DW, Stoesser N, Golubchik T, Harding RM, Wilson DJ, Griffiths D, Vaughan A, Finney JM, Wyllie DH, Oakley SJ, Fawley WN, Freeman J, Morris K, Martin J, Howard P, Gorbach S, Goldstein EJC, Citron DM, Hopkins S, Hope R, Johnson AP, Wilcox MH, Peto TEA, Walker AS, Crook DW, Modernising Medical Microbiology Informatics G. Effects of control interventions on Clostridium difficile infection in England: an observational study. Lancet Infect Dis. 2017;17(4):411-21. PubMed PMID: 28130063. Pubmed Central PMCID: 5368411. doi: 10.1016/S1473-3099(16)30514-X

5. Hecker MT, Son AH, Murphy NN, Sethi AK, Wilson BM, Watkins RR, Donskey CJ. Impact of syndrome-specific antimicrobial stewardship interventions on use of and resistance to fluoroquinolones: An interrupted time series analysis. Am J Infect Control. 2019;47(8):869-75. PubMed PMID: 30850252. doi: 10.1016/j.ajic.2019.01.026

6. Jump RL, Olds DM, Seifi N, Kypriotakis G, Jury LA, Peron EP, Hirsch AA, Drawz PE, Watts B, Bonomo RA, Donskey CJ. Effective antimicrobial stewardship in a long-term care facility through an infectious disease consultation service: keeping a LID on antibiotic use. Infect Control Hosp Epidemiol. 2012;33(12):1185-92. PubMed PMID: 23143354. Pubmed Central PMCID: 4370223. doi: 10.1086/668429

7. Sitzlar B, Deshpande A, Fertelli D, Kundrapu S, Sethi AK, Donskey CJ. An environmental disinfection odyssey: evaluation of sequential interventions to improve disinfection of Clostridium difficile isolation rooms. Infect Control Hosp Epidemiol. 2013;34(5):459-65. PubMed PMID: 23571361. doi: 10.1086/670217

8. Giancola SE, Williams RJ, 2nd, Gentry CA. Prevalence of the Clostridium difficile BI/NAP1/027 strain across the United States Veterans Health Administration. Clin Microbiol Infect. 2018;24(8):877-81. PubMed PMID: 29174729. doi: 10.1016/j.cmi.2017.11.011

9. Kelly AA, Jones MM, Echevarria KL, Kralovic SM, Samore MH, Goetz MB, Madaras-Kelly KJ, Simbartl LA, Morreale AP, Neuhauser MM, Roselle GA. A Report of the Efforts of the Veterans Health Administration National Antimicrobial Stewardship Initiative. Infect Control Hosp Epidemiol. 2017;38(5):513-20. PubMed PMID: 28118861. doi: 10.1017/ice.2016.328

10. FDA Drug Safety Communication: FDA updates warnings for oral and injectable fluoroquinolone antibiotics due to disabling side effects. Food and Drug Administration website. https://www.fda.gov/downloads/Drugs/ DrugSafety/UCM513019.pdf. Published 2016. Accessed September 19, 2019.

11. Dumford D, 3rd, Suwantarat N, Bhasker V, Kundrapu S, Zabarsky TF, Drawz P, Zhu H, Donskey CJ. Outbreak of fluoroquinolone-resistant Escherichia coli infections after transrectal ultrasound-guided biopsy of the prostate. Infect Control Hosp Epidemiol. 2013;34(3):269-73. PubMed PMID: 23388361. doi: 10.1086/669512

12. Suwantarat N, Dumford DM, 3rd, Ponce-Terashima R, Kundrapu S, Zabarsky TF, Zhu H, Donskey CJ. Modification of antimicrobial prophylaxis based on rectal culture results to prevent fluoroquinolone-resistant Escherichia coli infections after prostate biopsy. Infect Control Hosp Epidemiol. 2013;34(9):973-6. PubMed PMID: 23917913. doi: 10.1086/671734

13. Suwantarat N, Rudin SD, Marshall SH, Hujer AM, Perez F, Hujer KM, Domitrovic TN, Dumford DM, 3rd, Donskey CJ, Bonomo RA. Infections caused by fluoroquinolone-resistant Escherichia coli following transrectal ultrasound-guided biopsy of the prostate. J Glob Antimicrob Resist. 2014;2(2):71-6. PubMed PMID: 25024933. Pubmed Central PMCID: 4093839. doi: 10.1016/j.jgar.2013.07.003

14. Yarrington ME, Anderson DJ, Dodds Ashley E, Jones T, Davis A, Johnson M, Lokhnygina Y, Sexton DJ, Moehring RW. Impact of FDA black box warning on fluoroquinolone and alternative antibiotic use in southeastern US hospitals. Infect Control Hosp Epidemiol. 2019:1-4. PubMed PMID: 31474240. doi: 10.1017/ice.2019.247

15. Almalki ZS, Yue X, Xia Y, Wigle PR, Guo JJ. Utilization, Spending, and Price Trends for Quinolones in the US Medicaid Programs: 25 Years' Experience 1991-2015. Pharmacoecon Open. 2017;1(2):123-31. PubMed PMID: 29442334. Pubmed Central PMCID: 5691846. doi: 10.1007/s41669-016-0007-y

16. Werner NL, Hecker MT, Sethi AK, Donskey CJ. Unnecessary use of fluoroquinolone antibiotics in hospitalized patients. BMC Infect Dis. 2011;11:187. PubMed PMID: 21729289. Pubmed Central PMCID: 3145580. doi: 10.1186/1471-2334-11-187

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