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Fluoroquinolone Restriction as an Effective Antimicrobial Stewardship Intervention

  • Kimberly C. Claeys
  • Teri L. Hopkins
  • Ana D. Vega
  • Emily L. Heil
Healthcare Associated Infections (G Bearman and D Morgan, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Healthcare Associated Infections

Abstract

Purpose of review

Fluoroquinolones are a commonly prescribed antibiotic class that has come under scrutiny in recent years due to mounting evidence of association between adverse drug events, C. difficile infection and isolation of antibiotic-resistant bacteria.

Recent findings

Inpatient antimicrobial stewardship (AMS) programs have a toolbox of potential interventions to curb inappropriate antibiotic use, prevent antibiotic-associated adverse drug events, and avoid unnecessary costs of care. Fluoroquinolone restriction policies in the acute care setting have demonstrated beneficial effects, including decreased rates of C. difficile infection and ESBL-producing Enterobacteriaceae. However, a simple blanket restriction policy may “squeeze the antibiotic balloon” and will likely be insufficient if not implemented in conjunction with other AMS interventions.

Summary

There is a growing body of evidence to support formulary restriction of fluoroquinolones in the acute care setting to decrease rates of C. difficile infection and development of ESBL-producing organisms. Data on how to best implement these restrictions or how to implement outside of acute care settings is limited.

Keywords

Antibiotic restriction C. difficile Extended-spectrum beta-lactamase Fluoroquinolones 

Notes

Compliance with Ethical Standards

Conflict of Interest

Kimberly C. Claeys, Teri L. Hopkins, Ana D. Vega, and Emily L. Heil declare they have no conflicts of interests.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    • Barlam TF, Cosgrove SE, Abbo LM, MacDougall C, Schuetz AN, Septimus EJ, et al. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis. 2016;62(10):e51–77. Official IDSA/SHEA guidelines for antimicrobial stewardship. CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    •• Tamma PD, Avdic E, Keenan JF, Zhao Y, Anand G, Cooper J, et al. What Is the More Effective Antibiotic Stewardship Intervention: Preprescription Authorization or Postprescription Review With Feedback? Clin Infect Dis. 2017;64(5):537–43. Study comparing the efficacy of two common stewardship approaches; preprescription authorization versus post-prescription review with feedback that showed a larger impact on decreasing antibiotic DOTs with post-prescription review with feedback. PubMedGoogle Scholar
  3. 3.
    Campbell TJ, Decloe M, Gill S, Ho G, McCready J, Powis J. Every antibiotic, every day: maximizing the impact of prospective audit and feedback on total antibiotic use. PLoS One. 2017;12(5):e0178434.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    •• Pitiriga V, Vrioni G, Saroglou G, Tsakris A. The impact of antibiotic stewardship programs in combating quinolone resistance: a systematic review and recommendations for more efficient interventions. Adv Ther. 2017;34(4):854–65. Systematic review of antibiotic stewardship programs on fluoroquinolone resistance along with expert opinion recommendations for effective interventions including a focus on diagnostic stewardship CrossRefPubMedGoogle Scholar
  5. 5.
    Fleming-Dutra KE, Hersh AL, Shapiro DJ, Bartoces M, Enns EA, File TM Jr, et al. prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. JAMA. 2016;315(17):1864–73.CrossRefPubMedGoogle Scholar
  6. 6.
    Food and Drug Administration (FDA). FDA Drug Safety Communication: FDA advises restricting fluoroquinolone antibiotic use for certain uncomplicated infections; warns about disabling side effects that can occur together. 2017; Available at: https://www.fda.gov/Drugs/DrugSafety/ucm500143.htm. Accessed 08.10.2017, 2017.
  7. 7.
    Food and Drug Administration (FDA),. The Benefits and Risks of Systemic Fluoroquinolone Antibacterial Drugs for the Treatment of Acute Bacterial Sinusitis (ABS), Acute Bacterial Exacerbation of Chronic Bronchitis in Patients Who Have Chronic Obstructive Pulmonary Disease (ABECB-COPD), and Uncomplicated Urinary Tract Infections (uUTI). 2017; Available at: https://www.fda.gov/downloads/advisorycommittees/committeesmeetingmaterials/drugs/anti-infectivedrugsadvisorycommittee/ucm467383.pdf. Accessed 09.27, 2017.
  8. 8.
    Cheng JZ, Sodhi M, Etminan M, Carleton BC. Fluoroquinolone Use and Risk of carpal tunnel syndrome: a Pharmacoepidemiologic study. Clin Infect Dis. 2017;65:684–6.CrossRefPubMedGoogle Scholar
  9. 9.
    Arabyat RM, Raisch DW, McKoy JM, Bennett CL. Fluoroquinolone-associated tendon-rupture: a summary of reports in the Food and Drug Administration's adverse event reporting system. Expert Opin Drug Saf. 2015;14(11):1653–60.CrossRefPubMedGoogle Scholar
  10. 10.
    Bidell MR, Lodise TP. Fluoroquinolone-associated tendinopathy: does levofloxacin pose the greatest risk? Pharmacotherapy. 2016 Jun;36(6):679–93.CrossRefPubMedGoogle Scholar
  11. 11.
    • Dingle KE, Didelot X, Quan TP, Eyre DW, Stoesser N, Golubchik T, et al. Effects of control interventions on Clostridium difficile infection in England: an observational study. Lancet Infect Dis. 2017;17(4):411–21. Retrospective study of prescribing data and whole-genome sequencing to demonstrate the importance of fluoroquinolone restriction as evidenced by significant declines in cases caused by fluoroquinolone-resistant isolates CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Lawes T, Lopez-Lozano JM, Nebot CA, Macartney G, Subbarao-Sharma R, Wares KD, et al. Effect of a national 4C antibiotic stewardship intervention on the clinical and molecular epidemiology of Clostridium difficile infections in a region of Scotland: a non-linear time-series analysis. Lancet Infect Dis. 2017;17(2):194–206.CrossRefPubMedGoogle Scholar
  13. 13.
    Dial S, Kezouh A, Dascal A, Barkun A, Suissa S. Patterns of antibiotic use and risk of hospital admission because of Clostridium difficile infection. CMAJ. 2008;179(8):767–72.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bignardi GE. Risk factors for Clostridium difficile infection. J Hosp Infect. 1998;40(1):1–15.CrossRefPubMedGoogle Scholar
  15. 15.
    Slimings C, Riley TV. Antibiotics and hospital-acquired Clostridium difficile infection: update of systematic review and meta-analysis. J Antimicrob Chemother. 2014;69(4):881–91.CrossRefPubMedGoogle Scholar
  16. 16.
    Tacconelli E, De Angelis G, Cataldo MA, Mantengoli E, Spanu T, Pan A, et al. Antibiotic usage and risk of colonization and infection with antibiotic-resistant bacteria: a hospital population-based study. Antimicrob Agents Chemother. 2009;53(10):4264–9.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Nseir S, Di Pompeo C, Soubrier S, Delour P, Lenci H, Roussel-Delvallez M, et al. First-generation fluoroquinolone use and subsequent emergence of multiple drug-resistant bacteria in the intensive care unit. Crit Care Med. 2005;33(2):283–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Weber SG, Gold HS, Hooper DC, Karchmer AW, Fluoroquinolones CY. The risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis. 2003;9(11):1415–22.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Parienti JJ, Cattoir V, Thibon P, Lebouvier G, Verdon R, Daubin C, et al. Hospital-wide modification of fluoroquinolone policy and meticillin-resistant Staphylococcus aureus rates: a 10-year interrupted time-series analysis. J Hosp Infect. 2011;78(2):118–22.CrossRefPubMedGoogle Scholar
  20. 20.
    Kardas-Sloma L, Boelle PY, Opatowski L, Brun-Buisson C, Guillemot D, Temime L. Impact of antibiotic exposure patterns on selection of community-associated methicillin-resistant Staphylococcus aureus in hospital settings. Antimicrob Agents Chemother. 2011;55(10):4888–95.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wu HH, Liu HY, Lin YC, Hsueh PR, Lee YJ. Correlation between levofloxacin consumption and the incidence of nosocomial infections due to fluoroquinolone-resistant Escherichia coli. J Microbiol Immunol Infect. 2016;49(3):424–9.CrossRefPubMedGoogle Scholar
  22. 22.
    Boel J, Andreasen V, Jarlov JO, Ostergaard C, Gjorup I, Boggild N, et al. Impact of antibiotic restriction on resistance levels of Escherichia coli: a controlled interrupted time series study of a hospital-wide antibiotic stewardship programme. J Antimicrob Chemother. 2016;71(7):2047–51.CrossRefPubMedGoogle Scholar
  23. 23.
    Dubberke ER, Olsen MA. Burden of Clostridium difficile on the healthcare system. Clin Infect Dis. 2012;55(Suppl 2):S88–92.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    O'Brien JA, Lahue BJ, Caro JJ, Davidson DM. The emerging infectious challenge of clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infect Control Hosp Epidemiol. 2007;28(11):1219–27.CrossRefPubMedGoogle Scholar
  25. 25.
    Song X, Bartlett JG, Speck K, Naegeli A, Carroll K, Perl TM. Rising economic impact of clostridium difficile-associated disease in adult hospitalized patient population. Infect Control Hosp Epidemiol. 2008;29(9):823–8.CrossRefPubMedGoogle Scholar
  26. 26.
    Shah DN, Aitken SL, Barragan LF, Bozorgui S, Goddu S, Navarro ME, et al. Economic burden of primary compared with recurrent Clostridium difficile infection in hospitalized patients: a prospective cohort study. J Hosp Infect. 2016;93(3):286–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Khanafer N, Vanhems P, Barbut F, Luxemburger C. CDI01 study group. Factors associated with Clostridium difficile infection: a nested case-control study in a three year prospective cohort. Anaerobe. 2017;44:117–23.CrossRefPubMedGoogle Scholar
  28. 28.
    Vincent C, Miller MA, Edens TJ, Mehrotra S, Dewar K, Manges AR. Bloom and bust: intestinal microbiota dynamics in response to hospital exposures and Clostridium difficile colonization or infection. Microbiome. 2016;4:12–016. 0156-3.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Deshpande A, Pasupuleti V, Thota P, Pant C, Rolston DD, Sferra TJ, et al. Community-associated Clostridium difficile infection and antibiotics: a meta-analysis. J Antimicrob Chemother. 2013;68(9):1951–61.CrossRefPubMedGoogle Scholar
  30. 30.
    Wieczorkiewicz JT, Lopansri BK, Cheknis A, Osmolski JR, Hecht DW, Gerding DN, et al. 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. 2015;60(1):418–23.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Dancer SJ, Kirkpatrick P, Corcoran DS, Christison F, Farmer D, Robertson C. Approaching zero: temporal effects of a restrictive antibiotic policy on hospital-acquired Clostridium difficile, extended-spectrum beta-lactamase-producing coliforms and meticillin-resistant Staphylococcus aureus. Int J Antimicrob Agents. 2013;41(2):137–42.CrossRefPubMedGoogle Scholar
  32. 32.
    Aldeyab MA, Kearney MP, Scott MG, Aldiab MA, Alahmadi YM, Darwish Elhajji FW, et al. An evaluation of the impact of antibiotic stewardship on reducing the use of high-risk antibiotics and its effect on the incidence of Clostridium difficile infection in hospital settings. J Antimicrob Chemother. 2012;67(12):2988–96.CrossRefPubMedGoogle Scholar
  33. 33.
    Fowler S, Webber A, Cooper BS, Phimister A, Price K, Carter Y, et al. Successful use of feedback to improve antibiotic prescribing and reduce Clostridium difficile infection: a controlled interrupted time series. J Antimicrob Chemother. 2007;59(5):990–5.CrossRefPubMedGoogle Scholar
  34. 34.
    •• Feazel LM, Malhotra A, Perencevich EN, Kaboli P, Diekema DJ, Schweizer ML. Effect of antibiotic stewardship programmes on Clostridium difficile incidence: a systematic review and meta-analysis. J Antimicrob Chemother. 2014;69(7):1748–54. Systematic review and meta-analysis of 16 quasi-experimental or observational studies demonstrated a significant risk reduction in C. difficile rate associated with restrictive efforts targeting cephalosporins and fluoroquinolones. CrossRefPubMedGoogle Scholar
  35. 35.
    •• Baur D, Gladstone BP, Burkert F, Carrara E, Foschi F, Dobele S, et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis. Lancet Infect Dis 2017. Systematic review and meta-analysis of 32 studies demonstrated significantly reduced incidence of infections and colonization with multi-drug resistant Gram-negative bacteria, and methicillin-resistance S. Aureus, as well as the incidence of C. Difficile infection with restriction. Google Scholar
  36. 36.
    Shea KM, Hobbs AL, Jaso TC, Bissett JD, Cruz CM, Douglass ET, et al. Effect of a healthcare-system respiratory fluoroquinolone restriction program to Alter utilization and impact rates of C. Difficile infection. Antimicrob Agents Chemother. 2017;61:e00125–17.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Wenisch JM, Equiluz-Bruck S, Fudel M, Reiter I, Schmid A, Singer E, et al. Decreasing Clostridium difficile infections by an antimicrobial stewardship program that reduces moxifloxacin use. Antimicrob Agents Chemother. 2014;58(9):5079–83.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    • Sarma JB, Marshall B, Cleeve V, Tate D, Oswald T, Woolfrey S. Effects of fluoroquinolone restriction (from 2007 to 2012) on Clostridium difficile infections: interrupted time-series analysis. J Hosp Infect. 2015;91(1):74–80. Interrupted time-series analysis that showed that fluoroquinolone use was significantly associated with incidence of CDI, which decreased in the setting of a fluoroquinolone restriction policy. CrossRefPubMedGoogle Scholar
  39. 39.
    Hunter PA, Dawson S, French GL, Goossens H, Hawkey PM, Kuijper EJ, et al. Antimicrobial-resistant pathogens in animals and man: prescribing, practices and policies. J Antimicrob Chemother. 2010;65(Suppl 1):i3–17.CrossRefPubMedGoogle Scholar
  40. 40.
    Neuhauser MM, Weinstein RA, Rydman R, Danziger LH, Karam G, Quinn JP. Antibiotic resistance among gram-negative bacilli in US intensive care units: implications for fluoroquinolone use. JAMA. 2003;289(7):885–8.CrossRefPubMedGoogle Scholar
  41. 41.
    Cook PP, Das TD, Gooch M, Catrou PG. Effect of a program to reduce hospital ciprofloxacin use on nosocomial Pseudomonas aeruginosa susceptibility to quinolones and other antimicrobial agents. Infect Control Hosp Epidemiol. 2008;29(8):716–22.CrossRefPubMedGoogle Scholar
  42. 42.
    Lafaurie M, Porcher R, Donay JL, Touratier S, Molina JM. Reduction of fluoroquinolone use is associated with a decrease in methicillin-resistant Staphylococcus aureus and fluoroquinolone-resistant Pseudomonas aeruginosa isolation rates: a 10 year study. J Antimicrob Chemother. 2012;67(4):1010–5.CrossRefPubMedGoogle Scholar
  43. 43.
    Lewis GJ, Fang X, Gooch M, Cook PP. Decreased resistance of Pseudomonas aeruginosa with restriction of ciprofloxacin in a large teaching hospital's intensive care and intermediate care units. Infect Control Hosp Epidemiol. 2012;33(4):368–73.CrossRefPubMedGoogle Scholar
  44. 44.
    Aubert G, Carricajo A, Vautrin AC, Guyomarc'h S, Fonsale N, Page D, et al. Impact of restricting fluoroquinolone prescription on bacterial resistance in an intensive care unit. J Hosp Infect. 2005;59(2):83–9.CrossRefPubMedGoogle Scholar
  45. 45.
    O'Brien KA, Zhang J, Mauldin PD, Gomez J, Hurst JM, Sean Boger M, et al. Impact of a stewardship-initiated restriction on empirical use of ciprofloxacin on Nonsusceptibility of Escherichia coli urinary isolates to ciprofloxacin. Pharmacotherapy. 2015;35(5):464–9.CrossRefPubMedGoogle Scholar
  46. 46.
    Aldeyab MA, Harbarth S, Vernaz N, Kearney MP, Scott MG, Darwish Elhajji FW, et al. The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings. Br J Clin Pharmacol. 2012;74(1):171–9.CrossRefPubMedGoogle Scholar
  47. 47.
    • Sarma JB, Marshall B, Cleeve V, Tate D, Oswald T, Woolfrey S. Effects of fluoroquinolone restriction (from 2007 to 2012) on resistance in Enterobacteriaceae: interrupted time-series analysis. J Hosp Infect. 2015;91(1):68–73. Interrupted time series analysis demonstrated a large decline in ciprofloxacin-resistant ESBL E. coli isolates in hospital and community settings during a fluoroquinolone restriction CrossRefPubMedGoogle Scholar
  48. 48.
    Shapiro DJ, Hicks LA, Pavia AT, Hersh AL. Antibiotic prescribing for adults in ambulatory care in the USA, 2007-09. J Antimicrob Chemother. 2014;69(1):234–40.CrossRefPubMedGoogle Scholar
  49. 49.
    Suda KJ, Hicks LA, Roberts RM, Hunkler RJ, Danziger LH. A national evaluation of antibiotic expenditures by healthcare setting in the United States, 2009. J Antimicrob Chemother. 2013;68(3):715–8.CrossRefPubMedGoogle Scholar
  50. 50.
    Linder JA. Antibiotic prescribing for acute respiratory infections--success that's way off the mark: comment on “a cluster randomized trial of decision support strategies for reducing antibiotic use in acute bronchitis”. JAMA Intern Med. 2013;173(4):273–5.CrossRefPubMedGoogle Scholar
  51. 51.
    Meeker D, Linder JA, Fox CR, Friedberg MW, Persell SD, Goldstein NJ, et al. Effect of behavioral interventions on inappropriate antibiotic prescribing among primary care practices: a randomized clinical trial. JAMA. 2016;315(6):562–70.CrossRefPubMedGoogle Scholar
  52. 52.
    Peterson LR. Squeezing the antibiotic balloon: the impact of antimicrobial classes on emerging resistance. Clin Microbiol Infect. 2005;11(Suppl 5):4–16.CrossRefPubMedGoogle Scholar
  53. 53.
    MELINTA THERAPEUTICS,. Melinta Therapeutics Announces U.S. FDAS Approval of Baxdela™ (Delafloxacin) for Acute Bacterial Skin And Skin Structure Infections (ABSSSI). Available at: http://melinta.com/melinta-therapeutics-announces-u-s-fda-approval-baxdela-delafloxacin-acute-bacterial-skin-skin-structure-infections-absssi/. Accessed 9.17, 2017.

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Kimberly C. Claeys
    • 1
    • 2
  • Teri L. Hopkins
    • 3
  • Ana D. Vega
    • 1
  • Emily L. Heil
    • 1
    • 2
  1. 1.Department of Pharmacy Practice and ScienceUniversity of Maryland School of PharmacyBaltimoreUSA
  2. 2.Department of PharmacyUniversity of Maryland Medical CenterBaltimoreUSA
  3. 3.Department of PharmacySouth Texas Veterans Health Care SystemSan AntonioUSA

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