Advances in Therapy

, Volume 34, Issue 4, pp 854–865 | Cite as

The Impact of Antibiotic Stewardship Programs in Combating Quinolone Resistance: A Systematic Review and Recommendations for More Efficient Interventions

  • Vasiliki Pitiriga
  • Georgia Vrioni
  • George Saroglou
  • Athanasios Tsakris
Review

Abstract

Quinolones are among the most commonly prescribed antibiotics worldwide. A clear relationship has been demonstrated between excessive quinolone use and the steady increase in the incidence of quinolone-resistant bacterial pathogens, both in hospital and community sites. In addition, exposure to quinolones has been associated with colonization and infection with healthcare-associated pathogens such as methicillin-resistant Staphylococcus aureus and Clostridium difficile in hospitalized patients. Therefore, the management of quinolone prescribing in hospitals through antibiotic stewardship programs is considered crucial. Although suggestions have been made by previous studies on the positive impact of stewardship programs concerning the emergence and spread of multidrug-resistant bacteria at hospital level, the association of quinolone-targeted interventions with reduction of quinolone resistance is vague. The purpose of this article was to evaluate the impact of stewardship interventions on quinolone resistance rates and healthcare-associated infections, through a literature review using systematic methods to identify and select the appropriate studies. Recommendations for improvements in quinolone-targeted stewardship programs are also proposed. Efforts in battling quinolone resistance should combine various interventions such as restriction formulary policies, prospective audits with feedback to prescribers, infection prevention and control measures, prompt detection of low-level resistance, educational programs, and guidelines for optimal quinolone usage. However, the effectiveness of such strategies should be assessed by properly designed and conducted clinical trials. Finally, novel approaches in diagnostic stewardship for rapidly detecting bacterial resistance, including PCR-based techniques, mass spectrometry, microarrays, and whole-genome sequencing as well as the prompt investigation on the clonality of quinolone-resistant strains, will strengthen our ability to personalize quinolone prescribing to individual patients.

Keywords

Antimicrobial stewardship program Feedback Infection control Infectious diseases Preauthorization Prospective audit Quinolones Resistance Restrictive policies 

References

  1. 1.
    Goossens H, Ferech M, Coenen S, Stephens P, European Surveillance of Antimicrobial Consumption Project Group. Comparison of outpatient systemic antibacterial use in 2004 in the United States and 27 European countries. Clin Infect Dis. 2007;44(8):1091–5.CrossRefPubMedGoogle Scholar
  2. 2.
    Owens RC, Ambrose PG. Antimicrobial safety: focus on fluoroquinolones. Clin Infect Dis. 2005;15(41 Suppl 2):S144–57.CrossRefGoogle Scholar
  3. 3.
    European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance surveillance in Europe 2012. http://ecdc.europa.eu/en/publications/Publications/antimicrobial-resistance-surveillance-europe-2012.pdf. Accessed 2 Dec 2014.
  4. 4.
    Weber SG, Gold HS, Hooper DC, Karchmer AW, Carmeli Y. Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis. 2003;9(11):1415–22.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Owens RA, Donskey CJ, Gaynes RP, Loo VG, Muto CA. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin Infect Dis. 2008;46:S19–31.CrossRefPubMedGoogle Scholar
  6. 6.
    Tanimoto K, Tomita H, Fujimoto S, Okuzumi K, Ike Y. Fluoroquinolones enhances the mutation frequency for meropenem-selected carbapenem resistance in Pseudomonas aeruginosa, but use of the high-potency drug doripenem inhibits mutant formation. Antimicrob Agents Chemother. 2008;52(10):3795–800.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Siegel JD, Rhinehart E, Jackson M, Chiarello L, Healthcare Infection Control Practices Advisory Committee. Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control. 2007;35(10 Suppl 2):S165–93.CrossRefPubMedGoogle Scholar
  8. 8.
    Dellit TH, Owens RC, McGowan JE, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007;44(2):159–77.CrossRefPubMedGoogle Scholar
  9. 9.
    Cook PP, Catrou PG, Christie JD, Young PD, Polk RE. Reduction in broad-spectrum antimicrobial use associated with no improvement in hospital antibiogram. J Antimicrob Chemother. 2004;53(5):853–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Charbonneau P, Parienti JJ, Thibon P, et al. Fluoroquinolone use and methicillin-resistant Staphylococcus aureus isolation rates in hospitalized patients: a quasi experimental study. Clin Infect Dis. 2006;42(6):778–84.CrossRefPubMedGoogle Scholar
  11. 11.
    Madaras-Kelly KJ, Remington RE, Lewis PG, Stevens DL. Evaluation of an intervention designed to decrease the rate of nosocomial methicillin-resistant Staphylococcus aureus infection by encouraging decreased fluoroquinolone use. Infect Control Hosp Epidemiol. 2006;27(2):155–69.CrossRefPubMedGoogle Scholar
  12. 12.
    Mutnick AH, Rhomberg PR, Sader HS, Jones RN. Antimicrobial usage and resistance trend relationships from the MYSTIC Programme in North America (1999–2001). J Antimicrob Chemother. 2004;53(2):290–6.CrossRefPubMedGoogle Scholar
  13. 13.
    Lipsitch M. The rise and fall of antimicrobial resistance. Trends Microbiol. 2001;9(9):438–44.CrossRefPubMedGoogle Scholar
  14. 14.
    Paterson DL. The role of antimicrobial management programs in optimizing antibiotic prescribing within hospitals. Clin Infect Dis. 2006;42:S90–5.CrossRefPubMedGoogle Scholar
  15. 15.
    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
  16. 16.
    Charbonneau P, Parienti JJ, Thibon P, et al. Fluoroquinolone use and methicillin-resistant Staphylococcus aureus isolation rates in hospitalized patients: a quasi experimental study. Clin Infect Dis. 2006;42(6):778–84.CrossRefPubMedGoogle Scholar
  17. 17.
    Talpaert MJ, Gopal Rao G, Cooper BS, Wade P. Impact of guidelines and enhanced antibiotic stewardship on reducing broad-spectrum antibiotic usage and its effect on incidence of Clostridium difficile infection. J Antimicrob Chemother. 2011;66(9):2168–74.CrossRefPubMedGoogle Scholar
  18. 18.
    Livermore DM. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin Infect Dis. 2002;34:634–40.CrossRefPubMedGoogle Scholar
  19. 19.
    Aubert G, Carricajo A, Vautrin AC, Guyomarch S, 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
  20. 20.
    Gruson D, Hilbert G, Vargas F, et al. Rotation and restricted use of antibiotics in a medical intensive unit. Impact on the incidence of ventilator-associated pneumonia caused by antibiotic-resistant Gram negative bacteria. Am J Respir Crit Care Med. 2000;162(3 Pt 1):837–43.CrossRefPubMedGoogle Scholar
  21. 21.
    Lee YJ, Liu HY, Lin YC, Sun KL, Chun CL, Hsueh PR. Fluoroquinolone resistance of Pseudomonas aeruginosa isolates causing nosocomial infection is correlated with levofloxacin but not ciprofloxacin use. Int J Antimicrob Agents. 2010;35(3):261–4.CrossRefPubMedGoogle Scholar
  22. 22.
    Pakyz AL, Lee JA, Ababneh MA, Harpe SE, Oinonen MJ, Polk RE. Fluoroquinolone use and fluoroquinolone-resistant Pseudomonas aeruginosa is declining in US academic medical centre hospitals. J Antimicrob Chemother. 2012;67(6):1562–4.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    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
  24. 24.
    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
  25. 25.
    Peterson LR, Postelnick M, Pozdol TL, Reisberg B, Noskin GA. Management of fluoroquinolone resistance in Pseudomonas aeruginosa—outcome of monitored use in a referral hospital. Int J Antimicrob Agents. 1998;10:207–14.CrossRefPubMedGoogle Scholar
  26. 26.
    Boel J, Andreasen V, Jarløv JO, 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
  27. 27.
    Willemsen I, Cooper B, van Buitenen C, Winters M, Andriesse G, Kluytmans J. Improving quinolone use in hospitals by using a bundle of interventions in an interrupted time series analysis. Antimicrob Agents Chemother. 2010;54(9):3763–9.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Gottesman BS, Carmeli Y, Shitrit P, Chowers M. Impact of quinolone restriction on resistance patterns of Escherichia coli isolated from urine by culture in a community setting. Clin Infect Dis. 2009;49(6):869–75.CrossRefPubMedGoogle Scholar
  29. 29.
    Sarma JB, Marshall B, Cleeve V, Tate D, Oswald T, Woolfrey S. Effects of fluoroquinolone restriction (from 2007 to 2012) on resistance in Enterobacteriaceae. J Hosp Infect. 2015;91(1):68–73.CrossRefPubMedGoogle Scholar
  30. 30.
    Troughton JA, Millar G, Smyth ET, Doherty L, McMullan R. Ciprofloxacin use and susceptibility of gram-negative organisms to quinolone and non-quinolone antibiotics. J Antimicrob Chemother. 2011;66(9):2152–8.CrossRefPubMedGoogle Scholar
  31. 31.
    Aldeyab MA, Harbarth S, Vernaz N, 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
  32. 32.
    Parienti JJ, Cattoir V, Thibon P, et al. Hospital-wide modification of fluoroquinolone policy and methicillin-resistant Staphylococcus aureus rates: a 10-year interrupted time-series analysis. J Hosp Infect. 2011;78(2):118–22.CrossRefPubMedGoogle Scholar
  33. 33.
    Liebowitz LD, Blunt MC. Modification in prescribing practices for third-generation cephalosporins and ciprofloxacin is associated with a reduction in methicillin-resistant Staphylococcus aureus bacteraemia rate. J Hosp Infect. 2008;69(4):328–36.CrossRefPubMedGoogle Scholar
  34. 34.
    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 β-lactamase-producing coliforms and methicillin-resistant Staphylococcus aureus. Int J Antimicrob Agents. 2013;41(2):137–42.CrossRefPubMedGoogle Scholar
  35. 35.
    Tedeschi S, Trapani F, Giannella M, et al. An antimicrobial stewardship program based on systematic infectious disease consultation in a rehabilitation facility. Infect Control Hosp Epidemiol. 2017;38:76–82.Google Scholar
  36. 36.
    Talpaert MJ, Gopal Rao G, Cooper BS, Wade P. Impact of guidelines and enhanced antibiotic stewardship on reducing broad-spectrum antibiotic usage and its effect on incidence of Clostridium difficile infection. J Antimicrob Chemother. 2011;66(9):2168–74.CrossRefPubMedGoogle Scholar
  37. 37.
    Wenisch JM, Equiluz-Bruck S, Fudel M, 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.
    Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol. 2010;74(3):417–33.CrossRefGoogle Scholar
  39. 39.
    Wener KM, Schechner V, Gold HS, Wright SB, Carmeli Y. Treatment with fluoroquinolones or with beta-lactam-beta-lactamase inhibitor combinations is a risk factor for isolation of extended-spectrum-beta-lactamase-producing Klebsiella species in hospitalized patients. Antimicrob Agents Chemother. 2010;54(5):2010–6.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Morosini MI, Garcia-Castillo M, Coque TM, et al. Antibiotic co-resistance in extended-spectrum-beta-lactamase-producing Enterobacteriaceae and in vitro activity of tigecycline. Antimicrob Agents Chemother. 2006;50(8):2695–9.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ruiz J, Gómez J, Navia MM, et al. High prevalence of nalidixic acid resistant, ciprofloxacin susceptible phenotype among clinical isolates of Escherichia coli and other Enterobacteriaceae. Diagn Microbiol Infect Dis. 2002;42(4):257–61.CrossRefPubMedGoogle Scholar
  42. 42.
    Masterton RG. Antibiotic heterogeneity. Int J Antimicrob Agents. 2010;36(Suppl 3):S15–8.CrossRefPubMedGoogle Scholar
  43. 43.
    Cobos-Trigueros N, Solé M, Castro P, et al. Evaluation of a mixing versus a cycling strategy of antibiotic use in critically-ill medical patients: impact on acquisition of resistant microorganisms and clinical outcomes. PLoS One. 2016;11(3):e0150274.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Sandiumenge A, Diaz E, Rodriguez A, et al. Impact of diversity of antibiotic use on the development of antimicrobial resistance. J Antimicrob Chemother. 2006;57(6):1197–204.CrossRefPubMedGoogle Scholar
  45. 45.
    Infectious Diseases Society of America. New antibiotic stewardship guidelines focus on practical advice for implementation. IDSA. 14 Apr 2016. https://www.idsociety.org/New_Antimicrobial_Stewardship_Guideline_2016. Accessed 3 Mar 2017.
  46. 46.
    van Belkum A, Dunne WM. Next-generation antimicrobial susceptibility testing. J Clin Microbiol. 2013;51:2018–24.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Agodi A, Barchitta M, Quattrocchi A, et al. Antibiotic trends of Klebsiella pneumoniae and Acinetobacter baumannii resistance indicators in an intensive care unit of Southern Italy, 2008–2013. Antimicrob Resist Infect Control. 2015;4:43.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Cohen A, Bont L, Engelhard D. A multifaceted ‘omics’ approach for addressing the challenge of antimicrobial resistance. Future Microbiol. 2015;10(3):365–76.CrossRefPubMedGoogle Scholar
  49. 49.
    Dik JWH, Poelman R, Friedrich AW, et al. An integrated stewardship model: antimicrobial, infection prevention and diagnostic (AID). Future Microbiol. 2016;11(1):93–102.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Healthcare 2017

Authors and Affiliations

  • Vasiliki Pitiriga
    • 1
  • Georgia Vrioni
    • 1
  • George Saroglou
    • 2
  • Athanasios Tsakris
    • 1
  1. 1.Department of Microbiology, Medical SchoolUniversity of AthensAthensGreece
  2. 2.Metropolitan General HospitalPiraeusGreece

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