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.
Access this article
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
Similar content being viewed by others
References
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.
Owens RC, Ambrose PG. Antimicrobial safety: focus on fluoroquinolones. Clin Infect Dis. 2005;15(41 Suppl 2):S144–57.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lipsitch M. The rise and fall of antimicrobial resistance. Trends Microbiol. 2001;9(9):438–44.
Paterson DL. The role of antimicrobial management programs in optimizing antibiotic prescribing within hospitals. Clin Infect Dis. 2006;42:S90–5.
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.
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.
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.
Livermore DM. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin Infect Dis. 2002;34:634–40.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol. 2010;74(3):417–33.
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.
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.
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.
Masterton RG. Antibiotic heterogeneity. Int J Antimicrob Agents. 2010;36(Suppl 3):S15–8.
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.
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.
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.
van Belkum A, Dunne WM. Next-generation antimicrobial susceptibility testing. J Clin Microbiol. 2013;51:2018–24.
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.
Cohen A, Bont L, Engelhard D. A multifaceted ‘omics’ approach for addressing the challenge of antimicrobial resistance. Future Microbiol. 2015;10(3):365–76.
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.
Acknowledgements
No funding or sponsorship was received for this study or publication of this article. All named authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship for this manuscript, take responsibility for the integrity of the work as a whole, and have given final approval for the version to be published.
Disclosures
Vasiliki Pitiriga, Georgia Vrioni, George Saroglou, and Athanasios Tsakris have no conflicts of interest.
Compliance with Ethics Guidelines
This article is based on previously conducted studies and does not involve any new studies of human or animal subjects performed by any of the authors.
Author information
Authors and Affiliations
Corresponding author
Additional information
Enhanced content
To view enhanced content for this article go to http://www.medengine.com/Redeem/35F7F060516A3EDC.
Rights and permissions
About this article
Cite this article
Pitiriga, V., Vrioni, G., Saroglou, G. et al. The Impact of Antibiotic Stewardship Programs in Combating Quinolone Resistance: A Systematic Review and Recommendations for More Efficient Interventions. Adv Ther 34, 854–865 (2017). https://doi.org/10.1007/s12325-017-0514-y
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12325-017-0514-y