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Systematic analysis of the relationship between antibiotic use and extended-spectrum beta-lactamase resistance in Enterobacteriaceae in a French hospital: a time series analysis

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Abstract

The influence of hospital use of antibiotics other than cephalosporins and fluoroquinolones on extended-spectrum beta-lactamase (ESBL) resistance among Enterobacteriaceae is poorly known. Our objective was to explore the association between ESBL and hospital use of various classes of antibacterial agents. The relationship between monthly use of 19 classes of antibacterial agents and incidence of nosocomial ESBL-producing Enterobacteriaceae in a French hospital was studied between 2007 and 2013. Five antibiotic classes were significantly and independently associated with ESBL resistance. Uses of tetracyclines (link estimate ± SE, 0.0066 ± 0.0033), lincosamides (0.0093 ± 0.0029), and other antibacterial agents (0.0050 ± 0.0023) were associated with an increased incidence, while nitrofurantoin (−0.0188 ± 0.0062) and ticarcillin and piperacillin with or without enzyme inhibitor (−0.0078 ± 0.0031) were associated with a decreased incidence. In a multivariate model including 3rd- and 4th-generation cephalosporins, fluoroquinolones, amoxicillin, and amoxicillin–clavulanate, 3rd- and 4th-generation cephalosporins (0.0019 ± 0.0009) and fluoroquinolones (0.0020 ± 0.0008) were associated with an increased ESBL resistance, whereas amoxicillin and amoxicillin–clavulanate were not. Hospital use of tetracyclines and lincosamides may promote ESBL resistance in Enterobacteriaceae. Nitrofurantoin and ticarcillin and piperacillin with or without enzyme inhibitor should be considered as potential alternatives to broad-spectrum cephalosporins and fluoroquinolones to control the diffusion of ESBL resistance.

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References

  1. Zilberberg MD, Shorr AF (2013) Secular trends in gram-negative resistance among urinary tract infection hospitalizations in the United States, 2000–2009. Infect Control Hosp Epidemiol 34:940–946

    Article  PubMed  Google Scholar 

  2. Colodner R, Rock W, Chazan B et al (2004) Risk factors for the development of extended-spectrum beta-lactamase-producing bacteria in nonhospitalized patients. Eur J Clin Microbiol Infect Dis 23:163–167

    Article  CAS  PubMed  Google Scholar 

  3. Kaier K, Frank U, Hagist C et al (2009) The impact of antimicrobial drug consumption and alcohol-based hand rub use on the emergence and spread of extended-spectrum beta-lactamase-producing strains: a time-series analysis. J Antimicrob Chemother 63:609–614

    Article  CAS  PubMed  Google Scholar 

  4. Kanafani ZA, Mehio-Sibai A, Araj GF et al (2005) Epidemiology and risk factors for extended-spectrum beta-lactamase-producing organisms: a case control study at a tertiary care center in Lebanon. Am J Infect Control 33:326–332

    Article  PubMed  Google Scholar 

  5. Rodríguez-Baño J, Alcalá JC, Cisneros JM et al (2008) Community infections caused by extended-spectrum beta-lactamase-producing Escherichia coli. Arch Intern Med 168:1897–1902

    Article  PubMed  Google Scholar 

  6. Aldeyab MA, Harbarth S, Vernaz N et al (2012) 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 74:171–179

    Article  PubMed Central  PubMed  Google Scholar 

  7. Vernaz N, Huttner B, Muscionico D et al (2011) Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-based data from a large hospital and its surrounding community. J Antimicrob Chemother 66:928–935

    Article  CAS  PubMed  Google Scholar 

  8. Li D, Chen Y, Zhang W et al (2013) Risk factors for hospital-acquired bloodstream infections caused by extended-spectrum beta-lactamase Klebsiella pneumoniae among cancer patients. Ir J Med Sci 183:463–469

  9. Gedik H (2012) Does antimicrobial use increase the rate of antimicrobial resistance? A one year experience. Indian J Med Microbiol 30:198–202

    Article  CAS  PubMed  Google Scholar 

  10. Gbaguidi-Haore H, Dumartin C, L’Hériteau F et al (2013) Antibiotics involved in the occurrence of antibiotic-resistant bacteria: a nationwide multilevel study suggests differences within antibiotic classes. J Antimicrob Chemother 68:461–470

    Article  CAS  PubMed  Google Scholar 

  11. Hsu LY, Tan TY, Tam VH et al (2010) Surveillance and correlation of antibiotic prescription and resistance of Gram-negative bacteria in Singaporean hospitals. Antimicrob Agents Chemother 54:1173–1178

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Freeman JT, McBride SJ, Nisbet MS et al (2012) Bloodstream infection with extended-spectrum beta-lactamase-producing Enterobacteriaceae at a tertiary care hospital in New Zealand: risk factors and outcomes. Int J Infect Dis 16:e371–e374

    Article  PubMed  Google Scholar 

  13. Somily AM, Alsubaie SS, BinSaeed AA et al (2014) Extended-spectrum beta-lactamase-producing Klebsiella pneumoniae in the neonatal intensive care unit: does vancomycin play a role? Am J Infect Control 42:277–282

    Article  PubMed  Google Scholar 

  14. Han JH, Nachamkin I, Zaoutis TE et al (2012) Risk factors for gastrointestinal tract colonization with extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli and Klebsiella species in hospitalized patients. Infect Control Hosp Epidemiol 33:1242–1245

    Article  PubMed Central  PubMed  Google Scholar 

  15. Boetius Hertz F, Løbner-Olesen A, Frimodt-Møller N (2014) Antibiotic selection of Escherichia coli sequence type 131 in a mouse intestinal colonization model. Antimicrob Agents Chemother 58:6139–6144

    Article  PubMed Central  PubMed  Google Scholar 

  16. Comité de l’Antibiogramme de la Société Française de Microbiologie (2014) Recommandations 2014. Available online at: http://www.sfm-microbiologie.org/UserFiles/files/casfm/CASFM_EUCAST_V1_0_2014.pdf. Last accessed 21 Jun 2014

  17. Judge GG, Griffiths WE, Hill RC et al (1985) The theory and practice of econometrics. John Wiley & Sons, New York, 1056 pp

    Google Scholar 

  18. Hubert B, Watier L, Garnerin P et al (1992) Meningococcal disease and influenza-like syndrome: a new approach to an old question. J Infect Dis 166:542–545

    Article  CAS  PubMed  Google Scholar 

  19. Opatowski L, Varon E, Dupont C et al (2013) Assessing pneumococcal meningitis association with viral respiratory infections and antibiotics: insights from statistical and mathematical models. Proc Biol Sci 280:20130519

    Article  PubMed Central  PubMed  Google Scholar 

  20. Geser N, Stephan R, Hächler H (2012) Occurrence and characteristics of extended-spectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res 8:21

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Reist M, Geser N, Hächler H et al (2013) ESBL-producing Enterobacteriaceae: occurrence, risk factors for fecal carriage and strain traits in the Swiss slaughter cattle population younger than 2 years sampled at abattoir level. PLoS One 8:e71725

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Geser N, Stephan R, Korczak BM et al (2012) Molecular identification of extended-spectrum-beta-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrob Agents Chemother 56:1609–1612

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Batard E, Ollivier F, Boutoille D et al (2013) Relationship between hospital antibiotic use and quinolone resistance in Escherichia coli. Int J Infect Dis 17:e254–e258

    Article  CAS  PubMed  Google Scholar 

  24. Sun L, Klein EY, Laxminarayan R (2012) Seasonality and temporal correlation between community antibiotic use and resistance in the United States. Clin Infect Dis 55:687–694

    Article  CAS  PubMed  Google Scholar 

  25. Adams SJ, Cunliffe WJ, Cooke EM (1985) Long-term antibiotic therapy for acne vulgaris: effects on the bowel flora of patients and their relatives. J Invest Dermatol 85:35–37

    Article  CAS  PubMed  Google Scholar 

  26. Perez F, Pultz MJ, Endimiani A et al (2011) Effect of antibiotic treatment on establishment and elimination of intestinal colonization by KPC-producing Klebsiella pneumoniae in mice. Antimicrob Agents Chemother 55:2585–2589

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Sherley M, Gordon DM, Collignon PJ (2004) Evolution of multi-resistance plasmids in Australian clinical isolates of Escherichia coli. Microbiology 150:1539–1546

    Article  CAS  PubMed  Google Scholar 

  28. Hoyen CK, Pultz NJ, Paterson DL et al (2003) Effect of parenteral antibiotic administration on establishment of intestinal colonization in mice by Klebsiella pneumoniae strains producing extended-spectrum beta-lactamases. Antimicrob Agents Chemother 47:3610–3612

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Lautenbach E, LaRosa LA, Marr AM et al (2003) Changes in the prevalence of vancomycin-resistant enterococci in response to antimicrobial formulary interventions: impact of progressive restrictions on use of vancomycin and third-generation cephalosporins. Clin Infect Dis 36:440–446

    Article  CAS  PubMed  Google Scholar 

  30. Gupta K, Hooton TM, Naber KG et al (2011) International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 52:e103–e120

    Article  PubMed  Google Scholar 

  31. Leroy J, Patry I, Faure C et al (2011) Regional audit on fluoroquinolones usage in the hospital and the community: are these antibiotics over-used? Pathol Biol (Paris) 59:e103–e107

    Article  CAS  Google Scholar 

  32. Tängdén T, Eriksson BM, Melhus A et al (2011) Radical reduction of cephalosporin use at a tertiary hospital after educational antibiotic intervention during an outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae. J Antimicrob Chemother 66:1161–1167

    Article  PubMed  Google Scholar 

  33. Petrikkos G, Markogiannakis A, Papaparaskevas J et al (2007) Differences in the changes in resistance patterns to third- and fourth-generation cephalosporins and piperacillin/tazobactam among Klebsiella pneumoniae and Escherichia coli clinical isolates following a restriction policy in a Greek tertiary care hospital. Int J Antimicrob Agents 29:34–38

    Article  CAS  PubMed  Google Scholar 

  34. Lee J, Pai H, Kim YK et al (2007) Control of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in a children’s hospital by changing antimicrobial agent usage policy. J Antimicrob Chemother 60:629–637

    Article  CAS  PubMed  Google Scholar 

  35. Livermore DM, Hope R, Reynolds R et al (2013) Declining cephalosporin and fluoroquinolone non-susceptibility among bloodstream Enterobacteriaceae from the UK: links to prescribing change? J Antimicrob Chemother 68:2667–2674

    Article  CAS  PubMed  Google Scholar 

  36. Schechner V, Temkin E, Harbarth S et al (2013) Epidemiological interpretation of studies examining the effect of antibiotic usage on resistance. Clin Microbiol Rev 26:289–307

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors acknowledge Véronique Dilé for providing hospital activity data (number of patient days).

Funding

This study was undertaken without specific funding.

Conflict of interest

The authors declare no conflict of interest.

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Authors and Affiliations

  1. INSERM, U657 Pharmaco-épidémiologie et évaluation de l’impact des produits de santé sur les populations, Paris, France

    M.-A. Vibet

  2. EA3826 Thérapeutiques cliniques et expérimentales des infections, Faculté de Médecine, Université de Nantes, 1 rue Gaston Veil, 44000, Nantes, France

    J. Roux, E. Montassier, S. Corvec, D. Lepelletier & E. Batard

  3. Emergency Department, Centre Hospitalier Universitaire de Nantes, Nantes, France

    E. Montassier & E. Batard

  4. Department of Microbiology and Infection Control, Centre Hospitalier Universitaire de Nantes, Nantes, France

    S. Corvec, M.-E. Juvin & D. Lepelletier

  5. Health Information Management Department, Centre Hospitalier Universitaire de Nantes, Nantes, France

    C. Ngohou

Authors
  1. M.-A. Vibet
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  2. J. Roux
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  3. E. Montassier
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  7. D. Lepelletier
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  8. E. Batard
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Correspondence to E. Batard.

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Vibet, MA., Roux, J., Montassier, E. et al. Systematic analysis of the relationship between antibiotic use and extended-spectrum beta-lactamase resistance in Enterobacteriaceae in a French hospital: a time series analysis. Eur J Clin Microbiol Infect Dis 34, 1957–1963 (2015). https://doi.org/10.1007/s10096-015-2437-3

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  • DOI: https://doi.org/10.1007/s10096-015-2437-3

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