1887

Journal of Medical Microbiology logo

Volume 66, Issue 12

Susceptibility of vancomycin-resistant and -sensitive obtained from Danish hospitals to benzalkonium chloride, chlorhexidine and hydrogen peroxide biocides Free

Abstract

In Danish hospitals, the number of infections caused by vancomycin-resistant (VRE ) has dramatically increased in recent years. Hospital disinfectants are essential in eliminating pathogenic microorganisms, and reduced susceptibility may contribute to hospital-associated infections. We have addressed whether clinical VRE display decreased biocide susceptibility when compared to vancomycin-sensitive (VSE ) isolates.

In total 12 VSE and 37 VRE isolates obtained from Danish hospitals over an extended time period were tested for susceptibility towards three commonly applied biocides, namely benzalkonium chloride, chlorhexidine and hydrogen peroxide.

For benzalkonium chloride, 89 % of VRE strains had a minimal inhibitory concentration (MIC) of 8 mg l, whereas for VSE , only 25 % of the strains had an MIC of 8 mg l. For chlorhexidine, the MIC of 95 % of VRE strains was 4 mg l or higher, while only 33 % of VSE strains displayed MIC values at the same level. In contrast, both VRE and VSE displayed equal susceptibility to hydrogen peroxide, but a higher minimal bactericidal concentration (MBC) was found for the former. The efflux activity was also assessed, and this was generally higher for the VRE strains compared to VSE .

VRE from Danish hospitals demonstrated decreased susceptibility towards benzalkonium chloride and chlorhexidine compared to VSE , where the use of chlorhexidine is particularly heavy in the hospital environment. These findings suggest that biocide tolerance may characterize VRE isolated in Danish hospitals.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): benzalkonium chloride , biocide tolerance , chlorhexidine , Enterococcus faecium , nosocomial infection , VRE and VSE
© 2017 The Authors
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000642
2017-12-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/12/1744.html?itemId=/content/journal/jmm/10.1099/jmm.0.000642&mimeType=html&fmt=ahah

References

  1. Arias CA, Murray BE. The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 2012; 10:266–278 [View Article][PubMed]
     [Google Scholar]
  2. Pinholt M, Larner-Svensson H, Littauer P, Moser CE, Pedersen M et al. Multiple hospital outbreaks of vanA Enterococcus faecium in Denmark, 2012–13, investigated by WGS, MLST and PFGE. J Antimicrob Chemother 2015; 70:2474–2482 [View Article][PubMed]
     [Google Scholar]
  3. Bager F, Birk T, Høg BB, Jensen LB, Jensen AN. DANMAP 2014-Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark; 2015
  4. Hammerum AM, Baig S, Kamel Y, Roer L, Pinholt M et al. Emergence of vanA Enterococcus faecium in Denmark, 2005–15. J Antimicrob Chemother 2017; 72:2184–2190 [View Article][PubMed]
     [Google Scholar]
  5. Willems RJ, Top J, van Schaik W, Leavis H, Bonten M et al. Restricted gene flow among hospital subpopulations of Enterococcus faecium. MBio 2012; 3:e00151-12 [View Article][PubMed]
     [Google Scholar]
  6. Arthur M, Reynolds P, Courvalin P. Glycopeptide resistance in enterococci. Trends Microbiol 1996; 4:401–407 [View Article][PubMed]
     [Google Scholar]
  7. Cattoir V, Leclercq R. Twenty-five years of shared life with vancomycin-resistant enterococci: is it time to divorce?. J Antimicrob Chemother 2013; 68:731–742 [View Article][PubMed]
     [Google Scholar]
  8. Chen C, Sun J, Guo Y, Lin D, Guo Q et al. High prevalence of vanM in vancomycin-resistant Enterococcus faecium isolates from Shanghai, China. Antimicrob Agents Chemother 2015; 59:7795–7798 [View Article][PubMed]
     [Google Scholar]
  9. Landerslev KG, Jakobsen L, Olsen SS, Pedersen MB, Kristensen B et al. Polyclonal spread of vanA Enterococcus faecium in Central Denmark region, 2009–2013, investigated using PFGE, MLST and WGS. Int J Antimicrob Agents 2016; 48:767–768 [View Article][PubMed]
     [Google Scholar]
  10. Russell AD. Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations. Lancet Infect Dis 2003; 3:794–803 [View Article][PubMed]
     [Google Scholar]
  11. Otter JA, French GL. Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor. J Clin Microbiol 2009; 47:205–207 [View Article][PubMed]
     [Google Scholar]
  12. Webber MA, Piddock LJ. The importance of efflux pumps in bacterial antibiotic resistance. J Antimicrob Chemother 2003; 51:9–11 [View Article][PubMed]
     [Google Scholar]
  13. Bischoff M, Bauer J, Preikschat P, Schwaiger K, Mölle G et al. First detection of the antiseptic resistance gene qacA/B in Enterococcus faecalis. Microb Drug Resist 2012; 18:7–12 [View Article][PubMed]
     [Google Scholar]
  14. Rizzotti L, Rossi F, Torriani S. Biocide and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from the swine meat chain. Food Microbiol 2016; 60:160–164 [View Article][PubMed]
     [Google Scholar]
  15. Schwaiger K, Harms KS, Bischoff M, Preikschat P, Mölle G et al. Insusceptibility to disinfectants in bacteria from animals, food and humans-is there a link to antimicrobial resistance?. Front Microbiol 2014; 5:88 [View Article][PubMed]
     [Google Scholar]
  16. Saurina G, Landman D, Quale JM. Activity of disinfectants against vancomycin-resistant Enterococcus faecium. Infect Control Hosp Epidemiol 1997; 18:345–347 [View Article][PubMed]
     [Google Scholar]
  17. Hammerum AM, Jensen LB. Prevalence of esp, encoding the enterococcal surface protein, in Enterococcus faecalis and Enterococcus faecium isolates from hospital patients, poultry, and pigs in Denmark. J Clin Microbiol 2002; 40:4396 [View Article][PubMed]
     [Google Scholar]
  18. Lester CH, Sandvang D, Olsen SS, Schønheyder HC, Jarløv JO et al. Emergence of ampicillin-resistant Enterococcus faecium in Danish hospitals. J Antimicrob Chemother 2008; 62:1203–1206 [View Article][PubMed]
     [Google Scholar]
  19. Dutka-Malen S, Evers S, Courvalin P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J clinical microbiology 1995; 33:24–27
     [Google Scholar]
  20. CLSI (Clinical and Laboratory Standards Institute) (formerly NCCLS) Performance Standards for Antimicrobial Susceptibility Testing, Twenty-second informational supplement. CLSI; 2012 M02-A11-M07-A9
    [Google Scholar]
  21. Skovgaard S, Larsen MH, Nielsen LN, Skov RL, Wong C et al. Recently introduced qacA/B genes in Staphylococcus epidermidis do not increase chlorhexidine MIC/MBC. J Antimicrob Chemother 2013; 68:2226–2233 [View Article][PubMed]
     [Google Scholar]
  22. Seier-Petersen MA, Nielsen LN, Ingmer H, Aarestrup FM, Agersø Y. Biocide susceptibility of Staphylococcus aureus CC398 and CC30 isolates from pigs and identification of the biocide resistance genes, qacG and qacC. Microb Drug Resist 2015; 21:527–536 [View Article][PubMed]
     [Google Scholar]
  23. Skovgaard S, Nielsen LN, Larsen MH, Skov RL, Ingmer H et al. Staphylococcus epidermidis isolated in 1965 are more susceptible to triclosan than current isolates. PLoS One 2013; 8:e62197 [View Article][PubMed]
     [Google Scholar]
  24. Liu Y, Li J, du J, Hu M, Bai H et al. Accurate assessment of antibiotic susceptibility and screening resistant strains of a bacterial population by linear gradient plate. Sci China Life Sci 2011; 54:953–960 [View Article][PubMed]
     [Google Scholar]
  25. Maeder ML, Thibodeau-Beganny S, Sander JD, Voytas DF, Joung JK et al. Oligomerized pool engineering (OPEN): an 'open-source' protocol for making customized zinc-finger arrays. Nat Protoc 2009; 4:1471–1501 [View Article][PubMed]
     [Google Scholar]
  26. Martins M, Couto I, Viveiros M, Amaral L. Identification of efflux-mediated multi-drug resistance in bacterial clinical isolates by two simple methods. Methods Mol Biol 2010; 642:143–157 [View Article][PubMed]
     [Google Scholar]
  27. Suller MT, Russell AD. Antibiotic and biocide resistance in methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococcus. J Hosp Infect 1999; 43:281–291 [View Article][PubMed]
     [Google Scholar]
  28. Morrissey I, Oggioni MR, Knight D, Curiao T, Coque T et al. Evaluation of epidemiological cut-off values indicates that biocide resistant subpopulations are uncommon in natural isolates of clinically-relevant microorganisms. PLoS One 2014; 9:e86669 [View Article][PubMed]
     [Google Scholar]
  29. Beier RC, Duke SE, Ziprin RL, Harvey RB, Hume ME et al. Antibiotic and disinfectant susceptibility profiles of vancomycin-resistant Enterococcus faecium (VRE) isolated from community wastewater in Texas. Bull Environ Contam Toxicol 2008; 80:188–194 [View Article][PubMed]
     [Google Scholar]
  30. Wales AD, Davies RH. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics 2015; 4:567–604 [View Article][PubMed]
     [Google Scholar]
  31. Gullberg E, Albrecht LM, Karlsson C, Sandegren L, Andersson DI. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. MBio 2014; 5:e01918-14 [View Article][PubMed]
     [Google Scholar]
  32. Wassenaar TM, Ussery D, Nielsen LN, Ingmer H. Review and phylogenetic analysis of qac genes that reduce susceptibility to quaternary ammonium compounds in Staphylococcus species. Eur J Microbiol Immunol 2015; 5:44–61 [View Article][PubMed]
     [Google Scholar]
  33. Paulsen IT, Brown MH, Skurray RA. Proton-dependent multidrug efflux systems. Microbiol Rev 1996; 60:575–608[PubMed]
     [Google Scholar]
  34. Putman M, van Veen HW, Degener JE, Konings WN. Antibiotic resistance: era of the multidrug pump. Mol Microbiol 2000; 36:772–773 [View Article][PubMed]
     [Google Scholar]
  35. Levy SB. Active efflux, a common mechanism for biocide and antibiotic resistance. J Appl Microbiol 2002; 92:65S–71S [View Article][PubMed]
     [Google Scholar]
  36. Poole K. Mechanisms of bacterial biocide and antibiotic resistance. J Appl Microbiol 2002; 92:55S–64S [View Article][PubMed]
     [Google Scholar]
  37. Piddock LJ. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 2006; 19:382–402 [View Article][PubMed]
     [Google Scholar]
  38. Guzmán Prieto AM, Wijngaarden J, Braat JC, Rogers MRC, Majoor E et al. The two-component system chtrs contributes to chlorhexidine tolerance in Enterococcus faecium. Antimicrob Agents Chemother 2017; 61:e02122-16 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000642
Loading
Susceptibility of vancomycin-resistant and -sensitive Enterococcus faecium obtained from Danish hospitals to benzalkonium chloride, chlorhexidine and hydrogen peroxide biocides
J. Med. Microbiol. 66, 1744 (2017); https://doi.org/10.1099/jmm.0.000642
/content/journal/jmm/10.1099/jmm.0.000642
/content/journal/jmm/10.1099/jmm.0.000642
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error