Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong

https://doi.org/10.1016/j.jhin.2011.02.018Get rights and content

Summary

Reduced biocide susceptibility in staphylococci is associated with quaternary ammonium compound (qac) gene-encoding efflux proteins. This study compared the prevalence of antiseptic-resistance genes (qacA/B, smr) in staphylococci colonising nurses and non-healthcare workers. Staphylococcus aureus and coagulase-negative staphylococci (CoNS) isolated from 249 nurses were compared for qacA/B and smr positivity with carriage isolates from non-healthcare workers. Associations between qac genes and antibiotic resistance were investigated and minimum inhibitory concentrations (MICs)/minimum bactericidal concentrations (MBCs) to benzalkonium chloride and chlorhexidine determined. Both genes had higher prevalence in CoNS from nurses (OR: 8.4; 95% CI: 5.4–13.2) and qacA/B was more common in nurses’ S. aureus isolates than those of the general population (OR: 5.5; 95% CI: 2.7–11.2). Meticillin-resistant S. aureus (MRSA) carriage was low (3.2% nurses; 0.5% general population). The risk of harbouring qacA/B and smr was associated with presence of mecA (OR: 2.9; 95% CI: 1.8–4.8) and contact with MRSA-infected patients (OR: 2.0; 95% CI: 1.0–3.9) in S. aureus and CoNS. S. aureus with qac genes displayed significantly more antibiotic resistance and all gene-positive isolates had higher MICs and MBCs to antiseptics. Increased prevalence of antiseptic-resistance genes in staphylococci from nurses indicates that the hospital environment could exert selective pressure for carriage of these strains. The increased proportion of qac genes in meticillin-resistant strains suggests co-selection of these genes, as does the increased carriage of gene-positive strains by those in contact with MRSA-positive patients. Reduced antiseptic susceptibility may allow persistence of organisms in the presence of low level residues and contribute to survival of MRSA.

Introduction

Staphylococcus aureus is a major human pathogen, and resistant strains, especially meticillin-resistant S. aureus (MRSA), are important causes of nosocomial infection. There are increasing numbers of reports of coagulase-negative staphylococci (CoNS) as causative organisms of disease in immunocompromised patients and increased prevalence of multidrug-resistant strains.1

To prevent the spread of pathogens in the hospital and community, disinfectants/antiseptics such as those containing chlorhexidine and benzalkonium chloride (BC) are widely used for decontamination of surfaces, hand disinfection, and decolonisation of patients. Guidelines also recommend their use for decolonisation of high risk groups and routine bathing of patients when basic interventions have failed to reduce rates of MRSA infection.2 Though rigid implementation of infection control practices has led to reductions in infection rates, the ability of MRSA strains to persist in hospital environments has been demonstrated.3, 4

Evidence suggests that widespread use of biocides may impose selective pressure and could contribute to the emergence of bacteria with decreased antiseptic susceptibility. Extensive use may also contribute to emergence of cross-resistance between widely used biocides and antibiotics.5 Quaternary ammonium compound (QAC) resistance determinants, including qacA/B and smr (qac genes), have been shown to be located adjacent to antibiotic resistance genes on transferrable genetic elements, which can allow rapid spread of resistance.6 These genes encode for proton-dependent export proteins and their efflux mechanisms appear to be the major mechanism of tolerance in staphylococci.7

Staphylococcal strains harbouring plasmid-encoded genes, conferring increased minimum bactericidal concentrations (MBCs) to antiseptics, have been demonstrated in clinical isolates of MRSA from Japan (32.6%), Europe (63%), and China (62%).8, 9, 10 Prevalence of these genes may be increasing in MRSA strains, as a longitudinal study reported absence of antiseptic resistance genes in 1990 but 26.7% of isolates were qacA/B positive by 1995, rising to 33.3% by 2005.11

The distribution of qac genes in S. aureus and CoNS has been investigated in clinical isolates, with most focus on MRSA, but little is known about the frequency of these genes in flora of the general public.8, 9, 10, 11, 12 This study determined the prevalence of qac genes in colonising strains of S. aureus and CoNS from nurses and the general public and investigated risk factors for their carriage. The association between the presence of qac genes and antibiotic resistance in isolates was investigated.

Section snippets

Study design

A cross-sectional study of nasal colonisation rates with S. aureus and CoNS harbouring qac genes in nurses and the general public was performed. A minimum sample size of 202 was estimated based on an S. aureus carriage rate of 20% and an assumed 5% carriage rate of qac genes in S. aureus and CoNS with 3% error and 95% confidence intervals (CIs).8, 13, 14 Nurses were recruited from 15 local hospitals and designated as ‘fresh’ (<2 years of nursing experience in the hospital) or ‘experienced’ (≥2

Results

Samples were obtained from 249 nurses, of whom 157 (63.1%) were experienced and 92 (36.9%) fresh. There was no significant difference between S. aureus carriage rates of nurses (51/249; 20.5%) and the general population (186/775; 24%). Eight nurses (3.2%), seven experienced, were colonised with MRSA compared with only 4/775 (0.5%) of the general population (OR: 6.4; 95% CI: 1.9–21.4; P = 0.002). There was a significantly lower rate of meticillin resistance in CoNS isolated from the general public

Discussion

To our knowledge, this is the first report of qac genes in colonising staphylococci from the general public, though these genes have previously been reported in clinical isolates.8, 9, 10, 11, 12, 20 Carriage rates of S. aureus in nurses and the general population were similar to those of previous studies.13, 14 MRSA carriage was lower in the general population and in young nurses. The comparatively shorter exposure time or limited exposure to critically ill patients may explain the lower MRSA

Acknowledgements

The authors wish to thank F. Wong and M. Tsang for their technical assistance.

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