JAC Advance Access originally published online on August 11, 2008
Journal of Antimicrobial Chemotherapy 2008 62(5):1160-1162; doi:10.1093/jac/dkn332
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Research letters |
Use of antibacterial consumer products containing quaternary ammonium compounds and drug resistance in the community
1 Department of Epidemiology, Columbia University Mailman School of Public Health, 722 West 168th Street, New York, NY 10032, USA 2 Columbia University School of Nursing, 630 West 168th Street, New York, NY 10032, USA 3 Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA, USA 4 Department of Epidemiology, University of Michigan School of Public Health, Center for Social Epidemiology and Population Health, 3659 SPH Tower, 109 Observatory, Ann Arbor, MI 48109-2029, USA
* Corresponding author. Tel: +1-734-615-9213; Fax: +1-734-763-5706; E-mail: aielloa{at}umich.edu
Keywords: antibiotic resistance , antimicrobial resistance surveillance , antibacterial products , biocide
Quaternary ammonium compounds (QACs), such as benzalkonium chloride (BAC), are broad-spectrum antimicrobials widely used for decades to disinfect environmental surfaces in clinical and industrial settings. Reports examining the relationships between biocide use and bacterial resistance among isolates from the community setting are limited.1 We assessed the effect of antibacterial product usage in the home environment on susceptibility to BAC to determine whether there is a correlation between BAC and triclosan MICs and antibiotic resistance.
Data were collected as part of a longitudinal double-blind, randomized clinical trial conducted in a Northern Manhattan neighbourhood.2 Participant enrolment began in October 2000, with a 12 month follow-up period. At baseline, 238 households were enrolled, and 224 (94.1%) households completed the study. Households were randomly assigned to receive either antibacterial or non-antibacterial personal hygiene and household cleaning products. Households randomized to the antibacterial group received a liquid kitchen spray containing QACs (0.08% alkyl dimethyl benzyl ammonium chlorides and 0.02% alkyl benzyl ammonium chlorides), an ‘all-purpose’ surface cleaner containing QACs (2.7% alkyl benzyl ammonium chlorides) and an antimicrobial handwashing soap containing 0.2% triclosan. The non-antibacterial group received similar products lacking antimicrobial ingredients. Informed consent was obtained from each household, and The Institutional Review Board of Columbia University Medical Center approved the study.
At the beginning (baseline) and at the end of the follow-up period, a culture was obtained from a randomly selected hand of the primary caregiver in the household. The hand culture was taken before and after washing with the assigned liquid handwashing product.
The sample collection and bacterial culture methods have been described in detail previously.3 Antibiotic susceptibility was determined using MicroScan WalkAway 96 SI (Dade Behring, Deerfield, IL, USA) and classified using the recommendations from the CLSI. All Gram-negative bacteria were tested against gentamicin, imipenem and ciprofloxacin. Additional tested antibiotics that were only applicable to certain species included: amikacin and ticarcillin/clavulanate for Acinetobacter baumannii and Acinetobacter lwoffii, trimethoprim/sulfamethoxazole for Enterobacter agglomerans and Enterobacter cloacae, trimethoprim/sulfamethoxazole, piperacillin/tazobactam and ceftriaxone for Klebsiella pneumoniae, and piperacillin/tazobactam and ceftazidime for Pseudomonas fluorescens/putida. Antibiotic resistance was defined as resistance or intermediate resistance to at least one antimicrobial agent among all agents tested. Staphylococcal species were tested against oxacillin to ascertain methicillin resistance. The MICs for each isolate of BAC and triclosan were determined using a modified agar dilution method from 0.5 to 256 mg/L and 0.012 to 32 mg/L, respectively.2 As there are no uniform definitions for ‘resistance’ to BAC and triclosan, the median MIC for the isolates of each species at the baseline data collection period was used as a breakpoint to dichotomize susceptibility as high or low for both biocides. ‘High’ susceptibility was defined as an MIC greater than the median value and ‘low’ susceptibility was defined as an MIC less than or equal to the median value for each species at baseline. Regression models with generalized estimating equations (GEEs) were used to assess whether high BAC MICs were associated with high triclosan MICs. Finally, GEEs were used to assess whether high BAC MICs were associated with antibiotic susceptibility of bacterial species. Statistical analyses were conducted using SAS Version 8.02 (Cary, NC, USA).
A total of 645 hand isolates were examined for their BAC and triclosan MICs: 264 at baseline and 381 at the end of the year. At baseline, there was no significant association for any species between high BAC and triclosan MICs (all P > 0.05). However, after 1 year of assigned product use, there was a significant association between high BAC and triclosan MICs for A. lwoffii (OR = 6.57, 95% CI = 1.30–33.33) and for all species combined (OR = 2.18, 95% CI = 1.44–3.29) (Table 1). At the end of 1 year of assigned product usage, there was also a significant association between high BAC MICs and antibiotic resistance for all species combined (Table 1), but not for each species individually (all P > 0.05). Among the Gram-negative bacterial isolates, the association was significant after 1 year (OR = 3.71, 95% CI = 1.32–10.46). There was a significant association between high BAC MICs and antibiotic resistance at baseline, but not at the end of the year among staphylococcal isolates (Table 1).
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This is the first randomized intervention study to assess the relationships between antibacterial product usage, BAC MICs, triclosan MICs and antibiotic susceptibility among isolates obtained from the household setting. We found that after 1 year of assigned product usage, bacterial isolates with high BAC MICs were more likely to have high MICs of triclosan and be resistant to one or more antibiotics.
The current body of literature is inconclusive regarding the potential for decreased susceptibility to biocides among antibiotic-resistant bacteria or increased antibiotic resistance among bacterial isolates with increased tolerance to QACs and other biocides. In one study, hospital isolates adapted to BAC were found to be less susceptible to other QACs, but not resistant to other biocides or antibiotics.4 However, other instances of isolates displaying decreased susceptibility to both QACs and antibiotics have been reported.5,6 Although we observed a significant relationship between high BAC MICs and antibiotic resistance among staphylococcal species at baseline, the relationship was not apparent at the end of the year. Of note, there was a large decrease in the number of methicillin-resistant Staphylococcus aureus-positive isolates over the year, limiting statistical power to detect a significant association. Our findings raise concern that the exposure of bacteria to antibacterial-containing products, such as QACs, may exert a selective pressure resulting in the co-selection of genes encoding reduced susceptibility for both biocides and antibiotics. As the potential role of disinfectants and biocides in minimizing the spread of infectious diseases in homes has not been established, concern over potential decreased susceptibility to biocides and resistance to antibiotics is warranted.
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This project was funded by The National Institute for Nursing Research, NIH, 1 RO1 NR05251.
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None of the contributing authors has a commercial or other association that might pose a conflict of interest.
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Acknowledgements |
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S. Lin (Columbia University School of Nursing) contributed to statistical considerations and sample size calculations.
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References |
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TopFundingTransparency declarationsReferences |
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1 Aiello AE, Larson EL, Levy SB. Consumer antibacterial soaps: effective or just risky? Clin Infect Dis (2007) 45(Suppl 2):S137–47.[CrossRef][Web of Science][Medline]
2
Larson EL, Lin SX, Gomez-Pichardo C, et al. Effect of antibacterial home cleaning and handwashing products on infectious disease symptoms. Ann Intern Med (2004) 140:321–30.
3
Aiello AE, Marshall B, Levy SB, et al. Relationship between triclosan and the susceptibilities of bacteria isolated from hands in the community. Antimicrob Agents Chemother (2004) 48:2973–9.
4
Loughlin MF, Jones MV, Lambert PA. Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J Antimicrob Chemother (2002) 49:631–9.
5 Walsh SE, Maillard JY, Russell AD, et al. Development of bacterial resistance to several biocides and effects on antibiotic susceptibility. J Hosp Infect (2003) 55:98–107.[CrossRef][Web of Science][Medline]
6
Bjorland J, Sunde M, Waage S. Plasmid-borne smr gene causes resistance to quaternary ammonium compounds in bovine Staphylococcus aureus. J Clin Microbiol (2001) 39:3999–4004.
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