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JAC Advance Access originally published online on September 13, 2007
Journal of Antimicrobial Chemotherapy 2007 60(5):947-955; doi:10.1093/jac/dkm314
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© The Author 2007. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Prolonged treatment of Salmonella enterica serovar Typhimurium with commercial disinfectants selects for multiple antibiotic resistance, increased efflux and reduced invasiveness

Kimon A. G. Karatzas1,*, Mark A. Webber2, Frieda Jorgensen3, Martin J. Woodward4, Laura J. V. Piddock2 and Tom J. Humphrey1

1 Zoonotic Infections Group, Division of Veterinary Pathology, Infection and Immunity, School of Clinical Veterinary Science, University of Bristol, Langford House, Langford, Bristol BS40 5DU, UK 2 Antimicrobial Agents Research Group, Division of Immunity and Infection, The Medical School, The University of Birmingham, Birmingham B15 2TT, UK 3 Food Borne Zoonoses Unit, Health Protection Agency South West, School of Clinical Veterinary Science, University of Bristol, Langford House, Langford, Bristol BS40 5DU, UK 4 Department of Food and Environmental Safety, Veterinary Laboratories Agency (Weybridge), New Haw, Addlestone, Surrey KT15 3NB, UK

Received 24 May 2007; returned 20 June 2007; revised 30 July 2007; accepted 31 July 2007

* Correspondence address. Bacterial Stress Response Group, Department of Microbiology National University of Ireland Galway, Galway, Ireland. Tel: +353-91-495091; Fax: +353-91-494598; E-mail: kimon-andreas.karatzas{at}nuigalway.ie

Objectives: To study how disinfectants affect antimicrobial susceptibility and phenotype of Salmonella enterica serovar Typhimurium SL1344.

Methods: Wild-type strain SL1344 and its isogenic gyrA mutant were passaged daily for 7 days in subinhibitory concentrations, and separately for 16 days in gradually increasing concentrations of a quaternary ammonium disinfectant containing formaldehyde and glutaraldehyde (QACFG), an oxidizing compound blend (OXC), a phenolic tar acids-based disinfectant (TOP) and triclosan. The MICs of antimicrobials and antibiotics for populations and representative isolates and the proportion of cells resistant to the MICs for the wild-type were determined. Expression of acrB gene, growth at 37°C and invasiveness of populations in Caco-2 intestinal epithelial cells were assessed.

Results: QACFG and triclosan showed the highest selectivity for variants with reduced susceptibility to chloramphenicol, tetracycline, ampicillin, acriflavine and triclosan. Populations treated with the above biocides had reduced invasiveness in Caco-2 cells, and altered growth kinetics. Resistance to disinfectants was observed only after exposure to gradually increasing concentrations of triclosan, accompanied with a 2000-fold increase in its MIC. Growth in OXC and TOP did not affect the MICs of antibiotics, but resulted in the appearance of a proportion of cells resistant to the MIC of acriflavine and triclosan for the wild-type. Randomly selected stable variants from all populations, except the one treated with TOP, over-expressed acrB.

Conclusions: In vitro exposure to QACFG and triclosan selects for Salmonella Typhimurium cells with reduced susceptibility to several antibiotics. This is associated with overexpression of AcrAB efflux pump, but accompanied with reduced invasiveness.

Keywords: quaternary ammonium , triclosan , AcrAB


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