Exposure to Quaternary Ammonium Compounds Selects Resistance to Ciprofloxacin in Listeria monocytogenes

In this contribution, the antimicrobial susceptibility toward 11 antibiotics and four biocides of a panel of 205 Listeria monocytogenes (Lm) strains isolated from different ecological niches (i.e., food, animals and natural environment) was evaluated. The impact of exposure to biocides on the antibiotic susceptibilities of Lm was also investigated. Lm strains isolated from food exhibited overall a lower susceptibility (higher minimal inhibitory concentrations, MIC) for ammonium quaternary compounds (QACs) and peracetic acid (PAC) than strains isolated from animals and natural environments. Conversely, the ecological origins of Lm strains did not significantly affect their susceptibilities towards antibiotics. Interestingly, repeated exposure to QACs recurrently led to a decrease in susceptibility toward ciprofloxacin (CIP), a fluoroquinolone antibiotic, largely used in human medicine. Moreover, these lower levels of susceptibility to CIP remained stable in most Lm strains even after subcultures without biocide selection pressure, suggesting an adaptation involving modifications at the genetic level. Results underlined the ability of Lm to adapt to biocides, especially QACs, and the potential link between this adaptation and the selection of resistance toward critical antibiotics such as ciprofloxacin. These data support a potential role of the extensive use of QACs from “farm to fork” in the selection of biocide and antibiotic resistance in pathogenic bacteria such as Lm.

[1]  J. Dewulf,et al.  Effect of subinhibitory exposure to quaternary ammonium compounds on the ciprofloxacin susceptibility of Escherichia coli strains in animal husbandry , 2020, BMC Microbiology.

[2]  W. Messens,et al.  The European Union One Health 2018 Zoonoses Report , 2019, EFSA journal. European Food Safety Authority.

[3]  R. Capita,et al.  Susceptibility of Listeria monocytogenes planktonic cultures and biofilms to sodium hypochlorite and benzalkonium chloride. , 2019, Food microbiology.

[4]  M. Noll,et al.  Biocide-Tolerant Listeria monocytogenes Isolates from German Food Production Plants Do Not Show Cross-Resistance to Clinically Relevant Antibiotics , 2019, Applied and Environmental Microbiology.

[5]  G. Kampf Antibiotic Resistance Can Be Enhanced in Gram-Positive Species by Some Biocidal Agents Used for Disinfection , 2019, Antibiotics.

[6]  Xiaobing Jiang,et al.  MdrL, a major facilitator superfamily efflux pump ofListeria monocytogenesinvolved in tolerance to benzalkonium chloride , 2018, Applied Microbiology and Biotechnology.

[7]  Lei Shi,et al.  Effect of Benzalkonium Chloride Adaptation on Sensitivity to Antimicrobial Agents and Tolerance to Environmental Stresses in Listeria monocytogenes , 2018, Front. Microbiol..

[8]  R. Nannapaneni,et al.  Listeria monocytogenes Response to Sublethal Chlorine Induced Oxidative Stress on Homologous and Heterologous Stress Adaptation , 2018, Front. Microbiol..

[9]  R. Holley,et al.  Emergence of Antibiotic Resistance in Listeria monocytogenes Isolated from Food Products: A Comprehensive Review. , 2018, Comprehensive reviews in food science and food safety.

[10]  Edward M. Fox,et al.  Antimicrobial Resistance in Listeria Species , 2018, Microbiology spectrum.

[11]  D. Vázquez-Sánchez,et al.  Current Knowledge on Listeria monocytogenes Biofilms in Food-Related Environments: Incidence, Resistance to Biocides, Ecology and Biocontrol , 2018, Foods.

[12]  A. Gálvez,et al.  Effects of exposure to quaternary-ammonium-based biocides on antimicrobial susceptibility and tolerance to physical stresses in bacteria from organic foods. , 2017, Food microbiology.

[13]  P. Teixeira,et al.  Survival of Listeria monocytogenes with different antibiotic resistance patterns to food-associated stresses. , 2017, International journal of food microbiology.

[14]  G. Nychas,et al.  Variability of Listeria monocytogenes strains in biofilm formation on stainless steel and polystyrene materials and resistance to peracetic acid and quaternary ammonium compounds. , 2016, International journal of food microbiology.

[15]  M. Denis,et al.  Reduced susceptibilities to biocides and resistance to antibiotics in food‐associated bacteria following exposure to quaternary ammonium compounds , 2016, Journal of applied microbiology.

[16]  J. Martínez-Suárez,et al.  Potential Impact of the Resistance to Quaternary Ammonium Disinfectants on the Persistence of Listeria monocytogenes in Food Processing Environments , 2016, Front. Microbiol..

[17]  C. Knight,et al.  Variable Effects of Exposure to Formulated Microbicides on Antibiotic Susceptibility in Firmicutes and Proteobacteria , 2016, Applied and Environmental Microbiology.

[18]  M. Gilmour,et al.  Tolerance of Listeria monocytogenes to Quaternary Ammonium Sanitizers Is Mediated by a Novel Efflux Pump Encoded by emrE , 2015, Applied and Environmental Microbiology.

[19]  N. Speybroeck,et al.  The global burden of listeriosis: a systematic review and meta-analysis. , 2014, The Lancet. Infectious diseases.

[20]  C. Gerba Quaternary Ammonium Biocides: Efficacy in Application , 2014, Applied and Environmental Microbiology.

[21]  I. Morrissey,et al.  Evaluation of Epidemiological Cut-Off Values Indicates that Biocide Resistant Subpopulations Are Uncommon in Natural Isolates of Clinically-Relevant Microorganisms , 2014, PloS one.

[22]  D. Garmyn,et al.  Listeria monocytogenes, a down-to-earth pathogen , 2013, Front. Cell. Infect. Microbiol..

[23]  Lin Li,et al.  Expression of efflux pump gene lde in ciprofloxacin‐resistant foodborne isolates of Listeria monocytogenes , 2012, Microbiology and immunology.

[24]  J. Pagés,et al.  Cross-resistance between biocides and antimicrobials: an emerging question. , 2012, Revue scientifique et technique.

[25]  S. Kathariou,et al.  Listeria monocytogenes Strains Selected on Ciprofloxacin or the Disinfectant Benzalkonium Chloride Exhibit Reduced Susceptibility to Ciprofloxacin, Gentamicin, Benzalkonium Chloride, and Other Toxic Compounds , 2011, Applied and Environmental Microbiology.

[26]  M. Griffiths,et al.  Role of Efflux Pumps in Adaptation and Resistance of Listeria monocytogenes to Benzalkonium Chloride , 2006, Applied and Environmental Microbiology.

[27]  C. Jacquet,et al.  Efflux Pump Lde Is Associated with Fluoroquinolone Resistance in Listeria monocytogenes , 2003, Antimicrobial Agents and Chemotherapy.

[28]  M. Griffiths,et al.  Postadaptational Resistance to Benzalkonium Chloride and Subsequent Physicochemical Modifications of Listeria monocytogenes , 2002, Applied and Environmental Microbiology.

[29]  J. Maillard Bacterial target sites for biocide action , 2002, Journal of applied microbiology.

[30]  A. Audurier,et al.  Low Sensitivity of Listeria monocytogenes to Quaternary Ammonium Compounds , 2000, Applied and Environmental Microbiology.