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

Abstract

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.

Effect of Gaseous Ozone on Listeria monocytogenes Planktonic Cells and Biofilm: An In Vitro Study

“…Environmental strains showed a higher tolerance to ozone exposure than food isolates ( Figure 2 b,c). The latter outcome appears justifiable, since it has been demonstrated that environmental strains of L. monocytogenes can persist in food processing plants for months or years, developing a greater resistance to different types of stress and several antimicrobial compounds [ 10 , 15 , 16 , 17 , 36 ].…”

“…However, there are several concerns related to the intensive and prolonged use of these substances. Long-term exposure to antimicrobial agents, for example, may increase the tolerance of microorganisms to certain compounds and lead to a phenomenon known as antimicrobial cross-resistance [ 14 , 15 , 16 , 17 ]. In addition, the most commonly used biocide products may have an environmental and human health impact [ 18 ].…”

Low-Level Tolerance to Fluoroquinolone Antibiotic Ciprofloxacin in QAC-Adapted Subpopulations of Listeria monocytogenes

“…DDAC-exposed cells exhibited a 4.5-fold increase in MIC from 2.1 µg/mL for the control to 9.48 µg/mL in the adapted strains. Additionally, these strains continued to exhibit reduced susceptibility to ciprofloxacin after the de-adaptation step [ 25 ]. Other pathogens such as Pseudomonas aeruginosa , which was enriched for 33 generations in QAC, demonstrated as high as 256-fold increase in MIC of ciprofloxacin [ 26 ].…”

Selection of a Gentamicin-Resistant Variant Following Polyhexamethylene Biguanide (PHMB) Exposure in Escherichia coli Biofilms

“…Large quantities of biocides are used every day to prevent the spread of pathogenic microorganisms in a wide variety of sectors. An increasing quantity of evidence emphasizes a connection between biocide exposure and the modification of susceptibility toward antibiotics in bacteria [ 3 , 4 ]. A better understanding of the potential of various biocides to select resistance toward antibiotics, along with the associated mechanisms, is therefore required in the perspective to combat antibiotic resistance emergence.…”

“…In industries, medical areas, public spaces or at home, biocides are broadly used to avoid the dissemination of pathogenic bacteria and guarantee the microbiological quality of equipment, production surfaces and products. However, an increasing number of studies reported the potential of different biocides to impact antibiotic susceptibility in various bacterial species [ 3 , 4 , 5 ]. Indeed, some mechanisms responsible for a lower susceptibility in adapted bacteria following a biocide exposure could be also involved in antibiotic resistance, as for instance an upregulated non-specific efflux mediated by multidrug pumps, one of the most recurrently described [ 6 , 7 , 8 ].…”