Tolerance to quaternary ammonium compound disinfectants may enhance growth of Listeria monocytogenes in the food industry

Abstract

The antibacterial effect of disinfectants is crucial for the control of Listeria monocytogenes in food processing environments. Tolerance of L. monocytogenes to sublethal levels of disinfectants based on quaternary ammonium compounds (QAC) is conferred by the resistance determinants qacH and bcrABC. The presence and distribution of these genes have been anticipated to have a role in the survival and growth of L. monocytogenes in food processing environments where QAC based disinfectants are in common use. In this study, a panel of 680 L. monocytogenes from nine Norwegian meat- and salmon processing plants were grouped into 36 MLVA profiles. The presence of qacH and bcrABC was determined in 101 isolates from the 26 most common MLVA profiles. Five MLVA profiles contained qacH and two contained bcrABC. Isolates with qacH and bcrABC showed increased tolerance to the QAC Benzalkonium chloride (BC), with minimal inhibitory concentrations (MICs) of 5-12, 10-13 and <5ppm for strains with qacH (two allele variants observed), bcrABC, and neither gene, respectively. Isolates with qacH or bcrABC were not more tolerant to BC in bactericidal tests in suspension or in biofilms compared with isolates lacking the genes. Water residue samples collected from surfaces in meat processing plants after QAC disinfection had bactericidal effect against L. monocytogenes when the sample BC levels were high (>100ppm). A sample with lower BC concentrations (14ppm of chain length C-12 and 2.7ppm of chain length C-14) inhibited growth of L. monocytogenes not containing bcrABC or qacH, compared to strains with these genes. The study has shown that L. monocytogenes harbouring the QAC resistance genes qacH and bcrABC are prevalent in the food industry and that residuals of QAC may be present in concentrations after sanitation in the industry that result in a growth advantage for bacteria with such resistance genes.

The effect of initial sonication on disinfectant efficacy against Listeria monocytogenes biofilm

“…Quaternary ammonium compounds (QAC) are cationic agents that act by cell membrane disruption. QAC are widely used in hospitals, household and food industry [6]. A serious problem determining bacteria resistance in the biofilm structure is the synthesis of EPS (Extracellular Polymeric Substances) [1,5].…”

Interaction and inactivation of Listeria and Lactobacillus cells in single and mixed species biofilms exposed to different disinfectants

“…The principle of their action involves the impairment of the permeability of bacterial cell membrane, which results in the leakage of low-molecular-weight intracellular substances and in the coagulation of cytoplasmic proteins, which in turn contributes to the inhibition of the primary vital functions and eventually leads to cell death (McDonnell & Russell, 1999). One of the QAC-based disinfectants widely used in the food industry is the benzalkonium chloride (BAC), which contains a mixture of alkyl molecules with a chain length from C12 to C16 (Møretrø et al, 2017). Because of the wide spread usage of QACs, L. monocytogenes is believed to develop resistance to these antimicrobials by the expression of membrane active efflux pumps (Kovacevic et al, 2015;Martínez-Suárez, Ortiz, & López-Alonso, 2016;Romanova, Wolffs, Brovko, & Griffiths, 2006) and by the modification of fatty acid composition in cell membranes (To, Favrin, Romanova, & Griffiths, 2002).…”

Evaluation of ATP bioluminescence‐based methods for hygienic assessment in fish industry

“…The ATP content of bacteria was examined for five strains of L. monocytogenes, one strain of L. innocua and nine strains of other bacteria frequently associated with fish and fish processing. The five L. monocytogenes strains were all isolated from Norwegian plants processing farmed salmon and to some extent also farmed trout (Møretrø et al ). Listeria innocua, from a conveyor belt in a salmon processing plant (Langsrud et al ), was included for comparison with L. monocytogenes , as a representative of other Listeria species than L. monocytogenes .…”