Adaptation to a Commercial Quaternary Ammonium Compound Sanitizer Leads to Cross-Resistance to Select Antibiotics in Listeria monocytogenes Isolated From Fresh Produce Environments

The effective elimination of Listeria monocytogenes through cleaning and sanitation is of great importance to the food processing industry. Specifically in fresh produce operations, the lack of a kill step requires effective cleaning and sanitation to mitigate the risk of cross-contamination from the environment. As facilities rely on sanitizers to control L. monocytogenes, reports of the development of tolerance to sanitizers and other antimicrobials through cross-resistance is of particular concern. We investigated the potential for six L. monocytogenes isolates from fresh produce handling and processing facilities and packinghouses to develop cross-resistance between a commercial sanitizer and antibiotics. Experimental adaptation of isolates belonging to hypervirulent clonal complexes (CC2, CC4, and CC6) to a commercial quaternary ammonium compound sanitizer (cQAC) resulted in elevated minimum inhibitory concentrations (2–3 ppm) and minimum bactericidal concentrations (3–4 ppm). Susceptibility to cQAC was restored for all adapted (qAD) isolates in the presence of reserpine, a known efflux pump inhibitor. Reduced sensitivity to 7/17 tested antibiotics (chloramphenicol, ciprofloxacin, clindamycin, kanamycin, novobiocin, penicillin, and streptomycin) was observed in all tested isolates. qAD isolates remained susceptible to antibiotics commonly used in the treatment of listeriosis (i.e., ampicillin and gentamicin). The whole genome sequencing of qAD strains, followed by comparative genomic analysis, revealed several mutations in fepR, the regulator for FepA fluoroquinolone efflux pump. The results suggest that mutations in fepR play a role in the reduction in antibiotic susceptibility following low level adaptation to cQAC. Further investigation into the cross-resistance mechanisms and pressures leading to the development of this phenomenon among L. monocytogenes isolates recovered from different sources is needed to better understand the likelihood of cross-resistance development in food chain isolates and the implications for the food industry.

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Inactivation of Listeria monocytogenes by Disinfectants and Bacteriophages in Suspension and Stainless Steel Carrier Tests

Journal of Food Protection ◽

10.4315/0362-028x.jfp-14-151 ◽

2014 ◽

Vol 77 (12) ◽

pp. 2012-2020 ◽

Cited By ~ 27

Author(s):

N. CHAITIEMWONG ◽

W. C. HAZELEGER ◽

R. R. BEUMER

Keyword(s):

Stainless Steel ◽

Listeria Monocytogenes ◽

Quaternary Ammonium ◽

Antimicrobial Effect ◽

Quaternary Ammonium Compound ◽

Steel Plates ◽

Ammonium Compound ◽

Standard Requirement ◽

Sodium Dichloroisocyanurate ◽

Food Residues

To simulate food contact surfaces with pits or cracks, stainless steel plates with grooves (depths between 0.2 and 5 mm) were constructed. These plates were artificially contaminated with Listeria monocytogenes in clean conditions, with organic soiling, or after 14 days of biofilm formation after which inactivation of the pathogen by Suma Tab D4 (sodium dichloroisocyanurate, 240 and 300 mg/liter), Suma Bac D10 (quaternary ammonium compound, 740 mg/liter), and bacteriophage suspension (Listex P100) was determined. Both chemical disinfectants performed well in suspension tests and in clean carrier tests according to the European standard with a reduction of more than 5 and 4 log units, respectively, of Listeria cells after 5 min of contact time. However, for the plates with grooves, the reduction could not meet the standard requirement, although a higher reduction of L. monocytogenes was observed in the shallow grooves compared with the deeper grooves. Furthermore, presence of food residues and biofilm reduced the effect of the disinfectants especially in the deep grooves, which was dependent on type of food substrate. Bacteriophages showed the best antimicrobial effect compared with the chemical disinfectants (sodium dichloroisocyanurate and quaternary ammonium compound) in most cases in the shallow grooves, but not in the deep grooves. The chlorine based disinfectants were usually less effective than quaternary ammonium compound. The results clearly demonstrate that surfaces with grooves influenced the antimicrobial effect of the chemical disinfectants and bacteriophages because the pathogen is protected in the deep grooves. The use of bacteriophages to inactivate pathogens on surfaces could be helpful in limited cases; however, use of large quantities in practice may be costly and phage-resistant strains may develop.

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Characterization of proteobacterial plasmid integron-encoded qac efflux pump sequence diversity and quaternary ammonium compound antiseptic selection in E. coli grown planktonically and as biofilms

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.01069-21 ◽

2021 ◽

Author(s):

Carmine J. Slipski ◽

Taylor R. Jamieson-Datzkiw ◽

George G. Zhanel ◽

Denice C. Bay

Keyword(s):

Escherichia Coli ◽

Quaternary Ammonium ◽

Susceptibility Testing ◽

Efflux Pump ◽

Multidrug Resistant ◽

Quaternary Ammonium Compound ◽

Ammonium Compound ◽

E Coli ◽

Susceptibility Patterns

Qac efflux pumps from proteobacterial multidrug-resistant plasmids are integron-encoded and confer resistance to quaternary ammonium compound (QAC) antiseptics, however, many are uncharacterized and misannotated. A survey of >2000 plasmid-encoded qac identified 37 unique qac sequences that correspond to one of five representative motifs: QacE, QacEΔ1, QacF/L, QacH/I, and QacG. Antimicrobial susceptibility testing of each cloned qac member in Escherichia coli , highlighted distinctive antiseptic susceptibility patterns that were most prominent when cells grew as biofilms.

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Biological inactivation of adhering Listeria monocytogenes by listeriaphages and a quaternary ammonium compound.

Applied and Environmental Microbiology ◽

10.1128/aem.59.9.2914-2917.1993 ◽

1993 ◽

Vol 59 (9) ◽

pp. 2914-2917 ◽

Cited By ~ 46

Author(s):

B Roy ◽

H W Ackermann ◽

S Pandian ◽

G Picard ◽

J Goulet

Keyword(s):

Listeria Monocytogenes ◽

Quaternary Ammonium ◽

Quaternary Ammonium Compound ◽

Ammonium Compound

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Genetic Subtyping, Biofilm-Forming Ability and Biocide Susceptibility of Listeria monocytogenes Strains Isolated from a Ready-to-Eat Food Industry

Antibiotics ◽

10.3390/antibiotics9070416 ◽

2020 ◽

Vol 9 (7) ◽

pp. 416

Author(s):

Joana Catarina Andrade ◽

António Lopes João ◽

Carlos de Sousa Alonso ◽

António Salvador Barreto ◽

Ana Rita Henriques

Keyword(s):

Listeria Monocytogenes ◽

Quaternary Ammonium ◽

Benzalkonium Chloride ◽

Food Industry ◽

Raw Materials ◽

Foodborne Pathogen ◽

Positive Association ◽

Quaternary Ammonium Compound ◽

Ammonium Compound ◽

Food Grade

Listeria monocytogenes is a foodborne pathogen of special concern for ready-to-eat food producers. The control of its presence is a critical step in which food-grade sanitizers play an essential role. L. monocytogenes is believed to persist in food processing environments in biofilms, exhibiting less susceptibility to sanitizers than planktonic cells. This study aimed to test the susceptibility of L. monocytogenes in planktonic culture and biofilm to three commercial food-grade sanitizers and to benzalkonium chloride; together with the genetic subtyping of the isolates. L. monocytogenes isolates were collected from raw materials, final products and food-contact surfaces during a 6-year period from a ready-to-eat meat-producing food industry and genetically characterized. Serogrouping and pulsed-field gel electrophoresis (PFGE) revealed genetic variability and differentiated L. monocytogenes isolates in three clusters. The biofilm-forming ability assay revealed that the isolates were weak biofilm producers. L. monocytogenes strains were susceptible both in the planktonic and biofilm form to oxidizing and ethanol-based compounds and to benzalkonium chloride, but not to quaternary ammonium compound. A positive association of biofilm-forming ability and LD90 values for quaternary ammonium compound and benzalkonium chloride was found. This study highlights the need for preventive measures improvement and for a conscious selection and use of sanitizers in food-related environments to control Listeria monocytogenes.

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

International Journal of Food Microbiology ◽

10.1016/j.ijfoodmicro.2016.10.025 ◽

2017 ◽

Vol 241 ◽

pp. 215-224 ◽

Cited By ~ 66

Author(s):

Trond Møretrø ◽

Bjørn C.T. Schirmer ◽

Even Heir ◽

Annette Fagerlund ◽

Pernille Hjemli ◽

...

Keyword(s):

Listeria Monocytogenes ◽

Quaternary Ammonium ◽

Food Industry ◽

Quaternary Ammonium Compound ◽

Ammonium Compound

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Transfer of Persistent Listeria monocytogenes Contamination between Food-Processing Plants Associated with a Dicing Machine

Journal of Food Protection ◽

10.4315/0362-028x-65.7.1129 ◽

2002 ◽

Vol 65 (7) ◽

pp. 1129-1133 ◽

Cited By ~ 109

Author(s):

JANNE M. LUNDÉN ◽

TIINA J. AUTIO ◽

HANNU J. KORKEALA

Keyword(s):

Stainless Steel ◽

Listeria Monocytogenes ◽

Sodium Hypochlorite ◽

Quaternary Ammonium ◽

Quaternary Ammonium Compound ◽

Pfge Type ◽

Ammonium Compound ◽

Type I ◽

Minimal Inhibitory Concentrations ◽

Steel Surfaces

The possibility of the transfer of persistent Listeria monocytogenes contamination from one plant to another with a dicing machine was evaluated, and possible reasons for persistent contamination were analyzed. A dicing machine that diced cooked meat products was transferred from plant A to plant B and then to plant C. After the transfer of the dicing machine, L. monocytogenes PFGE type I, originally found in plant A, was soon also found in plants B and C. This L. monocytogenes PFGE type I caused persistent contamination of the dicing lines in plants B and C. The persistent L. monocytogenes strain and three nonpersistent L. monocytogenes strains found in the dicing line of plant C were tested for adherence to stainless steel surfaces and minimal inhibitory concentrations of a quaternary ammonium compound and sodium hypochlorite, disinfectants widely used in the dicing lines. The persistent strain showed significantly higher adherence to stainless steel surfaces than did the nonpersistent strains. The minimal inhibitory concentrations of sodium hypochlorite were similar for all strains, and the minimal inhibitory concentrations of the quaternary ammonium compound for three of the L. monocytogenes PFGE types, including the persistent PFGE type, were high. All persistent L. monocytogenes PFGE type I isolates were found in an area with high hygienic standards, with the dicing machine being the first point of contamination. These observations show that the dicing machine sustained the contamination and suggest that the dicing machine transferred the persistent L. monocytogenes PFGE type from one plant to another.

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Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes

International Journal of Food Microbiology ◽

10.1016/s0168-1605(00)00357-3 ◽

2000 ◽

Vol 62 (1-2) ◽

pp. 57-63 ◽

Cited By ~ 150

Author(s):

Brit Aase ◽

Gunhild Sundheim ◽

Solveig Langsrud ◽

Liv Marit Rørvik

Keyword(s):

Listeria Monocytogenes ◽

Quaternary Ammonium ◽

Quaternary Ammonium Compound ◽

Ammonium Compound

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Prevalence and Detection of qac Genes from Disinfectant-Resistant Staphylococcus aureus Isolated from Salon Tools in Ishaka Town, Bushenyi District of Uganda

Canadian Journal of Infectious Diseases and Medical Microbiology ◽

10.1155/2020/1470915 ◽

2020 ◽

Vol 2020 ◽

pp. 1-9

Author(s):

Solange Gahongayire ◽

Adamu Almustapha Aliero ◽

Charles Drago Kato ◽

Alice Namatovu

Keyword(s):

Sodium Hypochlorite ◽

Quaternary Ammonium ◽

Bacterial Infections ◽

Healthcare Providers ◽

Quaternary Ammonium Compound ◽

Diffusion Method ◽

Ammonium Compound ◽

Bacterial Strains ◽

Microbiological Methods ◽

Phenotypic Methods

Bacterial infections are on a rise with causal-resistant strains increasing the economic burden to both patients and healthcare providers. Salons are recently reported as one of the sources for transmission of such resistant bacterial strains. The current study aimed at the identification of the prevalent bacteria and characterization of quaternary ammonium compound (qac) genes from disinfectant-resistant S. aureus isolated from salon tools in Ishaka town, Bushenyi District of Uganda. A total of 125 swabs were collected from different salon tools (combs, brushes, scissors, clippers, and shaving machines), and prevalent bacteria were isolated using standard microbiological methods. Identification of isolated bacteria was done using standard phenotypic methods including analytical profile index (API). Susceptibility patterns of the isolated bacteria to disinfectant were determined using the agar well diffusion method. Quaternary ammonium compound (qac) genes (qacA/B and qacC) associated with disinfectant resistances were detected from disinfectant-resistant S. aureus using multiplex polymerase chain reaction (PCR) and Sanger sequencing methods. Of the 125 swab samples collected from salons, 78 (62.4%) were contaminated with different bacteria species. Among the salon tools, clippers had the highest contamination of 20 (80.0%), while shaving machines had the lowest contamination of 11 (44.0%). The most prevalent bacteria identified were Staphylococcus epidermidis (28.1%) followed by S. aureus (26.5%). Of all the disinfectants tested, the highest resistance was shown with sodium hypochlorite 1%. Out of the eight (8) disinfectant-resistant S. aureus analysed for qac genes, 2 (25%) isolates (STP6 and STP9) were found to be qacA/B positive, while 2 (25%) isolates (STP8 and STP9) were found to be qacC gene positive. This study has shown that bacterial contamination of salon tools is common, coupled with resistance to disinfectants with sodium hypochlorite resistance being more common. Furthermore, observed resistance was attributed to the presence of qac genes among S. aureus isolates. A search for qac genes for disinfectant resistance from other bacteria species is recommended.

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