Abstract
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.
Highlights
Listeria monocytogenes is a Gram-positive bacterium that remains one of the leading causes of mortality among foodborne pathogens in the United States (Scallan et al, 2011; de Noordhout et al, 2014)
Reserpine had no effect on the minimum bactericidal concentration (MBC) of WT strains; the WT strains were no longer able to grow in the presence of 1 ppm of commercial quaternary ammonium compound sanitizer (cQAC)
Our data demonstrate the potential for L. monocytogenes isolates to develop cross-resistance between a cQAC and antibiotics representing different classes
Summary
Listeria monocytogenes is a Gram-positive bacterium that remains one of the leading causes of mortality among foodborne pathogens in the United States (Scallan et al, 2011; de Noordhout et al, 2014). Listeria monocytogenes is well adapted to agricultural environments, where it proliferates in decaying plant matter in the soil (Linke et al, 2014; Liao et al, 2021). It is frequently recovered from diverse food processing environments (Gray et al, 2006; Freitag et al, 2009; Cherifi et al, 2018; Kim et al, 2018; Hurley et al, 2019; Sullivan and Wiedmann, 2020). Sanitizers are formulated at concentrations that will deliver a bactericidal effect, and in general many-fold higher than the minimum bactericidal concentration (MBC) for foodborne pathogens of concern (Cruz and Fletcher, 2012)
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