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

Kode, Divya; Nannapaneni, Ramakrishna; Bansal, Mohit; Chang, Sam K. C.; Cheng, Wen‐Hsing; Sharma, Chander Shekhar; Kiess, Aaron S.

doi:10.3390/microorganisms9051052

Cited by 10 publications

(11 citation statements)

References 35 publications

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“…Although we did not address the mechanisms underlying adaptation to QAC and trimethoprim tolerance development, this work will provide valuable guidance to expand to different environmental conditions where QAC effluents may persist in the food processing environments for a broader understanding of this phenomenon. Besides trimethoprim, we observed the development of low-level tolerance to fluoroquinolone antibiotic ciprofloxacin in QAC-adapted subpopulations of L. monocytogenes strains which was published recently [37]. The other recent studies indicate that such low-level tolerance to antibiotics can accelerate the emergence of resistance [38], therefore, the data from this study is a first step in deducing any changes against trimethoprim resistance in L. monocytogenes.…”

Section: Discussionsupporting

confidence: 65%

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

Kode

Nannapaneni

Chang

2021

Foods

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Between January and July 2021, there were as many as 30 recalls in the U.S. due to potential Listeria monocytogenes contamination from a variety of food products including muffins, kimchi, chicken salad, ready-to-eat chicken, smoked fish, mushrooms, queso fresco cheese, ice cream, turkey sandwiches, squash, and other foods. A contaminated food chain can serve as a potential vehicle for transmitting antibiotic resistant bacteria since there is a slow emergence of multi-drug antibiotic resistance in L. monocytogenes. Biocides are essential for safe food processing, but they may also induce unintended selective pressure at sublethal doses for the expression of antibiotic resistance in L. monocytogenes. To better understand the sources of such slow emergence of antibiotic resistance through biocide residues present in the food environments, we are working on the role of sublethal doses of commonly used biocides in defined broth and water models for understanding L. monocytogenes adaptation. We recently published the development of low-level tolerance to fluoroquinolone antibiotic ciprofloxacin in quaternary ammonium compound (QAC) adapted subpopulations of L. monocytogenes (Microorganisms 9, 1052). Of the six different antibiotics tested to determine heterologous stress adaptation in eight strains of L. monocytogenes, trimethoprim was the second one that exhibited low-level tolerance development after continuous exposure (by three approaches) to sublethal concentrations of QAC against actively growing planktonic cells of L. monocytogenes. When adapted to daily cycles of fixed or gradually increasing sublethal concentrations of QAC, we observed three main findings in eight L. monocytogenes strains against trimethoprim: (a) 3 of the 8 strains exhibited significant increase in short-range minimum inhibitory concentration (MIC) of trimethoprim by 1.7 to 2.5 fold in QAC-adapted subpopulations compared to non-adapted cells (p < 0.05); (b) 2 of the 8 strains exhibited significant increase in growth rate in trimethoprim (optical density (OD) by 600 nm at 12 h) by 1.4 to 4.8 fold in QAC-adapted subpopulations compared to non-adapted cells (p < 0.05); and (c) 5 of the 8 strains yielded significantly higher survival by 1.3-to-3.1 log CFU/mL in trimethoprim in QAC-adapted subpopulations compared to the non-adapted control (p < 0.05). However, for 3/8 strains of L. monocytogenes, there was no increase in the survival of QAC-adapted subpopulations compared to non-adapted control in trimethoprim. These findings suggest the potential formation of low-level trimethoprim tolerant subpopulations in some L. monocytogenes strains where QAC may be used widely. These experimental models are useful in developing early detection methods for tracking the slow emergence of antibiotic tolerant strains through food chain. Also, these findings are useful in understanding the predisposing conditions leading to slow emergence of antibiotic resistant strains of L. monocytogenes in various food production and food processing environments.

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Section: Discussionsupporting

confidence: 65%

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

Kode

Nannapaneni

Chang

2021

Foods

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“…These less-than-ideal environments can create scenarios where L. monocytogenes could be exposed to sublethal sanitizer concentrations. Links between reduced susceptibility to QACs and antibiotic resistance have been reported for various foodborne bacteria, including L. monocytogenes (Heir et al, 1999;Braoudaki and Hilton, 2004;Langsrud et al, 2004;Rakic-Martinez et al, 2011;Gnanadhas et al, 2013;Kovacevic et al, 2013;Bansal et al, 2018;Kode et al, 2021). This phenomenon of cross-resistance can occur when microorganisms develop survival methods that are effective against different antimicrobial agents with similar mechanisms of action (SCENIHR, 2009).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2022

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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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“…A study by Kode et al. (2021) also found that sublethal adaptation to BC resulted in reduced susceptibility to ciprofloxacin for eight L. monocytogenes strains tested. These findings further emphasize the diversity among isolates and that while co‐selection is important to monitor, our current understanding of co‐selection and cross‐resistance is not at the level that can effectively predict why we see it in some isolates and not others.…”

Section: Sanitizer Tolerance In L Monocytogenesmentioning

confidence: 87%

“…This was further supported by Roedel et al (2019), who found that QAC-tolerant L. monocytogenes strains from German food processing facilities did not exhibit co-tolerance to antibiotics (i.e., amoxicillin and gentamicin). A study by Kode et al (2021) also found that sublethal adaptation to BC resulted in reduced susceptibility to ciprofloxacin for eight L. monocytogenes strains tested. These findings further emphasize the diversity among isolates and that while co-selection is important to monitor, our current understanding of co-selection and crossresistance is not at the level that can effectively predict why we see it in some isolates and not others.…”

Section: Co-selection Cross-resistance and Heteroresistancementioning

confidence: 88%

Probing antimicrobial resistance and sanitizer tolerance themes and their implications for the food industry through the Listeria monocytogenes lens

Bland

Brown

Waite‐Cusic

et al. 2022

Comp Rev Food Sci Food Safe

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The development of antibiotic resistance is a serious public health crisis, reducing our ability to effectively combat infectious bacterial diseases. The parallel study of reduced susceptibility to sanitizers is growing, particularly for environmental foodborne pathogens, such as Listeria monocytogenes. As regulations demand a seek‐and‐destroy approach for L. monocytogenes, understanding sanitizer efficacy and its uses are critical for the food industry. Studies have reported the ability of L. monocytogenes to survive in sanitizer concentrations 10–1000 times lower than the manufacturer‐recommended concentration (MRC). Notably, data show that at MRC and when applied according to the label instructions, sanitizers remain largely effective. Studies also report that variables such as the presence of organic material, application time/temperature, and bacterial attachment to surfaces can impact sanitizer effectiveness. Due to the lack of standardization in the methodology and definitions of sanitizer resistance, tolerance, and susceptibility, different messages are conveyed in different studies. In this review, we examine the diversity of definitions, terminology, and methodologies used in studies examining L. monocytogenes resistance and susceptibility to antimicrobials. Research available to date fails to demonstrate “resistance” of L. monocytogenes to recommended sanitizer treatments as prescribed by the label. As such, sanitizer tolerance would be a more accurate description of L. monocytogenes response to low sanitizer concentrations (i.e., sub‐MRC). Conservative use of word “resistance” will reduce confusion and allow for concise messaging as sanitizer research findings are communicated to industry and regulators.

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

Cited by 10 publications

References 35 publications

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

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

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

Probing antimicrobial resistance and sanitizer tolerance themes and their implications for the food industry through the Listeria monocytogenes lens

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