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

Abstract

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.

Nonsynonymous Mutations in fepR Are Associated with Adaptation of Listeria monocytogenes and Other Listeria spp. to Low Concentrations of Benzalkonium Chloride but Do Not Increase Survival of L. monocytogenes and Other Listeria spp. after Exposure to Benzalkonium Chloride Concentrations Recommended for Use in Food Processing Environments

“…With respect to clinical antibiotics, the term resistance is generally referred to, in both scientific literature ( 31 ) and by government organizations such as the World Health Organization ( https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance ), as the ability of bacteria to maintain growth in therapeutic levels of an antibiotic agent. This definition is less relevant when applied to sanitizers such as BC, because use-level concentrations of BC are highly unlikely to support bacterial growth ( 32 ). In addition, in the context of food processing environments, improper development or implementation of sanitation standard operating procedures can result in the presence of BC at concentrations below use-level concentrations ( 18 ).…”

“…exposed to BC at concentrations below the recommended use-level concentrations. Recently, the term “tolerance” has been proposed as an alternative to the term “resistance” to describe the ability of microorganisms to show reduced susceptibility to sanitizers at concentrations below use-level concentrations ( 32 ). In this study, we sought to investigate the ability of L. monocytogenes and Listeria spp.…”

“…In this study, we sought to investigate the ability of L. monocytogenes and Listeria spp. to grow in low levels of BC (defined here as <20 mg/L), and we will henceforth use the term “tolerance” (as defined in reference 32 ) to refer to the capacity of strains of L. monocytogenes and Listeria spp. to acquire the ability to grow in low levels of BC to which they were once sensitive.…”

Listeria monocytogenes in food businesses: From persistence strategies to intervention/prevention strategies—A review

“…The concentration where 99.9% or more of the initial inoculum is killed. Meyer, 2006;Meyer & Cookson, 2010Bland et al, 2021…”

A Comprehensive Virulence and Resistance Characteristics of Listeria monocytogenes Isolated from Fish and the Fish Industry Environment

“…L. monocytogenes contamination leads to a significant threat for risk groups, including the elderly, pregnant women, neonates, and the immunocompromised [ 1 ], for whom fatality rate can reach 20–30% [ 2 ]. In recent years, it has been responsible for large-scale outbreaks related to fresh produce, deli meats, and other RTE products worldwide [ 3 ]. While listeriosis is often associated with the consumption of contaminated RTE food products, such as cheese, meat and fish products, graved and smoked fish are the most frequently contaminated with L. monocytogenes around the world [ 4 , 5 , 6 , 7 , 8 ].…”