Food Safety: Persistence of Listeria monocytogenes in Food Production Environments

A special issue of Foods (ISSN 2304-8158). This special issue belongs to the section "Food Microbiology".

Deadline for manuscript submissions: closed (30 November 2022) | Viewed by 34682

Special Issue Editor

Department of Animal Science, Iowa State University, Ames, IA, United States
Interests: Listeria monocytogenes; persistence, plasmids; genome; food safety; food microbiology

Special Issue Information

Dear Colleagues, 

The facultative intracellular pathogen Listeria (L.) monocytogenes is responsible for listeriosis, a rare but severe disease in humans, which is acquired primarily through the consumption of contaminated food, particularly "ready-to-eat food" is of high risk. Persistence describes the repeated detection of highly similar or (virtually) identical L. monocytogenes strains over long time periods (usually six months or more) in the same food production environment (FPE). The persistence of L. monocytogenes in FPEs is a considerable challenge for food safety in many areas of food production, as persistence of L. monocytogenes in food production is widely observed. Recent studies have shown that certain L. monocytogenes strains from specific sequence types or lineages can be particularly abundant in FPEs and that increased disinfectant/sanitizer tolerance is one of the mechanisms contributing to the survival of L. monocytogenes in FPEs. A better understanding of the molecular mechanisms contributing to L. monocytogenes persistence in FPEs is thus urgently needed to increase food safety and to develop better control mechanisms against L. monocytogenes in the long-term.

Dr. Stephan Schmitz-Esser
Guest Editor

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Keywords

  • Listeria monocytogenes
  • persistence
  • food safety
  • stress survival

Published Papers (6 papers)

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Research

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22 pages, 1757 KiB  
Article
Evaluation of the Persistence and Characterization of Listeria monocytogenes in Foodservice Operations
by Magaly Toro, Jessica Williams-Vergara, Camila Solar, Ana María Quesille-Villalobos, Hee Jin Kwon, Paola Navarrete, Jianghong Meng, Yi Chen and Angélica Reyes-Jara
Foods 2022, 11(6), 886; https://doi.org/10.3390/foods11060886 - 20 Mar 2022
Cited by 2 | Viewed by 3826
Abstract
Listeria monocytogenes is a major foodborne pathogen that can contaminate food products and colonize food-producing facilities. Foodservice operations (FSOp) are frequently responsible for foodborne outbreaks due to food safety practices failures. We investigated the presence of and characterized L. monocytogenes from two FSOp [...] Read more.
Listeria monocytogenes is a major foodborne pathogen that can contaminate food products and colonize food-producing facilities. Foodservice operations (FSOp) are frequently responsible for foodborne outbreaks due to food safety practices failures. We investigated the presence of and characterized L. monocytogenes from two FSOp (cafeterias) distributing ready-to-eat meals and verified FSOp’s compliance with good manufacturing practices (GMP). Two facilities (FSOp-A and FSOp-B) were visited three times each over 5 months. We sampled foods, ingredients, and surfaces for microbiological analysis, and L. monocytogenes isolates were characterized by phylogenetic analyses and phenotypic characteristics. GMP audits were performed in the first and third visits. A ready-to-eat salad (FSOp-A) and a frozen ingredient (FSOp-B) were contaminated with L. monocytogenes, which was also detected on Zone 3 surfaces (floor, drains, and a boot cover). The phylogenetic analysis demonstrated that FSOp-B had persistent L. monocytogenes strains, but environmental isolates were not closely related to food or ingredient isolates. GMP audits showed that both operations worked under “fair” conditions, and “facilities and equipment” was the section with the least compliances. The presence of L. monocytogenes in the environment and GMP failures could promote food contamination with this pathogen, presenting a risk to consumers. Full article
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15 pages, 4136 KiB  
Article
Conditions of In Vitro Biofilm Formation by Serogroups of Listeria monocytogenes Isolated from Hass Avocados Sold at Markets in Mexico
by María Guadalupe Avila-Novoa, Velia Navarrete-Sahagún, Jean Pierre González-Gómez, Carolina Novoa-Valdovinos, Pedro Javier Guerrero-Medina, Ramón García-Frutos, Liliana Martínez-Chávez, Nanci Edid Martínez-Gonzáles and Melesio Gutiérrez-Lomelí
Foods 2021, 10(9), 2097; https://doi.org/10.3390/foods10092097 - 05 Sep 2021
Cited by 4 | Viewed by 2995
Abstract
Listeria monocytogenes is an important pathogen that has been implicated in foodborne illnesses and the recall of products such as fruit and vegetables. This study determines the prevalence of virulence-associated genes and serogroups and evaluates the effects of different growth media and environmental [...] Read more.
Listeria monocytogenes is an important pathogen that has been implicated in foodborne illnesses and the recall of products such as fruit and vegetables. This study determines the prevalence of virulence-associated genes and serogroups and evaluates the effects of different growth media and environmental conditions on biofilm formation by L. monocytogenes. Eighteen L. monocytogenes isolates from Hass avocados sold at markets in Guadalajara, Mexico, were characterized by virulence-associated genes and serogroup detection with PCR. All isolates harbored 88.8% actA, 88.8% plcA, 83.3% mpl, 77.7% inlB, 77.7% hly, 66.6% prfA, 55.5% plcB, and 33.3% inlA. The results showed that 38.8% of isolates harbored virulence genes belonging to Listeria pathogenicity island 1 (LIPI-1). PCR revealed that the most prevalent serogroup was serogroup III (1/2b, 3b, and 7 (n = 18, 66.65%)), followed by serogroup IV (4b, 4d–4e (n = 5, 27.7%)) and serogroup I (1/2a–3a (n = 1, 5.5%)). The assessment of the ability to develop biofilms using a crystal violet staining method revealed that L. monocytogenes responded to supplement medium TSBA, 1/10 diluted TSBA, and TSB in comparison with 1/10 diluted TSB (p < 0.05) on polystyrene at 240 h (p < 0.05). In particular, the biofilm formation by L. monocytogenes (7.78 ± 0.03–8.82 ± 0.03 log10 CFU/cm2) was significantly different in terms of TSBA on polypropylene type B (PP) (p < 0.05). In addition, visualization by epifluorescence microscopy, scanning electron microscopy (SEM), and treatment (DNase I and proteinase K) revealed the metabolically active cells and extracellular polymeric substances of biofilms on PP. L. monocytogenes has the ability to develop biofilms that harbor virulence-associated genes, which represent a serious threat to human health and food safety. Full article
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16 pages, 1152 KiB  
Article
Intensive Environmental Surveillance Plan for Listeria monocytogenes in Food Producing Plants and Retail Stores of Central Italy: Prevalence and Genetic Diversity
by Gabriella Centorotola, Fabrizia Guidi, Guglielmo D’Aurizio, Romolo Salini, Marco Di Domenico, Donatella Ottaviani, Annalisa Petruzzelli, Stefano Fisichella, Anna Duranti, Franco Tonucci, Vicdalia Aniela Acciari, Marina Torresi, Francesco Pomilio and Giuliana Blasi
Foods 2021, 10(8), 1944; https://doi.org/10.3390/foods10081944 - 20 Aug 2021
Cited by 12 | Viewed by 3198
Abstract
Listeria monocytogenes (Lm) can persist in food processing environments (FPEs), surviving environmental stresses and disinfectants. We described an intensive environmental monitoring plan performed in Central Italy and involving food producing plants (FPPs) and retail grocery stores (RSs). The aim of the [...] Read more.
Listeria monocytogenes (Lm) can persist in food processing environments (FPEs), surviving environmental stresses and disinfectants. We described an intensive environmental monitoring plan performed in Central Italy and involving food producing plants (FPPs) and retail grocery stores (RSs). The aim of the study was to provide a snapshot of the Lm circulation in different FPEs during a severe listeriosis outbreak, using whole genome sequencing (WGS) to investigate the genetic diversity of the Lm isolated, evaluating their virulence and stress resistance profiles. A total of 1217 samples were collected in 86 FPEs with 12.0% of positive surfaces at FPPs level and 7.5% at RSs level; 133 Lm isolates were typed by multilocus sequencing typing (MLST) and core genome MLST (cgMLST). Clonal complex (CC) 121 (25.6%), CC9 (22.6%), CC1 (11.3%), CC3 (10.5%), CC191 (4.5%), CC7 (4.5%) and CC31 (3.8%) were the most frequent MLST clones. Among the 26 cgMLST clusters obtained, 5 of them persisted after sanitization and were re-isolated during the follow-up sampling. All the CC121 harboured the Tn6188_qac gene for tolerance to benzalkonium chloride and the stress survival islet SSI-2. The CC3, CC7, CC9, CC31 and CC191 carried the SSI-1. All the CC9 and CC121 strains presented a premature stop codon in the inlA gene. In addition to the Lm Pathogenicity Island 1 (LIPI-1), CC1, CC3 and CC191 harboured the LIPI-3. The application of intensive environmental sampling plans for the detection and WGS analysis of Lm isolates could improve surveillance and early detection of outbreaks. Full article
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Review

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27 pages, 2585 KiB  
Review
Novel Approaches to Environmental Monitoring and Control of Listeria monocytogenes in Food Production Facilities
by Priyanka Gupta and Achyut Adhikari
Foods 2022, 11(12), 1760; https://doi.org/10.3390/foods11121760 - 15 Jun 2022
Cited by 5 | Viewed by 3769
Abstract
Listeria monocytogenes is a serious public health hazard responsible for the foodborne illness listeriosis. L. monocytogenes is ubiquitous in nature and can become established in food production facilities, resulting in the contamination of a variety of food products, especially ready-to-eat foods. Effective and [...] Read more.
Listeria monocytogenes is a serious public health hazard responsible for the foodborne illness listeriosis. L. monocytogenes is ubiquitous in nature and can become established in food production facilities, resulting in the contamination of a variety of food products, especially ready-to-eat foods. Effective and risk-based environmental monitoring programs and control strategies are essential to eliminate L. monocytogenes in food production environments. Key elements of the environmental monitoring program include (i) identifying the sources and prevalence of L. monocytogenes in the production environment, (ii) verifying the effectiveness of control measures to eliminate L. monocytogenes, and (iii) identifying the areas and activities to improve control. The design and implementation of the environmental monitoring program are complex, and several different approaches have emerged for sampling and detecting Listeria monocytogenes in food facilities. Traditional detection methods involve culture methods, followed by confirmation methods based on phenotypic, biochemical, and immunological characterization. These methods are laborious and time-consuming as they require at least 2 to 3 days to obtain results. Consequently, several novel detection approaches are gaining importance due to their rapidness, sensitivity, specificity, and high throughput. This paper comprehensively reviews environmental monitoring programs and novel approaches for detection based on molecular methods, immunological methods, biosensors, spectroscopic methods, microfluidic systems, and phage-based methods. Consumers have now become more interested in buying food products that are minimally processed, free of additives, shelf-stable, and have a better nutritional and sensory value. As a result, several novel control strategies have received much attention for their less adverse impact on the organoleptic properties of food and improved consumer acceptability. This paper reviews recent developments in control strategies by categorizing them into thermal, non-thermal, biocontrol, natural, and chemical methods, emphasizing the hurdle concept that involves a combination of different strategies to show synergistic impact to control L. monocytogenes in food production environments. Full article
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18 pages, 1073 KiB  
Review
An Exploration of Listeria monocytogenes, Its Influence on the UK Food Industry and Future Public Health Strategies
by Joshua Macleod, Michael L. Beeton and James Blaxland
Foods 2022, 11(10), 1456; https://doi.org/10.3390/foods11101456 - 17 May 2022
Cited by 4 | Viewed by 4222
Abstract
Listeria monocytogenes is a Gram-positive intracellular pathogen that can cause listeriosis, an invasive disease affecting pregnant women, neonates, the elderly, and immunocompromised individuals. Principally foodborne, the pathogen is transmitted typically through contaminated foods. As a result, food manufacturers exert considerable efforts to eliminate [...] Read more.
Listeria monocytogenes is a Gram-positive intracellular pathogen that can cause listeriosis, an invasive disease affecting pregnant women, neonates, the elderly, and immunocompromised individuals. Principally foodborne, the pathogen is transmitted typically through contaminated foods. As a result, food manufacturers exert considerable efforts to eliminate L. monocytogenes from foodstuffs and the environment through food processing and disinfection. However, L. monocytogenes demonstrates a range of environmental stress tolerances, resulting in persistent colonies that act as reservoirs for the reintroduction of L. monocytogenes to food contact surfaces and food. Novel technologies for the rapid detection of L. monocytogenes and disinfection of food manufacturing industries have been developed to overcome these obstacles to minimise the risk of outbreaks and sporadic cases of listeriosis. This review is aimed at exploring L. monocytogenes in the UK, providing a summary of outbreaks, current routine microbiological testing and the increasing awareness of biocide tolerances. Recommendations for future research in the UK are made, pertaining to expanding the understanding of L. monocytogenes dissemination in the UK food industry and the continuation of novel technological developments for disinfection of food and the food manufacturing environment. Full article
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24 pages, 2194 KiB  
Review
Implementation of Food Safety Management Systems along with Other Management Tools (HAZOP, FMEA, Ishikawa, Pareto). The Case Study of Listeria monocytogenes and Correlation with Microbiological Criteria
by Jocelyn C. Lee, Aura Daraba, Chrysa Voidarou, Georgios Rozos, Hesham A. El Enshasy and Theodoros Varzakas
Foods 2021, 10(9), 2169; https://doi.org/10.3390/foods10092169 - 13 Sep 2021
Cited by 22 | Viewed by 14908
Abstract
The food industry’s failure in planning and designing of and in implementing a Food Safety Management System and its foundation elements leads, in most instances, to compromised food safety and subsequent foodborne illness outbreaks. This phenomenon was noticed, worldwide, for all food processors, [...] Read more.
The food industry’s failure in planning and designing of and in implementing a Food Safety Management System and its foundation elements leads, in most instances, to compromised food safety and subsequent foodborne illness outbreaks. This phenomenon was noticed, worldwide, for all food processors, but with a much higher incidence in the medium- and small-sized food processing plants. Our study focuses on the importance of Food Safety Management System (FSMS), Critical Control Points Hazard Analysis (HACCP) and the Prerequisite Programs (PRPs) as the foundation of HACCP, in preventing foodborne outbreaks. For emphasis, we make use of the example of organizational food safety culture failures and the lack of managerial engagement which resulted in a multi-state listeriosis outbreak in USA. Moreover, we correlate this with microbiological criteria. Implementation of food safety management systems (ISO 22000:2018) along with incorporation of management tools such as HAZOP, FMEA, Ishikawa and Pareto have proved to be proactive in the maintenance of a positive food safety culture and prevention of cross-contamination and fraud. Full article
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