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The Role of Food Chain in the Spread of Antimicrobial Resistance

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

Deadline for manuscript submissions: closed (31 May 2022) | Viewed by 11202

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Dr. Wioleta Chajȩcka-Wierzchowska

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Department of Industrial and Food Microbiology, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland
Interests: antimicrobial resistance; food microbiology; coagulase-negative staphylococci; enterococci; Listeria monocytogenes; pathogens; biofilm; virulence factors
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Dr. Maria João Fraqueza

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CIISA-Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Avenida da Universidade Técnica, 1300-477 Lisboa, Portugal
Interests: food safety; traditional meat products; emergent technologies; protective starters
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Dear Colleagues,

Antibiotic resistance is currently one of the most important public health issues. The food chain is recognized as one of the ways of transmitting antibiotic-resistant bacteria. Resistant bacteria can pass on their resistance genes to other bacteria through horizontal transfer mechanisms (conjugation, transduction and transformation). The issue of horizontal resistance gene transfer is addressed either as a direct hazard (food-borne resistant bacteria) or an indirect hazard by the horizontal transfer of mobile genetic element elements like plasmids, transposons, or integrons carrying genes conferring resistance to antimicrobials from non-pathogenic commensal, probiotic, technological strains to pathogenic ones in the food industry. The transfer of genetic elements involved in resistance can occur anywhere throughout the food chain: in the environment, in food producing animals, on food-industry surfaces, in foods or in the human body (e.g., intestinal tract or skin). Usually both direct and indirect hazards act together.

The selective pressure exerted by the use of biocides, including compounds widely used in the food industry, could contribute to the expression and dissemination of antibiotic resistance mechanisms, both in human and in environmental bacteria Genetically modified (GM) crops with antibiotic resistance genes, microorganisms added intentionally to the food chain (probiotic or technological) with potentially transferable antimicrobial resistance genes, and food processing technologies used at sub-lethal doses (e.g., alternative non-thermal treatments) are also issues for concern.

Recent advances in the next-generation sequencing (NGS) offers new possibilities to monitor foods and food production environments, detect and investigate outbreaks, and to result in an understanding of foodborne diseases, opportunities for antibiotic resistant pathogens to be namely those caused by antibiotic resistant bacteria. Whole-genome sequencing (WGS) of bacterial pathogens has shown potential for epidemiological surveillance, outbreak detection, and infection control. In addition, whole metagenome sequencing (WMS) allows for the culture-independent analysis of complex microbial communities, providing useful information on antibiotic resistance genes occurrence. Both technologies can assist the tracking of antibiotic resistance genes and mobile genetic elements, providing the necessary information for the implementation of quantitative risk assessments and allowing for the identification of hotspots and routes of transmission of antimicrobial resistance across the food chain. Metagenomics are also a promising tool for monitoring the spread of antibiotic resistance in different settings through the food chain.

We invite you to submit a review article or original research article related to these topics. In particular, we welcome manuscripts that provide new insights into the role of food and food processing in the spread of antibiotic resistance.

Dr Wioleta Chajęcka-Wierzchowska

Prof. Maria João Fraqueza

Published Papers (5 papers)

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Research

14 pages, 729 KiB

Open AccessArticle

Antimicrobial Susceptibility of Fresh Produce-Associated Enterobacteriaceae and Enterococci in Oman

by Zahra S. Al-Kharousi, Nejib Guizani, Abdullah M. Al-Sadi and Ismail M. Al-Bulushi

Foods 2022, 11(19), 3085; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11193085 - 05 Oct 2022

Cited by 1 | Viewed by 1691

Abstract

Fresh produce bacteria may have phenotypic and/or genotypic antimicrobial resistance traits that may lead to various consequences on the environment and human health. This study evaluated the susceptibility of fresh produce bacteria (banana, cabbage, capsicum, carrots, cucumber, dates, lettuce, mango, papaya, pomegranate, radish, tomato and watermelon) to chlorhexidine and the antibiotic resistance of enterococci. Eighty-eight Enterobacteriaceae bacteria and 31 enterococci were screened for their susceptibility to chlorhexidine using the broth microdilution method. Susceptibility of enterococci to various antibiotics was determined using agar dilution, colorimetric, and Kirby-Bauer disc diffusion methods. Enterococci were more susceptible to chlorhexidine than Enterobacteriaceae indicated by chlorhexidine minimum inhibitory concentration (MIC) of 1 to 8 µg/mL for the former and 1 to 64 µg/mL for the latter. The IntI 1, qacEΔ1, qacE and qacG genes were distributed weakly in three, two, two, and three Enterobacteriaceae isolates, respectively. Enterococci had resistance to chloramphenicol (3%), tetracycline (19%), erythromycin (68%), ciprofloxacin (55%), and vancomycin (10%) while 19% of them were multi-drug resistant. In conclusion, this research detected a low to moderate level of antibiotic resistance in enterococci. Some Enterobacteriaceae bacteria had reduced chlorhexidine MICs that were not 10x less than the recommended concentration (100–200 µg/mL) in food production areas which might challenge the success of the disinfection processes or have clinical implications if the involved bacteria are pathogens. The prevalence of antimicrobial-resistant bacteria in fresh produce should be monitored in the future. Full article

(This article belongs to the Special Issue The Role of Food Chain in the Spread of Antimicrobial Resistance)

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8 pages, 1055 KiB

Open AccessCommunication

Short Communication: Low Prevalence of Clinically Important Antibiotic-Resistant Strains among Non-Pathogenic Genera of the Tribe Klebsielleae

by Arkadiusz Józef Zakrzewski, Wioleta Chajęcka-Wierzchowska and Anna Zadernowska

Foods 2022, 11(15), 2270; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11152270 - 29 Jul 2022

Cited by 1 | Viewed by 1501

Abstract

Hafnia sp. and Serratia sp. belong to the Tribe Klebsielleae; although they are not considered pathogenic bacteria, there are many documented cases of diseases caused by these microorganisms. The aim of this study was to determine the antibiotic resistance profiles of strains belonging to the genus Hafnia and Serratia isolated from fish and shrimps. Phenotypic antibiotic resistance was determined using the semi-automatic Vitek 2 system (bioMérieux, Marcy-l’Étoile, France), while the presence of the extended-spectrum beta-lactamase, AmpC beta-lactamases, Klebsiella pneumoniae carbapenemases and Metallo-β-Lactamase producing strains were determined using the MIC Test Strip (Liofilchem, Roseto degli Abbruzzi, Italy). As a result of the conducted research, it was observed that a vast number of Hafnia sp. strains were resistant to cefalexin (84.61%), while Serratia sp. Strains to cefuroxime (79.41%) and nitrofurantoin (85.29%). In addition, it was observed that of all strains, only one had an ability to produce enzymes typical for β-lactamase-producing Enterobacterales. Although the strains of Hafnia sp. and Serratia sp. isolated from fish and shrimp are not characterized by frequent resistance to antibiotics, taking into account the constantly growing number of antibiotic-resistant strains, this may be a problem in the future, mainly due to gene transfer through mobile genetic elements and the acquisition of resistance expressed phenotypically through contact with stress factors. Therefore, studies monitoring the antibiotic resistance profile of these species should be carried out on a regular basis. Full article

(This article belongs to the Special Issue The Role of Food Chain in the Spread of Antimicrobial Resistance)

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9 pages, 401 KiB

Open AccessArticle

Linezolid-Resistant Enterococcus spp. Isolates from Foods of Animal Origin—The Genetic Basis of Acquired Resistance

by Urszula Zarzecka, Arkadiusz Józef Zakrzewski, Wioleta Chajęcka-Wierzchowska and Anna Zadernowska

Foods 2022, 11(7), 975; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11070975 - 28 Mar 2022

Cited by 5 | Viewed by 2645

Abstract

Enterococci are important opportunistic pathogens with the capacity to acquire and spread antibiotic resistance. At present, linezolid-resistant enterococci (LRE) pose a great challenge. Linezolid is considered as a last resort antibiotic in the treatment of enterococcal infections, so it is important to monitor the occurrence of LRE in various environments. The aim of this study was to define the genetic mechanisms of linezolid resistance in enterococci (E. faecalis, E. faecium, E. hirae, E. casseliflavus) isolated from foods of animal origin (n = 104). Linezolid resistance (LR) was shown by 26.9% of isolates. All of them displayed linezolid MICs of 8–32 µg/mL, and 96.4% of them were multidrug multidrug-resistant. The most common acquired linezolid resistance gene in LR isolates was poxtA (64%), followed by optrA (28%) and cfr (12%). According to the authors’ knowledge, this research is the first to indicate the presence of the cfr gene among isolates from food. In 28.6% of the isolates, the point mutation G2576T in the V domain of the 23S rRNA was responsible for linezolid resistance. All isolates harbored the wild-type rplC, rplD and rplV genes. The obtained results indicate that linezolid resistance among enterococci in animal-derived food may result from various genetic mechanisms. The most worrying is that this resistance is encoded on mobile genetic elements, so there is a risk of its rapid transmission, even despite the lack of selective pressure resulting from the use of antibiotics. Full article

(This article belongs to the Special Issue The Role of Food Chain in the Spread of Antimicrobial Resistance)

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16 pages, 929 KiB

Open AccessArticle

Evaluation of Virulence Factors, Antibiotic Resistance, and Biofilm Formation of Escherichia coli Isolated from Milk and Dairy Products in Isfahan, Iran

by Arghavan Madani, Zahra Esfandiari, Parisa Shoaei and Behrooz Ataei

Foods 2022, 11(7), 960; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11070960 - 26 Mar 2022

Cited by 7 | Viewed by 2674

Abstract

Diarrheagenic E. coli (DEC) strains are important causes of gastrointestinal diseases worldwide, especially in developing countries. This study aimed to investigate the presence, antibiotic resistance, and potential biofilm formation in dairy products in Isfahan, Iran. A total of 200 samples, including traditional and pasteurized dairy products, were analyzed. In 200 samples, 54 E. coli isolates, including (48/110) and (6/90) positive samples of traditional and pasteurized dairy products, were detected. Furthermore, pathogenic strains were isolated from 30% of traditional dairy products and 5.55% of pasteurized dairy products. Most isolates were classified as enteropathogenic E. coli (EPEC). Moreover, antibiotic resistance was evaluated using the disk diffusion method for pathogenic E. coli. Overall, 73.68% of contaminated samples by pathogenic strains were resistant to at least one antibiotic. The highest resistance was observed against streptomycin (57.9%), followed by tetracycline (50%). Additionally, all isolates were sensitive to amikacin. For evaluating biofilm formation, the violet crystal assay was applied on a polystyrene microplate well for pathogenic isolates. In total, 68.42% of isolates were able to form biofilms. The presence of E. coli in dairy products indicates potential health risks for Iranian consumers. Serious measures are needed to control and prevent the spread of this pathogen. Full article

(This article belongs to the Special Issue The Role of Food Chain in the Spread of Antimicrobial Resistance)

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16 pages, 2964 KiB

Open AccessArticle

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

by Divya Kode, Ramakrishna Nannapaneni and Sam Chang

Foods 2021, 10(8), 1800; https://0-doi-org.brum.beds.ac.uk/10.3390/foods10081800 - 04 Aug 2021

Cited by 5 | Viewed by 1734

Abstract

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. Full article

(This article belongs to the Special Issue The Role of Food Chain in the Spread of Antimicrobial Resistance)

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