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Antimicrobial Resistance in Food-borne Pathogens

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A special issue of Antibiotics (ISSN 2079-6382).

Deadline for manuscript submissions: closed (31 December 2022) | Viewed by 23315

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Special Issue Editor

Dr. Friederike Hilbert

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Guest Editor

Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria
Interests: foodborne pathogens; bacteriophage; resistance transfer; transduction; food microbiology; antimicrobial activity
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Antimicrobial resistance (AMR) in bacteria represents a major challenge for public health. The use of antibiotics in livestock and agriculture is known to have contributed to the emergence of AMR. AMR food-borne pathogens in food-producing animals can spread to humans via consumption of contaminated food or water, and direct contact with animals. Additionally produce (fruits and vegetables) and other plant-based foods can get contaminated by AMR food-borne pathogens during farming and processing and may bear a risk for AMR transfer to humans.

This Special Issue aims to collect multidisciplinary research related to the possible emergence, spread and transfer of AMR in the food chain. The papers in this issue will constitute a valuable knowledge reservoir for scientists working in the field of AMR.

Dr. Friederike Hilbert
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Antibiotics is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

Antimicrobial resistance
food-borne pathogens
food safety
AMR control

Published Papers (9 papers)

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Research

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9 pages, 1385 KiB

Open AccessArticle

Salmonella Prophages, Their Propagation, Host Specificity and Antimicrobial Resistance Gene Transduction

by Lisa Trofeit, Elisabeth Sattler, Johannes Künz and Friederike Hilbert

Antibiotics 2023, 12(3), 595; https://doi.org/10.3390/antibiotics12030595 - 16 Mar 2023

Cited by 1 | Viewed by 1773

Abstract

Salmonella enterica subsp. enterica is a zoonotic bacterial pathogen that causes foodborne outbreaks in humans. Lytic bacteriophages to control Salmonella in food production are already being used in scientific studies and some are commercially available. However, phage application is still controversial. In addition to virulent phages, which are used in phage therapy and lyse the bacterial host, lysogenic phages coexist in the environment and can reside as prophages in the bacterial host. Therefore, information about Salmonella prophages is essential to understand successful phage therapy. In 100 Salmonella food isolates of the serovars Enteritidis and Typhimurium, we propagated prophages by oxidative stress. In isolates of the serovars Typhimurium and Enteritidis, 80% and 8% prophages could be activated, respectively. In the phage lysates from the serovar Typhimurium, the following antibiotic resistance genes or gene fragments were detected by PCR: sul1, sul2, bla_TEM, strA and cmlA; however, no tetA,B,C, bla_OXA, bla_CMY, aadA1, dfr1,2 or cat were detected. In contrast, no resistance genes were amplified in the phage lysates of the serovar Enteritidis. None of the phage lysates was able to transduce phenotypic resistance to WT 14028s. Most of the prophage lysates isolated were able to infect the various Salmonella serovars tested. The high abundance of prophages in the genome of the serovar Typhimurium may counteract phage therapy through phage resistance and the development of hybrid phages. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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10 pages, 1713 KiB

Open AccessArticle

Low-Level Tetracycline Resistance Gene tet(O)_3 in Campylobacter jejuni

by Cátia Pacífico, Marc M. S. M. Wösten and Friederike Hilbert

Antibiotics 2023, 12(3), 426; https://doi.org/10.3390/antibiotics12030426 - 21 Feb 2023

Viewed by 1653

Abstract

Campylobacter (C.) spp. are the most important foodborne, bacterial, and zoonotic pathogens worldwide. Resistance monitoring of foodborne bacterial pathogens is an important tool to control antimicrobial resistance as a part of the “One Health” approach. The detection and functionality of new resistance genes are of paramount importance in applying more effective screening methods based on whole genome sequencing (WGS). Most tetracycline-resistant C. spp. isolates harbor tet(O), a gene that encodes a ribosomal protection protein. Here we describe tet(O)_3, which has been identified in two food isolates of C. jejuni and is very similar to the tet(O) gene in Streptococcus pneumoniae, having a truncated promoter sequence. This gene confers resistance to tetracycline below 1 mg/L, which is the epidemiological cut-off value. We have analyzed the entire genome of these two isolates, together with a C. jejuni isolate found to have high-level resistance to tetracycline. In contrast to the highly resistant isolate, the promoter of tet(O)_3 is highly responsive to tetracycline, as observed by reverse transcription polymerase chain reaction (RT-PCR). In addition, the two isolates possess a CRISPR repeat, fluoroquinolone resistance due to the gyrA point mutation C257T, a β-lactamase resistance gene bla_OXA-184, a multidrug efflux pump CmeABC and its repressor CmeR, but no plasmid. Low-level antibiotic resistant C. jejuni might therefore have an advantage for surviving in non-host environments. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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19 pages, 2587 KiB

Open AccessArticle

Surveillance on ESBL-Escherichia coli and Indicator ARG in Wastewater and Reclaimed Water of Four Regions of Spain: Impact of Different Disinfection Treatments

by Márcia Oliveira, Pilar Truchado, Rebeca Cordero-García, María I. Gil, Manuel Abellán Soler, Amador Rancaño, Francisca García, Avelino Álvarez-Ordóñez and Ana Allende

Antibiotics 2023, 12(2), 400; https://doi.org/10.3390/antibiotics12020400 - 16 Feb 2023

Cited by 2 | Viewed by 2035

Abstract

In the present study, the occurrence of indicator antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) both in the influent and the effluent of four Spanish wastewater treatment plants (WWTPs) was monitored for 12 months, and the susceptibility profiles of 89 recovered extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolates were obtained against a wide range of antimicrobials. The aim of the study was to better understand whether the current wastewater treatment practices allow us to obtain safe reclaimed water mitigating the spread of ARB and ARGs to the environment. Results showed high concentrations of ESBL-producing E. coli as well as a high prevalence of a range of ARGs in the influent samples. The reclamation treatments implemented in the WWTPs were effective in reducing both the occurrence of ESBL E. coli and ARGs, although significant differences were observed among WWTPs. Despite these reductions in occurrence observed upon wastewater treatment, our findings suggest that WWTP effluents may represent an important source of ARGs, which could be transferred among environmental bacteria and disseminate antimicrobial resistance through the food chain. Remarkably, no major differences were observed in the susceptibility profiles of the ESBL E. coli isolated from influent and effluent waters, indicating that water treatments do not give rise to the emergence of new resistance phenotypes. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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21 pages, 711 KiB

Open AccessArticle

Prevalence and Antibiotic Resistance of Staphylococcus aureus and Escherichia coli Isolated from Bovine Raw Milk in Lebanon: A study on Antibiotic Usage, Antibiotic Residues, and Assessment of Human Health Risk Using the One Health Approach

by Maha Hoteit, Joseph Yaghi, Andre El Khoury, Rouaa Daou, Pamela Hindieh, Jean Claude Assaf, Jana Al Dawi, Jennifer El Khoury and Ayoub Al Jawaldeh

Antibiotics 2022, 11(12), 1815; https://doi.org/10.3390/antibiotics11121815 - 14 Dec 2022

Viewed by 1685

Abstract

The emergence, persistence, and spread of antibiotic-resistant microbes is a tremendous public health threat that is considered nowadays a critical One Health issue. In Lebanon, the consumption of raw bovine milk has been recently reported as a result of the financial crisis. The objectives of the current study were (1) to evaluate raw bovine milk samples in a comprehensive manner for the types of antibiotics used and their residues, (2) to determine the presence of mesophilic bacteria, extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and methicillin-resistant Staphylococcus aureus (MRSA), and (3) to determine the associated human health risk caused by drinking raw milk with antibiotic residues among all age categories. LC-MS-MS was used to carry out the analysis. From 200 milk samples, 30 (15%) were found contaminated with four major antibiotics. The highest average concentration detected was for oxytetracyline 31.51 ± 13.23 μg/kg, followed by 5.5 ± 0.55 μg/kg for gentamicin, 4.56 ± 0.73 μg/kg for colistin, and 4.44 ± 0.89 μg/kg for tylosin. The mean contamination among most samples was below the maximum residue limits (MRLs). Upon comparison with the acceptable daily intake (ADI), the estimated daily intake (EDI) across all age groups was acceptable. The hazard quotient (HQ) was also below 1 across all age groups, signifying the absence of associated health risks for the Lebanese consumers. On the other hand, all milk samples were found exceeding the maximum tolerable value of mesophilic flora. Antibiotic-resistant bacteria (ARB) were detected and represented by ESBL-producing E. coli and MRSA isolates. Thus, the greatest threat of antibiotic use in Lebanon does not fall under antibiotic residues but rather the proliferation of antibiotic resistance in potentially pathogenic bacteria. In this study, the virulence profile of detected bacteria was not investigated; thus their pathogenicity remains unknown. Therefore, to mitigate this health threat in Lebanon, a “One Health” action plan against ABR is required. It will provide a framework for continued, more extensive action to reduce the emergence and spread of ABR in Lebanon. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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9 pages, 1503 KiB

Open AccessArticle

Plasmid-Coded Linezolid Resistance in Methicillin-Resistant Staphylococcus aureus from Food and Livestock in Germany

by Tobias Lienen, Mirjam Grobbel, Bernd-Alois Tenhagen and Sven Maurischat

Antibiotics 2022, 11(12), 1802; https://doi.org/10.3390/antibiotics11121802 - 12 Dec 2022

Cited by 6 | Viewed by 1475

Abstract

Resistance of methicillin-resistant Staphylococcus aureus (MRSA) from food and livestock to last resort antibiotics such as linezolid is highly concerning, since treatment options for infections in humans might be diminished. Known mechanisms of linezolid resistance include point mutations in the 23S rRNA gene and in the ribosomal proteins L3, L4 and L22 as well as an acquisition of the cfr, optrA or poxtA gene. The objective of our study was to characterize antimicrobial resistance (AMR) determinants and phylogenetic relationships among linezolid-resistant (LR-) MRSA from food and livestock. In total, from more than 4000 incoming isolates in the years 2012 to 2021, only two strains from 2015 originating from pig samples exhibited linezolid resistance in the antimicrobial susceptibility testing with MICs of ≥8 mg/L. These LR-MRSA were characterized in detail by whole-genome sequencing and phylogenetic analyses using cgMLST. The LR-MRSA strains showed resistances to ten and eight different antibiotics, respectively. Both strains harbored plasmid-coded cfr genes mediating the linezolid resistance. The cfr genes showed identical sequences in both strains. In addition to the cfr gene, genes for phenicol and clindamycin resistance were detected on the respective plasmids, opening the possibility for a co-selection. The LR-MRSA differed distantly in the phylogenetic analyses and also to other MRSA from pig samples in the year 2015. In conclusion, the occurrence of LR-MRSA in food and livestock seems to be very rare in Germany. However, carriage of plasmids with linezolid resistance determinants could lead to further linezolid-resistant strains by horizontal gene transfer. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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19 pages, 2930 KiB

Open AccessArticle

Antimicrobial Resistance Genes Analysis of Publicly Available Staphylococcus aureus Genomes

by Vincenzo Pennone, Miguel Prieto, Avelino Álvarez-Ordóñez and José F. Cobo-Diaz

Antibiotics 2022, 11(11), 1632; https://doi.org/10.3390/antibiotics11111632 - 16 Nov 2022

Cited by 5 | Viewed by 2608

Abstract

Staphylococcus aureus is a pathogen that can cause severe illness and express resistance to multiple antimicrobial agents. It is part of the ESKAPE organisms and it has been included by the Centers for Disease Control and Prevention (CDC) of USA in the list of serious threats to humans. Many antimicrobial mechanisms have been identified, and, in particular, antimicrobial resistance genes (ARGs) can be determined by whole genome sequencing. Mobile genetic elements (MGEs) can determine the spread of these ARGs between strains and species and can be identified with bioinformatic analyses. The scope of this work was to analyse publicly available genomes of S. aureus to characterise the occurrence of ARGs present in chromosomes and plasmids in relation to their geographical distribution, isolation sources, clonal complexes, and changes over time. The results showed that from a total of 29,679 S. aureus genomes, 24,765 chromosomes containing 73 different ARGs, and 21,006 plasmidic contigs containing 47 different ARGs were identified. The most abundant ARG in chromosomes was mecA (84%), while blaZ was the most abundant in plasmidic contigs (30%), although it was also abundant in chromosomes (42%). A total of 13 clonal complexes were assigned and differences in ARGs and CC distribution were highlighted among continents. Temporal changes during the past 20 years (from 2001 to 2020) showed that, in plasmids, MRSA and macrolide resistance occurrence decreased, while the occurrence of ARGs associated with aminoglycosides resistance increased. Despite the lack of metadata information in around half of the genomes analysed, the results obtained enable an in-depth analysis of the distribution of ARGs and MGEs throughout different categories to be undertaken through the design and implementation of a relatively simple pipeline, which can be also applied in future works with other pathogens, for surveillance and screening purposes. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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10 pages, 1179 KiB

Open AccessArticle

Phylogenetic Groups and Antimicrobial Resistance Genes in Escherichia coli from Different Meat Species

by Angelika Sacher-Pirklbauer, Daniela Klein-Jöbstl, Dmitrij Sofka, Anne-Béatrice Blanc-Potard and Friederike Hilbert

Antibiotics 2021, 10(12), 1543; https://doi.org/10.3390/antibiotics10121543 - 16 Dec 2021

Cited by 8 | Viewed by 2510

Abstract

Escherichia coli isolated from meat of different animal species may harbour antimicrobial resistance genes and may thus be a threat to human health. The objectives of this study were to define antimicrobial resistance genes in E. coli isolates from pork, beef, chicken- and turkey meat and analyse whether their resistance genotypes associated with phylogenetic groups or meat species. A total number of 313 E. coli samples were isolated using standard cultural techniques. In 98% of resistant isolates, a dedicated resistance gene could be identified by PCR. Resistance genes detected were tet(A) and tet(B) for tetracycline resistance, strA and aadA1 for streptomycin resistance, sulI and sulII for resistance against sulphonamides, dfr and aphA for kanamycin resistance and bla_TEM for ampicillin resistance. One stx1 harbouring E. coli isolated from pork harboured the tet(A) gene and belonged to phylogenetic group B2, whilst another stx1 positive isolate from beef was multi-resistant and tested positive for bla_TEM,aphA, strA–B, sulII, and tet(A) and belonged to phylogenetic group A. In conclusion, the distribution of resistance elements was almost identical and statistically indifferent in isolates of different meat species. Phylogenetic groups did not associate with the distribution of resistance genes and a rather low number of diverse resistance genes were detected. Most E. coli populations with different resistance genes against one drug often revealed statistically significant different MIC values. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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22 pages, 2545 KiB

Open AccessArticle

Prevalence and Antimicrobial Resistance Profiles of Foodborne Pathogens Isolated from Dairy Cattle and Poultry Manure Amended Farms in Northeastern Ohio, the United States

by Woinshet Hailu, Yosra A. Helmy, Geoffrey Carney-Knisely, Michael Kauffman, Dean Fraga and Gireesh Rajashekara

Antibiotics 2021, 10(12), 1450; https://doi.org/10.3390/antibiotics10121450 - 25 Nov 2021

Cited by 33 | Viewed by 4520

Abstract

Foodborne pathogens significantly impact public health globally. Excessive antimicrobial use plays a significant role in the development of the public health crisis of antibiotic resistance. Here, we determined the prevalence and antimicrobial resistance profiles of E. coli O157, Salmonella, L. monocytogenes, and Campylobacter isolated between 2016 and 2020 from small scale agricultural settings that were amended with dairy cattle or poultry manure in Northeastern Ohio. The total prevalence of the foodborne pathogens was 19.3%: Campylobacter 8%, Listeria monocytogenes 7.9%, Escherichia coli O157 1.8%, and Salmonella 1.5%. The prevalence was significantly higher in dairy cattle (87.7%) compared to poultry (12.2%) manure amended farms. Furthermore, the prevalence was higher in manure samples (84%) compared to soil samples (15.9%; p < 0.05). Multiple drug resistance was observed in 73%, 77%, 100%, and 57.3% of E. coli O157, Salmonella, L. monocytogenes, and Campylobacter isolates recovered, respectively. The most frequently observed resistance genes were mphA, aadA, and aphA1 in E. coli O157; blaTEM, tet(B), and strA in Salmonella; penA, ampC, lde, ermB, tet(O), and aadB in L. monocytogenes and blaOXA-61, tet(O), and aadE in Campylobacter. Our results highlight the critical need to address the dissemination of foodborne pathogens and antibiotic resistance in agricultural settings. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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Review

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14 pages, 1800 KiB

Open AccessReview

Antibiotic Resistance of Salmonella Typhimurium Monophasic Variant 1,4,[5],12:i:-in China: A Systematic Review and Meta-Analysis

by Xiaojie Qin, Mingzhe Yang, Hua Cai, Yangtai Liu, Leon Gorris, Muhammad Zohaib Aslam, Kai Jia, Tianmei Sun, Xiang Wang and Qingli Dong

Antibiotics 2022, 11(4), 532; https://doi.org/10.3390/antibiotics11040532 - 16 Apr 2022

Cited by 25 | Viewed by 4082

Abstract

Antibiotic resistance in Salmonella is a global public health problem. Salmonella enterica serovar 1,4,[5],12:i:- (S. 1,4,[5],12:i:-), a monophasic variant of Salmonella Typhmurium, is one of the leading Salmonella serovars in several countries. This study aimed to assess the prevalence of antibiotic resistance to this serovar in China through a systematic review and meta-analysis. Nineteen eligible studies during 2011–2021 were included. A total of 4514 isolates from humans, animals, foods, and the environment were reported, which mainly concerned isolates found in Guangdong, Guangxi, Jiangsu, and Shanghai. A random-effects model was used to estimate the pooled resistance rate of S. 1,4,[5],12:i:-. Rates were found to be very high (values ≥ 75%) for tetracycline, ampicillin, sulfisoxazole, and streptomycin; high (50–75%) for nalidixic acid, amoxicillin–clavulanic acid, and chloramphenicol; and moderate (25–50%) for trimethoprim–sulfamethoxazole, kanamycin, trimethoprim, and gentamicin. The rates of resistance to ciprofloxacin, cefotaxime, ceftriaxone, cefepime, ceftazidime, and colistin were low (values ≤ 25%), but of great concern in terms of their current clinical importance. Furthermore, a high multidrug resistance rate (86%, 95% CI: 78–92%) was present in S. 1,4,[5],12:i:-, with the ASSuT pattern largely dominating. Subgroup analysis results showed that the high heterogeneity of resistance rates was not entirely dependent on isolated sources. Taken together, the severity of antibiotic resistance in S. 1,4,[5],12:i:- urgently requires the rational use of antibiotics in future infection control and antibiotic stewardship programs. Full article

(This article belongs to the Special Issue Antimicrobial Resistance in Food-borne Pathogens)

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