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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Food Microbiology".

Deadline for manuscript submissions: closed (15 February 2024) | Viewed by 21729

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Dr. Toni L. Poole

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Food and Feed Safety Research Unit, Agricultural Research Service, Southern Plains Agricultural Research Center, U.S. Department of Agriculture, 2881 F&B Road, College Station, TX 77845, USA
Interests: antimicrobial resistance
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Special Issue Information

Dear Colleagues,

This Special Issue of Microorganisms addresses antimicrobial resistance (AMR) with regard to foodborne pathogens. There has been an increased prevalence of multidrug-resistant bacterial pathogens that have become a global threat to human and animal health. More recently, the term “One Health” constitutes an approach to health that is based on the understanding that human health is closely linked to a healthy balance between food, animals, and the environment. Some One Health initiatives that include AMR neglect to include animals and the environment. Currently, in agriculture, there is large focus on pre- and post-harvest food production with regard to AMR foodborne pathogens. There are an abundance of niches and reservoirs for AMR foodborne pathogens. In addition to the spread of foodborne pathogens that display AMR, an important means of dissemination involves horizontal transfer of mobile genetic elements harbored by AMR bacteria. Most commonly, this involves broad-host range plasmids that are extrachromosomal genetic elements existing in bacteria. In recent years, a complex reservoir of mobile genetic elements has been elucidated and is referred to as a mobilome. These include transposons, integrons, integrative and conjugative elements, etc. All these mobile elements may provide a rapid means of dissemination at the molecular level.

Dr. Toni L. Poole
Guest Editor

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Keywords

antimicrobial resistance
mobilome
conjugation
conjugative or mobilizable antimicrobial resistance plasmids
whole-genome shotgun (WGS)
sequencing
non-typhoidal Salmonella enterica (NTS)
Escherichia coli
Aeromonas spp.
poultry
fish
livestock production
retail meats and vegetables

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Published Papers (11 papers)

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15 pages, 920 KiB

Open AccessArticle

Genomic Analysis Points to Multiple Genetic Mechanisms for Non-Transformable Campylobacter jejuni ST-50

by Craig T. Parker, David A. Villafuerte, William G. Miller, Steven Huynh, Mary H. Chapman, Zahra Hanafy, James H. Jackson III, Morgan A. Miller and Sophia Kathariou

Microorganisms 2024, 12(2), 327; https://doi.org/10.3390/microorganisms12020327 - 4 Feb 2024

Cited by 1 | Viewed by 1263

Abstract

Campylobacter jejuni and Campylobacter coli are well known for their natural competence, i.e., their capacity for the uptake of naked DNA with subsequent transformation. This study identifies non-transformable C. jejuni and C. coli strains from domestic animals and employs genomic analysis to investigate the strain genotypes and their associated genetic mechanisms. The results reveal genetic associations leading to a non-transformable state, including functional DNase genes from bacteriophages and mutations within the cts-encoded DNA-uptake system, which impact the initial steps of the DNA uptake during natural transformation. Interestingly, all 38 tested C. jejuni ST-50 strains from the United States exhibit a high prevalence of non-transformability, and the strains harbor a variety of these genetic markers. This research emphasizes the role of these genetic markers in hindering the transfer of antimicrobial resistance (AMR) determinants, providing valuable insights into the genetic diversity of Campylobacter. As ST-50 is a major clone of C. jejuni globally, we additionally determined the prevalence of the genetic markers for non-transformability among C. jejuni ST-50 from different regions of the world, revealing distinct patterns of evolution and a strong selective pressure on the loss of competence in ST-50 strains, particularly in the agricultural environment in the United States. Our findings contribute to a comprehensive understanding of genetic exchange mechanisms within Campylobacter strains, and their implications for antimicrobial resistance dissemination and evolutionary pathways within specific lineages. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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18 pages, 2254 KiB

Open AccessArticle

Multiplex Real-Time PCR for the Detection of Tetracycline, Ciprofloxacin, and Erythromycin Resistance Determinants from Human and Foodborne Campylobacter jejuni and Campylobacter coli

by Véronique Zeller-Péronnet, Nancy Bretschneider, Johanna Lausch, Nadera Hanifi, Melanie Pavlovic, Michael Zarske, Huong Quynh Luu, Ulrich Busch, Kerstin Stingl and Ingrid Huber

Microorganisms 2023, 11(12), 2927; https://doi.org/10.3390/microorganisms11122927 - 6 Dec 2023

Viewed by 1481

Abstract

Campylobacter jejuni and Campylobacter coli are the predominant thermophilic species responsible for foodborne gastroenteritis worldwide. Elevated resistance to certain antibiotics was observed due to antimicrobial therapy in farm animals and humans, while reduced antimicrobial usage partially reduced antibiotic resistance. Monitoring the antimicrobial resistance demonstrated a substantial fraction of multi-resistant isolates, indicating the necessity of reliable tools for their detection. In this study, resistance determinants in 129 German and 21 Vietnamese isolates were selected to establish a novel multiplex real-time PCR (qPCR), facilitating the simultaneous detection of four resistance determinants. These comprised tet(O) gene variants associated with tetracycline resistance, point mutations GyrA_T86I and GyrA_T86V associated with ciprofloxacin resistance, and the erm(B) gene together with the point mutation A2075G in the 23S rRNA gene, associated with erythromycin resistance. Moreover, the performance of the qPCR assay was evaluated by comparing the results of qPCR to phenotypic antimicrobial resistance profiles, obtained with standardized EUCAMP3 microdilution panel, which showed 100% similarity (inclusivity and exclusivity). Variation in measurement methods, including qPCR machines and master mixes showed robustness, essential for laboratories. The assay can be used for the rapid detection of resistance determinants, and is beneficial for monitoring the spread of antibiotic resistance in C. jejuni and C. coli. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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17 pages, 5420 KiB

Open AccessArticle

Two-Dose Ceftiofur Treatment Increases Cephamycinase Gene Quantities and Fecal Microbiome Diversity in Dairy Cows Diagnosed with Metritis

by Claudia Ossa-Trujillo, Ethan A. Taylor, Fatima Sarwar, Javier Vinasco, Ellen R. Jordan, Jose A. García Buitrago, G. Robert Hagevoort, Sara D. Lawhon, Juan M. Piñeiro, Jessica Galloway-Peña, Keri N. Norman and Harvey Morgan Scott

Microorganisms 2023, 11(11), 2728; https://doi.org/10.3390/microorganisms11112728 - 8 Nov 2023

Cited by 1 | Viewed by 2056

Abstract

Antimicrobial resistance is a significant concern worldwide; meanwhile, the impact of 3rd generation cephalosporin (3GC) antibiotics on the microbial communities of cattle and resistance within these communities is largely unknown. The objectives of this study were to determine the effects of two-dose ceftiofur crystalline-free acid (2-CCFA) treatment on the fecal microbiota and on the quantities of second-and third-generation cephalosporin, fluoroquinolone, and macrolide resistance genes in Holstein-Friesian dairy cows in the southwestern United States. Across three dairy farms, 124 matched pairs of cows were enrolled in a longitudinal study. Following the product label regimen, CCFA was administered on days 0 and 3 to cows diagnosed with postpartum metritis. Healthy cows were pair-matched based on lactation number and calving date. Fecal samples were collected on days 0, 6, and 16 and pooled in groups of 4 (n = 192) by farm, day, and treatment group for community DNA extraction. The characterization of community DNA included real-time PCR (qPCR) to quantify the following antibiotic resistance genes: bla_CMY-2, bla_CTX-M, mphA, qnrB19, and the highly conserved 16S rRNA back-calculated to gene copies per gram of feces. Additionally, 16S rRNA amplicon sequencing and metagenomics analyses were used to determine differences in bacterial community composition by treatment, day, and farm. Overall, bla_CMY-2 gene copies per gram of feces increased significantly (p ≤ 0.05) in the treated group compared to the untreated group on day 6 and remained elevated on day 16. However, bla_CTX-M, mphA, and qnrB19 gene quantities did not differ significantly (p ≥ 0.05) between treatment groups, days, or farms, suggesting a cephamycinase-specific enhancement in cows on these farms. Perhaps unexpectedly, 16S rRNA amplicon metagenomic analyses showed that the fecal bacterial communities from treated animals on day 6 had significantly greater (p ≤ 0.05) alpha and beta diversity than the untreated group. Two-dose ceftiofur treatment in dairy cows with metritis elevates cephamycinase gene quantities among all fecal bacteria while paradoxically increasing microbial diversity. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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16 pages, 1270 KiB

Open AccessArticle

Monophasic Variant of Salmonella Typhimurium 4,[5],12:i:- (ACSSuGmTmpSxt Type) Outbreak in Central Italy Linked to the Consumption of a Roasted Pork Product (Porchetta)

by Maira Napoleoni, Laura Villa, Lisa Barco, Claudia Lucarelli, Alessia Tiengo, Giulia Baggio, Anna Maria Dionisi, Antonio Angellotti, Ezio Ferretti, Simonetta Ruggeri, Monica Staffolani, Elena Rocchegiani, Valentina Silenzi, Benedetto Morandi and Giuliana Blasi

Microorganisms 2023, 11(10), 2567; https://doi.org/10.3390/microorganisms11102567 - 15 Oct 2023

Cited by 4 | Viewed by 2149

Abstract

The monophasic variant of S. Typhimurium 4,[5],12:i:- (MVST) is the third most commonly reported Salmonella serovar involved in human infections (8.8%) in the EU and ranks after S. Enteritidis (54.6%) and S. Typhimurium (11.4%). In Italy, in contrast, the MVST has achieved peculiar epidemiological and ecological success which has allowed it to be, since 2011, the serovar most frequently isolated from humans. In the summer of 2022, a foodborne outbreak of the MVST involving 63 people occurred in the Marche Region (Central Italy). A common food exposure source among some human cases was a roasted, ready-to-eat (RTE) pork product, porchetta, which is a typical product of Central Italy. This paper describes the results of investigations conducted to clarify this outbreak. The porchetta was produced by a local manufacturing plant and distributed to at least two local retail stores, one of which was the retail outlet for the manufacturing plant. The MVST was isolated from surface samples collected at the porchetta manufacturing plant and at both local retail stores via bacterial analysis, and the porchetta sampled at one store contained the MVST. These data confirm this type of RTE pork product can be a source of Salmonella infection in humans. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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18 pages, 1084 KiB

Open AccessArticle

First Report and Characterization of the mcr-1 Positive Multidrug-Resistant Escherichia coli Strain Isolated from Pigs in Croatia

by Gordan Kompes, Sanja Duvnjak, Irena Reil, Rene S. Hendriksen, Lauge Holm Sørensen, Maja Zdelar-Tuk, Boris Habrun, Luka Cvetnić, Antonela Bagarić and Silvio Špičić

Microorganisms 2023, 11(10), 2442; https://doi.org/10.3390/microorganisms11102442 - 28 Sep 2023

Viewed by 1492

Abstract

The emergence and rapid spread of the plasmid-mediated colistin-resistant mcr-1 gene introduced a serious threat to public health. In 2021, a multi-drug resistant, mcr-1 positive Escherichia coli EC1945 strain, was isolated from pig caecal content in Croatia. Antimicrobial susceptibility testing and whole genome sequencing were performed. Bioinformatics tools were used to determine the presence of resistance genes, plasmid Inc groups, serotype, sequence type, virulence factors, and plasmid reconstruction. The isolated strain showed phenotypic and genotypic resistance to nine antimicrobial classes. It was resistant to colistin, gentamicin, ampicillin, cefepime, cefotaxime, ceftazidime, sulfamethoxazole, chloramphenicol, nalidixic acid, and ciprofloxacin. Antimicrobial resistance genes included mcr-1, bla_TEM-1B, bla_CTX-M-1, aac(3)-IId, aph(3’)-Ia, aadA5, sul2, catA1, gyrA (S83L, D87N), and parC (A56T, S80I). The mcr-1 gene was located within the conjugative IncX4 plasmid. IncI1, IncFIB, and IncFII plasmids were also detected. The isolate also harbored 14 virulence genes and was classified as ST744 and O101:H10. ST744 is a member of the ST10 group which includes commensal, extraintestinal pathogenic E. coli isolates that play a crucial role as a reservoir of genes. Further efforts are needed to identify mcr-1-carrying E. coli isolates in Croatia, especially in food-producing animals to identify such gene reservoirs. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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10 pages, 462 KiB

Open AccessArticle

First Report of Campylobacter jejuni Strains Belonging to ST-21 Clonal Complex Isolated from Human, Poultry and Wild Birds in Croatia: Antimicrobial Resistance and Genetic Distance

by Silvija Šoprek, Josip Ujević, Gordan Kompes, Luka Jurinović and Arjana Tambić Andrašević

Microorganisms 2023, 11(8), 1884; https://doi.org/10.3390/microorganisms11081884 - 26 Jul 2023

Cited by 1 | Viewed by 1328

Abstract

In the era of growing antimicrobial resistance, a threat affecting humans, endangering animals, as well as livelihoods and food security worldwide, we wanted to find possible explanations for its continuous spread from a new perspective. The ubiquity of resistance genes requires a One Health approach to finding the explanations for continuous AMR spread. The natural transformability of Campylobacter jejuni, its high incidence of infections, and emerging resistance worldwide inspired us to choose C. jejuni ST-21CC to be our pathogen for analyzing its contribution and connection to the cycle of AMR dissemination. ST-21CC is known as a generalist among humans and broilers, the most prevalent lineage worldwide, but it is rarely found in wild birds. Emerging in wild birds, genetic relatedness and similar resistance profiles were expected. We analyzed 23 Croatian C. jejuni strains belonging specifically to ST-21CC from humans, broilers, and wild birds. The genomic data obtained through whole genome sequencing and phenotypic susceptibility data of strains were compared. Our findings suggest high fluoroquinolone resistance in ST-21CC strains, with more diverse genetic backgrounds in wild birds. Intriguing were three isolates of ST-822 (from human and storks), sharing a similar genetic fingerprint. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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18 pages, 1844 KiB

Open AccessArticle

Occurrence and Patterns of Enterotoxin Genes, spa Types and Antimicrobial Resistance Patterns in Staphylococcus aureus in Food and Food Contact Surfaces in Singapore

by Ker Li Lim, Wei Ching Khor, Kar Hui Ong, Lois Timothy and Kyaw Thu Aung

Microorganisms 2023, 11(7), 1785; https://doi.org/10.3390/microorganisms11071785 - 10 Jul 2023

Cited by 6 | Viewed by 2445

Abstract

Staphylococcus aureus contamination of food and food contact surfaces is a public health concern given its virulent and antimicrobial-resistant properties worldwide. In this study, a total of 181 MSSA isolates were analyzed for SE genes, antimicrobial resistance patterns, and spa types. Overall, 24.9% of isolates were positive for SE gene detection, with sea being the most prevalent classical SE (18.8%). The most predominant sample sources for SE gene contamination were hand swabs for sea (6/48), meat dishes for seb (3/14) and seafood dishes for sec (2/24). Antimicrobial resistance was also observed at relatively high frequencies for the clinically important antibiotics penicillin G and ampicillin (both 54.7%), followed by tetracycline (14.9%) and azithromycin (8.8%). In addition, characterization of spa types revealed spa type t5078 to be the most predominant (40.3%), with significant associations between spa types t127 and t5521 and the sea gene. This study offers insights into the enterotoxin gene and antimicrobial resistance profiles of S. aureus in cooked or ready-to-eat food to inform future surveillance and epidemiological studies. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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11 pages, 298 KiB

Open AccessArticle

Antimicrobial Resistance of Campylobacter coli Isolated from Caecal Samples of Fattening Pigs at Slaughter

by Triin Tedersoo, Mati Roasto, Mihkel Mäesaar, Maria Fredriksson-Ahomaa and Kadrin Meremäe

Microorganisms 2023, 11(6), 1540; https://doi.org/10.3390/microorganisms11061540 - 9 Jun 2023

Cited by 3 | Viewed by 1582

Abstract

Pigs are known as the main Campylobacter coli reservoirs. Campylobacteriosis, the most commonly reported gastrointestinal disease in humans, is mainly caused by the consumption of poultry meat, and little is known about the role of pork. Pigs are often associated with C. coli, including antimicrobial-resistant isolates. Therefore, the entire pork production chain must be considered as an important source of antimicrobial-resistant C. coli. This study aimed to determine the antimicrobial resistance of Campylobacter spp. isolated from caecal samples of fattening pigs at the Estonian slaughterhouse level over a five-year period. The proportion of Campylobacter-positive caecal samples was 52%. All Campylobacter isolates were identified as C. coli. A high proportion of the isolates were resistant to most of the studied antimicrobials. The resistance to streptomycin, tetracycline, ciprofloxacin and nalidixic acid was 74.8%, 54.4%, 34.4% and 31.9%, respectively. In addition, a high proportion (15.1%) of the isolates were multidrug-resistant and, in total, 93.3% were resistant to at least one antimicrobial. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

13 pages, 328 KiB

Open AccessArticle

Defined Pig Microbiota with a Potential Protective Effect against Infection with Salmonella Typhimurium

by Kristyna Horvathova, Nikol Modrackova, Igor Splichal, Alla Splichalova, Ahmad Amin, Eugenio Ingribelli, Jiri Killer, Ivo Doskocil, Radko Pechar, Tereza Kodesova and Eva Vlkova

Microorganisms 2023, 11(4), 1007; https://doi.org/10.3390/microorganisms11041007 - 12 Apr 2023

Cited by 4 | Viewed by 2410

Abstract

A balanced microbiota is a main prerequisite for the host’s health. The aim of the present work was to develop defined pig microbiota (DPM) with the potential ability to protect piglets against infection with Salmonella Typhimurium, which causes enterocolitis. A total of 284 bacterial strains were isolated from the colon and fecal samples of wild and domestic pigs or piglets using selective and nonselective cultivation media. Isolates belonging to 47 species from 11 different genera were identified by MALDI-TOF mass spectrometry (MALDI-TOF MS). The bacterial strains for the DPM were selected for anti-Salmonella activity, ability to aggregate, adherence to epithelial cells, and to be bile and acid tolerant. The selected combination of 9 strains was identified by sequencing of the 16S rRNA gene as Bacillus sp., Bifidobacterium animalis subsp. lactis, B. porcinum, Clostridium sporogenes, Lactobacillus amylovorus, L. paracasei subsp. tolerans, Limosilactobacillus reuteri subsp. suis, and Limosilactobacillus reuteri (two strains) did not show mutual inhibition, and the mixture was stable under freezing for at least 6 months. Moreover, strains were classified as safe without pathogenic phenotype and resistance to antibiotics. Future experiments with Salmonella-infected piglets are needed to test the protective effect of the developed DPM. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

14 pages, 969 KiB

Open AccessArticle

In-Package Atmospheric Cold Plasma Treatment and Storage Effects on Membrane Integrity, Oxidative Stress, and Esterase Activity of Listeria monocytogenes

by Barun Yadav and M. S. Roopesh

Microorganisms 2023, 11(3), 682; https://doi.org/10.3390/microorganisms11030682 - 7 Mar 2023

Viewed by 2043

Abstract

Atmospheric cold plasma (ACP) treatment can reduce bacterial pathogens in foods. Additional reduction in bacterial cells during storage after ACP treatment was previously reported. The underlying mechanisms of bacterial inactivation during ACP treatment and post-treatment storage need to be understood. This study investigated the changes in the morpho-physiological status of Listeria monocytogenes on ham surfaces after post-ACP-treatment storage of 1 h, 24 h, and 7 days at 4 °C. The membrane integrity, intracellular oxidative stress, and esterase activity of L. monocytogenes were evaluated by flow cytometry. L. monocytogenes cells were under high oxidative stress conditions with slightly permeabilized membranes after 1 h of post-ACP-treatment storage according to the flow cytometry data. During the extended storage of 24 h, the percentage of cells with a slightly permeabilized membrane increased; subsequently, the percentage of cells with intact membranes decreased. The percentage of L. monocytogenes cells with intact membranes decreased to <5% with a treatment time of 10 min and after 7 days of post-treatment storage. In addition, the percentage of L. monocytogenes cells under oxidation stress decreased to <1%, whereas the percentage of cells with completely permeabilized membranes increased to more than 90% for samples treated with ACP for 10 min and 7 days of post-treatment storage. With increased ACP treatment time, for 1 h stored samples, the percentage of cells with active esterase and slightly permeabilized membranes increased. However, during the extended post-treatment storage of 7 days, the percentage of cells with active esterase and slightly permeabilized membranes decreased to below 1%. At the same time, the percentage of cells with permeabilized membrane increased to more than 92% with an increase in ACP treatment time of 10 min. In conclusion, the higher inactivation after 24 h and 7 days post-ACP-treatment storage compared to 1 h stored samples correlated with the loss of esterase activity and membrane integrity of L. monocytogenes cells. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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Review

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24 pages, 819 KiB

Open AccessReview

Foodborne Microbial Communities as Potential Reservoirs of Antimicrobial Resistance Genes for Pathogens: A Critical Review of the Recent Literature

by Paola Zinno, Giuditta Perozzi and Chiara Devirgiliis

Microorganisms 2023, 11(7), 1696; https://doi.org/10.3390/microorganisms11071696 - 29 Jun 2023

Cited by 5 | Viewed by 2008

Abstract

Antimicrobial resistance (AMR) is a global and increasing threat to human health. Several genetic determinants of AMR are found in environmental reservoirs, including bacteria naturally associated with widely consumed fermented foods. Through the food chain, these bacteria can reach the gut, where horizontal gene transfer (HGT) can occur within the complex and populated microbial environment. Numerous studies on this topic have been published over the past decades, but a conclusive picture of the potential impact of the non-pathogenic foodborne microbial reservoir on the spread of AMR to human pathogens has not yet emerged. This review critically evaluates a comprehensive list of recent experimental studies reporting the isolation of AMR bacteria associated with fermented foods, focusing on those reporting HGT events, which represent the main driver of AMR spread within and between different bacterial communities. Overall, our analysis points to the methodological heterogeneity as a major weakness impairing determination or a causal relation between the presence of AMR determinants within the foodborne microbial reservoir and their transmission to human pathogens. The aim is therefore to highlight the main gaps and needs to better standardize future studies addressing the potential role of non-pathogenic bacteria in the spread of AMR. Full article

(This article belongs to the Special Issue Foodborne Pathogens and Antimicrobial Resistance)

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