Antibiotic Resistance and Virulence Factors of Bacteria Isolated from Food

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

Deadline for manuscript submissions: 31 July 2024 | Viewed by 10658

Special Issue Editors


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Guest Editor
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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Guest Editor
Department of Industrial and Food Microbiology, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland
Interests: antibiotic resistance; pathogens; food safety; food processing; food analysis

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Guest Editor
Department of Industrial and Food Microbiology, Faculty of Food Science, University of Warmia and Mazury, Plac Cieszyński 1, 10-726 Olsztyn, Poland
Interests: food safety in the production process; food microbiology; the assessment of antibiotic resistance; enterotoxicity and virulence factors of staphylococci (mainly S. aureus) isolated from food; milk and dairy products; transfer of genes

Special Issue Information

Dear Colleagues,

Food products are a source of many group of opportunistic and/or pathogenic microorganisms. Antimicrobial resistance is one of the biggest threats to the global health, food security and development today. It is worth emphasizing, that food products are even more recognized as important carrier for the transfer of antibiotic-resistant bacteria and antimicrobial resistance genes. Virulence factors are important for microbial pathogenesis, which factors include. secreted products such as toxins, enzymes, exopolysaccharides, but also cell surface structures like capsules, lipopolysaccharides, glycoproteins and lipoproteins. As food microbiota, a many group of bacteria can transfer antibiotic resistance genes and virulence factors to other microorganisms present in food, therefore the food chain may be potential source of transmission of virulent strains. Nowadays it is significant to continue research aimed to understand the microbiology, virulence and antimicrobial resistance of bacteria isolated from food. Therefore, we encourage Authors to submit review article or original research articles related to these topics. We aim to present manuscripts that provide new insights into the role of virulence factors or antibiotic resistance determinants among the opportunistic, or pathogenic microorganisms isolated from food.

Dr. Wioleta Chajȩcka-Wierzchowska
Prof. Dr. Anna Zadernowska
Dr. Joanna Gajewska
Guest Editors

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Keywords

  • antimicrobial resistance
  • food microbiology
  • food chain
  • virulence
  • biofilm
  • antimicrobial resistance mechanisms

Published Papers (6 papers)

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Research

15 pages, 805 KiB  
Article
Antibiotic Resistance Profile of Salmonella sp. Isolates from Commercial Laying Hen Farms in Central-Western Brazil
by Dunya Mara Cardoso Moraes, Ana Maria De Souza Almeida, Maria Auxiliadora Andrade, Eduardo de Paula Nascente, Sabrina Castilho Duarte, Iolanda Aparecida Nunes, Valéria De Sá Jayme and Cíntia Minafra
Microorganisms 2024, 12(4), 669; https://doi.org/10.3390/microorganisms12040669 - 27 Mar 2024
Viewed by 652
Abstract
Microbial resistance to antibiotics poses a significant threat to both human and animal health, necessitating international efforts to mitigate this issue. This study aimed to assess the resistance profiles of Salmonella sp. isolates and identify the presence of intl1, sul1, and [...] Read more.
Microbial resistance to antibiotics poses a significant threat to both human and animal health, necessitating international efforts to mitigate this issue. This study aimed to assess the resistance profiles of Salmonella sp. isolates and identify the presence of intl1, sul1, and blaTEM resistance genes within antigenically characterized isolates, including Agona, Livingstone, Cerro, Schwarzengrund, Salmonella enterica subsp. enterica serotype O:4.5, Anatum, Enteritidis, Johannesburg, Corvallis, and Senftenberg. These isolates underwent susceptibility testing against 14 antibiotics. The highest resistance percentages were noted for sulfamethoxazole (91%), sulfonamides (51%), and ceftiofur (28.9%), while no resistance was observed for ciprofloxacin. Salmonella Johannesburg and Salmonella Corvallis showed resistance to one antibiotic, whereas other serovars were resistant to at least two. Salmonella Schwarzengrund exhibited resistance to 13 antibiotics. The intl1 gene was detected in six out of the ten serovars, and the sul1 gene in three, always co-occurring with intl1. The blaTEM gene was not identified. Our findings highlight the risk posed by the detected multiple resistances and genes to animal, human, and environmental health. The multidrug resistance, especially to third-generation cephalosporins and fluoroquinolones, highlights the need for stringent monitoring of Salmonella in laying hens. The potential of the environment, humans, eggs, and their products to act as vectors for antibiotic resistance represents a significant concern for One Health. Full article
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16 pages, 2182 KiB  
Article
Characterization of Cronobacter sakazakii and Cronobacter malonaticus Strains Isolated from Powdered Dairy Products Intended for Consumption by Adults and Older Adults
by Julio Parra-Flores, Fernanda Flores-Soto, Carolina Flores-Balboa, María P. Alarcón-Lavín, Adriana Cabal-Rosel, Beatriz Daza-Prieto, Burkhard Springer, Ariadnna Cruz-Córdova, José Leiva-Caro, Stephen Forsythe and Werner Ruppitsch
Microorganisms 2023, 11(12), 2841; https://doi.org/10.3390/microorganisms11122841 - 23 Nov 2023
Viewed by 1046
Abstract
The objective of this study was to characterize Cronobacter spp. and related organisms isolated from powder dairy products intended for consumption by adults and older adults using whole-genome sequencing (WGS), and to identify genes and traits that encode antibiotic resistance and virulence. Virulence [...] Read more.
The objective of this study was to characterize Cronobacter spp. and related organisms isolated from powder dairy products intended for consumption by adults and older adults using whole-genome sequencing (WGS), and to identify genes and traits that encode antibiotic resistance and virulence. Virulence (VGs) and antibiotic resistance genes (ARGs) were detected with the Comprehensive Antibiotic Resistance Database (CARD) platform, ResFinder, and MOB-suite tools. Susceptibility testing was performed using disk diffusion. Five presumptive strains of Cronobacter spp. were identified by MALDI–TOF MS and ribosomal MLST. Three C. sakazakii strains were of the clinical pathovar ST1, one was ST31, and the remaining isolate was C. malonaticus ST60. In addition, Franconibacter helveticus ST345 was identified. The C. sakazakii ST1 strains were further distinguished using core genome MLST based on 2831 loci. Moreover, 100% of the strains were resistant to cefalotin, 75% to ampicillin, and 50% to amikacin. The C. sakazakii ST1 strains were multiresistant (MDR) to four antibiotics. Additionally, all the strains adhered to the N1E-115 cell line, and two invaded it. Eighteen ARGs mainly involved in antibiotic target alteration and antibiotic efflux were detected. Thirty VGs were detected and clustered as flagellar proteins, outer membrane proteins, chemotaxis, hemolysins, and genes involved in metabolism and stress. The pESA3, pSP291-1, and pCMA1 plasmids were detected, and the prevalent mobile genetic elements (MGEs) were ISEsa1, ISEc52, and IS26. The isolates of C. sakazakii and C. malonaticus exhibited multiresistance to antibiotics, harbored genes encoding various antibiotic resistance proteins, and various virulence factors. Consequently, these contaminated powdered dairy products pose a risk to the health of hypersensitive adults. Full article
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22 pages, 2682 KiB  
Article
Viability and Virulence of Listeria monocytogenes in Poultry
by Sarah Panera-Martínez, Rosa Capita, Camino García-Fernández and Carlos Alonso-Calleja
Microorganisms 2023, 11(9), 2232; https://doi.org/10.3390/microorganisms11092232 - 04 Sep 2023
Viewed by 1213
Abstract
The prevalence of Listeria monocytogenes in 30 samples of poultry was determined using culture-dependent (isolation on OCLA and confirmation by conventional polymerase chain reaction -PCR-, OCLA&PCR) and culture-independent (real-time polymerase chain reaction, q-PCR) methods. L. monocytogenes was detected in 15 samples (50.0%) by [...] Read more.
The prevalence of Listeria monocytogenes in 30 samples of poultry was determined using culture-dependent (isolation on OCLA and confirmation by conventional polymerase chain reaction -PCR-, OCLA&PCR) and culture-independent (real-time polymerase chain reaction, q-PCR) methods. L. monocytogenes was detected in 15 samples (50.0%) by OCLA&PCR and in 20 (66.7%) by q-PCR. The concentrations (log10 cfu/g) of L. monocytogenes (q-PCR) ranged from 2.40 to 5.22 (total cells) and from <2.15 to 3.93 (viable cells). The two methods, q-PCR using a viability marker (v-PCR) and OCLA&PCR (gold standard), were compared for their capacity to detect viable cells of L. monocytogenes, with the potential to cause human disease. The values for sensitivity, specificity and efficiency of the v-PCR were 100%, 66.7% and 83.3%, respectively. The agreement between the two methods (kappa coefficient) was 0.67. The presence of nine virulence genes (hlyA, actA, inlB, inlA, inlC, inlJ, prfA, plcA and iap) was studied in 45 L. monocytogenes isolates (three from each positive sample) using PCR. All the strains harbored between six and nine virulence genes. Fifteen isolates (33.3% of the total) did not show the potential to form biofilm on a polystyrene surface, as determined by a crystal violet assay. The remaining strains were classified as weak (23 isolates, 51.1% of the total), moderate (one isolate, 2.2%) or strong (six isolates, 13.3%) biofilm producers. The strains were tested for susceptibility to a panel of 15 antibiotics. An average of 5.11 ± 1.30 resistances per isolate was observed. When the values for resistance and for reduced susceptibility were taken jointly, this figure rose to 6.91 ± 1.59. There was a prevalence of resistance or reduced susceptibility of more than 50.0% for oxacillin, cefoxitin, cefotaxime, cefepime ciprofloxacin, enrofloxacin and nitrofurantoin. For the remaining antibiotics tested, the corresponding values ranged from 0.0% for chloramphenicol to 48.9% for rifampicin. The high prevalence and level of L. monocytogenes with numerous virulence factors in poultry underline how crucial it is to follow correct hygiene procedures during the processing of this foodstuff in order to reduce the risk of human listeriosis. Full article
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12 pages, 562 KiB  
Article
High Levels of Antibiotic Resistance in MDR-Strong Biofilm-Forming Salmonella Typhimurium ST34 in Southern China
by Yuan Gao, Kaifeng Chen, Runshan Lin, Xuebin Xu, Fengxiang Xu, Qijie Lin, Yaping Hu, Hongxia Zhang, Jianmin Zhang, Ming Liao and Xiaoyun Qu
Microorganisms 2023, 11(8), 2005; https://doi.org/10.3390/microorganisms11082005 - 03 Aug 2023
Viewed by 874
Abstract
Salmonella enterica subsp. enterica serovar Typhimurium (S. typhimurium) is an important zoonotic pathogen with important public health significance. To understand S. typhimurium’s epidemiological characteristics in China, multi-locus sequence typing, biofilm-forming ability, antimicrobial susceptibility testing, and resistant genes of isolates from [...] Read more.
Salmonella enterica subsp. enterica serovar Typhimurium (S. typhimurium) is an important zoonotic pathogen with important public health significance. To understand S. typhimurium’s epidemiological characteristics in China, multi-locus sequence typing, biofilm-forming ability, antimicrobial susceptibility testing, and resistant genes of isolates from different regions and sources (human, food) were investigated. Among them, ST34 accounted for 82.4% (243/295), with ST19 ranking second (15.9%; 47/295). ST34 exhibited higher resistance levels than ST19 (p < 0.05). All colistin, carbapenem, and ciprofloxacin-resistant strains were ST34, as were most cephalosporin-resistant strains (88.9%; 32/36). Overall, 91.4% (222/243) ST34 isolates were shown to have multidrug resistance (MDR), while 53.2% (25/47) ST19 isolates were (p < 0.05). Notably, 97.8% (45/46) of the MDR-ACSSuT (resistance to Ampicillin, Chloramphenicol, Streptomycin, Sulfamethoxazole, and Tetracycline) isolates were ST34, among which 69.6% (32/46) of ST34 isolates were of human origin, while 30.4% (14/46) were derived from food (p < 0.05). Moreover, 88.48% (215/243) ST34 showed moderate to strong biofilm-forming ability compared with 10.9% (5/46) ST19 isolates (p < 0.01). This study revealed the emergence of high-level antibiotic resistance S. typhimurium ST34 with strong biofilm-forming ability, posing concerns for public health safety. Full article
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13 pages, 2507 KiB  
Article
Bacillus cereus in the Artisanal Cheese Production Chain in Southwestern Mexico
by Itzel-Maralhi Cruz-Facundo, Jeiry Toribio-Jiménez, Natividad Castro-Alarcón, Marco-Antonio Leyva-Vázquez, Hugo-Alberto Rodríguez-Ruíz, José-Humberto Pérez-Olais, Roberto Adame-Gómez, Elvia Rodríguez-Bataz, Joel Reyes-Roldán, Salvador Muñoz-Barrios and Arturo Ramírez-Peralta
Microorganisms 2023, 11(5), 1290; https://doi.org/10.3390/microorganisms11051290 - 15 May 2023
Cited by 2 | Viewed by 1723
Abstract
Background: Bacillus cereus is associated with milk, dairy product, and dairy farm contamination. The aim of this study was to characterize strains of B. cereus in the small-scale artisanal cheese production chain in southwestern Mexico. Methods: 130 samples were collected. B. cereus isolation [...] Read more.
Background: Bacillus cereus is associated with milk, dairy product, and dairy farm contamination. The aim of this study was to characterize strains of B. cereus in the small-scale artisanal cheese production chain in southwestern Mexico. Methods: 130 samples were collected. B. cereus isolation was performed on Mannitol Egg Yolk Polymyxin (MYP) agar. Genotyping, enterotoxigenic profile, and determination of genes involved in the formation of B. cereus biofilm were performed by PCR. An antimicrobial susceptibility test was made by broth microdilution assay. The phylogenetic analysis was performed by amplification and sequencing of 16s rRNA. Results: B. cereus sensu lato was isolated and molecularly identified in 16 samples and B. cereus sensu stricto (B. cereus) was the most frequently isolated and identified species (81.25%). Of all the isolated B. cereus sensu lato strains, 93.75% presented at least one gene for some diarrheagenic toxins, 87.5% formed biofilms, and 18.75% were amylolytic. All B. cereus sensu lato strains were resistant to beta-lactams and folate inhibitors. A close phylogenetic relationship between isolates was found between the cheese isolates and the air isolates. Conclusions: Strains of B. cereus sensu lato were found in small-scale artisanal cheeses on a farm in southwestern Mexico. Full article
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11 pages, 1602 KiB  
Article
Prevalence and Antibiotic Resistance of Bacillus sp. Isolated from Raw Milk
by Patryk Adamski, Zuzanna Byczkowska-Rostkowska, Joanna Gajewska, Arkadiusz Józef Zakrzewski and Lucyna Kłębukowska
Microorganisms 2023, 11(4), 1065; https://doi.org/10.3390/microorganisms11041065 - 19 Apr 2023
Cited by 9 | Viewed by 4378
Abstract
Milk, due to its diversity in terms of its nutritional content, is an important element of the human diet, as well as a good medium for the development of bacteria. The genus Bacillus contains ubiquitous aerobic, rod-shaped, endospore-producing gram-positive bacteria. Representatives of the [...] Read more.
Milk, due to its diversity in terms of its nutritional content, is an important element of the human diet, as well as a good medium for the development of bacteria. The genus Bacillus contains ubiquitous aerobic, rod-shaped, endospore-producing gram-positive bacteria. Representatives of the Bacillus cereus group and the Bacillus subtilis group contribute to shortening the shelf life of milk and dairy products by degrading milk components and its additives. They also produce a number of heat-stable toxins and can cause a number of ailments, mainly in the digestive system. The aim of this research was to identify Bacillus sp. strains isolated from raw milk and to determine their antibiotic resistance. Strains isolated from raw milk samples (n = 45) were identified by MALDI-TOF MS. Ninety strains of Bacillus sp. were identified, for which the antibiotic resistance phenotype was determined. A total of 90 strains of Bacillus were classified in five groups (the Bacillus cereus group (n = 35), B. licheniformis (n = 7), the B. subtilis group (n = 29), B. pumilus (n = 16), and Bacillus sp. (n = 3). All isolates were susceptible to chloramphenicol and meropenem. The antibiotic resistance profiles of the tested groups of Bacillus spp. differed from each other, which is of particular concern in relation to multidrug-resistant representatives of the B. cereus group resistant to cefotaxime (94.29%), ampicillin (88.57%), rifampicin (80%), and norfloxacin (65.71%). Our study provides data on the prevalence and antibiotic sensitivity of Bacillus sp. In raw milk, suggesting a potential risk to health and the dairy industry. Full article
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