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Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach

Escherichia coli is a key indicator of food hygiene, and its monitoring in meat samples points to the potential presence of antimicrobial-resistant strains capable of causing infections in humans, encompassing resistance profiles categorized as serious threats by the Centers for Disease Control and...

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Autores principales: Menck-Costa, Maísa Fabiana, Baptista, Ana Angelita Sampaio, Sanches, Matheus Silva, dos Santos, Beatriz Queiroz, Cicero, Claudinéia Emidio, Kitagawa, Hellen Yukari, Justino, Larissa, Medeiros, Leonardo Pinto, de Souza, Marielen, Rocha, Sergio Paulo Dejato, Nakazato, Gerson, Kobayashi, Renata Katsuko Takayama
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10672981/
https://www.ncbi.nlm.nih.gov/pubmed/38004724
http://dx.doi.org/10.3390/microorganisms11112712
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author Menck-Costa, Maísa Fabiana
Baptista, Ana Angelita Sampaio
Sanches, Matheus Silva
dos Santos, Beatriz Queiroz
Cicero, Claudinéia Emidio
Kitagawa, Hellen Yukari
Justino, Larissa
Medeiros, Leonardo Pinto
de Souza, Marielen
Rocha, Sergio Paulo Dejato
Nakazato, Gerson
Kobayashi, Renata Katsuko Takayama
author_facet Menck-Costa, Maísa Fabiana
Baptista, Ana Angelita Sampaio
Sanches, Matheus Silva
dos Santos, Beatriz Queiroz
Cicero, Claudinéia Emidio
Kitagawa, Hellen Yukari
Justino, Larissa
Medeiros, Leonardo Pinto
de Souza, Marielen
Rocha, Sergio Paulo Dejato
Nakazato, Gerson
Kobayashi, Renata Katsuko Takayama
author_sort Menck-Costa, Maísa Fabiana
collection PubMed
description Escherichia coli is a key indicator of food hygiene, and its monitoring in meat samples points to the potential presence of antimicrobial-resistant strains capable of causing infections in humans, encompassing resistance profiles categorized as serious threats by the Centers for Disease Control and Prevention (CDC), such as Extended-Spectrum Beta-Lactamase (ESBL)—a problem with consequences for animal, human, and environmental health. The objective of the present work was to isolate and characterize ESBL-producing E. coli strains from poultry, pork, and beef meat samples, with a characterization of their virulence and antimicrobial resistance profiles. A total of 450 meat samples (150 chicken, 150 beef, and 150 pork) were obtained from supermarkets and subsequently cultured in medium supplemented with cefotaxime. The isolated colonies were characterized biochemically, followed by antibiogram testing using the disk diffusion technique. Further classification involved biofilm formation and the presence of antimicrobial resistance genes (bla(CTX-M), AmpC-type, mcr-1, and fosA3), and virulence genes (eaeA, st, bfpA, lt, stx1, stx2, aggR, iss, ompT, hlyF, iutA, iroN, fyuA, cvaC, and hylA). Statistical analysis was performed via the likelihood-ratio test. In total, 168 strains were obtained, with 73% originating from chicken, 22% from pork, and 17% from beef samples. Notably, strains exhibited greater resistance to tetracycline (51%), ciprofloxacin (46%), and fosfomycin (38%), apart from β-lactams. The detection of antimicrobial resistance in food-isolated strains is noteworthy, underscoring the significance of antimicrobial resistance as a global concern. More than 90% of the strains were biofilm producers, and strains carrying many ExPEC genes were more likely to be biofilm formers (OR 2.42), which increases the problem since the microorganisms have a greater chance of environment persistence and genetic exchange. Regarding molecular characterization, bovine samples showed a higher prevalence of bla(CTX-M-1) (OR 6.52), while chicken strains were more likely to carry the fosA3 gene (OR 2.43, CI 1.17–5.05) and presented between 6 to 8 ExPEC genes (OR 2.5, CI 1.33–5.01) compared to other meat samples. Concerning diarrheagenic E. coli genes, two strains harbored eae. It is important to highlight these strains, as they exhibited both biofilm-forming capacities and multidrug resistance (MDR), potentially enabling colonization in diverse environments and causing infections. In conclusion, this study underscores the presence of β-lactamase-producing E. coli strains, mainly in poultry samples, compared to beef and pork samples. Furthermore, all meat sample strains exhibited many virulence-associated extraintestinal genes, with some strains harboring diarrheagenic E. coli (DEC) genes.
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spelling pubmed-106729812023-11-06 Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach Menck-Costa, Maísa Fabiana Baptista, Ana Angelita Sampaio Sanches, Matheus Silva dos Santos, Beatriz Queiroz Cicero, Claudinéia Emidio Kitagawa, Hellen Yukari Justino, Larissa Medeiros, Leonardo Pinto de Souza, Marielen Rocha, Sergio Paulo Dejato Nakazato, Gerson Kobayashi, Renata Katsuko Takayama Microorganisms Article Escherichia coli is a key indicator of food hygiene, and its monitoring in meat samples points to the potential presence of antimicrobial-resistant strains capable of causing infections in humans, encompassing resistance profiles categorized as serious threats by the Centers for Disease Control and Prevention (CDC), such as Extended-Spectrum Beta-Lactamase (ESBL)—a problem with consequences for animal, human, and environmental health. The objective of the present work was to isolate and characterize ESBL-producing E. coli strains from poultry, pork, and beef meat samples, with a characterization of their virulence and antimicrobial resistance profiles. A total of 450 meat samples (150 chicken, 150 beef, and 150 pork) were obtained from supermarkets and subsequently cultured in medium supplemented with cefotaxime. The isolated colonies were characterized biochemically, followed by antibiogram testing using the disk diffusion technique. Further classification involved biofilm formation and the presence of antimicrobial resistance genes (bla(CTX-M), AmpC-type, mcr-1, and fosA3), and virulence genes (eaeA, st, bfpA, lt, stx1, stx2, aggR, iss, ompT, hlyF, iutA, iroN, fyuA, cvaC, and hylA). Statistical analysis was performed via the likelihood-ratio test. In total, 168 strains were obtained, with 73% originating from chicken, 22% from pork, and 17% from beef samples. Notably, strains exhibited greater resistance to tetracycline (51%), ciprofloxacin (46%), and fosfomycin (38%), apart from β-lactams. The detection of antimicrobial resistance in food-isolated strains is noteworthy, underscoring the significance of antimicrobial resistance as a global concern. More than 90% of the strains were biofilm producers, and strains carrying many ExPEC genes were more likely to be biofilm formers (OR 2.42), which increases the problem since the microorganisms have a greater chance of environment persistence and genetic exchange. Regarding molecular characterization, bovine samples showed a higher prevalence of bla(CTX-M-1) (OR 6.52), while chicken strains were more likely to carry the fosA3 gene (OR 2.43, CI 1.17–5.05) and presented between 6 to 8 ExPEC genes (OR 2.5, CI 1.33–5.01) compared to other meat samples. Concerning diarrheagenic E. coli genes, two strains harbored eae. It is important to highlight these strains, as they exhibited both biofilm-forming capacities and multidrug resistance (MDR), potentially enabling colonization in diverse environments and causing infections. In conclusion, this study underscores the presence of β-lactamase-producing E. coli strains, mainly in poultry samples, compared to beef and pork samples. Furthermore, all meat sample strains exhibited many virulence-associated extraintestinal genes, with some strains harboring diarrheagenic E. coli (DEC) genes. MDPI 2023-11-06 /pmc/articles/PMC10672981/ /pubmed/38004724 http://dx.doi.org/10.3390/microorganisms11112712 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Menck-Costa, Maísa Fabiana
Baptista, Ana Angelita Sampaio
Sanches, Matheus Silva
dos Santos, Beatriz Queiroz
Cicero, Claudinéia Emidio
Kitagawa, Hellen Yukari
Justino, Larissa
Medeiros, Leonardo Pinto
de Souza, Marielen
Rocha, Sergio Paulo Dejato
Nakazato, Gerson
Kobayashi, Renata Katsuko Takayama
Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach
title Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach
title_full Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach
title_fullStr Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach
title_full_unstemmed Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach
title_short Resistance and Virulence Surveillance in Escherichia coli Isolated from Commercial Meat Samples: A One Health Approach
title_sort resistance and virulence surveillance in escherichia coli isolated from commercial meat samples: a one health approach
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10672981/
https://www.ncbi.nlm.nih.gov/pubmed/38004724
http://dx.doi.org/10.3390/microorganisms11112712
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