In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk

IntroductionThe spread of antimicrobial resistance (AMR) has become a threat against human and animal health. Third and fourth generation cephalosporins have been defined as critically important antimicrobials by The World Health Organization. Exposure to Extended spectrum cephalosporin-resistant E....

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Main Authors: May Linn Buberg, Yngvild Wasteson, Bjørn Arne Lindstedt, Ingun Lund Witsø
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1050143/full
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author May Linn Buberg
Yngvild Wasteson
Bjørn Arne Lindstedt
Ingun Lund Witsø
author_facet May Linn Buberg
Yngvild Wasteson
Bjørn Arne Lindstedt
Ingun Lund Witsø
author_sort May Linn Buberg
collection DOAJ
description IntroductionThe spread of antimicrobial resistance (AMR) has become a threat against human and animal health. Third and fourth generation cephalosporins have been defined as critically important antimicrobials by The World Health Organization. Exposure to Extended spectrum cephalosporin-resistant E. coli may result in consumers becoming carriers if these bacteria colonize the human gut or their resistance genes spread to other bacteria in the gut microbiota. In the case that these resistant bacteria at later occasions cause disease, their resistance characteristics may lead to failure of treatment and increased mortality. We hypothesized that ESC-resistant E. coli from poultry can survive digestion and thereby cause infections and/or spread their respective resistance traits within the gastro-intestinal tract.MethodsIn this study, a selection of 31 ESC-resistant E. coli isolates from retail chicken meat was exposed to a static in vitro digestion model (INFOGEST). Their survival, alteration of colonizing characteristics in addition to conjugational abilities were investigated before and after digestion. Whole genome data from all isolates were screened through a custom-made virulence database of over 1100 genes for virulence- and colonizing factors.Results and discussionAll isolates were able to survive digestion. Most of the isolates (24/31) were able to transfer their blaCMY2-containing plasmid to E. coli DH5-á, with a general decline in conjugation frequency of digested isolates compared to non-digested. Overall, the isolates showed a higher degree of cell adhesion than cell invasion, with a slight increase after digestion compared non-digested, except for three isolates that displayed a major increase of invasion. These isolates also harbored genes facilitating invasion. In the virulence-associated gene analysis two isolates were categorized as UPEC, and one isolate was considered a hybrid pathogen. Altogether the pathogenic potential of these isolates is highly dependent on the individual isolate and its characteristics. Poultry meat may represent a reservoir and be a vehicle for dissemination of potential human pathogens and resistance determinants, and the ESC-resistance may complicate treatment in the case of an infection.
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spelling doaj.art-d18b03ad411d43a1a514dacc5e7b35c52023-02-09T09:58:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.10501431050143In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health riskMay Linn Buberg0Yngvild Wasteson1Bjørn Arne Lindstedt2Ingun Lund Witsø3Department of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Ås, NorwayDepartment of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Ås, NorwayFaculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, NorwayDepartment of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Ås, NorwayIntroductionThe spread of antimicrobial resistance (AMR) has become a threat against human and animal health. Third and fourth generation cephalosporins have been defined as critically important antimicrobials by The World Health Organization. Exposure to Extended spectrum cephalosporin-resistant E. coli may result in consumers becoming carriers if these bacteria colonize the human gut or their resistance genes spread to other bacteria in the gut microbiota. In the case that these resistant bacteria at later occasions cause disease, their resistance characteristics may lead to failure of treatment and increased mortality. We hypothesized that ESC-resistant E. coli from poultry can survive digestion and thereby cause infections and/or spread their respective resistance traits within the gastro-intestinal tract.MethodsIn this study, a selection of 31 ESC-resistant E. coli isolates from retail chicken meat was exposed to a static in vitro digestion model (INFOGEST). Their survival, alteration of colonizing characteristics in addition to conjugational abilities were investigated before and after digestion. Whole genome data from all isolates were screened through a custom-made virulence database of over 1100 genes for virulence- and colonizing factors.Results and discussionAll isolates were able to survive digestion. Most of the isolates (24/31) were able to transfer their blaCMY2-containing plasmid to E. coli DH5-á, with a general decline in conjugation frequency of digested isolates compared to non-digested. Overall, the isolates showed a higher degree of cell adhesion than cell invasion, with a slight increase after digestion compared non-digested, except for three isolates that displayed a major increase of invasion. These isolates also harbored genes facilitating invasion. In the virulence-associated gene analysis two isolates were categorized as UPEC, and one isolate was considered a hybrid pathogen. Altogether the pathogenic potential of these isolates is highly dependent on the individual isolate and its characteristics. Poultry meat may represent a reservoir and be a vehicle for dissemination of potential human pathogens and resistance determinants, and the ESC-resistance may complicate treatment in the case of an infection.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1050143/fullvirulenceExPECconjugationINFOGESThybrid pathogen
spellingShingle May Linn Buberg
Yngvild Wasteson
Bjørn Arne Lindstedt
Ingun Lund Witsø
In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk
Frontiers in Microbiology
virulence
ExPEC
conjugation
INFOGEST
hybrid pathogen
title In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk
title_full In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk
title_fullStr In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk
title_full_unstemmed In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk
title_short In vitro digestion of ESC-resistant Escherichia coli from poultry meat and evaluation of human health risk
title_sort in vitro digestion of esc resistant escherichia coli from poultry meat and evaluation of human health risk
topic virulence
ExPEC
conjugation
INFOGEST
hybrid pathogen
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1050143/full
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