Dataset Information

Dissemination of Quinolone-Resistant Escherichia coli in the Norwegian Broiler and Pig Production Chains and Possible Persistence in the Broiler Production Environment.

ABSTRACT: In Norway, the use of quinolones in livestock populations is very low, and prophylactic use is prohibited. Despite this, quinolone-resistant Escherichia coli (QREC) isolates are present at low levels in several animal species. The source of these QREC isolates is unknown. The aim of this study was to characterize and compare QREC isolates from different animal species to identify putative factors that may promote the occurrence of QREC. A total of 280 QREC isolates, from broilers, pigs, red foxes, and wild birds, were whole-genome sequenced and analyzed. Well-known chromosomal and plasmid-mediated resistance mechanisms were identified. In addition, mutations in marR, marA, and rpoB causing novel amino acid substitutions in their respective proteins were detected. Phylogenetic analyses were used to determine the relationships between the isolates. Quinolone resistance mechanism patterns appeared to follow sequence type groups. Similar QREC isolates with similar resistance mechanism patterns were detected from the samples, and further phylogenetic analysis indicated close evolutionary relationships between specific isolates from different sources. This suggests the dissemination of highly similar QREC isolates between animal species and also the persistence of QREC strains within the broiler production chain. This highlights the importance of both control measures at the top of the production chain as well as biosecurity measures to avoid the further dissemination and persistence of QREC in these environments.IMPORTANCE Since antimicrobial usage is low in Norwegian animal husbandry, Norway is an ideal country to study antimicrobial resistance in the absence of selective pressure from antimicrobial usage. In particular, the usage of quinolones is very low, which makes it possible to investigate the spread and development of quinolone resistance in natural environments. Comparison of quinolone-resistant E. coli (QREC) isolates from livestock and wild animals in light of this low quinolone usage provides new insights into the development and dissemination of QREC in both natural and production environments. With this information, preventive measures may be taken to prevent further dissemination within Norwegian livestock and between other animals, thus maintaining the favorable situation in Norway.

SUBMITTER: Kaspersen H

PROVIDER: S-EPMC7082582 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Dissemination of Quinolone-Resistant Escherichia coli in the Norwegian Broiler and Pig Production Chains and Possible Persistence in the Broiler Production Environment.

Kaspersen Håkon H Sekse Camilla C Zeyl Fiskebeck Eve E Slettemeås Jannice Schau JS Simm Roger R Norström Madelaine M Urdahl Anne Margrete AM Lagesen Karin K

Applied and environmental microbiology 20200318 7

In Norway, the use of quinolones in livestock populations is very low, and prophylactic use is prohibited. Despite this, quinolone-resistant <i>Escherichia coli</i> (QREC) isolates are present at low levels in several animal species. The source of these QREC isolates is unknown. The aim of this study was to characterize and compare QREC isolates from different animal species to identify putative factors that may promote the occurrence of QREC. A total of 280 QREC isolates, from broilers, pigs, r ...[more]

PMID: 31953334

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Project description:Poultry and swine farming are large contributors to environmental impacts, such as climate change, eutrophication, acidification, and air and water pollution. Feed production and manure management are identified as the main sources of these impacts. Reducing dietary crude protein levels is a nutritional strategy recognized to both decrease the use of high-impact feed ingredients and alter manure composition, reducing emissions of harmful components. For a successful implementation of this technique, feed-grade amino acid supplementation is crucial to maintaining animal performance. Reducing crude protein lowers nitrogen excretion, especially excess nitrogen excreted in urea or uric acid form, improving nitrogen efficiency. At the feed-gate, low-crude protein diets can reduce the carbon footprint of feed production through changes in raw material inclusion. The magnitude of this reduction mainly depends on the climate change impact of soybean meal and its land-use change on the feed-grade amino acids used. Reducing dietary crude protein also lowers the environmental impact of manure management in housing, storage, and at spreading: nitrogen emissions from manure (ammonia, nitrates, nitrous oxide) are reduced through reduction of nitrogen excretion. Moreover, synergetic effects exist with nitrogen form, water excretion, and manure pH, further reducing emissions. Volatilization of nitrogen is more reduced in poultry than in pigs, but emissions are more studied and better understood for pig slurry than poultry litter. Ammonia emissions are also more documented than other N-compounds. Low-crude protein diets supplemented with amino acids is a strategy reducing environmental impact at different stages of animal production, making life cycle assessment the best-suited tool to quantify reduction of environmental impacts. Recent studies report an efficient reduction of environmental impacts with low-crude protein diets. However, more standardization of limits and methods used is necessary to compare results. This review summarizes the current knowledge on mitigation of environmental impacts with low-crude protein diets supplemented with amino acids in poultry and swine, its quantification, and the biological mechanisms involved. A comparison between pigs and poultry is also included. It provides concrete information based on quantified research for decision making for the livestock industry and policy makers.

Project description:BackgroundQuinolone resistant Escherichia coli (QREC) have been found in samples from Norwegian broiler chicken, despite quinolones not being administered to poultry in Norway. Biofilm production may be one factor contributing to the observed persistence in the broiler production chain. In the present study, 158 QREC strains from chicken caecal and retail meat samples were screened for biofilm production in microtiter plates, biofilm morphotype on Congo Red (CR) agar plates and phylotype by multiplex PCR. Furthermore, the dynamics in mixed biofilms with strains of different morphotypes were studied on glass slides and on CR agar plates.ResultsAll strains but one produced biofilm in microtiter plates and/or on CR agar plates at room temperature. There were no differences between strains from chicken caecum and chicken retail meat in the mean amount of biofilm produced in microtiter plates. Furthermore, no differences in biofilm production were observed between phylotypes. However, significant differences in biofilm production were found between biofilm morphotypes. The morphotype RDAR (red dry and rough, which has both curli and cellulose in the matrix, was displayed by 70% of the strains. Mean biofilm production by these strains were significantly higher than by strains with the morphotypes PDAR (pink dry and rough) with only cellulose or BDAR (brown dry and rough) with only curli. Interestingly, the two latter morphotypes produced biofilms with the morphotype RDAR when grown together. None of the strains achieved significantly higher numbers of colony forming units (cfu) in mixed biofilms than in single strain biofilms on glass slides.ConclusionsThe results indicate that QREC can form biofilm reservoirs on both inert and organic surfaces in production environments, as well as on meat. This may contribute to persistence and dissemination of the strains. Strains with both curli and cellulose in the biofilm matrix were significantly better biofilm formers than strains lacking one of these components. However, strains with only one of the components could compensate for this by producing mixed biofilms with strains having the other component, and thereby most likely enhance their probabilities of persistence in the production environment.

Project description:Escherichia coli resistant to extended-spectrum cephalosporins have been detected in the Norwegian broiler production, despite the fact that antimicrobial agents are rarely used. The genetic mechanism responsible for cephalosporin resistance is mainly attributed to the presence of the blaCMY-2 gene encoding a plasmid-mediated AmpC-beta-lactamase (pAmpC). The aim of this study was to characterize and compare blaCMY-2 containing Escherichia coli isolated from the intestinal flora of broilers and retail chicken meat (fillets) to identify possible successful clones and/or resistance plasmids widespread in the Norwegian broiler production. Methods used included PCR based phylotyping, conjugation experiments, plasmid replicon typing, pulsed-field gel electrophoresis, multiple locus variable-number tandem-repeats analysis and whole genome sequencing. The nucleotide sequence of an IncK plasmid carrying blaCMY-2 was determined. Intestinal isolates displayed a higher degree of genetic diversity than meat isolates. A cluster of genetically related isolates belonging to ST38, phylogroup D, carrying blaCMY-2 containing IncK plasmids was identified. Furthermore, genes encoding plasmid stability systems (relBE/stbDE and pndAC) were identified on the IncK plasmid. Single nucleotide polymorphism (SNP) analysis of a subset of isolates confirmed a close genetic relationship within the two most prevalent STs. The IncK plasmids within these two STs also shared a high degree of similarity. Cephalosporin-resistant E. coli with the same genetic characteristics have been identified in the broiler production in other European countries, and the IncK plasmid characterized in this study showed close homology to a plasmid isolated from retail chicken meat in the Netherlands. The results indicate that both clonal expansion and horizontal transfer of blaCMY-2 containing plasmids contribute to dissemination of cephalosporin resistant E. coli in the broiler production. The presence of plasmid stability systems may explain why the IncK plasmid containing blaCMY-2 is maintained and disseminated in the Norwegian broiler production in absence of selection pressure from the use of antimicrobial agents.

Dataset Information

Dissemination of Quinolone-Resistant Escherichia coli in the Norwegian Broiler and Pig Production Chains and Possible Persistence in the Broiler Production Environment.

Publications

Dissemination of Quinolone-Resistant Escherichia coli in the Norwegian Broiler and Pig Production Chains and Possible Persistence in the Broiler Production Environment.

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