Dynamics of Salmonella enterica and antimicrobial resistance in the Brazilian poultry industry and global impacts on public health

Alikhan, Nabil-Fareed, Moreno, Luisa Zanolli, Castellanos, Luis Ricardo, Chattaway, Marie Anne, McLauchlin, Jim, Lodge, Martin, O'Grady, Justin, Zamudio, Roxana, Doughty, Emma, Petrovska, Liljana, Cunha, Marcos Paulo Vieira, Knöbl, Terezinha, Moreno, Andrea Micke and Mather, Alison E. (2022) Dynamics of Salmonella enterica and antimicrobial resistance in the Brazilian poultry industry and global impacts on public health. PLoS Genetics, 18 (6). ISSN 1553-7390

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Non-typhoidal Salmonella enterica is a common cause of diarrhoeal disease; in humans, consumption of contaminated poultry meat is believed to be a major source. Brazil is the world’s largest exporter of chicken meat globally, and previous studies have indicated the introduction of Salmonella serovars through imported food products from Brazil. Here we provide an in-depth genomic characterisation and evolutionary analysis to investigate the most prevalent serovars and antimicrobial resistance (AMR) in Brazilian chickens and assess the impact to public health of products contaminated with S. enterica imported into the United Kingdom from Brazil. To do so, we examine 183 Salmonella genomes from chickens in Brazil and 357 genomes from humans, domestic poultry and imported Brazilian poultry products isolated in the United Kingdom. S. enterica serovars Heidelberg and Minnesota were the most prevalent serovars in Brazil and in meat products imported from Brazil into the UK. We extended our analysis to include 1,259 publicly available Salmonella Heidelberg and Salmonella Minnesota genomes for context. The Brazil genomes form clades distinct from global isolates, with temporal analysis suggesting emergence of these Salmonella Heidelberg and Salmonella Minnesota clades in the early 2000s, around the time of the 2003 introduction of the Enteritidis vaccine in Brazilian poultry. Analysis showed genomes within the Salmonella Heidelberg and Salmonella Minnesota clades shared resistance to sulphonamides, tetracyclines and beta-lactams conferred by sul2, tetA and blaCMY-2 genes, not widely observed in other co-circulating serovars despite similar selection pressures. The sul2 and tetA genes were concomitantly carried on IncC plasmids, whereas blaCMY-2 was either co-located with the sul2 and tetA genes on IncC plasmids or independently on IncI1 plasmids. Long-term surveillance data collected in the UK showed no increase in the incidence of Salmonella Heidelberg or Salmonella Minnesota in human cases of clinical disease in the UK following the increase of these two serovars in Brazilian poultry. In addition, almost all of the small number of UK-derived genomes which cluster with the Brazilian poultry-derived sequences could either be attributed to human cases with a recent history of foreign travel or were from imported Brazilian food products. These findings indicate that even should Salmonella from imported Brazilian poultry products reach UK consumers, they are very unlikely to be causing disease. No evidence of the Brazilian strains of Salmonella Heidelberg or Salmonella Minnesota were observed in UK domestic chickens. These findings suggest that introduction of the Salmonella Enteritidis vaccine, in addition to increasing antimicrobial use, could have resulted in replacement of salmonellae in Brazilian poultry flocks with serovars that are more drug resistant, but less associated with disease in humans in the UK. The plasmids conferring resistance to beta-lactams, sulphonamides and tetracyclines likely conferred a competitive advantage to the Salmonella Minnesota and Salmonella Heidelberg serovars in this setting of high antimicrobial use, but the apparent lack of transfer to other serovars present in the same setting suggests barriers to horizontal gene transfer that could be exploited in intervention strategies to reduce AMR. The insights obtained reinforce the importance of One Health genomic surveillance.

Item Type: Article
Additional Information: Data Availability: Sequenced raw reads from isolates collected from Brazilian chickens are available from European Nucleotide Archive (ENA) PRJEB46151. All UKHSA sequence data, including sequence data used here from cultures from chicken meat imported into the UK, is routinely deposited in the NCBI Sequence Read Archive (SRA) under BioProject accession PRJNA248792 (https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA248792). All APHA sequence data are available in the European Nucleotide Archive (ENA) (accession PRJEB46896). Funding: This project was supported by Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/R022682/1 and BB/S018913/1 to AEM. NFA was supported in part by Quadram Institute Bioscience BBSRC funded Core Capability Grant (project number BB/CCG1860/1) and RZ was supported by Medical Research Council grant MR/R000948/1. In Brazil, this project was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (São Paulo Research Foundation, FAPESP) (grants 2017/50453-2 and 2018/21216-5). MPVC was a recipient of FAPESP fellowship (grant 2019/18551-0). TK and AMM are Conselho Nacional de Desenvolvimento Científico e Tecnológico (National Council for Scientific and Technological Development, CNPq) fellows (grants 306396/2020-3 and 310736/2018-8). LZM is supported by CNPq (grant 151908/2020-6). AEM is a Food Standards Agency Fellow. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Uncontrolled Keywords: ecology, evolution, behavior and systematics,molecular biology,genetics,genetics(clinical),cancer research,sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Medicine and Health Sciences > Norwich Medical School
UEA Research Groups: Faculty of Medicine and Health Sciences > Research Centres > Metabolic Health
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Depositing User: LivePure Connector
Date Deposited: 04 Nov 2022 16:30
Last Modified: 06 Jun 2024 15:21
URI: https://ueaeprints.uea.ac.uk/id/eprint/89627
DOI: 10.1371/journal.pgen.1010174


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