Researchers find that the Salmonella vaccine for poultry contributed to the rise of antibiotic-resistant bacteria in the UK.
Image Credit: Mary Parker, Quadram Institute (CC-BY 4.0)
A new investigation into the evolution of Salmonella bacteria infecting Brazilian poultry shows that the introduction of a Salmonella vaccine, combined with increasing antibiotic usage by Brazilian farmers, has led to the rise of strains that are more antibiotic-resistant, but less likely to cause disease in humans. This is the conclusion by Andrea Micke Moreno of the University of São Paulo, Brazil, Alison Mather of Quadram Institute Bioscience, UK, and their colleagues, who conducted the investigation.
Their findings are published today the open access journal PLOS Genetics.
Information provided by PLOS ahead of publication explains:
The bacterium Salmonella enterica is a common cause of food poisoning in humans that frequently results from contaminated poultry. Brazil is the world’s largest exporter of chicken meat globally, and a team led by Micke Moreno and Mather wanted to know if the strains of Salmonella present in Brazil were contributing to food poisoning cases in countries that import their products. The researchers compared the genomes of 183 Salmonella collected from chickens in Brazil and 357 Salmonella genomes collected from humans, domestic poultry, and imported Brazilian poultry products in the United Kingdom. They also looked at more than 1,200 publicly available genomes of the two main types of Salmonella found in Brazil to see what they could learn about the evolution of the Brazilian strains.In their abstract and authors' summary the authors say:
The team found that distinct lineages of the two main Salmonella types developed in Brazil in the early 2000s, around the same time that the country introduced a Salmonella vaccine for poultry. These bacteria possess genes that make them resistant to three types of antibiotics. But despite their rise in Brazil, these antibiotic-resistant bacteria have caused very few cases of Salmonella in humans in the UK and have not spread to domestic chickens.Through our genomic detective work, we have tracked how changes in chicken rearing in Brazil have changed the profile of Salmonella bacteria found circulating within the poultry industry. Whilst this poses no immediate health risk to importing countries like the UK, the bacteria were resistant to antimicrobial drugs, and this highlights the importance of taking a ‘One Health’ approach that sees the connections between the health of people, animals and the environment, especially when assessing global food supply chains.
Alison Mather, co-author
Quadram Institute Bioscience, Norwich, Norfolk, UK
Overall, these findings suggest that the use of the Salmonella vaccine in Brazil, along with greater antibiotic usage, enabled the rise of drug-resistant forms of Salmonella, but that these bacteria have not led to greater numbers of food poisoning cases in the UK. The researchers point out that their evaluation of Salmonella genomes from a range of sources in Brazil and the UK reinforces the importance of taking a "One Health" approach to disease, which involves collaborative, multidisciplinary efforts to improve the health of people, animals, and the environment.
AbstractIt looks then that we (and Brazilian farmers) were lucky that the resulting strains, evolved under the selection pressures of antibiotics, were less associated with diseases in humans and not more.
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.
Author summary
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. Here we determine that S. enterica serovars Heidelberg and Minnesota were the most prevalent serovars in Brazilian poultry and in poultry products imported from Brazil into the UK. However, long-term surveillance data collected by the UK Health Security Agency 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. 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. 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.
Alikhan N-F, Moreno LZ, Castellanos LR, Chattaway MA, McLauchlin J, Lodge M, et al. (2022)
Dynamics of Salmonella enterica and antimicrobial resistance in the Brazilian poultry industry and global impacts on public health.
PLoS Genet 18(6): e1010174. https://doi.org/10.1371/journal.pgen.1010174
Copyright: © 2022 The authors.
Published by PLoS. Open access
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
Creationists might like to note that the Theory of Evolution by natural selection forms the basis of interpretation of these findings, with not the slightest sign that the TOE is in some way a theory in crisis. In fact, the torrent of evidence such as this shows that creationism is the notion in crisis while the TOE is alive and well and still the only scientific theory which is making sense of evidence such as this.
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