Salmonella. Image by Dr Mary Parker, the Quadram Institute
Researchers have used genome surveillance for Salmonella on Brazilian chicken to better understand the impact on global public health of intensive poultry farming.
Scientists from the Quadram Institute, University of East Anglia, UK Health Security Agency, Animal and Plant Health Agency in the UK and the University of São Paulo in Brazil have tracked how changes in chicken rearing in Brazil have changed the profile of Salmonella bacteria found circulating within the poultry industry. Their genomic detective work has shown that whilst this poses no immediate health risk to importing countries like the UK, the bacteria were resistant to antimicrobial drugs.
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.
Brazil produces almost 14 million tons of chicken meat each year and is the world’s largest exporter. Previous studies have reported the presence of Salmonella enterica on meat being imported into the UK and EU. These bacteria are one of the most common causes of diarrheal disease, and can also carry genes that make them resistant to antibiotics used to treat human infection. The intensive farming techniques used in Brazil to produce large amounts of chicken meat relies on the use of antimicrobials, but this is a known driver of genetic resistance to antimicrobials.
Genome surveillance for Salmonella
Phylogeny of Salmonella samples. the colours of the outer ring show the different types, with Heidelberg (purple) and Minnesota (orange) the most common. From PLOS Genetics DOI: 10.1371/journal.pgen.1010174
To investigate Salmonella in Brazilian poultry and the potential risks to food safety, researchers from the Quadram Institute and the University of São Paulo carried out a genomic survey of Salmonella samples obtained from chickens in Brazil as part of routine monitoring for the bacteria over a seven-year span. They compared these with Salmonella genomes from poultry products exported from Brazil to the UK and other European countries as well as genomes from humans and domestic poultry in the UK, all put in context with hundreds of Salmonella genomes from across the world.
The study was supported by the Biotechnology and Biological Sciences Research Council, part of UK Research and Innovation, and the São Paulo Research Foundation.
The survey of Brazilian poultry found dozens of different types of Salmonella, with two particular types, called Heidelberg and Minnesota, the most dominant. Salmonella Enteritidis, a predominant cause of food poisoning, accounted for only 2% of samples. Of the samples from meat imported into the UK, 91% were either Heidelberg or Minnesota.
Are these imported Salmonella types causing significant disease in the UK?
Working with the UK Health Security Agency (UKHSA), the team looked at the types of Salmonella that were behind infections from samples going back 15 years. Around one in two hundred were attributed to Heidelberg or Minnesota, and some of these could be attributed to recent foreign travel. Importantly, by comparing the Brazilian Heidelberg and Minnesota genomes with others collected and deposited around the world, including the UK, it was clear that the Brazilian Salmonella types formed a distinct subgroup separate from human cases. In addition, collaboration with the Animal and Plant Health Agency (APHA) showed that the Brazilian-associated Salmonella were not found in UK chickens.
“Our findings show that Salmonella from imported Brazilian poultry products have not caused a major disease burden to UK consumers” said Professor Alison Mather from the Quadram Institute, who led the study along with Professor Andrea Micke Moreno from the University of São Paulo.
When did these Salmonella types emerge in Brazil?
To answer this, the team looked back further, including in their analysis genomes obtained from other studies examining Salmonella from imported Brazilian chicken. This suggested that the Brazilian Salmonella types derived from a common ancestor that emerged around 2006.
This relatively recent introduction and rise to dominance appears to have been tied to the introduction of a vaccine against Salmonella Enteriditis in 2003.
“The results show that the constant monitoring of key pathogens such as Salmonella involving animal and human populations is extremely important to comprehend the effects of prevention and control programs implemented in a specific population” said Professor Andrea Micke Moreno from the University of São Paulo.
Similar changes in the predominant types of Salmonella have been seen before following human interventions, like vaccine development, that clear a niche that others can exploit. The question is what is it that allowed two very different salmonellae, Heidelberg and Minnesota, to fill that niche in Brazil. To find the answer, the researchers looked again into their genomes, this time in more detail.
What they found was that both Salmonella Heidelberg and Salmonella Minnesota carried a combination of specific genes conferring resistance to different classes of antimicrobials: sulphonamides, tetracyclines and beta lactams. This likely gave these types of Salmonella a competitive advantage in the poultry production environment in Brazil, where antibiotic usage is high.
Lead author Dr Nabil-Fareed Alikhan said “It was very exciting to work with all of our collaborators on this project. With their support, we had independent data to link these types of Salmonella and their impact across the food production chain.”
Intriguingly, other types of Salmonella circulating don’t appear to have picked up the resistance genes. This is somewhat unusual, as Salmonella like other bacteria frequently swap genes. The researchers are keen to get a better understanding of the barriers to the transfer of the antimicrobial resistance genes as it might point to new ways of tackling this global problem.
Dynamics of Salmonella enterica and antimicrobial resistance in the Brazilian poultry industry and global impacts on public health. Nabil-Fareed Alikhan, Luisa Zanolli Moreno, Luis Ricardo Castellanos, Marie Anne Chattaway, Jim McLauchlin, Martin Lodge, Justin O’Grady, Roxana Zamudio, Emma Doughty, Liljana Petrovska, Marcos Paulo Vieira Cunha, Terezinha Knöbl, Andrea Micke Moreno, Alison E. Mather PLOS GENETICS 18(6): e1010174. DOI: 10.1371/journal.pgen.1010174