Abstract
The World Health Organisation has defined “highest priority critically important antimicrobials” (CIAs) as those requiring the greatest control during food production. Evidence demonstrating that restricted antimicrobial usage prevents the emergence of resistance to CIA’s amongst pathogenic and commensal organisms on a production system-wide scale would strengthen international efforts to control antimicrobial resistance (AMR). Therefore, in a designed survey of all major chicken-meat producers in Australia, we investigated the phenotypic AMR of E. coli (n = 206) and Salmonella (n = 53) from caecal samples of chickens at slaughter (n = 200). A large proportion of E. coli isolates (63.1%) were susceptible to all tested antimicrobials. With regards to CIA resistance, only two E.coli isolates demonstrated resistance to fluoroquinolones, attributed to mutations in the quinolone resistance-determining regions of gyrA. Antimicrobial resistance was observed for trimethoprim/sulfamethoxazole (8.7%), streptomycin (9.7%), ampicillin (14.1%), tetracycline (19.4%) and cefoxitin (0.5%). All Salmonella isolates were susceptible to ceftiofur, chloramphenicol, ciprofloxacin, colistin, florfenicol, gentamicin and tetracycline. A low frequency of Salmonella isolates exhibited resistance to streptomycin (1.9%), ampicillin (3.8%), and cefoxitin (11.3%). AMR was only observed among Salmonella Sofia serovars. None of the Salmonella isolates exhibited a multi-class-resistant phenotype. Whole genome sequencing did not identify any known resistance mechanisms for the Salmonella isolates demonstrating resistance to cefoxitin. The results provide strong evidence that resistance to highest priority CIA’s is absent in commensal E. coli and Salmonella isolated from Australian meat chickens, and demonstrates low levels of resistance to compounds with less critical ratings such as cefoxitin, trimethoprim/sulfamethoxazole, and tetracycline. Apart from regulated exclusion of CIAs from most aspects of livestock production, vaccination against key bacterial pathogens and stringent biosecurity are likely to have contributed to the favorable AMR status of the Australian chicken meat industry. Nevertheless, industry and government need to proactively monitor AMR and antimicrobial stewardship practices to ensure the long-term protection of both animal and human health.
Highlights
Pathogenic Gram-negative bacteria resistant to highest priority critically important antimicrobials (CIAs) including extended-spectrum cephalosporins (ESCs), fluoroquinolones, carbapenems, and colistin, are a significant public health threat due to limited therapeutic options for treatment [1]
We investigated the antimicrobial resistance characteristics of E. coli and Salmonella isolated from meat chickens in Australia
The results strongly support our hypothesis that highest priority CIA resistance is absent in commensal E. coli and Salmonella isolated from Australian meat chickens
Summary
Pathogenic Gram-negative bacteria resistant to highest priority critically important antimicrobials (CIAs) including extended-spectrum cephalosporins (ESCs), fluoroquinolones, carbapenems, and colistin, are a significant public health threat due to limited therapeutic options for treatment [1]. CIA-resistant bacteria have been detected in food-producing animals with the number of reports identifying CIA-resistant bacteria in animals markedly increasing in recent years [2, 3] These resistant bacteria present a possible risk of direct transmission via crossinfection and colonisation of humans or indirect transfer of associated mobile genetic elements to potentially pathogenic organisms of the human gastrointestinal tract via the food chain [4]. In a recent review [5] the rates of resistance in E. coli isolates from healthy broilers were compared from available studies in a number of countries (USA, Brazil, China, Poland, United Kingdom, Germany, France and Spain). For third generation cephalosporins (ceftiofur and cefotaxime), all countries except the United Kingdom, showed conclusive evidence of resistance being present (median resistance exceeding 5% of isolates, with some countries as high as 50%). With reference to colistin resistance in E. coli and Salmonella from poultry a recent international review shows resistance as being widespread in both developed and developing countries, often exceeding 5% of isolates [7]
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