Abstract
BackgroundTherapeutic and growth-promoting antibiotics are frequently used in broiler production. Indirect evidence indicates that these practices are linked to the proliferation of antimicrobial resistance (AMR), the spread of antibiotic-resistant bacteria from food animals to humans, and the environment, but there is a lack of comprehensive experimental data supporting this. We investigated the effects of growth promotor (bacitracin) and therapeutic (enrofloxacin) antibiotic administration on AMR in broilers for the duration of a production cycle, using a holistic approach that integrated both culture-dependent and culture-independent methods. We specifically focused on pathogen-harboring families (Enterobacteriaceae, Enterococcaceae, and Staphylococcaceae).ResultsAntibiotic-resistant bacteria and antibiotic resistance genes were ubiquitous in chicken cloaca and litter regardless of antibiotic administration. Environment (cloaca vs. litter) and growth stage were the primary drivers of variation in the microbiomes and resistomes, with increased bacterial diversity and a general decrease in abundance of the pathogen-harboring families with age. Bacitracin-fed groups had higher levels of bacitracin resistance genes and of vancomycin-resistant Enterococcaceae (total Enterococcaceae counts were not higher). Although metagenomic analyses classified 28–76% of the Enterococcaceae as the commensal human pathogens E. faecalis and E. faecium, culture-based analysis suggested that approximately 98% of the vancomycin-resistant Enterococcaceae were avian and not human-associated, suggesting differences in the taxonomic profiles of the resistant and non-resistant strains. Enrofloxacin treatments had varying effects, but generally facilitated increased relative abundance of multidrug-resistant Enterobacteriaceae strains, which were primarily E. coli. Metagenomic approaches revealed a diverse array of Staphylococcus spp., but the opportunistic pathogen S. aureus and methicillin resistance genes were not detected in culture-based or metagenomic analyses. Camphylobacteriaceae were significantly more abundant in the cloacal samples, especially in enrofloxacin-treated chickens, where a metagenome-assembled C. jejuni genome harboring fluoroquinolone and β-lactam resistance genes was identified.ConclusionsWithin a “farm-to-fork, one health” perspective, considering the evidence that bacitracin and enrofloxacin used in poultry production can select for resistance, we recommend their use be regulated. Furthermore, we suggest routine surveillance of ESBL E. coli, vancomycin-resistant E. faecalis and E. faecium, and fluoroquinolone-resistant C. jejuni strains considering their pathogenic nature and capacity to disseminate AMR to the environment.E2eQV6Q9BhTz4idhLosSegVideo
Highlights
Therapeutic and growth-promoting antibiotics are frequently used in broiler production
We focused on vancomycin-resistant enterococci (VRE), methicillin-resistant staphylococci (MRS), and extended-spectrum betalactamase-producing Enterobacteriaceae (ESBL-E) that are resistant to third-generation cephalosporins, due to the clinical importance of priority pathogens from these groups such as vancomycin-resistant E. faecium and E. faecalis, methicillin-resistant Staphylococcus aureus, and ESBL-producing Klebsiella pneumonia and E. coli
On day 28, half of the animals in each dietary treatment group were treated for 3 days with the fluoroquinolone enrofloxacin administered through drinking water at a standard therapeutic dose
Summary
Therapeutic and growth-promoting antibiotics are frequently used in broiler production. AGPs on the other hand are feed additives given at sub-therapeutic doses for most of the growth cycle, regardless of the presence of a disease or specific pathogens, and are believed to improve weight gain [1,2,3]. The fluoroquinolone enrofloxacin was first licensed for the treatment of respiratory diseases in poultry in the USA in 1996, but the clinical importance of fluoroquinolones and the alarming evidence of quinolone-resistant zoonotic pathogens (e.g., Campylobacter spp., Enterobacteriales), led the USA, European Union, and other countries to ban their use in food animal production [4,5,6,7]. Banning fluoroquinolones has not completely eliminated the occurrence of resistant populations [9] This may be explained by the fact that bacteria can remain resistant to antibiotics long after eliminating selection or due to the fact that many environmental bacteria intrinsically harbor ARGs, regardless of selective pressure [10]
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