The Role of European Starlings (Sturnus vulgaris) in the Dissemination of Multidrug-Resistant Escherichia coli among Concentrated Animal Feeding Operations

Abstract

Antimicrobial use in livestock production is a driver for the development and proliferation of antimicrobial resistance (AMR). Wildlife interactions with livestock, acquiring associated AMR bacteria and genes, and wildlife's subsequent dispersal across the landscape are hypothesized to play an important role in the ecology of AMR. Here, we examined priority AMR phenotypes and genotypes of Escherichia coli isolated from the gastrointestinal tracts of european starlings (Sturnus vulgaris) found on concentrated animal feeding operations (CAFOs). European starlings may be present in high numbers on cAfos (>100,000 birds), interact with urban environments, and can migrate distances exceeding 1,500 km in North America. In this study, 1,477 European starlings from 31 feedlots in five U.S. states were sampled for E. coli resistant to third generation cephalosporins (3G-C) and fluoroquinolones. The prevalence of 3G-C and fluoroquinolone-resistant E. coli was 4% and 10%, respectively. Multidrug resistance in the E. coli isolates collected (n = 236) was common, with the majority of isolates displaying resistance to six or more classes of antibiotics. Genetic analyses of a subset of these isolates identified 94 genes putatively contributing to AMR, including seven class A and c β-lactamases as well as mutations in gyrA and parC recognized to confer resistance to quinolones. Phylogenetic and subtyping assessments showed that highly similar isolates (≥99.4% shared core genome, ≥99.6% shared coding sequence) with priority AMR were found in birds on feedlots separated by distances exceeding 150 km, suggesting that European starlings could be involved in the interstate dissemination of priority AMR bacteria. Antibiotic use in animal agriculture for prophylaxis, therapy, and growth promotion is generally recognized to coincide with the proliferation of antimicrobial resistance (AMR) in associated bacterial communities 1-3. This is problematic not only for animal agriculture, but also because many antibiotics used in livestock are identical in structure or function to those used in human medicine 4,5. Furthermore, the use of antibiotics in food animals is predicted to increase globally for the foreseeable future and is expected to exacerbate the AMR problem 6 .

Multidrug-Resistant Phenotypes of Escherichia coli Isolates in Wild Canarian Egyptian Vultures (Neophron percnopterus majorensis)

“…Antimicrobial resistance has been detected in many wildlife species on all continents, including Antarctica and the Arctic [3][4][5][6][7][8][9], even when wildlife are not treated with these compounds. This supports the possibility of transmission of resistant bacteria between human, livestock and domestic animals, wildlife and the environment, as well as the possible selective pressure exerted by antibiotic residues present in the environment [10][11][12][13][14]. Surveillance of antimicrobial resistant (AMR) bacteria in wildlife can help to understand the extent of the problem and propose possible solutions [15].…”

European Starlings (Sturnus vulgaris) as Vectors and Reservoirs of Pathogens Affecting Humans and Domestic Livestock

“…Starlings also carry a variety of antibiotic resistant strains [ 9 , 22 , 23 , 24 , 25 , 26 , 27 ], at frequencies of 10–20% of individuals ( Table 2 ). Circumstantial evidence suggests that they play a role in spreading these strains to cattle [ 23 , 24 , 25 ].…”

“…Starlings also carry a variety of antibiotic resistant strains [ 9 , 22 , 23 , 24 , 25 , 26 , 27 ], at frequencies of 10–20% of individuals ( Table 2 ). Circumstantial evidence suggests that they play a role in spreading these strains to cattle [ 23 , 24 , 25 ]. Strains resistant to tetracycline, ampicillin, and streptomycin [ 9 ], in addition to the fluoroquinolone ciprafloxacin [ 22 , 24 , 25 , 26 ] and the cephalosporin cefotaxime [ 24 , 25 , 26 ] are well documented, and many of these same strains also show resistance to a wide range of other antibiotics, including tetracycline and β-lactam antibiotics [ 24 ].…”

“…Circumstantial evidence suggests that they play a role in spreading these strains to cattle [ 23 , 24 , 25 ]. Strains resistant to tetracycline, ampicillin, and streptomycin [ 9 ], in addition to the fluoroquinolone ciprafloxacin [ 22 , 24 , 25 , 26 ] and the cephalosporin cefotaxime [ 24 , 25 , 26 ] are well documented, and many of these same strains also show resistance to a wide range of other antibiotics, including tetracycline and β-lactam antibiotics [ 24 ]. The genetic mechanisms providing resistance are numerous (more than 90 different genes) and are spread over many mechanisms of action, including drug efflux, cellular target alteration, and drug inactivation [ 9 , 24 ].…”

High-Throughput Detection and Characterization of Antimicrobial Resistant Enterococcus sp. Isolates from GI Tracts of European Starlings Visiting Concentrated Animal Feeding Operations

“…Instead of tracking AMR pathogen movement, which can prove difficult, monitoring commensal bacteria is more convenient because of the widespread availability and ease of comparison to relevant pathogenic populations; thus, development of an “early alert system” for the transmission of microorganisms of interest to the food production system can be more easily executed [ 8 ]. Since food animals encounter wildlife, especially avian scavengers, on a continuous basis, testing of commensal bacterial samples from animals in concentrated animal feeding operations (CAFOs) and associated wildlife provides a better understanding of CAFO microbial ecology, which could be used to implement targeted programs to control the dissemination and evolution of AMR bacteria [ 9 , 10 , 11 ]. European starlings ( Sturnus vulgaris ) are commonly associated with many human and livestock pathogens and have been on the Invasive Species Specialist Group’s list “100 of the World’s Worst Invasive Alien Species” for many years, continually plaguing agricultural operations [ 12 , 13 ].…”