Antimicrobial resistance and prevalence of extended-spectrum beta-lactamase-producing Klebsiella species in East Tennessee dairy farms

Abstract

ABSTRACT Klebsiella species commonly reside in dairy cattle guts and are consistently exposed to beta-lactam antibiotics, including ceftiofur, which are frequently used on the U.S. dairy farms. This may impose selection pressure and result in the emergence of extended-spectrum beta-lactamase (ESBL)-producing strains. However, information on the status and antimicrobial resistance (AMR) profile of ESBL- Klebsiella spp. in the U.S. dairy farms is largely unknown. This study aimed to determine the prevalence and AMR profile of ESBL- Klebsiella spp. and the factors affecting their occurrence in dairy cattle farms. Rectal fecal samples ( n = 508) and manure, feed, and water samples ( n = 64) were collected from 14 dairy farms in Tennessee. Samples were directly plated on CHROMagar ESBL, and presumptive Klebsiella spp. were confirmed using matrix-assisted laser desorption/ionization-time of flight mass spectrometry. Antimicrobial susceptibility testing was performed on the isolates against panels of 14 antimicrobial agents from 10 classes using minimum inhibitory concentration. Of 572 samples, 57 (10%) were positive for ESBL- Klebsiella spp. The fecal prevalence of ESBL- Klebsiella spp. was 7.2% (95% CI: 6.5–8.0). The herd-level fecal prevalence of ESBL- Klebsiella spp. was 35.7% (95% CI: 12.7–64.8). The fecal prevalence of ESBL- Klebsiella spp. was significantly higher in calves than in cows and higher in cows with higher parity (≥3) as compared to cows with low parity ( P < 0.001). Most (96.5%, n = 57) ESBL- Klebsiella spp. were resistant to ceftriaxone. The highest level of acquired co-resistance to ceftriaxone in ESBL- Klebsiella spp. was to sulfisoxazole (66.7%; 38/57). About 19% of ESBL-K lebsiella spp. were multidrug resistant. The presence of ESBL-producing Klebsiella spp. in dairy cattle, feed, and water obtained from troughs could play a crucial epidemiological role in maintaining and spreading the bacteria on farms and serving as a point source of transmission. IMPORTANCE We collected 572 samples from dairy farms, including rectal feces, manure, feed, and water. We isolated and identified extended-spectrum beta-lactamase (ESBL)- Klebsiella spp. and conducted an antimicrobial susceptibility test and analyzed different variables that may be associated with ESBL- Klebsiella spp. in dairy farms. The results of our study shed light on how ESBL- Klebsiella spp. are maintained through fecal-oral routes in dairy farms and possibly exit from the farm into the environment. We determine the prevalence of ESBL- Klebsiella spp. and their antimicrobial susceptibility profiles, underscoring their potential as a vehicle for multiple resistance gene dissemination within dairy farm settings. We also collected data on variables affecting their occurrence and spread in dairy farms. These findings have significant implications in determining sources of community-acquired ESBL- Enterobacteriaceae infections and designing appropriate control measures to prevent their spread from food animal production systems to humans, animals, and environments.