Proteus mirabilis (P. mirabilis) is a Gram-negative, motile opportunistic pathogen with a broad host range. It causes both community- and hospital-acquired infections and is increasingly detected in poultry and food chains, raising food-safety concerns. This study systematically evaluated the prevalence, antimicrobial-susceptibility profiles, and the distribution of resistance genes, virulence-associated genes (VAGs), and metal-tolerance genes in chicken-derived P. mirabilis in Hunan Province. From June 2022 to January 2025, 1,679 chicken cloacal swabs were collected in Hunan; 192 P. mirabilis isolates were recovered (prevalence 11.44%). Antimicrobial-susceptibility testing (AST) was performed on a simple random sample of 118 isolates (118/192, 61.5%) using CLSI-recommended disk diffusion. The results showed that the MDR rate was 72.0% (85/118). Resistance was most frequent to Trimethoprim - Sulfamethoxazole (SXT) (81.4%), Ampicillin (AMP) (79.7%), Ciprofloxacin (CIP) (78.0%), and Gentamicin (GEN) (75.4%), followed by Neomycin (NEO) (63.6%) and Chloramphenicol (CHL) (61.0%). Carbapenem resistance was detected in a subset of isolates, including meropenem (MEM) (6.8%) and imipenem (IPM) (11.0%). Resistance-gene screening identified high prevalence of plasmid-mediated quinolone resistance (PMQR) determinants qnrA 58.9% (113/192) and aac(6')-Ib-cr 59.9% (115/192). The carbapenemase gene blaNDM-1 was detected in 10.4% (20/192) of isolates, and 24.0% (46/192) were positive for vanA. Markers associated with class 1 integrons, including qacEΔ1 and the integrase intI1, were detected in 71.9% and 49.5% of isolates, respectively. Furthermore, copper-tolerance genes copB and pcoA were detected in 49.5% and 10.4% of isolates, respectively. In summary, poultry-derived P. mirabilis in Hunan demonstrated high MDR prevalence and frequent carriage of resistance-, virulence-, and environment-related markers. Our findings enrich the epidemiological data on Proteus mirabilis at the farm level and provide scientific guidance for the prevention and control of this disease.
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