Multicenter genomic analysis reveals environmental hotspots and near-clonal subclusters of Acinetobacter baumannii in veterinary hospitals in Beijing, China.

INTRODUCTION: Acinetobacter baumannii is a major healthcare-associated opportunistic pathogen with exceptional environmental persistence. However, its ecological distribution and potential transmission pathways in veterinary hospital environments remain poorly characterized.

METHODS: Samples were collected from multiple departments and surface types across eight veterinary hospitals in Beijing from September to December 2020. A. baumannii isolates were recovered and subjected to antimicrobial susceptibility testing and whole-genome sequencing. Environmental risk factors were assessed using generalized linear mixed-effects models (GLMMs) with a binomial distribution and logit link, with hospital included as a random intercept and sampling site and department as fixed effects. Genomic analyses included profiling of antimicrobial resistance genes, virulence factors, and biocide/metal resistance genes, as well as Bayesian population structure and cgMLST to infer potential transmission patterns.

RESULTS: Among 1,136 environmental samples collected across eight veterinary hospitals in Beijing, 64 A. baumannii isolates were recovered, with an overall isolation rate of 5.63% and hospital-level rates ranging from 0.54% to 15.33%. The X-ray room showed the highest observed department-level isolation rate (16.36%, 9/55) and was significantly associated with increased A. baumannii recovery compared with the clinic room reference category in the multivariable GLMM. Floors (12.40%, 31/250), sinks (9.80%, 10/102), and staff uniforms (9.73%, 11/113) showed the highest surface-level isolation rates and were significantly associated with increased recovery compared with the door reference category (all P < 0.05). Most isolates were susceptible to the tested antimicrobial agents, while ceftriaxone showed the highest non-susceptibility rate (43.8% intermediate, 4.7% resistant). Two isolates were multidrug-resistant, including one carrying a 7,561-bp resistance region with a class 1 integron cassette array (aadA1-cmlA-aadA2-bla PSE-1). Whole-genome analysis revealed a conserved baseline resistome, core virulence determinants related to adhesion, biofilm formation, nutrient acquisition, regulation, and secretion systems, as well as broadly distributed metal tolerance and oxidative-stress defense genes. In contrast, accessory ARGs, VFs, and disinfectant- or metal-associated resistance determinants showed lineage- or isolate-specific variability. Bayesian population structure analysis resolved nine BAPS lineages with distinct spatial distribution patterns, including hospital-restricted, locally shared, and spatially dispersed lineages. cgMLST further identified hospital-specific near-clonal subclusters within these lineages, defined by ≤8 allelic differences and 0-3 core-genome SNPs. These subclusters were detected across multiple departments and environmental surfaces within the same hospital, indicating broad within-hospital environmental distribution of highly related isolates.

CONCLUSIONS: This study demonstrates heterogeneous environmental contamination of A. baumannii in veterinary hospitals, with higher recovery from X-ray rooms, wet sites, staff uniforms, floors, and other shared or frequently contacted surfaces. Although most isolates were not multidrug-resistant, they carried conserved resistance-, virulence-, and environmental survival-associated genomic determinants, suggesting that their ecological risk may be related to surface survival, stress tolerance, and redistribution within hospital environments rather than widespread MDR clone dissemination. Population structure and cgMLST analyses revealed both inter-hospital lineage sharing and hospital-specific near-clonal subclusters, indicating the presence of highly related A. baumannii isolates across multiple departments and environmental surfaces within individual hospitals. These findings highlight the need to incorporate environmental opportunistic bacteria such as A. baumannii into veterinary hospital surveillance and infection prevention and control planning, particularly in high-use functional areas, wet zones, staff uniforms, shared equipment, and high-touch surfaces.