Epidemiological, phylogenetic, and resistance heterogeneity among Acinetobacter baumannii in a major US Deep South healthcare center

Acinetobacter baumannii (Ab) disease in the U.S. is commonly attributed to outbreaks of one or two monophyletic carbapenem resistance (CR) Ab lineages that vary by region. However, there is limited knowledge regarding Ab epidemiology and population structure in the U.S. Deep South, and few studies compare contemporary CR and carbapenem-susceptible (Cs) Ab, despite prevalence of the latter. We performed a 12-year time series analysis of Ab cases in a large hospital in Birmingham, AL, and 89 isolates from an ongoing surveillance project started in November 2021 were analyzed by whole genome sequencing and antibiotic susceptibility testing (AST). Cumulative CR rate among 2462 cases since 2011 was 19.4%, with increased rates during winter months resulting from seasonal changes in CsAb incidence. Sequenced CRAb belonged to clonal complex (CC) 1, CC108, CC250, CC2, and CC499. Most CRAb CCs were comprised of isolates that clustered apart from U.S. counterparts in phylogenetic analysis, despite being identified in unrelated cases occurring [≥]3 months apart. In contrast, 38/47 (81%) CsAb isolates each belonged to a distinct CC. CRAb isolates displayed lineage-distinct AST features, including unique carbapenem resistance genetic determinants and presumptive heteroresistance behaviors unique to CC108 and CC499 isolates. This first comprehensive analysis of Ab cases in the U.S. Deep South revealed epidemiological trends consistent with those in other regions and an unusually high degree of phylogenetic diversity among regional CRAb isolates. We also describe emergent U.S. CRAb lineages whose unconventional antimicrobial resistance features must be integrated into ongoing diagnostic, treatment, and surveillance efforts.