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

Abstract

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.

Competing Interest Statement

The authors have declared no competing interest.

Funding Statement

This work was supported by the NIH/NIAID grant number K08 AI148582 and the UAB IMPACT award to J.J.C.

Author Declarations

I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained.

Yes

The details of the IRB/oversight body that provided approval or exemption for the research described are given below:

This study was approved by the University of Alabama at Birmingham (UAB) Institutional Review Board (IRB# 30003572 and 30008212.

I confirm that all necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived, and that any patient/participant/sample identifiers included were not known to anyone (e.g., hospital staff, patients or participants themselves) outside the research group so cannot be used to identify individuals.

Yes

I understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance).

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I have followed all appropriate research reporting guidelines, such as any relevant EQUATOR Network research reporting checklist(s) and other pertinent material, if applicable.

Yes

Data Availability

All raw sequence files and assemblies derived from UAB study strains are available under NCBI BioProject PRJNA1005294. All other data in the present study are available upon reasonable request to the corresponding author.

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