Comparative genomic surveillance of carbapenem-resistant <i>Acinetobacter baumannii</i> in the Netherlands in 2015–2017 and 2022–2024

We investigated the genomic epidemiology of carbapenem-resistant <i>Acinetobacter baumannii</i> (CRAb) during two surveillance periods: 2015-2017 (pilot 1) and 2022-2024 (pilot 2) in an international context to identify potential circulating high-risk lineages in the Netherlands. A total of 204 CRAb isolates were all analyzed by the carbapenem inactivation method, meropenem Etest, and whole-genome sequencing (combining Illumina and Nanopore). Comparative resistome, multilocus sequence typing (MLST), and whole-genome MLST (wgMLST) analyses were performed between pilots and compared to 577 international CRAb genomes. The Dutch CRAb population remained genetically diverse and stable between pilots and was dominated by international clone (IC)2 (61.8%), followed by IC9 (11.3%), IC1 (6.4%), and IC6 (5.9%). Also, epidemiological and clinical characteristics remained stable across both pilots. In contrast, CRAb in patients from Ukraine was genetically diverse and an epidemiologically distinct group. wgMLST indicated an increase in genetic clustering in 2022-2024, with unique CRAb clusters associated with Ukrainian patients. Of 26 identified clusters, 69% were linked to international sources. Differences in resistomes were observed between CRAb in patients from the Netherlands and Ukraine, and between pilots. Overall, 75% of isolates harbored <i>bla</i>_OXA-23-like genes, and <i>bla</i>_NDM genes increased from 16% to 21%. None of the CRAb isolates from Ukrainian patients carried <i>bla</i>_NDM genes; instead, they harbored <i>bla</i>_OXA-23-like and <i>bla</i>_OXA-24-like genes. Hybrid assemblies showed that carbapenemase genes were predominantly chromosomal. In conclusion, CRAb in the Netherlands showed genetic stability over time, yet the presence of New Delhi metallo-β-lactamase-carbapenemases and import of strains from high-risk regions underline the necessity for ongoing national surveillance.IMPORTANCEIn 2015-2017 and 2022-2024, pilot surveillance of carbapenem-resistant <i>Acinetobacter baumannii</i> (CRAb) was performed in the Netherlands. Three distinct groups were compared based on epidemiological and genomic data: CRAb from 2015 to 2017 and for the 2022-2024 period, CRAb in patients from the Netherlands, and CRAb in patients from Ukraine in the Netherlands. The genomic epidemiology of CRAb has been mostly stable between 2015-2017 and 2022-2024 but seems to be strongly affected by the introduction of CRAb from foreign countries. A proportion of the 2022-2024 isolates were from Ukrainian patients. The resistance genes of CRAb from Ukrainian patients were different from those of the Netherlands. CRAb in the Netherlands are acquiring New Delhi metallo-β-lactamase-carbapenemase genes, aided by the introduction of CRAb from foreign countries. Healthcare professionals should remain aware of the risk of hospitalization in a high-risk country and the potential secondary transmission of CRAb to patients in countries with a low prevalence of this organism.