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. 2025 Jan 28;10(1):e0079324.
doi: 10.1128/msphere.00793-24. Epub 2024 Dec 31.

Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii group in Taiwan

Affiliations

Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii group in Taiwan

Tran Lam Tu Quyen et al. mSphere. .

Abstract

Acinetobacter, particularly the Acinetobacter baumannii group, is a major cause of nosocomial infections, and carbapenem-resistant Acinetobacter spp. are important human pathogens. We collected 492 Acinetobacter spp. strains from two hospitals in Taiwan and classified them using MALDI-TOF MS and blaOXA-51-like PCR; 94.5% were A. baumannii, and 5.5% were non-A. baumannii (NAB). We confirmed their identity by rpoB gene sequencing of 239 randomly selected A. baumannii strains and all 27 NAB strains. Our analysis revealed that the rpoB alleles of OXA51-like-negative strains matched those of two NAB species, A. seifertii and A. nosocomialis, while all OXA51-like-positive strains matched A. baumannii, as per the Pasteur MLST scheme database. Among the 492 strains, 240 exhibited carbapenem resistance, including 237 carbapenem-resistant A. baumannii (CRAB) strains and three CR-NAB strains. All CRAB strains were positive for blaOXA-51-like; 72.6% also carried blaOXA-23-like, 22.8% carried blaOXA-24-like, 3.4% co-carried blaOXA-23-like+blaOXA-24-like, and 1.27% carried blaOXA-51-like alone. Among the three CR-NAB strains, one carried blaNDM-1, and two co-carried blaOXA-58-like+blaIMP. We also established a new multiplex PCR method for rapid screening of common capsular types (KL), which showed a difference between CRAB and carbapenem-susceptible A. baumannii (CSAB). KL2, KL10, KL22, and KL52 accounted for 76.6% of CRAB strains, whereas about half of the CSAB strains were other KL types. Of the remaining CSAB strains, KL14 was the most predominant type at 10.3%. We further conducted MLST Pasteur typing for 262 isolates and found that the carbapenemase genes were correlated with either ST or KL types. Additionally, KL types showed correlations with ST types, carbapenem resistance, and certain clinical records. Whole-genome sequencing of a blaNDM-1-carrying A. seifertii strain revealed a plasmid transferable via in vitro conjugation, suggesting A. seifertii may be a reservoir for NDM-1 plasmids.IMPORTANCECarbapenem-resistant Acinetobacter spp. have been identified by the World Health Organization as a top priority for new antibiotic development. We established a rapid KL-typing method for efficient screening of Acinetobacter baumannii strains to enable epidemiological surveillance and provide a foundation for effective infection control. Our investigation of the molecular epidemiology of the A. baumannii group isolates revealed the prevalence of carbapenemase genes and major KL types among CR and CS strains of A. baumannii and NAB. We identified an A. seifertii strain carrying a Ti-type conjugative operon on a small plasmid that harbored genes encoding the NDM-1 carbapenemase alongside genes conferring resistance to aminoglycosides and bleomycin and closely resembled sequences detected in A. soli and A. pittii in Taiwan and China, respectively, suggesting its potential for transmitting multidrug resistance and contributing to the spread of antimicrobial resistance.

Keywords: Acinetobacter baumannii group; capsular types; carbapenemase genes; wzy multiplex PCR.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig 1
Fig 1
Genotyping characteristics of Acinetobacter baumannii (AB) group isolates. (A) Flowchart for the sample collection, genotypes, demographics, and species characteristics. A total of 492 samples from patients with bacteremia (either nosocomial or community-acquired) were analyzed in this study. Abbreviation: AB, Acinetobacter baumannii; NAB, non-A. baumannii; CRAB, carbapenem-resistant A. baumannii; CSAB, carbapenem-susceptible A. baumannii; CR-NAB carbapenem-resistant non-A. baumannii; CS-NAB, carbapenem-susceptible non-A. baumannii; MIC, minimum inhibitor concentration; IMP, Imipenem; MER, Meropenem; WGS, whole-genome sequence; MLST, multi-locus sequence type. (B) Capsular types (KL types), sequence types (ST types), and carbapenemase genes of 262 isolates, including 235 AB and 27 NAB isolates. The rpoB allele analysis (n = 266, including 239 AB + 27 NAB) was used to confirm species differentiation within the AB group.
Fig 2
Fig 2
Carbapenemase-producing strains over 7 years in Taiwan. (A) The percentage of isolates carrying carbapenemase genes, blaOXA-23-like, blaOXA-24-like, blaOXA-23-like+blaOXA-24-like, blaNDM-1 (shown in red color), and others (blaIMP+OXA-58, blaOXA-51-like only) in different years are displayed. The number of isolates is shown in parentheses. (B) MIC distribution of carbapenems among carbapenem-resistant (CR) isolates with different carbapenemase gene patterns (IMP, Imipenem; MER, Meropenem). The number of isolates carrying carbapenemase genes in different carbapenem MICs is displayed in each square.
Fig 3
Fig 3
Multiplex wzy PCR for rapid capsular typing. (A) Flow diagram of capsular typing using multiplex-three-stages wzy PCR. The size of each amplicon is indicated in text boxes. (B) Agarose gel electrophoresis (1.7%) was used for the separation of the different multiplex wzy PCR products. M1 multiplex detecting KL2 (KL2/81+ + cgmA-), KL81 (KL2/81+ + cgmA+); KL3 (KL22/3+ + cgmA-), KL22 (KL22/3+ + cgmA+); KL6 (KL6+ + cgmA-). M2 multiplex detecting KL9; KL10; KL14; KL52. M3 multiplex detecting KL1; KL47; KL49; lane “non−M1/2/3”, the PCR reaction was a mixture of M1, M2, or M3 primers with DNA of KL33. ddH2O was used as a negative control. M, 100 bp DNA ladder.
Fig 4
Fig 4
Percentage of variants of capsular types (KL) among 492 Acinetobacter spp. isolates. (A) The distribution KL of carbapenem-resistant Acinetobacter spp. (CRA) and carbapenem-susceptible Acinetobacter spp. (CSA) from 2015 to 2021. The number of isolates is shown in parentheses. (B) The comparison of variants of KL types between A. baumannii (AB) and non-A. baumannii (NAB) among carbapenem-resistant Acinetobacter (CRA) and carbapenem-susceptible Acinetobacter (CSA) isolates.
Fig 5
Fig 5
Comparison of pAS39-2 and other NDM-1-positive plasmids. (A) Comparative linear map of plasmid pAS39-2 and pM131_NDM1 plasmids. Arrows indicate the extent and directions of genes and ORFs. The blaNDM-1 gene is colored in red, and the other genes are colored according to their annotated functions: pink, antimicrobial resistance genes; yellow, genes with homology to conjugative transfer or type IV secretion system genes; dark blue and light blue, transposases encoded by full-copy IS elements and transposases without their corresponding IS elements or transposons in full, respectively; green, other functions and hypothetical protein-encoding genes. The extent of regions with >99% nucleotide sequence identities is indicated in the gray-shaded area. (B) Comparative map of the regions surrounding the blaNDM-1 gene in other Acinetobacter plasmids. Arrows indicate the extent and directions of the genes and ORFs. Accession numbers for the comparative map are as follows: pAP_D499 (accession no. NZ_AGFH01000030; nt 7,154–28,210); p6200-47.274kb (accession no. CP010399; nt 37,973–47 and continued from nt 3–10,798); pNDM-BJ02 (accession no. JQ060896; nt 454–20,404); pAbNDM-1 (accession no. JN377410; nt 454–22,697). The extent of regions with nucleotide sequence identities of between 96% and 100% is shown in gray.

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