Epidemiology, resistance genomics and susceptibility of <i>Acinetobacter</i> species: results from the 2020 Spanish nationwide surveillance study

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Abstract

Background

As increasing antibiotic resistance in Acinetobacter baumannii poses a global healthcare challenge, understanding its evolution is crucial for effective control strategies.

Aim

We aimed to evaluate the epidemiology, antimicrobial susceptibility and main resistance mechanisms of Acinetobacter spp. in Spain in 2020, and to explore temporal trends of A. baumannii.

Methods

We collected 199 single-patient Acinetobacter spp. clinical isolates in 2020 from 18 Spanish tertiary hospitals. Minimum inhibitory concentrations (MICs) for nine antimicrobials were determined. Short-read sequencing was performed for all isolates, and targeted long-read sequencing for A. baumannii. Resistance mechanisms, phylogenetics and clonality were assessed. Findings on resistance rates and infection types were compared with data from 2000 and 2010.

Results

Cefiderocol and colistin exhibited the highest activity against A. baumannii, although colistin susceptibility has significantly declined over 2 decades. A. non- baumannii strains were highly susceptible to most tested antibiotics. Of the A. baumannii isolates, 47.5% (56/118) were multidrug-resistant (MDR). Phylogeny and clonal relationship analysis of A. baumannii revealed five prevalent international clones, notably IC2 (ST2, n = 52; ST745, n = 4) and IC1 (ST1, n = 14), and some episodes of clonal dissemination. Genes bla _OXA-23, bla _OXA-58 and bla _OXA-24/40 were identified in 49 (41.5%), eight (6.8%) and one (0.8%) A. baumannii isolates, respectively. IS Aba1 was found upstream of the gene (a bla _OXA-51-like ₎ in 10 isolates.

Conclusions

The emergence of OXA-23-producing ST1 and ST2, the predominant MDR lineages, shows a pivotal shift in carbapenem-resistant A. baumannii (CRAB) epidemiology in Spain. Coupled with increased colistin resistance, these changes underscore notable alterations in regional antimicrobial resistance dynamics.

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Most cited references 36

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Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel (2014)

Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes

Donovan Parks, Michael Imelfort, Connor Skennerton … (2015)

Large-scale recovery of genomes from isolates, single cells, and metagenomic data has been made possible by advances in computational methods and substantial reductions in sequencing costs. Although this increasing breadth of draft genomes is providing key information regarding the evolutionary and functional diversity of microbial life, it has become impractical to finish all available reference genomes. Making robust biological inferences from draft genomes requires accurate estimates of their completeness and contamination. Current methods for assessing genome quality are ad hoc and generally make use of a limited number of “marker” genes conserved across all bacterial or archaeal genomes. Here we introduce CheckM, an automated method for assessing the quality of a genome using a broader set of marker genes specific to the position of a genome within a reference genome tree and information about the collocation of these genes. We demonstrate the effectiveness of CheckM using synthetic data and a wide range of isolate-, single-cell-, and metagenome-derived genomes. CheckM is shown to provide accurate estimates of genome completeness and contamination and to outperform existing approaches. Using CheckM, we identify a diverse range of errors currently impacting publicly available isolate genomes and demonstrate that genomes obtained from single cells and metagenomic data vary substantially in quality. In order to facilitate the use of draft genomes, we propose an objective measure of genome quality that can be used to select genomes suitable for specific gene- and genome-centric analyses of microbial communities.

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Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain

Keith Jolley, Carly M. Bliss, Julia S. Bennett … (2012)

No single genealogical reconstruction or typing method currently encompasses all levels of bacterial diversity, from domain to strain. We propose ribosomal multilocus sequence typing (rMLST), an approach which indexes variation of the 53 genes encoding the bacterial ribosome protein subunits (rps genes), as a means of integrating microbial genealogy and typing. As with multilocus sequence typing (MLST), rMLST employs curated reference sequences to identify gene variants efficiently and rapidly. The rps loci are ideal targets for a universal characterization scheme as they are: (i) present in all bacteria; (ii) distributed around the chromosome; and (iii) encode proteins which are under stabilizing selection for functional conservation. Collectively, the rps loci exhibit variation that resolves bacteria into groups at all taxonomic and most typing levels, providing significantly more resolution than 16S small subunit rRNA gene phylogenies. A web-accessible expandable database, comprising whole-genome data from more than 1900 bacterial isolates, including 28 draft genomes assembled de novo from the European Bioinformatics Institute (EBI) sequence read archive, has been assembled. The rps gene variation catalogued in this database permits rapid and computationally non-intensive identification of the phylogenetic position of any bacterial sequence at the domain, phylum, class, order, family, genus, species and strain levels. The groupings generated with rMLST data are consistent with current nomenclature schemes and independent of the clustering algorithm used. This approach is applicable to the other domains of life, potentially providing a rational and universal approach to the classification of life that is based on one of its fundamental features, the translation mechanism.

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Author and article information

Journal

Journal ID (nlm-ta): Euro Surveill

Journal ID (iso-abbrev): Euro Surveill

Journal ID (publisher-id): eurosurveillance

Title: Eurosurveillance

Publisher: European Centre for Disease Prevention and Control (ECDC)

ISSN (Print): 1025-496X

ISSN (Electronic): 1560-7917

Publication date (Print): 11 April 2024

Volume: 29

Issue: 15

Electronic Location Identifier: 2300352

Affiliations

[1 ]Microbiology Department, A Coruña University Hospital (CHUAC), Institute of Biomedical Research of A Coruña (INIBIC), Spain

[2 ]NANOBIOFAR, Centre for Research in Molecular Medicine and Chronic Diseases (CiMUS), Universidad de Santiago de Compostela, Santiago de Compostela, Spain

[3 ]Department of Computer Science and Information Technologies, Faculty of Computer Science, Research Center of Information and Communication Technologies (CITIC), University of A Coruña, A Coruña, Spain

[4 ]CIBER de Enfermedades Infecciosas (CIBERINFEC), A Coruña, Spain

Author notes

[*]

These authors contributed equally to this work and share first authorship.

[**]

These authors contributed equally to this work and share last authorship.

Correspondence: Juan Carlos Vázquez-Ucha ( Juan.Carlos.Vazquez.Ucha@ 123456sergas.es )

Author information

Cristina Lasarte-Monterrubio https://orcid.org/0000-0003-3351-2064

Paula Guijarro-Sánchez https://orcid.org/0000-0002-8456-0085

Isaac Alonso-Garcia https://orcid.org/0000-0002-1681-969X

Michelle Outeda https://orcid.org/0000-0002-6737-0239

Lucia González-Pinto https://orcid.org/0000-0002-8387-3784

Marta Martínez-Guitián https://orcid.org/0000-0002-3457-0613

Juan Carlos Vázquez-Ucha https://orcid.org/0000-0003-4949-0779

Jorge Arca-Suárez https://orcid.org/0000-0002-4248-503X

Alejandro Beceiro https://orcid.org/0000-0002-6340-7815

Article

Publisher ID: 2300352 Publisher ID: 2300352

DOI: 10.2807/1560-7917.ES.2024.29.15.2300352

PMC ID: 11010588

PubMed ID: 38606569

SO-VID: ef79f7cf-59b5-4bd8-b4fa-d47a07a66beb

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution (CC BY 4.0) Licence. You may share and adapt the material, but must give appropriate credit to the source, provide a link to the licence, and indicate if changes were made.

History

Date received : 10 July 2023

Date accepted : 13 December 2023

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sequence 153

Keywords: acinetobacter spp.,acinetobacter baumannii,epidemiology,antimicrobial susceptibility,wgs,chdls

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Keywords: acinetobacter spp., acinetobacter baumannii, epidemiology, antimicrobial susceptibility, wgs, chdls

Epidemiology, resistance genomics and susceptibility of Acinetobacter species: results from the 2020 Spanish nationwide surveillance study

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Most cited references 36

Trimmomatic: a flexible trimmer for Illumina sequence data

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes

Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain

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