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      Temporo-spatial variations in resistance determinants and clonality of Acinetobacter baumannii and Pseudomonas aeruginosa strains from Romanian hospitals and wastewaters

      research-article
      1 , 2 , 1 , 2 , , 2 , 3 , 7 , 2 , 2 , 1 , 2 , 4 , 4 , 4 , 4 , 4 , 5 , 6 , 5 , 5 , 5 , 7 , 6 , 7 , 7 , 7 , 6 , 7 , 5 , 1 , 2 , 8
      Antimicrobial Resistance and Infection Control
      BioMed Central
      Antimicrobial resistance, Nonfermenting gram-negative Bacilli, Nosocomial infections, Wastewater, Epidemic clones

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          Abstract

          Background

          Romania is one of the European countries reporting very high antimicrobial resistance (AMR) rates and consumption of antimicrobials. We aimed to characterize the AMR profiles and clonality of 304 multi-drug resistant (MDR) Acinetobacter baumannii ( Ab) and Pseudomonas aeruginosa ( Pa) strains isolated during two consecutive years (2018 and 2019) from hospital settings, hospital collecting sewage tanks and the receiving wastewater treatment plants (WWTPs) located in the main geographical regions of Romania.

          Methods

          The strains were isolated on chromogenic media and identified by MALDI-TOF-MS. Antibiotic susceptibility testing and confirmation of ESBL- and CP- producing phenotypes and genotypes were performed. The genetic characterization also included horizontal gene transfer experiments, whole-genome sequencing (WGS), assembling, annotation and characterization.

          Results

          Both clinical and aquatic isolates exhibited high MDR rates, especially the Ab strains isolated from nosocomial infections and hospital effluents. The phenotypic resistance profiles and MDR rates have largely varied by sampling point and geographic location. The highest MDR rates in the aquatic isolates were recorded in Galați WWTP, followed by Bucharest. The Ab strains harbored mostly bla OXA-23, bla OXA-24, bla SHV, bla TEM and bla GES, while Pa strains bla IMP, bla VIM, bla NDM, bla VEB, bla GES and bla TEM, with high variations depending on the geographical zone and the sampling point. The WGS analysis revealed the presence of antibiotic resistance genes (ARGs) to other antibiotic classes, such as aminoglycosides, tetracyclines, sulphonamides, fosfomycin, phenicols, trimethoprim-sulfamethoxazole as well as class 1 integrons. The molecular analyses highlighted: (i) The presence of epidemic clones such as ST2 for Ab and ST233 and ST357 for Pa; (ii) The relatedness between clinical and hospital wastewater strains and (iii) The possible dissemination of clinical Ab belonging to ST2 (also proved in the conjugation assays for bla OXA-23 or bla OXA-72 genes), ST79 and ST492 and of Pa strains belonging to ST357, ST640 and ST621 in the wastewaters.

          Conclusion

          Our study reveals the presence of CP-producing Ab and Pa in all sampling points and the clonal dissemination of clinical Ab ST2 strains in the wastewaters. The prevalent clones were correlated with the presence of class 1 integrons, suggesting that these isolates could be a significant reservoir of ARGs, being able to persist in the environment.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s13756-022-01156-1.

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          Most cited references61

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          RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

          Motivation: Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next-generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community. Results: I present some of the most notable new features and extensions of RAxML, such as a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date 50-page user manual covering all new RAxML options is available. Availability and implementation: The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML. Contact: alexandros.stamatakis@h-its.org Supplementary information: Supplementary data are available at Bioinformatics online.
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            Prokka: rapid prokaryotic genome annotation.

            T Seemann (2014)
            The multiplex capability and high yield of current day DNA-sequencing instruments has made bacterial whole genome sequencing a routine affair. The subsequent de novo assembly of reads into contigs has been well addressed. The final step of annotating all relevant genomic features on those contigs can be achieved slowly using existing web- and email-based systems, but these are not applicable for sensitive data or integrating into computational pipelines. Here we introduce Prokka, a command line software tool to fully annotate a draft bacterial genome in about 10 min on a typical desktop computer. It produces standards-compliant output files for further analysis or viewing in genome browsers. Prokka is implemented in Perl and is freely available under an open source GPLv2 license from http://vicbioinformatics.com/. © The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.
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              Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.

              Many different definitions for multidrug-resistant (MDR), extensively drug-resistant (XDR) and pandrug-resistant (PDR) bacteria are being used in the medical literature to characterize the different patterns of resistance found in healthcare-associated, antimicrobial-resistant bacteria. A group of international experts came together through a joint initiative by the European Centre for Disease Prevention and Control (ECDC) and the Centers for Disease Control and Prevention (CDC), to create a standardized international terminology with which to describe acquired resistance profiles in Staphylococcus aureus, Enterococcus spp., Enterobacteriaceae (other than Salmonella and Shigella), Pseudomonas aeruginosa and Acinetobacter spp., all bacteria often responsible for healthcare-associated infections and prone to multidrug resistance. Epidemiologically significant antimicrobial categories were constructed for each bacterium. Lists of antimicrobial categories proposed for antimicrobial susceptibility testing were created using documents and breakpoints from the Clinical Laboratory Standards Institute (CLSI), the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and the United States Food and Drug Administration (FDA). MDR was defined as acquired non-susceptibility to at least one agent in three or more antimicrobial categories, XDR was defined as non-susceptibility to at least one agent in all but two or fewer antimicrobial categories (i.e. bacterial isolates remain susceptible to only one or two categories) and PDR was defined as non-susceptibility to all agents in all antimicrobial categories. To ensure correct application of these definitions, bacterial isolates should be tested against all or nearly all of the antimicrobial agents within the antimicrobial categories and selective reporting and suppression of results should be avoided. © 2011 European Society of Clinical Microbiology and Infectious Diseases. No claim to original US government works.
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                Author and article information

                Contributors
                iryna_84@yahoo.com
                ilda.barbu@bio.unibuc.ro
                lpbio_laura@yahoo.com
                gratiela87@gmail.com
                bmarcelica@yahoo.com
                lumi.marutescu@gmail.com
                mihai.nita@incdecoind.ro
                alina.banciu@incdecoind.ro
                catalina.stoica@incdecoind.ro
                stefania.gheorghe@incdecoind.ro
                bioteste.ecoind@gmail.com
                oanasandulescu1@gmail.com
                mona_manaila@yahoo.com
                marius.surleac@gmail.com
                dtalapan@gmail.com
                muntean.alex@gmail.com
                madalina.prd@gmail.com
                mmada.muntean@gmail.com
                ceraseladragomirescu@yahoo.com
                mircea.ioan.popa@gmail.com
                dotelea@mateibals.ro
                carmen_balotescu@yahoo.com
                Journal
                Antimicrob Resist Infect Control
                Antimicrob Resist Infect Control
                Antimicrobial Resistance and Infection Control
                BioMed Central (London )
                2047-2994
                14 September 2022
                14 September 2022
                2022
                : 11
                : 115
                Affiliations
                [1 ]GRID grid.5100.4, ISNI 0000 0001 2322 497X, Department of Microbiology and Immunology, Faculty of Biology, , University of Bucharest, ; Bucharest, Romania
                [2 ]GRID grid.5100.4, ISNI 0000 0001 2322 497X, Research Institute of the University of Bucharest (ICUB), ; Bucharest, Romania
                [3 ]GRID grid.435400.6, ISNI 0000 0004 0369 4845, National Institute of Research and Development for Biological Sciences, ; Bucharest, Romania
                [4 ]GRID grid.493449.7, ISNI 0000 0001 0604 2859, National Research and Development Institute for Industrial Ecology (INCD ECOIND), ; Bucharest, Romania
                [5 ]GRID grid.8194.4, ISNI 0000 0000 9828 7548, National Institute for Infectious Diseases ‘Matei Bals’, ; Bucharest, Romania
                [6 ]GRID grid.8194.4, ISNI 0000 0000 9828 7548, University of Medicine and Pharmacy “Carol Davila”, ; Bucharest, Romania
                [7 ]“Cantacuzino” National Medical-Military Research and Development Institute, Bucharest, Romania
                [8 ]GRID grid.418333.e, ISNI 0000 0004 1937 1389, Romanian Academy, ; 050045 Bucharest, Romania
                Article
                1156
                10.1186/s13756-022-01156-1
                9476303
                36104761
                b362695f-0b9a-4c93-af28-5e1e03640357
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 25 January 2022
                : 26 August 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100006595, Unitatea Executiva pentru Finantarea Invatamantului Superior, a Cercetarii, Dezvoltarii si Inovarii;
                Award ID: PN-III-P1.1-PD-2016-1798
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P4-ID-PCCF-2016-0114
                Award ID: PN-III-P1.1-PD-2016-1798
                Award Recipient :
                Funded by: Ministerul Cercetarii, Inovarii si Digitalizarii, Romania
                Award ID: C1.2.PFE-CDI.2021-587
                Award ID: C1.2.PFE-CDI.2021-587
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2022

                Infectious disease & Microbiology
                antimicrobial resistance,nonfermenting gram-negative bacilli,nosocomial infections,wastewater,epidemic clones

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