1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 15, 11/Apr/2024
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

As increasing antibiotic resistance in 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 spp. in Spain in 2020, and to explore temporal trends of .

Methods

We collected 199 single-patient 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 . 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 , although colistin susceptibility has significantly declined over 2 decades. non- strains were highly susceptible to most tested antibiotics. Of the isolates, 47.5% (56/118) were multidrug-resistant (MDR). Phylogeny and clonal relationship analysis of 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 , and were identified in 49 (41.5%), eight (6.8%) and one (0.8%) isolates, respectively. IS1 was found upstream of the gene (a -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 (CRAB) epidemiology in Spain. Coupled with increased colistin resistance, these changes underscore notable alterations in regional antimicrobial resistance dynamics.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.15.2300352
2024-04-11
2024-04-29
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.15.2300352
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/15/eurosurv-29-15_3.html?itemId=/content/10.2807/1560-7917.ES.2024.29.15.2300352&mimeType=html&fmt=ahah

References

  1. Wong D, Nielsen TB, Bonomo RA, Pantapalangkoor P, Luna B, Spellberg B. Clinical and pathophysiological overview of Acinetobacter infections: A century of challenges. Clin Microbiol Rev. 2017;30(1):409-47.  https://doi.org/10.1128/CMR.00058-16  PMID: 27974412 
  2. Tamma PD, Aitken SL, Bonomo RA, Mathers AJ, van Duin D, Clancy CJ. Infectious diseases society of America guidance on the treatment of AmpC β-Lactamase-producing Enterobacterales, Carbapenem-resistant Acinetobacter baumannii, and Stenotrophomonas maltophilia infections. Clin Infect Dis. 2022;74(12):2089-114.  https://doi.org/10.1093/cid/ciab1013  PMID: 34864936 
  3. Uppalapati SR, Sett A, Pathania R. The outer membrane proteins OmpA, CarO, and OprD of Acinetobacter baumannii confer a two-pronged defense in facilitating its success as a potent human Pathogen. Front Microbiol. 2020;11:589234.  https://doi.org/10.3389/fmicb.2020.589234  PMID: 33123117 
  4. Roy S, Junghare V, Dutta S, Hazra S, Basu S. Differential binding of carbapenems with the AdeABC efflux pump and modulation of the expression of AdeB linked to novel mutations within two-component system AdeRS in Carbapenem-resistant Acinetobacter baumannii. mSystems. 2022;7(4):e0021722.  https://doi.org/10.1128/msystems.00217-22  PMID: 35735748 
  5. Penwell WF, Shapiro AB, Giacobbe RA, Gu RF, Gao N, Thresher J, et al. Molecular mechanisms of sulbactam antibacterial activity and resistance determinants in Acinetobacter baumannii. Antimicrob Agents Chemother. 2015;59(3):1680-9.  https://doi.org/10.1128/AAC.04808-14  PMID: 25561334 
  6. Chiu CH, Lee HY, Tseng LY, Chen CL, Chia JH, Su LH, et al. Mechanisms of resistance to ciprofloxacin, ampicillin/sulbactam and imipenem in Acinetobacter baumannii clinical isolates in Taiwan. Int J Antimicrob Agents. 2010;35(4):382-6.  https://doi.org/10.1016/j.ijantimicag.2009.12.009  PMID: 20138741 
  7. Krizova L, Poirel L, Nordmann P, Nemec A. TEM-1 β-lactamase as a source of resistance to sulbactam in clinical strains of Acinetobacter baumannii. J Antimicrob Chemother. 2013;68(12):2786-91.  https://doi.org/10.1093/jac/dkt275  PMID: 23838947 
  8. Trebosc V, Gartenmann S, Tötzl M, Lucchini V, Schellhorn B, Pieren M, et al. Dissecting colistin resistance mechanisms in extensively drug-resistant Acinetobacter baumannii clinical isolates. MBio. 2019;10(4):1-12.  https://doi.org/10.1128/mBio.01083-19  PMID: 31311879 
  9. Moffatt JH, Harper M, Adler B, Nation RL, Li J, Boyce JD. Insertion sequence ISAba11 is involved in colistin resistance and loss of lipopolysaccharide in Acinetobacter baumannii. Antimicrob Agents Chemother. 2011;55(6):3022-4.  https://doi.org/10.1128/AAC.01732-10  PMID: 21402838 
  10. Malik S, Kaminski M, Landman D, Quale J. Cefiderocol resistance in Acinetobacter baumannii: roles of β-lactamases, siderophore receptors, and penicillin binding protein 3. Antimicrob Agents Chemother. 2020;64(11):e01221-20.  https://doi.org/10.1128/AAC.01221-20  PMID: 32868330 
  11. Poirel L, Sadek M, Nordmann P. Contribution of PER-type and NDM-type beta-lactamases to cefiderocol resistance in Acinetobacter baumannii. Antimicrob Agents Chemother. 2021;65(10):e0087721.  https://doi.org/10.1128/AAC.00877-21  PMID: 34252309 
  12. Fernández-Cuenca F, Pascual A, Ribera A, Vila J, Bou G, Cisneros JM, et al. Diversidad clonal y sensibilidad a los antimicrobianos de Acinetobacter baumannii aislados en hospitales españoles. Estudio multicéntrico nacional: proyecto GEIH-Ab 2000. [Clonal diversity and antimicrobial susceptibility of Acinetobacter baumannii isolated in Spain. A nationwide multicenter study: GEIH-Ab project (2000)]. Enferm Infecc Microbiol Clin. 2004;22(5):267-71. Spanish.  https://doi.org/10.1016/S0213-005X(04)73085-2  PMID: 15207117 
  13. Rodríguez-Baño J, Cisneros JM, Fernández-Cuenca F, Ribera A, Vila J, Pascual A, et al. Clinical features and epidemiology of Acinetobacter baumannii colonization and infection in Spanish hospitals. Infect Control Hosp Epidemiol. 2004;25(10):819-24.  https://doi.org/10.1086/502302  PMID: 15518022 
  14. Fernández-Cuenca F, Tomás-Carmona M, Caballero-Moyano F, Bou G, Martínez-Martínez L, Vila J, et al. Actividad de 18 agentes antimicrobianos frente a aislados clínicos de Acinetobacter baumannii: segundo estudio nacional multicéntrico (proyecto GEIH-REIPI-Ab 2010). [In vitro activity of 18 antimicrobial agents against clinical isolates of Acinetobacter spp.: multicenter national study GEIH-REIPI-Ab 2010]. Enferm Infecc Microbiol Clin. 2013;31(1):4-9. Spanish.  https://doi.org/10.1016/j.eimc.2012.06.010  PMID: 22939566 
  15. Villar M, Cano ME, Gato E, Garnacho-Montero J, Miguel Cisneros J, Ruíz de Alegría C, et al. Epidemiologic and clinical impact of Acinetobacter baumannii colonization and infection: a reappraisal. Medicine (Baltimore). 2014;93(5):202-10.  https://doi.org/10.1097/MD.0000000000000036  PMID: 25181313 
  16. Clinical and Laboratory Standards Institute (CLSI). CLSI M100-ED32: Performance standards for antimicrobial susceptibility testing, 32rd Edition. Wayne, Pennsylvania: CLSI; 2022. Available from: https://clsi.org
  17. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20.  https://doi.org/10.1093/bioinformatics/btu170  PMID: 24695404 
  18. Poirel L, Naas T, Nordmann P. Diversity, epidemiology, and genetics of class D β-lactamases. Antimicrob Agents Chemother. 2010;54(1):24-38.  https://doi.org/10.1128/AAC.01512-08  PMID: 19721065 
  19. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25(7):1043-55.  https://doi.org/10.1101/gr.186072.114  PMID: 25977477 
  20. Schwengers O, Jelonek L, Dieckmann MA, Beyvers S, Blom J, Goesmann A. Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb Genom. 2021;7(11):000685.  https://doi.org/10.1099/mgen.0.000685  PMID: 34739369 
  21. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology (Reading). 2012;158(Pt 4):1005-15.  https://doi.org/10.1099/mic.0.055459-0  PMID: 22282518 
  22. R Core Team. R Commander (Version 4.2.3). Vienna: R Foundation for Statistical Computing; 2023. Available from: https://www.R-project.org
  23. Ruiz M, Marti S, Fernandez-Cuenca F, Pascual A, Vila J. Prevalence of IS(Aba1) in epidemiologically unrelated Acinetobacter baumannii clinical isolates. FEMS Microbiol Lett. 2007;274(1):63-6.  https://doi.org/10.1111/j.1574-6968.2007.00828.x  PMID: 17610514 
  24. Sociedad Española de Medicina Preventiva y Salud Pública. Estudio de Prevalencia de las Infecciones Nosocomiales en España (EPINE). [Prevalence study on nosocomial infections in Spain (EPINE)]. Majadahonda: Sociedad Española de Medicina Preventiva y Salud Pública. [Accessed: 9 Jun 2023]. Spanish. Available from: https://epine.es
  25. European Centre for Disease Prevention and Control (ECDC). Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals 2011-2012. Stockholm: ECDC; 2013. Available from: https://www.ecdc.europa.eu/en/publications-data/point-prevalence-survey-healthcare-associated-infections-and-antimicrobial-use-0
  26. European Centre for Disease Prevention and Control (ECDC). Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals 2016-2017. Stockholm: ECDC; 2023. Available from: https://www.ecdc.europa.eu/en/publications-data/point-prevalence-survey-healthcare-associated-infections-and-antimicrobial-use-5
  27. European Surveillance of Antimicrobial Consumption Network (ESAC-Net). Antimicrobial Consumption (AMC) Dashboard. Latest surveillance data on antimicrobial consumption. Stockholm: ECDC. [Accessed: 9 Jun 2023]. Available from: https://qap.ecdc.europa.eu/public/extensions/AMC2_Dashboard/AMC2_Dashboard.html#eu-consumption-tab
  28. Sastre-Femenia MÀ, Fernández-Muñoz A, Gomis-Font MA, Taltavull B, López-Causapé C, Arca-Suárez J, et al. Pseudomonas aeruginosa antibiotic susceptibility profiles, genomic epidemiology and resistance mechanisms: a nation-wide five-year time lapse analysis. Lancet Reg Health Eur. 2023;34:100736.  https://doi.org/10.1016/j.lanepe.2023.100736  PMID: 37753216 
  29. European Centre for Disease Prevention and Control (ECDC). Surveillance atlas of infectious diseases. Stockholm: ECDC. [Accessed: 19 Oct 2023]. Available from: https://atlas.ecdc.europa.eu/public/index.aspx
  30. Wohlfarth E, Kresken M, Higgins PG, Stefanik D, Wille J, Hafner D, et al. The evolution of carbapenem resistance determinants and major epidemiological lineages among carbapenem-resistant Acinetobacter baumannii isolates in Germany, 2010-2019. Int J Antimicrob Agents. 2022;60(5-6):106689.  https://doi.org/10.1016/j.ijantimicag.2022.106689  PMID: 36375774 
  31. Karlowsky JA, Hackel MA, McLeod SM, Miller AA. In vitro activity of Sulbactam-Durlobactam against global isolates of Acinetobacter baumannii-calcoaceticus complex collected from 2016 to 2021. Antimicrob Agents Chemother. 2022;66(9):e0078122.  https://doi.org/10.1128/aac.00781-22  PMID: 36005804 
  32. Castanheira M, Mendes RE, Gales AC. Global Epidemiology and mechanisms of resistance of Acinetobacter baumannii-calcoaceticus complex. Clin Infect Dis. 2023;76(2) Suppl 2;S166-78.  https://doi.org/10.1093/cid/ciad109  PMID: 37125466 
  33. Zarrilli R, Pournaras S, Giannouli M, Tsakris A. Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages. Int J Antimicrob Agents. 2013;41(1):11-9.  https://doi.org/10.1016/j.ijantimicag.2012.09.008  PMID: 23127486 
  34. Hamidian M, Nigro SJ. Emergence, molecular mechanisms and global spread of carbapenem-resistant Acinetobacter baumannii. Microb Genom. 2019;5(10):e000306.  https://doi.org/10.1099/mgen.0.000306  PMID: 31599224 
  35. Jeannot K, Diancourt L, Vaux S, Thouverez M, Ribeiro A, Coignard B, et al. Molecular epidemiology of carbapenem non-susceptible Acinetobacter baumannii in France. PLoS One. 2014;9(12):e115452.  https://doi.org/10.1371/journal.pone.0115452  PMID: 25517732 
  36. Tsai YK, Liou CH, Lin JC, Fung CP, Chang FY, Siu LK. Effects of different resistance mechanisms on antimicrobial resistance in Acinetobacter baumannii: a strategic system for screening and activity testing of new antibiotics. Int J Antimicrob Agents. 2020;55(4):105918.  https://doi.org/10.1016/j.ijantimicag.2020.105918  PMID: 32007593 
  37. Mosqueda N, Gato E, Roca I, López M, de Alegría CR, Fernández Cuenca F, et al. Characterization of plasmids carrying the blaOXA-24/40 carbapenemase gene and the genes encoding the AbkA/AbkB proteins of a toxin/antitoxin system. J Antimicrob Chemother. 2014;69(10):2629-33.  https://doi.org/10.1093/jac/dku179  PMID: 24879663 
  38. Koirala J, Tyagi I, Guntupalli L, Koirala S, Chapagain U, Quarshie C, et al. OXA-23 and OXA-40 producing carbapenem-resistant Acinetobacter baumannii in Central Illinois. Diagn Microbiol Infect Dis. 2020;97(1):114999.  https://doi.org/10.1016/j.diagmicrobio.2020.114999  PMID: 32059871 
  39. Pournaras S, Dafopoulou K, Del Franco M, Zarkotou O, Dimitroulia E, Protonotariou E, et al. Predominance of international clone 2 OXA-23-producing-Acinetobacter baumannii clinical isolates in Greece, 2015: results of a nationwide study. Int J Antimicrob Agents. 2017;49(6):749-53.  https://doi.org/10.1016/j.ijantimicag.2017.01.028  PMID: 28427842 
  40. Yang Y, Xu Q, Li T, Fu Y, Shi Y, Lan P, et al. OXA-23 is a prevalent mechanism contributing to sulbactam resistance in diverse Acinetobacter baumannii clinical strains. Antimicrob Agents Chemother. 2018;63(1):1-4. PMID: 30348663 
  41. Lasarte-Monterrubio C, Guijarro-Sánchez P, Bellés A, Vázquez-Ucha JC, Arca-Suárez J, Fernández-Lozano C, et al. Carbapenem resistance in Acinetobacter nosocomialis and Acinetobacter junii conferred by acquisition of blaoxa-24/40 and genetic characterization of the transmission mechanism between Acinetobacter genomic species. Microbiol Spectr. 2022;10(1):e0273421.  https://doi.org/10.1128/spectrum.02734-21  PMID: 35138195 
  42. Poirel L, Figueiredo S, Cattoir V, Carattoli A, Nordmann P. Acinetobacter radioresistens as a silent source of carbapenem resistance for Acinetobacter spp. Antimicrob Agents Chemother. 2008;52(4):1252-6.  https://doi.org/10.1128/AAC.01304-07  PMID: 18195058 
  43. Novović K, Jovčić B. Colistin resistance in Acinetobacter baumannii: molecular mechanisms and epidemiology. Antibiotics (Basel). 2023;12(3):516.  https://doi.org/10.3390/antibiotics12030516  PMID: 36978383 
Epidemiology, resistance genomics and susceptibility of Acinetobacter species: results from the 2020 Spanish nationwide surveillance study
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Cristina+Lasarte-Monterrubio&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lasarte-Monterrubio Cristina</a>, <a href="/search?value1=Paula+Guijarro-S%C3%A1nchez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Guijarro-Sánchez Paula</a>, <a href="/search?value1=Isaac+Alonso-Garcia&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Alonso-Garcia Isaac</a>, <a href="/search?value1=Michelle+Outeda&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Outeda Michelle</a>, <a href="/search?value1=Romina+Maceiras&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Maceiras Romina</a>, <a href="/search?value1=Lucia+Gonz%C3%A1lez-Pinto&option1=author&noRedirect=true" class="nonDisambigAuthorLink">González-Pinto Lucia</a>, <a href="/search?value1=Marta+Mart%C3%ADnez-Guiti%C3%A1n&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Martínez-Guitián Marta</a>, <a href="/search?value1=Carlos+Fern%C3%A1ndez-Lozano&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fernández-Lozano Carlos</a>, <a href="/search?value1=Juan+Carlos+V%C3%A1zquez-Ucha&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Vázquez-Ucha Juan Carlos</a>, <a href="/search?value1=German+Bou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bou German</a>, <a href="/search?value1=Jorge+Arca-Su%C3%A1rez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Arca-Suárez Jorge</a>, <a href="/search?value1=Alejandro+Beceiro&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Beceiro Alejandro</a></span>. Epidemiology, resistance genomics and susceptibility of Acinetobacter species: results from the 2020 Spanish nationwide surveillance study. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(15):pii=2300352. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.15.2300352" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.15.2300352</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 10 Jul 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 13 Dec 2023 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.15.2300352
/content/10.2807/1560-7917.ES.2024.29.15.2300352
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error