Dissemination of Metallo-β-Lactamase-Producing Pseudomonas aeruginosa in Serbian Hospital Settings: Expansion of ST235 and ST654 Clones
Abstract
:1. Introduction
2. Results
2.1. Antimicrobial Resistance
2.2. Molecular Detection of MBL- and ESBL-Encoding Genes
2.3. Multilocus Sequence Typing Analysis
2.4. Phylogenomic Analysis of blaNDM-Positive Strains
2.5. The Genetic Context of the Detected MBL Genes
3. Discussion
4. Materials and Methods
4.1. Bacterial Isolates
4.2. Antibiotic Susceptibility Testing
4.3. PCR Amplification of Resistance Genes
4.4. Multilocus Sequence Typing
4.5. Phylogenomic and Genomic Analysis of blaNDM-Positive Strains
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Thaden, J.T.; Park, L.P.; Maskarinec, S.A.; Ruffin, F.; Fowler, V.G.; van Duin, D. Results from a 13-Year Prospective Cohort Study Show Increased Mortality Associated with Bloodstream Infections Caused by Pseudomonas aeruginosa Compared to Other Bacteria. Antimicrob. Agents Chemother. 2017, 61, e02671-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pachori, P.; Gothalwal, R.; Gandhi, P. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis. 2019, 6, 109–119. [Google Scholar] [CrossRef] [PubMed]
- Hu, Y.-Y.; Cao, J.-M.; Yang, Q.; Chen, S.; Lv, H.-Y.; Zhou, H.-W.; Wu, Z.; Zhang, R. Risk Factors for Carbapenem-Resistant Pseudomonas aeruginosa, Zhejiang Province, China. Emerg. Infect. Dis. 2019, 25, 1861–1867. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murray, C.J.; Ikuta, K.S.; Sharara, F.; Swetschinski, L.; Aguilar, G.R.; Gray, A.; Han, C.; Bisignano, C.; Rao, P.; Wool, E.; et al. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [Google Scholar] [CrossRef]
- Malkoçoğlu, G.; Aktaş, E.; Bayraktar, B.; Otlu, B.; Bulut, M.E. VIM-1, VIM-2, and GES-5 Carbapenemases Among Pseudomonas aeruginosa Isolates at a Tertiary Hospital in Istanbul, Turkey. Microb. Drug Resist. 2017, 23, 328–334. [Google Scholar] [CrossRef]
- Tacconelli, E.; Sifakis, F.; Harbarth, S.; Schrijver, R.; van Mourik, M.; Voss, A.; Sharland, M.; Rajendran, N.B.; Rodríguez-Baño, J.; Bielicki, J.; et al. Surveillance for control of antimicrobial resistance. Lancet Infect. Dis. 2018, 18, e99–e106. [Google Scholar] [CrossRef] [Green Version]
- Rice, L.B. Federal Funding for the Study of Antimicrobial Resistance in Nosocomial Pathogens: No ESKAPE. J. Infect. Dis. 2008, 197, 1079–1081. [Google Scholar] [CrossRef]
- Central Asian and Eastern European Surveillance of Antimicrobial Resistance. Annual Report. 2020. Available online: https://www.euro.who.int/__data/assets/pdf_file/0003/469200/Central-Asian-and-European-Surveillance-of-Antimicrobial-Resistance.-Annual-report-2020-eng.pdf (accessed on 15 July 2022).
- Potron, A.; Poirel, L.; Nordmann, P. Emerging broad-spectrum resistance in Pseudomonas aeruginosa and Acinetobacter baumannii: Mechanisms and epidemiology. Int. J. Antimicrob. Agents 2015, 45, 568–585. [Google Scholar] [CrossRef] [Green Version]
- Davies, T.A.; Queenan, A.M.; Morrow, B.J.; Shang, W.; Amsler, K.; He, W.; Lynch, A.S.; Pillar, C.; Flamm, R.K. Longitudinal survey of carbapenem resistance and resistance mechanisms in Enterobacteriaceae and non-fermenters from the USA in 2007–09. J. Antimicrob. Chemother. 2011, 66, 2298–2307. [Google Scholar] [CrossRef]
- Choudhury, D.; Das Talukdar, A.; Choudhury, M.D.; Maurya, A.P.; Paul, D.; Chanda, D.D.; Chakravorty, A.; Bhattacharjee, A. Transcriptional Analysis of MexAB-OprM Efflux Pumps System of Pseudomonas aeruginosa and Its Role in Carbapenem Resistance in a Tertiary Referral Hospital in India. PLoS ONE 2015, 10, e0133842. [Google Scholar] [CrossRef]
- Mirsalehian, A.; Kalantar-Neyestanaki, D.; Nourijelyani, K.; Asadollahi, K.; Taherikalani, M.; Emaneini, M.; Jabalameli, F. Detection of AmpC-β-lactamases producing isolates among carbapenem resistant P. aeruginosa isolated from burn patient. Iran. J. Microbiol. 2014, 6, 306–310. [Google Scholar]
- Livermore, D.M. Multiple Mechanisms of Antimicrobial Resistance in Pseudomonas aeruginosa: Our Worst Nightmare? Clin. Infect. Dis. 2002, 34, 634–640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jovcic, B.; Lepsanovic, Z.; Suljagic, V.; Rackov, G.; Begovic, J.; Topisirovic, L.; Kojic, M. Emergence of NDM-1 Metallo-β-Lactamase in Pseudomonas aeruginosa Clinical Isolates from Serbia. Antimicrob. Agents Chemother. 2011, 55, 3929–3931. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Treepong, P.; Kos, V.; Guyeux, C.; Blanc, D.; Bertrand, X.; Valot, B.; Hocquet, D. Global emergence of the widespread Pseudomonas aeruginosa ST235 clone. Clin. Microbiol. Infect. 2018, 24, 258–266. [Google Scholar] [CrossRef] [Green Version]
- Woodford, N.; Turton, J.; Livermore, D.M. Multiresistant Gram-negative bacteria: The role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol. Rev. 2011, 35, 736–755. [Google Scholar] [CrossRef] [Green Version]
- Bocharova, Y.; Savinova, T.; Lazareva, A.; Polikarpova, S.; Gordinskaya, N.; Mayanskiy, N.; Chebotar, I. Genotypes, carbapenemase carriage, integron diversity and oprD alterations among carbapenem-resistant Pseudomonas aeruginosa from Russia. Int. J. Antimicrob. Agents 2020, 55, 105899. [Google Scholar] [CrossRef]
- Bush, L.M.; Perez, M.T. Typhoid Fever. Pseudomonas and Related Infections—Infectious Diseases—MSD Manual Professional Edition. 2020. Available online: https://www.merckmanuals.com/professional/infectious-diseases/gram-negative-bacilli/pseudomonas-and-related-infections (accessed on 19 July 2022).
- Aloush, V.; Navon-Venezia, S.; Seigman-Igra, Y.; Cabili, S.; Carmeli, Y. Multidrug-Resistant Pseudomonas aeruginosa: Risk Factors and Clinical Impact. Antimicrob. Agents Chemother. 2006, 50, 43–48. [Google Scholar] [CrossRef] [Green Version]
- Radovanovic, R.S.; Savic, N.R.; Ranin, L.; Smitran, A.; Opavski, N.V.; Tepavcevic, A.M.; Ranin, J.; Gajic, I. Biofilm Production and Antimicrobial Resistance of Clinical and Food Isolates of Pseudomonas spp. Curr. Microbiol. 2020, 77, 4045–4052. [Google Scholar] [CrossRef]
- European Centre for Disease Prevention and Control. Antimicrobial Resistance Surveillance in Europe 2022–2020 Data. 2022. Available online: https://www.ecdc.europa.eu/en/publications-data/antimicrobial-resistance-surveillance-europe-2022-2020-data (accessed on 1 July 2022).
- Durante-Mangoni, E.; Andini, R.; Zampino, R. Management of carbapenem-resistant Enterobacteriaceae infections. Clin. Microbiol. Infect. 2019, 25, 943–950. [Google Scholar] [CrossRef]
- Karlowsky, J.A.; Kazmierczak, K.M.; de Jonge, B.L.M.; Hackel, M.A.; Sahm, D.F.; Bradford, P.A. In Vitro Activity of Aztreonam-Avibactam against Enterobacteriaceae and Pseudomonas aeruginosa Isolated by Clinical Laboratories in 40 Countries from 2012 to 2015. Antimicrob. Agents Chemother. 2017, 61, e00472-17. [Google Scholar] [CrossRef] [Green Version]
- Partridge, S.R.; Kwong, S.M.; Firth, N.; Jensen, S.O. Mobile Genetic Elements Associated with Antimicrobial Resistance. Clin. Microbiol. Rev. 2018, 31, e00088-17. [Google Scholar] [CrossRef] [PubMed]
- O’Neall, D.; Juhász, E.; Tóth, A.; Urbán, E.; Szabó, J.; Melegh, S.; Katona, K.; Kristóf, K. Ceftazidime–avibactam and ceftolozane–tazobactam susceptibility of multidrug resistant Pseudomonas aeruginosa strains in Hungary. Acta Microbiol. Immunol. Hung. 2020, 67, 61–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahmed, M.A.S.; Hassan, A.; Abu Jarir, S.; Hadi, H.A.; Bansal, D.; Wahab, A.A.; Muneer, M.; Mohamed, S.; Zahraldin, K.; Hamid, J.; et al. Emergence of Multidrug- and Pandrug- Resistant Pseudomonas aeruginosa from Five Hospitals in Qatar. Infect. Prev. Pract. 2019, 1, 100027. [Google Scholar] [CrossRef] [PubMed]
- El-Baky, R.M.A.; Masoud, S.M.; Mohamed, D.S.; Waly, N.G.; A Shafik, E.; A Mohareb, D.; Elkady, A.; Elbadr, M.M.; Hetta, H.F. Prevalence and Some Possible Mechanisms of Colistin Resistance Among Multidrug-Resistant and Extensively Drug-Resistant Pseudomonas aeruginosa. Infect. Drug Resist. 2020, 13, 323–332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsuji, B.T.; Pogue, J.M.; Zavascki, A.P.; Paul, M.; Daikos, G.L.; Forrest, A.; Giacobbe, D.R.; Viscoli, C.; Giamarellou, H.; Karaiskos, I.; et al. International Consensus Guidelines for the Optimal Use of the Polymyxins: Endorsed by the American College of Clinical Pharmacy (ACCP), European Society of Clinical Microbiology and Infectious Diseases (ESCMID), Infectious Diseases Society of America (IDSA), International Society for Anti-infective Pharmacology (ISAP), Society of Critical Care Medicine (SCCM), and Society of Infectious Diseases Pharmacists (SIDP). Pharmacother. J. Hum. Pharmacol. Drug Ther. 2019, 39, 10–39. [Google Scholar] [CrossRef] [Green Version]
- Urbanowicz, P.; Izdebski, R.; Baraniak, A.; Żabicka, D.; Hryniewicz, W.; Gniadkowski, M. Molecular and genomic epidemiology of VIM/IMP-like metallo-β-lactamase-producing Pseudomonas aeruginosa genotypes in Poland. J. Antimicrob. Chemother. 2021, 76, 2273–2284. [Google Scholar] [CrossRef]
- Papagiannitsis, C.C.; Medvecky, M.; Chudejova, K.; Skalova, A.; Rotova, V.; Spanelova, P.; Jakubu, V.; Zemlickova, H.; Hrabak, J. Molecular Characterization of Carbapenemase-Producing Pseudomonas aeruginosa of Czech Origin and Evidence for Clonal Spread of Extensively Resistant Sequence Type 357 Expressing IMP-7 Metallo-β-Lactamase. Antimicrob. Agents Chemother. 2017, 61, e01811-17. [Google Scholar] [CrossRef] [Green Version]
- Nordmann, P.; Ronco, E.; Naas, T.; Duport, C.; Michel-Briand, Y.; Labia, R. Characterization of a novel extended-spectrum beta-lactamase from Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1993, 37, 962–969. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Libisch, B.; Poirel, L.; Lepsanovic, Z.; Mirovic, V.; Balogh, B.; Pászti, J.; Hunyadi, Z.; Dobák, A.; Füzi, M.; Nordmann, P. Identification of PER-1 extended-spectrum β-lactamase producing Pseudomonas aeruginosa clinical isolates of the international clonal complex CC11 from Hungary and Serbia. FEMS Immunol. Med. Microbiol. 2008, 54, 330–338. [Google Scholar] [CrossRef] [Green Version]
- Weldhagen, G.F.; Poirel, L.; Nordmann, P. Ambler Class A Extended-Spectrum β-Lactamases in Pseudomonas aeruginosa: Novel Developments and Clinical Impact. Antimicrob. Agents Chemother. 2003, 47, 2385–2392. [Google Scholar] [CrossRef] [Green Version]
- Pagani, L.; Mantengoli, E.; Migliavacca, R.; Nucleo, E.; Pollini, S.; Spalla, M.; Daturi, R.; Romero, E.; Rossolini, G.M. Multifocal Detection of Multidrug-Resistant Pseudomonas aeruginosa Producing the PER-1 Extended-Spectrum β-Lactamase in Northern Italy. J. Clin. Microbiol. 2004, 42, 2523–2529. [Google Scholar] [CrossRef] [PubMed]
- Çiçek, A.; Ertürk, A.; Ejder, N.; Rakici, E.; Kostakoğlu, U.; Yıldız, I.E.; Özyurt, S.; Sönmez, E. Screening of Antimicrobial Resistance Genes and Epidemiological Features in Hospital and Community-Associated Carbapenem-Resistant Pseudomonas aeruginosa Infections. Infect. Drug Resist. 2021, 14, 1517–1526. [Google Scholar] [CrossRef] [PubMed]
- Akhi, M.T.; Khalili, Y.; Ghottaslou, R.; Aghazadeh, M.; Seroush Bar Hagh, M.H.; Yousefi, S. Prevalence of PER-1- type ex-tended-spectrum beta-lactamases in clinical strains of Pseudomonas aeruginosa isolated from Tabriz, Iran. Iran. J. Basic. Med. Sci. 2012, 15, 678–682. [Google Scholar]
- Yoon, E.-J.; Jeong, S.H. Mobile Carbapenemase Genes in Pseudomonas aeruginosa. Front. Microbiol. 2021, 12, 614058. [Google Scholar] [CrossRef]
- Abril, D.; Marquez-Ortiz, R.A.; Castro-Cardozo, B.; Moncayo, I.; Escobar, N.M.O.; Rozo, Z.L.C.; Reyes, N.; Tovar, C.; Sánchez, H.F.; Castellanos, J.; et al. Genome plasticity favours double chromosomal Tn4401b-blaKPC-2 transposon insertion in the Pseudomonas aeruginosa ST235 clone. BMC Microbiol. 2019, 19, 45. [Google Scholar] [CrossRef]
- Del Barrio-Tofiño, E.; López-Causapé, C.; Oliver, A. Pseudomonas aeruginosa epidemic high-risk clones and their association with horizontally-acquired β-lactamases: 2020 update. Int. J. Antimicrob. Agents. 2020, 56, 106196. [Google Scholar] [CrossRef]
- Janvier, F.; Jeannot, K.; Tessé, S.; Robert-Nicoud, M.; Delacour, H.; Rapp, C.; Mérens, A. Molecular Characterization of bla NDM-1 in a Sequence Type 235 Pseudomonas aeruginosa Isolate from France. Antimicrob. Agents Chemother. 2013, 57, 3408–3411. [Google Scholar] [CrossRef] [Green Version]
- Carattoli, A.; Fortini, D.; Galetti, R.; Garcia-Fernandez, A.; Nardi, G.; Orazi, D.; Capone, A.; Majolino, I.; Proia, A.; Mariani, B.; et al. Isolation of NDM-1-producing Pseudomonas aeruginosa sequence type ST235 from a stem cell transplant patient in Italy, May 2013. Eurosurveillance 2013, 18, 20633. [Google Scholar] [CrossRef] [Green Version]
- Kostyanev, T.; Nguyen, M.; Markovska, R.; Stankova, P.; Xavier, B.; Lammens, C.; Marteva-Proevska, Y.; Velinov, T.; Cantón, R.; Goossens, H.; et al. Emergence of ST654 Pseudomonas aeruginosa co-harbouring blaNDM-1 and blaGES-5 in novel class I integron In1884 from Bulgaria. J. Glob. Antimicrob. Resist. 2020, 22, 672–673. [Google Scholar] [CrossRef]
- European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 11.0. 2021. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_12.0_Breakpoint_Tables.pdf (accessed on 1 July 2022).
- Poirel, L.; Walsh, T.R.; Cuvillier, V.; Nordmann, P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn. Microbiol. Infect. Dis. 2011, 70, 119–123. [Google Scholar] [CrossRef]
- Opazo, A.; Sonnevend, A.; Lopes, B.; Hamouda, A.; Ghazawi, A.; Pal, T.; Amyes, S.G.B. Plasmid-encoded PER-7 -lactamase responsible for ceftazidime resistance in Acinetobacter baumannii isolated in the United Arab Emirates. J. Antimicrob. Chemother. 2012, 67, 1619–1622. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Celenza, G.; Pellegrini, C.; Caccamo, M.; Segatore, B.; Amicosante, G.; Perilli, M. Spread of blaCTX-M-type and blaPER-2 β-lactamase genes in clinical isolates from Bolivian hospitals. J. Antimicrob. Chemother. 2006, 57, 975–978. [Google Scholar] [CrossRef] [PubMed]
- Yoshizumi, A.; Ishii, Y.; Aoki, K.; Testa, R.; Nichols, W.W.; Tateda, K. In vitro susceptibility of characterized β-lactamase-producing Gram-negative bacteria isolated in Japan to ceftazidime-, ceftaroline-, and aztreonam-avibactam combinations. J. Infect. Chemother. 2015, 21, 148–151. [Google Scholar] [CrossRef] [PubMed]
- Bae, I.K.; Jang, S.J.; Kim, J.; Jeong, S.H.; Cho, B.; Lee, K. Interspecies Dissemination of the bla Gene Encoding PER-1 Extended-Spectrum β-Lactamase. Antimicrob. Agents Chemother. 2011, 55, 1305–1307. [Google Scholar] [CrossRef] [Green Version]
- Curran, B.; Jonas, D.; Grundmann, H.; Pitt, T.; Dowson, C.G. Development of a Multilocus Sequence Typing Scheme for the Opportunistic Pathogen Pseudomonas aeruginosa. J. Clin. Microbiol. 2004, 42, 5644–5649. [Google Scholar] [CrossRef] [Green Version]
- Winsor, G.L.; Griffiths, E.J.; Lo, R.; Dhillon, B.K.; Shay, J.A.; Brinkman, F.S.L. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res. 2015, 44, D646–D653. [Google Scholar] [CrossRef] [Green Version]
- Wick, R.R.; Judd, L.M.; Gorrie, C.L.; Holt, K.E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 2017, 13, e1005595. [Google Scholar] [CrossRef] [Green Version]
- Lee, I.; Chalita, M.; Ha, S.-M.; Na, S.-I.; Yoon, S.-H.; Chun, J. ContEst16S: An algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int. J. Syst. Evol. Microbiol. 2017, 67, 2053–2057. [Google Scholar] [CrossRef]
- Wick, R.R.; Schultz, M.B.; Zobel, J.; Holt, K.E. Bandage: Interactive visualization of de novo genome assemblies. Bioinformatics 2015, 31, 3350–3352. [Google Scholar] [CrossRef] [Green Version]
- Seemann, T. Prokka: Rapid Prokaryotic Genome Annotation. Bioinformatics 2014, 30, 2068–2069. [Google Scholar] [CrossRef] [Green Version]
- Lagesen, K.; Hallin, P.; Rødland, E.A.; Staerfeldt, H.-H.; Rognes, T.; Ussery, D.W. RNAmmer: Consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007, 35, 3100–3108. [Google Scholar] [CrossRef] [PubMed]
- Carattoli, A.; Zankari, E.; Garcìa-Fernandez, A.; Larsen, M.; Lund, O.; Voldby Villa, L.; Møller Aarestrup, F.; Hasman, H. In Silico Detection and Typing of Plasmids. Antimicrob using PlasmidFinder and plasmid multilocus sequence typing. Agents Chemother. 2014, 58, 3895–3903. [Google Scholar] [CrossRef] [PubMed]
- Page, A.J.; Cummins, C.A.; Hunt, M.; Wong, V.K.; Reuter, S.; Holden, M.T.G.; Fookes, M.; Falush, D.; Keane, J.A.; Parkhill, J. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015, 31, 3691–3693. [Google Scholar] [CrossRef] [Green Version]
- Page, A.J.; Taylor, B.; Delaney, A.J.; Soares, J.; Seemann, T.; Keane, J.A.; Harris, S.R. SNP-sites: Rapid efficient extraction of SNPs from multi-FASTA alignments. Microb. Genom. 2016, 2, e000056. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef] [PubMed]
- Siguier, P.; Perochon, J.; Lestrade, L.; Mahillon, J.; Chandler, M. ISfinder: The reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006, 34, D32–D36. [Google Scholar] [CrossRef]
Characteristic | No. (%) |
---|---|
Gender | |
Male gender | 172 (53.8) |
Female gender | 148 (46.2) |
Admission ward | |
Intensive care unit | 126 (39.4) |
Thoracic surgery | 3 (0.9) |
Orthopedic surgery | 3 (0.9) |
Plastic surgery | 6 (1.9) |
Cardiovascular surgery | 39 (12.2) |
Neurosurgery | 10 (3.1) |
General surgery | 29 (9.1) |
Urology surgery | 3 (0.9) |
Internal wards | 52 (16.3) |
Department for COVID-19-positive patients | 23 (7.2) |
Geriatric department | 19 (5.9) |
Department of Oncology | 7 (2.2) |
Type of specimen | |
Tracheal aspirate | 74 (23.1) |
Bronchoalveolar lavage | 26 (8.1) |
Sputum | 20 (6.3) |
Wound specimen | 108 (33.8) |
Blood | 21 (6.6) |
Urine | 71 (22.2) |
Comorbidity | |
Malignancy | 36 (11.2) |
Chronic venous insufficiency | 18 (5.6) |
Heart insufficiency | 18 (5.6) |
Diabetes | 23 (7.2) |
COVID-19 pneumonia | 23 (7.2) |
Invasive procedures | |
Any surgical procedure | 93 (29.1) |
Mechanical ventilation | 72 (22.5) |
Central venous catheter | 42 (13.1) |
Urinary catheter | 139 (43.4) |
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Kabic, J.; Fortunato, G.; Vaz-Moreira, I.; Kekic, D.; Jovicevic, M.; Pesovic, J.; Ranin, L.; Opavski, N.; Manaia, C.M.; Gajic, I. Dissemination of Metallo-β-Lactamase-Producing Pseudomonas aeruginosa in Serbian Hospital Settings: Expansion of ST235 and ST654 Clones. Int. J. Mol. Sci. 2023, 24, 1519. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24021519
Kabic J, Fortunato G, Vaz-Moreira I, Kekic D, Jovicevic M, Pesovic J, Ranin L, Opavski N, Manaia CM, Gajic I. Dissemination of Metallo-β-Lactamase-Producing Pseudomonas aeruginosa in Serbian Hospital Settings: Expansion of ST235 and ST654 Clones. International Journal of Molecular Sciences. 2023; 24(2):1519. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24021519
Chicago/Turabian StyleKabic, Jovana, Gianuario Fortunato, Ivone Vaz-Moreira, Dusan Kekic, Milos Jovicevic, Jovan Pesovic, Lazar Ranin, Natasa Opavski, Célia M. Manaia, and Ina Gajic. 2023. "Dissemination of Metallo-β-Lactamase-Producing Pseudomonas aeruginosa in Serbian Hospital Settings: Expansion of ST235 and ST654 Clones" International Journal of Molecular Sciences 24, no. 2: 1519. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24021519