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Abstract

Catheter-associated urinary tract infections (CAUTIs) represent one of the major healthcare-associated infections, and is a common Gram-negative bacterium associated with catheter infections in Egyptian clinical settings. The present study describes the phenotypic and genotypic characteristics of 31 . isolates recovered from CAUTIs in an Egyptian hospital over a 3 month period. Genomes of isolates were of good quality and were confirmed to be by comparison to the type strain (average nucleotide identity, phylogenetic analysis). Clonal diversity among the isolates was determined; eight different sequence types were found (STs 244, 357, 381, 621, 773, 1430, 1667 and 3765), of which ST357 and ST773 are considered to be high-risk clones. Antimicrobial resistance (AMR) testing according to European Committee on Antimicrobial Susceptibility Testing (EUCAST) guidelines showed that the isolates were highly resistant to quinolones [ciprofloxacin (12/31, 38.7 %) and levofloxacin (9/31, 29 %) followed by tobramycin (10/31, 32.5 %)] and cephalosporins (7/31, 22.5 %). Genotypic analysis of resistance determinants predicted all isolates to encode a range of AMR genes, including those conferring resistance to aminoglycosides, β-lactamases, fluoroquinolones, fosfomycin, sulfonamides, tetracyclines and chloramphenicol. One isolate was found to carry a 422 938 bp pBT2436-like megaplasmid encoding , the first report from Egypt of this emerging family of clinically important mobile genetic elements. All isolates were able to form biofilms and were predicted to encode virulence genes associated with adherence, antimicrobial activity, anti-phagocytosis, phospholipase enzymes, iron uptake, proteases, secretion systems and toxins. The present study shows how phenotypic analysis alongside genomic analysis may help us understand the AMR and virulence profiles of contributing to CAUTIs in Egypt.

Funding
This study was supported by the:
  • The Egyptian Ministry of Higher Education & Scientific Research
    • Principle Award Recipient: MohamedEladawy
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-10-30
2024-05-03
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References

  1. Haque M, Sartelli M, McKimm J, Abu Bakar M. Health care-associated infections - an overview. Infect Drug Resist 2018; 11:2321–2333 [View Article] [PubMed]
    [Google Scholar]
  2. Tan CW, Chlebicki MP. Urinary tract infections in adults. Singapore Med J 2016; 57:485–490 [View Article] [PubMed]
    [Google Scholar]
  3. Feneley RCL, Hopley IB, Wells PNT. Urinary catheters: history, current status, adverse events and research agenda. J Med Eng Technol 2015; 39:459–470 [View Article] [PubMed]
    [Google Scholar]
  4. Kalsi J, Arya M, Wilson P, Mundy A. Hospital-acquired urinary tract infection. Int J Clini Pract 2003; 57:388–391 [View Article]
    [Google Scholar]
  5. Mestrovic T, Robles Aguilar G, Swetschinski LR, Ikuta KS, Gray AP et al. The burden of bacterial antimicrobial resistance in the WHO European region in 2019: a cross-country systematic analysis. The Lancet Public Health 2022; 7:e897–e913 [View Article]
    [Google Scholar]
  6. Lamas Ferreiro JL, Álvarez Otero J, González González L, Novoa Lamazares L, Arca Blanco A et al. Pseudomonas aeruginosa urinary tract infections in hospitalized patients: mortality and prognostic factors. PLoS One 2017; 12:e0178178 [View Article] [PubMed]
    [Google Scholar]
  7. ECDC Antimicrobial resistance in the EU/EEA (EARS-Net)-Annual epidemiological report for 2021; 2022 https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-resistance-europe-2021
  8. WHO & ECDC Antimicrobial resistance surveillance in Europe 2022 - 2020 data; 2022 https://www.ecdc.europa.eu/en/publications-data/antimicrobial-resistance-surveillance-europe-2022-2020-data
  9. WHO WHO publishes list of bacteria for which new antibiotics are urgently needed; 2017 https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed
  10. Morales E, Cots F, Sala M, Comas M, Belvis F et al. Hospital costs of nosocomial multi-drug resistant Pseudomonas aeruginosa acquisition. BMC Health Serv Res 2012; 12:1–8 [View Article] [PubMed]
    [Google Scholar]
  11. CDC Antibiotic resistance threats report by centers for disease control and prevention; 2019 https://www.cdc.gov/drugresistance/biggest-threats.html
  12. Ramadan R, Omar N, Dawaba M, Moemen D. Bacterial biofilm dependent catheter associated urinary tract infections: characterization, antibiotic resistance pattern and risk factors. Egyptian J Basic Appl Sci 2021; 8:64–74 [View Article]
    [Google Scholar]
  13. Al-Orphaly M, Hadi HA, Eltayeb FK, Al-Hail H, Samuel BG et al. Epidemiology of multidrug-resistant Pseudomonas aeruginosa in the middle East and North Africa Region. mSphere 2021; 6:e00202–00221 [View Article] [PubMed]
    [Google Scholar]
  14. Eladawy M, El-Mowafy M, El-Sokkary MMA, Barwa R. Antimicrobial resistance and virulence characteristics in ERIC-PCR typed biofilm forming isolates of P. aeruginosa. Microb Pathog 2021; 158:105042 [View Article] [PubMed]
    [Google Scholar]
  15. Merritt JH, Kadouri DE, O’Toole GA. Growing and analyzing static biofilms. Curr Protoc Microbiol 2005; Chapter 1:1B [View Article] [PubMed]
    [Google Scholar]
  16. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40:175–179 [View Article] [PubMed]
    [Google Scholar]
  17. Hayward MR, Petrovska L, Jansen VAA, Woodward MJ. Population structure and associated phenotypes of Salmonella enterica serovars Derby and Mbandaka overlap with host range. BMC Microbiol 2016; 16:15 [View Article] [PubMed]
    [Google Scholar]
  18. Newberry F, Shibu P, Smith-Zaitlik T, Eladawy M, McCartney AL et al. Lytic bacteriophage vB_KmiS-Kmi2C disrupts biofilms formed by members of the Klebsiella oxytoca complex, and represents a novel virus family and genus. J Appl Microbiol 2023; 134:lxad079 [View Article] [PubMed]
    [Google Scholar]
  19. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  20. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  21. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article] [PubMed]
    [Google Scholar]
  22. Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res 2017; 27:737–746 [View Article] [PubMed]
    [Google Scholar]
  23. Huang YT, Liu PY, Shih PW. Homopolish: a method for the removal of systematic errors in nanopore sequencing by homologous polishing. Genome Biol 2021; 22:95 [View Article] [PubMed]
    [Google Scholar]
  24. Wick RR, Holt KE. Polypolish: short-read polishing of long-read bacterial genome assemblies. PLoS Comput Biol 2022; 18:e1009802 [View Article] [PubMed]
    [Google Scholar]
  25. Zimin AV, Salzberg SL. The genome polishing tool POLCA makes fast and accurate corrections in genome assemblies. PLoS Comput Biol 2020; 16:e1007981 [View Article] [PubMed]
    [Google Scholar]
  26. Hu J, Fan J, Sun Z, Liu S, Berger B. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics 2020; 36:2253–2255 [View Article]
    [Google Scholar]
  27. Bushnell B. BBMap: a fast, accurate, splice-aware aligner; 2014 https://www.osti.gov/biblio/1241166
  28. 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; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  29. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  30. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  31. Schwengers O, Jelonek L, Dieckmann MA, Beyvers S, Blom J et al. Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb Genom 2021; 7:11 [View Article] [PubMed]
    [Google Scholar]
  32. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 2005; 33:D325–8 [View Article] [PubMed]
    [Google Scholar]
  33. Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 2004; 42:5644–5649 [View Article] [PubMed]
    [Google Scholar]
  34. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  35. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA et al. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 2013; 57:3348–3357 [View Article]
    [Google Scholar]
  36. Asnicar F, Thomas AM, Beghini F, Mengoni C, Manara S et al. Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0. Nat Commun 2020; 11:2500 [View Article] [PubMed]
    [Google Scholar]
  37. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
    [Google Scholar]
  38. Cazares A, Moore MP, Hall JPJ, Wright LL, Grimes M et al. A megaplasmid family driving dissemination of multidrug resistance in Pseudomonas. Nat Commun 2020; 11:1370 [View Article] [PubMed]
    [Google Scholar]
  39. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 2011; 17:10 [View Article]
    [Google Scholar]
  40. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv arXiv 2013
    [Google Scholar]
  41. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  42. Giménez M, Ferrés I, Iraola G. Improved detection and classification of plasmids from circularized and fragmented assemblies. bioRxiv 2022 [View Article]
    [Google Scholar]
  43. Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 2016; 4:e2584 [View Article]
    [Google Scholar]
  44. Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol 2017; 35:1026–1028 [View Article] [PubMed]
    [Google Scholar]
  45. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
    [Google Scholar]
  46. Rebelo AR, Bortolaia V, Leekitcharoenphon P, Hansen DS, Nielsen HL et al. One day in Denmark: comparison of phenotypic and genotypic antimicrobial susceptibility testing in bacterial isolates from clinical settings. Front Microbiol 2022; 13:804627 [View Article] [PubMed]
    [Google Scholar]
  47. Vanstokstraeten R, Piérard D, Crombé F, De Geyter D, Wybo I et al. Genotypic resistance determined by whole genome sequencing versus phenotypic resistance in 234 Escherichia coli isolates. Sci Rep 2023; 13:449 [View Article] [PubMed]
    [Google Scholar]
  48. Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol 2017; 35:725–731 [View Article] [PubMed]
    [Google Scholar]
  49. Redondo-Salvo S, Bartomeus-Peñalver R, Vielva L, Tagg KA, Webb HE et al. COPLA, a taxonomic classifier of plasmids. BMC Bioinformatics 2021; 22:390 [View Article] [PubMed]
    [Google Scholar]
  50. Li Y, Zhu Y, Zhou W, Chen Z, Moran RA et al. Alcaligenes faecalis metallo-β-lactamase in extensively drug-resistant Pseudomonas aeruginosa isolates. Clin Microbiol Infect 2022; 28:880 [View Article] [PubMed]
    [Google Scholar]
  51. Arnold M, Wibberg D, Blom J, Schatschneider S, Winkler A et al. Draft genome sequence of Pseudomonas aeruginosa strain WS136, a highly cytotoxic ExoS-positive wound isolate recovered from pyoderma gangrenosum. Genome Announc 2015; 3:e00680-15 [View Article] [PubMed]
    [Google Scholar]
  52. Klockgether J, Cramer N, Wiehlmann L, Davenport CF, Tümmler B. Pseudomonas aeruginosa genomic structure and diversity. Front Microbiol 2011; 2:150 [View Article] [PubMed]
    [Google Scholar]
  53. Cottalorda A, Dahyot S, Soares A, Alexandre K, Zorgniotti I et al. Phenotypic and genotypic within-host diversity of Pseudomonas aeruginosa urinary isolates. Sci Rep 2022; 12:5421 [View Article] [PubMed]
    [Google Scholar]
  54. Cottalorda A, Leoz M, Dahyot S, Gravey F, Grand M et al. Within-host microevolution of Pseudomonas aeruginosa urinary isolates: a seven-patient longitudinal genomic and phenotypic study. Front Microbiol 2020; 11:611246 [View Article] [PubMed]
    [Google Scholar]
  55. Angeletti S, Cella E, Prosperi M, Spoto S, Fogolari M et al. Multi-drug resistant Pseudomonas aeruginosa nosocomial strains: molecular epidemiology and evolution. Microb Pathog 2018; 123:233–241 [View Article] [PubMed]
    [Google Scholar]
  56. Kocsis B, Gulyás D, Szabó D. Diversity and distribution of resistance markers in Pseudomonas aeruginosa international high-risk clones. Microorganisms 2021; 9:359 [View Article] [PubMed]
    [Google Scholar]
  57. Zafer MM, Al-Agamy MH, El-Mahallawy HA, Amin MA, El Din Ashour S. Dissemination of VIM-2 producing Pseudomonas aeruginosa ST233 at tertiary care hospitals in Egypt. BMC Infect Dis 2015; 15:122 [View Article] [PubMed]
    [Google Scholar]
  58. Zafer MM, Amin M, El Mahallawy H, Ashour M-D, Al Agamy M. First report of NDM-1-producing Pseudomonas aeruginosa in Egypt. Int J Infect Dis 2014; 29:80–81 [View Article] [PubMed]
    [Google Scholar]
  59. Alamri AM, Alfifi S, Aljehani Y, Alnimr A. Whole genome sequencing of ceftolozane-tazobactam and ceftazidime-avibactam resistant Pseudomonas aeruginosa isolated from a blood stream infection reveals VEB and chromosomal metallo-beta lactamases as genetic determinants: a case report. Infect Drug Resist 2020; 13:4215–4222 [View Article] [PubMed]
    [Google Scholar]
  60. Bitar I, Salloum T, Merhi G, Hrabak J, Araj GF et al. Genomic characterization of mutli-drug resistant Pseudomonas aeruginosa clinical isolates: evaluation and determination of ceftolozane/tazobactam activity and resistance mechanisms. Front Cell Infect Microbiol 2022; 12:922976 [View Article] [PubMed]
    [Google Scholar]
  61. Sid Ahmed MA, Abdel Hadi H, Abu Jarir S, Ahmad Khan F, Arbab MA et al. Prevalence and microbiological and genetic characteristics of multidrug-resistant Pseudomonas aeruginosa over three years in Qatar. Antimicrob Steward Healthc Epidemiol 2022; 2:e96 [View Article] [PubMed]
    [Google Scholar]
  62. Sid Ahmed MA, Khan FA, Sultan AA, Söderquist B, Ibrahim EB et al. β-lactamase-mediated resistance in MDR-Pseudomonas aeruginosa from Qatar. Antimicrob Resist Infect Control 2020; 9:170 [View Article] [PubMed]
    [Google Scholar]
  63. Zowawi HM, Syrmis MW, Kidd TJ, Balkhy HH, Walsh TR et al. Identification of carbapenem-resistant Pseudomonas aeruginosa in selected hospitals of the gulf cooperation council states: dominance of high-risk clones in the region. J Med Microbiol 2018; 67:846–853 [View Article] [PubMed]
    [Google Scholar]
  64. Yousefi S, Nahaei MR, Farajnia S, Aghazadeh M, Iversen A et al. A multiresistant clone of Pseudomonas aeruginosa sequence type 773 spreading in a burn unit in Orumieh, Iran. APMIS 2013; 121:146–152 [View Article] [PubMed]
    [Google Scholar]
  65. Lambert PA. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. J R Soc Med 2002; 95 Suppl 41:22–26 [PubMed]
    [Google Scholar]
  66. Hall JPJ, Botelho J, Cazares A, Baltrus DA. What makes a megaplasmid?. Phil Trans R Soc B 2022; 377:20200472 [View Article]
    [Google Scholar]
  67. Urbanowicz P, Bitar I, Izdebski R, Baraniak A, Literacka E et al. Epidemic territorial spread of IncP-2-Type VIM-2 carbapenemase-encoding megaplasmids in nosocomial Pseudomonas aeruginosa populations. Antimicrob Agents Chemother 2021; 65:e02122-20 [View Article] [PubMed]
    [Google Scholar]
  68. Croughs PD, Klaassen CHW, van Rosmalen J, Maghdid DM, Boers SA et al. Unexpected mechanisms of resistance in Dutch Pseudomonas aeruginosa isolates collected during 14 years of surveillance. Int J Antimicrob Agents 2018; 52:407–410 [View Article] [PubMed]
    [Google Scholar]
  69. 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 [View Article] [PubMed]
    [Google Scholar]
  70. Blanco P, Hernando-Amado S, Reales-Calderon JA, Corona F, Lira F et al. Bacterial multidrug efflux pumps: much more than antibiotic resistance determinants. Microorganisms 2016; 4:14 [View Article] [PubMed]
    [Google Scholar]
  71. Kishk RM, Abdalla MO, Hashish AA, Nemr NA, El Nahhas N et al. Efflux MexAB-mediated resistance in P. aeruginosa isolated from patients with healthcare associated infections. Pathogens 2020; 9:471 [View Article] [PubMed]
    [Google Scholar]
  72. Abdelkhalik AM, Agha MM, Zaki AM, Tahoun AT. Clinical and lab-assessed antibiotic resistance pattern of uropathogens among women with acute uncomplicated cystitis. Egypt J Hosp Med 2018; 73:7860–7868 [View Article]
    [Google Scholar]
  73. Nouh K, Kasem A, Shaher H, Elawady H, Gomaa R et al. The Egyptian Urological Guidelines, First Edition, Chapter XI: Urinary Tract Infections Guidelines 2021
    [Google Scholar]
  74. Moustafa BH, Rabie MM, El Hakim IZ, Badr A, El Balshy M et al. Egyptian pediatric clinical practice guidelines for urinary tract infections in infants and children (evidence based). Egypt Pediatric Association Gaz 2021; 69:43 [View Article]
    [Google Scholar]
  75. Ramadan AA, Abdelaziz NA, Amin MA, Aziz RK. Novel blaCTX-M variants and genotype-phenotype correlations among clinical isolates of extended spectrum beta lactamase-producing Escherichia coli. Sci Rep 2019; 9:4224 [View Article] [PubMed]
    [Google Scholar]
  76. Rodloff A, Bauer T, Ewig S, Kujath P, Müller E. Susceptible, intermediate, and resistant – the intensity of antibiotic action. Deutsches Arzteblatt Int 2008; 105:657–662 [View Article]
    [Google Scholar]
  77. Tsutsumi K, Yonehara R, Ishizaka-Ikeda E, Miyazaki N, Maeda S et al. Structures of the wild-type MexAB-OprM tripartite pump reveal its complex formation and drug efflux mechanism. Nat Commun 2019; 10:1520 [View Article] [PubMed]
    [Google Scholar]
  78. Köhler T, Michéa-Hamzehpour M, Henze U, Gotoh N, Curty LK et al. Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol Microbiol 1997; 23:345–354 [View Article] [PubMed]
    [Google Scholar]
  79. Masuda N, Sakagawa E, Ohya S, Gotoh N, Tsujimoto H et al. Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2000; 44:3322–3327 [View Article]
    [Google Scholar]
  80. Zhang L, Li X-Z, Poole K. Fluoroquinolone susceptibilities of efflux-mediated multidrug-resistant Pseudomonas aeruginosa, Stenotrophomonas maltophilia and Burkholderia cepacia. J Antimicrob Chemother 2001; 48:549–552 [View Article] [PubMed]
    [Google Scholar]
  81. Mima T, Sekiya H, Mizushima T, Kuroda T, Tsuchiya T. Gene cloning and properties of the RND-type multidrug efflux pumps MexPQ-OpmE and MexMN-OprM from Pseudomonas aeruginosa. Microbiol Immunol 2005; 49:999–1002 [View Article] [PubMed]
    [Google Scholar]
  82. Sekiya H, Mima T, Morita Y, Kuroda T, Mizushima T et al. Functional cloning and characterization of a multidrug efflux pump, mexHI-opmD, from a Pseudomonas aeruginosa mutant. Antimicrob Agents Chemother 2003; 47:2990–2992 [View Article] [PubMed]
    [Google Scholar]
  83. Nikaido H, Pagès JM. Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol Rev 2012; 36:340–363 [View Article] [PubMed]
    [Google Scholar]
  84. Abbas HA, El-Ganiny AM, Kamel HA. Phenotypic and genotypic detection of antibiotic resistance of Pseudomonas aeruginosa isolated from urinary tract infections. Afr Health Sci 2018; 18:11–21 [View Article] [PubMed]
    [Google Scholar]
  85. Basha AM, El-Sherbiny GM, Mabrouk MI. Phenotypic characterization of the Egyptian isolates “extensively drug-resistant Pseudomonas aeruginosa” and detection of their metallo-β-lactamases encoding genes. Bull Natl Res Cent 2020; 44:117 [View Article]
    [Google Scholar]
  86. El-Domany RA, Emara M, El-Magd MA, Moustafa WH, Abdeltwab NM. Emergence of imipenem-resistant Pseudomonas aeruginosa clinical isolates from Egypt coharboring VIM and IMP carbapenemases. Microb Drug Resist 2017; 23:682–686 [View Article] [PubMed]
    [Google Scholar]
  87. Al-Agamy MH, Jeannot K, El-Mahdy TS, Samaha HA, Shibl AM et al. Diversity of molecular mechanisms conferring carbapenem resistance to Pseudomonas aeruginosa isolates from Saudi Arabia. Can J Infect Dis Med Microbiol 2016; 2016:4379686 [View Article] [PubMed]
    [Google Scholar]
  88. El-Shouny WA, Ali SS, Sun J, Samy SM, Ali A. Drug resistance profile and molecular characterization of extended spectrum beta-lactamase (ESβL)-producing Pseudomonas aeruginosa isolated from burn wound infections. Essential oils and their potential for utilization. Microb Pathog 2018; 116:301–312 [View Article] [PubMed]
    [Google Scholar]
  89. Ku PM, Hobbs DA, Gilmore M, Hobbs AL. 1234. can susceptibility to one carbapenem be conferred to another? frequency of discordance in gram-negative clinical isolates. Open Forum Infect Dis 2021; 8:S706–S707
    [Google Scholar]
  90. Doyle RM, O’Sullivan DM, Aller SD, Bruchmann S, Clark T et al. Discordant bioinformatic predictions of antimicrobial resistance from whole-genome sequencing data of bacterial isolates: an inter-laboratory study. Microb Genom 2020; 6:e000335 [View Article] [PubMed]
    [Google Scholar]
  91. Gajdács M, Baráth Z, Kárpáti K, Szabó D, Usai D et al. No correlation between biofilm formation, virulence factors, and antibiotic resistance in Pseudomonas aeruginosa: results from a laboratory-based in vitro study. Antibiotics 2021; 10:1134 [View Article] [PubMed]
    [Google Scholar]
  92. Nabal Díaz SG, Algara Robles O, García-Lechuz Moya JM. New definitions of susceptibility categories EUCAST 2019: clinic application. Rev Esp Quimioter 2022; 35 Suppl 3:84–88 [View Article] [PubMed]
    [Google Scholar]
  93. Ellington MJ, Ekelund O, Aarestrup FM, Canton R, Doumith M et al. The role of whole genome sequencing in antimicrobial susceptibility testing of bacteria: report from the EUCAST Subcommittee. Clin Microbiol Infect 2017; 23:2–22 [View Article] [PubMed]
    [Google Scholar]
  94. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015; 13:269–284 [View Article] [PubMed]
    [Google Scholar]
  95. Datar R, Coello Pelegrin A, Orenga S, Chalansonnet V, Mirande C et al. Phenotypic and genomic variability of serial peri-lung transplantation Pseudomonas aeruginosa isolates from cystic fibrosis patients. Front Microbiol 2021; 12:604555 [View Article] [PubMed]
    [Google Scholar]
  96. Thi MTT, Wibowo D, Rehm BHA. Pseudomonas aeruginosa biofilms. Int J Mol Sci 2020; 21:8671 [View Article]
    [Google Scholar]
  97. Díaz-Ríos C, Hernández M, Abad D, Álvarez-Montes L, Varsaki A et al. New sequence type ST3449 in multidrug-resistant Pseudomonas aeruginosa isolates from a cystic fibrosis patient. Antibiotics 2021; 10:491 [View Article] [PubMed]
    [Google Scholar]
  98. Deligianni E, Pattison S, Berrar D, Ternan NG, Haylock RW et al. Pseudomonas aeruginosa cystic fibrosis isolates of similar RAPD genotype exhibit diversity in biofilm forming ability in vitro. BMC Microbiol 2010; 10:38 [View Article] [PubMed]
    [Google Scholar]
  99. Sultan M, Arya R, Kim KK. Roles of two-component systems in Pseudomonas aeruginosa virulence. Int J Mol Sci 2021; 22:22 [View Article] [PubMed]
    [Google Scholar]
  100. Redfern J, Wallace J, van Belkum A, Jaillard M, Whittard E et al. Biofilm associated genotypes of multiple antibiotic resistant Pseudomonas aeruginosa. BMC Genomics 2021; 22:572 [View Article] [PubMed]
    [Google Scholar]
  101. Karthikeyan RS, Priya JL, Leal SM, Toska J, Rietsch A et al. Host response and bacterial virulence factor expression in Pseudomonas aeruginosa and Streptococcus pneumoniae corneal ulcers. PLoS One 2013; 8:e64867 [View Article] [PubMed]
    [Google Scholar]
  102. Rodrigues YC, Furlaneto IP, Maciel AHP, Quaresma AJPG, de Matos ECO et al. High prevalence of atypical virulotype and genetically diverse background among Pseudomonas aeruginosa isolates from a referral hospital in the Brazilian Amazon. PLoS ONE 2020; 15:e0238741 [View Article]
    [Google Scholar]
  103. Sarges E do SNF, Rodrigues YC, Furlaneto IP, de Melo MVH, Brabo GL da C et al. Pseudomonas aeruginosa type III secretion system virulotypes and their association with clinical features of cystic fibrosis patients. Infect Drug Resist 2020; 13:3771–3781 [View Article] [PubMed]
    [Google Scholar]
  104. Botelho J, Grosso F, Quinteira S, Mabrouk A, Peixe L. The complete nucleotide sequence of an IncP-2 megaplasmid unveils a mosaic architecture comprising a putative novel blaVIM-2-harbouring transposon in Pseudomonas aeruginosa. J Antimicrob Chemother 2017; 72:2225–2229 [View Article] [PubMed]
    [Google Scholar]
  105. Li M, Guan C, Song G, Gao X, Yang W et al. Characterization of a conjugative multidrug resistance IncP-2 megaplasmid, pPAG5, from a clinical Pseudomonas aeruginosa isolate. Microbiol Spectr 2022; 10:e0199221 [View Article]
    [Google Scholar]
  106. Xiong J, Alexander DC, Ma JH, Déraspe M, Low DE et al. Complete sequence of pOZ176, a 500-kilobase IncP-2 plasmid encoding IMP-9-mediated carbapenem resistance, from outbreak isolate Pseudomonas aeruginosa 96. Antimicrob Agents Chemother 2013; 57:3775–3782 [View Article]
    [Google Scholar]
  107. Zheng D, Wang X, Wang P, Peng W, Ji N et al. Genome sequence of Pseudomonas citronellolis SJTE-3, an estrogen- and polycyclic aromatic hydrocarbon-degrading bacterium. Genome Announc 2016; 4:e01373-16 [View Article] [PubMed]
    [Google Scholar]
  108. Schmid M, Frei D, Patrignani A, Schlapbach R, Frey JE et al. Pushing the limits of de novo genome assembly for complex prokaryotic genomes harboring very long, near identical repeats. Nucleic Acids Res 2018; 46:8953–8965 [View Article]
    [Google Scholar]
  109. Yuan M, Chen H, Zhu X, Feng J, Zhan Z et al. Psy153-MDR, a P12969-DIM-related MEGA plasmid carrying Bla(IMP-45) and armA, from clinical Pseudomonas putida. Oncotarget 2017; 8: [View Article]
    [Google Scholar]
  110. Abd El-Baky RM, Masoud SM, Mohamed DS, Waly NG, Shafik EA et al. Prevalence and some possible mechanisms of colistin resistance among multidrug-resistant and extensively drug-resistant Pseudomonas aeruginosa. Infect Drug Resist 2020; 13:323–332 [View Article] [PubMed]
    [Google Scholar]
  111. Abdel-Rhman SH, Rizk DE. Serotypes, antibiogram and genetic relatedness of Pseudomonas aeruginosa isolates from urinary tract infections at urology and nephrology center, Mansoura, Egypt. AiM 2018; 08:625–638 [View Article]
    [Google Scholar]
  112. Abou-Dobara MI, Deyab MA, Elsawy EM, Mohamed HH. Antibiotic susceptibility and genotype patterns of Escherichia coli, Klebsiella pneumoniae and Pseudomonas aeruginosa isolated from urinary tract infected patients. Pol J Microbiol 2010; 59:207–212 [PubMed]
    [Google Scholar]
  113. Ahmed O, Mohamed H, Salem W, Afifi M, Song Y. Efficacy of ethanolic extract of Syzygium aromaticum in the treatment of multidrug-resistant Pseudomonas aeruginosa clinical isolates associated with urinary tract infections. Evid Based Complement Alternat Med 2021; 2021:6612058 [View Article] [PubMed]
    [Google Scholar]
  114. Edward EA, El Shehawy MR, Abouelfetouh A, Aboulmagd E. Prevalence of different virulence factors and their association with antimicrobial resistance among Pseudomonas aeruginosa clinical isolates from Egypt. BMC Microbiol 2023; 23:161 [View Article]
    [Google Scholar]
  115. El-Mahdy R, El-Kannishy G. Virulence factors of carbapenem-resistant Pseudomonas aeruginosa In hospital-acquired infections in Mansoura, Egypt. Infect Drug Resist 2019; 12:3455–3461 [View Article] [PubMed]
    [Google Scholar]
  116. El-Mokhtar MA, Hassanein KM, Ahmed AS, Gad GF, Amin MM et al. Antagonistic activities of cell-free supernatants of lactobacilli against extended-spectrum β-lactamase producing Klebsiella pneumoniae and Pseudomonas aeruginosa. Infect Drug Resist 2020; 13:543–552 [View Article] [PubMed]
    [Google Scholar]
  117. El Shamy AA, Zakaria Z, Tolba MM, Salah Eldin N, Rabea A-T et al. AmpC β-lactamase variable expression in common multidrug-resistant nosocomial bacterial pathogens from a tertiary hospital in Cairo, Egypt. Int J Microbiol 2021; 2021:6633888 [View Article] [PubMed]
    [Google Scholar]
  118. Elbargisy RM. Characterization of uropathogenic Pseudomonas aeruginosa: serotypes, resistance phenotypes, and virulence genotypes. J Pure Appl Microbiol 2022; 16:1284–1297 [View Article]
    [Google Scholar]
  119. Elnegery AA, Mowafy WK, Zahra TA, Abou El-Khier NT. Study of quorum-sensing LasR and RhlR genes and their dependent virulence factors in Pseudomonas aeruginosa isolates from infected burn wounds. Access Microbiol 2021; 3:000211 [View Article] [PubMed]
    [Google Scholar]
  120. Farhan SM, Ibrahim RA, Mahran KM, Hetta HF, Abd El-Baky RM. Antimicrobial resistance pattern and molecular genetic distribution of metallo-β-lactamases producing Pseudomonas aeruginosa isolated from hospitals in Minia, Egypt. Infect Drug Resist 2019; 12:2125–2133 [View Article] [PubMed]
    [Google Scholar]
  121. Gad GF, el-Domany RA, Ashour HM. Antimicrobial susceptibility profile of Pseudomonas aeruginosa isolates in Egypt. J Urol 2008; 180:176–181 [View Article] [PubMed]
    [Google Scholar]
  122. Gad GF, Mohamed HA, Ashour HM. Aminoglycoside resistance rates, phenotypes, and mechanisms of Gram-negative bacteria from infected patients in upper Egypt. PLoS One 2011; 6:e17224 [View Article] [PubMed]
    [Google Scholar]
  123. Hamza EH, El-Shawadfy AM, Allam AA, Hassanein WA. Study on pyoverdine and biofilm production with detection of LasR gene in MDR Pseudomonas aeruginosa. Saudi J Biol Sci 2023; 30:103492 [View Article] [PubMed]
    [Google Scholar]
  124. Hashem H, Hanora A, Abdalla S, Shawky A, Saad A. Carbapenem susceptibility and multidrug-resistance in Pseudomonas aeruginosa isolates in Egypt. Jundishapur J Microbiol 2016; 9:e30257 [View Article] [PubMed]
    [Google Scholar]
  125. Mohamed WF, Askora AA, Mahdy MMH, El-Hussieny EA, Abu-Shady HM. Isolation and characterization of bacteriophages active against Pseudomonas aeruginosa strains isolated from diabetic foot infections. Arch Razi Inst 2022; 77:2187–2200 [View Article] [PubMed]
    [Google Scholar]
  126. Nassar O, Desouky SE, El-Sherbiny GM, Abu-Elghait M. Correlation between phenotypic virulence traits and antibiotic resistance in Pseudomonas aeruginosa clinical isolates. Microb Pathog 2022; 162:105339 [View Article] [PubMed]
    [Google Scholar]
  127. Mohamed S, Marwa A, Hamada H, Amro H. Mutations in -lactamases detected in multidrug resistant gram negative bacteria isolated from community acquired urinary tract infections in Assiut, Egypt. Afr J Microbiol Res 2016; 10:1938–1943 [View Article]
    [Google Scholar]
  128. Shaaban M, Al-Qahtani A, Al-Ahdal M, Barwa R. Molecular characterization of resistance mechanisms in Pseudomonas aeruginosa isolates resistant to carbapenems. J Infect Dev Ctries 2017; 11:935–943 [View Article]
    [Google Scholar]
  129. Zafer MM, Al-Agamy MH, El-Mahallawy HA, Amin MA, Ashour MSE-D. Antimicrobial resistance pattern and their beta-lactamase encoding genes among Pseudomonas aeruginosa strains isolated from cancer patients. Biomed Res Int 2014; 2014:101635 [View Article] [PubMed]
    [Google Scholar]
  130. Kuepper J, Ruijssenaars HJ, Blank LM, de Winde JH, Wierckx N. Complete genome sequence of solvent-tolerant Pseudomonas putida S12 including megaplasmid pTTS12. J Biotechnol 2015; 200:17–18 [View Article] [PubMed]
    [Google Scholar]
  131. Scheetz MH, Hoffman M, Bolon MK, Schulert G, Estrellado W et al. Morbidity associated with Pseudomonas aeruginosa bloodstream infections. Diagn Microbiol Infect Dis 2009; 64:311–319 [View Article] [PubMed]
    [Google Scholar]
  132. Eltoukhy A, Jia Y, Lamraoui I, Abo-Kadoum MA, Atta OM et al. Transcriptome analysis and cytochrome P450 monooxygenase reveal the molecular mechanism of Bisphenol A degradation by Pseudomonas putida strain YC-AE1. BMC Microbiol 2022; 22:294 [View Article]
    [Google Scholar]
  133. Chung H, Merakou C, Schaefers MM, Flett KB, Martini S et al. Rapid expansion and extinction of antibiotic resistance mutations during treatment of acute bacterial respiratory infections. Nat Commun 2022; 13:1231 [View Article] [PubMed]
    [Google Scholar]
  134. Zhang X, Wang L, Li D, Li P, Yuan L et al. An Incp-2 plasmid sublineage associated with dissemination of Bla(IMP-45) among carbapenem-resistant Pseudomonas aeruginosa. Emerg Microbes Infect 2021; 10:442–449 [View Article]
    [Google Scholar]
  135. Zhu Y, Chen J, Shen H, Chen Z, Yang QW et al. Emergence of ceftazidime- and avibactam-resistant Klebsiella pneumoniae carbapenemase-producing Pseudomonas aeruginosa in China. mSystems 2021; 6:e0078721 [View Article] [PubMed]
    [Google Scholar]
  136. Long X, Wang X, Mao D, Wu W, Luo Y. A novel XRE-type regulator mediates phage lytic development and multiple host metabolic processes in Pseudomonas aeruginosa. Microbiol Spectr 2022; 10:e0351122 [View Article] [PubMed]
    [Google Scholar]
  137. Zhang B, Xu X, Song X, Wen Y, Zhu Z et al. Emerging and re-emerging KPC-producing hypervirulent Pseudomonas aeruginosa ST697 and ST463 between 2010 and 2021. Emerg Microbes Infect 2022; 11:2735–2745 [View Article] [PubMed]
    [Google Scholar]
  138. Fang Y, Baloch Z, Zhang W, Hu Y, Zheng R et al. Emergence of carbapenem-resistant ST244, ST292, and ST2446 Pseudomonas aeruginosa clones in burn patients in Yunnan province. Infect Drug Resist 2022; Volume 15:1103–1114 [View Article]
    [Google Scholar]
  139. Gao J, Wei X, Yin L, Jin Y, Bai F et al. Emergence and transfer of plasmid-harbored rmtB in a clinical multidrug-resistant Pseudomonas aeruginosa strain. Microorganisms 2022; 10:1818 [View Article]
    [Google Scholar]
  140. Chen M, Cai H, Li Y, Wang N, Zhang P et al. Plasmid-borne AFM alleles in Pseudomonas aeruginosa clinical isolates from China. Microbiol Spectr 2022; 10:e0203522 [View Article] [PubMed]
    [Google Scholar]
  141. Hu Y, Liu C, Wang Q, Zeng Y, Sun Q et al. Emergence and expansion of a carbapenem-resistant Pseudomonas aeruginosa clone are associated with plasmid-borne bla KPC-2 and virulence-related genes. mSystems 2021; 6:e00154-21 [View Article] [PubMed]
    [Google Scholar]
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