Skip to content
1887

Journal of Medical Microbiology logo Journal of Medical Microbiology

Volume 74, Issue 2

Genotypic and phenotypic analyses of two distinct sets of urinary tract isolates Open Access

Abstract

Urinary tract infections (UTIs) are associated with a high burden of morbidity, mortality and cost. employs a myriad of virulence factors, including biofilm formation and motility mechanisms, to cause infections including persistent UTIs. is highly resistant to antibiotics, and the World Health Organization has identified it as a pathogen for which novel antimicrobials are urgently required.

Genotypic and phenotypic characterization of from UTIs is underreported. In addition, the rise of antimicrobial resistance (AMR) is a cause for concern, particularly in many countries where surveillance is severely lacking.

To identify genotypic and phenotypic characteristics of UTI isolates sourced from the UK and the state of Kuwait, with an emphasis on genotypic diversity and AMR.

Twenty-three . UTI isolates were sourced from the UK and Kuwait. To establish the phenotypes of UK isolates, growth analysis, biofilm formation assays, motility assays and antibiotic disc diffusion assays were performed. Whole-genome sequencing, antimicrobial susceptibility assays and detection of AMR-associated genes were conducted on both sets of isolates.

In terms of their phenotypic characteristics and genomic composition, the UTI isolates varied. Multiple resistance genes are associated with resistance to various classes of antibiotics, such as aminoglycosides, fluoroquinolones and -lactams, particularly in isolates from Kuwait. Extreme antibiotic resistance was detected in the isolates obtained from Kuwait, indicating that the country may be an antibiotic resistance hotspot.

This study highlights that isolates from UTIs are diverse and can display extremely high resistance. Surveillance in countries such as Kuwait is currently limited, and this study suggests the need for greater surveillance.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial resistance , biofilm formation , Pseudomonas aeruginosa , urinary tract infections and virulence factors
© 2025 The Authors
  • 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.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001971
2025-02-27
2026-03-06

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/jmm/74/2/jmm001971.html?itemId=/content/journal/jmm/10.1099/jmm.0.001971&mimeType=html&fmt=ahah

References

  1. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis Mon 2003; 49:53–70 [View Article] [PubMed]
     [Google Scholar]
  2. 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]
     [Google Scholar]
  3. NHS Digital Hospital admissions relating to urinary tract infections; 2023 https://digital.nhs.uk/supplementary-information/2023/hospital-admissions-relating-to-urinary-tract-infections
  4. Vihta K-D, Stoesser N, Llewelyn MJ, Quan TP, Davies T et al. Trends over time in Escherichia coli bloodstream infections, urinary tract infections, and antibiotic susceptibilities in Oxfordshire, UK, 1998-2016: a study of electronic health records. Lancet Infect Dis 2018; 18:1138–1149 [View Article] [PubMed]
     [Google Scholar]
  5. Jarvis WR, Martone WJ. Predominant pathogens in hospital infections. J Antimicrob Chemother 1992; 29 Suppl A:19–24 [View Article] [PubMed]
     [Google Scholar]
  6. Gellatly SL, Hancock REW. Pseudomonas aeruginosa : new insights into pathogenesis and host defenses. Pathogens Disease 2013; 67:159–173 [View Article]
     [Google Scholar]
  7. Tacconelli E, Magrini N, Carmeli Y, Harbarth S, Kahlmeter G et al. Global Priority List Of Antibiotic-Resistant Bacteria To Guide Research, Discovery And Development Of New Antibiotics World Heal Organ; 2017
     [Google Scholar]
  8. Breidenstein EBM, de la Fuente-Núñez C, Hancock REW. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 2011; 19:419–426 [View Article] [PubMed]
     [Google Scholar]
  9. Wei Q, Ma LZ. Biofilm matrix and its regulation in Pseudomonas aeruginosa. IJMS 2013; 14:20983–21005 [View Article]
     [Google Scholar]
  10. Ma L, Conover M, Lu H, Parsek MR, Bayles K et al. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 2009; 5:e1000354 [View Article] [PubMed]
     [Google Scholar]
  11. Balasubramanian D, Schneper L, Merighi M, Smith R, Narasimhan G et al. The regulatory repertoire of Pseudomonas aeruginosa AmpC ß-lactamase regulator AmpR includes virulence genes. PLoS One 2012; 7:e34067 [View Article] [PubMed]
     [Google Scholar]
  12. Freschi L, Vincent AT, Jeukens J, Emond-Rheault J-G, Kukavica-Ibrulj I et al. The Pseudomonas aeruginosa pan-genome provides new insights on its population structure, horizontal gene transfer, and pathogenicity. Genome Biol Evol 2019; 11:109–120 [View Article] [PubMed]
     [Google Scholar]
  13. Winstanley C, Langille MGI, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C et al. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool epidemic strain of Pseudomonas aeruginosa. Genome Res 2009; 19:12–23 [View Article]
     [Google Scholar]
  14. Sadikot RT, Blackwell TS, Christman JW, Prince AS. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 2005; 171:1209–1223 [View Article] [PubMed]
     [Google Scholar]
  15. Mekonnen SA, El Husseini N, Turdiev A, Carter JA, Belew AT et al. Catheter-associated urinary tract infection by Pseudomonas aeruginosa progresses through acute and chronic phases of infection. Proc Natl Acad Sci USA 2022; 119:e2209383119 [View Article] [PubMed]
     [Google Scholar]
  16. Penaranda C, Chumbler NM, Hung DT. Dual transcriptional analysis reveals adaptation of host and pathogen to intracellular survival of Pseudomonas aeruginosa associated with urinary tract infection. PLoS Pathog 2021; 17:e1009534 [View Article] [PubMed]
     [Google Scholar]
  17. Xu Z-G, Gao Y, He J-G, Xu W-F, Jiang M et al. Effects of azithromycin on Pseudomonas aeruginosa isolates from catheter-associated urinary tract infection. Exp Ther Med 2015; 9:569–572 [View Article]
     [Google Scholar]
  18. Sabharwal N, Dhall S, Chhibber S, Harjai K. Molecular detection of virulence genes as markers in Pseudomonas aeruginosa isolated from urinary tract infections. Int J Mol Epidemiol Genet 2014; 5:125–134 [PubMed]
     [Google Scholar]
  19. Ironmonger D, Edeghere O, Bains A, Loy R, Woodford N et al. Surveillance of antibiotic susceptibility of urinary tract pathogens for a population of 5.6 million over 4 years. J Antimicrob Chemother 2014; 70:1744–1750 [View Article]
     [Google Scholar]
  20. Ironmonger D, Edeghere O, Bains A, Loy R, Woodford N et al. Surveillance of antibiotic susceptibility of urinary tract pathogens for a population of 5.6 million over 4 years. J Antimicrob Chemother 2015; 70:1744–1750 [View Article]
     [Google Scholar]
  21. Balkhy HH, Assiri AM, Mousa HA, Al-Abri SS, Al-Katheeri H et al. The strategic plan for combating antimicrobial resistance in Gulf Cooperation Council States. J Infect Public Health 2016; 9:375–385 [View Article]
     [Google Scholar]
  22. 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]
  23. Kapiszewski A. Arab versus Asian migrant workers in the GCC countries. In South Asian Migration to Gulf Countries: History, Policies, Development 2016
     [Google Scholar]
  24. Ostholm-Balkhed A, Tärnberg M, Nilsson M, Nilsson LE, Hanberger H et al. Travel-associated faecal colonization with ESBL-producing enterobacteriaceae: incidence and risk factors. J Antimicrob Chemother 2013; 68:2144–2153 [View Article] [PubMed]
     [Google Scholar]
  25. Al-Yamani A, Khamis F, Al-Zakwani I, Al-Noomani H, Al-Noomani J et al. Patterns of antimicrobial prescribing in a tertiary care hospital in Oman. Oman Med J 2016; 31:35–39 [View Article] [PubMed]
     [Google Scholar]
  26. Butt AA, Navasero CS, Thomas B, Marri SA, Katheeri HA et al. Antibiotic prescription patterns for upper respiratory tract infections in the outpatient Qatari population in the private sector. Int J Infect Dis 2017; 55:20–23 [View Article] [PubMed]
     [Google Scholar]
  27. Aly M, Balkhy HH. The prevalence of antimicrobial resistance in clinical isolates from Gulf Cooperation Council countries. Antimicrob Resist Infect Control 2012; 1:26 [View Article] [PubMed]
     [Google Scholar]
  28. Al Benwan K, Al Sweih N, Rotimi VO. Etiology and antibiotic susceptibility patterns of community- and hospital-acquired urinary tract infections in a general hospital in Kuwait. Med Princ Pract 2010; 19:440–446 [View Article] [PubMed]
     [Google Scholar]
  29. Ha D-G, Kuchma SL, O’Toole GA. Plate-Based Assay for Swimming Motility in Pseudomonas aeruginosa BT - Pseudomonas Methods and Protocols. In: Filloux A, Ramos J-L, editors New York, NY: Springer; 2014 pp 59–65 [View Article]
     [Google Scholar]
  30. The European Committee on Antimicrobial Susceptibility Testing (EUCAST) Breakpoint tables for interpretation of MICs and zone diameters; 2018 http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_9.0_Breakpoint_Tables.pdf
  31. Andrews JM. Testing for the BWP on S. BSAC standardized disc susceptibility testing method (version 8). J Antimicrob Chemother 2009; 64:454–489 [View Article]
     [Google Scholar]
  32. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet j 2011; 17:10 [View Article]
     [Google Scholar]
  33. NA J, JN F. Sickle: a sliding-window, adaptive, quality-based trimming tool for fastq files 2011 https://github.com/najoshi/sickle
  34. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 2017; 45:D566–D573 [View Article] [PubMed]
     [Google Scholar]
  35. Dasgupta N, Arora SK, Ramphal R. The flagellar system of Pseudomonas aeruginosa BT - Pseudomonas: volume 1 Genomics, life style and molecular architecture. In Ramos J-L. ed Boston, MA: Springer US; 2004 pp 675–698
  36. Leech AJ, Mattick JS. Effect of site-specific mutations in different phosphotransfer domains of the chemosensory protein ChpA on Pseudomonas aeruginosa motility. J Bacteriol 2006; 188:8479–8486 [View Article] [PubMed]
     [Google Scholar]
  37. Murray TS, Kazmierczak BI. Pseudomonas aeruginosa exhibits sliding motility in the absence of type IV pili and flagella. J Bacteriol 2008; 190:2700–2708 [View Article] [PubMed]
     [Google Scholar]
  38. EUCAST EC on AST Antimicrobial susceptibility testing EUCAST disk diffusion method - version 7.0. Eur Soc Clin Microbiol Infect Dis 2019
     [Google Scholar]
  39. Winsor GL, Griffiths EJ, Lo R, Dhillon BK, Shay JA et al. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res 2016; 44:D646–53 [View Article] [PubMed]
     [Google Scholar]
  40. Kos VN, Déraspe M, McLaughlin RE, Whiteaker JD, Roy PH et al. The resistome of Pseudomonas aeruginosa in relationship to phenotypic susceptibility. Antimicrob Agents Chemother 2015; 59:427–436 [View Article] [PubMed]
     [Google Scholar]
  41. Meyer R. Replication and conjugative mobilization of broad host-range IncQ plasmids. Plasmid 2009; 62:57–70 [View Article] [PubMed]
     [Google Scholar]
  42. Lin Z, Shouguang J. aph(3′)-IIb, a gene encoding an aminoglycoside-modifying enzyme, is under the positive control of surrogate regulator HpaA. Antimicrob Agents Chemother 2003; 47:3867–3876 [View Article]
     [Google Scholar]
  43. Chávez-Jacobo VM, Hernández-Ramírez KC, Romo-Rodríguez P, Pérez-Gallardo RV, Campos-García J et al. CrpP is a novel ciprofloxacin-modifying enzyme encoded by the Pseudomonas aeruginosa pUM505 plasmid. Antimicrob Agents Chemother 2018; 62:e02629-17 [View Article] [PubMed]
     [Google Scholar]
  44. Zubyk HL, Wright GD. CrpP Is Not a fluoroquinolone-inactivating enzyme. Antimicrob Agents Chemother 2021; 65:e0077321 [View Article] [PubMed]
     [Google Scholar]
  45. Rodríguez-Martínez J-M, Poirel L, Nordmann P. Extended-spectrum cephalosporinases in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2009; 53:1766–1771 [View Article]
     [Google Scholar]
  46. Clinical presentations and epidemiology of urinary tract infections. Microbiol Spectr 2016
     [Google Scholar]
  47. Rasamiravaka T, Labtani Q, Duez P, El Jaziri M. The formation of biofilms by Pseudomonas aeruginosa: a review of the natural and synthetic compounds interfering with control mechanisms. Biomed Res Int 2015; 2015:759348 [View Article] [PubMed]
     [Google Scholar]
  48. Patriquin GM, Banin E, Gilmour C, Tuchman R, Greenberg EP et al. Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 2008; 190:662–671 [View Article] [PubMed]
     [Google Scholar]
  49. Suman E, Blat KG, Hegde BK. Mucoid Pseudomonas aeruginosa in urinary tract infection. Trop Doct 1993; 23:180–181 [View Article] [PubMed]
     [Google Scholar]
  50. Odugbemi T, Anandan N, Lina OF. Urinary tract pathogens with a special reference to mucoid Pseudomonas aeruginosa at Aflaj General Hospital. Ann Saudi Med 1992; 12:581–582 [View Article] [PubMed]
     [Google Scholar]
  51. Wang EW, Jung JY, Pashia ME, Nason R, Scholnick S et al. Otopathogenic Pseudomonas aeruginosa strains as competent biofilm formers. Arch Otolaryngol Head Neck Surg 2005; 131:983 [View Article]
     [Google Scholar]
  52. Varga JJ, Barbier M, Mulet X, Bielecki P, Bartell JA et al. Genotypic and phenotypic analyses of a Pseudomonas aeruginosa chronic bronchiectasis isolate reveal differences from cystic fibrosis and laboratory strains. BMC Genomics 2015; 16:883 [View Article]
     [Google Scholar]
  53. Zegans ME, DiGiandomenico A, Ray K, Naimie A, Keller AE et al. Association of biofilm formation, Psl exopolysaccharide expression, and clinical outcomes in Pseudomonas aeruginosa keratitis: analysis of isolates in the steroids for corneal ulcers trial. JAMA Ophthalmol 2016; 134:383–389 [View Article] [PubMed]
     [Google Scholar]
  54. Schaber JA, Griswold JA, Burrowes BH, Colmer-Hamood JA et al. Diversity of biofilms produced by quorum-sensing-deficient clinical isolates of Pseudomonas aeruginosa. J Med Microbiol 2007; 56:738–748 [View Article] [PubMed]
     [Google Scholar]
  55. Mittal R, Sharma S, Chhibber S, Aggarwal S, Gupta V et al. Correlation between serogroup, in vitro biofilm formation and elaboration of virulence factors by uropathogenic Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 2010; 58:237–243 [View Article]
     [Google Scholar]
  56. Vipin C, Mujeeburahiman M, Arun AB, Ashwini P, Mangesh SV et al. Adaptation and diversification in virulence factors among urinary catheter-associated Pseudomonas aeruginosa isolates. J Appl Microbiol 2019; 126:641–650 [View Article]
     [Google Scholar]
  57. Tielen P, Narten M, Rosin N, Biegler I, Haddad I et al. Genotypic and phenotypic characterization of Pseudomonas aeruginosa isolates from urinary tract infections. Int J Med Microbiol 2011; 301:282–292 [View Article] [PubMed]
     [Google Scholar]
  58. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S et al. Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 1998; 66:43–51 [View Article] [PubMed]
     [Google Scholar]
  59. Ruzicka F, Olejnickova K, Hola v. Catheter-related infections caused by Pseudomonas aeruginosa: virulence factors involved and their relationships. Pathog Dis 2014; 72:n [View Article]
     [Google Scholar]
  60. O’Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998; 30:295–304 [View Article]
     [Google Scholar]
  61. Burrows LL. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol 2012; 66:493–520 [View Article] [PubMed]
     [Google Scholar]
  62. Winstanley C, Kaye SB, Neal TJ, Chilton HJ, Miksch S et al. Genotypic and phenotypic characteristics of Pseudomonas aeruginosa isolates associated with ulcerative keratitis. J Med Microbiol 2005; 54:519–526 [View Article] [PubMed]
     [Google Scholar]
  63. Zolfaghar I, Evans DJ, Fleiszig SMJ. Twitching motility contributes to the role of pili in corneal infection caused by Pseudomonas aeruginosa. Infect Immun 2003; 71:5389–5393 [View Article] [PubMed]
     [Google Scholar]
  64. Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M et al. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 2006; 62:1264–1277 [View Article] [PubMed]
     [Google Scholar]
  65. Jones BV, Young R, Mahenthiralingam E, Stickler DJ. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect Immun 2004; 72:3941–3950 [View Article] [PubMed]
     [Google Scholar]
  66. Al Sweih N, Jamal W, Rotimi VO. Spectrum and antibiotic resistance of uropathogens isolated from hospital and community patients with urinary tract infections in two large hospitals in Kuwait. Med Princ Pract 2005; 14:401–407 [View Article]
     [Google Scholar]
  67. Alali WQ, Abdo NM, AlFouzan W, Dhar R. Antimicrobial resistance pattern in clinical Escherichia coli and Pseudomonas aeruginosa isolates obtained from a secondary-care hospital prior to and during the COVID-19 pandemic in Kuwait. Germs 2022; 12:372–383 [View Article] [PubMed]
     [Google Scholar]
  68. Dobardzic AM, Dobardzic R. Epidemiological features of complicated UTI in a district hospital of Kuwait. Eur J Epidemiol 1997; 13:465–470 [View Article] [PubMed]
     [Google Scholar]
  69. Alshimmiri MM, Hammoud MS, Al-Saleh EA, Alsaeid KMS. Ethnic variations in birthweight percentiles in Kuwait. Paediatr Perinat Epidemiol 2003; 17:355–362 [View Article] [PubMed]
     [Google Scholar]
  70. Kadlec K, Kehrenberg C, Schwarz S. Molecular basis of resistance to trimethoprim, chloramphenicol and sulphonamides in Bordetella bronchiseptica. J Antimicrob Chemother 2005; 56:485–490 [View Article] [PubMed]
     [Google Scholar]
  71. 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]
  72. Pinder R, Berry D, Sallis A, Chadborn T, Pinder RJ. Behaviour change and antibiotic prescribing in healthcare settings literature review and behavioural analysis. Public Health England 2015
     [Google Scholar]
  73. Klockgether J, Munder A, Neugebauer J, Davenport CF, Stanke F et al. Genome diversity of Pseudomonas aeruginosa PAO1 laboratory strains. J Bacteriol 2010; 192:1113–1121 [View Article] [PubMed]
     [Google Scholar]
  74. Schroth MN, Cho JJ, Green SK, Kominos SD. Epidemiology of Pseudomonas aeruginosa in agricultural areas. J Med Microbiol 2018; 67:1191–1201 [View Article] [PubMed]
     [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001971
Loading
Genotypic and phenotypic analyses of two distinct sets of Pseudomonas aeruginosa urinary tract isolates
J. Med. Microbiol. 74, 001971 (2025); https://doi.org/10.1099/jmm.0.001971
/content/journal/jmm/10.1099/jmm.0.001971
/content/journal/jmm/10.1099/jmm.0.001971
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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