1887

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Volume 66, Issue 5

Occurrence and characterization of class 1 integrons in from healthy individuals and those with urinary infection Free

Abstract

Class 1 integrons are among the main vehicles that facilitate the spread of antibiotic-resistance genes, with serious public health consequences. The aim of this cross-sectional study was to investigate the presence of class 1 integrons and to characterize their variable regions, as well as the antimicrobial resistance profiles and phylogenetic groups of a collection of isolates recovered from healthy subjects (=42) and those with urinary infection (=40).

The methods used included PCR, sequencing and antimicrobial susceptibility testing.

PCR screening for the integrase gene () revealed a higher incidence of class 1 integrons in uropathogenic (65 %, UPEC) than in commensal isolates (11.9 %). Eight of 31 -positive isolates, all of them UPEC, harboured empty integrons. The variable regions of the other 23 contained gene cassettes encoding resistance to -lactams (-1), aminoglycosides ( and ), trimethoprim ( and ) and an ORF. To our knowledge this is the first report of an ORF identified as a putative phage tail protein associated with a class 1 integron. The and arrays prevailed in commensal and UPEC, respectively. UPEC isolates were highly resistant to the antimicrobials tested, in contrast to commensal isolates. The isolates carrying gene cassettes associated with class 1 integrons were found to be unrelated to any phylogroup or multiresistance.

Co-resistance to clinically relevant fluoroquinolone and trimethoprim-sulfamethazole in all UPEC isolates is a cause for concern. These results expand the current knowledge of gene cassettes in both commensal and pathogenic .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): class-1 integron , commensal Escherichia-coli , humans , integrons , multidrug resistance , phylogenetic group and uropathogenic Escherichia coli
© 2017 The Authors
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2017-05-01
2024-04-26
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References

  1. Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 2010; 8:207–217 [View Article][PubMed]
     [Google Scholar]
  2. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2:123–140 [View Article][PubMed]
     [Google Scholar]
  3. World Health Organization 2014; Antimicrobial resistance: global report on surveillance. www.who.int/drugresistance/documents/surveillancereport/en/ [accessed 9 November 2016]
  4. Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E et al. Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 2015; 13:310–317 [View Article][PubMed]
     [Google Scholar]
  5. Domingues S, Da Silva GJ, Nielsen KM. Integrons: vehicles and pathways for horizontal dissemination in bacteria. Mob Genet Elements 2012; 2:211–223 [View Article][PubMed]
     [Google Scholar]
  6. Gillings MR. Integrons: past, present, and future. Microbiol Mol Biol Rev 2014; 78:257–277 [View Article][PubMed]
     [Google Scholar]
  7. Solberg OD, Ajiboye RM, Riley LW. Origin of class 1 and 2 integrons and gene cassettes in a population-based sample of uropathogenic Escherichia coli. J Clin Microbiol 2006; 44:1347–1351 [View Article][PubMed]
     [Google Scholar]
  8. Gündoğdu A, Long YB, Vollmerhausen TL, Katouli M. Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 2011; 60:1633–1642 [View Article][PubMed]
     [Google Scholar]
  9. Wei Q, Jiang X, Li M, Li G, Hu Q et al. Diversity of gene cassette promoter variants of class 1 integrons in uropathogenic Escherichia coli. Curr Microbiol 2013; 67:543–549 [View Article][PubMed]
     [Google Scholar]
  10. Poey ME, Laviña M. Integrons in uropathogenic Escherichia coli and their relationship with phylogeny and virulence. Microb Pathog 2014; 77:73–77 [View Article][PubMed]
     [Google Scholar]
  11. Skurnik D, Le Menac'h A, Zurakowski D, Mazel D, Courvalin P et al. Integron-associated antibiotic resistance and phylogenetic grouping of Escherichia coli isolates from healthy subjects free of recent antibiotic exposure. Antimicrob Agents Chemother 2005; 49:3062–3065 [View Article][PubMed]
     [Google Scholar]
  12. Machado E, Coque TM, Cantón R, Sousa JC, Peixe L. Commensal Enterobacteriaceae as reservoirs of extended-spectrum beta-lactamases, integrons, and sul genes in Portugal. Front Microbiol 2013; 4:80 [View Article][PubMed]
     [Google Scholar]
  13. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009; 33:757–784 [View Article][PubMed]
     [Google Scholar]
  14. Kor SB, Choo QC, Chew CH. New integron gene arrays from multiresistant clinical isolates of members of the Enterobacteriaceae and Pseudomonas aeruginosa from hospitals in Malaysia. J Med Microbiol 2013; 62:412–420 [View Article][PubMed]
     [Google Scholar]
  15. Zeighami H, Haghi F, Hajiahmadi F. Molecular characterization of integrons in clinical isolates of betalactamase-producing Escherichia coli and Klebsiella pneumoniae in Iran. J Chemother 2015; 27:145–151 [View Article][PubMed]
     [Google Scholar]
  16. Xu X, Li X, Luo M, Liu P, Su K et al. Molecular characterisations of integrons in clinical isolates of Klebsiella pneumoniae in a Chinese tertiary hospital. Microb Pathog 2017; 104:164–170 [View Article][PubMed]
     [Google Scholar]
  17. Zgurskaya HI. Rethinking antibiotics. Front Microbiol 2015; 6:132 [View Article]
     [Google Scholar]
  18. Paiva MC, Nascimento AM, Camargo IL, Lima-Bittencourt CI, Nardi RM. The first report of the qnrB19, qnrS1 and aac(6´)-Ib-cr genes in urinary isolates of ciprofloxacin-resistant Escherichia coli in Brazil. Mem Inst Oswaldo Cruz 2012; 107:687–689 [View Article][PubMed]
     [Google Scholar]
  19. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66:4555–4558 [View Article][PubMed]
     [Google Scholar]
  20. Lévesque C, Roy PH. PCR analysis of integrons. In Persing DH, Smith TF, Tenover FC, White TJ. (editors) Diagnostic Molecular Microbiology: Principles and Applications Washington, DC: American Society for Microbiology; 1993 pp. 590–594
     [Google Scholar]
  21. CLSI Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Six Informational Supplement M100-S26 Wayne, PA: Clinical and Laboratory Standards Institute; 2016
     [Google Scholar]
  22. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281 [View Article][PubMed]
     [Google Scholar]
  23. Mazel D, Dychinco B, Webb VA, Davies J. Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. Antimicrob Agents Chemother 2000; 44:1568–1574 [View Article][PubMed]
     [Google Scholar]
  24. Díaz-Mejía JJ, Amábile-Cuevas CF, Rosas I, Souza V. An analysis of the evolutionary relationships of integron integrases, with emphasis on the prevalence of class 1 integrons in Escherichia coli isolates from clinical and environmental origins. Microbiology 2008; 154:94–102 [View Article][PubMed]
     [Google Scholar]
  25. Moura A, Pereira C, Henriques I, Correia A. Novel gene cassettes and integrons in antibiotic-resistant bacteria isolated from urban wastewaters. Res Microbiol 2012; 163:92–100 [View Article][PubMed]
     [Google Scholar]
  26. Bissonnette L, Roy PH. Characterization of In0 of Pseudomonas aeruginosa plasmid pVS1, an ancestor of integrons of multiresistance plasmids and transposons of Gram-negative bacteria. J Bacteriol 1992; 174:1248–1257 [View Article][PubMed]
     [Google Scholar]
  27. Dessie HK, Bae DH, Lee YJ. Characterization of integrons and their cassettes in Escherichia coli and Salmonella isolates from poultry in Korea. Poult Sci 2013; 92:3036–3043 [View Article][PubMed]
     [Google Scholar]
  28. Sarria-Guzmán Y, López-Ramírez MP, Chávez-Romero Y, Ruiz-Romero E, Dendooven L et al. Identification of antibiotic resistance cassettes in class 1 integrons in Aeromonas spp. strains isolated from fresh fish (Cyprinus carpio L.). Curr Microbiol 2014; 68:581–586 [View Article][PubMed]
     [Google Scholar]
  29. Collis CM, Hall RM. Gene cassettes from the insert region of integrons are excised as covalently closed circles. Mol Microbiol 1992; 6:2875–2885 [View Article][PubMed]
     [Google Scholar]
  30. Vinué L, Jové T, Torres C, Ploy MC. Diversity of class 1 integron gene cassette Pc promoter variants in clinical Escherichia coli strains and description of a new P2 promoter variant. Int J Antimicrob Agents 2011; 38:526–529 [View Article][PubMed]
     [Google Scholar]
  31. Wu K, Wang F, Sun J, Wang Q, Chen Q et al. Class 1 integron gene cassettes in multidrug-resistant Gram-negative bacteria in southern China. Int J Antimicrob Agents 2012; 40:264–267 [View Article][PubMed]
     [Google Scholar]
  32. Kheiri R, Akhtari L. Antimicrobial resistance and integron gene cassette arrays in commensal Escherichia coli from human and animal sources in IRI. Gut Pathog 2016; 8:40 [View Article][PubMed]
     [Google Scholar]
  33. El-Najjar NG, Farah MJ, Hashwa FA, Tokajian ST. Antibiotic resistance patterns and sequencing of class I integron from uropathogenic Escherichia coli in Lebanon. Lett Appl Microbiol 2010; 51:456–461 [View Article][PubMed]
     [Google Scholar]
  34. White PA, Mciver CJ, Deng Y, Rawlinson WD. Characterisation of two new gene cassettes, aadA5 and dfrA17. FEMS Microbiol Lett 2000; 182:265–269 [View Article][PubMed]
     [Google Scholar]
  35. Mcquiston Haslund J, Rosborg Dinesen M, Sternhagen Nielsen AB, Llor C, Bjerrum L. Different recommendations for empiric first-choice antibiotic treatment of uncomplicated urinary tract infections in Europe. Scand J Prim Health Care 2013; 31:235–240 [View Article][PubMed]
     [Google Scholar]
  36. Fasugba O, Gardner A, Mitchell BG, Mnatzaganian G. Ciprofloxacin resistance in community- and hospital-acquired Escherichia coli urinary tract infections: a systematic review and meta-analysis of observational studies. BMC Infect Dis 2015; 15:545 [View Article][PubMed]
     [Google Scholar]
  37. Mokracka J, Koczura R, Kaznowski A. Transferable integrons of Gram-negative bacteria isolated from the gut of a wild boar in the buffer zone of a national park. Ann Microbiol 2012; 62:877–880 [View Article][PubMed]
     [Google Scholar]
  38. Gordon DM, Clermont O, Tolley H, Denamur E. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol 2008; 10:2484–2496 [View Article][PubMed]
     [Google Scholar]
  39. Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N et al. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 1999; 67:546–553[PubMed]
     [Google Scholar]
  40. Nowrouzian FL, Wold AE, Adlerberth I. Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J Infect Dis 2005; 191:1078–1083 [View Article][PubMed]
     [Google Scholar]
  41. Bailey JK, Pinyon JL, Anantham S, Hall RM. Commensal Escherichia coli of healthy humans: a reservoir for antibiotic-resistance determinants. J Med Microbiol 2010; 59:1331–1339 [View Article][PubMed]
     [Google Scholar]
  42. Zhang L, Foxman B, Marrs C. Both urinary and rectal Escherichia coli isolates are dominated by strains of phylogenetic group B2. J Clin Microbiol 2002; 40:3951–3955 [View Article][PubMed]
     [Google Scholar]
  43. Moreno E, Johnson JR, Pérez T, Prats G, Kuskowski MA et al. Structure and urovirulence characteristics of the fecal Escherichia coli population among healthy women. Microbes Infect 2009; 11:274–280 [View Article][PubMed]
     [Google Scholar]
  44. Nielsen KL, Dynesen P, Larsen P, Frimodt-Møller N. Faecal Escherichia coli from patients with E. coli urinary tract infection and healthy controls who have never had a urinary tract infection. J Med Microbiol 2014; 63:582–589 [View Article][PubMed]
     [Google Scholar]
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Occurrence and characterization of class 1 integrons in Escherichia coli from healthy individuals and those with urinary infection
J. Med. Microbiol. 66, 577 (2017); https://doi.org/10.1099/jmm.0.000468
/content/journal/jmm/10.1099/jmm.0.000468
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