Kuwait Medical Electronic Library

The characterization and antibiotic resistance profiles of clinical Escherichia coli O25b-B2-ST131 isolates in Kuwait

Ali A Dashti, Leila Vali 1, Sherief El-Shazly, Mehrez M Jadaon

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28 August 2014

Abstract

Background: Escherichia coli O25b-B2-ST131 are considered virulent extra-intestinal pathogens causing serious clinical complications such as urinary tract infection and bacteraemia. Our main objectives in this study were to characterise the multi-drug resistant (MDR) isolates of this lineage in Kuwait, and to demonstrate whether reduced susceptibility is spread clonally.

Results: A subset of 83 (10%) non-duplicate and non-selective E. coli O25b-B2-ST131 out of 832 MDR E. coli was identified and collected. Minimum inhibitory concentrations of the isolates were determined and pulsed-field gel electrophoresis was used for typing.The majority (95.2%) of the 83 E. coli O25b-B2-ST131 harboured at least one bla gene with blaCTX-M-15 being the most prevalent. blaCTX-M-2 was present in one isolate. Also one isolate harboured blaCTX-M-56, qnrB1 and blaCMY-2 genes and carried IncF1 plasmids of about 97 kb and160 kb. qnrB and qnrS were found in 8 other blaCTX-M-15 containing isolates. The blaNDM, blaIMP, blaVIM and qnrA were not detected, however, the blaOXA-48 was present in two (2.4%).

Conclusions: The majority of isolates harbouring qnr genes demonstrated relatedness (≥85%) by PFGE. However, the diversity in PFGE profiles for the other MDR isolates reflected the changes in population genetics of E. coli O25b-B2-ST131. We identified for the first time the appearance of blaCTX-M-2 in the Middle East and blaCTX-M-56 outside the Latin American countries. The isolate harbouring blaCTX-M-56 also contained qnrB1 and blaCMY-2 genes and carried IncF1 plasmids. The appearance of a highly virulent E. coli O25b-ST131 that is resistant to penicillins, most cephalosproins, β-lactamase inhibitors as well as fluoroquinolones is a cause for concern.

Figures

Figure 1 PFGE profiles of E. coli O25b-B2-ST131isolates collected in this study harbouring qnr genes. The degree of similarity is shown on the scale at the top left of the figure. Isolate no. Specimen Age Gender.

Figure 2 Relationship between banding patterns after digestion with Xba I endonuclease enzyme showing the percentage similarity between group types and clusters for 83 E. coli O25b-B2-ST131 isolates using DICE/UPGMA with an optimization of 1.0% and a tolerance of 0.5% generated by BioNumerics software (v.7.1).

Figure 3 PFGE profiles of E. coli O25b-B2-ST131isolates containing Class II integron.

Figure 4 Agarose gel showing S1 nuclease PFGE-based sizing of large plasmids from E. coli O25b-B2-ST131 harbouring bla CTX-M-56 .

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KMEL References

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References

1. Peirano G, Pitout JDD. Molecular epidemiology of Escherichia coli producing CTX-M beta-lactamases: the worldwide emergence of clone ST131 O25:H4. Int J Antimicrob Agents. 2010;35:316–321. doi: 10.1016/j.ijantimicag.2009.11.003. - DOI - PubMed
1. Dahbi G, Mora A, López C, Alonso MP, Mamani R, Marzoa J, Coira A, García-Garrote F, Pita JM, Velasco D, Herrera A, Viso S, Blanco JE, Blanco M, Blanco J. Emergence of new variants of ST131 clonal group among extraintestinal pathogenic Escherichia coli producing extended-spectrum β-lactamases. Int J Antimicrob Agents. 2013;42:347–351. doi: 10.1016/j.ijantimicag.2013.06.017. - DOI - PubMed
1. Karisik E, Ellington MJ, Pike R, Warren RE, Livermore DM, Woodford N. Molecular characterization of plasmids encoding CTX-M-15 β-lactamases from Escherichia coli strains in the United States. J Antimicrob Chemother. 2006;58:665–668. doi: 10.1093/jac/dkl309. - DOI - PubMed
1. Lau SH, Kaufmann MK, Livermore DM, Woodford N, Willshaw GA, Cheasty T, Stamper K, Reddy S, Cheesbrough J, Bolton FJ, Fox AJ, Upton M. UK epidemic Escherichia coli strains A E, with CTX-M-15 β-lactamase, all belong to the international O25:H4-ST131 clone. J Antimicrob Chemother. 2008;62:1241–1244. doi: 10.1093/jac/dkn380. - DOI - PubMed
1. Pitout JDD, Gregson DB, Campbell L, Laupland KB. Molecular characteristics of extended-spectrum β-lactamase-producing Escherichia coli isolates causing bacteremia in the Calgary health region from 2000 to 2007: Emergence of clone ST131 as a cause of community-acquired infections. Antimicrob Agents Chemother. 2007;2009(53):2846–2851. - PMC - PubMed
1. Johnson JR, Johnson B, Clabots C, Kuskowski MA, Pendyala S, DebRoy C, Nowicki B, Rice J. Escherichia coli sequence type ST131 as an emerging fluoroquinolone-resistant uropathogen among renal transplant recipients. Antimicrob Agents Chemother. 2010;54:546–550. doi: 10.1128/AAC.01089-09. - DOI - PMC - PubMed
1. Amyes SG, Walsh FM, Bradley JS. Best in class: a good principle for antibiotic usage to limit resistance development? J Antimicrob Chemother. 2007;59:825–826. doi: 10.1093/jac/dkm059. - DOI - PubMed
1. Pérez-Pérez FJ, Hanson ND. Detection of plasmid-mediated AmpC β-Lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol. 2002;40:2153–2162. doi: 10.1128/JCM.40.6.2153-2162.2002. - DOI - PMC - PubMed
1. Blanco M, Alonso MP, Nicolas-Chanoine MH, Dahbi G, Mora A, Blanco JE, López C, Cortés P, Llagostera M, Leflon-Guibout V, Puentes B, Mamani R, Herrera A, Coira MA, García-Garrote F, Pita JM, Blanco J. Molecular epidemiology of Escherichia coli producing extended-spectrum β-lactamases in Lugo (Spain): dissemination of clone O25b:H4-ST131 producing CTX-M-15. J Antimicrob Chemother. 2009;63:1135–1141. doi: 10.1093/jac/dkp122. - DOI - PubMed
1. Mora A, Herrera A, Mamani R, López C, Alonso MP, Blanco JE, Blanco M, Dahbi G, García-Garrote F, Pita JM, Coira A, Bernárdez MI, Blanco J. Recent emergence of clonal group O25b:K1:H4-B2-ST131 ibeA strains among Escherichia coli poultry isolates, including CTX-M-9-producing strains, and comparison with clinical human isolates. Appl Environ Microbiol. 2010;76:6991–6997. doi: 10.1128/AEM.01112-10. - DOI - PMC - PubMed
1. Vetting MW, Hegde SS, Fajardo JE, Fiser A, Roderick SL, Takiff HE, Blanchard JS. Pentapeptide repeat proteins. Biochemistry. 2006;45:1–10. doi: 10.1021/bi052130w. - DOI - PMC - PubMed
1. Nordmann P, Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother. 2005;56:463–469. doi: 10.1093/jac/dki245. - DOI - PubMed
1. Poirel L, Hombrouck-Alet C, Freneaux C, Bernabeu S, Nordmann P. Global spread of New Delhi metallo-β-lactamase 1. Lancet Infect Dis. 2010;10:832. doi: 10.1016/S1473-3099(10)70279-6. - DOI - PubMed
1. Woodford N, Turton JF, Livermore DM. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev. 2011;35:736–755. doi: 10.1111/j.1574-6976.2011.00268.x. - DOI - PubMed
1. Nordmann P, Poirel L, Carrer A, Toleman MA, Walsh TR. How to detect NDM-1 producers. J Clin Microbiol. 2011;49:718–721. doi: 10.1128/JCM.01773-10. - DOI - PMC - PubMed
1. Mantengoli E, Luzzaro F, Pecile P, Cecconi D, Cavallo A, Attala L, Bartoloni A, Rossolini GM. Escherichia coli ST131 producing extended-spectrum β-lactamases plus VIM-1 carbapenemase: further narrowing of treatment options. Clin Infect Dis. 2011;52:690–691. doi: 10.1093/cid/ciq194. - DOI - PubMed
1. Jamal W, Rotimi VO, Albert MJ, Khodakhast F, Udo EE, Poirel L. Emergence of nosocomial New Delhi metallo-β-lactamase-1 (NDM-1)-producing Klebsiella pneumoniae in patients admitted to a tertiary care hospital in Kuwait. Int J Antimicrob Agents. 2012;39:183–184. doi: 10.1016/j.ijantimicag.2011.10.002. - DOI - PubMed
1. Dortet L, Poirel L, Al Yaqoubi F, Nordmann P. NDM-1, OXA-48 and OXA-181 carbapenemase-producing Enterobacteriaceae in Sultanate of Oman. Clin Microbiol Infect. 2012;18:E144–E148. doi: 10.1111/j.1469-0691.2012.03796.x. - DOI - PubMed
1. Poirel L, Carbonnelle E, Bernabeu S, Gutmann L, Rotimi V, Nordmann P. Importation of OXA-48-producing Klebsiella pneumoniae from Kuwait. J Antimicrob Chemother. 2012;67:2051–2052. doi: 10.1093/jac/dks167. - DOI - PubMed
1. Stolle I, Prenger-Berninghoff E, Stamm I, Scheufen S, Hassdenteufel E, Guenther S, Bethe A, Pfeifer Y, Ewers C. Emergence of OXA-48 carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in dogs. J Antimicrob Chemother. 2013;68:2802–2808. doi: 10.1093/jac/dkt259. - DOI - PubMed
1. Grisold AJ, Hoenigle M, Ovcina I, Valentin T, Fruhwald S. Ventilator-associated pneumonia caused by OXA-48-producing Escherichia coli complicated by ciprofloxacin-associated rhabdomyolysis. J Infect Chemother. 2013;19:1214–1217. doi: 10.1007/s10156-013-0628-3. - DOI - PubMed
1. Zowawi HM, Balkhy HH, Walsh TR, Paterson DL. β-Lactamase production in key gram-negative pathogen isolates from the Arabian Peninsula. Clin Microbiol Rev. 2013;26:361–380. doi: 10.1128/CMR.00096-12. - DOI - PMC - PubMed
1. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66:4555–4558. doi: 10.1128/AEM.66.10.4555-4558.2000. - DOI - PMC - PubMed
1. Clermont O, Dhanji H, Upton M, Gibreel T, Fox A, Boyd D, Mulvey MR, Nordmann P, Ruppé E, Sarthou JL, Frank T, Vimont S, Arlet G, Branger C, Woodford N, Denamur E. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15 producing strains. J Antimicrob Chemother. 2009;64:274–277. doi: 10.1093/jac/dkp194. - DOI - PubMed
1. Clinical and Laboratory Standards Institute . Document M100-S21. Wayne, PA: CLSI; 2012. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement.
1. Pitout JD, Gregson DB, Church DL, Laupland KB. Population-based laboratory surveillance for AmpC beta-lactamase-producing Escherichia coli, Calgary. Emerg Infect Dis. 2007;13:443–448. doi: 10.3201/eid1303.060447. - DOI - PMC - PubMed
1. Dashti AA, Jadaon MM, Gomaa HH, Noronha B, Udo EE. Transmission of a Klebsiella pneumoniae clone harbouring genes for CTX-M-15-like and SHV-112 enzymes in a neonatal intensive care unit of a Kuwaiti hospital. J Med Microbiol. 2010;59:687–692. doi: 10.1099/jmm.0.019208-0. - DOI - PubMed
1. Sonnevend A, Al Dhaheri K, Mag T, Herpay M, Kolodziejek J, Nowotny N, Usmani A, Sheikh FA, Pal T. CTX-M-15-producing multidrug-resistant enteroaggregative Escherichia coli in the United Arab Emirates. Clin Microbiol Infect. 2006;12:582–585. doi: 10.1111/j.1469-0691.2006.01413.x. - DOI - PubMed
1. Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P. Multiplex PCR for detection of plasmid-medicated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother. 2007;60:394–397. doi: 10.1093/jac/dkm204. - DOI - PubMed
1. Cattoir V, Weill FX, Poirel L, Fabre L, Soussy CJ, Nordmann P. Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother. 2007;59:751–5744. doi: 10.1093/jac/dkl547. - DOI - PubMed
1. Park CH, Rovicsek A, Jacoby GA, Sahm D, Hooper DC. Prevalence in the United States of aac(6)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother. 2006;50:3953–3955. doi: 10.1128/AAC.00915-06. - DOI - PMC - PubMed
1. Mammeri H, Van De Loo M, Poirel L, Martinez-Martinez L, Nordmann P. Emergence of plasmid-mediated quinolone resistance in Escherichia coli in Europe. Antimicrob Agents Chemother. 2005;49:71–76. doi: 10.1128/AAC.49.1.71-76.2005. - DOI - PMC - PubMed
1. Giraud E, Brisabois A, Martel JL, Chaslus-Dancla EP. Comparative study of mutations in animal isolates and experimental in-vitro and in-vivo mutation of Salmonella spp. suggests a counter selection of highly fluoroquinolone resistant strains in the field. Antimicrob Agents Chemother. 1999;43:2131–2137. - PMC - PubMed
1. 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. doi: 10.1128/AAC.44.6.1568-1574.2000. - DOI - PMC - PubMed
1. Sánez Y, Briñas L, Domínguez E, Zarazaga M, Vila J, Torres C. Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins. Antimicrob Agents Chemother. 2004;48:3996–4001. doi: 10.1128/AAC.48.10.3996-4001.2004. - DOI - PMC - PubMed
1. Kiratisin P, Apisarnthanarak A, Saifon P, Laesripa C, Kitphati R, Mundy LM. The emergence of a novel ceftazidime-resistant CTX-M extended-spectrum beta-lactamase, CTX-M-55, in both community-onset and hospital-acquired infections in Thailand. Diagn Microbiol Infect Dis. 2007;58:349–355. doi: 10.1016/j.diagmicrobio.2007.02.005. - DOI - PubMed
1. Ribot FM, Fair NA, Gautom R, Carmeron DN, Hunter SB, Swaminathan B, Barrett TJ. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157, Salmonella and Shigella for pulsenet. Foodborne Pathog Dis. 2006;3:59–67. doi: 10.1089/fpd.2006.3.59. - DOI - PubMed
1. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods. 2005;63:219–228. doi: 10.1016/j.mimet.2005.03.018. - DOI - PubMed
1. Mshana SE, Imirzalioglu C, Hossain H, Hain T, Domann E, Chakraborty T. Conjugative IncFI plasmids carrying CTX-M-15 among Escherichia coli ESBL producing isolates at a University hospital in Germany. BMC Infect Dis. 2009;9:97. doi: 10.1186/1471-2334-9-97. - DOI - PMC - PubMed
1. Khan MA, Lemmens N, Riera E, Blonk T, Goedhart J, Van Belkum A, Goessens W, Hays JP, Van Westreenen M. Dominance of CTX-M-2 and CTX-M-56 among extended-spectrum β-lactamases produced by Klebsiella pneumoniae and Escherichia coli isolated in hospitals in Paraguay. J Antimicrob Chemother. 2009;64:1330–1332. doi: 10.1093/jac/dkp382. - DOI - PubMed
1. Suzuki S, Shibata N, Yamane K, Wachino JI, Ito K, Arakawa Y. Change in the prevalence of extended-spectrum-β-lactamase-producing Escherichia coli in Japan by clonal spread. J Antimicrob Chemother. 2009;63:72–79. doi: 10.1093/jac/dkn463. - DOI - PubMed
1. Pallecchi L, Bartoloni A, Fiorelli C, Mantella A, Di Maggio T, Gamboa H, Gotuzzo E, Kronvall G, Paradisi F, Rossolini GM. Rapid dissemination and diversity of CTX-M Extended-Spectrum β-Lactamase genes in commensal Escherichia coli isolates from healthy children from low-resource settings in Latin America. Antimicrob Agents Chemother. 2007;51:2720–2725. doi: 10.1128/AAC.00026-07. - DOI - PMC - PubMed
1. Chaïbi EB, Sirot D, Paul G, Labia R. Inhibitor-resistant TEM beta-lactamases: phenotypic, genetic and biochemical characteristics. J Antimicrob Chemother. 1999;43:447–458. doi: 10.1093/jac/43.4.447. - DOI - PubMed
1. Du bois SK, Marriott MS, Amyes SG. TEM- and SHV-derived extended-spectrum β-lactamases: relationship between selection, structure and function. J Antimicrob Chemother. 1995;35:7–22. doi: 10.1093/jac/35.1.7. - DOI - PubMed
1. Poirel L, Decousser JW, Nordmann P. Insertion sequence ISEcp1B is involved in expression and mobilization of a blaCTX-M betalactamase gene. Antimicrob Agents Chemother. 2003;47:2938–2945. doi: 10.1128/AAC.47.9.2938-2945.2003. - DOI - PMC - PubMed
1. Potron A, Nordmann P, Rondinaud E, Jaureguy F, Poirel L. A mosaic transposon encoding OXA-48 and CTX-M-15: towards pan-resistance. J Antimicrob Chemother. 2013;68:476–477. doi: 10.1093/jac/dks397. - DOI - PubMed
1. Woodford N, Carattoli A, Karisik E, Underwood A, Ellington MJ, Livermore DM. Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M Enzymes in Three Major Escherichia coli Lineages from the United Kingdom, All Belonging to the International O25:H4-ST131 Clone. Antimicrob Agents Chemother. 2009;53:4472–4482. doi: 10.1128/AAC.00688-09. - DOI - PMC - PubMed

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