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Prolonged carriage of resistant E. coli by returned travellers: clonality, risk factors and bacterial characteristics

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Abstract

The aim of this study was to delineate the potential risks and dynamics of the prolonged carriage of resistant E. coli in returned travellers. A sample of 274 previously collected E. coli resistant to ceftriaxone (CRO), ciprofloxacin, gentamicin and/or nalidixic acid recovered from 102 travellers was studied. Travellers were assessed pre-travel then longitudinally (maximum 6 months) with peri-rectal/rectal swabs. Clonality was determined by REP-PCR and the presence of O25b-ST131 was assessed. Comparison was made longitudinally for individuals and between identified co-travellers. The risk of prolonged carriage was lower for CRO than for ciprofloxacin or gentamicin resistance. Repeated isolation of the same phenotype at different time points occurred in 19% of initial CRO-resistant carriers compared with 50% of ciprofloxacin- or gentamicin-resistant carriers. The duration of carriage was also longer for the latter resistance phenotypes (75th quartile 8 vs 62 and 63 days respectively). In multivariate analysis, risks of prolonged carriage included antimicrobial use whilst travelling (3.3, 1.3–8.4) and phylogenetic group B2 (9.3, 3.4–25.6) and D (3.8, 1.6–8.8). Clonality amongst longitudinal isolates from the same participant was demonstrated in 92% of participants who were assessable and most marked amongst CRO-resistant isolates. ST-131 was surprisingly infrequent (3% of participants). Prolonged carriage of ciprofloxacin- and gentamicin-resistant isolates is more frequent and prolonged than CRO resistance after travel. Risks of prolonged carriage indicate a contribution of host and bacterial factors to this carriage. These require further elucidation. The strong clonality identified suggests that carriage of a “phenotype” was mediated by persistence of bacteria/plasmid combinations rather than persistence of the plasmid after horizontal transfer to other bacteria.

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References

  1. Tham J, Odenholt I, Walder M, Brolund A, Ahl J, Melander E (2010) Extended-spectrum beta-lactamase-producing Escherichia coli in patients with travellers' diarrhoea. Scand J Infect Dis 42(4):275–280

    Article  PubMed  CAS  Google Scholar 

  2. Tangden T, Cars O, Melhus A, Lowdin E (2010) Foreign travel is a major risk factor for colonization with Escherichia coli producing CTX-M-type extended-spectrum beta-lactamases: a prospective study with Swedish volunteers. Antimicrob Agents Chemother 54(9):3564–3568

    Article  PubMed  Google Scholar 

  3. Dhanji H, Patel R, Wall R, Doumith M, Patel B, Hope R, Livermore DM, Woodford N (2011) Variation in the genetic environments of bla(CTX-M-15) in Escherichia coli from the faeces of travellers returning to the United Kingdom. J Antimicrob Chemother 66(5):1005–1012

    Article  PubMed  CAS  Google Scholar 

  4. Kennedy K, Collignon P (2010) Colonisation with Escherichia coli resistant to “critically important” antibiotics: a high risk for international travellers. Eur J Clin Microbiol Infect Dis 29(12):1501–1506

    Article  PubMed  CAS  Google Scholar 

  5. Peirano G, Laupland KB, Gregson DB, Pitout JD (2011) Colonization of returning travelers with CTX-M-producing Escherichia coli. J Travel Med 18(5):299–303

    Article  PubMed  Google Scholar 

  6. O'Fallon E, Gautam S, D'Agata EM (2009) Colonization with multidrug-resistant gram-negative bacteria: prolonged duration and frequent cocolonization. Clin Infect Dis 48(10):1375–1381

    Article  PubMed  Google Scholar 

  7. Lautenbach E, Tolomeo P, Mao X, Fishman NO, Metlay JP, Bilker WB, Nachamkin I (2006) Duration of outpatient fecal colonization due to Escherichia coli isolates with decreased susceptibility to fluoroquinolones: longitudinal study of patients recently discharged from the hospital. Antimicrob Agents Chemother 50(11):3939–3943

    Article  PubMed  CAS  Google Scholar 

  8. Horcajada JP, Vila J, Moreno-Martinez A, Ruiz J, Martinez JA, Sanchez M, Soriano E, Mensa J (2002) Molecular epidemiology and evolution of resistance to quinolones in Escherichia coli after prolonged administration of ciprofloxacin in patients with prostatitis. J Antimicrob Chemother 49(1):55–59

    Article  PubMed  CAS  Google Scholar 

  9. Weintrob AC, Roediger MP, Barber M, Summers A, Fieberg AM, Dunn J, Seldon V, Leach F, Huang XZ, Nikolich MP, Wortmann GW (2010) Natural history of colonization with gram-negative multidrug-resistant organisms among hospitalized patients. Infect Control Hosp Epidemiol 31(4):330–337

    Article  PubMed  Google Scholar 

  10. Oethinger M, Jellen-Ritter AS, Conrad S, Marre R, Kern WV (1998) Colonization and infection with fluoroquinolone-resistant Escherichia coli among cancer patients: clonal analysis. Infection 26(6):379–384

    Article  PubMed  CAS  Google Scholar 

  11. Stuart RL, Kotsanas D, Webb B, Vandergraaf S, Gillespie EE, Hogg GG, Korman TM (2011) Prevalence of antimicrobial-resistant organisms in residential aged care facilities. Med J Aust 195(9):530–533

    Article  PubMed  Google Scholar 

  12. Sidjabat HE, Silveira FP, Potoski BA, Abu-Elmagd KM, Adams-Haduch JM, Paterson DL, Doi Y (2009) Interspecies spread of Klebsiella pneumoniae carbapenemase gene in a single patient. Clin Infect Dis 49(11):1736–1738

    Article  PubMed  CAS  Google Scholar 

  13. Kennedy KJ, Roberts JL, Collignon PJ (2008) Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust 188(4):209–213

    PubMed  Google Scholar 

  14. Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66(10):4555–4558

    Article  PubMed  CAS  Google Scholar 

  15. Clermont O, Dhanji H, Upton M, Gibreel T, Fox A, Boyd D, Mulvey MR, Nordmann P, Ruppe E, Sarthou JL, Frank T, Vimont S, Arlet G, Branger C, Woodford N, Denamur E (2009) Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother 64(2):274–277

    Article  PubMed  CAS  Google Scholar 

  16. Rodriguez-Bano J, Navarro MD, Romero L, Martinez-Martinez L, Muniain MA, Perea EJ, Perez-Cano R, Pascual A (2004) Epidemiology and clinical features of infections caused by extended-spectrum beta-lactamase-producing Escherichia coli in nonhospitalized patients. J Clin Microbiol 42(3):1089–1094

    Article  PubMed  Google Scholar 

  17. Patel U, Dasgupta P, Amoroso P, Challacombe B, Pilcher J, Kirby R (2011) Infection after transrectal ultrasonography-guided prostate biopsy: increased relative risks after recent international travel or antibiotic use. BJU Int doi:10.1111/j.1464-410X.2011.10561.x

    Google Scholar 

  18. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD (2008) Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect 57(6):441–448

    Article  PubMed  Google Scholar 

  19. Gupta K, Hooton TM, Naber KG, Wullt B, Colgan R, Miller LG, Moran GJ, Nicolle LE, Raz R, Schaeffer AJ, Soper DE (2011) International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 52(5):e103–e120

    Article  PubMed  Google Scholar 

  20. Antibiotic Expert Group, Spicer J, Therapeutic Guidelines Limited (2010) Therapeutic guidelines: antibiotic. Therapeutic Guidelines, Melbourne, p xxxiv, 445

    Google Scholar 

  21. Willing BP, Russell SL, Finlay BB (2011) Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol 9(4):233–243

    Article  PubMed  CAS  Google Scholar 

  22. Manges AR, Tabor H, Tellis P, Vincent C, Tellier PP (2008) Endemic and epidemic lineages of Escherichia coli that cause urinary tract infections. Emerg Infect Dis 14(10):1575–1583

    Article  PubMed  CAS  Google Scholar 

  23. Rogers BA, Aminzadeh Z, Hayashi Y, Paterson DL (2011) Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clin Infect Dis 53(1):49–56

    Article  PubMed  Google Scholar 

  24. Bailey JK, Pinyon JL, Anantham S, Hall RM (2010) Distribution of human commensal Escherichia coli phylogenetic groups. J Clin Microbiol 48(9):3455–3456

    Article  PubMed  Google Scholar 

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Acknowledgements

Thank you to Prof. Mark Schembri for his review of this manuscript.

Conflict of interests

BR, KK, HS, MJ and DP declare that they have no conflicts of interest.

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Correspondence to B. A. Rogers.

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Rogers, B.A., Kennedy, K., Sidjabat, H.E. et al. Prolonged carriage of resistant E. coli by returned travellers: clonality, risk factors and bacterial characteristics. Eur J Clin Microbiol Infect Dis 31, 2413–2420 (2012). https://doi.org/10.1007/s10096-012-1584-z

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