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Subsequent infection with extended-spectrum β-lactamase-producing Enterobacteriaceae in patients with prior infection or fecal colonization

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Abstract

In clinical practice, there is a growing need to assess the impact of prior colonization or infection with extended-spectrum β-lactamase-producing Enterobacteriaceae (EPE) on new EPE infections. We have investigated the frequency of, and duration to, a subsequent EPE infection in patients with prior fecal carriage or infection with EPE. Culture data for 3272 EPE-positive patients in Western Sweden during 2004–2014 were evaluated. The median follow-up time was 3.7 years. The first recorded EPE-positive fecal screen, or clinical (urine, blood) culture, and subsequent EPE-positive clinical samples were analyzed, focusing on the first and last recurrence of EPE infection. ESBL Escherichia coli dominated (95%). Almost all (94%) patients initially positive in fecal screen (n = 1436) and 72 and 71% of those initially positive in urine (n = 1717) and blood (n = 119) had no further EPE clinical isolates. Subsequent EPE bacteremia was only detected in 0.7, 1.6, and 4.2% of the respective patient group. Recurrent EPE-positive urine cultures occurred in 27% (460/1717), most (75%) within 6 months, and rarely (13%) after 1 year. Repeated EPE-positive clinical samples were significantly (p < 0.01) more common in patients > 65 years and in men with ESBL Klebsiella pneumoniae. In our low-endemic setting, subsequent EPE infections in previously colonized patients were rare. On the other hand, in patients previously EPE-positive in urine or blood, subsequent EPE urinary tract infections were common, especially within 6 months and in patients > 65 years old.

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References

  1. Pitout JD, Laupland KB (2008) Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8:159–166

    Article  PubMed  CAS  Google Scholar 

  2. Paterson DL, Bonomo RA (2005) Extended-spectrum beta-lactamases: a clinical update. Clinical Microbiol Rev 18:657–686

    Article  CAS  Google Scholar 

  3. World Health Organization (2014) Antimicrobial resistance - Global report on surveillance. Available from: http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748_eng.pdf?ua=1

  4. Schwaber MJ, Carmeli Y (2007) Mortality and delay in effective therapy associated with extended-spectrum beta-lactamase production in Enterobacteriaceae bacteraemia: a systematic review and meta-analysis. J Antimicrob Chemother 60:913–920

    Article  PubMed  CAS  Google Scholar 

  5. Melzer M, Petersen I (2007) Mortality following bacteraemic infection caused by extended spectrum beta-lactamase (ESBL) producing E. coli compared to non-ESBL producing E. coli. J Inf Secur 55:254–259

    Google Scholar 

  6. Tumbarello M, Spanu T, Di Bidino R, Marchetti M, Ruggeri M, Trecarichi EM, De Pascale G, Proli EM, Cauda R, Cicchetti A, Fadda G (2010) Costs of bloodstream infections caused by Escherichia coli and influence of extended-spectrum-beta-lactamase production and inadequate initial antibiotic therapy. Antimicrob Agents Chemother 54:4085–4091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Alevizakos M, Karanika S, Detsis M, Mylonakis E (2016) Colonisation with extended-spectrum beta-lactamase-producing Enterobacteriaceae and risk for infection among patients with solid or haematological malignancy: a systematic review and meta-analysis. Int J Antimicrob Agents 48:647–654

    Article  PubMed  CAS  Google Scholar 

  8. Trecarichi EM, Cauda R, Tumbarello M (2012) Detecting risk and predicting patient mortality in patients with extended-spectrum beta-lactamase-producing Enterobacteriaceae bloodstream infections. Future Microbiol 7:1173–1189

    Article  PubMed  CAS  Google Scholar 

  9. Vodovar D, Marcade G, Rousseau H, Raskine L, Vicaut E, Deye N, Baud FJ, Megarbane B (2014) Predictive factors for extended-spectrum beta-lactamase producing Enterobacteriaceae causing infection among intensive care unit patients with prior colonization. Infection 42:743–748

    Article  PubMed  CAS  Google Scholar 

  10. Reddy P, Malczynski M, Obias A, Reiner S, Jin N, Huang J, Noskin GA, Zembower T (2007) Screening for extended-spectrum beta-lactamase-producing Enterobacteriaceae among high-risk patients and rates of subsequent bacteremia. Clin Infect 45:846–852

    Article  CAS  Google Scholar 

  11. Rottier WC, Bamberg YR, Dorigo-Zetsma JW, van der Linden PD, Ammerlaan HS, Bonten MJ (2015) Predictive value of prior colonization and antibiotic use for third-generation cephalosporin-resistant enterobacteriaceae bacteremia in patients with sepsis. Clin Infect Dis 60:1622–1630

    Article  PubMed  Google Scholar 

  12. Turbett SE, Mansour MK (2016) Editorial commentary: fecal ESBL screening: are we ready for this information? Clin Infect Dis 63:319–321

    Article  PubMed  PubMed Central  Google Scholar 

  13. Armand-Lefevre L, Angebault C, Barbier F, Hamelet E, Defrance G, Ruppe E, Bronchard R, Lepeule R, Lucet JC, El Mniai A, Wolff M, Montravers P, Plesiat P, Andremont A (2013) Emergence of imipenem-resistant gram-negative bacilli in intestinal flora of intensive care patients. Antimicrob Agents Chemother 57:1488–1495

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Available from: http://www.eucast.org/clinical_breakpoints/

  15. Karami N, Helldal L, Welinder-Olsson C, Ahren C, Moore ER (2013) Sub-typing of extended-spectrum-beta-lactamase-producing isolates from a nosocomial outbreak: application of a 10-loci generic Escherichia coli multi-locus variable number tandem repeat analysis. PLoS One 8:e83030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Goulenok T, Ferroni A, Bille E, Lecuyer H, Join-Lambert O, Descamps P, Nassif X, Zahar JR (2013) Risk factors for developing ESBL E. coli: can clinicians predict infection in patients with prior colonization? J Hosp Infect 84:294–299

    Article  PubMed  CAS  Google Scholar 

  17. Martinez JA, Aguilar J, Almela M, Marco F, Soriano A, Lopez F, Balasso V, Pozo L, Mensa J (2006) Prior use of carbapenems may be a significant risk factor for extended-spectrum beta-lactamase-producing Escherichia coli or Klebsiella spp. in patients with bacteraemia. J Antimicrob Chemother 58:1082–1085

    Article  PubMed  CAS  Google Scholar 

  18. Cornejo-Juarez P, Suarez-Cuenca JA, Volkow-Fernandez P, Silva-Sanchez J, Barrios-Camacho H, Najera-Leon E, Velazquez-Acosta C, Vilar-Compte D (2016) Fecal ESBL Escherichia coli carriage as a risk factor for bacteremia in patients with hematological malignancies. Support Care Cancer 24:253–259

    Article  PubMed  Google Scholar 

  19. Arnan M, Gudiol C, Calatayud L, Linares J, Dominguez MA, Batlle M, Ribera JM, Carratala J, Gudiol F (2011) Risk factors for, and clinical relevance of, faecal extended-spectrum beta-lactamase producing Escherichia coli (ESBL-EC) carriage in neutropenic patients with haematological malignancies. Eur J Clin Microb Infect Dis 30:355–360

    Article  CAS  Google Scholar 

  20. Ny S, Lofmark S, Borjesson S, Englund S, Ringman M, Bergstrom J, Naucler P, Giske CG, Byfors S (2017) Community carriage of ESBL-producing Escherichia coli is associated with strains of low pathogenicity: a Swedish nationwide study. J Antimicrob Chemother 72:582–588

    Article  PubMed  Google Scholar 

  21. Skjot-Rasmussen L, Hammerum AM, Jakobsen L, Lester CH, Larsen P, Frimodt-Moller N (2011) Persisting clones of Escherichia coli isolates from recurrent urinary tract infection in men and women. J Med Microbiol 60:550–554

    Article  PubMed  Google Scholar 

  22. Ejrnaes K, Sandvang D, Lundgren B, Ferry S, Holm S, Monsen T, Lundholm R, Frimodt-Moller N (2006) Pulsed-field gel electrophoresis typing of Escherichia coli strains from samples collected before and after pivmecillinam or placebo treatment of uncomplicated community-acquired urinary tract infection in women. J Clin Microbiol 44:1776–1781

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Banerjee R, Johnson JR (2014) A new clone sweeps clean: the enigmatic emergence of Escherichia coli sequence type 131. Antimicrob Agents Chemother 58:4997–5004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Foxman B, Gillespie B, Koopman J, Zhang L, Palin K, Tallman P, Marsh JV, Spear S, Sobel JD, Marty MJ, Marrs CF (2000) Risk factors for second urinary tract infection among college women. Am J Epidemiol 151:1194–1205

    Article  PubMed  CAS  Google Scholar 

  25. Foxman B (1990) Recurring urinary tract infection: incidence and risk factors. Am J Public Health 80:331–333

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Ikaheimo R, Siitonen A, Heiskanen T, Karkkainen U, Kuosmanen P, Lipponen P, Makela PH (1996) Recurrence of urinary tract infection in a primary care setting: analysis of a 1-year follow-up of 179 women. Clin Infect Dis 22:91–99

    Article  PubMed  CAS  Google Scholar 

  27. Karkkainen UM, Ikaheimo R, Katila ML, Siitonen A (2000) Recurrence of urinary tract infections in adult patients with community-acquired pyelonephritis caused by E. coli: a 1-year follow-up. Scand J Infect Dis 32:495–499

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank the personnel at the Clinical Microbiology Laboratory at Sahlgrenska University Hospital for performing the bacterial culturing.

Funding

This work was supported by the Centre for Antibiotic Resistance Research (CARe), University of Gothenburg and by Region Västra Götaland, Sweden (VGFOUREG-660231).

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Authors and Affiliations

  1. Department of Infectious Diseases, Institute of Biomedicine, Sahlgrenska Academy and Centre for Antibiotic Resistance Research (CARe), University of Gothenburg, Gothenburg, Sweden

    Anna Lindblom, Nahid Karami & Christina Åhrén

  2. Department of Clinical Microbiology, Sahlgrenska University Hospital, Guldhedsgatan 10 A, 413 46, Gothenburg, Sweden

    Anna Lindblom, Nahid Karami & Tim Magnusson

  3. Swedish Strategic Program Against Antimicrobial Resistance (Strama), Region Västra Götaland, Gothenburg, Sweden

    Christina Åhrén

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  1. Anna Lindblom
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  2. Nahid Karami
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  4. Christina Åhrén
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Correspondence to Anna Lindblom.

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This study was conducted in accordance with the Declaration of Helsinki and national and institutional regulations.

Ethical approval

The study was approved by the Regional Ethical Review Board in Gothenburg, Sweden (recordal: 170-17).

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The authors declare that they have no conflict of interest.

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Lindblom, A., Karami, N., Magnusson, T. et al. Subsequent infection with extended-spectrum β-lactamase-producing Enterobacteriaceae in patients with prior infection or fecal colonization. Eur J Clin Microbiol Infect Dis 37, 1491–1497 (2018). https://doi.org/10.1007/s10096-018-3275-x

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  • DOI: https://doi.org/10.1007/s10096-018-3275-x

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