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Incidence and antimicrobial resistance trends in bloodstream infections caused by ESKAPE and Escherichia coli at a large teaching hospital in Rome, a 9-year analysis (2007–2015)

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Abstract

The proportion of antimicrobial resistance (AMR) among the ESKAPE and Escherichia coli (ESKAPEEc) pathogens causing bloodstream infection (BSI) increased worldwide. We described longitudinal trends in ESKAPEEc BSI and AMR over 9 years (2007–2015) at a large teaching hospital in Italy. Of 9720 unique BSI episodes, 6002 (61.7%) were caused by ESKAPEEc pathogens. The majority of these episodes (4374; 72.9%) were hospital-onset infections. The most frequent pathogen was E. coli (32.8%), followed by Staphylococcus aureus (20.6%), Klebsiella pneumoniae (16.1%), and Pseudomonas aeruginosa (11.6%). There was a significant increase of hospital-onset K. pneumoniae (from 2.3 to 5.0 per 10,000 patient-days; P = 0.001) and community-onset E. coli (from 3.3 to 9. 1 per 10,000 emergency admissions; P = 0.04) BSIs. Among hospital-onset BSIs, increases of extended-spectrum β-lactamase (ESBL)-producing E. coli (from 25.4 to 35.2%, P = 0.006), carbapenemase-producing K. pneumoniae (from 4.2 to 51.6%, P < 0.001), and methicillin-resistant S. aureus (from 33.9 to 44.4%, P < 0.001) BSIs were observed between the 2007–2009 and 2010–2012 study periods. In contrast, a decrease of BSIs caused by P. aeruginosa resistant to ceftazidime (from 45.5 to 28.2%, P < 0.001), ciprofloxacin (from 46 to 36.3%, P = 0.05), and meropenem (from 55 to 39.9%, P = 0.03) was observed through all 9 years of the study period. Among community-onset BSIs, increases of BSIs caused by ESBL-producing E. coli (from 28.6 to 42.2%, P = 0.002) and carbapenemase-producing K. pneumoniae (from 0 to 17.6%) were observed between the 2007–2009 and 2010–2012 study periods. Our findings show increased rates of BSI and relative AMR for specific pathogen-health care setting combinations, and call for continued active surveillance and infection control policies.

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References

  1. Goto M, Al-Hasan MN (2013) Overall burden of bloodstream infection and nosocomial bloodstream infection in North America and Europe. Clin Microbiol Infect 19:501–509. https://doi.org/10.1111/1469-0691.12195

    Article  PubMed  CAS  Google Scholar 

  2. Laupland KB (2013) Incidence of bloodstream infection. Clin Microbiol Infect 19:492–500. https://doi.org/10.1111/1469-0691.12144

    Article  PubMed  CAS  Google Scholar 

  3. Rice LB (2008) Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J Infect Dis 197:1079–1081. https://doi.org/10.1086/533452

    Article  PubMed  Google Scholar 

  4. Peleg AY, Hooper DC (2010) Hospital-acquired infections due to Gram-negative bacteria. N Engl J Med 362:1804–1813. https://doi.org/10.1056/NEJMra0904124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Luzzaro F, Ortisi G, Larosa M, Drago M, Brigante G, Gesu G (2011) Prevalence and epidemiology of microbial pathogens causing bloodstream infections: results of the OASIS multicenter study. Diagn Microbiol Infect Dis 69:363–369. https://doi.org/10.1016/j.diagmicrobio.2010.10.016

    Article  PubMed  Google Scholar 

  6. Karlowsky JA, Hoban DJ, Hackel MA, Lob SH, Sahm DF (2017) Resistance among Gram-negative ESKAPE pathogens isolated from hospitalized patients with intra-abdominal and urinary tract infections in Latin American countries: SMART 2013-2015. Braz J Infect Dis 21:343–348. https://doi.org/10.1016/j.bjid.2017.03.006

    Article  PubMed  Google Scholar 

  7. Zhang H, Yang Q, Liao K, Ni Y, Yu Y, Hu B, Sun Z, Huang W, Wang Y, Wu A, Feng X, Luo Y, Hu Z, Chu Y, Chen S, Cao B, Su J, Gui B, Duan Q, Zhang S, Shao H, Kong H, Badal RE, Xu Y (2015) Antimicrobial susceptibilities of aerobic and facultative Gram-negative bacilli from intra-abdominal iInfections in patients from seven regions in China in 2012 and 2013. Antimicrob Agents Chemother 60:245–251. https://doi.org/10.1128/AAC.00956-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Goto M, McDanel JS, Jones MM, Livorsi DJ, Ohl ME, Beck BF, Richardson KK, Alexander B, Perencevich EN (2017) Antimicrobial nonsusceptibility of Gram-negative bloodstream isolates, veterans health administration system, United States, 2003-20131. Emerg Infect Dis 23:1815–1825. https://doi.org/10.3201/eid2311.161214

    Article  PubMed  PubMed Central  Google Scholar 

  9. World Health Organization (2015) Global Action Plan on Antimicrobial resistance. Home page at: http://www.wpro.who.int. Accessed 04 May 2017

  10. World Health Organization (2017) Global Priority List of Antibiotic-Resistance Bacteria to Guide Research, Discovery, and Development of New Antibiotics. Home page at: http://www.who.int. Accessed 4 January 2018

  11. Tängdén T, Giske CG (2015) Global dissemination of extensively drug-resistant carbapenemase-producing Enterobacteriaceae: clinical perspectives on detection, treatment and infection control. J Intern Med 277:501–512. https://doi.org/10.1111/joim.12342

    Article  PubMed  CAS  Google Scholar 

  12. Giani T, Antonelli A, Caltagirone M, Mauri C, Nicchi J, Arena F, Nucleo E, Bracco S, Pantosti A; AMCLI-CoSA survey participants, Luzzaro F, Pagani L, Rossolini GM (2017) Evolving beta-lactamase epidemiology in Enterobacteriaceae from Italian nationwide surveillance, October 2013: KPC-carbapenemase spreading among outpatients. Euro Surveill 22(31): DOI: https://doi.org/10.2807/1560-7917

  13. Samuelsen Ø, Overballe-Petersen S, Bjørnholt JV, Brisse S, Doumith M, Woodford N, Hopkins KL, Aasnæs B, Haldorsen B, Sundsfjord A, Norwegian Study Group on CPE (2017) Molecular and epidemiological characterization of carbapenemase-producing Enterobacteriaceae in Norway, 2007 to 2014. PLoS One 12(11):e0187832. https://doi.org/10.1371/journal.pone.0187832

    Article  PubMed  PubMed Central  Google Scholar 

  14. European Centre for Disease Prevention and Control (2017) Surveillance of antimicrobial resistance in Europe 2016. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Home page at: https://ecdc.europa.eu/. Accessed 04 January 2018

  15. European Centre for Disease Prevention and Control (2016) Summary of the latest data on antibiotic resistance in the European Union. Home page at: https://ecdc.europa.eu/. Accessed 04 January 2018

  16. Gagliotti C, Balode A, Baquero F, Degener J, Grundmann H, Gür D, Jarlier V, Kahlmeter G, Monen J, Monnet DL, Rossolini GM, Suetens C, Weist K, Heuer O; EARS-Net Participants (Disease Specific Contact Points for AMR) (2011) Escherichia coli and Staphylococcus aureus: bad news and good news from the European Antimicrobial Resistance Surveillance Network (EARS-Net, formerly EARSS), 2002 to 2009. Euro Surveill 16(11):pii=19819. https://doi.org/10.2807/ese.16.11.19819-en

  17. Schlackow I, Stoesser N, Walker AS, Crook DW, Peto TE, Wyllie DH, Infections in Oxfordshire Research Database Team (2012) Increasing incidence of Escherichia coli bacteraemia is driven by an increase in antibiotic-resistant isolates: electronic database study in Oxfordshire 1999–2011. J Antimicrob Chemother 67:1514–1524. https://doi.org/10.1093/jac/dks082

    Article  PubMed  CAS  Google Scholar 

  18. Arnaud I, Maugat S, Jarlier V, Astagneau P; National Early Warning, Investigation and Surveillance of Healthcare-Associated Infections Network (RAISIN)/multidrug resistance study group (2015) Ongoing increasing temporal and geographical trends of the incidence of extended-spectrum beta-lactamase-producing Enterobacteriaceae infections in France, 2009 to 2013. Euro Surveill 20(36):pii=30014. https://doi.org/10.2807/1560-7917

  19. Perez F, Endimiani A, Hujer KM, Bonomo RA (2007) The continuing challenge of ESBLs. Curr Opin Pharmacol 7:459–469. https://doi.org/10.1016/j.coph.2007.08.003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Founou RC, Founou LL, Essack SY (2017) Clinical and economic impact of antibiotic resistance in developing countries: a systematic review and meta-analysis. PLoS One 12(12):e0189621. https://doi.org/10.1371/journal.pone.0189621

    Article  PubMed  PubMed Central  Google Scholar 

  21. Vrijens F, Hulstaert F, Van de Sande S, Devriese S, Morales I, Parmentier Y (2010) Hospital-acquired, laboratory-confirmed bloodstream infections: linking national surveillance data to clinical and financial hospital data to estimate increased length of stay and healthcare costs. J Hosp Infect 75:158–162. https://doi.org/10.1016/j.jhin.2009.12.006

    Article  PubMed  CAS  Google Scholar 

  22. Thaden JT, Li Y, Ruffin F, Maskarinec SA, Hill-Rorie JM, Wanda LC, Reed SD, Fowler VG Jr (2017) Increased costs associated with bloodstream infections caused by multidrug-resistant Gram-negative bacteria are due primarily to patients with hospital-acquired infections. Antimicrob Agents Chemother 61:e01709-16. https://doi.org/10.1128/AAC.01709-16

    Article  PubMed  PubMed Central  Google Scholar 

  23. Tumbarello M, Sanguinetti M, Montuori E, Trecarichi EM, Posteraro B, Fiori B, Citton R, D'Inzeo T, Fadda G, Cauda R, Spanu T (2007) Predictors of mortality in patients with bloodstream infections caused by extended-spectrum-beta-lactamase-producing Enterobacteriaceae: importance of inadequate initial antimicrobial treatment. Antimicrob Agents Chemother 51:1987–1994. https://doi.org/10.1128/AAC.01509-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Tumbarello M, Sali M, Trecarichi EM, Leone F, Rossi M, Fiori B, De Pascale G, D'Inzeo T, Sanguinetti M, Fadda G, Cauda R, Spanu T (2008) Bloodstream infections caused by extended-spectrum-beta-lactamase- producing Escherichia coli: risk factors for inadequate initial antimicrobial therapy. Antimicrob Agents Chemother 52:3244–3252. https://doi.org/10.1128/AAC.00063-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Tumbarello M, Repetto E, Trecarichi EM, Bernardini C, De Pascale G, Parisini A, Rossi M, Molinari MP, Spanu T, Viscoli C, Cauda R, Bassetti M (2011) Multidrug-resistant Pseudomonas aeruginosa bloodstream infections: risk factors and mortality. Epidemiol Infect 139:1740–1749. https://doi.org/10.1017/S0950268810003055

    Article  PubMed  CAS  Google Scholar 

  26. Tumbarello M, Viale P, Viscoli C, Trecarichi EM, Tumietto F, Marchese A, Spanu T, Ambretti S, Ginocchio F, Cristini F, Losito AR, Tedeschi S, Cauda R, Bassetti M (2012) Predictors of mortality in bloodstream infections caused by Klebsiella pneumoniae carbapenemase-producing Kp: importance of combination therapy. Clin Infect Dis 55:943–950. https://doi.org/10.1093/cid/cis588

    Article  PubMed  CAS  Google Scholar 

  27. Tumbarello M, Trecarichi EM, De Rosa FG, Giannella M, Giacobbe DR, Bassetti M, Losito AR, Bartoletti M, Del Bono V, Corcione S, Maiuro G, Tedeschi S, Celani L, Cardellino CS, Spanu T, Marchese A, Ambretti S, Cauda R, Viscoli C, Viale P, ISGRI-SITA (Italian Study Group on Resistant Infections of the Società Italiana Terapia Antinfettiva) (2015) Infections caused by KPC-producing Klebsiella pneumoniae: differences in therapy and mortality in a multicentre study. J Antimicrob Chemother 70:2133–2143. https://doi.org/10.1093/jac/dkv086

    Article  PubMed  CAS  Google Scholar 

  28. Bassetti M, Peghin M, Trecarichi EM, Carnelutti A, Righi E, Del Giacomo P, Ansaldi F, Trucchi C, Alicino C, Cauda R, Sartor A, Spanu T, Scarparo C, Tumbarello M (2017) Characteristics of Staphylococcus aureus bacteraemia and predictors of early and late mortality. PLoS One 12:e0170236. https://doi.org/10.1371/journal.pone.0170236

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. European Committee on Antimicrobial Susceptibility Testing (2018) Breakpoint tables for interpretation of MICs and zone diameters. Version 8. 0. Home page at: http://www.eucast.org. Accessed 8 January 2018

  30. European Committee on Antimicrobial Susceptibility Testing (2017) EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. Version 2.0. 0 . Home page at: http://www.eucast.org . Accessed 20 May 2017

  31. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281. https://doi.org/10.1111/j.1469-0691.2011.03570

    Article  PubMed  CAS  Google Scholar 

  32. Kelly AM, Mathema B, Larson EL (2017) Carbapenem-resistant Enterobacteriaceae in the community: a scoping review. Int J Antimicrob Agents 50(2):127–134. https://doi.org/10.1016/j.ijantimicag.2017.03.012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Mendes RE, Spanu T, Deshpande L, Castanheira M, Jones RN, Fadda G (2009) Clonal dissemination of two clusters of Acinetobacter baumannii producing OXA-23 or OXA-58 in Rome, Italy. Clin Microbiol Infect 15:588–592. https://doi.org/10.1111/j.1469-0691.2009.02770

    Article  PubMed  CAS  Google Scholar 

  34. Rello J, van Engelen TSR, Alp E, Calandra T, Cattoir V, Kern WV, Netea MG, Nseir S, Opal SM, van de Veerdonk FL, Wilcox MH, Wiersinga WJ (2018) Towards precision medicine in Sepsis: a position paper from the European Society of Clinical Microbiology and Infectious Diseases. Clin Microbiol Infect. https://doi.org/10.1016/j.cmi.2018.03.011

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Acknowledgments

The authors would like to thank Maria Federica Ventriglia for her technical assistance.

Funding

This work was performed as part of our routine work. No external funding was required for the project.

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Correspondence to Maurizio Sanguinetti.

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The authors declare that they have no conflicts of interest.

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The Ethics Committee of our institution approved the study (no. 0040288).

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Because of the retrospective nature of the study, informed consent was not required.

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De Angelis, G., Fiori, B., Menchinelli, G. et al. Incidence and antimicrobial resistance trends in bloodstream infections caused by ESKAPE and Escherichia coli at a large teaching hospital in Rome, a 9-year analysis (2007–2015). Eur J Clin Microbiol Infect Dis 37, 1627–1636 (2018). https://doi.org/10.1007/s10096-018-3292-9

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