CEN Case Reports

, Volume 8, Issue 1, pp 38–41 | Cite as

NDM-1-producing Enterobacter aerogenes isolated from a patient with a JJ ureteric stent in situ

  • Irena Franolić
  • Branka Bedenić
  • Nataša Beader
  • Amarela Lukić-Grlić
  • Slobodan Mihaljević
  • Luka Bielen
  • Gernot Zarfel
  • Tomislav MeštrovićEmail author
Case Report


Urinary tract infections after JJ stent insertion are among the most common complications, and the associated microorganisms carry more antibiotic resistance determinants than those found in urine prior to stent insertion. In line with the trends in healthcare epidemiology which implicate multi-resistant microorganisms in a plethora of healthcare-associated infections, prosthetic stent material also represents an ideal milieu for biofilm formation and subsequent infection development with resistant bacterial agents. Here we describe a case of a 73-year-old Caucasian woman presenting with urinary tract infection after JJ ureteric stent insertion due to ureteric obstruction and hydronephrosis of her left kidney. Extensive microbiological work-up and comprehensive molecular analysis identified the putative microorganism as carbapenem-resistant Enterobacter aerogenes carrying New Delhi metallo-beta-lactamase 1 (NDM-1). This is a first literature report implicating such extensively resistant strain of this species in early indwelling ureteric stent complications, and also the first report of NDM-1 in Enterobacter aerogenes in Croatia and Europe.


Enterobacter aerogenes NDM-1 Antimicrobial resistance JJ stent Ureteric obstruction 


Author contributions

IF, BB, NB, ALG and GZ conceived and planned the experiments pertinent for this case description. IF, BB, NB and GZ carried out the experiments. IF, BB, ALG, LB and GZ contributed to sample preparation. BB, NB, SM, LB and TM contributed to the interpretation of the results. IF, BB and TM took the lead in writing the manuscript. All authors provided critical feedback and helped shape the research, analysis and final version of the manuscript.


No funding or financial support was received.

Compliance with ethical standards

Conflict of interest

All authors have declared that no conflict of interest exists. No funding or financial support was received.

Ethical approval

The study describes clinical and diagnostic procedures of a specific case. All procedures performed were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.

Informed consent

Informed consent has been obtained from the patient presented in this paper.


  1. 1.
    Liaw A, Knudsen B. Urinary tract infections associated with ureteral stents: a review. Arch Esp Urol. 2016;69:479–84.Google Scholar
  2. 2.
    Al-Marhoon MS, Shareef O, Venkiteswaran KP. Complications and outcomes of JJ stenting of the ureter in urological practice: a single-centre experience. Arab J Urol. 2012;10:372–7.CrossRefGoogle Scholar
  3. 3.
    Kehinde EO, Rotimi VO, Al-Hunayan A, Abdul-Halim H, Boland F, Al-Awadi KA. Bacteriology of urinary tract infection associated with indwelling J ureteral stents. J Endourol. 2004;18:891–6.CrossRefGoogle Scholar
  4. 4.
    Shabeena KS, Bhargava R, Manzoor MAP, Mujeeburahiman M. Characteristics of bacterial colonization after indwelling double-J ureteral stents for different time duration. Urol Ann. 2018;10:71–5.CrossRefGoogle Scholar
  5. 5.
    Zumstein V, Betschart P, Albrich WC, Buhmann MT, Ren Q, Schmid HP, et al. Biofilm formation on ureteral stents—incidence, clinical impact, and prevention. Swiss Med Wkly. 2017;147:w14408.Google Scholar
  6. 6.
    Elwell LP, Falkow S. The characterization of R plasmids and the detection of plasmid-specified genes. In: Lorian V, editor. Antibiotics in laboratory medicine. 2nd ed. Baltimore: Williams and Wilkins; 1986. p. 683–721.Google Scholar
  7. 7.
    Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis. 2006;6:629–40.CrossRefGoogle Scholar
  8. 8.
    Jeong SH, Lee K, Chong Y, Yum JH, Lee SH, Choi HJ, et al. Characterization of a new integron containing VIM-2, a metallo-beta-lactamase gene cassette, in a clinical isolate of Enterobacter cloacae. J Antimicrob Chemother. 2003;51:397–400.CrossRefGoogle Scholar
  9. 9.
    Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, 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;18:268–81.CrossRefGoogle Scholar
  10. 10.
    Ahmad N, Khalid S, Ali SM, Khan AU. Occurrence of blaNDM variants among Enterobacteriaceae from a neonatal intensive care unit in a Northern India hospital. Front Microbiol. 2018;9:407.CrossRefGoogle Scholar
  11. 11.
    Shen Y, Xiao WQ, Gong JM, Pan J, Xu QX. Detection of New Delhi metallo-beta-lactamase (encoded by bla NDM-1) in Enterobacter aerogenes in China. J Clin Lab Anal. 2017;31:e22044.CrossRefGoogle Scholar
  12. 12.
    Tran HH, Ehsani S, Shibayama K, Matsui M, Suzuki S, Nguyen MB, et al. Common isolation of New Delhi metallo-beta-lactamase 1-producing Enterobacteriaceae in a large surgical hospital in Vietnam. Eur J Clin Microbiol Infect Dis. 2015;34:1247–54.CrossRefGoogle Scholar
  13. 13.
    Seija V, Medina Presentado JC, Bado I, Papa Ezdra R, Batista N, Gutierrez C, et al. Sepsis caused by New Delhi metallo-β-lactamase (bla NDM–1) and qnrD-producing Morganella morganii, treated successfully with fosfomycin and meropenem: case report and literature review. Int J Infect Dis. 2015;30:20–6.CrossRefGoogle Scholar
  14. 14.
    Cantón R, Akóva M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect. 2012;18:413–31.CrossRefGoogle Scholar
  15. 15.
    Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis. 2011;17:1791–8.CrossRefGoogle Scholar
  16. 16.
    Mazzariol A, Bošnjak Z, Ballarini P, Budimir A, Bedenić B, Kalenić S, et al. NDM-1-producing Klebsiella pneumoniae, Croatia. Emerg Infect Dis. 2012;18:532–4.CrossRefGoogle Scholar
  17. 17.
    Zujić Atalić V, Bedenić B, Kocsis E, Mazzariol A, Sardelić S, Barišić M, et al. Diversity of carbapenemases in clinical isolates of Enterobacteriaceae in Croatia—the results of a multicentre study. Clin Microbiol Infect. 2014;20:O894–903.CrossRefGoogle Scholar
  18. 18.
    Bedenić B, Sardelić S, Luxner J, Bošnjak Z, Varda-Brkić D, Lukić-Grlić A, et al. Molecular characterization of class b carbapenemases in advanced stage of dissemination and emergence of class d carbapenemases in Enterobacteriaceae from Croatia. Infect Genet Evol. 2016;43:74–82.CrossRefGoogle Scholar

Copyright information

© Japanese Society of Nephrology 2018

Authors and Affiliations

  • Irena Franolić
    • 1
  • Branka Bedenić
    • 2
    • 3
  • Nataša Beader
    • 2
    • 3
  • Amarela Lukić-Grlić
    • 2
    • 4
  • Slobodan Mihaljević
    • 2
    • 3
  • Luka Bielen
    • 2
    • 3
  • Gernot Zarfel
    • 5
  • Tomislav Meštrović
    • 6
    Email author
  1. 1.Institute of Public Health of Lika-Senj CountyGospićCroatia
  2. 2.School of MedicineUniversity of ZagrebZagrebCroatia
  3. 3.University Hospital Centre ZagrebZagrebCroatia
  4. 4.Children’s Hospital ZagrebZagrebCroatia
  5. 5.Institute for Hygiene, Microbiology and Environmental MedicineMedical University of GrazGrazAustria
  6. 6.Clinical Microbiology and Parasitology UnitPolyclinic “Dr. Zora Profozić”ZagrebCroatia

Personalised recommendations