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Detection and characterization of carbapenemase-producing Enterobacteriaceae in wounded Syrian patients admitted to hospitals in northern Israel

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Abstract

Since 2013, four hospitals in northern Israel have been providing care for Syrian nationals, primarily those wounded in the ongoing civil war. We analyzed carbapenemase-producing Enterobacteriaceae (CPE) isolates obtained from these patients. Isolate identification was performed using the VITEK 2 system. Polymerase chain reaction (PCR) was performed for the presence of bla KPC, bla NDM, and bla OXA-48. Susceptibility testing and genotyping were performed on selected isolates. During the study period, 595 Syrian patients were hospitalized, most of them young men. Thirty-two confirmed CPE isolates were grown from cultures taken from 30 patients. All but five isolates were identified as Klebsiella pneumoniae and Escherichia coli. Nineteen isolates produced NDM and 13 produced OXA-48. Among a further 29 isolates tested, multilocus sequence typing (MLST) showed that ST278 and ST38 were the major sequence types among the NDM-producing K. pneumoniae and OXA-48-producing E. coli isolates, respectively. Most were resistant to all three carbapenems in use in Israel and to gentamicin, but susceptible to colistin and fosfomycin. The source for bacterial acquisition could not be determined; however, some patients admitted to different medical centers were found to carry the same sequence type. CPE containing bla NDM and bla OXA-48 were prevalent among Syrian wounded hospitalized patients in northern Israel. The finding of the same sequence type among patients at different medical centers implies a common, prehospital source for these patients. These findings have implications for public health throughout the region.

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References

  1. El-Herte RI, Kanj SS, Matar GM, Araj GF (2012) The threat of carbapenem-resistant Enterobacteriaceae in Lebanon: an update on the regional and local epidemiology. J Infect Public Health 5:233–243. doi:10.1016/j.jiph.2012.02.003

    Article  PubMed  Google Scholar 

  2. Glupczynski Y, Huang TD, Bouchahrouf W et al (2012) Rapid emergence and spread of OXA-48-producing carbapenem-resistant Enterobacteriaceae isolates in Belgian hospitals. Int J Antimicrob Agents 39:168–172. doi:10.1016/j.ijantimicag.2011.10.005

    Article  PubMed  CAS  Google Scholar 

  3. Österblad M, Kirveskari J, Hakanen AJ, Tissari P, Vaara M, Jalava J (2012) Carbapenemase-producing Enterobacteriaceae in Finland: the first years (2008–11). J Antimicrob Chemother 67:2860–2864. doi:10.1093/jac/dks299

    Article  PubMed  Google Scholar 

  4. Peretz A, Labay K, Zonis Z, Glikman D (2014) Disengagement does not apply to bacteria: a high carriage rate of antibiotic-resistant pathogens among Syrian civilians treated in Israeli hospitals. Clin Infect Dis 59:753–754. doi:10.1093/cid/ciu374

    Article  PubMed  Google Scholar 

  5. Zarka S, Barhoum M, Bader T et al (2014) Israel’s medical support to victims of the civil War in Syria. Isr Med Assoc J 16:71–72

    PubMed  Google Scholar 

  6. Dortet L, Poirel L, Nordmann P (2012) Rapid identification of carbapenemase types in Enterobacteriaceae and Pseudomonas spp. by using a biochemical test. Antimicrob Agents Chemother 56:6437–6440. doi:10.1128/AAC.01395-12

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S (2005) Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 43:4178–4182

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  8. Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  9. Poirel L, Potron A, Nordmann P (2012) OXA-48-like carbapenemases: the phantom menace. J Antimicrob Chemother 67:1597–1606. doi:10.1093/jac/dks121

    Article  PubMed  CAS  Google Scholar 

  10. Rafei R, Dabboussi F, Hamze M et al (2014) First report of bla NDM-1-producing Acinetobacter baumannii isolated in Lebanon from civilians wounded during the Syrian war. Int J Infect Dis 21:21–23. doi:10.1016/j.ijid.2014.01.004

    Article  PubMed  CAS  Google Scholar 

  11. Adler A, Shklyar M, Schwaber MJ et al (2011) Introduction of OXA-48-producing Enterobacteriaceae to Israeli hospitals by medical tourism. J Antimicrob Chemother 66:2763–2766

    Article  PubMed  CAS  Google Scholar 

  12. Hammerum AM, Larsen AR, Hansen F et al (2012) Patients transferred from Libya to Denmark carried OXA-48-producing Klebsiella pneumoniae, NDM-1-producing Acinetobacter baumannii and meticillin-resistant Staphylococcus aureus. Int J Antimicrob Agents 40:191–192. doi:10.1016/j.ijantimicag.2012.05.003

    Article  PubMed  CAS  Google Scholar 

  13. Potron A, Poirel L, Rondinaud E, Nordmann P (2013) Intercontinental spread of OXA-48 beta-lactamase-producing Enterobacteriaceae over a 11-year period, 2001 to 2011. Euro Surveill 18. pii: 20549

  14. Espedido BA, Steen JA, Ziochos H et al (2013) Whole genome sequence analysis of the first Australian OXA-48-producing outbreak-associated Klebsiella pneumoniae isolates: the resistome and in vivo evolution. PLoS One 8, e59920. doi:10.1371/journal.pone.0059920

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  15. Poirel L, Bernabeu S, Fortineau N, Podglajen I, Lawrence C, Nordmann P (2011) Emergence of OXA-48-producing Escherichia coli clone ST38 in France. Antimicrob Agents Chemother 55:4937–4938. doi:10.1128/AAC.00413-11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Dimou V, Dhanji H, Pike R, Livermore DM, Woodford N (2012) Characterization of Enterobacteriaceae producing OXA-48-like carbapenemases in the UK. J Antimicrob Chemother 67:1660–1665. doi:10.1093/jac/dks124

    Article  PubMed  CAS  Google Scholar 

  17. Crémet L, Bourigault C, Lepelletier D et al (2012) Nosocomial outbreak of carbapenem-resistant Enterobacter cloacae highlighting the interspecies transferability of the bla OXA-48 gene in the gut flora. J Antimicrob Chemother 67:1041–1043

    Article  PubMed  Google Scholar 

  18. Agabou A, Pantel A, Ouchenane Z et al (2014) First description of OXA-48-producing Escherichia coli and the pandemic clone ST131 from patients hospitalised at a military hospital in Algeria. Eur J Clin Microbiol Infect Dis 33:1641–1646. doi:10.1007/s10096-014-2122-y

    Article  PubMed  CAS  Google Scholar 

  19. Poirel L, Yilmaz M, Istanbullu A et al (2014) Spread of NDM-1-producing Enterobacteriaceae in a neonatal intensive care unit in Istanbul, Turkey. Antimicrob Agents Chemother 58:2929–2933. doi:10.1128/AAC.02047-13

    Article  PubMed  PubMed Central  Google Scholar 

  20. Poirel L, Dortet L, Bernabeu S, Nordmann P (2011) Genetic features of bla NDM-1-positive Enterobacteriaceae. Antimicrob Agents Chemother 55:5403–5407. doi:10.1128/AAC.00585-11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. Voulgari E, Gartzonika C, Vrioni G et al (2014) The Balkan region: NDM-1-producing Klebsiella pneumoniae ST11 clonal strain causing outbreaks in Greece. J Antimicrob Chemother 69:2091–2097. doi:10.1093/jac/dku105

    Article  PubMed  CAS  Google Scholar 

  22. Bushnell G, Mitrani-Gold F, Mundy LM (2013) Emergence of New Delhi metallo-β-lactamase type 1-producing Enterobacteriaceae and non-Enterobacteriaceae: global case detection and bacterial surveillance. Int J Infect Dis 17:e325–e333. doi:10.1016/j.ijid.2012.11.025

    Article  PubMed  CAS  Google Scholar 

  23. Schwaber MJ, Lev B, Israeli A et al (2011) Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin Infect Dis 52:848–855. doi:10.1093/cid/cir025

    Article  PubMed  Google Scholar 

  24. Schechner V, Kotlovsky T, Tarabeia J et al (2011) Predictors of rectal carriage of carbapenem-resistant Enterobacteriaceae (CRE) among patients with known CRE carriage at their next hospital encounter. Infect Control Hosp Epidemiol 32:497–503. doi:10.1086/659762

    Article  PubMed  Google Scholar 

  25. Oren I, Sprecher H, Finkelstein R et al (2013) Eradication of carbapenem-resistant Enterobacteriaceae gastrointestinal colonization with nonabsorbable oral antibiotic treatment: a prospective controlled trial. Am J Infect Control 41:1167–1172. doi:10.1016/j.ajic.2013.04.018

    Article  PubMed  CAS  Google Scholar 

  26. Berçot B, Poirel L, Dortet L, Nordmann P (2011) In vitro evaluation of antibiotic synergy for NDM-1-producing Enterobacteriaceae. J Antimicrob Chemother 66:2295–2297. doi:10.1093/jac/dkr296

    Article  PubMed  Google Scholar 

  27. Tzouvelekis LS, Markogiannakis A, Psichogiou M, Tassios PT, Daikos GL (2012) Carbapenemases in Klebsiella pneumoniae and other Enterobacteriaceae: an evolving crisis of global dimensions. Clin Microbiol Rev 25:682–707. doi:10.1128/CMR.05035-11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  28. Tzouvelekis LS, Markogiannakis A, Piperaki E, Souli M, Daikos GL (2014) Treating infections caused by carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect 20:862–872. doi:10.1111/1469-0691.12697

    Article  PubMed  CAS  Google Scholar 

  29. Dautzenberg MJ, Ossewaarde JM, de Kraker ME et al (2014) Successful control of a hospital-wide outbreak of OXA-48 producing Enterobacteriaceae in the Netherlands, 2009 to 2011. Euro Surveill 19. pii: 20723

  30. Lachish T, Elimelech M, Arieli N, Adler A, Rolain JM, Assous MV (2012) Emergence of New Delhi metallo-β-lactamase in Jerusalem, Israel. Int J Antimicrob Agents 40:566–567. doi:10.1016/j.ijantimicag.2012.07.011

    Article  PubMed  CAS  Google Scholar 

  31. Adler A, Solter E, Masarwa S et al (2013) Epidemiological and microbiological characteristics of an outbreak caused by OXA-48-producing Enterobacteriaceae in a neonatal intensive care unit in Jerusalem, Israel. J Clin Microbiol 51:2926–2930. doi:10.1128/JCM.01049-13

    Article  PubMed  PubMed Central  Google Scholar 

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    Authors and Affiliations

    1. National Center for Infection Control, Israel Ministry of Health, Tel Aviv, Israel

      A. Lerner, E. Solter, E. Rachi, A. Adler, Y. Carmeli & M. J. Schwaber

    2. Department of Infectious Disease Consultation Service, Ziv Medical Center, Safed, Israel

      H. Rechnitzer, D. Miron & L. Krupnick

    3. Infectious Disease Unit, Galilee Medical Center, Nahariya, Israel

      S. Sela, E. Aga & Y. Ziv

    4. Infectious Disease Unit, Baruch Padeh Medical Center, Poriya, Israel

      A. Peretz, K. Labay & G. Rahav

    5. Infectious Diseases Institute, Rambam Health Care Campus, Haifa, Israel

      Y. Geffen, K. Hussein & O. Eluk

    6. Faculty of Medicine in the Galilee, Bar-Ilan University, Ramat Gan, Israel

      H. Rechnitzer, D. Miron, L. Krupnick, S. Sela, E. Aga, Y. Ziv, A. Peretz, K. Labay & G. Rahav

    7. Ruth and Bruce Rappaport Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel

      Y. Geffen, K. Hussein & O. Eluk

    8. Reference Laboratory, National Center for Infection Control, 6 Weizmann St., Tel Aviv, 6423906, Israel

      A. Lerner, E. Rachi & A. Adler

    9. Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

      A. Lerner, E. Solter, E. Rachi, A. Adler, Y. Carmeli & M. J. Schwaber

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    1. A. Lerner
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    2. E. Solter
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    3. E. Rachi
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    Correspondence to A. Lerner.

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    The authors declare no competing interests.

    Compliance with ethical standards

    All procedures performed in studies involving human participants were in accordance with the ethical standards of the jurisdictional research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

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    A. Lerner and E. Solter contributed equally to this work.

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    Lerner, A., Solter, E., Rachi, E. et al. Detection and characterization of carbapenemase-producing Enterobacteriaceae in wounded Syrian patients admitted to hospitals in northern Israel. Eur J Clin Microbiol Infect Dis 35, 149–154 (2016). https://doi.org/10.1007/s10096-015-2520-9

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    • DOI: https://doi.org/10.1007/s10096-015-2520-9

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