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Co-colonization by multidrug-resistant bacteria in two Greek intensive care units

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European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Our goal was to identify the risk factors for co-colonization by KPC-producing Klebsiella pneumoniae (KPC-Kp), vancomycin-resistant enterococci (VRE), and methicillin-resistant Staphylococcus aureus (MRSA) upon intensive care unit (ICU) admission and during stay. Rectal and nasal samples were taken from each patient upon admission at two Greek ICUs and each week afterwards, and were inoculated onto chromogenic agar. Representative colonies were characterized with standard methods and Vitek-2 technology. The presence of the bla KPC gene (K. pneumoniae isolates), vanA and vanB (Enterococcus faecium and E. faecalis isolates), and mecA (S. aureus isolates) was confirmed by polymerase chain reaction (PCR). Upon ICU admission, among 481 patients, 59 (12 %), 63 (13 %), and 20 (4 %) were colonized by KPC-Kp, VRE, or MRSA, respectively. Simultaneous colonization by KPC-Kp and VRE upon admission (34 patients) was associated with the number of co-morbidities [adjusted odds ratio (aOR): 1.5; confidence interval (CI) 1.0–2.5], administered antibiotics (aOR: 1.7; CI 1.3–2.3), and prior KPC-Kp infection (aOR: 24.4; CI 1.5–396.0). Among patients with an ICU stay of more than 6 days, 181 (73 %), 31 (13 %), and 9 (4 %) became KPC-Kp, VRE, or MRSA colonized during ICU stay, respectively. KPC-Kp colonization was an independent risk factor for VRE colonization upon admission (aOR: 2.7; CI 1.0–7.2) and during stay (aOR: 7.4; CI 2.0–27.4), whereas VRE colonization was a risk factor for KPC-Kp upon admission (aOR: 5.1; CI 1.9–13.9) and MRSA colonization upon admission (aOR: 3.5; CI 1.2–10.1) and during ICU stay (aOR: 14.5; CI 2.1–100.1). Colonization by a multidrug pathogen could promote colonization by another.

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References

  1. Kofteridis DP, Valachis A, Dimopoulou D, Maraki S, Christidou A, Mantadakis E, Samonis G (2014) Risk factors for carbapenem-resistant Klebsiella pneumoniae infection/colonization: a case–case–control study. J Infect Chemother 20(5):293–297

    Article  PubMed  Google Scholar 

  2. Glasner C, Albiger B, Buist G, Tambić Andrasević A, Canton R, Carmeli Y, Friedrich AW, Giske CG, Glupczynski Y, Gniadkowski M, Livermore DM, Nordmann P, Poirel L, Rossolini GM, Seifert H, Vatopoulos A, Walsh T, Woodford N, Donker T, Monnet DL, Grundmann H; European Survey on Carbapenemase-Producing Enterobacteriaceae (EuSCAPE) Working Group (2013) Carbapenemase-producing Enterobacteriaceae in Europe: a survey among national experts from 39 countries, February 2013. Euro Surveill 18(28). pii: 20525

  3. Drougka E, Foka A, Liakopoulos A, Doudoulakakis A, Jelastopulu E, Chini V, Spiliopoulou A, Levidiotou S, Panagea T, Vogiatzi A, Lebessi E, Petinaki E, Spiliopoulou I (2014) A 12-year survey of methicillin-resistant Staphylococcus aureus infections in Greece: ST80-IV epidemic? Clin Microbiol Infect 20(11):O796–O803

    Article  CAS  PubMed  Google Scholar 

  4. European Centre for Disease Prevention and Control (ECDC) (2013) Annual Epidemiological Report 2013. Reporting on 2011 surveillance data and 2012 epidemic intelligence data. ECDC, Stockholm. Available online at: http://ecdc.europa.eu/en/publications/Publications/Annual-Epidemiological-Report-2013.pdf. Accessed 30 March 2015

  5. Schwaber MJ, Lev B, Israeli A, Solter E, Smollan G, Rubinovitch B, Shalit I, Carmeli Y; Israel Carbapenem-Resistant Enterobacteriaceae Working Group (2011) Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin Infect Dis 52(7):848–855

    Article  PubMed  Google Scholar 

  6. Papadimitriou-Olivgeris M, Drougka E, Fligou F, Kolonitsiou F, Liakopoulos A, Dodou V, Anastassiou ED, Petinaki E, Marangos M, Filos KS, Spiliopoulou I (2014) Risk factors for enterococcal infection and colonization by vancomycin-resistant enterococci in critically ill patients. Infection 42(6):1013–1022

    Article  CAS  PubMed  Google Scholar 

  7. Papadimitriou-Olivgeris M, Marangos M, Fligou F, Christofidou M, Sklavou C, Vamvakopoulou S, Anastassiou ED, Filos KS (2013) KPC-producing Klebsiella pneumoniae enteric colonization acquired during intensive care unit stay: the significance of risk factors for its development and its impact on mortality. Diagn Microbiol Infect Dis 77(2):169–173

    Article  PubMed  Google Scholar 

  8. Kalafati M (2012) How Greek healthcare services are affected by the Euro crisis. Emerg Nurse 20(3):26–27

    Article  PubMed  Google Scholar 

  9. Kaier K, Mutters NT, Frank U (2012) Bed occupancy rates and hospital-acquired infections—should beds be kept empty? Clin Microbiol Infect 18(10):941–945

    Article  CAS  PubMed  Google Scholar 

  10. Clinical and Laboratory Standards Institute (CLSI) (2011) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Approved standard—Seventh edition. CLSI document M7-A7. CLSI, Wayne, PA

  11. Queenan AM, Bush K (2007) Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 20(3):440–458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Bell J, Turnidge J, Coombs G, O’Brien F (1998) Emergence and epidemiology of vancomycin-resistant enterococci in Australia. Commun Dis Intell 22(11):249–252

    CAS  PubMed  Google Scholar 

  13. Petinaki E, Arvaniti A, Dimitracopoulos G, Spiliopoulou I (2001) Detection of mecA, mecR1 and mecI genes among clinical isolates of methicillin-resistant staphylococci by combined polymerase chain reactions. J Antimicrob Chemother 47(3):297–304

    Article  CAS  PubMed  Google Scholar 

  14. Papadimitriou-Olivgeris M, Marangos M, Fligou F, Christofidou M, Bartzavali C, Anastassiou ED, Filos KS (2012) Risk factors for KPC-producing Klebsiella pneumoniae enteric colonization upon ICU admission. J Antimicrob Chemother 67(12):2976–2981

    Article  CAS  PubMed  Google Scholar 

  15. Yamakawa K, Tasaki O, Fukuyama M, Kitayama J, Matsuda H, Nakamori Y, Fujimi S, Ogura H, Kuwagata Y, Hamasaki T, Shimazu T (2011) Assessment of risk factors related to healthcare-associated methicillin-resistant Staphylococcus aureus infection at patient admission to an intensive care unit in Japan. BMC Infect Dis 11:303

    Article  PubMed Central  PubMed  Google Scholar 

  16. Hayakawa K, Marchaim D, Bathina P, Martin ET, Pogue JM, Sunkara B, Kamatam S, Ho K, Willis LB, Ajamoughli M, Patel D, Khan A, Lee KP, Suhrawardy U, Jagadeesh KK, Reddy SM, Levine M, Ahmed F, Omotola AM, Mustapha M, Moshos JA, Rybak MJ, Kaye KS (2013) Independent risk factors for the co-colonization of vancomycin-resistant Enterococcus faecalis and methicillin-resistant Staphylococcus aureus in the region most endemic for vancomycin-resistant Staphylococcus aureus isolation. Eur J Clin Microbiol Infect Dis 32(6):815–820

    Article  CAS  PubMed  Google Scholar 

  17. Furuno JP, Perencevich EN, Johnson JA, Wright MO, McGregor JC, Morris JG Jr, Strauss SM, Roghman MC, Nemoy LL, Standiford HC, Hebden JN, Harris AD (2005) Methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci co-colonization. Emerg Infect Dis 11(10):1539–1544

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. McKinnell JA, Miller LG, Eells SJ, Cui E, Huang SS (2013) A systematic literature review and meta-analysis of factors associated with methicillin-resistant Staphylococcus aureus colonization at time of hospital or intensive care unit admission. Infect Control Hosp Epidemiol 34(10):1077–1086

    Article  PubMed  Google Scholar 

  19. Sievert DM, Rudrik JT, Patel JB, McDonald LC, Wilkins MJ, Hageman JC (2008) Vancomycin-resistant Staphylococcus aureus in the United States, 2002–2006. Clin Infect Dis 46(5):668–674

    Article  CAS  PubMed  Google Scholar 

  20. Jung E, Byun S, Lee H, Moon SY, Lee H (2014) Vancomycin-resistant Enterococcus colonization in the intensive care unit: clinical outcomes and attributable costs of hospitalization. Am J Infect Control 42(10):1062–1066

    Article  PubMed  Google Scholar 

  21. Falagas ME, Rafailidis PI, Kofteridis D, Virtzili S, Chelvatzoglou FC, Papaioannou V, Maraki S, Samonis G, Michalopoulos A (2007) Risk factors of carbapenem-resistant Klebsiella pneumoniae infections: a matched case control study. J Antimicrob Chemother 60(5):1124–1130

    Article  CAS  PubMed  Google Scholar 

  22. Celen MK, Tamam Y, Hosoglu S, Ayaz C, Geyik MF, Apak I (2006) Multiresistant bacterial colonization due to increased nurse workload in a neurology intensive care unit. Neurosciences (Riyadh) 11(4):265–270

    Google Scholar 

  23. Vincent JL, Sakr Y, Sprung CL, Ranieri VM, Reinhart K, Gerlach H, Moreno R, Carlet J, Le Gall JR, Payen D; Sepsis Occurrence in Acutely Ill Patients Investigators (2006) Sepsis in European intensive care units: results of the SOAP study. Crit Care Med 34(2):344–353

    Article  PubMed  Google Scholar 

  24. Gasink LB, Edelstein PH, Lautenbach E, Synnestvedt M, Fishman NO (2009) Risk factors and clinical impact of Klebsiella pneumoniae carbapenemase-producing K. pneumoniae. Infect Control Hosp Epidemiol 30(12):1180–1185

    Article  PubMed Central  PubMed  Google Scholar 

  25. Papadimitriou-Olivgeris M, Giormezis N, Fligou F, Liakopoulos A, Marangos M, Anastassiou ED, Petinaki E, Filos KS, Spiliopoulou I (2013) Factors influencing linezolid-nonsusceptible coagulase-negative staphylococci dissemination among patients in the intensive care unit: a retrospective cohort study. Chemotherapy 59(6):420–426

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Mrs. Antigoni Foka, Bsc, PhD, Mrs. Eleanna Drougka, Bsc, and Mrs. Christina Bartzavali, Bsc, PhD, Department of Microbiology, School of Medicine, University of Patras, for their technical assistance.

Funding

This study was supported by funds from the Department of Microbiology, School of Medicine, University of Patras.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was carried out under the “Hospital Surveillance Programme for multi-drug resistant bacterial colonization of patients at risk and HCWs”, and was approved by the University Hospital Ethics Committee, which waived the need for informed consent (HEC no.: 571).

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Correspondence to E. D. Anastassiou.

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Papadimitriou-Olivgeris, M., Spiliopoulou, I., Christofidou, M. et al. Co-colonization by multidrug-resistant bacteria in two Greek intensive care units. Eur J Clin Microbiol Infect Dis 34, 1947–1955 (2015). https://doi.org/10.1007/s10096-015-2436-4

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  • DOI: https://doi.org/10.1007/s10096-015-2436-4

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