Withdrawal of Staphylococcus aureus from intensive care units in Turkey


      In the past, Staphylococcus aureus infections have displayed various patterns of epidemiologic curves in hospitals, particularly in intensive care units (ICUs). This study aimed to characterize the current trend in a nationwide survey of ICUs in Turkey.


      A total of 88 ICUs from 36 Turkish tertiary hospitals were included in this retrospective study, which was performed during the first 3 months of both 2008 (period [P] 1) and 2011 (P2). A P value ≤.01 was considered significant.


      Although overall rates of hospital-acquired infection (HAI) and device-associated infection densities were similar in P1 and P2, the densities of HAIs due to S aureus and methicillin-resistant S aureus (MRSA) were significantly lower in P2 (P < .0001). However, the proportion of HAIs due to Acinetobacter was significantly higher in P2 (P < .0001).


      The incidence of S aureus infections is declining rapidly in Turkish ICUs, with potential impacts on empirical treatment strategies in these ICUs.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to American Journal of Infection Control
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Grundmann H.
        • Aires-de-Sousa M.
        • Boyce J.
        • Tiemersma E.
        Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat.
        Lancet. 2006; 368: 874-885
        • Johnson A.P.
        Methicillin-resistant Staphylococcus aureus: the European landscape.
        J Antimicrob Chemother. 2011; 66: iv43-iv48
        • Johnson A.P.
        • Pearson A.
        • Duckworth G.
        Surveillance and epidemiology of MRSA bacteraemia in the UK.
        J Antimicrob Chemother. 2005; 56: 455-462
        • Panlilio A.L.
        • Culver D.H.
        • Gaynes R.P.
        • Banerjee S.
        • Henderson T.S.
        • Tolson J.S.
        • et al.
        Methicillin-resistant Staphylococcus aureus in US hospitals, 1975-1991.
        Infect Control Hosp Epidemiol. 1992; 13: 582-586
        • Que Y.
        • Moreillon P.
        Staphylococcus aureus (including staphylococcal toxic shock).
        in: Mandell G.L. Bennett J.E. Dolin R. Mandell, Douglas, and Bennett's principles and practice of infectious diseases. Churchill Livingstone, Philadelphia2010: 2543-2579
        • Stefani S.
        • Chung D.R.
        • Lindsay J.A.
        • Friedrich A.W.
        • Kearns A.M.
        • Westh H.
        • et al.
        Meticillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonisation of typing methods.
        Int J Antimicrob Agents. 2012; 39: 273-282
        • van Duijn P.J.
        • Dautzenberg M.J.
        • Oostdijk E.A.
        Recent trends in antibiotic resistance in European ICUs.
        Curr Opin Crit Care. 2011; 17: 658-665
        • Jarlier V.
        • Trystram D.
        • Brun-Buisson C.
        • Fournier S.
        • Carbonne A.
        • Marty L.
        • et al.
        Curbing methicillin-resistant Staphylococcus aureus in 38 French hospitals through a 15-year institutional control program.
        Arch Intern Med. 2010; 170: 552-559
        • Edgeworth J.D.
        Has decolonization played a central role in the decline in UK methicillin-resistant Staphylococcus aureus transmission? A focus on evidence from intensive care.
        J Antimicrob Chemother. 2011; 66: ii41-ii47
        • van Cleef B.A.
        • Kluytmans J.A.
        • van Benthem B.H.
        • Haenen A.
        • Monen J.
        • Daniels-Haardt I.
        • et al.
        Cross-border comparison of MRSA bacteraemia between The Netherlands and North Rhine-Westphalia (Germany): a cross-sectional study.
        PLoS ONE. 2012; 7: e42787
        • Garner J.S.
        • Jarvis W.R.
        • Emori T.G.
        • Horan T.C.
        • Hughes J.M.
        CDC definitions for nosocomial infections, 1988.
        Am J Infect Control. 1988; 16: 128-140
        • Rosenthal V.D.
        • Maki D.G.
        • Jamulitrat S.
        • Medeiros E.A.
        • Todi S.K.
        • Gomez D.Y.
        • et al.
        International Nosocomial Infection Control Consortium (INICC) report, data summary for 2003-2008, issued June 2009.
        Am J Infect Control. 2010; 38: 95-104
        • Dudeck M.A.
        • Horan T.C.
        • Peterson K.D.
        • Allen-Bridson K.
        • Morrell G.
        • Pollock D.A.
        • et al.
        National Healthcare Safety Network (NHSN) Report, data summary for 2010, device-associated module.
        Am J Infect Control. 2011; 39: 798-816
        • Stefani S.
        • Varaldo P.E.
        Epidemiology of methicillin-resistant staphylococci in Europe.
        Clin Microbiol Infect. 2003; 9: 1179-1186
        • Gagliotti C.
        • Balode A.
        • Baquero F.
        • Degener J.
        • Grundmann H.
        • Gur D.
        • et al.
        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. 2011; 16 (pii: 19819)
        • de Kraker M.E.
        • Davey P.G.
        • Grundmann H.
        Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe.
        PLoS Med. 2011; 8: e1001104
        • Livermore D.M.
        Fourteen years in resistance.
        Int J Antimicrob Agents. 2012; 39: 283-294
        • Inan A.
        • Ozgultekin A.
        • Akcay S.S.
        • Engin D.O.
        • Turan G.
        • Ceran N.
        • et al.
        Alterations in bacterial spectrum and increasing resistance rates in isolated microorganisms from device-associated infections in an intensive care unit of a teaching hospital in Istanbul (2004-2010).
        Jpn J Infect Dis. 2012; 65: 146-151
        • Rosenthal V.D.
        • Rodrigues C.
        • Alvarez-Moreno C.
        • Madani N.
        • Mitrev Z.
        • Ye G.
        • et al.
        Effectiveness of a multidimensional approach for prevention of ventilator-associated pneumonia in adult intensive care units from 14 developing countries of four continents: findings of the International Nosocomial Infection Control Consortium.
        Crit Care Med. 2012; 40: 3121-3128
        • Hu B.
        • Tao L.
        • Rosenthal V.D.
        • Liu K.
        • Yun Y.
        • Suo Y.
        • et al.
        Device-associated infection rates, device use, length of stay, and mortality in intensive care units of 4 Chinese hospitals: International Nosocomial Control Consortium findings.
        Am J Infect Control. 2013; 41: 301-306
        • Cesur S.
        • Irmak H.
        • Simsek H.
        • Coplu N.
        • Kilic H.
        • Arslan U.
        • et al.
        Evaluation of antibiotic susceptibilities and VISA-VRSA rates among MRSA strains isolated from hospitalized patients in intensive care units of hospitals in seven provinces of Turkey.
        Mikrobiyol Bul. 2012; 46: 352-358
        • Viviani M.
        • Van Saene H.K.
        • Pisa F.
        • Lucangelo U.
        • Silvestri L.
        • Momesso E.
        • et al.
        The role of admission surveillance cultures in patients requiring prolonged mechanical ventilation in the intensive care unit.
        Anaesth Intensive Care. 2010; 38: 325-335
        • Nseir S.
        • Grailles G.
        • Soury-Lavergne A.
        • Minacori F.
        • Alves I.
        • Durocher A.
        Accuracy of American Thoracic Society/Infectious Diseases Society of America criteria in predicting infection or colonization with multidrug-resistant bacteria at intensive-care unit admission.
        Clin Microbiol Infect. 2010; 16: 902-908
        • Tacconelli E.
        • De Angelis G.
        • Cataldo M.A.
        • Pozzi E.
        • Cauda R.
        Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? A systematic review and meta-analysis.
        J Antimicrob Chemother. 2008; 61: 26-38
        • Erdem H.
        • Kurtaran B.
        • Arun O.
        • Yilmaz H.
        • Celebi| G.
        • Ozkaya H.D.
        • et al.
        The place and the efficacy of infectious disease consultations in hospitals.
        Infect Dis Clin Pract. 2012; 20: 131-136
        • Inan A.
        • Dagli O.
        • Şenbayrak-Akçay S.
        • Öztürk-Engin D.
        • Karagül E.
        • Çelik-Özyürek S.
        Antibiotic use and cost in a teaching hospital in Istanbul.
        J Microbiol Infect Dis. 2011; 1: 128-133
        • Erdem H.
        • Akova M.
        Leading infectious diseases problems in Turkey.
        Clin Microbiol Infect. 2012; 18: 1056-1067
        • Rello J.
        • Molano D.
        • Villabon M.
        • Reina R.
        • Rita-Quispe R.
        • Previgliano I.
        • et al.
        Differences in hospital- and ventilator-associated pneumonia due to Staphylococcus aureus (methicillin-susceptible and methicillin-resistant) between Europe and Latin America: a comparison of the EUVAP and LATINVAP study cohorts.
        Med Intens. 2012 Jun 27; ([Epub ahead of print.])
        • Souli M.
        • Galani I.
        • Giamarellou H.
        Emergence of extensively drug-resistant and pandrug-resistant Gram-negative bacilli in Europe.
        Euro Surveill. 2008; 13 (pii: 19045)
        • Chen Y.Y.
        • Chen L.Y.
        • Lin S.Y.
        • Chou P.
        • Liao S.Y.
        • Wang F.D.
        Surveillance on secular trends of incidence and mortality for device-associated infection in the intensive care unit setting at a tertiary medical center in Taiwan, 2000-2008: a retrospective observational study.
        BMC Infect Dis. 2012; 12: 209
        • Miyakis S.
        • Pefanis A.
        • Tsakris A.
        The challenges of antimicrobial drug resistance in Greece.
        Clin Infect Dis. 2011; 53: 177-184
        • Allen D.M.
        • Hartman B.J.
        Acinetobacter species.
        in: Mandell G.L. Bennett J.E. Dolin R. Mandell, Douglas, and Bennett's principles and practice of infectious diseases. Churchill Livingstone, Philadelphia2010: 2881-2887
        • Doughari H.J.
        • Ndakidemi P.A.
        • Human I.S.
        • Benade S.
        The ecology, biology and pathogenesis of Acinetobacter spp: an overview.
        Microbes Environ. 2011; 26: 101-112
        • Cohen A.L.
        • Calfee D.
        • Fridkin S.K.
        • Huang S.S.
        • Jernigan J.A.
        • Lautenbach E.
        • et al.
        Recommendations for metrics for multidrug-resistant organisms in healthcare settings: SHEA/HICPAC position paper.
        Infect Control Hosp Epidemiol. 2008; 29: 901-913
        • Apisarnthanarak A.
        • Khawcharoenporn T.
        • Mundy L.M.
        Practices to prevent multidrug-resistant Acinetobacter baumannii and methicillin-resistant Staphylococcus aureus in Thailand: a national survey.
        Am J Infect Control. 2013; 41: 416-421