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Acquisition and Cross-Transmission of Staphylococcus aureus in European Intensive Care Units

Published online by Cambridge University Press:  02 January 2015

Alexander L. A. Bloemendaal*
Affiliation:
Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, the Netherlands Department of Surgery, University Medical Center Utrecht, Utrecht, the Netherlands
Ad C. Fluit
Affiliation:
Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, the Netherlands
Wouter M. T. Jansen
Affiliation:
Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, the Netherlands
Menno R. Vriens
Affiliation:
Department of Surgery, University Medical Center Utrecht, Utrecht, the Netherlands
Tristan Ferry
Affiliation:
Université Lyon 1, Centre National de Référence des Staphylocoques, Faculté Laennec, Lyon, France
Laurent Argaud
Affiliation:
Service de Réanimation Médicale Pôle d'Activité d'Urgences et de Réanimation Médicales Groupement Hospitalier Edouard Herriot Hospices Civils de Lyon, Lyon, France
Jose M. Amorim
Affiliation:
Department of Microbiology, Hospital Geral de Santo Antonio, Porto, Portugal
A. C. Resende
Affiliation:
Service de Réanimation Médicale Pôle d'Activité d'Urgences et de Réanimation Médicales Groupement Hospitalier Edouard Herriot Hospices Civils de Lyon, Lyon, France
Alvaro Pascual
Affiliation:
Department of Microbiology, Hospital Virgen Macarena, Seville, Spain
Lorena López-Cerero
Affiliation:
Department of Microbiology, Hospital Virgen Macarena, Seville, Spain
Stefania Stefani
Affiliation:
Department of Microbiology, Catania, Italy
Giacomo Castiglione
Affiliation:
Intensive Care Unit Ward, Vittorio Emanuele Hospital, Catania, Italy
Penelope Evangelopoulou
Affiliation:
Athens University School of Nursing, Intensive Care Unit, Athens, Greece
Sophia Tsiplakou
Affiliation:
Microbiology and Immunology Department, KAT Hospital, Athens, Greece
Inne H. M. Borel Rinkes
Affiliation:
Department of Surgery, University Medical Center Utrecht, Utrecht, the Netherlands
Jan Verhoef
Affiliation:
Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, the Netherlands
*
Department of Surgery, Room G04.228, University Medical Center Utrecht, Heidelberglaan 100, P.O. Box 85500, 3508 GA Utrecht, The Netherlands ([email protected])

Abstract

Objective.

To study the acquisition and cross-transmission of Staphylococcus aureus in different intensive care units (ICUs).

Methods.

We performed a multicenter cohort study. Six ICUs in 6 countries participated. During a 3-month period at each ICU, all patients had nasal and perineal swab specimens obtained at ICU admission and during their stay. All S. aureus isolates that were collected were genotyped by spa typing and multilocus variable-number tandem-repeat analysis typing for cross-transmission analysis. A total of 629 patients were admitted to ICUs, and 224 of these patients were found to be colonized with S. aureus at least once during ICU stay (22% were found to be colonized with methicillin-resistant S. aureus [MRSA]). A total of 316 patients who had test results negative for S. aureus at ICU admission and had at least 1 follow-up swab sample obtained for culture were eligible for acquisition analysis.

Results.

A total of 45 patients acquired S. aureus during ICU stay (31 acquired methicillin-susceptible S. aureus [MSSA], and 14 acquired MRSA). Several factors that were believed to affect the rate of acquisition of S. aureus were analyzed in univariate and multivariate analyses, including the amount of hand disinfectant used, colonization pressure, number of beds per nurse, antibiotic use, length of stay, and ICU setting (private room versus open ICU treatment). Greater colonization pressure and a greater number of beds per nurse correlated with a higher rate of acquisition for both MSSA and MRSA. The type of ICU setting was related to MRSA acquisition only, and the amount of hand disinfectant used was related to MSSA acquisition only. In 18 (40%) of the cases of S. aureus acquisition, cross-transmission from another patient was possible.

Conclusions.

Colonization pressure, the number of beds per nurse, and the treatment of all patients in private rooms correlated with the number of S. aureus acquisitions on an ICU. The amount of hand disinfectant used was correlated with the number of cases of MSSA acquisition but not with the number of cases of MRSA acquisition. The number of cases of patient-to-patient cross-transmission was comparable for MSSA and MRSA.

Type
Original Articles
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2009

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References

1.Alberti, C, Brun-Buisson, C, Burchardi, H, et al.Epidemiology of sepsis and infection in ICU patients from an international multicentre cohort study. Intensive Care Med 2002;28:108121.CrossRefGoogle ScholarPubMed
2.Ibelings, MM, Bruining, HA. Methicillin-resistant Staphylococcus aureus: acquisition and risk of death in patients in the intensive care unit. Eur J Surg 1998;164:411418.CrossRefGoogle ScholarPubMed
3.Vincent, JL, Bihari, DJ, Suter, PM, et al. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) study. EPIC International Advisory Committee. JAMA 1995;274:639644.Google Scholar
4.Jevons, MP, Coe, AW, Parker, MT. Methicillin resistance in staphylococci. Lancet 1963;1:904907.Google Scholar
5.Benner, EJ, Kayser, FH. Growing clinical significance of methcillin-resis-tant Staphylococcus aureus. Lancet 1968;2:741744.CrossRefGoogle ScholarPubMed
6.European Antimicrobial Resistance Surveillance System (EARSS) Management Team. EARSS annual report 2006. Biltoven, The Netherlands: EARSS, 2007.Google Scholar
7.Wertheim, HF, Voss, MC, Ott, A, et al.Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 2004;364:703705.Google Scholar
8.Merrer, J, Santol i, F, Appéré de, Vecchi C, Tran, B, De Jonghe, B, Outin, H. Colonization pressure and risk of acquisition of methicillin-resistant Staphylococcus aureus in a medical intensive care unit. Infect Control Hosp Epidemiol 2000;21:718723.Google Scholar
9.Graffunder, EM, Venezia, RA. Risk factors associated with nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection including previous use of antimicrobials. J Antimicrob Chemother 2002;49:9991005.CrossRefGoogle ScholarPubMed
10.Marshall, C, Wolfe, R, Kossman, T, Wesselingh, S, Harrington, G, Spelman, D. Risk factors for acquisition of methicillin-resistant Staphylococcus aureus (MRSA) by trauma patients in the intensive care unit. J Hosp Infect 2004;57:245252.Google Scholar
11.Muller, AA, Mauny, F, Bertin, M, et al.Relationship between spread of methicillin-resistant Staphylococcus aureus and antimicrobial use in a French university hospital. Clin Infect Dis 2003;36:971978.Google Scholar
12.Washio, M. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) infection in a Japanese elderly care nursing home. Epidemiol Infect 1997;119:285.CrossRefGoogle Scholar
13.Washio, M, Mizoue, T, Yoshimitsu, T, et al.Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) infection in a Japanese geriatric hospital. Public Health 1997;111:187190.CrossRefGoogle Scholar
14.Barrett, SP, Mummery, RV, Chattopadhyay, B. Trying to control MRSA causes more problems than it solves. J Hosp Infect 1998;39:8593.Google Scholar
15.Cepeda, JA, Whitehouse, T, Cooper, B, et al.Isolation of patients in single rooms or cohorts to reduce spread of MRSA in intensive-care units: prospective two-centre study. Lancet 2005;365:295304.Google Scholar
16.Cooper, BS, Stone, SP, Kibbler, CC, et al.Isolation measures in the hospital management of methicillin resistant Staphylococcus aureus (MRSA): systematic review of the literature. BMJ 2004;329:533541.CrossRefGoogle ScholarPubMed
17.Eckmanns, T, Schwab, F, Bessert, J, et al.Hand rub consumption and hand hygiene compliance are not indicators of pathogen transmission in intensive care units. J Hosp Infect 2006;63:406411.CrossRefGoogle Scholar
18.Lucet, JC, Paoletti, X, Lolom, I, et al.Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med 2005;31:10511057.CrossRefGoogle ScholarPubMed
19.Blok, HE, Troelstra, A, Kamp-Hopmans, TE, et al.Role of healthcare workers in outbreaks of methicillin-resistant Staphylococcus aureus: a 10-year evaluation from a Dutch university hospital. Infect Control Hosp Epidemiol 2003;24:679685.Google Scholar
20.Hardy, KJ, Oppenheim, BA, Gossain, S, Gao, F, Hawkey, PM. A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA. Infect Control Hosp Epidemiol 2006;27:127132.CrossRefGoogle ScholarPubMed
21.Oztoprak, N, Cevik, MA, Akinci, E, et al.Risk factors for ICU-acquired methicillin-resistant Staphylococcus aureus infections. Am J Infect Control 2006;34:15.CrossRefGoogle ScholarPubMed
22.Shiomori, T, Miyamoto, H, Makishima, K, et al.Evaluation of bedmaking-related airborne and surface methicillin-resistant Staphylococcus aureus contamination. J Hosp Infect 2002;50:3035.Google Scholar
23.Talon, D, Rouget, C, Cailleaux, V, et al.Nasal carriage of Staphylococcus aureus and cross-contamination in a surgical intensive care unit: efficacy of mupirocin ointment. J Hosp Infect 1995;30:3949.CrossRefGoogle Scholar
24.Weist, K, Pollege, K, Schulz, I, et al.How many nosocomial infections are associated with cross-transmission?: a prospective cohort study in a surgical intensive care unit. Infect Control Hosp Epidemiol 2002;23:127132.CrossRefGoogle Scholar
25.Wilson, RD, Huang, SJ, McLean, AS. The correlation between airborne methicillin-resistant Staphylococcus aureus with the presence of MRSA colonized patients in a general intensive care unit. Anaesth Intensive Care 2004;32:202209.CrossRefGoogle Scholar
26.Blatnik, J, Lesnicar, G. Propagation of methicillin-resistant Staphylococcus aureus due to the overloading of medical nurses in intensive care units. J Hosp Infect 2006;63:162166.CrossRefGoogle Scholar
27.Dancer, SJ, Coyne, M, Speekenbrink, A, Samavedam, S, Kennedy, J, Wallace, PG. MRSA acquisition in an intensive care unit. Am J Infect Control 2006;34:1017.CrossRefGoogle Scholar
28.Onorato, M, Borucki, MJ, Baillargeon, G, et al.Risk factors for colonization or infection due to methicillin-resistant Staphylococcus aureus in HIV-positive patients: a retrospective case-control study. Infect Control Hosp Epidemiol 1999;20:2630.CrossRefGoogle ScholarPubMed
29.Grundmann, H, Hori, S, Winter, B, Tami, A, Austin, DI. Risk factors for the transmission of methicillin-resistant Staphylococcus aureus in an adult intensive care unit: fitting a model to the data. J Infect Dis 2002;185:481488.CrossRefGoogle Scholar
30.Grundmann, H, Bärwolff, S, Tami, A, et al.How many infections are caused by patient-to-patient transmission in intensive care units? Crit Care Med 2005;33:946951.CrossRefGoogle ScholarPubMed
31.Nijssen, S, Bonten, MJ, Weinstein, RA. Are active microbiological surveillance and subsequent isolation needed to prevent the spread of methicillin-resistant Staphylococcus aureus? Clin Infect Dis 2005;40:405409.Google Scholar
32.Vriens, MR, Fluit, AC, Troelstra, A, Verhoef, J, van der Werken, C. Is methicillin-resistant Staphylococcus aureus more contagious than meth-icillin-susceptible S. aureus in a surgical intensive care unit? Infect Control Hosp Epidemiol 2002;23:491494.CrossRefGoogle Scholar
33.Koreen, L, Ramaswamy, SV, Graviss, EA, Naidich, S, Musser, JM, Kreiswirth, BN. Spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro-and macrovariation. J Clin Microbiol 2004;42:792799.Google Scholar
34.Lindstedt, BA. Multiple-locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria. Electrophoresis 2005;26:25672582.Google Scholar
35.Malachowa, N, Sabat, A, Gniadkowski, M, et al.Comparison of multiple-locus variable-number tandem-repeat analysis with pulsed-field gel electrophoresis, spa typing, and multilocus sequence typing for clonal characterization of Staphylococcus aureus isolates. J Clin Microbiol 2005;43:30953100.Google Scholar
36.van Belkum, A. Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). FEMS Immunol Med Microbiol 2007;49:2227.Google Scholar
37.Maes, N, Magdalena, J, Rottiers, S, De Gheldre, Y, Straelens, MJ. Evaluation of a triplex PCR assay to discriminate Staphylococcus aureus from co-agulase-negative staphylococci and determine methicillin resistance from blood cultures. J Clin Microbiol 2002;40:15141517.CrossRefGoogle Scholar
38.Hardy, KJ, Ussery, DW, Oppenheim, BA, Hawkey, PM. Distribution and characterization of staphylococcal interspersed repeat units (SIRUs) and potential use for strain differentiation. Microbiology 2004;150:40454052.Google Scholar
39.Sabat, A, Krzyszton-Russjan, J, Strzalka, W, et al.New method for typing Staphylococcus aureus strains: multiple-locus variable-number tandem repeat analysis of polymorphism and genetic relationships of clinical isolates. J Clin Microbiol 2003;41:18011804.Google Scholar
40.Ikawaty, R, Willems, RJ, Box, AT, Verhoef, J, Fluit, AC. A novel multiple-locus variable-number tandem repeat (VNTR) analysis (MLVA) for rapid molecular typing of human Staphylococcus aureus. J Clin.Microbiol 2008;46:314751.Google Scholar
41.Ridom SpaServer database. Available at: http://www.SpaServer.ridom.de. Accessed December 2, 2008.Google Scholar
42.Huskins, WC. Interventions to prevent transmission of antimicrobial-resistant bacteria in the intensive care unit. Curr Opin Crit Care 2007;13:572577.Google Scholar
43.Eckmanns, T, Bessert, J, Behnke, M, Gastmeier, P, Ruden, H. Compliance with antiseptic hand rub use in intensive care units: the Hawthorne effect. Infect Control Hosp Epidemiol 2006;27:931934.CrossRefGoogle ScholarPubMed
44.Bracco, D, Dubois, MJ, Bouali, R, Eggimann, P. Single rooms may help to prevent nosocomial bloodstream infection and cross-transmission of methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med 2007;33:836840.Google Scholar
45.Coello, R, Jiménez, J, Garcia, M, et al.Prospective study of infection, colonization and carriage of methicillin-resistant Staphylococcus aureus in an outbreak affecting 990 patients. Eur J Clin Microbiol Infect Dis 1994;13:7481.CrossRefGoogle Scholar
46.Cosseron-Zerbib, M, Roque Afonso, AM, Naas, T, et al.A control programme for MRSA (methicillin-resistant Staphylococcus aureus) containment in a paediatric intensive care unit: evaluation and impact on infections caused by other micro-organisms. J Hosp Infect 1998;40:225235.CrossRefGoogle Scholar
47.Gastmeier, P, Kampf, G, Wischnewski, N, et al.Prevalence of nosocomial infections in representative German hospitals. J Hosp Infect 1998;38:3749.Google Scholar
48.Harbarth, S, Martin, Y, Rohner, P, Henry, N, Auckenthaler, R, Pittet, D. Effect of delayed infection control measures on a hospital outbreak of methicillin-resistant Staphylococcus aureus. J Hosp Infect 2000;46:4349.Google Scholar
49.Amorim, ML, Faria, NA, Oliveira, DC, et al.Changes in the clonal nature and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus isolates associated with spread of the EMRSA-15 clone in a tertiary care Portuguese hospital. J Clin Microbiol 2007;45:28812888.CrossRefGoogle Scholar
50.Marshall, C, Harrington, G, Wolfe, R, Fairley, CK, Wesselingh, S, Spelman, D. Acquisition of methicillin-resistant Staphylococcus aureus in a large intensive care unit. Infect Control Hosp Epidemiol 2003;24:322326.Google Scholar