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Highly Resistant Gram-Negative Microorganisms Incidence Density and Occurrence of Nosocomial Transmission (TRIANGLe Study)

  • I. Willemsen (a1), S. Elberts (a1), C. Verhulst (a1), M. Rijnsburger (a2), M. Filius (a3), P. Savelkoul (a2), J. Kluytmans (a1) (a2), TRIANGLe Study Group, E. Lommerse (a4), L. Spanjaard (a4), B. Vlaminckx (a5), A. Vos (a6), M. Wulf (a7), M. Vos (a8), R. Wintermans (a9), G. Andriesse (a10), J. van Zeijl (a11), E. van der Vorm (a12), A. Buiting (a13), P. Sturm (a14), H. Blok (a15), A. Troelstra (a15), A. Kaiser (a2) and C. Vandenbroucke-Grauls (a2)...



The objectives of this study were to determine the incidence density and the occurrence of horizontal spread of highly resistant gram-negative rods (HR-GNRs) in Dutch hospitals. The factors that influence these outcome measures were also investigated.


All patients with HR-GNRs, as determined by sample testing, who were hospitalized in 1 of 18 hospitals during a 6-month period (April through October 2007) were included in this study. For all available isolates, the species was identified, susceptibility was determined (including the presence of extended-spectrum β-lactamases [ESBLs]), and molecular typing was performed. On the basis of a combination of species identification, molecular typing, and epidemiological data, the occurrence of nosocomial transmission was determined.


The mean incidence density of patients with HR-GNRs was 55 per 100,000 patient-days (cumulative incidence, 39 per 10,000 patients admitted). A facility being a university hospital was a statistically significant (P = .03) independent determinant of a higher incidence of patients with HR-GNRs. The majority of HR-GNR isolates were ESBL producers. The adjusted transmission index—the ratio between secondary and primary cases—in the participating hospitals ranged from 0.0 to 0.2. The overall adjusted transmission index of HR-GNRs was 0.07. No determinants for a higher transmission index were identified.


The nosocomial transmission rate of HR-GNRs was relatively low in all hospitals where well-established transmission-based precautions were used. The incidence density of patients with HR-GNRs was higher in university hospitals, probably due to the patient population and the complexity of the care provided.


Corresponding author

Consultant Infection Control, Department of Medical Microbiology and Infection Control, Amphia Hospital, PO Box 90158, 4800 RK Breda, the Netherlands ( or


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