Identification of vancomycin-resistant enterococci clones and inter-hospital spread during an outbreak in Taiwan

Lee et al. BMC Infectious Diseases 2013, 13:163 http://www.biomedcentral.com/1471-2334/13/163 RESEARCH ARTICLE Open Access Identification of vancomycin-resistant enterococci clones and inter-hospital spread during an outbreak in Taiwan Sai-Cheong Lee1*, Mi-Si Wu2, Hsiang-Ju Shih1, Shu-Huan Huang3, Meng-Jiun Chiou4, Lai-Chu See4,5 and Liang-Kee Siu6 Abstract Background: In 2003, nosocomial infections caused by vancomycin-resistant enterococci (VRE) occurred rarely in Taiwan. Between 2003 and 2010, however, the average prevalence of vancomycin resistance among enterococci spp. increased from 2% to 16% in community hospitals and from 3% to 21% in medical centers of Taiwan. We used molecular methods to investigate the epidemiology of VRE in a tertiary teaching hospital in Taiwan. Methods: Between February 2009 and February 2011, rectal samples and infection site specimens were collected from all inpatients in the nephrology ward after patient consent was obtained. VRE strain types were determined by pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). Results: A total of 59 vanA gene-containing VRE isolates (1 per patient) were obtained; 24 originated from rectal sample surveillance of patients who exhibited no symptoms (22 Enterococcus faecium and 2 Enterococcus faecalis), and 35 had developed infections over 3 days after admission (32 E. faecium, 2 E. faecalis, and 1 Enterococcus durans). The 59 VRE isolates demonstrated vancomycin minimum inhibitory concentrations (MICs) of ≥256 μg/m. The MIC range for linezolid, tigecycline, and daptomycin was 0.25–1.5 μg/mL, 0.032–0.25 and 1–4 μg/mL, respectively. For 56 isolates, the MIC for teicoplanin was >8 μg/mL. The predominant types in the nephrology ward were MLST types 414, 78, and18 as well as PFGE types A, C, and D. Conclusion: VREs are endemic in nephrology wards. MLST 414 is the most predominant strain. The increase VRE prevalence is due to cross-transmission of VRE clones ST 414,78,18 by undetected VRE carriers. Because similar VRE STs had been reported in a different hospital of Taiwan, this finding may indicate inter-hospital VRE spread in Taiwan. Active surveillance and effective infection control policies are important controlling the spread of VRE in high risk hospital zones. All endemic VRE strains are resistant to teicoplanin but are sensitive to daptomycin, linezolid, and tigecycline. Keywords: VRE, MLST, Outbreak, Inter-hospital spread Background For most immunocompetent patients, colonization with vancomycin-resistant enterococci (VRE) does not present a significant personal health risk; however, these patients may function as carriers, and following hospital admission, may pose a substantial risk for transmission [1-4]. In 2003, nosocomial infections caused by VRE occurred rarely in * Correspondence: 1 Division of Infectious Diseases, Chang Gung Memorial Hospital, Keelung, Chang Gung University, 222, Mai Chin Road, Kwei-Shan, Tao-Yuan, Taiwan Full list of author information is available at the end of the article Taiwan [5]. Between 2003 and 2010, however, the prevalence of vancomycin resistance among enterococci spp. in community-hospitals and medical centers has increased from 2% to 16% and from 3% to 21%, respectively [5]. Little is known about the epidemiology of VRE, and most information has derived from the descriptions of monoclonal outbreaks [6-11]. The reasons underlying the rapid emergence of VRE had not been investigated in Taiwan thus far. Taiwan’s current management guidelines for VRE colonization and infection mimic those of the United States, which involve reasonably strict isolation measures © 2013 Lee et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Lee et al. BMC Infectious Diseases 2013, 13:163 http://www.biomedcentral.com/1471-2334/13/163 [3,6]. The complete enforcement of these policies for VRE-colonized patients is difficult and impractical; the isolation rooms in most teaching hospitals are inadequate and high in cost [7]. Thus, we used multi-locus sequence typing (MLST) and pulsed-field gel electrophoresis (PFGE) to assess the epidemiology of VRE in a hospital setting, investigate the need for these policies, and discover new VRE clones. We also investigated the in-vitro susceptibilities of VRE to current antimicrobial agents. Page 2 of 6 The colonies were identified as those of Enterococcus spp. based on known enterococcus characteristics, including the presence of gram-positive cocci, optochin resistance, bile-esculin color change to black, and growth in 6.5% sodium chloride (NaCl) [1,2]. Specific enterococcus spp. were identified by differential utilization of arginine, sorbitol, arabinose, and raffinose and by the rapid 32 Strep kit test (bioMerieux Vitek Inc., Hazelwood, Missouri, USA) [1,2]. VRE presence was confirmed by growth in brain heart infusion agar that contained 6 μg/mL vancomycin [13,14]. Methods Setting and study design Pulsed-field gel electrophoresis Chang Gung Memorial Hospital at Keelung in Taiwan is a 1088-bed, tertiary-care, teaching hospital. The prevalence of vancomycin resistance among enterococci spp. in this hospital rose from 10% in 2003 to 30% in 2009, and it was most pronounced in the nephrology ward. A VRE outbreak was suspected in the nephrology ward because the prevalence rate, 30%, was higher than the average rate,16%, in Taiwan [5]. This research plan was approved by the Human Trial and Ethics Committee of Chang Gung Memorial Hospital on December 24, 2008 (reference number 97-2117B). Between February 2010 and February 2011, a VRE surveillance study was conducted on both hemodialysis and non-hemodialysis inpatients in the nephrology ward of this hospital. Rectal swab cultures for VRE were collected from all nephrology inpatients during admission after patient consent was obtained. Colonization was defined as VRE isolation from rectal swabs in the absence of infection symptoms or signs. Infection was defined as VRE isolation from a sterile or non-sterile site along with the presentation of fever, leukocytosis, and other signs caused by the VRE. All VRE-infected patients were confined to a single room or a double room with two beds for 2 VRE-infected patients of the same sex. All health-care workers (HCW) who administered care on VRE-infected patients were asked to follow infection control policies during patient care, including hand washing and glove and gown wearing when necessary [12]. During this study period, active surveillance was performed on inpatients of the nephrology ward after patient consent was obtained. Further, within this study period, potential VRE specimens were collected both from HCWs after they provided consent and from the nephrology (...truncated)