Skip to main content Accessibility help
×
Home

Defining the Role of the Environment in the Emergence and Persistence of vanA Vancomycin-Resistant Enterococcus (VRE) in an Intensive Care Unit: A Molecular Epidemiological Study

  • Andie S. Lee (a1) (a2), Elizabeth White (a3), Leigh G. Monahan (a4), Slade O. Jensen (a5) (a6), Raymond Chan (a1) (a2) and Sebastiaan J. van Hal (a1) (a5) (a6)...

Abstract

OBJECTIVE

To describe the transmission dynamics of the emergence and persistence of vanA vancomycin-resistant enterococcus (VRE) in an intensive care unit (ICU) using whole-genome sequencing of patient and environmental isolates.

DESIGN

Retrospective cohort study.

SETTING

ICU in a tertiary referral center.

PARTICIPANTS

Patients admitted to the ICU over an 11-month period.

METHODS

VanA VRE isolated from patients (n=31) were sequenced using the Illumina MiSeq platform. Environmental samples from bed spaces, equipment, and waste rooms were collected. All vanA VRE-positive environmental samples (n=14) were also sequenced. Data were collected regarding patient ward and bed movements.

RESULTS

The 31 patient vanA VRE isolates were from screening (n=19), urine (n=4), bloodstream (n=3), skin/wound (n=3), and intra-abdominal (n=2) sources. The phylogeny from sequencing data confirmed several VRE clusters, with 1 group accounting for 38 of 45 isolates (84%). Within this cluster, cross-transmission was extensive and complex across the ICU. Directionality indicated that colonized patients contaminated environmental sites. Similarly, environmental sources not only led to patient colonization but also to infection. Notably, shared equipment acted as a conduit for transmission between different ICU areas. Infected patients, however, were not linked to further VRE transmission.

CONCLUSIONS

Genomic sequencing confirmed a predominantly clonal outbreak of VRE with complex transmission dynamics. The environmental reservoir, particularly from shared equipment, played a key role in ongoing VRE spread. This study provides evidence to support the use of multifaceted strategies, with an emphasis on measures to reduce bacterial burden in the environment, for successful VRE control.

Infect Control Hosp Epidemiol 2018;39:668–675

Copyright

Corresponding author

Address correspondence to Andie S. Lee, Department of Microbiology, Royal Prince Alfred Hospital, Missenden Road, Camperdown NSW 2050, Sydney, NSW, Australia (andie.lee@health.nsw.gov.au).

Footnotes

Hide All

PREVIOUS PRESENTATION. Data in this manuscript were presented in abstract form at the Australian Society of Antimicrobials (ASA) Conference on February 24, 2017, in Melbourne, Australia.

Footnotes

References

Hide All
1. Wisplinghoff, H, Bischoff, T, Tallent, SM, Seifert, H, Wenzel, RP, Edmond, MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 2004;39:309317.
2. Weiner, LM, Webb, AK, Limbago, B, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2011–2014. Infect Control Hosp Epidemiol 2016;37:12881301.
3. Prematunge, C, MacDougall, C, Johnstone, J, et al. VRE and VSE bacteremia outcomes in the era of effective VRE therapy: a systematic review and meta-analysis. Infect Control Hosp Epidemiol 2016;37:2635.
4. Arias, CA, Contreras, GA, Murray, BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect 2010;16:555562.
5. Morgan, DJ, Murthy, R, Munoz-Price, LS, et al. Reconsidering contact precautions for endemic methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus. Infect Control Hosp Epidemiol 2015;36:11631172.
6. Humphreys, H. Measures to prevent and control vancomycin-resistant enterococci: Do they really matter? Infect Control Hosp Epidemiol 2017;38:507509.
7. Coombs, GW, Pearson, JC, Daley, DA, et al. Molecular epidemiology of enterococcal bacteremia in Australia. J Clin Microbiol 2014;52:897905.
8. van Hal, SJ, Espedido, BA, Coombs, GW, et al. Polyclonal emergence of vanA vancomycin-resistant Enterococcus faecium in Australia. J Antimicrob Chemother 2017;72:9981001.
9. Cetinkaya, Y, Falk, P, Mayhall, CG. Vancomycin-resistant enterococci. Clin Microbiol Rev 2000;13:686707.
10. Gold, HS. Vancomycin-resistant enterococci: mechanisms and clinical observations. Clin Infect Dis 2001;33:210219.
11. Adams, DN. Shortcut detection of the vanB gene cluster in enterococci by a duplex real-time PCR assay. Pathology 2006;38:349352.
12. Hand hygiene auditing and evaluation. New South Wales Clinical Excellence Commision website. http://www.cec.health.nsw.gov.au/patient-safety-programs/assurance-governance/hand-hygiene/auditing-and-evaluation#navigation. Accessed September 9, 2017.
13. Sax, H, Allegranzi, B, Uckay, I, Larson, E, Boyce, J, Pittet, D. ‘My five moments for hand hygiene’: a user-centred design approach to understand, train, monitor and report hand hygiene. J Hosp Infect 2007;67:921.
14. Gardner, SN, Slezak, T, Hall, BG. kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics 2015;31:28772878.
15. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006;22:26882690.
16. Cheng, L, Connor, TR, Siren, J, Aanensen, DM, Corander, J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Molec Biol Evol 2013;30:12241228.
17. Jombart, T, Cori, A, Didelot, X, Cauchemez, S, Fraser, C, Ferguson, N. Bayesian reconstruction of disease outbreaks by combining epidemiologic and genomic data. PLoS Comput Biol 2014;10:e1003457.
18. Bonilla, HF, Zervos, MJ, Kauffman, CA. Long-term survival of vancomycin-resistant Enterococcus faecium on a contaminated surface. Infect Control Hosp Epidemiol 1996;17:770772.
19. Carter, GP, Buultjens, AH, Ballard, SA, et al. Emergence of endemic MLST non-typeable vancomycin-resistant Enterococcus faecium . J Antimicrob Chemother 2016;71:33673371.
20. Hayden, MK, Bonten, MJ, Blom, DW, Lyle, EA, van de Vijver, DA, Weinstein, RA. Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis 2006;42:15521560.
21. Grabsch, EA, Mahony, AA, Cameron, DR, et al. Significant reduction in vancomycin-resistant enterococcus colonization and bacteraemia after introduction of a bleach-based cleaning-disinfection programme. J Hosp Infect 2012;82:234242.
22. Anderson, RE, Young, V, Stewart, M, Robertson, C, Dancer, SJ. Cleanliness audit of clinical surfaces and equipment: Who cleans what? J Hosp Infect 2011;78:178181.
23. Dancer, SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev 2014;27:665690.
24. Huang, SS, Datta, R, Platt, R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 2006;166:19451951.
25. Drees, M, Snydman, DR, Schmid, CH, et al. Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci. Clin Infect Dis 2008;46:678685.
26. Bodily, M, McMullen, KM, Russo, AJ, Kittur, ND, Hoppe-Bauer, J, Warren, DK. Discontinuation of reflex testing of stool samples for vancomycin-resistant enterococci resulted in increased prevalence. Infect Control Hosp Epidemiol 2013;34:838840.
27. Lam, F, Johnstone, J, Adomako, K, et al. Vancomycin-resistant enterococcus (VRE) rates in Ontario, Canada after the discontinuation of VRE screening and control practices by some hospitals: interim results. Open Forum Infectious Diseases 2014;1:S257.
28. D’Agata, EM, Gautam, S, Green, WK, Tang, YW. High rate of false-negative results of the rectal swab culture method in detection of gastrointestinal colonization with vancomycin-resistant enterococci. Clin Infect Dis 2002;34:167172.
29. Gouliouris, T, Blane, B, Brodrick, HJ, et al. Comparison of two chromogenic media for the detection of vancomycin-resistant enterococcal carriage by nursing home residents. Diagn Microbiol Infect Dis 2016;85:409412.
30. Kuch, A, Stefaniuk, E, Ozorowski, T, Hryniewicz, W. New selective and differential chromogenic agar medium, chromID VRE, for screening vancomycin-resistant Enterococcus species. J Microbiol Methods 2009;77:124126.
31. Graham, M, Ballard, SA, Grabsch, EA, Johnson, PD, Grayson, ML. High rates of fecal carriage of nonenterococcal vanB in both children and adults. Antimicrob Agents Chemother 2008;52:11951197.
Type Description Title
WORD
Supplementary materials

Lee et al. supplementary material
Lee et al. supplementary material

 Word (51 KB)
51 KB
WORD
Supplementary materials

Lee et al. supplementary material
Tables S1-S2

 Word (21 KB)
21 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed