Skip to main content Accessibility help

Control of Simultaneous Outbreaks of Carbapenemase-Producing Enterobacteriaceae and Extensively Drug-Resistant Acinetobacter baumannii Infection in an Intensive Care Unit Using Interventions Promoted in the Centers for Disease Control and Prevention 2012 Carbapenemase-Resistant Enterobacteriaceae Toolkit

  • Kyle B. Enfield (a1) (a2), Nujhat N. Huq (a3), Megan F. Gosseling (a2), Darla J. Low (a2), Kevin C. Hazen (a4), Denise M. Toney (a5), Gavin Slitt (a3), Heidi J. Zapata (a3), Heather L. Cox (a3), Jessica D. Lewis (a3), John R. Kundzins (a3), Amy J. Mathers (a3) and Costi D. Sifri (a2) (a3)...



We describe the efficacy of enhanced infection control measures, including those recommended in the Centers for Disease Control and Prevention’s 2012 carbapenem-resistant Enterobacteriaceae (CRE) toolkit, to control concurrent outbreaks of carbapenemase-producing Enterobacteriaceae (CPE) and extensively drug-resistant Acinetobacter baumannii (XDR-AB).


Before-after intervention study.


Fifteen-bed surgical trauma intensive care unit (ICU).


We investigated the impact of enhanced infection control measures in response to clusters of CPE and XDR-AB infections in an ICU from April 2009 to March 2010. Polymerase chain reaction was used to detect the presence of bla KPC and resistance plasmids in CRE. Pulsed-field gel electrophoresis was performed to assess XDR-AB clonality. Enhanced infection-control measures were implemented in response to ongoing transmission of CPE and a new outbreak of XDR-AB. Efficacy was evaluated by comparing the incidence rate (IR) of CPE and XDR-AB before and after the implementation of these measures.


The IR of CPE for the 12 months before the implementation of enhanced measures was 7.77 cases per 1,000 patient-days, whereas the IR of XDR-AB for the 3 months before implementation was 6.79 cases per 1,000 patient-days. All examined CPE shared endemic bla KPC resistance plasmids, and 6 of the 7 XDR-AB isolates were clonal. Following institution of enhanced infection control measures, the CPE IR decreased to 1.22 cases per 1,000 patient-days (P = .001), and no more cases of XDR-AB were identified.


Use of infection control measures described in the Centers for Disease Control and Prevention’s 2012 CRE toolkit was associated with a reduction in the IR of CPE and an interruption in XDR-AB transmission.


Corresponding author

Division of Infectious Diseases and International Health, Hospital Epidemiology/Infection Prevention and Control, University of Virginia Health System, P.O. Box 800473, Charlottesville, VA 22908 (


Hide All

K.B.E. and N.N.H. contributed equally to this article.



Hide All
1. Peleg, AY, Hooper, DC. Hospital-acquired infections due to gram-negative bacteria. N Engl J Med 2010;362:18041813.
2. Karageorgopoulos, DE, Falagas, ME. Current control and treatment of multidrug-resistant Acinetobacter baumannii infections. Lancet Infect Dis 2008;8:751762.
3. Gupta, N, Limbago, BM, Patel, JB, Kallen, AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis 2011;53:6067.
4. Centers for Disease Control and Prevention. 2012 CRE toolkit: guidance for control of carbapenem-resistance Enterobacteriaceae (CRE). Accessed January 5, 2013.
5. Magiorakos, AP, Srinivasan, A, Carey, RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268281.
6. Rutala, WA, Weber, DJ; Healthcare Infection Control Practice Advisory Committee (HICPAC). Guideline for disinfection and sterilization in healthcare facilities, 2008. Accessed January 12, 2013.
7. World Health Organization (WHO) Collaborating Centre for Drug Statistics Methodology. ATC/DDD index 2013. Accessed November 29, 2013.
8. Mathers, AJ, Cox, HL, Kitchel, B, et al. Molecular dissection of an outbreak of carbapenem-resistant Enterobacteriaceae reveals intergenus KPC carbapenemase transmission through a promiscuous plasmid. MBio 2011;2:e00204–e00211.
9. Mathers, AJ, Carroll, J, Sifri, CD, Hazen, KC. Modified Hodge test versus indirect carbapenemase test: prospective evaluation of a phenotypic assay for detection of Klebsiella pneumoniae carbapenemase (KPC) in Enterobacteriaceae . J Clin Microbiol 2013;51:12911293.
10. Mathers, AJ, Hazen, KC, Carroll, J, et al. First clinical cases of OXA-48-producing carbapenem-resistant Klebsiella pneumoniae in the United States: the “menace” arrives in the new world. J Clin Microbiol 2013;51:680683.
11. Mathers, AJ, Poulter, M, Dirks, D, Carroll, J, Sifri, CD, Hazen, KC. Clinical microbiology costs for methods of active surveillance for Klebsiella pneumoniae carbapenemase (KPC) producing Enterobacteriaceae Infect Control Hosp Epidemiol 2014;35(4):350355.
12. Ribot, EM, Fair, MA, Gautom, R, et al. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157: H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 2006;3:5967.
13. Tenover, FC, Arbeit, RD, Goering, RV, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995;33:22332239.
14. Wagner, AK, Soumerai, SB, Zhang, F, Ross-Degnan, D. Segmented regression analysis of interrupted time series studies in medication use research. J Clin Pharm Ther 2002;27:299309.
15. McCullagh, P. Quasi-likelihood functions. Ann Statist 1983;11:5967.
16. Mathers, AJ, Cox, HL, Bonatti, H, et al. Fatal cross infection by carbapenem-resistant Klebsiella in two liver transplant recipients. Transpl Infect Dis 2009;11:257265.
17. Swaminathan, M, Sharma, S, Poliansky Blash, S, et al. Prevalence and risk factors for acquisition of carbapenem-resistant Enterobacteriaceae in the setting of endemicity. Infect Control Hosp Epidemiol 2013;34:809817.
18. Corbella, X, Pujol, M, Ayats, J, et al. Relevance of digestive tract colonization in the epidemiology of nosocomial infections due to multiresistant Acinetobacter baumannii . Clin Infect Dis 1996;23:329334.
19. Jung, JY, Park, MS, Kim, SE, et al. Risk factors for multi-drug resistant Acinetobacter baumannii bacteremia in patients with colonization in the intensive care unit. BMC Infect Dis 2012;10:228.


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