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Modeling Spread of KPC-Producing Bacteria in Long-Term Acute Care Hospitals in the Chicago Region, USA

  • Manon R. Haverkate (a1) (a2), Martin C. J. Bootsma (a1) (a3), Shayna Weiner (a2), Donald Blom (a2), Michael Y. Lin (a2), Karen Lolans (a4), Nicholas M. Moore (a5), Rosie D. Lyles (a6), Robert A. Weinstein (a2) (a6), Marc J. M. Bonten (a1) (a7) and Mary K. Hayden (a2) (a4)...



Prevalence of bla KPC-encoding Enterobacteriaceae (KPC) in Chicago long-term acute care hospitals (LTACHs) rose rapidly after the first recognition in 2007. We studied the epidemiology and transmission capacity of KPC in LTACHs and the effect of patient cohorting.


Data were available from 4 Chicago LTACHs from June 2012 to June 2013 during a period of bundled interventions. These consisted of screening for KPC rectal carriage, daily chlorhexidine bathing, medical staff education, and 3 cohort strategies: a pure cohort (all KPC-positive patients on 1 floor), single rooms for KPC-positive patients, and a mixed cohort (all KPC-positive patients on 1 floor, supplemented with KPC-negative patients). A data-augmented Markov chain Monte Carlo (MCMC) method was used to model the transmission process.


Average prevalence of KPC colonization was 29.3%. On admission, 18% of patients were colonized; the sensitivity of the screening process was 81%. The per admission reproduction number was 0.40. The number of acquisitions per 1,000 patient days was lowest in LTACHs with a pure cohort ward or single rooms for colonized patients compared with mixed-cohort wards, but 95% credible intervals overlapped.


Prevalence of KPC in LTACHs is high, primarily due to high admission prevalence and the resultant impact of high colonization pressure on cross transmission. In this setting, with an intervention in place, patient-to-patient transmission is insufficient to maintain endemicity. Inclusion of a pure cohort or single rooms for KPC-positive patients in an intervention bundle seemed to limit transmission compared to use of a mixed cohort.

Infect Control Hosp Epidemiol 2015;36(10):1148–1154


Corresponding author

Address correspondence to Manon R. Haverkate, Huispostnummer Geuns 5.02, Heidelberglaan 100, 3584 CK Utrecht (


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Preliminary results from this study were presented at IDWeek 2014; October 8–12, 2014, Philadelphia, Pennsylvania, USA.



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1. Nordmann, P, Dortet, L, Poirel, L. Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol Med 2012;18:263272.
2. Canton, R, Akova, M, Carmeli, Y, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect 2012;18:413431.
3. Nordmann, P, Naas, T, Poirel, L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 2011;17:17911798.
4. Nordmann, P, Cuzon, G, Naas, T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis 2009;9:228236.
5. Munoz-Price, LS, Hayden, MK, Lolans, K, et al. Successful control of an outbreak of Klebsiella pneumoniae carbapenemase-producing K. pneumoniae at a long-term acute care hospital. Infect Control Hosp Epidemiol 2010;31:341347.
6. Munoz-Price, LS, De La, CC, Adams, S, et al. Successful eradication of a monoclonal strain of Klebsiella pneumoniae during a K. pneumoniae carbapenemase-producing K. pneumoniae outbreak in a surgical intensive care unit in Miami, Florida. Infect Control Hosp Epidemiol 2010;31:10741077.
7. Won, SY, Munoz-Price, LS, Lolans, K, Hota, B, Weinstein, RA, Hayden, MK. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis 2011;53:532540.
8. Chitnis, AS, Caruthers, PS, Rao, AK, et al. Outbreak of carbapenem-resistant Enterobacteriaceae at a long-term acute care hospital: sustained reductions in transmission through active surveillance and targeted interventions. Infect Control Hosp Epidemiol 2012;33:984992.
9. Munoz-Price, LS. Long-term acute care hospitals. Clin Infect Dis 2009;49:438443.
10. Lin, MY, Lyles-Banks, RD, Lolans, K, et al. The importance of long-term acute care hospitals in the regional epidemiology of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis 2013;57:12461252.
11. Prabaker, K, Lin, MY, McNally, M, et al. Transfer from high-acuity long-term care facilities is associated with carriage of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae: a multihospital study. Infect Control Hosp Epidemiol 2012;33:11931199.
12. Ben-David, D, Masarwa, S, Navon-Venezia, S, et al. Carbapenem-resistant Klebsiella pneumoniae in post-acute-care facilities in Israel. Infect Control Hosp Epidemiol 2011;32:845853.
13. Schechner, V, Kotlovsky, T, Tarabeia, J, et al. Predictors of rectal carriage of carbapenem-resistant Enterobacteriaceae (CRE) among patients with known CRE carriage at their next hospital encounter. Infect Control Hosp Epidemiol 2011;32:497503.
14. Donker, T, Wallinga, J, Slack, R, Grundmann, H. Hospital networks and the dispersal of hospital-acquired pathogens by patient transfer. PLoS One 2012;7:e35002.
15. Donker, T, Wallinga, J, Grundmann, H. Patient referral patterns and the spread of hospital-acquired infections through national health care networks. PLoS Comput Biol 2010;6:e1000715.
16. Lee, BY, Bartsch, SM, Wong, KF, et al. Simulation shows hospitals that cooperate on infection control obtain better results than hospitals acting alone. Health Aff (Millwood) 2012;31:22952303.
17. Smith, DL, Dushoff, J, Perencevich, EN, Harris, AD, Levin, SA. Persistent colonization and the spread of antibiotic resistance in nosocomial pathogens: resistance is a regional problem. Proc Natl Acad Sci U S A 2004;101:37093714.
18. Huang, SS, Avery, TR, Song, Y, et al. Quantifying interhospital patient sharing as a mechanism for infectious disease spread. Infect Control Hosp Epidemiol 2010;31:11601169.
19. Barnes, SL, Harris, AD, Golden, BL, Wasil, EA, Furuno, JP. Contribution of interfacility patient movement to overall methicillin-resistant Staphylococcus aureus prevalence levels. Infect Control Hosp Epidemiol 2011;32:10731078.
20. Lee, BY, McGlone, SM, Wong, KF, et al. Modeling the spread of methicillin-resistant Staphylococcus aureus (MRSA) outbreaks throughout the hospitals in Orange County, California. Infect Control Hosp Epidemiol 2011;32:562572.
21. Lee, BY, Bartsch, SM, Wong, KF, et al. The importance of nursing homes in the spread of methicillin-resistant Staphylococcus aureus (MRSA) among hospitals. Med Care 2013;51:205215.
22. Lee, BY, Yilmaz, SL, Wong, KF, et al. Modeling the regional spread and control of vancomycin-resistant Enterococci. Am J Infect Control 2013;41:668673.
23. Domenech de, CM, Zahar, JR, Abadie, V, Guillemot, D. Limits of patient isolation measures to control extended-spectrum beta-lactamase-producing Enterobacteriaceae: model-based analysis of clinical data in a pediatric ward. BMC Infect Dis 2013;13:187.
24. Hayden, MK, Lin, MY, Lolans, K, et al. Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase-producing enterobacteriaceae in long term acute care hospitals. Clin Infect Dis 2015;60:1153–1161.
25. Cole, JM, Schuetz, AN, Hill, CE, Nolte, FS. Development and evaluation of a real-time PCR assay for detection of Klebsiella pneumoniae carbapenemase genes. J Clin Microbiol 2009;47:322326.
26. Lolans, K, Calvert, K, Won, S, Clark, J, Hayden, MK. Direct ertapenem disk screening method for identification of KPC-producing Klebsiella pneumoniae and Escherichia coli in surveillance swab specimens. J Clin Microbiol 2010;48:836841.
27. Mangold, KA, Santiano, K, Broekman, R, et al. Real-time detection of blaKPC in clinical samples and surveillance specimens. J Clin Microbiol 2011;49:33383339.
28. Bonten, MJ. Colonization pressure: a critical parameter in the epidemiology of antibiotic-resistant bacteria. Crit Care 2012;16:142.
29. Worby, CJ, Jeyaratnam, D, Robotham, JV, et al. Estimating the effectiveness of isolation and decolonization measures in reducing transmission of methicillin-resistant Staphylococcus aureus in hospital general wards. Am J Epidemiol 2013;177:13061313.
30. Borenstein, M, Hedges, L, Rothstein, H. Meta-analysis: fixed effect vs. random effects. Meta-analysis website. Published 2007. Accessed June 19, 2015.
31. Neyeloff, JL, Fuchs, SC, Moreira, LB. Meta-analyses and Forest plots using a microsoft excel spreadsheet: step-by-step guide focusing on descriptive data analysis. BMC Res Notes 2012;5:52.
32. Diekmann, O, Heesterbeek, H, Britton, T. Mathematical Tools for Understanding Infectious Disease Dynamics. Princeton: Princeton University Press, 2012.
33. Cooper, BS, Medley, GF, Stone, SP, et al. Methicillin-resistant Staphylococcus aureus in hospitals and the community: stealth dynamics and control catastrophes. Proc Natl Acad Sci U S A 2004;101:1022310228.
34. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. MMWR 2009;58:256260.
35. Ben-David, D, Masarwa, S, Adler, A, Mishali, H, Carmeli, Y, Schwaber, MJ. A national intervention to prevent the spread of carbapenem-resistant Enterobacteriaceae in Israeli post-acute care hospitals. Infect Control Hosp Epidemiol 2014;35:802809.
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