Hostname: page-component-857557d7f7-nfgnx Total loading time: 0.001 Render date: 2025-11-22T19:36:26.699Z Has data issue: false hasContentIssue false
  • English
  • Français

Predictors of Persistent Carbapenem-Resistant Enterobacteriaceae Carriage upon Readmission and Score Development

Published online by Cambridge University Press:  11 January 2016

Pnina Ciobotaro ,
Natalie Flaks-Manov ,
Maly Oved ,
Ami Schattner ,
Moshe Hoshen ,
Eli Ben-Yosef ,
Ran D. Balicer  and
Oren Zimhony
Pnina Ciobotaro*
Affiliation:
Infectious Diseases Unit, Kaplan Medical Center, Rehovot, Israel Hebrew University Hadassah Medical School, Jerusalem, Israel Clalit Research Institute, Chief Physician's Office, Clalit Health Services, Tel-Aviv, Israel
Natalie Flaks-Manov
Affiliation:
Clalit Research Institute, Chief Physician's Office, Clalit Health Services, Tel-Aviv, Israel
Maly Oved
Affiliation:
Infectious Diseases Unit, Kaplan Medical Center, Rehovot, Israel Hebrew University Hadassah Medical School, Jerusalem, Israel
Ami Schattner
Affiliation:
Hebrew University Hadassah Medical School, Jerusalem, Israel Department of Medicine, Kaplan Medical Center, Rehovot, Israel
Moshe Hoshen
Affiliation:
Clalit Research Institute, Chief Physician's Office, Clalit Health Services, Tel-Aviv, Israel
Eli Ben-Yosef
Affiliation:
Hebrew University Hadassah Medical School, Jerusalem, Israel Computer Department, Kaplan Medical Center, Rehovot, Israel
Ran D. Balicer
Affiliation:
Clalit Research Institute, Chief Physician's Office, Clalit Health Services, Tel-Aviv, Israel Epidemiology Department, Ben-Gurion University, Beer-Sheva, Israel
Oren Zimhony*
Affiliation:
Infectious Diseases Unit, Kaplan Medical Center, Rehovot, Israel Hebrew University Hadassah Medical School, Jerusalem, Israel
*
Address correspondence to Pnina Ciobotaro, MD, Infectious Diseases Unit, Kaplan Medical Center, P.O. Box 1, Rehovot, Israel (Pninaci@clalit.org.il) or Zimhony Oren, MD, Infectious Diseases Unit, Kaplan Medical Center, P.O.B. 1, Rehovot, Israel (oren_z@clalit.org.il).
Address correspondence to Pnina Ciobotaro, MD, Infectious Diseases Unit, Kaplan Medical Center, P.O. Box 1, Rehovot, Israel (Pninaci@clalit.org.il) or Zimhony Oren, MD, Infectious Diseases Unit, Kaplan Medical Center, P.O.B. 1, Rehovot, Israel (oren_z@clalit.org.il).
Get access Rights & Permissions [Opens in a new window]

Abstract

BACKGROUND

Carriers of carbapenem-resistant Enterobacteriaceae (CRE) are often readmitted, exposing patients to CRE cross-transmission.

OBJECTIVE

To identify predictors of persistent CRE carriage upon readmission, directing a risk prediction score.

DESIGN

Retrospective cohort study.

SETTING

University-affiliated general hospital.

PATIENTS

A cohort of 168 CRE carriers with 474 readmissions.

METHODS

The primary and secondary outcomes were CRE carriage status at readmission and length of CRE carriage. Predictors of persistent CRE carriage upon readmission were analyzed using a generalized estimating equations (GEE) multivariable model. Readmissions were randomly divided into derivation and validation sets. A CRE readmission score was derived to predict persistent CRE carriage in 3 risk groups: high, intermediate, and low. The discriminatory ability of the model and the score were expressed as C statistics.

RESULTS

CRE carrier status persisted for 1 year in 33% of CRE carriers. Positive CRE status was detected in 202 of 474 readmissions (42.6%). The following 4 variables were associated with persistent CRE carriage at readmission: readmission within 1 month (odds ratio [OR], 6.95; 95% confidence interval [CI], 2.79–17.30), positive CRE status on preceding admission (OR, 5.46; 95% CI, 3.06–9.75), low Norton score (OR, 3.07; 95% CI, 1.26–7.47), and diabetes mellitus (OR, 1.84; 95% CI, 0.98–3.44). The C statistics were 0.791 and 0.789 for the derivation set (n=322) model and score, respectively, and the C statistic was 0.861 for the validation set of the score (n=152). The rates of CRE carriage at readmissions (validation set) for the groups with low, intermediate, and high scores were 8.6%, 38.9%, and 77.6%, respectively.

CONCLUSIONS

CRE carrier state commonly persists upon readmission, and this risk can be estimated to guide screening policy and infection control measures.

Infect. Control Hosp. Epidemiol. 2016;37(2):188–196

Information

Type
Original Articles
Information
Infection Control & Hospital Epidemiology , Volume 37 , Issue 2 , February 2016 , pp. 188 - 196
Copyright
© 2016 by The Society for Healthcare Epidemiology of America. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

a

Authors with equal contribution.

References

REFERENCES

1. Schwaber, MJ, Carmeli, Y. Carbapenem-resistant Enterobacteriaceae: a potential threat. JAMA 2008;300:2911–2913.Google Scholar
2. Schwaber, MJ, Klarfeld-Lidji, S, Navon-Venezia, S, Schwartz, D, Leavitt, A, Carmeli, Y. Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality. Antimicrob Agents Chemother 2008;52:1028–1033.Google Scholar
3. Nordmann, P, Naas, T, Poirel, L. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 2011;17:1791–1798.CrossRefGoogle ScholarPubMed
4. Glasner, C, Albiger, B, Buist, G, et al. Carbapenemase-producing Enterobacteriaceae in Europe: a survey among national experts from 39 countries, February 2013. Euro Surveill 2013;18(28):pii=20525.Google Scholar
5. Hidron, AI, Edwards, JR, Patel, J, et al. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol 2008;29:996–1011.Google Scholar
6. Hirsch, EB, Tam, VH. Detection and treatment options for Klebsiella pneumoniae carbapenemases (KPCs): an emerging cause of multidrug-resistant infection. J Antimicrob Chemother 2010;65:1119–1125.CrossRefGoogle ScholarPubMed
7. Van Duin, D, Kaye, KS, Neuner, EA, Bonomo, RA. Carbapenem-resistant Enterobacteriaceae: a review of treatment and outcomes. Diagn Microbiol Infect Dis 2013;75:115–120.CrossRefGoogle ScholarPubMed
8. Patel, G, Huprikar, S, Factor, SH, Jenkins, SG, Calfee, DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol 2008;29:1099–1106.Google Scholar
9. Borer, A, Saidel-Odes, L, Riesenberg, K, et al. Attributable mortality rate for carbapenem-resistant Klebsiella pneumoniae bacteremia. Infect Control Hosp Epidemiol 2009;30:972–976.Google Scholar
10. Center for Disease Control and Prevention. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. MMWR 2009;58:256–260.Google Scholar
11. Schwaber, MJ, Lev, B, Israeli, A, et al. Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin Infect Dis 2011;52:848–855.Google Scholar
12. Ciobotaro, P, Oved, M, Nadir, E, Bardenstein, R, Zimhony, O. An effective intervention to limit the spread of an epidemic carbapenem-resistant Klebsiella pneumoniae strain in an acute care setting: From theory to practice. Am J Infect Control 2011;39:671–677.Google Scholar
13. Schwaber, MJ, Carmeli, Y. An ongoing national intervention to contain the spread of carbapenem-resistant Enterobacteriaceae. Clin Infect Dis 2013, doi:10.1093/cid/cit795.Google ScholarPubMed
14. Ben-David, D, Maor, Y, Keller, N, et al. Potential role of active surveillance in the control of a hospital-wide outbreak of carbapenem-resistant Klebsiella pneumoniae infection. Infect Control Hosp Epidemiol 2010;31:620–626.Google Scholar
15. Marchaim, D, Chopra, T, Perez, F, et al. Outcomes and genetic relatedness of carbapenem-resistant enterobacteriaceae at Detroit medical center. Infect Control Hosp Epidemiol 2011;32:861–871.CrossRefGoogle ScholarPubMed
16. Neuner, EA, Yeh, J-Y, Hall, GS, et al. Treatment and outcomes in carbapenem-resistant Klebsiella pneumoniae bloodstream infections. Diagn Microbiol Infect Dis 2011;69:357–362.CrossRefGoogle ScholarPubMed
17. Emerson, CB, Eyzaguirre, LM, Albrecht, JS, Comer, AC, Harris, AD, Furuno, JP. Healthcare-associated infection and hospital readmission. Infect Control Hosp Epidemiol 2012;33:539–544.CrossRefGoogle ScholarPubMed
18. 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;53:532–540.Google Scholar
19. Souli, M, Galani, I, Antoniadou, A, et al. An outbreak of infection due to beta-lactamase Klebsiella pneumoniae carbapenemase 2-producing K. pneumoniae in a Greek University Hospital: molecular characterization, epidemiology, and outcomes. Clin Infect Dis 2010;50:364–373.CrossRefGoogle Scholar
20. Landman, D, Salvani, JK, Bratu, S, Quale, J. Evaluation of techniques for detection of carbapenem-resistant Klebsiella pneumoniae in stool surveillance cultures. J Clin Microbiol 2005;43:5639–5641.Google Scholar
21. Schechner, V, Straus-Robinson, K, Schwartz, D, et al. Evaluation of PCR-based testing for surveillance of KPC-producing carbapenem-resistant members of the Enterobacteriaceae family. J Clin Microbiol 2009;47:3261–3265.Google Scholar
22. Feldman, N, Adler, A, Molshatzki, N, et al. Gastrointestinal colonization by KPC-producing Klebsiella pneumoniae following hospital discharge: duration of carriage and risk factors for persistent carriage. Clin Microbiol Infect 2013;19:E190–E196.CrossRefGoogle ScholarPubMed
23. Hussein, K, Raz-Pasteur, A, Finkelstein, R, et al. Impact of carbapenem resistance on the outcome of patients’ hospital-acquired bacteraemia caused by Klebsiella pneumoniae . J Hosp Infect 2013;83:307–313.CrossRefGoogle ScholarPubMed
24. Zimmerman, FS, Assous, M V, Bdolah-Abram, T, Lachish, T, Yinnon, AM, Wiener-Well, Y. Duration of carriage of carbapenem-resistant Enterobacteriaceae following hospital discharge. Am J Infect Control 2013;41:190–194.Google Scholar
25. 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;32:497–503.Google Scholar
26. 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;32:845–853.Google Scholar
27. Samra, Z, Bahar, J, Madar-Shapiro, L, Aziz, N, Israel, S, Bishara, J. Evaluation of CHROMagar KPC for rapid detection of carbapenem-resistant Enterobacteriaceae. J Clin Microbiol 2008;46:3110–3111.Google Scholar
28. Anderson, KF, Lonsway, DR, Rasheed, JK, et al. Evaluation of methods to identify the Klebsiella pneumoniae carbapenemase in Enterobacteriaceae. J Clin Microbiol 2007;45:2723–2725.Google Scholar
29. CLSI. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Third Informational Supplement CLSI document M100-S23Wayne, PA: Clinical and Laboratory Standards Institute, 2013.Google Scholar
30. Norton, D, McLaren, R, Exton-Smith, A. An Investigation of Geriatric Nursing Problems in the Hospital. Edinburgh: Churchill Livingstone, 1975.Google Scholar
31. Zeger, SL, Liang, KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics 1986;42:121–130.Google Scholar
32. Hanley, JA, Negassa, A, Edwardes, MD deB, Forrester, JE. Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 2003;157:364–375.CrossRefGoogle Scholar
33. Balla, U, Malnick, S, Schattner, A. Early readmissions to the department of medicine as a screening tool for monitoring quality of care problems. Medicine (Baltimore) 2008;87:294–300.Google Scholar
34. Justo, D, Vislapu, N, Shvedov, V, et al. Admission Norton scale scores (ANSS) correlate with rehabilitation outcome and length in elderly patients following hip arthroplasty. Arch Gerontol Geriatr 2011;53:e33–e36.CrossRefGoogle ScholarPubMed
35. Gold, A, Sever, R, Lerman, Y, Salai, M, Justo, D. Admission Norton scale scores (ANSS) and postoperative complications following hip fracture surgery in the elderly. Arch Gerontol Geriatr 2012;55:173–176.CrossRefGoogle ScholarPubMed
36. Adler, A, Gniadkowski, M, Baraniak, A, et al. Transmission dynamics of ESBL-producing Escherichia coli clones in rehabilitation wards at a tertiary care centre. Clin Microbiol Infect 2012;18:E497–E505.Google Scholar
37. Lim, CJ, Cheng, AC, Kennon, J, et al. Prevalence of multidrug-resistant organisms and risk factors for carriage in long-term care facilities: a nested case-control study. J Antimicrob Chemother 2014, doi:10.1093/jac/dku077.Google Scholar
38. O’Sullivan, NP, Keane, CT. Risk factors for colonization with methicillin-resistant Staphylococcus aureus among nursing home residents. J Hosp Infect 2000;45:206–210.Google Scholar
39. McKinnell, JA, Miller, LG, Eells, SJ, Cui, E, Huang, SS. A systematic literature review and meta-analysis of factors associated with methicillin-resistant Staphylococcus aureus colonization at time of hospital or intensive care unit admission. Infect Control Hosp Epidemiol 2013;34:1077–1086.CrossRefGoogle ScholarPubMed
40. Day, D. Keeping patients safe during intrahospital transport. Crit Care Nurse 2010;30:18–32.Google Scholar