Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T05:16:19.209Z Has data issue: false hasContentIssue false

Modifiable Risk Factors for the Spread of Klebsiella pneumoniae Carbapenemase-Producing Enterobacteriaceae Among Long-Term Acute-Care Hospital Patients

Published online by Cambridge University Press:  11 April 2017

Koh Okamoto*
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States
Michael Y. Lin
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States
Manon Haverkate
Affiliation:
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, Netherlands
Karen Lolans
Affiliation:
Department of Pathology, Rush University Medical Center, Chicago, Illinois, United States
Nicholas M. Moore
Affiliation:
Department of Pathology, Rush University Medical Center, Chicago, Illinois, United States Department of Medical Laboratory Science, Rush University Medical Center, Chicago, Illinois, United States
Shayna Weiner
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States
Rosie D. Lyles
Affiliation:
Department of Medicine, Division of Infectious Diseases, Cook County Health and Hospitals System, Chicago, Illinois, United States
Donald Blom
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States
Yoona Rhee
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States
Sarah Kemble
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States
Louis Fogg
Affiliation:
Department of Nursing, Rush University Medical Center, Chicago, Illinois, United States
David W. Hines
Affiliation:
Metro Infectious Disease Consultants, LLC, Burr Ridge, Illinois, United States
Robert A. Weinstein
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States Department of Medicine, Division of Infectious Diseases, Cook County Health and Hospitals System, Chicago, Illinois, United States
Mary K. Hayden*
Affiliation:
Department of Internal Medicine, Division of Infectious Diseases, Rush University Medical Center, Chicago, Illinois, United States Department of Pathology, Rush University Medical Center, Chicago, Illinois, United States
*
Address correspondence to Koh Okamoto, MD, MS, Department of Infectious Diseases, University of Tokyo Hospital, 7-3-1, Hongo, Bunkyo, Tokyo 113-8655, Japan (kokamoto-tky@umin.ac.jp) or Mary Hayden, MD, Rush University Medical Center, 1653 W Congress Pkwy, Chicago, IL 60612 (mhayden@rush.edu).
Address correspondence to Koh Okamoto, MD, MS, Department of Infectious Diseases, University of Tokyo Hospital, 7-3-1, Hongo, Bunkyo, Tokyo 113-8655, Japan (kokamoto-tky@umin.ac.jp) or Mary Hayden, MD, Rush University Medical Center, 1653 W Congress Pkwy, Chicago, IL 60612 (mhayden@rush.edu).

Abstract

OBJECTIVE

To identify modifiable risk factors for acquisition of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae (KPC) colonization among long-term acute-care hospital (LTACH) patients.

DESIGN

Multicenter, matched case-control study.

SETTING

Four LTACHs in Chicago, Illinois.

PARTICIPANTS

Each case patient included in this study had a KPC-negative rectal surveillance culture on admission followed by a KPC-positive surveillance culture later in the hospital stay. Each matched control patient had a KPC-negative rectal surveillance culture on admission and no KPC isolated during the hospital stay.

RESULTS

From June 2012 to June 2013, 2,575 patients were admitted to 4 LTACHs; 217 of 2,144 KPC-negative patients (10.1%) acquired KPC. In total, 100 of these patients were selected at random and matched to 100 controls by LTACH facility, admission date, and censored length of stay. Acquisitions occurred a median of 16.5 days after admission. On multivariate analysis, we found that exposure to higher colonization pressure (OR, 1.02; 95% CI, 1.01–1.04; P=.002), exposure to a carbapenem (OR, 2.25; 95% CI, 1.06–4.77; P=.04), and higher Charlson comorbidity index (OR, 1.14; 95% CI, 1.01–1.29; P=.04) were independent risk factors for KPC acquisition; the odds of KPC acquisition increased by 2% for each 1% increase in colonization pressure.

CONCLUSIONS

Higher colonization pressure, exposure to carbapenems, and a higher Charlson comorbidity index independently increased the odds of KPC acquisition among LTACH patients. Reducing colonization pressure (through separation of KPC-positive patients from KPC-negative patients using strict cohorts or private rooms) and reducing carbapenem exposure may prevent KPC cross transmission in this high-risk patient population.

Infect Control Hosp Epidemiol 2017;38:670–677

Type
Original Articles
Copyright
© 2017 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.)

Footnotes

PREVIOUS PRESENTATION. The findings reported here were presented in part at IDWeek 2015, San Diego, California, on October 10, 2015 (abstract no. 1332).

References

REFERENCES

1. Nordmann, P, Naas, T, Poirel, L. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 2011;17:17911798.CrossRefGoogle ScholarPubMed
2. Gupta, N, Limbago, BM, Patel, JB, Kallen, AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis 2011;53:6067.Google Scholar
3. Centers for Disease C, Prevention. Vital signs: carbapenem-resistant Enterobacteriaceae. Morb Mortal Wkly Rep 2013;62:165170.Google Scholar
4. Tumbarello, M, Trecarichi, EM, De Rosa, FG, et al. Infections caused by KPC-producing Klebsiella pneumoniae: differences in therapy and mortality in a multicentre study. J Antimicrob Chemother 2015;70:21332143.Google Scholar
5. 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;52:848855.Google Scholar
6. Munoz-Price, LS, Poirel, L, Bonomo, RA, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013;13:785796.Google Scholar
7. Marquez, P, Terashita, D, Dassey, D, Mascola, L. Population-based incidence of carbapenem-resistant Klebsiella pneumoniae along the continuum of care, Los Angeles County. Infect Control Hosp Epidemiol 2013;34:144150.CrossRefGoogle ScholarPubMed
8. 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.Google Scholar
9. Munoz-Price, LS. Long-term acute care hospitals. Clin Infect Dis 2009;49:438443.Google Scholar
10. Gould, CV, Rothenberg, R, Steinberg, JP. Antibiotic resistance in long-term acute care hospitals: the perfect storm. Infect Control Hosp Epidemiol 2006;27:920925.Google Scholar
11. 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;60:11531161.Google Scholar
12. Bonten, MJ, Slaughter, S, Ambergen, AW, et al. The role of “colonization pressure” in the spread of vancomycin-resistant enterococci: an important infection control variable. Arch Intern Med 1998;158:11271132.Google Scholar
13. Charlson, ME, Pompei, P, Ales, KL, MacKenzie, CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373383.CrossRefGoogle ScholarPubMed
14. 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.Google Scholar
15. 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.CrossRefGoogle ScholarPubMed
16. 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.Google Scholar
17. 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.Google Scholar
18. Papadimitriou-Olivgeris, M, Marangos, M, Fligou, F, et al. KPC-producing Klebsiella pneumoniae enteric colonization acquired during intensive care unit stay: the significance of risk factors for its development and its impact on mortality. Diagn Microbiol Infect Dis 2013;77:169173.Google Scholar
19. Bonten, MJ. Colonization pressure: a critical parameter in the epidemiology of antibiotic-resistant bacteria. Crit Care 2012;16:142.Google Scholar
20. Schwartz-Neiderman, A, Braun, T, Fallach, N, Schwartz, D, Carmeli, Y, Schechner, V. Risk factors for carbapenemase-producing carbapenem-resistant enterobacteriaceae (CP-CRE) acquisition among contacts of newly diagnosed CP-CRE patients. Infect Control Hosp Epidemiol 2016:17.Google Scholar
21. Ajao, AO, Harris, AD, Roghmann, MC, et al. Systematic review of measurement and adjustment for colonization pressure in studies of methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and Clostridium difficile acquisition. Infect Control Hosp Epidemiol 2011;32:481489.Google Scholar
22. 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.Google Scholar
23. Mills, JP, Talati, NJ, Alby, K, Han, JH. The epidemiology of carbapenem-resistant Klebsiella pneumoniae colonization and infection among long-term acute care hospital residents. Infect Control Hosp Epidemiol 2016;37:5560.Google Scholar
24. Papadimitriou-Olivgeris, M, Spiliopoulou, I, Christofidou, M, et al. Co-colonization by multidrug-resistant bacteria in two Greek intensive care units. Eur J Clin Microbiol Infect Dis 2015;34:19471955.CrossRefGoogle ScholarPubMed
25. Tumbarello, M, Trecarichi, EM, Tumietto, F, et al. Predictive models for identification of hospitalized patients harboring KPC-producing Klebsiella pneumoniae . Antimicrob Agents Chemother 2014;58:35143520.CrossRefGoogle ScholarPubMed
26. Orsi, GB, Bencardino, A, Vena, A, et al. Patient risk factors for outer membrane permeability and KPC-producing carbapenem-resistant Klebsiella pneumoniae isolation: results of a double case-control study. Infection 2013;41:6167.Google Scholar
27. Papadimitriou-Olivgeris, M, Marangos, M, Fligou, F, et al. Risk factors for KPC-producing Klebsiella pneumoniae enteric colonization upon ICU admission. J Antimicrob Chemother 2012;67:29762981.Google Scholar
28. Wu, D, Cai, J, Liu, J. Risk factors for the acquisition of nosocomial infection with carbapenem-resistant Klebsiella pneumoniae . South Med J 2011;104:106110.CrossRefGoogle ScholarPubMed
29. Orsi, GB, Garcia-Fernandez, A, Giordano, A, et al. Risk factors and clinical significance of ertapenem-resistant Klebsiella pneumoniae in hospitalised patients. J Hosp Infect 2011;78:5458.Google Scholar
30. Hussein, K, Sprecher, H, Mashiach, T, Oren, I, Kassis, I, Finkelstein, R. Carbapenem resistance among Klebsiella pneumoniae isolates: risk factors, molecular characteristics, and susceptibility patterns. Infect Control Hosp Epidemiol 2009;30:666671.Google Scholar
31. 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;29:10991106.Google Scholar
32. Kwak, YG, Choi, SH, Choo, EJ, et al. Risk factors for the acquisition of carbapenem-resistant Klebsiella pneumoniae among hospitalized patients. Microb Drug Resist 2005;11:165169.Google Scholar
33. 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;52:10281033.CrossRefGoogle ScholarPubMed
34. Prepublication standards—new antimicrobial stewardship standard. The Joint Commission website. https://www.jointcommission.org/standards_information/prepublication_standards.aspx. Published 2016. Accessed November 24, 2016.Google Scholar
35. Bhargava, A, Hayakawa, K, Silverman, E, et al. Risk factors for colonization due to carbapenem-resistant Enterobacteriaceae among patients exposed to long-term acute care and acute care facilities. Infect Control Hosp Epidemiol 2014;35:398405.CrossRefGoogle ScholarPubMed
36. 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.CrossRefGoogle Scholar
37. Safdar, N, Maki, DG. The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, enterococcus, gram-negative bacilli, Clostridium difficile, and Candida . Ann Intern Med 2002;136:834844.CrossRefGoogle ScholarPubMed
38. Haverkate, MR, Bootsma, MC, Weiner, S, et al. Modeling spread of KPC-producing bacteria in long-term acute care hospitals in the Chicago region, USA. Infect Control Hosp Epidemiol 2015:17.Google ScholarPubMed