Risk Factors for Colonization Due to Carbapenem-Resistant Enterobacteriaceae Among Patients Exposed to Long-term Acute Care and Acute Care Facilities

Ashish Bhargava, MD; Kayoko Hayakawa, MD; Ethan Silverman, BS; Samran Haider, MBBS; Krishna Chaitanya Alluri, MBBS; Satya Datla, MBBS; Sreelatha Diviti, MBBS; Vamsi Kuchipudi, MBBS; Kalyan Srinivas Muppavarapu, MBBS; Paul R. Lephart; Dror Marchaim, MD; Keith S. Kaye, MD, MPH


Infect Control Hosp Epidemiol. 2014;35(4):398-405. 

In This Article

Abstract and Introduction


Background. This study aimed to identify risk factors associated with carbapenem-resistant Enterobacteriaceae (CRE) colonization among patients screened with rectal cultures upon admission to a hospital or long-term acute care (LTAC) center and to compare risk factors among patients who were screen positive for CRE at the time of hospital admission with those screen positive prior to LTAC admission.

Methods. A retrospective nested matched case-control study was conducted from June 2009 to December 2011. Patients with recent LTAC exposure were screened for CRE carriage at the time of hospital admission, and patients admitted to a regional LTAC facility were screened prior to LTAC admission. Cases were patients with a positive CRE screening culture, and controls (matched in a 3:1 ratio to cases) were patients with negative screening cultures.

Results. Nine hundred five cultures were performed on 679 patients. Forty-eight (7.1%) cases were matched to 144 controls. One hundred fifty-eight patients were screened upon hospital admission and 521 prior to LTAC admission. Independent predictors for CRE colonization included Charlson's score greater than 3 (odds ratio [OR], 4.85 [95% confidence interval (CI), 1.64–14.41]), immunosuppression (OR, 3.92 [95% CI, 1.08–1.28]), presence of indwelling devices (OR, 5.21 [95% CI, 1.09–2.96]), and prior antimicrobial exposures (OR, 3.89 [95% CI, 0.71–21.47]). Risk factors among patients screened upon hospital admission were similar to the entire cohort. Among patients screened prior to LTAC admission, the characteristics of the CRE-colonized and noncolonized patients were similar.

Conclusions. These results can be used to identify patients at increased risk for CRE colonization and to help target active surveillance programs in healthcare settings.


Carbapenems are extended-spectrum antimicrobials effective against many multidrug-resistant gram-negative pathogens. The spread of carbapenem-resistant Enterobacteriaceae (CRE) is an emerging and concerning public health threat.[1] CREs are extensively drug-resistant pathogens associated with high rates of mortality.[2,3] The most common carbapenemase in the United States is Klebsiella pneumoniae carbapenemase (KPC). Since the first KPC-producing K. pneumoniae was reported in 2001,[4] KPC-producing isolates have disseminated widely. KPCs are transmissible through mobile genetic elements (ie, mainly through the transposon Tn4401)[5,6] and have the potential to spread rapidly in healthcare settings.[7] Thus, preventing CRE transmission and infections due to CRE have become important clinical and public health objectives.

Asymptomatically colonized patients with CRE are often a source of CRE transmission in healthcare settings. Active surveillance is a strategy to identify asymptomatic colonization with multidrug-resistant pathogens[8] and has been associated with reduction in transmission of methicillin-resistant Staphylococcus aureus[9] and vancomycin-resistant enterococci.[10] Early identification of carriers through active surveillance, coupled with implementation of contact precautions and cohorting of patients and staff, has been associated with reduction in horizontal, patient-to-patient transmission of multidrug-resistant pathogens, including CREs.[11,12] Active surveillance with cultures and/or polymerase chain reaction of rectal swabs has been used to effectively identify asymptomatic carriers of CRE.[11,13]

Risk factors for CRE colonization and infections have been reported. These include advanced age, dependent functional status, residency in a long-term care facility, invasive procedures, and recent exposure to antibiotics.[3,14,15,16,17,18] Long-term acute care (LTAC) institutions have been identified as an important reservoir for CRE in Southeast Michigan as well as in other regions.[19,20] No studies in the United States, to our knowledge, have identified risk factors for CRE colonization at the time of LTAC admission, and no studies have compared and contrasted risk factors for CRE colonization among patients being admitted to a hospital with those being admitted to an LTAC facility.

Since June 2009, patients admitted to Detroit Medical Center (DMC) who had resided in an LTAC facility in the preceding 12 months have been screened for CRE colonization via rectal cultures. During this same time period, an LTAC facility that resided within DMC screened all new admissions for CRE colonization. There were 2 main objectives of this study: to identify predictors of CRE colonization at the time of hospital or LTAC admission and to compare and contrast risk factors for colonization at the time of hospital admission with risk factors for colonization at the time of LTAC admission. Identifying the risk factors for CRE colonization at the time of admission to a healthcare institution is an important initial step toward minimizing CRE spread and improving the management of colonized and infected patients.