Risk factors for isolation of carbapenem-resistant Enterobacterales from normally sterile sites and urine

Published:December 24, 2021DOI:


      • 576 patients with urine or sterile site cultures positive for CRE were evaluated.
      • Risk factors for positive urine and sterile site cultures were compared.
      • Invasive devices and recent surgery associated with positive sterile site cultures.
      • Focusing on indwelling device care and removal may decrease CRE infection risk.


      Invasive infections caused by carbapenem-resistant Enterobacterales (CRE) are of significant concern in health care settings. We assessed risk factors for a positive CRE culture from a sterile site (invasive infection) compared to isolation from urine in a large patient cohort in Atlanta from August 2011 to December 2015.


      CRE cases required isolation, from urine or a normally-sterile site, of E. coli, Klebsiella spp., or Enterobacter spp. that were carbapenem-nonsusceptible (excluding ertapenem) and resistant to all third-generation cephalosporins tested. Risk factors were compared between patients with invasive and urinary infections using multivariable logistic regression.


      A total of 576 patients had at least 1 incident case of CRE, with 91 (16%) having an invasive infection. In multivariable analysis, the presence of a central venous catheter (OR 3.58; 95% CI: 2.06-6.23) or other indwelling device (OR 2.34; 95% CI: 1.35-4.06), and recent surgery within the last year (OR 1.81; 95% CI: 1.08-3.05) were associated with invasive infection when compared to urinary infection.


      Health care exposures and devices were associated with invasive infections in patients with CRE, suggesting that targeting indwelling catheters, including preventing unwarranted insertion or encouraging rapid removal, may be a potential infection control intervention.


      Future infection prevention efforts to decrease CRE cases in health care settings should focus on minimizing unnecessary devices.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to American Journal of Infection Control
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • CDC
        Vital signs: carbapenem-resistant Enterobacteriaceae.
        Morb Mortal Wkly Rep. 2013; 62: 165-170
        • Rhomberg PR
        • Jones RN.
        Summary trends for the Meropenem Yearly Susceptibility Test Information Collection Program: a 10-year experience in the United States (1999-2008).
        Diagn Microbiol Infect Dis. 2009; 65: 414-426
        • Thaden JT
        • Lewis SS
        • Hazen KC
        • et al.
        Rising rates of carbapenem-resistant enterobacteriaceae in community hospitals: a mixed-methods review of epidemiology and microbiology practices in a network of community hospitals in the southeastern United States.
        Infect Control Hosp Epidemiol. 2014; 35: 978-983
        • Falagas ME
        • Tansarli GS
        • Karageorgopoulos DE
        • Vardakas KZ.
        Deaths attributable to carbapenem-resistant Enterobacteriaceae infections.
        Emerg Infect Dis. 2014; 20: 1170-1175
        • Bogan C
        • Kaye KS
        • Chopra T
        • et al.
        Outcomes of carbapenem-resistant Enterobacteriaceae isolation: matched analysis.
        Am J Infect Control. 2014; 42: 612-620
        • Bartsch SM
        • McKinnell JA
        • Mueller LE
        • et al.
        Potential economic burden of carbapenem-resistant Enterobacteriaceae (CRE) in the United States.
        Clin Microbiol Infect. 2017; 23 (e49-48.e16): 48
        • 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
        • van Loon K
        • Voor In ’t Holt AF
        • Vos MC
        A systematic review and meta-analyses of the clinical epidemiology of carbapenem-resistant Enterobacteriaceae.
        Antimicrob Agents Chemother. 2018; 62: e01730-17
        • Chiotos K
        • Tamma PD
        • Flett KB
        • et al.
        Multicenter study of the risk factors for colonization or infection with carbapenem-resistant Enterobacteriaceae in children.
        Antimicrob Agents Chemother. 2017; 61: e01440-17
        • 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
        • Kofteridis DP
        • Valachis A
        • Dimopoulou D
        • et al.
        Risk factors for carbapenem-resistant Klebsiella pneumoniae infection/colonization: a case-case-control study.
        J Infect Chemother. 2014; 20: 293-297
        • 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: 809-817
        • 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: 144-150
        • 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: 398-405
        • 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: 257-265
        • Freire MP
        • Oshiro IC
        • Pierrotti LC
        • et al.
        Carbapenem-Resistant Enterobacteriaceae acquired before liver transplantation: impact on recipient outcomes.
        Transplantation. 2017; 101: 811-820
        • Borer A
        • Saidel-Odes L
        • Eskira S
        • et al.
        Risk factors for developing clinical infection with carbapenem-resistant Klebsiella pneumoniae in hospital patients initially only colonized with carbapenem-resistant K pneumoniae.
        Am J Infect Control. 2012; 40: 421-425
        • Schechner V
        • Kotlovsky T
        • Kazma M
        • et al.
        Asymptomatic rectal carriage of blaKPC producing carbapenem-resistant Enterobacteriaceae: who is prone to become clinically infected?.
        Clin Microbiol Infect. 2013; 19: 451-456
        • Reno J
        • Schenck C
        • Scott J
        • et al.
        Querying automated antibiotic susceptibility testing instruments: a novel population-based active surveillance method for multidrug-resistant gram-negative bacilli.
        Infect Control Hosp Epidemiol. 2014; 35: 336-341
      1. Performance Standards for Antimicrobial Susceptibility Testing: Twentieth Information Supplement.
        Clinical and Laboratory Standards Institute, Wayne, PA2010
        • Aleidan FAS
        • Alkhelaifi H
        • Alsenaid A
        • et al.
        Incidence and risk factors of carbapenem-resistant Enterobacteriaceae infection in intensive care units: a matched case-control study.
        Expert Rev Anti Infect Ther. 2021; 19: 393-398
        • Predic M
        • Delano JP
        • Tremblay E
        • Iovine N
        • Brown S
        • Prins C.
        Evaluation of patient risk factors for infection with carbapenem-resistant Enterobacteriaceae.
        Am J Infect Control. 2020; 48: 1028-1031
        • Guh AY
        • Bulens SN
        • Mu Y
        • et al.
        Epidemiology of carbapenem-resistant Enterobacteriaceae in 7 US communities, 2012-2013.
        JAMA. 2015; 314: 1479-1487
        • Centers for Disease C, Prevention
        Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities.
        MMWR Morb Mortal Wkly Rep. 2009; 58: 256-260