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Provider Role in Transmission of Carbapenem-Resistant Enterobacteriaceae

  • Marika E. Grabowski (a1), Hyojung Kang (a2), Kristen M. Wells (a1), Costi D. Sifri (a3), Amy J. Mathers (a3) and Jennifer M. Lobo (a1)...



We sought to evaluate the role healthcare providers play in carbapenem-resistant Enterobacteriaceae (CRE) acquisition among hospitalized patients.


A 1:4 case-control study with incidence density sampling.


Academic healthcare center with regular CRE perirectal screening in high-risk units.


We included case patients with ≥1 negative CRE test followed by positive culture with a length of stay (LOS) >9 days. For controls, we included patients with ≥2 negative CRE tests and assignment to the same unit set as case patients with a LOS >9 days.


Controls were time-matched to each case patient. Case exposure was evaluated between days 2 and 9 before positive culture and control evaluation was based on maximizing overlap with the case window. Exposure sources were all CRE-colonized or -infected patients. Nonphysician providers were compared between study patients and sources during their evaluation windows. Dichotomous and continuous exposures were developed from the number of source-shared providers and were used in univariate and multivariate regression.


In total, 121 cases and 484 controls were included. Multivariate analysis showed odds of dichotomous exposure (≥1 source-shared provider) of 2.27 (95% confidence interval [CI], 1.25–4.15; P=.006) for case patients compared to controls. Multivariate continuous exposure showed odds of 1.02 (95% CI, 1.01–1.03; P=.009) for case patients compared to controls.


Patients who acquire CRE during hospitalization are more likely to receive care from a provider caring for a patient with CRE than those patients who do not acquire CRE. These data support the importance of hand hygiene and cohorting measures for CRE patients to reduce transmission risk.

Infect Control Hosp Epidemiol 2017;38:1329–1334


Corresponding author

Address correspondence to Jennifer M. Lobo, PhD, 1300 Jefferson Park Avenue, PO Box 800717, Charlottesville, VA 22908 (


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1. Magill, SS, Edwards, JR, Bamberg, W, et al. Multistate point-prevalence survey of health care–associated infections. N Engl J Med 2014;370:11981208.
2. Umscheid, CA, Mitchell, MD, Doshi, JA, Agarwal, R, Williams, K, Brennan, PJ. Estimating the proportion of healthcare-associated infections that are reasonably preventable and the related mortality and costs. Infect Control Hosp Epidemiol 2011;32:101114.
3. Allegranzi, B, Pittet, D. Role of hand hygiene in healthcare-associated infection prevention. J Hosp Infect 2009;73:305315.
4. Zawacki, A, O’Rourke, E, Potter-Bynoe, G, Macone, A, Harbarth, S, Goldmann, D. An outbreak of Pseudomonas aeruginosa pneumonia and bloodstream infection associated with intermittent otitis externa in a healthcare worker. Infect Control Hosp Epidemiol 2004;25:10831089.
5. Moolenaar, RL, Crutcher, JM, San Joaquin, VH, et al. A prolonged outbreak of Pseudomonas aeruginosa in a neonatal intensive care unit did staff fingernails play a role in disease transmission? Infect Control Hosp Epidemiol 2000;21:8085.
6. US Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013. Centers for Disease Control and Prevention, US Department of Health and Human Services; 2013.
7. Ben-David, D, Kordevani, R, Keller, N, et al. Outcome of carbapenem resistant Klebsiella pneumoniae bloodstream infections. Clin Microbiol Infect 2012;18:5460.
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;29:10991106.
9. Tracking CRE. US Centers for Disease Control and Prevention website. Updated 2017. Accessed September 25, 2017.
10. Summary of state CRE reporting requirements. Association for Professionals in Infection Control and Epidemiology website. Published 2013. Accessed September 25, 2017.
11. Most hospitals aren’t required to report superbug outbreaks. Should they be? Advisory Board Web site. Updated 2015. Accessed September 25, 2017.
12. U.S. Centers for Disease Control and Prevention. Facility guidance for control of carbapenem-resistant Enterobacteriaceae (CRE). November 2015 Update - CRE Toolkit. 2015.
13. Enfield, KB, Huq, NN, Gosseling, MF, et al. Control of simultaneous outbreaks of carbapenemase-producing enterobacteriaceae and extensively drug-resistant Acinetobacter baumannii infection in an intensive care unit using interventions promoted in the Centers for Disease Control and Prevention 2012 carbapenemase-resistant Enterobacteriaceae toolkit. Infect Control Hosp Epidemiol 2014;35:810817.
14. Correa, L, Martino, MDV, Siqueira, I, et al. A hospital-based matched case–control study to identify clinical outcome and risk factors associated with carbapenem-resistant Klebsiella pneumoniae infection. BMC Infect Dis 2013;13:1.
15. 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;37:12191225.
16. 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.
17. Ray, MJ, Lin, MY, Weinstein, RA, Trick, WE. Spread of carbapenem-resistant Enterobacteriaceae among Illinois healthcare facilities: the role of patient sharing. Clin Infect Dis 2016;63:889893.
18. Mathers, AJ, Poulter, M, Dirks, D, Carroll, J, Sifri, CD, Hazen, KC. Clinical microbiology costs for methods of active surveillance for Klebsiella pneumoniae carbapenemase–producing Enterobacteriaceae. Infect Control Hosp Epidemiol 2014;35:350355.
19. Mathers, AJ, Hazen, KC, Carroll, J, et al. First clinical cases of OXA-48-producing carbapenem-resistant Klebsiella pneumoniae in the United States: the “menace” arrives in the new world. J Clin Microbiol 2013;51:680683.
20. Lewis, JD, Bishop, M, Heon, B, Mathers, AJ, Enfield, KB, Sifri, CD. Admission surveillance for carbapenamase-producing Enterobacteriaceae at a long-term acute care hospital. Infect Control Hosp Epidemiol 2013;34:832834.
21. Carbapenem-resistant Enterobacteriaceae in healthcare settings. Centers for Disease Control and Prevention website. Updated 2016. Accessed February 22, 2016.
22. Stone, SP, Fuller, C, Savage, J, et al. Evaluation of the national Cleanyourhands campaign to reduce Staphylococcus aureus bacteraemia and Clostridium difficile infection in hospitals in England and Wales by improved hand hygiene: four year, prospective, ecological, interrupted time series study. BMJ 2012;344:e3005.
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