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Infection Control & Hospital Epidemiology


associated transmission. The CDC recommends CRE colonization screening in limited instances (eg, patients with recent interna- tional hospitalization),2 but most US hospitals do not perform routine CRE colonization screening. Evaluating patients admitted to a MICU and a solid organ transplant unit, we found that CRE colonization a unit admission was infrequent (3.9%), and only 21% of CREs were carbapenemase producers. These findings are similar to the proportions of CRE (3.1%) and CP-CRE (32% of CRE) among clinical isolates reported to the National Healthcare Safety Network in 2015 and 2017, respectively.6 Most CRE- and CP-CRE–colonized patients were not on


contact precautions at unit admission. Of particular concern, only 1 CP-CRE carrier (2 encounters) had a known history of CRE, which may reflect a true lack of prior positive cultures or incomplete data from institutions outside the Johns Hopkins Health System. Moreover, no CP-CRE–colonized patients were recently hospitalized internationally. Our findings suggest that many CP-CRE carriers, and the potential they pose for onward transmission, are missed for infection control interventions under existing institutional protocols. Although most CRE-colonized patients were not on contact


precautions at unit admission, CRE- and CP-CRE–colonized patients were still 2–3 times more likely than noncarriers to be on contact precautions. The most common indications were histories of VRE, MRSA, and/or MDRGNs. These findings are consistent with the overlap in risk factors (eg, antibiotic use and exposure to high- risk healthcare facilities) between CRE and other drug-resistant organisms.7–9 Moreover, an MDRGN history was associated with colonization with CRE, but not CP-CRE, which may reflect differing acquisition pathways between CRE types.10 Identifying additional risk factors for CRE colonization, particularly among patients who lack MDRGN histories, could enhance targeted screening efforts. This study has several limitations. This was a single-center


study with some missing swabs, and our results should be vali- dated in other cohorts. In addition, contact precautions policies vary among hospitals, which could impact generalizability of these findings. We only ascertained contact precaution status at unit admission, and patient status may have changed during unit stay. Screening method may also affect organism recovery, although CDC guidance endorses perirectal swabs for CRE surveillance.2 In summary, most CRE-colonized patients who participated in


this study were not on contact precautions at unit admission. Given low colonization prevalence, further research on CRE colonization risk factors among US inpatients is necessary to develop algorithms for identifying and screening patients at greatest risk of harboring CRE.


Acknowledgments. We would like to thank Verna Scheeler, Michael Anderson, Dina Khamash, and Sean Thompson for their assistance with study coordination, and data collection, and validation, as well as Belita Opene, Shawna Lewis, and Krizia Chambers for their work processing surveillance cultures. We would also like to thank members of the JHU Clinical Micro- biology Laboratory staff for helping with the collection of surveillance swabs for the study.


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Financial support. This work was supported by the Centers for Disease Control (CDC) Prevention Epicenters Program (CDC grant no. 1U54CK000447), by the CDC MIND-Healthcare Program (grant no. 1U01CK000536), by the Agency for Healthcare Research and Quality (AHRQ grant no. R36HS025089), and by The Sherrilyn and Ken Fisher Center for Environmental Infectious Diseases.


Conflicts of interest. Dr Milstone reports personal fees from Becton Dick- inson Diagnostics, Dr Rock reports grant support from The Clorox Company, and Dr Tamma reports grants from Merck, all outside the scope of the sub- mitted work. Dr Simner reports grants and personal fees from Accelerate Diagnostics, grants from BD Diagnostics, grants from bioMerieux, grants from Check-Points Diagnostics, grants from Hardy Diagnostics, personal fees from Roche Diagnostics, personal fees from Opgen, and personal fees from Oxford Nanopore, all outside the scope of the submitted work. All other authors report no potential conflicts of interest.


References


1. Antibiotic resistance threats in the United States, 2013. Centers for Disease Control and Prevention website. https://www.cdc.gov/drugresis- tance/threat-report-2013/index.html. Published 2013. Accessed Septem- ber 5, 2018.


2. Facility Guidance for Control of Carbapenem-resistant Enterobacteriaceae (CRE)— November 2015 Update CRE Toolkit. Centers for Disease Control and Prevention website. https://www.cdc.gov/hai/organisms/cre/ cre-toolkit/index.html. Published 2015. Accessed September 5, 2018.


3. Simner PJ, Martin I, Opene B, Tamma PD, Carroll KC, Milstone AM. Evaluation of multiple methods for the detection of gastrointestinal colonization of carbapenem-resistant organisms from rectal swabs. J Clin Microbiol 2016;54:1664–1667.


4. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing, 28th ed., Supplement M100S. Wayne, PA: CLSI; 2018.


5. Pierce VM, Simner PJ, Lonsway DR, et al. Modified carbapenem inactivation method for phenotypic detection of carbapenemase production among Enterobacteriaceae. J Clin Microbiol 2017; 55:2321–2333.


6. Woodworth KR, Walters MS, Weiner LM, et al. Vital signs: containment of novel multidrug-resistant organisms and resistance mechanisms— United States, 2006–2017. Morb Mortal Wkly Rep 2018; 67: 396–401.


7. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis 2017;215 Suppl 1:S28–S36.


8. 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.


9. Simner PJ, Goodman KE, Carroll KC, Harris AD, Han JH, Tamma PD. Using patient risk factors to identify whether carbapenem-resistant Enterobacteriaceae infections are caused by carbapenemase-producing organisms. Open Forum Infect Dis 2018; 5: ofy094–ofy094.


10. Goodman KE, Simner PJ, Tamma PD, Milstone AM. Infection control implications of heterogeneous resistance mechanisms in carbapenem- resistant Enterobacteriaceae (CRE). Expert Rev Anti-infect Ther 2016;14:95–108.


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