Dangel, Marc

Frei, Reno

Stranden, Anne

Tschudin-Sutter, Sarah

Widmer, Andreas Franz

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INFECTION CONTROL AND HOSPITAL EPIDEMIOLOGY NOVEMBER 2 0 1 2 , VOL. 3 3 , NO. 11 R E S E A R C H B R I E F S Sites of Colonization with Extended-Spectrum jS-Lactamases (ESBL)-Producing Enterobacteriaceae: The Rationale for Screening Extended-spectrum ^-lactamases (ESBL)-producing organ-isms have emerged as one of the most important multi-resistant pathogens in hospitals.1 They are spreading in the community worldwide, mainly causing urinary tract infec-tions.2 Infections caused by ESBL-producing organisms are associated with poor outcomes, reduced rates of clinical re-sponse, longer hospital stays, and greater expenses.3 Author-ities at the Centers for Disease Control and Prevention (CDC) recommend performance of active surveillance cultures from patients in populations at risk, for example, patients in in-tensive care, burn, bone marrow or stem cell transplant, and oncology units, patients transferred from facilities known to have high prevalence rates, roommates of colonized or in-fected persons, and patients known to have been previously infected or colonized.4 Despite the CDC's recommendation, standardized screening schemes for carriage of multiresistant gram-negative pathogens, including ESBL-producing Enter-obacteriaceae, are lacking. Knowledge of the body sites most commonly colonized with these pathogens is of great im-portance to inform appropriate and cost-effective screening procedure policies. The aim of this study, therefore, was to determine the frequency of colonization for each body site. University Hospital Basel is an 855-bed tertiary care center with 5 intensive care units (ICUs). The study was approved by the local ethics committee as part of the quality assurance program. From January 2008 to December 2010, all consec-utive adult patients in whom an ESBL-producing Entero-bacteriaceae was detected in any clinical specimen routinely taken for suspected infection were included in the study. Pa-tients were screened for colonization by examination of urine samples and rectal, inguinal, and throat swabs. Specimens were cultured onto the chromogenic BBL CHROMagar Ori-entation medium (Becton Dickinson) or chromID ESBL me-dium (bioMerieux). No screening was performed if patients were receiving antibiotics active against ESBL-producing En-terobacteriaceae, as this may have led to false-negative screen-ing results. Patients who did not receive screening of all 4 body sites (urine, rectum, groin, and throat) were excluded. For microbiological detection of ESBL producers, the guidelines of the Clinical and Laboratory Standards Institute were followed.5 The frequency of detection was calculated for each site. The proportion of CTX-M genotype was deter-mined by polymerase chain reaction using the degenerative oligonucleotides CTX-F2 (5'-GTGCAGYACCAGTAARGT-KATGG-3') and CTX-M-R1 (5'-CDCMGCT GCCGGTYT-TATC-3').6'7 Sequencing of amplicons was performed with an ABI 3130 Genetic Analyzer (Applied Biosystems). ESBL-producing strains were detected in 204 patients, of whom 133 (65.2%) had all 4 sites swabbed and 58 (28.4%) did not undergo swabbing because they were under treatment with a systemic antibiotic with activity against ESBL-producing pathogens or had already been discharged or transferred to another hospital. The remaining 13 patients (6.4%) were swabbed in 1 or 2 of the 4 sites but not in all 4 because of noncompliance with written instructions. Of the 133 patients swabbed at all 4 sites, 60 (45.1%) were hospitalized on the medical wards, 44 (33.1%) on the general surgical wards, 17 (12.8%) on the gynecology department, 8 (6.0%) on the urol-ogy department, 2 (1.5%) on the neurology department, and 2 (1.5%) on the bone marrow transplant unit. Patients' me-dian age was 66 years (range, 18-93), with a female predom-inance of 60.2% (80/133 patients). Escherichia coli accounted for the majority of all ESBL-producing Enterobacteriaceae (85.7%, 114/133), followed by Klebsiella pneumoniae (13.5%, 18/133) and Citrobacter freun-dii (0.8%, 1/133). The CTX-M genotype was detected in 109 of 133 patients (82.0%), accounting for 85.1% (97/114) of all ESBL-producing E. coli and 66.7% (12/18) of ESBL-producing K. pneumoniae isolates. ESBL-producing Enterobacteriaceae were most commonly recovered from urine samples, which were positive in 82.7% (110/133) of patients, followed by rectal swabs (69.2%, 92/ 133), skin swabs of the groin (35.3%, 47/133), and throat swabs (12.8%, 17/133; Table 1). Urine and the rectum were most commonly colonized with ESBL-producing Enterobacteriaceae (82.7% and 69.2%, re-spectively). Our finding that urine was the only positive screening site in 24.1% of our patients provides strong evi-dence that urine samples should be included in a standardized screening regimen. The CDC recommends performance of active surveillance cultures for patients from populations at risk,4 as patients colonized with ESBL-producing Enterobacteriaceae are at in-creased risk to develop invasive infections with these path-ogens. A 5-fold increased risk for invasive infection with an ESBL-producing Enterobacteriaceae for ICU patients with rectal colonization has been described,8 and Reddy et al9 found that 8.5% of patients colonized with ESBL-producing Enterobacteriaceae developed subsequent bloodstream infec-tions with these pathogens. The authors therefore concluded that active surveillance for ESBL-producing Enterobacteria-ceae may have important clinical implications for empiric treatment of febrile episodes. In these 2 studies, however, screening for colonization was performed only by collection of rectal swabs. More than 20% of ESBL-positive patients may remain undetected with this approach, which does not include screening of the urine. https:/www.cambridge.org/core/terms. https://doi.org/10.1086/668027Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 20:16:50, subject to the Cambridge Core terms of use, available atRESEARCH BRIEFS I I 7 1 TABLE 1. Overview of the Different Colonization Patterns Detected in 133 Patients No. of Pattern \ patients (%) 1 colonization site Urine Rectum Groin Throat 2 colonization sites Urine, rectum Urine, groin Urine, throat Rectum, groin Rectum, throat Groin, throat 3 colonization sites Urine, rectum, groin Urine, rectum, throat Urine, groin, throat Rectum, groin, throat 4 colonization sites Urine, rectum, groin, throat Site totals Patients with colonization of the Patients with colonization of the Patients with colonization of the urine rectum groin Patients with colonization of the throat 32 (24.1) 11 (8.3) 1 (0.7) 1 (0.7) 38 (28.6) 5 (3.8) 1 (0.7) 6 (4.6) 1 (0.7) 0 (0.0) 23 (17.3) 2 (1.5) 1 (0.7) 3 (2.3) 8 (6.0) 110 (82.7) 92 (69.2) 47 (35.3) 17 (12.8) The high percentage of the CTX-M genotype of ESBL-producing Enterobacteriaceae detected in our study reflects the worldwide trend of the spread of these multiresistant pathogens to the community.10 Future screening strategies may have to take this expanding epidemiology into account. Important limitations of our study are its observational design, its being conducted at a single center, and the small sample size, limiting generalizability. Only hospitalized pa-tients with detection of ESBLs in any clinical specimen rou-tinely taken for suspected infection and not receiving anti-biotics active against ESBL-producing Enterobacteriaceae at the time of swabbing were included, so the results cannot necessarily be extrapolated to an outpatient setting or to healthy individuals. We conclude that a standardized screening regimen for ESBL-producing Enterobacteriaceae should include both urine samples and rectal swabs. ACKNOWLEDGMENTS Financial support. University Hospital Basel funded in part the microbio-logical analyses of the samples as part of the quality improvement program. No other funding, in particular no commercial funding, was received for the study. Potential conflicts of interest. All authors report no conflicts of interest relevant to this article. All authors submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and the conflicts that the editors consider relevant to this article are disclosed here. Sarah Tschudin-Sutter, MD;1 Reno Frei, MD;2 Marc Dangel, MPH;1 Anne Stranden, PhD;1 Andreas Franz Widmer, MD, MSc1 Affiliations: 1. Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, Basel, Switzerland; 2. Division of Clinical Micro-biology, University Hospital Basel, Basel, Switzerland. Address correspondence to Professor Andreas E Widmer, MD, MSc, Di-vision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, Petersgraben 4, CH-4031 Basel, Switzerland (widmera@uhbs.ch). Received March 30, 2012; accepted June 3, 2012; electronically published September 21, 2012. Presented in part: 21st European Congress of Clinical Microbiology and Infectious Diseases (ECCMID); Milan, Italy; May 2011. Infect Control Hosp Epidemiol 2012;33(11):1170-1171 © 2012 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2012/3311-0019$15.00. DOI: 10.1086/668027 R E F E R E N C E S 1. Peleg AY, Hooper DC. Hospital-acquired infections due to gram-negative bacteria. N Engl J Med 2010;362(19):1804-1813. 2. Pitout JDD, Laupland KB. Extended-spectrum /3-lactamase-producing Enterobacteriaceae: an emerging public-health con-cern. Lancet Infect Dis 2008;8(3):159-166. 3. Lautenbach E, Patel JB, Bilker WB, Edelstein PH, Fishman NO. Extended-spectrum /3-lactamase-producing Escherichia coli and Klebsiella pneumoniae: risk factors for infection and impact of resistance on outcomes. Clin Infect Dis 2001;32(8):1162-1171. 4. Siegel JD, Rhinehart E, Jackson M, Chiarello L; and the Health-care Infection Control Practices Advisory Committee. 2007 guideline for isolation precautions: preventing transmission of infectious agents in healthcare settings, http://www.cdc.gov /hicpac/pdf/isolation/isolation2007.pdf. 5. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing: Eighteenth In-formational Supplement. Wayne, PA: CLSI, 2008. CLSI document M100-S18. 6. Bonnet R. 2004. Growing group of extended-spectrum /?-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 2004;48(1):1-14. 7. Xu L, Ensor V, Gossain S, Nye K, Hawkey P. Rapid and simple detection of WaCTX_M genes by multiplex PCR assay. / Med Mi-crobiol 2005;54(12):1183-1187. 8. Christiaens G, Ciccarella Y, Damas P, et al. Prospective survey of digestive tract colonization with Enterobacteriaceae that pro-duce extended-spectrum /3-lactamases in intensive care units. / Hosp Infect 2006;62(3):386-388. 9. Reddy P, Malczynski M, Obias A, et al. Screening for extended-spectrum /3-lactamase-producing Enterobacteriaceae among high-risk patients and rates of subsequent bacteremia. Clin Infect Dis 2007;45(7):846-852. 10. Pitout JDD, Nordmann P, Laupland KB, Poirel L. Emergence of Enterobacteriaceae producing extended-spectrum (3-lacta-mases (ESBLs) in the community. J Antimicrob Chemother 2005; 56(l):52-59. https:/www.cambridge.org/core/terms. https://doi.org/10.1086/668027Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 20:16:50, subject to the Cambridge Core terms of use, available at

Sites of Colonization with Extended-Spectrum β-Lactamases (ESBL)-Producing Enterobacteriaceae: The Rationale for Screening

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