Major article

Disparity in infection control practices for

lisESOnt

Extended-spectrum b-lactamase-producingEnterobacteriaceae

ESBLCarbapenem-resistant EnterobacteriaceaeCREAdmission screening

Disease Control and Prevention, the Public Health Agency of Canada(PHAC), and others, it is not clear to what extent their recom-mendations have been implemented.12-14

We hypothesized that infection control practices for both ESBL-E and CRE vary widely among hospitals, evenwithin a single healthcare system and a dened geographic area. To test this hypothesis,we conducted a survey of infection control practices for ESBL-E andCRE in hospitals in Toronto, Canada. Our results may have impli-

Members of the Toronto ESBL Working Group: Brigette Boaretto (SouthlakeRegional Health Centre), Sheila Churilla (Markham-Stouffville Hospital), JanineDomingos (William Osler Health Centre), Shasta Gibson (Credit Valley Hospital), DrSusy Hota (University Health Network), Judy McCarten (Lakeridge Health), Chris-tine Moore (Mount Sinai Hospital), Vydia Nankoosingh (The Scarborough Hospital),Dr Daniel Ricciuto (Lakeridge Health), Dr David Richardson (William Osler HealthCentre), Dr Valerie Sales (Markham-Stouffville Hospital), Dr Alicia Sarabia (CreditValley Hospital), Dr Michael Silverman (Lakeridge Health), Dr Andrew Simor(Sunnybrook Health Sciences Centre), Arla Tomiczek (Toronto East General

Contents lists availab

American Journal of

journal homepage: w

American Journal of Infection Control 40 (2012) 836-9Hospital).Extended-spectrum b-lactamase-producing Enterobacteriaceae(ESBL-E) are globally endemic multidrug-resistant organisms.1-3

Carbapenem-resistant Enterobacteriaceae (CRE) have also becomea global concern. In Canada, the prevalence of ESBL-producingEscherichia coli is 4.3%, although higher rates have been reportedfrom Ontario (6.3%).4 Thus far, CRE are a rare occurrence in Canada,but cases, as well as transmission, of both Klebsiella pneumoniae

carbapenemase (KPC) andNew-Delhimetallo-b-lactamase (NDM-1)have been described.5-7

Despite the urgency of this problem, there is uncertaintyregarding the extent to which in-hospital transmission contributesto the overall incidence of ESBL-E compared with antibiotic use/overuse and/or community transmission (including potential foodand water borne transmission).8,9 Without clear empiric evidencesupporting specic infection control strategies, recommendationsfor ESBL-E are incorporated into general guidance on the control ofresistant gram-negative organisms.10,11 Although guidelines for thecontrol of CRE transmission have been issued by the Centers for

* Address correspondence to Matthew P. Muller, PhD, MD, St. Michaels Hospital,30 Bond Street, 4CC-North, Room 4-178, Toronto, ON, M5B 1W8, Canada.

E-mail address: MullerM@smh.ca (M.P. Muller).Conicts of interest: None to report.

0196-6553/$36.00 - Copyright 2012 by the Associadoi:10.1016/j.ajic.2011.11.008Background: There is a lack of empiric evidence regarding the optimal approach to controlling thetransmission of extended-spectrum b-lactamase-producing Enterobacteriaceae (ESBL-E) and carbapenem-resistant Enterobacteriaceae (CRE). In this context, we expect that infection control practices for theseorganisms vary widely between hospitals.Methods: A survey examining infection control practices for ESBL-E and CRE was distributed to 6academic and 9 community hospitals in Toronto, Canada.Results: All hospitals responded to the survey. Among 15 hospitals in 1 geographic area, 8 differentapproaches to the management of ESBL-E were utilized. There was wide variation in the use infectioncontrol practices including admission screening (53% and 53%), contact precautions (53% and 100%), andisolation (60% and 100%) for ESBL-E and CRE, respectively. Of hospitals performing admission screening,75% used risk factor-based screening for ESBL-E and CRE.Conclusion: Evenwithin a single geographic area, there is wide variation in infection control strategies tocontain or control ESBL-E and CRE. These results are concerning given evidence that a coordinatedapproach may be required to prevent or limit the emergence of CRE.

Copyright 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc.Published by Elsevier Inc. All rights reserved.Key Words:Christopher Lowe MDa, Kevin Katz MSc, MD a,b, AlMatthew P. Muller PhD, MD a,d,*, and the TorontoaDepartment of Laboratory Medicine and Pathobiology, University of Toronto, Toronto,bNorth York General Hospital, Toronto, Ontario, CanadacMount Sinai Hospital, Toronto, Ontario, Canadad St. Michaels Hospital, Toronto, Ontario, Canadation for Professionals in Infectionmultidrug-resistant Enterobacteriaceae

on McGeer MSc, MD a,c,BL Working Groupario, Canada

le at ScienceDirect

Infection Control

ww.aj ic journal .org

American Journal of Infection Controlcations for the emergence of CRE in Canada because a unied

Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Com(n

8Contact precautionsAll patients 3 (50.0) 5

476 (66.7) 11 (73.3) 1 (16.7) 6 (66.7) 7 (46.7)

1 (11.1) 2 (13.3) 0 (0) 1 (11.1) 1 (6.7)7 (77.8) 8 (53.3) 2 (33.3) 2 (22.2) 4 (26.7)1 (11.1) 5 (33.3) 4 (66.7) 4 (44.4) 8 (53.3)0 (0) 0 (0) 0 (0) 2 (22.2) 2 (13.3)6 (66.7) 8 (53.3) 6 (100.0) 7 (77.8) 13 (86.7)

2 (22.2) 7 (46.7) 4 (66.7) 2 (22.2) 6 (40.0)5 (55.6) 6 (40.0) 2 (33.3) 4 (44.4) 6 (40.0)2 (22.2) 2 (13.3) 0 (0) 2 (22.2) 2 (13.3)0 (0) 0 (0) 0 (0) 1 (11.1) 1 (6.7)

1 (11.1) 1 (6.7) 0 (0) 2 (22.2) 2 (13.3)1 (11.1) 2 (13.3) 1 (16.7) 2 (22.2) 3 (20.0)y

1 (11.1) 1 (6.7) 0 (0) 0 (0) 0 (0)0 (0) 0 (0) 2 (33.3) 3 (33.3) 5 (33.3)y

6 (66.7) 11 (73.3) 4 (66.7) 1 (11.1) 5 (33.3)Not yet determined 0 (0) 0 (0) 0 (0) 0 (0) 1 (11.1) 1 (6.7)

4 (44.4) 5 (33.3) 4 (66.7) 2 (22.2) 6 (40.0)3 (33.3) 4 (26.7) 0 (0) 3 (33.3) 3 (20.0)

of InContact tracingNo follow-up 1 (16.7)Screened once 1 (16.7)Patients with increased risk of transmitting 3 (50.0)Private rooms 2 (33.3)Cohorting 5 (83.3)Discontinuation of precautionsAfter 1 negative specimen (from the original positive site) 1 (16.7)After 3 negative screens separated by 1 week 1 (16.7)Until discharge 4 (66.7)Not yet determined 0 (0)

Positives agged in the clinical database 2 (33.3)Admission screeningNo screening 5 (83.3)Risk factor-based screening 1 (16.7)Universal screening 0 (0)Not yet determined 0 (0)

Point prevalence surveysNot performed 0 (0)Periodically on all units 1 (16.7)Periodically on units with high incidence 0 (0)New colonized patient identied 0 (0)Only in outbreak situations 5 (83.3)Table 1Infection control practices for ESBL-E and CRE

Academic(n 6), n (%)

Written infection control policies 2 (33.3)

C. Lowe et al. / American Journalapproach to CRE may be required to prevent or delay the emer-gence of CRE.9,15

METHODS

As part of an ongoing study examining the incidence of ESBL-Ecolonization and infection in Toronto area hospitals, 15 hospitalsparticipated in a survey to determine current infection control prac-tices related to the control of ESBL-E and CRE. All academic hospitalsparticipated, and community hospitals of varying sizes andgeographic locations in Toronto agreed to participate. The surveygathered informationonhospital characteristicsand infectioncontrolpractices including the use of active screening, contact precautions,isolation, cohorting, and laboratory-based surveillance practices forESBL-E and CRE identication (Supplementary Data, available onlineonly). Contact precautions were dened as the use of gowns andgloves for patient contact. The survey was addressed to the profes-sional most responsible for ESBL-E or CRE control at each institution.ResearchEthics Board approvalwasobtained at all participating sites.

RESULTS

Thirteen of 15 hospitals completed the survey betweenNovember 2010 and April 2011; 2 hospitals (C5 and C6) respondedafter the initial April 2011 deadline and completed the surveyretrospectively. This was after the release of the PHAC guidance oncontrol of CRE in Canadian health care settings in November 2010.12

For academic hospitals (A1, A2, A3, A4, A5, A6), mean beds perhospital were 344 (range, 136-460), mean admissions per year

Screened twice separated by 1 week 1 (16.7) 2Only screened if actively soiling 3 (50.0) 0Not yet determined 0 (0) 0

NOTE. Unless otherwise stated, the Table refers to infected and colonized patients.*Hospital C7 utilized contact precautions and isolation for infected but not colonized payHospital A2 cited point prevalence surveys periodically on all units and if a new coloniESBL-E CRE

munity9), n (%)

Total(n 15), n (%)

Academic(n 6), n (%)

Community(n 9), n (%)

Total(n 15), n (%)

(88.9) 10 (66.7) 2 (33.3) 3 (33.3) 5 (33.3)

(55.6) 8 (53.3) 6 (100.0) 9 (100.0)* 15 (100.0)(44.4) 7 (46.7) 0 (0.0) 0 (0) 0 (0)(77.8) 9 (60.0) 6 (100.0) 9 (100.0)* 15 (100.0)

fection Control 40 (2012) 836-9 837were 17,300 (range, 4,531-26,317), and mean inpatient days permonth were 10,655 (range, 3,375-17,627). At community hospitals(C1, C2, C3, C4, C5, C6, C7, C8, C9), mean beds per hospital were 401(range, 208-703), mean admissions per year were 20,751 (range,11,713-45,285), and mean inpatient days per month were 10,618(range, 5,220-23,221). Respondents included infection controlprofessionals (8/15, 53%), infection control physicians (6/15, 41%),and a microbiologist (1/15, 7%).

Whereas all hospitals describedhavingwrittenpolicies for gram-positive antibiotic resistant organisms (ie, methicillin-resistantStaphylococcus aureus, vancomycin-resistant Enterococcus), fewerhad policies for ESBL-E (67%, 10/15) or CRE (5/15, 33%) (Table 1).

(22.2) 3 (20.0) 2 (33.3) 3 (33.3) 5 (33.3)(0) 3 (20.0) 0 (0) 0 (0) 0 (0)(0) 0 (0) 0 (0) 1 (11.1) 1 (6.7)

tients.zed patient was identied.

Table 2Risk factors considered in hospitals utilizing risk factor based admission screening

Risk factor

Hospitals

A2 C3 C4 C5 C6 C7

Admission to a unit or service X* Xy Xy Xz

Previous ESBL-E or exposure to ESBL-E X XPrevious hospitalization X X XPrevious hospitalization outside of Canada X X X X X XResident of a long-term care facility or

rehabilitation centerX X

Patient at increased risk of environmentalcontaminationx

X X

*Intensive care unit/neonatal intensive care unit, medical ward, or surgical wardwith risk factors (hospitalized within 2 years, transferred from a nursing home, orprevious history of an antibiotic-resistant organism).yIntensive care unit.zIntensive care unit or neonatal intensive care unit.xIncontinent of stool, diarrhea and draining wounds.

iseen

Toro

of InESBL-E practiceswere based on evidence (4), local epidemiology (4),or both (4). The remaining hospitals based practices on peers (2) orwere unsure of their rationale (1). The rationale for CRE policies wasnot addressed because the recent release of Canadian guidelinesafforded hospitals limited time to adjust their policies beforeresponding to the survey.

Table 1 summarizes the infection control practices of hospitalssurveyed. Eight hospitals initiated contact precautions for allidentied ESBL-E patients, and 7 instituted precautions only forpatients/situations thought to be a high risk for transmission. Thiswas dened as fecal/urinary incontinence, diarrhea, or drainingwounds (4); intensive care unit patients (2); or intensive care unitpatients with 1 of the aforementioned risk factors (1). Threemethods of admission screening were reported: no screening, risk-factor based, and universal. Among hospitals instituting screening,

Yes

AdmScr

8 Hospitals

Hospitals:C2,C9

Contact Precautions

(All)

Isolation

Cohort

Hospitals: A2,C5,C6

Contact Precautions

(All)

Isolation

No Cohorting

Hospital: C7

Contact Precautions

(HR)

No Isolation

Cohort

Hospitals: C3,C4

Contact Precautions

(HR)

Isolation

Cohort

Fig 1. Diversity in infection control practices for ESBL-E in

C. Lowe et al. / American Journal8387 of 8 were from the community. Risk factors used for screening byeach hospital are listed in Table 2. International hospitalizationwascited as a risk factor by all 6 hospitals. All 8 hospitals conductingscreening utilized rectal swabs with some also performing urineculture (1/8) or wound (3/8) and invasive device (3/8) swabs.

The practice variation is only partially appreciated by reviewingindividual control strategies separately; if one considers infectioncontrol bundles, the true extent of variation in practice for ESBL-Ecan be better appreciated as 8 different approaches were used atthe 15 surveyed hospitals (Fig 1).

Similarly, there were a broad range of practices for CRE.However, in general, hospitals appeared more likely to utilizecontact precautions for all patients, isolate colonized/infectedpatients, andmaintain precautions until discharge for patients withCRE as comparedwith ESBL-E (Table 1). Seven hospitals performingadmission screening for ESBL-E also adopted admission screeningfor CRE, largely from the same specimens, whereas the remaininghospital (C6) performing screening for ESBL-E had yet to developprotocols for screening of CRE. Hospital A3 did not screen for ESBL-E but adopted CRE screening, although only for patients returningfrom endemic areas.

Routine point prevalent surveys were infrequently performedfor either ESBL-E or CRE and were used primarily for case ndingduring identied outbreaks rather than for routine surveillance.All laboratories serving the 15 surveyed hospitals tested for andreported the presence of KPC-producing Enterobacteriaceae, and14 of 15 reported the capability to identify NDM-1 producingEnterobacteriaceae.

DISCUSSION

Despite growing concerns regarding the spread of ESBL (eg,CTX-M-1516), serine carbapenemases (eg, KPC17), and metallo-b-lactamases (eg, NDM-118), the optimal method to prevent noso-comial spread of these organisms is unknown. During outbreaks,infection control intervention bundles and coordinated efforts atregional and national levels have been shown to be effective.15

However, less is known about the appropriate approach tocontrolling ESBL-E in nonoutbreak settings,19 while the economicand resource implications of implementing such policies areconsiderable.20,21

No

sion ing

7 Hospitals

Hospitals: A3,C1

Contact Precautions

(All)

Isolation

Cohort

Hospital: A1

Contact Precautions

(All)

No Isolation

Cohort

Hospitals: A4,A5,A6

Contact Precautions

(HR)

No Isolation

Cohort

HospitalC8

Contact Precautions

(HR)

No Isolation

No Cohorting

nto, Canada. *HR, individuals at high risk of transmission.

fection Control 40 (2012) 836-9Harris et al suggested that, in the absence of empiric evidence,decisions regarding the use of screening or contact precautions forthe control of drug-resistant gram-negative bacteria should bebased on the relative proportion of resistance attributable toperson-to-person transmission compared with the proportionresulting from antibiotic use on an organism specic basis.8

Transmission of ESBL K pneumoniae and E coli has been demon-strated.22-24 Whereas there is less experience with CRE, the ex-pected mode of transmission should be similar because both areplasmid-encoded b-lactamases in Enterobacteriaceae. The primarydifference between ESBL-E and CRE is clinical: for patients withsevere infections because of CRE, available antibiotic therapy maybe suboptimal and mortality higher.25

In a 2002 survey of Ontario hospitals, 70% of respondentsrequired contact precautions for some or all patients colonizedwith ESBL-E and 48% required isolation as compared with 100% and60% in this survey.26 Similarly, in 2007 survey of Canadian hospitals,only 1 of 26 hospitals performed universal or risk factor-basedscreening for ESBL-E as compared with 53% in our survey.27

Although these surveys are not directly comparable, they demon-strate the potential for variation in infection control practices forESBL-E across geographical regions while suggesting an evolutiontoward a more standardized approach, at least for contactprecautions.

Point prevalence surveys are recommended by the Centers forDisease Control and Prevention and PHAC if an unrecognized case

C. Lowe et al. / American Journal of Infection Control 40 (2012) 836-9 839of CRE is discovered on retrospective review of microbiologyrecords over the previous 6 to 12months.12,13 The variability seen inimplementation of prevalence screens may be reective of therelatively low incidence of CRE in Toronto.4,6,7 However, our surveydemonstrates that adoption of these new guidelines is still in itsearly stages, with 2 community hospitals not planning to performprevalence screening and 1 with protocols still to be determined.

Based on the clinical importance of multidrug resistance,particularly to carbapenems, it appears rational to take an early andcoordinated approach to prevent CRE from becoming endemic.14,15

Guidelines for CRE appear to be moving in this direction asEuropean guidelines recommend active surveillance, whereasCanadian and US guidelines suggest surveillance to detect asymp-tomatic patients when hospital transmission is identied.12-14

Whereas our survey conrms that many hospitals are imple-menting these approaches, practices continue to vary widely andfall short of complete implementation at most facilities.

Our study has several limitations. It was conducted in a singlegeographic area, and its generalizability may be limited. However,15 diverse academic and community hospitals participated, and theresponse rate was high. Our results demonstrate the potential forwidespread practice variation even within a single health caresystem and geographic area when evidence and guidelines arelacking. The study results, particularly for CRE, must be interpretedcautiously because the study was conducted only shortly afterCanadian guidance for CRE was released, and hospitals may be inthe process of developing or modifying their practices with respectto CRE. Finally, because of the low prevalence of CRE in Toronto,there is limited experience managing CRE infected/colonizedpatients from an infection control perspective, and approaches arelikely to change as institutions begin to face more clinical cases.

Although ESBL-E emerged over 25 years ago, a lack of evidenceand evidence-based guidelines has led to a diverse range of infec-tion control practices that may in part be responsible for theincreasing incidence of ESBL-E. This is particularly concerning inthe face of the threat of CRE and pan-drug-resistant gram-negativebacteria. Guidance for CRE in Canada has recently been developed,but the document cites a lack of evidence in important areas such asactive screening and discontinuation of contact precautions.12

Research is urgently needed to identify the optimal infectioncontrol approaches to control both ESBL-E and CRE transmission;while this evidence base evolves, it may be prudent to takea coordinated approach to controlling CRE.

SUPPLEMENTARY DATA

Supplementary data related to this article can be found online atdoi:10.1016/j.ajic.2011.11.008.

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Disparity in infection control practices for multidrug-resistant EnterobacteriaceaeMethodsResultsDiscussionSupplementary dataReferences