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pdfManagement of
Multidrug-Resistant
Organisms In
Healthcare Settings,
2006
Jane D. Siegel, MD; Emily Rhinehart, RN MPH CIC; Marguerite Jackson, PhD; Linda
Chiarello, RN MS; the Healthcare Infection Control Practices Advisory Committee
Acknowledgement:
The authors and HICPAC gratefully acknowlege Dr. Larry Strausbaugh for his many contributions
and valued guidance in the preparation of this guideline.
1
Healthcare Infection Control Practices Advisory Committee (HICPAC):
Chair
Patrick J. Brennan, MD
Professor of Medicine
Division of Infectious Diseases
University of Pennsylvania Medical School
Executive Secretary
Michael Bell, MD
Division of Healthcare Quality Promotion
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Members
BRINSKO, Vicki L., RN, BA
Infection Control Coordinator
Vanderbilt University Medical Center
DELLINGER, E. Patchen., MD
Professor of Surgery
University of Washington School of
Medicine
ENGEL, Jeffrey, MD
Head General Communicable Disease Control
Branch
North Carolina State Epidemiologist
GORDON, Steven M., MD
Chairman, Department of Infections Diseases
Hospital Epidemiologist
Cleveland Clinic Foundation
Department of Infectious Disease
HARRELL, Lizzie J., PhD, D(ABMM)
Research Professor of Molecular Genetics,
Microbiology and Pathology
Associate Director, Clinical Microbiology
Duke University Medical Center
O’BOYLE, Carol, PhD, RN
Assistant Professor, School of Nursing
University of Minnesota
PEGUES, David Alexander, MD
Division of Infectious Diseases
David Geffen School of Medicine at UCLA
PERROTTA, Dennis M. PhD., CIC
Adjunct Associate Professor of Epidemiology
University of Texas School of Public Health
Texas A&M University School of Rural Public
Health
PITT, Harriett M., MS, CIC, RN
Director, Epidemiology
Long Beach Memorial Medical Center
RAMSEY, Keith M., MD
Professor of Medicine
Medical Director of Infection Control
The Brody School of Medicine at East Carolina
University
SINGH, Nalini, MD, MPH
Professor of Pediatrics
Epidemiology and International Health
The George Washington University Children’s National
Medical Center
STEVENSON, Kurt Brown, MD, MPH
Division of Infectious Diseases
Department of Internal Medicine
The Ohio State University Medical Center
SMITH, Philip W., MD
Chief, Section of Infectious Diseases
Department of Internal Medicine
University of Nebraska Medical Center
HICPAC membership (past)
Robert A. Weinstein, MD (Chair)
Cook County Hospital
Chicago, IL
Jane D. Siegel, MD (Co-Chair)
University of Texas Southwestern Medical Center
Dallas, TX
Michele L. Pearson, MD
(Executive Secretary)
Centers for Disease Control and Prevention
Atlanta, GA
Raymond Y.W. Chinn, MD
Sharp Memorial Hospital
San Diego, CA
Alfred DeMaria, Jr, MD
Massachusetts Department of Public Health
Jamaica Plain, MA
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James T. Lee, MD, PhD
University of Minnesota
Minneapolis, MN
William A. Rutala, PhD, MPH
University of North Carolina Health Care System
Chapel Hill, NC
William E. Scheckler, MD
University of Wisconsin
Madison, WI
Beth H. Stover, RN
Kosair Children’s Hospital
Louisville, KY
Marjorie A. Underwood, RN, BSN CIC
Mt. Diablo Medical Center
Concord, CA
HICPAC Liaisons
William B. Baine, MD
Liaison to Agency for Healthcare Quality
Research
Lorine J. Jay MPH, RN, CPHQ
Liaison to Healthcare Resources Services
Administration
Stephen F. Jencks, MD, MPH
Liaison to Center for Medicare and Medicaid Services
Sheila A. Murphey, MD
Liaison to Food and Drug Administration
Mark Russi, MD, MPH
Liaison to American College of Occupational and
Environmental Medicine
Rachel L. Stricof, MPH
Liaison to Advisory Committee on Elimination of
Tuberculosis
Michael L. Tapper, MD
Liaison to Society for Healthcare Epidemiology of
America
Robert A. Wise, MD
Liaison to Joint Commission on the Accreditation of
Healthcare Organizations
Authors’ Associations
Joan Blanchard, RN, MSN, CNOR
Liaison to Association of periOperative
Registered Nurses
Patrick J. Brennan, MD
Liaison to Board of Scientific Counselors
Nancy Bjerke, RN, MPH, CIC
Liaison to Association of Professionals in
Infection Prevention and Control
Jeffrey P. Engel, MD
Liaison to Advisory Committee on Elimination of
Tuberculosis
David Henderson, MD
Liaison to National Institutes of Health
Jane D. Siegel, MD
Professor of Pediatrics
Department of Pediatrics
University of Texas Southwestern Medical Center
Emily Rhinehart RN MPH CIC CPHQ
Vice President
AIG Consultants, Inc.
Marguerite Jackson, RN PhD CIC
Director, Administrative Unit, National Tuberculosis
Curriculum Consortium,Department of Medicine
University of California San Diego
Linda Chiarello, RN MS
Division of Healthcare Quality Promotion
National Center for Infectious Diseases, CDC
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I. Introduction
Multidrug-resistant organisms(MDROs), including methicillin-resistant Staphylococcus
aureus (MRSA), vancomycin-resistant enterococci (VRE) and certain gram-negative bacilli
(GNB) have important infection control implications that either have not been addressed or
received only limited consideration in previous isolation guidelines. Increasing experience
with these organisms is improving understanding of the routes of transmission and effective
preventive measures. Although transmission of MDROs is most frequently documented in
acute care facilities, all healthcare settings are affected by the emergence and transmission
of antimicrobial-resistant microbes. The severity and extent of disease caused by these
pathogens varies by the population(s) affected and by the institution(s) in which they are
found. Institutions, in turn, vary widely in physical and functional characteristics, ranging
from long-term care facilities (LTCF) to specialty units (e.g., intensive care units [ICU], burn
units, neonatal ICUs [NICUs]) in tertiary care facilities. Because of this, the approaches to
prevention and control of these pathogens need to be tailored to the specific needs of each
population and individual institution. The prevention and control of MDROs is a national
priority - one that requires that all healthcare facilities and agencies assume responsibility(1)
(2). The following discussion and recommendations are provided to guide the
implementation of strategies and practices to prevent the transmission of MRSA, VRE, and
other MDROs. The administration of healthcare organizations and institutions should ensure
that appropriate strategies are fully implemented, regularly evaluated for effectiveness, and
adjusted such that there is a consistent decrease in the incidence of targeted MDROs.
Successful prevention and control of MDROs requires administrative and scientific
leadership and a financial and human resource commitment(3-5). Resources must be
made available for infection prevention and control, including expert consultation, laboratory
support, adherence monitoring, and data analysis. Infection prevention and control
professionals have found that healthcare personnel (HCP) are more receptive and adherent
to the recommended control measures when organizational leaders participate in efforts to
reduce MDRO transmission(3).
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II. Background
MDRO definition. For epidemiologic purposes, MDROs are defined as microorganisms,
predominantly bacteria, that are resistant to one or more classes of antimicrobial agents (1).
Although the names of certain MDROs describe resistance to only one agent (e.g., MRSA,
VRE), these pathogens are frequently resistant to most available antimicrobial agents .
These highly resistant organisms deserve special attention in healthcare facilities (2). In
addition to MRSA and VRE, certain GNB, including those producing extended spectrum
beta-lactamases (ESBLs) and others that are resistant to multiple classes of antimicrobial
agents, are of particular concern.1 In addition to Escherichia coli and Klebsiella pneumoniae,
these include strains of Acinetobacter baumannii resistant to all antimicrobial agents, or all
except imipenem,(6-12), and organisms such as Stenotrophomonas maltophilia (12-14),
Burkholderia cepacia (15, 16), and Ralstonia pickettii(17) that are intrinsically resistant to the
broadest-spectrum antimicrobial agents. In some residential settings (e.g., LTCFs), it is
important to control multidrug-resistant S. pneumoniae (MDRSP) that are resistant to
penicillin and other broad-spectrum agents such as macrolides and fluroquinolones (18, 19).
Strains of S. aureus that have intermediate susceptibility or are resistant to vancomycin (i.e.,
vancomycin-intermediate S. aureus [VISA], vancomycin-resistant S. aureus [VRSA]) (20-30)
have affected specific populations, such as hemodialysis patients.
Clinical importance of MDROs. In most instances, MDRO infections have clinical
manifestations that are similar to infections caused by susceptible pathogens. However,
options for treating patients with these infections are often extremely limited. For example,
until recently, only vancomycin provided effective therapy for potentially life-threatening
MRSA infections and during the 1990’s there were virtually no antimicrobial agents to treat
infections caused by VRE. Although antimicrobials are now available for treatment of
MRSA and VRE infections, resistance to each new agent has already emerged in clinical
1 Multidrug-resistant strains of M. tuberculosis are not addressed in this document because of the markedly different patterns of
transmission and spread of the pathogen and the very different control interventions that are needed for prevention of M. tuberculosis
infection. Current recommendations for prevention and control of tuberculosis can be found at: http://www.cdc.gov/mmwr/pdf/rr/rr5417.pdf
.
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isolates(31-37). Similarly, therapeutic options are limited for ESBL-producing isolates of
gram-negative bacilli, strains of A. baumannii resistant to all antimicrobial agents except
imipenem(8-11, 38) and intrinsically resistant Stenotrophomonas sp.(12-14, 39). These
limitations may influence antibiotic usage patterns in ways that suppress normal flora and
create a favorable environment for development of colonization when exposed to potential
MDR pathogens (i.e., selective advantage)(40).
Increased lengths of stay, costs, and mortality also have been associated with MDROs (4146). Two studies documented increased mortality, hospital lengths of stay, and hospital
charges associated with multidrug-resistant gram-negative bacilli (MDR-GNBs), including an
NICU outbreak of ESBL-producing Klebsiella pneumoniae (47) and the emergence of thirdgeneration cephalosporin resistance in Enterobacter spp. in hospitalized adults (48).
Vancomycin resistance has been reported to be an independent predictor of death from
enterococcal bacteremia(44, 49-53). Furthermore, VRE was associated with increased
mortality, length of hospital stay, admission to the ICU, surgical procedures, and costs when
VRE patients were compared with a matched hospital population (54).
However, MRSA may behave differently from other MDROs. When patients with MRSA
have been compared to patients with methicillin-susceptible S. aureus (MSSA), MRSAcolonized patients more frequently develop symptomatic infections(55, 56). Furthermore,
higher case fatality rates have been observed for certain MRSA infections, including
bacteremia(57-62), poststernotomy mediastinitis(63), and surgical site infections(64). These
outcomes may be a result of delays in the administration of vancomycin, the relative
decrease in the bactericidal activity of vancomycin(65), or persistent bacteremia associated
with intrinsic characteristics of certain MRSA strains (66). Mortality may be increased further
by S. aureus with reduced vancomycin susceptibility (VISA) (26, 67). Also some studies
have reported an association between MRSA infections and increased length of stay, and
healthcare costs(46, 61, 62), while others have not(64). Finally, some hospitals have
observed an increase in the overall occurrence of staphylococcal infections following the
introduction of MRSA into a hospital or special-care unit(68, 69).
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III. Epidemiology of MDROs
Trends: Prevalence of MDROs varies temporally, geographically, and by healthcare
setting(70, 71). For example, VRE emerged in the eastern United States in the early 1990s,
but did not appear in the western United States until several years later, and MDRSP varies
in prevalence by state(72). The type and level of care also influence the prevalence of
MDROs. ICUs, especially those at tertiary care facilities, may have a higher prevalence of
MDRO infections than do non-ICU settings (73, 74). Antimicrobial resistance rates are also
strongly correlated with hospital size, tertiary-level care, and facility type (e.g., LTCF)(75,
76). The frequency of clinical infection caused by these pathogens is low in LTCFs(77, 78).
Nonetheless, MDRO infections in LTCFs can cause serious disease and mortality, and
colonized or infected LTCF residents may serve as reservoirs and vehicles for MDRO
introduction into acute care facilities (78-88). Another example of population differences in
prevalence of target MDROs is in the pediatric population. Point prevalence surveys
conducted by the Pediatric Prevention Network (PPN) in eight U.S. PICUs and 7 U.S.
NICUs in 2000 found < 4% of patients were colonized with MRSA or VRE compared with
10-24% were colonized with ceftazidime- or aminoglycoside-resistant gram-negative bacilli;
< 3% were colonized with ESBL-producing gram negative bacilli. Despite some evidence
that MDRO burden is greatest in adult hospital patients, MDRO require similar control efforts
in pediatric populations as well(89).
During the last several decades, the prevalence of MDROs in U.S. hospitals and medical
centers has increased steadily(90, 91). MRSA was first isolated in the United States in
1968. By the early 1990s, MRSA accounted for 20%-25% of Staphylococcus aureus
isolates from hospitalized patients(92). In 1999, MRSA accounted for >50% of S. aureus
isolates from patients in ICUs in the National Nosocomial Infection Surveillance (NNIS)
system; in 2003, 59.5% of S. aureus isolates in NNIS ICUs were MRSA (93). A similar rise
in prevalence has occurred with VRE (94). From 1990 to 1997, the prevalence of VRE in
enterococcal isolates from hospitalized patients increased from <1% to approximately 15%
(95). VRE accounted for almost 25% of enterococcus isolates in NNIS ICUs in 1999 (94),
and 28.5% in 2003 (93).
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GNB resistant to ESBLs, fluoroquinolones, carbapenems, and aminoglycosides also have
increased in prevalence. For example, in 1997, the SENTRY Antimicrobial Surveillance
Program found that among K. pneumoniae strains isolated in the United States, resistance
rates to ceftazidime and other third-generation cephalosporins were 6.6%, 9.7%, 5.4%, and
3.6% for bloodstream, pneumonia, wound, and urinary tract infections, respectively (95) In
2003, 20.6% of all K. pneumoniae isolates from NNIS ICUs were resistant to these drugs
((93)). Similarly, between 1999 and 2003, Pseudomonas aeruginosa resistance to
fluoroquinolone antibiotics increased from 23% to 29.5% in NNIS ICUs(74). Also, a 3-month
survey of 15 Brooklyn hospitals in 1999 found that 53% of A. baumannii strains exhibited
resistance to carbapenems and 24% of P. aeruginosa strains were resistant to imipenem
(10). During 1994-2000, a national review of ICU patients in 43 states found that the overall
susceptibility to ciprofloxacin decreased from 86% to 76% and was temporally associated
with increased use of fluoroquinolones in the United States (96).
Lastly, an analysis of temporal trends of antimicrobial resistance in non-ICU patients in 23
U.S. hospitals during 1996-1997 and 1998-1999 (97) found significant increases in the
prevalence of resistant isolates including MRSA, ciprofloxacin-resistant P. aeruginosa, and
ciprofloxacin- or ofloxacin-resistant E. coli. Several factors may have contributed to these
increases including: selective pressure exerted by exposure to antimicrobial agents,
particularly fluoroquinolones, outside of the ICU and/or in the community(7, 96, 98);
increasing rates of community-associated MRSA colonization and infection(99, 100);
inadequate adherence to infection control practices; or a combination of these factors.
Important concepts in transmission. Once MDROs are introduced into a healthcare
setting, transmission and persistence of the resistant strain is determined by the availability
of vulnerable patients, selective pressure exerted by antimicrobial use, increased potential
for transmission from larger numbers of colonized or infected patients (“colonization
pressure”)(101, 102); and the impact of implementation and adherence to prevention efforts.
Patients vulnerable to colonization and infection include those with severe disease,
especially those with compromised host defenses from underlying medical conditions;
recent surgery; or indwelling medical devices (e.g., urinary catheters or endotracheal
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tubes(103, 104)). Hospitalized patients, especially ICU patients, tend to have more risk
factors than non-hospitalized patients do, and have the highest infection rates. For example,
the risk that an ICU patient will acquire VRE increases significantly once the proportion of
ICU patients colonized with VRE exceeds 50%(101) or the number days of exposure to a
VRE-patient exceeds 15 days(105). A similar effect of colonization pressure has been
demonstrated for MRSA in a medical ICU(102). Increasing numbers of infections with
MDROs also have been reported in non-ICU areas of hospitals(97).
There is ample epidemiologic evidence to suggest that MDROs are carried from one person
to another via the hands of HCP(106-109). Hands are easily contaminated during the
process of care-giving or from contact with environmental surfaces in close proximity to the
patient(110-113). The latter is especially important when patients have diarrhea and the
reservoir of the MDRO is the gastrointestinal tract(114-117). Without adherence to
published recommendations for hand hygiene and glove use(111) HCP are more likely to
transmit MDROs to patients. Thus, strategies to increase and monitor adherence are
important components of MDRO control programs(106, 118).
Opportunities for transmission of MDROs beyond the acute care hospital results from
patients receiving care at multiple healthcare facilities and moving between acute-care,
ambulatory and/or chronic care, and LTC environments. System-wide surveillance at LDS
Hospital in Salt Lake City, Utah, monitored patients identified as being infected or colonized
with MRSA or VRE, and found that those patients subsequently received inpatient or
outpatient care at as many as 62 different healthcare facilities in that system during a 5-year
span(119).
Role of colonized HCP in MDRO transmission. Rarely, HCP may introduce an MDRO
into a patient care unit(120-123). Occasionally, HCP can become persistently colonized with
an MDRO, but these HCP have a limited role in transmission, unless other factors are
present. Additional factors that can facilitate transmission, include chronic sinusitis(120),
upper respiratory infection(123), and dermatitis(124).
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Implications of community-associated MRSA (CA-MRSA). The emergence of new
epidemic strains of MRSA in the community, among patients without established MRSA risk
factors, may present new challenges to MRSA control in healthcare settings(125-128).
Historically, genetic analyses of MRSA isolated from patients in hospitals worldwide
revealed that a relatively small number of MRSA strains have unique qualities that facilitate
their transmission from patient to patient within healthcare facilities over wide geographic
areas, explaining the dramatic increases in HAIs caused by MRSA in the 1980s and early
1990s(129). To date, most MRSA strains isolated from patients with CA-MRSA infections
have been microbiologically distinct from those endemic in healthcare settings, suggesting
that some of these strains may have arisin de novo in the community via acquisition of
methicillin resistance genes by established methicillin-susceptible S. aureus (MSSA)
strains(130-132). Two pulsed-field types, termed USA300 and USA400 according to a
typing scheme established at CDC, have accounted for the majority of CA-MRSA infections
characterized in the United States, whereas pulsed-field types USA100 and USA200 are the
predominant genotypes endemic in healthcare settings(133).
USA300 and USA400 genotypes almost always carry type IV of the staphylococcal
chromosomal cassette (SCC) mec, the mobile genetic element that carries the mecA
methicillin-resistance gene (133, 134). This genetic cassette is smaller than types I through
III, the types typically found in healthcare associated MRSA strains, and is hypothesized to
be more easily transferable between S. aureus strains.
CA-MRSA infection presents most commonly as relatively minor skin and soft tissue
infections, but severe invasive disease, including necrotizing pneumonia, necrotizing
fasciitis, severe osteomyelitis, and a sepsis syndrome with increased mortality have also
been described in children and adults(134-136).
Transmission within hospitals of MRSA strains first described in the community (e.g.
USA300 and USA400) are being reported with increasing frequency(137-140). Changing
resistance patterns of MRSA in ICUs in the NNIS system from 1992 to 2003 provide
additional evidence that the new epidemic MRSA strains are becoming established
10
healthcare-associated as well as community pathogens(90). Infections with these strains
have most commonly presented as skin disease in community settings. However, intrinsic
virulence characteristics of the organisms can result in clinical manifestations similar to or
potentially more severe than traditional healthcare-associated MRSA infections among
hospitalized patients. The prevalence of MRSA colonization and infection in the
surrounding community may therefore affect the selection of strategies for MRSA control in
healthcare settings.
IV. MDRO Prevention and Control
Prevention of Infections. Preventing infections will reduce the burden of MDROs in
healthcare settings. Prevention of antimicrobial resistance depends on appropriate clinical
practices that should be incorporated into all routine patient care. These include optimal
management of vascular and urinary catheters, prevention of lower respiratory tract
infection in intubated patients, accurate diagnosis of infectious etiologies, and judicious
antimicrobial selection and utilization. Guidance for these preventive practices include the
Campaign to Reduce Antimicrobial Resistance in Healthcare Settings
(www.cdc.gov/drugresistance/healthcare/default.htm), a multifaceted, evidence-based
approach with four parallel strategies: infection prevention; accurate and prompt diagnosis
and treatment; prudent use of antimicrobials; and prevention of transmission. Campaign
materials are available for acute care hospitals, surgical settings, dialysis units, LTCFs and
pediatric acute care units.
To reduce rates of central-venous-line associated bloodstream infections(CVL-BSIs) and
ventilator-associated pneumonia (VAP), a group of bundled evidence-based clinical
practices have been implemented in many U.S. healthcare facilities(118, 141-144). One
report demonstrated a sustained effect on the reduction in CVL-BSI rates with this
approach(145). Although the specific effect on MDRO infection and colonization rates have
not been reported, it is logical that decreasing these and other healthcare-associated
infections will in turn reduce antimicrobial use and decrease opportunities for emergence
and transmission of MDROs.
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Prevention and Control of MDRO transmission
Overview of the MDRO control literature. Successful control of MDROs has been
documented in the United States and abroad using a variety of combined interventions.
These include improvements in hand hygiene, use of Contact Precautions until patients are
culture-negative for a target MDRO, active surveillance cultures (ASC), education,
enhanced environmental cleaning, and improvements in communication about patients with
MDROs within and between healthcare facilities.
Representative studies include:
Reduced rates of MRSA transmission in The Netherlands, Belgium, Denmark, and other
Scandinavian countries after the implementation of aggressive and sustained infection
control interventions (i.e., ASC; preemptive use of Contact Precautions upon admission
until proven culture negative; and, in some instances, closure of units to new
admissions). MRSA generally accounts for a very small proportion of S. aureus clinical
isolates in these countries(146-150).
Reduced rates of VRE transmission in healthcare facilities in the three-state Siouxland
region (Iowa, Nebraska, and South Dakota) following formation of a coalition and
development of an effective region-wide infection control intervention that included ASC
and isolation of infected patients. The overall prevalence rate of VRE in the 30
participating facilities decreased from 2.2% in 1997 to 0.5% in 1999(151).
Eradication of endemic MRSA infections from two NICUs. The first NICU included
implementation of ASC, Contact Precautions, use of triple dye on the umbilical cord, and
systems changes to improve surveillance and adherence to recommended practices and
to reduce overcrowding(152). The second NICU used ASC and Contact Precautions;
surgical masks were included in the barriers used for Contact Precautions(153).
Control of an outbreak and eventual eradication of VRE from a burn unit over a 13month period with implementation of aggressive culturing, environmental cleaning, and
barrier isolation(154).
Control of an outbreak of VRE in a NICU over a 3-year period with implementation of
ASC, other infection control measures such as use of a waterless hand disinfectant, and
mandatory in-service education(155).
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Eradication of MDR-strains of A. baumannii from a burn unit over a 16-month period with
implementation of strategies to improve adherence to hand hygiene, isolation,
environmental cleaning, and temporary unit closure(38).
In addition, more than 100 reports published during 1982-2005 support the efficacy of
combinations of various control interventions to reduce the burden of MRSA, VRE, and
MDR-GNBs (Tables 1 and 2). Case-rate reduction or pathogen eradication was reported
in a majority of studies.
VRE was eradicated in seven special-care units(154, 156-160), two hospitals(161, 162),
and one LTCF(163).
MRSA was eradicated from nine special-care units(89, 152, 153, 164-169), two
hospitals(170), one LTCF(167), and one Finnish district(171). Furthermore, four MRSA
reports described continuing success in sustaining low endemic MDRO rates for over 5
years(68, 166, 172, 173).
An MDR-GNB was eradicated from 13 special-care units(8, 9, 38, 174-180) and two
hospitals (11, 181).
These success stories testify to the importance of having dedicated and knowledgeable
teams of healthcare professionals who are willing to persist for years, if necessary, to
control MDROs. Eradication and control of MDROs, such as those reported, frequently
required periodic reassessment and the addition of new and more stringent interventions
over time (tiered strategy). For example, interventions were added in a stepwise fashion
during a 3-year effort that eventually eradicated MRSA from an NICU(152). A series of
interventions was adopted throughout the course of a year to eradicate VRE from a burn
unit(154). Similarly, eradication of carbapenem-resistant strains of A. baumannii from a
hospital required multiple and progressively more intense interventions over several
years(11).
Nearly all studies reporting successful MDRO control employed a median of 7 to 8 different
interventions concurrently or sequentially (Table 1). These figures may underestimate the
actual number of control measures used, because authors of these reports may have
considered their earliest efforts routine (e.g., added emphasis on handwashing), and did not
include them as interventions, and some ”single measures” are, in fact, a complex
13
combination of several interventions. The use of multiple concurrent control measures in
these reports underscores the need for a comprehensive approach for controlling MDROs.
Several factors affect the ability to generalize the results of the various studies reviewed,
including differences in definition, study design, endpoints and variables measured, and
period of follow-up. Two-thirds of the reports cited in Tables 1 and 2 involved perceived
outbreaks, and one-third described efforts to reduce endemic transmission. Few reports
described preemptive efforts or prospective studies to control MDROs before they had
reached high levels within a unit or facility.
With these and other factors, it has not been possible to determine the effectiveness of
individual interventions, or a specific combination of interventions, that would be appropriate
for all healthcare facilities to implement in order to control their target MDROs. Randomized
controlled trials are necessary to acquire this level of evidence. An NIH-sponsored,
randomized controlled trial on the prevention of MRSA and VRE transmission in adult ICUs
is ongoing and may provide further insight into optimal control measures
(http://clinicaltrials.gov/ct/show/NCT00100386?order=1). This trial compares the use of
education (to improve adherence to hand hygiene) and Standard Precautions to the use of
ASC and Contact Precautions.
Control Interventions. The various types of interventions used to control or eradicate
MDROs may be grouped into seven categories. These include administrative support,
judicious use of antimicrobials, surveillance (routine and enhanced), Standard and Contact
Precautions, environmental measures, education and decolonization. These interventions
provide the basis for the recommendations for control of MDROs in healthcare settings that
follow this review and as summarized in Table 3. In the studies reviewed, these
interventions were applied in various combinations and degrees of intensity, with differences
in outcome.
1. Administrative support. In several reports, administrative support and involvement
were important for the successful control of the target MDRO(3, 152, 182-185), and
authorities in infection control have strongly recommended such support(2, 106, 107,
14
186). There are several examples of MDRO control interventions that require
administrative commitment of fiscal and human resources. One is the use of ASC(8,
38, 68, 107, 114, 151, 152, 167, 168, 183, 184, 187-192). Other interventions that
require administrative support include: 1) implementing system changes to ensure
prompt and effective communications e.g., computer alerts to identify patients
previously known to be colonized/infected with MDROs(184, 189, 193, 194); 2),
providing the necessary number and appropriate placement of hand washing sinks
and alcohol-containing hand rub dispensers in the facility(106, 195); 3) maintaining
staffing levels appropriate to the intensity of care required(152, 196-202); and 4)
enforcing adherence to recommended infection control practices (e.g., hand hygiene,
Standard and Contact Precautions) for MDRO control. Other measures that have
been associated with a positive impact on prevention efforts, that require
administrative support, are direct observation with feedback to HCP on adherence to
recommended precautions and keeping HCP informed about changes in
transmission rates(3, 152, 182, 203-205). A “How-to guide” for implementing change
in ICUs, including analysis of structure, process, and outcomes when designing
interventions, can assist in identification of needed administrative interventions(195).
Lastly, participation in existing, or the creation of new, city-wide, state-wide, regional
or national coalitions, to combat emerging or growing MDRO problems is an effective
strategy that requires administrative support(146, 151, 167, 188, 206, 207).
2. Education. Facility-wide, unit-targeted, and informal, educational interventions were
included in several successful studies(3, 189, 193, 208-211). The focus of the
interventions was to encourage a behavior change through improved understanding
of the problem MDRO that the facility was trying to control. Whether the desired
change involved hand hygiene, antimicrobial prescribing patterns, or other outcomes,
enhancing understanding and creating a culture that supported and promoted the
desired behavior, were viewed as essential to the success of the intervention.
Educational campaigns to enhance adherence to hand hygiene practices in
conjunction with other control measures have been associated temporally with
decreases in MDRO transmission in various healthcare settings(3, 106, 163).
15
3. Judicious use of antimicrobial agents. While a comprehensive review of
antimicrobial stewardship is beyond the scope of this guideline, recommendations for
control of MDROs must include attention to judicious antimicrobial use. A temporal
association between formulary changes and decreased occurrence of a target MDRO
was found in several studies, especially in those that focused on MDR-GNBs(98,
177, 209, 212-218). Occurrence of C. difficile-associated disease has also been
associated with changes in antimicrobial use(219). Although some MRSA and VRE
control efforts have attempted to limit antimicrobial use, the relative importance of this
measure for controlling these MDROs remains unclear(193, 220). Limiting
antimicrobial use alone may fail to control resistance due to a combination of factors;
including 1) the relative effect of antimicrobials on providing initial selective pressure,
compared to perpetuating resistance once it has emerged; 2) inadequate limits on
usage; or 3) insufficient time to observe the impact of this intervention. With the intent
of addressing #2 and #3 above in the study design, one study demonstrated a
decrease in the prevalence of VRE associated with a formulary switch from ticarcillinclavulanate to piperacillin-tazobactam(221).
The CDC Campaign to Prevent Antimicrobial Resistance that was launched in 2002
provides evidence-based principles for judicious use of antimicrobials and tools for
implementation(222) www.cdc.gov/drugresistance/healthcare. This effort targets all
healthcare settings and focuses on effective antimicrobial treatment of infections, use
of narrow spectrum agents, treatment of infections and not contaminants, avoiding
excessive duration of therapy, and restricting use of broad-spectrum or more potent
antimicrobials to treatment of serious infections when the pathogen is not known or
when other effective agents are unavailable. Achieving these objectives would likely
diminish the selective pressure that favors proliferation of MDROs. Strategies for
influencing antimicrobial prescribing patterns within healthcare facilities include
education; formulary restriction; prior-approval programs, including pre-approved
indications; automatic stop orders; academic interventions to counteract
pharmaceutical influences on prescribing patterns; antimicrobial cycling(223-226);
16
computer-assisted management programs(227-229); and active efforts to remove
redundant antimicrobial combinations(230). A systematic review of controlled studies
identified several successful practices. These include social marketing (i.e. consumer
education), practice guidelines, authorization systems, formulary restriction,
mandatory consultation, and peer review and feedback. It further suggested that
online systems that provide clinical information, structured order entry, and decision
support are promising strategies(231). These changes are best accomplished
through an organizational, multidisciplinary, antimicrobial management program(232).
4. MDRO surveillance. Surveillance is a critically important component of any MDRO
control program, allowing detection of newly emerging pathogens, monitoring
epidemiologic trends, and measuring the effectiveness of interventions. Multiple
MDRO surveillance strategies have been employed, ranging from surveillance of
clinical microbiology laboratory results obtained as part of routine clinical care, to use
of ASC to detect asymptomatic colonization.
Surveillance for MDROs isolated from routine clinical cultures.
Antibiograms. The simplest form of MDRO surveillance is monitoring of clinical
microbiology isolates resulting from tests ordered as part of routine clinical care. This
method is particularly useful to detect emergence of new MDROs not previously
detected, either within an individual healthcare facility or community-wide. In addition,
this information can be used to prepare facility- or unit-specific summary antimicrobial
susceptibility reports that describe pathogen-specific prevalence of resistance among
clinical isolates. Such reports may be useful to monitor for changes in known
resistance patterns that might signal emergence or transmission of MDROs, and also
to provide clinicians with information to guide antimicrobial prescribing practices(233235).
MDRO Incidence Based on Clinical Culture Results. Some investigators have
used clinical microbiology results to calculate measures of incidence of MDRO
isolates in specific populations or patient care locations (e.g. new MDRO
17
isolates/1,000 patient days, new MDRO isolates per month)(205, 236, 237). Such
measures may be useful for monitoring MDRO trends and assessing the impact of
prevention programs, although they have limitations. Because they are based solely
on positive culture results without accompanying clinical information, they do not
distinguish colonization from infection, and may not fully demonstrate the burden of
MDRO-associated disease. Furthermore, these measures do not precisely measure
acquisition of MDRO colonization in a given populaton or location. Isolating an
MDRO from a clinical culture obtained from a patient several days after admission to
a given unit or facility does not establish that the patient acquired colonization in that
unit. On the other hand, patients who acquire MDRO colonization may remain
undetected by clinical cultures(107). Despite these limitations, incidence measures
based on clinical culture results may be highly correlated with actual MDRO
transmission rates derived from information using ASC, as demonstrated in a recent
multicenter study(237). These results suggest that incidence measures based on
clinical cultures alone might be useful surrogates for monitoring changes in MDRO
transmission rates.
MDRO Infection Rates. Clinical cultures can also be used to identify targeted MDRO
infections in certain patient populations or units(238, 239). This strategy requires
investigation of clinical circumstances surrounding a positive culture to distinguish
colonization from infection, but it can be particularly helpful in defining the clinical
impact of MDROs within a facility.
Molecular typing of MDRO isolates. Many investigators have used molecular
typing of selected isolates to confirm clonal transmission to enhance understanding
of MDRO transmission and the effect of interventions within their facility(38, 68, 89,
92, 138, 152, 190, 193, 236, 240).
Surveillance for MDROs by Detecting Asymptomatic Colonization
Another form of MDRO surveillance is the use of active surveillance cultures (ASC) to
identify patients who are colonized with a targeted MDRO(38, 107, 241). This
18
approach is based upon the observation that, for some MDROs, detection of
colonization may be delayed or missed completely if culture results obtained in the
course of routine clinical care are the primary means of identifying colonized
patients(8, 38, 107, 114, 151, 153, 167, 168, 183, 184, 187, 189, 191-193, 242-244).
Several authors report having used ASC when new pathogens emerge in order to
define the epidemiology of the particular agent(22, 23, 107, 190). In addition, the
authors of several reports have concluded that ASC, in combination with use of
Contact Precautions for colonized patients, contributed directly to the decline or
eradication of the target MDRO(38, 68, 107, 151, 153, 184, 217, 242). However, not
all studies have reached the same conclusion. Poor control of MRSA despite use of
ASC has been described(245). A recent study failed to identify cross-transmission of
MRSA or MSSA in a MICU during a 10 week period when ASC were obtained,
despite the fact that culture results were not reported to the staff(246). The
investigators suggest that the degree of cohorting and adherence to Standard
Precautions might have been the important determinants of transmission prevention,
rather than the use of ASC and Contact Precautions for MRSA-colonized patients.
The authors of a systematic review of the literature on the use of isolation measures
to control healthcare-associated MRSA concluded that there is evidence that
concerted efforts that include ASC and isolation can reduce MRSA even in endemic
settings. However, the authors also noted that methodological weaknesses and
inadequate reporting in published research make it difficult to rule out plausible
alternative explanations for reductions in MRSA acquisition associated with these
interventions, and therefore concluded that the precise contribution of active
surveillance and isolation alone is difficult to assess(247).
Mathematical modeling studies have been used to estimate the impact of ASC use in
control of MDROs. One such study evaluating interventions to decrease VRE
transmission indicated that use of ASC (versus no cultures) could potentially
decrease transmission 39% and that with pre-emptive isolation plus ASC,
transmission could be decreased 65%(248). Another mathematical model examining
the use of ASC and isolation for control of MRSA predicted that isolating colonized or
19
infected patients on the basis of clinical culture results is unlikely to be successful at
controlling MRSA, whereas use of active surveillance and isolation can lead to
successful control, even in settings where MRSA is highly endemic.(249) There is
less literature on the use of ASC in controlling MDR-GNBs. Active surveillance
cultures have been used as part of efforts to successful control of MDR-GNBs in
outbreak settings. The experience with ASC as part of successful control efforts in
endemic settings is mixed. One study reported successful reduction of extendedspectrum beta-lactamase –producing Enterobacteriaceae over a six year period
using a multifaceted control program that included use of ASC(245). Other reports
suggest that use of ASC is not necessary to control endemic MDR-GNBs.(250, 251).
More research is needed to determine the circumstances under which ASC are most
beneficial(252), but their use should be considered in some settings, especially if
other control measures have been ineffective. When use of ASC is incorporated into
MDRO prevention programs, the following should be considered:
•
The decision to use ASC as part of an infection prevention and control program
requires additional support for successful implementation, including: 1) personnel
to obtain the appropriate cultures, 2) microbiology laboratory personnel to process
the cultures, 3) mechanism for communicating results to caregivers, 4) concurrent
decisions about use of additional isolation measures triggered by a positive
culture (e.g. Contact Precautions) and 5) mechanism for assuring adherence to
the additional isolation measures.
•
The populations targeted for ASC are not well defined and vary among published
reports. Some investigators have chosen to target specific patient populations
considered at high risk for MDRO colonization based on factors such as location
(e.g. ICU with high MDRO rates), antibiotic exposure history, presence of
underlying diseases, prolonged duration of stay, exposure to other MDROcolonized patients, patients transferred from other facilities known to have a high
prevalence of MDRO carriage, or having a history of recent hospital or nursing
home stays(107, 151, 253). A more commonly employed strategy involves
obtaining surveillance cultures from all patients admitted to units experiencing
20
high rates of colonization/infection with the MDROs of interest, unless they are
already known to be MDRO carriers(153, 184, 242, 254). In an effort to better
define target populations for active surveillance, investigators have attempted to
create prediction rules to identify subpopulations of patients at high risk for
colonization on hospital admission(255, 256). Decisions about which populations
should be targeted for active surveillance should be made in the context of local
determinations of the incidence and prevalence of MDRO colonization within the
intervention facility as well as other facilities with whom patients are frequently
exchanged(257).
•
Optimal timing and interval of ASC are not well defined. In many reports, cultures
were obtained at the time of admission to the hospital or intervention unit or at the
time of transfer to or from designated units (e.g., ICU)(107). In addition, some
hospitals have chosen to obtain cultures on a periodic basis [e.g., weekly(8, 153,
159) to detect silent transmission. Others have based follow-up cultures on the
presence of certain risk factors for MDRO colonization, such as antibiotic
exposure, exposure to other MDRO colonized patients, or prolonged duration of
stay in a high risk unit(253).
•
Methods for obtaining ASC must be carefully considered, and may vary
depending upon the MDRO of interest.
o MRSA: Studies suggest that cultures of the nares identify most patients
with MRSA and perirectal and wound cultures can identify additional
carriers(152, 258-261).
o VRE: Stool, rectal, or perirectal swabs are generally considered a sensitive
method for detection of VRE. While one study suggested that rectal swabs
may identify only 60% of individuals harboring VRE, and may be affected
by VRE stool density(262), this observation has not been reported
elsewhere in the literature.
o MDR-GNBs: Several methods for detection of MDR-GNBs have been
employed, including use of peri-rectal or rectal swabs alone or in
combination with oro-pharyngeal, endotracheal, inguinal, or wound
cultures. The absence of standardized screening media for many gram-
21
negative bacilli can make the process of isolating a specific MDR-GNB a
relatively labor-intensive process(38, 190, 241, 250).
o Rapid detection methods: Using conventional culture methods for active
surveillance can result in a delay of 2-3 days before results are available. If
the infection control precautions (e.g., Contact Precautions) are withheld
until the results are available, the desired infection control measures could
be delayed. If empiric precautions are used pending negative surveillance
culture results, precautions may be unnecessarily implemented for many, if
not most, patients. For this reason, investigators have sought methods for
decreasing the time necessary to obtain a result from ASC. Commercially
available media containing chromogenic enzyme substrates (CHROMagar
MRSA(263, 264) has been shown to have high sensitivity and specificity
for identification of MRSA and facilitate detection of MRSA colonies in
screening cultures as early as 16 hours after inoculation. In addition, realtime PCR-based tests for rapid detection of MRSA directly from culture
swabs (< 1-2 hours) are now commercially available(265-267), as well as
PCR-based tests for detection of vanA and van B genes from rectal
swabs(268). The impact of rapid testing on the effectiveness of active
surveillance as a prevention strategy, however, has not been fully
determined. Rapid identification of MRSA in one study was associated with
a significant reduction in MRSA infections acquired in the medical ICU, but
not the surgical ICU(265). A mathematical model characterizing MRSA
transmission dynamics predicted that, in comparison to conventional
culture methods, the use of rapid detection tests may decrease isolation
needs in settings of low-endemicity and result in more rapid reduction in
prevalence in highly-endemic settings(249).
•
Some MDRO control reports described surveillance cultures of healthcare
personnel during outbreaks, but colonized or infected healthcare personnel are
rarely the source of ongoing transmission, and this strategy should be reserved
for settings in which specific healthcare personnel have been epidemiologically
implicated in the transmission of MDROs(38, 92, 152-154, 188).
22
5. Infection Control Precautions. Since 1996 CDC has recommended the use of
Standard and Contact Precautions for MDROs “judged by an infection control
program…to be of special clinical and epidemiologic significance.” This
recommendation was based on general consensus and was not necessarily
evidence-based. No studies have directly compared the efficacy of Standard
Precautions alone versus Standard Precautions and Contact Precautions, with or
without ASC, for control of MDROs. Some reports mention the use of one or both
sets of precautions as part of successful MDRO control efforts; however, the
precautions were not the primary focus of the study intervention(164, 190, 205, 269271). The NIH-sponsored study mentioned earlier (Section: Overview of the MDRO
control literature) may provide some answers,
http://clinicaltrials.gov/ct/show/NCT00100386?order=1).
Standard Precautions have an essential role in preventing MDRO transmission,
even in facilities that use Contact Precautions for patients with an identified MDRO.
Colonization with MDROs is frequently undetected; even surveillance cultures may
fail to identify colonized persons due to lack of sensitivity, laboratory deficiencies, or
intermittent colonization due to antimicrobial therapy(262). Therefore, Standard
Precautions must be used in order to prevent transmission from potentially colonized
patients. Hand hygiene is an important component of Standard Precautions. The
authors of the Guideline for Hand Hygiene in Healthcare Settings(106) cited nine
studies that demonstrated a temporal relationship between improved adherence to
recommended hand hygiene practices and control of MDROs. It is noteworthy that in
one report the frequency of hand hygiene did not improve with use of Contact
Precautions but did improve when gloves were used (per Standard Precautions) for
contact with MDRO patients(272).
MDRO control efforts frequently involved changes in isolation practices, especially
during outbreaks. In the majority of reports, Contact Precautions were implemented
for all patients found to be colonized or infected with the target MDRO (See Table 2).
23
Some facilities also preemptively used Contact Precautions, in conjunction with ASC,
for all new admissions or for all patients admitted to a specific unit, until a negative
screening culture for the target MDRO was reported(30, 184, 273).
Contact Precautions are intended to prevent transmission of infectious agents,
including epidemiologically important microorganisms, which are transmitted by direct
or indirect contact with the patient or the patient’s environment. A single-patient room
is preferred for patients who require Contact Precautions. When a single-patient
room is not available, consultation with infection control is necessary to assess the
various risks associated with other patient placement options (e.g., cohorting,
keeping the patient with an existing roommate). HCP caring for patients on Contact
Precautions should wear a gown and gloves for all interactions that may involve
contact with the patient or potentially contaminated areas in the patient’s
environment. Donning gown and gloves upon room entry and discarding before
exiting the patient room is done to contain pathogens, especially those that have
been implicated in transmission through environmental contamination (e.g., VRE, C.
difficile, noroviruses and other intestinal tract agents; RSV)(109, 111, 274-277).
Cohorting and other MDRO control strategies. In several reports, cohorting of
patients(152, 153, 167, 183, 184, 188, 189, 217, 242), cohorting of staff(184, 217,
242, 278), use of designated beds or units(183, 184), and even unit closure(38, 146,
159, 161, 279, 280) were necessary to control transmission. Some authors indicated
that implementation of the latter two strategies were the turning points in their control
efforts; however, these measures usually followed many other actions to prevent
transmission. In one, two-center study, moving MRSA-positive patients into single
rooms or cohorting these patients in designated bays failed to reduce transmission in
ICUs. However, in this study adherence to recommendations for hand hygiene
between patient contacts was only 21%(281). Other published studies, including one
commissioned by the American Institute of Architects and the Facility Guidelines
Institute (www.aia.org/aah_gd_hospcons), have documented a beneficial relationship
between private rooms and reduction in risk of acquiring MDROs(282). Additional
24
studies are needed to define the specific contribution of using single-patient rooms
and/or cohorting on preventing transmission of MDROs.
Duration of Contact Precautions. The necessary duration of Contact Precautions
for patients treated for infection with an MDRO, but who may continue to be
colonized with the organism at one or more body sites, remains an unresolved issue.
Patients may remain colonized with MDROs for prolonged periods; shedding of these
organisms may be intermittent, and surveillance cultures may fail to detect their
presence(84, 250, 283). The 1995 HICPAC guideline for preventing the transmission
of VRE suggested three negative stool/perianal cultures obtained at weekly intervals
as a criterion for discontinuation of Contact Precautions(274). One study found these
criteria generally reliable(284). However, this and other studies have noted a
recurrence of VRE positive cultures in persons who subsequently receive
antimicrobial therapy and persistent or intermittent carriage of VRE for more than 1
year has been reported(284-286). Similarly, colonization with MRSA can be
prolonged(287, 288). Studies demonstrating initial clearance of MRSA following
decolonization therapy have reported a high frequency of subsequent carriage(289,
290). There is a paucity of information in the literature on when to discontinue
Contact Precautions for patients colonized with a MDR-GNB, possibly because
infection and colonization with these MDROs are often associated with outbreaks.
Despite the uncertainty about when to discontinue Contact Precautions, the studies
offer some guidance. In the context of an outbreak, prudence would dictate that
Contact Precautions be used indefinitely for all previously infected and known
colonized patients. Likewise, if ASC are used to detect and isolate patients colonized
with MRSA or VRE, and there is no decolonization of these patients, it is logical to
assume that Contact Precautions would be used for the duration of stay in the setting
where they were first implemented. In general, it seems reasonable to discontinue
Contact Precautions when three or more surveillance cultures for the target MDRO
are repeatedly negative over the course of a week or two in a patient who has not
received antimicrobial therapy for several weeks, especially in the absence of a
25
draining wound, profuse respiratory secretions, or evidence implicating the specific
patient in ongoing transmission of the MDRO within the facility.
Barriers used for contact with patients infected or colonized with MDROs.
Three studies evaluated the use of gloves with or without gowns for all patient
contacts to prevent VRE acquisition in ICU settings(30, 105, 273). Two of the studies
showed that use of both gloves and gowns reduced VRE transmission(30, 105) while
the third showed no difference in transmission based on the barriers used(273). One
study in a LTCF compared the use of gloves only, with gloves plus contact isolation,
for patients with four MDROs, including VRE and MRSA, and found no
difference(86). However, patients on contact isolation were more likely to acquire
MDR-K. pneumoniae strains that were prevalent in the facility; reasons for this were
not specifically known. In addition to differences in outcome, differing methodologies
make comparisons difficult. Specifically, HCP adherence to the recommended
protocol, the influence of added precautions on the number of HCP-patient
interactions, and colonization pressure were not consistently assessed.
Impact of Contact Precautions on patient care and well-being. There are limited
data regarding the impact of Contact Precautions on patients. Two studies found that
HCP, including attending physicians, were half as likely to enter the rooms of(291), or
examine(292), patients on Contact Precautions. Other investigators have reported
similar observations on surgical wards(293). Two studies reported that patients in
private rooms and on barrier precautions for an MDRO had increased anxiety and
depression scores(294, 295). Another study found that patients placed on Contact
Precautions for MRSA had significantly more preventable adverse events, expressed
greater dissatisfaction with their treatment, and had less documented care than
control patients who were not in isolation(296). Therefore, when patients are placed
on Contact Precautions, efforts must be made by the healthcare team to counteract
these potential adverse effects.
26
6. Environmental measures. The potential role of environmental reservoirs, such as
surfaces and medical equipment, in the transmission of VRE and other MDROs has
been the subject of several reports(109-111, 297, 298). While environmental cultures
are not routinely recommended(299), environmental cultures were used in several
studies to document contamination, and led to interventions that included the use of
dedicated noncritical medical equipment(217, 300), assignment of dedicated cleaning
personnel to the affected patient care unit(154), and increased cleaning and
disinfection of frequently-touched surfaces (e.g., bedrails, charts, bedside
commodes, doorknobs). A common reason given for finding environmental
contamination with an MDRO was the lack of adherence to facility procedures for
cleaning and disinfection. In an educational and observational intervention, which
targeted a defined group of housekeeping personnel, there was a persistent
decrease in the acquisition of VRE in a medical ICU(301). Therefore, monitoring for
adherence to recommended environmental cleaning practices is an important
determinant for success in controlling transmission of MDROs and other pathogens
in the environment(274, 302).
In the MDRO reports reviewed, enhanced environmental cleaning was frequently
undertaken when there was evidence of environmental contamination and ongoing
transmission. Rarely, control of the target MDRO required vacating a patient care unit
for complete environmental cleaning and assessment(175, 279).
7. Decolonization. Decolonization entails treatment of persons colonized with a
specific MDRO, usually MRSA, to eradicate carriage of that organism. Although
some investigators have attempted to decolonize patients harboring VRE(220), few
have achieved success. However, decolonization of persons carrying MRSA in their
nares has proved possible with several regimens that include topical mupirocin alone
or in combination with orally administered antibiotics (e.g., rifampin in combination
with trimethoprim- sulfamethoxazole or ciprofloxacin) plus the use of an antimicrobial
soap for bathing(303). In one report, a 3-day regimen of baths with povidone-iodine
and nasal therapy with mupirocin resulted in eradication of nasal MRSA
27
colonization(304). These and other methods of MRSA decolonization have been
thoroughly reviewed.(303, 305-307).
Decolonization regimens are not sufficiently effective to warrant routine use.
Therefore, most healthcare facilities have limited the use of decolonization to MRSA
outbreaks, or other high prevalence situations, especially those affecting special-care
units. Several factors limit the utility of this control measure on a widespread basis: 1)
identification of candidates for decolonization requires surveillance cultures; 2)
candidates receiving decolonization treatment must receive follow-up cultures to
ensure eradication; and 3) recolonization with the same strain, initial colonization with
a mupirocin-resistant strain, and emergence of resistance to mupirocin during
treatment can occur(289, 303, 308-310). HCP implicated in transmission of MRSA
are candidates for decolonization and should be treated and culture negative before
returning to direct patient care. In contrast, HCP who are colonized with MRSA, but
are asymptomatic, and have not been linked epidemiologically to transmission, do
not require decolonization.
IV. Discussion
This review demonstrates the depth of published science on the prevention and control of
MDROs. Using a combination of interventions, MDROs in endemic, outbreak, and nonendemic settings have been brought under control. However, despite the volume of
literature, an appropriate set of evidence-based control measures that can be universally
applied in all healthcare settings has not been definitively established. This is due in part to
differences in study methodology and outcome measures, including an absence of
randomized, controlled trials comparing one MDRO control measure or strategy with
another. Additionally, the data are largely descriptive and quasi-experimental in
design(311). Few reports described preemptive efforts or prospective studies to control
MDROs before they had reached high levels within a unit or facility. Furthermore, small
hospitals and LTCFs are infrequently represented in the literature.
A number of questions remain and are discussed below.
28
Impact on other MDROS from interventions targeted to one MDRO Only one report
described control efforts directed at more than one MDRO, i.e., MDR-GNB and MRSA(312).
Several reports have shown either decreases or increases in other pathogens with efforts to
control one MDRO. For example, two reports on VRE control efforts demonstrated an
increase in MRSA following the prioritization of VRE patients to private rooms and cohort
beds(161). Similarly an outbreak of Serratia marcescens was temporally associated with a
concurrent, but unrelated, outbreak of MRSA in an NICU(313). In contrast, Wright and
colleagues reported a decrease in MRSA and VRE acquisition in an ICU during and after
their successful effort to eradicate an MDR-strain of A. baumannii from the unit(210).
Colonization with multiple MDROs appears to be common(314, 315). One study found that
nearly 50% of residents in a skilled-care unit in a LTCF were colonized with a target MDRO
and that 26% were co-colonized with >1 MDRO; a detailed analysis showed that risk factors
for colonization varied by pathogen(316). One review of the literature(317) reported that
patient risk factors associated with colonization with MRSA, VRE, MDR-GNB, C. difficile and
Candida sp were the same. This review concluded that control programs that focus on only
one organism or one antimicrobial drug are unlikely to succeed because vulnerable patients
will continue to serve as a magnet for other MDROs.
Costs. Several authors have provided evidence for the cost-effectiveness of approaches
that use ASC(153, 191, 253, 318, 319). However, the supportive evidence often relied on
assumptions, projections, and estimated attributable costs of MDRO infections. Similar
limitations apply to a study suggesting that gown use yields a cost benefit in controlling
transmission of VRE in ICUs(320). To date, no studies have directly compared the benefits
and costs associated with different MDRO control strategies.
Feasibility. The subject of feasibility, as it applies to the extrapolation of results to other
healthcare settings, has not been addressed. For example, smaller hospitals and LTCFs
may lack the on-site laboratory services needed to obtain ASC in a timely manner. This
factor could limit the applicability of an aggressive program based on obtaining ASC and
preemptive placement of patients on Contact Precautions in these settings. However, with
29
the growing problem of antimicrobial resistance, and the recognized role of all healthcare
settings for control of this problem, it is imperative that appropriate human and fiscal
resources be invested to increase the feasibility of recommended control strategies in every
setting.
Factors that influence selection of MDRO control measures. Although some common
principles apply, the preceding literature review indicates that no single approach to the
control of MDROs is appropriate for all healthcare facilities. Many factors influence the
choice of interventions to be applied within an institution, including:
•
Type and significance of problem MDROs within the institution. Many
facilities have an MRSA problem while others have ESBL-producing K.
pneumoniae. Some facilities have no VRE colonization or disease; others have
high rates of VRE colonization without disease; and still others have ongoing VRE
outbreaks. The magnitude of the problem also varies. Healthcare facilities may
have very low numbers of cases, e.g., with a newly introduced strain, or may have
prolonged, extensive outbreaks or colonization in the population. Between these
extremes, facilities may have low or high levels of endemic colonization and
variable levels of infection.
•
Population and healthcare-settings. The presence of high-risk patients (e.g.,
transplant, hematopoietic stem-cell transplant) and special-care units (e.g. adult,
pediatric, and neonatal ICUs; burn; hemodialysis) will influence surveillance
needs and could limit the areas of a facility targeted for MDRO control
interventions. Although it appears that MDRO transmission seldom occurs in
ambulatory and outpatient settings, some patient populations (e.g., hemodialysis,
cystic fibrosis) and patients receiving chemotherapeutic agents are at risk for
colonization and infection with MDROs. Furthermore, the emergence of VRSA
within the outpatient setting(22, 23, 25) demonstrates that even these settings
need to make MDRO prevention a priority.
30
Differences of opinion on the optimal strategy to control MDROs. Published guidance
on the control of MDROs reflects areas of ongoing debate on optimal control strategies. A
key issue is the use of ASC in control efforts and preemptive use of Contact Precautions
pending negative surveillance culture results(107, 321, 322). The various guidelines
currently available exhibit a spectrum of approaches, which their authors deem to be
evidence-based. One guideline for control of MRSA and VRE, the Society for Healthcare
Epidemiology of America (SHEA) guideline from 2003(107), emphasizes routine use of ASC
and Contact Precautions. That position paper does not address control of MDR-GNBs. The
salient features of SHEA recommendations for MRSA and VRE control and the
recommendations in this guideline for control of MDROs, including MRSA and VRE, have
been compared(323); recommended interventions are similar. Other guidelines for VRE
and MRSA, e.g., those proffered by the Michigan Society for Infection Control (www.msiconline.org/resource_sections/aro_guidelines), emphasize consistent practice of Standard
Precautions and tailoring the use of ASC and Contact Precautions to local conditions, the
specific MDROs that are prevalent and being transmitted, and the presence of risk factors
for transmission. A variety of approaches have reduced MDRO rates(3, 164, 165, 209, 214,
240, 269, 324). Therefore, selection of interventions for controlling MDRO transmission
should be based on assessments of the local problem, the prevalence of various MDRO
and feasibility. Individual facilities should seek appropriate guidance and adopt effective
measures that fit their circumstances and needs. Most studies have been in acute care
settings; for non-acute care settings (e.g., LCTF, small rural hospitals), the optimal approach
is not well defined.
Two-Tiered Approach for Control of MDROs. Reports describing successful
control of MDRO transmission in healthcare facilities have included seven categories of
interventions (Table 3). As a rule, these reports indicate that facilities confronted with an
MDRO problem selected a combination of control measures, implemented them, and
reassessed their impact. In some cases, new measures were added serially to further
enhance control efforts. This evidence indicates that the control of MDROs is a dynamic
process that requires a systematic approach tailored to the problem and healthcare setting.
The nature of this evidence gave rise to the two-tiered approach to MDRO control
31
recommended in this guideline. This approach provides the flexibility needed to prevent
and control MDRO transmission in every kind of facility addressed by this guideline.
Detailed recommendations for MDRO control in all healthcare settings follow and are
summarized in Table 3. Table 3, which applies to all healthcare settings, contains two tiers
of activities. In the first tier are the baseline level of MDRO control activities designed to
ensure recognition of MDROs as a problem, involvement of healthcare administrators, and
provision of safeguards for managing unidentified carriers of MDROs.
With the emergence of an MDRO problem that cannot be controlled with the basic set of
infection control measures, additional control measures should be selected from the second
tier of interventions presented in Table 3. Decisions to intensify MDRO control activity arise
from surveillance observations and assessments of the risk to patients in various settings.
Circumstances that may trigger these decisions include:
•
Identification of an MDRO from even one patient in a facility or special unit
with a highly vulnerable patient population (e.g., an ICU, NICU, burn unit) that
had previously not encountered that MDRO.
•
Failure to decrease the prevalence or incidence of a specific MDRO (e.g.,
incidence of resistant clinical isolates) despite infection control efforts to stop
its transmission.(Statistical process control charts or other validated methods
that account for normal variation can be used to track rates of targeted
MDROs)(205, 325, 326).
The combination of new or increased frequency of MDRO isolates and patients at risk
necessitates escalation of efforts to achieve or re-establish control, i.e., to reduce rates of
transmission to the lowest possible level. Intensification of MDRO control activities should
begin with an assessment of the problem and evaluation of the effectiveness of measures in
current use. Once the problem is defined, appropriate additional control measures should
be selected from the second tier of Table 3. A knowledgeable infection prevention and
control professional or healthcare epidemiologist should make this determination. This
approach requires support from the governing body and medical staff of the facility. Once
interventions are implemented, ongoing surveillance should be used to determine whether
selected control measures are effective and if additional measures or consultation are
32
indicated. The result of this process should be to decrease MDRO rates to minimum levels.
Healthcare facilities must not accept ongoing MDRO outbreaks or high endemic rates as the
status quo. With selection of infection control measures appropriate to their situation, all
facilities can achieve the desired goal and reduce the MDRO burden substantially.
33
V. Prevention of transmission of Multidrug Resistant Organisms
(Table 3)
The CDC/HICPAC system for categorizing recommendations is as follows:
Category IA Strongly recommended for implementation and strongly supported by welldesigned experimental, clinical, or epidemiologic studies.
Category IB Strongly recommended for implementation and supported by some
experimental, clinical, or epidemiologic studies and a strong theoretical rationale.
Category IC Required for implementation, as mandated by federal and/or state regulation
or standard.
Category II Suggested for implementation and supported by suggestive clinical or
epidemiologic studies or a theoretical rationale.
No recommendation Unresolved issue. Practices for which insufficient evidence or no
consensus regarding efficacy exists.
V.A.
General recommendations for all healthcare settings independent of the prevalence
of multidrug resistant organism (MDRO) infections or the population served.
V.A.1.
Administrative measures
V.A.1.a. Make MDRO prevention and control an organizational patient safety
priority.(3, 146, 151, 154, 182, 185, 194, 205, 208, 210, 242, 327, 328)
Category IB
V.A.1.b. Provide administrative support, and both fiscal and human resources, to
prevent and control MDRO transmission within the healthcare organization
(3, 9, 146, 152, 182-184, 208, 328, 329) Category IB
V.A.1.c. In healthcare facilities without expertise for analyzing epidemiologic data,
recognizing MDRO problems, or devising effective control strategies (e.g.,
small or rural hospitals, rehabilitation centers, long-term care facilities
[LTCFs], freestanding ambulatory centers), identify experts who can
provide consultation as needed.(151, 188) Category II
V.A.1.d. Implement systems to communicate information about reportable MDROs
[e.g., VRSA, VISA, MRSA, Penicillin resistant S. pneumoniae(PRSP)] to
administrative personnel and as required by state and local health
34
authorities (www.cdc.gov/epo/dphsi/nndsshis.htm). Refer to websites for
updated requirements of local and state health departments. Category II/IC
V.A.1.e. Implement a multidisciplinary process to monitor and improve healthcare
personnel (HCP) adherence to recommended practices for Standard and
Contact Precautions(3, 105, 182, 184, 189, 242, 273, 312, 330). Category
IB
V.A.1.f.
Implement systems to designate patients known to be colonized or infected
with a targeted MDRO and to notify receiving healthcare facilities and
personnel prior to transfer of such patients within or between facilities.(87,
151) Category IB
V.A.1.g. Support participation of the facility or healthcare system in local, regional,
and national coalitions to combat emerging or growing MDRO
problems.(41, 146, 151, 167, 188, 206, 207, 211, 331). Category IB
V.A.1.h. Provide updated feedback at least annually to healthcare providers and
administrators on facility and patient-care-unit trends in MDRO infections.
Include information on changes in prevalence or incidence of infection,
results of assessments for system failures, and action plans to improve
adherence to and effectiveness of recommended infection control practices
to prevent MDRO transmission.(152, 154, 159, 184, 204, 205, 242, 312,
332) Category IB
V.A.2.
Education and training of healthcare personnel
V.A.2.a. Provide education and training on risks and prevention of MDRO
transmission during orientation and periodic educational updates for
healthcare personnel; include information on organizational experience
with MDROs and prevention strategies.(38, 152, 154, 173, 176, 189, 190,
203, 204, 217, 242, 330, 333, 334) Category IB
V.A.3.
Judicious use of antimicrobial agents. The goal of the following
recommendations is to ensure that systems are in place to promote optimal
treatment of infections and appropriate antimicrobial use.
V.A.3.a. In hospitals and LTCFs, ensure that a multidisciplinary process is in place
to review antimicrobial utilization, local susceptibility patterns
35
(antibiograms), and antimicrobial agents included in the formulary to foster
appropriate antimicrobial use.(209, 212, 214, 215, 217, 242, 254, 334-339)
Category IB
V.A.3.b. Implement systems (e.g., computerized physician order entry, comment in
microbiology susceptibility report, notification from a clinical pharmacist or
unit director) to prompt clinicians to use the appropriate antimicrobial agent
and regimen for the given clinical situation.(156, 157, 161, 166, 174, 175,
212, 214, 218, 254, 334, 335, 337, 340-346) Category IB
V.A.3.b.i.
Provide clinicians with antimicrobial susceptibility reports and
analysis of current trends, updated at least annually, to guide
antimicrobial prescribing practices.(342, 347) Category IB
V.A.3.b.ii.
In settings that administer antimicrobial agents but have limited
electronic communication system infrastructures to implement
physician prompts (e.g., LTCFs, home care and infusion
companies), implement a process for appropriate review of
prescribed antimicrobials. Prepare and distribute reports to
prescribers that summarize findings and provide suggestions for
improving antimicrobial use. (342, 348, 349) Category II
V.A.4.
Surveillance
V.A.4.a. In microbiology laboratories, use standardized laboratory methods and
follow published guidance for determining antimicrobial susceptibility of
targeted (e.g., MRSA, VRE, MDR-ESBLs) and emerging (e.g., VRSA,
MDR-Acinetobacter baumannii) MDROs.(8, 154, 177, 190, 193, 209, 254,
347, 350-353) Category IB
V.A.4.b.
In all healthcare organizations, establish systems to ensure that clinical
microbiology laboratories (in-house and out-sourced) promptly notify
infection control staff or a medical director/ designee when a novel
resistance pattern for that facility is detected.(9, 22, 154, 162, 169)
Category IB
V.A.4.c. In hospitals and LTCFs, develop and implement laboratory protocols for
storing isolates of selected MDROs for molecular typing when needed to
36
confirm transmission or delineate the epidemiology of the MDRO within the
healthcare setting.(7, 8, 38, 140, 153, 154, 187, 190, 208, 217, 354, 355)
Category IB
V.A.4.d. Prepare facility-specific antimicrobial susceptibility reports as
recommended by the Clinical and Laboratory Standards Institute (CLSI)
(www.phppo.cdc.gov/dls/master/default.aspx); monitor these reports for
evidence of changing resistance patterns that may indicate the emergence
or transmission of MDROs.(347, 351, 356, 357) Category IB/IC
V.A.4.d.i.
In hospitals and LTCFs with special-care units (e.g., ventilatordependent, ICU, or oncology units), develop and monitor unitspecific antimicrobial susceptibility reports.(358-361)
V.A.4.d.ii.
Category IB
Establish a frequency for preparing summary reports based on
volume of clinical isolates, with updates at least annually.(347, 362)
Category II/IC
V.A.4.d.iii.
In healthcare organizations that outsource microbiology laboratory
services (e.g., ambulatory care, home care, LTCFs, smaller acute
care hospitals), specify by contract that the laboratory provide either
facility-specific susceptibility data or local or regional aggregate
susceptibility data in order to identify prevalent MDROs and trends
in the geographic area served.(363) Category II
V.A.4.e. Monitor trends in the incidence of target MDROs in the facility over time
using appropriate statistical methods to determine whether MDRO rates
are decreasing and whether additional interventions are needed.(152, 154,
183, 193, 205, 209, 217, 242, 300, 325, 326, 364, 365) Category IA
V.A.4.e.i.
Specify isolate origin (i.e., location and clinical service) in MDRO
monitoring protocols in hospitals and other large multi-unit facilities
with high-risk patients.(8, 38, 152-154, 217, 358, 361) Category IB
V.A.4.e.ii.
Establish a baseline (e.g., incidence) for targeted MDRO isolates by
reviewing results of clinical cultures; if more timely or localized
information is needed, perform baseline point prevalence studies of
colonization in high-risk units. When possible, distinguish
37
colonization from infection in analysis of these data.(152, 153, 183,
184, 189, 190, 193, 205, 242, 365) Category IB
V.A.5.
Infection control precautions to prevent transmission of MDROs
V.A.5.a. Follow Standard Precautions during all patient encounters in all settings in
which healthcare is delivered.(119, 164, 255, 315, 316) Category IB
V.A.5.b. Use masks according to Standard Precautions when performing splashgenerating procedures (e.g., wound irrigation, oral suctioning, intubation);
when caring for patients with open tracheostomies and the potential for
projectile secretions; and in circumstances where there is evidence of
transmission from heavily colonized sources (e.g., burn wounds). Masks
are not otherwise recommended for prevention of MDRO transmission
from patients to healthcare personnel during routine care (e.g., upon room
entry).(8, 22, 151, 152, 154, 189, 190, 193, 208, 240, 366) Category IB
V.A.5.c. Use of Contact Precautions
V.A.5.c.i.
In acute-care hospitals, implement Contact Precautions routinely for
all patients infected with target MDROs and for patients that have
been previously identified as being colonized with target MDROs
(e.g., patients transferred from other units or facilities who are
known to be colonized). (11, 38, 68, 114, 151, 183, 188, 204, 217,
242, 304) Category IB
V.A.5.c.ii.
In LTCFs, consider the individual patient’s clinical situation and
prevalence or incidence of MDRO in the facility when deciding
whether to implement or modify Contact Precautions in addition to
Standard Precautions for a patient infected or colonized with a
target MDRO. Category II
V.A.5.c.ii.1. For relatively healthy residents (e.g., mainly independent) follow
Standard Precautions, making sure that gloves and gowns are
used for contact with uncontrolled secretions, pressure ulcers,
draining wounds, stool incontinence, and ostomy tubes/bags. (7880, 85, 151, 367, 368) Category II
38
V.A.5.c.ii.2. For ill residents (e.g., those totally dependent upon healthcare
personnel for healthcare and activities of daily living, ventilatordependent) and for those residents whose infected secretions or
drainage cannot be contained, use Contact Precautions in
addition to Standard Precautions.(316, 369, 370) Category II
V.A.5.c.iii.
For MDRO colonized or infected patients without draining wounds,
diarrhea, or uncontrolled secretions, establish ranges of permitted
ambulation, socialization, and use of common areas based on their
risk to other patients and on the ability of the colonized or infected
patients to observe proper hand hygiene and other recommended
precautions to contain secretions and excretions.(151, 163, 371)
Category II
V.A.5.d. In ambulatory settings, use Standard Precautions for patients known to be
infected or colonized with target MDROs, making sure that gloves and
gowns are used for contact with uncontrolled secretions, pressure ulcers,
draining wounds, stool incontinence, and ostomy tubes and bags. Category
II
V.A.5.e. In home care settings
y
Follow Standard Precautions making sure to use gowns and
gloves for contact with uncontrolled secretions, pressure ulcers,
draining wounds, stool incontinence, and ostomy tubes and
bags. Category II
y
Limit the amount of reusable patient-care equipment that is
brought into the home of patients infected or colonized with
MDROs. When possible, leave patient-care equipment in the
home until the patient is discharged from home care services.
Category II
y
If noncritical patient-care equipment (e.g., stethoscopes) cannot
remain in the home, clean and disinfect items before removing
them from the home, using a low to intermediate level
disinfectant, or place reusable items in a plastic bag for transport
39
to another site for subsequent cleaning and disinfection.
Category II
V.A.5.e.i.
No recommendation is made for routine use of gloves, gowns, or
both to prevent MDRO transmission in ambulatory or home care
settings. Unresolved issue
V.A.5.e.ii.
In hemodialysis units, follow the “Recommendations to Prevent
Transmission of Infections in Chronic Hemodialysis
Patients”(372)(www.cms.hhs.gov/home/regsguidance.asp).
Category IC
V.A.5.f.
Discontinuation of Contact Precautions. No recommendation can be made
regarding when to discontinue Contact Precautions. Unresolved issue (See
Background for discussion of options)
V.A.5.g. Patient placement in hospitals and LTCFs
V.A.5.g.i.
When single-patient rooms are available, assign priority for these
rooms to patients with known or suspected MDRO colonization or
infection. Give highest priority to those patients who have conditions
that may facilitate transmission, e.g., uncontained secretions or
excretions.(8, 38, 110, 151, 188, 208, 240, 304) Category IB
V.A.5.g.ii.
When single-patient rooms are not available, cohort patients with
the same MDRO in the same room or patient-care area.(8, 38, 92,
151-153, 162, 183, 184, 188, 217, 242, 304) Category IB
V.A.5.g.iii.
When cohorting patients with the same MDRO is not possible, place
MDRO patients in rooms with patients who are at low risk for
acquisition of MDROs and associated adverse outcomes from
infection and are likely to have short lengths of stay. Category II
V.A.6.
Environmental measures
V.A.6.a. Clean and disinfect surfaces and equipment that may be contaminated with
pathogens, including those that are in close proximity to the patient (e.g.,
bed rails, over bed tables) and frequently-touched surfaces in the patient
care environment (e.g., door knobs, surfaces in and surrounding toilets in
patients’ rooms) on a more frequent schedule compared to that for minimal
40
touch surfaces (e.g., horizontal surfaces in waiting rooms).(111, 297, 373)
Category IB
V.A.6.b. Dedicate noncritical medical items to use on individual patients known to
be infected or colonized with MDROs.(38, 217, 324, 374, 375) Category
IB
V.A.6.c.
Prioritize room cleaning of patients on Contact Precautions. Focus on
cleaning and disinfecting frequently touched surfaces (e.g., bedrails,
bedside commodes, bathroom fixtures in the patient’s room, doorknobs)
and equipment in the immediate vicinity of the patient.(109, 110, 114-117,
297, 301, 373, 376, 377) Category IB
V.B.
Intensified interventions to prevent MDRO transmission
The interventions presented below have been utilized in various combinations to
reduce transmission of MDROs in healthcare facilities. Neither the effectiveness of
individual components nor that of specific combinations of control measures has
been assessed in controlled trials. Nevertheless, various combinations of control
elements selected under the guidance of knowledgeable content experts have
repeatedly reduced MDRO transmission rates in a variety of healthcare settings.
V.B.1.
Indications and approach
V.B.1.a. Indications for intensified MDRO control efforts (VII.B.1.a.i and VII.B.1.a.ii)
should result in selection and implementation of one or more of the
interventions described in VII.B.2 to VII.B.8 below. Individualize the
selection of control measures according to local considerations(8, 11, 38,
68, 114, 152-154, 183-185, 189, 190, 193, 194, 209, 217, 242, 312, 364,
365). Category IB
V.B.1.a.i.
When incidence or prevalence of MDROs are not decreasing
despite implementation of and correct adherence to the routine
control measures described above, intensify MDRO control efforts
by adopting one or more of the interventions described below.(92,
152, 183, 184, 193, 365) Category IB
V.B.1.a.ii.
When the first case or outbreak of an epidemiologically important
MDRO (e.g., VRE, MRSA, VISA, VRSA, MDR-GNB) is identified
41
within a healthcare facility or unit.(22, 23, 25, 68, 170, 172, 184,
240, 242, 378) Category IB
V.B.1.b. Continue to monitor the incidence of target MDRO infection and
colonization after additional interventions are implemented. If rates do not
decrease, implement more interventions as needed to reduce MDRO
transmission.(11, 38, 68, 92, 152, 175, 184, 365) Category IB
V.B.2.
Administrative measures
V.B.2.a. Identify persons with experience in infection control and the epidemiology
of MDRO, either in house or through outside consultation, for assessment
of the local MDRO problem and for the design, implementation, and
evaluation of appropriate control measures (3, 68, 146, 151-154, 167, 184,
190, 193, 242, 328, 377). Category IB
V.B.2.b. Provide necessary leadership, funding, and day-to-day oversight to
implement interventions selected. Involve the governing body and
leadership of the healthcare facility or system that have organizational
responsibility for this and other infection control efforts.(8, 38, 152, 154,
184, 189, 190, 208) Category IB
V.B.2.c. Evaluate healthcare system factors for their role in creating or perpetuating
transmission of MDROs, including: staffing levels, education and training,
availability of consumable and durable resources, communication
processes, policies and procedures, and adherence to recommended
infection control measures (e.g., hand hygiene and Standard or Contact
Precautions). Develop, implement, and monitor action plans to correct
system failures.(3, 8, 38, 152, 154, 172, 173, 175, 188, 196, 198, 199, 208,
217, 280, 324, 379, 380) Category IB
V.B.2.d. During the process, update healthcare providers and administrators on the
progress and effectiveness of the intensified interventions. Include
information on changes in prevalence, rates of infection and colonization;
results of assessments and corrective actions for system failures; degrees
of adherence to recommended practices; and action plans to improve
42
adherence to recommended infection control practices to prevent MDRO
transmission.(152, 154, 159, 184, 204, 205, 312, 332, 381) Category IB
V.B.3.
Educational interventions
Intensify the frequency of MDRO educational programs for healthcare
personnel, especially those who work in areas in which MDRO rates are not
decreasing. Provide individual or unit-specific feedback when available.(3, 38,
152, 154, 159, 170, 182, 183, 189, 190, 193, 194, 204, 205, 209, 215, 218,
312) Category IB
V.B.4.
Judicious use of antimicrobial agents
Review the role of antimicrobial use in perpetuating the MDRO problem
targeted for intensified intervention. Control and improve antimicrobial use as
indicated. Antimicrobial agents that may be targeted include vancomycin,
third-generation cephalosporins, and anti-anaerobic agents for VRE(217);
third-generation cephalosporins for ESBLs(212, 214, 215); and quinolones
and carbapenems(80, 156, 166, 174, 175, 209, 218, 242, 254, 329, 334, 335,
337, 341). Category IB
V.B.5.
Surveillance
V.B.5.a. Calculate and analyze prevalence and incidence rates of targeted MDRO
infection and colonization in populations at risk; when possible, distinguish
colonization from infection(152, 153, 183, 184, 189, 190, 193, 205, 215,
242, 365). Category IB
V.B.5.a.i.
Include only one isolate per patient, not multiple isolates from the
same patient, when calculating rates(347, 382). Category II
V.B.5.a.ii.
Increase the frequency of compiling and monitoring antimicrobial
susceptibility summary reports for a targeted MDRO as indicated by
an increase in incidence of infection or colonization with that MDRO.
Category II
V.B.5.b. Develop and implement protocols to obtain active surveillance cultures
(ASC) for targeted MDROs from patients in populations at risk (e.g.,
patients in intensive care, burn, bone marrow/stem cell transplant, and
oncology units; patients transferred from facilities known to have high
43
MDRO prevalence rates; roommates of colonized or infected persons; and
patients known to have been previously infected or colonized with an
MDRO).(8, 38, 68, 114, 151-154, 167, 168, 183, 184, 187-190, 192, 193,
217, 242) Category IB
V.B.5.b.i.
Obtain ASC from areas of skin breakdown and draining wounds. In
addition, include the following sites according to target MDROs:
V.B.5.b.i.1.
For MRSA: Sampling the anterior nares is usually sufficient;
throat, endotracheal tube aspirate, percutaneous gastrostomy
sites, and perirectal or perineal cultures may be added to increase
the yield. Swabs from several sites may be placed in the same
selective broth tube prior to transport.(117, 383, 384) Category IB
V.B.5.b.i.2.
For VRE: Stool, rectal, or perirectal samples should be
collected.(154, 193, 217, 242)
Category IB
V.B.5.b.i.3.
For MDR-GNB: Endotracheal tube aspirates or sputum should
be cultured if a respiratory tract reservoir is suspected, (e.g.,
Acinetobacter spp., Burkholderia spp.).(385, 386) Category IB.
V.B.5.b.ii.
Obtain surveillance cultures for the target MDRO from patients at
the time of admission to high-risk areas, e.g., ICUs, and at periodic
intervals as needed to assess MDRO transmission.(8, 151, 154,
159, 184, 208, 215, 242, 387) Category IB
V.B.5.c.
Conduct culture surveys to assess the efficacy of the enhanced MDRO
control interventions.
V.B.5.c.i.
Conduct serial (e.g., weekly, until transmission has ceased and then
decreasing frequency) unit-specific point prevalence culture surveys
of the target MDRO to determine if transmission has decreased or
ceased.(107, 167, 175, 184, 188, 218, 339) Category IB
V.B.5.c.ii.
Repeat point-prevalence culture surveys at routine intervals or at
time of patient discharge or transfer until transmission has
ceased.(8, 152-154, 168, 178, 190, 215, 218, 242, 388) Category IB
44
V.B.5.c.iii.
If indicated by assessment of the MDRO problem, collect cultures to
asses the colonization status of roommates and other patients with
substantial exposure to patients with known MDRO infection or
colonization.(25, 68, 167, 193) Category IB
V.B.5.d. Obtain cultures of healthcare personnel for target MDRO when there is
epidemiologic evidence implicating the healthcare staff member as a
source of ongoing transmission.(153, 365) Category IB
V.B.6.
Enhanced infection control precautions
V.B.6.a. Use of Contact Precautions
V.B.6.a.i.
Implement Contact Precautions routinely for all patients colonized or
infected with a target MDRO.(8, 11, 38, 68, 114, 151, 154, 183, 188,
189, 217, 242, 304) Category IA
V.B.6.a.ii.
Because environmental surfaces and medical equipment, especially
those in close proximity to the patient, may be contaminated, don
gowns and gloves before or upon entry to the patient’s room or
cubicle.(38, 68, 154, 187, 189, 242) Category IB
V.B.6.a.iii.
In LTCFs, modify Contact Precautions to allow MDROcolonized/infected patients whose site of colonization or infection
can be appropriately contained and who can observe good hand
hygiene practices to enter common areas and participate in group
activities.(78, 86, 151, 367) Category IB
V.B.6.b. When ASC are obtained as part of an intensified MDRO control program,
implement Contact Precautions until the surveillance culture is reported
negative for the target MDRO.(8, 30, 153, 389, 390) Category IB
V.B.6.c. No recommendation is made regarding universal use of gloves, gowns, or
both in high-risk units in acute-care hospitals.(153, 273, 312, 320, 391)
Unresolved issue
V.B.7.
Implement policies for patient admission and placement as needed to prevent
transmission of a problem MDRO.(183, 184, 189, 193, 242, 339, 392)
Category IB
45
V.B.7.a.i.
Place MDRO patients in single-patient rooms.(6, 151, 158, 160, 166,
170, 187, 208, 240, 282, 393-395) Category IB
V.B.7.a.ii.
Cohort patients with the same MDRO in designated areas (e.g.,
rooms, bays, patient care areas.(8, 151, 152, 159, 161, 176, 181,
183, 184, 188, 208, 217, 242, 280, 339, 344) Category IB
V.B.7.a.iii.
When transmission continues despite adherence to Standard and
Contact Precautions and cohorting patients, assign dedicated
nursing and ancillary service staff to the care of MDRO patients
only. Some facilities may consider this option when intensified
measures are first implemented.(184, 217, 242, 278) Category IB
V.B.7.a.iv.
Stop new admissions to the unit of facility if transmission continues
despite the implementation of the enhanced control measures
described above. (Refer to state or local regulations that may apply
upon closure of hospital units or services.).(9, 38, 146, 159, 161,
168, 175, 205, 279, 280, 332, 339, 396) Category IB
V.B.8.
Enhanced environmental measures
V.B.8.a. Implement patient-dedicated or single-use disposable noncritical
equipment (e.g., blood pressure cuff, stethoscope) and instruments and
devices.(38, 104, 151, 156, 159, 163, 181, 217, 324, 329, 367, 389, 390,
394) Category IB
V.B.8.b. Intensify and reinforce training of environmental staff who work in areas
targeted for intensified MDRO control and monitor adherence to
environmental cleaning policies. Some facilities may choose to assign
dedicated staff to targeted patient care areas to enhance consistency of
proper environmental cleaning and disinfection services.(38, 154, 159, 165,
172, 173, 175, 178-181, 193, 205, 208, 217, 279, 301, 327, 339, 397)
Category IB
V.B.8.c.
Monitor (i.e., supervise and inspect) cleaning performance to ensure
consistent cleaning and disinfection of surfaces in close proximity to the
patient and those likely to be touched by the patient and HCP (e.g.,
46
bedrails, carts, bedside commodes, doorknobs, faucet handles).(8, 38,
109, 111, 154, 169, 180, 208, 217, 301, 333, 398) Category IB
V.B.8.d. Obtain environmental cultures (e.g., surfaces, shared medical equipment)
when there is epidemiologic evidence that an environmental source is
associated with ongoing transmission of the targeted MDRO.(399-402)
Category IB
V.B.8.e. Vacate units for environmental assessment and intensive cleaning when
previous efforts to eliminate environmental reservoirs have failed.(175,
205, 279, 339, 403) Category II
V.B.9.
Decolonization
V.B.9.a. Consult with physicians with expertise in infectious diseases and/or
healthcare epidemiology on a case-by-case basis regarding the
appropriate use of decolonization therapy for patients or staff during limited
periods of time, as a component of an intensified MRSA control program
).(152, 168, 170, 172, 183, 194, 304) Category II
V.B.9.b. When decolonization for MRSA is used, perform susceptibility testing for
the decolonizing agent against the target organism in the individual being
treated or the MDRO strain that is epidemiologically implicated in
transmission. Monitor susceptibility to detect emergence of resistance to
the decolonizing agent. Consult with a microbiologist for appropriate testing
for mupirocin resistance, since standards have not been established.(289,
290, 304, 308) Category IB
V.B.9.b.i.
Because mupirocin-resistant strains may emerge and because it is
unusual to eradicate MRSA when multiple body sites are colonized,
do not use topical mupirocin routinely for MRSA decolonization of
patients as a component of MRSA control programs in any
healthcare setting.(289, 404) Category IB
V.B.9.b.ii.
Limit decolonization of HCP found to be colonized with MRSA to
persons who have been epidemiologically linked as a likely source
of ongoing transmission to patients. Consider reassignment of HCP
47
if decolonization is not successful and ongoing transmission to
patients persists.(120, 122, 168) Category IB
V.B.9.c. No recommendation can be made for decolonizing patients with VRE or
MDR-GNB. Regimens and efficacy of decolonization protocols for VRE and
MDR-GNB have not been established.(284, 286, 288, 307, 387, 405)
Unresolved issue
48
Glossary - Multidrug-Resistant Organisms
Ambulatory care settings. Facilities that provide health care to patients who do not remain
overnight (e.g., hospital-based outpatient clinics, nonhospital-based clinics and physician
offices, urgent care centers, surgicenters, free-standing dialysis centers, public health
clinics, imaging centers, ambulatory behavioral health and substance abuse clinics, physical
therapy and rehabilitation centers, and dental practices.
Cohorting. In the context of this guideline, this term applies to the practice of grouping
patients infected or colonized with the same infectious agent together to confine their care
to one area and prevent contact with susceptible patients (cohorting patients). During
outbreaks, healthcare personnel may be assigned to a cohort of patients to further limit
opportunities for transmission (cohorting staff).
Contact Precautions. Contact Precautions are a set of practices used to prevent
transmission of infectious agents that are spread by direct or indirect contact with the patient
or the patient’s environment. Contact Precautions also apply where the presence of
excessive wound drainage, fecal incontinence, or other discharges from the body suggest
an increased transmission risk. A single patient room is preferred for patients who require
Contact Precautions. When a single patient room is not available, consultation with infection
control is helpful to assess the various risks associated with other patient placement options
(e.g., cohorting, keeping the patient with an existing roommate). In multi-patient rooms, >3
feet spatial separation of between beds is advised to reduce the opportunities for
inadvertent sharing of items between the infected/colonized patient and other patients.
Healthcare personnel caring for patients on Contact Precautions wear a gown and gloves
for all interactions that may involve contact with the patient or potentially contaminated
areas in the patient’s environment. Donning of gown and gloves upon room entry, removal
before exiting the patient room and performance of hand hygiene immediately upon exiting
are done to contain pathogens.
49
Epidemiologically important pathogens. Infectious agents that have one or more of the
following characteristics: 1)A propensity for transmission within healthcare facilities based
on published reports and the occurrence of temporal or geographic clusters of > 2 patients,
(e.g., VRE, MRSA and MSSA, Clostridium difficile, norovirus, RSV, influenza, rotavirus,
Enterobacter spp; Serratia spp., group A streptococcus). However, for group A
streptococcus, most experts consider a single case of healthcare-associated disease a
trigger for investigation and enhanced control measures because of the devastating
outcomes associated with HAI group A streptococcus infections. For susceptible bacteria
that are known to be associated with asymptomatic colonization, isolation from normally
sterile body fluids in patients with significant clinical disease would be the trigger to consider
the organism as epidemiologically important. 2) Antimicrobial resistance implications:
o Resistance to first-line therapies (e.g., MRSA, VRE, VISA, VRSA, ESBLproducing organisms).
o Unusual or usual agents with unusual patterns of resistance within a facility,
(e.g., the first isolate of Burkholderia cepacia complex or Ralstonia spp. in
non-CF patients or a quinolone-resistant strain of Pseudomonas in a facility.
o Difficult to treat because of innate or acquired resistance to multiple classes of
antimicrobial agents (e.g., Stenotrophomonas maltophilia, Acinetobacter spp.).
3) Associated with serious clinical disease, increased morbidity and mortality (e.g., MRSA
and MSSA, group A streptococcus); or 4) A newly discovered or reemerging pathogen. The
strategies described for MDROs may be applied for control of epidemiologically important
organisms other than MDROs.
Hand hygiene. A general term that applies to any one of the following: 1) handwashing with
plain (nonantimicrobial) soap and water); 2) antiseptic hand wash (soap containing
antiseptic agents and water); 3) antiseptic hand rub (waterless antiseptic product, most
often alcohol-based, rubbed on all surfaces of hands); or 4) surgical hand antisepsis
50
(antiseptic hand wash or antiseptic hand rub performed preoperatively by surgical personnel
to eliminate transient hand flora and reduce resident hand flora).
Healthcare-associated infection (HAI). An infection that develops in a patient who is cared
for in any setting where healthcare is delivered (e.g., acute care hospital, chronic care
facility, ambulatory clinic, dialysis center, surgicenter, home) and is related to receiving
health care (i.e., was not incubating or present at the time healthcare was provided). In
ambulatory and home settings, HAI would apply to any infection that is associated with a
medical or surgical intervention performed in those settings.
Healthcare epidemiologist A person whose primary training is medical (M.D., D.O.) and/or
masters or doctorate-level epidemiology who has received advanced training in healthcare
epidemiology. Typically these professionals direct or provide consultation to an infection
prevention and control program in a hospital, long term care facility (LTCF), or healthcare
delivery system (also see infection prevention and control professional).
Healthcare personnel (HCP). All paid and unpaid persons who work in a healthcare
setting, also known as healthcare workers (e.g. any person who has professional or
technical training in a healthcare-related field and provides patient care in a healthcare
setting or any person who provides services that support the delivery of healthcare such as
dietary, housekeeping, engineering, maintenance personnel).
Home care. A wide-range of medical, nursing, rehabilitation, hospice, and social services
delivered to patients in their place of residence (e.g., private residence, senior living center,
assisted living facility). Home health-care services include care provided by home health
aides and skilled nurses, respiratory therapists, dieticians, physicians, chaplains, and
volunteers; provision of durable medical equipment; home infusion therapy; and physical,
speech, and occupational therapy.
Infection prevention and control professional (ICP). A person whose primary training is
in either nursing, medical technology, microbiology, or epidemiology and who has acquired
51
specialized training in infection control. Responsibilities may include collection, analysis, and
feedback of infection data and trends to healthcare providers; consultation on infection risk
assessment, prevention and control strategies; performance of education and training
activities; implementation of evidence-based infection control practices or those mandated
by regulatory and licensing agencies; application of epidemiologic principles to improve
patient outcomes; participation in planning renovation and construction projects (e.g., to
ensure appropriate containment of construction dust); evaluation of new products or
procedures on patient outcomes; oversight of employee health services related to infection
prevention; implementation of preparedness plans; communication within the healthcare
setting, with local and state health departments, and with the community at large concerning
infection control issues; and participation in research.
Infection prevention and control program. A multidisciplinary program that includes a
group of activities to ensure that recommended practices for the prevention of healthcareassociated infections are implemented and followed by healthcare personnel, making the
healthcare setting safe from infection for patients and healthcare personnel. The Joint
Commission on Accreditation of Healthcare Organizations (JCAHO) requires the following
five components of an infection prevention and control program for accreditation: 1)
surveillance: monitoring patients and healthcare personnel for acquisition of infection and/or
colonization; 2) investigation: identification and analysis of infection problems or undesirable
trends; 3) prevention: implementation of measures to prevent transmission of infectious
agents and to reduce risks for device- and procedure-related infections; 4) control:
evaluation and management of outbreaks; and 5) reporting: provision of information to
external agencies as required by state and federal law and regulation (www.jcaho.org). The
infection prevention and control program staff has the ultimate authority to determine
infection control policies for a healthcare organization with the approval of the organization’s
governing body.
Long-term care facilities (LTCFs).An array of residential and outpatient facilities designed
to meet the bio-psychosocial needs of persons with sustained self-care deficits. These
include skilled nursing facilities, chronic disease hospitals, nursing homes, foster and group
homes, institutions for the developmentally disabled, residential care facilities, assisted
52
living facilities, retirement homes, adult day health care facilities, rehabilitation centers, and
long-term psychiatric hospitals.
Mask. A term that applies collectively to items used to cover the nose and mouth and
includes both procedure masks and surgical masks
(www.fda.gov/cdrh/ode/guidance/094.html#4).
Multidrug-resistant organisms (MDROs). In general, bacteria (excluding M. tuberculosis)
that are resistant to one or more classes of antimicrobial agents and usually are resistant to
all but one or two commercially available antimicrobial agents (e.g., MRSA, VRE, extended
spectrum beta-lactamase [ESBL]-producing or intrinsically resistant gram-negative bacilli).
Nosocomial infection. Derived from two Greek words “nosos” (disease) and “komeion” (to
take care of). Refers to any infection that develops during or as a result of an admission to
an acute care facility (hospital) and was not incubating at the time of admission.
Standard Precautions. A group of infection prevention practices that apply to all patients,
regardless of suspected or confirmed diagnosis or presumed infection status. Standard
Precautions are a combination and expansion of Universal Precautions and Body
Substance Isolation. Standard Precautions are based on the principle that all blood, body
fluids, secretions, excretions except sweat, nonintact skin, and mucous membranes may
contain transmissible infectious agents. Standard Precautions includes hand hygiene, and
depending on the anticipated exposure, use of gloves, gown, mask, eye protection, or face
shield. Also, equipment or items in the patient environment likely to have been
contaminated with infectious fluids must be handled in a manner to prevent transmission of
infectious agents, (e.g. wear gloves for handling, contain heavily soiled equipment, properly
clean and disinfect or sterilize reusable equipment before use on another patient).
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1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
IOM (1998), eds. Harrison, P. F. & Lederberg, J. (National Academy Press, Washington,
DC), pp. 8-74.
Shlaes, D. M., Gerding, D. N., John, J. F., Jr., Craig, W. A., Bornstein, D. L., Duncan, R. A.,
Eckman, M. R., Farrer, W. E., Greene, W. H., Lorian, V., et al. (1997) Infect Control Hosp
Epidemiol 18, 275-291.
Larson, E. L., Early, E., Cloonan, P., Sugrue, S., & Parides, M. (2000) Behav Med 26, 14-22.
Goldmann, D. A., Weinstein, R. A., Wenzel, R. P., Tablan, O. C., Duma, R. J., Gaynes, R. P.,
Schlosser, J., & Martone, W. J. (1996) JAMA 275, 234-240.
Murthy, R. (2001) Chest 119, 405S-411S.
Mahgoub, S., Ahmed, J., & Glatt, A. E. (2002) Infect Control Hosp Epidemiol 23, 477-479.
Fournier, P. E. & Richet, H. (2006) Clin Infect Dis 42, 692-699.
Fierobe, L., Lucet, J. C., Decre, D., Muller-Serieys, C., Deleuze, A., Joly-Guillou, M. L.,
Mantz, J., & Desmonts, J. M. (2001) Infect Control Hosp Epidemiol 22, 35-40.
Ling, M. L., Ang, A., Wee, M., & Wang, G. C. (2001) Infect Control Hosp Epidemiol 22, 4849.
Landman, D., Quale, J. M., Mayorga, D., Adedeji, A., Vangala, K., Ravishankar, J., Flores,
C., & Brooks, S. (2002) Arch Intern Med 162, 1515-1520.
Urban, C., Segal-Maurer, S., & Rahal, J. J. (2003) Clin Infect Dis 36, 1268-1274.
Gales, A. C., Jones, R. N., Forward, K. R., Linares, J., Sader, H. S., & Verhoef, J. (2001) Clin
Infect Dis 32 Suppl 2, S104-113.
del Toro, M. D., Rodriguez-Bano, J., Herrero, M., Rivero, A., Garcia-Ordonez, M. A., Corzo,
J., & Perez-Cano, R. (2002) Medicine (Baltimore) 81, 228-239.
Hanes, S. D., Demirkan, K., Tolley, E., Boucher, B. A., Croce, M. A., Wood, G. C., &
Fabian, T. C. (2002) Clin Infect Dis 35, 228-235.
Saiman, L. & Siegel, J. (2003) Infect Control Hosp Epidemiol 24, S6-52.
Loukil, C., Saizou, C., Doit, C., Bidet, P., Mariani-Kurkdjian, P., Aujard, Y., Beaufils, F., &
Bingen, E. (2003) Infect Control Hosp Epidemiol 24, 707-710.
Ryan, M. P., Pembroke, J. T., & Adley, C. C. (2006) J Hosp Infect 62, 278-284.
Fry, A. M., Udeagu, C. C., Soriano-Gabarro, M., Fridkin, S., Musinski, D., LaClaire, L.,
Elliott, J., Cook, D. J., Kornblum, J., Layton, M., et al. (2005) Infect Control Hosp Epidemiol
26, 239-247.
Carter, R. J., Sorenson, G., Heffernan, R., Kiehlbauch, J. A., Kornblum, J. S., Leggiadro, R.
J., Nixon, L. J., Wertheim, W. A., Whitney, C. G., & Layton, M. (2005) Infect Control Hosp
Epidemiol 26, 248-255.
Whitener, C. J., Park, S. Y., Browne, F. A., Parent, L. J., Julian, K., Bozdogan, B.,
Appelbaum, P. C., Chaitram, J., Weigel, L. M., Jernigan, J., et al. (2004) Clin Infect Dis 38,
1049-1055.
CDC (1997) MMWR Morb Mortal Wkly Rep 46 (33), 765-766.
CDC (2002) MMWR Morb Mortal Wkly Rep 51 (26), 565-567.
CDC (2002) MMWR - Morbidity & Mortality Weekly Report 51(40), 902.
CDC (2004) MMWR Morb Mortal Wkly Rep 53, 322-323.
Chang, S., Sievert, D. M., Hageman, J. C., Boulton, M. L., Tenover, F. C., Downes, F. P.,
Shah, S., Rudrik, J. T., Pupp, G. R., Brown, W. J., et al. (2003) N Engl J Med 348, 13421347.
54
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
Fridkin, S. K., Hageman, J., McDougal, L. K., Mohammed, J., Jarvis, W. R., Perl, T. M., &
Tenover, F. C. (2003) Clin Infect Dis 36, 429-439.
Hageman, J. C., Fridkin, S. K., Mohammed, J. M., Steward, C. D., Gaynes, R. P., & Tenover,
F. C. (2003) Infect Control Hosp Epidemiol 24, 356-361.
Rotun, S. S., McMath, V., Schoonmaker, D. J., Maupin, P. S., Tenover, F. C., Hill, B. C., &
Ackman, D. M. (1999) Emerg Infect Dis 5, 147-149.
Smith, T. L., Pearson, M. L., Wilcox, K. R., Cruz, C., Lancaster, M. V., Robinson-Dunn, B.,
Tenover, F. C., Zervos, M. J., Band, J. D., White, E., et al. (1999) N Engl J Med 340, 493501.
Srinivasan, A., Dick, J. D., & Perl, T. M. (2002) Clin Microbiol Rev 15, 430-438.
Gonzales, R. D., Schreckenberger, P. C., Graham, M. B., Kelkar, S., DenBesten, K., & Quinn,
J. P. (2001) Lancet 357, 1179.
Soltani, M., Beighton, D., Philpott-Howard, J., & Woodford, N. (2001) Antimicrob Agents
Chemother 45, 645-646.
Pai, M. P., Rodvold, K. A., Schreckenberger, P. C., Gonzales, R. D., Petrolatti, J. M., &
Quinn, J. P. (2002) Clin Infect Dis 35, 1269-1272.
Pillai, S. K., Sakoulas, G., Wennersten, C., Eliopoulos, G. M., Moellering, R. C., Jr., Ferraro,
M. J., & Gold, H. S. (2002) J Infect Dis 186, 1603-1607.
Hershberger, E., Donabedian, S., Konstantinou, K., & Zervos, M. J. (2004) Clin Infect Dis 38,
92-98.
Mangili, A., Bica, I., Snydman, D. R., & Hamer, D. H. (2005) Clin Infect Dis 40, 1058-1060.
Sabol, K., Patterson, J. E., Lewis, J. S., 2nd, Owens, A., Cadena, J., & Jorgensen, J. H. (2005)
Antimicrob Agents Chemother 49, 1664-1665.
Simor, A. E., Lee, M., Vearncombe, M., Jones-Paul, L., Barry, C., Gomez, M., Fish, J. S.,
Cartotto, R. C., Palmer, R., & Louie, M. (2002) Infect Control Hosp Epidemiol 23, 261-267.
Clarke, N. M., Patterson, J., & Lynch, I. J. (2003) Curr Opin Crit Care 9, 413-423.
Martone, W. J. (1998) Infect Control Hosp Epidemiol 19, 539-545.
The Brooklyn Antibiotic Task Force (2002) Infect Control Hosp Epidemiol 23, 106-108.
Wilson, S. J., Knipe, C. J., Zieger, M. J., Gabehart, K. M., Goodman, J. E., Volk, H. M., &
Sood, R. (2004) Am J Infect Control 32, 342-344.
Qavi, A., Segal-Maurer, S., Mariano, N., Urban, C., Rosenberg, C., Burns, J., Chiang, T.,
Maurer, J., & Rahal, J. J. (2005) Infect Control Hosp Epidemiol 26, 63-68.
Song, X., Srinivasan, A., Plaut, D., & Perl, T. M. (2003) Infect Control Hosp Epidemiol 24,
251-256.
Aloush, V., Navon-Venezia, S., Seigman-Igra, Y., Cabili, S., & Carmeli, Y. (2006)
Antimicrob Agents Chemother 50, 43-48.
Cosgrove, S. E. (2006) Clin Infect Dis 42 Suppl 2, S82-89.
Stone, P. W., Gupta, A., Loughrey, M., Della-Latta, P., Cimiotti, J., Larson, E., Rubenstein,
D., & Saiman, L. (2003) Infect Control Hosp Epidemiol 24, 601-606.
Cosgrove, S. E., Kaye, K. S., Eliopoulous, G. M., & Carmeli, Y. (2002) Arch Intern Med 162,
185-190.
Linden, P. K., Pasculle, A. W., Manez, R., Kramer, D. J., Fung, J. J., Pinna, A. D., & Kusne,
S. (1996) Clin Infect Dis 22, 663-670.
Vergis, E. N., Hayden, M. K., Chow, J. W., Snydman, D. R., Zervos, M. J., Linden, P. K.,
Wagener, M. M., Schmitt, B., & Muder, R. R. (2001) Ann Intern Med 135, 484-492.
Salgado, C. D. & Farr, B. M. (2003) Infect Control Hosp Epidemiol 24, 690-698.
55
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.
DiazGranados, C. A. & Jernigan, J. A. (2005) J Infect Dis 191, 588-595.
DiazGranados, C. A., Zimmer, S. M., Klein, M., & Jernigan, J. A. (2005) Clin Infect Dis 41,
327-333.
Carmeli, Y., Eliopoulos, G., Mozaffari, E., & Samore, M. (2002) Arch Intern Med 162, 22232228.
Davis, K. A., Stewart, J. J., Crouch, H. K., Florez, C. E., & Hospenthal, D. R. (2004) Clin
Infect Dis 39, 776-782.
Muder, R. R., Brennen, C., Wagener, M. M., Vickers, R. M., Rihs, J. D., Hancock, G. A.,
Yee, Y. C., Miller, J. M., & Yu, V. L. (1991) Ann Intern Med 114, 107-112.
Cosgrove, S. E., Sakoulas, G., Perencevich, E. N., Schwaber, M. J., Karchmer, A. W., &
Carmeli, Y. (2003) Clin Infect Dis 36, 53-59.
Melzer, M., Eykyn, S. J., Gransden, W. R., & Chinn, S. (2003) Clin Infect Dis 37, 1453-1460.
Selvey, L. A., Whitby, M., & Johnson, B. (2000) Infect Control Hosp Epidemiol 21, 645648.(s).
Romero-Vivas, J., Rubio, M., Fernandez, C., & Picazo, J. J. (1995) Clin Infect Dis 21, 14171423.
Blot, S. I., Vandewoude, K. H., Hoste, E. A., & Colardyn, F. A. (2002) Arch Intern Med 162,
2229-2235.
Reed, S. D., Friedman, J. Y., Engemann, J. J., Griffiths, R. I., Anstrom, K. J., Kaye, K. S., &
al., e. (2005) Infect Control Hosp Epidemiol 26, 175-183.
Mekontso-Dessap, A., Kirsch, M., Brun-Buisson, C., & Loisance, D. (2001) Clin Infect Dis
32, 877-883.
Engemann, J. J., Carmeli, Y., Cosgrove, S. E., Fowler, V. G., Bronstein, M. Z., Trivette, S. L.,
Briggs, J. P., Sexton, D. J., & Kaye, K. S. (2003) Clin Infect Dis 36, 592-598.
Jones, R. N. (2006) Clin Infect Dis 42 Suppl 1, S13-24.
Fowler, V. G., Jr., Sakoulas, G., McIntyre, L. M., Meka, V. G., Arbeit, R. D., Cabell, C. H.,
Stryjewski, M. E., Eliopoulos, G. M., Reller, L. B., Corey, G. R., et al. (2004) J Infect Dis
190, 1140-1149.
Woods, C. W., Cheng, A. C., Fowler, V. G., Jr., Moorefield, M., Frederick, J., Sakoulas, G.,
Meka, V. G., Tenover, F. C., Zwadyk, P., & Wilson, K. H. (2004) Clin Infect Dis 38, 11881191.
Jernigan, J. A., Clemence, M. A., Stott, G. A., Titus, M. G., Alexander, C. H., Palumbo, C.
M., & Farr, B. M. (1995) Infect Control Hosp Epidemiol 16, 686-696.
Stamm, A. M., Long, M. N., & Belcher, B. (1993) Am J Infect Control 21, 70-74.
Harbarth, S., Albrich, W., Goldmann, D. A., & Huebner, J. (2001) Lancet Infect Dis 1, 251261.
Zinn, C. S., Westh, H., & Rosdahl, V. T. (2004) Microb Drug Resist 10, 160-168.
Whitney, C. G., Farley, M. M., Hadler, J., Harrison, L. H., Lexau, C., Reingold, A.,
Lefkowitz, L., Cieslak, P. R., Cetron, M., Zell, E. R., et al. (2000) N Engl J Med 343, 19171924.
Kollef, M. H. & Fraser, V. J. (2001) Ann Intern Med 134, 298-314.
Fridkin, S. K. (2001) Crit Care Med 29, N64-68.
Diekema, D. J., BootsMiller, B. J., Vaughn, T. E., Woolson, R. F., Yankey, J. W., Ernst, E. J.,
Flach, S. D., Ward, M. M., Franciscus, C. L., Pfaller, M. A., et al. (2004) Clin Infect Dis 38,
78-85.
56
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
91.
92.
93.
94.
95.
96.
97.
98.
99.
100.
Polgreen, P. M., Beekmann, S. E., Chen, Y. Y., Doern, G. V., Pfaller, M. A., Brueggemann,
A. B., Herwaldt, L. A., & Diekema, D. J. (2006) Infect Control Hosp Epidemiol 27, 252-256.
Bradley, S. F., Terpenning, M. S., Ramsey, M. A., Zarins, L. T., Jorgensen, K. A., Sottile, W.
S., Schaberg, D. R., & Kauffman, C. A. (1991) Ann Intern Med 115, 417-422.
Brennen, C., Wagener, M. M., & Muder, R. R. (1998) J Am Geriatr Soc 46, 157-160.
Strausbaugh, L. J., Crossley, K. B., Nurse, B. A., & Thrupp, L. D. (1996) Infect Control Hosp
Epidemiol 17, 129-140.
Bradley, S. F. (1999) Infect Control Hosp Epidemiol 20, 362-366.
Bradley, S. F. (1999) Am J Med 106, 2S-10S; discussion 48S-52S.
Wiener, J., Quinn, J. P., Bradford, P. A., Goering, R. V., Nathan, C., Bush, K., & Weinstein,
R. A. (1999) Jama 281, 517-523.
McNeil, S. A., Mody, L., & Bradley, S. F. (2002) Geriatrics 57, 16-18, 21-14, 27.
Pacio, G. A., Visintainer, P., Maguire, G., Wormser, G. P., Raffalli, J., & Montecalvo, M. A.
(2003) Infect Control Hosp Epidemiol 24, 246-250.
Rahimi, A. R. (1998) J Am Geriatr Soc 46, 1555-1557.
Trick, W. E., Weinstein, R. A., DeMarais, P. L., Tomaska, W., Nathan, C., McAllister, S. K.,
Hageman, J. C., Rice, T. W., Westbrook, G., & Jarvis, W. R. (2004) J Am Geriatr Soc 52,
2003-2009.
Ben-Ami, R., Schwaber, M. J., Navon-Venezia, S., Schwartz, D., Giladi, M., Chmelnitsky, I.,
Leavitt, A., & Carmeli, Y. (2006) Clin Infect Dis 42, 925-934.
Elizaga, M. L., Weinstein, R. A., & Hayden, M. K. (2002) Clin Infect Dis 34, 441-446.
Saiman, L., Cronquist, A., Wu, F., Zhou, J., Rubenstein, D., Eisner, W., Kreiswirth, B. N., &
Della-Latta, P. (2003) Infect Control Hosp Epidemiol 24, 317-321.
Klevens, R. M., Edwards, J. R., Tenover, F. C., McDonald, L. C., Horan, T., & Gaynes, R.
(2006) Clin Infect Dis 42, 389-391.
Gaynes, R. & Edwards, J. R. (2005) Clin Infect Dis 41, 848-854.
Boyce, J. M., Jackson, M. M., Pugliese, G., Batt, M. D., Fleming, D., Garner, J. S., Hartstein,
A. I., Kauffman, C. A., Simmons, M., Weinstein, R., et al. (1994) Infect Control Hosp
Epidemiol 15, 105-115.
NNIS (2003) Am J Infect Control 31, 481-498.
Fridkin, S. K., Edwards, J. R., Courval, J. M., Hill, H., Tenover, F. C., Lawton, R., Gaynes, R.
P., & McGowan, J. E., Jr. (2001) Ann Intern Med 135, 175-183.
Jones, R. N. (2001) Chest 119, 397S-404S.
Neuhauser, M. M., Weinstein, R. A., Rydman, R., Danziger, L. H., Karam, G., & Quinn, J. P.
(2003) JAMA 289, 885-888.
Fridkin, S. K., Hill, H. A., Volkova, N. V., Edwards, J. R., Lawton, R. M., Gaynes, R. P., &
McGowan, J. E., Jr. (2002) Emerg Infect Dis 8, 697-701.
Madaras-Kelly, K. J., Remington, R. E., Lewis, P. G., & Stevens, D. L. (2006) Infect Control
Hosp Epidemiol 27, 155-169.
Fridkin, S. K., Hageman, J. C., Morrison, M., Sanza, L. T., Como-Sabetti, K., Jernigan, J. A.,
Harriman, K., Harrison, L. H., Lynfield, R., & Farley, M. M. (2005) N Engl J Med 352, 14361444.
Kuehnert, M. J., Kruszon-Moran, D., Hill, H. A., McQuillan, G., McAllister, S. K., Fosheim,
G., McDougal, L. K., Chaitram, J., Jensen, B., Fridkin, S. K., et al. (2006) J Infect Dis 193,
172-179.
57
101.
102.
103.
104.
105.
106.
107.
108.
109.
110.
111.
112.
113.
114.
115.
116.
117.
118.
119.
120.
121.
122.
123.
124.
125.
Bonten, M. J., Slaughter, S., Ambergen, A. W., Hayden, M. K., van Voorhis, J., Nathan, C.,
& Weinstein, R. A. (1998) Arch Intern Med 158, 1127-1132.
Merrer, J., Santoli, F., Appere de Vecchi, C., Tran, B., De Jonghe, B., & Outin, H. (2000)
Infect Control Hosp Epidemiol 21, 718-723.
Lautenbach, E., Patel, J. B., Bilker, W. B., Edelstein, P. H., & Fishman, N. O. (2001) Clin
Infect Dis 32, 1162-1171.
Goetz, A. M., Rihs, J. D., Wagener, M. M., & Muder, R. R. (1998) Am J Infect Control 26,
558-562.
Puzniak, L. A., Leet, T., Mayfield, J., Kollef, M., & Mundy, L. M. (2002) Clin Infect Dis 35,
18-25.
CDC (2002) MMWR 51(16), 1-44.
Muto, C. A., Jernigan, J. A., Ostrowsky, B. E., Richet, H. M., Jarvis, W. R., Boyce, J. M., &
Farr, B. M. (2003) Infect Control Hosp Epidemiol 24, 362-386.
Almuneef, M. A., Baltimore, R. S., Farrel, P. A., Reagan-Cirincione, P., & Dembry, L. M.
(2001) Clin Infect Dis 32, 220-227.
Duckro, A. N., Blom, D. W., Lyle, E. A., Weinstein, R. A., & Hayden, M. K. (2005) Arch
Intern Med 165, 302-307.
Boyce, J. M., Potter-Bynoe, G., Chenevert, C., & King, T. (1997) Infect Control Hosp
Epidemiol 18, 622-627.(mj).
Bhalla, A., Pultz, N. J., Gries, D. M., Ray, A. J., Eckstein, E. C., Aron, D. C., & Donskey, C.
J. (2004) Infect Control Hosp Epidemiol 25, 164-167.
Larson, E. L., Cimiotti, J. P., Haas, J., Nesin, M., Allen, A., Della-Latta, P., & Saiman, L.
(2005) Pediatr Crit Care Med 6, 457-461.
Lee, Y. L., Cesario, T., Lee, R., Nothvogel, S., Nassar, J., Farsad, N., & Thrupp, L. (1994) Am
J Infect Control 22, 346-351.
Boyce, J. M., Opal, S. M., Chow, J. W., Zervos, M. J., Potter-Bynoe, G., Sherman, C. B.,
Romulo, R. L., Fortna, S., & Medeiros, A. A. (1994) J Clin Microbiol 32, 1148-1153.
Gerding, D. N., Johnson, S., Peterson, L. R., Mulligan, M. E., & Silva, J., Jr. (1995) Infect
Control Hosp Epidemiol 16, 459-477.
Donskey, C. J. (2004) Clin Infect Dis 39, 219-226.
Boyce, J. M., Havill, N. L., & Maria, B. (2005) J Clin Microbiol 43, 5992-5995.
www.ihi.org/IHI/Programs/Campaign.
Evans, R., Lloyd, J. F., Abouzelof, R. H., Taylor, C. W., Anderson, V. R., & Samore, M. H.
(2004) Medinfo 2004, 212-216.
Boyce, J. M., Opal, S. M., Potter-Bynoe, G., & Medeiros, A. A. (1993) Clin Infect Dis 17,
496-504.
Zawacki, A., O'Rourke, E., Potter-Bynoe, G., Macone, A., Harbarth, S., & Goldmann, D.
(2004) Infect Control Hosp Epidemiol 25, 1083-1089.
Faibis, F., Laporte, C., Fiacre, A., Delisse, C., Lina, G., Demachy, M.-C., & Botterel, F.
(2005) Infect Control Hosp Epidemiol 26, 213-215.
Sheretz, R. J., Reagan, D. R., Hampton, K. D., Robertson, K. L., Streed, S. A., Hoen, H. M.,
Thomas, R., & Gwaltney, J. M., Jr. (1996) Ann Intern Med 124, 539-547.
Wang, J. T., Chang, S. C., Ko, W. J., Chang, Y. Y., Chen, M. L., Pan, H. J., & Luh, K. T.
(2001) J Hosp Infect 47, 104-109.
Herold, B. C., Immergluck, L. C., Maranan, M. C., Lauderdale, D. S., Gaskin, R. E., BoyleVavra, S., Leitch, C. D., & Daum, R. S. (1998) JAMA 279, 593-598.
58
126.
127.
128.
129.
130.
131.
132.
133.
134.
135.
136.
137.
138.
139.
140.
141.
142.
143.
144.
145.
146.
147.
148.
CDC (1999) MMWR - Morbidity & Mortality Weekly Report 48, 707-710.
Fergie, J. E. & Purcell, K. (2001) Pediatr Infect Dis J 20, 860-863.
Sattler, C. A., Mason, E. O., Jr., & Kaplan, S. L. (2002) Pediatr Infect Dis J 21, 910-917.
Enright, M. C., Robinson, D. A., Randle, G., Feil, E. J., Grundmann, H., & Spratt, B. G.
(2002) Proc Natl Acad Sci U S A 99, 7687-7692.
Pan, E. S., Diep, B. A., Carleton, H. A., Charlebois, E. D., Sensabaugh, G. F., Haller, B. L., &
Perdreau-Remington, F. (2003) Clin Infect Dis 37, 1384-1388.
Daum, R. S., Ito, T., Hiramatsu, K., Hussain, F., Mongkolrattanothai, K., Jamklang, M., &
Boyle-Vavra, S. (2002) J Infect Dis 186, 1344-1347.
Said-Salim, B., Mathema, B., & Kreiswirth, B. N. (2003) Infect Control Hosp Epidemiol 24,
451-455.
McDougal, L. K., Steward, C. D., Killgore, G. E., Chaitram, J. M., McAllister, S. K., &
Tenover, F. C. (2003) J Clin Microbiol 41, 5113-5120.
Zetola, N., Francis, J. S., Nuermberger, E. L., & Bishai, W. R. (2005) Lancet Infect Dis 5,
275-286.
Adem, P. V., Montgomery, C. P., Husain, A. N., Koogler, T. K., Arangelovich, V., Humilier,
M., Boyle-Vavra, S., & Daum, R. S. (2005) N Engl J Med 353, 1245-1251.
Bocchini, C. E., Hulten, K. G., Mason, E. O., Jr., Gonzalez, B. E., Hammerman, W. A., &
Kaplan, S. L. (2006) Pediatrics 117, 433-440.
Healy, C. M., Hulten, K. G., Palazzi, D. L., Campbell, J. R., & Baker, C. J. (2004) Clin Infect
Dis 39, 1460-1466.
Saiman, L., O'keefe, M., Graham, P. L., Wu, F., Said-Salim, B., Kreiswirth, B., LaSala, A.,
Schlievert, P. M., & Della Latta, P. (2003) Clin Infect Dis 37, 1313-1319.
Eckhardt, C., Halvosa, J. S., Ray, S. M., & Blumberg, H. M. (2003) Infect Control Hosp
Epidemiol 24, 460-461.
Seybold, U., Kourbatova, E. V., Johnson, J. G., Halvosa, S. J., Wang, Y. F., King, M. D.,
Ray, S. M., & Blumberg, H. M. (2006) Clin Infect Dis 42, 647-656.
Berenholtz, S. M., Pronovost, P. J., Lipsett, P. A., Hobson, D., Earsing, K., Farley, J. E.,
Milanovich, S., Garrett-Mayer, E., Winters, B. D., Rubin, H. R., et al. (2004) Crit Care Med
32, 2014-2020.
Coopersmith, C. M., Rebmann, T. L., Zack, J. E., Ward, M. R., Corcoran, R. M., Schallom,
M. E., Sona, C. S., Buchman, T. G., Boyle, W. A., Polish, L. B., et al. (2002) Crit Care Med
30, 59-64.
Babcock, H. M., Zack, J. E., Garrison, T., Trovillion, E., Jones, M., Fraser, V. J., & Kollef,
M. H. (2004) Chest 125, 2224-2231.
Warren, D. K., Zack, J. E., Cox, M. J., Cohen, M. M., & Fraser, V. J. (2003) Crit Care Med
31, 1959-1963.
Eggimann, P., Hugonnet, S., Sax, H., Harbarth, S., Chevrolet, J. C., & Pittet, D. (2005) Ann
Intern Med 142, 875-876.
Verhoef, J., Beaujean, D., Blok, H., Baars, A., Meyler, A., van der Werken, C., & Weersink,
A. (1999) Eur J Clin Microbiol Infect Dis 18, 461-466.
Salmenlinna, S., Lyytikainen, O., Kotilainen, P., Scotford, R., Siren, E., & Vuopio-Varkila, J.
(2000) Eur J Clin Microbiol Infect Dis 19, 101-107.
Struelens, M. J., Ronveaux, O., Jans, B., & Mertens, R. (1996) Infect Control Hosp Epidemiol
17, 503-508.
59
149.
150.
151.
152.
153.
154.
155.
156.
157.
158.
159.
160.
161.
162.
163.
164.
165.
166.
167.
168.
169.
170.
171.
172.
Voss, A., Milatovic, D., Wallrauch-Schwarz, C., Rosdahl, V. T., & Braveny, I. (1994) Eur J
Clin Microbiol Infect Dis 13, 50-55.
Rosdahl, V. T. & Knudsen, A. M. (1991) Infect Control Hosp Epidemiol 12, 83-88.
Ostrowsky, B. E., Trick, W. E., Sohn, A. H., Quirk, S. B., Holt, S., Carson, L. A., Hill, B. C.,
Arduino, M. J., Kuehnert, M. J., & Jarvis, W. R. (2001) N Engl J Med 344, 1427-1433.
Haley, R. W., Cushion, N. B., Tenover, F. C., Bannerman, T. L., Dryer, D., Ross, J., Sanchez,
P. J., & Siegel, J. D. (1995) J Infect Dis 171, 614-624.
Jernigan, J. A., Titus, M. G., Groschel, D. H., Getchell-White, S., & Farr, B. M. (1996) Am J
Epidemiol 143, 496-504.
Falk, P. S., Winnike, J., Woodmansee, C., Desai, M., & Mayhall, C. G. (2000) Infect Control
Hosp Epidemiol 21, 575-582.
Sherer, C. R., Sprague, B. M., Campos, J. M., Nambiar, S., Temple, R., Short, B., & Singh, N.
(2005) Emerg Infect Dis 11, 1470-1472.
Nourse, C., Byrne, C., Murphy, H., Kaufmann, M. E., Clarke, A., & Butler, K. (2000)
Epidemiol Infect 124, 53-59.
Rubin, L. G., Tucci, V., Cercenado, E., Eliopoulos, G., & Isenberg, H. D. (1992) Infect
Control Hosp Epidemiol 13, 700-705.
Karanfil, L. V., Murphy, M., Josephson, A., Gaynes, R., Mandel, L., Hill, B. C., & Swenson,
J. M. (1992) Infect Control Hosp Epidemiol 13, 195-200.
Hanna, H., Umphrey, J., Tarrand, J., Mendoza, M., & Raad, I. (2001) Infect Control Hosp
Epidemiol 22, 217-219.
Dembry, L. M., Uzokwe, K., & Zervos, M. J. (1996) Infect Control Hosp Epidemiol 17, 286292.
Bartley, P. B., Schooneveldt, J. M., Looke, D. F., Morton, A., Johnson, D. W., & Nimmo, G.
R. (2001) J Hosp Infect 48, 43-54.
Christiansen, K. J., Tibbett, P. A., Beresford, W., Pearman, J. W., Lee, R. C., Coombs, G. W.,
Kay, I. D., O'Brien, F. G., Palladino, S., Douglas, C. R., et al. (2004) Infect Control Hosp
Epidemiol 25, 384-390.
Armstrong-Evans, M., Litt, M., McArthur, M. A., Willey, B., Cann, D., Liska, S.,
Nusinowitz, S., Gould, R., Blacklock, A., Low, D. E., et al. (1999) Infect Control Hosp
Epidemiol 20, 312-317.
Webster, J., Faoagali, J. L., & Cartwright, D. (1994) J Paediatr Child Health 30, 59-64.
Zafar, A. B., Butler, R. C., Reese, D. J., Gaydos, L. A., & Mennonna, P. A. (1995) Am J
Infect Control 23, 200-208.
Carrier, M., Marchand, R., Auger, P., Hebert, Y., Pellerin, M., Perrault, L. P., Cartier, R.,
Bouchard, D., Poirier, N., & Page, P. (2002) J Thorac Cardiovasc Surg 123, 40-44.
Kotilainen, P., Routamaa, M., Peltonen, R., Evesti, P., Eerola, E., Salmenlinna, S., VuopioVarkila, J., & Rossi, T. (2001) Arch Intern Med 161, 859-863.
Back, N. A., Linnemann, C. C., Jr., Staneck, J. L., & Kotagal, U. R. (1996) Infect Control
Hosp Epidemiol 17, 227-231.
Embil, J. M., McLeod, J. A., Al-Barrak, A. M., Thompson, G. M., Aoki, F. Y., Witwicki, E.
J., Stranc, M. F., Kabani, A. M., Nicoll, D. R., & Nicolle, L. E. (2001) Burns 27, 681-688.
Rao, N., Jacobs, S., & Joyce, L. (1988) Infect Control Hosp Epidemiol 9, 255-260.
Kotilainen, P., Routamaa, M., Peltonen, R., Oksi, J., Rintala, E., Meurman, O., Lehtonen, O.
P., Eerola, E., Salmenlinna, S., Vuopio-Varkila, J., et al. (2003) Emerg Infect Dis 9, 169-175.
Cohen, S. H., Morita, M. M., & Bradford, M. (1991) Am J Med 91, 233S-237S.
60
173.
174.
175.
176.
177.
178.
179.
180.
181.
182.
183.
184.
185.
186.
187.
188.
189.
190.
191.
192.
193.
194.
195.
196.
Adeyemi-Doro, F. A., Scheel, O., Lyon, D. J., & Cheng, A. F. (1997) Infect Control Hosp
Epidemiol 18, 765-767.
van der Zwet, W. C., Parlevliet, G. A., Savelkoul, P. H., Stoof, J., Kaiser, A. M., Koeleman, J.
G., & Vandenbroucke-Grauls, C. M. (1999) J Hosp Infect 42, 295-302.
Macrae, M. B., Shannon, K. P., Rayner, D. M., Kaiser, A. M., Hoffman, P. N., & French, G.
L. (2001) J Hosp Infect 49, 183-192.
Villari, P., Crispino, M., Salvadori, A., & Scarcella, A. (2001) Infect Control Hosp Epidemiol
22, 630-634.
Paterson, D. L., Singh, N., Rihs, J. D., Squier, C., Rihs, B. L., & Muder, R. R. (2001) Clin
Infect Dis 33, 126-128.
Bukholm, G., Tannaes, T., Kjelsberg, A. B., & Smith-Erichsen, N. (2002) Infect Control
Hosp Epidemiol 23, 441-446.
Roberts, S. A., Findlay, R., & Lang, S. D. (2001) J Hosp Infect 48, 228-232.
Hollander, R., Ebke, M., Barck, H., & von Pritzbuer, E. (2001) J Hosp Infect 48, 207-213.
Podnos, Y. D., Cinat, M. E., Wilson, S. E., Cooke, J., Gornick, W., & Thrupp, L. D. (2001)
Surgical Infections 2, 297-301.
Pittet, D., Hugonnet, S., Harbarth, S., Mourouga, P., Sauvan, V., Touveneau, S., & Perneger,
T. V. (2000) Lancet 356, 1307-1312.
Murray-Leisure, K. A., Geib, S., Graceley, D., Rubin-Slutsky, A. B., Saxena, N., Muller, H.
A., & Hamory, B. H. (1990) Infect Control Hosp Epidemiol 11, 343-350.
Jochimsen, E. M., Fish, L., Manning, K., Young, S., Singer, D. A., Baker, R., & Jarvis, W. R.
(1999) Infect Control Hosp Epidemiol 20, 106-109.
Calfee, D. P. & Farr, B. M. (2002) Infect Control Hosp Epidemiol 23, 407-410.
Scheckler, W. E., Brimhall, D., Buck, A. S., Farr, B. M., Friedman, C., Garibaldi, R. A.,
Gross, P. A., Harris, J. A., Hierholzer, W. J., Jr., Martone, W. J., et al. (1998) Infect Control
Hosp Epidemiol 19, 114-124.
Boyce, J. M., Mermel, L. A., Zervos, M. J., Rice, L. B., Potter-Bynoe, G., Giorgio, C., &
Medeiros, A. A. (1995) Infect Control Hosp Epidemiol 16, 634-637.
Nicolle, L. E., Dyck, B., Thompson, G., Roman, S., Kabani, A., Plourde, P., Fast, M., &
Embil, J. (1999) Infect Control Hosp Epidemiol 20, 202-205.
Lucet, J. C., Decre, D., Fichelle, A., Joly-Guillou, M. L., Pernet, M., Deblangy, C., Kosmann,
M. J., & Regnier, B. (1999) Clin Infect Dis 29, 1411-1418.
D'Agata, E. M., Thayer, V., & Schaffner, W. (2000) Infect Control Hosp Epidemiol 21, 588591.
Papia, G., Louie, M., Tralla, A., Johnson, C., Collins, V., & Simor, A. E. (1999) Infect
Control Hosp Epidemiol 20, 473-477.
Siddiqui, A. H., Harris, A. D., Hebden, J., Wilson, P. D., Morris, J. G., Jr., & Roghmann, M.
C. (2002) Am J Infect Control 30, 40-43.
Byers, K. E., Anglim, A. M., Anneski, C. J., Germanson, T. P., Gold, H. S., Durbin, L. J.,
Simonton, B. M., & Farr, B. M. (2001) Infect Control Hosp Epidemiol 22, 140-147.
Harbarth, S., Martin, Y., Rohner, P., Henry, N., Auckenthaler, R., & Pittet, D. (2000) J Hosp
Infect 46, 43-49.
Curtis, J. R., Cook, D. J., Wall, R. J., Angus, D. C., Bion, J., Kacmarek, R., Kane-Gill, S. L.,
Kirchhoff, K. T., Levy, M., Mitchell, P. H., et al. (2006) Crit Care Med 34, 211-218.
Arnow, P., Allyn, P. A., Nichols, E. M., Hill, D. L., Pezzlo, M., & Bartlett, R. H. (1982) J
Trauma 22, 954-959.
61
197.
198.
199.
200.
201.
202.
203.
204.
205.
206.
207.
208.
209.
210.
211.
212.
213.
214.
215.
216.
217.
218.
219.
220.
221.
222.
Fridkin, S. K., Pear, S. M., Williamson, T. H., Galgiani, J. N., & Jarvis, W. R. (1996) Infect
Control Hosp Epidemiol 17, 150-158.
Harbarth, S., Sudre, P., Dharan, S., Cadenas, M., & Pittet, D. (1999) Infect Control Hosp
Epidemiol 20, 598-603.
Vicca, A. F. (1999) J Hosp Infect 43, 109-113.
Robert, J., Fridkin, S. K., Blumberg, H. M., Anderson, B., White, N., Ray, S. M., Chan, J., &
Jarvis, W. R. (2000) Infect Control Hosp Epidemiol 21, 12-17.(mj).
Jackson, M., Chiarello, L. A., Gaynes, R. P., & Gerberding, J. L. (2002) Am J Infect Control
30, 199-206.
Grundmann, H., Hori, S., Winter, B., Tami, A., & Austin, D. J. (2002) J Infect Dis 185, 481488.
Dubbert, P. M., Dolce, J., Richter, W., Miller, M., & Chapman, S. W. (1990) Infect Control
Hosp Epidemiol 11, 191-193.
Nettleman, M. D., Trilla, A., Fredrickson, M., & Pfaller, M. (1991) Am J Med 91, 228S-232S.
Curran, E. T., Benneyan, J. C., & Hood, J. (2002) Infect Control Hosp Epidemiol 23, 13-18.
Gerber, S. I., Jones, R. C., Scott, M. V., Price, J. S., Dworkin, M. S., Filippell, M. B., Rearick,
T., Pur, S. L., McAuley, J. B., Lavin, M. A., et al. (2006) Infect Control Hosp Epidemiol 27,
139-145.
Chicago Antimicrobial Resistance Project.
Rampling, A., Wiseman, S., Davis, L., Hyett, A. P., Walbridge, A. N., Payne, G. C., &
Cornaby, A. J. (2001) J Hosp Infect 49, 109-116.
Rice, L. B., Eckstein, E. C., DeVente, J., & Shlaes, D. M. (1996) Clin Infect Dis 23, 118-124.
Wright, M. O., Hebden, J. N., Harris, A. D., Shanholtz, C. B., Standiford, H. C., Furuno, J. P.,
& Perencevich, E. N. (2004) Infect Control Hosp Epidemiol 25, 167-168.
Smith, D. L., Dushoff, J., Perencevich, E. N., Harris, A. D., & Levin, S. A. (2004) Proc Natl
Acad Sci U S A 101, 3709-3714.
Rahal, J. J., Urban, C., Horn, D., Freeman, K., Segal-Maurer, S., Maurer, J., Mariano, N.,
Marks, S., Burns, J. M., Dominick, D., et al. (1998) JAMA 280, 1233-1237.
Rahal, J. J., Urban, C., & Segal-Maurer, S. (2002) Clin Infect Dis 34, 499-503.
Meyer, K. S., Urban, C., Eagan, J. A., Berger, B. J., & Rahal, J. J. (1993) Ann Intern Med
119, 353-358.
Pena, C., Pujol, M., Ardanuy, C., Ricart, A., Pallares, R., Linares, J., Ariza, J., & Gudiol, F.
(1998) Antimicrob Agents Chemother 42, 53-58.
Quale, J. M., Landman, D., Bradford, P. A., Visalli, M., Ravishankar, J., Flores, C., Mayorga,
D., Vangala, K., & Adedeji, A. (2002) Clin Infect Dis 35, 834-841.
Rupp, M. E., Marion, N., Fey, P. D., Bolam, D. L., Iwen, P. C., Overfelt, C. M., & Chapman,
L. (2001) Infect Control Hosp Epidemiol 22, 301-303.
Calil, R., Marba, S. T., von Nowakonski, A., & Tresoldi, A. T. (2001) Am J Infect Control 29,
133-138.
McDonald, L. C. (2005) Infect Control Hosp Epidemiol 26, 672-675.
Harbarth, S., Cosgrove, S., & Carmeli, Y. (2002) Antimicrob Agents Chemother 46, 16191628.
Winston, L. G., Charlebois, E. D., Pang, S., Bangsberg, D. R., Perdreau-Remington, F., &
Chambers, H. F. (2004) Am J Infect Control 32, 462-469.
Brinsley, K., Srinivasan, A., Sinkowitz-Cochran, R., Lawton, R., McIntyre, R., Kravitz, G.,
Burke, B., Shadowen, R., & Cardo, D. (2005) Am J Infect Control 33, 53-54.
62
223.
224.
225.
226.
227.
228.
229.
230.
231.
232.
233.
234.
235.
236.
237.
238.
239.
240.
241.
242.
243.
244.
245.
246.
247.
248.
249.
250.
Bruno-Murtha, L. A., Brusch, J., Bor, D., Li, W., & Zucker, D. (2005) Infect Control Hosp
Epidemiol 26, 81-87.
Fridkin, S. K. (2003) Clin Infect Dis 36, 1438-1444.
John, J. F., Jr. (2000) Infect Control Hosp Epidemiol 21, 9-11.
McGowan, J. E., Jr. (2000) Infect Control Hosp Epidemiol 21, S36-43.
Evans, R. S., Pestotnik, S. L., Classen, D. C., Clemmer, T. P., Weaver, L. K., Orme, J. F., Jr.,
Lloyd, J. F., & Burke, J. P. (1998) N Engl J Med 338, 232-238.
Huskins, W. C. (2001) Semin Pediatr Infect Dis 12, 138-146.
Mullett, C. J., Evans, R. S., Christenson, J. C., & Dean, J. M. (2001) Pediatrics 108, E75.
Glowacki, R. C., Schwartz, D. N., Itokazu, G. S., Wisniewski, M. F., Kieszkowski, P., &
Weinstein, R. A. (2003) Clin Infect Dis 37, 59-64.
Parrino, T. A. (2005) Pharmacotherapy 25, 289-298.
Paterson, D. L. (2006) Clin Infect Dis 42 Suppl 2, S90-95.
Binkley, S., Fishman, N. O., LaRosa, L. A., Marr, A. M., Nachamkin, I., Wordell, D., Bilker,
W. B., & Lautenbach, E. (2006) Infect Control Hosp Epidemiol 27, 682-687.
McGowan, J. E., Jr. & Tenover, F. C. (2004) Nat Rev Microbiol 2, 251-258.
Fridkin, S. K., Edwards, J. R., Tenover, F. C., Gaynes, R. P., & McGowan, J. E., Jr. (2001)
Clin Infect Dis 33, 324-330.
Foca, M., Jakob, K., Whittier, S., Della Latta, P., Factor, S., Rubenstein, D., & Saiman, L.
(2000) N Engl J Med 343, 695-700.
Huang (In press) J Infect Dis.
Gaynes, R. P. & Emori, T. G. (2001) in Saunders Infection Control Reference Service, eds.
Abrutyn, E., Goldmann, D. A., & Scheckler, W. E. (W.B. Saunders Company, Philadelphia,
PA), pp. 40-44.
Pottinger, J. M., Herwaldt, L. A., & Perl, T. M. (1997) Infect Control Hosp Epidemiol 18,
513-527.
Hartstein, A. I., LeMonte, A. M., & Iwamoto, P. K. (1997) Infect Control Hosp Epidemiol 18,
42-48.
Piagnerelli, M., Kennes, B., Brogniez, Y., Deplano, A., & Govaerts, D. (2000) Infect Control
Hosp Epidemiol 21, 651-653.
Montecalvo, M. A., Jarvis, W. R., Uman, J., Shay, D. K., Petrullo, C., Rodney, K., Gedris, C.,
Horowitz, H. W., & Wormser, G. P. (1999) Ann Intern Med 131, 269-272.
Talon, D. R. & Bertrand, X. (2001) Infect Control Hosp Epidemiol 22, 505-509.
Lucet, J. C., Grenet, K., Armand-Lefevre, L., Harnal, M., Bouvet, E., Regnier, B., & al., e.
(2005) Infect Control Hosp Epidemiol 26.
Troche, G., Joly, L. M., Guibert, M., & Zazzo, J. F. (2005) Infect Control Hosp Epidemiol 26,
161-165.
Nijssen, S., Bonten, M. J., & Weinstein, R. A. (2005) Clin Infect Dis 40, 405-409.
Cooper, B. S., Stone, S. P., Kibbler, C. C., Cookson, B. D., Roberts, J. A., Medley, G. F.,
Duckworth, G., Lai, R., & Ebrahim, S. (2004) Bmj 329, 533.
Perencevich, E. N., Fisman, D. N., Lipsitch, M., Harris, A. D., Morris, J. G., Jr., & Smith, D.
L. (2004) Clin Infect Dis 38, 1108-1115.
Bootsma, M. C., Diekmann, O., & Bonten, M. J. (2006) Proc Natl Acad Sci U S A 103, 56205625.
Gardam, M. A., Burrows, L. L., Kus, J. V., Brunton, J., Low, D. E., Conly, J. M., & Humar,
A. (2002) J Infect Dis 186, 1754-1760.
63
251.
252.
253.
254.
255.
256.
257.
258.
259.
260.
261.
262.
263.
264.
265.
266.
267.
268.
269.
270.
271.
272.
273.
274.
275.
Thouverez, M., Talon, D., & Bertrand, X. (2004) Infect Control Hosp Epidemiol 25, 838-841.
Armeanu, E. & Bonten, M. J. (2005) Clin Infect Dis 41, 210-216.
Muto, C. A., Giannetta, E. T., Durbin, L. J., Simonton, B. M., & Farr, B. M. (2002) Infect
Control Hosp Epidemiol 23, 429-435.
Morris, J. G., Jr., Shay, D. K., Hebden, J. N., McCarter, R. J., Jr., Perdue, B. E., Jarvis, W.,
Johnson, J. A., Dowling, T. C., Polish, L. B., & Schwalbe, R. S. (1995) Ann Intern Med 123,
250-259.
Furuno, J. P., McGregor, J. C., Harris, A. D., Johnson, J. A., Johnson, J. K., Langenberg, P.,
Venezia, R. A., Finkelstein, J., Smith, D. L., Strauss, S. M., et al. (2006) Arch Intern Med
166, 580-585.
Harbarth, S., Sax, H., Fankhauser-Rodriguez, C., Schrenzel, J., Agostinho, A., & Pittet, D.
(2006) Am J Med 119, 275 e215-223.
Lee, T. A., Hacek, D. M., Stroupe, K. T., Collins, S. M., & Peterson, L. R. (2005) Infect
Control Hosp Epidemiol 26, 39-46.
Manian, F. A., Senkel, D., Zack, J., & Meyer, L. (2002) Infect Control Hosp Epidemiol 23,
516-519.
Troillet, N., Carmeli, Y., Samore, M. H., Dakos, J., Eichelberger, K., DeGirolami, P. C., &
Karchmer, A. W. (1998) Infect Control Hosp Epidemiol 19, 181-185.
Sanford, M. D., Widmer, A. F., Bale, M. J., Jones, R. N., & Wenzel, R. P. (1994) Clin Infect
Dis 19, 1123-1128.
Lucet, J. C., Chevret, S., Durand-Zaleski, I., Chastang, C., & Regnier, B. (2003) Arch Intern
Med 163, 181-188.
D'Agata, E. M., et al. (2002) Clin Infect Dis 34, 167-172.
Flayhart, D., Hindler, J. F., Bruckner, D. A., Hall, G., Shrestha, R. K., Vogel, S. A., Richter,
S. S., Howard, W., Walther, R., & Carroll, K. C. (2005) J Clin Microbiol 43, 5536-5540.
Perry, J. D., Davies, A., Butterworth, L. A., Hopley, A. L., Nicholson, A., & Gould, F. K.
(2004) J Clin Microbiol 42, 4519-4523.
Harbarth, S., Masuet-Aumatell, C., Schrenzel, J., Francois, P., Akakpo, C., Renzi, G., Pugin,
J., Ricou, B., & Pittet, D. (2006) Crit Care 10, R25.
Huletsky, A., Lebel, P., Picard, F. J., Bernier, M., Gagnon, M., Boucher, N., & Bergeron, M.
G. (2005) Clin Infect Dis 40, 976-981.
Warren, D. K., Liao, R. S., Merz, L. R., Eveland, M., & Dunne, W. M., Jr. (2004) J Clin
Microbiol 42, 5578-5581.
Palladino, S., Kay, I. D., Flexman, J. P., Boehm, I., Costa, A. M., Lambert, E. J., &
Christiansen, K. J. (2003) J Clin Microbiol 41, 2483-2486.
Fazal, B. A., Telzak, E. E., Blum, S., Turett, G. S., Petersen-Fitzpatrick, F. E., & Lorian, V.
(1996) Infect Control Hosp Epidemiol 17, 372-374.
Toltzis, P., Hoyen, C., & et al. (1999) Pediatrics 103 (4 Pt1), 719-723.
Weinstein, R. A. & Kabins, S. A. (1981) Am J Med 70, 449-454.
Kim, P. W., Roghmann, M. C., Perencevich, E. N., & Harris, A. D. (2003) Am J Infect
Control 31, 97-103.
Slaughter, S., Hayden, M. K., Nathan, C., Hu, T. C., Rice, T., Van Voorhis, J., Matushek, M.,
Franklin, C., & Weinstein, R. A. (1996) Ann Intern Med 125, 448-456.
CDC (1995) MMWR Recomm Rep 44 (RR-12), 1-13.
Evans, M. R., Meldrum, R., Lane, W., Gardner, D., Ribeiro, C. D., Gallimore, C. I., &
Westmoreland, D. (2002) Epidemiol Infect 129, 355-360.
64
276.
277.
278.
279.
280.
281.
282.
283.
284.
285.
286.
287.
288.
289.
290.
291.
292.
293.
294.
295.
296.
297.
298.
299.
300.
301.
Hall, C. B., Douglas, R. G., Jr., Schnabel, K. C., & Geiman, J. M. (1981) Infect Immun 33,
779-783.
Wu, H. M., Fornek, M., Kellogg, J. S., Chapin, A. R., Gibson, K., Schwab, E., Spencer, C., &
Henning, K. (2005) Infect Control Hosp Epidemiol 26, 802-810.
Austin, D. J., Bonten, M. J., Weinstein, R. A., Slaughter, S., & Anderson, R. M. (1999) Proc
Natl Acad Sci U S A 96, 6908-6913.
Law, M. R., Gill, O. N., & Turner, A. (1988) Epidemiol Infect 101, 301-309.
Ruchel, R., Mergeryan, H., Boger, O., Langefeld, C., & Witte, W. (1999) Infect Control Hosp
Epidemiol 20, 353-355.
Cepeda, J. A., Whitehouse, T., Cooper, B., Hails, J., Jones, K., Kwaku, F., Taylor, L.,
Hayman, S., Cookson, B., Shaw, S., et al. (2005) Lancet 365, 295-304.
Mulin, B., Rouget, C., Clement, C., Bailly, P., Julliot, M. C., Viel, J. F., Thouverez, M.,
Vieille, I., Barale, F., & Talon, D. (1997) Infect Control Hosp Epidemiol 18, 499-503.
Nouwen, J. L., Ott, A., Kluytmans-Vandenbergh, M. F., Boelens, H. A., Hofman, A., van
Belkum, A., & Verbrugh, H. A. (2004) Clin Infect Dis 39, 806-811.
Byers, K. E., Anglim, A. M., Anneski, C. J., & Farr, B. M. (2002) Infect Control Hosp
Epidemiol 23, 207-211.
Baden, L. R., Thiemke, W., Skolnik, A., Chambers, R., Strymish, J., Gold, H. S., Moellering,
R. C., Jr., & Eliopoulos, G. M. (2001) Clin Infect Dis 33, 1654-1660.
Donskey, C. J., Hoyen, C. K., Das, S. M., Helfand, M. S., & Hecker, M. T. (2002) Infect
Control Hosp Epidemiol 23, 436-440.
Ridenour, G. A., Wong, E. S., Call, M. A., & Climo, M. W. (2006) Infect Control Hosp
Epidemiol 27, 271-278.
Scanvic, A., Denic, L., Gaillon, S., Giry, P., Andremont, A., & Lucet, J. C. (2001) Clin Infect
Dis 32, 1393-1398.
Kauffman, C. A., Terpenning, M. S., He, X., Zarins, L. T., Ramsey, M. A., Jorgensen, K. A.,
Sottile, W. S., & Bradley, S. F. (1993) Am J Med 94, 371-378.
Strausbaugh, L. J., Jacobson, C., Sewell, D. L., Potter, S., & Ward, T. T. (1992) Infect
Control Hosp Epidemiol 13, 151-159.
Kirkland, K. B. & Weinstein, J. M. (1999) Lancet 354, 1177-1178.
Saint, S., Higgins, L. A., Nallamothu, B. K., & Chenoweth, C. (2003) Am J Infect Control 31,
354-356.
Evans, H. L., Shaffer, M. M., Hughes, M. G., Smith, R. L., Chong, T. W., Raymond, D. P.,
Pelletier, S. J., Pruett, T. L., & Sawyer, R. G. (2003) Surgery 134, 180-188.
Catalano, G., Houston, S. H., Catalano, M. C., Butera, A. S., Jennings, S. M., Hakala, S. M.,
Burrows, S. L., Hickey, M. G., Duss, C. V., Skelton, D. N., et al. (2003) South Med J 96, 141145.
Tarzi, S., Kennedy, P., Stone, S., & Evans, M. (2001) J Hosp Infect 49, 250-254.
Stelfox, H. T., Bates, D. W., & Redelmeier, D. A. (2003) JAMA 290, 1899-1905.
Hota, B. (2004) Clin Infect Dis 39, 1182-1189.
Martinez, J. A., Ruthazer, R., Hansjosten, K., Barefoot, L., & Snydman, D. R. (2003) Arch
Intern Med 163, 1905-1912.
CDC (2003) MMWR 52(RR10);1-42.
Simor, A. E. (2001) Infect Control Hosp Epidemiol 22, 459-463.
Hayden, M. K., Bonten, M. J., Blom, D. W., Lyle, E. A., van de Vijver, D. A., & Weinstein,
R. A. (2006) Clin Infect Dis 42, 1552-1560.
65
302.
303.
304.
305.
306.
307.
308.
309.
310.
311.
312.
313.
314.
315.
316.
317.
318.
319.
320.
321.
322.
323.
324.
325.
326.
327.
328.
Lai, K. K., Kelley, A. L., Melvin, Z. S., Belliveau, P. P., & Fontecchio, S. A. (1998) Infect
Control Hosp Epidemiol 19, 647-652.
Boyce, J. M. (2001) J Hosp Infect 48 Suppl A, S9-14.
Montesinos, I., Salido, E., Delgado, T., Lecuona, M., & Sierra, A. (2003) Infect Control Hosp
Epidemiol 24, 667-672.
Chen, S. F. (2005) Pediatr Infect Dis J 24, 79-80.
Kaplan, S. L. (2005) Pediatr Infect Dis J 24, 457-458.
Loeb, M., Main, C., Walker-Dilks, C., & Eady, A. (2003) Cochrane Database Syst Rev,
CD003340.
Deshpande, L. M., Fix, A. M., Pfaller, M. A., & Jones, R. N. (2002) Diagn Microbiol Infect
Dis 42, 283-290.
Mody, L., Kauffman, C. A., McNeil, S. A., Galecki, A. T., & Bradley, S. F. (2003) Clin Infect
Dis 37, 1467-1474.
Walker, E. S., Vasquez, J. E., Dula, R., Bullock, H., & Sarubbi, F. A. (2003) Infect Control
Hosp Epidemiol 24, 342-346.
Harris, A. D., Bradham, D. D., Baumgarten, M., Zuckerman, I. H., Fink, J. C., & Perencevich,
E. N. (2004) Clin Infect Dis 38, 1586-1591.
Eveillard, M., Eb, F., Tramier, B., Schmit, J. L., Lescure, F. X., Biendo, M., Canarelli, B.,
Daoudi, F., Laurans, G., Rousseau, F., et al. (2001) J Hosp Infect 47, 116-124.
Campbell, J. R., Zaccaria, E., Mason, E. O., Jr., & Baker, C. J. (1998) Infect Control Hosp
Epidemiol 19, 924-928.
Harris, A. D., Nemoy, L., Johnson, J. A., Martin-Carnahan, A., Smith, D. L., Standiford, H.,
& Perencevich, E. N. (2004) Infect Control Hosp Epidemiol 25, 105-108.
Warren, D. K., Nitin, A., Hill, C., Fraser, V. J., & Kollef, M. H. (2004) Infect Control Hosp
Epidemiol 25, 99-104.
Trick, W. E., Weinstein, R. A., DeMarais, P. L., Kuehnert, M. J., Tomaska, W., Nathan, C.,
Rice, T. W., McAllister, S. K., Carson, L. A., & Jarvis, W. R. (2001) J Am Geriatr Soc 49,
270-276.
Safdar, N. & Maki, D. G. (2002) Ann Intern Med 136, 834-844.
Montecalvo, M. A., Jarvis, W. R., Uman, J., Shay, D. K., Petrullo, C., Horowitz, H. W., &
Wormser, G. P. (2001) Infect Control Hosp Epidemiol 22, 437-442.
Rubinovitch, B. & Pittet, D. (2001) J Hosp Infect 47, 9-18.
Puzniak, L. A., Gillespie, K. N., Leet, T., Kollef, M., & Mundy, L. M. (2004) Infect Control
Hosp Epidemiol 25, 418-424.
Cookson, B. (1997) Bmj 314, 664-665.
Farr, B. M. & Jarvis, W. R. (2002) Infect Control Hosp Epidemiol 23, 65-68.
Strausbaugh, L. J., Siegel, J. D., & Weinstein, R. A. (2006) Clin Infect Dis 42, 828-835.
Brooks, S., Khan, A., Stoica, D., Griffith, J., Friedeman, L., Mukherji, R., Hameed, R., &
Schupf, N. (1998) Infect Control Hosp Epidemiol 19, 333-336.
Benneyan, J. C., Lloyd, R. C., & Plsek, P. E. (2003) Qual Saf Health Care 12, 458-464.
Gustafson, T. L. (2000) Am J Infect Control 28, 406-414.
Aubry-Damon, H., Legrand, P., Brun-Buisson, C., Astier, A., Soussy, C. J., & Leclercq, R.
(1997) Clin Infect Dis 25, 647-653.
Cooper, B. S., Medley, G. F., Stone, S. P., Kibbler, C. C., Cookson, B. D., Roberts, J. A.,
Duckworth, G., Lai, R., & Ebrahim, S. (2004) Proc Natl Acad Sci U S A 101, 10223-10228.
66
329.
330.
331.
332.
333.
334.
335.
336.
337.
338.
339.
340.
341.
342.
343.
344.
345.
346.
347.
348.
349.
350.
351.
352.
353.
354.
Brown, A. R., Amyes, S. G., Paton, R., Plant, W. D., Stevenson, G. M., Winney, R. J., &
Miles, R. S. (1998) J Hosp Infect 40, 115-124.
Cromer, A. L., Hutsell, S. O., Latham, S. C., Bryant, K. G., Wacker, B. B., Smith, S. A.,
Bendyk, H. A., Valainis, G. T., & Carney, M. C. (2004) Am J Infect Control 32, 451-455.
Pittsburgh Regional Project.
Assadian, O., Berger, A., Aspock, C., Mustafa, S., Kohlhauser, C., & Hirschl, A. M. (2002)
Infect Control Hosp Epidemiol 23, 457-461.
Byers, K. E., Durbin, L. J., Simonton, B. M., Anglim, A. M., Adal, K. A., & Farr, B. M.
(1998) Infect Control Hosp Epidemiol 19, 261-264.
Patterson, J. E., Hardin, T. C., Kelly, C. A., Garcia, R. C., & Jorgensen, J. H. (2000) Infect
Control Hosp Epidemiol 21, 455-458.
Bantar, C., Sartori, B., Vesco, E., Heft, C., Saul, M., Salamone, F., & Oliva, M. E. (2003)
Clin Infect Dis 37, 180-186.
Bisson, G., Fishman, N. O., Patel, J. B., Edelstein, P. H., & Lautenbach, E. (2002) Infect
Control Hosp Epidemiol 23, 254-260.
Carling, P., Fung, T., Killion, A., Terrin, N., & Barza, M. (2003) Infect Control Hosp
Epidemiol 24, 699-706.
Quale, J., Landman, D., Saurina, G., Atwood, E., DiTore, V., & Patel, K. (1996) Clin Infect
Dis 23, 1020-1025.
Sample, M. L., Gravel, D., Oxley, C., Toye, B., Garber, G., & Ramotar, K. (2002) Infect
Control Hosp Epidemiol 23, 468-470.
Burke, J. P. & Pestotnik, S. L. (1999) J Chemother 11, 530-535.
Cooper, E., Paull, A., & O'Reilly, M. (2002) Infect Control Hosp Epidemiol 23, 151-153.
Lagerlov, P., Loeb, M., Andrew, M., & Hjortdahl, P. (2000) Qual Health Care 9, 159-165.
Lemmen, S. W., Zolldann, D., Gastmeier, P., & Lutticken, R. (2001) Am J Infect Control 29,
89-93.
Liu, S. C., Leu, H. S., Yen, M. Y., Lee, P. I., & Chou, M. C. (2002) Am J Infect Control 30,
381-385.
Monnet, D. L. (1998) Infect Control Hosp Epidemiol 19, 552-559.
Pestotnik, S. L., Classen, D. C., Evans, R. S., & Burke, J. P. (1996) Ann Intern Med 124, 884890.
NCCLS (2002).
Kupronis, B. A., Richards, C. L., & Whitney, C. G. (2003) J Am Geriatr Soc 51, 1520-1525.
Viray, M., Linkin, D., Maslow, J. N., Stieritz, D. D., Carson, L. S., Bilker, W. B., &
Lautenbach, E. (2005) Infect Control Hosp Epidemiol 26, 56-62.
Chaitram, J. M., Jevitt, L. A., Lary, S., & Tenover, F. C. (2003) J Clin Microbiol 41, 23722377.
Ernst, E. J., Diekema, D. J., BootsMiller, B. J., Vaughn, T., Yankey, J. W., Flach, S. D.,
Ward, M. M., Franciscus, C. L., Acosta, E., Pfaller, M. A., et al. (2004) Diagn Microbiol
Infect Dis 49, 141-145.
Ginocchio, C. C. (2002) Am J Health Syst Pharm 59, S7-11.
Stevenson, K. B., Samore, M., Barbera, J., Moore, J. W., Hannah, E., Houck, P., Tenover, F.
C., & Gerberding, J. L. (2003) Diagn Microbiol Infect Dis 47, 303-311.
Gupta, A., Della-Latta, P., Todd, B., San Gabriel, P., Haas, J., Wu, F., Rubenstein, D., &
Saiman, L. (2004) Infect Control Hosp Epidemiol 25, 210-215.
67
355.
356.
357.
358.
359.
360.
361.
362.
363.
364.
365.
366.
367.
368.
369.
370.
371.
372.
373.
374.
375.
376.
377.
378.
379.
380.
381.
382.
Rodriguez-Bano, J., Navarro, M. D., Romero, L., Muniain, M. A., Perea, E. J., Perez-Cano,
R., Hernandez, J. R., & Pascual, A. (2006) Clin Infect Dis 42, 37-45.
Bhavnani, S. M., Hammel, J. P., Forrest, A., Jones, R. N., & Ambrose, P. G. (2003) Clin
Infect Dis 37, 344-350.
Halstead, D. C., Gomez, N., & McCarter, Y. S. (2004) J Clin Microbiol 42, 1-6.
Fridkin, S. K., Steward, C. D., Edwards, J. R., Pryor, E. R., McGowan, J. E., Jr., Archibald, L.
K., Gaynes, R. P., & Tenover, F. C. (1999) Clin Infect Dis 29, 245-252.
Lang, A., De Fina, G., Meyer, R., Aschbacher, R., Rizza, F., Mayr, O., & Casini, M. (2001)
Eur J Clin Microbiol Infect Dis 20, 657-660.
White, R. L., Friedrich, L. V., Mihm, L. B., & Bosso, J. A. (2000) Clin Infect Dis 31, 16-23.
Zoutman, D. E. & Ford, B. D. (2005) Am J Infect Control 33, 1-5.
cms.
Peterson, L. R., Hamilton, J. D., Baron, E. J., Tompkins, L. S., Miller, J. M., Wilfert, C. M.,
Tenover, F. C., & Thomson Jr, R. B., Jr. (2001) Clin Infect Dis 32, 605-611.
Calfee, D. P., Giannetta, E. T., Durbin, L. J., Germanson, T. P., & Farr, B. M. (2003) Clin
Infect Dis 37, 326-332.
Thompson, R. L., Cabezudo, I., & Wenzel, R. P. (1982) Ann Intern Med 97, 309-317.
Lacey, S., Flaxman, D., Scales, J., & Wilson, A. (2001) J Hosp Infect 48, 308-311.
Greenaway, C. A. & Miller, M. A. (1999) Infect Control Hosp Epidemiol 20, 341-343.
Spindel, S. J., Strausbaugh, L. J., & Jacobson, C. (1995) Infect Control Hosp Epidemiol 16,
217-223.
Bula, C. J., Ghilardi, G., Wietlisbach, V., Petignat, C., & Francioli, P. (2004) J Am Geriatr
Soc 52, 700-706.
High, K. P., Bradley, S., Loeb, M., Palmer, R., Quagliarello, V., & Yoshikawa, T. (2005) Clin
Infect Dis 40, 114-122.
Silverblatt, F. J., Tibert, C., Mikolich, D., Blazek-D'Arezzo, J., Alves, J., Tack, M., &
Agatiello, P. (2000) J Am Geriatr Soc 48, 1211-1215.
CDC (2001) MMWR 50(RR05), 1-43.
Samore, M. H., Venkataraman, L., DeGirolami, P. C., Arbeit, R. D., & Karchmer, A. W.
(1996) Am J Med 100, 32-40.
Brooks, S. E., Veal, R. O., Kramer, M., Dore, L., Schupf, N., & Adachi, M. (1992) Infect
Control Hosp Epidemiol 13, 98-103.
Jernigan, J. A., Siegman-Igra, Y., Guerrant, R. C., & Farr, B. M. (1998) Infect Control Hosp
Epidemiol 19, 494-499.
Chang, V. T. & Nelson, K. (2000) Clin Infect Dis 31, 717-722.
Nicolle, L. E. (2000) Clin Infect Dis 31, 752-756.
Bonten, M. J., Slaughter, S., Hayden, M. K., Nathan, C., van Voorhis, J., & Weinstein, R. A.
(1998) Crit Care Med 26, 2001-2004.
Loeb, M. B., Craven, S., McGeer, A. J., Simor, A. E., Bradley, S. F., Low, D. E., ArmstrongEvans, M., Moss, L. A., & Walter, S. D. (2003) Am J Epidemiol 157, 40-47.
McDonald, L. C., Banerjee, S. N., & Jarvis, W. R. (1998) Infect Control Hosp Epidemiol 19,
772-777.
Montecalvo, M. A., de Lencastre, H., Carraher, M., Gedris, C., Chung, M., VanHorn, K., &
Wormser, G. P. (1995) Infect Control Hosp Epidemiol 16, 680-685.
Shannon, K. P. & French, G. L. (2002) J Antimicrob Chemother 50, 965-969.
68
383.
384.
385.
386.
387.
388.
389.
390.
391.
392.
393.
394.
395.
396.
397.
398.
399.
400.
401.
402.
403.
404.
405.
406.
407.
408.
Singh, K., Gavin, P. J., Vescio, T., Thomson Jr, R. B., Jr., Deddish, R. B., Fisher, A., Noskin,
G. A., & Peterson, L. R. (2003) J Clin Microbiol 41, 2755-2757.
Grmek-Kosnik, I., Ihan, A., Dermota, U., Rems, M., Kosnik, M., & Jorn Kolmos, H. (2005) J
Hosp Infect 61, 155-161.
Villegas, M. V. & Hartstein, A. I. (2003) Infect Control Hosp Epidemiol 24, 284-295.
Ramsey, A. H., Skonieczny, P., Coolidge, D. T., Kurzynski, T. A., Proctor, M. E., & Davis, J.
P. (2001) Infect Control Hosp Epidemiol 22, 423-426.
Harbarth, S., Liassine, N., Dharan, S., Herrault, P., Auckenthaler, R., & Pittet, D. (2000) Clin
Infect Dis 31, 1380-1385.
Lucet, J. C., Chevret, S., Decre, D., Vanjak, D., Macrez, A., Bedos, J. P., Wolff, M., &
Regnier, B. (1996) Clin Infect Dis 22, 430-436.
Malik, R. K., Montecalvo, M. A., Reale, M. R., Li, K., Maw, M., Munoz, J. L., Gedris, C.,
van Horn, K., Carnevale, K. A., Levi, M. H., et al. (1999) Pediatr Infect Dis J 18, 352-356.
Stosor, V., Kruszynski, J., Suriano, T., Noskin, G. A., & Peterson, L. R. (1999) Infect Control
Hosp Epidemiol 20, 653-659.
Srinivasan, A., Song, X., Ross, T., Merz, W., Brower, R., & Perl, T. M. (2002) Infect Control
Hosp Epidemiol 23, 424-428.
Rumbak, M. J. & Cancio, M. R. (1995) Crit Care Med 23, 1200-1203.
Quale, J., Landman, D., Atwood, E., Kreiswirth, B., Willey, B. M., Ditore, V., Zaman, M.,
Patel, K., Saurina, G., Huang, W., et al. (1996) Am J Infect Control 24, 372-379.
Livornese, L. L., Jr., Dias, S., Samel, C., Romanowski, B., Taylor, S., May, P., Pitsakis, P.,
Woods, G., Kaye, D., Levison, M. E., et al. (1992) Ann Intern Med 117, 112-116.
Gastmeier, P., Schwab, F., Geffers, C., & Ruden, H. (2004) Infect Control Hosp Epidemiol
25, 109-113.
Ridwan, B., Mascini, E., van Der Reijden, N., Verhoef, J., & Bonten, M. (2002) Bmj 324,
666-668.
Hitomi, S., Kubota, M., Mori, N., Baba, S., Yano, H., Okuzumi, K., & Kimura, S. (2000) J
Hosp Infect 46, 123-129.
Weber, D. J. & Rutala, W. A. (1997) Infect Control Hosp Epidemiol 18, 306-309.
Schelenz, S. & French, G. (2000) J Hosp Infect 46, 23-30.
Kirschke, D. L., Jones, T. F., Craig, A. S., Chu, P. S., Mayernick, G. G., Patel, J. A., &
Schaffner, W. (2003) N Engl J Med 348, 214-220.
Srinivasan, A., Wolfenden, L. L., Song, X., Mackie, K., Hartsell, T. L., Jones, H. D., Diette,
G. B., Orens, J. B., Yung, R. C., Ross, T. L., et al. (2003) N Engl J Med 348, 221-227.
Mangram, A. & Jarvis, W. R. (1996) Infect Control Hosp Epidemiol 17, 718-720.
Vriens, M. R., Fluit, A. C., Troelstra, A., Verhoef, J., & van der Werken, C. (2002) Infect
Control Hosp Epidemiol 23, 491-494.
Cederna, J. E., Terpenning, M. S., Ensberg, M., Bradley, S. F., & Kauffman, C. A. (1990)
Infect Control Hosp Epidemiol 11, 13-16.
Hachem, R. & Raad, I. (2002) Infect Control Hosp Epidemiol 23, 43-44.
Lui, S. L., Luk, W. K., Cheung, C. Y., Chan, T. M., Lai, K. N., & Peiris, J. S. (2001)
Transplantation 71, 59-64.
Zafar, A. B., Sylvester, L. K., & Beidas, S. O. (2002) Am J Infect Control 30, 425-429.
Darouiche, R., Wright, C., Hamill, R., Koza, M., Lewis, D., & Markowski, J. (1991)
Antimicrob Agents Chemother 35, 1612-1615.
69
409.
410.
411.
412.
Goetz, M. B., Mulligan, M. E., Kwok, R., O'Brien, H., Caballes, C., & Garcia, J. P. (1992)
Am J Med 92, 607-614.
Pan, A., Carnevale, G., Catenazzi, P., Colombini, P., Crema, L., Dolcetti, L., Ferrari, L.,
Mondello, P., Signorini, L., Tinelli, C., et al. (2005) Infect Control Hosp Epidemiol 26, 127133.
Silvestri, L., Milanese, M., Oblach, L., Fontana, F., Gregori, D., Guerra, R., & van Saene, H.
K. (2002) Am J Infect Control 30, 391-399.
Weber, J. M., Sheridan, R. L., Schulz, J. T., Tompkins, R. G., & Ryan, C. M. (2002) Infect
Control Hosp Epidemiol 23, 549-551.
70
71
Table 1. Categorization of Reports about Control of MDROs in Healthcare Settings, 19822005
MDRO
MDR-GNB
MRSA
VRE
No. of Studies
30
35
39
Reviewed/category
Types of Healthcare Facilities from which Study or Report Arose
No. (%) from
30 (100)
28 (80)
33 (85)
academic
facilitiesα
No. (%) from other 0
4 (11)
3 (8)
hospitals
No. (%) from
0
1 (3)
2 (5)
LTCFs
No. (%) from
0
2 (6)
1 (2)
multiple facilities in
a region
Unit of Study for MDRO Control Efforts
20
13
19
Special unitβ
Hospital
10
19
17
LTCF
0
1
2
Region
0
2
1
χ
Nature of Study or Report on MDRO Control
Outbreak
22
19
28
Non-outbreak
8
16
11
Total Period of Observation after Interventions Introduced
Less than 1 year
17
14
25
1-2 years
6
6
6
2-5 years
5
11
8
Greater than 5
2
4
years
Numbers of Control Measures Employed in Outbreaks/Studies
Range
2-12
0-11
1-12
Median
7
7
8
Mode
8
7
9
α
Variably described as university hospitals, medical school affiliated hospitals, VA teaching
hospitals, and, to a much lesser extent, community teaching hospitals
β
Includes intensive care units, burn units, dialysis units, hematology/oncology units, neonatal
units, neonatal intensive care units, and, in a few instances, individual wards of a hospital
χ
Based on authors’ description – if they called their experience an outbreak or not; authors
vary in use of term so there is probable overlap between two categories
71
72
Table 2. Control Measures for MDROs Employed in Studies Performed in Healthcare
Settings, 1982-2005
Focus of MDRO
(No. of Studies)
MDR-GNB
MRSA
VRE
(n=30)
(n=35)
(n=39)
No. (%) of Studies Using Control Measure
19 (63)
11 (31)
20 (53)
Education of staff, patients or
visitors
Emphasis on handwashing
16 (53)
21 (60)
9 (23)
Use of antiseptics for
8 (30)
12 (36)
16 (41)
handwashing
27 (77)
34 (87)
Contact Precautions or glove useα 20 (67)
Private Rooms
4 (15)
10 (28)
10 (27)
Segregation of cases
4 (15)
3 (9)
5 (14)
Cohorting of Patients
11 (37)
12 (34)
14 (36)
Cohorting of Staff
2 (7)
6 (17)
9 (23)
Change in Antimicrobial Use
12 (41)
1 (3)
17 (44)
Surveillance cultures of patients
19 (63)
34 (97)
36 (92)
Surveillance cultures of staff
9 (31)
8 (23)
7 (19)
Environmental cultures
15 (50)
14 (42)
15 (38)
Extra cleaning & disinfection
11 (37)
7 (21)
20 (51)
Dedicated Equipment
5 (17)
0
12 (32)
Decolonization
3 (10)
25 (71)
4 (11)
Ward closure to new admission or 6 (21)
4 (12)
5 (14)
to all patients
Other miscellaneous measures
6 (22) β
9 (27)χ
17 (44)δ
α
Contact Precautions mentioned specifically, use of gloves with gowns or aprons mentioned,
barrier precautions, strict isolation, all included under this heading
β
includes signage, record flagging, unannounced inspections, selective decontamination, and
peer compliance monitoring (1 to 4 studies employing any of these measures)
χ
includes requirements for masks, signage, record tracking, alerts, early discharge, and
preventive isolation of new admissions pending results of screening cultures (1 to 4 studies
employing any of these measures)
δ
includes computer flags, signage, requirement for mask, one-to-one nursing, changing type of
thermometer used, and change in rounding sequence (1 to 7 studies employing any of these
measures)
References for Tables 1 and 2
MDR-GNBs: (6, 8, 9, 11, 16, 38, 174, 175, 180, 209, 210, 213-215, 218, 334, 388, 406, 407)
MRSA: (68, 89, 152, 153, 165-173, 183, 188, 194, 204, 205, 208, 240, 269, 279, 280, 289, 304,
312, 327, 365, 392, 397, 408-412)
72
73
Table 3.
Tier 1. General Recommendations for Routine Prevention and Control of MDROs in Healthcare Settings
Administrative
Measures/Adherence Monitoring
Make MDRO prevention/control an
organizational priority. Provide
administrative support and both fiscal
and human resources to prevent and
control MDRO transmission. (IB)
Identify experts who can provide
consultation and expertise for analyzing
epidemiologic data, recognizing MDRO
problems, or devising effective control
strategies, as needed. (II)
Implement systems to communicate
information about reportable MDROs
to administrative personnel and
state/local health departments. (II)
Implement a multi-disciplinary process
to monitor and improve HCP adherence
to recommended practices for Standard
and Contact Precautions.(IB)
Implement systems to designate
patients known to be colonized or
infected with a targeted MDRO and to
notify receiving healthcare facilities or
personnel prior to transfer of such
patients within or between facilities. (IB)
Support participation in local, regional
and/or national coalitions to combat
emerging or growing MDRO
problems.(IB)
Provide updated feedback at least
annually to healthcare providers and
administrators on facility and patientcare unit MDRO infections. Include
information on changes in prevalence
and incidence, problem assessment
and performance improvement plans.
(IB)
MDRO Education
Provide education and training
on risks and prevention of
MDRO transmission during
orientation and periodic
educational updates for HCP;
include information on
organizational experience with
MDROs and prevention
strategies. (IB)
Judicious
Antimicrobial Use
In hospitals and
LTCFs, ensure that a
multi-disciplinary
process is in place to
review local
susceptibility patterns
(antibiograms), and
antimicrobial agents
included in the
formulary, to foster
appropriate
antimicrobial use. (IB)
Implement systems
(e.g., CPOE,
susceptibility report
comment, pharmacy or
unit director
notification) to prompt
clinicians to use the
appropriate agent and
regimen for the given
clinical situation. (IB)
Provide clinicians with
antimicrobial
susceptibility reports
and analysis of current
trends, updated at least
annually, to guide
antimicrobial
prescribing practices.
(IB)
In settings with limited
electronic
communication system
infrastructures to
implement physician
prompts, etc., at a
minimum implement a
process to review
antibiotic use. Prepare
and distribute reports
to providers. (II)
Surveillance
Use standardized laboratory methods
and follow published guidelines for
determining antimicrobial
susceptibilities of targeted and
emerging MDROs.
Establish systems to ensure that
clinical micro labs (in-house and
outsourced) promptly notify infection
control or a medical director/designee
when a novel resistance pattern for
that facility is detected. (IB)
In hospitals and LTCFs:
…develop and implement laboratory
protocols for storing isolates of
selected MDROs for molecular typing
when needed to confirm transmission
or delineate epidemiology of MDRO
in facility. (IB)
…establish laboratory-based systems
to detect and communicate evidence
of MDROs in clinical isolates (IB)
…prepare facility-specific
antimicrobial susceptibility reports as
recommended by CLSI; monitor
reports for evidence of changing
resistance that may indicate
emergence or transmission of
MDROs (IA/IC)
Infection Control Precautions to Prevent
Transmission
Follow Standard Precautions in all healthcare
settings. (IB)
Use of Contact Precautions (CP):
--- In acute care settings : Implement CP for all
patients known to be colonized/infected with target
MDROs.(IB)
--- In LTCFs: Consider the individual patient’s clinical
situation and facility resources in deciding whether to
implement CP (II)
--- In ambulatory and home care settings, follow
Standard Precautions (II)
---In hemodialysis units: Follow dialysis specific
guidelines (IC)
No recommendation can be made regarding when to
discontinue CP. (Unresolved issue)
Masks are not recommended for routine use to
prevent transmission of MDROs from patients to
HCWs. Use masks according to Standard
Precautions when performing splash-generating
procedures, caring for patients with open
tracheostomies with potential for projectile secretions,
and when there is evidence for transmission from
heavily colonized sources (e.g., burn wounds).
Patient placement in hospitals and LTCFs:
…develop and monitor special-care
unit-specific antimicrobial
susceptibility reports (e.g., ventilatordependent units, ICUs, oncology
units). (IB)
When single-patient rooms are available, assign
priority for these rooms to patients with known or
suspected MDRO colonization or infection. Give
highest priority to those patients who have conditions
that may facilitate transmission, e.g., uncontained
secretions or excretions. When single-patient rooms
are not available, cohort patients with the same
MDRO in the same room or patient-care area. (IB)
…monitor trends in incidence of
target MDROs in the facility over time
to determine if MDRO rates are
decreasing or if additional
interventions are needed. (IA)
When cohorting patients with the same MDRO is not
possible, place MDRO patients in rooms with patients
who are at low risk for acquisition of MDROs and
associated adverse outcomes from infection and are
likely to have short lengths of stay. (II)
73
Environmental Measures
Follow recommended
cleaning, disinfection and
sterilization guidelines for
maintaining patient care areas
and equipment.
Dedicate non-critical medical
items to use on individual
patients known to be infected
or colonized with an MDRO.
Prioritize room cleaning of
patients on Contact
Precautions. Focus on
cleaning and disinfecting
frequently touched surfaces
(e.g., bed rails, bedside
commodes, bathroom fixtures
in patient room, doorknobs)
and equipment in immediate
vicinity of patient.
Decolonization
Not recommended
routinely
74
Tier 2. Recommendations for Intensified MDRO control efforts
Institute one or more of the interventions described below when 1) incidence or prevalence of MDROs are not decreasing despite the use of routine control measures; or 2) the first case or outbreak of an
epidemiologically important MDRO (e.g., VRE, MRSA, VISA, VRSA, MDR-GNB) is identified within a healthcare facility or unit (IB) Continue to monitor the incidence of target MDRO infection and
colonization; if rates do not decrease, implement additional interventions as needed to reduce MDRO transmission.
Administrative
Measures/Adherence Monitoring
Obtain expert consultation from persons
with experience in infection control and
the epidemiology of MDROS, either inhouse or through outside consultation,
for assessment of the local MDRO
problem and guidance in the design,
implementation and evaluation of
appropriat4e control measures. (IB)
Provide necessary leadership, funding
and day-to-day oversight to implement
interventions selected. (IB)
Evaluate healthcare system factors for
role in creating or perpetuating MDRO
transmission, including staffing levels,
education and training, availability of
consumable and durable resources;
communication processes, and
adherence to infection control
measures.(IB)
Update healthcare providers and
administrators on the progress and
effectiveness of the intensified
interventions. (IB)
MDRO Education
Intensify the frequency of
educational programs for
healthcare personnel,
especially for those who work
in areas where MDRO rates
are not decreasing. Provide
individual or unit-specific
feedback when available. (IB)
Judicious
Antimicrobial Use
Review the role of
antimicrobial use in
perpetuating the
MDRO problem
targeted for intensified
intervention. Control
and improve
antimicrobial use as
indicated. Antimicrobial
agents that may be
targeted include
d
vancomycin, thirdgeneration
cephalosporins, antianaerobic agents for
VRE; third generation
cephalosporins for
ESBLs; and quinolones
and carbapenems. (IB)
Surveillance
Calculate and analyze incidence
rates of target MDROs (single
isolates/patient; location-, servicespecific) (IB)
Increase frequency of compiling,
monitoring antimicrobial susceptibility
summary reports (II)
Implement laboratory protocols for
storing isolates of selected MDROs
for molecular typing; perform typing if
needed (IB)
Develop and implement protocols to
obtain active surveillance cultures
from patients in populations at risk.
(IB) (See recommendations for
appropriate body sites and culturing
methods.)
Conduct culture surveys to assess
efficacy of intensified MDRO control
interventions.
Conduct serial (e.g., weekly) unitspecific point prevalence culture
surveys of the target MDRO to
determine if transmission has
decreased or ceased.(IB)
Repeat point-prevalence culturesurveys at routine intervals and at
time of patient discharge or transfer
until transmission has ceased. (IB)
If indicated by assessment of the
MDRO problem, collect cultures to
assess the colonization status of
roommates and other patients with
substantial exposure to patients with
known MDRO infection or
colonization. (IB)
Obtain cultures from HCP for target
MDROs when there is epidemiologic
evidence implicating the staff member
as a source of ongoing transmission.
(IB)
74
Infection Control Precautions to Prevent
Transmission
Use of Contact Precautions:
Implement Contact Precautions (CP) routinely for
all patients colonized or infected with a target
MDRO. (IA)
Don gowns and gloves before or upon entry to
the patient’s room or cubicle. (IB)
In LTCFs, modify CP to allow MDROcolonized/infected patients whose site of
colonization or infection can be appropriately
contained and who can observe good hand
hygiene practices to enter common areas and
participate in group activities
When active surveillance cultures are obtained as
part of an intensified MDRO control program,
implement CP until the surveillance culture is
reported negative for the target MDRO (IB)
No recommendation is made for universal use of
gloves and/or gowns. (Unresolved issue)
Implement policies for patient admission and
placement as needed to prevent transmission of
the problem MDRO. (IB)
When single-patient rooms are available, assign
priority for these rooms to patients with known or
suspected MDRO colonization or infection. Give
highest priority to those patients who have conditions
that may facilitate transmission, e.g., uncontained
secretions or excretions. When single-patient rooms
are not available, cohort patients with the same
MDRO in the same room or patient-care area. (IB)
When cohorting patients with the same MDRO is not
possible, place MDRO patients in rooms with patients
who are at low risk for acquisition of MDROs and
associated adverse outcomes from infection and are
likely to have short lengths of stay. (II)
Stop new admissions to the unit or facility if
transmission continues despite the
implementation of the intensified control
measures. (IB)
Environmental Measures
Implement patient.-dedicated
use of non-critical equipment
(IB)
Intensify and reinforce training
of environmental staff who
work in areas targeted for
intensified MDRO control.
Some facilities may choose to
assign dedicated staff to
targeted patient care areas to
enhance consistency of proper
environmental cleaning and
disinfection services (IB)
Monitor cleaning
performance to ensure
consistent cleaning and
disinfection of surfaces in
close proximity to the
patient and those likely to be
touched by the patient and
HCWs (e.g., bedrails, carts,
bedside commodes,
doorknobs, faucet handles)
(IB).
Obtain environmental cultures
(e.g., surfaces, shared
equipment) only when
epidemiologically implicated in
transmission (IB)
Vacate units for
environmental assessment
and intensive cleaning when
previous efforts to control
environmental transmission
have failed (II)
Decolonization
Consult with experts on a
case-by-case basis
regarding the appropriate
use of decolonization
therapy for patients or
staff during limited period
of time as a component of
an intensified MRSA
control program (II)
When decolonization for
MRSA is used, perform
susceptibility testing for
the decolonizing agent
against the target
organism or the MDRO
strain epidemiologically
implicated in
transmission. Monitor
susceptibility to detect
emergence of resistance
to the decolonizing agent.
Consult with
microbiologists for
appropriate testing for
mupirocin resistance,
since standards have not
been established.
Do not use topical
mupirocin routinely for
MRSA decolonization of
patients as a component
of MRSA control
programs in any
healthcare setting. (IB)
Limit decolonization to
HCP found to be
colonized with MRSA who
have been
epidemiologically
implicated in ongoing
transmission of MRSA to
patients. (IB)
No recommendation can
be made for
decolonization of patients
who carry VRE or MDRGNB.
| File Type | application/pdf |
| File Title | Microsoft Word - MDRO guideline 2006 Nov 21 _2_.doc |
| Author | bzw8 |
| File Modified | 2007-07-24 |
| File Created | 2006-12-07 |