Management of multidrug-resistant organisms in health care settings, 2006

Article Outline

• Background
  • MDRO definition
  • Clinical importance of MDROs
• Epidemiology of MDRO
  • Trends
  • Important concepts in transmission
  • Role of colonized HCP in MDRO transmission
  • Implications of community-associated MRSA
• MDRO prevention and control
  • Prevention of infections
  • Prevention and control of MDRO transmission: overview of the MDRO control literature
  • Control interventions
    • Administrative support
    • Education
    • Judicious use of antimicrobial agents
    • MDRO surveillance
  • Surveillance for MDROs isolated from routine clinical cultures: antibiograms
  • MDRO incidence based on clinical culture results
  • MDRO infection rates
  • Molecular typing of MDRO isolates
  • Surveillance for MDROs by detecting asymptomatic colonization
    • Infection control precautions
  • Cohorting and other MDRO control strategies
  • Duration of contact precautions
  • Barriers used for contact with patients infected or colonized with MDROs
  • Impact of contact precautions on patient care and well-being
    • Environmental measures
    • Decolonization
• Discussion
  • Impact on other MDROs from interventions targeted to 1 MDRO
  • Costs
  • Feasibility
  • Factors that influence selection of MDRO control measures
  • Differences of opinion on the optimal strategy to control MDROs
  • Two-tiered approach for control of MDROs
• Prevention of transmission of MDROs
  • Glossary: MDROs
• Acknowledgment
• References
• Copyright

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 health care 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 (eg, 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 health care 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 health care 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 require administrative and scientific leadership and a financial and human resource commitment.³, ⁴, 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 health care personnel (HCP) are more receptive and adherent to the recommended control measures when organizational leaders participate in efforts to reduce MDRO transmission.³

Back to Article Outline

Background 

MDRO definition 

For epidemiologic purposes, MDROs are defined as microorganisms, predominantly bacteria, that are resistant to 1 or more classes of antimicrobial agents.¹ Although the names of certain MDROs describe resistance to only 1 agent (eg, MRSA, VRE), these pathogens are frequently resistant to most available antimicrobial agents. These highly resistant organisms deserve special attention in health care facilities.² In addition to MRSA and VRE, certain GNB, including those producing extended spectrum β-lactamases (ESBLs) and others that are resistant to multiple classes of antimicrobial agents, are of particular concern. (Multidrug-resistant strains of Mycobacterium 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.) In addition to Escherichia coli and Klebsiella pneumoniae, these include strains of Acinetobacter baumannii resistant to all antimicrobial agents, or all except imipenem,⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹² and organisms such as Stenotrophomonas maltophilia,¹², ¹³, ¹⁴ Burkholderia cepacia,¹⁵, ¹⁶ and Ralstonia pickettii¹⁷ that are intrinsically resistant to the broadest spectrum antimicrobial agents. In some residential settings (eg, LTCFs), it is important to control multidrug-resistant Streptococcus 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 (ie, vancomycin-intermediate S aureus [VISA], vancomycin-resistant S aureus [VRSA])²⁰, ²¹, ²², ²³, ²⁴, ²⁵, ²⁶, ²⁷, ²⁸, ²⁹, 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 1990s, 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 isolates.³¹, ³², ³³, ³⁴, ³⁵, ³⁶, 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, ⁹, ¹⁰, ¹¹, ³⁸ and intrinsically resistant Stenotrophomonas species.¹², ¹³, 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 (ie, selective advantage).⁴⁰

Increased lengths of stay, costs, and mortality also have been associated with MDROs.⁴¹, ⁴², ⁴³, ⁴⁴, ⁴⁵, ⁴⁶ Two studies documented increased mortality, hospital lengths of stay, and hospital charges associated with multidrug-resistant gram-negative bacilli (MDR-GNBs), including a NICU outbreak of ESBL-producing Klebsiella pneumoniae⁴⁷ and the emergence of third-generation cephalosporin resistance in Enterobacter species in hospitalized adults.⁴⁸ Vancomycin resistance has been reported to be an independent predictor of death from enterococcal bacteremia.⁴⁴, ⁴⁹, ⁵⁰, ⁵¹, ⁵², 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 with patients with methicillin-susceptible S aureus (MSSA), MRSA-colonized patients more frequently develop symptomatic infections.⁵⁵, ⁵⁶ Furthermore, higher case fatality rates have been observed for certain MRSA infections, including bacteremia,⁵⁷, ⁵⁸, ⁵⁹, ⁶⁰, ⁶¹, 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 health care costs,⁴⁶, ⁶¹, ⁶² whereas 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

Back to Article Outline

Epidemiology of MDRO 

Trends 

Prevalence of MDROs varies temporally, geographically, and by health care 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 (eg, 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, ⁷⁹, ⁸⁰, ⁸¹, ⁸², ⁸³, ⁸⁴, ⁸⁵, ⁸⁶, ⁸⁷, 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 8 US pediatric ICUs and 7 US NICUs in 2000 found that ≤4% of patients were colonized with MRSA or VRE compared with 10% to 24% who 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 US 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% to 25% of S 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 1999⁹⁴ and 28.5% in 2003.⁹³

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 that 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

Last, an analysis of temporal trends of antimicrobial resistance in non-ICU patients in 23 US hospitals during 1996-1997 and 1998-1999⁹⁷ 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 the following: selective pressure exerted by exposure to antimicrobial agents, particularly fluoroquinolones, outside of the ICU and/or in the community⁷, ⁹⁶, ⁹⁸; increasing rates of community-associated MRSA colonization and infection⁹⁹, ¹⁰⁰; inadequate adherence to infection control practices; or a combination of these factors.

Important concepts in transmission 

Once MDROs are introduced into a health care 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 (eg, urinary catheters or endotracheal tubes.¹⁰³, ¹⁰⁴ Hospitalized patients, especially ICU patients, tend to have more risk factors than nonhospitalized patients 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 of 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, ¹⁰⁷, ¹⁰⁸, ¹⁰⁹ Hands are easily contaminated during the process of caregiving or from contact with environmental surfaces in close proximity to the patient.¹¹⁰, ¹¹¹, ¹¹², ¹¹³ The latter is especially important when patients have diarrhea and the reservoir of the MDRO is the gastrointestinal tract.¹¹⁴, ¹¹⁵, ¹¹⁶, 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 result from patients receiving care at multiple health care facilities and moving between acute care, ambulatory, and/or chronic care and LTC environments. System-wide surveillance at LDS Hospital in Salt Lake City, UT, 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 health care 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, ¹²¹, ¹²², 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

Implications of community-associated 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 health care settings.¹²⁵, ¹²⁶, ¹²⁷, 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 health care 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 community-associated (CA)-MRSA infections have been microbiologically distinct from those endemic in health care settings, suggesting that some of these strains may have arisen de novo in the community via acquisition of methicillin resistance genes by established MSSA strains.¹³⁰, ¹³¹, ¹³² Two pulsed-field types, termed USA300 and USA400 according to a typing scheme established at the Centers for Disease Control and Prevention (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 health care settings.¹³³

USA300 and USA400 genotypes almost always carry type IV of the staphylococcal chromosomal cassette 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 health care-associated MRSA strains, and is hypothesized to be more easily transferable among 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, ¹³⁵, ¹³⁶

Transmission within hospitals of MRSA strains first described in the community (eg, USA300 and USA400) are being reported with increasing frequency.¹³⁷, ¹³⁸, ¹³⁹, 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 health care-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 health care-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 health care settings.

Back to Article Outline

MDRO prevention and control 

Prevention of infections 

Preventing infections will reduce the burden of MDROs in health care 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 4 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 has been implemented in many US health care facilities.¹¹⁸, ¹⁴¹, ¹⁴², ¹⁴³, 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 has not been reported, it is logical that decreasing these and other health care-associated infections will in turn reduce antimicrobial use and decrease opportunities for emergence and transmission of MDROs.

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 health care facilities. Representative studies include the following:

•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 (Table 1, Table 2). Case-rate reduction or pathogen eradication was reported in a majority of studies.

Table 1. Categorization of reports about control of MDROs in health care settings, 1982-2005

MDRO	MDR-GNB	MRSA	VRE
No. of studies reviewed/category	30	35	39
Types of health care facilities from which study or report arose
No. (%) from academic facilities∗	30 (100)	28 (80)	33 (85)
No. (%) from other hospitals	0	4 (11)	3 (8)
No. (%) from LTCFs	0	1 (3)	2 (5)
No. (%) from multiple facilities in a region	0	2 (6)	1 (2)
Unit of study for MDRO control efforts
Special unit†	20	13	19
Hospital	10	19	17
LTCF	0	1	2
Region	0	2	1
Nature of study or report on MDRO control‡
Outbreak	22	19	28
Nonoutbreak	8	16	11
Total period of observation after interventions introduced
Less than 1 yr	17	14	25
1-2 yr	6	6	6
2-5 yr	5	11	8
Greater than 5 yr	2	4
Numbers of control measures employed in outbreaks/studies
Range	2-12	0-11	1-12
Median	7	7	8
Mode	8	7	9

References for MDR-GNBs.⁶, ⁸, ⁹, ¹¹, ¹⁶, ³⁸, ¹⁷⁴, ¹⁷⁵, ¹⁸⁰, ²⁰⁹, ²¹⁰, ²¹³, ²¹⁴, ²¹⁵, ²¹⁸, ³³⁴, ³⁸⁸, ⁴⁰⁶, ⁴⁰⁷ References for MRSA.⁶⁸, ⁸⁹, ¹⁵², ¹⁵³, ¹⁶⁵, ¹⁶⁶, ¹⁶⁷, ¹⁶⁸, ¹⁶⁹, ¹⁷⁰, ¹⁷¹, ¹⁷², ¹⁷³, ¹⁸³, ¹⁸⁸, ¹⁹⁴, ²⁰⁴, ²⁰⁵, ²⁰⁸, ²⁴⁰, ²⁶⁹, ²⁷⁹, ²⁸⁰, ²⁸⁹, ³⁰⁴, ³¹², ³²⁷, ³⁶⁵, ³⁹², ³⁹⁷, ⁴⁰⁸, ⁴⁰⁹, ⁴¹⁰, ⁴¹¹, ⁴¹²

∗Variably described as university hospitals, medical school affiliated hospitals, VA teaching hospitals, and, to a much lesser extent, community teaching hospitals.

†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.

‡Based on authors' description: whether they called their experience an outbreak or not; authors vary in use of term, so there is probable overlap between 2 categories.

Table 2. Control measures for MDROs employed in studies performed in health care settings, 1982-2005

	MDR-GNB (n = 30)	MRSA (n = 35)	VRE (n = 39)
Focus of MDRO (No. of studies)	No. (%) of studies using control measure
Education of staff, patients, or visitors	19 (63)	11 (31)	20 (53)
Emphasis on handwashing	16 (53)	21 (60)	9 (23)
Use of antiseptics for handwashing	8 (30)	12 (36)	16 (41)
Contact precautions or glove use∗	20 (67)	27 (77)	34 (87)
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 and 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 to all patients	6 (21)	4 (12)	5 (14)
Other miscellaneous measures	6 (22)†	9 (27)‡	17 (44)§

References for MDR-GNBs.⁶, ⁸, ⁹, ¹¹, ¹⁶, ³⁸, ¹⁷⁴, ¹⁷⁵, ¹⁸⁰, ²⁰⁹, ²¹⁰, ²¹³, ²¹⁴, ²¹⁵, ²¹⁸, ³³⁴, ³⁸⁸, ⁴⁰⁶, ⁴⁰⁷ References for MRSA.⁶⁸, ⁸⁹, ¹⁵², ¹⁵³, ¹⁶⁵, ¹⁶⁶, ¹⁶⁷, ¹⁶⁸, ¹⁶⁹, ¹⁷⁰, ¹⁷¹, ¹⁷², ¹⁷³, ¹⁸³, ¹⁸⁸, ¹⁹⁴, ²⁰⁴, ²⁰⁵, ²⁰⁸, ²⁴⁰, ²⁶⁹, ²⁷⁹, ²⁸⁰, ²⁸⁹, ³⁰⁴, ³¹², ³²⁷, ³⁶⁵, ³⁹², ³⁹⁷, ⁴⁰⁸, ⁴⁰⁹, ⁴¹⁰, ⁴¹¹, ⁴¹²

∗Contact precautions mentioned specifically, use of gloves with gowns or aprons mentioned, barrier precautions, strict isolation, all included under this heading.

†Includes signage, record flagging, unannounced inspections, selective decontamination, and peer compliance monitoring (1 to 4 studies employing any of these measures).

‡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).

§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).

These success stories testify to the importance of having dedicated and knowledgeable teams of health care 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 a 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 (eg, added emphasis on handwashing) and did not include them as interventions, and some “single measures” are, in fact, a complex 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, end points and variables measured, and period of follow-up. Two thirds of the reports cited in Table 1, Table 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 health care facilities to implement to control their target MDROs. Randomized controlled trials are necessary to acquire this level of evidence. A National Institutes of Health (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 7 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 health care 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.

Table 3. General recommendations for routine prevention and control of MDROs in health care settings

NOTE. Institute 1 or more of the interventions described in Tier 2 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 (eg, VRE, MRSA, VISA, VRSA, MDR-GNB) is identified within a health care 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.

CP, contact precautions; CPOE, computerized physician order entry.

In several reports, administrative support and involvement were important for the successful control of the target MDRO,³, ¹⁵², ¹⁸², ¹⁸³, ¹⁸⁴, ¹⁸⁵ and authorities in infection control have strongly recommended such support.², ¹⁰⁶, ¹⁰⁷, 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, ¹⁸⁸, ¹⁸⁹, ¹⁹⁰, ¹⁹¹, ¹⁹² Other interventions that require administrative support include the following: (1) implementing system changes to ensure prompt and effective communications, eg, computer alerts to identify patients previously known to be colonized/infected with MDROs¹⁸⁴, ¹⁸⁹, ¹⁹³, ¹⁹⁴; (2), providing the necessary number and appropriate placement of handwashing sinks and alcohol-containing handrub dispensers in the facility¹⁰⁶, ¹⁹⁵; (3) maintaining staffing levels appropriate to the intensity of care required¹⁵², ¹⁹⁶, ¹⁹⁷, ¹⁹⁸, ¹⁹⁹, ²⁰⁰, ²⁰¹, ²⁰²; and (4) enforcing adherence to recommended infection control practices (eg, hand hygiene, standard and contact precautions) for MDRO control. Other measures that have been associated with a positive impact on prevention efforts, which 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, ²⁰⁴, 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 Last, 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

Facility-wide, unit-targeted, and informal, educational interventions were included in several successful studies.³, ¹⁸⁹, ¹⁹³, ²⁰⁸, ²⁰⁹, ²¹⁰, 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 health care settings.³, ¹⁰⁶, ¹⁶³

Although 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, ²¹³, ²¹⁴, ²¹⁵, ²¹⁶, ²¹⁷, 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 because of a combination of factors, including (1) the relative effect of antimicrobials on providing initial selective pressure, compared with 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 numbers 2 and 3 above in the study design, one study demonstrated a decrease in the prevalence of VRE associated with a formulary switch from ticarcillin-clavulanate 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 implementation²²² (www.cdc.gov/drugresistance/healthcare). This effort targets all health care 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 health care facilities include education; formulary restriction; prior approval programs, including preapproved indications; automatic stop orders; academic interventions to counteract pharmaceutical influences on prescribing patterns; antimicrobial cycling²²³, ²²⁴, ²²⁵, ²²⁶; computer-assisted management programs²²⁷, ²²⁸, ²²⁹; and active efforts to remove redundant antimicrobial combinations.²³⁰ A systematic review of controlled studies identified several successful practices. These include social marketing (ie, 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

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 health care 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.²³³, ²³⁴, ²³⁵

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 (eg, new MDRO isolates/1000 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 population or location. Isolating a 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 ASC to identify patients who are colonized with a targeted MDRO.³⁸, ¹⁰⁷, ²⁴¹ This approach is based on 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, ¹⁹², ¹⁹³, ²⁴², ²⁴³, ²⁴⁴ Several authors report having used ASC when new pathogens emerge 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 health care-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 methodologic 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 (vs no cultures) could potentially decrease transmission 39% and that, with preemptive 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 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 in which 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 extended-spectrum β-lactamase-producing Enterobacteriaceae over a 6-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:

Since 1996, the 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, ²⁶⁹, ²⁷⁰, ²⁷¹ 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 because of lack of sensitivity, laboratory deficiencies, or intermittent colonization because of antimicrobial therapy.²⁶² Therefore, standard precautions must be used 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 Settings¹⁰⁶ cited 9 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).

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 (eg, 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 (eg, VRE, C difficile, noroviruses and other intestinal tract agents; respiratory syncytial virus).¹⁰⁹, ¹¹¹, ²⁷⁴, ²⁷⁵, ²⁷⁶, 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 closure³⁸, ¹⁴⁶, ¹⁵⁹, ¹⁶¹, ²⁷⁹, ²⁸⁰ were necessary to control transmission. Some authors indicated that implementation of the latter 2 strategies were the turning points in their control efforts; however, these measures usually followed many other actions to prevent transmission. In one, 2-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 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 3 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 received antimicrobial therapy, and persistent or intermittent carriage of VRE for more than 1 year has been reported.²⁸⁴, ²⁸⁵, 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 in which they were first implemented. In general, it seems reasonable to discontinue contact precautions when 3 or more surveillance cultures for the target MDRO are repeatedly negative over the course of a week or 2 in a patient who has not received antimicrobial therapy for several weeks, especially in the absence of a 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 whereas 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 4 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, 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 rooms²⁹¹ or examine²⁹² 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 health care team to counteract these potential adverse effects.

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, ¹¹⁰, ¹¹¹, ²⁹⁷, ²⁹⁸ Although 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 (eg, bed rails, charts, bedside commodes, doorknobs). A common reason given for finding environmental contamination with a 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

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 (eg, 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 colonization.³⁰⁴ These and other methods of MRSA decolonization have been thoroughly reviewed.³⁰³, ³⁰⁵, ³⁰⁶, ³⁰⁷

Decolonization regimens are not sufficiently effective to warrant routine use. Therefore, most health care 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, ³⁰⁹, 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.

Back to Article Outline

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 health care 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 quasiexperimental 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.

Impact on other MDROs from interventions targeted to 1 MDRO 

Only 1 report described control efforts directed at more than 1 MDRO, ie, MDR-GNB and MRSA.³¹² Several reports have shown either decreases or increases in other pathogens with efforts to control 1 MDRO. For example, 2 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 a NICU.³¹³ In contrast, Wright et al 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 cocolonized with >1 MDRO; a detailed analysis showed that risk factors for colonization varied by pathogen.³¹⁶ One review of the literature³¹⁷ reported that patient risk factors associated with colonization with MRSA, VRE, MDR-GNB, C difficile, and Candida species were the same. This review concluded that control programs that focus on only 1 organism or 1 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 health care 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 the growing problem of antimicrobial resistance, and the recognized role of all health care 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 health care facilities. Many factors influence the choice of interventions to be applied within an institution, including the following:

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 compared³²³; recommended interventions are similar. Other guidelines for VRE and MRSA, eg, 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, 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 nonacute care settings (eg, 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 health care facilities have included 7 categories of interventions (Table 3). As a rule, these reports indicate that facilities confronted with a MDRO problem selected a combination of control measures, implemented them, and reassessed their impact. In some cases, new measures were added serially to enhance further the control efforts. This evidence indicates that the control of MDROs is a dynamic process that requires a systematic approach tailored to the problem and health care setting. The nature of this evidence gave rise to the 2-tiered approach to MDRO control 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 health care settings follow and are summarized in Table 3. Table 3, which applies to all health care settings, contains 2 tiers of activities. In the first tier is the baseline level of MDRO control activities designed to ensure recognition of MDROs as a problem, of involvement of health care administrators, and of provision of safeguards for managing unidentified carriers of MDROs.

With the emergence of a 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 the following:

The combination of new or increased frequency of MDRO isolates and patients at risk necessitates escalation of efforts to achieve or reestablish control, ie, 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 health care 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 whether additional measures or consultation are indicated. The result of this process should be to decrease MDRO rates to minimum levels. Health care 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.

Back to Article Outline

Prevention of transmission of MDROs 

The CDC/HICPAC system for categorizing recommendations is as follows:

Category IA: Strongly recommended for implementation and strongly supported by well-designed 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 health care settings independent of the prevalence of 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 health care organization.³, ⁹, ¹⁴⁶, ¹⁵², ¹⁸², ¹⁸³, ¹⁸⁴, ²⁰⁸, ³²⁸, ³²⁹ Category IB.

V.A.1.c. In health care facilities without expertise for analyzing epidemiologic data, recognizing MDRO problems, or devising effective control strategies (eg, small or rural hospitals, rehabilitation centers, 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 (eg, VRSA, VISA, MRSA, penicillin-resistant S pneumoniae) to administrative personnel and as required by state and local health authorities (www.cdc.gov/epo/dphsi/nndsshis.htm). Refer to Web sites for updated requirements of local and state health departments. Category II/IC.

V.A.1.e. Implement a multidisciplinary process to monitor and improve 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 health care 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 health care 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 health care 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 HCP.

V.A.2.a. 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.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 (antibiograms), and antimicrobial agents included in the formulary to foster appropriate antimicrobial use.²⁰⁹, ²¹², ²¹⁴, ²¹⁵, ²¹⁷, ²⁴², ²⁵⁴, ³³⁴, ³³⁵, ³³⁶, ³³⁷, ³³⁸, ³³⁹ Category IB.

V.A.3.b. Implement systems (eg, 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, ³⁴¹, ³⁴², ³⁴³, ³⁴⁴, ³⁴⁵, 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 (eg, 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 (eg, MRSA, VRE, MDR-ESBLs) and emerging (eg, VRSA, MDR-Acinetobacter baumannii) MDROs.⁸, ¹⁵⁴, ¹⁷⁷, ¹⁹⁰, ¹⁹³, ²⁰⁹, ²⁵⁴, ³⁴⁷, ³⁵⁰, ³⁵¹, ³⁵², ³⁵³ Category IB.

V.A.4.b. In all health care organizations, establish systems to ensure that clinical microbiology laboratories (in-house and outsourced) 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 confirm transmission or delineate the epidemiology of the MDRO within the health care 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 (eg, ventilator dependent, ICU, or oncology units), develop and monitor unit-specific antimicrobial susceptibility reports.³⁵⁸, ³⁵⁹, ³⁶⁰, ³⁶¹ Category IB.

V.A.4.d.ii. 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 health care organizations that outsource microbiology laboratory services (eg, 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 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 (ie, location and clinical service) in MDRO monitoring protocols in hospitals and other large multiunit facilities with high-risk patients.⁸, ³⁸, ¹⁵², ¹⁵³, ¹⁵⁴, ²¹⁷, ³⁵⁸, ³⁶¹ Category IB.

V.A.4.e.ii. Establish a baseline (eg, 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 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 health care is delivered.¹¹⁹, ¹⁶⁴, ²⁵⁵, ³¹⁵, ³¹⁶ Category IB.

V.A.5.b. Use masks according to standard precautions when performing splash-generating procedures (eg, wound irrigation, oral suctioning, intubation); when caring for patients with open tracheostomies and the potential for projectile secretions; and in circumstances in which there is evidence of transmission from heavily colonized sources (eg, burn wounds). Masks are not otherwise recommended for prevention of MDRO transmission from patients to HCP during routine care (eg, 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 who have been previously identified as being colonized with target MDROs (eg, 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 (eg, 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.⁷⁸, ⁷⁹, ⁸⁰, ⁸⁵, ¹⁵¹, ³⁶⁷, ³⁶⁸ Category II.

V.A.5.c.ii.2. For ill residents (eg, those totally dependent on HCP for health care and activities of daily living, ventilator dependent) 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, the following apply:

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 section 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, eg, 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, ¹⁵², 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 (eg, bed rails, over bed tables) and frequently touched surfaces in the patient care environment (eg, doorknobs, surfaces in and surrounding toilets in patients' rooms) on a more frequent schedule compared with that for minimal touch surfaces (eg, 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 (eg, bed rails, bedside commodes, bathroom fixtures in the patient's room, doorknobs) and equipment in the immediate vicinity of the patient.¹⁰⁹, ¹¹⁰, ¹¹⁴, ¹¹⁵, ¹¹⁶, 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 health care 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 health care 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 1 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, ¹⁵³, ¹⁵⁴, ¹⁸³, ¹⁸⁴, ¹⁸⁵, ¹⁸⁹, ¹⁹⁰, ¹⁹³, ¹⁹⁴, ²⁰⁹, ²¹⁷, ²⁴², ³¹², ³⁶⁴, ³⁶⁵ Category IB within a health care facility or unit.²², ²³, ²⁵, ⁶⁸, ¹⁷⁰, ¹⁷², ¹⁸⁴, ²⁴⁰, ²⁴², ³⁷⁸ 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 1 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 (eg, VRE, MRSA, VISA, VRSA, MDR-GNB) is identified.

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, ¹⁵², ¹⁵³, 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 health care 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 health care 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 (eg, 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 health care 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 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 HCP, 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 antianaerobic agents for VRE²¹⁷; third-generation cephalosporins for ESBLs²¹², 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 1 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 ASC for targeted MDROs from patients in populations at risk (eg, patients in intensive care, burn, bone marrow/stem cell transplant, and oncology units; patients transferred from facilities known to have high 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, ¹⁵², ¹⁵³, ¹⁵⁴, ¹⁶⁷, ¹⁶⁸, ¹⁸³, ¹⁸⁴, ¹⁸⁷, ¹⁸⁸, ¹⁸⁹, 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, (eg, Acinetobacter species, Burkholderia species).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, eg, 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 (eg, weekly, until transmission has ceased and then decreasing frequency) unit-specific point prevalence culture surveys of the target MDRO to determine whether 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, ¹⁵³, ¹⁵⁴, ¹⁶⁸, ¹⁷⁸, ¹⁹⁰, ²¹⁵, ²¹⁸, ²⁴², ³⁸⁸ Category IB.

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 HCP for target MDRO when there is epidemiologic evidence implicating the health care 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 MDRO-colonized/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.

V.B.7.a.i. Place MDRO patients in single-patient rooms.⁶, ¹⁵¹, ¹⁵⁸, ¹⁶⁰, ¹⁶⁶, ¹⁷⁰, ¹⁸⁷, ²⁰⁸, ²⁴⁰, ²⁸², ³⁹³, ³⁹⁴, ³⁹⁵ Category IB.

V.B.7.a.ii. Cohort patients with the same MDRO in designated areas (eg, 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 (eg, 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, ¹⁷⁹, ¹⁸⁰, ¹⁸¹, ¹⁹³, ²⁰⁵, ²⁰⁸, ²¹⁷, ²⁷⁹, ³⁰¹, ³²⁷, ³³⁹, ³⁹⁷ Category IB.

V.B.8.c. Monitor (ie, 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 (eg, bed rails, 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 (eg, surfaces, shared medical equipment) when there is epidemiologic evidence that an environmental source is associated with ongoing transmission of the targeted MDRO.³⁹⁹, ⁴⁰⁰, ⁴⁰¹, 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 health care 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 because standards have not been established.²⁸⁹, ²⁹⁰, ³⁰⁴, ³⁰⁸ Category IB if decolonization is not successful and ongoing transmission to patients persists.¹²⁰, ¹²², ¹⁶⁸ 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 health care 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.

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.

Glossary: MDROs 

Ambulatory care settings: Facilities that provide health care to patients who do not remain overnight (eg, hospital-based outpatient clinics, nonhospital-based clinics and physician offices, urgent care centers, surgicenters, freestanding 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 1 area and prevent contact with susceptible patients (cohorting patients). During outbreaks, HCP may be assigned to a cohort of patients to limit further the 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 (eg, cohorting, keeping the patient with an existing roommate). In multipatient 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. HCP 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.

Epidemiologically important pathogens: Infectious agents that have 1 or more of the following characteristics: (1) a propensity for transmission within health care facilities based on published reports and the occurrence of temporal or geographic clusters of ≥2 patients, (eg, VRE, MRSA, MSSA, Clostridium difficile, norovirus, RSV, influenza, rotavirus, Enterobacter species, Serratia species, group A streptococcus). However, for group A streptococcus, most experts consider a single case of health care-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:

(3) associated with serious clinical disease and increased morbidity and mortality (eg, 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 1 of the following: (1) handwashing with plain (nonantimicrobial) soap and water; (2) antiseptic handwash (soap containing antiseptic agents and water; (3) antiseptic handrub (waterless antiseptic product, most often alcohol based, rubbed on all surfaces of hands); or (4) surgical hand antisepsis (antiseptic handwash or antiseptic handrub performed preoperatively by surgical personnel to eliminate transient hand flora and reduce resident hand flora).

HAI: An infection that develops in a patient who is cared for in any setting in which health care is delivered (eg, acute care hospital, chronic care facility, ambulatory clinic, dialysis center, surgicenter, home) and is related to receiving health care (ie, was not incubating or present at the time health care 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.

Health care epidemiologist: A person whose primary training is medical (MD, DO) and/or masters- or doctorate-level epidemiology who has received advanced training in health care epidemiology. Typically, these professionals direct or provide consultation to an infection prevention and control program in a hospital, LTCF, or health care delivery system (also see infection prevention and control professional).

HCP: All paid and unpaid persons who work in a health care setting (also known as health care workers) (eg, any person who has professional or technical training in a health care-related field and provides patient care in a health care setting or any person who provides services that support the delivery of health care 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 (eg, 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.

ICP: A person whose primary training is in either nursing, medical technology, microbiology, or epidemiology and who has acquired specialized training in infection control. Responsibilities may include collection, analysis, and feedback of infection data and trends to health care providers; consultation on infection risk assessment, on prevention and on 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 (eg, 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 health care 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 health care-associated infections are implemented and followed by HCP, making the health care setting safe from infection for patients and HCP. The Joint Commission on Accreditation of Healthcare Organizations (JCAHO) requires the following 5 components of an infection prevention and control program for accreditation: (1) surveillance: monitoring patients and HCP 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 health care organization with the approval of the organization's governing body.

LTCFs: An array of residential and outpatient facilities designed to meet the biopsychosocial 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 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).

MDROs: In general, bacteria (excluding M tuberculosis) that are resistant to 1 or more classes of antimicrobial agents and usually are resistant to all but 1 or 2 commercially available antimicrobial agents (eg, MRSA, VRE, ESBL-producing or intrinsically resistant gram-negative bacilli).

Nosocomial infection: Derived from 2 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 include 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 (eg, wear gloves for handling, contain heavily soiled equipment, properly clean and disinfect or sterilize reusable equipment before use on another patient).

Back to Article Outline

The authors and HICPAC thank Dr. Larry Strausbaugh for his many contributions and valued guidance in the preparation of this guideline.

Back to Article Outline

References 

1. IOM. In:  Harrison PF,  Lederberg J editor. Washington, DC: National Academy Press; 1998;p. 8–74
   • View In Article
2. Shlaes DM, Gerding DN, John JF, Craig WA, Bornstein DL, Duncan RA, et al. Infect Control Hosp Epidemiol. 1997;18:275–291
   • View In Article
   • MEDLINE
3. Larson EL, Early E, Cloonan P, Sugrue S, Parides M. Behav Med. 2000;26:14–22
   • View In Article
   • MEDLINE
   • CrossRef
4. Goldmann DA, Weinstein RA, Wenzel RP, Tablan OC, Duma RJ, Gaynes RP, et al. JAMA. 1996;275:234–240
   • View In Article
   • MEDLINE
5. Murthy R. Chest. 2001;119:S405–S411
   • View In Article
6. Mahgoub S, Ahmed J, Glatt AE. Infect Control Hosp Epidemiol. 2002;23:477–479
   • View In Article
   • MEDLINE
   • CrossRef
7. Fournier PE, Richet H. Clin Infect Dis. 2006;42:692–699
   • View In Article
   • CrossRef
8. Fierobe L, Lucet JC, Decre D, Muller-Serieys C, Deleuze A, Joly-Guillou ML, et al. Infect Control Hosp Epidemiol. 2001;22:35–40
   • View In Article
   • MEDLINE
   • CrossRef
9. Ling ML, Ang A, Wee M, Wang GC. Infect Control Hosp Epidemiol. 2001;22:48–49
   • View In Article
   • MEDLINE
   • CrossRef
10. Landman D, Quale JM, Mayorga D, Adedeji A, Vangala K, Ravishankar J, et al. Arch Intern Med. 2002;162:1515–1520
    • View In Article
    • MEDLINE
    • CrossRef
11. Urban C, Segal-Maurer S, Rahal JJ. Clin Infect Dis. 2003;36:1268–1274
    • View In Article
    • CrossRef
12. Gales AC, Jones RN, Forward KR, Linares J, Sader HS, Verhoef J. Clin Infect Dis. 2001;32(Suppl 2):S104–S113
    • View In Article
    • CrossRef
13. del Toro MD, Rodriguez-Bano J, Herrero M, Rivero A, Garcia-Ordonez MA, Corzo J, et al. Medicine (Baltimore). 2002;81:228–239
    • View In Article
    • MEDLINE
    • CrossRef
14. Hanes SD, Demirkan K, Tolley E, Boucher BA, Croce MA, Wood GC, et al. Clin Infect Dis. 2002;35:228–235
    • View In Article
    • CrossRef
15. Saiman L, Siegel J. Infect Control Hosp Epidemiol. 2003;24:S6–S52
    • View In Article
    • MEDLINE
    • CrossRef
16. Loukil C, Saizou C, Doit C, Bidet P, Mariani-Kurkdjian P, Aujard Y, et al. Infect Control Hosp Epidemiol. 2003;24:707–710
    • View In Article
    • MEDLINE
    • CrossRef
17. Ryan MP, Pembroke JT, Adley CC. J Hosp Infect. 2006;62:278–284
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (127 KB)
    • CrossRef
18. Fry AM, Udeagu CC, Soriano-Gabarro M, Fridkin S, Musinski D, LaClaire L, et al. Infect Control Hosp Epidemiol. 2005;26:239–247
    • View In Article
    • MEDLINE
    • CrossRef
19. Carter RJ, Sorenson G, Heffernan R, Kiehlbauch JA, Kornblum JS, Leggiadro RJ, et al. Infect Control Hosp Epidemiol. 2005;26:248–255
    • View In Article
    • MEDLINE
    • CrossRef
20. Whitener CJ, Park SY, Browne FA, Parent LJ, Julian K, Bozdogan B, et al. Clin Infect Dis. 2004;38:1049–1055
    • View In Article
    • CrossRef
21. CDC . MMWR Morb Mortal Wkly Rep. 1997;46:765–766
    • View In Article
    • MEDLINE
22. CDC . MMWR Morb Mortal Wkly Rep. 2002;51:565–567
    • View In Article
    • MEDLINE
23. CDC . MMWR Morb Mortal Wkly Rep. 2002;51:902
    • View In Article
    • MEDLINE
24. CDC . MMWR Morb Mortal Wkly Rep. 2004;53:322–323
    • View In Article
25. Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, Downes FP, et al. N Engl J Med. 2003;348:1342–1347
    • View In Article
    • CrossRef
26. Fridkin SK, Hageman J, McDougal LK, Mohammed J, Jarvis WR, Perl TM, et al. Clin Infect Dis. 2003;36:429–439
    • View In Article
    • CrossRef
27. Hageman JC, Fridkin SK, Mohammed JM, Steward CD, Gaynes RP, Tenover FC. Infect Control Hosp Epidemiol. 2003;24:356–361
    • View In Article
    • MEDLINE
    • CrossRef
28. Rotun SS, McMath V, Schoonmaker DJ, Maupin PS, Tenover FC, Hill BC, et al. Emerg Infect Dis. 1999;5:147–149
    • View In Article
    • MEDLINE
29. Smith TL, Pearson ML, Wilcox KR, Cruz C, Lancaster MV, Robinson-Dunn B, et al. N Engl J Med. 1999;340:493–501
    • View In Article
    • MEDLINE
    • CrossRef
30. Srinivasan A, Dick JD, Perl TM. Clin Microbiol Rev. 2002;15:430–438
    • View In Article
    • MEDLINE
    • CrossRef
31. Gonzales RD, Schreckenberger PC, Graham MB, Kelkar S, DenBesten K, Quinn JP. Lancet. 2001;357:1179
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (48 KB)
    • CrossRef
32. Soltani M, Beighton D, Philpott-Howard J, Woodford N. Antimicrob Agents Chemother. 2001;45:645–646
    • View In Article
    • MEDLINE
    • CrossRef
33. Pai MP, Rodvold KA, Schreckenberger PC, Gonzales RD, Petrolatti JM, Quinn JP. Clin Infect Dis. 2002;35:1269–1272
    • View In Article
    • CrossRef
34. Pillai SK, Sakoulas G, Wennersten C, Eliopoulos GM, Moellering RC, Ferraro MJ, et al. J Infect Dis. 2002;186:1603–1607
    • View In Article
    • MEDLINE
    • CrossRef
35. Hershberger E, Donabedian S, Konstantinou K, Zervos MJ. Clin Infect Dis. 2004;38:92–98
    • View In Article
    • CrossRef
36. Mangili A, Bica I, Snydman DR, Hamer DH. Clin Infect Dis. 2005;40:1058–1060
    • View In Article
    • CrossRef
37. Sabol K, Patterson JE, Lewis JS, Owens A, Cadena J, Jorgensen JH. Antimicrob Agents Chemother. 2005;49:1664–1665
    • View In Article
    • MEDLINE
    • CrossRef
38. Simor AE, Lee M, Vearncombe M, Jones-Paul L, Barry C, Gomez M, et al. Infect Control Hosp Epidemiol. 2002;23:261–267
    • View In Article
    • MEDLINE
    • CrossRef
39. Clarke NM, Patterson J, Lynch IJ. Curr Opin Crit Care. 2003;9:413–3
    • View In Article
40. Martone WJ. Infect Control Hosp Epidemiol. 1998;19:539–545
    • View In Article
    • MEDLINE
41. The Brooklyn Antibiotic Task Force. Infect Control Hosp Epidemiol. 2002;23:106–108
    • View In Article
    • MEDLINE
    • CrossRef
42. Wilson SJ, Knipe CJ, Zieger MJ, Gabehart KM, Goodman JE, Volk HM, et al. Am J Infect Control. 2004;32:342–344
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (67 KB)
    • CrossRef
43. Qavi A, Segal-Maurer S, Mariano N, Urban C, Rosenberg C, Burns J, et al. Infect Control Hosp Epidemiol. 2005;26:63–68
    • View In Article
    • MEDLINE
    • CrossRef
44. Song X, Srinivasan A, Plaut D, Perl TM. Infect Control Hosp Epidemiol. 2003;24:251–256
    • View In Article
    • MEDLINE
    • CrossRef
45. Aloush V, Navon-Venezia S, Seigman-Igra Y, Cabili S, Carmeli Y. Antimicrob Agents Chemother. 2006;50:43–48
    • View In Article
    • MEDLINE
    • CrossRef
46. Cosgrove SE. Clin Infect Dis. 2006;42(Suppl 2):S82–S89
    • View In Article
    • CrossRef
47. Stone PW, Gupta A, Loughrey M, Della-Latta P, Cimiotti J, Larson E, et al. Infect Control Hosp Epidemiol. 2003;24:601–606
    • View In Article
    • MEDLINE
    • CrossRef
48. Cosgrove SE, Kaye KS, Eliopoulous GM, Carmeli Y. Arch Intern Med. 2002;162:185–190
    • View In Article
    • MEDLINE
    • CrossRef
49. Linden PK, Pasculle AW, Manez R, Kramer DJ, Fung JJ, Pinna AD, et al. Clin Infect Dis. 1996;22:663–670
    • View In Article
    • MEDLINE
    • CrossRef
50. Vergis EN, Hayden MK, Chow JW, Snydman DR, Zervos MJ, Linden PK, et al. Ann Intern Med. 2001;135:484–492
    • View In Article
    • MEDLINE
51. Salgado CD, Farr BM. Infect Control Hosp Epidemiol. 2003;24:690–698
    • View In Article
    • MEDLINE
    • CrossRef
52. DiazGranados CA, Jernigan JA. J Infect Dis. 2005;191:588–595
    • View In Article
    • MEDLINE
    • CrossRef
53. DiazGranados CA, Zimmer SM, Klein M, Jernigan JA. Clin Infect Dis. 2005;41:327–333
    • View In Article
    • CrossRef
54. Carmeli Y, Eliopoulos G, Mozaffari E, Samore M. Arch Intern Med. 2002;162:2223–2228
    • View In Article
    • MEDLINE
    • CrossRef
55. Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR. Clin Infect Dis. 2004;39:776–782
    • View In Article
    • CrossRef
56. Muder RR, Brennen C, Wagener MM, Vickers RM, Rihs JD, Hancock GA, et al. Ann Intern Med. 1991;114:107–112
    • View In Article
    • MEDLINE
57. Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y. Clin Infect Dis. 2003;36:53–59
    • View In Article
    • CrossRef
58. Melzer M, Eykyn SJ, Gransden WR, Chinn S. Clin Infect Dis. 2003;37:1453–1460
    • View In Article
    • CrossRef
59. Selvey LA, Whitby M, Johnson B. Infect Control Hosp Epidemiol. 2000;21:645–648
    • View In Article
    • MEDLINE
    • CrossRef
60. Romero-Vivas J, Rubio M, Fernandez C, Picazo JJ. Clin Infect Dis. 1995;21:1417–1423
    • View In Article
    • MEDLINE
    • CrossRef
61. Blot SI, Vandewoude KH, Hoste EA, Colardyn FA. Arch Intern Med. 2002;162:2229–2235
    • View In Article
    • MEDLINE
    • CrossRef
62. Reed SD, Friedman JY, Engemann JJ, Griffiths RI, Anstrom KJ, Kaye KS, et al. Infect Control Hosp Epidemiol. 2005;26:175–183
    • View In Article
    • MEDLINE
    • CrossRef
63. Mekontso-Dessap A, Kirsch M, Brun-Buisson C, Loisance D. Clin Infect Dis. 2001;32:877–883
    • View In Article
    • MEDLINE
    • CrossRef
64. Engemann JJ, Carmeli Y, Cosgrove SE, Fowler VG, Bronstein MZ, Trivette SL, et al. Clin Infect Dis. 2003;36:592–598
    • View In Article
    • CrossRef
65. Jones RN. Clin Infect Dis. 2006;42(Suppl 1):S13–S24
    • View In Article
    • CrossRef
66. Fowler VG, Sakoulas G, McIntyre LM, Meka VG, Arbeit RD, Cabell CH, et al. J Infect Dis. 2004;190:1140–1149
    • View In Article
    • MEDLINE
    • CrossRef
67. Woods CW, Cheng AC, Fowler VG, Moorefield M, Frederick J, et al. Clin Infect Dis. 2004;38:1188–1191
    • View In Article
    • CrossRef
68. Jernigan JA, Clemence MA, Stott GA, Titus MG, Alexander CH, Palumbo CM, et al. Infect Control Hosp Epidemiol. 1995;16:686–696
    • View In Article
    • MEDLINE
69. Stamm AM, Long MN, Belcher B. Am J Infect Control. 1993;21:70–74
    • View In Article
    • Abstract
    • Full-Text PDF (648 KB)
    • CrossRef
70. Harbarth S, Albrich W, Goldmann DA, Huebner J. Lancet Infect Dis. 2001;1:251–261
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (471 KB)
    • CrossRef
71. Zinn CS, Westh H, Rosdahl VT. Microb Drug Resist. 2004;10:160–168
    • View In Article
    • MEDLINE
    • CrossRef
72. Whitney CG, Farley MM, Hadler J, Harrison LH, Lexau C, Reingold A, et al. N Engl J Med. 2000;343:1917–1924
    • View In Article
    • MEDLINE
    • CrossRef
73. Kollef MH, Fraser VJ. Ann Intern Med. 2001;134:298–314
    • View In Article
    • MEDLINE
74. Fridkin SK. Crit Care Med. 2001;29:N64–N68
    • View In Article
    • MEDLINE
    • CrossRef
75. Diekema DJ, Boots Miller BJ, Vaughn TE, Woolson RF, Yankey JW, Ernst EJ, et al. Clin Infect Dis. 2004;38:78–85
    • View In Article
    • CrossRef
76. Polgreen PM, Beekmann SE, Chen YY, Doern GV, Pfaller MA, Brueggemann AB, et al. Infect Control Hosp Epidemiol. 2006;27:252–256
    • View In Article
    • MEDLINE
    • CrossRef
77. Bradley SF, Terpenning MS, Ramsey MA, Zarins LT, Jorgensen KA, Sottile WS, et al. Ann Intern Med. 1991;115:417–422
    • View In Article
    • MEDLINE
78. Brennen C, Wagener MM, Muder RR. J Am Geriatr Soc. 1998;46:157–160
    • View In Article
    • MEDLINE
79. Strausbaugh LJ, Crossley KB, Nurse BA, Thrupp LD. Infect Control Hosp Epidemiol. 1996;17:129–140
    • View In Article
    • MEDLINE
80. Bradley SF. Infect Control Hosp Epidemiol. 1999;20:362–366
    • View In Article
    • MEDLINE
    • CrossRef
81. Bradley SF. Am J Med. 1999;106:S2–S10discussion S48–S52
    • View In Article
82. Wiener J, Quinn JP, Bradford PA, Goering RV, Nathan C, Bush K, et al. JAMA. 1999;281:517–523
    • View In Article
    • MEDLINE
    • CrossRef
83. McNeil SA, Mody L, Bradley SF. Geriatrics. 2002;57:16–27
    • View In Article
    • MEDLINE
84. Pacio GA, Visintainer P, Maguire G, Wormser GP, Raffalli J, Montecalvo MA. Infect Control Hosp Epidemiol. 2003;24:246–250
    • View In Article
    • MEDLINE
    • CrossRef
85. Rahimi AR. J Am Geriatr Soc. 1998;46:1555–1557
    • View In Article
    • MEDLINE
86. Trick WE, Weinstein RA, DeMarais PL, Tomaska W, Nathan C, McAllister SK, et al. J Am Geriatr Soc. 2004;52:2003–2009
    • View In Article
    • MEDLINE
    • CrossRef
87. Ben-Ami R, Schwaber MJ, Navon-Venezia S, Schwartz D, Giladi M, Chmelnitsky I, et al. Clin Infect Dis. 2006;42:925–934
    • View In Article
    • CrossRef
88. Elizaga ML, Weinstein RA, Hayden MK. Clin Infect Dis. 2002;34:441–446
    • View In Article
    • CrossRef
89. Saiman L, Cronquist A, Wu F, Zhou J, Rubenstein D, Eisner W, et al. Infect Control Hosp Epidemiol. 2003;24:317–321
    • View In Article
    • MEDLINE
    • CrossRef
90. Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R. Clin Infect Dis. 2006;42:389–391
    • View In Article
    • CrossRef
91. Gaynes R, Edwards JR. Clin Infect Dis. 2005;41:848–854
    • View In Article
    • CrossRef
92. Boyce JM, Jackson MM, Pugliese G, Batt MD, Fleming D, Garner JS, et al. Infect Control Hosp Epidemiol. 1994;15:105–115
    • View In Article
    • MEDLINE
93. NNIS . Am J Infect Control. 2003;31:481–498
    • View In Article
    • Full Text
    • Full-Text PDF (218 KB)
    • CrossRef
94. Fridkin SK, Edwards JR, Courval JM, Hill H, Tenover FC, Lawton R, et al. Ann Intern Med. 2001;135:175–183
    • View In Article
    • MEDLINE
95. Jones RN. Chest. 2001;119:S397–S404
    • View In Article
96. Neuhauser MM, Weinstein RA, Rydman R, Danziger LH, Karam G, Quinn JP. JAMA. 2003;289:885–888
    • View In Article
    • MEDLINE
    • CrossRef
97. Fridkin SK, Hill HA, Volkova NV, Edwards JR, Lawton RM, Gaynes RP, et al. Emerg Infect Dis. 2002;8:697–701
    • View In Article
    • MEDLINE
98. Madaras-Kelly KJ, Remington RE, Lewis PG, Stevens DL. Infect Control Hosp Epidemiol. 2006;27:155–169
    • View In Article
    • MEDLINE
    • CrossRef
99. Fridkin SK, Hageman JC, Morrison M, Sanza LT, Como-Sabetti K, Jernigan JA, et al. N Engl J Med. 2005;352:1436–1444
    • View In Article
    • CrossRef
100. Kuehnert MJ, Kruszon-Moran D, Hill HA, McQuillan G, McAllister SK, Fosheim G, et al. J Infect Dis. 2006;193:172–179
     • View In Article
     • MEDLINE
     • CrossRef
101. Bonten MJ, Slaughter S, Ambergen AW, Hayden MK, van Voorhis J, Nathan C, et al. Arch Intern Med. 1998;158:1127–1132
     • View In Article
     • MEDLINE
     • CrossRef
102. Merrer J, Santoli F, Appere de Vecchi C, Tran B, De Jonghe B, Outin H. Infect Control Hosp Epidemiol. 2000;21:718–723
     • View In Article
     • MEDLINE
     • CrossRef
103. Lautenbach E, Patel JB, Bilker WB, Edelstein PH, Fishman NO. Clin Infect Dis. 2001;32:1162–1171
     • View In Article
     • MEDLINE
     • CrossRef
104. Goetz AM, Rihs JD, Wagener MM, Muder RR. Am J Infect Control. 1998;26:558–562
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (36 KB)
     • CrossRef
105. Puzniak LA, Leet T, Mayfield J, Kollef M, Mundy LM. Clin Infect Dis. 2002;35:18–25
     • View In Article
     • CrossRef
106. CDC . MMWR. 2002;51:1–44
     • View In Article
107. Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, et al. Infect Control Hosp Epidemiol. 2003;24:362–386
     • View In Article
     • MEDLINE
     • CrossRef
108. Almuneef MA, Baltimore RS, Farrel PA, Reagan-Cirincione P, Dembry LM. Clin Infect Dis. 2001;32:220–227
     • View In Article
     • MEDLINE
     • CrossRef
109. Duckro AN, Blom DW, Lyle EA, Weinstein RA, Hayden MK. Arch Intern Med. 2005;165:302–307
     • View In Article
     • MEDLINE
     • CrossRef
110. Boyce JM, Potter-Bynoe G, Chenevert C, King T. Infect Control Hosp Epidemiol. 1997;18:622–627
     • View In Article
     • MEDLINE
111. Bhalla A, Pultz NJ, Gries DM, Ray AJ, Eckstein EC, Aron DC, et al. Infect Control Hosp Epidemiol. 2004;25:164–167
     • View In Article
     • MEDLINE
     • CrossRef
112. Larson EL, Cimiotti JP, Haas J, Nesin M, Allen A, Della-Latta P, et al. Pediatr Crit Care Med. 2005;6:457–461
     • View In Article
     • MEDLINE
     • CrossRef
113. Lee YL, Cesario T, Lee R, Nothvogel S, Nassar J, Farsad N, et al. Am J Infect Control. 1994;22:346–351
     • View In Article
     • Abstract
     • Full-Text PDF (648 KB)
     • CrossRef
114. Boyce JM, Opal SM, Chow JW, Zervos MJ, Potter-Bynoe G, Sherman CB, et al. J Clin Microbiol. 1994;32:1148–1153
     • View In Article
     • MEDLINE
115. Gerding DN, Johnson S, Peterson LR, Mulligan ME, Silva J. Infect Control Hosp Epidemiol. 1995;16:459–477
     • View In Article
     • MEDLINE
116. Donskey CJ. Clin Infect Dis. 2004;39:219–226
     • View In Article
     • CrossRef
117. Boyce JM, Havill NL, Maria B. J Clin Microbiol. 2005;43:5992–5995
     • View In Article
     • MEDLINE
     • CrossRef
118. Available at: www.ihi.org/IHI/Programs/Campaign. Accessed November 21, 2006.
     • View In Article
119. Evans R, Lloyd JF, Abouzelof RH, Taylor CW, Anderson VR, Samore MH. Medinfo. 2004;11:212–216
     • View In Article
120. Boyce JM, Opal SM, Potter-Bynoe G, Medeiros AA. Clin Infect Dis. 1993;17:496–504
     • View In Article
     • MEDLINE
     • CrossRef
121. Zawacki A, O'Rourke E, Potter-Bynoe G, Macone A, Harbarth S, Goldmann D. Infect Control Hosp Epidemiol. 2004;25:1083–1089
     • View In Article
     • MEDLINE
     • CrossRef
122. Faibis F, Laporte C, Fiacre A, Delisse C, Lina G, Demachy M-C, et al. Infect Control Hosp Epidemiol. 2005;26:213–215
     • View In Article
     • MEDLINE
     • CrossRef
123. Sheretz RJ, Reagan DR, Hampton KD, Robertson KL, Streed SA, Hoen HM, et al. Ann Intern Med. 1996;124:539–547
     • View In Article
     • MEDLINE
124. Wang JT, Chang SC, Ko WJ, Chang YY, Chen ML, Pan HJ, et al. J Hosp Infect. 2001;47:104–109
     • View In Article
     • Abstract
     • Full-Text PDF (99 KB)
     • CrossRef
125. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, et al. JAMA. 1998;279:593–598
     • View In Article
     • MEDLINE
     • CrossRef
126. CDC . MMWR Morb Mortal Wkly Rep. 1999;48:707–710
     • View In Article
127. Fergie JE, Purcell K. Pediatr Infect Dis J. 2001;20:860–863
     • View In Article
     • MEDLINE
     • CrossRef
128. Sattler CA, Mason EO, Kaplan SL. Pediatr Infect Dis J. 2002;21:910–917
     • View In Article
     • MEDLINE
     • CrossRef
129. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG. Proc Natl Acad Sci U S A. 2002;99:7687–7692
     • View In Article
     • MEDLINE
     • CrossRef
130. Pan ES, Diep BA, Carleton HA, Charlebois ED, Sensabaugh GF, Haller BL, et al. Clin Infect Dis. 2003;37:1384–1388
     • View In Article
     • CrossRef
131. Daum RS, Ito T, Hiramatsu K, Hussain F, Mongkolrattanothai K, Jamklang M, et al. J Infect Dis. 2002;186:1344–1347
     • View In Article
     • MEDLINE
     • CrossRef
132. Said-Salim B, Mathema B, Kreiswirth BN. Infect Control Hosp Epidemiol. 2003;24:451–455
     • View In Article
     • MEDLINE
     • CrossRef
133. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC. J Clin Microbiol. 2003;41:5113–5120
     • View In Article
     • MEDLINE
     • CrossRef
134. Zetola N, Francis JS, Nuermberger EL, Bishai WR. Lancet Infect Dis. 2005;5:275–286
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (285 KB)
     • CrossRef
135. Adem PV, Montgomery CP, Husain AN, Koogler TK, Arangelovich V, Humilier M, et al. N Engl J Med. 2005;353:1245–1251
     • View In Article
     • CrossRef
136. Bocchini CE, Hulten KG, Mason EO, Gonzalez BE, Hammerman WA, Kaplan SL. Pediatrics. 2006;117:433–440
     • View In Article
137. Healy CM, Hulten KG, Palazzi DL, Campbell JR, Baker CJ. Clin Infect Dis. 2004;39:1460–1466
     • View In Article
     • CrossRef
138. Saiman L, O'keefe M, Graham PL, Wu F, Said-Salim B, Kreiswirth B, et al. Clin Infect Dis. 2003;37:1313–1319
     • View In Article
     • CrossRef
139. Eckhardt C, Halvosa JS, Ray SM, Blumberg HM. Infect Control Hosp Epidemiol. 2003;24:460–461
     • View In Article
     • MEDLINE
     • CrossRef
140. Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, King MD, et al. Clin Infect Dis. 2006;42:647–656
     • View In Article
     • CrossRef
141. Berenholtz SM, Pronovost PJ, Lipsett PA, Hobson D, Earsing K, Farley JE, et al. Crit Care Med. 2004;32:2014–2020
     • View In Article
     • MEDLINE
     • CrossRef
142. Coopersmith CM, Rebmann TL, Zack JE, Ward MR, Corcoran RM, Schallom ME, et al. Crit Care Med. 2002;30:59–64
     • View In Article
     • MEDLINE
     • CrossRef
143. Babcock HM, Zack JE, Garrison T, Trovillion E, Jones M, Fraser VJ, et al. Chest. 2004;125:2224–2231
     • View In Article
     • MEDLINE
     • CrossRef
144. Warren DK, Zack JE, Cox MJ, Cohen MM, Fraser VJ. Crit Care Med. 2003;31:1959–1963
     • View In Article
     • MEDLINE
     • CrossRef
145. Eggimann P, Hugonnet S, Sax H, Harbarth S, Chevrolet JC, Pittet D. Ann Intern Med. 2005;142:875–876
     • View In Article
146. Verhoef J, Beaujean D, Blok H, Baars A, Meyler A, van der Werken C, et al. Eur J Clin Microbiol Infect Dis. 1999;18:461–466
     • View In Article
     • MEDLINE
     • CrossRef
147. Salmenlinna S, Lyytikainen O, Kotilainen P, Scotford R, Siren E, Vuopio-Varkila J. Eur J Clin Microbiol Infect Dis. 2000;19:101–107
     • View In Article
     • MEDLINE
     • CrossRef
148. Struelens MJ, Ronveaux O, Jans B, Mertens R. Infect Control Hosp Epidemiol. 1996;17:503–508
     • View In Article
     • MEDLINE
149. Voss A, Milatovic D, Wallrauch-Schwarz C, Rosdahl VT, Braveny I. Eur J Clin Microbiol Infect Dis. 1994;13:50–55
     • View In Article
     • MEDLINE
     • CrossRef
150. Rosdahl VT, Knudsen AM. Infect Control Hosp Epidemiol. 1991;12:83–88
     • View In Article
     • MEDLINE
151. Ostrowsky BE, Trick WE, Sohn AH, Quirk SB, Holt S, Carson LA, et al. N Engl J Med. 2001;344:1427–1433
     • View In Article
     • MEDLINE
     • CrossRef
152. Haley RW, Cushion NB, Tenover FC, Bannerman TL, Dryer D, Ross J, et al. J Infect Dis. 1995;171:614–624
     • View In Article
     • MEDLINE
     • CrossRef
153. Jernigan JA, Titus MG, Groschel DH, Getchell-White S, Farr BM. Am J Epidemiol. 1996;143:496–504
     • View In Article
     • MEDLINE
     • CrossRef
154. Falk PS, Winnike J, Woodmansee C, Desai M, Mayhall CG. Infect Control Hosp Epidemiol. 2000;21:575–582
     • View In Article
     • MEDLINE
     • CrossRef
155. Sherer CR, Sprague BM, Campos JM, Nambiar S, Temple R, Short B, et al. Emerg Infect Dis. 2005;11:1470–1472
     • View In Article
     • MEDLINE
156. Nourse C, Byrne C, Murphy H, Kaufmann ME, Clarke A, Butler K. Epidemiol Infect. 2000;124:53–59
     • View In Article
     • MEDLINE
     • CrossRef
157. Rubin LG, Tucci V, Cercenado E, Eliopoulos G, Isenberg HD. Infect Control Hosp Epidemiol. 1992;13:700–705
     • View In Article
     • MEDLINE
158. Karanfil LV, Murphy M, Josephson A, Gaynes R, Mandel L, Hill BC, et al. Infect Control Hosp Epidemiol. 1992;13:195–200
     • View In Article
     • MEDLINE
159. Hanna H, Umphrey J, Tarrand J, Mendoza M, Raad I. Infect Control Hosp Epidemiol. 2001;22:217–219
     • View In Article
     • MEDLINE
     • CrossRef
160. Dembry LM, Uzokwe K, Zervos MJ. Infect Control Hosp Epidemiol. 1996;17:286–292
     • View In Article
     • MEDLINE
161. Bartley PB, Schooneveldt JM, Looke DF, Morton A, Johnson DW, Nimmo GR. J Hosp Infect. 2001;48:43–54
     • View In Article
     • Abstract
     • Full-Text PDF (154 KB)
     • CrossRef
162. Christiansen KJ, Tibbett PA, Beresford W, Pearman JW, Lee RC, Coombs GW, et al. Infect Control Hosp Epidemiol. 2004;25:384–390
     • View In Article
     • MEDLINE
     • CrossRef
163. Armstrong-Evans M, Litt M, McArthur MA, Willey B, Cann D, Liska S, et al. Infect Control Hosp Epidemiol. 1999;20:312–317
     • View In Article
     • MEDLINE
     • CrossRef
164. Webster J, Faoagali JL, Cartwright D. J Paediatr Child Health. 1994;30:59–64
     • View In Article
     • MEDLINE
     • CrossRef
165. Zafar AB, Butler RC, Reese DJ, Gaydos LA, Mennonna PA. Am J Infect Control. 1995;23:200–208
     • View In Article
     • Abstract
     • Full-Text PDF (874 KB)
     • CrossRef
166. Carrier M, Marchand R, Auger P, Hebert Y, Pellerin M, Perrault LP, et al. J Thorac Cardiovasc Surg. 2002;123:40–44
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (69 KB)
     • CrossRef
167. Kotilainen P, Routamaa M, Peltonen R, Evesti P, Eerola E, Salmenlinna S, et al. Arch Intern Med. 2001;161:859–863
     • View In Article
     • MEDLINE
     • CrossRef
168. Back NA, Linnemann CC, Staneck JL, Kotagal UR. Infect Control Hosp Epidemiol. 1996;17:227–231
     • View In Article
     • MEDLINE
169. Embil JM, McLeod JA, Al-Barrak AM, Thompson GM, Aoki FY, Witwicki EJ, et al. Burns. 2001;27:681–688
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (445 KB)
     • CrossRef
170. Rao N, Jacobs S, Joyce L. Infect Control Hosp Epidemiol. 1988;9:255–260
     • View In Article
     • MEDLINE
171. Kotilainen P, Routamaa M, Peltonen R, Oksi J, Rintala E, Meurman O, et al. Emerg Infect Dis. 2003;9:169–175
     • View In Article
     • MEDLINE
172. Cohen SH, Morita MM, Bradford M. Am J Med. 1991;91:S233–S237
     • View In Article
     • Abstract
     • Full-Text PDF (603 KB)
     • CrossRef
173. Adeyemi-Doro FA, Scheel O, Lyon DJ, Cheng AF. Infect Control Hosp Epidemiol. 1997;18:765–767
     • View In Article
     • MEDLINE
174. van der Zwet WC, Parlevliet GA, Savelkoul PH, Stoof J, Kaiser AM, Koeleman JG, et al. J Hosp Infect. 1999;42:295–302
     • View In Article
     • Abstract
     • Full-Text PDF (116 KB)
     • CrossRef
175. Macrae MB, Shannon KP, Rayner DM, Kaiser AM, Hoffman PN, French GL. J Hosp Infect. 2001;49:183–192
     • View In Article
     • Abstract
     • Full-Text PDF (342 KB)
     • CrossRef
176. Villari P, Crispino M, Salvadori A, Scarcella A. Infect Control Hosp Epidemiol. 2001;22:630–634
     • View In Article
     • MEDLINE
     • CrossRef
177. Paterson DL, Singh N, Rihs JD, Squier C, Rihs BL, Muder RR. Clin Infect Dis. 2001;33:126–128
     • View In Article
     • MEDLINE
     • CrossRef
178. Bukholm G, Tannaes T, Kjelsberg AB, Smith-Erichsen N. Infect Control Hosp Epidemiol. 2002;23:441–446
     • View In Article
     • MEDLINE
     • CrossRef
179. Roberts SA, Findlay R, Lang SD. J Hosp Infect. 2001;48:228–232
     • View In Article
     • Abstract
     • Full-Text PDF (73 KB)
     • CrossRef
180. Hollander R, Ebke M, Barck H, von Pritzbuer E. J Hosp Infect. 2001;48:207–213
     • View In Article
     • Abstract
     • Full-Text PDF (118 KB)
     • CrossRef
181. Podnos YD, Cinat ME, Wilson SE, Cooke J, Gornick W, Thrupp LD. Surgical Infections. 2001;2:297–301
     • View In Article
     • MEDLINE
     • CrossRef
182. Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V, Touveneau S, et al. Lancet. 2000;356:1307–1312
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (105 KB)
     • CrossRef
183. Murray-Leisure KA, Geib S, Graceley D, Rubin-Slutsky AB, Saxena N, Muller HA, et al. Infect Control Hosp Epidemiol. 1990;11:343–350
     • View In Article
     • MEDLINE
184. Jochimsen EM, Fish L, Manning K, Young S, Singer DA, Baker R, et al. Infect Control Hosp Epidemiol. 1999;20:106–109
     • View In Article
     • MEDLINE
     • CrossRef
185. Calfee DP, Farr BM. Infect Control Hosp Epidemiol. 2002;23:407–410
     • View In Article
     • MEDLINE
     • CrossRef
186. Scheckler WE, Brimhall D, Buck AS, Farr BM, Friedman C, Garibaldi RA, et al. Infect Control Hosp Epidemiol. 1998;19:114–124
     • View In Article
     • MEDLINE
187. Boyce JM, Mermel LA, Zervos MJ, Rice LB, Potter-Bynoe G, Giorgio C, et al. Infect Control Hosp Epidemiol. 1995;16:634–637
     • View In Article
     • MEDLINE
188. Nicolle LE, Dyck B, Thompson G, Roman S, Kabani A, Plourde P, et al. Infect Control Hosp Epidemiol. 1999;20:202–205
     • View In Article
     • MEDLINE
     • CrossRef
189. Lucet JC, Decre D, Fichelle A, Joly-Guillou ML, Pernet M, Deblangy C, et al. Clin Infect Dis. 1999;29:1411–1418
     • View In Article
     • MEDLINE
     • CrossRef
190. D'Agata EM, Thayer V, Schaffner W. Infect Control Hosp Epidemiol. 2000;21:588–591
     • View In Article
     • MEDLINE
     • CrossRef
191. Papia G, Louie M, Tralla A, Johnson C, Collins V, Simor AE. Infect Control Hosp Epidemiol. 1999;20:473–477
     • View In Article
     • MEDLINE
     • CrossRef
192. Siddiqui AH, Harris AD, Hebden J, Wilson PD, Morris JG, Roghmann MC. Am J Infect Control. 2002;30:40–43
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (62 KB)
     • CrossRef
193. Byers KE, Anglim AM, Anneski CJ, Germanson TP, Gold HS, Durbin LJ, et al. Infect Control Hosp Epidemiol. 2001;22:140–147
     • View In Article
     • MEDLINE
     • CrossRef
194. Harbarth S, Martin Y, Rohner P, Henry N, Auckenthaler R, Pittet D. J Hosp Infect. 2000;46:43–49
     • View In Article
     • Abstract
     • Full-Text PDF (119 KB)
     • CrossRef
195. Curtis JR, Cook DJ, Wall RJ, Angus DC, Bion J, Kacmarek R, et al. Crit Care Med. 2006;34:211–218
     • View In Article
     • MEDLINE
     • CrossRef
196. Arnow P, Allyn PA, Nichols EM, Hill DL, Pezzlo M, Bartlett RH. J Trauma. 1982;22:954–959
     • View In Article
     • MEDLINE
197. Fridkin SK, Pear SM, Williamson TH, Galgiani JN, Jarvis WR. Infect Control Hosp Epidemiol. 1996;17:150–158
     • View In Article
     • MEDLINE
198. Harbarth S, Sudre P, Dharan S, Cadenas M, Pittet D. Infect Control Hosp Epidemiol. 1999;20:598–603
     • View In Article
     • MEDLINE
     • CrossRef
199. Vicca AF. J Hosp Infect. 1999;43:109–113
     • View In Article
     • Abstract
     • Full-Text PDF (231 KB)
     • CrossRef
200. Robert J, Fridkin SK, Blumberg HM, Anderson B, White N, Ray SM, et al. Infect Control Hosp Epidemiol. 2000;21:12–17
     • View In Article
     • MEDLINE
     • CrossRef
201. Jackson M, Chiarello LA, Gaynes RP, Gerberding JL. Am J Infect Control. 2002;30:199–206
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (102 KB)
     • CrossRef
202. Grundmann H, Hori S, Winter B, Tami A, Austin DJ. J Infect Dis. 2002;185:481–488
     • View In Article
     • MEDLINE
     • CrossRef
203. Dubbert PM, Dolce J, Richter W, Miller M, Chapman SW. Infect Control Hosp Epidemiol. 1990;11:191–193
     • View In Article
     • MEDLINE
204. Nettleman MD, Trilla A, Fredrickson M, Pfaller M. Am J Med. 1991;91:S228–S232
     • View In Article
     • Abstract
     • Full-Text PDF (2125 KB)
     • CrossRef
205. Curran ET, Benneyan JC, Hood J. Infect Control Hosp Epidemiol. 2002;23:13–18
     • View In Article
     • MEDLINE
     • CrossRef
206. Gerber SI, Jones RC, Scott MV, Price JS, Dworkin MS, Filippell MB, et al. Infect Control Hosp Epidemiol. 2006;27:139–145
     • View In Article
     • MEDLINE
     • CrossRef
207. Chicago Antimicrobial Resistance Project (CARP). Available at: http://www.carp-net.org
     • View In Article
208. Rampling A, Wiseman S, Davis L, Hyett AP, Walbridge AN, Payne GC, et al. J Hosp Infect. 2001;49:109–116
     • View In Article
     • Abstract
     • Full-Text PDF (109 KB)
     • CrossRef
209. Rice LB, Eckstein EC, DeVente J, Shlaes DM. Clin Infect Dis. 1996;23:118–124
     • View In Article
     • MEDLINE
     • CrossRef
210. Wright MO, Hebden JN, Harris AD, Shanholtz CB, Standiford HC, Furuno JP, et al. Infect Control Hosp Epidemiol. 2004;25:167–168
     • View In Article
     • MEDLINE
     • CrossRef
211. Smith DL, Dushoff J, Perencevich EN, Harris AD, Levin SA. Proc Natl Acad Sci U S A. 2004;101:3709–3714
     • View In Article
     • MEDLINE
     • CrossRef
212. Rahal JJ, Urban C, Horn D, Freeman K, Segal-Maurer S, Maurer J, et al. JAMA. 1998;280:1233–1237
     • View In Article
     • MEDLINE
     • CrossRef
213. Rahal JJ, Urban C, Segal-Maurer S. Clin Infect Dis. 2002;34:499–503
     • View In Article
     • CrossRef
214. Meyer KS, Urban C, Eagan JA, Berger BJ, Rahal JJ. Ann Intern Med. 1993;119:353–358
     • View In Article
     • MEDLINE
215. Pena C, Pujol M, Ardanuy C, Ricart A, Pallares R, Linares J, et al. Antimicrob Agents Chemother. 1998;42:53–58
     • View In Article
     • MEDLINE
216. Quale JM, Landman D, Bradford PA, Visalli M, Ravishankar J, Flores C, et al. Clin Infect Dis. 2002;35:834–841
     • View In Article
     • CrossRef
217. Rupp ME, Marion N, Fey PD, Bolam DL, Iwen PC, Overfelt CM, et al. Infect Control Hosp Epidemiol. 2001;22:301–303
     • View In Article
     • MEDLINE
     • CrossRef
218. Calil R, Marba ST, von Nowakonski A, Tresoldi AT. Am J Infect Control. 2001;29:133–138
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (87 KB)
     • CrossRef
219. McDonald LC. Infect Control Hosp Epidemiol. 2005;26:672–675
     • View In Article
     • MEDLINE
     • CrossRef
220. Harbarth S, Cosgrove S, Carmeli Y. Antimicrob Agents Chemother. 2002;46:1619–1628
     • View In Article
     • MEDLINE
     • CrossRef
221. Winston LG, Charlebois ED, Pang S, Bangsberg DR, Perdreau-Remington F, Chambers HF. Am J Infect Control. 2004;32:462–469
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (184 KB)
     • CrossRef
222. Brinsley K, Srinivasan A, Sinkowitz-Cochran R, Lawton R, McIntyre R, Kravitz G, et al. Am J Infect Control. 2005;33:53–54
     • View In Article
     • Full Text
     • Full-Text PDF (64 KB)
     • CrossRef
223. Bruno-Murtha LA, Brusch J, Bor D, Li W, Zucker D. Infect Control Hosp Epidemiol. 2005;26:81–87
     • View In Article
     • MEDLINE
     • CrossRef
224. Fridkin SK. Clin Infect Dis. 2003;36:1438–1444
     • View In Article
     • CrossRef
225. John JF. Infect Control Hosp Epidemiol. 2000;21:9–11
     • View In Article
     • MEDLINE
     • CrossRef
226. McGowan JE. Infect Control Hosp Epidemiol. 2000;21:S36–S43
     • View In Article
     • MEDLINE
     • CrossRef
227. Evans RS, Pestotnik SL, Classen DC, Clemmer TP, Weaver LK, Orme JF, et al. N Engl J Med. 1998;338:232–238
     • View In Article
     • MEDLINE
     • CrossRef
228. Huskins WC. Semin Pediatr Infect Dis. 2001;12:138–146
     • View In Article
     • CrossRef
229. Mullett CJ, Evans RS, Christenson JC, Dean JM. Pediatrics. 2001;108:E75
     • View In Article
     • CrossRef
230. Glowacki RC, Schwartz DN, Itokazu GS, Wisniewski MF, Kieszkowski P, Weinstein RA. Clin Infect Dis. 2003;37:59–64
     • View In Article
     • CrossRef
231. Parrino TA. Pharmacotherapy. 2005;25:289–298
     • View In Article
     • MEDLINE
     • CrossRef
232. Paterson DL. Clin Infect Dis. 2006;42(Suppl 2):S90–S95
     • View In Article
     • CrossRef
233. Binkley S, Fishman NO, LaRosa LA, Marr AM, Nachamkin I, Wordell D, et al. Infect Control Hosp Epidemiol. 2006;27:682–687
     • View In Article
     • MEDLINE
     • CrossRef
234. McGowan JE, Tenover FC. Nat Rev Microbiol. 2004;2:251–258
     • View In Article
     • MEDLINE
     • CrossRef
235. Fridkin SK, Edwards JR, Tenover FC, Gaynes RP, McGowan JE. Clin Infect Dis. 2001;33:324–330
     • View In Article
     • MEDLINE
     • CrossRef
236. Foca M, Jakob K, Whittier S, Della Latta P, Factor S, Rubenstein D, et al. N Engl J Med. 2000;343:695–700
     • View In Article
     • MEDLINE
     • CrossRef
237. Huang SS, Rifas-Shiman SL, Warren DK, Fraser VJ, Climo MW, Wong ES, et al. and the Centers for Disease control and Prevention Epicenters Program. Improving methicillin-resistant Staphylococcus aureus surveillance and reporting in intensive care units. J Infect Dis. 2007;195:330–338
     • View In Article
     • MEDLINE
     • CrossRef
238. Gaynes RP, Emori TG. In:  Abrutyn E,  Goldmann DA,  Scheckler WE editor. Saunders infection control reference service. Philadelphia, PA: W.B. Saunders Company; 2001;p. 40–44
     • View In Article
239. Pottinger JM, Herwaldt LA, Perl TM. Infect Control Hosp Epidemiol. 1997;18:513–527
     • View In Article
     • MEDLINE
240. Hartstein AI, LeMonte AM, Iwamoto PK. Infect Control Hosp Epidemiol. 1997;18:42–48
     • View In Article
     • MEDLINE
241. Piagnerelli M, Kennes B, Brogniez Y, Deplano A, Govaerts D. Infect Control Hosp Epidemiol. 2000;21:651–653
     • View In Article
     • MEDLINE
     • CrossRef
242. Montecalvo MA, Jarvis WR, Uman J, Shay DK, Petrullo C, Rodney K, et al. Ann Intern Med. 1999;131:269–272
     • View In Article
     • MEDLINE
243. Talon DR, Bertrand X. Infect Control Hosp Epidemiol. 2001;22:505–509
     • View In Article
     • MEDLINE
     • CrossRef
244. Lucet JC, Grenet K, Armand-Lefevre L, Harnal M, Bouvet E, Regnier B, et al. Infect Control Hosp Epidemiol. 2005;26:121–126
     • View In Article
     • MEDLINE
     • CrossRef
245. Troche G, Joly LM, Guibert M, Zazzo JF. Infect Control Hosp Epidemiol. 2005;26:161–165
     • View In Article
     • MEDLINE
     • CrossRef
246. Nijssen S, Bonten MJ, Weinstein RA. Clin Infect Dis. 2005;40:405–409
     • View In Article
     • CrossRef
247. Cooper BS, Stone SP, Kibbler CC, Cookson BD, Roberts JA, Medley GF, et al. BMJ. 2004;329:533
     • View In Article
     • CrossRef
248. Perencevich EN, Fisman DN, Lipsitch M, Harris AD, Morris JG, Smith DL. Clin Infect Dis. 2004;38:1108–1115
     • View In Article
     • CrossRef
249. Bootsma MC, Diekmann O, Bonten MJ. Proc Natl Acad Sci U S A. 2006;103:5620–5625
     • View In Article
     • MEDLINE
     • CrossRef
250. Gardam MA, Burrows LL, Kus JV, Brunton J, Low DE, Conly JM, et al. J Infect Dis. 2002;186:1754–1760
     • View In Article
     • MEDLINE
     • CrossRef
251. Thouverez M, Talon D, Bertrand X. Infect Control Hosp Epidemiol. 2004;25:838–841
     • View In Article
     • MEDLINE
     • CrossRef
252. Armeanu E, Bonten MJ. Clin Infect Dis. 2005;41:210–216
     • View In Article
     • CrossRef
253. Muto CA, Giannetta ET, Durbin LJ, Simonton BM, Farr BM. Infect Control Hosp Epidemiol. 2002;23:429–435
     • View In Article
     • MEDLINE
     • CrossRef
254. Morris JG, Shay DK, Hebden JN, McCarter RJ, Perdue BE, Jarvis W, et al. Ann Intern Med. 1995;123:250–259
     • View In Article
     • MEDLINE
255. Furuno JP, McGregor JC, Harris AD, Johnson JA, Johnson JK, Langenberg P, et al. Arch Intern Med. 2006;166:580–585
     • View In Article
     • MEDLINE
     • CrossRef
256. Harbarth S, Sax H, Fankhauser-Rodriguez C, Schrenzel J, Agostinho A, Pittet D. Am J Med. 2006;119:e215–e223
     • View In Article
257. Lee TA, Hacek DM, Stroupe KT, Collins SM, Peterson LR. Infect Control Hosp Epidemiol. 2005;26:39–46
     • View In Article
     • MEDLINE
     • CrossRef
258. Manian FA, Senkel D, Zack J, Meyer L. Infect Control Hosp Epidemiol. 2002;23:516–519
     • View In Article
     • MEDLINE
     • CrossRef
259. Troillet N, Carmeli Y, Samore MH, Dakos J, Eichelberger K, DeGirolami PC, et al. Infect Control Hosp Epidemiol. 1998;19:181–185
     • View In Article
     • MEDLINE
260. Sanford MD, Widmer AF, Bale MJ, Jones RN, Wenzel RP. Clin Infect Dis. 1994;19:1123–1128
     • View In Article
     • MEDLINE
     • CrossRef
261. Lucet JC, Chevret S, Durand-Zaleski I, Chastang C, Regnier B. Arch Intern Med. 2003;163:181–188
     • View In Article
     • MEDLINE
     • CrossRef
262. D'Agata EM, Gautam S, Green WK, Tang YW. Clin Infect Dis. 2002;34:167–172
     • View In Article
     • CrossRef
263. Flayhart D, Hindler JF, Bruckner DA, Hall G, Shrestha RK, Vogel SA, et al. J Clin Microbiol. 2005;43:5536–5540
     • View In Article
     • MEDLINE
     • CrossRef
264. Perry JD, Davies A, Butterworth LA, Hopley AL, Nicholson A, Gould FK. J Clin Microbiol. 2004;42:4519–4523
     • View In Article
     • MEDLINE
     • CrossRef
265. Harbarth S, Masuet-Aumatell C, Schrenzel J, Francois P, Akakpo C, Renzi G, et al. Crit Care. 2006;10:R25
     • View In Article
     • CrossRef
266. Huletsky A, Lebel P, Picard FJ, Bernier M, Gagnon M, Boucher N, et al. Clin Infect Dis. 2005;40:976–981
     • View In Article
     • CrossRef
267. Warren DK, Liao RS, Merz LR, Eveland M, Dunne WM. J Clin Microbiol. 2004;42:5578–5581
     • View In Article
     • MEDLINE
     • CrossRef
268. Palladino S, Kay ID, Flexman JP, Boehm I, Costa AM, Lambert EJ, et al. J Clin Microbiol. 2003;41:2483–2486
     • View In Article
     • MEDLINE
     • CrossRef
269. Fazal BA, Telzak EE, Blum S, Turett GS, Petersen-Fitzpatrick FE, Lorian V. Infect Control Hosp Epidemiol. 1996;17:372–374
     • View In Article
     • MEDLINE
270. Toltzis P, Hoyen C, et al. Pediatrics. 1999;103:719–723
     • View In Article
     • MEDLINE
     • CrossRef
271. Weinstein RA, Kabins SA. Am J Med. 1981;70:449–454
     • View In Article
     • MEDLINE
272. Kim PW, Roghmann MC, Perencevich EN, Harris AD. Am J Infect Control. 2003;31:97–103
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (105 KB)
     • CrossRef
273. Slaughter S, Hayden MK, Nathan C, Hu TC, Rice T, Van Voorhis J, et al. Ann Intern Med. 1996;125:448–456
     • View In Article
     • MEDLINE
274. CDC . MMWR Recomm Rep. 1995;44(RR-12):1–13
     • View In Article
     • MEDLINE
275. Evans MR, Meldrum R, Lane W, Gardner D, Ribeiro CD, Gallimore CI, et al. Epidemiol Infect. 2002;129:355–360
     • View In Article
     • MEDLINE
276. Hall CB, Douglas RG, Schnabel KC, Geiman JM. Infect Immun. 1981;33:779–783
     • View In Article
     • MEDLINE
277. Wu HM, Fornek M, Kellogg JS, Chapin AR, Gibson K, Schwab E, et al. Infect Control Hosp Epidemiol. 2005;26:802–810
     • View In Article
     • MEDLINE
     • CrossRef
278. Austin DJ, Bonten MJ, Weinstein RA, Slaughter S, Anderson RM. Proc Natl Acad Sci U S A. 1999;96:6908–6913
     • View In Article
     • MEDLINE
     • CrossRef
279. Law MR, Gill ON, Turner A. Epidemiol Infect. 1988;101:301–309
     • View In Article
     • MEDLINE
     • CrossRef
280. Ruchel R, Mergeryan H, Boger O, Langefeld C, Witte W. Infect Control Hosp Epidemiol. 1999;20:353–355
     • View In Article
     • MEDLINE
     • CrossRef
281. Cepeda JA, Whitehouse T, Cooper B, Hails J, Jones K, Kwaku F, et al. Lancet. 2005;365:295–304
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (161 KB)
     • CrossRef
282. Mulin B, Rouget C, Clement C, Bailly P, Julliot MC, Viel JF, et al. Infect Control Hosp Epidemiol. 1997;18:499–503
     • View In Article
     • MEDLINE
283. Nouwen JL, Ott A, Kluytmans-Vandenbergh MF, Boelens HA, Hofman A, van Belkum A, et al. Clin Infect Dis. 2004;39:806–811
     • View In Article
     • CrossRef
284. Byers KE, Anglim AM, Anneski CJ, Farr BM. Infect Control Hosp Epidemiol. 2002;23:207–211
     • View In Article
     • MEDLINE
     • CrossRef
285. Baden LR, Thiemke W, Skolnik A, Chambers R, Strymish J, Gold HS, et al. Clin Infect Dis. 2001;33:1654–1660
     • View In Article
     • MEDLINE
     • CrossRef
286. Donskey CJ, Hoyen CK, Das SM, Helfand MS, Hecker MT. Infect Control Hosp Epidemiol. 2002;23:436–440
     • View In Article
     • MEDLINE
     • CrossRef
287. Ridenour GA, Wong ES, Call MA, Climo MW. Infect Control Hosp Epidemiol. 2006;27:271–278
     • View In Article
     • MEDLINE
     • CrossRef
288. Scanvic A, Denic L, Gaillon S, Giry P, Andremont A, Lucet JC. Clin Infect Dis. 2001;32:1393–1398
     • View In Article
     • MEDLINE
     • CrossRef
289. Kauffman CA, Terpenning MS, He X, Zarins LT, Ramsey MA, Jorgensen KA, et al. Am J Med. 1993;94:371–378
     • View In Article
     • Abstract
     • Full-Text PDF (1057 KB)
     • CrossRef
290. Strausbaugh LJ, Jacobson C, Sewell DL, Potter S, Ward TT. Infect Control Hosp Epidemiol. 1992;13:151–159
     • View In Article
     • MEDLINE
291. Kirkland KB, Weinstein JM. Lancet. 1999;354:1177–1178
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (45 KB)
     • CrossRef
292. Saint S, Higgins LA, Nallamothu BK, Chenoweth C. Am J Infect Control. 2003;31:354–356
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (164 KB)
     • CrossRef
293. Evans HL, Shaffer MM, Hughes MG, Smith RL, Chong TW, Raymond DP, et al. Surgery. 2003;134:180–188
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (652 KB)
     • CrossRef
294. Catalano G, Houston SH, Catalano MC, Butera AS, Jennings SM, Hakala SM, et al. South Med J. 2003;96:141–145
     • View In Article
     • MEDLINE
     • CrossRef
295. Tarzi S, Kennedy P, Stone S, Evans M. J Hosp Infect. 2001;49:250–254
     • View In Article
     • Abstract
     • Full-Text PDF (98 KB)
     • CrossRef
296. Stelfox HT, Bates DW, Redelmeier DA. JAMA. 2003;290:1899–1905
     • View In Article
     • CrossRef
297. Hota B. Clin Infect Dis. 2004;39:1182–1189
     • View In Article
     • CrossRef
298. Martinez JA, Ruthazer R, Hansjosten K, Barefoot L, Snydman DR. Arch Intern Med. 2003;163:1905–1912
     • View In Article
     • MEDLINE
     • CrossRef
299. CDC . MMWR. 2003;52(RR10):1–42
     • View In Article
300. Simor AE. Infect Control Hosp Epidemiol. 2001;22:459–463
     • View In Article
     • MEDLINE
     • CrossRef
301. Hayden MK, Bonten MJ, Blom DW, Lyle EA, van de Vijver DA, Weinstein RA. Clin Infect Dis. 2006;42:1552–1560
     • View In Article
     • CrossRef
302. Lai KK, Kelley AL, Melvin ZS, Belliveau PP, Fontecchio SA. Infect Control Hosp Epidemiol. 1998;19:647–652
     • View In Article
     • MEDLINE
303. Boyce JM. J Hosp Infect. 2001;48(Suppl A):S9–S14
     • View In Article
     • Abstract
     • Full-Text PDF (644 KB)
     • CrossRef
304. Montesinos I, Salido E, Delgado T, Lecuona M, Sierra A. Infect Control Hosp Epidemiol. 2003;24:667–672
     • View In Article
     • MEDLINE
     • CrossRef
305. Chen SF. Pediatr Infect Dis J. 2005;24:79–80
     • View In Article
     • MEDLINE
     • CrossRef
306. Kaplan SL. Pediatr Infect Dis J. 2005;24:457–458
     • View In Article
     • MEDLINE
     • CrossRef
307. Loeb M, Main C, Walker-Dilks C, Eady A. Cochrane Database Syst Rev. 2003;CD003340
     • View In Article
308. Deshpande LM, Fix AM, Pfaller MA, Jones RN. Diagn Microbiol Infect Dis. 2002;42:283–290
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (192 KB)
     • CrossRef
309. Mody L, Kauffman CA, McNeil SA, Galecki AT, Bradley SF. Clin Infect Dis. 2003;37:1467–1474
     • View In Article
     • CrossRef
310. Walker ES, Vasquez JE, Dula R, Bullock H, Sarubbi FA. Infect Control Hosp Epidemiol. 2003;24:342–346
     • View In Article
     • MEDLINE
     • CrossRef
311. Harris AD, Bradham DD, Baumgarten M, Zuckerman IH, Fink JC, Perencevich EN. Clin Infect Dis. 2004;38:1586–1591
     • View In Article
     • CrossRef
312. Eveillard M, Eb F, Tramier B, Schmit JL, Lescure FX, Biendo M, et al. J Hosp Infect. 2001;47:116–124
     • View In Article
     • Abstract
     • Full-Text PDF (105 KB)
     • CrossRef
313. Campbell JR, Zaccaria E, Mason EO, Baker CJ. Infect Control Hosp Epidemiol. 1998;19:924–928
     • View In Article
     • MEDLINE
314. Harris AD, Nemoy L, Johnson JA, Martin-Carnahan A, Smith DL, Standiford H, et al. Infect Control Hosp Epidemiol. 2004;25:105–108
     • View In Article
     • MEDLINE
     • CrossRef
315. Warren DK, Nitin A, Hill C, Fraser VJ, Kollef MH. Infect Control Hosp Epidemiol. 2004;25:99–104
     • View In Article
     • MEDLINE
     • CrossRef
316. Trick WE, Weinstein RA, DeMarais PL, Kuehnert MJ, Tomaska W, Nathan C, et al. J Am Geriatr Soc. 2001;49:270–276
     • View In Article
     • MEDLINE
     • CrossRef
317. Safdar N, Maki DG. Ann Intern Med. 2002;136:834–844
     • View In Article
318. Montecalvo MA, Jarvis WR, Uman J, Shay DK, Petrullo C, Horowitz HW, et al. Infect Control Hosp Epidemiol. 2001;22:437–442
     • View In Article
     • MEDLINE
     • CrossRef
319. Rubinovitch B, Pittet D. J Hosp Infect. 2001;47:9–18
     • View In Article
     • Abstract
     • Full-Text PDF (99 KB)
     • CrossRef
320. Puzniak LA, Gillespie KN, Leet T, Kollef M, Mundy LM. Infect Control Hosp Epidemiol. 2004;25:418–424
     • View In Article
     • MEDLINE
     • CrossRef
321. Cookson B. BMJ. 1997;314:664–665
     • View In Article
     • MEDLINE
     • CrossRef
322. Farr BM, Jarvis WR. Infect Control Hosp Epidemiol. 2002;23:65–68
     • View In Article
     • MEDLINE
     • CrossRef
323. Strausbaugh LJ, Siegel JD, Weinstein RA. Clin Infect Dis. 2006;42:828–835
     • View In Article
     • CrossRef
324. Brooks S, Khan A, Stoica D, Griffith J, Friedeman L, Mukherji R, et al. Infect Control Hosp Epidemiol. 1998;19:333–336
     • View In Article
     • MEDLINE
325. Benneyan JC, Lloyd RC, Plsek PE. Qual Saf Health Care. 2003;12:458–464
     • View In Article
     • MEDLINE
     • CrossRef
326. Gustafson TL. Am J Infect Control. 2000;28:406–414
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (115 KB)
     • CrossRef
327. Aubry-Damon H, Legrand P, Brun-Buisson C, Astier A, Soussy CJ, Leclercq R. Clin Infect Dis. 1997;25:647–653
     • View In Article
     • MEDLINE
328. Cooper BS, Medley GF, Stone SP, Kibbler CC, Cookson BD, Roberts JA, et al. Proc Natl Acad Sci U S A. 2004;101:10223–10228
     • View In Article
     • MEDLINE
     • CrossRef
329. Brown AR, Amyes SG, Paton R, Plant WD, Stevenson GM, Winney RJ, et al. J Hosp Infect. 1998;40:115–124
     • View In Article
     • Abstract
     • Full-Text PDF (2135 KB)
     • CrossRef
330. Cromer AL, Hutsell SO, Latham SC, Bryant KG, Wacker BB, Smith SA, et al. Am J Infect Control. 2004;32:451–455
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (263 KB)
     • CrossRef
331. Pittsburgh Regional Project. Available at: http://www.cdc.gov/drugresistence.htm
     • View In Article
332. Assadian O, Berger A, Aspock C, Mustafa S, Kohlhauser C, Hirschl AM. Infect Control Hosp Epidemiol. 2002;23:457–461
     • View In Article
     • MEDLINE
     • CrossRef
333. Byers KE, Durbin LJ, Simonton BM, Anglim AM, Adal KA, Farr BM. Infect Control Hosp Epidemiol. 1998;19:261–264
     • View In Article
     • MEDLINE
334. Patterson JE, Hardin TC, Kelly CA, Garcia RC, Jorgensen JH. Infect Control Hosp Epidemiol. 2000;21:455–458
     • View In Article
     • MEDLINE
     • CrossRef
335. Bantar C, Sartori B, Vesco E, Heft C, Saul M, Salamone F, et al. Clin Infect Dis. 2003;37:180–186
     • View In Article
     • CrossRef
336. Bisson G, Fishman NO, Patel JB, Edelstein PH, Lautenbach E. Infect Control Hosp Epidemiol. 2002;23:254–260
     • View In Article
     • MEDLINE
     • CrossRef
337. Carling P, Fung T, Killion A, Terrin N, Barza M. Infect Control Hosp Epidemiol. 2003;24:699–706
     • View In Article
     • MEDLINE
     • CrossRef
338. Quale J, Landman D, Saurina G, Atwood E, DiTore V, Patel K. Clin Infect Dis. 1996;23:1020–1025
     • View In Article
     • MEDLINE
     • CrossRef
339. Sample ML, Gravel D, Oxley C, Toye B, Garber G, Ramotar K. Infect Control Hosp Epidemiol. 2002;23:468–470
     • View In Article
     • MEDLINE
     • CrossRef
340. Burke JP, Pestotnik SL. J Chemother. 1999;11:530–535
     • View In Article
     • MEDLINE
341. Cooper E, Paull A, O'Reilly M. Infect Control Hosp Epidemiol. 2002;23:151–153
     • View In Article
     • MEDLINE
     • CrossRef
342. Lagerlov P, Loeb M, Andrew M, Hjortdahl P. Qual Health Care. 2000;9:159–165
     • View In Article
     • MEDLINE
     • CrossRef
343. Lemmen SW, Zolldann D, Gastmeier P, Lutticken R. Am J Infect Control. 2001;29:89–93
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (77 KB)
     • CrossRef
344. Liu SC, Leu HS, Yen MY, Lee PI, Chou MC. Am J Infect Control. 2002;30:381–385
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (142 KB)
     • CrossRef
345. Monnet DL. Infect Control Hosp Epidemiol. 1998;19:552–559
     • View In Article
     • MEDLINE
346. Pestotnik SL, Classen DC, Evans RS, Burke JP. Ann Intern Med. 1996;124:884–890
     • View In Article
     • MEDLINE
347. NCCLS . Reference method for broth dilution antifungal susceptibility testing of conidium-forming filamentous fungi: proposed standards. NCCLS document M38-A. Wayne (PA): National Committee for Clinical Laboratory Standards; 2002;
     • View In Article
348. Kupronis BA, Richards CL, Whitney CG. J Am Geriatr Soc. 2003;51:1520–1525
     • View In Article
     • MEDLINE
     • CrossRef
349. Viray M, Linkin D, Maslow JN, Stieritz DD, Carson LS, Bilker WB, et al. Infect Control Hosp Epidemiol. 2005;26:56–62
     • View In Article
     • MEDLINE
     • CrossRef
350. Chaitram JM, Jevitt LA, Lary S, Tenover FC. J Clin Microbiol. 2003;41:2372–2377
     • View In Article
     • MEDLINE
     • CrossRef
351. Ernst EJ, Diekema DJ, BootsMiller BJ, Vaughn T, Yankey JW, Flach SD, et al. Diagn Microbiol Infect Dis. 2004;49:141–145
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (159 KB)
     • CrossRef
352. Ginocchio CC. Am J Health Syst Pharm. 2002;59:S7–S11
     • View In Article
     • MEDLINE
353. Stevenson KB, Samore M, Barbera J, Moore JW, Hannah E, Houck P, et al. Diagn Microbiol Infect Dis. 2003;47:303–311
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (95 KB)
     • CrossRef
354. Gupta A, Della-Latta P, Todd B, San Gabriel P, Haas J, Wu F, et al. Infect Control Hosp Epidemiol. 2004;25:210–215
     • View In Article
     • MEDLINE
     • CrossRef
355. Rodriguez-Bano J, Navarro MD, Romero L, Muniain MA, Perea EJ, et al. Clin Infect Dis. 2006;42:37–45
     • View In Article
     • CrossRef
356. Bhavnani SM, Hammel JP, Forrest A, Jones RN, Ambrose PG. Clin Infect Dis. 2003;37:344–350
     • View In Article
     • CrossRef
357. Halstead DC, Gomez N, McCarter YS. J Clin Microbiol. 2004;42:1–6
     • View In Article
     • MEDLINE
     • CrossRef
358. Fridkin SK, Steward CD, Edwards JR, Pryor ER, McGowan JE, Archibald LK, et al. Clin Infect Dis. 1999;29:245–252
     • View In Article
     • MEDLINE
359. Lang A, De Fina G, Meyer R, Aschbacher R, Rizza F, Mayr O, et al. Eur J Clin Microbiol Infect Dis. 2001;20:657–660
     • View In Article
     • MEDLINE
360. White RL, Friedrich LV, Mihm LB, Bosso JA. Clin Infect Dis. 2000;31:16–23
     • View In Article
     • MEDLINE
     • CrossRef
361. Zoutman DE, Ford BD. Am J Infect Control. 2005;33:1–5
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (99 KB)
     • CrossRef
362. cms.
     • View In Article
363. Peterson LR, Hamilton JD, Baron EJ, Tompkins LS, Miller JM, Wilfert CM, et al. Clin Infect Dis. 2001;32:605–611
     • View In Article
     • MEDLINE
     • CrossRef
364. Calfee DP, Giannetta ET, Durbin LJ, Germanson TP, Farr BM. Clin Infect Dis. 2003;37:326–332
     • View In Article
     • CrossRef
365. Thompson RL, Cabezudo I, Wenzel RP. Ann Intern Med. 1982;97:309–317
     • View In Article
     • MEDLINE
366. Lacey S, Flaxman D, Scales J, Wilson A. J Hosp Infect. 2001;48:308–311
     • View In Article
     • Abstract
     • Full-Text PDF (67 KB)
     • CrossRef
367. Greenaway CA, Miller MA. Infect Control Hosp Epidemiol. 1999;20:341–343
     • View In Article
     • MEDLINE
     • CrossRef
368. Spindel SJ, Strausbaugh LJ, Jacobson C. Infect Control Hosp Epidemiol. 1995;16:217–223
     • View In Article
     • MEDLINE
369. Bula CJ, Ghilardi G, Wietlisbach V, Petignat C, Francioli P. J Am Geriatr Soc. 2004;52:700–706
     • View In Article
     • MEDLINE
     • CrossRef
370. High KP, Bradley S, Loeb M, Palmer R, Quagliarello V, Yoshikawa T. Clin Infect Dis. 2005;40:114–122
     • View In Article
     • CrossRef
371. Silverblatt FJ, Tibert C, Mikolich D, Blazek-D'Arezzo J, Alves J, Tack M, et al. J Am Geriatr Soc. 2000;48:1211–1215
     • View In Article
     • MEDLINE
372. CDC . MMWR. 2001;50(RR-05):1–43
     • View In Article
373. Samore MH, Venkataraman L, DeGirolami PC, Arbeit RD, Karchmer AW. Am J Med. 1996;100:32–40
     • View In Article
     • Abstract
     • Full-Text PDF (3671 KB)
     • CrossRef
374. Brooks SE, Veal RO, Kramer M, Dore L, Schupf N, Adachi M. Infect Control Hosp Epidemiol. 1992;13:98–103
     • View In Article
     • MEDLINE
375. Jernigan JA, Siegman-Igra Y, Guerrant RC, Farr BM. Infect Control Hosp Epidemiol. 1998;19:494–499
     • View In Article
     • MEDLINE
376. Chang VT, Nelson K. Clin Infect Dis. 2000;31:717–722
     • View In Article
     • MEDLINE
     • CrossRef
377. Nicolle LE. Clin Infect Dis. 2000;31:752–756
     • View In Article
     • MEDLINE
     • CrossRef
378. Bonten MJ, Slaughter S, Hayden MK, Nathan C, van Voorhis J, Weinstein RA. Crit Care Med. 1998;26:2001–2004
     • View In Article
     • MEDLINE
     • CrossRef
379. Loeb MB, Craven S, McGeer AJ, Simor AE, Bradley SF, et al. Am J Epidemiol. 2003;157:40–47
     • View In Article
     • MEDLINE
     • CrossRef
380. McDonald LC, Banerjee SN, Jarvis WR. Infect Control Hosp Epidemiol. 1998;19:772–777
     • View In Article
     • MEDLINE
381. Montecalvo MA, de Lencastre H, Carraher M, Gedris C, Chung M, VanHorn K, et al. Infect Control Hosp Epidemiol. 1995;16:680–685
     • View In Article
     • MEDLINE
382. Shannon KP, French GL. J Antimicrob Chemother. 2002;50:965–969
     • View In Article
     • MEDLINE
     • CrossRef
383. Singh K, Gavin PJ, Vescio T, Thomson RB, Deddish RB, Fisher A, et al. J Clin Microbiol. 2003;41:2755–2757
     • View In Article
     • MEDLINE
     • CrossRef
384. Grmek-Kosnik I, Ihan A, Dermota U, Rems M, Kosnik M, Jorn Kolmos H. J Hosp Infect. 2005;61:155–161
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (172 KB)
     • CrossRef
385. Villegas MV, Hartstein AI. Infect Control Hosp Epidemiol. 2003;24:284–295
     • View In Article
     • MEDLINE
     • CrossRef
386. Ramsey AH, Skonieczny P, Coolidge DT, Kurzynski TA, Proctor ME, Davis JP. Infect Control Hosp Epidemiol. 2001;22:423–426
     • View In Article
     • MEDLINE
     • CrossRef
387. Harbarth S, Liassine N, Dharan S, Herrault P, Auckenthaler R, Pittet D. Clin Infect Dis. 2000;31:1380–1385
     • View In Article
     • MEDLINE
     • CrossRef
388. Lucet JC, Chevret S, Decre D, Vanjak D, Macrez A, Bedos JP, et al. Clin Infect Dis. 1996;22:430–436
     • View In Article
     • MEDLINE
     • CrossRef
389. Malik RK, Montecalvo MA, Reale MR, Li K, Maw M, Munoz JL, et al. Pediatr Infect Dis J. 1999;18:352–356
     • View In Article
     • MEDLINE
     • CrossRef
390. Stosor V, Kruszynski J, Suriano T, Noskin GA, Peterson LR. Infect Control Hosp Epidemiol. 1999;20:653–659
     • View In Article
     • MEDLINE
     • CrossRef
391. Srinivasan A, Song X, Ross T, Merz W, Brower R, Perl TM. Infect Control Hosp Epidemiol. 2002;23:424–428
     • View In Article
     • MEDLINE
     • CrossRef
392. Rumbak MJ, Cancio MR. Crit Care Med. 1995;23:1200–1203
     • View In Article
     • MEDLINE
     • CrossRef
393. Quale J, Landman D, Atwood E, Kreiswirth B, Willey BM, Ditore V, et al. Am J Infect Control. 1996;24:372–379
     • View In Article
     • Abstract
     • Full-Text PDF (885 KB)
     • CrossRef
394. Livornese LL, Dias S, Samel C, Romanowski B, Taylor S, May P, et al. Ann Intern Med. 1992;117:112–116
     • View In Article
     • MEDLINE
395. Gastmeier P, Schwab F, Geffers C, Ruden H. Infect Control Hosp Epidemiol. 2004;25:109–113
     • View In Article
     • MEDLINE
     • CrossRef
396. Ridwan B, Mascini E, van Der Reijden N, Verhoef J, Bonten M. BMJ. 2002;324:666–668
     • View In Article
     • CrossRef
397. Hitomi S, Kubota M, Mori N, Baba S, Yano H, Okuzumi K, et al. J Hosp Infect. 2000;46:123–129
     • View In Article
     • Abstract
     • Full-Text PDF (134 KB)
     • CrossRef
398. Weber DJ, Rutala WA. Infect Control Hosp Epidemiol. 1997;18:306–309
     • View In Article
     • MEDLINE
399. Schelenz S, French G. J Hosp Infect. 2000;46:23–30
     • View In Article
     • Abstract
     • Full-Text PDF (734 KB)
     • CrossRef
400. Kirschke DL, Jones TF, Craig AS, Chu PS, Mayernick GG, Patel JA, et al. N Engl J Med. 2003;348:214–220
     • View In Article
     • CrossRef
401. Srinivasan A, Wolfenden LL, Song X, Mackie K, Hartsell TL, Jones HD, et al. N Engl J Med. 2003;348:221–227
     • View In Article
     • CrossRef
402. Mangram A, Jarvis WR. Infect Control Hosp Epidemiol. 1996;17:718–720
     • View In Article
     • MEDLINE
403. Vriens MR, Fluit AC, Troelstra A, Verhoef J, van der Werken C. Infect Control Hosp Epidemiol. 2002;23:491–494
     • View In Article
     • MEDLINE
     • CrossRef
404. Cederna JE, Terpenning MS, Ensberg M, Bradley SF, Kauffman CA. Infect Control Hosp Epidemiol. 1990;11:13–16
     • View In Article
     • MEDLINE
405. Hachem R, Raad I. Infect Control Hosp Epidemiol. 2002;23:43–44
     • View In Article
     • MEDLINE
     • CrossRef
406. Lui SL, Luk WK, Cheung CY, Chan TM, Lai KN, Peiris JS. Transplantation. 2001;71:59–64
     • View In Article
     • MEDLINE
     • CrossRef
407. Zafar AB, Sylvester LK, Beidas SO. Am J Infect Control. 2002;30:425–429
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (80 KB)
     • CrossRef
408. Darouiche R, Wright C, Hamill R, Koza M, Lewis D, Markowski J. Antimicrob Agents Chemother. 1991;35:1612–1615
     • View In Article
     • MEDLINE
409. Goetz MB, Mulligan ME, Kwok R, O'Brien H, Caballes C, Garcia JP. Am J Med. 1992;92:607–614
     • View In Article
     • Abstract
     • Full-Text PDF (2241 KB)
     • CrossRef
410. Pan A, Carnevale G, Catenazzi P, Colombini P, Crema L, Dolcetti L, et al. Infect Control Hosp Epidemiol. 2005;26:127–133
     • View In Article
     • MEDLINE
     • CrossRef
411. Silvestri L, Milanese M, Oblach L, Fontana F, Gregori D, Guerra R, et al. Am J Infect Control. 2002;30:391–399
     • View In Article
     • Abstract
     • Full Text
     • Full-Text PDF (147 KB)
     • CrossRef
412. Weber JM, Sheridan RL, Schulz JT, Tompkins RG, Ryan CM. Infect Control Hosp Epidemiol. 2002;23:549–551
     • View In Article
     • MEDLINE
     • CrossRef