Essential practices

• Antimicrobial stewardship has been reclassified from an unresolved issue to an essential practice.

• Although contact precautions remain an essential practice, considerations have been provided for hospitals that have strong horizontal prevention measures and neither ongoing MRSA outbreaks nor high or increasing rates of MRSA infection or hospital-onset MRSA-positive cultures and that choose to modify the use of contact precautions for some or all MRSA-colonized or MRSA-infected patients.

Additional approaches

• Active surveillance testing (AST) remains an additional practice, but specific recommendations, supporting data, and quality-of-evidence ratings for the use of AST in several specific patient populations have been added.

• Decolonization therapy for patients with MRSA colonization remains an additional practice, but specific recommendations, supporting data, and quality-of-evidence ratings for the use of universal or targeted decolonization in several specific patient populations have been added.

Burden of MRSA infection

1. 1. HAIs caused by MRSA are common in acute-care facilities.

   1. a. Worldwide, an estimated 15% of ICU infections are caused by Staphylococcus aureus, and nearly one-third of those (31%) are due to MRSA. ^{Reference Vincent, Sakr and Singer3} In North America, an estimated 23% of ICU infections are caused by S. aureus, and nearly half of those (44%) are due to MRSA.

   2. b. In the United States, S. aureus remains one of the most common pathogens associated with HAI.

      1. i. Among the device-associated infections and surgical site infections (SSIs) reported to the CDC National Healthcare Safety Network (NHSN) between 2015 and 2017, S. aureus was the first and second most common pathogen reported in pediatric and adult infections, respectively. ^{Reference Weiner-Lastinger, Abner and Benin4,Reference Weiner-Lastinger, Abner and Edwards5}

      2. ii. During this period, 48.4% of device-associated infections and 41.9% of SSIs caused by S. aureus were due to MRSA. Among device-associated S. aureus infections, rates of methicillin resistance ranged from 36.9% among possible ventilator-associated pneumonia (PVAP) to 51.7% among central-line–associated bloodstream infections (CLABSIs). ^{Reference Weiner-Lastinger, Abner and Edwards5} Compared to data from 2009–2010, the proportions caused by MRSA are lower for each of these HAIs. ^{Reference Sievert, Ricks and Edwards6}

      3. iii. A national study examining S. aureus bloodstream infections in the United States reported that the rate of hospital-onset MRSA bloodstream infections decreased 17% per year between 2012 and 2017. ^{Reference Kourtis, Hatfield and Baggs7}

      4. iv. Although these findings suggest some success in preventing healthcare-associated MRSA transmission and infection, many patients and patient groups continue to be at risk. In fact, hospital-onset MRSA bloodstream infections increased 15% in US hospitals between 2019 and 2020 in association with the onset of the COVID-19 pandemic. ⁸ This finding provides an important reminder of the importance of implementation of and adherence to preventive measures.

2. 2. Outcomes associated with MRSA HAIs

   1. a. MRSA infections are associated with significant morbidity and mortality.

   2. b. An estimated 80,461 invasive MRSA infections occurred in the United States in 2011, with an all-cause in-hospital mortality rate of 14%. ^{Reference Dantes, Mu and Belflower9}

   3. c. Another US study reported an unadjusted in-hospital mortality rate of 29% for hospital-onset MRSA bloodstream infections occurring between 2012 and 2017. ^{Reference Kourtis, Hatfield and Baggs7}

   4. d. A recent study using 2010–2014 data from the National Inpatient Sample from the Agency for Healthcare Research and Quality compared costs of hospitalization between MSSA and MRSA infections and noted that costs associated with MSSA infection approach those for MRSA infection. However, a higher adjusted mortality rate for MRSA-related hospitalizations was observed. ^{Reference Klein, Jiang and Mojica10}

Risk factors for MRSA

1. 1. MRSA HAI among colonized patients

   1. a. A substantial proportion of colonized patients will subsequently develop a MRSA infection such as pneumonia, soft-tissue infection, or primary bloodstream infection. ^{Reference Huang and Platt11–Reference Milstone, Goldner, Ross, Shepard, Carroll and Perl16} Among adults, this proportion has ranged from 9% to 33%. ^{Reference Huang, Singh and McKinnell17}

      1. i. Risk of infection among those colonized is not limited to the period of concomitant hospitalization but persists beyond discharge. One study of persons in whom MRSA colonization had been identified during a previous hospital stay reported that the risk of developing a MRSA infection within 18 months of detection of MRSA colonization was 29%. ^{Reference Huang and Platt11} Others have reported that among those who develop MRSA infections after discharge, these account for a substantial number of readmissions. ^{Reference Huang, Hinrichsen and Datta12} A more recent study, in which individuals identified during hospitalization to be MRSA carriers were followed, found that 9% developed MRSA infection within 1 year and that 85% of those who developed MRSA infection required hospitalization. ^{Reference Huang, Singh and McKinnell17}

   2. b. Among pediatric patients, 8.5% of children found to be colonized on admission subsequently developed a MRSA infection. Also, among patients who acquired MRSA colonization while being cared for in the pediatric intensive care unit, 47% subsequently developed MRSA infection. ^{Reference Milstone, Goldner, Ross, Shepard, Carroll and Perl16}

2. 2. Risk factors for MRSA colonization and HAI

   1. a. Risk factors for MRSA colonization include severe underlying illness or comorbid conditions, prolonged hospital stay, exposure to broad-spectrum antimicrobials, the presence of invasive devices such as central venous catheters, and frequent contact with the healthcare system or healthcare personnel (HCP).

   2. b. Colonization pressure (the ratio of MRSA-carrier days to total patient days) has been identified as an independent risk factor for hospital-associated acquisition of MRSA. ^{Reference Merrer, Santoli, Appéré de Vecchi, Tran, De Jonghe and Outin18}

   3. c. Community-associated MRSA (CA-MRSA) strains are a significant problem among persons without traditional healthcare-related risk factors ^{Reference Merrer, Santoli, Appéré de Vecchi, Tran, De Jonghe and Outin18–Reference Popovich, Weinstein and Hota20} ; however, transmission of CA-MRSA can and does occur in hospitals. ^{Reference Klevens, Morrison and Nadle19–Reference Milstone, Carroll, Ross, Shangraw and Perl24}

      1. i. In recent studies, an increasing proportion of hospital-onset invasive MRSA infections have been caused by community strains. ^{Reference Rhee, Aroutcheva, Hota, Weinstein and Popovich25}

      2. ii. Genomic studies suggest that there is an intermixing of community and hospital transmission networks for MRSA, underscoring that community factors should be an important consideration in determining MRSA risk. ^{Reference Popovich, Snitkin and Hota26}

      3. iii. Estimates from the CDC Emerging Infections Program from 2011 to 2016 demonstrated the significant intersection of the opioid epidemic and invasive MRSA infections. Injection drug users were 16.3 times more likely to have an invasive MRSA infection than others. ^{Reference Jackson, Bohm and Brooks27}

      4. iv. MRSA colonization and infection is occurring more frequently in those without classic risk factors. Therefore, community exposures (eg, injection drug use, correctional-facility exposure, crowding, and unstable housing) need to be considered as risk factors. ^{Reference Jackson, Bohm and Brooks27–Reference See, Wesson and Gualandi30}

3. 3. Reservoir for MRSA transmission in acute-care facilities

   1. a. In healthcare facilities, antimicrobial use provides a selective advantage for MRSA to survive.

   2. b. The reservoir for MRSA in hospitals includes colonized or infected patients and HCP as well as contaminated objects within the patient care environment. Transmission is complex but occurs largely through patient-to-patient spread.

      1. i. MRSA-colonized and MRSA-infected patients readily contaminate their environment, and HCP coming into contact with the patient or their environment readily contaminate their hands, clothing, and equipment. ^{Reference Bhalla, Pultz and Gries31–Reference Nadimpalli, O’Hara and Pineles43}

      2. ii. The risk for acquisition of MRSA is higher among hospital patients admitted to a room in which the previous occupant was colonized or infected with MRSA than among patients admitted into a room in which the previous patient was not colonized or infected with MRSA. ^{Reference Huang, Datta and Platt41,Reference Blanco, O’Hara and Harris44}

Surveillance definitions for MRSA

1. 1. Laboratory-identified event surveillance (ie, surveillance based on identification of MRSA laboratory results) and clinical infection surveillance are the 2 commonly used approaches for MRSA surveillance. These 2 surveillance strategies are not mutually exclusive and are often used in conjunction with one another.

   1. a. Regardless of the type of MRSA surveillance selected for use, consistent application of the chosen surveillance definitions is necessary to generate reliable and accurate data that will allow detection of changes in the epidemiology of MRSA within the facility over time.

   2. b. The CDC NHSN definitions for laboratory-based surveillance and infection surveillance are frequently used for MRSA surveillance. ⁴⁵ Because surveillance definitions are subject to change and refinement, users should always refer to source documents (eg, NHSN protocols) to determine currently recommended definitions.

2. 2. Laboratory-identified event surveillance: The NSHN laboratory-identified event reporting definitions provide proxy measures of MRSA healthcare acquisition, exposure burden (colonization pressure or prevalence), and infection burden based solely on laboratory data and basic admission data (eg, date of admission, inpatient location). ⁴⁵

   1. a. These definitions allow classification of clinical MRSA cultures as either healthcare-facility onset or community onset.

   2. b. Similar definitions have also been published by SHEA and the Healthcare Infection Control Practices Advisory Committee. ^{Reference Cohen, Calfee and Fridkin46}

3. 3. Clinical infection surveillance: Clinical infection surveillance can also be used to classify MRSA isolates as healthcare or community onset and to identify patients with specific types of healthcare-associated MRSA infection (eg, CLABSI or SSI). ⁴⁵

   1. a. Unlike laboratory event–based definitions, which classify cultures based solely on the time of specimen collection relative to time of hospital admission, clinical infection surveillance definitions also include an evaluation of the patient’s clinical history and prior healthcare exposures.

Surveillance methods for MRSA and detection of patients with MRSA

1. 1. The reservoir for transmission of MRSA is largely composed of 2 groups of patients: those with clinical MRSA infection and a much larger group who are asymptomatic MRSA carriers. Various detection methods can be used to identify one or both groups.

   1. a. Routine review of data from clinical specimens: Clinically infected patients and some asymptomatically colonized patients can be detected when MRSA is isolated from a clinical specimen obtained for clinical decision-making purposes.

   2. b. Review of active surveillance testing (AST) data: AST for MRSA is defined as diagnostic testing performed to identify persons who are asymptomatic carriers of MRSA. AST is discussed in more detail in Section 4 and the Appendix.

Summary of existing guidelines and recommendations

1. 1. Several governmental, public health, and professional organizations have published evidence-based guidelines and/or policies for the prevention and control of MRSA. ^{Reference Coia, Wilson and Bak47,Reference Milstone, Elward and Brady48} These guidelines provide similar recommendations, differing primarily on the emphasis placed on the use of AST to identify patients asymptomatically colonized with MRSA and in recommendations for routine decolonization of MRSA carriers.

2. 2. IHI ⁴⁹ and APIC ⁵⁰ have developed practical suggestions for implementation and monitoring of several of the prevention measures specified in evidence-based guidelines.

Infrastructure requirements

1. 1. Infrastructure requirements of a MRSA prevention program include the following:

   1. a. An infection prevention and control program that (1) is staffed by sufficient trained HCP to implement and sustain MRSA surveillance and prevention efforts without compromising other infection prevention and control activities and (2) has the authority to implement preventive measures.

   2. b. Information technology systems that (1) can allow rapid notification of clinical staff and infection prevention and control HCP of new MRSA isolates, (2) can collect data needed for MRSA surveillance and outcome measure calculations, and (3) can identify MRSA-colonized patients upon readmission.

   3. c. Sufficient supplies for hand hygiene, contact precautions (eg, gowns and gloves), environmental cleaning and disinfection, and other infection prevention interventions implemented as part of the facility’s MRSA control program.

   4. d. An antimicrobial stewardship program is an important part of many quality and safety metrics, including MRSA prevention. The reader is referred to Barlam et al ^{Reference Barlam, Cosgrove and Abbo51} for a more detailed description of antimicrobial stewardship program infrastructure.

   5. e. Resources to provide appropriate education and training to direct care and other HCP, patients, and visitors.

   6. f. Adequate laboratory support: sufficient staffing and resources for routine clinical testing and for additional testing (ie, active surveillance) when necessary, and timely provision of relevant data to clinicians and the infection prevention program.

   7. g. Leadership accountability and support in prioritizing resources needed to maintain a MRSA prevention program and implement effective interventions.

Essential practices for preventing MRSA recommended for all acute-care hospitals

1. 1. Implement a MRSA monitoring program. (Quality of evidence: LOW)

   1. a. The MRSA monitoring program should do the following:

      1. i. Identify any patient with a current or prior history of MRSA to ensure application of infection prevention strategies for these patients according to hospital policy (eg, contact precautions).

      2. ii. Provide a mechanism for tracking hospital-onset cases of MRSA for purposes of assessing transmission and infection and the need for response.

2. 2. Conduct a MRSA risk assessment. (Quality of evidence: LOW)

   1. a. The risk assessment should be attentive to 2 important factors: the opportunity for MRSA transmission and estimates of the facility-specific MRSA burden and rates of transmission and infection.

      1. i. The opportunity for transmission is affected by the proportion of patients who are MRSA carriers (colonization prevalence) who serve as a reservoir for transmission. Estimates of facility-specific MRSA transmission and infection rates reflect the ability of the facility’s current activities to contain MRSA, regardless of the burden of MRSA that is imported into the facility.

      2. ii. Both colonization prevalence from sites performing active surveillance and rates of transmission and infection (eg, MRSA bloodstream infections, all MRSA-positive cultures) can be measured at either the total hospital level or for specific hospital units.

   2. b. Findings from the risk assessment should be incorporated into the overall infection control program risk assessment and used to develop or refine mitigation strategies, surveillance, and goals based on the program’s prioritized risks.

   3. c. Data used for initial and ongoing risk assessment can provide a baseline and can be used to monitor trends to inform the need for additional interventions. Metrics that might be used in the MRSA risk assessment are discussed in greater detail in Section 5 of this document.

3. 3. Promote compliance with CDC or World Health Organization (WHO) hand hygiene recommendations. (Quality of evidence: MODERATE)

   1. a. Hand hygiene is a fundamental strategy for the prevention of pathogen transmission in healthcare facilities. ^{Reference Huang, Singh and McKinnell17,Reference Derde, Cooper and Goossens52}

   2. b. A common mode of transmission of MRSA to patients is by contact with contaminated hands of HCP, and some investigators have attributed reduced rates of MRSA among hospital inpatients in part to efforts made to improve hand hygiene practices of HCP. ^{Reference Johnson, Martin and Burrell53,Reference Gopal Rao, Jeanes, Osman, Aylott and Green54}

   3. c. Promote patient hand hygiene.

4. 4. Use contact precautions for MRSA-colonized and MRSA-infected patients. (Quality of evidence: MODERATE). A facility that chooses or has already chosen to modify the use of contact precautions for some or all of these patients should conduct a MRSA-specific risk assessment to evaluate the facility for transmission risks and to assess the effectiveness of other MRSA risk mitigation strategies (eg, hand hygiene, cleaning and disinfection of the environment, single occupancy patient rooms) and should establish a process for ongoing monitoring, oversight, and risk assessment.

   1. a. Evidence for the use of contact precautions for MRSA-colonized and MRSA-infected patients

      1. i. Studies have demonstrated that HCP interacting with MRSA-colonized or MRSA-infected patients often become contaminated with the organism. ^{Reference O’Hara, Calfee and Miller42,Reference Nadimpalli, O’Hara and Pineles43,Reference Morgan, Rogawski and Thom55,Reference Gopal Rao, Jeanes, Osman, Aylott and Green56}

      2. ii. Similarly, studies in acute-care hospitals have demonstrated that surfaces and objects in the patient’s environment frequently and quickly become contaminated. ^{Reference Chang, Sethi, Stiefel, Cadnum and Donskey57–Reference Wolfensberger, Mang and Gibson60} Placing patients with MRSA colonization or infection under contact precautions may help reduce patient-to-patient spread of MRSA within the hospital. ^{Reference Siegel, Rhinehart and Jackson61–Reference Jain, Kralovic and Evans64}

      3. iii. Several recent nonrandomized studies and reports support the use of contact precautions for MRSA-colonized and MRSA-infected patients. ^{Reference Harris, Morgan, Pineles, Perencevich and Barnes56,Reference Jain, Kralovic and Evans64} From 2005 to 2016, the incidence of hospital-onset MRSA bloodstream infections in the United States declined 74%. ^{Reference Kourtis, Hatfield and Baggs7} The reasons for this decline probably are multifactorial, but interventions to reduce MRSA transmission likely played a role. In 2007, the US Department of Veterans’ Affairs (VA) implemented a MRSA prevention bundle at VA acute-care hospitals nationwide. Introduction of this bundle, which included universal nasal surveillance for MRSA, contact precautions for MRSA carriers, hand hygiene, and increased institutional awareness of infection control, was associated with significant reductions in healthcare-associated MRSA infections and MRSA transmission in ICU and non-ICU settings. ^{Reference Jain, Kralovic and Evans64} By 2017, hospital-onset MRSA infections at VA hospitals had declined 66% compared to baseline, while hospital-onset MSSA infections declined by only 19%. ^{Reference Jones, Jernigan, Evans, Roselle, Hatfield and Samore65} Decreases in MRSA infections at VA hospitals during this time were significantly higher among patients with negative MRSA admission screening tests compared to those with positive MRSA admission screening tests, suggesting that interventions to decrease transmission within hospitals played a large role in reducing MRSA infections. A mathematical modeling study published in 2021 of the VA MRSA prevention intervention estimated that contact precautions alone reduced MRSA transmission by 47%. ^{Reference Khader, Thomas and Stevens66} A large cluster-randomized trial conducted in ICUs outside the VA system demonstrated significant reductions in MRSA transmission with the implementation of universal glove and gown use. ^{Reference Harris, Pineles and Belton63} In this trial, mathematical models estimated that universal glove and gown use was estimated to have reduced transmission by 44%. ^{Reference Harris, Morgan, Pineles, Perencevich and Barnes56}

      4. iv. Based on a 2020 review of the current evidence, the CDC continues to recommend the use of contact precautions for MRSA colonized or infected patients ⁶⁷

      5. v. During the COVID-19 pandemic, hospital-onset MRSA bloodstream infections increased nationally; however, whether declining use of contact precautions for MRSA-colonized or MRSA-infected patients played a significant role in this increase remains unknown. ^{Reference Weiner-Lastinger, Pattabiraman and Konnor68}

      6. vi. Studies have suggested that patients may be persistent MRSA carriers for prolonged periods (median duration in one study, 8.5 months). ^{Reference Sanford, Widmer, Bale, Jones and Wenzel69,Reference Scanvic, Denic, Gaillon, Giry, Andremont and Lucet70} Use of contact precautions for patients with a history of MRSA is recommended. ⁶⁷ However, the appropriate duration of contact precautions necessary for patients with MRSA remains an unresolved issue. Further considerations for discontinuing contact precautions for patients with MRSA can be found in the SHEA Expert Guidance by Banach et al. ^{Reference Banach, Bearman and Barnden71}

   2. b. Numerous studies have attempted to address whether contact precautions lead to an increase in adverse events. ^{Reference Schrank, Snyder, Davis, Branch-Elliman and Wright72–Reference Abad, Fearday and Safdar74} Some observational studies have shown an increase in adverse events including increased depression, anxiety, falls, electrolyte disorders, and decreased patient satisfaction. ^{Reference Abad, Fearday and Safdar74,Reference Stelfox, Bates and Redelmeier75} However, most of these studies did not control for comorbidity of patients and severity of illness of patients; thus, they suffer from confounding by indication. The only randomized trial to assess whether contact precautions lead to more adverse events showed a significantly lower frequency of HCP visits per hour (4.28 vs 5.24; P = .02) in ICUs using gowns and gloves for contact with all patients compared with control ICUs using gowns and gloves only for patients known to be colonized or infected with antimicrobial-resistant organisms and as otherwise required for CDC-defined contact precautions. ^{Reference Harris, Pineles and Belton63} The incidence of adverse events, though, was not significantly different between the 2 groups. In fact, rates of preventable, nonpreventable, severe, and nonsevere ICU adverse events were all nonsignificantly lower in the intervention group. Rates of hand hygiene on room exit were significantly higher in the universal glove-and-gown group. With randomized trials being a higher level of evidence than observational studies, current evidence does not indicate that contact precautions lead to an increase in adverse events.

   3. c. Evidence on the impact of discontinuation of contact precautions for MRSA-colonized and MRSA-infected patients:

      1. i. In recent years, several studies have sought to characterize the impact of discontinuing contact precautions for MRSA-colonized and MRSA-infected patients. Many of these studies have demonstrated that discontinuing contact precautions did not lead to an increase in HAIs. ^{Reference Marra, Edmond, Schweizer, Ryan and Diekema76–Reference Haessler, Martin and Scales78} However, most were single-center, quasi-experimental studies that were underpowered and did not assess the effect of discontinuing contact precautions on MRSA acquisition or postdischarge MRSA infections. Thus, they were not designed to adequately detect the full impact of discontinuing contact precautions. Only 2 discontinuation studies used MRSA acquisition as an outcome. ^{Reference McKinnell, Eells and Clark79,Reference Renaudin, Llorens and Goetz80} We acknowledge that, due to the large cost of performing cluster-randomized trials, no trial at present has evaluated contact precautions versus no contact precautions for MRSA. The closest study was the BUGG trial, which demonstrated significant reductions in MRSA acquisitions in ICUs that adopted universal gown-and-glove use. ^{Reference Harris, Morgan, Pineles, Perencevich and Barnes56}

   4. d. Considerations for facilities that choose to modify the use of contact precautions for some or all MRSA-colonized or MRSA-infected patients:

      1. i. Hospitals should conduct a MRSA risk assessment based on internal infection rates, local epidemiology, hospital infrastructure (eg, proportion of non-private patient room) that may contribute to patient-to-patient transmission of MRSA if contact precautions are not used, and other factors. Please refer to Essential Practices recommendations 2. and 4.f.2 regarding use of a MRSA risk assessment and Section 5 for a list of metrics that can be used in the risk assessment.

         1. 1. When making the decision to discontinue contact precautions for all or a subset of patients with MRSA, a facility should establish a policy and process that supports and communicates this change.

         2. 2. At a minimum, a facility should provide guidance related to inclusion and exclusion criteria related to the process change; laboratory testing and surveillance strategies; implementation and communication; ongoing risk assessment; and oversight (eg, infection prevention committee) as appropriate.

      2. ii. Hospitals with ongoing MRSA outbreaks or with high or increasing rates of MRSA infection or hospital-onset MRSA-positive cultures* should not discontinue contact precautions for MRSA-colonized or MRSA-infected patients. *If active surveillance testing is used hospital-wide or in select situations, data regarding rates of acquisition of MRSA colonization may also be used in decisions to modify the use of contact precautions.

      3. iii. Based on the risk assessment, hospitals may choose to prioritize certain high-risk populations for which to continue contact precautions. High-risk populations identified may include the following:

         1. 1. ICU patients

         2. 2. NICU patients

         3. 3. Burn-unit patients

         4. 4. Dialysis patients

         5. 5. Transplant and other specialty units with immunocompromised patients

         6. 6. Patients with indwelling devices such as central venous catheters

         7. 7. Patients with active infections, particularly those with uncontained wounds or secretions

         8. 8. Residents of long-term acute-care hospitals

         9. 9. Residents of long-term care facilities

      4. iv. Hospitals that choose to modify the use of contact precautions for some or all MRSA-colonized or MRSA-infected patients should, at a minimum, have strong horizontal prevention practices in place and demonstrate high adherence to these mitigation strategies. These practices may include audits, rounding, and teams to address the following:

         1. 1. Hand hygiene

         2. 2. Standard precautions

         3. 3. Environmental cleaning and disinfection

         4. 4. PPE adherence and discontinuation of extended use and reuse of gowns and gloves

         5. 5. CLABSI prevention

         6. 6. SSI prevention

   5. e. Hospitals that choose to modify the use of contact precautions for some or all MRSA-colonized or MRSA-infected patients should consider implementing a MRSA decolonization program for certain high-risk groups or high-risk settings (eg, ICUs). (See decolonization recommendations in the Additional Approaches section.)

   6. f. Hospitals that choose to modify the use of contact precautions for some or all MRSA-colonized or MRSA-infected patients should monitor key metrics (see 4.f.2) and reconsider the use of contact precautions if an outbreak occurs or if MRSA rates increase.

      1. i. Establish appropriate metrics that capture changes in rates of MRSA infection or transmission. Incorporate these metrics in the ongoing risk assessment and make adjustments to the use of contact precautions or other infection prevention strategies when appropriate. Note: These metrics may be underpowered and limited in their ability able to identify all downstream effects of changes to the use of contact precautions.

      2. ii. Possible key metrics to monitor include the following:

         1. 1. MRSA clinical culture positivity rates

         2. 2. Hand hygiene compliance

         3. 3. Compliance with hospital designated decolonization protocols including chlorhexidine bathing and intranasal treatment (eg, mupirocin)

         4. 4. Hospital-onset MRSA infections, including device-associated infections, procedure-associated infections such as SSIs, bloodstream infections, and other infection types such as pneumonia or skin and soft tissue as appropriate based on historical data

         5. 5. MRSA acquisition rates if active surveillance testing is in place (see active surveillance testing recommendations in Section 5, Additional Approaches for Preventing MRSA Infection)

         6. 6. Rates of admission with new MRSA infection or colonization (among persons without prior history of MRSA colonization or infection) within 30–90 days of prior hospital discharge

            1. a. This metric is intended to identify patients who may have acquired MRSA during a recent hospital admission. Studies have demonstrated that prior hospitalization is a common risk factor for non–hemodialysis-related healthcare-associated community-onset MRSA infection, with the majority occurring within 12 weeks of a prior hospital admission. ^{Reference Dantes, Mu and Belflower9}

5. 5. Ensure cleaning and disinfection of equipment and the environment. (Quality of evidence: MODERATE)

   1. a. MRSA contaminates the patient environment (eg, overbed tables, bedrails, furniture, sinks, floors) and patient care equipment (eg, stethoscopes, blood pressure cuffs, etc). ^{Reference Hardy, Oppenheim, Gossain, Gao and Hawkey81} MRSA contamination on surfaces around the patient zone varies in bioburden concentration.

   2. b. Exposure to this contaminated environment has been associated with acquisition of MRSA. ^{Reference Huang, Datta and Platt41} Improvements in environmental cleaning have been associated with reductions in MRSA acquisition among patients admitted to rooms in which the previous occupant was colonized or infected with MRSA. ^{Reference Datta, Platt, Yokoe and Huang82}

   3. c. Cleaning and disinfection are horizontal infection practices that can prevent transmission of multiple pathogens.

   4. d. Objective monitoring of the thoroughness of cleaning and disinfection using direct observation, fluorescent marking systems, and/or ATP detection systems with feedback of monitoring results to personnel responsible for cleaning has been associated with improvements in environmental cleaning and disinfection in healthcare settings.

6. 6. Implement a laboratory-based alert system that notifies HCP of new MRSA-colonized or MRSA-infected patients in a timely manner. (Quality of evidence: LOW)

   1. a. Timely notification of new MRSA-positive test results to clinical caregivers and infection preventionists facilitates rapid implementation of contact precautions and other interventions (eg, treatment of infection) as appropriate according to facility policy, assessment of risk, and timely surveillance for HAIs.

7. 7. Implement an alert system that identifies readmitted or transferred MRSA-colonized or MRSA-infected patients. (Quality of evidence: LOW)

   1. a. An alert system allows information regarding the MRSA status of the patient to be available at the first point of contact (eg, emergency department arrival, presentation to admitting department), prior to bed assignment, to promptly initiate appropriate control measures and minimize opportunities for transmission.

   2. b. Alerts facilitate early prevention interventions within the continuity of care, such as internal transfers between inpatient units or interfacility transfers managed via regional patient transfer centers.

   3. c. Communication at the time of procedure scheduling and verbal hand-off safety practices (eg, SBAR—situation, background, assessment, recommendation) allows for planning and continuity of prevention activities at the time of patient transport and in the receiving service department (ie, imaging, cardiac catheterization, etc).

8. 8. Provide MRSA data and outcome measures to key stakeholders, including senior leadership, physicians, nursing staff, and others. (Quality of evidence: LOW)

   1. a. Provision of MRSA data and other information related to the activities of the MRSA prevention program to key stakeholders on a regular and frequent basis may optimize focus on MRSA prevention efforts, substantiate requests for resources, and increase engagement in the MRSA prevention program. (See Section 5 for suggested metrics for assessment of the MRSA prevention program.)

9. 9. Educate healthcare personnel (HCP) about MRSA. (Quality of evidence: LOW)

   1. a. Several key components of an effective MRSA prevention program involve modification of HCP behavior (eg, hand hygiene, contact precautions, environmental cleaning, and disinfection).

   2. b. HCP should be educated about their role in MRSA prevention and other MRSA-related topics as appropriate.

10. 10. Educate patients and families about MRSA. (Quality of evidence: LOW)

    1. a. Patients and their families should be educated regarding the importance of hand hygiene and respiratory etiquette to reduce the risk of spread of MRSA and other pathogens during the hospital stay.

    2. b. Patients who are colonized or infected with MRSA and their families should be educated about MRSA and what they can do to reduce the risk of infection and transmission.

11. 11. Implement an antimicrobial stewardship program. (Quality of evidence: LOW)

    1. a. Receipt of antibiotics without MRSA activity has been associated with significant increases in the intranasal burden of MRSA. ^{Reference Kanwar, Cadnum, Jencson and Donskey83} Thus, receipt of such antibiotics may increase the risk of infection in the colonized person and/or increase risk of transmission to others.

    2. b. However, the association between antimicrobial stewardship interventions and rates of MRSA infection and colonization has varied among studies. Of 3 recent systematic reviews and/or meta-analyses, 2 found an association between implementation of antimicrobial stewardship interventions and a decreased incidence of MRSA infection and/or colonization. ^{Reference Karanika, Paudel, Grigoras, Kalbasi and Mylonakis84–Reference Davey, Marwick and Scott86}

    3. c. The quality of evidence for antimicrobial stewardship as a component of a MRSA prevention program is low (eg, mostly single-center, nonrandomized, uncontrolled studies). However, a theoretical rationale and some evidence of benefit do exist, and no evidence of harm has been reported. In addition, benefits of antimicrobial stewardship have been established for other important outcomes (eg, C. difficile prevention).

    4. d. Please refer to the “Compendium of Strategies to Prevent Surgical Site Infections in Acute Care Hospitals: 2022 Update” ^{Reference Calderwood, Anderson and Bratzler87} and current guidelines for surgical antibiotic prophylaxis ^{Reference Bratzler, Dellinger and Olsen88} for recommendations regarding surgical antibiotic prophylaxis among patients known to be colonized with MRSA.

Active surveillance testing (AST)

Active surveillance testing is based on the premise that clinical cultures identify only a small proportion of hospital patients who are colonized with MRSA and that these asymptomatic carriers serve as a substantial reservoir for person-to-person transmission of MRSA in the acute-care hospital. Studies have reported that clinical cultures alone may underestimate the overall hospital prevalence of MRSA by as much as 85% and the monthly average prevalence of MRSA in ICUs by 18.6%–63.5%. ^{Reference Milstone, Carroll, Ross, Shangraw and Perl24,Reference Salgado and Farr89,Reference Huang, Rifas-Shiman and Warren90} AST is used to identify these asymptomatic MRSA carriers so that additional infection control measures (eg, contact precautions, decolonization) can be put into place to decrease the risk of transmission to other patients and HCP and/or to decrease the risk of infection to carriers themselves (decolonization). AST is also used as part of antibiotic stewardship to reduce vancomycin usage, ^{Reference Parente, Cunha, Mylonakis and Timbrook91,Reference Mergenhagen, Starr, Wattengel, Lesse, Sumon and Sellick92} to clear contact precautions, ^{Reference Ghosh, Jiao, Al-Mutawa, O’Neill and Mertz93,Reference Shenoy, Lee and Hou94} and as part of implementing postdischarge interventions. ^{Reference Huang, Singh and McKinnell17,Reference Nelson, Evans and Simbartl95,Reference Gupta, Martinello, Young, Strymish, Cho and Lawler96}

1. 1. Implement a MRSA active surveillance testing (AST) program for select patient populations as part of a multifaceted strategy to control and prevent MRSA. (Quality of evidence: MODERATE). ^{Reference Patel, Olmsted and Hung97} Recommendations for specific populations may have different evidence ratings.

2. 2. Active surveillance for MRSA in conjunction with decolonization can be performed in targeted populations prior to surgery to prevent postsurgical MRSA infection. (Quality of evidence: MODERATE)

   1. a. A large meta-analysis demonstrated a reduction in MRSA surgical site infection (SSI) when active surveillance was coupled with targeted nasal decolonization of MRSA carriers prior to undergoing surgery with hardware. ^{Reference Schweizer, Perencevich and McDanel98} Several other studies, including large clinical trials, have demonstrated a similar reduction in both SSI and nosocomial disease when employing S. aureus active surveillance and targeted decolonization of carriers. (See MRSA Decolonization, recommendation 2, in the Additional Approaches section.)

   2. b. Please refer to the “Compendium of Strategies to Prevent Surgical Site Infections in Acute Care Hospitals: 2022 Update” ^{Reference Calderwood, Anderson and Bratzler87} for recommendations regarding active surveillance and decolonization for organisms other than MRSA (eg, all S. aureus).

3. 3. Active surveillance with contact precautions is inferior to universal decolonization for reduction of MRSA clinical isolates in adult ICUs. (Quality of evidence: HIGH)

   1. a. A 43-hospital cluster-randomized trial in ICUs (REDUCE MRSA Trial) ^{Reference Huang, Septimus and Kleinman99} directly compared (1) active surveillance for MRSA coupled with contact precautions, (2) active surveillance for MRSA coupled with contact precautions and targeted decolonization, and (3) stopping active surveillance, continuing contact precautions for known MRSA carriers, and performing universal decolonization for all ICU patients. Universal decolonization with chlorhexidine bathing and nasal mupirocin was superior to the other arms, resulting in a 37% reduction in MRSA clinical isolates (from 3.4 per 1,000 ICU days to 2.1 per 1,000 ICU days) and a 44% reduction in all-cause bloodstream infections (6.1 per 1,000 ICU days to 3.6 per 1,000 ICU days). Universal decolonization should be pursued in lieu of targeted actions informed by active surveillance for the purpose of reducing MRSA.

4. 4. Hospital-wide active surveillance for MRSA can be used in conjunction with contact precautions to reduce the incidence of MRSA infection. (Quality of evidence: MODERATE)

   1. a. Most hospitals across the United States do not perform active surveillance for all patients. ^{Reference Morgan, Murthy and Munoz-Price100} However, between 2007 and the beginning of the COVID-19 pandemic, US Department of Veterans’ Affairs (VA) acute-care hospitals conducted hospital-wide active surveillance. In 2007, VA acute-care hospitals nationwide launched a MRSA control program that included universal nasal active surveillance for MRSA, contact precautions for MRSA carriers, hand hygiene, and increased institutional awareness of infection control. This program resulted in significant reductions in healthcare-associated MRSA infections and MRSA transmission in ICU and non-ICU settings. ^{Reference Jain, Kralovic and Evans64} By 2017, hospital-onset MRSA infections at VA hospitals had declined 66% compared to baseline, and hospital-onset MSSA infections had declined 19%. ^{Reference Jones, Jernigan, Evans, Roselle, Hatfield and Samore65} Questions have arisen regarding what aspects of the VA policy led to the decline, especially relative to active surveillance. Questions have also been raised about the generalizability of findings at VA acute-care hospitals to other hospitals. ^{Reference Morgan, Zhan and Goto101} Hospitals that do not want to conduct whole-hospital active surveillance should consider instituting a more targeted policy based on high-risk patients or high-risk encounters. ^{Reference O’Hara, Calfee and Miller42,Reference Nadimpalli, O’Hara and Pineles43} In addition, hospitals should consider using their baseline risk assessment and additional MRSA monitoring and assessments to help guide their decision making. ^{Reference Saint, Meddings and Fowler102} (See the Risk Assessment and Contact Precautions recommendations in the Essential Approaches section above and Section 5 “Performance Measures” below.) Active surveillance testing has cost implications. Cost and yield considerations should be used to help guide cost-effective policies to attain reductions in MRSA transmission and disease. ^{Reference Gidengil, Gay, Huang, Platt, Yokoe and Lee103–Reference Robotham, Deeny, Fuller, Hopkins, Cookson and Stone105}

5. 5. Active surveillance can be performed in the setting of a MRSA outbreak or evidence of ongoing transmission of MRSA within a unit as part of a multifaceted strategy to halt transmission. (Quality of evidence: MODERATE).

   1. a. During outbreaks, serial (eg, weekly until outbreak is over) AST can provide important information about the scope of the outbreak, and AST helps identify new cases to enable communication and response (eg, contact precautions, decolonization).

   2. b. See the Decolonization recommendations below for discussion of components of a multimodal strategy.

   3. c. The CDC 2020 NICU guidelines provide information regarding application of this recommendation in the neonatal ICU. ^{Reference Milstone, Elward and Brady48}

   4. d. See the “Screen HCP for MRSA infection or colonization” recommendation below for additional discussion regarding use of AST for HCP.

Screen HCP for MRSA infection or colonization

1. 1. Screen HCP for MRSA infection or colonization if they are epidemiologically linked to a cluster of MRSA infections. (Quality of evidence: LOW)

   1. a. HCP can become transiently or persistently colonized with MRSA and can be the source of hospital outbreaks.

      1. i. Routine screening of HCP for MRSA is not currently recommended in the endemic setting. ^{Reference Gurieva, Bootsma and Bonten106}

      2. ii. Screening of HCP can be an important component of an outbreak investigation if HCP have been epidemiologically linked to a clonal cluster of MRSA cases or if there is evidence of ongoing transmission despite comprehensive implementation of basic MRSA control measures. ^{Reference Gurieva, Bootsma and Bonten106}

      3. iii. See MRSA decolonization below and Section 6: Implementation Strategies for discussion of targeted decolonization therapy regimens that can be used for the treatment of MRSA-colonized HCP.

MRSA decolonization

MRSA decolonization therapy most commonly refers to the administration of topical antimicrobial or antiseptic agents for the purpose of eradicating or suppressing the carrier state and ultimately reducing clinical infection. MRSA decolonization can be targeted to MRSA carriers or applied universally to populations deemed at high risk for infection. For the purpose of this document, MRSA decolonization is considered to be intranasal antimicrobial and/or antiseptic treatment with chlorhexidine (CHG) skin antisepsis.

Because MRSA carriage is the strongest predictor of subsequent MRSA infection, decolonizing carriers is important if MRSA prevalence or disease is a target for improvement. Intranasal treatment is necessary to eliminate MRSA in the nose, which is recognized as a primary carriage site. Clearance of the nasal reservoir has been shown to be both necessary and sufficient for infection reduction among S. aureus carriers. ^{Reference von Eiff, Becker, Machka, Stammer and Peters107–Reference Fritz, Camins and Eisenstein110} A discussion of agents that have been used for nasal decolonization is provided in the Appendix. MRSA may also contaminate and/or colonize skin sites, most commonly axilla and groin, although other skin sites may also harbor MRSA. Skin antisepsis is often used during decolonization and for source control of MRSA. Finally, although nasal eradication of MRSA is a necessary component to prevent infection in MRSA carriers, some evidence indicates that skin antisepsis alone may reduce MRSA transmission to others in ICUs. ^{Reference Derde, Cooper and Goossens52} Hospitals may choose to use a CHG-only decolonization strategy to target other pathogens or reduce bloodstream infections, but if the goal is to reduce MRSA, then nasal decolonization may be necessary to optimize the likelihood of success.

Several randomized clinical trials (discussed below) have shown that decolonization significantly reduces MRSA carriage, transmission, and subsequent infection in patients known to carry MRSA or to be at risk of MRSA acquisition and/or infection. These are discussed below within the specific recommendations.

S. aureus outcomes identified through the literature review for MRSA outcomes have been described due to the relevant interest for healthcare-associated infection (HAI) reduction from S. aureus regardless of susceptibility pattern, but the recommendations are based on available evidence to reduce MRSA.

Few studies of high-quality evidence have evaluated MRSA outcomes in children. Most data supporting the recommendations below have been generated in adult patient populations. When available, pediatric data are noted.

Complications of decolonization therapy are rare and generally mild; however, hospitals should be aware of potential adverse effects, such as drug-related toxicities and development of resistance (eg, mupirocin) or reduced susceptibility (eg, chlorhexidine) to the agents used, when considering the potential benefits and risks of implementing a MRSA or S. aureus decolonization program. ^{Reference Miller, Dascal, Portnoy and Mendelson111–Reference Teo, Low, Ding, Koh and Hsu113}

1. 1. Use universal decolonization (daily CHG bathing plus 5 days of nasal decolonization) for all patients in adult ICUs to reduce endemic MRSA clinical cultures. (Quality of evidence: HIGH)

   1. a. The previously described REDUCE MRSA Trial demonstrated that universal decolonization of ICU patients with daily CHG bathing and 5 days of twice-daily mupirocin was superior to screening and targeted decolonization as well as to screening and targeted contact precautions for prevention of MRSA-positive clinical isolates and all-cause bloodstream infection. ^{Reference Huang, Septimus and Kleinman99} (See Section 4 Additional Approaches for Preventing MRSA, Active Surveillance Testing recommendation.) For determining the applicability of this regimen to hospitals, trial benefit occurred at fairly low endemic levels of >3 MRSA clinical cultures per 1,000 ICU days. This approach has been demonstrated to be cost-effective, including sparing the cost of screening. ^{Reference Gidengil, Gay, Huang, Platt, Yokoe and Lee103,Reference Huang, Septimus and Avery114}

   2. b. Climo et al ^{Reference Climo, Yokoe and Warren115} reported that universal CHG alone in adult ICUs reduced bloodstream infections by 28% and reduced the composite of MRSA and vancomycin-resistant enterococcal (VRE) acquisition by 23%. Derde et al (2013) ^{Reference Derde, Cooper and Goossens52} also demonstrated that CHG bathing decreased MRSA acquisition in ICU standardization phases leading up to an RCT that showed no benefit of either conventional or rapid PCR MRSA screening and isolation over high compliance hand hygiene and universal CHG bathing.

   3. c. Even though universal CHG alone does not decolonize carriers, it is effective in reducing transmission of MRSA from carriers to noncarriers in ICUs. Thus, for the purpose of optimally addressing MRSA, the combined effects of mupirocin plus universal CHG are recommended.

   4. d. Finally, although universal decolonization has been found to be superior to screening and targeted decolonization, hospitals may have other reasons for screening patients for MRSA. These may include outbreak response, desire for surveillance data, desire to implement contact precautions for known carriers, and clinical reasons related to restricting empiric anti-MRSA therapy or preoperative vancomycin prophylaxis to known MRSA carriers.

2. 2. Perform preoperative nares screening with targeted use of CHG and nasal decolonization in MRSA carriers to reduce MRSA SSI in surgical procedures involving implantation of hardware. (Quality of evidence: MODERATE)

   1. a. Note that decolonization can be applied universally as an alternative.

   2. b. Preoperative targeted screening and decolonization of S. aureus carriers is commonly performed for surgical procedures involving the placement of hardware to reduce SSI. Although most studies have evaluated S. aureus outcomes and are not specific to MRSA, a large meta-analysis of RCTs and other studies involving surgeries with hardware similarly found that targeted or universal nasal decolonization reduced S. aureus SSI and that nasal decolonization of MRSA carriers reduced MRSA SSI. ^{Reference Schweizer, Chiang and Septimus116}

   3. c. S. aureus outcomes were not the target of this guidance document or its search strategy. Nevertheless, we highlight some the S. aureus evidence here because MRSA is a subset of S. aureus. In a large, 20-hospital, interventional cohort study of cardiac, hip, and knee surgeries, targeted nasal decolonization reduced S. aureus SSI. ^{Reference Schweizer, Chiang and Septimus116} Additionally, in a post-hoc analysis of a single-center RCT of 1,697 patients undergoing arthroplasty or spinal fusion, universal nasal 5% povidone-iodine was superior to universal 2% mupirocin for S. aureus deep SSI. ^{Reference Phillips, Rosenberg and Shopsin117} Universal nasal decolonization without nasal screening can be employed for pragmatic reasons to spare the logistics for screening for S. aureus or MRSA. Use of povidone-iodine may also be chosen for pragmatic reasons because it does not require a prescription, including prescription-related transportation needs or insurance copays that may affect patient adherence.

   4. d. Please refer to the “Compendium of Strategies to Prevent Surgical Site Infections in Acute Care Hospitals: 2022 Update” ^{Reference Calderwood, Anderson and Bratzler87} for recommendations regarding decolonization for organisms other than MRSA.

3. 3. Screen for MRSA and provide targeted decolonization with CHG bathing and nasal decolonization to MRSA carriers in surgical units to reduce postoperative MRSA inpatient infections. (Quality of evidence: MODERATE)

   1. a. Note that decolonization can be applied universally as an alternative.

   2. b. In a multinational trial of 33 surgical units in 10 hospitals involving 126,750 admissions, an intervention of enhanced hand hygiene plus universal screening and targeted decolonization of MRSA carriers reduced MRSA clinical cultures by 12% per month. In a secondary analysis of clean surgical patients, universal screening and targeted decolonization of MRSA carriers reduced MRSA clinical cultures by 15% per month and MRSA infections by 17% per month. ^{Reference Lee, Cooper and Malhotra-Kumar118}

   3. c. S. aureus outcomes were not the target of this guidance document nor its search strategy. Nevertheless, we highlight the key S. aureus evidence here because MRSA is a subset of S. aureus. In an RCT of 1,000 mostly surgical patients that evaluated universal inpatient screening for S. aureus and CHG and mupirocin for identified carriers, a significant 58% reduction was achieved in inpatient S. aureus infection among carriers. ^{Reference Bode, Kluytmans and Wertheim119} In addition, decolonization can reduce postsurgical inpatient infections beyond SSI. The Mupirocin and the Risk of Staphylococcus aureus (MARS) Study ^{Reference Perl, Cullen and Wenzel120} was a 3,864-person RCT of the addition of mupirocin to preoperative chlorhexidine (CHG) for S. aureus carriers undergoing a variety of surgical procedures (ie, general, gynecologic, neurologic, oncologic, and cardiothoracic surgery) with and without hardware. This mupirocin addition significantly decreased nosocomial S. aureus infections by 51% among S. aureus carriers, although it did not significantly reduce S. aureus SSIs.

4. 4. Provide CHG bathing plus nasal decolonization to known MRSA carriers outside the ICU with medical devices, specifically central lines, midline catheters, and lumbar drains, to reduce MRSA-positive clinical cultures. (Quality of evidence: MODERATE)

   1. a. The Active Bathing to Eliminate Infection (ABATE Infection) Trial ^{Reference Huang, Septimus and Kleinman121} was a 53-hospital cluster-randomized trial involving nearly 340,000 patients comparing routine care to universal decolonization with CHG bathing plus targeted nasal mupirocin for known MRSA carriers. Active screening was not a component of this trial. No overall reduction in the composite outcome of MRSA or VRE carriage, nor all-cause bloodstream infections was detected. However, in a post-hoc analysis, non-ICU patients with medical devices had a significant 37% reduction in MRSA and VRE and a significant 32% reduction in all-cause bloodstream infections. Patients with medical devices (specifically, central lines, midlines, and lumbar drains) were only 10% of inpatients, but they had 37% of MRSA and VRE cultures and 56% of all-cause bloodstream infections.

5. 5. Consider postdischarge decolonization of MRSA carriers to reduce postdischarge MRSA infections and readmission. (Quality of evidence: HIGH).

   1. a. The Changing Lives by Eradicating Antibiotic Resistance (CLEAR) Trial ^{Reference Huang, Singh and McKinnell17} was an RCT to decrease postdischarge infections in MRSA carriers comparing routine care to postdischarge decolonization (CHG bathing, CHG mouthwash, nasal mupirocin) given for 5 days twice monthly for 6 months. The trial involved 2,121 MRSA carriers. Decolonization significantly reduced MRSA infection (most requiring rehospitalization) by 30% in the 1-year follow-up period, with a number needed to treat of 30. The impact of a shorter duration of decolonization is not known, but the risk of postdischarge infection was higher with closer proximity to discharge.

   2. b. Postdischarge decolonization was first systematically performed by the Dutch Search and Destroy program to decolonize MRSA carriers to prevent infection. ^{Reference Ammerlaan, Kluytmans and Berkhout122} These postdischarge efforts require coordination and investment uncommonly adopted by hospitals. Because population-based medicine continues to be a goal for HAI prevention across the continuum of care, assessments of pragmatic implementation and adherence need to be addressed.

6. 6. Neonatal ICUs should consider targeted or universal decolonization during times of above-average MRSA infection rates or targeted decolonization for patients at high risk of MRSA infection (eg, low birth weight, indwelling devices, or prior to high-risk surgeries). (Quality of evidence: MODERATE)

   1. a. S. aureus is a leading cause of HAI in neonatal intensive care units (NICUs). Neonates in the NICU, especially low-birthweight neonates, are at high risk of invasive S. aureus disease. ^{Reference Ericson, Popoola and Smith123} Because most neonates have never left the hospital, neonates usually develop MRSA colonization or infection as a result of hospital-based transmission. Neonates acquire MRSA from colonized parents, HCP, or the environment. MRSA is the most commonly reported cause of NICU outbreaks, ^{Reference Johnson and Quach124} so when neonates in the NICU are identified with a hospital-onset MRSA infection, further assessment is warranted to identify an ongoing cluster of transmission.

      1. i. MRSA colonization is an important risk factor for subsequent infection in this population. Quasi-experimental studies have shown that decolonization can reduce MRSA infections during endemic and outbreak settings. ^{Reference Milstone, Elward and Brady48,Reference Akinboyo, Zangwill, Berg, Cantey, Huizinga and Milstone125}

      2. ii. Targeted and universal decolonization approaches have both been successfully used to reduce MRSA in this population. ^{Reference Huang, Lien and Lin126–Reference Popoola and Milstone128} Decolonization reduces MRSA colonization, acquisition and infection in neonates. ^{Reference Pierce, Lessler, Popoola and Milstone129}

      3. iii. Decolonization also reduces MSSA colonization and infections in this population. ^{Reference Voskertchian, Akinboyo, Colantuoni, Johnson and Milstone130–Reference Kotloff, Shirley and Creech132}

      4. iv. Mupirocin and chlorhexidine are the most commonly used decolonization agents in NICUs. In a recent RCT, 66 infants were assigned to intranasal mupirocin, and no product-related moderate, serious, or severe adverse events occurred. ^{Reference Kotloff, Shirley and Creech132} Chlorhexidine has been safely used in neonates, but due to potential for skin irritation and systemic absorption, it should be used with caution in premature infants. ^{Reference Popoola, Colantuoni and Suwantarat133} The US Food and Drug Administration notes that chlorhexidine should be “used with care in premature infants or infants under 2 months of age.” ¹³⁴ Chlorhexidine is used widely in NICUs and its use increased from 59% in 2009 to 86% in 2015 in a survey of US NICUs. ^{Reference Johnson, Bracken, Tamma, Aucott, Bearer and Milstone135,Reference Tamma, Aucott and Milstone136} Chlorhexidine-associated adverse events are infrequent, but many NICUs limit chlorhexidine use, especially in preterm infants within the first month of life. ^{Reference Akinboyo, Zangwill, Berg, Cantey, Huizinga and Milstone125,Reference Johnson, Bracken, Tamma, Aucott, Bearer and Milstone135}

      5. v. In addition to HCP and the environment, parents can be an important reservoir for S. aureus and can expose their neonates in the NICU. The TREAT PARENTS trial showed that decolonizing parents with intranasal mupirocin and topical chlorhexidine gluconate baths reduced transmission of MRSA and MSSA to neonates in the NICU. ^{Reference Milstone, Voskertchian and Koontz137}

7. 7. Burn units should consider targeted or universal decolonization during times of above-average MRSA infection rates. (Quality of evidence: Moderate)

   1. a. Higher quality evidence is needed to support a recommendation for routine decolonization of burn patients (unresolved issue).

   2. b. Burn patients are at high risk of MRSA acquisition and infection.

   3. c. Quasi-experimental studies have shown that decolonization can reduce MRSA infections. Decolonization strategies have included universal intranasal mupirocin with chlorhexidine antisepsis, universal decolonization using mupirocin and daily hypochlorous acid solution, and octenidine antisepsis for intact skin and nasal mucosa. ^{Reference Baier, Ipaktchi and Schwab138–Reference Johnson, Nygaard, Cohen, Fey and Wagner141}

   4. d. Given inconsistent results on the safety of antiseptics to interfere with wound healing, the role of topical antisepsis in this population for MRSA prevention must carefully balance the risk of toxicity and benefit of preventing MRSA infections. Therefore, the decision to implement targeted or universal decolonization in burn patients should be guided by a local risk assessment of MRSA incidence.

8. 8. Consider targeted or universal decolonization of hemodialysis patients. (Quality of evidence: MODERATE) Higher-quality evidence is needed to support a recommendation for routine decolonization of dialysis patients.

   1. a. MRSA bloodstream infections complicate care of hemodialysis patients. MRSA colonization predisposes individuals to subsequent MRSA infections, and hemodialysis patients have one of the highest risks of MRSA invasive disease, with a risk of 45 per 1,000 patients, which as 100-fold higher than that of the average population. ^{142,Reference Nguyen, Shugart and Lines143}

   2. b. A systematic review and meta-analysis found that intranasal mupirocin with chlorhexidine body washes can eradicate MRSA carriage in hemodialysis patients. ^{Reference Gebreselassie, Priore and Marschall144} Data are not available demonstrating effectiveness of decolonization on reducing MRSA infections. However, a separate systematic review and meta-analysis found an 82% reduction in the risk of S. aureus bacteremia, comparing those who did and did not receive mupirocin. ^{Reference Tacconelli, Carmeli, Aizer, Ferreira, Foreman and D’Agata145}

9. 9. Decolonization should be strongly considered as part of a multimodal approach to control MRSA outbreaks. (Quality of evidence: MODERATE)

   1. a. Although no clinical trials have tested strategies to control MRSA outbreaks, many quasi-experimental studies have demonstrated successful outbreak control that includes MRSA decolonization as part of a multimodal approach to reduce MRSA transmission and infection.

   2. b. In outbreak situations, decolonization can protect colonized individuals from infection and reduce colonization pressure that may promote transmission.

      1. i. Intranasal therapy reduces infection risk for individual patients.

      2. ii. Topical skin decontamination reduces bioburden and helps reduce organism transmission.

   3. c. Decolonization can be implemented universally or in combination with AST

      1. i. In an outbreak setting, active surveillance cultures can help measure the extent of organism spread in the unit and provide organisms for strain typing.

      2. ii. In addition to identifying patients as a reservoir for propagating outbreaks, successful outbreak control may involve screening HCP to detect reservoirs, especially in high-risk units like the neonatal ICU and burn units. ^{Reference Kossow, Kampmeier, Schaumburg, Knaack, Moellers and Mellmann146} HCP have been implicated as reservoirs for MRSA transmission during adult hospital unit and NICU outbreaks and during times of ongoing clonal transmission. ^{Reference Hawkins, Stewart, Blatchford and Reilly147,Reference Cimolai148} After implementation and failure of other basic MRSA prevention and control measures (eg, hand hygiene, contact precautions, enhanced environmental cleaning, screening and decolonizing neonates), screening and decolonizing HCWs has helped successfully control MRSA outbreaks in adult units and NICUs. ^{Reference Popoola, Budd and Wittig149–Reference Leroyer, Lehours and Tristan151}

Universal use of gowns and gloves

1. 1. Use gowns and gloves when providing care to or entering the room of all adult ICU patients, regardless of MRSA colonization status. (Quality of evidence: MODERATE)

   1. a. A cluster-randomized trial conducted in 20 adult medical and surgical ICUs compared the effect of universal glove and gown use for all patient contact and when entering any patient room with standard practice (ie, the use of gowns and gloves only for patients known to be infected or colonized with antimicrobial-resistant organisms) on the rate of acquisition of antimicrobial-resistant gram-positive organisms and healthcare-associated infections. ^{Reference Harris, Pineles and Belton63} Although the investigators found no difference in the primary outcome of acquisition of either MRSA or VRE, there was a significantly greater relative reduction in the prespecified secondary outcome of MRSA acquisition in intervention units compared to control units (40.2% vs 15%; P = .046).

      1. i. On intervention units, contamination of HCW clothing was 70% lower during the intervention period than during standard practice in the postintervention period (7.1% vs 23%; OR, 0.3; 95% CI, 0.2–0.6). ^{Reference Williams, McGraw and Schneck152} In addition to the use of gowns and gloves, a lower frequency of HCP visits (4.28 vs 5.24 per hour; P = .02) and higher hand-hygiene compliance (78.3% vs 62.9% upon exit; P = .02) in the intervention arm compared to the control arm may have played a role in the observed difference in MRSA acquisition between the 2 groups. In subsequent mathematical modeling, the decrease in MRSA acquisition was found to be primarily due to the gown-and-glove use intervention, with additional but smaller effects from improved hand hygiene and lower HCP–patient contact rates. ^{Reference Harris, Morgan, Pineles, Perencevich and Barnes56}

      2. ii. In a subsequent secondary analysis of data from this trial, the intervention was associated with a nonsignificant decrease in acquisition of antibiotic-resistant gram-negative bacteria (rate ratio, 0.90; 95% CI, 0.71–1.12). ^{Reference Harris, Morgan, Pineles, Magder, O’Hara and Johnson153} This finding suggests that universal gown-and-glove use when providing care in adult ICUs may provide benefits in addition to the potential to reduce MRSA transmission.

Unresolved issues

Several unresolved issues remain related to MRSA and its transmission. A full discussion of these issues is beyond the scope of this document, but a brief mention of some of these important topics is worthwhile.

1. 1. Universal MRSA decolonization

   1. a. Additional study is needed to determine the incremental benefit of the addition of mupirocin to daily chlorhexidine bathing in the adult ICU because the REDUCE MRSA study used both mupirocin and CHG for their decolonization arm. ^{Reference Huang, Septimus and Kleinman99}

   2. b. Additional study is needed to evaluate the role of routine universal decolonization of NICU patients.

2. 2. Mupirocin and chlorhexidine resistance: The risk for development of resistance to mupirocin and/or chlorhexidine as they become more widely used is currently unknown, although some centers have reported increased rates of resistance.

   1. a. Chlorhexidine: Although some published data have demonstrated reduced susceptibility in vitro to chlorhexidine among staphylococci by at least 2 mechanisms of resistance, the definitions used in these studies often use an MIC threshold far below standard CHG applications (eg, often an MIC of 8 µg/mL is used to define “resistance,” even though 2% CHG applies 20,000 µg/mL to the skin). Clinical trials have evaluated, but have not identified, the emergence of resistance to CHG. ^{Reference Climo, Yokoe and Warren115,Reference Hayden, Lolans and Haffenreffer154}

   2. b. Mupirocin resistance has been studied extensively; however, the ability of hospital laboratories to provide mupirocin resistance data is limited.

      1. i. Mupirocin resistance is phenotypically categorized into 2 levels based on the minimum inhibitory concentration (MIC). Low-level resistance (MICs of 8–256 mg/mL), and high-level resistance (MICs > 512 mg/mL). ^{Reference Patel, Gorwitz and Jernigan155} The molecular mechanism of low-level mupirocin resistance involves point mutations and is mediated by plasmid encoded genes in high-level mupirocin.

      2. ii. A recent meta-analysis described a global increase in the prevalence high-level mupirocin resistance among clinical S. aureus isolates over time. Because mupirocin remains the most effective antibiotic for MSSA and MRSA decolonization, a reduction in its effectiveness presents a risk. ^{Reference Dadashi, Hajikhani, Darban-Sarokhalil, van Belkum and Goudarzi156}

      3. iii. Emergence of mupirocin resistance following increased use has not been reported consistently. The use of universal ICU decolonization with mupirocin in the REDUCE MRSA Trial was not associated with emergence of mupirocin resistance when evaluating thousands of MRSA isolates from the trial. ^{Reference Hayden, Lolans and Haffenreffer154} Additional studies of mupirocin resistance have been hampered by a lack of availability of routine susceptibility testing in most hospital laboratories. Large-scale studies on decolonization failure associated with increased mupirocin use are needed to provide an understanding of the risk.

3. 3. MRSA-colonized HCP: The optimal use of AST to identify asymptomatic carriage of MRSA among HCP and the optimal management (eg, decolonization therapy, follow-up monitoring) of MRSA-colonized HCP have not been definitively determined.

Internal reporting

The performance measures described here are intended to support internal hospital quality-improvement efforts and do not necessarily address external reporting requirements. The process and outcome measures suggested here are derived from published guidelines and other relevant literature. A more detailed description of outcome measures that may be useful for MRSA transmission and infection prevention programs is available in a position paper published in 2008 by SHEA and HICPAC. ^{Reference Cohen, Calfee and Fridkin46}

Process measures

Process measures can be used to assess compliance with various components of a MRSA prevention program. Such measures may include compliance with essential practices, such as hand hygiene and contact precautions (eg, use of gown and gloves), as well as compliance with additional approaches that have been implemented by the hospital (eg, daily bathing with chlorhexidine and/or AST).

Outcome measures

In 2008, SHEA and the HICPAC published recommendations for monitoring multidrug-resistant organisms (MDROs) in healthcare settings. ^{Reference Cohen, Calfee and Fridkin46} These recommendations are applicable to MRSA as well as other MDROs. That position paper describes the following MRSA outcome measures.

1. A. Basic outcome measures for all acute-care hospitals

   1. 1. MRSA-specific line lists (eg, electronic databases) for tracking patients who have MRSA;

   2. 2. Annual antibiograms for monitoring antimicrobial susceptibility patterns (eg, rates of methicillin resistance) among isolates recovered from patients;

   3. 3. Estimates of the MRSA infection burden that use objective, laboratory-based metrics such as the incidence (or incidence density) of hospital-onset MRSA bacteremia; and

   4. 4. Proxy measures of healthcare-acquisition of MRSA such as incidence (or incidence density) of hospital-onset MRSA based on clinical culture data.

2. B. Supplemental/advanced outcome measures for acute-care hospitals

   1. 1. Additional measures of the burden of healthcare-associated infection (eg, incidence or incidence density of hospital-associated MRSA infections),

   2. 2. Estimates of burden of MRSA exposure within the facility (eg, rates of overall and admission MRSA prevalence, point prevalence), and the burden of hospital-associated acquisition of MRSA (eg, incidence of hospital-onset MRSA based on clinical culture data and AST data).

In calculating these outcome measures, guidelines recommend careful consideration of how duplicate isolates from the same patient during the selected surveillance period will be handled. More specific details regarding these metrics (eg, definitions, methods of calculation) are available in the original SHEA/HICPAC position paper. ^{Reference Cohen, Calfee and Fridkin46} In addition to calculating outcome measures locally, hospitals that report MRSA data to the CDC NHSN Multidrug Resistant Organism and C. difficile Infection (MDRO/CDI) Module have the option of having a number of outcome measures calculated automatically. ¹⁵⁷ The metrics included in this NHSN module are similar to some of those described in the SHEA-HICPAC position paper. ^{Reference Cohen, Calfee and Fridkin46} Relative to MRSA, certain outcome measures are available to hospitals that submit only bloodstream isolate data (eg, hospital-onset MRSA bloodstream infection incidence). Additional outcomes data are available to those who submit information regarding MRSA isolates from other clinical specimens or from AST.

External reporting: State and federal requirements

1. 1. Federal requirements: In the United States, the Centers for Medicare & Medicaid Services (CMS) Hospital Inpatient Quality Reporting (IQR) Program requires acute-care hospitals to report hospital-wide inpatient MRSA bloodstream isolates via the CDC NHSN Multidrug-Resistant Organism and C. difficile Infection (MDRO/CDI) Module. ¹⁵⁸

2. 2. State requirements: States may have additional reporting requirements for MRSA-related data. Contact your local or state health department for state-specific requirements.

Engage

1. 1. Collaborate with representatives from departments and groups appropriate for the strategy being implemented (eg, hospital administration, nursing staff, medical staff, environmental services/housekeeping, facilities management, procurement, clinical laboratory, admitting and bed assignment department, case management, human resources, risk management, community and/or patient education specialists, information technology). Include opinion leaders, role models, and unit champions from these groups in planning and implementation of initiatives.

2. 2. Consultation with a trained individual with expertise in MRSA control and prevention may be useful for program development and assessment if such a person is not available within the hospital.

3. 3. Engage executive leadership based on clinical outcomes data, public reporting requirements, and locally determined return on investment calculations.

Educate

1. 1. Provide an educational program to foster desired behavior changes. Include a discussion of MRSA risk factors, routes of transmission, outcomes associated with infection, organization-specific prevention measures (and the evidence supporting their use), local MRSA epidemiology (MRSA infection rates, etc), the potential adverse effects of contact isolation, roles that HCP play in MRSA prevention, and current data regarding HCP compliance with infection prevention and control measures.

2. 2. Target educational programs based on HCP needs (ie, healthcare practitioner, support personnel). Given the wide range of educational backgrounds and job descriptions among hospital personnel, several educational programs will be needed to provide the necessary information at the appropriate level for all relevant personnel.

3. 3. Provide evidence that supports the use of selected strategies.

4. 4. Education should utilize principles of adult learning (eg, use relatable case scenarios or situations) and may be accomplished in settings and formats that are determined to be the most effective by the organization, including classroom, unit-based meetings, or computer stations. Possible formats include internet-based training, newsletters, communication board postings, and other communication means. Coaching sessions, one-to-one engagement, etc, may be useful to reinforce implementation of educational materials.

5. 5. To ensure consistent messaging to learners, consider providing standardized educational materials such as guidelines, templates, observation tools, skills training, scripting, etc., which outline minimum expectations of the organization that are relevant to the learner.

Execute

In addition to the examples provided, please refer to the Appendix for a more detailed discussion of factors to consider during the implementation of a MRSA AST program. Guidance for the implementation of an effective hand hygiene program is available in the Compendium document on strategies for optimizing hand hygiene. ^{Reference Glowicz, Landon and Sickbert Bennett159,160}

Contact precautions

1. 1. Place patients in a single or private room when available.

2. 2. Place patients who have MRSA in cohorts when a single or private room is not available.

3. 3. Cohort placement does not eliminate the need for compliance with hand hygiene and other infection prevention measures between patient contacts.

4. 4. Don gown and gloves upon entry into the patient’s room and change the gown and gloves before having contact with a subsequent patient or the subsequent patient’s immediate environment.

5. 5. HCP should have a thorough understanding of the benefits and potential adverse effects associated with the use of contact precautions.

6. 6. Patients placed on contact precautions should continue to receive the same level and quality of care as those who are not on contact precautions.

7. 7. Dedicate noncritical patient care items such as blood pressure cuffs, stethoscopes, etc, to a single patient when they are known to be colonized or infected with MRSA. When equipment must be shared among patients, clean and disinfect the equipment between patients.

8. 8. Establish institutional criteria for discontinuation of contact precautions.

   1. a. A test-based strategy may be used to determine whether a patient remains colonized with MRSA. Because a single negative surveillance test may not adequately detect the persistence of MRSA colonization, facilities may choose to require multiple negative tests prior to discontinuing contact precautions. Expert guidance is available to assist facilities in making institutional policies for discontinuation of contact precautions. ^{Reference Siegel, Rhinehart, Jackson and Chiarello62,Reference Banach, Bearman and Barnden71} When retesting MRSA patients to document clearance is considered, waiting at least a few months (eg, 4–6 months) since the last positive test is often advised. Some hospitals may choose to consider MRSA-colonized patients to be colonized indefinitely.

Cleaning and disinfection

Current guidelines outline environmental and equipment disinfection and sterilization standards as follows. ^{Reference Siegel, Rhinehart and Jackson61,Reference Sehulster, Chinn and Cdc161,162}

1. 1. Develop written protocols for daily and terminal cleaning and disinfection of patient rooms. Protocols should address the type of equipment or surface, persons responsible for performing the tasks, frequency, disinfectant product appropriate to the device or surface, and required contact time to achieve effective disinfection.

2. 2. Pay close attention to cleaning and disinfection of high-touch surfaces in patient care areas (eg, bed rails, carts, bedside commodes, doorknobs, and faucet handles).

3. 3. Disinfect portable, reusable healthcare equipment after each use, at the time of patient discharge from the room in which the equipment is located, when the equipment is moved out of a room, between uses on different patients, and at the frequency recommended by the device manufacturer if specified in the instructions for use.

4. 4. The use of supplemental disinfection methods, such as hydrogen peroxide vapor, ultraviolet light, and antimicrobial surfaces, has been shown in some non-randomized studies to have potential benefit in reducing the burden of organisms in the healthcare environment. However, these additional technologies are costly, and their clinical effectiveness for prevention of MRSA transmission has not yet been definitively proven ^{Reference Anderson, Chen and Weber163–Reference Salgado, Sepkowitz and John166} Notably, these methods should be used as supplements to, but not as replacements for, routine cleaning and disinfection.

Alert systems

1. 1. Laboratory alerts for new MRSA-positive patients and alerts to identify MRSA-positive patients on readmission or transfer ^{Reference Kac, Grohs and Durieux167–Reference Wright169}

   1. a. Patients with newly identified MRSA

      1. i. The laboratory-based manual alerting system may include immediate notification of clinical and IP staff via fax, phone, pager, email, or notification in EMR or electronic surveillance system.

   2. b. Readmission or intrafacility transfer of patients with MRSA

      1. i. Manual or computer-based databases of patients’ MRSA status may be used to identify known MRSA-positive patients at the time of readmission and bed assignment. A designated field in the EMR may be used to indicate a patient’s MRSA-positive status.

      2. ii. The receiving unit should be notified of the patient’s MRSA-positive status prior to the patient’s arrival on the unit.

      3. iii. The alert should remain in effect until the facility’s MRSA clearance criteria have been met.

   3. c. Interfacility transfer of patients with MRSA

      1. i. A patient’s MRSA-positive status should be communicated to a receiving healthcare facility prior to the patient’s transfer.

      2. ii. Collaborate with nursing, discharge planning, and case management to include relevant infection control data, such as MRSA infection or colonization, on communication tools.

      3. iii. Create an infection prevention interfacility transfer tool such as the one developed by the CDC (http://www.cdc.gov/HAI/toolkits/InterfacilityTransferCommunicationForm11-2010.pdf).

      4. iv. If the patient has been transferred to another facility before susceptibility information is available, the receiving organization should be notified.

      5. v. When receiving patients in transfer from another healthcare facility, require the transferring healthcare facility to provide MRSA status information and other relevant infection control information during the transfer hand-off communication process.

Educating patients and their families about MRSA

1. 1. Provide standardized information about MRSA and contact precautions. Methods of information dissemination might include patient education sheets in appropriate languages, patient education channels, websites, or video presentations. A member of the care team should assess the patient’s understanding and answer specific questions that remain.

2. 2. Include information that addresses concerns and anticipates questions, such as general information about MRSA, the difference between colonization and infection, the hospital’s MRSA prevention program, the components of and rationale for contact precautions, and the risk of transmission to family and visitors. ^{Reference Abad, Fearday and Safdar74,Reference Mozzillo, Ortiz and Miller170}

3. 3. To alleviate MRSA-related concerns that remain after patient discharge, provide education and helpful tips about managing MRSA in the home setting. ^{Reference Briggs and Milstone171}

4. 4. Determine whether educational materials will be developed by facility personnel or obtained from an external resource (eg, professional societies, public health authorities, commercial vendors).

Active surveillance testing

Please refer to the Appendix for a more detailed discussion of the issues outlined below.