SHEA/IDSA/APIC Practice Recommendation: Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute-care hospitals: 2022 Update

Previously published guidelines have provided comprehensive recommendations for detecting and preventing healthcare-associated infections (HAIs). The intent of this document is to highlight practical recommendations in a concise format designed to assist acute-care hospitals in implementing and prioritizing efforts to prevent methicillin-resistant Staphylococcus aureus (MRSA) transmission and infection. This document updates the “Strategies to Prevent Methicillin-Resistant Staphylococcus aureus Transmission and Infection in Acute Care Hospitals” published in 2014.1 This expert guidance document is sponsored by the Society for Healthcare Epidemiology of America (SHEA). It is the product of a collaborative effort led by SHEA, the Infectious Diseases Society of America (IDSA), the Association for Professionals in Infection Control and Epidemiology (APIC), the American Hospital Association (AHA), and The Joint Commission, with major contributions from representatives of a number of organizations and societies with content expertise.


Purpose
Previously published guidelines have provided comprehensive recommendations for detecting and preventing healthcareassociated infections (HAIs). The intent of this document is to highlight practical recommendations in a concise format designed to assist acute-care hospitals in implementing and prioritizing efforts to prevent methicillin-resistant Staphylococcus aureus (MRSA) transmission and infection. This document updates the "Strategies to Prevent Methicillin-Resistant Staphylococcus aureus Transmission and Infection in Acute Care Hospitals" published in 2014. 1 This expert guidance document is sponsored by the Society for Healthcare Epidemiology of America (SHEA). It is the product of a collaborative effort led by SHEA, the Infectious Diseases Society of America (IDSA), the Association for Professionals in Infection Control and Epidemiology (APIC), the American Hospital Association (AHA), and The Joint Commission, with major contributions from representatives of a number of organizations and societies with content expertise.

Summary of major changes
This section lists major changes from the "Strategies to Prevent Methicillin-Resistant Staphylococcus aureus Transmission and Infection in Acute Care Hospitals" published in 2014, 1 including recommendations that have been added, removed, or altered. Recommendations are categorized as essential practices that should be adopted by all acute-care hospitals (in 2014 these were "basic practices," renamed to highlight their importance as foundational for HAI prevention programs) or additional approaches that can be considered for use in locations and/or populations within hospitals when transmission or infection from MRSA is not controlled after implementation of essential practices (in 2014 these were "special approaches"). See Table 1 for a complete summary of the recommendations contained in this document.

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 MRSAcolonized or MRSA-infected patients.
Additional approaches • Active surveillance testing (AST) remains an additional practice, but specific recommendations, supporting data, and quality-ofevidence 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.

Intended use
This document was developed following the process outlined in the Handbook for SHEA-Sponsored Guidelines and Expert Guidance Documents. 2 No guideline or expert guidance document can anticipate all clinical situations, and this document is not meant to be a substitute for individual clinical judgment by qualified professionals. This document is based on a synthesis of evidence, theoretical rationale, current practices, practical considerations, writinggroup consensus, and consideration of potential harm, where applicable. A summary recommendations is provided in Table 1.

Methods
SHEA recruited 2 subject-matter experts in the prevention of MRSA to lead the panel of members representing the Compendium partnering organizations: SHEA, IDSA, APIC, AHA, and The Joint Commission, as well as the Centers for Disease Control and Prevention (CDC).
SHEA utilized a consultant medical librarian who worked with each panel to develop a comprehensive search strategy for PubMed and Embase (January 2012-July 2019, updated to August 2021). Article abstracts were reviewed by panel members in a double-blind fashion using the abstract management software Covidence (Melbourne, Australia) and were subsequently reviewed as full text. The Compendium Lead Authors group voted to update the literature findings, and the librarian reran the search to update it to August 2021. Panel members reviewed the abstracts of these articles via Covidence and incorporated relevant references.
Recommendations resulting from this literature review process were classified based on the quality of evidence and the balance between desirable and potential for undesirable effects of various interventions ( Table 2). Panel members met via video conference to discuss literature findings; recommendations; quality of evidence for these recommendations; and classification as essential practices, additional approaches, or unresolved issues. Panel members reviewed and approved the document and its recommendations.
The Compendium Expert Panel, composed of members with broad healthcare epidemiology and infection prevention expertise, reviewed the draft manuscript after consensus had been reached by writing-panel members. Following review and approval by the Expert Panel, the 5 partnering organizations, stakeholder organizations, and the CDC reviewed the document. Prior to dissemination, the guidance document was reviewed and approved by the SHEA Guidelines Committee, the IDSA Standards and Practice Guidelines Committee, and the Boards of SHEA, IDSA, and APIC, as well as by the AHA and The Joint Commission.
All panel members complied with SHEA and IDSA policies on conflict-of-interest disclosure.

Section 1: Rationale and statements of concern
Burden of MRSA infection 1. HAIs caused by MRSA are common in acute-care facilities.
a. Worldwide, an estimated 15% of ICU infections are caused by Staphylococcus aureus, and nearly one-third of those (31%) are due to MRSA. 3 In North America, an estimated 23% of ICU infections are caused by S. aureus, and nearly half of those (44%) are due to MRSA. b. In the United States, S. aureus remains one of the most common pathogens associated with HAI. 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. 4,5 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). 5 Compared to data from 2009-2010, the proportions caused by MRSA are lower for each of these HAIs. 6 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. 7 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. Outcomes associated with MRSA HAIs a. MRSA infections are associated with significant morbidity and mortality. 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%. 9 c. Another US study reported an unadjusted in-hospital mortality rate of 29% for hospital-onset MRSA bloodstream infections occurring between 2012 and 2017. 7 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. 10 Risk factors for MRSA 1. MRSA HAI among colonized patients a. A substantial proportion of colonized patients will subsequently develop a MRSA infection such as pneumonia, soft-tissue infection, or primary bloodstream infection. [11][12][13][14][15][16] Among adults, this proportion has ranged from 9% to 33%. 17 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%. 11 Others have reported that among those who develop MRSA infections after discharge, these account for a substantial number of readmissions. 12 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  Highly confident that the true effect lies close to that of the estimated size and direction of the effect. Evidence is rated as "high" quality when there are a wide range of studies with no major limitations, there is little variation between studies, and the summary estimate has a narrow confidence interval.
Moderate The true effect is likely to be close to the estimated size and direction of the effect, but there is a possibility that it is substantially different. Evidence is rated as "moderate" quality when there are only a few studies and some have limitations but not major flaws, there is some variation between studies, or the confidence interval of the summary estimate is wide.

Low
The true effect may be substantially different from the estimated size and direction of the effect. Evidence is rated as "low" quality when supporting studies have major flaws, there is important variation between studies, the confidence interval of the summary estimate is very wide, or there are no rigorous studies.
Surveillance methods for MRSA and detection of patients with MRSA g. Leadership accountability and support in prioritizing resources needed to maintain a MRSA prevention program and implement effective interventions.

Section 4: Recommended strategies to prevent MRSA
Recommendations are categorized as either (1) essential practices that should be adopted by all acute-care hospitals or (2) additional approaches that can be considered in locations and/or populations within hospitals when MRSA transmission is not controlled by essential practices. Essential practices include recommendations in which the potential to affect risk for transmission or infection of MRSA clearly outweighs the potential for undesirable effects. Additional approaches include recommendations in which the intervention is likely to reduce MRSA risk but there is concern about the risks for undesirable outcomes, recommendations for which the quality of evidence is low, recommendations in which cost-to-benefit ratio may be high, and recommendations in which evidence supports the impact of the intervention in select settings (eg, during outbreaks) or for select patient populations. Hospitals can prioritize their efforts by initially focusing on implementation of the prevention strategies listed as essential practices. If MRSA surveillance or other risk assessments suggest ongoing opportunities for improvement, hospitals should consider adopting some or all of the prevention approaches listed as additional approaches. These can be implemented in specific locations or patient populations or can be implemented hospital-wide, depending on outcome data, risk assessment, and/or local requirements. Each infection prevention recommendation has been given a quality-of-evidence grade (  [72][73][74] Some observational studies have shown an increase in adverse events including increased depression, anxiety, falls, electrolyte disorders, and decreased patient satisfaction. 74,75 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. 63 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.
c. Evidence on the impact of discontinuation of contact precautions for MRSA-colonized and MRSA-infected patients: 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. [76][77][78] However, most were single-center, quasiexperimental 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. 79,80 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. 56 83 Thus, receipt of such antibiotics may increase the risk of infection in the colonized person and/or increase risk of transmission to others. 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. 84 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. [107][108][109][110] 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. 52 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. 111 129 iii. Decolonization also reduces MSSA colonization and infections in this population. 130-132 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. 132 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. 133 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. 135,136 Chlorhexidine-associated adverse events are infrequent, but many NICUs limit chlorhexidine use, especially in preterm infants within the first month of life. 125 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. 63 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). 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). 152 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 handhygiene 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-andglove use intervention, with additional but smaller effects from improved hand hygiene and lower HCP-patient contact rates. 56 ii. In a subsequent secondary analysis of data from this trial, the intervention was associated with a nonsignificant decrease in acquisition of antibiotic-resistant gramnegative bacteria (rate ratio, 0.90; 95% CI, 0.71-1.12). 153 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. Universal MRSA decolonization 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. 99 b. Additional study is needed to evaluate the role of routine universal decolonization of NICU patients. 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. 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. 115,154 b. Mupirocin resistance has been studied extensively; however, the ability of hospital laboratories to provide mupirocin resistance data is limited. 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). 155 The molecular mechanism of low-level mupirocin resistance involves point mutations and is mediated by plasmid encoded genes in high-level mupirocin. 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. 156 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. 154 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. 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.

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. 46 These recommendations are applicable to MRSA as well as other MDROs. That position paper describes the following MRSA outcome measures.
A. Basic outcome measures for all acute-care hospitals 1. MRSA-specific line lists (eg, electronic databases) for tracking patients who have MRSA; 2. Annual antibiograms for monitoring antimicrobial susceptibility patterns (eg, rates of methicillin resistance) among isolates recovered from patients; 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. Proxy measures of healthcare-acquisition of MRSA such as incidence (or incidence density) of hospital-onset MRSA based on clinical culture data.
B. Supplemental/advanced outcome measures for acute-care hospitals 1. Additional measures of the burden of healthcare-associated infection (eg, incidence or incidence density of hospitalassociated MRSA infections), 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. 46 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. 46 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.

Section 6: Implementation strategies
Accountability is an essential principle for preventing HAIs. It provides the necessary link between science and implementation. Without clear accountability, scientifically based implementation strategies will be used in an inconsistent and fragmented way, decreasing their effectiveness in preventing HAIs. Accountability begins with the chief executive officer and other senior leaders who provide the imperative for HAI prevention, thereby making HAI prevention an organizational priority. Senior leadership is accountable for providing adequate resources needed for effective implementation of an HAI prevention program. These resources include necessary personnel (clinical and nonclinical), education, and equipment. The information provided below is intended to assist hospitals with implementation of the essential and additional practices that they have selected for their infection prevention program. In addition to the examples provided below, please refer to the Appendix for a more detailed discussion of factors to consider during the implementation of MRSA AST and decolonization programs. Guidance for the implementation of an effective hand hygiene program is available in the Compendium document on strategies for optimizing hand hygiene. 159 Engage 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. 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. Engage executive leadership based on clinical outcomes data, public reporting requirements, and locally determined return on investment calculations.

Educate
1. Provide an educational program to foster desired behavior changes. Include a discussion of MRSA risk factors, routes of transmission, outcomes associated with infection, organizationspecific 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. 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. Provide evidence that supports the use of selected strategies. 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. 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. 159,160 MRSA monitoring program 1. A common detection strategy used by infection control programs to identify and track patients from whom MRSA has been isolated from any clinical or AST specimen includes a daily review of laboratory results to identify patients from whom MRSA has been isolated. b. Initial isolates as well as subsequent clinical infections should be classified as either hospital or community onset using prespecified definitions (see Section 2). c. In addition, patients known to be MRSA-colonized orinfected based on testing performed at another healthcare facility should be included in the line list. d. Additional information commonly contained in the line list includes the date of collection of specimens from which MRSA was isolated, site from which the specimen was obtained, and hospital location at the time of collection. e. Ideally, the line list is an electronic database generated from the organization's electronic health record, which can integrate relevant hospital data systems (eg, culture results, admissions, discharge, transfer (ADT) data, etc) to populate an electronic line list.

Contact precautions
1. Place patients in a single or private room when available. 2. Place patients who have MRSA in cohorts when a single or private room is not available. 3. Cohort placement does not eliminate the need for compliance with hand hygiene and other infection prevention measures between patient contacts. 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. HCP should have a thorough understanding of the benefits and potential adverse effects associated with the use of contact precautions. 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. 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. Establish institutional criteria for discontinuation of contact precautions. 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. 62,71 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. 61,161,162 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. 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. 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. 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 [163][164][165][166] Notably, these methods should be used as supplements to, but not as replacements for, routine cleaning and disinfection.

Active surveillance testing
Please refer to the Appendix for a more detailed discussion of the issues outlined below.
AST among patients 1. Select the patient population that will be included in the screening program (eg, all patients or only high-risk patients or patients on high-risk units). 2. Develop a reliable system to identify patients who meet the criteria for screening. 3. Determine how screening specimens will be ordered (eg, standardized nursing protocol, admission order set, individual patient order), who will initiate the order (eg, physician, nurse) and who will obtain the specimens (eg, unit-based nursing personnel, designated MRSA monitoring program personnel, patient). 4. Determine when screening will be performed (see Appendix). 5. Determine the anatomic sites that will be sampled. 6. Select the laboratory method that will be used to detect MRSA. 7. Determine how to manage patients while awaiting the results of screening tests 8. Assess the availability of single rooms and develop a plan and protocol for situations in which the number of single rooms is insufficient. 61 [175][176][177] it is important to be aware of these distinctions when screening programs are undertaken. Different infection prevention strategies may be more impactful if the HCP is the primary or secondary source of transmission. 2. Often, staff will be concerned about the interpretation of a positive test and whether it will identify them as the source of an outbreak. Often, the pressing goal is to contain transmission, and not to distinguish between primary and secondary sources. Conveying to staff the goal of containment over source identification can be helpful in HCP screening programs in which positive carriers are decolonized to prevent transmission to other HCP or patients regardless of the source. 3. Estimating source determination is increasingly possible due to genomic advancement. However, the goal should be to enhance practices of infection prevention to prevent spread from an ongoing common source. 4. Determine how and when to collect specimens for testing. 5. Select the laboratory method that will be used to detect MRSA. 6. Determine how to manage personnel who are identified as an ongoing primary or secondary source of MRSA transmission.

Decolonization therapy
1. Conduct a risk assessment to identify populations with high rates of MRSA infection that might benefit from decolonization. 2. Determine whether targeted or universal decolonization will be utilized. a. Targeted decolonization includes AST to identify colonized individuals followed by decolonization for those with MRSA colonization. b. Universal decolonization avoids testing and provides treatment to the entire at-risk population. This approach may provide added benefit of reducing MSSA disease in addition to MRSA disease, and it may help address concern that a single screening of limited body sites is insufficient to identify all MRSA carriers. 3. Select a decolonization regimen. (Note: Decolonization regimens typically include a combination of nasal and skin antisepsis.) 4. Consider developing standardized or protocol-based order sets to optimize compliance.
5. Standardize care processes. 6. Ensure adequate supplies of products used for decolonization (eg, chlorhexidine bottles or cloths) to reduce barriers to implementation. 7. Review chlorhexidine compatibility of patient hygiene and skincare products and remove incompatible products that are used on the body below the neckline. 8. HCP responsible for implementing MRSA decolonization programs should receive competency-based training with return demonstration for the application of intranasal antimicrobials or antiseptics and topical CHG. 178   Competing interests. The following disclosures reflect what has been reported to SHEA. To provide transparency, SHEA requires full disclosure of all relationships, regardless of relevancy to the guideline topic. Such relationships as potential conflicts of interest are evaluated in a review process that includes assessment by the SHEA Conflict of Interest Committee and may include the Board of Trustees and Editor of Infection Control and Hospital Epidemiology. The assessment of disclosed relationships for possible conflicts of interest has been based on the relative weight of the financial relationship (ie, monetary amount) and the relevance of the relationship (ie, the degree to which an association might reasonably be interpreted by an independent observer as related to the topic or recommendation of consideration. consider identifying a specific day of the week when specimens will be collected. This will simplify the process and allow the microbiology laboratory to anticipate the increased volume of specimens and plan staffing and supplies accordingly. 5. Determine the anatomic sites that will be sampled. a. The sensitivity of surveillance specimens obtained from a variety of anatomic sites has been evaluated in several settings and patient populations. Although no single site will detect all MRSA-colonized persons, most studies have found the anterior nares to be the most frequently positive site, with sensitivity ranging from 48% to 93%. 194,[196][197][198][199][200] Because of this and the accessibility of the site, the anterior nares have generally been considered to be the primary site for sampling in MRSA screening programs. However, collection of samples from other sites, such as skin (groin, perineum, wounds), foreign body (eg, gastrostomy or tracheostomy tube) exit sites, throat, and the perianal area, will allow identification of additional colonized patients that would not be identified by nasal specimens alone. Several recent studies have demonstrated that sampling from 1 or more additional sites, such as the throat and/or perineum, was required to increase the sensitivity of AST to >90%. 194,196,198,199 b. The neonatal ICU has a number of unique features that should be considered when planning an AST program for that setting. 24 For management of MRSA outbreaks in NICUs, nares samples alone may be sufficient to detect MRSA-colonized neonates, 164 but a sampling strategy that includes collection of specimens from other sites, such as the umbilicus, may have greater sensitivity for detection of MRSA than sampling the nares alone. 125,201 c. To simplify the specimen collection procedure and optimize resource utilization, some hospitals performing multisite sampling use a single swab to collect specimens from multiple sites (eg, nose, axillae, and groin). 166 When using molecular-based testing methods, confirm with laboratory personnel that the test has been validated for use with all sampling sites.
6. Select the laboratory method that will be used to detect MRSA. a. MRSA can be detected using culture-based methods or molecular diagnostic testing methods, such as polymerase chain reaction (PCR). Many factors must be considered when determining which laboratory method(s) will be used in a MRSA screening program. These factors include but are not limited to performance characteristics of the test (eg, sensitivity, specificity), batch testing, turnaround time, capabilities of the laboratory that will be providing the service (whether an in-house or reference lab), number of specimens that will be processed, and facility-specific costbenefit calculations. b. A detailed discussion of the various laboratory methods for MRSA detection is beyond the scope of this guideline, but some of the key features of the most common methods are discussed below. i. Culture-based methods: Numerous microbiologic media and culture techniques have been described for use in the detection of MRSA colonization. One of the more commonly used selective media is mannitol salt agar (MSA) with or without antimicrobial (eg, oxacillin or cefoxitin) supplementation to increase specificity for methicillin-resistant organisms. The time required for detection of MRSA is ∼48 hours using most culturebased techniques. Several chromogenic agar media have been developed that allow more rapid detection of MRSA than conventional media, usually within 24 hours. Studies using established collections of isolates and clinical specimens have shown that these chromogenic media rival or outperform more conventional microbiological techniques. [202][203][204][205][206][207][208] Additional enrichment steps, such as overnight incubation in trypticase soy broth, can further increase the yield of standard and chromogenic culture-based methods. [209][210][211] ii. Molecular testing methods: In recent years, there have been advances in molecular diagnostic testing methods, such as real-time PCR, for detection of MRSA. Earlier evaluations of these PCR assays found them to be highly sensitive (90%-100%) and specific (91.7%-98.4%) compared to standard culture-based methods. [212][213][214][215] Although more costly than culture-based techniques, one potential advantage of these molecular tests is their ability to provide a result in <2 hours from the time of specimen collection, although in actual practice the turn-around time may be longer due to batching of samples. At least 1 uncontrolled study 216 and 3 mathematical models [217][218][219] have suggested that rapid testing may allow for more effective use of contact precautions and enhanced prevention of MRSA transmission. However, a cluster randomized crossover trial of universal screening in general wards failed to identify a difference in MRSA acquisition rates with the use of rapid testing as compared with the use of a culture-based method. 52,[220][221][222] These data suggest that the clinical and economic benefits of rapid testing may vary among individual hospitals and settings. 7. Determine how to manage patients while awaiting the results of screening tests. 57 a. Before implementing a screening program, a decision should be made regarding how a patient will be managed while waiting for the result of the admission MRSA screening test.
There are 2 common approaches: (1) await the test result and implement contact precautions only if the screening test is positive or (2) place the patient on empiric contact precautions until a negative admission screening test result is documented. i. It has been shown that patients colonized with MRSA often contaminate the hospital environment prior to the availability of AST results. 57 Thus, empiric use of contact precautions could minimize the risk of MRSA transmission from unrecognized sources, and some have suggested that this approach has contributed to more effective control of MRSA. 189 However, several logistical difficulties may be associated with this approach. Empiric use of contact precautions substantially increases the need for single rooms and the quantity of supplies needed to practice contact precautions. When only a small proportion of screened patients are colonized with MRSA and single rooms are of limited quantity, a large number of patients whose screening test results are negative will need to be moved so that their single room can be used for another patient. These room reassignments and the necessary cleaning before the vacated room can be reoccupied can impede patient flow within the hospital. In many acute-care hospitals, implementing contact precautions at the time of receipt of a positive screening test result is a reasonable initial approach. The empiric use of contact precautions for all tested patients while awaiting test results may be most feasible in hospitals where a relatively large proportion of screened patients are MRSA-positive or where a large proportion of patient rooms are single rooms and in individual hospital units, such as many ICUs, where each patient is in an individual room or bay. ii. Despite its potential logistic difficulties, empiric use of contact precautions should be considered if transmission continues despite introduction of a screening program in which contact precautions are implemented only after a positive MRSA screening test.
AST among HCP 1. Determine how and when to collect specimens for testing. a. Consideration should be given to testing epidemiologically linked personnel when transmission continues despite implementation of basic control measures. b. Data on optimal anatomic sites for screening among HCP are not readily available. There is no evidence to suggest that anatomic screening sites among personnel should be different than those sampled in patients for the purpose of detecting colonization (See Appendix). In many published reports of MRSA outbreak investigations that included AST of HCP, the nares were sampled to detect colonization. Some reports have cited sampling of other sites, either alone or in addition to the nares, including the fingertips, skin (areas of dermatitis), the perineum, and pharynx. 223 c. The timing of collection of screening specimens may affect the results of HCP screening. Screening during or at the end of a work shift may identify transiently colonized HCP in addition to persistently colonized HCP who may be a source of ongoing transmission. 224 Thus, collection of specimens at the beginning of a shift or after several days away from the clinical setting may optimize the specificity of testing. d. When screening HCP for outbreak control, consider having occupational health staff inquire about or directly evaluate HCP for areas of dermatitis or any skin breakdown or wounds because these symptoms have been associated with ongoing sources of transmission, both primary and secondary. Convenience, efficiency, privacy, and comprehensive surveillance should be considered when determining whether screening occurs in a designated private location near an affected unit or work site versus in the occupational health department. 2. Select the laboratory method that will be used to detect MRSA.
a. When choosing between culture-based vs molecular based MRSA tests, be sure to evaluate whether organisms are needed for further testing, such as sequencing for clonality. Considerations regarding optimal laboratory tests for detection of MRSA carriage include the following: i. Molecular testing (eg, pulse-field gel electrophoresis or whole-genome sequencing) to establish clonality of MRSA isolates and determine whether patient isolates and isolate(s) obtained from HCP are related has been useful in some investigations. 63,146,172,[225][226][227] ii. Whole-genome sequencing can be integrated into outbreak investigations along with epidemiologic data to improve understanding of MRSA transmission. 228 3. Determine how to manage personnel who are identified as an ongoing primary or secondary source of MRSA transmission. a. Develop a facility policy to manage HCP who are either infected or colonized with an outbreak strain of MRSA in a standard fashion. Most published reports of MRSA transmission from colonized HCP have indicated that transmission was interrupted after the introduction of several simultaneous interventions. 174,223 No controlled studies have examined the specific impact of isolated interventions on interrupting HCP to patient transmission of MRSA. Thus, there are no evidence-based recommendations for managing MRSA-colonized HCP who have been associated with ongoing MRSA transmission within a healthcare facility. b. Consideration of the MRSA-colonized HCP's specific jobrelated activities may help to determine the course of action.
Interventions that may be considered include the following: i. Evaluate the MRSA-colonized HCP's infection prevention practices for opportunities for education and improvement. For example, in one report, an HCP with chronic sinusitis linked to a cluster of MRSA cases was identified as a carrier of the outbreak strain, and breaches in recommended infection control practices were identified. 173 ii. Ensure appropriate treatment of active MRSA infection. iii. Decolonization therapy may be considered for personnel with persistent MRSA colonization. Refer to Section 4 (Additional Strategies) and to the "Implementing Decolonization Therapy Programs" information below for further details on decolonization therapy. c. Work restrictions: HCP work restrictions have been used as a part of outbreak management in some, but not all, reports. Work restrictions include approaches such as furlough, restriction from patient care activities, and temporary reassignment. Work restrictions have been used for some, but certainly not all, MRSA-colonized HCP who have been infants or infants under 2 months old; these products may cause irritation or chemical burns." Concerns in children aged <2 months old include skin irritation and systemic absorption following topical exposure, events that may be more likely in preterm infants in the first month of life. 136 e. Provide physical barriers to prevent chlorhexidine solution from depositing onto linens to minimize staining when linens contact bleach oxidizers during commercial laundering. f. If the decolonization regimen will include intranasal application of mupirocin, determine how mupirocin will be provided (eg, in single-dose or multidose tubes).