mrsa control in the hospital setting and transmission...

What is MRSA?

Methicillin-resistant S. aureus (MRSA) is a type of Staphylococcus aureus

(staph) that is resistant to most antimicrobials. MRSA first emerged in a

hospitals and became known as hospital acquired (or associated) MRSA,

HA-MRSA. In recent years, there was a major change in the

epidemiology of MRSA, where MRSA cases appeared in the community,

affecting people with no direct connection to hospitals. This MRSA

lineage is known as community acquired (or associated) MRSA, CA-

MRSA. As well, a third lineage appeared in pets and livestock animals,

referred to as livestock acquired (or associated) MRSA, LA-MRSA. All

three lineages stem from the original HA-MRSA and it is becoming more

difficult to distinguish among them.

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MRSA Control in the Hospital Setting and Transmission Among Species: Executive Summary

About the Literature Review

This review spans across two areas of research:

Best practices to control and eradicate nosocomial MRSA in the ICU, and

Human –animal transmission of MRSA.

Methods Used to Obtain Journal Articles

Two independent searchers were conducted using the MEDLINE, PUBMED, Web of Knowledge, and the Cochrane Library electronic databases. The U of S Health Science librarian was consulted to obtain the relevant search keywords.

In total 326 relevant articles from 2008 to present were retrieved:

183 for the first search topic,

143 for the second topic.

The titles and abstracts were read carefully to select 40 most relevant articles for each topic. The selected articles were read carefully and selected further for the literature review. In total the literature review used 50 journal articles.

Best Practices to Control and Eradicate HA-MRSA

The most effective intervention implemented to control MRSA is the

“MRSA bundle.” It encompasses pre-existing Centre for Disease Control

and Prevention guidelines and consists of:

Universal surveillance,

Contact precautions,

Hand hygiene,

Environmental control, and

Cultural transformation (safety culture).

Implementation of the bundle as a whole is effective in reducing the HA-MRSA rates. Application of MRSA bundle in Veteran Affairs (VA) hospitals nationwide resulted in up to 79% decrease in bloodstream MRSA infection and a 75% decrease in rates of pneumonia related to a device, urinary tract, skin and soft tissue infections.

Although the implementation of the bundle as a whole shows to be most effective, the current literature indicates that this is rarely done. Typically, one or several components are selectively employed and reported. As well, there are inconstancies in how these interventions are implemented and reported making it difficult to compare across studies and finings.

Therefore, the following section provides a summary of the main findings from the literature review for each bundle component.

http://www.usask.ca/vpresearch/our_office/assocvphealth/about-avp-health.php

Surveillance

According to the guidelines of the MRSA bundle, all patients being admitted, transferred, or discharged should be screened for MRSA and the result should be communicated in a timely fashion. The literature on this topic is mixed and some studies question the practicality of surveillance. Findings show that surveillance alone does not directly relate to decreased nosocomial MRSA rates, even though more MRSA-positive patients are detected. Cost-benefit analyses indicate that active targeted surveillance would be most effective. Other findings show that no surveillance, but universal patient decolonization is most effective.

Contact Precautions

Literature on the impact of contact precautions and isolation is also mixed and drawing any substantial conclusions would be presumptuous. The MRSA bundle recommends that all patients prior to their test results or who are MRSA-positive should be treated with precautions and assumed to be a possible threat.

Hand Hygiene

Hand hygiene is considered to be a cornerstone of mitigating nosocomial transmission. Studies suggest that although it is essential to ensure hand hygiene precautions are maintained, it is not the “magic bullet” answer in controlling nosocomial MRSA. In addition to healthcare provider hand hygiene, patient and visitor hand hygiene protocols should be considered as literature indicates reduced nosocomial transmission when such protocols are implemented.

Environmental Control

Environmental control has emerged as an essential part in the control of the nosocomial infection with MRSA. MRSA has been isolated on various surfaces in hospitals. Also patients have a higher rate of infection with MRSA when occupying a room previously occupied by an MRSA-positive patient. Furthermore, maintaining strict environmental cleanliness regimen has reduced infections with other pathogens in addition to MRSA.

Cultural Transformation

The cultural transformation is considered to be the most crucial in the successful implementation of the bundle or any other prevention. Staff compliance may be difficult to attain, but frequent follow up and frontline leadership engagement have been effective.

Review of MRSA Bundle Components

Transmission of MRSA between Humans and Animals

MRSA transmission between humans and animals is wide-spread and involves animals for food production and pets. The main source of transfer is either direct or indirect contact. Pets become infected with MRSA from their owners, veterinary clinics, and hospitals. The strains isolated from these pets are typically undistinguishable from their human contacts. It is accepted that pets become infected from their colonized owners and pass MRSA back to humans. MRSA has been reported in farm animals including cows, pigs, goats, sheep, chickens, and horses. Pigs have shown to carry a specific MRSA clone, CC398, readily found in North America and Europe, but this clone has now been reported in other species including wild animals with direct contact to MRSA-positive farms. As well, increased rates of MRSA and the CC398 strain have been reported in slaughterhouses and sampled retail meat. The CC398 strain is transmitted between animals and humans and has been linked with outbreaks in hospitals. However, it appears that CC398 does not easily transmit between humans and the outbreaks, so far, are limited compared to the traditional hospital acquired strains. None the less, there is a growing concern that LA-MRSA shows high adaptability and poses an increased risk in public health and nosocomial MRSA infections.

MRSA: Best practices in control within hospitals and colonisation among species

Literature Review

Office of the Associate Vice-President Research – Health (U of S)/ Vice-President Research and Innovation (SHR)

Prepared by: Izabela Szelest

Date: October 28, 2013

Office of the Associate Vice-President Research - Health MRSA Literature Review

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General Introduction

Staphylococcus aureus, commonly known as “staph”, is a wide-spread pathogen which may cause a variety of infections extending from superficial skin and soft tissue infections to life-threatening endocarditis, toxic-shock syndrome, and necrotizing pneumonia (Verkade & Kluytmans, 2013). Methicillin-resistant strand of S. aureus (MRSA) was identified shortly after the introduction of penicillin in the mid-1960s and has been recognized as a predominantly hospital-associated pathogen (aka, HA-MRSA). In the mid-1990s another wave of MRSA emerged in individuals with no association to healthcare and this type was referred to as community acquired (CA)–MRSA. Finally, a third type, (LA)-MRSA, has been isolated in animals, mainly livestock, with the first reported sighting in cases of bovine mastitis. LA-MRSA has now been reported in numerous species including pigs, horses, goats, and various poultry (for review see Crombé et al., 2013). These three types of MRSA strains vary based on their accessory genome, the populations they infect, and clinical symptoms (Crombé et al., 2013).

Although the three MRSA lineages show distinct characteristics, they all contain human origin and are becoming more difficult to distinguish. Clones with a typical HA genetic background enter the community and clones with CA genetic background have been found in hospital settings (see Crombé et al., 2013 for review). The same is true for the LA strains, especially the clone commonly referred to as CC398 (or ST398), which in addition to livestock animals has now been reported in humans (for review see Crombé et al., 2013). Furthermore, this clone has been linked to MRSA outbreaks in some hospitals resulting in severe patient illnesses (Verkade & Kluytmans, 2013) highlighting the emerging threat of non HA-MRSA strains on human health in healthcare settings (Köck et al., 2011).

This literature review is a compilation of recent publications from two distinct areas of research. The first area focuses on the best-practices used to control and eradicate hospital acquired (HA)-MRSA and is presented first in the review. The second area focuses on the MRSA prevalence and transmission between humans and animals (and vice-versa) and is presented second. Although the prevalence of MRSA in long-term care and nursing homes was not part of this review, the literature in both areas draws attention to the importance of this issue. Elderly people admitted to the ICU (Intensive Care Units) from nursing homes have shown to be a major risk factor in transmitting nosocomial MRSA. Also, this population has been linked with the transmission of MRSA between humans and pets. Therefore, considering the significant older population living in Saskatchewan, a brief summary was also included.

Best practices in control and eradication of hospital acquired methicillin-resistant Staphylococcus aureus (HA-MRSA)

The Centre for Disease Control and Prevention as well as the Association for Professionals in Infection Control and Epidemiology (APIC) have recognized the implementation of multiple interventions, known as the “MRSA bundle,” as the most effective practice to control or eradicate nosocomial MRSA in the ICU (Camus et al., 2011). Based on published guidelines, the MRSA bundle is a quality-improvement program, which uses applications from the Toyota Production System approach (Jain et al., 2011) and consists of the following components:

Universal active surveillance;

Contact precautions for patients who are carriers of MRSA or tested as MRSA-positive;

Hand hygiene before and after patient contact;

Environmental decontamination (Pennsylvania Patient Safety Advisory); and

Cultural transformation where infection control becomes the responsibility of everyone who have

contact with patients (Bonuel, Byers, & Gray-Becknell, 2009; Agency for Healthcare Research

and Quality).


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In 2001, the MRSA bundle was first implemented as a pilot project in the acute care Veterans Affairs (VA) Pittsburgh Healthcare System. Due to the success of this pilot, in 2007, the MRSA bundle was implemented in all VA hospitals nationwide and published in The New England Journal of Medicine (Jain et al., 2011). The data was gathered between October 2007 and June 2010 from the 153 VA hospitals. In total, 196 medical, coronary care, and surgical ICUs, as well as 428 medical, surgical, rehabilitation medicine, and spinal cord injury units provided the data. This resulted in an analysis of 1,934,598 admissions to, transfers within, or discharges from these units and 8,318,675 patient days. The summary of reported findings includes the comparison between the initial and end stages of implementation for each tracked indicator in ICU and non-ICU settings. Overall, the findings show a substantial decrease in the transmission and infection with MRSA in most of the indicators:

Initial rate (per 1000

patient-days)

End rate (per

1000 patient-days)

% change

Stat sig

(p)

ICU

Bloodstream MRSA infection not related to a device

0.14 0.03 -79% <0.001

Rate of pneumonia related to a device 0.32 0.08 -75% <0.001

Urinary tract infection 0.16 0.04 -75% <0.001

Skin and soft tissue infections 0.16 0.04 -75% <0.001

Ventilator associated MRSA pneumonia 1.17 (device days)

0.33 -72% <0.001

Rate of healthcare associated MRSA infection 1.64 0.62 -62% <0.001

Quarterly rate of bloodstream MRSA infection related to device

0.16 0.06 -62% <0.001

Quarterly rate of pneumonia not related to a device

0.35 0.22 -37% =0.001

Bloodstream MRSA infection associated with central venous catheters

0.46 0.31 -33% <0.001

Rate of transmission in the ICU 3.02 2.5 -17% <0.001

Rate of patient-days in the ICU on which mechanical ventilation was received to the total number of patient-days in the ICU

0.29 0.25 -14% =0.005

Rate of patient-days in the ICU on which central venous catheters were used to the total number of patient-days in the ICU

0.46 0.44 No

change =0.75

non-ICU


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Rate of blood stream infection 0.12 0.05 -58% =0.11

Skin and soft-tissue infections 0.15 0.07 -53% =0.009

Rate of health care associated MRSA infection 0.47 0.26 -45% <0.001

Urinary tract infection 0.09 0.05 -44% =0.43

Pneumonia 0.08 0.05 -38% 0.02

Rate of transmission in non-ICU 2.54 2.0 -21% <0.001

Adapted from Jain et al., 2011.

The effectiveness of this bundle shows substantial sustainability when implemented. Recently, Evans, et al. (2013) reported in a follow up study which used the same indicators as reported by Jain et al., 2011. However, the time period considered was from July 2010 to June 2012. The findings showed a maintained reduction in MRSA transmission in ICU and non-ICU setting. Taken together, the VA initiative has been sustained for over 57 months in a large national health care system and shows to be exceptionally effective.

Although the implementation of the MRSA bundle has shown significant declines in MRSA transmission, the literature indicates that it is rarely applied in its entirety. What seems to be common is that selected components of the bundle are investigated either in isolation or in a combination of selected interventions. One of the most common combinations includes surveillance, patient isolation and hand hygiene intervention. Therefore, the subsequent sections of this review focus on each of the MRSA bundle components and their effectiveness in battling MRSA transmission and control in a hospital. Generally, these components show to be most effective when implemented with other interventions. It is important to note that the studies have also shown a substantial variability in how the data from these interventions is reported, making the results difficult to interpret. Therefore, only general conclusions can be comfortably derived.

Surveillance (Screening)

This section evaluates the practices and effectiveness of patient screening for MRSA. Overall, the literature shows universal screening of patients is recommended as part of the MRSA bundle guidelines. However, the effectives of this intervention alone is highly debated as despite the fact that more patients are recognized to be MRSA-positive, this method alone does not lead to reduced infection rates.

Early identification of patients with MRSA can potentially trigger the use of necessary infection control strategies, thus justifying the implementation of varying early screening methods. In fact, according to the protocols outlined in the “MRSA bundle”, active surveillance for MRSA should be conducted on every admitted, discharged, or transferred patient (Pennsylvania Patient Safety Advisory). The swabbing for MRSA can be done solely to the nostrils (Bonuel, 2009; Holzmann-Pazgal et al., 2011; Karas, Enoch, Eagle, & Emery, 2009) or at multiple sites, including the groin (Camus et al., 2011; Huskins et al., 2011; Karas et al., 2009; Rodríguez-Baño et al., 2010). Positive test results should be relayed to the unit staff in a timely fashion (Bonuel, 2009), informing the staff to maintain the heightened contact precaution or to implement standard precautionary contact protocols.

The screening of patients upon their arrival to the intensive care unit undoubtedly increases the detection rates of MRSA as compared to no screening. For example, Kohlenberg, Schwab, Behnke, Geffers, and Gastmeier (2011) using a questionnaire evaluated the association between MRSA


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incidence densities and the use of three screening methods in 186 ICUs in Germany: the universal admission screening, targeted screening of risk patients, and no specific screening procedures. In addition to screening, different isolation methods were implemented, including single-room, pre-emptive and decolonization. The findings revealed that ICUs with universal screening upon admission were able to identify MRSA cases more often than ICUs performing targeted or no screening procedures. Similarly, Rymzhanova, Thouverez, Talon, and Bertrand (2009) also concluded that adding weekly MRSA screening to already established admission and clinical sampling increased MRSA detection rate which would have otherwise remained undetected. Finally, Jain et al. (2011) reported that active surveillance is capable of identifying more than 90% of MRSA carriers who enter the ICU. This indicates a significant number of patients who could be colonized with MRSA without any present symptoms and highlights the effectiveness of MRSA detection using comprehensive screening techniques (Jain et al., 2011).

Practicality of screening for MRSA

Implementation of comprehensive screening techniques requires substantial logistical and financial resources which smaller hospitals may not have at their disposal (Kohlenberg, et al., 2011). Overall, the literature of the efficacy of patient screening for MRSA indicates an implementation of various protocols followed by various isolation and eradication methods. These interventions are reported inconstantly making any substantial conclusions difficult to make (Halcomb et al, 2008). What shows to be consistent, however, is that screening alone may not be an effective method in controlling nosocomial MRSA infections. For example, Sakamoto, Yamada, Suzuki, Sugiura, and Tokuda (2010) showed in their time-series study that active surveillance was not sufficient to control the spread of MRSA even though it has been practiced at the test facility since the 1980s. In another study, Huang, Lien, Su, Chou, and Lin (2011) reported that surveillance did not correlate with the reduced rates of hospital acquired infections in a seven-year campaign to control MRSA in a neonatal ICU, where MRSA was considered to be endemic.

Substantial success in the reduction of nosocomial MRSA has been reported when, in addition to screening, a combination of other bundle protocols was implemented, including hand hygiene (Sakamoto et al., 2010), patient isolation and cohorting (Kok, O’Sullivan, & Gilbert, 2011), contact isolation (Holzmann-Pazgal et al., 2011), and decolonization (Karas et al., 2009). Conversely, failure to implement these components showed limited effects in reducing nosocomial MRSA transmission. For example, Kellie, Timmins, and Brown (2011) in a statewide implementation of the Active Surveillance Testing (AST) and the MRSA bundle in urban and rural hospitals of New Mexico, reported a non-significant decrease of MRSA rates from 0.79 to 0.41 per 10,000 patient days. The access to data, initial cost of AST, attitudes of administrators, physicians, and staff, and lack of adherence to contact precautions formed substantial barriers affecting the results. A similar conclusion was reached by Kok et al. (2011) who reported that, in addition to targeted active surveillance, hand hygiene and adherence to contact precautions by all staff are essential to decrease transmission of MDROs including MRSA.

Screening for MRSA and subsequent decolonization using intranasal mupirocin and chlorhexidine bathing multiday regimen has been implemented as a method of controlling nosocomial MRSA transmission (for examples see: Huang et al., 2013; Lucet & Regnier, 2010; Rodríguez-Baño et al., 2010; Karas et al., 2009). The successful reduction of MRSA colonization rates in an inpatient population was reported by Karas et al., (2009), where a systematic decolonization of MRSA carriers occurred, in addition to random colonization surveillance, over a five-and-a-half-year period. The rates of colonization decreased the most in an intervention where beds in targeted wards were screened randomly on a regular basis, all MRSA cases were decolonized, and all 65-year-old emergency patients were screened and begun decolonization treatment even prior to the test results.


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An impressive three-group, random control trial study, published in the New England Journal of Medicine, directly compared the effectiveness of targeted vs. universal decolonization to prevent MRSA infections in the ICU (Huang et al. 2013). In total 43 hospitals were randomly assigned to three groups:

Group 1: Screening and isolation (no decolonization);

Group 2: Targeted decolonization (i.e. screening, isolation, and decolonization of MRSA

carriers); and

Group 3: Universal decolonization (i.e. no screening, isolation, and decolonization of all patients

with intranasal mupirocin and chlorhexidine bathing).

In total, there was a 44% reduction in bloodstream infections from MRSA and a 37% reduction of MRSA-positive clinical cultures in the third group. These results showed that universal decolonization, with no screening, was more effective in reduction of MRSA-positive clinical cultures than targeted decolonization, or screening and isolation (Huang et al., 2013).

The literature reporting cost-benefit analysis of MRSA screening is unsatisfactory and sparse (Gould, Reilly, Bunyan, & Walker, 2010). Overall, there is an indication that admission surveillance cultures and barrier precautions of MRSA-positive patients may be effective and cost-efficient, but there has not been a strong, well designed, and robust intervention to report this observation. A study that comes closest is a modeling of 800-bed academic hospital with 40,000 annual admissions (Kang, Mandsager, Biddle, & Weber, 2012). The researchers modeled the cost-effectiveness of universal surveillance screening for all patients, targeted surveillance screening of ICU patients, and no surveillance screening. The results of the model showed that if the hospital was unwilling to pay more than $71,300 per MRSA HAI prevented, then the targeted surveillance screening was the most cost-effective approach. It cost the least and prevented the most MRSA infections. As well, targeted screening showed to be cost effective when there was a reduction of nosocomial infections by at least 21%. However, if the hospital was willing to pay more than the $71,300, then the universal strategy showed to be most cost-effective. Overall the authors indicate that according to this model, targeted strategy is cost saving, compared with no surveillance and is cost-effective when compared to the universal screening strategy (Kang et al., 2012).

Taken together, identifying MRSA-carriers as soon as they are admitted to the unit may lead to higher detection rates, but it appears that screening alone may not have much effect on reducing the rates of transmission. In fact, the implementation of surveillance and decolonization may reduce the rates of MRSA colonization; however, there is a concern that individual decolonization alone may not be effective in the long-term. Re-infection may take place and multiple cycles of decolonization may increase the risk of MRSA resistance to mupirocin (Lucet & Regnier, 2010). Hence, an integration of other processes in addition to decolonization, such as contact precautions, hand hygiene, and environmental control (introduced in a later section) must also take place in order to reduce the colonization and transmission of MRSA. Therefore, as some data suggests, a universal approach, rather than MRSA specific, may make the most impact on reducing MRSA and other pathogens. Conversely, a haphazard implementation of the bundle may show only limited success regardless of how thorough the surveillance may be (Kellie et al., 2011).

Contact Precautions/ Isolation

The literature on the efficacy of patient isolation and contact precautions as a sole factor contributing to the spread of MRSA is limited.

As part of the MRSA bundle, once the patient is admitted or has been recognized to be MRSA-positive (either colonized or infected), isolation and contact precautions are implemented (Pennsylvania Patient Safety Advisory). These precautions are applicable to staff and include wearing gowns and gloves when providing care and masks if the patient has MRSA pneumonia. Red tape is strategically placed


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on the floor in the patient’s room to alert the staff and visitors that contact precautions are in place. Furthermore, visitors are instructed to adhere to hand hygiene protocols on entry and exit to the patients’ room, but are not typically required to wear gowns and gloves (Pennsylvania Patient Safety Advisory).

Typically, contact precautions and isolation is embedded in other interventions such as hand hygiene or patient screening. There is evidence supporting and refuting the efficacy of isolation protocols. For example, Hansen et al. (2010) reported a significant association between lower MRSA prevalence and patient isolation in single rooms with an effective use of alcohol-based solutions for hand hygiene in Finland and Sweden. Conversely, in a large study published in the New England Journal of Medicine, Huskins et al. (2011) showed no difference in incidence of MRSA and VRE colonization rates between a group where active surveillance and barrier precautions were used, as compared with control where existing hospital practice was implemented. Although this study reports interesting results relating to the importance of patient screening and isolation protocols, it should be considered with caution as the authors indicated several variables, which could have given the null results, including the short intervention period and decreased staff compliance with contact precautions protocols (Huskins et al., 2011).

Hand Hygiene

Aggressive hand hygiene protocol should be a cornerstone in pathogen prevention efforts (CDC website http://www.cdc.gov/HAI/prevent/prevention_tools.html). As part of the intervention, the following should be ensured:

Easy access to soap and water or alcohol-based hand gels;

Education for healthcare personnel and patients;

Observation of practices especially around high-risk procedures and before and after contact

with colonized or infected patients; and

Regular timely feedback on rates, failures, and improvements in hand hygiene performance

(http://www.cdc.gov/HAI/prevent/prevention_tools.html).

In addition to rigorous hand hygiene protocols for staff, hand hygiene protocols should also be developed and implemented for visitors (Pennsylvania Patient Safety Advisory).

The implementation of effective hand hygiene protocols, whether through the availability of hand washing stations or alcohol-based hand sanitizers, in patients, staff, and visitors has been linked with the reduction of MRSA rates (Mears et al., 2009; Sakamoto et al., 2010). A significant association between lower MRSA prevalence, the use of alcohol-based solutions and MRSA-patient isolation was established in countries such as Finland and Sweden. Furthermore countries with decreasing rates of MRSA such as France and Slovenia, have been linked with an increased availability of hand sanitizers (Hansen et al., 2010).

The extension of hand hygiene protocols to all patients and visiting relatives has shown to reduce MRSA infections by as much as 51% (Gagné, Bédard, & Maziade, 2010). A year-long (2003-2004) hand hygiene intervention was implemented at a Canadian hospital where all patients and visiting relatives were supervised to clean their hands twice a day of every weekday (not the weekend due to staff availability). As well, the patients and visitors were taught about the benefits of proper hand hygiene and given a brochure about nosocomial infections. The indicators considered in the study and their corresponding infection rates are summarized in the table below:

http://www.cdc.gov/HAI/prevent/prevention_tools.html

http://www.cdc.gov/HAI/prevent/prevention_tools.html


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Adapted from Gagné et al., 2010.

Although successful implementation of and adherence to hand hygiene protocols were shown to have a substantial impact on the reduction of MRSA infections in the hospital, in isolation it is not the “magic bullet” solution. Concurrent infection control practices are essential to influence nosocomial MRSA infection rates as indicated by McLaws et al., (2009). The findings, indeed, showed an increased rate in hand hygiene compliance and a reduced rate of infection. However this reduction mirrored the nation-wide data and cannot be assumed as a result of the implemented hand hygiene intervention. Furthermore, Hitoto et al. (2011), assessed the impact of hand hygiene compliance by staff who was notified which patients were MRSA carriers and non-carriers. The results showed that although the staff was aware who the MRSA-positive patients were, it did not increase the compliance with hand hygiene protocols. Taken together, this data shows that implementation of hand hygiene protocols will not necessarily result in decreased rates of MRSA infection and other interventions are required for a holistic control of the MRSA transmission, which can circumvent the lack of compliance for a particular protocol.

Environmental decontamination

As indicated above, screening, contact precautions, and hand hygiene protocols help mitigate the spread of pathogens and hence nosocomial infections; however, they do not eliminate it completely (Carling, Parry, Bruno-Murtha, & Dick, 2010). It has been well established that pathogens, such as MRSA and VRE are readily transmitted from environmental surfaces to healthcare workers’ hands (see Carling et al., 2010). Therefore, implementing only hand hygiene or contact precautions will decrease the spread of MRSA, but the contamination of the environment with such pathogens will not allow for a complete elimination from the hospital unit. Overall, the findings indicate room cleanliness as an emerging essential component in the control of the nosocomial MRSA as well as other pathogens found in the hospital.

It has been shown that patients admitted to rooms previously occupied by individuals infected or colonized with MRSA are at a significant risk of acquiring these organisms (Carling et al., 2010; Datta, Platt, Yokoe, & Huang, 2011). Squeri, Grillo, and La Fauci (2013) collected samples from the hands of


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the health workers and select workplace surfaces, and found MRSA on only 14.7% of the hands of the 235 tested workers. More importantly, MRSA was detected on 35.7% of the tested surfaces including medication trolleys, door handles, and telephones situated in treatment rooms, operating theatres and wards, highlighting the importance of environmental cleanliness even in comparison to hand hygiene protocols. Therefore, it has been “highly recommended” that hospitals “ensure compliance by housekeeping staff with cleaning and disinfecting procedures” (see Carling et al., 2010).

To highlight the importance of surface cleanliness, Goodman, Platt, Bass, Onderdonk, Yokoe, and Huang (2008) implemented an intervention following a baseline, which consisted of:

A change from the use of pour bottles to bucket immersion for applying hospital-grade

quaternary ammonium disinfectant to cleaning cloths,

An educational campaign, and

Feedback regarding adequacy of discharge cleaning.

A novel non-toxic tracking marker that is visible under a UV lamp (black light) was also implemented to assess the quality of environmental cleaning. The marker was invisible to the naked eye, could be removed only with sufficient moisture, and applied pressure. In total, 15 “high touch” surfaces were recognized using a survey and consisted of:

Main doorknob,

Bathroom doorknob,

Main countertop,

Linen hamper,

Monitor touch pad,

Equipment cart top,

Equipment cart handle,

Window countertop,

Intravenous pump,

Sink handle,

Bedside table,

Curtain,

Light switch,

Toilet flush handle, and

Bed rail.

The results of the report, which were readily available to the staff and supervisors, showed an improvement in removal of the black-light mark on the 15 high-touch surfaces, indicating an increased moisture and pressure application to surfaces while cleaning. More interestingly, the collected culture samples showed a significant intervention effect, which reduced environmental MRSA and VRE contamination, when cultures were used as the unit of analysis and data were clustered by room. Furthermore, the findings showed that although there was no direct association between the cleanliness of the specific surface (as observed by effective black-mark removal), the proportion of removed marks in a given room was significantly predictive of fewer MRSA-positive and VRE-positive environmental cultures (Goodman et al, 2008). These findings do not point to cleaning a particular surface, but to the general cleanliness of the room itself to effectively reduce the impact of MRSA prevalence. This intervention has also been shown to reduce the risk of acquiring MRSA from prior room occupants (Datta et al., 2011). The MRSA acquisition decreased during the intervention as compared the baseline periods: 3.0% to 1.5%, respectively. Therefore, patients in rooms previously occupied by MRSA carriers had an increased risk of MRSA acquisition during the baseline, where no


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increased emphasis on cleanliness of “high touch” surfaces was made, as compared to the intervention.

Conversely, some research has shown no positive relationship between room cleanliness and MRSA rates (Mears et al., 2009). For example, Wilson et al., (2011) determined the effect of enhanced cleaning of the near-patient environment on the isolation of hospital pathogens from the bed area and staff hands. The results showed that enhanced cleaning reduced the environmental contamination and hand carriage, but there were no significant effects on patient acquisition of MRSA. Therefore, the findings show that environmental control alone may not impact the acquisition rate of MRSA per se, but it does impact the overall contamination on staff hands and the environment.

Cultural Transformation

Possibly the most difficult yet most effective component in prevention and control of nosocomial MRSA transmission is the engagement of the involved personnel. The “Positive Deviance” problem-solving approach is based on the observation that in every community there are certain persons or groups whose uncommon behaviour or strategies, as compared with those of their peers, enable them to find better solutions to problems (Pennsylvania Patient Safety Advisory). Fostering culture change in practice to allow infection control and prevention should become the responsibility of everyone involved in the care of patients, allowing an engaged front-line staff (Pennsylvania Patient Safety Advisory). Bonuel (2009) outlines the necessary components required for positive deviance technique to drive change from the frontline staff and showed successful reduction in MRSA transmission and infection during the “zero in on MRSA” initiative. The components included:

community ownership,

self-discovery,

the people are “the experts”,

immediacy of action,

emphasis on practice, and

ongoing measurement reinforcing change (Bonuel, 2009).

Frontline staff involvement was shown to be critical, not only when implementing the MRSA bundle, but also when implementing any other MRSA preventive method (Pennsylvania Patient Safety Advisory). Furthermore, an implementation of a protocol itself did not necessarily ensure an immediate compliance by the staff. As indicated by Cheng et al., (2010) compliance with infection control protocols relies on a personal commitment, where a significantly higher compliance of hand hygiene and isolation protocols occurred only after several staff members died during the SARS epidemic. Fortunately, such dramatic incidents are not the only factors leading to increased compliance in healthcare workers. Kok et al. (2011), indicated that regular and frequent feedback following education about preventive measures was associated with an increased compliance to the protocol and a reduction in the incidence of intravascular device-associated bacteraemias.

In addition, leadership engagement has also shown to be necessary in the success of the program (Welsh, Flanagan, Kiess, & Doebbeling, 2011). Support in the form of money, personnel, and sponsorship from the senior administration and active unit leadership were essential in the alignment of resources such as purchasing isolation supplies, hand hygiene dispensers, isolation signs, carts, gowns, gloves, and disposable equipment. Also, appropriate personnel were needed to manage the data and motivate the staff ensuring the program remains a priority (Welsh et al., 2011).

Nursing homes and MRSA


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Although the prevalence of MRSA infections and transmission based on the age of the population was not in scope of the current review, due to the demographic distribution of the province and the emerging literature, it poses as an important variable, which could possibly contribute to the spread of MRSA. Lee et al., (2013) augmented the existing agent-based model of all hospitals in Orange County to include all county nursing homes. The simulation was run to mimic MRSA outbreaks in various health care facilities. The results showed an extended impact on hospitals, led by an outbreak in nursing homes 6 months prior. Therefore, factoring in the age of the admitted patient and whether they come from a nursing home may be an important factor in controlling nosocomial MRSA transmission in the hospital.

To add to this complexity, pets in nursing homes may not pose a significant threat to the transmission of MRSA. Gandolfi-Decristophoris et al. (2012) assessed the carriage of MRSA in residents living in nursing homes with or without pets. The results showed no evidence that pets provide an increased risk of carriage of MRSA for the residents, therefore adding to the elusive nature of MRSA transmission and infection in humans.

MRSA prevalence and transmission between humans and animals

MRSA has been shown to be wide-spread in animals, most likely as a result of contact with humans (Allen et al., 2010). MRSA lineages have been found in cows, pigs, goats, sheep, chickens, horses, cats, dogs, rats, seals, rabbits, turtles, parrots, bats, and ostriches (for review see McCarthy, Lindsay, & Loeffler, 2012). In addition, the these species camels, lions, chimpanzees and squirrels also have confirmed Staphylococcus aureus lineages which are methicillin-sensitive (MSSA), widening the concerns of MRSA infection and transmission among species (McCarthy et al., 2012).

This portion of the review explores the prevalence of MRSA in livestock, pets and veterinary clinics, retail meat, and wild animals where MRSA is prevalent and direct transfer to humans has been documented. The main message of these sections is that MRSA is more prevalent in the environment than previously thought and although there is no substantial link with the pervasiveness of HA-MRSA infections yet, there is a growing concern that LA-MRSA may play an important part in the hospital and community infections (Cohn & Middleton, 2010; Graveland, Duim, van Duijkeren, Heederik, & Wagenaar, 2011; Kluytmans, 2010; Köck et al., 2013; Köck et al., 2011; Petinaki & Spiliopoulou, 2012; Wieler, Ewers, Guenther, Walther, & Lübke-Becker, 2011; but see Cuny, Köck, & Witte, 2013).

MRSA in Livestock (LA-MRSA)

The literature reviewed in this section indicates a substantial prevalence of MRSA in nearly all animals used as a food source and beyond. LA-MRSA strains have been reported to cause outbreaks in hospitals, but show different characteristics than typical HA-MRSA.

Farm animals, pigs in particular, appear to be an important reservoir for MRSA colonization and infection of humans (for review see Crombé et al., 2013; Petinaki & Spiliopoulou, 2012). The common strain of MRSA prevalent in North American and European farm animals is the CC398 while the ST9 strain has been prevalent in Asian countries (see Crombé et al., 2013). The CC398, with the use of genome sequencing data, has been shown to originate from humans and later transferred to livestock animals (Price, Stegger, Hasman, Aziz, Larsen & Andersen, 2012).

Contact is the predominant avenue of transmission and can be either direct pig-to-pig, or indirect, with a facilitation of a vector (intermediate carrier). Literature shows that humans, companion animals, other livestock cohabitating at the farm, and wild rodents are susceptible to colonization or contamination with LA-MRSA (Cohn & Middleton, 2010; Kluytmans, 2010; McCarthy et al., 2012; Petinaki & Spiliopoulou, 2012; Pletinckx et al., 2013; Verkade & Kluytmans, 2013). In addition, MRSA has been found in the air of contaminated farms as well as on surfaces and materials, further widening transmission routes (Friese et al., 2012; Masclaux, Sakwinska, Charrière, Semaani, & Oppliger, 2013; Schulz et al., 2012).


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Therefore, housing conditions, group density in slaughterhouses, and transport play an important role as only a few infected animals can result in the propagation of MRSA throughout the herd (Crombé et al., 2013).

Transmission of MRSA from livestock to humans has been widely reported (for review see Crombé et al., 2013). Typically, persons with direct contact with the infected animal, such as farmers, veterinarians, and slaughterhouse workers have been reported to be at an increased risk for being colonized (Petinaki & Spiliopoulou, 2012). The exact routes of transmission between pigs and companion animals have not yet been directly investigated, but it is assumed that it occurs by direct contact and contaminated air or environment (Crombé et al., 2013). In fact, Friese et al. (2012), showed that the air was contaminated with MRSA in 85.2% of the sampled MRSA-positive barns. In addition to isolating LA-MRSA from animals, floor and air samples in the barn, Schulz et al., (2012) was able to isolate LA-MRSA from soil surfaces as far as 300 m downwind from the barns. It appears that LA-MRSA types found in the area surrounding the barn are strongly influenced by wind direction and seasons with greater spread being downwind and in the summer months.

The colonization of MRSA in humans, especially the CC398 strain remains somewhat elusive as research indicates that after a short occupational exposure to MRSA-positive pigs, only 17% of the field workers were contaminated. Of these workers, 94% were cleared of MRSA within 24-hours and the rest shortly after (see Crombé et al., 2013). However, such speedy recovery from MRSA contamination does not show to be consistent with all colonisations. Köck et al., (2012) investigated whether absence from direct contact with pigs during holidays would impact the rates of nasal MRSA colonization in farmers working directly with the infected animals. Over half, 59%, of the farmers did not clear the colonization during their 7 – 14 day leave (Köck et al., 2012). To add to this complexity, MRSA does not seem to be easily transmitted between family members (Crombé et al., 2013). There are reduced rates of colonization in farmer’s family members who do not directly work with the colonized animals or have a reduced contact with the MRSA-positive locations (Crombé et al., 2013).

So far, hospital outbreaks caused by LA-MRSA, especially the CC398 strain, have been occasionally reported (for references see Crombé et al., 2013). Overall, little is known about LA-MRSA occurrence and impact on hospital outbreaks. Köck et al., (2013) investigated the occurrence of LA-MRSA CC398 as compared to hospital acquired MRSA lineages in Germany. A significant proportion, 17%, of MRSA isolates was associated with LA-MRSA CC398 in 2006, but increased to 29% in 2012. Furthermore, the proportion changed drastically based on the geographical distribution of the hospitals. Samples collected in parts of Germany reached proportions as high as 89% in areas closest to the Dutch side of the border, where pig production is highest (Köck et al., 2013).

LA-MRSA CC398 has been isolated from clinical specimens including blood cultures (8%) and deep respiratory tract secretions (14%) (Köck et al., 2013). When considering the characteristics of the hospital patients colonized with LA-MRSA CC398 and other MRSA clones, Köck et al. (2011), showed that the CC398 clone accounted for 25% of all MRSA carriage in patients admitted to German hospitals. However, only 7% of MRSA from all clinical specimens were the LA-MRSA CC398 strain. The patients carrying the MRSA CC398 strain were younger, had shorter loss of service (LOS), and were less frequently required to be admitted to the ICUs as compared to other hospital acquired strains. Moreover, patients colonized with MRSA CC398 strain were less likely to develop metabolic disorders, heart or respiratory diseases, diseases of the digestive system and renal failure as compared to patients carrying HA-MRSA strains (Köck et al., 2011).

MRSA in retail meat In addition to MRSA presence in livestock animals, the transfer of MRSA also occurs in meat sold for human consumption. Only a few positive animals can result in propagation of MRSA on farms and


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beyond (Crombé et al., 2013). Therefore, the contamination in slaughterhouses is most likely due to the high density of the animals creating a suitable environment for convenient animal-to-animal contamination (for review see Crombé et al., 2013). In fact, people working in the slaughterhouses have shown one of the highest rates of MRSA infection, further strengthening animal-to-human and vice versa transmission (for review see Crombé et al., 2013). Furthermore, the Dutch Good Safety Agency conducted an exemplary survey investigating the MRSA contamination in food. MRSA was isolated from 11.9% of the overall collected samples, which included:

turkey (35.3%),

chicken (16%),

veal (15.2%),

pork (10.7%),

beef (10.6%),

lamb and mutton (6.2%),

fowl (3.4%), and

game (2.2%) (Kluytmans, 2010).

Another survey found that 46% of the retail meat was contaminated and the most common strains included CC398 and USA300 (for review see Kluytmans, 2010). These findings indicate that not only is MRSA prevalent in livestock, but it is also found in food for human consumption. The CC398 isolates originate from raw ingredients and can be killed by adequate cooking or pasteurization processes (Andreoletti et al., 2009).

MRSA in companion animals and pets

In addition to livestock animals, companion animals, such as cats and dogs, have been recognized as carriers of MRSA strains resembling those of their owners (for review see Crombé et al., 2013). In fact, some researchers speculate that the human epidemic is driving the veterinary epidemic as the reports of MRSA isolated from pets have recently increased in parallel with increased MRSA isolation in humans (Davis et al., 2012). Basic strand typing showed that MRSA isolates from pets and people were closely related or identical, thus indicating a transfer of hospital acquired (HA) MRSA from people to their companion animals (McCarthy et al., 2012). Pets have been colonized with or infected with HA-MRSA strains (e.g. ST22, EMRSA-15) and community acquired (CA)-MRSA strains (e.g. Canadian MRSA-2, ST80 strains), which have been shown to cause disease in humans (Davis et al., 2012). In addition, an increased likelihood of the staphylococcal species transfer has been suggested to occur in household settings, as MRSA has shown to survive on environmental surfaces (for review see Davis et al., 2012).

The cross-transmission between humans and pets has been established in veterinary clinics (Davis et al., 2012). Vet clinic staff, including veterinarians, have shown an increased rates of colonization with MRSA strains similar to the ones found in residents and their pets who visit the clinic (for review see Davis et al., 2012). As well, recent literature suggests that pets do not naturally host at least some strains, such as MRSA CC22. Finally, MRSA has shown continuous adaptation, as established by its genetic variation, which could raise public health concern (Loeffler et al., 2013).

MRSA in wild animals

Non-domesticated animals have also been shown to harbour MRSA strains (Crombé et al., 2013; Petinaki & Spiliopoulou, 2012; Pletinckx et al., 2013). There is an indication of two categories of animals that are likely to be infected. The first group consists of wild animals with access to farms and farm animals harbouring MRSA. In fact, literature suggests that a high number of rodents, as much as


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70.6% of black rats (Rattus rattus) and voles (Microtus arvalis) caught on MRSA-positive farms carried MRSA CC398 strains (Crombé et al., 2013; Pletinckx et al., 2013).

The second group of wild animals recognized to transmit MRSA includes ones that do not have a direct access to farm animals. Allen et al., (2010) highlight that transmission to wild animals may typically occur by human exposure with wild animals and their microbiota by:

“1.Translocation of wildlife into suburban areas owing to game release, habitat destruction, pollution and changes to water storage, irrigation or the climate. 2. Ecotourism, hunting and camping. 3. Exotic foods, wet markets, bushmeat and game farms. 4. Exotic pets and the long-distance transport of live animals. 5. Zoos, aquaria, wildlife safari parks and circuses. 6. Trapping or rearing of fur-bearing animals.” (Allen et al., 2010).

General Conclusion

It is apparent that the pervasiveness of MRSA within a hospital setting is troublesome and requires an immediate attention. The best described and effective method to control and eradicate MRSA has been the MRSA bundle, which includes: universal screening, contact precautions and isolation, hand hygiene protocols for healthcare staff, patients, and visitors, and environmental control. In order for this intervention, there must be a substantial engagement from the staff and management. So far, there is much debate on the effectiveness of these individual interventions to control nosocomial MRSA and it is apparent that the implementation of all components is required for successful control and eradication of these pathogens. Although the beginnings of MRSA may have been strictly human based in hospital setting, it is evident that this is no longer the case. Furthermore, it remains consistent that control of MRSA transfer and outbreaks is essential in the hospital setting as the HA strains show to be severe for human health. It is no longer reasonable to assume that MRSA is solely a problem which must be addressed only in the hospital. The MRSA strains have shown substantial adaptation and evolution where strains have been exchanged between several species including humans, possibly multiple times. Therefore, tackling MRSA may require a new, holistic approach as opposed to individually focusing on either hospital or farm settings.


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Review Articles Search Methods The focus of this literature review was to provide recent (2008 – present) findings on two major topics:

1. What are the best practices to control and eradicate nosocomial MRSA in the ICU, and 2. Is there an indication that MRSA can be transmitted between humans and animals, with the

focus on livestock. Studies published in 2008 or later were identified through the MEDLINE, PUBMED, and the Cochrane Library electronic databases and with the assistance of a librarian to find the relative journal articles. To review the first question the following keywords were used:

nosocomial MRSA in ICU, and

prevention guidelines.

In total, 180 articles were found. The titles and abstracts of the articles were reviewed. The articles which indicated various techniques to prevent and control MRSA prevalence and outbreak were selected. The focus was on large scale and long-term initiatives. Once this selection was completed, there were 40 articles which were read carefully to include the most relevant articles in the summary. These references and abstracts also include the articles outlined in the reference page. As this search did not originally yield any substantial literature on the cost-benefit analysis of surveillance, and additional search was performed. The keywords used were MRSA surveillance and cost-benefit analysis. There were four articles, two of which were included in this review. Similarly, to address the second topic of the literature review, the same sources were searched using a Boolean search allowing combining the following keywords:

MRSA transmission, and

Animals.

Only articles in the English language were considered in the review. In total, the search yielded 143 articles. Similarly, the abstracts were read for all these articles to select the most relevant articles. Following, the selected articles were read carefully and included in the summary. In total there were 41 articles which were considered relevant and read carefully in their entirety. The articles included in the literature review are listed in the reference section below. To complete the literature review, 50 of the most relevant and representative articles were included.


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References used in the review

Allen, H. K., Donato, J., Wang, H. H., Cloud-Hansen, K. A., Davies, J., & Handelsman, J. (2010). Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology, 8(4), 251 – 259. doi:10.1038/nrmicro2312

Andreoletti, O., Budka, H., Buncic, S., Colin, P., Collins, J. D., De Koeijer, … Vanopbenbosch, E. (2009). Assessment of the public health significance of methicillin resistant Staphylococcus aureus (MRSA) in animals and foods. The European Food Safety Authority Journal, 993, 1 - 73.

Bonuel, N., Byers, P., & Gray-Becknell, T. (2009). Methicillin-resistant Staphylococcus aureus (MRSA) prevention through facility-wide culture change. Critical Care Nursing Quarterly, 32(2), 144 – 148.

Camus, C., Bellissant, E., Legras, A., Renault, A., Gacouin, A., Lavoué, S., … Thomas, R. (2011). Randomized comparison of 2 protocols to prevent acquisition of methicillin-resistant Staphylococcus aureus: results of a 2-center study involving 500 patients. Infection Control and Hospital Epidemiology, 32(11), 1064 – 1072. doi:10.1086/662180

Carling, P. C., Parry, M. F., Bruno-Murtha, L. A., & Dick, B. (2010). Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission. Critical Care Medicine, 38(4), 1054 – 1059. doi:10.1097/CCM.0b013e3181cdf705

Cheng, V. C. C., Tai, J. W. M., Chan, W. M., Lau, E. H. Y., Chan, J. F. W., To, K. K. W., … Yuen, K. Y. (2010). Sequential introduction of single room isolation and hand hygiene campaign in the control of methicillin-resistant Staphylococcus aureus in intensive care unit. BMC infectious diseases, 10, 263 – 273. doi:10.1186/1471-2334-10-263

Cohn, L. A., & Middleton, J. R. (2010). A veterinary perspective on methicillin-resistant staphylococci. Journal of Veterinary Emergency and Critical Care, 20(1), 31 – 45. doi:10.1111/j.1476-4431.2009.00497.x

Crombé, F., Argudín, M. A., Vanderhaeghen, W., Hermans, K., Haesebrouck, F., & Butaye, P. (2013). Transmission dynamics of methicillin-resistant Staphylococcus aureus in pigs. Frontiers in Microbiology, 4(57), 1 – 21. doi:10.3389/fmicb.2013.00057

Cuny, C., Köck, R., & Witte, W. (2013). Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany. International Journal of Medical Microbiology, 303, 331 – 337. doi:10.1016/j.ijmm.2013.02.010

Datta, R., Platt, R., Yokoe, D. S., & Huang, S. S. (2011). Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants. Archives of Internal Medicine, 171(6), 491 – 494. doi:10.1001/archinternmed.2011.64

Davis, M. F., Iverson, S. A., Baron, P., Vasse, A., Silbergeld, E. K., Lautenbach, E., & Morris, D. O. (2012). Household transmission of meticillin-resistant Staphylococcus aureus and other staphylococci. The Lancet Infectious Diseases, 12(9), 703 – 716. doi:10.1016/S1473-3099(12)70156-1

Evans, M. E., Kralovic, S. M., Simbartl, L. A., Freyberg, R. W., Obrosky, S. D., Roselle, G. A., & Jain, R. (2013). Veterans Affairs methicillin-resistant Staphylococcus aureus prevention initiative


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associated with a sustained reduction in transmissions and health care-associated infections. American Journal of Infection Control, 41, 1093 - 1095.

Friese, A., Schulz, J., Hoehle, L., Fetsch, A., Tenhagen, B.-A., Hartung, J., & Roesler, U. (2012). Occurrence of MRSA in air and housing environment of pig barns. Veterinary Microbiology, 158, 129 – 135. doi:10.1016/j.vetmic.2012.01.019

Gagné, D., Bédard, G., & Maziade, P. J. (2010). Systematic patients’ hand disinfection: impact on meticillin-resistant Staphylococcus aureus infection rates in a community hospital. The Journal of Hospital Infection, 75(4), 269 – 272. doi:10.1016/j.jhin.2010.02.028

Gandolfi-Decristophoris, P., De Benedetti, A., Petignat, C., Attinger, M., Guillaume, J., Fiebig, L., … Schelling, E. (2012). Evaluation of pet contact as a risk factor for carriage of multidrug-resistant staphylococci in nursing home residents. American Journal of Infection Control, 40(2), 128 – 133. doi:10.1016/j.ajic.2011.04.007

Gould, I. M., Peilly, J., Bunyan., D., & Walker, A. (2010). Costs of healthcare-associated methicillin-resistant Staphylococcus aureus and its control. Clinical Microbiology and Infection, 16, 1721-1728.

Graveland, H., Duim, B., van Duijkeren, E., Heederik, D., & Wagenaar, J. a. (2011). Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. International Journal of Medical Microbiology, 301(8), 630 – 634. doi:10.1016/j.ijmm.2011.09.004

Hansen, S., Schwab, F., Asensio, A., Carsauw, H., Heczko, P., Klavs, I., … Gastmeier, P. (2010). Methicillin-resistant Staphylococcus aureus (MRSA) in Europe: which infection control measures are taken? Infection, 38(3), 159 – 164. doi:10.1007/s15010-010-0001-8

Hitoto, H., Kouatchet, A., Dubé, L., Lemarié, C., Kempf, M., Mercat, A., … Eveillard, M. (2011). Impact of screening and identifying methicillin-resistant Staphylococcus aureus carriers on hand hygiene compliance in 4 intensive care units. American Journal of Infection Control, 39(7), 571 – 576. doi:10.1016/j.ajic.2010.10.029

Holzmann-Pazgal, G., Monney, C., Davis, K., Wanger, A., Strobel, N., & Zhong, F. (2011). Active surveillance culturing impacts methicillin-resistant Staphylococcus aureus acquisition in a pediatric intensive care unit. Pediatric Critical Care Medicine, 12(4), e171 – e175. doi:10.1097/PCC.0b013e3181f39222

Huang, S. S., Septimus, E., Kleinman, K., Moody, J., Hickok, J., Avery, T. R., … Platt, R. (2013). Targeted versus universal decolonization to prevent ICU infection. The New England Journal of Medicine, 368(24), 2255 – 2265. doi:10.1056/NEJMoa1207290

Huang, Y.C., Lien, R.I., Su, L.H., Chou, Y.H., & Lin, T.Y. (2011). Successful control of methicillin-resistant Staphylococcus aureus in endemic neonatal intensive care units: A 7-year campaign. PloS one, 6(8), e23001. doi:10.1371/journal.pone.0023001

Huskins, W. C., Huckabee, C. M., O’Grady, N. P., Murray, P., Kopetskie, H., Zimmer, L., … Goldmann, D. A. (2011). Intervention to reduce transmission of resistant bacteria in intensive care. The New England Journal of Medicine, 364(15), 1407 – 1418. doi:10.1056/NEJMoa1000373


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Jain, R., Kralovic, S., Evans, M., Ambrose, M., Simbartl, L. A., Obrosky, D. S., … Roselle, G. A. (2011). Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. The New England Journal of Medicine, 364(15), 1419 – 1430.

Kang, J.,Mandsager, P., Biddle, A. K., & Weber, D. J. (2012). Cost-effectiveness analysis of active surveillance screening for methicillin-resistant Staphylococcus aureus in an academic hospital setting. Infection Control and Hospital Epdemiology, 33, 477 - 486.

Karas, J. A., Enoch, D. A., Eagle, H. J., & Emery, M. M. (2009). Random meticillin-resistant Staphylococcus aureus carrier surveillance at a district hospital and the impact of interventions to reduce endemic carriage. The Journal of Hospital Infection, 71(4), 327 – 332. doi:10.1016/j.jhin.2008.12.002

Kellie, S. M., Timmins, A., & Brown, C. (2011). A statewide collaborative to reduce methicillin-resistant Staphylococcus aureus bacteremias in New Mexico. Joint Commission Journal on Quality and Patient Safety, 37(4), 154 – 162. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/21500715

Kluytmans, J. A J. W. (2010). Methicillin-resistant Staphylococcus aureus in food products: cause for concern or case for complacency? Clinical Microbiology and Infection, 16(1), 11 – 15. doi:10.1111/j.1469-0691.2009.03110.x

Köck, R., Siam, K., Al-Malat, S., Christmann, J., Schaumburg, F., Becker, K., & Friedrich, A. W. (2011). Characteristics of hospital patients colonized with livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) CC398 versus other MRSA clones. The Journal of Hospital Infection, 79(4), 292 – 296. doi:10.1016/j.jhin.2011.08.011

Köck, R., Loth, B., Köksal, M., Schulte-Wülwer, J., Harlizius, J., & Friedrich, A. W. (2012). Persistence of nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers after holidays from pig exposure. Applied and Environmental Microbiology, 78(11), 4046 – 4047. doi:10.1128/AEM.00212-12

Köck, R., Schaumburg, F., Mellmann, A., Köksal, M., Jurke, A., Becker, K., & Friedrich, A. W. (2013). Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PloS one, 8(2), e55040. doi:10.1371/journal.pone.0055040

Kohlenberg, A., Schwab, F., Behnke, M., Geffers, C., & Gastmeier, P. (2011). Screening and control of methicillin-resistant Staphylococcus aureus in 186 intensive care units: different situations and individual solutions. Critical Care, 15(6), R285. doi:10.1186/cc10571

Kok, J., O’Sullivan, M. V, & Gilbert, G. L. (2011). Feedback to clinicians on preventable factors can reduce hospital onset Staphylococcus aureus bacteraemia rates. The Journal of Hospital Infection, 79(2), 108 – 114. doi:10.1016/j.jhin.2011.04.023

Lee, B. Y., Bartsch, S. M., Wong, K. F., Singh, A., Avery, T. R., Kim, D. S., … Huang, S. S. (2013). The importance of nursing homes in the spread of methicillin-resistant Staphylococcus aureus (MRSA) among hospitals. Medical Care, 51(3), 205–215.

Loeffler, A., McCarthy, A., Lloyd, D. H., Musilová, E., Pfeiffer, D. U., & Lindsay, J. A. (2013). Whole-genome comparison of meticillin-resistant Staphylococcus aureus CC22 SCCmecIV from people and their in-contact pets. Veterinary Dermatology, 24(5), 538 – e128. doi:10.1111/vde.12062


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Lucet, J.C., & Regnier, B. (2010). Screening and decolonization: does methicillin-susceptible Staphylococcus aureus hold lessons for methicillin-resistant S. aureus? Clinical Infectious Diseases, 51(5), 585 – 590. doi:10.1086/655695

Masclaux, F. G., Sakwinska, O., Charrière, N., Semaani, E., & Oppliger, A. (2013). Concentration of airborne Staphylococcus aureus (MRSA and MSSA), total bacteria, and endotoxins in pig farms. The Annals of Occupational Hygiene, 57(5), 550 – 557. doi:10.1093/annhyg/mes098

McCarthy, A. J., Lindsay, J. A., & Loeffler, A. (2012). Are all meticillin-resistant Staphylococcus aureus (MRSA) equal in all hosts? Epidemiological and genetic comparison between animal and human MRSA. Veterinary Dermatology, 23(4), 267 – e54. doi:10.1111/j.1365-3164.2012.01072.x

McLaws, M., Pantle, A. C., Fitzpatrick, K. R., Hughes, C. F., Medical, T., & Journal, M. (2009). More than hand hygiene is needed to affect methicillin-resistant Staphylococcus aureus clinical indicator rates: Clean hands save lives, Part IV. Medical Journal of Australia, 191(8), S26 - S31.

Mears, A., White, A., Cookson, B., Devine, M., Sedgwick, J., Phillips, E., … Bardsley, M. (2009). Healthcare-associated infection in acute hospitals: which interventions are effective? The Journal of Hospital Infection, 71(4), 307 – 313. doi:10.1016/j.jhin.2008.12.004

Petinaki, E., & Spiliopoulou, I. (2012). Methicillin-resistant Staphylococcus aureus among companion and food-chain animals: impact of human contacts. Clinical Microbiology and Infection, 18(7), 626 – 634. doi:10.1111/j.1469-0691.2012.03881.x

Pletinckx, L. J., Verhegghe, M., Crombé, F., Dewulf, J., De Bleecker, Y., Rasschaert, G., … De Man, I. (2013). Evidence of possible methicillin-resistant Staphylococcus aureus ST398 spread between pigs and other animals and people residing on the same farm. Preventive Veterinary Medicine, 109(3-4), 293 – 303. doi:10.1016/j.prevetmed.2012.10.019

Rodríguez-Baño, J., García, L., Ramírez, E., Lupión, C., Muniain, M. a, Velasco, C., … Pascual, A. (2010). Long-term control of endemic hospital-wide methicillin-resistant Staphylococcus aureus (MRSA): The impact of targeted active surveillance for MRSA in patients and healthcare workers. Infection Control and Hospital Epidemiology, 31(8), 786 – 795. doi:10.1086/654003

Rymzhanova, R., Thouverez, M., Talon, D., & Bertrand, X. (2009). Usefulness of weekly methicillin-resistant Staphylococcus aureus screening. Infection Control and Hospital Epidemiology, 30(11), 1113 – 1115. doi:10.1086/644753

Sakamoto, F., Yamada, H., Suzuki, C., Sugiura, H., & Tokuda, Y. (2010). Increased use of alcohol-based hand sanitizers and successful eradication of methicillin-resistant Staphylococcus aureus from a neonatal intensive care unit: A multivariate time series analysis. American Journal of Infection Control, 38(7), 529 – 534. doi:10.1016/j.ajic.2009.12.014

Schulz, J., Friese, A., Klees, S., Tenhagen, B. A., Fetsch, A., Rösler, U., & Hartung, J. (2012). Longitudinal study of the contamination of air and of soil surfaces in the vicinity of pig barns by livestock-associated methicillin-resistant Staphylococcus aureus. Applied and Environmental Microbiology, 78(16), 5666 – 5671. doi:10.1128/AEM.00550-12

Verkade, E., & Kluytmans, J. (2013). Livestock-associated Staphylococcus aureus CC398: Animal reservoirs and human infections. Infection, Genetics and Evolution, in press. doi:10.1016/j.meegid.2013.02.013


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Welsh, C. A., Flanagan, M. E., Kiess, C., & Doebbeling, B. N. (2011). Implementing the MRSA Bundle in ICUs : One Citywide Collaborative’ s Key Lessons Learned. Infection Control and Hospital Epidemiology, 32(9), 918 – 921.

Wieler, L. H., Ewers, C., Guenther, S., Walther, B., & Lübke-Becker, A. (2011). Methicillin-resistant staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)-producing Enterobacteriaceae in companion animals: nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. International Journal of Medical Microbiology, 301(8), 635 – 641. doi:10.1016/j.ijmm.2011.09.009

Wilson, A. P. R., Smyth, D., Moore, G., Singleton, J., Jackson, R., Gant, V., … Bellingan, G. (2011). The impact of enhanced cleaning within the intensive care unit on contamination of the near-patient environment with hospital pathogens: a randomized crossover study in critical care units in two hospitals. Critical Care Medicine, 39(4), 651 – 658. doi:10.1097/CCM.0b013e318206bc66

References not used in the review (formatting as per RefWorks)

Al Reyami E, Al Zoabi K, Rahmani A, Tamim M & Chedid F. (2009). Is isolation of outborn infants required at admission to the neonatal intensive care unit?. American Journal of Infection Control, 37, 335-7. doi:10.1016/j.ajic.2008.09.023

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