gms | German Medical Science

GMS Hygiene and Infection Control

Deutsche Gesellschaft für Krankenhaushygiene (DGKH)

ISSN 2196-5226

Implementing the MRSA recommendations made by the Commission for Hospital Hygiene and Infection Prevention (KRINKO) of 1999 – current considerations by the DGKH Management Board

Umsetzung der MRSA-Empfehlung der Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch-Institut – Kommentar der Deutschen Gesellschaft für Krankenhaushygiene

Review Article

Suche in Medline nach

  • corresponding author Arne Simon - Children's Hospital Medical Centre, University of Bonn, Germany
  • Martin Exner - Institute for Hygiene and Public Health, University of Bonn, Germany
  • author Axel Kramer - Institute for Hygiene and Environmental Medicine, Medical Faculty, Ernst Moritz Arndt University Greifswald, Germany
  • Steffen Engelhart - Institute for Hygiene and Public Health, University of Bonn, Germany

GMS Krankenhaushyg Interdiszip 2009;4(1):Doc02

doi: 10.3205/dgkh000127, urn:nbn:de:0183-dgkh0001278

Veröffentlicht: 9. April 2009

© 2009 Simon et al.
Dieser Artikel ist ein Open Access-Artikel und steht unter den Creative Commons Lizenzbedingungen (http://creativecommons.org/licenses/by-nc-nd/3.0/deed.de). Er darf vervielfältigt, verbreitet und öffentlich zugänglich gemacht werden, vorausgesetzt dass Autor und Quelle genannt werden.


Abstract

In Germany, recommendations on dealing with patients who are colonised with methicillin-resistant S. aureus (MRSA) for the inpatient sector have been published in 1999 by the Commission for Hospital Hygiene and Infection Prevention (KRINKO). Some challenges arise with regard to the practical implementation of the KRINKO recommendations. These challenges do not principally question the benefit of the recommendations but have come into criticism from users. In this commentary the German Society for Hospital Hygiene (DGKH) discusses some controversial issues and adds suggestions for unresolved problems regarding the infection control management of MRSA in healthcare settings.

Keywords: MRSA, nosocomial infection, infection control

Zusammenfassung

In Deutschland wurde 1999 von der Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch-Institut (KRINKO) die ‚Empfehlung zur Prävention und Kontrolle von Methicillin-resistenten Staphylococcus aureus-Stämmen (MRSA) in Krankenhäusern und anderen medizinischen Einrichtungen’ publiziert. Die praktische Umsetzung dieser Empfehlung stellt das gesamte Behandlungsteam vor erhebliche Herausforderungen. Die mit der Umsetzung verbundenen Probleme stellen den Nutzen der Empfehlung nicht prinzipiell infrage, führen aber zu anhaltender Kritik von Seiten einiger Anwender. In diesem Kommentar thematisiert die Deutschen Gesellschaft für Krankenhaushygiene einige kontroverse Themen der MRSA-Empfehlung und ergänzt Vorschläge zur praktischen Umsetzung.

Schlüsselwörter: MRSA, nosokomiale Infektion, Infektionsprävention, Infektionskontrolle


1. Introduction and scope of this commentary

Treating and dealing with patients who are colonised with methicillin-resistant S. aureus (MRSA) [1], [2] or suffer from nosocomial infections caused by MRSA, poses a particular challenge to all healthcare facilities, such as hospitals [3], specialist outpatient clinics, nursing homes [4], [5], [6], [7], [8], [9] and office-based primary care physicians [5], [10]. In Germany, recommendations on this topic for the inpatient sector have been published in 1999 by the Commission for Hospital Hygiene and Infection Prevention (KRINKO) [11], [12]. The contents of these recommendations do not differ essentially from comparable recommendations issued by other European countries [13] or US-American professional societies [14] / Centres for Disease Control and Prevention (CDC) [15], [16].

Regarding MRSA screening and isolating patients whose MRSA status has not yet been clarified, the specifications of the recommendations are not as strict as the “search and destroy” policy in the healthcare system in the Netherlands [17], [18], a directly adjacent country with very low MRSA prevalence [19], [20], [21], [22], [23].

A commentary on the KRINKO recommendations was published in 2004 and provides information on patients with an increased risk of MRSA colonisation [11]. An updated version of this commentary was published in issue 42 of the Epidemiologisches Bulletin (2008). The aim of these commentaries is to provide on-site support to doctors in attendance, hospital infection control personnel, microbiologists and the administrative hospital management for establishing a local guideline for MRSA screening [24], [25], [26].

Some challenges arise with regard to the practical implementation of the KRINKO recommendations. These challenges do not principally question the benefit of the recommendations but have come into criticism from users. This criticism of the KRINKO recommendations [27], [28] especially refers to the following aspects:

1.
Relativisation of the clinical meaning of MRSA
(“MRSA is not an epidemic plague“)
2.
Single room isolation and special safety measures, such as wearing protective gowns and masks before entering the isolation room
3.
Risk of inadequate medical care of MRSA-colonised patients due to isolation (surveillance of vital functions, regular status evaluations, diagnostic and therapeutic interventions)
4.
Restricted mobility, social stigmatisation and psychological stress of isolated patients
5.
Specific considerations on operations in MRSA-colonised or -infected patients
6.
How to deal with nursing and medical staff who are MRSA carriers; necessity of decolonisation treatment of medical staff
7.
Problems in pre- and post-inpatient care of MRSA-positive patients

These points are commented on by the German Society for Hospital Hygiene (DGKH) below.


2. Commentaries issued by the DGKH

2.1. Is MRSA a significant infection-epidemiological pathogen?

Some critics of the KRINKO recommendations argue that MRSA is not an epidemic pathogen (Definition: highly contagious pathogen, which results in serious illnesses in the majority of people in case of a transmission), such as M. tuberculosis, Y. pestis or S. typhi, and deduce from this that standard hygiene measures are sufficient for controlling nosocomial spread. This allegation is misleading because

  • the KRINKO recommendations [12] do not classify MRSA as an ‘epidemic plague’;
  • the measures required for preventing nosocomial transmission of a certain pathogen are derived from possible transmission paths and not exclusively from its contagiousness (probability of transmission to people who come into contact with an infectious agent) or virulence (pathogen-specific property; describes the risk of illness for people who come into contact with the pathogen or are colonised) for otherwise healthy people.
  • a pathogen, which is not an epidemic pathogen, is therefore by no means less dangerous to infected patients. As a matter of fact, far more patients die from nosocomial MRSA infections (e.g. pneumonia, sepsis) in Germany than from tuberculosis, the plague and typhoid as a whole [29].

MRSA is indeed not the cause of an epidemic plague but still of paramount epidemiological importance as is also shown by the following considerations.

2.1.1 Epidemiological development of MRSA infections since 1999

According to the results of the prevalence studies carried out by the Paul-Ehrlich Society for Chemotherapy (http://www.p-e-g.org/ag_resistenz/main.htm), the proportion of oxacillin-resistant S. aureus was less than 2% in 1990, 12.9% in 1995, 15.8% in 1998 [30], 20.7% in 2001 and 22.6% in 2004 [31]. Tiemersma et al. documented 8.5% MRSA in 1999, 18.5% in 2002, 19.6% in 2004, 20.6% in 2006 and 23.2% in 2008 in the EARSS database (European Antimicrobial Resistance Surveillance System; http://www.rivm.nl/earss/database/) [21].

The SARI project [32] highlighted the following MRSA rates for German intensive care units: 26.3% in 2001, 22.2% in 2002, 20.8% in 2003, 19.5% in 2004, 22.3% in 2005, 22.1% in 2006 and 20.3% in 2007. The Hospital Infection Surveillance System (KISS) collects data from more than 200 intensive care units (ICU) in Germany.

The prevalence of MRSA as a share of all S. aureus isolates within this collection system rose on average from 8% in 1997 to 30% in 2003; whereby the share of MRSA in primary S. aureus sepsis was at 37.8% and of nosocomial pneumonia at 21.5 % [20], [33]. In a current review, Gastmeier et al. [34] assume at least 14,000 nosocomial MRSA infections in Germany per year.

Whilst this data always refer to certain selected patient groups, a trend in the spread of MRSA in German clinics must be assumed; this trend has been constantly on the rise for many years now [3], [20]. Some studies, amongst others, of the University Hospital Heidelberg [35], reveal that the epidemically occurring nosocomial MRSA isolates are mostly a few PFGE-identical clones, which are, presumably, particularly well adapted to the hospital environment.

Given the increase in prevalence, it is not reasonable and irresponsible to fundamentally question the basic statements of the 1999 KRINKO recommendations [12]. Implementation of the KRINKO recommendations, which is not pursued with the same consistency in all facilities [20], is the direct responsibility of hospital management and operators [36], [37], [38], the hygiene experts in charge, nursing and medical staff in attendance, and, in addition, should also be subject to health surveillance by the competent medical authority according to § 36 and § 23 of the German Infection Protection Act (IfSG) [39]. Numerous studies have proven that consistently implementing pertinent prevention and control concepts sustainably reduces the rate of MRSA transmissions and infections [16], [18], [40], [41], [42], [43], [44], [45], [46], [47], [48], [49], [50], [51], [52].

2.1.2 MRSA colonisation and risk of an MRSA infection

Patients colonised with MRSA run an increased risk of developing nosocomial MRSA infections [19], [53], [54]. Colonisation precedes infection with the exception of cases where MRSA is directly transmitted to a previously uncolonised patient with pre-existing risk factors (e.g. due to a lack in hygiene/antisepsis during change of dressing or when dealing with vascular catheters or respiration equipment) [55], [56]. According to a meta-analysis of Safdar et al., MRSA-colonised patients have a 4-fold increased risk of consecutive MRSA infection (OR 4.08, 95% CI95 2.10–7.44) [57]. This is why it is necessary in the interests of patients possibly colonised with MRSA as well as for the sake of protecting other patients to

  • examine the MRSA status of patients with certain risk factors [22], [23], [25], [58] and
  • ensure that patients who are not colonised with MRSA (“MRSA-negative“) do not come into direct or indirect contact with this infectious agent [26].

In order to avoid nosocomial transmissions, it is vital to ensure that patients with proven MRSA according to the KRINKO recommendations are consistently isolated and decolonised even if on-site resources are not sufficient for implementing prospective admission screening, and/or until such a screening has been established [14], [59], [60]. The nosocomial MRSA isolates detected in Germany do not constitute any risk for otherwise healthy people without particular co-morbidities and risk factors. (Community acquired (c-)MRSA isolates with particular virulence factors, such as the synthesis of the Panton-Valentine Leukocidin, need to be differentiated from this. These cMRSA strains have so far been very rare in Germany, and have above all occurred as triggers of regional epidemics. The development in the US during the last 10 years shows that an increase in cMRSA infections must probably be expected also in Germany. The preventive measures required in this context exceed the various aspects of control in healthcare facilities of the healthcare system by far but are not the topic of this commentary.)

The situation of patients with pre-existing co-morbidities and risk factors for nosocomial infections is totally different [19]. In case of an MRSA colonisation, at least one MRSA infection must be expected in up to 30% of such patients in clinical course [61]. According to the study of Thompson et al., the incidence of MRSA bacteriaemiae in intensive care unit patients with nosocomial MRSA transmission amounted to 20% (15%–25%) [61].

According to a survey on MRSA infections in paediatrics, published in 2003 [62], an average of 35% (16%–52%) of colonised patients developed an infection in the course of colonisation and within the context of outbreaks; within this context, the high ratio of publications on MRSA in pre-term infants that have received intensive care needs be taken into account [63], [64].

In a surgical intensive care unit, Vriens et al. were able to prove that MRSA was more easily transmitted to other patients and nursing and medical staff than MSSA [65]. Patients in orthopaedic [55], [66], and cardiac surgery departments [56] as well as dialysis patients [58], [67] in particular have higher complication risks after surgical interventions if they are colonised with MRSA.

For this reason, the risk of nosocomial transmissions of MRSA must be minimised in hospitals and other healthcare facilities by an evidence-based prevention and control concept in line with the Infection Protection Act's (IfSG) intended purpose, as described in § 1 paragraphs 1 and 2. Moreover, the attempt of decolonisation treatment is recommended for colonised patients (and patients with an MRSA infection alongside systemic antibacterial therapy) [12].

2.1.3 Morbidity and lethality

MRSA infections increase morbidity and mortality rates, especially in patients with pre-existing risk factors, as opposed to patients not suffering from an MRSA infection. This also holds true with regard to patients who have developed a nosocomial infection caused by methicillin-sensible S. aureus (MSSA) [68], [69], [70].

The lethality of MRSA infections is fundamentally determined by pre-existing conditions, a particular pre-disposition for serious infections and the infection actually involved (e.g. postoperative wound infection, infection of a chronic wound, skin and soft part infection, osteomyelitis, pneumonia with or without pre-existing artificial respiration, sepsis or endocarditis).

In the studies analysed by Cosgrove et al., which refer to patient groups treated after 1990, the lethality of predominantly nosocomially acquired MRSA sepsis ranges from 11% to 58% [70]. According to Patel et al. and with regard to intensive care patients, MRSA colonisation (adjusted odds ratio [OR], 3.7 CI95 1.5–8.9; P=.003) and the onset of MRSA infection after the patient's discharge (adjusted OR, 7.6 CI95, 2.48–23.2; P<.001) are linked to an increased lethality risk [62].

In a case-control study, Thompson et al. noted that lethality increased by 21.8% (8.0%–40.1%) in intensive care patients with MRSA sepsis [71].

Blot et al. were able to prove that MRSA sepsis results in 23.4% increased lethality, while MSSA sepsis did not have a significant independent influence on lethality rates [72]. In a multivariate analysis, Shurland et al. also confirmed increased mortality rates in adults, mostly old and multi-morbid patients with MRSA bacteriaemia compared to patients with MSSA bacteriaemia [73].

Mortality of MRSA infections was between 11% and 38% in paediatric and neonatology intensive care patients [62], and 16.5% according to the largest study available on this topic [74].

It is reasonable to assume that significantly more than 5000 people die from acute complications or direct consequences of nosocomial MRSA infections in Germany per year despite the possibilities of antibacterial and intensive care treatments available today.

2.1.4 Expenses

Numerous studies document prolonged periods of hospitalisation as a result of MRSA infections [43], [69]. This is linked to higher medical expenses (compared with patients without such an event and also compared with patients acquiring an MSSA infection). Respirator time is significantly longer in patients with nosocomial MRSA pneumonia compared to those with MSSA pneumonia (17 days vs. 6 days; p<0.01) [75].

Some studies have revealed that the financial expenditure invested in MRSA prevention (screenings and control) is cost-effective [76] and results in even lower overall costs for the medical treatment unit [42], [43], [77], [78]. Implementing a prevention plan geared towards the KRINKO recommendations in clinical practice primarily involves additional investments. For this reason, it is vital that the key decision-makers of hospital administrations and the medical head office are actively involved in establishing instructions for MRSA surveillance, prevention and control and that they provide proper support for both the nursing and medical staff as well as the hygiene experts in its implementation [26], [79], [80].

2.1.5 Consequences in public

Hospitals that do not have a written concept of MRSA prevention and control which is firmly implemented and geared towards the specifications of the KRINKO recommendations will be answerable to the healthcare authorities and are at risk of coming under public pressure in the event of an MRSA outbreak. As can be seen from situations where there is an outbreak of nosocomial infections, a decline in patients must be expected if patients lose confidence in the safety of hygiene strategies of the respective hospital. This particularly applies if safety measures are not already preventively implemented, and are instead consistently implemented in the event of an outbreak due to a fundamental misinterpretation of the importance of MRSA.

Since comprehensive information on MRSA is freely available today, via Internet for instance, and many patients and their relatives actively read up on it, a constant increase in legal actions taken by patients with nosocomial MRSA infections against hospital operators must be factored in. The patients involved are now also represented by their own pressure groups aiming to improve the protection of patients against nosocomial infections in hospitals, and are billing doctors in attendance for the tremendous follow-up costs resulting from complicated pathogeneses.

The economic damage caused by legal consequences and negative publicity can thus be substantial, leading to a drop in referrals from physicians in private practices or other healthcare facilities and can wreak lasting damage on the hospital's public profile [81].

Hospitals which actively implement a concept (established with foresight) for hospital hygiene and infection prevention according to the KRINKO's recommendations and also provide the structural-organisational and personnel prerequisites for this purpose are protected against these consequences. Moreover, they can positively communicate their investments in the fields of quality assurance and patient safety to the public. The number of patients, who thoroughly read up on these quality features of a hospital before selective hospitalisation is constantly increasing.

2.1.6 MRSA and glycopeptide consumption in hospitals

MRSA prevalence in clinics and hospitals is linked to the consumption of glycopeptide antibiotics, to the extent that significantly more glycopeptides are prescribed in hospitals with high MRSA prevalence [82], [83], [84], [85]; this again increases the selection pressure for glycopeptide-resistant enterococci [86], [87], another multi-resistant pathogen of nosocomial infections.

Documentation of the MRSA status of a patient is of paramount importance for the empirical therapy of nosocomial infections (with or without vancomycin?) [88]. In this context, it is also important to note that the treatment of an MSSA infection with vancomycin is not considered optimal therapy [89].

2.2. Are the measures demanded by the KRINKO recommendations medically and economically justified?

2.2.1. Single room isolation

Numerous studies have been published since the KRINKO recommendations were published. According to these studies' findings, it is still justifiable to recommend accommodation in single rooms (or in common rooms in case of cohort isolation) (Cat. IB) [16], [40], [41], [42], [43], [44], [90], [91]. Single room isolation provides the best guarantee for consistently implementing all required measures for preventing and controlling further spread of MRSA.

The nursing and medical staff, especially in specialised departments treating very seriously ill or immunosuppressed patients, face the almost daily challenges in clinical practice that construction and functional issues pose; and personnel-organisational resources do not allow for consistent single room isolation [92].

This problem is further exacerbated by the lack of funds for building and refurbishment activities, under manning [93], [94], [95], increasing prevalence of multi-resistant infectious agents (MRSA, VRE; multi-resistant Gram-negative pathogens) and a rise in the number of intensely immunocompromised patients [83], [96].

Since a whole set of measures is always implemented in prevention and control [97], the single contribution of individual components in the multi-barrier concept against nosocomial MRSA spread has not yet been proven by prospectively randomised trials. However, a meta-analysis published in 2004 concludes that implementation of the barrier measures recommended by CDCs is to be continued [98].

The same goes for a survey published by Aboelela et al. in the American Journal of Infection Control in 2006 [99]. Moreover, the authors of this study present the prerequisites for scientifically sound, randomised controlled trials in a much differentiated manner and in relation to the importance of individual hygiene measures in the multi-barrier concept. Such trials require an interdisciplinary study committee comprised of nursing scientists, clinicians, infectiologists, microbiologists, hospital hygienists, statisticians and administrative staff; all of which goes hand in hand with considerable expense and manpower requirements (estimated monocentric magnitude: at least 50,000 Euro; multicentric: several hundreds of thousands of Euro) and are only convincing and meaningful if compliance with the respective hygiene measures in both comparison groups is systematically and continually supervised.

Such trials are not practically feasible in treatment centres of German universities given the extremely limited financial and human resources.

Since no patient must receive worse medical care due to his/her colonisation or infection with a multi-resistant pathogen (see Point 2.3), nursing and medical staff are routinely forced to implement different forms of contact isolation instead of single room isolation [14].

In this respect, it has to be noted that:

  • The operators of hospitals must take into account the increasing prevalence of multi-resistant infectious pathogens (MRE) and the increasing share of stationary treated patients with risk factors for nosocomial infections, and must significantly increase the single-room ratio in the long term (to 50% and more) so as to effectively guarantee necessary single room isolation.
  • The nursing and medical staff should reach a written agreement with the responsible hospital hygienist on special measures of contact isolation for patients who are colonised or infected with multi-resistant pathogens and cannot be treated in a single room owing to limited resources; this agreement should be countersigned by the medical director and the director of administration [79], [100].

The study published by Cepeda et al. in 2005 [101] does not provide a valid answer to the question of whether it makes sense to isolate MRSA-colonised or -infected patients in single rooms in ICUs. Besides many other methodical deficits, hand disinfection compliance of 21% as observed by the authors annuls the effect of all additional measures.

Also, the findings of the monocentric observational study published by Nijssen et al. in 2005 [102] are neither appropriate for underpinning an IA nor an IB recommendation. It is especially unacceptable in ethical terms that nursing and medical staff was not informed about an MRSA case which was detected in the course of this study. This information can be life-saving for patients if systemic infection occurs, which needs to be treated with an MRSA-effective antibiotic as early as possible.

2.2.2 Special safety measures, such as wearing protective gowns and masks covering mouth and nose before entering the room

MRSA is able to persist in the inanimate environment of patients for weeks and even months after [103], [104], [105], [106], [107], [108], [109].

Patients who are being treated together with an MRSA-colonised patient in the same room run an increased risk of MRSA transmission [110], [111]. MRSA is not just transmitted to staff or other patients by direct contact with the patient but also by contact with contaminated objects or surfaces in the patients' environment [104], [110], [112], [113], [114], [115]. This is why preventing nosocomial MRSA transmission requires a great deal more in terms of personnel for routine environment disinfection [104], [109], [116], [117], [118]. Methods of applying detergents without added disinfectants instead of adequate surface disinfectants make a sizeable contribution to spreading MRSA on all “seemingly clean” surfaces [119].

Regarding MRSA-positive patients, the pathogen is most frequently found in the vestibules of the nose; a relevant share, however, also colonises other parts of the body, e.g. underarms (15%–25%), perineum (30%–40%) and hands and forearms (40%) [104]. In the case of some patients, an ongoing colonisation of the gastrointestinal tract can ensue, especially after an antibacterial therapy (disturbed colonisation resistance) [120], [121], [122], [123], [124]. MRSA is also found significantly more frequently on the skin of gastrointestinally colonised patients [125]. If these patients develop diarrhoea for other reasons (e.g. antibiotic-associated), massive contamination of the patient environment with MRSA might ensue [2].

Outlets of drainages, stomata, catheters and chronic wounds are also reservoirs of lasting colonisation. Surfaces of the inanimate environment in the isolation room are significantly more frequently contaminated in the case of patients with perineal MRSA colonisation [126].

The tenacity (resistance to unfavourable environmental factors) and spreading tendency of nosocomial MRSA isolates make it unsuitable to consider the MRSA colonisation of a patient statically and on the basis of a single swab series because the number of colonised areas can change daily.

For example, an “only nasally” colonised patient who catches a cold in hospital or coughs for other reasons (asthma, COPD, smoker), can become the starting point of massive MRSA contamination to the environment without a mask covering mouth and nose.

Many people often unconsciously touch their noses and thus possibly contaminate their hands and subsequently their environment with MRSA. If a mask covering mouth and nose is always worn outside the isolation room (in addition to hygienic hand disinfection) the probability of such a “hygiene error” is decreased.

In addition, a significant part of MRSA-colonised patients is not able to consistently stick to the required hygiene measures [127]. Problems in terms of compliance with hand hygiene [128], [129], [130], [131], [132], [133], [134] or the use of disposable gloves [135] arise again and again, even in case of well-trained and experienced nursing or medical service staff. In this context, it is unrealistic to act on the assumption of the ideal of a well-informed, judicious and cooperative patient who immediately and completely grasps all barrier measures and is able to consistently implement them [127], [136], [137].

There is an increased likelihood that nursing scrubs will be contaminated if additional, patient-related protective gowns are not worn [84], [104], [116], [138]. Since certain zones of nursing scrubs and objects [139] (bags, pagers, computers, ball-pens etc.) frequently come into contact with hands [140], [141], [142], [143], [144] in clinical practice, a pathogen might be secondarily transmitted from contaminated nursing scrubs to the hands of nursing and medical staff. Moreover, MRSA can be transmitted through droplet infection in case of nasal or pharyngeal colonisation or infections of the deeper respiratory tract. This by no means only applies to patients with infections of the upper airways or tracheostoma, although the risk is significantly increased in these situations [84].

Protective gowns stored in the room can be contaminated with MRSA before use. In this respect, it is advisable to store fresh protective gowns in front of the isolation room, in the sluice area or in a specific “MRSA carriage” [40], and to put on the protective gown and the mask covering mouth and nose before entering the isolation room and dispose of them when leaving the room.

Staff who wear a mask covering mouth and nose in the isolation room/(area), dispose of this mask when leaving the room/(area) and subsequently disinfect their hands have a reduced probability of unconsciously touching their own nasal mucosa with contaminated gloves.

Without discussing all specific shortfalls in conception and implementation in detail, it is merely worth noting that neither the examination on “droplet precautions” [145] published by Mangini et al. in 2007 nor the randomised monocentric trial on wearing protective gowns [146] published by Grant et al. in 2006 meet the method requirements of a sound and convincing scientific study regarding all these important problems and questions. For this reason, these papers should on no account be quoted as if their conclusions were scientifically proven facts.

2.2.3. Specific considerations on operations in MRSA-colonised or -infected patients
  • The question of when a patient will be operated is answered by the medical indications for the operation, and not the MRSA colonisation status.
  • Elective operations should always be postponed if sufficient time for a promising decolonisation attempt is available.
  • Necessary diagnostic and smaller therapeutic interventions can also be performed in procedures rooms – instead of isolation rooms – if firmly established procedures controlled by the hospital hygienist and hygiene experts for prevention and control (including subsequent disinfection) are guaranteed.
  • Disinfectant intermediate cleaning is extended to the patient-remote area (floors, not walls) in case of probable release of MRSA during the operation to the environment (e.g. MRSA colonisation or infection in the operation area). Before preparing the new operation drying of the disinfectant must be awaited.
  • The operating team must go through the airlock again in case of probable contamination of the surgery team's scrubs (including a change of shoes).

2.3. Do MRSA patients get worse medical/nursing care?

An oft-cited study by Stelfox et al. [147], and also other studies [148] has suggested that patients who were isolated due to a colonisation or infection with multi-resistant pathogens

  • are less frequently monitored and examined [149];
  • show more complications in clinical course; these complications could possibly be prevented in case of better continuous care.

These problems and the associated ethical questions are not specific to MRSA [150], [151], [152]. When interpreting the aforementioned studies it has to be considered though that they are merely observational studies without intervention. Yet, section 7 of the KRINKO recommendations needs to be specified for ethical reasons:

  • On principle, colonisation or infection with a multi-resistant pathogen must not result in patients receiving worse medical care and being denied medically indicated diagnostic and therapeutic measures.
  • Hospitals treating MRE-colonised or -infected patients must create the structural-organisational and staff requirements such that the necessary medical surveillance and care is also guaranteed for patients who must be isolated for reasons of infection prevention.
  • The recommendations for performing diagnostic procedures in an MRE-colonised patient in the isolation room must not result in an increased risk of undesired complications or worse surveillance of vital functions during or after the intervention.

2.4. Do the isolation measures result in restrictions in mobility, social stigmatisation and psychological stress of patients?

Patients who are isolated in an isolation room or in a correspondingly marked area due to an MRSA colonisation or infection

  • are restricted in their mobility;
  • run an increased risk of social isolation and stigmatisation;
  • are exposed to additional psychological stress [153];
  • are possibly unhappy with medical care.

These aspects of the utmost practical importance are not discussed in the KRINKO recommendations of 1999. In an observational study, increased anxiety and depression scores in isolated patients (because of MRSA or VRE) were found after just one week [154]. The authors of this investigation point out that it is merely an observational study without intervention.

They quote studies from the field of protective isolation within the context of allogeneic stem cell transplantations; these problems were anticipated in these studies and could be alleviated by suitable interventions.

Reference to studies discussing psychological stress of patients and relatives in the course of the SARS epidemic [155], [156] is not appropriate in this paper because separating patients from their relatives (or even separating children from their parents) is not necessary in case of an MRSA colonisation.

The following measures can be helpful:

  • Cooperative, judicious and mobile patients should be allowed to leave the isolation room, e.g. to go for a walk in the clinic's garden, after a written agreement has been made and a consultation with a physician has taken place. It is self-evident that direct or indirect contacts with other patients must be avoided.
  • In case of nasal or pharyngeal colonisation, the patient must wear a mask covering mouth and nose when leaving the room. All MRSA-colonised wounds must be covered meticulously with an adequate, liquid-proof dressing.
  • A specific treatment plan should be set up in conjunction with the hospital hygienist (hygiene experts) for patients who need physiotherapy treatment which cannot be given in the isolation room. The risk of transmitting MRSA can be minimised by subsequently thoroughly wet disinfecting all potentially contaminated surfaces with an approved disinfectant and by adhering to special safety measures, both seen to by the physiotherapists.
  • Isolation rooms for patients who can otherwise unrestrictedly communicate with their fellow patients and relatives should be equipped with a telephone, with radio, and with television but it has to be ensured that control panels can be regularly disinfected.
  • Transparent face protection shields instead of the usual mask covering mouth and nose should be developed for treating children and other patients who notably rely on non-verbal communication (reassuring and friendly signals, such as smiling etc.); these shields must protect against droplet infections.
  • Physicians and nurses explaining the necessity of isolation should also actively address the problem of additional psychological stress.
  • When calculating the necessary working time with patients, medical staff should allow for extra time for talking to patients.
  • The indication for professional psychological care of selected patients is given by the doctors in attendance.

The risk of social stigmatisation can be reduced by:

  • Marking the room's door with the information “intensive care” (the following safety measures must be adhered to, visitors should report to the ward staff...) instead of a warning sign which publicly communicates the patient's colonisation state without permission.
  • Information material informing patients and relatives about the meaning, transmission paths and required prevention and control measures of MRE [157].
  • Computer-aided automated alerts can be used in clinics with a digital patient documentation system for immediately isolating patients with known or highly likely MRSA colonisation upon the patients' admissions in such a way that patients must not be transferred from a common room during their hospitalisation [158], [159].

Patients' satisfaction with their medical care does not depend on the question of whether they are isolated or not, if the necessary extra time is considered in structural and organisational terms and if management is purposeful and far-sighted [160]. On the contrary, clinical experience often shows that patients properly cared for in this context feel particularly safe and experience the extra time allocated to them as positive [161].

It basically makes sense to instruct patients as partners in preventing nosocomial infections and also recommend hygienic hand disinfection to them (the same being applicable to nursing and medical staff) [137].

2.5. How to deal with medical and nursing staff who are MRSA carriers

According to a current survey [162], medical and nursing staff are more frequently colonised with MRSA [114], [118], [163] and are more often involved in nosocomial transmissions than originally thought [164]. The authors identify 18 studies, in which transmission from asymptomatic, MRSA-colonised staff to patients was proven with molecular biological typing methods, and 26 studies, in which such a transmission was very likely in epidemiological terms.

The hospital hygienist in charge, the clinic management and the on-site occupational health officer must decide on the necessary procedure regarding staff screening for MRSA. It might not make sense to limit staff screening to symptomatic staff.

Nurses and orderlies often feel more responsible for individual patients assigned to them than medical staff. They often want to be tested themselves if “their patients” have been found to have MRSA. This shows strongly developed hygiene awareness. Testing should thus be made possible after consultation of the hygiene experts. The same survey [162] makes further important information accessible:

  • 5% of all MRSA-positive staff (48 of 942 examined staff with available information) fell ill with an MRSA infection themselves.
  • In addition to nose swabs, pharynx swabs are required to safely exclude MRSA colonisation [165], [166], [167].
  • The success rate of an antiseptic decolonisation treatment combined with mupirocin nose ointment is excellent for medical staff (90% after 5 days; 93% after 10 days Mupirocin plus oral antibiotics, e.g. rifampicin and cotrimoxazole or doxycyclin). Additional benefits of supplementary preventive treatments with certain antibiotics (according to in vitro sensitivity testing, e.g. rifampicin, cotrimoxazole) have to be carefully weighed up against undesired effects to be expected.
  • In case of some staff, underlying diseases, such as chronic sinusitis [168], otitis externa [169] or chronic hand eczema [170] need to be treated concomitantly to obtain long-term decolonisation.
  • The domestic area (including certain pets) should be included in the respective intervention strategy [171], [172], [173], especially in case of staff who cannot be treated successfully.

The question of whether it is reasonable to temporarily release MRSA-colonised staff from near-patient activities during a decolonisation treatment must be decided on the job in a written standard, the drafting of which should include all relevant occupational groups including clinic management and administration.

Absenteeism must not be declared as “sick leave” in this context, and the costs for the decolonisation treatment of staff are to be borne by the hospital.

Since under manning of nursing staff is itself an independent risk factor for MRSA transmission in the context of outbreaks [94], [174], staff released from their duties must be temporarily replaced by additional staff.

If this is not possible MRSA-colonised staff should exclusively nurse MRSA-colonised patients – after another intensive briefing regarding the necessary barrier measures – until they have successfully been decolonised themselves.

2.6. Problems in the pre- and post-inpatient care area

Since not all MRSA-colonised patients have been successfully treated by the end of their hospitalisation [10], and the duration of inpatient treatment of patients is declining as a whole, more and more MRSA-colonised/-infected patients are discharged to outpatient care or to other treatment facilities (e.g. old people's homes and nursing homes) [4].

Further medical treatment of these patients is provided by physicians in private practices or specialist outpatient clinics, and many of these people are cared for by outpatient nursing services [175].

The special costs that are incurred by eradication treatment [176], microbiological follow-up or the extra time in outpatient care of MRSA-colonised or -infected patients have not been creditable so far. This funding void also affects MRSA screening of patients with increased risk of MRSA colonisation before elective inpatient hospitalisation [26], [78] as well as MRSA screening of family members of MRSA-positive patients. In this field, urgent action is needed by the legislators and cost-bearers of outpatient medical care.


Notes

Conflict of interest

None of the authors declares a conflict of interest.


References

1.
Rice LB. Antimicrobial resistance in gram-positive bacteria. Am J Med. 2006;119:S11-9; discussion S62-70. DOI: 10.1016/j.amjmed.2006.03.012 Externer Link
2.
Boyce JM, Cookson B, Christiansen K, Hori S, Vuopio-Varkila J, Kocagoz S, Oztop AY, Vandenbroucke-Grauls CM, Harbarth S, Pittet D. Meticillin-resistant Staphylococcus aureus. Lancet Infect Dis. 2005;5:653-63.
3.
Witte W, Kresken M, Braulke C, Cuny C. Increasing incidence and widespread dissemination of methicillin-resistant Staphylococcus aureus (MRSA) in hospitals in central Europe, with special reference to German hospitals. Clin Microbiol Infect. 1997;3:414-22. DOI: 10.1111/j.1469-0691.1997.tb00277.x Externer Link
4.
Daeschlein G, Assadian O, Rangous I, Kramer A. Risk factors for Staphylococcus aureus nasal carriage in residents of three nursing homes in Germany. J Hosp Infect. 2006;63:216-20. DOI: 10.1016/j.jhin.2005.12.014 Externer Link
5.
Woltering R, Hoffmann G, Daniels-Haardt I, Gastmeier P, Chaberny IF. MRSA-Prävalenz in medizinischen und pflegerischen Einrichtungen eines Landkreises [Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in patients in long-term care in hospitals, rehabilitation centers and nursing homes of a rural district in Germany]. Dtsch Med Wochenschr. 2008;133:999-1003. DOI: 10.1055/s-2008-1075683 Externer Link
6.
McGoldrick M, Rhinehart E. Managing multidrug-resistant organisms in home care and hospice: surveillance, prevention, and control. Home Healthc Nurse. 2007;25:580-6; quiz 7-8. DOI: 10.1097/01.NHH.0000296115.41320.f8 Externer Link
7.
Smith PW, Bennett G, Bradley S, Drinka P, Lautenbach E, Marx J, Mody L, Nicolle L, Stevenson K. SHEA/APIC guideline: infection prevention and control in the long-term care facility, July 2008. Infect Control Hosp Epidemiol. 2008;29:785-814. DOI: 10.1086/592416 Externer Link
8.
Eveillard M, Charru P, Rufat P, Hippeaux MC, Lancien E, Benselama F, Branger C. Methicillin-resistant Staphylococcus aureus carriage in a long-term care facility: hypothesis about selection and transmission. Age Ageing. 2008;37:294-9. DOI: 10.1093/ageing/afn021 Externer Link
9.
Heudorf U, Bremer V, Heuck D. MRSA-Besiedelung bei Bewohnern von Alten- und Pflegeheimen sowie bei Patienten einer geriatrischen Rehabilitationsklinik in Frankfurt am Main, 1999 [Methicillin-resistant Staphylococcus aureus in long-term care facilities for the aged in Frankfurt am Main, Germany, in 1999]. Gesundheitswesen. 2001;63:447-54. DOI: 10.1055/s-2001-15924 Externer Link
10.
Dettenkofer M, Widmer AF, Kern WV. MRSA und andere multiresistente Erreger: ein Problem zunehmend auch in der ambulanten Medizin [MRSA and other multi-resistant pathogens: an ever increasing problem even in ambulant medicine]. Dtsch Med Wochenschr. 2008;133:370-1. DOI: 10.1055/s-2008-1046722 Externer Link
11.
Kommission für Krankenhaushygiene und Infektionsprävention am Robert Koch-Institut. Kommentar zu den Empfehlungen zur Prävention von Methicillin-resistenten Staphylococcus aureus Stämmen in Krankenhäusern und anderen medizinschen Einrichtungen. Epidemiologisches Bulletin. 2004;46:396.
12.
Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch-Institut. Empfehlung zur Prävention und Kontrolle von Methicillin-resistenten Staphylococcus aureus-Stämmen (MRSA) in Krankenhäusern und anderen medizinischen Einrichtungen - Mitteilung der Kommission für Krankenhaushygiene und Infektionsprävention am RKI. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 1999;42:954-8.
13.
Coia JE, Duckworth GJ, Edwards DI, Farrington M, Fry C, Humphreys H, Mallaghan C, Tucker DR. Guidelines for the control and prevention of meticillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities. J Hosp Infect. 2006;63 Suppl 1:S1-44. DOI: 10.1016/j.jhin.2006.01.001 Externer Link
14.
Calfee DP, Salgado DC, Classen D, Arias KM, Podgorny K, Anderson DJ, Burstin H, Coffin SE, Dubberke ER, et al. Strategies to Prevent Transmission of Methicillin-Resistant Staphylococcus aureus in Acute Care Hospitals. Infect Control Hosp Epidemiol. 2008;29:S62-S80. DOI: 10.1086/591061 Externer Link
15.
Muto CA. Methicillin-Resistant Staphylococcus aureus Control: We Didn't Start the Fire, but It's Time to Put It Out. Infect Control Hosp Epidemiol. 2006;27:111-5. DOI: 10.1086/501489 Externer Link
16.
Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, Farr BM. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol. 2003;24:362-86. DOI: 10.1086/502213 Externer Link
17.
Kluytmans-Vandenbergh MF, Kluytmans JA, Voss A. Dutch guideline for preventing nosocomial transmission of highly resistant microorganisms (HRMO). Infection. 2005;33:309-13. DOI: 10.1007/s15010-005-5079-z Externer Link
18.
Wertheim HF, Vos MC, Boelens HA, Voss A, Vandenbroucke-Grauls CM, Meester MH, Kluytmans JA, van Keulen PH, Verbrugh HA. Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infect. 2004;56:321-5. DOI: 10.1016/j.jhin.2004.01.026 Externer Link
19.
Farr BM. Prevention and control of methicillin-resistant Staphylococcus aureus infections. Curr Opin Infect Dis. 2004;17:317-22. DOI: 10.1097/01.qco.0000136926.52673.cd Externer Link
20.
Robert Koch-Institut. Fachtagung der AG Nosokomiale Infektionen am RKI zur Intensivierung der Umsetzungen von Präventionsstrategien bei MRSA. Epidemiologisches Bulletin. 2005;5:31-7.
21.
Tiemersma EW, Bronzwaer SL, Lyytikainen O, Degener JE, Schrijnemakers P, Bruinsma N, Monen J, Witte W, Grundman H. Methicillin-resistant Staphylococcus aureus in Europe, 1999-2002. Emerg Infect Dis. 2004;10:1627-34.
22.
Friedrich AW, Daniels-Haardt I, Köck R, Verhoeven F, Mellmann A, Harmsen D, van Gemert-Pijnen JE, Becker K, Hendrix MG. EUREGIO MRSA-net Twente/Münsterland--a Dutch-German cross-border network for the prevention and control of infections caused by methicillin-resistant Staphylococcus aureus. Euro Surveill. 2008;13(35). pii: 18965.
23.
Friedrich AW, Witte W, de Lencastre H, Hryniewicz W, Scheres J, Westh H; SeqNet.org participants. A European laboratory network for sequence-based typing of methicillin-resistant Staphylococcus aureus (MRSA) as a communication platform between human and veterinary medicine--an update on SeqNet.org. Euro Surveill. 2008;13(19). pii: 18862.
24.
Gastmeier P, Witte W, Chaberny I. Zum Management des MRSA Screenings - Zur Praxis des aktuellen MRSA-Screenings an deutschen Universitätskliniken. Epidemiologisches Bulletin. 2005;(42):385-91.
25.
Chaberny IF, Schwab F, Ziesing S, Suerbaum S, Gastmeier P. Impact of routine surgical ward and intensive care unit admission surveillance cultures on hospital-wide nosocomial methicillin-resistant Staphylococcus aureus infections in a university hospital: an interrupted time-series analysis. J Antimicrob Chemother. 2008;62(6):1422-9. DOI: 10.1093/jac/dkn373 Externer Link
26.
Bartels C, Ewert R, Steinmetz I, Kramer A. Methicillin-resistente Staphylokokken - Frühes Screening senkt die Zahl der Infektionen. Dtsch Ärztebl. 2008;105:A672-A673.
27.
Kappstein I. Aktuelle MRSA-Problematik: Epidemiologie, Diagnostik, Pravention und Therapie [Current issues of methicillin-resistant Staphylococcus aureus: epidemiology, diagnostics, prevention, and therapy]. Chirurg. 2006;77:499-500, 502-5. DOI: 10.1007/s00104-006-1185-4 Externer Link
28.
Kappstein I, van der Mühlen K, Meschzan D, Vatou V, Bieg-Habermann S. Prävention von MRSA-Übertragungen: Standardhygiene statt Isolierung [Prevention of transmission of methicillin-resistant Staphylococcus aureus (MRSA) infection: standard precautions instead of isolation : A 6-year surveillance in a University hospital]. Chirurg. 2009;80(1):49-61. DOI: 10.1007/s00104-008-1565-z Externer Link
29.
Gastmeier P, Sohr D, Geffers C, Zuschneid I, Behnke M, Ruden H. Letalität auf deutschen Intensivstationen: Mit oder wegen nosokomialer Infektion? [Mortality in German intensive care units: dying from or with a nosocomial infection?]. Anasthesiol Intensivmed Notfallmed Schmerzther. 2005;40:267-72. DOI: 10.1055/s-2005-861354 Externer Link
30.
Kresken M, Hafner D. Resistenzsituation bei klinisch wichtigen Infektionserregern gegenüber Chemotherapeutika in Mitteleuropa. Ergebnisse einer multizentrischen Studie der Arbeitsgemeinschaft "Resistenz" in der Paul-Ehrlich-Gesellschaft für Chemotherapie e.V. aus dem Jahre 1998. Chemotherapie Journal. 2000;9:51-86.
31.
Kresken M, Hafner D, Schmitz FJ, Wichelhaus TA. Resistenzsituation bei klinisch wichtigen Infektionserregern gegenüber Antibiotika in Deutschland und im mitteleuropäischen Raum. Bericht über die Ergebnisse einer multizentrischen Studie der Arbeitsgemeinschaft Empfindlichkeitsprüfungen & Resistenz der Paul-Ehrlich-Gesellschaft für Chemotherapie e.V. aus dem Jahre 2004. Rheinbach: Antiinfectives Intelligence; 2006. Available from: http://www.p-e-g.org/ag_resistenz/PEG-Resistenzstudie%202004.pdf Externer Link
32.
Meyer E, Gastmeier P, Schwab F. The burden of multiresistant bacteria in German intensive care units. J Antimicrob Chemother. 2008;62(6):1474-6. DOI: 10.1093/jac/dkn391 Externer Link
33.
Gastmeier P, Schwab F, Geffers C, Ruden H. To isolate or not to isolate? Analysis of data from the German Nosocomial Infection Surveillance System regarding the placement of patients with methicillin-resistant Staphylococcus aureus in private rooms in intensive care units. Infect Control Hosp Epidemiol. 2004;25:109-13. DOI: 10.1086/502359 Externer Link
34.
Gastmeier P, Geffers C. Nosokomiale Infektionen in Deutschland: Wie viele gibt es wirklich? Eine Schätzung für das Jahr 2006 [Nosocomial infections in Germany. What are the numbers, based on the estimates for 2006?]. Dtsch Med Wochenschr. 2008;133:1111-5. DOI: 10.1055/s-2008-1077224 Externer Link
35.
Petersdorf S, Oberdorfer K, Wendt C. Longitudinal study of the molecular epidemiology of methicillin-resistant Staphylococcus aureus at a university hospital. J Clin Microbiol. 2006;44:4297-302. DOI: 10.1128/JCM.01168-06 Externer Link
36.
Infektionsschutzgesetz. Gesetz zur Verhütung und Bekämpfung von Infektionskrankheiten beim Menschen (Infektionsschutzgesetz - IfSG). Bundesgesetzblatt. 2000;1:1045.
37.
Robert Koch-Institut Berlin. Surveillance nosokomialer Infektionen sowie die Erfassung von Erregern mit speziellen Resistenzen und Multiresistenzen (§6 Abs.3 und §23 Abs.1 und 2 in Verbindung mit §4 Abs.2 Nr.2b IfSG. Rechtliche Voraussetzungen und Umsetzungsempfehlungen. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2000;43:887-90. DOI: 10.1007/s001030050376 Externer Link
38.
Robert Koch-Institut Berlin. Mitteilung der Kommission für Krankenhaushygiene und Infektionsprävention zur Surveillance (Erfassung und Bewertung) von nosokomialen Infektionen (Umsetzung von §23 IfSG). Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2001;44:523-6. DOI: 10.1007/s001030170027 Externer Link
39.
Daniels-Haardt I, Verhoeven F, Mellmann A, Hendrix MG, Gemert-Pijnen JE, Friedrich AW. EUREGIO-Projekt MRSA-net Twente/Münsterland. Regionale Netzwerkbildung zur Bekämpfung von MRSA [EUREGIO-projekt MRSA-net Twente/Munsterland. Creation of a regional network to combat MRSA]. Gesundheitswesen. 2006;68:674-8. DOI: 10.1055/s-2006-927258 Externer Link
40.
Trautmann M, Pollitt A, Loh U, Synowzik I, Reiter W, Stecher J, Rohs M, May U, Meyer E. Implementation of an intensified infection control program to reduce MRSA transmissions in a German tertiary care hospital. Am J Infect Control. 2007;35:643-9. DOI: 10.1016/j.ajic.2007.04.280 Externer Link
41.
Bootsma MC, Diekmann O, Bonten MJ. Controlling methicillin-resistant Staphylococcus aureus: Quantifying the effects of interventions and rapid diagnostic testing. Proc Natl Acad Sci U S A. 2006;103(14):5620-5. DOI: 10.1073/pnas.0510077103 Externer Link
42.
Wernitz MH, Swidsinski S, Weist K, Sohr D, Witte W, Franke KP, Roloff D, Ruden H, Veit SK. Effectiveness of a hospital-wide selective screening programme for methicillin-resistant Staphylococcus aureus (MRSA) carriers at hospital admission to prevent hospital-acquired MRSA infections. Clin Microbiol Infect. 2005;11:457-65. DOI: 10.1111/j.1469-0691.2005.01152.x Externer Link
43.
Karchmer TB, Durbin LJ, Simonton BM, Farr BM. Cost-effectiveness of active surveillance cultures and contact/droplet precautions for control of methicillin-resistant Staphylococcus aureus. J Hosp Infect. 2002;51:126-32. DOI: 10.1053/jhin.2002.1200 Externer Link
44.
Safdar N, Marx J, Meyer NA, Maki DG. Effectiveness of preemptive barrier precautions in controlling nosocomial colonization and infection by methicillin-resistant Staphylococcus aureus in a burn unit. Am J Infect Control. 2006;34:476-83. DOI: 10.1016/j.ajic.2006.01.011 Externer Link
45.
Harberg D. Society for Healthcare Epidemiology of America guideline approach works to control a methicillin-resistant Staphylococcus aureus outbreak. Infect Control Hosp Epidemiol. 2005;26:115-6. DOI: 10.1086/503509 Externer Link
46.
Hartstein AI, Denny MA, Morthland VH, LeMonte AM, Pfaller MA. Control of methicillin-resistant Staphylococcus aureus in a hospital and an intensive care unit. Infect Control Hosp Epidemiol. 1995;16:405-11.
47.
Kotilainen P, Routamaa M, Peltonen R, Evesti P, Eerola E, Salmenlinna S, Vuopio-Varkila J, Rossi T. Eradication of methicillin-resistant Staphylococcus aureus from a health center ward and associated nursing home. Arch Intern Med. 2001;161:859-63. DOI: 10.1001/archinte.161.6.859 Externer Link
48.
Kotilainen P, Routamaa M, Peltonen R, Oksi J, Rintala E, Meurman O, Lehtonen OP, Eerola E, Salmenlinna S, Vuopio-Varkila J, Rossi T. Elimination of epidemic methicillin-resistant Staphylococcus aureus from a university hospital and district institutions, Finland. Emerg Infect Dis. 2003;9:169-75.
49.
Tomic V, Svetina Sorli P, Trinkaus D, Sorli J, Widmer AF, Trampuz A. Comprehensive strategy to prevent nosocomial spread of methicillin-resistant Staphylococcus aureus in a highly endemic setting. Arch Intern Med. 2004;164:2038-43. DOI: 10.1001/archinte.164.18.2038 Externer Link
50.
Vandenbroucke-Grauls CM, Frenay HM, van Klingeren B, Savelkoul TF, Verhoef J. Control of epidemic methicillin-resistant Staphylococcus aureus in a Dutch university hospital. Eur J Clin Microbiol Infect Dis. 1991;10:6-11. DOI: 10.1007/BF01967090 Externer Link
51.
Vos MC, Ott A, Verbrugh HA. Successful search-and-destroy policy for methicillin-resistant Staphylococcus aureus in The Netherlands. J Clin Microbiol. 2005;43: 2034; author reply 2034-5. DOI: 10.1128/JCM.43.4.2034-2035.2005 Externer Link
52.
Otter JA, Klein JL, Watts TL, Kearns AM, French GL. Identification and control of an outbreak of ciprofloxacin-susceptible EMRSA-15 on a neonatal unit. J Hosp Infect. 2007;67:232-9. DOI: 10.1016/j.jhin.2007.07.024 Externer Link
53.
Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5:751-62. DOI: 10.1016/S1473-3099(05)70295-4 Externer Link
54.
Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, van Keulen PH, Vandenbroucke-Grauls CM, Meester MH, Verbrugh HA. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet. 2004;364:703-5. DOI: 10.1016/S0140-6736(04)16897-9 Externer Link
55.
Kalmeijer MD, van Nieuwland-Bollen E, Bogaers-Hofman D, de Baere GA. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect Control Hosp Epidemiol. 2000;21:319-23. DOI: 10.1086/501763 Externer Link
56.
Munoz P, Hortal J, Giannella M, Barrio JM, Rodriguez-Creixems M, Perez MJ, Rincon C, Bouza E. Nasal carriage of S. aureus increases the risk of surgical site infection after major heart surgery. J Hosp Infect. 2008;68:25-31. DOI: 10.1016/j.jhin.2007.08.010 Externer Link
57.
Safdar N, Bradley EA. The risk of infection after nasal colonization with Staphylococcus aureus. Am J Med. 2008;121:310-5. DOI: 10.1016/j.amjmed.2007.07.034 Externer Link
58.
Lederer SR, Riedelsdorf G, Schiffl H. Nasal carriage of meticillin resistant Staphylococcus aureus: the prevalence, patients at risk and the effect of elimination on outcomes among outclinic haemodialysis patients. Eur J Med Res. 2007;12:284-8.
59.
Edmond MB, Ober JF, Bearman G. Active surveillance cultures are not required to control MRSA infections in the critical care setting. Am J Infect Control. 2008;36:461-3. DOI: 10.1016/j.ajic.2007.09.011 Externer Link
60.
Yokoe DS, Classen D. Improving Patient Safety Through Infection Control: A New Healthcare Imperative. Infect Control Hosp Epidemiol. 2008;29:S3-S11. DOI: 10.1086/591063 Externer Link
61.
Lepelletier D. Staphylococcus aureus résistant à la méticilline: incidence, facteurs de risque de colonisation et intérêt du dépistage systématique en unité de soins intensifs et réanimation [Meticillin-resistant Staphylococcus aureus: incidence, risk factors and interest of systematic screening for colonization in intensive-care unit]. Ann Fr Anesth Reanim. 2006;25:626-32. DOI: 10.1016/j.annfar.2006.01.016 Externer Link
62.
Simon A, Schaaf F, Marklein G, Exner M. Methicillin-resistente Staphylococcus aureus [MRSA]. Übersicht zu Bedeutung und Management in der stationären Kinderheilkunde. Hyg Med. 2003;28:62-74.
63.
Gerber SI, Jones RC, Scott MV, Price JS, Dworkin MS, Filippell MB, Rearick T, Pur SL, McAuley JB, et al. Management of Outbreaks of Methicillin-Resistant Staphylococcus aureus Infection in the Neonatal Intensive Care Unit: A Consensus Statement. Infect Control Hosp Epidemiol. 2006;27:139-45. DOI: 10.1086/501216 Externer Link
64.
Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch-Insitut. Empfehlung zur Prävention nosokomialer Infektionen bei neonatologischen Intensivpflegepatienten mit einem Geburtsgewicht unter 1500 g. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2007;50:1265-303. DOI: 10.1007/s00103-007-0337-0 Externer Link
65.
Vriens MR, Fluit AC, Troelstra A, Verhoef J, van der Werken C. Is methicillin-resistant Staphylococcus aureus more contagious than methicillin-susceptible S. aureus in a surgical intensive care unit? Infect Control Hosp Epidemiol. 2002;23:491-4. DOI: 10.1086/502094 Externer Link
66.
Shams WE, Rapp RP. Methicillin-resistant staphylococcal infections: an important consideration for orthopedic surgeons. Orthopedics. 2004;27:565-8.
67.
Reed SD, Friedman JY, Engemann JJ, Griffiths RI, Anstrom KJ, Kaye KS, Stryjewski ME, Szczech LA, Reller LB, et al. Costs and outcomes among hemodialysis-dependent patients with methicillin-resistant or methicillin-susceptible Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol. 2005;26:175-83. DOI: 10.1086/502523 Externer Link
68.
Cosgrove SE. The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clin Infect Dis. 2006;42 Suppl 2:S82-9. DOI: 10.1086/499406 Externer Link
69.
Cosgrove SE, Qi Y, Kaye KS, Harbarth S, Karchmer AW, Carmeli Y. The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges. Infect Control Hosp Epidemiol. 2005;26:166-74. DOI: 10.1086/502522 Externer Link
70.
Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis. 2003;36:53-9. DOI: 10.1086/345476 Externer Link
71.
Thompson DS, Workman R, Strutt M. Contribution of acquired meticillin-resistant Staphylococcus aureus bacteraemia to overall mortality in a general intensive care unit. J Hosp Infect. 2008;70(3):223-7. DOI: 10.1016/j.jhin.2008.07.004 Externer Link
72.
Blot SI, Vandewoude KH, Hoste EA, Colardyn FA. Outcome and attributable mortality in critically Ill patients with bacteremia involving methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Arch Intern Med. 2002;162:2229-35. DOI: 10.1001/archinte.162.19.2229 Externer Link
73.
Shurland S, Zhan M, Bradham DD, Roghmann MC. Comparison of mortality risk associated with bacteremia due to methicillin-resistant and methicillin-susceptible Staphylococcus aureus. Infect Control Hosp Epidemiol. 2007;28:273-9. DOI: 10.1086/512627 Externer Link
74.
Haley RW, Cushion NB, Tenover FC, Bannerman TL, Dryer D, Ross J, Sanchez PJ, Siegel JD. Eradication of endemic methicillin-resistant Staphylococcus aureus infections from a neonatal intensive care unit. J Infect Dis. 1995;171:614-24.
75.
Vidaur L, Planas K, Sierra R, Dimopoulos G, Ramirez A, Lisboa T, Rello J. Ventilator-associated pneumonia: impact of organisms on clinical resolution and medical resources utilization. Chest. 2008;133:625-32. DOI: 10.1378/chest.07-2020 Externer Link
76.
Gould IM. Costs of hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) and its control. Int J Antimicrob Agents. 2006;28:379-84. DOI: 10.1016/j.ijantimicag.2006.09.001 Externer Link
77.
Wernitz MH, Keck S, Swidsinski S, Schulz S, Veit SK. Cost analysis of a hospital-wide selective screening programme for methicillin-resistant Staphylococcus aureus (MRSA) carriers in the context of diagnosis related groups (DRG) payment. Clin Microbiol Infect. 2005;11:466-71. DOI: 10.1111/j.1469-0691.2005.01153.x Externer Link
78.
Diller R, Sonntag AK, Mellmann A, Grevener K, Senninger N, Kipp F, Friedrich AW. Evidence for cost reduction based on pre-admission MRSA screening in general surgery. Int J Hyg Environ Health. 2008;211:205-12. DOI: 10.1016/j.ijheh.2007.06.001 Externer Link
79.
Zell BL, Goldmann DA. Healthcare-associated infection and antimicrobial resistance: moving beyond description to prevention. Infect Control Hosp Epidemiol. 2007;28:261-4. DOI: 10.1086/513722 Externer Link
80.
Boyce JM. Consequences of inaction: importance of infection control practices. Clin Infect Dis. 2001;33 Suppl 3:S133-7. DOI: 10.1086/321839 Externer Link
81.
Gortner L, Borkhardt A, Reiss I. Consequences of scientific reports of complications. Lancet. 2000;356:2015. DOI: 10.1016/S0140-6736(05)72992-5 Externer Link
82.
Rogues AM, Dumartin C, Amadeo B, Venier AG, Marty N, Parneix P, Gachie JP. Relationship between rates of antimicrobial consumption and the incidence of antimicrobial resistance in Staphylococcus aureus and Pseudomonas aeruginosa isolates from 47 French hospitals. Infect Control Hosp Epidemiol. 2007;28:1389-95. DOI: 10.1086/523280 Externer Link
83.
Farr BM, Salgado CD, Karchmer TB, Sherertz RJ. Can antibiotic-resistant nosocomial infections be controlled? Lancet Infect Dis. 2001;1:38-45. DOI: 10.1016/S1473-3099(01)00020-2 Externer Link
84.
Snyder GM, Thom KA, Furuno JP, Perencevich EN, Roghmann MC, Strauss SM, Netzer G, Harris AD. Detection of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on the gowns and gloves of healthcare workers. Infect Control Hosp Epidemiol. 2008;29:583-9. DOI: 10.1086/588701 Externer Link
85.
Rogues AM, Dumartin C, Lasheras A, Venier AG, Fourrier A, Parneix P, Gachie JP. Determinants of glycopeptides consumption in hospitals. Microb Drug Resist. 2007;13:199-203. DOI: 10.1089/mdr.2007.754 Externer Link
86.
Murray BE. Vancomycin-resistant enterococcal infections. N Engl J Med. 2000;342:710-21. DOI: 10.1056/NEJM200003093421007 Externer Link
87.
Wendt C, Rüden H, Edmond M. Vancomycin-resistente Enterokokken - Epidemiologie, Risikofaktoren und Prävention. Dtsch Ärztebl. 1998;95:A1604-A1611.
88.
Schweizer ML, Furuno JP, Harris AD, McGregor JC, Thom KA, Johnson JK, Shardell MD, Perencevich EN. Clinical utility of infection control documentation of prior methicillin-resistant Staphylococcus aureus colonization or infection for optimization of empirical antibiotic therapy. Infect Control Hosp Epidemiol. 2008;29:972-4. DOI: 10.1086/590665 Externer Link
89.
Kopp BJ, Nix DE, Armstrong EP. Clinical and economic analysis of methicillin-susceptible and -resistant Staphylococcus aureus infections. Ann Pharmacother. 2004;38:1377-82. DOI: 10.1345/aph.1E028 Externer Link
90.
Chaix C, Durand-Zaleski I, Alberti C, Brun-Buisson C. Control of endemic methicillin-resistant Staphylococcus aureus: a cost-benefit analysis in an intensive care unit. Jama. 1999;282:1745-51. DOI: 10.1001/jama.282.18.1745 Externer Link
91.
Bracco D, Dubois MJ, Bouali R, Eggimann P. Single rooms may help to prevent nosocomial bloodstream infection and cross-transmission of methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med. 2007;33:836-40. DOI: 10.1007/s00134-007-0559-5 Externer Link
92.
Beaujean D, Blok H, Gigengack-Baars A, Kamp-Hopmans T, Ballemans K, Verhoef J, Weersink A. Five-year surveillance of patients with communicable diseases nursed in isolation. J Hosp Infect. 2001;47:210-7. DOI: 10.1053/jhin.2000.0899 Externer Link
93.
Stone PW, Pogorzelska M, Kunches L, Hirschhorn LR. Hospital staffing and health care-associated infections: a systematic review of the literature. Clin Infect Dis. 2008;47:937-44. DOI: 10.1086/591696 Externer Link
94.
Andersen BM, Lindemann R, Bergh K, Nesheim BI, Syversen G, Solheim N, Laugerud F. Spread of methicillin-resistant Staphylococcus aureus in a neonatal intensive unit associated with understaffing, overcrowding and mixing of patients. J Hosp Infect. 2002;50:18-24. DOI: 10.1053/jhin.2001.1128 Externer Link
95.
Grundmann H, Hori S, Winter B, Tami A, Austin DJ. Risk factors for the transmission of methicillin-resistant Staphylococcus aureus in an adult intensive care unit: fitting a model to the data. J Infect Dis. 2002;185:481-8. DOI: 10.1086/338568 Externer Link
96.
Safdar N, Maki DG. The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, enterococcus, gram-negative bacilli, Clostridium difficile, and Candida. Ann Intern Med. 2002;136:834-44.
97.
Boyce JM, Havill NL, Kohan C, Dumigan DG, Ligi CE. Do infection control measures work for methicillin-resistant Staphylococcus aureus? Infect Control Hosp Epidemiol. 2004;25:395-401. DOI: 10.1086/502412 Externer Link
98.
Cooper BS, Stone SP, Kibbler CC, Cookson BD, Roberts JA, Medley GF, Duckworth G, Lai R, Ebrahim S. Isolation measures in the hospital management of methicillin resistant Staphylococcus aureus (MRSA): systematic review of the literature. Bmj. 2004;329:533. DOI: 10.1136/bmj.329.7465.533 Externer Link
99.
Aboelela SW, Saiman L, Stone P, Lowy FD, Quiros D, Larson E. Effectiveness of barrier precautions and surveillance cultures to control transmission of multidrug-resistant organisms: a systematic review of the literature. Am J Infect Control. 2006;34:484-94. DOI: 10.1016/j.ajic.2006.03.008 Externer Link
100.
Institute for Healthcare Improvement. Reduce Methicillin-Resistant Staphylococcus aureus (MRSA) Infection. Getting Started Kit: How-to Guide. Cambridge, MA: IHI; 2008. Available from: http://www.ihi.org/IHI/Programs/Campaign/MRSAInfection.htm. Externer Link
101.
Cepeda JA, Whitehouse T, Cooper B, Hails J, Jones K, Kwaku F, Taylor L, Hayman S, Cookson B, et al. Isolation of patients in single rooms or cohorts to reduce spread of MRSA in intensive-care units: prospective two-centre study. Lancet. 2005;365:295-304.
102.
Nijssen S, Bonten MJ, Weinstein RA. Are active microbiological surveillance and subsequent isolation needed to prevent the spread of methicillin-resistant Staphylococcus aureus? Clin Infect Dis. 2005;40:405-9. DOI: 10.1086/427281 Externer Link
103.
Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis. 2006;6:130. DOI: 10.1186/1471-2334-6-130 Externer Link
104.
Dancer SJ. Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Dis. 2007;8(2):101-13. DOI: 10.1016/S1473-3099(07)70241-4 Externer Link
105.
Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis. 2004;39:1182-9. DOI: 10.1086/424667 Externer Link
106.
Rutala WA, Weber DJ. Disinfection and sterilization in health care facilities: what clinicians need to know. Clin Infect Dis. 2004;39:702-9. DOI: 10.1086/423182 Externer Link
107.
Rutala WA, Weber DJ. The benefits of surface disinfection. Am J Infect Control. 2004;32:226-31. DOI: 10.1016/j.ajic.2004.04.197 Externer Link
108.
Rutala WA, White MS, Gergen MF, Weber DJ. Bacterial contamination of keyboards: efficacy and functional impact of disinfectants. Infect Control Hosp Epidemiol. 2006;27:372-7. DOI: 10.1086/503340 Externer Link
109.
Goodman ER, Platt R, Bass R, Onderdonk AB, Yokoe DS, Huang SS. Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms. Infect Control Hosp Epidemiol. 2008;29:593-9. DOI: 10.1086/588566 Externer Link
110.
Moore C, Dhaliwal J, Tong A, Eden S, Wigston C, Willey B, McGeer A. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) acquisition in roommate contacts of patients colonized or infected with MRSA in an acute-care hospital. Infect Control Hosp Epidemiol. 2008;29:600-6. DOI: 10.1086/588567 Externer Link
111.
Chaberny IF, Ziesing S, Mattner F, Barwolff S, Brandt C, Eckmanns T, Ruden H, Sohr D, Weist K, Gastmeier P. The burden of MRSA in four German university hospitals. Int J Hyg Environ Health. 2005;208:447-53. DOI: 10.1016/j.ijheh.2005.08.004 Externer Link
112.
Bhalla A, Pultz NJ, Gries DM, Ray AJ, Eckstein EC, Aron DC, Donskey CJ. Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients. Infect Control Hosp Epidemiol. 2004;25:164-7. DOI: 10.1086/502369 Externer Link
113.
Harris AD. How important is the environment in the emergence of nosocomial antimicrobial-resistant bacteria? Clin Infect Dis. 2008;46:686-8. DOI: 10.1086/527395 Externer Link
114.
Lin YC, Lauderdale TL, Lin HM, Chen PC, Cheng MF, Hsieh KS, Liu YC. An outbreak of methicillin-resistant Staphylococcus aureus infection in patients of a pediatric intensive care unit and high carriage rate among health care workers. J Microbiol Immunol Infect. 2007;40:325-34.
115.
Hardy KJ, Oppenheim BA, Gossain S, Gao F, Hawkey PM. A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA. Infect Control Hosp Epidemiol. 2006;27:127-32. DOI: 10.1086/500622 Externer Link
116.
Mundy LM. Contamination, acquisition, and transmission of pathogens: implications for research and practice of infection control. Infect Control Hosp Epidemiol. 2008;29:590-2. DOI: 10.1086/589558 Externer Link
117.
Bartels MD, Kristoffersen K, Slotsbjerg T, Rohde SM, Lundgren B, Westh H. Environmental meticillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide. J Hosp Infect. 2008;70:35-41.
118.
Rashid A, Solomon LK, Lewis HG, Khan K. Outbreak of epidemic methicillin-resistant Staphylococcus aureus in a regional burns unit: management and implications. Burns. 2006;32:452-7. DOI: 10.1016/j.burns.2005.10.016 Externer Link
119.
Exner M, Vacata V, Hornei B, Dietlein E, Gebel J. Household cleaning and surface disinfection: new insights and strategies. J Hosp Infect. 2004;56 Suppl 2:S70-5. DOI: 10.1016/j.jhin.2003.12.037 Externer Link
120.
Boyce JM, Havill NL, Maria B. Frequency and possible infection control implications of gastrointestinal colonization with methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:5992-5. DOI: 10.1128/JCM.43.12.5992-5995.2005 Externer Link
121.
Boyce JM, Havill NL, Otter JA, Adams NM. Widespread environmental contamination associated with patients with diarrhea and methicillin-resistant Staphylococcus aureus colonization of the gastrointestinal tract. Infect Control Hosp Epidemiol. 2007;28:1142-7. DOI: 10.1086/520737 Externer Link
122.
Cerda E, Abella A, de la Cal MA, Lorente JA, Garcia-Hierro P, van Saene HK, Alia I, Aranguren A. Enteral vancomycin controls methicillin-resistant Staphylococcus aureus endemicity in an intensive care burn unit: a 9-year prospective study. Ann Surg. 2007;245:397-407. DOI: 10.1097/01.sla.0000250418.14359.31 Externer Link
123.
Klotz M, Zimmermann S, Opper S, Heeg K, Mutters R. Possible risk for re-colonization with methicillin-resistant Staphylococcus aureus (MRSA) by faecal transmission. Int J Hyg Environ Health. 2005;208:401-5. DOI: 10.1016/j.ijheh.2005.05.004 Externer Link
124.
Squier C, Rihs JD, Risa KJ, Sagnimeni A, Wagener MM, Stout J, Muder RR, Singh N. Staphylococcus aureus rectal carriage and its association with infections in patients in a surgical intensive care unit and a liver transplant unit. Infect Control Hosp Epidemiol. 2002;23:495-501. DOI: 10.1086/502095 Externer Link
125.
Bhalla A, Aron DC, Donskey CJ. Staphylococcus aureus intestinal colonization is associated with increased frequency of S. aureus on skin of hospitalized patients. BMC Infect Dis. 2007;7:105. DOI: 10.1186/1471-2334-7-105 Externer Link
126.
Rohr U, Kaminski A, Wilhelm M, Jurzik L, Gatermann S, Muhr G. Colonization of patients and contamination of the patients' environment by MRSA under conditions of single-room isolation. Int J Hyg Environ Health. 2009;212(2):209-15. DOI: 10.1016/j.ijheh.2008.05.003 Externer Link
127.
Anderson DJ, Chen LF, Schmader KE, Sexton DJ, Choi Y, Link K, Sloane R, Kaye KS. Poor functional status as a risk factor for surgical site infection due to methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol. 2008;29:832-9. DOI: 10.1086/590124 Externer Link
128.
Harbarth S, Pittet D, Grady L, Goldmann DA. Compliance with hand hygiene practice in pediatric intensive care. Pediatr Crit Care Med. 2001;2:311-4. DOI: 10.1097/00130478-200110000-00004 Externer Link
129.
Harbarth S, Pittet D, Grady L, Zawacki A, Potter-Bynoe G, Samore MH, Goldmann DA. Interventional study to evaluate the impact of an alcohol-based hand gel in improving hand hygiene compliance. Pediatr Infect Dis J. 2002;21:489-95. DOI: 10.1097/00006454-200206000-00002 Externer Link
130.
Boyce JM, Pittet D. Guideline for Hand Hygiene in Health-Care Settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Infect Control Hosp Epidemiol. 2002;23:S3-40. DOI: 10.1086/503164 Externer Link
131.
Aboelela SW, Stone PW, Larson EL. Effectiveness of bundled behavioural interventions to control healthcare-associated infections: a systematic review of the literature. J Hosp Infect. 2007;66:101-8. DOI: 10.1016/j.jhin.2006.10.019 Externer Link
132.
Pittet D. Improving compliance with hand hygiene in hospitals. Infect Control Hosp Epidemiol. 2000;21:381-6. DOI: 10.1086/501777 Externer Link
133.
Trampuz A, Widmer AF. Hand hygiene: a frequently missed lifesaving opportunity during patient care. Mayo Clin Proc. 2004;79:109-16. DOI: 10.4065/79.1.109 Externer Link
134.
Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch Institut. Händehygiene - Mitteilung der Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch-Institut. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2000;43:230-3. DOI: 10.1007/s001030050042 Externer Link
135.
McBryde ES, Bradley LC, Whitby M, McElwain DL. An investigation of contact transmission of methicillin-resistant Staphylococcus aureus. J Hosp Infect. 2004;58:104-8. DOI: 10.1016/j.jhin.2004.06.010 Externer Link
136.
Malani PN. Commentary: debility and the risk for surgical site infection: defining the next steps. Infect Control Hosp Epidemiol. 2008;29:840-1. DOI: 10.1086/591324 Externer Link
137.
Tomic V, Ursic V, Seme K. Has the Time Come to Recommend the Use of Alcohol-Based Hand Rub to Hospitalized Patients? Infect Control Hosp Epidemiol. 2008;29:987-9. DOI: 10.1086/591031 Externer Link
138.
Boyce JM, Potter-Bynoe G, Chenevert C, King T. Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol. 1997;18:622-7.
139.
Panhotra BR, Saxena AK, Al-Mulhim AS. Contamination of patients' files in intensive care units: an indication of strict handwashing after entering case notes. Am J Infect Control. 2005;33:398-401. DOI: 10.1016/j.ajic.2004.12.009 Externer Link
140.
Neely AN, Maley MP. Dealing with contaminated computer keyboards and microbial survival. Am J Infect Control. 2001;29:131-2. DOI: 10.1067/mic.2001.114664 Externer Link
141.
Neely AN, Sittig DF. Basic microbiologic and infection control information to reduce the potential transmission of pathogens to patients via computer hardware. J Am Med Inform Assoc. 2002;9:500-8. DOI: 10.1197/jamia.M1082 Externer Link
142.
Beer D, Vandermeer B, Brosnikoff C, Shokoples S, Rennie R, Forgie S. Bacterial Contamination of Health Care Workers' Pagers and the Efficacy of Various Disinfecting Agents. Pediatr Infect Dis J. 2006;25:1074-5. DOI: 10.1097/01.inf.0000242649.27400.94 Externer Link
143.
Nunez S, Moreno A, Green K, Villar J. The stethoscope in the Emergency Department: a vector of infection? Epidemiol Infect. 2000;124:233-7. DOI: 10.1017/S0950268800003563 Externer Link
144.
Smith MA, Mathewson JJ, Ulert IA, Scerpella EG, Ericsson CD. Contaminated stethoscopes revisited. Arch Intern Med. 1996;156:82-4. DOI: 10.1001/archinte.156.1.82 Externer Link
145.
Mangini E, Segal-Maurer S, Burns J, Avicolli A, Urban C, Mariano N, Grenner L, Rosenberg C, Rahal JJ. Impact of contact and droplet precautions on the incidence of hospital-acquired methicillin-resistant Staphylococcus aureus infection. Infect Control Hosp Epidemiol. 2007;28:1261-6. DOI: 10.1086/521658 Externer Link
146.
Grant J, Ramman-Haddad L, Dendukuri N, Libman MD. The role of gowns in preventing nosocomial transmission of methicillin-resistant Staphylococcus aureus (MRSA): gown use in MRSA control. Infect Control Hosp Epidemiol. 2006;27:191-4. DOI: 10.1086/500623 Externer Link
147.
Stelfox HT, Bates DW, Redelmeier DA. Safety of patients isolated for infection control. Jama. 2003;290:1899-905. DOI: 10.1001/jama.290.14.1899 Externer Link
148.
Kirkland KB, Weinstein JM. Adverse effects of contact isolation. Lancet. 1999;354:1177-8. DOI: 10.1016/S0140-6736(99)04196-3 Externer Link
149.
Saint S, Higgins LA, Nallamothu BK, Chenoweth C. Do physicians examine patients in contact isolation less frequently? A brief report. Am J Infect Control. 2003;31:354-6. DOI: 10.1016/S0196-6553(02)48250-8 Externer Link
150.
Coia JE, Duckworth G, Edwards DI, Farrington M, Humphreys H, Mallaghan C, Tucker DR. MRSA behind bars? J Hosp Infect. 2006;63:354-5; author reply 356-7. DOI: 10.1016/j.jhin.2006.03.004 Externer Link
151.
Santos RP, Mayo TW, Siegel JD. Healthcare epidemiology: active surveillance cultures and contact precautions for control of multidrug-resistant organisms: ethical considerations. Clin Infect Dis. 2008;47:110-6. DOI: 10.1086/588789 Externer Link
152.
Bryan CS, Call TJ, Elliott KC. The ethics of infection control: philosophical frameworks. Infect Control Hosp Epidemiol. 2007;28:1077-84. DOI: 10.1086/519863 Externer Link
153.
Hartmann C. Wie erleben Patienten die Isolierung wegen einer Infektion oder Kolonisierung mit MRSA? [How do patients experience isolation due to an infection or colonisation with MRSA?]. Pflege Z. 2006;59:suppl 2-8.
154.
Catalano G, Houston SH, Catalano MC, Butera AS, Jennings SM, Hakala SM, Burrows SL, Hickey MG, Duss CV, et al. Anxiety and depression in hospitalized patients in resistant organism isolation. South Med J. 2003;96:141-5. DOI: 10.1097/01.SMJ.0000050683.36014.2E Externer Link
155.
Koller DF, Nicholas DB, Goldie RS, Gearing R, Selkirk EK. Bowlby and Robertson revisited: the impact of isolation on hospitalized children during SARS. J Dev Behav Pediatr. 2006;27:134-40.
156.
Koller DF, Nicholas DB, Goldie RS, Gearing R, Selkirk EK. When family-centered care is challenged by infectious disease: pediatric health care delivery during the SARS outbreaks. Qual Health Res. 2006;16:47-60. DOI: 10.1177/1049732305284010 Externer Link
157.
Robert J, Renard L, Grenet K, Galerne E, Dal Farra A, Aussant M, Jarlier V. Implementation of isolation precautions: role of a targeted information flyer. J Hosp Infect. 2006;62:163-5. DOI: 10.1016/j.jhin.2005.07.003 Externer Link
158.
Kho AN, Dexter PR, Warvel JS, Belsito AW, Commiskey M, Wilson SJ, Hui SL, McDonald CJ. An effective computerized reminder for contact isolation of patients colonized or infected with resistant organisms. Int J Med Inform. 2008;77:194-8. DOI: 10.1016/j.ijmedinf.2007.02.005 Externer Link
159.
Evans RS, Wallace CJ, Lloyd JF, Taylor CW, Abouzelof RH, Sumner S, Johnson KV, Wuthrich A, Harbarth S, Samore MH. Rapid identification of hospitalized patients at high risk for MRSA carriage. J Am Med Inform Assoc. 2008;15:506-12. DOI: 10.1197/jamia.M2721 Externer Link
160.
Gasink LB, Singer K, Fishman NO, Holmes WC, Weiner MG, Bilker WB, Lautenbach E. Contact isolation for infection control in hospitalized patients: is patient satisfaction affected? Infect Control Hosp Epidemiol. 2008;29:275-8. DOI: 10.1086/527508 Externer Link
161.
Safdar N, Maki DG. Quality of care and satisfaction among patients isolated for infection control. Jama. 2004;291:420-1; author reply 421-2. DOI: 10.1001/jama.291.4.420-b Externer Link
162.
Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? Lancet Infect Dis. 2008;8:289-301. DOI: 10.1016/S1473-3099(08)70097-5 Externer Link
163.
Blok HE, Troelstra A, Kamp-Hopmans TE, Gigengack-Baars AC, Vandenbroucke-Grauls CM, Weersink AJ, Verhoef J, Mascini EM. Role of healthcare workers in outbreaks of methicillin-resistant Staphylococcus aureus: a 10-year evaluation from a Dutch university hospital. Infect Control Hosp Epidemiol. 2003;24:679-85. DOI: 10.1086/502275 Externer Link
164.
Vonberg RP, Stamm-Balderjahn S, Hansen S, Zuschneid I, Ruden H, Behnke M, Gastmeier P. How often do asymptomatic healthcare workers cause methicillin-resistant Staphylococcus aureus outbreaks? A systematic evaluation. Infect Control Hosp Epidemiol. 2006;27:1123-7. DOI: 10.1086/507922 Externer Link
165.
Mertz D, Frei R, Jaussi B, Tietz A, Stebler C, Fluckiger U, Widmer AF. Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin Infect Dis. 2007;45:475-7. DOI: 10.1086/520016 Externer Link
166.
Ringberg H, Cathrine Petersson A, Walder M, Hugo Johansson PJ. The throat: an important site for MRSA colonization. Scand J Infect Dis. 2006;38:888-93. DOI: 10.1080/00365540600740546 Externer Link
167.
Harbarth S, Schrenzel J, Renzi G, Akakpo C, Ricou B. Is throat screening necessary to detect methicillin-resistant Staphylococcus aureus colonization in patients upon admission to an intensive care unit? J Clin Microbiol. 2007;45:1072-3. DOI: 10.1128/JCM.02121-06 Externer Link
168.
Faibis F, Laporte C, Fiacre A, Delisse C, Lina G, Demachy MC, Botterel F. An outbreak of methicillin-resistant Staphylococcus aureus surgical-site infections initiated by a healthcare worker with chronic sinusitis. Infect Control Hosp Epidemiol. 2005;26:213-5. DOI: 10.1086/502529 Externer Link
169.
Bertin ML, Vinski J, Schmitt S, Sabella C, Danziger-Isakov L, McHugh M, Procop GW, Hall G, Gordon SM, Goldfarb J. Outbreak of Methicillin-Resistant Staphylococcus aureus Colonization and Infection in a Neonatal Intensive Care Unit Epidemiologically Linked to a Healthcare Worker With Chronic Otitis. Infect Control Hosp Epidemiol. 2006;27:581-5. DOI: 10.1086/504933 Externer Link
170.
Berthelot P, Grattard F, Fascia P, Fichtner C, Moulin M, Lavocat MP, Teyssier G, Lucht F, Pozzetto B. Implication of a healthcare worker with chronic skin disease in the transmission of an epidemic strain of methicillin-resistant Staphylococcus aureus in a pediatric intensive care unit. Infect Control Hosp Epidemiol. 2003;24:299-300. DOI: 10.1086/502208 Externer Link
171.
Allen KD, Anson JJ, Parsons LA, Frost NG. Staff carriage of methicillin-resistant Staphylococcus aureus (EMRSA 15) and the home environment: a case report. J Hosp Infect. 1997;35:307-11. DOI: 10.1016/S0195-6701(97)90225-5 Externer Link
172.
Wagenvoort JH, De Brauwer EI, Sijstermans ML, Toenbreker HM. Risk of re-introduction of methicillin-resistant Staphylococcus aureus into the hospital by intrafamilial spread from and to healthcare workers. J Hosp Infect. 2005;59:67-8. DOI: 10.1016/j.jhin.2004.07.025 Externer Link
173.
Kniehl E, Becker A, Forster DH. Bed, bath and beyond: pitfalls in prompt eradication of methicillin-resistant Staphylococcus aureus carrier status in healthcare workers. J Hosp Infect. 2005;59:180-7. DOI: 10.1016/j.jhin.2004.06.016 Externer Link
174.
Haley RW, Bregman DA. The role of understaffing and overcrowding in recurrent outbreaks of staphylococcal infection in a neonatal special-care unit. J Infect Dis. 1982;145:875-85.
175.
Scott E, Duty S, Callahan M. A pilot study to isolate Staphylococcus aureus and methicillin-resistant S aureus from environmental surfaces in the home. Am J Infect Control. 2008;36:458-60. DOI: 10.1016/j.ajic.2007.10.012 Externer Link
176.
Masterton RG, Coia JE, Notman AW, Kempton-Smith L, Cookson BD. Refractory methicillin-resistant Staphylococcus aureus carriage associated with contamination of the home environment. J Hosp Infect. 1995;29:318-9. DOI: 10.1016/0195-6701(95)90284-8 Externer Link