Review
Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning

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Summary

In the UK, we continue to debate the importance of hospital cleaning in relation to increasing numbers of patients acquiring meticillin-resistant Staphylococcus aureus (MRSA). However, there is little direct evidence for the effectiveness of cleaning because it has never been afforded scientific status. Hospital hygiene is usually assessed visually, but this does not necessarily correlate with microbiological risk. A more robust case for hospital cleaning can be presented by considering the evidence for all the stages of the staphylococcal transmission cycle between human beings and their environment. Cleaning has already been accepted as an important factor in the control of other hardy environmental pathogens, such as Clostridium difficile, vancomycin-resistant enterococci, norovirus, and Acinetobacter spp. This Review will show why the removal of dirt might have more impact on the control of MRSA than previously thought. Introduction of additional cleaning services is easier than improvements in hand-hygiene compliance.

Introduction

There is much concern over the state of hygiene in hospitals.1, 2, 3 The UK general public seem to associate visibly dirty wards with increasing rates of meticillin-resistant Staphylococcus aureus (MRSA) acquisition,4 but historically there has been little evidence that the environment is important in endemic hospital-acquired infection.5, 6, 7, 8, 9 This premise has been challenged since the increase in MRSA in hospitals in the past decade.1, 10 Because a clean environment is usually taken for granted, it is not surprising that there is little evidence to show that cleanliness could be an important control factor in the spread of MRSA.11 Furthermore, the measurement of how clean a hospital is other than by visual assessment, which is both subjective and inaccurate, is difficult because such an assessment does not necessarily correlate with microbiological risk.12, 13, 14

Various audits and standards have been published for the express purpose of improving the appearance of the hospital environment and thus helping to alleviate public concern.15, 16 There have also been cleaning manuals, model cleaning contracts, infection-control guidance, and monitoring strategies.17, 18, 19, 20 These government-sponsored documents may address the aesthetic demands from patients and their relatives about the superficial appearance of hospitals, but they are based on visual assessment and fail to recognise that microorganisms, including human pathogens, are invisible to the naked eye.

The issue of hospital-acquired infections is compounded by the current politically generated drive to reduce waiting lists. Hospitals are crowded with sick people in close proximity to one another, even though years of work in infection control have shown us that patients pass their microorganisms to those nearby. This was first recognised by Florence Nightingale in the 19th century, at least 10 years before the advent of bacteriology.21 She concluded that the use of small separate rooms could have prevented the high rate of mortality in maternity cases after an outbreak of erysipelas at a midwife training school.22 However, lack of isolation facilities and continued pressure on the availability of beds provide a serious challenge to standard principles of infection control. A recent study has confirmed an association between MRSA bacteraemia rates, bed occupancies, and even bed turnover times.23 Despite this finding, a UK House of Lords debate on MRSA included a response that stated that there is no conflict between good cross-infection control and good bed management.24 Therefore, not only do governmental faculties not understand the link between visible dirt and the presence of pathogenic microorganisms, but they also do not support the premise that crowded hospitals facilitate the spread of infection.23, 24 This attitude reminds us of the situation 150 years ago in the hospital at Scutari, and then on return to the UK, when Florence Nightingale tried to convince the authorities of the need for basic hygiene and ventilation in health-care institutions, poorhouses, and army barracks.22

Only a few studies provide evidence that cleaning reduces the risk of acquiring MRSA in health-care institutions.10, 25, 26, 27 There is another way, however, of justifying cleaning as a useful control strategy for MRSA. We already have evidence to support each of the individual components of the staphylococcal transmission cycle between patients, staff, and the inanimate environment.28, 29, 30 Much of the work on coagulase-positive staphylococcus, originally done 50 years ago, is as relevant for MRSA as it is for its susceptible predecessor. The epidemiological properties of S aureus, whether meticillin resistant or not, remain the same. One difference between the hospital staphylococcus of the 1960s and current MRSA strains is that isoxazolyl penicillins (eg, flucloxacillin) quickly cured patients with S aureus infections before it had a chance to spread to other patients or into the environment. Additionally, the hospitals received more cleaning at that time, since they had not been exposed to today's emphasis on cost cutting. Now, of course, we do not have a quick cure for MRSA—currently available drugs are either toxic or expensive, or relatively inefficient, and most have to be given parenterally.31 Resistance has already been shown for newly released agents.32, 33 This condemns colonised or mildly infected patients to conservative management only, thus enhancing their risk for future sepsis as well as providing the organism with an opportunity for dispersal throughout the environment and to others.

Even if the epidemiology of the staphylococcus has not changed over the years, there are, however, differences in the type of patients that we see nowadays and the clinical environments in which they are nursed. Patients are older, immunologically weaker, and are subjected to far more invasive procedures and devices than the patients of 50 years ago. Furthermore, there has been a huge influx of electronic equipment into the near-patient vicinity, providing more hand-touch sites that require a greater degree of sophisticated cleaning attention. Certain liquid cleaning agents would damage many items of medical and nursing equipment. All of these differences could have contributed towards an increase in MRSA acquisition in modern hospitals.

This Review will present the evidence that supports the epidemiological and transmission characteristics of coagulase-positive staphylococci. Each component of the transmission cycle can be considered independently in order to assess the potential impact of cleaning.

Section snippets

The transmission cycle

The staphylococcal transmission cycle can be broken down into several stages, each of which is supported by studies. Additionally, there is direct evidence for the benefits of cleaning, both for control of staphylococci and for other hardy hospital pathogens in the clinical environment (panel 1). The propagation of this generally human commensal bacterium is perpetuated by a dynamic staphylococcal transmission cycle between human beings and their environment (figure 1). The coagulase-positive

Survival of staphylococci in the hospital environment

Although MRSA seems to contaminate the air and general environment throughout the hospital, this would not matter if the organism were unable to survive outside the human host. However, all members of the staphylococcal family (coagulase negative and positive) show an avid ability to survive in the environment, over a wide range of temperatures, humidity, and exposure to sunlight.60, 61 Staphylococci's resistance to desiccation is also long established.62 Persistence has been shown by DNA

People transmit staphylococci to other people

There are reports detailing staphylococcal transmission between people in hospitals and people at home. These cases may relate to outbreak situations involving health-care workers or patients newly transferred from elsewhere.92, 93 Other reports document transmission from health-care workers to family members,94, 95, 96 spread between patients in the community,97 and transmission between ambulant patients.98 Such evidence for person-to-person transmission of MRSA effectively negates the

Staphylococci spread between people and the environment

People who are not habitual staphylococcal carriers are able to acquire S aureus from hand-touch sites or from the air, and transmit it to others or to other environmental sites.30 They may carry certain strains for various lengths of time at various sites but do not seem to do so long term. Staphylococcal carriage has been associated with contamination of the home environment and refractory carriage has been linked with the continued presence of MRSA at home.100, 101 In hospital, one study

Numbers of staphylococci required to initiate infection

What size of staphylococcal inoculum is required to initiate an infection? The answer to this question is only relevant if contamination on clinical surfaces is thought to represent a risk for transmission. If fingertips pick up only a few CFUs of MRSA from the environment to deliver to a patient, are these enough to cause infection?

Experimental induction causes infection within 24–48 h in human skin samples, but the inoculum required is four to eight million staphylococci.103 Experimental

Various cleaning methods reduce MRSA in the environment

Several studies detailing the effects of various methods to reduce environmental MRSA have recently been published, including a study examining the effect of portable high-efficiency particulate air filtration on airborne MRSA in isolation rooms.111 The cleaning methods included routine vacuuming and detergent-based cleaning, deep cleaning with disinfectants, and gaseous decontamination using hydrogen peroxide vapour.27, 64, 70 All of these methods seemed to reduce MRSA in the hospital

Discussion

Cleaning has two main functions. The first is non-microbiological—to improve or restore appearance, maintain function, and prevent deterioration. The second is microbiological—to reduce the numbers of microbes present and any substances that support their growth or interfere with subsequent disinfection or sterilisation.7 Reduction of the numbers of microbes on an object or in the general environment should not only reduce the risk of there being a pathogen present, but should reduce the risk

Search strategy and selection criteria

Data for this Review were identified by searches of Medline, PubMed, and references from relevant articles. Many articles were identified through searches of the author's own personal collection of papers relating to hospital cleaning. Search terms used were “hospital cleaning”, “met(h)icillin-resistant Staphylococcus aureus”, “MRSA”, “staphylococci”, “epidemiology”, “hospital”, “cloud adult”, “transmission”, “environment”, “healthcare”, and “contamination”. Only English language papers

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