Introduction
A healthcare-associated infection (HCAI) is defined as any infection acquired as a consequence of a person's treatment by a healthcare provider, or which is acquired by a healthcare worker in the course of their duties.1 The Health and Social Care Act 2008 makes it clear that prevention and control of HCAI should be part of everyday practice and applied consistently by everyone.1 In 2006, about 8% of inpatients in acute hospitals in England were identified as having a HCAI.2
HCAIs obviously waste NHS resources. A patient with a methicillin-resistant Staphylococcus aureus (MRSA) bacteraemia spends an average additional 10 days in hospital and for Clostridium difficile the additional length of stay is 21 days. Infections can cost a trust an extra £4,000–£10,000 per patient.3 Although it is not possible to prevent all infections,1 the emphasis placed on MRSA bacteraemias and C. difficile has shown it is possible to reduce numbers of these specific infections.
A national target was introduced by the Department of Health (DH) in November 2004 to reduce MRSA bloodstream infection by 50% by 2008, against the baseline figure for 2003–4. Aggregate numbers for 2007–8 showed a 42% decrease, and a 61% decrease for 2008–9.4 Following the mandatory surveillance scheme introduced in January 2004, a national target was introduced in October 2007 to reduce numbers of C. difficile infection by 30% across all age groups by 2010–11, against the 2007–8 baseline. By December 2008, the numbers reported showed a 41% reduction.4
Although these two infections have been the main focus of the DH's national approach to reducing HCAI, they represent only 15% of all such infection.5 Bloodstream infections represent 7% of infections of which 19% are Staphylococcus aureus (4% are MRSA).5
The overall prevalence of HCAI in England has remained relatively constant over the past two decades, although a modest decrease in prevalence from 9% to 8.2% has been shown between the national prevalence surveys carried out in 1993–4 and 2006.5 However during this period hospital infection prevention and control teams have had to meet the challenges posed by additional new or increasingly common pathogens such as vancomycin-resistant Enterococci (VRE), extended spectrum beta lactamase (ESBL) producing coliforms, virulent C. difficile 027 strains and the newly recognised multiantibiotic resistant carbapenemase producing (NDM-1) coliforms, with increasing numbers of elderly and immunocompromised patients being treated within hospitals.
Hospital medical staff in recent years have been expected to completely change the way they dress and hence how they may be perceived by patients. Compare the consultants of the 1970s, 1980s and 1990s wearing smart suits or long white coats over double cuff shirts and ties with the average hospital doctor in a short sleeved open necked shirt with no white coat. The impetus for the change was the publication of the bare-below-the-elbows (BBE) dress code.6,7 This requirement has been challenged on many fronts including not having a wristwatch8–10 and the lack of evidence that it is necessary to achieve adequate hand hygiene11,12 and the effect it has on patient perception.13 Other measures introduced for infection control reasons have also been challenged, such as not sitting on patients' beds14 and doing away with white coats.15–17
The challenges are understandable given the uncertainty about which measures introduced for infection prevention and control purposes are actually crucial and which ones have little or no effect.18 There is a concern that putting excessive time and resource into promoting hand decontamination will mean that other equally important initiatives are not fully implemented including prudent antimicrobial prescribing, ensuring optimal wound, urinary catheter and intravascular catheter care together with increased nurse:patient ratios, reduced bed occupancy and optimal cleaning. Decontaminating hands needs to be viewed as just one component of a hospital's infection prevention and control programme19 which is seen as part of the responsibility of all healthcare workers.1
The BBE campaign is just one part of the important hand decontamination initiative but there is a danger that the importance of the message about hand hygiene will be lost in the debate about specific components of the programme. There is, however, an argument that healthcare workers who roll up their sleeves, remove wrist watches and ties are taking their role in infection prevention and control seriously and offers a visible sign that the hospital is a different environment to other workplaces.
So which infection prevention and control interventions matter?
The white coat
The DH published guidelines in 200720 (updated in 201021) for healthcare workers regarding work wear, suggesting that good practice meant that white coats should not be worn during patient activity.21
The possibility of a doctor's white coat being contaminated with microorganisms has been the subject of debate and research for decades. Cuffs and pockets of coats were found to be the most highly contaminated area, with Staphylococcus aureus isolated from a quarter of the coats examined22 and, more recently, sampling of lapels, pockets and cuffs found 23% contaminated with S. aureus, of which six (18%) were MRSA.23
Nurses' uniforms become similarly contaminated during routine shifts on wards with heavy levels of contamination (more than 400 colonies per site sampled) throughout a shift24 with S. aureus, C. difficile and VRE all being detected.25 Fungi, including Aspergillus spores and Candida have also been found on healthcare workers' overalls including those in an infectious diseases department.26
Experiments have demonstrated that MRSA and VRE can survive on various fabrics including smooth cotton (clothes) or cotton terry (towels) for days, with some organisms such as enterococci surviving for over 90 days. Smaller inocula (100 organisms) survived for shorter times but still generally for days.27
A study of the viability of pathogenic bacteria on the fabric of a white coat showed that immediately after inoculation for S. aureus only 0.16% of the inoculum of 3.7 × 105 colony forming units survived. The number of viable cells decreased further to 0.046% after one hour and 0.014% after 24 hours. There was a similar decrease in viable cells for Serratia marcescens (a gram negative bacillary coliform) and Pseudomonas aeruginosa with no recovery possible after eight hours and three hours respectively.28
Experiments carried out in the 1950s demonstrated that two to eight million S. aureus organisms were required to cause a pus-forming intradermal infection by injection of humans. However, the dramatic effect of sutures reducing the required inoculums, in some cases 100 S. aureus, to produce a stitch abscess.29,30
There are circumstances, therefore, where even the low surviving inoculum of pathogens on white coats could cause an infection of a vulnerable wound if a foreign body, such as sutures or an intravenous catheter, was present. It is true, however, that the hypothesis that uniforms/clothing could be a vehicle for the transmission of infections is not supported by existing evidence from a search of the small number of relevant studies published.31
A recent study16 demonstrated that bacteria, including MRSA contamination, occurred at similar levels on newly laundered short sleeved uniforms and physicians' white coats, with no difference found in contamination of the skin at the wrists of physicians wearing either garment. Bacterial contamination was found to occur within hours of putting on uniforms, so by three hours, nearly 50% of the organism total count after eight hours was already present.
The ‘bare-below-the-elbows’ policy
Pathogens are readily transmitted on healthcare workers hands and hand hygiene is recognised as the best way of preventing transmission of microorganisms between patients.32 The BBE policy is relevant if it can be demonstrated that having long sleeves or wearing a wrist watch could result in less effective hand decontamination. Alcohol gel is recommended for hand decontamination in most clinical situations,33 but its efficacy is affected by hand-washing technique.34,35
Studies have demonstrated that a group of non-BBE doctors and medical students missed significantly more of the wrist compared with a BBE group.36 However, both groups missed significantly more areas on the wrists than on the hands, emphasising the importance of technique. This study showed that being BBE does improve wrist washing; however as is so often the case in infection control, there is no evidence to date that effective wrist washing actually reduces HCAI.
Other studies, while demonstrating that hand washing did produce a significant reduction in the number of bacterial colonies on staff hands, being non-BBE did not impede this reduction when BBE and non-BBE groups were compared.11
Specifically regarding wrist watches, it has been demonstrated that wearing a wrist watch results in increased bacterial contamination of the wrist, but excess hand contamination was not found unless the watch is manipulated.37
Balanced against this is the fact that there is a clinical value to a wrist watch as estimating heart and respiratory rate without being able to see a second hand is very inaccurate.38
It is worth observing that infection control manuals throughout the country recommend removing wrist watches before performing sterile procedures or surgical operations: should the same standard not apply to day-to-day direct patient contact?
Do not sit on the bed
The general prohibition on staff sitting on beds in acute hospitals in the UK has been questioned.14 There is a case to be made that sitting down with the same eye level as a patient enhances the interaction. However, the overall infection control evidence suggests that there are real concerns about it being accepted as common practice.
Bed components, including bed frames and mattresses, become contaminated by microorganisms through direct contact with skin scales, and body fluids including urine and faeces, and thus become a source of infection.39 Studies conducted in isolation rooms have found MRSA isolated from mattresses, bed frames and air with the isolates found being identical to the patients' strains suggesting contact and aerial spread.40,41 Although MRSA can be found on numerous sites in hospital rooms occupied by patients colonised or infected with the organism, sites such as linen, curtains, beds, lockers and over-bed tables have been found to harbour MRSA more frequently than others with contamination of near-patient hand-touch sites providing the largest risk.42–46
Transmission of MRSA from environmental surfaces to gloves or hands of healthcare workers has been documented. Forty-two per cent of 12 nurses contaminated their gloves by touching objects in rooms of patients with MRSA in a wound or urine, even if they had no direct patient contact.45 Thirty-one per cent of volunteers who touched bed rails and over-bed tables in patient rooms contaminated their hands with S. aureus (35% of which were MRSA).47
VRE are capable of surviving on various surfaces for prolonged periods and for at least 11 days on most fabrics.27 Environmental contamination occurs with VRE–46% of environmental cultures from rooms of VRE-positive patients who had diarrhoea were contaminated, while 15% of surfaces were found positive even if the patients did not have diarrhoea.48 In hospital settings, the sites most often contaminated with VRE include bed rails and bedside tables.49 Transmission of VRE from contaminated surfaces to healthcare workers' hands or gloves has been documented,47,50,51 with organisms also proven to be transmitted from positive sites to negative sites in the environment on healthcare workers' hands.52
C. difficile as a spore-forming anaerobe has been recovered in large numbers from the environment near symptomatic patients.53 Environmental contamination with spores is a definite risk factor for patients acquiring C. difficile infection.54
A person with C. difficile infection can excrete between 1 × 104 and 1 × 107 of C. difficile per gram of faeces.55 In elderly hospitalised patients, excretion of C. difficile may occur for over 10 days even if treated with oral metronidazole or vancomycin,56 so the potential for environmental contamination continues even though the diarrhoea may have settled, albeit at a probable lower rate.
Pyjamas and sheets become contaminated by a variety of organisms even after a single overnight use with Enterococci, S. aureus and a variety of Gram-negative bacilli including Pseudomonas being detected.69
The norovirus viral load in stool ranges from 2.2 × 104 to 7.7 × 1010 viruses per gram57 and in vomit can range up to 106 per ml.58 The small infecting inoculum makes norovirus one of the most infectious agents described with an estimated median infectious dose of just 18 viruses.59
It has been established that long-term shedding of norovirus can occur for more than one month in children60 and for a median of three months in immunocompromised hosts.61 Of importance also is evidence that up to 32% of immunocompetent hosts challenged with norovirus develop asymptomatic infection.62 Norovirus is also environmentally stable and resistant to many cleaning agents.63
The period of infectivity of excreted virus has not been clarified, but basic infection control precautions should be taken possibly for up to four weeks for known infected patients who remain in hospital, even after symptomatic recovery. Within a hospital where norovirus cases have occurred there may be asymptomatic excretors who have acquired the organism and may also have contaminated the environment, including their bed. Considering the large viral load excreted and the very small infectious dose, not sitting on any hospital bed as a standard infection control precaution seems justified.
The role of the hospital environment
As discussed, it is known that the hospital bed and bed linen is frequently contaminated with potential pathogens. The same is true of other hospital surfaces which is one of the reasons for including hand decontamination after touching potentially contaminated surfaces in the World Health Organization (WHO) ‘five moments of hand hygiene’ initiative.64 Frequently touched surfaces of general public areas, such as the handrail of an escalator, inside buttons of escalators and registration counters, were found contaminated with potentially pathogenic bacteria in over 85% of samples taken.65 Organisms found included MRSA. MRSA has also been found on hospital curtains66 and hospital bed handsets.67,68
Environmental contamination has been recognised as making an important contribution to hospital infection,70 including MRSA, VRE, C. difficile, Acinetobacter species and norovirus,71 with effective environmental cleaning being vital to the control of HCAIs.72,73
It would, therefore, be appropriate to consider all surfaces in the ward environment as being potentially contaminated, but especially the frequently touched ones. The appropriate control measure is adequate regular cleaning. The WHO ‘five moments of hand hygiene’ initiative is sensible in principle but an element of practicality has to be applied to the concept of decontaminating hands after contact with every contaminated surface. If taken literally this would be after every contact with a patient's notes, notes trolley, patient chart, keyboard, telephone, door knob etc. Following recommended hand hygiene procedure for each contact would be extremely time consuming. As has been observed, having an aggressive zero tolerance approach to when healthcare workers are observed to fail observation audits when they have not decontaminated their hands after touching a patient's notes or ward surface, is not likely to be helpful in achieving the highest level of hand hygiene when it is most appropriate.18
Can any conclusions be made?
Infection control precautions do make a difference as can be judged from the decrease in MRSA bacteraemia and C. difficile infections seen recently. The explanation is likely to be multi-factorial and understanding which interventions are the most important is difficult. There is evidence that lower MRSA infection rates are linked to hand hygiene and isolation and a lower rate of C. difficile infection being linked to cleanliness, good antimicrobial prescribing practices and surveillance of infection.74
The DH's Saving lives initiative with an emphasis on high impact interventions and care bundles, which includes peripheral intravenous cannula, central venous catheter, urinary catheter, surgical site infection and C. difficile, helps concentrate resource on medical interventions known to be associated with nosocomial infection.75
Near-patient hand-touch sites frequently become contaminated with pathogens so the answer is to ensure that they are cleaned sufficiently often and carefully enough to reduce the risk of such sites acting as a reservoir of infection to a minimum.
Beds and bed linen do become contaminated with pathogens and not necessarily only from patients with symptomatic infections due to identified pathogens. Avoiding potentially widespread contamination of a healthcare worker's clothes by not sitting directly on the bed is an appropriate response and does not necessarily make medical care less compassionate: there is always the option of sitting on a chair to be at the same eye level as the patient. Being BBE does provide a visible sign of infection control and is an unambiguous policy. Allowing long sleeves or wrist watches brings with it the uncertainty of what is then acceptable: would double cuffs with large cuff links or wrist watches with wide fabric/velcro bands be appropriate? There is evidence that being BBE allows more efficient wrist washing and that increased bacterial counts are found under watches–what is lacking is the evidence that this may directly lead to infection, although there are clinical scenarios involving vulnerable wounds in immunocompromised patients where a very small inoculum of pathogenic bacteria could cause infection. If wrist watches are removed and sleeves rolled up before performing a ‘sterile procedure’, why not maintain the same standards for all patient contact since it is easily achievable. A fob watch is the answer to the lack of a wrist watch.
All uniforms, be they long sleeved white coats or short sleeved uniforms may become contaminated with potential pathogens during normal patient care. White coats would not be an issue if they were available as clean laundered items every day, although it can be argued as previously suggested, they should have short sleeves. Patients when questioned may prefer to see doctors in formal attire as being professional and the easiest way of identifying a person as a doctor, if given a choice between a doctor in formal attire, scrubs or BBE.76 However, if the reasons for the BBE policy are explained or why surgical scrubs are worn, the preference often disappears.77 Patients appreciate being able to readily differentiate staff groups but it can be argued that there are ways of ensuring doctors are easily identifiable without the need for them to wear long white coats or suits.
The goal of most professionals working in infection prevention and control is to get all healthcare workers to accept responsibility about infection prevention and understand what measures are known to be critical, such as appropriate hand decontamination before and after direct patient contact, the high impact interventions care bundle, appropriate patient isolation, appropriate antimicrobial stewardship and appropriate environmental cleaning.
When there is 100% compliance with all of these measures then it would be worth re-evaluating the evidence for not wearing white coats or being BBE but, until then, sufficient evidence exists to show that the BBE policy may prevent some infections, as does the policy of not sitting on beds or wearing long sleeved white coats.
- © 2011 Royal College of Physicians
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