Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study

Background Increasing hospital-acquired infections have generated much attention over the last decade. There is evidence that hygienic cleaning has a role in the control of hospital-acquired infections. This study aimed to evaluate the potential impact of one additional cleaner by using microbiological standards based on aerobic colony counts and the presence of Staphylococcus aureus including meticillin-resistant S. aureus. Methods We introduced an additional cleaner into two matched wards from Monday to Friday, with each ward receiving enhanced cleaning for six months in a cross-over design. Ten hand-touch sites on both wards were screened weekly using standardised methods and patients were monitored for meticillin-resistant S. aureus infection throughout the year-long study. Patient and environmental meticillin-resistant S. aureus isolates were characterised using molecular methods in order to investigate temporal and clonal relationships. Results Enhanced cleaning was associated with a 32.5% reduction in levels of microbial contamination at hand-touch sites when wards received enhanced cleaning (P < 0.0001: 95% CI 20.2%, 42.9%). Near-patient sites (lockers, overbed tables and beds) were more frequently contaminated with meticillin-resistant S. aureus/S. aureus than sites further from the patient (P = 0.065). Genotyping identified indistinguishable strains from both hand-touch sites and patients. There was a 26.6% reduction in new meticillin-resistant S. aureus infections on the wards receiving extra cleaning, despite higher meticillin-resistant S. aureus patient-days and bed occupancy rates during enhanced cleaning periods (P = 0.032: 95% CI 7.7%, 92.3%). Adjusting for meticillin-resistant S. aureus patient-days and based upon nine new meticillin-resistant S. aureus infections seen during routine cleaning, we expected 13 new infections during enhanced cleaning periods rather than the four that actually occurred. Clusters of new meticillin-resistant S. aureus infections were identified 2 to 4 weeks after the cleaner left both wards. Enhanced cleaning saved the hospital £30,000 to £70,000. Conclusion Introducing one extra cleaner produced a measurable effect on the clinical environment, with apparent benefit to patients regarding meticillin-resistant S. aureus infection. Molecular epidemiological methods supported the possibility that patients acquired meticillin-resistant S. aureus from environmental sources. These findings suggest that additional research is warranted to further clarify the environmental, clinical and economic impact of enhanced hygienic cleaning as a component in the control of hospital-acquired infection.


Background
Increasing hospital-acquired infections have generated much attention over the last decade. The public has linked these infections with their experience of dirty hospitals, but the precise role of cleaning in the control of infection remains unknown [1]. Finding evidence for benefit from routine cleaning is difficult because there are no measurable standards available. This means that healthcare environments are assessed by visual inspection only, which may fulfil aesthetic obligations but does not provide a scientific assessment of the infection risk for patients [2].
Meticillin-resistant Staphylococcus aureus (MRSA) is one of the main causes of hospital-acquired infection. Hospitals provide a long-term reservoir for MRSA, since it can survive for months in the environment [1,3]. It can be found on general surfaces such as floors and furniture, and on clinical equipment [2,[4][5][6]. Certain sites, such as curtains, beds, lockers and overbed tables, tend to harbour MRSA more frequently than others [7,8]. These sites are often situated right beside the patient [8,9]. For these reasons, MRSA was chosen as an indicator organism in proposed microbiological standards for surface-level hygiene in hospitals [2].
Patients generally acquire MRSA from hands, and it is possible that healthcare workers transmit MRSA via hands after touching contaminated environmental surfaces [5,10]. This transmission cycle could be broken by more conscientious hand-hygiene but it is notoriously difficult to get everyone to clean their hands at the appropriate time [11,12]. When staff are busy, infection control precautions go awry, including hand washing and cleaning of equipment [13]. It has already been suggested that the limitations of hand hygiene could be mitigated by concentrating resources on cleaning hand-touch sites [8,10].
The main aim of this prospective cross-over study was to introduce one additional cleaner into a surgical ward from Monday to Friday and measure the effect on the clinical environment. After 6 months the cleaner was switched to another matched surgical ward so that each ward acted as a control for the other. We also hoped to investigate the transmission pathways between patients and the environment using molecular epidemiological methods.

Study wards
Two surgical wards with endemic MRSA were matched for bed numbers, bed occupancy rates, floor area, staffing levels, case mix, antibiotic consumption, cleaning schedules and state and maintenance of internal fabric. Each ward contains 21 beds, with two side-rooms at the ward entrance and the remaining beds in groups of three to five in open cubicles on either side of the ward. Ward A is an acute male surgical ward situated on the first floor of a Victorian block, and Ward B, directly above, is for females, although each occasionally hosts patients of the opposite sex. Most patients were admitted for general surgical procedures, with occasional vascular and orthopaedic cases. Routine antibiotic prophylaxis for general surgical cases is amoxicillin, gentamicin and metronidazole, with cephalosporins used for patients allergic to penicillin. The wards share clinical staff and cleaning is performed by the same domestic team to a set specification [14]. Bed occupancy rates are routinely monitored by Greater Glasgow & Clyde NHS Trust. In 2005, each ward experienced 20 new cases of MRSA, most thought to be ward-acquired.

Ward screening
We screened 10 hand-touch sites on both wards every week for 1 year in order to ascertain overall aerobic colony counts, presence of MRSA and meticillin-susceptible Staphylococcus aureus (MSSA) [7,8]. Once-weekly screening took place on different days after the ward had received its routine daily clean. Sites chosen were hand-touch sites at bedside areas (patient lockers, overbed tables and bed frames), clinical equipment (patient hoist, infusion pump and blood pressure (BP) stand), sites at the nurses' work station (computer keyboard, desk and patient notes) and a side-room door handle. Patient curtains were not included because it was not possible to replace these outside of routine procedures. Hand-touch sites were sampled from one ward hoist, BP stand and computer keyboard but from different sites representing the remaining items throughout the ward, excluding those in the isolation rooms. Screening was continued for 7 weeks after completion of the study in order to monitor any residual effects.

Patient screening
Both wards adhered to identical infection control, screening and antimicrobial policies during the year. Any change in routine screening policy would have confounded the effect of cleaning as a single intervention, since it has already been shown to be an effective control mechanism in its own right [15]. Patients awaiting surgery were routinely screened pre-admission or on the ward if they had been transferred from another unit, hospital or nursing home, or had a history of recent hospital admission, prior MRSA or recent contact with MRSA. All patients with newly diagnosed infections were also screened for MRSA, along with other clinically relevant specimens, in order to detect ward-acquired MRSA infection. Such infections were diagnosed by senior surgical staff using national criteria for surgical site, catheter-associated and respiratory infections [16]. Those patients with no prior history of MRSA, who had been on the ward for >48 hours, had evidence of infection, and from whom the laboratory isolated MRSA were regarded as new cases of MRSA infection. These, along with known MRSA cases, were then screened every week until discharge from the ward.

Management of patients with MRSA
Patients with MRSA were placed in isolation and managed according to local infection control policies. They were screened at carrier sites, started on a 5-day topical clearance regimen (chlorhexidine washes, mupirocin nasal cream and Corsodyl™ throat spray), and treated with appropriate antibiotics. Patients situated nearby were also screened for MRSA after any new case was found on the ward. If there were no isolation rooms available, patients were cohorted or moved to another ward; this included the other study ward. MSSA acquisition and infection were not audited during the study.

Enhanced cleaning protocol
Enhanced cleaning began on Ward A in July 2006. The study domestic cleaned from 0730 h until 1530 h each weekday, with holiday and sickness cover provided by a colleague. Both cleaners were recruited from the existing domestic pool and trained to clean hand-touch sites. The study specification included all near-patient hand-touch sites two to three times per day, hand-touch sites at the nurses' station one to two times per day and clinical equipment one to two times per day regardless of nurses' cleaning responsibilities. The study cleaner also cleaned all door handles on the ward two to three times per day as well as items such as plastic wall-mounted racks for leaflets, visitors' chairs and hand-touch sites in the ward office and kitchen.
Day-to-day management responsibilities fell to senior nurses but the cleaners remained professionally accountable to the domestic supervisor. Routine ward cleaning continued as usual, including regular quality control audits on environmental cleaning [14]. Routine cleaning comprised 2 to 3 hours each morning, concentrating on floors and bathroom facilities. There was a 'spot-check' performed later on during the day, in case toilets, in particular, required further cleaning attention. Equipment and cleaning consumables were standard NHS issue, stored separately and maintained according to current protocol. Consumables were chiefly CINCH™ detergent (AGMA, Haltwhistle, UK) and water and Tuffie™ wipes (Health Care Services, Nottinghamshire, UK). Disinfectants are not routinely used on these wards. The extra cleaner only operated on one ward at a time for a period of 6 months before being moved to the other ward. Each ward therefore acted as a control for the other. There was no additional cleaning performed out-of-hours, including weekends.

MRSA patient-days
Total weekly MRSA patient-days were estimated by calculating all MRSA-positive patient-days each week for each ward [13]. This was done by prospective auditing of all microbiological specimens submitted from both wards and knowledge of patient admission and discharge dates throughout the study. In addition, every patient with MRSA infection and/or persistent colonisation was screened weekly until discharge. Given that we did not screen every new admission to the ward, we probably underestimated the number of MRSA patient-days during the study, but this would have been consistent for both wards and study periods given the cross-over design. All cases of MRSA infection were identified promptly, whether acquired on the ward or before admission to the ward. Patients with MRSA infection are known to shed the organism into the environment more readily than those who are merely colonised [5].

Microbiology
Clinical samples were processed in the clinical laboratory according to standard operating procedures. Dipslides (Biotrace ® , Bridgend, UK) were used for environmental screening; these were coated with Baird-Parker (for staphylococci) and nutrient agars (for aerobic colony counts) [7,8,14,17]. Colonial growth was subjected to both quantitative (cfu/cm 2 ) and qualitative assessment [2]. One dipslide was used to screen adjacent sites, with each side pressed against the site for 5 seconds at a pressure of approximately 25 g/cm 2 [18].
After sampling, dipslides were incubated at 30°C in air for 48 hours. Microbial growth on nutrient agar was quantified as <2.5 cfu/cm 2 , 2.5 to 12 cfu/cm 2 , 12 to 40 cfu/cm 2 , and 40 to 100 cfu/cm 2 , according to the manufacturer's recommendations. Black colonies on Baird Parker were identified to genus level by colonial morphology and Gram film. Gram-positive cocci were differentiated by catalase test and staphylococci designated S. aureus or coagulase-negative staphylococci (CNS) by Staph-plus (Pastorex ® , Stockport, UK). Coagulase-positive isolates were subcultured onto MRSA chromogenic agar (Oxoid, UK) and incubated overnight at 37°C in air. Antimicrobial susceptibility testing was performed using the Vitek ® system (bioMerieux, Basingstoke, UK) standardised in accordance with the Clinical and Laboratory Standards Institute guidelines.

Scottish MRSA reference laboratory methods
Clinical and environmental MRSA were sent to the Scottish MRSA Reference Laboratory, which confirmed identification by latex agglutination and DNase test. All isolates were subjected to PCR detection of S. aureus species-specific nuc gene, followed by PCR for the mecA gene [19,20]. Pulsed-field gel electrophoresis (PFGE) typing of SmaI-(Invitrogen, UK) digested DNA was performed by a modification of a previously described method [21]. Briefly, S. aureus colonies from overnight cultures were incorporated into agarose plugs. After bacterial lysis, genomic DNA was digested using SmaI. PFGE was performed by clamped homogeneous electric field (CHEF) electrophoresis with a CHEF-mapper system (Bio-Rad Laboratories, California, USA). The fragments were separated with a linear ramped pulse time of 6.8 to 63.8 seconds over a period of 23 hours at 14°C. Gels were analysed using DNA analysis software GelCompar II version 5.1 (Applied Maths, Belgium) using the Dice correlation co-efficient. A dendrogram was generated using UPGMA with a tolerance of 1.5%.

Hygiene status analysis
The standard set for finding a potential pathogen is <1 cfu/cm 2 [2]. For this study, we chose both MRSA and MSSA as indicator organisms [22]. A second standard states that total aerobic colony counts (ACCs) from a hand-touch site should not exceed 2.5 to 5 cfu/cm 2 [2,23]. Exceeding these levels suggests insufficient cleaning, masks the presence of a pathogen or implies an increased chance of finding a pathogen with similar epidemiological properties, for example, CNS and S. aureus [2]. We therefore defined a hygiene failure as a site with ACC greater than 2.5 cfu/cm 2 .

Epidemiological and cost analyses
Environmental screening data and cases of hospitalacquired MRSA infection were modelled against routine and extra cleaning periods, MRSA patient-days and bed occupancy rates. Any potential transmission between patients and environment were investigated using molecular typing results, dates of isolation and location. Typing also allowed us to ascertain longevity of unique strains in the environment.
Since the project began in July, this allowed each ward to receive 6 months of enhanced cleaning to encompass both winter and summer months. The project was presented to domestic, nursing and medical staff and to the Trust Infection Control Committee for approval and comments before it was launched. It was approved by the R & D department and Ethics committee at the study hospital.
We calculated the overall costs of new MRSA infections potentially saved by the efforts from an extra cleaner. The study cleaner earned £12,320 pa and one new case of MRSA infection was assumed to cost £9,000 [24,25]. Cost of cleaning consumables was included in the calculation.

Statistical methods
From previous data we expected a background rate of two to four hygiene failures per week [7]. The study was powered to detect a 50% reduction in hygiene failures over a 6-month period, with powers of 97% assuming a background rate of four per week in the normally cleaned ward, 93% with a background rate of three, and 81% with a background rate of two. We expected to find about 20 new MRSA cases on the control ward over the year, assumed to have been acquired on the ward. This only has a power of about 44% to detect a 50% reduction in the numbers of MRSA cases.
The main test of the hypothesis that extra cleaning has an effect on ACC is based upon a linear regression of the log total ACC with terms of cleaning, ward, period and quarter used to investigate the effect of enhanced cleaning on total ACC. A log transformation was required to satisfy the normality assumption in the linear regression and residual plots were used to verify that this assumption was appropriate. This analysis is more powerful than an analysis of hygiene failures, since ACC is a quantitative measurement and hygiene failure is a categorisation of that. The study was powered in terms of hygiene failures, and the powers for ACC analysis will be higher as it is a quantitative measurement rather than a categorical variable. Binomial logistic regression models with factors for ward, cleaning and site were used to estimate the effect of enhanced cleaning on environmental levels of MRSA/ MSSA and hygiene failures. Poisson log-linear regression models were used to estimate the effect of enhanced cleaning on new MRSA infections in a ward adjusting for MRSA patient-days and ward, and interaction tests were used to assess the differences in effect over the two wards. Significance levels of 5% were used for the pre-specified hypotheses and 95% confidence intervals for the estimated effects, which, for the overall effect of enhanced relative to routine cleaning, were adjusted for ward differences. Figure 1 shows the total quantity of microbial growth recovered from both wards over the year and for 2 months after the study finished. New patient MRSA infections are also indicated. ACCs were 32.5% less with enhanced cleaning compared with normal cleaning (P < 0.0001; 95% CI 20.2%, 42.9%) ( Table 1). Ward B had an overall 19.0% lower ACC than Ward A (P = 0.015; 95% CI 4.3%, 31.4%). There was no residual evidence of any temporal effects of period (P = 0.58) or quarter (P = 0.18). In Ward B, the extra cleaning was associated with a 45.4% reduction in ACC (P < 0.0001; 95% CI 33.8%, 55.1%), whereas it was only associated with a 16.5% reduction in ACC for Ward A (P = 0.21; 95% CI 36.7% reduction,-10.1% increase).

Hygiene failures
The rate of hygiene failures with routine cleaning averaged 3.2 per week, as anticipated. Over both periods the enhanced cleaning was associated with a 50.3% reduction in the odds of a hygiene failure (95% CI 33.8%, 62.7% reduction), though there was evidence of a different effect between the two wards, P < 0.0001, and the two periods (P = 0.0002). In period 1 there were 86 hygiene failures in Ward B (normal cleaning) and 73 in Ward A (extra cleaning), corresponding to a 21.0% reduction (95% CI 45.6% reduction, 14.8% increase) in the odds of having a hygiene failure at a site with enhanced cleaning. In period 2 there were 82 hygiene failures in Ward A (normal cleaning) and 27 in Ward B (extra cleaning), corresponding to a 74.7% reduction (95% CI 84.3%, 59.3%) in the odds of having a hygiene failure with enhanced cleaning. In Ward A, where the extra cleaner was used in the first period, the odds of hygiene failure was 15.3% lower (95% CI 41.8% reduction, 23.5% increase) when the extra cleaner was used. In Ward B, the odds of hygiene failure was 76.5% lower (95% CI 85.4%, 62.1%) when the extra cleaner was used.

Effect on environmental MSSA and MRSA
MRSA was recovered from 12 sites when the wards received extra cleaning compared with 16 sites when the wards were being routinely cleaned (P = 0.45) ( Table 1). This was in contrast to the number of MSSA isolates recovered during routine and enhanced cleaning periods, since MSSA was recovered from 37 sites on wards receiving enhanced cleaning and from 30 sites on wards during routine cleaning periods (P = 0.37).

Site contamination of MRSA and MSSA
There was some evidence for different amounts of MRSA/ MSSA across the sites (P = 0.065) (data not shown). Sites more frequently contaminated with MSSA/MRSA were the bedside locker (17 isolates), overbed table (13 isolates) and bed frame (12 isolates). These are the three sites closest to the patient. There was less contamination on the infusion pump, BP stand and computer keyboard. Whether or not the ward had enhanced cleaning did not affect the site contamination rankings (P = 0.52), nor did the ward on which sites were located (P = 0.15). The leastcontaminated site throughout the study was a touch pad on the infusion pump.

Bed occupancy rates, MRSA patient-days and number of positive MRSA screens
There was little difference in bed occupancy rates between the two wards throughout the study, although both had higher rates during their respective extra cleaning periods (  period (routine clean) and nine during the second period (enhanced clean). These numbers include the patients who acquired their MRSA on the wards. There were no changes in antibiotic policies during the study, nor differences in antibiotic consumption, save for a small increase in use of linezolid on Ward A for complicated MRSA infections. There were no additional handhygiene interventions other than routine educational visits from the infection control team including poster reminders. We did not formally audit hand-hygiene compliance.

Costs
A simple cost analysis was performed. The study cleaner earned £12,320 per annum and consumables were £1,100; this was offset against the number of patients potentially spared MRSA infection. The average cost of one hospital-acquired surgical site infection (SSI) caused by MRSA is estimated as £9,000 [24,25]. If it is correct to assume that five to nine patients were potentially spared MRSA SSI, the hospital saved in the region of £45,000 to £81,000 minus the costs of the cleaner and consumables for one year. This gave overall cost savings of £31,600 to £67,600. Tables 2 and 3 show the PFGE profiles of patient and environmental MRSA strains and their isolation dates. Not all isolates were typed, since some did not survive storage. On Ward A, there were six different PFGE profiles from both patients and the environment ( There were thus indistinguishable strains from patients, which were later found in the environment, and vice versa ( Figure 2). Indistinguishable strains were recovered from different sites around the ward, sometimes weeks apart [3,[5][6][7]. Not surprisingly, some strains appeared to move between wards. Staff were not screened during this study, however, which means that a carrier role by staff cannot be excluded in any transmission hypotheses [6,7].

Discussion
This study has demonstrated the effect of one extra cleaner in a prospective cross-over study on two surgical wards. Despite the fact that the cleaning intervention was only delivered on weekdays, it still had a significant impact on the overall levels of microbial contamination from handtouch sites. The effect was greater on Ward B than for Ward A, one reason for this being the fact that environmental screening was more likely to be performed on a Monday in Ward A during the first few months of the trial. It is possible that the study cleaner did not have time to remove all the accumulated dirt from the weekend. Whilst this creates bias for the results overall, it does provide an indication of the sensitivity of the monitoring method used.
Ward A had the extra cleaner during the first 6 months of the study and the small impact from enhanced cleaning Dendrogram illustrating genetic diversity among MRSA strains recovered from patients and the environment from Wards A, B and additional ward during the study Figure 2 Dendrogram illustrating genetic diversity among MRSA strains recovered from patients and the environment from Wards A, B and additional ward during the study. Seven clusters are highlighted: P = patient; E = environment; individual strains are also highlighted in Tables 2 and 3.   100  95  90  85  80  75  70  65  60 Tables 2 & 3 could be evidence of a carry-over effect or an effect of practice. It is likely to be the latter, as there is little evidence of an effect from the extra cleaning in the first 6 months -a reduction of 16.7% (P = 0.19; 95% CI 36.2, -8.9%), while there is a large reduction of 45.3% during the second 6 months (P < 0.0001; 95% CI 32.8%, 55.5%).
A notable increase is seen in the overall colony counts on Ward A following withdrawal of the cleaner after 6 months ( Figure 1). This rebound effect was also seen on Ward B, on completion of the study. It is possible that the withdrawal of enhanced cleaning increased the risk for patient infection, since there were four new MRSA infections on Ward A 4 weeks after the cleaner left (February 2007) and two new infections on Ward B 2 weeks after the study finished (July 2007). Two of the strains from the first cluster on Ward A and both from Ward B in July were genotypically indistinguishable, so these could have been due to patient-to-patient spread without any help from a contaminated environment (Figure 2). The three strains from Ward A in February were different from each other and from MRSA strains from other patients on the ward. These could have occurred as individual episodes of acquisition from hands after touching contaminated environmental sites. The two new cases on Ward B were not included in the overall results of the study, since they occurred after the study had finished. Even if patient-topatient transmission did occur, the first patient had to acquire MRSA from somewhere before spreading it to another. For each of the two-patient clusters with indistinguishable strains, an apparently similar strain was identified from an environmental source previously (Figure 2).  Table 3 and Figure 2), and two occurred after the study had finished (Patients 8B and 9B; Table 3 and Figure 2). All the other MRSA strains from cases with new infections were different, although we identified known patients with similar strains who had been resident on the ward previously. These patients had been discharged well before new cases had emerged with similar strains, because these wards were acute surgical wards and did not host long-stay patients. High bed occupancy rates may also be associated with increased risk of MRSA acquisition, but there was little difference in occupancy rates between the wards, whether they were receiving extra cleaning or not (Table 1) [26][27][28]. Both wards were actually busier during their enhanced cleaning periods. In addition, higher bed occupancy rates are associated with an increased chance of finding higher ACC, including MRSA/MSSA, from handtouch sites in the clinical environment [7,8]. This might go some way to explain the small effect from the extra cleaning on the amount of MRSA recovered, and the fact that there was actually more MSSA recovered when Ward B, in particular, was receiving extra cleaning.
We directed the study cleaners to clean hand-touch sites on clinical equipment. Routine cleaning adheres to specified procedures for all surface levels and clinical equipment [29]. It appears that general surfaces receive more attention than others when there are time constraints; that is, staff are more likely to clean floors and toilets, than attend to handles, taps and other hand-touch surfaces [7,13,30]. Nurses are responsible for cleaning bedside areas and clinical equipment but they cannot clean these items properly when they are busy. Furthermore, the effects of a contaminated environment erode any benefits from increasing hand hygiene compliance [31]. This further supports extra cleaning for a ward, particularly one with high bed occupancy, high turnover and nurse shortages [10].
There are several reports in the literature documenting the effect of enhanced cleaning, introduced with educational programmes, in order to improve the quality of environmental cleaning [32][33][34]. These studies all report success in reducing environmental contamination from hospital pathogens, and one, using the presence of vancomycinresistant enterococci as hygiene indicator, also demonstrated a reduction in the number of patients colonised with this organism [32]. A more recent study describes the effect of vapourised hydrogen peroxide on Clostridium difficile in the environment [35]. The results indicated a significant reduction in environmental contamination of C. difficile and in the incidence of C. difficile infection on five wards. The findings from these studies support the results presented here, in that the environment plays an important role in the acquisition of hospital infection and that cleaning or other decontamination methods protect patients from hospital pathogens [32][33][34][35].

Conclusion
In summary, this study has shown that one additional cleaner on two surgical wards over 1 year can have an impact on the microbial contamination of high-risk hand-touch sites. Molecular epidemiological methods supported the possibility that patients acquired MRSA from these sites. There is a suggestion that the number of new MRSA infections were reduced relative to the level of MRSA patient-days. Further studies on targeted cleaning of hand-touch sites would be justified in terms of the overall costs of managing MRSA.