Floor cleaning: effect on bacteria and organic materials in hospital rooms
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1 Journal of Hospital Infection (29) 71, 57e65 Available online at Floor cleaning: effect on bacteria and organic materials in hospital rooms B.M. Andersen a,b, *, M. Rasch a, J. Kvist a, T. Tollefsen a, R. Lukkassen c, L. Sandvik d, A. Welo c a Department of Hospital Infections, Ullevål University Hospital, Oslo, Norway b Diakonova University College, Oslo, Norway c Department of Internal Service, Ullevål University, Oslo, Norway d Centre for Clinical Research, Ullevål University Hospital, Norway Received 16 December 27; accepted 16 September 28 Available online 17 November 28 KEYWORDS Floor mopping; Hospital cleaning; Infection control; Organic materials; Bacteria on floor Summary Routine surface cleaning is recommended to control the spread of pathogens in hospital environments. In Norway, ordinary cleaning of patient rooms is traditionally performed with soap and water. In this study, four floor-mopping methods e dry, spray, moist and wet mopping e were compared by two systems using adenosine triphosphate (ATP) bioluminescence (Hygiena and Biotrace). These systems assess residual organic soil on surfaces. The floor-mopping methods were also assessed by microbiological samples from the floor and air, before and after cleaning. All methods reduced organic material on the floors but wet and moist mopping seemed to be the most effective (P <.1, P <.11, respectively, ATP Hygiena). The two ATP methods were easy to use, although each had their own reading scales. Cleaning reduced organic material to 5e36% of the level present before cleaning, depending upon mopping method. All four mopping methods reduced bacteria on the floor from about 6e1 to 3e6 colony-forming units (cfu)/2 cm 2 floor. Wet, moist and dry mopping seemed to be more effective in reducing bacteria on the floor, than the spray mopping (P ¼.7, P ¼.2 and P ¼.11, respectively). The burden of bacteria in air increased for all methods just after mopping. The overall best cleaning methods seemed to be moist and wet mopping. ª 28 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. * Corresponding author. Address: Department of Hospital Infections, Ullevål University Hospital, Oslo, Norway. Tel.: þ ; fax: þ address: bomarand@hotmail.com /$ - see front matter ª 28 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:1.116/j.jhin
2 58 B.M. Andersen et al. Introduction Good hygienic routines based on cleaning of surfaces are recommended to help control the spread of pathogens in hospital environments. 1e11 In Norway, cleaning of all types of floors in patient rooms have traditionally been performed with ordinary soap without disinfectants and water. 5,8,9 Disinfectants such as 5% chloramine have been used for disinfection during isolation and for terminal decontamination of isolation rooms after discharge of patients with infections. 5,12 In recent years, a dry mist of hydrogen peroxide disinfectant has also been used in rooms contaminated with meticillin-resistant Staphylococcus aureus (MRSA). 13,14 Nosocomial transmission is especially associated with robust and long-living environmental microbes, such as Clostridium difficile, Acinetobacter baumannii, S. aureus including MRSA, Pseudomonas, vancomycin-resistant enterococci (VRE) and norovirus. 1,11,14e22 Floor cleaning mechanically removes organic soil and dirt that supports bacterial growth and also removes some of the resident flora. 1e9 However, within a few hours the floor is contaminated with new microbes. 4 Organic materials on surfaces may be detected by the use of an adenosine triphosphate (ATP) bioluminescence test. 2,6e9 The aim of this study was to examine the load of organic materials and bacteria (colony-forming units: cfu) on the floors in patient rooms during ordinary use and to study the effect of four floorcleaning methods on the presence of organic materials and bacteria. In addition we studied the ease of use of two adenosine triphosphate (ATP) bioluminescence swab methods, with different scales on their instruments, for assessing organic soil on the floors before and after cleaning. Methods Study setting and routine cleaning routines Four bedrooms at the Department of Geriatrics, Ullevål University Hospital, were chosen for the study. The rooms were two-bed rooms, nearly identical in size: w22 m 2. The floor was vinyl-covered. Patients using the rooms had different disease categories and had the ability to move around. The patients were mostly women and stayed for w5e7 days in the ward. There were no known infections during the study period. The rooms had common bathrooms in the corridor. There was no specific ventilation system. Each morning, after finishing the experiment, there was an ordinary cleaning of all rooms with moist mopping five days and wet mopping two days per week. 5 Experiment area A preset area of 1 1 m at the foot end of the first bed in the room was used during all cleaning experiments. During the study period (cleaning and sampling period) no person stepped over this area. The patients were either in bed or outside the room during the period. Only one cleaning experiment (in the preset area) was performed in a room each day. A preset rotation system ensured that each cleaning method had been tried in the same room during a four-day period. Cleaning methods Four cleaning methods were compared: dry, spray, moist and wet mopping. The mop pad used was Swep Classic MicroTechnomop (SWEP-High speed Finnmopp, Vileda, Freudenberg Haushaltsprodukte KG, Weinheim, Germany). All cleaning utilities (cart, rack, soap bottles, etc.) were cleaned between rooms, and buckets, soap bottles and mops were decontaminated (85 C) within the last 18 h before use. The cleaning cart was placed in the corridor outside the actual study room. Water was taken from the ordinary sink for floor cleaning. It comes from the communal waterserving system and contains 2 ppm chloride on leaving the central system and ppm at the designated sink. Samples from the central water system are controlled once a week, with an alert issued to the hospital if there is any contamination. That did not occur during the study period. The degree of pressure used in cleaning was not studied. The cleaning agent used was Allrent (Ren Såpeindustri A/S, Fredrikstad, Norway; containing 2-propanol: 1e5% weight; tensides 1e5% weight; 6e1% weight water) and tested negative for microbial growth. Two trained persons cleaned the floors, in accordance with usual work routines in the department. There was no observation of the pressure used during the cleaning process. Each member of the cleaning staff used a clean suit and new clean single-use gloves for each experiment. The cleaning process The cleaning was performed by wiping the mop once across the test surface by moving it in form of an 8, from one side to the other.
3 Floor-cleaning methods for hospitals 59 e Dry mopping: Swep 5 cm, dry micro mop, 1% microfibre. Each time a clean, dry, new mop was used. e Spray mopping: Swep 5 cm, dry micro mop, 95% microfibre (1% polyester fibre) was used. 15e2 ml water with soap was added to the floor before washing. e Moist mopping: Swep 5 cm, micro mop (see above), was moist after washing at temperature up to 85 C and centrifugation for 3e 5 min, put in a clean plastic bag and placed in cooler until next morning. e Wet mopping: Blue Swep mop, polyester fibre 5% and viscose 5%. The mop was moistened in 3 L soap water 4 C before washing over the area, followed by dry mopping over the same area, but inside the wet area (see above). Sampling Sampling was performed just before, and within 1 min after cleaning, inside the preset area. Floor samples were not taken from visibly stained areas. A preset area of 1 1 m outside the foot end of the first bed in the room was used during the experiments. The sampling point was chosen because it was not too close to the washing stand and was a site exposed to nearly all persons entering the room during the 24 h period. The samples of ATP and colony-forming units (cfu) were taken at different, randomly chosen, not fixed sites, within this area. Before and after each cleaning, the ATP samples were taken first, then the microbiological samples. Samples were taken at three different positions before and after cleaning (see above). Standard contact plates (w2 cm 2 area) filled with 15 ml tryptic soy agar (TSA, Difco/Becton Dickinson, no. 1143) were used. The agar plates were tested for sterility and growth of three control organisms (Bacillus subtilis ATCC 6633, Staphylococcus aureus ATCC 6538 and Candida albicans ATCC 1231) before use. The plates were incubated at 37 C for 48 h and cfu counted. The counting limit was 25 cfu per plate, i.e. dishes with more colonies were classified as >25 cfu. An SAS air sampler was used to take air samples; one 1 L air/sample before and one after cleaning. The tryptic soy agar plates were incubated and read as shown above. The presence of organic material was tested indirectly by bioluminescence detection of adenosine triphosphate (ATP) by two different methods; the ATP Biotrace (Biotrace International Plc, Bridgend, UK, using a Uni-Lite luminometer) and the Hygiena (read using a system SURE II ATP luminometer, Hygiena International Ltd, and Food Diagnostics AS, Oslo, Norway). Three separate samples were taken before and after cleaning using each method. The sample sites were three separate areas of 1 1 cm within the preset floor area, and were all different for the two ATP methods. The sample pencils were turned around while sweeping 1 times over the 1 1 cm area. All results were read immediately after sampling as relative light units (RLU). Statistical analysis All statistical analyses were done using SPSS 1. for windows (SPSS, Chicago, IL, USA). Differences between mean number of groups were assessed by t-test, paired samples statistics, two-tailed and alpha set at.5. Results Effect on organic materials measured by ATP Altogether 96 samples were taken before, and 96 after, each of the four cleaning methods using the two ATP systems in parallel. Presence of organic materials varied between rooms and days, dependent on activities of the patients and personnel. The mean value before cleaning was 856 (1e4352) (RLU) for the ATP Hygiena and 8443 (399e46 493) RLU for the ATP Biotrace. The percentage residual ATP after cleaning varied between mopping methods, and from one day to another, as shown for both ATP methods (Figures 1 and 2). Moist and wet mopping was associated with lower residual amounts of organic materials than dry and spray mopping (Figure 3). Wet mopping was significantly more effective in reducing organic materials on the floor than spray and dry mopping (P ¼.11 and P <.1, respectively), although not as effective as moist mopping (Table I). Moist mopping was more effective than dry mopping and spray mopping (P ¼.7 and P ¼.51, respectively, ATP Hygiena) (Table I). After cleaning, the ATP level was 5e36% of the value before cleaning (Figure 3). Each of the two ATP methods had different scales, concerning the RLU values (Figure 4), as further demonstrated in Table II. Cleaning reduced the ATP from 7e9 before, to <1 RLU after, measured by ATP Hygiena, and from 8e9 before, to <5 RLU after, measured by the ATP Biotrace.
4 6 B.M. Andersen et al Percent residual ATP after mopping Number of separate experiments Figure 1 Residual organic material after mopping, measured by ATP Hygiena Percent residual ATP after mopping Number of separate experiments Figure 2 Residual organic material after mopping measured by ATP Biotrace.
5 Floor-cleaning methods for hospitals residual ATP (mean) Percent residual ATP after mopping Biotrace Hygiena Biotrace Hygiena Biotrace Hygiena Biotrace Hygiena Figure 3 Percentage residual organic materials after mopping, measured by two ATP methods. Mean values of 16 experiments each with three paired samples, before and after mopping. Mopping effect on microbes on the floor Bacteria on the floor showed a large day-to-day variation (Figure 5). Before cleaning, the mean bacterial count was 83 cfu/2 cm 2. A mean of w6% of cfu was removed by dry, moist and wet mopping, but only 3% by the spray mopping (Figure 6). All four methods reduced the bacteria on the floor from 6e1 to 3e6 cfu/2 cm 2 (Figure 7). Mean values, standard error and range for cfu are shown in Table III. Wet, moist and dry mopping reduced counts on the floor more effectively than spray mopping (P ¼.7, P ¼.2 and P ¼.11, respectively). Mopping effect on cfu/m 3 air There was no significant difference between the four mopping methods concerning effect on bacteria in air, but after mopping, the mean numbers of cfu/m 3 air increased for all four methods. Discussion In Norway, the use of ordinary soap (without disinfectants) and water is recommended for cleaning of patient wards without special infections. This is done to avoid development of microbial resistance to disinfectants. 5,8,1,11,22e27 Table I Percent residual organic material (mean) detected by ATP Hygiena and ATP Biotrace after cleaning with four mopping methods (paired samples statistics) Mopping methods compared ATP Hygiena ATP Biotrace Mean Mean (2-tailed) P value Mean Mean (2-tailed) P value Dry: wet < Spray: wet < Moist: wet
6 62 B.M. Andersen et al ATP relative light units Before After Before After Before After Before After Before After Before After Before After Before After Biotrace Hygiena Biotrace Hygiena Biotrace Hygiena Biotrace Hygiena Figure 4 Organic materials on the floor before and after mopping, studied by two ATP methods, Biotrace and Hygiena. Black bars: mean; white bars: SD. This study attempted to measure organic soil and bacteria on the floors in patient rooms during ordinary use, and to observe the effect of four floor-cleaning methods: dry, spray, moist and wet mopping. Two different adenosine triphosphate (ATP) bioluminescence swab methods, ATP Hygiena and ATP Biotrace, were used to assess residual organic soil on the floors, before and after cleaning. The rooms were in ordinary use during the study period, with patients, personnel and visitors coming and going. Limitations of this study was a non-standardised, variable contamination of the patient room by more or less bed-ridden, elderly persons, and variable activity of personnel and visitors. Only two trained personnel cleaned the floor each time; however, differences in washing technique may have influenced the results. Thus, the organic and bacterial loads and the cleaning technique could probably have influenced the results. The mean value of organic materials before cleaning the ward floor was 856 (1e4352) (RLU) for Table II Organic material detected by ATP relative light units (RLU) using ATP Hygiena and ATP Biotrace before and after cleaning the floor with four mopping methods Mopping method ATP sampled ATP Hygiena ATP Biotrace ATP RLU Residual ATP (%) ATP RLU Residual ATP (%) Mean SE Range Mean SE Range Dry Before e e After e e Spray Before e e35 8 After e e Moist Before e e33 63 After e e Wet Before e e46493 After e e
7 Floor-cleaning methods for hospitals Dry mopping Sprinkle mopping Moist mopping Wet mopping Percent residual cfu compared to before mopping Number of separate experiments Figure 5 Effect of four mopping methods on bacteria (cfu) on floor. the ATP Hygiena and 8443 (399e46 493) RLU for the ATP Biotrace. A cleaned floor area tended to have an ATP value of <1 RLU by ATP Hygiena and <5 RLU by ATP Biotrace. Using the ATP Biotrace system, Griffith et al. found a mean of (1698e163 87) RLU on ward floor before and 1911 (341e3926) RLU after cleaning with a modified sanitiser. 7 A study from the UK Department of Health, using ATP Hygiena, cfu Dry Spray Moist Wet Figure 6 Percentage of mean residual cfu on the floors after mopping. found a mean of 269 (14e165) RLU on the floor under beds. 28 Both instruments were easy to use, but had different scales of registration. It is not possible from our study to define the best ATP method, since the presence of organic material measured was not standardised. To compare sensitivity and reproducibility, a laboratory trial would need to be done with known and fixed levels of soil under more tightly controlled conditions. All four cleaning methods reduced organic materials on the floors. The ATP level after cleaning was 5e36% of the value before cleaning, dependent on mopping method. Wet mopping was more effective than dry and spray mopping (P <.1 and P ¼.11, respectively). Moist mopping was also more effective than dry and spray mopping (P ¼.7 and P ¼.51, respectively). All four cleaning methods reduced bacteria on the floor from a mean of 6e1 to 3e6 cfu/2 cm 2 floor. Wet, moist and dry mopping were more effective in reducing bacteria on the floor than spray mopping; P ¼.7, P ¼.2 and P ¼.11, respectively. The burden of bacteria (mean values) increased in air after mopping with all methods.
8 64 B.M. Andersen et al cfu Before After Before After Before After Before After Figure 7 Colony-forming units (cfu) on the floor before and after mopping. Black bars: mean; white bars: SD. It has been shown that increased environmental cleaning regimens may stop or reduce the infection rate or outbreaks both inside and outside the healthcare system. 1,1,11,14e16,19e21,26 Since visual assessments may be a poor indicator of cleaning efficacy, indicators such as ATP and cfu may be useful as controls, providing there is a standardisation of the methods. 1,2,6,7,28e31 In conclusion, all cleaning methods reduced organic soil on floors, but wet and moist mopping seemed to be the most effective. All four methods reduced bacteria on floors, but may have contributed towards increased bacterial counts in the air Table III Colony-forming units (cfu) 2 cm 2 floor before and after cleaning with four mopping methods Mopping method Sampled cfu Residual cfu (%) Mean SE Range Dry Before e263 After e Spray Before e4 After e2 72. Moist Before e2 After e Wet Before e4 After e just after mopping. The overall best cleaning methods seemed to be moist and wet mopping. The presence of ATP and bacteria may be used as indicators for surface soil and cleaning effectiveness but further studies and standardisation are needed. Acknowledgement K. Torgvær, L. Saliendra and S. Aydin, Department of Internal Service, Ullevål University Hospital are thanked for participation in the study. Conflict of interest statement None declared. Funding sources None. References 1. Dancer SJ. Mopping up hospital infection. J Hosp Infect 1999;43:85e1. 2. Griffith CJ, Cooper RA, Gilmore J, Davies C, Lewis M. An evaluation of hospital cleaning regimes and standards. J Hosp Infect 2;45:19e28.
9 Floor-cleaning methods for hospitals Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 24;39:1182e Ayliffe GAJ, Fraise AP, Geddes AM, Mitchell K. Control of hospital infections: a practical handbook. 4th ed. London: Hodder Arnold; Syvrud EJ, Lukkassen R, Solheim N, Andersen BM, Hochlin K, Rasch M. Cleaning in patient wards. In: Andersen BM, editor. Handbook in hygiene and infection control. Oslo: Ullevaal University Hospital; 23. p. 48e Dancer SJ. How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals. J Hosp Infect 24;56:1e Griffith CJ, Obee P, Cooper RA, Burton NF, Lewis M. The effectiveness of existing and modified cleaning regimes in a Welsh hospital. J Hosp Infect 27;66:352e Andersen BM, Solheim N, Kruger Ø, Sogn K, Moløkken I, Levy F. Effect of cleaning on bacteria and organic materials in patient rooms. Tidsskr Nor Lægeforen 1997;117:838e Andersen BM, Røed RTh, Solheim N, et al. Air quality and microbial contamination in operation rooms with and without laminary air flow. Tidsskr Nor Lægeforen 1998;2:3148e Boyce JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 27; 65:5e Fraise AP. Decontamination of the environment. J Hosp Infect 27;65:58e Andersen BM, Bånrud H, Bøe E, Bjordal O, Drangsholt F. Comparison of UVC light and chemicals for disinfection of surfaces in hospital isolation units. Infect Control Hosp Epidemiol 26;27:729e Andersen BM, Rasch M, Hochlin K, Jensen JF, Wismar P, Fredriksen JE. Decontamination of rooms, medical equipment and ambulances, using a dry mist of hydrogen peroxide disinfectant. J Hosp Infect 26;62:149e French GL, Otter JA, Shannon KP, Adams NMT, Watling D, Parks MJ. Tackling contamination of the hospital environment by methicillin-resistant Staphylococcus aureus (MRSA): a comparison between conventional terminal cleaning and hydrogen peroxide vapour decontamination. J Hosp Infect 24;57:31e Weber DJ, Rutala WA. The emerging nosocomial pathogens Cryptosporidium, Escherichia coli O 157:H7, Helicobacter pylori, and hepatitis C: epidemiology, environmental survival, efficacy of disinfection, and control measures. Infect Control Hosp Epidemiol 21;22:36e Rutala WA, Weber DJ. Environmental interventions to control nosocomial infections. Infect Control Hosp Epidemiol 1995;16:442e Levin AS, Gobara S, Mendes C, Cursino R, Sinto S. Environmental contamination by multidrug-resistant Acinetobacter baumannii in an intensive care unit. Infect Control Hosp Epidemiol 21;22:717e Shiomori T, Miyamoto H, Makishima K, et al. Evaluation of bedmaking-related airborne and surface methicillin-resistant Staphyloccus aureus contamination. J Hosp Infect 22;5:3e Rampling A, Wiseman S, Davis L, et al. Evidence that hospital hygiene is important in the control of methicillinresistant Staphylococcus aureus. J Hosp Infect 21;49: 19e Wilcox MH. Cleaning up Clostridium difficile infection. Lancet 1996;348:767e Denton M, Wilcox MH, Parnell P, et al. Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit. J Hosp Infect 24;56:16e Kuusi K, Nuorti JP, Maunula L, et al. A prolonged outbreak of Norwalk-like calicivirus (NLV) gastroenteritis in a rehabilitation centre due to environmental contamination. Epidemiol Infect 22;129:133e Weist K, Pollege K, Schulz I, Ruden H, Gastmeier P. How many nosocomial infections are associated with cross-transmission? A prospective cohort study in a surgical intensive care unit. Infect Control Hosp Epidemiol; 22;23: 127e Wisplinghoff H, Schmitt R, Wøhrmann A, Stefanik D, Seifert H. Resistance to disinfectants in epidemiologically defined clinical isolates of Acinetobacter baumannii. J Hosp Infect 27;66:174e Maillard J-Y. Bacterial resistance to biocides in the healthcare environment: should it be of genuine concern? J Hosp Infect 27;65:6e Dettenkofer M, Spencer RC. Importance of environmental decontamination. A critical view. J Hosp Infect 27;65: 55e Terpstra FG, van den Blink AE, Bos LM, et al. Resistance of surface-dried virus to common disinfection procedures. J Hosp Infect 27;66:332e Department of Health, UK. Evaluation of ATP bioluminiscence swabbing as a monitoring and training tool for effective hospital cleaning. London: Department of Health; Griffith CJ. Improving surface sampling and detection of contamination. In: Handbook of hygiene control in the food industry. Cambridge: Woodhead Publishing; Malik RE, Cooper RA, Griffith CJ. Use of audit tools to evaluate efficacy of cleaning systems in hospitals. Am J Infect Control 27;31:181e Cooper R, Griffith CJ, Malik RE, Obee P, Looker N. Monitoring the effectiveness of cleaning in four British hospitals. Am J Infect Control 27;35:338e341.
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