Abstract
Purpose of Review
The purpose of this review is to give the reader an update on recent studies and developments regarding the hospital environment role in transmission of healthcare-associated infections (HAIs), and novel strategies to obtain a cleaner, safer patient environment. Hospital patient rooms are increasingly recognized as a reservoir of multi-drug-resistant organisms that contribute to HAIs. In simulated environments, surfaces can easily be adequately disinfected of pathogenic bacteria. However, translation into real healthcare settings has been less reliable and efficacious, with barriers to implementation of best practices.
Recent Findings
In this review, we describe and compare new and evolving technologies for enhancing room disinfection, such as UV-C, hydrogen peroxide vapor, ozone, and chlorine. We also review recent studies examining antimicrobial surfaces such as copper and silver and introduce a novel transdisciplinary human factors, systems engineering, and infection prevention approach to improve manual room cleaning. We highlight outstanding questions, including additional benefit of no touch technology in a human factors-optimized manual cleaning setting, and cost-effectiveness of optimized manual cleaning vs additional of no touch technology.
Summary
There are evolving technologies and strategies to enhance patient room cleaning and decrease risk of HAI transmission. It is important for the infection prevention community to keep up to date with, and understand the implications of, these developments so as to best inform hospital HAI reduction strategy.
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Introduction
It is widely accepted that a contaminated healthcare environment plays a role in transmission of high-consequence pathogens in healthcare settings. The hospital physical environment is becoming increasingly recognized as a reservoir for multi-drug-resistant organisms (MDRO) and as an independent risk factor for acquisition of drug-resistant organisms and subsequent infections [1,2,3,4,5,6,7]. Important bacteria implicated in nosocomial infections such as methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, drug-resistant Acinetobacter, Clostridium difficile, and carbapenem-resistant Enterobactericiae as well as many pathogenic viruses have all been found in patient rooms [8,9,10,11,12,13,14,15]. Additionally, studies have demonstrated transmission of these organisms from the environment to the patient [16,17,18]. However, the role of the environment in transmission of pathogens is complex, how “clean” high touch surfaces need to be to prevent transmission of bacteria, and the relative importance of environmental cleaning to other aspects of a bundled infection prevention approach had not been elucidated [19••].
Hospitals in the USA are increasingly accountable for healthcare-associated infections (HAIs), measures that plays a significant role in hospital reimbursement and reputation [20,21]. When addressing interventions to prevent transmission of pathogens in the healthcare setting, more attention is being given to the role of the environment and environmental cleaning and disinfection. An increasing number of environmental strategies including disinfectants and no touch technologies are on the market for healthcare organizations to choose.
The purpose of this paper is to review newer developments in hospital disinfection and cleaning including no touch technologies such as UV-C, hydrogen peroxide vapor, ozone, and chlorine, and antimicrobial surfaces, and human factors and systems engineering approaches to improving manual room cleaning.
Current status
Adequate environmental cleaning is a vital component to prevent transmission of pathogens in the healthcare environment. Unfortunately, the efficacy of environmental cleaning has not met this important goal [14, 22,23,24,25,26]. Studies have shown that in research settings, adequate microbiologic disinfection with appropriate cleaning can be achieved; however, the translation of these practices into real-world settings has been disappointing. There is considerable variability in cleaning practice and outcomes by EVS staff [27,28,29,30]. Several interventions, including use of invisible markers and chemicals detecting organic substances coupled with feedback interventions, have been attempted with varying degrees of success [31,32,33,34,35,36,37,38,39,40,41,42].
Human factors and systems engineering approaches
The suboptimal cleaning of patient environment is commonly attributed to the environmental care (EVC) associate’s insufficient knowledge or skills, or inappropriate attitude. To date, performance improvement efforts have focused on monitoring the performance of EVC associates and with feedback and training [43,44]. While these studies have demonstrated improvements, the application of a human factors-based model such as the SEIPS (Systems Engineering Initiative for Patient Safety) to the process of patient room cleaning may offer benefits by incorporating the work system [37,40,45]. The SEIPS model explores the work system factors associated with patient room cleaning. This includes people (e.g., EVC associates, patients and families, healthcare providers), tools and technologies used (e.g., cleaning tools and supplies, documentation system), tasks performed (e.g., preparing carts, cleaning high-touch surfaces), and physical (e.g., size and layout of the patient room, design of the patient bed, and other environmental surfaces) and organizational (e.g., unit culture, work schedule, incentive structure) environments in which EVC associates work [46,47]. Ongoing work to address these issues may result in more sustainable improvement in patient room cleaning, thus negating the incremental benefit of additional no touch or other technologies.
No touch technologies
“No touch technologies,” the most well known being ultraviolet light and hydrogen peroxide vapor, are increasingly being used as an adjunct to manual disinfection in the hospital environment [48,49,50]. Published studies most commonly use these approaches as an adjunct to discharge cleaning and disinfection, targeted at rooms where the prior occupant is known to have harbored C. difficile or MDROs and have demonstrated improvements [51,52,53, 54••]. Much of the published literature on this topic, however, are not planned epidemiologically robust studies, but rather outbreak scenarios where a no touch technology is employed as part of a bundled infection prevention approach. One recent cluster-randomized, crossover trial at nine hospitals in the southeastern USA (the Benefits of Enhanced Terminal Room Disinfection study) by Anderson et al. was a targeted vertical approach examining the use of UV-C disinfection for discharge of patients known to harbor C. difficile or a MDRO: three different strategies of disinfection were compared with a standard strategy of quaternary ammonium for all except for C. difficile rooms where bleach was used. Intervention 1 was the standard strategy plus UV-C on discharge; intervention 2 was bleach for all rooms on discharge; intervention 3 was bleach plus UV-C for all rooms on discharge. Clinical outcomes were newly acquired positive culture of a patient who was in a room where the previous occupant was known to harbor that MDRO. Patients admitted to rooms previously occupied by patients harboring a MDRO or C. difficile were 10–30% less likely to acquire the same organism if the room was terminally disinfected using an enhanced strategy. Interestingly, similar risk reduction was found with bleach alone as with bleach and UV-C [54••].
Studies to date have looked at using UV-C light as a vertical approach, where it is used for those rooms where the occupant is known to harbor a MDRO or C. difficile. A single site cluster randomized controlled study is currently underway in cancer and transplant units of an academic hospital where UV-C is attempted to be used every day in every patient room and bathroom, regardless of MDRO or C. difficile status [55].
However, these technologies are costly, both in the purchase of the machines and for the personnel to implement it. The cost-effectiveness of these technologies compared with enhanced manual cleaning has not been fully elucidated. Other limitations include the need for manual cleaning before UV-C (as with most other no touch technologies including hydrogen peroxide vapor), specific trained personnel to use the device, and implementation challenges including delay in room turn over and timely coordination.
Hydrogen peroxide vapor
Hydrogen peroxide vapor (HPV) has been shown to be effective against multiple bacteria (including spore-forming) and viruses [56,57]. HPV-generating devices are marketed for patient room cleaning and decontamination. The device holds HP liquid (typically 30–35% weight/weight) which comes into contact with a hot plate and is vaporized, evaporated, and dispersed into the air of the patient room. When HPV concentration is higher than that of the surrounding air, a thin layer of HPV condensate settles on the surrounding surfaces. The remaining HPV in the air is broken down to water vapor and oxygen over time. As HPV is potentially harmful to humans (can cause irritation to eyes and oral mucosa), the room should not be entered until the occupational exposure limits (OEL) are less than 1 part per million [58].
There are multiple studies demonstrating effectiveness of HPV at reducing bacterial load in the patient environment [59]. A study using clinical outcomes demonstrated 64% reduction in any MDRO acquisition of subsequent room occupants when HPV was used post-discharge of known MDRO patients; the biggest impact was seen with VRE acquisition (adjusted incidence risk ratio, 0.20; 95% CI, 0.08–0.52) [60]. While this study did not find a statistically significant decrease on C. difficile acquisition, other studies have demonstrated reduced C. difficile acquisition [56,61,62]. A study in a 650-bed hospital in North Mississippi found C. difficile rate reduction from 1 case/1000 patient days to 0.4 cases/1000 patient days after implementing HPV disinfection throughout the center [50,57,61,62,63,64].
Cost-effectiveness analysis has been performed comparing resources and cost of eight different types of disinfection method: 1000 ppm chlorine-releasing agent (current practice of the study team), hydrogen peroxide vapor, dry ozone, microfiber cloths (Vermop) used in combination with and without a chlorine-releasing agent, and high temperature over heated dry atomized steam cleaning, steam cleaning, and peracetic acid wipes. Hospital rooms were disinfected and then contaminated with C. difficile spores, after which they were disinfected with one of the methods. Pre- and post-disinfection colony counts for each method were noted. The three most effective methods were hydrogen peroxide, 1000 ppm chlorine-releasing agent, and peracetic acid wipes. The total costs of each method per use and per month were calculated by summing the staff, equipment, or resources. For HPV, steam, and ozone, each machine was assumed to have a 3-year lifespan; dividing the capital cost by 36 gave a monthly depreciation cost. Each was compared to the 1000 ppm chlorine-releasing agent to assess incremental benefit. HPV had extra incremental cost of 138 lb above 1000 ppm chlorine. The authors recognize that there are newer devices such as chlorine dioxide that were not studied.
One of the disadvantages of HPV is that it requires the room to be left unoccupied until the OEL returns to safe levels. Although a lower concentration of HP would have practical benefits as the room would not need to be unoccupied post-usage for as long for air to reach the OEL, 10% HPV while nonpathogenic bacteria such as Geobacillus stearothermophilus (commonly used in bio-indicator cards to assess efficacy) are significantly reduced, it did not adequately disinfect MRSA. When studying the safest time to re-enter the room after hydrogen peroxide disinfection, Murdoch et al. found that even at 5%, there was still a concentration of 9.0 ppm after letting the gas naturally break down for over 3 h; above the safe OEL limit of 1.0 ppm, they suggest using forced aeration to shorten the time needed to ensure the safety of all who enter the room after cleaning [64].
Ozone
Bactericidal properties of ozone, an oxidizing agent, have been known for many years. In 1985, it was found to have extremely potent effects on vegetative bacteria, but was much less effective against fungi and bacterial spores [65,66]. However, its capability to damage materials and surfaces has limited its utilization in the clinical setting.
Sharma et al. tested the bactericidal capacity of ozone against 15 unique bacteria commonly found in hospital settings on plastic surfaces and both wet and dry fabric samples, to simulate a hospital room environment. The resulting data showed that at 25 ppm, relative humidity 90%, and 20-min exposure time, ozone was bactericidal, displaying a 3log10 reduction in bacterial CFU/ml. Additionally, they found the gas removal expedient and once removed posed no toxicity to the patient entering the room [67]. Another group found that ozone has distinct advantages over other disinfection methods—the disinfection time was 25 min shorter than that of hydrogen peroxide disinfection because of the shorter time it takes to get back to safe levels [68]. Recently, ozone has also been tested against antibiotic-resistant bacteria. It has been shown that at a dose of 3 mg/L decreased both the antibiotic-resistant bacteria and associated antibiotic-resistant genes by more than 90%; however, this reduction in the antibiotic resistance genes was stated to be incomplete and relatively ineffective [69].
However in 2012, a study using ozone for disinfection of C. difficile-contaminated rooms found only a 1.303log10 median reduction in colony count [68]. A more recent study by Martinelli et al. showed that using airborne ozone caused a moderate reduction in C. difficile colony count at 36 °C and no reduction at 22 °C [70]. Ozone was found to be ineffective at disinfection of hepatitis B virus, even when used for up to 90 min [71]. As with HPV, ozone also requires trained personnel to operate, and surfaces must be cleaned manually before ozone disinfection, extending the total disinfection time [68].
In recent years, ozone has been tested as a possible decontamination agent for specific hospital equipment such as corrugated tubing for ventilation machines and for decontaminating wastewater from the hospital, which normally carries with it highly concentrated cleaners, antibiotic-resistant bacteria, and discarded medications [72,73]. Additionally, some groups are beginning to look at the use of ozone combined with hydrogen peroxide for newer forms of combination cleaning for high-level disinfection of medical equipment, to our knowledge, there is no patient room cleaning combination product [74].
Steam
Steam disinfection is a new technology that has become portable and more easily used in recent years. The technology works by transforming water into a superheated, low-moisture steam which can then disrupt the cell membrane, thereby making bacteria more susceptible to high temperatures [75].
A number of groups have looked at the effects of steam disinfection on various bacteria and different surfaces that would be in the hospital room environment [76,77•]. Escherichia coli, Shigella flexneri, VRE, MRSA, Salmonella enterica, methicillin-sensitive Staphylococcus aureus, MS2 coliphage (a surrogate for nonenveloped viruses), Candida albicans, Aspergillus niger, and the endospores of C. difficile have been inoculated on six porous surfaces and then treated with steam disinfection. After only 5 s, all pathogens were completely inactivated [78]. Furthermore, when testing steam disinfection against extensively drug-resistant Acinetobacter baumannii, Pseudomonas aeruginosa, carbapenemase-producing Klebsiella pneumonia, MRSA, high-level aminoglycoside-resistant Enterococcus faecalis, Candida parapsilosis, and Aspergillus fumigatus on glass surfaces, Bagattini et al. found that they could achieve complete bacterial reduction from 109 CFU/ml with 5–7 min at 180 °C of steam contact time [79]. Some groups are recommending microfiber cloths and steam disinfection for use in discharge cleansing and in times of pathogen outbreaks, stating that the results are the same or better than traditional cleaning methods with less labor, fewer chemicals, less water consumed, and mass approval from the cleaning staff [76,77•].
Steam disinfection technology may have impact on biofilm formation and removal in the hospital room and on equipment. Song et al. tested the efficacy of steam on disrupting biofilms (composed of E. coli, P. aeruginosa, S. aureus, or A. baumannii) on polycarbonate surfaces. They found that even a 3-s steam treatment could kill each biofilm with 99.5% efficacy. They compared the efficacy of 1 s of steam disinfection to 10–20 min of contact time with sodium hypochlorite and found the steam more effective [75].
Steam disinfection methods do have some disadvantages. Like HPV, ozone, and UV-C cleaning methods, manual cleaning must be done before steam disinfection. There may also be condensate water on the floor after the steam disinfection has completed, which may act as a nidus for infection or lead to patient falls [68]. Steam disinfection uses a large amount of water and energy when used in the clinical setting. However, water and electricity usage can be reduced significantly when the steam sterilizer is turned to offsetting while not in use [80].
In recent years, there are emerging uses for steam disinfection. It has been demonstrated to be an effective method for cleaning nebulizers used for patients with cystic fibrosis; however, they should be left damp after cleaning because drying the devices after cleaning may be a source of recontamination [81].
Antimicrobial surfaces
There is increasing interest in materials used to make surfaces of hospital products, and novel approaches to prevention of bacteria from adhering onto items in the patient room.
Copper
In 2008, Weaver et al. described copper alloys with copper content > 70% having significant reduction in survival of C. difficile vegetative and spores compared with lower content copper or stainless steel surfaces [82]. Copper alloys are recognized by Environmental Protection Agency for continual antimicrobial effectiveness and may also have a role in decreasing surface biofilm formation [83]. More recent studies have translated those findings into the clinical setting [84,85,86, 87•, 88]. An ICU in Greece, endemic with multi-drug-resistant organisms, performed an interventional comparative cross over trial, introducing copper-coated beds and accessories into patient rooms. Environmental sampling found decreased percentage of surfaces colonized by MDR gram-negative and enterococci on the copper surfaces [84]. Most of the studies to date are looking at the effect of copper in adult ICUs; however, there are now studies looking at medical-surgical adult units and pediatric ICUs with similar type findings. On a medical-surgical unit, half the rooms on were outfitted with copper alloy materials, and compared with control rooms (traditional surfaces such as plastic, metal), and a decreased bacterial bioburden on copper alloy surfaces was found (median 0 vs 364 CFU/100 cm2). A 16-room pediatric ICU in Chile found a nonstatistically significant decrease in hospital-associated infections when copper surfaces were installed in 8 rooms, from 10.6 vs 13.0 per 1000 patient days for copper and noncopper-exposed patients [87•]. A study with patient-level randomization to available rooms with or without copper in ICUs of three hospitals found an overall lower proportion of patients developing any HAI, defined as a composite of bloodstream infection, pneumonia, urinary tract infection, Clostridium difficile infection (0.071 vs 0.128 p = 0.013), although there were questions regarding the definition of outcome data, and biological plausibility of the study findings [85,89,90].
The role of copper alloy in decreasing HAIs shows promise; however, sound epidemiologically designed trials, such as adequately powered cluster randomized trials, are needed to definitively answer the question of effectiveness of copper alloy surfaces on clinical outcomes. Patient-level randomization to examine this issue has significant limitations: due to potential decreases in colonization pressure, there is potential benefit to “control” patients on the unit, and operational difficulty in randomization in real world and not have spill over from intervention to control when patients are transferred to different room on the unit.
Silver
There is investigation into the effectiveness of silver in the hospital environment, as surfaces coated with agents containing silver ions appear to decrease adherence of microorganisms [91]. It is likely that the antimicrobial properties are due to its ability to bind with thiol on organism proteins and enzymes thereby rendering them inactive [92]. In two similar UK outpatient units, surfaces in one unit were treated with silver (BioCote®), and compared with the control unit, environmental sampling found decreased bacterial CFU from the surfaces in the silver-treated unit. There were also decreased bacterial counts on the untreated products in the same unit as silver-treated products, indicating possible benefit on the wider environment by decreasing bacterial load on some surfaces [93]. A more recent study, using a different silver ion containing product (BactiBlock®) did not find the same level of consistent efficacy [94]. In this quasi-experimental study conducted in two post-operative recovery units, weekly environmental sampling of surfaces was carried out pre- and post-application of silver coating of surfaces in the patient room. An antimicrobial acrylic coating with zinc pyrithione was sprayed on bedside table, wall, and bed rails. These surfaces had an increased mean CFU of bacteria in the post-intervention period (bedside table OR 2.59, 95% CI 1.22, 5.52). The floors and sinks were treated with a polyurethane silver coating, which was applied with a roller, had lower mean CFU in the post-period (sink OR 0.42, 95% CI 0.19–0.92). The authors hypothesize that more contamination was possibly due to the spray application, the different composition of the silver product used, and the difference in surface type.
Studies to date have been small; larger, more epidemiologically robust studies may help elucidate the true additional benefit of silver coating, and optimal method of application.
Conclusions
Despite the progress in strategies for disinfection of the hospital environment, there are still remaining unresolved issues and challenges. The benefit of sporicidal agent universal use, including in patient rooms not known to harbor clostridium difficile, and the role of Clostridium difficile carriers in transmission are not fully elucidated. The true additional benefit of “no touch” technology if manual cleaning is at a maximum is not understood, nor is the cost comparison of no touch technology vs. investment in optimizing manual cleaning infrastructure and systems (such as with use of human factors engineering approaches). The role of regulatory bodies, such as the Joint Commission or Centers for Disease Control and Prevention, in mandating monitoring and reporting of environmental cleaning is not fully explored, and could serve to be an impetus for hospitals to conduct performance improvement in this area. Difficulty in the establishment of industry standards, in order for new technologies to reach the market, and also for the hospital infection preventionist to easily be able to compare different technologies remains elusive. The increasing amount of equipment in the patient room, such as tablets and other handheld devices, will require infection prevention oversight. From future development perspective, HAIs remain rare outcomes which present challenges for research examining different disinfection approaches and implementation strategies with clinical outcomes. Mathematical modeling approaches may help with this, and use of surrogate outcomes. In addition, funding opportunities and philanthropy in this area are not plentiful. However, we remain optimistic that future studies will continue to inform and guide best practices and reduce the risk of HAI acquisition due to the hospital environment.
References and Recommended Reading
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance.
de Regt MJ, van der Wagen LE, Top J, Blok HE, et al. High acquisition and environmental contamination rates of CC17 ampicillin-resistant Enterococcus faecium in a Dutch hospital. J Antimicrob Chemother. 2008;62:1401–6.
Weber DJ, Anderson D, Rutala WA. The role of the surface environment in healthcare-associated infections. Curr Opin Infect Dis. 2013;26:338–44.
Weber DJ, Rutala WA, Miller MB, Huslage K, Sickbert-Bennett E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: Norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control. 2010;38:S25–33.
Smith SJ, Young V, Robertson C, Dancer SJ. Where do hands go? An audit of sequential hand-touch events on a hospital ward. J Hosp Infect. 2012;80:206–11.
Carling P. Methods for assessing the adequacy of practice and improving room disinfection. Am J Infect Control. 2013;41:S20–5.
Cheng VCC, Chau PH, Lee WM, Ho SKY, Lee DWY, So SYC, et al. Hand-touch contact assessment of high-touch and mutual-touch surfaces among healthcare workers, patients, and visitors. J Hosp Infect. 2015;90:220–5.
Grabsch EA, Burrell LJ, Padiglione A, O’Keeffe JM, Ballard S, Grayson ML. Risk of environmental and healthcare worker contamination with vancomycin-resistant enterococci during outpatient procedures and hemodialysis. Infect Control Hosp Epidemiol. 2006;27:287–93.
Weinstein RA, Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis. 2004;39:1182–9.
Lerner A, Adler A, Abu-Hanna J, Meitus I, Navon-Venezia S, Carmeli Y. Environmental contamination by Carbapenem-resistant Enterobacteriaceae. J Clin Microbiol. 2013;51:177–81.
Manian FA, Griesenauer S, Senkel D, Setzer JM, Doll SA, Perry AM, et al. Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better? Infect Control Hosp Epidemiol. 2011;32:667–72.
Mutters R, Nonnenmacher C, Susin C, Albrecht U, Kropatsch R, Schumacher S. Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction. J Hosp Infect. 2009;71:43–8.
Pankhurst L, Cloutman-Green E, Canales M, D’Arcy N, Hartley JC. Routine monitoring of adenovirus and norovirus within the health care environment. Am J Infect Control. 2014;42:1229–32.
Sexton T, Clarke P, O’Neill E, Dillane T, Humphreys H. Environmental reservoirs of methicillin-resistant Staphylococcus aureus in isolation rooms: correlation with patient isolates and implications for hospital hygiene. J Hosp Infect. 2006;62:187–94.
Strassle P, Thom KA, Johnson JK, Leekha S, Lissauer M, Zhu J, et al. The effect of terminal cleaning on environmental contamination rates of multidrug-resistant Acinetobacter baumannii. Am J Infect Control. 2012 [cited 2018 Jan 9]; 40. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3855251/.
Verity P, Wilcox MH, Fawley W, Parnell P. Prospective evaluation of environmental contamination by Clostridium difficile in isolation side rooms. J Hosp Infect. 2001;49:204–9.
Datta R, Platt R, Yokoe DS, Huang SS. Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants. Arch Intern Med. 2011;171:491–4.
Huang SS, Datta R, Platt R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med. 2006;166:1945–51.
Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A. Risk of acquiring multidrug-resistant Gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect. 2011;17:1201–8.
•• Ray AJ, Deshpande A, Fertelli D, Sitzlar BM, Thota P, Sankar CT, et al. A multicenter randomized trial to determine the effect of an environmental disinfection intervention on the incidence of healthcare-associated Clostridium difficile infection. Infect Control Amp Hosp Epidemiol. 2017;38:777–83. Fifteen hospital, 12 month, randomized trial comparing standard cleaning to enhanced cleaning with monitoring of environmental services staff found improved removal of fluorescent marker post cleaning and decreased recovery of Clostridium difficile in the patient environment but did not show reduction in incidence of healthcare associated CDI. Demonstrates the complexity of C. difficile acquisition and infection in the in-patient setting; environmental cleaning is one aspect of a bundled approach required to impact this measure.
Medicare C for, Baltimore MS 7500 SB, Usa M. HAC-Reduction-Program [Internet]. 2017 [cited 2018 Jan 9]. Available from: https://www.cms.gov/Medicare/Medicare-Fee-for-Service-Payment/AcuteInpatientPPS/HAC-Reduction-Program.html
Find and compare information about Hospitals | Hospital Compare [Internet]. [cited 2018 Jan 9]. Available from: https://www.medicare.gov/hospitalcompare/search.html
Carling PC, Briggs J, Hylander D, Perkins J. An evaluation of patient area cleaning in 3 hospitals using a novel targeting methodology. Am J Infect Control. 2006;34:513–9.
Carling PC, Von Beheren S, Kim P, Woods C. Intensive care unit environmental cleaning: an evaluation in sixteen hospitals using a novel assessment tool. J Hosp Infect. 2008;68:39–44.
Gavaldà L, Pequeño S, Soriano A, Dominguez MA. Environmental contamination by multidrug-resistant microorganisms after daily cleaning. Am J Infect Control. 2015;43:776–8.
Sigler V, Hensley S. Persistence of mixed staphylococci assemblages following disinfection of hospital room surfaces. J Hosp Infect. 2013;83:253–6.
Gordon L, Bruce N, Suh KN, Roth V. Evaluating and operationalizing an environmental auditing program: a pilot study. Am J Infect Control. 2014;42:702–7.
Boyce J, Havill N, Lipka A, Havill H, Rizvani R. Variations in hospital daily cleaning practices. Infect Control Hosp Epidemiol Off J Soc Hosp Epidemiol Am. 2010;31:99–101.
Rupp ME, Adler A, Schellen M, Cassling K, Fitzgerald T, Sholtz L, et al. The Time Spent Cleaning a Hospital Room Does Not Correlate with the Thoroughness of Cleaning. Infect Control Amp Hosp Epidemiol. 2013;34:100–2.
Eckstein BC, Adams DA, Eckstein EC, Rao A, Sethi AK, Yadavalli GK, et al. Reduction of Clostridium Difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods. BMC Infect Dis. 2007;7:61.
Aldeyab MA, McElnay JC, Elshibly SM, Hughes CM, McDowell DA, McMahon MAS, et al. Evaluation of the efficacy of a conventional cleaning regimen in removing Methicillin-resistant Staphylococcus aureus from contaminated surfaces in an intensive care unit. Infect Control Amp Hosp Epidemiol. 2009;30:304–6.
Carling PC, Parry MM, Rupp ME, Po JL, Dick B, Beheren SV, et al. Improving cleaning of the environment surrounding patients in 36 acute care hospitals. Infect Control Amp Hosp Epidemiol. 2008;29:1035–41.
Blue J, O’Neill C, Speziale P, Revill J, Ramage L, Ballantyne L. Use of a fluorescent chemical as a quality indicator for a hospital cleaning program. Can J Infect Control Off J Community Hosp Infect Control Assoc Can Rev Can Prev Infect. 2008;23:216–9.
Boyce JM, Havill NL, Dumigan DG, Golebiewski M, Balogun O, Rizvani R. Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay. Infect Control Amp Hosp Epidemiol. 2009;30:678–84.
Boyce JM, Havill NL, Havill HL, Mangione E, Dumigan DG, Moore BA. Comparison of fluorescent marker systems with 2 quantitative methods of assessing terminal cleaning practices. Infect Control Amp Hosp Epidemiol. 2011;32:1187–93.
Branch-Elliman W, Robillard E, McCarthy G, Gupta K. Direct feedback with the ATP luminometer as a process improvement tool for terminal cleaning of patient rooms. Am J Infect Control. 2014;42:195–7.
Carling PC, Briggs JL, Perkins J, Highlander D. Improved cleaning of patient rooms using a new targeting method. Clin Infect Dis. 2006;42:385–8.
Carling PC, Parry MF, Bruno-Murtha LA, Dick B. Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission*. Crit Care Med. 2010;38:1054–9.
Carling PC, Huang SS. Improving healthcare environmental cleaning and disinfection current and evolving issues. Infect Control Amp Hosp Epidemiol. 2013;34:507–13.
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 Off J Soc Hosp Epidemiol Am. 2008;29:593–9.
Munoz-Price LS, Ariza-Heredia E, Adams S, Olivier M, Francois L, Socarras M, et al. Use of UV powder for surveillance to improve environmental cleaning. Infect Control Hosp Epidemiol. 2011;32:283–5.
Ragan K, Khan A, Zeynalova N, McKernan P, Baser K, Muller MP. Use of audit and feedback with fluorescent targeting to achieve rapid improvements in room cleaning in the intensive care unit and ward settings. Am J Infect Control. 2012;40:284–6.
Sitzlar B, Deshpande A, Fertelli D, Kundrapu S, Sethi AK, Donskey CJ. An environmental disinfection odyssey: evaluation of sequential interventions to improve disinfection of Clostridium difficile isolation rooms. Infect Control Amp Hosp Epidemiol. 2013;34:459–65.
Han JH, Sullivan N, Leas BF, Pegues DA, Kaczmarek JL, Umscheid CA. Cleaning hospital room surfaces to prevent health care–associated infections. Ann Intern Med. 2015;163:598–607.
Mitchell G. Selecting the best theory to implement planned change. Nurs Manag Harrow Lond Engl 1994. 2013;20:32–7.
Rock C, Cosgrove SE, Keller SC, Enos-Graves H, Andonian J, Maragakis LL, et al. Using a human factors engineering approach to improve patient room cleaning and disinfection. Infect Control Amp Hosp Epidemiol. 2016;37:1502–6.
Holden RJ, Carayon P, Gurses AP, Hoonakker P, Hundt AS, Ozok AA, et al. SEIPS 2.0: A human factors framework for studying and improving the work of healthcare professionals and patients. Ergonomics. 2013 [cited 2018 Jan 9]; 56. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3835697/
Xie A, Carayon P. A systematic review of Human Factors and Ergonomics (HFE)-based healthcare system redesign for quality of care and patient safety. Ergonomics. 2015;58:33–49.
Rutala WA, Gergen MF, Weber DJ. Room decontamination with UV radiation. Infect Control Amp Hosp Epidemiol. 2010;31:1025–9.
Boyce JM, Havill NL, Moore BA. Terminal decontamination of patient rooms using an automated mobile UV light unit. Infect Control Amp Hosp Epidemiol. 2011;32:737–42.
Boyce J, Havill N, Otter J, Mcdonald L, Adams NM, Cooper T, et al. Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting. Infect Control Hosp Epidemiol Off J Soc Hosp Epidemiol Am. 2008;29:723–9.
Umezawa K, Asai S, Inokuchi S, Miyachi H. A comparative study of the bactericidal activity and daily disinfection housekeeping surfaces by a new portable pulsed UV radiation device. Curr Microbiol. 2012;64:581–7.
Anderson DJ, Gergen MF, Smathers E, Sexton DJ, Chen LF, Weber DJ, et al. Decontamination of targeted pathogens from patient rooms using an automated ultraviolet-C-emitting device. Infect Control Hosp Epidemiol. 2013;34:466–71.
Wong T, Woznow T, Petrie M, Murzello E, Muniak A, Kadora A, et al. Postdischarge decontamination of MRSA, VRE, and Clostridium difficile isolation rooms using 2 commercially available automated ultraviolet-C–emitting devices. Am J Infect Control. 2016;44:416–20.
•• Anderson DJ, Chen LF, Weber DJ, Moehring RW, Lewis SS, Triplett PF, et al. Enhanced terminal room disinfection and acquisition and infection caused by multidrug-resistant organisms and Clostridium difficile (the Benefits of Enhanced Terminal Room Disinfection study): a cluster-randomised, multicentre, crossover study. Lancet. 2017;389:805–14. Larger cluster randomized controlled trial using UV in conjunction with usual use (quaternary ammonia and bleach for c. diff) and enhanced use (bleach for all discharge) disinfection. This paper reinforced the knowledge that the hospital environment does play a role in transmission of Clostridium difficile and multidrug resistant organisms, however, UV plus bleach or bleach alone, on discharge showed similar reduction in risk of acquisition for the next patient occupant.
Ultra violet-C light evaluation as an adjunct to removing multi-drug resistant organisms (UVCLEAR-MDRO) - Full Text View - ClinicalTrials.gov [Internet]. [cited 2018 Jan 9]. Available from: https://clinicaltrials.gov/ct2/show/NCT02605499
Kokubo M, Inoue T, Akers J. Resistance of common environmental spores of the genus Bacillus to vapor hydrogen peroxide. PDA J Pharm Sci Technol. 1998;52:228–31.
Ali S, Muzslay M, Bruce M, Jeanes A, Moore G, Wilson APR. Efficacy of two hydrogen peroxide vapour aerial decontamination systems for enhanced disinfection of Methicillin-resistant Staphylococcus aureus, Klebsiella pneumoniae and Clostridium difficile in single isolation rooms. J Hosp Infect. 2016;93:70–7.
Bioquell Hydrogen Technology | Bioquell Advanced technologies Science [Internet]. Bioquell. [cited 2018 Jan 9]. Available from: https://www.bioquell.com/life-sciences/our-technology-for-life-sciences/
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. 2004;57:31–7.
Passaretti CL, Otter JA, Reich NG, Myers J, Shepard J, Ross T, et al. An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms. Clin Infect Dis. 2013;56:27–35.
McCord J, Prewitt M, Dyakova E, Mookerjee S, Otter JA. Reduction in Clostridium difficile infection associated with the introduction of hydrogen peroxide vapour automated room disinfection. J Hosp Infect. 2016;94:185–7.
Horn K, Otter JA. Hydrogen peroxide vapor room disinfection and hand hygiene improvements reduce Clostridium difficile infection, Methicillin-resistant Staphylococcus aureus, Vancomycin-resistant enterococci, and extended-spectrum β-lactamase. Am J Infect Control. 2015;43:1354–6.
Manian FA, Griesnauer S, Bryant A. Implementation of hospital-wide enhanced terminal cleaning of targeted patient rooms and its impact on endemic Clostridium difficile infection rates. Am J Infect Control. 2013;41:537–41.
Murdoch LE, Bailey L, Banham E, Watson F, Adams NMT, Chewins J. Evaluating different concentrations of hydrogen peroxide in an automated room disinfection system. Lett Appl Microbiol. 2016;63:178–82.
de Boer HEL, van Elzelingen-Dekker CM, van Rheenen-Verberg CMF, Spanjaard L. Use of gaseous ozone for eradication of Methicillin-resistant Staphylococcus aureus From the Home Environment of a Colonized Hospital Employee. Infect Control Amp Hosp Epidemiol. 2006;27:1120–2.
Foegeding PM. Ozone inactivation of Bacillus and Clostridium spore populations and the importance of the spore coat to resistance. Food Microbiol. 1985;2:123–34.
Sharma M, Hudson JB. Ozone gas is an effective and practical antibacterial agent. Am J Infect Control. 2008;36:559–63.
Doan L, Forrest H, Fakis A, Craig J, Claxton L, Khare M. Clinical and cost effectiveness of eight disinfection methods for terminal disinfection of hospital isolation rooms contaminated with Clostridium difficile 027. J Hosp Infect. 2012;82:114–21.
Sharma VK, Johnson N, Cizmas L, McDonald TJ, Kim H. A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere. 2016;150:702–14.
Martinelli M, Giovannangeli F, Rotunno S, Trombetta CM, Montomoli E. Water and air ozone treatment as an alternative sanitizing technology. J Prev Med Hyg. 2017;58:E48–52.
Guo D, Li Z, Jia B, Che X, Song T, Huang W. Comparison of the effects of formaldehyde and gaseous ozone on HBV-contaminated hospital quilts. Int J Clin Exp Med. 2015;8:19,454–9.
Lopes MS, JRF F, da Silva KB, de Oliveira Bacelar Simplício I, de Lima CJ, Fernandes AB. Disinfection of corrugated tubing by ozone and ultrasound in mechanically ventilated tracheostomized patients. J Hosp Infect. 2015;90:304–9.
Lee Y, Kovalova L, McArdell CS, von Gunten U. Prediction of micropollutant elimination during ozonation of a hospital wastewater effluent. Water Res. 2014;64:134–48.
Wallace CA. New developments in disinfection and sterilization. Am J Infect Control. 2016;44:e23–7.
Song L, Wu J, Xi C. Biofilms on environmental surfaces: evaluation of the disinfection efficacy of a novel steam vapor system. Am J Infect Control. 2012;40:926–30.
Abernethy M, Gillespie E, Snook K, Stuart RL. Microfiber and steam for environmental cleaning during an outbreak. Am J Infect Control. 2013;41:1134–5.
• Gillespie E, Williams N, Sloane T, Wright L, Kotsanas D, Stuart RL. Using microfiber and steam technology to improve cleaning outcomes in an intensive care unit. Am J Infect Control. 2015;43:177–9. The new cleaning involved using microfiber dampened with water for daily cleaning and a combination of microfiber with steam for discharge cleaning. The steam is used to dislodge organic matter, and no scrubbing is required. The microfiber collects the loosened organic matter, leaving surfaces visibly clean and removing bacterial burden. Microfiber cloths are being increasingly used, this novel pairing with steam may impact transmission of bacteria in the in-patient setting and deserves further evaluation.
Tanner BD. Reduction in infection risk through treatment of microbially contaminated surfaces with a novel, portable, saturated steam vapour disinfection system. Am J Infect Control. 2009;37:20–7.
Bagattini M, Buonocore R, Giannouli M, Mattiacci D, Bellopede R, Grimaldi N, et al. Effect of treatment with an overheated dry-saturated steam vapour disinfection system on multidrug and extensively drug-resistant nosocomial pathogens and comparison with sodium hypochlorite activity. BMC Res. Notes [Internet]. 2015 [cited 2017 Dec 19];8. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4600216/
McGain F, Moore G, Black J. Hospital steam sterilizer usage: could we switch off to save electricity and water? J Health Serv Res Policy. 2016;21:166–71.
Hohenwarter K, Prammer W, Aichinger W, Reychler G. An evaluation of different steam disinfection protocols for cystic fibrosis nebulizers. J Cyst Fibros. 2016;15:78–84.
Weaver L, Michels HT, Keevil CW. Survival of Clostridium difficile on copper and steel: futuristic options for hospital hygiene. J Hosp Infect. 2008;68:145–51.
Różańska A, Chmielarczyk A, Romaniszyn D, Bulanda M, Walkowicz M, Osuch P, et al. Antibiotic resistance, ability to form biofilm and susceptibility to copper alloys of selected staphylococcal strains isolated from touch surfaces in Polish hospital wards. Antimicrob Resist Infect Control. 2017;6:80.
Souli M, Antoniadou A, Katsarolis I, Mavrou I, Paramythiotou E, Papadomichelakis E, et al. Reduction of environmental contamination with multidrug-resistant bacteria by copper-alloy coating of surfaces in a highly endemic setting. Infect Control Amp Hosp Epidemiol. 2017;38:765–71.
Salgado CD, Sepkowitz KA, John JF, Cantey JR, Attaway HH, Freeman KD, et al. Copper surfaces reduce the rate of healthcare-acquired infections in the intensive care unit. Infect Control Hosp Epidemiol. 2013;34:479–86.
Sifri CD, Burke GH, Enfield KB. Reduced health care-associated infections in an acute care community hospital using a combination of self-disinfecting copper-impregnated composite hard surfaces and linens. Am J Infect Control. 2016;44:1565–71.
• von Dessauer B, Navarrete MS, Benadof D, Benavente C, Schmidt MG. Potential effectiveness of copper surfaces in reducing health care-associated infection rates in a pediatric intensive and intermediate care unit: a nonrandomized controlled trial. Am J Infect Control. 2016;44:e133–9. Individual patient (pediatric) level assignment to room furnished with or without limited number of copper alloyed surfaces. Found 10.6 vs 13.0 per 1,000 patient days for copper and non-copper exposed patients. This contributes to the understanding of how to estimate the effect size that copper may have on HAI acquisition. This important study could inform study design and power calculations for larger studies needed to answer the true effect of copper alloyed surfaces.
Schmidt MG, von Dessauer B, Benavente C, Benadof D, Cifuentes P, Elgueta A, et al. Copper surfaces are associated with significantly lower concentrations of bacteria on selected surfaces within a pediatric intensive care unit. Am J Infect Control. 2016;44:203–9.
Harbarth S, Maiwald M, Dancer S. The environment and healthcare-acquired infections: why accurate reporting and evaluation of biological plausibility are important. Infect Control Hosp Epidemiol Off J Soc Hosp Epidemiol Am. 2013;34:996–7.
Salgado CD, Sepkowitz KA, John JF, Cantey JR, Attaway HH, Freeman KD, et al. Reply to Harbarth et al. Infect Control Hosp Epidemiol. 2013;34:997–9.
Dancer SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev. 2014;27:665–90.
Lansdown ABG. Silver in health care: antimicrobial effects and safety in use. Curr Probl Dermatol. 2006;33:17–34.
Taylor L, Phillips P, Hastings R. Reduction of bacterial contamination in a healthcare environment by silver antimicrobial technology. J Infect Prev. 2009;10:6–12.
Ortí-Lucas RM, Muñoz-Miguel J. Effectiveness of surface coatings containing silver ions in bacterial decontamination in a recovery unit. Antimicrob Resist Infect Control. 2017 [cited 2018 Jan 9];6. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5470207/
Acknowledgments
Clare Rock receives research funding from Centers for Disease Control and Prevention Epicenter Program, Johns Hopkins University, grant number 1U54CK000447-01.
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Clare Rock leads a research study examining use of daily UV-C disinfection funded to Johns Hopkins University School of Medicine by The Clorox Company.
Bryce A. Small and Kerri A. Thom declare that they have no conflict of interest.
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This article does not contain any studies with human or animal subjects performed by any of the authors.
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This article is part of the Topical Collection on New Technologies and Advances in Infections Prevention
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Rock, C., Small, B.A., Thom, K.A. et al. Innovative Methods of Hospital Disinfection in Prevention of Healthcare-Associated Infections. Curr Treat Options Infect Dis 10, 65–77 (2018). https://doi.org/10.1007/s40506-018-0153-0
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DOI: https://doi.org/10.1007/s40506-018-0153-0