Use of gaseous decontamination technologies for wards and isolation rooms in hospitals and healthcare settings☆

Use of gaseous decontamination technologies for wards and isolation rooms in hospitals and healthcare settings☆

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T. Pottage, J.T. Walker Public Health England, London, United Kingdom

14.1 Introduction Gaseous decontamination can be used to decontaminate (and sterilize) a wide range of items and chambers. These range from small single-use medical devices [1] to large buildings, e.g., decontamination of buildings during the 2001 Bacillus anthracis US anthrax attacks [2]. There are a wide range of gaseous decontaminant options available for use depending on the application required, turnaround time, residue formation, and environmental conditions, etc. Gaseous decontamination has been used for many years to decontaminate enclosures and instruments [3–5] both prior to and after handling biological agents. Decontamination is used to lower the microbial contamination on a surface before use to ensure there is no contamination transferred to other surfaces. This principle can also be used in the hospital environment to ensure a room or ward is free from any harmful microorganisms prior to occupation by a patient or patients, reducing the risk of these patient(s) becoming ill and preventing an extension of their stay in the hospital which would otherwise incur more time and cost. There is evidence to show that contaminated hospital surfaces can result in the transmission of nosocomial pathogens [6]. Specifically, the admission of a patient into a room previously occupied by a meticillin-resistant Staphylococcus aureus (MRSA) or vancomycin-resistant Enterococcus (VRE) positive patient significantly increased the risk of transmission to the new occupant [7]. A more recent study found that there was a 40% increased risk of acquiring a MRSA or VRE infection in an intensive care unit if the previous patient was positive for these organisms [8]. Common hand touch sites near MRSA-infected patients frequently become contaminated with MRSA. Healthcare workers can then contaminate their hands when touching these sites and transmit the organisms to other patients [9–11], visitors, and other healthcare workers. To combat the organisms responsible for healthcare-acquired infections (HAIs), recommended interventions for improving decontamination procedures by Datta et al. [8] ☆

This chapter is a reprint of the chapter originally published in the first edition of Decontamination in hospitals and healthcare.

Decontamination in Hospitals and Healthcare. https://doi.org/10.1016/B978-0-08-102565-9.00014-5 © 2020 Elsevier Ltd. All rights reserved.

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consisted of saturating cleaning cloths in disinfectant before use and increasing the education of staff about repeated bucket immersion while cleaning [8]. In general good cleaning and disinfection procedures have been shown to reduce the incidence of HAIs [9]. Some of the more common organisms causing HAIs are relatively resistant to the disinfectants used within hospitals [12] and this indicates that further cleaning and decontamination steps may be needed to reduce the risk of organism transmission from person to surface to person. In fact inadequate disinfection procedures can lead to environmental transmission of pathogenic organisms to patients within hospitals [13]. HAI agents have also been shown to persist in the environment for extended periods of time, ranging from weeks to months for some organisms [12, 14, 15]. Spores of Clostridium difficile that were inoculated onto part of a hospital floor were found to be viable for up to 5 months [12]. Epidemic strains of MRSA were found to survive on Formica coupons for up to 14 days [16] and clinical strains of VRE pipetted onto polyvinyl chloride were recovered after drying and storage for 4 months [17]. In contrast to manual terminal cleaning (used on its own to decontaminate hospital surfaces), gaseous decontamination is used at present as an aid in the decontamination of side rooms after patients carrying HAIs [18], e.g., MRSA and C. difficile, have vacated the room. The gaseous decontamination technologies are used in conjunction with traditional surface cleaning methods to ensure all surfaces have been adequately decontaminated. There are two main approaches to gaseous decontamination used by the manufacturers. The first approach is to energize a liquid to create a vapor which is then injected into the enclosure above the dew point and condensation will form on the surfaces. Again there are different approaches to this; liquid is either heated to produce the vapor [18, 19] or through passing the liquid through a fine nozzle to produce a mist [20, 21]. This approach will allow contact of the vaporized decontaminant and the surfaces within the enclosure, allowing the decontaminant to destroy the microorganisms present. With this approach the injection of a vaporized liquid will cause the humidity in the chamber to increase to the point where the decontaminant will condense onto the surfaces. Technologies have been developed where the decontamination generator can be connected to (or incorporate) a dehumidifier. Air from the enclosure is passed through the dehumidifier and the relative humidity decreased, which in turn allows a higher concentration of vaporized decontaminant to be injected into the enclosure without condensation forming on the surfaces. The second approach is to use a true gas for the decontamination of the enclosure. This approach will not cause any condensation to form on surfaces. Technologies producing a true gas can generally decontaminate a larger volume with one generator because the gas will penetrate further into the chamber without condensing on surfaces. Chlorine dioxide is an example of a true gas decontamination technology, but it has been found by one of the main producers of the technology that humidity greater than 65% is needed in the enclosure for an effective decontamination cycle [22]. A lower humidity can be used but longer cycle times are needed and a much greater decontaminant concentration has to be produced which could lead to material compatibility issues [23], which have been witnessed when using liquid chlorine dioxide [24]. Gaseous decontamination is currently used within the hospital environment for the sterilization of medical devices that are thermolabile and therefore cannot be

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d­ econtaminated using traditional autoclaving methods [1, 25]. The decontamination technologies use small, sealable chambers where the equipment, packaged in bags that allow vapor penetration, is placed onto a rack to allow for diffusion around the chamber. The following sections of the chapter will detail problems associated with using gaseous decontamination and review current applications in the healthcare setting:

14.2 Challenges and considerations for gaseous decontamination in a healthcare setting The transition of using gaseous decontaminant from a laboratory to a healthcare environment is not a straightforward process. Some systems are already used for medical device decontamination within hospitals. These systems use small, specialized chambers where the gaseous decontaminant can be injected and removed in a tightly controlled environment. An example of this type of system is the hydrogen peroxide gas plasma; this decontamination approach has been designed for the decontamination of heat-labile instruments, using small chambers (up to 150 L) where a vacuum is drawn prior to gas injection. This technology has quick cycle times due to the small chamber size allowing quick diffusion of the gas, and during aeration a vacuum can be drawn to facilitate the removal of the decontaminant in the chamber. Systems such as ethylene oxide have been used successfully for many years to decontaminate medical items [26]. The ethylene oxide systems have the advantage that the gas can easily diffuse through porous packaging, allowing sterilization of packaged equipment and maintaining sterility of the item when it is removed from the system. This section will establish the main challenges that need to be addressed and overcome for the technologies to be used in situ.

14.2.1 Decontaminant toxicity One of the major drawbacks of any gaseous decontamination process is the toxicity of the decontaminant itself [27]. By definition, a decontaminant needs to have a certain level of toxicity to ensure it effectively destroys the microorganisms it contacts. When used at an effective concentration the gaseous decontaminant is likely to be harmful to any person who comes in contact with it, and workplace exposure limits (WELs) have been set to protect users [27]. In the laboratory, fumigation is undertaken in specially designed enclosures, such as safety cabinets and the laboratories themselves. The facilities are engineered with the specific purpose of being sealable to stop any of the microorganisms under investigation being released to the surrounding area and potentially infecting people, animals, or the environment. This sealability also means that a toxic gas can be introduced with a minimal risk of leakage. Hospitals range from new builds that can be designed for gaseous decontamination to older buildings, with Nightingale wards, which were not designed to have sealed rooms for gaseous decontamination. A leak in the room being decontaminated would cause a safety issue with

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Table 14.1  Workplace exposure limits for gaseous decontaminants. Agent

Short-term exposure limits European (ppm)

Long-term exposure limits European (ppm)

Formaldehyde Hydrogen peroxide Chlorine dioxide

0.3–1 0.5–2 0.1–0.3

0.3–0.5 0.5–1 0.1

the levels of decontaminant escaping to other populated areas above the workplace exposure limits [27]. Table 14.1 shows the WEL for three commonly used gaseous decontaminants. A leak of decontaminant from the room could also cause the level within the room to drop below the concentration required for an effective decontamination, potentially leaving viable hazardous organisms. Rooms can be adapted and their sealability increased using engineering designs such as replacement of older windows with modern sealed units. The provision of gas-tight dampers in the air conditioning system will allow for sealing prior to decontamination, stopping leaks of decontaminant through the ventilation system. False ceilings, a fixture in many hospitals, will need to be made airtight to stop the spread of decontaminant between areas of the hospital. Certain items, for example doors, can be sealed with the use of waterproof tape to ensure no gaseous decontaminant escapes during the cycle. The decontamination process should always be monitored at regular intervals around the extremities of the room to determine if there is a leak during the cycle. A calibrated hand-held detector is a quick and easy way to measure any leak from a room [21]. The ideal generator will also constantly monitor the level of decontaminant in the room using an integral probe in the room. The generator’s safety feature will stop and abort the cycle if any major drop in the concentration of decontaminant is detected or the expected level is not reached. The toxicity of the gas itself and the necessity to seal the room means that the room needs to remain empty for an extended period of time during the fumigation process. The length of time the room has to remain empty will be determined from previous scientific studies and validation runs within similarly sized rooms. The validation processes are described in more detail in Section 14.4.

14.2.2 Microbial resistance The gaseous decontamination cycles are validated using biological indicators (BIs) consisting of resistant bacterial endospores. Previous studies have shown these spores might not be the most resistant organism for the process [28]. Hydrogen peroxide naturally breaks down into constituent parts of oxygen and water, and this breakdown is accelerated in the presence of the enzyme catalase [29]. Therefore, any organism which produces catalase can have an increased tolerance to the effects of hydrogen peroxide. Bacterial endospores show a high degree of resistance to hydrogen peroxide due to the presence of catalase in the spore’s coat layer [30]. Other organisms also produce catalase which has a protective effect, and studies have shown that MRSA, a common HAI and catalase producer, can exhibit a greater resistance than Geobacillus

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stearothermophilus, which is the biological indicator recommended for use with hydrogen peroxide [28]. A further study investigating the penetration of hydrogen peroxide into biofilms, formed from catalase positive and catalase negative Pseudomonas aeruginosa organisms, found that catalase protects the bacteria within the biofilm by limiting the penetration of hydrogen peroxide [31]. Organisms that do not produce catalase, such as VRE, show a rapid reduction in numbers when exposed to gaseous hydrogen peroxide in relation to catalase-producing bacteria [32]. Spores of Bacillus thuringiensis have demonstrated extreme resistance to gaseous chlorine dioxide in comparison to the indicator organism of choice, Bacillus atrophaeus [33, 34]. Organic material has also been found to increase the resistance of microorganisms to gaseous hydrogen peroxide treatment [35, 36]. This indicates that spills of bodily fluids, e.g., blood and feces, might protect the organisms within them during the gaseous decontamination process [36]. This protective effect could lead to possible infection of a patient or a worker within a room which has been declared decontaminated. Greater attention to details and protocols should be paid when performing the initial surface cleaning of rooms using liquid disinfectants to ensure that any bodily fluid spills have been removed. The removal of dried spills should decrease the problems associated with the gaseous technology’s difficulty in spill penetration. Different gaseous hydrogen peroxide systems have shown a variation in the rate of kill for bacteriophage dried in an organic soil [36]. The hydrogen peroxide vapor (HPV) system demonstrated a quicker initial kill than the vapor hydrogen peroxide (VHP) technology, but over the entire exposure period the VHP exhibited a greater overall reduction. The mode of action for how the two systems work might explain why there is this difference. The HPV technology is a wet system that injects hydrogen peroxide vapor into the chamber at a concentration above the dew point, thus creating microcondensation on the surfaces. This condensation can rehydrate and allow penetration into the spill, giving an initial quicker kill. However the system will only inject HPV once into the chamber and the hydrogen peroxide will break down and the concentration decreased, as opposed to the “dry” VHP system that dehumidifies the chamber prior to hydrogen peroxide injection, which will then be below the dew point and no condensation will form on the surfaces. This will limit the penetration into the spill and the kill of organisms underneath the outer layer, but VHP technology produces the greater kill by means of continually injecting hydrogen peroxide into the chamber during the cycle and the spill is gradually penetrated but at a slower pace than the HPV [36, 37]. These problems of resistant organisms, protective media, and initial loading concentration highlight the need to choose a suitable biological indicator when validating the cycle. The indicator used must also accurately reflect the level of contamination which is seen in the room, allowing the operator of the generator a high degree of confidence that all the organisms present will be destroyed during the cycle.

14.2.3 Environmental conditions The environmental conditions within the chamber will have an impact on the success of the decontamination cycle. Humidity levels within the chamber can affect the level of contact of decontaminant on the surfaces. A technology that relies on condensation

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will produce more condensation on the internal surfaces when the initial humidity is high. Maintaining the conditions of a room between runs can be difficult, in terms of both the environment and the physical aspects. First, for technologies that do not regulate the conditions before injection of the disinfectant, the change of humidity and temperature (seen in older buildings that have no heating, ventilation, and air conditioning (HVAC) regulation and are more susceptible to change) can affect the level of decontaminant contacting the surfaces, which in turn might produce different results from those in which the cycle is validated and may lead to variations in results between runs [32]. A low humidity and high temperature will cause more of the vapor injected into the room to remain as a vapor and less to condense onto surfaces. Increasing the level of hydrogen peroxide injected into a chamber and increasing the humidity will increase the speed of decontamination of the BI. However, a similar kill was observed using a lower hydrogen peroxide concentration and an increased humidity in the same chamber [38]. These conditions will affect the systems that rely on condensation as the primary method for decontamination [39]. Second, location of a cold surface within the room, such as a window or outer wall, will cause more condensation, which will leave less decontaminant to condense onto other surfaces around the room. The decontamination cycle should therefore be modified in response to these factors.

14.2.4 Room penetration The advantage of using gaseous decontamination is that the vapor will be able to reach sites that are inaccessible to cleaners [40, 41]. With many generators, the gas will be exhausted from the generator at a velocity great enough to create turbulence within the room assisting with the mixing of the gas in the room. Studies using an HPV generator with a high exhaust velocity have an acceptable killing around the test room, while dry mist hydrogen peroxide (DMHP), which uses diffusion around the room, only showed efficacy near the generator [18]. Quick mixing and diffusion around the room will help to reduce the decontamination time as the peak concentration of decontaminant will be reached rapidly. Units that do not produce enough exhaust velocity might require one or more fans in a room to aid the mixing of the decontaminant. Fans will also be needed to redistribute the air as the size of the room increases because the effect of the exhaust velocity will decrease with an increase in room size, leading to inadequate gas distribution around the room. To ensure all the surfaces are contacted by the decontaminant all enclosed spaces should be opened to allow penetration of the decontaminant [35]. Enclosed spaces such as drawers and cupboards will not be penetrated by the gas if they are sealed and therefore the microbial contamination will remain. If the internal surfaces need to be decontaminated then the drawers and doors should be opened, or conversely if items inside should not be decontaminated then the drawers and doors should be closed and sealed using waterproof tape.

14.2.5 Surface coverage Each decontamination cycle will be developed dependent on the size and surface loading of the room. The effective parameters will be reused for each subsequent

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d­ econtamination cycle. Each time that cycle is used the room should be checked to ensure there is a similar surface area in the room. This is important to note because a change in surface area can affect the efficacy of the fumigation. Gaseous decontamination relies on a certain concentration of decontaminant to contact all of the surfaces for a predetermined length of time in order to kill the microorganisms. The volume of decontaminant required to adequately cover all the surfaces in an empty room will not be adequate if objects are introduced into the room increasing the surface area and decreasing the amount decontaminant covering the surfaces. The amount of objects (bed, cupboard, medical equipment, etc.) within the room should be regulated between decontamination cycles to ensure there is consistency and reproducibility.

14.2.6 Gaseous decontaminant removal The removal of gaseous decontaminant from the laboratory can be as straightforward as switching the HVAC system on and venting to the external atmosphere. The laboratory ventilation should be set up and designed with this in mind, whereas a hospital room or ward will not have been designed with the air handling ability to do this. To facilitate the removal of the gaseous decontaminant for hospital rooms the generators are either fitted with a catalyst that will break the decontaminant down to harmless by-products [42] or the decontaminant is passed through an “air scrubber” designed to facilitate removal [19]. Both of these methods of decontaminant removal will require additional time in comparison to direct removal via an HVAC system. An independent study found that a range of decontamination technologies failed to reduce the levels of airborne decontaminant to below the acceptable WEL after the generator’s own aeration period [21], potentially allowing staff to re-enter a room before it is safe to do so. Absorbent materials within the room will have an effect on the peak level of decontaminant reached, the length of aeration needed, and the level of off-gassing postaeration. Materials in the room, e.g., curtains and cardboard, will reduce the concentration of decontaminant by absorbing the vapor and reducing the amount of decontaminant contacting other surfaces, in the worst case leading to a failed decontamination. These absorbent materials will also slowly leach the decontaminant back into the room in small pockets over time after aeration. This will probably not affect the length of aeration, but gas pockets that contain high concentrations of the decontaminant above the WEL may cause harm to individuals entering the room. This has been witnessed previously during room decontaminations using HPV, where absorbent material within the room caused increased levels of hydrogen peroxide vapor release after the aeration period has been completed (anecdotal evidence). This problem can be eliminated by removing any soft furnishings that can absorb the gaseous decontaminant, or materials can be sealed in airtight bags before the cycle is started, followed by close monitoring of decontaminant levels within the room after aeration using a handheld sensor [21].

14.2.7 Cycle duration The duration of the decontamination process can cause issues in the healthcare setting. When used in the laboratory, a fumigation cycle is generally run overnight to

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allow for adequate contact time. Within the majority of healthcare settings, bed space is at a premium and while conventional wet cleaning techniques might not be seen as effective as gaseous decontamination they can be performed more quickly, reducing the patient bed occupancy turnaround time. A typical HPV cycle will take 90–120 min and the room will need to be sealed for the entirety of this period [43], although when HPV was used within the healthcare setting the average cycle length for gaseous decontamination was 139 min (including equipment set-up time). This extended to 206 min when taking into account the period of time from the room being vacated by the patient to the end of the gaseous decontamination cycle and extended further to 270 min from when the room was vacated by the patient to the end of secondary cleaning after gaseous decontamination [43]. This was greater than the 67 min taken for the comparative bleach cleaning of the room (cumulative time from room vacation to the end of the cleaning process) [43]. Access to the room after gaseous decontamination is dependent on the removal of the gas to levels below that of the WEL. A study investigating a range of gaseous decontamination technologies, in a controlled air chamber with an internal volume of 35 m3, found that at the end of the majority of the different technologies’ cycles an extension to the aeration period was needed because the level of decontaminant in the chamber was still above the WEL [21]. Otter et  al. [43] found that during the trial, HPV decontamination of rooms was not undertaken because of time constraints as the hospital’s occupancy rate increased. This indicates that due to time constraints inclusion of gaseous decontamination as part of a regular cleaning regime might be dependent on the occupation rate of the hospital. However, an alternative strategy would be to only target rooms that have been occupied by patients known to have been colonized with an organism that could cause an HAI, i.e., carrying out a risk assessment and using a more targeted approach.

14.2.8 Material compatibility The use of powerful oxidizing agents for decontamination of rooms can cause progressive damage to surfaces and equipment exposed to the processes [21]. High concentrations of liquid hydrogen peroxide have been shown to corrode certain metals [40]. There is very little evidence published highlighting any material compatibility issues for the gaseous technologies. For example, X-ray film is one material recommended to be removed from the room before decontamination with HPV, as this can be degraded [42]. If possible, any material that could potentially react or be damaged by the decontaminant should be removed from the room prior to decontamination. An example of chemicals cross-reacting, in the laboratory setting, is formaldehyde reacting with chlorine-based products to form the highly carcinogenic 2,4-bis chloromethyl ether by-product. There is advice from the manufacturer (Steris Technology) for the removal of any electro-chemical sensors from the room being decontaminated [37]. There are no documented problems with any medical equipment that has been left in the rooms being decontaminated with the Bioquell and Glosair technologies [42, 44–46].

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14.2.9 Surface recontamination Gaseous decontamination has the ability to rapidly reduce the contamination of the hospital environment [19, 43]. As might be expected for a process that does not leave antimicrobial residues on surfaces, there can be rapid recontamination as soon as a colonized patient is readmitted. Recontamination was witnessed in a UK hospital side room within 5 days of readmission of a patient carrying MRSA and Gram-negative rod (GNR) contaminants after HPV decontamination [47]. Surfaces were contaminated within 24 h following readmission of an MRSA colonized patient into a room decontaminated using HPV [48]. These results show that continual cleaning regimes, including traditional terminal disinfection and gaseous decontamination, will ensure that surface contamination is kept as low as possible at all times between occupants of the same room. But it has been debated as to whether such extensive and long cleaning regimes are needed when there is rapid recontamination of the room when a patient is readmitted [48]. Although there are no gaseous decontamination technologies that can answer all of these challenges completely [41], there are technologies that will perform better than others. Certain challenges will carry more weight when considering technologies to use in the hospital environment. The problems associated with turn-around times, efficacy, and material compatibility will rate highly and technologies that show good performances in these areas will be selected first. The gaseous hydrogen peroxide technologies that have exhibited good performance within the pharmaceutical and microbiological laboratory fields and over the last 10  years have been specifically developed for hospital use.

14.3 Validation methods to determine efficacy The demonstration of a decontamination process is very difficult to prove, requiring comprehensive postcycle analysis of all the surfaces within the area decontaminated using microbial analysis. This analysis would be very time-consuming, expensive, and potentially lead to recontamination of the area. To overcome this problem, BIs are used to accurately validate and demonstrate the effectiveness of the decontamination process. Some applications require constant validation of every decontamination process using BIs, for example in the pharmaceutical industry. This can be time intensive because the BIs must be processed, incubated, and results obtained prior to the decontamination process being signed off as effective. In most laboratory applications, however, both the initial validation of the decontamination and any decontamination before servicing are performed using BIs. The decontamination cycle is started and the real-time data generated are recorded (usually decontaminant vapor concentration, humidity, temperature, and exposure period); once these parameters have been determined to give the required reduction in the BI population the subsequent cycles do not need BIs as long as the parameters remain constant. Under constant test conditions the decontamination process can be used to determine the decimal reduction time (D-value). The D-value is the time taken to reduce a microbial population by 90%

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(1 log) at a given concentration of decontaminant. The D-value can be worked out for a given BI concentration and then used to determine the length of time needed for a cycle where the starting concentration of organisms present differs from that of the BI. BIs are produced using a liquid suspension of resistant organisms which is dried onto a representative substrate of the environment being decontaminated [49, 50]. Fig. 14.1 shows commercially available BIs using B. atrophaeus (left) and G. stearothermophilus (right). BIs are readily available from commercial manufacturers but an organism suspension can also be used to make BIs “in house,” if the user would like to change the validation parameters, e.g., using a lower concentration of spores on an indicator. The chosen organism used on the BI should have been proven to be highly resistant to the decontamination method and therefore will present a difficult challenge to kill. Bacterial endospores have a high resistance to many of the gaseous decontamination technologies [21, 30, 51]. Two of the most regularly used organisms for BIs are G. stearothermophilus and B. atrophaeus. Both of these organisms are spore-forming bacteria which exhibit a high level of resistance to gaseous decontamination techniques. G. stearothermophilus is a thermophile and grows at 60°C, which when processing will help reduce the number of potential contaminants that could give a false positive. This organism is the recommended BI for use with gaseous hydrogen peroxide [5]. B. atrophaeus is a mesophile which grows at 37°C and produces orange colonies on trypcase soy agar (TSA) allowing for easy identification. B. atrophaeus is regarded as the BI of choice for chlorine dioxide gas and formaldehyde vapor decontamination processes [22]. In certain situations other organisms might prove a more realistic challenge to the decontamination process and they should be considered for use as biological indicators. For instance, as discussed previously, MRSA has been shown to exhibit a high degree of resistance to HPV [28]. The chosen BI organisms are often presented as a washed suspension, where the spores or cells have been washed and resuspended

Fig. 14.1  Two different commercially prepared BIs, Bacillus atrophaeus (left) and Geobacillus stearothermophilus (right).

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in water or ethanol to remove any organic contamination, presenting the BIs as single spores/cells. This process can create an artificial challenge in comparison to how microorganisms are presented on surfaces where they will be potentially clumped together and be associated with organic material. The addition of organic material to a BI suspension will decrease the efficacy of the decontamination cycle, reducing penetration into the spill and also reacting with the decontaminant [36]. BIs can also be selected on the loading concentration on the coupon. Commercial BIs can be purchased in a range of concentrations from 104 to 106 colony forming units per indicator. The choice of indicator concentration will depend on the level of decontamination that needs to be demonstrated. A BI with a higher loading should be used to validate a decontamination cycle that will be used in an environment that is heavily contaminated; conversely low-loaded BI can be used for validation in a lesser contaminated environment. The most commonly used indicators often have a concentration of 106 organisms. Previous research has shown that the D-value of an organism presented on a BI is dependent on the loading concentration, where a higher initial loading of an organism will lead to a greater D-value compared with a lower initial organism loading with a smaller D-value [32, 36]. The substrate that the BI organisms are dried on to should ideally replicate the surfaces that will be decontaminated. Therefore if a substrate found in the room offers protection to an organism [1, 52] then the indicators should ideally be adjusted to reflect this and give an adequate reflection of the exposure time needed for decontamination. Sigwarth carried out an extensive study investigating resistance of G. stearothermophilus spores when placed onto a range of materials found in laboratories and highlighted that laboratories should be designed to incorporate the materials easiest to decontaminate and that certain materials, such as white paint—Aptek 2711, should be avoided as they can increase resistance to gaseous decontamination [52, 53]. The BIs will then be sealed within a porous material pouch which will allow the entry of the gaseous decontaminant but not any other organisms or the release of the BI organism. An effective packaging material used by commercial suppliers is Tyvek. The BIs should be positioned around the room in a variety of places to accurately represent the areas of contamination that would be encountered; these can include under beds and on top of shelving. BIs will represent a challenge to the cleaning and decontamination regime where they can be placed in areas which are not readily accessible for normal cleaning and where only a gaseous decontaminant might reach. The BI can be assayed either qualitatively or quantitatively. Qualitative processing requires no formal training to have been undertaken by the worker, is rapid, and will limit the possibility of contamination. Using this processing method the BI should be taken from the room where it has been exposed and transferred to a biological safety cabinet. The Tyvek pouch can then be opened above a universal tube containing the appropriate growth medium and the coupon should drop into the medium. No contact should be made directly with the coupon as this might lead to contamination and a false positive result. The universal tube should then be incubated at the appropriate temperature and for the recommended time. Positive and negative samples should also be included for quality control. If growth occurs from a coupon then the medium would become cloudy and can be compared with that of the positive control. This

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method can be used to easily determine whether a decontamination procedure has been successful or not and will often be used in the hospital environment to validate the process. A quantitative assay will determine the exact number of organisms that are present on the BI. This method requires the BI to be placed in a buffer solution which is then rapidly mixed to remove the organisms from the coupon. The buffer solution can then be serially diluted and pipetted onto agar plates and incubated under the correct conditions. If organisms are present then they will form colonies on the agar plate which can be enumerated. This method requires training and can lead to potential contamination as there are numerous steps. While this method provides a high degree of knowledge about the number of organisms present in a sample it is generally only used in the development of a cycle where coupons can be taken at different times to determine the kinetics of the decontamination process. Indicators are not just restricted to a biological form, as chemical indicators are readily available. These indicators have a chemical impregnated on their surface which will react with the decontaminant and change color to allow for visualization that exposure to the indicator has occurred. The best use of chemical indicators during a decontamination cycle is to position them at specific points around the room and they will provide data on where the decontaminant has reached. These data can then be used in conjunction with data from the BIs to determine if any failure of the decontamination cycle is due to inadequate mixing or levels of the gas. For the decontamination generator to perform correctly for each cycle, it is necessary for the components to be working appropriately and regularly calibrated to ensure they are performing consistently as intended. An example of a component requiring calibration is the decontaminant sensor probe; in some generators these will intrinsically feed back to the generator on the level of decontaminant in the room. If this was to malfunction or to go out of calibration then the cycle might not be effective and could lead to contamination remaining after decontamination. A regular and rigorous maintenance and calibration schedule should be followed to ensure the generator ­functions correctly.

14.4 Practical use of gaseous decontamination in hospitals Current gaseous decontamination technologies that are or have been used in the hospital setting all employ the use of gaseous hydrogen peroxide to decontaminate the surfaces in a room. Hydrogen peroxide has a long history of use as a liquid decontaminant [29]; the compound is highly oxidative and reacts readily with organic material [29]. More recently it has been employed as a gaseous decontamination technology for laboratories, clean room facilities, the space industry and now, increasingly, hospitals. The manufacturers of these technologies are Bioquell, Glosair (formerly Sterinis) Advanced Sterilization Products, and Steris. This section will review the published literature accompanying each of these technologies and assess how developed and practical they are for hospital use.

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14.4.1 Bioquell This technology uses HPV within a closed-loop system to decontaminate the chamber or room it is connected to or placed within (Fig. 14.2). Prior to cycle initiation the room dimensions are measured, to calculate the volume and this is entered into the generator’s control unit so the unit can calculate how much hydrogen peroxide to inject. The generator pumps liquid hydrogen peroxide onto a vaporization plate and injects the HPV into the chamber above the dew point of the surrounding air [39]. This process will allow for a microcondensation layer (<50 μm thickness) of liquid hydrogen peroxide to form on the surfaces; there must be a close regulation of the amount of vapor injected into the chamber to stop visible condensation from forming. After injection the system will remain in the dwell phase of the cycle for a predetermined period where the microcondensation contacts the surfaces and destroys the microorganisms. Currently the manufacturer recommends cycles that will produce an HPV concentration of approximately 10 g/m3 [18]. The HPV system is perhaps the most tested and documented technology to be used in the hospital setting. HPV has been used for more than 10  years in the pharmaceutical and scientific fields, and for over 5 years in the hospital decontamination field. The HPV technology has demonstrated efficacy against a wide range of laboratory organisms [54] and more specific HAI organisms [41, 47, 55]. A large reduction in samples testing positive for MRSA was seen when an HPV unit was used to decontaminate a surgical ward; the

Fig. 14.2  A Bioquell HPV RBDS generator and aeration unit.

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p­ ositive sample numbers were reduced from 27.6% to 3.4% (from 29 sample sites; [56]). Laboratory testing of the HPV system against HAI agents suspended in 0.3% bovine serum albumin found a greater than 6-log reduction in organisms when exposed for 90 min [32]. This study did not publish the actual environmental conditions achieved in the chamber during the runs but commented “HPV concentration and relative humidity peaked at levels consistent with the onset of microcondensation on surfaces” [32]. Part of the study by Otter and French investigated the variances seen with different initial loading of organisms onto the indicators, the findings of which are similar to those in Pottage et al.’s study where a high initial loading led to an increase in the time needed for effective decontamination when compared to a lower initial loading [32, 36]. A comparison of traditional terminal cleaning and the use of HPV to reduce MRSA found the latter much better in the reduction of MRSA [19]. Swabs were taken prior to and after traditional cleaning procedures, and a reduction from 89.5% to 66.1% positive swabs was seen using the traditional cleaning methods following NHS standards. In comparison, swabs taken of similar areas before and after HPV decontamination showed over a 70% reduction in detectable MRSA [19]. Although a large reduction in MRSA was seen using HPV in this trial the average cycle time was 5 h [19] in comparison to a typical HPV cycle of 90–120 min [43]. HPV has also been demonstrated as effective against Serratia marcescens [45]. The HPV technology was used in a hospital neonatal intensive care unit to eradicate the environmental S. marcescens contamination. The decontamination of the 150 m3 rooms was undertaken overnight after standard cleaning using liquid detergent sterilizer, with all of the equipment left in the rooms. After the combined decontamination process no organisms were cultured, with the exception of a coagulase-negative Staphylococcus. The impact of HPV on reducing C. difficile in an American hospital has been assessed by Boyce et al. [55]. The normal cleaning regime was used prior to gaseous decontamination; this method included cleaning visible dirt with a detergent-based liquid cleaner, and where the rooms were occupied with patients exhibiting C. difficile-­ associated disease (CDAD) they were cleaned every day with a 1000 ppm sodium hypochlorite solution. After use of HPV there was no C. difficile detectable on any of the previously contaminated surfaces and a 44% and 53% reduction in CDAD was witnessed on five intensive wards and across the whole hospital respectively (P = 0.047). The incidence of C. difficile infection increased during this study when rooms were only decontaminated with standard bleach cleaning regimes [43]. HPV decontamination has also been successfully integrated into the decontamination regime for a critical care unit that had handled a patient who was infected with Lassa fever [46]. There are drawbacks in using HPV decontamination. Equipment in the room being decontaminated that has a narrow lumen will need to be decontaminated using an alternative method [25, 42, 57]. These medical devices should be decontaminated using washer disinfectors or a vacuum-based gaseous decontamination method because under thermolabile conditions the HPV will not penetrate into the lumen. However, gaseous decontamination technologies that are able to penetrate narrow lumens have now been developed and being installed into hospitals to be used on endoscopes of over 1 m in length [58]. While effective at reducing microbial contamination, as discussed previously, the readmission of contaminated patients into the room will lead to rapid recontamination of the surfaces [48].

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14.4.2 Glosair The Glosair system is an alternative decontamination technology which produces a vapor of DMHP from a liquid solution of 5% hydrogen peroxide [35, 59]. The hydrogen peroxide solution also contains trace amounts of silver cations and phosphoric acid, both at concentrations of <50 ppm [35, 59]. The generator is positioned within the room and produces small aerosolized (aHP) particles (8sit μm) which diffuse through the room. The cycles generally produce a lower concentration of hydrogen peroxide within the room than the Bioquell and Steris systems. Peaks of 17.4 and 60 ppm of gaseous hydrogen peroxide have been detected in the rooms during Glosair use [40]. The technology has been trialed within the hospital environment where it has been tested against a range of HAI organisms. A trial within a Turkish hospital showed that DMHP was effective at killing MRSA and Acinetobacter baumannii when presented on stainless steel disks positioned around a 53 m3 isolation room [35]. The DMHP was less effective when the organisms were presented in 5% sterile serum to simulate organic load associated with bodily fluids, and the system did not penetrate into semiclosed spaces as well as open spaces [35]. Bartels et  al. [44] also established that DMHP was effective at killing epidemic MRSA strains presented artificially on surfaces in a variety of hospital settings. Three elderly care wards were treated using DMHP to reduce the environmental contamination from C. difficile. Initially in 10 high-risk care rooms, 24% of the samples taken tested positive for C. difficile. These rooms were then exposed to one treatment from the Sterinis (now Glosair) system and then resampled. Following decontamination, only 3% of the samples tested positive for C. difficile and the average colony forming unit per sample was decreased from 6.8 to 0.4 per 10 samples [59]. This study has been followed by a study from Barbut et al. [20] comparing the efficacy of DMHP to a 0.5% sodium hypochlorite solution. The DMHP showed a 91% reduction in positive samples for C. difficile compared to a reduction in positive samples of 50% following sodium hypochlorite treatment. A selection of DMHP cycles were used to decontaminate hospital rooms, garages, and ambulances in a study completed by Andersen et al. [40]. In this study the use of multiple cycles was investigated to kill B. atrophaeus spores and the results showed that using three increasing cycles killed all of the indicators in the operating department, but single and double cycles failed to kill any of the indicators. A similar pattern was found with the attempted decontamination of ambulances within garages. After exposure to three cycles, all the indicators were deactivated, but no deactivation was witnessed with one or two cycles. In laboratory studies, DMHP was effective for the decontamination of Mycobacterium tuberculosis when impregnated into cotton tissues [60]. This presentation method was thought to allow penetration of the DMHP on all sides of the tissue which allowed for decontamination of the M. tuberculosis. A conflicting study by Andersen et al. [61] presented M. tuberculosis dried onto plastic dishes. After exposure to three DMHP cycles 70% of the samples remained positive; the number of positive samples were further reduced to 50% after six cycles. These results reinforce that differences in efficacy are seen when organisms are presented on different substrates to the same decontamination process. A direct comparison between the HPV and DMHP technologies was undertaken using both commercially available indicators (G. stearothermophilus) and in-house

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indicators (MRSA, C. difficile, and A. baumannii) [18]. Indicators were positioned around a large hospital room with an en-suite bathroom; the commercial indicators were loaded at both 104 and 106 spores per coupon, with the in-house indicators prepared from water, 3% and 10% BSA and air dried. Four replicates of each cycle were used for commercial indicators and three replicates were used for in-house coupons. All the indicators were enumerated to establish the exact microbial reduction after decontamination. The results from the experiments showed that after HPV exposure only 4.5% and 9.1% of G. stearothermophilus coupons were positive (104 and 106 spore concentration, respectively) in comparison to 63.6% and 93.2% positive for the DMHP technology. Similar results for the in-house prepared indicators were seen for both technologies. The HPV technology performed well against all three organisms with only a low number of positive samples recovered, although soiling reduced efficacy. The DMHP performed worse, specifically against the catalase producing MRSA and A. baumannii, with a high number of positive samples returned [18]. This comparison highlights the need for evaluation and validation of the technologies to be used against such strains. In this study, even the better performing HPV technology did not effectively kill all of the indicators and further development of the cycle would be needed before it should be used.

14.4.3 Steris Steris’s VHP is the gaseous decontamination technology that has been investigated least in terms of published scientific literature when applied in hospitals (Fig. 14.3). The VHP technology has been used to eliminate environmental contamination of

Fig. 14.3  A Steris VHP 100ARD decontamination unit and dehumidifying pod.

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A. baumannii in a long-term acute care hospital. Samples taken immediately, 1 day and 1 week, after decontamination were negative for A. baumannii, but recontamination occurred immediately when a colonized patient was reintroduced to the room [62]. VHP was used to control multidrug-resistant A. baumannii (MRAB) outbreaks on two separate occasions at a large teaching hospital in Poland. After persistence of MRAB in the intensive care units of the hospital, two cycles of VHP (250 ppm for 90 min then 400 ppm for 30 min) were used within the rooms [63]. After the first treatment there were no new cases of MRAB for 7 months; after the second treatment there were no new cases before the end of the study (13 months).

14.5 Conclusion and future trends There are only a limited number of companies that have technologies for gaseous decontamination in hospitals. The developed technologies are able to address and overcome some of the obstacles described previously such as surface coverage, material compatibility, and cycle times. Perhaps the greatest obstacle the manufacturers have to address is the cost of the technology. There is a high cost for the initial outlay of the technology, which will be accompanied by costs of consumables [21], staff training/ support staff, maintenance, and servicing costs for the technology. The Bioquell Q-10 bio-decontamination system which is used for non-good manufacturing practice (GMP) environments has a basic cost of ~£22,500 (exclusive of training at a cost of £1600), the price of the Q-10 suite (including generator, aeration unit, two vent sealers, and training) rises to above £26,000. These prices exclude the cost of consumables needed for the generator’s operation. The price for the Glosair 400 unit (used in UK hospitals) and training is £15,000. The ongoing cost of annual maintenance equates to £1400. The fluid consumable cost for the Glosair 400 unit is approximately £1510 per year, which provides enough to decontaminate 67 three-bed bays (~150 m3). The final costs for the generator and associated ongoing costs over 5 years will be £28,150. The prices have been quoted in 2012. These high costs have been addressed by the companies with the provision of an emergency outbreak service or scheduled decontamination, for example by Bioquell that will remove the necessity of the hospital trust purchasing the equipment. Ideally the technologies that are already used in hospitals will continue to be developed in several areas. The primary area will be engineering. The generators should be designed to be as compact as possible for easy movement and storage, and the reliability issues that have been raised in previous studies should be addressed [21]. Further engineering options should include making the operation of the technologies easier and reducing the cycle times, which in turn will decrease the length of time the rooms will be unoccupied and will increase turnaround times. Development of the technologies will increase the efficiency of the technology leading to reduced costs and cycle times. Hospital-based studies being undertaken and published will increase the knowledge foundation for the use of these technologies. These studies may highlight areas which can be improved by the existing technologies or can be replaced with newer,

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less proven technologies. Newer technologies are being investigated for their use in the healthcare environment. Gaseous chlorine dioxide has been shown to effectively kill bed bugs and inactivate their eggs, although extensive exposure periods were required, but the cycles failed to inactivate all of the B. atrophaeus indicators used [64]. Gaseous ozone was used to successfully eradicate MRSA from a pediatric nurse’s home, but the nurse and family needed to be relocated while the process was undertaken [65]. In conclusion, the use of gaseous decontamination can help reduce the surface contamination in hospital rooms from HAI organisms but limitations of the technologies previously described in this chapter preclude its use as a stand-alone technique for hospital decontamination. Gaseous decontamination should be used in conjunction with conventional terminal cleaning techniques to form an effective process for reducing and controlling microbial contamination in hospitals.

14.6 Sources of further information and advice Further information on the subject of gaseous decontamination of hospitals and more specific data on the decontamination technologies can be found on the Internet or by directly contacting the companies involved. A list of useful company websites is given below: Bioquell—www.bioquell.com Glosair—www.aspjj.com/us/products/glosair Steris—www.steris.com

References [1] Diab-Elschahawi M, Blacky A, Bachhofner N, Koller W. Challenging the Sterrad 100NX sterilizer with different carrier materials and wrappings under experimental ‘clean’ and ‘dirty’ conditions. Am J Infect Control 2010;38:806–10. [2] Canter D. Addressing residual risk issues at anthrax cleanups: how clean is safe? J Toxicol Environ Health A 2005;68:1017–32. [3] Cheney  JE, Collins  CH. Formaldehyde disinfection in laboratories: limitations and ­hazards. Br J Biochem Sci 1995;52:195–201. [4] Kahnert A, Seiler P, Stein M, Axe B, McDonnell G, Kaufmann S. Decontamination with vaporized hydrogen peroxide is effective against Mycobacterium tuberculosis. Lett Appl Microbiol 2005;40:448–52. [5] Krause  J, McDonnell  G, Riedesel  H. Biodecontamination of animal rooms and heat-­ sensitive equipment with vaporized hydrogen peroxide. Contemp Top Lab Anim Sci 2001;40:18–21. [6] Boyce JM. New approaches to decontamination of rooms after patients are discharged. Infect Control Hosp Epidemiol 2009;30:515–7. [7] Huang  SS, Datta  R, Platt  R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 2006;166:1945–51.

Use of gaseous decontamination technologies

319

[8] 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. [9] Boyce  JM, Potter-Bynoe  G, Chenevert  C, King  T. Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol 1997;18:622–7. [10] Casewell M, Phillips I. Hands as route of transmission for Klebsiella species. Br Med J 1977;2:1315–7. [11] Sanderson PJ, Weissler S. Recovery of coliforms from the hands of nurses and patients: activities leading to contamination. J Hosp Infect 1992;21:85–93. [12] 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. [13] Weber  DJ, Rutala  WA. The emerging nosocomial pathogens Cryptosporidium, Escherichia coli O157:H7, Helicobacter pylori, and hepatitis C: epidemiology, environmental survival, efficacy of disinfection, and control measures. Infect Control Hosp Epidemiol 2001;22:306–15. [14] Boyce  JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 2007;65(Suppl. 2):50–4. [15] Oie S, Kamiya A. Survival of methicillin-resistant Staphylococcus aureus (MRSA) on naturally contaminated dry mops. J Hosp Infect 1996;34:145–9. [16] Duckworth GJ, Jordens JZ. Adherence and survival properties of an epidemic methicillin-­ resistant strain of Staphylococcus aureus compared with those of methicillin-sensitive strains. J Med Microbiol 1990;32:195–200. [17] Wendt  C, Wiesenthal  B, Dietz  E, Ruden  H. Survival of vancomycin-resistant and vancomycin-­susceptible enterococci on dry surfaces. J Clin Microbiol 1998;36:3734–6. [18] Fu TY, Gent P, Kumar V. Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems. J Hosp Infect 2012;80:199–205. [19] French  GL, Otter  JA, Shannon  KP, Adams  NM, 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. [20] Barbut F, Menuet D, Verachten M, Girou E. Comparison of the efficacy of a hydrogen peroxide dry-mist disinfection system and sodium hypochlorite solution for eradication of Clostridium difficile spores. Infect Control Hosp Epidemiol 2009;30:507–14. [21] Beswick  AJ, Farrant  J, Makison  C, Gawn  J, Frost  G, Crook  B, Pride  J. Comparison of multiple systems for laboratory whole room fumigation. J Appl Biosafety 2011;16:139–57. [22] Luftman  HS, Regits  MA. Bacillus atrophaeus and Geobacillus stearothermophilus biological indicators for chlorine dioxide gas decontamination. J Appl Biosafety 2008;13:143–57. [23] Hubbard H, Poppendieck D, Corsi RL. Chlorine dioxide reactions with indoor materials during building disinfection: surface uptake. Environ Sci Technol 2009;43:1329–35. [24] Rutala WA, Weber DJ. Infection control: the role of disinfection and sterilization. J Hosp Infect 1999;43(Suppl):S43–55. [25] Okpara-Hofmann  J, Knoll  M, Durr  M, Schmitt  B, Borneff-Lipp  M. Comparison of low-temperature hydrogen peroxide gas plasma sterilization for endoscopes using various Sterrad models. J Hosp Infect 2005;59:280–5.

320

Decontamination in Hospitals and Healthcare

[26] Kanemitsu K, Imasaka T, Ishikawa S, Kunishima H, Harigae H, Ueno K, Takemura H, Hirayama  Y, Kaku  M. A comparative study of ethylene oxide gas, hydrogen peroxide gas plasma, and low-temperature steam formaldehyde sterilization. Infect Control Hosp Epidemiol 2005;26:486–9. [27] Health and Safety Executive. EH40/2005 workplace exposure limits; 2011. [28] Pottage T, Macken S, Walker JT, Bennett AM. Meticillin-resistant Staphylococcus aureus is more resistant to vaporized hydrogen peroxide than commercial Geobacillus stearothermophilus biological indicators. J Hosp Infect 2012;80:41–5. [29] Block SS. Disinfection, sterilization and preservation. Lippincott, Williams and Wilkins; 2001. [30] Checinska A, Burbank M, Paszczynski AJ. Protection of Bacillus pumilus spores by catalases. Appl Environ Microbiol 2012;28:6413–22. [31] Stewart PS, Roe F, Rayner J, Elkins JG, Lewandowski Z, Ochsner UA, Hassett DJ. Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2000;66:836–8. [32] Otter JA, French GL. Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor. J Clin Microbiol 2009;47:205–7. [33] Han Y, Applegate B, Linton RH, Nelson PE. Decontamination of Bacillus thuringiensis spores on selected surfaces by chlorine dioxide gas. J Environ Health 2003;66:16–21. [34] Pottage  T, Macken  S, Giri  K, Walker  J, Bennett  A. Low temperature decontamination for space applications—a comparison of hydrogen peroxide and chlorine dioxide. Appl Environ Microbiol 2012;78:4169–74. [35] Piskin N, Celebi G, Kulah C, Mengeloglu Z, Yumusak M. Activity of a dry mist-­generated hydrogen peroxide disinfection system against methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii. Am J Infect Control 2011;39:757–62. [36] Pottage  T, Richardson  C, Parks  S, Walker  JT, Bennett  AM. Evaluation of hydrogen peroxide gaseous disinfection systems to decontaminate viruses. J Hosp Infect 2010;74:55–61. [37] McDonnell G. Hydrogen peroxide fogging/fumigation. J Hosp Infect 2006;62:385–6. [38] Unger-Bimczok B, Kottke V, Hertel C, Rauschnabel J. The influence of humidity, hydrogen peroxide concentration, and condensation on the inactivation of Geobacillus stearothermophilus spores with hydrogen peroxide vapor. J Pharm Innov 2008;3:123–33. [39] Watling  D, Ryle  C, Parks  M, Christopher  M. Theoretical analysis of the condensation of hydrogen peroxide gas and water vapour as used in surface decontamination. PDA J Pharm Sci Technol 2002;56:291–9. [40] Andersen BM, Rasch M, Hochlin K, Jensen FH, Wismar P, Fredriksen JE. Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant. J Hosp Infect 2006;62:149–55. [41] Rogers  J, Sabourin  C, Choi  Y, Richter  W, Rudnicki  D, Riggs  K, Taylor  M, Chang  J. Decontamination assessment of Bacillus anthracis, Bacillus subtilis and Geothermophilus stearothermophilus spores on indoor surfaces using a hydrogen peroxide gas generator. J Appl Microbiol 2005;99:739–48. [42] Otter JA, French GL, Adams NM, Watling D, Parks MJ. Hydrogen peroxide vapour decontamination in an overcrowded tertiary care referral centre: some practical answers. J Hosp Infect 2006;62:384–5. [43] Otter JA, Puchowicz M, Ryan D, Salkeld JA, Cooper TA, Havill NL, Tuozzo K, Boyce JM. Feasibility of routinely using hydrogen peroxide vapor to decontaminate rooms in a busy United States hospital. Infect Control Hosp Epidemiol 2009;30:574–7.

Use of gaseous decontamination technologies

321

[44] Bartels  MD, Kristoffersen  K, Slotsbjerg  T, Rohde  SM, Lundgren  B, Westh  H. Environmental methicillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide. J Hosp Infect 2008;70:35–41. [45] Bates CJ, Pearse R. Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit. J Hosp Infect 2005;61:364–6. [46] Otter JA, Barnicoat M, Down J, Smyth D, Yezli S, Jeanes A. Hydrogen peroxide vapour decontamination of a critical care unit room used to treat a patient with Lassa fever. J Hosp Infect 2010;75:335–7. [47] Otter JA, Cummins M, Ahmad F, van Tonder C, Drabu YJ. Assessing the biological efficacy and rate of recontamination following hydrogen peroxide vapour decontamination. J Hosp Infect 2007;67:182–8. [48] Hardy  KJ, Gossain  S, Henderson  N, Drugan  C, Oppenheim  BA, Gao  F, Hawkey  PM. Rapid recontamination with MRSA of the environment of an intensive care unit after decontamination with hydrogen peroxide vapour. J Hosp Infect 2007;66:360–8. [49] Melly E, Cowan A, Setlow P. Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. J Appl Microbiol 2002;93:316–25. [50] Sutton JM, Dickinson J, Walker JT, Raven ND. Introduction of methods for the decontamination of CJD-contaminated material; where to set the standard? Clin Infect Dis 2006;43:757–64. [51] Riesenman P, Nicholson W. Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B and solar UV radiation. Appl Environ Microbiol 2000;66:620–6. [52] Chung S, Kern R, Koukol R, Barengoltz J, Cash H. Vapor hydrogen peroxide as alternative to dry heat microbial reduction. Adv Space Res 2008;42:1150–60. [53] Sigwarth V, Stark A. Effect of carrier materials on the resistance of spores of Bacillus stearothermophilus to gaseous hydrogen peroxide. PDA J Pharm Sci Technol 2003;57:3–11. [54] Hall L, Otter JA, Chewins J, Wengenack NL. Use of hydrogen peroxide vapor for deactivation of Mycobacterium tuberculosis in a biological safety cabinet and a room. J Clin Microbiol 2007;45:810–5. [55] Boyce JM, Havill NL, Otter JA, McDonald LC, Adams NM, Cooper T, Thompson A, Wiggs  L, Killgore  G, Tauman  A, Noble-Wang  J. Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting. Infect Control Hosp Epidemiol 2008;29:723–9. [56] Dryden M, Parnaby R, Dailly S, Lewis T, Davis-Blues K, Otter JA, Kearns AM. Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward. J Hosp Infect 2008;68:190–2. [57] Kyi MS, Holton J, Ridgway GL. Assessment of the efficacy of a low temperature hydrogen peroxide gas plasma sterilization system. J Hosp Infect 1995;31:275–84. [58] Young T. Transforming scope decontamination. Med Dev Decontam 2011;16:6–10. [59] Shapey  S, Machin  K, Levi  K, Boswell  TC. Activity of a dry mist hydrogen peroxide system against environmental Clostridium difficile contamination in elderly care wards. J Hosp Infect 2008;70:136–41. [60] Grare M, Dailloux M, Simon L, Dimajo P, Laurain C. Efficacy of dry mist of hydrogen peroxide (DMHP) against Mycobacterium tuberculosis and use of DMHP for routine decontamination of biosafety level 3 laboratories. J Clin Microbiol 2008;46:2955–8. [61] Andersen BM, Syversen G, Thoresen H, Rasch M, Hochlin K, Seljordslia B, Snevold I, Berg E. Failure of dry mist of hydrogen peroxide 5% to kill Mycobacterium tuberculosis. J Hosp Infect 2010;76:80–3.

322

Decontamination in Hospitals and Healthcare

[62] Ray  A, Perez  F, Beltramini  AM, Jakubowycz  M, Dimick  P, Jacobs  MR, Roman  K, Bonomo RA, Salata RA. Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital. Infect Control Hosp Epidemiol 2010;31:1236–41. [63] Chmielarczyk A, Higgins PG, Wojkowska-Mach J, Synowiec E, Zander E, Romaniszyn D, Gosiewski T, Seifert H, Heczko P, Bulanda M. Control of an outbreak of Acinetobacter baumannii infections using vaporized hydrogen peroxide. J Hosp Infect 2012;81:239–45. [64] Gibbs SG, Lowe JJ, Smith PW, Hewlett AL. Gaseous chlorine dioxide as an alternative for bedbug control. Infect Control Hosp Epidemiol 2012;33:495–9. [65] De Boer HE, van Elzelingen-Dekker CM, van Rheenen-Verberg CM, Spanjaard L. Use of gaseous ozone for eradication of methicillin-resistant Staphylococcus aureus from the home environment of a colonized hospital employee. Infect Control Hosp Epidemiol 2006;27:1120–2.