Airborne Hydrogen Peroxide€¦ · decontamination: HP vapour devices that vaporise a solution of...

Version: 1.1

Date: December 2016

Review: December 2019

Literature Review and Practice Recommendations: Existing and emerging technologies used for

decontamination of the healthcare environment

Airborne Hydrogen Peroxide

Literature Review and Practice Recommendations: Existing and emerging technologies used for decontamination of the healthcare environment: Airborne Hydrogen Peroxide

Version 1.1. December 2016 of 28

DOCUMENT CONTROL SHEET Key Information:

Title: Existing and emerging technologies used for decontamination of the healthcare environment: Airborne Hydrogen Peroxide

Date Published/Issued: December 2016 Date Effective From: December 2016 Version/Issue Number: 1.1 Document Type: Literature Review Document status: Final Author: Name: D. Scott, F. Hansraj

Role: Healthcare Scientists (Health Protection) Division: HPS

Owner: Infection Control Approver: Annette Rankin Approved by and Date: December 2016 Contact Name: Infection Control Team

Tel: 0141 300 1175 Email: [email protected]

Version History:

This literature review will be updated in real time if any significant changes are found in the professional

literature or from national guidance/policy.

Version Date Summary of changes Changes marked

1.1 December 2016 Addition of categories for recommendations. No changes made to the content of the literature review.

1.0 May 2015 Final for publication

mailto:[email protected]�



Contents Topic .................................................................................................................................... 4

Background .......................................................................................................................... 4

Aim....................................................................................................................................... 5

Objectives ............................................................................................................................ 5

Research Questions ............................................................................................................ 5

Methodology ........................................................................................................................ 6

Search Strategy ........................................................................................................................... 6

Exclusion Criteria ........................................................................................................................ 6

Screening .................................................................................................................................... 7

Critical Appraisal ......................................................................................................................... 7

Results ................................................................................................................................. 7

Research Questions .................................................................................................................... 8

Discussion ......................................................................................................................... 19

Recommendations for Clinical Practice ..................................................................................... 19

Implications for Research .......................................................................................................... 21

Conclusion ......................................................................................................................... 22

Appendix 1: MEDLINE Search (2014) ............................................................................... 23

Appendix 2: MEDLINE Search (2016) ............................................................................... 24

References ........................................................................................................................ 25



Topic

The use of airborne hydrogen peroxide (HP) for decontamination of the healthcare environment.

Background

Current microbiological and epidemiological evidence indicates that contaminated surfaces in

hospital settings can contribute to the transmission of nosocomial pathogens.1 In particular, there

appears to be a risk of pathogen acquisition from prior room occupants for methicillin-resistant

Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), Clostridium difficile and

Acinetobacter baumannii.2 Accordingly, existing research implies that improved surface cleaning

and disinfection can reduce healthcare-associated infections.3

Manual processes for terminal cleaning are frequently sub-optimal, suggesting that automated

decontamination processes might offer an opportunity to improve cleaning efficacy and

consistency.4 There are two major airborne HP systems currently in use for environmental

decontamination: HP vapour devices that vaporise a solution of 30 – 35 % HP, and aerosolised HP

systems that dispense a dry aerosol of 3 – 7 % HP with or without the addition of silver ions.5

Automated mobile airborne HP devices can be placed in patient rooms following discharge as an

adjunct to terminal cleaning. However, airborne HP systems are suggested as a supplement to,

rather than a replacement for, standard discharge cleaning measures due to the requirement of

physical removal of dirt from surfaces.6

The advantages of airborne HP devices include greater laboratory sporicidal activity over UV light

devices, bactericidal effectiveness throughout an enclosed space including surfaces not in direct

line-of-sight (unlike UV light systems), and the lack of need to arrange furniture and equipment pre-

exposure to allow maximal disinfection.7 However, airborne HP systems require a longer

decontamination cycle than UV light systems, necessitating that patients rooms are unavailable to

admission for a longer time period.6 Their main disadvantages also include the requirement to

disable HVAC (heating, ventilation and air conditioning) systems, substantial set-up costs for

equipment, the necessity to remove staff and patients from the room before disinfection, and the

need to physically remove dirt and debris before use.7

It has been reported that airborne HP systems are capable of substantially reducing the number of

environmental C. difficile spores, indicating their applicability for the terminal cleaning of rooms

following the discharge of patients under contact precautions.8 The NHSScotland National Infection

Prevention and Control Manual9 currently recommends the use of a disinfectant solution at a

dilution of 1,000 parts per million (ppm) available chlorine for routine and terminal room cleaning

under transmission-based precautions. This review intends to assess the evidence base on the



appropriateness of using airborne HP decontamination systems for both routine cleaning and

terminal (or discharge) cleaning in the healthcare environment.

Aim

To review the evidence base for using airborne hydrogen peroxide (HP) for decontamination of the

healthcare environment.

Objectives

• To provide a generic description of airborne HP decontamination systems, including the

proposed or actual mechanism of action and the procedure for use.

• To assess the scientific evidence for effectiveness of airborne HP decontamination

systems.

• To explore practical and safety considerations related to the use of airborne HP

decontamination systems.

• To explore the costs associated with airborne HP decontamination systems.

• To produce a concise evidence summary for airborne HP to assist the Equipment and

Environmental Decontamination Steering Expert Advisory Group in making practical

recommendations on the use of airborne HP decontamination systems for NHS Scotland.

Research Questions

The following research questions will be addressed:

1. Are airborne HP decontamination systems currently in use in UK healthcare settings?

2. What is the actual or proposed mechanism of action of airborne HP decontamination

systems?

3. What is the procedure for using airborne HP decontamination systems?

4. What is the scientific evidence for effectiveness of airborne HP for decontamination of the

healthcare environment?

5. Are there any safety considerations associated with using airborne HP decontamination

systems in the healthcare setting?

6. Are there any practical or logistical considerations associated with using airborne HP

decontamination systems in the healthcare setting?

7. What costs are associated with using airborne HP decontamination systems in the

healthcare setting?



8. Have airborne HP decontamination systems been assessed by the Rapid Review Panel?

Methodology

Search Strategy

The following databases and websites were searched to identify relevant academic and grey

literature:

• MEDLINE

• CINAHL

• EMBASE

• NHS Evidence (http://www.evidence.nhs.uk/)

• Health Technology Assessment (HTA) database (http://www.crd.york.ac.uk/CRDWeb/)

• Database of Abstracts of Reviews of Effects (DARE) (http://www.crd.york.ac.uk/CRDWeb/)

• National Patient Safety Agency (NPSA) (http://www.npsa.nhs.uk/)

• National Institute for Health and Care Excellence (NICE) (http://www.nice.org.uk/)

• Medicines & Healthcare products Regulatory Agency (MHRA) (http://www.mhra.gov.uk/)

• Rapid Review Panel (RRP): product evaluation statements

(http://www.gov.uk/government/groups/rapid-review-panel/)

Search terms were developed and adapted to suit each database/website. Initial literature

searches were run between 24/06/2014 and 01/07/2014. For the update, the literature search was

performed on 08/08/2016. Different search strategies were applied in each year. See Appendix 1

for an example of the search run in the MEDLINE database in 2014 and Appendix 2 for an

example of the updated search conducted in 2016.

Exclusion Criteria

Academic and grey literature was excluded from the review on the basis of the following exclusion

criteria:

• Article was released before 2004

• Article was not published in the English language

• Article does not concern airborne hydrogen peroxide (HP) decontamination systems in the

healthcare environment (off-topic)

• Article is an opinion piece, a non-systematic review or a conference abstract

• Article does not present evidence compatible with the McDonald-Arduino evidentiary

hierarchy10

http://www.evidence.nhs.uk/�

http://www.crd.york.ac.uk/CRDWeb/�

http://www.crd.york.ac.uk/CRDWeb/�

http://www.npsa.nhs.uk/�

http://www.nice.org.uk/�

http://www.mhra.gov.uk/�

http://www.gov.uk/government/groups/rapid-review-panel/�



• Article concerns a study that did not have an appropriate comparison in the form of

standard cleaning methods

Screening

There was a two-stage process for screening the items returned from the literature searches. In the

first stage, the title/abstract was screened against the exclusion criteria by the lead reviewer. Items

that were not excluded at the screening stage progressed to the second screening stage. In the

second stage of the screening process, the full text of remaining items was screened against the

exclusion criteria by the lead reviewer. Items that were not excluded at the second screening stage

were included in the review.

Critical Appraisal

Critical appraisal of the studies included in this review and considered judgement of the evidence

was carried out by the lead reviewer using the Scottish Intercollegiate Guidelines Network (SIGN)

methodology.11 The McDonald-Arduino evidentiary hierarchy was used as a framework for

assessing the evidence.10

Results

The search found 326 articles. After the first stage of screening this was reduced to 90 articles, and

after the second stage there were eight articles to critically appraise.12-19 The update search

retrieved a further 98 articles, of which 21 passed the first stage of screening, and three were

critically appraised.20-22 The 11 included studies used two different types of airborne HP

disinfection: 10 studies used HP vapour13-22 and two studies used aerosolised HP12;22 (one study

compared HP vapour with aerosolised HP22). Four of the 11 studies were conducted in the United

Kingdom (UK),13;16;18;19 three studies took place in the United States of America (USA),14;15;21 two

studies were situated in France,12;22 one study was conducted in the Netherlands,17 and another

study was set in Australia.20

All of the studies included a comparison with terminal cleaning methods. These included the use of

sodium hypochlorite solution at varying concentrations of available chlorine (e.g. 1,000 ppm and

2,000 ppm), quaternary ammonium compound disinfectants or neutral pH detergents. Many of the

studies were funded by the manufacturers of the airborne HP systems and, in a few instances, the

funding bodies were also involved in the design and execution of the projects. It is important to

bear this in mind when evaluating the findings.

Four of the 11 studies monitored the effect of airborne HP on the incidence of healthcare-

associated infections or patient acquisition of nosocomial pathogens.14;15;20;21 By contrast, seven of



the studies evaluated the impact of airborne HP on the reduction of environmental

bioburden.12;13;16-19;22

There were a range of airborne HP disinfection systems available that exhibited effectiveness

against various comparison groups. Of the four studies that demonstrated greater levels of

effectiveness than terminal room cleaning with hypochlorite solution, two studies used aerosolised

HP disinfection devices12;22 and three studies used HP vapour systems15;17;22 (one study compared

both aerosolised HP and HP vapour systems with hypochlorite solution22). Two other studies

observed that terminal cleaning with hypochlorite solution exhibited similar effectiveness to HP

vapour devices.16;18 Of the five studies that demonstrated greater levels of effectiveness than

terminal room cleaning with quaternary ammonium disinfectants or detergents, all studies used HP

vapour disinfection.13;14;19-21

Research Questions

Are airborne HP decontamination systems currently in use in UK healthcare settings?

There is no mention of airborne HP decontamination systems in the NHSScotland National

Cleaning Services Specification.23 The NHSScotland National Infection Prevention and Control

Manual9 recommends that, should airborne HP decontamination systems be considered for

adoption in NHSScotland, a formal assessment of the cost, benefit, potential hazards and user

safety should be undertaken. The National Patient Safety Agency (NPSA) Revised Healthcare

Cleaning Manual24 and the Association of Healthcare Cleaning Professionals (AHCP) Revised

Healthcare Cleaning Manual25 both feature sections on airborne HP decontamination systems

alongside other new technologies for environmental disinfection. They summarise that the use of

airborne HP systems for disinfection of patient rooms is increasing, although there is currently

insufficient evidence to confirm their cost-effectiveness for routine cleaning.

These findings suggest that airborne HP decontamination systems are not widely in use within UK

healthcare settings.



What is the actual or proposed mechanism of action of airborne HP decontamination systems?

HP is an oxidising agent, responsible for the production of free radicals that are capable of

damaging microbial DNA and cell constituents.26 There are a number of different methods of

airborne HP decontamination,5 two of the most commonly used being:

• Hydrogen peroxide vapour

• Aerosolised hydrogen peroxide

The HP vapour system manufactured by Bioquell® produces vapour from a 30 % HP solution.

These vapour particles are less than 1 micron in size, allowing the vapour to disperse effectively.

At the end of the process, the HP vapour is catalytically broken down into water and oxygen.27

The aerosolised HP system Sterinis® produces a dry mist by aerosolising a solution of 5 % HP,

consisting of < 50 ppm silver ions, < 50 ppm phosphoric acid, < 1 ppm gum arabic, and 95 % bi-

osmotic water. The aerosol is stabilised using silver ions and other chemicals to avoid aggregation

before the drops reach the target.12;28;29 The particles are electrically charged, ranging in diameter

from 8 to 12 microns, and are able to circulate freely in the air as a dry aerosol disinfectant with

access to all surfaces.12 This airborne HP system is alternately referred to as “dry mist” HP.12

Holmdahl et al.29 compared HP vapour and aerosolised HP systems and found that a key

difference was the peak HP concentration, which was twice as high in HP vapour systems than in

aerosolised HP systems, while the total HP concentration was also seen to be higher for HP

vapour.

What is the procedure for using airborne HP decontamination systems?

Airborne HP disinfection systems should only be used as a supplement to standard terminal

cleaning, as biological soiling of surfaces will reduce the effectiveness of decontamination.30 HP is

hazardous to human health, so it can only be used in areas which have been vacated by people

and, in some instances such as the use of HP vapour, properly sealed prior to the disinfection

process.31 This increases the time required for disinfection and the subsequent costs, since

airborne HP must only be applied in rooms that have been vacated. The time required for a cycle

of airborne HP disinfection is proportional to the size of the area to be disinfected.30

The HP vapour system produced by Bioquell® consists of four portable units: a generator unit to

produce HP vapour; an aeration unit to break down the HP vapour catalytically after the exposure

period; an instrumentation module which measures the concentration of HP, as well as the

temperature and relative humidity of the room; and a control computer situated outside the room.13

The generator unit is used to vaporise 30 % liquid HP at 130 oC and the vapour produced is

delivered via a dual axis vapour distribution system that ensures high kinetic energy and even



distribution throughout the room.13 After decontamination has been completed, aeration units

inside the room catalytically convert the HP vapour into water and oxygen.13;32 The time required to

complete the process depends upon the size of the room, the process typically taking 90 minutes

for a single room.31

The HP vapour system manufactured by Steris® produces an aqueous solution of HP while

controlling the temperature and humidity levels within the room.33 It operates as a dry system,

reducing the relative humidity inside the room so that condensation does not form on surfaces.34

The HP vapour is degraded to oxygen and water in the aeration process, leaving behind no

chemical residues behind.33

The aerosolised HP system Sterinis® consists of a robot that can be pre-programmed to dispense

the required concentration of HP needed for full disinfection.12 The time taken to disinfect a room

depends on the volume of the room. The system uses Sterusil®, a mixture of HP (5 %), silver ions

(< 50 ppm) and phosphoric acid (< 50 ppm).32;35 The device needs to be placed in the corner of the

room as instructed by the user manual. According to the manufacturers, the technology uses the

processes of ionisation and nucleation to allow the small electrically charged droplets, which have

a particle size of approximately 8 to 12 microns, to bond to micro-organisms on surfaces or in the

environment.35 As with other airborne HP systems, disinfection may only take place within vacant

rooms. In the study by Barbut et al.12 it was not deemed necessary to seal the rooms, although the

doors and windows were closed.12;32

What is the scientific evidence for effectiveness of airborne HP for decontamination of the healthcare environment?

One cohort study,14 a cross-over study,22 six before-and-after studies,12;13;15;17;18;21 two interrupted

time series19;20 and a non-randomised trial16 evaluated the efficacy of airborne HP for

decontamination of the healthcare environment. It was demonstrated that this intervention could

reduce environmental surface contamination and decrease the incidence of healthcare-associated

infections.

As detailed in the methodology, the McDonald-Arduino evidentiary hierarchy10 was used as a

framework for assessing the evidence relevant to this research question.

Level V – Demonstration of reduced microbial pathogen acquisition (colonisation or infection) by patients via non-outbreak surveillance testing and clinical incidence:

Manian et al.15 compared standard methods of terminal isolation room cleaning with the use of HP

vapour and its impact on Clostridium difficile infection rates, using a before-and-after study. This

study monitored the number of cases of C. difficile-associated diarrhoea (CDAD) before (using

standard cleaning methods) and during the intervention periods (using HP vapour) and showed a



37 % reduction in CDAD rates following its introduction. However, it is worth noting that this was a

single-centre study so the findings may not be transferable to other hospitals. It is also worth noting

that this study took place in the USA, where infection control practices may differ to those in the

UK: most notably, the use of quaternary ammonium compounds for terminal cleaning.

Horn and Otter21 undertook a before-and-after study (USA) in which patient room decontamination

was provided using HP vapour on the discharge of all patients with Clostridium difficile infection

(CDI), methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci

(VRE) or extended-spectrum beta-lactamases (ESBL) producing Gram-negative bacteria. After the

12-month baseline period, in which non-specified standard discharge cleaning was performed,

rates of nosocomial infections were measured over the following 24 months. Over the intervention

period, there was a decrease in CDI from 1.38 to 0.90 cases per 1,000 patient-days (p = 0.009), a

decrease in VRE from 0.21 to 0.01 (p < 0.001), and a decrease in ESBL producing bacteria from

0.16 to 0.01 (p = 0.001). There was also a decrease in MRSA, although this reduction was not

statistically significant (p = 0.188). The authors concluded that using HP vapour for disinfection

was more effective than standard discharge cleaning. However, the standard cleaning practices in

use were not specified and may not represent current practice within NHSScotland. Improvements

in hand hygiene were judged by the authors to be likely to have contributed to the reduction in

infection rates and, therefore, this is a probable confounding factor. One of the authors is employed

part-time by Bioquell®, the manufacturer of a HP vapour system. For this reason, there is the

possibility of investigator bias due to financial interests.

Passaretti et al.14 compared the risk of acquiring multidrug resistant organisms (MDROs) in

patients admitted to a room decontaminated using HP vapour compared to a room disinfected

using standard methods. This was a prospective cohort intervention study comparing acquisition

rates of MDROs. Patients in the HP vapour cohort were significantly less likely to acquire any

MDROs than the patients in the standard cleaning cohort, even after adjustment for confounding

factors; essentially HP vapour used in addition to standard cleaning reduced the risk of MDRO

acquisition by 64 %. This reduction of MDRO acquisition was largely due to patients in the HP

vapour cohort being five times less likely to acquire VRE than the standard cleaning cohort;

reductions in the rates of MRSA, MDR-Gram-negative rods and C. difficile were not statistically

significant. Comparison of the cohorts indicated that over an 18-month period 28 MDRO

transmissions were likely to have been prevented by the use of HP vapour in three units. HP

vapour decontamination also decreased levels of environmental contamination, particularly in

rooms with multiple MDROs. However, it is worth noting that this study took place in a single

institution, so the results are not necessarily amenable to generalisation. It is also significant that

this study was conducted in the USA, which may have led to different infection control practices,

including the use of quaternary ammonium cleaning products as part of a terminal clean. The



authors also note that there were other infection prevention initiatives ongoing at the time of the

study. In addition, Bioquell® (the manufacturers of a HP vapour system) contributed to the study

design, collection of data and the writing of the report, increasing the risk of investigator bias.

Mitchell et al.20 conducted an interrupted time series in a public hospital (Australia) that introduced

a combination of HP vapour for single rooms (n = 1363) and HP wipes for shared rooms (n = 349),

after discharge of patients either colonised or infected with MRSA. Following a baseline period of

12 months, in which terminal discharge room cleaning was provided using neutral pH detergent (n

= 1917), airborne HP was utilised by in-house hospital cleaning staff for a further period of 24

months. After the intervention was introduced, the incidence of MRSA acquisition reduced from 9.0

to 5.3 per 10,000 patient-days (p < 0.001). Meanwhile the incidence of MRSA bacteraemia also

reduced from 0.16 to 0.11 per 10,000 patient-days, although this change was not statistically

significant (p = 0.58). The authors concluded that using HP vapour and HP wipes in combination

was more effective than detergent cleaning alone. Detergent cleaning is not recommended

practice for discharge cleaning of MRSA-contaminated patient rooms in NHSScotland; thus, it does

not make a suitable comparator. In addition, the study combines multiple intervention components,

so it is not possible to determine whether this impact was solely due to the use of HP vapour or HP

wipes. A number of potential confounders were recognised: additional MRSA screening, changing

antimicrobial consumption, staff feedback on terminal cleaning, and quicker laboratory methods of

MRSA isolation. However, hand hygiene compliance was consistent throughout the study duration.

Level IV – Demonstration of reduced microbial pathogen acquisition (colonisation or infection) by patients via outbreak surveillance testing and clinical incidence:

No evidence identified.

Level III – Demonstration of in-use bioburden reduction that may be clinically relevant:

Otter et al.19 assessed the efficacy of terminal cleaning and HP vapour for the decontamination of

environmental surfaces in the ward side-room of a patient with an extensive history of MRSA,

Gram-negative rods (GNRs) and VRE infection and colonisation. The rate of environmental

recontamination following HP vapour decontamination was also assessed. Terminal cleaning

reduced the number of sites with MRSA from 60 % to 40 % and, for GNRs, from 30 % to 10 %. HP

vapour reduced the number of sites with MRSA to 3.3 % and no GNRs were isolated. VRE was

isolated from 6.7 % of sites before and after cleaning but was not isolated from any sites after HP

disinfection. The patient remained colonised with MRSA during and after both experiments, so HP

vapour decontamination did not lead to the decolonisation of the patient through removal of the

environmental reservoir. This might have been due to the intrinsic colonisation of the patient

leading to recontamination of the environment immediately after cleaning occurs. However, the

GNRs seen in the environment did not match the species infecting or colonising the patient, so it is



unlikely that the patient was the source of the GNRs. It is worth noting that only 15 sample sites

were used for the environmental sampling and that only one patient was included in the study.

Terminal cleaning was conducted using quaternary ammonium compounds – a product that is not

currently recommended by the NHS in Scotland.

Level II – Demonstration of in-use bioburden reduction effectiveness:

Otter et al.17 compared the effect of a terminal clean using 2,000 ppm hypochlorite solution with the

use of HP vapour to remove environmental reservoirs of multidrug resistant GNRs during an

outbreak. In this study, 10 of 21 areas yielded GNRs after a terminal clean; however, no GNRs

were found after the use of HP vapour. The study also looked at acquisition rates of MDROs and

found no new cases until at least 3 months after HP vapour disinfection had taken place. This

would indicate that HP vapour was more effective at removing GNRs from surfaces than a terminal

clean with hypochlorite solution, and that the chain of transmission was broken during the

outbreak. However, this study used a before-and-after study design, whereas a cohort design

might have allowed a more appropriate comparison to be made. No rationale was provided for the

use of hypochlorite with 2,000 ppm available chlorine over the concentration of 1,000 ppm

currently recommended in NHS Scotland. In addition, there were a limited number of sample sites

used and the study took place on a single site in a hospital in the Netherlands, so the results

cannot be generalised.

Barbut et al.12 compared the efficacy of an aerosolised (or “dry mist”) HP system with a

hypochlorite solution containing 5,000 ppm available chlorine for eradicating C. difficile spores.

There were 31 rooms included in this study; 15 rooms were treated with HP and 16 rooms were

treated with hypochlorite. Before cleaning, C. difficile spores were detected in 21 % of surface

samples and 74 % of rooms. After disinfection, the percentage of samples showing environmental

contamination decreased in both arms; spores were detected in 12 % of samples from the

hypochlorite-treated rooms and 2 % of the HP-treated rooms. The decrease in the percentage of

contaminated samples was significantly greater in the HP group (91 %) than in the hypochlorite

group (50 %). The percentage of rooms with at least one sample positive for C. difficile in the

hypochlorite disinfection arm was 69 % before treatment and 50 % after treatment. In the HP

disinfection arm, the percentage of rooms with at least one sample positive for C. difficile was 80 %

before treatment and 20 % after treatment. This demonstrates that the aerosolised HP system had

a greater efficacy for the removal of C. difficile than 5,000 ppm hypochlorite. This study took place

in two university hospitals in France. The study was financially supported by Sterinis® (the

manufacturer of the HP system used). The company also provided the reagents, equipment and

contributed to the costs of consumables, potentially leading to a conflict of interest. No rationale

was provided for the use of hypochlorite with 5,000 ppm available chlorine rather than the

concentration of 1,000 ppm currently recommended in NHSScotland.



French et al.13 compared terminal cleaning and HP vapour decontamination of a hospital

environment using the presence of MRSA as an outcome measure. Using matched sites, 90 % of

248 sites had MRSA before terminal cleaning and 66 % had MRSA after terminal cleaning. 72 % of

85 sites had MRSA before HP vapour disinfection and 1.2 % of sites had MRSA after HP

disinfection. These results indicated that HP vapour was more effective at removing environmental

MRSA than standard terminal cleaning. However, a few points are important to bear in mind: firstly,

this study took place in 2004 and HP vapour technology has changed significantly since then, in

terms of the equipment available and the time taken for decontamination to take place. Secondly,

standard terminal cleaning used a solution of detergent sanitiser containing 5 – 15 % non-ionic

surfactant and 5 – 15 % cationic surfactant, diluted at a ratio of 1:500, which is not in line with

current guidance in Scotland. The study was funded by Bioquell®, a company that also declares

an involvement in the conception, design and execution of the project. There is no mention of the

rooms being cleaned before HP vapour decontamination took place, despite current guidance

stating that this could impact on the results observed.

Doan et al.16 investigated and compared the effectiveness of HP vapour with standard hypochlorite

cleaning using 1,000 ppm available chlorine to decontaminate rooms contaminated with C. difficile

027. The clinical effectiveness was measured using standardised median log10 reductions in colony

counts and, based on this measurement, the chlorine releasing agent was found to be as effective

as HP vapour. However, despite standardised techniques, each room started at different baseline

counts of C. difficile spores and, even with a standardised inoculation density, it was not possible

to control how many C. difficile spores germinated and how many bacteria grew. This variability in

results was compensated for in the statistical analysis by using median values and standardised

reduction.

Blazejewski et al.22 embarked upon a randomised cross-over study in a university hospital (France)

that randomly allocated patient rooms to either HP vapour (n = 93) or aerosolised HP/peracetic

acid (n = 89) for disinfection, after standard terminal cleaning using quaternary ammonium

compounds, detergent and a sodium hypochlorite solution. A total of 24 environmental

microbiological samples were collected per room, from eight high-touch surfaces, at three time

points: after patient discharge, after standard cleaning, and after HP disinfection. Standard terminal

cleaning reduced environmental bacterial load (p < 0.001) without affecting MDRO contamination

(p = 0.371). But HP reduced environmental MDRO contamination from 6 % to 0.5 % (p = 0.004),

although no significant difference was found between HP vapour and aerosolised HP/peracetic

acid. The authors concluded that both HP systems were more effective at reducing environmental

contamination than standard terminal cleaning. The prevalence of MDRO within the patient rooms

was relatively low (8%); therefore, the sample size (which was calculated assuming a prevalence

of 30 – 40 %) may not have been large enough to detect a statistically significant difference



between the two HP systems. In addition, Bioquell® and Anios® donated the airborne HP systems

for the trial. Although neither company had any role in the data analysis or reporting, Bioquell® did

contribute to the study design. This raises the possibility of investigator bias due to financial

interests.

Level I – Laboratory demonstration of bioburden reduction efficacy:

Lawley et al.18 used C. difficile spores as an outcome measure to evaluate hypochlorite solution

with 10,000 ppm available chlorine in relation to 3 % and 10 % HP vapour provided by Sigma®

and Bioquell®. They demonstrated that C. difficile spores were inactivated by 10,000 ppm

hypochlorite as well as 10 % HP vapour. They also investigated the time dependency involved in

the use of HP vapour, demonstrating that prolonged exposure was required to achieve a six-log

reduction of bacterial spores (20 minutes at 10 %).

To summarise the evidence, it can be concluded that there is low- to moderate-quality evidence to

support the use of airborne HP decontamination as an adjunct to standard cleaning procedures in

the healthcare environment. In accordance with SIGN methodology, the cohort study constituted

level 2+ evidence (well-conducted controlled analytic studies with a low risk of confounding, bias,

or chance and a moderate probability that the relationship is causal). In contrast, the cross-over

studies, before-and-after studies and interrupted time series were all designated level 3 evidence

(uncontrolled analytic studies).

Are there any safety considerations associated with using airborne HP decontamination systems in the healthcare setting?

Chlorine-releasing agents are considered easy-to-use and the least expensive environmental

disinfection method available. However, they do feature a number of limitations such as the

release of irritating vapours and toxic gases which may affect the eyes and respiratory tracts of

healthcare workers at high concentrations (i.e. 10,000 ppm available chlorine), and personal

protective equipment is recommended for this reason. Sodium hypochlorite-based products can be

corrosive to various materials and potentially cause damage to environmental surfaces. In addition,

the disinfection process must be performed manually, which can be time-consuming, with the

quality of disinfection depending on the staff member performing the procedure. This has led to a

renewed interest in alternative methods of environmental decontamination.12;16;36

HP appears to have low levels of toxicity and, as it degrades into oxygen and water, it is

compatible with most materials. Monitoring units are able to measure the residual concentrations of

HP and ensure that exposure is appropriate.12;30 Johnston et al.37 found HP vapour to be safe and

environmentally-compatible for decontaminating areas such as biological safety cabinets and



microbiology containment laboratories. Passaretti et al.14 have also reported no safety, equipment,

or material compatibility concerns.

Ernstgard et al.38 tested the effects of exposure to HP vapour in humans. The key limitation of this

study was that only 11 people were included. In this study, no exposure-related effects on

pulmonary function were observed. Similarly, there were no exposure-related effects on markers of

inflammation or coagulation. Mild irritation of the upper respiratory airways was observed when

people were exposed to HP vapour at 2.2 ppm, though no effects were observed at 0.5 ppm.

There were no effects on lung function or inflammatory markers at either exposure level.

Manian et al.15 state that they found HP vapour to be safe with no instances of vapour leaking

outside the sealed rooms during the decontamination process. During their intervention, there were

no significant adverse reactions attributed to HP vapour in either patients or healthcare workers.

Barbut et al.12 compared an aerosolised HP disinfection system with a hypochlorite clean and

found that the HP-based formulations had greater material compatibility, while also being less toxic

to human beings and the environment. The aerosolised HP system also had an advantage over

HP vapour systems in that, while disinfection still needs to take place in a vacant room, there is no

need to seal the room.

Are there any practical or logistical considerations associated with using airborne HP decontamination systems in the healthcare setting?

Airborne HP decontamination offers a number of benefits compared to standard cleaning with

hypochlorite. Automated HP systems are not subject to user error in the way that manual cleaning

may be. The quality of manual cleaning can vary and has been shown to be suboptimal, not least

because manual cleaning is limited to areas that are easily accessible.32;39 Airborne HP can reach

sites that would be inaccessible for cleaners, such as cracks, crevices or other hard-to-reach

surfaces.30;39;40 Airborne HP can also be used to decontaminate electrical equipment which may be

damaged by the use of cleaning liquids.40 Equipment that may be missed in standard

decontamination can be collected together in a room and effectively decontaminated at the same

time using airborne HP.16

HP systems are able to ensure adequate contact times between the disinfectant and

environmental sites, ensuring the application of correct disinfectant concentrations. These are key

issues for the effectiveness of the disinfection process, and can be achieved more successfully by

using pre-programmed robots rather than relying on cleaning personnel.30;39;40

There a number of practical and logistical considerations with using airborne HP systems. One key

limitation is the need to remove debris and organic matter from all surfaces so that the HP is not

prevented from accessing micro-organisms.40 Pottage et al.34 found that biological soiling reduced



the efficacy of airborne HP decontamination. Their study demonstrated that the presence of

organic matter resulted in a slower inactivation of bacteriophage using HP vapour decontamination

and that this was exacerbated as the concentration of organic matter increased. This highlights the

importance of effective cleaning prior to gaseous disinfection especially in the hospital setting

where infective agents are likely to be suspended in body fluids. Therefore, it is recommended that

surfaces are manually cleaned with appropriate disinfectants prior to the deployment of airborne

HP decontamination.

The use of all airborne HP decontamination systems require the area to be vacated for the duration

of the decontamination process.14 If a hospital ward needs to be decontaminated, then the whole

ward needs to be moved to alternative accommodation which is a major undertaking and depends

on the availability of additional space.40;41 If HP vapour is used then all heating, ventilation and air

conditioning ducts in the area to be decontaminated must be sealed, along with any doors.14;42 The

airborne HP systems require a team of trained personnel to operate the specialised machinery.16;41

Airborne HP decontamination is relatively time-consuming, even if it is limited to rooms rather than

wards. This is due to the need for an effective initial clean, followed by the use of airborne HP

decontamination and aeration processes, and then monitoring of the environment to ensure that it

is safe to re-enter. This entails a longer process than a standard clean.40;41 If it could be applied

without the need to wait for a deep clean to take place, the process would be easier, less time-

consuming and more cost-effective for healthcare use.41

Another key issue to be considered when using airborne HP decontamination is the rapid rate of

recontamination with pathogens that occurs as soon as patients are readmitted.27 Best et al.40

highlighted this issue in their study investigating the effectiveness of airborne HP against C. difficile

infection (CDI). They found that the rate of CDI influenced how long the enhanced antimicrobial

effectiveness of airborne HP lasted, and depended on whether the ward it was used in was in an

outbreak or non-outbreak setting. Their results demonstrated that airborne HP may be a useful

decontamination method for a hospital ward with a high incidence of CDI.

What costs are associated with using airborne HP decontamination systems in the healthcare setting?

Airborne HP systems are significantly more expensive than the hypochlorite solutions used in

standard cleaning. Doan et al.16 compared the cost-effectiveness of HP vapour and a chlorine-

releasing agent. Their studies demonstrated that the chlorine-releasing agent cost £14.14 per use

and £149.65 per month, compared with £108.96 per use and £1,154.98 per month for HP vapour.

They concluded that HP vapour was more effective at reducing spore counts than the chlorine-

releasing agent but was also more expensive. They found that there was insufficient evidence for

the cost-effectiveness of HP over traditional hypochlorite based cleaning.



Best et al.40 report that the cost of using airborne HP amounted to about £7,000 per ward, including

staff costs and materials, and therefore may only be justifiable in some cases, e.g. following an

outbreak. The requirement for areas to be vacated while they are being decontaminated using

airborne HP systems incurs additional costs and can potentially lead to delays in bed availability.14

Another factor to consider in terms of the cost of airborne HP decontamination is the rapid rate of

recontamination seen to take place.41

Have airborne HP decontamination systems been assessed by the Rapid Review Panel?

The Rapid Review Panel43 (RRP) is a panel of UK experts established by the Department of Health

to review new technologies with the potential to aid in the prevention and control of healthcare-

associated infections. The RRP has reviewed a number of airborne HP disinfection products

between 2005 and 2008:

2005: Sterinis (Related Life Sciences Ltd)

2007: Bioquell Hydrogen Peroxide Vapour System (Bioquell)

2008: Vaporised Hydrogen Peroxide (Steris)

The aerosolised HP system Sterinis® was assessed in 2005 and awarded a recommendation 4

status. The RRP has since altered their recommendation system to encompass 4a and 4b

categories:

“Not a significant improvement on equipment/materials/products already available which claim to

contribute to reducing health care associated infection; no further consideration needed.” (R4a)

“Unlikely to contribute to the reduction of health care associated infection; no further consideration

needed.” (R4b)

A HP vapour system produced by Bioquell® was assessed in 2007 and awarded a

recommendation 1 status:

“Basic research and development, validation and recent in use evaluations have shown benefits

that should be available to NHS bodies to include as appropriate in their cleaning, hygiene or

infection control protocols.” (R1)

A HP vapour system produced by Steris® was assessed in 2008 and awarded a recommendation

2 status:

“Basic research and development has been completed and the product may have potential value;

in use evaluations/trials are now needed in an NHS clinical setting.” (R2)



Discussion

This systematic review incorporated the results of 11 studies into its findings. The quality of

included studies was predominantly of level 3 (low-quality) evidence; however, there was one

study classified as level 2+ (moderate-quality) evidence. The study design of choice was a

before-and-after study, an interrupted time series or a cohort study. They primarily concerned

either in-use bioburden reduction (level III) or reduced microbial pathogen acquisition in a non-

outbreak setting (level V). The findings identified by the review were used to develop the following

recommendations for clinical practice.

Recommendations for Clinical Practice

This review makes the following recommendations based on an assessment of the extant

professional literature on airborne hydrogen peroxide (HP) systems for environmental

decontamination:

• Airborne HP systems can be used as an adjunct to manual cleaning when performing

terminal room decontamination.

(Grade C recommendation)

• The use of airborne HP systems for environmental decontamination should only be adopted

following completion of a manual clean as residual dirt can reduce efficacy.

(Grade D recommendation)

• Prior to an airborne HP system being considered, an assessment of the area to be

decontaminated must be undertaken to ensure the area can be sealed and the use of HP

made safe.


• Airborne HP systems must only be used in an area which has been cleared of all patients

and staff. No entry to the decontamination area is allowed once the decontamination

process has commenced.


• Consideration must be given to whether airborne HP will interact with the fire alarm system

and, if so, ensure that local estates are involved to isolate the fire alarm system.


• Airborne HP systems in use must be maintained in good working order and a system of

programmed maintenance in place with documented evidence.

(Good Practice Point)



• Airborne HP may be considered for cleaning of the environment and/or equipment where

ongoing transmission of an organism has occurred and the environment and/or equipment

is considered the route of transmission.


• Airborne HP systems should not be used for routine cleaning.


• If fumigation is the recommended decontamination process (e.g. disinfection of Ebola-

contaminated equipment), then HP should be considered.


• The use of airborne HP cleaning does not reduce the importance of general cleaning

routinely and between patients.


• All users of airborne HP systems, whether an NHS Board employee or an external

contractor, must be trained in the product use and potential hazards of the system, and

have assurance of product safety.


• A Standard Operating Procedure (SOP) must be established and detail processes of when

and how airborne HP cleaning is used regardless of the provision of use by NHS Boards or

external contractors.


• Validation processes must be in place by NHS Boards and external contractors following

decontamination to ensure the healthcare environment is clean.




Implications for Research

The review identified several gaps in the literature in relation to airborne HP decontamination

systems. Many of the relevant studies identified could not be included in this review as they did not

make a suitable comparison in the form of standard cleaning as recommended for NHSScotland in

the National Infection Prevention and Control Manual.9 These studies variously compared the use

of airborne HP disinfection with sodium hypochlorite at a range of concentrations, quaternary

ammonium compound disinfectants, or the use of detergent only. Future studies assessing the

clinical effectiveness of airborne HP systems for decontamination should include suitable

comparison groups to enable the results to be transferable to clinical practice within NHSScotland.

It was also notable that several of the studies combined multiple infection control interventions with

the use of airborne HP disinfection, such as the simultaneous introduction of airborne HP and HP

wipes, the provision of staff feedback on terminal cleaning, and additional screening for colonised

patients. Ideally, studies that evaluate the effectiveness of airborne HP decontamination systems

should exclude other infection control interventions in order to minimise the risk of confounding

factors producing a spurious result.

Finally, very few studies thus far have evaluated the cost-effectiveness of airborne HP

decontamination systems. Of the few that have, the majority have primarily considered the capital

costs of the necessary equipment and the cost of manual labour to operate the devices, in

comparison against the costs of disinfectants used for traditional cleaning. It can be seen from

these studies that a comprehensive cost-effectiveness evaluation for the use of airborne HP

decontamination systems in NHSScotland would be timely.



Conclusion

The contribution of environmental contamination in healthcare settings to the cross-transmission of

nosocomial infections has been thoroughly demonstrated: firstly, by interventional studies in which

improved surface cleaning has reduced the incidence of HAIs;1 and secondly, by observational

studies which have evidenced the higher risk of pathogen acquisition in patients admitted to rooms

where the prior occupant was known to be infected or colonised.2 Airborne hydrogen peroxide (HP)

decontamination systems provide an example of a novel technology that may supplement standard

cleaning practices and potentially further reduce the transmission of nosocomial pathogens. This

review aimed to provide a concise evidence summary outlining: the evidence of effectiveness for,

the practical and safety considerations of, and the costs associated with, the use of airborne HP

decontamination systems.

The review found that there was a larger quantity of evidence supporting the use of HP vapour

systems than aerosolised HP systems, although this evidence was of low- to moderate-quality.

Nine of the eleven studies demonstrated that using airborne HP systems after standard cleaning

was more effective than standard cleaning alone. For four of these studies, airborne HP was more

effective than hypochlorite while for five of the studies, airborne HP was more effective than

quaternary ammonium disinfectants or detergents. The two other studies showed that airborne HP

systems were similar in effectiveness to hypochlorite solution. However, the studies often lacked a

concurrent control group and frequently combined multiple infection control interventions within a

single study. In addition, the standard cleaning measures adopted did not always reflect current

best practice recommended for use in NHSScotland.

To ensure staff and patient safety, it is recommended that all personnel should be cleared from the

room before use and that the room should be closed to entry for the duration. There is a risk that

airborne HP systems can interfere with the normal operation of heating, ventilation and air

conditioning systems. Consideration should be given to whether airborne HP devices will interact

with these systems and, if so, measures should be implemented to disable them. There has also

been little in the way of cost-effectiveness evaluations of airborne HP systems in the UK.

The Rapid Review Panel (RRP) has evaluated three airborne HP disinfection systems: one that

uses aerosolised HP and two that use HP vapour. Both HP vapour devices were assigned a

recommendation grade of 1 or 2. This classification advises that the product has either shown

benefits that should be available to NHS bodies or that the product may have potential value, and

that in-use evaluations are needed in an NHS clinical setting. The only aerosolised HP device was

categorised with a grade 4: a product that does not show a significant improvement over the

alternatives currently available.



Appendix 1: MEDLINE Search (2014)

Ovid MEDLINE(R) 1946 to present with daily update

AND

Ovid MEDLINE(R) In-process & other non-indexed citations

Search dates

24/06/2014 and 25/06/2014

1 (all “OR”) 2 (all “OR”) 3 (all “OR”)

Hydrogen peroxide/ hydrogen peroxide.mp. HPV.mp.

AND

Sterilization/ Decontamination/ Disinfection/ Housekeeping, Hospital/ clean*.mp.

AND

Aerosols/ Volatilization/ mist*.mp. fog*.mp. vapo?r*.mp.

Limits

English Language

Publication Year 2004 – 2014 Results: 136



Appendix 2: MEDLINE Search (2016)

Ovid MEDLINE(R) 1946 to present with daily update

Search dates

08/08/2016

1 (all “OR”) 2 (all “OR”)

(hydrogen peroxide adj2 disinfect*).mp. (hydrogen peroxide adj2 decontaminat*).mp. (hydrogen peroxide adj2 vapo?r*).mp. (hydrogen peroxide adj2 aerosol*).mp.

AND

Sterilization/ Decontamination/ Disinfection/ Housekeeping, Hospital/ clean*.mp.

Limits

English Language

Publication Year 2014 – Current Results: 28



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