Environmental contamination plays an important role in the transmission of several key health care-associated pathogens. Effective and thorough cleaning/disinfecting of the patient environment is essential. Room decontamination units (such as ultraviolet-C and hydrogen peroxide systems) aid in reducing environmental contamination after terminal room cleaning and disinfection.
Key Words
Health care-associated infections remain an important source of morbidity and mortality with an estimated 1.7 million infections and 99,000 deaths annually.
1
The major source of nosocomial pathogens is thought to be the patient’s endogenous flora, but an estimated 20% to 40% of health care-associated infections have been attributed to cross infection via the hands of health care personnel.2
Contamination of the hands of health care personnel could in turn result from either direct patient contact or indirectly from touching contaminated environmental surfaces. Health care personnel have frequent contact with the environmental surfaces in patient’s rooms, providing ample opportunity for contamination of gloves and/or hands.3
Two recent studies demonstrated that contact with the environment was just as likely to contaminate the hands of health care workers as was direct contact with the patient.4
, 5
Furthermore, it has been observed that there is lower compliance with hand hygiene by health care personnel following contact with the patient’s environment than directly with the patient.6
There is excellent evidence in the scientific literature that environmental contamination plays an important role in the transmission of several key health care-associated pathogens including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus (VRE), Acinetobacter, norovirus, and Clostridium difficile.
7
, 8
, 9
, 10
All these pathogens have been demonstrated to persist in the environment for hours to days (in some cases months),11
to frequently contaminate the environmental surfaces in rooms of colonized or infected patients, to transiently colonize the hands of health care personnel, to be transmitted by health care personnel, and to cause outbreaks in which environmental transmission was deemed to play a role. Furthermore, admission to a room in which the previous patient had been colonized or infected with MRSA, VRE, Acinetobacter, or C difficile has been shown to be a risk factor for the newly admitted patient to develop colonization or infection.12
, 13
, 14
Adequacy of room cleaning and disinfection using chemical germicides
It has long been recommended in the United States that environmental surfaces in patient rooms be cleaned/disinfected on a regular basis (eg, daily, 3 times per week), when surfaces are visibly soiled, and following patient discharge (terminal cleaning).
15
Studies have demonstrated that adequate environment cleaning is frequently lacking. For example, Carling et al assessed the thoroughness of terminal cleaning in the patient’s immediate environment in 23 acute care hospitals (1,119 patient rooms) by using a transparent, easily cleaned, stable solution that fluoresces when exposed to hand-held ultraviolet (UV) light.Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.
16
The overall thoroughness of cleaning, expressed as a percent of surfaces evaluated, was 49% (range for all hospitals, 35%-81%). Using a similar design, Carling et al assessed the environmental cleaning in intensive care unit rooms in 16 hospitals (2,320 objects) and demonstrated that only 57.1% of sites were cleaned following discharge of the room’s occupant.17
A study by Havill et al using adenosine triphosphate (ATP) bioluminescence assays and aerobic cultures demonstrated that medical equipment frequently had not been disinfected as per protocol.18
Disinfection is generally performed using an US Environmental Protection Agency (EPA)-registered hospital disinfectant such as quaternary ammonium compounds, chlorine-containing compound, phenolics, or improved hydrogen peroxide (HP) (Table 1). The improved HP-based environmental surface disinfectants have proved to be more effective (>6-log10 reduction) and fast-acting (30-60 seconds) microbicides in the presence of a soil load (to simulate the presence of body fluids) than commercially available HP.
19
Table 1Summary of advantages and disadvantages of disinfectants used as low-level disinfectants
15
Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.
| Low-level disinfectant | Advantages | Disadvantages |
|---|---|---|
| Alcohol |
|
|
| Chlorine |
|
|
| Improved hydrogen peroxide |
|
|
| Iodophors |
|
|
| Phenolics |
|
|
| Quaternary ammonium compounds |
|
|
Effective cleaning/disinfecting of the patient environment is essential; however, there have been few studies that have assessed various cleaning methods. A recent study comparing several cleaning/disinfecting methods against C difficile (eg, saturated cloth; spray [let sit 10 seconds] and wipe; spray, wipe, spray [let sit 1 minute] and wipe; use of disposable pop-up wipes) demonstrated no difference in the effectiveness of various wiping procedures. Wiping with a sporicidal agent eliminated ≥3.90 log10 C difficile by both physical removal and inactivation.
20
Improving room cleaning/disinfection and demonstrating the effectiveness of surface decontamination in reducing health care-associated infections
Several investigators have reported that intervention programs aimed at environmental services workers resulted in significant improvement in cleaning practices.
21
, 22
, 23
Such interventions have generally included multiple activities: improved education, monitoring the thoroughness of cleaning (eg, by use of ATP assays or fluorescent dyes) with feedback of performance to the environmental service workers, and/or use of cleaning checklists. We have found that a specific assignment of cleaning responsibility for each hospital unit (eg, medical equipment to be cleaned by nursing; environmental surfaces to be cleaned by environmental service) is also important to ensure all objects and surfaces are decontaminated, especially the surfaces of medical equipment (eg, cardiac monitors). Improved environmental cleaning has been demonstrated to reduce the environmental contamination with VRE,24
, 25
, - Goodman E.R.
- Platt R.
- Bass R.
- Onderdonk A.B.
- Yokoe D.S.
- Huang S.S.
Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
Infect Control Hosp Epidemiol. 2008; 29: 593-599
26
MRSA,25
and C difficile.- Goodman E.R.
- Platt R.
- Bass R.
- Onderdonk A.B.
- Yokoe D.S.
- Huang S.S.
Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
Infect Control Hosp Epidemiol. 2008; 29: 593-599
26
Importantly, no study has reported, in the postintervention period, proper cleaning of more than 85% of objects. A concern of published studies is that they have only demonstrated improved cleaning of a limited number of “high risk” objects (or “targeted” objects) and not an improvement in the overall thoroughness of room decontamination. The focus of disinfection efforts should be directed at thorough, room disinfection24
and not focused on “high risk” surfaces because they have not been demonstrated to be associated with an increased risk of contamination of health care personnel hands/gloves or increased risk for patient-to-patient transmission of pathogens. Nor should the disinfection efforts be focused on “high-touch” surfaces because the level of contamination is similar to that of lower, less frequently contacted surfaces (eg, high touch surface 71.9 colony-forming units [CFU]/Rodac vs low touch surface 56.7 CFU/Rodac before cleaning).27
More emphasis should be placed on adequately training environmental service workers and providing timely feedback on the thoroughness of cleaning using fluorescent marking or ATP-based methods and surface disinfection of all “touchable” surfaces.Contact time for disinfection of noncritical surfaces and patient care equipment
The US Centers for Disease and Prevention (CDC) guideline discusses a 1-minute contact time (ie, wet time) for low-level disinfection of noncritical environmental surfaces and patient care equipment. To get EPA clearance of the CDC Guideline, it was necessary to insert the sentences “By law, all applicable label instructions on EPA-registered products must be followed. If the user selects exposure conditions that differ from those on the EPA-registered product label, the user assumes liability from any injuries resulting from off-label use and is potentially subject to enforcement action under FIFRA.”
15
There are several points that should be made about this apparent disconnect between label instructions and what scientific studies demonstrate to include: (1) multiple scientific studies have demonstrated the efficacy of hospital disinfectants against pathogens causing health care-associated infections with a contact time of at least 1 minuteRutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.
15
; (2) there are no data that demonstrate improved infection prevention by a 10-minute contact time versus a 1-minute contact time; and (3) we are not aware of an enforcement action by the EPA against health care facilities for “off label” use of a surface disinfectant. Furthermore, the only way an institution can achieve a contact time of 10 minutes is to reapply the surface disinfectant multiple times to the surface (which is unlikely) because the typical dry time for a water-based disinfectant is 1.5 to 2 minutes. Last, as important as disinfectant contact time is to surface disinfection, nothing is more important than the thoroughness of cleaning/disinfecting all hand contact surfaces (eg, environmental surfaces or patient care equipment) because current studies demonstrate that less than 50% of high-risk objects are cleaned/disinfected at terminal cleaning.Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.
21
, 22
Wiping all “hand contact” or “touchable” surfaces/equipment, and not just perceived “high risk” surfaces/equipment, is essential because “high risk” surfaces/equipment have not been epidemiologically defined. In addition, “high touch” surfaces have only recently been defined but there was no significant difference in microbial contamination of “high,” “medium,” and “low” touch surfaces.3
If an institution chooses to use a product with a nonachievable label claim (eg, 10 minutes), it should prepare a formal risk assessment (see http://www.unc.edu/depts/spice/dis/SurfDisRiskAssess2011.pdf) to be presented to surveyors (eg, The Joint Commission) when challenged. Alternatively, the hospital could purchase and use for low-level disinfection of noncritical surfaces and patient care equipment an EPA-registered disinfectant with an achievable contact time such as a disinfectant with a 30 second to 2 minute bactericidal claim (see http://www.epa.gov/oppad001/chemregindex.htm).Another issue is which pathogen on the disinfectant label should be used to identify contact time (eg, bacteria, Candida, mycobacteria, spores) for surfaces in health care facilities. The CDC Guideline based the 1-minute contact time on demonstration of bactericidal activity for vegetative bacteria such as S aureus, Enterococcus, Eschericihia coli, coagulase-negative Staphylococcus, Pseudomonas aeruginosa, Klebsiella spp, Enterobacter spp, and others. These vegetative bacteria are the pathogens that cause the vast majority of health care-associated infections (85%-90%).
28
, 29
Furthermore, contaminated surfaces with organisms such as Candida, nontuberculous mycobacteria, and other fungi have rarely, if ever, been shown to be a risk factor for health care-associated infections. The only exception to this principle is the use of EPA-registered disinfectant effective against C difficile spores or norovirus for disinfecting the rooms of patients with one of these pathogens (see http://www.epa.gov/oppad001/chemregindex.htm).- Hidron A.I.
- Edwards J.R.
- Patel J.
- Horan T.C.
- Sievert D.M.
- Pollock D.A.
- et al.
Antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007.
Infect Control Hosp Epidemiol. 2008; 29: 996-1011
“No Touch” methods for room disinfection
As noted above, multiple studies have demonstrated that environmental surfaces and objects in rooms are frequently not properly cleaned. Furthermore, whereas interventions aimed at improving cleaning thoroughness have demonstrated effectiveness, many surfaces remain inadequately cleaned and therefore potentially contaminated. For this reason, several manufacturers have developed room disinfection units that can decontaminate environmental surfaces and objects. These systems use 1 of 2 methods: either UV light or HP (Table 2, Table 3, Table 4).
1
, 30
These technologies supplement, but do not replace, standard cleaning and disinfection because surfaces must be physically cleaned of dirt and debris. Additionally, these methods can only be used for terminal or discharge room decontamination (ie, cannot be used for daily room decontamination) because the room must be emptied of people. This paper will update and expand on a recent publication of this topic.1
Table 2Comparison of room decontamination systems using hydrogen peroxide and ultraviolet irradiation
NOTE. Adapted from Rutala and Weber
1
Otter and Yezli.42
| Glosair (formerly Sterinis) | Steris | Bioquell | Tru-D | |
|---|---|---|---|---|
| Abbreviation | DMHP (dry mist HP) | VHP (vaporized HP) | HPV (HP vapor) | UV-C |
| Active agent | 5% hydrogen peroxide, <50 ppm silver cations, <50 ppm ortho-phosphoric acid | Vaprox (35% hydrogen peroxide) | 35% hydrogen peroxide | UV-C irradiation at 254 nm |
| Application | Aerosol of active solution | Vapor, noncondensing | Vapor, condensing | UV irradiation; direct and reflected |
| Aeration (removal of active agent from enclosure) | Passive decomposition | Active catalytic conversion | Active catalytic conversion | Not necessary |
| Sporicidal efficacy | Single cycle does not inactivate Bacillus atrophaeus BIs; ∼4-log10 reduction of C difficile and incomplete inactivation in situ | Inactivation of Geobacillus stearothermophilus BIs | Inactivation of Geobacillus stearothermophilus BIs; >6-log10 reduction of C difficile in vitro and complete inactivation in situ | 1.8- to 4-log10 reduction of C difficile in situ |
| Evidence of clinical impact | None published | None published | Significant reduction in the incidence of C difficile | None published |
BIs, Biologic indicators; UV-C, ultraviolet-C light; VRE, vancomycin-resistant Enterococcus.
Glosair (Advanced Sterilization Products, Irvine, CA); Steris (Mentor, OH); Bioquell (Horsham, PA); Tru-D (Lumalier Conporation, Memphis, TN).
Table 3Efficacy of hydrogen peroxide systems for decontamination of the hospital environment, by health care-associated pathogen
NOTE. Modified from Falagas et al.
36
| Lead author, year | HP system | Pathogen | Sites revealing contamination before HPV | Sites revealing contamination after HPV | % Reduction |
|---|---|---|---|---|---|
| French, 2004 35
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: 31-37 | HPV | MRSA | 61/85-72% | 1/85-1% | 98 |
| Bates, 2005 43 | HPV | Serratia | 2/42-5% | 0/24-0% | 100 |
| Jeanes, 2005 44 | HPV | MRSA | 10/28-36% | 0/50-0% | 100 |
| Otter, 2007 46 | HPV | MRSA | 18/30-60% | 1/30-3% | 95 |
| Dryden, 2008 45 | HPV | MRSA | 8/29-28% | 1/29-3% | 88 |
| Boyce, 2008 39 | HPV | C difficile | 11/43-26% | 0/37-0% | 100 |
| Bartels, 2008 47 | HP dry mist | MRSA | 4/14-29% | 0/14-0% | 100 |
| Shapey, 2008 48 | HP dry mist | C difficile | 48/203-24% | 7/203-3% | 88 |
| Barbut, 2009 49 | HP dry mist | C difficile | 34/180-19% | 4/180-2% | 88 |
| Otter, 2010 50 | HPV | GNR | 10/21-48% | 0/63-0% | 100 |
HPV, Hydrogen peroxide vapor.
Table 4Advantages and disadvantages of room decontamination by ultraviolet irradiation and hydrogen peroxide
1
| Ultraviolet irradiation |
|---|
| Advantages |
|
|
|
|
|
|
|
|
| Disadvantages |
|
|
|
|
|
|
|
| Decontamination by hydrogen peroxide systems |
| Advantages |
|
|
|
|
|
|
|
|
| Disadvantages |
|
|
|
|
|
|
|
HVAC, Heating, ventilation, and air conditioning.
UV light for room decontamination
UV irradiation has been used for the control of pathogenic microorganisms in a variety of applications, such as control of legionellosis, as well as disinfection of air, surfaces, and instruments.
31
, 32
At certain wavelengths, UV light will break the molecular bonds in DNA, thereby destroying the organism. UV-C has a characteristic wavelength of 200 to 270 nm (eg, 254 nm), which lies in the germicidal active portion of the electromagnetic spectrum of 200 to 320 nm. The efficacy of UV irradiation is a function of many different parameters such as intensity, exposure time, lamp placement, and air movement patterns.An automated mobile UV-C unit (Tru-D; Lumalier Corporation; Memphis, TN) has been shown to eliminate > 3-log10 vegetative bacteria (MRSA, VRE, Acinetobacter baumannii) and > 2.4-log10 C difficile seeded onto formica surfaces in patients’ rooms experimentally contaminated.
10
There are 3 studies that have demonstrated that this UV-C system is capable of reducing vegetative bacteria inoculated on a carrier by >3- to 4-log10 in 15 to 20 minutes and C difficile by >1.7- to 4-log10 in 35 to 100 minutes.10
, 33
, 34
The studies also demonstrate reduced effectiveness when surfaces were not in direct line-of-sight.HP systems for room decontamination
Several systems that produce HP (eg, HP vapor, aerosolized dry mist HP, vaporized HP) have been studied for their ability to decontaminate environmental surfaces and objects in hospital rooms (Tables 2 and 3). A system using HP vapor has been demonstrated to completely inactivate >106 Bacillus stearothermophilus spores contained in biologic indicators hung in patient rooms and almost eliminate all MRSA surface contamination.
35
Other studies have also demonstrated the ability of HP systems to almost eliminate MRSA, VRE, M tuberculosis, spores, viruses, and multidrug-resistant gram-negative bacilli.- French G.L.
- Otter J.A.
- Shannon K.P.
- Adams N.M.T.
- Watling D.
- Parks M.J.
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: 31-37
36
, 37
, 38
Importantly, using a before-after design, Boyce et al have previously shown that use of the HP systems was associated with a significant reduction in the incidence of C difficile infection on 5 high-incidence wards.39
A recent paper by Passaretti et al demonstrated that environmental decontamination with HP vapor reduced the risk of a patient admitted to a room previously occupied by a colonized or infected patient with a multidrug-resistant organism from acquiring an multidrug-resistant organism by 64% compared with using standard disinfection methods.40
However, HP system decontamination was shown to require more than 4-times longer to complete than conventional cleaning, thus resulting in prolonged bed turn-over time.41
Comparison of UV irradiation versus HP for room decontamination
The UV-C system and the systems that use HP have their own advantages and disadvantages (Table 4). The main advantage of both units is their ability to achieve substantial reductions in vegetative bacteria. As noted above, manual cleaning has been demonstrated to be suboptimal because many environmental surfaces are not cleaned. Another advantage is their ability to substantially reduce C difficile spores as low-level disinfectants (such as quaternary ammonium compounds) have only limited or no measurable activity against spore-forming bacteria. Both systems are residual free, and they decontaminate all exposed surfaces and equipment in the room.
The major disadvantages of both decontamination systems are the substantial capital equipment costs; the need to remove personnel and patients from the room, thus limiting their use to terminal room disinfection (must prevent/minimize exposure to UV and HP); the staff time needed to transport the system to rooms to be decontaminated and monitor its use; and the need to physically clean the room of dust and debris. There are several important differences between the 2 systems. The UV-C system offers faster decontamination, which reduces the “down” time of the room before another patient can be admitted. A UV reflective wall coating reduced the time necessary to decontaminate a room using a UV-C emitting device from 25 minutes to 5 minutes for MRSA and from 44 minutes to 9 minutes for C difficile spores (Unpublished results, Rutala, Gergen, Tande, Weber, 2012). The HP systems have been demonstrated to be more effective in eliminating spore-forming organisms. Whether this improved sporicidal activity is clinically important is unclear because studies have demonstrated that, although environmental contamination is common in the rooms of patients with C difficile infection, the level of contamination is relatively low (also true for MRSA, VRE). Finally, the HP system was demonstrated to reduce C difficile incidence in a clinical study, whereas similar studies with the UV-C system have not been published.
Conclusion
Ample evidence exists that environmental contamination with important health care-associated pathogens (MRSA, VRE, Acinetobacter, norovirus, and Clostridium difficile) poses a risk for patient-to-patient transmission of these organisms. Multiple studies have demonstrated that environmental service workers frequently fail to decontaminate “high-risk” objects. Importantly, recent studies demonstrated that contact with the environment was just as likely to contaminate the hands of health care workers as was direct contact with the patient.
4
, 5
Whereas an intervention bundle can improve cleaning by environmental service workers, it still remains suboptimal with many objects and surfaces not cleaned. Furthermore, the ability to achieve high rates of cleaning long-term has not been demonstrated. Although “no touch” room decontamination systems might aid in reducing/eliminating environmental contamination after terminal room disinfection, we still need to develop new practices or technologies to improve the thoroughness of daily room cleaning (eg, tinted germicides that color surfaces when applied, but the color disappears once it dries). Finally, cost-effectiveness analysis of these no-touch methods should be performed.
There is now ample evidence that “no touch” systems such as UV-C or HP can reduce environmental contamination with health care-associated pathogens. However, each specific system should be studied and their efficacy demonstrated (similar to systems in Table 2) before introduction into health care facilities. Importantly, only a single study that used a before-after design has been published, which demonstrates that such a system can reduce health care-associated infections. Additional studies assessing the effectiveness of “no touch” room decontamination systems are needed to further assess the benefits of these technologies. In addition, cost-effectiveness studies would be useful in aiding selection among the different room decontamination technologies and specific systems. Last, if additional studies continue to demonstrate benefit, widespread adoption of these technologies (eg, a supplemental intervention during outbreaks, after discharge of patients on Contact Precautions, on a regular basis in special rooms [eg, operating rooms]) should be considered for terminal room disinfection in health care facilities.
References
- Are room decontamination units needed to prevent transmission of environmental pathogens?.Infect Control Hosp Epidemiol. 2011; 32: 743-747
- Epidemiology and control of nosocomial infections in adult intensive care units.Am J Med. 1991; 9: S179-S184
- A quantitative approach to defining high-touch surfaces in hospitals.Infect Control Hosp Epidemiol. 2010; 31: 850-853
- Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients.Infect Control Hosp Epidemiol. 2011; 32: 185-187
- Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.Am J Infect Control. 2012; 40: 556-558
- Twenty-four hour observational study of hospital hand hygiene compliance.J Hosp Infect. 2010; 76: 252-255
- The role of environmental cleaning in the control of hospital-acquired infection.J Hosp Infect. 2009; 73: 378-385
- Environmental contamination makes an important contribution to hospital infection.J Hosp Infect. 2007; 65: 50-54
- 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-S33
- Room decontamination by ultraviolet radiation.Infect Control Hosp Epidemiol. 2010; 31: 1025-1029
- How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.BMC Infect Dis. 2006; 6: 130
- Risk of acquiring antibiotic-resistant bacteria from prior room occupants.Arch Int Med. 2006; 166: 1945-1951
- Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.Infect Control Hosp Epidemiol. 2011; 32: 201-206
- The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699
Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.
- Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.Infect Control Hosp Epidemiol. 2008; 29: 1-7
- Intensive care unit environmental cleaning: an evaluation in sixteen hospitals using a novel assessment tool.J Hosp Infect. 2008; 68: 39-44
- Cleanliness of portable medical equipment disinfected by nursing staff.Am J Infect Control. 2011; 39: 602-604
- Efficacy of improved hydrogen peroxide against important healthcare-associated pathogens.Infect Control Hosp Epidemiol. 2012; 33: 1159-1161
- Efficacy of different “cleaning/disinfection” methods against Clostridium difficile spores: importance of physical removal versus sporicidal inactivation.Infect Control Hosp Epidemiol. 2012; 33: 1255-1258
- Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.Crit Care Med. 2010; 38: 1054-1059
- Improving cleaning of the environment surrounding patients in 36 acute care hospitals.Infect Control Hosp Epidemiol. 2008; 29: 1035-1041
- A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces.J Hosp Infect. 2008; 69: 156-163
- Intervention evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.J Hosp Infect. 2009; 71: 123-131
- Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.Infect Control Hosp Epidemiol. 2008; 29: 593-599
- Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.BMC Infect Dis. 2007; 7: 61
- Microbial assessment of high, medium, and low-touch hospital room surfaces.Infect Control Hosp Epidemiol. 2013; 34: 211-212
- Relative frequency of healthcare-associated pathogens by infection site at a university hospital from 1980-2008.Am J Infect Control. 2012; 40: 416-420
- Antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007.Infect Control Hosp Epidemiol. 2008; 29: 996-1011
- Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.J Hosp Infect. 2011; 77: 199-203
- Sterilization, high-level disinfection, and environmental cleaning.Infect Dis Clin N Am. 2011; 25: 45-76
- Applications of ultraviolet germicidal irradiation disinfection in health care facilities: effective adjunct, but not stand-alone technology.Am J Infect Control. 2010; 38: S13-S24
- Terminal decontamination of patient rooms using an automated mobile UV light unit.Infect Control Hosp Epidemiol. 2011; 32: 743-747
- Evaluation of an automated ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens in hospital rooms.BMC Infect Dis. 2010; 10: 197
- 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: 31-37
- Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review.J Hosp Infect. 2011; 78: 171-177
- Use of hydrogen peroxide vapor for deactivation of Mycobacterium tuberculosis in a biological safety cabinet and a room.J Clin Microbiol. 2007; 45: 810-815
- Hydrogen peroxide vapour decontamination of surfaces artifically contaminated with norovirus surrogate feline calicivirus.J Hosp Infect. 2012; 80: 116-121
- Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.Infect Control Hosp Epidemiol. 2008; 29: 723-729
- An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.Clin Infect Dis. 2013; 56: 27-35
- Feasibility of routinely using hydrogen peroxide vapor to decontaminate rooms in a busy United States hospital.Infect Control Hosp Epidemiol. 2009; 30: 574-577
- A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.J Hosp Infect. 2011; 77: 83
- Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.J Hosp Infect. 2005; 61: 364-366
- Eradication of persistent environmental MRSA.J Hosp Infect. 2005; 61: 85-86
- Hydrogen peroxide vapour decontamination in the control of a polyclonal methicillin-resistant Staphylococcus aureus outbreak on a surgical ward.J Hosp Infect. 2008; 68: 190-192
- Assessing the biological efficacy and rate of recontamination following hydrogen peroxide vapour decontamination.J Hosp Infect. 2007; 67: 182-188
- Environmental methicillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide.J Hosp Infect. 2008; 70: 35-41
- Activity of a dry mist hydrogen peroxide system against environmental Clostridium difficile contamination in elderly care wards.J Hosp Infect. 2008; 70: 136-141
- 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: 515-517
- Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.Am J Infect Control. 2010; 38: 754-756
Article info
Footnotes
Publication of this article was supported by Advanced Sterilization Products (ASP).
Conflicts of interest: W.A.R. provides consultation to Advanced Sterilization Products and Clorox, and D.J.W. provides consultative service to Clorox.
Identification
Copyright
© 2013 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
