Methods to improve disinfection of environmental surfaces in hospital rooms include improving cleaning/disinfection by environmental service workers through education and feedback on cleaning effectiveness (eg, use of fluorescent dyes), “no-touch” methods (eg, UV-C light), and self-disinfecting surfaces. Self-disinfecting surfaces can be created by impregnating or coating surfaces with heavy metals (eg, silver or copper), germicides (eg, triclosan), or miscellaneous methods (eg, light-activated antimicrobials). These methods are under active investigation but to date have not been assessed for their ability to reduce health care-associated infections.
Key Words
More than 20 years ago, Dr Robert Weinstein estimated that source of pathogens for health care-associated pathogens was cross infection via the hands of health care personnel (HCP) is 20% to 40% and the environment is another 20%.
1
In the intervening years, substantial scientific evidence has accumulated that contamination of environmental surfaces in hospital rooms plays an important role in the transmission of several key health care-associated pathogens, including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus species (VRE), Clostridium difficile, Acinetobacter species, and norovirus.2
, 3
, 4
All of these pathogens have been demonstrated to persist in the environment for hours to days (and in some cases for months), to frequently contaminate the surface environment and equipment in the rooms of colonized or infected patients, to transiently colonize the hands of HCP, to be associated with patient-to-patient transmission via the hands of HCP, and to cause outbreaks in which environmental transmission was deemed to play a role. Furthermore, hospitalization in a room in which the previous patient had been colonized or infected with MRSA, VRE, C difficile, or Acinetobacter species has been shown to be a risk factor for colonization or infection with the same pathogen to the next patient admitted to the room.3
, 4
Pathogen transfer from an infected patient to a susceptible patient occurs most commonly via the hands of HCP, but contaminated hospital surfaces, medical equipment, water, and air can be directly or indirectly involved in the transmission pathways. These transmission pathways and methods to interrupt transmission have been diagramed.
4
, 5
HCP have frequent contact with the environmental surfaces in patient’s rooms, providing ample opportunity for contamination of gloves and/or hands.6
Furthermore, it has observed that there is lower compliance with hand hygiene by HCP following contact with the patient’s environment than directly with the patient.7
Hand contamination with MRSA has been demonstrated to occur with equal frequency when HCP contact a colonized/infected patient or through only touching contaminated surfaces.8
Finally, the most significant risk factor for hand/glove contamination of HCP with multidrug-resistant pathogens has been demonstrated to be positive environmental cultures.9
Potential methods of decreasing the frequency and level of contamination of environmental surfaces in hospital rooms have included routine and terminal disinfection with chemical germicides
10
and, more recently, the use of “no touch” methods of terminal room disinfection with ultraviolet (UV) light or aerosolized and/or vaporized hydrogen peroxide.Rutala WA, Weber DJ, and Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: http://www.cdc.gov/hicpac/Disinfection_Sterilization/acknowledg.html. Accessed October 14, 2011.
11
Unfortunately, routine and terminal cleaning of room surfaces by environmental service workers and portable medical equipment by nursing staff is frequently inadequate. Multiple studies have demonstrated that less than 50% of hospital room surfaces are adequately cleaned and disinfected when chemical germicides are used.12
, 13
However, with implementation of enhanced performance feedback, education, and other interventions, the frequency of appropriate cleaning can be increased to 71% to 77%.- Goodman E.R.
- Platt R.
- Bass R.
- Onderdonk A.B.
- Yokoe D.S.
- Huang S.S.
Impact of a 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
13
, - Goodman E.R.
- Platt R.
- Bass R.
- Onderdonk A.B.
- Yokoe D.S.
- Huang S.S.
Impact of a 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
14
Similarly, inadequate cleaning of portable medical equipment by nursing staff has also been demonstrated.15
The use of “no-touch” methods such as devices that emit UV light or produce hydrogen peroxide have been developed to improve room disinfection. However, a major limitation of these technologies is that currently they can only be used for terminal room disinfection because they require removal of the patients and HCP from the room. Other limitations include the high acquisition costs of room decontamination units and increased time of room turnover.11
Recently, another method of reducing the frequency and level of surface contamination in hospital rooms has been described: self-disinfecting surfaces (Table 1). Such surfaces have also been called “self-sanitizing,” and, because microbial killing requires direct contact with the surface, the term “contact killing” has also been used. This paper will expand on our recent commentary on this subject,
16
as well as providing updated information.Table 1Self-disinfecting surfaces: Possible methodologies
NOTE. Adapted from Weber and Rutala.
16
| Methodology | Options |
|---|---|
| Surface impregnated with a metal | Silver; copper |
| Surface impregnated with a germicide | Triclosan; antimicrobial surfactant/quaternary ammonium salt |
| Miscellaneous | Altered topography; light-activated antimicrobial coating |
Surfaces impregnated or coated with a heavy metal
Heavy metals comprise approximately 65 elements that are considered metals and have a specific gravity greater than 5.
17
, 18
Most heavy metals are either insoluble or extremely rare, and their effects on biologic systems are of minor importance. However, more than 30 heavy metals are potentially able to interact with microorganisms including silver (Ag), gold (Au), bismuth (Bi), cobalt (Co), copper (Cu), iron (Fe), mercury (Hg), manganese (Mn), nickel (Ni), lead (Pb), platinum (Pt), antimony (Sb), tin (Sn), titanium (Ti), and zinc (Zn). It has been known since antiquity that some heavy metals possess anti-infective activity. Among the use of heavy metals to prevent or treat infections have been the use of copper-clad ships to resist the growth of barnacles; mercurials, arsenic derivatives and bismuth compounds to treat syphilis; silver nitrate to prevent gonococcal neonatal conjunctivitis, and silver compounds as topic agents to prevent infection in burn patients.17
Despite the fact that modern antibiotics have largely replaced heavy metal therapeutics for treating infection, intense research is being conducted into the use of heavy metal containing complexes (platinum, copper, zinc, and gold) for the treatment of cancer19
and metal-based drugs (antimony, ruthenium, gold, platinum, palladium, and zinc) for the treatment of malaria, trypanosomiasis, and leishmaniasis.20
Although the development of self-disinfecting surfaces impregnated or coated with silver or copper is farthest advanced (see below), the use of other heavy metals such as titanium is also being studied.21
Silver
Silver has been used extensively throughout recorded history for a variety of medical purposes.
22
Silver compounds continue to be used for topical antisepsis (eg, silver nitrate and silver sulfadiazine).23
The effectiveness of central venous catheters impregnated with silver sulfadiazine-chlorhexidine or silver iontophoretic in preventing central line-associated bloodstream infections has been demonstrated in multiple randomized clinical trials and meta-analyses.24
, 25
Other indwelling medical devices impregnated with a silver compound have been developed including endotracheal tubes26
and urinary catheters.27
More recently, silver nanoparticles have been incorporated into wound dressings, indwelling catheters, bone cement and other implants, clothing and environmental surfaces and some of these products are now commercially available.28
, 29
, 30
Silver ions have the highest level of antimicrobial activity of all the heavy metals.
31
Although many mechanisms for silver’s bactericidal activity have been proposed, the observed bactericidal efficacy of silver is thought to be through the strong binding with disulfide (S-S) and sulfhydral (-SH) groups found in the proteins of microbial cell walls. Through this binding event, normal metabolic processes are disrupted, leading to cell death.31
Both intrinsic and acquired silver resistance has been well described in bacteria.31
, 32
The major mechanisms appear to be either exclusion of silver from the bacterial cell or mobilization outside the cell.31
Silver may be added to polymers to confer antimicrobial activity and has been incorporated into such consumer products as toys, telephones, and infant pacifiers.
31
To date, only one product (Surfacine; Surfacine Development Company, Tyngsborough, MA) has been assessed for use as a self-disinfecting surface in hospitals. It incorporates a water-soluble antimicrobial compound (silver iodide) in a surface-immobilized coating (a modified polyhexamethlyenebiguanide) that is capable of chemical recognition and interaction with the lipid bilayer of the bacterial outer cell membrane by electrostatic attraction.33
Microorganisms contacting the coating accumulate silver until the toxicity threshold is exceeded. Surfacine can be applied to inanimate surfaces by dipping, brushing, or spraying without prior surface treatment. Surfaces to which this agent had been applied have been shown to kill 3.3- to 4.3-log10 S aureus and 2.2- to 4.8-log10 Pseudomonas aeruginosa hours after application of Surfacine.34
In addition, a greater than 3-log10 kill of MRSA and VRE was also achieved. Residual activity of Surfacine against VRE has been shown for 13 days.33
However, to date there are no published studies assessing the ability of this agent to reduce the microbial contamination on environmental surfaces in actual hospital rooms or to decrease the incidence of health care-associated infections. Silver is made by complexing alkaline earth metals with crystal aluminosilicate, which is partially replaced by silver ions using ion exchange method. The antibacterial efficacy of a silver/zinc zeolite ceramic coating on stainless steel has been demonstrated by challenge with S aureus, but to date there are no studies of actual hospital surfaces coated with a silver/zinc zeolite.35
The effectiveness of silver nanoparticles when incorporated into environmental surfaces has not been assessed in the hospital environment.Copper
Copper is an essential trace element in most living organisms, and more than 30 types of copper-containing proteins have been described.
36
, 37
, 38
, 39
, 40
Copper has been used for centuries as a medicinal and to prevent growth of barnacles on the hulls of ships.37
, 38
However, copper ions at increased levels are toxic to most microorganisms because of their ability to generate reactive oxygen species and act as a strong soft metal (eg, leading to release of iron from Fe-S clusters).37
, 39
The copper generated radicals can damage lipids, nucleic acids, and proteins, leading to cell death. In health care, copper compounds (ie, copper-silver ionization) are used for control of Legionella species in water supplies41
and Aspergillus on building materials (ie, copper-8-quinolinolate).42
More recently, copper-coated or -impregnated surfaces have been evaluated in hospitals.37
, 39
, 40
The contact killing of microbes by copper has been assessed in multiple in vitro studies.
38
, 40
Most microbes were inactivated by copper within minutes to hours, but, because parameters such as inoculation technique, incubation temperature, and copper content of the alloy were not investigated in a systematic way, comparisons between studies are difficult.38
According to Grass et al, a few general principles can be drawn from these in vitro studies: higher copper content of alloys, higher temperature, and higher relative humidity increased the efficacy of killing.38
Treatments that lowered corrosion rates (eg, application of corrosion inhibitors or a thick copper oxide layer) lowered the antimicrobial effectiveness of copper surfaces. Contact with copper has been demonstrated to kill a variety of health care-associated pathogens including S aureus, MRSA, Enterococcus species, Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii, P aeruginosa, and Mycobacterium tuberculosis in minutes to several hours.38
, 43
Spore-forming bacteria such as Bacillus and Clostridium pose a substantial challenge to germicides that work by contact killing because spores are relatively resistant to heat, radiation, desiccation, and germicides. Copper has been shown to kill greater than 6-log10 of vegetative C difficile cells within 30 minutes.
44
However, the same authors demonstrated no reduction in viability of dormant C difficile spores within 3 hours, although a greater than 99% reduction of germinating C difficile spores was noted at 3 hours. Greater than 3-log10 of C difficile spores have been shown to be completely inactivated by copper surfaces in 24 to 48 hours.45
As with silver, microorganisms have developed mechanisms to survive copper ion challenge including efflux pumps, permeability barriers, intra- and extracellular sequestration, enzymatic detoxification, and reduction in the sensitivity of cellular targets to copper ions.
36
, 40
Some strains of bacteria isolated from copper coins have been demonstrated to survive for more than 48 hours on dry copper surfaces.46
However, contact with copper alloys will kill most copper ion-resistant strains (eg, Salmonella enterica pv typhimurium, E coli, P aeruginosa) within 60 minutes although one strain of Enterococcus faecium survived for greater than 2 hours on a dry copper surface.37
Multiple studies of copper containing surfaces or devices have been conducted in the health care setting comparing the level and frequency of surface contamination to control surfaces.
47
, 48
, 49
, 50
, 51
Studies have either used concurrent non-copper-containing control surfaces47
, 48
, 49
, 50
or a crossover design.51
Casey et al demonstrated that a copper toilet seat would result in a 94% to 98% reduction in total aerobic colony-forming units (cfu).47
In a similar study, it was demonstrated that copper-coated desks, trolleys, and surfaces (top of cupboard and windowsill) resulted in a 1- to 2-log10 decrease in mean cfu.48
Rai et al have demonstrated that copper coating of the arms of phlebotomy chair and tray over the chair reduced median total aerobic cfu by 88% and 90%, respectively.50
Mikolay et al demonstrated a 37% reduction of total aerobic cfu on door knobs, push plates, and light switches.49
Finally, Karpanen et al have described the surface contamination levels on 14 types of frequently touched items made of copper alloys that were installed in various locations on an acute medical ward.51
Items included door handles, toilet seats, grab rails, light switches, over-bed tables, commodes, and others. The copper items were switched to similar non-copper items halfway through the 24-week study period. Eight of the 14 copper item types had significantly lower microbial counts on their surfaces compared with those made of standard materials. MRSA, VRE, coliforms, and C difficile were found to contaminate 0.4% to 8.1% of surfaces; contamination by VRE and coliforms was statistically reduced on the copper items, and no significant reduction was noted for MRSA and C difficile. Repeated cleaning/disinfection of a copper surface over 5 days with either 1% sodium hypochlorite or 70% industrial methylated spirit were shown to lead to “surface conditioning,” which resulted in decreased killing of S aureus.52
In interpreting the results of some of the above studies, it is important to note that neither the study by Rai et al50
nor that of Karpanen et al51
assessed the thoroughness of cleaning of surfaces, thus the finding may have been due to improved cleaning rather than the effect of copper on decreasing bioburden. Copper-containing paints,53
fabrics,40
hand rubs,40
microfiber cleaning cloths,54
pens,55
and fins within air-conditioning units56
have also been evaluated for use in health care.Surfaces impregnated or coated with a germicide
Surfaces and devices impregnated or coated with a germicide are widely available. Concern has been raised that the use of such surfaces and devices might lead to bacteria developing resistance to the germicide with possible cross-resistance to clinically useful antibiotics.
57
, 58
Triclosan
Triclosan (2,4,4’-trichloro-2’-hydroxy-diphenyl ether) is a nonionic, colorless substance that has antimicrobial activity at concentrations of 0.2% to 2%.
59
Triclosan has a broad range of antimicrobial activity, but it is often bacteriostatic.59
Its activity against gram-positive organisms is greater than its activity against gram-negative bacilli. Triclosan has been incorporated into a wide range of home and personal care objects, including soaps, underarm deodorants, toothpaste, and cutting boards.58
, 60
Triclosan-impregnated cutting boards have been shown to lead to decreases in bacteria applied to the boards, including reductions of 0.5- to 1.0-log10 for S aureus and Serratia species and 1.5- to 1.7-log10 for E coli and Salmonella species.Triclosan: White paper produced by The Alliance for the Prudent Use of Antibiotics (APUA), January 2011. Available from: www.tufts.edu/med/apua/.../personal_home_21_4240495089.pdf. Accessed August 17, 2012.
61
P aeruginosa is intrinsically resistant to triclosan.62
When P aeruginosa was grown as biofilm on discs of polyethylene, Teflon, and stainless steel, 1% triclosan was only effective in achieving a reduction in organisms of less than 1-log10.63
In the laboratory, bacteria with reduced susceptibility to triclosan can be produced fairly readily by serial passage in increasing triclosan concentration.62
However, the minimum inhibitory concentration of such strains generally are substantially below the concentration of triclosan contained in antimicrobial products. We were unable to find any studies evaluating the use of triclosan-impregnated hospital environmental surfaces or devices.Quaternary ammonium compounds
Recently, an antimicrobial surfactant whose core product is a quaternary ammonium salt, Goldshield, has been evaluated.
64
Using a carrier test, the agent was demonstrated to kill 0.5- to 2.4-log10 MRSA and 0.6- to 0.9-log10 P aeruginosa and E coli within 30 minutes on formica and stainless steel.64
Rechallenge after 4 days generally did not demonstrate microbial inactivation, although a statistical reduction was noted for MRSA on formica (but not stainless steel) carriers. No published studies are available on using this agent on environmental surfaces in hospital rooms. Data demonstrate that quaternary ammonium disinfectants continue to have persistent antimicrobial activity that extends beyond their wet time on the surface; activity may extend beyond 24 hours provided the disinfectant is left on the surface undisturbed.65
Miscellaneous methods to achieve self-disinfecting surfaces
Several promising new technologies are under examination to develop self-disinfecting surfaces including altered surface typography and light-activated germicides bound to surfaces.
Altered topography
A novel approach to the development of self-disinfecting surfaces is the use of an engineered microtopography to inhibit bacterial biofilm formation. One such design is Sharklet AF (Sharklet Technologies, Alachua, FL), which seeks to use topography similar to shark skin to inhabit biofilms. Reduced biofilm formation and growth of S aureus has been described on molds employing Sharklet AF.
66
Urogenic E coli were inhibited on silicone elastomer coupons, suggesting that this method could be used to develop Foley catheters, which would inhibit microbial growth.67
We are unaware of any published studies assessing this new technology to inhibit microbial growth on actual indwelling medical devices or hospital environmental surfaces.- Reddy S.T.
- Chung K.K.
- McDaniel C.J.
- Darouiche R.O.
- Landman J.
- Brennan A.B.
Micropatterned surfaces for reducing the risk of catheter-associated urinary tract infection: an in vitro study on the effect of Sharklet micropatterned surfaces to inhibit bacterial colonization and migration of uropathogenic Escherichia coli.
J Endourol. 2011; 25: 1547-1552
Light-activated antimicrobial coatings
Light-activated antimicrobial coatings are currently being studied for the continuous disinfection of surfaces. Irradiation of certain compounds (photosentizers) with visible light results in the production of cytotoxic species such as singlet oxygen and free radicals. Wilson studied a cellulose acetate layer containing the photosensitizer toluidine blue O and demonstrated kills of 94% for S aureus and 99.9% for P aeruginosa when in contact with impregnated acetate layer following exposure to light (400-700 nm wavelength) for 24 hours.
68
More recently, a cellulose acetate coating containing toluidine blue O and rose Bengal has been studied.69
, 70
, 71
Illumination of 6 hours resulted in a 2- to 3-log10 reduction in S. aureus, but, if the organism was suspended in saliva or horse serum, reductions of <1-log10 were noted.69
Exposures of ≥6 hours have been demonstrated to inactivate >6-log10 of S aureus, MRSA, E coli, and C difficile (mainly vegetative cells) under experimental conditions.70
In a clinical environment, a 63.8% reduction in aerobes and 81.8% reduction in anaerobes have been reported.71
Silicone polymers containing the light-activated antimicrobial agent methylene blue were more effective in reducing the microbial load on surfaces in a clinical environment when combined with gold nanoparticles.72
Conclusion
The novel technologies, especially those employing nanotechnology, has dramatically improved the likelihood of developing a self-disinfecting surface. The potential development of such surfaces has tremendous possibilities. Most importantly, the use of such surfaces could minimize the impact of poor cleaning and disinfecting practices during both routine and terminal room cleaning and disinfection. It is important to note that the currently available “no-touch” technologies such as UV-C light irradiation and vaporized/aerosolized hydrogen peroxide can only be used for terminal room disinfection at the present time because they are hazardous to patients and staff. However, novel “no touch” methods such as using continuous low-dose (ie, 0.2 ppm) hydrogen peroxide vapor or high-intensity, narrow-spectrum (ie, 405 nm) visible light are being evaluated.
73
, 74
The potential advantages and current limitations of self-disinfecting technologies are summarized in Table 2. Of the different technologies available (Table 1), copper-impregnated or -coated surfaces have been the most extensively evaluated.40
Table 2Advantages and disadvantages of currently proposed self-disinfecting surfaces in hospital rooms
| Advantages |
|
|
|
|
| Current limitations |
|
|
|
|
|
|
However, a few cautions regarding self-disinfecting surfaces should be noted. First, many of these surfaces have demonstrated only modest killing (<2-log10 pathogens). Second, the ability of these new surfaces to kill intrinsically more resistant pathogens such as C difficile spores and norovirus has often not been fully evaluated. Third, the cost of installing and maintaining such surfaces has not been described. Fourth, only incomplete information is available on the durability of such surfaces and whether their antimicrobial activity is affected by temperature, humidity, frequency of cleaning, and presence of organic load. Fifth, the relative benefits and limitations of different self-disinfecting technologies have not been studied in comparative trials. Finally, no studies have been published that demonstrate that installing such surfaces reduces health care-associated infections. In addition, it is important to note that the level of microbial contamination of hospital room surfaces does not correlate with the frequency with which they are touched by HCP, suggesting that, for self-disinfecting surfaces to reduce health care-associated infections, multiple self-disinfecting surfaces and devices would need to be installed.
75
Despite the current unknowns with regard to the utility of self-disinfecting surfaces, continued research and evaluation of clinical value in this area are clearly warranted as means of reducing the impact of environmental contamination in the transmission of health care-associated pathogens.References
- Epidemiology and control of nosocomial infections in adult intensive care units.Am J Med. 1991; 91: S179-S184
- 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 spp.Am J Infect Control. 2010; 38: S25-S33
- The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699
- Cleaning, disinfection, and sterilization.in: Ruth Carrico APIC text of infection control and epidemiology. 3rd ed. Association for Professionals in Infection Control and Epidemiology, Inc, Washington [DC]2009 (p. 21–21-18)
- A quantitative approach to defining high-touch surfaces in hospitals.Infect Control Hosp Epidemiol. 2010; 31: 850-853
- Twenty-four hour observational study of hospital hand hygiene compliance.J Hosp Infect. 2010; 76: 252-255
- 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
- Transfer of multidrug-resistant bacteria to healthcare workers’ gloves and gowns after patient contact increases with environmental contamination.Crit Care Med. 2012; 40: 1045-1051
Rutala WA, Weber DJ, and Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: http://www.cdc.gov/hicpac/Disinfection_Sterilization/acknowledg.html. Accessed October 14, 2011.
- Are room decontamination units needed to prevent transmission of environmental pathogens?.Infect Control Hosp Epidemiol. 2011; 32: 743-747
- Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.Infect Control Hosp Epidemiol. 2008; 29: 1-7
- Impact of a 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
- Improving cleaning of the environment surrounding patients in 36 acute care hospitals.Infect Control Hosp Epidemiol. 2008; 29: 1035-1041
- Cleanliness of portable medical equipment disinfecting by nursing staff.Am J Infect Control. 2011; 39: 602-604
- Self-disinfecting surfaces.Infect Control Hosp Epidemiol. 2012; 33: 10-13
- Use of metals as microbiocides in the prevention of nosocomial infections.in: Rutata W.A. Chemical germicides in health care. Association for Professionals in Infection Control and Epidemiology, Inc, Washington [DC]1994: 271-285
- Use of metals as microbicides in preventing infections in healthcare.in: Block S.S. Disinfection, sterilization, and preservation. 5th ed. Lippincott Williams & Wilkins, Philadelphia [PA]2001: 415-430
- Novel metals and metal complexes as platforms for cancer therapy.Curr Pharm Des. 2010; 16: 1813-1825
- Metal-based drugs for malaria, trypanosomiasis and leishmaniasis: recent achievements and perspectives.Drug Discovery Today. 2010; 15: 1070-1078
- Titanium oxide antibacterial surfaces in biomedical devices.Int J Artif Organs. 2011; 34: 929-946
- History of the medical use of silver.Surg Infect. 2009; 10: 289-292
- Evidence-based review of silver dressing use on chronic wounds.J Am Acad Nurse Practitioners. 2011; 23: 183-192
- The clinical effectiveness of central venous catheters treated with anti-infective agents in preventing catheter-related bloodstream infections: a systematic review.Crit Care Med. 2009; 37: 702-712
- Effectiveness of different central venous catheters for catheter-related infections: a network meta-analysis.J Hosp Infect. 2010; 76: 1-11
- Silver-coated endotracheal tubes and incidence of ventilator-associated pneumonia: the NASCENT randomized trial.JAMA. 2008; 300: 805-813
- Silver alloy vs. uncoated urinary catheters: a systematic review of the literature.J Clin Nurs. 2011; 20: 2098-2108
- Nanosilver: a nanoproduct in medical application.Toxicol Lett. 2008; 176: 1-12
- Silver nanoparticles as a new generation of antimicrobials.Biotechnol Adv. 2009; 27: 76-83
- Nanosilver as a new generation of nanoproduct in biomedical applications.Trends Biotechnol. 2010; 28: 580-588
- Silver as a disinfectant.Rev Environ Contam Toxicol. 2007; 191: 23-45
- Bacterial resistance to silver in wound care.J Hosp Infect. 2005; 60: 1-7
- New disinfection and sterilization methods.Emerg Infect Dis. 2001; 7: 348-353
- Persistent silver disinfectant for the environmental control of pathogenic bacteria.Am J Infect Control. 2003; 31: 208-214
- Rapid reduction of Stahylococcus aureus populations on stainless steel surfaces by zeolite ceramic coatings containing silver and zinc ions.J Hosp Infect. 2002; 52: 307-309
- Copper toxicity and the origin of bacterial resistance: new insights and applications.Metallomics. 2011; 3: 1109-1118
- Advantages and challenges of increased antimicrobial copper use and copper mining.Appl Microbiol Biotechnol. 2011; 91: 237-249
- Metallic copper as an antimicrobial surface.Appl Environ Microbiol. 2011; 77: 1541-1547
- Copper in microbial pathogenesis: meddling with the metal.Cell Host Microbe. 2012; 11: 106-115
- Application of copper to prevent and control infection. Where are we now?.J Hosp Infect. 2012; 81: 217-223
- Controlling Legionella in hospital drinking water: an evidence-based review of disinfection methods.Infect Control Hosp Epidemiol. 2011; 32: 166-173
- Preventing healthcare-associated Aspergillus infections: review of recent CDC/HICPAC recommendations.Med Mycol. 2009; 47: S199-S209
- The antimicrobial activity of copper and copper alloys against nosocomial pathogens and Mycobacterium tuberculosis isolated from healthcare facilities in the Western Cape: an in-vitro study.J Hosp Infect. 2008; 68: 45-51
- Antimicrobial efficacy of copper surfaces against spores and vegetative cells of Clostridium difficile: the germination theory.J Antimicrob Chemother. 2008; 62: 522-525
- Survival of Clostridium difficile on copper and steel: futuristic options for hospital hygiene.J Hosp Infect. 2008; 68: 145-151
- Isolation and characterization of bacteria resistant to metallic copper surfaces.Appl Environ Microbiol. 2010; 76: 1341-1348
- Role of copper in reducing hospital environment contamination.J Hosp Infect. 2010; 74: 72-77
- Antimicrobial efficacy of copper touch surfaces in reducing environmental bioburden in a South African community healthcare facility.J Hosp Infect. 2010; 74: 80-81
- Survival of bacteria on metallic copper surfaces in a hospital trial.Appl Microbiol Biotechnol. 2010; 87: 1875-1879
- Evolution of the antimicrobial properties of copper surfaces in an outpatient infectious disease practice.Infect Control Hosp Epidemiol. 2012; 33: 200-201
- The antimicrobial efficacy of copper alloy furnishing in the clinical environment: a crossover study.Infect Control Hosp Epidemiol. 2012; 33: 3-9
- Potential use of copper as a hygienic surface; problems associated with cumulative soiling and cleaning.J Hosp Infect. 2007; 67: 271-277
- Bactericidal activity of copper and noncopper paints.Infect Control Hosp Epidemiol. 1995; 16: 444-450
- Performance of ultramicrofibre cleaning technology with or without addition of a novel copper-based biocide.J Hosp Infect. 2010; 74: 62-71
- A comparative study to evaluate surface microbial contamination associated with copper-containing and stainless steel pens used by nurses in the critical care unit.Am J Infect Control. 2011; 39: e52-e54
- Potential for preventing spread of fungi in air-conditioning systems constructed using copper instead of aluminum.Lett Applied Microbiol. 2010; 50: 18-23
- Antimicrobial biocides in the healthcare environment: efficacy, usage, policies, and perceived problems.Ther Clin Risk Manag. 2005; 1: 307-320
- Use of germicides in the home and healthcare settings: is there a relationship between germicide use and antibiotic resistance?.Infect Control Hosp Epidemiol. 2006; 27: 1107-1119
- Guideline for hand hygiene in health-care settings.MMWR. 2002; 51: 1-45
Triclosan: White paper produced by The Alliance for the Prudent Use of Antibiotics (APUA), January 2011. Available from: www.tufts.edu/med/apua/.../personal_home_21_4240495089.pdf. Accessed August 17, 2012.
- Assessment of the antibacterial activity of a triclosan-containing cutting board.Int J Food Microbiol. 2011; 146: 157-162
- Whither triclosan?.J Antimicrob Chemother. 2004; 53: 693-695
- Efficacy of common hospital biocides with biofilms of multi-drug resistant clinical isolates.J Med Microbiol. 2008; 57: 966-973
- In vitro evaluation of a novel process for reducing bacterial contamination of environmental surfaces.Am J Infect Control. 2011; 39: 483-487
- Bacterial contamination of keyboards: efficacy and functional impact of disinfectants.Infect Control Hosp Epidemiol. 2006; 27: 372-377
- Impact of engineered surface microtopography on biofilm formation of Staphylococcus aureus.Biointerphases. 2007; 2: 89-94
- Micropatterned surfaces for reducing the risk of catheter-associated urinary tract infection: an in vitro study on the effect of Sharklet micropatterned surfaces to inhibit bacterial colonization and migration of uropathogenic Escherichia coli.J Endourol. 2011; 25: 1547-1552
- Light-activated antimicrobial coating for continuous disinfection of surfaces.Infect Control Hosp Epidemiol. 2003; 24 (Wilson M): 782-784
- Novel light-activated antimicrobial coatings are effective against surface-deposited Staphylococcus aureus.Curr Microbiol. 2008; 57: 269-273
- Cellulose acetate containing toluidine blue and rose bengal is an effective antimicrobial coating when exposed to white light.Appl Environ Microbiol. 2006; 72: 4436-4439
- Assessment of the activity of a novel light-activated antimicrobial coating in a clinical environment.Infect Control Hosp Epidiomiol. 2008; 29: 1181-1184
- Efficacy of a novel light-activated antimicrobial coating for disinfecting hospital surfaces.Infect Control Hosp Epidemiol. 2011; 32: 1130-1132
- Sporicidal effects of high-intensity 405-nm visible light on endospore-forming bacteria.Photochem Photobiol. 2013; 89: 120-126
- Environmental decontamination of a hospital isolation room using high-intensity narrow-spectrum light.J Hosp Infect. 2010; 76: 247-251
- Microbial assessment of high, medium, and low-touch hospital room surfaces.Infect Control Hosp Epidemiol. 2013; 34: 211-212
Article Info
Footnotes
Publication of this article was supported by Advanced Sterilization Products (ASP).
Conflicts of interest: W.A.R. has served as consultant for ASP and Clorox, and D.J.W. has served as a consultant for Clorox.
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© 2013 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
