The spread of infections through contact is linked to a range of environmental conditions that affect the growth and transmission of pathogens. Many pathogens have been found to persist in the environment and remain for days or even months (Dancer, 2014; McQueen & Ehnes, 2018; Mitchell, Spencer, & Edmiston, 2015; Schettler, 2016). Though the transmission of infection (direct or indirect) is most likely to occur via person-to-person contact, the role of surfaces in contact transmission should not be ignored (Fijan & Turk, 2012; Yeargin, Buckley, Fraser, & Jiang, 2016).
Surfaces are generally classified as either hard surfaces (e.g., window sills, charting stations and workstations, floors, walls, ceilings) or soft surfaces (e.g., bed linen, upholstery, privacy curtains, apparel). Hand hygiene has been the primary focus of infection prevention efforts; however, the design and selection of built environment surfaces (especially those identified as “high-touch surfaces”) are also important considerations in interrupting the transmission chain.
High-touch surfaces that may increase the risk of transmission are often considered in the context of the patient room (e.g., bed rails, overbed tables, door hardware, call systems), but high-touch items are found in public areas, too (e.g., public seating, elevator buttons, information desks). When selecting finishes for these surfaces, different materials and cleaning products should be thoroughly assessed based on the evidence, proposed application, cost, and logistics involved in order to achieve the desired outcomes.
Along with surfaces, ambient environmental factors like temperature, relative humidity, air change rate, ventilation, and pressure differentials to adjacent spaces have been found to affect the growth and transmission of microorganisms (Campoccia, Montanaro, & Arciola, 2013; Lopez et al., 2013; Ramos, Dedesko, Siegel, Gilbert, & Stephens, 2015; Şimşek, Grassie, Emre, & Gevrek, 2017; Tang, 2009; Verdier, Coutand, Bertron, & Roques, 2014; Yau, Chandrasegaran, & Badarudin, 2011). The design and selection of surfaces, materials, and finishes must also be considered in light of organizational policies and cleaning procedures (as summarized in the accompanying issue brief, Contact Transmission, Part 2: The Role of Materials, Design, and Cleaning in HAIs). Solutions include manual cleaning with disinfectants, no-touch automated disinfection technologies, and self-disinfecting surfaces (Rutala & Weber, 2013).
In order to reduce the transmission of HAIs through contact using design methods, the design process must take into account both surface selection and appropriate cleaning strategies. The literature reveals that operations, people, and built environmental factors can all play a role in infection prevention (Figure 1). For each element within the organization, it is necessary to pay close attention to the hosts, reservoirs, and carriers of infections, including inanimate surfaces that may be potential routes of transmission. In other words, stakeholders must take a systems approach that considers all the elements and interactions of the system holistically in order to optimize design for infection control.
Healthcare-associated infections (HAIs) are infections that are contracted over the course of receiving medical care. One in 31 hospitalized patients in the United States has HAIs (Centers for Disease Control and Prevention, 2018). Increased awareness has led to a better understanding of how inanimate objects (fomites) contribute to the transmission of healthcare-associated pathogens (Beggs, Knibbs, Johnson, & Morawska, 2015; Boyce, 2007; Carling, 2016; Dancer, 2014).
Those that kill or inhibit the growth of organisms
A subset of antimicrobial agents specific to bacteria
A subset of antimicrobial agents specific to bacteria that kills bacteria (>99.9% of an inoculum within 24 hours)
Substances or chemicals used for sterilization and disinfection
Destruction of or damage to microorganisms at the cellular level
As discussed in the Hand Hygiene issue brief, the economic burden associated with HAIs is significant. Some preventable infections, such as central line-associated bloodstream infections (CLABSIs), catheter-associated urinary tract infections (CAUTIs), surgical site infections (SSIs), hospital-acquired pneumonia (HAP) (including ventilator-associated pneumonia (VAP)), Methicillin-resistant Staphylococcus aureus (MRSA), and Clostridium difficile (C. diff or CDI), are tracked and reported as part of CMS reimbursement programs (Diekema, 2017; Schmier et al., 2016).
The threat of infections resulting from multidrugresistant organisms (MDRO) has been another area of focus, with MRSA attracting the most attention (Sandora & Goldmann, 2012). Antimicrobial stewardship programs are often established to optimize antimicrobial use, decrease the incidence of MDRO-related infections, and reduce the risk of drug resistance (Moehring & Anderson, 2012). Though they are most often addressed in the context of antibiotics, Donskey (2013) states that environmental disinfection interventions “are analogous to antimicrobial stewardship interventions.”
Common terms used in these discussions include antimicrobial agents (those that kill or inhibit the growth of organisms), antibacterial agents (a subset of antimicrobial agents specific to bacteria), bactericidal agents (also a subset of antimicrobial agents specific to bacteria), biocidal agents (substances or chemicals used for sterilization and disinfection), and biocidal/antimicrobial activity (destruction of or damage to microorganisms at the cellular level). Distinctions can be further drawn according to whether a treatment is applied as a coating, impregnated into the surface, or exists as an inherent material characteristic (further discussed in Part 2).
In scientific terms, “bactericidal” refers to an agent that kills bacteria (>99.9% of an inoculum within 24 hours), while “bacteriostatic” refers to an agent that prevents the growth of bacteria (Pankey & Sabath, 2004). However, it’s worth noting that bactericidal agents usually fail to kill every organism within 24 hours of testing, and most bacteriostatic agents kill some bacteria within the same timeframe (though not enough to be called bactericidal).
Epidemiology of Infections
Healthcare workers, patients, and care partners can be exposed to multiple pathogens throughout the care process (McQueen & Ehnes, 2018; Mitchell et al., 2015; Schettler, 2016). The most common pathogens are shown in Table 1; these pathogens are found to persist in the environment and remain for days or even months (Dancer, 2014; McQueen & Ehnes, 2018; Mitchell et al., 2015; Schettler, 2016). Pathogen characteristics including type, shape, dimensions, structural variation and complexity, and adherence to a surface impact the retention and transfer of infection (Campoccia et al., 2013; Lichter, Van Vliet, & Rubner, 2009).
A fomite is defined as an inanimate object (hard or soft) that can be the vehicle of transmission for an infectious agent. In the hospital, fomites include patient care items and environmental surfaces.
Biofilms (architectural colonies of microorganisms, a prevalent source of infection) result when bacteria attach to static surfaces and self-produce a matrix of extracellular polymeric substance that becomes resistant to antimicrobial agents (Costerton, Stewart, & Greenberg, 1999; Jamal et al., 2018). Disinfectants may only kill the bacteria on the top layer of the biofilm and have little to no effect on the bacteria located deeper within the microcolony (Tripathy, Sen, Su, & Briscoe, 2017). While biofilm investigations have typically focused on wet areas (e.g., faucets, sink drains) and medical devices (e.g., implants), recent research has found that dry surface bacteria are nearly universal on hospital surfaces (Ledwoch et al., 2018; Otter et al., 2015) and can be transferred from hands to fomites, highlighting the biofilm’s role as a persistent environmental source of pathogens (Chowdhury et al., 2018). It has also been suggested that since biofilms on dry hospital surfaces may interfere with traditional environmental sampling, the conditions of environmental surfaces as reservoirs may be underestimated (Yezli & Otter, 2012).
Microbes can be studied under various morphologies, one descriptor being shape (i.e., sphere, rod, or spiral). Verran et al., (2009) found that rod-shaped cells were retained in higher numbers on surfaces with small width features due to alignments of certain shapes with the surface topography. Other characteristics include the composition of the outermost cell envelope (e.g., Gram-positive and Gram-negative bacteria) and the presence of protein fibers that can extend from the cell wall and bond to surfaces. It is necessary to document the structural characteristics of pathogens to understand their mechanisms of existence and survival.
Chain of Contact Transmission
As described in an analysis report of 1,022 published HAI outbreaks, the most common pathogen reservoirs were patients, followed by medical equipment or devices, the environment, and staff members (Gastmeier et al., 2005). Though the transmission of infection (direct or indirect) is most likely to occur through person-to-person contact, air, water, or droplets, the role of fomites in contact transmission should not be ignored (Fijan & Turk, 2012; Yeargin et al., 2016).
Surfaces can be classified as either hard surfaces (e.g., window sills, charting stations and workstations, floors, walls, ceilings) or soft surfaces (e.g., bed linen, upholstery, privacy curtains, apparel). Multiple studies have reported that these surfaces are constantly touched by healthcare workers during patient care, thus becoming potential reservoirs of microbes and spores (CDC, 2003; Cohen et al., 2018; Dancer, 2014; Rutala & Weber, 2013; Sehulster, 2017; Siani & Maillard, 2015; Zimring, 2013). As shown in Figure 2, this indirect chain of transmission might include the organism or agent (i.e., a pathogen), a reservoir (e.g., a surface), objects or materials in and around the patient zone that can carry infection (i.e., fomites), a susceptible host carrier (e.g., a caregiver’s hands), and a susceptible host reservoir (e.g., the patient).
(Steinberg et al., 2013) conceptualized the role of healthcare facility design in breaking the chain of contact transmission through environmental interventions. Solutions include hand hygiene, physical barriers, touchless systems, private rooms, isolation, surface selection, and cleaning strategies. Hand hygiene has been the primary focus of infection prevention efforts; however, the design and selection of built environment surfaces (especially those identified as “high-touch surfaces”) are also important considerations in interrupting the transmission chain. Individual surfaces must be evaluated in the context of affordable and applicable cleaning strategies and technologies.
Several studies showing reduced infection rates have tested built environment and organizational factors such as the number of patients in a room, prior room occupancy, and activity level (Cohen et al., 2018; Datta et al., 2011; Ramos et al., 2015; Stiller et al., 2016; Vaisman et al., 2017). Ambient environmental factors like temperature, relative humidity, air change rate, ventilation, and pressure differentials to adjacent rooms have been found to affect the growth and transmission of microorganisms (Campoccia et al., 2013; Lopez et al., 2013; Ramos et al., 2015; Şimşek et al., 2017; Tang, 2009; Verdier et al., 2014; Yau et al., 2011). Figure 3 shows the range of environmental conditions recommended by ASHRAE 170 in the 2018 FGI Guidelines.
Though there has been no conclusive research, temperatures between 20 and 25°C, humidity under 68%, and 6 to 15 air changes per hour (ACH) have been recommended in the Guidelines for Environmental Infection Control by the CDC and Healthcare Infection Control Practices Advisory Committee (HICPAC) (L. M. Sehulster et al., 2004). Patient comfort and environmental preferences should also be taken into account.
In a study by Lopez et al., (2013), transfer efficiency from fomite-to-finger was determined under low and high relative humidity conditions. Though most organisms had greater transfer efficiencies under high relative humidity, every microorganism reacted differently to different environmental conditions. Variations in pathogen behavior on a range of surfaces relative to temperature and humidity are summarized in Table 2.
Cleaning and Disinfecting Environmental Surfaces
The benefits of cleaning soiled surfaces have been acknowledged for over 150 years (Smith, Watkins, & Hewlett, 2012). Several design factors affecting cleanliness, including room type, configuration, and occupancy, have been discussed in other issue briefs. In addition to the ambient environmental conditions mentioned in the previous section, the design and selection of surfaces, materials, and finishes must be considered in light of organizational policies and cleaning procedures (as summarized in Part 2).
It is counterproductive to specify materials that cannot be effectively maintained. With this in mind, the choice of strategies for cleaning environmental surfaces should be determined by factors such as the nature of the items to be cleaned (i.e., critical, semi-critical, or noncritical surfaces), the amount of microorganisms present, their potential for resistance, the level of disinfection required (i.e., high, intermediate, low), and any limitations or specifications of the available products (Quan, Taylor & Zborowsky, 2015; CDC, 2003). As illustrated in Figure 4, disinfection solutions from the literature have been broadly classified (Rutala & Weber, 2013) into three categories:
- Manual cleaning with disinfectants,
- No-touch automated disinfection technologies, and
- Self-disinfecting surfaces.
Spraying disinfectants (e.g., chlorines, phenols, hypochlorites, quaternary ammonium compounds, accelerated hydrogen peroxide) and wiping surfaces with microfiber/cotton wipes or mops are the first steps of the cleaning process. The concentration of the disinfectant, the choice of applicator, the application process, the ratio of volume to surface area, and the overall contact time can enhance or undermine surface decontamination. In some instances, pathogens can build up on surfaces following cumulative soiling and cleaning cycles (Airey & Verran, 2007). Researchers have observed that after these initial cleaning operations, no viable cells were found on mirror finishes made of steel or copper. However, after repeated soiling/cleaning cycles over the course of five days, cell buildup was observed (more so on the copper surface).
While regular cleaning is necessary to eliminate pathogens and maintain hygiene, it is not the only mechanism available. Several strategies, such as newer cleaning technologies and self-disinfecting materials, have been outlined in Part 2.
Contrary to expectations of cleanliness, studies have shown that less than 50% of hard surfaces are adequately cleaned when chemical germicides are used (Weber & Rutala, 2013). Moreover, studies show that some lesser known high-touch reservoirs of pathogens (e.g., privacy curtains) are not cleaned or sanitized unless visibly soiled (Bloomfield et al., 2015; Kukla, 2013; McQueen & Ehnes, 2018). The cleanliness of high-touch surfaces in healthcare settings has usually been assessed by visual inspection. But when ATP (adenosine triphosphate) bioluminescence and microbiological screenings (e.g., aerobic colony count) were employed, surfaces that seemed clean did not meet benchmark requirements (Mulvey et al., 2011). Malik et al. (2003) found that 90% of tested surfaces did not meet the required standards.
As a result, a systems approach that takes into account the organization, the people, and the environment is required. Table 3 summarizes the systems approach that could improve design to reduce HAIs via contact transmission.
In the United States, chemical sanitizers, disinfectants, and sterilants are regulated by the Antimicrobials Division of the Environmental Protection Agency (EPA). Any substance intended to prevent, destroy, repel, or mitigate microorganism growth (not including those in or on living humans or animals) must be registered (CDC, 2016b). Treated products are defined as “items that are treated with an antimicrobial pesticide to protect the item itself” (EPA, 2015). The treatment (i.e., pesticide) is usually added to the product during or after manufacture, but prior to usage.
Manufacturers of treated products often claim that they protect against harmful microorganisms, placing them in a regulatory category of implied or explicit public health pesticidal claims. There is, however, a “treated articles exemption” that covers substances claiming to protect the article or substance itself, but not those bearing public health claims against human pathogens (EPA, 2014). In Europe, similar regulations and exemptions are included in the EU Biocides Regulation (Health Safety Executive, 2012).
According to the EPA exemption clause, some examples of language requiring registration as a pesticide include:
- Antibacterial, bactericidal, germicidal
- Kills pathogenic bacteria
- Effective against E. coli and Staphylococcus aureus
- Provides a germ/bacteria-resistant surface
- Kills/controls/minimizes the growth of common Gram-positive and Gram-negative bacteria
Furthermore, the EPA has established some protocols for antimicrobial product testing and labeling. These include testing products against biofilms (EPA, 2017) or Clostridium difficile spores on hard, non-porous surfaces (EPA, 2018), as well as evaluating the bactericidal activity of hard, non-porous copper-containing surface products (e.g., door knobs) (EPA, 2016). All of this speaks to the importance of thoroughly researching any product claims before use.
This issue brief has provided an overview of a systems model that can help design teams to understand the epidemiology of infections and their interaction with the healthcare environment. The current and emerging technologies introduced here are discussed in greater depth in Part 2 . If and when changes are made to enhance infection control efforts based on these findings, it is important for design teams to consider the impact of both methods and materials on cleanability and the cleaning process.
Despite research efforts toward improving surface cleanability, as well as guidance from the CDC, EPA, and other government agencies, HAIs continue to be transmitted through fomites in the healthcare environment. There is no single solution to the problem, and no one way to achieve benchmark cleanliness. Every organization must base its design decisions, cleaning procedures, and monitoring methods on the individual environment, organizational values, policies, objectives, and people involved.
For more information, refer to Contact Transmission, Part 2: The Role of Materials, Design, and Cleaning in HAIs.
Airey, P., & Verran, J. (2007). Potential use of copper as a hygienic surface; problems associated with cumulative soiling and cleaning. Journal of Hospital Infection, 67(3), 271–277. https://doi.org/10.1016/j.jhin.2007.09.002
Beggs, C. B., Knibbs, L. D., Johnson, G. R., & Morawska, L. (2015). Environmental contamination and hospital acquired infection: factors that are easily overlooked. Indoor Air, 25(5), 462–474. https://doi.org/10.1111/ina.12170
Bloomfield, S., Exner, M., Flemming, H.-C., Goroncy-Bermes, P., Hartemann, P., Heeg, P., … Trautmann, M. (2015). Lesser-known or hidden reservoirs of infection and implications for adequate prevention strategies: Where to look and what to look for. GMS Hygiene and Infection Control, 10, 1–14.
Boyce, J. M. (2007). Environmental contamination makes an important contribution to hospital infection. Journal of Hospital Infection, 65, 50–54. https://doi.org/10.1016/S0195-6701(07)60015-2
Campoccia, D., Montanaro, L., & Arciola, C. R. (2013). A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials, 34(34), 8533–8554. https://doi.org/10.1016/j.biomaterials.2013.07.089
Carling, P. C. (2016). Optimizing Health Care Environmental Hygiene. Infectious Disease Clinics of North America, 30(3), 639–660. https://doi.org/10.1016/j.idc.2016.04.010
Centers for Disease Control and Prevention. (2016a). National and State Healthcare Associated Infections Progress Report. Retrieved July 9, 2018, from https://www.cdc.gov/hai/surveillance/progress-report/index.html
Centers for Disease Control and Prevention. (2016b). Regulatory Framework - Disinfection & Sterilization Guidelines [Guidelines Library: Infection Control]. Retrieved from CDC website: https://www.cdc.gov/infectioncontrol/guidelines/disinfection/disinfection-methods/regulatory-framework.html
Centers for Disease Control and Prevention. (2018, October 25). HAI Data. Retrieved April 25, 2019, from CDC Healthcare-associated Infections website: https://www.cdc.gov/hai/data/index.html
Chowdhury, D., Tahir, S., Legge, M., Hu, H., Prvan, T., Johani, K., … Vickery, K. (2018). Transfer of dry surface biofilm in the healthcare environment: the role of healthcare workers’ hands as vehicles. Journal of Hospital Infection. https://doi.org/10.1016/j.jhin.2018.06.021
Cohen, B., Liu, J., Cohen, A. R., & Larson, E. (2018). Association between Healthcare-Associated Infection and Exposure to Hospital Roommates and Previous Bed Occupants with the Same Organism. Infection Control & Hospital Epidemiology, in press. https://doi.org/10.1017/ice.2018.22
Costerton, J. W., Stewart, P. S., & Greenberg, E. P. (1999). Bacterial Biofilms: A Common Cause of Persistent Infections. Science, 284(5418), 1318–1322. https://doi.org/10.1126/science.284.5418.1318
Dancer, S. J. (2014). Controlling Hospital-Acquired Infection: Focus on the Role of the Environment and New Technologies for Decontamination. Clinical Microbiology Reviews, 27(4), 665–690. https://doi.org/10.1128/CMR.00020-14
Datta, R., Platt, R., Yokoe, D. S., & Huang, S. S. (2011). Environmental Cleaning Intervention and Risk of Acquiring Multidrug-Resistant Organisms from Prior Room Occupants. Archives of Internal Medicine, 171(6), 491–494. https://doi.org/10.1001/archinternmed.2011.64
Diekema, D. J. (2017). Rising Stakes for Health Care-Associated Infection Prevention: Implications for the Clinical Microbiology Laboratory. Journal of Clinical Microbiology, 55(4), 996–1001. https://doi.org/10.1128/JCM.02544-16
Doidge, M., Allworth, A. M., Woods, M., Marshall, P., Terry, M., O’Brien, K., … Paterson, D. L. (2010). Control of an Outbreak of Carbapenem‐Resistant Acinetobacter baumannii in Australia after Introduction of Environmental Cleaning with a Commercial Oxidizing Disinfectant. Infection Control and Hospital Epidemiology, 31(4), 418–420. https://doi.org/10.1086/651312
Donskey, C. J. (2013). Does improving surface cleaning and disinfection reduce health care-associated infections? American Journal of Infection Control, 41(5, Supplement), S12–S19. https://doi.org/10.1016/j.ajic.2012.12.010
EPA, O. (2014). PRN 2000-1: Applicability of the Treated Articles Exemption to Antimicrobial Pesticides [Policies and Guidance]. Retrieved from US EPA website: https://www.epa.gov/pesticide-registration/prn-2000-1-applicability-treated-articles-exemption-antimicrobial-pesticides
EPA, O. (2015). Consumer Products Treated with Pesticides [Overviews and Factsheets]. Retrieved from US EPA website: https://www.epa.gov/safepestcontrol/consumer-products-treated-pesticides
EPA, O. (2016). Updated Draft Protocol for the Evaluation of Bactericidal Activity of Hard, Non-porous Copper Containing Surface Products [Policies and Guidance]. Retrieved from US EPA website: https://www.epa.gov/pesticide-registration/updated-draft-protocol-evaluation-bactericidal-activity-hard-non-porous
EPA, O. (2017). Methods and Guidance for Testing the Efficacy of Antimicrobial Products Against Biofilms on Hard, Non-Porous Surfaces [Policies and Guidance]. Retrieved from US EPA website: https://www.epa.gov/pesticide-analytical-methods/methods-and-guidance-testing-efficacy-antimicrobial-products-against
EPA, O. (2018). Methods and Guidance for Testing the Efficacy of Antimicrobial Products Against Spores of Clostridium difficile on Hard Non-Porous Surfaces (February 2018) [Policies and Guidance]. Retrieved from US EPA website: https://www.epa.gov/pesticide-registration/methods-and-guidance-testing-efficacy-antimicrobial-products-against-spores
Fijan, S., & Turk, S. Š. (2012). Hospital Textiles, Are They a Possible Vehicle for Healthcare-Associated Infections? International Journal of Environmental Research and Public Health, 9(9), 3330–3343. https://doi.org/10.3390/ijerph9093330
Gastmeier, P., Stamm-Balderjahn, S., Hansen, S., Nitzschke-Tiemann, F., Zuschneid, I., Groneberg, K., & Rüden, H. (2005). How Outbreaks Can Contribute to Prevention of Nosocomial Infection: Analysis of 1,022 Outbreaks. Infection Control & Hospital Epidemiology, 26(04), 357–361. https://doi.org/10.1086/502552
Grabsch, E. A., Burrell, L. J., Padiglione, A., O’Keeffe, J. M., Ballard, S., & Grayson, M. L. (2006). Risk of environmental and healthcare worker contamination with vancomycin-resistant enterococci during outpatient procedures and hemodialysis. Infection Control and Hospital Epidemiology, 27(3), 287–293. https://doi.org/10.1086/503174
Health Safety Executive. (2012). The EU Biocides Regulation 528/2012 (EU BPR). Retrieved from http://www.hse.gov.uk/biocides/eu-bpr/index.htm
Jamal, M., Ahmad, W., Andleeb, S., Jalil, F., Imran, M., Nawaz, M. A., … Kamil, M. A. (2018). Bacterial biofilm and associated infections. Journal of the Chinese Medical Association: JCMA, 81(1), 7–11. https://doi.org/10.1016/j.jcma.2017.07.012
Kotsanas, D., Wijesooriya, W. R. P. L. I., Korman, T. M., Gillespie, E. E., Wright, L., Snook, K., … Stuart, R. L. (2013). “Down the drain”: carbapenem-resistant bacteria in intensive care unit patients and handwashing sinks. The Medical Journal of Australia, 198(5), 267–269. https://doi.org/10.5694/mja12.11757
Kukla, C. (2013). A New Frontier: The Dangers of Pathogens on Soft Surfaces. Infection Control Today. Retrieved from https://www.infectioncontroltoday.com/environmental-hygiene/new-frontier-dangers-pathogens-soft-surfaces
Ledwoch, K., Dancer, S. J., Otter, J. A., Kerr, K., Roposte, D., Rushton, L., … Maillard, J.-Y. (2018). Beware biofilm! Dry biofilms containing bacterial pathogens on multiple healthcare surfaces; a multi-centre study. Journal of Hospital Infection. https://doi.org/10.1016/j.jhin.2018.06.028
Lichter, J. A., Van Vliet, K. J., & Rubner, M. F. (2009). Design of Antibacterial Surfaces and Interfaces: Polyelectrolyte Multilayers as a Multifunctional Platform. Macromolecules, 42(22), 8573–8586. https://doi.org/10.1021/ma901356s
Loo, V. G. (2015). Environmental Interventions to Control Clostridium difficile. Infectious Disease Clinics of North America, 29(1), 83–91. https://doi.org/10.1016/j.idc.2014.11.006
Lopez, G. U., Gerba, C. P., Tamimi, A. H., Kitajima, M., Maxwell, S. L., & Rose, J. B. (2013). Transfer Efficiency of Bacteria and Viruses from Porous and Nonporous Fomites to Fingers under Different Relative Humidity Conditions. Applied and Environmental Microbiology, 79(18), 5728–5734. https://doi.org/10.1128/AEM.01030-13
Magill, S. S., Edwards, J. R., Bamberg, W., Beldavs, Z. G., Dumyati, G., Kainer, M. A., … Emerging Infections Program Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team. (2014). Multistate point-prevalence survey of health care-associated infections. The New England Journal of Medicine, 370(13), 1198–1208. https://doi.org/10.1056/NEJMoa1306801
Malik, R. E., Cooper, R. A., & Griffith, C. J. (2003). Use of audit tools to evaluate the efficacy of cleaning systems in hospitals. American Journal of Infection Control, 31(3), 181–187. https://doi.org/10.1067/mic.2003.34
McQueen, R. H., & Ehnes, B. L. (2018). Antimicrobial textiles and infection prevention - Clothes and inanimate environment. In G. Bearman, S. Munoz-Price, D. Morgan, & R. Murthy (Eds.), New Perspectives and Controversies in Infection Prevention (p. in press). Springer International Publishing.
Michels, H. T., Noyce, J. O., & Keevil, C. W. (2009). Effects of temperature and humidity on the efficacy of methicillin-resistant Staphylococcus aureus challenged antimicrobial materials containing silver and copper. Letters in Applied Microbiology, 49(2), 191–195. https://doi.org/10.1111/j.1472-765X.2009.02637.x
Mitchell, A., Spencer, M., & Edmiston, C. (2015). Role of healthcare apparel and other healthcare textiles in the transmission of pathogens: a review of the literature. Journal of Hospital Infection, 90(4), 285–292. https://doi.org/10.1016/j.jhin.2015.02.017
Moehring, R. W., & Anderson, D. J. (2012). Antimicrobial Stewardship as Part of the Infection Prevention Effort. Current Infectious Disease Reports, 14(6), 592–600. https://doi.org/10.1007/s11908-012-0289-x
Mulvey, D., Redding, P., Robertson, C., Woodall, C., Kingsmore, P., Bedwell, D., & Dancer, S. J. (2011). Finding a benchmark for monitoring hospital cleanliness. Journal of Hospital Infection, 77(1), 25–30. https://doi.org/10.1016/j.jhin.2010.08.006
Otter, J. A., Vickery, K., Walker, J. T., deLancey Pulcini, E., Stoodley, P., Goldenberg, S. D., … Edgeworth, J. D. (2015). Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection. Journal of Hospital Infection, 89(1), 16–27. https://doi.org/10.1016/j.jhin.2014.09.008
Otter, J. A., Yezli, S., & French, G. L. (2014). The Role of Contaminated Surfaces in the Transmission of Nosocomial Pathogens. In Use of Biocidal Surfaces for Reduction of Healthcare Acquired Infections (pp. 27–58). https://doi.org/10.1007/978-3-319-08057-4_3
Pankey, G. A., & Sabath, L. D. (2004). Clinical Relevance of Bacteriostatic versus Bactericidal Mechanisms of Action in the Treatment of Gram-Positive Bacterial Infections. Clinical Infectious Diseases, 38(6), 864–870. https://doi.org/10.1086/381972
Ramos, T., Dedesko, S., Siegel, J. A., Gilbert, J. A., & Stephens, B. (2015). Spatial and Temporal Variations in Indoor Environmental Conditions, Human Occupancy, and Operational Characteristics in a New Hospital Building. PLoS ONE, 10(3), e0118207. https://doi.org/10.1371/journal.pone.0118207
Rutala, W. A., & Weber, D. J. (2013). Disinfectants used for environmental disinfection and new room decontamination technology. American Journal of Infection Control, 41(5), S36–S41. https://doi.org/10.1016/j.ajic.2012.11.006
Sandora, T. J., & Goldmann, D. A. (2012). Preventing Lethal Hospital Outbreaks of Antibiotic-Resistant Bacteria. New England Journal of Medicine, 367(23), 2168–2170. https://doi.org/10.1056/NEJMp1212370
Schettler, T. (2016). Antimicrobials in Hospital Furnishings: Do They Help Reduce Healthcare-Associated Infections? Retrieved from Health Care Without Harm website: https://noharm-uscanada.org/sites/default/files/documents-files/3854/Antimicrobials%20Report%202016_1.pdf
Schmier, J. K., Hulme-Lowe, C. K., Semenova, S., Klenk, J. A., DeLeo, P. C., Sedlak, R., & Carlson, P. A. (2016). Estimated hospital costs associated with preventable health care-associated infections if health care antiseptic products were unavailable. ClinicoEconomics and Outcomes Research: CEOR, 8, 197–205. https://doi.org/10.2147/CEOR.S102505
Sehulster, L. M., Chinn, R. Y. W., Arduino, M. J., Carpenter, J., Donlan, R., Besser, R., … Cleveland, J. (2004). Guidelines for environmental infection control in health-care facilities. Recommendations from CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). Retrieved from American Society for Healthcare Engineering/American Hospital Association website: http://www.cdc.gov/hicpac/pdf/guidelines/eic_in_hcf_03.pdf
Sehulster, Lynne M. (2017, October 6). Diligence in Infection Prevention is Key to Maintaining the Quality of Laundered Healthcare Textiles. Infection Control Today. Retrieved from https://www.infectioncontroltoday.com/laundry/diligence-infection-prevention-key-maintaining-quality-laundered-healthcare-textiles
Siani, H., & Maillard, J. -y. (2015). Best practice in healthcare environment decontamination. European Journal of Clinical Microbiology and Infectious Diseases; Heidelberg, 34(1), 1–11. http://dx.doi.org/10.1007/s10096-014-2205-9
Siegel, J. D., Rhinehart, E., Jackson, M., & Chiarello, L. (2007). Management of multidrug-resistant organisms in health care settings, 2006. American Journal of Infection Control, 35(10, Supplement 2), S165–S193. https://doi.org/10.1016/j.ajic.2007.10.006
Şimşek, E. M., Grassie, S. S., Emre, C., & Gevrek, S. Ç. (2017). Relationship between Environmental Conditions and Nosocomial Infection Rates in Intensive Care Unit. Medical Journal of Islamic World Academy of Sciences, 25(1), 15–18. https://doi.org/10.5505/ias.2017.66742
Smith, P. W., Watkins, K., & Hewlett, A. (2012). Infection control through the ages. American Journal of Infection Control, 40(1), 35–42. https://doi.org/10.1016/j.ajic.2011.02.019
Steinberg, J. P., Denham, M. E., Zimring, C., Kasali, A., Hall, K. K., & Jacob, J. T. (2013). The Role of the Hospital Environment in the Prevention of Healthcare-Associated Infections by Contact Transmission. HERD: Health Environments Research & Design Journal, 7(1_suppl), 46–73. https://doi.org/10.1177/193758671300701S06
Stiller, A., Schröder, C., Gropmann, A., Schwab, F., Behnke, M., Geffers, C., … Gastmeier, P. (2016). ICU ward design and nosocomial infection rates – a cross sectional study in Germany. Journal of Hospital Infection, 95(1), 71–75. https://doi.org/10.1016/j.jhin.2016.10.011
Tang, J. W. (2009). The effect of environmental parameters on the survival of airborne infectious agents. Journal of The Royal Society Interface, rsif20090227. https://doi.org/10.1098/rsif.2009.0227.focus
Tripathy, A., Sen, P., Su, B., & Briscoe, W. H. (2017). Natural and bioinspired nanostructured bactericidal surfaces. Advances in Colloid and Interface Science, 248, 85–104. https://doi.org/10.1016/j.cis.2017.07.030
Vaisman, A., Jula, M., Wagner, J., & Winston, L. G. (2017). Association between Hospital-Onset Clostridium difficile infection and Admission to a Multi-Bed Room: A Case–control Study. Open Forum Infectious Diseases, 4(Suppl 1), S400. https://doi.org/10.1093/ofid/ofx163.1000
Verdier, T., Coutand, M., Bertron, A., & Roques, C. (2014). A review of indoor microbial growth across building materials and sampling and analysis methods. Building and Environment, 80, 136–149. https://doi.org/10.1016/j.buildenv.2014.05.030
Verran, J., Packer, A., Kelly, P., & Whitehead, K. A. (2009). The retention of bacteria on hygienic surfaces presenting scratches of microbial dimensions. Letters in Applied Microbiology, 50(3), 258–263. https://doi.org/10.1111/j.1472-765X.2009.02784.x
Weber, D. J., Anderson, D., & Rutala, W. A. (2013). The role of the surface environment in healthcare-associated infections: Current Opinion in Infectious Diseases, 26(4), 338–344. https://doi.org/10.1097/QCO.0b013e3283630f04
Weber, D. J., & Rutala, W. A. (2013). Self-disinfecting surfaces: Review of current methodologies and future prospects. American Journal of Infection Control, 41(5, Supplement), S31–S35. https://doi.org/10.1016/j.ajic.2012.12.005
Yau, Y. H., Chandrasegaran, D., & Badarudin, A. (2011). The ventilation of multiple-bed hospital wards in the tropics: A review. Building and Environment, 46(5), 1125–1132. https://doi.org/10.1016/j.buildenv.2010.11.013
Yeargin, T., Buckley, D., Fraser, A., & Jiang, X. (2016). The survival and inactivation of enteric viruses on soft surfaces: A systematic review of the literature. American Journal of Infection Control, 44(11), 1365–1373. https://doi.org/10.1016/j.ajic.2016.03.018
Yezli, S., & Otter, J. A. (2012). Does the discovery of biofilms on dry hospital environmental surfaces change the way we think about hospital disinfection? Journal of Hospital Infection, 81(4), 293–294. https://doi.org/10.1016/j.jhin.2012.05.012
Zimring, C., Denham, M. E., Jacob, J. T., Kamerow, D. B., Lenfestey, N., Hall, K. K., … Steinberg, J. P. (2013). The Role of Facility Design in Preventing Healthcare-Associated Infection: Interventions, Conclusions, and Research Needs. HERD: Health Environments Research & Design Journal, 7(1_suppl), 127–139. https://doi.org/10.1177/193758671300701S09