Environmental Hygiene: What We Know from Scientific Studies

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Editor's note: ICT offers related resources. A special digital issue, "Pathogen Persistence, Transmission and Cross-Contamination Prevention" is available for download. For the accompanying slide show, CLICK HERE.  

By Kelly M. Pyrek

A renewed interest in the healthcare environment and to what degree surface contamination contributes to the spread of infectious pathogens is driving a growing body of research in this area. Let's take a look at what we know about various aspects of environmental hygiene from the scientific literature:

- Hand hygiene alone isn't enough
Dancer (2010) makes a compelling case for not allowing a dependence on hand hygiene to eclipse the need for rigorous environmental cleaning coupled with other key infection prevention-related interventions: "With the predominant focus on clean hands, there is less interest in the surfaces that they touch. Even exceptional hand hygiene is rendered invalid if the first object handled transfers pathogens to the patient via fingertips ... Infection control requires a multimodal focus encompassing a wide range of strategies. Each of these interventions plays an integral role in an overall hygiene program, which implies that all deserve consideration and resourcing. To single out hand hygiene while the wards remain grubby, antibiotic prescribing continues unabated, or hospitals overflow with patients will confound any possible benefits from clean hand programs. In addition, penalizing staff over perceived hand hygiene practices will foster resentment and disenchantment. People either will or will not clean their hands, whatever policies are imposed upon them, whereas cleaning, antimicrobial prescribing, laboratory protocol, screening, isolation, and bed management are not subject to human whim and theoretically could be strengthened by clinicians and managers." Dancer adds, "We should balance the current focus on hand hygiene by prioritizing additional strategies. All deserve more support and investment, because none has received the attention that so far has been given to hand hygiene. Because people will not—or cannot—always clean their hands, let us engage managerial support for space, time, isolation capacity, staffing, and sufficient cleaning of all hand‐touch surfaces."

- Microorganisms collect on hospital environment surfaces and are spread
In the past, experts believed that the most significant source of hospital-acquired pathogens was the patient's own endogenous flora; however, Weber, et al. (2010) point out that an estimated 20 percent to 40 percent of nosocomial infections have been attributed to cross-infection via the hands of healthcare workers. They add that this hand contamination could in turn result from either direct patient contact or indirectly from touching contaminated environmental surfaces. They also acknowledge that less commonly, a patient could become colonized with a nosocomial pathogen by direct contact with a contaminated environmental surface -- they say that in some cases, the extent of patient-to-patient transmission has been found to be directly proportional to the level of environmental contamination.

- Pathogens persist on environmental surfaces
Kramer, et al. (2006) summarize data on the persistence of different nosocomial pathogens on inanimate surfaces. The researchers found that most Gram-positive bacteria, such as Enterococcus spp. (including VRE), Staphylococcus aureus (including MRSA), or Streptococcus pyogenes, survive for months on dry surfaces, while many Gram-negative species, such as Acinetobacter spp., Escherichia coli, Klebsiella spp., Pseudomonas aeruginosa, Serratia marcescens, or Shigella spp., can also survive for months. Most viruses from the respiratory tract, such as corona, coxsackie, influenza, SARS or rhinovirus, can persist on surfaces for a few days; viruses from the gastrointestinal tract, such as astrovirus, HAV, poliovirus or rotavirus, persist for approximately two months; and bloodborne viruses, such as HBV or HIV, can persist for more than one week. Their review emphasizes that the most common nosocomial pathogens may be a continuous source of transmission if no regular preventive surface disinfection is performed.

- Acquisition of specific organisms is impacted by environmental cleaning
Wilson, et al. (2006) found that enhanced cleaning reduced environmental contamination and hand carriage, but no significant effect was observed on patient acquisition of methicillin-resistant Staphylococcus aureus. Hayden, et al. (2006) found that decreasing environmental contamination may help to control the spread of some antibiotic-resistant bacteria in hospitals, specifically vancomycin-resistant enterococci (VRE).


Mamoon, et al. (2009) demonstrated that higher-level cleaning can be effective in removing MRSA from a range of environmental sites that are high risk of patient and/or healthcare worker hand contact in critical areas, such as ICUs. However, in the absence of any residual cleaning and/or disinfectant effects, the clear beneficial effects of such decontamination interventions are transient and rapidly negated by subsequent failures in infection control practice. These findings highlight the need for further work on detergent and disinfectant materials that have long‐lasting biocidal effects.

- Environmental contamination might lead to infection
Weber, et al. (2010) say that in order for environmental contamination to play an important role in the acquisition of a nosocomial pathogen, the pathogen must demonstrate certain microbiologic characteristics: pathogen able to survive for prolonged periods of time on environmental surfaces; ability to remain virulent after environmental exposure; contamination of the hospital environment frequent; ability to colonize patients (Acinetobacter, C difficile, MRSA, VRE); ability to transiently colonize the hands of healthcare workers; transmission via the contaminated hands of healthcare workers; small inoculating dose (C difficile, norovirus); and relative resistance to disinfectants used on environmental surfaces (C difficile, norovirus).
 
- Prior-room occupants can impact acquisition of pathogens
Otter, et al. (2011) point out that, "A number of studies have identified the previous presence of a colonized or infected patient in a side room as a risk factor for the acquisition of the same pathogen by a new occupant, presumably because of residual room contamination that is not removed through terminal cleaning and disinfection. This effect has been shown for VRE, MRSA, C. difficile, multidrug-resistant P. aeruginosa and A. baumannii."

Datta, et al. (2011) say that enhanced intensive care unit cleaning using the intervention methods (cleaning cloths saturated with disinfectant via bucket immersion, targeted feedback using a black-light marker, and increased education) may reduce MRSA and VRE transmission. It may also eliminate the risk of MRSA acquisition due to an MRSA-positive prior room occupant.

Shaughnessy, et al. (2011) determined that  prior room occupant with CDI is a significant risk factor for CDI acquisition, independent of established CDI risk factors.

Nseir, et al. (2011) concluded that admission to an ICU room previously occupied by a patient with MDR P. aeruginosa or A. baumannii is an independent risk factor for acquisition of these bacteria by subsequent room occupants; this relationship was not identified for ESBL-producing GNB.

Carling and Bartley (2010) demonstrated that admission of a patient into a bed previously occupied by an infected patient significantly increases the chance of acquiring the same pathogen, regardless of compliance with hand hygiene. And as Dancer (2010) notes, "Newly cleaned hands touching contaminated environmental sites consistently undermine hand hygiene success."

Drees, et al. (2008) found that patients colonized with vancomycin-resistant enterococci (VRE) frequently contaminate their environment, and that prior room contamination, whether measured via environmental cultures or prior room occupancy by VRE-colonized patients, was highly predictive of VRE acquisition.

Huang, et al. (2006) asserted that admission to a room previously occupied by an MRSA-positive patient or a VRE-positive patient significantly increased the odds of acquisition for MRSA and VRE. However, this route of transmission was a minor contributor to overall transmission. They noted that the effect of current cleaning practices in reducing the risk to the observed levels and the potential for further reduction were unknown.

- Cleaning is essential
Dancer (2009) issued a clarion call when she observed that until cleaning becomes an evidence-based science, with established methods for assessment, the importance of a clean environment is likely to remain speculative. In her review, she examined the links between the hospital environment and persistent pathogens, noted their vulnerability to the cleaning and disinfection process, and established the potential for impact on patient infection rates when high-touch surfaces were addressed. She also suggested that using proposed standards for hospital hygiene could provide further evidence that cleaning is a cost-effective intervention for controlling healthcare-associated infection.

Weber, et al. (2010) emphasize that the role of surface contamination in transmission of healthcare-associated pathogens is an important issue because transmission can be interrupted by appropriate hand hygiene and cleaning/disinfection of environmental surfaces.


Otter, et al. (2011) remind us that "cleaning is the removal of soil and contaminants from surfaces, whereas disinfection relates to the inactivation of pathogens by use of a disinfectant" and that "Microorganisms vary in their resistance to disinfectants, so agents must be chosen carefully for their effectiveness, particularly for C. difficile spores. Furthermore, the hospital environment is complex and often difficult to clean, and use of a cleaning agent that is not effective against the target organism can spread pathogens to other surfaces." The researchers also note, "Cleaning and disinfection does not always eradicate pathogens from surfaces" and that "…it is difficult to determine whether it is the products, the procedures, or a combination of the two that is responsible for the failure to eradicate pathogens from surfaces."

- Cleaning practices vary and can be subpar
Dancer (2011) suggests that "cleaning practices should be tailored to clinical risk, given the wide-ranging surfaces, equipment and building design. There is confusion between nursing and domestic personnel over the allocation of cleaning responsibilities and neither may receive sufficient training and/or time to complete their duties. Since less laborious practices for dirt removal are always attractive, there is a danger that traditional cleaning methods are forgotten or ignored."


Boyce, et al. (2010) acknowledge that substantial variations can be found in the amount of time spent cleaning high‐touch surfaces, in the number of disinfectant wipes used in each room, and in the level of cleanliness achieved by housekeepers. They concluded that a number of variables need to be considered when assessing hospital cleaning practices and that providing housekeepers with continuing education and feedback is necessary to achieve compliance with recommended daily cleaning practices. Further studies using ATP bioluminescence assays for monitoring hospital cleanliness are warranted.

Carling, et al. (2010) report that nine studies of thoroughness of cleaning and disinfection which included more than 62,500 high-touch surfaces in 103 different institutions and 142 study sites identified opportunities for improved cleaning in all venues, documenting that cleaning and disinfection must be improved across a broad range of U.S. healthcare settings as part of efforts to prevent transmission of pathogens. 

Hota, et al. (2009) conducted a trial in which a multifaceted environmental cleaning improvement intervention was introduced (the intervention included educational lectures for housekeepers and an observational program of their activities without changes in cleaning products or written procedures). They suggested that surface contamination with VRE is due to a failure to clean rather than to a faulty cleaning procedure or product.

Carling, et al. (2008) identified significant opportunities in all participating hospitals to improve the cleaning of frequently touched objects in the patient's immediate environment. The overall thoroughness of terminal cleaning, expressed as a percentage of surfaces evaluated, was 49 percent (the range for all 23 hospitals in the study was 35 percent to 81 percent). There was significant variation in cleaning efficacy with respect to the cleaning of toilet handholds, bedpan cleaners, light switches, and door knobs (mean cleaning rates less than 30 percent);  sinks, toilet seats, and tray tables were consistently relatively well cleaned (mean cleaning rates over 75 percent). Patient telephones, nurse call devices, and bedside rails were inconsistently cleaned.

- Cleaning efficacy must be monitored and improved
Otter, et al. (2011) say that while there is some evidence that focused efforts can improve the efficacy of cleaning, including improved monitoring of cleaning, routine quantitative microbiological culture, and educational interventions, the long-term effect of educational cleaning improvements has not yet been evaluated fully.

Guh and Carling (2010) encourage hospitals to develop programs to optimize the thoroughness of high-touch surface cleaning as part of terminal room cleaning at the time of discharge or transfer of patients. The program should be based on the institution's level of dedicated resources to implement objective monitoring programs. The program will be an infection preventionist/hospital epidemiologist infection prevention and control (IPC)-based program internally coordinated and maintained through environmental services (EVS) management level participation. The program should be based on a joint (IC/EVS) definition of institutional expectations consistent with CDC standards and a terminal room cleaning checklist. The responsibilities of ES staff and other hospital personnel for cleaning high-touch surfaces (e.g., equipment in ICU rooms) should be clearly defined. Structured education of the EVS staff should be undertaken to define, carry out and monitor programmatic and institutional expectations. Monitoring measures will be undertaken by the IPC/ES team and may include competency evaluation of EVS staff by EVS management, IPC staff or both. Regular ongoing structured monitoring of the program will be performed and documented.  Interventions to optimize the thoroughness of terminal room cleaning and disinfection will be a standing agenda item for the Infection Control Committee (ICC) or Quality Committee as appropriate for the facility. In a more advanced program, Guh and Carling (2010) advocate for an objective assessment of terminal room thoroughness of surface disinfection cleaning done using one or more of the methods recommended by the CDC to document the pre-intervention thoroughness of disinfection cleaning. They also advise scheduled ongoing monitoring of the  cleaning at least three times a year. The results should be used in ongoing educational activity and feedback to EVS staff following each cycle of evaluation. Results of the objective monitoring program and interventions to optimize the thoroughness of terminal room cleaning and disinfection should be a standing agenda item for the ICC.

Guh and Carling (2010) also review the various methods that can be employed to evaluate environmental cleaning: direct practice observation; swab cultures; agar slide cultures; fluorescent markers; and ATP bioluminesence.

Dolan, et al. (2011) caution that recovery of bacteria from environmental samples varies with the swabs and methodology used and negative culture results do not exclude a pathogen-free environment. Both Dolan, et al. (2011) and Hedin, et al. (2010) call for greater standardization to facilitate the assessment of cleanliness of healthcare environments.


Munoz-Price, et al. (2012) compared cleaning rates associated with use of a white ultraviolet (UV) powder versus a transparent UV gel among units with various degrees of previous experience with UV powder. They found discordant cleaning (removal of powder without the removal of gel, or vice versa) and higher frequency of discordance in high-experience units (31 percent) than in no-experience units (8 percent).  In 92 percent of discordant findings, the powder was removed but not the gel, suggesting preferential cleaning of visible UV targets among units with high levels of previous experience with powder.

Sitzlar, et al. (2011) report that removal of DAZO (part of a fluorescent targeting method) correlated well with removal of bacteria or C. difficile spores from the site of marker placement, but did not ensure that other high-touch sites on the same surfaces were cleaned. 

 
Moore, et al. (2010) urge caution when assessing cleaning programs while using adenosine triphosphate (ATP) bioluminescence, and to consider if surfaces sampled could also be considered adequately clean prior to them being cleaned by EVS staff. Use of benchmark values can help continually monitor the efficacy of existing cleaning programs; however, when evaluating novel or new cleaning practices, baseline cleanliness (the level of cleanliness routinely achieved using normal cleaning procedures) must also be taken into consideration, or the efficacy of modified cleaning will be overestimated.

Boyce, et al. (2011) note that fluorescent markers are useful in determining how frequently high-touch surfaces are wiped during terminal cleaning. However, contaminated surfaces classified as clean according to fluorescent marker criteria after terminal cleaning were significantly less likely to be classified as clean according to ACC and ATP assays.

- Disinfectant contact/dwell times are problematic
Rutala and Weber (2008) note, "An important issue concerning use of disinfectants for noncritical surfaces in health-care settings is that the contact time specified on the label of the product is often too long to be practically followed. The labels of most products registered by EPA for use against HBV, HIV, or M. tuberculosis specify a contact time of 10 minutes. Such a long contact time is not practical for disinfection of environmental surfaces in a healthcare setting because most healthcare facilities apply a disinfectant and allow it to dry (~1 minute). Multiple scientific papers have demonstrated significant microbial reduction with contact times of 30 to 60 seconds.  In addition, EPA will approve a shortened contact time for any product for which the manufacturers will submit confirmatory efficacy data. Currently, some EPA-registered disinfectants have contact times of one to three minutes. By law, users must follow all applicable label instructions for EPA-registered products. Ideally, product users should consider and use products that have the shortened contact time. However, disinfectant manufacturers also need to obtain EPA approval for shortened contact times so these products will be used correctly and effectively in the healthcare environment."


Rutala (undated) addresses how healthcare workers should interpret the recommendation about contact time for disinfectants used on noncritical items in terms of a disconnect between the label instructions and what the studies show: "In order 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.' There are several points that should be made about this apparent disconnect between label instructions and what studies show to include:
- multiple scientific studies have demonstrated the efficacy of hospital disinfectants against pathogens causing healthcare-associated infections with a contact time of at least 1 minute
- the only way an institution can achieve a contact time of 10 minutes is to reapply the surface disinfectant 5-6 times to the surface as the typical dry time for a water-based disinfectant is 1.5-2 minutes and currently, healthcare facilities like UNC Health Care are achieving surface disinfection of non-critical patient care items and environmental surfaces by one application of a disinfectant and requiring a >1 minute dry time
- equally important as disinfectant contact time is the application of the disinfectant to the surface or equipment to ensure that all contaminated surfaces and non-critical patient care equipment are wiped as current studies demonstrate that only approximately 50 percent of high-risk objects are cleaned at terminal cleaning
- there are no data that demonstrate improved infection prevention by a 10 minute contact time versus a 1-minute contact time; we are not aware of an enforcement action against healthcare facilities for "off label" use of a surface disinfectant

 
Thus, Rutala (undated) says, "We believe the guideline allows us to continue our use of low-level disinfectants for noncritical environmental surfaces and patient care equipment with a 1 minute contact time. Additionally, all healthcare facilities should reemphasize the thoroughness of cleaning to ensure that all contaminated surfaces are wiped."

- Wipes are efficient, but must be used according to manufacturer instructions
Orenstein, et al. (2011) evaluated daily cleaning with germicidal bleach wipes on wards with a high incidence of hospital-acquired Clostridium difficile infection (CDI). The intervention reduced hospital-acquired CDI incidence by 85 percent, from 24.2 to 3.6 cases per 10,000 patient-days, and prolonged the median time between hospital-acquired CDI cases from 8 to 80 days.

Carter, et al. (2011) found that the introduction of sporicidal wipes resulted in a significant reduction in C difficile rates, thus supporting the need to review and enhance traditional environmental cleaning regimens for preventing and controlling C difficile in acute settings.

Cheng, et al. (2011) assessed the effectiveness of disinfection in clinical areas by assessment of the wipe-rinse method to MRSA in the immediate patient environment, on both the bed rails and the cleaning wipes. The presence of MRSA in the proximity of the patient, i.e., the bed rails as well as the cleaning tool (the wipe), was demonstrated. If thorough rinsing was not conducted between wiping, bacteria accumulated on the wipes, which can result in cross transmission.

Siani, et al. (2011) tested wipes for sporicidal efficacy using a three-stage protocol that measures the ability of the wipe to remove microbial bioburden from a surface, the potential for microbial transfer from the wipe to other surfaces, and the sporicidal activity of the wipe. The ability of the sporicidal wipes to remove C difficile spores from an inanimate surface ranged from 0.22 to 4.09 log(10) spores removed within 10 seconds. None of the wipes demonstrated high sporicidal activity (>4 log(10) reduction) within 5 minutes of contact time, except for a control wipe soaked in 5,000-ppm sodium hypochlorite. All but one wipe demonstrated that spores could be repeatedly transferred to other surfaces. They say that although the use of sporicidal wipes might offer additional control of microbial burden on surfaces, current efficacy tests might be inadequate to reflect the activity of these wipes in practice, lleading to the use of wipes that might not be appropriate for applications in the healthcare environment.

Williams, et al. (2009) examined the efficacy of two commercially available wipes to effectively remove, kill and prevent the transfer of both methicillin‐resistant and methicillin‐susceptible Staphylococcus aureus from contaminated surfaces, noting that although wipes play a role in decreasing the number of pathogenic bacteria from contaminated surfaces, they can potentially transfer bacteria to other surfaces if they are reused. They recommended that a wipe not be used on more than one surface, that it be used only on a small area, and that it be discarded immediately after use, to reduce the risk of microbial spread.

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